Pluripotent Stem Cells
Hossein Azizi
Institute for Anatomy and Cell Biology, Department of Neuroanatomy, Medical Faculty, University of Heidelberg, Heidelberg, Germany
Amol University of Special Modern Technologies, Amol, Iran
Department of Stem Cells and Developmental Biology at Cell Science Research Center, Royan Institute for Stem Cell Biology and Technology, ACECR, Tehran, Iran
Search for more papers by this authorAkbar Hajizadeh Moghaddam
Amol University of Special Modern Technologies, Amol, Iran
Search for more papers by this authorThomas Skutella
Institute for Anatomy and Cell Biology, Department of Neuroanatomy, Medical Faculty, University of Heidelberg, Heidelberg, Germany
Search for more papers by this authorHossein Azizi
Institute for Anatomy and Cell Biology, Department of Neuroanatomy, Medical Faculty, University of Heidelberg, Heidelberg, Germany
Amol University of Special Modern Technologies, Amol, Iran
Department of Stem Cells and Developmental Biology at Cell Science Research Center, Royan Institute for Stem Cell Biology and Technology, ACECR, Tehran, Iran
Search for more papers by this authorAkbar Hajizadeh Moghaddam
Amol University of Special Modern Technologies, Amol, Iran
Search for more papers by this authorThomas Skutella
Institute for Anatomy and Cell Biology, Department of Neuroanatomy, Medical Faculty, University of Heidelberg, Heidelberg, Germany
Search for more papers by this authorHossein Baharvand
Search for more papers by this authorNasser Aghdami
Search for more papers by this authorSummary
The combination of pluripotent stem cells and nanotechnology could present a new, promising path towards curing diseases in regenerative medicine and tissue engineering. Pluripotent stem cells (PSCs)can be established from different procedures and have the potential to differentiate into cells of all different germ layers, thereby providing cell sources ranging from more nonspecific to differentiated cells. Understanding the mechanisms for their generation, regulation, gene expression, and differentiation is of great importance. Nanotechnology could definitely provide a sufficient source for different applications with PSCs, including sorting and isolation, scaffolds for the propagation and differentiation in various cell-culture systems, the transplantation of un/differentiated cells from pluripotent cells for therapy, tracing cells, gene delivery system, tissue engineering and immunoassays. In this review we have mostly focused on PSCs and generation of these cells by different approaches, especially from induced pluripotent stem cells (iPSCs) and germ cells, and current applications of nanotechnology in PSC biology.
References
- Evans MJ and MH Kaufman (1981). Establishment in culture of pluripotential cells from mouse embryos. Nature 292(5819): 154–156.
- Thomson JA, J Itskovitz-Eldor, SS Shapiro, MA Waknitz, JJ Swiergiel, VS Marshall, JM Jones (1998). Embryonic stem cell lines derived from human blastocysts. Science, 282(5391): 1145–1147.
- Shamblott MJ, J Axelman, S Wang, EM Bugg, JW Littlefield, PJ Donovan, PD Blumenthal, GR Huggins, JD Gearhart (1998). Derivation of pluripotent stem cells from cultured human primordial germ cells. Proceedings of the National Academy of Sciences USA 95(23): 13726–13731.
- Labosky PA, DP Barlow and BL Hogan (1994). Mouse embryonic germ (EG) cell lines: transmission through the germline and differences in the methylation imprint of insulin-like growth factor 2 receptor (Igf2r) gene compared with embryonic stem (ES) cell lines. Development 120(11): 3197–3204.
- Takahashi K, K Tanabe, M Ohnuki, M Narita, T Ichisaka, K Tomoda, S Yamanaka (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5): 861–872.
- Takahashi K and S Yamanaka (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4): 663–676.
- Lim JJ, HJ Kim, KS Kim, JY Hong, DR Lee (2013). In vitro culture-induced pluripotency of human spermatogonial stem cells. Biomedical Research International 2013: 143028.
- Zhang Z, J Liu, Y Liu, Z Li, WQ Gao, Z He (2013). Generation, characterization and potential therapeutic applications of mature and functional hepatocytes from stem cells. Journal of Cell Physiology 228(2): 298–305.
