Paullinia cupana (Kunth) stimulates behavior patterns and regulates oxidative stress markers in lobster cockroach Nauphoeta cinerea

Authors

  • Thalyta Julyanne Silva de Oliveira Vegetable Eco-physiology Laboratory, Department of Biological Sciences, Universidade Regional do Cariri (URCA), Crato, Brazil
  • José Wellington Macêdo Viana Biology Laboratory, Center for Agricultural Sciences and Biodiversity, Universidade Federal do Cariri (UFCA), Crato, Brazil
  • Pedro Silvino Pereira Vegetable Eco-physiology Laboratory, Department of Biological Sciences, Universidade Regional do Cariri (URCA), Crato, Brazil https://orcid.org/0000-0002-0001-7238
  • Elayne Eally Silva de Oliveira Morais Vegetable Eco-physiology Laboratory, Department of Biological Sciences, Universidade Regional do Cariri (URCA), Crato, Brazil
  • Jailson Renato de Lima Silva Biology and Toxicology Laboratory, Department of Biological Sciences, URCA, Crato, Brazil
  • Carlos Vinícius Barros de Oliveira Biology and Toxicology Laboratory, Department of Biological Sciences, URCA, Crato, Brazil https://orcid.org/0000-0003-2126-1464
  • Adrielle Rodrigues Costa Biology and Toxicology Laboratory, Department of Biological Sciences, URCA, Crato, Brazil
  • Irwin Rose Alencar de Menezes Coordinator of the Applied Microbiology Laboratory of Cariri, Universidade Regional do Cariri (URCA), Crato, Brazil https://orcid.org/0000-0003-1065-9581
  • Antonia Eliene Duarte Coordinator of the Vegetable Eco-physiology Laboratory, Department of Biological Sciences, Universidade Regional do Cariri (URCA), Crato, Brazil
  • Jean Paul Kamdem Researcher in Toxicology, Biochemistry and Pharmacology of Natural Products at the African Scientific Institute in the United States, Yaoundé, Cameroon https://orcid.org/0000-0003-1730-8602
  • Luiz Marivando Barros Coordinator of the Biology and Toxicology Laboratory, Department of Biological Sciences, Universidade Regional do Cariri (URCA), Crato, Brazil.

DOI:

https://doi.org/10.14295/bjs.v1i11.185

Keywords:

Antioxidant properties, Behavioral patterns, Paullinia cupana (Guarana), Oxidative stress markers

Abstract

Paullinia cupana (Kunth), popularly known as guarana, is a plant species from the Amazon Region of Brazil that stands out for being one of the most promising herbal medicines of the Brazilian flora since it has relevant biological properties. However, studies are still needed to use this species as a direct approach to evaluate aspects related to behavior and oxidative stress in invertebrate model animals. In this context, we aimed to evaluate the stimulant and the antioxidant effects of P. cupana in lobster cockroach Nauphoeta cinerea. For that, cockroaches were exposed to a diet separately supplemented by the decoction of P. cupana powder decoction at increasing concentrations of 1, 25, 50 and 100 mg/g for 42 days. Behavioral and biochemical assays were performed, respectively, to assess the locomotor/exploratory performance and oxidative stress marker levels of the cockroaches. They exhibited an outstanding increase in the locomotion performance and in the cell viability content, as well as in the protein and non-protein thiol levels. Moreover, there was a decrease in lipid peroxidation levels and in free Fe2+ ion contents. Together, our results demonstrate the stimulant and the antioxidant capacity of P. cupana by acting positively in behavioral patterns and by regulating oxidative stress markers in lobster cockroach N cinerea. These findings encourage further laboratory analyzes in order to better enlighten the specific mechanisms of action attributed to guarana.

