Integrin control of tumor invasion

Critical Reviews in Eukaryotic Gene Expression

Volumn 22, Issue 4, 2012, Pages 309-324

  Missan, Dara S ^a   DiPersio, C Michael ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

Author keywords

Cell adhesion; Extracellular matrix; Metastasis; Signal transduction

Indexed keywords

ALPHA6BETA4 INTEGRIN; CD51 ANTIGEN; CELL SURFACE PROTEIN; CILENGITIDE; ETARACIZUMAB; FOCAL ADHESION KINASE; INTEGRIN; INTEGRIN ALPHA7 BETA1; INTEGRIN ALPHA9 BETA1; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 1; VERY LATE ACTIVATION ANTIGEN 2; VERY LATE ACTIVATION ANTIGEN 3; VERY LATE ACTIVATION ANTIGEN 4; VERY LATE ACTIVATION ANTIGEN 5; VERY LATE ACTIVATION ANTIGEN 6; VOLOCIXIMAB;

ANGIOGENESIS; ARTICLE; CANCER CELL; CANCER INVASION; CARCINOGENESIS; CELL INVASION; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; INTRACELLULAR SIGNALING; MOLECULARLY TARGETED THERAPY; PRIORITY JOURNAL; PROTEIN FUNCTION; TUMOR PROMOTION;

ANIMALS; EXTRACELLULAR MATRIX; HUMANS; INTEGRINS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 84871594829     PISSN: 10454403     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevEukarGeneExpr.v22.i4.50     Document Type: Article

References (176)

1. Hynes RO, Zhao Q. The evolution of cell adhesion. J Cell Biol. 2000 Jul 24;150(2):F89-96.
2. Hynes RO. The extracellular matrix: not just pretty fibrils. Science. 2009 Nov 27;326(5957):1216-19.
3. Lu P, Weaver VM, Werb Z. The extracellular matrix: A dynamic niche in cancer progression. J Cell Biol. 2012 February 20, 2012;196(4):395-406.
4. McCawley LJ, Matrisian LM. Matrix metalloproteinases: they're not just for matrix anymore! Curr Opin Cell Biol. 2001 Oct;13(5):534-40.
5. Keely PJ. Mechanisms by which the extracellular matrix and integrin signaling act to regulate the switch between tumor suppression and tumor promotion. J Mammary Gland Biol Neoplasia. 2011 Sep;16(3):205-19.
6. Giancotti FG, Ruoslahti E. Integrin signaling. Science. 1999;285:1028-32.
7. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell. 2002 Sep 20;110(6):673-87.
8. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR. Cell migration: integrating signals from front to back. Science. 2003 Dec 5;302(5651):1704-9.
9. Delon I, Brown NH. Integrins and the actin cytoskeleton. Curr Opin Cell Biol. 2007 Feb;19(1):43-50.
10. Schwartz MA, Ginsberg MH. Networks and crosstalk: integrin signalling spreads. Nat Cell Biol. 2002 Apr;4(4):E65-68.
11. Harburger DS, Calderwood DA. Integrin signalling at a glance. J Cell Sci. 2009 Jan 15;122(Pt 2):159-63.
12. Salo T, Lyons JG, Rahemtulla F, Birkedal-Hansen H, Larjava H. Transforming growth factor-beta 1 up-regulates type IV collagenase expression in cultured human keratinocytes. J Biol Chem. 1991 Jun 25;266(18):11436-41.
13. Brakebusch C, Bouvard D, Stanchi F, Sakai T, Fassler R. Integrins in invasive growth. J Clin Invest. 2002 Apr;109(8):999-1006.
14. Felding-Habermann B. Integrin adhesion receptors in tumor metastasis. Clin Exp Metastasis. 2003;20(3):203-13.
15. Desgrosellier JS, Cheresh DA. Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer. 2010 Jan;10(1):9-22.
16. Brooks PC, Stromblad S, Sanders LC, von Schalscha TL, Aimes RT, Stetler-Stevenson WG, Quigley JP, Cheresh DA. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin avb3. Cell. 1996;85:683-93.
17. Ellerbroek SM, Fishman DA, Kearns AS, Bafetti LM, Stack MS. Ovarian carcinoma regulation of matrix metalloproteinase-2 and membrane type 1 matrix metalloproteinase through beta1 integrin. Cancer Res. 1999 Apr 1;59(7):1635-41.
18. Morini M, Mottolese M, Ferrari N, Ghiorzo F, Buglioni S, Mortarini R, Noonan DM, Natali PG, Albini A. The alpha 3 beta 1 integrin is associated with mammary carcinoma cell metastasis, invasion, and gelatinase B (MMP9) activity. Int J Cancer. 2000;87(3):336-42.
19. Thomas GJ, Lewis MP, Hart IR, Marshall JF, Speight PM. AlphaVbeta6 integrin promotes invasion of squamous carcinoma cells through up-regulation of matrix metalloproteinase-9. Int J Cancer. 2001;92(5):641-50.
20. Iyer V, Pumiglia K, DiPersio CM. α3β1 integrin regulates MMP-9 mRNA stability in immortalized keratinocytes: a novel mechanism of integrin-mediated MMP gene expression. J Cell Sci. 2005;118:1185-95.
21. Symowicz J, Adley BP, Gleason KJ, Johnson JJ, Ghosh S, Fishman DA, Hudson LG, Stack MS. Engagement of collagen-binding integrins promotes matrix metalloproteinase-9-dependent E-cadherin ectodomain shedding in ovarian carcinoma cells. Cancer Res. 2007 Mar 1;67(5):2030-39.
