Extracellular matrix collagen alters cell proliferation and cell cycle progression of human uterine leiomyoma smooth muscle cells

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Koohestani, Faezeh ^a   Braundmeier, Andrea G ^a   Mahdian, Arash ^b   Seo, Jane ^a   Bi, Jia Jia ^a   Nowak, Romana A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b WOLFRAM RESEARCH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; FIBRILLAR COLLAGEN; FOCAL ADHESION KINASE; NONFIBRILLAR COLLAGEN; PLATELET DERIVED GROWTH FACTOR; PROTEIN P21; ACTIN; COLLAGEN;

ARTICLE; CARCINOGENESIS; CELL CYCLE PROGRESSION; CELL INTERACTION; CELL PROLIFERATION; CELL STIMULATION; CELL STRUCTURE; CONTROLLED STUDY; CULTURE MEDIUM; CYTOSKELETON; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EXTRACELLULAR MATRIX; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TUMOR GROWTH; UTERUS MYOMA; CELL CYCLE; CHEMISTRY; FOCAL ADHESION; LEIOMYOMA; METABOLISM; PATHOLOGY; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE;

ACTINS; CELL CYCLE; CELL PROLIFERATION; COLLAGEN; CYTOSKELETON; EXTRACELLULAR MATRIX; FEMALE; FIBRILLAR COLLAGENS; FOCAL ADHESIONS; HUMANS; LEIOMYOMA; MAP KINASE SIGNALING SYSTEM; MYOCYTES, SMOOTH MUSCLE; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY;

EID: 84899973851     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075844     Document Type: Article

References (94)

1. Houston KD, Hunter DS, Hodges LC, Walker CL (2001) Uterine leiomyomas: mechanisms of tumorigenesis. Toxicol Pathol 29: 100-104. doi:10.1080/019262301301418900. PubMed: 11215673.
2. Day Baird D, Dunson DB, Hill MC, Cousins D, Schectman JM (2003) High cumulative incidence of uterine leiomyoma in black and white women: ultrasound evidence. Am J Obstet Gynecol 188: 100-107. doi: 10.1067/mob.2003.99. PubMed: 12548202.
3. Bowden W, Skorupski J, Kovanci E, Rajkovic A (2009) Detection of novel copy number variants in uterine leiomyomas using highresolution SNP arrays. Mol Hum Reprod 15: 563-568. doi:10.1093/molehr/gap050. PubMed: 19567454.
4. Kawaguchi K, Fujii S, Konishi I, Nanbu Y, Nonogaki H et al. (1989) Mitotic activity in uterine leiomyomas during the menstrual cycle. Am J Obstet Gynecol 160: 637-641. doi:10.1016/S0002-9378(89)80046-8. PubMed: 2929683.
5. Stewart EA, Friedman AJ, Peck K, Nowak RA (1994) Relative overexpression of collagen type I and collagen type III messenger ribonucleic acids by uterine leiomyomas during the proliferative phase of the menstrual cycle. J Clin Endocrinol Metab 79: 900-906. doi: 10.1210/jc.79.3.900. PubMed: 8077380.
6. Stewart EA (2001) Uterine fibroids. Lancet 357: 293-298. doi:10.1016/S0140-6736(00)03622-9. PubMed: 11214143.
7. Leppert PC, Baginski T, Prupas C, Catherino WH, Pletcher S et al. (2004) Comparative ultrastructure of collagen fibrils in uterine leiomyomas and normal myometrium. Fertil Steril 82: 1182-1187. doi: 10.1016/j.fertnstert.2004.04.030. PubMed: 15474093.
8. Malik M, Norian J, McCarthy-Keith D, Britten J, Catherino WH (2010) Why leiomyomas are called fibroids: the central role of extracellular matrix in symptomatic women. Semin Reprod Med 28: 169-179. doi: 10.1055/s-0030-1251475. PubMed: 20414841.
9. Iwahashi M, Muragaki Y (2011) Increased type I and V collagen expression in uterine leiomyomas during the menstrual cycle. Fertil Steril 95: 2137-2139. doi:10.1016/j.fertnstert.2010.12.028. PubMed: 21215393.
