Human urine-derived stem cells alone or genetically-modified with FGF2 improve type 2 diabetic erectile dysfunction in a rat model

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Ouyang, Bin ^a   Sun, Xiangzhou ^a   Han, Dayu ^a   Chen, Shenfu ^a   Yao, Bing ^a   Gao, Yong ^a   Bian, Jun ^b   Huang, Yanping ^c   Zhang, Yadong ^a   Wan, Zi ^a   Yang, Bin ^d,e   Xiao, Haipeng ^a   Songyang, Zhou ^a,f   Liu, Guihua ^a,e   Zhang, Yuanyuan ^e   Deng, Chunhua ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b SOUTHERN MEDICAL UNIVERSITY   (China)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^e WAKE FOREST SCHOOL OF MEDICINE   (United States)

^f BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; DESMIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FIBROBLAST GROWTH FACTOR 2; LENTIVIRUS VECTOR; SMOOTHELIN; VASCULOTROPIN; VON WILLEBRAND FACTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CORPUS CAVERNOSUM; ENDOTHELIUM CELL; ERECTILE DYSFUNCTION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIPID DIET; MALE; MEAN ARTERIAL PRESSURE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PENIS ERECTION; PROTEIN EXPRESSION; RAT; STEM CELL GENE THERAPY; STEM CELL TRANSPLANTATION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; THERAPY EFFECT; URINE DERIVED STEM CELL TRANSPLANTATION; VIRAL GENE DELIVERY SYSTEM; ANIMAL; BIOSYNTHESIS; DIABETES COMPLICATIONS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; GENETIC TRANSDUCTION; GENETICS; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT; STEM CELL; XENOGRAFT;

ADULT; ANIMALS; DIABETES COMPLICATIONS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; ERECTILE DYSFUNCTION; FIBROBLAST GROWTH FACTOR 2; HETEROGRAFTS; HUMANS; MALE; RATS; RATS, SPRAGUE-DAWLEY; STEM CELL TRANSPLANTATION; STEM CELLS; TRANSDUCTION, GENETIC;

EID: 84899680068     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092825     Document Type: Article

References (48)

