The sex-determining region Y-Box 4 and homeobox C6 transcriptional networks in prostate cancer progression: Crosstalk with the Wnt, Notch, and PI3K pathways

American Journal of Pathology

Volumn 176, Issue 2, 2010, Pages 518-527

  Moreno, Carlos S ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN; MICRORNA; MIXED LINEAGE LEUKEMIA PROTEIN; NOTCH RECEPTOR; TESTIS DETERMINING FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NKX3.1; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; CANCER GROWTH; IMMUNOHISTOCHEMISTRY; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN ANALYSIS; PROTEIN TARGETING;

EID: 76149131381     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090657     Document Type: Article

References (129)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ: Cancer statistics, 2009. CA Cancer J Clin 2009, 59:225-249
2. Cunha GR, Ricke W, Thomson A, Marker PC, Risbridger G, Hayward SW, Wang YZ, Donjacour AA, Kurita T: Hormonal, cellular, and molecular regulation of normal and neoplastic prostatic development. J Steroid Biochem Mol Biol 2004, 92:221-236
3. Assinder SJ, Dong Q, Kovacevic Z, Richardson DR: The TGF-beta, PI3K/Akt and PTEN pathways: established and proposed biochemical integration in prostate cancer. Biochem J 2009, 417:411-421
4. Shaw A, Bushman W: Hedgehog signaling in the prostate. J Urol 2007, 177:832-838
5. Leong KG, Gao WQ: The Notch pathway in prostate development and cancer. Differentiation 2008, 76:699-716
6. Robinson DR, Zylstra CR, Williams BO: Wnt signaling and prostate cancer. Curr Drug Targets 2008, 9:571-580
7. Thomson AA: Role of androgens and fibroblast growth factors in prostatic development. Reproduction 2001, 121:187-195
8. Freestone SH, Marker P, Grace OC, Tomlinson DC, Cunha GR, Harnden P, Thomson AA: Sonic hedgehog regulates prostatic growth and epithelial differentiation. Dev Biol 2003, 264:352-362
9. Wang XD, Leow CC, Zha J, Tang Z, Modrusan Z, Radtke F, Aguet M, de Sauvage FJ, Gao WQ: Notch signaling is required for normal prostatic epithelial cell proliferation and differentiation. Dev Biol 2006, 290:66-80
10. Orr B, Grace OC, Vanpoucke G, Ashley GR, Thomson AA: A role for notch signaling in stromal survival and differentiation during prostate development. Endocrinology 2009, 150:463-472
11. Blum R, Gupta R, Burger PE, Ontiveros CS, Salm SN, Xiong X, Kamb A, Wesche H, Marshall L, Cutler G, Wang X, Zavadil J, Moscatelli D, Wilson EL: Molecular signatures of prostate stem cells reveal novel signaling pathways and provide insights into prostate cancer. PLoS One 2009, 4:e5722
12. Eguchi M, Nguyen C, Lee SC, Kahn M: ICG-001, a novel small molecule regulator of TCF/beta-catenin transcription. Med Chem 2005, 1:467-472
13. Feldmann G, Fendrich V, McGovern K, Bedja D, Bisht S, Alvarez H, Koorstra JB, Habbe N, Karikari C, Mullendore M, Gabrielson KL, Sharma R, Matsui W, Maitra A: An orally bioavailable small-molecule inhibitor of Hedgehog signaling inhibits tumor initiation and metastasis in pancreatic cancer. Mol Cancer Ther 2008, 7:2725-2735
14. Rao SS, O'Neil J, Liberator CD, Hardwick JS, Dai X, Zhang T, Tyminski E, Yuan J, Kohl NE, Richon VM, Van der Ploeg LH, Carroll PM, Draetta GF, Look AT, Strack PR, Winter CG: Inhibition of NOTCH signaling by gamma secretase inhibitor engages the RB pathway and elicits cell cycle exit in T-cell acute lymphoblastic leukemia cells. Cancer Res 2009, 69:3060-3068
