Anti-inflammatory effects of ethanolic extract of Rosmarinus officinalis L. and rosmarinic acid in a rat model of neuropathic pain

Biomedicine and Pharmacotherapy

Volumn 86, Issue , 2017, Pages 441-449

  Ghasemzadeh Rahbardar, Mahboobeh ^a   Amin, Bahareh ^b   Mehri, Soghra ^c   Mirnajafi Zadeh, Seyed Javad ^a   Hosseinzadeh, Hossein ^c  

^a TARBIAT MODARES UNIVERSITY   (Iran)

^b SABZEVAR UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c MASHHAD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Chronic constriction injury; Inflammatory markers; Neuropathic pain; Rosmarinic acid; Rosmarinus officinalis

Indexed keywords

BETA ACTIN; BIOLOGICAL MARKER; CYCLOOXYGENASE 2; GABAPENTIN; GELATINASE A; INTERLEUKIN 1BETA; NITRIC OXIDE; PROSTAGLANDIN E2; ROSMARINIC ACID; ROSMARINUS OFFICINALIS EXTRACT; ALCOHOL; ANTIINFLAMMATORY AGENT; CINNAMIC ACID DERIVATIVE; DEPSIDE; PLANT EXTRACT;

ADULT; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CHRONIC CONSTRICTION INJURY; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG EFFECT; EXPERIMENTAL SCIATIC NERVE INJURY; LUMBAR SPINAL CORD; MALE; NEUROPATHIC PAIN; NONHUMAN; OXIDATIVE STRESS; PERIPHERAL NEUROPATHY; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ROSEMARY; TRADITIONAL MEDICINE; WESTERN BLOTTING; ANIMAL; CHEMISTRY; INFLAMMATION; METABOLISM; NEURALGIA; PHYTOTHERAPY; PROCEDURES; ROSMARINUS; WISTAR RAT;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CINNAMATES; CYCLOOXYGENASE 2; DEPSIDES; DINOPROSTONE; ETHANOL; INFLAMMATION; INTERLEUKIN-1BETA; MALE; MATRIX METALLOPROTEINASE 2; NEURALGIA; PHYTOTHERAPY; PLANT EXTRACTS; RATS; RATS, WISTAR; ROSMARINUS;

EID: 85007256836     PISSN: 07533322     EISSN: 19506007     Source Type: Journal    
DOI: 10.1016/j.biopha.2016.12.049     Document Type: Article

References (66)

