Polymorphisms, haplotypes and mutations in the protamine 1 and 2 genes

International Journal of Andrology

Volumn 34, Issue 5 PART 1, 2011, Pages 470-485

  Jodar, M ^a   Oriola, J ^a   Mestre, G ^a   Castillo, J ^a   Giwercman, A ^b   Vidal Taboada, J M ^c   Ballesca J L ^d   Oliva, R ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b LUND UNIVERSITY HOSPITAL   (Sweden)

^c UNIVERSITY OF BARCELONA   (Spain)

^d HOSPITAL CLÍNIC   (Spain)

Author keywords

Haplotype; Infertility; Mutation; P1; P2; PRM1; PRM2; Protamine; SNP; Spermatozoa

Indexed keywords

PROTAMINE; PROTAMINE P1; PROTAMINE P2; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; FEMALE; GENE SEQUENCE; HAPLOTYPE; HUMAN; HUMAN CELL; INFERTILITY; MAJOR CLINICAL STUDY; MALE; MISSENSE MUTATION; POPULATION GENETICS; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM;

HAPLOTYPES; HUMANS; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION, MISSENSE; POLYMORPHISM, GENETIC; PROMOTER REGIONS, GENETIC; PROTAMINES; SPAIN; SPERMATOZOA; SWEDEN;

EID: 79956115888     PISSN: 01056263     EISSN: 13652605     Source Type: Journal    
DOI: 10.1111/j.1365-2605.2010.01115.x     Document Type: Article

References (78)

