Caveolin-1 (P132L), a common breast cancer mutation, confers mammary cell invasiveness and defines a novel stem cell/metastasis-associated gene signature

American Journal of Pathology

Volumn 174, Issue 5, 2009, Pages 1650-1662

  Bonuccelli, Gloria ^a,b   Casimiro, Mathew C ^a,b   Sotgia, Federica ^a,b,c   Wang, Chenguang ^a,b   Liu, Manran ^a,b   Katiyar, Sanjay ^a,b   Zhou, Jie ^a,b   Dew, Elliott ^a,b   Capozza, Franco ^a,b   Daumer, Kristin M ^a,b   Minetti, Carlo ^c   Milliman, Janet N ^a,b   Alpy, Fabien ^d   Rio, Marie Christine ^d   Tomasetto, Catherine ^d   Mercier, Isabelle ^a,b   Flomenberg, Neal ^a   Frank, Philippe G ^a,b   Pestell, Richard G ^a,b   Lisanti, Michael P ^a,b,c  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c UNIVERSITY OF GENOA   (Italy)

^d INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; INTEGRIN; MATRIX PROTEIN; PROTEIN TYROSINE KINASE; PROTEINASE; ESR1 PROTEIN, HUMAN; ESTROGEN RECEPTOR ALPHA; TUMOR MARKER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; BREAST CELL; CANCER RECURRENCE; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CELL STRAIN; CELL STRAIN MET 1; FEMALE; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE MUTATION; METASTASIS; MOUSE; NONHUMAN; ORTHOTOPIC TRANSPLANTATION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; STEM CELL; ANIMAL; CANCER INVASION; CANCER STEM CELL; CELL MOTION; CELL PROLIFERATION; DNA MICROARRAY; ENZYME IMMUNOASSAY; EXPERIMENTAL NEOPLASM; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MAMMARY GLAND; METABOLISM; MUTATION; PATHOLOGY; PROGNOSIS; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CAVEOLIN 1; CELL MOVEMENT; CELL PROLIFERATION; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOENZYME TECHNIQUES; MAMMARY GLANDS, HUMAN; MAMMARY NEOPLASMS, ANIMAL; MICE; MUTATION; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROGNOSIS; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL;

EID: 65649133092     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2009.080648     Document Type: Article

References (86)

1. Hayashi K, Matsuda S, Machida K, Yamamoto T, Fukuda Y, Nimura Y, Hayakawa T, Hamaguchi M: Invasion activating caveolin-1 mutation in human scirrhous breast cancers. Cancer Res 2001, 61:2361-2364 (Pubitemid 32685805)
2. Li T, Sotgia F, Vuolo MA, Li M, Yang WC, Pestell RG, Sparano JA, Lisanti MP: Caveolin-1 mutations in human breast cancer: functional association with estrogen receptor alpha-positive status. Am J Pathol 2006, 168:1998-2013
3. Lee H, Park DS, Razani B, Russell RG, Pestell RG, Lisanti MP: Caveolin-1 mutations (P132L and null) and the pathogenesis of breast cancer: caveolin-1 (P132L) behaves in a dominant-negative manner and caveolin-1 (-/-) null mice show mammary epithelial cell hyperplasia. Am J Pathol 2002, 161:1357-1369
4. Park DS, Lee H, Frank PG, Razani B, Nguyen AV, Parlow AF, Russell RG, Hulit J, Pestell RG, Lisanti MP: Caveolin-1-deficient mice show accelerated mammary gland development during pregnancy, premature lactation, and hyperactivation of the Jak-2/STAT5a signaling cascade. Mol Biol Cell 2002, 13:3416-3430 (Pubitemid 35191364)
