TBHP-induced oxidative stress alters microRNAs expression in mouse testis

Journal of Assisted Reproduction and Genetics

Volumn 31, Issue 10, 2014, Pages 1287-1293

  Fatemi, Nayeralsadat ^a   Sanati, Mohammad Hossein ^a,b   Shamsara, Mehdi ^b   Moayer, Fariborz ^c   Zavarehei, Mansour Jamali ^d   Pouya, Alireza ^a   Sayyahpour, ForoughAzam ^a   Ayat, Hoda ^e   Gourabi, Hamid ^a  

^a ROYAN INSTITUTE FOR REPRODUCTIVE BIOMEDICINE   (Iran)

^b NATIONAL INSTITUTE OF GENETIC ENGINEERING AND BIOTECHNOLOGY   (Iran)

^c ISLAMIC AZAD UNIVERSITY   (Iran)

^d TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^e SHAHREKORD UNIVERSITY   (Iran)

Author keywords

Male infertility; MicroRNA (miRNA); Oxidative stress; Reactive oxygen species; Tertiary butyl hydroperoxide (TBHP)

Indexed keywords

MICRORNA; MICRORNA 122A; MICRORNA 181B; MICRORNA 34A; MICRORNA 449; MICRORNA LET 7; REACTIVE OXYGEN METABOLITE; TERT BUTYL HYDROPEROXIDE; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE REGULATION; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; GERM CELL; LD 50; LEYDIG CELL; MALE; MALE INFERTILITY; MOUSE; NONHUMAN; OXIDATIVE STRESS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEMINIFEROUS TUBULE; SPERMATOGENESIS; SPERMATOZOON; TESTIS; TESTIS CELL; ANIMAL; BAGG ALBINO MOUSE; DRUG EFFECTS; GENETICS; METABOLISM; OXIDATION REDUCTION REACTION;

MUS;

ANIMALS; INFERTILITY, MALE; MALE; MICE; MICE, INBRED BALB C; MICRORNAS; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SPERMATOGENESIS; TERT-BUTYLHYDROPEROXIDE; TESTIS;

EID: 84918524432     PISSN: 10580468     EISSN: 15737330     Source Type: Journal    
DOI: 10.1007/s10815-014-0302-4     Document Type: Article

References (58)

