Analgesic and antiinflammatory effects of Nigella orientalis L. seeds fixed oil: Pharmacological potentials and molecular mechanisms.


Journal

Phytotherapy research : PTR
ISSN: 1099-1573
Titre abrégé: Phytother Res
Pays: England
ID NLM: 8904486

Informations de publication

Date de publication:
Mar 2022
Historique:
revised: 17 01 2022
received: 13 10 2021
accepted: 17 01 2022
pubmed: 24 2 2022
medline: 26 3 2022
entrez: 23 2 2022
Statut: ppublish

Résumé

Nigella species have been widely used in traditional medicine. The aim of this study was to evaluate the antiinflammatory and analgesic potentials of Nigella orientalis L. seeds fixed oil (NOO). The acetic acid writhing test and the formaldehyde-induced licking paw were performed to assess the analgesic activity of the oil. The antiinflammatory activity was first evaluated in vitro by the erythrocyte membrane stabilization then in vivo by xylene- and carrageenan-induced ear and paw edema, respectively. To further understand the molecular mechanism of action of the Nigella extract, lipopolysaccharide-activated RAW 264.7 macrophages were used. Nitric oxide (NO) production was measured by Griess reaction and cell viability by MTT assay. The gene and protein expression of inflammatory mediators were assessed by RT-PCR and western blot, respectively. NOO exerted a potent analgesic effect in in vivo models of writhing test and induced edema. The analyzed molecular mechanisms revealed a role for NO and prostaglandins as molecules mediating the pharmacological effects of the extract through a mechanism involving nuclear factor-κB and mitogen-activated protein kinases. This study demonstrates, for the first time, that the fixed oil of N. orientalis has strong antinociceptive and antiinflammatory properties and might be a promising agent for the treatment of certain inflammation-related diseases.

Identifiants

pubmed: 35194856
doi: 10.1002/ptr.7400
doi:

Substances chimiques

Analgesics 0
Anti-Inflammatory Agents 0
Plant Extracts 0
Carrageenan 9000-07-1

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1372-1385

Subventions

Organisme : Algerian Ministry of Higher Education and Scientific Research for Exceptional National Program Grant
ID : PNE 2019/2020-No.115
Organisme : Consellería de Economía, Emprego e Industria, Xunta de Galicia
ID : GAIN GPC IN607B2019/10
Organisme : Instituto de Salud Carlos III
ID : PI17/00409
Organisme : Instituto de Salud Carlos III
ID : PI20/00902
Organisme : Instituto de Salud Carlos III
ID : PI18/00821
Organisme : Instituto de Salud Carlos III
ID : CB16/11/00226
Organisme : Instituto de Salud Carlos III
ID : RD16/0012/0014
Organisme : Instituto de Salud Carlos III
ID : RD21/0002/0025
Organisme : Research Executive Agency
ID : MSCA-RISE 734899
Organisme : Secretaría de Estado de Universidades, Investigación, Desarrollo e Innovación, Ministerio de Universidades
ID : FPU2018-04165
Organisme : Xunta de Galicia
ID : IN606A-2020/010
Organisme : Fondo Regional de Desarrollo Regional
ID : Exp.18/00188

Informations de copyright

© 2022 John Wiley & Sons Ltd.

