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On the origin of crossover interference : a chromosome oscillatory movement (COM) model

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Hultén, Maj A.. (2011) On the origin of crossover interference : a chromosome oscillatory movement (COM) model. Molecular Cytogenetics, Vol.4 (No.10). ISSN 1755-8166

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Official URL: http://dx.doi.org/10.1186/1755-8166-4-10

Abstract

Background: It is now nearly a century since it was first discovered that crossovers between homologous parental chromosomes, originating at the Prophase stage of Meiosis I, are not randomly placed. In fact, the number and distribution of crossovers are strictly regulated with crossovers/chiasmata formed in optimal positions along the length of individual chromosomes, facilitating regular chromosome segregation at the first meiotic division. In spite of much research addressing this question, the underlying mechanism(s) for the phenomenon called crossover/ chiasma interference is/are still unknown; and this constitutes an outstanding biological enigma. Results: The Chromosome Oscillatory Movement (COM) model for crossover/chiasma interference implies that, during Prophase of Meiosis I, oscillatory movements of the telomeres (attached to the nuclear membrane) and the kinetochores (within the centromeres) create waves along the length of chromosome pairs (bivalents) so that crossing-over and chiasma formation is facilitated by the proximity of parental homologs induced at the nodal regions of the waves thus created. This model adequately explains the salient features of crossover/chiasma interference, where (1) there is normally at least one crossover/chiasma per bivalent, (2) the number is correlated to bivalent length, (3) the positions are dependent on the number per bivalent, (4) interference distances are on average longer over the centromere than along chromosome arms, and (5) there are significant changes in carriers of structural chromosome rearrangements. Conclusions: The crossover/chiasma frequency distribution in humans and mice with normal karyotypes as well as in carriers of structural chromosome rearrangements are those expected on the COM model. Further studies are underway to analyze mechanical/mathematical aspects of this model for the origin of crossover/chiasma interference, using string replicas of the homologous chromosomes at the Prophase stage of Meiosis I. The parameters to vary in this type of experiment will include: (1) the mitotic karyotype, i.e. ranked length and centromere index of the chromosomes involved, (2) the specific bivalent/multivalent length and flexibility, dependent on the way this structure is positioned within the nucleus and the size of the respective meiocyte nuclei, (3) the frequency characteristics of the oscillatory movements at respectively the telomeres and the kinetochores.

Item Type: Journal Article
Subjects: Q Science > QH Natural history > QH426 Genetics
Divisions: Faculty of Medicine > Warwick Medical School
Library of Congress Subject Headings (LCSH): Crossing over (Genetics)
Journal or Publication Title: Molecular Cytogenetics
Publisher: BioMed Central Ltd.
ISSN: 1755-8166
Date: 8 April 2011
Volume: Vol.4
Number: No.10
Identification Number: 10.1186/1755-8166-4-10
Status: Peer Reviewed
Access rights to Published version: Open Access
