Neuropeptide Y in the rostral ventromedial medulla reverses inflammatory and nerve injury hyperalgesia in rats via non-selective excitation of local neurons

Neuroscience

Volumn 271, Issue , 2014, Pages 149-159

  Cleary, D R ^a   Roeder, Z ^a   Elkhatib, R ^a,b   Heinricher, M M ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b CAIRO UNIVERSITY   (Egypt)

Author keywords

Descending pain modulation; Nociception; NPY; OFF cells; ON cells; Raphe magnus

Indexed keywords

NEUROPEPTIDE Y; NEUROPEPTIDE Y1 RECEPTOR; ANALGESIC AGENT; FREUND ADJUVANT; NEUROPEPTIDE Y RECEPTOR; NEUROPEPTIDE Y-Y1 RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; BRAIN REGION; CELL ACTIVATION; CELL ACTIVITY; CHRONIC INFLAMMATION; CONTROLLED STUDY; EVOKED RESPONSE; HYPERALGESIA; HYPERSENSITIVITY; HYPOALGESIA; MALE; NERVE CELL STIMULATION; NERVE INJURY; NONHUMAN; PRIORITY JOURNAL; RAT; ROSTRAL VENTROMEDIAL MEDULLA; SEROTONINERGIC NERVE CELL; ACTION POTENTIAL; ANIMAL; DOSE RESPONSE; DRUG EFFECTS; HEAT; INFLAMMATION; MEDULLA OBLONGATA; METABOLISM; NERVE CELL; NERVE CELL INHIBITION; NOCICEPTIVE PAIN; PAIN THRESHOLD; PATHOPHYSIOLOGY; PHYSIOLOGY; SPINAL NERVE; SPRAGUE DAWLEY RAT; TOUCH;

ACTION POTENTIALS; ANALGESICS; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; FREUND'S ADJUVANT; HOT TEMPERATURE; HYPERALGESIA; INFLAMMATION; MALE; MEDULLA OBLONGATA; NEURAL INHIBITION; NEURONS; NEUROPEPTIDE Y; NOCICEPTIVE PAIN; PAIN THRESHOLD; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROPEPTIDE Y; SEROTONERGIC NEURONS; SPINAL NERVES; TOUCH;

EID: 84900826990     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.04.035     Document Type: Article

References (59)

