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Fetal Cell Reprogramming and Transformation

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Fetal Stem Cells in Regenerative Medicine

Part of the book series: Stem Cell Biology and Regenerative Medicine ((STEMCELL))

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Abstract

The fetal cells in primordial organs have the ability to make terminally differentiated cells within the context of embryonic development and organogenesis. Recent advances in the stem cell field confirm the reprogramming capacity of fetal cells to transform into the different cells of the same or other lineages under specific cellular environments called ‘niche.’ In particular, cells existing in primordial organs show multipotent or pluripotent properties, which further emphasizes the importance of these cells in regenerative medicine and tissue engineering in both humans and animals. Reprogramming fetal cells involves manipulations of genetic configuration and changes in both cellular and acellular microenvironments. While this technology is widely used to establish transplantable reprogrammed cells and their derivatives to regenerate or replace damaged tissues, careful considerations should be made in terms of genetic and cellular plasticity as well as anticipated ethical issues. In this chapter, general concepts of fetal cell reprogramming and subsequent phenotypic transformation are reviewed to understand genetic and cellular aspects of cellular plasticity. Potential feasibility of fetal cell manipulation with the consideration of ethical issues has been described subsequently.

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Abbreviations

BMP:

Bone morphogenetic protein

cDNA:

Complementary DNA

CFFs:

Colony forming fibroblasts

CPP:

Cell penetrating protein

DNA:

Deoxyribonucleic acid

ECCs:

Embryonic carcinoma cells

EGCs:

Embryonic germ cells

EMT:

Epithelial-to-mesenchymal transition

ESCs:

Embryonic stem cells

FACS:

Fluorescent activated cell sorter

FGF:

Fibroblast growth factor

FSCs:

Fetal stem cells

GDNF:

Glial-derived neurotrophic factor

HIV:

Human immunodeficiency virus

HSCs:

Hematopoietic stem cells

iPSCs:

Induce pluripotent stem cells

MACS:

Magnetic activated cell sorter

MET:

Mesenchymal-to-epithelial transition

miRNA:

microRNA

MMLV:

Moloney murine leukemia virus

mRNA:

Messenger RNA

MSCs:

Mesenchymal stem cells

NSCs:

Neural stem cells

PB:

Piggyback

PGCs:

Primordial germ cells

RNA:

Ribonucleic acid

ROS:

Reactive oxygen species

SCNT:

Somatic cell nuclear transfer

SLAM:

Signaling lymphocyte activation molecule

SNP:

Single-nucleotide polymorphism

SOP:

Standard operation protocol

SSCs:

Spermatogonial stem cells

TGF:

Transforming growth factor

UCB:

Umbilical cord blood

References

  1. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126(4):663–76.

    Article  CAS  PubMed  Google Scholar 

  2. Wernig M, et al. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature. 2007;448(7151):318–24.

    Article  CAS  PubMed  Google Scholar 

  3. Brambrink T, et al. Sequential expression of pluripotency markers during direct reprogramming of mouse somatic cells. Cell Stem Cell. 2008;2(2):151–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Sommer CA, et al. Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells. 2009;27(3):543–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Fusaki N, et al. Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proc Jpn Acad Ser B Phys Biol Sci. 2009;85(8):348–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Stadtfeld M, et al. Induced pluripotent stem cells generated without viral integration. Science. 2008;322(5903):945–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Wilson MH, Coates CJ, George Jr AL. PiggyBac transposon-mediated gene transfer in human cells. Mol Ther. 2007;15(1):139–45.

    Article  CAS  PubMed  Google Scholar 

  8. Okita K, et al. Generation of mouse induced pluripotent stem cells without viral vectors. Science. 2008;322(5903):949–53.

    Article  CAS  PubMed  Google Scholar 

  9. Gonzalez F, et al. Generation of mouse-induced pluripotent stem cells by transient expression of a single nonviral polycistronic vector. Proc Natl Acad Sci U S A. 2009;106(22):8918–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Yu J, et al. Human induced pluripotent stem cells free of vector and transgene sequences. Science. 2009;324(5928):797–801.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Hu K. All roads lead to induced pluripotent stem cells: the technologies of iPSC generation. Stem Cells Dev. 2014;23(12):1285–300.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Si-Tayeb K, et al. Generation of human induced pluripotent stem cells by simple transient transfection of plasmid DNA encoding reprogramming factors. BMC Dev Biol. 2010;10:81.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Narsinh KH, et al. Generation of adult human induced pluripotent stem cells using nonviral minicircle DNA vectors. Nat Protoc. 2011;6(1):78–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Warren L, et al. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell. 2010;7(5):618–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Anokye-Danso F, et al. Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell. 2011;8(4):376–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Freberg CT, et al. Epigenetic reprogramming of OCT4 and NANOG regulatory regions by embryonal carcinoma cell extract. Mol Biol Cell. 2007;18(5):1543–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Kim D, et al. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell. 2009;4(6):472–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Hansis C, et al. Nuclear reprogramming of human somatic cells by xenopus egg extract requires BRG1. Curr Biol. 2004;14(16):1475–80.

