Endomorphin-2 is released from newborn rat primary sensory neurons in a frequency- and calcium-dependent manner

European Journal of Neuroscience

Volumn 27, Issue 10, 2008, Pages 2629-2642

  Scanlin, Heather L ^a   Carroll, Elizabeth A ^a   Jenkins, Victoria K ^a   Balkowiec, Agnieszka ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Activity dependent release; Dorsal root ganglion; Nodose petrosal; Opiates

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM CHANNEL; DEXTRO PHENYLALANYLCYSTEINYLTYROSYL DEXTRO TRYPTOPHYLARGINYLTHREONYLPENICILLAMINYLTHREONINAMIDE 2,7 DISULFIDE; ENDOMORPHIN 2; POTASSIUM CHLORIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CELL SUBPOPULATION; CONTROLLED STUDY; ELECTROSTIMULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR CALCIUM; IMMUNOREACTIVITY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION; RAT; SENSORY NERVE CELL; SPINAL GANGLION; SYNAPSE;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELLS, CULTURED; ELECTRIC STIMULATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; GANGLIA, SENSORY; GANGLIA, SPINAL; NEURONAL PLASTICITY; NEURONS, AFFERENT; NODOSE GANGLION; OLIGOPEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 44649196530     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06238.x     Document Type: Article

References (93)

1. Abbadie, C., Rossi, G.C., Orciuolo, A., Zadina, J.E. Pasternak, G.W. (2002) Anatomical and functional correlation of the endomorphins with mu opioid receptor splice variants. Eur. J. Neurosci., 16, 1075 1082.
2. Abramoff, M.D., Magelhaes, P.J. Ram, S.J. (2004) Image processing with ImageJ. Biophotonics Intl., 11, 36 42.
3. Aicher, S.A., Goldberg, A., Sharma, S. Pickel, V.M. (2000) μ-Opioid receptors are present in vagal afferents and their dendritic targets in the medial nucleus tractus solitarius. J. Comp. Neurol., 422, 181 190.
4. Aicher, S.A., Schreihofer, A.M., Kraus, J.A., Sharma, S., Milner, T.A. Guyenet, P.G. (2001) Mu-opioid receptors are present in functionally identified sympathoexcitatory neurons in the rat rostral ventrolateral medulla. J. Comp. Neurol., 433, 34 47.
5. Arvidsson, U., Riedl, M., Chakrabarti, S., Lee, J.H., Nakano, A.H., Dado, R.J., Loh, H.H., Law, P.Y., Wessendorf, M.W. Elde, R. (1995) Distribution and targeting of a μ-opioid receptor (MOR1) in brain and spinal cord. J. Neurosci., 15, 3328 3341.
6. Balkowiec, A. Katz, D.M. (2000) Activity-dependent release of endogenous brain-derived neurotrophic factor from primary sensory neurons detected by ELISA in situ. J. Neurosci., 20, 7417 7423.
7. Balkowiec, A. Katz, D.M. (2002) Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J. Neurosci., 22, 10399 10407.
8. Balkowiec, A., Kunze, D.L. Katz, D.M. (2000) Brain-derived neurotrophic factor acutely inhibits AMPA-mediated currents in developing sensory relay neurons. J. Neurosci., 20, 1904 1911.
9. Barr, G.A. Zadina, J.E. (1999a) The ontogeny of endomorphin-1- and endomorphin-2-like immunoreactivity in rat brain and spinal cord. Ann. NY Acad. Sci., 897, 145 153.
10. Barr, G.A. Zadina, J.E. (1999b) Maturation of endomorphin-2 in the dorsal horn of the medulla and spinal cord of the rat. Neuroreport, 10, 3857 3860.
11. Beland, B. Fitzgerald, M. (2001) Mu- and delta-opioid receptors are downregulated in the largest diameter primary sensory neurons during postnatal development in rats. Pain, 90, 143 150.
12. Brain, S.D. Cox, H.M. (2006) Neuropeptides and their receptors: innovative science providing novel therapeutic targets. Br. J. Pharmacol., 147 (Suppl 1 S202 S211.
