Spermiogenic nuclear protein transitions and chromatin condensation. proposal for an ancestral model of nuclear spermiogenesis

Journal of Experimental Zoology Part B: Molecular and Developmental Evolution

Volumn 312, Issue 3, 2009, Pages 149-163

  Kurtz, Kathryn ^a   Saperas, Núria ^b   Ausió, Juan ^c   Chiva, Manel ^a  

^a Faculty of Medicine and Health Sciences   (Spain)

^b UNIVERSITAT POLITÈCNICA DE CATALUNYA   (Spain)

^c UNIVERSITY OF VICTORIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; NUCLEAR PROTEIN;

ANIMAL; ARTICLE; BASS; CELL NUCLEUS; CHROMATIN; MALE; METABOLISM; MOLLUSC; PHYSIOLOGY; SEA BREAM; SEQUENCE ANALYSIS; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; ULTRASTRUCTURE;

ANIMALS; BASS; CELL NUCLEUS; CHROMATIN; HISTONES; MALE; MOLLUSCA; NUCLEAR PROTEINS; SEA BREAM; SEQUENCE ANALYSIS, PROTEIN; SPERMATIDS; SPERMATOCYTES; SPERMATOGENESIS;

ANIMALIA; DICENTRARCHUS LABRAX; MONODONTA TURBINATA;

EID: 67049119072     PISSN: 15525007     EISSN: 15525015     Source Type: Journal    
DOI: 10.1002/jez.b.21271     Document Type: Article

References (56)