15. Bolos V, Grego-Bessa J, de la Pompa JL: Notch signaling in development and cancer. Endocr Rev 2007, 28:339-363
16. Lai EC: Notch signaling: control of cell communication and cell fate. Development 2004, 131:965-973
17. Nobta M, Tsukazaki T, Shibata Y, Xin C, Moriishi T, Sakano S, Shindo H, Yamaguchi A: Critical regulation of bone morphogenetic proteininduced osteoblastic differentiation by Delta1/Jagged1-activated Notch1 signaling. J Biol Chem 2005, 280:15842-15848
18. Ceder JA, Jansson L, Helczynski L, Abrahamsson PA: Delta-like 1 (Dlk-1), a novel marker of prostate basal and candidate epithelial stem cells, is downregulated by notch signalling in intermediate/transit amplifying cells of the human prostate. Eur Urol 2008, 54: 1344-1353
19. Sciaudone M, Gazzerro E, Priest L, Delany AM, Canalis E: Notch 1 impairs osteoblastic cell differentiation. Endocrinology 2003, 144: 5631-5639
20. Hallahan AR, Pritchard JI, Hansen S, Benson M, Stoeck J, Hatton BA, Russell TL, Ellenbogen RG, Bernstein ID, Beachy PA, Olson JM: The SmoA1 mouse model reveals that notch signaling is critical for the growth and survival of sonic hedgehog-induced medulloblastomas. Cancer Res 2004, 64:7794-7800
21. Sheng T, Li C, Zhang X, Chi S, He N, Chen K, McCormick F, Gatalica Z, Xie J: Activation of the hedgehog pathway in advanced prostate cancer. Mol Cancer 2004, 3:29
22. Sanchez P, Hernandez AM, Stecca B, Kahler AJ, DeGueme AM, Barrett A, Beyna M, Datta MW, Datta S, Ruiz i Altaba A: Inhibition of prostate cancer proliferation by interference with sonic hedgehog-GLI1 signaling. Proc Natl Acad Sci USA 2004, 101:12561-12566
23. Huber MA, Kraut N, Beug H: Molecular requirements for epithelialmesenchymal transition during tumor progression. Curr Opin Cell Biol 2005, 17:548-558
24. Dalrymple S, Antony L, Xu Y, Uzgare AR, Arnold JT, Savaugeot J, Sokoll LJ, De Marzo AM, Isaacs JT: Role of notch-1 and E-cadherin in the differential response to calcium in culturing normal versus malignant prostate cells. Cancer Res 2005, 65:9269-9279
25. Ayyanan A, Civenni G, Ciarloni L, Morel C, Mueller N, Lefort K, Mandinova A, Raffoul W, Fiche M, Dotto GP, Brisken C: Increased Wnt signaling triggers oncogenic conversion of human breast epithelial cells by a Notch-dependent mechanism. Proc Natl Acad Sci USA 2006, 103:3799-3804
26. Bafico A, Liu G, Yaniv A, Gazit A, Aaronson SA: Novel mechanism of Wnt signalling inhibition mediated by Dickkopf-1 interaction with LRP6/Arrow. Nat Cell Biol 2001, 3:683-686
27. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW: Identification of c-MYC as a target of the APC pathway. Science 1998, 281:1509-1512
28. Tetsu O, McCormick F: Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 1999, 398:422-426
29. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, Kinzler KW: Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 1997, 275:1787-1790
30. Verras M, Brown J, Li X, Nusse R, Sun Z: Wnt3a growth factor induces androgen receptor-mediated transcription and enhances cell growth in human prostate cancer cells. Cancer Res 2004, 64: 8860-8866
31. Lu W, Tinsley HN, Keeton A, Qu Z, Piazza GA, Li Y: Suppression of Wnt/beta-catenin signaling inhibits prostate cancer cell proliferation. Eur J Pharmacol 2009, 602:8-14
32. Salas TR, Kim J, Vakar-Lopez F, Sabichi AL, Troncoso P, Jenster G, Kikuchi A, Chen SY, Shemshedini L, Suraokar M, Logothetis CJ, DiGiovanni J, Lippman SM, Menter DG: Glycogen synthase kinase-3 beta is involved in the phosphorylation and suppression of androgen receptor activity. J Biol Chem 2004, 279:19191-19200
