Analgetic effect of docosahexaenoic acid is mediated by modulating the microglia activity in the dorsal root ganglia in a rat model of neuropathic pain

Acta Histochemica

Volumn 117, Issue 7, 2015, Pages 659-666

  Manzhulo, Igor V ^a,b   Ogurtsova, Olga S ^a   Lamash, Nina E ^a   Latyshev, Nikolay A ^a   Kasyanov, Sergey P ^a   Dyuizen, Inessa V ^a  

^a INSTITUTE OF MARINE BIOLOGY   (Russian Federation)

^b FAR EASTERN FEDERAL UNIVERSITY   (Russian Federation)

Author keywords

Apoptosis; CCI; Docosahexaenoic acid; Dorsal root ganglia; Microglia; Satellite cells

Indexed keywords

DOCOSAHEXAENOIC ACID; PROTEIN P53; ANALGESIC AGENT;

ALLODYNIA; ANALGESIC ACTIVITY; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; GLIA CELL; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MALE; MICROGLIA; MUSCLE ATROPHY; NEUROPATHIC PAIN; NEUROPROTECTION; NONHUMAN; PAIN INTENSITY; PROTEIN EXPRESSION; RAT; SPINAL GANGLION; TREATMENT DURATION; TREATMENT RESPONSE; WEIGHT BEARING; ANIMAL; DISEASE MODEL; DRUG EFFECTS; METABOLISM; NEURALGIA; SCIATIC NERVE; WISTAR RAT;

ANALGESICS; ANIMALS; DISEASE MODELS, ANIMAL; DOCOSAHEXAENOIC ACIDS; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; NEURALGIA; RATS; RATS, WISTAR; SCIATIC NERVE;

EID: 84940958729     PISSN: 00651281     EISSN: 16180372     Source Type: Journal    
DOI: 10.1016/j.acthis.2015.07.001     Document Type: Article

References (53)

