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Induced Pluripotent Stem (iPS) Cells pp 451–464Cite as

Generation of iPS Cells from Granulosa Cells

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Part of the book series: Methods in Molecular Biology ((MIMB,volume 1357))

Abstract

Various types of somatic cells can be reprogrammed to induced pluripotent stem (iPS) cells. Somatic stem cells may generate iPS cells more efficiently than do differentiated cells. We show that granulosa cells exhibit characteristic of somatic stem cells and can be reprogrammed to iPS cells more efficiently or with few factors. Here, we describe generation of mouse and pig iPS cells from granulosa cells with high efficiency.

An erratum of the original chapter can be found under DOI 10.1007/7651_2015_308

An erratum to this chapter can be found at http://dx.doi.org/10.1007/7651_2015_308

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References

  1. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676

    Article  PubMed  CAS  Google Scholar 

  2. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–872

    Article  PubMed  CAS  Google Scholar 

  3. Aoi T, Yae K, Nakagawa M, Ichisaka T, Okita K, Takahashi K, Chiba T, Yamanaka S (2008) Generation of pluripotent stem cells from adult mouse liver and stomach cells. Science 321:699–702

    Article  PubMed  CAS  Google Scholar 

  4. Loh YH, Agarwal S, Park IH, Urbach A, Huo H, Heffner GC, Kim K, Miller JD, Ng K, Daley GQ (2009) Generation of induced pluripotent stem cells from human blood. Blood 113:5476–5479

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  5. Aasen T, Raya A, Barrero MJ, Garreta E, Consiglio A, Gonzalez F, Vassena R, Bilic J, Pekarik V, Tiscornia G et al (2008) Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat Biotechnol 26:1276–1284

    Article  PubMed  CAS  Google Scholar 

  6. Haase A, Olmer R, Schwanke K, Wunderlich S, Merkert S, Hess C, Zweigerdt R, Gruh I, Meyer J, Wagner S et al (2009) Generation of induced pluripotent stem cells from human cord blood. Cell Stem Cell 5:434–441

    Article  PubMed  CAS  Google Scholar 

  7. Giorgetti A, Montserrat N, Aasen T, Gonzalez F, Rodriguez-Piza I, Vassena R, Raya A, Boue S, Barrero MJ, Corbella BA et al (2009) Generation of induced pluripotent stem cells from human cord blood using OCT4 and SOX2. Cell Stem Cell 5:353–357

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  8. Tamaoki N, Takahashi K, Tanaka T, Ichisaka T, Aoki H, Takeda-Kawaguchi T, Iida K, Kunisada T, Shibata T, Yamanaka S et al (2010) Dental pulp cells for induced pluripotent stem cell banking. J Dent Res 89:773–778

    Article  PubMed  CAS  Google Scholar 

  9. Yan X, Qin H, Qu C, Tuan RS, Shi S, Huang GT (2010) iPS cells reprogrammed from human mesenchymal-like stem/progenitor cells of dental tissue origin. Stem Cells Dev 19:469–480

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  10. Oda Y, Yoshimura Y, Ohnishi H, Tadokoro M, Katsube Y, Sasao M, Kubo Y, Hattori K, Saito S, Horimoto K et al (2010) Induction of pluripotent stem cells from human third molar mesenchymal stromal cells. J Biol Chem 285:29270–29278

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  11. Brown ME, Rondon E, Rajesh D, Mack A, Lewis R, Feng X, Zitur LJ, Learish RD, Nuwaysir EF (2010) Derivation of induced pluripotent stem cells from human peripheral blood T lymphocytes. PLoS One 5:e11373

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Loh YH, Hartung O, Li H, Guo C, Sahalie JM, Manos PD, Urbach A, Heffner GC, Grskovic M, Vigneault F et al (2010) Reprogramming of T cells from human peripheral blood. Cell Stem Cell 7:15–19

    Article  PubMed  PubMed Central  Google Scholar 

  13. Seki T, Yuasa S, Oda M, Egashira T, Yae K, Kusumoto D, Nakata H, Tohyama S, Hashimoto H, Kodaira M et al (2010) Generation of induced pluripotent stem cells from human terminally differentiated circulating T cells. Cell Stem Cell 7:11–14