    Article  CAS  PubMed  Google Scholar 

  19. Ding X, et al. The polycomb protein Ezh2 impacts on induced pluripotent stem cell generation. Stem Cells Dev. 2014;23(9):931–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Kabouridis PS. Biological applications of protein transduction technology. Trends Biotechnol. 2003;21(11):498–503.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Sandgren S, Cheng F, Belting M. Nuclear targeting of macromolecular polyanions by an HIV-Tat derived peptide. Role for cell-surface proteoglycans. J Biol Chem. 2002;277(41):38877–83.

    Article  CAS  PubMed  Google Scholar 

  22. Liang G, He J, Zhang Y. Kdm2b promotes induced pluripotent stem cell generation by facilitating gene activation early in reprogramming. Nat Cell Biol. 2012;14(5):457–66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Hou P, et al. Pluripotent stem cells induced from mouse somatic cells by small-molecule compounds. Science. 2013;341(6146):651–4.

    Article  CAS  PubMed  Google Scholar 

  24. Kono T. Nuclear transfer and reprogramming. Rev Reprod. 1997;2(2):74–80.

    Article  CAS  PubMed  Google Scholar 

  25. Wakayama T, et al. Differentiation of embryonic stem cell lines generated from adult somatic cells by nuclear transfer. Science. 2001;292(5517):740–3.

    Article  CAS  PubMed  Google Scholar 

  26. Byrne JA, et al. Producing primate embryonic stem cells by somatic cell nuclear transfer. Nature. 2007;450(7169):497–502.

    Article  CAS  PubMed  Google Scholar 

  27. Wakayama T, et al. Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature. 1998;394(6691):369–74.

    Article  CAS  PubMed  Google Scholar 

  28. Couldrey C, Lee RS. DNA methylation patterns in tissues from mid-gestation bovine foetuses produced by somatic cell nuclear transfer show subtle abnormalities in nuclear reprogramming. BMC Dev Biol. 2010;10:27.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Ross PJ, Cibelli JB. Bovine somatic cell nuclear transfer. Methods Mol Biol. 2010;636:155–77.

    Article  PubMed  Google Scholar 

  30. Cowan CA, et al. Nuclear reprogramming of somatic cells after fusion with human embryonic stem cells. Science. 2005;309(5739):1369–73.

    Article  CAS  PubMed  Google Scholar 

  31. Obokata H, et al. Stimulus-triggered fate conversion of somatic cells into pluripotency. Nature. 2014;505(7485):641–7.

    Article  CAS  PubMed  Google Scholar 

  32. Lee ST, et al. Transformation of somatic cells into stem cell-like cells under a stromal niche. Faseb J. 2013;27(7):2644–56.

    Google Scholar 

  33. Tan KY, et al. Efficient generation of iPS cells from skeletal muscle stem cells. PLoS One. 2011;6(10):e26406.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Kleger A, et al. Increased reprogramming capacity of mouse liver progenitor cells, compared with differentiated liver cells, requires the BAF complex. Gastroenterology. 2012;142(4):907–17.

    Article  PubMed  Google Scholar 

  35. Eminli S, et al. Differentiation stage determines potential of hematopoietic cells for reprogramming into induced pluripotent stem cells. Nat Genet. 2009;41(9):968–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Hansel MC, et al. Increased reprogramming of human fetal hepatocytes compared with adult hepatocytes in feeder-free conditions. Cell Transplant. 2014;23(1):27–38.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. Molecular biology of the cell. New York: Garland Science; 2002.

    Google Scholar 

  38. Twyman R. Developmental biology. Oxford: Bios Scientific Publishers; 2001.

    Google Scholar 

  39. Cinalli RM, Rangan P, Lehmann R. Germ cells are forever. Cell. 2008;132(4):559–62.

    Article  CAS  PubMed  Google Scholar 

  40. Kunwar PS, Lehmann R. Developmental biology: germ-cell attraction. Nature. 2003;421(6920):226–7.

    Article  CAS  PubMed  Google Scholar 

  41. Ginsburg M, Snow MH, McLaren A. Primordial germ cells in the mouse embryo during gastrulation. Development. 1990;110(2):521–8.

