Mutual effect of subcutaneously transplanted human adipose-derived stem cells and pancreatic islets within fibrin gel

Biomaterials

Volumn 34, Issue 30, 2013, Pages 7247-7256

  Bhang, Suk Ho ^a   Jung, Min Jin ^b   Shin, Jung Youn ^a   La, Wan Geun ^a   Hwang, Yong Hwa ^b   Kim, Min Jun ^b   Kim, Byung Soo ^a,c   Lee, Dong Yun ^b  

^a Seoul National University   (South Korea)

^b Hanyang University   (South Korea)

^c Bio MAX Institute   (South Korea)

Author keywords

Adipose derived stem cells; Diabetes; Hypoxia; Pancreatic islets; Transplantation

Indexed keywords

ADIPOSE DERIVED STEM CELLS; FIBROBLAST GROWTH FACTOR-2; HUMAN ENDOTHELIAL CELLS; HYPOXIA; ISLET TRANSPLANTATION; PANCREATIC ISLET; SUBCUTANEOUS TISSUES; VASCULAR ENDOTHELIAL GROWTH FACTOR;

CELL ENGINEERING; ENDOTHELIAL CELLS; INSULIN; MAMMALS; MEDICAL PROBLEMS; STEM CELLS; TISSUE; TRANSPLANTATION (SURGICAL);

SYNCHROTRONS;

ADENOSINE DIPHOSPHATE; FIBRIN; FIBROBLAST GROWTH FACTOR 2; GLUCOSE; INSULIN; VASCULOTROPIN;

ADIPOSE DERIVED STEM CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL VIABILITY; CONTROLLED STUDY; DIABETES MELLITUS; ENDOTHELIUM CELL; GEL; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INSULIN RELEASE; MALE; MICROVASCULATURE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL; PANCREAS TRANSPLANTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUBCUTANEOUS TISSUE; TREATMENT INDICATION;

ADIPOSE-DERIVED STEM CELLS; DIABETES; HYPOXIA; PANCREATIC ISLETS; TRANSPLANTATION;

ADIPOSE TISSUE; ANIMALS; BIOLOGICAL MARKERS; COCULTURE TECHNIQUES; DIABETES MELLITUS, EXPERIMENTAL; FIBRIN; FIBROBLAST GROWTH FACTOR 2; GELS; HUMANS; ISLETS OF LANGERHANS; ISLETS OF LANGERHANS TRANSPLANTATION; MICE; MICROVESSELS; NEOVASCULARIZATION, PHYSIOLOGIC; RATS; RATS, INBRED LEW; STEM CELL TRANSPLANTATION; SUBCUTANEOUS TISSUE; TISSUE SURVIVAL; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

MUS; RATTUS;

EID: 84880511706     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.06.018     Document Type: Article

References (50)

