PAX8 promotes tumor cell growth by transcriptionally regulating E2F1 and stabilizing RB protein

Oncogene

Volumn 30, Issue 48, 2011, Pages 4824-4834

  Li, C G ^a,c   Nyman, J E ^a   Braithwaite, A W ^a,b   Eccles, M R ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF SYDNEY   (Australia)

^c STANFORD UNIVERSITY   (United States)

Author keywords

Cell cycle; E2F1; PAX8; RB; Senescence

Indexed keywords

CELL CYCLE PROTEIN 6; CYCLIN A2; MESSENGER RNA; RETINOBLASTOMA PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR PAX8;

ARTICLE; BLADDER CANCER; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL VIABILITY; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; KIDNEY CARCINOMA; NEGATIVE FEEDBACK; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENESCENCE; THYROID CANCER; TUMOR GROWTH; UPREGULATION;

CELL LINE, TUMOR; E2F1 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; PAIRED BOX TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC; RETINOBLASTOMA PROTEIN; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 82455209048     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.190     Document Type: Article

References (62)

1. Berezutskaya E, Bagchi S. (1997). The human papillomavirus E7 oncoprotein functionally interacts with the S4 subunit of the 26 S proteasome. J Biol Chem 272: 30135-30140. (Pubitemid 27512212)
2. Bouchard M, Souabni A, Mandler M, Neubuser A, Busslinger M. (2002). Nephric lineage specification by Pax2 and Pax8. Genes Dev 16: 2958-2970. (Pubitemid 35334743)
3. Bowen NJ, Logani S, Dickerson EB, Kapa LB, Akhtar M, Benigno BB et al. (2007). Emerging roles for PAX8 in ovarian cancer and endosalpingeal development. Gynecol Oncol 104: 331-337. (Pubitemid 46135661)
4. Boyer SN, Wazer DE, Band V. (1996). E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res 56: 4620-4624. (Pubitemid 26338060)
5. Burkhart DL, Sage J. (2008). Cellular mechanisms of tumour suppression by the retinoblastoma gene. Nat Rev Cancer 8: 671-682.
6. Buttitta LA, Edgar BA. (2007). Mechanisms controlling cell cycle exit upon terminal differentiation. Curr Opin Cell Biol 19: 697-704. (Pubitemid 350216428)
7. Chan HM, Krstic-Demonacos M, Smith L, Demonacos C, La Thangue NB. (2001). Acetylation control of the retinoblastoma tumour-suppressor protein. Nat Cell Biol 3: 667-674. (Pubitemid 32624423)
8. Chellappan SP, Hiebert S, Mudryj M, Horowitz JM, Nevins JR. (1991). The E2F transcription factor is a cellular target for the RB protein. Cell 65: 1053-1061. (Pubitemid 121001693)
9. Chen YJ, Campbell HG, Wiles AK, Eccles MR, Reddel RR, Braithwaite AW et al. (2008). PAX8 regulates telomerase reverse transcriptase and telomerase RNA component in glioma. Cancer Res 68: 5724-5732.
10. Dahl E, Koseki H, Balling R. (1997). Pax genes and organogenesis. Bioessays 19: 755-765. (Pubitemid 27383751)
11. Dahl JA, Collas P. (2008). A rapid micro chromatin immunoprecipitation assay (microChIP). Nat Protoc 3: 1032-1045. (Pubitemid 351818692)
12. Daniel L, Lechevallier E, Giorgi R, Sichez H, Zattara-Cannoni H, Figarella-Branger D et al. (2001). Pax-2 expression in adult renal tumors. Hum Pathol 32: 282-287. (Pubitemid 32246801)
13. Dyson N. (1998). The regulation of E2F by pRB-family proteins. Genes Dev 12: 2245-2262. (Pubitemid 28371346)
