Primate Models for the Assisted Reproductive Technologies and Embryonic Stem Cell Biology

  • Don P. Wolf
  • Shoukhrat Mitalipov
  • James A. Byrne

Abstract

Nonhuman primates (NHPs) represent clinically relevant animal models used in studies on the etiology and treatment of human diseases. In the context of reproduction, NHP models are relevant to research interests as diverse as the etiology and treatment of infertility and contraceptive development to an evaluation of cell or tissue-based therapies of disease employing embryonic stem cell-derived phenotypes. The assisted reproductive technologies (ARTs) are used in the production of animals carrying desired MHC alleles for HIV vaccine development and could be used in the production of genetically identical animals by somatic cell nuclear transfer (SCNT). SCNT in turn is relevant to rescuing the unique genetics of aging or even deceased animals, to testing the efficacy of therapeutic cloning, and in combination with gene targeting, to creating monkey models of genetically based, neurodegenerative diseases. Since most NHP experience in applying the ARTs and in deriving embryonic stem cells (ESCs) involves Old World monkeys, principally rhesus and cynomolgus macaques and baboons, studies with these species will be featured in this chapter.

Key Words

Nonhuman primates Assisted reproductive technology Embryonic stem cells Cloning 

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References

  1. 1.
    Bernacky BJ, Gibson SV, Keeling ME, Abee CR. Nonhuman primates. In: Fox JG, Anderson LC, Loew FM, Quimby FW, Eds. Laboratory Animal Medicine, 2nd ed. London: Academic Press, 2002:676–791.Google Scholar
  2. 2.
    Hewitson L. Primate models for assisted reproductive technologies. Reproduction 2004;128:293–299.PubMedGoogle Scholar
  3. 3.
    Schramm RD, Bavister BD. A macaque model for studying mechanisms controlling oocyte development and maturation in human and non-human primates. Hum Reprod 1999;14:2544–2555.PubMedGoogle Scholar
  4. 4.
    Schramm RD, Paprocki AM. Birth of rhesus monkey infant after transfer of embryos derived from in-vitro matured oocytes: Short communication. Hum Reprod 2000;15:2411–2414.PubMedGoogle Scholar
  5. 5.
    Zheng P, Si W, Bavister BD, Yang J, Ding CH, Ji W. 17β-Estradiol and progesterone improve in-vitro cytoplasmic maturation of oocytes from unstimulated prepubertal and adult rhesus monkeys. Hum Reprod 2003;18:2137–2144.PubMedGoogle Scholar
  6. 6.
    Yin H, Duffy DM, Gosden RG. Comparative maturation of cynomolgus monkey oocytes in vivo and in vitro. Reprod Biol Endocrinol 2006;4:14.PubMedGoogle Scholar
  7. 7.
    Chen C, Liow S-L, Abdullah RB, Embong WKW, Yip W-Y, Tan L-G, Tong G-Q, Ng SC. Developmental competence of transported in vitro matured macaque oocytes. Reprod Biol Endocrinol 2006;23:50–59.Google Scholar
  8. 8.
    Lee DM, Yeoman RR, Battaglia DE, Stouffer RL, Zelinski-Wooten MB, Fanton JW, Wolf DP. Live birth after ovarian tissue transplant. Nature 2004;428:137–138.PubMedGoogle Scholar
  9. 9.
    Dukelow WR, Pierce DL, Roudebush WE, Jarosz SJ, Sengoku K. In vitro fertilization in nonhuman primates. J Med Primatol 1990;19:627–639.PubMedGoogle Scholar
  10. 10.
    Kubisch HM, Gagliardi C, Williams VM, Ribka EP, Ratterree MS. In vitro fertilization in the pigtailed macaque (Macaca nemestrina). Theriogenology 2006;66(4): 749–754.PubMedGoogle Scholar
  11. 11.
