ADAM8 expression in invasive breast cancer promotes tumor dissemination and metastasis

EMBO Molecular Medicine

Volumn 6, Issue 2, 2014, Pages 278-294

  Romagnoli, Mathilde ^a   Mineva, Nora D ^a   Polmear, Michael ^b   Conrad, Catharina ^c   Srinivasan, Srimathi ^a   Loussouarn, Delphine ^d   Barillé Nion, Sophie ^d   Georgakoudi, Irene ^b   Dagg, Áine ^e,f   Mcdermott, Enda W ^f   Duffy, Michael J ^f   Mcgowan, Patricia M ^e,f   Schlomann, Uwe ^c   Parsons, Maddy ^g   Bartsch, Jörg W ^c   Sonenshein, Gail E ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Tufts University   (United States)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

^d Team 12   (France)

^e ST VINCENT S UNIVERSITY HOSPITAL   (Ireland)

^f UNIVERSITY COLLEGE DUBLIN   (Ireland)

^g KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

ADAM8; Breast cancer; Cancer progression; Metastasis; Therapeutic target; Triple negative

Indexed keywords

ADAM PROTEIN; ADAM8 PROTEIN; BETA1 INTEGRIN; UNCLASSIFIED DRUG; VASCULOTROPIN A;

ANGIOGENESIS; ARTICLE; BRAIN METASTASIS; BREAST CANCER; CELL MIGRATION; CIRCULATING TUMOR CELL; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; METASTASIS; PHENOTYPE; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRIPLE NEGATIVE BREAST CANCER; TUMOR INVASION; VASCULARIZATION;

ADAM PROTEINS; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD29; BREAST NEOPLASMS; CELL ADHESION; CELL HYPOXIA; CELL MOVEMENT; CELL PROLIFERATION; ENDOTHELIAL CELLS; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; MEMBRANE PROTEINS; MICE; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASTIC CELLS, CIRCULATING; NEOVASCULARIZATION, PATHOLOGIC; PHENOTYPE; PROGNOSIS; PROTEIN STRUCTURE, TERTIARY; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELLS, CULTURED;

EID: 84893770998     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201303373     Document Type: Article

References (46)

