Mammalian Genome

, Volume 17, Issue 12, pp 1183–1192 | Cite as

Reciprocal chromosome painting between three laboratory rodent species

  • Svetlana A. Romanenko
  • Polina L. Perelman
  • Natalya A. Serdukova
  • Vladimir A. Trifonov
  • Larisa S. Biltueva
  • Jinhuan Wang
  • Tangliang Li
  • Wenhui Nie
  • Patricia C.M. O’Brien
  • Vitaly T. Volobouev
  • Roscoe Stanyon
  • Malcolm A. Ferguson-Smith
  • Fengtang Yang
  • Alexander S. Graphodatsky
Article

Abstract

The laboratory mouse (Mus musculus, 2n = 40), the Chinese hamster (Cricetulus griseus, 2n = 22), and the golden (Syrian) hamster (Mesocricetus auratus, 2n = 44) are common laboratory animals, extensively used in biomedical research. In contrast with the mouse genome, which was sequenced and well characterized, the hamster species has been set aside. We constructed a chromosome paint set for the golden hamster, which for the first time allowed us to perform multidirectional chromosome painting between the golden hamster and the mouse and between the two species of hamster. From these data we constructed a detailed comparative chromosome map of the laboratory mouse and the two hamster species. The golden hamster painting probes revealed 25 autosomal segments in the Chinese hamster and 43 in the mouse. Using the Chinese hamster probes, 23 conserved segments were found in the golden hamster karyotype. The mouse probes revealed 42 conserved autosomal segments in the golden hamster karyotype. The two largest chromosomes of the Chinese hamster (1 and 2) are homologous to seven and five chromosomes of the golden hamster, respectively. The golden hamster karyotype can be transformed into the Chinese hamster karyotype by 15 fusions and 3 fissions. Previous reconstructions of the ancestral murid karyotype proposed diploid numbers from 2n = 52 to 2n = 54. By integrating the new multidirectional chromosome painting data presented here with previous comparative genomics data, we can propose that syntenies to mouse Chrs 6 and 16 were both present and to hypothesize a diploid number of 2n = 48 for the ancestral Murinae/Cricetinae karyotype.

