Expression of the high mobility group A family member p8 is essential to maintaining tumorigenic potential by promoting cell cycle dysregulation in LβT2 cells

Cancer Letters

Volumn 254, Issue 1, 2007, Pages 146-155

  Brannon, K M ^a   Million Passe, C M ^b   White, C R ^a   Bade, N A ^b   King, M W ^c   Quirk, C C ^a,b  

^a INDIANA UNIVERSITY   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Indiana University   (United States)

Author keywords

Aneuploidy; Cell cycle; HMG; p21; p27; p57; p8; Senescence; Tumorigenesis

Indexed keywords

HIGH MOBILITY GROUP A PROTEIN; PROTEIN P8; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENICITY; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CONTROLLED STUDY; DIPLOIDY; GENOMIC INSTABILITY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BETA-GALACTOSIDASE; BLOTTING, WESTERN; CELL AGING; CELL CYCLE; CELL LINE, TRANSFORMED; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLIN-DEPENDENT KINASE INHIBITOR P57; DNA-BINDING PROTEINS; G0 PHASE; G1 PHASE; GENE EXPRESSION; HMGA PROTEINS; MICE; MICE, NUDE; MUTATION; NEOPLASM PROTEINS; NEOPLASMS, EXPERIMENTAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIME FACTORS;

EID: 34447300707     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2007.03.011     Document Type: Article

References (51)