10. Wolańska M, Sobolewski K, Drozdzewicz M, Bańkowski E (1998) Extracellular matrix components in uterine leiomyoma and their alteration during the tumour growth. Mol Cell Biochem 189: 145-152. doi:10.1023/A:1006914301565. PubMed: 9879665.
11. Leppert PC, Catherino WH, Segars JH (2006) A new hypothesis about the origin of uterine fibroids based on gene expression profiling with microarrays. Obstet Gynecol 195: 415-420. doi:10.1016/j.ajog. 2005.12.059.
12. Catherino WH, Leppert PC, Stenmark MH, Payson M, Potlog-Nahari C et al. (2004) Reduced dermatopontin expression is a molecular link between uterine leiomyomas and keloids. Genes Chromosomes Cancer 40: 204-217. doi:10.1002/gcc.20035. PubMed: 15139000.
13. Tsibris JC, Segars J, Coppola D, Mane S, Wilbanks GD et al. (2002) Insights from gene arrays on the development and growth regulation of uterine leiomyomata. Fertil Steril 78: 114-121. doi:10.1016/S0015-0282(02)03683-X. PubMed: 12095500.
14. Wolańska M, Sobolewski K, Bańkowski E, Jaworski S (2004) Matrix metalloproteinases of human leiomyoma in various stages of tumor growth. Gynecol Obstet Invest 58: 14-18. doi:10.1159/000077177. PubMed: 15004438.
15. Dimitrova IK, Richer JK, Rudolph MC, Spoelstra NS, Reno EM et al. (2009) Gene expression profiling of multiple leiomyomata uteri and matched normal tissue from a single patient. Fertil Steril 91: 2650-2663. doi:10.1016/j.fertnstert.2008.03.071. PubMed: 18672237.
16. Palmer SS, Haynes-Johnson D, Diehl T, Nowak RA (1998) Increased expression of stromelysin 3 mRNA in leiomyomas (uterine fibroids) compared with myometrium. J Soc Gynecol Invest 5: 203-209. doi: 10.1016/S1071-5576(98)00009-4. PubMed: 9699179.
17. Rogers R, Norian J, Malik M, Christman G, Abu-Asab M et al. (2008) Mechanical homeostasis is altered in uterine leiomyoma. Am J Obstet Gynecol 198:474: e1-e11. PubMed: 18395046.
18. Norian JM, Owen CM, Taboas J, Korecki C, Tuan R et al. (2011) Characterization of tissue biomechanics and mechanical signaling in uterine leiomyoma. Matrix Biol 31: 57-65. PubMed: 21983114.
19. Pickering JG (2001) Regulation of vascular cell behavior by collagen : form is function. Circ Res 88: 458-459. doi:10.1161/01.RES.88.5.458. PubMed: 11249867.
20. Henriet P, Zhong ZD, Brooks PC, Weinberg KI, DeClerck YA (2000) Contact with fibrillar collagen inhibits melanoma cell proliferation by up-regulating p27KIP1. Proc Natl Acad Sci U S A 97: 10026-10031. doi: 10.1073/pnas.170290997. PubMed: 10944199.
21. Sato K, Hattori S, Irie S, Kawashima S (2003) Spike formation by fibroblasts adhering to fibrillar collagen I gel. Cell Struct Funct 28: 229-241. doi:10.1247/csf.28.229. PubMed: 14586133.
22. Koyama H, Raines EW, Bornfeldt KE, Roberts JM, Ross R (1996) Fibrillar collagen inhibits arterial smooth muscle proliferation through regulation of Cdk2 inhibitors. Cell 87: 1069-1078. doi:10.1016/S0092-8674(00)81801-2. PubMed: 8978611.
23. Grinnell F (2000) Fibroblast-collagen-matrix contraction: growth-factor signalling and mechanical loading. Trends Cell Biol 10: 362-365. doi: 10.1016/S0962-8924(00)01802-X. PubMed: 10932093.
