Angiotensinergic neurotransmission in the peripheral autonomic nervous system

Frontiers in Bioscience

Volumn 17, Issue 7, 2011, Pages 2419-2432

  Bohlender, Jurgen ^a,b   Imboden, Hans ^b  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY OF BERN   (Switzerland)

Author keywords

Angiotensin; Angiotensinogen; Celiac ganglion; Dorsal root ganglion; Heart; Neuron; Neuropeptide; Neurotransmission; Renin; Review; Sympathetic nervous system

Indexed keywords

RATTUS;

EID: 84860283110     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/4062     Document Type: Article

References (110)

1. Llewellyn-Smith IJ: Anatomy of synaptic circuits controlling the activity of sympathetic preganglionic neurons. J Chem Neuroanat 38, 231-239 (2009)
2. Hokfelt T, C Broberger, ZQ Xu, V Sergeyev, R Ubink, M Diez: Neuropeptides-an overview. Neuropharmacology 39, 1337-1356 (2000)
3. Paul M, A Poyan Mehr, R Kreutz: Physiology of local renin-angiotensin systems. Physiol Rev 86, 747-803 (2006) (Pubitemid 44033382)
4. Johns EJ: Angiotensin II in the brain and the autonomic control of the kidney. Exp Physiol 90, 163-168 (2005) (Pubitemid 40364793)
5. Patil J, E Heiniger, T Schaffner, O Muhlemann, H Imboden: Angiotensinergic neurons in sympathetic coeliac ganglia innervating rat and human mesenteric resistance blood vessels. Regul Pept 147, 82-87 (2008)
6. Patil J, A Schwab, J Nussberger, T Schaffner, JM Saavedra, H Imboden: Intraneuronal angiotensinergic system in rat and human dorsal root ganglia. Regul Pept 162, 90-98 (2010)
7. Salio C, L Lossi, F Ferrini, A Merighi: Neuropeptides as synaptic transmitters. Cell Tissue Res 326, 583-598 (2006) (Pubitemid 44444794)
8. Gibbins IL, JL Morris: Structure of peripheral synapses: autonomic ganglia. Cell Tissue Res 326, 205-220 (2006) (Pubitemid 44435803)
9. Herring N, DJ Paterson: Neuromodulators of peripheral cardiac sympatho-vagal balance. Exp Physiol 94, 46-53 (2009)
10. Deutch AY, RH Roth: Neurotransmitters. In: Fundamental Neuroscience. Eds: MJ Zigmond, SC Landis, LR Squirrer, Academic Press, San Diego, Ca, 193-234 (1999)
11. Burnstock G: Cotransmission. Curr Opin Pharmacol 4, 47-52 (2004) (Pubitemid 38145837)
12. Burnstock G: Non-synaptic transmission at autonomic neuroeffector junctions. Neurochem Int 52, 14-25 (2008) (Pubitemid 350235685)
13. Halliday GM, YW Li, TH Joh, RG Cotton, PR Howe, LB Geffen, WW Blessing: Distribution of substance P-like immunoreactive neurons in the human medulla oblongata: co-localization with monoamine-synthesizing neurons. Synapse 2, 353-370 (1988)
14. Horvath TL, I Bechmann, F Naftolin , SP Kalra, C Leranth: Heterogeneity in the neuropeptide Y-containing neurons of the rat arcuate nucleus: GABAergic and non-GABAergic subpopulations. Brain Res 756, 283-286 (1997) (Pubitemid 27241638)
15. Herring N, DJ Paterson: Neuromodulators of peripheral cardiac sympatho-vagal balance. Exp Physiol 94, 46-53 (2009)
16. Ju G, T Hokfelt, E Brodin, J Fahrenkrug, JA Fischer, P Frey, RP Elde, JC Brown: Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, galanin-, vasoactive intestinal polypeptideand cholecystokinin-immunoreactive ganglion cells. Cell Tissue Res 247, 417-431 (1987) (Pubitemid 17006755)