    Bavister BD, Boatman DE, Collins K, Dierschke DJ, Eisele SG. Birth of rhesus monkey infant after in vitro fertilization and nonsurgical embryo transfer. Proc Natl Acad Sci USA 1984;81:2218–2222.PubMedGoogle Scholar
  12. 12.
    Wolf DP, Thomson JA, Zelinski-Wooten MB, Stouffer RL. In vitro fertilization-embryo transfer in nonhuman primates: The technique and its applications. Mol Reprod Dev 1990;27:261–280.PubMedGoogle Scholar
  13. 13.
    Meng L, Ely JJ, Stouffer RL, Wolf DP. Rhesus monkeys produced by nuclear transfer. Biol Reprod 1997;57:454–459.PubMedGoogle Scholar
  14. 14.
    Nusser KD, Mitalipov S, Widmann A, Gerami-Naini B, Yeoman RR, Wolf DP. Developmental competence of oocytes after ICSI in the rhesus monkey. Hum Reprod 2001;16:130–137.PubMedGoogle Scholar
  15. 15.
    Mitalipov SM, Yeoman RR, Kuo HC, Wolf DP. Monozygotic twinning in rhesus monkeys by manipulation of in vitro-derived embryos. Biol Reprod 2002;66:1449–1455.PubMedGoogle Scholar
  16. 16.
    Stouffer RL, Zelinski-Wooten M, Chandrasekher YA, Wolf DP. Stimulation of follicle and oocyte development in macaques for IVF procedures. In: Wolf DP, Stouffer RL, Brenner RM, Eds. In Vitro Fertilization and Embryo Transfer in Primates. New York: Springer-Verlag, 1992:124–141.Google Scholar
  17. 17.
    Ouhibi N, Zelinski-Wooten M, Thomson JA, Wolf DP. Assisted fertilization and nuclear transfer in non human primates. In: Wolf DP, Zelinski-Wooten M, Eds. Assisted Fertilization and Nuclear Transfer in Mammals. Totowa, NJ: Humana Press, 2001:253–284.Google Scholar
  18. 18.
    Wolf DP. Assisted reproductive technologies in rhesus macaques. Reprod Biol Endocrinol 2004;2:37.PubMedGoogle Scholar
  19. 19.
    Wolf DP, Thormahlen S, Ramsey C, Fanton J, Mitalipov S. Use of assisted reproductive technologies in the propagation of rhesus macaque offspring. Biol Reprod 2004;71:486–493.PubMedGoogle Scholar
  20. 20.
    Wolf DP, Vandevoort CA, Meyer-Haas GR, Zelinski-Wooten MB, Hess DL, Baughman WL, Stouffer RL. In vitro fertilization and embryo transfer in the rhesus monkey. Biol Reprod 1989;41:335–346.PubMedGoogle Scholar
  21. 21.
    Lanzendorf SE, Zelinski-Wooten MB, Stouffer RL, Wolf DP. Maturity at collection and the developmental potential of rhesus monkey oocytes. Biol Reprod 1990;42:703–711.PubMedGoogle Scholar
  22. 22.
    Boatman DE. In vitro growth of nonhuman primate pre-and periimplantation embryos. In: Bavister BD, Ed. The Mammalian Preimplantation Embryo: Regulation of Growth and Differentiation In Vitro. New York: Plenum, 1987:273–308.Google Scholar
  23. 23.
    Roussel JD, Austin CR. Preservation of primate spermatozoa by freezing. J Reprod Fertil 1967;13:333–335.PubMedGoogle Scholar
  24. 24.
    Leverage WE, Valerio DA, Schultz AP, Kingsbury E, Dorey C. Comparative study on the freeze preservation of spermatozoa. Primate, bovine, and human. Lab Anim Sci 1972;22:882–889.PubMedGoogle Scholar
  25. 25.
    Yeoman RR, Mitalipov S, Gerami-Naini B, Nusser KD, Wolf DP. Low temperature storage of rhesus monkey spermatozoa and fertility evaluation by intracytoplasmic injection. Theriogenology 2005;63:2356–2371.PubMedGoogle Scholar
  26. 26.
