ECM compliance regulates osteogenesis by influencing MAPK signaling downstream of RhoA and ROCK

Journal of Bone and Mineral Research

Volumn 24, Issue 5, 2009, Pages 886-898

  Khatiwala, Chirag B ^a   Kim, Peter D ^a   Peyton, Shelly R ^a   Putnam, Andrew J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California at Irvine   (United States)

Author keywords

Bone; Differentiation; Extracellular matrix; Extracellular signal regulated kinase mitogen activated protein kinase; Rhoa

Indexed keywords

ALKALINE PHOSPHATASE; BONE SIALOPROTEIN; MACROGOL; MITOGEN ACTIVATED PROTEIN KINASE; OSTEOCALCIN; PROTEIN ROCK; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; EXTRACELLULAR MATRIX; GENE EXPRESSION; MINERALIZATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ALKALINE PHOSPHATASE; ANIMALS; BONE MATRIX; CALCIFICATION, PHYSIOLOGIC; CELL ADHESION; CELL LINE; COMPLIANCE; CORE BINDING FACTOR ALPHA 1 SUBUNIT; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; HYDROGELS; MAP KINASE SIGNALING SYSTEM; MICE; MODELS, BIOLOGICAL; OSTEOCALCIN; OSTEOGENESIS; PHOSPHORYLATION; POLYETHYLENE GLYCOLS; PROTEIN KINASE INHIBITORS; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SIALOGLYCOPROTEINS;

EID: 65949097929     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1359/jbmr.081240     Document Type: Article

References (71)

