Vagal afferents are necessary for the establishment but not the maintenance of kainic acid-induced hyperalgesia in mice

Pain

Volumn 102, Issue 1-2, 2003, Pages 39-49

  Tien, Duc ^a   Ohara, Peter T ^a   Larson, Alice A ^b   Jasmin, Luc ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Morphine; Nociceptive threshold; Nodose ganglion; Pain; Vagus nerve

Indexed keywords

KAINIC ACID; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN FOS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; FOREBRAIN; HYPERALGESIA; MALE; MOLECULAR BIOLOGY; MOUSE; NICK END LABELING; NOCICEPTION; NONHUMAN; PAIN ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SOLITARY TRACT NUCLEUS; SURGICAL TECHNIQUE; TAIL FLICK TEST; VAGOTOMY; VAGUS NERVE;

EID: 0346035795     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/s0304-3959(02)00336-6     Document Type: Article

References (65)

1. Abraham K.E., McGinty J.F., Brewer K.L. The role of kainic acid/AMPA and metabotropic glutamate receptors in the regulation of opioid mRNA expression and the onset of pain-related behavior following excitotoxic spinal cord injury. Neuroscience. 104:2001;863-874.
2. Baulmann J., Spitznagel H., Herdegen T., Unger T., Culman J. Tachykinin receptor inhibition and c-Fos expression in the rat brain following formalin-induced pain. Neuroscience. 95:2000;813-820.
3. Ben-Sasson S., Sherman Y., Gavrieli Y. Identification of dying cells - in situ staining. Schwartz L., Osborne B. Cell Death. 1995;29-39 Academic Press, New York, NY. (L. Wilson and P. Matsudaira).
4. Berger M.L., Lefauconnier J.M., Tremblay E., Ben-Ari Y. Limbic seizures induced by systemically applied kainic acid: how much kainic acid reaches the brain? Adv Exp Med Biol. 203:1986;199-209.
5. Bing G., Wilson B., Hudson P., Jin L., Feng Z., Zhang W., Bing R., Hong J.S. A single dose of kainic acid elevates the levels of enkephalins and activator protein-1 transcription factors in the hippocampus for up to 1 year. Proc Natl Acad Sci USA. 94:1997;9422-9427.
6. Bullitt E. Expression of c-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat. J Comp Neurol. 296:1990;517-530.
7. Burkey A.R., Carstens E., Wenniger J.J., Tang J., Jasmin L. An opioidergic cortical antinociception triggering site in the agranular insular cortex of the rat that contributes to morphine antinociception. J Neurosci. 16:1996;6612-6623.
8. Cechetto D., Saper C. Role of the cerebral cortex in autonomic function. Loewy A., Spyer K. Central regulation of autonomic function. 1990;208-223 Oxford University Press, New York, NY.
9. Coggeshall R.E., Carlton S.M. Ultrastructural analysis of NMDA, AMPA, and kainate receptors on unmyelinated and myelinated axons in the periphery. J Comp Neurol. 391:1998;78-86.
10. Ding M., Haglid K.G., Hamberger A. Quantitative immunochemistry on neuronal loss, reactive gliosis and BBB damage in cortex/striatum and hippocampus/amygdala after systemic kainic acid administration. Neurochem Int. 36:2000;313-318.
11. Douglass J., Grimes L., Shook J., Lee P.H., Hong J.S. Systemic administration of kainic acid differentially regulates the levels of prodynorphin and proenkephalin mRNA and peptides in the rat hippocampus. Brain Res Mol Brain Res. 9:1991;79-86.
12. Du J., Koltzenburg M., Carlton S.M. Glutamate-induced excitation and sensitization of nociceptors in rat glabrous skin. Pain. 89:2001;187-198.
13. Eriksson C., Tehranian R., Iverfeldt K., Winblad B., Schultzberg M. Increased expression of mRNA encoding interleukin-1beta and caspase-1, and the secreted isoform of interleukin-1 receptor antagonist in the rat brain following systemic kainic acid administration. J Neurosci Res. 60:2000;266-279.
14. Ferrer I., Lopez E., Blanco R., Rivera R., Krupinski J., Marti E. Differential c-Fos and caspase expression following kainic acid excitotoxicity. Acta Neuropathol (Berl). 99:2000;245-256.
15. Fields H.L. Pain modulation: expectation, opioid analgesia and virtual pain. Prog Brain Res. 122:2000;245-253.
16. Gauriau C., Bernard J.F. Pain pathways and parabrachial circuits in the rat. Exp Physiol. 87:2002;251-258.
17. Gilron I., Max M.B., Lee G., Booher S.L., Sang C.N., Chappell A.S., Dionne R.A. Effects of the 2-amino-3-hydroxy-5-methyl-4-isoxazole-proprionic acid/kainate antagonist LY293558 on spontaneous and evoked postoperative pain. Clin Pharmacol Ther. 68:2000;320-327.
