Combined strategy of mesenchymal stem cell injection with vascular endothelial growth factor gene therapy for the treatment of diabetes-associated erectile dysfunction

Journal of Andrology

Volumn 33, Issue 1, 2012, Pages 37-44

  Qiu, Xuefeng ^a   Sun, Chao ^a   Yu, Wen ^a   Lin, Haocheng ^a   Sun, Zhaorui ^a   Chen, Yun ^a   Wang, Run ^b   Dai, Yutian ^a  

^a NANJING UNIVERSITY   (China)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Cell transplantation; Diabetes mellitus; VEGF

Indexed keywords

PHOSPHATE BUFFERED SALINE; VASCULOTROPIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORPUS CAVERNOSUM; DISEASE ASSOCIATION; ELECTROSTIMULATION; ENDOTHELIUM; ENZYME LINKED IMMUNOSORBENT ASSAY; ERECTILE DYSFUNCTION; GENE THERAPY; HISTOPATHOLOGY; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MESENCHYMAL STEM CELL; NERVE STIMULATION; NONHUMAN; PENIS ERECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE; STREPTOZOCIN DIABETES;

ANIMALS; DIABETES COMPLICATIONS; ERECTILE DYSFUNCTION; GENE THERAPY; MALE; MESENCHYMAL STEM CELLS; RATS; RATS, SPRAGUE-DAWLEY; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84863083395     PISSN: 01963635     EISSN: 19394640     Source Type: Journal    
DOI: 10.2164/jandrol.110.012666     Document Type: Article

References (41)