    Article  PubMed  CAS  Google Scholar 

  14. Staerk J, Dawlaty MM, Gao Q, Maetzel D, Hanna J, Sommer CA, Mostoslavsky G, Jaenisch R (2010) Reprogramming of human peripheral blood cells to induced pluripotent stem cells. Cell Stem Cell 7:20–24

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  15. Hanna J, Markoulaki S, Schorderet P, Carey BW, Beard C, Wernig M, Creyghton MP, Steine EJ, Cassady JP, Foreman R et al (2008) Direct reprogramming of terminally differentiated mature B lymphocytes to pluripotency. Cell 133:250–264

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  16. Pereira CF, Terranova R, Ryan NK, Santos J, Morris KJ, Cui W, Merkenschlager M, Fisher AG (2008) Heterokaryon-based reprogramming of human B lymphocytes for pluripotency requires Oct4 but not Sox2. PLoS Genet 4:e1000170

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Eminli S, Foudi A, Stadtfeld M, Maherali N, Ahfeldt T, Mostoslavsky G, Hock H, Hochedlinger K (2009) Differentiation stage determines potential of hematopoietic cells for reprogramming into induced pluripotent stem cells. Nat Genet 41:968–976

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  18. Chronowska E (2012) Stem cell characteristics of ovarian granulosa cells - review. Ann Anim Sci 12:151–157

    Article  Google Scholar 

  19. Kossowska-Tomaszczuk K, De Geyter C, De Geyter M, Martin I, Holzgreve W, Scherberich A, Zhang H (2009) The multipotency of luteinizing granulosa cells collected from mature ovarian follicles. Stem Cells 27:210–219

    Article  PubMed  CAS  Google Scholar 

  20. Kossowska-Tomaszczuk K, De Geyter C (2013) Cells with stem cell characteristics in somatic compartments of the ovary. Biomed Res Int 2013:310859

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Zuo B, Yang J, Wang F, Wang L, Yin Y, Dan J, Liu N, Liu L (2012) Influences of lamin A levels on induction of pluripotent stem cells. Biol Open 1:1118–1127

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  22. Meyer N, Penn LZ (2008) Reflecting on 25 years with MYC. Nat Rev Cancer 8:976–990

    Article  PubMed  CAS  Google Scholar 

  23. Rowland BD, Peeper DS (2006) KLF4, p21 and context-dependent opposing forces in cancer. Nat Rev Cancer 6:11–23

    Article  PubMed  CAS  Google Scholar 

  24. Okita K, Ichisaka T, Yamanaka S (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448:313–317

    Article  PubMed  CAS  Google Scholar 

  25. Nakagawa M, Takizawa N, Narita M, Ichisaka T, Yamanaka S (2010) Promotion of direct reprogramming by transformation-deficient Myc. Proc Natl Acad Sci U S A 107:14152–14157

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  26. Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T, Aoi T, Okita K, Mochiduki Y, Takizawa N, Yamanaka S (2008) Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 26:101–106

    Article  PubMed  CAS  Google Scholar 

  27. Miura K, Okada Y, Aoi T, Okada A, Takahashi K, Okita K, Nakagawa M, Koyanagi M, Tanabe K, Ohnuki M et al (2009) Variation in the safety of induced pluripotent stem cell lines. Nat Biotechnol 27:743–745

    Article  PubMed  CAS  Google Scholar 

  28. Shi Y, Do JT, Desponts C, Hahm HS, Scholer HR, Ding S (2008) A combined chemical and genetic approach for the generation of induced pluripotent stem cells. Cell Stem Cell 2:525–528

    Article  PubMed  CAS  Google Scholar 

  29. Eminli S, Utikal J, Arnold K, Jaenisch R, Hochedlinger K (2008) Reprogramming of neural progenitor cells into induced pluripotent stem cells in the absence of exogenous Sox2 expression. Stem Cells 26:2467–2474

