Receptor tyrosine kinase signaling favors a protumorigenic state in breast cancer cells by inhibiting the adaptive immune response

Cancer Research

Volumn 70, Issue 20, 2010, Pages 7776-7787

  Ursini Siegel, Josie ^a,h   Cory, Sean ^a,c   Zuo, Dongmei ^a   Hardy, William R ^d   Rexhepaj, Elton ^e   Lam, Sonya ^a   Schade, Babette ^a   Jirstrom, Karin ^f   Bjur, Eva ^b   Piccirillo, Ciriaco A ^b   DeNardo, David ^g   Coussens, Lisa M ^g   Brennan, Donal J ^e   Gallagher, William M ^e   Park, Morag ^a   Pawson, Tony ^d   Hallett, Michael ^a,c   Muller, William J ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d MOUNT SINAI HOSPITAL   (Canada)

^e UNIVERSITY COLLEGE DUBLIN   (Ireland)

^f Malmö University Hospital   (Sweden)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; PROTEIN; PROTEIN SHCA; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER SURVIVAL; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; FEMALE; HUMORAL IMMUNITY; IMMUNE DEFICIENCY; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; SIGNAL TRANSDUCTION; TUMOR IMMUNITY;

ANIMALS; BREAST NEOPLASMS; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; HUMANS; IMMUNOSUPPRESSION; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, TRANSGENIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PARITY; PREGNANCY; PROPORTIONAL HAZARDS MODELS; RECEPTOR PROTEIN-TYROSINE KINASES; RNA, NEOPLASM; SHC SIGNALING ADAPTOR PROTEINS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TREATMENT OUTCOME;

EID: 78049271279     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-2229     Document Type: Article

References (41)