    CAS  PubMed  Google Scholar 

  42. Lawson KA, et al. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 1999;13(4):424–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Ying Y, Qi X, Zhao GQ. Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways. Proc Natl Acad Sci U S A. 2001;98(14):7858–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Mei J, et al. C1q-like factor, a target of miR-430, regulates primordial germ cell development in early embryos of Carassius auratus. Int J Biol Sci. 2013;10(1):15–24.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Magnusdottir E, et al. A tripartite transcription factor network regulates primordial germ cell specification in mice. Nat Cell Biol. 2013;15(8):905–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Okamura D, et al. REST and its downstream molecule Mek5 regulate survival of primordial germ cells. Dev Biol. 2012;372(2):190–202.

    Article  CAS  PubMed  Google Scholar 

  47. Childs AJ, et al. LIN28 is selectively expressed by primordial and pre-meiotic germ cells in the human fetal ovary. Stem Cells Dev. 2012;21(13):2343–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Leitch HG, Smith A. The mammalian germline as a pluripotency cycle. Development. 2013;140(12):2495–501.

    Article  CAS  PubMed  Google Scholar 

  49. Leitch HG, Tang WW, Surani MA. Primordial germ-cell development and epigenetic reprogramming in mammals. Curr Top Dev Biol. 2013;104:149–87.

    Article  CAS  PubMed  Google Scholar 

  50. Monk M. A stem-line model for cellular and chromosomal differentiation in early mouse-development. Differentiation. 1981;19(2):71–6.

    Article  CAS  PubMed  Google Scholar 

  51. Monk M, et al. Preimplantation sexing and diagnosis of hypoxanthine phosphoribosyl transferase deficiency in mice by biochemical microassay. Am J Med Genet. 1990;35(2):201–5.

    Article  CAS  PubMed  Google Scholar 

  52. Pesce M, et al. Differential expression of the Oct-4 transcription factor during mouse germ cell differentiation. Mech Dev. 1998;71(1–2):89–98.

    Article  CAS  PubMed  Google Scholar 

  53. Shim H, Anderson GB. In vitro survival and proliferation of porcine primordial germ cells. Theriogenology. 1998;49(3):521–8.

    Article  CAS  PubMed  Google Scholar 

  54. Resnick JL, et al. Long-term proliferation of mouse primordial germ cells in culture. Nature. 1992;359(6395):550–1.

    Article  CAS  PubMed  Google Scholar 

  55. Nagy A, Nagy K, Gertsenstein M. Production of mouse chimeras by aggregating pluripotent stem cells with embryos. Methods Enzymol. 2010;476:123–49.

    Article  CAS  PubMed  Google Scholar 

  56. Gardner RL. Clonal analysis of early mammalian development. Philos Trans R Soc Lond B Biol Sci. 1985;312(1153):163–78.

    Article  CAS  PubMed  Google Scholar 

  57. Gardner RL. Mouse chimeras obtained by the injection of cells into the blastocyst. Nature. 1968;220(5167):596–7.

    Article  CAS  PubMed  Google Scholar 

  58. Gardner RL, Rossant J. Investigation of the fate of 4-5 day post-coitum mouse inner cell mass cells by blastocyst injection. J Embryol Exp Morphol. 1979;52:141–52.

    CAS  PubMed  Google Scholar 

  59. Wang ZQ, et al. Generation of completely embryonic stem cell-derived mutant mice using tetraploid blastocyst injection. Mech Dev. 1997;62(2):137–45.

    Article  CAS  PubMed  Google Scholar 

  60. Nichols J, Smith A. Naive and primed pluripotent states. Cell Stem Cell. 2009;4(6):487–92.

    Article  CAS  PubMed  Google Scholar 

  61. Matsui Y, Zsebo K, Hogan BL. Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell. 1992;70(5):841–7.

    Article  CAS  PubMed  Google Scholar 

  62. Leitch HG, et al. Embryonic germ cells from mice and rats exhibit properties consistent with a generic pluripotent ground state. Development. 2010;137(14):2279–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Sharova LV, et al. Global gene expression profiling reveals similarities and differences among mouse pluripotent stem cells of different origins and strains. Dev Biol. 2007;307(2):446–59.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Durcova-Hills G, Surani A. Reprogramming primordial germ cells (PGC) to embryonic germ (EG) cells. Curr Protoc Stem Cell Biol. 2008;Chapter 1:Unit1A3.

    Google Scholar 

  65. Turnpenny L, et al. Evaluating human embryonic germ cells: concord and conflict as pluripotent stem cells. Stem Cells. 2006;24(2):212–20.