    VandeVoort CA, Baughman WL, Stouffer RL. Comparison of different regimens of human gonadotropins for superovulation of rhesus monkeys: Ovulatory response and subsequent luteal function. J In Vitro Fert Embryo Transfer 1989;6:85–91.Google Scholar
  27. 27.
    Abassi R, Kenigsberg D, Danforth D, Falk RJ, Hodgen HG. Cumulative ovulation rate in human menopausal/human chorionic gonadotropin-treated monkeys: “Step-up” versus “step-down” dose regimens. Fertil Steril 1987;47:1019–1024.Google Scholar
  28. 28.
    Boatman DE, Morgan PM, Bavister BD. Variables affecting the yield and developmental potential of embryos following superstimulation and in vitro fertilization in rhesus monkeys. Gamete Res 1986;13:327–338.Google Scholar
  29. 29.
    Zhang L, Weston AM, Denniston RS, Goodeaux LL, Godke RA, Wolf DP. Developmental potential of rhesus monkey embryos produced by in vitro fertilization. Biol Reprod 1994; 51:433–440.PubMedGoogle Scholar
  30. 30.
    Weston AM, Zelinski-Wooten MB, Hutchison JS, Stouffer RL, Wolf DP. Developmental potential of embryos produced by in-vitro fertilization from gonadotrophin-releasing hormone antagonisttreated macaques stimulated with recombinant human follicle stimulating hormone alone or in combination with luteinizing hormone. Hum Reprod 1996;11:608–613.PubMedGoogle Scholar
  31. 31.
    Seshagiri PB, Hearn JP. In-vitro development of in-vivo produced rhesus monkey morulae and blastocysts to hatched, attached, and post-attached blastocyst stages: Morphology and early secretion of chorionic gonadotrophin. Hum Reprod 1993;8:279–287.PubMedGoogle Scholar
  32. 32.
    Weston AM, Wolf DP. Differential preimplantation development of rhesus monkey embryos in serum-supplemented media. Mol Reprod Dev 1996;44:88–92.PubMedGoogle Scholar
  33. 33.
    Schramm RD, Bavister BD. Development of in-vitro-fertilized primate embryos into blastocysts in a chemically defined, proteinfree culture medium. Hum Reprod 1996;11:1690–1697.PubMedGoogle Scholar
  34. 34.
    Alak BM, Wolf DP. Rhesus monkey oocyte maturation and fertilization in vitro: Roles of the menstrual cycle phase and of exogenous gonadotropins. Biol Reprod 1994;51:879–887.PubMedGoogle Scholar
  35. 35.
    Goodeaux L, Thibodeaux JK, Voelkel S, Anzalone CA, Roussel JD, Cohen JC, Menezo Y. Collection, co-culture and transfer of rhesus preimplantation embryos. ARTA 1990;1:370–379.Google Scholar
  36. 36.
    Seshagiri PB, Dierschke DJ, Eisele SG, Scheffler J, Hearn JP. Recovery of rhesus monkey preimplantation embryos by non-surgical uterine flushing. Biol Reprod 1991;44(Suppl. 1):157.Google Scholar
  37. 37.
    Boatman DE, Bavister BD. Stimulation of rhesus monkey sperm capacitation by cyclic nucleotide mediators. J Reprod Fertil 1984;71:357–366.PubMedGoogle Scholar
  38. 38.
    Morgan PM, Boatman DE, Bavister BD. Relationships between follicular fluid steroid hormone concentrations, oocyte maturity, in vitro fertilization and embryonic development in the rhesus monkey. Mol Reprod Dev 1990;27:145–151.PubMedGoogle Scholar
  39. 39.
    Goodeaux LL, Anzalone CA, Thibodeaux JK, Menezo Y, Roussel JD, Voelkel SA. Successful non-surgical collection of Macaca mulatta embryos. Theriogenology 1990;34:1159–1167.Google Scholar
  40. 40.