24. Kuzuya M, Satake S, Ramos MA, Kanda S, Koike T et al. (1999) Induction of apoptotic cell death in vascular endothelial cells cultured in three-dimensional collagen lattice. Exp Cell Res 248: 498-508. doi: 10.1006/excr.1999.4422. PubMed: 10222141.
25. Kojima N, Sato M, Imai K, Miura M, Matano Y et al. (1998) Hepatic stellate cells (vitamin A-storing cells) change their cytoskeleton structure by extracellular matrix components through a signal transduction system. Histochem Cell Biol 110: 121-128. doi:10.1007/s004180050273. PubMed: 9720984.
26. Herz DB, Aitken K, Bagli DJ (2003) Collagen directly stimulates bladder smooth muscle cell growth in vitro: regulation by extracellular regulated mitogen activated protein kinase. J Urol 170: 2072-2076. doi: 10.1097/01.ju.0000091810.33953.13. PubMed: 14532856.
27. Fassett J, Tobolt D, Hansen LK (2006) Type I collagen structure regulates cell morphology and EGF signaling in primary rat hepatocytes through cAMP-dependent protein kinase A. Mol Biol Cell 17: 345-356. PubMed: 16251347.
28. Nakagawa S, Pawelek P, Grinnell F (1989) Extracellular matrix organization modulates fibroblast growth and growth factor responsiveness. Exp Cell Res 182: 572-582. doi: 10.1016/0014-4827(89)90260-7. PubMed: 2721593.
29. Raines EW, Koyama H, Carragher NO (2000) The extracellular matrix dynamically regulates smooth muscle cell responsiveness to PDGF. Ann N Y Acad Sci 39: 51-62. PubMed: 10865824.
30. Wren FE, Schor AM, Schor SL, Grant ME (1986) Modulation of smooth muscle cell behaviour by platelet-derived factors and the extracellular matrix. J Cell Physiol 127: 297-302. doi:10.1002/jcp.1041270217. PubMed: 3700485.
31. Hollenbeck ST, Itoh H, Louie O, Faries PL, Liu B et al. (2004) Type I collagen synergistically enhances PDGF-induced smooth muscle cell proliferation through pp60src-dependent crosstalk between the α2β1 integrin and PDGFβ receptor. Biochem Biophys Res Commun 325: 328-337. doi:10.1016/j.bbrc.2004.10.031. PubMed: 15522237.
32. Mettouchi A, Klein S, Guo W, Lopez-Lago M, Lemichez E et al. (2001) Integrin-specific activation of Rac controls progression through the G(1) phase of the cell cycle. Mol Cell 8: 115-127. doi:10.1016/S1097-2765(01)00285-4. PubMed: 11511365.
33. Zhao J, Pestell R, Guan JL (2001) Transcriptional activation of cyclin D1 promoter by FAK contributes to cell cycle progression. Mol Biol Cell 12: 4066-4077. doi:10.1091/mbc.12.12.4066. PubMed: 11739801.
34. Provenzano PP, Inman DR, Eliceiri KW, Keely PJ (2009) Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene 28: 4326-4343. doi:10.1038/onc.2009.299. PubMed: 19826415.
35. Provenzano PP, Keely PJ (2011) Mechanical signaling through the cytoskeleton regulates cell proliferation by coordinated focal adhesion and Rho GTPase signaling. J Cell Sci 124: 1195-1205. doi:10.1242/jcs. 067009. PubMed: 21444750.
36. Klein EA, Yin L, Kothapalli D, Castagnino P, Byfield FJ et al. (2009) Cell-cycle control by physiological matrix elasticity and in vivo tissue stiffening. Curr Biol 19: 1511-1518. doi:10.1016/j.cub.2009.07.069. PubMed: 19765988.
37. Wall SJ, Werner E, Werb Z, DeClerck YA (2005) Discoidin domain receptor 2 mediates tumor cell cycle arrest induced by fibrillar collagen. J Biol Chem 280: 40187-40194. doi:10.1074/jbc.M508226200. PubMed: 16186104.