13. Brigadski, T., Hartmann, M. Lessmann, V. (2005) Differential vesicular targeting and time course of synaptic secretion of the mammalian neurotrophins. J. Neurosci., 25, 7601 7614.
14. Brooks, J.W., Thompson, S.W., Rice, A.S. Malcangio, M. (2004) (S)-AMPA inhibits electrically evoked calcitonin gene-related peptide (CGRP) release from the rat dorsal horn: reversal by cannabinoid receptor antagonist SR141716A. Neurosci. Lett., 372, 85 88.
15. Budai, D. Fields, H.L. (1998) Endogenous opioid peptides acting at mu-opioid receptors in the dorsal horn contribute to midbrain modulation of spinal nociceptive neurons. J. Neurophysiol., 79, 677 687.
16. Buldyrev, I., Tanner, N.M., Hsieh, H.Y., Dodd, E.G., Nguyen, L.T. Balkowiec, A. (2006) Calcitonin gene-related peptide enhances release of native brain-derived neurotrophic factor from trigeminal ganglion neurons. J. Neurochem., 99, 1338 1350.
17. Canossa, M., Gartner, A., Campana, G., Inagaki, N. Thoenen, H. (2001) Regulated secretion of neurotrophins by metabotropic glutamate group I (mGluRI) and Trk receptor activation is mediated via phospholipase C signalling pathways. EMBO J., 20, 1640 1650.
18. Cazalis, M., Dayanithi, G. Nordmann, J.J. (1985) The role of patterned burst and interburst interval on the excitation-coupling mechanism in the isolated rat neural lobe. J. Physiol. (Lond.), 369, 45 60.
19. Champion, H.C., Zadina, J.E., Kastin, A.J., Hackler, L., Ge, L.J. Kadowitz, P.J. (1997) Endomorphin 1 and 2, endogenous ligands for the mu-opioid receptor, decrease cardiac output, and total peripheral resistance in the rat. Peptides, 18, 1393 1397.
20. Chapman, V., Diaz, A. Dickenson, A.H. (1997) Distinct inhibitory effects of spinal endomorphin-1 and endomorphin-2 on evoked dorsal horn neuronal responses in the rat. Br. J. Pharmacol., 122, 1537 1539.
21. Chen, C.Y., Horowitz, J.M. Bonham, A.C. (1999) A presynaptic mechanism contributes to depression of autonomic signal transmission in NTS. Am. J. Physiol., 277, H1350 H1360.
22. Czapla, M.A., Champion, H.C., Zadina, J.E., Kastin, A.J., Hackler, L., Ge, L.J. Kadowitz, P.J. (1998) Endomorphin 1 and 2, endogenous μ-opioid agonists, decrease systemic arterial pressure in the rat. Life Sci., 62, 175 179.
23. Diaz, A. Dickenson, A.H. (1997) Blockade of spinal N- and P-type, but not L-type, calcium channels inhibits the excitability of rat dorsal horn neurons produced by subcutaneous formalin inflammation. Pain, 69, 93 100.
24. Ding, Y.Q., Nomura, S., Kaneko, T. Mizuno, N. (1995) Co-localization of μ-opioid receptor-like and substance P-like immunoreactivities in axon terminals within the superficial layers of the medullary and spinal dorsal horns of the rat. Neurosci. Lett., 198, 45 48.
25. Dun, N.J., Dun, S.L., Wu, S.Y., Williams, C.A. Kwok, E.H. (2000) Endomorphins: localization, release and action on rat dorsal horn neurons. J. Biomed. Sci., 7, 213 220.
26. Franck, J., Brodin, E. Fried, G. (1993) Differential release of endogenous 5-hydroxytryptamine, substance P, and neurokinin A from rat ventral spinal cord in response to electrical stimulation. J. Neurochem., 61, 704 711.
27. Ghosh, A., Ginty, D.D., Bading, H. Greenberg, M.E. (1994) Calcium regulation of gene expression in neuronal cells. J. Neurobiol., 25, 294 303.
