1,605
Views
3
CrossRef citations to date
0
Altmetric
Original Article

Pathobiology of ischiocavernosus and bulbospongiosus muscles in long-term diabetic male rats and its implication on erectile dysfunction

ORCID Icon, , &
Pages 979-990 | Received 21 Jun 2019, Accepted 15 Jul 2019, Published online: 01 Aug 2019

References

  • Panach-Navarrete J, Martínez-Jabaloyas JM. The influence of comorbidities on the aging males' symptoms scale in patients with erectile dysfunction. Aging Male. 2017;20:146–152.
  • Salama MN, Eid AA, Hatem A, et al. Prevalence of erectile dysfunction in Egyptian males with metabolic syndrome. Aging Male. 2018;19:1–7.
  • Guay AT. Testosterone and erectile physiology. Aging Male. 2006;9:201–206.
  • Haider KS, Haider A, Doros G, et al. Long-term testosterone therapy improves urinary and sexual function, and quality of life in men with hypogonadism: results from a propensity matched subgroup of a controlled registry study. J Urol. 2018;199:257–265.
  • Saad F, Caliber M, Doros G, et al. Long-term treatment with testosterone undecanoate injections in men with hypogonadism alleviates erectile dysfunction and reduces risk of major adverse cardiovascular events, prostate cancer, and mortality. Aging Male. 2019;20:1–12.
  • Aykurt Karlıbel İ, Dülger S, Kasapoğlu Aksoy M, et al. Effect of cigarette smoking on sexual functions, psychological factors, and disease activity in male patients with ankylosing spondylitis. Aging Male. 2019;22:109–115.
  • Basat S, Sivritepe R, Ortaboz D, et al. The relationship between vitamin D level and erectile dysfunction in patients with type 2 diabetes mellitus. Aging Male. 2018;21:111–115.
  • Demirtaş Şahin T, Yazir Y, Utkan T, et al. TNF-α antagonism with etanercept enhances penile NOS expression, cavernosal reactivity, and testosterone levels in aged rats. Can J Physiol Pharmacol. 2018;96:200–207.
  • De Berardis G, Pellegrini F, Franciosi M, et al. Clinical and psychological predictors of incidence of self-reported erectile dysfunction in patients with type 2 diabetes. J Urol. 2007;177:252–257.
  • Corona G, Mannucci E, Petrone L, et al. Association of hypogonadism and type II diabetes in men attending an outpatient erectile dysfunction clinic. Int J Impot Res. 2006;18:190–197.
  • Maiorino MI, Bellastella G, Esposito K. Diabetes and sexual dysfunction: current perspectives. Diabetes Metab Syndr Obes. 2014;7:95–105.
  • Saenz de Tejada I, Goldstein I, Azadzoi K, et al. Impaired neurogenic and endothelium-mediated relaxation of penile smooth muscle from diabetic men with impotence. N Engl J Med. 1989;320:1025–1030.
  • Escrig A, Marin R, Abreu P, et al. Changes in mating behavior, erectile function and nitric oxide levels in penile corpora cavernosa in streptozotocin-diabetic rats. Biol Reprod. 2002;66:185–189.
  • Braunstein GD. Impotence in diabetic men. Mt Sinai J Med. 1987;54:236–240.
  • Dinulovic D, Radonjic G. Diabetes mellitus/male infertility (review). Arch Androl. 1990;25:277–293.
  • Scarano WR, Messias AG, Oliva SU, et al. Sexual behaviour sperm quality and quantity after short-term streptozotocin induced hyperglycemia in rats. Int J Androl. 2006;26:482–488.
  • Jesmin S, Sakuma I, Salah-eldin A, et al. 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 Mole Endo. 2003;31:401–418.
  • Saenz de Tejada I, Goldstein I. Diabetic penile neuropathy. Urol Clin North Am. 1988;15:17–22.
  • Cellek S, Foxwell NA, Moncada S. Two phases of nitrergic neuropathy in streptozotocin-induced diabetic rats. Diabetes. 2003;52:2353–2363.
  • Schmeichel AM, Schmelzer JD, Low PA. Oxidative injury and apoptosis of dorsal root ganglion neurons in chronic experimental diabetic neuropathy. Diabetes. 2003;52:165–171.
