Autonomic neurotransmission: 60 years since sir Henry Dale.

In the early twentieth century, Sir Henry Dale and others described brilliant studies of autonomic neurotransmission utilizing acetylcholine and noradrenaline. However, within the past 60 years, new discoveries have changed our understanding of the organization of the autonomic nervous system, including the structure and function of the nonsynaptic autonomic neuroeffector junction, the multiplicity of neurotransmitters, cotransmission, neuromodulation, dual control of vascular tone by perivascular nerves and endothelial cells, the molecular biology of receptors, and trophic signaling. Further, it is now recognized that an outstanding feature of autonomic neurotransmission is the inherent plasticity afforded by its structural and neurochemical organization and the interaction between expression of neural mediators and environmental factors. In this way, autonomic neurotransmission is matched to ongoing changes in demands and can sometimes be compensatory in pathophysiological situations.

[1]  S. Duckles Influence of age on vascular adrenergic responsiveness. , 1987, Blood vessels.

[2]  G. Burnstock Morphological changes produced by drugs acting on the autonomic nervous system. , 1979, Pharmacology & therapeutics. Part B: General & systematic pharmacology.

[3]  G. Burnstock,et al.  Fine-structural Identification of Autonomic Nerves and their Relation to Smooth Muscle , 1971 .

[4]  G. Burnstock Chapter 1 – Introduction: Changing Face of Autonomic and Sensory Nerves in the Circulation , 1993 .

[5]  G. Burnstock Purine-mediated signalling in pain and visceral perception. , 2001, Trends in pharmacological sciences.

[6]  G. Burnstock The changing face of autonomic neurotransmission. , 1986, Acta physiologica Scandinavica.

[7]  G. Burnstock Purinergic Signalling in Lower Urinary Tract , 2001 .

[8]  G. Burnstock Noradrenaline and ATP: cotransmitters and neuromodulators. , 1995, Journal of physiology and pharmacology : an official journal of the Polish Physiological Society.

[9]  O. Appenzeller,et al.  The autonomic nervous system and hypoxia: mountain medicine. , 1996, Journal of the autonomic nervous system.

[10]  G. Burnstock,et al.  ATP as a co-transmitter in rat tail artery. , 1984, European journal of pharmacology.

[11]  G. Burnstock,et al.  Purine and pyrimidine receptors , 2007, Cellular and Molecular Life Sciences.

[12]  G Burnstock,et al.  Receptors for purines and pyrimidines. , 1998, Pharmacological reviews.

[13]  G. Burnstock Recent Concepts of Chemical Communication between Excitable Cells , 1983 .

[14]  G. Burnstock,et al.  A new method of destroying adrenergic nerves in adult animals using guanethidine , 1971, British journal of pharmacology.

[15]  G. Burnstock,et al.  Sympathetic and nonsympathetic neuropeptide Y-containing nerves in the rat myocardium and coronary arteries. , 1990, Circulation research.

[16]  G. Burnstock,et al.  Nitric Oxide in Health and Disease , 1997 .

[17]  E. Benarroch,et al.  Enteric nervous system , 2007, Neurology.

[18]  M. Bennett,et al.  P2X (purinergic) receptor distributions in rat blood vessels. , 1999, Journal of the autonomic nervous system.

[19]  G. Burnstock,et al.  Histochemical diagnosis of Hirschsprung's disease. , 1969, Lancet.

[20]  G. Burnstock,et al.  Cellular distribution and functions of P2 receptor subtypes in different systems. , 2004, International review of cytology.

[21]  G. Burnstock,et al.  New insights into the local regulation of blood flow by perivascular nerves and endothelium. , 1994, British journal of plastic surgery.

[22]  Eduardo E. Benarroch,et al.  Central Autonomic Control , 2004 .

[23]  G. Burnstock,et al.  The ultrastructure of Auerbach's plexus in the guinea-pig. II. Non-neuronal elements , 1976 .

[24]  G. Burnstock A basis for distinguishing two types of purinergic receptor , 1978 .

[25]  G. Burnstock Purinergic nerves. , 1972, Pharmacological reviews.

[26]  H. Takeda,et al.  The possible role of adenosine triphosphate in chemical transmission between the hypogastric nerve terminal and seminal vesicle in the guinea-pig. , 1973, Japanese journal of pharmacology.

