Contrasting behavior of heterochromatic and euchromatic chromosome portions and pericentric genome separation in pre-bouquet spermatocytes of hybrid mice

Chromosoma

Volumn 123, Issue 6, 2014, Pages 609-624

  Scherthan, Harry ^a,b,c   Schöfisch, Karina ^b,e   Dell, Thomas ^c,d   Illner, Doris ^a  

^a Institut fur Radiobiologie der Bundeswehr   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^c France   (Germany)

^d Max Planck Institut für Stoffwechselforschung ^*  (Germany)

^e MAX PLANCK INSTITUTE FOR NEUROLOGICAL RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EUCHROMATIN; HETEROCHROMATIN;

ANIMAL; CENTROMERE; CHEMISTRY; CHROMOSOME; CHROMOSOME INVERSION; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; EUCHROMATIN; FEMALE; FERTILITY; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; GENOME; HETEROCHROMATIN; HYBRIDIZATION; MALE; MEIOSIS; MOUSE; NUCLEOTIDE REPEAT; SPERMATOCYTE; SPERMATOGENESIS; TELOMERE;

ANIMALS; CENTROMERE; CHROMOSOME INVERSION; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CHROMOSOMES, MAMMALIAN; EUCHROMATIN; FEMALE; FERTILITY; GENOME; HETEROCHROMATIN; HYBRIDIZATION, GENETIC; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; MEIOSIS; MICE; REPETITIVE SEQUENCES, NUCLEIC ACID; SPERMATOCYTES; SPERMATOGENESIS; TELOMERE;

EID: 84934295583     PISSN: 00095915     EISSN: 14320886     Source Type: Journal    
DOI: 10.1007/s00412-014-0479-4     Document Type: Article

References (58)

