Presence of histone H3 acetylated at lysine 9 in male germ cells and its distribution pattern in the genome of human spermatozoa

Reproduction, Fertility and Development

Volumn 23, Issue 8, 2011, Pages 997-1011

  Steilmann, C ^a   Paradowska, A ^a   Bartkuhn, M ^a   Vieweg, M ^a   Schuppe, H C ^a   Bergmann, M ^a   Kliesch, S ^b   Weidner, W ^a   Steger, K ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

epigenetic mark; H3K9ac; human spermatogenesis

Indexed keywords

HISTONE H3; LYSINE; PROTAMINE;

ADULT; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EPIGENETICS; FERTILIZATION; GENE EXPRESSION; GERM CELL; HISTONE ACETYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MALE FERTILITY; MALE INFERTILITY; NUCLEOTIDE SEQUENCE; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; SEMEN ANALYSIS; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; SPERMATOZOON; TESTIS BIOPSY;

ACETYLATION; ADULT; CELLS, CULTURED; CHROMATIN; EPIGENESIS, GENETIC; GENOME; HELA CELLS; HISTONES; HUMANS; LYSINE; MALE; MIDDLE AGED; PROSTATE; SPERMATOGENESIS; SPERMATOZOA;

EID: 80054110847     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD10197     Document Type: Article

References (74)

