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Journal articles on the topic 'Mechanostimulation'

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Author: Grafiati

Published: 10 December 2022

Last updated: 28 January 2023

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1

Govoni, Marco, Claudio Muscari, Carlo Guarnieri, and Emanuele Giordano. "Mechanostimulation Protocols for Cardiac Tissue Engineering." BioMed Research International 2013 (2013): 1–10. http://dx.doi.org/10.1155/2013/918640.

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Owing to the inability of self-replacement by a damaged myocardium, alternative strategies to heart transplantation have been explored within the last decades and cardiac tissue engineering/regenerative medicine is among the present challenges in biomedical research. Hopefully, several studies witness the constant extension of the toolbox available to engineer a fully functional, contractile, and robust cardiac tissue using different combinations of cells, template bioscaffolds, and biophysical stimuli obtained by the use of specific bioreactors. Mechanical forces influence the growth and shape of every tissue in our body generating changes in intracellular biochemistry and gene expression. That is why bioreactors play a central role in the task of regenerating a complex tissue such as the myocardium. In the last fifteen years a large number of dynamic culture devices have been developed and many results have been collected. The aim of this brief review is to resume in a single streamlined paper the state of the art in this field.

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2

Kadem, Laith F., K. Grace Suana, Michelle Holz, Wei Wang, Hannes Westerhaus, Rainer Herges, and Christine Selhuber-Unkel. "High-Frequency Mechanostimulation of Cell Adhesion." Angewandte Chemie International Edition 56, no. 1 (November 30, 2016): 225–29. http://dx.doi.org/10.1002/anie.201609483.

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3

Kadem, Laith F., K. Grace Suana, Michelle Holz, Wei Wang, Hannes Westerhaus, Rainer Herges, and Christine Selhuber-Unkel. "High-Frequency Mechanostimulation of Cell Adhesion." Angewandte Chemie 129, no. 1 (November 30, 2016): 231–35. http://dx.doi.org/10.1002/ange.201609483.

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4

Ghosh, Ritesh, Adelin Barbacci, and Nathalie Leblanc-Fournier. "Mechanostimulation: a promising alternative for sustainable agriculture practices." Journal of Experimental Botany 72, no. 8 (January 29, 2021): 2877–88. http://dx.doi.org/10.1093/jxb/erab036.

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Abstract Plants memorize events associated with environmental fluctuations. The integration of environmental signals into molecular memory allows plants to cope with future stressors more efficiently—a phenomenon that is known as ‘priming’. Primed plants are more resilient to environmental stresses than non-primed plants, as they are capable of triggering more robust and faster defence responses. Interestingly, exposure to various forms of mechanical stimuli (e.g. touch, wind, or sound vibration) enhances plants’ basal defence responses and stress tolerance. Thus, mechanostimulation appears to be a potential priming method and a promising alternative to chemical-based priming for sustainable agriculture. According to the currently available method, mechanical treatment needs to be repeated over a month to alter plant growth and defence responses. Such a long treatment protocol restricts its applicability to fast-growing crops. To optimize the protocol for a broad range of crops, we need to understand the molecular mechanisms behind plant mechanoresponses, which are complex and depend on the frequency, intervals, and duration of the mechanical treatment. In this review, we synthesize the molecular underpinnings of plant mechanoperception and signal transduction to gain a mechanistic understanding of the process of mechanostimulated priming.

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Hernandez, Marylens, Julia Patzig, Sonia R. Mayoral, Kevin D. Costa, Jonah R. Chan, and Patrizia Casaccia. "Mechanostimulation Promotes Nuclear and Epigenetic Changes in Oligodendrocytes." Journal of Neuroscience 36, no. 3 (January 20, 2016): 806–13. http://dx.doi.org/10.1523/jneurosci.2873-15.2016.

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6

Osborn, Eric A., Aleksandr Rabodzey, C. Forbes Dewey, and John H. Hartwig. "Endothelial actin cytoskeleton remodeling during mechanostimulation with fluid shear stress." American Journal of Physiology-Cell Physiology 290, no. 2 (February 2006): C444—C452. http://dx.doi.org/10.1152/ajpcell.00218.2005.

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Fluid shear stress stimulation induces endothelial cells to elongate and align in the direction of applied flow. Using the complementary techniques of photoactivation of fluorescence and fluorescence recovery after photobleaching, we have characterized endothelial actin cytoskeleton dynamics during the alignment process in response to steady laminar fluid flow and have correlated these results to motility. Alignment requires 24 h of exposure to fluid flow, but the cells respond within minutes to flow and diminish their movement by 50%. Although movement slows, the actin filament turnover rate increases threefold and the percentage of total actin in the polymerized state decreases by 34%, accelerating actin filament remodeling in individual cells within a confluent endothelial monolayer subjected to flow to levels used by dispersed nonconfluent cells under static conditions for rapid movement. Temporally, the rapid decrease in filamentous actin shortly after flow stimulation is preceded by an increase in actin filament turnover, revealing that the earliest phase of the actin cytoskeletal response to shear stress is net cytoskeletal depolymerization. However, unlike static cells, in which cell motility correlates positively with the rate of filament turnover and negatively with the amount polymerized actin, the decoupling of enhanced motility from enhanced actin dynamics after shear stress stimulation supports the notion that actin remodeling under these conditions favors cytoskeletal remodeling for shape change over locomotion. Hours later, motility returned to pre-shear stress levels but actin remodeling remained highly dynamic in many cells after alignment, suggesting continual cell shape optimization. We conclude that shear stress initiates a cytoplasmic actin-remodeling response that is used for endothelial cell shape change instead of bulk cell translocation.

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7

Halbwirth, Florian, Eugenia Niculescu-Morzsa, Hannes Zwickl, Christoph Bauer, and Stefan Nehrer. "Mechanostimulation changes the catabolic phenotype of human dedifferentiated osteoarthritic chondrocytes." Knee Surgery, Sports Traumatology, Arthroscopy 23, no. 1 (November 7, 2014): 104–11. http://dx.doi.org/10.1007/s00167-014-3412-8.

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8

Indra, Indrajyoti, Alexander N. Gasparski, and Karen A. Beningo. "An in vitro correlation of metastatic capacity and dual mechanostimulation." PLOS ONE 13, no. 11 (November 14, 2018): e0207490. http://dx.doi.org/10.1371/journal.pone.0207490.

