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Current Pharmaceutical Design

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ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Review Article

Role of Histamine as a Peripheral Sympathetic Neuromediator and its Interrelation with Substance P

Author(s): Augusto S. Manzo Atencio*, Flor A. Perez de Manzo and Manuel Velasco

Volume 26, Issue 35, 2020

Page: [4486 - 4495] Pages: 10

DOI: 10.2174/1381612826666200813132951

Price: $65

Abstract

This article is an educational review about the fundamental aspects related to the proposal of the existence of a peripheral sympathetic reflex regulated by histamine, through its effect on presynaptic H3 type receptors, under the interaction of a sensory neuron that would be mediated by Substance P. In this respect, we consider it useful to highlight the role of histamine, so we discuss some aspects about its history, metabolism, and function, as well as its interaction with H3 type receptors that are considered as neuroreceptors, which define and typify it as a neuromediator at both levels of the nervous system, central and peripheral.

Keywords: Histamine, peripheral sympathetic reflex, substance P, capsaicin, vas deferens, nervous system.

[1]
Campos HA. Histamine and the sympathetic system of the rat vas deferens. In: Velasco M, Ed. Proceedings of the first Interamerican Congress of Clinical Pharmacology Therapy. International Congress Series 119-20
[2]
Campos HA. A possible crossed histamine-containing pathway adjacent to the sympathetic system of the rat vas deferens. J Pharmacol Exp Ther 1988; 244(3): 1121-7.
[PMID: 2472479]
[3]
Campos HA, Briceño E. Two models of peripheral sympathetic autoregulation: role of neuronal histamine. J Pharmacol Exp Ther 1992; 261(3): 943-50.
[PMID: 1602400]
[4]
Domínguez J, Sosa A, Campos HA. Hypertension in the rat induced by ᾳ-fluoromethylhistidine. Abstract of the 9th Scientific Meeting of International Society of Hypertension. Rio do Janeiro. Hypertension 1991; 17: 428.
[5]
Magaldi L, Israel A, Campos HA. Chronic inhibition of the enzyme histidine decarboxylase with alpha-fluoromethylhistidine: a new model of arterial hypertension. Arch Venez Farmacol Ter 1993; 12: 98-101. [In Spanish language]
[6]
Campos HA, Acuña Y, Magaldi L, Israel A. Alpha-fluoromethylhistidine, an inhibitor of histamine biosynthesis, causes arterial hypertension. Naunyn Schmiedebergs Arch Pharmacol 1996; 354(5): 627-32.
[http://dx.doi.org/10.1007/BF00170838] [PMID: 8938662]
[7]
Campos HA, Domínguez J. Interaction between noradrenergic and histamine-containing neurons in the rat vas deferens. J Pharmacol Exp Ther 1995; 272(2): 732-8.
[PMID: 7853187]
[8]
Cajal SR. Structure of the optic kiasma and general theory of the intersections of the nerve pathways Quarterly Micrographic Magazine 1898; ll
[9]
Campos HA, Montenegro M. Footshock-induced rise of rat blood histamine depends upon the activation of postganglionic sympathetic neurons. Eur J Pharmacol 1998; 347(2-3): 159-64.
[http://dx.doi.org/10.1016/S0014-2999(98)00097-1] [PMID: 9653876]
[10]
Acuña Y, Mathison Y, Campos HA, Israel A. Thioperamide, a histamine H3-receptor blocker, facilitates vasopressor response to footshocks. Inflamm Res 1998; 47(3): 109-14.
[http://dx.doi.org/10.1007/s000110050294] [PMID: 9580433]
[11]
Campos HA, Montenegro M, Velasco M, Romero E, Álvarez R, Urbina A. Treadmill exercise-induced stress causes a rise of blood histamine in normotensive but not in primary hypertensive humans. Eur J Pharmacol 1999; 383(1): 69-73.
[http://dx.doi.org/10.1016/S0014-2999(99)00598-1] [PMID: 10556683]
[12]
Alvarado SL, Campos HA, Navas T. Study of a peripheral reflex that compensates for sympathetic activity in diabetic patients with and without autonomic neuropathy through the use of a dynamometer. Internal Med (Caracas) 2008; 24: 42-57. [In the Spanish language]
[13]
Campos HA, Losada M, Bravo C. Role of neuronal histamine and capsaicin-sensitive neurons in modulating peripheral sympathetic activity and arterial pressure.Velasco M, Hernández R New advances in cardiovascular Physiology and Pharmacology Amsterdam 1998 Excerpta Medica. International Congress Series 1184 1998; pp 217-21.
