Co-expression of MET and CD47 is a novel prognosticator for survival of luminal-type breast cancer patients

Oncotarget

Volumn 5, Issue 18, 2014, Pages 8147-8160

  Baccelli, Irène ^a,b   Stenzinger, Albrecht ^c   Vogel, Vanessa ^a,b,c   Pfitzner, Berit Maria ^d   Klein, Corinna ^a,b   Wallwiener, Markus ^c   Scharpff, Martina ^c   Saini, Massimo ^a,b   Holland Letz, Tim ^b   Sinn, Hans Peter ^c   Schneeweiss, Andreas ^c   Denkert, Carsten ^b,d   Weichert, Wilko ^b,c   Trumpp, Andreas ^a,b  

^a Exp Hematology Group Heidelberg Institute for Stem Cell Technology and Experimental Medicine GGmbH   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Biomarker; Breast cancer; CD47; Circulating tumor cells; MET; Metastasis; Metastasis stem cell; Prognosis

Indexed keywords

CD47 ANTIGEN; SCATTER FACTOR RECEPTOR; CD47 PROTEIN, HUMAN; MET PROTEIN, HUMAN; TUMOR MARKER;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD SAMPLING; BREAST CANCER; CANCER DIAGNOSIS; CANCER PROGNOSIS; CANCER SURVIVAL; CIRCULATING TUMOR CELL; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LUMINAL TYPE PRIMARY BREAST CANCER; LYMPH NODE METASTASIS; MOUSE; NONHUMAN; OVERALL SURVIVAL; PROTEIN EXPRESSION; RETROSPECTIVE STUDY; RISK ASSESSMENT; TUMOR XENOGRAFT; ANIMAL; BREAST NEOPLASMS; CARCINOMA; COMPARATIVE STUDY; DRUG SCREENING; METABOLISM; MIDDLE AGED; MORTALITY; MULTIVARIATE ANALYSIS; NONOBESE DIABETIC MOUSE; PATHOLOGY; PREDICTIVE VALUE; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; RISK FACTOR; SCID MOUSE; SECONDARY; TUMOR EMBOLISM; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTIGENS, CD47; BREAST NEOPLASMS; CARCINOMA; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED NOD; MICE, SCID; MIDDLE AGED; MULTIVARIATE ANALYSIS; NEOPLASTIC CELLS, CIRCULATING; PREDICTIVE VALUE OF TESTS; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; PROTO-ONCOGENE PROTEINS C-MET; RETROSPECTIVE STUDIES; RISK FACTORS; TUMOR MARKERS, BIOLOGICAL; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84907994959     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2385     Document Type: Article

References (58)

