Download PDF
Planta Med 2016; 82(07): 612-620
DOI: 10.1055/s-0042-102062
Biological and Pharmacological Activity
Original Papers
Georg Thieme Verlag KG Stuttgart · New York

Effect of Ginger and Turmeric Rhizomes on Inflammatory Cytokines Levels and Enzyme Activities of Cholinergic and Purinergic Systems in Hypertensive Rats

Ayodele Jacob Akinyemi
1   Functional Foods and Nutraceuticals Unit, Department of Biochemistry, Federal University of Technology, Akure, Nigeria
2   Department of Biochemistry, Afe Babalola University, Ado-Ekiti, Nigeria
3   Programa de Pós Graduação em Ciências Biológicas: Bioquímica Toxicológica, Centro de Ciências Naturais e Exatas, Universidade Federal de Santa Maria, Camobi, Santa Maria, RS, Brazil
,
Gustavo Roberto Thomé
3   Programa de Pós Graduação em Ciências Biológicas: Bioquímica Toxicológica, Centro de Ciências Naturais e Exatas, Universidade Federal de Santa Maria, Camobi, Santa Maria, RS, Brazil
,
Vera Maria Morsch
3   Programa de Pós Graduação em Ciências Biológicas: Bioquímica Toxicológica, Centro de Ciências Naturais e Exatas, Universidade Federal de Santa Maria, Camobi, Santa Maria, RS, Brazil
,
Nathieli B. Bottari
3   Programa de Pós Graduação em Ciências Biológicas: Bioquímica Toxicológica, Centro de Ciências Naturais e Exatas, Universidade Federal de Santa Maria, Camobi, Santa Maria, RS, Brazil
,
Jucimara Baldissarelli
3   Programa de Pós Graduação em Ciências Biológicas: Bioquímica Toxicológica, Centro de Ciências Naturais e Exatas, Universidade Federal de Santa Maria, Camobi, Santa Maria, RS, Brazil
,
Lizielle Souza de Oliveira
3   Programa de Pós Graduação em Ciências Biológicas: Bioquímica Toxicológica, Centro de Ciências Naturais e Exatas, Universidade Federal de Santa Maria, Camobi, Santa Maria, RS, Brazil
,
Jeferson Ferraz Goularte
4   Health Basic Sciences Institute, Department of Physiology, Federal University of Rio Grande do Sul, Porto Alegre, RS, Brazil
,
Adriane Belló-Klein
4   Health Basic Sciences Institute, Department of Physiology, Federal University of Rio Grande do Sul, Porto Alegre, RS, Brazil
,
Thiago Duarte
5   Centro de Ciências da Saude, Universidade Luterana do Brazil (ULBRA), Campus Santa Maria, Santa Maria, RS, Brazil
,
Marta Duarte
5   Centro de Ciências da Saude, Universidade Luterana do Brazil (ULBRA), Campus Santa Maria, Santa Maria, RS, Brazil
,
Aline Augusti Boligon
6   Departamento de Farmácia Industrial, Programa de Pós Graduação em Ciências Farmacêuticas, Universidade Federal de Santa Maria, Camobi, Santa Maria, Rio Grande do Sul, Brazil
,
Margareth Linde Athayde
6   Departamento de Farmácia Industrial, Programa de Pós Graduação em Ciências Farmacêuticas, Universidade Federal de Santa Maria, Camobi, Santa Maria, Rio Grande do Sul, Brazil
,
Akintunde Afolabi Akindahunsi
1   Functional Foods and Nutraceuticals Unit, Department of Biochemistry, Federal University of Technology, Akure, Nigeria
,
Ganiyu Oboh
1   Functional Foods and Nutraceuticals Unit, Department of Biochemistry, Federal University of Technology, Akure, Nigeria
,
Maria Rosa Chitolina Schetinger
3   Programa de Pós Graduação em Ciências Biológicas: Bioquímica Toxicológica, Centro de Ciências Naturais e Exatas, Universidade Federal de Santa Maria, Camobi, Santa Maria, RS, Brazil
› Author Affiliations
Further Information

Publication History

received 19 August 2015
revised 15 January 2016

accepted 21 January 2016

Publication Date:
22 March 2016 (online)

