Development of the central nervous system in equine twin fetuses derived by somatic cell nuclear transfer
N. N. Rigoglio A B , O. E. Smith A , G. S. S. Matias B , M. A. Miglino B C and L. C. Smith A
+ Author Affiliations
- Author Affiliations
A Centre de recherche en reproduction et fertilité, Department of Veterinary Biomedicine, School of Veterinary Medicine, University of Montreal, Saint-Hyacinthe, 3200 Rue Sicotte – QC J2S 2M2, Canada.
B Department of Surgery, School of Veterinary Medicine and Animal Science, University of Sao Paulo, Sao Paulo, Butanta, 87 Ave. Dr. Prof. Orlando de Marques Paiva – 05508-270, Sao Paulo, Brazil.
C Corresponding author. Email: miglino@usp.br
Reproduction, Fertility and Development 31(5) 941-952 https://doi.org/10.1071/RD18215
Submitted: 9 June 2018 Accepted: 20 December 2018 Published: 29 January 2019
Abstract
Because of the growing importance of horses in leisure and several sports, somatic cell nuclear transfer (SCNT) is being used more frequently for cloning animals for performance and reproductive purposes. However, because of the need to perforate the zona pellucida during microsurgical reconstruction of the oocyte, it is possible that SCNT-derived embryos undergo premature hatching, resulting in embryo bisection and twinning. Therefore, because equine twin pregnancies often lead to abnormal embryo development and pregnancy failure, we performed a detailed comparative assessment of equine twin fetuses derived by SCNT with particular attention on the development of the central nervous system at 40 and 60 days gestation. The results of this study indicate that although cloned twin embryos show small differences in size, they do not exhibit apparent macro- or microscopic developmental discrepancies in the central nervous system, suggesting that the twining phenomenon resulting from SCNT does not affect fetal differentiation.
Additional keywords: cloned fetuses, twinning.
References
Adams, G. P., Kastelic, J. P., Bergfelt, D. R., and Ginther, O. J. (1987). Effect of uterine inflammation and ultrasononically-detected uterine pathology on fertility in the mare. J. Reprod. Fertil. Suppl. 35, 445–454.| 3316644PubMed |
Allen, W. R., and Pashen, R. L. (1984). Production of monozygotic (identical) horse twins by embryo micromanipulation. J. Reprod. Fertil. 71, 607–613.
| Production of monozygotic (identical) horse twins by embryo micromanipulation.Crossref | GoogleScholarGoogle Scholar | 6747968PubMed |
Allen, W. R., and Wilsher, S. (2009). A review of implantation and early placentation in the mare. Placenta 30, 1005–1015.
| A review of implantation and early placentation in the mare.Crossref | GoogleScholarGoogle Scholar | 19850339PubMed |
Armstrong, E., Schleicher, A., Omran, H., Curtis, M., and Zilles, K. (1995). The ontogeny of human gyrification. Cereb. Cortex 5, 56–63.
| The ontogeny of human gyrification.Crossref | GoogleScholarGoogle Scholar | 7719130PubMed |
Bartley, A. J., Jones, D. W., and Weinberger, D. R. (1997). Genetic variability of human brain size and cortical gyral patterns. Brain 120, 257–269.
| Genetic variability of human brain size and cortical gyral patterns.Crossref | GoogleScholarGoogle Scholar | 9117373PubMed |
Bartzokis, G., Beckson, M., Lu, P. H., Nuechterlein, K. H., Edwards, N., and Mintz, J. (2001). Age-related changes in frontal and temporal lobe volumes in men: a magnetic resonance imaging study. Arch. Gen. Psychiatry 58, 461–465.
| Age-related changes in frontal and temporal lobe volumes in men: a magnetic resonance imaging study.Crossref | GoogleScholarGoogle Scholar | 11343525PubMed |
Bergfelt, D. R., and Ginther, O. J. (1992). Embryonic loss in mares: role of the embryonic vesicle, corpus luteum and progesterone. J. Reprod. Fertil. 95, 339–347.