1. Adroer R & Oliva R. (1998) Nucleosome positioning in the rat protamine 1 gene in vivo and in vitro. Biochim Biophys Acta 1442, 252-260.
2. Ando T, Yamasaki M & Suzuki K. (1973) Protamines. Isolation, characterization, structure and function. Mol Biol Biochem Biophys 12, 1-114.
3. Aoki VW, Liu L & Carrell DT. (2005) Identification and evaluation of a novel sperm protamine abnormality in a population of infertile males. Hum Reprod 20, 1298-1306.
4. Aoki VW, Christensen GL, Atkins JF & Carrell DT. (2006a) Identification of novel polymorphisms in the nuclear protein genes and their relationship with human sperm protamine deficiency and severe male infertility. Fertil Steril 86, 1416-1422.
5. Aoki VW, Emery BR, Liu L & Carrell DT. (2006b) Protamine levels vary between individual sperm cells of infertile human males and correlate with viability and DNA integrity. J Androl 27, 890-898.
6. Aoki VW, Liu L & Carrell DT. (2006c) A novel mechanism of protamine expression deregulation highlighted by abnormal protamine transcript retention in infertile human males with sperm protamine deficiency. Mol Hum Reprod 121, 41-50.
7. Aoki VW, Liu L, Jones KP, Hatasaka HH, Gibson M, Peterson CM & Carrell DT. (2006d) Sperm protamine 1/protamine 2 ratios are related to in vitro fertilization pregnancy rates and predictive of fertilization ability. Fertil Steril 865, 1408-1415.
8. Arpanahi A, Brinkworth M, Iles D, Krawetz SA, Paradowska A, Platts AE et al. (2009) Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences. Genome Res 8, 1338-1349.
9. Bach O, Glander HJ, Scholz G & Schwarz J. (1990) Electrophoretic patterns of spermatozoal nucleoproteins (NP) in fertile men and infertility patients and comparison with NP of somatic cells. Andrology 22, 217-224.
10. Balhorn R. (2007) The protamine family of sperm nuclear proteins. Genome Biol 8, 227.1-227.8.
11. Balhorn R, Reed S & Tanphaichitr N. (1988) Aberrant protamine 1/protamine 2 ratios in sperm of infertile human males. Experientia 44, 52-55.
12. Barrett JC, Fry B, Maller J & Daly MJ. (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263-265.
13. Belokopytova IA, Kostyleva EI, Tomilin AN & Vorob'ev VI. (1993) Human male infertility may be due to a decrease of the protamine P2 content in sperm chromatin. Mol Reprod Dev 34, 53-57.
14. Bench G, Corzett MH, De Yebra L, Oliva R & Balhorn R. (1998) Protein and DNA contents in sperm from an infertile human male possessing protamine defects that vary over time. Mol Reprod Dev 50, 345-353.
15. Björndahl L & Kvist U. (2010) Human sperm chromatin stabilization: a proposed model including zinc bridges. Mol Hum Reprod 16, 23-29.
16. Blanchard Y, Lescoat D & Le Lannou D. (1990) Anomalous distribution of nuclear basic proteins in round-headed human spermatozoa. Andrology 22, 549-555.
17. Bloch DP. (1969) A catalog of sperm histones. Genetics 61(Suppl), 93-111.
18. Calvin HI. (1976) Comparative analysis of the nuclear basic proteins in rat, human, guinea pig, mouse and rabbit spermatozoa. Biochim Biophys Acta 434, 377-389.
19. Carrell DT, Emery BR & Hammoud S. (2007) Altered protamine expression and diminished spermatogenesis: what is the link?. Hum Reprod Update 13, 313-327.
20. Cho C, Willis WD, Goulding EH, Jung-Ha H, Choi YC, Hecht NB & Eddy EM. (2001) Haploinsufficiency of protamine-1 or -2 causes infertility in mice. Nat Genet 28, 82-86.
21. Choi YC, Aizawa A & Hecht NB. (1997) Genomic analysis of the mouse protamine 1, protamine 2, and transition protein 2 gene cluster reveals hypermethylation in expressing cells. Mamm Genome 8, 317-323.
22. Domínguez-Fandos D, Camejo MI, Ballescà JL & Oliva R. (2007) Human sperm DNA fragmentation: correlation of TUNEL results as assessed by flow cytometry and optical microscopy. Cytometry A 71, 1011-1018.
23. Egger M, Smith GD & Altman DG. (2001) Systematic Reviews in Health Care: Meta-Analysis in Context, 2nd edn BMJ Publishing, London.
24. Eirín-López JM & Ausió J. (2009) Origin and evolution of chromosomal sperm proteins. Bioessays 31, 1062-1070.
25. Eirin-Lopez JM, Frehlick LJ & Ausio J. (2006) Protamines, in the footsteps of linker histone evolution. J Biol Chem 281, 1-4.
26. Engel W, Keime S, Kremling H, Hameister H & Schlüter G. (1992) The genes for protamine 1 and 2 (PRM1 and PRM2) and transition protein 2 (TNP2) are closely linked in the mammalian genome. Cytogenet Cell Genet 61, 158-159.
27. Gázquez C, Oriola J, de Mateo S, Vidal-Taboada JM, Ballesca JL & Oliva R. (2008) A common protamine 1 promotor polymorphism (-190 C→A) correlates with abnormal sperm morphology and increased protamine P1/P2 ratio in infertile patients. J Androl 29, 540-548.