[27]  G. Burnstock,et al.  Adrenergic Neurons: Their Organization, Function and Development in the Peripheral Nervous System , 1975 .

[28]  B. Folkow,et al.  Adaptive changes in “reactivity” and wall/lumen ratio in cat blood vessels exposed to prolonged transmural pressure difference , 1968 .

[29]  G. Burnstock Structural and Chemical Organization of the Autonomic Neuroeffector System , 2002 .

[30]  G. Burnstock,et al.  Purinergic signalling: pathophysiological roles. , 1998, Japanese journal of pharmacology.

[31]  A. J. Hobbs,et al.  l‐NG‐monomethyl arginine and l‐NG‐nitro arginine inhibit non‐adrenergic, non‐cholinergic relaxation of the mouse anococcygeus muscle , 1990, British journal of pharmacology.

[32]  G. Burnstock,et al.  Nitric oxide synthase immunoreactivity and NADPH-diaphorase activity in a subpopulation of intrinsic neurones of the guinea-pig heart , 1992, Neuroscience Letters.

[33]  G. Burnstock,et al.  Noradrenaline uptake by non‐innervated smooth muscle , 1971, British journal of pharmacology.

[34]  V. Hamburger,et al.  In vitro experiments on the effects of mouse sarcomas 180 and 37 on the spinal and sympathetic ganglia of the chick embryo. , 1954, Cancer research.

[35]  G. Burnstock,et al.  Substance P is released from the endothelium of normal and capsaicin-treated rat hind-limb vasculature, in vivo, by increased flow. , 1990, Circulation research.

[36]  Geoffrey Burnstock,et al.  Physiology and pathophysiology of purinergic neurotransmission. , 2007, Physiological reviews.

[37]  G. Burnstock Evolution of the autonomic innervation of visceral and cardiovascular systems in vertebrates. , 1969, Pharmacological reviews.

[38]  G. Burnstock,et al.  Ultrastructural localization of choline acetyltransferase in vascular endothelial cells in rat brain , 1985, Nature.

[39]  G. Burnstock The effects of acetylcholine on membrane potential, spike frequency, conduction velocity and excitability in the taenia coli of the guinea‐pig , 1958, The Journal of physiology.

[40]  G. Burnstock,et al.  Distribution and Colocalization of Nitric Oxide Synthase and Calretinin in Myenteric Neurons of Developing, Aging, and Crohn's Disease Human Small Intestine , 1999, Digestive Diseases and Sciences.

[41]  Naoki Yoshimura,et al.  Mechanisms underlying the recovery of lower urinary tract function following spinal cord injury. , 2006, Progress in brain research.

[42]  G. Burnstock,et al.  Dual Control by Nerves and Endothelial Cells of Arterial Blood Flow in Atherosclerosis , 1991 .

[43]  D. Chadwick,et al.  P2 purinoceptors : localization, function, and transduction mechanisms , 1996 .

[44]  G. Burnstock Autonomic neuroeffector junctions--reflex vasodilatation of the skin. , 1977, The Journal of investigative dermatology.

[45]  G. Burnstock,et al.  P2 receptor web: complexity and fine-tuning. , 2006, Pharmacology & therapeutics.

[46]  Geoffrey Burnstock,et al.  Do some nerve cells release more than one transmitter? , 1976, Neuroscience.

[47]  S. Z. Langer,et al.  Possible involvement of a transmitter different from norepinephrine in the residual responses to nerve stimulation of the cat nictitating membrane after pretreatment with reserpine. , 1976, The Journal of pharmacology and experimental therapeutics.

[48]  G. Burnstock,et al.  Properties of Intramural Neurones Cultured from the Heart and Bladder , 1987 .

[49]  G. Burnstock,et al.  CORRELATION OF FINE STRUCTURE AND PHYSIOLOGY OF THE INNERVATION OF SMOOTH MUSCLE IN THE GUINEA PIG VAS DEFERENS , 1963, The Journal of cell biology.

[50]  G. Burnstock,et al.  [3H]Adenosine Triphosphate: Release during Stimulation of Enteric Nerves , 1971, Science.

[51]  J. Gert van Dijk,et al.  AUTONOMIC FAILURE: A TEXTBOOK OF CLINICAL DISORDERS OF THE AUTONOMIC NERVOUS SYSTEM. , 2000 .