1. Mohammad H.P., Seachrist D.D., Quirk C.C., and Nilson J.H. Reexpression of p8 contributes to tumorigenic properties of pituitary cells and appears in a subset of prolactinomas in transgenic mice that hypersecrete luteinizing hormone. Mol. Endocrinol. 18 (2004) 2583-2593
2. Vasseur S., Vidal Mallo G., Fiedler F., Bodeker H., Canepa E., Moreno S., and Iovanna J.L. Cloning and expression of the human p8, a nuclear protein with mitogenic activity. Eur. J. Biochem. 259 (1999) 670-675
3. Encinar J.A., Mallo G.V., Mizyrycki C., Giono L., Gonzalez-Ros J.M., Rico M., Canepa E., Moreno S., Neira J.L., and Iovanna J.L. Human p8 is a HMG-I/Y-like protein with DNA binding activity enhanced by phosphorylation. J. Biol. Chem. 276 (2001) 2742-2751
4. Iakoucheva L.M., Brown C.J., Lawson J.D., Obradovic Z., and Dunker A.K. Intrinsic disorder in cell-signaling and cancer-associated proteins. J. Mol. Biol. 323 (2002) 573-584
5. Cmarik J.L., Li Y., Ogram S.A., Min H., Reeves R., and Colburn N.H. Tumor promoter induces high mobility group HMG-Y protein expression in transformation-sensitive but not -resistant cells. Oncogene 16 (1998) 3387-3396
6. Ram T.G., Reeves R., and Hosick H.L. Elevated high mobility group-I(Y) gene expression is associated with progressive transformation of mouse mammary epithelial cells. Cancer Res. 53 (1993) 2655-2660
7. Liu W.M., Guerra-Vladusic F.K., Kurakata S., Lupu R., and Kohwi-Shigematsu T. HMG-I(Y) recognizes base-unpairing regions of matrix attachment sequences and its increased expression is directly linked to metastatic breast cancer phenotype. Cancer Res. 59 (1999) 5695-5703
8. Tamimi Y., van der Poel H.G., Denyn M.M., Umbas R., Karthaus H.F., Debruyne F.M., and Schalken J.A. Increased expression of high mobility group protein I(Y) in high grade prostatic cancer determined by in situ hybridization. Cancer Res. 53 (1993) 5512-5516
9. Reeves R., Edberg D.D., and Li Y. Architectural transcription factor HMGI(Y) promotes tumor progression and mesenchymal transition of human epithelial cells. Mol. Cell. Biol. 21 (2001) 575-594
10. Ree A.H., Tvermyr M., Engebraaten O., Rooman M., Rosok O., Hovig E., Meza-Zepeda L.A., Bruland O.S., and Fodstad O. Expression of a novel factor in human breast cancer cells with metastatic potential. Cancer Res. 59 (1999) 4675-4680
11. Su S.B., Motoo Y., Iovanna J.L., Xie M.J., Mouri H., Ohtsubo K., Yamaguchi Y., Watanabe H., Okai T., Matsubara F., and Sawabu N. Expression of p8 in human pancreatic cancer. Clin. Cancer Res. 7 (2001) 309-313
12. Ito Y., Yoshida H., Motoo Y., Miyoshi E., Iovanna J.L., Tomoda C., Uruno T., Takamura Y., Miya A., Kobayashi K., Matsuzuka F., Matsuura N., Kuma K., and Miyauchi A. Expression and cellular localization of p8 protein in thyroid neoplasms. Cancer Lett. 201 (2003) 237-244
13. Ree A.H., Bratland A., Kroes R.A., Aasheim H.C., Florenes V.A., Moskal J.R., Fodstad O., Bruland O.S., and Maelandsmo G.M. Clinical and cell line specific expression profiles of a human gene identified in experimental central nervous system metastases. Anticancer Res. 22 (2002) 1949-1957
14. Vasseur S., Hoffmeister A., Garcia S., Bagnis C., Dagorn J.C., and Iovanna J.L. p8 is critical for tumour development induced by rasV12 mutated protein and E1A oncogene. EMBO Rep. 3 (2002) 165-170
15. Mohammad H.P., Abbud R.A., Parlow A.F., Lewin J.S., and Nilson J.H. Targeted overexpression of luteinizing hormone causes ovary-dependent functional adenomas restricted to cells of the Pit-1 lineage. Endocrinology 144 (2003) 4626-4636
16. Vasseur S., Hoffmeister A., Garcia-Montero A., Mallo G.V., Feil R., Kuhbandner S., Dagorn J.C., and Iovanna J.L. p8-deficient fibroblasts grow more rapidly and are more resistant to adriamycin-induced apoptosis. Oncogene 21 (2002) 1685-1694
17. Mallo G.V., Fiedler F., Calvo E.L., Ortiz E.M., Vasseur S., Keim V., Morisset J., and Iovanna J.L. Cloning and expression of the rat p8 cDNA, a new gene activated in pancreas during the acute phase of pancreatitis, pancreatic development, and regeneration, and which promotes cellular growth. J. Biol. Chem. 272 (1997) 32360-32369
18. Path G., Opel A., Knoll A., and Seufert J. Nuclear protein p8 is associated with glucose-induced pancreatic β-cell growth. Diabetes 53 Suppl. 1 (2004) S82-S85
19. Garcia-Montero A.C., Vasseur S., Giono L.E., Canepa E., Moreno S., Dagorn J.C., and Iovanna J.L. Transforming growth factor β-1 enhances Smad transcriptional activity through activation of p8 gene expression. Biochem. J. 357 (2001) 249-253
20. Bratland A., Risberg K., Maelandsmo G.M., Gutzkow K.B., Olsen O.E., Moghaddam A., Wang M.Y., Hansen C.M., Blomhoff H.K., Berg J.P., Fodstad O., and Ree A.H. Expression of a novel factor, com1, is regulated by 1,25-dihydroxyvitamin D3 in breast cancer cells. Cancer Res. 60 (2000) 5578-5583
21. Jiang W.G., Davies G., Martin T.A., Kynaston H., Mason M.D., and Fodstad O. Com-1/p8 acts as a putative tumour suppressor in prostate cancer. Int. J. Mol. Med. 18 (2006) 981-986
22. Malicet C., Lesavre N., Vasseur S., and Iovanna J.L. p8 inhibits the growth of human pancreatic cancer cells and its expression is induced through pathways involved in growth inhibition and repressed by factors promoting cell growth. Mol. Cancer 2 (2003) 37
23. Quirk C.C., Seachrist D.D., and Nilson J.H. Embryonic expression of the luteinizing hormone β gene appears to be coupled to the transient appearance of p8, a high mobility group-related transcription factor. J. Biol. Chem. 278 (2003) 1680-1685
