Effect of peptidases on the ability of exogenous and endogenous neurokinins to produce neurokinin 1 receptor internalization in the rat spinal cord

British Journal of Pharmacology

Volumn 140, Issue 8, 2003, Pages 1389-1398

  Marvizón, Juan Carlos G ^a,b   Wang, Xueren ^a,c   Lao, Li Ju ^a   Song, Bingbing ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Aminopeptidase; C fiber; Dipeptidyl carboxypeptidase; Dorsal horn; EC 3.4.15.1; EC 3.4.24.11; Neurokinin; Neurokinin 1 receptor; Neutral endopeptidase; Primary afferent; Substance P; Tachykinin

Indexed keywords

ACTINONIN; AMASTATIN; AMINOPEPTIDASE INHIBITOR; BACITRACIN; BESTATIN; CAPTOPRIL; DIPEPTIDYL CARBOXYPEPTIDASE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; ENZYME INHIBITOR; MEMBRANE METALLOENDOPEPTIDASE; NEUROKININ; NEUROKININ 1 RECEPTOR; NEUROKININ A; NEUROKININ B; PEPTIDASE; PUROMYCIN; SUBSTANCE P; THIORPHAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DORSAL ROOT; DRUG ACTIVITY; DRUG EFFECT; DRUG MECHANISM; ELECTROSTIMULATION; ENZYME ACTIVITY; ENZYME ANALYSIS; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SENSORY NERVE; SPINAL CORD;

AMINOPEPTIDASES; ANIMALS; ELECTRIC STIMULATION; ENZYME INHIBITORS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; NEUROKININ A; NEUROKININ B; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROKININ-1; SPINAL CORD; SPINAL NERVE ROOTS; SUBSTANCE P;

EID: 0346688591     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0705578     Document Type: Article

References (62)