- Kanatsu-Shinohara M, K Inoue, J Lee, M Yoshimoto, N Ogonuki, H Miki, S Baba, T Kato, Y Kazuki, S Toyokuni, M Toyoshima, et al. (2004). Generation of pluripotent stem cells from neonatal mouse testis. Cell 119(7): 1001–112.
- Conrad S, M Renninger, J Hennenlotter, T Wiesner, L Just, M Bonin, W Aicher, HJ Buhring, U Mattheus, A Mack, HJ Wagner, et al. (2008). Generation of pluripotent stem cells from adult human testis. Nature 456(7220): 344–349.
- Ko K, N Tapia, G Wu, JB Kim, MJ Bravo, P Sasse, T Glaser, D Ruau, DW Han, B Greber, K Hausdorfer, et al. (2009). Induction of pluripotency in adult unipotent germline stem cells. Cell Stem Cell 5(1): 87–96.
- Jiang Y, BN Jahagirdar, RL Reinhardt, RE Schwartz, CD Keene, XR Ortiz-Gonzalez, M Reyes, T Lenvik, T Lund, M Blackstad, J Du, et al. (2002). Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418(6893): 41–49.
- Shin DM, EK Zuba-Surma, W Wu, J Ratajczak, M Wysoczynski, MZ Ratajczak, M Kucia (2009). Novel epigenetic mechanisms that control pluripotency and quiescence of adult bone marrow-derived Oct4(+) very small embryonic-like stem cells. Leukemia 23(11): 2042–2051.
- Farzaneh Z, B Pournasr, M Ebrahimi, N Aghdami, H Baharvand (2010). Enhanced functions of human embryonic stem cell-derived hepatocyte-like cells on three-dimensional nanofibrillar surfaces. Stem Cell Reviews 6(4): 601–610.
- Smith LA and PX Ma (2004). Nano-fibrous scaffolds for tissue engineering. Colloids and Surfaces B: Biointerfaces 39(3): 125–131.
- Wang Z, J Ruan and D Cui (2009). Advances and prospect of nanotechnology in stem cells. Nanoscale Research Letters 4(7): 593–605.
- Yamanaka S (2007). Strategies and new developments in the generation of patient-specific pluripotent stem cells. Cell Stem Cell 1(1): 39–49.
- Heer R, AC Hepburn, SC Williamson, A Kennedy, A El-Sherif, NM Soomro, CD Brown, CN Robson (2013). Renal differentiation from adult spermatogonial stem cells. Renal Failure 35(10): 1387–1391.
- Lister R, M Pelizzola, YS Kida, RD Hawkins, JR Nery, G Hon, J Antosiewicz-Bourget, R O'Malley, R Castanon, S Klugman, M Downes, et al. (2011). Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 471(7336): 68–73.
- Hu BY, JP Weick, J Yu, LX Ma, XQ Zhang, JA Thomson, SC Zhang (2010). Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proceedings of the National Academy of Sciences USA 107(9): 4335–4340.
- Conrad S, Azizi H, Hatami M, Kubista M, Bonin M, Hennenlotter J, Renninger M, Skutella T (2014). Differential gene expression profiling of enriched human spermatogonia after short- and long-term culture. Biomedical Research International 2014: 138350.
- Kossack N, J Meneses, S Shefi, HN Nguyen, S Chavez, C Nicholas, J Gromoll, PJ Turek, RA Reijo-Pera (2009). Isolation and characterization of pluripotent human spermatogonial stem cell-derived cells. Stem Cells 27(1): 138–149.
- Golestaneh N, M Kokkinaki, D Pant, J Jiang, D DeStefano, C Fernandez-Bueno, JD Rone, BR Haddad, GI Gallicano, M Dym (2009). Pluripotent stem cells derived from adult human testes. Stem Cells and Development 18(8): 1115–1126.
- Oatley JM and RL Brinster (2008). Regulation of spermatogonial stem cell self-renewal in mammals. Annual Reviews in Cell Development Biology 24: 263–286.
- Ying QL, J Nichols, I Chambers, A Smith (2003). BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115(3): 281–292.
- Niwa H, T Burdon, I Chambers, A Smith (1998). Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes and Development 12(13): 2048–2060.
- Xu RH, X Chen, DS Li, R Li, GC Addicks, C Glennon, TP Zwaka, JA Thomson (2002). BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nature Biotechnology 20(12): 1261–1264.
