Decreased Substance P and NK1 Receptor Immunoreactivity and Function in the Spinal Cord Dorsal Horn of Morphine-Treated Neonatal Rats

Journal of Pain

Volumn 9, Issue 1, 2008, Pages 11-19

  Thomson, Lisa M ^a   Terman, Gregory W ^a   Zeng, Jinsong ^a   Lowe, Janet ^a   Chavkin, Charles ^a   Hermes, Sam M ^b   Hegarty, Deborah M ^b   Aicher, Sue A ^b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

NK1 receptor; Opiate tolerance; spinal cord; substance P; whole cell voltage clamp

Indexed keywords

MORPHINE; NEUROKININ 1 RECEPTOR; SUBSTANCE P;

ANALGESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; EXCITATORY POSTSYNAPTIC POTENTIAL; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; NEWBORN; NONHUMAN; RAT; SPINAL CORD DORSAL HORN;

ANALGESICS, OPIOID; ANIMALS; ANIMALS, NEWBORN; DOWN-REGULATION; DRUG TOLERANCE; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; MORPHINE; NOCICEPTORS; ORGAN CULTURE TECHNIQUES; PAIN; PATCH-CLAMP TECHNIQUES; POSTERIOR HORN CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROKININ-1; RNA, MESSENGER; SUBSTANCE P;

EID: 37349048199     PISSN: 15265900     EISSN: 15288447     Source Type: Journal    
DOI: 10.1016/j.jpain.2007.07.008     Document Type: Article

References (47)