1. [1] Treede, R.-D., Jensen, T.S., Campbell, J., Cruccu, G., Dostrovsky, J., Griffin, J., Hansson, P., Hughes, R., Nurmikko, T., Serra, J., Neuropathic pain redefinition and a grading system for clinical and research purposes. Neurology 70 (2008), 1630–1635.
2. [2] Hervera, A., Leánez, S., Negrete, R., Motterlini, R., Pol, O., Carbon monoxide reduces neuropathic pain and spinal microglial activation by inhibiting nitric oxide synthesis in mice. PLoS One, 7, 2012, e43693.
3. [3] Attal, N., Pharmacologic treatment of neuropathic pain. Acta Neurol. Belg. 101 (2001), 53–64.
4. [4] Sacerdote, P., Franchi, S., Moretti, S., Castelli, M., Procacci, P., Magnaghi, V., Panerai, A.E., Cytokine modulation is necessary for efficacious treatment of experimental neuropathic pain. J. Neuroimmune Pharmacol. 8 (2013), 202–211.
5. [5] Old, E.A., Clark, A.K., Malcangio, M., The role of glia in the spinal cord in neuropathic and inflammatory pain. Pain Control 227 (2015), 145–170.
6. [6] Valsecchi, A.E., Franchi, S., Panerai, A.E., Rossi, A., Sacerdote, P., Colleoni, M., The soy isoflavone genistein reverses oxidative and inflammatory state neuropathic pain, neurotrophic and vasculature deficits in diabetes mouse model. Eur. J. Pharmacol. 650 (2011), 694–702.
7. [7] Liu, T., Gao, Y.-J., Ji, R.-R., Emerging role of Toll-like receptors in the control of pain and itch. Neurosci. Bull. 28 (2012), 131–144.
8. [8] Gao, Y.-J., Ji, R.-R., Targeting astrocyte signaling for chronic pain. Neurotherapeutics 7 (2010), 482–493.
9. [9] Vanegas, H., Schaible, H.-G., Prostaglandins and cycloxygenases in the spinal cord. Prog. Neurobiol. 64 (2001), 327–363.
10. [10] Vasko, M.R., Campbell, W., Waite, K., Prostaglandin E2 enhances bradykinin-stimulated release of neuropeptides from rat sensory neurons in culture. J. Neurosci. 14 (1994), 4987–4997.
11. [11] Hingtgen, C.M., Waite, K.J., Vasko, M.R., Prostaglandins facilitate peptide release from rat sensory neurons by activating the adenosine 3' 5'-cyclic monophosphate transduction cascade. ‎J. Neurosci. 15 (1995), 5411–5419.
12. [12] Costigan, M., Scholz, J., Woolf, C.J., Neuropathic pain: a maladaptive response of the nervous system to damage. Annu. Rev. Neurosci. 32 (2009), 1–32.
13. [13] Page-McCaw, A., Ewald, A.J., Werb, Z., Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell. Biol. 8 (2007), 221–233.
14. [14] Lakhan, S.E., Avramut, M., Matrix metalloproteinases in neuropathic pain and migraine: friends, enemies, and therapeutic targets. Pain. Res. Treat., 2012, 2012, 952906.
15. [15] Ji, R.-R., Xu, Z.-Z., Wang, X., Lo, E.H., Matrix metalloprotease regulation of neuropathic pain. Trends. Pharmacol. Sci. 30 (2009), 336–340.
16. [16] Amin, B., Poureshagh, E., Hosseinzadeh, H., The effect of verbascoside in neuropathic pain induced by chronic constriction injury in rats. Phytother. Res. 30 (2016), 128–135.
17. [17] Berman, J.S., Symonds, C., Birch, R., Efficacy of two cannabis based medicinal extracts for relief of central neuropathic pain from brachial plexus avulsion: results of a randomised controlled trial. Pain 112 (2004), 299–306.
18. [18] Amin, B., Abnous, K., Motamedshariaty, V., Hosseinzadeh, H., Attenuation of oxidative stress, inflammation and apoptosis by ethanolic and aqueous extracts of Crocus sativus L. stigma after chronic constriction injury of rats. An. Acad. Bras. Cienc. 86 (2014), 1821–1832.