38. Hou G, Wang D, Bendeck MP (2011) Deletion of discoidin domain receptor 2 does not affect smooth muscle cell adhesion, migration, or proliferation in response to type I collagen. Cardiovasc Pathol 21: 214-218. PubMed: 21865059.
39. Lu KK, Trcka D, Bendeck MP (2010) Collagen stimulates discoidin domain receptor 1-mediated migration of smooth muscle cells through Src. Cardiovasc Pathol 20: 71-76. PubMed: 20093046.
40. Elliott JT, Tona A, Woodward JT, Jones PL, Plant AL (2003) Thin films of collagen affect smooth muscle cell morphology. Langmuir 19: 1506-1514. doi:10.1021/la026216r.
41. Yeh YT, Lee CI, Lim SH, Chen LJ, Wang WL et al. (2012) Convergence of physical and chemical signaling in the modulation of vascular smooth muscle cell cycle and proliferation by fibrillar collagen-regulated P66Shc. Biomaterials 33: 6728-6738. doi:10.1016/j.biomaterials.2012.06.030. PubMed: 22770800.
42. Schuliga M, Ong SC, Soon L, Zal F, Harris T et al. (2010) Airway smooth muscle remodels pericellular collagen fibrils: implications for proliferation. Am J Physiol Lung Cell Mol Physiol 298: L584-L592. doi: 10.1152/ajplung.00312.2009. PubMed: 20081066.
43. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE (1997) Geometric control of cell life and death. Science 276: 1425-1428. doi: 10.1126/science.276.5317.1425. PubMed: 9162012.
44. Cretel E, Pierres A, Benoliel AM, Bongrand P (2008) How cells feel their environment: a focus on early dynamic events. Cell Mol Bioeng 1: 5-14. doi:10.1007/s12195-008-0009-7. PubMed: 21151920.
45. Le Beyec J, Xu R, Lee SY, Nelson CM, Rizki A et al. (2007) Cell shape regulates global histone acetylation in human mammary epithelial cells. Exp Cell Res 313: 3066-3075. doi:10.1016/j.yexcr.2007.04.022. PubMed: 17524393.
46. Raines EW (2000) The extracellular matrix can regulate vascular cell migration, proliferation, and survival: relationships to vascular disease. Int J Exp Pathol 81: 173-182. PubMed: 10971738.
47. Tee SY, Fu J, Chen CS, Janmey PA (2011) Cell shape and substrate rigidity both regulate cell stiffness. Biophys J 100: L25-L27. doi: 10.1016/j.bpj.2010.12.342. PubMed: 21354386.
48. Hintze V, Miron A, Möller S, Schnabelrauch M, Heinemann S et al. (2012) Artificial extracellular matrices of collagen and sulphated hyaluronan enhance the differentiation of human mesenchymal stem cells in the presence of dexamethasone. J Tissue Eng Regen Med 4: 226-236. PubMed: 22718572.
49. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689. doi:10.1016/j.cell.2006.06.044. PubMed: 16923388.
50. Engler AJ, Griffin MA, Sen S, Bönnemann CG, Sweeney HL et al. (2004) Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J Cell Biol 166: 877-887. doi:10.1083/jcb.200405004. PubMed: 15364962.
51. Georges PC, Miller WJ, Meaney DF, Sawyer ES, Janmey PA (2006) Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. Biophys J 90: 3012-3018. doi:10.1529/biophysj.105.073114. PubMed: 16461391.
52. Goffin JM, Pittet P, Csucs G, Lussi JW, Meister JJ et al. (2006) Focal adhesion size controls tension-dependent recruitment of alpha-smooth muscle actin to stress fibers. J Cell Biol 172: 259-268. doi:10.1083/jcb. 200506179. PubMed: 16401722.
53. Lo CM, Wang HB, Dembo M, Wang YL (2000) Cell movement is guided by the rigidity of the substrate. Biophys J 79: 144-152. doi: 10.1016/S0006-3495(00)76279-5. PubMed: 10866943.