22. Gu X, Niu J, Dorahy DJ, Scott R, Agrez MV. Integrin alpha(v)beta6-associated ERK2 mediates MMP-9 secretion in colon cancer cells. Br J Cancer. 2002 Jul 29;87(3):348-51.
23. Han Q, Leng J, Bian D, Mahanivong C, Carpenter KA, Pan ZK, Han J, Huang S. Rac1-MKK3-p38-MAP-KAPK2 pathway promotes urokinase plasminogen activator mRNA stability in invasive breast cancer cells. J Biol Chem. 2002 Dec 13;277(50):48379-85.
24. Ghosh S, Johnson JJ, Sen R, Mukhopadhyay S, Liu Y, Zhang F, Wei Y, Chapman HA, Stack MS. Functional relevance of urinary-type plasminogen activator receptoralpha3beta1 integrin association in proteinase regulatory pathways. J Biol Chem. 2006 May 12;281(19):13021-29.
25. Ghosh S, Brown R, Jones JC, Ellerbroek SM, Stack MS. Urinary-type plasminogen activator (uPA) expression and uPA receptor localization are regulated by alpha 3beta 1 integrin in oral keratinocytes. J Biol Chem. 2000 Aug 4;275(31):23869-76.
26. Mulgrew K, Kinneer K, Yao XT, Ward BK, Damschroder MM, Walsh B, Mao SY, Gao C, Kiener PA, Coats S, Kinch MS, Tice DA. Direct targeting of alphavbeta3 integrin on tumor cells with a monoclonal antibody, Abegrin. Mol Cancer Ther. 2006 Dec;5(12):3122-29.
27. Wu H, Beuerlein G, Nie Y, Smith H, Lee BA, Hensler M, Huse WD, Watkins JD. Stepwise in vitro affinity maturation of Vitaxin, an alphav beta3-specific humanized mAb. Proc Natl Acad Sci U S A. 1998 May 26;95(11):6037-42.
28. Stupp R, Ruegg C. Integrin inhibitors reaching the clinic. J Clin Oncol. 2007 May 1;25(13):1637-38.
29. Rust WL, Carper SW, Plopper GE. The promise of integrins as effective targets for anticancer agents. J Biomed Biotechnol. 2002;2(3):124-30.
30. Goodman SL, Picard M. Integrins as therapeutic targets. Trends Pharmacol Sci. 2012;33(7):405-12.
31. Stipp CS. Laminin-binding integrins and their tetraspanin partners as potential antimetastatic targets. Expert Rev Mol Med. 2010;12:e3.
32. Mitchell K, Svenson KB, Longmate WM, Gkirtzimanaki K, Sadej R, Wang X, Zhao J, Eliopoulos AG, Berditchevski F, Dipersio CM. Suppression of integrin alpha3beta1 in breast cancer cells reduces cyclooxygenase-2 gene expression and inhibits tumorigenesis, invasion, and cross-talk to endothelial cells. Cancer Res. 2010 Aug 1;70(15):6359-67.
33. Wang H, Fu W, Im JH, Zhou Z, Santoro SA, Iyer V, DiPersio CM, Yu QC, Quaranta V, Al-Mehdi A, Muschel RJ. Tumor cell {alpha}3{beta}1 integrin and vascular laminin-5 mediate pulmonary arrest and metastasis. J Cell Biol. 2004 Mar 15;164(6):935-41.
34. Yang XH, Richardson AL, Torres-Arzayus MI, Zhou P, Sharma C, Kazarov AR, Andzelm MM, Strominger JL, Brown M, Hemler ME. CD151 accelerates breast cancer by regulating alpha 6 integrin function, signaling, and molecular organization. Cancer Res. 2008 May 1;68(9):3204-13.
35. Gupta SK, Oommen S, Aubry MC, Williams BP, Vlahakis NE. Integrin α9β1 promotes malignant tumor growth and metastasis by potentiating epithelial-mesenchymal transition. Oncogene. 2012 Feb 27. doi: 10.1038/ onc.2012.41. [Epub ahead of print].
36. 1 integrin is a metastasis suppressor in mouse models and human cancer. J Clin Invest. 2011 Jan;121(1):226-37.
37. Yue J, Zhang K, Chen J. Role of integrins in regulating proteases to mediate extracellular matrix remodeling. Cancer Microenviron. 2012 Dec;5(3):275-83.
38. Guo W, Giancotti FG. Integrin signalling during tumour progression. Nat Rev Mol Cell Biol. 2004 Oct;5(10):816-26.
39. Hood JD, Cheresh DA. Role of integrins in cell invasion and migration. Nat Rev Cancer. 2002 Feb;2(2):91-100.
40. Vicente-Manzanares M, Choi CK, Horwitz AR. Integrins in cell migration-the actin connection. J Cell Sci. 2009 Jan 15;122(Pt 2):199-206.
41. Friedl P, Wolf K. Plasticity of cell migration: a multiscale tuning model. J Cell Biol. 2010 Jan 11;188(1):11-19.
42. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell. 2010 Apr 2;141(1):52-67.
43. Murphy G. The ADAMs: signalling scissors in the tumour microenvironment. Nat Rev Cancer. 2008 Dec;8(12):929-41.
44. Lamar JM, Pumiglia KM, DiPersio CM. An immortalization-dependent switch in integrin function up-regulates MMP-9 to enhance tumor cell invasion. Cancer Res. 2008 Sep 15;68(18):7371-79.
45. Sugiura T, Berditchevski F. Function of alpha3beta1tetraspan protein complexes in tumor cell invasion. Evidence for the role of the complexes in production of matrix metalloproteinase 2 (MMP-2). J Cell Biol. 1999;146:1375-89.
