Periaqueductal gray neuroplasticity following chronic morphine varies with age: Role of oxidative stress

Neuroscience

Volumn 226, Issue , 2012, Pages 165-177

  Bajic, D ^a,b   Berde, C B ^a   Commons, K G ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

C fos; Fos; Nitric oxide; NNOS; Opioid tolerance; Periaqueductal gray

Indexed keywords

MORPHINE SULFATE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PEROXIDE; PROTEIN FOS; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; SODIUM CHLORIDE; SUPEROXIDE;

ADULT ANIMAL; AGING; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DRUG TOLERANCE; FEMALE; GENE EXPRESSION; HOT PLATE TEST; IMMUNOHISTOCHEMISTRY; LATERODORSAL TEGMENTAL NUCLEUS; LONG TERM EXPOSURE; MALE; MORNING DOSAGE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; OXIDATIVE STRESS; PERIAQUEDUCTAL GRAY MATTER; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TEGMENTUM; TREATMENT DURATION;

AGING; ANIMALS; ANIMALS, NEWBORN; CELL COUNT; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GENE EXPRESSION; GENES, FOS; HOT TEMPERATURE; IMMUNOHISTOCHEMISTRY; MORPHINE; NADPH DEHYDROGENASE; NARCOTICS; NEURONAL PLASTICITY; NEURONS; NITRIC OXIDE SYNTHASE TYPE I; OXIDATIVE STRESS; PAIN MEASUREMENT; PERIAQUEDUCTAL GRAY; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84867314606     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.09.028     Document Type: Article

References (81)

