The common marmoset (Callithrix jacchus) as a model for histone and protamine expression during human spermatogenesis

Human Reproduction

Volumn 24, Issue 3, 2009, Pages 536-545

  Hecht, Nadine ^a   Behr, Rüdiger ^b   Hild, Anne ^c   Bergmann, Martin ^c   Weidner, Wolfgang ^a   Steger, Klaus ^a,d  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b GERMAN PRIMATE CENTER   (Germany)

^c Institute of Veterinary Anatomy Histology and Embryology   (Germany)

^d UNIVERSITY HOSPITAL GIESSEN   (Germany)

Author keywords

Histone; Human; Marmoset; Protamine; Spermatogenesis

Indexed keywords

ANTIBODY; HISTONE H4; LYSINE; MESSENGER RNA; PROTAMINE; PROTAMINE P1; PROTAMINE P2; UNCLASSIFIED DRUG;

ADULT; AGED; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MARMOSET; NONHUMAN; PACHYTENE; PROTEIN EXPRESSION; SEMINIFEROUS TUBULE EPITHELIUM; SPERM; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; TESTIS;

ANIMALIA; CALLITHRIX JACCHUS; MARMOSETS;

EID: 61449125023     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/den390     Document Type: Article

References (61)

1. Balhorn R, Reed S, Tanphaichitr N. Aberrant protamine 2 ratios in sperm of infertile human males. Experientia 1988;44:52-55.
2. Behr R, Weinbauer GF. Germ cell-specific cyclic adenosine 3′,5′-monophosphate response element modulator expression in the rodent and primate testis is maintained despite gonadotropin deficiency. Endocrinology 1999;140:2746-2754.
3. Bench GS, Friz AM, Corzett MH, Morse DH, Balhorn R. DNA and total protamine masses in individual sperm from fertile semen of selected mammals. Cytometry 1996;23:263-271.
4. Bradbury EM. Reversible histone modifications and the chromosome cell cycle. Bioessays 1992;14:9-16.
5. Brand HM. Influence of season on birth distribution in marmoset and tamarins. Lab Anim 1980;14:301-302.
6. Chandolia RK, Luetjens CM, Wistuba J, Yeung CH, Nieschlag E, Simoni M. Changes in endocrine profile and reproductive organs during puberty in the male marmoset monkey (Callithrix jacchus). Reproduction 2006;132:355- 363.
7. Christensen ME, Dixon GH. Hyperacetylation of histone H4 correlates with the terminal, transcriptionally inactive stages of spermatogenesis in rainbow trout. Dev Biol 1982;93:404-415.
8. Christensen ME, Rattner JB, Dixon GH. Hyperacetylation of histone H4 promotes chromatin decondensation prior to histone replacement by protamines during spermatogenesis in rainbow trout. Nucleic Acids Res 1984;12:4575-4592.
9. Clermont Y. The cycle of the seminiferous epithelium in man. Am J Anat 1963;112:35-46.
10. Corzett M, Mazrimas J, Balhorn R. Protamine 1: Protamine 2 stoichiometry in the sperm of eutherian mammals. Mol Reprod Dev 2002;61:519-527.
11. Cui KH, Flaherty SP, Newble CD, Guerin MV, Napier AJ, Matthews CD. Collection and analysis of semen from the common marmoset (Callithrix jacchus). J Androl 1991;12:214-220.
12. Davie JR. Covalent modifications of histones: expression from chromatin templates. Curr Opin Genet Dev 1998;8:173-178.
13. Depa-Martynów M, Kempisty B, Lianeri M, Jagodziński PP, Jedrzejczak P. Association between fertilin β, protamines 1 and 2 and spermatid-specific linker histone H1-like protein mRNA levels, fertilization ability of human spermatozoa, and quality of preimplantation embryos. Folia Histochem Cytobiol 2007;45:79-85.
14. Einspanier A, Ivell R, Rune G, Hodges J. Oxytocin gene expression and oxytocin immunoactivity in the ovary of the common marmoset monkey (Callithrix jacchus). Biol Reprod 1994;50:1216-1222.
15. Gatewood JM, Cook GR, Balhorn R, Bradbury EM, Schmid CW. Sequence-specific packaging of DNA in human sperm chromatin. Science 1987;236:962-964.
16. Gatewood JM, Cook GR, Balhorn R, Schmid CW, Bradbury EM. Isolation of four core histones from human sperm chromatin representing a minor subset of somatic histones. J Biol Chem 1990;25:20662-20666.