54. Yeung T, Georges PC, Flanagan LA, Marg B, Ortiz M et al. (2005) Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil Cytoskeleton 60: 24-34. doi:10.1002/cm. 20041. PubMed: 15573414.
55. Wozniak MA, Modzelewska K, Kwong L, Keely PJ (2004) Focal adhesion regulation of cell behavior. Biochim Biophys Acta 1692: 103-119. doi:10.1016/j.bbamcr.2004.04.007. PubMed: 15246682.
56. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI et al. (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8: 241-254. doi:10.1016/j.ccr.2005.08.010. PubMed: 16169468.
57. McDaniel DP, Shaw GA, Elliott JT, Bhadriraju K, Meuse C et al. (2007) The stiffness of collagen fibrils influences vascular smooth muscle cell phenotype. Biophys J 92: 1759-1769. doi:10.1529/biophysj. 106.089003. PubMed: 17158565.
58. Tsai KS, Kao SY, Wang CY, Wang YJ, Wang JP et al. (2010) Type I collagen promotes proliferation and osteogenesis of human mesenchymal stem cells via activation of ERK and Akt pathways. J Biomed Mater Res A 94: 673-682. PubMed: 20336745.
59. Mierke CT, Kollmannsberger P, Zitterbart DP, Diez G, Koch TM et al. (2010) Vinculin facilitates cell invasion into three-dimensional collagen matrices. J Biol Chem 285: 13121-13130. doi:10.1074/jbc.M109.087171. PubMed: 20181946.
60. Bhadriraju K, Chung KH, Spurlin TA, Haynes RJ, Elliott JT et al. (2009) The relative roles of collagen adhesive receptor DDR2 activation and matrix stiffness on the downregulation of focal adhesion kinase in vascular smooth muscle cells. Biomaterials 30: 6687-6694. doi: 10.1016/j.biomaterials.2009.08.036. PubMed: 19762078.
61. Cukierman E, Pankov R, Yamada KM (2002) Cell interactions with three-dimensional matrices. Curr Opin Cell Biol 14: 633-639. doi: 10.1016/S0955-0674(02)00364-2. PubMed: 12231360.
62. Ichii T, Koyama H, Tanaka S, Kim S, Shioi A et al. (2001) Fibrillar collagen specifically regulates human vascular smooth muscle cell genes involved in cellular responses and the pericellular matrix environment. Circ Res 88: 460-467. doi:10.1161/01.RES.88.5.460. PubMed: 11249868.
63. Karra L, Shushan A, Ben-Meir A, Rojansky N, Klein BY et al. (2010) Changes related to phosphatidylinositol 3-kinase/Akt signaling in leiomyomas: possible involvement of glycogen synthase kinase 3alpha and cyclin D2 in the pathophysiology. Fertil Steril 93: 2646-2651. doi: 10.1016/j.fertnstert.2009.03.100. PubMed: 19464003.
64. Kwon SH, Park JC, Ramachandran S, Cha SD, Kwon KY et al. (2008) Loss of cyclin g1 expression in human uterine leiomyoma cells induces apoptosis. Reprod Sci 215: 400-410. PubMed: 18497347.
65. Gao X, Yu L, Castro L, Tucker CJ, Moore AB et al. (2012) An essential role of p27 downregulation in fenvalerate-induced cell growth in human uterine leiomyoma and smooth muscle cells. Am J Physiol Endocrinol Metab 303: E1025-E1035. doi:10.1152/ajpendo.00107.2012. PubMed: 22850687.
66. Hwu YM, Li SH, Lee RK, Tsai YH, Yeh TS et al. (2008) Increased expression of platelet-derived growth factor C messenger ribonucleic acid in uterine leiomyomata. Fertil Steril 89: 468-471. doi:10.1016/j.fertnstert.2007.02.031. PubMed: 17482170.
67. Liang M, Wang H, Zhang Y, Lu S, Wang Z (2006) Expression and functional analysis of platelet-derived growth factor in uterine leiomyomata. Cancer Biol Ther 5: 28-33. doi:10.4161/cbt.5.1.2234. PubMed: 16294022.