[14]
Dale HH. Some chemical factors in the control of the circulation. Lancet 1929; 1: 1179-1183, 1233-1237, 1285-1290.
[15]
Hotta H. Neurogenic control of parenchymal arterioles in the cerebral cortexProg Brain Res 2016; 225: 3-39.
[http://dx.doi.org/10.1016/bs.pbr.2016.03.001] [PMID: 27130409]
[16]
Duncker DJ, Bache RJ. Regulation of coronary blood flow during exercise. Physiol Rev 2008; 88(3): 1009-86.
[http://dx.doi.org/10.1152/physrev.00045.2006] [PMID: 18626066]
[17]
Davison AN. Pyridoxal phosphate as coenzyme of diamine oxidase. Biochem J 1956; 64(3): 546-8.
[http://dx.doi.org/10.1042/bj0640546] [PMID: 13373807]
[18]
Moncada S, Roderic KJ, Vane F, Vane J. The Pharmacological Bases of the Therapeutics7th Edition - Reprint in Spanish Pan. American Medical Editorial Buenos Aires. 1987 Cap 28; 627-339..
[19]
Boerth RC, Ryan MJ, Brody MJ. Pharmacologic blockade of reflex vasodilatation: effects on postulated neurohumoral mechanisms. J Pharmacol Exp Ther 1970; 172(1): 52-61.
[PMID: 4190454]
[20]
Florey. The endothelial cell. BMJ 1966; 2(5512): 487-90.
[http://dx.doi.org/10.1136/bmj.2.5512.487] [PMID: 5913081]
[21]
Chester AH, Yacoub MH, Moncada S. Nitric oxide and pulmonary arterial hypertension. Glob Cardiol Sci Pract 2017; 2017(2): 14.
[http://dx.doi.org/10.21542/gcsp.2017.14] [PMID: 29644226]
[22]
Levin JA, Barlett JD, Beck I. Active reflex vasodilatation. Effect on postulated neurohumoral mechanisms. J Pharmacol Exp Ther 1968; 161: 262-70.
[PMID: 4967783]
[23]
Tobia AJ, Adams MD, Miya TS, Bousquet WF. Altered reflex vasodilatation in the hypertensive rat: possible role of histamine. J Pharmacol Exp Ther 1970; 175(3): 619-26.
[PMID: 4992408]
[24]
Burn JH, Rand MJ. Acethylcholine in adrenergic transmission. Annu Rev Pharmacol 1965; 5: 163-82.
[http://dx.doi.org/10.1146/annurev.pa.05.040165.001115] [PMID: 14290806]
[25]
Burn JH, Dale HH. The vaso-dilator action of histamine, and its physiological significance. J Physiol 1926; 61(2): 185-214.
[http://dx.doi.org/10.1113/jphysiol.1926.sp002283] [PMID: 16993782]
[26]
Campos HA. Peripheral neuronal histamine down regulates sympathetic activity and arterial pressure. In: Yanai Timmerman, Ed. Histamine Symposium in the New Millennium. 259-65.
[27]
Thurmond RL, Kazerouni K, Chaplan SR, Greenspan AJ. Peripheral Neuronal Mechanism of Itch: Histamine and ItchCarstens E, Akiyama T, editors Itch: Mechanisms and Treatment. Boca Raton (FL): CRC Press/Taylor Francis Chapter 10. Frontiers in Neuroscience 2014.
[28]
Haaksma EEJ, Leurs R, Timmerman H. Histamine receptors: subclasses and specific ligands. Pharmacol Ther 1990; 47(1): 73-104.
[http://dx.doi.org/10.1016/0163-7258(90)90046-5] [PMID: 2195558]
[29]
Beck L. Histamine as the potential mediator of active reflex dilatation. Fed Proc 1965; 24(6): 1298-310.
[PMID: 4379084]
[30]
Brody MJ, Dorr LD, Shaffer RA. Reflex vasodilatation and sympathetic transmission in the renal hypertensive dog. Am J Physiol 1970; 219(6): 1746-50.
