Differential activation and inhibition of rhoa by fluid flow induced shear stress in chondrocytes

Cell Biology International

Volumn 37, Issue 6, 2013, Pages 568-576

  Wan, Qiaoqiao ^a   Kim, Seung Joon ^a   Yokota, Hiroki ^a   Na, Sungsoo ^a  

^a Indiana University Purdue University Indianapolis   (United States)

Author keywords

Actin cytoskeleton; Cartilage; Fluorescence resonance energy transfer (FRET); Mechanical Loading; Rho GTPase; Traction force

Indexed keywords

GUANOSINE TRIPHOSPHATASE; METALLOPROTEINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ACTIN FILAMENT; ARTICLE; CARTILAGE CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; FLUID FLOW; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; MECHANOTRANSDUCTION; PROTEIN EXPRESSION; SHEAR STRESS;

EID: 84878178259     PISSN: 10656995     EISSN: 10958355     Source Type: Journal    
DOI: 10.1002/cbin.10072     Document Type: Article

References (43)

1. Amano M, Chihara K, Kimura K, Fukata Y, Nakamura N, Matsuura Y, Kaibuchi K (1997) Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 275: 1308-1
2. Arthur WT, Petch LA, Burridge K (2000) Integrin engagement suppresses RhoA activity via a c-Src-dependent mechanism. Curr Biol 10: 719-2
3. Burridge K, Wennerberg K (2004) Rho and Rac take center stage. Cell 116: 167-7
4. Butler JP, Tolic-Norrelykke IM, Fabry B, Fredberg JJ (2002) Traction fields, moments, and strain energy that cells exert on their surroundings. Am J Physiol Cell Physiol 282: C595-60
5. Chrzanowska-Wodnicka M, Burridge K (1996) Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J Cell Biol 33: 1403-1
6. Discher DE, Janmey P, Wang YL (2005) Tissue cells feel and respond to the stiffness of their substrate. Science 310: 1139-4
7. Etienne-Manneville S, Hall A (2002) Rho GTPases in cell biology. Nature 420: 629-3
8. Giannone G, Sheetz MP (2006) Substrate rigidity and force define form through tyrosine phosphatase and kinase pathways. Trends Cell Biol 16: 213-2
9. Goldring MB, Birkhead JR, Suen LF, Yamin R, Mizuno S, Glowacki J, Arbiser JL, Apperley JF (1994) Interleukin-1 beta-modulated gene expression in immortalized human chondrocytes. J Clin Invest 94: 2307-1
10. Guilluy C, Swaminathan V, Garcia-Mata R, O'Brien ET, Superfine R, Burridge K (2011) The Rho GEFs LARG and GEF-H1 regulate the mechanical response to force on integrins. Nat Cell Biol 13: 722-
11. Haudenschild DR, Nguyen B, Chen J, D'Lima DD, LotzMK. (2008) Rho kinase-dependent CCL20 induced by dynamic compression of human chondrocytes. Arthritis Rheum 58: 2735-4
12. Haudenschild DR, Chen J, Steklov N, Lotz MK, D'Lima DD (2009) Characterization of the chondrocyte actin cytoskeleton in living three-dimensional culture: response to anabolic and catabolic stimuli. Mol Cell Biomech 6: 135-4
13. Haudenschild DR, Chen J, Pang N, Lotz MK, D'Lima DD (2010) Rho kinase-dependent activation of SOX9 in chondrocytes. Arthritis Rheum 62: 191-20
14. Ingber DE (2003) Mechanobiology and diseases of mechanotransduction. Ann Med 35: 564-7
15. Jaalouk DE, Lammerding J (2009) Mechanotransduction gone awry. Nat Rev Mol Cell Biol 10: 63-7
16. Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21: 247-6
17. Janmey PA, McCulloch CA (2007) Cell mechanics: integrating cell responses tomechanical stimuli. Annual Rev Biomed Eng 9: 1-3
18. Johnson CP, Tang HY, Carag C, Speicher DW, Discher DE (2007) Forced unfolding of proteins within cells. Science 317: 663-
19. Kawamura S, Miyamoto S, Brown JH (2003) Initiation and transduction of stretch-induced RhoA and Rac1 activation through caveolae: cytoskeletal regulation of ERK translocation. J Biol Chem 78: 31111-
20. Kumar A,Murphy R, Robinson P,Wei L, Boriek AM. (2004) Cyclic mechanical strain inhibits skeletal myogenesis through activation of focal adhesion kinase, Rac-1 GTPase, and NF-kappaB transcription factor. FASEB J 18: 1524-3