1. Ambasta R.K., Kumar P., Griendling K.K., Schmidt H.H., Busse R., Brandes R.P. Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J Biol Chem 2004, 279:45935-45941.
2. Anand K.J., Willson D.F., Berger J., Harrison R., Meert K.L., Zimmerman J., Carcillo J., Newth C.J., Prodhan P., Dean J.M., Nicholson C. Tolerance and withdrawal from prolonged opioid use in critically Ill children. Pediatrics 2010, 125:1208-1225.
3. Babey A.M., Kolesnikov Y., Cheng J., Inturrisi C.E., Trifilletti R.R., Pasternak G.W. Nitric oxide and opioid tolerance. Neuropharmacology 1994, 33:1463-1470.
4. Banfi B., Clark R.A., Steger K., Krause K.H. Two novel proteins activate superoxide generation by the NADPH oxidase NOX1. J Biol Chem 2003, 278:3510-3513.
5. Barbaresi P. Postnatal development of GABA-immunoreactive neurons and terminals in rat periaqueductal gray matter: a light and electron microscopic study. J Comp Neurol 2010, 518:2240-2260.
6. Barr G.A., Wang S. Tolerance and withdrawal to chronic morphine treatment in the week-old rat pup. Eur J Pharmacol 1992, 215:35-42.
7. Barr G.A., Miya D.Y., Paredes W. Analgesic effects of intraventricular and intrathecal injection of morphine and ketocyclazocine in the infant rat. Brain Res 1992, 584:83-91.
8. Basbaum A.I., Fields H.L. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 1984, 7:309-338.
9. Blottner D., Grozdanovic Z., Gossrau R. Histochemistry of nitric oxide synthase in the nervous system. Histochem J 1995, 27:785-811.
10. Buwalda B., Nyakas C., Gast J., Luiten P.G., Schmidt H.H. Aldehyde fixation differentially affects distribution of diaphorase activity but not of nitric oxide synthase immunoreactivity in rat brain. Brain Res Bull 1995, 38:467-473.
11. Chang S.L., Squinto S.P., Harlan R.E. Morphine activation of c-fos expression in rat brain. Biochem Biophys Res Commun 1988, 157:698-704.
12. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987, 162:156-159.
13. Commons K.G., Aicher S.A., Kow L.M., Pfaff D.W. Presynaptic and postsynaptic relations of mu-opioid receptors to gamma-aminobutyric acid-immunoreactive and medullary-projecting periaqueductal gray neurons. J Comp Neurol 2000, 419:532-542.
14. Cork R.J., Perrone M.L., Bridges D., Wandell J., Scheiner C.A., Mize R.R. A web-accessible digital atlas of the distribution of nitric oxide synthase in the mouse brain. Prog Brain Res 1998, 118:37-50.
15. Dragunow M., Faull R. The use of c-fos as a metabolic marker in neuronal pathway tracing. J Neurosci Methods 1989, 29:261-265.
16. Fields H.L., Basbaum A.I., Heinricher M.M. Central nervous systems mechanisms of pain modulation. Textbook of Pain 2006, 125-142. Elsevier, Churchill Livingston, Philadelphia, PA. S.B. McMahon, M. Koltzenburg (Eds.).
17. Fitzgerald M., Walker S.M. Infant pain management: a developmental neurobiological approach. Nat Clin Pract Neurol 2009, 5:35-50.
18. Fonsmark L., Rasmussen Y.H., Carl P. Occurrence of withdrawal in critically ill sedated children. Crit Care Med 1999, 27:196-199.
19. Gonzalez-Hernandez T., Perez de la Cruz M.A., Mantolan-Sarmiento B. Histochemical and immunohistochemical detection of neurons that produce nitric oxide: effect of different fixative parameters and immunoreactivity against non-neuronal NOS antisera. J Histochem Cytochem 1996, 44:1399-1413.
20. Gotti S., Sica M., Viglietti-Panzica C., Panzica G. Distribution of nitric oxide synthase immunoreactivity in the mouse brain. Microsc Res Tech 2005, 68:13-35.
21. Harris L.S., Pierson A.K. Some narcotic antagonists in the benzomorphan series. J Pharmacol Exp Ther 1964, 143:141-148.
22. Heinzen E.L., Pollack G.M. The development of morphine antinociceptive tolerance in nitric oxide synthase-deficient mice. Biochem Pharmacol 2004, 67:735-741.
23. Heinzen E.L., Pollack G.M. Pharmacodynamics of morphine-induced neuronal nitric oxide production and antinociceptive tolerance development. Brain Res 2004, 1023:175-184.
24. Herdegen T., Leah J.D. Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res Brain Res Rev 1998, 28:370-490.
25. Herman B.H., Vocci F., Bridge P. The effects of NMDA receptor antagonists and nitric oxide synthase inhibitors on opioid tolerance and withdrawal. Medication development issues for opiate addiction. Neuropsychopharmacology 1995, 13:269-293.
26. Holmstrand E.C., Sesack S.R. Projections from the rat pedunculopontine and laterodorsal tegmental nuclei to the anterior thalamus and ventral tegmental area arise from largely separate populations of neurons. Brain Struct Funct 2011, 216:331-345.
27. Hope B.T., Michael G.J., Knigge K.M., Vincent S.R. Neuronal NADPH diaphorase is a nitric oxide synthase. Proc Natl Acad Sci USA 1991, 88:2811-2814.
28. Jacquet Y.F., Lajtha A. The periaqueductal gray: site of morphine analgesia and tolerance as shown by 2-way cross tolerance between systemic and intracerebral injections. Brain Res 1976, 103:501-513.
29. Jensen T.S., Yaksh T.L. Comparison of antinociceptive action of morphine in the periaqueductal gray, medial and paramedial medulla in rat. Brain Res 1986, 363:99-113.
