Transplantation of human menstrual blood progenitor cells improves hyperglycemia by promoting endogenous progenitor differentiation in type 1 diabetic mice

Stem Cells and Development

Volumn 23, Issue 11, 2014, Pages 1245-1257

  Wu, Xiaoxing ^a   Luo, Yueqiu ^a   Chen, Jinyang ^a   Pan, Ruolang ^b   Xiang, Bingyu ^a   Du, Xiaochun ^c   Xiang, Lixin ^b   Shao, Jianzhong ^b   Xiang, Charlie ^a,c,d  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c S Evans Biosciences   (China)

^d Institute for Cell Based Drug Development of Zhejiang Province   (China)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; NEUROGENIN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL REGENERATION; CELL STRUCTURE; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EPITHELIUM; FEMALE; GENE EXPRESSION; HISTOLOGY; HUMAN; HUMAN CELL; HYPERGLYCEMIA; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MENSTRUATION; MOUSE; NONHUMAN; PANCREAS; PANCREAS DUCT; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGENERATIVE MEDICINE; STEM CELL TRANSPLANTATION; WEIGHT REDUCTION; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CELL CULTURE; COMPLICATION; CYTOLOGY; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; PERIPHERAL BLOOD STEM CELL TRANSPLANTATION; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; FEMALE; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; HYPERGLYCEMIA; MALE; MENSTRUATION; MICE; MICE, INBRED BALB C; PERIPHERAL BLOOD STEM CELL TRANSPLANTATION;

EID: 84901378248     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2013.0390     Document Type: Article

References (53)