1. Siegel R, Naishadham D and Jemal A. Cancer statistics, 2012. CA Cancer J Clin. 2012; 62(1):10-29.
2. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lonning PE, Borresen-Dale AL and et al. Molecular portraits of human breast tumours. Nature. 2000; 406(6797):747-752.
3. Curtis C, Shah SP, Chin SF, Turashvili G, Rueda OM, Dunning MJ, Speed D, Lynch AG, Samarajiwa S, Yuan Y, Graf S, Ha G, Haffari G, Bashashati A, Russell R, McKinney S and et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature. 2012.
4. Sotiriou C and Pusztai L. Gene-expression signatures in breast cancer. N Engl J Med. 2009; 360(8):790-800.
5. Abd El-Rehim DM, Ball G, Pinder SE, Rakha E, Paish C, Robertson JF, Macmillan D, Blamey RW and Ellis IO. High-throughput protein expression analysis using tissue microarray technology of a large well-characterised series identifies biologically distinct classes of breast cancer confirming recent cDNA expression analyses. Int J Cancer. 2005; 116(3):340-350.
6. Makretsov NA, Huntsman DG, Nielsen TO, Yorida E, Peacock M, Cheang MC, Dunn SE, Hayes M, van de Rijn M, Bajdik C and Gilks CB. Hierarchical clustering analysis of tissue microarray immunostaining data identifies prognostically significant groups of breast carcinoma. Clin Cancer Res. 2004; 10(18 Pt 1):6143-6151.
7. Nguyen PL, Taghian AG, Katz MS, Niemierko A, Abi Raad RF, Boon WL, Bellon JR, Wong JS, Smith BL and Harris JR. Breast cancer subtype approximated by estrogen receptor, progesterone receptor, and HER-2 is associated with local and distant recurrence after breast-conserving therapy. J Clin Oncol. 2008; 26(14):2373-2378.
8. Hammond ME, Hayes DF, Dowsett M, Allred DC, Hagerty KL, Badve S, Fitzgibbons PL, Francis G, Goldstein NS, Hayes M, Hicks DG, Lester S, Love R, Mangu PB, McShane L, Miller K and et al. American Society of Clinical Oncology/College Of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J Clin Oncol. 2010; 28(16):2784-2795.
9. Wolff AC, Hammond ME, Hicks DG, Dowsett M, McShane LM, Allison KH, Allred DC, Bartlett JM, Bilous M, Fitzgibbons P, Hanna W, Jenkins RB, Mangu PB, Paik S, Perez EA, Press MF and et al. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update. J Clin Oncol. 2013; 31(31):3997-4013.
10. Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, Davies S, Fauron C, He X, Hu Z, Quackenbush JF, Stijleman IJ, Palazzo J, Marron JS, Nobel AB, Mardis E, and et al Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol. 2009; 27(8):1160-1167.
11. Zaha DC, Lazar E and Lazureanu C. Clinicopathologic features and five years survival analysis in molecular subtypes of breast cancer. Rom J Morphol Embryol. 2010; 51(1):85-89.
12. Pantel K, Alix-Panabieres C and Riethdorf S. Cancer micrometastases. Nat Rev Clin Oncol. 2009; 6(6):339-351.
13. Ghoussoub RA, Dillon DA, D'Aquila T, Rimm EB, Fearon ER and Rimm DL. Expression of c-met is a strong independent prognostic factor in breast carcinoma. Cancer. 1998; 82(8):1513-1520.
14. Raghav KP, Wang W, Liu S, Chavez-MacGregor M, Meng X, Hortobagyi GN, Mills GB, Meric-Bernstam F, Blumenschein GR, Jr. and Gonzalez-Angulo AM. cMET and phospho-cMET protein levels in breast cancers and survival outcomes. Clin Cancer Res. 2012; 18(8):2269-2277.
15. Lengyel E, Prechtel D, Resau JH, Gauger K, Welk A, Lindemann K, Salanti G, Richter T, Knudsen B, Vande Woude GF and Harbeck N. C-Met overexpression in node-positive breast cancer identifies patients with poor clinical outcome independent of Her2/neu. Int J Cancer. 2005; 113(4):678-682.
16. Camp RL, Rimm EB and Rimm DL. Met expression is associated with poor outcome in patients with axillary lymph node negative breast carcinoma. Cancer. 1999; 86(11):2259-2265.
17. Tolgay Ocal I, Dolled-Filhart M, D'Aquila TG, Camp RL and Rimm DL. Tissue microarray-based studies of patients with lymph node negative breast carcinoma show that met expression is associated with worse outcome but is not correlated with epidermal growth factor family receptors. Cancer. 2003; 97(8):1841-1848.
18. Gentile A, Trusolino L and Comoglio PM. The Met tyrosine kinase receptor in development and cancer. Cancer Metastasis Rev. 2008; 27(1):85-94.
19. Trusolino L, Bertotti A and Comoglio PM. MET signalling: principles and functions in development, organ regeneration and cancer. Nat Rev Mol Cell Biol. 2010; 11(12):834-848.