21. Langelier E, Suetterlin R, Hoemann CD, Aebi U, Buschmann MD (2000) The chondrocyte cytoskeleton in mature articular cartilage: structure and distribution of actin, tubulin, and vimentin filaments. J Histochem Cytochem 48: 1307-2
22. Lee CR, Grodzinsky AJ, Spector M (2003) Modulation of the contractile and biosynthetic activity of chondrocytes seeded in collagen-glycosaminoglycan matrices. Tissue Eng 9: 27-3
23. Li S, Chen BP, Azuma N, Hu YL, Wu SZ, Sumpio BE, Shyy JY, Chien S (1999) Distinct roles for the small GTPases Cdc42 and Rho in endothelial responses to shear stress. J Clin Invest 103: 1141-5
24. Na S, Collin O, Chowdhury F, Tay B, Ouyang M,Wang Y,Wang N. (2008) Rapid signal transduction in living cells is a unique feature of mechanotransduction. Proc Natl Acad Sci USA 105: 6626-3
25. Olson MF (2004) Contraction reaction: mechanical regulation of Rho GTPase. Trends Cell Biol 14: 111-
26. Park S, Costa KD, Ateshian GA, Hong KS (2009) Mechanical properties of bovine articular cartilage under microscale indentation loading from atomic force microscopy. Proceedings of the Institution of Mechanical Engineers Part H. J Eng Med 223: 339-4
27. Pelham RJ, Jr,Wang Y (1997) Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci USA 94: 13661-
28. Poh YC, Na S, Chowdhury F, Ouyang M, Wang Y, Wang N (2009) Rapid activation of Rac GTPase in living cells by force is independent of Src. PLoS ONE 4: e788
29. Putnam AJ, Cunningham JJ, Pillemer BB, Mooney DJ (2003) External mechanical strain regulates membrane targeting of Rho GTPases by controlling microtubule assembly. AmJ Physiol Cell Physiol 284: C627-3
30. Qi YX, Qu MJ, Long DK, Liu B, Yao QP, Chien S, Jiang ZL (2008) Rho-GDP dissociation inhibitor alpha downregulated by low shear stress promotes vascular smooth muscle cell migration and apoptosis: a proteomic analysis. Cardiovasc Res 80: 114-2
31. Qiao J, Holian O, Lee BS, Huang F, Zhang J, Lum H (2008) Phosphorylation of GTP dissociation inhibitor by PKA negatively regulates RhoA. Am J Physiol Cell Physiol 295: C1161-
32. Ren XD, Kiosses WB, Sieg DJ, Otey CA, Schlaepfer DD, Schwartz MA (2000) Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover. J Cell Sci 113: 3673-
33. Ridley A (2000) Rho GTPases. Integrating integrin signaling. J Cell Biol 150: F107-
34. Sawada Y, Tamada M, Dubin-Thaler BJ, Cherniavskaya O, Sakai R, Tanaka S, Sheetz MP (2006) Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127: 1015-2
35. Shiu YT, Li S, Marganski WA, Usami S, Schwartz MA, Wang YL, Dembo M, Chien S (2004) Rho mediates the shear-enhancement of endothelial cell migration and traction force generation. Biophys J 86: 2558-6
36. Smith PG, Roy C, Zhang YN, Chauduri S (2003)Mechanical stress increases RhoA activation in airway smooth muscle cells. Am J Respir Cell Mol Biol 28: 436-4
37. Tzima E, del Pozo MA, Shattil SJ, Chien S, Schwartz MA. (2001) Activation of integrins in endothelial cells by fluid shear stress mediates Rho-dependent cytoskeletal alignment. EMBO J 20: 4639-4
38. Vogel V, Sheetz M (2006) Local force and geometry sensing regulate cell functions. Nat Rev Mol Cell Biol 7: 265-7
39. Wang Y, Botvinick EL, Zhao Y, Berns MW, Usami S, Tsien RY, Chien S (2005) Visualizing the mechanical activation of Src. Nature 434: 1040-
40. Wojciak-Stothard B, Ridley AJ (2003) Shear stress-induced endothelial cell polarization is mediated by Rho and Rac but not Cdc42 or PI 3-kinases. J Cell Biol 161: 429-3
41. Woods A,Wang G, Beier F (2005) RhoA/ROCK signaling regulates Sox9 expression and actin organization during chondrogenesis. J Biol Chem 280: 11626-3
42. Yokota H, Leong DJ, Sun HB (2011) Mechanical loading: bone remodeling and cartilage maintenance. Curr Osteoporos Rep 9: 237-4
43. Yoshizaki H, Ohba Y, Kurokawa K, Itoh RE, Nakamura T, Mochizuki N,Nagashima K, MatsudaM. (2003) Activity of Rhofamily GTPases during cell division as visualized with FRETbased probes. J Cell Biol 162: 223-3