17. Li JY, A Kling-Petersen, A Dahlstrom: Influence of spinal cord transection on the presence and axonal transport of CGRP-, chromogranin A-, VIP-, synapsin I-, and synaptophysin-like immunoreactivities in rat motor nerve. J Neurobiol 23, 1094-1110 (1992)
18. Gibbins IL, JB Furness, M Costa , I MacIntyre, CJ Hillyard, S Girgis: Co-localization of calcitonin generelated peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of guinea pigs. Neurosci Lett 57, 125-130 (1985) (Pubitemid 15058286)
19. Ekblad E, L Edvinsson, C Wahlestedt, R Uddman, R Hakanson, F Sundler: Neuropeptide Y co-exists and cooperates with noradrenaline in perivascular nerve fibers. Regul Pept 8, 225-235 (1984) (Pubitemid 14109276)
20. Lynch KR, MJ Peach: Molecular biology of angiotensinogen. Hypertension 17, 263-269 (1991)
21. L Wei , F Alhenc-Gelas, P Corvol, E Clauser: The two homologous domains of human angiotensin I-converting enzyme are both catalytically active. J Biol Chem 266, 9002-9008 (1991) (Pubitemid 21906610)
22. Doobay MF, LS Talman, TD Obr, X Tian, RL Davisson, E Lazartigues: Differential expression of neuronal ACE2 in transgenic mice with overexpression of the brain renin-angiotensin system. Am J Physiol 292, R373-381 (2007) (Pubitemid 46089851)
23. Genest J, M Cantin, R Garcia, G Thibault, J Gutkowska, E Schiffrin, O Kuchel, P Hamet: Extrarenal angiotensin-forming enzymes. Clin Exp Hypertens A 5, 1065-1080 (1983) (Pubitemid 13013694)
24. McKinley MJ, AL Albiston, AM Allen, ML Mathai, CN May, RM McAllen, BJ Oldfield, FA Mendelsohn, SY Chai: The brain renin-angiotensin system: location and physiological roles. Int J Biochem Cell Biol 35, 901-918 (2003) (Pubitemid 36379330)
25. Lind RW, LW Swanson, D Ganten: Organization of angiotensin II immunoreactive cells and fibers in the rat central nervous system. An immunohistochemical study. Neuroendocrinology 40, 2-24 (1985) (Pubitemid 15194786)
26. Imboden H, D Felix: An immunocytochemical comparison of the angiotensin and vasopressin hypothalamo-neurohypophysial systems in normotensive rats. Regul Pept 36, 197-218 (1991)
27. Imboden H, JW Harding, U Hilgenfeldt, MR Celio, D Felix: Localization of angiotensinogen in multiple cell types of rat brain. Brain Res 410, 74-77 (1987) (Pubitemid 17075183)
28. Thomas WG, C Sernia: Immunocytochemical localization of angiotensinogen in the rat brain. Neuroscience 25, 319-341 (1988)
29. Kumar A, A Rassoli, MK Raizada: Angiotensinogen gene expression in neuronal and glial cells in primary cultures of rat brain. J Neurosci Res 19, 287-90 (1988)
30. Thomas WG, KJ Greenland, TA Shinkel, C Sernia: Angiotensinogen is secreted by pure rat neuronal cell cultures. Brain Res 588, 191-200 (1992)
31. Fischer-Ferraro C, VE Nahmod, DJ Goldstein, S Finkielman: Angiotensin and renin in rat and dog brain. J Exp Med 133, 353-361 (1971)
32. Ganten D, A Marquez-Julio, P Granger, K Hayduk, K P Karsunky, R Boucher, J Genest: Renin in dog brain. Am J Physiol 221, 1733-1737 (1971)
33. Dzau VJ, J Ingelfinger, RE Pratt, KE Ellison: Identification of renin and angiotensinogen messenger RNA sequences in mouse and rat brains. Hypertension 8, 544-548 (1986) (Pubitemid 16037831)
34. Grobe JL, D Xu, CD Sigmund: An intracellular reninangiotensin system in neurons: fact, hypothesis, or fantasy. Physiology 23, 187-193 (2008)
35. Lynch KR, VI Simnad, ET Ben-Ari, JC Garrison: Localization of preangiotensinogen messenger RNA sequences in the rat brain. Hypertension 8, 540-543 (1986) (Pubitemid 16037830)
