Integrin-mediated adhesion: Tipping the balance between chemosensitivity and chemoresistance

Advances in Experimental Medicine and Biology

Volumn 608, Issue , 2007, Pages 87-100

  Zutter, Mary M ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRIN;

APOPTOSIS; BREAST TUMOR; CELL ADHESION; CELL PROLIFERATION; DRUG RESISTANCE; EXTRACELLULAR MATRIX; FEMALE; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PHYSIOLOGY; REVIEW;

APOPTOSIS; BREAST NEOPLASMS; CELL ADHESION; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; EXTRACELLULAR MATRIX; FEMALE; HUMANS; INTEGRINS;

EID: 38449113305     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-0-387-74039-3_6     Document Type: Review

References (165)

1. Loftus JC, Smith JW, Ginsberg MH. Integrin-mediated cell adhesion: The extracellular face. J Biol Chem 1994;269(41):25235-25238.
2. Hood JD, Cheresh DA. Role of integrins in cell invasion and migration. Nat Rev Cancer 2002;2(2):91-100.
3. Guo W, Giancotti FG. Integrin signalling during tumour progression. Nat Rev Mol Cell Biol 2000;5(10):816-826.
4. Hynes RO. Cell adhesion: Old and new questions. Trends Cell Biol 1999;9(12):M33-M37.
5. Gustafsson E, Fassler R. Insights into extracellular matrix functions from mutant mouse models. Exp Cell Res 2000;261(1):52-68.
6. Hynes RO. A reevaluation of integrins as regulators of angiogenesis. Nat Med 2002;8(9):918-921.
7. Tucker GC. Inhibitors of integrins. Current Opinion in Pharmacology 2002;2:394-401.
8. Damiano JS. Integrins as novel drug targets for overcoming innate drug resistance. Curr Cancer Drug Targets 2002;2(1):37-43.
9. Longley DB, Johnston PG. Molecular mechanisms of drug resistance. J Pathology 2005;205:275-292.
10. Zutter MM, Sun H, Santoro S. Altered integrin expression and the malignant phenotype: The contribution of multiple integrated integrin receptors. J Mammary Gland Biol Neoplasia 1998;3(2):191-200.
11. Hynes RO. Integrins: Bidirectional, allosteric signaling machines. Cell 2002;110(6):673-687.
12. Hynes RO, Zhao Q. The evolution of cell adhesion. J Cell Biol 2000;150(2):F89-F96.
13. Clark EA, Brugge JS. Integrins and signal transduction pathways: The road taken. Science 1995;268(5208):233-239.
14. Liddington RC, Ginsberg MH. Integrin activation takes shape. J Cell Biol 2002;158(5):833-839.
15. Giancotti FG, Rouslahti E. Integrin signaling. Science 1999;285:1028-1032.
16. Wary KK, Mainiero F, Isakoff SJ et al. The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell 1996;87(4):733-743.
17. Wary KK, Mariotti A, Zurzolo C et al. A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 1998;94(5):625-634.
18. Guan JL, Shalloway D. Regulation of focal adhesion-associated protein tyrosine kinase by both cellular adhesion and oncogenic transformation. Nature 199; 358(6388):690-692.
19. Schaller MD, Borgman CA, Cobb BS et al. pp125FAK a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc Natl Acad Sci USA 1992;89(11):5192-5196.
20. Schaller MD, Parsons JT. Focal adhesion kinase and associated proteins. Curr Opin Cell Biol 1994;6(5):705-710.
21. Hannigan GE, Leung-Hagesteijn C, Fitz-Gibbon L et al. Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature 1996;379(6560):91-96.
22. Dedhar S, Hannigan GE. Integrin cytoplasmic interactions and bidirectional transmembrane signalling. Curr Opin Cell Biol 1996;8(5):657-669.
23. Lewis JM, Baskaran R, Taagepera S et al. Integrin regulation of c-Abl tyrosine kinase activity and cytoplasmic-nuclear transport. Proc Natl Acad Sci USA 1996;93(26):15174-15179.
