Breast cancer cell migration is regulated through junctional adhesion molecule-A-mediated activation of Rap1 GTPase

Breast Cancer Research

Volumn 13, Issue 2, 2011, Pages

  McSherry, Elaine A ^a   Brennan, Kieran ^a   Hudson, Lance ^a   Hill, Arnold D K ^a   Hopkins, Ann M ^a  

^a BEAUMONT HOSPITAL   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA5 INTEGRIN; BETA1 INTEGRIN; CD51 ANTIGEN; FIBRONECTIN; JUNCTIONAL ADHESION MOLECULE A; MEMBRANE PROTEIN; RAP1 PROTEIN; CELL ADHESION MOLECULE; CELL SURFACE RECEPTOR; F11R PROTEIN, HUMAN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; KINESIN; MLLT4 PROTEIN, HUMAN; MYOSIN; NERVE PROTEIN; RAPGEF2 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ARTICLE; BREAST CANCER; CANCER CELL; CELL MIGRATION; CELL STRAIN MCF 7; COMPLEX FORMATION; ENZYME ACTIVATION; HUMAN; HUMAN CELL; METASTASIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; BIOSYNTHESIS; BREAST TUMOR; CELL ADHESION; CELL MOTION; FEMALE; GENETICS; METABOLISM; PATHOLOGY; RNA INTERFERENCE; TUMOR CELL LINE;

ANTIGENS, CD29; BREAST NEOPLASMS; CELL ADHESION; CELL ADHESION MOLECULES; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; FIBRONECTINS; GTP PHOSPHOHYDROLASES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; KINESIN; MYOSINS; NEOPLASM METASTASIS; NERVE TISSUE PROTEINS; RAP1 GTP-BINDING PROTEINS; RECEPTORS, CELL SURFACE; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84860389407     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr2853     Document Type: Article

References (61)

1. Ferlay J, Autier P, Boniol M, Heanue M, Colombet M, Boyle P. Estimates of the cancer incidence and mortality in Europe in 2006. Ann Oncol 2007, 18:581-592. 10.1093/annonc/mdl498, 17287242.
2. Molitoris BA, Nelson WJ. Alterations in the establishment and maintenance of epithelial cell polarity as a basis for disease processes. J Clin Invest 1990, 85:3-9. 10.1172/JCI114427, 296379, 2404027.
3. Hough CD, Sherman-Baust CA, Pizer ES, Montz FJ, Im DD, Rosenshein NB, Cho KR, Riggins GJ, Morin PJ. Large-scale serial analysis of gene expression reveals genes differentially expressed in ovarian cancer. Cancer Res 2000, 60:6281-6287.
4. Kominsky SL, Argani P, Korz D, Evron E, Raman V, Garrett E, Rein A, Sauter G, Kallioniemi OP, Sukumar S. Loss of the tight junction protein claudin-7 correlates with histological grade in both ductal carcinoma in situ and invasive ductal carcinoma of the breast. Oncogene 2003, 22:2021-2033. 10.1038/sj.onc.1206199, 12673207.
5. Martin TA, Watkins G, Mansel RE, Jiang WG. Loss of tight junction plaque molecules in breast cancer tissues is associated with a poor prognosis in patients with breast cancer. Eur J Cancer 2004, 40:2717-2725. 10.1016/j.ejca.2004.08.008, 15571953.
6. Polette M, Gilles C, Nawrocki-Raby B, Lohi J, Hunziker W, Foidart JM, Birembaut P. Membrane-type 1 matrix metalloproteinase expression is regulated by zonula occludens-1 in human breast cancer cells. Cancer Res 2005, 65:7691-7698.
7. Aranda V, Haire T, Nolan ME, Calarco JP, Rosenberg AZ, Fawcett JP, Pawson T, Muthuswamy SK. Par6-aPKC uncouples ErbB2 induced disruption of polarized epithelial organization from proliferation control. Nat Cell Biol 2006, 8:1235-1245. 10.1038/ncb1485, 17060907.