33. Wang G, Wang J, Sadar MD: Crosstalk between the androgen receptor and beta-catenin in castrate-resistant prostate cancer. Cancer Res 2008, 68:9918-9927
34. Hall CL, Kang S, MacDougald OA, Keller ET: Role of Wnts in prostate cancer bone metastases. J Cell Biochem 2006, 97:661-672
35. Hall CL, Bafico A, Dai J, Aaronson SA, Keller ET: Prostate cancer cells promote osteoblastic bone metastases through Wnts. Cancer Res 2005, 65:7554-7560
36. Ohigashi T, Mizuno R, Nakashima J, Marumo K, Murai M: Inhibition of Wnt signaling downregulates Akt activity and induces chemosensitivity in PTEN-mutated prostate cancer cells. Prostate 2005, 62: 61-68
37. Liu P, Ramachandran S, Ali-Seyed M, Scharer CD, Laycock N, Dalton WB, Williams H, Karanam S, Datta MW, Jaye D, Moreno CS: Sex-determining region Y box 4 is a transforming oncogene in human prostate cancer cells. Cancer Res 2006, 46:4011-4019
38. Lodygin D, Epanchintsev A, Menssen A, Diebold J, Hermeking H: Functional epigenomics identifies genes frequently silenced in prostate cancer. Cancer Res 2005, 65:4218-4227
39. Kawano Y, Kitaoka M, Hamada Y, Walker MM, Waxman J, Kypta RM: Regulation of prostate cell growth and morphogenesis by Dickkopf-3. Oncogene 2006, 25:6528-6537
40. Kawano Y, Diez S, Uysal-Onganer P, Darrington RS, Waxman J, Kypta RM: Secreted Frizzled-related protein-1 is a negative regulator of androgen receptor activity in prostate cancer. Br J Cancer 2009, 100:1165-1174
41. Dhanasekaran SM, Barrette TR, Ghosh D, Shah R, Varambally S, Kurachi K, Pienta KJ, Rubin MA, Chinnaiyan AM: Delineation of prognostic biomarkers in prostate cancer. Nature 2001, 412:822-826
42. Varambally S, Yu J, Laxman B, Rhodes DR, Mehra R, Tomlins SA, Shah RB, Chandran U, Monzon FA, Becich MJ, Wei JT, Pienta KJ, Ghosh D, Rubin MA, Chinnaiyan AM: Integrative genomic and proteomic analysis of prostate cancer reveals signatures of metastatic progression. Cancer Cell 2005, 8:393-406
43. Yu YP, Landsittel D, Jing L, Nelson J, Ren B, Liu L, McDonald C, Thomas R, Dhir R, Finkelstein S, Michalopoulos G, Becich M, Luo JH: Gene expression alterations in prostate cancer predicting tumor aggression and preceding development of malignancy. J Clin Oncol 2004, 22:2790-2799
44. Rhodes DR, Barrette TR, Rubin MA, Ghosh D, Chinnaiyan AM: Meta-analysis of microarrays: interstudy validation of gene expression profiles reveals pathway dysregulation in prostate cancer. Cancer Res 2002, 62:4427-4433
45. Ernst T, Hergenhahn M, Kenzelmann M, Cohen CD, Bonrouhi M, Weninger A, Klaren R, Grone EF, Wiesel M, Gudemann C, Kuster J, Schott W, Staehler G, Kretzler M, Hollstein M, Grone HJ: Decrease and gain of gene expression are equally discriminatory markers for prostate carcinoma: a gene expression analysis on total and microdissected prostate tissue. Am J Pathol 2002, 160:2169-2180
46. Lapointe J, Li C, Higgins JP, Van De Rijn M, Bair E, Montgomery K, Ferrari M, Egevad L, Rayford W, Bergerheim U, Ekman P, DeMarzo AM, Tibshirani R, Botstein D, Brown PO, Brooks JD, Pollack JR: Gene expression profiling identifies clinically relevant subtypes of prostate cancer. Proc Natl Acad Sci USA 2004, 101:811-816
47. Luo J, Duggan DJ, Chen Y, Sauvageot J, Ewing CM, Bittner ML, Trent JM, Isaacs WB: Human prostate cancer and benign prostatic hyperplasia: molecular dissection by gene expression profiling. Cancer Res 2001, 61:4683-4688