1. Ahmed EA, Agay D, Schrock G, Drouet M, Meineke V, Scherthan H (2012) Persistent DNA damage after high dose in vivo gamma exposure of minipig skin. PLoS One 7:e39521
2. Bardhan A, Chuong H, Dawson DS (2010) Meiotic cohesin promotes pairing of nonhomologous centromeres in early meiotic prophase. Mol Biol Cell 21:1799–1809
3. Baudat F, Manova K, Yuen JP, Jasin M, Keeney S (2000) Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell 6:989–998
4. Bisig CG, Guiraldelli MF, Kouznetsova A, Scherthan H, Hoog C, Dawson DS, Pezza RJ (2012) Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes. PLoS Genet 8:e1002701
5. Boateng KA, Bellani MA, Gregoretti IV, Pratto F, Camerini-OteroRD (2013) Homologous pairing preceding SPO11-mediated double-strandbreaks in mice. Dev Cell 24:196–205
6. Brero A, Easwaran HP, Nowak D, Grunewald I, Cremer T, Leonhardt H, Cardoso MC (2005) Methyl CpG-bindingproteins induce large-scalechromatin reorganization during terminal differentiation. J Cell Biol 169:733–743
7. Buaas FW, Kirsh AL, Sharma M, McLean DJ, Morris JL, Griswold MD, de Rooij DG, Braun RE (2004) Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 36:647–652
8. Chiolo I, Minoda A, Colmenares SU, Polyzos A, Costes SV, Karpen GH (2011) Double-strandbreaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144:732–744
9. Corredor E, Lukaszewski AJ, Pachon P, Allen DC, Naranjo T (2007) Terminal regions of wheat chromosomes select their pairing partners in meiosis. Genetics 177:699–706
10. Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, Sukhwani M, Orwig KE, Wolgemuth DJ, Pandolfi PP (2004) Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 36:653–659
11. De Piccoli G, Torres-Rosell J, Aragón L. (2009) The unnamed complex: what do we know about Smc5-Smc6? Chromosome Res 17:251–263
12. Ding X, Xu R, Yu J, Xu T, Zhuang Y, Han M (2007) SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev Cell 12:863–872
13. Guenatri M, Bailly D, Maison C, Almouzni G (2004) Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J Cell Biol 166:493–505
14. Gómez R, Jordan PW, Viera A, Alsheimer M, Fukuda T, Jessberger R, Llano E, Pendás AM, Handel MA, Suja JA. (2013) Dynamic localization of SMC5/6 complex proteins during mammalian meiosis and mitosis suggests functions in distinct chromosome processes. J Cell Sci 126(Pt 18):4239–4252
15. Horn HF, Kim DI, Wright GD, Wong ES, Stewart CL, Burke B, Roux KJ (2013) A mammalian KASH domain protein coupling meiotic chromosomes to the cytoskeleton. J Cell Biol 202:1023–1039
16. Hsu TC, Cooper JE, Mace ML Jr, Brinkley BR (1971) Arrangement of centromeres in mouse cells. Chromosoma 34:73–87
17. Iannuccelli E, Mompart F, Gellin J, Lahbib-MansaisY, Yerle M, Boudier T (2010) NEMO: a tool for analyzing gene and chromosome territory distributions from 3D-FISHexperiments. Bioinformatics 26:696–697
18. Ishiguro K, Kim J, Fujiyama-NakamuraS, Kato S, Watanabe Y (2011) A new meiosis-specificcohesin complex implicated in the cohesin code for homologous pairing. EMBO Rep 12:267–275
19. Ishiguro K, Kim J, Shibuya H, Hernandez-HernandezA, Suzuki A, Fukagawa T, Shioi G, Kiyonari H, Li XC, Schimenti J, Hoog C, Watanabe Y (2014) Meiosis-specific cohesin mediates homolog recognition in mouse spermatocytes. Genes Dev 28:594–607
20. Jantsch M, Hamilton B, Mayr B, Schweizer D (1990) Meiotic chromosome behaviour reflects levels of sequence divergence in Sus scrofa domestica satellite DNA. Chromosoma 99:330–335
21. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080
22. Kipling D, Ackford HE, Taylor BA, Cooke HJ (1991) Mouse minor satellite DNA genetically maps to the centromere and is physically linked to the proximal telomere. Genomics 11:235–241
23. Klutstein M, Cooper JP (2014) The chromosomal courtship dance — homolog pairing in early meiosis. Curr Opin Cell Biol 26:123–131
24. Lammers JH, Offenberg HH, van M Aalderen, Vink AC, Dietrich AJ, Heyting C (1994) The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes. Mol Cell Biol. 14:1137–1146
25. Lichter P, Cremer T, Borden J, Manuelidis L, Ward DC (1988) Delineation of individual human chromosomes in metaphase and interphase cells by in situ suppression hybridization using recombinant DNA libraries. Hum Genet 80:224–234
26. Lomberk G, Wallrath L, Urrutia R (2006) The heterochromatin protein 1 family. Genome Biol 7:228
27. Mahadevaiah SK, Turner JM, Baudat F, Rogakou EP, de Boer P, Blanco-RodriguezJ, Jasin M, Keeney S, Bonner WM, Burgoyne PS (2001) Recombinational DNA double-strandbreaks in mice precede synapsis. Nat Genet 27:271–276
28. Martinez-Perez E, Shaw P, Reader S, Aragon-AlcaideL, Miller T, Moore G (1999) Homologous chromosome pairing in wheat. J Cell Sci 112(Pt 11):1761–1769
29. Matsuda Y, Hirobe T, Chapman VM (1991) Genetic basis of X-Ychromosome dissociation and male sterility in interspecific hybrids. Proc Natl Acad Sci U S A 88:4850–4854
30. Matsuda Y, Moens PB, Chapman VM (1992) Deficiency of X and Y chromosomal pairing at meiotic prophase in spermatocytes of sterile interspecific hybrids between laboratory mice (Mus domesticus) and Mus spretus. Chromosoma 101:483–492