1. Abounader R., Hamel E. Associations between neuropeptide Y nerve terminals and intraparenchymal microvessels in rat and human cerebral cortex. J Comp Neurol 1997, 388:444-453.
2. Bee L.A., Dickenson A.H. Rostral ventromedial medulla control of spinal sensory processing in normal and pathophysiological states. Neuroscience 2007, 147:786-793.
3. Burgess S.E., Gardell L.R., Ossipov M.H., Malan T.P., Vanderah T.W., Lai J., Porreca F. Time-dependent descending facilitation from the rostral ventromedial medulla maintains, but does not initiate, neuropathic pain. J Neurosci 2002, 22:5129-5136.
4. Carlson J.D., Maire J.J., Martenson M.E., Heinricher M.M. Sensitization of pain-modulating neurons in the rostral ventromedial medulla after peripheral nerve injury. J Neurosci 2007, 27:13222-13231.
5. Cauli B., Tong X.K., Rancillac A., Serluca N., Lambolez B., Rossier J., Hamel E. Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J Neurosci 2004, 24:8940-8949.
6. Chen Q., King T., Vanderah T.W., Ossipov M.H., Malan T.P., Lai J., Porreca F. Differential blockade of nerve injury-induced thermal and tactile hypersensitivity by systemically administered brain-penetrating and peripherally restricted local anesthetics. J Pain 2004, 5:281-289.
7. Cleary D.R., Heinricher M.M. Adaptations in responsiveness of brainstem pain-modulating neurons in acute compared with chronic inflammation. Pain 2013, 154:845-855.
8. Cleland C.L., Lim F.Y., Gebhart G.F. Pentobarbital prevents the development of C-fiber-induced hyperalgesia in the rat. Pain 1994, 57:31-43.
9. Da Silva L.F., Desantana J.M., Sluka K.A. Activation of NMDA receptors in the brainstem, rostral ventromedial medulla, and nucleus reticularis gigantocellularis mediates mechanical hyperalgesia produced by repeated intramuscular injections of acidic saline in rats. J Pain 2010, 11:378-387.
10. Da Silva L.F., Walder R.Y., Davidson B.L., Wilson S.P., Sluka K.A. Changes in expression of NMDA-NR1 receptor subunits in the rostral ventromedial medulla modulate pain behaviors. Pain 2010, 151:155-161.
11. Dacey R.G., Bassett J.E., Takayasu M. Vasomotor responses of rat intracerebral arterioles to vasoactive intestinal peptide, substance P, neuropeptide Y, and bradykinin. J Cereb Blood Flow Metab 1988, 8:254-261.
12. De Felice M., Sanoja R., Wang R., Vera-Portocarrero L., Oyarzo J., King T., Ossipov M.H., Vanderah T.W., Lai J., Dussor G.O., Fields H.L., Price T.J., Porreca F. Engagement of descending inhibition from the rostral ventromedial medulla protects against chronic neuropathic pain. Pain 2011, 152:2701-2709.
13. Dias M.B., Li A., Nattie E. Focal CO2 dialysis in raphe obscurus does not stimulate ventilation but enhances the response to focal CO2 dialysis in the retrotrapezoid nucleus. J Appl Physiol 2008, 105:83-90.
14. Fields H.L., Heinricher M.M. Anatomy and physiology of a nociceptive modulatory system. Philos Trans R Soc Lond B Biol Sci 1985, 308:361-374.
15. Fields H.L., Bry J., Hentall I., Zorman G. The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heat. J Neurosci 1983, 3:2545-2552.
16. Gau R., Sevoz-Couche C., Hamon M., Bernard J.F. Noxious stimulation excites serotonergic neurons: a comparison between the lateral paragigantocellular reticular and the raphe magnus nuclei. Pain 2013, 154:647-659.
17. Gonçalves L., Almeida A., Pertovaara A. Pronociceptive changes in response properties of rostroventromedial medullary neurons in a rat model of peripheral neuropathy. Eur J Neurosci 2007, 26:2188-2195.
18. Guan Y., Terayama R., Dubner R., Ren K. Plasticity in excitatory amino acid receptor-mediated descending pain modulation after inflammation. J Pharmacol Exp Ther 2002, 300:513-520.
19. Hamity M.V., White S.R., Hammond D.L. Effects of neurokinin-1 receptor agonism and antagonism in the rostral ventromedial medulla of rats with acute or persistent inflammatory nociception. Neuroscience 2010, 165:902-913.
20. Heinricher M.M., Fields H.L. Central nervous system mechanisms of pain modulation. Wall & Melzack's textbook of pain 2013, 129-142. Elsevier, London. 6th ed. S. McMahon, M. Koltzenburg, I. Tracey, D. Turk (Eds.).
21. Heinricher M.M., Ingram S.L. The brainstem and nociceptive modulation. The senses, a comprehensive reference 2008, vol. 5:593-626. Academic Press, San Diego.
22. Heinricher M.M., Neubert M.J. Neural basis for the hyperalgesic action of cholecystokinin in the rostral ventromedial medulla. J Neurophysiol 2004, 92:1982-1989.
23. Heinricher M.M., Barbaro N.M., Fields H.L. Putative nociceptive modulating neurons in the rostral ventromedial medulla of the rat: firing of on- and off-cells is related to nociceptive responsiveness. Somatosens Mot Res 1989, 6:427-439.
24. Heinricher M.M., Haws C.M., Fields H.L. Evidence for GABA-mediated control of putative nociceptive modulating neurons in the rostral ventromedial medulla: iontophoresis of bicuculline eliminates the off-cell pause. Somatosens Mot Res 1991, 8:215-225.
25. Heinricher M.M., Morgan M.M., Tortorici V., Fields H.L. Disinhibition of off-cells and antinociception produced by an opioid action within the rostral ventromedial medulla. Neuroscience 1994, 63:279-288.
26. Heinricher M.M., Tavares I., Leith J.L., Lumb B.M. Descending control of nociception: specificity, recruitment and plasticity. Brain Res Rev 2009, 60:214-225.
27. Heinricher M.M., Maire J.J., Lee D., Nalwalk J.W., Hough L.B. Physiological basis for inhibition of morphine and improgan antinociception by CC12, a P450 epoxygenase inhibitor. J Neurophysiol 2010, 104:3222-3230.