48. Magee JA, Araki T, Patil S, Ehrig T, True L, Humphrey PA, Catalona WJ, Watson MA, Milbrandt J: Expression profiling reveals hepsin overexpression in prostate cancer. Cancer Res 2001, 61:5692-5696
49. Welsh JB, Sapinoso LM, Su AI, Kern SG, Wang-Rodriguez J, Moskaluk CA, Frierson HF Jr, Hampton GM: Analysis of gene expression identifies candidate markers and pharmacological targets in prostate cancer. Cancer Res 2001, 61:5974-5978
50. Hughes C, Murphy A, Martin C, Sheils O, O'Leary J: Molecular pathology of prostate cancer. J Clin Pathol 2005, 58:673-684
51. Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, Sanda MG, Ghosh D, Pienta KJ, Sewalt RG, Otte AP, Rubin MA, Chinnaiyan AM: The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 2002, 419:624-629
52. Tomlins SA, Laxman B, Dhanasekaran SM, Helgeson BE, Cao X, Morris DS, Menon A, Jing X, Cao Q, Han B, Yu J, Wang L, Montie JE, Rubin MA, Pienta KJ, Roulston D, Shah RB, Varambally S, Mehra R, Chinnaiyan AM: Distinct classes of chromosomal rearrangements create oncogenic ETS gene fusions in prostate cancer. Nature 2007, 448:595-599
53. Ramachandran S, Liu P, Young AN, Yin-Goen Q, Lim SD, Laycock N, Amin MB, Carney JK, Marshall FF, Petros JA, Moreno CS: Loss of HOXC6 expression induces apoptosis in prostate cancer cells. Oncogene 2005, 24:188-198
54. Kumar-Sinha C, Tomlins SA, Chinnaiyan AM: Recurrent gene fusions in prostate cancer. Nat Rev Cancer 2008, 8:497-511
55. Carver BS, Tran J, Gopalan A, Chen Z, Shaikh S, Carracedo A, Alimonti A, Nardella C, Varmeh S, Scardino PT, Cordon-Cardo C, Gerald W, Pandolfi PP: Aberrant ERG expression cooperates with loss of PTEN to promote cancer progression in the prostate. Nat Genet 2009, 41:619-624
56. Iljin K, Wolf M, Edgren H, Gupta S, Kilpinen S, Skotheim RI, Peltola M, Smit F, Verhaegh G, Schalken J, Nees M, Kallioniemi O: TMPRSS2 fusions with oncogenic ETS factors in prostate cancer involve unbalanced genomic rearrangements and are associated with HDAC1 and epigenetic reprogramming. Cancer Res 2006, 66:10242-10246
57. Bachmann IM, Halvorsen OJ, Collett K, Stefansson IM, Straume O, Haukaas SA, Salvesen HB, Otte AP, Akslen LA: EZH2 expression is associated with high proliferation rate and aggressive tumor subgroups in cutaneous melanoma and cancers of the endometrium, prostate, and breast. J Clin Oncol 2006, 24:268-273
58. Saramaki OR, Tammela TL, Martikainen PM, Vessella RL, Visakorpi T: The gene for polycomb group protein enhancer of zeste homolog 2 (EZH2) is amplified in late-stage prostate cancer. Genes Chromosomes Cancer 2006, 45:639-645
59. Cooper CS, Foster CS: Concepts of epigenetics in prostate cancer development. Br J Cancer 2009, 100:240-245
60. Wu X, Gong Y, Yue J, Qiang B, Yuan J, Peng X: Cooperation between EZH2: NSPc1-mediated histone H2A ubiquitination and Dnmt1 in HOX gene silencing. Nucleic Acids Res 2008, 36: 3590-3599
61. Yu J, Rhodes DR, Tomlins SA, Cao X, Chen G, Mehra R, Wang X, Ghosh D, Shah RB, Varambally S, Pienta KJ, Chinnaiyan AM: A polycomb repression signature in metastatic prostate cancer predicts cancer outcome. Cancer Res 2007, 67:10657-10663
62. Karanam S, Moreno CS: CONFAC: automated application of comparative genomic promoter analysis to DNA microarray datasets. Nucleic Acids Res 2004, 32:W475-W484