1. Ursini-Siegel J, Muller WJ. The ShcA adaptor protein is a critical regulator of breast cancer progression. Cell Cycle 2008;7:1936-43.
2. Davol PA, Bagdasaryan R, Elfenbein GJ, Maizel AL, Frackelton AR, Jr. Shc proteins are strong, independent prognostic markers for both node-negative and node-positive primary breast cancer. Cancer Res 2003;63:6772-83.
3. Dankort D, Maslikowski B, Warner N, et al. Grb2 and Shc adapter proteins play distinct roles in Neu (ErbB-2)-induced mammary tumor-igenesis: implications for human breast cancer. Mol Cell Biol 2001;21:1540-51. (Pubitemid 32156374)
4. Ursini-Siegel J, Hardy WR, Zuo D, et al. ShcA signalling is essential for tumour progression in mouse models of human breast cancer. EMBO J 2008;27:910-20. (Pubitemid 351417168)
5. Webster MA, Hutchinson JN, Rauh MJ, et al. Requirement for both Shc and phosphatidylinositol 3′ kinase signaling pathways in polyomavirus middle T-mediated mammary tumorigenesis. Mol Cell Biol 1998;18:2344-59.
6. Hardy WR, Li L, Wang Z, et al. Combinatorial ShcA docking interactions support diversity in tissue morphogenesis. Science 2007;317:251-6. (Pubitemid 47076202)
7. Saucier C, Khoury H, Lai KM, et al. The Shc adaptor protein is critical for VEGF induction by Met/HGF and ErbB2 receptors and for early onset of tumor angiogenesis. Proc Natl Acad Sci U S A 2004;101:2345-50. (Pubitemid 38269314)
8. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol 1992;12:954-61.
9. White DE, Kurpios NA, Zuo D, et al. Targeted disruption of β1-integrin in a transgenic mouse model of human breast cancer reveals an essential role in mammary tumor induction. Cancer Cell 2004;6:159-70. (Pubitemid 39485688)
10. Schade B, Lam SH, Cernea D, et al. Distinct ErbB-2 coupled signaling pathways promote mammary tumors with unique pathologic and transcriptional profiles. Cancer Res 2007;67:7579-88. (Pubitemid 47281349)
11. Gentleman RC, Carey VJ, Bates DM, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004;5:R80.
12. Parker JS, Mullins M, Cheang MC, et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 2009;27:1160-7.
13. Polyak K. Pregnancy and breast cancer: the other side of the coin. Cancer Cell 2006;9:151-3. (Pubitemid 43357941)
14. Jones N, Hardy WR, Friese MB, et al. Analysis of a Shc family adaptor protein, ShcD/Shc4, that associates with muscle-specific kinase. Mol Cell Biol 2007;27:4759-73. (Pubitemid 47016129)
15. O'Bryan JP, Songyang Z, Cantley L, Der CJ, Pawson T. A mammalian adaptor protein with conserved Src homology 2 and phosphotyrosine-binding domains is related to Shc and is specifically expressed in the brain. Proc Natl Acad Sci U S A 1996;93:2729-34. (Pubitemid 26114317)
16. Vandercappellen J, Van Damme J, Struyf S. The role of CXC chemokines and their receptors in cancer. Cancer Lett 2008;267:226-44.
17. Watts TH, DeBenedette MA. T cell co-stimulatory molecules other than CD28. Curr Opin Immunol 1999;11:286-93.
18. Waldmann TA. The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat Rev Immunol 2006;6:595-601. (Pubitemid 44134092)
19. Zhu J, Paul WE. CD4 T cells: fates, functions, and faults. Blood 2008;112:1557-69.
20. Johansson M, Denardo DG, Coussens LM. Polarized immune responses differentially regulate cancer development. Immunol Rev 2008;222:145-54. (Pubitemid 351430362)
21. Glimcher LH, Murphy KM. Lineage commitment in the immune system: the T helper lymphocyte grows up. Genes Dev 2000;14:1693-711.
22. DeNardo DG, Coussens LM. Inflammation and breast cancer. Balancing immune response: crosstalk between adaptive and innate immune cells during breast cancer progression. Breast Cancer Res 2007;9:212-21.
23. Lin EY, Jones JG, Li P, et al. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am J Pathol 2003;163:2113-26. (Pubitemid 37310040)
24. Boersma BJ, Reimers M, Yi M, et al. A stromal gene signature associated with inflammatory breast cancer. Int J Cancer 2008;122:1324-32. (Pubitemid 351287233)
25. Finak G, Bertos N, Pepin F, et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat Med 2008;14:518-27.
26. Walser TC, Ma X, Kundu N, Dorsey R, Goloubeva O, Fulton AM. Immune-mediated modulation of breast cancer growth and metastasis by the chemokine Mig (CXCL9) in a murine model. J Immunother 2007;30:490-8. (Pubitemid 46988082)
27. DeNardo DG, Barreto JB, Andreu P, et al. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 2009;16:91-102.
28. Martin ML, Wall EM, Sandwith E, et al. Density of tumour stroma is correlated to outcome after adoptive transfer of CD4(+) and CD8 (+) T cells in a murine mammary carcinoma model. Breast Cancer Res Treat 2010;121:753-63.
29. Trimboli AJ, Cantemir-Stone CZ, Li F, et al. Pten in stromal fibroblasts suppresses mammary epithelial tumours. Nature 2009;461:1084-91.
30. Peng SL, Szabo SJ, Glimcher LH. T-bet regulates IgG class switching and pathogenic autoantibody production. Proc Natl Acad Sci U S A 2002;99:5545-50.
31. Cheang MC, Voduc D, Bajdik C, et al. Basal-like breast cancer defined by five biomarkers has superior prognostic value than triple-negative phenotype. Clin Cancer Res 2008;14:1368-76. (Pubitemid 351413917)
32. Graveel CR, DeGroot JD, Su Y, et al. Met induces diverse mammary carcinomas in mice and is associated with human basal breast cancer. Proc Natl Acad Sci U S A 2009;106:12909-14.
33. Nalwoga H, Arnes JB, Wabinga H, Akslen LA. Expression of EGFR and c-kit is associated with the basal-like phenotype in breast carcinomas of African women. APMIS 2008;116:515-25.
34. Ponzo MG, Lesurf R, Petkiewicz S, et al. Met induces mammary tumors with diverse histologies and is associated with poor outcome and human basal breast cancer. Proc Natl Acad Sci U S A 2009;106:12903-8.
35. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987;235:177-82.
36. Wiseman SM, Makretsov N, Nielsen TO, et al. Coexpression of the type 1 growth factor receptor family members HER-1, HER-2, and HER-3 has a synergistic negative prognostic effect on breast carcinoma survival. Cancer 2005;103:1770-7.
37. Batzer AG, Blaikie P, Nelson K, Schlessinger J, Margolis B. The phosphotyrosine interaction domain of Shc binds an LXNPXY motif on the epidermal growth factor receptor. Mol Cell Biol 1995;15:4403-9.
38. Dankort DL, Wang Z, Blackmore V, Moran MF, Muller WJ. Distinct tyrosine autophosphorylation sites negatively and positively modulate neu-mediated transformation. Mol Cell Biol 1997;17:5410-25. (Pubitemid 27357639)
39. Lennartsson J, Blume-Jensen P, Hermanson M, Ponten E, Carlberg M, Ronnstrand L. Phosphorylation of Shc by Src family kinases is necessary for stem cell factor receptor/c-kit mediated activation of the Ras/MAP kinase pathway and c-fos induction. Oncogene 1999;18:5546-53. (Pubitemid 29481501)
40. Schaeper U, Gehring NH, Fuchs KP, Sachs M, Kempkes B, Birchmeier W. Coupling of Gab1 to c-Met, Grb2, and Shp2 mediates biological responses. J Cell Biol 2000;149:1419-32. (Pubitemid 30437616)
41. Vijapurkar U, Cheng K, Koland JG. Mutation of a Shc binding site tyrosine residue in ErbB3/HER3 blocks heregulin-dependent activation of mitogen-activated protein kinase. J Biol Chem 1998;273:20996-1002. (Pubitemid 28385383)