Spinal ceramide and neuronal apoptosis in morphine antinociceptive tolerance

Neuroscience Letters

Volumn 463, Issue 1, 2009, Pages 49-53

  Bryant, Leesa ^a   Doyle, Tim ^a   Chen, Zhoumo ^a   Cuzzocrea, Salvatore ^b   Masini, Emanuela ^c   Vinci, M Cristina ^c   Esposito, Emanuela ^b   Mazzon, Emanuela ^b   Petrusca, Daniela Nicoleta ^d   Petrache, Irina ^d   Salvemini, Daniela ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MESSINA   (Italy)

^c UNIVERSITY OF FLORENCE   (Italy)

^d INDIANA UNIVERSITY   (United States)

Author keywords

Ceramide; Morphine tolerance; Neuronal apoptosis; Nitroxidative stress; Peroxynitrite

Indexed keywords

CERAMIDE; FUMONISIN B1; MORPHINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTINOCICEPTION; ARTICLE; BIOSYNTHESIS; CHRONIC DRUG ADMINISTRATION; COMPETITIVE INHIBITION; CONTROLLED STUDY; DOSE RESPONSE; DRUG TOLERABILITY; MALE; MOUSE; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD DORSAL HORN; UPREGULATION;

ANALGESICS, OPIOID; ANIMALS; APOPTOSIS; CERAMIDES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG TOLERANCE; ENZYME ACTIVATION; MALE; MICE; MORPHINE; OXIDOREDUCTASES; POSTERIOR HORN CELLS; SPINAL CORD; UP-REGULATION;

EID: 68149098861     PISSN: 03043940     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neulet.2009.07.051     Document Type: Article

References (41)