28. Goldberg, I.E., Rossi, G.C., Letchworth, S.R., Mathis, J.P., Ryan-Moro, J., Leventhal, L., Su, W., Emmel, D., Bolan, E.A. Pasternak, G.W. (1998) Pharmacological characterization of endomorphin-1 and endomorphin-2 in mouse brain. J. Pharmacol. Exp. Ther., 286, 1007 1013.
29. Gordon, F.J. (1990) Opioids and central baroreflex control: a site of action in the nucleus tractus solitarius. Peptides, 11, 305 309.
30. Greenwell, T.N., Martin-Schild, S., Inglis, F.M. Zadina, J.E. (2007) Colocalization and shared distribution of endomorphins with substance P, calcitonin gene-related peptide, ã-aminobutyric acid, and the mu opioid receptor. J. Comp. Neurol., 503, 319 333.
31. Guyenet, P.G., Stornetta, R.L., Schreihofer, A.M., Pelaez, N.M., Hayar, A., Aicher, S. Llewellyn-Smith, I.J. (2002) Opioid signalling in the rat rostral ventrolateral medulla. Clin. Exp. Pharmacol. Physiol., 29, 238 242.
32. Hamra, M., McNeil, R.S., Runciman, M. Kunze, D.L. (1999) Opioid modulation of calcium current in cultured sensory neurons: mu-modulation of baroreceptor input. Am. J. Physiol., 277, H705 H713.
33. 2+ channels to nociceptive transmission in rat spinal lamina I neurons. Eur. J. Neurosci., 19, 103 111.
34. Holz, G.G. IV., Dunlap, K. Kream, R.M. (1988) Characterization of the electrically evoked release of substance P from dorsal root ganglion neurons: methods and dihydropyridine sensitivity. J. Neurosci., 8, 463 471.
35. Huang, L.Y. Neher, E. (1996) Ca(2+)-dependent exocytosis in the somata of dorsal root ganglion neurons. Neuron, 17, 135 145.
36. Iverfeldt, K., Serfozo, P., Diaz Arnesto, L. Bartfai, T. (1989) Differential release of coexisting neurotransmitters: frequency dependence of the efflux of substance P, thyrotropin releasing hormone and [3H]serotonin from tissue slices of rat ventral spinal cord. Acta Physiol. Scand., 137, 63 71.
37. Janecka, A., Kruszynski, R., Fichna, J., Kosson, P. Janecki, T. (2006) Enzymatic degradation studies of endomorphin-2 and its analogs containing N-methylated amino acids. Peptides, 27, 131 135.
38. Kasamatsu, K., Chitravanshi, V.C. Sapru, H.N. (2004) Depressor and bradycardic responses to microinjections of endomorphin-2 into the NTS are mediated via ionotropic glutamate receptors. Am. J. Physiol., 287, R715 R728.
39. Lessmann, V., Gottmann, K. Malcangio, M. (2003) Neurotrophin secretion: current facts and future prospects. Prog. Neurobiol., 69, 341 374.
40. Lever, I.J., Bradbury, E.J., Cunningham, J.R., Adelson, D.W., Jones, M.G., McMahon, S.B., Marvizon, J.C. Malcangio, M. (2001) Brain-derived neurotrophic factor is released in the dorsal horn by distinctive patterns of afferent fiber stimulation. J. Neurosci., 21, 4469 4477.
41. Lever, I.J., Grant, A.D., Pezet, S., Gerard, N.P., Brain, S.D. Malcangio, M. (2003) Basal and activity-induced release of substance P from primary afferent fibres in NK1 receptor knockout mice: evidence for negative feedback. Neuropharmacology, 45, 1101 1110.
42. Lisi, T.L. Sluka, K.A. (2006) A new electrochemical HPLC method for analysis of enkephalins and endomorphins. J. Neurosci. Methods, 150, 74 79.
43. Liu, X. Sandkuhler, J. (1997) Characterization of long-term potentiation of C-fiber-evoked potentials in spinal dorsal horn of adult rat: essential role of NK1 and NK2 receptors. J. Neurophysiol., 78, 1973 1982.
