Generation of functional insulin-producing cells from mouse embryonic stem cells through 804G cell-derived extracellular matrix and protein transduction of transcription factors

Stem Cells Translational Medicine

Volumn 3, Issue 1, 2014, Pages 114-127

  Kaitsuka, Taku ^a   Noguchi, Hirofumi ^b   Shiraki, Nobuaki ^a   Kubo, Takuya ^a   Wei, Fan Yan ^a   Hakim, Farzana ^a   Kume, Shoen ^a   Tomizawa, Kazuhito ^a,c  

^a KUMAMOTO UNIVERSITY   (Japan)

^b SAKURA NATIONAL HOSPITAL   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Diabetes; Embryonic stem cells; Induced pluripotent stem cells; Pancreatic differentiation; Transcription factors

Indexed keywords

C PEPTIDE; INSULIN; NEUROGENIC DIFFERENTIATION FACTOR; RECOMBINANT PROTEIN; TRANSCRIPTION FACTOR MAFA; TRANSCRIPTION FACTOR PDX 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DIABETES MELLITUS; EMBRYONIC STEM CELL; ENDOCRINE CELL; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL; PLURIPOTENT STEM CELL; PROTEIN DOMAIN; PROTEIN SECRETION; PROTEIN SYNTHESIS REGULATION; PROTEIN TRANSDUCTION DOMAIN; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL TRANSPLANTATION; WESTERN BLOTTING;

DIABETES; EMBRYONIC STEM CELLS; INDUCED PLURIPOTENT STEM CELLS; PANCREATIC DIFFERENTIATION; TRANSCRIPTION FACTORS;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINE; DIABETES MELLITUS, EXPERIMENTAL; EMBRYONIC STEM CELLS; EXTRACELLULAR MATRIX; GREEN FLUORESCENT PROTEINS; HOMEODOMAIN PROTEINS; INSULIN; INSULIN-SECRETING CELLS; MAF TRANSCRIPTION FACTORS, LARGE; MICE; NERVE TISSUE PROTEINS; PROTEIN TRANSPORT; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSDUCTION, GENETIC;

EID: 84892689842     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2013-0075     Document Type: Article

References (72)

1. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663-676.
2. Kroon E, Martinson LA, Kadoya K et al. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol 2008;26:443-452.
3. Maehr R, Chen S, Snitow M et al. Generation of pluripotent stem cells from patients with type 1 diabetes. Proc Natl Acad Sci USA 2009; 106:15768-15773.
4. Zhang D, Jiang W, Liu M et al. Highly efficient differentiation of human ES cells and iPS cells into mature pancreatic insulin-producing cells. Cell Res 2009;19:429-438.
5. Zhou Q, Brown J, Kanarek A et al. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 2008;455:627-632.
6. Joliot A, Prochiantz A. Transduction peptides: From technology to physiology. Nat Cell Biol 2004;6:189-196.
7. Gump JM, Dowdy SF. TAT transduction: The molecular mechanism and therapeutic prospects. Trends Mol Med 2007;13:443-448.
8. Vivès E, Schmidt J, Pèlegrin A. Cellpenetrating and cell-targeting peptides in drug delivery. Biochim Biophys Acta 2008;1786:126-138.
9. Frankel AD, Pabo CO. Cellular uptake of the tat protein from human immunodeficiency virus. Cell 1988;55:1189-1193.
10. Green M, Loewenstein PM. Autonomous functional domains of chemically synthesized human immunodeficiency virus tat transactivator protein. Cell 1988;55:1179-1188.
11. Joliot A, Pernelle C, Deagostini-Bazin H et al. Antennapedia homeobox peptide regulates neural morphogenesis. Proc Natl Acad Sci USA 1991;88:1864-1868.
12. van den Berg A, Dowdy SF. Protein transduction domain delivery of therapeuticmacromolecules. Curr Opin Biotechnol 2011;22:888-893.
13. Kim D, Kim CH, Moon JI et al. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 2009;4:472-476.
14. Zhou H, Wu S, Joo JY et al. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 2009;4:381-384.
15. Lima MJ, Docherty HM, Chen Y et al. Pancreatic transcription factors containing protein transduction domains drive mouse embryonic stem cells towards endocrine pancreas. PLoS One 2012;7:e36481.
16. Vargas N, ' Alvarez-Cubela S, Giraldo JA etal. TAT-mediatedtransductionofMafAprotein inuteroresults inenhancedpancreatic insulinexpression and changes in islet morphology. PLoS One 2011;6:e22364.
17. Wilson ME, Scheel D, German MS. Gene expression cascades in pancreatic development. Mech Dev 2003;120:65-80.
18. Habener JF, Kemp DM, Thomas MK. Minireview: Transcriptional regulation in pancreatic development. Endocrinology 2005;146: 1025-1034.
19. Zhou Q, Law AC, Rajagopal J et al. A multipotent progenitor domain guides pancreatic organogenesis. Dev Cell 2007;13: 103-114.
20. Xu H, Tsang KS, Chan JC et al. The combined expression of Pdx1 and MafA with either Ngn3 or NeuroD improves the differentiation efficiency of mouse embryonic stem cells into insulinproducing cells. Cell Transplant 2013;22:147-158.
21. Huang HP, Liu M, El-HodiriHMet al. Regulation of the pancreatic islet-specific gene BETA2 (neuroD) by neurogenin 3. Mol Cell Biol 2000;20:3292-3307.
22. Noguchi H, Kaneto H, Weir GC et al. PDX-1 protein containing its own antennapedia-like protein transduction domain can transduce pancreatic duct and islet cells. Diabetes 2003; 52:1732-1737.
23. Noguchi H, Bonner-Weir S, Wei FY et al. BETA2/NeuroD protein can be transduced into cells due to an arginine-and lysine-rich sequence. Diabetes 2005;54:2859-2866.
24. Matsushita M, Tomizawa K, Moriwaki A et al. A high-efficiency protein transduction system demonstrating the role of PKA in longlasting long-term potentiation. J Neurosci 2001; 21:6000-6007.
25. Matsui H, Tomizawa K, Lu YF et al. Protein therapy: In vivo protein transduction by polyarginine (11R)PTD and subcellular targeting delivery. Curr Protein Pept Sci 2003;4:151-157.
26. Gu G, Wells JM, Dombkowski D et al. Global expression analysis of gene regulatory pathways during endocrine pancreatic development. Development 2004;131:165-179.
27. Shiraki N, Yoshida T, Araki K et al. Guided differentiation of embryonic stem cells into Pdx1-expressing regional-specific definitive endoderm. STEM CELLS 2008;26:874-885.
28. HaraM, WangX, KawamuraT et al. Transgenic mice with green fluorescent protein-labeled pancreatic beta-cells. Am J Physiol Endocrinol Metab 2003;284:E177-E183.
29. Higuchi Y, Shiraki N, Yamane K et al. Synthesized basement membranes direct the differentiation of mouse embryonic stem cells into pancreatic lineages. J Cell Sci 2010;123: 2733-2742.
30. Okita K, Ichisaka T, Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature 2007;448:313-317.
31. Bosco D, Meda P, Halban PA et al. Importance of cell-matrix interactions in rat islet betacell secretion in vitro: Role of alpha6beta1 integrin. Diabetes 2000;49:233-243.
32. Takahashi K, Tanabe K, OhnukiMet al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131:861-872.
33. Fusaki N, Ban H, Nishiyama A et al. Efficient induction of transgene-free humanpluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proc Jpn Acad, Ser B, Phys Biol Sci 2009;85:348-362.
34. D'Amour KA, Bang AG, Eliazer S et al. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol 2006;24:1392-1401.
35. Hitsuda T, Michiue H, Kitamatsu M et al. A protein transduction method using oligoarginine (3R) for the delivery of transcription factors into cell nuclei. Biomaterials 2012;33: 4665-4672.
36. Carlotti F, Zaldumbide A, Charif H et al. The 45-kDa form of Pdx-1 does not result from post-translational modifications. Biochem Biophys Res Commun 2008;370:225-229.
37. Oliver-Krasinski JM, Stoffers DA. On the origin of the beta cell. Genes Dev 2008;22: 1998-2021.
38. Murtaugh LC. Pancreas and beta-cell development: From the actual to the possible. Development 2007;134:427-438.