[52]  Marcello Costa,et al.  Identification of transmitters of functionally defined enteric neurons , 2011 .

[53]  G. Burnstock,et al.  The electrophysiologic and neurochemical properties of paratracheal neurones in situ and in dissociated cell culture. , 1987, The American review of respiratory disease.

[54]  D. Goldstein Autonomic Failure: A Textbook of Clinical Disorders of the Autonomic Nervous System , 1985 .

[55]  C. Hill,et al.  Development of neurons synthesizing noradrenaline and acetylcholine in the superior cervical ganglion of the rat in vivo and in vitro , 1977, Neuroscience.

[56]  E. Tansey Chemical neurotransmission in the autonomic nervous system: Sir Henry Dale and acetylcholine , 1991, Clinical Autonomic Research.

[57]  G. Burnstock Plasticity in expression of co-transmitters and autonomic nerves in aging and disease. , 1991, Advances in experimental medicine and biology.

[58]  Takao Shimizu,et al.  Lipid mediators in health and disease: enzymes and receptors as therapeutic targets for the regulation of immunity and inflammation. , 2009, Annual review of pharmacology and toxicology.

[59]  R. Bevan Effect of Sympathetic Denervation on Smooth Muscle Cell Proliferation in the Growing Rabbit Ear Artery , 1975, Circulation research.

[60]  A. Ciechanover,et al.  Targeting proteins for destruction by the ubiquitin system: implications for human pathobiology. , 2009, Annual review of pharmacology and toxicology.

[61]  Geoffrey Burnstock,et al.  Urinary bladder hyporeflexia and reduced pain-related behaviour in P2X 3-deficient mice , 2000, Nature.

[62]  G. Burnstock,et al.  Enhanced vasoconstrictor responses in renal and femoral arteries of the golden hamster during hibernation , 1998, The Journal of physiology.

[63]  J. Lundberg Pharmacology of cotransmission in the autonomic nervous system: integrative aspects on amines, neuropeptides, adenosine triphosphate, amino acids and nitric oxide. , 1996, Pharmacological reviews.

[64]  W. Groat,et al.  Mechanisms underlying the recovery of lower urinary tract function following spinal cord injury , 1995, Paraplegia.

[65]  R. Khurana Autonomic failure: A textbook of clinical disorders of the autonomic nervous system, 4th ed , 2000 .

[66]  C. Bell Dual Vasoconstrictor and Vasodilator Innervation of the Uterine Arterial Supply in the Guinea Pig , 1968, Circulation research.

[67]  P. Vanhoutte,et al.  Hypoxia releases a vasoconstrictor substance from the canine vascular endothelium. , 1985, The Journal of physiology.

[68]  G. Burnstock Review lecture. Neurotransmitters and trophic factors in the autonomic nervous system. , 1981, The Journal of physiology.

[69]  J. Taxi,et al.  Ultrastructural evidence for a functional unit between nerve fibers and type II cerebral mast cells in the cerebral vascular wall , 1987, Neuroscience.

[70]  E. Goetzl,et al.  Nerve–Mast Cell Interactions—Partnership in Health and Disease , 2003 .

[71]  G. Burnstock Purinergic Signaling and Vascular Cell Proliferation and Death , 2002, Arteriosclerosis, thrombosis, and vascular biology.

[72]  G. Burnstock,et al.  The transmission of excitation from autonomic nerve to smooth muscle , 1961, The Journal of physiology.

[73]  G. Burnstock,et al.  Vasoactive Intestinal Polypeptide-like Immunoreactive Nerves in Diabetic Penis: A Comparison Between Streptozotocin-treated Rats and Man , 1983, Diabetes.

[74]  J. Catravas,et al.  Subject Index, Vol. 44, 1992 , 1992 .

[75]  G. Dockray 20 – Peptidergic Neurotransmission , 2004 .

[76]  G. Burnstock,et al.  Ultrastructural localisation of substance P and choline acetyltransferase in endothelial cells of rat coronary artery and release of substance P and acetylcholine during hypoxia , 1989, Experientia.

[77]  G. Burnstock The action of adrenaline on excitability and membrane potential in the taenia coli of the guinea‐pig and the effect of DNP on this action and on the action of acetylcholine , 1958, The Journal of physiology.