1. Giugliano F, Maiorino M, Bellastella G, Gicchino M, Giugliano D, et al. (2010) Determinants of erectile dysfunction in type 2 diabetes. Int J Impot Res 22: 204-209.
2. Malavige LS, Levy JC (2009) Erectile dysfunction in diabetes mellitus. J Sex Med 6: 1232-1247.
3. Bacon CG, Hu FB, Giovannucci E, Glasser DB, Mittleman MA, et al. (2002) Association of type and duration of diabetes with erectile dysfunction in a large cohort of men. Diabetes Care 25: 1458-1463.
4. Kalter-Leibovici O, Wainstein J, Ziv A, Harman-Bohem I, Murad H, et al. (2005) Clinical, socioeconomic, and lifestyle parameters associated with erectile dysfunction among diabetic men. Diabetes Care 28: 1739-1744. (Pubitemid 40923086)
5. Penson DF, Latini DM, Lubeck DP, Wallace KL, Henning JM, et al. (2003) Do impotent men with diabetes have more severe erectile dysfunction and worse quality of life than the general population of impotent patients? Results from the Exploratory Comprehensive Evaluation of Erectile Dysfunction (ExCEED) database. Diabetes Care 26: 1093-1099. (Pubitemid 36929254)
6. Liu G, Sun X, Dai Y, Zheng F, Wang D, et al. (2010) Chronic administration of sildenafil modified the impaired VEGF system and improved the erectile function in rats with diabetic erectile dysfunction. J Sex Med 7: 3868-3878.
7. Rinaldi B, Donniacuo M, Sodano L, Gritti G, Signoriello S, et al. (2013) Effects of sildenafil on the gastrocnemius and cardiac muscles of rats in a model of prolonged moderate exercise training. PLoS One 8: e69954.
8. Shamloul R, Ghanem H (2013) Erectile dysfunction. Lancet 381: 153-165.
9. Lalu MM, McIntyre L, Pugliese C, Fergusson D, Winston BW, et al. (2012) Safety of cell therapy with mesenchymal stromal cells (SafeCell): a systematic review and meta-analysis of clinical trials. PLoS One 7: e47559.
10. Liu G, Sun X, Bian J, Wu R, Guan X, et al. (2013) Correction of diabetic erectile dysfunction with adipose derived stem cells modified with the vascular endothelial growth factor gene in a rodent diabetic model. PLoS One 8: e72790.
11. Qiu X, Lin H, Wang Y, Yu W, Chen Y, et al. (2011) Intracavernous transplantation of bone marrow-derived mesenchymal stem cells restores erectile function of streptozocin-induced diabetic rats. J Sex Med 8: 427-436.
12. Qiu X, Sun C, Yu W, Lin H, Sun Z, et al. (2011) Combined Strategy of Mesenchymal Stem Cells Injection with VEGF Gene Therapy for the Treatment of Diabetes Associated Erectile Dysfunction. J Androl.
13. Gou X, He WY, Xiao MZ, Qiu M, Wang M, et al. (2011) Transplantation of endothelial progenitor cells transfected with VEGF165 to restore erectile function in diabetic rats. Asian J Androl 13: 332-338.
14. Garcia MM, Fandel TM, Lin G, Shindel AW, Banie L, et al. (2010) Treatment of erectile dysfunction in the obese type 2 diabetic ZDF rat with adipose tissue-derived stem cells. J Sex Med 7: 89-98.
15. Bahk JY, Jung JH, Han H, Min SK, Lee YS (2010) Treatment of diabetic impotence with umbilical cord blood stem cell intracavernosal transplant: preliminary report of 7 cases. Exp Clin Transplant 8: 150-160.
16. Zhang Y, McNeill E, Tian H, Soker S, Andersson KE, et al. (2008) Urine derived cells are a potential source for urological tissue reconstruction. J Urol 180: 2226-2233.
17. Bharadwaj S, Liu G, Shi Y, Markert C, Andersson KE, et al. (2011) Characterization of urine-derived stem cells obtained from upper urinary tract for use in cell-based urological tissue engineering. Tissue Eng Part A 17: 2123-2132.
18. Bodin A, Bharadwaj S, Wu S, Gatenholm P, Atala A, et al. (2010) Tissue-engineered conduit using urine-derived stem cells seeded bacterial cellulose polymer in urinary reconstruction and diversion. Biomaterials 31: 8889-8901.
19. Wu S, Liu Y, Bharadwaj S, Atala A, Zhang Y (2011) Human urine-derived stem cells seeded in a modified 3D porous small intestinal submucosa scaffold for urethral tissue engineering. Biomaterials 32: 1317-1326.
20. Wu S, Wang Z, Bharadwaj S, Hodges SJ, Atala A, et al. (2011) Implantation of autologous urine derived stem cells expressing vascular endothelial growth factor for potential use in genitourinary reconstruction. J Urol 186: 640-647.
21. Vlodavsky I, Korner G, Ishai-Michaeli R, Bashkin P, Bar-Shavit R, et al. (1990) Extracellular matrix-resident growth factors and enzymes: possible involvement in tumor metastasis and angiogenesis. Cancer Metastasis Rev 9: 203-226. (Pubitemid 20380379)
22. Green PJ, Walsh FS, Doherty P (1996) Promiscuity of fibroblast growth factor receptors. Bioessays 18: 639-646. (Pubitemid 26312001)
23. Bahramsoltani M, De Spiegelaere W, Janczyk P, Hiebl B, Cornillie P, et al. (2010) Quantitation of angiogenesis in vitro induced by VEGF-A and FGF-2 in two different human endothelial cultures - an all-in-one assay. Clin Hemorheol Microcirc 46: 189-202.