| Embryonic loss in mares: role of the embryonic vesicle, corpus luteum and progesterone.Crossref | GoogleScholarGoogle Scholar | 1517992PubMed |
Bignami, A., and Dahl, D. (1974). Astrocyte-specific protein and neurological differentiation – an immunofluorescence study with antibodies to the glial fibrillary acidic protein J. Comp. Neurol. 153, 27–37.
| Astrocyte-specific protein and neurological differentiation – an immunofluorescence study with antibodies to the glial fibrillary acidic proteinCrossref | GoogleScholarGoogle Scholar | 4593733PubMed |
Biondi, A., Nogueira, H., Dormont, D., Duyme, M., Hasboun, D., Zouaoui, A., Chantome, M., and Marsault, C. (1998). Are the brains of monozygotic twins similar? A three-dimensional MR study. AJNR Am. J. Neuroradiol. 19, 1361–1367.
| 9726483PubMed |
Blickstein, I. (2005). Estimation of iatrogenic monozygotic twinning rate following assisted reproduction: pitfalls and caveats. Am. J. Obstet. Gynecol. 192, 365–368.
| Estimation of iatrogenic monozygotic twinning rate following assisted reproduction: pitfalls and caveats.Crossref | GoogleScholarGoogle Scholar | 15695973PubMed |
Blickstein, I., Jones, C., and Keith, L. G. (2003). Zygotic-splitting rates after single-embryo transfers in in vitro fertilization. N. Engl. J. Med. 348, 2366–2367.
| Zygotic-splitting rates after single-embryo transfers in in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 12789011PubMed |
Bordignon, V., Keyston, R., Lazaris, A., Bilodeau, A. S., Pontes, J. H., Arnold, D., Fecteau, G., Keefer, C., and Smith, L. C. (2003). Transgene expression of green fluorescent protein and germ line transmission in cloned calves derived from in vitro-transfected somatic cells. Biol. Reprod. 68, 2013–2023.
| Transgene expression of green fluorescent protein and germ line transmission in cloned calves derived from in vitro-transfected somatic cells.Crossref | GoogleScholarGoogle Scholar | 12606490PubMed |
Bovolenta, P., Liem, R. H. K., and Mason, C. A. (1984). Development of cerebellar astroglia – transitions in form and cytoskeletal content Dev. Biol. 102, 248–259.
| Development of cerebellar astroglia – transitions in form and cytoskeletal contentCrossref | GoogleScholarGoogle Scholar | 6538151PubMed |
Brisville, A. C., Fecteau, G., Boysen, S., Desrochers, A., Dorval, P., Buczinski, S., Lefebvre, R., Helie, P., Blondin, P., and Smith, L. C. (2013). Neonatal morbidity and mortality of 31 calves derived from somatic cloning. J. Vet. Intern. Med. 27, 1218–1227.
| Neonatal morbidity and mortality of 31 calves derived from somatic cloning.Crossref | GoogleScholarGoogle Scholar | 23782425PubMed |
Brooks, P. H., and Cole, D. J. (1978). Monochorionic ‘twins’ in multiparous sows. Vet. Rec. 102, 16.
| Monochorionic ‘twins’ in multiparous sows.Crossref | GoogleScholarGoogle Scholar | 636205PubMed |
Carmelli, D., DeCarli, C., Swan, G. E., Jack, L. M., Reed, T., Wolf, P. A., and Miller, B. L. (1998). Evidence for genetic variance in white matter hyperintensity volume in normal elderly male twins. Stroke 29, 1177–1181.
| Evidence for genetic variance in white matter hyperintensity volume in normal elderly male twins.Crossref | GoogleScholarGoogle Scholar | 9626291PubMed |
Choi, B. H., and Lapham, L. W. (1978). Radial glia in the human fetal cerebrum – a combined Golgi, immunofluorescent and electron microscopic study Brain Res. 148, 295–311.
| Radial glia in the human fetal cerebrum – a combined Golgi, immunofluorescent and electron microscopic studyCrossref | GoogleScholarGoogle Scholar |
Davidoff, M. S., Middendorff, R., Köfüncü, E., Müller, D., Jesek, D., and Holstein, A. F. (2002). Leydig cells of human testis possess astrocyte and oligodendrocyte marker molecules. Acta Histochem. 104, 39–49.
