MicroRNA-34c enhances murine male germ cell apoptosis through targeting ATF1

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Liang, Xiaoxuan ^a   Zhou, Doudou ^a   Wei, Chao ^a   Luo, Haoshu ^a   Liu, Jiali ^a   Fu, Rui ^a   Cui, Sheng ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 1; MESSENGER RNA; MICRORNA; MICRORNA 34C; PROTEIN BAX; PROTEIN BCL 2; TESTOSTERONE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATF1 GENE; CONTROLLED STUDY; GENE EXPRESSION; GENE FUNCTION; GENE SILENCING; GENE TARGETING; GENETIC TRANSFECTION; GERM CELL; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; MALE GENITAL SYSTEM; MARKER GENE; MOUSE; NONHUMAN; PACHYTENE; PROTEIN EXPRESSION; RNA ANALYSIS; SPERMATID; SPERMATOCYTE;

ACTIVATING TRANSCRIPTION FACTOR 1; ANIMALS; APOPTOSIS; BASE SEQUENCE; BCL-2-ASSOCIATED X PROTEIN; CELL LINE; DRUG RESISTANCE; FEMALE; FLUTAMIDE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE ORDER; GENE SILENCING; MALE; MICE; MICRORNAS; MOLECULAR SEQUENCE DATA; SPERMATOZOA; TESTIS;

MURINAE;

EID: 84859152310     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033861     Document Type: Article

References (56)

