Signalling pathways linking integrins with cell cycle progression

Matrix Biology

Volumn 34, Issue , 2014, Pages 144-153

  Moreno Layseca, Paulina ^a   Streuli, Charles H ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Adhesion complex; Akt; Cell cycle progression; ECM; Erk; Growth factor; Integrin; Proliferation; Rac

Indexed keywords

GROWTH FACTOR RECEPTOR; INTEGRIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; RAC PROTEIN;

CELL ADHESION; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL PROLIFERATION; CELL TYPE; CELLULAR DISTRIBUTION; MECHANOTRANSDUCTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; CELL CYCLE CHECKPOINT; EXTRACELLULAR MATRIX; GENETICS; HUMAN; METABOLISM; SIGNAL TRANSDUCTION;

CELL ADHESION; CELL CYCLE CHECKPOINTS; CELL PROLIFERATION; EXTRACELLULAR MATRIX; HUMANS; INTEGRINS; SIGNAL TRANSDUCTION;

EID: 84900342191     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2013.10.011     Document Type: Review

References (100)

1. Aszodi A., Hunziker E.B., Brakebusch C., Fässler R. Beta1 integrins regulate chondrocyte rotation, G1 progression, and cytokinesis. Genes Dev. 2003, 17:2465-2479.
2. Bartolomé R.A., Barderas R., Torres S., Fernandez-Aceñero M.J., Mendes M., García-Foncillas J., Lopez-Lucendo M., Casal J.I. Cadherin-17 interacts with α2β1 integrin to regulate cell proliferation and adhesion in colorectal cancer cells causing liver metastasis. Oncogene 2013.
3. Beebe K., Lee W.-C., Micchelli C.A. JAK/STAT signaling coordinates stem cell proliferation and multilineage differentiation in the Drosophila intestinal stem cell lineage. Dev. Biol. 2010, 338:28-37.
4. Bengtsson T., Aszodi A., Nicolae C., Hunziker E.B., Lundgren-Akerlund E., Fässler R. Loss of α10β1 integrin expression leads to moderate dysfunction of growth plate chondrocytes. J. Cell Sci. 2005, 118:929-936.
5. Biteau B., Jasper H. EGF signaling regulates the proliferation of intestinal stem cells in Drosophila. Development 2011, 138:1045-1055.
6. Blaess S., Graus-Porta D., Belvindrah R., Radakovits R., Pons S., Littlewood-Evans A., Senften M., Guo H., Li Y., Miner J.H., Reichardt L.F., Müller U. Beta1-integrins are critical for cerebellar granule cell precursor proliferation. J. Neurosci. 2004, 24:3402-3412.
7. Bon G., Di Carlo S.E., Folgiero V., Avetrani P., Lazzari C., D'Orazi G., Brizzi M.F., Sacchi A., Soddu S., Blandino G., Mottolese M., Falcioni R. Negative regulation of beta4 integrin transcription by homeodomain-interacting protein kinase 2 and p53 impairs tumor progression. Cancer Res. 2009, 69:5978-5986.
8. Bond M., Wu Y.-J., Sala-Newby G.B., Newby A.C. Rho GTPase, Rac1, regulates Skp2 levels, vascular smooth muscle cell proliferation, and intima formation in vitro and in vivo. Cardiovasc. Res. 2008, 80:290-298.
9. Borza C.M., Chen X., Mathew S., Mont S., Sanders C.R., Zent R., Pozzi A. Integrin α1β1 promotes caveolin-1 dephosphorylation by activating T cell protein-tyrosine phosphatase. J. Biol. Chem. 2010, 285:40114-40124.
10. Bott K., Upton Z., Schrobback K., Ehrbar M., Hubbell J.A., Lutolf M.P., Rizzi S.C. The effect of matrix characteristics on fibroblast proliferation in 3D gels. Biomaterials 2010, 31:8454-8464.
11. Brakebusch C., Grose R., Quondamatteo F., Ramirez A., Jorcano J.L., Pirro A., Svensson M., Herken R., Sasaki T., Timpl R., Werner S., Fässler R. Skin and hair follicle integrity is crucially dependent on beta 1 integrin expression on keratinocytes. EMBO J. 2000, 19:3990-4003.