46. Morozevich G, Kozlova N, Cheglakov I, Ushakova N, Berman A. Integrin alpha5beta1 controls invasion of human breast carcinoma cells by direct and indirect modulation of MMP-2 collagenase activity. Cell Cycle. 2009 Jul 15;8(14):2219-25.
47. Li DM, Feng YM. Signaling mechanism of cell adhesion molecules in breast cancer metastasis: potential therapeutic targets. Breast Cancer Res Treat. 2011 Jul;128(1):7-21.
48. Deryugina EI, Bourdon MA, Luo GX, Reisfeld RA, Strongin A. Matrix metalloproteinase-2 activation modulates glioma cell migration. J Cell Sci. 1997 Oct;110 (Pt 19):2473-82.
49. Rathinam R, Alahari SK. Important role of integrins in the cancer biology. Cancer Metastasis Rev. 2010 Mar;29(1):223-37.
50. Thomas GJ, Lewis MP, Hart IR, Marshall JF, Speight PM. AlphaVbeta6 integrin promotes invasion of squamous carcinoma cells through up-regulation of matrix metalloproteinase-9. Int J Cancer. 2001 Jun 1;92(5):641-50.
51. Zeng ZZ, Jia Y, Hahn NJ, Markwart SM, Rockwood KF, Livant DL. Role of focal adhesion kinase and phosphatidylinositol 3′-kinase in integrin fibronectin receptor-mediated, matrix metalloproteinase-1-dependent invasion by metastatic prostate cancer cells. Cancer Res. 2006 Aug 15;66(16):8091-99.
52. Jia Y, Zeng ZZ, Markwart SM, Rockwood KF, Ignatoski KM, Ethier SP, Livant DL. Integrin fibronectin receptors in matrix metalloproteinase-1-dependent invasion by breast cancer and mammary epithelial cells. Cancer Res. 2004 Dec 1;64(23):8674-81.
53. Stefanidakis M, Koivunen E. Cell-surface association between matrix metalloproteinases and integrins: role of the complexes in leukocyte migration and cancer progression. Blood. 2006 Sep 1;108(5):1441-50.
54. He Y, Liu XD, Chen ZY, Zhu J, Xiong Y, Li K, Dong JH, Li X. Interaction between cancer cells and stromal fibroblasts is required for activation of the uPAR-uPAMMP-2 cascade in pancreatic cancer metastasis. Clin Cancer Res. 2007 Jun 1;13(11):3115-24.
55. Barker HE, Chang J, Cox TR, Lang G, Bird D, Nicolau M, Evans HR, Gartland A, Erler JT. LOXL2-mediated matrix remodeling in metastasis and mammary gland involution. Cancer Res. 2011 Mar 1;71(5):1561-72.
56. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, Fong SF, Csiszar K, Giaccia A, Weninger W, Yamauchi M, Gasser DL, Weaver VM. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell. 2009 Nov 25;139(5):891-906.
57. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, Tanzawa K, Thorpe P, Itohara S, Werb Z, Hanahan D. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol. 2000;2(10):737-44.
58. Chang SH, Liu CH, Conway R, Han DK, Nithipatikom K, Trifan OC, Lane TF, Hla T. Role of prostaglandin E2-dependent angiogenic switch in cyclooxygenase 2-induced breast cancer progression. Proc Natl Acad Sci U S A. 2004 Jan 13;101(2):591-96.
59. Sadej R, Romanska H, Baldwin G, Gkirtzimanaki K, Novitskaya V, Filer AD, Krcova Z, Kusinska R, Ehrmann J, Buckley CD, Kordek R, Potemski P, Eliopoulos AG, Lalani el N, Berditchevski F. CD151 regulates tumorigenesis by modulating the communication between tumor cells and endothelium. Mol Cancer Res. 2009 Jun;7(6):787-98.
60. Janes SM, Watt FM. Switch from alphavbeta5 to alphav beta6 integrin expression protects squamous cell carcinomas from anoikis. J Cell Biol. 2004 Aug 2;166(3):419-31.
61. DiPersio CM, Shao M, Di Costanzo L, Kreidberg JA, Hynes RO. Mouse keratinocytes immortalized with large T antigen acquire a3b1 integrin-dependent secretion of MMP-9/gelatinase B. J Cell Sci. 2000;113:2909-21.
62. Jones PH, Harper S, Watt FM. Stem cell patterning and fate in human epidermis. Cell. 1995 Jan 13;80(1):83-93.
63. Choma DP, Pumiglia K, DiPersio CM. Integrin alpha-3beta1 directs the stabilization of a polarized lamellipodium in epithelial cells through activation of Rac1. J Cell Sci. 2004 Sep 1;117(Pt 17):3947-59.
64. Benitah SA, Frye M, Glogauer M, Watt FM. Stem cell depletion through epidermal deletion of Rac1. Science. 2005 Aug 5;309(5736):933-35.
65. Mercurio AM, Rabinovitz I, Shaw LM. The alpha 6 beta 4 integrin and epithelial cell migration. Curr Opin Cell Biol. 2001 Oct;13(5):541-45.
66. Lipscomb EA, Mercurio AM. Mobilization and activation of a signaling competent alpha6beta4integrin underlies its contribution to carcinoma progression. Cancer Metastasis Rev. 2005 Sep;24(3):413-23.
67. Litjens SH, de Pereda JM, Sonnenberg A. Current insights into the formation and breakdown of hemidesmosomes. Trends Cell Biol. 2006 Jul;16(7):376-83.
