The tumor-suppressive microRNA-1/133a cluster targets PDE7A and inhibits cancer cell migration and invasion in endometrial cancer

International Journal of Oncology

Volumn 47, Issue 1, 2015, Pages 325-334

  Yamamoto, Noriko ^a   Nishikawa, Rika ^a   Chiyomaru, Takeshi ^b   Goto, Yusuke ^a   Fukumoto, Ichiro ^a   Usui, Hirokazu ^a   Mitsuhashi, Akira ^a   Enokida, Hideki ^b   Nakagawa, Masayuki ^b   Shozu, Makio ^a   Seki, Naohiko ^a  

^a CHIBA UNIVERSITY   (Japan)

^b KAGOSHIMA UNIVERSITY   (Japan)

Author keywords

Endometrial cancer; MicroRNA; MicroRNA 1; MicroRNA 133a; Phosphodiesterase 7A; Tumor suppressor

Indexed keywords

MICRORNA; MICRORNA 1; MICRORNA 133A; PHOSPHODIESTERASE; PHOSPHODIESTERASE 7A; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; MIRN1 MICRORNA, HUMAN; MIRN133 MICRORNA, HUMAN; PDE7A PROTEIN, HUMAN; PHOSPHODIESTERASE VII;

3' UNTRANSLATED REGION; ADULT; AGED; ARTICLE; BINDING SITE; CANCER CELL; CANCER INHIBITION; CANCER STAGING; CARCINOGENESIS; CELL MIGRATION; CELL PROLIFERATION; CLINICAL ARTICLE; COMPUTER MODEL; CONTROLLED STUDY; DOWN REGULATION; ENDOMETRIUM CANCER; FEMALE; GENE CONTROL; GENE OVEREXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; LYMPH NODE METASTASIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; TUMOR INVASION; WESTERN BLOTTING; CELL MOTION; ENDOMETRIUM TUMOR; GENE EXPRESSION REGULATION; GENETICS; MIDDLE AGED; MULTIGENE FAMILY; PATHOLOGY; TUMOR CELL LINE; VERY ELDERLY;

3' UNTRANSLATED REGIONS; ADULT; AGED; AGED, 80 AND OVER; CELL LINE, TUMOR; CELL MOVEMENT; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 7; ENDOMETRIAL NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; MIDDLE AGED; MULTIGENE FAMILY; NEOPLASM INVASIVENESS;

EID: 84931031637     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2015.2986     Document Type: Article

References (43)