1. Aboua YG, du Plessis SS, Brooks N. Impact of organic hydroperoxides on rat testicular tissue and epididymal sperm. Afr J Biotechnol. 2009;8:6416–24.
2. Aitken R.J. (1994) A free radical theory of male infertility. Reprod Fertil Dev 6, 19–23; discussion −4.
3. Acharya UR, Mishra M, Tripathy RR, Mishra I. Testicular dysfunction and antioxidative defense system of swiss mice after chromic acid exposure. Reprod Toxicol. 2006;22:87–91.
4. Bao J, Li D, Wang L, Wu J, Hu Y, Wang Z, et al. MicroRNA-449 and microRNA-34b/c function redundantly in murine testes by targeting E2F transcription factor-retinoblastoma protein (E2F-pRb) pathway. J Biol Chem. 2012;287:21686–98.
5. Bauché F, Fouchard M-H, Jégou B. Antioxidant system in rat testicular cells. FEBS Lett. 1994;349:392–6.
6. Bommer GT, Gerin I, Feng Y, Kaczorowski AJ, Kuick R, Love RE, et al. p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol. 2007;17:1298–307.
7. Bou Kheir T, Futoma-Kazmierczak E, Jacobsen A, Krogh A, Bardram L, Hother C, et al. miR-449 inhibits cell proliferation and is down-regulated in gastric cancer. Mol Cancer. 2011;18:10–29.
8. Bouhallier F, Allioli N, Lavial F, Chalmel F, Perrard MH, Durand P, et al. Role of miR-34c microRNA in the late steps of spermatogenesis. RNA. 2010;16:720–31.
9. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science. 2004;303:2011–5.
10. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, Lee KH, et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell. 2007;26:745–52.
11. Chuang JC, Jones PA. Epigenetics and microRNAs. Pediatr Res. 2007;61:24R–9R.
12. de Lamirande E, Gagnon C. Impact of reactive oxygen species on spermatozoa: a balancing act between beneficial and detrimental effects. Hum Reprod. 1995;10:15–21.
13. Dikalov S, Griendling KK, Harrison DG. Measurement of reactive oxygen species in cardiovascular studies. Hypertension. 2007;49:717–27.
14. Dym M, Jia MC, Dirami G, Price JM, Rabin SJ, Mocchetti I, et al. Expression of c-kit receptor and its autophosphorylation in immature rat type A spermatogonia. Biol Reprod. 1995;52:8–19.
15. Farombi EO, Ugwuezunmba MC, Ezenwadu TT, Oyeyemi MO, Ekor M. Tetracycline-induced reproductive toxicity in male rats: effects of vitamin C and nacetylcysteine. Exp Toxicol Pathol. 2008;60:77–85.
16. Fatemi NSM, Jamali Zavarehei M, Ayat H, Esmaeili V, Golkar-Narenji A, Zarabi M, et al. Effect of tertiary-butyl hydroperoxide (TBHP)-induced oxidative stress on mice sperm quality and testis histopathology. Andrologia. 2013;45:232–9.
17. Finney DJ. Probit Regression Analysis. Cambridge: Cambridge Univ. Press; 1977. 333.
18. Golalipour MJ, Azarhoush R, Ghafari S, Gharravi AM, Fazeli SA, Davarian A. Formaldehyde exposure induces histopathological and morphometric changes in the rat testis. Folia Morphol (Warsz). 2007;66:167–71.
19. Fragoso R, Mao T, Wang S, Schaffert S, Gong X, Yue S, et al. Modulating the strength and threshold of NOTCH oncogenic signals by mir-181a-1/b-1. PLoS Genet. 2012;8:e1002855.
20. Gupta S, Malhotra N, Sharma D, Chandra A, Agarwal A. Oxidative stress and its role in female infertility and assisted reproduction: clinical implications. Int J Fertil Steril. 1999;2:147–64.
21. He L, He X, Lim LP, de Stanchina E, Xuan Z, Liang Y, et al. A microRNA component of the p53 tumour suppressor network. Nature. 2007;447:1130–4.
22. Hermeking H. The miR-34 family in cancer and apoptosis. Cell Death Differ. 2010;17:193–9.
23. Hulsmans M, De Keyzer D, Holvoet P. MicroRNAs regulating oxidative stress and inflammation in relation to obesity and atherosclerosis. FASEB J. 2011;25:2515–27.
24. Johnson CD, Esquela-Kerscher A, Stefani G, Byrom M, Kelnar K, Ovcharenko D, et al. The let-7 microRNA represses cell proliferation pathways in human cells. Cancer Res. 2007;67:7713–22.
25. Kaur P, Kaur G, Bansal MP. Tertiary-butyl hydroperoxide induced oxidative stress and male reproductive activity in mice: role of transcription factor NF-kappaB and testicular antioxidant enzymes. Reprod Toxicol. 2006;22:479–84.
26. Kaur P, Kaur G, Bansal MP. Upregulation of AP1 by tertiary butyl hydroperoxide induced oxidative stress and subsequent effect on spermatogenesis in mice testis. Mol Cell Biochem. 2008;308:177–81.
27. Kumar TR et al. Male-mediated dominant lethal mutations in mice following prooxidant treatment. Mutat Res. 1999;444:145–9.
28. Kumar TR et al. Induction of oxidative stress by organic hydroperoxides in testis and epididymal sperm of rats in vivo. J Androl. 2007;28:77–85.
29. Livak KJST. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods. 2001;25:402–8.
