Generic placeholder image

Current Stem Cell Research & Therapy

Editor-in-Chief

ISSN (Print): 1574-888X
ISSN (Online): 2212-3946

Research Article

Evaluation of Pancreatic β-cell Differentiation Efficiency of Human iPSC Lines for Clinical Use

Author(s): Ayumi Horikawa, Kyoko Tsuda, Takayoshi Yamamoto and Tatsuo Michiue*

Volume 19, Issue 11, 2024

Published on: 05 January, 2024

Page: [1449 - 1460] Pages: 12

DOI: 10.2174/011574888X267226231126185532

Price: $65

Abstract

Background: Transplantation of pancreatic β-cells generated from human induced pluripotent stem cells (hiPSCs) has great potential as a root treatment for type 1 diabetes. However, their current level of efficiency to differentiate into β-cells is still not at par for clinical use. Previous research has shown that differentiation efficiency varies among human embryonic stem cells and mouse-induced pluripotent stem cell lines. Therefore, selecting a suitable cell line for efficient induction into desired tissues and organs is crucial.

Methods: In this study, we have evaluated the efficiency of 15 hiPSC lines available for clinical use to differentiate into pancreatic β-cells.

Results: Our investigation has revealed induction efficiency to differ among the hiPSC lines, even when derived from the same donor. Among the hiPSC lines tested, the 16A01 cell line exhibited the highest Insulin expression and low Glucagon expression, suggesting that this cell line is suitable for differentiation into β-cells.

Conclusion: Our study has demonstrated the importance of selecting a suitable hiPSC line for effective differentiation into β-cells.

Keywords: iPS cells, β-cells , regenerative medicine, diabetes, insulin, stem cell, pancreas.