1. Loomans CJ, EJ de Koning, FJ Staal, MB Rookmaaker, C Verseyden, HC de Boer, MC Verhaar, B Braam, TJ Rabelink and AJ van Zonneveld. (2004). Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes 53:196-199.
2. Laing SP, AJ Swerdlow, SD Slater, AC Burden, A Morris, NR Waugh, WGatling, PJ Bingley and CC Patterson. (2003). Mortality from heat diseases in a cohort of 23, 000 patients with insulin-treated diabetes. Diabetologia 46:760-765.
3. Ryan EA, BW Paty, PA Senior, D Bigam, E Alfadhli, NM Kneteman, JR Lakey and AM Shapiro. (2005). Five-year follow-up after clinical islet transplantation. Diabetes 54: 2060-2069.
4. Shapiro AM, JR Lakey, EA Ryan, GS Korbutt, E Toth, GL Warnock, NM Kneteman and RV Rajotte. (2000). Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N Engl J Med 343:230-238.
5. Ezquer FE, ME Ezquer, DB Parrau, D Carpio, AJ Yañez and PA Conget. (2008). Systemic administration of multipotent mesenchymal stromal cells reverts hyperglycemia and prevents nephropathy in type 1 diabetic mice. Biol Blood Marrow Transplant 14:631-640.
6. Lee RH, MJ Seo, RL Reger, JL Spees, AA Pulin, SD Olson and DJ Prockop. (2006). Multipotent stromal cells from human marrow home to and promote repair of pancreatic islets and renal glomeruli in diabetic NOD/scid mice. Proc Natl Acad Sci U S A 103:17438-17443.
7. Ende N, R Chen and AS Reddi. (2004). Effect of human umbilical cord blood cells on glycemia and insulitis in type 1 diabetic mice. Biochem Biophys Res Commun 325:665-669.
8. Ende N, R Chen and AS Reddi. (2004). Transplantation of human umbilical cord blood cells improves glycemia and glomerular hypertrophy in type 2 diabetic mice. Biochem Biophys Res Commun 321:168-171.
9. Baksh D, R Yao and RS Tuan. (2007). Comparison of proliferative and multilineage differentiation potential of human mesenchymal stem cells derived from umbilical cord and bone marrow. Stem Cells 25:1384-1392.
10. Kern S, H Eichler, J Stoeve, H Klüter and K Bieback. (2006). Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24:1294-1301.
11. Stenderup K, J Justesen, C Clausen and M Kassem. (2003). Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 33:919-926.
12. Cui CH, T Uyama, K Miyado, M Terai, S Kyo, T Kiyono and A Umezawa. (2007). Menstrual blood-derived cells confer human dystrophin expression in the murine model of Duchenne muscular dystrophy via cell fusion and myogenic transdifferentiation. Mol Biol Cell 18:1586-1594.
13. Meng X, TE Ichim, J Zhong, A Rogers, Z Yin, J Jackson, H Wang, W Ge, V Bogin, et al. (2007). Endometrial regenerative cells: a novel stem cell population. J Transl Med 5:57.
14. Patel AN, E Park, M Kuzman, F Benetti, FJ Silva and JG Allickson. (2008). Multipotent menstrual blood stromal stem cells: isolation, characterization, and differentiation. Cell Transplant 17:303-311.
15. Rossignoli F, A Caselli, G Grisendi, S Piccinno, JS Burns, A Murgia, E Veronesi, P Loschi, C Masini, et al. (2013). Isolation, characterization, and transduction of endometrial decidual tissue multipotent mesenchymal stromal/stem cells from menstrual blood. Biomed Res Int 2013:901821.
16. Zhong Z, AN Patel, TE Ichim, NH Riordan, H Wang, WP Min, EJ Woods, M Reid, E Mansilla, et al. (2009). Feasibility investigation of allogeneic endometrial regenerative cells. J Transl Med 7:15.
17. Nikoo S, M Ebtekar, M Jeddi-Tehrani, A Shervin, M Bozorgmehr, S Kazemnejad and AH Zarnani. (2012). Effect of menstrual blood-derived stromal stem cells on proliferative capacity of peripheral blood mononuclear cells in allogeneic mixed lymphocyte reaction. J Obstet Gynaecol Res 38:804-809.
18. Murphy MP, H Wang, AN Patel, S Kambhampati, N Angle, K Chan, AM Marleau, A Pyszniak, E Carrier, TE Ichim and NH Riordan. (2008). Allogeneic endometrial regenerative cells: An "Off the shelf solution" for critical limb ischemia? J Transl Med 6:45.
19. Hida N, N Nishiyama, S Miyoshi, S Kira, K Segawa, T Uyama, T Mori, K Miyado, Y Ikegami, et al. (2008). Novel cardiac precursor-like cells from human menstrual bloodderived mesenchymal cells. Stem Cells 26:1695-1704.
20. Borlongan CV, Y Kaneko, M Maki, SJ Yu, M Ali, JG Allickson, CD Sanberg, N Kuzmin-Nichols and PR Sanberg. (2010). Menstrual blood cells display stem cell-like phenotypic markers and exert neuroprotection following transplantation in experimental stroke. Stem Cells Dev 19:439-452.
21. Jiang Z, X Hu, H Yu, Y Xu, L Wang, H Chen, H Chen, R Wu, Z Zhang, et al. (2013). Human endometrial stem cells confer enhanced myocardial salvage and regeneration by paracrine mechanisms. J Cell Mol Med 17:1247-1260.
22. Xavier S, EM Efi, YZ Feng, W Erin and ST Hugh. (2011). Derivation of insulin producing cells from human endometrial stromal stem cells and use in the treatment of murine diabetes. Mol Ther 19:2065-2071.
23. Lumelsky N, O Blondel, P Laeng, I Velasco, R Ravin and R McKay. (2001). Differentiation of embryonic stem cells to insulin-secreting structures similar to pancreatic islets. Science 292:1389-1394.
24. Jiang W, Y Shi, DZ Zhao, S Chen, J Yong, J Zhang, TT Qing, X Sun, P Zhang, et al. (2007). In vitro derivation of functional insulin-producing cells from human embryonic stem cells. Cell Res 17:333-334.
25. Koga H, T Muneta, YJ Ju, T Nagase, A Nimura, T Mochizuki, S Ichinose, K von der Mark and I Sekiya. (2007). Synovial stem cells are regionally specified according to local microenvironments after implantation for cartilage regeneration. Stem Cells 25:689-696.
