Segregation of met-enkephalin from vesicular acetylcholine transporter and choline acetyltransferase in sympathetic preganglionic varicosities mostly lacking synaptophysin and synaptotagmin

Neuroscience

Volumn 163, Issue 1, 2009, Pages 180-189

  Samano C ^a   Zetina, M E ^a   Cifuentes, F ^a   Morales, M A ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

cholinergic synapse; cotransmission; peptides; transmitters

Indexed keywords

CHOLINE ACETYLTRANSFERASE; METENKEPHALIN; SYNAPTOPHYSIN; SYNAPTOTAGMIN; VESICULAR ACETYLCHOLINE TRANSPORTER;

ANIMAL TISSUE; ARTICLE; CELL VACUOLE; CONTROLLED STUDY; FEMALE; IMMUNOREACTIVITY; NERVE FIBER; NONHUMAN; PERIKARYON; PREGANGLIONIC NERVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD; SUPERIOR CERVICAL GANGLION; TISSUE SECTION;

ACETYLCHOLINE; ANIMALS; CHOLINE O-ACETYLTRANSFERASE; ENKEPHALIN, METHIONINE; GANGLIA, SYMPATHETIC; IMMUNOHISTOCHEMISTRY; MALE; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION; SYNAPTOPHYSIN; SYNAPTOTAGMINS; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS;

EID: 68549110172     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.06.010     Document Type: Article

References (58)