[http://dx.doi.org/10.1152/ajplegacy.1970.219.6.1746] [PMID: 4320913]
[31]
Heitz DC, Brody MJ. Possible mechanism of histamine release during active vasodilatation. Am J Physiol 1975; 228(5): 1351-7.
[http://dx.doi.org/10.1152/ajplegacy.1975.228.5.1351] [PMID: 48345]
[32]
Crossland J. Chemical transmission in the central nervous system. J Pharm Pharmacol 1960; 12: 1-36.
[http://dx.doi.org/10.1111/j.2042-7158.1960.tb12627.x] [PMID: 13813022]
[33]
Arrang JM, Garbarg M, Lancelot JC, et al. Highly potent and selective ligands for histamine H3-receptors. Nature 1987; 327(6118): 117-23.
[http://dx.doi.org/10.1038/327117a0] [PMID: 3033516]
[34]
Arrang JM, Garbarg M, Schwartz JC. Autoinhibition of histamine synthesis mediated by presynaptic H3-receptors. Neuroscience 1987; 23(1): 149-57.
[http://dx.doi.org/10.1016/0306-4522(87)90279-X] [PMID: 2446202]
[35]
Timmerman H. Histamine H3 ligands: just pharmacological tools or potential therapeutic agents? J Med Chem 1990; 33(1): 4-11.
[http://dx.doi.org/10.1021/jm00163a001] [PMID: 1967317]
[36]
Boudier MMJ, Gerhart F. Effect of prolonged inhibition of histidine descarboxylase on tissue histamine concentration. Experiencia 1983; 39: 1303-5.
[http://dx.doi.org/10.1007/BF01990382]
[37]
Douglas WW. Histamine and 5-hydroxytryptamine (serotonin) and its antagonistsGoodman Gilman A, Goodman LS, Rall TW, Murad F Goodman Gilman The Pharmacological Bases of Therapeutics 7th Ed,. Panamerican Medical Ed. 1987; pp. 577-607.
[38]
Taylor KM, Snyder SH. Histamine in rat brain: sensitive assay of endogenous levels, formation in vivo and lowering by inhibitors of histidine decarboxylase. J Pharmacol Exp Ther 1971; 179(3): 619-33.
[PMID: 5138032]
[39]
Weinreich D. Synaptic responses mediated by identified histamine-containing neurones. Nature 1977; 267(5614): 854-6.
[http://dx.doi.org/10.1038/267854a0] [PMID: 19706]
[40]
Green JP. Histamine and serotoninBasic Neurochemistry. 4th ed. New York Raven Press 1989; p. 262.
[41]
Watanabe T, Taguchi Y, Shiosaka S, et al. Distribution of the histaminergic neuron system in the central nervous system of rats; a fluorescent immunohistochemical analysis with histidine decarboxylase as a marker. Brain Res 1984; 295(1): 13-25.
[http://dx.doi.org/10.1016/0006-8993(84)90811-4] [PMID: 6713171]
[42]
Häppölä O, Soinila S, Päivärinta H, Panula P, Eränkö O. Histamine-immunoreactive cells in the superior cervical ganglion and in the coeliac-superior mesenteric ganglion complex of the rat. Histochemistry 1985; 82(1): 1-3.
[http://dx.doi.org/10.1007/BF00502083] [PMID: 3980245]
[43]
Häppölä O, Soinila S, Päivärinta H, Joh TH, Panula P. Histamine-immunoreactive endocrine cells in the adrenal medulla of the rat. Brain Res 1985; 339(2): 393-6.
[http://dx.doi.org/10.1016/0006-8993(85)90113-1] [PMID: 3896403]
[44]
Päivärinta H, Häppölä O, Joh TH, Steinbusch H, Watanabe T, Panula P. Immunocytochemical colocalization of histamine, histidine decarboxylase, 5-hydroxytryptamine and tyrosine hydroxylase in the superior cervical ganglion of the rat. Histochem J 1987; 19(6-7): 319-26.
[http://dx.doi.org/10.1007/BF01680447] [PMID: 2889701]
[45]
Eränkö O. Small intensely fluorescent (SIF) cells and nervous transmission in sympathetic ganglia. Annu Rev Pharmacol Toxicol 1978; 18: 417-30.
[http://dx.doi.org/10.1146/annurev.pa.18.040178.002221] [PMID: 206195]
[46]
Panula P, Flügge G, Fuchs E, Pirvola U, Auvinen S, Airaksinen MS. Histamine-immunoreactive nerve fibers in the mammalian spinal cord. Brain Res 1989; 484(1-2): 234-9.