1. Agalioti, T., Chen, G., and Thanos, D. (2002). Deciphering the transcriptional histone acetylation code for a human gene. Cell 111, 381-392 doi:101016/S0092-8674(02)01077-2 (Pubitemid 35341391)
2. Arpanahi, A., Brinkworth, M., Iles, D., Krawetz, S. A., Paradowska, A., Platts, A. E., Saida, M., Steger, K., Tedder, P., and Miller, D. (2009). Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences. Genome Res. 19, 1338-1349 doi:101101/GR.094953109
3. Banerjee, S., and Smallwood, A. (1998). Chromatin modification of imprinted H19 gene in mammalian spermatozoa. Mol. Reprod. Dev.50, 474-484 doi:101002/(SICI)1098-2795(199808)50:4,474::AIDMRD1130 CO;2-2 (Pubitemid 28294789)
4. Barber, R. D., Harmer, D. W., Coleman, R. A., and Clark, B. J. (2005). GAPDHas a housekeeping gene: analysis of GAPDHmRNAexpression in a panel of 72 human tissues. Physiol. Genomics 21, 389-395 doi:101152/PHYSIOLGENOMICS. 000252005
5. Bergmann, M., and Kliesch, S. (2010). Testicular biopsy and histology. In 'Andrology: Male Reproductive Health and Dysfunction'. 3rd edn. (Eds E. Nieschlag, H. M. Behre and S. Nieschlag.) pp. 155-167 (Springer: Heidelberg.)
6. Bernstein, B. E., Meissner, A., and Lander, E. S. (2007). The mammalian epigenome. Cell 128, 669-681 doi:101016/J.CELL.200701033
7. Bulger, M., Schübeler, D., Bender, M. A., Hamilton, J., Farrell, C. M., Hardison, R. C., and Groudine, M. (2003). A complex chromatin landscape revealed by patterns of nuclease sensitivity and histone modification within the mouse beta-globin-locus. Mol. Cell. Biol. 23, 5234-5244 doi:101128/MCB. 23155234-52442003
8. Burke, L. J., Zhang, R., Bartkuhn, M., Tiwari, V. K., Tavoosidana, G., Kurukuti, S., Weth, C., Galjart, N., Ohlsson, R., and Renkawitz, R. (2005). CTCF binding and higher order chromatin structure of the H19 locus are maintained in mitotic chromatin. EMBO J. 24, 3291-3300 doi:101038/SJ.EMBOJ.7600793
9. Carter, C. W., Jr. (1978). Histone packing in the nucleosome core particle of chromatin. Proc. Natl Acad. Sci. USA 75, 3649-3653 doi:101073/ PNAS.7583649
10. Cheng, H. J., Bagri, A., Yaron, A., Stein, E., Pleasure, S. J., and Tessier- Lavigne, M. (2001). Plexin-A3 mediates semaphorin signalling and regulates the development of hippocampal axonal projections. Neuron 32, 249-263 doi:101016/S0896-6273(01)00478-0 (Pubitemid 33030193)
11. Christensen, M. E., Rattner, J. B., and Dixon, G. H. (1984). Hyperacetlytion of histone H4 promotes chromatin decondensation prior to histone replacement by protamines during spermatogenesis in rainbow trout. Nucleic Acids Res. 12, 4575-4592 doi:101093/NAR/12114575
12. Cooper, T. G., Noonan, E., von Eckardstein, S., Auger, J., Baker, H. W., Behre, H. M., Haugen, T. B., Kruger, T., Wang, C., Mbizvo, M. T., and Vogelsong, K. M. (2010). World Health Organization reference values for human semen characteristics. Hum. Reprod. Update 16, 231-245 doi:101093/HUMUPD/DMP048
13. Cox, G. F., Bürger, J., Lip, V., Mau, U. A., Sperling, K., Wu, B., and Horsthemke, B. (2002). Intracytoplasmic sperm injection may increase the risk of imprinting defects. Am. J. Hum. Genet. 71, 162-164doi:101086/341096 (Pubitemid 34734717)
14. Davie, J. R. (1998). Covalent modifications of histones: expression from chromatin templates. Curr. Opin. Genet. Dev. 8, 173-178 doi:101016/ S0959-437X(98)80138-X (Pubitemid 28206280)
15. De Rycke, M., Liebaers, I., and Van Steirteghem,A. (2002). Epigenetic risks related to assisted reproductive technologies: risk analysis and epigenetic inheritance. Hum. Reprod. 17, 2487-2494 doi:101093/ HUMREP/17102487 (Pubitemid 35174092)
16. DeBaun, M. R., Niemitz, E. L., and Feinberg, A. P. (2003). Association of in vitro fertilization with Beckwith-Wiedemann syndrome and epigenetic alterations of LIT1 and H19 Am. J. Hum. Genet. 72, 56-160 doi:101086/346031
17. Delaval, K., Govin, J., and Cerqueira, F. (2007). Differential histone modifications mark mouse imprinting control regions during spermatogenesis. EMBO J. 26, 720-729 doi:101038/SJ.EMBOJ.7601513
18. Felsenfeld, G., and Groudine, M. (2003). Controlling the double helix. Nature 421, 448-453 doi:101038/NATURE01411