68. Carter WG, Kaur P, Gil SG, Gahr PJ, Wayner EA. Distinct functions for integrins a3b1 in focal adhesions and a6b4/bullous antigen in a new stable anchoring contact (SAC) of keratinocytes: relation to hemidesmosomes. J Cell Biol. 1990;111:3141-54.
69. Mercurio AM, Rabinovitz I. Towards a mechanistic understanding of tumor invasion--lessons from the alpha6beta 4 integrin. Semin Cancer Biol. 2001 Apr;11(2):129-41.
70. Rabinovitz I, Toker A, Mercurio AM. Protein kinase C-dependent mobilization of the alpha6beta4 integrin from hemidesmosomes and its association with actin-rich cell protrusions drive the chemotactic migration of carcinoma cells. J Cell Biol. 1999 Sep 6;146(5):1147-60.
71. Mariotti A, Kedeshian PA, Dans M, Curatola AM, Gagnoux-Palacios L, Giancotti FG. EGF-R signaling through Fyn kinase disrupts the function of integrin alpha6beta4 at hemidesmosomes: role in epithelial cell migration and carcinoma invasion. J Cell Biol. 2001 Oct 29;155(3):447-58.
72. Trusolino L, Bertotti A, Comoglio PM. A signaling adapter function for alpha6beta4 integrin in the control of HGF-dependent invasive growth. Cell. 2001 Nov 30;107(5):643-54.
73. Santoro MM, Gaudino G, Marchisio PC. The MSP receptor regulates alpha6beta4 and alpha3beta1 integrins via 14-3-3 proteins in keratinocyte migration. Dev Cell. 2003 Aug;5(2):257-71.
74. Mainiero F, Murgia C, Wary KK, Curatola AM, Pepe A, Blumenberhg M, Westwick JK, Der CJ, Giancotti FG. The coupling of a6b4 integrin to the Ras-MAP kinase pathways mediated by Shc controls keratinocyte proliferation. EMBO J. 1997;16:2365-75.
75. O'Connor KL, Nguyen BK, Mercurio AM. RhoA function in lamellae formation and migration is regulated by the alpha6beta4 integrin and cAMP metabolism. J Cell Biol. 2000 Jan 24;148(2):253-58.
76. Russell AJ, Fincher EF, Millman L, Smith R, Vela V, Waterman EA, Dey CN, Guide S, Weaver VM, Marinkovich MP. Alpha 6 beta 4 integrin regulates keratinocyte chemotaxis through differential GTPase activation and antagonism of alpha 3 beta 1 integrin. J Cell Sci. 2003 Sep 1;116(Pt 17):3543-56.
77. Schwartz MA, Ginsberg MH. Networks and crosstalk: integrin signalling spreads. Nat Cell Biol. 2002;4(4):E65-E68.
78. Playford MP, Schaller MD. The interplay between Src and integrins in normal and tumor biology. Oncogene. 2004 Oct 18;23(48):7928-46.
79. Brunton VG, Frame MC. Src and focal adhesion kinase as therapeutic targets in cancer. Curr Opin Pharmacol. 2008 Aug;8(4):427-32.
80. McLean GW, Carragher NO, Avizienyte E, Evans J, Brunton VG, Frame MC. The role of focal-adhesion kinase in cancer-a new therapeutic opportunity. Nat Rev Cancer. 2005 Jul;5(7):505-15.
81. Mitra SK, Schlaepfer DD. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol. 2006 Oct;18(5):516-23.
82. Zhao J, Guan JL. Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Rev. 2009 Jun;28(1-2):35-49.
83. McLean GW, Komiyama NH, Serrels B, Asano H, Reynolds L, Conti F, Hodivala-Dilke K, Metzger D, Chambon P, Grant SG, Frame MC. Specific deletion of focal adhesion kinase suppresses tumor formation and blocks malignant progression. Genes Dev. 2004 Dec 15;18(24):2998-3003.
84. Schaller MD, Hildebrand JD, Parsons JT. Complex for-mation with focal adhesion kinase: a mechanism to regulate activity and subcellular localization of Src kinases. Mol Biol Cell. 1999 Oct;10(10):3489-505.
85. Cary LA, Guan JL. Focal adhesion kinase in integrin mediated signaling. Front Biosci. 1999;4:D102-13.
86. Grille SJ, Bellacosa A, Upson J, Klein-Szanto AJ, van Roy F, Lee-Kwon W, Donowitz M, Tsichlis PN, Larue L. The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Res. 2003 May 1;63(9):2172-78.
87. Chattopadhyay N, Wang Z, Ashman LK, Brady-Kalnay SM, Kreidberg JA. alpha3beta1 integrin-CD151, a component of the cadherin-catenin complex, regulates PTPmu expression and cell-cell adhesion. J Cell Biol. 2003 Dec 22;163(6):1351-62.
88. Comoglio PM, Boccaccio C, Trusolino L. Interactions between growth factor receptors and adhesion molecules: breaking the rules. Curr Opin Cell Biol. 2003 Oct;15(5):565-71.
89. Porter JC, Hogg N. Integrins take partners: cross-talk between integrins and other membrane receptors. Trends Cell Biol. 1998 Oct;8(10):390-96.
90. Hemler ME. Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol. 2005 Oct;6(10):801-11.
91. Berditchevski F. Complexes of tetraspanins with integrins: more than meets the eye. J Cell Sci. 2001 Dec;114(Pt 23):4143-51.
92. Del Pozo MA, Schwartz MA. Rac, membrane heterogeneity, caveolin and regulation of growth by integrins. Trends Cell Biol. 2007 May;17(5):246-50.
