Role of purinergic signaling pathways in the adaptogenic-like activity of methyl jasmonate in rats exposed to unpredictable chronic mild stress

Oritoke M. Aluko; Solomon Umukoro

doi:10.1515/dmpt-2020-0117

Article

Role of purinergic signaling pathways in the adaptogenic-like activity of methyl jasmonate in rats exposed to unpredictable chronic mild stress

Oritoke M. Aluko and Solomon Umukoro

Published/Copyright: July 22, 2020

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From the journal Drug Metabolism and Personalized Therapy Volume 35 Issue 3

Abstract

Objectives

Purinergic signaling pathway has been implicated in maladaptation of animals subjected to chronic stress. Previous studies have shown that methyl jasmonate (MJ) exhibited adaptogenic properties in mice exposed to unpredictable chronic mild stress (UCMS) via antioxidant and neuroprotective-related mechanisms.

Methods

This study evaluated the role of purinergic system in adaptogenic-like activity of MJ. Male Wistar rats were treated intraperitoneally with vehicle (10 mL/kg) or MJ (25, 50, or 100 mg/kg) 30 min prior exposure to UCMS. Thereafter, rats were assessed for swimming endurance in forced swim test (FST) and post-swimming motor coordination on beam walk test (BWT) apparatus. The rats’ brains were processed for adenosine triphosphate (ATP), adenosine diphosphate (ADP), adenosine deaminase, and arginase quantification. Hematological parameters, cholesterol, triglyceride, creatinine, and urea nitrogen were also determined.

Results

MJ prolonged swimming endurance time and reversed stress-induced post-swimming motor dysfunction. The altered hematological parameters induced by UCMS in rats were significantly (p<0.05) attenuated by MJ. MJ also reversed UCMS-induced alterations of total cholesterol, triglyceride, creatinine, and urea nitrogen levels. MJ averted UCMS-induced alterations in purinergic system by decreasing ATP and ADP hydrolysis, adenosine deaminase, and arginase activities in rats’ brains.

Conclusions

Overall, these findings further suggest that MJ has adaptogenic-like activity in rats exposed to UCMS, which may be related to modulation of the purinergic signaling pathway.

Keywords: adaptogen; anti-fatigue; chronic unpredictable mild stress; methyl jasmonate; purinergic signaling

Corresponding author: Oritoke M. Aluko, Department of Physiology, School of Health and Health Technology, Federal University of Technology, Akure, Nigeria; and Department of Pharmacology and Therapeutics, Faculty of Basic Medical Sciences, University of Ibadan, Ibadan, Nigeria, Phone: +2348067197998, E-mail: oritokealuko@gmail.com, omaluko@futa.edu.ng

Research funding: None declared.
Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.
Competing interests: Authors state no conflict of interest.
Ethical approval: The experimental procedures were approved by the University of Ibadan Animal Care and Use Research Ethics Committee (UI-ACUREC/App/2016/034).

References

1. Fingrut, O, Reischer, D, Rotem, R, Goldin, N, Altboum, I, Zan-Bar, I, et al. Jasmonates induce nonapoptotic death in high-resistance mutant p53-expressing B-lymphoma cells. Br J Pharmacol 2005;146:800–8. https://doi.org/10.1038/sj.bjp.0706394.Search in Google Scholar PubMed PubMed Central

2. Cesari, IM, Carvalho, E, Figueiredo, RM, Mendonça, BM, Amôedo, ND, Rumjanek, FD. Methyl jasmonate: putative mechanisms of action on cancer cells cycle, metabolism, and apoptosis. Int J Cell Biol 2014;225:698–723. https://doi.org/10.1155/2014/572097.Search in Google Scholar PubMed PubMed Central

3. Hossain, SJ, Aoshima, H, Koda, H, Kiso, Y. Fragrances in oolong tea that enhance the response of GABA-A receptors. Biosci Biotechnol Biochem 2004;68:1842–8. https://doi.org/10.1271/bbb.68.1842.Search in Google Scholar PubMed

4. Aluko, OM, Umukoro, S, Annafi, O, Adewole, FA, Omorogbe, O. Effects of methyl jasmonate on acute stress responses in mice subjected to forced swim and anoxic tests. Sci Pharm 2015;83:635–44. https://doi.org/10.3797/scipharm.1504-04.Search in Google Scholar PubMed PubMed Central

