Treatment with CB2 agonist JWH-133 reduces histological features associated with erectile dysfunction in hypercholesterolemic mice

Clinical and Developmental Immunology

Volumn 2013, Issue , 2013, Pages

  Fraga Silva, Rodrigo Araujo ^a   Costa Fraga, Fabiana Pereira ^a   Montecucco, Fabrizio ^b,c   Faye, Younouss ^a   Savergnini, Silvia Quintao ^a   Lenglet, Sébastien ^b   MacH, François ^b   Steffens, Sabine ^b   Stergiopulos, Nikolaos ^a   Souza Dos Santos, Robson Augusto ^d   Da Silva, Rafaela Fernandes ^d  

^a EPFL   (Switzerland)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^c UNIVERSITY OF GENOA   (Italy)

^d FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

1 DEOXY 3 (1,1 DIMETHYLBUTYL) DELTA8 TETRAHYDROCANNABINOL; APOLIPOPROTEIN E; CANNABINOID 2 RECEPTOR; COLLAGEN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FATTY ACID; HIGH DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NITRIC OXIDE; PHENYLEPHRINE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TRIACYLGLYCEROL; 1,1 DIMETHYLBUTYL 1 DEOXY DELTA(9) THC; 1,1-DIMETHYLBUTYL-1-DEOXY-DELTA(9)-THC; CANNABINOID; LIPID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; CORPUS CAVERNOSUM; ERECTILE DYSFUNCTION; HISTOLOGY; HYPERCHOLESTEROLEMIA; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PENILE FIBROSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE FIBER; ANIMAL; BLOOD; DISEASE MODEL; DRUG EFFECT; DRUG POTENTIATION; FIBROSIS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PENIS;

ANIMALS; CANNABINOIDS; DISEASE MODELS, ANIMAL; ERECTILE DYSFUNCTION; FIBROSIS; HYPERCHOLESTEROLEMIA; LIPIDS; MALE; MICE; MICE, KNOCKOUT; NADPH OXIDASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PENIS; REACTIVE OXYGEN SPECIES; RECEPTOR, CANNABINOID, CB2;

EID: 84888864938     PISSN: 17402522     EISSN: 17402530     Source Type: Journal    
DOI: 10.1155/2013/263846     Document Type: Article

References (56)