1. Jemal A, Bray F, Center M.M., Ferlay J., Ward E and Forman D: Global cancer statistics. CA Cancer J Clin 61: 69-90, 2011.
2. Rose PG: Endometrial carcinoma. N Engl J Med 335: 640-649, 1996.
3. Creasman WT, Odicino F, Maisonneuve P., Quinn MA, Beller U, Benedet JL, Heintz A.P., Ngan HY and Pecorelli S: Carcinoma of the corpus uteri. FIGO 26th Annual Report on the Results of Treatment in Gynecological Cancer. Int J Gynaecol Obstet 95 (Suppl 1): S105-S143, 2006.
4. Murali R, Soslow RA and Weigelt B: Classification of endometrial carcinoma: More than two types. Lancet Oncol 15: e268-e278, 2014
5. Makker V, Hensley ML, Zhou Q, Iasonos A and Aghajanian CA: Treatment of advanced or recurrent endometrial carcinoma with doxorubicin in patients progressing after paclitaxel/carboplatin: Memorial Sloan-Kettering Cancer Center experience from 1995 to 2009 Int J Gynecol Cancer 23: 929-934, 2013.
6. Bartel DP: MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116: 281-297, 2004
7. Hobert O: Gene regulation by transcription factors and microRNAs. Science 319: 1785-1786, 2008.
8. Iorio MV and Croce CM: MicroRNAs in cancer: Small molecules with a huge impact. J Clin Oncol 27: 5848-5856, 2009
9. Filipowicz W, Bhattacharyya SN and Sonenberg N Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nat Rev Genet 9: 102-114, 2008.
10. Friedman JM and Jones PA: MicroRNAs: Critical mediators of differentiation, development and disease. Swiss Med Wkly 139: 466-472, 2009
11. Nohata N, Hanazawa T, Kikkawa N., Sakurai D, Sasaki K, Chiyomaru T., Kawakami K, Yoshino H, Enokida H, Nakagawa M, et al.: Identification of novel molecular targets regulated by tumor suppressive miR-l/miR-133a in maxillary sinus squamous cell carcinoma. Int J Oncol 39: 1099-1107, 2011.
12. Yoshino H, Chiyomaru T, Enokida H., Kawakami K, Tatarano S, Nishiyama K., Nohata N, Seki N and Nakagawa M: The tumour-suppressive function of miR-1 and miR-133a targeting TAGLN2 in bladder cancer. Br J Cancer 104 808-818, 2011.
13. Kojima S, Chiyomaru T, Kawakami K., Yoshino H, Enokida H, Nohata N., Fuse M, Ichikawa T, Naya Y, Nakagawa M, et al.: Tumour suppressors miR-1 and miR-133a target the oncogenic function of purine nucleoside Phosphorylase (PNP) in prostate cancer. Br J Cancer 106: 405-413, 2012.
14. Mataki H, Enokida H, Chiyomaru T., Mizuno K, Matsushita R, Goto Y., Nishikawa R, Higashimoto I, Samukawa T, Nakagawa M, et al.: Downregulation of the microRNA-l/133a cluster enhances cancer cell migration and invasion in lung-squamous cell carcinoma via regulation of CoroninlC. J Hum Genet 60: 53-61, 2015
15. Berg A, Hoivik EA, Mjøs S, Hoist F, Werner HM, Tangen IL, Taylor-Weiner A, Gibson WJ, Kusonmano K, Wik E, et al.: Molecular profiling of endometrial carcinoma precursor, primary and metastatic lesions suggests different targets for treatment in obese compared to non-obese patients. Oncotarget 6: 1327-1339, 2015
16. Banno K, Yanokura M, Kisu I., Yamagami W, Susumu N and Aoki D: MicroRNAs in endometrial cancer. Int J Clin Oncol 18: 186-192, 2013.
17. Karaayvaz M, Zhang C, Liang S., Shroyer KR and Ju J: Prognostic significance of miR-205 in endometrial cancer. PLoS One 7: e35158, 2012.
18. Itesako T, Seki N, Yoshino H., Chiyomaru T, Yamasaki T, Hidaka H., Yonezawa T, Nohata N, Kinoshita T, Nakagawa M, et al.: The microRNA expression signature of bladder cancer by deep sequencing: The functional significance of the miR-195/497 cluster. PLoS One 9: e84311, 2014
19. Hidaka H, Seki N, Yoshino H., Yamasaki T, Yamada Y, Nohata N., Fuse M, Nakagawa M and Enokida H: Tumor suppressive microRNA-1285 regulates novel molecular targets: Aberrant expression and functional significance in renal cell carcinoma. Oncotarget 3: 44-57, 2012.
20. Kinoshita T, Hanazawa T, Nohata N., Kikkawa N, Enokida H, Yoshino H., Yamasaki T, Hidaka H, Nakagawa M, Okamoto Y, et al.: Tumor suppressive microRNA-218 inhibits cancer cell migration and invasion through targeting laminin-332 in head and neck squamous cell carcinoma. Oncotarget 3: 1386-1400, 2012.
21. Kinoshita T, Nohata N, Hanazawa T., Kikkawa N, Yamamoto N, Yoshino H., Itesako T, Enokida H, Nakagawa M, Okamoto Y, et al.: Tumour-suppressive microRNA-29s inhibit cancer cell migration and invasion by targeting laminin-integrin signalling in head and neck squamous cell carcinoma. Br J Cancer 109: 2636-2645, 2013.
22. Nishikawa R, Goto Y, Kojima S., Enokida H, Chiyomaru T, Kinoshita T., Sakamoto S, Fuse M, Nakagawa M, Naya Y, et al.: Tumor-suppressive microRNA-29s inhibit cancer cell migration and invasion via targeting LAMC1 in prostate cancer. Int J Oncol 45: 401-410, 2014
