The influence of microglia activation on the efficacy of amitriptyline, doxepin, milnacipran, venlafaxine and fluoxetine in a rat model of neuropathic pain

European Journal of Pharmacology

Volumn 749, Issue , 2015, Pages 115-123

  Zychowska, Magdalena ^a   Rojewska, Ewelina ^a   Makuch, Wioletta ^a   Przewlocka, Barbara ^a   Mika, Joanna ^a  

^a INSTITUTE OF PHARMACOLOGY   (Poland)

Author keywords

Antidepressants; Astroglia; Microglia; Neuropathic pain

Indexed keywords

ACTIN BINDING PROTEIN; AIF1 PROTEIN, RAT; AMITRIPTYLINE; ANTIDEPRESSANT AGENT; CALCIUM BINDING PROTEIN; CYCLOHEXANOL DERIVATIVE; CYCLOPROPANE DERIVATIVE; DOXEPIN; DRUG THERAPY; FLUOXETINE; GLIAL FIBRILLARY ACIDIC PROTEIN; MILNACIPRAN; MINOCYCLINE; PHARMACOLOGY; VENLAFAXINE;

ALLODYNIA; ANALGESIA; ANIMAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECTS; DRUG EFFICACY; DRUG POTENTIATION; DRUG THERAPY; HYPERALGESIA; INJURIES; LUMBAR SPINAL CORD; MACROGLIA; MACROPHAGE; MALE; METABOLISM; MICROGLIA; NEURALGIA; NEUROPATHIC PAIN; NONHUMAN; RAT; SCIATIC NERVE; SCIATIC NERVE INJURY; SINGLE DRUG DOSE; SPINAL CORD; SPINAL CORD NERVE CELL; SPINAL GANGLION; TREATMENT OUTCOME; UPREGULATION; WISTAR RAT;

AMITRIPTYLINE; ANIMALS; ANTIDEPRESSIVE AGENTS; CALCIUM-BINDING PROTEINS; CYCLOHEXANOLS; CYCLOPROPANES; DOXEPIN; DRUG EFFECTS; DRUG THERAPY; FLUOXETINE; GANGLIA, SPINAL; HYPERALGESIA; INJURIES; MALE; METABOLISM; MICROFILAMENT PROTEINS; MICROGLIA; NEURALGIA; PHARMACOLOGY; RATS, WISTAR; SCIATIC NERVE; SPINAL CORD; THERAPEUTIC USE; TREATMENT OUTCOME;

EID: 84964290777     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2014.11.022     Document Type: Article

References (55)