    Hewitson L, Dominko T, Takahashi D, Martinovich C, Ramalho-Santos J, Sutovsky P, Fanton J, Jacob D, Monteith D, Neuringer M, Battaglia D, Simerly C, Schatten G. Unique checkpoints during the first cell cycle of fertilization after intracytoplasmic sperm injection in rhesus monkeys. Nat Med 1999;5:431–433.PubMedGoogle Scholar
  41. 41.
    Balmaceda JP, Pool TB, Arana JB, Heitman TS, Asch RH. Successful in vitro fertilization and embryo transfer in cynomolgus monkeys. Fertil Steril 1984;42:791–795.PubMedGoogle Scholar
  42. 42.
    Kreitman O, Lynch A, Nixon WE, G.D. H. Ovum collection, induced luteal dysfunction, in vitro fertilization, embryo development and low tubal ovum transfer in primates. In: Hafez ESE, Semm K, Eds. In Vitro Fertilization and Embryo Transfer. Lancaster, UK: MTP Press Ltd., 1982:303–324.Google Scholar
  43. 43.
    Cho F, Honjo S, Makita T. Fertility of frozen-preserved spermatozoa of cynomolgus monkeys. In: Kondo S, Kawai M, Ehara A, Eds. Contemporary Primatology. Basel: S. Karger, 1975:125–133.Google Scholar
  44. 44.
    Cho F, Honjo S. A simplified method for collecting and preserving cynomolgus macaque semen. Jpn J Med Sci Biol 1973;26: 261–268.PubMedGoogle Scholar
  45. 45.
    Mahone JP, Dukelow WR. Semen preservation in Macaca fascicularis. Lab Anim Sci 1978;28:556–561.PubMedGoogle Scholar
  46. 46.
    Tollner TL, VandeVoort CA, Overstreet JW, Drobnis EZ. Cryopreservation of spermatozoa from cynomolgus monkeys (Macaca fascicularis). J Reprod Fertil 1990;90:347–352.PubMedGoogle Scholar
  47. 47.
    Schenken RS, Williams RF, Hodgen GD. Ovulation induction using “pure” follicle-stimulating hormone in monkeys. Fertil Steril 1984;41:629–634.PubMedGoogle Scholar
  48. 48.
    Fujisaki M, Suzuki M, Kohno M, Cho F, Honjo S. Early embryonal culture of the cynomolgus monkey (Macaca fascicularis). Am J Primatol 1989;18:303–313.Google Scholar
  49. 49.
    Balmaceda JP, Gastaldi C, Ord T, Borrero C, Asch RH. Tubal embryo transfer in cynomolgus monkeys: Effects of hyperstimulation and synchrony. Hum Reprod 1988;3:441–443.PubMedGoogle Scholar
  50. 50.
    Balmaceda JP, Heitman TO, Garcia MR, Pauerstein CJ, Pool TB. Embryo cryopreservation in cynomolgus monkeys. Fertil Steril 1986;45:403–406.PubMedGoogle Scholar
  51. 51.
    Cranfield MR, Schaffer N, Bavister BD, Berger NG, Boatman DE, Kempske SE, et al. Assessment of oocytes retrieved from stimulated and unstimulated ovaries of pig-tailed macaques (Macaca nemestrina) as a model to enhance the genetic diversity of captive liontailed macaques (Macaca silenus). Zool Biol 1989;Suppl. 1:33–46.Google Scholar
  52. 52.
    Cranfield MR, Bavister BD, Boatman DE, Berger NG, Schaffer N, Kempske SE, et al. Assisted reproduction in the propagation management of the endangered lion-tailed macaque (Macaca silenus). In: Wolf DP, Stouffer RL, Brenner RM, Eds. In vitro Fertilization and Embryo Transfer in Primates. New York: Springer-Verlag, 1993:331–348.Google Scholar
  53. 53.