93. Salanueva IJ, Cerezo A, Guadamillas MC, del Pozo MA. Integrin regulation of caveolin function. J Cell Mol Med. 2007 Sep-Oct;11(5):969-80.
94. Yauch RL, Berditchevsky F, Harler MB, Reichner J, Hemler ME. Highly stoichiometric, stable, and specific association of integrin a3b1 with CD151 provides a major link to phosphatidylinositol 4-kinase, and may regulate cell migration. Mol Biol Cell. 1998;9:2751-65.
95. Winterwood NE, Varzavand A, Meland MN, Ashman LK, Stipp CS. A critical role for tetraspanin CD151 in alpha3beta1 and alpha6beta4 integrin-dependent tumor cell functions on laminin-5. Mol Biol Cell. 2006 Jun;17(6):2707-21.
96. Li Q, Yang XH, Xu F, Sharma C, Wang HX, Knoblich K, Rabinovitz I, Granter SR, Hemler ME. Tetraspanin CD151 plays a key role in skin squamous cell carcinoma. Oncogene. 2012 Jul 23. doi: 10.1038/onc.2012.205. [Epub ahead of print].
97. Yang XH, Flores LM, Li Q, Zhou P, Xu F, Krop IE, Hemler ME. Disruption of laminin-integrin-CD151-focal adhesion kinase axis sensitizes breast cancer cells to ErbB2 antagonists. Cancer Res. 2010 Mar 15;70(6):2256-63.
98. Smith HW, Marshall CJ. Regulation of cell signalling by uPAR. Nat Rev Mol Cell Biol. 2010 Jan;11(1):23-36.
99. Smith HW, Marra P, Marshall CJ. uPAR promotes formation of the p130Cas-Crk complex to activate Rac through DOCK180. J Cell Biol. 2008 Aug 25;182(4):777-90.
100. Tang CH, Hill ML, Brumwell AN, Chapman HA, Wei Y. Signaling through urokinase and urokinase receptor in lung cancer cells requires interactions with beta1 integrins. J Cell Sci. 2008 Nov 15;121(Pt 22):3747-56.
101. Aguirre-Ghiso JA, Liu D, Mignatti A, Kovalski K, Ossowski L. Urokinase receptor and fibronectin regulate the ERK(MAPK) to p38(MAPK) activity ratios that determine carcinoma cell proliferation or dormancy in vivo. Mol Biol Cell. 2001 Apr;12(4):863-79.
102. Wei Y, Eble JA, Wang Z, Kreidberg JA, Chapman HA. Urokinase receptors promote beta1 integrin function through interactions with integrin alpha3beta1. Mol Biol Cell. 2001 Oct;12(10):2975-86.
103. Gilcrease MZ, Zhou X, Lu X, Woodward WA, Hall BE, Morrissey PJ. Alpha6beta4 integrin crosslinking induces EGFR clustering and promotes EGF-mediated Rho activation in breast cancer. J Exp Clin Cancer Res. 2009;28:67.
104. Guo W, Pylayeva Y, Pepe A, Yoshioka T, Muller WJ, Inghirami G, Giancotti FG. Beta 4 integrin amplifies ErbB2 signaling to promote mammary tumorigenesis. Cell. 2006 Aug 11;126(3):489-502.
105. ffrench-Constant C, Colognato H. Integrins: versatile integrators of extracellular signals. Trends Cell Biol. 2004 Dec;14(12):678-86.
106. Gilcrease MZ. Integrin signaling in epithelial cells. Cancer Lett. 2007 Mar 8;247(1):1-25.
107. Taipale J, Miyazono K, Heldin CH, Keski-Oja J. Latent transforming growth factor-beta 1 associates to fibroblast extracellular matrix via latent TGF-beta binding protein. J Cell Biol. 1994 Jan;124(1-2):171-81.
108. Sheppard D. Integrin-mediated activation of latent transforming growth factor beta. Cancer Metastasis Rev. 2005 Sep;24(3):395-402.
109. Munger JS, Huang X, Kawakatsu H, Griffiths MJ, Dalton SL, Wu J, Pittet JF, Kaminski N, Garat C, Matthay MA, Rifkin DB, Sheppard D. The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell. 1999 Feb 5;96(3):319-28.
110. Annes JP, Chen Y, Munger JS, Rifkin DB. Integrin alphaVbeta6-mediated activation of latent TGF-beta requires the latent TGF-beta binding protein-1. J Cell Biol. 2004 Jun 7;165(5):723-34.
111. McCawley LJ, Matrisian LM. Tumor progression: defining the soil round the tumor seed. Curr Biol. 2001;11(1):R25-27.
112. Gailit J, Welch MP, Clark RA. TGF-beta 1 stimulates expression of keratinocyte integrins during re-epithelialization of cutaneous wounds. J Invest Dermatol. 1994 Aug;103(2):221-27.
113. Zambruno G, Marchisio PC, Marconi A, Vaschieri C, Melchiori A, Giannetti A, De Luca M. Transforming growth factor-beta 1 modulates beta 1 and beta 5 integrin receptors and induces the de novo expression of the alpha v beta 6 heterodimer in normal human keratinocytes: implications for wound healing. J Cell Biol. 1995;129(3):853-65.
114. Giannelli G, Fransvea E, Marinosci F, Bergamini C, Colucci S, Schiraldi O, Antonaci S. Transforming growth factor-beta1 triggers hepatocellular carcinoma invasiveness via alpha3beta1 integrin. Am J Pathol. 2002 Jul;161(1):183-93.
