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Chromosoma

, Volume 100, Issue 6, pp 410–418 | Cite as

Scanning electron microscopy of mammalian chromosomes from prophase to telophase

  • A. T. Sumner
Article

Abstract

Changes in the morphology of human and murine chromosomes during the different stages of mitosis have been examined by scanning electron microscopy. Two important findings have emerged from this study. The first is that prophase chromosomes do not become split into pairs of chromatids until late prophase or early metaphase. This entails two distinct processes of condensation, the earlier one starting as condensations of chromosomes into chromomeres which then fuse to form a cylindrical body. After this cylindrical body has split in two longitudinally, further condensation occurs by mechanisms that probably include coiling of the chromatids as well as other processes. The second finding is that the centromeric heterochromatin does not split in two at the same time as the rest of the chromosome, but remains undivided until anaphase. It is proposed that the function of centromeric heterochromatin is to hold the chromatids together until anaphase, when they are separated by the concerted action of topoisomerase II acting on numerous similar sites provided by the repetitive nature of the satellite DNA in the heterochromatin. A lower limit to the size of blocks of centromeric heterochromatin is placed by the need for adequate mechanical strength to hold the chromatids together, and a higher limit by the necessity for rapid splitting of the heterochromatin at anaphase. Beyond these limits malsegregation will occur, leading to aneuploidy. Because the centromere remains undivided until anaphase, it cannot undergo the later stage of condensation found in the chromosome arms after separation into chromatids, and therefore the centromere remains as a constriction.