    Clayton O, Kuehl TJ. The first successful in vitro fertilization and embryo transfer in a nonhuman primate. Theriogenology 1984; 21:228.Google Scholar
  54. 54.
    Fourie FR, Snyman E, van der Merwe JV, Grace A. Primate in vitro fertilization research: Preliminary results on the folliculogenic effects of three different ovulatory induction agents on the chacma baboon, Papio ursinus. Comp Biochem Physiol 1987;87:889–893.Google Scholar
  55. 55.
    Kraemer DC, Vera Cruz NC. Collection, gross characteristics and freezing of baboon semen. J Reprod Fertil 1969;20:345–348.PubMedGoogle Scholar
  56. 56.
    Pope V, Pope E, Beck L. In vitro development of the primate embryo. In: Brans YW, Kuehl TJ, Eds. Nonhuman Primates in Perinatal Research. New York: John Wiley & Sons; 1988: 161–174.Google Scholar
  57. 57.
    Pope C, Pope V, Beck LR. Live birth following cryopreservation and transfer of a baboon embryo. Fertil Steril 1984;42:143–145.PubMedGoogle Scholar
  58. 58.
    Hess DL, Hendrickx AG, Stabenfeldt GH. Reproductive and hormonal patterns in the African green monkey (Cercopithecus aethiops). J Med Primatol 1979;8:273–281.PubMedGoogle Scholar
  59. 59.
    Van Der Horst G, Seier JV, Spinks AC, Hendricks S. The maturation of sperm motility in the epididymis and vas deferens of the vervet monkey, Cercopithecus aethiops. Int J Androl 1999;22:197–207.Google Scholar
  60. 60.
    Sparman ML, Ramsey C, Thomas CM, Mitalipov S, Fanton J, Maginnis GM, Stouffer RL, Wolf DP. Evaluation of the vervet (Cercopithecus aethiops) as a model for the assisted reproductive technologies. Am J Primatol 2007;69:1–13.Google Scholar
  61. 61.
    Sankai T, Cho F, Yoshikawa Y. In vitro fertilization and preimplantation embryo development of African green monkeys (Cercopithecus aethiops). Am J Primatol 1997;43:43–50.PubMedGoogle Scholar
  62. 62.
    Lopata A, Summers PM, Hearn JP. Births following the transfer of cultured embryos obtained by in vitro and in vivo fertilization in the marmoset monkey (Callithrix jacchus). Fertil Steril 1988;50: 503–509.PubMedGoogle Scholar
  63. 63.
    Wilton LJ, Marshall VS, Piercy EC, Moore HD. In vitro fertilization and embryo development in the marmoset monkey (Callithrix jacchus). J Reprod Fertil 1993;97:481–486.PubMedGoogle Scholar
  64. 64.
    Marshall VS, Kalishman J, Thomson JA. Nonsurgical embryo transfer in the common marmoset monkey. J Med Primatol 1997; 26:241–247.PubMedGoogle Scholar
  65. 65.
    Gould KG, Cline EM, Williams WL. Observations on the induction of ovulation and fertilization in vitro in the squirrel monkey (Saimiri sciureus). Fertil Steril 1973;24:260–268.PubMedGoogle Scholar
  66. 66.
    Kuehl TJ, Dukelow WR. Time relations of squirrel monkey (Saimiri sciureus) sperm capacitation and ovum maturation in an in vitro fertilization system. J Reprod Fertil 1982;64:135–137.PubMedGoogle Scholar
  67. 67.
    Dukelow WR. Human chorionic gonadotropin: Induction of ovulation in the squirrel monkey. Science 1979;206:234–235.PubMedGoogle Scholar
  68. 68.
    Denis LT, Poindexter AN, Ritter MB, Seager SWJ, Deter RL. Freeze preservation of squirrel monkey sperm for use in timed fertilization studies. Fertil Steril 1976;27:723–729.PubMedGoogle Scholar
  69. 69.
