Influence of sex on the meiotic segregation of a t(13;17) Robertsonian translocation: A case study in the pig

Human Reproduction

Volumn 24, Issue 8, 2009, Pages 2034-2043

  Pinton, A ^a   Calgaro, A ^a   Bonnet, N ^a   Ferchaud, S ^b   Billoux, S ^a   Dudez, A M ^a   Mary, N ^a   Massip, K ^a   Bonnet Garnier, A ^a   Yerle, M ^a   Ducos, A ^a  

^a CNRS   (France)

^b CEMAGREF   (France)

Author keywords

Chromosome pairing; Meiosis; Pig; Robertsonian translocation; Segregation

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CELL MATURATION; CHROMOSOME SEGREGATION; CONTROLLED STUDY; FLUORESCENCE IN SITU HYBRIDIZATION; IMMUNOLOCALIZATION; NONHUMAN; PACHYTENE; ROBERTSONIAN CHROMOSOME TRANSLOCATION; SEX; SEX CHROMOSOME; SPERMATOZOON; SWINE;

ANIMALIA; MAMMALIA; ROBERTSONIA; SUIDAE; SUS SCROFA DOMESTICA;

EID: 67651121818     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/dep118     Document Type: Article

References (72)

1. Angell RR. Predivision in human oocytes at meiosis I: a mechanism for trisomy formation in man. Hum Genet 1991;86:383-387.
2. Anton E, Blanco J, Egozcue J, Vidal F. Sperm FISH studies in seven male carriers of Robertsonian translocation t(13;14)(q10;q10). Hum Reprod 2004;19:1345-1351.
3. Anton E, Vidal F, Blanco J. Role of sperm FISH studies in the genetic reproductive advice of structural reorganization carriers. Hum Reprod 2007;22:2088-2092.
4. Aranha IP, Martin-DeLeon PA. Segregation analysis of the mouse Rb(6.16) translocation in zygotes produced by heterozygous female carriers. Cytogenet Cell Genet 1994;66:51-53.
5. Archibald AL, Haley CS, Brown JF, Couperwhite S, McQueen HA, Nicholson D, Coppieters W, Van de Weghe A, Stratil A, Wintero AK et al. The PiGMaP consortium linkage map of the pig (Sus scrofa). Mamm Genome 1995;6:157-175.
6. Bonnet-Garnier A, Lacaze S, Beckers JF, Berland HM, Pinton A, Yerle M, Ducos A. Meiotic segregation analysis in cows carrying the t(1;29) Robertsonian translocation. Cytogenet Genome Res 2008;120:91-96.
7. Burgoyne PS, Mahadevaiah SK, Turner JM. The consequences of asynapsis for mammalian meiosis. Nat Rev Genet 2009;10:207-216.
8. Chen Y, Huang J, Liu P, Qiao J. Analysis of meiotic segregation patterns and interchromosomal effects in sperm from six males with Robertsonian translocations. J Assist Reprod Genet 2007;24:406-411.
9. Codina-Pascual M, Oliver-Bonet M, Navarro J, Campillo M, Garcia F, Egozcue S, Abad C, Egozcue J, Benet J. Synapsis and meiotic recombination analyses: MLH1 focus in the XY pair as an indicator. Hum Reprod 2005;20:2133-2139.
10. Dagnélie P. Les tests d'indépendance et les méthodes relatives aux proportions, Théorie et méthodes statistiques, applications agronomiques. Les Presses Agronomiques de Gembloux, Gembloux 1975;2:81-105.
11. Ducos A, Revay T, Kovacs A, Hidas A, Pinton A, Bonnet-Garnier A, Molteni L, Slota E, Switonski M, Arruga MV et al. Cytogenetic screening of livestock populations in Europe: an overview. Cytogenet Genome Res 2008;120:26-41.
12. Durban M, Benet J, Boada M, Fernandez E, Calafell JM, Lailla JM, Sanchez-Garcia JF, Pujol A, Egozcue J, Navarro J. PGD in female carriers of balanced Robertsonian and reciprocal translocations by first polar body analysis. Hum Reprod Update 2001;7:591-602.
13. Eaker S, Pyle A, Cobb J, Handel MA. Evidence for meiotic spindle checkpoint from analysis of spermatocytes from Robertsonianchromosome heterozygous mice. J Cell Sci 2001;114:2953-2965.
14. Ferguson KA, Chow V, Ma S. Silencing of unpaired meiotic chromosomes and altered recombination patterns in an azoospermic carrier of a t(8;13) reciprocal translocation. Hum Reprod 2008;23:988-995.
