精子发生及冷冻过程中表观遗传调控的研究进展

Abstract

Abstract: Epigenetics modification is the heritable changes in gene activity which are not involved in changes in the DNA sequences, including DNA methylation and chromatin remodeling, histone modification and non-coding RNAs, which plays important roles in gene expression, spermatogenesis, development and maturation. During spermatogenesis, normal morphology, motility and fertility were proven to be modulated by epigenetic changes. Cryopreservation causes dramatic changes of the sperm viability, motility and fertility, and the cryoinjury might be involved in some epigenetic factors. The epigenetic modifications involved in spermatogenesis and cryopreservation and their relationship were reviewed.

Key words: spermatogenesis; cryopreservation; epigenetic modification

CLC Number:

S814.8

PENG Wen-pei, ZENG Chang-jun. Research Progress on Epigenetic Modifications during Spermatogenesis and Cryopreservation[J]. China Animal Husbandry & Veterinary Medicine, 2014, 41(9): 199-205.

References

1 Aihara H, Nakagawa T, Yasui K,et al. Nucleosomal histone kinase-1 phosphorylates H2A Thr119 during mitosis in the early Drosophila embryo[J]. Genes & Development, 2004, 18(8): 877～888.

2 Aravin A A, Sachidanandam R, Girard A, et al. Developmentally regulated piRNA clusters implicate MILI in transposon control[J]. Science, 2007, 316(5825): 744～747.

3 Bartel D P. MicroRNAs: Genomics, biogenesis, mechanism, and function[J]. Cell, 2004, 116(2): 281～297.

4 Bartel D P. MicroRNAs: Target recognition and regulatory functions[J]. Cell, 2009, 136(2): 215～233.

5 Benchaib M, Braun V, Ressnikof D, et al. Influence of global sperm DNA methylation on IVF results[J]. Human Reproduction, 2005, 20(3): 768～773.

6 Berger S L. Histone modifications in transcriptional regulation[J]. Curr Opin Genet Dev, 2002, 12(2): 142~148.

7 Biggar K K, Dubuc A, Storey K. MicroRNA regulation below zero: Differential expression of miRNA-21 and miRNA-16 during freezing in wood frogs[J]. Cryobiology, 2009, 59(3): 317～321.

8 Bour?his D, Bestor T H. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking DNMT3L[J]. Nature, 2004, 431(7004): 96～99.

9 Carmell M A, Girard A, van de Kant H J, et al. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline[J]. Developmental Cell, 2007, 12(4): 503～514.

10 Carrell D T, Hammoud S S. The human sperm epigenome and its potential role in embryonic development[J]. Mol Hum Reprod, 2010, 16(1): 37～47.

11 Casas-Mollano J A, Jeong B R, Xu J, et al. The MUT9p kinase phosphorylates histone H3 threonine 3 and is necessary for heritable epigenetic silencing in Chlamydomonas[J]. Proceedings of the National Academy of Sciences, 2008, 105(17): 6486～6491.

12 Chan D, Cushnie D W, Neaga O R, et al. Strain-specific defects in testicular development and sperm epigenetic patterns in 5, 10-methylenetetrahydrofolate reductase-deficient mice[J]. Endocrinology, 2010, 151(7): 3363～3373.

13 Chao S, Li J, Jin X, et al. Epigenetic reprogramming of embryos derived from sperm frozen at-20 degrees C[J]. Sci China Life Sci, 2012, 55(4): 349～357.

14 Chong S, Whitelaw E. Epigenetic germline inheritance[J]. Curr Opin Genet Dev, 2004, 14(6): 692～696.

15 Cimmino A, Calin G A, Fabbri M, et al. miR-15 and miR-16 induce apoptosis by targeting BCL2[J]. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(39): 13944～13949.

16 Costa Y, Speed R M, Gautier P, et al. Mouse MAELSTROM: The link between meiotic silencing of unsynapsed chromatin and microRNA pathway[J]. Human Molecular Genetics, 2006, 15(15): 2324～2334.

