Neuropeptide coding of sympathetic preganglionic neurons; focus on adrenally projecting populations

Neuroscience

Volumn 170, Issue 3, 2010, Pages 789-799

  Kumar, N N ^a   Allen, K ^a   Parker, L ^a   Damanhuri, H ^a   Goodchild, A K ^a  

^a MACQUARIE UNIVERSITY   (Australia)

Author keywords

Adrenaline; Dorsal root ganglia; Enkephalin; Noradrenaline; PACAP

Indexed keywords

ADRENALIN; ENKEPHALIN; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; MESSENGER RNA; NEUROPEPTIDE; NORADRENALIN; PROENKEPHALIN;

ADRENAL MEDULLA; ADRENALIN RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL SUBPOPULATION; CHROMAFFIN CELL; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NERVE PROJECTION; NONHUMAN; NORADRENALIN RELEASE; NUCLEOTIDE SEQUENCE; PREGANGLIONIC NERVE CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RAT; SENSORY NERVE; SPINAL CORD; SPINAL GANGLION; SYMPATHETIC NERVE CELL;

ADRENAL MEDULLA; ANIMALS; AUTONOMIC FIBERS, PREGANGLIONIC; ENKEPHALINS; GANGLIA, SPINAL; MALE; NEUROPEPTIDES; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; PROTEIN PRECURSORS; RATS; RATS, SPRAGUE-DAWLEY; SENSORY RECEPTOR CELLS; SYMPATHETIC NERVOUS SYSTEM;

EID: 79958034496     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.07.047     Document Type: Article

References (75)

