IMP3 promotes stem-like properties in triple-negative breast cancer by regulating SLUG

Oncogene

Volumn 35, Issue 9, 2016, Pages 1111-1121

  Samanta, S ^a   Sun, H ^a   Goel, H L ^a   Pursell, B ^a   Chang, C ^a   Khan, A ^a   Greiner, D L ^a   Cao, S ^b   Lim, E ^b   Shultz, L D ^c   Mercurio, A M ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c JACKSON LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN LIKE GROWTH FACTOR 2 MICRORNA BINDING PROTEIN 3; ONCOFETAL ANTIGEN; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; IMP3 PROTEIN, HUMAN; MESSENGER RNA; RNA BINDING PROTEIN; SNAIL FAMILY TRANSCRIPTION FACTORS; SOX2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX; TUMOR MARKER;

5' UNTRANSLATED REGION; ARTICLE; CANCER CELL; CANCER PATIENT; CANCER PROGNOSIS; CANCER STEM CELL; CELL DIFFERENTIATION; COMPARATIVE STUDY; DISEASE ASSOCIATION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; OUTCOME ASSESSMENT; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; TRIPLE NEGATIVE BREAST CANCER; TUMOR XENOGRAFT; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; PATHOLOGY; PROGNOSIS;

BIOMARKERS, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASTIC STEM CELLS; PROGNOSIS; RNA, MESSENGER; RNA-BINDING PROTEINS; SOXB1 TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84959542726     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.164     Document Type: Article

References (50)

1. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100: 3983-3988.
2. Visvader JE, Lindeman GJ. Cancer stem cells: current status and evolving complexities. Cell Stem Cell 2012; 10: 717-728.
3. Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 2010; 140: 62-73.
4. Nielsen J, Christiansen J, Lykke-Andersen J, Johnsen AH, Wewer UM, Nielsen FC. A family of insulin-like growth factor II mRNA-binding proteins represses translation in late development. Mol Cell Biol 1999; 19: 1262-1270.
5. Walter O, Prasad M, Lu S, Quinlan RM, Edmiston KL, Khan A. IMP3 is a novel biomarker for triple negative invasive mammary carcinoma associated with a more aggressive phenotype. Hum Pathol 2009; 40: 1528-1533.
6. Jiang Z, Chu PG, Woda BA, Rock KL, Liu Q, Hsieh CC et al. Analysis of RNA-binding protein IMP3 to predict metastasis and prognosis of renal-cell carcinoma: a retrospective study. Lancet Oncol 2006; 7: 556-564.
7. Liu R, Wang X, Chen GY, Dalerba P, Gurney A, Hoey T et al. The prognostic role of a gene signature from tumorigenic breast-cancer cells. N Engl J Med 2007; 356: 217-226.
8. Grimshaw MJ, Cooper L, Papazisis K, Coleman JA, Bohnenkamp HR, Chiapero-Stanke L et al. Mammosphere culture of metastatic breast cancer cells enriches for tumorigenic breast cancer cells. Breast Cancer Res 2008; 10: R52.
9. Tam WL, Lu H, Buikhuisen J, Soh BS, Lim E, Reinhardt F et al. Protein kinase C alpha is a central signaling node and therapeutic target for breast cancer stem cells. Cancer Cell 2013; 24: 347-364.
10. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ et al. In vitro propagation and transcriptional profiling of human mammary stem/ progenitor cells. Genes Dev 2003; 17: 1253-1270.
11. Iliopoulos D, Hirsch HA, Wang G, Struhl K. Inducible formation of breast cancer stem cells and their dynamic equilibrium with non-stem cancer cells via IL6 secretion. Proc Natl Acad Sci USA 2011; 108: 1397-1402.
12. Goel HL, Gritsko T, Pursell B, Chang C, Shultz LD, Greiner DL et al. Regulated splicing of the alpha6 integrin cytoplasmic domain determines the fate of breast cancer stem cells. Cell Rep 2014; 7: 747-761.
13. Rodriguez-Pinilla SM, Sarrio D, Moreno-Bueno G, Rodriguez-Gil Y, Martinez MA, Hernandez L et al. Sox2: a possible driver of the basal-like phenotype in sporadic breast cancer. Mod Pathol 2007; 20: 474-481.
14. Chen Y, Shi L, Zhang L, Li R, Liang J, Yu W et al. The molecular mechanism governing the oncogenic potential of SOX2 in breast cancer. J Biol Chem 2008; 283: 17969-17978.
15. Idowu MO, Kmieciak M, Dumur C, Burton RS, Grimes MM, Powers CN et al. CD44 (+)/CD24(-/low) cancer stem/progenitor cells are more abundant in triplenegative invasive breast carcinoma phenotype and are associated with poor outcome. Hum Pathol 2012; 43: 364-373.
16. Oguro H, Yuan J, Ichikawa H, Ikawa T, Yamazaki S, Kawamoto H et al. Poised lineage specification in multipotential hematopoietic stem and progenitor cells by the polycomb protein Bmi1. Cell Stem Cell 2010; 6: 279-286.
17. Tada Y, Yamaguchi Y, Kinjo T, Song X, Akagi T, Takamura H et al. The stem cell transcription factor ZFP57 induces IGF2 expression to promote anchorageindependent growth in cancer cells. Oncogene 2015; 34: 752-760.
18. Lehmann BD, Bauer JA, Chen X, Sanders ME, 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: 2750-2767.
19. Storci G, Sansone P, Trere D, Tavolari S, Taffurelli M, Ceccarelli C et al. The basallike breast carcinoma phenotype is regulated by SLUG gene expression. J Pathol 2008; 214: 25-37.
20. Proia TA, Keller PJ, Gupta PB, Klebba I, Jones AD, Sedic M et al. Genetic predisposition directs breast cancer phenotype by dictating progenitor cell fate. Cell Stem Cell 2011; 8: 149-163.
21. Zhao X, Sun B, Sun D, Liu T, Che N, GuQet al. Slug promotes hepatocellular cancer cell progression by increasing sox2 and nanog expression. Oncol Rep 2015; 33: 149-156.
22. Su P, Hu J, Zhang H, Li W, Jia M, Zhang X et al. IMP3 expression is associated with epithelial-mesenchymal transition in breast cancer. Int J Clin Exp Pathol 2014; 7: 3008-3017.
23. Cancer Genome Atlas Network, Comprehensive molecular portraits of human breast tumours. Nature 2012; 490: 61-70.
24. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 2013; 6: pl1.
25. 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: 401-404.
26. Calcagno AM, Salcido CD, Gillet JP, Wu CP, Fostel JM, Mumau MD et al. Prolonged drug selection of breast cancer cells and enrichment of cancer stem cell characteristics. J Natl Cancer Inst 2010; 102: 1637-1652.
