Primordial germ cell differentiation of nuclear transfer embryonic stem cells using surface modified electroconductive scaffolds

  • Tarlan Eslami-Arshaghi
  • Saeid Vakilian
  • Ehsan Seyedjafari
  • Abdolreza Ardeshirylajimi
  • Masoud Soleimani
  • Mohammad Salehi
Article
  • 199 Downloads

Abstract

A combination of nanotopographical cues and surface modification of collagen and fibronectin is a potential platform in primordial germ cells (PGCs) differentiation. In the present study, the synergistic effect of nanotopography and surface modification on differentiation of nuclear transfer embryonic stem cells (nt-ESCs) toward PGC lineage was investigated. In order to achieve this goal, poly-anyline (PANi) was mix within poly-l-lactic acid (PLLA). Afterward, the random composite mats were fabricated using PLLA and PANi mix solution. The nanofiber topography notably upregulated the expressions of prdm14, mvh and c-kit compared with tissue culture polystyrene (TCP). Moreover, the combination of nanofiber topography and surface modification resulted in more enhancement of PGCs differentiation compared with non-modified nanofibrous scaffold. Additionally, gene expression results showed that mvh and c-kit were expressed at higher intensity in cells exposed to collagen and fibronectin rather than collagen or fibronectin solitary. These results demonstrated the importance of combined effect of collagen and fibronectin in order to develop a functional extracellular matrix (ECM) mimic in directing stem cell fate and the potential of such biofunctional scaffolds for treatment of infertility.

Keywords

Nuclear transfer embryonic stem cells Primordial germ cells Collagen Fibronectin Electroconductive scaffolds 