68. Mesquita FS, Dyer SN, Heinrich DA, Bulun SE, Marsh EE et al. (2010 Reactive oxygen species mediate mitogenic growth factor signaling pathways in human leiomyoma smooth muscle cells. Biol Reprod 82: 341-351. PubMed: 19741209.
69. DeMali KA, Balciunaite E, Kazlauskas A (1999) Integrins enhance platelet-derived growth factor (PDGF)-dependent responses by altering the signal relay enzymes that are recruited to the PDGF beta receptor. J Biol Chem 274: 19551-19558. doi:10.1074/jbc.274.28.19551. PubMed: 10391888.
70. Plopper GE, McNamee HP, Dike LE, Bojanowski K, Ingber DE (1995) Convergence of integrin and growth factor receptor signaling pathways within the focal adhesion complex. Mol Biol Cell 6: 1349-1365. doi: 10.1091/mbc.6.10.1349. PubMed: 8573791.
71. Schneller M, Vuori K, Ruoslahti E (1997) Alphavbeta3 integrin associates with activated insulin and PDGFbeta receptors and potentiates the biological activity of PDGF. EMBO J 16: 5600-5607. doi: 10.1093/emboj/16.18.5600. PubMed: 9312019.
72. Soung YH, Clifford JL, Chung J (2010) Crosstalk between integrin and receptor tyrosine kinase signaling in breast carcinoma progression. BMB Rep 43:311-318
73. Woodard AS, García-Cardeña G, Leong M, Madri JA, Sessa WC et al. (1998) The synergistic activity of alphavbeta3 integrin and PDGF receptor increases cell migration. J Cell Sci 111: 469-478. PubMed: 9443896.
74. Yamada KM, Even-Ram S (2002) Integrin regulation of growth factor receptors. Nat Cell Biol 4: E75-E76. doi:10.1038/ncb0402-e75. PubMed: 11944037.
75. Ross RS (2004) Molecular and mechanical synergy: cross-talk between integrins and growth factor receptors. Cardiovasc Res 63: 381-390. doi: 10.1016/j.cardiores.2004.04.027. PubMed: 15276463.
76. Mahabeleshwar GH, Feng W, Reddy K, Plow EF, Byzova TV (2007) Mechanisms of integrin-vascular endothelial growth factor receptor cross-activation in angiogenesis. Circ Res 101: 570-580. doi:10.1161/CIRCRESAHA.107.155655. PubMed: 17641225.
77. Schrader J, Gordon-Walker TT, Aucott RL, van Deemter M, Quaas A et al. (2011) Matrix stiffness modulates proliferation, chemotherapeutic response, and dormancy in hepatocellular carcinoma cells. Hepatology 53: 1192-1205. doi:10.1002/hep.24108. PubMed: 21442631.
78. Gotoh Y, Nishida E, Yamashita T, Hoshi M, Kawakami M et al. (1990) Microtubule-associated-protein (MAP) kinase activated by nerve growth factor and epidermal growth factor in PC12 cells. Identity with the mitogen-activated MAP kinase of fibroblastic cells. Eur J Biochem 193: 661-669. doi:10.1111/j.1432-1033.1990.tb19384.x. PubMed: 2174361.
79. Nguyen TT, Scimeca JC, Filloux C, Peraldi P, Carpentier JL et al. (1993) Co-regulation of the mitogen-activated protein kinase, extracellular signal-regulated kinase 1, and the 90-kDa ribosomal S6 kinase in PC12 cells. Distinct effects of the neurotrophic factor, nerve growth factor, and the mitogenic factor, epidermal growth factor. J Biol Chem 268: 9803-9810. PubMed: 8387505.
80. Yamamoto T, Ebisuya M, Ashida F, Okamoto K, Yonehara S et al. (2006) Continuous ERK activation downregulates antiproliferative genes throughout G1 phase to allow cell-cycle progression. Curr Biol 16: 1171-1182. doi:10.1016/j.cub.2006.04.044. PubMed: 16782007.