63. Veraksa A, Del Campo M, McGinnis W: Developmental patterning genes and their conserved functions: from model organisms to humans. Mol Genet Metab 2000, 69:85-100
64. Cillo C, Cantile M, Faiella A, Boncinelli E: Homeobox genes in normal and malignant cells. J Cell Physiol 2001, 188:161-169
65. Celetti A, Barba P, Cillo C, Rotoli B, Boncinelli E, Magli MC: Characteristic patterns of HOX gene expression in different types of human leukemia. Int J Cancer 1993, 53:237-244
66. Abate-Shen C: Deregulated homeobox gene expression in cancer: cause or consequence? Nat Rev Cancer 2002, 2:777-785
67. Bodey B, Bodey B Jr, Siegel SE, Luck JV, Kaiser HE: Homeobox B3, B4, and C6 gene product expression in osteosarcomas as detected by immunocytochemistry. Anticancer Res 2000, 20: 2717-2721
68. Bodey B, Bodey B Jr, Siegel SE, Kaiser HE: Immunocytochemical detection of the homeobox B3, B4, and C6 gene products in childhood medulloblastomas/ primitive neuroectodermal tumors. Anticancer Res 2000, 20:1769-1780
69. Dressman HK, Hans C, Bild A, Olson JA, Rosen E, Marcom PK, Liotcheva VB, Jones EL, Vujaskovic Z, Marks J, Dewhirst MW, West M, Nevins JR, Blackwell K: Gene expression profiles of multiple breast cancer phenotypes and response to neoadjuvant chemotherapy. Clin Cancer Res 2006, 12:819-826
70. Bodey B, Bodey B Jr, Groger AM, Siegel SE, Kaiser HE: Immunocytochemical detection of homeobox B3, B4, and C6 gene product expression in lung carcinomas. Anticancer Res 2000, 20:2711-2716
71. Miller GJ, Miller HL, van Bokhoven A, Lambert JR, Werahera PN, Schirripa O, Lucia MS, Nordeen SK: Aberrant HOXC expression accompanies the malignant phenotype in human prostate. Cancer Res 2003, 63:5879-5888
72. Bibikova M, Chudin E, Arsanjani A, Zhou L, Garcia EW, Modder J, Kostelec M, Barker D, Downs T, Fan JB, Wang-Rodriguez J: Expression signatures that correlated with Gleason score and relapse in prostate cancer. Genomics 2007, 89:666-672
73. McCabe CD, Spyropoulos DD, Martin D, Moreno CS: Genome-wide analysis of the homeobox C6 transcriptional network in prostate cancer. Cancer Res 2008, 68:1988-1996
74. Koeneman KS, Yeung F, Chung LW: Osteomimetic properties of prostate cancer cells: a hypothesis supporting the predilection of prostate cancer metastasis and growth in the bone environment. Prostate 1999, 39:246-261
75. Franceschi RT, Wang D, Krebsbach PH, Rutherford RB: Gene therapy for bone formation: in vitro and in vivo osteogenic activity of an adenovirus expressing BMP7. J Cell Biochem 2000, 78:476-486
76. Buijs JT, Rentsch CA, van der Horst G, van Overveld PG, Wetterwald A, Schwaninger R, Henriquez NV, Ten Dijke P, Borovecki F, Markwalder R, Thalmann GN, Papapoulos SE, Pelger RC, Vukicevic S, Cecchini MG, Lowik CW, van der Pluijm G: BMP7, a putative regulator of epithelial homeostasis in the human prostate, is a potent inhibitor of prostate cancer bone metastasis in vivo. Am J Pathol 2007, 171:1047-1057
77. Buijs JT, Henriquez NV, van Overveld PG, van der Horst G, ten Dijke P, van der Pluijm G: TGF-beta and BMP7 interactions in tumour progression and bone metastasis. Clin Exp Metastasis 2007, 24:609-617
78. Grishina IB, Kim SY, Ferrara C, Makarenkova HP, Walden PD: BMP7 inhibits branching morphogenesis in the prostate gland and interferes with Notch signaling. Dev Biol 2005, 288:334-347
79. Ricort JM, Binoux M: Insulin-like growth factor-binding protein-3 activates a phosphotyrosine phosphatase: effects on the insulinlike growth factor signaling pathway. J Biol Chem 2002, 277: 19448-19454
