RKIP and HMGA2 regulate breast tumor survival and metastasis through lysyl oxidase and syndecan-2

Oncogene

Volumn 33, Issue 27, 2014, Pages 3528-3537

  Sun, M ^a,b   Gomes, S ^a   Chen, P ^b   Frankenberger, C A ^a   Sankarasharma, D ^c   Chung, C H ^d   Chada, K K ^c   Rosner, M R ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

breast; HMGA2; LOX; metastasis; RKIP; SDC2

Indexed keywords

CELL ADHESION MOLECULE; HIGH MOBILITY GROUP A2 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR; MICRORNA 200B; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; PROTEIN LYSINE 6 OXIDASE; SYNDECAN 2; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOINFORMATICS; BONE METASTASIS; BREAST CANCER CELL LINE; BREAST CARCINOGENESIS; BREAST TUMOR; CELL GROWTH; CELL INVASION; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; GENE EXPRESSION; GENE ONTOLOGY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; METASTASIS; METASTASIS FREE SURVIVAL; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR GENE; UPREGULATION;

MOUSE MAMMARY TUMOR VIRUS;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HMGA2 PROTEIN; HUMANS; MICE; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; PROGNOSIS; PROTEIN-LYSINE 6-OXIDASE; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; SYNDECAN-2;

EID: 84903901117     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.328     Document Type: Article

References (55)

