Cells respond to mechanical stress and corresponding mechanisms of signal transduction_West China Medical Journal

Authors：

 WEI Tangqiang , NIU Chao , WU Ji , LI Yunxiang , ZHANG Zongping , WANG Anguo

Department of Urology, Affiliated Nanchong Central Hospital of North Sichuan Medical College, Nanchong, Sichuan 637000, P. R. China;

Corresponding author：

WEI Tangqiang, Email: 564533486@qq.com

Keywords：

Mechanical stress; signal transduction; cytoskeleton; integrin; ion channel

DOI：

10.7507/1002-0179.202007336

Video：

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Mechanical stress modulates almost all functions of cells. The key to exploring its biological effects lies in studying the perception of mechanical stress and its mechanism of mechanotransduction. This article details the perception and mechanotransduction mechanism of mechanical stress by extracellular matrix, cell membrane, cytoskeleton and nucleus. There are two main pathways for the perception and mechanotransduction of mechanical stress by cells, one is the direct transmission of force, and the other is the conversion of mechanical signal into chemical signal. The purpose of this study is to provide some reference for the exploration of precise treatment of mechanical stress-related diseases and the optimization of construction of tissue engineered organs by mechanical stress.

Citation： WEI Tangqiang, NIU Chao, WU Ji, LI Yunxiang, ZHANG Zongping, WANG Anguo. Cells respond to mechanical stress and corresponding mechanisms of signal transduction. West China Medical Journal, 2022, 37(3): 449-452. doi: 10.7507/1002-0179.202007336 Copy