References

  1. Alsberg E, von Recum HA, Mahoney MJ (2006) Environmental cues to guide stem cell fate decision for tissue engineering applications. Expert Opin Biol Ther 6:847–866CrossRefPubMedGoogle Scholar
  2. Battista S, Guarnieri D, Borselli C, Zeppetelli S, Borzacchiello A, Mayol L, Gerbasio D, Keene DR, Ambrosio L, Netti PA (2005) The effect of matrix composition of 3D constructs on embryonic stem cell differentiation. Biomaterials 26:6194–6207CrossRefPubMedGoogle Scholar
  3. Bhartiya D, Hinduja I, Patel H, Bhilawadikar R (2014) Making gametes from pluripotent stem cells-a promising role for very small embryonic-like stem cells. Reprod Biol Endocrinol 12:114CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bianco P, Robey PG (2001) Stem cells in tissue engineering. Nature 414:118–121CrossRefPubMedGoogle Scholar
  5. Bongso A, Fong CY, Gauthaman K (2008) Taking stem cells to the clinic: major challenges. J Cell Biochem 105:1352–1360CrossRefPubMedGoogle Scholar
  6. Castrillon DH, Quade BJ, Wang T, Quigley C, Crum CP (2000) The human VASA gene is specifically expressed in the germ cell lineage. Proc Natl Acad Sci 97:9585–9590CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chu GC, Dunn NR, Anderson DC, Oxburgh L, Robertson EJ (2004) Differential requirements for Smad4 in TGFβ-dependent patterning of the early mouse embryo. Development 131:3501–3512CrossRefPubMedGoogle Scholar
  8. Chuma S, Kanatsu-Shinohara M, Inoue K, Ogonuki N, Miki H, Toyokuni S, Hosokawa M, Nakatsuji N, Ogura A, Shinohara T (2005) Spermatogenesis from epiblast and primordial germ cells following transplantation into postnatal mouse testis. Development 132:117–122CrossRefPubMedGoogle Scholar
  9. Clark AT, Bodnar MS, Fox M, Rodriquez RT, Abeyta MJ, Firpo MT, Pera RAR (2004) Spontaneous differentiation of germ cells from human embryonic stem cells in vitro. Hum Mol Genet 13:727–739CrossRefPubMedGoogle Scholar
  10. De Miguel MP, Cheng L, Holland EC, Federspiel MJ, Donovan PJ (2002) Dissection of the c-kit signaling pathway in mouse primordial germ cells by retroviral-mediated gene transfer. Proc Natl Acad Sci 99:10458–10463CrossRefPubMedPubMedCentralGoogle Scholar
  11. Doshi J, Reneker, DH (1993) Electrospinning process and applications of electrospun fibers. Industry Applications Society Annual Meeting, 1993, Conference Record of the 1993 IEEE. IEEE, pp. 1698–1703Google Scholar
  12. Eslami-Arshaghi T, Salehi M, Soleimani M, Gholipourmalekabadi M, Mossahebi-Mohammadi M, Ardeshirylajimi A, Rajabi H (2015) Lymphoid lineage differentiation potential of mouse nuclear transfer embryonic stem cells. Biologicals 43:349–354CrossRefPubMedGoogle Scholar
  13. Farifteh F, Salehi M, Bandehpour M, Nariman M, Novin MG, Hosseini T, Nematollahi S, Noroozian M, Keshavarzi S, Hosseini A (2014) Histone modification of embryonic stem cells produced by somatic cell nuclear transfer and fertilized blastocysts. Cell Journal (Yakhteh) 15:316Google Scholar
  14. Feng Q, Lu SJ, Klimanskaya I, Gomes I, Kim D, Chung Y, Honig GR, Kim KS, Lanza R (2010) Hemangioblastic derivatives from human induced pluripotent stem cells exhibit limited expansion and early senescence. Stem Cells 28:704–712CrossRefPubMedGoogle Scholar
  15. Gauthaman K, Venugopal JR, Yee FC, Peh GSL, Ramakrishna S, Bongso A (2009) Nanofibrous substrates support colony formation and maintain stemness of human embryonic stem cells. J Cell Mol Med 13:3475–3484CrossRefPubMedPubMedCentralGoogle Scholar
  16. Geijsen N, Horoschak M, Kim K, Gribnau J, Eggan K, Daley GQ (2004) Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature 427:148–154CrossRefPubMedGoogle Scholar
  17. Ghasemi-Mobarakeh L, Prabhakaran MP, Tian L, Shamirzaei-Jeshvaghani E, Dehghani L, Ramakrishna S (2015) Structural properties of scaffolds: crucial parameters towards stem cells differentiation. World Journal of Stem Cells 7:728CrossRefPubMedPubMedCentralGoogle Scholar
  18. Ginsburg M, Snow M, McLAREN A (1990) Primordial germ cells in the mouse embryo during gastrulation. Development 110:521–528PubMedGoogle Scholar
  19. Halley-Stott RP, Pasque V, Gurdon J (2013) Nuclear reprogramming. Development 140:2468–2471CrossRefPubMedGoogle Scholar
  20. Hayashi K, de Sousa Lopes SMC, Surani MA (2007) Germ cell specification in mice. Science 316:394–396CrossRefPubMedGoogle Scholar
  21. Hübner K, Fuhrmann G, Christenson LK, Kehler J, Reinbold R, De La Fuente R, Wood J, Strauss JF, Boiani M, Schöler HR (2003) Derivation of oocytes from mouse embryonic stem cells. Science 300:1251–1256CrossRefPubMedGoogle Scholar
