Prognostic significance of cytoplasmic SOX9 in invasive ductal carcinoma and metastatic breast cancer

Experimental Biology and Medicine

Volumn 236, Issue 2, 2011, Pages 145-155

  Chakravarty, Geetika ^a   Moroz, Krzysztof ^a   Makridakis, Nick M ^a,b   Lloyd, Shelby Alaine ^a   Galvez, Sarah E ^a   Canavello, Peter R ^a   Lacey, Michelle R ^b,c   Agrawal, Krishna ^a   Mondal, Debasis ^a  

^a TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Tulane University   (United States)

Author keywords

Biomarker; Human breast cancer; Ki 67; Metastasis; Progenitor cells; Prognosis; SOX9

Indexed keywords

ESTROGEN RECEPTOR; KI 67 ANTIGEN; TRANSCRIPTION FACTOR SOX9; TUMOR MARKER;

ARTICLE; BREAST CANCER; CANCER CELL; CANCER INVASION; CELL PROLIFERATION; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOPLASM; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; OVERALL SURVIVAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MICROARRAY;

BIOLOGICAL MARKERS; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CYTOPLASM; GENE EXPRESSION PROFILING; HUMANS; IMMUNOHISTOCHEMISTRY; KI-67 ANTIGEN; LYMPH NODES; MICROARRAY ANALYSIS; NEOPLASM METASTASIS; PROGNOSIS; SEVERITY OF ILLNESS INDEX; SOX9 TRANSCRIPTION FACTOR; SURVIVAL ANALYSIS;

EID: 79951658237     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1258/ebm.2010.010086     Document Type: Article

References (44)

