Cytoplasmic Impact on Cross-Genus Cloned Fish Derived from Transgenic Common Carp (Cyprinus carpio) Nuclei and Goldfish (Carassius auratus) Enucleated Eggs1

Abstract In previous studies of nuclear transplantation, most cloned animals were obtained by intraspecies nuclear transfer and are phenotypically identical to their nuclear donors; furthermore, there was no further report on successful fish cloning since the report of cloned zebrafish. Here we report the production of seven cross-genus cloned fish by transferring nuclei from transgenic common carp into enucleated eggs of goldfish. Nuclear genomes of the cloned fish were exclusively derived from the nuclear donor species, common carp, whereas the mitochondrial DNA from the donor carp gradually disappeared during the development of nuclear transfer (NT) embryos. The somite development process and somite number of nuclear transplants were consistent with the recipient species, goldfish, rather than the nuclear donor species, common carp. This resulted in a long-lasting effect on the vertebral numbers of the cloned fish, which belonged to the range of goldfish. These demonstrate that fish egg cytoplasm not only can support the development driven by transplanted nuclei from a distantly related species at the genus scale but also can modulate development of the nuclear transplants.

[1]  B. Barboni,et al.  Genetic rescue of an endangered mammal by cross-species nuclear transfer using post-mortem somatic cells , 2001, Nature Biotechnology.

[2]  Yaping Wang,et al.  Sequences of Transgene Insertion Sites in Transgenic F4 Common Carp , 2004, Transgenic Research.

[3]  P. Bănărescu,et al.  The Cyprinid Fishes of China, Vol. I , 1967 .

[4]  P K Maini,et al.  Clock and induction model for somitogenesis , 2000, Developmental dynamics : an official publication of the American Association of Anatomists.

[5]  Zuo-yan Zhu,et al.  Characterization of transgene integration pattern in F4 hGH-transgenic common carp (Cyprinus carpio L.) , 2005, Cell Research.

[6]  P. Lemaire,et al.  Vertebrate embryonic inductions. , 1994, BioEssays : news and reviews in molecular, cellular and developmental biology.

[7]  Y. Saga,et al.  The making of the somite: molecular events in vertebrate segmentation , 2001, Nature Reviews Genetics.

[8]  Zuoyan Zhu,et al.  Whole-body amino acid pattern of F4 human growth hormone gene-transgenic red common carp (Cyprinus carpio) fed diets with different protein levels. , 2000 .

[9]  O. Pourquié,et al.  Vertebrate somitogenesis. , 2001, Annual review of cell and developmental biology.

[10]  S P Allen,et al.  Somite number and vertebrate evolution. , 1998, Development.

[11]  E. Wolf,et al.  Heteroplasmy in Bovine Fetuses Produced by Intra- and Inter-Subspecific Somatic Cell Nuclear Transfer: Neutral Segregation of Nuclear Donor Mitochondrial DNA in Various Tissues and Evidence for Recipient Cow Mitochondria in Fetal Blood1 , 2003, Biology of reproduction.

[12]  M. West,et al.  Cloning of an endangered species (Bos gaurus) using interspecies nuclear transfer. , 2000, Cloning.

[13]  Y Tsunoda,et al.  Eight calves cloned from somatic cells of a single adult. , 1998, Science.

[14]  M. Kinoshita,et al.  Fertile and diploid nuclear transplants derived from embryonic cells of a small laboratory fish, medaka (Oryzias latipes). , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[15]  M. Waksmundzka.  Development of rat x mouse hybrid embryos produced by microsurgery. , 1994, The Journal of experimental zoology.

[16]  J. Gurdon,et al.  Nuclear Transplantation in Eggs and Oocytes , 1986, Journal of Cell Science.

[17]  J. Eisen,et al.  Segmental relationship between somites and vertebral column in zebrafish. , 2002, Development.

[18]  C. Moraes,et al.  Expanding the functional human mitochondrial DNA database by the establishment of primate xenomitochondrial cybrids. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[19]  J. Enríquez,et al.  Autonomous Regulation in Mammalian Mitochondrial DNA Transcription , 1999, Biological chemistry.

[20]  M. Destrempes,et al.  Production of goats by somatic cell nuclear transfer , 1999, Nature Biotechnology.

[21]  I. Wilmut,et al.  Viable offspring derived from fetal and adult mammalian cells , 1997, Nature.

[22]  E. Schon,et al.  Mitochondrial DNA genotypes in nuclear transfer-derived cloned sheep , 1999, Nature Genetics.

[23]  Ki-Young Lee,et al.  Cloned zebrafish by nuclear transfer from long-term-cultured cells , 2002, Nature Biotechnology.

[24]  C. Kimmel,et al.  The zebrafish midblastula transition. , 1993, Development.

[25]  C. Hew,et al.  The potential impact of modern biotechnology on fish aquaculture , 2002 .

[26]  C. Stern,et al.  Clocked gene expression in somite formation. , 1998, BioEssays : news and reviews in molecular, cellular and developmental biology.

[27]  E. Memili,et al.  Bovine oocyte cytoplasm supports development of embryos produced by nuclear transfer of somatic cell nuclei from various mammalian species. , 1999, Biology of reproduction.

[28]  Yifan Dai,et al.  Cloned pigs produced by nuclear transfer from adult somatic cells , 2000, Nature.

[29]  G. Brem,et al.  Coexistence of Bos taurus and B. indicus mitochondrial DNAs in nuclear transfer-derived somatic cattle clones. , 2002, Genetics.

[30]  Maurizio Zuccotti,et al.  Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei , 1998, Nature.

[31]  R. Briggs,et al.  Transplantation of Living Nuclei From Blastula Cells into Enucleated Frogs' Eggs. , 1952, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Yi Yonglan,et al.  NUCLEAR TRANSPLANTATION IN TELEOSTS——HYBRID FISH FROM THE NUCLEUS OF CRUCIAN AND THE CYTOPLASM OF CARP , 1984 .

[33]  Thomas D. Bunch,et al.  A Mule Cloned from Fetal Cells by Nuclear Transfer , 2003, Science.

[34]  Zhuzuoyan,et al.  Embryonic and genetic manipulation in fish , 2000 .

[35]  Casey,et al.  Near extinction of a large, widely distributed fish , 1998, Science.

[36]  Carl L. Hubbs,et al.  Fishes of the World. , 1978 .