[http://dx.doi.org/10.1016/0006-8993(89)90366-1] [PMID: 2713684]
[47]
Takagi H, Morishima Y, Matsuyama T, Hayashi H, Watanabe T, Wada H. Histaminergic axons in the neostriatum and cerebral cortex of the rat: a correlated light and electron microscopic immunocytochemical study using histidine decarboxylase as a marker. Brain Res 1986; 364(1): 114-23.
[http://dx.doi.org/10.1016/0006-8993(86)90992-3] [PMID: 3004646]
[48]
Wouterlood FG, Sauren YM, Steinbusch HWM. Histaminergic neurons in the rat brain: correlative immunocytochemistry, Golgi impregnation, and electron microscopy. J Comp Neurol 1986; 252(2): 227-44.
[http://dx.doi.org/10.1002/cne.902520207] [PMID: 3023456]
[49]
Schwartz JC, Lampart C, Rose C. Properties and regional distribution of histidine decarboxylase in rat brain. J Neurochem 1970; 17(11): 1527-34.
[http://dx.doi.org/10.1111/j.1471-4159.1970.tb03722.x] [PMID: 5474655]
[50]
Berridge MJ, Irvine RF. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 1984; 312(5992): 315-21.
[http://dx.doi.org/10.1038/312315a0] [PMID: 6095092]
[51]
Hill SJ. Histamine receptors branch out. Nature 1987; 327(6118): 104-5.
[http://dx.doi.org/10.1038/327104a0] [PMID: 3033514]
[52]
Owen DAA. Histamine receptors in the cardiovascular. Gen Pharmacol 1977; 8(3): 141-56.
[http://dx.doi.org/10.1016/0306-3623(77)90043-X] [PMID: 340337]
[53]
Panula P, Chazot PL, Cowart M, et al. International union of basic and clinical pharmacology. Pharmacol Rev 2015; 67(3): 601-55.
[http://dx.doi.org/10.1124/pr.114.010249] [PMID: 26084539]
[54]
Bongers G, Bakker RA, Leurs R. Molecular aspects of the histamine H3 receptor. Biochem Pharmacol 2007; 73(8): 1195-204.
[http://dx.doi.org/10.1016/j.bcp.2007.01.008] [PMID: 17276412]
[55]
Nieto-Alamilla G, Márquez-Gómez R, García-Gálvez AM, Morales-Figueroa GE, Arias-Montaño JA. The histamine H3 receptor: structure, pharmacology and function. Mol Pharmacol 2016; 90(5): 649-73.
[http://dx.doi.org/10.1124/mol.116.104752] [PMID: 27563055]
[56]
Silver RB, Mackins CJ, Smith NC, et al. Coupling of histamine H3 receptors to neuronal Na+/H+ exchange: a novel protective mechanism in myocardial ischemia. Proc Natl Acad Sci USA 2001; 98(5): 2855-9.
[http://dx.doi.org/10.1073/pnas.051599198] [PMID: 11226330]
[57]
van Willigen G, Nieuwland R, Nürnberg B, Gorter G, Akkerman JW. Negative regulation of the platelet Na+/H+ exchanger by trimeric G-proteins. Eur J Biochem 2000; 267(24): 7102-8.
[http://dx.doi.org/10.1046/j.1432-1327.2000.01813.x] [PMID: 11106421]
[58]
Garbarg M, Barbin G, Rodergas E, Schwartz JC. Inhibition of histamine synthesis in brain by alpha-fluoromethylhistidine, a new irreversible inhibitor: in vitro and in vivo studies. J Neurochem 1980; 35(5): 1045-52.
[http://dx.doi.org/10.1111/j.1471-4159.1980.tb07858.x] [PMID: 7452304]
[59]
Lovenberg TW, Roland BL, Wilson SJ, et al. Cloning and functional expression of the human histamine H3 receptor. Mol Pharmacol 1999; 55(6): 1101-7.
[http://dx.doi.org/10.1124/mol.55.6.1101] [PMID: 10347254]
[60]
Yoshikawa T, Naganuma F, Iida T, et al. Molecular mechanism of histamine clearance by primary human astrocytes. Glia 2013; 61(6): 905-16.