36. Yang G, TS Gray, CD Sigmund, MD Cassell: The angiotensinogen gene is expressed in both astrocytes and neurons in murine central nervous system. Brain Res 817, 123-131 (1999) (Pubitemid 29225353)
37. Allen AM, EL O'Callaghan, D Chen, JK Bassi: Central neural regulation of cardiovascular function by angiotensin: a focus on the rostral ventrolateral medulla. Neuroendocrinology 89, 361-369 (2009)
38. Lavoie JL, MD Cassell, KW Gross, CD Sigmund: Adjacent expression of renin and angiotensinogen in the rostral ventrolateral medulla using a dual-reporter transgenic model. Hypertension 43, 1116-1119 (2004) (Pubitemid 38579923)
39. Xu D, GR Borges, DR Davis, K Agassandian, ML Sequeira Lopez, RA Gomez, MD Cassell, JL Grobe, CD Sigmund: Neuron-or glial-specific ablation of secreted renin does not affect renal renin, baseline arterial pressure, or metabolism. Physiol Genomics 43, 286-294 (2011)
40. Lee-Kirsch MA, F Gaudet, MC Cardoso, K Lindpaintner: Distinct renin isoforms generated by tissuespecific transcription initiation and alternative splicing. Circ Res 84, 240-246 (1999) (Pubitemid 29070120)
41. Rogerson FM, I Schlawe, G Paxinos, SY Chai, MJ McKinley, FA Mendelsohn: Localization of angiotensin converting enzyme by in vitro autoradiography in the rabbit brain. J Chem Neuroanat 8, 227-243 (1995) (Pubitemid 124019968)
42. Barnes K, AJ Turner, AJ Kenny: Membrane localization of endopeptidase-24.11 and peptidyl dipeptidase A (angiotensin converting enzyme) in the pig brain: a study using subcellular fractionation and electron microscopic immunocytochemistry. J Neurochem 58, 2088-2096 (1992)
43. Wright JW, JW Harding: Important roles for angiotensin III and IV in the brain renin-angiotensin system. Brain Res Rev 25, 96-124 (1997) (Pubitemid 27459723)
44. Lawrence AC, LJ Clarke, DJ Campbell: Angiotensin peptides in brain and pituitary of rat and sheep. J Neuroendocrinol 4, 237-244 (1992)
45. Zini S, MC Fournie-Zaluski, E Chauvel, BP Roques, P Corvol, C Llorens-Cortes: Identification of metabolic pathways of brain angiotensin II and III using specific aminopeptidase inhibitors: predominant role of angiotensin III in the control of vasopressin release. Proc Natl Acad Sci U S A 93, 11968-11973 (1996) (Pubitemid 26347232)
46. Guo DF, I Chenier, V Tardif, SN Orlov, T Inagami: Type 1 angiotensin II receptor-associated protein ARAP1 binds and recycles the receptor to the plasma membrane. Biochem Biophys Res Commun 310, 1254-1265 (2003) (Pubitemid 37237670)
47. Robson DK, JW Ironside, WA Reid, PR Bogue: Immunolocalization of cathepsin D in the human central nervous system and central nervous system neoplasms. Neuropathol Appl Neurobiol 16, 39-44 (1990) (Pubitemid 20141684)
48. Savage MJ, M Iqbal, T Loh, SP Trusko, R Scott, R Siman: Cathepsin G: localization in human cerebral cortex and generation of amyloidogenic fragments from the betaamyloid precursor protein. Neuroscience 60, 607-619 (1994) (Pubitemid 24163910)
49. Lopes ES, M Sumitani, L Juliano, WT Beraldo, JL Pesquero: Distribution of tonin-and kallikrein-like activities in rat brain. Brain Res 769, 152-157 (1997) (Pubitemid 27455897)
50. Ferguson AV, DL Washburn, KJ Latchford: Hormonal and neurotransmitter roles for angiotensin in the regulation of central autonomic function. Exp Biol Med 226, 85-96 (2001)