17. Gilchrist RB, Nayudu PL, Hodges JK. Maturation, fertilization, and development of marmoset monkey oocytes in vitro. Biol Reprod 1997;56:238-246.
18. Grimes SR, Henderson N. Hyperacetylation of histone H4 in rat testis spermatids. Exp Cell Res 1984a;152:91-97.
19. Grimes SR, Henderson N. Acetylation of rat testis histones H2B and TH2B. Dev Biol 1984b;101:516-521.
20. Grunewald S, Paasch U, Glander HJ, Anderegg U. Mature human spermatozoa do not transcribe novel RNA. Andrologia 2005;37:69-71.
21. Hammoud S, Emery BR, Aoki VW, Carrell DT. Identification of genetic variation in the 5′ and 3′ non-coding regions of the protamine genes in patients with protamine deregulation. Arch Androl 2007;53:267-274.
22. Hayashi S, Yang J, Christenson L, Yanagimachi R, Hecht NB. Mouse preimplantation embryos developed from oocytes injected with round spermatids or spermatozoa have similar but distinct patterns of early messenger RNA expression. Biol Reprod 2003;69:1170-1176.
23. Holt WV, Moore HD. Ultrastructural aspects of spermatogenesis in the common marmoset (Callithrix jacchus). J Anat 1984;138:175-188.
24. Imhof A, Wolffe AP. Transcription: gene control by targeted histone acetylation. Curr Biol 1998;8:R422-R424.
25. Isachenko EF, Nayudu PL, Isachenko VV, Nawroth F, Michelmann HW. Congenitally caused fused labia in the common marmoset (Callithrix jacchus). J. Med Primatol 2002;31:350-355.
26. Jenuwein T, Allis CD. Translating the histone code. Science 2001;293:1074-1080.
27. Johnson L, Mckenzie KS, Snell JR. Partial wave in human seminiferous tubules appears to be a random occurrence. Tissue Cell 1996;28:127-136.
28. Kempisty B, Antosik P, Bukowska D, Jackowska M, Lianeri M, Jaśkowski JM, Jagodziński PP. Analysis of selected transcript levels in porcine spermatozoa, oocytes, zygotes and two-cell stage embryos. Reprod Fert Dev 2008;20:513-518.
29. Kholkute SD. Diurnal and annual variations in plasma androgen levels in the adult male marmoset (Callithrix jacchus). Int J Androl 1984;7:431-438.
30. Kholkute SD, Jayaraman S, Kumar RA, Puri CP. Continuous light environment has no effect on the circadian testosterone rhythm, spermatogenesis or fertility of the marmoset (Callithrix jacchus). Int J Androl 1987;10:635-642.
31. Kuederling I, Schneiders A, Sonksen J, Nayudu PL, Hodges JK. Non-invasive collection of ejaculates from the common marmoset (Callithrix jacchus) using penile vibrostimulation. Am J Primatol 2000;52:149-154.
32. Kuo MH, Allis CD. Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays 1998;20:615-626.
33. Lewis FA, Wells M. Detection of virus in infected human tissue by in-situ hybridization. In: Wilkinson DG (ed). In-situ Hybridization, A Practical Approach. Oxford University Press, 1992, 121-135.
34. Li LH, Donald JM, Golub MS. Review on testicular development, structure, function, and regulation in common marmoset. Birth Defects Research B Dev Reprod Toxicol 2005;74:450-469.
35. Meistrich ML, Trostle-Weige PK, Lin R, Bhatnagar YM, Allis CD. Highly acetylated H4 is associated with histone displacement in rat spermatids. Mol Reprod Dev 1992;31:170-181.
36. Millar MR, Sharpe RM, Weinbauer GF, Fraser HM, Saunders PTK. Marmoset spermatogenesis: organizational similarities to the human. Int J Androl 2000;23:266-277.
37. Oliva R, Mezquita C. Histone H4 hyperacetylation and rapid turnover of its acetyl groups in transcriptionally inactive rooster testis spermatids. Nucleic Acids Res 1982;10:8049-8059.
38. Ostermeier GC, Dix DJ, Miller D, Khatri P, Krawetz SA. Spermatozoal RNA profiles of normal fertile men. Lancet 2002;360:772-777.
39. Ostermeier GC, Miller D, Huntriss JD, Diamond MP, Krawetz SA. Delivering spermatozoan RNA to the oocytes. Nature 2004;429:154.
40. Paterson M, Koothan P, Morris K, O'Byrne K, Braude P, Williams A, Aitken RJ. Analysis of the contraceptive potential of antibodies against native and deglycosylated porcine ZP3 in vivo and in vitro. Biol Reprod 1992;46:523-534.