24. Delcommenne M, Tan C, Gray V et al. Phosphoinositide-3-OH kinase-dependent regulation of glycogen synthase kinase 3 and protein kinase B/AKT by the integrin-linked kinase. Proc Natl Acad Sci USA 1998;95(19):11211- 11216.
25. Schaller MD, Hildebrand JD, Parsons JT. Complex formation with focal adhesion kinase: A mechanism to regulate activity and subcellular localization of Src kinases. Mol Biol Cell 1999;10(10):3489-3505.
26. Schlaepfer DD, Hanks SK, Hunter T et al. Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature 1994;372(6508):786-791.
27. Richardson A, Parsons T. A mechanism for regulation of the adhesion-associated proteintyrosine kinase pp125FAK. Nature 1996;380(6574):538- 450
28. (Erratum in Nature 1996;381(6585):810).
29. Vuori K, Hirai H, Aizawa S et al. Introduction of p130cas signaling complex formation upon integrin-mediated cell adhesion: A role for Src family kinases. Mol Cell Biol 1996;16(6):2606-2613.
30. Frisch SM, Vuori K, Ruoslahti E et al. Control of adhesion-dependent cell survival by focal adhesion kinase. J Cell Biol 1996;134(3):793-799.
31. Schlaepfer DD, Broome MA, Hunter T. Fibronectin-stimulated signaling from a focal adhesion kinase-c-Src complex: Involvement of the Grb2, p130cas, and Nck adaptor proteins. Mol Cell Biol 1997;17(3):1702-1713.
32. Oktay M, Wary KK, Dans M et al. Integrin-mediated activation of focal adhesion kinase is required for signaling to Jun. NH2-terminal kinase and progression through the G1 phase of the cell cycle. J Cell Biol 1999;145(7):1461-1469.
33. Chen HC, Appeddu PA, Parsons JT et al. Interaction of focal adhesion kinase with cytoskeletal protein talin. J Biol Chem 1995;270(28):16995-16999.
34. Berditchevski F, Chang S, Bodorova J et al. A novel link between integrins, transmembrane-4 superfamily proteins (CD63 and CD81), and phosphatidylinositol 4-kinase. J Biol Chem 1997;272(5):2595-2598.
35. Lindberg FP, Gresham HD, Schwarz E et al. Molecular cloning of integrin-associated protein: An immunoglobulin family member with multiple membrane-spanning domains implicated in alpha v beta 3-dependent ligand binding. J Cell Biol 1993;123(2):485-496.
36. Chung J, Gao A, Frazier WA. Thrombspondin acts via integrin-associated protein to activate the platelet integrin alphaIIbbeta3. J Biol Chem 1997;272(23):14740-14746.
37. Rojiani MV, Finlay BB, Gray V et al. In vitro interaction of a polypeptide homologous to human Ro/SS-A antigen (calreticulin) with a highly conserved amino acid sequence in the cytoplasmic domain of integrin alpha subunits. Biochemistry 1991;30(41):9859-9866.
38. Kieffer JD, Plopper G, Ingber DE et al. Direct binding of F actin to the cytoplasmic domain of the alpha 2 integrin chain in vitro. Biochem Biophys Res Commun 1995;217(2):466-474.
39. Liu S, Thomas SM, Woodside DG et al. Binding of paxillin to alpha4 integrins modifies integrin-dependent biological responses. Nature 1999;402(6762):676-681.
40. Alahari SK, Lee JW, Juliano RL. Nischarin, a novel protein that interacts with the integrin alpha5 subunit and inhibits cell migration. J Cell Biol 2000;151(6):1141-1154.
41. Wixler V, Laplantine E, Geerts D et al. Identification of novel interaction partners for the conserved membrane proximal region of alpha-integrin cytoplasmic domains. FEBS Lett 1999;445(2-3): 351-355.
42. Hannigan GE, Leung-Hagesteijn C, Fitz-Gibbon L et al. Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature 1996;379(6560):91-96.
43. Nikolopoulos SN, Turner CE. Molecular dissection of actopaxin-integrin- linked kinase-paxillin interactions and their role in subcellular localization. J Biol Chem 2002;277:1568-1575.