    Article  PubMed  CAS  Google Scholar 

  30. Kim JB, Zaehres H, Wu G, Gentile L, Ko K, Sebastiano V, Arauzo-Bravo MJ, Ruau D, Han DW, Zenke M et al (2008) Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature 454:646–650

    Article  PubMed  CAS  Google Scholar 

  31. Giorgetti A, Montserrat N, Rodriguez-Piza I, Azqueta C, Veiga A, Izpisua Belmonte JC (2010) Generation of induced pluripotent stem cells from human cord blood cells with only two factors: Oct4 and Sox2. Nat Protoc 5:811–820

    Article  PubMed  CAS  Google Scholar 

  32. Mao J, Zhang Q, Ye X, Liu K, Liu L (2014) Efficient induction of pluripotent stem cells from granulosa cells by Oct4 and Sox2. Stem Cells Dev 23:779–789

    Article  PubMed  CAS  Google Scholar 

  33. Hou P, Li Y, Zhang X, Liu C, Guan J, Li H, Zhao T, Ye J, Yang W, Liu K et al (2013) Pluripotent stem cells induced from mouse somatic cells by small-molecule compounds. Science 341:651–654

    Article  PubMed  CAS  Google Scholar 

  34. Wakayama T, Perry ACF, Zuccotti M, Johnson KR, Yanagimachi R (1998) Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394:369–374

    Article  PubMed  CAS  Google Scholar 

  35. Wells DN, Misica PM, Tervit HR (1999) Production of cloned calves following nuclear transfer with cultured adult mural granulosa cells. Biol Reprod 60:996–1005

    Article  PubMed  CAS  Google Scholar 

  36. Park K-W, Kühholzer B, Lai L, Macháty Z, Sun Q-Y, Day BN, Prather RS (2001) Development and expression of the green fluorescent protein in porcine embryos derived from nuclear transfer of transgenic granulosa-derived cells. Anim Reprod Sci 68:111–120

    Article  PubMed  CAS  Google Scholar 

  37. Polejaeva IA, Chen S-H, Vaught TD, Page RL, Mullins J, Ball S, Dai Y, Boone J, Walker S, Ayares DL et al (2000) Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407:86–90

    Article  PubMed  CAS  Google Scholar 

  38. Gibbons J, Arat S, Rzucidlo J, Miyoshi K, Waltenburg R, Respess D, Venable A, Stice S (2002) Enhanced survivability of cloned calves derived from roscovitine-treated adult somatic cells. Biol Reprod 66:895–900

    Article  PubMed  CAS  Google Scholar 

  39. Keefer CL, Keyston R, Lazaris A, Bhatia B, Begin I, Bilodeau AS, Zhou FJ, Kafidi N, Wang B, Baldassarre H et al (2002) Production of cloned goats after nuclear transfer using adult somatic cells. Biol Reprod 66:199–203

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Qian Zhang, Xiaoying Ye, Kai Liu, Jihong Yuan, Jiaojiao Li, and Mengyuan Liu for helping with the experiments. We thank important funding by the China MOST National Major Basic Research Program (2011CBA01002, 2009CB941004).

Author information

Authors and Affiliations

  1. State Key Laboratory of Medicinal Chemical Biology, Department of Cell Biology and Genetics, College of Life Sciences, Nankai University, 96 Weijin Road, Tianjin, 300071, China

    Jian Mao & Lin Liu

Authors
  1. Jian Mao
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  2. Lin Liu
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Corresponding author

Correspondence to Lin Liu .

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Editors and Affiliations

  1. Ottawa Hospital Research Institute, Ottawa, Ontario, Canada

    Kursad Turksen

  2. Mount Sinai Hospital Samuel Lunenfeld Research Inst, Toronto, Ontario, Canada

    Andras Nagy

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Mao, J., Liu, L. (2014). Generation of iPS Cells from Granulosa Cells. In: Turksen, K., Nagy, A. (eds) Induced Pluripotent Stem (iPS) Cells. Methods in Molecular Biology, vol 1357. Humana Press, New York, NY. https://doi.org/10.1007/7651_2014_135

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  • DOI: https://doi.org/10.1007/7651_2014_135

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  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-3054-8

  • Online ISBN: 978-1-4939-3055-5

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