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Pathophysiology of Diabetic Erectile Dysfunction: Potential Contribution of Vasa Nervorum and Advanced Glycation Endproducts

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Pathophysiology of Diabetic Erectile Dysfunction: Potential Contribution of Vasa Nervorum and Advanced Glycation Endproducts International Journal of Impotence Research (2013) 25, 1–6 & 2013 Macmillan Publishers Limited All rights reserved 0955-9930/13 www.nature.com/ijir REVIEW Pathophysiology of diabetic erectile dysfunction: potential contribution of vasa nervorum and advanced glycation endproducts S Cellek1, NE Cameron2, MA Cotter2 and A Muneer3 Erectile dysfunction (ED) due to diabetes mellitus remains difficult to treat medically despite advances in pharmacotherapeutic approaches in the field. This unmet need has resulted in a recent re-focus on the pathophysiology, in order to understand the cellular and molecular mechanisms leading to ED in diabetes. Diabetes-induced ED is often resistant to PDE5 inhibitor treatment, thus there is a need to discover targets that may lead to novel approaches for a successful treatment. The aim of this brief review is to update the reader in some of the latest development on that front, with a particular focus on the role of impaired neuronal blood flow and the formation of advanced glycation endproducts. International Journal of Impotence Research (2013) 25, 1–6; doi:10.1038/ijir.2012.30; published online 23 August 2012 Keywords: advanced glycation endproducts; diabetes mellitus; erectile dysfunction; hypoxia; microvessel; nitric oxide; vasa nervorum INTRODUCTION disease and is likely to precede a coronary event by 5 years.8,9 Penile erection is the result of relaxation of smooth muscle in the Combined with the prevalence of obesity and metabolic syndrome cavernous body and associated blood vessels.1 Smooth muscle in these men, it is apparent that disease progression is likely to relaxation is mediated primarily by nitric oxide (NO), which is a reduce the efficacy of conventional pharmacotherapeutic options gaseous and labile mediator, yet one of the most potent for the treatment of ED in diabetic men. This has meant that endogenous smooth muscle relaxants. NO is synthesised by diabetic men form a large group of patients undergoing end-stage neuronal NO synthase (nNOS) in the autonomic postganglionic treatment in the form of penile prosthesis surgery. parasympathetic nerves (nitrergic nerves)2,3 and by endothelial Our knowledge regarding the pathophysiology of ED in nitric oxide synthase in the endothelium lining the blood vessels diabetes has gradually increased since the 1990s. As NO is the and cavernosal sinusoids. Nerve impulses in response to sexual main erectile mediator, the field has focussed on how diabetes stimulus are carried from the spinal cord to the hypogastric plexus alters the nitrergic and endothelial NO function. The aim of this where the cell bodies of the nitrergic nerves are located. Once paper is to update the reader with some of the latest development activated, the nitrergic neurones within the hypogastric plexus on that front, with a particular focus on the role of impaired transmit action potential through their axons to the penile neuronal blood flow, and the formation of advanced glycation end vasculature. These nitrergic axons then release high quantities of products. NO on to the nearby smooth muscle cells. NO diffuses rapidly into the smooth muscle cells, causing relaxation by increasing the intracellular concentrations of cGMP. The relaxation of the A NEED FOR TEMPORAL ANALYSIS cavernosal and arterial smooth muscle results in an increase in Thetoneofpenilevascularandcavernosal smooth muscle is blood flow into the penis. In turn, this causes shear stress on the regulated by vasodilators such as NO and vasoactive intestinal pep- endothelial lining, which promotes phosphorylation and tide, and by vasoconstrictors such as noradrenaline and endothelins. prolonged activation of endothelial nitric oxide synthase leading An imbalance in favour of the vasoconstrictors has been demon- to long-lasting release of NO from the endothelium to maintain the strated in both type 1 and 2 diabetes.9,10 Such an imbalance seems smooth muscle relaxation.4 As the intracavernosal pressure reaches to be caused by several factors, all playing equal roles, such as the level of the systemic arterial blood pressure, the subtunical decreased NO production from either nitrergic nerves or endothe- venules are compressed, which results in a rigid erection. lium,10 low responsiveness of the smooth muscle to vasodilators,1 Diabetes mellitus is one of the predominant risk factors of upregulation of the receptors for vasoconstrictor mediators such as erectile dysfunction (ED) and also one of the most difficult to endothelin11 and increased vasoconstrictor production and/or treat.5,6 Approximately 50% of diabetic men will suffer from ED release and hyper-responsiveness