Graphical Abstract
[1]
Foster, N.C.; Beck, R.W.; Miller, K.M.; Clements, M.A.; Rickels, M.R.; DiMeglio, L.A.; Maahs, D.M.; Tamborlane, W.V.; Bergenstal, R.; Smith, E.; Olson, B.A.; Garg, S.K. State of type 1 diabetes management and outcomes from the T1D exchange in 2016–2018. Diabetes Technol. Ther., 2019, 21(2), 66-72.
[http://dx.doi.org/10.1089/dia.2018.0384] [PMID: 30657336]
[2]
Miller, K.M.; Hermann, J.; Foster, N.; Hofer, S.E.; Rickels, M.R.; Danne, T.; Clements, M.A.; Lilienthal, E.; Maahs, D.M.; Holl, R.W.; Weinstock, R.; Izquierdo, R.; Sheikh, U.; Conboy, P.; Bulger, J.; Bzdick, S.; Klingensmith, G.; Banion, C.; Barker, J.; Cain, C.; Nadeau, K.; Rewers, M.; Rewers, A.; Slover, R.; Steck, A.; Wadwa, P.; Zeitler, P.; Alonso, G.; Forlenza, G.; Gerard-Gonzalez, A.; Green, M.; Gross, S.; Majidi, S.; Messer, L.; Reznick-Lipina, T.; Simmons, E.; Thivener, K.; Weber, I.; Willi, S.; Lipman, T.; Kucheruk, O.; Minnock, P.; Carchidi, C.; Grant, B.; Olivos, D.; DiMeglio, L.; Hannon, T.; Evans-Molina, C.; Hansen, D.; Pottorff, T.; Woerner, S.; Hildinger, M.; Hufferd, R.; Newnum, A.; Purtlebaugh, D.; Smith, L.; Wendholt, K.; Goland, R.; Gandica, R.; Williams, K.; Pollack, S.; Casciano, E.; Hochberg, J.; Uche, C.; Lee, J.; Gregg, B.; Tan, M.; Ang, L.; Pop-Busui, R.; Thomas, I.; Dhadphale, E.; Dominowski, J.; Garrity, A.; Leone, V.; Plunkett, C.; Plunkett, B.; Monzavi, R.; Cheung, C.; Fisher, L.; Kim, M.; Miyazaki, B.; Pitukcheewanont, P.; Sandstrom, A.; Austin, J.; Change, N.; Raymond, J.; Ichihara, B.; Lipton, M.; Flores Garcia, J.; Garg, S.; Michels, A.; Garcetti, R.; Green, M.; Gutin, R.; Nadeau, K.; Polsky, S.; Shah, V.; Voelmle, M.; Myers, L.; Coe, G.; Demmitt, J.; Garcia Reyes, Y.; Giordano, D.; Joshee, P.; Nease, E.; Nguyen, N.; Wolfsdorf, J.; Quinn, M.; Fontanet, C.; Mukherjee, S.; Bethin, K.; Quattrin, T.; Majumdar, I.; Mastrandrea, L.; Gorman, E.; House, A.; Michalovic, S.; Musial, W.; Shine, B.; Ahmann, A.; Castle, J.; Joarder, F.; Aby-Daniel, D.; Guttmann-Bauman, I.; Klopfenstein, B.; Morimoto, V.; Cady, N.; Fitch, R.; DeFrang, D.; Jahnke, K.; Patoine, C.; Raman, V.; Foster, C.; Murray, M.; Brown, T.; Davis, C.; Slater, H.; Langvardt, J.; Bode, B.; Boyd, J.; Johnson, J.; Newton, C.; Ownby, J.; Hosey, R.S.; Rastogi, N.; Winslett, B.; Hirsch, I.; DeSantis, A.; Failor, R.A.; Greenbaum, C.; Trence, D.; Trikudanathan, S.; Khakpour, D.; Thomson, P.; Sameshima, L.; Tordillos, C.; Clements, M.; Turpin, A.; Babar, G.; Broussard, J.; Cernich, J.; Dileepan, K.; Feldt, M.; Moore, W.; Musick, T.; Patton, S.; Yan, Y.; Tsai, S.; Bedard, J.; Elrod, A.; Hester, L.; Beidelschies, M.; de la Garza, J.; Haith, E.; James, J.; Ramey, E.; Slover, J.; Valentine, A.; Watkins, D.; Whisenhunt, M.; Wierson, J.; Wilson, D.; Buckingham, B.; Maahs, D.; Prahalad, P.; Hsu, L.; Kingman, R.; Tabatabai, I.; Liljenquist, D.; Sulik, M.; Vance, C.; Halford, J.; Funke, C.; Appiagyei-Dankah, Y.; Beltz, E.; Moran, K.; Starkman, H.; Cerame, B.; Chin, D.; Ebner-Lyon, L.; Sabanosh, K.; Silverman, L.; Wagner, C.; Cheruvu, S.; Fox, M.; Melchionne, F.; Bergenstal, R.; Madden, M.; Martens, T.; Criego, A.; Powers, M.; Carlson, A.; Beasley, S.; Olson, B.; Thomas, L.A.; McCann, K.; Dunnigan, S.; Ashanti, C.; Simmons, J.; Russell, W.; Jaser, S.; Kelley, J.; Brendle, F.; Williams, L.; Savin, K.; Flowers, K.; Williams, G.; Hamburger, E.; Davis, A.; Hammel, B.; Cengiz, E.; Tamborlane, W.; Weyman, K.; Van