  • Zheng H, Bidasee KR, Mayhan WG, et al. Lack of central nitric oxide triggers erectile dysfunction in diabetes. Am J Physiol Regul Integr Comp Physiol. 2007;292:R1158–R1164.
  • Dorfman VB, Vega MC, Coirini H. Reduction of the spinal nucleus of the bulbocavernosous volume by experimental diabetes. Brain Res. 2004;1019:265–269.
  • Suresh S, Prakash S. Effect of Mucuna pruriens (Linn.) on oxidative stress‐induced structural alteration of corpus cavernosum in streptozotocin‐induced diabetic rat. J Sex Med. 2011;8:1943–1956.
  • Suresh S, Prakash S. Effect of Mucuna pruriens (Linn.) on sexual behavior and sperm parameters in streptozotocin‐induced diabetic male rat. J Sex Med. 2012;9:3066–3078.
  • Prakash S, Ibrahim M, Karthik Ganesh M, et al. Therapeutic potential of Mucuna pruriens (Linn.) on ageing induced damage in dorsal nerve of the penis and its implication on erectile function: an experimental study using albino rats. Aging Male. 2018;15:1–14. doi:10.1080/13685538.2018.1439005
  • Skandalakis JE, Colborn GL, Weidman TA, et al. Male genital system. In: Skandalakis JE, editor. Skandalakis’ surgical anatomy: the embryologic and anatomic basis of modern surgery. 1st ed. Athens, Greece: Paschalidis Medical Publications; 2004. p. 1381–1473.
  • Prakash S, Muhammed I. The penile baculum in monkey (Macaca radiata), rat (Rattus norvegicus), and bat (Pipistrellus mimus) and its functional significance—a mini review. J Basic Appl Zool. 2018;79:38.
  • Breza J, Aboseif SR, Orvis BR, et al. Detailed anatomy of penile neurovascular structures: surgical significance. J Urol. 1989;141:437–443.
  • Shafik A, Sibai OEL, Shafik AA, et al. Cavernosus muscle contraction during erection: is it voluntary or reflex, given the striated nature of the muscles? J Androl. 2006;27:695–699.
  • Andersson KE, Wagner G. Physiology of penile erection. Physiol Rev. 1995;75:191–236.
  • Sachs BD. Role of striated penile muscles in penile reflexes, copulation, and induction of pregnancy in the rat. J Reprod Fertil. 1982;66:433–443.
  • Lue TF, Tanagho EA. Hemodynamics of erection. In: Tanagho EA, Lue TF, McClure RD, editors. Contemporary management of impotence and infertility. 1st ed. Baltimore, MD: Williams & Wilkins; 1988. p. 28–38.
  • CPCSEA guidelines for laboratory animal facility. Indian J Pharmacol. 2003;35:257–274.
  • Suresh S, Prithiviraj E, Prakash S. Dose- and time-dependent effects of ethanolic extract of Mucuna pruriens Linn. seed on sexual behaviour of normal male rats. J Ethnopharmcol. 2009;22:497–501.
  • Holmes G, Chapple WD, Leipheimer RE, Sachs BD. Electromyographic analysis of male rat perineal muscles during copulation and reflexive erections. Physiol Behav. 1991;49:1235–1246.
  • Prakash S, Prithiviraj E, Suresh S. Development of seminiferous tubules in prenatal, postnatal and adult testis of bonnet monkey (Macaca radiata.). Anat Hist Emb. 2008;37:19–23.
  • Lowry OH, Rosebrough NJ, Farr AL, et al. Protein measurement with the Folin’s phenol reagent. J Biol Chem. 1951;193:265–276.
  • Zar JH. Biostatistical analysis. Engle Wood Cliffs, NJ: Prentice Hall Inc.; 1974.
  • Rowland DL, Greenleaf WJ, Dorfman LJ, et al. Aging and sexual function in men. Arch Sex Behav. 1993;22:545–557.
  • Bacon CG, Mittleman MA, Kawachi I, et al. Sexual function in men older than 50 years of age: results from the health professionals follow-up study. Ann Intern Med. 2003;139:161–168.
  • Dean R, Lue T. Physiology of penile erection and pathophysiology of erectile dysfunction. Urol Clin North Am. 2005;32:379–395.
  • Romanelli F, Sansone A, Lenzi A. Erectile dysfunction in aging male. Acta Biomed. 2010;81:89–94.