1. Alhaider, A.A., Wilcox, G.L., 1993. Differential roles of 5-hydroxytryptaminelA and 5-hydroxytryptaminelB receptor subtypes in modulating spinal nociceptive transmission in mice. J. Pharmacol. Exp. Then 265, 378-385.
2. Arnold, L.M., Hess, E.V., Hudson, J.I., Welge, J.A., Berno, S.E., 2002. A randomized, placebo-controlled, double-blind, flexible-dose study of fluoxetine in the treatment of women with fibromyalgia. Am. J. Med. 112, 191-197.
3. Baldessarini, R.J., 2001. Drugs for the treatment of psychiatric disorders. In: Hardman, J.G., Limbird, L.E., Goodman Gilman, A. (Eds.), Goodman & Gilman's The Pharmacological Basis of Therapeutics, 10th ed. McGraw Hill, New York, USA, pp. 447-483.
4. Benbouzid, M., Choucair-Jaafar, N., Yalcin, I., Waltisperger, E., Muller, A., Freund-Mercier, M.J., Barrot, M., 2008. Chronic, but not acute, tricyclic antidepressant treatment alleviates neuropathic allodynia after sciatic nerve cuffing in mice. Eur. J. Pain 12, 1008-1017.
5. Bennett, G.J., Xie, Y.K., 1988. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33, 87-107.
6. Berrocoso, E., Mico, J.A., Vitton, O., Ladure, P., Newman-Tancredi, A., Depoortère, R., Bardin, L., 2011. Evaluation of milnacipran, in comparison with amitriptyline, on cold and mechanical allodynia in a rat model of neuropathic pain. Eur. J. Pharmacol. 655, 46-51.
7. Bomholt, S.F., Mikkelsen, J.D., Blackburn-Munro, G., 2005. Antinociceptive effects of the antidepressants amitriptyline, duloxetine, mirtazapine and citalopram in animal models of acute, persistent and neuropathic pain. Neuropharmacology 48, 252-263.
8. Bravo, L., Mico, J.A., Rey-Brea, R., Pérez-Nievas, B., Leza, J.C., Berrocoso, E., 2012. Depressive-like states heighten the aversion to painful stimuli in a rat model of comorbid chronic pain and depression. Anesthesiology 117, 613-625.
9. Coluzzi, F., Mattia, C., 2005. Mechanism-based treatment in chronic neuropathic pain: the role of antidepressants. Curr. Pharm. Des. 23, 2945-2960.
10. DeLeo, J.A., Tawfik, V.L., LaCroix-Fralish, M.L., 2006. The tetrapartite synapse: path to CNS sensitization and chronic pain. Pain 122, 17-21.
11. Dhami, K.S., Churchward, M.A., Baker, G.B., Todd, K.G., 2013. Fluoxetine and citalopram decrease microglial release of glutamate and d-serine to promote cortical neuronal viability following ischemic insult. Mol. Cell. Neurosci. 56, 365-374.
12. Fava, M., 2003. The role of the serotonergic and noradrenergic neurotransmitter systems in the treatment of psychological and physical symptoms of depression. J. Clin. Psychiatry 13, 26-29.
13. Feng, J., Zhang, Z., Wu, X., Mao, A., Chang, F., Deng, X., Gao, H., Ouyang, C., Dery, K.J., Le, K., Longmate, J., Marek St, C., Amand, R.P., Krontiris, T.G., Shively, J.E., 2013. Discovery of potential new gene variants and inflammatory cytokine associations with fibromyalgia syndrome by whole exome sequencing. PLoS One 8 (6), e65033. http://dx.doi.org/10.1371/journal.pone.0065033.
14. Fishbain, D., 2000. Evidence-based data on pain relief with antidepressants. Ann. Med. 32, 305-316.
15. Grundt, I.K., Nyland, H., 1994. Activation of cultured glial cells by amitriptyline and platelet activating factor. Toxicol. In Vitro 8, 1015-1020.
16. 3 receptors mediate descending facilitation and contribute to behavioral hypersensitivity via a reciprocal neuron-glial signaling cascade. Mol. Pain 10, 35. http://dx.doi.org/10.1186/1744-8069-10-35.
17. Ikeda, T., Ishida, Y., Naono, R., Takeda, R., Abe, H., Nakamura, T., Nishimori, T., 2009. Effects of intrathecal administration of newer antidepressants on mechanical allodynia in rat models of neuropathic pain. Neurosci. Res. 63, 42-46.
18. Jagla, G., Mika, J., Makuch, W., Obara, I., Wordliczek, J., Przewlocka, B., 2014. Analgesic effects of antidepressants alone and after their local co-administration with morphine in a rat model of neuropathic pain. Pharm. Rep. 66, 459-465.