51. Phillips MI, C Sumners: Angiotensin II in central nervous system physiology. Regul Pept 78, 1-11 (1998) (Pubitemid 28561511)
52. Bains JS, AV Ferguson: Paraventricular nucleus neurons projecting to the spinal cord receive excitatory input from the subfornical organ. Am J Physiol 268, R625-633 (1995)
53. Pickel VM, J Chan: Co-localization of angiotensin II and gamma-aminobutyric acid in axon terminals in the rat subfornical organ. Neurosci Lett 193, 89-92 (1995)
54. Maley BE: Immunohistochemical localization of neuropeptides and neurotransmitters in the nucleus solitarius. Chem Senses 21, 367-376 (1996) (Pubitemid 26183870)
55. Imboden H, J Patil, J Nussberger, F Nicoud, B Hess, N Ahmed, T Schaffner, M Wellner, D Muller, T Inagami, T Senbonmatsu, J Pavel, JM Saavedra: Endogenous angiotensinergic system in neurons of rat and human trigeminal ganglia. Regul Pept 154, 23-31 (2009)
56. Patil J, S Stucki, J Nussberger, T Schaffner, S Gygax, J Bohlender, H Imboden: Angiotensinergic and noradrenergic neurons in the rat and human heart. Regul Pept 167, 31-41 (2011)
57. Diz DI, CM Ferrario: Bidirectional transport of angiotensin II binding sites in the vagus nerve. Hypertension 11(2 Pt 2), I139-143 (1988)
58. Wang JM, D Slembrouck, WD Potter: Expression of angiotensinogen mRNA and localization of angiotensin II and renin in peripheral adrenergic neurons in primary culture. Biochem Biophys Res Commun 229, 876-681 (1996)
59. Imboden H, JW Harding, D Felix: Hypothalamic angiotensinergic fibre systems terminate in the neurohypophysis. Neurosci Lett 96, 42-46 (1989) (Pubitemid 19003447)
60. Frei N, J Weissenberger, AG Beck-Sickinger, M Höfliger, J Weis, H Imboden: Immunocytochemical localization of angiotensin II receptor subtypes and angiotensin II with monoclonal antibodies in the rat adrenal gland. Regul Pept 101, 149-155 (2001) (Pubitemid 32728381)
61. Maslyukov PM, MB Korzina, AI Emanuilov, VV Shilkin: Neurotransmitter composition of neurons in the cranial cervical and celiac sympathetic ganglia in postnatal ontogenesis. Neurosci Behav Physiol 40, 143-147 (2010)
62. Morales MA, K Holmberg, ZQ Xu, C Cozzari, BK Hartman, P Emson, M Goldstein, LG Elfvin, T Hokfelt: Localization of choline acetyltransferase in rat peripheral sympathetic neurons and its coexistence with nitric oxide synthase and neuropeptides. Proc Natl Acad Sci U S A 92, 11819-11823 (1995) (Pubitemid 26014202)
63. Romeo HE, T Fink, N Yanaihara, E Weihe: Distribution and relative proportions of neuropeptide Yand proenkephalin-containing noradrenergic neurones in rat superior cervical ganglion: Separate projections to submaxillary lymph nodes. Peptides 15, 1479-1487 (1994) (Pubitemid 124016342)
64. Chiu AT, WA Roscoe, DE McCall, PB Timmermans: Angiotensin II-1 receptors mediate both vasoconstrictor and hypertrophic responses in rat aortic smooth muscle cells. Receptor 1, 133-140 (1991)
65. Bergdahl A, T Nilsson, L Cantera, L Nilsson, XY Sun, T Hedner, D Erlinge, S Valdemarson, L Edvinsson: Neuropeptide Y potentiates noradrenaline-induced contraction through the neuropeptide Y Y1 receptor. Eur J Pharmacol 316, 59-64 (1996) (Pubitemid 26426930)