1. Carthew RW, Sontheimer EJ, (2009) Origins and Mechanisms of miRNAs and siRNAs. Cell 136: 642-655.
2. Idler RK, Yan W, (2011) Control of messenger RNA fate by RNA binding proteins: an emphasis on mammalian spermatogenesis. J Androl.
3. Nef S, Papaioannou MD, (2010) microRNAs in the Testis: Building Up Male Fertility. Journal of Andrology 31: 26-33.
4. Zamore PD, Ghildiyal M, (2009) Small silencing RNAs: an expanding universe. Nature Reviews Genetics 10: 94-108.
5. Harfe BD, Maatouk DM, Loveland KL, McManus MT, Moore K, (2008) Dicer1 is required for differentiation of the mouse male germline. Biology of Reproduction 79: 696-703.
6. Hayashi K, Lopes SMCD, Kaneda M, Tang FC, Hajkova P, et al. (2008) MicroRNA Biogenesis Is Required for Mouse Primordial Germ Cell Development and Spermatogenesis. Plos One 3.
7. Korhonen HM, Meikar O, Yadav RP, Papaioannou MD, Romero Y, et al. (2011) Dicer Is Required for Haploid Male Germ Cell Differentiation in Mice. Plos One 6.
8. Alvarez-Salas LM, Lopez JA, (2011) Differential effects of miR-34c-3p and miR-34c-5p on SiHa cells proliferation apoptosis, migration and invasion. Biochemical and Biophysical Research Communications 409: 513-519.
9. Bushell M, Cannell IG, (2010) Regulation of Myc by miR-34c A mechanism to prevent genomic instability? Cell Cycle 9: 2726-2730.
10. Ceder Y, Hagman Z, Larne O, Edsjo A, Bjartell A, et al. (2010) miR-34c is downregulated in prostate cancer and exerts tumor suppressive functions. International Journal of Cancer 127: 2768-2776.
11. Hannon GJ, He XY, He L, (2007) The guardian's little helper: MicroRNAs in the p53 tumor suppressor network. Cancer Research 67: 11099-11101.
12. Harris CC, Kumamoto K, Spillare EA, Fujita K, Horikawa I, et al. (2008) Nutlin-3a activates p53 to both down-regulate inhibitor of growth 2 and up-regulate mir-34a, mir-34b, and mir-34c expression, and induce senescence. Cancer Research 68: 3193-3203.
13. Ji Q, Hao XB, Zhang M, Tang WH, Meng Y, et al. (2009) MicroRNA miR-34 Inhibits Human Pancreatic Cancer Tumor-Initiating Cells. Plos One 4.
14. Missero C, Antonini D, Russo MT, De Rosa L, Gorrese M, et al. (2010) Transcriptional Repression of miR-34 Family Contributes to p63-Mediated Cell Cycle Progression in Epidermal Cells. Journal of Investigative Dermatology 130: 1249-1257.
15. Nikitin AY, Corney DC, Flesken-Nikitin A, Godwin AK, Wang W, (2007) MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Research 67: 8433-8438.
16. Rokhlin OW, Scheinker VS, Taghiyev AF, Bumcrot D, Glover RA, et al. (2008) MicroRNA-34 mediates AR-dependent p53-induced apoptosis in prostate cancer. Cancer Biology & Therapy 7: 1288-1296.
17. Yamakuchi M, Lowenstein CJ, (2009) MiR-34, SIRT1 and p53 The feedback loop. Cell Cycle 8: 712-715.
18. Rouault JP, Bouhallier F, Allioli N, Lavial F, Chalmel F, et al. (2010) Role of miR-34c microRNA in the late steps of spermatogenesis. Rna-a Publication of the Rna Society 16: 720-731.
19. Yan NH, Lu YL, Sun HQ, Tao DC, Zhang SZ, et al. (2007) A microarray for microRNA profiling in mouse testis tissues. Reproduction 134: 73-79.
20. Yan W, Ro S, Park C, Sanders KM, McCarrey JR, (2007) Cloning and expression profiling of testis-expressed microRNAs. Developmental Biology 311: 592-602.
21. Zavolan M, Landgraf P, Rusu M, Sheridan R, Sewer A, et al. (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129: 1401-1414.
22. Klemm DJ, Roesler WJ, Boras T, Colton LA, Felder K, et al. (1998) Insulin stimulates cAMP-response element binding protein activity in HepG2 and 3T3-L1 cell lines. Journal of Biological Chemistry 273: 917-923.
23. Dong ZG, Liu KD, Cho YY, Yao K, Nadas J, et al. (2011) Eriodictyol Inhibits RSK2-ATF1 Signaling and Suppresses EGF-induced Neoplastic Cell Transformation. Journal of Biological Chemistry 286: 2057-2066.
24. O'Neill C, Jin XL, (2010) The Presence and Activation of Two Essential Transcription Factors (cAMP Response Element-Binding Protein and cAMP-Dependent Transcription Factor ATF1) in the Two-Cell Mouse Embryo. Biology of Reproduction 82: 459-468.
25. Schutz G, Bleckmann SC, Blendy JA, Rudolph D, Monaghan AP, et al. (2002) Activating transcription factor 1 and CREB are important for cell survival during early mouse development. Molecular and Cellular Biology 22: 1919-1925.
26. Hisaoka M, Ishida T, Kuo TT, Matsuyama A, Imamura T, et al. (2008) Clear cell sarcoma of soft tissue- A clinicopathologic, immunohistochemical, and molecular analysis of 33 cases. American Journal of Surgical Pathology 32: 452-460.
27. Knudson CM, Tung KS, Tourtellotte WG, Brown GA, Korsmeyer SJ, (1995) Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270: 96-99.
28. Yu X, Kubota H, Wang R, Saegusa J, Ogawa Y, et al. (2001) Involvement of Bcl-2 family genes and Fas signaling system in primary and secondary male germ cell apoptosis induced by 2-bromopropane in rat. Toxicol Appl Pharmacol 174: 35-48.
29. Sinha Hikim AP, Swerdloff RS, (1999) Hormonal and genetic control of germ cell apoptosis in the testis. Reviews of Reproduction 4: 38-47.
30. Mackey TJ, Borkowski A, Amin P, Jacobs SC, Kyprianou N, (1998) bcl-2/bax ratio as a predictive marker for therapeutic response to radiotherapy in patients with prostate cancer. Urology 52: 1085-1090.