References

Adedara, I. A., Awogbindin, I. O., Afolabi, B. A., Ajayi, B. O., Rocha, J. B. T., & Farombi, E. O. (2020). Hazardous impact of diclofenac exposure on the behavior and antioxidant defense system in Nauphoeta cinerea. Environmental Pollution, 265, e115053. 10.1016/j.envpol.2020.115053 DOI: https://doi.org/10.1016/j.envpol.2020.115053

Adedara, I. A., Godswill, U. A. S., Mike, M. A., Afolabi, B. A., Amorha, C. C., Sule, J., & Farombi, E. O. (2021). Chronic ciprofloxacin and atrazine co-exposure aggravates locomotor and exploratory deficits in non-target detritivore speckled cockroach (Nauphoeta cinerea). Environmental Science and Pollution Research, 28(20), 25680-25691. 10.1007/s11356-021-12460-5 DOI: https://doi.org/10.1007/s11356-021-12460-5

Adedara, I. A., Rosemberg, D. B., Souza, D. O., Farombi, E. O., Aschner, M., & Rocha, J. B. T. (2016). Neuroprotection of luteolin against methylmercury-induced toxicity in lobster cockroach Nauphoeta cinerea. Environmental Toxicology and Pharmacology, 42, 243-251. https://doi.org/10.1016/j.etap.2016.02.001 DOI: https://doi.org/10.1016/j.etap.2016.02.001

Adedara, I. A., Rosemberg, D. B., Souza, D. O., Kamdem, J. P., Farombi, E. O., Aschner, M. &, Rocha, J. B. T. (2015). Biochemical and behavioral deficits in the lobster cockroach Nauphoeta cinerea model of methylmercury exposure. Toxicology Research, 4(2), 442-451. https://doi.org/10.1039/C4TX00231H DOI: https://doi.org/10.1039/C4TX00231H

Ayala, T. B., Romero, A. C., & Chaverri, J. P. (2014). New insights into antioxidant strategies against paraquat toxicity. Free Radical Research, 48(6), 623-640. https://doi.org/10.3109/10715762.2014.899694 DOI: https://doi.org/10.3109/10715762.2014.899694

Bender, J. A., Simpson, E. M., Tietz, B. R., Daltorio, K. A., Quinn, R. D., & Ritzmann, R. E. (2011). Kinematic and behavioral evidence for a distinction between trotting and ambling gaits in the cockroach Blaberus discoidalis. Journal of Experimental Biology, 214(12), 2057-2064. https://doi.org/10.1242/jeb.056481 DOI: https://doi.org/10.1242/jeb.056481

Bittencourt, L. S., Bortolin, R. C., Kolling, E. A., Schnorr, C. E., Filho, A. Z., Gelain, D. P., & Moreira, J. C. F. (2016). Antioxidant profile characterization of a commercial Paullinia cupana (Guarana) extracts. Journal of Natural Product and Plant Resources, 2, 47-52.

Carrazoni T, de Avila Heberle, M., Perin, A. P. A., Zanatt, A. P., Rodrigues, P. V., dos Santos, F. D. M., de Almeida, C. G. M., Breda, R. V., dos Santos, D. S., Pinto, P. M., da Costa, J. C., Carlini, C. R., & Dal Belo, C. L. (2016). Central and peripheral neurotoxicity induced by the Jack Bean Urease (JBU) in Nauphoeta cinerea cockroaches. Toxicology, 368/369, 162-171. https://doi.org/10.1016/j.tox.2016.09.007 DOI: https://doi.org/10.1016/j.tox.2016.09.007

Costa, K. C., Ribeiro, E. E., Ribeiro, E. A. M., Moresco, R. N., Ugalde, M. R. M. I, Santos Montagner, G. F. F., Machado, M. M., Viegas, K., Brito, E., & Cruz, I. B. M. (2011). Habitual intake of Guarana and metabolic morbidities: an epidemiological study of an elderly Amazonian population. Phytotherapy Research, 25(9), 1367-1374. https://doi.org/10.1002/ptr.3437 DOI: https://doi.org/10.1002/ptr.3437

Da Silva, C. S., de Cássia, G. L. R., Elekofehinti, O. O., Ogunbolude, Y., Duarte, A. E., Rocha, J. B. T., Alencar de Menezes, I. R., Barros, L. M., Tsopmo, A., Lukong, K. E., & Kamdem, J. P. (2018). Caffeine-supplemented diet modulates oxidative stress markers and improves locomotor behavior in the lobster cockroach Nauphoeta cinerea. Chemico-Biological Interactions, 282, 77-84. https://doi.org/10.1016/j.cbi.2018.01.011 DOI: https://doi.org/10.1016/j.cbi.2018.01.011

