1932

Abstract

This is a personal historical account of events leading from the earliest success in vertebrate nuclear transfer to the current hope that nuclear reprogramming may facilitate cell replacement therapy. Early morphological evidence in Amphibia for the toti- or multipotentiality of some nuclei from differentiated cells first established the principle of the conservation of the genome during cell differentiation. Molecular markers show that many somatic cell nuclei are reprogrammed to an embryonic pattern of gene expression soon after nuclear transplantation to eggs. The germinal vesicles of oocytes in first meiotic prophase have a direct reprogramming activity on mammalian as well as amphibian nuclei and offer a route to identify nuclear reprogramming molecules. Amphibian eggs and oocytes have a truly remarkable ability to transcribe genes as DNA or nuclei, to translate mRNA, and to modify or localize proteins injected into them. The development of nuclear transplant embryos depends on the ability of cells to interpret small concentration changes of signal factors in the community effect and in morphogen gradients. Many difficulties in a career can be overcome by analyzing in increasing depth the same fundamentally interesting and important problem.

Loading

Article metrics loading...

/content/journals/10.1146/annurev.cellbio.22.090805.140144
2006-11-10
2024-05-24
Loading full text...

Full text loading...

/deliver/fulltext/cb/22/1/annurev.cellbio.22.090805.140144.html?itemId=/content/journals/10.1146/annurev.cellbio.22.090805.140144&mimeType=html&fmt=ahah