28. González JR, Armengol L, Solé X, Guinó E, Mercader JM, Estivill X & Moreno V. (2007) SNPassoc: an R package to perform whole genome association studies. Bioinformatics 23, 644-645.
29. Grzmil P, Boinska D, Kleene KC, Adham I, Schlüter G, Kämper M et al. (2008) Prm3, the fourth gene in the mouse protamine gene cluster, encodes a conserved acidic protein that affects sperm motility. Biol Reprod 78, 958-967.
30. Hammoud S, Emery BR, Aoki VW & Carrell DT. (2007) Identification of genetic variation in the 5' and 3' non-coding regions of the protamine genes in patients with protamine deregulation. Andrology 53, 267-274.
31. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT & Cairns BR. (2009) Distinctive chromatin in human sperm packages genes for embryo development. Nature 460, 473-478.
32. Hossain AM, Rizk B, Behzadian A & Thorneycroft IH. (1997) Modified guanidinium thiocyanate method for human sperm DNA isolation. Mol Hum Reprod 3, 953-956.
33. Iguchi N, Yang S, Lamb DJ & Hecht NB. (2006) An SNP in protamine 1: a possible genetic cause of male infertility? J Med Genet 43, 382-384.
34. Imken L, Rouba H, El Houate B, Louanjli N, Barakat A, Chafik A & McElreavey K. (2009) Mutations in the protamine locus: association with spermatogenic failure?. Mol Hum Reprod 15, 733-738.
35. Kichine E, Msaidie S, Bokilo AD, Ducourneau A, Navarro A, Levy N et al. (2008) Low-frequency protamine 1 gene transversions c.102G->T and c.-107G->C do not correlate with male infertility. J Med Genet 45, 255-256.
36. Kramer JA, Zang S, Yaron Y, Zhao Y & Krawetz SA. (1997) Genetic testing for male infertility: a postulated role for mutations in sperm nuclear matrix attachment regions. Genet Test 1, 125-129.
37. Kramer JA, Adams MD, Singh GB, Doggett NA & Krawetz SA. (1998) Extended analysis of the region encompassing the PRM1-->PRM2-->TNP2 domain: genomic organization, evolution and gene identification. J Exp Zool 282, 245-253.
38. Kruger TF, Ackerman SB, Simmons KF, Swanson RJ, Brugo SS & Acosta AA. (1987) A quick, reliable staining technique for human sperm morphology. Arch Androl 18, 275-277.
39. Lee S, Kasif S, Weng Z & Cantor CR. (2008) Quantitative analysis of single nucleotide polymorphisms within copy number variation. PLoS ONE 3, e3906.
40. Li Y, Lalancette C, Miller D & Krawetz SA. (2008) Characterization of nucleohistone and nucleoprotamine components in the mature human sperm nucleus. Asian J Androl 10, 535-541.
41. Martínez-Heredia J, Estanyol JM, Ballescà JL & Oliva R. (2006) Proteomic identification of human sperm proteins. Proteomics 6, 4356-4369.
42. Martínez-Heredia J, de Mateo S, Vidal-Taboada JM, Estanyol JM, Ballescà JL & Oliva R. (2008) Proteomic expression differences between asthenozoospermic and normozoospermic sperm samples. Hum Reprod 23, 783-791.
43. Martins RP, Ostermeier GC & Krawetz SA. (2004) Nuclear matrix interactions at the human protamine domain: a working model of potentiation. J Biol Chem 279, 51862-51868.
44. de Mateo S, Martínez-Heredia J, Estanyol JM, Domíguez-Fandos D, Vidal-Taboada JM, Ballescà JL & Oliva R. (2007) Marked correlations in protein expression identified by proteomic analysis of human spermatozoa. Proteomics 7, 4264-4277.
45. de Mateo S, Gázquez C, Guimerà M, Balasch J, Meistrich ML, Ballescà JL & Oliva R. (2008) Protamine 2 precursors (pre-P2), protamine 1 to protamine 2 ratio (P1/P2), and assisted reproduction outcome. Fertil Steril 91, 715-722.
46. de Mateo S, Ramos L, van der Vlag J, de Boer P & Oliva R. (2010) Improvement in chromatin maturity of human spermatozoa selected through density gradient centrifugation. Int J Androl; doi:.
47. Mengual L, Ballesca JL, Ascaso C & Oliva R. (2003) Marked differences in protamine content and P1/P2 ratios in sperm cells from Percoll fractions between patients and controls. J Androl 24, 438-447.
48. Mitchell V, Steger K, Marchetti C, Herbaut JC, Devos P & Rigot JM. (2005) Cellular expression of protamine 1 and 2 transcripts in testicular spermatids from azoospermic men submitted to TESE-ICSI. Mol Hum Reprod 11, 373-379.
49. Oliva R. (2006) Protamines and male infertility. Hum Reprod Update 12, 417-435.
50. Oliva R & Dixon GH. (1990) Vertebrate protamine gene evolution I sequence alignments. J Mol Evol 30, 333-346.
51. Oliva R & Dixon GH. (1991) Vertebrate protamine genes and the histone to protamine replacement reaction. Prog Nucleic Acid Res Mol Biol 40, 25-94.
52. Oliva R & Mezquita C. (1986) Marked differences in the ability of distinct protamines to disassemble nucleosomal core particles "in vitro". Biochemistry 25, 6508-6511.