44. Nikolopoulos SN, Turner CE. Integrin-linked kinase (ILK) binding to paxillin LD1 motif regulates ILK localization to focal adhesions. J Biol Chem 2001;276(26):23499-23505.
45. Olski TM, Noegel AA, Korenbaum E. Parvin: A 42-kDa focal adhesion protein, related to the alpha-actinin superfamily. J Cell Sci 2001;114:525-538.
46. Tu Y, Huang Y, Zhang Z et al. A new focal adhesion protein that interacts with integrin-linked kinase and regulates cell adhesion and spreading. J Cell Biol 2001;153:585-598.
47. Dedhar S. Cell-substrate interactions and signaling through ILK. Curr Opin Cell Biol 2000;12:250-256.
48. Radeva G, Petrocelli T, Behrend E et al. Overexpression of the integrin-linked kinase promotes anchorage-independent cell cycle progression. J Biol Chem 1997;272:13937-13944.
49. Attwell S, Roskelley C, Dedhar S. The integrin-linked kinase (ILK) suppresses anoikis. Oncogene 2000;19:3811-3815.
50. Bottazzi MC, Assoian RK. The extracellular matrix and mitogenic growth factors control G1 phase cyclins and cyclin-dependent kinsae inhibitors. Trends Cell Biol 1997;7:348-352.
51. Albanese C, Johnson J, Watanabe G et al. Transforming p21ras mutants and c-Ets-2 activate the cyclin D1 promoter through distinguishable regions. J Biol Chem 1995;270(40):23589-23597.
52. Aplin AE, Howe AK, Juliano RL. Cell adhesion molecules, signal transduction and cell growth. Curr Opin Cell Biol 1999;11(6):737-744.
53. Howe AK, Aplin AE, Juliano RL. Anchorage-dependent ERK signaling-mechanisms and consequences. Curr Opin Genet Dev 2000;12(1):30-35.
54. Koyama H, Raines EW, Bornfeldt KE et al. Fibrillar collagen inhibits arterial smooth muscle proliferation through regulation of Cdk2 inhibitors. Cell 1996;87(6):1069-1078.
55. Fang F, Orend G, Watanabe N et al. Dependence of cyclin E-CDK2 kinase activity on cell anchorage. Science 1996;271(5248):499-502.
56. Zhu X, Ohtsubo M, Bohmer RM et al. Adhesion-dependent cell cycle progression linked to the expression of cyclin D1, activation of cyclin E-cdk2, and phosphorylation of the retinoblastoma protein. J Cell Biol 1996;133(2):391-403.
57. Assoian RK. Anchorage-dependent cell cycle progression. J Cell Biol 1997;136(1):1-4.
58. Assoian RK. Common sense signalling. Nat Cell Biol 2002;4(8):E187-E188.
59. Sherr CJ, Roberts JM. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev 1995;9(10):1149-1163.
60. Frisch SM, Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 1994;124(4):619-626.
61. Meredith Jr JE, Fazeli B, Schwartz MA. The extracellular matrix as a cell survival factor. Mol Biol Cell 1993;4(9):953-961.
62. Lewis JM, Truong TN, Schwartz MA. Integrins regulate the apoptotic response to DNA damage through modulation of p53. Proc Natl Acad Sci USA 2002;99(6):3627-3632.
63. Yawata A, Adachi M, Okuda H et al. Prolonged cell survival enhances peritoneal dissemination of gastric cancer cells. Oncogene 1999;16:2681-2686.
64. Streuli CH, Gilmore AP. Adhesion-mediated signaling in the regulation of mammary epithelial cell survival. J Mammary Gland Biol Neoplasia 1999;4:183-191.
65. Shanmugathasan M, Jothy S. Apoptosis, anoikis and their relevance to the pathobiology of colon cancer. Pathol Int 2000;50:273-279.
66. Wei L, Yang Y, Yu Q. Tyrosine kinase-dependent P13-kinase and mitogen-activated protein-kinase-independent signaling pathways prevent lung adenocarcinoma anoikis. Cancer Res 2001;61:2439-2444.