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2.	Lee HP, Gu L, Mooney DJ, et al. Mechanical confinement regulates cartilage matrix formation by chondrocytes. Nat Mater, 2017, 16(12): 1243-1251.
3.	Fusco F, Creta M, De Nunzio C, et al. Progressive bladder remodeling due to bladder outlet obstruction: a systematic review of morphological and molecular evidences in humans. BMC Urol, 2018, 18(1): 15.
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5.	Janota CS, Calero-Cuenca FJ, Gomes ER. The role of the cell nucleus in mechanotransduction. Curr Opin Cell Biol, 2020, 63: 204-211.
6.	Theocharis AD, Skandalis SS, Gialeli C, et al. Extracellular matrix structure. Adv Drug Deliv Rev, 2016, 97: 4-27.
7.	Lou J, Stowers R, Nam S, et al. Stress relaxing hyaluronic acid-collagen hydrogels promote cell spreading, fiber remodeling, and focal adhesion formation in 3D cell culture. Biomaterials, 2018, 154: 213-222.
8.	Papanicolaou M, He P, Rutting S, et al. Extracellular matrix oxidised by the granulocyte oxidants hypochlorous and hypobromous acid reduces lung fibroblast adhesion and proliferation in vitro. Cells, 2021, 10(12): 3351.
9.	Ruddy JM, Akerman AW, Kimbrough D, et al. Differential hypertensive protease expression in the thoracic versus abdominal aorta. J Vasc Surg, 2017, 66(5): 1543-1552.
10.	Chaudhuri O, Gu L, Klumpers D, et al. Hydrogels with tunable stress relaxation regulate stem cell fate and activity. Nat Mater, 2016, 15(3): 326-334.
11.	Chen Y, Ju L, Rushdi M, et al. Receptor-mediated cell mechanosensing. Mol Biol Cell, 2017, 28(23): 3134-3155.
12.	Kim J, Lee J, Jang J, et al. Topological adaptation of transmembrane domains to the force-modulated lipid bilayer is a basis of sensing mechanical force. Curr Biol, 2020, 30(13): 2649.
13.	Folgering JH, Sharif-Naeini R, Dedman A, et al. Molecular basis of the mammalian pressure-sensitive ion channels: focus on vascular mechanotransduction. Prog Biophys Mol Biol, 2008, 97(2/3): 180-195.
14.	Li H. TRP channel classification. Adv Exp Med Biol, 2017, 976: 1-8.
15.	Feng J, Armillei MK, Yu AS, et al. Ca²⁺ signaling in cardiac fibroblasts and fibrosis-associated heart diseases. J Cardiovasc Dev Dis, 2019, 6(4): 34.
16.	Nikolaev YA, Cox CD, Ridone P, et al. Mammalian TRP ion channels are insensitive to membrane stretch. J Cell Sci, 2019, 132(23): jcs238360.
17.	Jernigan NL, Drummond HA. Myogenic vasoconstriction in mouse renal interlobar arteries: role of endogenous beta and gammaENaC. Am J Physiol Renal Physiol, 2006, 291(6): F1184-F1191.
18.	Knoepp F, Ashley Z, Barth D, et al. Shear force sensing of epithelial Na⁺ channel (ENaC) relies on N-glycosylated asparagines in the palm and knuckle domains of αENaC. Proc Natl Acad Sci U S A, 2020, 117(1): 717-726.
19.	Del Mármol J, Rietmeijer RA, Brohawn SG. Studying mechanosensitivity of two-pore domain k⁺ channels in cellular and reconstituted proteoliposome membranes. Methods Mol Biol, 2018, 1684: 129-150.
20.	Fancher IS, Levitan I. Endothelial inwardly-rectifying K⁺ channels as a key component of shear stress-induced mechanotransduction. Curr Top Membr, 2020, 85: 59-88.
21.	Campbell ID, Humphries MJ. Integrin structure, activation, and interactions. Cold Spring Harb Perspect Biol, 2011, 3(3): a004994.
22.	Fang Y, Wu D, Birukov KG. Mechanosensing and mechanoregulation of endothelial cell functions. Compr Physiol, 2019, 9(2): 873-904.
23.	Gerthoffer WT, Gunst SJ. Invited review: focal adhesion and small heat shock proteins in the regulation of actin remodeling and contractility in smooth muscle. J Appl Physiol (1985), 2001, 91(2): 963-972.
24.	Baker BM, Trappmann B, Wang WY, et al. Cell-mediated fibre recruitment drives extracellular matrix mechanosensing in engineered fibrillar microenvironments. Nat Mater, 2015, 14(12): 1262-1268.
25.	Shyy JY, Chien S. Role of integrins in cellular responses to mechanical stress and adhesion. Curr Opin Cell Biol, 1997, 9(5): 707-713.
26.	Owen LM, Adhikari AS, Patel M, et al. A cytoskeletal clutch mediates cellular force transmission in a soft, three-dimensional extracellular matrix. Mol Biol Cell, 2017, 28(14): 1959-1974.
27.	Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science, 2005, 310(5751): 1139-1143.
28.	Hohmann T, Dehghani F. The cytoskeleton-a complex interacting meshwork. Cells, 2019, 8(4): 362.
29.	Forgacs G. On the possible role of cytoskeletal filamentous networks in intracellular signaling: an approach based on percolation. J Cell Sci, 1995, 108(Pt 6): 2131-2143.
30.	Graham DM, Burridge K. Mechanotransduction and nuclear function. Curr Opin Cell Biol, 2016, 40: 98-105.
31.	Chakraborty S, Banerjee S, Raina M, et al. Force-directed “mechanointeractome” of talin-integrin. Biochemistry, 2019, 58(47): 4677-4695.
32.	Sivaramakrishnan S, Schneider JL, Sitikov A, et al. Shear stress induced reorganization of the keratin intermediate filament network requires phosphorylation by protein kinase C zeta. Mol Biol Cell, 2009, 20(11): 2755-2765.
33.	Joca HC, Coleman AK, Ward CW, et al. Quantitative tests reveal that microtubules tune the healthy heart but underlie arrhythmias in pathology. J Physiol, 2020, 598(7): 1327-1338.
34.	Maurer M, Lammerding J. The driving force: nuclear mechanotransduction in cellular function, fate, and disease. Annu Rev Biomed Eng, 2019, 21: 443-468.
35.	Cho S, Vashisth M, Abbas A, et al. Mechanosensing by the lamina protects against nuclear rupture, DNA damage, and cell-cycle arrest. Dev Cell, 2019, 49(6): 920-935.e5.
36.	Tajik A, Zhang Y, Wei F, et al. Transcription upregulation via force-induced direct stretching of chromatin. Nat Mater, 2016, 15(12): 1287-1296.
37.	Elosegui-Artola A, Andreu I, Beedle AEM, et al. Force triggers YAP nuclear entry by regulating transport across nuclear pores. Cell, 2017, 171(6): 1397-1410.e14.
38.	Lohberger B, Kaltenegger H, Weigl L, et al. Mechanical exposure and diacerein treatment modulates integrin-FAK-MAPKs mechanotransduction in human osteoarthritis chondrocytes. Cell Signal, 2019, 56: 23-30.
39.	Boutahar N, Guignandon A, Vico L, et al. Mechanical strain on osteoblasts activates autophosphorylation of focal adhesion kinase and proline-rich tyrosine kinase 2 tyrosine sites involved in ERK activation. J Biol Chem, 2004, 279(29): 30588-30599.
40.	Jeon YM, Kook SH, Son YO, et al. Role of MAPK in mechanical force-induced up-regulation of type Ⅰ collagen and osteopontin in human gingival fibroblasts. Mol Cell Biochem, 2009, 320(1/2): 45-52.