19. Forsberg, E. C., Downs, K. M., Christensen, H. M., Im, H., Nuzzi, P. A., and Bresnick, E. H. (2000). Developmentally dynamic histone acteylation pattern of a tissue-specific chromatin domain. Proc. Natl Acad. Sci. USA 97, 14 494-14 499 doi:101073/PNAS.972614494
20. Frank, S. R., Schroeder, M., Fernandez, P., Taubert, S., and Amati, B. (2001). Binding of c-Myc to chromatin mediates mitogen-induced acetylation of histone H4 and gene activation. Genes Dev. 15, 2069-2082 doi:101101/GAD.906601
21. Gardiner-Garden, M., Ballesteros, M., Gordon, M., and Tam, P. P. (1998). Histone- and protamine-DNA association: conservation of different patterns within the β-globin domain in human sperm. Mol. Cell. Biol. 18, 3350-3356
22. Gatewood, J. M., Cook, G. R., Balhorn, R., Bradbury, E. M., and Schmid, C. W. (1987). Sequence-specific packaging of DNA in human sperm chromatin. Science 236, 962-964 doi:101126/SCIENCE.3576213 (Pubitemid 17107947)
23. Gatewood, J. M., Cook, G. R., Schmid, C. W., and Bradbury, E. M. (1990). Isolation of four core histones from human sperm chromatin representing a minor subset o somatic chromatin. J. Biol. Chem. 265, 20 662- 20 666
24. Grimes, S. R., Jr, and Smart, P. G. (1985). Changes in structural organization of chromatin during spermatogenesis in the rat. Biochim. Biophys. Acta 824, 128-139 (Pubitemid 15139165)
25. Guenther, M. G., Lebine, S. S., Bover, L. A., Jaenisch, R., and Young, R. A. (2007). A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130, 77-88 doi:101016/J.CELL. 200705042 (Pubitemid 47031323)
26. Gurtner, A., Fuschi, P., Magi, F., Colussi, C., Gaetano, C., Dobbelstein, M., Sacchi, A., and Piaggio, G. (2008). NF-Y dependent epigenetic modifications discriminate between proliferating and postmitotic tissue. PLoS One 3, e2047 doi:101371/JOURNAL.PONE.0002047
27. Hammoud, S. S., Nix, D. A., Zhang, H., Purwar, J., Carell, D. T., and Cairns, B. R. (2009). Distinctive chromatin in human sperm packages genes for embryo development. Nature 460, 473-478
28. Hebbes, T. R., Thorne, A. W., and Crane-Robinson, C. (1988). A direct link between core histone acetlytion and transcriptionally active chromatin. EMBO J. 7, 1395-1402
29. Hebbes, T. R., Clayton, A. L., Thorne, A. W., and Crane-Robinson, C. (1994). Core histone hyperacetylation co-maps with generalized DNAse I sensitivity in the chicken β-globin chromosomal domain. EMBO J. 13, 1823-1830 (Pubitemid 24124515)
30. Hecht, N., Behr, R., Hild, A., Bergmann, M., Weidner, W., and Steger, K. (2009). The common marmoset (Callithrix jacchus) as a model for histone and protamine expression during human spermatogenesis. Hum. Reprod. 24, 536-545 doi:101093/HUMREP/DEN390
31. Heidaran, M. A., Showman, R. M., and Kistler, W. S. (1988). A cytochemical study of the transcriptional and translational regulation of nuclear transition protein (TP1), a major chromosomal protein of mammalian spermatids. J. Cell Biol. 106, 1427-1433 doi:101083/JCB.10651427
32. Henkel, R. R., Franken, D. R., Lombard, C. J., and Schill, W. B. (1994). Selective capacity of glass-wool filtration for the separation of human spermatozoa with condensed chromatin: a possible therapeutic modality for male-factor cases? J. Assist. Reprod. Genet. 11, 395-400 doi:101007/BF02211725
33. Hofmann, N., Hilscher, B., Mörchen, B., Schuppe, H. C., and Bielfeld, P. (1995). Comparative studies on various modes of classification of morphology of sperm heads and results in in vitro fertilization: a preliminary report. Andrologia 27, 19-23 doi:101111/J.1439-0272 1995TB02090X
34. Kouzarides, T. (2007). Chromatin modifications and their function. Cell 128, 693-705 doi:101016/J.CELL.200702005
35. Kurdistani, S. K., Tavazoie, S., and Grunstein, M. (2004). Mapping global histone acelylation patterns to gene expression. Cell 117, 721-733 doi:101016/J.CELL.200405023
36. Lescoat, D., Blanchard, Y., Lavault, M. T., Quernée, D., and Le Lannou, D. (1993). Ultrastructural and immunocytochemical study of P1 protamine localization in human testis. Andrologia 25, 93-99 doi:101111/J.1439- 02721993TB02689X (Pubitemid 23073991)
37. Li, J., Liu, F., Wang, H., Liu, X., Liu, J., Li, N., Wan, F., Wang, W., Zhang, C., Jin, S., Liu, J., Zhu, P., and Liu, Y. (2010). Systematic mapping and functional analysis of a family of human epididymal secretory sperm-located proteins. Mol. Cell. Proteomics 9, 2517-2528 doi:101074/MCP.M110001719