15. Gabriel-Robez O, Rumpler Y. The meiotic pairing behaviour in human spermatocytes carrier of chromosome anomalies and their repercussions on reproductive fitness. I: Inversions and insertions. A European collaborative study. Ann Genet 1994;37:3-10.
16. Gabriel-Robez O, Jaafar H, Ratomponirina C, Boscher J, Bonneau J, Popescu CP, Rumpler Y. Heterosynapsis in a heterozygous fertile boar carrier of a 3;7 translocation. Chromosoma 1988;97:26-32.
17. Guo Y, Mao H, Ren J, Yan X, Duan Y, Yang G, Ren D, Zhang Z, Yang B, Ouyang J et al. A linkage map of the porcine genome from a large-scale White Duroc x Erhualian resource population and evaluation of factors affecting recombination rates. Anim Genet 2009;40:47-52.
18. Hassanane M, Kovacs A, Laurent P, Lindblad K, Gustavsson I. Simultaneous detection of X- and Y-bearing bull spermatozoa by double colour fluorescence in situ hybridization. Mol Reprod Dev 1999; 53:407-412.
19. Honda H, Miharu N, Samura O, He H, Ohama K. Meiotic segregation analysis of a 14;21 Robertsonian translocation carrier by fluorescence in situ hybridization. Hum Genet 2000;106:188-193.
20. Hunt PA, Hassold TJ. Sex matters in meiosis. Science 2002; 296:2181-2183.
21. Jaafar H, Gabriel-Robez O, Ratomponirina C, Boscher J, Bonneau M, Popescu CP, Rumpler Y. Analysis of synaptonemal complexes in two fertile heterozygous boars, both carriers of a reciprocal translocation involving an acrocentric chromosome. Cytogenet Cell Genet 1989; 50:220-225.
22. Jaafar H, Bouvet A, Gabriel-Robez O, Bonneau M, Boscher J, Maetz JL, Popescu CP, Rumpler Y. Heterosynapsis in two fertile but hypoprolific boars carriers of reciprocal translocations. Ann Genet 1992;35:3-7.
23. Jaafar H, Gabriel-Robez O, Rumpler Y. Chromosomal anomalies and disturbance of transcriptional activity at the pachytene stage of meiosis: relationship to male sterility. Cytogenet Cell Genet 1993; 64:273-280.
24. Johannisson R, Lohrs U, Wolff HH, Schwinger E. Two different XY-quadrivalent associations and impairment of fertility in men. Cytogenet Cell Genet 1987;45:222-230.
25. Johannisson R, Schwinger E, Wolff HH, vom Ende V, Lohrs U. The effect of 13;14 Robertsonian translocations on germ-cell differentiation in infertile males. Cytogenet Cell Genet 1993;63:151-155.
26. Kauppi L, Jeffreys AJ, Keeney S. Where the crossovers are: recombination distributions in mammals. Nat Rev Genet 2004;5:413-424.
27. Lechniak D, Warzych E, Pers-Kamczyc E, Sosnowski J, Antosik P, Rubes J. Gilts and sows produce similar rate of diploid oocytes in vitro whereas the incidence of aneuploidy differs significantly. Theriogenology 2007; 68:755-762.
28. LiW, Fann CS, Ott J. Low-order polynomial trends of female-to-male map distance ratios along human chromosomes. Hum Hered 1998; 48:266-270.
29. Lifschytz E, Lindsley DL. The role of X-chromosome inactivation during spermatogenesis (Drosophila-allocycly-chromosome evolution-male sterility-dosage compensation). Proc Natl Acad Sci USA 1972; 69:182-186.
30. Luciani JM, Guichaoua MR, Mattei A, Morazzani MR. Pachytene analysis of a man with a 13q;14q translocation and infertility. Behavior of the trivalent and nonrandom association with the sex vesicle. Cytogenet Cell Genet 1984;38:14-22.
31. Marchal R, Feugang JM, Perreau C, Venturi E, Terqui M, Mermillod P. Meiotic and developmental competence of prepubertal and adult swine oocytes. Theriogenology 2001;56:17-29.
32. Marklund L, Johansson Moller M, Hoyheim B, Davies W, Fredholm M, Juneja RK, Mariani P, Coppieters W, Ellegren H, Andersson L. A comprehensive linkage map of the pig based on a wild pig-Large White intercross. Anim Genet 1996;27:255-269.
33. Martin RH. Cytogenetic determinants of male fertility. Hum Reprod Update 2008;14:379-390.