1. Albersen M, Fandel TM, Lin G, Wang G, Banie L, Lin CS, Lue TF. Injections of adipose injections of adipose tissue-derived stem cells and stem cell lysate improve recovery of erectile function in a rat model of cavernous nerve injury. J Sex Med. 2010;7:3331-3340.
2. Bivalacqua TJ, Deng WW, Kendirci M, Usta MF, Robinson C, Taylor BK, Murthy SN, Champion HC, Hellstrom WJG, Kadowitz PJ. 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. 2007;292:H1278-H1290.
3. Bivalacqua TJ, Usta MF, Kendirci M, Pradhan L, Alvarez X, Champion HC, Kadowitz PJ, Hellstrom WJG. Superoxide anion production in the rat penis impairs erectile function in diabetes: influence of in vivo extracellular superoxide dismutase gene therapy. J Sex Med. 2005;2:187-197.
4. Burchardt T, Burchardt M, Karden J, Buttyan R, Shabsigh A, de la Taille A, Ng PY, Anastasiadis AG, Shabsigh R. Reduction of endothelial and smooth muscle density in the corpora cavernosa of the streptozotocin induced diabetic rat. J Urol. 2000;164 1807-1811.
5. Carmeliet P. VEGF gene therapy: stimulating angiogenesis or angioma-genesis? Nat Med. 2000;6:1102-1103.
6. Chitaley K. Type 1 and type 2 diabetic-erectile dysfunction: same diagnosis (ICD-9), different disease? J Sex Med. 2009;6:262-268.
7. Dai QS, Silverstein AD, Davies MG, Hagen PO, Donatucci CF, Annex BH. Systemic basic fibroblast growth factor induces favorable histological changes in the corpus cavernosum of hypercholesterolemic rabbits. J Urol. 2003;170:664-668.
8. De Young LX, Domes T, Lim K, Carson J, Brock GB. Endothelial rehabilitation: the impact of chronic PDE5 inhibitors on erectile function and protein alterations in cavernous tissue of diabetic rats. Eur Urol. 2008;54:213-220.
9. Fall PA, Izikki M, Tu L, Swieb S, Giuliano F, Bernabe J, Souktani R, Abbou C, Adnot S, Eddahibi S, Yiou R. Apoptosis and effects of intracavernous bone marrow cell injection in a rat model of postprostatectomy erectile dysfunction. Eur Urol. 2009;56:716-725.
10. Feldman HA, Goldstein I, Hatzichristou DG, Krane RJ, McKinlay JB. Impotence and its medical and psychosocial correlates: results of the Massachusetts Male Aging Study. J Urol. 1994;151:54-61.
11. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med. 2003;9:669-676.
12. Galmiche MC, Koteliansky VE, Briere J, Herve P, Charbord P. Stromal cells from human long-term marrow cultures are mesenchymal cells that differentiate following a vascular smooth muscle differentiation pathway. Blood. 1993;82:66-76.
13. Garcia MM, Fandel TM, Lin GT, Shindel AW, Banie L, Lin CS, Lue TF. Treatment of erectile dysfunction in the obese type 2 diabetic ZDF rat with adipose tissue-derived stem cells. J Sex Med. 2010;7:89-98.
14. Gerber HP, McMurtrey A, Kowalski J, Yan MH, Keyt BA, Dixit V, Ferrara N. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 39-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem. 1998;273:30336-30343.
15. Goldstein I, Lue TF, Padma-Nathan H, Rosen RC, Steers WD, Wicker PA, Sildenafil Study Group. Oral sildenafil in the treatment of erectile dysfunction. N Engl J Med. 1998;338:1397-1404.
16. Hidalgo-Tamola J, Chitaley K. Type 2 diabetes mellitus and erectile dysfunction. J Sex Med. 2009;6:916-926.
17. Huang YC, Ning HX, Shindel AW, Fandel TM, Lin GT, Harraz AM, Lue TF, Lin CS. The effect of intracavernous injection of adipose tissue-derived stem cells on hyperlipidemia-associated erectile dysfunction in a rat model. J Sex Med. 2010;7:1391-1400.
18. Iyer SS, Rojas M. Anti-inflammatory effects of mesenchymal stem cells: novel concept for future therapies. Expert Opin Biol Ther. 2008;8:569-581.
19. Jiang YH, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du JB, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature. 2002;418:41-49.
20. Jin HR, Kim WJ, Song JS, Choi MJ, Piao S, Shin SH, Tumurbaatar M, Tuvshintur B, Nam MS, Ryu JK, Suh JK. Functional and morphologic characterizations of the diabetic mouse corpus cavernosum: comparison of a multiple low-dose and a single high-dose streptozotocin protocols. J Sex Med. 2009;6:3289-3304.
21. Le Blanc K, Ringden O. Immunomodulation by mesenchymal stem cells and clinical experience. J Intern Med. 2007;262:509-525.