80. van der Geer P, Hunter T, Lindberg RA: Receptor protein-tyrosine kinases and their signal transduction pathways. Annu Rev Cell Biol 1994, 10:251-337
81. Cotton LM, O'Bryan MK, Hinton BT: Cellular signaling by fibroblast growth factors (FGFs) and their receptors (FGFRs) in male reproduction. Endocr Rev 2008, 29:193-216
82. Wissmann C, Wild PJ, Kaiser S, Roepcke S, Stoehr R, Woenckhaus M, Kristiansen G, Hsieh JC, Hofstaedter F, Hartmann A, Knuechel R, Rosenthal A, Pilarsky C: WIF1, a component of the Wnt pathway, is down-regulated in prostate, breast, lung, and bladder cancer. J Pathol 2003, 201:204-212
83. Zou H, Molina JR, Harrington JJ, Osborn NK, Klatt KK, Romero Y, Burgart LJ, Ahlquist DA: Aberrant methylation of secreted frizzledrelated protein genes in esophageal adenocarcinoma and Barrett's esophagus. Int J Cancer 2005, 116:584-591
84. Cheung M, Abu-Elmagd M, Clevers H, Scotting PJ: Roles of Sox4 in central nervous system development. Brain Res Mol Brain Res 2000, 79:180-191
85. Sinner D, Kordich JJ, Spence JR, Opoka R, Rankin S, Lin SC, Jonatan D, Zorn AM, Wells JM: Sox17 and Sox4 differentially regulate beta-catenin/T-cell factor activity and proliferation of colon carcinoma cells. Mol Cell Biol 2007, 27:7802-7815
86. Scharer CD, McCabe CD, Ali-Seyed M, Berger MF, Bulyk ML, Moreno CS: Genome-wide promoter analysis of the SOX4 transcriptional network in prostate cancer cells. Cancer Res 2009, 69: 709-717
87. Takahashi K, Yamanaka S: Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676
88. Fevr T, Robine S, Louvard D, Huelsken J: Wnt/beta-catenin is essential for intestinal homeostasis and maintenance of intestinal stem cells. Mol Cell Biol 2007, 27:7551-7559
89. Ya J, Schilham MW, de Boer PA, Moorman AF, Clevers H, Lamers WH: Sox4-deficiency syndrome in mice is an animal model for common trunk. Circ Res 1998, 83:986-994
90. van de Wetering M, Oosterwegel M, van Norren K, Clevers H: Sox-4, an Sry-like HMG box protein, is a transcriptional activator in lymphocytes. EMBO J 1993, 12:3847-3854
91. Wilson ME, Yang KY, Kalousova A, Lau J, Kosaka Y, Lynn FC, Wang J, Mrejen C, Episkopou V, Clevers HC, German MS: The HMG box transcription factor Sox4 contributes to the development of the endocrine pancreas. Diabetes 2005, 54:3402-3409
92. Nissen-Meyer LS, Jemtland R, Gautvik VT, Pedersen ME, Paro R, Fortunati D, Pierroz DD, Stadelmann VA, Reppe S, Reinholt FP, Del Fattore A, Rucci N, Teti A, Ferrari S, Gautvik KM: Osteopenia, decreased bone formation and impaired osteoblast development in Sox4 heterozygous mice. J Cell Sci 2007, 120:2785-2795
93. Potzner MR, Griffel C, Lutjen-Drecoll E, Bosl MR, Wegner M, Sock E: Prolonged Sox4 expression in oligodendrocytes interferes with normal myelination in the central nervous system. Mol Cell Biol 2007, 27:5316-5326
94. Hunt SM, Clarke CL: Expression and hormonal regulation of the Sox4 gene in mouse female reproductive tissues. Biol Reprod 1999, 61:476-481
95. Andersson A, Ritz C, Lindgren D, Eden P, Lassen C, Heldrup J, Olofsson T, Rade J, Fontes M, Porwit-Macdonald A, Behrendtz M, Hoglund M, Johansson B, Fioretos T: Microarray-based classification of a consecutive series of 121 childhood acute leukemias: prediction of leukemic and genetic subtype as well as of minimal residual disease status. Leukemia 2007, 21:1198-1203