1. Hynes RO 1992 Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 69:11-25.
2. Clark EA, Brugge JS 1995 Integrins and signal transduction pathways: The road taken. Science 268:233-239.
3. Schwartz MA 1997 Integrins, oncogenes, and anchorage independence. J Cell Biol 139:575-578.
4. Howe A, Aplin AE, Alahari SK, Juliano RL 1998 Integrin signaling and cell growth control. Curr Opin Cell Biol 10:220-231.
5. Engler A, Bacakova L, Newman C, Hategan A, Griffin M, Discher D 2004 Substrate compliance versus ligand density in cell on gel responses. Biophys J 86:617-628.
6. Engler AJ, Sen S, Sweeney HL, Discher DE 2006 Matrix elasticity directs stem cell lineage specification. Cell 126:677-689.
7. Khatiwala CB, Peyton SR, Putnam AJ 2006 Intrinsic mechanical properties of the extracellular matrix affect the behavior of pre-osteoblastic MC3T3-E1 cells. Am J Physiol Cell Physiol 290:C1640-C1650.
8. Peyton SR, Putnam AJ 2005 Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J Cell Physiol.
9. Polte TR, Eichler GS, Wang N, Ingber DE 2004 Extracellular matrix controls myosin light chain phosphorylation and cell contractility through modulation of cell shape and cytoskeletal prestress. Am J Physiol Cell Physiol 286:C518-C528.
10. Wong JY, Velasco A, Rajagopalan P, Pham Q 2003 Directed movement of vascular smooth muscle cells on gradient-compliant hydrogels. Langmuir 19:1908-1913.
11. Pelham RJ Jr, Wang Y 1997 Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci USA 94:13661- 13665.
12. Koch JC 1917 The laws of bone architecture. Am J Anat 21:177-298.
13. Wolff J 1982 Das Gesetz der Transformation der Knochen. Verlag August Hirschwald, Berlin, Germany.
14. Sikavitsas VI, Temenoff JS, Mikos AG 2001 Biomaterials and bone mechanotransduction. Biomaterials 22:2581-2593.
15. Peyton SR, Ghajar CM, Khatiwala CB, Putnam AJ 2007 The emergence of ECM mechanics and cytoskeletal tension as important regulators of cell function. Cell Biochem Biophys 47:300-320.
16. Ge C, Xiao G, Jiang D, Franceschi RT 2007 Critical role of the extracellular signal-regulated kinase-MAPK pathway in osteoblast differentiation and skeletal development. J Cell Biol 176:709-718.
17. Higuchi C, Myoui A, Hashimoto N, Kuriyama K, Yoshioka K, Yoshikawa H, Itoh K 2002 Continuous inhibition of MAPK signaling promotes the early osteoblastic differentiation and mineralization of the extracellular matrix. J Bone Miner Res 17:1785-1794.
18. Jadlowiec J, Koch H, Zhang X, Campbell PG, Seyedain M, Sfeir C 2004 Phosphophoryn regulates the gene expression and differentiation of NIH3T3, MC3T3-E1, and human mesen-chymal stem cells via the integrin/MAPK signaling pathway. J Biol Chem 279:53323-53330.
19. Jaiswal RK, Jaiswal N, Bruder SP, Mbalaviele G, Marshak DR, Pittenger MF 2000 Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase. J Biol Chem 275:9645-9652.
20. Klees RF, Salasznyk RM, Kingsley K, Williams WA, Boskey A, Plopper GE 2005 Laminin-5 induces osteogenic gene expression in human mesenchymal stem cells through an ERK-dependent pathway. Mol Biol Cell 16:881-890.
21. Salasznyk RM, Klees RF, Hughlock MK, Plopper GE 2004 ERK signaling pathways regulate the osteogenic differentiation of human mesenchymal stem cells on collagen I and vi-tronectin. Cell Commun Adhes 11:137-153.
22. Xiao G, Gopalakrishnan R, Jiang D, Reith E, Benson MD, Franceschi RT 2002 Bone morphogenetic proteins, extracellular matrix, and mitogen-activated protein kinase signaling pathways are required for osteoblast-specific gene expression and differentiation in MC3T3-E1 cells. J Bone Miner Res 17:101-110.
23. Xiao G, Jiang D, Gopalakrishnan R, Franceschi RT 2002 Fi-broblast growth factor 2 induction of the osteocalcin gene requires MAPK activity and phosphorylation of the osteoblast transcription factor, Cbfal/Runx2. J Biol Chem 277:36181-36187.
24. Xiao G, Jiang D, Thomas P, Benson MD, Guan K, Karsenty G, Franceschi RT 2000 MAPK pathways activate and phos-phorylate the osteoblast-specific transcription factor, Cbfa1. J Biol Chem 275:4453-4459.