    Gould KG. Ovum recovery and in vitro fertilization in the chimpanzee. Fertil Steril 1983;40:378–383.PubMedGoogle Scholar
  70. 70.
    Pope CE, Dresser BL, Chin NW, Liu JH, Loskutoff NM, Behnke EJ, Brown C, McRae MA, Sinoway CE, Campbell MK, Cameron KN, Owens OM, Johnson CA, Evans RR, Cedars MI. Birth of a western lowland gorilla (Gorilla gorilla gorilla) following in vitro fertilization and embryo transfer. Am J Primatol 1997;41: 247–260.PubMedGoogle Scholar
  71. 71.
    Lanzendorf SE, Holmgren WJ, Schaffer N, Hatasaka H, Wentz AC. In vitro fertilization and gamete micromanipulation in lowland gorilla. J Assist Reprod Genet 1992;9:358–364.PubMedGoogle Scholar
  72. 72.
    Huntress SL, Loskutoff NM, Raphael BL, Yee B, Bowsher TR, Putman JM, Kraemer DC. Pronucleus formation following in vitro fertilization of oocytes recovered from a gorilla (Gorilla gorilla gorilla) with unilateral endometroid adenocarcinoma of the ovary. Am J Primatol 1989;18:259–266.Google Scholar
  73. 73.
    Iliff SA, Molskness TA, Stouffer RL. Anti-human gonadotropin antibodies generated during in vitro fertilization (IVF)-related cycles: Effect on fertility of rhesus macaques. J Med Primatol 1995;24:7–11.PubMedGoogle Scholar
  74. 74.
    Chan AW, Dominko T, Luetjens CM, Neuber E, Martinovich C, Hewitson L, Simerly CR, Schatten GP. Clonal propagation of primate offspring by embryo splitting. Science 2000;287:317–319.PubMedGoogle Scholar
  75. 75.
    Mitalipov SM, Yeoman RR, Nusser KD, Wolf DP. Rhesus monkey embryos produced by nuclear transfer from embryonic blastomeres or somatic cells. Biol Reprod 2002;66:1367–1373.PubMedGoogle Scholar
  76. 76.
    Mitalipov S, Wolf DP. Nuclear transfer in non-human primates. In: Verna P, Trounson A, Eds. Nuclear Transfer Protocols: Cell Reprogramming and Transgenesis. Totowa, NJ: Humana Press, 2006.Google Scholar
  77. 77.
    Simerly C, Dominko T, Navara C, Payne C, Capuano S, Gosman G, Chong KY, Takahashi D, Chace C, Compton D, Hewitson L, Schatten G. Molecular correlates of primate nuclear transfer failures. Science 2003;300:297.PubMedGoogle Scholar
  78. 78.
    Simerly C, Navara C, Hyun SH, Lee BC, Kang SK, Capuano S, Gosman G, Dominko T, Chong KY, Compton D, Hwang WS, Schatten G. Embryogenesis and blastocyst development after somatic cell nuclear transfer in nonhuman primates: Overcoming defects caused by meiotic spindle extraction. Dev Biol 2004;276:237–252.PubMedGoogle Scholar
  79. 79.
    Ng SC, Chen N, Yip WY, Liow SL, Tong GQ, Martelli B, Tan LG, Martelli P. The first cell cycle after transfer of somatic cell nuclei in a non-human primate. Development 2004;131:2475–2484.PubMedGoogle Scholar
  80. 80.
    Zhou Q, Yang SH, Ding CH, He XC, Xie YH, Hildebrandt TB, Mitalipov SM, Tang XH, Wolf DP, Ji WZ. A comparative approach to somatic cell nuclear transfer in the rhesus monkey. Hum Reprod 2006;22:22.Google Scholar
  81. 81.