8. Zhan L, Rosenberg A, Bergami KC, Yu M, Xuan Z, Jaffe AB, Allred C, Muthuswamy SK. Deregulation of scribble promotes mammary tumorigenesis and reveals a role for cell polarity in carcinoma. Cell 2008, 135:865-878. 10.1016/j.cell.2008.09.045, 3015046, 19041750.
9. Liang TW, DeMarco RA, Mrsny RJ, Gurney A, Gray A, Hooley J, Aaron HL, Huang A, Klassen T, Tumas DB, Fong S. Characterization of huJAM: evidence for involvement in cell-cell contact and tight junction regulation. Am J Physiol Cell Physiol 2000, 279:C1733-1743.
10. Mandell KJ, Babbin BA, Nusrat A, Parkos CA. Junctional adhesion molecule 1 regulates epithelial cell morphology through effects on beta1 integrins and Rap1 activity. J Biol Chem 2005, 280:11665-11674. 10.1074/jbc.M412650200, 15677455.
11. Sobocka MB, Sobocki T, Banerjee P, Weiss C, Rushbrook JI, Norin AJ, Hartwig J, Salifu MO, Markell MS, Babinska A, Ehrlich YH, Kornecki E. Cloning of the human platelet F11 receptor: a cell adhesion molecule member of the immunoglobulin superfamily involved in platelet aggregation. Blood 2000, 95:2600-2609.
12. Ostermann G, Weber KS, Zernecke A, Schroder A, Weber C. JAM-1 is a ligand of the beta(2) integrin LFA-1 involved in transendothelial migration of leukocytes. Nat Immunol 2002, 3:151-158. 10.1038/ni755, 11812992.
13. Cavusoglu E, Kornecki E, Sobocka MB, Babinska A, Ehrlich YH, Chopra V, Yanamadala S, Ruwende C, Salifu MO, Clark LT, Eng C, Pinsky DJ, Marmur JD. Association of plasma levels of F11 receptor/junctional adhesion molecule-A (F11R/JAM-A) with human atherosclerosis. J Am Coll Cardiol 2007, 50:1768-1776. 10.1016/j.jacc.2007.05.051, 17964041.
14. Laukoetter MG, Nava P, Lee WY, Severson EA, Capaldo CT, Babbin BA, Williams IR, Koval M, Peatman E, Campbell JA, Dermody TS, Nusrat A, Parkos CA. JAM-A regulates permeability and inflammation in the intestine in vivo. J Exp Med 2007, 204:3067-3076. 10.1084/jem.20071416, 2150975, 18039951.
15. Vetrano S, Rescigno M, Cera MR, Correale C, Rumio C, Doni A, Fantini M, Sturm A, Borroni E, Repici A, Locati M, Malesci A, Dejana E, Danese S. Unique role of junctional adhesion molecule-a in maintaining mucosal homeostasis in inflammatory bowel disease. Gastroenterology 2008, 135:173-184. 10.1053/j.gastro.2008.04.002, 18514073.
16. Gutwein P, Schramme A, Voss B, Abdel-Bakky MS, Doberstein K, Ludwig A, Altevogt P, Hansmann ML, Moch H, Kristiansen G, Pfeilschifter J. Downregulation of junctional adhesion molecule-A is involved in the progression of clear cell renal cell carcinoma. Biochem Biophys Res Commun 2009, 380:387-391. 10.1016/j.bbrc.2009.01.100, 19250634.
17. Koshiba H, Hosokawa K, Kubo A, Tokumitsu N, Watanabe A, Honjo H. Junctional adhesion molecule A [corrected] expression in human endometrial carcinoma. Int J Gynecol Cancer 2009, 19:208-213. 10.1111/IGC.0b013e31819bc6e9, 19395995.
18. Naik MU, Naik TU, Suckow AT, Duncan MK, Naik UP. Attenuation of junctional adhesion molecule-A is a contributing factor for breast cancer cell invasion. Cancer Res 2008, 68:2194-2203. 10.1158/0008-5472.CAN-07-3057, 18381425.
19. McSherry EA, McGee SF, Jirstrom K, Doyle EM, Brennan DJ, Landberg G, Dervan PA, Hopkins AM, Gallagher WM. JAM-A expression positively correlates with poor prognosis in breast cancer patients. Int J Cancer 2009, 125:1343-1351. 10.1002/ijc.24498, 19533747.
