β1 and β4 integrins: From breast development to clinical practice

Breast Cancer Research

Volumn 16, Issue 1, 2014, Pages

  Nisticò, Paola ^a   Modugno, Francesca Di ^a   Spada, Sheila ^a,b   Bissell, Mina J ^c  

^a REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; BETA4 INTEGRIN; LAPATINIB; TRASTUZUMAB;

BREAST CANCER; BREAST CARCINOGENESIS; BREAST DEVELOPMENT; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER SURVIVAL; CLINICAL PRACTICE; EXTRACELLULAR MATRIX; HUMAN; MAMMARY GLAND FUNCTION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SUBUNIT; PROTEIN TARGETING; REVIEW; TUMOR DIFFERENTIATION; ANIMAL; BREAST NEOPLASMS; CELL ADHESION; DISEASE COURSE; DRUG RESISTANCE; FEMALE; GROWTH, DEVELOPMENT AND AGING; MAMMARY GLAND; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; ANTIGENS, CD29; BREAST NEOPLASMS; CELL ADHESION; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; INTEGRIN BETA4; MAMMARY GLANDS, HUMAN;

EID: 85047286136     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/s13058-014-0459-x     Document Type: Review

References (70)

1. Zardavas D, Baselga J, Piccart M: Emerging targeted agents in metastatic breast cancer. Nat Rev Clin Oncol 2013, 10:191-210.
2. Hynes RO: Integrins: versatility, modulation, and signaling in cell adhesion. Cell 1992, 69:11-25.
3. Ginsberg MH, Du X, Plow EF: Inside-out integrin signalling. Curr Opin Cell Biol 1992, 4:766-771.
4. Schwartz MA, Ginsberg MH: Networks and crosstalk: integrin signalling spreads. Nat Cell Biol 2002, 4:E65-E68.
5. Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, Damsky C, Bissell MJ: Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol 1997, 137:231-245.
6. 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, 14:1050-1058.
7. Nam JM, Ahmed KM, Costes S, Zhang H, Onodera Y, Olshen AB, Hatanaka KC, Kinoshita R, Ishikawa M, Sabe H, Shirato H, Park CC: Beta1-integrin via NF-kappaB signaling is essential for acquisition of invasiveness in a model of radiation treated in situ breast cancer. Breast Cancer Res 2013, 15:R60.
8. Zawistowski JS, Nakamura K, Parker JS, Granger DA, Golitz BT, Johnson GL: MicroRNA 9-3p targets β1 integrin to sensitize claudin-low breast cancer cells to MEK inhibition. Mol Cell Biol 2013, 33:2260-2274.
9. Pontiggia O, Sampayo R, Raffo D, Motter A, Xu R, Bissell MJ, Joffé EB, Simian M: The tumor microenvironment modulates tamoxifen resistance in breast cancer: a role for soluble stromal factors and fibronectin through β1 integrin. Breast Cancer Res Treat 2012, 133:459-471.
10. 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.
11. Huang C, Park CC, Hilsenbeck SG, Ward R, Rimawi MF, Wang YC, Shou J, Bissell MJ, Osborne CK, SchiffR: β1 integrin mediates an alternative survival pathway in breast cancer cells resistant to lapatinib. Breast Cancer Res 2011, 13:R84.
12. Jahangiri A, Aghi MK, Carbonell WS: β1 integrin: critical path to antiangiogenic therapy resistance and beyond. Cancer Res 2014, 74:3-7.
13. Nam JM, Onodera Y, Bissell MJ, Park CC: Breast cancer cells in threedimensional culture display an enhanced radioresponse after coordinate targeting of integrin alpha5beta1 and fibronectin. Cancer Res 2010, 70:5238-5248.
14. Folgiero V, Avetrani P, Bon G, Di Carlo SE, Fabi A, Nisticò C, Vici P, Melucci E, Buglioni S, Perracchio L, Sperduti I, Rosanò L, Sacchi A, Mottolese M, Falcioni R: Induction of ErbB-3 expression by alpha6beta4 integrin contributes to tamoxifen resistance in ERbeta1-negative breast carcinomas. PLoS One 2008, 3:e1592.
15. Lahlou H, Muller WJ: β1-integrins signaling and mammary tumor progression in transgenic mouse models: implications for human breast cancer. Breast Cancer Res 2011, 13:229-239.