30. Ma L, Liu J, Shen J, Liu L, Wu J, Li W, et al. Expression of miR-122 mediated by adenoviral vector induces apoptosis and cell cycle arrest of cancer cells. Cancer Biol Ther. 2010;9:554–61.
31. Mahfouz R, Sharma R, Lackner J, Aziz N, Agarwal A. Evaluation of chemiluminescence and flow cytometry as tools in assessing production of hydrogen peroxide and superoxide anion in human spermatozoa. Fertil Steril. 2009;92:819–27.
32. Majumder PK, Kumar VL. Inhibitory effects of formaldehyde on the reproductive system of male rats. Indian J Physiol Pharmacol. 1995;39:80–2.
33. Makker K, Agarwal A, Sharma R. Oxidative stress & male infertility. Indian J Med Res. 2009;129:357–67.
34. McLachlan RI, de Kretser DM. Male infertility: the case for continued research. Med J Aust. 2001;174:116–7.
35. Ostermeier GC, Goodrich RJ, Moldenhauer JS, Diamond MP, Krawetz SA. A suite of novel human spermatozoal RNAs. J Androl. 2005;26:70–4.
36. Padron OF, Brackett NL, Sharma RK, Lynne CM, Thomas Jr AJ, Agarwal A. Seminal reactive oxygen species and sperm motility and morphology in men with spinal cord injury. Fertil Steril. 1997;67:1115–20.
37. Pentikäinen V, Suomalainen L, Erkkilä K, Martelin E, Parvinen M, Pentikäinen MO, et al. Nuclear factor-kappa b activation in human testicular apoptosis. Am J Pathol. 2002;160:205–18.
38. Rj A. Free radicals, lipid peroxidation and sperm function. Reprod Fertil Dev. 1995;7:659–68.
39. Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, Moskovits N, et al. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell. 2007;26:731–43.
40. Ro S, Park C, Sanders KM, McCarrey JR, Yan W. Cloning and expression profiling of testis-expressed microRNAs. Dev Biol. 2007;311:592–602.
41. Rousseaux S, Caron C, Govin J, Lestrat C, Faure AK, Khochbin S. Establishment of male-specific epigenetic information. Gene. 2005;345:139–53.
42. Rw C. Gene regulation by microRNAs. Curr Opin Genet Dev. 2006;16:203–8.
43. Salminen A, Kaarniranta K, Kauppinen A. Crosstalk between oxidative stress and SIRT1: impact on the aging process. Int J Mol Sci. 2013;14:3834–59.
44. Sengupta A, Molkentin JD, Paik JH, DePinho RA, Yutzey KE. FoxO transcription factors promote cardiomyce survival upon induction of oxidative stress. J Biol Chem. 2011;286:7468–78.
45. Shi LCZ, Zhang J, Li R, Zhao P, Fu Z, You Y. hsa-mir-181a and hsa-mir-181b function as tumor suppressors in human glioma cells. Brain Res. 2008;1236:185–93.
46. Shrilatha B. Occurrence of oxidative impairments, response of antioxidant defences and associated biochemical perturbations in male reproductive milieu in the Streptozotocin-diabetic rat. Int J Androl. 2007;30:508–18.
47. Shrilatha B et al. Early oxidative stress in testis and epididymal sperm in streptozotocin-induced diabetic mice: its progression and genotoxic consequences. ReprodToxicol. 2007;23:578–87.
48. Simone NL, Soule BP, Ly D, Saleh AD, Savage JE, Degraff W, et al. Ionizing radiation-induced oxidative stress alters miRNA expression. PLoS One. 2009;4:e6377.
49. Sun FFH, Liu Q, Tie Y, Zhu J, Xing R, Sun Z, et al. Down-regulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest. FEBS Lett. 2008;582:1564–8.
50. Sun X, Icli B, Wara AK, Belkin N, He S, Kobzik L, et al. MicroRNA-181b regulates NF-κB-mediated vascular inflammation. J Clin Invest. 2012;122:1973–90.
51. Tang M, Xie Y, Yi Y, Wang W. Effects of formaldehyde on germ cells of male mice. Wei Sheng Yan Jiu. 2003;32:544–8.
52. Thomas M, Lieberman J, Lal A. Desperately seeking microRNA targets. Nat Struct Mol Biol. 2010;17:1169–74.
53. Wang A, Fanning L, Anderson DJ, Loughlin KR. Generation of reactive oxygen species by leukocytes and sperm following exposure to urogenital tract infection. Arch Androl. 1997;39:11–7.
54. Welch CCY, Stallings RL. MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells. Oncogene. 2007;26:5017–22.
55. Yamakuchi M, Ferlito M, Lowenstein CJ. miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci U S A. 2008;105:13421–6.
56. Yang XFM, Jiang X, Wu Z, Li Z, Aau M, Yu Q. miR-449a and miR-449b are direct transcriptional targets of E2F1 and negatively regulate pRb-E2F1 activity through a feedback loop by targeting CDK6 and CDC25A. Genes Dev. 2009;23:2388–93.
57. Yan N, Lu Y, Sun H, Tao D, Zhang S, Liu W, et al. A microarray for microRNA profiling in mouse testis tissues. Reproduction. 2007;134:73–9.
58. Yu Z, Raabe T, Hecht NB. MicroRNA Mirn122a reduces expression of the posttranscriptionally regulated germ cell transition protein 2 (Tnp2) messenger RNA (mRNA) by mRNA cleavage. Biol Reprod. 2005;73:427–33.