19. [19] Al-Sereiti, M., Abu-Amer, K., Sen, P., Pharmacology of rosemary (Rosmarinus officinalis Linn.) and its therapeutic potentials. Indian J. Exp. Biol. 37 (1999), 124–130.
20. [20] Atlas de las plantas medicinales tradicionales mexicanas. Argueta, A., Cano, L., Rodarte, M., (eds.), 1994, Instituto Nacional Indigenista, México (pp. 1786).
21. [21] González-Trujano, M., Peña, E., Martínez, A., Moreno, J., Guevara-Fefer, P., Deciga-Campos, M., López-Muñoz, F., Evaluation of the antinociceptive effect of Rosmarinus officinalis L. using three different experimental models in rodents. J. Ethnopharmacol. 111 (2007), 476–482.
22. [22] Martínez, A.L., González-Trujano, M.E., Pellicer, F., López-Muñoz, F.J., Navarrete, A., Antinociceptive effect and GC/MS analysis of Rosmarinus officinalis L. essential oil from its aerial parts. Planta Med. 75 (2009), 508–511.
23. [23] Yu, M.-H., Choi, J.-H., Chae, I.-G., Im, H.-G., Yang, S.-A., More, K., Lee, I.-S., Lee, J., Suppression of LPS-induced inflammatory activities by Rosmarinus officinalis L. Food Chem. 136 (2013), 1047–1054.
24. [24] Scarpati, M.L., Oriente, G., Isolamento e costituzione dell'acido rosmarinico (dal rosmarinus off.). Ric. Sci. 28 (1958), 2329–2333.
25. [25] Makino, T., Ono, T., Muso, E., Honda, G., Inhibitory effect of Perilla frutescens and its phenolic constituents on cultured murine mesangial cell proliferation. Planta Med. 64 (1998), 541–545.
26. [26] Peng, C.-H., Su, J.-D., Chyau, C.-C., Sung, T.-Y., Ho, S.-S., Peng, C.-C., Peng, R.Y., Supercritical fluid extracts of rosemary leaves exhibit potent anti-inflammation and anti-tumor effects. Biosci. Biotechnol. Biochem. 71 (2007), 2223–2232.
27. [27] Hosseinzadeh, H., Nourbakhsh, M., Effect of Rosmarinus officinalis L. aerial parts extract on morphine withdrawal syndrome in mice. Phytother. Res. 17 (2003), 938–941.
28. [28] Osakabe, N., Yasuda, A., Natsume, M., Sanbongi, C., Kato, Y., Osawa, T., Yoshikawa, T., Rosmarinic acid a major polyphenolic component of Perilla frutescens, reduces lipopolysaccharide (LPS)-induced liver injury in D-galactosamine (D-GalN)-sensitized mice. Free Radic. Biol. Med. 33 (2002), 798–806.
29. [29] Hassani, F.V., Shirani, K., Hosseinzadeh, H., Rosemary (Rosmarinus officinalis) as a potential therapeutic plant in metabolic syndrome: a review. Naunyn Schmiedebergs Arch. Pharmacol. 389 (2016), 931–949.
30. [30] Tavafi, M., Diabetic nephropathy and antioxidants. J. Nephropathol. 2 (2013), 20–27.
31. [31] González-Vallinas, M., Reglero, G., Ramírez de Molina, A., Rosemary (Rosmarinus officinalis L.) extract as a potential complementary agent in anticancer therapy. Nutr. Cancer 67 (2015), 1223–1231.
32. [32] Ito, N., Yabe, T., Gamo, Y., Nagai, T., Oikawa, T., Yamada, H., Hanawa, T., Rosmarinic acid from Perillae Herba produces an antidepressant-like effect in mice through cell proliferation in the hippocampus. Biol. Pharm. Bull. 31 (2008), 1376–1380.
33. [33] Lee, H.J., Cho, H.-S., Park, E., Kim, S., Lee, S.-Y., Kim, C.-S., Kim, D.K., Kim, S.-J., Chun, H.S., Rosmarinic acid protects human dopaminergic neuronal cells against hydrogen peroxide-induced apoptosis. Toxicology 250 (2008), 109–115.
34. [34] Bigford, G.E., Del Rossi, G., Supplemental substances derived from foods as adjunctive therapeutic agents for treatment of neurodegenerative diseases and disorders. Adv. Nutr. 5 (2014), 394–403.