44. Liu, Z., Chen, C.Y. Bonham, A.C. (1998) Metabotropic glutamate receptors depress vagal and aortic baroreceptor signal transmission in the NTS. Am. J. Physiol., 275, H1682 H1694.
45. Liu, Z., Chen, C.Y. Bonham, A.C. (2000) Frequency limits on aortic baroreceptor input to nucleus tractus solitarii. Am. J. Physiol., 278, H577 H585.
46. Llewellyn-Smith, I.J., Schreihofer, A.M. Guyenet, P.G. (2001) Distribution and amino acid content of enkephalin-immunoreactive inputs onto juxtacellularly labelled bulbospinal barosensitive neurons in rat rostral ventrolateral medulla. Neuroscience, 108, 307 322.
47. Lundberg, J.M., Fried, G., Pernow, J. Theodorsson-Norheim, E. (1986) Co-release of neuropeptide Y and catecholamines upon adrenal activation in the cat. Acta Physiol. Scand., 126, 231 238.
48. Malcangio, M. Bowery, N.G. (1996) Calcitonin gene-related peptide content, basal outflow and electrically-evoked release from monoarthritic rat spinal cord in vitro. Pain, 66, 351 358.
49. Malcangio, M. Lessmann, V. (2003) A common thread for pain and memory synapses? Brain-derived neurotrophic factor and trkB receptors Trends Pharmacol. Sci., 24, 116 121.
50. Malcangio, M., Garrett, N.E. Tomlinson, D.R. (1997) Nerve growth factor treatment increases stimulus-evoked release of sensory neuropeptides in the rat spinal cord. Eur. J. Neurosci., 9, 1101 1104.
51. Mannion, R.J., Costigan, M., Decosterd, I., Amaya, F., Ma, Q.P., Holstege, J.C., Ji, R.R., Acheson, A., Lindsay, R.M., Wilkinson, G.A. Woolf, C.J. (1999) Neurotrophins: peripherally and centrally acting modulators of tactile stimulus-induced inflammatory pain hypersensitivity. Proc. Natl Acad. Sci. USA, 96, 9385 9390.
52. Martin-Schild, S., Zadina, J.E., Gerall, A.A., Vigh, S. Kastin, A.J. (1997) Localization of endomorphin-2-like immunoreactivity in the rat medulla and spinal cord. Peptides, 18, 1641 1649.
53. Martin-Schild, S., Gerall, A.A., Kastin, A.J. Zadina, J.E. (1998) Endomorphin-2 is an endogenous opioid in primary sensory afferent fibers. Peptides, 19, 1783 1789.
54. Martin-Schild, S., Gerall, A.A., Kastin, A.J. Zadina, J.E. (1999) Differential distribution of endomorphin 1- and endomorphin 2-like immunoreactivities in the CNS of the rodent. J. Comp. Neurol., 405, 450 471.
55. Matthews, E.A. Dickenson, A.H. (2001) Effects of spinally delivered N- and P-type voltage-dependent calcium channel antagonists on dorsal horn neuronal responses in a rat model of neuropathy. Pain, 92, 235 246.
56. Moises, H.C., Rusin, K.I. MacDonald, R.L. (1994) Mu- and kappa-opioid receptors selectively reduce the same transient components of high-threshold calcium current in rat dorsal root ganglion sensory neurons. J. Neurosci., 14, 5903 5916.
57. Moore, A.N., Waxham, M.N. Dash, P.K. (1996) Neuronal activity increases the phosphorylation of the transcription factor cAMP response element-binding protein (CREB) in rat hippocampus and cortex. J. Biol. Chem., 271, 14214 14220.
58. Murakami, M., Nakagawasai, O., Suzuki, T., Mobarakeh, I.I., Sakurada, Y., Murata, A., Yamadera, F., Miyoshi, I., Yanai, K., Tan-No, K., Sasano, H., Tadano, T. Iijima, T. (2004) Antinociceptive effect of different types of calcium channel inhibitors and the distribution of various calcium channel alpha 1 subunits in the dorsal horn of spinal cord in mice. Brain Res., 1024, 122 129.