12. Cabodi S., Morello V., Masi A., Cicchi R., Broggio C., Distefano P., Brunelli E., Silengo L., Pavone F., Arcangeli A., Turco E., Tarone G., Moro L., Defilippi P. Convergence of integrins and EGF receptor signaling via PI3K/Akt/FoxO pathway in early gene Egr-1 expression. J. Cell. Physiol. 2009, 218:294-303.
13. Cailleteau L., Estrach S., Thyss R., Boyer L., Doye A., Domange B., Johnsson N., Rubinstein E., Boucheix C., Ebrahimian T., Silvestre J.-S., Lemichez E., Meneguzzi G., Mettouchi A. α2β1 integrin controls association of Rac with the membrane and triggers quiescence of endothelial cells. J. Cell Sci. 2010, 123:2491-2501.
14. Chen X., Whiting C., Borza C., Hu W., Mont S., Bulus N., Zhang M.-Z., Harris R.C., Zent R., Pozzi A. Integrin α1β1 regulates epidermal growth factor receptor activation by controlling peroxisome proliferator-activated receptor γ-dependent caveolin-1 expression. Mol. Cell. Biol. 2010, 30:3048-3058.
15. Cohen K., Ellis M., Khoury S., Davis P.J., Hercbergs A., Ashur-Fabian O. Thyroid hormone is a MAPK-dependent growth factor for human myeloma cells acting via αvβ3 integrin. Mol. Cancer Res. 2011, 9:1385-1394.
16. Danussi C., Petrucco A., Wassermann B., Pivetta E., Modica T.M.E., Del Bel Belluz L., Colombatti A., Spessotto P. EMILIN1-α4/α9 integrin interaction inhibits dermal fibroblast and keratinocyte proliferation. J. Cell Biol. 2011, 195:131-145.
17. Dellinger M.T., Brekken R.A. Phosphorylation of Akt and ERK1/2 is required for VEGF-A/VEGFR2-induced proliferation and migration of lymphatic endothelium. PLoS ONE 2011, 6:e28947.
18. Diaferia G.R., Jimenez-Caliani A.J., Ranjitkar P., Yang W., Hardiman G., Rhodes C.J., Crisa L., Cirulli V. β1 integrin is a crucial regulator of pancreatic β-cell expansion. Development 2013.
19. Dong J.-M., Lau L.-S., Ng Y.-W., Lim L., Manser E. Paxillin nuclear-cytoplasmic localization is regulated by phosphorylation of the LD4 motif: evidence that nuclear paxillin promotes cell proliferation. Biochem. J. 2009, 418:173-184.
20. Du J., Liu J., Smith B.J., Tsao M.S., Cullen J.J. Role of Rac1-dependent NADPH oxidase in the growth of pancreatic cancer. Cancer Gene Ther. 2011, 18:135-143.
21. DuFort C.C., Paszek M.J., Weaver V.M. Balancing forces: architectural control of mechanotransduction. Nat. Rev. Mol. Cell Biol. 2011, 12:308-319.
22. Dydensborg A.B., Teller I.C., Groulx J.-F., Basora N., Paré F., Herring E., Gauthier R., Jean D., Beaulieu J.-F. Integrin α6Bβ4 inhibits colon cancer cell proliferation and c-Myc activity. BMC Cancer 2009, 9:223.
23. Eyckmans J., Boudou T., Yu X., Chen C.S. A hitchhiker's guide to mechanobiology. Dev. Cell 2011, 21:35-47.
24. Fang I.-M., Yang C.-H., Yang C.-M., Chen M.-S. Overexpression of integrin α6 and β4 enhances adhesion and proliferation of human retinal pigment epithelial cells on layers of porcine Bruch's membrane. Exp. Eye Res. 2009, 88:12-21.
25. Faraldo M.M., Deugnier M.A., Thiery J.P., Glukhova M.A. Growth defects induced by perturbation of beta1-integrin function in the mammary gland epithelium result from a lack of MAPK activation via the Shc and Akt pathways. EMBO Rep. 2001, 2:431-437.