1. Ajmone-Cat A.M., Salvatori L.M., De Simone R., Mancini M., Biagioni S., Bernardo A., Cacci E., Minghetti L. Docosahexaenoic acid modulates inflammatory and antineurogenic functions of activated microglial cells. J. Neurosci. Res. 2012, 90:575-587.
2. Arkhipova S.S., Raginov I.S., Mukhitov A.R., Chelyshev Y.A. Satellite cells of sensory neurons after various types of sciatic nerve trauma in the rat. Neurosci. Behav. Physiol. 2010, 40:609-614.
3. Bazan N.G. Omega-3 fatty acids, pro-inflammatory signaling and neuroprotection. Curr. Opin. Clin. Nutr. Metab. Care 2007, 10:136-141.
4. Belayev L., Marcheselli V.L., Khoutorova L. Docosahexaenoic acid complexed to albumin elicits high-grade ischemic neuroprotection. Stroke 2005, 36:118-123.
5. Bennett G.J., Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 1988, 33:87-107.
6. Bennett G.J. An animal model of neuropathic pain: a review. Muscle Nerve 1993, 16:1040-1048.
7. Bousquet M., Gibrat C., Saint-Pierre M., Julien C., Calon F., Cicchetti F. Modulation of brain-derived neurotrophic factor as a potential neuroprotective mechanism of action of omega-3 fatty acids in a parkinsonian animal model. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2009, 33:1401-1408.
8. Casals-Díaz L., Vivo M., Navarro X. Nociceptive responses and spinal plastic changes of afferent C-fibers in three neuropathic pain models induced by sciatic nerve injury in the rat. Exp. Neurol. 2009, 217:84-95.
9. Chen M., Wang J. Initiator caspases in apoptosis signaling pathways. Apoptosis 2002, 7:313-319.
10. Costigan M., Scholz J., Woolf C. Neuropathic pain: a maladaptive response of the nervous system to damage. Ann. Rev. Neurosci. 2009, 32:1-32.
11. Cunnane S.C., Plourde M., Pifferi F., Bégin M., Féart C., Barberger-Gateau P. Fish, docosahexaenoic acid and Alzheimer's disease. Prog. Lipid Res. 2009, 48:239-256.
12. David S., Kroner A. Repertoire of microglial and macrophage responses after spinal cord injury. Nat. Rev. Neurosci. 2011, 12:388-399.
13. Di Cesare M.L., Pacini A., Micheli L., Tani A., Zanardelli M., Ghelardini C. Glial role in oxaliplatin-induced neuropathic pain. Exp. Neurol. 2014, 261:22-33.
14. Dong X.X., Wang Y.R., Qin S., Liang Z.Q., Liu B.H., Qin Z.H., Wang Y. p53 mediates autophagy activation and mitochondria dysfunction in kainic acid-induced excitotoxicity in primary striatal neurons. Neuroscience 2012, 207:52-64.
15. Dubovy P., Jancalek R., Klusakova I., Svizenska I., Pejchalova K. Intra- and extraneuronal changes of immunofluorescence staining for TNF-alpha and TNFR1 in the dorsal root ganglia of rat peripheral neuropathic pain models. Cell. Mol. Neurobiol. 2006, 26:1205-1217.
16. Dyuizen I.V., Manzhulo I.V., Ogurtsova O.S., Lamash N.E., Latyshev N.A., Kasyanov S.P. Specific features of analgesic effect of docosahexaenoic acid in rats with neuropathic pain syndrome. Bull. Exp. Biol. Med. 2013, 156:647-649.
17. Endo H., Kamada H., Nito C., Nishi T., Chan P.H. Mitochondrial translocation of p53 mediates release of cytochrome c and hippocampal CA1 neuronal death after transient global cerebral ischemia in rats. J. Neurosci. 2006, 26:7974-7983.
18. Gamoh S., Hashimoto M., Sugioka K., Shahdat H.M., Hata N., Misawa Y., Masumura S. Chronic administration of docosahexaenoic acid improves reference memory-related learning ability in young rats. Neuroscience 1999, 93:237-241.
19. Goldberg R.J., Katz J. A meta-analysis of the analgesic effects of omega-3 polyunsaturated fatty acid supplementation for inflammatory joint pain. Pain 2007, 129:210-223.
20. Hjorth E., Freund-Levi Y. Immunomodulation of microglia by docosahexaenoic acid and eicosapentaenoic acid. Curr. Opin. Clin. Nutr. Metab. Care 2012, 15:134-143.
21. Ji R.R., Xu Z., Strichartz G., Serhan C.N. Emerging roles of resolvins in the resolution of inflammation and pain. Trends Neurosci. 2011, 34:599-609.
22. Joseph E.K., Levine J.D. Caspase signaling in neuropathic and inflammatory pain in the rat. Eur. J. Neurosci. 2004, 20:2896-2902.
23. Kigerl K.A., Gensel J.C., Ankeny D.P., Alexander J.K., Donnelly D.J., Popovich P.G. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci. 2009, 29:13435-13444.
24. Kobayashi K., Imagama S., Ohgomori T., Hirano K., Uchimura K., Sakamoto K., Hirakawa A., Takeuchi H., Suzumura A., Ishiguro N., Kadomatsu K. Minocycline selectively inhibits M1 polarization of microglia. Cell Death Dis. 2013, 4:1-9.
25. Korzhevsky D.E., Kirik O.V., Sukhorukova E.G., Vlasov T.D. Structural organization of striatum microglia after transient focal ischemia. Morphology 2012, 141:28-32.
26. Ladeby R., Wirenfeldt M., Garcia-Ovejero D., Fenger C., Dissing-Olesen L., Dalmau I., Finsen B. Microglial cell population dynamics in the injured adult central nervous system. Brain Res. Rev. 2005, 48:196-206.
27. Latyshev N.A., Ermolenko E.V., Kasyanov S.P. Concentration and purification of polyunsaturated fatty acids from squid liver processing wastes. Eur. J. Lipid Sci. Technol. 2014, 116:234-236.
28. Liao B., Zhao W., Beers D.R., Henkel J.S., Appel S.H. Transformation from a neuroprotective to a neurotoxic microglial phenotype in a mouse model of ALS. Exp. Neurol. 2012, 237:147-152.