  22. Kehler J, Tolkunova E, Koschorz B, Pesce M, Gentile L, Boiani M, Lomelí H, Nagy A, McLaughlin KJ, Schöler HR (2004) Oct4 is required for primordial germ cell survival. EMBO Rep 5:1078–1083CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kim K, Doi A, Wen B, Ng K, Zhao R, Cahan P, Kim J, Aryee M, Ji H, Ehrlich L (2010) Epigenetic memory in induced pluripotent stem cells. Nature 467:285–290CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kobolak J, Mamo S, Rungsiwiwut R, Ujhelly O, Csonka E, Hadlaczky G, Dinnyes A (2012) Comparative analysis of nuclear transfer embryo-derived mouse embryonic stem cells. Part I: cellular characterization. Cellular Reprogramming (Formerly “Cloning and Stem Cells”) 14:56–67Google Scholar
  25. Lacham-Kaplan O, Chy H, Trounson A (2006) Testicular cell conditioned medium supports differentiation of embryonic stem cells into ovarian structures containing oocytes. Stem Cells 24:266–273CrossRefPubMedGoogle Scholar
  26. Laflamme MA, Chen KY, Naumova AV, Muskheli V, Fugate JA, Dupras SK, Reinecke H, Xu C, Hassanipour M, Police S (2007) Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25:1015–1024CrossRefPubMedGoogle Scholar
  27. Levenberg S, Huang NF, Lavik E, Rogers AB, Itskovitz-Eldor J, Langer R (2003) Differentiation of human embryonic stem cells on three-dimensional polymer scaffolds. Proc Natl Acad Sci 100:12741–12746CrossRefPubMedPubMedCentralGoogle Scholar
  28. Li W-J, Tuli R, Huang X, Laquerriere P, Tuan RS (2005) Multilineage differentiation of human mesenchymal stem cells in a three-dimensional nanofibrous scaffold. Biomaterials 26:5158–5166CrossRefPubMedGoogle Scholar
  29. Lutolf M, Hubbell J (2005) Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 23:47–55CrossRefPubMedGoogle Scholar
  30. MacGregor GR, Zambrowicz BP, Soriano P (1995) Tissue non-specific alkaline phosphatase is expressed in both embryonic and extraembryonic lineages during mouse embryogenesis but is not required for migration of primordial germ cells. Development 121:1487–1496PubMedGoogle Scholar
  31. Mansouri V, Salehi M, Nourozian M, Fadaei F, Farahani RM, Piryaei A, Delbari A (2015) The ability of mouse nuclear transfer embryonic stem cells to differentiate into primordial germ cells. Genet Mol Biol 38:220–226CrossRefPubMedPubMedCentralGoogle Scholar
  32. Marcho C, Cui W, Mager J (2015) Epigenetic dynamics during preimplantation development. Reproduction 150:R109–R120CrossRefPubMedPubMedCentralGoogle Scholar
  33. Mintz B, Russell ES (1957) Gene-induced embryological modifications of primordial germ cells in the mouse. J Exp Zool 134:207–237CrossRefPubMedGoogle Scholar
  34. Nayernia K, Nolte J, Michelmann HW, Lee JH, Rathsack K, Drusenheimer N, Dev A, Wulf G, Ehrmann IE, Elliott DJ (2006) In vitro-differentiated embryonic stem cells give rise to male gametes that can generate offspring mice. Dev Cell 11:125–132CrossRefPubMedGoogle Scholar
  35. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Schöler H, Smith A (1998) Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95:379–391CrossRefPubMedGoogle Scholar
  36. Nikolic A, Volarevic V, Armstrong L, Lako M, Stojkovic M (2015) Primordial germ cells: current knowledge and perspectives. Stem Cells Int 2015:1741072Google Scholar
  37. Niwa H, Miyazaki J-i, Smith AG (2000) Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24:372–376CrossRefPubMedGoogle Scholar
  38. Ogawa T, Dobrinski I, Avarbock MR, Brinster RL (2000) Transplantation of male germ line stem cells restores fertility in infertile mice. Nat Med 6:29–34CrossRefPubMedPubMedCentralGoogle Scholar
  39. Ohinata Y, Payer B, O’Carroll D, Ancelin K, Ono Y, Sano M, Barton SC, Obukhanych T, Nussenzweig M, Tarakhovsky A (2005) Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436:207–213CrossRefPubMedGoogle Scholar
  40. Prabhakaran MP, Mobarakeh LG, Kai D, Karbalaie K, Nasr-Esfahani MH, Ramakrishna S (2014) Differentiation of embryonic stem cells to cardiomyocytes on electrospun nanofibrous substrates. J Biomed Mater Res B Appl Biomater 102:447–454CrossRefPubMedGoogle Scholar
  41. Print CG, Loveland KL (2000) Germ cell suicide: new insights into apoptosis during spermatogenesis. BioEssays 22:423–430CrossRefPubMedGoogle Scholar
  42. Richardson TP, Peters MC, Ennett AB, Mooney DJ (2001) Polymeric system for dual growth factor delivery. Nat Biotechnol 19:1029–1034CrossRefPubMedGoogle Scholar
  43. Saitou M (2009) Specification of the germ cell lineage in mice. Front Biosci 14:1068–1087CrossRefGoogle Scholar
  44. Saitou M, Yamaji M (2012) Primordial germ cells in mice. Cold Spring Harb Perspect Biol 4:a008375CrossRefPubMedPubMedCentralGoogle Scholar
