Ras signaling is a key determinant for metastatic dissemination and poor survival of luminal breast cancer patients

Cancer Research

Volumn 75, Issue 22, 2015, Pages 4960-4972

  Wright, Katherine L ^a,b   Adams, Jessica R ^a,b   Liu, Jeff C ^c   Loch, Amanda J ^a   Wong, Ruth G ^a   Jo, Christine E B ^a   Beck, Lauren A ^a   Santhanam, Divya R ^a   Weiss, Laura ^a   Mei, Xue ^a   Lane, Timothy F ^d   Koralov, Sergei B ^e   Done, Susan J ^f   Woodgett, James R ^g   Zacksenhaus, Eldad ^c   Hu, Pingzhao ^h   Egan, Sean E ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^f PRINCESS MARGARET HOSPITAL   (Canada)

^g MOUNT SINAI HOSPITAL   (Canada)

^h UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR; K RAS PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; STAT3 PROTEIN; RAS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST ADENOCARCINOMA; BREAST CANCER; BREAST METASTASIS; CANCER MORTALITY; CANCER PATIENT; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER SURVIVAL; CONTROLLED STUDY; EPIDERMAL GROWTH FACTOR RECEPTOR 2 POSITIVE BREAST CANCER; ESTROGEN RECEPTOR POSITIVE BREAST CANCER; FEMALE; GENETIC ASSOCIATION; HUMAN; LUMINAL A BREAST CANCER; LUMINAL B BREAST CANCER; MAJOR CLINICAL STUDY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; ONCOGENE; ONCOGENE K RAS; OVERALL SURVIVAL; PI3K GENE; PI3KCA GENE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STAT3 GENE; ANIMAL; BREAST TUMOR; DISEASE FREE SURVIVAL; DNA MICROARRAY; IMMUNOHISTOCHEMISTRY; KAPLAN MEIER METHOD; METABOLISM; MORTALITY; PATHOLOGY; PHYSIOLOGY; TUMOR INVASION; TUMOR RECURRENCE;

ANIMALS; BREAST NEOPLASMS; DISEASE-FREE SURVIVAL; FEMALE; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; MICE; NEOPLASM INVASIVENESS; NEOPLASM RECURRENCE, LOCAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RAS PROTEINS; SIGNAL TRANSDUCTION;

EID: 84955267683     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-2992     Document Type: Article

References (63)