1. Adams RH, Alitalo K (2007) Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 8: 464-478
2. Avraamides CJ, Garmy-Susini B, Varner JA (2008) Integrins in angiogenesis and lymphangiogenesis. Nat Rev Cancer 8: 604-617
3. Baren JP, Stewart GD, Stokes A, Gray K, Pennington CJ, O'Neill R, Deans DA, Paterson-Brown S, Riddick AC, Edwards DR et al (2012) mRNA profiling of the cancer degradome in oesophago-gastric adenocarcinoma. Br J Cancer 107: 143-149
4. Bartsch JW, Wildeboer D, Koller G, Naus S, Rittger A, Moss ML, Minai Y, Jockusch H (2010) Tumor necrosis factor-alpha (TNF-alpha) regulates shedding of TNF-alpha receptor 1 by the metalloprotease-disintegrin ADAM8: evidence for a protease-regulated feedback loop in neuroprotection. J Neurosci 30: 12210-12218
5. Bergers G, Benjamin LE (2003) Tumorigenesis and the angiogenic switch. Nat Rev Cancer 3: 401-410
6. Bertucci F, Finetti P, Birnbaum D (2012) Basal breast cancer: a complex and deadly molecular subtype. Curr Mol Med 12: 96-110
7. Boyle P (2012) Triple-negative breast cancer: epidemiological considerations and recommendations. Ann Oncol 23(Suppl. 6): vi7-12
8. Bridges LC, Bowditch RD (2005) ADAM-Integrin Interactions: potential integrin regulated ectodomain shedding activity. Curr Pharm Des 11: 837-847
9. Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Matera J, Miller MC, Reuben JM, Doyle GV, Allard WJ, Terstappen LW et al (2004) Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med 351: 781-791
10. Desgrosellier JS, Cheresh DA (2010) Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 10: 9-22
11. Duffy MJ, McKiernan E, O'Donovan N, McGowan PM (2009) Role of ADAMs in cancer formation and progression. Clin Cancer Res 15: 1140-1144
12. Duffy MJ, Mullooly M, O'Donovan N, Sukor S, Crown J, Pierce A, McGowan PM (2011) The ADAMs family of proteases: new biomarkers and therapeutic targets for cancer? Clin Proteomics 8: 9.
13. Eyles J, Puaux AL, Wang X, Toh B, Prakash C, Hong M, Tan TG, Zheng L, Ong LC, Jin Y et al (2010) Tumor cells disseminate early, but immunosurveillance limits metastatic outgrowth, in a mouse model of melanoma. J Clin Invest 120: 2030-2039
14. Greiner C, Hunter M, Rius F, Huang P, Georgakoudi I (2011) Confocal backscattering-based detection of leukemic cells in flowing blood samples. Cytometry A 79: 874-883
15. Harris AL (2002) Hypoxia-a key regulatory factor in tumour growth. Nat Rev Cancer 2: 38-47
16. Hawinkels LJ, Zuidwijk K, Verspaget HW, de Jonge-Muller ES, van Duijn W, Ferreira V, Fontijn RD, David G, Hommes DW, Lamers CB et al (2008) VEGF release by MMP-9 mediated heparan sulphate cleavage induces colorectal cancer angiogenesis. Eur J Cancer 44: 1904-1913
17. Hwu D, Boutrus S, Greiner C, DiMeo T, Kuperwasser C, Georgakoudi I (2011) Assessment of the role of circulating breast cancer cells in tumor formation and metastatic potential using in vivo flow cytometry. J Biomed Opt 16: 040501.
18. Kelly K, Hutchinson G, Nebenius-Oosthuizen D, Smith AJ, Bartsch JW, Horiuchi K, Rittger A, Manova K, Docherty AJ, Blobel CP (2005) Metalloprotease-disintegrin ADAM8: expression analysis and targeted deletion in mice. Dev Dyn 232: 221-231
19. Koller G, Schlomann U, Golfi P, Ferdous T, Naus S, Bartsch JW (2009) ADAM8/MS2/CD156, an emerging drug target in the treatment of inflammatory and invasive pathologies. Curr Pharm Des 15: 2272-2281
20. Lee S, Jilani SM, Nikolova GV, Carpizo D, Iruela-Arispe ML (2005) Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors. J Cell Biol 169: 681-691
21. Lee SB, Schramme A, Doberstein K, Dummer R, Abdel-Bakky MS, Keller S, Altevogt P, Oh ST, Reichrath J, Oxmann D et al (2010) ADAM10 is upregulated in melanoma metastasis compared with primary melanoma. J Invest Dermatol 130: 763-773
22. Linderholm BK, Hellborg H, Johansson U, Elmberger G, Skoog L, Lehtio J, Lewensohn R (2009) Significantly higher levels of vascular endothelial growth factor (VEGF) and shorter survival times for patients with primary operable triple-negative breast cancer. Ann Oncol 20: 1639-1646
23. Lohela M, Bry M, Tammela T, Alitalo K (2009) VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol 21: 154-165
24. Majmundar AJ, Wong WJ, Simon MC (2010) Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 40: 294-309
25. Maretzky T, Evers A, Zhou W, Swendeman SL, Wong PM, Rafii S, Reiss K, Blobel CP (2011) Migration of growth factor-stimulated epithelial and endothelial cells depends on EGFR transactivation by ADAM17. Nat Commun 2: 229.