Name, M.; Patel, N.; Sherr, J.; Tichy, E.; Steffen, A.; Zgorski, M.; Carria, L.; Finnegan, J.; Duran, E.; Mehta, S.; Katz, M.; Laffel, L.; Giani, E.; Snelgrove, R.; Hanono, A.; Commissariat, P.; Griffith, J.; Atkins, A.; Harrington, K.; Kim, K.; Masclans, L.; Naik, N.; Ambler-Osborn, L.; Schultz, A.; Cohen, C.; Anderson, B.; McGill, J.; Granados, A.; Clifton, M.J.; Hurst, S.; Kissel, S.; Recklein, C.; Kruger, D.; Bhan, A.; Brown, T.; Tassopoulos, A.; Hailey, A.; Remtema, H.; Cushman, T.; Wintergerst, K.; Watson, S.; Kingery, S.; Rayborn, L.; Rush, H.; Foster, M.; Deuser, A.; Rodriguez-Luna, M.; Eubanks, S.; Rodriguez, H.; Bollepalli, S.; Smith, L.; Shulman, D.; Jorgensen, E.V.; Eyth, E.; Brownstein, R.; Rodriguez, J.; O’Bria, J.; Aleppo-Kacmarek, G.; Hahr, A.; Molitch, M.; Muayed, E.; Toft, D.; Fulkerson, C.; Adelman, D.; Massaro, E.; Webb, K.; Peters, A.; Ruelas, V.; Harmel, M.; Daniels, M.; Forghani, N.; Flannery, T.; Reh, C.; Bhangoo, A.; Kashmiri, H.; Montgomery, K.; Trinh, L.; Speer, H.; Lane, K.; Bergenstal, R.; Martens, T.; Madden, M.; Powers, M.; Criego, A.; Carlson, A.; Olson, B.; Beasley, S.; McCann, K.; Thomas, L.A.; Miller, C.; Ashanti, C.; Solorzano, C.B.; Puskaric, J.; Benjamin, R.; Adkins, D.; Spruill, A.; Williams, C.; Tsalikian, E.; Tansey, M.; Bansl, N.; Cabbage, J.; Coffey, J.; Schatz, D.; Clare-Salzler, M.; Cusi, K.; Fudge, B.; Haller, M.; Meehan, C.; Rohrs, H.; Silverstein, J.; Walker, A.; Albanese-O’Niell, A.; Foss, S.; Adams, J.; Cintron, M.; Thomas, N.; Gottschalk, M.; Newfield, R.; Hashiguchi, M.; Sparling, D.; Tryggested, J.; Beck, J.; Less, J.; Weber, L.; Adi, S.; Gitelman, S.; Sanda, S.; Wong, J.; McDonnell, M.; Mueller, M.; Izadi, Z.; Mistry, S.; Nelson, B.; Looper, L.; Frost, C.; Redondo, M.; Lyons, S.; Klinepeter, S.; Fegan-Bohm, K.; Bacha, F.; DeSalvo, D.; Butler, A.; Hilliard, M.; Khetani, F.; Yulatic, R.; Hudson, R.; Irvine, L.; Zubair, S.; Pace, C.; Pitrello, A.; Levy, W.; Njoku, C.; Zipf, W.; Dyer, J.; Lozano, R.; Seiple, D.; Corven, G.; Jaycox, M.; Wood, J.; Macleish, S.; Gubitosi-Klug, R.; Adams, R.; McGuigan, P.; Casey, T.; Campbell, W.; Kittelsrud, J.; Gupta, A.; Peterson, V.; Libman, I.; Diaz, A.; Jelley, D.; Crowder, C.; Greer, D.; Crawford, J.; Goudeau, S.; Pihoker, C.; Yi-Frazier, J.; Kearns, S.; Pascual, M.; Loots, B.; Beauregard, N.; Rickels, M.; O’Brien, S.; Agarwal, S.; Peleckis, A.; Dalton-Bakes, C.; Markmann, E.; Umpierrez, G.; Muir, A.; Ramos, C.; Behbahani, K.; Dhruv, N.; Gartzman, N.; Nathan, B.; Bellin, M.; Sunni, M.; Flaherty, N.; Leschyshyn, J.; Schmid, K.; Weingartner, D.; Ludwig, M.; Nelson, B.; Kogler, A.; Bartyzal, A.; Street, A.; Pappenfus, B.; Sweet, J.; Buse, J.; Young, L.; Bergamo, K.; Goley, A.; Kirkman, M.; Diner, J.; Kass, A.; Dezube, M.; Arnold, K.; Evans, T.; Sellers, S.; Blackman, S.; Abel, K-L.; Rasbach, L.; Ali, O.; Wolfgram, P.; Fiallo-Sharer, R.; Kramer, J.; Beesley, C.; Bingham-Tyson, C.; Unteutsh, R.; Harlan, D.; Lee, M.; Soyka, L.; Feldman, P.; Thompson, M.; Gallagher-Dorval, K.; Hubacz, L.; Hartigan, C.; Ciccarelli, C.; Edelen, R.; Edelen, M.; Borgwadt, T.; Stauffacher, K.; DeGrote, K.; Gruetzmacher, C.; Shepperd, M.; Bhargava, A.; Wright, D.; Fitzgerald, K.; Khoo, T.; Young, N.; Borg, L.; Stifel, K.; Rail, C.; Casas, L.; Eidenshink, E.; Huber, C.; Rieder, A.; Tuchscherer, A.; Broadbent, M.; Dolan, L.; Corathers, S.; Kichler, J.; Sheanon, N.; Baugh, H.; Standiford, D.; Weis, T.; Fox, C.; Schultz, C.; Ritter, A.; Vendrame, F.; Blashke, C.; Matheson, D.; Sanders-Branca, N.; Rudolph, J.; Biersdorf, D.; Fitch-Danielson, J.; Eckerle-Mize, D.; Brendle, F.; Fry, J.; Davis, D.; Lovell, C.; Hammel, B.; Williams, L.; Hoffman, R.; Chaudhari, M.; Kamboj, M.; Carr, L.; Casas, L.; Blehm, J.; Tello, A.; Walter, J.A.; Ward, R.; Broadbent, M.; Blomquist, G.; Stewart, M.; Cross, P.; Racki, S.; Sterchi, L.; Gouine, D.; Kiesow, B.; Welch, S.; Philis-Tsimikas, A.; Daily, G.; Chang, A.; McCallum, J.; Garcia, I.; Vela, T.; Loupasi, I.; Rosal, R.; Toschi, E.; Middelbeek, R.; Munshi, M.; Slyne, C.; Atakov-Castillo, A.; Fox, L.; Mauras, N.; Wasserman, R.; Damaso, L.; Englert, K.; Sikes, K.; Ponthieux, K.; Phillipson, L.; Cohen, A.; Gannon, G.; Deeb, L.; Shiver, A.; Schroeder, L.; Schworm, W.; Graham, K.; Levy, C.; Lam, D.; Burtman, E.; Levister, C.; Ogyaadu, S.; Gassner, H.; Duke, J.; Touger, L.; Newbern, D.; Hoekstra, F.; Harwood, K.; Prasad, V.; Daguanno, J.A.; Pratley, R.; Corbin, K.; Wright, M.; Nagel, S.; Water, N.; Ghere, M.; Whitaker, K.; Heptulla, R.; Katikaneni, R.; Johnson-Newell, D.; Crandall, J.; Powell, D.; Anghel, V.; Ghanny, S.; Aisenberg, J.; Chartoff, A.; Sivitz, J.; Mathus, S.; Cospito, T-L.; Thailkill, K.; Fowlkes, J.; Kalaitzoglou, E.; Morales Pozzo, A.; Edwards, K. Longitudinal changes in continuous glucose monitoring use among individuals with type 1 Diabetes: International comparison in the German and Austrian DPV and U.S. T1D exchange registries. Diabetes Care, 2020, 43(1), e1-e2.
[http://dx.doi.org/10.2337/dc19-1214] [PMID: 31672703]
[3]
Posselt, A.M.; Szot, G.L.; Frassetto, L.A.; Masharani, U.; Tavakol, M.; Amin, R.; McElroy, J.; Ramos, M.D.; Kerlan, R.K.; Fong, L.; Vincenti, F.; Bluestone, J.A.; Stock, P.G. Islet transplantation in type 1 diabetic patients using calcineurin inhibitor-free immunosuppressive protocols based on T-cell adhesion or costimulation blockade. Transplantation, 2010, 90(12), 1595-1601.
[http://dx.doi.org/10.1097/TP.0b013e3181fe1377] [PMID: 20978464]
[4]
Barton, F.B.; Rickels, M.R.; Alejandro, R.; Hering, B.J.; Wease, S.; Naziruddin, B.; Oberholzer, J.; Odorico, J.S.; Garfinkel, M.R.; Levy, M.; Pattou, F.; Berney, T.; Secchi, A.; Messinger, S.; Senior, P.A.; Maffi, P.; Posselt, A.; Stock, P.G.; Kaufman, D.B.; Luo, X.; Kandeel, F.; Cagliero, E.; Turgeon, N.A.; Witkowski, P.; Naji, A.; O’Connell, P.J.; Greenbaum, C.; Kudva, Y.C.; Brayman, K.L.; Aull, M.J.; Larsen, C.; Kay, T.W.H.; Fernandez, L.A.; Vantyghem, M.C.; Bellin, M.; Shapiro, A.M.J. Improvement in outcomes of clinical islet transplantation: 1999-2010. Diabetes Care, 2012, 35(7), 1436-1445.