17 Curry E, Safranski T J, Pratt S L. Differential expression of porcine sperm microRNAs and their association with sperm morphology and motility[J]. Theriogenology, 2011, 76(8): 1532～1539.

18 De Leeuw F, Colenbrander B, Verkleij A. The role membrane damage plays in cold shock and freezing injury[J]. Reprod Domest Anim, 1990, 1: 95～104.

19 DeBaun M R, Niemitz E L, Feinberg A P. Association of in vitro fertilization with beckwith-wiedemann syndrome and epigenetic alterations of LIT1 and H19 [J]. The American Journal of Human Genetics, 2003, 72(1): 156～160.

20 DeManno D A, Cottom J E, Kline M P, et al. Follicle-stimulating hormone promotes histone H3 phosphorylation on serine-10[J]. Molecular Endocrinology, 1999, 13(1): 91～105.

21 Deng W, Lin H. Miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis[J]. Developmental Cell, 2002, 2(6): 819～830.

22 Denomme M M, Mann M R. Genomic imprints as a model for the analysis of epigenetic stability during assisted reproductive technologies[J]. Reproduction, 2012, 144(4): 393～409.

23 Duru N K, Morshedi M, Schuffner A, et al. Cryopreservation-thawing of fractionated human spermatozoa and plasma membrane translocation of phosphatidylserine[J]. Fertil Steril, 2001, 75(2): 263～268.

24 Eun S H, Gan Q, Chen X. Epigenetic regulation of germ cell differentiation[J]. Curr Opin Cell Biol, 2010, 22(6): 737～743.

25 Feng S, Jacobsen S E, Reik W. Epigenetic reprogramming in plant and animal development[J]. Science, 2010, 330(6004): 622～627.

26 Fernandez-Capetillo O, Mahadevaiah S K, Celeste A, et al. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis[J]. Developmental Cell, 2003, 4(4): 497～508.

27 Filipowicz W, Bhattacharyya S N, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight[J]. Nature Reviews Genetics, 2008, 9(2): 102～114.

28 Fraser L, Strzezek J. Is there a relationship between the chromatin status and DNA fragmentation of boar spermatozoa following freezing-thawing[J]. Theriogenology, 2007, 68(2): 248～257.

29 García-Herrero S, Garrido N, Martínez-Conejero J A, et al. Differential transcriptomic profile in spermatozoa achieving pregnancy or not via ICSI[J]. Reproductive Biomedicine Online, 2011, 22(1): 25～36.

30 Gatewood J, Cook G, Balhorn R, et al. Isolation of four core histones from human sperm chromatin representing a minor subset of somatic histones[J]. Journal of Biological Chemistry, 1990, 265(33): 20662～20666.

31 Girard A, Sachidanandam R, Hannon G J, et al. A germline-specific class of small RNAs binds mammalian piwi proteins[J]. Nature, 2006, 442(7099): 199～202.

32 Godmann M, Auger V, Ferraroni-Aguiar V, et al. Dynamic regulation of histone H3 methylation at lysine 4 in mammalian spermatogenesis[J]. Biol Reprod, 2007, 77(5): 754～764.

33 Hajkova P, Erhardt S, Lane N, et al. Epigenetic reprogramming in mouse primordial germ cells[J]. Mechanisms of Development, 2002, 117(1): 15～23.

34 Hammadeh M, Askari A, Georg T, et al. Effect of freeze-thawing procedure on chromatin stability, morphological alteration and membrane integrity of human spermatozoa in fertile and subfertile men[J]. International Journal of Andrology, 1999, 22(3): 155～162.

35 Hayashi K, de Sousa Lopes S M C, Kaneda M, et al. Micro-RNA biogenesis is required for mouse primordial germ cell development and spermatogenesis[J]. PLoS One, 2008, 3(3): e1738.