    Article  PubMed  Google Scholar 

  66. Leitch HG, et al. Rebuilding pluripotency from primordial germ cells. Stem Cell Rep. 2013;1(1):66–78.

    Article  CAS  Google Scholar 

  67. Johnson L. Efficiency of spermatogenesis. Microsc Res Tech. 1995;32(5):385–422.

    Article  CAS  PubMed  Google Scholar 

  68. Ryu BY, et al. Conservation of spermatogonial stem cell self-renewal signaling between mouse and rat. Proc Natl Acad Sci U S A. 2005;102(40):14302–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Itman C, et al. All in the family: TGF-beta family action in testis development. Reproduction. 2006;132(2):233–46.

    Article  CAS  PubMed  Google Scholar 

  70. Oatley JM, Brinster RL. Regulation of spermatogonial stem cell self-renewal in mammals. Annu Rev Cell Dev Biol. 2008;24:263–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Barrios F, et al. Opposing effects of retinoic acid and FGF9 on Nanos2 expression and meiotic entry of mouse germ cells. J Cell Sci. 2010;123(Pt 6):871–80.

    Article  CAS  PubMed  Google Scholar 

  72. Tegelenbosch RA, de Rooij DG. A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse. Mutat Res. 1993;290(2):193–200.

    Article  CAS  PubMed  Google Scholar 

  73. Sato T, et al. In vitro sperm production from mouse spermatogonial stem cell lines using an organ culture method. Nat Protoc. 2013;8(11):2098–104.

    Article  CAS  PubMed  Google Scholar 

  74. Jung JG, et al. Development of novel markers for the characterization of chicken primordial germ cells. Stem Cells. 2005;23(5):689–98.

    Article  CAS  PubMed  Google Scholar 

  75. Jung JG, et al. Identification, culture, and characterization of germline stem cell-like cells in chicken testes. Biol Reprod. 2007;76(1):173–82.

    Article  CAS  PubMed  Google Scholar 

  76. Urven LE, et al. Differential gene expression in fetal mouse germ cells. Biol Reprod. 1993;48(3):564–74.

    Article  CAS  PubMed  Google Scholar 

  77. Clermont Y, Perey B. Quantitative study of the cell population of the seminiferous tubules in immature rats. Am J Anat. 1957;100(2):241–67.

    Article  CAS  PubMed  Google Scholar 

  78. Kluin PM, de Rooij DG. A comparison between the morphology and cell kinetics of gonocytes and adult type undifferentiated spermatogonia in the mouse. Int J Androl. 1981;4(4):475–93.

    Article  CAS  PubMed  Google Scholar 

  79. Yoshida S, et al. The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Development. 2006;133(8):1495–505.

    Article  CAS  PubMed  Google Scholar 

  80. Roosen-Runge EC, Giesel Jr LO. Quantitative studies on spermatogenesis in the albino rat. Am J Anat. 1950;87(1):1–30.

    Article  CAS  PubMed  Google Scholar 

  81. Clermont Y, Leblond CP. Renewal of spermatogonia in the rat. Am J Anat. 1953;93(3):475–501.

    Article  CAS  PubMed  Google Scholar 

  82. Monesi V. Autoradiographic study of DNA synthesis and the cell cycle in spermatogonia and spermatocytes of mouse testis using tritiated thymidine. J Cell Biol. 1962;14:1–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Clermont Y, Bustos-Obregon E. Re-examination of spermatogonial renewal in the rat by means of seminiferous tubules mounted “in toto”. Am J Anat. 1968;122(2):237–47.

    Article  CAS  PubMed  Google Scholar 

  84. Dym M, Clermont Y. Role of spermatogonia in the repair of the seminiferous epithelium following x-irradiation of the rat testis. Am J Anat. 1970;128(3):265–82.

    Article  CAS  PubMed  Google Scholar 

  85. Clermont Y, Hermo L. Spermatogonial stem cells in the albino rat. Am J Anat. 1975;142(2):159–75.

    Article  CAS  PubMed  Google Scholar 

  86. Clermont Y, Leblond CP. Differentiation and renewal of spermatogonia in the monkey, Macacus rhesus. Am J Anat. 1959;104:237–73.

    Article  CAS  PubMed  Google Scholar 

  87. Clermont Y, Antar M. Duration of the cycle of the seminiferous epithelium and the spermatogonial renewal in the monkey Macaca arctoides. Am J Anat. 1973;136(2):153–65.

    Article  CAS  PubMed  Google Scholar 

  88. Tilly JL, Johnson J. Recent arguments against germ cell renewal in the adult human ovary: is an absence of marker gene expression really acceptable evidence of an absence of oogenesis? Cell Cycle. 2007;6(8):879–83.