22. Lin CS, Ho HC, Chen KC, Lin G, Nunes L, Lue TF. Intracavernosal injection of vascular endothelial growth factor induces nitric oxide synthase isoforms. BJU Int. 2002;89:955-960.
23. Magnasco A, Corselli M, Bertelli R, Ibatici A, Peresi M, Gaggero G, Cappiello V, Chiavarina B, Mattioli G, Gusmano R, Ravetti JL, Frassoni F, Ghiggeri GM. Mesenchymal stem cells protective effect in adriamycin model of nephropathy. Cell Transplant. 2008; 17:1157-1167.
24. Malavige LS, Levy JC. Erectile dysfunction in diabetes mellitus. J Sex Med. 2009;6:1232-1247.
25. McCulloch DK, Campbell IW, Wu FC, Prescott RJ, Clarke BF. The prevalence of diabetic impotence. Diabetologia. 1980;18:279-283.
26. Mias C, Lairez O, Trouche E, Roncalli J, Calise D, Seguelas MH, Ordener C, Piercecchi-Marti MD, Auge N, Salvayre AN, Bourin P, Parini A, Cussac D. Mesenchymal stem cells promote matrix metalloproteinase secretion by cardiac fibroblasts and reduce cardiac ventricular fibrosis after myocardial infarction. Stem Cells. 2009;27:2734-2743.
27. Oswald J, Boxberger S, Jorgensen B, Feldmann S, Ehninger G, Bornhauser M, Werner C. Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells. 2004;22: 377-384.
28. Penson DF, Latini DM, Lubeck DP, Wallace KL, Henning JM, Lue TF. 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. 2003;26:1093-1099.
29. Pons J, Huang Y, Arakawa-Hoyt J, Washko D, Takagawa J, Ye JQ, Grossman W, Su H. VEGF improves survival of mesenchymal stem cells in infarcted hearts. Biochem Biophys Res Commun. 2008;376:419-422.
30. Qiu X, Lin H, Wang Y, Yu W, Chen Y, Wang R, Dai Y. Intracavernous transplantation of bone marrow-derived mesenchymal stem cells restores erectile function of streptozocin-induced diabetic rats. J Sex Med. 2011;8(2):427-436.
31. Rajfer J, Aronson WJ, Bush PA, Dorey FJ, Ignarro LJ. Nitric oxide as a mediator of relaxation of the corpus cavernosum in response to nonadrenergic, noncholinergic neurotransmission. N Engl J Med. 1992;326:90-94.
32. Rendell MS, Rajfer J, Wicker PA, Smith MD. Sildenafil for treatment of erectile dysfunction in men with diabetes: a randomized controlled trial. Sildenafil Diabetes Study Group. JAMA. 1999;281:421-426.
33. Ryu JK, Cho CH, Shin HY, Song SU, Oh SM, Lee M, Piao S, Han JY, Kim IH, Koh GY, Suh JK. Combined angiopoietin-1 and vascular endothelial growth factor gene transfer restores cavernous angiogenesis and erectile function in a rat model of hypercholesterolemia. Mol Ther. 2006;13:705-715.
34. Saigal CS, Wessells H, Pace J, Schonlau M, Wilt TJ; Urologic Diseases in America Project. Predictors and prevalence of erectile dysfunction in a racially diverse population. Arch Intern Med. 2006;166:207-212.
35. Segers VFM, Van Riet I, Andries LJ, Lemmens K, Demolder MJ, De Becker A, Kockx MM, De Keulenaer GW. Mesenchymal stem cell adhesion to cardiac microvascular endothelium: activators and mechanisms. Am J Physiol Heart Circ Physiol. 2006;290:H1370-H1377.
36. Tang YL, Zhao Q, Zhang YC, Cheng LL, Liu MY, Shi JH, Yang YZ, Pan CZ, Ge JB, Phillips MI. Autologous mesenchymal stem cell transplantation induce VEGF and neovascularization in ischemic myocardium. Regul Pept. 2004;117:3-10.
37. Wang YJ, Sun ZR, Qiu XF, Li Y, Qin JZ, Han XD. Roles of Wnt/beta-catenin signaling in epithelial differentiation of mesenchymal stem cells. Biochem Biophys Res Commun. 2009;390: 1309-1314.
38. Xie DH, Pippen AM, Odronic SI, Annex BH, Donatucci CF. Intracavernosal basic fibroblast growth factor improves vasoreactivity in the hypercholesterolemic rabbit. J Sex Med. 2006; 3:223-232.
39. Yaman O, Yilmaz E, Bozlu M, Anafarta K. Alterations of intracorporeal structures in patients with erectile dysfunction. Urol Int. 2003;71:87-90.
40. Yamanaka M, Shirai M, Shiina H, Tanaka Y, Enokida H, Tsujimura A, Matsumiya K, Okuyama A, Dahiya R. Vascular endothelial growth factor restores erectile function through inhibition of apoptosis in diabetic rat penile crura. J Urol. 2005;173:318-323.
41. Yang R, Yang B, Wen YT, Fang F, Cui SX, Lin GT, Sun ZY, Wang R, Dai YT. Losartan, an angiotensin type I receptor, restores erectile function by downregulation of cavernous renin-angiotensin system in streptozocin-induced diabetic rats. J Sex Med. 2009;6:696-707.