References: 1. Page SL, Hawley RS: Chromosome choreography: the meiotic ballet. Science (New York, NY) 2003, 301:785-789. 2. Marston AL, Amon A: Meiosis: cell-cycle controls shuffle and deal. Nat Rev Mol Cell Biol 2004, 5:983-997. 3. Hultén MA: Meiosis. Encyclopedia of Life Sciences (eLS) Chichester: John Wiley & Sons, Ltd; Published: On Line 15 Sep 2010. 4. Sturtevant AH: A Third Group of Linked Genes in Drosophila ampelophila. Science (New York, NY) 1913, 37:990-992. 5. Muller HJ: The Mechanism of Crossing-Over. The American Naturalist 1916, 50:193-221. 6. Crow EW, Crow JF: 100 years ago: Walter Sutton and the chromosome theory of heredity. Genetics 2002, 160:1-4. 7. Satzinger H: Theodor and Marcella Boveri: chromosomes and cytoplasm in heredity and development. Nature reviews 2008, 9:231-238. 8. Colombo PC, Jones GH: Chiasma interference is blind to centromeres. Heredity 1997, 79(Pt 2):214-227. 9. van Veen JE, Hawley RS: Meiosis: when even two is a crowd. Curr Biol 2003, 13:R831-833. 10. Hillers KJ: Crossover interference. Curr Biol 2004, 14:R1036-1037. 11. Jones GH, Franklin FC: Meiotic crossing-over: obligation and interference. Cell 2006, 126:246-248. 12. Mezard C, Vignard J, Drouaud J, Mercier R: The road to crossovers: plants have their say. Trends Genet 2007, 23:91-99. 13. Martinez-Perez E, Colaiacovo MP: Distribution of meiotic recombination events: talking to your neighbors. Curr Opin Genet Dev 2009, 19:105-112. 14. Berchowitz LE, Copenhaver GP: Genetic interference: don’t stand so close to me. Curr Genomics 2010, 11:91-102. 15. Youds JL, Boulton SJ: The choice in meiosis - defining the factors that influence crossover or non-crossover formation. Journal of cell science 2011, 124:501-513. 16. Tease C, Hultén MA: Meiosis. In Nature Encyclopedia of the Human Genome. Volume 2. Edited by: Cooper DN. London: Nature Publishing Group; 2003:865-873. 17. Hultén MA, Tease C: Genetic mapping: comparison of direct and indirect approaches. In Nature Encyclopedia of the Human Genome. Volume 2. Edited by: Cooper DN. London: Nature Publishing Group; 2003:876-881. 18. Hultén MA, Tease C: Genetic maps: direct meiotic analysis. In Nature Encyclopedia of the Human Genome. Volume 2. Edited by: Cooper DN. London: Nature Publishing Group; 2003:882-887. 19. Hultén MA, Tease C, Lawrie NM: Chiasma-based genetic map of the mouse × chromosome. Chromosoma 1995, 104:223-227. 20. Lawrie NM, Tease C, Hultén MA: Chiasma frequency, distribution and interference maps of mouse autosomes. Chromosoma 1995, 104:308-314. 21. Ferguson-Smith MA: Human chromosomes in meiosis. In Human Genetics, Proceedings of the Firth International Congress of Human Genertics, Paris, 6-11 September, 1971 Edited by: de Grouchy J 195-211. 22. Ferguson-Smith MA: Meiosis in the human male. In Chromosomes Today, Proceedings of the Leiden Chromosome Conference July 15-17, 1974. Edited by: Pearson PL, Lewis KR. published 1976 by John Wiley 33-41. 23. Hultén M, Lindsten J: Cytogenetic aspects of human male meiosis. Advances in human genetics 1973, 4:327-387. 24. McDermott A: The frequency and distribution of chiasmata in man. Annals of human genetics 1973, 37:13-20. 25. Hultén M: Chiasma distribution at diakinesis in the normal human male. Hereditas 1974, 76:55-78. 26. Hultén M, Lindsten J: The behaviour of structural aberrations at male meiosis, Information from man. Human Population Cytogenetics Edinburgh: University of Edinburgh Press; 1970, 24-61, Pfizer Medical Monograph. 27. Laurie DA, Hultén M, Jones GH: Chiasma frequency and distribution in a sample of human males: chromosomes 1, 2, and 9. Cytogenetics and cell genetics 1981, 31:153-166. 28. Laurie DA, Hultén MA: Further studies on bivalent chiasma frequency in human males with normal karyotypes. Annals of human genetics 1985, 49:189-201. 29. Laurie DA, Hultén MA: Further studies on chiasma distribution and interference in the human male. Annals of human genetics 1985, 49:203-214. 30. Hultén MA: The topology of meiotic chiasmata prevents terminalization. Annals of human genetics 1990, 54:307-314. 31. Povey S, Smith M, Haines J, Kwiatkowski D, Fountain J, Bale A, Abbott C, Jackson I, Lawrie M, Hultén M: Report and abstracts of the First International Workshop on Chromosome 9, Held at Girton College Cambridge, UK, 22-24 March, 1992. Annals of human genetics 1992, 56:167-182. 