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9

John, Susan P., and Karl H. Hasenstein. "Effects of mechanostimulation on gravitropism and signal persistence in flax roots." Plant Signaling & Behavior 6, no. 9 (September 2011): 1365–70. http://dx.doi.org/10.4161/psb.6.9.16601.

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10

Tretner, C., U. Huth, and B. Hause. "Mechanostimulation of Medicago truncatula leads to enhanced levels of jasmonic acid." Journal of Experimental Botany 59, no. 10 (July 1, 2008): 2847–56. http://dx.doi.org/10.1093/jxb/ern145.

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11

Halbwirth, Florian, E. Niculescu-Morzsa, H. Zwickl, and S. Nehrer. "V 44 Effekt von Mechanostimulation auf 3-D-kultivierte osteoarthritische Knorpelzellen." Sport-Orthopädie - Sport-Traumatologie - Sports Orthopaedics and Traumatology 26, no. 2 (January 2010): 123. http://dx.doi.org/10.1016/j.orthtr.2010.02.031.

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12

Bobo, Justin, Akash Garg, Prahatha Venkatraman, Manoj Puthenveedu, and Philip R. LeDuc. "3D In Vitro Neuron on a Chip for Probing Calcium Mechanostimulation." Advanced Biosystems 4, no. 10 (September 2, 2020): 2000080. http://dx.doi.org/10.1002/adbi.202000080.

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13

Möltner, A., D. Kleinböhl, D. Schellberg, B. Winkens, and R. Hölzl. "702 Slow cortical responses to slow visceral and somatic mechanostimulation in humans." International Journal of Psychophysiology 30, no. 1-2 (September 1998): 265–66. http://dx.doi.org/10.1016/s0167-8760(98)90701-2.

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14

Mezencevová, Viktória, Jozef Torok, Tatiana Czánová, and Ján Zajac. "Endermologie New Aproach in the Medicine Treatment." Technological Engineering 14, no. 1 (October 26, 2017): 27–30. http://dx.doi.org/10.1515/teen-2017-0007.

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Abstract Using the effect of mechanical forces affecting cellular response in the treatment of post-traumatic, postoperative, post-imlantation conditions through the application of Endermologie®- mechanotransduction represents a revolutionary solution in tissue-rehabilitation and positive target tissue influencing, with faster regeneration (1). Endermologie® is a noninvasive, painless, natural method of treatments of all connective tissue transformations, muscle and circulation pathologies. The aim of our study is investigation and explanation the mechanism of action by observing the physiological effects of Endermologie® based on human studies. The paper is focused on monitoring of possitive effect tissue regeneration using endermologie as a tools mechanostimulation improvements of systems integridy and health improvement.

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15

Armbruster, Caroline, Constanze Dassow, Katharina Gamerdinger, Matthias Schneider, Migle Sumkauskaite, Josef Guttmann, and Stefan Schumann. "Mechanostimulation, electrostimulation and force measurement in anin vitromodel of the isolated rat diaphragm." Physiological Measurement 32, no. 12 (October 28, 2011): 1899–912. http://dx.doi.org/10.1088/0967-3334/32/12/002.

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16

Moon, P., S. Penuela, D. Laird, C. Attali, F. Berenbaum, and F. Beier. "Investigating the role of panx3 in mechanostimulation and pro-inflammatory responses in chondrocytes." Osteoarthritis and Cartilage 25 (April 2017): S150—S151. http://dx.doi.org/10.1016/j.joca.2017.02.249.

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17

Armbruster, Caroline, Matthias Schneider, Stefan Schumann, Katharina Gamerdinger, Maximiliano Cuevas, Sophie Rausch, Gerhard Baaken, and Josef Guttmann. "Characteristics of highly flexible PDMS membranes for long-term mechanostimulation of biological tissue." Journal of Biomedical Materials Research Part B: Applied Biomaterials 91B, no. 2 (November 2009): 700–705. http://dx.doi.org/10.1002/jbm.b.31446.

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18

Phua, Sin-Yong, Lorcan McGarvey, Meng Ngu, and Alvin Ing. "The Differential Effect of Gastroesophageal Reflux Disease on Mechanostimulation and Chemostimulation of the Laryngopharynx." Chest 138, no. 5 (November 2010): 1180–85. http://dx.doi.org/10.1378/chest.09-2387.

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19

Middleton, K., S. Al-Dujaili, X. Mei, A. Günther, and L. You. "Microfluidic co-culture platform for investigating osteocyte-osteoclast signalling during fluid shear stress mechanostimulation." Journal of Biomechanics 59 (July 2017): 35–42. http://dx.doi.org/10.1016/j.jbiomech.2017.05.012.

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20

Kotak, Vibhakar C., Charles H. Page, and Frank Abenante. "Intersegmental modulation of abdominal postural responses initiated by mechanostimulation of the swimmeret in lobster." Journal of Neurobiology 19, no. 3 (April 1988): 223–37. http://dx.doi.org/10.1002/neu.480190305.

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21

Micheler, Carina M., Paulina A. Geck, Fiona Charitou, René Leix, Peter Foehr, Jan J. Lang, Nikolas J. Wilhelm, Jutta L. Tuebel, and Rainer H. H. Burgkart. "Bioreactor design for the mechanical stimulation by compression of 3D cell cultures." Current Directions in Biomedical Engineering 7, no. 2 (October 1, 2021): 899–902. http://dx.doi.org/10.1515/cdbme-2021-2229.

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Abstract Bioreactors with a controlled physiological environment are being developed to study various cell processes. The influences of mechanostimulation on bone cell cultures can be investigated using a compression bioreactor. The developed bioreactor system applies a cyclic compression force to the specimen via an eccentrically mounted push rod. The compression force is monitored by a force sensor to detect changes in the material properties of the specimen. Depending on the piston setting, a stroke of 0.28 - 2.50 mm can be applied to the specimen. The bioreactor system was tested with a trial run of 18 days. A sample was continuously stimulated with a loading frequency of 2 Hz and a stroke of 1.50 mm. The sterility in the cell chamber as well as the functionality of the realised bioreactor stimulation system could be successfully confirmed

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22

Simakou, Theodoros, Robin Freeburn, and Fiona L. Henriquez. "Gene expression during THP-1 differentiation is influenced by vitamin D3 and not vibrational mechanostimulation." PeerJ 9 (July 14, 2021): e11773. http://dx.doi.org/10.7717/peerj.11773.

