Integrin-dependent response to laminin-511 regulates breast tumor cell invasion and metastasis

International Journal of Cancer

Volumn 130, Issue 3, 2012, Pages 555-566

  Kusuma, Nicole ^a,b   Denoyer, Delphine ^a   Eble, Johannes A ^c   Redvers, Richard P ^a   Parker, Belinda S ^a,b   Pelzer, Rebecca ^a   Anderson, Robin L ^a,b   Pouliot, Normand ^a,b  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

breast cancer metastasis; integrin; invasion; laminin; lebein

Indexed keywords

BETA1 INTEGRIN; BETA4 INTEGRIN; DISINTEGRIN; INTEGRIN; INTEGRIN RECEPTOR; LAMININ 10; LEBEIN 1; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE METASTASIS; BREAST CARCINOMA; CANCER INVASION; CELL ADHESION; CELL MIGRATION; CELL SUBPOPULATION; CHEMOTAXIS; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOTAXIS; FEMALE; HUMANS; INTEGRINS; LAMININ; MICE; MICE, INBRED BALB C; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; TUMOR BURDEN; VIPER VENOMS;

EID: 82255175213     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.26018     Document Type: Article

References (44)

1. Coleman RE, Smith P, Rubens RD,. Clinical course and prognostic factors following bone recurrence from breast cancer. Br J Cancer 1998; 77: 336-40. (Pubitemid 28029553)
2. Joyce JA, Pollard JW,. Microenvironmental regulation of metastasis. Nat Rev Cancer 2009; 9: 239-52.
3. Casimiro S, Guise TA, Chirgwin J,. The critical role of the bone microenvironment in cancer metastases. Mol Cell Endocrinol 2009; 310: 71-81.
4. Dai CY, Haqq CM, Puzas JE,. Molecular correlates of site-specific metastasis. Semin Radiat Oncol 2006; 16: 102-10.
5. Dittmar T, Heyder C, Gloria-Maercker E, Hatzmann W, Zanker KS,. Adhesion molecules and chemokines: the navigation system for circulating tumor (stem) cells to metastasize in an organ-specific manner. Clin Exp Metastasis 2008; 25: 11-32. (Pubitemid 351191223)
6. Nguyen DX, Bos PD, Massague J,. Metastasis: From dissemination to organ-specific colonization. Nat Rev Cancer 2009; 9: 274-84.
7. Hynes RO,. Metastatic potential: Generic predisposition of the primary tumor or rare, metastatic variants-or both? Cell 2003; 113: 821-3. (Pubitemid 36792026)
8. Talmadge JE,. Clonal selection of metastasis within the life history of a tumor. Cancer Res 2007; 67: 11471-5.
9. Aslakson CJ, Miller FR,. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res 1992; 52: 1399-405.
10. Eckhardt BL, Parker BS, van Laar RK, Restall CM, Natoli AL, Tavaria MD, Stanley KL, Sloan EK, Moseley JM, Anderson RL,. Genomic analysis of a spontaneous model of breast cancer metastasis to bone reveals a role for the extracellular matrix. Mol Cancer Res 2005; 3: 1-13. (Pubitemid 40189591)
11. Lelekakis M, Moseley JM, Martin TJ, Hards D, Williams E, Ho P, Lowen D, Javni J, Miller FR, Slavin J, Anderson RL,. A novel orthotopic model of breast cancer metastasis to bone. Clin Exp Metastasis 1999; 17: 163-70. (Pubitemid 29335443)
12. Chia J, Kusuma N, Anderson R, Parker B, Bidwell B, Zamurs L, Nice E, Pouliot N,. Evidence for a role of tumor-derived laminin-511 in the metastatic progression of breast cancer. Am J Pathol 2007; 170: 2135-48. (Pubitemid 47339285)
13. Fujita M, Khazenzon NM, Bose S, Sekiguchi K, Sasaki T, Carter WG, Ljubimov AV, Black KL, Ljubimova JY,. Overexpression of beta1-chain-containing laminins in capillary basement membranes of human breast cancer and its metastases. Breast Cancer Res 2005; 7: R411-21.