36 Horike S, Ferreira J C, Meguro-Horike M, et al. Screening of DNA methylation at the H19 promoter or the distal region of its ICR1 ensures efficient detection of chromosome 11p15 epimutations in Russell-Silver syndrome[J]. Am J Med Genet A, 2009, 149A(11): 2415～2423.

37 Houshdaran S, Cortessis V K, Siegmund K, et al. Widespread epigenetic abnormalities suggest a broad DNA methylation erasure defect in abnormal human sperm[J]. PLoS One, 2007, 2(12): e1289.

38 Hu J, Zhu W, Liu W, et al. Factors affecting fecundity among sperm donors: A multivariate analysis[J]. Andrologia, 2011, 43(3): 155～162.

39 Huang Y, Wang Y, Wang M, et al. Differential methylation of TSP50 and mTSP50 genes in different types of human tissues and mouse spermatic cells[J]. Biochemical and Biophysical Research Communications, 2008, 374(4): 658～661.

40 Kelly T, Trasler J. Developmental biology: Frontiers for clinical genetics. reproductive epigenetics[J]. Clinical Genetics, 2004, 65(4): 247～260.

41 Khalil A M, Boyar F Z, Driscoll D J. Dynamic histone modifications mark sex chromosome inactivation and reactivation during mammalian spermatogenesis[J]. Proc Natl Acad Sci USA, 2004, 101(47): 16583～16587.

42 Khalil A M, Wahlestedt C. Epigenetic mechanisms of gene regulation during mammalian spermatogenesis[J]. Epigenetics, 2008, 3(1): 21～28.

43 Khazamipour N, Noruzinia M, Fatehmanesh P, et al. MTHFR promoter hypermethylation in testicular biopsies of patients with non-obstructive azoospermia: The role of epigenetics in male infertility[J]. Human Reproduction, 2009, 24(9): 2361～2364.

44 Kimmins S, Sassone-Corsi P. Chromatin remodelling and epigenetic features of germ cells[J]. Nature, 2005, 434(7033): 583～589.

45 Klaver R, Bleiziffer A, Redmann K, et al. Routine cryopreservation of spermatozoa is safe——Evidence from the DNA methylation pattern of nine spermatozoa genes[J]. J Assist Reprod Genet, 2012, 29(9): 943～950.

46 Kota S K, Feil R. Epigenetic transitions in germ cell development and meiosis[J]. Dev Cell, 2010, 19(5): 675～686.

47 Kuramochi-Miyagawa S, Kimura T, Ijiri T W, et al. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis[J]. Development, 2004, 131(4): 839～849.

48 Lahn B T, Tang Z L, Zhou J, et al. Previously uncharacterized histone acetyltransferases implicated in mammalian spermatogenesis[J]. Proceedings of the National Academy of Sciences, 2002, 99(13): 8707～8712.

49 Marchal R, Chicheportiche A, Dutrillaux B, et al. DNA methylation in mouse gametogenesis[J]. Cytogenetic and Genome Research, 2004, 105(2～4): 316～324.

50 Marques C J, Joao P M, Carvalho F, et al. DNA methylation imprinting marks and DNA methyltransferase expression in human spermatogenic cell stages[J]. Epigenetics, 2011, 6(11): 1354～1361.

51 Marushige Y, Marushige K. Transformation of sperm histone during formation and maturation of rat spermatozoa[J]. Journal of Biological Chemistry, 1975, 250(1): 39～45.

52 Morin Jr P, Dubuc A, Storey K B. Differential expression of microRNA species in organs of hibernating ground squirrels: A role in translational suppression during torpor[J]. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms, 2008, 1779(10): 628～633.

53 Neal K C, Pannuti A, Smith E R, et al. A new human member of the MYST family of histone acetyl transferases with high sequence similarity to Drosophila MOF[J]. Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression, 2000, 1490(1): 170～174.