27. Loi S, Haibe-Kains B, Desmedt C, Lallemand F, Tutt AM, Gillet C et al. Definition of clinically distinct molecular subtypes in estrogen receptor-positive breast carcinomas through genomic grade. J Clin Oncol 2007; 25: 1239-1246.
28. Hajra KM, Chen DY, Fearon ER. The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res 2002; 62: 1613-1618.
29. Bolos V, Peinado H, Perez-Moreno MA, Fraga MF, Esteller M, Cano A. The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J Cell Sci 2003; 116: 499-511.
30. Chaudhary J, Skinner MK. Basic helix-loop-helix proteins can act at the E-box within the serum response element of the c-fos promoter to influence hormoneinduced promoter activation in Sertoli cells. Mol Endocrinol 1999; 13: 774-786.
31. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008; 40: 499-507.
32. Phillips S, Prat A, Sedic M, Proia T, Wronski A, Mazumdar S et al. Cell-state transitions regulated by SLUG are critical for tissue regeneration and tumor initiation. Stem Cell Rep 2014; 2: 633-647.
33. Jonson L, Christiansen J, Hansen TV, Vikesa J, Yamamoto Y, Nielsen FC, IMP3 RNP. safe houses prevent miRNA-directed HMGA2 mRNA decay in cancer and development. Cell Rep 2014; 7: 539-551.
34. Boumahdi S, Driessens G, Lapouge G, Rorive S, Nassar D, Le Mercier M et al. SOX2 controls tumour initiation and cancer stem-cell functions in squamous-cell carcinoma. Nature 2014; 511: 246-250.
35. Leis O, Eguiara A, Lopez-Arribillaga E, Alberdi MJ, Hernandez-Garcia S, Elorriaga K et al. Sox2 expression in breast tumours and activation in breast cancer stem cells. Oncogene 2012; 31: 1354-1365.
36. Zhao D, Pan C, Sun J, Gilbert C, Drews-Elger K, Azzam DJ et al. VEGF drives cancer-initiating stem cells through VEGFR-2/Stat3 signaling to upregulate Myc and Sox2. Oncogene 2015; 34: 3107-3119.
37. Siegle JM, Basin A, Sastre-Perona A, Yonekubo Y, Brown J, Sennett R et al. SOX2 is a cancer-specific regulator of tumour initiating potential in cutaneous squamous cell carcinoma. Nat Commun 2014; 5: 4511.
38. Basu-Roy U, Seo E, Ramanathapuram L, Rapp TB, Perry JA, Orkin SH et al. Sox2 maintains self renewal of tumor-initiating cells in osteosarcomas. Oncogene 2012; 31: 2270-2282.
39. Rybak AP, Tang D. SOX2 plays a critical role in EGFR-mediated selfrenewal of human prostate cancer stem-like cells. Cell Signal 2013; 25: 2734-2742.
40. Singh S, Trevino J, Bora-Singhal N, Coppola D, Haura E, Altiok S et al. EGFR/Src/Akt signaling modulates Sox2 expression and self-renewal of stem-like side-population cells in non-small cell lung cancer. Mol Cancer 2012; 11: 73.
41. Samanta S, Sharma VM, Khan A, Mercurio AM. Regulation of IMP3 by EGFR signaling and repression by ERbeta: implications for triple-negative breast cancer. Oncogene 2012; 31: 4689-4697.
42. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 2008; 100: 672-679.
43. Samanta S, Pursell B, Mercurio AM. IMP3 protein promotes chemoresistance in breast cancer cells by regulating breast cancer resistance protein (ABCG2) expression. J Biol Chem 2013; 288: 12569-12573.
44. Chen CL, Tsukamoto H, Liu JC, Kashiwabara C, Feldman D, Sher L et al. Reciprocal regulation by TLR4 and TGF-beta in tumor-initiating stem-like cells. J Clin Invest 2013; 123: 2832-2849.
45. Bhola NE, Balko JM, Dugger TC, Kuba MG, Sanchez V, Sanders M et al. TGF-beta inhibition enhances chemotherapy action against triple-negative breast cancer. J Clin Invest 2013; 123: 1348-1358.
46. Kono K, Iinuma H, Akutsu Y, Tanaka H, Hayashi N, Uchikado Y et al. Multicenter, phase II clinical trial of cancer vaccination for advanced esophageal cancer with three peptides derived from novel cancer-testis antigens. J Transl Med 2012; 10: 141.
47. Janiszewska M, Suva ML, Riggi N, Houtkooper RH, Auwerx J, Clement-Schatlo V et al. Imp2 controls oxidative phosphorylation and is crucial for preserving glioblastoma cancer stem cells. Genes Dev 2012; 26: 1926-1944.
48. Fillmore CM, Gupta PB, Rudnick JA, Caballero S, Keller PJ, Lander ES et al. Estrogen expands breast cancer stem-like cells through paracrine FGF/Tbx3 signaling. Proc Natl Acad Sci USA 2010; 107: 21737-21742.
49. Goel HL, Pursell B, Chang C, Shaw LM, Mao J, Simin K et al. GLI1 regulates a novel neuropilin-2/alpha6beta1 integrin based autocrine pathway that contributes to breast cancer initiation. EMBO Mol Med 2013; 5: 488-508.
50. Mak P, Leung YK, Tang WY, Harwood C, Ho SM. Apigenin suppresses cancer cell growth through ERbeta. Neoplasia 2006; 8: 896-904.