[http://dx.doi.org/10.2337/dc12-0063] [PMID: 22723582]
[5]
Russ, H.A.; Parent, A.V.; Ringler, J.J.; Hennings, T.G.; Nair, G.G.; Shveygert, M.; Guo, T.; Puri, S.; Haataja, L.; Cirulli, V.; Blelloch, R.; Szot, G.L.; Arvan, P.; Hebrok, M. Controlled induction of human pancreatic progenitors produces functional beta-like cells in vitro. EMBO J., 2015, 34(13), 1759-1772.
[http://dx.doi.org/10.15252/embj.201591058] [PMID: 25908839]
[6]
Rezania, A.; Bruin, J.E.; Arora, P.; Rubin, A.; Batushansky, I.; Asadi, A.; O’Dwyer, S.; Quiskamp, N.; Mojibian, M.; Albrecht, T.; Yang, Y.H.C.; Johnson, J.D.; Kieffer, T.J. Reversal of diabetes with Insulin-producing cells derived in vitro from human pluripotent stem cells. Nat. Biotechnol., 2014, 32(11), 1121-1133.
[http://dx.doi.org/10.1038/nbt.3033] [PMID: 25211370]
[7]
Yabe, S.G.; Fukuda, S.; Takeda, F.; Nashiro, K.; Shimoda, M.; Okochi, H. Efficient generation of functional pancreatic β-cells from human induced pluripotent stem cells. J. Diabetes, 2017, 9(2), 168-179.
[http://dx.doi.org/10.1111/1753-0407.12400] [PMID: 27038181]
[8]
Yabe, S.G.; Fukuda, S.; Nishida, J.; Takeda, F.; Nashiro, K.; Okochi, H. Induction of functional islet-like cells from human iPS cells by suspension culture. Regen. Ther., 2019, 10, 69-76.
[http://dx.doi.org/10.1016/j.reth.2018.11.003] [PMID: 30623004]
[9]
Raikwar, S.P.; Kim, E.M.; Sivitz, W.I.; Allamargot, C.; Thedens, D.R.; Zavazava, N. Human iPS cell-derived Insulin producing cells form vascularized organoids under the kidney capsules of diabetic mice. PLoS One, 2015, 10(1), e0116582.
[http://dx.doi.org/10.1371/journal.pone.0116582] [PMID: 25629318]
[10]
Umekage, M.; Sato, Y.; Takasu, N. Overview: An iPS cell stock at CiRA. Inflamm. Regen., 2019, 39(1), 17.
[http://dx.doi.org/10.1186/s41232-019-0106-0] [PMID: 31497180]
[11]
Hanatani, T.; Takasu, N. CiRA iPSC seed stocks (CiRA’s iPSC Stock Project). Stem Cell Res., 2021, 50, 102033.
[http://dx.doi.org/10.1016/j.scr.2020.102033] [PMID: 33445065]
[12]
Yoshida, S.; Kato, T.M.; Sato, Y.; Umekage, M.; Ichisaka, T.; Tsukahara, M.; Takasu, N.; Yamanaka, S. A clinical-grade HLA haplobank of human induced pluripotent stem cells matching approximately 40% of the Japanese population. Med, 2023, 4(1), 51-66.e10.
[http://dx.doi.org/10.1016/j.medj.2022.10.003] [PMID: 36395757]
[13]
Kim, S.E.; Kim, B.K.; Gil, J.E.; Kim, S.K.; Kim, J.H. Comparative analysis of the developmental competence of three human embryonic stem cell lines in vitro. Mol. Cells, 2007, 23(1), 49-56.
[PMID: 17464211]
[14]
Osafune, K.; Caron, L.; Borowiak, M.; Martinez, R.J.; Fitz-Gerald, C.S.; Sato, Y.; Cowan, C.A.; Chien, K.R.; Melton, D.A. Marked differences in differentiation propensity among human embryonic stem cell lines. Nat. Biotechnol., 2008, 26(3), 313-315.