115. Decline F, Okamoto O, Mallein-Gerin F, Helbert B, Bernaud J, Rigal D, Rousselle P. Keratinocyte motility induced by TGF-beta1 is accompanied by dramatic changes in cellular interactions with laminin 5. Cell Motil Cytoskeleton. 2003 Jan;54(1):64-80.
116. Galliher AJ, Schiemann WP. Src phosphorylates Tyr284 in TGF-beta type II receptor and regulates TGF-beta stimulation of p38 MAPK during breast cancer cell proliferation and invasion. Cancer Res. 2007 Apr 15;67(8):3752-58.
117. Jeong HW, Kim IS. TGF-beta1 enhances betaig-h3-mediated keratinocyte cell migration through the alpha3beta1 integrin and PI3K. J Cell Biochem. 2004 Jul 1;92(4):770-80.
118. Reynolds LE, Conti FJ, Silva R, Robinson SD, Iyer V, Rudling R, Cross B, Nye E, Hart IR, Dipersio CM, Hodivala-Dilke KM. alpha3beta1 integrin-controlled Smad7 regulates reepithelialization during wound healing in mice. J Clin Invest. 2008 Mar 3;118(3):965-74.
119. Margadant C, Sonnenberg A. Integrin-TGF-beta cross-talk in fibrosis, cancer and wound healing. EMBO Rep. 2010 Feb;11(2):97-105.
120. Lamar JM, Iyer V, DiPersio CM. Integrin alpha3beta1 potentiates TGFbeta-mediated induction of MMP-9 in immortalized keratinocytes. J Invest Dermatol. 2008 Mar;128(3):575-86.
121. Wick W, Platten M, Weller M. Glioma cell invasion: regulation of metalloproteinase activity by TGF-beta. J Neurooncol. 2001 Jun;53(2):177-85.
122. Cai T, Lei QY, Wang LY, Zha XL. TGF-beta 1 modulated the expression of alpha 5 beta 1 integrin and integrin-mediated signaling in human hepatocarcinoma cells. Biochem Biophys Res Commun. 2000 Aug 2;274(2):519-25.
123. Giannelli G, Fransvea E, Marinosci F, Bergamini C, Colucci S, Schiraldi O, Antonaci S. Transforming growth factor-β1 triggers hepatocellular carcinoma invasiveness via α3β1 integrin. Am J Pathol. 2002;161(1):183-93.
124. Pedersen P-H, Ness GO, Engebraaten O, Bjerkvig R, Lillehaug JR, Laerum OD. Heterogeneous response to the growth factors [EGF, PDGF (bb), TGF-α, bFGF, IL2] on glioma spheroid growth, migration and invasion. Int J Cancer. 1994;56(2):255-61.
125. Zeigler ME, Dutcheshen NT, Gibbs DF, Varani J. Growth factor-induced epidermal invasion of the dermis in human skin organ culture: expression and role of matrix metalloproteinases. Invasion Metastasis. 1996;16(1):11-18.
126. Zeigler ME, Krause S, Karmiol S, Varani J. Growth factor-induced epidermal invasion of the dermis in human skin organ culture: dermal invasion correlated with epithelial cell motility. Invasion Metastasis. 1996;16(1):3-10.
127. Mercurio AM, Bachelder RE, Bates RC, Chung J. Autocrine signaling in carcinoma: VEGF and the α6β4 integrin. Semin Cancer Biol. 2004;14(2):115-22.
128. Huhtala P, Humphries MJ, McCarthy JB, Tremble P, Werb Z, Damsky CH. Cooperative signalling by a5b1 and a4b1 integrins regulates metalloproteinase gene expression in fibroblasts adhering to fibronectin. J Cell Biol. 1995;129:867-79.
129. Khabar KS. Post-transcriptional control during chronic inflammation and cancer: a focus on AU-rich elements. Cell Mol Life Sci. 2010 Sep;67(17):2937-55.
130. Hitti E, Khabar KS. Sequence variations affecting AU-rich element function and disease. Front Biosci. 2012;17:1846-60.
131. Subbaram S, Kuentzel M, Frank D, Dipersio CM, Chittur SV. Determination of alternate splicing events using the Affymetrix Exon 1.0 ST arrays. Methods Mol Biol. 2010;632:63-72.
132. Lapuk A, Marr H, Jakkula L, Pedro H, Bhattacharya S, Purdom E, Hu Z, Simpson K, Pachter L, Durinck S, Wang N, Parvin B, Fontenay G, Speed T, Garbe J, Stampfer M, Bayandorian H, Dorton S, Clark TA, Schweitzer A, Wyrobek A, Feiler H, Spellman P, Conboy J, Gray JW. Exon-level microarray analyses identify alternative splicing programs in breast cancer. Mol Cancer Res. 2010 Jul;8(7):961-74.
133. Dutertre M, Lacroix-Triki M, Driouch K, de la Grange P, Gratadou L, Beck S, Millevoi S, Tazi J, Lidereau R, Vagner S, Auboeuf D. Exon-based clustering of murine breast tumor transcriptomes reveals alternative exons whose expression is associated with metastasis. Cancer Res. 2010 Feb 1;70(3):896-905.
134. Gerson KD, Shearstone JR, Maddula VS, Seligmann BE, Mercurio AM. Integrin beta4 regulates SPARC protein to promote invasion. J Biol Chem. 2012 Mar 23;287(13):9835-44.
135. Gerson KD, Krishna Maddula VSR, Seligmann BE, Shearstone JR, Khan A, Mercurio AM. Effects of β4 integrin expression on microRNA patterns in breast cancer. Biology Open. 2012 July 15;658-66.