1. Anderson C.R. Identification of cardiovascular pathways in the sympathetic nervous system. Clin Exp Pharmacol Physiol 1998, 25:449-452.
2. Anderson C.R., McLachlan E.M., Srb-Christie O. Distribution of sympathetic preganglionic neurons and monoaminergic nerve terminals in the spinal cord of the rat. J Comp Neurol 1989, 283:269-284.
3. Arvidsson U., Riedl M., Elde R., Meister B. Vesicular acetylcholine transporter (VAChT) protein: a novel and unique marker for cholinergic neurons in the central and peripheral nervous systems. J Comp Neurol 1997, 378:454-467.
4. Bacon S.J., Smith A.D. Preganglionic sympathetic neurones innervating the rat adrenal medulla: immunocytochemical evidence of synaptic input from nerve terminals containing substance P, GABA or 5-hydroxytryptamine. J Auton Nerv Syst 1988, 24:97-122.
5. Beaudet M.M., Braas K.M., May V. Pituitary adenylate cyclase activating polypeptide (PACAP) expression in sympathetic preganglionic projection neurons to the superior cervical ganglion. J Neurobiol 1998, 36:325-336.
6. Brain S.D., Cox H.M. Neuropeptides and their receptors: innovative science providing novel therapeutic targets. Br J Pharmacol 2006, 147:S202-S211.
7. Cao W.H., Morrison S.F. Differential chemoreceptor reflex responses of adrenal preganglionic neurons. Am J Physiol Regul Integr Comp Physiol 2001, 281:R1825-R1832.
8. Chanthaphavong R.S., Murphy S.M., Anderson C.R. Chemical coding of sympathetic neurons controlling the tarsal muscle of the rat. Auton Neurosci 2003, 105:77-89.
9. Dàlsgaard C.J., Hökfelt T., Elfvin L.G., Terenius L. Enkephalin-containing sympathetic preganglionic neurons projecting to the inferior mesenteric ganglion: evidence from combined retrograde tracing and immunohistochemistry. Neuroscience 1982, 7:2039-2050.
10. Dun N.J., Miyazaki T., Tang H., Dun E.C. Pituitary adenylate cyclase activating polypeptide immunoreactivity in the rat spinal cord and medulla: implication of sensory and autonomic functions. Neuroscience 1996, 73:677-686.
11. Dun N.J., Tang H., Dun S.L., Huang R., Dun E.C., Wakade A.R. Pituitary adenylate cyclase activating polypeptide-immunoreactive sensory neurons innervate rat adrenal medulla. Brain Res 1996, 716:11-21.
12. Edwards S.L., Anderson C.R., Southwell B.R., McAllen R.M. Distinct preganglionic neurons innervate noradrenaline and adrenaline cells in the cat adrenal medulla. Neuroscience 1996, 70:825-832.
13. Farnham M.M.J., Li Q., Goodchild A.K., Pilowsky P.M. PACAP is expressed in sympathoexcitatory bulbospinal C1 neurons of the brain stem and increases sympathetic nerve activity in vivo. Am J Physiol Regul Integr Comp Physiol 2008, 294:1304-1311.
14. Gagner J.P., Gauthier S., Sourkes T.L. Descending spinal pathways mediating the responses of adrenal tyrosine hydroxylase and catecholamines to insulin and 2-deoxyglucose. Brain Res 1985, 325:187-197.
15. Gaspo R., Lamarche L., De Champlain J., Yamaguchi N. Canine adrenal catecholamine response to VIP is blocked by PACAP-(6-27) in vivo. Am J Physiol 1997, 272:R1606-R1612.
16. Ghzili H., Grumolato L., Thouënnon E., Tanguy Y., Turquier V., Vaudry H., Anouar Y. Role of PACAP in the physiology and pathology of the sympathoadrenal system. Front Neuroendocrinol 2008, 29:128-141.
17. Gibbins I.L. Vasoconstrictor, vasodilator and pilomotor pathways in sympathetic ganglia of guinea-pigs. Neuroscience 1992, 47:657-672.
18. Grkovic I., Anderson C.R. Calretinin-containing preganglionic nerve terminals in the rat superior cervical ganglion surround neurons projecting to the submandibular salivary gland. Brain Res 1995, 684:127-135.
19. Grkovic I., Anderson C.R. Calbindin D28K-immunoreactivity identifies distinct subpopulations of sympathetic pre- and postganglionic neurons in the rat. J Comp Neurol 1997, 386:245-259.