20. Boccaccio C and Comoglio PM. Invasive growth: a MET-driven genetic programme for cancer and stem cells. Nat Rev Cancer. 2006; 6(8):637-645.
21. Polyak K and Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer. 2009; 9(4):265-273.
22. Birchmeier C, Birchmeier W, Gherardi E and Vande Woude GF. Met, metastasis, motility and more. Nat Rev Mol Cell Biol. 2003; 4(12):915-925.
23. Yap TA and de Bono JS. Targeting the HGF/c-Met axis: state of play. Mol Cancer Ther. 2010; 9(5):1077-1079.
24. Sierra JR and Tsao MS. c-MET as a potential therapeutic target and biomarker in cancer. Ther Adv Med Oncol. 2011; 3(1 Suppl):S21-35.
25. Gherardi E, Birchmeier W, Birchmeier C and Woude GV. Targeting MET in cancer: rationale and progress. Nat Rev Cancer. 2012; 12(2):89-103.
26. Scagliotti GV, Novello S and von Pawel J. The emerging role of MET/HGF inhibitors in oncology. Cancer Treat Rev. 2013.
27. Sequist LV, von Pawel J, Garmey EG, Akerley WL, Brugger W, Ferrari D, Chen Y, Costa DB, Gerber DE, Orlov S, Ramlau R, Arthur S, Gorbachevsky I, Schwartz B and Schiller JH. Randomized phase II study of erlotinib plus tivantinib versus erlotinib plus placebo in previously treated non-small-cell lung cancer. J Clin Oncol. 2011; 29(24):3307-3315.
28. Scagliotti GV, Novello S, Schiller JH, Hirsh V, Sequist LV, Soria JC, von Pawel J, Schwartz B, Von Roemeling R and Sandler AB. Rationale and design of MARQUEE: a phase III, randomized, double-blind study of tivantinib plus erlotinib versus placebo plus erlotinib in previously treated patients with locally advanced or metastatic, nonsquamous, non-small-cell lung cancer. Clin Lung Cancer. 2012; 13(5):391-395.
29. Goyal L, Muzumdar MD and Zhu AX. Targeting the HGF/c-MET Pathway in Hepatocellular Carcinoma. Clin Cancer Res. 2013; 19(9):2310-2318.
30. Santoro A, Rimassa L, Borbath I, Daniele B, Salvagni S, Van Laethem JL, Van Vlierberghe H, Trojan J, Kolligs FT, Weiss A, Miles S, Gasbarrini A, Lencioni M, Cicalese L, Sherman M, Gridelli C and et al. Tivantinib for second-line treatment of advanced hepatocellular carcinoma: a randomised, placebo-controlled phase 2 study. Lancet Oncol. 2013; 14(1):55-63.
31. Barclay AN and Van den Berg TK. The interaction between signal regulatory protein alpha (SIRPalpha) and CD47: structure, function, and therapeutic target. Annual review of immunology. 2014; 32:25-50.
32. Jaiswal S, Jamieson CH, Pang WW, Park CY, Chao MP, Majeti R, Traver D, van Rooijen N and Weissman IL. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell. 2009; 138(2):271-285.
33. Willingham SB, Volkmer JP, Gentles AJ, Sahoo D, Dalerba P, Mitra SS, Wang J, Contreras-Trujillo H, Martin R, Cohen JD, Lovelace P, Scheeren FA, Chao MP, Weiskopf K, Tang C, Volkmer AK and et al. The CD47-signal regulatory protein alpha (SIRPa) interaction is a therapeutic target for human solid tumors. Proc Natl Acad Sci U S A. 2012; 109(17):6662-6667.
34. Chan KS, Espinosa I, Chao M, Wong D, Ailles L, Diehn M, Gill H, Presti J Jr., Chang HY, van de Rijn M, Shortliffe L and Weissman IL. Identification, molecular characterization, clinical prognosis, and therapeutic targeting of human bladder tumor-initiating cells. Proc Natl Acad Sci U S A. 2009; 106(33):14016-14021.
35. Majeti R, Chao MP, Alizadeh AA, Pang WW, Jaiswal S, Gibbs KD Jr., van Rooijen N and Weissman IL. CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell. 2009; 138(2):286-299.
36. Jiang H, Fu R, Wang H, Li L, Liu H and Shao Z. CD47 is expressed abnormally on hematopoietic cells in myelodysplastic syndrome. Leuk Res. 2013.
37. Chao MP, Alizadeh AA, Tang C, Myklebust JH, Varghese B, Gill S, Jan M, Cha AC, Chan CK, Tan BT, Park CY, Zhao F, Kohrt HE, Malumbres R, Briones J, Gascoyne RD and et al. Anti-CD47 antibody synergizes with rituximab to promote phagocytosis and eradicate non-Hodgkin lymphoma. Cell. 2010; 142(5):699-713.
38. Chao MP, Alizadeh AA, Tang C, Jan M, Weissman-Tsukamoto R, Zhao F, Park CY, Weissman IL and Majeti R. Therapeutic antibody targeting of CD47 eliminates human acute lymphoblastic leukemia. Cancer Res. 2011; 71(4):1374-1384.
39. Chao MP, Weissman IL and Majeti R. The CD47-SIRPalpha pathway in cancer immune evasion and potential therapeutic implications. Curr Opin Immunol. 2012; 24(2):225-232.