1. Benham-Pyle BW, Pruitt BL, Nelson WJ. Cell adhesion. Mechanical strain induces E-cadherin-dependent Yap1 and β-catenin activation to drive cell cycle entry. Science, 2015, 348(6238): 1024-1027.
2. Lee HP, Gu L, Mooney DJ, et al. Mechanical confinement regulates cartilage matrix formation by chondrocytes. Nat Mater, 2017, 16(12): 1243-1251.
3. Fusco F, Creta M, De Nunzio C, et al. Progressive bladder remodeling due to bladder outlet obstruction: a systematic review of morphological and molecular evidences in humans. BMC Urol, 2018, 18(1): 15.
4. Hoffman BD, Grashoff C, Schwartz MA. Dynamic molecular processes mediate cellular mechanotransduction. Nature, 2011, 475(7356): 316-323.
5. Janota CS, Calero-Cuenca FJ, Gomes ER. The role of the cell nucleus in mechanotransduction. Curr Opin Cell Biol, 2020, 63: 204-211.
6. Theocharis AD, Skandalis SS, Gialeli C, et al. Extracellular matrix structure. Adv Drug Deliv Rev, 2016, 97: 4-27.
7. Lou J, Stowers R, Nam S, et al. Stress relaxing hyaluronic acid-collagen hydrogels promote cell spreading, fiber remodeling, and focal adhesion formation in 3D cell culture. Biomaterials, 2018, 154: 213-222.
8. Papanicolaou M, He P, Rutting S, et al. Extracellular matrix oxidised by the granulocyte oxidants hypochlorous and hypobromous acid reduces lung fibroblast adhesion and proliferation in vitro. Cells, 2021, 10(12): 3351.
9. Ruddy JM, Akerman AW, Kimbrough D, et al. Differential hypertensive protease expression in the thoracic versus abdominal aorta. J Vasc Surg, 2017, 66(5): 1543-1552.
10. Chaudhuri O, Gu L, Klumpers D, et al. Hydrogels with tunable stress relaxation regulate stem cell fate and activity. Nat Mater, 2016, 15(3): 326-334.
11. Chen Y, Ju L, Rushdi M, et al. Receptor-mediated cell mechanosensing. Mol Biol Cell, 2017, 28(23): 3134-3155.
12. Kim J, Lee J, Jang J, et al. Topological adaptation of transmembrane domains to the force-modulated lipid bilayer is a basis of sensing mechanical force. Curr Biol, 2020, 30(13): 2649.
13. Folgering JH, Sharif-Naeini R, Dedman A, et al. Molecular basis of the mammalian pressure-sensitive ion channels: focus on vascular mechanotransduction. Prog Biophys Mol Biol, 2008, 97(2/3): 180-195.
14. Li H. TRP channel classification. Adv Exp Med Biol, 2017, 976: 1-8.
15. Feng J, Armillei MK, Yu AS, et al. Ca²⁺ signaling in cardiac fibroblasts and fibrosis-associated heart diseases. J Cardiovasc Dev Dis, 2019, 6(4): 34.
16. Nikolaev YA, Cox CD, Ridone P, et al. Mammalian TRP ion channels are insensitive to membrane stretch. J Cell Sci, 2019, 132(23): jcs238360.
17. Jernigan NL, Drummond HA. Myogenic vasoconstriction in mouse renal interlobar arteries: role of endogenous beta and gammaENaC. Am J Physiol Renal Physiol, 2006, 291(6): F1184-F1191.
18. Knoepp F, Ashley Z, Barth D, et al. Shear force sensing of epithelial Na⁺ channel (ENaC) relies on N-glycosylated asparagines in the palm and knuckle domains of αENaC. Proc Natl Acad Sci U S A, 2020, 117(1): 717-726.
19. Del Mármol J, Rietmeijer RA, Brohawn SG. Studying mechanosensitivity of two-pore domain k⁺ channels in cellular and reconstituted proteoliposome membranes. Methods Mol Biol, 2018, 1684: 129-150.
20. Fancher IS, Levitan I. Endothelial inwardly-rectifying K⁺ channels as a key component of shear stress-induced mechanotransduction. Curr Top Membr, 2020, 85: 59-88.
21. Campbell ID, Humphries MJ. Integrin structure, activation, and interactions. Cold Spring Harb Perspect Biol, 2011, 3(3): a004994.