1. Dillon DA, Guidi AJ, Schnitt SJ. Chapter 28: Pathology of invasive breast cancer. In: Harris JR, Lippman ME, Morrow M, Osborne CK, eds. Diseases of the Breast. 4th edn. Philadelphia: Lippincott Williams & Wilkins, 2010
2. Chakravarty G, Roy D, Gonzales M, Gay J, Contreras A, Rosen JM. P190-B, a Rho-GTPase-activating protein, is differentially expressed in terminal end buds and breast cancer. Cell Growth Differ 2000;11:343-54 (Pubitemid 30619562)
3. Fidler IJ. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer 2003;3:453-8
4. Boersma BJ, Reimers M, Yi M, Ludwig JA, Luke BT, Stephens RM, Yfantis HG, Lee DH, Weinstein JN, Ambs S. A stromal gene signature associated with inflammatory breast cancer. Int J Cancer 2008;122:1324-32 (Pubitemid 351287233)
5. van 't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, Schreiber GJ, Kerkhoven RM, Roberts C, Linsley PS, Bernards R, Friend SH. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002;415:530-6
6. Mehlen P, Puisieux A. Metastasis: a question of life or death. Nat Rev Cancer 2006;6:449-58
7. Zhu ML, Kyprianou N. Androgen receptor and growth factor signaling cross-talk in prostate cancer cells. Endocr Relat Cancer 2008;15:841-9
8. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002;2:442-54
9. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial- mesenchymal transitions. Nat Rev Mol Cell Biol 2006;7:131-42 (Pubitemid 43278296)
10. Albini A, Mirisola V, Pfeffer U. Metastasis signatures: genes regulating tumor-microenvironment interactions predict metastatic behavior. Cancer Metastasis Rev 2008;27:75-83
11. Radisky DC, Kenny PA, Bissell MJ. Fibrosis and cancer: do myofibroblasts come also from epithelial cells via EMT? J Cell Biochem 2007;101:830-9
12. Lynch RG. Differentiation and cancer: the conditional autonomy of phenotype. Proc Natl Acad Sci USA 1995;92:647-8
13. Fantozzi A, Christofori G. Mouse models of breast cancer metastasis. Breast Cancer Res 2006;8:212
14. Roarty K, Baxley SE, Crowley MR, Frost AR, Serra R. Loss of TGF-beta or Wnt5a results in an increase in Wnt/beta-catenin activity and redirects mammary tumour phenotype. Breast Cancer Res 2009;11:R19
15. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004;117:927-39 (Pubitemid 38798858)
16. Mani SA, Yang J, Brooks M, Schwaninger G, Zhou A, Miura N, Kutok JL, Hartwell K, Richardson AL, Weinberg RA. Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Proc Natl Acad Sci USA 2007;104:10069-74 (Pubitemid 47175264)
17. Barrionuevo F, Scherer G. SOX E genes: SOX9 and SOX8 in mammalian testis development. Int J Biochem Cell Biol 2010;42:433-6
18. Darido C, Buchert M, Pannequin J, Bastide P, Zalzali H, Mantamadiotis T, Bourgaux JF, Garambois V, Jay P, Blache P, Joubert D, Hollande F. Defective claudin-7 regulation by Tcf-4 and Sox-9 disrupts the polarity and increases the tumorigenicity of colorectal cancer cells. Cancer Res 2008;68:4258-68
19. Passeron T, Valencia JC, Bertolotto C, Hoashi T, Le Pape E, Takahashi K, Ballotti R, Hearing VJ. SOX9 is a key player in ultraviolet B-induced melanocyte differentiation and pigmentation. Proc Natl Acad Sci USA 2007;104:13984-9 (Pubitemid 350003323)
20. Wang H, Leav I, Ibaragi S, Wegner M, Hu GF, Lu ML, Balk SP, Yuan X. SOX9 is expressed in human fetal prostate epithelium and enhances prostate cancer invasion. Cancer Res 2008;68:1625-30 (Pubitemid 351416545)
21. Pask AJ, Harry JL, Graves JA, O'Neill RJ, Layfield SL, Shaw G, Renfree MB. SOX9 has both conserved and novel roles in marsupial sexual differentiation. Genesis 2002;33:131-9 (Pubitemid 34851271)
22. Afonja O, Raaka BM, Huang A, Das S, Zhao X, Helmer E, Juste D, Samuels HH. RAR agonists stimulate SOX9 gene expression in breast cancer cell lines: evidence for a role in retinoid-mediated growth inhibition. Oncogene 2002;21:7850-60 (Pubitemid 35398843)
23. Akiyama H, Kim JE, Nakashima K, Balmes G, Iwai N, Deng JM, Zhang Z, Martin JF, Behringer RR, Nakamura T, de Crombrugghe B. Osteo-chondroprogenitor cells are derived from Sox9 expressing precursors. Proc Natl Acad Sci USA 2005;102:14665-70 (Pubitemid 41457113)
24. Andl T, Reddy ST, Gaddapara T, Millar SE. WNT signals are required for the initiation of hair follicle development. Dev Cell 2002;2:643-653 (Pubitemid 34538144)