20. Hadjipavlou A., Simmons J.W., Yang J., Bi L., Simmons D., Necessary J. Torsional injury resulting in disc degeneration in the rabbit: II. Associative changes in dorsal root ganglion and spinal cord neurotransmitter production. J Spinal Disord 1998, 11:318-321.
21. Hamelink C., Tjurmina O., Damadzic R., Young W.S., Weihe E., Lee H.W., Eiden L.E. Pituitary adenylate cyclase-activating polypeptide is a sympathoadrenal neurotransmitter involved in catecholamine regulation and glucohomeostasis. Proc Natl Acad Sci U S A 2002, 99:461.
22. Hannibal J. Pituitary adenylate cyclase-activating peptide in the rat central nervous system: an immunohistochemical and in situ hybridization study. J Comp Neurol 2002, 453:389-417.
23. Harlan R.E., Shivers B.D., Romano G.J., Pfaff D.W., Howells R.D. Localization of preproenkephalin mRNA in the rat brain and spinal cord by in situ hybridization. J Comp Neurol 1987, 258:159-184.
24. Hervonen A., Pelto-Huikko M., Helén P., Alho H. Electron-microscopic localization of enkephalin-like imnmunoreactivity in axon terminals of human sympathetic ganglia. Histochemistry 1980, 70:1-6.
25. Heym C., Braun B., Klimaschewski L., Kummer W. Chemical codes of sensory neurons innervating the guinea-pig adrenal gland. Cell Tissue Res 1995, 279:169-181.
26. Holgert H., Holmberg K., Hannibal J., Fahrenkrug J., Brimijoin S., Hartman B.K., Hökfelt T. PACAP in the adrenal gland-relationship with choline acetyltransferase, enkephalin and chromaffin cells and effects of immunological sympathectomy. Neuroreport 1996, 8:297.
27. Hong Y., Weaver L.C. Distribution of immunoreactivity for enkephalin, substance P and vasoactive intestinal peptide in fibres surrounding splanchnic sympathetic preganglionic neurons in rats. Neuroscience 1993, 57:1121-1133.
28. Iijima T., Matsumoto G., Kidokoro Y. Synaptic activation of rat adrenal medulla examined with a large photodiode array in combination with a voltage-sensitive dye. Neuroscience 1992, 51:211-219.
29. Jarry H., Dietrich M., Barthel A., Giesler A., Wuttke W. In Vivo demonstration of a paracrine, inhibitory action of met-enkephalin on adrenomedullary catecholamine release in the rat. Endocrinology 1989, 125:624-629.
30. Kent C., Coupland R. Localisation of chromogranin A and B, met-enkephalin-arg6-gly7-leu8 and PGP95-like immunoreactivity in the developing and adult rat adrenal medulla and extra-adrenal chromaffin tissue. J Anat 1989, 166:213-225.
31. Kesse W.K., Parker T.L., Coupland R.E. The innervation of the adrenal gland. I. The source of pre- and postganglionic nerve fibres to the rat adrenal gland. J Anat 1988, 157:33-41.
32. Khalil Z., Livett B.G., Marley P.D. The role of sensory fibres in the rat splanchnic nerve in the regulation of adrenal medullary secretion during stress. J Physiol 1986, 370:201-215.
33. Kimura T., Katoh M., Satoh S. Inhibition by opioid agonists and enhancement by antagonists of the release of catecholamines from the dog adrenal gland in response to splanchnic nerve stimulation: evidence for the functional role of opioid receptors. J Pharmacol Exp Ther 1988, 244:1098-1102.
34. Kondo H., Kuramoto H., Wainer B.H., Yanaihara N. Evidence for the coexistence of acetylcholine and enkephalin in the sympathetic preganglionic neurons of rats. Brain Res 1985, 335:309-314.
35. Kumar N.N., Ferguson J., Padley J.R., Pilowsky P.M., Goodchild A.K. Differential muscarinic receptor gene expression levels in the ventral medulla of spontaneously hypertensive and Wistar-Kyoto rats: role in sympathetic baroreflex function. J Hypertens 2009, 27:1001-1008.
36. Kuramoto H., Kondo H., Fujita T. Substance P-like immunoreactivity in adrenal chromaffin cells and intra-adrenal nerve fibers of rats. Histochem Cell Biol 1985, 82:507-512.
37. Kuramoto H., Kondo H., Fujita T. Neuropeptide tyrosine(NPY)-like immunoreactivity in adrenal chromaffin cells and intraadrenal nerve fibers of rats. Anat Rec 1986, 214:321-328.
38. Lamouche S., Yamaguchi N. Role of PAC1 receptor in adrenal catecholamine secretion induced by PACAP and VIP in vivo. Am J Physiol Regul Integr Comp Physiol 2001, 280:R510-R518.