5. Williams TM, Cheung MW, Park DS, Razani B, Cohen AW, Muller WJ, Di Vizio D, Chopra NG, Pestell RG, Lisanti MP: Loss of caveolin-1 gene expression accelerates the development of dysplastic mammary lesions in tumor-prone transgenic mice. Mol Biol Cell 2003, 14:1027-1042 (Pubitemid 36337450)
6. Williams TM, Lee H, Cheung MW, Cohen AW, Razani B, Iyengar P, Scherer PE, Pestell RG, Lisanti MP: Combined loss of INK4a and caveolin-1 synergistically enhances cell proliferation and oncogene-induced tumorigenesis. J Biol Chem 2004, 279:24745-24756
7. Williams TM, Medina F, Badano I, Hazan RB, Hutchinson J, Muller WJ, Chopra NG, Scherer PE, Pestell RG, Lisanti MP: Caveolin-1 gene disruption promotes mammary tumorigenesis and dramatically enhances lung metastasis in vivo: role of Cav-1 in cell invasiveness and matrix metalloproteinase (MMP-2/9) secretion. J Biol Chem 2004, 279:51630-51646 (Pubitemid 40017914)
8. Williams TM, Lisanti MP: Caveolin-1 in oncogenic transformation, cancer, and metastasis. Am J Physiol 2005, 288:C494-C506 (Pubitemid 40229478)
9. Bouras T, Lisanti MP, Pestell RG: Caveolin-1 in breast cancer. Cancer Biol Ther 2004, 3:931-941 (Pubitemid 41351015)
10. Tang Z, Okamoto T, Boontrakulpoontawee P, Katada T, Otsuka AJ, Lisanti MP: Identification, sequence, and expression of an invertebrate caveolin gene family from the nematode Caenorhabditis elegans: implications for the molecular evolution of mammalian caveolin genes. J Biol Chem 1997, 272:2437-2445 (Pubitemid 27058533)
11. Minetti C, Sotgia F, Bruno C, Scartezzini P, Broda P, Bado M, Masetti E, Mazzocco P, Egeo A, Donati MA, Volonte' D, Galbiati F, Cordone G, Bricarelli FD, Lisanti MP, Zara F: Mutations in the caveolin-3 gene cause autosomal dominant limb-girdle muscular dystrophy. Nat Genet 1998, 18:365-368 (Pubitemid 28158166)
12. Galbiati F, Volonte D, Minetti C, Bregman DB, Lisanti MP: Limb-girdle muscular dystrophy (LGMD-1C) mutants of caveolin-3 undergo ubiquitination and proteasomal degradation. Treatment with proteasomal inhibitors blocks the dominant negative effect of LGMD-1C mutanta and rescues wild-type caveolin-3. J Biol Chem 2000, 275:37702-37711
13. Galbiati F, Volonte D, Engelman JA, Watanabe G, Burk R, Pestell RG, Lisanti MP: Targeted downregulation of caveolin-1 is sufficient to drive cell transformation and hyperactivate the p42/44 MAP kinase cascade. EMBO J 1998, 17:6633-6648 (Pubitemid 28521797)
14. Borowsky AD, Namba R, Young LJ, Hunter KW, Hodgson JG, Tepper CG, McGoldrick ET, Muller WJ, Cardiff RD, Gregg JP: Syngeneic mouse mammary carcinoma cell lines: two closely related cell lines with divergent metastatic behavior. Clin Exp Metastasis 2005, 22:47-59 (Pubitemid 41185861)
15. Namba R, Young LJ, Abbey CK, Kim L, Damonte P, Borowsky AD, Qi J, Tepper CG, MacLeod CL, Cardiff RD, Gregg JP: Rapamycin inhibits growth of premalignant and malignant mammary lesions in a mouse model of ductal carcinoma in situ. Clin Cancer Res 2006, 12:2613-2621
16. Alpy F, Boulay A, Moog-Lutz C, Andarawewa KL, Degot S, Stoll I, Rio MC, Tomasetto C: Metastatic lymph node 64 (MLN64), a gene overexpressed in breast cancers, is regulated by Sp/KLF transcription factors. Oncogene 2003, 22:3770-3780 (Pubitemid 36760739)