[http://dx.doi.org/10.1038/nbt1383] [PMID: 18278034]
[15]
Pringle, S.; De Bari, C.; Dell’Accio, F.; Przyborski, S.; Cooke, M.J.; Minger, S.L.; Grigoriadis, A.E. Mesenchymal differentiation propensity of a human embryonic stem cell line. Cell Prolif., 2011, 44(2), 120-127.
[http://dx.doi.org/10.1111/j.1365-2184.2011.00744.x] [PMID: 21401753]
[16]
Wu, H.; Xu, J.; Pang, Z.P.; Ge, W.; Kim, K.J.; Blanchi, B.; Chen, C.; Südhof, T.C.; Sun, Y.E. Integrative genomic and functional analyses reveal neuronal subtype differentiation bias in human embryonic stem cell lines. Proc. Natl. Acad. Sci. USA, 2007, 104(34), 13821-13826.
[http://dx.doi.org/10.1073/pnas.0706199104] [PMID: 17693548]
[17]
Martinez Arias, A.; Brickman, J.M. Gene expression heterogeneities in embryonic stem cell populations: Origin and function. Curr. Opin. Cell Biol., 2011, 23(6), 650-656.
[http://dx.doi.org/10.1016/j.ceb.2011.09.007] [PMID: 21982544]
[18]
Cahan, P.; Daley, G.Q. Origins and implications of pluripotent stem cell variability and heterogeneity. Nat. Rev. Mol. Cell Biol., 2013, 14(6), 357-368.
[http://dx.doi.org/10.1038/nrm3584] [PMID: 23673969]
[19]
Hayashi, Y.; Ohnuma, K.; Furue, M.K. Pluripotent stem cell heterogeneity. In: Stem cells heterogeneity - Novel concepts. Advances in experimental medicine and biology; Birbrair, A., Ed.; Springer: Cham, 2019; vol 1123, pp. 71-94.
[http://dx.doi.org/10.1007/978-3-030-11096-3_6]
[20]
Yang, S.; Cho, Y.; Jang, J. Single cell heterogeneity in human pluripotent stem cells. BMB Rep., 2021, 54(10), 505-515.
[http://dx.doi.org/10.5483/BMBRep.2021.54.10.094] [PMID: 34488931]
[21]
Ohno, Y.; Yuasa, S.; Egashira, T.; Seki, T.; Hashimoto, H.; Tohyama, S.; Saito, Y.; Kunitomi, A.; Shimoji, K.; Onizuka, T.; Kageyama, T.; Yae, K.; Tanaka, T.; Kaneda, R.; Hattori, F.; Murata, M.; Kimura, K.; Fukuda, K. Distinct iPS cells show different cardiac differentiation efficiency. Stem Cells Int., 2013, 2013, 1-11.
[http://dx.doi.org/10.1155/2013/659739] [PMID: 24367382]
[22]
Ninomiya, H.; Mizuno, K.; Terada, R.; Miura, T.; Ohnuma, K.; Takahashi, S.; Asashima, M.; Michiue, T. Improved efficiency of definitive endoderm induction from human induced pluripotent stem cells in feeder and serum-free culture system. In vitro Cell. Dev. Biol. Anim., 2015, 51(1), 1-8.
[http://dx.doi.org/10.1007/s11626-014-9801-y] [PMID: 25124871]
[23]
Horikawa, A.; Mizuno, K.; Tsuda, K.; Yamamoto, T.; Michiue, T. A simple method of hiPSCs differentiation into Insulin-producing cells is improved with vitamin C and RepSox. PLoS One, 2021, 16(7), e0254373.
[http://dx.doi.org/10.1371/journal.pone.0254373] [PMID: 34252142]
[24]
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(5), 861-872.
[http://dx.doi.org/10.1016/j.cell.2007.11.019] [PMID: 18035408]
[25]
Ohnuki, M.; Takahashi, K.; Yamanaka, S. Generation and characterization of human induced pluripotent stem cells. Curr. Protoc. Stem Cell Biol., 2009, 9(1), 2.
[http://dx.doi.org/10.1002/9780470151808.sc04a02s9] [PMID: 19536759]
[26]