- Vallier L, M Alexander and RA Pedersen (2005). Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. Journal of Cell Science 118(19): 4495–509.
- Oatley JM, AV Kaucher, MR Avarbock, RL Brinster (2010). Regulation of mouse spermatogonial stem cell differentiation by STAT3 signaling. Biology of Reproduction 83(3): 427–33.
- Shimizu T, J Ueda, JC Ho, K Iwasaki, L Poellinger, I Harada, Y Sawada (2012). Dual inhibition of Src and GSK3 maintains mouse embryonic stem cells, whose differentiation is mechanically regulated by Src signaling. Stem Cells 30(7): 1394–1404.
- Nichols J and A Smith (2009). Naive and primed pluripotent states. Cell Stem Cell 4(6): 487–492.
- Boyer LA, TI Lee, MF Cole, SE Johnstone, SS Levine, JP Zucker, MG Guenther, RM Kumar, HL Murray, RG Jenner, DK Gifford, et al. (2005). Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122(6): 947–956.
- Xu N, T Papagiannakopoulos, G Pan, JA Thomson, KS Kosik (2009). MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 137(4): 647–658.
- Thomson M, SJ Liu, LN Zou, Z Smith, A Meissner, S Ramanathan (2011). Pluripotency factors in embryonic stem cells regulate differentiation into germ layers. Cell 145(6): 875–889.
- Niwa H, J Miyazaki and AG Smith (2000). Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nature Genetics 24(4): 372–376.
- Oatley JM, JJ Reeves and D. McLean (2004). Biological activity of cryopreserved bovine spermatogonial stem cells during in vitro culture. Biology of Reproduction 71(3): 942–947.
- Masui S, Y Nakatake, Y Toyooka, D Shimosato, R Yagi, K Takahashi, H Okochi, A Okuda, R Matoba, AA Sharov, et al. (2007). Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nature Cell Biology 9(6): 625–635.
- Mitsui K, Y Tokuzawa, H Itoh, K Segawa, M Murakami, K Takahashi, M Maruyama, M Maeda, S Yamanaka (2003). The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113(5): 631–642.
- Zhou Y, S Li, Q Huang, L Xie, X Zhu (2013). Nanog suppresses cell migration by downregulating thymosin beta4 and Rnd3. Journal of Molecular Cell Biology 5(4): 239–249.
- Chambers I, J Silva, D Colby, J Nichols, B Nijmeijer, M Robertson, J Vrana, K Jones, L Grotewold, A Smith (2007). Nanog safeguards pluripotency and mediates germline development. Nature 450(7173): 1230–1234.
- Dang CV (1999). c-Myc target genes involved in cell growth, apoptosis, and metabolism. Molecular and Cell Biology 19(1): 1–11.
- Nakatake Y, J Silva, D Colby, J Nichols, B Nijmeijer, M Robertson, J Vrana, K Jones, L Grotewold, A Smith (2006). Klf4 cooperates with Oct3/4 and Sox2 to activate the Lefty1 core promoter in embryonic stem cells. Molecular and Cell Biology 26(20): 7772–7782.
- Lin S, X Xie, MR Patel, YH Yang, Z Li, F Cao, O Gheysens, Y Zhang, SS Gambhir, JH Rao, et al. (2007).Quantum dot imaging for embryonic stem cells. BMC Biotechnology 7: 67.
- Nagesha D, GS Laevsky, P Lampton, R Banyal, C Warner, C DiMarzio, S Sridhar (2007). In vitro imaging of embryonic stem cells using multiphoton luminescence of gold nanoparticles. International Journal of Nanomedicine 2(4): 813–819.
- Gauthaman K, JR Venugopal, FC Yee, GS Peh, S Ramakrishna, A Bongso (2009). Nanofibrous substrates support colony formation and maintain stemness of human embryonic stem cells. Journal of Cellular and Molecular Medicine 13(9B): 3475–3484.
- Hashemi SM, S Soudi, I Shabani, M Naderi, M Soleimani (2011). The promotion of stemness and pluripotency following feeder-free culture of embryonic stem cells on collagen-grafted 3-dimensional nanofibrous scaffold. Biomaterials 32(30): 7363–7374.
- Nur EKA, I Ahmed, J Kamal, M Schindler, S Meiners (2006). Three-dimensional nanofibrillar surfaces promote self-renewal in mouse embryonic stem cells. Stem Cells 24(2): 426–433.