    Article  CAS  PubMed  Google Scholar 

  89. Tilly JL, Telfer EE. Purification of germline stem cells from adult mammalian ovaries: a step closer towards control of the female biological clock? Mol Hum Reprod. 2009;15(7):393–8.

    Article  PubMed  PubMed Central  Google Scholar 

  90. Zheng W, Zhang H, Liu K. The two classes of primordial follicles in the mouse ovary: their development, physiological functions, and implications for future research. Mol Hum Reprod. 2014;20(4):286–92.

    Article  PubMed  Google Scholar 

  91. Johnson J, et al. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature. 2004;428(6979):145–50.

    Article  CAS  PubMed  Google Scholar 

  92. Johnson J, et al. Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell. 2005;122(2):303–15.

    Article  CAS  PubMed  Google Scholar 

  93. Kim IW, et al. Derivation of developmentally competent oocytes by the culture of preantral follicles retrieved from adult ovaries: maturation, blastocyst formation, and embryonic stem cell transformation. Fertil Steril. 2009;92(5):1716–24.

    Article  PubMed  Google Scholar 

  94. Choi JH, et al. Generation of viable embryos and embryonic stem cell-like cells from cultured primary follicles in mice. Biol Reprod. 2011;85(4):744–54.

    Article  CAS  PubMed  Google Scholar 

  95. Lenie S, et al. A reproducible two-step culture system for isolated primary mouse ovarian follicles as single functional units. Biol Reprod. 2004;71(5):1730–8.

    Article  CAS  PubMed  Google Scholar 

  96. Cortvrindt R, Smitz J, Van Steirteghem AC. Assessment of the need for follicle stimulating hormone in early preantral mouse follicle culture in vitro. Hum Reprod. 1997;12(4):759–68.

    Article  CAS  PubMed  Google Scholar 

  97. Makris A, Ryan KJ. Progesterone, androstenedione, testosterone, estrone, and estradiol synthesis in hamster ovarian follicle cells. Endocrinology. 1975;96(3):694–701.

    Article  CAS  PubMed  Google Scholar 

  98. Cecconi S, et al. In vitro development of sheep preantral follicles. Biol Reprod. 1999;60(3):594–601.

    Article  CAS  PubMed  Google Scholar 

  99. Echternkamp SE, et al. Ovarian follicular development in cattle selected for twin ovulations and births. J Anim Sci. 2004;82(2):459–71.

    CAS  PubMed  Google Scholar 

  100. Gougeon A. Dynamics of follicular growth in the human: a model from preliminary results. Hum Reprod. 1986;1(2):81–7.

    CAS  PubMed  Google Scholar 

  101. Liu J, et al. Maturation of mouse primordial follicles by combination of grafting and in vitro culture. Biol Reprod. 2000;62(5):1218–23.

    Article  CAS  PubMed  Google Scholar 

  102. Cortvrindt R, Smitz J, Van Steirteghem AC. In-vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepuberal mice in a simplified culture system. Hum Reprod. 1996;11(12):2656–66.

    Article  CAS  PubMed  Google Scholar 

  103. Eppig JJ, Schroeder AC. Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biol Reprod. 1989;41(2):268–76.

    Article  CAS  PubMed  Google Scholar 

  104. Choi JK, Agarwal P, He X. In vitro culture of early secondary preantral follicles in hanging drop of ovarian cell-conditioned medium to obtain MII oocytes from outbred deer mice. Tissue Eng Part A. 2013;19(23–24):2626–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Sadeu JC, Adriaenssens T, Smitz J. Expression of growth differentiation factor 9, bone morphogenetic protein 15, and anti-Mullerian hormone in cultured mouse primary follicles. Reproduction. 2008;136(2):195–203.

    Article  CAS  PubMed  Google Scholar 

  106. Lee ST, et al. Establishment of autologous embryonic stem cells derived from preantral follicle culture and oocyte parthenogenesis. Fertil Steril. 2008;90(5):1910–20.

    Article  CAS  PubMed  Google Scholar 

  107. Gong SP, et al. Improved establishment of autologous stem cells derived from preantral follicle culture and oocyte parthenogenesis. Stem Cells Dev. 2008;17(4):695–712.

    Article  CAS  PubMed  Google Scholar 

  108. Adriaens I, Cortvrindt R, Smitz J. Differential FSH exposure in preantral follicle culture has marked effects on folliculogenesis and oocyte developmental competence. Hum Reprod. 2004;19(2):398–408.

    Article  CAS  PubMed  Google Scholar 

  109. Revazova ES, et al. Patient-specific stem cell lines derived from human parthenogenetic blastocysts. Cloning Stem Cells. 2007;9(3):432–49.