    Mitalipov SM, Zhou Q, Byrne J, Ji WZ, Wolf DP. Reprogramming events and developmental competence of rhesus monkey embryos produced by somatic cell nuclear transfer. Annual Conference of the International Embryo Transfer Society, Orlando, FL. 7–11 January 2006, 139.Google Scholar
  82. 82.
    Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981;292:154–156.PubMedGoogle Scholar
  83. 83.
    Thomson JA, Kalishman J, Golos TG, Durning M, Harris CP, Becker RA, Hearn JP. Isolation of a primate embryonic stem cell line. Proc Natl Acad Sci USA 1995;92:7844–7848.PubMedGoogle Scholar
  84. 84.
    Thomson JA, Kalishman J, Golos TG, Durning M, Harris CP, Hearn JP. Pluripotent cell lines derived from common marmoset (Callithrix jacchus) blastocysts. Biol Reprod 1996;55:254–259.PubMedGoogle Scholar
  85. 85.
    Suemori H, Tada T, Torii R, Hosoi Y, Kobayashi K, Imahie H, Kondo Y, Iritani A, Nakatsuji N. Establishment of embryonic stem cell lines from cynomolgus monkey blastocysts produced by IVF or ICSI. Dev Dyn 2001;222:273–279.PubMedGoogle Scholar
  86. 86.
    Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 1998;282:1145–1147.PubMedGoogle Scholar
  87. 87.
    Donovan PJ, Gearhart J. The end of the beginning for pluripotent stem cells. Nature 2001;414:92–97.PubMedGoogle Scholar
  88. 88.
    Ginis I, Luo Y, Miura T, Thies S, Brandenberger R, Gerecht-Nir S, Amit M, Hoke A, Carpenter MK, Itskovitz-Eldor J, Rao MS. Differences between human and mouse embryonic stem cells. Dev Biol 2004;269:360–380.PubMedGoogle Scholar
  89. 89.
    Marshall VS, Waknitz MA, Thomson JA. Isolation and maintenance of primate embryonic stem cells. Methods Mol Biol 2001;158:11–18.PubMedGoogle Scholar
  90. 90.
    Mitalipov S, Kuo HC, Byrne J, Clepper L, Meisner L, Johnson J, Zeier R, Wolf D. Isolation and characterization of novel rhesus monkey embryonic stem cell lines. Stem Cells 2006;1:1.Google Scholar
  91. 91.
    Cibelli JB, Grant KA, Chapman KB, Cunniff K, Worst T, Green HL, Walker SJ, Gutin PH, Vilner L, Tabar V, Dominko T, Kane J, Wettstein PJ, Lanza RP, Studer L, Vrana KE, West MD. Parthenogenetic stem cells in nonhuman primates. Science 2002;295:819.PubMedGoogle Scholar
  92. 92.
    Sasaki E, Hanazawa K, Kurita R, Akatsuka A, Yoshizaki T, Ishii H, Tanioka Y, Ohnishi Y, Suemizu H, Sugawara A, Tamaoki N, Izawa K, Nakazaki Y, Hamada H, Suemori H, Asano S, Nakatsuji N, Okano H, Tani K. Establishment of novel embryonic stem cell lines derived from the common marmoset (Callithrix jacchus). Stem Cells 2005;23:1304–1313.PubMedGoogle Scholar
  93. 93.
    Vrana KE, Hipp JD, Goss AM, McCool BA, Riddle DR, Walker SJ, Wettstein PJ, Studer LP, Tabar V, Cunniff K, Chapman K, Vilner L, West MD, Grant KA, Cibelli JB. Nonhuman primate parthenogenetic stem cells. Proc Natl Acad Sci USA 2003;100: 11911–11916.PubMedGoogle Scholar
  94. 94.
    Li T, Wang S, Xie Y, Lu Y, Zhang X, Wang L, Yang S, Wolf D, Zhou Q, Ji W. Homologous feeder cells support undifferentiated growth and pluripotency in monkey embryonic stem cells. Stem Cells 2005;23:1192–1199.PubMedGoogle Scholar
  95. 95.