| Leydig cells of human testis possess astrocyte and oligodendrocyte marker molecules.Crossref | GoogleScholarGoogle Scholar | 11993850PubMed |
Derom, C., Vlietinck, R., Derom, R., Van den Berghe, H., and Thiery, M. (1987). Increased monozygotic twinning rate after ovulation induction. Lancet 329, 1236–1238.
| Increased monozygotic twinning rate after ovulation induction.Crossref | GoogleScholarGoogle Scholar |
Eng, L. F., Ghirnikar, R. S., and Lee, Y. L. (2000). Glial fibrillary acidic protein: GFAP – thirty-one years (1969–2000). Neurochem. Res. 25, 1439–1451.
| Glial fibrillary acidic protein: GFAP – thirty-one years (1969–2000).Crossref | GoogleScholarGoogle Scholar | 11059815PubMed |
Frazer, G. S. (2003). Twins. In ‘Current Therapy in Equine Medicine’. 5th edn. (Ed. N. E. Robinson.) pp. 245–248. (W. B. Saunders: St Louis.)
Galli, C., Lagutina, I., Crotti, G., Colleoni, S., Turini, P., Ponderato, N., Duchi, R., and Lazzari, G. (2003). Pregnancy: a cloned horse born to its dam twin. Nature 424, 635.
| Pregnancy: a cloned horse born to its dam twin.Crossref | GoogleScholarGoogle Scholar | 12904778PubMed |
Gardner, D. S., Buttery, P. J., Daniel, Z., and Symonds, M. E. (2007). Factors affecting birth weight in sheep: maternal environment. Reproduction 133, 297–307.
| Factors affecting birth weight in sheep: maternal environment.Crossref | GoogleScholarGoogle Scholar | 17244755PubMed |
Giedd, J. N., Snell, J. W., Lange, N., Rajapakse, J. C., Casey, B. J., Kozuch, P. L., Vaituzis, A. C., Vauss, Y. C., Hamburger, S. D., Kaysen, D., and Rapoport, J. L. (1996). Quantitative magnetic resonance imaging of human brain development: ages 4–18. Cereb. Cortex 6, 551–559.
| Quantitative magnetic resonance imaging of human brain development: ages 4–18.Crossref | GoogleScholarGoogle Scholar | 8670681PubMed |
Gilmore, J. H., Schmitt, J. E., Knickmeyer, R. C., Smith, J. K., Lin, W., Styner, M., Gerig, G., and Neale, M. C. (2010). Genetic and environmental contributions to neonatal brain structure: a twin study. Hum. Brain Mapp. 31, 1174–1182.
| 20063301PubMed |
Ginther, O. J. (1983). Mobility of the equine conceptus. Theriogenology 19, 603–611.
| Mobility of the equine conceptus.Crossref | GoogleScholarGoogle Scholar | 16725808PubMed |
Ginther, O. J. (1985). Dynamical physical interactions between the equine embryo and uterus. Equine Vet. J. Suppl. 3, 41–47.
Ginther, O. J., Bergfelt, D. R., Leith, G. S., and Scraba, S. T. (1985). Embryonic loss in mares: incidence and ultrasonic morphology. Theriogenology 24, 73–86.
| Embryonic loss in mares: incidence and ultrasonic morphology.Crossref | GoogleScholarGoogle Scholar | 16726060PubMed |
Heyman, Y., Chavatte-Palmer, P., LeBourhis, D., Camous, S., Vignon, X., and Renard, J. P. (2002). Frequency and occurrence of late-gestation losses from cattle cloned embryos. Biol. Reprod. 66, 6–13.
| Frequency and occurrence of late-gestation losses from cattle cloned embryos.Crossref | GoogleScholarGoogle Scholar | 11751257PubMed |
Hill, J., Winger, Q., Jones, K., Keller, D., King, W. A., and Westhusin, M. (2004). The effect of donor cell serum starvation and oocyte activation compounds on the development of somatic cell cloned embryos. Cloning 1, 201–208.