18. Giovengo S.L., Kitto K.F., Kurtz H.J., Velazquez R.A., Larson A.A. Parenterally administered kainic acid induces a persistent hyperalgesia in the mouse and rat. Pain. 83:1999;347-358.
19. Goutan E., Marti E., Ferrer I. BDNF, and full length and truncated TrkB expression in the hippocampus of the rat following kainic acid excitotoxic damage. Evidence of complex time-dependent and cell-specific responses. Brain Res Mol Brain Res. 59:1998;154-164.
20. Gray W.P., Sundstrom L.E. Kainic acid increases the proliferation of granule cell progenitors in the dentate gyrus of the adult rat. Brain Res. 790:1998;52-59.
21. Haas K.Z., Sperber E.F., Moshe S.L., Stanton P.K. Kainic acid-induced seizures enhance dentate gyrus inhibition by downregulation of GABA(B) receptors. J Neurosci. 16:1996;4250-4260.
22. Herbert H., Moga M.M., Saper C.B. Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J Comp Neurol. 293:1990;540-580.
23. Hunt S.P., Mantyh P.W. The molecular dynamics of pain control. Nat Rev Neurosci. 2:2001;83-91.
24. Hwang S.J., Pagliardini S., Rustioni A., Valtschanoff J.G. Presynaptic kainate receptors in primary afferents to the superficial laminae of the rat spinal cord. J Comp Neurol. 436:2001;275-289.
25. Jänig W., Khasar S.G., Levine J.D., Miao F.J. The role of vagal visceral afferents in the control of nociception. Prog Brain Res. 122:2000;273-287.
26. Jasmin L., Burkey A.R., Card J.P., Basbaum A.I. Transneuronal labeling of a nociceptive pathway, the spino-(trigemino-)parabrachio-amygdaloid, in the rat. J Neurosci. 17:1997;3751-3765.
27. Jasmin L., Gogas K.R., Ahlgren S.C., Levine J.D., Basbaum A.I. Walking evokes a distinctive pattern of Fos-like immunoreactivity in the caudal brainstem and spinal cord of the rat. Neuroscience. 58:1994;275-286.
28. Jasmin L., Tien D., Weinshenker D., Palmiter R.D., Green P.G., Janni G., Ohara P.T. The NK1 receptor mediates both the hyperalgesia and the resistance to morphine in mice lacking noradrenaline. Proc Natl Acad Sci USA. 99:2002;1029-1034.
29. Jasmin L., Wang H., Tarczy-Hornoch K., Levine J.D., Basbaum A.I. Differential effects of morphine on noxious stimulus-evoked fos-like immunoreactivity in subpopulations of spinoparabrachial neurons. J Neurosci. 14:1994;7252-7260.
30. Jensen T.S. Opioids in the brain: supraspinal mechanisms in pain control. Acta Anaesthesiol Scand. 41:1997;123-132.
31. Ji R.R., Baba H., Brenner G.J., Woolf C.J. Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat Neurosci. 2:1999;1114-1119.
32. Kerr J., Gobé G., Winterford C., Harmon B. Anatomical methods in cell death. Schwartz L., Osborne B. Cell Death. 1995;1-27 Academic Press, New York, NY. (L. Wilson and P. Matsudaira).
33. Khasar S.G., Miao J.P., Jänig W., Levine J.D. Modulation of bradykinin-induced mechanical hyperalgesia in the rat by activity in abdominal vagal afferents. Eur J Neurosci. 10:1998;435-444.
34. Kinkelin I., Brocker E.B., Koltzenburg M., Carlton S.M. Localization of ionotropic glutamate receptors in peripheral axons of human skin. Neurosci Lett. 283:2000;149-152.
35. Kitayama T., Ogita K., Yoneda Y. Sustained potentiation of AP1 DNA binding is not always associated with neuronal death following systemic administration of kainic acid in murine hippocampus. Neurochem Int. 35:1999;453-462.
36. Larson A.A., Giovengo S.L., Shi Q., Velazquez R.A., Kovacs K.J. Zinc in the extracellular area of the central nervous system is necessary for the development of kainic acid-induced persistent hyperalgesia in mice. Pain. 86:2000;177-184.
37. Lefauconnier J.M., Tayarani Y., Bernard G. Blood-brain barrier permeability to excitatory amino acids. Adv Exp Med Biol. 203:1986;191-198.
38. Lewis S.J., Cincotta M., Verberne A.J., Jarrott B., Lodge D., Beart P.M. Receptor autoradiography with [3H]L-glutamate reveals the presence and axonal transport of glutamate receptors in vagal afferent neurones of the rat. Eur J Pharmacol. 144:1987;413-415.
39. Lewis S.J., Verberne A.J., Louis C.J., Jarrott B., Beart P.M., Louis W.J. Excitotoxin-induced degeneration of rat vagal afferent neurons. Neuroscience. 34:1990;331-339.
40. Li P., Wilding T.J., Kim S.J., Calejesan A.A., Huettner J.E., Zhuo M. Kainate-receptor-mediated sensory synaptic transmission in mammalian spinal cord. Nature. 397:1999;161-164.
41. Loewy A. Central autonomic pathways. Loewy A., Spyer K. Central regulation of autonomic function. 1990;88-103 Oxford University Press, New York, NY.