1. Ausió J. 1988. An unusual cysteine-containing histone Hl-like protein and two protamine-like proteins are the major nuclear proteins of the sperm of the bivalve mollusc Macoma nasuta. J Biol Chem 263:10140-10150.
2. Ausió J. 1992. Presence of a highly specific histone H1-like protein in the chromatin of the sperm of the bivalve molluscs. Mol Cell Biochem 115:163-172.
3. Ausió J. 1995. Histone H1 and the evolution of the nuclear sperm specific proteins. In: Jamieson BGM, Ausió J, Justine JL, editors. Advances in spermatozoal taxonomy and phylogeny. Paris: Mémoires du Muséum National d'Histoire Naturelle. p 447-462.
4. Ausió J. 1999. Histone H1 and evolution of sperm nuclear basic proteins. J Biol Chem 274:31115-31118.
5. Ausió J, Subirana JA. 1982. Nuclear proteins and the organization of chromatin in spermatozoa of Mytilus edulis. Exp Cell Res 141:39-45.
6. Ausió J, van Veghel MLJ, Gomez R, Barreda D. 1997. The sperm nuclear basic proteins (SNBPs) of the sponge Neofibularia nolitangere: implications for the molecular evolution of SNBPs. J Mol Evol 45:91-96.
7. Ausió J, Eirín-López JM, Frehlick LJ. 2007. Evolution of vertebrate chromosomal sperm proteins: implications for fertility and sperm competition. Soc Reprod Fertil Suppl 65:63-79.
8. Bloch DP. 1969. A catalog of sperm histones. Genetics (Suppl) 61:93-111.
9. Bloch DP. 1976. Histones of sperm. In: King RC, editor. Handbook of genetics Vol. 5. New York: Plennum Press. p 139-167.
10. Bulger M. 2005. Hyperacetylated chromatin domains: lessons from heterochromatin. J Biol Chem 280:21689-21692.
11. Cáceres C, Giménez-Bonafé P, Ribes E, Wouters-Tyrou D, Martinage A, Kouach M, Sautiére P, Muller S, Palau J, Subirana JA, Cornudella L, Chiva M. 1999. DNA-interacting proteins in the spermiogenesis of the mollusc Murex brandaris. J Biol Chem 247:649-656.
12. Calestagne-Moreli A, Ausió J. 2006. Long-range histone acetylation: biological significance structural implications and mechanisms. Biochem Cell Biol 84:518-527.
13. Casas MT, Muñoz-Guerra S, Subirana JA. 1981. Preliminary report on the ultrastructure of chromatin in the histone containing spermatozoa of a teleost fish. Biol Cell 40:87-92.
14. Chiva M, Daban M, Rosenberg E, Kasinsky HE. 1992. Protamines in polyplacophores and gastropods as a model for evolutionary changes in molluscan sperm basic proteins. In: Baccetti B, editor. Comparative spermatology. New York: Raven Press. p 77-82.
15. Coupez M, Martin-Ponthieu A, Sautiére P. 1987. Histone H4 from cuttlefish testis is sequentially acetylated. J Biol Chem 252:2854-2860.
16. Courtens JL, Kistler WS, Plöen L. 1995. Ultrastructural immunolocalisation of histones H2B, H3, H4, transition protein TP1 and protamine in rabbit spermatids and spermatozoa nuclei. Relation to condensation of the chromatin. Reprod Nutr Dev 35:569-582.
17. Daban JR. 2000. Physical constraints in the condensation of eukaryotic chromosomes. Local concentration of DNA versus linear packing ratio in higher order chromatin structures. Biochem 39:3861-3866.
18. Daban M, Morriconi E, Kasinsky HE, Chiva, M. 1990. Characterization of nuclear basic sperm proteins in one archaeogastropod: comparison of protamines between species. Comp Biochem Physiol 96B: 123-127.
19. Daban M, Chiva M, Rosenberg E, Kasinsky HE, Subirana JA. 1991. Protamines in prosobranchian grastropods (Mollusca) vary with differnt modes of reproduction. J Exp Zool 257:265-283.
20. Daban M, Martinage A, Kouach M, Chiva M, Subirana JA, Sautiére P. 1995. Sequence analysis and structural features of the largest known protamine isolated from the sperm of the archaeogastropod Monodonta turbinata. J Mol Evol 40:663-670.
21. Frehlick LJ, Eirín-López JM, Jeffery ED, Hunt DF, Ausió J. 2006. The characterization of amphibian nucleoplasmins yields new insight into their role in sperm chromatin remodelling. BMC Genomics 7:1-13.
22. García-Ramírez M, Rocchini C, Ausió J. 1995. Modulation of chromatin folding by histone acetylation. J Biol Chem 270:17923-17928.
23. Gatewood JM, Cook GR, Balhorn R, Schmid CW, Bradbury EM. 1990. Isolation of four core histones from human sperm chromatin representing a minor subset of somatic histones. J Biol Chem 265:20662-20666.
24. Giménez-Bonafé P, Ribes E, Sautiére P, Gonzalez A, Kasinsky HE, Kouach M, Sautiére PE, Ausió J, Chiva M. 2002. Chromatin condensation, cysteine-rich protamine, and establishment of disulphide interprotamine bonds during spermiogenesis of Eledone cirrhosa (Cephalopoda). Eur J Cell Biol 81:341-349.
25. Giménez-Bonafé P, Martínez-Soler F, Buesa C, Ribes E, Sautiére PE, Ausió J, Kouach M, Kasinsky H, Chiva M. 2004. Chromatin organization during spermiogenesis in Octopus vulgaris. II: DNA-interacting proteins. Mol Reprod Dev 68:232-239.
26. Grimes Jr SR, Henderson N. 1983. Acetylation of histones during spermatogenesis in the rat. Arch Biochem Biophys 221:108-116.
27. Gwo JC, Gwo HH. 1993. Spermatogenesis in the Black Porgy Acanthopagrus schlegeli Teleostei: Perciformes: Sparidae. Mol Reprod Dev 36:75-83.
28. Gwo JC, Chiu JY, Lin CY, Su Y, Yu SL. 2005. Spermatozoal ultrastructure of four Sparidae fishes: Acanthopagrus berda, Acanthopagrus australis, Lagodon rhomboids, and Archosargus probatocephus. Tissue Cell 37:109-115.
