Drug-Induced Naïve iPS Cells Exhibit Better Performance than Primed iPS Cells with Respect to the Ability to Differentiate into Pancreatic β-Cell Lineage
Abstract
:1. Introduction
2. Experimental Section
2.1. Ethical Approval
2.2. Induction of HDDPC-NSCs
2.3. Reverse Transcription-Polymerase Chain Reaction and Densitometric Image Analysis
2.4. Induced Differentiation into Pancreatic β-Cell Lineage
2.5. Teratoma Formation/Tumorigenicity Assay
2.6. Immunostaining and Cytochemical Staining
2.7. Fluorescence Observation
2.8. Statistical Analysis
3. Results
3.1. Formation of Drug-Induced HDDPC-NSCs
3.2. Differentiation Induction toward β-Cell Lineage
3.3. Pancreatic Marker Gene Expression in NSCs-Derived Cells
3.4. Intrapancreatic Grafting of NSCs-Derived Cells Leads to the Generation of Insulin-Positive Cell Mass
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Dabelea, D. The accelerating epidemic of childhood diabetes. Lancet 2009, 373, 1999–2000. [Google Scholar] [CrossRef]
- Shapiro, A.M.; Lakey, J.R.; Ryan, E.A.; Korbutt, G.S.; Toth, E.; Warnock, G.L.; Kneteman, N.M.; Rajotte, R.V. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N. Engl. J. Med. 2000, 343, 230–238. [Google Scholar] [CrossRef] [PubMed]
- Ryan, E.A.; Paty, B.W.; Senior, P.A.; Bigam, D.; Alfadhli, E.; Kneteman, N.M.; Lakey, J.R.; Shapiro, A.J. Five-year follow-up after clinical islet transplantation. Diabetes 2005, 54, 2060–2069. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brons, I.G.; Smithers, L.E.; Trotter, M.W.B.; Rugg-Gunn, P.; Sun, B.; Chuva de Sousa Lopes, S.M.; Howlett, S.K.; Clarkson, A.; Ahrlund-Richter, L.; Pedersen, R.A.; et al. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 2007, 448, 191–195. [Google Scholar] [CrossRef] [PubMed]
- Tesar, P.J.; Chenoweth, J.G.; Brook, F.A.; Davies, T.J.; Evans, E.P.; Mack, D.L.; Gardner, R.L.; McKay, R.D.G. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 2007, 448, 196–199. [Google Scholar] [CrossRef]
- Nichols, J.; Smith, A. Naive and primed pluripotent states. Cell Stem Cell 2009, 4, 487–492. [Google Scholar] [CrossRef] [Green Version]
- Huang, Y.; Osorno, R.; Tsakiridis, A.; Wilson, V. In vivo differentiation potential of epiblast stem cells revealed by chimeric embryo formation. Cell Rep. 2012, 2, 1571–1578. [Google Scholar] [CrossRef] [Green Version]
- Nichols, J.; Smith, A. The origin and identity of embryonic stem cells. Development 2011, 138, 3–8. [Google Scholar] [CrossRef] [Green Version]
- Takahashi, K.; Tanabe, K.; Ohnuki, M.; Narita, M.; Ichisaka, T.; Tomoda, K.; Yamanaka, S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131, 861–872. [Google Scholar] [CrossRef] [Green Version]
- Inada, E.; Saitoh, I.; Kubota, N.; Iwase, Y.; Murakami, T.; Sawami, T.; Yamasaki, Y.; Sato, M. Increased expression of cell surface SSEA-1 is closely associated with naive-like conversion from human deciduous teeth dental pulp cells-derived iPS cells. Int. J. Mol. Sci. 2019, 20, 1651. [Google Scholar] [CrossRef] [Green Version]
- Ying, Q.L.; Wray, J.; Nichols, J.; Batlle-Morera, L.; Doble, B.; Woodgett, J.; Cohen, P.; Smith, A. The ground state of embryonic stem cell self-renewal. Nature 2008, 453, 519–523. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hanna, J.; Cheng, A.W.; Saha, K.; Kim, J.; Lengner, C.J.; Soldner, F.; Cassady, J.P.; Muffat, J.; Carey, B.W.; Jaenisch, R. Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc. Natl. Acad. Sci. USA 2010, 107, 9222–9227. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kilens, S.; Meistermann, D.; Moreno, D.; Chariau, C.; Gaignerie, A.; Reignier, A.; Lelièvre, Y.; Casanova, M.; Vallot, C.; Nedellec, S.; et al. Parallel derivation of isogenic human primed and naive induced pluripotent stem cells. Nat. Commun. 2018, 9, 360. [Google Scholar] [CrossRef] [PubMed]