26. Wiebke S, JH Friedrich, B Marc, H Matthias, B Alexander, R Claudia, S Markus, L Thomas, N Andreas, et al. (2008). Tracking of human cells in mice. Histochem Cell Bio 130:329-338.
27. Gang EJ, D Bosnakovski, CA Figueiredo, JW Visser and RC Perlingeiro. (2007). SSEA-4 identifies mesenchymal stem cells from bone marrow. Blood 109:1743-1751.
28. Rosu-Myles M, J McCully, J Fair, J Mehic, P Menendez, R Rodriguez and C Westwood. (2013). The globoseries glycosphingolipid SSEA-4 is a marker of bone marrowderived clonal multipotent stromal cells in vitro and in vivo. Stem Cells Dev 22:1387-1397.
29. Huss R and S Moosmann. (2002). The co-expression of CD117 (c-kit) and osteocalcin in activated bone marrow stem cells in different diseases. Br J Haematol 118:305-312.
30. Romanov YA, AN Darevskaya, NV Meralikina and LB Buravkova. (2005). Mesenchymal stem cells from human bone marrow and adipose tissue: isolation, characterization, and differentiation potentialities. Bull Exp BiolMed 140:138-143.
31. Grajales L, J García, K Banach and DL Geenen. (2010). Delayed enrichment of mesenchymal cells promotes cardiac lineage and calcium transient development. J Mol Cell Cardiol 48:735-745.
32. Lu LL, YJ Liu, SG Yang, QJ Zhao, X Wang, W Gong, ZB Han, ZS Xu, YX Lu, et al. (2006). Isolation and characterization of human umbilical cord mesenchymal stem cells with hematopoiesis-supportive function and other potentials. Haematologica 91:1017-1026.
33. Bell GI, HC Broughton, KD Levac, DA Allan, A Xenocostas and DA Hess. (2012). Transplanted human bone marrow progenitor subtypes stimulate endogenous islet regeneration and revascularization. Stem cells Dev 21:97-109.
34. Koblas T, K Zacharovová, Z Berková, I Leontovic, E Dovolilová, L Zámecník and F Saudek. (2009). In vivo differentiation of human umbilical cord blood-derived cells into insulin-producing b cells. Folia Biol 55:224-232.
35. Lenzen S. (2008). The mechanisms of alloxan- and streptozotocin- induced diabetes. Diabetologia 51:216-226.
36. Szkudelski T. (2001). The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol Res 50:537-546.
37. Lenzen S. (2008). Oxidative stress: the vulnerable beta-cell. Biochem Soc Trans 36(Pt 3):343-347.
38. Cnop M, N Welsh, JC Jonas, A Jörns, S Lenzen and DL Eizirik. (2005). Mechanisms of pancreatic beta-cell death in type 1 and type 2 diabetes: many differences, few similarities. Diabetes 54(Suppl 2):S97-S107.
39. Lenzen S, J Drinkgern and M Tiedge. (1996). Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues. Free Radic Biol Med 20:463-466.
40. Halliwell B and M Whiteman. (2004). Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? Br J Pharmacol 142:231-255.
41. Chen MF, CT Lin, WC Chen, CT Yang, CC Chen, SK Liao, JM Liu, CH Lu and KD Lee. (2006). The sensitivity of human mesenchymal stem cells to ionizing radiation. Int J Radiat Oncol Biol Phys 66:244-253.
42. Valle-Prieto A and PA Conget. (2010). Human mesenchymal stem cells efficiently manage oxidative stress. Stem Cells Dev 19:1885-1893.
43. Cho KA, SY Woo, JY Seoh, HS Han and KH Ryu. (2012). Mesenchymal stem cells restore CCl4-induced liver injury byan antioxidative process. Cell Biol Int 36:1267-1274.
44. Hess D, L Li, M Martin, S Sakano, D Hill, B Strutt, S Thyssen, DA Gray and M Bhatia. (2003). Bone marrowderived stem cells initiate pancreatic regeneration. Nat Biotechnol 21:763-770.
45. Lin P, L Chen, N Yang, Y Sun and YX Xu. (2009). Evaluation of stem cell differentiation in diabetic rats transplanted with bone marrow mesenchymal stem cells. J Transplant Proc 41:1891-1893.
46. Kubo A, R Stull, M Takeuchi, K Bonham, V Gouon-Evans, M Sho, M Iwano, Y Saito, G Keller and R Snodgrass. (2011). Pdx1 and Ngn3 overexpression enhances pancreatic differentiation of mouse ES cell-derived endoderm population. PLoS One 6:e24058.
47. Gradwohl G, A Dierich, M LeMeur and F Guillemot. (2000). Neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proc Natl Acad Sci U S A 97:1607-1611.
48. Schwitzgebel VM, DW Scheel, JR Conners, J Kalamaras, JE Lee, DJ Anderson, L Sussel, JD Johnson and MS German. (2000). Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development 127:3533-3542.
49. Xu X, J D'Hoker, G Stangé, S Bonné, N De Leu, X Xiao, M Van de Casteele, G Mellitzer, Z Ling, et al. (2008). β cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell 132:197-207.
50. Li WC, JM Rukstalis, W Nishimura, V Tchipashvili, JF Habener, A Sharma and S Bonner-Weir. (2010). Activation of pancreatic-duct-derived progenitor cells during pancreas regeneration in adult rats. J Cell Sci 123:2793-2802.
51. Inada A, C Nienaber, H Katsuta, Y Fujitani, J Levine, R Morita, A Sharma and S Bonner-Weir. (2008). Carbonic anhydrase II-positive pancreatic cells are progenitors for both endocrine and exocrine pancreas after birth. Proc Natl Acad Sci U S A 105:19915-19919.
52. Gu G, J Dubauskaite and DA Melton. (2002). Direct evidence for the pancreatic lineage: NGN3 + cells are islet progenitors and are distinct from duct progenitors. Development 129:2447-2457.
53. Xu YX, L Chen, RWang, WK Hou, P Lin, L Sun, Y Sun and QYDong. (2008).Mesenchymal stemcell therapy for diabetes through paracrine mechanisms.Med Hypotheses 71:390-393.