39. Lamouche S., Yamaguchi N. PACAP release from the canine adrenal gland in vivo: its functional role in severe hypotension. Am J Physiol Regul Integr Comp Physiol 2003, 284:R588-R597.
40. Linnoila R.I., Diaugustine R.P., Hervonen A., Miller R.J. Distribution of [Met5]- and [Leu5]-enkephalin-, vasoactive intestinal polypeptide- and substance P-like immunoreactivities in human adrenal glands. Neuroscience 1980, 5:2247-2259.
41. Mansvelder H.D., Kits K.S. Calcium channels and the release of large dense core vesicles from neuroendocrine cells: spatial organization and functional coupling. Prog Neurobiol 2000, 62:427-441.
42. Marley P.D., Mitchelhill K.I., Livett B.G. Effects of opioid peptides containing the sequence of Met5-enkephalin or Leu5-enkephalin on nicotine-induced secretion from bovine adrenal chromaffin cells. J Neurochem 1986, 46:1-11.
43. Mikulits W., Pradet-Balade B., Habermann B., Beug H., Garcia-Sanz J., Mullner E. Isolation of translationally controlled mRNAs by differential screening. FASEB J 2000, 14:1641-1652.
44. Moller K., Zhang Y.Z., Håkanson R., Luts A., Sjölund B., Uddman R., Sundler F. Pituitary adenylate cyclase activating peptide is a sensory neuropeptide: immunocytochemical and immunochemical evidence. Neuroscience 1993, 57:725-732.
45. Morales M., Holmberg K., Xu Z., Cozzari C., Hartman B., Emson P., Goldstein M., Elfvin L., Hökfelt T. 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 1995, 92:11819-11823.
46. Morrison S.F., Cao W.H. Different adrenal sympathetic preganglionic neurons regulate epinephrine and norepinephrine secretion. Am J Physiol Regul Integr Comp Physiol 2000, 279:R1763-R1775.
47. Muroi M., Funahashi H., Zhou C.J., Ohtaki H., Arimura A., Shioda S. PACAP receptor expression in the rat adrenal medulla by in situ hybridization and immunocytochemistry. Ann N Y Acad Sci 2000, 921:349-351.
48. Murphy S.M., McAllen R., Campbell G.D., Howe P.R., Anderson C.R. Re-establishment of neurochemical coding of preganglionic neurons innervating transplanted targets. Neuroscience 2003, 117:347-360.
49. Nicholson R., Small J., Dixon A.K., Spanswick D., Lee K. Serotonin receptor mRNA expression in rat dorsal root ganglion neurons. Neurosci Lett 2003, 337:119-122.
50. Oomori Y., Okuno S., Fujisawa H., Ono K. Immunoelectron microscopic study of tyrosine hydroxylase immunoreactive nerve fibers and ganglion cells in the rat adrenal gland. Anat Rec 1991, 229:407-414.
51. Padley J.R., Kumar N.N., Li Q., Nguyen T.B.V., Pilowsky P.M., Goodchild A.K. Central command regulation of circulatory function mediated by descending pontine cholinergic inputs to sympathoexcitatory rostral ventrolateral medulla neurons. Circ Res 2007, 100:284-291.
52. Parker T., Kesse W., Mohamed A., Afework M. The innervation of the mammalian adrenal gland. J Anat 1993, 183:265-276.
53. Pelto-Huikko M., Salminen T., Hervonen A. Localization of enkephalins in adrenaline cells and the nerves innervating adrenaline cells in rat adrenal medulla. Histochem Cell Biol 1985, 82:377-383.
54. Pettersson L.M.E., Heine T., Verge V.M.K., Sundler F., Danielsen N. PACAP mRNA is expressed in rat spinal cord neurons. J Comp Neurol 2004, 471:85-96.
55. Pyner S., Coote J.H. A comparison between the adult rat and neonate rat of the architecture of sympathetic preganglionic neurones projecting to the superior cervical ganglion, stellate ganglion and adrenal medulla. J Auton Nerv Syst 1994, 48:153-166.
56. Pyner S., Coote J.H. Evidence that sympathetic preganglionic neurones are arranged in target-specific columns in the thoracic spinal cord of the rat. J Comp Neurol 1994, 342:15-22.
57. Sámano C., Zetina M.E., Cifuentes F., Morales M.A. Segregation of met-enkephalin from vesicular acetylcholine transporter and choline acetyltransferase in sympathetic preganglionic varicosities mostly lacking synaptophysin and synaptotagmin. Neuroscience 2009, 163:180-189.