34. Mau-Holzmann UA. Somatic chromosomal abnormalities in infertile men and women. Cytogenet Genome Res 2005;111:317-336.
35. Mikawa S, Akita T, Hisamatsu N, Inage Y, Ito Y, Kobayashi E, Kusumoto H, Matsumoto T, Mikami H, Minezawa M et al. A linkage map of 243 DNA markers in an intercross of Gottingen miniature and Meishan pigs. Anim Genet 1999;30:407-417.
36. Moradkhani K, Puechberty J, Bhatt S, Lespinasse J, Vago P, Lefort G, Sarda P, Hamamah S, Pellestor F. Rare Robertsonian translocations and meiotic behaviour: sperm FISH analysis of t(13;15) and t(14;15) translocations: a case report. Hum Reprod 2006a;21:3193-3198.
37. Moradkhani K, Puechberty J, Bhatt S, Vago P, Janny L, Lefort G, Hamamah S, Sarda P, Pellestor F. Meiotic segregation of rare Robertsonian translocations: sperm analysis of three t(14q;22q) cases. Hum Reprod 2006b;21:1166-1171.
38. Morel F, Roux C, Bresson JL. FISH analysis of the chromosomal status of spermatozoa from three men with 45,XY,der(13;14)(q10;q10) karyotype. Mol Hum Reprod 2001;7:483-488.
39. Morelli MA, Cohen PE. Not all germcells are created equal: aspects of sexual dimorphism in mammalian meiosis. Reproduction 2005;130:761- 781.
40. Munne S, Escudero T, Sandalinas M, Sable D, Cohen J. Gamete segregation in female carriers of Robertsonian translocations. Cytogenet Cell Genet 2000;90:303-308.
41. Navarro J, Vidal F, Benet J, Templado C, Marina S, Egozcue J. XY-trivalent association and synaptic anomalies in a male carrier of a Robertsonian t(13;14) translocation. Hum Reprod 1991;6:376-381.
42. Nielsen J, Wohlert M. Chromosome abnormalities found among 34,910 newborn children: results from a 13-year incidence study in Arhus, Denmark. Hum Genet 1991;87:81-83.
43. Ogur G, Van Assche E, VegettiW, Verheyen G, Tournaye H, Bonduelle M, Van Steirteghem A, Liebaers I. Chromosomal segregation in spermatozoa of 14 Robertsonian translocation carriers. Mol Hum Reprod 2006;12:209- 215.
44. Oliver-Bonet M, Benet J, Sun F, Navarro J, Abad C, Liehr T, Starke H, Greene C, Ko E, Martin RH. Meiotic studies in two human reciprocal translocations and their association with spermatogenic failure. Hum Reprod 2005;20:683-688.
45. Pardo-Manuel de Villena F, Sapienza C. Transmission ratio distortion in offspring of heterozygous female carriers of Robertsonian translocations. Hum Genet 2001;108:31-36.
46. Pellestor F. Analysis of meiotic segregation in a man heterozygous for a 13;15 Robertsonian translocation and a review of the literature. Hum Genet 1990;85:49-54.
47. Pinton A, Ducos A, Seguela A, Berland HM, Darre R, Darre A, Pinton P, Schmitz A, Cribiu EP, Yerle M. Characterization of reciprocal translocations in pigs using dual-colour chromosome painting and primed in situ DNA labelling. Chromosome Res 1998;6:361-366.
48. Pinton A, Ducos A, Yerle M. Estimation of the proportion of genetically unbalanced spermatozoa in the semen of boars carrying chromosomal rearrangements using FISH on sperm nuclei. Genet Sel Evol 2004; 36:123-137.
49. Pinton A, Faraut T, Yerle M, Gruand J, Pellestor F, Ducos A. Comparison of male and female meiotic segregation patterns in translocation heterozygotes: a case study in an animal model (Sus scrofa domestica L.). Hum Reprod 2005;20:2476-2482.
50. Pinton A, Raymond Letron I, Berland HM, Bonnet N, Calgaro A, Garnier-Bonnet A, Yerle M, Ducos A. Meiotic studies in an azoospermic boar carrying a Y;14 translocation. Cytogenet Genome Res 2008;120:106- 111.
51. Pujol A, Boiso I, Benet J, Veiga A, Durban M, Campillo M, Egozcue J, Navarro J. Analysis of nine chromosome probes in first polar bodies and metaphase II oocytes for the detection of aneuploides. Eur J Hum Genet 2003;11:325-336.
52. Rives N, Ravel C, Duchesne V, Siffroi JP, Mousset-Simeon N, Mace B. Molecular cytogenetics analysis with whole chromosome paint probes of sperm nuclei from a (13;15) Robertsonian translocation carrier. J Hum Genet 2005;50:360-364.
53. Roeder GS, Bailis JM. The pachytene checkpoint. Trends Genet 2000; 16:395-403.
54. Rohrer GA, Alexander LJ, Hu Z, Smith TP, Keele JW, Beattie CW. A comprehensivemap of the porcine genome. Genome Res 1996;6:371-391.
55. Rousseaux S, Chevret E, Monteil M, Cozzi J, Pelletier R, Delafontaine D, Sele B. Sperm nuclei analysis of a Robertsonian t(14q21q) carrier, by FISH, using three plasmids and two YAC probes. Hum Genet 1995; 96:655-660.
56. Roux C, Tripogney C, Morel F, Joanne C, Fellmann F, Clavequin MC, Bresson JL. Segregation of chromosomes in sperm of Robertsonian translocation carriers. Cytogenet Genome Res 2005;111:291-296.
57. Schulz R, Underkoffler LA, Collins JN, Oakey RJ. Nondisjunction and transmission ratio distortion of Chromosome 2 in a (2.8) Robertsonian translocation mouse strain. Mamm Genome 2006;17:239-247.
58. Sciurano R, Rahn M, Rey-Valzacchi G, Solari AJ. The asynaptic chromatin in spermatocytes of translocation carriers contains the histone variant gamma-H2AX and associates with the XY body. Hum Reprod 2007; 22:142-150.
59. Shan J, Zhang C, Sun J, Li L. Synaptonemal complex analysis of 13/17 Robertsonian translocation in the domestic pig. Yi Chuan Xue Bao 1994;21:96-103.
60. Solari AJ. Synaptosomal complexes and associated structures in microspread human spermatocytes. Chromosoma 1980;81:315-337.
61. Solari AJ. Synaptonemal complex analysis in human male infertility. Eur J Histochem 1999;43:265-276.
62. Sosnowski J, Waroczyk M, Switonski M. Chromosome abnormalities in secondary pig oocytes matured in vitro. Theriogenology 2003;60:571-581.
63. Sun F, Oliver-Bonet M, Liehr T, Starke H, Turek P, Ko E, Rademaker A, Martin RH. Variation in MLH1 distribution in recombination maps for individual chromosomes from human males. Hum Mol Genet 2006; 15:2376-2391.
64. Turner JM, Mahadevaiah SK, Fernandez-Capetillo O, Nussenzweig A, Xu X, Deng CX, Burgoyne PS. Silencing of unsynapsed meiotic chromosomes in the mouse. Nat Genet 2005;37:41-47.
65. Turner JM, Mahadevaiah SK, Ellis PJ, Mitchell MJ, Burgoyne PS. Pachytene asynapsis drives meiotic sex chromosome inactivation and leads to substantial postmeiotic repression in spermatids. Dev Cell 2006; 10:521-529.
66. Underkoffler LA, Mitchell LE, Abdulali ZS, Collins JN, Oakey RJ. Transmission ratio distortion in offspring of mouse heterozygous carriers of a (7.18) Robertsonian translocation. Genetics 2005; 169:843-848.
67. Vidal F, Templado C, Navarro J, Marina S, Egozcue J. Meiotic and synaptonemal complex studies in a 14/21 translocation carrier. Int J Androl 1982;5:21-26.
68. Villagomez DA. Zygotene-pachytene substaging and synaptonemal complex karyotyping of boar spermatocytes. Hereditas 1993; 118:87-99.
69. Villagomez DA, Pinton A. Chromosomal abnormalities, meiotic behavior and fertility in domestic animals. Cytogenet Genome Res 2008; 120:69-80.
70. Villagomez DA, Gustavsson I, Alabay B, Ploen L. Meiotic chromosome asynapsis in a boar with a reciprocal translocation and acquired testicular degeneration. Hereditas 1993;118:101-111.
71. Villagomez DA, Gustavsson I, Jonsson L, Ploen L. Reciprocal chromosome translocation, rcp(7;17)(q26;q11), in a boar giving reduced litter size and increased rate of piglets dying in the early life. Hereditas 1995; 122:257-267.
72. Vozdova M, Machatkova M, Kubikova S, Zudova D, Jokesova E, Rubes J. Frequency of aneuploidy in pig oocytes matured in vitro and of the corresponding first polar bodies detected by fluorescent in situ hybridization. Theriogenology 2001;56:771-776.