    Permissions and Reprints

Abstract

Inflammation exerts a crucial pathogenic role in the development of hypertension. Hence, the aim of the present study was to investigate the effects of ginger (Zingiber officinale) and turmeric (Curcuma longa) on enzyme activities of purinergic and cholinergic systems as well as inflammatory cytokine levels in Nω-nitro-L-arginine methyl ester hydrochloride-induced hypertensive rats. The rats were divided into seven groups (n = 10); groups 1–3 included normotensive control rats, hypertensive (Nω-nitro-L-arginine methyl ester hydrochloride) rats, and hypertensive control rats treated with atenolol (an antihypertensive drug), while groups 4 and 5 included normotensive and hypertensive (Nω-nitro-L-arginine methyl ester hydrochloride) rats treated with 4 % supplementation of turmeric, respectively, and groups 6 and 7 included normotensive and hypertensive rats treated with 4 % supplementation of ginger, respectively. The animals were induced with hypertension by oral administration of Nω-nitro-L-arginine methyl ester hydrochloride, 40 mg/kg body weight. The results revealed a significant increase in ATP and ADP hydrolysis, adenosine deaminase, and acetylcholinesterase activities in lymphocytes from Nω-nitro-L-arginine methyl ester hydrochloride hypertensive rats when compared with the control rats. In addition, an increase in serum butyrylcholinesterase activity and proinflammatory cytokines (interleukin-1 and − 6, interferon-γ, and tumor necrosis factor-α) with a concomitant decrease in anti-inflammatory cytokines (interleukin-10) was observed in Nω-nitro-L-arginine methyl ester hydrochloride hypertensive rats. However, dietary supplementation of both rhizomes was efficient in preventing these alterations in hypertensive rats by decreasing ATP hydrolysis, acetylcholinesterase, and butyrylcholinesterase activities and proinflammatory cytokines in hypertensive rats. Thus, these activities could suggest a possible insight about the protective mechanisms of the rhizomes against hypertension-related inflammation.

Key words

Zingiber officinale - Curcuma longa - Zingiberaceae - hypertension - inflammation - cytokines
 