54 Oakes C, La Salle S, Smiraglia D, et al. Developmental acquisition of genome-wide DNA methylation occurs prior to meiosis in male germ cells[J]. Dev Biol, 2007, 307(2): 368～379.

55 Oakes C C, La Salle S, Smiraglia D J, et al. Developmental acquisition of genome-wide DNA methylation occurs prior to meiosis in male germ cells[J]. Dev Biol, 2007, 307(2): 368～379.

56 Okada Y, Scott G, Ray M K, et al. Histone demethylase JHDM2A is critical for Tnp1 and Prm1 transcription and spermatogenesis[J]. Nature, 2007, 450(7166): 119～123.

57 Okada Y, Tateishi K, Zhang Y. Histone demethylase JHDM2A is involved in male infertility and obesity[J]. J Androl, 2010, 31(1): 75～78.

58 Olek A, Walter J. The pre-implantation ontogeny of the H19 methylation imprint[J]. Nature genetics, 1997, 17(3): 275～276.

59 Pacheco S E, Houseman E A, Christensen B C, et al. Integrative DNA methylation and gene expression analyses identify DNA packaging and epigenetic regulatory genes associated with low motility sperm[J]. PLoS One, 2011, 6(6): e20280.

60 Peters A H, O’Carroll D, Scherthan H, et al. Loss of the suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability[J]. Cell, 2001, 107(3): 323～337.

61 Rajender S, Avery K, Agarwal A. Epigenetics, spermatogenesis and male infertility[J]. Mutation Research/Reviews in Mutation Research, 2011, 727(3): 62～71.

62 Riesco M F, Robles V. Cryopreservation causes genetic and epigenetic changes in zebrafish genital ridges[J]. PLoS One, 2013, 8(6): e67614.

63 Rodriguez-Martinez H, Pena V F. Semen technologies in domestic animal species[J]. Animal Frontiers, 2013, 3(4): 26～33.

64 Rosenbluth E M, Shelton D N, Sparks A E, et al. MicroRNA expression in the human blastocyst[J]. Fertil Steril, 2013, 99(3): 855～861.

65 Rossignol S, Steunou V, Chalas C, et al. The epigenetic imprinting defect of patients with Beckwith-Wiedemann syndrome born after assisted reproductive technology is not restricted to the 11p15 region[J]. J Med Genet, 2006, 43(12): 902～907.

66 Royere D, Hamamah S, Nicolle J, et al. Chromatin alterations induced by freeze-thawing influence the fertilizing ability of human sperm[J]. International Journal of Andrology, 1991, 14(5): 328～332.

67 Sasaki H, Matsui Y. Epigenetic events in mammalian germ-cell development: Reprogramming and beyond[J]. Nat Rev Genet, 2008, 9(2): 129～140.

68 Sassone-Corsi P. Unique chromatin remodeling and transcriptional regulation in spermatogenesis[J]. Science, 2002, 296(5576): 2176～2178.

69 Sauvat F, Capito C, Sarnacki S, et al. Immature cryopreserved ovary restores puberty and fertility in mice without alteration of epigenetic marks[J]. PLoS One, 2008, 3(4): e1972.

70 Seki Y, Yamaji M, Yabuta Y, et al. Cellular dynamics associated with the genome-wide epigenetic reprogramming in migrating primordial germ cells in mice[J]. Development, 2007, 134(14): 2627～2638.

71 Shi Y, Lan F, Matson C, et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1[J]. Cell, 2004, 119(7): 941～953.

72Shi Y, Whetstine J R. Dynamic regulation of histone lysine methylation by demethylases[J]. Mol Cell, 2007, 25(1): 1～14.

73 Shovlin T, Bour?his D, La Salle S, et al. Sex-specific promoters regulate Dnmt3L expression in mouse germ cells[J]. Human Reproduction, 2007, 22(2): 457～467.