26. Feltri M.L., Graus Porta D., Previtali S.C., Nodari A., Migliavacca B., Cassetti A., Littlewood-Evans A., Reichardt L.F., Messing A., Quattrini A., Mueller U., Wrabetz L. Conditional disruption of beta 1 integrin in Schwann cells impedes interactions with axons. J. Cell Biol. 2002, 156:199-209.
27. Fjellbirkeland L., Cambier S., Broaddus V.C., Hill A., Brunetta P., Dolganov G., Jablons D., Nishimura S.L. Integrin αvβ8-mediated activation of transforming growth factor-beta inhibits human airway epithelial proliferation in intact bronchial tissue. Am. J. Pathol. 2003, 163:533-542.
28. Fournier N.M., Lee B., Banasr M., Elsayed M., Duman R.S. Vascular endothelial growth factor regulates adult hippocampal cell proliferation through MEK/ERK- and PI3K/Akt-dependent signaling. Neuropharmacology 2012, 63:642-652.
29. Franzen C.A., Chen C.-C., Todorović V., Juric V., Monzon R.I., Lau L.F. Matrix protein CCN1 is critical for prostate carcinoma cell proliferation and TRAIL-induced apoptosis. Mol. Cancer Res. 2009, 7:1045-1055.
30. Freindorf M., Furlani T.R., Kong J., Cody V., Davis F.B., Davis P.J. Combined QM/MM study of thyroid and steroid hormone analogue interactions with αvβ3 integrin. J. Biomed. Biotechnol. 2012, 2012:959057.
31. Goodman S.L., Picard M. Integrins as therapeutic targets. Trends Pharmacol. Sci. 2012, 33:405-412.
32. Grassian A.R., Schafer Z.T., Brugge J.S. ErbB2 stabilizes epidermal growth factor receptor (EGFR) expression via Erk and Sprouty2 in extracellular matrix-detached cells. J. Biol. Chem. 2011, 286:79-90.
33. Grose R., Hutter C., Bloch W., Thorey I., Watt F.M., Fässler R., Brakebusch C., Werner S. A crucial role of beta 1 integrins for keratinocyte migration in vitro and during cutaneous wound repair. Development 2002, 129:2303-2315.
34. Guo W., Pylayeva Y., Pepe A., Yoshioka T., Muller W.J., Inghirami G., Giancotti F.G. Beta 4 integrin amplifies ErbB2 signaling to promote mammary tumorigenesis. Cell 2006, 126:489-502.
35. He H., Shulkes A., Baldwin G.S. PAK1 interacts with beta-catenin and is required for the regulation of the beta-catenin signalling pathway by gastrins. Biochim. Biophys. Acta 2008, 1783:1943-1954.
36. Hirsch E., Barberis L., Brancaccio M., Azzolino O., Xu D., Kyriakis J.M., Silengo L., Giancotti F.G., Tarone G., Fässler R., Altruda F. Defective Rac-mediated proliferation and survival after targeted mutation of the beta1 integrin cytodomain. J. Cell Biol. 2002, 157:481-492.
37. Hu Y., Ylivinkka I., Chen P., Li L., Hautaniemi S., Nyman T.A., Keski-Oja J., Hyytiäinen M. Netrin-4 promotes glioblastoma cell proliferation through integrin β4 signaling. Neoplasia 2012, 14:219-227.
38. Jeanes A.I., Wang P., Moreno-Layseca P., Paul N., Cheung J., Tsang R., Akhtar N., Foster F.M., Brennan K., Streuli C.H. Specific β-containing integrins exert differential control on proliferation and two-dimensional collective cell migration in mammary epithelial cells. J. Biol. Chem. 2012, 287:24103-24112.
39. Jung G.-Y., Park Y.-J., Han J.-S. Mediation of Rac1 activation by kindlin-2: an essential function in osteoblast adhesion, spreading, and proliferation. J. Cell. Biochem. 2011, 112:2541-2548.
40. Kalfa T.A., Pushkaran S., Zhang X., Johnson J.F., Pan D., Daria D., Geiger H., Cancelas J.A., Williams D.A., Zheng Y. Rac1 and Rac2 GTPases are necessary for early erythropoietic expansion in the bone marrow but not in the spleen. Haematologica 2010, 95:27-35.