  • References

  • 1 Virdis A, DellʼAgnello U, Taddei S. Impact of inflammation on vascular disease in hypertension. Maturitas 2014; 78: 179-183
    CrossrefPubMedGoogle Scholar
  • 2 Virdis A, Schiffrin EL. Vascular inflammation: a role in vascular disease in hypertension. Curr Opin Nephrol Hypertens 2003; 12: 181-187
    CrossrefPubMedGoogle Scholar
  • 3 Vita JA, Keaney jr. JF. Endothelial function: a barometer for cardiovascular risk?. Circulation 2002; 106: 640-642
    CrossrefPubMedGoogle Scholar
  • 4 Cardoso AM, Abdalla FH, Bagatini MD, Martins CC, Fiorin F, Baldissarelli J, Costa P, de Mello FF, Fiorenza AM, da Silva Serres JD, Goncalves JF, Chaves H, Royes LFF, Bello-Klein A, Morsch VM, Schetinger MRC. Swimming training prevents alterations in acetylcholinesterase and butyrylcholinesterase activities in hypertensive rats. Am J Hypertens 2014; 27: 522-529
    CrossrefPubMedGoogle Scholar
  • 5 Fürstenau CR, Trentin DS, Gossenheimer AN, Ramos DB, Casali EA, Barreto-Chaves MLM, Sarkis JJF. Ectonucleotidase activities are altered in serum and platelets of L-NAME-treated rats. Blood Cells Mol Dis 2008; 41: 223-229
    CrossrefPubMedGoogle Scholar
  • 6 Delves PJ, Roitt IM. The immune system. Second of two parts. N Engl J Med 2000; 343: 108-117
    CrossrefPubMedGoogle Scholar
  • 7 Bours MJ, Swennen EL, Di Virgilio F, Cronstein BN, Dagnelie PC. Adenosine 5′-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol Ther 2006; 112: 358-404
    CrossrefPubMedGoogle Scholar
  • 8 Bertoncheli Cde M, Zimmermann CE, Jaques JA, Leal CA, Ruchel JB, Rocha BC, Pinheiro Kde V, Souza Vdo C, Stainki DR, Luz SC, Schetinger MR, Leal DB. Increased NTPDase activity in lymphocytes during experimental sepsis. ScientificWorldJournal 2012; 2012: 941906
    PubMedGoogle Scholar
  • 9 Rodrigues R, Debom G, Soares F, Machado C, Pureza J, Peres W, de Lima Garcias G, Duarte MF, Schetinger MR, Stefanello F, Braganhol E, Spanevello R. Alterations of ectonucleotidases and acetylcholinesterase activities in lymphocytes of Down syndrome subjects: relation with inflammatory parameters. Clin Chim Acta 2014; 433: 105-110
    CrossrefPubMedGoogle Scholar
  • 10 Polachini CR, Spanevello RM, Casali EA, Zanini D, Pereira LB, Martins CC, Baldissareli J, Cardoso AM, Duarte MF, da Costa P, Prado AL, Schetinger MR, Morsch VM. Alterations in the cholinesterase and adenosine deaminase activities and inflammation biomarker levels in patients with multiple sclerosis. Neuroscience 2014; 266: 266-274
    CrossrefPubMedGoogle Scholar
  • 11 Hasko G, Linden J, Cronstein B, Pacher P. Adenosine receptors: therapeutic aspects for inflammatory and immune diseases. Nat Rev Drug Discov 2008; 7: 759-770
    CrossrefPubMedGoogle Scholar
  • 12 Yegutkin GG. Nucleotide- and nucleoside-converting ectoenzymes: important modulators of purinergic signalling cascade. Biochim Biophys Acta 2008; 1783: 673-694
    CrossrefPubMedGoogle Scholar
  • 13 Cordero OJ, Salgado FJ, Fernández-Alonso CM, Herrera C, Lluis C, Franco R, Nogueira M. Cytokines regulate membrane adenosine deaminase on human activated lymphocytes. J Leukoc Biol 2001; 70: 920-930
    PubMedGoogle Scholar
  • 14 Das UN. Acetylcholinesterase and butyrylcholinesterase as possible markers of low-grade systemic inflammation. Med Sci Monit 2007; 13: RA214-RA221
    PubMedGoogle Scholar
  • 15 Reyes-Gordillo K, Segovia J, Shibayama M, Vergara P, Moreno MG, Muriel P. Curcumin protects against acute liver damage in the rat by inhibiting NF-kappaB, proinflammatory cytokines production and oxidative stress. Biochim Biophys Acta 2007; 1770: 989-996
    CrossrefPubMedGoogle Scholar
  • 16 Chan EWC, Lim Y, Wong SK, Lim KK, Tan SP, Lintao FS, Yong MY. Effects of different drying methods on the antioxidant properties of leaves and tea of ginger species. Food Chem 2009; 113: 166-172
    CrossrefPubMedGoogle Scholar
  • 17 Mann A. Biopotency role of culinary spices and herbs and their chemical constituents in health and commonly used spices in Nigerian dishes and snacks. African J Food Sci 2011; 5: 111-124
    PubMedGoogle Scholar
