Generation of insulin-producing pancreatic β cells from multiple human stem cell lines

Nathaniel J. Hogrebe, Kristina G. Maxwell, Punn Augsornworawat, Jeffrey R. Millman

Published: 2021-08-03 DOI: 10.1038/s41596-021-00560-y

pluripotent stem cells

Pancreatic β cells

Stem cell differentiation

Insulin secretion

Planar culture

AI 解读

Supplementary information

Supplementary Information

Supplementary Figs. 1–7.

Reporting Summary

Author Correction: Full-length sequencing of circular DNA viruses and extrachromosomal circular DNA using CIDER-Seq

Generation of heart-forming organoids from human pluripotent stem cells

Design and fabrication of wearable electronic textiles using twisted fiber-based threads

Activation of mechanoluminescent nanotransducers by focused ultrasound enables light delivery to deep-seated tissue in vivo

Chromatin accessibility profiling by ATAC-seq

Deoxyfluorination of phenols for chemoselective18F-labeling of peptides

Author Correction: cfSNV: a software tool for the sensitive detection of somatic mutations from cell-free DNA

Human primordial germ cell-like cells specified from resetting precursors develop in human hindgut organoids

An inexpensive semi-automated sample processing pipeline for cell-free RNA extraction

Application of CHyMErA Cas9-Cas12a combinatorial genome-editing platform for genetic interaction mapping and gene fragment deletion screening