Eberle, M. E. L., Oliveira, M. de C., Zidiotti, G. R., Cabreira, M. N., Barão, C. E., & Marcolino, V. A. (2020). Comparative study of different methodologies applied in the extraction of caffeine in energy drinks. Brazilian Journal of Development, 6, 8592-8608. https://doi.org/10.34117/bjdv6n2-245 DOI: https://doi.org/10.34117/bjdv6n2-245

Espinosa, J. C. A., & Sobrino Mejía, F. E. Cafeína y cefalea: consideraciones especiales. (2017). Neurología, 32(6), 394-398. https://doi.org/10.1016/j.nrl.2014.12.016 DOI: https://doi.org/10.1016/j.nrl.2014.12.016

Filho, V. M. B., Waczuk, E. P., Kamdem, J. P., Abolaji, A. O., Lacerda, S. R., da Costa, J. G. M., de Menezes, I. R. A., Boligon, A. A., Athayde, M. L., da Rocha, J. B. T., & Posser, T. (2014). Phytochemical constituents, antioxidant activity, cytotoxicity and osmotic fragility effects of Caju (Anacardium microcarpum). Industrial Crops and Products, 55(14), 280-288. https://doi.org/10.1016/j.indcrop.2014.02.021 DOI: https://doi.org/10.1016/j.indcrop.2014.02.021

Fisher, M. L., & Santos, J. Z. (2018). Bem-estar em Invertebrados: um parâmetro ético de responsabilidade científica e social da pesquisa? Revista Latinoamericana de Bioética, 18(1), 18-35. https://doi.org/10.18359/rlbi.2865 DOI: https://doi.org/10.18359/rlbi.2865

Forma, H. J., & Zhang, H. (2021). Targeting oxidative stress in disease: promise and limitations of antioxidant therapy. Nature Reviews Drug Discovery, 20(9), 689-709. https://doi.org/10.1038/s41573-021-00233-1 DOI: https://doi.org/10.1038/s41573-021-00233-1

Heard, C. M., Johnson, S., Moss, G., & Thomas, C. P. (2016). In vitro transdermal delivery of caffeine, theobromine, theophylline and catechin from extract of Guarana, Paullini cupana. International Journal of Pharmacology, 317(1), 26-31. https://doi.org/10.1016/j.ijpharm.2016.02.042 DOI: https://doi.org/10.1016/j.ijpharm.2006.02.042

Jedidi, S., Aloui, F,, Rtibi, K., Sammari, H., Selmi, H., Rejeb, A., Toumib, L,, & Sebai, H. (2020). Individual and synergistic protective properties of Salvia officinalis decoction extract and sulfasalazine against ethanol-induced gastric and small bowel injuries. RSC Advances, 10(59), 35998-36013. https://doi.org/10.1039/D0RA03265D DOI: https://doi.org/10.1039/D0RA03265D

Karthik, C. S., Mallesha, L., Nagashree, S., Mallu, P., Patil, V., & Kumar, S. (2016). Schiff bases of 4-(methylthio)benzaldehydes: Synthesis, characterization, antibacterial, antioxidant and cytotoxicity Studies. Current Chemistry Letters, 5, 71-82. https://10.5267/j.ccl.2015.12.002 DOI: https://doi.org/10.5267/j.ccl.2015.12.002

Kennedy, D. O., Haskell, C. F., Robertson, B., Reay, J., Brewster-Maund, C., Luedemann, J., Maggini, S., Ruf, M., Zangara, A., & Scholey, A. B. (2008). Improved cognitive performance and mental fatigue following a multi-vitamin and mineral supplement with added guaraná (Paullinia cupana). Appetite, 50(2-3), 506-513. https://doi.org/10.1016/j.appet.2007.10.007 DOI: https://doi.org/10.1016/j.appet.2007.10.007

Kurutas, E. B. (2016). The importance of antioxidants which play the role in cellular response against oxidative/nitrosative stress: current state. Nutrition Journal, 15(1), 01-22. https://doi.org/10.1186/s12937-016-0186-5 DOI: https://doi.org/10.1186/s12937-016-0186-5