19. Jesse, C.R., Wilhelm, E.A., Nogueira, C.W., 2010. Depression-like behavior and mechanical allodynia are reduced by bis selenide treatment in mice with chronic constriction injury: a comparison with fluoxetine, amitriptyline, and bupropion. Psychopharmacology 212, 513-522.
20. 3A-/- and 5-HTT-/- knock-out male mice. Pain 130, 235-248.
21. Kim, Y.S., Chu, Y., Han, L., Li, M., Li, Z., Lavinka, P.C., Sun, S., Tang, Z., Park, K., Caterina, M.J., Ren, K., Dubner, R., Wei, F., Dong, X., 2014. Central terminal sensitization of TRPV1 by descending serotonergic facilitation modulates chronic pain. Neuron 81 (4), 873-887. http://dx.doi.Org/10.1016/j.neuron.2013.12.011.
22. Kjorsvik, A., Tjolsen, A., Hole, K., 2001. Activation of spinal serotonin(2A/2 C) receptors augments nociceptive responses in the rat. Brain Res. 910, 179-181.
23. Kubera, M., Maes, M., Kenis, G., Kim, Y.-K., Lason, W., 2005. Effects of serotonin and serotonergic agonists and antagonists on the production of tumor necrosis factor α and interleukin-6. Psychiatry Res. 134, 251-258.
24. LaBuda, C.J., Little, P.J., 2005. Pharmacological evaluation of the selective spinal nerve ligation model of neuropathic pain in the rat. J. Neurosci. Methods 144, 175-181.
25. Levin, M.E., Jin, J.G., Ji, R.R., Tong, J., Pomonis, J.D., Laveiy, D.J., Miller, S.W., Chiang, L.W., 2008. Complement activation in the peripheral nervous system following the spinal nerve ligation model of neuropathic pain. Pain 137, 182-201.
26. Lim, C.M., Kim, S.W., Park, J.Y., Kim, C., Yoon, S.H., Lee, J.K., 2009. Fluoxetine affords robust neuroprotection in the postischemic brain via its anti-inflammatory effect. J. Neurosci. Res. 87, 1037-1045.
27. Liu, D., Wang, Z., Liu, S., Wang, F., Zhao, S., Hao, A., 2011. Anti-inflammatory effects of fluoxetine in lipopolysaccharide (LPS)-stimulated microglial cells. Neuropharmacology 61, 592-599.
28. Makuch, W., Mika, J., Rojewska, E., Zychowska, M., Przewlocka, B., 2013. Effects of selective and non-selective inhibitors of nitric oxide synthase on morphine- and endomorphin-1-induced analgesia in acute and neuropathic pain in rats. Neuropharmacology 75C, 445-457.
29. Marchand, F., Alloui, A., Chapuy, E., Hernandez, A., Pelissier, T., Ardid, D., Eschalier, A., 2003a. The antihyperalgesic effect of venlafaxine in diabetic rats does not involve the opioid system. Neurosci. Lett. 342, 105-108.
30. Marchand, F., Alloui, A., Chapuy, E., Jourdan, D., Pelissier, T., Ardid, D., Hernandez, A., Eschalier, A., 2003b. Evidence for a monoamine mediated, opioid-independent, antihyperalgesic effect of venlafaxine, a non-tricyclic antidepressant, in a neurogenic pain model in rats. Pain 103, 229-235.
31. Marchand, F., Alloui, A., Pelissier, T., Hernández, A., Authier, N., Alvarez, P., Eschalier, A., Ardid, D., 2003c. Evidence for an antihy-peralgesic effect of venlafaxine in vincristine-induced neuropathy in rat. Brain Res. 980, 117-120.
32. McMahon, S.B., Cafferty, W.B., Marchand, F., 2005. Immune and glial cell factors as pain mediators and modulators. Exp. Neurol. 192, 444-462.
33. Mika, J., Korostynski, M., Kaminska, D., Wawrzczak-Bargiela, A., Osikowicz, M., Makuch, W., Przewlocki, R., Przewlocka, B., 2008. Interleukin-1 alpha has antiallodynic and antihyperalgesic activities in a rat neuropathic pain model. Pain 138, 587-597.
34. Mika, J., Rojewska, E., Makuch, W., Przewlocka, B., 2010. Minocycline reduces the injury-induced expression of prodynorphin and pronociceptin in the dorsal root ganglion in a rat model of neuropathic pain. Neuroscience 165, 1420-1428.
35. Mika, J., Wawrzczak-Bargiela, A., Osikowicz, M., Makuch, W., Przewlocka, B., 2009. Attenuation of morphine tolerance by minocycline and pentoxifylline in naive and neuropathic mice. Brain Behav. Immun. 23, 75-84.