| The effect of donor cell serum starvation and oocyte activation compounds on the development of somatic cell cloned embryos.Crossref | GoogleScholarGoogle Scholar |
Hinrichs, K. (2010). In vitro production of equine embryos: state of the art. Reprod. Domest. Anim. 45, 3–8.
| In vitro production of equine embryos: state of the art.Crossref | GoogleScholarGoogle Scholar | 20591059PubMed |
Hinrichs, K. (2013). Assisted reproduction techniques in the horse. Reprod. Fertil. Dev. 25, 80–93.
| Assisted reproduction techniques in the horse.Crossref | GoogleScholarGoogle Scholar |
Hodder, A. D., Coyne, C. P., and Madigan, J. E. (2010). Birth of live triplets in a mare. Equine Vet. J. 42, 84–85.
| Birth of live triplets in a mare.Crossref | GoogleScholarGoogle Scholar | 20121920PubMed |
Jeffcott, L. B., and Whitwell, K. E. (1973). Twinning as a cause of foetal and neonatal loss in the thoroughbred mare. J. Comp. Pathol. 83, 91–106.
| Twinning as a cause of foetal and neonatal loss in the thoroughbred mare.Crossref | GoogleScholarGoogle Scholar | 4731313PubMed |
Johnson, A. K., Clark-Price, S. C., Choi, Y. H., Hartman, D. L., and Hinrichs, K. (2010). Physical and clinicopathologic findings in foals derived by use of somatic cell nuclear transfer: 14 cases (2004–2008). J. Am. Vet. Med. Assoc. 236, 983–990.
| Physical and clinicopathologic findings in foals derived by use of somatic cell nuclear transfer: 14 cases (2004–2008).Crossref | GoogleScholarGoogle Scholar | 20433399PubMed |
Kato, T., Iwamoto, K., Kakiuchi, C., Kuratomi, G., and Okazaki, Y. (2005). Genetic or epigenetic difference causing discordance between monozygotic twins as a clue to molecular basis of mental disorders. Mol. Psychiatry 10, 622–630.
| Genetic or epigenetic difference causing discordance between monozygotic twins as a clue to molecular basis of mental disorders.Crossref | GoogleScholarGoogle Scholar | 15838537PubMed |
Keefer, C. L. (2015). Artificial cloning of domestic animals. Proc. Natl Acad. Sci. USA 112, 8874–8878.
| Artificial cloning of domestic animals.Crossref | GoogleScholarGoogle Scholar | 26195770PubMed |
Lambroso, P. J., and Rubenstein, J. L. R. (1998). Development of the cerebral cortex: V. Transcription factors and brain development. J. Am. Acad. Child Adolesc. Psychiatry 37, 561–562.
| Development of the cerebral cortex: V. Transcription factors and brain development.Crossref | GoogleScholarGoogle Scholar |
Laugier, C., Foucher, N., Sevin, C., Leon, A., and Tapprest, J. (2011). A 24-year retrospective study of equine abortion in Normandy (France). J. Equine Vet. Sci. 31, 116–123.
| A 24-year retrospective study of equine abortion in Normandy (France).Crossref | GoogleScholarGoogle Scholar |
Leckman, J. F., and Lombroso, P. J. (1998). Development of the cerebral cortex: IV. Transcription factors. J. Am. Acad. Child Adolesc. Psychiatry 37, 451–452.
| Development of the cerebral cortex: IV. Transcription factors.Crossref | GoogleScholarGoogle Scholar | 9549968PubMed |
Levitt, P., and Rakic, P. (1980). lmmunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brain J. Comp. Neurol. 193, 815–840.
| lmmunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brainCrossref | GoogleScholarGoogle Scholar | 7002963PubMed |
Li, X., Morris, L. H., and Allen, W. R. (2001). Influence of co-culture during maturation on the developmental potential of equine oocytes fertilized by intracytoplasmic sperm injection (ICSI). Reproduction 121, 925–932.
| Influence of co-culture during maturation on the developmental potential of equine oocytes fertilized by intracytoplasmic sperm injection (ICSI).Crossref | GoogleScholarGoogle Scholar | 11373179PubMed |
Liedtke, W., Edelmann, W., Bieri, P. L., Chiu, F. C., Cowan, N. J., Kucherlapati, R., and Raine, C. S. (1996). GFAP is necessary for the integrity of CNS white matter architecture and long-term maintenance of myelination. Neuron 17, 607–615.