Literature Cited

  1. Ashe HL, Briscoe J. 2006. The interpretation of morphogen gradients. Development 133:385–94 [Google Scholar]
  2. Bard JB, French V. 1984. Butterfly wing patterns: how good a determining mechanism is the simple diffusion of a single morphogen. J. Embryol. Exp. Morphol. 84:255–74 [Google Scholar]
  3. Blau HM, Chiu CP, Webster C. 1983. Cytoplasmic activation of human nuclear genes in stable heterocaryons. Cell 32:1171–80 [Google Scholar]
  4. Blow JJ, Laskey RA. 1986. Initiation of DNA replication in nuclei and purified DNA by a cell-free extract of Xenopus eggs. Cell 47:577–87 [Google Scholar]
  5. Boiani M, Eckardt S, Scholer HR, McLaughlin KJ. 2002. Oct4 distribution and level in mouse clones: consequences for pluripotency. Genes Dev. 16:1209–19 [Google Scholar]
  6. Bortvin A, Eggan K, Skaletsky H, Akutsu H, Berry DL. et al. 2003. Incomplete reactivation of Oct4-related genes in mouse embryos cloned from somatic nuclei. Development 130:1673–80 [Google Scholar]
  7. Bourillot PY, Garrett N, Gurdon JB. 2002. A changing morphogen gradient is interpreted by continuous transduction flow. Development 129:2167–80 [Google Scholar]
  8. Boycott AE, Diver C. 1923. On the inheritance of sinistrality in Limnaea peregra. Proc. R. Soc. London Ser. B 95:207–13 [Google Scholar]
  9. Brachet J. 1957. Biochemical Cytology. New York: Academic.516 pp.
  10. Briggs R, King TJ. 1952. Transplantation of living nuclei from blastula cells into enucleated frogs' eggs. Proc. Natl. Acad. Sci. USA 38:455–63 [Google Scholar]
  11. Briggs R, King TJ. 1957. Changes in the nuclei of differentiating endoderm cells as revealed by nuclear transplantation. J. Morphol. 100:269–312 [Google Scholar]
  12. Brink RA. 1960. Paramutation and chromosome organization. Q. Rev. Biol. 35:120–37 [Google Scholar]
  13. Brown DD. 1982. How a simple animal gene works. Harvey Lect. 76:27–44 [Google Scholar]
  14. Brown DD. 1994. Some genes were isolated and their structure studied before the recombinant DNA era. Bioessays 16:139–43 [Google Scholar]
  15. Brown DD. 2004. A tribute to the Xenopus laevis oocyte and egg. J. Biol. Chem. 279:45291–99 [Google Scholar]
  16. Brown DD, Gurdon JB. 1964. Absence of ribosomal RNA synthesis in the anucleolate mutant of Xenopus laevis. Proc. Natl. Acad. Sci. USA 51:139–46 [Google Scholar]
  17. Brown DD, Gurdon JB. 1977. High-fidelity transcription of 5S DNA injected into Xenopus oocytes. Proc. Natl. Acad. Sci. USA 74:2064–68 [Google Scholar]
  18. Brunetti CR, Selegue JE, Monteiro A, French V, Brakefield PM, Carroll SB. 2001. The generation and diversification of butterfly eyespot color patterns. Curr. Biol. 11:1578–85 [Google Scholar]
  19. Buscaglia M, Duboule D. 2002. Developmental biology in Geneva: a three century-long tradition. Int. J. Dev. Biol. 46:5–13 [Google Scholar]
  20. Byrne JA, Simonsson S, Western PS, Gurdon JB. 2003. Nuclei of adult mammalian somatic cells are directly reprogrammed to Oct-4 stem cell gene expression by amphibian oocytes. Curr. Biol. 13:1206–13 [Google Scholar]
  21. Callan HG. 1982. The Croonian Lecture, 1981. Lampbrush chromosomes. Proc. R. Soc. London Ser. B 214:417–48 [Google Scholar]
  22. Callan HG, Lloyd L. 1960. Lampbrush chromosomes of crested newts Triturus cristatus (Laurenti). Philos. Trans. R. Soc. London Ser. B 243:135–219 [Google Scholar]
  23. Campbell KH, McWhir J, Ritchie WA, Wilmut I. 1996. Sheep cloned by nuclear transfer from a cultured cell line. Nature 380:64–66 [Google Scholar]
  24. Coverley D, Laskey RA. 1994. Regulation of eukaryotic DNA replication. Annu. Rev. Biochem. 63:745–76 [Google Scholar]
  25. De Robertis EM, Gurdon JB. 1977. Gene activation in somatic nuclei after injection into amphibian oocytes. Proc. Natl. Acad. Sci. USA 74:2470–74 [Google Scholar]