    Article  CAS  PubMed  Google Scholar 

  110. Cibelli JB, et al. Parthenogenetic stem cells in nonhuman primates. Science. 2002;295(5556):819.

    Article  CAS  PubMed  Google Scholar 

  111. Hirabayashi M, et al. Derivation of embryonic stem cell lines from parthenogenetically developing rat blastocysts. Stem Cells Dev. 2014;23(2):107–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Kaufman MH, Barton SC, Surani MA. Normal postimplantation development of mouse parthenogenetic embryos to the forelimb bud stage. Nature. 1977;265(5589):53–5.

    Article  CAS  PubMed  Google Scholar 

  113. Kaufman MH, et al. Establishment of pluripotential cell lines from haploid mouse embryos. J Embryol Exp Morphol. 1983;73:249–61.

    CAS  PubMed  Google Scholar 

  114. Gong SP, et al. Change in gene expression of mouse embryonic stem cells derived from parthenogenetic activation. Hum Reprod. 2009;24(4):805–14.

    Article  CAS  PubMed  Google Scholar 

  115. Kawahara M, et al. High-frequency generation of viable mice from engineered bi-maternal embryos. Nat Biotechnol. 2007;25(9):1045–50.

    Article  CAS  PubMed  Google Scholar 

  116. Mai Q, et al. Derivation of human embryonic stem cell lines from parthenogenetic blastocysts. Cell Res. 2007;17(12):1008–19.

    Article  CAS  PubMed  Google Scholar 

  117. Ju JY, et al. Establishment of stem cell lines from nuclear transferred and parthenogenetically activated mouse oocytes for therapeutic cloning. Fertil Steril. 2008;89(5 Suppl):1314–23.

    Article  CAS  PubMed  Google Scholar 

  118. Navarro P, et al. A role for the E-cadherin cell-cell adhesion molecule during tumor progression of mouse epidermal carcinogenesis. J Cell Biol. 1991;115(2):517–33.

    Article  CAS  PubMed  Google Scholar 

  119. Onder TT, et al. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res. 2008;68(10):3645–54.

    Article  CAS  PubMed  Google Scholar 

  120. Davies JA. Mesenchyme to epithelium transition during development of the mammalian kidney tubule. Acta Anat (Basel). 1996;156(3):187–201.

    Article  CAS  Google Scholar 

  121. Nakaya Y, et al. Mesenchymal-epithelial transition during somitic segmentation is regulated by differential roles of Cdc42 and Rac1. Dev Cell. 2004;7(3):425–38.

    Article  CAS  PubMed  Google Scholar 

  122. Nakajima Y, et al. Mechanisms involved in valvuloseptal endocardial cushion formation in early cardiogenesis: roles of transforming growth factor (TGF)-beta and bone morphogenetic protein (BMP). Anat Rec. 2000;258(2):119–27.

    Article  CAS  PubMed  Google Scholar 

  123. Li B, et al. Evidence for mesenchymal-epithelial transition associated with mouse hepatic stem cell differentiation. PLoS One. 2011;6(2):e17092.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Samavarchi-Tehrani P, et al. Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell. 2010;7(1):64–77.

    Article  CAS  PubMed  Google Scholar 

  125. Yori JL, et al. Kruppel-like factor 4 inhibits epithelial-to-mesenchymal transition through regulation of E-cadherin gene expression. J Biol Chem. 2010;285(22):16854–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Lim JM, Gong SP. Somatic cell transformation into stem cell-like cells induced by different microenvironments. Organogenesis. 2013;9(4):245–8.

    Google Scholar 

  127. Chang HY, et al. Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci U S A. 2002;99(20):12877–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Lindvall O. Neural transplantation: a hope for patients with Parkinson’s disease. Neuroreport. 1997;8(14):3–10.

    Article  Google Scholar 

  129. Kordower JH, et al. Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson’s disease. N Engl J Med. 1995;332(17):1118–24.

    Article  CAS  PubMed  Google Scholar 

  130. Abdulrazzak H, et al. Biological characteristics of stem cells from foetal, cord blood and extraembryonic tissues. J R Soc Interface. 2010;7 Suppl 6:S689–706.

    Article  PubMed  PubMed Central  Google Scholar 

  131. De Coppi P, et al. Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol. 2007;25(1):100–6.

    Article  PubMed  CAS  Google Scholar 

  132. Weissman IL, Shizuru JA. The origins of the identification and isolation of hematopoietic stem cells, and their capability to induce donor-specific transplantation tolerance and treat autoimmune diseases. Blood. 2008;112(9):3543–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Linch DC, et al. Studies of circulating hemopoietic progenitor cells in human fetal blood. Blood. 1982;59(5):976–9.