5. Umukoro, S, Aluko, OM, Eduviere, AT, Owoeye, O. Evaluation of adaptogenic-like property of methyl jasmonate in mice exposed to unpredictable chronic mild stress. Brain Res Bull 2016;121:105–14. https://doi.org/10.1016/j.brainresbull.2015.11.016.Search in Google Scholar PubMed

6. Sperlagh, B, Csolle, C, Romeo, D, Goloncser, F, Kittel, A, Baranyi, M. The role of purinergic signaling in depressive disorders. Neuropsychopharmacol Hung 2012;4:231–238. https://doi.org/10.5706/nph201212003.Search in Google Scholar

7. Burnstock, G. Purinergic signalling: therapeutic developments. Front Pharmacol 2017;8:661–75. https://doi.org/10.3389/fphar.2017.00661.Search in Google Scholar PubMed PubMed Central

8. Lindberg, D, Shan, D, Ayers-Ringler, J, Oliveros, A, Benitez, J, Prieto, M, et al. Purinergic signaling and energy homeostasis in psychiatric disorders. Curr Mol Med 2015;15:275–95. https://doi.org/10.2174/1566524015666150330163724.Search in Google Scholar PubMed PubMed Central

9. Hao, G, Zhang, C, Cao, W, Hao, J. Effects of intragastric administration of five oyster components on endurance exercise performance in mice. Pharm Biol 2014;52:723–8. https://doi.org/10.3109/13880209.2013.866966.Search in Google Scholar PubMed

10. Lamou, B, Taiwe, GS, Hamadou, A, Abene Houlray, J, Atour, MM, Tan, PV. Antioxidant and antifatigue properties of the aqueous extract of Moringa oleifera in rats subjected to forced swimming endurance test. Oxid Med Cell Longev 2016;2016:1–9. https://doi.org/10.1155/2016/3517824.Search in Google Scholar PubMed PubMed Central

11. Willner, P. Validity, reliability, and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology 2017;134:319–329. https://doi.org/10.1007/s002130050456.Search in Google Scholar

12. Ducottet, C, Griebel, G, Belzung, C. Effects of the selective non-peptide corticotropin-releasing factor receptor 1 antagonist antalarmin in the chronic mild stress model of depression in mice. Prog Neuropsychopharmacol Biol Psychiatry 2003;27:625–31. https://doi.org/10.1016/s0278-5846(03)00051-4.Search in Google Scholar

13. Nollet, M, Le Guisquet, AM, Belzung, C. Models of depression: unpredictable chronic mild stress in mice. Curr Prot Pharmacol 2013;61:5.65.1–5.65.17. https://doi.org/10.1002/0471141755.ph0565s61.Search in Google Scholar

14. Detke, MJ, Rickels, M, Lucki, I. Active behaviors in the rat forced swimming test differentially produced serotonergic and noradrenergic antidepressants. Psychopharmacology 1995;121:66–72. https://doi.org/10.1007/bf02245592.Search in Google Scholar

15. Carter, RJ, Morton, J, Dunnett, SB. Motor coordination and balance in rodents. Curr Prot Neurosci 2001;8:8–12. https://doi.org/10.1002/0471142301.ns0812s15.Search in Google Scholar

16. Leal, DBR, Streher, CA, Neu, TN, Bittencourt, FP, Leal, CAM, Silva, JEP, et al. Characterization of NTPDase (NTPDase 1; ectoapyrase; ecto-diphosphohydrolase; CD39; EC 3.6.1.5) activity in human lymphocytes. Biochim Biophys Acta 2005;1721:9–15. https://doi.org/10.1016/j.bbagen.2004.09.006.Search in Google Scholar

17. Mendez, JD, Sosa, A, Palomar-Morales, M. Effect of l-arginine on arginase activity in male accessory sex glands of alloxan-treated rats. Reprod Toxicol 2002;16:809–13. https://doi.org/10.1016/s0890-6238(02)00057-6.Search in Google Scholar

18. Dacie, JV, Lewis, SM. Practical hematology. 7th ed. London: Churchill Livingstone; 1991;227–257.Search in Google Scholar

19. Young, DS, Friedman, RB. Effects of disease on clinical laboratory tests. Washington: AACC Press; 2001;86:321–351.Search in Google Scholar

20. Bucolo, G, David, H. Quantitative determination of serum triglycerides by the use of enzymes. Clin Chem 1973;19:476–82. https://doi.org/10.1093/clinchem/19.5.476.Search in Google Scholar