58. Sámano C., Zetina M.E., Marín M.A., Cifuentes F., Morales M.A. Choline acetyl transferase and neuropeptide immunoreactivities are colocalized in somata, but preferentially localized in distinct axon fibers and boutons of cat sympathetic preganglionic neurons. Synapse 2006, 60:295-306.
59. Schramm L. Spinal sympathetic interneurons: their identification and roles after spinal cord injury. Prog Brain Res 2006, 152:27-37.
60. Schultzberg M., Hökfelt T., Lundberg J., Terenius L., Elfvin L., Elde R. Enkephalin-like immunoreactivity in nerve terminals in sympathetic ganglia and adrenal medulla and in adrenal medullary gland cells. Acta Physiol Scand 1978, 103:475-477.
61. Senba E., Yanaihara C., Yanaihara N., Tohyama M. Proenkephalin opioid peptide product in the sensory ganglia of the rat: a developmental immunohistochemical study. Brain Res Dev Brain Res 1989, 48:263-271.
62. Shafton A.D., Oldfield B.J., McAllen R.M. CRF-like immunoreactivity selectively labels preganglionic sudomotor neurons in cat. Brain Res 1992, 599:253-260.
63. Springell D.A., Powers-Martin K., Phillips J.K., Pilowsky P.M., Goodchild A.K. Phosphorylated extracellular signal-regulated kinase 1/2 immunoreactivity identifies a novel subpopulation of sympathetic preganglionic neurons. Neuroscience 2005, 133:583-590.
64. Stornetta R.L., Schreihofer A.M., Pelaez N.M., Sevigny C.P., Guyenet P.G. Preproenkephalin mRNA is expressed by C 1 and non-C 1 barosensitive bulbospinal neurons in the rostral ventrolateral medulla of the rat. J Comp Neurol 2001, 435:111-126.
65. Strack A.M., Sawyer W.B., Marubio L.M., Loewy A.D. Spinal origin of sympathetic preganglionic neurons in the rat. Brain Res 1988, 455:187-191.
66. Strack A.M., Sawyer W.B., Platt K.B., Loewy A.D. CNS cell groups regulating the sympathetic outflow to adrenal gland as revealed by transneuronal cell body labeling with pseudorabies virus. Brain Res 1989, 491:274-296.
67. Tornoe K., Hannibal J., Jensen T.B., Georg B., Rickelt L.F., Andreasen M.B., Fahrenkrug J., Holst J.J. PACAP-(1-38) as neurotransmitter in the porcine adrenal glands. Am J Physiol Endocrinol Metab 2000, 279:E1413-E1425.
68. Verhofstad A.A.J., Coupland R.E., Parker T.R., Goldstein M. Immunohistochemical and biochemical study on the development of the noradrenaline- and adrenaline-storing cells of the adrenal medulla of the rat. Cell Tissue Res 1985, 242:233-243.
69. Vollmer R.R. Selective neural regulation of epinephrine and norepinephrine cells in the adrenal medulla-cardiovascular implications. Clin Exp Hypertens 1996, 18:731-751.
70. Vollmer R.R., Balcita-Pedicino J.J., Debnam A.J., Edwards D.J. Adrenal medullary catecholamine secretion patterns in rats evoked by reflex and direct neural stimulation. Clin Exp Hypertens 2000, 22:705-715.
71. Vollmer R.R., Baruchin A., Kolibalpegher S.S., Corey S.P., Stricker E.M., Kaplan B.B. Selective activation of norepinephrine-secreting and epinephrine-secreting chromaffin cells in rat adrenal-medulla. Am J Physiol 1992, 263:R716-R721.
72. Watanabe T., Shimamoto N., Takahashi A., Fujino M. PACAP stimulates catecholamine release from adrenal medulla: a novel noncholinergic secretagogue. Am J Physiol Endocrinol Metab 1995, 269:E903-E909.
73. Wooten G.F., Kopin I.J., Axelrod J. Effects of colchicine and vinblastine on axonal transport and transmitter release in sympathetic nerves. Ann N Y Acad Sci 1975, 253:528-534.
74. Yamaguchi N., Lamouche S. Enhanced reactivity of the adrenal medulla in response to pituitary adenylate cyclase activating polypeptide 1-27 (PACAP) during insulin-induced hypoglycemia in anesthetized dogs. Can J Physiol Pharmacol 1999, 77:819-826.
75. Zhou X.F., Oldfield B.J., Livett B.G. Substance P-containing sensory neurons in the rat dorsal root ganglia innervate the adrenal medulla. J Auton Nerv Syst 1991, 33:247-254.