| GFAP is necessary for the integrity of CNS white matter architecture and long-term maintenance of myelination.Crossref | GoogleScholarGoogle Scholar | 8893019PubMed |
Long, C. R., Westhusin, M. E., and Golding, M. C. (2014). Reshaping the transcriptional frontier: epigenetics and somatic cell nuclear transfer. Mol. Reprod. Dev. 81, 183–193.
| Reshaping the transcriptional frontier: epigenetics and somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 24167064PubMed |
Macpherson, M. L., and Reimer, J. M. (2000). Twin reduction in the mare: current options. Anim. Reprod. Sci. 60–61, 233–244.
| Twin reduction in the mare: current options.Crossref | GoogleScholarGoogle Scholar | 10844198PubMed |
Mancill, S. S., Blodgett, G., Arnott, R. J., Alvarenga, M., Love, C. C., and Hinrichs, K. (2011). Description and genetic analysis of three sets of monozygotic twins resulting from transfers of single embryos to recipient mares. J. Am. Vet. Med. Assoc. 238, 1040–1043.
| Description and genetic analysis of three sets of monozygotic twins resulting from transfers of single embryos to recipient mares.Crossref | GoogleScholarGoogle Scholar | 21492048PubMed |
Mariz, T. M. de A., dos Anjos, A. G., Flor, J. M. De A., Lima, C. B., Givisiez, P. E. N., and de Azevedo, P. S. (2008). Influências do clima sobre a atividade reprodutiva de éguas da raça mangalarga marchador no estado de sergipe. Acta Vet. Brasílica 2, 39–43.
McCue, P. M., Thayer, J., Squires, E. L., Brinsko, S. P., and Vanderwall, D. K. (1998). Twin pregnancies following transfer of single embryos in three mares: a case report. J. Equine Vet. Sci. 18, 832–834.
| Twin pregnancies following transfer of single embryos in three mares: a case report.Crossref | GoogleScholarGoogle Scholar |
McKinnon, A. O. (2007). Twin reduction techniques. In ‘Current Therapy in Equine Reproduction’. (Eds J. C. Samper, J. F. Pycock, and A. O. McKinnon.) pp. 357–373. (Saunders: St Louis.)
McKinnon, A. O., and Rantanen, N. W. (1998). Twins. In ‘Equine Diagnostic Ultrasonography’. (Eds N. W. Rantanen and A. O. McKinnon.) pp. 141–156. (Willians and Wilkins: Baltimore.)
Meadows, S. J., Binns, M. M., Newcombe, J. R., Thompson, C. J., and Rossdale, P. D. (1995). Identical triplets in a thoroughbred mare. Equine Vet. J. 27, 394–397.
| Identical triplets in a thoroughbred mare.Crossref | GoogleScholarGoogle Scholar | 8654356PubMed |
Morris, L. H. A., and Allen, W. R. (2002). Reproductive efficiency of intensively managed Thoroughbred mares in Newmarket. Equine Vet. J. 34, 51–60.
| Reproductive efficiency of intensively managed Thoroughbred mares in Newmarket.Crossref | GoogleScholarGoogle Scholar |
Moyaert, I., Bouters, R., and Bouquet, Y. (1982). Birth of a monozygotic cattle twin following non surgical transfer of a single 7 day old embryo. Theriogenology 18, 127–132.
| Birth of a monozygotic cattle twin following non surgical transfer of a single 7 day old embryo.Crossref | GoogleScholarGoogle Scholar | 16725734PubMed |
Oback, B. (2008). Climbing Mount Efficiency – small steps, not giant leaps towards higher cloning success in farm animals. Reprod. Domest. Anim. 43, 407–416.