35. [35] Rahbardar, M.G., Amin, B., Mehri, S., Mirnajafi-Zadeh, S.J., Hosseinzadeh, H., Effect of alcoholic extract of aerial parts of Rosmarinus officinalis L. on pain, inflammation and apoptosis induced by chronic constriction injury (CCI) model of neuropathic pain in rats. J. Ethnopharmacol. 194 (2016), 117–130.
36. [36] Singh, D., Kennedy, D.H., The use of gabapentin for the treatment of postherpetic neuralgia. Clin. Ther. 25 (2003), 852–889.
37. [37] Heidari Vala, H., Ebrahimi Hariry, R., Sadeghi, M.R., Akhondi, M.M., Ghaffari Novin, M., Heidari, M., Evaluation of an aqueous-ethanolic extract from Rosmarinus officinalis (Rosemary) for its activity on the hormonal and cellular function of testes in adult male rat. Iran. J. Pharm. Res. 12 (2013), 445–451.
38. [38] Maneuf, Y., Luo, Z., Lee, K., α2δ and the mechanism of action of gabapentin in the treatment of pain. Semin. Cell Dev. Biol. 17 (2006), 565–570.
39. [39] Zimmermann, M., Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983), 109–110.
40. [40] Bennett, G.J., Xie, Y.-K., A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33 (1988), 87–107.
41. [41] Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976), 248–254.
42. [42] Cheng, J.K., Chiou, L.C., Mechanisms of the antinociceptive action of gabapentin. J. Pharm. Sci. 100 (2006), 471–486.
43. [43] Sant'Anna, M.B., Kusuda, R., Bozzo, T.A., Bassi, G.S., Alves-Filho, J.C., Cunha, F.Q., Ferreira, S.H., Souza, G.R., Cunha, T.M., Medial plantar nerve ligation as a novel model of neuropathic pain in mice: pharmacological and molecular characterization. Sci. Rep., 6, 2016, 26955.
44. [44] Lee, B.-S., Jun, I.-G., Kim, S.-H., Park, J.Y., Intrathecal gabapentin increases interleukin-10 expression and inhibits pro-inflammatory cytokine in a rat model of neuropathic pain. J. Korean Med. Sci. 28 (2013), 308–314.
45. [45] Kilic, F.S., Sirmagul, B., Yildirim, E., Oner, S., Erol, K., Antinociceptive effects of gabapentin & its mechanism of action in experimental animal studies. Indian J. Med. Res. 135 (2012), 630–635.
46. [46] Ellis, A., Bennett, D., Neuroinflammation and the generation of neuropathic pain. Br. J. Anaesth. 111 (2013), 26–37.
47. [47] Schäfers, M., Marziniak, M., Sorkin, L.S., Yaksh, T.L., Sommer, C., Cyclooxygenase inhibition in nerve-injury-and TNF-induced hyperalgesia in the rat. Exp. Neurol. 185 (2004), 160–168.
48. [48] Yoon, W.-J., Ham, Y.M., Kim, S.-S., Yoo, B.-S., Moon, J.-Y., Baik, J.S., Lee, N.H., Hyun, C.-G., Suppression of pro-inflammatory cytokines iNOS, and COX-2 expression by brown algae Sargassum micracanthum in RAW 264.7 macrophages. EurAsia. J. BioSci. 3 (2009), 130–143.
49. [49] Ghilardi, J.R., Svensson, C.I., Rogers, S.D., Yaksh, T.L., Mantyh, P.W., Constitutive spinal cyclooxygenase-2 participates in the initiation of tissue injury-induced hyperalgesia. ‎J. Neurosci. 24 (2004), 2727–2732.
50. [50] Svensson, C.I., Yaksh, T.L., The spinal phospholipase-cyclooxygenase-prostanoid cascade in nociceptive processing. Annu. Rev. Pharmacol. Toxicol. 42 (2002), 553–583.
51. [51] Matsunaga, A., Kawamoto, M., Shiraishi, S., Yasuda, T., Kajiyama, S., Kurita, S., Yuge, O., Intrathecally administered COX-2 but not COX-1 or COX-3 inhibitors attenuate streptozotocin-induced mechanical hyperalgesia in rats. ‎Eur. J. Pharmacol. 554 (2007), 12–17.