16. Streuli CH, Bailey N, Bissell MJ: Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell-cell interaction and morphological polarity. J Cell Biol 1991, 115:1383-1395.
17. Taddei I, Faraldo MM, Teulière J, Deugnier MA, Thiery JP, Glukhova MA: Integrins in mammary gland development and differentiation of mammary epithelium. J Mammary Gland Biol Neoplasia 2003, 8:383-394.
18. Sonnenberg A, Calafat J, Janssen H, Daams H, van der Raaij-Helmer LM, Falcioni R, Kennel SJ, Aplin JD, Baker J, Loizidou M: Integrin alpha 6/beta 4 complex is located in hemidesmosomes, suggesting a major role in epidermal cell-basement membrane adhesion. J Cell Biol 1991, 113:907-917.
19. Petersen OW, Polyak K: Stem cells in the human breast. In The Mammary Gland as an Experimental Model, Cold Spring Harbor Perspectives in Biology. Edited by Bissell MJ, Polyak K, Rosen JM. New York: Cold Spring Harbor Laboratory Press; 2011:55-69.
20. Jolicoeur F: Intrauterine breast development and the mammary myoepithelial lineage. J Mammary Gland Biol Neoplasia 2005, 10:199-210.
21. Nelson CM, Vanduijn MM, Inman JL, Fletcher DA, Bissell MJ: Tissue geometry determines sites of mammary branching morphogenesis in organotypic cultures. Science 2006, 314:298-300.
22. Keely PJ, Wu JE, Santoro SA: The spatial and temporal expression of the alpha 2 beta 1 integrin and its ligands, collagen I, collagen IV, and laminin, suggest important roles in mouse mammary morphogenesis. Differentiation 1995, 59:1-13.
23. Schedin P, Keely PJ: Mammary gland ECM remodeling, stiffness, and mechanosignaling in normal development and tumor progression. In The Mammary Gland as an Experimental Model, Cold Spring Harbor Perspectives in Biology. Edited by Bissell MJ, Polyak K, Rosen JM. New York: Cold Spring Harbor Laboratory Press; 2011:123-144.
24. Mori H, Lo AT, Inman JL, Alcaraz J, Ghajar CM, Mott JD, Nelson CM, Chen CS, Zhang H, Bascom JL, Seiki M, Bissell MJ: Transmembrane/cytoplasmic, rather than catalytic, domains of Mmp14 signal to MAPK activation and mammary branching morphogenesis via binding to integrin β1. Development 2013, 140:343-352.
25. Klinowska TC, Alexander CM, Georges-Labouesse E, Van der Neut R, Kreidberg JA, Jones CJ, Sonnenberg A, Streuli CH: Epithelial development and differentiation in the mammary gland is not dependent on alpha 3 or alpha 6 integrin subunits. Dev Biol 2001, 233:449-467.
26. Stahl S, Weitzman S, Jones JC: The role of laminin-5 and its receptors in mammary epithelial cell branching morphogenesis. J Cell Sci 1997, 110:55-63.
27. Petersen OW, Rønnov-Jessen L, Howlett AR, Bissell MJ: Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. Proc Natl Acad Sci U S A 1992, 89:9064-9068.
28. Weaver VM, Lelièvre S, Lakins JN, Chrenek MA, Jones JC, Giancotti F, Werb Z, Bissell MJ: Beta4 integrin-dependent formation of polarized threedimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell 2002, 2:205-216.
29. Akhtar N, Streuli CH: An integrin-ILK-microtubule network orients cell polarity and lumen formation in glandular epithelium. Nat Cell Biol 2013, 15:17-27.
30. Naylor MJ, Li N, Cheung J, Lowe ET, Lambert E, Marlow R, Wang P, Schatzmann F, Wintermantel T, Schüetz 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.
31. Akhtar N, Marlow R, Lambert E, Schatzmann F, Lowe ET, Cheung J, Katz E, Li W, Wu C, Dedhar S, Naylor MJ, Streuli CH: Molecular dissection of integrin signalling proteins in the control of mammary epithelial development and differentiation. Development 2009, 136:1019-1027.
32. Muschler J, Lochter A, Roskelley CD, Yurchenco P, Bissell MJ: Division of labor among the alpha6beta4 integrin, beta1 integrins, and an E3 laminin receptor to signal morphogenesis and beta-casein expression in mammary epithelial cells. Mol Biol Cell 1999, 10:2817-2828.