1. Dean R. C., Lue T. F., Physiology of penile erection and pathophysiology of erectile dysfunction. Urologic Clinics of North America 2005 32 4 379 395 2-s2.0-27744607670 10.1016/j.ucl.2005.08.007 (Pubitemid 41607527)
2. Fraga-Silva R. A., Montecucco F., Mach F., Santos R. A., Stergiopulos N., Pathophysiological role of the renin-angiotensin system on erectile dysfunction. European Journal of Clinical Investigation 2013 43 9 978 985
3. Shin D., Pregenzer G. Jr., Gardin J. M., Erectile dysfunction: a disease marker for cardiovascular disease. Cardiology in Review 2011 19 1 5 11 2-s2.0-78650798186 10.1097/CRD.0b013e3181fb7eb8
4. Bivalacqua T. J., Usta M. F., Champion H. C., Kadowitz P. J., Hellstrom W. J., Endothelial dysfunction in erectile dysfunction: role of the endothelium in erectile physiology and disease. Journal of Andrology 2003 24 6 S17 S37 2-s2.0-0242541094 (Pubitemid 37370524)
5. Musicki B., Liu T., Lagoda G. A., Strong T. D., Sezen S. F., Johnson J. M., Burnett A. L., Hypercholesterolemia-induced erectile dysfunction: endothelial Nitric Oxide Synthase (eNOS) uncoupling in the mouse penis by NAD(P)H oxidase. The Journal of Sexual Medicine 2010 7 9 3023 3032 2-s2.0-77956286084 10.1111/j.1743-6109.2010.01880.x
6. Kim J. H., Klyachkin M. L., Svendsen E., Davies M. G., Hagen P.-O., Carson C. C. III, Experimental hypercholesterolemia in rabbits induces cavernosal atherosclerosis with endothelial and smooth muscle cell dysfunction. The Journal of Urology 1994 151 1 198 205 2-s2.0-0027958541 (Pubitemid 24046973)
7. Xie D., Odronic S. I., Wu F., Pippen A. M., Donatucci C. F., Annex B. H., A mouse model of hypercholesterolemia-induced erectile dysfunction. The Journal of Sexual Medicine 2007 4 4, part 1 898 907 2-s2.0-34447548638 10.1111/j.1743-6109.2007.00518.x (Pubitemid 47079627)
8. Nehra A., Azadzoi K. M., Moreland R. B., Pabby A., Siroky M. B., Krane R. J., Goldstein I., Udelson D., Cavernosal expandability is an erectile tissue mechanical property which predicts trabecular histology in an animal model of vasculogenic erectile dysfunction. The Journal of Urology 1998 159 6 2229 2236 2-s2.0-0032426699 (Pubitemid 29190812)
9. Yeşilli Ç., Yaman Ö., Anafarta K., Effect of experimental hypercholesterolemia on cavernosal structures. Urology 2001 57 6 1184 1188 2-s2.0-0343807449 10.1016/S0090-4295(01)00974-8 (Pubitemid 32455604)
10. Kim S. C., Kim I. K., Seo K. K., Baek K. J., Lee M. Y., Involvement of superoxide radical in the impaired endothelium-dependent relaxation of cavernous smooth muscle in hypercholesterolemic rabbits. Urological Research 1997 25 5 341 346 2-s2.0-0041885877 10.1007/BF01294663 (Pubitemid 27461607)
11. Azadzoi K. M., Saenz de Tejada I., Hypercholesterolemia impairs endothelium-dependent relaxation of rabbit corpus cavernosum smooth muscle. The Journal of Urology 1991 146 1 238 240 2-s2.0-0025942457
12. Behr-Roussel D., Bernabe J., Compagnie S., Rupin A., Verbeuren T. J., Alexandre L., Giuliano F., Distinct mechanisms implicated in atherosclerosis-induced erectile dysfunction in rabbits. Atherosclerosis 2002 162 2 355 362 2-s2.0-0036238784 10.1016/S0021-9150(01)00740-7 (Pubitemid 34457941)
13. Kim S. C., Seo K. K., Kim H. W., Lee M. Y., The effects if isolated lipoproteins and triglyceride, combined oxidized low density lipoprotein (LDL) plus triglyceride, and combined oxidized LDL plus high density lipoprotein on the contractile and relaxation response of rabbit cavernous smooth muscle. International Journal of Andrology 2000 23 supplement 2 26 29 2-s2.0-0034042184 (Pubitemid 30330228)
