Improved differentiation of umbilical cord blood-derived mesenchymal stem cells into insulin-producing cells by PDX-1 mRNA transfection

Differentiation

Volumn 87, Issue 5, 2014, Pages 200-208

  Van Pham, Phuc ^a   Thi My Nguyen, Phuoc ^a   Thai Quynh Nguyen, Anh ^a   Minh Pham, Vuong ^a   Nguyen Tu Bui, Anh ^a   Thi Tung Dang, Loan ^a   Gia Nguyen, Khue ^a   Kim Phan, Ngoc ^a  

^a UNIVERSITY OF NATURAL SCIENCES   (Viet Nam)

Author keywords

Insulin producing cells; Mesenchymal stem cells; MRNA transfection; PDX 1; UCB MSCs

Indexed keywords

C PEPTIDE; GLUCOSE; INSULIN; MESSENGER RNA; NEUROGENIN 3; TRANSCRIPTION FACTOR NKX6.1; TRANSCRIPTION FACTOR PDX 1; HOMEODOMAIN PROTEIN; PANCREATIC AND DUODENAL HOMEOBOX 1 PROTEIN; TRANSACTIVATOR PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOPLASM; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; INSULIN GENE; INSULIN RELEASE; MESENCHYMAL STEM CELL; MULTIPOTENT STEM CELL; NGN3 GENE; NKX6 1 GENE; PANCREAS ISLET BETA CELL; PDX 1 GENE; PROTEIN EXPRESSION; STEM CELL EXPANSION; UMBILICAL CORD BLOOD; BIOSYNTHESIS; CYTOLOGY; DIABETES MELLITUS; FETUS BLOOD; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY;

CELL DIFFERENTIATION; DIABETES MELLITUS; FETAL BLOOD; HOMEODOMAIN PROTEINS; HUMANS; INSULIN; INSULIN-SECRETING CELLS; MESENCHYMAL STROMAL CELLS; RNA, MESSENGER; TRANS-ACTIVATORS; TRANSFECTION;

EID: 84908573062     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2014.08.001     Document Type: Article

References (54)