[http://dx.doi.org/10.1002/glia.22484] [PMID: 23505051]
[61]
Ishikawa S, Sperelakis N. A novel class (H3) of histamine receptors on perivascular nerve terminals. Nature 1987; 327(6118): 158-60.
[http://dx.doi.org/10.1038/327158a0] [PMID: 3033517]
[62]
Parsons ME, Ganellin CR. Histamine and its receptors. Br J Pharmacol 2006; 147(Suppl. 1): S127-35.
[http://dx.doi.org/10.1038/sj.bjp.0706440] [PMID: 16402096]
[63]
Thurmond RL, Kazerouni K, Chalan SR, et al. Peripheral neuronal mechanism of ItchItch: Mechanisms and treatment. Boca Raton, Fl: CRC Press/Taylor & Francis 2014.
[http://dx.doi.org/10.1201/b16573-11]
[64]
Best CH, Dale HH, Dudley HW, Thorpe WV. The nature of the vaso-dilator constituents of certain tissue extracts. J Physiol 1927; 62(4): 397-417.
[http://dx.doi.org/10.1113/jphysiol.1927.sp002369] [PMID: 16993860]
[65]
Adams M, Hudgins PM. Characteristics of histamine disposition in vascular smooth muscle. Pharmacology 1976; 14: 330-8.
[http://dx.doi.org/10.1159/000136612]
[66]
El-Ackad TM, Brody MJ. Evidence for non-mast cell histamine in the vascular wall. Blood Vessels 1975; 12(3): 181-91.
[PMID: 1164563]
[67]
Von Euler US. Histamine as a specific constituent of certain autonomic fibers. Acta Physiol Scand 1949; 19: 85-93.
[68]
Von Euler US. Relationship between histamine and the autonomous nervous system. Handb Exp Pharmacol 1966; 18: 318-33.
[69]
Powell JR. Effects of histamine on vascular sympathetic neuroeffector transmission. J Pharmacol Exp Ther 1979; 208(3): 360-5.
[PMID: 219175]
[70]
Rexed B. von EULER US. The presence of histamine and noradrenalin in nerves as related to their content of myelinated and unmyelinated fibers. Acta Psychiatr Neurol Scand 1951; 26(1): 61-5.
[http://dx.doi.org/10.1111/j.1600-0447.1951.tb04632.x] [PMID: 14856806]
[71]
Kwiatkowski H. Histamine in nervous tissue. J Physiol 1943; 102(1): 32-41.
[http://dx.doi.org/10.1113/jphysiol.1943.sp004011] [PMID: 16991586]
[72]
Gross SS, Guo Z-G, Levi R, Bailey WH, Chenouda AA. Release of histamine by sympathetic nerve stimulation in the guinea pig heart and modulation of adrenergic responses. A physiological role for cardiac histamine? Circ Res 1984; 54(5): 516-26.
[http://dx.doi.org/10.1161/01.RES.54.5.516] [PMID: 6202436]
[73]
Grath M, Shepherd JT. Inhibition of adrenergic neurotransmission in canine vascular smooth muscle by histamine. Circ Res 1976; 39: 533-66.
[74]
Tuck ML. The sympathetic nervous system in essential hypertension. Am Heart J 1986; 112(4): 877-86.
[http://dx.doi.org/10.1016/0002-8703(86)90497-7] [PMID: 3532745]
[75]
Tyler HR, Dawson D. Hypertension and its relation to the nervous system. Ann Intern Med 1961; 55: 681-94. [Review]
[http://dx.doi.org/10.7326/0003-4819-55-4-681] [PMID: 13923357]
[76]
Uvnäs B. Sympathetic vasodilator outflow. Physiol Rev 1954; 34(3): 608-18.
[http://dx.doi.org/10.1152/physrev.1954.34.3.608] [PMID: 13185757]
[77]
Vanhoutte PM, Verbeuren TJ, Webb RC. Local modulation of adrenergic neuroeffector interaction in the blood vessel well. Physiol Rev 1981; 61(1): 151-247.
[http://dx.doi.org/10.1152/physrev.1981.61.1.151] [PMID: 6110212]
[78]
Lokhandwala MF. Inhibition of sympathetic nervous system by histamine:studies with H1- and H2-receptor antagonists. J Pharmacol Exp Ther 1978; 206(1): 115-22.