21. Hallett, CJ, Cook, JGH. Reduced nicotinamide adenine dinucleotide-coupled reaction for emergency blood urea estimation. Clin Chim Acta 1971;35:33–7. https://doi.org/10.1016/0009-8981(71)90289-0.Search in Google Scholar

22. Stemmelin, J, Cohen, C, Yalcin, I, Keane, P, Griebel, G. Implication of beta3-adrenoceptors in the antidepressant-like effects of amibegron using Adrb3 knockout mice in the chronic mild stress. Behav Brain Res 2010;206:310–2. https://doi.org/10.1016/j.bbr.2009.09.003.Search in Google Scholar PubMed

23. Lam, VYY, Raineki, C, Takeuchi, LE, Ellis, L, Woodward, TS, Weinberg, J. Chronic stress alters behavior in the forced swim test and underlying neural activity in animals exposed to alcohol prenatally: sex- and time-dependent effects. Front Behav Neurosci 2018;12:142–63. https://doi.org/10.3389/fnbeh.2018.00042.Search in Google Scholar

24. Yu, ZF, Kong, LD, Chen, Y. Antidepressant activity of aqueous extracts of Curcuma longa in mice. J Ethnopharmacol 2002;83:161–5. https://doi.org/10.1016/s0378-8741(02)00211-8.Search in Google Scholar

25. Tanaka, M, Baba, Y, Kataoka, Y, Kinbara, N, Sagesaka, YM, Kakuda, T, et al. Effects of (–)-epigallocatechin gallate in liver of an animal model of combined (physical and mental) fatigue. Nutrition 2008;24:599–603. https://doi.org/10.1016/j.nut.2008.03.001.Search in Google Scholar

26. Narkhede, AN, Jagtap, SD, Nirmal, PS, Giramkar, SA, Nagarkar, BE, Kulkarni, OP, et al. Anti-fatigue effect of Amarkand on endurance exercise capacity in rats. BMC Complement Altern Med 2016;16:23–35. https://doi.org/10.1186/s12906-016-0995-2.Search in Google Scholar

27. Perez-Polo, JR, Rea, HC, Johnson, KM, Parsley, MA, Unabia, GC, Xu, GJ, et al. Inflammatory consequences in a rodent model of mild traumatic brain injury. J Neurotrauma 2013;30:727–40. https://doi.org/10.1089/neu.2012.2650.Search in Google Scholar

28. Zimmermann, FF, Altenhofen, S, Kist, LW, Leite, CE, Bogo, MR, Cognato, GP, et al. Unpredictable chronic stress alters adenosine metabolism in zebrafish brain. Mol Neurobiol 2015;53:2518–28. https://doi.org/10.1007/s12035-015-9270-7.Search in Google Scholar

29. Reiche, EM, Nunes, SO, Morimoto, HK. Stress, depression, the immune system, and cancer. Lancet Oncol 2004;5:617–25. https://doi.org/10.1016/s1470-2045(04)01597-9.Search in Google Scholar

30. Kulkarni, MP, Juvekar, AR. Effect of Alstonia scholaris (Linn) R.Br. on stress and condition in mice. Indian J Exp Biol 2008;47:47–52. https://nopr.niscair.res.in/handle/123456789/2892. PMID: 19317351.Search in Google Scholar PubMed

31. Webster, MJ, Glaser, R. Stress hormones and immune function. Cell Immunol 2008;252:16–26. https://doi.org/10.1016/j.cellimm.2007.09.006.Search in Google Scholar

32. Pardon, MC, Gould, GG, Garcia, A, Phillips, L, Cook, MC, Miller, SA, et al. Stress reactivity of the brain noradrenergic system in three strains differing in their neuroendocrine and behavioral responses to stress: implication for susceptibility to stress-related neuropsychiatric disorders. Neuroscience 2002;115:229–42. https://doi.org/10.1016/s0306-4522(02)00364-0.Search in Google Scholar

33. Sumanth, M, Mustafa, SS. Antistress, adoptogenic activity of Sida cordifolia roots in mice. Indian J Pharm Sci 2009;71:323–4. https://doi.org/10.4103/0250-474x.56027.Search in Google Scholar PubMed PubMed Central

34. Kothiyal, P, Ratan, P. Antistress effect of Fagopyrum esculentum in rats subjected to forced swimming endurance test. Pharmacology Online 2011;3:290–296. https://pharmacologyonline.silae.it/files/archives/2011/vol3/030.ratan.pdf.Search in Google Scholar