1. Shapiro A.M., Ricordi C., Hering B.J., Auchincloss H., Lindblad R., Robertson R.P., et al. International trial of the Edmonton protocol for islet transplantation. NEngl J Med 2006, 355:1318-1330.
2. Ryan E.A., Lakey J.R., Rajotte R.V., Korbutt G.S., Kin T., Imes S., et al. Clinical outcomes and insulin secretion after islet transplantation with the Edmonton protocol. Diabetes 2001, 50:710-719.
3. Merani S., Toso C., Emamaullee J., Shapiro A.M. Optimal implantation site for pancreatic islet transplantation. Br J Surg 2008, 95:1449-1461.
4. Bennet W., Groth C.G., Larsson R., Nilsson B., Korsgren O. Isolated human islets trigger an instant blood mediated inflammatory reaction: implications for intraportal islet transplantation as a treatment for patients with type 1 diabetes. Ups J Med Sci 2000, 105:125-133.
5. Barshes N.R., Wyllie S., Goss J.A. Inflammation-mediated dysfunction and apoptosis in pancreatic islet transplantation: implications for intrahepatic grafts. JLeukoc Biol 2005, 77:587-597.
6. Citro A., Cantarelli E., Maffi P., Nano R., Melzi R., Mercalli A., et al. CXCR1/2 inhibition enhances pancreatic islet survival after transplantation. JClin Invest 2012, 122:3647-3651.
7. Carlsson P.O., Palm F., Andersson A., Liss P. Chronically decreased oxygen tension in rat pancreatic islets transplanted under the kidney capsule. Transplantation 2000, 69:761-766.
8. Carlsson P.O., Palm F., Andersson A., Liss P. Markedly decreased oxygen tension in transplanted rat pancreatic islets irrespective of the implantation site. Diabetes 2001, 50:489-495.
9. Fox I.J., Schafer D.F., Yannam G.R. Finding a home for cell transplants: location, location, location. Am J Transplant 2006, 6:5-6.
10. Pileggi A., Molano R.D., Ricordi C., Zahr E., Collins J., Valdes R., et al. Reversal of diabetes by pancreatic islet transplantation into a subcutaneous, neovascularized device. Transplantation 2006, 81:1318-1324.
11. Kawakami Y., Iwata H., Gu Y., Miyamoto M., Murakami Y., Yamasaki T., et al. Modified subcutaneous tissue with neovascularization is useful as the site for pancreatic islet transplantation. Cell Transplant 2000, 9:729-731.
12. Ohashi K., Yokoyama T., Yamato M., Kuge H., Kanehiro H., Tsutsumi M., et al. Engineering functional two- and three-dimensional liver systems invivo using hepatic tissue sheets. Nat Med 2007, 13:880-885.
13. Kemp C.B., Knight M.J., Scharp D.W., Ballinger W.F., Lacy P.E. Effect of transplantation site on the results of pancreatic islet isografts in diabetic rats. Diabetologia 1973, 9:486-491.
14. Kawakami Y., Iwata H., Gu Y.J., Miyamoto M., Murakami Y., Balamurugan A.N., et al. Successful subcutaneous pancreatic islet transplantation using an angiogenic growth factor-releasing device. Pancreas 2001, 23:375-381.
15. Bharat A., Benshoff N., Olack B., Ramachandran S., Desai N.M., Mohanakumar T. Novel invivo murine model to study islet potency: engraftment and function. Transplantation 2005, 79:1627-1630.
16. Rafael E., Wu G.S., Hultenby K., Tibell A., Wernerson A. Improved survival of macroencapsulated islets of Langerhans by preimplantation of the immunoisolating device: a morphometric study. Cell Transplant 2003, 12:407-412.
17. Dufour J.M., Rajotte R.V., Zimmerman M., Rezania A., Kin T., Dixon D.E., et al. Development of an ectopic site for islet transplantation, using biodegradable scaffolds. Tissue Eng 2005, 11:1323-1331.
18. Blomeier H., Zhang X., Rives C., Brissova M., Hughes E., Baker M., et al. Polymer scaffolds as synthetic microenvironments for extrahepatic islet transplantation. Transplantation 2006, 82:452-459.
19. Veriter S., Mergen J., Goebbels R.M., Aouassar N., Gregoire C., Jordan B., et al. Invivo selection of biocompatible alginates for islet encapsulation and subcutaneous transplantation. Tissue Eng Part A 2010, 16:1503-1513.
20. Cao Y., Sun Z., Liao L., Meng Y., Han Q., Zhao R.C. Human adipose tissue-derived stem cells differentiate into endothelial cells invitro and improve postnatal neovascularization invivo. Biochem Biophys Res Commun 2005, 332:370-379.
21. Planat-Benard V., Silvestre J.S., Cousin B., Andre M., Nibbelink M., Tamarat R., et al. Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 2004, 109:656-663.
22. Bhang S.H., Cho S.W., Lim J.M., Kang J.M., Lee T.J., Yang H.S., et al. Locally delivered growth factor enhances the angiogenic efficacy of adipose-derived stromal cells transplanted to ischemic limbs. Stem Cells 2009, 27:1976-1986.
23. Bhang S.H., Cho S.W., La W.G., Lee T.J., Yang H.S., Sun A.Y., et al. Angiogenesis in ischemic tissue produced by spheroid grafting of human adipose-derived stromal cells. Biomaterials 2011, 32:2734-2747.
24. Cousin B., Ravet E., Poglio S., De Toni F., Bertuzzi M., Lulka H., et al. Adult stromal cells derived from human adipose tissue provoke pancreatic cancer cell death both invitro and invivo. PLoS One 2009, 4:e6278.
25. Matsumoto D., Sato K., Gonda K., Takaki Y., Shigeura T., Sato T., et al. Cell-assisted lipotransfer: supportive use of human adipose-derived cells for soft tissue augmentation with lipoinjection. Tissue Eng 2006, 12:3375-3382.