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Background In injury or infection, monocytes migrate into the affected tissues from circulation and differentiate into macrophages which are subsequently involved in the inflammatory responses. Macrophage differentiation and activation have been studied in response to multiple chemokines and cytokines. However, mechanical, and physical stimuli can also influence macrophage differentiation, activation, cytokine production, and phagocytic activity. Methods In this study the macrophage differentiation from THP-1 monocytes was assessed upon the stimulation with 1,25-dihydroxyvitamin D3 and 1,000 Hz vibrations, using qPCR for quantification of transcript expression. Vitamin D binds the vitamin D receptor (VDR) and subsequently modulates the expression of a variety of genes in monocytes. The effects of the 1,000 Hz vibrational stimulation, and the combined treatment of vitamin D3 and 1000 Hz vibrations were unknown. The differentiation of macrophages was assessed by looking at transcription of macrophage markers (e.g., CD14, CD36), antigen presenting molecules (e.g., HLA-DRA), transcription factors (e.g., LEF-1, TCF7L2), and mechanosensors (e.g., PIEZO1 and PKD2). Results The results showed that vitamin D3 induced THP-1 macrophage differentiation, which was characterized by upregulation of CD14 and CD36, downregulation of HLA-DRA, upregulation of the PKD2 (TRPP2), and an inverse relationship between TCF7L2 and LEF-1, which were upregulated and downregulated respectively. The 1,000 Hz vibrations were sensed from the cells which upregulated PIEZO1 and TCF3, but they did not induce expression of genes that would indicate macrophage differentiation. The mRNA transcription profile in the cells stimulated with the combined treatment was comparable to that of the cells stimulated by the vitamin only. The 1,000 Hz vibrations slightly weakened the effect of the vitamin for the regulation of CD36 and HLA-DMB in the suspension cells, but without causing changes in the regulation patterns. The only exception was the upregulation of TCF3 in the suspension cells, which was influenced by the vibrations. In the adherent cells, the vitamin D3 cancelled the upregulating effect of the 1,000 Hz vibrations and downregulated TCF3. The vitamin also cancelled the upregulation of PIEZO1 gene by the 1,000 Hz vibrations in the combined treatment. Conclusion The mechanical stimulation with 1,000 Hz vibrations resulted in upregulation of PIEZO1 in THP-1 cells, but it did not affect the differentiation process which was investigated in this study. Vitamin D3 induced THP-1 macrophage differentiation and could potentially influence M2 polarization as observed by upregulation of CD36 and downregulation of HLA-DRA. In addition, in THP-1 cells undergoing the combined stimulation, the gene expression patterns were influenced by vitamin D3, which also ablated the effect of the mechanical stimulus on PIEZO1 upregulation.

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23

Ladabaum, Uri, and David Glidden. "Perception of noxious gastric mechanostimulation in healthy humans is stable across repetitions and experimental methods." Gastroenterology 120, no. 5 (April 2001): A462. http://dx.doi.org/10.1016/s0016-5085(08)82292-5.

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24

Brady, Mariea A., Reva Vaze, Harsh D. Amin, Darryl R. Overby, and C. Ross Ethier. "The Design and Development of a High-Throughput Magneto-Mechanostimulation Device for Cartilage Tissue Engineering." Tissue Engineering Part C: Methods 20, no. 2 (February 2014): 149–59. http://dx.doi.org/10.1089/ten.tec.2013.0225.

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25

LADABAUM, U., and D. GLIDDEN. "Perception of noxious gastric mechanostimulation in healthy humans is stable across repetitions and experimental methods." Gastroenterology 120, no. 5 (April 2001): A462. http://dx.doi.org/10.1016/s0016-5085(01)82292-7.

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26

Gamerdinger, Katharina, Florian Wernet, Eva Smudde, Matthias Schneider, Josef Guttmann, and Stefan Schumann. "Mechanical load and mechanical integrity of lung cells – Experimental mechanostimulation of epithelial cell- and fibroblast-monolayers." Journal of the Mechanical Behavior of Biomedical Materials 40 (December 2014): 201–9. http://dx.doi.org/10.1016/j.jmbbm.2014.08.013.

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27

Kim, Sun Wook, Jonathan Ehrman, Mok-Ryeon Ahn, Jumpei Kondo, Andrea A. Mancheno Lopez, Yun Sik Oh, Xander H. Kim, et al. "Shear stress induces noncanonical autophagy in intestinal epithelial monolayers." Molecular Biology of the Cell 28, no. 22 (November 2017): 3043–56. http://dx.doi.org/10.1091/mbc.e17-01-0021.

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Flow of fluids through the gut, such as milk from a neonatal diet, generates a shear stress on the unilaminar epithelium lining the lumen. We report that exposure to physiological levels of fluid shear stress leads to the formation of large vacuoles, containing extracellular contents within polarizing intestinal epithelial cell monolayers. These observations lead to two questions: how can cells lacking primary cilia transduce shear stress, and what molecular pathways support the formation of vacuoles that can exceed 80% of the cell volume? We find that shear forces are sensed by actin-rich microvilli that eventually generate the apical brush border, providing evidence that these structures possess mechanosensing ability. Importantly, we identified the molecular pathway that regulates large vacuole formation downstream from mechanostimulation to involve central components of the autophagy pathway, including ATG5 and LC3, but not Beclin. Together our results establish a novel link between the actin-rich microvilli, the macroscopic transport of fluids across cells, and the noncanonical autophagy pathway in organized epithelial monolayers.

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Meyer, S., S. Schumann, J. Guttmann, and K. Gamerdinger. "Time-dependent apoptosis induction after spontaneous-breathing or ventilation-analogue experimental mechanostimulation of monolayer lung cell cultures." Critical Care 18, Suppl 1 (2014): P279. http://dx.doi.org/10.1186/cc13469.

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29

Halbwirth, F., E. Niculescu-Morzsa, H. Zwickl, and S. Nehrer. "460 TRAIN THE CHONDROCYTES: MECHANOSTIMULATION REVERSES THE CATABOLIC PHENOTYPE OF HUMAN MATRIX-EMBEDDED CHONDROCYTES - A PRELIMINARY REPORT." Osteoarthritis and Cartilage 17 (September 2009): S247. http://dx.doi.org/10.1016/s1063-4584(09)60481-7.

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30

Auluck, Angela, Vivek Mudera, Nigel P. Hunt, and Mark P. Lewis. "A three-dimensional in vitro model system to study the adaptation of craniofacial skeletal muscle following mechanostimulation." European Journal of Oral Sciences 113, no. 3 (June 2005): 218–24. http://dx.doi.org/10.1111/j.1600-0722.2005.00215.x.