  26. DiBerardino MA, Hoffner NJ. 1983. Gene reactivation in erythrocytes: nuclear transplantation in oocytes and eggs of Rana. Science 219:862–64 [Google Scholar]
  27. DiBerardino MA, King TJ. 1967. Development and cellular differentiation of neural nuclear-transplants of known karyotype. Dev. Biol. 15:102–28 [Google Scholar]
  28. Drummond DR, Armstrong J, Colman A. 1985. The effect of capping and polyadenylation on the stability, movement and translation of synthetic messenger RNAs in Xenopus oocytes. Nucleic Acids Res. 13:7375–94 [Google Scholar]
  29. Dyson S, Gurdon JB. 1998. The interpretation of position in a morphogen gradient as revealed by occupancy of activin receptors. Cell 93:557–68 [Google Scholar]
  30. Elsdale TR, Fischberg M, Smith S. 1958. A mutation that reduces nucleolar number in Xenopus laevis. Exp. Cell Res. 14:642–43 [Google Scholar]
  31. Gall JG, Murphy C. 1998. Assembly of lampbrush chromosomes from sperm chromatin. Mol. Biol. Cell. 9:733–47 [Google Scholar]
  32. Gao S, Chung YG, Parseghian MH, King GJ, Adashi EY, Latham KE. 2004. Rapid H1 linker histone transitions following fertilization or somatic cell nuclear transfer: evidence for a uniform developmental program in mice. Dev. Biol. 266:62–75 [Google Scholar]
  33. Gonda K, Fowler J, Katoku-Kikyo N, Haroldson J, Wudel J, Kikyo N. 2003. Reversible disassembly of somatic nucleoli by the germ cell proteins FRGY2a and FRGY2b. Nat. Cell Biol. 5:205–10 [Google Scholar]
  34. Graham CF, Arms K, Gurdon JB. 1966. The induction of DNA synthesis by frog egg cytoplasm. Dev. Biol. 14:349–81 [Google Scholar]
  35. Green JBA, Smith JC. 1990. Graded changes in dose of a Xenopus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature 347:391–94 [Google Scholar]
  36. Gurdon JB, Harger P, Mitchell A, Lemaire P. 1994. Activin signalling and the spatial control of response to embryonic induction. Nature 371:487–92 [Google Scholar]
  37. Gurdon JB. 1962a. Adult frogs derived from the nuclei of single somatic cells. Dev. Biol. 4:256–73 [Google Scholar]
  38. Gurdon JB. 1962b. The developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles. J. Embryol. Exp. Morphol. 10:622–40 [Google Scholar]
  39. Gurdon JB. 1986. Nuclear transplantation in eggs and oocytes. J. Cell Sci. Suppl. 4:287–318 [Google Scholar]
  40. Gurdon JB. 1988. A community effect in animal development. Nature 336:772–74 [Google Scholar]
  41. Gurdon JB. 2005. Sinistral snails and gentlemen scientists. Cell 123:751–53 [Google Scholar]
  42. Gurdon JB, Birnstiel ML, Speight VA. 1969. The replication of purified DNA introduced into living egg cytoplasm. Biochim. Biophys. Acta 174:614–28 [Google Scholar]
  43. Gurdon JB, Bourillot PY. 2001. Morphogen gradient interpretation. Nature 413:797–803 [Google Scholar]
  44. Gurdon JB, Brennan S, Fairman S, Mohun TJ. 1984. Transcription of muscle-specific actin genes in early Xenopus development: nuclear transplantation and cell dissociation. Cell 38:691–700 [Google Scholar]
  45. Gurdon JB, Elsdale TR, Fischberg M. 1958. Sexually mature individuals of Xenopus laevis from the transplantation of single somatic nuclei. Nature 182:64–65 [Google Scholar]
  46. Gurdon JB, Hopwood N. 2000. The introduction of Xenopus laevis into developmental biology: of empire, pregnancy testing and ribosomal genes. Int. J. Dev. Biol. 44:43–50 [Google Scholar]
  47. Gurdon JB, Lane CD, Woodland HR, Marbaix G. 1971. The use of frog eggs and oocytes for the study of messenger RNA and its translation in living cells. Nature 233:177–82 [Google Scholar]
  48. Gurdon JB, Laskey RA, Reeves OR. 1975. The developmental capacity of nuclei transplanted from keratinized skin cells of adult frogs. J. Embryol. Exp. Morphol. 34:93–112 [Google Scholar]
  49. Gurdon JB, Melton DA. 1981. Gene transfer in amphibian eggs and oocytes. Annu. Rev. Genet. 15:189–218 [Google Scholar]
  50. Gurdon JB, Tiller E, Roberts J, Kato K. 1993. A community effect in muscle development. Curr. Biol. 3:1–11 [Google Scholar]