26. Ghannam S., Bouffi C., Djouad F., Jorgensen C., Noel D. Immunosuppression by mesenchymal stem cells: mechanisms and clinical applications. Stem Cell Res Ther 2010, 1:2.
27. Cappellesso-Fleury S., Puissant-Lubrano B., Apoil P.A., Titeux M., Winterton P., Casteilla L., et al. Human fibroblasts share immunosuppressive properties with bone marrow mesenchymal stem cells. JClin Immunol 2010, 30:607-619.
28. Keyser K.A., Beagles K.E., Kiem H.P. Comparison of mesenchymal stem cells from different tissues to suppress T-cell activation. Cell Transplant 2007, 16:555-562.
29. Tapp H., Hanley E.N., Patt J.C., Gruber H.E. Adipose-derived stem cells: characterization and current application in orthopaedic tissue repair. Exp Biol Med (Maywood) 2009, 234:1-9.
30. Fumimoto Y., Matsuyama A., Komoda H., Okura H., Lee C.M., Nagao A., et al. Creation of a rich subcutaneous vascular network with implanted adipose tissue-derived stromal cells and adipose tissue enhances subcutaneous grafting of islets in diabetic mice. Tissue Eng Part C Methods 2009, 15:437-444.
31. Clark H., Barbari T.A., Stump K., Rao G. Histologic evaluation of the inflammatory response around implanted hollow fiber membranes. JBiomed Mater Res 2000, 52:183-192.
32. Nakagami H., Maeda K., Morishita R., Iguchi S., Nishikawa T., Takami Y., et al. Novel autologous cell therapy in ischemic limb disease through growth factor secretion by cultured adipose tissue-derived stromal cells. Arterioscler Thromb Vasc Biol 2005, 25:2542-2547.
33. Rehman J., Traktuev D., Li J., Merfeld-Clauss S., Temm-Grove C.J., Bovenkerk J.E., et al. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 2004, 109:1292-1298.
34. Giaccia A., Siim B.G., Johnson R.S. HIF-1 as a target for drug development. Nat Rev Drug Discov 2003, 2:803-811.
35. Zelzer E., Levy Y., Kahana C., Shilo B.Z., Rubinstein M., Cohen B. Insulin induces transcription of target genes through the hypoxia-inducible factor HIF-1alpha/ARNT. EMBO J 1998, 17:5085-5094.
36. Feldser D., Agani F., Iyer N.V., Pak B., Ferreira G., Semenza G.L. Reciprocal positive regulation of hypoxia-inducible factor 1alpha and insulin-like growth factor 2. Cancer Res 1999, 59:3915-3918.
37. Stiehl D.P., Jelkmann W., Wenger R.H., Hellwig-Burgel T. Normoxic induction of the hypoxia-inducible factor 1alpha by insulin and interleukin-1beta involves the phosphatidylinositol 3-kinase pathway. FEBS Lett 2002, 512:157-162.
38. Roth U., Curth K., Unterman T.G., Kietzmann T. The transcription factors HIF-1 and HNF-4 and the coactivator p300 are involved in insulin-regulated glucokinase gene expression via the phosphatidylinositol 3-kinase/protein kinase B pathway. JBiol Chem 2004, 23(279):2623-2631.
39. Kietzmann T., Samoylenko A., Roth U., Jungermann K. Hypoxia-inducible factor-1 and hypoxia response elements mediate the induction of plasminogen activator inhibitor-1 gene expression by insulin in primary rat hepatocytes. Blood 2003, 101:907-914.
40. Jiang J., Au M., Lu K., Eshpeter A., Korbutt G., Fisk G., et al. Generation of insulin-producing islet-like clusters from human embryonic stem cells. Stem Cells 2007, 25:1940-1953.
41. D'Amour K.A., Bang A.G., Eliazer S., Kelly O.G., Agulnick A.D., Smart N.G., et al. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol 2006, 24:1392-1401.
42. Phillips B.W., Hentze H., Rust W.L., Chen Q.P., Chipperfield H., Tan E.K., et al. Directed differentiation of human embryonic stem cells into the pancreatic endocrine lineage. Stem Cells Dev 2007, 16:561-578.
43. Chao K.C., Chao K.F., Fu Y.S., Liu S.H. 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.
44. Lin H.Y., Tsai C.C., Chen L.L., Chiou S.H., Wang Y.J., Hung S.C. Fibronectin and laminin promote differentiation of human mesenchymal stem cells into insulin producing cells through activating Akt and ERK. JBiomed Sci 2010, 17:56.
45. Kang H.M., Kim J., Park S., Kim J., Kim H., Kim K.S., et al. Insulin-secreting cells from human eyelid-derived stem cells alleviate type I diabetes in immunocompetent mice. Stem Cells 2009, 27:1999-2008.
46. Kang H.M., Park S., Kim H. Insulin-like growth factor 2 enhances insulinogenic differentiation of human eyelid adipose stem cells via the insulin receptor. Cell Prolif 2011, 44:254-263.
47. Moon M.H., Kim S.Y., Kim Y.J., Kim S.J., Lee J.B., Bae Y.C., et al. Human adipose tissue-derived mesenchymal stem cells improve postnatal neovascularization in a mouse model of hindlimb ischemia. Cell Physiol Biochem 2006, 17:279-290.
48. Parr E.L., Bowen K.M., Lafferty K.J. Cellular changes in cultured mouse thyroid glands and islets of Langerhans. Transplantation 1980, 30:135-141.
49. Timper K., Seboek D., Eberhardt M., Linscheid P., Christ-Crain M., Keller U., et al. Human adipose tissue-derived mesenchymal stem cells differentiate into insulin, somatostatin, and glucagon expressing cells. Biochem Biophys Res Commun 2006, 341:1135-1140.
50. Lee J., Han D.J., Kim S.C. Invitro differentiation of human adipose tissue-derived stem cells into cells with pancreatic phenotype by regenerating pancreas extract. Biochem Biophys Res Commun 2008, 375:547-551.