1. Baluk P. Structure of autonomic ganglia. In: McLachlan E. (Ed). Autonomic ganglia (1995), Harwood Academic PublishersLuxembourg, Luxembourg 13-71
2. Berg E.A., Johnson R.J., Leeman S.E., Boyd N., Kimerer L., and Fine R.E. Isolation and characterization of substance P-containing dense core vesicles from rabbit optic nerve and termini. J Neurosci Res 62 (2000) 830-839
3. Blitz D.M., and Nusbaum M.P. Distinct functions for cotransmitters mediating motor pattern selection. J Neurosci 19 (1999) 6774-6783
4. Boarder M.R. Presynaptic aspects of cotransmission: relationship between vesicles and neurotransmitters. J Neurochem 53 (1989) 1-11
5. Bowers C.W., and Zigmond R.E. Localization of neurons in the rat superior cervical ganglion that project into different postganglionic trunks. J Comp Neurol 185 (1979) 381-391
6. Burnstock G. Co-transmission. Curr Opin Pharmacol 4 (2004) 47-52
7. Chanthaphavong R.S., Murphy S.M., and Anderson C.R. Chemical coding of sympathetic neurons controlling the tarsal muscle of the rat. Auton Neurosci Basic Clin 105 (2003) 77-89
8. Chun J.Y., Korner J., Kreiner T., Scheller R.H., and Axel R. The function and differential sorting of a family of aplysia prohormone processing enzymes. Neuron 12 (1994) 831-844
9. Colombo-Benkmann M., Heym C., and Schemann M. Preganglionic sympathetic neurons, innervating the guinea pig adrenal medulla, immunohistochemically contain choline acetyltransferase and also leu-enkephalin. Neurosci Lett 190 (1995) 155-158
10. Dal Bo G., Bérubé-Carrière N., Mendez J.A., Leo D., Riad M., Descarries L., Lévesque D., and Trudeau L.E. Enhanced glutamatergic phenotype of mesencephalic dopamine neurons after neonatal 6-hydroxydopamine lesion. Neuroscience 156 (2008) 59-70
11. Descarries L., Bérubé-Carrière N., Riad M., Bo G.D., Mendez J.A., and Trudeau L.E. Glutamate in dopamine neurons: synaptic versus diffuse transmission. Brain Res Rev 58 (2008) 290-302
12. Dobó E., Joó F., and Wolff J.R. Distinct subsets of neuropeptide Y-negative principal neurons receive basket-like innervation from enkephalinergic and gabaergic axons in the superior cervical ganglion of adult rats. Neuroscience 57 (1993) 833-844
13. Elfvin L.G., Lindh B., and Hökfelt T. The chemical neuroanatomy of sympathetic ganglia. Annu Rev Neurosci 16 (1993) 471-507
14. Fisher J.M., Sossin W., Newcomb R., and Scheller R.H. Multiple neuropeptides derived from a common precursor are differentially packaged and transported. Cell 54 (1988) 813-822
15. Furness J.B., Morris J.L., Gibbins I.L., and Costa M. Chemical coding of neurons and plurichemical transmission. Annu Rev Pharmacol Toxicol 29 (1989) 289-306
16. Gibbins I.L. Vasoconstrictor, vasodilator and pilomotor pathways in sympathetic ganglia of guinea-pigs. Neuroscience 47 (1992) 657-672
17. Gibbins I.L., Jobling P., Teo E.H., Matthew S.E., and Morris J.L. Heterogeneous expression of SNAP-25 and synaptic vesicle proteins by central and peripheral inputs to sympathetic neurons. J Comp Neurol 459 (2003) 25-43
18. Hattori T., Takada M., Moriizumi T., and Van Der Kooy D. Single dopaminergic nigrostriatal neurons form two chemically distinct synaptic types: possible transmitter segregation within neurons. J Comp Neurol 309 (1991) 391-401
19. Heym C., König R., Schröder H., and Gerold N. Immunofluorescent and biochemical studies on dopamine-beta-hydroxylase and catecholamines in SIF cells of the superior cervical ganglion. Acta Histochem Suppl 24 (1981) 123-129
20. Ito T., Hioki H., Nakamura K., Tanaka Y., Nakade H., Kaneko T., Iino S., and Nojyo Y. Gamma-aminobutyric acid-containing sympathetic preganglionic neurons in rat thoracic spinal cord send their axons to the superior cervical ganglion. J Comp Neurol 502 (2007) 113-125
21. Ito T., Iino S., and Nojyo Y. A part of cholinergic fibers in mouse superior cervical ganglia contain GABA or glutamate. Brain Res 1046 (2005) 234-238
22. Jiménez B., Mora-Valladares E., Zetina M.E., and Morales M.A. Occurrence, co-occurrence and topographic distribution of choline acetyltransferase, met-enkephalin and neurotensin in the stellate ganglion of the cat. Synapse 43 (2002) 163-174
23. Joyce M.P., and Rayport S. Mesoaccumbens dopamine neuron synapses reconstructed in vitro are glutamatergic. Neuroscience 99 (2000) 445-456
24. Karhula T., Soinila S., Lakomy M., Majewski M., Kaleczyk J., and Häppölä O. 5-Hydroxytryptamine-immunoreactive nerve fibers in the rat and porcine prevertebral sympathetic ganglia: effect of precursor loading and relation to catecholaminergic neurons. Neurosci Lett 194 (1995) 85-88
25. Kása P., Joó F., Dobó E., Wenthold R.J., Ottersen O.P., Storm-Mathisen J., and Wolff J.R. Heterogeneous distribution of GABA-immunoreactive nerve fibers and axon terminals in the superior cervical ganglion of adult rat. Neuroscience 26 (1988) 635-644
26. Kondo H., Kuramoto H., Wainer B.H., and Yanaihara N. Evidence for the coexistence of acetylcholine and enkephalin in the sympathetic preganglionic neurons of rats. Brain Res 335 (1985) 309-314
27. Kow L.M., and Pfaff D.W. Neuromodulatory actions of peptides. Annu Rev Pharmacol Toxicol 28 (1988) 163-188
28. Landis S.C. Neurotransmitter plasticity in sympathetic neurons. In: Björklund A., Hökfelt T., and Owman C. (Eds). Handbook of chemical neuroanatomy, Vol. 6. The peripheral nervous system (1988), Elsevier, Amsterdam 65-115
29. Landry M., Vila-Porcile E., Hokfelt T., and Calas A. Differential routing of coexisting neuropeptides in vasopressin neurons. Eur J Neurosci 17 (2003) 579-589
30. Li C., and Horn J.P. Physiological classification of sympathetic neurons in the rat superior cervical ganglion. J Neurophysiol 95 (2006) 187-195