  51. Harris H. 1970. Cell Fusion Oxford: Clarendon.108 pp.
  52. Hochedlinger K, Jaenisch R. 2002. Monoclonal mice generated by nuclear transfer from mature B and T donor cells. Nature 415:1035–38 [Google Scholar]
  53. Humpherys D, Eggan K, Akutsu H, Friedman A, Hochedlinger K. et al. 2002. Abnormal gene expression in cloned mice derived from embryonic stem cell and cumulus cell nuclei. Proc. Natl. Acad. Sci. USA 99:12889–94 [Google Scholar]
  54. Jullien J, Gurdon J. 2005. Morphogen gradient interpretation by a regulated trafficking step during ligand-receptor transduction. Genes Dev. 19:2682–94 [Google Scholar]
  55. Kato K, Gurdon JB. 1993. Single-cell transplantation determines the time when Xenopus muscle precursor cells acquire a capacity for autonomous differentiation. Proc. Natl. Acad. Sci. USA 90:1310–14 [Google Scholar]
  56. Kikyo N, Wade PA, Guschin D, Ge H, Wolffe AP. 2000. Active remodeling of somatic nuclei in egg cytoplasm by the nucleosomal ATPase ISWI. Science 289:2360–62 [Google Scholar]
  57. Kikyo N, Wolffe AP. 2000. Reprogramming nuclei: insights from cloning, nuclear transfer and heterokaryons. J. Cell Sci. 113:(Pt. 1)11–20 [Google Scholar]
  58. Kimura H, Tada M, Nakatsuji N, Tada T. 2004. Histone code modifications on pluripotential nuclei of reprogrammed somatic cells. Mol. Cell Biol. 24:5710–20 [Google Scholar]
  59. Krieg PA, Melton DA. 1984. Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res. 12:7057–70 [Google Scholar]
  60. Lane CD, Colman A, Mohun T, Morser J, Champion J. et al. 1980. The Xenopus oocyte as a surrogate secretory system. The specificity of protein export. Eur. J. Biochem. 111:225–35 [Google Scholar]
  61. Lane CD, Marbaix G, Gurdon JB. 1971. Rabbit hemoglobin synthesis in frog cells: the translation of reticulocyte 9 S RNA in frog oocytes. J. Mol. Biol. 61:73–91 [Google Scholar]
  62. Laskey RA, Gurdon JB. 1970. Genetic content of adult somatic cells tested by nuclear transplantation from cultured cells. Nature 228:1332–34 [Google Scholar]
  63. Lemaitre JM, Danis E, Pasero P, Vassetzky Y, Mechali M. 2005. Mitotic remodeling of the replicon and chromosome structure. Cell 123:787–801 [Google Scholar]
  64. Levi-Montalcini R. 1987. The nerve growth factor: thirty-five years later. EMBO J. 6:1145–54 [Google Scholar]
  65. Martinez Arias A. 2003. Wnts as morphogens? The view from the wing of Drosophila. Nat. Rev. Mol. Cell Biol. 4:321–25 [Google Scholar]
  66. Mertz JE, Gurdon JB. 1977. Purified DNAs are transcribed after microinjection into Xenopus oocytes. Proc. Natl. Acad. Sci. USA 74:1502–6 [Google Scholar]
  67. Mohun TJ, Brennan S, Dathan N, Fairman S, Gurdon JB. 1984. Cell type-specific activation of actin genes in the early amphibian embryo. Nature 311:716–21 [Google Scholar]
  68. Monteiro A, French V, Smit G, Brakefield PM, Metz JA. 2001. Butterfly eyespot patterns: evidence for specification by a morphogen diffusion gradient. Acta Biotheor 49:77–88 [Google Scholar]
  69. Morales A, Aleu J, Ivorra I, Ferragut JA, Gonzalez-Ros JM, Miledi R. 1995. Incorporation of reconstituted acetylcholine receptors from Torpedo into the Xenopus oocyte membrane. Proc. Natl. Acad. Sci. USA 92:8468–72 [Google Scholar]
  70. Nakamura O, Toivonen S. eds 1978. Organizer: A Milestone of a Half-Century from Spemann Amsterdam: Elsevier/North-Holland Biomed. Press.379 pp.
  71. Needham J. 1942. Biochemistry and Morphogenesis, Vols. 1–3 Cambridge, UK: Cambridge Univ. Press.2021 pp. [Google Scholar]
  72. Ng RK, Gurdon JB. 2005. Epigenetic memory of active gene transcription is inherited through somatic cell nuclear transfer. Proc. Natl. Acad. Sci. USA 102:1957–62 [Google Scholar]
  73. Nijhout HF. 1991. The development and evolution of butterfly wing patterns. Washington, D.C.: Smithsonian Instit.