1. Abbadie C., Brown J.L., Mantyh P.W., and Basbaum A.I. Spinal cord substance P receptor immunoreactivity increases in both inflammatory and nerve injury models of persistent pain. Neuroscience 70 (1996) 201-209
2. Afrah A.W., Fiska A., Gjerstad J., Gustafsson H., Tjolsen A., Olgart L., Stiller C.O., Hole K., and Brodin E. Spinal substance P release in vivo during the induction of long-term potentiation in dorsal horn neurons. Pain 96 (2002) 49-55
3. Aosaki T., and Kawaguchi Y. Actions of substance P on rat neostriatal neurons in vitro. J Neurosci 16 (1996) 5141-5153
4. Belanger S., Ma W., Chabot J.G., and Quirion R. Expression of calcitonin gene-related peptide, substance P and protein kinase C in cultured dorsal root ganglion neurons following chronic exposure to mu, delta and kappa opiates. Neuroscience 115 (2002) 441-453
5. Berger A.J., and Takahashi T. Serotonin enhances a low-voltage-activated calcium current in rat spinal motoneurons. J Neurosci 10 (1990) 1922-1928
6. Besson J.M., and Chaouch A. Peripheral and spinal mechanisms of nociception. Physiol Rev 67 (1987) 67-186
7. Cahill C.M., and Coderre T.J. Attenuation of hyperalgesia in a rat model of neuropathic pain after intrathecal pre- or post-treatment with a neurokinin-1 antagonist. Pain 95 (2002) 277-285
8. Cao Y.Q., Mantyh P.W., Carlson E.J., Gillespie A.M., Epstein C.J., and Basbaum A.I. Primary afferent tachykinins are required to experience moderate to intense pain. Nature 392 (1998) 390-394
9. De Biasi S., and Rustioni A. Glutamate and substance P coexist in primary afferent terminals in the superficial laminae of spinal cord. Proc Natl Acad Sci U S A 85 (1988) 7820-7824
10. Gainetdinov R.R., Premont R.T., Bohn L.M., Lefkowitz R.J., and Caron M.G. Desensitization of G protein-coupled receptors and neuronal functions. Annu Rev Neurosci 27 (2004) 107-144
11. Gibbs L.M., and Kendig J.J. Substance P and NMDA receptor-mediated slow potentials in neonatal rat spinal cord: Age-related changes. Brain Res 595 (1992) 236-241
12. Ho R.H. Widespread distribution of substance P- and somatostatin-immunoreactive elements in the spinal cord of the neonatal rat. Cell Tissue Res 232 (1983) 471-486
13. Honore P., Kamp E.H., Rogers S.D., Gebhart G.F., and Mantyh P.W. Activation of lamina I spinal cord neurons that express the substance P receptor in visceral nociception and hyperalgesia. J Pain 3 (2002) 3-11
14. Honore P., Rogers S.D., Schwei M.J., Salak-Johnson J.L., Luger N.M., Sabino M.C., Clohisy D.R., and Mantyh P.W. Murine models of inflammatory, neuropathic and cancer pain each generates a unique set of neurochemical changes in the spinal cord and sensory neurons. Neuroscience 98 (2000) 585-598
15. Hsu M.M., and Wong C.S. The roles of pain facilitatory systems in opioid tolerance. Acta Anaesthesiol Sin 38 (2000) 155-166
16. Hua X.Y., Chen P., Polgar E., Nagy I., Marsala M., Phillips E., Wollaston L., Urban L., Yaksh T.L., and Webb M. Spinal neurokinin NK1 receptor downregulation and antinociception: Effects of spinal NK1 receptor antisense oligonucleotides and NK1 receptor occupancy. J Neurochem 70 (1998) 688-698
17. Ishigooka M., Zermann D.H., Doggweiler R., Schmidt R.A., Hashimoto T., and Nakada T. Spinal NK1 receptor is upregulated after chronic bladder irritation. Pain 93 (2001) 43-50
18. Jang J.H., Nam T.S., Paik K.S., and Leem J.W. Involvement of peripherally released substance P and calcitonin gene-related peptide in mediating mechanical hyperalgesia in a traumatic neuropathy model of the rat. Neurosci Lett 360 (2004) 129-132
19. Khasabov S.G., Rogers S.D., Ghilardi J.R., Peters C.M., Mantyh P.W., and Simone D.A. Spinal neurons that possess the substance P receptor are required for the development of central sensitization. J Neurosci 22 (2002) 9086-9098
20. King T., Gardell L.R., Wang R., Vardanyan A., Ossipov M.H., Malan Jr. T.P., Vanderah T.W., Hunt S.P., Hruby V.J., Lai J., and Porreca F. Role of NK-1 neurotransmission in opioid-induced hyperalgesia. Pain 116 (2005) 276-288
21. King T., Ossipov M.H., Vanderah T.W., Porreca F., and Lai J. Is paradoxical pain induced by sustained opioid exposure an underlying mechanism of opioid antinociceptive tolerance?. Neurosignals 14 (2005) 194-205
22. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (2001) 402-408
23. Ma W., Zheng W.H., Kar S., and Quirion R. Morphine treatment induced calcitonin gene-related peptide and substance P increases in cultured dorsal root ganglion neurons. Neuroscience 99 (2000) 529-539