14. Musicki B., Liu T., Strong T., Jin L., Laughlin M. H., Turk J. R., Burnett A. L., Low-fat diet and exercise preserve eNOS regulation and endothelial function in the penis of early atherosclerotic pigs: a molecular analysis. The Journal of Sexual Medicine 2008 5 3 552 561 (Pubitemid 351337881)
15. Klein T. W., Newton C., Larsen K., Lu L., Perkins I., Nong L., Friedman H., The cannabinoid system and immune modulation. Journal of Leukocyte Biology 2003 74 4 486 496 2-s2.0-0346350327 10.1189/jlb.0303101 (Pubitemid 38040375)
16. Klein T. W., Cannabinoid-based drugs as anti-inflammatory therapeutics. Nature Reviews Immunology 2005 5 5 400 411 2-s2.0-18844400058 10.1038/nri1602 (Pubitemid 40685989)
17. Mach F., Montecucco F., Steffens S., Cannabinoid receptors in acute and chronic complications of atherosclerosis. British Journal of Pharmacology 2008 153 2 290 298 2-s2.0-38349093269 10.1038/sj.bjp.0707517
18. Steffens S., Veillard N. R., Arnaud C., Pelli G., Burger F., Staub C., Zimmer A., Frossard J.-L., Mach F., Low dose oral cannabinoid therapy reduces progression of atherosclerosis in mice. Nature 2005 434 7034 782 786 2-s2.0-17144400758 10.1038/nature03389 (Pubitemid 44739523)
19. Engeli S., Central and peripheral cannabinoid receptors as therapeutic targets in the control of food intake and body weight. Handbook of Experimental Pharmacology 2012 209 357 381 2-s2.0-84856348064 10.1007/978-3-642-24716-3-17
20. Lagneux C., Lamontagne D., Involvement of cannabinoids in the cardioprotection induced by lipopolysaccharide. British Journal of Pharmacology 2001 132 4 793 796 2-s2.0-0035120753 (Pubitemid 32193634)
21. 2 receptor activation reduces mouse myocardial ischemia-reperfusion injury: involvement of cytokine/chemokines and PMN. Journal of Leukocyte Biology 2004 75 3 453 459 2-s2.0-1542283728 10.1189/jlb.0703303 (Pubitemid 38316376)
22. Jones R. T., Cardiovascular system effects of marijuana. Journal of Clinical Pharmacology 2002 42 11, supplement 58S 63S 2-s2.0-0036838392 (Pubitemid 35205047)
23. 2 cannabinoid receptor activation is cardioprotective in a mouse model of ischemia/reperfusion. Journal of Molecular and Cellular Cardiology 2009 46 5 612 620 2-s2.0-63349100859 10.1016/j.yjmcc.2008.12.014
24. 1 receptors. BJU International 2007 100 6 1385 1390 2-s2.0-35748985833 10.1111/j.1464-410X.2007.07180.x (Pubitemid 350043915)
25. Ghasemi M., Sadeghipour H., Mani A. R., Tavakoli S., Hajrasouliha A. R., Ebrahimi F., Dehpour A. R., Effect of anandamide on nonadrenergic noncholinergic-mediated relaxation of rat corpus cavernosum. European Journal of Pharmacology 2006 544 1-3 138 145 2-s2.0-33746598540 10.1016/j.ejphar.2006.06. 002 (Pubitemid 44148567)
26. Vural I. M., Ozturk G. S., Sarioglu Y., Functional characterization of nonadrenergic noncholinergic neurotransmitter release via endocannabinoids: an in vitro study in rabbit corpus cavernosum. The Journal of Sexual Medicine 2009 6 3 717 729 2-s2.0-61549106635 10.1111/j.1743-6109.2008.01003.x
27. Gratzke C., Christ G. J., Stief C. G., Andersson K.-E., Hedlund P., Localization and function of cannabinoid receptors in the corpus cavernosum: basis for modulation of nitric oxide synthase nerve activity. European Urology 2010 57 2 342 348 2-s2.0-72149121295 10.1016/j.eururo.2008.12.024