Références

Abdel-Fattah, A. F. M., Matsumoto, K., & Watanabe, H. (2000). Antinociceptive effects of Nigella sativa oil and its major component, thymoquinone, in mice. European Journal of Pharmacology, 400(1), 89-97. https://doi.org/10.1016/S0014-2999(00)00340-X
Ajizian, S. J., English, B. K., & Meals, E. A. (1999). Specific inhibitors of p38 and extracellular signal-regulated kinase mitogen-activated protein kinase pathways block inducible nitric oxide synthase and tumor necrosis factor accumulation in murine macrophages stimulated with lipopolysaccharide and interferon-gamma. The Journal of Infectious Diseases, 179(4), 939-944. https://doi.org/10.1086/314659
Bentley, G. A., Newton, S. H., & Starr, J. (1983). Studies on the antinociceptive action of α-agonist drugs and their interactions with opioid mechanisms. British Journal of Pharmacology, 79(1), 125-134. https://doi.org/10.1111/j.1476-5381.1983.tb10504.x
Bindu, S., Mazumder, S., & Bandyopadhyay, U. (2020). Non-steroidal anti-inflammatory drugs (NSAIDs) and organ damage: A current perspective. Biochemical Pharmacology, 180(4), 114147. https://doi.org/10.1016/j.bcp.2020.114147
Bordoni, L., Fedeli, D., Nasuti, C., Maggi, F., Papa, F., Wabitsch, M., … Gabbianelli, R. (2019). Antioxidant and anti-inflammatory properties of Nigella sativa oil in human pre-adipocytes. Antioxidants, 8(2), 1-12. https://doi.org/10.3390/antiox8020051
Burits, M., & Bucar, F. (2000). Antioxidant activity of Nigella sativa essential oil. Phytotherapy Research, 14(5), 323-328. https://doi.org/10.1002/1099-1573(200008)14:5<323::AID-PTR621>3.0.CO;2-Q
Chemicals, O. G. (2001, December). Test No. 420. Acute oral toxicity, acute toxic class method. OECD guideline for testing of chemicals, pp. 1-14.
Chen, L., Deng, H., Cui, H., Fang, J., Zuo, Z., Deng, J., … Zhao, L. (2018). Inflammatory responses and inflammation-associated diseases in organs. Oncotarget, 9(6), 7204-7218. https://doi.org/10.18632/oncotarget.23208
de Carvalho, F. A. L., Munekata, P. E. S., Pateiro, M., Campagnol, P. C. B., Domínguez, R., Trindade, M. A., & Lorenzo, J. M. (2020). Effect of replacing backfat with vegetable oils during the shelf-life of cooked lamb sausages. LWT, 122(1), 109052. https://doi.org/10.1016/j.lwt.2020.109052
Efferth, T., & Oesch, F. (2021). Repurposing of plant alkaloids for cancer therapy: Pharmacology and toxicology. Seminars in Cancer Biology, 68(1), 143-163. https://doi.org/10.1016/j.semcancer.2019.12.010
Ersoy, N., Sener, S., Elidemir, A. Y., Evcil, E., & Dogen, E. (2016). Determination of pesticide residue present in cumin plant (Nigella orientalis L.) with LC-MS/MS and GC-MS. Asian Journal of Chemistry, 28(5), 1011-1014. https://doi.org/10.14233/ajchem.2016.19564
Farag, M. A., El-Kersh, D. M., Rasheed, D. M., & Heiss, A. G. (2017). Volatiles distribution in Nigella species (black cumin seeds) and in response to roasting as analyzed via solid-phase microextraction (SPME) coupled to chemometrics. Industrial Crops and Products, 108(7), 564-571. https://doi.org/10.1016/j.indcrop.2017.07.011
Farag, M. A., Gad, H. A., Heiss, A. G., & Wessjohann, L. A. (2014). Metabolomics driven analysis of six Nigella species seeds via UPLC-qTOF-MS and GC-MS coupled to chemometrics. Food Chemistry, 151, 333-342. https://doi.org/10.1016/j.foodchem.2013.11.032
Furman, D., Campisi, J., Verdin, E., Carrera-Bastos, P., Targ, S., Franceschi, C., … Slavich, G. M. (2019). Chronic inflammation in the etiology of disease across the life span. Nature Medicine, 25(12), 1822-1832. https://doi.org/10.1038/s41591-019-0675-0
González-Gallego, J., García-Mediavilla, M. V., Sánchez-Campos, S., & Tuñón, M. J. (2013). Anti-inflammatory and immunomodulatory properties of dietary flavonoids. In Polyphenols in Human Health and Disease (Vol. 1(Il), pp. 435-452). Amsterdam, The Netherlands: Elsevier Inc. https://doi.org/10.1016/B978-0-12-398456-2.00032-3
Hunskaar, S., & Hole, K. (1987). The formalin test in mice: Dissociation between inflammatory and non-inflammatory pain. Pain, 30(1), 103-114. https://doi.org/10.1016/0304-3959(87)90088-1
