Activation of MAPK pathways due to DUSP4 loss promotes cancer stem cell-like phenotypes in basal-like breast cancer

Cancer Research

Volumn 73, Issue 20, 2013, Pages 6346-6358

  Balko, Justin M ^a   Schwarz, Luis J ^a,b   Bhola, Neil E ^a   Kurupi, Richard ^a   Owens, Phillip ^a   Miller, Todd W ^c   Gómez, Henry ^b   Cook, Rebecca S ^a   Arteaga, Carlos L ^a  

^a VANDERBILT INGRAM CANCER CENTER   (United States)

^b INSTITUTO NACIONAL DE ENFERMEDADES NEOPLÁSICAS   (Peru)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD24 ANTIGEN; DUAL SPECIFICITY PHOSPHATASE 4; HERMES ANTIGEN; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; PHOSPHATASE; PROTEIN C FOS; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR ETS 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL LIKE BREAST CANCER; BREAST CARCINOGENESIS; CANCER STEM CELL; CD24 GENE; CD44 GENE; CONTROLLED STUDY; COPY NUMBER VARIATION; DNA METHYLATION; DOWN REGULATION; DUSP4 GENE; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE DELETION; GENE EXPRESSION REGULATION; GENE LOCUS; GENE LOSS; HUMAN; HUMAN CELL; IL 6 GENE; IL 8 GENE; IMMEDIATE EARLY GENE; LOSS OF FUNCTION MUTATION; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; BREAST NEOPLASMS; CELL CULTURE TECHNIQUES; DUAL-SPECIFICITY PHOSPHATASES; FEMALE; HETEROGRAFTS; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, NUDE; MITOGEN-ACTIVATED PROTEIN KINASE PHOSPHATASES; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASTIC STEM CELLS; PHENOTYPE; TRANSFECTION;

EID: 84886046699     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-1385     Document Type: Article

References (50)