[PMID: 26798]
[79]
Ryan MJ, Brody MJ. Neurogenic and vascular stores of histamine in the dog. J Pharmacol Exp Ther 1972; 181(1): 83-91.
[PMID: 4335171]
[80]
Harvey SC. Studies on myocardial histamine. Effects of catecholamine-depleting drugs. Arch Int Pharmacodyn Ther 1978; 232(1): 141-9.
[PMID: 666455]
[81]
McNeill JH. Histamine and the heart. Can J Physiol Pharmacol 1984; 62(6): 720-6.
[http://dx.doi.org/10.1139/y84-119] [PMID: 6331617]
[82]
Knigge U, Matzen S, Warberg J. Histamine as a neuroendocrine regulator of the stress-induced release of peripheral catecholamines. Endocrinology 1990; 126(3): 1430-4.
[http://dx.doi.org/10.1210/endo-126-3-1430] [PMID: 1968380]
[83]
Khan H. Clinical Updates on Substance-P Antagonist in Pain Management. Biol Med (Aligarh) 2015; 7: 1.
[84]
Severini C, Improta G, Falconieri-Erspamer G, Salvadori S, Erspamer V. The tachykinin peptide family. Pharmacol Rev 2002; 54(2): 285-322.
[http://dx.doi.org/10.1124/pr.54.2.285] [PMID: 12037144]
[85]
Hökfelt T, Elfvin LG, Schultzberg M, Goldstein M, Nilsson G. On the occurrence of substance P-containing fibers in sympathetic ganglia: immunohistochemical evidence. Brain Res 1977; 132(1): 29-41.
[http://dx.doi.org/10.1016/0006-8993(77)90704-1] [PMID: 329951]
[86]
Gamse R, Wax A, Zigmond RE, Leeman SE. Immunoreactive substance P in sympathetic ganglia: distribution and sensitivity towards capsaicin. Neuroscience 1981; 6(3): 437-41.
[http://dx.doi.org/10.1016/0306-4522(81)90136-6] [PMID: 6164015]
[87]
Cuello AC, Priestley JV, Matthews MR. Localization of substance P in neuronal pathways. Ciba Found Symp 1982; 91(91): 55-83.
[http://dx.doi.org/10.1002/9780470720738.ch5] [PMID: 6183080]
[88]
Regoli D, Boudon A, Fauchére JL. Receptors and antagonists for substance P and related peptides. Pharmacol Rev 1994; 46(4): 551-99.
[PMID: 7534932]
[89]
Hörtnagl H, Singer EA, Lenz K, Kleinberger G, Lochs H. Substance P is markedly increased in plasma of patients with hepatic coma. Lancet 1984; 1(8375): 480-3.
[http://dx.doi.org/10.1016/S0140-6736(84)92851-4] [PMID: 6199630]
[90]
Oehme P, Hecht K, Piesche L, Hilse H, Rathsack R. Relation of substance P to stress and catecholamine metabolism. Ciba Found Symp 1982; 91(91): 296-306.
[http://dx.doi.org/10.1002/9780470720738.ch17] [PMID: 6183076]
[91]
Chen J, Gao J, Zhu G, et al. The role of substance P in regulation of blood pressure and hypertension Annalas N Y Acad os Sci 1991.632: 413-4..
[http://dx.doi.org/10.1111/j.1749-6632.1991.tb33140.x]
[92]
Agabiti-Rosei E, Alicandri C, Fariello R, Muiesan G. Catecholamines and haemodynamics in fixed essential hypertension. Clin Sci (Lond) 1979; 57(Suppl. 5): 193s-6s.
[http://dx.doi.org/10.1042/cs057193s] [PMID: 540429]
[93]
Mistrova E, Kruzliak P, Chottova Dvorakova M. Role of substance P in the cardiovascular system. Neuropeptides 2016; 58: 41-51.
[http://dx.doi.org/10.1016/j.npep.2015.12.005] [PMID: 26706184]
[94]
Fox LP, Merk HF, Bickers DR. Dermatological PharmacologyBrunton LL, Lazo JS, Parker KL Goodman Gilman The Pharmacological Bases of Therapeutics 11th. McGraw-Hill-Colombia 2007; 1703..
[95]
Moritoki H, Iwamoto T, Kanaya J, Ishida Y, Ando K, Kitagawa K. Capsaicin enhances the non-adrenergic twitch response of rat vas deferens. Br J Pharmacol 1987; 92(2): 469-75.