1. Aarntzen E.H., Schreibelt G., Bol K., Lesterhuis W.J., Croockewit A.J., de Wilt J.H., van Rossum M.M., Blokx W.A., Jacobs J.F., Duiveman-de Boer T., Schuurhuis D.H., Mus R., Thielemans K., de Vries I.J., Figdor C.G., Punt C.J., Adema G.J. Vaccination with mRNA-electroporated dendritic cells induces robust tumor antigen-specific CD4+ and CD8+ T cells responses in stage III and IV melanoma patients. Clin. Cancer Res. 2012, 18:5460-5470. (An Official Journal of The American Association for Cancer Research).
2. Alipio Z., Liao W., Roemer E.J., Waner M., Fink L.M., Ward D.C., Ma Y. Reversal of hyperglycemia in diabetic mouse models using induced-pluripotent stem (iPS)-derived pancreatic beta-like cells. Proc. Nat. Acad. Sci. U.S.A. 2010, 107:13426-13431.
3. Arnold A., Naaldijk Y.M., Fabian C., Wirth H., Binder H., Nikkhah G., Armstrong L., Stolzing A. Reprogramming of human huntington fibroblasts using mRNA. ISRN Cell Biol. 2012, 2012:12.
4. Bernal J.A. RNA-based tools for nuclear reprogramming and lineage-conversion: towards clinical applications. J. Cardiovasc. Transl. Res. 2013, 6:956-968.
5. Bonehill A., Van Nuffel A.M., Corthals J., Tuyaerts S., Heirman C., Francois V., Colau D., van der Bruggen P., Neyns B., Thielemans K. Single-step antigen loading and activation of dendritic cells by mRNA electroporation for the purpose of therapeutic vaccination in melanoma patients. Clin. Cancer Res. 2009, 15:3366-3375. (An Official Journal of The American Association for Cancer Research).
6. Boroujeni Z.N., Aleyasin A. Insulin producing cells established using non-integrated lentiviral vector harboring PDX1 gene. World J. Stem Cells 2013, 5:217-228.
7. Bretherton-Watt D., Gore N., Boam D.S. Insulin upstream factor 1 and a novel ubiquitous factor bind to the human islet amyloid polypeptide/amylin gene promoter. Biochem. J. 1996, 313:495-502.
8. Carty M.D., Lillquist J.S., Peshavaria M., Stein R., Soeller W.C. Identification of cis- and trans-active factors regulating human islet amyloid polypeptide gene expression in pancreatic beta-cells. J. Biol. Chem. 1997, 272:11986-11993.
9. Chandra V.G S., Phadnis S., Nair P.D., Bhonde R.R. Generation of pancreatic hormone-expressing islet-like cell aggregates from murine adipose tissue-derived stem cells. Stem Cells (Dayton, Ohio) 2009, 27:1941-1953.
10. Coosemans A., Vanderstraeten A., Tuyaerts S., Verschuere T., Moerman P., Berneman Z., Vergote I., Amant F., Van Gool S.W. Immunological response after WT1 mRNA-loaded dendritic cell immunotherapy in ovarian carcinoma and carcinosarcoma. Anticancer Res. 2013, 33:3855-3859.
11. Dave U.P., Akagi K., Tripathi R., Cleveland S.M., Thompson M.A., Yi M., Stephens R., Downing J.R., Jenkins N.A., Copeland N.G. Murine leukemias with retroviral insertions at Lmo2 are predictive of the leukemias induced in SCID-X1 patients following retroviral gene therapy. PLos Genet. 2009, 5:e1000491.
12. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., Deans R., Keating A., Prockop D., Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-317.
13. Guo Q.S., Zhu M.Y., Wang L., Fan X.J., Lu Y.H., Wang Z.W., Zhu S.J., Wang Y., Huang Y. Combined transfection of the three transcriptional factors, PDX-1, NeuroD1, and MafA, causes differentiation of bone marrow mesenchymal stem cells into insulin-producing cells. Exp. Diabetes Res. 2012, 2012:672013.