Zhu, Y.; Liu, Q.; Zhou, Z.; Ikeda, Y. PDX1, Neurogenin-3, and MAFA: Critical transcription regulators for beta cell development and regeneration. Stem Cell Res. Ther., 2017, 8(1), 240.
[http://dx.doi.org/10.1186/s13287-017-0694-z] [PMID: 29096722]
[27]
Yang, Y.; Wang, H.; He, J.; Shi, W.; Jiang, Z.; Gao, L.; Jiang, Y.; Ni, R.; Yang, Q.; Luo, L. A single-cell–resolution fate map of endoderm reveals demarcation of pancreatic progenitors by cell cycle. Proc. Natl. Acad. Sci. USA, 2021, 118(25), e2025793118.
[http://dx.doi.org/10.1073/pnas.2025793118] [PMID: 34161274]
[28]
Krentz, N.A.J.; van Hoof, D.; Li, Z.; Watanabe, A.; Tang, M.; Nian, C.; German, M.S.; Lynn, F.C. Phosphorylation of NEUROG3 links endocrine differentiation to the cell cycle in pancreatic progenitors. Dev. Cell, 2017, 41(2), 129-142.e6.
[http://dx.doi.org/10.1016/j.devcel.2017.02.006] [PMID: 28441528]
[29]
Ning, H.; Horikawa, A.; Yamamoto, T.; Michiue, T. Chemical inhibitors of cyclin-dependent kinase (CDKi) improve pancreatic endocrine differentiation of iPS cells. In vitro Cell Dev Biol Anim 2023, 59, 410-419.
[http://dx.doi.org/10.1007/s11626-023-00776-0]
[30]
Aigha, I.I.; Abdelalim, E.M. NKX6.1 transcription factor: A crucial regulator of pancreatic β cell development, identity, and proliferation. Stem Cell Res. Ther., 2020, 11(1), 459.
[http://dx.doi.org/10.1186/s13287-020-01977-0] [PMID: 33121533]
[31]
Memon, B.; Younis, I.; Abubaker, F.; Abdelalim, E.M. PDX1 /NKX6.1 + progenitors derived from human pluripotent stem cells as a novel source of Insulin-secreting cells. Diabetes Metab. Res. Rev., 2021, 37(5), e3400.
[http://dx.doi.org/10.1002/dmrr.3400] [PMID: 32857429]
[32]
Paget, M.B.; Murray, H.E.; Bailey, C.J.; Flatt, P.R.; Downing, R. Rotational co-culture of clonal β-cells with endothelial cells: Effect of PPAR-γ agonism in vitro on Insulin and VEGF secretion. Diabetes Obes. Metab., 2011, 13(7), 662-668.
[http://dx.doi.org/10.1111/j.1463-1326.2011.01392.x] [PMID: 21435140]
[33]
Sabra, G.; Vermette, P. A 3D cell culture system: Separation distance between INS-1 cell and endothelial cell monolayers co-cultured in fibrin influences INS-1 cells Insulin secretion. Biotechnol. Bioeng., 2013, 110(2), 619-627.
[http://dx.doi.org/10.1002/bit.24716] [PMID: 22949028]
[34]
Kroon, E.; Martinson, L.A.; Kadoya, K.; Bang, A.G.; Kelly, O.G.; Eliazer, S.; Young, H.; Richardson, M.; Smart, N.G.; Cunningham, J.; Agulnick, A.D.; D’Amour, K.A.; Carpenter, M.K.; Baetge, E.E. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive Insulin-secreting cells in vivo. Nat. Biotechnol., 2008, 26(4), 443-452.
[http://dx.doi.org/10.1038/nbt1393] [PMID: 18288110]
[35]
Ramzy, A.; Thompson, D.M.; Ward-Hartstonge, K.A.; Ivison, S.; Cook, L.; Garcia, R.V.; Loyal, J.; Kim, P.T.W.; Warnock, G.L.; Levings, M.K.; Kieffer, T.J. Implanted pluripotent stem-cell-derived pancreatic endoderm cells secrete glucose-responsive C-peptide in patients with type 1 diabetes. Cell Stem Cell, 2021, 28(12), 2047-2061.e5.
[http://dx.doi.org/10.1016/j.stem.2021.10.003] [PMID: 34861146]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy