Adipose-derived mesenchymal stem cells improve glucose homeostasis in high-fat diet-induced obese mice

Stem Cell Research and Therapy

Volumn 6, Issue 1, 2015, Pages

  Cao, Mingjun ^a   Pan, Qingjie ^b   Dong, Huansheng ^b   Yuan, Xinxu ^c   Li, Yang ^a   Sun, Zhen ^d   Dong, Xiao ^a   Wang, Hongjun ^d  

^a QINGDAO AGRICULTURAL UNIVERSITY   (China)

^b Institute of Animal Science and Veterinary Medicine of Wuhan   (China)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INSULIN; INSULIN RECEPTOR; INTERLEUKIN 6; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRIACYLGLYCEROL; GLUCOSE BLOOD LEVEL;

ADIPOCYTE; ADIPOSE DERIVED MESENCHYMAL STEM CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIET INDUCED OBESITY; EX VIVO STUDY; F480 GENE; GENE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE; IL6 GENE; INSR GENE; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN TOLERANCE TEST; LIMIT OF QUANTITATION; LIPID DIET; LIVER; MALE; MESENCHYMAL STEM CELL; MOUSE; NOD2 GENE; NONHUMAN; PANCREAS; PANCREAS ISLET BETA CELL; PPARY GENE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; TRIACYLGLYCEROL BLOOD LEVEL; ADVERSE EFFECTS; ANIMAL; BLOOD; C57BL MOUSE; CELL CULTURE; GLUCOSE INTOLERANCE; HOMEOSTASIS; INTRAABDOMINAL FAT; LIPID METABOLISM; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; OBESITY; PATHOLOGY;

ANIMALS; BLOOD GLUCOSE; CELLS, CULTURED; DIET, HIGH-FAT; GLUCOSE; GLUCOSE INTOLERANCE; HOMEOSTASIS; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; LIPID METABOLISM; LIVER; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE, INBRED C57BL; OBESITY; TRIGLYCERIDES;

EID: 84945934247     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/s13287-015-0201-3     Document Type: Article

References (52)

1. Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U, Shaw JE. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract. 2014;103:137-49. doi:10.1016/j.diabres.2013.11.002.
2. Eckel RH, Kahn SE, Ferrannini E, Goldfine AB, Nathan DM, Schwartz MW, et al. Obesity and type 2 diabetes: what can be unified and what needs to be individualized? Diabetes Care. 2011;34:1424-30. doi:10.2337/dc11-0447.
3. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315-7. doi:10.1080/14653240600855905.
4. Stagg J, Galipeau J. Mechanisms of immune modulation by mesenchymal stromal cells and clinical translation. Curr Mol Med. 2013;13:856-67.
5. Cai L, Johnstone BH, Cook TG, Liang Z, Traktuev D, Cornetta K, et al. Suppression of hepatocyte growth factor production impairs the ability of adipose-derived stem cells to promote ischemic tissue revascularization. Stem Cells. 2007;25:3234-43. doi:10.1634/stemcells.2007-0388.
6. Wei X, Zhao L, Zhong J, Gu H, Feng D, Johnstone BH, et al. Adipose stromal cells-secreted neuroprotective media against neuronal apoptosis. Neurosci Lett. 2009;462:76-9. doi:10.1016/j.neulet.2009.06.054.
7. Sun M, Wang S, Li Y, Yu L, Gu F, Wang C, et al. Adipose-derived stem cells improved mouse ovary function after chemotherapy-induced ovary failure. Stem Cell Res Ther. 2013;4:80. doi:10.1186/scrt231.
8. Takehara Y, Yabuuchi A, Ezoe K, Kuroda T, Yamadera R, Sano C, et al. The restorative effects of adipose-derived mesenchymal stem cells on damaged ovarian function. Lab Invest. 2013;93:181-93. doi:10.1038/labinvest.2012.167.
9. Lee JA, Parrett BM, Conejero JA, Laser J, Chen J, Kogon AJ, et al. Biological alchemy: engineering bone and fat from fat-derived stem cells. Ann Plast Surg. 2003;50:610-7. doi:10.1097/01.SAP.0000069069.23266.35.
10. Tobita M, Uysal AC, Ogawa R, Hyakusoku H, Mizuno H. Periodontal tissue regeneration with adipose-derived stem cells. Tissue Eng Part A. 2008;14:945-53. doi:10.1089/ten.tea.2007.0048.
11. Lendeckel S, Jodicke A, Christophis P, Heidinger K, Wolff J, Fraser JK, et al. Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report. J Craniomaxillofac Surg. 2004;32:370-3. doi:10.1016/j.jcms.2004.06.002.
12. Lee WY, Park KJ, Cho YB, Yoon SN, Song KH. do Kim S, et al. Autologous adipose tissue-derived stem cells treatment demonstrated favorable and sustainable therapeutic effect for Crohn's fistula. Stem Cells. 2013;31:2575-81. doi:10.1002/stem.1357.
13. Yoshimura K, Sato K, Aoi N, Kurita M, Inoue K, Suga H, et al. Cell-Assisted lipotransfer for facial lipoatrophy: efficacy of clinical use of adipose-derived stem cells. Dermatol Surg. 2008;34:1178-85. doi:10.1111/j.1524-4725.2008.34256.x.
14. Brey EM, Patrick Jr CW. Tissue engineering applied to reconstructive surgery. IEEE Eng Med Biol Mag. 2000;19:122-5.
15. Moshtagh PR, Emami SH, Sharifi AM. Differentiation of human adiposederived mesenchymal stem cell into insulin-producing cells: An in vitro study. J Physiol Biochem. 2013;69:451-8. doi:10.1007/s13105-012-0228-1.
16. Marappagounder D, Somasundaram I, Dorairaj S, Sankaran RJ. Differentiation of mesenchymal stem cells derived from human bone marrow and subcutaneous adipose tissue into pancreatic islet-like clusters in vitro. Cell Mol Biol Lett. 2013;18:75-88. doi:10.2478/s11658-012-0040-5.
17. Dhanasekaran M, Indumathi S, Harikrishnan R, Mishra R, Lissa RP, Rajkumar JS, et al. Human omentum fat-derived mesenchymal stem cells transdifferentiates into pancreatic islet-like cluster. Cell Biochem Funct. 2013;31:612-9. doi:10.1002/cbf.2948.
18. Chandra V. G S, Phadnis S, Nair PD, Bhonde RR. Generation of pancreatic hormone-expressing islet-like cell aggregates from murine adipose tissuederived stem cells. Stem Cells. 2009;27:1941-53. doi:10.1002/stem.117.
19. 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;341:1135-40. doi:10.1016/j.bbrc.2006.01.072.