41. Kawano S., Mizutani K., Miyata M., Ikeda W., Takai Y. Interaction of integrin α6β4 with ErbB3 and implication in heregulin-induced ErbB3/ErbB2-mediated DNA synthesis. Genes Cells 2010, 15:995-1001.
42. Kelly M.L., Chernoff J. Mouse models of PAK function. Cell Logist. 2012, 2:84-88.
43. Kim J.-H., Asthagiri A.R. Matrix stiffening sensitizes epithelial cells to EGF and enables the loss of contact inhibition of proliferation. J. Cell Sci. 2011, 124:1280-1287.
44. Klein E.A., Yin L., Kothapalli D., Castagnino P., Byfield F.J., Xu T., Levental I., Hawthorne E., Janmey P.A., Assoian R.K. Cell-cycle control by physiological matrix elasticity and in vivo tissue stiffening. Curr. Biol. 2009, 19:1511-1518.
45. Kyrkou A., Soufi M., Bahtz R., Ferguson C., Bai M., Parton R.G., Hoffmann I., Zerial M., Fotsis T., Murphy C. RhoD participates in the regulation of cell-cycle progression and centrosome duplication. Oncogene 2013, 32:1831-1842.
46. LaFlamme S.E., Nieves B., Colello D., Reverte C.G. Integrins as regulators of the mitotic machinery. Curr. Opin. Cell Biol. 2008, 20:576-582.
47. Legate K.R., Wickström S.A., Fässler R. Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev. 2009, 23:397-418.
48. Li N., Zhang Y., Naylor M.J., Schatzmann F., Maurer F., Wintermantel T., Schuetz G., Mueller U., Streuli C.H., Hynes N.E. Beta1 integrins regulate mammary gland proliferation and maintain the integrity of mammary alveoli. EMBO J. 2005, 24:1942-1953.
49. Lin G., Zhang X., Ren J., Pang Z., Wang C., Xu N., Xi R. Integrin signaling is required for maintenance and proliferation of intestinal stem cells in Drosophila. Dev. Biol. 2013, 377:177-187.
50. López-Rovira T., Silva-Vargas V., Watt F.M. Different consequences of beta1 integrin deletion in neonatal and adult mouse epidermis reveal a context-dependent role of integrins in regulating proliferation, differentiation, and intercellular communication. J. Invest. Dermatol. 2005, 125:1215-1227.
51. Mack N.A., Whalley H.J., Castillo-Lluva S., Malliri A. The diverse roles of Rac signaling in tumorigenesis. Cell Cycle 2011, 10:1571-1581.
52. Margadant C., Cremers L., Sonnenberg A., Boonstra J. MAPK uncouples cell cycle progression from cell spreading and cytoskeletal organization in cycling cells. Cell. Mol. Life Sci. 2013, 70:293-307.
53. Meng R., Tang H.-Y., Westfall J., London D., Cao J.H., Mousa S.A., Luidens M., Hercbergs A., Davis F.B., Davis P.J., Lin H.-Y. Crosstalk between integrin αvβ3 and estrogen receptor-α is involved in thyroid hormone-induced proliferation in human lung carcinoma cells. PLoS ONE 2011, 6:e27547.
54. Müller U., Wang D., Denda S., Meneses J.J., Pedersen R.A., Reichardt L.F. Integrin α8β1 is critically important for epithelial-mesenchymal interactions during kidney morphogenesis. Cell 1997, 88:603-613.
55. Murgia C., Blaikie P., Kim N., Dans M., Petrie H.T., Giancotti F.G. Cell cycle and adhesion defects in mice carrying a targeted deletion of the integrin beta4 cytoplasmic domain. EMBO J. 1998, 17:3940-3951.
56. Mut M., Lule S., Demir O., Kurnaz I.A., Vural I. Both mitogen-activated protein kinase (MAPK)/extracellular-signal-regulated kinases (ERK) 1/2 and phosphatidylinositide-3-OH kinase (PI3K)/Akt pathways regulate activation of E-twenty-six (ETS)-like transcription factor 1 (Elk-1) in U138 glioblastoma cells. Int. J. Biochem. Cell Biol. 2012, 44:302-310.