Leal, A., Etiely, K., Yuri, C. B., Raquel, S., Oliveira, M. E., Rosa, B. T., Borges, B. T., Goulart, F. L., de Souza, V. Q., Laikowski, M. M., Moura, S., Vinadé, L., da Rocha, J. B. T., & Dal Belo, C. A. (2020). The insecticidal activity of Rhinella schneideri (Werner, 1894) paratoid secretion in Nauphoeta cinerea cockroaches. Toxins, 12(10), e630. https://doi.org/10.3390/toxins12100630 DOI: https://doi.org/10.3390/toxins12100630

Lepedda, A. J., Zinellu, A., Nieddu, G., Zinellu, E., Carru, C., Spirito, R., Guarino, A., De Muro, P., & Formato, M. (2013). Protein sulfhydryl group oxidation and mixed-disulfide modifications in stable and unstable human carotid plaques. Oxidative Medicine and Cellular Longevity, 20(13), e403973. https://doi.org/10.1155/2013/403973 DOI: https://doi.org/10.1155/2013/403973

Lipkind, D., Sakov, A., Kafkafi, N., Elmer, G. I., Benjamini, Y., & Golani, I. (2004). New replicable anxiety-related measures of wall vs. center behavior of mice in the open field. Journal of Applied Physiology, 97(1), 347-359. https://doi.org/10.1152/japplphysiol.00148.2004 DOI: https://doi.org/10.1152/japplphysiol.00148.2004

Lira, M. G. S., Cantanhêde, L. G., Miranda, G. S., & Neta, R. N. F. C. (2016). Bioética e uso de animais invertebrados em pesquisa: uma abordagem histórico-legislativa. Revista Investigação Medicina Veterinária, 15(1), 143-149.

Majhenič, L., Škerget, M., & Knez, Ž. (2017). Antioxidant and antimicrobial activity of guarana seed extracts. Food Chemistry, 104, 1258-1268. https://doi.org/10.1016/j.foodchem.2007.01.074 DOI: https://doi.org/10.1016/j.foodchem.2007.01.074

Marques, L. L. M., Ferreira, E. D. F., Paula, M. P., Klein, T., & Mello, J. C. P. (2019). Paullinia cupana: a multipurpose plant – a review. Brazilian Journal of Pharmacognosy. 29(1), 77-110. https://doi.org/10.1016/j.bjp.2018.08.007 DOI: https://doi.org/10.1016/j.bjp.2018.08.007

McLellan, T. M., Caldwell, J. A., & Lieberman, H. R. (2016). A review of caffeine’s effects on cognitive, physical and occupational performance. Neuroscience and Biobehavioral Reviews, 71, 294-312. https://doi.org/10.1016/j.neubiorev.2016.09.001 DOI: https://doi.org/10.1016/j.neubiorev.2016.09.001

Mendes, T. M. N., Murayama, Y., Yamaguchi, N., Sampaio, G. R., Fontes, L. C. B., Torres, E. A. F da S., Tamura, H., & Yonekura, L. (2019). Guarana (Paullinia cupana) catechins and procyanidins: gastrointestinal/colonic bioaccessibility, Caco-2 cell permeability and the impact of macronutrients. Journal of Functional Food, 55, 352-361. https://doi.org/10.1016/j.jff.2019.02.026 DOI: https://doi.org/10.1016/j.jff.2019.02.026

Nawrot, P., Jordan, S., Eastwood, J., Rotstein, J., Hugenholtz, A., & Feeley, M. (2003). Effects of caffeine on human health. Food Additives and Contaminants, 20, 01-30. https://doi.org/10.1080/0265203021000007840 DOI: https://doi.org/10.1080/0265203021000007840

Niveditha, S., Shivanandappa, T., & Ramesh, S. R. (2017). Ameliorative potential of natural antioxidants against Paraquat-induced oxidative stress and locomotor impairment in Drosophila melanogaster: comparative study. The Open Bioactive Compounds Journal, 5(2), 43-56.10.2174/1874847301705010043 DOI: https://doi.org/10.2174/1874847301705010043