67. Frisch SM, Screaton RA. Anoikis mechanisms. Curr Opin Cell Biol 2001;13(5):555-562.
68. Martin SS, Vuori K. Regulation of Bcl-2 proteins during anoikis and amorphosis. Biochim Biophys Acta 2004;1692(2-3): 145-157.
69. Matter ML, Ruoslahti E. A signaling pathway from the alpha5beta1 and alpha (v) beta3 integrins that elevates bcl-2 transcription. J Biol Chem 2001;276:27757-27763.
70. Zhang Z, Vuori K, Reed JC et al. The alpha 5 beta 1 integrin supports survival of cells on fibronectin and up-regulates Bcl-2 expression. Proc Natl Acad Sci USA 1995;92:6161-6165.
71. Scheid MP, Duronio V. Dissociation of cytokine-induced phosphorylation of Bad and activation of PKB/akt: Involvement of MEK upstream of Bad phosphorylation. Proc Natl Acad Sci USA 1998;95:7439-7444.
72. Scheid MP, Schubert KM, Duronio V. Regulation of bad phosphorylation and association with Bcl-x (L) by the MAPK/Erk kinase. J Biol Chem 1999;274:31108-31113.
73. Breitschopf K, Haendeler J, Malchow P et al. Posttranslational modification of Bcl-2 facilitates its proteasome-dependent degradation: Molecular characterization of the involved signaling pathway. Mol Cell Biol 2000;20:1886-1896.
74. Rytomaa M, Martins LM, Downward J. Involvement of FADD and caspase-8 signalling in detachment-induced apoptosis. Curr Biol 1999;9:1043-1046.
75. Coll ML, Rosen K, Ladeda V et al. Increased Bcl-xL expression mediates v-Src-induced resistance to anoikis in intestinal epithelial cells. Oncogene 2002;21:2908-2913.
76. Tiberio R, Marconi A, Fila C et al. Keratinocytes enriched for stem cells are protected from anoikis via an integrin signaling pathway in a Bcl-2 dependent manner. FEBS Lett 2002;524:139-144.
77. Stromblad S, Becker JC, Yebra M et al. Suppression of p53 activity and p21WAF1/CIP1 expression by vascular cell integrin alphaVbeta3 during angiogenesis. J Clin Invest 1996;98:426-433.
78. Miyashita T, Krajewski S, Krajewska et al. Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 1994;9:1799-1805.
79. Miyashita T, Reed JC. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 1995;80:293-299.
80. Valentijn AJ, Gilmore AP. Translocation of full-length Bid to mitochondria during anoikis. J Biol Chem 2004;279(31):32848-32857.
81. Reginato MJ, Mills KR, Paulus JK et al. Integrins and EGFR coordinately regulate the pro-apoptotic protein Bim to prevent anoikis. Nat Cell Biol 2003;5(8):733-740.
82. Wang P, Gilmore AP, Streuli CH. Bim is an apoptosis sensor that responds to loss of survival signals delivered by epidermal growth factor but not those provided by integrins. J Biol Chem 2004;279(40):41280-41285.
83. Hazlehurst LA, Landowski TH, Dalton WS. Role of the tumor microenvironment in mediating de novo resistance to drugs and physiological mediators of cell death. Oncogene 2003;22(47):7396-7402.
84. Puthalakath H, Huang DC, O'Reilly LA et al. The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol Cell 1999;3:287-296.
85. Puthalakath H, Villunger A, O'Reilly LA et al. Bmf: A proapoptotic BH3-only protein regulated by interaction with the myosin V actin motor complex, activated by anoikis. Science 2001;293:1829-1832.
86. Bouillet P, Strasser A. BH3-only proteins-evolutionarily conserved proapoptotic Bcl-2 family members essential for initiating programmed cell death. J Cell Sci 2002;115:1567-1574.
87. Bouillet P, Purton JF, Godfrey DI et al. BH3-only Bcl-2 family member Bim is required for apoptosis of autoreactive thymocytes. Nature 2002;415:922-926.