22. Fang Y, Wu D, Birukov KG. Mechanosensing and mechanoregulation of endothelial cell functions. Compr Physiol, 2019, 9(2): 873-904.
23. Gerthoffer WT, Gunst SJ. Invited review: focal adhesion and small heat shock proteins in the regulation of actin remodeling and contractility in smooth muscle. J Appl Physiol (1985), 2001, 91(2): 963-972.
24. Baker BM, Trappmann B, Wang WY, et al. Cell-mediated fibre recruitment drives extracellular matrix mechanosensing in engineered fibrillar microenvironments. Nat Mater, 2015, 14(12): 1262-1268.
25. Shyy JY, Chien S. Role of integrins in cellular responses to mechanical stress and adhesion. Curr Opin Cell Biol, 1997, 9(5): 707-713.
26. Owen LM, Adhikari AS, Patel M, et al. A cytoskeletal clutch mediates cellular force transmission in a soft, three-dimensional extracellular matrix. Mol Biol Cell, 2017, 28(14): 1959-1974.
27. Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science, 2005, 310(5751): 1139-1143.
28. Hohmann T, Dehghani F. The cytoskeleton-a complex interacting meshwork. Cells, 2019, 8(4): 362.
29. Forgacs G. On the possible role of cytoskeletal filamentous networks in intracellular signaling: an approach based on percolation. J Cell Sci, 1995, 108(Pt 6): 2131-2143.
30. Graham DM, Burridge K. Mechanotransduction and nuclear function. Curr Opin Cell Biol, 2016, 40: 98-105.
31. Chakraborty S, Banerjee S, Raina M, et al. Force-directed “mechanointeractome” of talin-integrin. Biochemistry, 2019, 58(47): 4677-4695.
32. Sivaramakrishnan S, Schneider JL, Sitikov A, et al. Shear stress induced reorganization of the keratin intermediate filament network requires phosphorylation by protein kinase C zeta. Mol Biol Cell, 2009, 20(11): 2755-2765.
33. Joca HC, Coleman AK, Ward CW, et al. Quantitative tests reveal that microtubules tune the healthy heart but underlie arrhythmias in pathology. J Physiol, 2020, 598(7): 1327-1338.
34. Maurer M, Lammerding J. The driving force: nuclear mechanotransduction in cellular function, fate, and disease. Annu Rev Biomed Eng, 2019, 21: 443-468.
35. Cho S, Vashisth M, Abbas A, et al. Mechanosensing by the lamina protects against nuclear rupture, DNA damage, and cell-cycle arrest. Dev Cell, 2019, 49(6): 920-935.e5.
36. Tajik A, Zhang Y, Wei F, et al. Transcription upregulation via force-induced direct stretching of chromatin. Nat Mater, 2016, 15(12): 1287-1296.
37. Elosegui-Artola A, Andreu I, Beedle AEM, et al. Force triggers YAP nuclear entry by regulating transport across nuclear pores. Cell, 2017, 171(6): 1397-1410.e14.
38. Lohberger B, Kaltenegger H, Weigl L, et al. Mechanical exposure and diacerein treatment modulates integrin-FAK-MAPKs mechanotransduction in human osteoarthritis chondrocytes. Cell Signal, 2019, 56: 23-30.
39. Boutahar N, Guignandon A, Vico L, et al. Mechanical strain on osteoblasts activates autophosphorylation of focal adhesion kinase and proline-rich tyrosine kinase 2 tyrosine sites involved in ERK activation. J Biol Chem, 2004, 279(29): 30588-30599.
40. Jeon YM, Kook SH, Son YO, et al. Role of MAPK in mechanical force-induced up-regulation of type Ⅰ collagen and osteopontin in human gingival fibroblasts. Mol Cell Biochem, 2009, 320(1/2): 45-52.

West China Medical Journal

Cells respond to mechanical stress and corresponding mechanisms of signal transduction

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