[http://dx.doi.org/10.1111/j.1476-5381.1987.tb11344.x] [PMID: 2445407]
[96]
Thurmond RL, Kazerouni K, Chaplan SR. Peripheral Neuronal Mechanism of Itch: Histamine and ItchCarstens E, Akiyama T, editors Itch: Mechanisms and Treatment. Boca Raton (FL): CRC Press/Taylor. Francis Frontiers in Neuroscience 2014..
[97]
Khalil Z, Livett BG, Marley PD. Sensory fibres modulate histamine-induced catecholamine secretion from the rat adrenal medulla and sympathetic nerves. J Physiol 1987; 391: 511-26.
[http://dx.doi.org/10.1113/jphysiol.1987.sp016753] [PMID: 3443956]
[98]
Melvin JE, McNeill TH, Hervonen A, Hamill RW. Organizational role of testosterone on the biochemical and morphological development of the hypogastric ganglion. Brain Res 1989; 485(1): 1-10.
[http://dx.doi.org/10.1016/0006-8993(89)90662-8] [PMID: 2566358]
[99]
Rogers H, Henderson G. Activation of mu- and delta-opioid receptors present on the same nerve terminals depresses transmitter release in the mouse hypogastric ganglion. Br J Pharmacol 1990; 101(3): 505-12.
[http://dx.doi.org/10.1111/j.1476-5381.1990.tb14112.x] [PMID: 1981687]
[100]
Keast J. Plasticity of Pelvic Autonomic Ganglia And Urogenital Innervation International Review of Citology Elsevier 2006; 248: 146.
[101]
Steers WD. Physiology of the vas deferens. World J Urol 1994; 12(5): 281-5.
[http://dx.doi.org/10.1007/BF00191208] [PMID: 7532517]
[102]
Ohkubo T, Shibata M. ATP-sensitive K+ channels mediate regulation of substance P release via the prejunctional histamine H3 receptor. Eur J Pharmacol 1995; 277(1): 45-9.
[http://dx.doi.org/10.1016/0014-2999(95)00057-R] [PMID: 7543412]
[103]
Hebel R, Stromberg WA. Anatomy and embryology of the laboratory rat. J Anat 1987; 153: 256.
[104]
Gabella G. Autonomic nervous systemPaxinos G (eds 1995; 81-103.
[105]
Berkley KJ. Autonomic nervous system and reproduction. 1999.
[106]
Hulsebosch CE, Coggeshall RE. An analysis of the axon populations in the nerves to the pelvic viscera in the rat. J Comp Neurol 1982; 211(1): 1-10.
[http://dx.doi.org/10.1002/cne.902110102] [PMID: 7174880]
[107]
Nadelhaft I, McKenna KE. Sexual dimorphism in sympathetic preganglionic neurons of the rat hypogastric nerve. J Comp Neurol 1987; 256(2): 308-15.
[http://dx.doi.org/10.1002/cne.902560210] [PMID: 3558884]
[108]
Steinman JL, Carlton SM, Willis WD. The segmental distribution of afferent fibers from the vaginal cervix and hypogastric nerve in rats. Brain Res 1992; 575(1): 25-31.
[http://dx.doi.org/10.1016/0006-8993(92)90418-9] [PMID: 1380393]
[109]
Harji F, Gonzales J, Galindo R, Dail WG. Preganglionic fibers in the rat hypogastric nerve project bilaterally to pelvic ganglia. Anat Rec 1998; 252(2): 229-34.
[http://dx.doi.org/10.1002/(SICI)1097-0185(199810)252:2<229:AID-AR8>3.0.CO;2-Y] [PMID: 9776077]
[110]
de Groat WC, Steers WD. Neural control of the urinary bladder and sexual organs Experimental studies in animals. Oxford Press 1988.
[111]
Steers WD, Mallory B, de Groat WC. Electrophysiological study of neural activity in penile nerve of the rat. Am J Physiol 1988; 254(6 Pt. 2): R989-R1000.
[PMID: 3381920]
[112]
Arellano J, Xelhuantzi N, Mirto N, Hernández ME, Cruz Y. Neural interrelationships of autonomic ganglia from the pelvic region of male rats. Auton Neurosci 2019; 217: 26-34.
[http://dx.doi.org/10.1016/j.autneu.2018.12.005] [PMID: 30704972]

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