59. Nemeth, J., Oroszi, G., Than, M., Helyes, Z.S., Pinter, E., Farkas, B. Szolcsanyi, J. (1999) Substance P radioimmunoassay for quantitative characterization of sensory neurotransmitter release. Neurobiology (Budapest), 7, 437 444.
60. Ng, B.K., Chen, L., Mandemakers, W., Cosgaya, J.M. Chan, J.R. (2007) Anterograde transport and secretion of brain-derived neurotrophic factor along sensory axons promote Schwann cell myelination. J. Neurosci., 27, 7597 7603.
61. Nomura, S., Ding, Y.Q., Kaneko, T., Li, J.L. Mizuno, N. (1996) Localization of μ-opioid receptor-like immunoreactivity in the central components of the vagus nerve: a light and electron microscope study in the rat. Neuroscience, 73, 277 286.
62. 2+ sparks and secretion in dorsal root ganglion neurons. Proc. Natl Acad. Sci. USA, 102, 12259 12264.
63. Pezet, S., Malcangio, M. McMahon, S.B. (2002) BDNF: a neuromodulator in nociceptive pathways? Brain Res. Rev., 40, 240 249.
64. Pierce, T.L., Grahek, M.D. Wessendorf, M.W. (1998) Immunoreactivity for endomorphin-2 occurs in primary afferents in rats and monkey. Neuroreport, 9, 385 389.
65. Qin, X., Wan, Y. Wang, X. (2005) CCL2 and CXCL1 trigger calcitonin gene-related peptide release by exciting primary nociceptive neurons. J. Neurosci. Res., 82, 51 62.
66. Randic, M., Jiang, M.C. Cerne, R. (1993) Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord. J. Neurosci., 13, 5228 5241.
67. Rusin, K.I. Moises, H.C. (1995) mu-Opioid receptor activation reduces multiple components of high-threshold calcium current in rat sensory neurons. J. Neurosci., 15, 4315 4327.
68. 2+ currents in rat nodose ganglion neurons. Neuroscience, 85, 939 956.
69. Sakurada, S., Hayashi, T., Yuhki, M., Orito, T., Zadina, J.E., Kastin, A.J., Fujimura, T., Murayama, K., Sakurada, C., Sakurada, T., Narita, M., Suzuki, T., Tan-No, K. Tseng, L.F. (2001) Differential antinociceptive effects induced by intrathecally administered endomorphin-1 and endomorphin-2 in the mouse. Eur. J. Pharmacol., 427, 203 210.
70. Sanderson Nydahl, K., Skinner, K., Julius, D. Basbaum, A.I. (2004) Co-localization of endomorphin-2 and substance P in primary afferent nociceptors and effects of injury: a light and electron microscopic study in the rat. Eur. J. Neurosci., 19, 1789 1799.
71. Scanlin, H.L. Balkowiec, A. (2004) Opioids regulate activity-dependent BDNF release from primary sensory neurons. Soc. Neurosci. Abstr., 726.9.
72. Scanlin, H., Pino, E.A. Balkowiec, A. (2006) Activity-dependent release of endomorphin-2 from early postnatal nodose ganglion neurons. Soc. Neurosci. Abstr., 321.18.
73. Shane, R., Wilk, S. Bodnar, R.J. (1999) Modulation of endomorphin-2-induced analgesia by dipeptidyl peptidase IV. Brain Res., 815, 278 286.
74. Silverman, M.B., Hermes, S.M., Zadina, J.E. Aicher, S.A. (2005) Mu-opioid receptor is present in dendritic targets of endomorphin-2 axon terminals in the nuclei of the solitary tract. Neuroscience, 135, 887 896.
75. Soignier, R.D., Vaccarino, A.L., Brennan, A.M., Kastin, A.J. Zadina, J.E. (2000) Analgesic effects of endomorphin-1 and endomorphin-2 in the formalin test in mice. Life Sci., 67, 907 912.