57. Muthuswamy S.K., Li D., Lelievre S., Bissell M.J., Brugge J.S. ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat. Cell Biol. 2001, 3:785-792.
58. Nho R.S., Kahm J. beta1-Integrin-collagen interaction suppresses FoxO3a by the coordination of Akt and PP2A. J. Biol. Chem. 2010, 285:14195-14209.
59. Nikolopoulos S.N., Blaikie P., Yoshioka T., Guo W., Puri C., Tacchetti C., Giancotti F.G. Targeted deletion of the integrin beta4 signaling domain suppresses laminin-5-dependent nuclear entry of mitogen-activated protein kinases and NF-kappaB, causing defects in epidermal growth and migration. Mol. Cell. Biol. 2005, 25:6090-6102.
60. Novitskaya V., Romanska H., Kordek R., Potemski P., Kusińska R., Parsons M., Odintsova E., Berditchevski F. Integrin α3β1-CD151 complex regulates dimerization of ErbB2 via RhoA. Oncogene 2013.
61. Oommen S., Gupta S.K., Vlahakis N.E. Vascular endothelial growth factor A (VEGF-A) induces endothelial and cancer cell migration through direct binding to integrin α9β1 identification of a specific α9β1 binding site. J. Biol. Chem. 2011, 286:1083-1092.
62. Panchatcharam M., Miriyala S., Yang F., Leitges M., Chrzanowska-Wodnicka M., Quilliam L.A., Anaya P., Morris A.J., Smyth S.S. Enhanced proliferation and migration of vascular smooth muscle cells in response to vascular injury under hyperglycemic conditions is controlled by beta3 integrin signaling. Int. J. Biochem. Cell Biol. 2010, 42:965-974.
63. Park J., Arakawa-Takeuchi S., Jinno S., Okayama H. Rho-associated kinase connects a cell cycle-controlling anchorage signal to the mammalian target of rapamycin pathway. J. Biol. Chem. 2011, 286:23132-23141.
64. Park J.H., Ryu J.M., Han H.J. Involvement of caveolin-1 in fibronectin-induced mouse embryonic stem cell proliferation: role of FAK, RhoA, PI3K/Akt, and ERK 1/2 pathways. J. Cell. Physiol. 2011, 226:267-275.
65. Paszek M.J., Zahir N., Johnson K.R., Lakins J.N., Rozenberg G.I., Gefen A., Reinhart-King C.A., Margulies S.S., Dembo M., Boettiger D., Hammer D.A., Weaver V.M. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005, 8:241-254.
66. Pitre A., Davis N., Paul M., Orr A.W., Skalli O. Synemin promotes AKT-dependent glioblastoma cell proliferation by antagonizing PP2A. Mol. Biol. Cell 2012, 23:1243-1253.
67. Popova S.N., Barczyk M., Tiger C.-F., Beertsen W., Zigrino P., Aszodi A., Miosge N., Forsberg E., Gullberg D. α11β1 integrin-dependent regulation of periodontal ligament function in the erupting mouse incisor. Mol. Cell. Biol. 2007, 27:4306-4316.
68. Raghavan S., Bauer C., Mundschau G., Li Q., Fuchs E. Conditional ablation of beta1 integrin in skin. Severe defects in epidermal proliferation, basement membrane formation, and hair follicle invagination. J. Cell Biol. 2000, 150:1149-1160.
69. Riopel M., Krishnamurthy M., Li J., Liu S., Leask A., Wang R. Conditional β1-integrin-deficient mice display impaired pancreatic β cell function. J. Pathol. 2011, 224:45-55.
70. Robinson S.D., Hodivala-Dilke K.M. The role of β3-integrins in tumor angiogenesis: context is everything. Curr. Opin. Cell Biol. 2011, 23:630-637.