29. Hazzouri M, Pivot-Pajot C, Faure AK, Usson Y, Pelletier R, Séle B, Khochbin S, Rousseaux S. 2000. Regulated hyperacetyla-tion of core histones during mouse spermatogenesis: involvement of histone-deacetylases. Eur J Cell Biol 79:950-960.
30. Hunt JG, Kasinsky HE, Elsey RM, Wright CL, Rice P, Bell JE, Sharp DJ, Kiss AJ, Hunt DF, Arnott DP, Russ MM, Shabanowits J, Ausió J. 1996. Protamines of reptiles. J Biol Chem 271:23547-23557.
31. Johnson EM, Littau VC, Allfrey VG, Bradbury EM. 1976. The subunit structure of chromatin from Physarum polycepha-lum. Nucl Acids Res 3:3313-3329.
32. Kasinsky HE. 1989. Specificity and distribution of sperm basic proteins. In: Hnilica LS, Stein GS, Stein JL, editor). Histones and other basic nuclear proteins. Boca Raton, FL: CRG Press, p 73-163.
33. Kasinsky HE, Gutovich L, Kulak D, Mackay M, Green DM, Hunt J, Ausiü J. 1999. Protamine-like sperm nuclear basic proteins in the primitive frog Ascaphus truei and histone reversions among more advanced frogs. J Exp Zool 284:717-728.
34. Kimmins S, Sassone-Corsi P. 2005. Chromatin remodelling and epigenetic features of germ cells. Nature 434:583-589.
35. Kouzarides T. 2007. Chromatin modifications and their function. Cell 128:693-705.
36. Kurtz K, Martínez-Soler F, Ausió J, Chiva M. 2007. Acetyla-tion of histone H4 in complex structural transitions of spermiogenic chromatin. J Cell Biochem 102:1432-1441.
37. Kurtz K, Martínez-Soler F, Ausió J, Chiva M. 2008. Histones and nucleosomes in Cancer sperm 88.
38. Muñoz-Guerra S, Azorín F, Casas MT, Marcel X, Maristany MA, Roca J, Subirana JA. 1982. Structural organization of sperm chromatin from the fish Carassius auratus. Exp Cell Res 137:47-53.
39. Oliva R, Dixon GM. 1991. Vertebrate protamine genes and the histone-to-protamine replacement reaction. Prog Nucleic Acid Res Mol Biol 40:25-94.
40. Ribes E, Sánchez de Romero LD, Kasinsky HE, del Valle L, Giménez-Bonafe P, Chiva M. 2001. Chromatin reorganization during spermiogenesis of the mollusc Thais hemostoma (Muricidae). Implications for sperm nuclear morphogenesis in cenogastropods. J Exp Zool 289:304-316.
41. Risley MS, Eckhardt RA, Mann M, Kasinsky HE. 1982. Determinants of sperm nuclear shaping in the genus Xenopus. Chromosoma 84:557-569.
42. Rocchini C, Marx RM, Carosfeld JS, Kasinsky HE, Rosenberg E, Sommer F, Ausio J. 1996. Replacement of histones by histone H1-like proteins during spermiogenesis in Cnidaria: evolutionary implications. J Mol Evol 42:240-246.
43. Rousseaux-Prévost P, Engelhardt RP, Rousseaux J, Wouters-Tyrou D, Sautiére P. 1988. Nuclear protein transitions in cuttle-fish spermiogenesis: immunocytochemicallocalization of a protein specific for the spermatic stage. Gamete Res 19:277-290.
44. Saperas N, Ribes E, Buesa C, García-Hegart F, Chiva M. 1993. Differences in chromatin condensation during spermiogenesis in two species of bony fish with distinct protamines. J Exp Zool 265:185-194.
45. Saperas N, Ausió J, Lloris D, Chiva M. 1994. On the evolution of protamines in bony fish: alternatives to the retroviral horizontal transmission. J Mol Evol 39:282-295.
46. Saperas N, Chiva M, Pfeiffer DC, Kasinsky HE, Ausió J. 1997. Sperm nuclear basic proteins (SNBPs) of agnathans and chondrichthyans: variability and evolution of sperm proi-tens in fish. J Mol Evol 44:422-431.
47. Saperas N, Chiva M, Casas MT, Campos L, Eirín-Lopez JM, Frehlick LJ, Prieto C, Subirana JA, Ausió J. 2006. A unique vertebrate histone Hl-related protamine-like protein results in an unusual sperm chromatin organization. FEBS J 273:4548-4561.
48. Subirana JA. 1975. On the biological role of basic proteins in spermatozoa and during spermiogenesis. In: Duckett JG, Racey PA, editors. The biology of the male gamete. Supplement No. 1 to the Biological Journal of the Linnean Society 7:239-244.
49. Subirana JA. 1983. Nuclear proteins in spermatozoa and their interactions with DNA. In: André J, editor. The sperm cell. The Hague: Martinus Nijohoff. p 197-213.
50. Th'ng JPH, Sung R, Ye M, Hendzel MJ. 2005. H1 family histones in the nucleus. J Biol Chem 280:27809-27814.
51. Vodicka M, Green GR, Poccia DL. 1990. Sperm histones and chromatin structure of the primitive sea urchin Eucidaris tribuloides. Dev Cell Biol 256:179-188.
52. Ward WS, Coffey DS 1991. DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol Reprod 44:569-574.
53. Wouters-Tyrou D, Chartier-Harlin MC, Martin-Ponthieu A, Boutillon C, van Dorsselaer A, Sautiére P. 1991. Cuttlefish spermatid-specific protein T. Molecular characterization of two variants T1 and T2: putative precursors of sperm protamine variants Spl and Sp2. J Biol Chem 266:17388-17395.
54. Zalenskaya IA, Pospelov VA, Zalensky AO, Vorob'ev VI. 1981. Nucleosomal structure of sea urchin and starfish sperm chromatin. Histone H2B is possibly involved in determining the length of linker DNA. Nucleic Acid Res 9:473-487.
55. Zhao M, Shirley CR, Mounsey S, Meistrich ML. 2004. Nucleoprotein transitions during spermiogenesis in mice with transition nuclear protein Tnp1 and Tnp2 mutations. Biol Reprod 71:1016-1025.
56. Zheng C, Hayes JJ. 2003. Structures and interactions of the core histone tail domains. Biopolymers 68:539-546.