17. Alpy F, Latchumanan VK, Kedinger V, Janoshazi A, Thiele C, Wendling C, Rio MC, Tomasetto C: Functional characterization of the MENTAL domain. J Biol Chem 2005, 280:17945-17952 (Pubitemid 41389036)
18. Alpy F, Stoeckel ME, Dierich A, Escola JM, Wendling C, Chenard MP, Vanier MT, Gruenberg J, Tomasetto C, Rio MC: The steroidogenic acute regulatory protein homolog MLN64, a late endosomal cholesterol-binding protein. J Biol Chem 2001, 276:4261-4269 (Pubitemid 37371514)
19. Alpy F, Tomasetto C: Give lipids a START: the StAR-related lipid transfer (START) domain in mammals. J Cell Sci 2005, 118:2791-2801 (Pubitemid 41136357)
20. Alpy F, Wendling C, Rio MC, Tomasetto C: MENTHO, a MLN64 homologue devoid of the START domain. J Biol Chem 2002, 277:50780-50787 (Pubitemid 36042242)
21. Degot S, Le Hir H, Alpy F, Kedinger V, Stoll I, Wendling C, Seraphin B, Rio MC, Tomasetto C: Association of the breast cancer protein MLN51 with the exon junction complex via its speckle localizer and RNA binding module. J Biol Chem 2004, 279:33702-33715 (Pubitemid 39063020)
22. Kedinger V, Alpy F, Tomasetto C, Thisse C, Thisse B, Rio MC: Spatial and temporal distribution of the traf4 genes during zebrafish development. Gene Expr Patterns 2005, 5:545-552 (Pubitemid 40331396)
23. Scherer PE, Lederkremer GZ, Williams S, Fogliano M, Baldini G, Lodish HF: Cab45, a novel (Ca2+)-binding protein localized to the Golgi lumen. J Cell Biol 1996, 133:257-268 (Pubitemid 26132528)
24. Williams TM, Sotgia F, Lee H, Hassan G, Di Vizio D, Bonuccelli G, Capozza F, Mercier I, Rui H, Pestell RG, Lisanti MP: Stromal and epithelial caveolin-1 both confer a protective effect against mammary hyperplasia and tumorigenesis: caveolin-1 antagonizes cyclin d1 function in mammary epithelial cells. Am J Pathol 2006, 169:1784-1801
25. Albini A, Iwamoto Y, Kleinman HK, Martin GR, Aaronson SA, Kozlowski JM, McEwan RN: A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res 1987, 47:3239-3245 (Pubitemid 17082655)
26. Hulit J, Suyama K, Chung S, Keren R, Agiostratidou G, Shan W, Dong X, Williams TM, Lisanti MP, Knudsen K, Hazan RB: N-cadherin signaling potentiates mammary tumor metastasis via enhanced extracellular signal-regulated kinase activation. Cancer Res 2007, 67:3106-3116 (Pubitemid 46724847)
27. Grigoriadis A, Mackay A, Reis-Filho JS, Steele D, Iseli C, Stevenson BJ, Jongeneel CV, Valgeirsson H, Fenwick K, Iravani M, Leao M, Simpson AJ, Strausberg RL, Jat PS, Ashworth A, Neville AM, O'Hare MJ: Establishment of the epithelial-specific transcriptome of normal and malignant human breast cells based on MPSS and array expression data. Breast Cancer Res 2006, 8:R56
28. Edelman E, Porrello A, Guinney J, Balakumaran B, Bild A, Febbo PG, Mukherjee S: Analysis of sample set enrichment scores: assaying the enrichment of sets of genes for individual samples in genome-wide expression profiles. Bioinformatics 2006, 22:e108-e116 (Pubitemid 44307811)
29. Moog-Lutz C, Tomasetto C, Regnier CH, Wendling C, Lutz Y, Muller D, Chenard MP, Basset P, Rio MC: MLN64 exhibits homology with the steroidogenic acute regulatory protein (STAR) and is over-expressed in human breast carcinomas. Int J Cancer 1997, 71:183-191 (Pubitemid 27252988)