71. Samuel M.S., Lopez J.I., McGhee E.J., Croft D.R., Strachan D., Timpson P., Munro J., Schröder E., Zhou J., Brunton V.G., Barker N., Clevers H., Sansom O.J., Anderson K.I., Weaver V.M., Olson M.F. Actomyosin-mediated cellular tension drives increased tissue stiffness and β-catenin activation to induce epidermal hyperplasia and tumor growth. Cancer Cell 2011, 19:776-791.
72. Schiller H.B., Hermann M.-R., Polleux J., Vignaud T., Zanivan S., Friedel C.C., Sun Z., Raducanu A., Gottschalk K.-E., Théry M., Mann M., Fässler R. β1- and αv-class integrins cooperate to regulate myosin II during rigidity sensing of fibronectin-based microenvironments. Nat. Cell Biol. 2013, 15:625-636.
73. Schittenhelm J., Schwab E.I., Sperveslage J., Tatagiba M., Meyermann R., Fend F., Goodman S.L., Sipos B. Longitudinal expression analysis of αv integrins in human gliomas reveals upregulation of integrin αvβ3 as a negative prognostic factor. J. Neuropathol. Exp. Neurol. 2013, 72:194-210.
74. Sen A., De Castro I., Defranco D.B., Deng F.-M., Melamed J., Kapur P., Raj G.V., Rossi R., Hammes S.R. Paxillin mediates extranuclear and intranuclear signaling in prostate cancer proliferation. J. Clin. Invest. 2012, 122:2469-2481.
75. Shanmugasundaram K., Block K., Nayak B.K., Livi C.B., Venkatachalam M.A., Sudarshan S. PI3K regulation of the SKP-2/p27 axis through mTORC2. Oncogene 2013, 32:2027-2036.
76. Shen Z., Ye Y., Kauttu T., Seppänen H., Vainionpää S., Wang S., Mustonen H., Puolakkainen P. Novel focal adhesion protein kindlin-2 promotes the invasion of gastric cancer cells through phosphorylation of integrin β1 and β3. J. Surg. Oncol. 2013, 108:106-112.
77. Singh P., Chen C., Pal-Ghosh S., Stepp M.A., Sheppard D., Van De Water L. Loss of integrin α9β1 results in defects in proliferation, causing poor re-epithelialization during cutaneous wound healing. J. Invest. Dermatol. 2009, 129:217-228.
78. Smith H.W., Marra P., Marshall C.J. uPAR promotes formation of the p130Cas-Crk complex to activate Rac through DOCK180. J. Cell Biol. 2008, 182:777-790.
79. Streuli C.H. Integrins and cell-fate determination. J. Cell Sci. 2009, 122:171-177.
80. Streuli C.H., Akhtar N. Signal co-operation between integrins and other receptor systems. Biochem. J. 2009, 418:491-506.
81. Su J.-L., Chiou J., Tang C.-H., Zhao M., Tsai C.-H., Chen P.-S., Chang Y.-W., Chien M.-H., Peng C.-Y., Hsiao M., Kuo M.-L., Yen M.-L. CYR61 regulates BMP-2-dependent osteoblast differentiation through the αvβ3 integrin/integrin-linked kinase/ERK pathway. J. Biol. Chem. 2010, 285:31325-31336.
82. Uberti B., Dentelli P., Rosso A., Defilippi P., Brizzi M.F. Inhibition of β1 integrin and IL-3Rβ common subunit interaction hinders tumour angiogenesis. Oncogene 2010, 29:6581-6590.
83. Villalonga P., Fernández de Mattos S., Ridley A.J. RhoE inhibits 4E-BP1 phosphorylation and eIF4E function impairing cap-dependent translation. J. Biol. Chem. 2009, 284:35287-35296.
84. Walker J.L., Assoian R.K. Integrin-dependent signal transduction regulating cyclin D1 expression and G1 phase cell cycle progression. Cancer Metastasis Rev. 2005, 24:383-393.
85. Wang P., Ballestrem C., Streuli C.H. The C terminus of talin links integrins to cell cycle progression. J. Cell Biol. 2011, 195:499-513.