88. Frisch SM, Vuori K, Ruoslahti E et al. Control of adhesion-dependent cell survival by focal adhesion kinase. J Cell Biol 1996;134(3):793-799.
89. Hungerford JE, Compton MT, Matter ML et al. Inhibition of pp125FAK in cultured fibroblasts results in apoptosis. J Cell Biol 1996;135(5):1383-1390.
90. Ilic D, Almeida EA, Schlaepfer DD et al. Extracellular matrix survival signals transduced by focal adhesion kinase suppress p53-mediated apoptosis. J Cell Biol 1998;143:547-560.
91. Almeida EA, Ilic D, Han Q et al. Matrix survival signaling: From fibronectin via focal adhesion kinase to c-Jun. NH (2)-terminal kinase. J Cell Biol 2000;149:741-754.
92. Khwaja A, Downward J. Lack of correlation between activation of Jun-NH2-terminal kinase and induction of apoptosis after detachment of epithelial cells. J Cell Biol 1997;139(4):1017-1023.
93. Kiyokawa E, Hashimoto Y, Kurata T et al. Evidence that DOCK180 up-regulates signals from the CrkII-p130 (Cas) complex. J Biol Chem 1998;273:24479-24484.
94. Aoudjit F, Vuori K. Engagement of the alpha2beta1 integrin inhibits Fas ligand expression and activation-induced cell death in T cells in a focal adhesion kinase-dependent manner. Blood 2000;95:2044-2051.
95. Gilmore AP, Metcalfe AD, Romer LH et al. Integrin-mediated survival signals regulate the apoptotic function of Bax through its conformation and subcellular localization. J Cell Biol 2000;149:431-446.
96. Khwaja A, Rodriguez-Viciana P, Wennstrom S et al. Matrix adhesion and Ras transformation both activate a phosphoinositide 3-OH kinase and protein kinase B/Akt cellular survival pathway. EMBO J 1997;16(10):2783-2793.
97. Datta SR, Dudek H, Tao X et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997;91(2):231-241.
98. Cardone MH, Roy N, Stennicke HR et al. Regulation of cell death protease caspase-9 by phosphorylation. Science 1998;282(5392):1318-1321.
99. Sonoda Y, Matsumoto Y, Funakoshi M et al. Anti-apoptotic role of FAK: Induction of inhibitor of apoptosis proteins and apoptosis suppression by the overexpression of FAK in a human leukemic cell line, HL-60. J Biol Chem 2000;275:16309-16315.
100. Hannigan G, Troussard AA, Dedhar S. Integrin-linked kinase: A cancer therapeutic target unique among its ILK. Nature Reviews Cancer 2005;5:51-63.
101. Persad S, Attwell S, Gray V et al. Inhibition of integrin-linked kinase (ILK) suppresses activation of protein kinase B/Akt and induces cell cycle arrest and apoptosis of PTEN-mutant prostate cancer cells. Proc Natl Acad Sci USA 2000;97:3207-3212.
102. Attwell S, Roskelle C, Dedhar S. The integrin-linked kinase (ILK) suppresses anoikis. Oncogene 2000;19:3811-3815.
103. Plantefaber LC, Hynes RO. Changes in integrin receptors on oncogenically transformed cells. Cell 1989;56(2):281-290.
104. Dedhar S, Saulnier R. Alterations in integrin receptor expression on chemically transformed human cells: Specific enhancement of laminin and collagen receptor complexes. J Cell Biol 1990;110(2):481-489.
105. Sainsbury JR, Nicholson S, Angus B et al. Epidermal growth factor receptor status of histological sub-types of breast cancer. Br J Cancer 1988;58(4):458-460.
106. Slamon DJ, Clark GM, Wong SG et al. Human breast cancer: Correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987;235(4785):177-182.
107. Slamon DJ, Godolphin W, Jones LA et al. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 1989;244(4905):707- 712.
108. Liu E, Thor A, He M et al. The HER2 (c-erbB-2) oncogene is frequently amplified in in situ carcinomas of the breast. Oncogene 1992;7(5):1027-1032.