30. Tomasetto C, Regnier C, Moog-Lutz C, Mattei MG, Chenard MP, Lidereau R, Basset P, Rio MC: Identification of four novel human genes amplified and overexpressed in breast carcinoma and localized to the q11-q21.3 region of chromosome 17. Genomics 1995, 28:367-376
31. Abdollahi A, Pisarcik D, Roberts D, Weinstein J, Cairns P, Hamilton TC: LOT1 (PLAGL1/ZAC1), the candidate tumor suppressor gene at chromosome 6q24-25, is epigenetically regulated in cancer. J Biol Chem 2003, 278:6041-6049 (Pubitemid 36800855)
32. Deng Y, Wu X: Peg3/Pw1 promotes p53-mediated apoptosis by inducing Bax translocation from cytosol to mitochondria. Proc Natl Acad Sci USA 2000, 97:12050-12055
33. Reis-Filho JS, Steele D, Di Palma S, Jones RL, Savage K, James M, Milanezi F, Schmitt FC, Ashworth A: Distribution and significance of nerve growth factor receptor (NGFR/p75NTR) in normal, benign and malignant breast tissue. Mod Pathol 2006, 19:307-319 (Pubitemid 43117617)
34. Kovacevic Z, Richardson DR: The metastasis suppressor, Ndrg-1: a new ally in the fight against cancer. Carcinogenesis 2006, 27:2355-2366
35. Gaul MD, Guo Y, Affleck K, Cockerill GS, Gilmer TM, Griffin RJ, Guntrip S, Keith BR, Knight WB, Mullin RJ, Murray DM, Rusnak DW, Smith K, Tadepalli S, Wood ER, Lackey K: Discovery and biological evaluation of potent dual ErbB-2/EGFR tyrosine kinase inhibitors: 6-thiazolylquinazolines. Bioorg Med Chem Lett 2003, 13:637-640 (Pubitemid 36298457)
36. Christensen JG, Schreck R, Burrows J, Kuruganti P, Chan E, Le P, Chen J, Wang X, Ruslim L, Blake R, Lipson KE, Ramphal J, Do S, Cui JJ, Cherrington JM, Mendel DB: A selective small molecule inhibitor of c-Met kinase inhibits c-Met-dependent phenotypes in vitro and exhibits cytoreductive antitumor activity in vivo. Cancer Res 2003, 63:7345-7355 (Pubitemid 37413476)
37. Sawyer JS, Anderson BD, Beight DW, Campbell RM, Jones ML, Herron DK, Lampe JW, McCowan JR, McMillen WT, Mort N, Parsons S, Smith EC, Vieth M, Weir LC, Yan L, Zhang F, Yingling JM: Synthesis and activity of new aryl- and heteroaryl-substituted pyrazole inhibitors of the transforming growth factor-beta type I receptor kinase domain. J Med Chem 2003, 46:3953-3956 (Pubitemid 37122441)
38. Gentile A, Trusolino L, Comoglio PM: The Met tyrosine kinase receptor in development and cancer. Cancer Metastasis Rev 2008, 27:85-94
39. Boccaccio C, Comoglio PM: Invasive growth: a MET-driven genetic programme for cancer and stem cells. Nat Rev Cancer 2006, 6:637-645 (Pubitemid 44140861)
40. Mazzone M, Comoglio PM: The Met pathway: master switch and drug target in cancer progression. FASEB J 2006, 20:1611-1621
41. Radisky ES, Radisky DC: Stromal induction of breast cancer: inflammation and invasion. Rev Endocr Metab Disord 2007, 8:279-287 (Pubitemid 47524870)
42. Sleeman JP, Cremers N: New concepts in breast cancer metastasis: tumor initiating cells and the microenvironment. Clin Exp Metastasis 2007, 24:707-715 (Pubitemid 50000183)
43. Strano S, Dell'Orso S, Di Agostino S, Fontemaggi G, Sacchi A, Blandino G: Mutant p53: an oncogenic transcription factor. Oncogene 2007, 26:2212-2219 (Pubitemid 46536646)
44. Li Y, Prives C: Are interactions with p63 and p73 involved in mutant p53 gain of oncogenic function? Oncogene 2007, 26:2220-2225
45. Lozano G: The oncogenic roles of p53 mutants in mouse models. Curr Opin Genet Dev 2007, 17:66-70 (Pubitemid 46109293)