Jain, C., Khatana, S., & Vijayvergia, R. (2019). Bioactivity of secondary metabolites of various plants: A review. International Journal of Pharmaceutical Sciences and Research, 10(2), 494-504. https://doi.org/10.13040/IJPSR.0975-8232.10(2).494-04
Kazimi, M. R., Abdus Subhan, S., Anjum, K., Abbas, T., Wahab, A., & Mehmood, N. (2015). Antimicrobial activity of aqueous extract, methanolic extract and oil of Nigella sativa (Kalonji) against gram positives and gram negatives clinical isolates. International Journal of Current Research, 7(2), 12294-12299.
Kim, J., Lee, K. W., & Lee, H. J. (2013). Polyphenols suppress and modulate inflammation: Possible roles in health and disease. In Polyphenols in human health and disease (Vol. 1, pp. 393-408). Amsterdam, The Netherlands: Elsevier Inc. https://doi.org/10.1016/B978-0-12-398456-2.00029-3
Kökdil, G., & Yilmaz, H. (2005). Analysis of the fixed oils of the genus Nigella L. (Ranunculaceae) in Turkey. Biochemical Systematics and Ecology, 33(12), 1203-1209. https://doi.org/10.1016/j.bse.2005.07.013
Koster, R., Anderson, M., & De Beer, E. J. (1959). Acetic acid for analgesic screening. Federation Proceedings, 18, 412-417.
Landa, P., Marsik, P., Havlik, J., Kloucek, P., Vanek, T., & Kokoska, L. (2009). Evaluation of antimicrobial and anti-inflammatory activities of seed extracts from six Nigella species. Journal of Medicinal Food, 12(2), 408-415. https://doi.org/10.1089/jmf.2007.0600
Majdalawieh, A. F., & Fayyad, M. W. (2015). International Immunopharmacology Immunomodulatory and anti-in fl ammatory action of Nigella sativa and thymoquinone: A comprehensive review. International Immunopharmacology, 28(1), 295-304. https://doi.org/10.1016/j.intimp.2015.06.023
Matsumoto, H., Naraba, H., Ueno, A., Fujiyoshi, T., Murakami, M., Kudo, I., & Oh-ishi, S. (1998). Induction of cyclooxygenase-2 causes an enhancement of writhing response in mice. European Journal of Pharmacology, 352(1), 47-52. https://doi.org/10.1016/S0014-2999(98)00340-9
Matthaus, B., & Özcan, M. M. (2011). Fatty acids, tocopherol, and sterol contents of some Nigella species seed oil. Czech Journal of Food Sciences, 29(2), 145-150. https://doi.org/10.17221/206/2008-cjfs
Miyagawa, M. (2010). Globally harmonized system of classification and labelling of chemicals (GHS) and its implementation in Japan. Nippon Eiseigaku Zasshi. Japanese Journal of Hygiene, 65(1), 5-13. https://doi.org/10.1265/jjh.65.5
Mongelli, E., Desmarchelier, C., Coussio, J., & Ciccia, G. (1997). Biological studies of Bolax gummifera, a plant of the Falkland Islands used as a treatment of wounds. Journal of Ethnopharmacology, 56(2), 117-121. https://doi.org/10.1016/S0378-8741(97)01516-X
Mutabagani, A., & El-Mahdy, S. A. M. (1997). A study of the anti-inflammatory activity of Nigella sativa L. and thymoquinone in rats. Saudi Pharmaceutical Journal, 5(2-3), 110-113.
Pise, H. N., & Padwal, S. L. (2017). Evaluation of anti-inflammatory activity of nigella sativa: An experimental study. National Journal of Physiology, Pharmacy and Pharmacology, 7(7), 707-711. https://doi.org/10.5455/njppp.2017.7.0204705032017
Pop, R. M., Sabin, O., Suciu, Ș., Vesa, S. C., Socaci, S. A., Chedea, V. S., … Buzoianu, A. D. (2020). Nigella Sativa's anti-inflammatory and antioxidative effects in experimental inflammation. Antioxidants, 9(10), 1-13. https://doi.org/10.3390/antiox9100921
Reininger, E. A., & Bauer, R. (2006). Prostaglandin-H-synthase (PGHS)-1 and -2 microtiter assays for the testing of herbal drugs and in vitro inhibition of PGHS-isoenzyms by polyunsaturated fatty acids from Platycodi radix. Phytomedicine, 13(3), 164-169. https://doi.org/10.1016/j.phymed.2005.03.006
Saiki, P., Kawano, Y., Van Griensven, L. J. L. D., & Miyazaki, K. (2017). The anti-inflammatory effect of: Agaricus brasiliensis is partly due to its linoleic acid content. Food & Function, 8(11), 4150-4158. https://doi.org/10.1039/c7fo01172e
Sakai, J., Cammarota, E., Wright, J. A., Cicuta, P., Gottschalk, R. A., Li, N., … Bryant, C. E. (2017). Lipopolysaccharide-induced NF-κB nuclear translocation is primarily dependent on MyD88, but TNFα expression requires TRIF and MyD88. Scientific Reports, 7(1), 1-9. https://doi.org/10.1038/s41598-017-01600-y