References

  1. Cavagna P, Stone G, Stanyon R (2002) Black rat (Rattus rattus) genomic variability characterized by chromosome painting. Mamm Genome 13, 157–163PubMedGoogle Scholar
  2. Dawson WD, Young SR, Wang Z, Liu LW, Greenbaum IF, et al. (1999) Mus and Peromyscus chromosome homology established by FISH with three mouse paint probes. Mamm Genome 10, 730–733CrossRefPubMedGoogle Scholar
  3. Engelbrecht A, Dobigny G, Robinson TJ (2006) Further insights into the ancestral murine karyotype: the contribution of the Otomys-Mus comparison using chromosome painting. Cytogenet Genome Res 112, 126–130CrossRefPubMedGoogle Scholar
  4. Ferguson-Smith MA (1997) Genetic analysis by chromosome sorting and painting: phylogenetic and diagnostic applications. Eur J Human Genet 5, 253–265Google Scholar
  5. Gamperl R, Vistorin G, Rosenkranz W (1978) Comparison of chromosome banding patterns in five members of Cricetinae with comments on possible relationships. Caryologia 31, 343–353Google Scholar
  6. Graphodatsky AS (1989) Conserved and variable elements of mammalian chromosomes. In Cytogenetics of Animals, Halnan C, (ed.) (Oxon: CAB International Press), pp 95–123Google Scholar
  7. Graphodatsky AS, Sablina OV, Meyer MN, Malikov VG, Isakova EA, et al. (2000) Comparative cytogenetics of hamsters of the genus Calomyscus. Cytogenet Cell Genet 88, 296–304CrossRefPubMedGoogle Scholar
  8. Graphodatsky AS, Yang F, O’Brien PC, Perelman P, Milne BS., et al. (2001) Phylogenetic implications of the 38 putative ancestral chromosome segments for four canid species. Cytogenet Cell Genet 92, 243–247CrossRefPubMedGoogle Scholar
  9. Guilly M-N, Fouchet P, de Chamisso P, Schmitz A, Dutrillaux B (1999) Comparative karyotype of rat and mouse using bidirectional chromosome painting. Chromosome Res 7, 213–221CrossRefPubMedGoogle Scholar
  10. Guilly M-N, Dano L, de Chamisso P, Fouchet P, Dutrillaux B, et al. (2001) Comparative karyotype using bidirectional chromosome painting: how and why? Meth Cell Sci 23, 163–170CrossRefGoogle Scholar
  11. Li S, Pathak S, Hsu TC (1982) High resolution G-banding patterns of Syrian hamster chromosomes. Cytogenet Cell Genet 33, 295–302PubMedGoogle Scholar
  12. Matsubara K, Nishida-Umehara C, Kuroiwa A, Tsuchiya K, Matsuda Y (2003) Identification of chromosome rearrangements between the laboratory mouse (Mus musculus) and the Indian spiny mouse (Mus platythrix) by comparative FISH analysis. Chromosome Res 11, 57–64CrossRefPubMedGoogle Scholar
  13. Matsubara K, Nishida-Umehara C, Tsuchiya K, Nukaya D, Matsuda Y (2004) Karyotypic evolution of Apodemus (Muridae, Rodentia) inferred from comparative FISH analyses. Chromosome Res 12, 383–395CrossRefPubMedGoogle Scholar
  14. Murphy WJ, Stanyon R, O’Brien SJ (2001) Evolution of mammalian genome organization inferred from comparative gene mapping. Genome Biol 2(6), 1–8CrossRefGoogle Scholar
  15. Murphy WJ, Larkin DM, Evert-van der Wind A, Bourque G, Tesler G, et al. (2005) Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science 309, 613–617CrossRefPubMedGoogle Scholar
  16. Pavia RA, Smith LW, Goldenberg DM (1977) An analysis of the G-banded chromosomes of the golden hamster. Int J Cancer 20, 460–465PubMedGoogle Scholar
  17. Popescu NC, DiPaolo JA (1972) Identification of Syrian hamster chromosomes by acetic-saline-Giemsa (ASG) and trypsin techniques. Cytogentics 11, 500–507Google Scholar
  18. Radjabli SI, Sablina OV, Graphodatsky AS (2006) Selected karyotypes. In ATLAS of Mammalian Karyotypes, O’Brien SJ, Nash WG, Menninger JC, (eds.) (New York: John Wiley & Sons), pp 305, 329–352Google Scholar
  19. Rambau RV, Robinson TJ (2003) Chromosome painting in the African four-striped mouse Rhabdomys pumilio: detection of possible murid specific contiguous segment combination. Chromosome Res 11, 91–98CrossRefPubMedGoogle Scholar
  20. Scherthan H, Cremer T, Arnason U, Weier HU, Lima-de-Faria A, et al. (1994) Comparative chromosome painting discloses homologous segments in distantly related mammals. Nat Genet 6(4), 342–347CrossRefPubMedGoogle Scholar
  21. Seabright M (1971) A rapid banding technique for human chromosomes. Lancet 2, 971–972CrossRefPubMedGoogle Scholar
  22. Stanyon R, Yang F, Cavagna P, O’Brien PC, Bagga M, et al. (1999) Reciprocal chromosome painting shows that genomic rearrangement between rat and mouse proceeds ten times faster than between humans and cats. Cytogenet Cell Genet 84(3–4), 150–155CrossRefPubMedGoogle Scholar
  23. Stanyon R, Yang F, Morescalchi AM, Galleni L (2004) Chromosome painting in the long-tailed field mouse provides insights into the ancestral murid karyotype. Cytogenet Genome Res 105, 406–411CrossRefPubMedGoogle Scholar
  24. Steppan S, Adkins R, Anderson J (2004) Phylogeny and divergence-data estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Syst Biol 53(4), 533–553CrossRefPubMedGoogle Scholar
  25. Telenius H, Pelmear AH, Tunnacliffe A, Carter NP, Behmel A, et al. (1992) Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes. Genes Chromosomes Cancer 4, 226–257Google Scholar
  26. Trifonov VA, Perelman PL, Kawada SI, Iwasa MA, Oda SI, et al. (2002) Complex structure of B-chromosomes in two mammalian species: Apodemus peninsulae (Rodentia) and Nyctereutes procyonoides (Carnivora) revealed by microdissection. Chromosome Res 10(2), 109–116CrossRefPubMedGoogle Scholar
  27. Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, et al. (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520–562CrossRefPubMedGoogle Scholar
  28. Yang F, Carter NP, Shi, Ferguson-Smith MA (1995) A comparative study of karyotypes of muntjacs by chromosome painting. Chromosoma 103, 642–652Google Scholar
  29. Yang F, O’Brien PC, Milne BS, Graphodatsky AS, Solanky N, et al. (1999) A complete comparative chromosome map for the dog, red fox, and human and its integration with canine genetic maps. Genomics 62, 189–202CrossRefPubMedGoogle Scholar
  30. Yang F, O’Brien PC, Ferguson-Smith MA (2000) Comparative chromosome map of the laboratory mouse and Chinese hamster defined by reciprocal chromosome painting. Chromosome Res 8, 219–227CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Svetlana A. Romanenko
    • 1
  • Polina L. Perelman
    • 1
  • Natalya A. Serdukova
    • 1
  • Vladimir A. Trifonov
    • 1
    • 2
  • Larisa S. Biltueva
    • 1
  • Jinhuan Wang
    • 3
  • Tangliang Li
    • 3
  • Wenhui Nie
    • 3
  • Patricia C.M. O’Brien
    • 2
  • Vitaly T. Volobouev
    • 4
  • Roscoe Stanyon
    • 5
  • Malcolm A. Ferguson-Smith
    • 2
  • Fengtang Yang
    • 3
    • 6
  • Alexander S. Graphodatsky
    • 1
    • 7
  1. 1.Institute of Cytology and Genetics, Siberian BranchRussian Academy of SciencesNovosibirskRussia
  2. 2.Centre for Veterinary Science, Department of Veterinary MedicineUniversity of CambridgeCambridgeUnited Kingdom
  3. 3.Key Laboratory of Cellular & Molecular EvolutionThe Chinese Academy of SciencesKunmingPeople’s Republic of China
  4. 4.Museum National d’Histoire Naturelle, Origine, Structure et Evolution de la BiodiversiteParisFrance
  5. 5.Department of Animal Biology and GeneticsUniversity of FlorenceFlorenceItaly
  6. 6.The Wellcome Trust Sanger InstituteHinxtonUnited Kingdom
  7. 7.Institute of Cytology and Genetics, SB RASNovosibirskRussia

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