28. Montecucco F., Di Marzo V., da Silva R. F., Vuilleumier N., Capettini L., Lenglet S., Pagano S., Piscitelli F., Quintao S., Bertolotto M., Pelli G., Galan K., Pilet L., Kuzmanovic K., Burger F., Pane B., Spinella G., Braunersreuther V., Gayet-Ageron A., Pende A., Viviani G. L., Palombo D., Dallegri F., Roux-Lombard P., Santos R. A. S., Stergiopulos N., Steffens S., Mach F., The activation of the cannabinoid receptor type 2 reduces neutrophilic protease-mediated vulnerability in atherosclerotic plaques. European Heart Journal 2011 33 7 846 856 2-s2.0-84859496535 10.1093/eurheartj/ehr449
29. Fraga-Silva R. A., Costa-Fraga FP F. P., Savergnini S. Q., An oral formulation of Angiotensin-(1-7) reverses corpus cavernosum damages induced by hypercholesterolemia. The Journal of Sexual Medicine 2013 10 10 2430 2442
30. Baumhäkel M., Custodis F., Schlimmer N., Laufs U., Böhm M., Improvement of endothelial function of the corpus cavernosum in apolipoprotein E knockout mice treated with irbesartan. Journal of Pharmacology and Experimental Therapeutics 2008 327 3 692 698 2-s2.0-57549099686 10.1124/jpet.108.140533
31. Chung E., De Young L., Brock G. B., Investigative models in erectile dysfunction: a state-of-the-art review of current animal models. The Journal of Sexual Medicine 2011 8 12 3291 3305 2-s2.0-82955237496 10.1111/j.1743-6109.2011. 02505.x
32. Jin L., Lagoda G., Leite R., Webb R. C., Burnett A. L., NADPH oxidase activation: a mechanism of hypertension-associated erectile dysfunction. The Journal of Sexual Medicine 2008 5 3 544 551 2-s2.0-40349113071 10.1111/j.1743-6109.2007.00733.x (Pubitemid 351337880)
33. Olivon V. C., Fraga-Silva R. A., Segers D., Arginase inhibition prevents the low shear stress-induced development of vulnerable atherosclerotic plaques in ApoE-/- mice. Atherosclerosis 2013 227 2 236 243
34. Seo K. K., Yun H.-Y., Kim H., Kim S. C., Involvement of endothelial nitric oxide synthase in the impaired endothelium-dependent relaxation of cavernous smooth muscle in hypercholesterolemic rabbit. Journal of Andrology 1999 20 2 298 306 2-s2.0-0345621621 (Pubitemid 29203360)
35. Gonzalez-Cadavid N. F., Mechanisms of penile fibrosis. The Journal of Sexual Medicine 2009 6 supplement 3 353 362 2-s2.0-61849137692 10.1111/j.1743-6109.2008.01195.x
36. 2) immune regulation in health and disease. Immunologic Research 2011 51 1 26 38 2-s2.0-80053571291 10.1007/s12026-011-8210-5
37. 2 in the liver. Gastroenterology 2005 128 3 742 755 2-s2.0-15744388722 10.1053/j.gastro.2004.12.050 (Pubitemid 40585376)
38. 2 receptor activation and nitric oxide production. Molecular and Cellular Biochemistry 2006 283 1-2 75 83 2-s2.0-33645783755 10.1007/s11010-006-2346-y
39. 2 cannabinoid receptor agonists attenuate TNF- α -induced human vascular smooth muscle cell proliferation and migration. British Journal of Pharmacology 2008 153 2 347 357 2-s2.0-38349113185 10.1038/sj.bjp.0707569
40. 2-receptor stimulation attenuates TNF- α -induced human endothelial cell activation, transendothelial migration of monocytes, and monocyte-endothelial adhesion. The American Journal of Physiology-Heart and Circulatory Physiology 2007 293 4 H2210 H2218 2-s2.0-35348946336 10.1152/ajpheart.00688.2007 (Pubitemid 47605864)
41. 2 receptor in cirrhotic rats. Journal of Pharmacology and Experimental Therapeutics 2008 324 2 475 483 2-s2.0-38749134463 10.1124/jpet.107.131896 (Pubitemid 351185849)
42. Barutta F., Piscitelli F., Pinach S., Bruno G., Gambino R., Rastaldi M. P., Salvidio G., Di Marzo V., Perin P. C., Gruden G., Protective role of cannabinoid receptor type 2 in a mouse model of diabetic nephropathy. Diabetes 2011 60 9 2386 2396 2-s2.0-80052897170 10.2337/db10-1809