35. Ding, JF, Li, YY, Xu, JJ, Su, XR, Gao, X, Yue, FP. Study on effect of jellyfish collagen hydrolysate on anti-fatigue and anti-oxidation. Food Hydro-colloids 2011;25:1350–3. https://doi.org/10.1016/j.foodhyd.2010.12.013.Search in Google Scholar

36. Hu, Y, Gursoy, E, Cardounel, A, Kalimi, M. Biological effects of single and repeated swimming stress in male rats: beneficial effects of glucocorticoids. Endocrine 2000;13:123–9. https://doi.org/10.1385/endo:13:1:123.10.1385/ENDO:13:1:123Search in Google Scholar

37. Cortez, CM, Costa, WS, Babinski, MA, Chagas, MA. Morphometrical and stereological analysis of the superior cervical glanglion of Rattus norvegicus submitted to chronic treatment with cortisol. Int J Morph 2003;21:211–26. https://doi.org/10.4067/s0717-95022003000300006.Search in Google Scholar

38. Benchimol de Souza, D, Silva, D, Marinho Costa Silva, C, Barcellos Sampaio, FJ, Silva Costa, W, Martins Cortez, C. Effects of immobilization stress on kidneys of Wistar male rats: a morphometrical and stereological analysis. Kidney Blood Press Res 2011;34:424–29. https://doi.org/10.1159/000328331.Search in Google Scholar

39. Cunningham, JJ, Gulino, MA, Meara, PA, Bode, HH. Enhanced hepatic insulin sensitivity and peripheral glucose uptake in cold acclimating rats. Endocrinology 1985;117:1585–9. https://doi.org/10.1210/endo-117-4-1585.Search in Google Scholar

40. Chen, M, Bao, W, Ceccatelli, S, Celsi, G. Prenatal exposure to high level of glucocorticoids increases susceptibility of renal proximal tubular cells to apoptosis induced by uropathogenic Escherichia coli toxins. Am J Nephrol 2004;24:497–502. https://doi.org/10.1159/000080726.Search in Google Scholar

41. Sarumathi, A, Saravanan, N. A study on the haematological parameters and brain acetylcholine esterase activity in immobilization induced stress and co-treatment with Centella asiatica leaves extract to Wistar rats. Int J Nutri Pharmacol Neurol Dis 2013;3:102–107. https://doi.org/10.4103/2231-0738.112829.Search in Google Scholar

42. Kori, RS, Aladkatti, RH, Desai, SD, Das, KK. Effect of antistress activity of fluoxetine on restrained stress-induced male albino rats in hematological parameters and whole brain histopathology. J Young Pharm 2017;9:246–50. https://doi.org/10.5530/jyp.2017.9.48.Search in Google Scholar

43. Tian, T, Wang, Z, Zhang, J. Pathomechanisms of oxidative stress in inflammatory bowel disease and potential antioxidant therapies. Oxid Med Cell Longev 2017;2017:1–18. https://doi.org/10.1155/2017/4535194.Search in Google Scholar

44. Pickler, L, Beirao, BC, Hayashi, RM, Durau, JF, Lourenco, MC, Caron, LF, et al. Effect of sanguinarine in drinking water on Salmonella control and the expression of immune cells in peripheral blood and intestinal mucosa of broilers. J Appl Poult Res 2013;22:430–8. https://doi.org/10.3382/japr.2012-00649.Search in Google Scholar

45. Sivakumar, V, Singh, G, Varshney, V. Antioxidants supplementation on acid-base balance during heat stress in goats. Asian Aust J Anim Sci 2010;23:1462–68. https://doi.org/10.5713/ajas.2010.90471.Search in Google Scholar

46. Srikandakumar, A, Johnson, EH, Mahgoub, O. Effect of heat stress on respiratory rate, rectal temperature and blood chemistry in Omani and Australian Merino sheep. Small Ruminant Res 2003;49:193–8. https://doi.org/10.1016/s0921-4488(03)00097-x.Search in Google Scholar

Received: 2020-05-01

Accepted: 2020-06-06

Published Online: 2020-07-22

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https://doi.org/10.1515/dmpt-2020-0117

Keywords for this article

adaptogen; anti-fatigue; chronic unpredictable mild stress; methyl jasmonate; purinergic signaling