28. Hurley R.W., Hammond D.L. The analgesic effects of supraspinal μ and δ opioid receptor agonists are potentiated during persistent inflammation. J Neurosci 2000, 20:1249-1259.
29. Kim S.H., Chung J.M. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 1992, 50:355-363.
30. Kincaid W., Neubert M.J., Xu M., Kim C.J., Heinricher M.M. Role for medullary pain facilitating neurons in secondary thermal hyperalgesia. J Neurophysiol 2006, 95:33-41.
31. LeBars D. Serotonin and pain. Neuronal serotonin 1988, 171-226. Wiley, New York. N.N. Osborne, M. Hamond (Eds.).
32. Leong M.L., Gu M., Speltz-Paiz R., Stahura E.I., Mottey N., Steer C.J., Wessendorf M. Neuronal loss in the rostral ventromedial medulla in a rat model of neuropathic pain. J Neurosci 2011, 31:17028-17039.
33. Martenson M.E., Cetas J.S., Heinricher M.M. A possible neural basis for stress-induced hyperalgesia. Pain 2009, 142:236-244.
34. Michel M.C. Receptors for neuropeptide Y: multiple subtypes and multiple second messengers. Trends Pharmacol Sci 1991, 12:389-394.
35. Miki K., Zhou Q.Q., Guo W., Guan Y., Terayama R., Dubner R., Ren K. Changes in gene expression and neuronal phenotype in brain stem pain modulatory circuitry after inflammation. J Neurophysiol 2002, 87:750-760.
36. Nattie E., Li A. CO2 dialysis in the medullary raphe of the rat increases ventilation in sleep. J Appl Physiol 2001, 90:1247-1257.
37. Neubert M.J., Kincaid W., Heinricher M.M. Nociceptive facilitating neurons in the rostral ventromedial medulla. Pain 2004, 110:158-165.
38. Ossipov M.H., Zhang E.T., Carvajal C., Gardell L., Quirion R., Dumont Y., Lai J., Porreca F. Selective mediation of nerve injury-induced tactile hypersensitivity by neuropeptide Y. J Neurosci 2002, 22:9858-9867.
39. Ossipov M.H., Lai J., King T., Vanderah T.W., Porreca F. Underlying mechanisms of pronociceptive consequences of prolonged morphine exposure. Biopolymers 2005, 80:319-324.
40. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1997, Academic Press, Sydney.
41. Pertovaara A., Wei H., Hamalainen M.M. Lidocaine in the rostroventromedial medulla and the periaqueductal gray attenuates allodynia in neuropathic rats. Neurosci Lett 1996, 218:127-130.
42. Phillips R.S., Cleary D.R., Nalwalk J.W., Arttamangkul S., Hough L.B., Heinricher M.M. Pain-facilitating medullary neurons contribute to opioid-induced respiratory depression. J Neurophysiol 2012, 108:2393-2404.
43. Porreca F., Burgess S.E., Gardell L.R., Vanderah T.W., Malan T.P., Ossipov M.H., Lappi D.A., Lai J. Inhibition of neuropathic pain by selective ablation of brainstem medullary cells expressing the μ-opioid receptor. J Neurosci 2001, 21:5281-5288.
44. Ren K. An improved method for assessing mechanical allodynia in the rat. Physiol Behav 1999, 67:711-716.
45. Ren K., Dubner R. Descending modulation in persistent pain: an update. Pain 2002, 100:1-6.
46. Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., Tinevez J.Y., White D.J., Hartenstein V., Eliceiri K., Tomancak P., Cardona A. Fiji: an open-source platform for biological-image analysis. Nat Methods 2012, 9:676-682.
47. Skagerberg G., Björklund A. Topographic principles in the spinal projections of serotonergic and non-serotonergic brainstem neurons in the rat. Neuroscience 1985, 15:445-480.
48. Smith P.A., Moran T.D., Abdulla F., Tumber K.K., Taylor B.K. Spinal mechanisms of NPY analgesia. Peptides 2007, 28:464-474.
49. Solway B., Bose S.C., Corder G., Donahue R.R., Taylor B.K. Tonic inhibition of chronic pain by neuropeptide Y. Proc Natl Acad Sci U S A 2011, 108:7224-7229.
50. Sugiyo S., Takemura M., Dubner R., Ren K. Trigeminal transition zone/rostral ventromedial medulla connections and facilitation of orofacial hyperalgesia after masseter inflammation in rats. J Comp Neurol 2005, 493:510-523.
51. Suzuki Y., Satoh S., Ikegaki I., Okada T., Shibuya M., Sugita K., Asano T. Effects of neuropeptide Y and calcitonin gene-related peptide on local cerebral blood flow in rat striatum. J Cereb Blood Flow Metab 1989, 9:268-270.
52. Suzuki R., Rygh L.J., Dickenson A.H. Bad news from the brain: descending 5-HT pathways that control spinal pain processing. Trends Pharmacol Sci 2004, 25:613-617.
53. Sykes K.T., White S.R., Hurley R.W., Mizoguchi H., Tseng L.F., Hammond D.L. Mechanisms responsible for the enhanced antinociceptive effects of mu-opioid receptor agonists in the rostral ventromedial medulla of male rats with persistent inflammatory pain. J Pharmacol Exp Ther 2007, 322:813-821.
54. Taylor B.K., Abhyankar S.S., Vo N.-T.T., Kriedt C.L., Churi S.B., Urban J.H. Neuropeptide Y acts at Y1 receptors in the rostral ventral medulla to inhibit neuropathic pain. Pain 2007, 131:83-95.
55. Terayama R., Dubner R., Ren K. The roles of NMDA receptor activation and nucleus reticularis gigantocellularis in the time-dependent changes in descending inhibition after inflammation. Pain 2002, 97:171-181.
56. Tuor U.I., Kelly P.A., Edvinsson L., McCulloch J. Neuropeptide Y and the cerebral circulation. J Cereb Blood Flow Metab 1990, 10:591-601.
57. Vanegas H., Schaible H.-G. Descending control of persistent pain: inhibitory or facilitatory?. Brain Res Rev 2004, 46:295-309.
58. Vera-Portocarrero L.P., Xie J.Y., Kowal J., Ossipov M.H., King T., Porreca F. Descending facilitation from the rostral ventromedial medulla maintains visceral pain in rats with experimental pancreatitis. Gastroenterology 2006, 130:2155-2164.
59. Zukowska-Grojec Z., Wahlestedt C. Origin and actions of neuropeptide y in the cardiovascular system. The biology of neuropeptide y and related peptides 1993, 315-388. Humana Press, London. W. Colmers, C. Wahlestedt (Eds.).