1. ABBADIE, C., TRAFTON, J., LIU, H., MANTYH, P.W. & BASBAUM, A.I. (1997). Inflammation increases the distribution of dorsal horn neurons that internalize the neurokinin-1 receptor in response to noxious and non-noxious stimulation. J. Neurosci., 17, 8049-8060.
2. ALLEN, B.J., ROGERS, S.D., GHILARDI, J.R., MENNING, P.M., KUSKOWSKI, M.A., BASBAUM, A.I., SIMONE, D.A. & MANTYH, P.W. (1997). Noxious cutaneous thermal stimuli induce a graded release of endogenous substance P in the spinal cord: imaging peptide action in vivo. J. Neurosci., 17, 5921-5927.
3. BLEAZARD, L., HILL, R.G. & MORRIS, R. (1994). The correlation between the distribution of the NK1 receptor and the actions of tachykinins agonists in the dorsal horn of the rat indicates that substance P does not have a functional role on substantia gelatinosa (lamina II) neurons. J. Neurosci., 14, 7655-7664.
4. BURLEY, S.K., DAVID, P.R. & LIPSCOMB, W.N. (1991). Leucine aminopeptidase: bestatin inhibition and a model for enzyme-catalyzed peptide hydrolysis. Proc. Natl. Acad. Sci. U.S.A., 88, 6916-6920.
5. CAO, Y.Q., MANTYH, P.W., CARLSON, E.J., GILLESPIE, A.M., EPSTEIN, C.J. & BASBAUM, A.I. (1998). Primary afferent tachykinins are required to experience moderate to intense pain. Nature, 392, 390-394.
6. CHEN, J.J., BARBER, L.A., DYMSHITZ, J. & VASKO, M.R. (1996). Peptidase inhibitors improve recovery of substance P and calcitonin gene-related peptide release from rat spinal cord slices. Peptides, 17, 31-37.
7. CHOU, J., TANG, J., DEL RIO, J., YANG, H.Y. & COSTA, E. (1984). Action of peptidase inhibitors on methionine5-enkephalin-arginine6- phenylalanine7 (YGGFMRF) and methionine5-enkephalin (YGGFM) metabolism and on electroacupuncture antinociception. J. Pharmacol. Exp. Ther., 230, 349-352.
8. DE FELIPE, C., HERRERO, J.F., O'BRIEN, J.A., PALMER, J.A., DOYLE, C.A., SMITH, A.J., LAIRD, J.M., BELMONTE, C., CERVERO, F. & HUNT, S.P. (1998). Altered nociception, analgesia and aggression in mice lacking the receptor for substance P. Nature, 392, 394-397.
9. DEVILLIER, P., ADVENIER, C., DRAPEAU, G., MARSAC, J. & REGOLI, D. (1988). Comparison of the effects of epithelium removal and of an enkephalinase inhibitor on the neurokinin-induced contractions of guinea-pig isolated trachea. Br. J. Pharmacol., 94, 675-684.
10. DUGGAN, A.W., SCHAIBLE, H.-G., HOPE, P.J. & LANG, C.W. (1992). Effect of peptidase inhibition on the pattern of intraspinally released immunoreactive substance P detected with antibody microprobes. Brain Res., 579, 261-269.
11. GEPPETTI, P., SANTICIOLI, P., RUBINI, I., SPILLANTINI, M.G., MAGGI, C.A. & SICUTERI, F. (1989). Thiorphan increases capsaicin-evoked release of substance P from slices of dorsal spinal cord of guinea pig. Neurosci. Lett., 103, 69-73.
12. GO, V.L.W. & YAKSH, T.L. (1987). Release of substance P from the cat spinal cord. J. Physiol., 391, 141-167.
13. GRADY, E.F., BALUK, P., BOHM, S., GAMP, P.D., WONG, H., PAYAN, D.G., ANSEL, J., PORTBURY, A.L., FURNESS, J.B., MCDONALD, D.M. & BUNNETT, N.W. (1996). Characterization of antisera specific to NK1, NK2, and NK3 neurokinin receptors and their utilization to localize receptors in the rat gastrointestinal tract. J. Neurosci., 16, 6975-6986.
14. GUYON, A., ROQUES, B.P., GUYON, F., FOUCAULT, A., PERDRISOT, R., SWERTS, J.P. & SCHWARTZ, J.C. (1979). Enkephalin degradation in mouse brain studied by a new H.P.L.C. method: further evidence for the involvement of carboxydipeptidase. Life Sci., 25, 1605-1611.
15. HARBECK, H.T. & MENTLEIN, R. (1991). Aminopeptidase P from rat brain. Purification and action on bioactive peptides. Eur. J. Biochem., 198, 451-458.
16. HENRY, J.L., YASHPAL, K., PITCHER, G.M., CHABOT, J. & CODERRE, T.J. (1999). Evidence for tonic activation of NK-1 receptors during the second phase of the formalin test in the rat. J. Neurosci., 19, 6588-6598.
17. HIRANUMA, T., KITAMURA, K., TANIGUCHI, T., KOBAYASHI, T., TAMAKI, R., KANAI, M., AKAHORI, K., IWAO, K. & OKA, T. (1998). Effects of three peptidase inhibitors, amastatin, captopril and phosphoramidon, on the hydrolysis of [Met5]-enkephalin-Arg6-Phe7 and other opioid peptides. Naunyn-Schmiedeberg's Arch. Pharmacol., 357, 276-282.
18. HONORE, P., MENNING, P.M., ROGERS, S.D., NICHOLS, M.L., BASBAUM, A.I., BESSON, J.M. & MANTYH, P.W. (1999). Spinal cord substance P receptor expression and internalization in acute, short-term, and long-term inflammatory pain states. J. Neurosci., 19, 7670-7678.
19. KOSLOW, M., BAK, A. & LI, C.L. (1973). C-fiber excitability in the cat. Exp. Neurol., 41, 745-753.