1. Massague J. Sorting out breast-cancer gene signatures. N Engl J Med 2007; 356: 294-297.
2. Steeg PS. Tumor metastasis: mechanistic insights and clinical challenges. Nat Med 2006; 12: 895-904.
3. Smith SC, Theodorescu D. Learning therapeutic lessons from metastasis suppressor proteins. Nat Rev Cancer 2009; 9: 253-264.
4. Fu Z, Smith PC, Zhang L, Rubin MA, Dunn RL, Yao Z et al. Effects of raf kinase inhibitor protein expression on suppression of prostate cancer metastasis. J Natl Cancer Inst 2003; 95: 878-889.
5. Fu Z, Kitagawa Y, Shen R, Shah R, Mehra R, Rhodes D et al. Metastasis suppressor gene Raf kinase inhibitor protein (RKIP) is a novel prognostic marker in prostate cancer. Prostate 2006; 66: 248-256.
6. Al-Mulla F, Hagan S, Behbehani AI, Bitar MS, George SS, Going JJ et al. Raf kinase inhibitor protein expression in a survival analysis of colorectal cancer patients. J Clin Oncol 2006; 24: 5672-5679.
7. Minoo P, Zlobec I, Baker K, Tornillo L, Terracciano L, Jass JR et al. Loss of raf-1 kinase inhibitor protein expression is associated with tumor progression and metastasis in colorectal cancer. Am J Clin Pathol 2007; 127: 820-827.
8. Yun J, Frankenberger CA, Kuo WL, Boelens MC, Eves EM, Cheng N et al. Signalling pathway for RKIP and Let-7 regulates and predicts metastatic breast cancer. EMBO J 2011; 30: 4500-4514.
9. Hagan S, Al-Mulla F, Mallon E, Oien K, Ferrier R, Gusterson B et al. Reduction of Raf-1 kinase inhibitor protein expression correlates with breast cancer metastasis. Clin Cancer Res 2005; 11: 7392-7397.
10. Dangi-Garimella S, Yun J, Eves EM, Newman M, Erkeland SJ, Hammond SM et al. Raf kinase inhibitory protein suppresses a metastasis signalling cascade involving LIN28 and let-7. EMBO J 2009; 28: 347-358.
11. Xu YF, Yi Y, Qiu SJ, Gao Q, Li YW, Dai CX et al. PEBP1 downregulation is associated to poor prognosis in HCC related to hepatitis B infection. J Hepatol 2010; 53: 872-879.
12. Yeung K, Seitz T, Li S, Janosch P, McFerran B, Kaiser C et al. Suppression of Raf-1 kinase activity and MAP kinase signalling by RKIP. Nature 1999; 401: 173-177.
13. Corbit KC, Trakul N, Eves EM, Diaz B, Marshall M, Rosner MR. Activation of Raf-1 signaling by protein kinase C through a mechanism involving Raf kinase inhibitory protein. J Biol Chem 2003; 278: 13061-13068.
14. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008; 10: 593-601.
15. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 2008; 22: 894-907.
16. Erler JT, Bennewith KL, Nicolau M, Dornhofer N, Kong C, Le QT et al. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 2006; 440: 1222-1226.
17. Erler JT, Bennewith KL, Cox TR, Lang G, Bird D, Koong A et al. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 2009; 15: 35-44.
18. 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: 537-549.
19. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4: 44-57.
20. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ et al. Combinatorial microRNA target predictions. Nat Genet 2005; 37: 495-500.
21. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adeno-sines, indicates that thousands of human genes are microRNA targets. Cell 2005; 120: 15-20.
22. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human MicroRNA targets. PLoS Biol 2004; 2: e363.
23. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. miRBase: tools for microRNA genomics. Nucleic Acids Res 2008; 36: D154-D158.
24. Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E. The role of site accessibility in microRNA target recognition. Nat Genet 2007; 39: 1278-1284.
25. Efron B, Tibshirani R. On testing the significance of sets of genes. Ann Appl Stat 2007; 1: 107-129.
26. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D et al. MicroRNA expression profiles classify human cancers. Nature 2005; 435: 834-838.
27. Csiszar K. Lysyl oxidases: a novel multifunctional amine oxidase family. Prog Nucleic Acid Res Mol Biol 2001; 70: 1-32.
28. Schuetz CS, Bonin M, Clare SE, Nieselt K, Sotlar K, Walter M et al. Progression-specific genes identified by expression profiling of matched ductal carcinomas in situ and invasive breast tumors, combining laser capture microdissection and oligonucleotide microarray analysis. Cancer Res 2006; 66: 5278-5286.
29. Peter ME. Let-7 and miR-200 microRNAs: guardians against pluripotency and cancer progression. Cell Cycle 2009; 8: 843-852.
30. Li Y, VandenBoom 2nd TG, Kong D, Wang Z, Ali S, Philip PA et al. Up-regulation of miR-200 and let-7 by natural agents leads to the reversal of epithelial-to-mesenchymal transition in gemcitabine-resistant pancreatic cancer cells. Cancer Res 2009; 69: 6704-6712.
31. Morishita A, Zaidi M, Mitoro A, Sankarasharma D, Szabolcs M, Okada Y et al. HMGA2 is an in vivo driver of tumor metastasis. Cancer Res 2013; 73: 4289-4299.
32. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 2009; 11: 1487-1495.
33. Lambaerts K, Wilcox-Adelman SA, Zimmermann P. The signaling mechanisms of syndecan heparan sulfate proteoglycans. Curr Opin Cell Biol 2009; 21: 662-669.
34. Barbareschi M, Maisonneuve P, Aldovini D, Cangi MG, Pecciarini L, Angelo Mauri F et al. High syndecan-1 expression in breast carcinoma is related to an aggressive phenotype and to poorer prognosis. Cancer 2003; 98: 474-483.
35. Loussouarn D, Campion L, Sagan C, Frenel JS, Dravet F, Classe JM et al. Prognostic impact of syndecan-1 expression in invasive ductal breast carcinomas. Br J Cancer 2008; 98: 1993-1998.
36. Nikolova V, Koo CY, Ibrahim SA, Wang Z, Spillmann D, Dreier R et al. Differential roles for membrane-bound and soluble syndecan-1 (CD138) in breast cancer progression. Carcinogenesis 2009; 30: 397-407.
37. De Oliveira T, Abiatari I, Raulefs S, Sauliunaite D, Erkan M, Kong B et al. Syndecan-2 promotes perineural invasion and cooperates with K-ras to induce an invasive pancreatic cancer cell phenotype. Mol Cancer 2012; 11: 19.
38. Park H, Kim Y, Lim Y, Han I, Oh ES. Syndecan-2 mediates adhesion and proliferation of colon carcinoma cells. J Biol Chem 2002; 277: 29730-29736.
39. Popovic A, Demirovic A, Spajic B, Stimac G, Kruslin B, Tomas D. Expression and prognostic role of syndecan-2 in prostate cancer. Prostate Cancer Prostatic Dis 2010; 13: 78-82.
40. Marion A, Dieudonne FX, Patino-Garcia A, Lecanda F, Marie PJ, Modrowski D. Calpain-6 is an endothelin-1 signaling dependent protective factor in chemore-sistant osteosarcoma. Int J Cancer 2012; 130: 2514-2525.
41. Minn AJ, Bevilacqua E, Yun J, Rosner MR. Identification of novel metastasis suppressor signaling pathways for breast cancer. Cell Cycle 2012; 11: 2452-2457.
42. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 2003; 31: e15.
43. Team RDC. R: A language and environment for statistical computing. 2009.
44. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004; 5: R80.
45. Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, Holloway A et al. A comparison of background correction methods for two-colour microarrays. Bioinformatics 2007; 23: 2700-2707.
46. Berger JA, Hautaniemi S, Jarvinen AK, Edgren H, Mitra SK, Astola J. Optimized LOWESS normalization parameter selection for DNA microarray data. BMC Bioinformatics 2004; 5: 194.
47. Li Z, Lu J, Sun M, Mi S, Zhang H, Luo RT et al. Distinct microRNA expression profiles in acute myeloid leukemia with common translocations. Proc Natl Acad Sci USA 2008; 105: 15535-15540.
48. Jiang X, Huang H, Li Z, Li Y, Wang X, Gurbuxani S et al. Blockade of miR-150 maturation by MLL-Fusion/MYC/LIN-28 is required for MLL-associated leukemia. Cancer Cell 2012; 22: 524-535.
49. Sun M, Song CX, Huang H, Frankenberger CA, Sankarasharma D, Gomes S et al. HMGA2/TET1/HOXA9 signaling pathway regulates breast cancer growth and metastasis. Proc Natl Acad Sci USA 2013; 110: 9920-9925.
50. Minn AJ, Gupta GP, Padua D, Bos P, Nguyen DX, Nuyten D et al. Lung metastasis genes couple breast tumor size and metastatic spread. Proc Natl Acad Sci USA 2007; 104: 6740-6745.
51. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD et al. Genes that mediate breast cancer metastasis to lung. Nature 2005; 436: 518-524.
52. Enerly E, Steinfeld I, Kleivi K, Leivonen SK, Aure MR, Russnes HG et al. miRNA-mRNA integrated analysis reveals roles for miRNAs in primary breast tumors. PLoS One 2011; 6: e16915.
53. Miller LD, Smeds J, George J, Vega VB, Vergara L, Ploner A et al. An expression signature for p53 status in human breast cancer predicts mutation status, transcrip-tional effects, and patient survival. Proc Natl Acad Sci USA 2005; 102: 13550-13555.
54. Desmedt C, Piette F, Loi S, Wang Y, Lallemand F, Haibe-Kains B et al. Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series. Clin Cancer Res 2007; 13: 3207-3214.
55. Wang Y, Klijn JG, Zhang Y, Sieuwerts AM, Look MP, Yang F et al. Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 2005; 365: 671-679.