23. Azevedo MF, Faucz FR, Bimpaki E, Horvath A., Levy I, de Alexandre RB, Ahmad F, Manganiello V and Stratakis CA: Clinical and molecular genetics of the phosphodiesterases (PDEs). Endocr Rev 35: 195-233, 2014
24. Bloom TJ and Beavo JA: Identification and tissue-specific expression of PDE7 phosphodiesterase splice variants. Proc Natl Acad Sci USA 93: 14188-14192, 1996.
25. Han P, Zhu X and Michaeli T: Alternative splicing of the high affinity cAMP-specific phosphodiesterase (PDE7A) mRNA in human skeletal muscle and heart. J Biol Chem 272: 16152-16157, 1997
26. Sasaki T, Kotera J, Yuasa K and Omori K Identification of human PDE7B, a cAMP-specific phosphodiesterase. Biochem Biophys Res Commun 271: 575-583, 2000.
27. Glavas NA, Ostenson C, Schaefer J.B., Vasta V and Beavo JA: T cell activation up-regulates cyclic nucleotide phosphodiesterases 8A1 and 7A3. Proc Natl Acad Sci USA 98: 6319-6324, 2001.
28. Safavi M, Baeeri M and Abdollahi M: New methods for the discovery and synthesis of PDE7 inhibitors as new drugs for neurological and inflammatory disorders. Expert Opin Drug Discov 8: 733-751, 2013.
29. Goto M, Kadoshima-Yamaoka K, Murakawa M., Yoshioka R, Tanaka Y, Inoue H., Murafuji H, Kanki S, Hayashi Y, Nagahira K, et al.: Phosphodiesterase 7A inhibitor ASB16165 impairs proliferation of keratinocytes in vitro and in vivo. Eur J Pharmacol 633: 93-97, 2010.
30. Zhang L, Murray F, Zahno A., Kanter JR, Chou D, Suda R, Fenlon M., Rassenti L, Cottam H, Kipps TJ, et al.: Cyclic nucleotide phosphodiesterase profiling reveals increased expression of phosphodiesterase 7B in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 105: 19532-19537, 2008.
31. Marko D, Romanakis K, Zankl H., FUrstenberger G, Steinbauer B and Eisenbrand G: Induction of apoptosis by an inhibitor of cAMP-specific PDE in malignant murine carcinoma cells over-expressing PDE activity in comparison to their non-malignant counterparts. Cell Biochem Biophys 28: 75-101, 1998.
32. Savai R, Pullamsetti SS, Banat G.A., Weissmann N., Ghofrani HA, Grimminger F and Schermuly RT: Targeting cancer with phosphodiesterase inhibitors. Expert Opin Investig Drugs 19: 117-131, 2010.
33. Dong H, Zitt C, Auriga C., Hatzelmann A and Epstein PM: Inhibition of PDE3, PDE4 and PDE7 potentiates glucocor-ticoid-induced apoptosis and overcomes glucocorticoid resistance in CEM T leukemic cells. Biochem Pharmacol 79: 321-329, 2010.
34. Yamanaka Y, Mammoto T, Kirita T., Mukai M, Mashimo T, Sugimura M., Kishi Y and Nakamura H: Epinephrine inhibits invasion of oral squamous carcinoma cells by modulating intracellular cAMR Cancer Lett 176: 143-148, 2002.
35. Timoshenko AV, Xu G, Chakrabarti S., Lala PK and Chakraborty C: Role of prostaglandin E2 receptors in migration of murine and human breast cancer cells. Exp Cell Res 289: 265-274, 2003.
36. Murata K, Kameyama M, Fukui F., Ohigashi H, Hiratsuka M, Sasaki Y., Kabuto T, Mukai M, Mammoto T, Akedo H, et al.: Phosphodiesterase type III inhibitor, cilostazol, inhibits colon cancer cell motility. Clin Exp Metastasis 17: 525-530, 1999.
37. McEwan DG, Brunton VG, Baillie G.S., Leslie NR, Houslay MD and Frame MC: Chemoresistant KM12C colon cancer cells are addicted to low cyclic AMP levels in a phosphodiesterase 4-regulated compartment via effects on phosphoinositide 3-kinase. Cancer Res 67 5248-5257, 2007
38. Cheng X, Ji Z, Tsalkova T and Mei F: Epac and PKA: A tale of two intracellular cAMP receptors. Acta Biochim Biophys Sin (Shanghai) 40: 651-662, 2008.
39. Dabizzi S, Noci I, Borri P., Borrani E, Giachi M, Balzi M., Taddei GL, Marchionni M, Scarselli GF and Arcangeli A: Luteinizing hormone increases human endometrial cancer cells invasiveness through activation of protein kinase A. Cancer Res 63: 4281-4286, 2003.
40. Howe AK: Regulation of actin-based cell migration by cAMP/PKA. Biochim Biophys Acta 1692: 159-174, 2004
41. McCawley LJ, Li S, Benavidez M., Halbleib J, Wattenberg EV and Hudson LG: Elevation of intracellular cAMP inhibits growth factor-mediated matrix metalloproteinase-9 induction and kera-tinocyte migration. Mol Pharmacol 58: 145-151, 2000.
42. Ou Y, Zheng X, Gao Y., Shu M, Leng T, Li Y., Yin W, Zhu W, Huang Y, Zhou Y, et al.: Activation of cyclic AMP/PKA pathway inhibits bladder cancer cell invasion by targeting MAP4-dependent microtubule dynamics. Urol Oncol 32: 47.e21-47.e28, 2014
43. Han P, Sonati P, Rubin C and Michaeli T: PDE7A1, a cAMP-specific phosphodiesterase, inhibits cAMP-dependent protein kinase by a direct interaction with C. J Biol Chem 281: 15050-15057, 2006.