    Xu C, Inokuma MS, Denham J, Golds K, Kundu P, Gold JD, Carpenter MK. Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 2001;19:971–974.PubMedGoogle Scholar
  96. 96.
    Levenstein ME, Ludwig TE, Xu RH, Llanas RA, VanDenHeuvel-Kramer K, Manning D, Thomson JA. Basic fibroblast growth factor support of human embryonic stem cell self-renewal. Stem Cells 2006;24:568–574.PubMedGoogle Scholar
  97. 97.
    Byrne J, Mitalipov S, Wolf D. Current progress with primate embryonic stem cells. Curr Stem Cell Res Ther 2006;1:127–138.PubMedGoogle Scholar
  98. 98.
    Fluckiger AC, Marcy G, Marchand M, Negre D, Cosset FL, Mitalipov S, Wolf D, Savatier P, Dehay C. Cell cycle features of primate embryonic stem cells. Stem Cells 2006;24:547–556.PubMedGoogle Scholar
  99. 99.
    Amit M, Carpenter MK, Inokuma MS, Chiu CP, Harris CP, Waknitz MA, Itskovitz-Eldor J, Thomson JA. Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev Biol 2000;227: 271–278.PubMedGoogle Scholar
  100. 100.
    Takada T, Suzuki Y, Kondo Y, Kadota N, Kobayashi K, Nito S, Kimura H, Torii R. Monkey embryonic stem cell lines expressing green fluorescent protein. Cell Transplant 2002; 11:631–635.PubMedGoogle Scholar
  101. 101.
    Ma J, Ramezani A, Lewis R, Hawley RG, Thomson JA. High-level sustained transgene expression in human embryonic stem cells using lentiviral vectors. Stem Cells 2003; 21:111–117.PubMedGoogle Scholar
  102. 102.
    Wang Z, Jaenisch R. At most three ES cells contribute to the somatic lineages of chimeric mice and of mice produced by EStetraploid complementation. Dev Biol 2004;275:192–201.PubMedGoogle Scholar
  103. 103.
    Asano T, Ageyama N, Takeuchi K, Momoeda M, Kitano Y, Sasaki K, Ueda Y, Suzuki Y, Kondo Y, Torii R, Hasegawa M, Ookawara S, Harii K, Terao K, Ozawa K, Hanazono Y. Engraftment and tumor formation after allogeneic in utero transplantation of primate embryonic stem cells. Transplantation 2003;76:1061–1067.PubMedGoogle Scholar
  104. 104.
    Fujimoto A, Mitalipov SM, Kuo HC, Wolf DP. Aberrant genomic imprinting in rhesus monkey embryonic stem cells. Stem Cells 2006;24:595–603.PubMedGoogle Scholar
  105. 105.
    Dean W, Bowden L, Aitchison A, Klose J, Moore T, Meneses JJ, Reik W, Feil R. Altered imprinted gene methylation and expression in completely ES cell-derived mouse fetuses: Association with aberrant phenotypes. Development 1998;125:2273–2282.PubMedGoogle Scholar
  106. 106.
    Rugg-Gunn PJ, Ferguson-Smith AC, Pedersen RA. Epigenetic status of human embryonic stem cells. Nat Genet 2005; 37: 585–587.PubMedGoogle Scholar
  107. 107.
    Nonomura N, Nishimura K, Miki T, Kanno N, Kojima Y, Yokoyama M, Okuyama A. Loss of imprinting of the insulin-like growth factor II gene in renal cell carcinoma. Cancer Res 1997;57:2575–2577.PubMedGoogle Scholar

Copyright information

© Humana Press Inc., Totowa, NJ 2008

Authors and Affiliations

  • Don P. Wolf
    • 1
  • Shoukhrat Mitalipov
    • 1
  • James A. Byrne
    • 1
  1. 1.Oregon National Primate Research CenterOregon Health and Science UniversityBeaverton

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