1. Wallace MD, Pfefferle AD, Shen L, McNairn AJ, Cerami EG, Fallon BL, et al. Comparative oncogenomics implicates the neurofibromin 1 gene (NF1) as a breast cancer driver. Genetics 2012;192:385-96.
2. McLaughlin SK, Olsen SN, Dake B, De Raedt T, Lim E, Bronson RT, et al. The RasGAP gene, RASAL2, is a tumor and metastasis suppressor. Cancer Cell 2013;24:365-78.
3. Egan SE, McClarty GA, Jarolim L, Wright JA, Spiro I, Hager G, et al. Expression of H-ras correlates with metastatic potential: evidence for direct regulation of the metastatic phenotype in 10T1/2 and NIH 3T3 cells. Mol Cell Biol 1987;7:830-37.
4. Sinn E, Muller W, Pattengale P, Tepler I, Wallace R, Leder P. Coexpression of MMTV/v-Ha-ras and MMTV/c-myc genes in transgenic mice: synergistic action of oncogenes in vivo. Cell 1987;49: 465-75.
5. Swarbrick A, Roy E, Allen T, Bishop JM. Id1 cooperates with oncogenic Ras to induce metastatic mammary carcinoma by subversion of the cellular senescence response. Proc Natl Acad Sci U S A 2008;105:5402-7.
6. McCaffrey LM, Montalbano J, Mihai C, Macara IG. Loss of the Par3 polarity protein promotes breast tumorigenesis and metastasis. Cancer Cell 2012; 22:601-14.
7. Sorlie T, Tibshirani R, Parker J, Hastie T, Marron JS, Nobel A, et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci U S A 2003;100:8418-23.
8. Hennessy BT, Gonzalez-Angulo AM, Stemke-Hale K, Gilcrease MZ, Krishnamurthy S, Lee JS, et al. Characterization of a naturally occurring breast cancer subset enriched in epithelial-to-mesenchymal transition and stem cell characteristics. Cancer Res 2009;69:4116-24.
9. Dawson SJ, Rueda OM, Aparicio S, Caldas C. A new genome-driven integrated classification of breast cancer and its implications. EMBOJ 2013; 32:617-28.
10. Santagata S, Thakkar A, Ergonul A, Wang B, Woo T, Hu R, et al. Taxonomyof breast cancer based on normal cell phenotype predicts outcome. J Clin Invest 2014;124:859-70.
11. Lee U, Frankenberger C, Yun J, Bevilacqua E, Caldas C, Chin SF, et al. A prognostic gene signature for metastasis-free survival of triple negative breast cancer patients. PLoS ONE 2013;8:e82125.
12. Adams JR, Schachter NF, Liu JC, Zacksenhaus E, Egan SE. Elevated PI3K signaling drives multiple breast cancer subtypes. Oncotarget 2011;2: 435-47.
13. Adams JR, Xu K, Liu JC, Agamez NM, Loch AJ, Wong RG, et al. Cooperation between Pik3ca and p53 Mutations in Mouse Mammary Tumor Formation. Cancer Res 2011;71:2706-17.
14. Meyer DS, Brinkhaus H, Muller U, Muller M, Cardiff RD, Bentires-Alj M. Luminal expression of PIK3CA mutant H1047R in the mammary gland induces heterogeneous tumors. Cancer Res 2011;71:4344-51.
15. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirusmiddle T oncogene: a transgenic mousemodel for metastatic disease. Mol Cell Biol 1992;12:954-61.
16. Guy CT, Webster MA, Schaller M, Parsons TJ, Cardiff RD, Muller WJ. Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc Natl Acad Sci USA 1992; 89:10578-82.
17. Rosner A, Miyoshi K, Landesman-Bollag E, Xu X, Seldin DC, Moser AR, et al. Pathway pathology: histological differences between ErbB/Ras and Wnt pathway transgenic mammary tumors. Am J Pathol 2002;161:1087-97.
18. Ranger JJ, Levy DE, Shahalizadeh S, Hallett M, Muller WJ. Identification of a Stat3-dependent transcription regulatory network involved in metastatic progression. Cancer Res 2009;69:6823-30.
19. Barbieri I, Pensa S, Pannellini T, Quaglino E, Maritano D, Demaria M, et al. Constitutively active Stat3 enhances neu-mediated migration and metastasis in mammary tumors via upregulation of Cten. Cancer Res 2010;70:2558-67.
20. Barbieri I, Quaglino E, Maritano D, Pannellini T, Riera L, Cavallo F, et al. Stat3 is required for anchorage-independent growth and metastasis but not for mammary tumor development downstream of the ErbB-2 oncogene. Mol Carcinog 2010;49:114-20.
21. Schade B, Rao T, Dourdin N, Lesurf R, Hallett M, Cardiff RD, et al. PTEN deficiency in a luminal ErbB-2 mouse model results in dramatic acceleration of mammary tumorigenesis and metastasis. J Biol Chem 2009;284: 19018-26.
22. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 1999;21:70-1.
23. Jackson EL, Willis N, Mercer K, Bronson RT, Crowley D, Montoya R, et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev 2001;15:3243-8.
24. Herschkowitz JI, Simin K, Weigman VJ, Mikaelian I, Usary J, Hu Z, et al. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol 2007;8:R76.
25. Gentleman R, Ihaka R 1997 The R Statistical Package. .
26. Harrington DP, Fleming TR. A class of rank test procedures for censored survival data. Biometrika 1982;69:553-66.
27. Xu K, Usary J, Kousis PC, Prat A, Wang DY, Adams JR, et al. Lunatic fringe deficiency cooperates with the Met/Caveolin gene amplicon to induce basal-like breast cancer. Cancer Cell 2012;21:626-41.
28. Gatza ML, Lucas JE, Barry WT, Kim JW, Wang Q, Crawford MD, et al. A pathway-based classification of human breast cancer. Proc Natl Acad Sci U S A 2010;107:6994-9.
29. Therneau TM, Grambsch PM. Modeling survival data: extending the Cox model. New York, NY: Springer; 2000. xiii, p. 350.
30. Hart JR, Liao L, Yates JR III, Vogt PK. Essential role of Stat3 in PI3K-induced oncogenic transformation. Proc Natl Acad Sci U S A 2011;108:13247-52.
31. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, Albanese C, et al. Stat3 as an oncogene. Cell 1999;98:295-303.
32. Koskela HL, Eldfors S, Ellonen P, van Adrichem AJ, Kuusanmaki H, Andersson EI, et al. Somatic STAT3 mutations in large granular lymphocytic leukemia. N Engl J Med 2012;366:1905-13.
33. Levine RL, Pardanani A, Tefferi A, Gilliland DG. Role of JAK2 in the pathogenesis and therapy of myeloproliferative disorders. Nat Rev Cancer 2007;7:673-83.
34. Berishaj M, Gao SP, Ahmed S, Leslie K, Al-Ahmadie H, Gerald WL, et al. Stat3 is tyrosine-phosphorylated through the interleukin-6/glycoprotein 130/Janus kinase pathway in breast cancer. Breast Cancer Res 2007;9:R32.
35. Casola S, Cattoretti G, Uyttersprot N, Koralov SB, Seagal J, Hao Z, et al. Tracking germinal center B cells expressing germ-line immunoglobulin gamma1 transcripts by conditional gene targeting. Proc Natl Acad SciUS A 2006;103:7396-401.
36. Mesaros A, Koralov SB, Rother E, Wunderlich FT, Ernst MB, Barsh GS, et al. Activation of Stat3 signaling in AgRP neurons promotes locomotor activity. Cell Metab 2008;7:236-48.
37. Leslie K, Gao SP, Berishaj M, Podsypanina K, Ho H, Ivashkiv L, et al. Differential interleukin-6/Stat3 signaling as a function of cellular context mediates Ras-induced transformation. Breast Cancer Res 2010;12:R80.
38. Pfefferle AD, Herschkowitz JI, Usary J, Harrell JC, Spike BT, Adams JR, et al. Transcriptomic classification of genetically engineered mouse models of breast cancer identifies human subtype counterparts. Genome Biol 2013; 14:R125.
39. McGlynn LM, Kirkegaard T, Edwards J, Tovey S, Cameron D, Twelves C, et al. Ras/Raf-1/MAPK pathway mediates response to tamoxifen but not chemotherapy in breast cancer patients. Clin Cancer Res 2009;15: 1487-95.
40. Wagenblast E, Soto M, Gutierrez-Angel S, Hartl CA, Gable AL, Maceli AR, et al. A model of breast cancer heterogeneity reveals vascular mimicry as a driver of metastasis. Nature 2015;520:358-62.
41. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell 2010;141:39-51.
42. Joyce JA, Pollard JW. Microenvironmental regulation ofmetastasis. Nat Rev Cancer 2009;9:239-52.
43. Tam WL, Weinberg RA. The epigenetics of epithelial-mesenchymal plasticity in cancer. Nat Med 2013;19:1438-49.
44. Klein CA. Selection and adaptation during metastatic cancer progression. Nature 2013;501:365-72.
45. Giancotti FG. Mechanisms governing metastatic dormancy and reactivation. Cell 2013;155:750-64.
46. Wan L, Pantel K, Kang Y. Tumor metastasis: moving new biological insights into the clinic. Nat Med 2013;19:1450-64.
47. Fidler IJ, Poste G. The "seed and soil" hypothesis revisited. Lancet Oncol 2008;9:808.
48. Erez N. Cancer: Angiogenic awakening. Nature 2013;500:37-8.
49. Ghajar CM, Peinado H, Mori H, Matei IR, Evason KJ, Brazier H, et al. The perivascular niche regulates breast tumour dormancy. Nat Cell Biol 2013; 15:807-17.
50. Pylayeva-Gupta Y, Grabocka E, Bar-Sagi D. RAS oncogenes: weaving a tumorigenic web. Nat Rev Cancer 2011;11:761-74.
51. Smakman N, Borel Rinkes IH, Voest EE, Kranenburg O. Control of colorectal metastasis formation by K-Ras. Biochimica et biophysica acta 2005;1756:103-14.
52. Campbell PM, Der CJ. Oncogenic Ras and its role in tumor cell invasion and metastasis. Semin Cancer Biol 2004;14:105-14.
53. Bos PD, Nguyen DX, Massague J. Modeling metastasis in the mouse. Curr Opin Pharmacol 2010;10:571-7.
54. Nguyen DX, Massague J. Genetic determinants of cancer metastasis. Nat Rev Genet 2007;8:341-52.
55. Nguyen DX, Bos PD, Massague J. Metastasis: from dissemination to organspecific colonization. Nat Rev Cancer 2009;9:274-84.
56. Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C, et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 2003;3:537-49.
57. Zhang XH, Wang Q, Gerald W, Hudis CA, Norton L, Smid M, et al. Latent bone metastasis in breast cancer tied to Src-dependent survival signals. Cancer Cell 2009;16:67-78.
58. Guise TA. Breast cancer bone metastases: it's all about the neighborhood. Cell 2013;154:957-9.
59. Kozma SC, Bogaard ME, Buser K, Saurer SM, Bos JL, Groner B, et al. The human c-Kirsten ras gene is activated by a novel mutation in codon 13 in the breast carcinoma cell line MDA-MB231. Nucleic Acids Res 1987;15: 5963-71.
60. Sun T, Aceto N, Meerbrey KL, Kessler JD, Zhou C, Migliaccio I, et al. Activation of Multiple Proto-oncogenic Tyrosine Kinases in Breast Cancer via Loss of the PTPN12 Phosphatase. Cell 2011;144: 703-18.
61. Bild AH, Parker JS, Gustafson AM, Acharya CR, Hoadley KA, Anders C, et al. An integration of complementary strategies for gene-expression analysis to reveal novel therapeutic opportunities for breast cancer. Breast Cancer Res 2009;11:R55.
62. Kasid A, Lippman ME, Papageorge AG, Lowy DR, Gelmann EP. Transfection of v-rasH DNA into MCF-7 human breast cancer cells bypasses dependence on estrogen for tumorigenicity. Science 1985;228:725-8.
63. Kasid A, Knabbe C, Lippman ME. Effect of v-rasH oncogene transfection on estrogen-independent tumorigenicity of estrogen-dependent human breast cancer cells. Cancer Res 1987;47:5733-8.