- Blin G, N Lablack, M Louis-Tisser and, C Nicolas, C Picart, M Puceat (2010). Nano-scale control of cellular environment to drive embryonic stem cells selfrenewal and fate. Biomaterials 31(7): 1742–1750.
- Zhu L, DW Chang, L Dai, Y Hong (2007). DNA damage induced by multiwalled carbon nanotubes in mouse embryonic stem cells. Nano Letters 7(12): 3592–3597.
- Ahamed M, M Karns, M Goodson, J Rowe, SM Hussain, JJ Schlager, Y Hong (2008). DNA damage response to different surface chemistry of silver nanoparticles in mammalian cells. Toxicology and Applied Pharmacology 233(3): 404–410.
- Levenberg S, NF Huang, E Lavik, AB Rogers, J Itskovitz-Eldor, R Langer (2003). Differentiation of human embryonic stem cells on three-dimensional polymer scaffolds. Proceedings of the National Academy of Sciences USA 100(22): 12741–12746.
- Caspi O, A Lesman, Y Basevitch, A Gepstein, G Arbel, IH Habib, L Gepstein, S Levenberg (2007). Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circulation Research 100(2): 263–272.
- Garreta E, E Genove, S Borros, CE Semino (2006). Osteogenic differentiation of mouse embryonic stem cells and mouse embryonic fibroblasts in a three-dimensional self-assembling peptide scaffold. Tissue Engineering 12(8): 2215–2227.
- Zare-Mehrjardi N, MT Khorasani, K Hemmesi, H Mirzadeh, H Azizi, B Sadatnia, M Hatami, S Kiani, J Barzin, H Baharvand (2011). Differentiation of embryonic stem cells into neural cells on 3D poly (D, L-lactic acid) scaffolds versus 2D cultures. International Journal of Artificial Organs 34(10): 1012–1023.
- Kabiri M, M Soleimani, I Shabani, K Futrega, N Ghaemi, HH Ahvaz, E Elahi, MR Doran (2012). Neural differentiation of mouse embryonic stem cells on conductive nanofiber scaffolds. Biotechnology Letters 34(7) 1357–1365.
- Park MV, W Annema, A Salvati, A Lesniak, A Elsaesser, C Barnes, G McKerr, CV Howard, I Lynch, KA Dawson, et al. (2009). In vitro developmental toxicity test detects inhibition of stem cell differentiation by silica nanoparticles. Toxicology and Applied Pharmacology 240(1): 108–116.
- Sridharan I, T Kim and R Wang (2009). Adapting collagen/CNT matrix in directing hESC differentiation. Biochemical and Biophysical Research Communications 381(4): 508–512.
- Levenberg S, JA Burdick, T Kraehenbuehl, R Langer (2005). Neurotrophin-induced differentiation of human embryonic stem cells on three-dimensional polymeric scaffolds. Tissue Engineering 11(3–4): 506–512.
- Evans ND, C Minelli, E Gentleman, V LaPointe, SN Patankar, M Kallivretaki, X Chen, CJ Roberts, MM Stevens (2009). Substrate stiffness affects early differentiation events in embryonic stem cells. European Cells and Materials 18: 1–13; discussion 13–14.
- Itzhaki I, L Maizels, I Huber, L Zwi-Dantsis, O Caspi, A Winterstern, O Feldman, A Gepstein, G Arbel, H Hammerman, et al. (2011). Modelling the long QT syndrome with induced pluripotent stem cells. Nature 471(7337): 225–229.
- Ko K, MJ Arauzo-Bravo, N Tapia, J Kim, Q Lin, C Bernemann, DW Han, L Gentile, P Reinhardt, B Greber, et al. (2010). Human adult germline stem cells in question. Nature 465(7301): E1; discussion E3.
- Chikhovskaya JV, MJ Jonker, A Meissner, TM Breit, S Repping, AM van Pelt (2011). Human testis-derived embryonic stem cell-like cells are not pluripotent, but possess potential of mesenchymal progenitors. Human Reproduction 27: 210–221.
- Airaksinen AJ, M Ahlgren and J Vepsalainen (2002). One-pot synthesis of 3,4-disubstituted 1H-pyrroles from 2-tropanones. Journal of Organic Chemistry 67(14): 5019–5021.