25. Blache P, van de Wetering M, Duluc I, Domon C, Berta P, Freund JN, Clevers H, Jay P. SOX9 is an intestine crypt transcription factor, is regulated by the Wnt pathway, and represses the CDX2 and MUC2 genes. J Cell Biol 2004;166:37-47 (Pubitemid 38931915)
26. Bellizzi A, Mangia A, Chiriatti A, Petroni S, Quaranta M, Schittulli F, Malfettone A, Cardone RA, Paradiso A, Reshkin SJ. RhoA protein expression in primary breast cancers and matched lymphocytes is associated with progression of the disease. Int J Mol Med 2008;22:25-31
27. Katoh M. Cancer genomics and genetics of FGFR2 (Review). Int J Oncol 2008;33:233-7
28. Kubo M, Nakamura M, Tasaki A, Yamanaka N, Nakashima H, Nomura M, Kuroki S, Katano M. Hedgehog signaling pathway is a new therapeutic target for patients with breast cancer. Cancer Res 2004;64:6071-4 (Pubitemid 39129406)
29. Moore LD, Isayeva T, Siegal GP, Ponnazhagan S. Silencing of transforming growth factor-beta1 in situ by RNA interference for breast cancer: implications for proliferation and migration in vitro and metastasis in vivo. Clin Cancer Res 2008;14:4961-70
30. Xu Z, Wang W, Deng CX, Man YG. Aberrant p63 and WT-1 expression in myoepithelial cells of pregnancy-associated breast cancer: implications for tumor aggressiveness and invasiveness. Int J Biol Sci 2009;5:82-96
31. Zardawi SJ, O'Toole SA, Sutherland RL, Musgrove EA. Dysregulation of Hedgehog, Wnt and Notch signalling pathways in breast cancer. Histol Histopathol 2009;24:385-98
32. OncomineTM (Compendia Bioscience, Ann Arbor, MI, USA)
33. Elfilali A, Lair S, Verbeke C, La Rosa P, Radvanyi F, Barillot E. ITTACA: a new database for integrated tumor transcriptome array and clinical data analysis. Nucleic Acids Res 2006;34(Database issue):D613-6
34. Endo Y, Deonauth K, Prahalad P, Hoxter B, Zhu Y, Byers SW. Role of Sox-9, ER81 and VE-cadherin in retinoic acid-mediated trans-differentiation of breast cancer cells. PLoS ONE 2008;3:e2714
35. Allred DC, Wu Y, Mao S, Nagtegaal ID, Lee S, Perou CM, Mohsin SK, O'Connell P, Tsimelzon A, Medina D. Ductal carcinoma in situ and the emergence of diversity during breast cancer evolution. Clin Cancer Res 2008;14:370-8 (Pubitemid 351226103)
36. Allred DC, Mohsin SK, Fuqua SA. Histological and biological evolution of human premalignant breast disease. Endocr Relat Cancer 2001;8:47-61 (Pubitemid 32520253)
37. Behbod F, Kittrell FS, LaMarca H, Edwards D, Kerbawy S, Heestand JC, Young E, Mukhopadhyay P, Yeh HW, Allred DC, Hu M, Polyak K, Rosen JM, Medina D. An intraductal human-in-mouse transplantation model mimics the subtypes of ductal carcinoma in situ. Breast Cancer Res 2009;11:R66
38. Miller FR, Santner SJ, Tait L, Dawson PJ. MCF10DCIS.com xenograft model of human comedo ductal carcinoma in situ. J Natl Cancer Inst 2000;92:1185-6
39. Miller FR, Soule HD, Tait L, Pauley RJ, Wolman SR, Dawson PJ, Heppner GH. Xenograft model of progressive human proliferative breast disease. J Natl Cancer Inst 1993;85:1725-32 (Pubitemid 23320842)
40. Gupta SK, Douglas-Jones AG, Fenn N, Morgan JM, Mansel RE. The clinical behavior of breast carcinoma is probably determined at the preinvasive stage (ductal carcinoma in situ). Cancer 1997;80:1740-5 (Pubitemid 27475931)
41. Hu M, Yao J, Carroll DK, Weremowicz S, Chen H, Carrasco D, Richardson A, Violette S, Nikolskaya T, Nikolsky Y, Bauerlein EL, Hahn WC, Gelman RS, Allred C, Bissell MJ, Schnitt S, Polyak K. Regulation of in situ to invasive breast carcinoma transition. Cancer Cell 2008;13:394-406 (Pubitemid 351609443)
42. Osborne CK, Schiff R. Estrogen-receptor biology: continuing progress and therapeutic implications. J Clin Oncol 2005;23:1616-22 (Pubitemid 46211414)
43. Lu B, Fang Y, Xu J, Wang L, Xu F, Xu E, Huang Q, Lai M. Analysis of SOX9 expression in colorectal cancer. Am J Clin Pathol 2008;130:897-904
44. van de Vijver MJ, He YD, van't Veer LJ, Dai H, Hart AA, Voskuil DW, Schreiber GJ, Peterse JL, Roberts C, Marton MJ, Parrish M, Atsma D, Witteveen A, Glas A, Delahaye L, van der Velde T, Bartelink H, Rodenhuis S, Rutgers ET, Friend SH, Bernards R. A gene-expression signature as a predictor of survival in breast cancer. N Engl J Med 2002;347:1999-2009