26. Mierke CT (2008) Role of the endothelium during tumor cell metastasis: is the endothelium a barrier or a promoter for cell invasion and metastasis? J Biophys 2008: 183516.
27. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, Viale A, Olshen AB, Gerald WL, Massague J (2005) Genes that mediate breast cancer metastasis to lung. Nature 436: 518-524
28. Mohammed RA, Green A, El-Shikh S, Paish EC, Ellis IO, Martin SG (2007) Prognostic significance of vascular endothelial cell growth factors -A, -C and -D in breast cancer and their relationship with angio- and lymphangiogenesis. Br J Cancer 96: 1092-1100
29. Naumov GN, Akslen LA, Folkman J (2006) Role of angiogenesis in human tumor dormancy: animal models of the angiogenic switch. Cell Cycle 5: 1779-1787
30. Pierce A, Saldova R, Abd Hamid UM, Abrahams JL, McDermott EW, Evoy D, Duffy MJ, Rudd PM (2010) Levels of specific glycans significantly distinguish lymph node-positive from lymph node-negative breast cancer patients. Glycobiology 20: 1283-1288
31. Price EA, Coombe DR, Murray JC (1996) beta-1 Integrins mediate tumour cell adhesion to quiescent endothelial cells in vitro. Br J Cancer 74: 1762-1766
32. Rao H, Lu G, Kajiya H, Garcia-Palacios V, Kurihara N, Anderson J, Patrene K, Sheppard D, Blair HC, Windle JJ et al (2006) Alpha9beta1: a novel osteoclast integrin that regulates osteoclast formation and function. J Bone Miner Res 21: 1657-1665
33. Richens J, Fairclough L, Ghaemmaghami AM, Mahdavi J, Shakib F, Sewell HF (2007) The detection of ADAM8 protein on cells of the human immune system and the demonstration of its expression on peripheral blood B cells, dendritic cells and monocyte subsets. Immunobiology 212: 29-38
34. Romagnoli M, Belguise K, Yu Z, Wang X, Landesman-Bollag E, Seldin DC, Chalbos D, Barille-Nion S, Jezequel P, Seldin ML et al (2012) Epithelial-to-mesenchymal transition induced by TGF-beta1 is mediated by Blimp-1-dependent repression of BMP-5. Cancer Res 72: 6268-6278
35. Roy R, Rodig S, Bielenberg D, Zurakowski D, Moses MA (2011a) ADAM12 transmembrane and secreted isoforms promote breast tumor growth: a distinct role for ADAM12-S protein in tumor metastasis. J Biol Chem 286: 20758-20768
36. Roy R, Zurakowski D, Pories S, Moss ML, Moses MA (2011b) Potential of fluorescent metalloproteinase substrates for cancer detection. Clin Biochem 44: 1434-1439
37. Schlomann U, Wildeboer D, Webster A, Antropova O, Zeuschner D, Knight CG, Docherty AJ, Lambert M, Skelton L, Jockusch H et al (2002) The metalloprotease disintegrin ADAM8. Processing by autocatalysis is required for proteolytic activity and cell adhesion. J Biol Chem 277: 48210-48219
38. Scott J, Kuhn P, Anderson AR (2012) Unifying metastasis-integrating intravasation, circulation and end-organ colonization. Nat Rev Cancer 12: 445-446
39. Sriraman V, Eichenlaub-Ritter U, Bartsch JW, Rittger A, Mulders SM, Richards JS (2008) Regulated expression of ADAM8 (a disintegrin and metalloprotease domain 8) in the mouse ovary: evidence for a regulatory role of luteinizing hormone, progesterone receptor, and epidermal growth factor-like growth factors. Biol Reprod 78: 1038-1048
40. Steeg PS (2006) Tumor metastasis: mechanistic insights and clinical challenges. Nat Med 12: 895-904
41. Toh B, Chew V, Dai X, Khoo K, Tham M, Wai LE, Hubert S, Velumani S, Zhi L, Huang C et al (2012) Immune predictors of cancer progression. Immunol Res 53: 229-234
42. Valkovskaya N, Kayed H, Felix K, Hartmann D, Giese NA, Osinsky SP, Friess H, Kleeff J (2007) ADAM8 expression is associated with increased invasiveness and reduced patient survival in pancreatic cancer. J Cell Mol Med 11: 1162-1174
43. van de Vijver MJ, He YD, van't Veer LJ, Dai H, Hart AA, Voskuil DW, Schreiber GJ, Peterse JL, Roberts C, Marton MJ et al (2002) A gene-expression signature as a predictor of survival in breast cancer. N Engl J Med 347: 1999-2009
44. Wang X, Belguise K, Kersual N, Kirsch KH, Mineva ND, Galtier F, Chalbos D, Sonenshein GE (2007) Oestrogen signalling inhibits invasive phenotype by repressing RelB and its target BCL2. Nat Cell Biol 9: 470-478
45. Yoshiyama K, Higuchi Y, Kataoka M, Matsuura K, Yamamoto S (1997) CD156 (human ADAM8): expression, primary amino acid sequence, and gene location. Genomics 41: 56-62
46. Zhong JL, Poghosyan Z, Pennington CJ, Scott X, Handsley MM, Warn A, Gavrilovic J, Honert K, Kruger A, Span PN et al (2008) Distinct functions of natural ADAM-15 cytoplasmic domain variants in human mammary carcinoma. Mol Cancer Res 6: 383-394