46. Menéndez JA, Mehmi I, Griggs DW, Lupu R: The angiogenic factor CYR61 in breast cancer: molecular pathology and therapeutic perspectives. Endocr Relat Cancer 2003, 10:141-152 (Pubitemid 36758643)
47. Chen Y, Du XY: Functional properties and intracellular signaling of CCN1/Cyr61. J Cell Biochem 2007, 100:1337-1345 (Pubitemid 46515568)
48. Schütze N, Schenk R, Fiedler J, Mattes T, Jakob F, Brenner RE: CYR61/CCN1 and WISP3/CCN6 are chemoattractive ligands for human multipotent mesenchymal stroma cells. BMC Cell Biol 2007, 8:45
49. Grote K, Salguero G, Ballmaier M, Dangers M, Drexler H, Schieffer B: The angiogenic factor CCN1 promotes adhesion and migration of circulating CD34+ progenitor cells: potential role in angiogenesis and endothelial regeneration. Blood 2007, 110:877-885 (Pubitemid 47267424)
50. Corbacho AM, Martinez De La Escalera G, Clapp C: Roles of prolactin and related members of the prolactin/growth hormone/placental lactogen family in angiogenesis. J Endocrinol 2002, 173:219-238 (Pubitemid 34552451)
51. Wang XY, Yin Y, Yuan H, Sakamaki T, Okano H, Glazer RI: Musashi1 modulates mammary progenitor cell expansion through proliferin-mediated activation of the Wnt and Notch pathways. Mol Cell Biol 2008, 28:3589-3599
52. Guise TA: Parathyroid hormone-related protein and bone metastases. Cancer 1997, 80:1572-1580 (Pubitemid 27444029)
53. Smid M, Wang Y, Klijn JG, Sieuwerts AM, Zhang Y, Atkins D, Martens JW, Foekens JA: Genes associated with breast cancer metastatic to bone. J Clin Oncol 2006, 24:2261-2267 (Pubitemid 46630655)
54. Jahkola T, Toivonen T, Nordling S, von Smitten K, Virtanen I: Expression of tenascin-C in intraductal carcinoma of human breast: relationship to invasion. Eur J Cancer 1998, 34:1687-1692 (Pubitemid 28474220)
55. Jahkola T, Toivonen T, Virtanen I, von Smitten K, Nordling S, von Boguslawski K, Haglund C, Nevanlinna H, Blomqvist C: Tenascin-C expression in invasion border of early breast cancer: a predictor of local and distant recurrence. Br J Cancer 1998, 78:1507-1513 (Pubitemid 28517549)
56. Jahkola T, Toivonen T, von Smitten K, Blomqvist C, Virtanen I: Expression of tenascin in invasion border of early breast cancer correlates with higher risk of distant metastasis. Int J Cancer 1996, 69:445-447 (Pubitemid 27050519)
57. von Holst A, Egbers U, Prochiantz A, Faissner A: Neural stem/progenitor cells express 20 tenascin C isoforms that are differentially regulated by Pax6. J Biol Chem 2007, 282:9172-9181 (Pubitemid 47093541)
58. Chu EY, Hens J, Andl T, Kairo A, Yamaguchi TP, Brisken C, Glick A, Wysolmerski JJ, Millar SE: Canonical WNT signaling promotes mammary placode development and is essential for initiation of mammary gland morphogenesis. Development 2004, 131:4819-4829 (Pubitemid 39433468)
59. Veltmaat JM, Van Veelen W, Thiery JP, Bellusci S: Identification of the mammary line in mouse by Wnt10b expression. Dev Dyn 2004, 229:349-356 (Pubitemid 38140474)
60. Liu YJ, Xu Y, Yu Q: Full-length ADAMTS-1 and the ADAMTS-1 fragments display pro- and antimetastatic activity, respectively. Oncogene 2006, 25:2452-2467