136. Schmidhauser C, Bissell MJ, Myers CA, Casperson GF. Extracellular matrix and hormones transcriptionally regulate bovine beta-casein 5′ sequences in stably transfected mouse mammary cells. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9118-22.
137. DiPersio CM, Jackson DA, Zaret KS. The extracellular matrix coordinately modulates liver transcription factors and hepatocyte morphology. Mol Cell Biol. 1991;11:4405-14.
138. Sitrin RG, Pan PM, Srikanth S, Todd RF, 3rd. Fibrinogen activates NF-kappa B transcription factors in mononuclear phagocytes. J Immunol. 1998 Aug 1;161(3):1462-70.
139. Xiao G, Wang D, Benson MD, Karsenty G, Franceschi RT. Role of the alpha2-integrin in osteoblast-specific gene expression and activation of the Osf2 transcription factor. J Biol Chem. 1998 Dec 4;273(49):32988-94.
140. Shi C, Zhang X, Chen Z, Sulaiman K, Feinberg MW, Ballantyne CM, Jain MK, Simon DI. Integrin engagement regulates monocyte differentiation through the forkhead transcription factor Foxp1. J Clin Invest. 2004 Aug;114(3):408-18.
141. Wang GJ, Collinge M, Blasi F, Pardi R, Bender JR. Posttranscriptional regulation of urokinase plasminogen activator receptor messenger RNA levels by leukocyte integrin engagement. Proc Natl Acad Sci U S A. 1998 May 26;95(11):6296-301.
142. Wang JG, Collinge M, Ramgolam V, Ayalon O, Fan XC, Pardi R, Bender JR. LFA-1-dependent HuR nuclear export and cytokine mRNA stabilization in T cell activation. J Immunol. 2006 Feb 15;176(4):2105-13.
143. Peng SS, Chen CY, Xu N, Shyu AB. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 1998 Jun 15;17(12):3461-70.
144. Fan XC, Steitz JA. Overexpression of HuR, a nuclearcytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 1998 Jun 15;17(12):3448-60.
145. Sirenko OI, Lofquist AK, DeMaria CT, Morris JS, Brewer G, Haskill JS. Adhesion-dependent regulation of an A+U-rich element-binding activity associated with AUF1. Mol Cell Biol. 1997 Jul;17(7):3898-906.
146. Retta SF, Cassara G, D'Amato M, Alessandro R, Pellegrino M, Degani S, De Leo G, Silengo L, Tarone G. Cross talk between beta(1) and alpha(V) integrins: beta(1) affects beta(3) mRNA stability. Mol Biol Cell. 2001 Oct;12(10):3126-38.
147. Winzen R, Kracht M, Ritter B, Wilhelm A, Chen CY, Shyu AB, Muller M, Gaestel M, Resch K, Holtmann H. The p38 MAP kinase pathway signals for cytokine induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J. 1999 Sep 15;18(18):4969-80.
148. Pages G, Berra E, Milanini J, Levy AP, Pouyssegur J. Stress-activated protein kinases (JNK and p38/HOG) are essential for vascular endothelial growth factor mRNA stability. J Biol Chem. 2000 Aug 25;275(34):26484-91.
149. Yang X, Wang W, Fan J, Lal A, Yang D, Cheng H, Gorospe M. Prostaglandin A2-mediated stabilization of p21 mRNA through an ERK-dependent pathway requiring RNA-binding protein HuR. J Biol Chem. 2004 Sep 14;279(47):49298-306.
150. Lasa M, Mahtani KR, Finch A, Brewer G, Saklatvala J, Clark AR. Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol Cell Biol. 2000 Jun;20(12):4265-74.
151. Montero L, Nagamine Y. Regulation by p38 mitogen-activated protein kinase of adenylate and uridylaterich element-mediated urokinase-type plasminogen activator (uPA) messenger RNA stability and uPA-dependent in vitro cell invasion. Cancer Res. 1999 Oct 15;59(20):5286-93.
152. Bromann PA, Korkaya H, Webb CP, Miller J, Calvin TL, Courtneidge SA. Platelet-derived growth factor stimulates Src-dependent mRNA stabilization of specific early gene in fibroblasts. J Biol Chem. 2005 Mar 18;280(11):10253-63.
153. Brennan CM, Steitz JA. HuR and mRNA stability. Cell Mol Life Sci. 2001 Feb;58(2):266-77.
154. Lebwohl DE, Muise-Helmericks R, Sepp-Lorenzino L, Serve S, Timaul M, Bol R, Borgen P, Rosen N. A truncated cyclin D1 gene encodes a stable mRNA in a human breast cancer cell line. Oncogene. 1994 Jul;9(7):1925-29.
155. Dixon DA, Tolley ND, King PH, Nabors LB, McIntyre TM, Zimmerman GA, Prescott SM. Altered expression of the mRNA stability factor HuR promotes cyclooxy-genase-2 expression in colon cancer cells. J Clin Invest. 2001 Dec;108(11):1657-65.
156. Akool el S, Kleinert H, Hamada FM, Abdelwahab MH, Forstermann U, Pfeilschifter J, Eberhardt W. Nitric oxide increases the decay of matrix metalloproteinase 9 mRNA by inhibiting the expression of mRNA-stabilizing factor HuR. Mol Cell Biol. 2003 Jul;23(14):4901-16.
157. Sehgal I, Thompson TC. Novel regulation of type IV collagenase (matrix metalloproteinase-9 and -2) activities by transforming growth factor-beta1 in human prostate cancer cell lines. Mol Biol Cell. 1999;10(2):407-16.