96. Talantov D, Mazumder A, Yu JX, Briggs T, Jiang Y, Backus J, Atkins D, Wang Y: Novel genes associated with malignant melanoma but not benign melanocytic lesions. Clin Cancer Res 2005, 11:7234-7242
97. Sun L, Hui AM, Su Q, Vortmeyer A, Kotliarov Y, Pastorino S, Passaniti A, Menon J, Walling J, Bailey R, Rosenblum M, Mikkelsen T, Fine HA: Neuronal and glioma-derived stem cell factor induces angiogenesis within the brain. Cancer Cell 2006, 9:287-300
98. Lee CJ, Appleby VJ, Orme AT, Chan WI, Scotting PJ: Differential expression of SOX4 and SOX11 in medulloblastoma. J Neurooncol 2002, 57:201-214
99. Aaboe M, Birkenkamp-Demtroder K, Wiuf C, Sorensen FB, Thykjaer T, Sauter G, Jensen KM, Dyrskjot L, Orntoft T: SOX4 expression in bladder carcinoma: clinical aspects and in vitro functional characterization. Cancer Res 2006, 66:3434-3442
100. Friedman R, Bangur C, Zasloff E, Fan L, Wang T, Watanabe Y, Kalos M: Molecular and immunological evaluation of the transcription factor SOX-4 as a lung tumor vaccine antigen. J Immunol 2004, 172:3319-3327
101. Boyd KE, Xiao YY, Fan K, Poholek A, Copeland NG, Jenkins NA, Perkins AS: Sox4 cooperates with Evi1 in AKXD-23 myeloid tumors via transactivation of proviral LTR. Blood 2006, 107:733-741
102. Velasco AM, Gillis KA, Li Y, Brown EL, Sadler TM, Achilleos M, Greenberger LM, Frost P, Bai W, Zhang Y: Identification and validation of novel androgen-regulated genes in prostate cancer. Endocrinology 2004, 145:3913-3924
103. Manalo DJ, Rowan A, Lavoie T, Natarajan L, Kelly BD, Ye SQ, Garcia JG, Semenza GL: Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 2005, 105:659-669
104. van Beijnum JR, Dings RP, van der Linden E, Zwaans BM, Ramaekers FC, Mayo KH, Griffioen AW: Gene expression of tumor angiogenesis dissected: specific targeting of colon cancer angiogenic vasculature. Blood 2006, 108:2339-2348
105. Harvell DM, Richer JK, Allred DC, Sartorius CA, Horwitz KB: Estradiol regulates different genes in human breast tumor xenografts compared with the identical cells in culture. Endocrinology 2006, 147:700-713
106. Banno T, Gazel A, Blumenberg M: Effects of tumor necrosis factoralpha (TNF-alpha) in epidermal keratinocytes revealed using global transcriptional profiling. J Biol Chem 2004, 279:32633-32642
107. Ruebel KH, Leontovich AA, Tanizaki Y, Jin L, Stilling GA, Zhang S, Coonse K, Scheithauer BW, Lombardero M, Kovacs K, Lloyd RV: Effects of TGFbeta1 on gene expression in the HP75 human pituitary tumor cell line identified by gene expression profiling. Endocrine 2008, 33:62-76
108. Lowry WE, Blanpain C, Nowak JA, Guasch G, Lewis L, Fuchs E: Defining the impact of beta-catenin/Tcf transactivation on epithelial stem cells. Genes Dev 2005, 19:1596-1611
109. Kobielak K, Stokes N, de la Cruz J, Polak L, Fuchs E: Loss of a quiescent niche but not follicle stem cells in the absence of bone morphogenetic protein signaling. Proc Natl Acad Sci USA 2007, 104:10063-10068
110. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, Barrette T, Pandey A, Chinnaiyan AM: Large-scale meta-analysis of cancer microarray data identifies common transcriptional profiles of neoplastic transformation and progression. Proc Natl Acad Sci USA 2004, 101:9309-9314
111. Tavazoie SF, Alarcon C, Oskarsson T, Padua D, Wang Q, Bos PD, Gerald WL, Massague J: Endogenous human microRNAs that suppress breast cancer metastasis. Nature 2008, 451:147-152
