PDX1- and NGN3-mediated in vitro reprogramming of human bone marrow-derived mesenchymal stromal cells into pancreatic endocrine lineages

References

• Halban PA. Cellular sources of new pancreatic beta cells and therapeutic implications for regenerative medicine. Nat Cell Biol. 2004;6:1021–5.
   PubMed Web of Science ®Google Scholar
• Ryan EA, Paty BW, Senior PA, Bigam D, Alfadhli E, Kneteman NM, . Five-year follow-up after clinical islet transplantation. Diabetes. 2005;54:2060–9.
   PubMed Web of Science ®Google Scholar
• Bonner-Weir S, Taneja M, Weir GC, Tatarkiewicz K, Song KH, Sharma A, . In vitro cultivation of human islets from expanded ductal tissue. Proc Natl Acad Sci USA. 2000;97:7999–8004.
   PubMed Web of Science ®Google Scholar
• Zulewski H, Abraham EJ, Gerlach MJ, Daniel PB, Moritz W, Muller B, . Multipotential nestin-positive stem cells isolated from adult pancreatic islets differentiate ex vivo into pancreatic endocrine, exocrine, and hepatic phenotypes. Diabetes. 2001;50:521–33.
   PubMed Web of Science ®Google Scholar
• Gallo R, Gambelli F, Gava B, Sasdelli F, Tellone V, Masini M, . Generation and expansion of multipotent mesenchymal progenitor cells from cultured human pancreatic islets. Cell Death Differ. 2007;14:1860–71.
   PubMed Web of Science ®Google Scholar
• Davani B, Ikonomou L, Raaka BM, Geras-Raaka E, Morton RA, Marcus-Samuels B, . Human islet-derived precursor cells are mesenchymal stromal cells that differentiate and mature to hormone-expressing cells in vivo. Stem Cells. 2007;25:3215–22.
   PubMed Web of Science ®Google Scholar
• Chase LG, Ulloa-Montoya F, Kidder BL, Verfaillie CM. Islet-derived fibroblast-like cells are not derived via epithelial-mesenchymal transition from Pdx-1 or insulin-positive cells. Diabetes. 2007;56:3–7.
   PubMed Web of Science ®Google Scholar
• Gershengorn MC, Hardikar AA, Wei C, Geras-Raaka E, Marcus-Samuels B, Raaka BM. Epithelial-to-mesenchymal transition generates proliferative human islet precursor cells. Science. 2004;306:2261–4.
   PubMed Web of Science ®Google Scholar
• Tang DQ, Cao LZ, Burkhardt BR, Xia CQ, Litherland SA, Atkinson MA, . In vivo and in vitro characterization of insulin-producing cells obtained from murine bone marrow. Diabetes. 2004;53:1721–32.
   PubMed Web of Science ®Google Scholar
• Owen M, Friedenstein AJ. Stromal stem cells: marrow-derived osteogenic precursors. Ciba Found Symp. 1988;136: 42–60.
   PubMedGoogle Scholar
• Gregory CA, Prockop DJ, Spees JL. Non-hematopoietic bone marrow stem cells: molecular control of expansion and differentiation. Exp Cell Res. 2005;306:330–5.
   PubMed Web of Science ®Google Scholar
• Chao KC, Chao KF, Fu YS, Liu SH. Islet-like clusters derived from mesenchymal stem cells in Wharton's jelly of the human umbilical cord for transplantation to control type 1 diabetes. PLoS One. 2008;3:e1451.
   PubMed Web of Science ®Google Scholar
• Dezawa M, Kanno H, Hoshino M, Cho H, Matsumoto N, Itokazu Y, . Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation. J Clin Invest. 2004;113:1701–10.
   PubMed Web of Science ®Google Scholar
• Luk JM, Wang PP, Lee CK, Wang JH, Fan ST. Hepatic potential of bone marrow stromal cells: development of in vitro co-culture and intra-portal transplantation models. J Immunol Methods. 2005;305:39–47.
   PubMed Web of Science ®Google Scholar
• Sacchetti B, Funari A, Michienzi S, Di Cesare S, Piersanti S, Saggio I, . Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell. 2007;131:324–36.
   PubMed Web of Science ®Google Scholar
• Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997;276:71–4.
   PubMed Web of Science ®Google Scholar
• Zalzman M, Gupta S, Giri RK, Berkovich I, Sappal BS, Karnieli O, . Reversal of hyperglycemia in mice by using human expandable insulin-producing cells differentiated from fetal liver progenitor cells. Proc Natl Acad Sci USA. 2003;100:7253–8.