14. Hacein-Bey-Abina S., Garrigue A., Wang G.P., Soulier J., Lim A., Morillon E., Clappier E., Caccavelli L., Delabesse E., Beldjord K., Asnafi V., MacIntyre E., Dal Cortivo L., Radford I., Brousse N., Sigaux F., Moshous D., Hauer J., Borkhardt A., Belohradsky B.H., Wintergerst U., Velez M.C., Leiva L., Sorensen R., Wulffraat N., Blanche S., Bushman F.D., Fischer A., Cavazzana-Calvo M. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J. Clin. Invest. 2008, 118:3132-3142.
15. He D., Wang J., Gao Y., Zhang Y. Differentiation of PDX1 gene-modified human umbilical cord mesenchymal stem cells into insulin-producing cells in vitro. Int. J. Mol. Med. 2011, 28:1019-1024.
16. Howe S.J., Mansour M.R., Schwarzwaelder K., Bartholomae C., Hubank M., Kempski H., Brugman M.H., Pike-Overzet K., Chatters S.J., de Ridder D., Gilmour K.C., Adams S., Thornhill S.I., Parsley K.L., Staal F.J., Gale R.E., Linch D.C., Bayford J., Brown L., Quaye M., Kinnon C., Ancliff P., Webb D.K., Schmidt M., von Kalle C., Gaspar H.B., Thrasher A.J. Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J. Clin. Invest. 2008, 118:3143-3150.
17. Hua X.F., Wang Y.W., Tang Y.X., Yu S.Q., Jin S.H., Meng X.M., Li H.F., Liu F.J., Sun Q., Wang H.Y., Li J.Y. Pancreatic insulin-producing cells differentiated from human embryonic stem cells correct hyperglycemia in SCID/NOD mice, an animal model of diabetes. PLoS One 2014, 9:e102198.
18. Jeon K., Lim H., Kim J.H., Thuan N.V., Park S.H., Lim Y.M., Choi H.Y., Lee E.R., Kim J.H., Lee M.S., Cho S.G. Differentiation and transplantation of functional pancreatic beta cells generated from induced pluripotent stem cells derived from a type 1 diabetes mouse model. Stem Cells Dev. 2012, 21:2642-2655.
19. Jiang J., Au M., Lu K., Eshpeter A., Korbutt G., Fisk G., Majumdar A.S. Generation of insulin-producing islet-like clusters from human embryonic stem cells. Stem Cells (Dayton, Ohio) 2007, 25:1940-1953.
20. Kadam S., Muthyala S., Nair P., Bhonde R. Human placenta-derived mesenchymal stem cells and islet-like cell clusters generated from these cells as a novel source for stem cell therapy in diabetes. Rev. Diabetic Stud.: RDS 2010, 7:168-182.
21. Lee M.W., Choi J., Yang M.S., Moon Y.J., Park J.S., Kim H.C., Kim Y.J. Mesenchymal stem cells from cryopreserved human umbilical cord blood. Biochem. Biophys. Res. Commun. 2004, 320:273-278.
22. Lee O.K., Kuo T.K., Chen W.M., Lee K.D., Hsieh S.L., Chen T.H. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood 2004, 103:1669-1675.
23. Li L., Li F., Qi H., Feng G., Yuan K., Deng H., Zhou H. Coexpression of Pdx1 and betacellulin in mesenchymal stem cells could promote the differentiation of nestin-positive epithelium-like progenitors and pancreatic islet-like spheroids. Stem Cells Dev. 2008, 17:815-823.
24. Li Y., Zhang R., Qiao H., Zhang H., Wang Y., Yuan H., Liu Q., Liu D., Chen L., Pei X. Generation of insulin-producing cells from PDX-1 gene-modified human mesenchymal stem cells. J. Cell. Physiol. 2007, 211:36-44.
25. Limbert C., Path G., Ebert R., Rothhammer V., Kassem M., Jakob F., Seufert J. PDX1- and NGN3-mediated in vitro reprogramming of human bone marrow-derived mesenchymal stromal cells into pancreatic endocrine lineages. Cytotherapy 2011, 13:802-813.
26. Lui K.O., Zangi L., Silva E.A., Bu L., Sahara M., Li R.A., Mooney D.J., Chien K.R. Driving vascular endothelial cell fate of human multipotent Isl1+ heart progenitors with VEGF modified mRNA. Cell Res. 2013, 23:1172-1186.
27. Mandal P.K., Rossi D.J. Reprogramming human fibroblasts to pluripotency using modified mRNA. Nat. Protoc. 2013, 8:568-582.