24. Mansikka H., Sheth R.N., DeVries C., Lee H., Winchurch R., and Raja S.N. Nerve injury-induced mechanical but not thermal hyperalgesia is attenuated in neurokinin-1 receptor knockout mice. Exp Neurol 162 (2000) 343-349
25. Mao J., Price D.D., and Mayer D.J. Mechanisms of hyperalgesia and morphine tolerance: A current view of their possible interactions. Pain 62 (1995) 259-274
26. Mao J., Sung B., Ji R.R., and Lim G. Chronic morphine induces downregulation of spinal glutamate transporters: Implications in morphine tolerance and abnormal pain sensitivity. J Neurosci 22 (2002) 8312-8323
27. Meert T.F., Vissers K., Geenen F., and Kontinen V.K. Functional role of exogenous administration of substance P in chronic constriction injury model of neuropathic pain in gerbils. Pharmacol Biochem Behav 76 (2003) 17-25
28. Murase K., Ryu P.D., and Randic M. Tachykinins modulate multiple ionic conductances in voltage-clamped rat spinal dorsal horn neurons. J Neurophysiol 61 (1989) 854-865
29. Nichols M.L., Allen B.J., Rogers S.D., Ghilardi J.R., Honore P., Luger N.M., Finke M.P., Li J., Lappi D.A., Simone D.A., and Mantyh P.W. Transmission of chronic nociception by spinal neurons expressing the substance P receptor. Science 286 (1999) 1558-1561
30. Ohtori S., Takahashi K., Ino H., Chiba T., Yamagata M., Sameda H., and Moriya H. Upregulation of substance P and NMDA receptor mRNA in dorsal horn and preganglionic sympathetic neurons during adjuvant-induced noxious stimulation in rats. Ann Anat 184 (2002) 71-76
31. Ossipov M.H., Lai J., King T., Vanderah T.W., and Porreca F. Underlying mechanisms of pronociceptive consequences of prolonged morphine exposure. Biopolymers 80 (2005) 319-324
32. Palecek J., Paleckova V., and Willis W.D. Postsynaptic dorsal column neurons express NK1 receptors following colon inflammation. Neuroscience 116 (2003) 565-572
33. Pitcher G.M., and Henry J.L. Nociceptive response to innocuous mechanical stimulation is mediated via myelinated afferents and NK-1 receptor activation in a rat model of neuropathic pain. Exp Neurol 186 (2004) 173-197
34. Powell K.J., Quirion R., and Jhamandas K. Inhibition of neurokinin-1-substance P receptor and prostanoid activity prevents and reverses the development of morphine tolerance in vivo and the morphine-induced increase in CGRP expression in cultured dorsal root ganglion neurons. Eur J Neurosci 18 (2003) 1572-1583
35. Robertson B., Schulte G., Elde R., and Grant G. Effects of sciatic nerve injuries on delta -opioid receptor and substance P immunoreactivities in the superficial dorsal horn of the rat. Eur J Pain 3 (1999) 115-129
36. Ruscheweyh R., and Sandkuhler J. Opioids and central sensitization, II: induction and reversal of hyperalgesia. Eur J Pain 9 (2005) 149-152
37. Schaible H.G., Jarrott B., Hope P.J., and Duggan A.W. Release of immunoreactive substance P in the spinal cord during development of acute arthritis in the knee joint of the cat: a study with antibody microprobes. Brain Res 529 (1990) 214-223
38. Shimoyama M., Tatsuoka H., Ohtori S., Tanaka K., and Shimoyama N. Change of dorsal horn neurochemistry in a mouse model of neuropathic cancer pain. Pain 114 (2005) 221-230
39. Sluka K.A., and Westlund K.N. Behavioral and immunohistochemical changes in an experimental arthritis model in rats. Pain 55 (1993) 367-777
40. Taylor B.K. Insights into morphine-induced plasticity and spinal tolerance. Pain 114 (2005) 1-2
41. Taylor B.K., and McCarson K.E. Neurokinin-1 receptor gene expression in the mouse dorsal horn increases with neuropathic pain. J Pain 5 (2004) 71-76
42. Terman G.W., Eastman C.L., and Chavkin C. Mu opiates inhibit long-term potentiation induction in the spinal cord slice. J Neurophysiol 85 (2001) 485-494
43. Thomson L.M., Zeng J., and Terman G.W. Differential effect of glutamate transporter inhibition on EPSCs in the morphine naive and morphine tolerant neonatal spinal cord slice. Neurosci Lett 407 (2006) 64-69
44. Vachon P., Masse R., and Gibbs B.F. Substance P and neurotensin are upregulated in the lumbar spinal cord of animals with neuropathic pain. Can J Vet Res 68 (2004) 86-92
45. Weng H.R., Mansikka H., Winchurch R., Raja S.N., and Dougherty P.M. Sensory processing in the deep spinal dorsal horn of neurokinin-1 receptor knockout mice. Anesthesiology 94 (2001) 1105-1112
46. Wu Z.Z., Guan B.C., Li Z.W., Yang Q., Liu C.J., and Chen J.G. Sustained potentiation by substance P of NMDA-activated current in rat primary sensory neurons. Brain Res 1010 (2004) 117-126
47. Zeng J., Thomson L.M., Aicher S.A., and Terman G.W. Primary afferent NMDA receptors increase dorsal horn excitation and mediate opiate tolerance in neonatal rats. J Neurosci 26 (2006) 12033-12042