1. Arai T., Bhunia A.K., Chatterjee S., and Bulkley G.B. Lactosylceramide stimulates human neutrophils to upregulate Mac-1, adhere to endothelium, and generate reactive oxygen metabolites in vitro. Circ. Res. 82 (1998) 540-547
2. Arena S., Pattarozzi A., Thellung S., Villa V., Corsaro A., Massa A., Diana F., Spoto G., Forcella S., Damonte G., Filocamo M., Benatti U., Schettini G., and Florioa T. Nitric oxide production stimulated by the basic fibroblast growth factor requires the synthesis of ceramide. Ann. N. Y. Acad. Sci. 973 (2002) 94-104
3. Batinic-Haberle I., Ndengele M.M., Cuzzocrea S., Reboucas J.S., Spasojevic I., and Salvemini D. Lipophilicity is a critical parameter that dominates the efficacy of metalloporphyrins in blocking the development of morphine antinociceptive tolerance through peroxynitrite-mediated pathways. Free Radic. Biol. Med. 46 (2009) 212-219
4. D'Amour F. A method for determining loss of pain sensation. J. Pharmacol. Exp. Ther. 72 (1941) 74-79
5. Dawkins J.L., Hulme D.J., Brahmbhatt S.B., Auer-Grumbach M., and Nicholson G.A. Mutations in SPTLC1, encoding serine palmitoyltransferase, long chain base subunit-1, cause hereditary sensory neuropathy type I. Nat. Genet. 27 (2001) 309-312
6. De Nadai C., Sestili P., Cantoni O., Lievremont J.P., Sciorati C., Barsacchi R., Moncada S., Meldolesi J., and Clementi E. Nitric oxide inhibits tumor necrosis factor-alpha-induced apoptosis by reducing the generation of ceramide. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 5480-5485
7. Delgado A., Casas J., Llebaria A., Abad J.L., and Fabrias G. Inhibitors of sphingolipid metabolism enzymes. Biochim. Biophys. Acta 1758 (2006) 1957-1977
8. Delogu G., Famularo G., Amati F., Signore L., Antonucci A., Trinchieri V., Di Marzio L., and Cifone M.G. Ceramide concentrations in septic patients: a possible marker of multiple organ dysfunction syndrome. Crit. Care Med. 27 (1999) 2413-2417
9. Franzen R., Pautz A., Brautigam L., Geisslinger G., Pfeilschifter J., and Huwiler A. Interleukin-1beta induces chronic activation and de novo synthesis of neutral ceramidase in renal mesangial cells. J. Biol. Chem. 276 (2001) 35382-35389
10. Franzen R., Pfeilschifter J., and Huwiler A. Nitric oxide induces neutral ceramidase degradation by the ubiquitin/proteasome complex in renal mesangial cell cultures. FEBS Lett. 532 (2002) 441-444
11. Garcia J.G., Liu F., Verin A.D., Birukova A., Dechert M.A., Gerthoffer W.T., Bamberg J.R., and English D. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J. Clin. Invest. 108 (2001) 689-701
12. Huwiler A., Dorsch S., Briner V.A., van den Bosch H., and Pfeilschifter J. Nitric oxide stimulates chronic ceramide formation in glomerular endothelial cells. Biochem. Biophys. Res. Commun. 258 (1999) 60-65
13. Huwiler A., Pfeilschifter J., and van den Bosch H. Nitric oxide donors induce stress signaling via ceramide formation in rat renal mesangial cells. J. Biol. Chem. 274 (1999) 7190-7195
14. Jagtap P., and Szabo C. Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat. Rev. Drug Discov. 4 (2005) 421-440
15. Johns D.G., Osborn H., and Webb R.C. Ceramide: a novel cell signaling mechanism for vasodilation. Biochem. Biophys. Res. Commun. 237 (1997) 95-97
16. Kolesnick R. The therapeutic potential of modulating the ceramide/sphingomyelin pathway. J. Clin. Invest. 110 (2002) 3-8
17. Kolesnick R., and Fuks Z. Radiation and ceramide-induced apoptosis. Oncogene 22 (2003) 5897-5906
18. Kolesnick R., and Golde D.W. The sphingomyelin pathway in tumor necrosis factor and interleukin-1 signaling. Cell 77 (1994) 325-328
19. Kroemer G. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat. Med. 3 (1997) 614-620
20. Lim G., Wang S., Lim J.A., and Mao J. Activity of adenylyl cyclase and protein kinase A contributes to morphine-induced spinal apoptosis. Neurosci. Lett. 389 (2005) 104-108
21. Lodovici M., Casalini C., Cariaggi R., Michelucci L., and Dolara P. Levels of 8-hydroxydeoxyguanosine as a marker of DNA damage in human leukocytes. Free Radic. Biol. Med. 28 (2000) 13-17
22. Mansat-de Mas V., Bezombes C., Quillet-Mary A., Bettaieb A., D'Orgeix A D.J., Laurent G., and Jaffrezou J.P. Implication of radical oxygen species in ceramide generation, c-Jun N-terminal kinase activation and apoptosis induced by daunorubicin. Mol. Pharmacol. 56 (1999) 867-874