to vasoconstrictors.12 within 10 years of the diagnosis.7 ED presenting in these men is It is important to study the progression of ED in a temporal widely regarded as a manifestation of more systemic vascular fashion in order to gain a better understanding of the 1Department of Translational Medicine, Cranfield Health, Cranfield University, Bedfordshire, UK; 2School of Medical Sciences, University of Aberdeen, Aberdeen, UK and 3Institute of Urology, University College London, London, UK. Correspondence: Dr S Cellek, Department of Translational Medicine, Cranfield Health, Cranfield University, Bedfordshire, MK43 0AL, UK. E-mail: s.cellek@cranfield.ac.uk Received 8 May 2012; revised 2 July 2012; accepted 20 July 2012; published online 23 August 2012 Vasa nervorum and AGEs in diabetic ED S Cellek et al 2 pathophysiology of the condition. Although such longitudinal large ones such as the sciatic nerve to small ones such as the studies investigating the mechanisms at different time points cavernous nerve, have their own vasa nervorum. Earlier studies of the disease are few,13 they provide invaluable information into have shown that vasa nervorum of the peripheral nerve trunks can our understanding of diabetic ED. Similar longitudinal studies be divided into three groups: epineurial, perineurial and from other fields within or outside the diabetes field14 also have endoneurial.35 Epineurial and perineurial blood vessels form a been extremely useful in broadening our comprehension of complex network known as the epineurial plexus.35 The epineurial pathophysiological events. plexus has prominent arteriovenous shunts, supplies the endoneurial vascular compartment and is innervated by autonomic nerves such as sympathetic and peptidergic nerves.36 THE STORY BEGINS WITH HYPERGLYCAEMIA However, such detailed information is not available for the vasa At the early stages of diabetes, before the patient has symptoms of nervorum of the autonomic ganglia, although ganglia have a any complications such as ED and may not even be aware of the much greater metabolic demand than peripheral nerve trunk.35 underlying diagnosis and high blood glucose levels, there are two Whether the vasa nervorum of autonomic ganglia can be divided very important factors that trigger the cascade of events: high into sub-compartments like in the peripheral nerve trunk is not blood glucose and low insulin (low insulin concentration in Type 1 known. Moreover, details on the innervation of ganglion vasa diabetes and low insulin action due to receptor resistance in nervorum are sparse. We have recently shown that the rat major Type 2). The effect of high glucose on endothelial NO-dependent pelvic ganglia are surrounded by numerous small diameter blood vasodilation has been debated: using isolated human blood vessels, vessels (20-120 mm), which are innervated by noradrenergic and high glucose concentrations have been shown to have varying nitrergic nerve fibres.37 A drop in blood flow by as much as 50% is effects on endothelial NO-dependent relaxations depending on the observed in the autonomic ganglia as early as 1 week after type of the vascular bed.15,16 In humans, early reports have shown diabetes induction,32,33 although such an early decrease in blood that elevation of blood glucose concentrations does not affect the flow is not associated with ED initially. Thus drawing parallels with forearm blood flow.16,17 Later, it has been found that the reason for vasa nervorum in nerve trunks, it is likely that such a reduction in glucose-induced vasodilatation could be because of increased perfusion would cause ganglionic neurons to be exposed to a insulin levels as a direct response to glucose; insulin is known hypoxic environment. to elicit vasodilation directly.17 When such studies were repeated using agents like octreotide to inhibit insulin secretion, hence removing the influence of insulin on vasodilation, high glucose CONSEQUENCES OF HYPOXIA IN AUTONOMIC GANGLIA AND concentrations caused an acute and transient reduction in AXONS endothelium-dependent vasodilation.18–22 This has been attribu- Hypoxia can trigger several neuronal events both in the cell body ted to increased vasoconstrictor mediators22 and decreased and axon of the neuron: disturbances in membrane conductivity, endothelial NO production23 as a direct response to hyper- impaired nerve conduction and action potential generation, and glycaemia. Therefore we can deduce that acute and direct effect decreased axonal transport. It is therefore not surprising that of hyperglycaemia could be a transient reduction in blood flow in a nitrergic function in the isolated human corpus cavernosum healthy individual. In diabetic patients or individuals with impaired deteriorates in hypoxic conditions.38 However it should be noted glucose tolerance, the recovery from reduced vasodilation has been that the corpus cavernosum does not contain the neuronal cell
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