Elevation of MIR-27b by HPV16 E7 inhibits PPARγ expression and promotes proliferation and invasion in cervical carcinoma cells

International Journal of Oncology

Volumn 47, Issue 5, 2015, Pages 1759-1766

  Zhang, Shimeng ^a,c   Liu, Fei ^a,b   Mao, Xinru ^a   Huang, Jinlan ^a   Yang, Junyao ^a   Yin, Xiaomao ^a   Wu, Lijuan ^a   Zheng, Lei ^a   Wang, Qian ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b Guangzhou Women and Children's Medical Center   (China)

^c Shekou People s Hospital   (China)

Author keywords

Cervical cancer; HPV16 E7; MIR 27b; NHE1; PPAR

Indexed keywords

MICRORNA; MICRORNA 27B; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SODIUM PROTON EXCHANGE PROTEIN 1; UNCLASSIFIED DRUG; CATION TRANSPORT PROTEIN; MIRN27 MICRORNA, HUMAN; ONCOGENE PROTEIN E7, HUMAN PAPILLOMAVIRUS TYPE 16; PROTEIN E7; SLC9A1 PROTEIN, HUMAN; SODIUM PROTON EXCHANGE PROTEIN;

ARTICLE; CANCER GROWTH; CARCINOGENESIS; CARCINOMA CELL; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; UPREGULATION; UTERINE CERVIX CARCINOMA; WESTERN BLOTTING; BIOSYNTHESIS; CARCINOMA; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PAPILLOMAVIRUS INFECTION; PATHOLOGY; TUMOR INVASION; UTERINE CERVIX TUMOR; VIROLOGY;

CARCINOMA; CATION TRANSPORT PROTEINS; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; NEOPLASM INVASIVENESS; PAPILLOMAVIRUS E7 PROTEINS; PAPILLOMAVIRUS INFECTIONS; PPAR GAMMA; SODIUM-HYDROGEN ANTIPORTER; UTERINE CERVICAL NEOPLASMS;

EID: 84942895551     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2015.3162     Document Type: Article

References (47)