14. Eccles MR, Yun K, Reeve AE, Fidler AE. (1995). Comparative in situ hybridization analysis of PAX2, PAX8, and WT1 gene transcription in human fetal kidney and Wilms' tumors. Am J Pathol 146: 40-45.
15. Esposito C, Miccadei S, Saiardi A, Civitareale D. (1998). PAX 8 activates the enhancer of the human thyroperoxidase gene. Biochem J 331(Part 1): 37-40. (Pubitemid 28163954)
16. Fabbro D, Pellizzari L, Mercuri F, Tell G, Damante G. (1998). Pax-8 protein levels regulate thyroglobulin gene expression. J Mol Endocrinol 21: 347-354. (Pubitemid 29005406)
17. Fernandez PC, Frank SR, Wang L, Schroeder M, Liu S, Greene J et al. (2003). Genomic targets of the human c-Myc protein. Genes Dev 17: 1115-1129. (Pubitemid 36534986)
18. Flemington EK, Speck SH, Kaelin Jr WG. (1993). E2F-1-mediated transactivation is inhibited by complex formation with the retinoblastoma susceptibility gene product. Proc Natl Acad Sci USA 90: 6914-6918. (Pubitemid 23222358)
19. Frolov MV, Dyson NJ. (2004). Molecular mechanisms of E2Fdependent activation and pRB-mediated repression. J Cell Sci 117(Part 11): 2173-2181. (Pubitemid 38807486)
20. He S, Yoon HS, Suh BJ, Eccles MR.. (2010). PAX3 is extensively expressed in benign and malignant tissues of the melanocytic lineage in humans. J Invest Dermatol 130: 1465-1468.
21. Hibbs K, Skubitz KM, Pambuccian SE, Casey RC, Burleson KM, Oegema Jr TR et al. (2004). Differential gene expression in ovarian carcinoma: identification of potential biomarkers. Am J Pathol 165: 397-414. (Pubitemid 38971371)
22. Higashitsuji H, Itoh K, Nagao T, Dawson S, Nonoguchi K, Kido T et al. (2000). Reduced stability of retinoblastoma protein by gankyrin, an oncogenic ankyrin-repeat protein overexpressed in hepatomas. Nat Med 6: 96-99. (Pubitemid 30048534)
23. Hofmann F, Martelli F, Livingston DM, Wang Z. (1996). The retinoblastoma gene product protects E2F-1 from degradation by the ubiquitin-proteasome pathway. Genes Dev 10: 2949-2959. (Pubitemid 26412522)
24. Hooghe B, Hulpiau P, van Roy F, De Bleser P. (2008). ConTra: a promoter alignment analysis tool for identification of transcription factor binding sites across species. Nucleic Acids Res 36(Web Server issue): W128-W132.
25. Hsu SI, Yang CM, Sim KG, Hentschel DM, O'Leary E, Bonventre JV. (2001). TRIP-Br: a novel family of PHD zinc finger- and bromodomain-interacting proteins that regulate the transcriptional activity of E2F-1/DP-1. EMBO J 20: 2273-2285. (Pubitemid 32410596)
26. Hueber PA, Waters P, Clark P, Eccles M, Goodyer P. (2006). PAX2 inactivation enhances cisplatin-induced apoptosis in renal carcinoma cells. Kidney Int 69: 1139-1145.
27. Johnson DG, Ohtani K, Nevins JR. (1994). Autoregulatory control of E2F1 expression in response to positive and negative regulators of cell cycle progression. Genes Dev 8: 1514-1525. (Pubitemid 24218286)
28. Kalejta RF, Shenk T. (2003). Proteasome-dependent, ubiquitinindependent degradation of the Rb family of tumor suppressors by the human cytomegalovirus pp71 protein. Proc Natl Acad Sci USA 100: 3263-3268. (Pubitemid 36356571)
29. Kelly K, Cochran BH, Stiles CD, Leder P. (1983). Cell-specific regulation of the c-myc gene by lymphocyte mitogens and plateletderived growth factor. Cell 35(3 Part 2): 603-610. (Pubitemid 14168364)