Keywords

Electron Microscopy Scan Electron Microscopy Lower Limit Developmental Biology Mechanical Strength 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Allshire RC, Cranston G, Gosden JR, Maule JC, Hastie ND, Fantes PA (1987) A fission yeast chromosome can replicate autonomously in mouse cells. Cell 50: 391–403Google Scholar
  2. Bostock CJ, Summer AT (1978) The eukaryotic chromosome. North Holland, AmsterdamGoogle Scholar
  3. Caserta M, Amadei A, diMauro E, Camilloni G (1989) In vitro preferential topoisomerization of bent DNA. Nucleic Acids Res 17: 8463–8474Google Scholar
  4. Cooke CA, Heck MMS, Earnshaw WC (1987) The inner centromere protein (INCENP) antigens; movement from inner centromere to midbody during mitosis. J Cell Biol 105: 2053–2067Google Scholar
  5. Darlington CD (1965) Cytology J & A Churchill, LondonGoogle Scholar
  6. Eigsti OJ, Dustin P (1955) Colchicine—in agriculture, biology and chemistry. Iowa State College Press, Ames, Ch. 2Google Scholar
  7. Flemming W (1880) Beitrag zur Kenntnis der Zelle und ihrer Lebenserscheinungen, Teil II. Archiv Mikrosk Anat 18: 151–259 (English translation in J Cell Biol 25: 1–69, 1965)Google Scholar
  8. German J (1979) Roberts' syndrome. I. Cytological evidence for a disturbance in chromatid pairing. Clin Genet 16: 441–447Google Scholar
  9. Golomb HM, Bahr GF (1974) Human chromatin from interphase to metaphase. Exp Cell Res 84: 79–87Google Scholar
  10. Harrison CJ, Britch M, Allen TD, Harris R (1981) Scanning electron microscopy of the G-banded human karyotype. Exp Cell Res 134: 141–153Google Scholar
  11. Harrison CJ, Jack EM, Allen TD (1987) Light and scanning electron microscopy of the same metaphase chromosomes. In: Hayat MA (ed) Correlative microscopy in biology: instrumentation and methods. Academic Press, New York, pp 189–248Google Scholar
  12. Heslop-Harrison JS, Leitch AR, Schwarzacher T, Smith JB, Atkinson MD, Bennett MD (1989) The volumes and morphology of human chromosomes in mitotic reconstructions. Hum Genet 84: 27–34Google Scholar
  13. Holm C, Stearns T, Botstein D (1989) DNA topoisomerase II must act at mitosis to prevent nondisjunction and chromosome breakage. Mol Cell Biol 9: 159–168Google Scholar
  14. John B (1988) The biology of heterochromatin. In: Verma RS (ed) Heterochromatin. Cambridge University Press, Cambridge, pp 1–147Google Scholar
  15. John B, Miklos GLG (1979) Functional aspects of satellite DNA and heterochromatin. Int Rev Cytol 58: 1–114Google Scholar
  16. Lica LM, Narayanswami S, Hamkalo BA (1986) Mouse satellite DNA, centromere structure, and sister chromatid pairing. J Cell Biol 103: 1145–1151Google Scholar
  17. Madan K, Lindhout D, Palan A (1987) Premature centromere division (PCD): a dominantly inherited cytogenetic anomaly. Hum Genet 77: 193–196Google Scholar
  18. Manton I (1950) The spiral structure of chromosomes. Biol Rev 25: 486–508Google Scholar
  19. Martinez-Balbas A, Rodriguez-Campos A, Garcia-Ramirez M, Sainz J, Carrera P, Aymami J, Azorin F (1990) Satellite DNAs contain sequences that induce curvature. Biochemistry 29: 2342–2348Google Scholar
  20. Mazia D (1961) Mitosis and the physiology of cell division. In: Brachet J, Mirsky AE (eds) the cell, vol III. Academic Press, New York, pp 77–412Google Scholar
  21. Mullinger AM, Johnson RT (1983) Units of chromosome replication and packing. J Cell Sci 64: 179–193Google Scholar
  22. Mullinger AM, Johnson RT (1987) Disassembly of the mammalian metaphase chromosome into its subunits: studies with ultraviolet light and repair synthesis inhibitors. J Cell Sci 87: 55–69Google Scholar
  23. Ohnuki Y (1968) Structure of chromosomes. I. Morphological studies of the spiral structure of human somatic chromosomes. Chromosoma 25: 402–428Google Scholar
  24. Radic MZ, Lundgren K, Hamkalo B (1987) Curvature of mouse satellite DNA and condensation of heterochromatin. Cell 50: 1101–1108Google Scholar
  25. Rieger R, Michaelis A, Green MM (1968) A glossary of genetics and cytogenetics, 3rd edn. George Allen & Unwin, London, Springer, BerlinGoogle Scholar
  26. Röhme D, Heneen WK (1982) Banding patterns in prematurely condensed chromosomes and the underlying structure of the chromosome. In: Rao PN, Johnson RT, Sperling K (eds) Premature chromosome condensation. Academic Press, New York, pp 131–157Google Scholar
  27. Rudd NL, Teshima IE, Martin SH, Sisken JE, Weksberg R (1983) A dominantly inherited cytogenetic anomaly: a possible cell division mutant. Hum Genet 65: 117–122Google Scholar
  28. Shen CC, Shen C-KJ (1990) Specificity and flexibility of the recognition of DNA helical structure by eukaryotic topoisomerase I. J Mol Biol 212: 67–78Google Scholar
  29. Sorsa V (1973) Condensation of chromosomes during mitotic prophase. Hereditas 75: 101–108Google Scholar
  30. Spitzner JR, Muller MT (1988) A consensus sequence for cleavage by vertebrate DNA topoisomerase II. Nucleic Acids Res 16: 5533–5556Google Scholar
  31. Sumner AT, Ross A (1989) Factors affecting preparation of chromosomes for scanning electron microscopy using osmium impregnation. Scanning Microsc [Suppl] 3: 87–99Google Scholar
  32. Swanson CP (1963) Cytology and cytogenetics. Macmillan, LondonGoogle Scholar
  33. Tomkins D, Hunter A, Roberts M (1979) Cytogenetic findings in Roberts-SC phocomelia syndrome(s). Am J Med Genet 4: 17–26Google Scholar
  34. Vig BK (1987) Sequence of centromere separation: a possible role for repetitive DNA. Mutagenesis. 2: 155–159Google Scholar
  35. Walker PMB (1971) “Repetitive” DNA in higher organisms. Prog Biophys Mol Biol 23: 145–190Google Scholar
  36. White MJD (1961) The chromosomes, 5th edn. Methuen, LondonGoogle Scholar
  37. Yanagida M (1989) Gene products required for chromosome separation. J Cell Sci [Suppl] 12: 213–229Google Scholar
  38. Yunis JJ, Bahr GF (1979) Chromatin fibre organisation of human interphase and prophase chromosomes. Exp Cell Res 122: 63–72Google Scholar
  39. Yunis JJ, Yasmineh WG (1971) Heterochromatin, satellite DNA, and cell function. Science 174: 1200–1209Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • A. T. Sumner
    • 1
  1. 1.MRC Human Genetics UnitWestern General HospitalEdinburghUK

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