76. Stone, L.S., Fairbanks, C.A., Laughlin, T.M., Nguyen, H.O., Bushy, T.M., Wessendorf, M.W. Wilcox, G.L. (1997) Spinal analgesic actions of the new endogenous opioid peptides endomorphin-1 and -2. Neuroreport, 8, 3131 3135.
77. Stornetta, R.L., Schreihofer, A.M., Pelaez, N.M., Sevigny, C.P. Guyenet, P.G. (2001) Preproenkephalin mRNA is expressed by C1 and non-C1 barosensitive bulbospinal neurons in the rostral ventrolateral medulla of the rat. J. Comp. Neurol., 435, 111 126.
78. Suarez-Roca, H. Maixner, W. (1995) Morphine produces a biphasic modulation of substance P release from cultured dorsal root ganglion neurons. Neurosci. Lett., 194, 41 44.
79. Thompson, S.W., Bennett, D.L., Kerr, B.J., Bradbury, E.J. McMahon, S.B. (1999) Brain-derived neurotrophic factor is an endogenous modulator of nociceptive responses in the spinal cord. Proc. Natl Acad. Sci. USA, 96, 7714 7718.
80. Tömböly, C., Péter, A. Tóth, G. (2002) In vitro quantitative study of the degradation of endomorphins. Peptides, 23, 1573 1580.
81. Verhage, M., McMahon, H.T., Ghijsen, W.E., Boomsma, F., Scholten, G., Wiegant, V.M. Nicholls, D.G. (1991) Differential release of amino acids, neuropeptides, and catecholamines from isolated nerve terminals. Neuron, 6, 517 524.
82. Viard, E. Sapru, H.N. (2006) Endomorphin-2 in the medial NTS attenuates the responses to baroreflex activation. Brain Res., 1073-1074, 365 373.
83. Wang, Q. Li, P. (1988) Inhibition of baroreflex following microinjection of GABA or morphine into the nucleus tractus solitarii in rabbits. J. Auton. Nerv. Syst., 25, 165 172.
84. Wang, Q.P., Zadina, J.E., Guan, J.L., Kastin, A.J., Funahashi, H. Shioda, S. (2002) Endomorphin-2 immunoreactivity in the cervical dorsal horn of the rat spinal cord at the electron microscopic level. Neuroscience, 113, 593 605.
85. Wang, Q.P., Zadina, J.E., Guan, J.L. Shioda, S. (2003) Morphological evidence of endomorphin as an agonist for the mu-opioid receptor in the rat spinal cord. Neurosci. Lett., 341, 107 110.
86. Whim, M.D. Lloyd, P.E. (1989) Frequency-dependent release of peptide cotransmitters from identified cholinergic motor neurons in Aplysia. Proc. Natl Acad. Sci. USA, 86, 9034 9038.
87. Whim, M.D. Lloyd, P.E. (1994) Differential regulation of the release of the same peptide transmitters from individual identified motor neurons in culture. J. Neurosci., 14, 4244 4251.
88. 2+ channels. J. Neurosci., 15, 4124 4132.
89. Williams, C.A., Wu, S.Y., Dun, S.L., Kwok, E.H. Dun, N.J. (1999) Release of endomorphin-2 like substances from the rat spinal cord. Neurosci. Lett., 273, 25 28.
90. 2+ channel currents to a mu opioid in isolectin B4-positive and -negative dorsal root ganglion neurons. J. Pharmacol. Exp. Ther., 311, 939 947.
91. Zadina, J.E., Hackler, L., Ge, L.J. Kastin, A.J. (1997) A potent and selective endogenous agonist for the mu-opiate receptor. Nature, 386, 499 502.
92. Zadina, J.E., Martin-Schild, S., Gerall, A.A., Kastin, A.J., Hackler, L., Ge, L.J. Zhang, X. (1999) Endomorphins: novel endogenous μ-opiate receptor agonists in regions of high μ-opiate receptor density. Ann. NY Acad. Sci., 897, 136 144.
93. 2+-independent but voltage-dependent secretion in mammalian dorsal root ganglion neurons. Nat. Neurosci., 5, 425 430.