66. Kushiku K, H Yamada, K Shibata, R Tokunaga, T Katsuragi, T Furukawa: Upregulation of immunoreactive angiotensin II release and angiotensinogen mRNA expression by high-frequency preganglionic stimulation at the canine cardiac sympathetic ganglia. Circ Res 88, 110-116 (2001) (Pubitemid 32064091)
67. Stromberg C, K Tsutsumi, M Viswanathan, JM Saavedra: Angiotensin II AT1 receptors in rat superior cervical ganglia: characterization and stimulation of phosphoinositide hydrolysis. Eur J Pharmacol 208, 331-336 (1991)
68. Brasch H, L Sieroslawski, P Dominiak: Angiotensin II increases norepinephrine release from atria by acting on angiotensin subtype 1 receptors. Hypertension 22, 699-704 (1993) (Pubitemid 23326217)
69. Ma X, MW Chapleau, CA Whiteis, FM Abboud, K Bielefeldt: Angiotensin selectively activates a subpopulation of postganglionic sympathetic neurons in mice. Circ Res 27 88, 787-793 (2001) (Pubitemid 32429974)
70. Dendorfer A, A Thornagel, W Raasch, O Grisk, K Tempel, P Dominiak: Angiotensin II induces catecholamine release by direct ganglionic excitation. Hypertension 40, 348-334 (2002)
71. Byku M, H Macarthur, TC Westfall: Nerve stimulation induced overflow of neuropeptide Y and modulation by angiotensin II in spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 295, H2188-2197 (2008)
72. Schalekamp MA, AH Danser: Facilitated diffusion of angiotensin II from perivascular interstitium to AT1 receptors of the arteriole. A regulating step in vasoconstriction. J Hypertens 29, 906-914 (2011)
73. Gold MS, S Dastmalchi, JD Levine: Co-expression of nociceptor properties in dorsal root ganglion neurons from the adult rat in vitro. Neuroscience 71, 265-275 (1996) (Pubitemid 26041899)
74. Ju G, T Hokfelt, E Brodin, J Fahrenkrug, JA Fischer, P Frey, RP Elde, JC Brown: Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, galanin-, vasoactive intestinal polypeptideand cholecystokinin-immunoreactive ganglion cells. Cell Tissue Res 247, 417-431 (1987) (Pubitemid 17006755)
75. Gibbins IL, JB Furness, M Costa: Pathway-specific patterns of the co-existence of substance P, calcitonin generelated peptide, cholecystokinin and dynorphin in neurons of the dorsal root ganglia of the guinea-pig. Cell Tissue Res 248, 417-437 (1987) (Pubitemid 17042741)
76. Kopp UC, MZ Cicha, LA Smith: Angiotensin blocks substance P release from renal sensory nerves by inhibiting PGE2-mediated activation of cAMP. Am J Physiol Renal Physiol 285, F472-483 (2003) (Pubitemid 37010857)
77. Franco-Cereceda A, H Henke, JM Lundberg, JB Petermann, T Hokfelt, JA Fischer: Calcitonin gene-related peptide (CGRP) in capsaicin-sensitive substance Pimmunoreactive sensory neurons in animals and man: distribution and release by capsaicin. Peptides 8, 399-410 (1987) (Pubitemid 17065147)
78. Fujimori A, A Saito, S Kimura, T Watanabe, Y Uchiyama, H Kawasaki, K Goto: Neurogenic vasodilation and release of calcitonin gene-related peptide (CGRP) from perivascular nerves in the rat mesenteric artery. Biochem Biophys Res Commun 165, 1391-1398 (1989) (Pubitemid 20029864)
79. De Mey JG, R Megens, GE Fazzi: Functional antagonism between endogenous neuropeptide Y and calcitonin gene-related peptide in mesenteric resistance arteries. J Pharmacol Exp Ther 324, 930-937 (2008) (Pubitemid 351397826)
80. Kawasaki H, C Nuki, A Saito, K Takasaki: NPY modulates neurotransmission of CGRP-containing vasodilator nerves in rat mesenteric arteries. Am J Physiol 261, H683-690 (1991)