20. LAIRD, J.M., OLIVAR, T., ROZA, C., DE FELIPE, C., HUNT, S.P. & CERVERO, F. (2000). Deficits in visceral pain and hyperalgesia of mice with a disruption of the tachykinin NK1 receptor gene. Neuroscience, 98, 345-352.
21. LAIRD, J.M., ROZA, C., DE FELIPE, C., HUNT, S.P. & CERVERO, F. (2001). Role of central and peripheral tachykinin NK1 receptors in capsaicin-induced pain and hyperalgesia in mice. Pain, 90, 97-103.
22. LEVER, I.J. & MALCANGIO, M. (2002). CB(1) receptor antagonist SR141716A increases capsaicin-evoked release of substance P from the adult mouse spinal cord. Br. J. Pharmacol., 135, 21-24.
23. LI, C.L. & BAK, A. (1976). Excitability characteristics of the A-and C-fibers in a peripheral nerve. Exp. Neurol., 50, 67-79.
24. LIU, H., BROWN, JL., JASMIN, L., MAGGIO, J.E., VIGNA, S.R., MANTYH, P.W. & BASBAUM, A.I. (1994). Synaptic relationship between substance P and the substance P receptor: light and electron microscopic characterization of the mismatch between neuropeptides and their receptors. Proc. NatL. Acad. Sci. U.S.A., 91, 1009-1013.
25. LIU, H., MANTYH, P.W. & BASBAUM, A.I. (1997). NMDA-receptor regulation of substance P release from primary afferent nociceptors. Nature, 386, 721-724.
26. 1 receptor. Trends Pharmacol. Sci., 18, 351-355.
27. B, but not gamma-aminobutyric acidA receptor activation, inhibits electrically evoked substance P-like immunoreactivity release from the rat spinal cord in vitro. J. Pharmacol. Exp. Ther., 266, 1490-1496.
28. MALCANGIO, M. & BOWERY, N.G. (1994). Effect of the tachykinin NK1 receptor antagonists, RP 67580 and SR 140333, on electrically-evoked substance P release from rat spinal cord. Br. J. Pharmacol., 113, 635-641.
29. MALCANGIO, M., GARRETT, N.E., CRUWYS, S. & TOMLINSON, D.R. (1997). Nerve growth factor-and neurotrophin-3-induced changes in nociceptive threshold and the release of substance P from the rat isolated spinal cord. J. Neurosci., 17, 8459-8467.
30. MANTYH, P.W., DEMASTER, E., MALHOTRA, A., GHILARDI, J.R., ROGERS, S.D., MANTYH, C.R., LIU, H., BASBAUM, A.I., VIGNA, S.R. & MAGGIO, J.E. (1995). Receptor endocytosis and dendrite reshaping in spinal neurons after somatosensory stimulation. Science, 268, 1629-1632.
31. MANTYH, P.W., ROGERS, S.D., HONORE, P., ALLEN, B.J., GHILARDI, J.R., LI, J., DAUGHTERS, R.S., LAPPI, D.A., WILEY, R.G. & SIMONE, D.A. (1997). Inhibition of hyperalgesia by ablation of lamina 1 spinal neurons expressing the substance P receptor. Science, 278, 275-279.
32. MARTLING, C.R., THEODORSSON-NORHEIM, E., NORHEIM, I. & LUNDBERG, J.M. (1987). Bronchoconstrictor and hypotensive effects in relation to pharmacokinetics of tachykinins in the guinea-pig - evidence for extraneuronal cleavage of neuropeptide K to neurokinin A. Naunyn-Schmiedeberg's Arch. Pharmacol., 336, 183-189.
33. MARVIZON, J.C., GRADY, E.F., STEFANI, E., BUNNETT, N.W. & MAYER, E.A. (1999a). Substance P release in the dorsal horn assessed by receptor internalization: NMDA receptors counteract a tonic inhibition by GABA(B) receptors. Eur. J. Neurosci., 11, 417-426.
34. MARVIZON, J.C., MARTINEZ, V., GRADY, E.F., BUNNETT, N.W. & MAYER, E.A. (1997). Neurokinin 1 receptor internalization in spinal cord slices induced by dorsal root stimulation is mediated by NMDA receptors. J. Neurosci., 17, 8129-8136.
35. MARVIZON, J.C., WANG, X., MATSUKA, Y., NEUBERT, J.K. & SPIGELMAN, I. (2003). Relationship between capsaicin-evoked substance P release and NK1 receptor internalization in the rat dorsal horn. Neuroscience, 118, 535-545.
36. MARVIZON, J.C.G., GRADY, E.F., WAZSAK-MCGEE, J. & MAYER, E.A. (1999b). Internalization of μ-opioid receptors in rat spinal cord slices. Neuro Report, 10, 2329-2334.
37. MAUBORGNE, A., BOURGOIN, S., BENOLIEL, J.J., HAMON, M. & CESSELIN, F. (1991). Is substance-P released from slices of the rat spinal-cord inactivated by peptidase(s) distinct from both enkephalinase and angiotensin-converting enzyme. Neurosci. Lett., 123, 221-225.
38. MOTULSKY, H. & CHRISTOPOULOS, A. (2003). Fitting Models to Biological Data Using Linear and Nonlinear Regression. San Diego, CA: GraphPad Software, Inc..
39. NOBLE, F., CORIC, P., FOURNIE-ZALUSKI, M.C. & ROQUES, B.P. (1992a). Lack of physical dependence in mice after repeated systemic administration of the mixed inhibitor prodrug of enkephalin-degrading enzymes, RB101. Eur. J. Pharmacol., 223, 91-96.