- Takashima, Y.; Guo, G.; Loos, R.; Nichols, J.; Ficz, G.; Krueger, F.; Oxley, D.; Santos, F.; Clarke, J.; Mansfield, W.; et al. Resetting transcription factor control circuitry toward ground-state pluripotency in human. Cell 2014, 158, 1254–1269. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Theunissen, T.W.; Powell, B.E.; Wang, H.; Mitalipova, M.; Faddah, D.A.; Reddy, J.; Fan, Z.P.; Maetzel, D.; Ganz, K.; Shi, L.; et al. Systematic identification of culture conditions for induction and maintenance of naive human pluripotency. Cell Stem Cell 2014, 15, 471–487. [Google Scholar] [CrossRef] [Green Version]
- Chapman, M.D.; Keir, G.; Petzold, A.; Thompson, E.J. Measurement of high affinity antibodies on antigen-immunoblots. J. Immunol. Methods. 2006, 310, 62–66. [Google Scholar] [CrossRef]
- D’Amour, K.A.; Bang, A.G.; Eliazer, S.; Kelly, O.G.; Agulnick, A.D.; Smart, N.G.; Moorman, M.A.; Kroon, E.; Carpenter, M.K.; Baetge, E.E. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat. Biotechnol. 2006, 24, 1392–1401. [Google Scholar] [CrossRef]
- Kroon, E.; Martinson, L.A.; Kadoya, K.; Bang, A.G.; Kelly, O.G.; Eliazer, S.; Young, H.; Richardson, M.; Smart, N.G.; Cunningham, J.; et al. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat. Biotechnol. 2008, 26, 443–452. [Google Scholar] [CrossRef]
- Sato, M.; Saitoh, I.; Murakami, T.; Kubota, N.; Nakamura, S.; Watanabe, S.; Inada, E. Intrapancreatic parenchymal injection of cells as a useful tool for allowing a small number of proliferative cells to grow in vivo. Int. J. Mol. Sci. 2017, 18, 1678. [Google Scholar] [CrossRef]
- Inada, E.; Saitoh, I.; Kubota, N.; Soda, M.; Matsueda, K.; Murakami, T.; Sawami, T.; Kagoshima, A.; Yamasaki, Y.; Sato, M. Alkaline phosphatase and OCT-3/4 as useful markers for predicting susceptibility of human deciduous teeth-derived dental pulp cells to reprogramming factor-induced iPS cells. J. Investig. Clin. Dent. 2017, 8, e12236. [Google Scholar] [CrossRef]
- Noguchi, H.; Saitoh, I.; Tsugata, T.; Kataoka, H.; Watanabe, M.; Noguchi, Y. Induction of tissue-specific stem cells by reprogramming factors, and tissue-specific selection. Cell Death Differ. 2015, 22, 145–155. [Google Scholar] [CrossRef] [Green Version]
- Saitoh, I.; Sato, M.; Soda, M.; Inada, E.; Iwase, Y.; Murakami, T.; Ohshima, H.; Hayasaki, H.; Noguchi, H. Tissue-specific stem cells obtained by reprogramming of non-obese diabetic (NOD) mouse-derived pancreatic cells confer insulin production in response to glucose. PLoS ONE 2016, 11, e0163580. [Google Scholar] [CrossRef]
- Nelakanti, R.V.; Kooreman, N.G.; Wu, J.C. Teratoma formation: A tool for monitoring pluripotency in stem cell research. Curr. Protoc. Stem. Cell. Biol. 2015, 32, 4A.8.1–4A.8.17. [Google Scholar] [CrossRef] [PubMed]
- Rezania, A.; Bruin, J.E.; Arora, P.; Rubin, A.; Batushansky, I.; Asadi, A.; O’Dwyer, S.; Quiskamp, N.; Mojiban, M.; Albrecht, T.; et al. Reversal of diabetes with insulin-producing cells derived in vitro from human pluripotent stem cells. Nat. Biotechnol. 2014, 32, 1121–1133. [Google Scholar] [CrossRef] [PubMed]
- Petersen, M.B.K.; Azad, A.; Ingvorsen, C.; Hess, K.; Hansson, M.; Grapin-Botton, A.; Honoré, C. Single-cell gene expression analysis of a human ESC model of pancreatic endocrine development reveals different paths to beta-cell differentiation. Stem. Cell Rep. 2017, 9, 1246–1261. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mansour, R.N.; Barati, G.; Soleimani, M.; Ghoraeian, P.; Aleagha, M.N.; Kehtari, M.; Mahboudi, H.; Hosseni, F.; Hassannia, H.; Abazari, M.F.; et al. Generation of high-yield insulin producing cells from human-induced pluripotent stem cells on polyethersulfone nanofibrous scaffold. Artif. Cells Nanomed. Biotechnol. 2018, 46, 733–739. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- D’Amour, K.A.; Agulnick, A.D.; Eliazer, S.; Kelly, O.G.; Kroon, E.; Baetge, E.E. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat. Biotechnol. 2005, 23, 1534–1541. [Google Scholar] [CrossRef] [PubMed]
- Kim, K.; Doi, A.; Wen, B.; Ng, K.; Zhao, R.; Cahan, P.; Kim, J.; Aryee, M.J.; Ji, H.; Ehrlich, L.I.R.; et al. Epigenetic memory in induced pluripotent stem cells. Nature 2010, 467, 285–290. [Google Scholar] [CrossRef] [Green Version]