52. [52] Bingham, S., Beswick, P.J., Bountra, C., Brown, T., Campbell, I.B., Chessell, I.P., Clayton, N., Collins, S.D., Davey, P.T., Goodland, H., The cyclooxygenase-2 inhibitor GW406381X [2-(4-ethoxyphenyl)-3-[4-(methylsulfonyl) phenyl]-pyrazolo [1,5-b] pyridazine] is effective in animal models of neuropathic pain and central sensitization. J. Pharm. Exp. Ther. 312 (2005), 1161–1169.
53. [53] Takahashi, M., Kawaguchi, M., Shimada, K., Nakashima, T., Furuya, H., Systemic meloxicam reduces tactile allodynia development after L5 single spinal nerve injury in rats. Reg. Anesth. Pain. Med. 30 (2005), 351–355.
54. [54] Kunori, S., Matsumura, S., Okuda-Ashitaka, E., Katano, T., Audoly, L.P., Urade, Y., Ito, S., A novel role of prostaglandin E2 in neuropathic pain: blockade of microglial migration in the spinal cord. Glia 59 (2011), 208–218.
55. [55] MacMicking, J., Xie, Q.-w., Nathan, C., Nitric oxide and macrophage function. Annu. Rev. Immunol. 15 (1997), 323–350.
56. [56] Huie, R.E., Padmaja, S., The reaction of NO with superoxide. Free Rad. Res. Commun. 18 (1993), 195–199.
57. [57] Liu, T., Jiang, C.Y., Fujita, T., Luo, S.W., Kumamoto, E., Enhancement by interleukin-1β of AMPA and NMDA receptor-mediated currents in adult rat spinal superficial dorsal horn neurons. Mol. Pain, 9, 2013, 16.
58. [58] Sung, C.-S., Wen, Z.-H., Chang, W.-K., Ho, S.-T., Tsai, S.-K., Chang, Y.-C., Wong, C.-S., Intrathecal interleukin-1β administration induces thermal hyperalgesia by activating inducible nitric oxide synthase expression in the rat spinal cord. Brain Res. 1015 (2004), 145–153.
59. [59] Ferreira, S.H., Lorenzetti, B.B., Bristow, A.F., Poole, S., Interleukin-1β as a potent hyperalgesic agent antagonized by a tripeptide analogue. Nature 334 (1988), 698–700.
60. [60] Samad, T.A., Moore, K.A., Sapirstein, A., Billet, S., Allchorne, A., Poole, S., Bonventre, J.V., Woolf, C.J., Interleukin-1β-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 410 (2001), 471–475.
61. [61] Kawasaki, Y., Xu, Z.-Z., Wang, X., Park, J.Y., Zhuang, Z.-Y., Tan, P.-H., Gao, Y.-J., Roy, K., Corfas, G., Lo, E.H., Distinct roles of matrix metalloproteases in the early-and late-phase development of neuropathic pain. Nat. Med. 14 (2008), 331–336.
62. [62] Schomberg, D., Ahmed, M., Miranpuri, G., Olson, J., Resnick, D.K., Neuropathic pain: role of inflammation, immune response, and ion channel activity in central injury mechanisms. Ann. Neurosci. 19 (2012), 125–132.
63. [63] Kawasaki, Y., Xu, Z.Z., Wang, X., Park, J.Y., Zhuang, Z.Y., Tan, P.H., Gao, Y.J., Roy, K., Corfas, G., Lo, E.H., Ji, R.R., Distinct roles of matrix metalloproteases in the early- and late-phase development of neuropathic pain. Nat. Med. 14 (2008), 331–336.
64. [64] Khamse, S., Sadr, S.S., Roghani, M., Hasanzadeh, G., Mohammadian, M., Rosmarinic acid exerts a neuroprotective effect in the kainate rat model of temporal lobe epilepsy: underlying mechanisms. Pharm. Biol. 53 (2015), 1818–1825.
65. [65] Qiao, S., Li, W., Tsubouchi, R., Haneda, M., Murakami, K., Takeuchi, F., Nisimoto, Y., Yoshino, M., Rosmarinic acid inhibits the formation of reactive oxygen and nitrogen species in RAW264.7 macrophages. Free. Radic. Res. 39 (2005), 995–1003.
66. [66] Raskovic, A., Milanovic, I., Pavlovic, N., Cebovic, T., Vukmirovic, S., Mikov, M., Antioxidant activity of rosemary (Rosmarinus officinalis L.) essential oil and its hepatoprotective potential. BMC Complement. Altern. Med., 14, 2014, 225.