109. Berdichevsky F, Gilbert C, Shearer M et al. Collagen-induced rapid morphogenesis of human mammary epithelial cells: The role of the alpha 2 beta 1 integrin. J Cell Sci 1992;102(Pt 3):437-446.
110. D'Souza B, Berdichevsky F, Kyprianou N et al. Collagen-induced morphogenesis and expression of the alpha 2-integrin subunit is inhibited in c-erbB2-transfected human mammary epithelial cells. Oncogene 1993;8(7):1797-1806.
111. Ye J, Xu RH, Taylor-Papadimitriou J et al. Sp1 binding plays a critical role in Erb-B2-and v-ras-mediated downregulation of alpha2-integrin expression in human mammary epithelial cells. Mol Cell Biol 1996;16(11):6178-6189.
112. Zutter MM, Mazoujian G, Santoro SA. Decreased expression of integrin adhesive protein receptors in adenocarcinoma of the breast. Am J Pathol 1990;137(4):863-870.
113. Koukoulis GK, Virtanen I, Korhonen M et al. Immunohistochemical localization of integrins in the normal, hyperplastic, and neoplastic breast. Correlations with their functions as receptors and cell adhesion molecules. Am J Pathol 1991;139(4):787-799.
114. Pignatelli M, Cardillo MR, Hanby A et al. Integrins and their accessory adhesion molecules in mammary carcinomas: Loss of polarization in poorly-differentiated tumors. Hum Pathol 1992;23(10):1159-1166.
115. Pignatelli M, Hanby AM, Stamp GW. Low expression of beta 1, alpha 2 and alpha 3 subunits of VLA integrins in malignant mammary tumours. J Pathol 1991;165(1):25-32.
116. Pignatelli M, Smith M E F, Bodmer WF. Low expression of collagen receptors in moderate and poorly-differentiated colorectal adenocarcinomas. Brit J Cancer 1991;61:636-638.
117. Stallmach A, von Lampe B, Matthes H et al. Diminished expression of integrin adhesion molecules on human colonic epithelial cells during the benign to malign tumour transformation. Gut 1992;33(3):342-346.
118. Bonkhoff H, Stein U, Remberger K. Differential expression of alpha 6 and alpha 2 very late antigen integrins in the normal, hyperplastic, and neoplastic prostate: Simultaneous demonstration of cell surface receptors and their extracellular ligands. Hum Pathol 1993;24(3):243-248.
119. Fridman R, Giaccone G, Kanemoto T et al. Reconstituted basement membrane (matrigel) and laminin can enhance the tumorigenicity and the drug resistance of small cell lung cancer cell lines. Proc Natl Acad Sci USA 1990;87(17):6698- 6702.
120. Kraus AC, Ferber I, Bachmann SO et al. In vitro chemo-and radio-resistance in small cell lung cancer correlates with cell adhesion and constitutive activation of AKT and MAP kinase pathways. Oncogene 2002;21(57):8683-8695.
121. Sethi T, Rintoul RC, Moore SM et al. Extracellular matrix proteins protect small cell lung cancer cells against apoptosis: A mechanism for small cell lung cancer growth and drug resistance in vivo. Nat Med 1999;5(6):662-668.
122. Buttery RC, Rintoul RC, Sethi T. Small cell lung cancer: The importance of the extracellular matrix. Int J Biochem Cell Biol 2004;36(7):1154-1160.
123. Hartmann TN, Burger M, Burger JA. The role of adhesion molecules and chemokine receptor CXCR4 (CD184) in small cell lung cancer. J Biol Regul Homeost Agents 2004;18:126-130.
124. Cordes N, Beinke C, Plasswilm L et al. Irradiation and various cytotoxic drugs enhance tyrosine phosphorylation and beta (1)-integrin clustering in human A549 lung cancer cells in a substratum-dependent manner in vitro. Strahlenther Onkol 2004;180(3):157-164.
125. Oshita F, Kameda Y, Hamanaka N et al. High expression of integrin β1 and p53 is a greater poor prognostic factor than clinical stage in small-cell lung cancer. Am J Clin Oncol 2000;27:215-219.