20. Guo W, Giancotti FG. Integrin signalling during tumour progression. Nat Rev Mol Cell Biol 2004, 5:816-826. 10.1038/nrm1490, 15459662.
21. Li N, Zhang Y, Naylor MJ, Schatzmann F, Maurer F, Wintermantel T, Schuetz G, Mueller U, Streuli CH, Hynes NE. Beta1 integrins regulate mammary gland proliferation and maintain the integrity of mammary alveoli. Embo J 2005, 24:1942-1953. 10.1038/sj.emboj.7600674, 1142608, 15889143.
22. Huck L, Pontier SM, Zuo DM, Muller WJ. beta1-integrin is dispensable for the induction of ErbB2 mammary tumors but plays a critical role in the metastatic phase of tumor progression. Proc Natl Acad Sci USA 2010, 107:15559-15564. 10.1073/pnas.1003034107, 2932605, 20713705.
23. Yao ES, Zhang H, Chen YY, Lee B, Chew K, Moore D, Park C. Increased beta1 integrin is associated with decreased survival in invasive breast cancer. Cancer Res 2007, 67:659-664. 10.1158/0008-5472.CAN-06-2768, 17234776.
24. Sebzda E, Bracke M, Tugal T, Hogg N, Cantrell DA. Rap1A positively regulates T cells via integrin activation rather than inhibiting lymphocyte signaling. Nat Immunol 2002, 3:251-258. 10.1038/ni765, 11836528.
25. Itoh M, Nelson CM, Myers CA, Bissell MJ. Rap1 integrates tissue polarity, lumen formation, and tumorigenic potential in human breast epithelial cells. Cancer Res 2007, 67:4759-4766. 10.1158/0008-5472.CAN-06-4246, 2841018, 17510404.
26. Stampfer M, Hallowes RC, Hackett AJ. Growth of normal human mammary cells in culture. In Vitro 1980, 16:415-425. 10.1007/BF02618365, 6993343.
27. Severson EA, Lee WY, Capaldo CT, Nusrat A, Parkos CA. Junctional adhesion molecule A interacts with Afadin and PDZ-GEF2 to activate Rap1A, regulate beta1 integrin levels, and enhance cell migration. Mol Biol Cell 2009, 20:1916-1925. 10.1091/mbc.E08-10-1014, 2663925, 19176753.
28. Severson EA, Jiang L, Ivanov AI, Mandell KJ, Nusrat A, Parkos CA. Cis-dimerization Mediates Function of Junctional Adhesion Molecule A. Mol Biol Cell 2008, 19:1862-1872. 10.1091/mbc.E07-09-0869, 2366836, 18272784.
29. Geiger B, Spatz JP, Bershadsky AD. Environmental sensing through focal adhesions. Nat Rev Mol Cell Biol 2009, 10:21-33. 10.1038/nrm2593, 19197329.
30. Webb DJ, Parsons JT, Horwitz AF. Adhesion assembly, disassembly and turnover in migrating cells -- over and over and over again. Nat Cell Biol 2002, 4:E97-100. 10.1038/ncb0402-e97, 11944043.
31. Johansson S, Svineng G, Wennerberg K, Armulik A, Lohikangas L. Fibronectin-integrin interactions. Front Biosci 1997, 2:d126-146.
32. Humphries JD, Byron A, Humphries MJ. Integrin ligands at a glance. J Cell Sci 2006, 119:3901-3903. 10.1242/jcs.03098, 16988024.
33. Reedquist KA, Ross E, Koop EA, Wolthuis RM, Zwartkruis FJ, van Kooyk Y, Salmon M, Buckley CD, Bos JL. The small GTPase, Rap1, mediates CD31-induced integrin adhesion. J Cell Biol 2000, 148:1151-1158. 10.1083/jcb.148.6.1151, 2174316, 10725328.
34. Zhang Z, Rehmann H, Price LS, Riedl J, Bos JL. AF6 negatively regulates Rap1-induced cell adhesion. J Biol Chem 2005, 280:33200-33205. 10.1074/jbc.M505057200, 16051602.