30. Knight JS, Sharma N, Robertson ES. (2005). Epstein-Barr virus latent antigen 3C can mediate the degradation of the retinoblastoma protein through an SCF cellular ubiquitin ligase. Proc Natl Acad Sci USA 102: 18562-18566. (Pubitemid 43011265)
31. Leung JY, Ehmann GL, Giangrande PH, Nevins JR. (2008). A role for Myc in facilitating transcription activation by E2F1. Oncogene 27: 4172-4179. (Pubitemid 351969908)
32. Little MH, Bertram JF. (2009). Is there such a thing as a renal stem cell? J Am Soc Nephrol 20: 2112-2117.
33. Long KB, Srivastava A, HirschMS, Hornick JL. (2010). PAX8 expression in well-differentiated pancreatic endocrine tumors: correlation with clinicopathologic features and comparison with gastrointestinal and pulmonary carcinoid tumors. Am J Surg Pathol 34: 723-729.
34. Macchia PE, Lapi P, Krude H, Pirro MT, Missero C, Chiovato L et al. (1998). PAX8 mutations associated with congenital hypothyroidism caused by thyroid dysgenesis. Nat Genet 19: 83-86. (Pubitemid 28242030)
35. Manning AL, Longworth MS, Dyson NJ. (2010). Loss of pRB causes centromere dysfunction and chromosomal instability. Genes Dev 24: 1364-1376.
36. Mansouri A, Chowdhury K, Gruss P. (1998). Follicular cells of the thyroid gland require Pax8 gene function. Nat Genet 19: 87-90. (Pubitemid 28242031)
37. Miccadei S, Provenzano C, Mojzisek M, Natali PG, Civitareale D. (2005). Retinoblastoma protein acts as Pax 8 transcriptional coactivator. Oncogene 24: 6993-7001. (Pubitemid 41573628)
38. Munro S, Khaire N, Inche A, Carr S, La Thangue NB. (2010). Lysine methylation regulates the pRb tumour suppressor protein. Oncogene 29: 2357-2367.
39. Narlis M, Grote D, Gaitan Y, Boualia SK, BouchardM. (2007). Pax2 and Pax8 regulate branching morphogenesis and nephron differentiation in the developing kidney. J Am Soc Nephrol 18: 1121-1129. (Pubitemid 46536898)
40. Nitta RT, Jameson SA, Kudlow BA, Conlan LA, Kennedy BK. (2006). Stabilization of the retinoblastoma protein by A-type nuclear lamins is required for INK4A-mediated cell cycle arrest. Mol Cell Biol 26: 5360-5372. (Pubitemid 44036205)
41. Ohno M, Zannini M, Levy O, Carrasco N, di Lauro R. (1999). The paired-domain transcription factor Pax8 binds to the upstream enhancer of the rat sodium/iodide symporter gene and participates in both thyroid-specific and cyclic-AMP-dependent transcription. Mol Cell Biol 19: 2051-2060. (Pubitemid 29098263)
42. Peeper DS, Dannenberg JH, Douma S, te Riele H, Bernards R. (2001). Escape from premature senescence is not sufficient for oncogenic transformation by Ras. Nat Cell Biol 3: 198-203. (Pubitemid 32118374)
43. Pfeffer PL, Gerster T, Lun K, Brand M, Busslinger M. (1998). Characterization of three novel members of the zebrafish Pax2/5/8 family: dependency of Pax5 and Pax8 expression on the Pax2.1 (noi) function. Development 125: 3063-3074. (Pubitemid 28434406)
44. Plachov D, Chowdhury K, Walther C, Simon D, Guenet JL, Gruss P. (1990). Pax8, a murine paired box gene expressed in the developing excretory system and thyroid gland. Development 110: 643-651. (Pubitemid 20330539)
45. Poleev A, Wendler F, Fickenscher H, Zannini MS, Yaginuma K, Abbott C et al. (1995). Distinct functional properties of three human paired-boxprotein, PAX8, isoforms generated by alternative splicing in thyroid, kidney and Wilms' tumors. Eur J Biochem 228: 899-911.
46. Rossi DL, Acebron A, Santisteban P. (1995). Function of the homeo and paired domain proteins TTF-1 and Pax-8 in thyroid cell proliferation. J Biol Chem 270: 23139-23142.