查看全部

Sections

Figures

References

Supplementary information

Brennan, D. C., Kopetskie, H. A. & Sayre, P. H. Long-term follow-up of the Edmonton protocol of islet transplantation in the United States. Am. J. Transpl. 16, 509–517 (2016).
Shapiro, J. et al. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N. Engl. J. Med. 343, 230–238 (2000).
D’Amour, K. A. et al. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat. Biotechnol. 23, 1534–1541 (2005).
D’Amour, K. A. et al. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat. Biotechnol. 24, 1392–1401 (2006).
Rezania, A. et al. Reversal of diabetes with insulin-producing cells derived in vitro from human pluripotent stem cells. Nat. Biotechnol. 32, 1121–1133 (2014).
Nostro, M. C. et al. Stage-specific signaling through TGFβ family members and WNT regulates patterning and pancreatic specification of human pluripotent stem cells. Development 138, 861–871 (2011).
Kunisada, Y., Tsubooka-Yamazoe, N., Shoji, M. & Hosoya, M. Small molecules induce efficient differentiation into insulin-producing cells from human induced pluripotent stem cells. Stem Cell Res. 8, 274–284 (2012).
Borowiak, M. et al. Small molecules efficiently direct endodermal differentiation of mouse and human embryonic stem cells. Cell Stem Cell 4, 348–358 (2009).
Sneddon, J. B., Borowiak, M. & Melton, D. A. Self-renewal of embryonic-stem-cell-derived progenitors by organ-matched mesenchyme. Nature 491, 765–768 (2012).
Mahaddalkar, P. U. et al. Generation of pancreatic β cells from CD177+ anterior definitive endoderm. Nat. Biotechnol. 38, 1061–1072 (2020).
Xu, X., Browning, V. L. & Odorico, J. S. Activin, BMP and FGF pathways cooperate to promote endoderm and pancreatic lineage cell differentiation from human embryonic stem cells. Mech. Dev. 128, 412–427 (2011).
Nostro, M. C. & Keller, G. Generation of beta cells from human pluripotent stem cells: Potential for regenerative medicine. Semin. Cell Dev. Biol. 23, 701–710 (2012).
Kroon, E. et al. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat. Biotechnol. 26, 443–452 (2008).
Rezania, A. et al. Maturation of human embryonic stem cell-derived pancreatic progenitors into functional islets capable of treating pre-existing diabetes in mice. Diabetes 61, 2016–2029 (2012).
Bruin, J. E. et al. Maturation and function of human embryonic stem cell-derived pancreatic progenitors in macroencapsulation devices following transplant into mice. Diabetologia 56, 1987–1998 (2013).
Bruin, J. E. et al. Accelerated maturation of human stem cell-derived pancreatic progenitor cells into insulin-secreting cells in immunodeficient rats relative to mice. Stem Cell Rep. 5, 1081–1096 (2015).
Rezania, A. et al. Enrichment of human embryonic stem cell-derived NKX6.1-expressing pancreatic progenitor cells accelerates the maturation of insulin-secreting cells in vivo. Stem Cells 31, 2432–2442 (2013).
Kelly, O. G. et al. Cell-surface markers for the isolation of pancreatic cell types derived from human embryonic stem cells. Nat. Biotechnol. 29, 750–756 (2011).
Schaffer, A. E., Freude, K. K., Nelson, S. B. & Sander, M. Nkx6 transcription factors and Ptf1a function as antagonistic lineage determinants in multipotent pancreatic progenitors. Dev. Cell 18, 1022–1029 (2010).
Nelson, S. B., Schaffer, A. E. & Sander, M. The transcription factors Nkx6.1 and Nkx6.2 possess equivalent activities in promoting beta-cell fate specification in Pdx1+ pancreatic progenitor cells. Development 134, 2491–2500 (2007).
Nostro, M. C. et al. Efficient generation of NKX6-1+ pancreatic progenitors from multiple human pluripotent stem cell lines. Stem Cell Rep. 4, 591–604 (2015).
Veres, A. et al. Charting cellular identity during human in vitro β -cell differentiation. Nature 569, 368–373 (2019).
Sharon, N. et al. Wnt signaling separates the progenitor and endocrine compartments during pancreas development. Cell Rep. 27, 2281–2291 (2019).
Johansson, K. A. et al. Temporal control of neurogenin3 activity in pancreas progenitors reveals competence windows for the generation of different endocrine cell types. Dev. Cell 12, 457–465 (2007).
Pagliuca, F. W. et al. Generation of functional human pancreatic β cells in vitro. Cell 159, 428–439 (2014).
Russ, H. A. et al. Controlled induction of human pancreatic progenitors produces functional beta-like cells in vitro. EMBO J. 34, 1759–1772 (2015).
Nair, G. G. et al. Recapitulating endocrine cell clustering in culture promotes maturation of human stem-cell-derived β cells. Nat. Cell Biol. 21, 263–274 (2019).
Sui, L. et al. β-Cell replacement in mice using human type 1 diabetes nuclear transfer embryonic stem cells. Diabetes 67, 26–35 (2018).
Alvarez-Dominguez, J. R. et al. Circadian entrainment triggers maturation of human in vitro islets. Cell Stem Cell 26, 108–122.e10 (2020).
Zhou, X. et al. LIN28B Impairs the transition of hESC-derived β cells from the juvenile to adult state. Stem Cell Rep. 14, 9–20 (2020).
Cogger, K. F. et al. Glycoprotein 2 is a specific cell surface marker of human pancreatic progenitors. Nat. Commun. 8, 331 (2017).
Johannesson, B., Sui, L., Freytes, D. O., Creusot, R. J. & Egli, D. Toward beta cell replacement for diabetes. EMBO J. 34, 841–855 (2015).
Sneddon, J. B. et al. Stem cell therapies for treating diabetes: progress and remaining challenges. Cell Stem Cell 22, 810–823 (2018).
Millman, J. R. & Pagliuca, F. W. Autologous pluripotent stem cell-derived β-like cells for diabetes cellular therapy. Diabetes 66, 1111–1120 (2017).
Nair, G. G., Tzanakakis, E. S. & Hebrok, M. Emerging routes to the generation of functional β-cells for diabetes mellitus cell therapy. Nat. Rev. Endocrinol. 16, 506–518 (2020).
Latres, E., Finan, D. A., Greenstein, J. L., Kowalski, A. & Kieffer, T. J. Navigating two roads to glucose normalization in diabetes: automated insulin delivery devices and cell therapy. Cell Metab. 29, 545–563 (2019).
Johnson, J. D. The quest to make fully functional human pancreatic beta cells from embryonic stem cells: climbing a mountain in the clouds. Diabetologia 59, 2047–2057 (2016).
Tremmel, D. M., Mitchell, S. A., Sackett, S. D. & Odorico, J. S. Mimicking nature-made beta cells: recent advances towards stem cell-derived islets. Curr. Opin. Organ Transplant. 24, 574–581 (2019).
Velazco-Cruz, L., Goedegebuure, M. M. & Millman, J. R. Advances toward engineering functionally mature human pluripotent stem cell-derived β cells. Front. Bioeng. Biotechnol. 8, 786 (2020).
Velazco-Cruz, L. et al. Acquisition of dynamic function in human stem cell-derived β cells. Stem Cell Rep. 12, 351–365 (2019).
Hogrebe, N. J., Augsornworawat, P., Maxwell, K. G., Velazco-Cruz, L. & Millman, J. R. Targeting the cytoskeleton to direct pancreatic differentiation of human pluripotent stem cells. Nat. Biotechnol. 38, 460–470 (2020).
Maxwell, K. G. et al. Gene-edited human stem cell–derived β cells from a patient with monogenic diabetes reverse preexisting diabetes in mice. Sci. Transl. Med. 12, eaax9106 (2020).
Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677–689 (2006).
Kilian, K. A., Bugarija, B., Lahn, B. T. & Mrksich, M. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc. Natl Acad. Sci. 107, 4872–4877 (2010).
McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K. & Chen, C. S. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6, 483–495 (2004).
Mamidi, A. et al. Mechanosignalling via integrins directs fate decisions of pancreatic progenitors. Nature 564, 114–118 (2018).
Rosado-Olivieri, E. A., Anderson, K., Kenty, J. H. & Melton, D. A. YAP inhibition enhances the differentiation of functional stem cell-derived insulin-producing β cells. Nat. Commun. 10, 1464 (2019).
Cebola, I. et al. TEAD and YAP regulate the enhancer network of human embryonic pancreatic progenitors. Nat. Cell Biol. 17, 615–626 (2015).
Dupont, S. et al. Role of YAP/TAZ in mechanotransduction. Nature 474, 179–183 (2011).
Slaoui, M. & Fiette, L. Histopathology procedures: from tissue sampling to histopathological evaluation. Methods Mol. Biol. 691, 69–82 (2011).
Augsornworawat, P., Maxwell, K. G., Velazco-Cruz, L. & Millman, J. R. Single-cell transcriptome profiling reveals β cell maturation in stem cell-derived islets after transplantation. Cell Rep. 32, 108067 (2020).

Generation of insulin-producing pancreatic β cells from multiple human stem cell lines

Supplementary information

推荐阅读