33. Raymond K, Cagnet S, Kreft M, Janssen H, Sonnenberg A, Glukhova MA: Control of mammary myoepithelial cell contractile function by a3β1 integrin signalling. EMBO J 2011, 30:1896-1906.
34. Koukoulis GK, Virtanen I, Korhonen M, Laitinen L, Quaranta V, Gould VE: 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, 139:787-799.
35. 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.
36. dos Santos PB, Zanetti JS, Ribeiro-Silva A, Beltrão EI: Beta 1 integrin predicts survival in breast cancer: a clinicopathological and immunohistochemical study. Diagn Pathol 2012, 7:104-113.
37. Rizki A, Weaver VM, Lee SY, Rozenberg GI, Chin K, Myers CA, Bascom JL, Mott JD, Semeiks JR, Grate LR, Mian IS, Borowsky AD, Jensen RA, Idowu MO, Chen F, Chen DJ, Petersen OW, Gray JW, Bissell MJ: A human breast cell model of preinvasive to invasive transition. Cancer Res 2008, 68:1378-1387.
38. 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.
39. Lahlou H, Sanguin-Gendreau V, Zuo D, CardiffRD, McLean GW, Frame MC, Muller WJ: Mammary epithelial-specific disruption of the focal adhesion kinase blocks mammary tumor progression. Proc Natl Acad Sci U S A 2007, 104:20302-20307.
40. 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 U S A 2010, 107:15559-15564.
41. Cagnet S, Faraldo MM, Kreft M, Sonnenberg A, Raymond K, Glukhova MA: Signaling events mediated by a3β1 integrin are essential for mammary tumorigenesis. Oncogene 2014, 33:4286-4295.
42. Pontier SM, Huck L, White DE, Rayment J, Sanguin-Gendreau V, Hennessy B, Zuo D, St-Arnaud R, Mills GB, Dedhar S, Marshall CJ, Muller WJ: Integrinlinked kinase has a critical role in ErbB2 mammary tumor progression: implications for human breast cancer. Oncogene 2010, 29:3374-3385.
43. Falcioni R, Antonini A, Nisticò P, Di Stefano S, Crescenzi M, Natali PG, Sacchi A: Alpha 6 beta 4 and alpha 6 beta 1 integrins associate with ErbB-2 in human carcinoma cell lines. Exp Cell Res 1997, 236:76-85.
44. 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, 126:489-502.
45. Nieto MA, Cano A: The epithelial-mesenchymal transition under control: global programs to regulate epithelial plasticity. Semin Cancer Biol 2012, 22:361-368.
46. Bhowmick NA, Zent R, Ghiassi M, McDonnell M, Moses HL: Integrin beta 1 signaling is necessary for transforming growth factor-beta activation of p38MAPK and epithelial plasticity. J Biol Chem 2001, 276:46707-46713.
47. Parvani JG, Galliher-Beckley AJ, Schiemann BJ, Schiemann WP: Targeted inactivation of β1 integrin induces β3 integrin switching, which drives breast cancer metastasis by TGF-β. Mol Biol Cell 2013, 24:3449-3459.
48. Ueda Y, Wang S, Dumont N, Yi JY, Koh Y, Arteaga CL: Overexpression of HER2 (erbB2) in human breast epithelial cells unmasks transforming growth factor beta-induced cell motility. J Biol Chem 2004, 279:24505-24513.
49. Beaty BT, Sharma VP, Bravo-Cordero JJ, Simpson MA, Eddy RJ, Koleske AJ, Condeelis J: β1 integrin regulates Arg to promote invadopodial maturation and matrix degradation. Mol Biol Cell 2013, 24:1661-1675.
50. Shibue T, Brooks MW, Weinberg RA: An integrin-linked machinery of cytoskeletal regulation that enables experimental tumor initiation and metastatic colonization. Cancer Cell 2013, 24:481-498.
51. Barkan D, El Touny LH, Michalowski AM, Smith JA, Chu I, Davis AS, Webster JD, Hoover S, Simpson RM, Gauldie J, Green JE: Metastatic growth from dormant cells induced by a col-I-enriched fibrotic environment. Cancer Res 2010, 70:5706-5716.
52. 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, 12:863-879.
