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Department of Pharmacology, Shiga University of Medical Science, Ohtsu, Japan (N.T., T.O.); and Department of Toyama Institute for Cardiovascular Pharmacology Research, Chuo-ku, Osaka, Japan (N.T.)
Unanticipated, novel hypothesis on nitric oxide (NO) radical, an inorganic, labile, gaseous molecule, as a neurotransmitter first appeared in late 1989 and into the early 1990s, and solid evidences supporting this idea have been accumulated during the last decade of the 20th century. The discovery of nitrergic innervation of vascular smooth muscle has led to a new understanding of the neurogenic control of vascular function. Physiological roles of the nitrergic nerve in vascular smooth muscle include the dominant vasodilator control of cerebral and ocular arteries, the reciprocal regulation with the adrenergic vasoconstrictor nerve in other arteries and veins, and in the initiation and maintenance of penile erection in association with smooth muscle relaxation of the corpus cavernosum. The discovery of autonomic efferent nerves in which NO plays key roles as a neurotransmitter in blood vessels, the physiological roles of this nerve in the control of smooth muscle tone of the artery, vein, and corpus cavernosum, and pharmacological and pathological implications of neurogenic NO have been reviewed. This nerve is a postganglionic parasympathetic nerve. Mechanical responses to stimulation of the nerve, mainly mediated by NO, clearly differ from those to cholinergic nerve stimulation. The naming "nitrergic or nitroxidergic" is therefore proposed to avoid confusion of the term "cholinergic nerve", from which acetylcholine is released as a major neurotransmitter. By establishing functional roles of nitrergic, cholinergic, adrenergic, and other autonomic efferent nerves in the regulation of vascular tone and the interactions of these nerves in vivo, especially in humans, progress in the understanding of cardiovascular dysfunctions and the development of pharmacotherapeutic strategies would be expected in the future.
Abstract I. Introduction II. Discovery of Nitrergic (Nitroxidergic) Nerve in Blood Vessels A. From Nonadrenergic Noncholinergic Nerve to Nitrergic Nerve B. Evidence for the Presence of Vasodilator Nerve-Releasing Nitric Oxide As a Neurotransmitter—Criteria for Transmitter C. Mechanism of Nitric Oxide Formation and Action 1. Formation of Nitrergic Neurotransmitter. a. L-Arginine. b. Ca2+ and Calmodulin. 2. Action of Nerve-Derived Nitric Oxide on Vascular Smooth Muscle. III. Nitrergic Innervation in Intra- and Extracranial Vasculature A. Cerebral Artery 1. In Vitro Studies in Various Mammals. 2. Nerve Stimulation by Electrical Pulses and by Nicotine and Related Compounds. 3. Is Protein Phosphorylation Involved in Neuronal Nitric-Oxide Synthase Activation? 4. In Vivo Studies. 5. Tracing the Origin of Nitrergic Nerve. 6. Hypercapnic and Hypoxic Cerebroarterial Dilation and Hypothermia. a. Hypercapnia. b. Hypoxia. c. Hypothermia. 7. Autoregulation. 8. Prejunctional Modulation of Nitrergic Nerve Function by Cholinergic and Adrenergic Neurotransmitters. 9. Histochemical Studies of Neurons Containing Nitric-Oxide Synthase. B. Ocular Vasculature 1. Retinal Artery and Arteriole. 2. Ciliary Artery. 3. Ophthalmic Artery. C. Lingual Artery D. Nasal Vasculature E. Temporal Vasculature IV. Nitrergic Innervation in Blood Vessels of Viscera A. Coronary Artery B. Pulmonary Vasculature C. Digestive Tract Vasculature D. Renal Vasculature E. Uterine Vasculature F. Penile Artery and Vein V. Nitrergic Innervation in Blood Vessels of Skin and Skeletal Muscle A. Cutaneous Small Artery B. Skeletal Muscle Vasculature VI. Interaction of Nitrergic, Cholinergic, and Adrenergic Nerves in Peripheral Vasculature VII. Nitrergic Innervation of Corpus Cavernosum and Penile Erection A. In Vitro Studies B. In Vivo Studies and Penile Erection C. Histochemical Studies of Neurons Containing Nitric-Oxide Synthase VIII. Blood Pressure Control by Neurogenic Nitric Oxide A. Involvement of Nitrergic Nerve Innervating Vasculature B. Effect of Centrally Applied Nitric Oxide Donors and Nitric-Oxide Synthase Inhibitors C. Nitric-Oxide Synthase Knockout Mice IX. Acupuncture, Axon Reflex, and Neurogenic Inflammation X. Pathological Implications of Neurogenic Nitric Oxide A. Cerebral Vasospasm after Subarachnoid Hemorrhage B. Migraine and Cluster Headache C. Impaired Ocular Circulation: Relation to Glaucoma D. Pre-Eclampsia (Pregnant Intoxication) E. Hypertension F. Erectile Dysfunction XI. Pharmacological Implications of Neurogenic Nitric Oxide A. Phosphodiesterase Type 5 Inhibitors B. Ginsenosides C. Free Radical Scavengers D. {alpha}2-Adrenoceptor Antagonists E. Antimuscarinic Agents F. Neuronal Nitric-Oxide Synthase Inhibitors G. Compounds That Suppress the Action of Endogenous Nitric-Oxide Synthase Inhibitors XII. A Possible Reason for Predominant Nitrergic Nerve Function in the Cerebral Artery and Corpus Cavernosum Compared with the Peripheral Vasculature XIII. A Proposal for a New Classification of Efferent Parasympathetic Innervation in Vascular and Nonvascular Smooth Muscle
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