30. Jones K.L., Barr G.A. Ontogeny of morphine withdrawal in the rat. Behav Neurosci 1995, 109:1189-1198.
31. Katz R., Kelly H.W., Hsi A. Prospective study on the occurrence of withdrawal in critically ill children who receive fentanyl by continuous infusion. Crit Care Med 1994, 22:763-767.
32. Kehoe P., Blass E.M. Behaviorally functional opioid systems in infant rats: II. Evidence for pharmacological, physiological, and psychological mediation of pain and stress. Behav Neurosci 1986, 100:624-630.
33. Kehoe P., Blass E.M. Central nervous system mediation of positive and negative reinforcement in neonatal albino rats. Brain Res 1986, 392:69-75.
34. Kielstein A., Tsikas D., Galloway G.P., Mendelson J.E. Asymmetric dimethylarginine (ADMA)-a modulator of nociception in opiate tolerance and addiction?. Nitric Oxide 2007, 17:55-59.
35. Lane D.A., Tortorici V., Morgan M.M. Behavioral and electrophysiological evidence for tolerance to continuous morphine administration into the ventrolateral periaqueductal gray. Neuroscience 2004, 125:63-69.
36. Lane D.A., Patel P.A., Morgan M.M. Evidence for an intrinsic mechanism of antinociceptive tolerance within the ventrolateral periaqueductal gray of rats. Neuroscience 2005, 135:227-234.
37. Lester D.B., Rogers T.D., Blaha C.D. Acetylcholine-dopamine interactions in the pathophysiology and treatment of CNS disorders. CNS Neurosci Ther 2010, 16:137-162.
38. Liu J., Nickolenko J., Sharp F.R. Morphine induces c-fos and junB in striatum and nucleus accumbens via D1 and N-methyl-d-aspartate receptors. Proc Natl Acad Sci USA 1994, 91:8537-8541.
39. Loyd D.R., Morgan M.M., Murphy A.Z. Morphine preferentially activates the periaqueductal gray-rostral ventromedial medullary pathway in the male rat: a potential mechanism for sex differences in antinociception. Neuroscience 2007, 147:456-468.
40. Loyd D.R., Morgan M.M., Murphy A.Z. Sexually dimorphic activation of the periaqueductal gray-rostral ventromedial medullary circuit during the development of tolerance to morphine in the rat. Eur J Neurosci 2008, 27:1517-1524.
41. Machelska H., Ziolkowska B., Mika J., Przewlocka B., Przewlocki R. Chronic morphine increases biosynthesis of nitric oxide synthase in the rat spinal cord. Neuroreport 1997, 8:2743-2747.
42. Mao J. NMDA and opioid receptors: their interactions in antinociception, tolerance and neuroplasticity. Brain Res Rev 1999, 30:289-304.
43. Mark G.P., Shabani S., Dobbs L.K., Hansen S.T. Cholinergic modulation of mesolimbic dopamine function and reward. Physiol Behav 2011, 104:76-81.
44. Martyn K.D., Frederick L.M., von Loehneysen K., Dinauer M.C., Knaus U.G. Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal 2006, 18:69-82.
45. Masters D.B., Berde C.B., Dutta S.K., Griggs C.T., Hu D., Kupsky W., Langer R. Prolonged regional nerve blockade by controlled release of local anesthetic from a biodegradable polymer matrix. Anesthesiology 1993, 79:340-346.
46. Matsumoto T., Nakane M., Pollock J.S., Kuk J.E., Forstermann U. A correlation between soluble brain nitric oxide synthase and NADPH-diaphorase activity is only seen after exposure of the tissue to fixative. Neurosci Lett 1993, 155:61-64.
47. Mayer D.J., Mao J., Holt J., Price D.D. Cellular mechanisms of neuropathic pain, morphine tolerance, and their interactions. Proc Natl Acad Sci USA 1999, 96:7731-7736.
48. McHaffie J.G., Beninato M., Stein B.E., Spencer R.F. Postnatal development of acetylcholinesterase in, and cholinergic projections to, the cat superior colliculus. J Comp Neurol 1991, 313:113-131.
49. Morgan M.M., Whitney P.K., Gold M.S. Immobility and flight associated with antinociception produced by activation of the ventral and lateral/dorsal regions of the rat periaqueductal gray. Brain Res 1998, 804:159-166.
50. Morgan M.M., Fossum E.N., Levine C.S., Ingram S.L. Antinociceptive tolerance revealed by cumulative intracranial microinjections of morphine into the periaqueductal gray in the rat. Pharmacol Biochem Behav 2006, 85:214-219.
51. Morris B.J., Simpson C.S., Mundell S., Maceachern K., Johnston H.M., Nolan A.M. Dynamic changes in NADPH-diaphorase staining reflect activity of nitric oxide synthase: evidence for a dopaminergic regulation of striatal nitric oxide release. Neuropharmacology 1997, 36:1589-1599.
52. Nandi R., Fitzgerald M. Opioid analgesia in the newborn. Eur J Pain 2005, 9:105-108.
53. Oakman S.A., Faris P.L., Kerr P.E., Cozzari C., Hartman B.K. Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J Neurosci 1995, 15:5859-5869.
54. Okere C.O., Waterhouse B.D. Activity-dependent heterogeneous populations of nitric oxide synthase neurons in the rat dorsal raphe nucleus. Brain Res 2006, 1086:117-132.
55. Okere C.O., Waterhouse B.D. Acute capsaicin injection increases nicotinamide adenine dinucleotide phosphate diaphorase staining independent of Fos activation in the rat dorsolateral periaqueductal gray. Neurosci Lett 2006, 404:288-293.