1. Perou CM, Sorlie T, Eisen M.B., van de Rijn M, Jeffrey SS, Rees CA, et al. Molecular portraits of human breast tumours. Nature 2000; 406: 747-52.
2. Blick T, Hugo H, Widodo E., Waltham M, Pinto C, Mani S.A., et al Epithelial mesenchymal transition traits in human breast cancer cell lines parallel the CD44(hi/)CD24 (lo/-) stem cell phenotype in human breast cancer. J Mammary Gland Biol Neoplasia 2010; 15:235-52.
3. Mirzoeva OK, Das D, Heiser L.M., Bhattacharya S., Siwak D, Gendelman R, et al Basalsub type and MAPK/ERKkinase(MEK)-phosphoinositide 3-kinase feedback signaling determine susceptibility of breast cancer cells to MEK inhibition. Cancer Res 2009; 69:565-72.
4. Neve RM, Chin K, Fridlyand J., Yeh J, Baehner FL, Fevr T, et al A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006; 10:515-27.
5. Prat A, Parker JS, Karginova O, Fan C., Livasy C, Herschkowitz JI, et al Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 2010; 12:R68.
6. Herschkowitz JI, Simin K, Weigman V.J., 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.
7. Creighton CJ, Li X, Landis M., Dixon JM, Neumeister VM, Sjolund A, et al Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci U S A 2009; 106:13820-5.
8. Morel AP, Lievre M, Thomas C., Hinkal G, Ansieau S, Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS ONE 2008; 3:e2888.
9. Mani SA, Guo W, Liao M.J., Eaton EN, Ayyanan A, Zhou AY, et al The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133:704-15.
10. Asiedu MK, Ingle JN, Behrens M.D., Radisky DC, Knutson KL TGFbeta/ TNF(alpha)-mediated epithelial-mesenchymal transition generates breast cancer stem cells with a claudin-low phenotype. Cancer Res 2011; 71:4707-19.
11. Liu M, Casimiro MC, Wang C, Shirley L.A., Jiao X., Katiyar S, et al p21CIP1 attenuates Ras- and c-Myc-dependent breast tumor epithelial mesenchymal transition and cancer stem cell-like gene expression in vivo. Proc Natl Acad Sci U S A 2009; 106: 19035-9.
12. Morel AP, Hinkal GW, Thomas C, Fauvet F., Courtois-Cox S, Wierinckx A, et al EMT inducers catalyze malignant transformation of mammary epithelial cells and drive tumorigenesis towards claudin-low tumors in transgenic mice. PLoS Genet 2012; 8:e1002723.
13. Sanchez-Munoz A., Gallego E, de Luque V, Perez-Rivas LG, Vicioso L., Ribelles N, et al Lack of evidence for KRAS oncogenic mutations in triple-negative breast cancer. BMC Cancer 2010; 10:136.
14. Comprehensive molecular portraits of human breast tumours. Nature 2012; 490:61-70.
15. Jeffrey KL, Camps M, Rommel C., Mackay CR Targeting dual-specificity phosphatases: manipulating MAP kinase signalling and immune responses. Nat Rev Drug Discov 2007; 6:391-403.
16. Balko JM, Cook RS, Vaught D.B., Kuba MG, Miller TW, Bhola NE, et al Profiling of residual breast cancers after neoadjuvant chemotherapy identifies DUSP4 deficiency as a mechanism of drug resistance. Nat Med 2012; 18:1052-9.
17. Lehmann BD, Bauer JA, Chen X, Sanders M.E., Chakravarthy AB, Shyr Y, et al Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 2011; 121:2750-67.
18. Balko JM, Jones BR, Coakley V.L., Black EP MEK and EGFR inhibition demonstrate synergistic activity in EGFR-dependent NSCLC. Cancer Biol Ther 2009; 8:522-30.
19. Hollenhorst PC, Shah AA, Hopkins C, Graves BJ Genome-wide analyses reveal properties of redundant and specific promoter occupancy within the ETS gene family. Genes Dev 2007; 21:1882-94.
20. Marinescu VD, Kohane IS, Riva A. The MAPPER database: a multigenome catalog of putative transcription factor binding sites. Nucleic Acids Res 2005; 33:D91-7.
21. Meerbrey KL, Hu G, Kessler J.D., Roarty K., Li MZ, Fang JE, et al The pINDUCER lentiviral toolkit for inducible RNA interference in vitro and in vivo. Proc Natl Acad Sci U S A 2011; 108:3665-70.
22. Armes JE, Hammet F, de Silva M, Ciciulla J, Ramus S.J., Soo WK, et al Candidate tumor-suppressor genes on chromosome arm 8p in earlyonset and high-grade breast cancers. Oncogene 2004; 23:5697-702.
23. Venter DJ, Ramus SJ, Hammet F.M., de Silva M, Hutchins AM, Petrovic V, et al Complex CGHalterations on chromosomearm8p at candidate tumor suppressor gene loci in breast cancer cell lines. Cancer Genet Cytogenet 2005; 160:134-40.
24. Anbazhagan R, Fujii H, Gabrielson E. Allelic loss of chromosomal arm 8p in breast cancer progression. Am J Pathol 1998; 152:815-9.