Saleem, T. M., Azeem, A. K., Dilip, C., Sankar, C., Prasanth, N. V., & Duraisami, R. (2011). Anti-inflammatory activity of the leaf extacts of Gendarussa vulgaris Nees. Asian Pacific Journal of Tropical Biomedicine, 1(2), 147-149. https://doi.org/10.1016/S2221-1691(11)60014-2
Salehi, B., Quispe, C., Imran, M., Ul-Haq, I., Živković, J., Abu-Reidah, I. M., … Sharifi-Rad, J. (2021). Nigella plants - Traditional uses, bioactive phytoconstituents, preclinical and clinical studies. Frontiers in Pharmacology, 12(4), 1-26. https://doi.org/10.3389/fphar.2021.625386
Salvemini, D., Wang, Z. Q., Wyatt, P. S., Bourdon, D. M., Marino, M. H., Manning, P. T., & Currie, M. G. (1996). Nitric oxide: A key mediator in the early and late phase of carrageenan-induced rat paw inflammation. British Journal of Pharmacology, 118(4), 829-838. https://doi.org/10.1111/j.1476-5381.1996.tb15475.x
Schindler, J. F., Monahan, J. B., & Smith, W. G. (2003). p38 pathway kinases as anti-inflammatory drug targets. Critical Reviews in Oral Biology & Medicine, 86(9), 800-811.
Scotece, M., Conde, J., Abella, V., López, V., Francisco, V., Ruiz, C., … Gualillo, O. (2018). Oleocanthal inhibits catabolic and inflammatory mediators in LPS-activated human primary osteoarthritis (OA) chondrocytes through MAPKs/NF-κB pathways. Cellular Physiology and Biochemistry, 49(6), 2414-2426. https://doi.org/10.1159/000493840
Seibert, K., Zhang, Y., Leahy, K., Hauser, S., Masferrer, J., Perkins, W., … Isakson, P. (1994). Pharmacological and biochemical demonstration of the role of cyclooxygenase 2 in inflammation and pain. Proceedings of the National Academy of Sciences of the United States of America, 91(25), 12013-12017. https://doi.org/10.1073/pnas.91.25.12013
Serrat, N., Sebastian, C., Pereira-Lopes, S., Valverde-Estrella, L., Lloberas, J., & Celada, A. (2014). The response of secondary genes to lipopolysaccharides in macrophages depends on histone deacetylase and phosphorylation of C/EBPβ. The Journal of Immunology, 192(1), 418-426. https://doi.org/10.4049/jimmunol.1203500
Singh, S., Nair, V., Jain, S., & Gupta, Y. K. (2008). Evaluation of anti-inflammatory activity of plant lipids containing α-linolenic acid. Indian Journal of Experimental Biology, 46(6), 453-456.
Smith, R. J., Sabin, C., Gilchrest, H., & Williams, S. (1976). Effect of anti-inflammatory drugs on lysosomes and lysosomal enzymes from rat liver. Biochemical Pharmacology, 25(19), 2171-2177. https://doi.org/10.1016/0006-2952(76)90129-5
Swanson, L., Katkar, G. D., Tam, J., Pranadinata, R. F., Chareddy, Y., Coates, J., … Ghosh, P. (2020). TLR4 signaling and macrophage inflammatory responses are dampened by GIV/Girdin. Proceedings of the National Academy of Sciences of the United States of America, 117(43), 26895-26906. https://doi.org/10.1073/pnas.2011667117
Tjølsen, A., Berge, O. G., Hunskaar, S., Rosland, J. H., & Hole, K. (1992). The formalin test: An evaluation of the method. Pain, 51(1), 5-17. https://doi.org/10.1016/0304-3959(92)90003-T
Wang, F. L., Wang, H., Wang, J. H., Wang, D. X., Gao, Y., Yang, B., … Xin, G. S. (2021). Analgesic and anti-inflammatory activities of sophocarpine from Sophora viciifolia hance. BioMed Research International, 2021, 8893563. https://doi.org/10.1155/2021/8893563
Winter, C. A., Risley, E. A., & Nuss, G. W. (1962). Carrageenin-induced edema in hind paw of the rat as an assay for antiinflammatory drugs. Proceedings of the Society for Experimental Biology and Medicine, 111(3), 544-547. https://doi.org/10.3181/00379727-111-27849
Xu, Q., Wang, Y., Guo, S., Shen, Z., Wang, Y., & Yang, L. (2014). Anti-inflammatory and analgesic activity of aqueous extract of Flos populi. Journal of Ethnopharmacology, 152(3), 540-545. https://doi.org/10.1016/j.jep.2014.01.037
Zhang, H., & Tsao, R. (2016). Dietary polyphenols, oxidative stress and antioxidant and anti-inflammatory effects. Current Opinion in Food Science, 8, 33-42. https://doi.org/10.1016/j.cofs.2016.02.002