Pereira, P. S., Costa, A. R., de Oliveira, T. J. S., Oliveira, C. V. B., de Lima, M. do C. A., de Oliveira, J. F., Kim, B., Coutinho, H. D. M., Duarte, A. L., Kamdem, J. P., & da Silva, T. G. (2022). Neurolocomotor behavior and oxidative stress markers of Thiazole and Thiazolidinedione derivatives against Nauphoeta cinerea. Antioxidants, 11(2), e420. https://doi.org/10.3390/antiox11020420 DOI: https://doi.org/10.3390/antiox11020420

Piccoli, B. C., Alvim, J. C., da Silva, F. D., Nogara, P. A., Olagoke, O. C., Aschner, M., Oliveira, C. S., & da Rocha, J. B. T. (2020). High level of methylmercury exposure causes persisted toxicity in Nauphoeta cinerea. Environmental Science and Pollution Reseacrh, 27(5), 4799-4813. https://doi.org/10.1007/s11356-019-06989-9 DOI: https://doi.org/10.1007/s11356-019-06989-9

Ribeiro, B. D., Coelho, M. A. Z., & Barreto, D. W. (2012). Production of caffeine-rich guarana extracts using an enzymatic process and tannin adsorption. Brazilian Journal of Food and Technology, 15, 261–270. https://doi.org/10.1590/S1981-67232012005000020 DOI: https://doi.org/10.1590/S1981-67232012005000020

Rodrigues, N. R., Nunes, M. E. M., Silva, D. G. C., Zemolin, A. P . P., Meinerz, D. F., Cruz, L. C., Pereira, A.B., da Rocha, J. B. T., Posser, T., & Franco, J. L. (2013). Is the lobster cockroach Nauphoeta cinerea a valuable model for evaluating mercury induced oxidative stress? Chemosphere, 92(9), 1177-1182. https://doi.org/10.1016/j.chemosphere.2013.01.084 DOI: https://doi.org/10.1016/j.chemosphere.2013.01.084

Rosemberg, D. B., Braga, M. M., Rico, E. P., Loss, C. M., Córdova, S. D., Mussulini, B. H. M., Blaser, R. E., Leite, C. E., Campos, C. M., Dias, R. D., Calcagnotto, M. E., de Oliveira, D. L., & Souza, D. O. (2012). Behavioral effects of taurine pretreatment in zebrafish acutely exposed to ethanol. Neuropharmacology, 63(4), 613-623. https://doi.org/10.1016/j.neuropharm.2012.05.009 DOI: https://doi.org/10.1016/j.neuropharm.2012.05.009

Schimpl, F. C., da Silva, J. F., Gonçalves, J. F. de C., & Mazzafera, P. (2013). Guarana: revisiting a highly caffeinated plant from the Amazon. Journal of Ethnopharmacology, 150(1), 14-31. https://doi.org/10.1016/j.jep.2013.08.023 DOI: https://doi.org/10.1016/j.jep.2013.08.023

Schneider, T., Gavrilova, I., & Budisa, N. (2019). Synthesis of a new metal chelating amino acid: Terpyridyl-alanine. Tetrahedron Letters, 60, 906-910. https://doi.org/10.1016/j.tetlet.2019.02.037 DOI: https://doi.org/10.1016/j.tetlet.2019.02.037

Silva, C. P., Soares-Freitas, R. A. M., Sampaio, G. R., de Camargo, A. C., & Torres, E. A. F. S. (2019). Guarana as a source of bioactive compounds. Journal of Food Bioactives, 6, 1–5. https://doi.org/10.31665/JFB.2019.6182 DOI: https://doi.org/10.31665/JFB.2019.6182

Temple, J. L., Bernard, C., Lipshultz, S. E., Czachor, J. D., Westphal, J. A., & Mestre, M. A. (2017). The safety of ingested caffeine: a comprehensive review. Frontiers in Psychiatry, 8(2), e80. https://doi.org/10.3389/fpsyt.2017.00080 DOI: https://doi.org/10.3389/fpsyt.2017.00080

Tfouni, S. A. V., Camargo, M. C. R., Vitorino, S. H. P., Menegário, T. F., & Toledo, M. C. de F. (2017). Contribuição do guaraná em pó (Paullinia cupana) como fonte de cafeína na dieta. Revista de Nutrição, 20, 63-68. https://doi.org/10.1590/S1415-52732007000100007 DOI: https://doi.org/10.1590/S1415-52732007000100007