32. Gorlov IP, Borodin PM: [Chiasmata distribution in the normal karyotype of mice]. Genetika 1991, 27:247-251. 33. Dumas D, Britton-Davidian J: Chromosomal rearrangements and evolution of recombination: comparison of chiasma distribution patterns in standard and robertsonian populations of the house mouse. Genetics 2002, 162:1355-1366. 34. Palmer RW, Hultén MA: Chiasma derived genetic maps and recombination fractions: chromosome 13 with reference to the proposed 13q14 retinoblastoma locus. Journal of medical genetics 1982, 19:125-129. 35. Saadallah N, Hultén M: Chiasma distribution, genetic lengths, and recombination fractions: a comparison between chromosomes 15 and 16. Journal of medical genetics 1983, 20:290-299. 36. Darlington C: Chromosome behaviour and structural hybridity in the Tradescantiae II. Journal of Genetics 1929, 21:207-286. 37. de Boer E, Lhuissier FG, Heyting C: Cytological analysis of interference in mouse meiosis. Methods in molecular biology, Clifton, NJ 2009, 558:355-382. 38. Peacock WJ: Replication, recombination, and chiasmata in Goniaea australasiae (Orthoptera:Acrididae). Genetics 1970, 65:593-617. 39. Jones GH: The analysis of exchanges in tritium-labelled meiotic chromosomes. Chromosoma 1971, 34:367-382. 40. Tease C: Cytological detection of crossing-over in BUdR substituted meiotic chromosomes using the fluorescent plus Giemsa technique. Nature 1978, 272:823-824. 41. Hultén MA, Palmer RW, Laurie DA: Chiasma derived genetic maps and recombination fractions: chromosome 1. Annals of human genetics 1982, 46:167-175. 42. Lynn A, Koehler KE, Judis L, Chan ER, Cherry JP, Schwartz S, Seftel A, Hunt PA, Hassold TJ: Covariation of synaptonemal complex length and mammalian meiotic exchange rates. Science (New York, NY) 2002, 296:2222-2225. 43. Kleckner N, Storlazzi A, Zickler D: Coordinate variation in meiotic pachytene SC length and total crossover/chiasma frequency under conditions of constant DNA length. Trends Genet 2003, 19:623-628. 44. Tease C, Hultén MA: Inter-sex variation in synaptonemal complex lengths largely determine the different recombination rates in male and female germ cells. Cytogenetic and genome research 2004, 107:208-215. 45. Petkov PM, Broman KW, Szatkiewicz JP, Paigen K: Crossover interference underlies sex differences in recombination rates. Trends Genet 2007, 23:539-542. 46. Belonogova NM, Borodin PM: Frequency of meiotic recombination in G and R chromosome bands of the common shrew (Sorex araneus). Dokl Biol Sci 2010, 433:268-270. 47. Jeffreys AJ, Kauppi L, Neumann R: Intensely punctate meiotic recombination in the class II region of the major histocompatibility complex. Nature genetics 2001, 29:217-222. 48. Guillon H, de Massy B: An initiation site for meiotic crossing-over and gene conversion in the mouse. Nature genetics 2002, 32:296-299. 49. Myers S, Bottolo L, Freeman C, McVean G, Donnelly P: A fine-scale map of recombination rates and hotspots across the human genome. Science (New York, NY) 2005, 310:321-324. 50. McVean G, Myers S: PRDM9 marks the spot. Nature genetics 2010, 42:821-822. 51. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, Przeworski M, Coop G, de Massy B: PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science, New York, NY 2010, 327:836-840. 52. Parvanov ED, Petkov PM, Paigen K: Prdm9 controls activation of mammalian recombination hotspots. Science, New York, NY 2010, 327:835. 53. Chandley AC, Seuanez H, Fletcher JM: Meiotic behaviour of five human translocation carriers. Cytogenetics and cell genetics 1976, 17:98-111. 54. Chandley AC, Hargreave TB, Fletcher JM: Translocation 21q22q in an infertile human male. Journal of medical genetics 1982, 19:366-369. 55. Chandley AC, Speed RM, McBeath S, Hargreave TB: A human 9;20 reciprocal translocation associated with male infertility analyzed at prophase and metaphase I of meiosis. Cytogenetics and cell genetics 1986, 41:145-153. 