47. Sage J, Miller AL, Perez-Mancera PA, Wysocki JM, Jacks T. (2003). Acute mutation of retinoblastoma gene function is sufficient for cell cycle re-entry. Nature 424: 223-228. (Pubitemid 36858693)
48. Sdek P, Ying H, Chang DL, Qiu W, Zheng H, Touitou R et al. (2005). MDM2 promotes proteasome-dependent ubiquitin-independent degradation of retinoblastoma protein. Mol Cell 20: 699-708. (Pubitemid 41740692)
49. Sellers WR, Novitch BG, Miyake S, Heith A, Otterson GA, Kaye FJ et al. (1998). Stable binding to E2F is not required for the retinoblastoma protein to activate transcription, promote differentiation, and suppress tumor cell growth. Genes Dev 12: 95-106. (Pubitemid 28083661)
50. Skapek SX, Pan YR, Lee EY. (2006). Regulation of cell lineage specification by the retinoblastoma tumor suppressor. Oncogene 25: 5268-5276. (Pubitemid 44299087)
51. Stoykova A, Gruss P. (1994). Roles of Pax-genes in developing and adult brain as suggested by expression patterns. J Neurosci 14(3 part 2): 1395-1412. (Pubitemid 24079992)
52. Tong GX, Melamed J, Mansukhani M, Memeo L, Hernandez O, Deng FM et al. (2006). PAX2: a reliable marker for nephrogenic adenoma. Mod Pathol 19: 356-363. (Pubitemid 43276989)
53. Tong GX, Yu WM, Beaubier NT, Weeden EM, Hamele-Bena D, Mansukhani MM et al. (2009). Expression of PAX8 in normal and neoplastic renal tissues: an immunohistochemical study. Mod Pathol 22: 1218-1227.
54. Vilain C, Rydlewski C, Duprez L, Heinrichs C, Abramowicz M, Malvaux P et al. (2001). Autosomal dominant transmission of congenital thyroid hypoplasia due to loss-of-function mutation of PAX8. J Clin Endocrinol Metab 86: 234-238. (Pubitemid 32109801)
55. Weinberg RA. (1995). The retinoblastoma protein and cell cycle control. Cell 81: 323-330.
56. Wells J, Yan PS, Cechvala M, Huang T, Farnham PJ. (2003). Identification of novel pRb binding sites using CpG microarrays suggests that E2F recruits pRb to specific genomic sites during S phase. Oncogene 22: 1445-1460. (Pubitemid 36390594)
57. Wyllie FS, Haughton MF, Rowson JM, Wynford-Thomas D. (1999). Human thyroid cancer cells as a source of isogenic, isophenotypic cell lines with or without functional p53. Br J Cancer 79: 1111-1120. (Pubitemid 29087883)
58. Yen A, Coder D, Varvayanis S. (1997). Concentration of RB protein in nucleus vs cytoplasm is stable as phosphorylation of RB changes during the cell cycle and differentiation. Eur J Cell Biol 72: 159-165. (Pubitemid 27095999)
59. Zalmas LP, Zhao X, Graham AL, Fisher R, Reilly C, Coutts AS et al. (2008). DNA-damage response control of E2F7 and E2F8. EMBO Rep 9: 252-259. (Pubitemid 351330990)
60. Zannini M, Francis-Lang H, Plachov D, Di Lauro R. (1992). Pax-8, a paired domain-containing protein, binds to a sequence overlapping the recognition site of a homeodomain and activates transcription from two thyroid-specific promoters. Mol Cell Biol 12: 4230-4241.
61. Zhang L, Rayner S, Katoku-Kikyo N, Romanova L, Kikyo N. (2007). Successful co-immunoprecipitation of Oct4 and Nanog using crosslinking. Biochem Biophys Res Commun 361: 611-614. (Pubitemid 47238030)
62. Zhang P, Zuo H, Nakamura Y, Nakamura M, Wakasa T, Kakudo K. (2006). Immunohistochemical analysis of thyroid-specific transcription factors in thyroid tumors. Pathol Int 56: 240-245.