25. Chen C, Koh AJ, Datta NS, Zhang J, Keller ET, Xiao G, Franceschi RT, D'Silva NJ, McCauley LK 2004 Impact of the mitogen-activated protein kinase pathway on parathyroid hormone-related protein actions in osteoblasts. J Biol Chem 279:29121-29129.
26. Hurley MM, Marcello K, Abreu C, Kessler M 1996 Signal transduction by basic fibroblast growth factor in rat osteoblastic Py1a cells. J Bone Miner Res 11:1256-1263.
27. Takeuchi Y, Suzawa M, Kikuchi T, Nishida E, Fujita T, Matsumoto T 1997 Differentiation and transforming growth factor-betareceptor down-regulation by collagen-alpha2betal integrin interaction is mediated by focal adhesion kinase and its downstream signals in murine osteoblastic cells. J Biol Chem 272:29309-29316.
28. You J, Reilly GC, Zhen X, Yellowley CE, Chen Q, Donahue HJ, Jacobs CR 2001 Osteopontin gene regulation by oscillatory fluid flow via intracellular calcium mobilization and activation of mitogen-activated protein kinase in MC3T3-E1 osteoblasts. J Biol Chem 276:13365-13371.
29. Khatiwala CB, Peyton SR, Metzke M, Putnam AJ 2007 The regulation of osteogenesis by ECM rigidity in MC3T3-E1 cells requires MAPK activation. J Cell Physiol 211:661-672.
30. Ren XD, Kiosses WB, Schwartz MA 1999 Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J 18:578-585.
31. Schoenwaelder SM, Burridge K 1999 Bidirectional signaling between the cytoskeleton and integrins. Curr Opin Cell Biol 11:274-286.
32. Clark EA, King WG, Brugge JS, Symons M, Hynes RO 1998 Integrin-mediated signals regulated by members of the rho family of GTPases. J Cell Biol 142:573-586.
33. Etienne-Manneville S, Hall A 2002 Rho GTPases in cell biology. Nature 420:629-635.
34. Hall A 1998 Rho GTPases and the actin cytoskeleton. Science 279:509-514.
35. Wittmann T, Waterman-Storer CM 2001 Cell motility: Can Rho GTPases and microtubules point the way? J Cell Sci 114:3795-3803.
36. Chong LD, Traynor-Kaplan A, Bokoch GM, Schwartz MA 1994 The small GTP-binding protein Rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells. Cell 79:507-513.
37. Chrzanowska-Wodnicka M, Burridge K 1996 Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J Cell Biol 133:1403-1415.
38. Nobes CD, Hall A 1995 Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81:53-62.
39. Putnam AJ, Cunningham JJ, Pillemer BB, Mooney DJ 2003 External mechanical strain regulates membrane targeting of Rho GTPases by controlling microtubule assembly. Am J Physiol Cell Physiol 284:C627-C639.
40. Matthews BD, Overby DR, Mannix R, Ingber DE 2006 Cellular adaptation to mechanical stress: Role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels. J Cell Sci 119:508-518.
41. Aikawa R, Komuro I, Yamazaki T, Zou Y, Kudoh S, Zhu W, Kadowaki T, Yazaki Y 1999 Rho family small G proteins play critical roles in mechanical stress-induced hypertrophic responses in cardiac myocytes. Circ Res 84:458-466.
42. Aoki H, Izumo S, Sadoshima J 1998 Angiotensin lI activates RhoA in cardiac myocytes: A critical role of RhoA in angiotensin II-induced premyofibril formation. Circ Res 82:666-676.
43. Katsumi A, Milanini J, Kiosses WB, del Pozo MA, Kaunas R, Chien S, Hahn KM, Schwartz MA 2002 Effects of cell tension on the small GTPase Rac. J Cell Biol 158:153-164.
44. Numaguchi K, Eguchi S, Yamakawa T, Motley ED, Inagami T 1999 Mechanotransduction of rat aortic vascular smooth muscle cells requires RhoA and intact actin filaments. Circ Res 85:5-11.
45. Sordella R, Jiang W, Chen GC, Curto M, Settleman J 2003 Modulation of Rho GTPase signaling regulates a switch between adipogenesis and myogenesis. Cell 113:147-158.
46. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS 2004 Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6:483-495.
47. Peyton SR, Raub CB, Keschrumrus VP, Putnam AJ 2006 The use of poly(ethylene glycol) hydrogels to investigate the impact of ECM chemistry and mechanics on smooth muscle cells. Biomaterials 27:4881-4893.