56. Egozcue J, Marina S, Templado C: Meiotic behaviour of two human reciprocal translocations. Journal of medical genetics 1981, 18:362-365. 57. Micic MD, Micic SR: Meiotic findings in human reciprocal 1;3 translocation. Human genetics 1981, 57:442-443. 58. Gonzales J, Lesourd S, Dutrillaux B: Mitotic and meiotic analysis of a reciprocal translocation t(Y;3) in an azoospermic male. Human genetics 1981, 57:111-114. 59. Faed MJ, Lamont MA, Baxby K: Cytogenetic and histological studies of testicular biopsies from subfertile men with chromosome anomaly. Journal of medical genetics 1982, 19:49-56. 60. Goldman AS, Hultén MA: Chromosome in situ suppression hybridisation in human male meiosis. Journal of medical genetics 1992, 29:98-102. 61. Laurent C, Chandley AC, Dutrillaux B, Speed RM: The use of surface spreading in the pachytene analysis of a human t (Y;17) reciprocal translocation. Cytogenetics and cell genetics 1982, 33:312-318. 62. Petit P, Unglik A, Fryns JP: Translocation 46, X, t(Y;14)(q122;q111) in a case of sterility in the male. Annales de genetique 1982, 25:63-64. 63. Zuffardi O, Tiepolo L: Frequencies and types of chromosome abnormalities associated with human male infertility. In Genetic Control, Gametic Production and Function. Edited by: PG C, Rubin BL. London: Academic Press; 1982:261-273. Hultén Molecular Cytogenetics 2011, 4:10 http://www.molecularcytogenetics.org/content/4/1/10 64. Palmer RW, Hultén MA: Chiasma-derived genetic lengths and recombination fractions: a reciprocal translocation 46, XY, t(1;22) (q32; q13). Annals of human genetics 1983, 47:299-310. 65. Laurie DA, Palmer RW, Hultén MA: Studies on chiasma frequency and distribution in two fertile men carrying reciprocal translocations; one with a t(9;10) karyotype and one with a t(Y;10) karyotype. Human genetics 1984, 68:235-247. 66. Micic M, Micic S: Meiotic studies in two infertile males with autosomal translocations. Human genetics 1984, 65:308-310. 67. Gabriel-Robez O, Ratomponirina C, Dutrillaux B, Carre-Pigeon F, Rumpler Y: Meiotic association between the XY chromosomes and the autosomal quadrivalent of a reciprocal translocation in two infertile men, 46, XY, t(19;22) and 46, XY, t(17;21). Cytogenetics and cell genetics 1986, 43:154-160. 68. Templado C, Navarro J, Requena R, Benet J, Ballesta F, Egozcue J: Meiotic and sperm chromosome studies in a reciprocal translocation t(1;2)(q32; q36). Human genetics 1990, 84:159-162. 69. Micic M, Nikolis J, Micic S: Clinical and meiotic studies in an infertile man with Y;13 translocation. Human reproduction (Oxford, England) 1992, 7:1118-1120. 70. Goldman AS, Hultén MA: Analysis of chiasma frequency and first meiotic segregation in a human male reciprocal translocation heterozygote, t (1;11)(p36.3;q13.1), using fluorescence in situ hybridisation. Cytogenetics and cell genetics 1993, 63:16-23. 71. Goldman AS, Hultén MA: Meiotic analysis by FISH of a human male 46, XY, t(15;20)(q11.2;q11.2) translocation heterozygote: quadrivalent configuration, orientation and first meiotic segregation. Chromosoma 1993, 102:102-111. 72. Armstrong SJ, Hultén MA: Meiotic segregation analysis by FISH investigations in sperm and spermatocytes of translocation heterozygotes. Eur J Hum Genet 1998, 6:430-431. 73. Armstrong SJ, Goldman AS, Speed RM, Hultén MA: Meiotic studies of a human male carrier of the common translocation, t(11;22), suggests postzygotic selection rather than preferential 3:1 MI segregation as the cause of liveborn offspring with an unbalanced translocation. American journal of human genetics 2000, 67:601-609. 74. Oliver-Bonet M, Navarro J, Codina-Pascual M, Abad C, Guitart M, Egozcue J, Benet J: From spermatocytes to sperm: meiotic behaviour of human male reciprocal translocations. Human reproduction (Oxford, England) 2004, 19:2515-2522. 75. Sarrate Z, Blanco J, Egozcue S, Vidal F, Egozcue J: Identification of meiotic anomalies with multiplex fluorescence in situ hybridization: Preliminary results. Fertility and sterility 2004, 82:712-717. 