20. Dave SD, Vanikar AV, Trivedi HL. Ex vivo generation of glucose sensitive insulin secreting mesenchymal stem cells derived from human adipose tissue. Indian J Endocrinol Metab. 2012;16:S65-69. doi:10.4103/2230-8210.94264.
21. Chandra V, Swetha G, Muthyala S, Jaiswal AK, Bellare JR, Nair PD, et al. Islet-like cell aggregates generated from human adipose tissue derived stem cells ameliorate experimental diabetes in mice. PLoS One. 2011;6, e20615. doi:10.1371/journal.pone.0020615.
22. Ohmura Y, Tanemura M, Kawaguchi N, Machida T, Tanida T, Deguchi T, et al. Combined transplantation of pancreatic islets and adipose tissue-derived stem cells enhances the survival and insulin function of islet grafts in diabetic mice. Transplantation. 2010;90:1366-73. doi:10.1097/TP.0b013e3181ffba31.
23. Veriter S, Aouassar N, Adnet PY, Paridaens MS, Stuckman C, Jordan B, et al. The impact of hyperglycemia and the presence of encapsulated islets on oxygenation within a bioartificial pancreas in the presence of mesenchymal stem cells in a diabetic Wistar rat model. Biomaterials. 2011;32:5945-56. doi:10.1016/j.biomaterials.2011.02.061.
24. Fumimoto Y, Matsuyama A, Komoda H, Okura H, Lee CM, 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;15:437-44. doi:10.1089/ten.tec.2008.0555.
25. Cavallari G, Olivi E, Bianchi F, Neri F, Foroni L, Valente S, et al. Mesenchymal stem cells and islet cotransplantation in diabetic rats: improved islet graft revascularization and function by human adipose tissue-derived stem cells preconditioned with natural molecules. Cell Transplant. 2012;21:2771-81. doi:10.3727/096368912X637046.
26. Vanikar AV, Dave SD, Thakkar UG, Trivedi HL. Cotransplantation of adipose tissue-derived insulin-secreting mesenchymal stem cells and hematopoietic stem cells: A novel therapy for insulin-dependent diabetes mellitus. Stem Cells Int. 2010;2010:582382. doi:10.4061/2010/582382.
27. Dave SD, Vanikar AV, Trivedi HL, Thakkar UG, Gopal SC, Chandra T. Novel therapy for insulin-dependent diabetes mellitus: infusion of in vitro-generated insulin-secreting cells. Clin Exp Med. 2015;15:41-5. doi:10.1007/s10238-013-0266-1.
28. Li YY, Liu HH, Chen HL, Li YP. Adipose-derived mesenchymal stem cells ameliorate STZ-induced pancreas damage in type 1 diabetes. Biomed Mater Eng. 2012;22:97-103. doi:10.3233/BME-2012-0694.
29. Rahavi H, Hashemi SM, Soleimani M, Mohammadi J, Tajik N. Adipose tissuederived mesenchymal stem cells exert in vitro immunomodulatory and beta cell protective functions in streptozotocin-induced diabetic mice model. J Diabetes Res. 2015;2015:878535. doi:10.1155/2015/878535.
30. Bassi EJ, Moraes-Vieira PM, Moreira-Sa CS, Almeida DC, Vieira LM, Cunha CS, et al. Immune regulatory properties of allogeneic adipose-derived mesenchymal stem cells in the treatment of experimental autoimmune diabetes. Diabetes. 2012;61:2534-45. doi:10.2337/db11-0844.
31. Yang Z, Li K, Yan X, Dong F, Zhao C. Amelioration of diabetic retinopathy by engrafted human adipose-derived mesenchymal stem cells in streptozotocin diabetic rats. Graefes Arch Clin Exp Ophthalmol. 2010;248:1415-22. doi:10.1007/s00417-010-1384-z.
32. Fang Y, Tian X, Bai S, Fan J, Hou W, Tong H, et al. Autologous transplantation of adipose-derived mesenchymal stem cells ameliorates streptozotocin-induced diabetic nephropathy in rats by inhibiting oxidative stress, pro-inflammatory cytokines and the p38 MAPK signaling pathway. Int J Mol Med. 2012;30:85-92. doi:10.3892/ijmm.2012.977.
33. Li D, Wang N, Zhang L, Hanyu Z, Xueyuan B, Fu B, et al. Mesenchymal stem cells protect podocytes from apoptosis induced by high glucose via secretion of epithelial growth factor. Stem Cell Res Ther. 2013;4:103. doi:10.1186/scrt314.