  • Traish AM1, Guay A, Feeley R, et al. The dark side of testosterone deficiency: I. Metabolic syndrome and erectile dysfunction. J Androl. 2008;30:10–22.
  • Sanchez E, Pastuszak AW, Khera M. Erectile dysfunction, metabolic syndrome, and cardiovascular risks: facts and controversies. Transl Androl Urol. 2017;6:28–36.
  • Murray FT, Orth J, Gunsalus G, et al. The pituitary – testicular axis in the streptozotocin diabetic male rat: evidence for gonadotroph, Sertoli cell and Leydig cell dysfunction. Int J Androl. 1981;4:265–280.
  • Davidson JM, Stefanick ML, Sachs BD, et al. Role of androgen in sexual reflexes of the male rat. Physiol Behav. 1978;21:141–146.
  • Baccetti B, La Marca A, Piomboni P, et al. Insulin-dependent diabetes in men is associated with hypothalamo-pituitary derangement and with impairment in semen quality. Hum Reprod. 2002;17:2673–2677.
  • Beatrice AM, Dutta D, Kumar M, et al. Testosterone levels and type 2 diabetes in men: current knowledge and clinical implications. Diabetes Metab Syndr Obes. 2014;7:481–486.
  • Griggs RC, Kingston W, Jozefowicz RF, et al. Effect of testosterone on muscle mass and muscle protein synthesis. J Appl Physiol. 1989;66:498–503.
  • Jiao Q, Pruznak AM, Huber D, et al. Castration differentially alters basal and leucine-stimulated tissue protein synthesis in skeletal muscle and adipose tissue. Am J Physiol Endocrinol Metab. 2009;297:E1222–E1232.
  • Biessels GJ, Van der Heide LP, Kamal A, et al. Ageing and diabetes: implications for brain function. Eur J Pharmacol. 2002;441:1–14.
  • Alp NJ, Mussa S, Khoo J, et al. Tetrahydrobiopterin-dependent preservation of nitric oxide-mediated endothelial function in diabetes by targeted transgenic GTP-cyclohydrolase I overexpression. J Clin Invest. 2003;112:725–735.
  • Crabtree MJ, Channon KM. Synthesis and recycling of tetrahydrobiopterin in endothelial function and vascular disease. Nitric Oxide. 2011;25:81–88.
  • Chen CA, Druhan LJ, Varadharaj S, et al. Phosphorylation of endothelial nitric-oxide synthase regulates superoxide generation from the enzyme. J Biol Chem. 2008;283:27038–27047.
  • Yeo TW, Lampah DA, Kenangalem E, et al. Impaired systemic tetrahydrobiopterin bioavailability and increased dihydrobiopterin in adult falciparum malaria: association with disease severity, impaired microvascular function and increased endothelial activation. PLoS Pathog. 2015;11:e1004667.
  • Bendall JK, Douglas G, McNeill E, et al. Tetrahydrobiopterin in cardiovascular health and disease. Antioxid Redox Signal. 2014;20:3040–3077.
  • Lee KH, Baek MY, Moon KY, et al. Nitric oxide as a messenger molecule for myoblast fusion. J Biol Chem. 1994;269:14371–14374.
  • Tidball JG, Wehling-Henricks M. Nitric oxide synthase deficiency and the pathophysiology of muscular dystrophy. J Physiol. 2014;592:4627–4638.
  • Gonzalez JP, Crassous PA, Schneider JS, et al. Neuronal nitric oxide synthase localizes to utrophin expressing intercalated discs and stabilizes their structural integrity. Neuromuscul Disord. 2015;25:964–976.
  • Dorfman VB, López-Costa JJ, Vega C, et al. Changes of NADPH-diaphorase reactivity in lumbar spinal cord of short-term streptozotocin induced diabetic rats. Brain Res. 2004;997:185–193.
  • Andreassen CS, Jakobsen J, Flyvbjerg A, et al. Expression of neurotrophic factors in diabetic muscle-relation to neuropathy and muscle strength. Brain. 2009;132:2724–2733.
  • Lavoisier P, Proulx J, Courtois F, et al. Relationship between perineal muscles contractions, penile tumescence and penile rigidity during nocturnal erections. J Urol. 1988;139:176–179.
  • Fournier GR, Juenemann KP, Lue TF, et al. Mechanisms of venous occlusion during canine penile erection: an anatomic demonstration. J Urol. 1987;137:163–167.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.