35. Dube N, Kooistra MR, Pannekoek WJ, Vliem MJ, Oorschot V, Klumperman J, Rehmann H, Bos JL. The RapGEF PDZ-GEF2 is required for maturation of cell-cell junctions. Cell Signal 2008, 20:1608-1615. 10.1016/j.cellsig.2008.05.006, 18585005.
36. Brenner H, Hakulinen T. Long-term cancer patient survival achieved by the end of the 20th century: most up-to-date estimates from the nationwide Finnish cancer registry. Br J Cancer 2001, 85:367-371. 10.1054/bjoc.2001.1905, 2364068, 11487267.
37. Dow LE, Elsum IA, King CL, Kinross KM, Richardson HE, Humbert PO. Loss of human Scribble cooperates with H-Ras to promote cell invasion through deregulation of MAPK signalling. Oncogene 2008, 27:5988-6001. 10.1038/onc.2008.219, 18641685.
38. Derksen PW, Liu X, Saridin F, van der Gulden H, Zevenhoven J, Evers B, van Beijnum JR, Griffioen AW, Vink J, Krimpenfort P, Peterse JL, Cardiff RD, Berns A, Jonkers J. Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 2006, 10:437-449. 10.1016/j.ccr.2006.09.013, 17097565.
39. Palacios J, Sarrio D, Garcia-Macias MC, Bryant B, Sobel ME, Merino MJ. Frequent E-cadherin gene inactivation by loss of heterozygosity in pleomorphic lobular carcinoma of the breast. Mod Pathol 2003, 16:674-678. 10.1097/01.MP.0000073974.42583.F7, 12861063.
40. Brennan K, Offiah G, McSherry EA, Hopkins AM. Tight junctions: a barrier to the initiation and progression of breast cancer?. J Biomed Biotechnol 2010, 2010:460607. 10.1155/2010/460607, 2777242, 19920867.
41. 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, 302:1704-1709. 10.1126/science.1092053, 14657486.
42. Brakebusch C, Fassler R. beta 1 integrin function in vivo: adhesion, migration and more. Cancer Metastasis Rev 2005, 24:403-411. 10.1007/s10555-005-5132-5, 16258728.
43. Streuli CH, Akhtar N. Signal co-operation between integrins and other receptor systems. Biochem J 2009, 418:491-506. 10.1042/BJ20081948, 19228122.
44. Mandicourt G, Iden S, Ebnet K, Aurrand-Lions M, Imhof BA. JAM-C regulates tight junctions and integrin-mediated cell adhesion and migration. J Biol Chem 2007, 282:1830-1837. 10.1074/jbc.M605666200, 17099249.
45. Naylor MJ, Li N, Cheung J, Lowe ET, Lambert E, Marlow R, Wang P, Schatzmann F, Wintermantel T, Schuetz G, Clarke AR, Mueller U, Hynes NE, Streuli CH. Ablation of beta1 integrin in mammary epithelium reveals a key role for integrin in glandular morphogenesis and differentiation. J Cell Biol 2005, 171:717-728. 10.1083/jcb.200503144, 2171573, 16301336.
46. White DE, Kurpios NA, Zuo D, Hassell JA, Blaess S, Mueller U, Muller WJ. Targeted disruption of beta1-integrin in a transgenic mouse model of human breast cancer reveals an essential role in mammary tumor induction. Cancer Cell 2004, 6:159-170. 10.1016/j.ccr.2004.06.025, 15324699.
47. Streuli CH. Integrins and cell-fate determination. J Cell Sci 2009, 122:171-177. 10.1242/jcs.018945, 2714415, 19118209.
48. Park CC, Zhang H, Pallavicini M, Gray JW, Baehner F, Park CJ, Bissell MJ. Beta1 integrin inhibitory antibody induces apoptosis of breast cancer cells, inhibits growth, and distinguishes malignant from normal phenotype in three dimensional cultures and in vivo. Cancer Res 2006, 66:1526-1535. 10.1158/0008-5472.CAN-05-3071, 2933188, 16452209.