38. Liu, C.L.,Kaplan,T.,Kim,M., Buratowski, S., Schreiber, S. L., Friedman,N., and Rando, O. J. (2005). Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol. 3, e328 doi:101371/JOURNAL. PBIO.0030328
39. Maestrini, E., Tamagnone, L., Longati, P., Cremona, O., Gulisano, M., Bione, S., Tamanini, F., Neel, B. G., Toniolo, D., and Comoglio, P. M. (1996). A family of transmembrane proteins with homology to the MET-hepatocyte growth factor receptor. Proc. Natl Acad. Sci. USA 93, 674-678 doi:101073/PNAS.932674
40. Menkveld, R., Stander, F. S., Kotze, T. J., Kruger, T. F., and van Zyl, J. A. (1990). The evaluation of morphological characteristic of human spermatozoa according to stricter criteria. Hum. Reprod. 5, 586-592
41. Merighe, G. K., Biase, F. H., Santos-Biase, W. K., Miranda, M. S., de Bem, T. H., Watanable, Y. F., and Meirelles, F. V. (2009). Gene silencing during development of in vitro-produced female bovine embryos. Genet. Mol. Res. 8, 1116-1127 doi:104238/VOL8-3GMR638
42. Morton Bradbury, E. (1992). Reversible histone modifications and the chromosome cell cycle. Bioessays 14(1), 9-16 doi:101002/BIES. 950140103
43. Morton, K. M., Herrmann, D., Sieg, B., Struckmann, C., Maxwell, W. M., Rath, D., Evans, G., Lucas-Hahn, A., Niemann, H., and Wrenzycki, C. (2007). Altered mRNA expression patterns in bovine blastocysts after fertilisation in vitro using flow-cytometrically sex-sorted sperm. Mol. Reprod. Dev. 74, 931-940 doi:101002/MRD.20573
44. Nahkuri, S., Taft, R. J., and Mattick, J. S. (2009). Nucleosomes are preferentially positioned at exon in somatic and sperm cells. Cell Cycle 8, 3420-3424 doi:104161/CC.8209916
45. Nallella, K. P., Sharma, R. K., Aziz, N., and Agarwal, A. (2006). Significance of sperm characteristics in the evaluation of male infertility. Fertil. Steril. 85, 629-634 doi:101016/J.FERTNSTERT.200508024
46. Nishida, H.,Kondo, S., Suzuki, T., Tsujimura,Y., Komatsu, S.,Wakayama, T., and Nayashizhaki, Y. (2008). An epigenetic aberration increased in intergenic regions of cloned mice. Mamm. Genome 19, 667-674 doi:101007/S00335- 008-9146-5
47. Onyango, P., Jiang, S., Uejima, H., Shamblott, M. J., Gearhart, J. D., Cui, H., and Feinberg, A. P. (2002). Monoallelic expression and methylation of imprinted genes in human and mouse embryonic germ cell lineages. Proc. Natl Acad. Sci. USA 99, 10 599-10 604 doi:101073/PNAS. 152327599
48. Ostermeier, G. C., Miller, D., Huntriss, J. D., Diamond, M. P., and Krawetz, S. A. (2004). Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature 429, 154 doi:101038/429154A
49. Pantke, P., Diemer, T., Marconi, M., Bergmann, M., Steger, K., Schuppe, H. C., and Weidner, W. (2008). Testicular sperm retrieval in azoospermic men. Eur. Urol. Suppl. 7, 703-714 doi:101016/J.EURSUP.2008 07006
50. Paradowska, A., Fenic, I., Konrad, L., Sturm, K., Wagenlehner, F., Weidner, W., and Steger, K. (2009).Aberrant epigenetic modifications in the CTCF binding domain of the IGF/H19 gene in prostate cancer compared with benign prostate hyperplasia. Int. J. Oncol. 35, 87-96 doi:103892/IJO-00000316
51. Perl, A. (2007). The pathogenesis of transaldolase deficiency. IUBMB Life 59, 365-373 doi:101080/15216540701387188
52. Prigent, Y., Muller, S., and Dadoune, J. P. (1996). Immunoelectron microscopial distribution of histones H2B and H3 and protamines during human spermatogenesis. Mol. Hum. Reprod. 2, 929-935 doi:101093/ MOLEHR/212929 (Pubitemid 126715953)
53. Regha, K., Sloane, M. A., Huang, R., Pauler, F. M., Warczok, K. E., Melikant, B., Radolf, M., Martens, J. H., Schotta, G., Jenuwein, T., and Barlow, D. P. (2007). Active and repressive chromatin are interspersed without spreading in an imprinted gene cluster in mammalian genome. Mol. Cell 27, 353-366 doi:101016/J.MOLCEL.200706024
54. Roh, T. Y., Cuddapah, S., Cui, K., and Zhao, K. (2006). The genomic landscape of histone modifications in human T cells. Proc. Natl Acad. Sci. USA 103, 15 782-15 787 doi:101073/PNAS.0607617103
55. Rousseaux, S., Reynoird, N., Escoffier, E., Thevenon, J., Caron, C., and Khochbin, S. (2008). Epigenetic reprogramming of the male genome during gametogenesis and in the zygote. Reprod. Biomed. Online 16, 492-503 doi:101016/S1472-6483(10)60456-7 (Pubitemid 351566164)