1. Comprehensive Cervical Cancer Control: A Guide to Essential Practice. World Health Organization. 2nd edition. Geneva, 2014.
2. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ and Muñoz N: Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 189: 12-19, 1999.
3. Tommasino M, Accardi R, Caldeira S, Dong W, Malanchi I, Smet A and Zehbe I: The role of TP53 in cervical carcinogenesis. Hum Mutat 21: 307-312, 2003.
4. Hwang SG, Lee D, Kim J, Seo T and Choe J: Human papil-lomavirus type 16 E7 binds to E2F1 and activates E2F1-driven transcription in a retinoblastoma protein-independent manner. J Biol Chem 277: 2923-2930, 2002.
5. Bartel DP: MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116: 281-297, 2004.
6. Calin GA and Croce CM: MicroRNA signatures in human cancers. Nat Rev Cancer 6: 857-866, 2006.
7. Di Leva G and Croce CM: Roles of small RNAs in tumor formation. Trends Mol Med 16: 257-267, 2010.
8. Esquela-Kerscher A and Slack FJ: Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 6: 259-269, 2006.
9. Zhang B, Pan X, Cobb GP and Anderson TA: microRNAs as oncogenes and tumor suppressors. Dev Biol 302: 1-12, 2007.
10. Lin Z and Flemington EK: miRNAs in the pathogenesis of oncogenic human viruses. Cancer Lett 305: 186-199, 2011.
11. Zheng ZM and Wang X: Regulation of cellular miRNA expression by human papillomaviruses. Biochim Biophys Acta 1809: 668-677, 2011.
12. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schütz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P, et al: The nuclear receptor superfamily: The second decade. Cell 83: 835-839, 1995.
13. Youssef J and Badr M: Peroxisome proliferator-activated receptors and cancer: Challenges and opportunities. Br J Pharmacol 164: 68-82, 2011.
14. Kim KY, Kim SS and Cheon HG: Differential anti-proliferative actions of peroxisome proliferator-activated receptor-gamma agonists in MCF-7 breast cancer cells. Biochem Pharmacol 72: 530-540, 2006.
15. Sarraf P, Mueller E, Jones D, King FJ, DeAngelo DJ, Partridge JB, Holden SA, Chen LB, Singer S, Fletcher C, et al: Differentiation and reversal of malignant changes in colon cancer through PPARgamma. Nat Med 4: 1046-1052, 1998.
16. Tontonoz P, Singer S, Forman BM, Sarraf P, Fletcher JA, Fletcher CD, Brun R P, Mueller E, Altiok S, Oppenheim H, et al: Terminal differentiation of human liposarcoma cells induced by ligands for peroxisome proliferator-activated receptor gamma and the retinoid X receptor. Proc Natl Acad Sci USA 94: 237-241, 1997.
17. Cellai I, Benvenuti S, Luciani P, Galli A, Ceni E, Simi L, Baglioni S, Muratori M, Ottanelli B, Serio M, et al: Antineoplastic effects of rosiglitazone and PPARgamma transactivation in neuroblastoma cells. Br J Cancer 95: 879-888, 2006.
18. Jung TI, Baek WK, Suh SI, Jang BC, Song DK, Bae JH, Kwon KY, Bae JH, Cha SD, Bae I, et al: Down-regulation of peroxisome proliferator-activated receptor gamma in human cervical carcinoma. Gynecol Oncol 97: 365-373, 2005.
19. Kumar AP, Quake AL, Chang MK, Zhou T, Lim KS, Singh R, Hewitt RE, Salto-Tellez M, Pervaiz S and Clément MV: Repression of NHE1 expression by PPARgamma activation is a potential new approach for specifc inhibition of the growth of tumor cells in vitro and in vivo. Cancer Res 69: 8636-8644, 2009.
20. + exchanger, pH regulation and cancer. Recent Pat Anticancer Drug Discov 8: 85-99, 2013.
21. + exchanger-dependent intracellular alkalinization is an early event in malignant transformation and plays an essential role in the development of subsequent transformation-associated phenotypes. FASEB J 14: 2185-2197, 2000.
22. Tang S, Tao M, McCoy JP Jr and Zheng ZM: The E7 oncoprotein is translated from spliced E6∗I transcripts in high-risk human papillomavirus type 16-or type 18-positive cervical cancer cell lines via translation reinitiation. J Virol 80: 4249-4263, 2006.
23. Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408, 2001.
24. Martinez I, Gardiner AS, Board KF, Monzon FA, Edwards RP and Khan SA: Human papillomavirus type 16 reduces the expression of microRNA-218 in cervical carcinoma cells. Oncogene 27: 2575-2582, 2008.
25. Karbiener M, Fischer C, Nowitsch S, Opriessnig P, Papak C, Ailhaud G, Dani C, Amri EZ and Scheideler M: microRNA miR-27b impairs human adipocyte differentiation and targets PPARgamma. Biochem Biophys Res Commun 390: 247-251, 2009.