74 Soloaga A, Thomson S, Wiggin G R, et al. MSK2 and MSK1 mediate the mitogen- and stress-induced phosphorylation of histone H3 and HMG-14[J]. The EMBO Journal, 2003, 22(11): 2788～2797.

75 Sonnack V, Failing K, Bergmann M, et al. Expression of hyperacetylated histone H4 during normal and impaired human spermatogenesis[J]. Andrologia, 2002, 34(6): 384～390.

76 Spano M, Cordelli E, Leter G, et al. Nuclear chromatin variations in human spermatozoa undergoing swim-up and cryopreservation evaluated by the flow cytometric sperm chromatin structure assay[J]. Mol Hum Reprod, 1999, 5(1): 29～37.

77 Suo L, Meng Q, Pei Y, et al. Effect of cryopreservation on acetylation patterns of lysine 12 of histone H4 (acH4K12) in mouse oocytes and zygotes[J]. J Assist Reprod Genet, 2010, 27(12): 735～741.

78 Thomas T, Loveland K L, Voss A K. The genes coding for the MYST family histone acetyltransferases, Tip60 and Mof, are expressed at high levels during sperm development[J]. Gene Expression Patterns, 2007, 7(6): 657～665.

79 Thomson L K, Fleming S D, Barone K, et al. The effect of repeated freezing and thawing on human sperm DNA fragmentation[J]. Fertil Steril, 2010, 93(4): 1147～1156.

80 Tsukada Y I, Fang J, Erdjument-Bromage H, et al. Histone demethylation by a family of JmjC domain-containing proteins[J]. Nature, 2005, 439(7078): 811～816.

81 Tunc O, Tremellen K. Oxidative DNA damage impairs global sperm DNA methylation in infertile men[J]. J Assist Reprod Genet, 2009, 26(9～10): 537～544.

82 Turek-Plewa J, Jagodzinski P. The role of mammalian DNA methyltransferases in the regulation of gene expression[J]. Cellular and Molecular Biology Letters, 2005, 10(4): 631.

83 Turner J M. Meiotic sex chromosome inactivation[J]. Development, 2007, 134(10): 1823～1831.

84 Warnecke P M, Mann J R, Frommer M, et al. Bisulfite sequencing in preimplantation embryos: DNA methylation profile of the upstream region of the mouse imprinted H19 gene[J]. Genomics, 1998, 51(2): 182～190.

85 Webster K E, O'Bryan M K, Fletcher S, et al. Meiotic and epigenetic defects in Dnmt3L-knockout mouse spermatogenesis[J]. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(11): 4068～4073.

86 Wong E C, Hatakeyama C, Robinson W P, et al. DNA methylation at H19/IGF2 ICR1 in the placenta of pregnancies conceived by in vitro fertilization and intracytoplasmic sperm injection[J]. Fertil Steril, 2011, 95(8): 2524～2526.

87 Yadav R P, Kotaja N. Small RNAs in spermatogenesis[J]. Mol Cell Endocrinol, 2014, 382(1): 498～508.

88 Yan N, Lu Y, Sun H, et al. A microarray for microRNA profiling in mouse testis tissues[J]. Reproduction, 2007, 134(1): 73～79.

89 Yang Y, Hu J F, Ulaner G A, et al. Epigenetic regulation of Igf2/H19 imprinting at CTCF insulator binding sites[J]. Journal of Cellular Biochemistry, 2003, 90(5): 1038～1055.

90 Yin L J, Zhang Y, Lv P P, et al. Insufficient maintenance DNA methylation is associated with abnormal embryonic development[J]. BMC Med, 2012, 10(1): 26.

91 Zamudio N M, Chong S, O’Bryan M K. Epigenetic regulation in male germ cells[J]. Reproduction, 2008, 136(2): 131～146.

92 Zhang R, Peng Y, Wang W, et al. Rapid evolution of an X-linked microRNA cluster in primates[J]. Genome Research, 2007, 17(5): 612～617.

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