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31

Yudin, E. K., Z. A. Tamarova, and O. A. Kryshtal'. "Responses Evoked in Afferent Fibers by Mechanostimulation of the Skin in vitro: Modulation by RFa-Like Peptides." Neurophysiology 37, no. 2 (March 2005): 120–26. http://dx.doi.org/10.1007/s11062-005-0053-z.

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32

Parisi, Cristian, Vikesh V. Chandaria, and Niamh C. Nowlan. "Blocking mechanosensitive ion channels eliminates the effects of applied mechanical loading on chick joint morphogenesis." Philosophical Transactions of the Royal Society B: Biological Sciences 373, no. 1759 (September 24, 2018): 20170317. http://dx.doi.org/10.1098/rstb.2017.0317.

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Abnormalities in joint shape are increasingly considered a critical risk factor for developing osteoarthritis in life. It has been shown that mechanical forces during prenatal development, particularly those due to fetal movements, play a fundamental role in joint morphogenesis. However, how mechanical stimuli are sensed or transduced in developing joint tissues is unclear. Stretch-activated and voltage-gated calcium ion channels have been shown to be involved in the mechanoregulation of chondrocytes in vitro . In this study, we analyse, for the first time, how blocking these ion channels influences the effects of mechanical loading on chick joint morphogenesis. Using in vitro culture of embryonic chick hindlimb explants in a mechanostimulation bioreactor, we block stretch-activated and voltage-gated ion channels using, respectively, gadolinium chloride and nifedipine. We find that the administration of high doses of either drug largely removed the effects of mechanical stimulation on growth and shape development in vitro , while neither drug had any effect in static cultures. This study demonstrates that, during joint morphogenesis, mechanical cues are transduced—at least in part—through mechanosensitive calcium ion channels, advancing our understanding of cartilage development and mechanotransduction. This article is part of the Theo Murphy meeting issue ‘Mechanics of development’.

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STERN, AMBER RATH, MATTHEW M. STERN, and MARK E. VAN DYKE. "TRANSDUCTION OF STRAIN TO CELLS SEEDED ONTO SCAFFOLDS EXPOSED TO UNIAXIAL STRETCHING: A THREE DIMENSIONAL FINITE ELEMENT STUDY." Journal of Mechanics in Medicine and Biology 12, no. 01 (March 2012): 1250022. http://dx.doi.org/10.1142/s0219519412004491.

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When preparing tissue engineering and regenerative medicine constructs, a commonly encountered problem is the failure of seeded cells to infiltrate the scaffold. In an increasing number of cases, constructs are being mechanically preconditioned with the expectation that preconditioning will enhance the construct's maturation and effectiveness by pre-exposing seeded cells to stimuli the tissue of interest experiences in vivo. However, whether or not mechanostimulation of a scaffold actually results in transmission of stimuli to the seeded cells remains poorly understood. The purpose of this research was to develop a model that quantifies how strain is transmitted to cells layered on a scaffold's surface compared to cells embedded within a scaffold. Three-dimensional finite element models representative of these conditions were created. When 10% strain was applied to the construct, embedded cells received the full imposed strain. However, cells growing on top of the scaffold received 5% strain within the first layer of cells, and the strain transmitted to cells in subsequent layers decreased exponentially with increasing distance from the scaffold's surface. When experimentally testing the model, strain-induced biological responses were muted in conditions where cell to scaffold contact was reduced. This research illustrates the importance of achieving cellular penetration and cell-to-scaffold contacts when mechanically conditioning tissue engineering constructs.

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R. Gintzler, Alan, and Barry R. Komisaruk. "Analgesia is produced by uterocervical mechanostimulation in rats: roles of afferent nerves and implications for analgesia of pregnancy and parturition." Brain Research 566, no. 1-2 (December 1991): 299–302. http://dx.doi.org/10.1016/0006-8993(91)91713-b.

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Haffner-Luntzer, Melanie, Anna Kovtun, Ina Lackner, Yvonne Mödinger, Steffen Hacker, Astrid Liedert, Jan Tuckermann, and Anita Ignatius. "Estrogen receptor α- (ERα), but not ERβ-signaling, is crucially involved in mechanostimulation of bone fracture healing by whole-body vibration." Bone 110 (May 2018): 11–20. http://dx.doi.org/10.1016/j.bone.2018.01.017.

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Feng, Nan-Hsiung, Hsang-Hsing Lee, Jeng-Chaun Shiang, and Ming-Chieh Ma. "Transient receptor potential vanilloid type 1 channels act as mechanoreceptors and cause substance P release and sensory activation in rat kidneys." American Journal of Physiology-Renal Physiology 294, no. 2 (February 2008): F316—F325. http://dx.doi.org/10.1152/ajprenal.00308.2007.

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Stimulation of capsaicin receptors results in an increase in afferent renal nerve activity (ARNA), but it is unclear how capsaicin contributes to sensory activation intrarenally. Here, we studied the relationships between capsaicin receptor activation, substance P (SP) release, and the sensory response in the rat renal pelvis. Immunoblots showed that one of the capsaicin receptors, transient receptor potential vanilloid type 1 channel (TRPV1), was found in various renal tissues and was especially abundant in the renal pelvis, where most sensory nerve fibers originate. Interestingly, immunolabeling showed colocalization of TRPV1, SP, and the panneuronal marker PGP9.5 in the renal pelvis. Electrophysiological recordings showed that SP and capsaicin activated the same mechanosensitive ARNA in a single-unit preparation. Intrapelvic administration of capsaicin or a specific TRPV1 agonist, resiniferatoxin, resulted in a dose-dependent increase in multi-unit ARNA and SP release, and these effects were blocked by the TRVP1 blocker capsazepine. Inhibition of the SP receptor by L-703,606 largely prevented capsaicin- or resiniferatoxin-induced ARNA. Capsazepine also prevented intrapelvic pressure (IPP)-dependent ARNA activation and contralateral diuresis/natriuresis in the renorenal reflex at an IPP of 20 mmHg, but had no effect at an IPP of 50 mmHg. These data indicate that TRPV1, a low-pressure baroreceptor, is present in the renal pelvis and exclusively regulates neuropeptide release from primary renal afferent C-fibers in response to mechanostimulation.