31. Mayer W, Fundele R, Haaf T (2000) Spatial separation of parental genomes during mouse interspecific (Mus musculus x M. spretus) spermiogenesis. Chromosom Res Int J Mol Supramol Evol Asp Chromosom Biol 8:555–558
32. Moore G, Shaw P (2009) Improving the chances of finding the right partner. Curr Opin Genet Dev 19:99–104
33. Narayanswami S, Doggett NA, Clark LM, Hildebrand CE, Weier HU, Hamkalo BA (1992) Cytological and molecular characterization of centromeres in Mus domesticus and Mus spretus. Mamm Genome Off J Int Mamm Genome Soc 2:186–194
34. Obeso D, Dawson DS (2010) Temporal characterization of homology-independentcentromere coupling in meiotic prophase. PLoS One 5:e10336
35. Obeso D, Pezza RJ, Dawson D (2014) Couples, pairs, and clusters: mechanisms and implications of centromere associations in meiosis. Chromosoma 123:43–55
36. Oka A, Mita A, Takada Y, Koseki H, Shiroishi T (2010) Reproductive isolation in hybrid mice due to spermatogenesis defects at three meiotic stages. Genetics 186:339–351
37. Peters AH, O’Carroll D, Scherthan H, Mechtler K, Sauer S, Schofer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A, Opravil S, Doyle M, Sibilia M, Jenuwein T (2001) Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107:323–337
38. Pinheiro I, Margueron R, Shukeir N, Eisold M, Fritzsch C, Richter FM, Mittler G, Genoud C, Goyama S, Kurokawa M, Son J, Reinberg D, Lachner M, Jenuwein T (2012) Prdm3 and Prdm16 are H3K9me1 methyltransferases required for mammalian heterochromatin integrity. Cell 150:948–960
39. Pinkel D, Landegent J, Collins C, Fuscoe J, Segraves R, Lucas J, Gray J (1988) Fluorescence in situ hybridization with human chromosome-specificlibraries: detection of trisomy 21 and translocations of chromosome 4. Proc Natl Acad Sci U S A 85:9138–9142
40. Rasmussen SW, Holm PB (1980) Mechanics of meiosis. Hereditas 93:187–216
41. Richards DM, Greer E, Martin AC, Moore G, Shaw PJ, Howard M (2012) Quantitative dynamics of telomere bouquet formation. PLoS Comput Biol 8:e1002812
42. Romanienko PJ, Camerini-OteroRD (2000) The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6:975–987
43. Scherthan H (2001) A bouquet makes ends meet. Nat Rev Mol Cell Biol 2:621–627
44. Scherthan H (2007) Telomere attachment and clustering during meiosis. Cell Mol Life Sci 64:117–124
45. Scherthan H, Cremer T (1994) Methodology of non isotopic in situ-hybridization in embedded tissue sections. In: Adolph KW (ed)Methods in molecular genetics, vol 5. Academic, San Diego, pp 223–238
46. Scherthan H, Eils R, Trelles-StickenE, Dietzel S, Cremer T, Walt H, Jauch A (1998) Aspects of three-dimensional chromosome reorganization during the onset of human male meiotic prophase. J Cell Sci 111(Pt 16):2337–2351
47. Scherthan H, Jerratsch M, Dhar S, Wang YA, Goff SP, Pandita TK (2000) Meiotic telomere distribution and Sertoli cell nuclear architecture are altered in Atm-and Atm-p53-deficientmice. Mol Cell Biol 20:7773–7783
48. Scherthan H, Weich S, Schwegler H, Heyting C, Harle M, Cremer T (1996) Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J Cell Biol 134:1109–1125
49. Tachibana M, Nozaki M, Takeda N, Shinkai Y (2007) Functional dynamics of H3K9 methylation during meiotic prophase progression. EMBO J 26:3346–3359
50. Takada Y, Naruse C, Costa Y, Shirakawa T, Tachibana M, Sharif J, Kezuka-ShiotaniF, Kakiuchi D, Masumoto H, Shinkai Y, Ohbo K, Peters AH, Turner JM, Asano M, Koseki H (2011) HP1gamma links histone methylation marks to meiotic synapsis in mice. Development 138:4207–4217
51. Takeo S, Lake CM, Morais-de-SaE, Sunkel CE, Hawley RS (2011) Synaptonemal complex-dependent centromeric clustering and the initiation of synapsis in Drosophila oocytes. Curr Biol 21:1845–1851
52. Tsubouchi T, Roeder GS (2005) A synaptonemal complex protein promotes homology-independentcentromere coupling. Science 308:870–873
53. Verver DE, van Pelt AM, Repping S, Hamer G (2013) Role for rodent Smc6 in pericentromeric heterochromatin domains during spermatogonial differentiation and meiosis. Cell Death Dis 4:e749
54. Vissel B, Choo KH (1989) Mouse major (gamma)satellite DNA is highly conserved and organized into extremely long tandem arrays: implications for recombination between nonhomologous chromosomes. Genomics 5:407–414
55. Wen R, Moore G, Shaw PJ (2012) Centromeres cluster de novo at the beginning of meiosis in Brachypodium distachyon. PLoS One 7:e44681
56. Wong AK, Biddle FG, Rattner JB (1990) The chromosomal distribution of the major and minor satellite is not conserved in the genus Mus. Chromosoma 99:190–195
57. Yoshioka H, McCarrey JR, Yamazaki Y (2009) Dynamic nuclear organization of constitutive heterochromatin during fetal male germ cell development in mice. Biol Reprod 80:804–812
58. Zhang J, Pawlowski WP, Han F (2013) Centromere pairing in early meiotic prophase requires active centromeres and precedes installation of the synaptonemal complex in maize. Plant Cell 25:3900–3909