[78]  F. Ingegnoli,et al.  [Raynaud's phenomenon]. , 2011, Reumatismo.

[79]  G Burnstock,et al.  Changes in expression of autonomic nerves in aging and disease. , 1990, Journal of the autonomic nervous system.

[80]  J. Wood Neuropathophysiology of functional gastrointestinal disorders. , 2007, World journal of gastroenterology.

[81]  G. Burnstock,et al.  Electron‐immunocytochemical studies of perivascular nerves of mesenteric and renal arteries of golden hamsters during and after arousal from hibernation , 1999, Journal of anatomy.

[82]  G. Burnstock,et al.  Interactions between autonomic nerves and smooth and cardiac muscle cells in tissue culture. , 1973, Developmental biology.

[83]  M. Abbracchio,et al.  Cardiovascular, respiratory, immune, metabolic, and gastrointestinal tract function , 2001 .

[84]  G. Burnstock Do some sympathetic neurones synthesize and release both noradrenaline and acetylcholine? , 1978, Progress in Neurobiology.

[85]  J A Peters,et al.  Guide to Receptors and Channels (GRAC), 3rd edition , 2008, British journal of pharmacology.

[86]  G. Burnstock,et al.  DEMONSTRATION OF "GAP JUNCTIONS" BETWEEN SMOOTH MUSCLE CELLS , 1970, The Journal of cell biology.

[87]  S. James,et al.  Nitric oxide in health and disease , 1998, Nature Medicine.

[88]  G. Burnstock Non-synaptic transmission at autonomic neuroeffector junctions , 2008, Neurochemistry International.

[89]  J. Mcleod,et al.  Autonomic neuropathy, II: Specific peripheral neuropathies , 1996, Journal of the Neurological Sciences.

[90]  S. Moncada Adventures in vascular biology: a tale of two mediators , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[91]  G. Burnstock,et al.  The ultrastructure of Auerbach's plexus in the guinea-pig. I. Neuronal elements , 1976, Journal of neurocytology.

[92]  G. Burnstock,et al.  Lack of release of vasoactive intestinal polypeptide and calcitonin gene-related peptide during electrical stimulation of enteric nerves in streptozotocin-diabetic rats. , 1987, Gastroenterology.

[93]  G. Burnstock,et al.  Development and ageing of perivascular adrenergic nerves in the rabbit. A quantitative fluorescence histochemical study using image analysis. , 1982, Journal of the autonomic nervous system.

[94]  G. Burnstock,et al.  Adrenergic innervation of the striated muscle of the intrinsic external urethral sphincter from patients with lower motor spinal cord lesion. , 1989, The Journal of urology.

[95]  T. Cowen,et al.  Plasticity in adult and ageing sympathetic neurons , 1998, Progress in Neurobiology.

[96]  Sadao Kimura,et al.  A novel potent vasoconstrictor peptide produced by vascular endothelial cells , 1988, Nature.

[97]  L. Bolis,et al.  Cell membrane receptors for drugs and hormones : a multidisciplinary approach , 1978 .

[98]  R. Stitzel,et al.  The postjunctional effects and neural release of purine compounds in the guinea-pig vas deferens. , 1978, European journal of pharmacology.

[99]  G. Burnstock,et al.  FINE STRUCTURE OF SMOOTH MUSCLE CELLS GROWN IN TISSUE CULTURE , 1971, The Journal of cell biology.

[100]  G. Burnstock Purinergic Signalling in Gut , 2001 .

[101]  G. Burnstock,et al.  The effects of hibernation on the myenteric plexus of the golden hamster small and large intestine , 1999, Cell and Tissue Research.

[102]  R. Furchgott,et al.  The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine , 1980, Nature.

[103]  G. Burnstock,et al.  Vascular control by purines with emphasis on the coronary system. , 1989, European heart journal.

[104]  R. Evans,et al.  Vasoconstriction of guinea‐pig submucosal arterioles following sympathetic nerve stimulation is mediated by the release of ATP , 1992, British journal of pharmacology.

[105]  T. Bonner,et al.  Definition of pharmacological receptors. , 1992, Pharmacological reviews.

[106]  G. Burnstock,et al.  A method for studying the effects of ions and drugs on the resting and action potentials in smooth muscle with external electrodes , 1958, The Journal of physiology.