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Khatib, N., C. Parisi, and NC Nowlan. "Differential effect of frequency and duration of mechanical loading on fetal chick cartilage and bone development." European Cells and Materials 41 (May 25, 2021): 531–45. http://dx.doi.org/10.22203/ecm.v041a34.

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Developmental engineering strategies aim to recapitulate aspects of development in vitro as a means of forming functional engineered tissues, including cartilage and bone, for tissue repair and regeneration. Biophysical stimuli arising from fetal movements are critical for guiding skeletogenesis, but there have been few investigations of the biomechanical parameters which optimally promote cartilage and bone development events in in vitro explants. The effect of applied flexion-extension movement frequencies (0.33 and 0.67 Hz) and durations (2 h periods, 1, 2 or 3 × per day) on knee (stifle) joint cartilage shape, chondrogenesis and diaphyseal mineralisation of fetal chick hindlimbs, cultured in a mechanostimulation bioreactor, were assessed both quantitatively and qualitatively. It was hypothesised that increasing frequency and duration of movements would synergistically promote cartilage and bone formation in a dose-dependent manner. Increasing loading duration promoted cartilage growth, shape development and mineralisation of the femoral condyles and tibiotarsus. While increasing frequency had a significant positive effect on mineralisation, hyaline cartilage growth and joint shape were unaffected by frequency change within the ranges assessed, and there were limited statistical interactions between the effects of movement frequency and duration on cartilage or bone formation. Increased glycosaminoglycan deposition and cell proliferation may have contributed to the accelerated cartilage growth and shape change under increasing loading duration. The results demonstrated that frequencies and durations of applied biomechanical stimulation differentially promoted cartilage and bone formation, with implications for developmentally inspired tissue engineering strategies aiming to modulate tissue construct properties.

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38

Zhang, Zhong, Kristie Payne, Chunhua Cao, and Thomas L. Pallone. "Mural propagation of descending vasa recta responses to mechanical stimulation." American Journal of Physiology-Renal Physiology 305, no. 3 (August 1, 2013): F286—F294. http://dx.doi.org/10.1152/ajprenal.00220.2013.

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To investigate the responses of descending vasa recta (DVR) to deformation of the abluminal surface, we devised an automated method that controls duration and frequency of stimulation by utilizing a stream of buffer from a micropipette. During stimulation at one end of the vessel, fluorescent responses from fluo4 or bis[1,3-dibutylbarbituric acid-(5)] trimethineoxonol [DiBAC4(3)], indicating cytoplasmic calcium ([Ca2+]CYT) or membrane potential, respectively, were recorded from distant cells. Alternately, membrane potential was recorded from DVR pericytes by nystatin whole cell patch-clamp. Mechanical stimulation elicited reversible [Ca2+]CYT responses that increased with frequency. Individual pericyte responses along the vessel were initiated within a fraction of a second of one another. Those responses were inhibited by gap junction blockade with 18 β-glycyrrhetinic acid (100 μM) or phosphoinositide 3 kinase inhibition with 2-morpholin-4-yl-8-phenylchromen-4-one (50 μM). [Ca2+]CYT responses were blocked by removal of extracellular Ca2+ or L-type voltage-gated channel blockade with nifedipine (10 μM). At concentrations selective for the T-type channel blockade, mibefradil (100 nM) was ineffective. During mechanostimulation, pericytes rapidly depolarized, as documented with either DiBAC4(3) fluorescence or patch-clamp recording. Single stimuli yielded depolarizations of 22.5 ± 2.2 mV while repetitive stimuli at 0.1 Hz depolarized pericytes by 44.2 ± 4.0 mV. We conclude that DVR are mechanosensitive and that rapid transmission of signals along the vessel axis requires participation of gap junctions, L-type Ca2+ channels, and pericyte depolarization.

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Johnson, R. D., and J. B. Munson. "Regenerating sprouts of axotomized cat muscle afferents express characteristic firing patterns to mechanical stimulation." Journal of Neurophysiology 66, no. 6 (December 1, 1991): 2155–58. http://dx.doi.org/10.1152/jn.1991.66.6.2155.

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1. In cats, we studied the physiological properties of regenerating sprouts of muscle afferent fibers and compared them with sprouts from cutaneous afferent fibers. 2. Muscle nerves to the triceps surae and cutaneous sural nerves were axotomized in the popliteal fossa, and the proximal ends were inserted into nerve cuffs. Six days later, we recorded action potentials from single Groups I and II muscle and mostly Group II cutaneous afferents driven by mechanostimulation of the cuff. 3. Most muscle afferent sprouts (91%) had a regular slowly adapting discharge in response to sustained mechanical displacement of the cuff, particularly to sustained stretch stimuli, whereas most cutaneous afferents (92%) did not. Muscle afferents were more likely to have a spontaneous discharge and afterdischarge. 4. Group II muscle afferent sprouts had lower stretch thresholds and a higher incidence of spontaneous discharge compared with Group I fiber sprouts, whereas Group I fibers had a higher incidence of high-frequency afterdischarge to mechanical stimuli. 5. We conclude that, 6 days after axotomy, regenerating sprouts of muscle afferents, particularly Group II afferents, have become mechanosensitive in the absence of a receptor target and exhibit physiological properties similar to those found when innervating their native muscle but significantly different from sprouts of cutaneous afferents. Expression of these native muscle afferent firing patterns after the inappropriate reinnervation of hairy skin may be due to inherent properties of the muscle afferent fiber.

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Szychlinska, Marta A., Ugo D'Amora, Silvia Ravalli, Luigi Ambrosio, Michelino Di Rosa, and Giuseppe Musumeci. "Functional Biomolecule Delivery Systems and Bioengineering in Cartilage Regeneration." Current Pharmaceutical Biotechnology 20, no. 1 (March 22, 2019): 32–46. http://dx.doi.org/10.2174/1389201020666190206202048.