14. Doi M, Thyboll J, Kortesmaa J, Jansson K, Iivanainen A, Parvardeh M, Timpl R, Hedin U, Swedenborg J, Tryggvason K,. Recombinant human laminin-10 (alpha5beta1gamma1). Production, purification, and migration-promoting activity on vascular endothelial cells. J Biol Chem 2002; 277: 12741-8. (Pubitemid 34952635)
15. Eble JA, Bruckner P, Mayer U,. Vipera lebetina venom contains two disintegrins inhibiting laminin-binding beta1 integrins. J Biol Chem 2003; 278: 26488-96. (Pubitemid 36876790)
16. Sloan EK, Pouliot N, Stanley KL, Chia J, Moseley JM, Hards DK, Anderson RL,. Tumor-specific expression of alphavbeta3 integrin promotes spontaneous metastasis of breast cancer to bone. Breast Cancer Res 2006; 8: R20.
17. Pouliot N, Nice EC, Burgess AW,. Laminin-10 mediates basal and EGF-stimulated motility of human colon carcinoma cells via alpha(3)beta(1) and alpha(6)beta(4) integrins. Exp Cell Res 2001; 266: 1-10. (Pubitemid 32989037)
18. Kikkawa Y, Sanzen N, Fujiwara H, Sonnenberg A, Sekiguchi K,. Integrin binding specificity of laminin-10/11: laminin-10/11 are recognized by alpha 3 beta 1, alpha 6 beta 1 and alpha 6 beta 4 integrins. J Cell Sci 2000; 113 (Pt 5): 869-76. (Pubitemid 30168655)
19. Pouliot N, Connolly LM, Moritz RL, Simpson RJ, Burgess AW,. Colon cancer cells adhesion and spreading on autocrine laminin-10 is mediated by multiple integrin receptors and modulated by EGF receptor stimulation. Exp Cell Res 2000; 261: 360-71. (Pubitemid 32010232)
20. Spessotto P, Gronkowska A, Deutzmann R, Perris R, Colombatti A,. Preferential locomotion of leukemic cells towards laminin isoforms 8 and 10. Matrix Biol 2003; 22: 351-61. (Pubitemid 36993760)
21. McLane MA, Sanchez EE, Wong A, Paquette-Straub C, Perez JC,. Disintegrins. Curr Drug Targets Cardiovasc Haematol Disord 2004; 4: 327-55. (Pubitemid 39562089)
22. Shipitsin M, Campbell LL, Argani P, Weremowicz S, Bloushtain-Qimron N, Yao J, Nikolskaya T, Serebryiskaya T, Beroukhim R, Hu M, Halushka MK, Sukumar S, et al,. Molecular definition of breast tumor heterogeneity. Cancer Cell 2007; 11: 259-73. (Pubitemid 46349843)
23. Durkin ME, Loechel F, Mattei MG, Gilpin BJ, Albrechtsen R, Wewer UM,. Tissue-specific expression of the human laminin alpha5-chain, and mapping of the gene to human chromosome 20q13.2-13.3 and to distal mouse chromosome 2 near the locus for the ragged (Ra) mutation. FEBS Lett 1997; 411: 296-300. (Pubitemid 27301473)
24. Miner JH, Patton BL, Lentz SI, Gilbert DJ, Snider WD, Jenkins NA, Copeland NG, Sanes JR,. The laminin alpha chains: Expression, developmental transitions, and chromosomal locations of alpha1-5, identification of heterotrimeric laminins 8-11, and cloning of a novel alpha3 isoform. J Cell Biol 1997; 137: 685-701. (Pubitemid 27200670)
25. Garcia T, Jackson A, Bachelier R, Clement-Lacroix P, Baron R, Clezardin P, Pujuguet P,. A convenient clinically relevant model of human breast cancer bone metastasis. Clin Exp Metastasis 2008; 25: 33-42. (Pubitemid 351191224)
26. Yoneda T, Williams PJ, Hiraga T, Niewolna M, Nishimura R,. A bone-seeking clone exhibits different biological properties from the MDA-MB-231 parental human breast cancer cells and a brain-seeking clone in vivo and in vitro. J Bone Miner Res 2001; 16: 1486-95. (Pubitemid 32675200)
27. Takahashi M, Furihata M, Akimitsu N, Watanabe M, Kaul S, Yumoto N, Okada T,. A highly bone marrow metastatic murine breast cancer model established through in vivo selection exhibits enhanced anchorage-independent growth and cell migration mediated by ICAM-1. Clin Exp Metastasis 2008; 25: 517-29.
28. Rose AA, Pepin F, Russo C, Abou Khalil JE, Hallett M, Siegel PM,. Osteoactivin promotes breast cancer metastasis to bone. Mol Cancer Res 2007; 5: 1001-14. (Pubitemid 350070756)