Auteurs

Djedjiga Ait Eldjoudi (D)

Laboratoire de Biotechnologies Végétales et Ethnobotanique, Faculté des Sciences de la Nature et de la Vie, Université de Bejaia, Bejaia, Algeria.
SERGAS (Servizo Galego de Saude) and IDIS (Instituto de Investigación Sanitaria de Santiago), NEIRID Lab (Neuroendocrine Interactions in Rheumatology and Inflammatory Diseases), Research Laboratory 9, Santiago University Clinical Hospital, Santiago de Compostela, Spain.

Clara Ruiz-Fernandez (C)

SERGAS (Servizo Galego de Saude) and IDIS (Instituto de Investigación Sanitaria de Santiago), NEIRID Lab (Neuroendocrine Interactions in Rheumatology and Inflammatory Diseases), Research Laboratory 9, Santiago University Clinical Hospital, Santiago de Compostela, Spain.

María González-Rodriguez (M)

SERGAS (Servizo Galego de Saude) and IDIS (Instituto de Investigación Sanitaria de Santiago), NEIRID Lab (Neuroendocrine Interactions in Rheumatology and Inflammatory Diseases), Research Laboratory 9, Santiago University Clinical Hospital, Santiago de Compostela, Spain.

Sihem Ait Atmane (S)

Laboratoire de Biotechnologies Végétales et Ethnobotanique, Faculté des Sciences de la Nature et de la Vie, Université de Bejaia, Bejaia, Algeria.

Alfonso Cordero-Barreal (A)

SERGAS (Servizo Galego de Saude) and IDIS (Instituto de Investigación Sanitaria de Santiago), NEIRID Lab (Neuroendocrine Interactions in Rheumatology and Inflammatory Diseases), Research Laboratory 9, Santiago University Clinical Hospital, Santiago de Compostela, Spain.

Yousof Farrag (Y)

SERGAS (Servizo Galego de Saude) and IDIS (Instituto de Investigación Sanitaria de Santiago), NEIRID Lab (Neuroendocrine Interactions in Rheumatology and Inflammatory Diseases), Research Laboratory 9, Santiago University Clinical Hospital, Santiago de Compostela, Spain.

Jesus Pino (J)

SERGAS (Servizo Galego de Saude) and IDIS (Instituto de Investigación Sanitaria de Santiago), NEIRID Lab (Neuroendocrine Interactions in Rheumatology and Inflammatory Diseases), Research Laboratory 9, Santiago University Clinical Hospital, Santiago de Compostela, Spain.

Jorge Sineiro (J)

Department of Chemical Engineering, University of Santiago de Compostela, Santiago de Compostela, Spain.

Francisca Lago (F)

Molecular and Cellular Cardiology Group, SERGAS (Servizo Galego de Saude) and IDIS (Instituto de Investigación Sanitaria de Santiago), Research Laboratory 7, Santiago University Clinical Hospital, Santiago de Compostela, Spain.

Javier Conde-Aranda (J)

IDIS (Instituto de Investigación Sanitaria de Santiago), Grupo de Gastroenterología Molecular y Celular, Santiago University Clinical Hospital, Santiago de Compostela, Spain.

Bachra Khettal (B)

Laboratoire de Biotechnologies Végétales et Ethnobotanique, Faculté des Sciences de la Nature et de la Vie, Université de Bejaia, Bejaia, Algeria.

Oreste Gualillo (O)

SERGAS (Servizo Galego de Saude) and IDIS (Instituto de Investigación Sanitaria de Santiago), NEIRID Lab (Neuroendocrine Interactions in Rheumatology and Inflammatory Diseases), Research Laboratory 9, Santiago University Clinical Hospital, Santiago de Compostela, Spain.

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