Changes in distribution of basic nuclear proteins and chromatin organization during spermiogenesis in the greater bandicoot rat, Bandicota indica

Cell and Tissue Research

Volumn 334, Issue 1, 2008, Pages 135-144

  Worawittayawong, Pakawadee ^a,b   Leigh, Chris ^b   Weerachatyanukul, Wattana ^a   Manochantr, Sirikul ^c   Sobhon, Prasert ^a   Breed, William G ^b   Sretarugsa, Prapee ^a  

^a Mahidol University   (Thailand)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c THAMMASAT UNIVERSITY   (Thailand)

Author keywords

Bandicota indica (Rodentia); Chromatin organization; Immunocytochemistry; Sperm basic nuclear proteins; Spermiogenesis

Indexed keywords

HISTONE ANTIBODY; HISTONE H2A; HISTONE H2B; HISTONE H3; HISTONE H4; NUCLEAR PROTEIN; PROTAMINE; TRITON X 100;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ULTRASTRUCTURE; CHROMATIN; CONTROLLED STUDY; EPIDIDYMIS TAIL; GEL ELECTROPHORESIS; GOLGI COMPLEX; IMMUNOCYTOCHEMISTRY; IMMUNOGOLD LABELING; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SPERMATID; SPERMATOGENESIS; SPERMATOZOON;

ANIMALS; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, IMMUNOELECTRON; MURINAE; NUCLEAR PROTEINS; PROTAMINES; RATS; SPERMATIDS; SPERMATOCYTES; SPERMATOGENESIS;

BANDICOTA INDICA; RATTUS; RODENTIA;

EID: 51749116696     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-008-0668-7     Document Type: Article

References (46)