26. Jennewein C, von Knethen A, Schmid T and Brüne B: MicroRNA-27b contributes to lipopolysaccharide-medi-ated peroxisome proliferator-activated receptor gamma (PPARgamma) mRNA destabilization. J Biol Chem 285: 11846-11853, 2010.
27. Ghittoni R, Accardi R, Hasan U, Gheit T, Sylla B and Tommasino M: The biological properties of E6 and E7 oncopro-teins from human papillomaviruses. Virus Genes 40: 1-13, 2010.
28. Cardone RA, Busco G, Greco MR, Bellizzi A, Accardi R, Cafarelli A, Monterisi S, Carratù P, Casavola V, Paradiso A, et al: HPV16 E7-dependent transformation activates NHE1 through a PKA-RhoA-induced inhibition of p38alpha. PLoS One 3: e3529, 2008.
29. Myklebust MP, Bruland O, Fluge Ø, Skarstein A, Balteskard L and Dahl O: MicroRNA-15b is induced with E2F-controlled genes in HPV-related cancer. Br J Cancer 105: 1719-1725, 2011.
30. Melar-New M and Laimins LA: Human papillomaviruses modulate expression of microRNA 203 upon epithelial differentiation to control levels of p63 proteins. J Virol 84: 5212-5221, 2010.
31. Kim SY, Kim AY, Lee HW, Son YH, Lee GY, Lee JW, Lee YS and Kim JB: miR-27a is a negative regulator of adipocyte differentiation via suppressing PPARgamma expression. Biochem Biophys Res Commun 392: 323-328, 2010.
32. Ye J, Wu X, Wu D, Wu P, Ni C, Zhang Z, Chen Z, Qiu F, Xu J and Huang J: miRNA-27b targets vascular endothelial growth factor C to inhibit tumor progression and angiogenesis in colorectal cancer. PLoS One 8: e60687, 2013.
33. Wan L, Zhang L, Fan K and Wang J: MiR-27b targets LIMK1 to inhibit growth and invasion of NSCLC cells. Mol Cell Biochem 390: 85-91, 2014.
34. Wang Y, Rathinam R, Walch A and Alahari SK: ST14 (suppression of tumorigenicity 14) gene is a target for miR-27b, and the inhibitory effect of ST14 on cell growth is independent of miR-27b regulation. J Biol Chem 284: 23094-23106, 2009.
35. Chen L, Li H, Han L, Zhang K, Wang G, Wang Y, Liu Y, Zheng Y, Jiang T, Pu P, et al: Expression and function of miR-27b in human glioma. Oncol Rep 26: 1617-1621, 2011.
36. Grommes C, Landreth GE, Sastre M, Beck M, Feinstein DL, Jacobs AH, Schlegel U and Heneka MT: Inhibition of in vivo glioma growth and invasion by peroxisome proliferator-activated receptor gamma agonist treatment. Mol Pharmacol 70: 1524-1533, 2006.
37. + brain tumour stem cells. Br J Cancer 99: 2044-2053, 2008.
38. Chang TH and Szabo E: Induction of differentiation and apoptosis by ligands of peroxisome proliferator-activated receptor gamma in non-small cell lung cancer. Cancer Res 60: 1129-1138, 2000.
39. Sato H, Ishihara S, Kawashima K, Moriyama N, Suetsugu H, Kazumori H, Okuyama T, Rumi MA, Fukuda R, Nagasue N, et al: Expression of peroxisome proliferator-activated receptor (PPAR) gamma in gastric cancer and inhibitory effects of PPARgamma agonists. Br J Cancer 83: 1394-1400, 2000.
40. Chen YX, Zhong XY, Qin YF, Bing W and He LZ: 15d-PGJ2 inhibits cell growth and induces apoptosis of MCG-803 human gastric cancer cell line. World J Gastroenterol 9: 2149-2153, 2003.
41. Motomura W, Okumura T, Takahashi N, Obara T and Kohgo Y: Activation of peroxisome proliferator-activated receptor gamma by troglitazone inhibits cell growth through the increase of p27KiP1 in human. Pancreatic carcinoma cells. Cancer Res 60: 5558-5564, 2000.
42. Motomura W, Nagamine M, Tanno S, Sawamukai M, Takahashi N, Kohgo Y and Okumura T: Inhibition of cell invasion and morphological change by troglitazone in human pancreatic cancer cells. J Gastroenterol 39: 461-468, 2004.
43. Chen HM, Zhang DG, Wu JX, Pei DS and Zheng JN: Ubiquitination of p53 is involved in troglitazone induced apoptosis in cervical cancer cells. Asian Pac J Cancer Prev 15: 2313-2318, 2014.
44. Li QH, Wang LH, Lin YN, Chang GQ, Li HW, Jin WN, Hu RH and Pang TX: Nuclear accumulation of calcineurin B homologous protein 2 (CHP2) results in enhanced proliferation of tumor cells. Genes Cells 16: 416-426, 2011.
45. + exchanger NHE1 by post-translational regulation that is important for cervical cancer cell invasiveness. J Cell Physiol 214: 810-819, 2008.
46. Lin Y, Wang J, Jin W, Wang L, Li H, Ma L, Li Q and Pang T: NHE1 mediates migration and invasion of HeLa cells via regulating the expression and localization of MT1-MMP. Cell Biochem Funct 30: 41-46, 2011.
47. Loo SY, Chang MK, Chua CS, Kumar A P, Pervaiz S and Clement MV: NHE-1: A promising target for novel anti-cancer therapeutics. Curr Pharm Des 18: 1372-1382, 2012.