| Climbing Mount Efficiency – small steps, not giant leaps towards higher cloning success in farm animals.Crossref | GoogleScholarGoogle Scholar | 18638154PubMed |
Ochoa-Cortes, F., Turco, F., Linan-Rico, A., Soghomonyan, S., Whitaker, E., Wehner, S., Cuomo, R., and Christofi, F. L. (2016). Enteric glial cells: a new frontier in neurogastroenterology and clinical target for inflammatory bowel diseases. Inflamm. Bowel Dis. 22, 433–449.
| Enteric glial cells: a new frontier in neurogastroenterology and clinical target for inflammatory bowel diseases.Crossref | GoogleScholarGoogle Scholar | 26689598PubMed |
Oppenheim, J. S., Skerry, J. E., Tramo, M. J., and Gazzaniga, M. S. (1989). Magnetic resonance imaging morphology of the corpus callosum in monozygotic twins. Ann. Neurol. 26, 100–104.
| Magnetic resonance imaging morphology of the corpus callosum in monozygotic twins.Crossref | GoogleScholarGoogle Scholar | 2774498PubMed |
Pascoe, R. R. (1983). Methods for the treatment of twin pregnancy in the mare. Equine Vet. J. 15, 40–42.
| Methods for the treatment of twin pregnancy in the mare.Crossref | GoogleScholarGoogle Scholar | 6572145PubMed |
Pennington, B. F., Filipek, P. A., Lefly, D., Chhabildas, N., Kennedy, D. N., Simon, J. H., Filley, C. M., Galaburda, A., and DeFries, J. C. (2000). A twin MRI study of size variations in human brain. J. Cogn. Neurosci. 12, 223–232.
| A twin MRI study of size variations in human brain.Crossref | GoogleScholarGoogle Scholar | 10769318PubMed |
Peper, J. S., Brouwer, R. M., Boomsma, D. I., Kahn, R. S., and Hulshoff Pol, H. E. (2007). Genetic influences on human brain structure: a review of brain imaging studies in twins. Hum. Brain Mapp. 28, 464–473.
| Genetic influences on human brain structure: a review of brain imaging studies in twins.Crossref | GoogleScholarGoogle Scholar | 17415783PubMed |
Peters, A., Morrison, J. H., Rosene, D. L., and Hyman, B. T. (1998). Feature article: are neurons lost from the primate cerebral cortex during normal aging? Cereb. Cortex 8, 295–300.
| Feature article: are neurons lost from the primate cerebral cortex during normal aging?Crossref | GoogleScholarGoogle Scholar | 9651126PubMed |
Pharoah, P. O. D. (2002). Neurological outcome in twins. Semin. Neonatol. 7, 223–230.
| Neurological outcome in twins.Crossref | GoogleScholarGoogle Scholar |
Posthuma, D., and Polderman, T. J. (2013). What have we learned from recent twin studies about the etiology of neurodevelopmental disorders? Curr. Opin. Neurol. 26, 111–121.
| What have we learned from recent twin studies about the etiology of neurodevelopmental disorders?Crossref | GoogleScholarGoogle Scholar | 23426380PubMed |
Price, B. (1950). Primary biases in twin studies; a review of prenatal and natal difference-producing factors in monozygotic pairs. Am. J. Hum. Genet. 2, 293–352.
| 14837903PubMed |
Raju, T., Bignami, A., and Dahl, D. (1981). In vivo and in vitro differentiation of neurons and astrocytes in the rat embryo Dev. Biol. 85, 344–357.
| In vivo and in vitro differentiation of neurons and astrocytes in the rat embryoCrossref | GoogleScholarGoogle Scholar | 6790318PubMed |
Rakic, P. (1988). Specification of cerebral cortical areas. Science 241, 170–176.
| Specification of cerebral cortical areas.Crossref | GoogleScholarGoogle Scholar | 3291116PubMed |
Rigoglio, N. N., Barreto, R. S., Favaron, P. O., Jacob, J. C., Smith, L. C., Gastal, M. O., Gastal, E. L., and Miglino, M. A. (2017). Central nervous system and vertebrae development in horses: a chronological study with differential temporal expression of nestin and GFAP. J. Mol. Neurosci. 61, 61–78.