24. King M.W., Ndiema M., and Neff A.W. Anterior structural defects by misexpression of Xgbx-2 in early Xenopus embryos are associated with altered expression of cell adhesion molecules. Dev. Dyn. 212 (1998) 563-579
25. Darzynkiewicz Z. Current Protocols in Cytometry (1997), J. Wiley & Sons, Inc., New York
26. Shapiro H. Practical Flow Cytometry (1988), Alan R. Liss, Inc., New York
27. de la Torre J., Mitchell A.R., and Summer A.T. Restriction endonuclease/nick translation of fixed mouse chromosomes: a study of factors affecting digestion of chromosomal DNA in situ. Chromosoma 100 (1991) 203-211
28. Passe C.M., Cooper G., and Quirk C.C. The murine p8 gene promoter is activated by activating transcription factor 4 (ATF4) in the gonadotrope-derived LβT2 cell line. Endocrine 30 (2006) 81-91
29. Heaney A.P., Fernando M., and Melmed S. PPAR-gamma receptor ligands: novel therapy for pituitary adenomas. J. Clin. Invest. 111 (2003) 1381-1388
30. Ahuja D., Saenz-Robles M.T., and Pipas J.M. SV40 large T antigen targets multiple cellular pathways to elicit cellular transformation. Oncogene 24 (2005) 7729-7745
31. Dimri G.P., Nakanishi M., Desprez P.Y., Smith J.R., and Campisi J. Inhibition of E2F activity by the cyclin-dependent protein kinase inhibitor p21 in cells expressing or lacking a functional retinoblastoma protein. Mol. Cell. Biol. 16 (1996) 2987-2997
32. Li W.W., Fan J., Hochhauser D., and Bertino J.R. Overexpression of p21waf1 leads to increased inhibition of E2F-1 phosphorylation and sensitivity to anticancer drugs in retinoblastoma-negative human sarcoma cells. Cancer Res. 57 (1997) 2193-2199
33. Rousseau D., Cannella D., Boulaire J., Fitzgerald P., Fotedar A., and Fotedar R. Growth inhibition by CDK-cyclin and PCNA binding domains of p21 occurs by distinct mechanisms and is regulated by ubiquitin-proteasome pathway. Oncogene 18 (1999) 4313-4325
34. Malicet C., Hoffmeister A., Moreno S., Closa D., Dagorn J.C., Vasseur S., and Iovanna J.L. Interaction of the stress protein p8 with Jab1 is required for Jab1-dependent p27 nuclear-to-cytoplasm translocation. Biochem. Biophys. Res. Commun. 339 (2006) 284-289
35. Turgeon J.L., Kimura Y., Waring D.W., and Mellon P.L. Steroid and pulsatile gonadotropin-releasing hormone (GnRH) regulation of luteinizing hormone and GnRH receptor in a novel gonadotrope cell line. Mol. Endocrinol. 10 (1996) 439-450
36. Vasseur S., and Iovanna J.L. [p8 gene is necessary for tumor establishment]. Med. Sci. (Paris) 19 (2003) 1259-1264
37. Andreassen P.R., Lohez O.D., Lacroix F.B., and Margolis R.L. Tetraploid state induces p53-dependent arrest of nontransformed mammalian cells in G1. Mol. Biol. Cell 12 (2001) 1315-1328
38. Margolis R.L., Lohez O.D., and Andreassen P.R. G1 tetraploidy checkpoint and the suppression of tumorigenesis. J. Cell. Biochem. 88 (2003) 673-683
39. Johnson D.G., and Degregori J. Putting the oncogenic and tumor suppressive activities of E2F into context. Curr. Mol. Med. 6 (2006) 731-738
40. Gartel A.L., Najmabadi F., Goufman E., and Tyner A.L. A role for E2F1 in Ras activation of p21(WAF1/CIP1) transcription. Oncogene 19 (2000) 961-964
41. Haapajarvi T., Kivinen L., Heiskanen A., des Bordes C., Datto M.B., Wang X.F., and Laiho M. UV radiation is a transcriptional inducer of p21(Cip1/Waf1) cyclin-kinase inhibitor in a p53-independent manner. Exp. Cell Res. 248 (1999) 272-279
42. Hiyama H., Iavarone A., and Reeves S.A. Regulation of the cdk inhibitor p21 gene during cell cycle progression is under the control of the transcription factor E2F. Oncogene 16 (1998) 1513-1523
43. Loignon M., Fetni R., Gordon A.J., and Drobetsky E.A. A p53-independent pathway for induction of p21waf1cip1 and concomitant G1 arrest in UV-irradiated human skin fibroblasts. Cancer Res. 57 (1997) 3390-3394
44. Geng Y., Lee Y., Welcker M., Swanger J., Zagozdzon A., Winer J.D., Roberts J.M., Kaldis P., Clurman B.E., and Sicinski P. Kinase-independent function of cyclin E. Mol. Cell. 25 (2007) 127-139
45. Zhang H. Life without kinase: cyclin E promotes DNA replication licensing and beyond. Mol. Cell. Biol. 25 (2007) 175-176
46. Dulic V., Kaufmann W.K., Wilson S.J., Tlsty T.D., Lees E., Harper J.W., Elledge S.J., and Reed S.I. p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell 76 (1994) 1013-1023
47. Polyak K., Lee M.H., Erdjument-Bromage H., Koff A., Roberts J.M., Tempst P., and Massague J. Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 78 (1994) 59-66
48. Zhang P., Wong C., DePinho R.A., Harper J.W., and Elledge S.J. Cooperation between the Cdk inhibitors p27(KIP1) and p57(KIP2) in the control of tissue growth and development. Genes Dev. 12 (1998) 3162-3167
49. Kagawa S., Fujiwara T., Kadowaki Y., Fukazawa T., Sok-Joo R., Roth J.A., and Tanaka N. Overexpression of the p21 sdi1 gene induces senescence-like state in human cancer cells: implication for senescence-directed molecular therapy for cancer. Cell Death Differ. 6 (1999) 765-772
50. Tsoli E., Gorgoulis V.G., Zacharatos P., Kotsinas A., Mariatos G., Kastrinakis N.G., Kokotas S., Kanavaros P., Asimacopoulos P., Bramis J., Kletsas D., Papavassiliou A.G., and Kittas C. Low levels of p27 in association with deregulated p53-pRb protein status enhance tumor proliferation and chromosomal instability in non-small cell lung carcinomas. Mol. Med. 7 (2001) 418-429
51. Tsugu A., Sakai K., Dirks P.B., Jung S., Weksberg R., Fei Y.L., Mondal S., Ivanchuk S., Ackerley C., Hamel P.A., and Rutka J.T. Expression of p57(KIP2) potently blocks the growth of human astrocytomas and induces cell senescence. Am. J. Pathol. 157 (2000) 919-932