31. Lindh B., and Hökfelt T. Structural and functional aspects of acetylcholine peptide coexistence in the autonomic nervous system. In: Aquilonius S.M., and Gillberg P.G. (Eds). Cholinergic Neurotransmission: Functional and Clinical Aspect, Progress in Brain Research Vol. 84 (1990), Elsevier, Amsterdam 175-191
32. Lindh B., Staines W., Hökfelt T., Terenius L., and Salvaterra P. Immunohistochemical demonstration of choline acetyltransferase-immunoreactive preganglionic nerve fibers in guinea pig autonomic ganglia. Proc Natl Acad Sci U S A 83 (1986) 5316-5320
33. Merighi A. Costorage and coexistence of neuropeptides in the mammalian CNS. Prog Neurobiol 66 (2002) 161-190
34. Morales M.A., Hancock J.C., and Hoover D.B. Neurochemical heterogeneity in sympathetic ganglia and its implications for cardiovascular regulation. In: Dun N.J., Machado B.H., and Pilowsky P.M. (Eds). Neural mechanisms of cardiovascular regulation (2004), Kluwer Academic Publishers, Boston 303-333
35. Morales M.A., Holmberg K., Xu Z., Cozzari C., Hartman B., Emson P., Goldstein M., Elfvin L., and 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 92 (1995) 11819-11823
36. Morris J.L., and Gibbins I. Co-transmission and neuromodulation. In: Burnstock G., and Hoyle C. (Eds). Autonomic neuroeffector mechanisms (1992), Harwood Academic Publishers, Philadelphia 33-119
37. Morrison S.F., Callaway J., Milner T.A., and Reis D.J. Glutamate in the spinal sympathetic intermediolateral nucleus: localization by light and electron microscopy. Brain Res 503 (1989) 5-15
38. Murphy S.M., Matthew S.E., Rodgers H.F., Lituri D.T., and Gibbins I.L. Synaptic organization of neuropeptide-containing preganglionic boutons in lumbar sympathetic ganglia of guinea pigs. J Comp Neurol 398 (1998) 551-567
39. Navone F., Di Gioia G., Jahn R., Browning M., Greengard P., and De Camilli P. Microvesicles of the neurohypophysis are biochemically related to small synaptic vesicles of presynaptic nerve terminals. J Cell Biol 109 (1989) 3425-3433
40. Nishimaru H., Restrepo C.E., Ryge J., Yanagawa Y., and Kiehn O. Mammalian motor neurons corelease glutamate and acetylcholine at central synapses. Proc Natl Acad Sci U S A 102 (2005) 5245-5249
41. Párducz A., Dobo E., Joo F., and Wolff J.R. Termination pattern and fine structural characteristics of GABA- and [Met]enkephalin-containing nerve fibers and synapses in the superior cervical ganglion of adult rat. Neuroscience 49 (1992) 963-971
42. Potter D.D., Matsumoto S.G., Landis S.C., Sah D.W.Y., and Furshpan E.J. Transmitter status in cultured sympathetic principal neurons: plasticity, graded expression and diversity. In: Hökfelt T., Fuxe K., and Pernow B. (Eds). Coexistence of Neuronal Messenger: A New Principle in Chemical Transmission, Progress in Brain Research Vol. 6 (1986), Elsevier, Amsterdam 103-120
43. Sámano C.G., Zetina M.E., Cifuentes F., and Morales M.A. Cholinergic markers-choline acetyl transferase or vesicular acetylcholine transporter-and methionine-enkephalin (m-enk) immunoreactivity are co-localized in somata but preferentially located in separate axon fibers of rat sympathetic preganglionic neurons. Program No 359.9. Abstract viewer and itinerary planner (2007), Society for Neuroscience, San Diego, CA
44. Sámano C., Zetina M.E., Marín M.A., Cifuentes F., and 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 60 (2006) 295-306
45. Scalettar B.A. How neurosecretory vesicles release their cargo. Neuroscientist 12 (2006) 164-176
46. Semba E., Kaneko N., Mizuno M., and Tohyama M. Somato-, branchio- and viscero-motor neurons contain glutaminase-like immunoreactivity. Br Res Bull 26 (1991) 85-97
47. Slonimsky J.D., Yang B., Hinterneder J.M., Nokes E.B., and Birren S.J. BDNF and CNTF regulate cholinergic properties of sympathetic neurons through independent mechanisms. Mol Cell Neurosci 23 (2003) 648-660
48. Sorra K.E., Mishra A., Kirov S.A., and Harris K.M. Dense core vesicles resemble active-zone transport vesicles and are diminished following synaptogenesis in mature hippocampal slices. Neuroscience 141 (2006) 2097-2106
49. Sossin W.S., Sweet-Cordero A., and Scheller R.H. Dale's hypothesis revised: differential neuropeptides derived from a common precursor are targeted to different processes. Proc Natl Acad Sci U S A 87 (1990) 4845-4848
50. Strand F.L. Neuropeptides: regulators of physiological process (1999), MIT Press, Cambridge, MA
51. Sulzer D., Joyce M.P., Lin L., Geldwert D., Haber S.N., Hattori T., and Rayport S. Dopamine neurons make glutamatergic synapses in vitro. J Neurosci 18 (1998) 4588-4602
52. Sulzer D., and Rayport S. Dale's principle and glutamate corelease from ventral midbrain dopamine neurons. Amino Acids 19 (2000) 45-52
53. Walch-Solimena C., Takei K., Marek K.L., Midyett K., Südhof T.C., De Camilli P., and Jahn R. Synaptotagmin: a membrane constituent of neuropeptide-containing large dense-core vesicles. J Neurosci 13 (1993) 3895-3903
54. r 38,000 characteristic of presynaptic vesicles. Cell 41 (1985) 1017-1028
55. Winkler H. Membrane composition of adrenergic large and small dense cored vesicles and of synaptic vesicles: consequences for their biogenesis. Neurochem Res 22 (1997) 921-932
56. Wolff J.R., Kasa P., Dobo E., Wenthold R.J., and Joo F. Quantitative analysis of the number and distribution of neurons richly innervated by GABA-immunoreactive axons in the rat superior cervical ganglion. J Comp Neurol 282 (1989) 264-273
57. Yang B., Slonimsky J.D., and Birren S.J. A rapid switch in sympathetic neurotransmitter release properties mediated by the p75 receptor. Nat Neurosci 5 (2002) 539-545
58. Zhai R.G., Vardinon-Friedman H., Cases-Langhoff C., Becker B., Gundelfinger E.D., Ziv N.E., and Garner C.C. Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron 29 (2001) 131-143