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Osteoarthritis (OA) is a common degenerative disease which involves articular cartilage, and leads to total joint disability in the advanced stages. Due to its avascular and aneural nature, damaged cartilage cannot regenerate itself. Stem cell therapy and tissue engineering represent a promising route in OA therapy, in which cooperation of mesenchymal stem cells (MSCs) and three-dimensional (3D) scaffolds contribute to cartilage regeneration. However, this approach still presents some limits such as poor mechanical properties of the engineered cartilage. The natural dynamic environment of the tissue repair process involves a collaboration of several signals expressed in the biological system in response to injury. For this reason, tissue engineering involving exogenous “influencers” such as mechanostimulation and functional biomolecule delivery systems (BDS), represent a promising innovative approach to improve the regeneration process. BDS provide a controlled release of biomolecules able to interact between them and with the injured tissue. Nano-dimensional BDS is the future hope for the design of personalized scaffolds, able to overcome the delivery problems. MSC-derived extracellular vesicles (EVs) represent an attractive alternative to BDS, due to their innate targeting abilities, immunomodulatory potential and biocompatibility. Future advances in cartilage regeneration should focus on multidisciplinary strategies such as modular assembly strategies, EVs, nanotechnology, 3D biomaterials, BDS, mechanobiology aimed at constructing the functional scaffolds for actively targeted biomolecule delivery. The aim of this review is to run through the different approaches adopted for cartilage regeneration, with a special focus on biomaterials, BDS and EVs explored in terms of their delivery potential, healing capabilities and mechanical features.

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Schulze-Tanzil, Gundula G., Manuel Delgado-Calcares, Richard Stange, Britt Wildemann, and Denitsa Docheva. "Tendon healing: a concise review on cellular and molecular mechanisms with a particular focus on the Achilles tendon." Bone & Joint Research 11, no. 8 (August 1, 2022): 561–74. http://dx.doi.org/10.1302/2046-3758.118.bjr-2021-0576.r1.

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Tendon is a bradytrophic and hypovascular tissue, hence, healing remains a major challenge. The molecular key events involved in successful repair have to be unravelled to develop novel strategies that reduce the risk of unfavourable outcomes such as non-healing, adhesion formation, and scarring. This review will consider the diverse pathophysiological features of tendon-derived cells that lead to failed healing, including misrouted differentiation (e.g. de- or transdifferentiation) and premature cell senescence, as well as the loss of functional progenitors. Many of these features can be attributed to disturbed cell-extracellular matrix (ECM) or unbalanced soluble mediators involving not only resident tendon cells, but also the cross-talk with immigrating immune cell populations. Unrestrained post-traumatic inflammation could hinder successful healing. Pro-angiogenic mediators trigger hypervascularization and lead to persistence of an immature repair tissue, which does not provide sufficient mechano-competence. Tendon repair tissue needs to achieve an ECM composition, structure, strength, and stiffness that resembles the undamaged highly hierarchically ordered tendon ECM. Adequate mechano-sensation and -transduction by tendon cells orchestrate ECM synthesis, stabilization by cross-linking, and remodelling as a prerequisite for the adaptation to the increased mechanical challenges during healing. Lastly, this review will discuss, from the cell biological point of view, possible optimization strategies for augmenting Achilles tendon (AT) healing outcomes, including adapted mechanostimulation and novel approaches by restraining neoangiogenesis, modifying stem cell niche parameters, tissue engineering, the modulation of the inflammatory cells, and the application of stimulatory factors. Cite this article: Bone Joint Res 2022;11(8):561–574.

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Schurman, Charles A., Stefaan W. Verbruggen, and Tamara Alliston. "Disrupted osteocyte connectivity and pericellular fluid flow in bone with aging and defective TGF-β signaling." Proceedings of the National Academy of Sciences 118, no. 25 (June 14, 2021): e2023999118. http://dx.doi.org/10.1073/pnas.2023999118.

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Skeletal fragility in the elderly does not simply result from a loss of bone mass. However, the mechanisms underlying the concurrent decline in bone mass, quality, and mechanosensitivity with age remain unclear. The important role of osteocytes in these processes and the age-related degeneration of the intricate lacunocanalicular network (LCN) in which osteocytes reside point to a primary role for osteocytes in bone aging. Since LCN complexity severely limits experimental dissection of these mechanisms in vivo, we used two in silico approaches to test the hypothesis that LCN degeneration, due to aging or an osteocyte-intrinsic defect in transforming growth factor beta (TGF-β) signaling (TβRIIocy−/−), is sufficient to compromise essential osteocyte responsibilities of mass transport and exposure to mechanical stimuli. Using reconstructed confocal images of bone with fluorescently labeled osteocytes, we found that osteocytes from aged and TβRIIocy−/− mice had 33 to 45% fewer, and more tortuous, canaliculi. Connectomic network analysis revealed that diminished canalicular density is sufficient to impair diffusion even with intact osteocyte numbers and overall LCN architecture. Computational fluid dynamics predicts that the corresponding drop in shear stress experienced by aged or TβRIIocy−/− osteocytes is highly sensitive to canalicular surface area but not tortuosity. Simulated expansion of the osteocyte pericellular space to mimic osteocyte perilacunar/canalicular remodeling restored predicted shear stress for aged osteocytes to young levels. Overall, these models show how loss of LCN volume through LCN pruning may lead to impaired fluid dynamics and osteocyte exposure to mechanostimulation. Furthermore, osteocytes emerge as targets of age-related therapeutic efforts to restore bone health and function.

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Schwenninger, David, Hanna Runck, Stefan Schumann, Jörg Haberstroh, and Josef Guttmann. "Locally measured shear moduli of pulmonary tissue and global lung mechanics in mechanically ventilated rats." Journal of Applied Physiology 113, no. 2 (July 15, 2012): 273–80. http://dx.doi.org/10.1152/japplphysiol.01620.2011.

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This study was aimed at measuring shear moduli in vivo in mechanically ventilated rats and comparing them to global lung mechanics. Wistar rats ( n = 28) were anesthetized, tracheally intubated, and mechanically ventilated in supine position. The animals were randomly assigned to the healthy control or the lung injury group where lung injury was induced by bronchoalveolar lavage. The respiratory system elastance Ers was analyzed based on the single compartment resistance/elastance lung model using multiple linear regression analysis. The shear modulus (G) of alveolar parenchyma was studied using a newly developed endoscopic system with adjustable pressure at the tip that was designed to induce local mechanostimulation. The data analysis was then carried out with an inverse finite element method. G was determined at continuous positive airway pressure (CPAP) levels of 15, 17, 20, and 30 mbar. The resulting shear moduli of lungs in healthy animals increased from 3.3 ± 1.4 kPa at 15 mbar CPAP to 5.8 ± 2.4 kPa at 30 mbar CPAP ( P = 0.012), whereas G was ∼2.5 kPa at all CPAP levels for the lung-injured animals. Regression analysis showed a negative correlation between G and relative Ers in the control group ( r = −0.73, P = 0.008 at CPA P = 20 mbar) and no significant correlation in the lung injury group. These results suggest that the locally measured G were inversely associated with the elastance of the respiratory system. Rejecting the study hypothesis the researchers concluded that low global respiratory system elastance is related to high local resistance against tissue deformation.