61. Kang JY, Dolled-Filhart M, Ocal IT, Singh B, Lin CY, Dickson RB, Rimm DL, Camp RL: Tissue microarray analysis of hepatocyte growth factor/Met pathway components reveals a role for Met, matriptase, and hepatocyte growth factor activator inhibitor 1 in the progression of node-negative breast cancer. Cancer Res 2003, 63:1101-1105 (Pubitemid 36278444)
62. Rubino D, Driggers P, Arbit D, Kemp L, Miller B, Coso O, Pagliai K, Gray K, Gutkind S, Segars J: Characterization of Brx, a novel Dbl family member that modulates estrogen receptor action. Oncogene 1998, 16:2513-2526 (Pubitemid 28258583)
63. Wirtenberger M, Tchatchou S, Hemminki K, Klaes R, Schmutzler RK, Bermejo JL, Chen B, Wappenschmidt B, Meindl A, Bartram CR, Burwinkel B: Association of genetic variants in the Rho guanine nucleotide exchange factor AKAP13 with familial breast cancer. Carcinogenesis 2006, 27:593-598 (Pubitemid 43372887)
64. Bühring HJ, Kuci S, Conze T, Rathke G, Bartolovic K, Grunebach F, Scherl-Mostageer M, Brummendorf TH, Schweifer N, Lammers R: CDCP1 identifies a broad spectrum of normal and malignant stem/progenitor cell subsets of hematopoietic and nonhematopoietic origin. Stem Cells 2004, 22:334-343 (Pubitemid 38736617)
65. Uekita T, Jia L, Narisawa-Saito M, Yokota J, Kiyono T, Sakai R: CUB domain-containing protein 1 is a novel regulator of anoikis resistance in lung adenocarcinoma. Mol Cell Biol 2007, 27:7649-7660 (Pubitemid 350033670)
66. Hooper JD, Zijlstra A, Aimes RT, Liang H, Claassen GF, Tarin D, Testa JE, Quigley JP: Subtractive immunization using highly metastatic human tumor cells identifies SIMA135/CDCP1, a 135 kDa cell surface phosphorylated glycoprotein antigen. Oncogene 2003, 22:1783-1794 (Pubitemid 36513138)
67. Bharti S, Inoue H, Bharti K, Hirsch DS, Nie Z, Yoon HY, Artym V, Yamada KM, Mueller SC, Barr VA, Randazzo PA: Src-dependent phosphorylation of ASAP1 regulates podosomes. Mol Cell Biol 2007, 27:8271-8283 (Pubitemid 350234239)
68. Fazioli F, Minichiello L, Matoskova B, Wong WT, Di Fiore PP: eps15, a novel tyrosine kinase substrate, exhibits transforming activity. Mol Cell Biol 1993, 13:5814-5828 (Pubitemid 23260682)
69. Kalinichenko VV, Gusarova GA, Kim IM, Shin B, Yoder HM, Clark J, Sapozhnikov AM, Whitsett JA, Costa RH: Foxf1 haploinsufficiency reduces Notch-2 signaling during mouse lung development. Am J Physiol 2004, 286:L521-L530 (Pubitemid 38233623)
70. Malin D, Kim IM, Boetticher E, Kalin TV, Ramakrishna S, Meliton L, Ustiyan V, Zhu X, Kalinichenko VV: Forkhead box F1 is essential for migration of mesenchymal cells and directly induces integrin-beta3 expression. Mol Cell Biol 2007, 27:2486-2498 (Pubitemid 46581341)
71. Ke Y, Wu D, Princen F, Nguyen T, Pang Y, Lesperance J, Muller WJ, Oshima RG, Feng GS: Role of Gab2 in mammary tumorigenesis and metastasis. Oncogene 2007, 26:4951-4960 (Pubitemid 47172654)
72. Bentires-Alj M, Gil SG, Chan R, Wang ZC, Wang Y, Imanaka N, Harris LN, Richardson A, Neel BG, Gu H: A role for the scaffolding adapter GAB2 in breast cancer. Nat Med 2006, 12:114-121 (Pubitemid 43050085)
73. van der Voort R, Taher TE, Wielenga VJ, Spaargaren M, Prevo R, Smit L, David G, Hartmann G, Gherardi E, Pals ST: Heparan sulfate-modified CD44 promotes hepatocyte growth factor/scatter factor-induced signal transduction through the receptor tyrosine kinase c-Met. J Biol Chem 1999, 274:6499-6506 (Pubitemid 29111066)