29. Lukiw W.J., Cui J.G., Marcheselli V.L., Bodker M., Botkjaer A., Gotlinger K., Serhan C.N., Bazan N.G. A role for docosahexaenoic acid-derived neuroprotectin D1 in neural cell survival and Alzheimer disease. J. Clin. Invest. 2005, 115:2774-2783.
30. Malmberg A.B., Basbaum A.I. Partial sciatic nerve injury in the mouse as a model of neuropathic pain: behavioral and neuroanatomical correlates. Pain 1998, 76:215-222.
31. Meissner F., Molawi K., Zychlinsky A. Mutant superoxide dismutase 1-induced IL-1beta accelerates ALS pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:13046-13050.
32. Mori I., Goshima F., Koshizuka T., Imai Y., Kohsaka S., Koide N., Sugiyama T., Yoshida T., Yokochi T., Kimura Y., Nishiyama Y. Iba1-expressing microglia respond to herpes simplex virus infection in the mouse trigeminal ganglion. Brain Res. Mol. Brain Res. 2003, 120:52-56.
33. Mukherjee P.K., Chawla A., Loayza M.S., Bazan N.G. Docosanoids are multifunctional regulators of neural cell integrity and fate: significance in aging and disease. Prostaglandins Leukot. Essent. Fatty Acids 2007, 77:233-238.
34. Mukherjee P.K., Marcheselli V.L., Serhan C.N., Bazan N.G. Neuroprotectin D1: a docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:8491-8496.
35. Nair V.D., McNaught K.S., Gonzalez-Maeso J., Sealfon S.C., Olanow C.W. p53 mediates nontranscriptional cell death in dopaminergic cells in response to proteasome inhibition. J. Biol. Chem. 2006, 281:39550-39560.
36. Nakamoto K., Nishinaka T. Antinociceptive effects of docosahexaenoic acid against various pain stimuli in mice. Biol. Pharm. Bull. 2010, 33:1070-1072.
37. Nakazato-Imasato E., Kurebayashi Y. Pharmacological characteristics of the hind paw weight bearing difference induced by chronic constriction injury of the sciatic nerve in rats. Life Sci. 2009, 84:622-626.
38. Ohara P.T., Vit J., Bhargava A., Romero M., Sundberg C., Charles A.C., Jasmin L. Gliopathic pain: when satellite glial cells go bad. Neuroscientist 2009, 15:450-463.
39. Ohara P.T., Vit J.P., Bhargava A., Jasmin L. Evidence for a role of connexin 43 in trigeminal pain using RNA interference in vivo. J. Neurophysiol. 2008, 100:3064-3073.
40. Ohtori S., Takahachi K., Moriya H., Myers R.R. TNF-alpha and TNF-alpha receptor type 1 upregulation in glia and neurons after peripheral nerve injury. Spine 2004, 29:1082-1088.
41. Otoshi K., Kikuchi S., Konno S., Sekiguchi M. The reactions of glial cells and endoneurial macrophages in the dorsal root ganglion and their contribution to pain-related behavior after application of nucleus pulposus onto the nerve root in rats. Spine 2010, 35:10-17.
42. Perez J., Ware M.A., Chevalier S., Gougeon R., Shir Y. Dietary omega-3 fatty acids may be associated with increased neuropathic pain in nerve-injured rats. Anesth. Analg. 2005, 101:444-448.
43. Perry M.J., Lawson S.N. Neurofilament in feline primary afferent neurones: a quantitative immunocytochemical study. Brain Res. 1993, 607:307-313.
44. Ponomarev E.D., Maresz K., Tan Y., Dittel B.N. CNS-derived interleukin-4 is essential for the regulation of autoimmune inflammation and induces a state of alternative activation in microglial cells. J. Neurosci. 2007, 27:10714-10721.
45. Schlereth T., Birklein F. The sympathetic nervous system and pain. Neuromol. Med. 2008, 10:141-147.
46. Scholz J., Broom D.C., Youn D.H., Mills C.D., Kohno T., Suter M.R., Moore K.A., Decosterd I., Coggeshall R.E., Woolf C.J. Blocking caspase activity prevents transsynaptic neuronal apoptosis and the loss of inhibition in lamina II of the dorsal horn after peripheral nerve injury. J. Neurosci. 2005, 25:7317-7323.
47. Serhan C.N., Gotlinger K., Hong S., Lu Y., Siegelman J., Baer T., Yang R., Colgan S.P., Petasis N.A. Anti-inflammatory actions of neuroprotectin D1/protectin D1 and its natural stereoisomers: assignments of dihydroxy-containing docosatrienes. J. Immunol. 2006, 176:1848-1859.
48. Serhan C.N. Novel chemical mediators in the resolution of inflammation: resolvin and protectins. Anesthesiol. Clin. 2006, 24:341-364.
49. Takeda M., Takahashi M., Matsumoto S. Contribution of activated interleukin receptors in trigeminal ganglion neurons to hyperalgesia via satellite glial interleukin-1beta paracrine mechanism. Brain Behav. Immun. 2008, 22:1016-1023.
50. Tishkina A.O. A method of automated quantitative analysis of brain slices microphotographs. Neurochem. J. 2009, 3:309-313.
51. Vit J.P., Ohara P.T., Bhargava A., Kelley K., Jasmin L. Silencing the Kir 4.1 potassium channel subunit in satellite glial cells of the rat trigeminal ganglion results in pain like behavior in the absence of nerve injury. J. Neurosci. 2008, 28:4161-4171.
52. Wang D.B., Kinoshita C., Kinoshita Y., Morrison R.S. p53 and mitochondrial function in neurons. Biochim. Biophys. Acta 2014, 1842:1186-1197.
53. Wang X., Zhao X., Mao Z.Y., Wang X.M., Liu Z.L. Neuroprotective effect of docosahexaenoic acid on glutamate-induced cytotoxicity in rat hippocampal cultures. NeuroReport 2003, 14:2457-2461.