81. Rescan C, Coutant A, Talarmin H, Theret N, Glaise D et al. (2001) Mechanism in the sequential control of cell morphology and S phase entry by epidermal growth factor involves distinct MEK/ERK activations. Mol Biol Cell 12: 725-738. doi:10.1091/mbc.12.3.725. PubMed: 11251083.
82. Chambard JC, Lefloch R, Pouysségur J, Lenormand P (2007) ERK implication in cell cycle regulation. Biochim Biophys Acta 1773: 1299-1310. doi:10.1016/j.bbamcr.2006.11.010. PubMed: 17188374.
83. Andreadi C, Noble C, Patel B, Jin H, Aguilar H et al. (2012) Regulation of MEK/ERK pathway output by subcellular localization of B-Raf. Biochem Soc Trans 40: 67-72. doi:10.1042/BST20110621. PubMed: 22260667.
84. Sewing A, Wiseman B, Lloyd AC, Land H (1997) High-intensity Raf signal causes cell cycle arrest mediated by p21Cip1. Mol Cell Biol 17: 5588-5597. PubMed: 9271434.
85. Woods D, Parry D, Cherwinski H, Bosch E, Lees E et al. (1997) Raf-induced proliferation or cell cycle arrest is determined by the level of Raf activity with arrest mediated by p21Cip1. Mol Cell Biol 17: 5598-5611. PubMed: 9271435.
86. Coleman ML, Marshall CJ, Olson MF (2003) Ras promotes p21(Waf1/Cip1) protein stability via a cyclin D1-imposed block in proteasome-mediated degradation. EMBO J 22: 2036-2046. doi:10.1093/emboj/cdg189. PubMed: 12727871.
87. Torii S, Yamamoto T, Tsuchiya Y, Nishida E (2006) ERK MAP kinase in G cell cycle progression and cancer. Cancer Sci 97: 697-702. doi: 10.1111/j.1349-7006.2006.00244.x. PubMed: 16800820.
88. Isoda M, Kanemori Y, Nakajo N, Uchida S, Yamashita K et al. (2009) The extracellular signal-regulated kinase-mitogen-activated protein kinase pathway phosphorylates and targets Cdc25A for SCF beta-TrCP-dependent degradation for cell cycle arrest. Mol Biol Cell 20: 2186-2195. doi:10.1091/mbc.E09-01-0008. PubMed: 19244340.
89. Wall SJ, Zhong ZD, DeClerck YA (2007) The cyclin-dependent kinase inhibitors p15INK4B and p21CIP1 are critical regulators of fibrillar collagen-induced tumor cell cycle arrest. J Biol Chem 282: 24471-24476. doi:10.1074/jbc.M702697200. PubMed: 17553787.
90. Caunt CJ, Rivers CA, Conway-Campbell BL, Norman MR, McArdle CA (2008) Epidermal growth factor receptor and protein kinase C signaling to ERK2: spatiotemporal regulation of ERK2 by dual specificity phosphatases. J Biol Chem 283: 6241-6252. doi:10.1074/jbc.M706624200. PubMed: 18178562.
91. Dikic I, Schlessinger J, Lax I (1994) PC12 cells overexpressing the insulin receptor undergo insulin-dependent neuronal differentiation. Curr Biol 4: 702-708. doi:10.1016/S0960-9822(00)00155-X. PubMed: 7953556.
92. Hong SK, Yoon S, Moelling C, Arthan D, Park JI (2009) Noncatalytic function of ERK1/2 can promote Raf/MEK/ERK-mediated growth arrest signaling. J Biol Chem 284: 33006-33018. doi:10.1074/jbc.M109.012591. PubMed: 19805545.
93. Hinz B (2010) The myofibroblast: Paradigm for a mechanically active cell. J Biomech 43: 146-155. doi:10.1016/j.jbiomech.2009.09.020. PubMed: 19800625.
94. Malik M, Catherino WH (2012) Development and validation of a three-dimensional in vitro model for uterine leiomyoma and patient-matched myometrium. Fertil Steril 97: 1287-1293. doi:10.1016/j.fertnstert. 2012.02.037. PubMed: 22425196.