   PubMed Web of Science ®Google Scholar
• Sapir T, Shternhall K, Meivar-Levy I, Blumenfeld T, Cohen H, Skutelsky E, . Cell-replacement therapy for diabetes: generating functional insulin-producing tissue from adult human liver cells. Proc Natl Acad Sci USA. 2005;102: 7964–9.
   PubMed Web of Science ®Google Scholar
• Karnieli O, Izhar-Prato Y, Bulvik S, Efrat S. Generation of insulin-producing cells from human bone marrow mesenchymal stem cells by genetic manipulation. Stem Cells. 2007; 25(11):2837–44.
   PubMed Web of Science ®Google Scholar
• Selander L, Edlund H. Nestin is expressed in mesenchymal and not epithelial cells of the developing mouse pancreas. Mech Dev. 2002;113:189–92.
   PubMed Web of Science ®Google Scholar
• Offield MF, Jetton TL, Labosky PA, Ray M, Stein RW, Magnuson MA, . PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development. 1996;122:983–95.
   PubMed Web of Science ®Google Scholar
• Gannon M, Ables ET, Crawford L, Lowe D, Offield MF, Magnuson MA, . pdx-1 function is specifically required in embryonic beta cells to generate appropriate numbers of endocrine cell types and maintain glucose homeostasis. Dev Biol. 2008;314:406–17.
   PubMed Web of Science ®Google Scholar
• Apelqvist A, Li H, Sommer L, Beatus P, Anderson DJ, Honjo T, . Notch signalling controls pancreatic cell differentiation. Nature. 1999;400:877–81.
   PubMed Web of Science ®Google Scholar
• Schwitzgebel VM, Scheel DW, Conners JR, Kalamaras J, Lee JE, Anderson DJ, . Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development. 2000;127:3533–42.
   PubMed Web of Science ®Google Scholar
• Lavon N, Yanuka O, Benvenisty N. The effect of overexpression of Pdx1 and Foxa2 on the differentiation of human embryonic stem cells into pancreatic cells. Stem Cells. 2006; 24:1923–30.
   PubMed Web of Science ®Google Scholar
• Kaneto H, Matsuoka TA, Nakatani Y, Miyatsuka T, Matsuhisa M, Hori M, . A crucial role of MafA as a novel therapeutic target for diabetes. J Biol Chem. 2005;280:15047–52.
   PubMed Web of Science ®Google Scholar
• Abdallah BM, Haack-Sorensen M, Burns JS, Elsnab B, Jakob F, Hokland P, . Maintenance of differentiation potential of human bone marrow mesenchymal stem cells immortalized by human telomerase reverse transcriptase gene despite extensive proliferation. Biochem Biophys Res Commun. 2005;326:527–38.
   PubMed Web of Science ®Google Scholar
• Limbert C, Ebert R, Schilling T, Path G, Benisch P, Klein-Hitpass L, . Functional signature of human islet-derived precursor cells compared to bone marrow-derived mesenchymal stem cells. Stem Cells Dev. 2010;19(5):679–91.
   Google Scholar
• Simonsen JL, Rosada C, Serakinci N, Justesen J, Stenderup K, Rattan SI, . Telomerase expression extends the proliferative life-span and maintains the osteogenic potential of human bone marrow stromal cells. Nat Biotechnol. 2002; 20:592–6.
   PubMed Web of Science ®Google Scholar
• Brandhorst H, Brandhorst D, Brendel MD, Hering BJ, Bretzel RG. Assessment of intracellular insulin content during all steps of human islet isolation procedure. Cell Transplant. 1998;7:489–95.
   Google Scholar
• Ricordi C, Lacy PE, Finke EH, Olack BJ, Scharp DW. Automated method for isolation of human pancreatic islets. Diabetes. 1988;37:413–20.
   PubMed Web of Science ®Google Scholar
• Otonkoski T, Beattie GM, Mally MI, Ricordi C, Hayek A. Nicotinamide is a potent inducer of endocrine differentiation in cultured human fetal pancreatic cells. J Clin Invest. 1993;92:1459–66.
   PubMed Web of Science ®Google Scholar
• Zalzman M, Anker-Kitai L, Efrat S. Differentiation of human liver-derived, insulin-producing cells toward the beta-cell phenotype. Diabetes. 2005;54:2568–75.
   PubMed Web of Science ®Google Scholar
• Lee JC, Smith SB, Watada H, Lin J, Scheel D, Wang J, . Regulation of the pancreatic pro-endocrine gene neurogenin3. Diabetes. 2001;50:928–36.
   PubMed Web of Science ®Google Scholar
• Niu X, Perakakis N, Laubner K, Limbert C, Stahl T, Brendel MD, . Human Kruppel-like factor 11 inhibits human proinsulin promoter activity in pancreatic beta cells. Diabetologia. 2007;50:1433–41.