    CAS  PubMed  Google Scholar 

  134. Zauli G, et al. In vitro growth of human fetal CD34+ cells in the presence of various combinations of recombinant cytokines under serum-free culture conditions. Br J Haematol. 1994;86(3):461–7.

    Article  CAS  PubMed  Google Scholar 

  135. Tocci A, et al. CD34+ cells from first-trimester fetal blood are enriched in primitive hemopoietic progenitors. Am J Obstet Gynecol. 2003;188(4):1002–10.

    Article  PubMed  Google Scholar 

  136. Shields LE, Andrews RG. Gestational age changes in circulating CD34+ hematopoietic stem/progenitor cells in fetal cord blood. Am J Obstet Gynecol. 1998;178(5):931–7.

    Article  CAS  PubMed  Google Scholar 

  137. Campagnoli C, et al. Circulating hematopoietic progenitor cells in first trimester fetal blood. Blood. 2000;95(6):1967–72.

    CAS  PubMed  Google Scholar 

  138. Clapp DW, et al. Molecular evidence that in situ-transduced fetal liver hematopoietic stem/progenitor cells give rise to medullary hematopoiesis in adult rats. Blood. 1995;86(6):2113–22.

    CAS  PubMed  Google Scholar 

  139. Lim FT, Kanhai HH, Falkenburg JH. Characterization of the human CD34+ hematopoietic progenitor cell compartment during the second trimester of pregnancy. Haematologica. 2005;90(2):173–9.

    PubMed  Google Scholar 

  140. Oguro H, Ding L, Morrison SJ. SLAM family markers resolve functionally distinct subpopulations of hematopoietic stem cells and multipotent progenitors. Cell Stem Cell. 2013;13(1):102–16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Wagner-Souza K, et al. Rhodamine 123 efflux in human subpopulations of hematopoietic stem cells: comparison between bone marrow, umbilical cord blood and mobilized peripheral blood CD34+ cells. Int J Mol Med. 2008;22(2):237–42.

    CAS  PubMed  Google Scholar 

  142. Chou BK, et al. Efficient human iPS cell derivation by a non-integrating plasmid from blood cells with unique epigenetic and gene expression signatures. Cell Res. 2011;21(3):518–29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Broxmeyer HE, et al. Hematopoietic stem/progenitor cells, generation of induced pluripotent stem cells, and isolation of endothelial progenitors from 21- to 23.5-year cryopreserved cord blood. Blood. 2011;117(18):4773–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Rollini P, et al. Long-term expansion of transplantable human fetal liver hematopoietic stem cells. Blood. 2004;103(3):1166–70.

    Article  CAS  PubMed  Google Scholar 

  145. Gallacher L, et al. Identification of novel circulating human embryonic blood stem cells. Blood. 2000;96(5):1740–7.

    CAS  PubMed  Google Scholar 

  146. Holyoake TL, Nicolini FE, Eaves CJ. Functional differences between transplantable human hematopoietic stem cells from fetal liver, cord blood, and adult marrow. Exp Hematol. 1999;27(9):1418–27.

    Article  CAS  PubMed  Google Scholar 

  147. Nava S, et al. Characterization of cells in the developing human liver. Differentiation. 2005;73(5):249–60.

    Article  CAS  PubMed  Google Scholar 

  148. Delaney C, Ratajczak MZ, Laughlin MJ. Strategies to enhance umbilical cord blood stem cell engraftment in adult patients. Expert Rev Hematol. 2010;3(3):273–83.

    Article  PubMed  PubMed Central  Google Scholar 

  149. McGuckin CP, et al. Umbilical cord blood stem cells can expand hematopoietic and neuroglial progenitors in vitro. Exp Cell Res. 2004;295(2):350–9.

    Article  CAS  PubMed  Google Scholar 

  150. Campagnoli C, et al. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood. 2001;98(8):2396–402.

    Article  CAS  PubMed  Google Scholar 

  151. Yu M, et al. Mid-trimester fetal blood-derived adherent cells share characteristics similar to mesenchymal stem cells but full-term umbilical cord blood does not. Br J Haematol. 2004;124(5):666–75.

    Article  PubMed  Google Scholar 

  152. Guillot PV, et al. Human first-trimester fetal MSC express pluripotency markers and grow faster and have longer telomeres than adult MSC. Stem Cells. 2007;25(3):646–54.

    Article  CAS  PubMed  Google Scholar 

  153. Chan J, et al. Galectin-1 induces skeletal muscle differentiation in human fetal mesenchymal stem cells and increases muscle regeneration. Stem Cells. 2006;24(8):1879–91.