48. Raouf A, Seth A 2000 Ets transcription factors and targets in osteogenesis. Oncogene 19:6455-6463.
49. Ducy P 2000 Cbfal: A molecular switch in osteoblast biology. Dev Dyn 219:461-471.
50. Peyton SR, Kim PD, Ghajar CM, Seliktar D, Putnam AJ 2008 The effects of matrix stiffness and RhoA on the phenotypic plasticity of smooth muscle cells in a 3-D biosynthetic hydrogel system. Biomaterials 29:2597-2607.
51. Engler AJ, Griffin MA, Sen S, Bonnemann CG, Sweeney HL, Discher DE 2004 Myotubes differentiate optimally on substrates with tissue-like stiffness: Pathological implications for soft or stiff microenvironments. J Cell Biol 166:877-887.
52. Aubin JE, Liu F, Malaval L, Gupta AK 1995 Osteoblast and chondroblast differentiation. Bone 17(Suppl):77S-83S.
53. Ridley AJ, Hall A 1992 The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70:389-399.
54. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T 1997 Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755-764.
55. Choi JY, Lee BH, Song KB, Park RW, Kim IS, Sohn KY, Jo JS, Ryoo HM 1996 Expression patterns of bone-related proteins during osteoblastic differentiation in MC3T3-E1 cells. J Cell Biochem 61:609-618.
56. Franceschi RT 1999 The developmental control of osteoblast-specific gene expression: Role of specific transcription factors and the extracellular matrix environment. Crit Rev Oral Biol Med 10:40-57.
57. Aubin JE 1998 Advances in the osteoblast lineage. Biochem Cell Biol 76:899-910.
58. Farley JR, Baylink DJ 1986 Skeletal alkaline phosphatase activity as a bone formation index in vitro. Metabolism 35:563-571.
59. Bershadsky AD, Balaban NQ, Geiger B 2003 Adhesion-dependent cell mechanosensitivity. Annu Rev Cell Dev Biol 19:677-695.
60. Kapur S, Baylink DJ, Lau KH 2003 Fluid flow shear stress stimulates human osteoblast proliferation and differentiation through multiple interacting and competing signal transduc-tion pathways. Bone 32:241-251.
61. Reusch HP, Chan G, Ives HE, Nemenoff RA 1997 Activation of JNK/SAPK and ERK by mechanical strain in vascular smooth muscle cells depends on extracellular matrix composition. Biochem Biophys Res Commun 237:239-244.
62. Tseng H, Peterson TE, Berk BC 1995 Fluid shear stress stimulates mitogen-activated protein kinase in endothelial cells. Circ Res 77:869-878.
63. Wadhwa S, Godwin SL, Peterson DR, Epstein MA, Raisz LG, Pilbeam CC 2002 Fluid flow induction of cyclo-oxygenase 2 gene expression in osteoblasts is dependent on an extracellular signal-regulated kinase signaling pathway. J Bone Miner Res 17:266-274.
64. 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 28:436-442.
65. Wesselman JP, Kuijs R, Hermans JJ, Janssen GM, Fazzi GE, van Essen H, Evelo CT, Struijker-Boudier HA, De Mey JG 2004 Role of the Rhoa/Rho kinase system in flow-related remodeling of rat mesenteric small arteries in vivo. J Vase Res 41:277-290.
66. Franceschi RT, Xiao G 2003 Regulation of the osteoblast-specific transcription factor, Runx2: Responsiveness to multiple signal transduction pathways. J Cell Biochem 88:446-454.
67. Franceschi RT, Xiao G, Jiang D, Gopalakrishnan R, Yang S, Reith E 2003 Multiple signaling pathways converge on the Cbfal/Runx2 transcription factor to regulate osteoblast differentiation. Connect Tissue Res 44(Suppl 1):109-116.
68. Ziros PG, Gil AP, Georgakopoulos T, Habeos I, Kletsas D, Basdra EK, Papavassiliou AG 2002 The bone-specific transcriptional regulator Cbfa1 is a target of mechanical signals in osteoblastic cells. J Biol Chem 277:23934-23941.
69. Wang FS, Wang CJ, Sheen-Chen SM, Kuo YR, Chen RF, Yang KD 2002 Superoxide mediates shock wave induction of ERK-dependent osteogenic transcription factor (CBFA1) and mesenchymal cell differentiation toward osteoprogenitors. J Biol Chem 277:10931-10937.
70. 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 103:1141-1150.
71. Shiu YT, Li S, Yuan S, Wang Y, Nguyen P, Chien S 2003 Shear stress-induced c-fos activation is mediated by Rho in a calcium-dependent manner. Biochem Biophys Res Commun 303:548-555.