126. Holcik M, Yeh C, Korneluk RG et al. Translational upregulation of X-linked inhibitor of apoptosis (XIAP) increases resistance to radiation induced cell death. Oncogene 2000;19:4174-4177.
127. Rodel C, Haas J, Groth A et al. Spontaneous and radiation-induced apoptosis in colorectal carcinoma cells with different intrinsic radiosensitivities: Survivin as a radioresistance factor. Int J Radiat Oncol Biol Phys 2003;55:1341-1347.
128. Monzo M, Rosell R, Felip E et al. A novel anti-apoptosis gene: Reexpression of survivin messenger RNA as a prognosis marker in nonsmall-cell lung cancers. J Clin Oncol 1999;17:2100-2104.
129. Ikehara M, Oshita F, Kameda Y et al. Expression of survivin correlated with vessel invasion is a marker of poor prognosis in small adenocarcinoma of the lung. Oncol Rep 2002;9:835-838.
130. Cao C, Mu Y, Hallahan DE et al. XIAP and survivin as therapeutic targets for radiation sensitization in preclinical models of lung cancer. Oncogene 2004;23(42):7047-7052.
131. Fornaro M, Plescia J, Chheang S et al. Fibronectin protects prostate cancer cells from tumor necrosis factor-alpha-induced apoptosis via the AKT/survivin pathway. J Biol Chem 2003;278(50):50402-50411.
132. Uhm JH, Dooley NP, Kyritsis AP et al. Vitronectin, a glioma-derived extracellular matrix protein, protects tumor cells from apoptotic death. Clin Cancer Res 1999;5:1587-1594.
133. Miyamoto H, Murakami T, Tsuchida K et al. Tumor-stroma interaction of human pancreatic cancer: Acquired resistance to anticancer drugs and proliferation regulation is dependent on extracellular matrix proteins. Pancreas 2004;28(1):38-44.
134. Burbridge MF, Venot V, Casara PJ et al. Decrease in survival threshold of quiescent colon carcinoma cells in the presence of a small molecule integrin antagonist. Mol Pharmacol 2003;63(6):1281-1288.
135. Maubant S, Cruet-Hennequart S, Poulain L et al. Altered adhesion properties and alphav integrin expression in a cisplatin-resistant human ovarian carcinoma cell line. Int J Cancer 2002;97(2):186-194.
136. Cruet-Hennequart S, Maubant S, Luis J et al. alpha (v) integrins regulate cell proliferation through integrin-linked kinase (ILK) in ovarian cancer cells. Oncogene 2003;22(11):1688-1702.
137. Nista A, Leonetti C, Bernardini G et al. Functional role of alpha4beta1 and alpha5beta1 integrin fibronectin receptors expressed on adriamycin-resistant MCF-7 human mammary carcinoma cells. Int J Cancer 1997;72:133-141.
138. Narita T, Kimura N, Sato M et al. Altered expression of integrins in adriamycin-resistant human breast cancer cells. Anticancer Res 1998;18(1A): 257-262.
139. Wewer UM, Shaw LM, Albrechtsen R et al. The integrin alpha 6 beta 1 promotes the survival of metastatic human breast carcinoma cells in mice. Am J Pathol 1997;151:1191-1198.
140. Aoudjit F, Vuori K. Integrin signaling inhibits paclitaxel-induced apoptosis in breast cancer cells. Oncogene 2001;20(36):4995-5004.
141. Menendez JA, Vellon L, Mehmi I et al. 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;24(5):761-779.
142. Tsai M-S, Hornby AE, Lakins J et al. Expression and function of CYR61, an angiogenic factor, in breast cancer cell lines and tumor biopsies. Cancer Res 2000;60:5603-5607.
143. Brigstock DR. The connective tissue growth factor/cysteine-rich 61/nephroblastoma overexpressed (CCN) family. Endocr Rev 1999;20:189-206.
144. Brigstock DR, Goldschmeding R, Katsube KI et al. Proposal for a unified CCN nomenclature. Mol Pathol 2003;56:127-128.