34. Kinoshita K, Kuno S, Ishimine H, Aoi N, Mineda K, Kato H, et al. Therapeutic Potential of Adipose-Derived SSEA-3-Positive Muse Cells for Treating Diabetic Skin Ulcers. Stem Cells Transl Med. 2015;4:146-55. doi:10.5966/sctm.2014-0181.
35. Dong H, Huang H, Yun X, Kim DS, Yue Y, Wu H, et al. Bilirubin increases insulin sensitivity in leptin-receptor deficient and diet-induced obese mice through suppression of ER stress and chronic inflammation. Endocrinology. 2014;155:818-28. doi:10.1210/en.2013-1667.
36. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3:301-13. doi:10.1016/j.stem.2008.07.003.
37. Wang H, Lee SS, Gao W, Czismadia E, McDaid J, Ollinger R, et al. Donor treatment with carbon monoxide can yield islet allograft survival and tolerance. Diabetes. 2005;54:1400-6.
38. Ezquer FE, Ezquer ME, Parrau DB, Carpio D, Yanez AJ, Conget PA. Systemic administration of multipotent mesenchymal stromal cells reverts hyperglycemia and prevents nephropathy in type 1 diabetic mice. Biol Blood Marrow Transplant. 2008;14:631-40. doi:10.1016/j.bbmt.2008.01.006.
39. Sordi V, Malosio ML, Marchesi F, Mercalli A, Melzi R, Giordano T, et al. Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood. 2005;106:419-27. doi:10.1182/blood-2004-09-3507.
40. Stienstra R, Duval C, Muller M, Kersten S. PPARs, Obesity, and Inflammation. PPAR Res. 2007;2007:95974. doi:10.1155/2007/95974.
41. Cerf ME. Beta cell dysfunction and insulin resistance. Front Endocrinol (Lausanne). 2013;4:37. doi:10.3389/fendo.2013.00037.
42. Del Guerra S, Lupi R, Marselli L, Masini M, Bugliani M, Sbrana S, et al. Functional and molecular defects of pancreatic islets in human type 2 diabetes. Diabetes. 2005;54:727-35.
43. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes. 2003;52:102-10.
44. Ji AT, Chang YC, Fu YJ, Lee OK, Ho JH. Niche-dependent regulations of metabolic balance in high-fat diet-induced diabetic mice by mesenchymal stromal cells. Diabetes. 2015;64:926-36. doi:10.2337/db14-1042.
45. Anzalone R, Lo Iacono M, Loria T, Di Stefano A, Giannuzzi P, Farina F, et al. Wharton's jelly mesenchymal stem cells as candidates for beta cells regeneration: extending the differentiative and immunomodulatory benefits of adult mesenchymal stem cells for the treatment of type 1 diabetes. Stem Cell Rev. 2011;7:342-63. doi:10.1007/s12015-010-9196-4.
46. Phinney DG, Prockop DJ. Concise review: mesenchymal stem/multipotent stromal cells: The state of transdifferentiation and modes of tissue repair-current views. Stem Cells. 2007;25:2896-902. doi:10.1634/stemcells.2007-0637.
47. Davey GC, Patil SB, O'Loughlin A, O'Brien T. Mesenchymal stem cell-based treatment for microvascular and secondary complications of diabetes mellitus. Front Endocrinol (Lausanne). 2014;5:86. doi:10.3389/fendo.2014.00086.
48. Darlington PJ, Boivin MN, Bar-Or A. Harnessing the therapeutic potential of mesenchymal stem cells in multiple sclerosis. Expert Rev Neurother. 2011;11:1295-303. doi:10.1586/ern.11.113.
49. Shin L, Peterson DA. Impaired therapeutic capacity of autologous stem cells in a model of type 2 diabetes. Stem Cells Transl Med. 2012;1:125-35. doi:10.5966/sctm.2012-0031.
50. Acosta L, Hmadcha A, Escacena N, Perez-Camacho I, de la Cuesta A, Ruiz-Salmeron R, et al. Adipose mesenchymal stromal cells isolated from type 2 diabetic patients display reduced fibrinolytic activity. Diabetes. 2013;62:4266-9. doi:10.2337/db13-0896.
51. Januszyk M, Sorkin M, Glotzbach JP, Vial IN, Maan ZN, Rennert RC, et al. Diabetes irreversibly depletes bone marrow-derived mesenchymal progenitor cell subpopulations. Diabetes. 2014;63:3047-56. doi:10.2337/db13-1366.
52. Yan J, Tie G, Wang S, Messina KE, DiDato S, Guo S, et al. Type 2 diabetes restricts multipotency of mesenchymal stem cells and impairs their capacity to augment postischemic neovascularization in db/db mice. J Am Heart Assoc. 2012;1, e002238. doi:10.1161/JAHA.112.002238.