  45. Salehi M, Ardeshirylajimi A, Mossahebi-Mohammadi M, Kondori Z, Jorjani M (2015) Oligodendrocyte progenitor cells differentiation of nuclear transferred mouse embryonic stem cells. Cell Mol Biol 61:56–59PubMedGoogle Scholar
  46. Sgarioto M, Vigneron P, Patterson J, Malherbe F, Nagel M-D, Egles C (2012) Collagen type I together with fibronectin provide a better support for endothelialization. Comptes rendus biologies 335:520–528CrossRefPubMedGoogle Scholar
  47. Sharma R, Biedenharn KR, Fedor JM, Agarwal A (2013) Lifestyle factors and reproductive health: taking control of your fertility. Reprod Biol Endocrinol 11:1CrossRefGoogle Scholar
  48. Shim J, Kim S, Woo D, Kim S, Oh C, McKay R, Kim J (2007) Directed differentiation of human embryonic stem cells towards a pancreatic cell fate. Diabetologia 50:1228–1238CrossRefPubMedGoogle Scholar
  49. Solter D (2006) From teratocarcinomas to embryonic stem cells and beyond: a history of embryonic stem cell research. Nat Rev Genet 7:319–327CrossRefPubMedGoogle Scholar
  50. Stoop H, Honecker F, Van de Geijn G, Gillis A, Cools M, de Boer M, Bokemeyer C, Wolffenbuttel K, Drop S, De Krijger R (2008) Stem cell factor as a novel diagnostic marker for early malignant germ cells. J Pathol 216:43–54CrossRefPubMedGoogle Scholar
  51. Toyooka Y, Tsunekawa N, Akasu R, Noce T (2003) Embryonic stem cells can form germ cells in vitro. Proc Natl Acad Sci 100:11457–11462CrossRefPubMedPubMedCentralGoogle Scholar
  52. Tremblay KD, Dunn NR, Robertson EJ (2001) Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development 128:3609–3621PubMedGoogle Scholar
  53. Tres LL, Rosselot C, Kierszenbaum AL (2004) Primordial germ cells: what does it take to be alive? Mol Reprod Dev 68:1–4CrossRefPubMedGoogle Scholar
  54. Vacanti JP, Langer R (1999) Tissue engineering: the design and fabrication of living replacement devices for surgical reconstruction and transplantation. Lancet 354:S32–S34CrossRefGoogle Scholar
  55. Vogelstein B, Alberts B, Shine K (2002) Please don’t call it cloning! Science 295:1237–1237CrossRefPubMedGoogle Scholar
  56. Yamaguchi S, Kurimoto K, Yabuta Y, Sasaki H, Nakatsuji N, Saitou M, Tada T (2009) Conditional knockdown of Nanog induces apoptotic cell death in mouse migrating primordial germ cells. Development 136:4011–4020CrossRefPubMedGoogle Scholar
  57. Yamaji M, Seki Y, Kurimoto K, Yabuta Y, Yuasa M, Shigeta M, Yamanaka K, Ohinata Y, Saitou M (2008) Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat Genet 40:1016–1022CrossRefPubMedGoogle Scholar
  58. Yang D, Zhang ZJ, Oldenburg M, Ayala M, Zhang SC (2008) Human embryonic stem cell-derived dopaminergic neurons reverse functional deficit in parkinsonian rats. Stem Cells 26:55–63CrossRefPubMedGoogle Scholar
  59. Yin Z, Chen X, Song H-x, Hu J-j, Tang Q-m, Zhu T, Shen W-l, Chen J-l, Liu H, Heng BC (2015) Electrospun scaffolds for multiple tissues regeneration in vivo through topography dependent induction of lineage specific differentiation. Biomaterials 44:173–185CrossRefPubMedGoogle Scholar
  60. Ying Y, Qi X, Zhao G-Q (2001) Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways. Proc Natl Acad Sci 98:7858–7862CrossRefPubMedPubMedCentralGoogle Scholar
  61. Yoo HS, Kim TG, Park TG (2009) Surface-functionalized electrospun nanofibers for tissue engineering and drug delivery. Adv Drug Deliv Rev 61:1033–1042CrossRefPubMedGoogle Scholar
  62. Zhou P, Lian H-Y, Cui W, Wei D-L, Li Q, Liu Y-X, Liu X-Y, Tan J-H (2012) Maternal-restraint stress increases oocyte aneuploidy by impairing metaphase I spindle assembly and reducing spindle assembly checkpoint proteins in mice. Biol Reprod 86:83CrossRefPubMedGoogle Scholar

Copyright information

© The Society for In Vitro Biology 2016

Authors and Affiliations

  • Tarlan Eslami-Arshaghi
    • 1
  • Saeid Vakilian
    • 1
  • Ehsan Seyedjafari
    • 2
  • Abdolreza Ardeshirylajimi
    • 1
    • 3
  • Masoud Soleimani
    • 4
  • Mohammad Salehi
    • 5
    • 6
  1. 1.Stem Cells Technology Research CenterTehranIran
  2. 2.Department of Biotechnology, College of ScienceUniversity of TehranTehranIran
  3. 3.Department of Tissue Engeneering and Regenerative Medicine, School of Advanced Technologies in MedicineShahid Beheshti University of Medical SciencesTehranIran
  4. 4.Department of Hematology and Blood Banking, Faculty of Medical SciencesTarbiat Modares UniversityTehranIran
  5. 5.Cellular and Molecular Biology Research CenterShahid Beheshti University of Medical SciencesTehranIran
  6. 6.Department of Biotechnology, School of Advanced Technologies in MedicineShahid Beheshti University of Medical SciencesTehranIran

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