36. Mika, J., Zychowska, M., Makuch, W., Rojewska, E., Przewłocka, B., 2013b. Neuronal and immunological basis of action of antidepressants in chronic pain - clinical and experimental studies Pharmacol. Rep. 65, 1611-1625.
37. Mika, J., Zychowska, M., Popiolek-Barczyk, K., Rojewska, E., Przewlocka, B., 2013a. Importance of glial activation in neuropathic pain. Eur. J. Pharmacol. 716, 106-119.
38. Millan, M.J., 2002. Descending control of pain. Prog. Neurobiol. 66, 355-474.
39. Onal, A., Parlar, A., Ulker, S., 2007. Milnacipran attenuates hyperalgesia and potentiates antihyperalgesic effect of tramadol in rats with mononeuropathic pain. Pharmacol. Biochem. Behav. 88, 171-178.
40. Pedersen, L.H., Nielsen, A.N., Blackburn-Munro, G., 2005. Anti-nociception is selectively enhanced by parallel inhibition of multiple subtypes of monoamine transporters in rat models of persistent and neuropathic pain. Psychopharmacology 182, 551-561.
41. Rodriguez Parkitna, J., Korostynski, M., Kaminska-Chowaniec, D., Obara, I., Mika, J., Przewlocka, B., Przewlocki, R., 2006. Comparison of gene expression profiles in neuropathic and inflammatory pain. J. Physiol. Pharmacol. 57, 401-414.
42. Roman, A., Kus̈mierczyk, J., Klimek, E., Rogóẓ, Z., Nalepa, I., 2012. Effects of co-administration of fluoxetine and risperidone on properties of peritoneal and pleural macrophages in rats subjected to the forced swimming test. Pharmacol. Rep. 64, 1368-1380.
43. Sansone, R.A., Sansone, L.A., 2008. Pain, pain, go away: antidepressants and pain management. Psychiatry 5, 16-19.
44. Sindrup, S.H., Otto, M., Finnerup, N.B., Jensen, T.S., 2005. Antidepressants in the treatment of neuropathic pain. Basic Clin. Pharmacol. Toxicol. 96, 399-409.
45. Suzuki, R., Rygh, L.J., Dickenson, A.H., 2004. Bad news from the brain: descending 5-HT pathways that control spinal pain processing. Trends Pharmacol. Sci. 25, 613-617.
46. Tynan, R.J., Weidenhofer, J., Hinwood, M., Cairns, M.J., Day, T.A., Walker, F.R., 2012. A comparative examination of the anti-inflammatory effects of SSRI and SNRI antidepressants on LPS stimulated microglia. Brain Behav. Immun. 26, 469-479.
47. Vollmar, P., Haghikia, A., Dermietzel, R., Faustmann, P.M., 2008. Venlafaxine exhibits an anti-inflammatory effect in an inflammatory co-culture model. Int. J. Neuropsychopharmacol. 11, 111-117.
48. Watkins, C.C., Sawa, A., Pomper, M.G., 2014. Glia and immune cell signaling in bipolar disorder: insights from neuropharmacology and molecular imaging to clinical application. Transl. Psychiatry 4, e350.
49. Watkins, L.R., Maier, S.F., 2003. Glia: a novel drug discovery target for clinical pain. Nat. Rev. Drug Discov. 2, 973-985.
50. Wolfe, F., Cathey, M.A., Hawley, D.J., 1994. A double-blind placebo controlled trial of fluoxetine in fibromyalgia. Scand. J. Rheumatol. 23, 255-259.
51. Wrzosek, A., Obara, I., Wordliczek, J., Przewlocka, B., 2009. Efficacy of tramadol in combination with doxepin or venlafaxine in inhibition of nociceptive process in the rat model of neuropathic pain: an isobolographic analysis. J. Physiol. Pharmacol. 60, 71-78.
52. Yee-Chi, L., Phoon-Ping, Ch., 2010. A review of SSRIs and SNRIs in neuropathic pain. Expert Opin. Pharmacother. 11, 2813-2815.
53. Zimmermann, M., 1983. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16, 109-110.
54. Zychowska, M., Rojewska, E., Kreiner, G., Nalepa, I., Przewlocka, B., Mika, J., 2013a. Minocycline influences the anti-inflammatory interleukins and enhances the effectiveness of morphine under mice diabetic neuropathy. J. Neuroimmunol. 262, 35-45.
55. Zychowska, M., Rojewska, E., Przewłocka, B., Mika, J., 2013b. Mechanisms and pharmacology of diabetic neuropathy - experimental and clinical studies. Pharmacol. Rep. 65, 1601-1610.