1. K Akama H Sato M Furihata-Yamauchi Y Komatsu T Tobita M Nakano 1996 Interaction of nucleosome core DNA with transition proteins 1 and 3 from boar late spermatid nuclei J Biochem (Tokyo) 119 448 455
2. PJ Alfonso WS Kistler 1993 Immunohistochemical localisation of spermatid nuclear transition protein 2 in the testes of rats and mice Biol Rep 48 522 539
3. MJ Allen XF Dong TE O'Neill P Yau SC Kowalczykowski J Gatewood R Balhorn EM Bradbury 1993 Atomic force microscope measurement of nucleosome cores assembled along defined DNA sequences Biochemistry 32 8390 8396
4. R Balhorn 1982 A model for the structure of chromatin in mammalian sperm J Cell Biol 93 298 305
5. Balhorn R (1989) Mammalian protamines: structure and molecular interactions. In: Adolph, KW (eds) Molecular biology of chromosome function. Springer, New York, pp 366-395
6. R Balhorn S Weston C Thomas AJ Wyrobek 1984 DNA packaging in mouse spermatids. Synthesis of protamine variants and four transition proteins Exp Cell Res 150 298 308
7. Balhorn R, Cosman M, Thornton K, Krishnan VV, Corzett M, Bench G, Kramer C, Lee JD, Hud NV, Allen MJ, Prieto M, Meyer-Iese W, Brown JT, Kirz J, Zhang X, Bradbury EM, Maki G, Braun RE, Breed W (1999) Protamine mediated condensation of DNA in mammalian sperm. In: Gagnon, C (eds) The male gamete: from basic science to clinical applications. Cache River, Vienna, pp 55-70
8. M Biggiogera S Muller JL Courtens S Fakan MG Romanini 1992 Immunoelectron microscopical distribution of histones H2B and H3 and protamines in the course of mouse spermiogenesis Microsc Res Tech 20 259 267
9. MWH Bishop CR Austin 1960 Mammalian spermatozoa Endeavour 16 137 150
10. WG Breed 1993 Novel organization of the spermatozoon in two species of murid rodents from southern Asia J Reprod Fertil 99 149 158
11. WG Breed 1998 Interspecific variation in structural organisation of the spermatozoon in the Asian Bandicoot rats, Bandicota species (family Muridae) Acta Zool 79 277 285
12. WG Breed 2004 The spermatozoon of Eurasian murine rodents: its morphological diversity and evolution J Morphol 261 52 69
13. L Brewer M Corzett R Balhorn 2002 Condensation of DNA by spermatid basic nuclear proteins J Biol Chem 277 38895 38900
14. N Caron S Veilleux G Boissonneault 2001 Stimulation of DNA repair by the spermatidal TP1 protein Mol Reprod Dev 58 437 443
15. D Churikov IA Zalenskaya AO Zelensky 2004 Male germline-specific histones in mouse and man Cytogenet Genome Res 105 203 214
16. M Corzett J Mazrimas R Balhorn 2002 Protamine 1:protamine 2 stoichiometry in the sperm of eutherian mammals Mol Reprod Dev 61 519 527
17. JL Courtens M Loir 1981 A cytochemical study of nuclear changes in boar, bull, goat, mouse, rat, and stallion spermatids J Ultrastruct Res 74 327 340
18. JL Courtens M Biggiogera S Fakan 1991 A cytochemical and immunocytochemical study of DNA distribution in spermatid nuclei of mouse, rabbit, and bull Cell Tissue Res 265 517 525
19. GB Dooher D Bennett 1973 Fine structural observations on the development of the sperm head in the mouse Am J Anat 136 339 361
20. GF Friend 1936 The sperms of British muridae Q J Microsc Sci 78 419 443
21. JM Gatewood GR Cook R Balhorn CW Schmid EM Bradbury 1990 Isolation of 4 core histones from human sperm chromatin represents a minor set of somatic histones J Biol Chem 265 20662 20666
22. SR Grimes ML Meistrich RD Platz LS Hnilica 1977 Nuclear protein transitions in rat testis spermatids Exp Cell Res 110 31 39
23. S Kimmins P Sassone-Corsi 2005 Chroamatin remodeling and epigenetic features of germ cells Nature 434 583 589
24. M Lalli Y Clermont 1981 Structural changes of the head components of the rat spermatid during spermiogenesis Am J Anat 160 419 434
25. M Loir JL Courtens 1979 Nuclear reorganization in ram spermatids J Ultrastruct Res 67 309 324
26. S Manochantr P Sretarugsa J Chavadej P Sobhon 2005 Chromatin organization and basic nuclear proteins in the male germ cells of Rana tigerina Mol Reprod Dev 70 184 197
27. Meistrich ML (1989) Histone and basic nuclear protein transitions in mammalian spermatogenesis. In: Hnilica LS, Stein GS, Stein JL (eds) Histones and other basic nuclear proteins. CRC Press, Orlando, pp 165-182
28. ML Meistrich B Mohapatra CR Shirley M Zhao 2003 Roles of transition nuclear proteins in spermiogenesis Chromosoma 111 483 488
29. RJ Oko V Jando CL Wagner WS Kistler LS Hermo 1996 Chromatin reorganization in rat spermatids during the disappearance of testis-specific histone, H1t, and the appearance of transition proteins TP1 and TP2 Biol Reprod 54 1141 1157
30. R Oliva GH Dixon 1991 Vertebrate protamine genes and the histone-to-protamine replacement reaction Prog Nucleic Acid Res Mol Biol 40 25 94
31. C Pittoggi L Renzi G Zaccagnini F Cimini F Degrassi R Giordano AR Magnano R Lorenzini P Lavia C Spadafora 1999 A fraction of mouse sperm chromatin is organized in nucleosomal hypersensitive domains enriched in retroposon DNA J Cell Sci 112 3537 3548
32. RD Platz SR Grimes ML Meistrich LS Hnilica 1975 Changes in nuclear proteins of rat testis cells separated by velocity sedimentation J Biol Chem 250 5791 5800
33. L Ploen J-L Courtens 1986 Comparative aspects of mammalian spermiogenesis Scanning Electron Microsc 11 639 652
34. Pradeepa MM, Rao MRS (2007) Chromatin remodeling during mammalian spermatogenesis: role of testis specific histone variants and transition proteins. In: Gupta SK, Koyoma K, Murray JF (eds) Gamete biology: emerging frontiers on fertility and contraceptive development. Nottingham University Press, Nottingham
35. R Queralt R Adroer R Oliva RJ Winkfein JD Retief GH Dixon 1995 Evolution of protamine P1 genes in mammals J Mol Evol 40 601 607
36. G Retzius 1909 Spermien der Nagetiere Biol Untersuch N F 14 133 162
37. J Singh MR Rao 1988 Interaction of rat testis protein, TP, with nucleosome core particle Biochem Int 17 701 710
38. P Sobhon C Chutatape P Chalermisarachai P Vongpayabal N Tanphaichitr 1982 Transmission and scanning electron microscopic studies of the human sperm chromatin decondensed by micrococcal nuclease and salt J Exp Zool 221 61 79
39. C Wanichanon W Weerachatyanukul W Suphamungmee A Meepool S Apisawetakan V Linthong P Sretarugsa J Chavadej P Sobhon 2001 Chromatin condensation during spermiogenesis in rats Sci Asia 27 211 220
40. P Worawittayawong CM Leigh G Cozens EJ Peirce BP Setchell P Sretarugsa A Dharmarajan WG Breed 2005 Unusual germ cell organization in the seminiferous epithelium of a murid rodent from southern Asia, the greater bandicoot rat, Bandicota indica Int J Androl 28 180 188
41. D Wouters-Tyrou A Martinage P Chevaillier P Sautiere 1998 Nuclear basic proteins in spermiogenesis Biochimie 80 117 128
42. SM Wykes SA Krawetz 2003 The structural organization of sperm chromatin J Biol Chem 278 29471 29477
43. YE Yu Y Zhang E Unni CR Shirey JM Deng LD Russell MM Weil RR Behringer ML Meistrich 2000 Abnormal spermatogenesis and reduced fertility in transition nuclear protein 1-deficient mice Proc Natl Acad Sci USA 97 4683 4688
44. M Zhao CR Shirley YE Yu B Mohapatra Y Zhang E Unni JM Deng NA Arango NHA Terry MM Weil LD Russel RR Behringer ML Meistrich 2001 Targeted disruption of the transition protein 2 gene affects sperm chromatin structure and reduces fertility in mice Mol Cell Biol 21 7243 7255
45. M Zhao CR Shirley S Mounsey ML Meistrich 2004 Nucleoprotein transitions during spermiogenesis in mice with transition nuclear protein Tnp1 and TNP 2 mutations Biol Rep 71 1016 1025
46. A Zweidler 1978 Resolution of histones by polyacrylamide gel electrophoresis in presence of nonionic detergents Methods Cell Biol 17 223 233