40. NOBLE, F., SOLEILHAC, J.M., SOROCA-LUCAS, E., TURCAUD, S., FOURNIE-ZALUSKI, M.C. & ROQUES, B.P. (1992b). Inhibition of the enkephalin-metabolizing enzymes by the first systemically active mixed inhibitor prodrug RB 101 induces potent analgesic responses in mice and rats. J. Pharmacol. Exp. Ther., 261, 181-190.
41. NOBLE, F., TURCAUD, S., FOURNIE-ZALUSKI, M.C. & ROQUES, B.P. (1992c). Repeated systemic administration of the mixed inhibitor of enkephalin- degrading enzymes, RB101, does not induce either antinociceptive tolerance or cross-tolerance with morphine. Eur. J. Pharmacol., 223, 83-89.
42. 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.
43. REGOLI, D., DRAPEAU, G., DION, S. & COUTURE, R. (1994). Receptors and antagonists for substance P and related peptides. Pharmacol. Rev., 46, 551-599.
44. RILEY, R.C., TRAFTON, J.A., CHI, S.I. & BASBAUM, A.I. (2001). Presynaptic regulation of spinal cord tachykinin signaling via GABA(B) but not GABA(A) receptor activation. Neuroscience, 103, 725-737.
45. ROQUES, B.P. (2000). Novel approaches to targeting neuropeptide systems. Trends Pharmacol. Sci., 21, 475-483.
46. ROUTH, V.H. & HELKE, C.J. (1995). Tachykinin receptors in the spinal cord. Prog. Brain Res., 104, 93-108.
47. SAKURADA, T., TAN-NO, K., YAMADA, T., SAKURADA, S. & KISARA, K. (1990). Phosphoramidon potentiates mammalian tachykinin-induced biting, licking and scratching behaviour in mice. Pharmacol. Biochem. Behav., 37, 779-783.
48. SANDKUHLER, J., CHEN, J.G., CHENG, G. & RANDIC, M. (1997). Low-frequency stimulation of afferent Aδ-fibers induces long-term depression at primary afferent synapses with substantia gelatinosa neurons in the rat. J. Neurosci., 17, 6483-6491.
49. SCHWEI, M.J., HONORE, P., ROGERS, S.D., SALAK-JOHNSON, J.L., FINKE, M.P., RAMNARAINE, M.L., CLOHISY, D.R. & MANTYH, P.W. (1999). Neurochemical and cellular reorganization of the spinal cord in a murine model of bone cancer pain. J. Neurosci., 19, 10886-10897.
50. SONG, B. & MARVIZON, J.C. (2003). Peptidases prevent μ-opioid receptor internalization in dorsal horn neurons by endogenously released opioids. J. Neurosci., 23, 1847-1858.
51. SUZUKI, H., YANAGISAWA, M., YOSHIOKA, K., HOSOKI, R. & OTSUKA, M. (1997). Enzymatic inactivation of enkephalin neurotransmitters in the spinal cord of the neonatal rat. Neurosci. Res., 28, 261-267.
52. SUZUKI, H., YOSHIOKA, K., YANAGISAWA, M., URAYAMA, O., KURIHARA, T., HOSOKI, R., SAITO, K. & OTSUKA, M. (1994). Involvement of enzymatic degradation in the inactivation of tachykinin neurotransmitters in neonatal rat spinal cord. Br. J. Pharmacol., 113, 310-316.
53. TIEKU, S. & HOOPER, N.M. (1992). Inhibition of aminopeptidases N, A and W. A re-evaluation of the actions of bestatin and inhibitors of angiotensin converting enzyme. Biochem. Pharmacol., 44, 1725-1730.
54. TODD, A.J., PUSKAR, Z., SPIKE, R.C., HUGHES, C., WATT, C. & FORREST, L. (2002). Projection neurons in lamina I of rat spinal cord with the neurokinin 1 receptor are selectively innervated by substance p-containing afferents and respond to noxious stimulation. J. Neurosci., 22, 4103-4113.
55. TRAFTON, J.A., ABBADIE, C. & BASBAUM, A.I. (2001). Differential contribution of substance P and neurokinin A to spinal cord neurokinin-1 receptor signaling in the rat. J. Neurosci., 21, 3656-3664.
56. TRAFTON, J.A., ABBADIE, C., MARCHAND, S., MANTYH, P.W. & BASBAUM, A.I. (1999). Spinal opioid analgesia: how critical is the regulation of substance P signaling? J. Neurosci., 19, 9642-9653.
57. TRAFTON, J.A., ABBADIE, C., MAREK, K. & BASBAUM, A.I. (2000). Postsynaptic signaling via the mu-opioid receptor: responses of dorsal horn neurons to exogenous opioids and noxious stimulation. J. Neurosci., 20, 8578-8584.
58. TRAUB, R.J. (1996). The spinal contribution of substance P to the generation and maintenance of inflammatory hyperalgesia in the rat. Pain, 67, 151-161.
59. WANG, X. & MARVIZON, J.C. (2002). Time-course of the internalization and recycling of neurokinin 1 receptors in rat dorsal horn neurons. Brain Res., 944, 239-247.
60. YAKSH, T.L. & CHIPKIN, R.E. (1989). Studies on the effect of SCH-34826 and thiorphan on [Met5]enkephalin levels and release in rat spinal cord. Eur. J. Pharmacol., 167, 367-373.
61. YOSHIMURA, M. & JESSELL, T. (1990). Amino acid-mediated EPSPs at primary afferent synapses with substantia gelatinosa neurones in the rat spinal cord. J. Physiol., 430, 315-335.
62. YOSHIMURA, M. & NISHI, S. (1996). Blind patch-clamp recordings from substantia gelatinosa neurons in adult rat spinal cord slices: pharmacological properties of synaptic currents. Neuroscience, 53, 519-526.