56. Roux, C., Gusse, M., Chevaillier, P., and Dadoune, J. P. (1988). An antiserum against protamines for immunohistochemical studies of histone to protamine transition during human spermatogenesis. J. Reprod. Fertil. 82, 35-42 doi:101530/JRF.00820035
57. Santos, F., Peters, A. H., Otte, A. P., Reik, W., and Dean, W. (2005). Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev. Biol. 280, 225-236 doi:101016/J.YDBIO.2005 01025 (Pubitemid 40342755)
58. Sarkar, S., Nelson, A. J., and Jones, O. W. (1977). Glucose-6-phosphate dehydrogenase (G6PD) activity of human sperm. J. Med. Genet. 14, 250-255 doi:101136/JMG.144250 (Pubitemid 8175889)
59. Sha, J., Zhou, Z., Li, J., Yin, L., Yang, H., Hu, G., Luo, M., Chan, H. C., and Zhou, K. (2002). Identification of testis development and spermatogenesis related genes in human and mouse testes using cDNA arrays. Mol. Hum. Reprod. 8, 511-517 doi:101093/MOLEHR/86511 (Pubitemid 34746283)
60. Shahbazian, M. D., and Grunstein, M. (2007). Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 76, 75-100doi:101146/ANNUREV.BIOCHEM.76052705162114
61. Shi, Y. Q., Wang, Q. Z., Liao, S. Y., Zhang, Y., Liu, Y. X., and Han, C. S. (2006). In vitro propagation of spermatogonial stem cells fromKMmice. Front. Biosci. 11, 2614-2622 doi:102741/1995 (Pubitemid 43806568)
62. Simon, R. H., Camerini-Otero, R. D., and Felsenfeld, G. (1978). An octamer of histones H3 and H4 forms a compact complex with DNA of nucleosome size. Nucleic Acids Res. 5, 4805-4818 doi:101093/NAR/ 5124805 (Pubitemid 9075914)
63. Simpson, R. T., and Bustin, M. (1976). Histone composition of chromatin subunits studied by immunosedimentation. Biochemistry 15, 4305-4312 doi:101021/BI00664A026
64. Sonnack, V., Failing, K., Bergmann, M., and Steger, K. (2002). Expression of hyperacetylated histone H4 during normal and impaired spermatogenesis. Andrologia 34, 384-390 doi:101046/J.1439-02722002 00524X (Pubitemid 35463785)
65. Steger, K. (1999). Transcriptional and translational regulation of gene expression in haploid spermatids. Anat. Embryol. 199, 471-487 doi:101007/S004290050245
66. Steger, K., Klonisch, T., Gavenis, K., Drabent, B., Doenecke, D., and Bergmann, M. (1998a). Expression of mRNA and protein of nucleoproteins during human spermatogenesis. Mol. Hum. Reprod. 4, 939-945 doi:101093/MOLEHR/410939 (Pubitemid 28475248)
67. Steger, K., Aleithe, I., Behre, H., and Bergmann,M. (1998b). The proliferation of spermatogonia in normal and pathological human seminiferous epithelium: an immunohistochemical study using monoclonal antibodies against Ki-67 protein and proliferating cell nuclear antigen. Mol. Hum. Reprod. 4, 227-233 doi:101093/MOLEHR/43227 (Pubitemid 28172588)
68. Steger, K., Pauls, K., Klonisch, T., Franke, F. E., and Bergmann, M. (2000). Expression of protamine-1 and 2 mRNA during human spermiogenesis. Mol. Hum. Reprod. 6, 219-225 doi:101093/MOLEHR/63219
69. Tanphaichitr, N., Sobhon, P., Taluppeth, N., and Chalermisarachai, P. (1978). Basic nuclear proteins in testicular cells and ejaculated spermatozoa in man. Exp. Cell Res. 117, 347-356 doi:101016/0014-4827(78) 90148-9 (Pubitemid 9076532)
70. Waimey, K. E., Huang, P. H., Chen, M., and Cheng, H. J. (2008). Plexin-A3 and plexin-A4 restrict the migration of the sympathetic neurons but not their neural crest precursors. Dev. Biol. 315, 448-458 doi:101016/ J.YDBIO.200801002
71. Wang, Z., Zang,C., Rosenfeld, J.A., Schones,D. E., Barski,A., Cuddapah, S., Cui, K., Roh, T. Y., Peng, W., Zhang, M. Q., and Zhao, K. (2008). Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 40, 897-903 doi:101038/NG.154
72. World Health Organization (1999). 'WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction.' 4th edn. (Cambrigde University Press: Cambridge.)
73. Wykes, S. M., and Krawetz, S. A. (2003). The structural organization of sperm chromatin. J. Biol. Chem. 278, 29 471-29 477 doi:101074/JBC. M304545200
74. Zhou, Q. Y., Quaife, C. J., and Palmiter, R. D. (1995). Targeted disruption of the tyrosine hydroxylase gene reveals that catecholamines are required for mouse fetal development. Nature 374, 640-643 doi:101038/ 374640A0