81. Kawasaki H, M Takenaga, H Araki, K Futagami, Y Gomita: Angiotensin inhibits neurotransmission of calcitonin gene-related peptide-containing vasodilator nerves in mesenteric artery of spontaneously hypertensive rats. J Pharmacol Exp Ther 284, 508-515 (1998) (Pubitemid 28086635)
82. Pavel J, H Tang, S Brimijoin, A Moughamian, T Nishioku, J Benicky, J M Saavedra: Expression and transport of Angiotensin II AT1 receptors in spinal cord, dorsal root ganglia and sciatic nerve of the rat. Brain Res 1246, 111-122 (2008)
83. Xu GY, LY Huang, ZQ Zhao: Activation of silent mechanoreceptive cat C and A sensory neurons and their substance P expression following peripheral inflammation. J Physiol 528, 339-348 (2000)
84. Oku R, M Satoh, N Fujii, A Otaka, H Yajima, H Takagi: Calcitonin gene-related peptide promotes mechanical nociception by potentiating release of substance P from the spinal dorsal horn in rats. Brain Res 403, 350-354 (1987) (Pubitemid 17019718)
85. Donoghue M, F Hsieh, E Baronas, K Godbout, M Gosselin, N Stagliano, M Donovan, B Woolf, K Robison, R Jeyaseelan, R E Breitbart, S Acton: A novel angiotensinconverting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1-9. Circ Res 87, E1-9 (2000)
86. Okamura T, DL Clemens, T Inagami: Renin, angiotensins, and angiotensin-converting enzyme in neuroblastoma cells: evidence for intracellular formation of angiotensins. Proc Natl Acad Sci U S A 78, 6940-6943 (1981) (Pubitemid 12216878)
87. Lam SY, PS Leung: A locally generated angiotensin system in rat carotid body. Regul Pept 107, 97-103 (2002) (Pubitemid 34876450)
88. Armour JA: Functional anatomy of intrathoracic neurons innervating the atria and ventricles. Heart Rhythm 7, 994-996 (2010)
89. Armour JA, DA Murphy, BX Yuan, S Macdonald, DA Hopkins: Gross and microscopic anatomy of the human intrinsic cardiac nervous system. Anat Rec 247, 289-298 (1997) (Pubitemid 27053904)
90. Crick SJ, RH Anderson, SY Ho, MN Sheppard: Localisation and quantitation of autonomic innervation in the porcine heart II: endocardium, myocardium and epicardium. J Anat 195, 359-363 (1999)
91. Marron K, J Wharton, MN Sheppard, D Fagan, D Royston, DM Kuhn, MR de Leval, BF Whitehead, RH Anderson, JM Polak: Distribution, morphology, and neurochemistry of endocardial and epicardial nerve terminal arborizations in the human heart. Circulation 92, 2343-2351 (1995)
92. Hoover DB, ER Isaacs, F Jacques, JL Hoard, P Page, JA Armour: Localization of multiple neurotransmitters in surgically derived specimens of human atrial ganglia. Neuroscience 164, 1170-1179 (2009)
93. Parsons RL, SA Locknar, BA Young, JL Hoard, DB Hoover: Presence and co-localization of vasoactive intestinal polypeptide with neuronal nitric oxide synthase in cells and nerve fibers within guinea pig intrinsic cardiac ganglia and cardiac tissue. Cell Tissue Res 323, 197-209 (2006) (Pubitemid 43100262)
94. Horackova M, JA Armour, Z Byczko: Distribution of intrinsic cardiac neurons in whole-mount guinea pig atria identified by multiple neurochemical coding. A confocal microscope study. Cell Tissue Res 297, 409-421 (1999) (Pubitemid 29410530)
95. Weihe E, B Schutz, W Hartschuh, M Anlauf, MK Schafer, LE Eiden: Coexpression of cholinergic and noradrenergic phenotypes in human and nonhuman autonomic nervous system. J Comp Neurol 492, 370-379 (2005) (Pubitemid 41547322)