31. Mauduit C, Bozec A, Chuzel F, Chater S, Paulin C, et al. (2004) The mitochondrial-dependent pathway is chronically affected in testicular germ cell death in adult rats exposed in utero to anti-androgens. Journal of Endocrinology 183: 79-90.
32. Hofmann MC, Hess RA, Goldberg E, Millan JL, (1994) Immortalized germ cells undergo meiosis in vitro. Proc Natl Acad Sci U S A 91: 5533-5537.
33. Chandrasekaran Y, McKee CM, Ye Y, Richburg JH, (2006) Influence of TRP53 status on FAS membrane localization, CFLAR (c-FLIP) ubiquitinylation, and sensitivity of GC-2spd (ts) cells to undergo FAS-mediated apoptosis. Biology of Reproduction 74: 560-568.
34. Yan NH, Lu YL, Sun HQ, Qiu WM, Tao DC, et al. (2009) Microarray profiling of microRNAs expressed in testis tissues of developing primates. Journal of Assisted Reproduction and Genetics 26: 179-186.
35. Meikar O, Da Ros M, Korhonen H, Kotaja N, (2011) Chromatoid body and small RNAs in male germ cells. Reproduction 142: 195-209.
36. Yomgogida K, (2008) Mammalian testis: A target of in vivo electroporation. Development Growth & Differentiation 50: 513-515.
37. Calin GA, Fabbri M, Bottoni A, Shimizu M, Spizzo R, et al. (2011) Association of a MicroRNA/TP53 Feedback Circuitry With Pathogenesis and Outcome of B-Cell Chronic Lymphocytic Leukemia. Jama-Journal of the American Medical Association 305: 59-67.
38. Lujambio A, Calin GA, Villanueva A, Ropero S, Sanchez-Cespedes M, et al. (2008) A microRNA DNA methylation signature for human cancer metastasis. Proceedings of the National Academy of Sciences of the United States of America 105: 13556-13561.
39. Hikim APS, Rajavashisth TB, Hikim IS, Lue YH, Bonavera JJ, et al. (1997) Significance of apoptosis in the temporal and stage-specific loss of germ cells in the adult rat after gonadotropin deprivation. Biology of Reproduction 57: 1193-1201.
40. Hikim APS, Swerdloff RS, (1999) Hormonal and genetic control of germ cell apoptosis in the testis. Reviews of Reproduction 4: 38-47.
41. Skinner MK, Griswold MD, (2005) Sertoli cell biology Amsterdam; Boston Elsevier Academic Press 412 p. of plates xv, 494.
42. Furuchi T, Masuko K, Nishimune Y, Obinata M, Matsui Y, (1996) Inhibition of testicular germ cell apoptosis and differentiation in mice misexpressing Bcl-2 in spermatogonia. Development 122: 1703-1709.
43. Clausen OPF, Oldereid NB, De Angelis P, Wiger R, (2001) Expression of Bcl-2 family proteins and spontaneous apoptosis in normal human testis. Molecular Human Reproduction 7: 403-408.
44. De Rooij DG, Beumer TL, Roepers-Gajadien HL, Gademan IS, Lock TMTW, et al. (2000) Apoptosis regulation in the testis: Involvement of Bcl-2 family members. Molecular Reproduction and Development 56: 353-359.
45. Lee JW, Richburg JH, Younkin SC, Boekelheide K, (1997) The Fas system is a key regulator of germ cell apoptosis in the testis. Endocrinology 138: 2081-2088.
46. Toppari J, Yan W, Suominen J, Samson M, Jegou B, (2000) Involvement of Bcl-2 family proteins in germ cell apoptosis during testicular development in the rat and pro-survival effect of stem cell factor on germ cells in vitro. Molecular and Cellular Endocrinology 165: 115-129.
47. De Cesare D, Sassone-Corsi P, (2000) Transcriptional regulation by cyclic AMP-responsive factors. Prog Nucleic Acid Res Mol Biol 64: 343-369.
48. Green MR, Persengiev SP, (2003) The role of ATF/CREB family members in cell growth, survival and apoptosis. Apoptosis 8: 225-228.
49. Dong L, Wang W, Wang F, Stoner M, Reed JC, et al. (1999) Mechanisms of transcriptional activation of bcl-2 gene expression by 17beta-estradiol in breast cancer cells. Journal of Biological Chemistry 274: 32099-32107.
50. Wilson BE, Mochon E, Boxer LM, (1996) Induction of bcl-2 expression by phosphorylated CREB proteins during B-cell activation and rescue from apoptosis. Molecular and Cellular Biology 16: 5546-5556.
51. Hibbitt O, Coward K, Kubota H, Prathalingham N, Holt W, et al. (2006) In vivo gene transfer by electroporation allows expression of a fluorescent transgene in hamster testis and epididymal sperm and has no adverse effects upon testicular integrity or sperm quality. Biology of Reproduction 74: 95-101.
52. Widlak W, Scieglinska D, Vydra N, Malusecka E, Krawczyk Z, (2003) In vivo electroporation of the testis versus transgenic mice model in functional studies of spermatocyte-speciftic hst70 gene promoter: A comparative study. Molecular Reproduction and Development 65: 382-388.
53. Fedorov Y, Anderson EM, Birmingham A, Reynolds A, Karpilow J, et al. (2006) Off-target effects by siRNA can induce toxic phenotype. Rna-a Publication of the Rna Society 12: 1188-1196.
54. Song R, Ro S, Michaels JD, Park C, McCarrey JR, et al. (2009) Many X-linked microRNAs escape meiotic sex chromosome inactivation. Nature Genetics 41: 488-493.
55. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, et al. (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Research 33: e179.
56. Zhang KY, Shang YL, Liao SY, Zhang W, Nian H, et al. (2007) Uncoupling protein 2 protects testicular germ cells from hyperthermia-induced apoptosis. Biochemical and Biophysical Research Communications 360: 327-332.