- Polo, J.M.; Liu, S.; Figueroa, M.E.; Kulalert, W.; Eminli, S.; Tan, K.H.; Apostolou, E.; Statdtfeld, M.; Li, Y.; Shioda, T.; et al. Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat. Biotechnol. 2010, 28, 848–855. [Google Scholar] [CrossRef] [Green Version]
- Doi, A.; Park, I.H.; Wen, B.; Murakami, P.; Aryee, M.J.; Irizarry, R.; Herb, B.; Ladd-Acosta, C.; Rho, J.; Loewer, S.; et al. Differential methylation of tissue- and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat. Genet. 2009, 41, 1350–1353. [Google Scholar] [CrossRef] [Green Version]
- Lister, R.; Pelizzola, M.; Kida, Y.S.; Hawkins, R.D.; Nery, J.R.; Hon, G.; Antosiewicz-Bourget, J.; O’Malley, R.; Castanon, R.; Klugman, S.; et al. Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 2011, 471, 68–73. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ohi, Y.; Qin, H.; Hong, C.; Blouin, L.; Polo, J.M.; Guo, T.; Qi, Z.; Downey, S.L.; Manos, P.D.; Rossi, D.J.; et al. Incomplete DNA methylation underlies a transcriptional memory of somatic cells in human iPS cells. Nat. Cell Biol. 2011, 13, 541–549. [Google Scholar] [CrossRef] [PubMed]
- Theunissen, T.W.; Friedli, M.; He, Y.; Planet, E.; O’Neil, R.C.; Markoulaki, S.; Pontis, J.; Wang, H.; Iouranova, A.; Imbeault, M.; et al. Molecular criteria for defining the naive human pluripotent state. Cell Stem Cell 2016, 19, 502–515. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ware, C.B.; Nelson, A.M.; Mecham, B.; Hesson, J.; Zhou, W.; Jonlin, E.C.; Jimenez-Caliani, A.J.; Deng, X.; Cavanaugh, C.; Cook, S.; et al. Derivation of naive human embryonic stem cells. Proc. Natl. Acad. Sci. USA 2014, 111, 4484–4489. [Google Scholar] [CrossRef] [Green Version]
- Park, T.S.; Zimmerlin, L.; Evans-Moses, R.; Zambidis, E.T. Chemical reversion of conventional human pluripotent stem cells to a naive-like state with improved multilineage differentiation potency. J. Vis. Exp. 2018, 136, 57921. [Google Scholar] [CrossRef]
- Cooke, M.J.; Stojkovic, M.; Przyborski, S.A. Growth of teratomas derived from human pluripotent stem cells is influenced by the graft site. Stem Cells Dev. 2006, 15, 254–259. [Google Scholar] [CrossRef]
- Prokhorova, T.A.; Harkness, L.M.; Frandsen, U.; Ditzel, N.; Schroder, H.D.; Burns, J.S.; Kassem, M. Teratoma formation by human embryonic stem cells is site dependent and enhanced by the presence of matrigel. Stem Cells Dev. 2009, 18, 47–54. [Google Scholar] [CrossRef]
- Blum, B.; Benvenisty, N. Clonal analysis of human embryonic stem cell differentiation into teratomas. Stem Cells 2007, 25, 1924–1930. [Google Scholar] [CrossRef]
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Kiyokawa, Y.; Sato, M.; Noguchi, H.; Inada, E.; Iwase, Y.; Kubota, N.; Sawami, T.; Terunuma, M.; Maeda, T.; Hayasaki, H.; et al. Drug-Induced Naïve iPS Cells Exhibit Better Performance than Primed iPS Cells with Respect to the Ability to Differentiate into Pancreatic β-Cell Lineage. J. Clin. Med. 2020, 9, 2838. https://doi.org/10.3390/jcm9092838
Kiyokawa Y, Sato M, Noguchi H, Inada E, Iwase Y, Kubota N, Sawami T, Terunuma M, Maeda T, Hayasaki H, et al. Drug-Induced Naïve iPS Cells Exhibit Better Performance than Primed iPS Cells with Respect to the Ability to Differentiate into Pancreatic β-Cell Lineage. Journal of Clinical Medicine. 2020; 9(9):2838. https://doi.org/10.3390/jcm9092838
Chicago/Turabian StyleKiyokawa, Yuki, Masahiro Sato, Hirofumi Noguchi, Emi Inada, Yoko Iwase, Naoko Kubota, Tadashi Sawami, Miho Terunuma, Takeyasu Maeda, Haruaki Hayasaki, and et al. 2020. "Drug-Induced Naïve iPS Cells Exhibit Better Performance than Primed iPS Cells with Respect to the Ability to Differentiate into Pancreatic β-Cell Lineage" Journal of Clinical Medicine 9, no. 9: 2838. https://doi.org/10.3390/jcm9092838
APA StyleKiyokawa, Y., Sato, M., Noguchi, H., Inada, E., Iwase, Y., Kubota, N., Sawami, T., Terunuma, M., Maeda, T., Hayasaki, H., & Saitoh, I. (2020). Drug-Induced Naïve iPS Cells Exhibit Better Performance than Primed iPS Cells with Respect to the Ability to Differentiate into Pancreatic β-Cell Lineage. Journal of Clinical Medicine, 9(9), 2838. https://doi.org/10.3390/jcm9092838