40. Edris B, Weiskopf K, Volkmer AK, Volkmer JP, Willingham SB, Contreras-Trujillo H, Liu J, Majeti R, West RB, Fletcher JA, Beck AH, Weissman IL and van de Rijn M. Antibody therapy targeting the CD47 protein is effective in a model of aggressive metastatic leiomyosarcoma. Proc Natl Acad Sci U S A. 2012; 109(17):6656-6661.
41. Baccelli I, Schneeweiss A, Riethdorf S, Stenzinger A, Schillert A, Vogel V, Klein C, Saini M, Bauerle T, Wallwiener M, Holland-Letz T, Hofner T, Sprick M, Scharpff M, Marme F, Sinn HP and et al. Identification of a population of blood circulating tumor cells from breast cancer patients that initiates metastasis in a xenograft assay. Nat Biotechnol. 2013.
42. Weichert W, Roske A, Gekeler V, Beckers T, Ebert MP, Pross M, Dietel M, Denkert C and Rocken C. Association of patterns of class I histone deacetylase expression with patient prognosis in gastric cancer: a retrospective analysis. Lancet Oncol. 2008; 9(2):139-148.
43. Wallwiener M, Hartkopf AD, Baccelli I, Riethdorf S, Schott S, Pantel K, Marme F, Sohn C, Trumpp A, Rack B, Aktas B, Solomayer EF, Muller V, Janni W, Schneeweiss A and Fehm TN. The prognostic impact of circulating tumor cells in subtypes of metastatic breast cancer. Breast Cancer Res Treat. 2013; 137(2):503-510.
44. Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Matera J, Miller MC, Reuben JM, Doyle GV, Allard WJ, Terstappen LW and Hayes DF. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med. 2004; 351(8):781-791.
45. Bidard FC, Peeters DJ, Fehm T, Nole F, Gisbert-Criado R, Mavroudis D, Grisanti S, Generali D, Garcia-Saenz JA, Stebbing J, Caldas C, Gazzaniga P, Manso L, Zamarchi R, de Lascoiti AF, De Mattos-Arruda L and et al. Clinical validity of circulating tumour cells in patients with metastatic breast cancer: a pooled analysis of individual patient data. Lancet Oncol. 2014; 15(4):406-414.
46. Baccelli I and Trumpp A. The evolving concept of cancer and metastasis stem cells. Journal of Cell Biology. 2012; 198(3):281-293.
47. Kalluri R and Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest. 2009; 119(6): 1420-1428.
48. Thiery JP, Acloque H, Huang RY and Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009; 139(5):871-890.
49. Toi M, Taniguchi T, Ueno T, Asano M, Funata N, Sekiguchi K, Iwanari H and Tominaga T. Significance of circulating hepatocyte growth factor level as a prognostic indicator in primary breast cancer. Clin Cancer Res. 1998; 4(3):659-664.
50. Hodgkinson CL, Morrow CJ, Li Y, Metcalf RL, Rothwell DG, Trapani F, Polanski R, Burt DJ, Simpson KL, Morris K, Pepper SD, Nonaka D, Greystoke A, Kelly P, Bola B, Krebs MG and et al. Tumorigenicity and genetic profiling of circulating tumor cells in small-cell lung cancer. Nat Med. 2014; 20(8):897-903.
51. Oskarsson T, Batlle E and Massague J. Metastatic stem cells: sources, niches, and vital pathways. Cell Stem Cell. 2014; 14(3):306-321.
52. Previdi S, Abbadessa G, Dalo F, France DS and Broggini M. Breast cancer-derived bone metastasis can be effectively reduced through specific c-MET inhibitor tivantinib (ARQ 197) and shRNA c-MET knockdown. Mol Cancer Ther. 2012; 11(1):214-223.
53. Theocharides AP, Jin L, Cheng PY, Prasolava TK, Malko AV, Ho JM, Poeppl AG, van Rooijen N, Minden MD, Danska JS, Dick JE and Wang JC. Disruption of SIRPalpha signaling in macrophages eliminates human acute myeloid leukemia stem cells in xenografts. J Exp Med. 2012; 209(10):1883-1899.
54. Gardai SJ, McPhillips KA, Frasch SC, Janssen WJ, Starefeldt A, Murphy-Ullrich JE, Bratton DL, Oldenborg PA, Michalak M and Henson PM. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell. 2005; 123(2): 321-334.
55. Chao MP, Majeti R and Weissman IL. Programmed cell removal: a new obstacle in the road to developing cancer. Nat Rev Cancer. 2011; 12(1):58-67.
56. Chao MP, Jaiswal S, Weissman-Tsukamoto R, Alizadeh AA, Gentles AJ, Volkmer J, Weiskopf K, Willingham SB, Raveh T, Park CY, Majeti R and Weissman IL. Calreticulin is the dominant pro-phagocytic signal on multiple human cancers and is counterbalanced by CD47. Sci Transl Med. 2010; 2(63):63ra94.
57. Elston CW and Ellis IO. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology. 1991; 19(5):403-410.
58. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M and Clark GM. Reporting recommendations for tumor marker prognostic studies (REMARK). J Natl Cancer Inst. 2005; 97(16):1180-1184.