74. Derksen PW, Keehnen RM, Evers LM, van Oers MH, Spaargaren M, Pals ST: Cell surface proteoglycan syndecan-1 mediates hepatocyte growth factor binding and promotes Met signaling in multiple myeloma. Blood 2002, 99:1405-1410 (Pubitemid 34547098)
75. Abdel-Ghany M, Cheng HC, Elble RC, Pauli BU: The breast cancer beta 4 integrin and endothelial human CLCA2 mediate lung metastasis. J Biol Chem 2001, 276:25438-25446 (Pubitemid 37413033)
76. Carraway III KL, Sweeney C: Co-opted integrin signaling in ErbB2-induced mammary tumor progression. Cancer Cell 2006, 10:93-95 (Pubitemid 44175911)
77. Trusolino L, Bertotti A, Comoglio PM: A signaling adapter function for alpha6beta4 integrin in the control of HGF-dependent invasive growth. Cell 2001, 107:643-654 (Pubitemid 34014865)
78. Bertotti A, Comoglio PM, Trusolino L: Beta4 integrin activates a Shp2- Src signaling pathway that sustains HGF-induced anchorage-independent growth. J Cell Biol 2006, 175:993-1003
79. Greco S, Elia MG, Muscella A, Romano S, Storelli C, Marsigliante S: Bradykinin stimulates cell proliferation through an extracellular-regulated kinase 1 and 2-dependent mechanism in breast cancer cells in primary culture. J Endocrinol 2005, 186:291-301 (Pubitemid 41167398)
80. Greco S, Muscella A, Elia MG, Romano S, Storelli C, Marsigliante S: Mitogenic signalling by B2 bradykinin receptor in epithelial breast cells. J Cell Physiol 2004, 201:84-96 (Pubitemid 39187047)
81. Fulford LG, Reis-Filho JS, Ryder K, Jones C, Gillett CE, Hanby A, Easton D, Lakhani SR: Basal-like grade III invasive ductal carcinoma of the breast: patterns of metastasis and long-term survival. Breast Cancer Res 2007, 9:R4 (Pubitemid 350215157)
82. Gaedcke J, Traub F, Milde S, Wilkens L, Stan A, Ostertag H, Christgen M, von Wasielewski R, Kreipe HH: Predominance of the basal type and HER-2/neu type in brain metastasis from breast cancer. Mod Pathol 2007, 20:864-870 (Pubitemid 47077270)
83. Niki T, Izumi S, Saegusa Y, Taira T, Takai T, Iguchi-Ariga SM, Ariga H: MSSP promotes ras/myc cooperative cell transforming activity by binding to c-Myc. Genes Cells 2000, 5:127-141 (Pubitemid 30120297)
84. Watson MA, Ylagan LR, Trinkaus KM, Gillanders WE, Naughton MJ, Weilbaecher KN, Fleming TP, Aft RL: Isolation and molecular profiling of bone marrow micrometastases identifies TWIST1 as a marker of early tumor relapse in breast cancer patients. Clin Cancer Res 2007, 13:5001-5009 (Pubitemid 47502064)
85. Choesmel V, Anract P, Hoifodt H, Thiery JP, Blin N: A relevant immunomagnetic assay to detect and characterize epithelial cell adhesion molecule-positive cells in bone marrow from patients with breast carcinoma: immunomagnetic purification of micrometastases. Cancer 2004, 101:693-703 (Pubitemid 39030923)
86. Spizzo G, Went P, Dirnhofer S, Obrist P, Simon R, Spichtin H, Maurer R, Metzger U, von Castelberg B, Bart R, Stopatschinskaya S, Kochli OR, Haas P, Mross F, Zuber M, Dietrich H, Bischoff S, Mirlacher M, Sauter G, Gastl G: High Ep-CAM expression is associated with poor prognosis in node-positive breast cancer. Breast Cancer Res Treat 2004, 86:207-213 (Pubitemid 39070963)