56. Okere C.O., Waterhouse B.D. Acute restraint increases NADPH-diaphorase staining in distinct subregions of the rat dorsal raphe nucleus: implications for raphe serotonergic and nitrergic transmission. Brain Res 2006, 1119:174-181.
57. Onstott D., Mayer B., Beitz A.J. Nitric oxide synthase immunoreactive neurons anatomically define a longitudinal dorsolateral column within the midbrain periaqueductal gray of the rat: analysis using laser confocal microscopy. Brain Res 1993, 610:317-324.
58. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, Orlando, FL.
59. Rahman W., Dickenson A.H. Development of spinal opioid systems. Reg Anesth Pain Med 1999, 24:383-385.
60. Rodrigo J., Springall D.R., Uttenthal O., Bentura M.L., Abadia-Molina F., Riveros-Moreno V., Martinez-Murillo R., Polak J.M., Moncada S. Localization of nitric oxide synthase in the adult rat brain. Philos Trans R Soc Lond B Biol Sci 1994, 345:175-221.
61. Shin J.H., Chung S., Park E.J., Uhm D.Y., Suh C.K. Nitric oxide directly activates calcium-activated potassium channels from rat brain reconstituted into planar lipid bilayer. FEBS Lett 1997, 415:299-302.
62. Simpson K.L., Waterhouse B.D., Lin R.C. Differential expression of nitric oxide in serotonergic projection neurons: neurochemical identification of dorsal raphe inputs to rodent trigeminal somatosensory targets. J Comp Neurol 2003, 466:495-512.
63. Siuciak J.A., Advokat C. Tolerance to morphine microinjections in the periaqueductal gray (PAG) induces tolerance to systemic, but not intrathecal morphine. Brain Res 1987, 424:311-319.
64. Spessert R., Layes E. Fixation conditions affect the intensity but not the pattern of NADPH-diaphorase staining as a marker for neuronal nitric oxide synthase in rat olfactory bulb. J Histochem Cytochem 1994, 42:1309-1315.
65. Sugaya K., McKinney M. Nitric oxide synthase gene expression in cholinergic neurons in the rat brain examined by combined immunocytochemistry and in situ hybridization histochemistry. Brain Res Mol Brain Res 1994, 23:111-125.
66. Takeya R., Ueno N., Kami K., Taura M., Kohjima M., Izaki T., Nunoi H., Sumimoto H. Novel human homologues of p47phox and p67phox participate in activation of superoxide-producing NADPH oxidases. J Biol Chem 2003, 278:25234-25246.
67. Thornton S.R., Smith F.L. Characterization of neonatal rat fentanyl tolerance and dependence. J Pharmacol Exp Ther 1997, 281:514-521.
68. Thornton S.R., Wang A.F., Smith F.L. Characterization of neonatal rat morphine tolerance and dependence. Eur J Pharmacol 1997, 340:161-167.
69. Tive L.A., Barr G.A. Analgesia from the periaqueductal gray in the developing rat: focal injections of morphine or glutamate and effects of intrathecal injection of methysergide or phentolamine. Brain Res 1992, 584:92-109.
70. Tortorici V., Robbins C.S., Morgan M.M. Tolerance to the antinociceptive effect of morphine microinjections into the ventral but not lateral-dorsal periaqueductal gray of the rat. Behav Neurosci 1999, 113:833-839.
71. Tortorici V., Morgan M.M., Vanegas H. Tolerance to repeated microinjection of morphine into the periaqueductal gray is associated with changes in the behavior of off- and on-cells in the rostral ventromedial medulla of rats. Pain 2001, 89:237-244.
72. Tseng L.F., Collins K.A., Wang Q. Differential ontogenesis of thermal and mechanical antinociception induced by morphine and beta-endorphin. Eur J Pharmacol 1995, 277:71-76.
73. Usunoff K.G., Kharazia V.N., Valtschanoff J.G., Schmidt H.H., Weinberg R.J. Nitric oxide synthase-containing projections to the ventrobasal thalamus in the rat. Anat Embryol (Berl) 1999, 200:265-281.
74. van der Veen B.S., de Winther M.P., Heeringa P. Myeloperoxidase: molecular mechanisms of action and their relevance to human health and disease. Antioxid Redox Signal 2009, 11:2899-2937.
75. von Lohneysen K., Noack D., Jesaitis A.J., Dinauer M.C., Knaus U.G. Mutational analysis reveals distinct features of the Nox4-p22 phox complex. J Biol Chem 2008, 283:35273-35282.
76. Xu Z.Q., Hokfelt T. Expression of galanin and nitric oxide synthase in subpopulations of serotonin neurons of the rat dorsal raphe nucleus. J Chem Neuroanat 1997, 13:169-187.
77. Xu J.Y., Hill K.P., Bidlack J.M. The nitric oxide/cyclic GMP system at the supraspinal site is involved in the development of acute morphine antinociceptive tolerance. J Pharmacol Exp Ther 1998, 284:196-201.
78. Yang Q., Chen S.R., Li D.P., Pan H.L. Kv1.1/1.2 channels are downstream effectors of nitric oxide on synaptic GABA release to preautonomic neurons in the paraventricular nucleus. Neuroscience 2007, 149:315-327.
79. Zhu H., Barr G.A. Inhibition of morphine withdrawal by the NMDA receptor antagonist MK-801 in rat is age-dependent. Synapse 2001, 40:282-293.
80. Zhu H., Barr G.A. Opiate withdrawal during development: are NMDA receptors indispensable?. Trends Pharmacol Sci 2001, 22:404-408.
81. Zhu H., Barr G.A. Ontogeny of NMDA receptor-mediated morphine tolerance in the postnatal rat. Pain 2003, 104:437-447.