    Article  CAS  PubMed  Google Scholar 

  154. Kennea NL, et al. Differentiation of human fetal mesenchymal stem cells into cells with an oligodendrocyte phenotype. Cell Cycle. 2009;8(7):1069–79.

    Article  CAS  PubMed  Google Scholar 

  155. Zhang ZY, et al. Superior osteogenic capacity for bone tissue engineering of fetal compared with perinatal and adult mesenchymal stem cells. Stem Cells. 2009;27(1):126–37.

    Article  PubMed  CAS  Google Scholar 

  156. in’t Anker PS, et al. Mesenchymal stem cells in human second-trimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogeneous multilineage differentiation potential. Haematologica. 2003;88(8):845–52.

    Google Scholar 

  157. Almeida-Porada G, et al. Differentiative potential of human metanephric mesenchymal cells. Exp Hematol. 2002;30(12):1454–62.

    Article  CAS  PubMed  Google Scholar 

  158. Hu Y, et al. Isolation and identification of mesenchymal stem cells from human fetal pancreas. J Lab Clin Med. 2003;141(5):342–9.

    Article  CAS  PubMed  Google Scholar 

  159. Ersek A, et al. Persistent circulating human insulin in sheep transplanted in utero with human mesenchymal stem cells. Exp Hematol. 2010;38(4):311–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Yen BL, et al. Placenta-derived multipotent cells differentiate into neuronal and glial cells in vitro. Tissue Eng Part A. 2008;14(1):9–17.

    Article  CAS  PubMed  Google Scholar 

  161. Anchan RM, et al. Amniocytes can serve a dual function as a source of iPS cells and feeder layers. Hum Mol Genet. 2011;20(5):962–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Kennea NL, Mehmet H. Neural stem cells. J Pathol. 2002;197(4):536–50.

    Article  PubMed  Google Scholar 

  163. Uchida N, et al. Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci U S A. 2000;97(26):14720–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Kim JB, et al. Direct reprogramming of human neural stem cells by OCT4. Nature. 2009;461(7264):649–53.

    Article  CAS  PubMed  Google Scholar 

  165. Kim JB, et al. Oct4-induced pluripotency in adult neural stem cells. Cell. 2009;136(3):411–9.

    Article  CAS  PubMed  Google Scholar 

  166. Gong SP, et al. Embryonic stem cell-like cells established by culture of adult ovarian cells in mice. Fertil Steril. 2010;93(8):2594–601. 2601 e1–9.

    Article  PubMed  Google Scholar 

  167. Pappa KI, Anagnou NP. Novel sources of fetal stem cells: where do they fit on the developmental continuum? Regen Med. 2009;4(3):423–33.

    Article  PubMed  Google Scholar 

  168. Johansson M, Ellegren H, Andersson L. Comparative mapping reveals extensive linkage conservation—but with gene order rearrangements—between the pig and the human genomes. Genomics. 1995;25(3):682–90.

    Article  CAS  PubMed  Google Scholar 

  169. Goureau A, et al. Human and porcine correspondence of chromosome segments using bidirectional chromosome painting. Genomics. 1996;36(2):252–62.

    Article  CAS  PubMed  Google Scholar 

  170. Rettenberger G, et al. Visualization of the conservation of synteny between humans and pigs by heterologous chromosomal painting. Genomics. 1995;26(2):372–8.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Departments of Agricultural Biotechnology, Seoul National University, Seoul, 151-921, South Korea

    Jeong Mook Lim D.V.M., Ph.D. & Ji Yeon Ahn Ph.D.

  2. Cancer Research Institute, Seoul National University Hospital, Seoul, 110-742, South Korea

    Jeong Mook Lim D.V.M., Ph.D.

  3. Research Institutes of Agriculture and Life Sciences, Seoul National University, Seoul, 151-921, South Korea

    Jeong Mook Lim D.V.M., Ph.D.

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  1. Jeong Mook Lim D.V.M., Ph.D.
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  2. Ji Yeon Ahn Ph.D.
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Correspondence to Jeong Mook Lim D.V.M., Ph.D. .

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Editors and Affiliations

  1. Department of Surgery, Childrens Hosp Boston & Harvard Med, Boston, Massachusetts, USA

    Dario O. Fauza

  2. Department of Cellular and Molecular Med, University of Ottawa, Faculty of Medicin, OTTAWA, Ontario, Canada

    Mahmud Bani

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Lim, J.M., Ahn, J.Y. (2016). Fetal Cell Reprogramming and Transformation. In: Fauza, D., Bani, M. (eds) Fetal Stem Cells in Regenerative Medicine. Stem Cell Biology and Regenerative Medicine. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-3483-6_6

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