  • 18 Ahmad RS, Sharma SB. Biochemical studies on combined effect of garlic (Allium sativum Linn) and ginger (Zingiber officinale Rosc) in albino rats. Indian J Exp Biol 1997; 35: 841-843
    PubMedGoogle Scholar
  • 19 Jeena K, Liju VB, Viswanathan R, Kuttan R. Antimutagenic potential and modulation of carcinogen-metabolizing enzymes by ginger essential oil. Phytother Res 2014; 28: 849-855
    CrossrefPubMedGoogle Scholar
  • 20 Ajayi BO, Adedara IA, Farombi EO. Pharmacological activity of 6-gingerol in dextran sulphate sodium-induced ulcerative colitis in BALB/c mice. Phytother Res 2015; 29: 566-572
    CrossrefPubMedGoogle Scholar
  • 21 Maghbooli M, Golipour F, Moghimi EA, Yousefi M. Comparison between the efficacy of ginger and sumatriptan in the ablative treatment of the common migraine. Phytother Res 2014; 28: 412-425
    CrossrefPubMedGoogle Scholar
  • 22 Ghayur MN, Gilani AH. Ginger lowers blood pressure through blockade of voltage-dependent calcium channels. J Cardiovasc Pharmacol 2005; 45: 74-80
    CrossrefPubMedGoogle Scholar
  • 23 Jurenka JS. Anti-inflammatory properties of curcumin, major constituent of Curcuma longa: a review of preclinical and clinical research. Altern Med Rev 2009; 14: 141-153
    PubMedGoogle Scholar
  • 24 Hatcher H, Planalp R, Cho J, Torti FM, Torti SV. Curcumin: from ancient medicine to current clinical trials. Cell Mol Life Sci 2008; 65: 1631-1652
    CrossrefPubMedGoogle Scholar
  • 25 Aggarwal BB, Harikumar KB. Potential therapeutic effects of curcumin, the anti-inflammatory agent, against neurodegenerative, cardiovascular, pulmonary, metabolic, autoimmune and neoplasic diseases. Int J Biochem Cell Biol 2009; 41: 40-49
    CrossrefPubMedGoogle Scholar
  • 26 Abe Y, Hashimoto S, Horie T. Curcumin inhibition of inflammatory cytokine production by human peripheral blood monocytes and alveolar macrophages. Pharmacol Res 1999; 39: 41-47
    CrossrefPubMedGoogle Scholar
  • 27 Tian N, Moore RS, Braddy S, Rose RA, Gu JW, Hughson MD, Manning jr. RD. Interactions between oxidative stress and inflammation in salt-sensitive hypertension. Am J Physiol Heart Circ Physiol 2007; 293: H3388-H3395
    CrossrefPubMedGoogle Scholar
  • 28 Meloche J, Renard S, Provencher S, Bonnet S. Anti-inflammatory and immunosuppressive agents in PAH. Handb Exp Pharmacol 2013; 218: 437-476
    PubMedGoogle Scholar
  • 29 Kherbeck N, Tamby MC, Bussone G, Dib H, Perros F, Humbert M, Mouthon L. The role of inflammation and autoimmunity in the pathophysiology of pulmonary arterial hypertension. Clin Rev Allergy Immunol 2013; 44: 31-38
    CrossrefPubMedGoogle Scholar
  • 30 Stenmark KR, Rabinovitch M. Emerging therapies for the treatment of pulmonary hypertension. Pediatr Crit Care Med 2010; 11: S85-S90
    CrossrefPubMedGoogle Scholar
  • 31 Spanevello RM, Mazzanti CM, Bagatini M, Correa M, Schmatz R, Stefanello N, Thomé G, Morsch VM, Becker L, Bellé L, de Oliveira L, Schetinger MR. Activities of the enzymes that hydrolyse adenine nucleotides in platelets from multiples sclerosis patients. J Neurol 2010; 257: 24-30
    CrossrefPubMedGoogle Scholar
  • 32 Jacob F, Perez Novo C, Bachert C, Van Crombrugge K. Purinergic signaling in inflammatory cells: P2 receptor expression, functional effects, and modulation of inflammatory responses. Purinergic Signal 2013; 9: 285-306
    CrossrefPubMedGoogle Scholar
  • 33 Burnstock G. Purinergic regulation of vascular tone and remodelling. Auton Autacoid Pharmacol 2009; 29: 63-72
    CrossrefPubMedGoogle Scholar
  • 34 Burnstock G, Ralevic V. Purinergic signaling and blood vessels in health and disease. Pharmacol Rev 2014; 66: 102-192
    PubMedGoogle Scholar
  • 35 Burnstock G, Pelleg A. Cardiac purinergic signalling in health and disease. Purinergic Signal 2015; 11: 1-46
    CrossrefPubMedGoogle Scholar
  • 36 Kaizer RR, Gutierres JM, Schmatz R, Spanevello RM, Morsch VM, Schetinger MR, Rocha JB. In vitro and in vivo interactions of aluminum on NTPDase and AChE activities in lymphocytes of rats. Cell Immunol 2010; 265: 133-138
    CrossrefPubMedGoogle Scholar