49. Cordes N, Park CC. beta1 integrin as a molecular therapeutic target. Int J Radiat Biol 2007, 83:753-760. 10.1080/09553000701639694, 18058364.
50. Lesniak D, Xu Y, Deschenes J, Lai R, Thoms J, Murray D, Gosh S, Mackey JR, Sabri S, Abdulkarim B. Beta1-integrin circumvents the antiproliferative effects of trastuzumab in human epidermal growth factor receptor-2-positive breast cancer. Cancer Res 2009, 69:8620-8628. 10.1158/0008-5472.CAN-09-1591, 19887601.
51. Bos JL. Linking Rap to cell adhesion. Curr Opin Cell Biol 2005, 17:123-128. 10.1016/j.ceb.2005.02.009, 15780587.
52. Zuo H, Gandhi M, Edreira MM, Hochbaum D, Nimgaonkar VL, Zhang P, Dipaola J, Evdokimova V, Altschuler DL, Nikiforov YE. Downregulation of Rap1GAP through epigenetic silencing and loss of heterozygosity promotes invasion and progression of thyroid tumors. Cancer Res 2010, 70:1389-1397. 10.1158/0008-5472.CAN-09-2812, 2822891, 20124489.
53. Bailey CL, Kelly P, Casey PJ. Activation of Rap1 promotes prostate cancer metastasis. Cancer Res 2009, 69:4962-4968. 10.1158/0008-5472.CAN-08-4269, 19470770.
54. Zhang L, Chenwei L, Mahmood R, van Golen K, Greenson J, Li G, D'Silva NJ, Li X, Burant CF, Logsdon CD, Simeone DM. Identification of a putative tumor suppressor gene Rap1GAP in pancreatic cancer. Cancer Res 2006, 66:898-906. 10.1158/0008-5472.CAN-05-3025, 16424023.
55. Cooke VG, Naik MU, Naik UP. Fibroblast growth factor-2 failed to induce angiogenesis in junctional adhesion molecule-A-deficient mice. Arterioscler Thromb Vasc Biol 2006, 26:2005-2011. 10.1161/01.ATV.0000234923.79173.99, 16809549.
56. Yan J, Li F, Ingram DA, Quilliam LA. Rap1a is a key regulator of fibroblast growth factor 2-induced angiogenesis and together with Rap1b controls human endothelial cell functions. Mol Cell Biol 2008, 28:5803-5810. 10.1128/MCB.00393-08, 2546931, 18625726.
57. Ebnet K, Schulz CU, Meyer Zu Brickwedde MK, Pendl GG, Vestweber D. Junctional adhesion molecule interacts with the PDZ domain-containing proteins AF-6 and ZO-1. J Biol Chem 2000, 275:27979-27988.
58. Boettner B, Herrmann C, Van Aelst L. Ras and Rap1 interaction with AF-6 effector target. Methods Enzymol 2001, 332:151-168. full_text, 11305093.
59. Letessier A, Garrido-Urbani S, Ginestier C, Fournier G, Esterni B, Monville F, Adelaide J, Geneix J, Xerri L, Dubreuil P, Viens P, Charafe-Jauffret E, Jacquemier J, Birnbaum D, Lopez M, Chaffanet M. Correlated break at PARK2/FRA6E and loss of AF-6/Afadin protein expression are associated with poor outcome in breast cancer. Oncogene 2007, 26:298-307. 10.1038/sj.onc.1209772, 16819513.
60. Bazzoni G, Tonetti P, Manzi L, Cera MR, Balconi G, Dejana E. Expression of junctional adhesion molecule-A prevents spontaneous and random motility. J Cell Sci 2005, 118:623-632. 10.1242/jcs.01661, 15657074.
61. Gotte M, Mohr C, Koo CY, Stock C, Vaske AK, Viola M, Ibrahim SA, Peddibhotla S, Teng YH, Low JY, Ebnet K, Kiesel L, Yip GW. miR-145-dependent targeting of Junctional Adhesion Molecule A and modulation of fascin expression are associated with reduced breast cancer cell motility and invasiveness. Oncogene 2010, 29:6569-6580. 10.1038/onc.2010.386, 20818426.