29. Hughes L, Malone C, Chumsri S, Burger AM, McDonnell S,. Characterisation of breast cancer cell lines and establishment of a novel isogenic subclone to study migration, invasion and tumourigenicity. Clin Exp Metastasis 2008; 25: 549-57.
30. Gudjonsson T, Ronnov-Jessen L, Villadsen R, Rank F, Bissell MJ, Petersen OW,. Normal and tumor-derived myoepithelial cells differ in their ability to interact with luminal breast epithelial cells for polarity and basement membrane deposition. J Cell Sci 2002; 115: 39-50. (Pubitemid 34105527)
31. Gusterson BA, Warburton MJ, Mitchell D, Ellison M, Neville AM, Rudland PS,. Distribution of myoepithelial cells and basement membrane proteins in the normal breast and in benign and malignant breast diseases. Cancer Res 1982; 42: 4763-70. (Pubitemid 13205987)
32. Martin KJ, Kwan CP, Nagasaki K, Zhang X, O'Hare MJ, Kaelin CM, Burgeson RE, Pardee AB, Sager R,. Down-regulation of laminin-5 in breast carcinoma cells. Mol Med 1998; 4: 602-13. (Pubitemid 28523113)
33. Sathyanarayana UG, Padar A, Huang CX, Suzuki M, Shigematsu H, Bekele BN, Gazdar AF,. Aberrant promoter methylation and silencing of laminin-5-encoding genes in breast carcinoma. Clin Cancer Res 2003; 9: 6389-94. (Pubitemid 38031824)
34. Putz E, Witter K, Offner S, Stosiek P, Zippelius A, Johnson J, Zahn R, Riethmuller G, Pantel K,. Phenotypic characteristics of cell lines derived from disseminated cancer cells in bone marrow of patients with solid epithelial tumors: establishment of working models for human micrometastases. Cancer Res 1999; 59: 241-8. (Pubitemid 29062984)
35. Tagliabue E, Ghirelli C, Squicciarini P, Aiello P, Colnaghi MI, Menard S,. Prognostic value of alpha 6 beta 4 integrin expression in breast carcinomas is affected by laminin production from tumor cells. Clin Cancer Res 1998; 4: 407-10. (Pubitemid 28122756)
36. Lu S, Simin K, Khan A, Mercurio AM,. Analysis of integrin beta4 expression in human breast cancer: association with basal-like tumors and prognostic significance. Clin Cancer Res 2008; 14: 1050-8. (Pubitemid 351302550)
37. Lipscomb EA, Simpson KJ, Lyle SR, Ring JE, Dugan AS, Mercurio AM,. The alpha6beta4 integrin maintains the survival of human breast carcinoma cells in vivo. Cancer Res 2005; 65: 10970-6. (Pubitemid 41713366)
38. Weaver VM, Lelievre S, Lakins JN, Chrenek MA, Jones JC, Giancotti F, Werb Z, Bissell MJ,. beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell 2002; 2: 205-16. (Pubitemid 41043976)
39. Chen M, Sinha M, Luxon BA, Bresnick AR, O'Connor KL,. Integrin alpha6beta4 controls the expression of genes associated with cell motility, invasion, and metastasis, including S100A4/metastasin. J Biol Chem 2009; 284: 1484-94.
40. Stipp CS,. Laminin-binding integrins and their tetraspanin partners as potential antimetastatic targets. Expert Rev Mol Med 2010; 12: e3.
41. 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 alpha3beta1 integrin and vascular laminin-5 mediate pulmonary arrest and metastasis. J Cell Biol 2004; 164: 935-41. (Pubitemid 38366904)
42. 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 (MMP-9) activity. Int J Cancer 2000; 87: 336-42. (Pubitemid 30451643)
43. 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; 70: 6359-67.
44. Rosenow F, Ossig R, Thormeyer D, Gasmann P, Schluter K, Brunner G, Haier J, Eble JA,. Integrins as antimetastatic targets of RGD-independent snake venom components in liver metastasis [corrected]. Neoplasia 2008; 10: 168-76.