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Lin, Chian-Shiung, Shang-Hsing Lee, Ho-Shiang Huang, Yih-Sharng Chen, and Ming-Chieh Ma. "H2O2 generated by NADPH oxidase 4 contributes to transient receptor potential vanilloid 1 channel-mediated mechanosensation in the rat kidney." American Journal of Physiology-Renal Physiology 309, no. 4 (August 15, 2015): F369—F376. http://dx.doi.org/10.1152/ajprenal.00462.2014.

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The presence of NADPH oxidase (Nox) in the kidney, especially Nox4, results in H2O2 production, which regulates Na+ excretion and urine formation. Redox-sensitive transient receptor potential vanilloid 1 channels (TRPV1s) are distributed in mechanosensory fibers of the renal pelvis and monitor changes in intrapelvic pressure (IPP) during urine formation. The present study tested whether H2O2 derived from Nox4 affects TRPV1 function in renal sensory responses. Perfusion of H2O2 into the renal pelvis dose dependently increased afferent renal nerve activity and substance P (SP) release. These responses were attenuated by cotreatment with catalase or TRPV1 blockers. In single unit recordings, H2O2 activated afferent renal nerve activity in response to rising IPP but not high salt. Western blots revealed that Nox2 (gp91 phox) and Nox4 are both present in the rat kidney, but Nox4 is abundant in the renal pelvis and originates from dorsal root ganglia. This distribution was associated with expression of the Nox4 regulators p22 phox and polymerase δ-interacting protein 2. Coimmunoprecipitation experiments showed that IPP increases polymerase δ-interacting protein 2 association with Nox4 or p22 phox in the renal pelvis. Interestingly, immunofluorescence labeling demonstrated that Nox4 colocalizes with TRPV1 in sensory fibers of the renal pelvis, indicating that H2O2 generated from Nox4 may affect TRPV1 activity. Stepwise increases in IPP and saline loading resulted in H2O2 and SP release, sensory activation, diuresis, and natriuresis. These effects, however, were remarkably attenuated by Nox inhibition. Overall, these results suggest that Nox4-positive fibers liberate H2O2 after mechanostimulation, thereby contributing to a renal sensory nerve-mediated diuretic/natriuretic response.

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Wehner, Sven, Bettina M. Buchholz, Silke Schuchtrup, Anatol Rocke, Nico Schaefer, Mariola Lysson, Andreas Hirner, and Joerg C. Kalff. "Mechanical strain and TLR4 synergistically induce cell-specific inflammatory gene expression in intestinal smooth muscle cells and peritoneal macrophages." American Journal of Physiology-Gastrointestinal and Liver Physiology 299, no. 5 (November 2010): G1187—G1197. http://dx.doi.org/10.1152/ajpgi.00452.2009.

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Mechanical trauma of the gut is an unavoidable event in abdominal surgery. Former studies demonstrated that intestinal manipulation induces a strong inflammation within the tunica muscularis. We hypothesized that mechanical strain initiates or aggravates proinflammatory responses in intestinal smooth muscle cells (iSMC) or macrophages. First, an appropriate isolation and culture method for neonatal rat iSMC was established. Purified iSMC and primary peritoneal macrophages (pMacs) were subjected to static or cyclic strain, and gene expression of inducible nitric oxide synthase (iNOS), cyclooxygenase-2 (COX-2), IL-6, and IL-1β was analyzed by quantitative PCR. Supernatants from stretched iSMC were transferred to untreated pMacs or contrariwise, and medium transfer-triggered inflammatory gene expression was measured in unstretched cells. Finally, we investigated the synergistic effect of static strain on LPS-induced proinflammatory gene expression. Although cyclic strain failed, static strain significantly induced iNOS, COX-2, and IL-1β mRNA in iSMC. pMacs showed an increase in all inflammatory genes investigated as well as macrophage inflammatory protein (MIP)-1α and MIP-2 mRNA after static strain. Both cell entities liberated unknown mediators in response to stretch that mutually stimulated iNOS gene expression. Finally, mechanostimulation amplified LPS-induced iNOS and IL-1β gene expression in iSMC as well as COX-2 and IL-6 mRNA in pMacs. In conclusion, static strain initiates proinflammatory gene expression in iSMC and pMacs and triggers a bidirectional paracrine communication between both cultured cell entities via the liberation of unknown mediators. Furthermore, static strain synergistically operates with Toll-like receptor 4 ligation in a cell-specific manner. Hence, this study demonstrates that mechanical strain functions as an immunomodulatory stimulus in abdominal cells.

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Yakupov, Rafail’, Denis Pavlov, Sergey Anan’ev, Valentina Golodnova, and Mikhail Balykin. "Effect of Noninvasive Electrical Stimulation of the Spinal Cord and Mechanostimulation of Leg Muscles on the Changes in Systemic Haemodynamics at Preserved and Disrupted Supraspinal Connections." Journal of Medical and Biological Research, no. 3 (September 20, 2020): 319–23. http://dx.doi.org/10.37482/2687-1491-z024.

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Tanaka, Leonardo Y., Thaís L. S. Araujo, Andres I. Rodriguez, Mariana S. Ferraz, Vitor B. Pelegati, Mauro C. C. Morais, Aline M. dos Santos, et al. "Peri/epicellular protein disulfide isomerase-A1 acts as an upstream organizer of cytoskeletal mechanoadaptation in vascular smooth muscle cells." American Journal of Physiology-Heart and Circulatory Physiology 316, no. 3 (March 1, 2019): H566—H579. http://dx.doi.org/10.1152/ajpheart.00379.2018.