96. Kapa S, KL Venkatachalam, SJ Asirvatham: The autonomic nervous system in cardiac electrophysiology: an elegant interaction and emerging concepts. Cardiol Rev 18, 275-284 (2010)
97. Hou XE, A Dahlstrom: Synaptic vesicle proteins and neuronal plasticity in adrenergic neurons. Neurochem Res 25, 1275-1300 (2000)
98. Morris JL, P Konig, T Shimizu, P Jobling, I L Gibbins: Most peptide-containing sensory neurons lack proteins for exocytotic release and vesicular transport of glutamate. J Comp Neurol 483, 1-16 (2005) (Pubitemid 40170683)
99. Dell'Italia LJ, QC Meng, E Balcells, CC Wei, R Palmer, GR Hageman, J Durand, G H. Hankes, S Oparil: Compartmentalization of angiotensin II generation in the dog heart. Evidence for independent mechanisms in intravascular and interstitial spaces. J Clin Invest 100, 253-258 (1997) (Pubitemid 27349070)
100. Maccarrone C, B Jarrott: Differential effects of surgical sympathectomy on rat heart concentrations of neuropeptide Y-immunoreactivity and noradrenaline. J Auton Nerv Syst 21, 101-107 (1987) (Pubitemid 18042271)
101. Sasaoka T, Y Egi, M Tawa, A Yamamoto, M Ohkita, M Takaoka, T Maruyama, T Akira, Y Matsumura: Angiotensin II type 2 receptor-mediated inhibition of norepinephrine release in isolated rat hearts. J Cardiovasc Pharmacol 52, 176-83 (2008)
102. Lambert C: Mechanisms of angiotensin II chronotropic effect in anaesthetized dogs. Br J Pharmacol 115, 795-800 (1995)
103. Von Lewinski D, J Kockskamper, SU Rubertus, D Zhu, JD Schmitto, FA Schondube, G Hasenfuss, B Pieske: Direct pro-arrhythmogenic effects of angiotensin II can be suppressed by AT1 receptor blockade in human atrial myocardium. Eur J Heart Fail 10, 1172-1176 (2008)
104. Kreusser MM, M Haass, SJ Buss, SE Hardt, SH Gerber, R Kinscherf, HA Katus, J Backs: Injection of nerve growth factor into stellate ganglia improves norepinephrine reuptake into failing hearts. Hypertension 47, 209-215 (2006) (Pubitemid 43189765)
105. Zhao Z, N Fefelova, M Shanmugam, P Bishara, GJ Babu, LH Xie: Angiotensin II induces afterdepolarizations via reactive oxygen species and calmodulin kinase II signaling. J Mol Cell Cardiol 50, 128-136 (2011)
106. ACTIVE I Investigators, S Yusuf, JS Healey, J Pogue, S Chrolavicius, M Flather, RG Hart, SH Hohnloser, CD Joyner, MA Pfeffer, SJ Connolly: Irbesartan in patients with atrial fibrillation. N Engl J Med 364, 928-938 (2011)
107. Li D, L Wang, C W Lee, TA Dawson, DJ Paterson: Noradrenergic cell specific gene transfer with neuronal nitric oxide synthase reduces cardiac sympathetic neurotransmission in hypertensive rats. Hypertension 50, 69-74 (2007) (Pubitemid 46986012)
108. Tissot AC, P Maurer, J Nussberger, R Sabat, T Pfister, S Ignatenko, HD Volk, H Stocker, P Muller, GT Jennings, F Wagner, MF Bachmann: Effect of immunisation against angiotensin II with CYT006-AngQb on ambulatory blood pressure: a double-blind, randomised, placebo-controlled phase IIa study. Lancet 371, 821-827 (2008) (Pubitemid 351323893)
109. Grassi G: Assessment of sympathetic cardiovascular drive in human hypertension: achievements and perspectives. Hypertension 54, 690-697 (2009)
110. Benemei S, P Nicoletti, JG Capone, P Geppetti: CGRP receptors in the control of pain and inflammation. Curr Opin Pharmacol 9, 9-14 (2009)