86. Wang Y., Yao M., Zhou J., Zheng W., Zhou C., Dong D., Liu Y., Teng Z., Jiang Y., Wei G., Cui X. The promotion of neural progenitor cells proliferation by aligned and randomly oriented collagen nanofibers through β1 integrin/MAPK signaling pathway. Biomaterials 2011, 32:6737-6744.
87. Welsh C.F. Rho GTPases as key transducers of proliferative signals in g1 cell cycle regulation. Breast Cancer Res. Treat. 2004, 84:33-42.
88. Wernimont S.A., Wiemer A.J., Bennin D.A., Monkley S.J., Ludwig T., Critchley D.R., Huttenlocher A. Contact-dependent T cell activation and T cell stopping require talin1. J. Immunol. 2011, 187:6256-6267.
89. Wozniak M.A., Cheng C.Q., Shen C.J., Gao L., Olarerin-George A.O., Won K.-J., Hogenesch J.B., Chen C.S. Adhesion regulates MAP kinase/ternary complex factor exchange to control a proliferative transcriptional switch. Curr. Biol. 2012, 22:2017-2026.
90. Xie J.-W., Haslam S.Z. Extracellular matrix, Rac1 signaling, and estrogen-induced proliferation in MCF-7 breast cancer cells. Breast Cancer Res. Treat. 2008, 110:257-268.
91. Xie Y., McElwee K.J., Owen G.R., Häkkinen L., Larjava H.S. Integrin β6-deficient mice show enhanced keratinocyte proliferation and retarded hair follicle regression after depilation. J. Invest. Dermatol. 2012, 132:547-555.
92. Yan Y., Gong Y., Guo Y., Lv Q., Guo C., Zhuang Y., Zhang Y., Li R., Zhang X. Mechanical strain regulates osteoblast proliferation through integrin-mediated ERK activation. PLoS ONE 2012, 7:e35709.
93. Yang J.-Y., Zong C.S., Xia W., Yamaguchi H., Ding Q., Xie X., Lang J.-Y., Lai C.-C., Chang C.-J., Huang W.-C., Huang H., Kuo H.-P., Lee D.-F., Li L.-Y., Lien H.-C., Cheng X., Chang K.-J., Hsiao C.-D., Tsai F.-J., Tsai C.-H., Sahin A.A., Muller W.J., Mills G.B., Yu D., Hortobagyi G.N., Hung M.-C. ERK promotes tumorigenesis by inhibiting FOXO3a via MDM2-mediated degradation. Nat. Cell Biol. 2008, 10:138-148.
94. Yoshida T., Iwata T., Umemoto T., Shiratsuchi Y., Kawashima N., Sugiyama T., Yamato M., Okano T. Promotion of mouse ameloblast proliferation by Lgr5 mediated integrin signaling. J. Cell. Biochem. 2013, 114:2138-2147.
95. Yoshioka T., Otero J., Chen Y., Kim Y.-M., Koutcher J.A., Satagopan J., Reuter V., Carver B., de Stanchina E., Enomoto K., Greenberg N.M., Scardino P.T., Scher H.I., Sawyers C.L., Giancotti F.G. β4 Integrin signaling induces expansion of prostate tumor progenitors. J. Clin. Invest. 2013, 123:682-699.
96. Zaidel-Bar R., Itzkovitz S., Ma'ayan A., Iyengar R., Geiger B. Functional atlas of the integrin adhesome. Nat. Cell Biol. 2007, 9:858-867.
97. Zehorai E., Yao Z., Plotnikov A., Seger R. The subcellular localization of MEK and ERK-a novel nuclear translocation signal (NTS) paves a way to the nucleus. Mol. Cell. Endocrinol. 2010, 314:213-220.
98. Zhang X., Rozengurt E., Reed E.F. HLA class I molecules partner with integrin β4 to stimulate endothelial cell proliferation and migration. Sci. Signal. 2010, 3:ra85.
99. Zhang S., Huan W., Wei H., Shi J., Fan J., Zhao J., Shen A., Teng H. FOXO3a/p27kip1 expression and essential role after acute spinal cord injury in adult rat. J. Cell. Biochem. 2013, 114:354-365.
100. Zhao Z.-S., Manser E. PAK family kinases: physiological roles and regulation. Cell Logist. 2012, 2:59-68.