39. Hammar E, Parnaud G, Bosco D et al. Extracellular matrix protects pancreatic beta-cells against apoptosis:Roleof short-andlong-term signaling pathways. Diabetes 2004;53:2034-2041.
40. Parnaud G, Bosco D, Berney T et al. Proliferation of sorted human and rat beta cells. Diabetologia 2008;51:91-100.
41. Bosco D, Gonelle-Gispert C, Wollheim CB et al. Increased intracellular calcium is required for spreading of rat islet beta-cells on extracellular matrix. Diabetes 2001;50:1039-1046.
42. Stoffers DA, Thomas MK, Habener JF. Homeodomain protein IDX-1: A master regulator of pancreas development and insulin gene expression. Trends Endocrinol Metab 1997;8: 145-151.
43. Habener JF, Stoffers DA. A newly discovered role of transcription factors involved in pancreas development and the pathogenesis of diabetes mellitus. Proc Assoc Am Physicians 1998;110:12-21.
44. Guz Y, Montminy MR, Stein R et al. Expression of murine STF-1, a putative insulin gene transcription factor, in beta cells of pancreas, duodenal epithelium and pancreatic exocrine and endocrine progenitors during ontogeny. Development 1995;121:11-18.
45. Naya FJ, Stellrecht CM, Tsai MJ. Tissuespecific regulation of the insulin gene by a novel basic helix-loop-helix transcription factor. Genes Dev 1995;9:1009-1019.
46. Schwitzgebel VM, ScheelDW, Conners JR et al. Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development 2000;127:3533-3542.
47. Hang Y, Stein R. MafA and MafB activity in pancreatic b cells. Trends Endocrinol Metab 2011;22:364-373.
48. Matsuoka TA, Zhao L, Artner I et al. Members of the large Maf transcription family regulate insulin gene transcription in islet beta cells. Mol Cell Biol 2003;23:6049-6062.
49. Olbrot M, Rud J, Moss LG et al. Identification of beta-cell-specific insulin gene transcription factor RIPE3b1 as mammalian MafA. Proc Natl Acad Sci USA 2002;99:6737-6742.
50. Kataoka K, Han SI, Shioda S et al. MafA is a glucose-regulated and pancreatic beta-cellspecific transcriptional activator for the insulin gene. J Biol Chem 2002;277:49903-49910.
51. Murtaugh LC, Melton DA. Genes, signals, and lineages in pancreas development. Annu Rev Cell Dev Biol 2003;19:71-89.
52. Jensen J. Gene regulatory factors in pancreatic development. Dev Dyn 2004;229: 176-200.
53. Wessells NK, Cohen JH. Early pancreas organogenesis: Morphogenesis, tissue interactions, and mass effects. Dev Biol 1967;15:237-270.
54. Wessells NK, Evans J. Ultrastructural studies of early morphogenesis and cytodifferentiation in the embryonic mammalian pancreas. Dev Biol 1968;17:413-446.
55. Ahlgren U, Jonsson J, Edlund H. The morphogenesis of the pancreatic mesenchyme is uncoupled from that of the pancreatic epithelium in IPF1/PDX1-deficient mice. Development 1996;122:1409-1416.
56. Offield MF, Jetton TL, Labosky PA et al. PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 1996;122:983-995.
57. Mutoh H, Fung BP, Naya FJ et al. The basic helix-loop-helix transcription factorBETA2/NeuroD is expressed in mammalian enteroendocrine cells and activates secretin gene expression. Proc Natl Acad Sci USA 1997;94:3560-3564.
58. Matsuoka TA, Artner I, Henderson E et al. The MafA transcription factor appears to be responsible for tissue-specific expressionof insulin. Proc Natl Acad Sci USA 2004;101:2930-2933.
59. Christodoulou C, Longmire TA, Shen SS et al. Mouse ES and iPS cells can form similar definitiveendodermdespitedifferences inimprinted genes. J Clin Invest 2011;121:2313-2325.
60. Mei Y, Hollister-Lock J, Bogatyrev SR et al. A high throughput micro-array system of polymer surfaces for the manipulation of primary pancreatic islet cells. Biomaterials 2010;31: 8989-8995.
61. Lefebvre VH, Otonkoski T, Ustinov J et al. Culture of adult human islet preparations with hepatocyte growth factor and 804G matrix is mitogenic for duct cells but not for beta-cells. Diabetes 1998;47:134-137.
62. Hayek A, Beattie GM, Cirulli V et al. Growth factor/matrix-induced proliferation of human adult beta-cells. Diabetes 1995; 44:1458-1460.
63. Riddelle KS, Green KJ, Jones JC. Formation of hemidesmosomes in vitro by a transformed rat bladder cell line. J Cell Biol 1991; 112:159-168.
64. Langhofer M, Hopkinson SB, Jones JC. The matrix secreted by 804G cells contains laminin-related components that participate in hemidesmosome assembly in vitro. J Cell Sci 1993;105:753-764.
65. Hormia M, Falk-Marzillier J, Plopper G et al. Rapid spreading and mature hemidesmosome formation in HaCaT keratinocytes induced by incubation with soluble laminin-5r. J Invest Dermatol 1995;105:557-561.
66. Baker SE, Hopkinson SB, Fitchmun M et al. Laminin-5 and hemidesmosomes: Role of the alpha 3 chain subunit in hemidesmosome stability and assembly. J Cell Sci 1996; 109:2509-2520.
67. Colognato H, Yurchenco PD. Form and function: The laminin family of heterotrimers. Dev Dyn 2000;218:213-234.
68. Aumailley M, El Khal A, Knöss N et al. Laminin 5 processing and its integration into the ECM. Matrix Biol 2003;22:49-54.
69. Teitelman G, Alpert S, Polak JM et al. Precursor cells of mouse endocrine pancreas coexpress insulin, glucagon and the neuronal proteins tyrosine hydroxylase and neuropeptide Y, but not pancreatic polypeptide. Development 1993;118:1031-1039.
70. Kunisada Y, Tsubooka-Yamazoe N, Shoji Met al. Small molecules induce efficient differentiation into insulin-producing cells from human induced pluripotent stem cells. Stem Cell Res (Amst) 2012;8:274-284.
71. Merino JF, Nacher V, Raurell M et al. Optimal insulin treatment in syngeneic islet transplantation. Cell Transplant 2000;9: 11-18.
72. Cheng X, Ying L, Lu L et al. Self-renewing endodermal progenitor lines generated from human pluripotent stem cells. Cell Stem Cell 2012;10:371-384.