76. Tease C: Chiasma distributions and chromosome segregation in male and female translocation heterozygous mice analysed using FISH. Chromosoma 1998, 107:549-558. 77. de Boer P: Proximal chiasma localization within an interstitial chromosome segment, a likely correlate of adjacent-2 segregation of translocation causing multivalents in the mouse. Environmental health perspectives 1979, 31:137-140. 78. Wallace BM, Searle JB, Everett CA: Male meiosis and gametogenesis in wild house mice (Mus musculus domesticus) from a chromosomal hybrid zone; a comparison between “simple” Robertsonian heterozygotes and homozygotes. Cytogenetics and cell genetics 1992, 61:211-220. 79. Bidau CJ, Gimenez MD, Palmer CL, Searle JB: The effects of Robertsonian fusions on chiasma frequency and distribution in the house mouse (Mus musculus domesticus) from a hybrid zone in northern Scotland. Heredity 2001, 87:305-313. 80. Torgasheva AA, Borodin PM: Synapsis and recombination in inversion heterozygotes. Biochemical Society transactions 2010, 38:1676-1680. 81. Batanian J, Hultén MA: Electron microscopic investigations of synaptonemal complexes in an infertile human male carrier of a pericentric inversion inv(1)(p32q42). Regular loop formation but defective synapsis including a possible interchromosomal effect. Human genetics 1987, 76:81-89. 82. Winsor EJ, Palmer CG, Ellis PM, Hunter JL, Ferguson-Smith MA: Meiotic analysis of a pericentric inversion, inv(7) (p22q32), in the father of a child with a duplication-deletion of chromosome 7. Cytogenetics and cell genetics 1978, 20:169-184. 83. Gorlov IP, Borodin PM: Recombination in single and double heterozygotes for two partially overlapping inversions in chromosome 1 of the house mouse. Heredity 1995, 75(Pt 2):113-125. 84. Borodin PM, Gorlov IP, Ladygina T: Synaptic interrelationships between the segments of the heteromorphic bivalent in double heterozygotes for paracentric inversions in chromosome 1 of the house mouse. Chromosoma 1992, 101:374-379. 85. Gorlov IP, Ladygina T, Borodin PM: Chiasma distribution in the first bivalent of mice carrying a double insertion of homogeneously-staining regions in homo- and heterozygous states. Heredity 1993, 70(Pt 6):642-647. 86. Barlow AL, Hultén MA: Combined immunocytogenetic and molecular cytogenetic analysis of meiosis I human spermatocytes. Chromosome Res 1996, 4:562-573. 87. Hultén M, Eliasson R, Tillinger KG: Low chiasma count and other meiotic irregularities in two infertile 46, XY men with spermatogenic arrest. Hereditas 1970, 65:285-290. 88. Templado C, Marina S, Egozcue J: Three cases of low chiasma frequency associated with infertility in man. Andrologia 1976, 8:285-289. 89. Chaganti RS, Jhanwar SC, Ehrenbard LT, Kourides IA, Williams JJ: Genetically determined asynapsis, spermatogenic degeneration, and infertility in men. American journal of human genetics 1980, 32:833-848. 90. Micic M, Micic S, Diklic V: Low chiasma frequency as an aetiological factor in male infertility. Clinical genetics 1982, 22:266-269. 91. Marcon E, Moens P: MLH1p and MLH3p localize to precociously induced chiasmata of okadaic-acid-treated mouse spermatocytes. Genetics 2003, 165:2283-2287. 92. Barlow AL, Hultén MA: Crossing over analysis at pachytene in man. Eur J Hum Genet 1998, 6:350-358. 93. Lynn A, Ashley T, Hassold T: Variation in human meiotic recombination. Annual review of genomics and human genetics 2004, 5:317-349. 94. Tease C, Hartshorne GM, Hultén MA: Patterns of meiotic recombination in human fetal oocytes. American journal of human genetics 2002, 70:1469-1479. 95. Gonsalves J, Sun F, Schlegel PN, Turek PJ, Hopps CV, Greene C, Martin RH, Pera RA: Defective recombination in infertile men. Human molecular genetics 2004, 13:2875-2883.
URI: http://wrap.warwick.ac.uk/id/eprint/35177

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