24. Masaki I, Yonemitsu Y, Yamashita A, Sata S, Tanii M, et al. (2002) Angiogenic gene therapy for experimental critical limb ischemia: acceleration of limb loss by overexpression of vascular endothelial growth factor 165 but not of fibroblast growth factor-2. Circ Res 90: 966-973. (Pubitemid 34633862)
25. Cao R, Brakenhielm E, Pawliuk R, Wariaro D, Post MJ, et al. (2003) Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2. Nat Med 9: 604-613. (Pubitemid 36597108)
26. Asplin IR, Wu SM, Mathew S, Bhattacharjee G, Pizzo SV (2001) Differential regulation of the fibroblast growth factor (FGF) family by alpha(2)- macroglobulin: evidence for selective modulation of FGF-2-induced angiogenesis. Blood 97: 3450-3457.
27. Szebenyi G, Fallon JF (1999) Fibroblast growth factors as multifunctional signaling factors. Int Rev Cytol 185: 45-106. (Pubitemid 129751072)
28. Ning H, Liu G, Lin G, Yang R, Lue TF, et al. (2009) Fibroblast growth factor 2 promotes endothelial differentiation of adipose tissue-derived stem cells. J Sex Med 6: 967-979.
29. Li W, Liu C, Qin J, Zhang L, Chen R, et al. (2010) Efficient genetic modification of cynomolgus monkey embryonic stem cells with lentiviral vectors. Cell Transplant 19: 1181-1193.
30. Sun XZ, Liu GH, Wang ZQ, Zheng FF, Bian J, et al. (2011) Over-expression of VEGF165 in the adipose tissue-derived stem cells via the lentiviral vector. Chin Med J (Engl) 124: 3093-3097.
31. Oswald J, Boxberger S, Jorgensen B, Feldmann S, Ehninger G, et al. (2004) Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 22: 377-384. (Pubitemid 38736621)
32. Bharadwaj S, Liu G, Shi Y, Wu R, Yang B, et al. (2013) Multi-Potential Differentiation of Human Urine-Derived Stem Cells: Potential for Therapeutic Applications in Urology. Stem Cells.
33. Albersen M, Lin G, Fandel TM, Zhang H, Qiu X, et al. (2011) Functional, Metabolic, and Morphologic Characteristics of a Novel Rat Model of Type 2 Diabetes-associated Erectile Dysfunction. Urology.
34. Heaton JP, Varrin SJ, Morales A (1991) The characterization of a bio-assay of erectile function in a rat model. J Urol 145: 1099-1102.
35. Lin G, Qiu X, Fandel T, Banie L, Wang G, et al. (2011) Tracking intracavernously injected adipose-derived stem cells to bone marrow. Int J Impot Res.
36. Huang YP, Zhang YD, Gao Y, Yao FJ, Wang Y, et al. (2012) Abnormal endothelial function in ED patients with normal nocturnal penile tumescence and rigidity: is it the role of psychogenic factors? Int J Impot Res 24: 247-250.
37. Bivalacqua TJ, Deng W, Kendirci M, Usta MF, Robinson C, et al. (2007) Mesenchymal stem cells alone or ex vivo gene modified with endothelial nitric oxide synthase reverse age-associated erectile dysfunction. Am J Physiol Heart Circ Physiol 292: H1278-H1290. (Pubitemid 46377115)
38. Jesmin S, Sakuma I, Salah-Eldin A, Nonomura K, Hattori Y, et al. (2003) Diminished penile expression of vascular endothelial growth factor and its receptors at the insulin-resistant stage of a type II diabetic rat model: a possible cause for erectile dysfunction in diabetes. J Mol Endocrinol 31: 401-418. (Pubitemid 38054513)
39. Seghezzi G, Patel S, Ren CJ, Gualandris A, Pintucci G, et al. (1998) Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angiogenesis. J Cell Biol 141: 1659-1673. (Pubitemid 28309179)
40. Fujii T, Yonemitsu Y, Onimaru M, Inoue M, Hasegawa M, et al. (2008) VEGF function for upregulation of endogenous PlGF expression during FGF-2-mediated therapeutic angiogenesis. Atherosclerosis 200: 51-57.
41. Grunewald M, Avraham I, Dor Y, Bachar-Lustig E, Itin A, et al. (2006) VEG-Finduced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 124: 175-189. (Pubitemid 43069318)
42. Moreland RB (2000) Pathophysiology of erectile dysfunction: the contributions of trabecular structure to function and the role of functional antagonism. Int J Impot Res 12 Suppl 4: S39-S46.
43. Lin CS, Lin G, Lue TF (2012) Allogeneic and xenogeneic transplantation of adipose-derived stem cells in immunocompetent recipients without immunosuppressants. Stem Cells Dev 21: 2770-2778.
44. Liechty KW, MacKenzie TC, Shaaban AF, Radu A, Moseley AM, et al. (2000) Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med 6: 1282-1286.
45. Zhu XY, Zhang XZ, Xu L, Zhong XY, Ding Q, et al. (2009) Transplantation of adipose-derived stem cells overexpressing hHGF into cardiac tissue. Biochem Biophys Res Commun 379: 1084-1090.
46. Wu RP SMLG (2012) Immunomodulatory properties of urine derived stem cells. The 3rd Annual Regenerative Medicine Foundation Conference 2012 Abstract Book. Charlotte, NC, USA. Oct. 18-19.
47. Billinton N, Knight AW (2001) Seeing the wood through the trees: a review of techniques for distinguishing green fluorescent protein from endogenous autofluorescence. Anal Biochem 291: 175-197. (Pubitemid 32373153)
48. Liu G, Pareta RA, Wu R, Shi Y, Zhou X, et al. (2013) Skeletal myogenic differentiation of urine-derived stem cells and angiogenesis using microbeads loaded with growth factors. Biomaterials 34: 1311-1326.