25. Pratilas CA, Taylor BS, Ye Q, Viale A., Sander C, Solit DB, et al (V600E) BRAF is associated with disabled feedback inhibition of RAF-MEK signaling and elevated transcriptional output of the pathway. Proc Natl Acad Sci U S A 2009; 106:4519-24.
26. Camps M, Nichols A, Arkinstall S. Dual specificity phosphatases: a gene family for control of MAP kinase function. FASEB J 2000; 14:6-16.
27. Gaedcke J, Grade M, Jung K., Camps J, Jo P, Emons G., et al Mutated KRAS results in overexpression of DUSP4, a MAP-kinase phosphatase, and SMYD3, a histone methyltransferase, in rectal carcinomas. Genes Chromosomes Cancer 2010; 49:1024-34.
28. Charafe-Jauffret E., Ginestier C, Iovino F., Wicinski J, Cervera N, Finetti P., et al Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 2009; 69:1302-13.
29. Ginestier C, Liu S, Diebel M.E., Korkaya H., Luo M, Brown M, et al CXCR1 blockade selectively targets human breast cancer stem cells in vitro and in xenografts. J Clin Invest 2010; 120:485-97.
30. Kim MY, Oskarsson T, Acharyya S., Nguyen DX, Zhang XH, Norton L, et al Tumor self-seeding by circulating cancer cells. Cell 2009; 139: 1315-26.
31. Sansone P, Storci G, Tavolari S., Guarnieri T, Giovannini C, Taffurelli M., et al IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J Clin Invest 2007; 117:3988-4002.
32. Smeal T, Binetruy B, Mercola D.A., Birrer M., Karin M. Oncogenic and transcriptional cooperation with Ha-Ras requires phosphorylation of cJun on serines 63 and 73. Nature 1991; 354:494-6.
33. Binetruy B, Smeal T, Karin M. Ha-Ras augments c-Jun activity and stimulates phosphorylation of its activation domain. Nature 1991; 351: 122-7.
34. Hibi M, Lin A, Smeal T., Minden A, Karin M. Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev 1993; 7:2135-48.
35. Brachmann SM, Hofmann I, Schnell C., Fritsch C, Wee S, Lane H., et al Specific apoptosis induction by the dual PI3K/mTor inhibitor NVPBEZ235 in HER2 amplified and PIK3CA mutant breast cancer cells. Proc Natl Acad Sci U S A 2009; 106:22299-304.
36. Cerami E, Gao J, Dogrusoz U., Gross BE, Sumer SO, Aksoy BA, et al The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2012; 2: 401-4.
37. Oh YT, Yue P, Zhou W., Balko JM, Black EP, Owonikoko TK, et al Oncogenic Ras and B-Raf proteins positively regulate death receptor 5 expression through co-activation of ERK and JNK signaling. J Biol Chem 2012; 287:257-67.
38. Spangler B, Kappelmann M, Schittek B., Meierjohann S, Vardimon L, Bosserhoff A.K., et al ETS-1/RhoC signaling regulates the transcription factor c-Jun in melanoma. Int J Cancer 2012; 130:2801-11.
39. Gupta PB, Onder TT, Jiang G, Tao K., Kuperwasser C, Weinberg RA, et al Identification of selective inhibitors of cancer stem cells by highthroughput screening. Cell 2009; 138:645-59.
40. Gupta PB, Fillmore CM, Jiang G, Shapira S.D., Tao K., Kuperwasser C, et al Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 2011; 146:633-44.
41. Elenbaas B, Spirio L, Koerner F., Fleming MD, Zimonjic DB, Donaher JL, et al Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev 2001; 15: 50-65.
42. Dontu G, Abdallah WM, Foley J.M., Jackson KW, Clarke MF, Kawamura MJ, et al In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003; 17:1253-70.
43. Al-Hajj M., Wicha MS, Benito-Hernandez A, Morrison S.J., Clarke MF Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003; 100:3983-8.
44. Ponti D, Costa A, Zaffaroni N., Pratesi G, Petrangolini G, Coradini D., et al Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 2005; 65: 5506-11.
45. Charafe-Jauffret E., Ginestier C, Iovino F., Tarpin C, Diebel M, Esterni B., et al Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer. Clin Cancer Res 2010; 16:45-55.
46. Huang EH, Hynes MJ, Zhang T, Ginestier C., Dontu G, Appelman H, et al Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 2009; 69:3382-9.
47. Hwang-Verslues W.W., Kuo WH, Chang P.H., Pan CC, Wang HH, Tsai ST, et al Multiple lineages of human breast cancer stem/progenitor cells identified by profiling with stem cell markers. PLoS ONE 2009; 4:e8377.
48. Hennessy BT, Gonzalez-Angulo AM, Stemke-Hale K, Gilcrease M.Z., 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.
49. Barretina J, Caponigro G, Stransky N., Venkatesan K, Margolin AA, Kim S, et al The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 2012; 483:603-7.
50. Parker JS, Mullins M, Cheang M.C., Leung S., Voduc D, Vickery T, et al Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 2009; 27:1160-7.