158. Han Q, Leng J, Bian D, Mahanivong C, Carpenter KA, Pan ZK, Han J, Huang S. Rac1-MKK3-p38-MAPKAPK2 pathway promotes urokinase plasminogen activator mRNA stability in invasive breast cancer cells. J Biol Chem. 2002 December 13, 2002;277(50):48379-85.
159. Ebert MS, Sharp PA. Roles for microRNAs in conferring robustness to biological processes. Cell. 2012 Apr 27;149(3):515-24.
160. Moore AE, Young LE, Dixon DA. MicroRNA and AUrich element regulation of prostaglandin synthesis. Cancer Metastasis Rev. 2011 Dec;30(3-4):419-35.
161. Fabian MR, Sonenberg N, Filipowicz W. Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem. 2010;79:351-79.
162. von Roretz C, Gallouzi IE. Decoding ARE-mediated decay: is microRNA part of the equation? J Cell Biol. 2008 Apr 21;181(2):189-94.
163. Burke PA, DeNardo SJ, Miers LA, Lamborn KR, Matzku S, DeNardo GL. Cilengitide targeting of alpha(v)beta(3) integrin receptor synergizes with radioimmunotherapy to increase efficacy and apoptosis in breast cancer xenografts. Cancer Res. 2002 Aug 1;62(15):4263-72.
164. Albert JM, Cao C, Geng L, Leavitt L, Hallahan DE, Lu B. Integrin alpha v beta 3 antagonist Cilengitide enhances efficacy of radiotherapy in endothelial cell and non small-cell lung cancer models. Int J Radiat Oncol Biol Phys. 2006 Aug 1;65(5):1536-43.
165. Tentori L, Dorio AS, Muzi A, Lacal PM, Ruffini F, Navarra P, Graziani G. The integrin antagonist cilengitide increases the antitumor activity of temozolomide against malignant melanoma. Oncol Rep. 2008 Apr;19(4):1039-43.
166. Stoeltzing O, Liu W, Reinmuth N, Fan F, Parry GC, Parikh AA, McCarty MF, Bucana CD, Mazar AP, Ellis LM. Inhibition of integrin alpha5beta1 function with a small peptide (ATN-161) plus continuous 5-FU infusion reduces colorectal liver metastases and improves survival in mice. Int J Cancer. 2003 Apr 20;104(4):496-503.
167. Menendez JA, Vellon L, Mehmi I, Teng PK, Griggs DW, Lupu R. A novel CYR61-triggered 'CYR61-alphavbeta3 integrin loop' regulates breast cancer cell survival and chemosensitivity through activation of ERK1/ ERK2 MAPK signaling pathway. Oncogene. 2005 Jan 27;24(5):761-79.
168. Abdollahi A, Griggs DW, Zieher H, Roth A, Lipson KE, Saffrich R, Grone HJ, Hallahan DE, Reisfeld RA, Debus J, Niethammer AG, Huber PE. Inhibition of alpha(v) beta3 integrin survival signaling enhances antiangiogenic and antitumor effects of radiotherapy. Clin Cancer Res. 2005 Sep 1;11(17):6270-79.
169. Tucker GC. Integrins: molecular targets in cancer therapy. Curr Oncol Rep. 2006 Mar;8(2):96-103.
170. Nabors LB, Mikkelsen T, Rosenfeld SS, Hochberg F, Akella NS, Fisher JD, Cloud GA, Zhang Y, Carson K, Wittemer SM, Colevas AD, Grossman SA. Phase I and correlative biology study of cilengitide in patients with recurrent malignant glioma. J Clin Oncol. 2007 May 1, 2007;25(13):1651-57.
171. Reynolds AR, Hart IR, Watson AR, Welti JC, Silva RG, Robinson SD, Da Violante G, Gourlaouen M, Salih M, Jones MC, Jones DT, Saunders G, Kostourou V, PerronSierra F, Norman JC, Tucker GC, Hodivala-Dilke KM. Stimulation of tumor growth and angiogenesis by low concentrations of RGD-mimetic integrin inhibitors. Nat Med. 2009 Apr;15(4):392-400.
172. Weller M, Reardon D, Nabors B, Stupp R. Will integrin inhibitors have proangiogenic effects in the clinic?. Nat Med. 2009 Jul;15(7):726; author reply 7.
173. Mitchell K, Szekeres C, Milano V, Svenson KB, Nilsen-Hamilton M, Kreidberg JA, DiPersio CM. Alpha3beta1 integrin in epidermis promotes wound angiogenesis and keratinocyte-to-endothelial-cell crosstalk through the induction of MRP3. J Cell Sci. 2009 Jun 1;122(Pt 11):1778-87.
174. da Silva RG, Tavora B, Robinson SD, Reynolds LE, Szekeres C, Lamar J, Batista S, Kostourou V, Germain MA, Reynolds AR, Jones DT, Watson AR, Jones JL, Harris A, Hart IR, Iruela-Arispe ML, Dipersio CM, Kreidberg JA, Hodivala-Dilke KM. Endothelial alpha3beta1-integrin represses pathological angiogenesis and sustains endothelial-VEGF. Am J Pathol. 2010 Sep;177(3):1534-48.
175. Alexis F, Basto P, Levy-Nissenbaum E, Radovic-Moreno AF, Zhang L, Pridgen E, Wang AZ, Marein SL, Westerhof K, Molnar LK, Farokhzad OC. HER-2-targeted nanoparticle-affibody bioconjugates for cancer therapy. ChemMedChem. 2008;3(12):1839-43.
176. Arosio D, Casagrande C, Manzoni L. Integrin-mediated drug delivery in cancer and cardiovascular diseases with peptide-functionalized nanoparticles. Curr Med Chem. 2012 Jul 1;19(19):3128-51.