112. Medina PP, Castillo SD, Blanco S, Sanz-Garcia M, Largo C, Alvarez S, Yokota J, Gonzalez-Neira A, Benitez J, Clevers HC, Cigudosa JC, Lazo PA, Sanchez-Cespedes M: The SRY-HMG box gene: SOX4, is a target of gene amplification at chromosome 6p in lung cancer. Hum Mol Genet 2009, 18:1343-1352
113. Suzuki T, Shen H, Akagi K, Morse HC, Malley JD, Naiman DQ, Jenkins NA, Copeland NG: New genes involved in cancer identified by retroviral tagging. Nat Genet 2002, 32:166-174
114. Lund AH, Turner G, Trubetskoy A, Verhoeven E, Wientjens E, Hulsman D, Russell R, DePinho RA, Lenz J, van Lohuizen M: Genome-wide retroviral insertional tagging of genes involved in cancer in Cdkn2adeficient mice. Nat Genet 2002, 32:160-165
115. Shin MS, Fredrickson TN, Hartley JW, Suzuki T, Agaki K, Morse HC 3rd: High-throughput retroviral tagging for identification of genes involved in initiation and progression of mouse splenic marginal zone lymphomas. Cancer Res 2004, 64:4419-4427
116. Pramoonjago P, Baras AS, Moskaluk CA: Knockdown of Sox4 expression by RNAi induces apoptosis in ACC3 cells. Oncogene 2006, 25:5626-5639
117. Ahn SG, Kim HS, Jeong SW, Kim BE, Rhim H, Shim JY, Kim JW, Lee JH, Kim IK: Sox-4 is a positive regulator of Hep3B and HepG2 cells' apoptosis induced by prostaglandin (PG)A(2) and delta(12)-PGJ(2). Exp Mol Med 2002, 34:243-249
118. Pan X, Zhao J, Zhang WN, Li HY, Mu R, Zhou T, Zhang HY, Gong WL, Yu M, Man JH, Zhang PJ, Li AL, Zhang XM: Induction of SOX4 by DNA damage is critical for p53 stabilization and function. Proc Natl Acad Sci USA 2009, 106:3788-3793
119. Jeffers JR, Parganas E, Lee Y, Yang C, Wang J, Brennan J, MacLean KH, Han J, Chittenden T, Ihle JN, McKinnon PJ, Cleveland JL, Zambetti GP: Puma is an essential mediator of p53-dependent and -independent apoptotic pathways. Cancer Cell 2003, 4: 321-328
120. Lei Q, Jiao J, Xin L, Chang CJ, Wang S, Gao J, Gleave ME, Witte ON, Liu X, Wu H: NKX3.1 stabilizes p53, inhibits AKT activation, and blocks prostate cancer initiation caused by PTEN loss. Cancer Cell 2006, 9:367-378
121. Milne TA, Briggs SD, Brock HW, Martin ME, Gibbs D, Allis CD, Hess JL: MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol Cell 2002, 10:1107-1117
122. Chowdhury T, Brady HJ: Insights from clinical studies into the role of the MLL gene in infant and childhood leukemia. Blood Cells Mol Dis 2008, 40:192-199
123. Abate-Shen C, Banach-Petrosky WA, Sun X, Economides KD, Desai N, Gregg JP, Borowsky AD, Cardiff RD, Shen MM: Nkx3.1; Pten mutant mice develop invasive prostate adenocarcinoma and lymph node metastases. Cancer Res 2003, 63:3886-3890
124. Rana TM: Illuminating the silence: understanding the structure and function of small RNAs. Nat Rev Mol Cell Biol 2007, 8:23-36
125. Robb GB, Rana TM: RNA helicase A interacts with RISC in human cells and functions in RISC loading. Mol Cell 2007, 26:523-537
126. Ma L, Teruya-Feldstein J, Weinberg RA: Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 2007, 449:682-688
127. Ambs S, Prueitt RL, Yi M, Hudson RS, Howe TM, Petrocca F, Wallace TA, Liu CG, Volinia S, Calin GA, Yfantis HG, Stephens RM, Croce CM: Genomic profiling of microRNA and messenger RNA reveals deregulated microRNA expression in prostate cancer. Cancer Res 2008, 68:6162-6170
128. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP: Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005, 102:15545-15550
129. Subramanian A, Kuehn H, Gould J, Tamayo P, Mesirov JP: GSEA-P: a desktop application for gene set enrichment analysis. Bioinformatics 2007, 23:3251-3253