43. Johnson S. D., Phelps D. L., Cottler L. B., The association of sexual dysfunction and substance use among a community epidemiological sample. Archives of Sexual Behavior 2004 33 1 55 63 2-s2.0-2342641434 10.1023/B:ASEB.0000007462. 97961.5a (Pubitemid 38979568)
44. 2 form functional heteromers in brain. The Journal of Biological Chemistry 2012 287 25 20851 20865
45. 2 receptor. Current Topics in Medicinal Chemistry 2008 8 3 187 204 2-s2.0-40349101686 10.2174/ 156802608783498014 (Pubitemid 351795769)
46. 2 protects against balloon-induced neointima formation. The American Journal of Physiology-Heart and Circulatory Physiology 2012 302 5 H1064 H1074 2-s2.0-84857346670 10.1152/ajpheart.00444.2011
47. Tostes R. C., Carneiro F. S., Lee A. J., Giachini F. R. C., Leite R., Osawa Y., Webb R. C., Cigarette smoking and erectile dysfunction: focus on NO bioavailability and ROS generation. The Journal of Sexual Medicine 2008 5 6 1284 1295 2-s2.0-44949152565 10.1111/j.1743-6109.2008.00804.x (Pubitemid 351803095)
48. Schlimmer N., Kratz M., Böhm M., Baumhäkel M., Telmisartan, ramipril and their combination improve endothelial function in different tissues in a murine model of cholesterol-induced atherosclerosis. British Journal of Pharmacology 2011 163 4 804 814 2-s2.0-79958023299 10.1111/j.1476-5381.2011. 01267.x
49. Rajesh M., Bátkai S., Kechrid M., Mukhopadhyay P., Lee W.-S., Horváth B., Holovac E., Cinar R., Liaudet L., Mackie K., Haskó G., Pacher P., Cannabinoid 1 receptor promotes cardiac dysfunction, oxidative stress, inflammation, and fibrosis in diabetic cardiomyopathy. Diabetes 2012 61 3 716 727 2-s2.0-84857397033 10.2337/db11-0477
50. Montecucco F., Di Marzo V., At the heart of the matter: the endocannabinoid system in cardiovascular function and dysfunction. Trends in Pharmacological Sciences 2012 33 6 331 340
51. Horvth B., Mukhopadhyay P., Hask G., Pacher P., The endocannabinoid system and plant-derived cannabinoids in diabetes and diabetic complications. The American Journal of Pathology 2012 180 2 432 442 2-s2.0-84856010479 10.1016/j.ajpath.2011.11.003
52. El-Remessy A. B., Rajesh M., Mukhopadhyay P., Horváth B., Patel V., Al-Gayyar M. M. H., Pillai B. A., Pacher P., Cannabinoid 1 receptor activation contributes to vascular inflammation and cell death in a mouse model of diabetic retinopathy and a human retinal cell line. Diabetologia 2011 54 6 1567 1578 2-s2.0-80052547791 10.1007/s00125-011-2061-4
53. Fernández-Ruiz J., Moreno-Martet M., Rodríguez-Cueto C., Palomo-Garo C., Gõmez-Cañas M., Valdeolivas S., Guaza C., Romero J., Guzmán M., Mechoulam R., Ramos J. A., Prospects for cannabinoid therapies in basal ganglia disorders. British Journal of Pharmacology 2011 163 7 1365 1378 2-s2.0-79960317325 10.1111/j.1476-5381.2011.01365.x
54. Costa C., Virag R., The endothelial-erectile dysfunction connection: an essential update. The Journal of Sexual Medicine 2009 6 9 2390 2404 2-s2.0-69949108553 10.1111/j.1743-6109.2009.01356.x
55. Burnett A. L., Lowenstein C. J., Bredt D. S., Chang T. S., Snyder S. H., Nitric oxide: a physiologic mediator of penile erection. Science 1992 257 5068 401 403 2-s2.0-0026649942
56. Baumhäkel M., Schlimmer N., Büyükafşar K., Arikan O., Böhm M., Nebivolol, but not metoprolol, improves endothelial function of the corpus cavernosum in apolipoprotein E-knockout mice. The Journal of Pharmacology and Experimental Therapeutics 2008 325 3 818 823 2-s2.0-44349127305 10.1124/jpet.107.135681 (Pubitemid 351728031)