28. Nguyen P.T.-M., Nguyen A.T.-Q., Nguyen N.T., Nguyen N.T.-M., Duong T.T., Truong N.H., Phan N.K. Human umbilical cord blood derived mesenchymal stem cells were differentiated into pancreatic endocrine cell by Pdx-1 electrotransfer. Biomed. Res. Ther. 2014, 1:50-56.
29. Noguchi H., Naziruddin B., Shimoda M., Fujita Y., Chujo D., Takita M., Peng H., Sugimoto K., Itoh T., Tamura Y., Olsen G.S., Kobayashi N., Onaca N., Hayashi S., Levy M.F., Matsumoto S. Induction of insulin-producing cells from human pancreatic progenitor cells. Transplant. Proc. 2010, 42:2081-2083.
30. Ohlsson H., Karlsson K., Edlund T. IPF1, a homeodomain-containing transactivator of the insulin gene. EMBO J. 1993, 12:4251-4259.
31. Overes I.M., Fredrix H., Kester M.G., Falkenburg J.H., van der Voort R., de Witte T.M., Dolstra H. Efficient activation of LRH-1-specific CD8+ T-cell responses from transplanted leukemia patients by stimulation with P2×5 mRNA-electroporated dendritic cells. J. Immunother. (Hagerstown, Md.: 1997) 2009, 32:539-551.
32. Parekh V.S., Joglekar M.V., Hardikar A.A. Differentiation of human umbilical cord blood-derived mononuclear cells to endocrine pancreatic lineage. Differ. Res. Biol. Divers. 2009, 78:232-240.
33. Phadnis S.M., Joglekar M.V., Dalvi M.P., Muthyala S., Nair P.D., Ghaskadbi S.M., Bhonde R.R., Hardikar A.A. Human bone marrow-derived mesenchymal cells differentiate and mature into endocrine pancreatic lineage in vivo. Cytotherapy 2011, 13:279-293.
34. Phuc P.V., Nhung T.H., Loan D.T., Chung D.C., Ngoc P.K. Differentiating of banked human umbilical cord blood-derived mesenchymal stem cells into insulin-secreting cells. In vitro cellular and developmental biology. Animal 2011, 47:54-63.
35. Plews J.R., Li J., Jones M., Moore H.D., Mason C., Andrews P.W., Na J. Activation of pluripotency genes in human fibroblast cells by a novel mRNA based approach. PLoS One 2010, 5:e14397.
36. Prabakar K.R., Dominguez-Bendala J., Molano R.D., Pileggi A., Villate S., Ricordi C., Inverardi L. Generation of glucose-responsive, insulin-producing cells from human umbilical cord blood-derived mesenchymal stem cells. Cell Transplant. 2012, 21:1321-1339.
37. Rahmati S., Alijani N., Kadivar M. In vitro generation of glucose-responsive insulin producing cells using lentiviral based pdx-1 gene transduction of mouse (C57BL/6) mesenchymal stem cells. Biochem. Biophys. Res. Commun. 2013, 437:413-419.
38. Serup P., Jensen J., Andersen F.G., Jorgensen M.C., Blume N., Holst J.J., Madsen O.D. Induction of insulin and islet amyloid polypeptide production in pancreatic islet glucagonoma cells by insulin promoter factor 1. Proc. Nat. Acad. Sci. U.S.A. 1996, 93:9015-9020.
39. Sun J., Yang Y., Wang X., Song J., Jia Y. Expression of Pdx-1 in bone marrow mesenchymal stem cells promotes differentiation of islet-like cells in vitro. Sci. China, Ser. C Life Sci./Chin. Acad. Sci. 2006, 49:480-489.
40. Talebi S., Aleyasin A., Soleimani M., Massumi M. Derivation of islet-like cells from mesenchymal stem cells using PDX1-transducing lentiviruses. Biotechnol. Appl. Biochem. 2012, 59:205-212.
41. Tavernier G., Wolfrum K., Demeester J., De Smedt S.C., Adjaye J., Rejman J. Activation of pluripotency-associated genes in mouse embryonic fibroblasts by non-viral transfection with in vitro-derived mRNAs encoding Oct4, Sox2, Klf4 and cMyc. Biomaterials 2012, 33:412-417.