Trivedi, M., Laurence, J., & Siahaan, T. (2019). The role of thiols and disulfides on protein stability. Current Protein and Peptide Science, 10(6), 614-625. https://doi.org/10.2174/138920309789630534 DOI: https://doi.org/10.2174/138920309789630534

Ventura, S., Rodrigues, M., Falcão, A., & Alves, G. (2018). Effects of Paullinia cupana extract on lamotrigine pharmacokinetics in rats: a herb-drug interaction on the gastrointestinal tract with potential clinical impact. Food Chemistry and Toxicology, 115, 170-177. https://doi.org/10.1016/j.fct.2018.03.011 DOI: https://doi.org/10.1016/j.fct.2018.03.011

Viana, J. W. M., De Lima, R. C. G., Silva, J. R. L., Nunes, R. G. S., Neto, J. E., & Barros, L. M. (2020). Protective effect of vitamin C against behavioral, histological changes and mortality rate induced by Paraquat in Drosophila melanogaster. Austin Food Sciemce, 5(1), e1036.

Viana, J. W. M., Torres, R. P., Bezerra, T. F., & Nobre, F. W. (2021a). Beneficial and adverse effects of caffeine consumption on human body: a comprehensive review. InterSciencePlace - International Scientific Journal, 16(2), 133-160. http://dx.doi.org/10.6020/1679-9844/v16n2a7

Viana, J. W. M., & Torres, R. P. (2021b). Review of protective effects of melatonin on neurological disorders and oxidative stress. InterSciencePlace - International Scientific Journal, 16(4), 19-43. http://dx.doi.org/10.6020/1679-9844/v16n4a2

Vrailas-Mortimer, A., Gomez, R., Dowse, H., & Sanyal, S. (2012). A survey of the protective effects of some commercially available antioxidant supplements in genetically and chemically induced models of oxidative stress in Drosophila melanogaster. Experimental Gerontology, 47, 712-722. DOI: https://doi.org/10.1016/j.exger.2012.06.016

Weckerle, C. S., Stutz, M. A., & Baumann, T. W. (2013). Purine alkaloids in Paullinia. Phytochemistry, 64(3), 35-742. https://doi.org/10.1016/s0031-9422(03)00372-8 DOI: https://doi.org/10.1016/S0031-9422(03)00372-8

Yonekura, L., Martins, C. A., Sampaio, G. R., Monteiro, M. P., César, L. A. M., Mioto, B. M., Mori, C. S., Mendes, T. M. N., Ribeiro, M. L., Arçari, D. P., & Torres, E. A. F da S. (2016). Bioavailability of catechins from guarana (Paullinia cupana) and its effect on antioxidant enzymes and other oxidative stress markers in healthy human subjects. Food and Function, 7(3), 2970-2978. https://doi.org/10.1039/C6FO00513F DOI: https://doi.org/10.1039/C6FO00513F

Zeidán-Chuliá, F., Gelain, D. P., Kolling, E. A., Rybarczyk-Filho, J. L., Ambrosi, P., Terra, S. R., Pires, A. S., da Rocha, J. B. T., Behr, G. A., & Moreira, J. C. F. (2013). Major components of energy drinks (Caffeine, Taurine, and Guarana) exert cytotoxic effects on human neuronal SH-SY5Y cells by decreasing Reactive Oxygen Species (ROS) production. Oxidative Medicine and Cellular Longevity, 20(13), e791795. https://doi.org/10.1155/2013/791795 DOI: https://doi.org/10.1155/2013/791795

Downloads

Published

2022-11-10

How to Cite

Oliveira, T. J. S. de, Viana, J. W. M., Pereira, P. S., Morais, E. E. S. de O., Silva, . J. R. de L., Oliveira , C. V. B. de, Costa, A. R., Menezes, I. R. A. de, Duarte, . A. E., Kamdem, J. P., & Barros, L. M. (2022). Paullinia cupana (Kunth) stimulates behavior patterns and regulates oxidative stress markers in lobster cockroach Nauphoeta cinerea. Brazilian Journal of Science, 1(11), 27–44. https://doi.org/10.14295/bjs.v1i11.185

Issue

Section

Agrarian and Biological Sciences