   Google Scholar
• Tondreau T, Lagneaux L, Dejeneffe M, Massy M, Mortier C, Delforge A, . Bone marrow-derived mesenchymal stem cells already express specific neural proteins before any differentiation. Differentiation. 2004;72:319–26.
   PubMed Web of Science ®Google Scholar
• Ferber S, Halkin A, Cohen H, Ber I, Einav Y, Goldberg I, . Pancreatic and duodenal homeobox gene 1 induces expression of insulin genes in liver and ameliorates streptozotocin-induced hyperglycemia. Nat Med. 2000;6:568–72.
   PubMed Web of Science ®Google Scholar
• Suzuki A, Nakauchi H, Taniguchi H. Prospective isolation of multipotent pancreatic progenitors using flow-cytometric cell sorting. Diabetes. 2004;53:2143–52.
   PubMedGoogle Scholar
• Neuss S, Becher E, Woltje M, Tietze L, Jahnen-Dechent W. Functional expression of HGF and HGF receptor/c-met in adult human mesenchymal stem cells suggests a role in cell mobilization, tissue repair, and wound healing. Stem Cells. 2004;22:405–14.
   PubMed Web of Science ®Google Scholar
• Zhou Q, Brown J, Kanarek A, Rajagopal J, Melton DA. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature. 2008;455:627–32.
   PubMed Web of Science ®Google Scholar
• Serakinci N, Guldberg P, Burns JS, Abdallah B, Schrodder H, Jensen T, . Adult human mesenchymal stem cell as a target for neoplastic transformation. Oncogene. 2004;23:5095–8.
   PubMed Web of Science ®Google Scholar
• Chou YH, Khuon S, Herrmann H, Goldman RD. Nestin promotes the phosphorylation-dependent disassembly of vimentin intermediate filaments during mitosis. Mol Biol Cell. 2003;14:1468–78.
   PubMed Web of Science ®Google Scholar
• Timper K, Seboek D, Eberhardt M, Linscheid P, Christ-Crain M, Keller U, . Human adipose tissue-derived mesenchymal stem cells differentiate into insulin, somatostatin, and glucagon expressing cells. Biochem Biophys Res Commun. 2006;341:1135–40.
   PubMed Web of Science ®Google Scholar
• Yamamoto K, Miyagawa J, Waguri M, Sasada R, Igarashi K, Li M, . Recombinant human betacellulin promotes the neogenesis of beta-cells and ameliorates glucose intolerance in mice with diabetes induced by selective alloxan perfusion. Diabetes. 2000;49:2021–7.
   PubMed Web of Science ®Google Scholar
• Moriscot C, de Fraipont F, Richard MJ, Marchand M, Savatier P, Bosco D, . Human bone marrow mesenchymal stem cells can express insulin and key transcription factors of the endocrine pancreas developmental pathway upon genetic and/or microenvironmental manipulation in vitro. Stem Cells. 2005;23:594–603.
   PubMed Web of Science ®Google Scholar
• Cerf ME. Transcription factors regulating beta-cell function. Eur J Endocrinol. 2006;155:671–9.
   PubMed Web of Science ®Google Scholar
• Xu X, D'Hoker J, Stange G, Bonne S, De Leu N, Xiao X, . Beta cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell. 2008;132:197–207.
   PubMed Web of Science ®Google Scholar
• Kodama S, Toyonaga T, Kondo T, Matsumoto K, Tsuruzoe K, Kawashima J, . Enhanced expression of PDX-1 and Ngn3 by exendin-4 during beta cell regeneration in STZ-treated mice. Biochem Biophys Res Commun. 2005;327:1170–8.
   PubMed Web of Science ®Google Scholar
• Joglekar MV, Parekh VS, Mehta S, Bhonde RR, Hardikar AA. MicroRNA profiling of developing and regenerating pancreas reveal post-transcriptional regulation of neurogenin3. Dev Biol. 2007;311:603–12.
   PubMed Web of Science ®Google Scholar
• Meissner A, Wernig M, Jaenisch R. Direct reprogramming of genetically unmodified fibroblasts into pluripotent stem cells. Nat Biotechnol. 2007;25:1177–81.
   PubMed Web of Science ®Google Scholar
• Park IH, Zhao R, West JA, Yabuuchi A, Huo H, Ince TA, . Reprogramming of human somatic cells to pluripotency with defined factors. Nature. 2008;451:141–6.
   PubMed Web of Science ®Google Scholar
• Duinsbergen D, Salvatori D, Eriksson M, Mikkers H. Tumors originating from induced pluripotent stem cells and methods for their prevention. Ann NY Acad Sci. 2009; 1176:197–204.
   Google Scholar