42. Tsai P.J., Wang H.S., Shyr Y.M., Weng Z.C., Tai L.C., Shyu J.F., Chen T.H. Transplantation of insulin-producing cells from umbilical cord mesenchymal stem cells for the treatment of streptozotocin-induced diabetic rats. J. Biomed. Sci. 2012, 19:47.
43. Van Nuffel A.M., Benteyn D., Wilgenhof S., Corthals J., Heirman C., Neyns B., Thielemans K., Bonehill A. Intravenous and intradermal TriMix-dendritic cell therapy results in a broad T-cell response and durable tumor response in a chemorefractory stage IV-M1c melanoma patient. Cancer Immunol., Immunother.: CII 2012, 61:1033-1043.
44. Van Nuffel A.M., Corthals J., Neyns B., Heirman C., Thielemans K., Bonehill A. Immunotherapy of cancer with dendritic cells loaded with tumor antigens and activated through mRNA electroporation. Methods Mol. Biol. (Clifton, N.J.) 2010, 629:405-452.
45. Waeber G., Thompson N., Nicod P., Bonny C. Transcriptional activation of the GLUT2 gene by the IPF-1/STF-1/IDX-1 homeobox factor. Mol. Endocrinol. (Baltimore, Md.) 1996, 10:1327-1334.
46. Wang J., Gao Y., Lu Y., Tang X., He D., Zhang Y. Induced differentiation of human umbilical cord mesenchymal stem modified by cells Pdx1gene into islet beta-like cells in vitro. Sheng wu yi xue gong cheng xue za zhi=J. Biomed. Eng.=Shengwu yixue gongchengxue zazhi 2011, 28(1175-1180):1206.
47. Warren L., Manos P.D., Ahfeldt T., Loh Y.H., Li H., Lau F., Ebina W., Mandal P.K., Smith Z.D., Meissner A., Daley G.Q., Brack A.S., Collins J.J., Cowan C., Schlaeger T.M., Rossi D.J. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 2010, 7:618-630.
48. Watada H., Kajimoto Y., Umayahara Y., Matsuoka T., Kaneto H., Fujitani Y., Kamada T., Kawamori R., Yamasaki Y. The human glucokinase gene beta-cell-type promoter: an essential role of insulin promoter factor 1/PDX-1 in its activation in HIT-T15 cells. Diabetes 1996, 45:1478-1488.
49. Wiehe J.M., Ponsaerts P., Rojewski M.T., Homann J.M., Greiner J., Kronawitter D., Schrezenmeier H., Hombach V., Wiesneth M., Zimmermann O., Torzewski J. mRNA-mediated gene delivery into human progenitor cells promotes highly efficient protein expression. J. Cell. Mol. Med. 2007, 11:521-530.
50. Wilgenhof S., Van Nuffel A.M., Corthals J., Heirman C., Tuyaerts S., Benteyn D., De Coninck A., Van Riet I., Verfaillie G., Vandeloo J., Bonehill A., Thielemans K., Neyns B. Therapeutic vaccination with an autologous mRNA electroporated dendritic cell vaccine in patients with advanced melanoma. J. Immunother. (Hagerstown, Md.: 1997) 2011, 34:448-456.
51. Yuan H., Liu H., Tian R., Li J., Zhao Z. Regulation of mesenchymal stem cell differentiation and insulin secretion by differential expression of Pdx-1. Mol. Biol. Rep. 2012, 39:7777-7783.
52. Zaldumbide A., Carlotti F., Goncalves M.A., Knaan-Shanzer S., Cramer S.J., Roep B.O., Wiertz E.J., Hoeben R.C. Adenoviral vectors stimulate glucagon transcription in human mesenchymal stem cells expressing pancreatic transcription factors. PLoS One 2012, 7:e48093.
53. Zangi L., Lui K.O., von Gise A., Ma Q., Ebina W., Ptaszek L.M., Spater D., Xu H., Tabebordbar M., Gorbatov R., Sena B., Nahrendorf M., Briscoe D.M., Li R.A., Wagers A.J., Rossi D.J., Pu W.T., Chien K.R. Modified mRNA directs the fate of heart progenitor cells and induces vascular regeneration after myocardial infarction. Nat. Biotechnol. 2013, 31:898-907.
54. Zhu F.F., Zhang P.B., Zhang D.H., Sui X., Yin M., Xiang T.T., Shi Y., Ding M.X., Deng H. Generation of pancreatic insulin-producing cells from rhesus monkey induced pluripotent stem cells. Diabetologia 2011, 54:2325-2336.