53. Oliva R, Bazett Jones D, Mezquita C & Dixon GH. (1987) Factors affecting nucleosome disassemble by protamines "in vitro" histone hyperacetylation and chromatin structure, time dependence, and the size of the sperm nuclear proteins. J Biol Chem 262, 17016-17025.
54. Oliva R, Martínez-Heredia J & Estanyol JM. (2008) Proteomics in the study of the sperm cell composition, differentiation and function. Syst Biol Reprod Med 54, 23-36.
55. Oliva R, de Mateo S & Estanyol JM. (2009) Sperm cell proteomics. Proteomics 9, 1004-1017.
56. Queralt R & Oliva R. (1993) Demonstration of conserved potential regulatory sequences of the protamine-encoding P1 genes from the different mammals. Gene 133, 197-204.
57. Queralt R, de Fàbregues-Boixar O, Adroer R, Gené M, Gómez-Catalán J, Huguet E & Oliva R. (1993) Direct sequencing of the human protamine P1 gene and application in forensic medicine. J Forensic Sci 38, 1491-1501.
58. Queralt R, Adroer R, Oliva R, Winkfein RJ, Retief JD & Dixon GH. (1995) Evolution of protamine P1 genes in mammals. J Mol Evol 40, 601-607.
59. Ravel C, Chantot-Bastaraud S, El Houate B, Berthaut I, Verstraete L, De Larouziere V et al. (2007) Mutations in the protamine 1 gene associated with male infertility. Mol Hum Reprod 13, 461-464.
60. Retief JD, Winkfein RJ, Dixon GH, Adroer R, Queralt R, Ballabriga J & Oliva R. (1993) Evolution of protamine P1 genes in primates. J Mol Evol 37, 426-434.
61. Schlicker M, Schnulle V, Schneppel L, Vorob'ev VI & Engel W. (1994) Disturbances of nuclear condensation in human spermatozoa: search for mutations in the genes for protamine 1, protamine 2 and transition protein 1. Hum Reprod 9, 2313-2317.
62. Schlüter G, Celik A, Obata R, Schlicker M, Hofferbert S, Schlung A et al. (1996) Sequence analysis of the conserved protamine gene cluster shows that it contains a fourth expressed gene. Mol Reprod Dev 43, 1-6.
63. Schnulle V, Schlicker M & Engel W. (1994) A (GA)n repeat polymorphism in the human protamine 2 (PRM 2) gene. Hum Mol Genet 3, 1445.
64. Steger K, Pauls K, Klonisch T, Franke FE & Bergmann M. (2000) Expression of protamine-1 and -2 mRNA during human spermiogenesis. Mol Hum Reprod 6, 219-225.
65. Steger K, Wilhelm J, Konrad L, Stalf T, Greb R, Diemer T et al. (2008) 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 23, 11-16.
66. Suganuma R, Yanagimachi R & Meistrich ML. (2005) Decline in fertility of mouse sperm with abnormal chromatin during epididymal passage as revealed by ICSI. Hum Reprod 20, 3101-3108.
67. Tanaka H, Miyagawa Y, Tsujimura A, Matsumiya K, Okuyama A & Nishimune Y. (2003) Single nucleotide polymorphisms in the protamine-1 and -2 genes of fertile and infertile human male populations. Mol Hum Repro 9, 69-73.
68. Torregrosa N, Domínguez-Fandos D, Camejo MI, Shirley C, Meistrich ML, Ballescà JL & Oliva R. (2006) Protamine 2 precursors, protamine 1/protamine 2 ratio, DNA integrity and other sperm parameters in infertile patients. Hum Reprod 21, 2084-2089.
69. Tüttelmann F, Křenková P, Römer S, Nestorovic AR, Ljujic M, Štambergová A et al. (2010) A common haplotype of protamine 1 and 2 genes is associated with higher sperm counts. Int J Androl 33, 240-248.
70. Van Den Bussche RA, Hoofer SR & Hansen EW. (2002) Characterization and phylogenetic utility of the mammalian protamine p1 gene. Mol Phylogenet Evol 22, 333-341.
71. Wallace BC, Schmid CH, Lau J & Trikalinos TA. (2009) Meta-Analyst: software for meta-analysis of binary, continuous and diagnostic data. BMC Med Res Methodol 9, 80; doi:.
72. WHO. (1999) WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction, 4th edn. Cambridge University Press, Cambridge.
73. de Yebra L & Oliva R. (1993) Rapid analysis of mammalian sperm nuclear proteins. Anal Biochem 209, 201-203.
74. de Yebra L, Ballesca JL, Vanrell JA, Bassas L & Oliva R. (1993) Complete selective absence of protamine P2 in humans. J Biol Chem 268, 10553-10557.
75. de Yebra L, Ballesca JL, Vanrell JA, Corzett M, Balhorn R & Oliva R. (1998) Detection of P2 precursors in the sperm cells of infertile patients who have reduced protamine P2 levels. Fertil Steril 69, 755-759.
76. Yeung CH, Tüttelmann F, Bergmann M, Nordhoff V, Vorona E & Cooper TG. (2009) Coiled sperm from infertile patients: characteristics, associated factors and biological implication. Hum Reprod 24, 1288-1295.
77. Zhao M, Shirley CR, Yu YE, Mohapatra B, Zhang Y, Unni E et al. (2001) Targeted disruption of the transition protein 2 gene affects sperm chromatin structure and reduces fertility in mice. Mol Cell Biol 21, 7243-7255.
78. Zhao M, Shirley CR, Hayashi S, Marcon L, Mohapatra B, Suganuma R et al. (2004) Transition nuclear proteins are required for normal chromatin condensation and functional sperm development. Genesis 38, 200-213.