53. Gupton SL, Riquelme D, Hughes-Alford SK, Tadros J, Rudina SS, Hynes RO, Lauffenburger D, Gertler FB: Mena binds a5 integrin directly and modulates a5β1 function. J Cell Biol 2012, 198:657-676.
54. Di Modugno F, Iapicca P, Boudreau A, Mottolese M, Terrenato I, Perracchio L, Carstens RP, Santoni A, Bissell MJ, Nisticò P: Splicing program of human MENA produces a previously undescribed isoform associated with invasive, mesenchymal-like breast tumors. Proc Natl Acad Sci U S A 2012, 109:19280-19285.
55. Carbonell WS, DeLay M, Jahangiri A, Park CC, Aghi MK: v1 integrin targeting potentiates antiangiogenic therapy and inhibits the growth of bevacizumab-resistant glioblastoma. Cancer Res 2013, 73:3145-3154.
56. Vieira AF, Ribeiro AS, Dionísio MR, Sousa B, Nobre AR, Albergaria A, Santiago-Gómez A, Mendes N, Gerhard R, Schmitt F, Clarke RB, Paredes J: P-cadherin signals through the laminin receptor a6β4 integrin to induce stem cell and invasive properties in basal-like breast cancer cells. Oncotarget 2014, 5:679-692.
57. 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, 146:1147-1160.
58. Wang F, Weaver VM, Petersen OW, Larabell CA, Dedhar S, Briand P, Lupu R, Bissell MJ: Reciprocal interactions between beta1-integrin and epidermal growth factor receptor in three-dimensional basement membrane breast cultures: a different perspective in epithelial biology. Proc Natl Acad Sci U S A 1998, 95:14821-14826.
59. Moro L, Dolce L, Cabodi S, Bergatto E, Boeri Erba E, Smeriglio M, Turco E, Retta SF, Giuffrida MG, Venturino M, Godovac-Zimmermann J, Conti A, Schaefer E, Beguinot L, Tacchetti C, Gaggini P, Silengo L, Tarone G, Defilippi P: Integrin-induced epidermal growth factor (EGF) receptor activation requires c-Src and p130Cas and leads to phosphorylation of specific EGF receptor tyrosines. J Biol Chem 2002, 277:9405-9414.
60. Bridgewater RE, Norman JC, Caswell PT: Integrin trafficking at a glance. J Cell Sci 2012, 125:3695-3701.
61. Onodera Y, Nam JM, Hashimoto A, Norman JC, Shirato H, Hashimoto S, Sabe H: Rab5c promotes AMAP1-PRKD2 complex formation to enhance β1 integrin recycling in EGF-induced cancer invasion. J Cell Biol 2012, 197:983-996.
62. Mercurio AM, Rabinovitz I, Shaw LM: The alpha 6 beta 4 integrin and epithelial cell migration. Curr Opin Cell Biol 2001, 13:541-545.
63. Golden EB, Pellicciotta I, Demaria S, Barcellos-HoffMH, Formenti SC: The convergence of radiation and immunogenic cell death signaling pathways. Front Oncol 2012, 2:1-13.
64. Park CC, Zhang HJ, Yao ES, Park CJ, Bissell MJ: Beta1 integrin inhibition dramatically enhances radiotherapy efficacy in human breast cancer xenografts. Cancer Res 2008, 68:4398-4405.
65. Ahmed KM, Zhang H, Park CC: NF-κB regulates radioresistance mediated by β1-integrin in three-dimensional culture of breast cancer cells. Cancer Res 2013, 73:3737-3748.
66. Eke I, Deuse Y, Hehlgans S, Gurtner K, Krause M, Baumann M, Shevchenko A, Sandfort V, Cordes N: β1 Integrin/FAK/cortactin signaling is essential for human head and neck cancer resistance to radiotherapy. J Clin Invest 2012, 122:1529-1540.
67. Spencer VA, Costes S, Inman JL, Xu R, Chen J, Hendzel MJ, Bissell MJ: Depletion of nuclear actin is a key mediator of quiescence in epithelial cells. J Cell Sci 2011, 124:123-132.
68. Boudreau N, Sympson CJ, Werb Z, Bissell MJ: Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 1995, 267:891-893.
69. Ghajar CM, Peinado H, Mori H, Matei IR, Evason KJ, Brazier H, Almeida D, Koller A, Hajjar KA, Stainier DY, Chen EI, Lyden D, Bissell MJ: The perivascular niche regulates breast tumour dormancy. Nat Cell Biol 2013, 15:807-817.
70. Thundimadathil J: Cancer treatment using peptides: current therapies and future prospects. J Amino Acids 2012, 2012:967347.