145. Lester FL, Stephen C-TL. The CCN family of angiogenic regulators: The integrin connection. Exp Cell Res 1999;248:44-57.
146. Perbal B. The CCN family of genes: A brief history. Mol Pathol 2001;54:103-104.
147. Perbal B. CCN proteins: Multifunctional signalling regulators. Lancet 2004;363:62-64.
148. Planque N, Perbal B. A structural approach to the role of CCN (CYR61/CTGF/NOV) proteins in tumourigenesis. Cancer Cell Int 2003;3:15.
149. Menendez JA, Mehmi I, Griggs DW et al. The angiogenic factor CYR61 in breast cancer: Molecular pathology and therapeutic perspectives. Endocrine Rel Cancer 2003;10:141-152.
150. Lupu R, Cardillo M, Cho C et al. The significance of heregulin in breast cancer tumor progression and drug resistance. Breast Cancer Res Treat 1996;38:57-66.
151. Tsai M-S, Bogart DF, Castaneda JM et al. Cyr61 promotes breast tumorigenesis and cancer progression. Oncogene 2002;21:8178-8185.
152. Tsai MS, Shamon-Taylor LA, Mehmi I et al. Blockage of heregulin expression inhibits tumorigenicity and metastasis of breast cancer. Oncogene 2003;22:761-768.
153. Atlas E, Mehmi I, Cardilla M et al. Heregulin is sufficient for the promotion of tumorigenicity and metastasis of breast cancer cells in vivo. Mol Cancer Res 2003;1:165-175.
154. Kayaselcuk F, Nursal TZ, Polat A et al. Expression of survivin, bcl-2, P53 and bax in breast carcinoma and ductal intraepithelial neoplasia (DIN 1a). J Exp Clin Cancer Res 2004;23(1):105-112.
155. Chu JS, Shew JY, Huang CS. Immunohistochemical analysis of survivin expression in primary breast cancers. J Formos Med Assoc 2004;103(12):925-931.
156. Tsuji N, Furuse K, Asanuma K et al. Mutations of the p53 gene and loss of heterozygosity at chromosome 17p13.1 are associated with increased survivin expression in breast cancer. Breast Cancer Res Treat 2004;87(1):23-31.
157. Zahir N, Weaver VM. Death in the third dimension: Apoptosis regulation and tissue architecture. Curr Opin Genet Dev 2004;14(1):71-80.
158. Teicher BA, Herman TS, Holden SA et al. Tumor resistance to alkylating agents conferred by mechanisms operative only in vivo. Science 1990;247(4949 Pt 1):1457-1461.
159. Kerbel RS, Rak J, Kobayashi H et al. Multicellular resistance: A new paradigm to explain aspects of acquired drug resistance of solid tumors. Cold Spring Harbor Symp Quant Biol 1994;59:661-672.
160. Kobayashi HS, Man SJ, Kapitain BA et al. Acquired multicellular-mediated resistance to alkylating agents in cancer. Proc Natl Acad Sci USA 1993;90:3294-3298.
161. Santini MT, Rainaldi G, Indovina PL. Apoptosis, cell adhesion and the extracellular matrix in the three-dimensional growth of multicellular tumor spheroids. Crit Rev Oncol Hematol 2000;36(2-3): 75-87.
162. Green SK, Francia G, Isidoro C et al. Antiadhesive antibodies targeting E-cadherin sensitize multicellular tumor spheroids to chemotherapy in vitro. Mol Cancer Ther 2004;3(2):149-159.
163. Boudreau N, Werb Z, Bissell MJ. Suppression of apoptosis by basement membrane requires three-dimensional tissue organization and withdrawal from the cell cycle. Proc Natl Acad Sci USA 1996;93(8):3509-3513.
164. Weaver VM, Lelievre S, Lakins JN et al. beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell 2002;2(3):205-16.
165. Zahir N, Lakins JN, Russell A et al. Autocrine laminin-5 ligates alpha6beta4 integrin and activates RAC and NFkappaB to mediate anchorage-independent survival of mammary tumors. J Cell Biol 2003;163(6):1397-1407.