  74. Okada TS. 1991. Transdifferentiation: Flexibility in Cell Differentiation Oxford, UK: Oxford Univ. Press.238 pp.
  75. Piepenburg O, Grimmer D, Williams PH, Smith JC. 2004. Activin redux: specification of mesodermal pattern in Xenopus by graded concentrations of endogenous activin B. Development 131:4977–86 [Google Scholar]
  76. Rideout WM, Eggan K, Jaenisch R. 2001. Nuclear cloning and epigenetic reprogramming of the genome. Science 293:1093–98 [Google Scholar]
  77. Rideout WM, Hochedlinger K, Kyba M, Daley GQ, Jaenisch R. 2002. Correction of a genetic defect by nuclear transplantation and combined cell and gene therapy. Cell 109:17–27 [Google Scholar]
  78. Rorvik DM. 1978. In His Image: The Cloning of a Man Philadelphia: JV Lippincott.207 pp.
  79. Saxén L, Toivonen S. 1962. Primary Embryonic Induction London: Logo.271 pp.
  80. Simonsson S, Gurdon J. 2004. DNA demethylation is necessary for the epigenetic reprogramming of somatic cell nuclei. Nat. Cell Biol. 6:984–90 [Google Scholar]
  81. Smith JC, Price BMJ, Van Nimmen K, Huylebroeck D. 1990. Identification of a potent Xenopus mesoderm-inducing factor as a homolog of activin A. Nature 345:729–31 [Google Scholar]
  82. Soloviev MM, Barnard EA. 1997. Xenopus oocytes express a unitary glutamate receptor endogenously. J. Mol. Biol. 273:14–18 [Google Scholar]
  83. Sonneborn TM. 1977. Genetics of cellular differentiation: stable nuclear differentiation in eucaryotic unicells. Annu. Rev. Genet. 11:349–67 [Google Scholar]
  84. Spemann H. 1928. Die Entwicklung seitlicher und dorso-ventraler Keimhalften bei verzogerter Kernversogung. Z. Wiss. Zool 132:105–34 [Google Scholar]
  85. Standley HJ, Zorn AM, Gurdon JB. 2001. eFGF and its mode of action in the community effect during Xenopus myogenesis. Development 128:1347–57 [Google Scholar]
  86. Tada M, Tada T, Lefebvre L, Barton SC, Surani MA. 1997. Embryonic germ cells induce epigenetic reprogramming of somatic nucleus in hybrid cells. EMBO J. 16:6510–20 [Google Scholar]
  87. Teranishi T, Tanaka M, Kimoto S, Ono Y, Miyakoshi K. et al. 2004. Rapid replacement of somatic linker histones with the oocyte-specific linker histone H1foo in nuclear transfer. Dev. Biol. 266:76–86 [Google Scholar]
  88. Tsunoda Y, Kato Y. 2002. Donor cell type and cloning efficiency in mammals. In Principles of Cloning ed. JB Cibelli, RP Lanza, KH Campbell, MD West pp. 267–77 San Diego: Academic [Google Scholar]
  89. Waddington CH, Needham J, Brachet J. 1936. Studies on the nature of the amphibian organization center. III. The activation of the evocator. Proc. R. Soc. London Ser. B 120:173–98 [Google Scholar]
  90. Wade PA, Kikyo N. 2002. Chromatin remodeling in nuclear cloning. Eur. J. Biochem. 269:2284–87 [Google Scholar]
  91. Wakayama T, Perry AC. 2002. Cloning of mice. In Principles of Cloning ed. JB Cibelli, RP Lanza, KH Campbell, MD West pp. 301–41 San Diego: Academic [Google Scholar]
  92. Wallace H, Birnstiel ML. 1966. Ribosomal cistrons and the nucleolar organizer. Biochim. Biophys. Acta 114:296–310 [Google Scholar]
  93. Weismann A. 1892. Das Keimplasma, eine Theorie der Vererbung. In The Germ-Plasm: A Theory of Heredity ed. WN Parker, H Ronnfeldt. London: Walter Scott [Google Scholar]
  94. Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KH. 1997. Viable offspring derived from fetal and adult mammalian cells. Nature 385:810–13 [Google Scholar]
  95. Wilson EB. 1925. The Cell in Development and Heredity New York: Macmillan.1232 pp.
  96. Woodland HR, Gurdon JB, Lingrel JB. 1974. The translation of mammalian globin mRNA injected into fertilized eggs of Xenopus laevis. II. The distribution of globin synthesis in different tissues. Dev. Biol. 39:134–40 [Google Scholar]
/content/journals/10.1146/annurev.cellbio.22.090805.140144
Loading
/content/journals/10.1146/annurev.cellbio.22.090805.140144
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error