23. Mao J., Price D.D., Zhu J., Lu J., and Mayer D.J. The inhibition of nitric oxide-activated poly(ADP-ribose) synthetase attenuates transsynaptic alteration of spinal cord dorsal horn neurons and neuropathic pain in the rat. Pain 72 (1997) 355-366
24. Masini E., Giannini L., Nistri S., Cinci L., Mastroianni R., Xu W., Comhair S.A., Li D., Cuzzocrea S., Matuschak G.M., and Salvemini D. Ceramide: a key signaling molecule in a Guinea pig model of allergic asthmatic response and airway inflammation. J. Pharmacol. Exp. Ther. 324 (2008) 548-557
25. Mayer D.J., Mao J., Holt J., and Price D.D. Cellular mechanisms of neuropathic pain, morphine tolerance, and their interactions. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 7731-7736
26. McCord J.M., and Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244 (1969) 6049-6055
27. Muscoli C., Cuzzocrea S., Ndengele M.M., Mollace V., Porreca F., Fabrizi F., Esposito E., Masini E., Matuschak G.M., and Salvemini D. Therapeutic manipulation of peroxynitrite attenuates the development of opiate-induced antinociceptive tolerance in mice. J. Clin. Invest. 117 (2007) 3530-3539
28. Ndengele M.M., Cuzzocrea S., Masini E., Vinci M.C., Esposito E., Muscoli C., Petrusca D.N., Mollace V., Mazzon E., Li D., Petrache I., Matuschak G.M., and Salvemini D. Spinal ceramide modulates the development of morphine antinociceptive tolerance via peroxynitrite-mediated nitroxidative stress and neuroimmune activation. J. Pharmacol. Exp. Ther. 329 (2009) 64-75
29. Pannu R., Won J.S., Khan M., Singh A.K., and Singh I. A novel role of lactosylceramide in the regulation of lipopolysaccharide/interferon-gamma-mediated inducible nitric oxide synthase gene expression: implications for neuroinflammatory diseases. J. Neurosci. 24 (2004) 5942-5954
30. Petrache I., Medler T.R., Richter A.T., Kamocki K., Chukwueke U., Zhen L., Gu Y., Adamowicz J., Schweitzer K.S., Hubbard W.C., Berdyshev E.V., Lungarella G., and Tuder R.M. Superoxide dismutase protects against apoptosis and alveolar enlargement induced by ceramide. Am. J. Physiol. Lung Cell. Mol. Physiol. 295 (2008) L44-L53
31. Petrache I., Natarajan V., Zhen L., Medler T.R., Richter A.T., Cho C., Hubbard W.C., Berdyshev E.V., and Tuder R.M. Ceramide upregulation causes pulmonary cell apoptosis and emphysema-like disease in mice. Nat. Med. 11 (2005) 491-498
32. Putcha G.V., Deshmukh M., and Johnson Jr. E.M. BAX translocation is a critical event in neuronal apoptosis: regulation by neuroprotectants, BCL-2, and caspases. J. Neurosci. 19 (1999) 7476-7485
33. Qiu H., Edmunds T., Baker-Malcolm J., Karey K.P., Estes S., Schwarz C., Hughes H., and Van Patten S.M. Activation of human acid sphingomyelinase through modification or deletion of C-terminal cysteine. J. Biol. Chem. 278 (2003) 32744-32752
34. Radi R., Rodriguez M., Castro L., and Telleri R. Inhibition of mitochondrial electron transport by peroxynitrite. Arch. Biochem. Biophys. 308 (1994) 89-95
35. Song P., and Zhao Z.Q. The involvement of glial cells in the development of morphine tolerance. Neurosci. Res. 39 (2001) 281-286
36. Takeda Y., Tashima M., Takahashi A., Uchiyama T., and Okazaki T. Ceramide generation in nitric oxide-induced apoptosis. Activation of magnesium-dependent neutral sphingomyelinase via caspase-3. J. Biol. Chem. 274 (1999) 10654-10660
37. Viani P., Giussani P., Ferraretto A., Signorile A., Riboni L., and Tettamanti G. Nitric oxide production in living neurons is modulated by sphingosine: a fluorescence microscopy study. FEBS Lett. 506 (2001) 185-190
38. Watkins L.R., Hutchinson M.R., Ledeboer A., Wieseler-Frank J., Milligan E.D., and Maier S.F. Norman Cousins Lecture. Glia as the "bad guys": implications for improving clinical pain control and the clinical utility of opioids. Brain Behav. Immun. 21 (2007) 131-146
39. Won J.S., Im Y.B., Khan M., Singh A.K., and Singh I. The role of neutral sphingomyelinase produced ceramide in lipopolysaccharide-mediated expression of inducible nitric oxide synthase. J. Neurochem. 88 (2004) 583-593
40. Xiang H., Kinoshita Y., Knudson C.M., Korsmeyer S.J., Schwartzkroin P.A., and Morrison R.S. Bax involvement in p53-mediated neuronal cell death. J. Neurosci. 18 (1998) 1363-1373
41. Zhang D.X., Zou A.P., and Li P.L. Ceramide-induced activation of NADPH oxidase and endothelial dysfunction in small coronary arteries. Am. J. Physiol. Heart Circ. Physiol. 284 (2003) H605-H612