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Although redox processes closely interplay with mechanoresponses to control vascular remodeling, redox pathways coupling mechanostimulation to cellular cytoskeletal organization remain unclear. The peri/epicellular pool of protein disulfide isomerase-A1 (pecPDIA1) supports postinjury vessel remodeling. Using distinct models, we investigated whether pecPDIA1 could work as a redox-dependent organizer of cytoskeletal mechanoresponses. In vascular smooth muscle cells (VSMCs), pecPDIA1 immunoneutralization impaired stress fiber assembly in response to equibiaxial stretch and, under uniaxial stretch, significantly perturbed cell repositioning perpendicularly to stretch orientation. During cyclic stretch, pecPDIA1 supported thiol oxidation of the known mechanosensor β1-integrin and promoted polarized compartmentalization of sulfenylated proteins. Using traction force microscopy, we showed that pecPDIA1 organizes intracellular force distribution. The net contractile moment ratio of platelet-derived growth factor-exposed to basal VSMCs decreased from 0.90 ± 0.09 (IgG-exposed controls) to 0.70 ± 0.08 after pecPDI neutralization ( P < 0.05), together with an enhanced coefficient of variation for distribution of force modules, suggesting increased noise. Moreover, in a single cell model, pecPDIA1 neutralization impaired migration persistence without affecting total distance or velocity, whereas siRNA-mediated total PDIA1 silencing disabled all such variables of VSMC migration. Neither expression nor total activity of the master mechanotransmitter/regulator RhoA was affected by pecPDIA1 neutralization. However, cyclic stretch-induced focal distribution of membrane-bound RhoA was disrupted by pecPDI inhibition, which promoted a nonpolarized pattern of RhoA/caveolin-3 cluster colocalization. Accordingly, FRET biosensors showed that pecPDIA1 supports localized RhoA activity at cell protrusions versus perinuclear regions. Thus, pecPDI acts as a thiol redox-dependent organizer and noise reducer mechanism of cytoskeletal repositioning, oxidant generation, and localized RhoA activation during a variety of VSMC mechanoresponses. NEW & NOTEWORTHY Effects of a peri/epicellular pool of protein disulfide isomerase-A1 (pecPDIA1) during mechanoregulation in vascular smooth muscle cells (VSMCs) were highlighted using approaches such as equibiaxial and uniaxial stretch, random single cell migration, and traction force microscopy. pecPDIA1 regulates organization of the cytoskeleton and minimizes the noise of cell alignment, migration directionality, and persistence. pecPDIA1 mechanisms involve redox control of β1-integrin and localized RhoA activation. pecPDIA1 acts as a novel organizer of mechanoadaptation responses in VSMCs.

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Berkley, K. J., A. Robbins, and Y. Sato. "Functional differences between afferent fibers in the hypogastric and pelvic nerves innervating female reproductive organs in the rat." Journal of Neurophysiology 69, no. 2 (February 1, 1993): 533–44. http://dx.doi.org/10.1152/jn.1993.69.2.533.

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1. The uterus, cervix, and vaginal canal are innervated by afferent fibers in the hypogastric and pelvic nerves. Four studies compared the innervation territory and sensitivity to peripheral stimuli of the two sets of fibers in adult virgin rats. 2. Innervation territory was studied anatomically by injecting different fluorescent dyes into different parts of the reproductive, lower urinary, and lower digestive tracts and examining retrogradely labeled neurons in dorsal root ganglia. It was also studied electrophysiologically in anesthetized rats by summing potentials evoked in branches of the two nerves by electrical stimulation of different parts of the reproductive tract. 3. In both studies sensory innervation of the reproductive tract shifted from the pelvic to the hypogastric nerve (i.e., shifted entry into the spinal cord from the L6-S1 to the T13-L3 dorsal root ganglia, respectively) as the dye or stimulating electrode shifted from the vaginal entrance to the uterine horns, with fibers from both nerves densely innervating the cervix region (i.e., entering the spinal cord through both sets of ganglia). The anatomic results suggested that the regions innervated by fibers in one nerve might also be innervated by a small component of normally quiescent fibers in the other nerve. 4. Response sensitivity was studied electrophysiologically by simultaneously recording multiunit activity in branches of the hypogastric and pelvic nerves in two ways. First, in intact, anesthetized rats, activity was recorded during mechanical stimulation of the reproductive tract (distension of the vagina and uterus, probing the cervix). Second, in an in vitro organ preparation of the uterus and vagina, activity was recorded during chemical stimulation through the uterine artery with bradykinin, serotonin, NaCN, CO2, and KCl. 5. Pelvic nerve fibers were markedly more sensitive than hypogastric nerve fibers to uterine and cervical mechanostimulation. Similarly, pelvic nerve fibers were more likely to respond or responded more vigorously than hypogastric nerve fibers to all chemical stimuli (except KCl). 6. These results provide strong evidence that afferent fibers in the pelvic and hypogastric nerves of nulliparous adult rats subserve different functions in reproduction and sensation. Pelvic nerve fibers seem closely tied to sensory and behavioral processes associated with mating and conception, whereas hypogastric fibers seem closely tied to pregnancy and nociception, with fibers in both nerves serving functions during parturition.

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Hao, Jizhe, and Patrick Delmas. "Recording of mechanosensitive currents using piezoelectrically driven mechanostimulator." Nature Protocols 6, no. 7 (June 16, 2011): 979–90. http://dx.doi.org/10.1038/nprot.2011.343.

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Johnson, R. D., and R. L. Kitchell. "Mechanoreceptor response to mechanical and thermal stimuli in the glans penis of the dog." Journal of Neurophysiology 57, no. 6 (June 1, 1987): 1813–36. http://dx.doi.org/10.1152/jn.1987.57.6.1813.

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In the dog, we isolated 126 mechanoreceptive afferent fibers of the A-delta myelinated fiber class from the dorsal nerve of the penis using microdissection and extracellular electrophysiological techniques. Receptive fields on the glans penis were stimulated with a computer-controlled mechanostimulator and Peltier effect thermostimulator. The great majority of units were categorized as either rapidly adapting (RA) or slowly adapting (SA) and were located primarily proximally and distally, respectively, on the glans. In comparison to values from other glabrous skin regions in other species, mean displacement and force thresholds of penile mechanoreceptors were high, whereas the mean velocity thresholds were low. SA units, generally poor encoders of static displacement, were distinguishable into two types based on static response firing pattern but were not homologous to either the SA I or SA II mechanoreceptors found in other skin regions. Fifty-five units were given simultaneous mechanical and thermal stimulation. Very few units responded to pure thermal stimulation or increased their discharge frequency to skin cooling. Warm receptive-field temperatures between 35 and 43 degrees C increased mechanical sensitivity, measured by displacement and velocity coding functions, in almost all units tested. We conclude that canine penile mechanoreceptors, capable of encoding a variety of skin movements when the penis is warm, provide the spinal cord with the sensory input necessary to drive the spinal sexual reflexes. However, many appear to be at least physiologically different from mechanoreceptors native to other skin areas.

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