42. McLean I.W., Nakane P.K. Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy. J Histochem Cytochem. 22:1974;1077-1083.
43. Miao F.J., Jänig W., Dallman M.F., Benowitz N.L., Heller P.H., Basbaum A.I., Levine J.D. Role of vagal afferents and spinal pathways modulating inhibition of bradykinin-induced plasma extravasation by intrathecal nicotine. J Neurophysiol. 72:1994;1199-1207.
44. Miao F.J., Jänig W., Jasmin L., Levine J.D. Spino-bulbo-spinal pathway mediating vagal modulation of nociceptive-neuroendocrine control of inflammation in the rat. J Physiol. 532:2001;811-822.
45. Michl T., Jocic M., Heinemann A., Schuligoi R., Holzer P. Vagal afferent signaling of a gastric mucosal acid insult to medullary, pontine, thalamic, hypothalamic and limbic, but not cortical, nuclei of the rat brain. Pain. 92:2001;19-27.
46. Molander C., Xu Q., Grant G. The cytoarchitectonic organization of the spinal cord in the rat. J Comp Neurol. 230:1984;133-141.
47. Norgren R. Projections from the nucleus of the solitary tract in the rat. Neuroscience. 3:1978;207-218.
48. Patel S., Meldrum B.S., Collins J.F. Distribution of [3H]kainic acid and binding sites in the rat brain: in vivo and in vitro receptor autoradiography. Neurosci Lett. 70:1986;301-307.
49. Paxinos G., Franklin K.B.J. The mouse brain in stereotaxic coordinates. 2001;Academic Press, New York, NY.
50. Pozas E., Ballabriga J., Planas A.M., Ferrer I. Kainic acid-induced excitotoxicity is associated with a complex c-Fos and c-Jun response which does not preclude either cell death or survival. J Neurobiol. 33:1997;232-246.
51. Randich A., Gebhart G.F. Vagal afferent modulation of nociception. Brain Res Rev. 17:1992;77-99.
52. Randich A., Robertson J.D., Willingham T. The use of specific opioid agonists and antagonists to delineate the vagally mediated antinociceptive and cardiovascular effects of intravenous morphine. Brain Res. 603:1993;186-200.
53. Ricardo J.A., Koh E.T. Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures in the rat. Brain Res. 153:1978;1-26.
54. Scarisbrick I.A., Isackson P.J., Windebank A.J. Differential expression of brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4/5 in the adult rat spinal cord: regulation by the glutamate receptor agonist kainic acid. J Neurosci. 19:1999;7757-7769.
55. Schreiber S.S., Najm I., Tocco G., Baudry M. Co-expression of HSP72 and c-fos in rat brain following kainic acid treatment. Neuroreport. 5:1993;269-272.
56. Schwob J.E., Fuller T., Price J.L., Olney J.W. Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: a histological study. Neuroscience. 5:1980;991-1014.
57. Simmons R.M., Li D.L., Hoo K.H., Deverill M., Ornstein P.L., Iyengar S. Kainate GluR5 receptor subtype mediates the nociceptive response to formalin in the rat. Neuropharmacology. 37:1998;25-36.
58. Ta L.E., Dionne R.A., Fricton J.R., Hodges J.S., Kajander K.C. SYM-2081 a kainate receptor antagonist reduces allodynia and hyperalgesia in a freeze injury model of neuropathic pain. Brain Res. 858:2000;106-120.
59. Ter Horst G.J., de Boer P., Luiten P.G., van Willigen J.D. Ascending projections from the solitary tract nucleus to the hypothalamus. A Phaseolus vulgaris lectin tracing study in the rat. Neuroscience. 31:1989;785-797.
60. Van Bockstaele E.J., Peoples J., Telegan P. Efferent projections of the nucleus of the solitary tract to peri-locus coeruleus dendrites in rat brain: evidence for a monosynaptic pathway. J Comp Neurol. 412:1999;410-428.
61. Watkins L.R., Wiertelak E.P., Goehler L.E., Mooney-Heiberger K., Martinez J., Furness L., Smith K.P., Maier S.F. Neurocircuitry of illness-induced hyperalgesia. Brain Res. 639:1994;283-299.
62. White K.P., Harth M. Classification, epidemiology, and natural history of fibromyalgia. Curr Pain Headache Rep. 5:2001;320-329.
63. Willoughby J.O., Mackenzie L., Medvedev A., Hiscock J.J. Fos induction following systemic kainic acid: early expression in hippocampus and later widespread expression correlated with seizure. Neuroscience. 77:1997;379-392.
64. Zhang J.W., Deb S., Gottschall P.E. Regional and differential expression of gelatinases in rat brain after systemic kainic acid or bicuculline administration. Eur J Neurosci. 10:1998;3358-3368.
65. Zhang W.Q., Rogers B.C., Tandon P., Hudson P.M., Sobotka T.J., Hong J.S., Tilson H.A. Systemic administration of kainic acid increases GABA levels in perfusate from the hippocampus of rats in vivo. Neurotoxicology. 11:1990;593-600.