41. Saunders PTK, Summers PM, Hearn J. Partial purification and characterization of chorionic gonadotrophin in plasma and in culture medium of trophoblast cells from the marmoset monkey (Callitrix jacchus). J Reprod Fertil 1987;80:463-472.
42. Saunders PTK, Gaughan J, Saxty BA, Kerr LE, Millar MR. Expression of protamine P2 in the testis of the common marmoset and man visualized using non-radioactive in-situ hybridization. Int J Androl 1996;19:212-219.
43. Schneiders A, Sonksen J, Hodges JK. Penile vibratory stimulation in the marmoset monkey: a practical alternative to electro-ejaculation, yielding ejaculates of enhanced quality. J Med Primatol 2004;33:98-104.
44. Sonnack V, Failing K, Bergmann M, Steger K. Expression of hyperacetylated histone H4 during normal and impaired human spermatogenesis. Andrologia 2002;34:1-7.
45. Steger K. Transcriptional and translational regulation of gene expression in haploid spermatids. Anat Embryol 1999;199:471-487.
46. Steger K, Klonisch T, Gavenis K, Drabent B, Doenecke D, Bergmann M. Expression of mRNA and protein of nucleoproteins during human spermiogenesis. Mol Hum Reprod 1998;4:939-945.
47. Steger K, Pauls K, Klonisch T, Franke FE, Bergmann M. Expression of protamine-1 and -2 mRNA during human spermiogenesis. Mol Hum Reprod 2000;6:219-225.
48. Steger K, Failing K, Klonisch T, Behre HM, Manning M, Weidner W, Hertle L, Bergmann M, Kliesch S. Round spermatids from infertile men exhibit decreased protamine-1 and -2 mRNA. Hum Reprod 2001;16:709-716.
49. Steger K, Fink L, Klonisch T, Bohle RM, Bergmann M. Protamine-1 and-2 mRNA in round spermatids is associated with RNA-binding proteins. Histochem Cell Biol 2002;117:227-234.
50. Steger K, Fink L, Failing K, Bohle RM, Kliesch S, Weidner W, Bergmann M. Decreased protamine-1 transcript levels in testes from infertile men. Mol Hum Reprod 2003;9:331-336.
51. Steger K, Wilhelm J, Konrad L, Stalf T, Greb R, Diemer T, Kliesch S, Bergmann M, Weidner W. Both protamine-1 to protamine-2 mRNA ratio and Bcl2 mRNA content in testicular spermatids and ejaculated spermatozoa discriminate between fertile and infertile men. Hum Reprod 2008;23:11-16.
52. Tanphaichitr N, Sohbon P, Taluppeth N, Chalermisarachai P. Basic nuclear proteins in testicular cells and ejaculated spermatozoa in man. Exp Cell Res 1978;117:347-350.
53. Tardif S, Jaquisch C. The common marmoset as a model for nutritional impacts upon reproduction. Ann NY Acad Sci 1994;709:214-215.
54. Turner BM. Histone acetylation and control of gene expression. J Cell Sci 1991;99:13-20.
55. Van der Heijden GW, Derijck AA, Ramos L, Giele M, van der Vlag J, de Boer P. Transmission of modified nucleosomes from the mouse male germline to the zygote and subsequent remodeling of paternal chromatin. Dev Biol 2006;298:458-469.
56. Wade PA, Pruss D, Wolffe AP. Histone acetylation: chromatin in action. Trends Biochem Sci 1997;22:128-132.
57. Weinbauer GF, Aslam H, Krishnamurthy H, Brinkworth MH, Einspanier A, Hodges JK. Quantitative analysis of spermatogenesis and apoptosis in the common marmoset (Callithrix jacchus) reveals high rates of spermatogonial turnover and high spermatogenic efficiency. Biol Reprod 2001;64:120-126.
58. Wistuba J, Schrod A, Greve B, Hodges JK, Aslam H, Weinbauer GF, Luetjens CM. Organization of seminiferous epithelium in primates: relationship to spermatogenic efficiency, phylogeny, and mating system. Biol Reprod 2003;69:582-591.
59. Wilton L, Marshall V, Piercy E, Moore H. In vitro fertilization and embryo development in the marmoset monkey (Callithrix jacchus). J Reprod Fertil 1993;97:481-486.
60. Wolf KW, Jeppesen P, Mitchell A. Spermatid nucleus of Megaselia scalaris Loew (Insecta, Diptera, Phoridae): a study using anti-histone antibodies, scanning electron microscopy, and a centromere-specific oligonucleotide. Mol Reprod Dev 1993;35:272-276.
61. Workman JL, Kingston RE. Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu Rev Biochem 1998;67:545-579.