| Central nervous system and vertebrae development in horses: a chronological study with differential temporal expression of nestin and GFAP.Crossref | GoogleScholarGoogle Scholar | 27525635PubMed |
Roberts, C. J. (1982). Termination of twin gestation by blastocyst crush in the broodmare. J. Reprod. Fertil. Suppl. 32, 447–449.
| 6962880PubMed |
Roberts, S. J., and Myhre, G. (1983). A review of twinning in horses and the possible therapeutic value of supplemental progesterone to prevent abortion of equine twin fetuses the latter half of the gestation period. Cornell Vet. 73, 257–264.
| 6884035PubMed |
Roberts, M. A., London, K., Campos-Chillon, L. F., and Altermatt, J. L. (2015). Presumed monozygotic twins develop following transfer of an in vitro-produced equine embryo. J. Equine Sci. 26, 89–94.
| Presumed monozygotic twins develop following transfer of an in vitro-produced equine embryo.Crossref | GoogleScholarGoogle Scholar | 26435682PubMed |
Rubenstein, J. L., and Rakic, P. (1999). Genetic control of cortical development. Cereb. Cortex 9, 521–523.
| Genetic control of cortical development.Crossref | GoogleScholarGoogle Scholar | 10498269PubMed |
Sidman, R. L., and Rakic, P. (1973). Neuronal migration, with special reference to developing human brain: a review. Brain Res. 62, 1–35.
| Neuronal migration, with special reference to developing human brain: a review.Crossref | GoogleScholarGoogle Scholar | 4203033PubMed |
Solter, D. (2000). Mammalian cloning: advances and limitations. Nat. Rev. Genet. 1, 199–207.
| Mammalian cloning: advances and limitations.Crossref | GoogleScholarGoogle Scholar | 11252749PubMed |
Tardy, M., Fages, C., Le Prinee, B., Rolland, B., and Nunez, J. (1990). Regulation of the glial fibrillary acidic protein (GFAP) and its encoding mRNA in the developing brain and in cultured astrocytes. Adv. Exp. Med. Biol. 265, 41–52.
| Regulation of the glial fibrillary acidic protein (GFAP) and its encoding mRNA in the developing brain and in cultured astrocytes.Crossref | GoogleScholarGoogle Scholar | 2165732PubMed |
Tramo, M. J., Loftus, W. C., Stukel, T. A., Green, R. L., Weaver, J. B., and Gazzaniga, M. S. (1998). Brain size, head size, and intelligence quotient in monozygotic twins. Neurology 50, 1246–1252.
| Brain size, head size, and intelligence quotient in monozygotic twins.Crossref | GoogleScholarGoogle Scholar | 9595970PubMed |
Triolo, D., Dina, G., Lorenzetti, I., Malaguti, M. C., Morana, P., Del Carro, U., Comi, G., Messing, A., Quattrini, A., and Previtali, S. C. (2006). Loss of glial fibrillary acidic protein (GFAP) impairs Schwann cell proliferation and delays nerve regeneration after damage. J. Cell Sci. 119, 3981–3993.
| Loss of glial fibrillary acidic protein (GFAP) impairs Schwann cell proliferation and delays nerve regeneration after damage.Crossref | GoogleScholarGoogle Scholar | 16988027PubMed |
Welker, W. (1990). Why does cerebral cortex fissure and fold. In ‘Cerebral Cortex’. (Eds E. G. Jones and A. Peters.) pp. 3–136. (Plenum Press: New York.)
Wilmut, I., Schnieke, A. E., McWhir, J., Kind, A. J., and Campbell, K. H. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810–813.
| Viable offspring derived from fetal and adult mammalian cells.Crossref | GoogleScholarGoogle Scholar | 9039911PubMed |
Woods, G. L., Baker, C. B., Hillman, R. B., and Schlafer, D. H. (1985). Recent studies relating to earlyembryonic death in themare. Equine Vet. J. Suppl. 3, 104–107.
Woods, G. L., White, K. L., Vanderwall, D. K., Li, G. P., Aston, K. I., Bunch, T. D., Meerdo, L. N., and Pate, B. J. (2003). A mule cloned from fetal cells by nuclear transfer. Science 301, 1063.
| A mule cloned from fetal cells by nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 12775846PubMed |