  • 37 Nizri E, Hamra-Amitay Y, Sicsic C, Lavon I, Brenner T. Anti-inflammatory properties of cholinergic up-regulation: a new role for acetylcholinesterase inhibitors. Neuropharmacology 2006; 50: 540-547
    CrossrefPubMedGoogle Scholar
  • 38 Abdalla FH, Cardoso AM, Pereira LB, Schmatz R, Goncalves JF, Stefanello N, Fiorenza AM, Gutierres JM, Serres JD, Zanini D, Pimentel VC, Vieira JM, Schetinger MR, Morsch VM, Mazzanti CM. Neuroprotective effect of quercetin in ectoenzymes and acetylcholinesterase activities in cerebral cortex synaptosomes of cadmium-exposed rats. Mol Cell Biochem 2013; 381: 1-8
    CrossrefPubMedGoogle Scholar
  • 39 de Almeida JP, Saldanha C. Non neuronal cholinergic system in human erythrocytes: biological role and clinical relevance. J Membr Biol 2010; 234: 227-234
    CrossrefPubMedGoogle Scholar
  • 40 van Westerloo DJ. The vagal immune reflex: a blessing from above. Wien Med Wochenschr 2010; 160: 112-117
    CrossrefPubMedGoogle Scholar
  • 41 Cerejeira J, Nogueira V, Luıs P, Vaz-Serra A, Mukaetova-Ladinska EB. The cholinergic system and inflammation: common pathways in delirium pathophysiology. J Am Geriatr Soc 2012; 60: 669-675
    CrossrefPubMedGoogle Scholar
  • 42 Guardia T, Rotelli AE, Juarez AO, Pelzer LE. Anti-inflammatory properties of plant flavonoids. Effects of rutin, quercetin and hesperidin on adjuvant arthritis in rat. Farmaco 2001; 56: 683-687
    CrossrefPubMedGoogle Scholar
  • 43 Chao CY, Mong MC, Chan KC, Yin MC. Anti-glycative and anti-inflammatory effects of caffeic acid and ellagic acid in kidney of diabetic mice. Mol Nutr Food Res 2010; 54: 388-395
    CrossrefPubMedGoogle Scholar
  • 44 Kroes BH, van den Berg AJ, Quarles van Ufford HC, van Dijk H, Labadie RP. Anti-inflammatory activity of gallic acid. Planta Med 1992; 58: 499-504
    Article in Thieme ConnectPubMedGoogle Scholar
  • 45 Nakmareong S, Kukongviriyapan V, Kongyingyoes B, Sompamit K, Phisalaphong C. Antioxidant and vascular protective effects of curcumin and tetrahydrocurcumin in rats with L-NAME-induced hypertension. Naunyn Schmiedebergs Arch Pharmacol 2011; 383: 519-529
    CrossrefPubMedGoogle Scholar
  • 46 Akinyemi AJ, Ademiluyi AO, Oboh G. Inhibition of angiotensin-1-converting enzyme activity by two varieties of ginger (Zingiber officinale) in rats fed a high cholesterol diet. J Med Food 2014; 17: 317-323
    CrossrefPubMedGoogle Scholar
  • 47 Böyum A. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Invest Suppl 1968; 97: 77-89
    PubMedGoogle Scholar
  • 48 Bergmeyer H. Methods of enzymatic analysis. Weinheim: Wiley-Verlag Chemie; 1983
    Google Scholar
  • 49 Paim FC, Duarte MMMF, Costa MM, Da Silva AS, Wolkmer P, Silva CB, Paim CB, França RT, Mazzanti CM, Monteiro SG, Krause A, Lopes ST. Cytokines in rats experimentally infected with Trypanosoma evansi . Exp Parasitol 2011; 128: 365-370
    CrossrefPubMedGoogle Scholar
  • 50 Leal DB, Streher CA, Neu TN, Bittencourt FP, Leal CA, da Silva JE, Morsch VM, Schetinger MR. Characterization of NTPDase (NTPDase1; ecto-apyrase; ecto-diphosphohydrolase; CD39; EC 3.6.1.5) activity in human lymphocytes. Biochim Biophys Acta 2005; 1721: 9-15
    CrossrefPubMedGoogle Scholar
  • 51 Chan K, Delfert D, Junger KD. A direct colorimetric assay for Ca2-ATPase activity. Anal Biochem 1986; 157: 375-378
    CrossrefPubMedGoogle Scholar
  • 52 Giusti G, Gakis C. Temperature conversion factors, activation energy, relative substrate specificity and optimum pH of adenosine deaminase from human serum and tissues. Enzyme 1971; 12: 417-425
    PubMedGoogle Scholar
  • 53 Ellman GL, Courtney KD, Andres Jr V, Feather-Stone RM. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 1961; 7: 88-95
    CrossrefPubMedGoogle Scholar
  • 54 Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-254
    CrossrefPubMedGoogle Scholar
  • 55 Barbosa-Filho VM, Waczuk EP, Kamdem JP, Abolaji AO, Lacerda SR, da Costa JGM, Alencar de Menezes IR, Augusti Boligon A, Athayde ML, Teixeira da Rocha JB, Posser T. Phytochemical constituents, antioxidant activity, cytotoxicity andosmotic fragility effects of Caju (Anacardium microcarpum). Ind Crops Prod 2014; 55: 280-288
    CrossrefPubMedGoogle Scholar