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Caffeine modulates brain purinergic signaling in Nile tilapia (Oreochromis niloticus) under hypoxia conditions: improvement of immune and inflammatory responses

  • Matheus D. Baldissera
  • Carine F. Souza
  • Sharine N. Descovi
  • Tiago G. Petrolli
  • Aleksandro S. da Silva
  • Bernardo Baldisserotto
Article

Abstract

Purinergic signaling is linked to neurodegenerative and proinflammatory damage during pathological conditions such as hypoxia, but involvement of this pathway in brain damage in fish exposed to environmental hypoxia remains unknown, and we propose dietary supplementation with caffeine in order to improve the immune response. Therefore, the aim of the study was to evaluate whether the enzymatic purinergic signaling pathway is associated with inflammatory brain damage in Nile tilapia (Oreochromis niloticus) exposed to environmental hypoxia and whether dietary supplementation with caffeine (5% and 8%) can prevent these changes in purinergic signaling. Animals were randomly divided into six groups (A–F, n = 6 per group, in triplicate), as follows: groups A–C were submitted to normoxia, while groups D–F were submitted to hypoxia. Groups A and D received the basal diet, while groups B and D and groups C and F received a diet containing 5% and 8% caffeine, respectively, and fed with their respective diets for 21 days. After 21 days, aeration was disconnected (groups D–F) and the dissolved oxygen levels were maintained as follows: group A (6.55 ± 0.23 mg/L), group B (6.51 ± 0.24 mg/L), group C (6.58 ± 0.22 mg/L), group D (1.23 ± 0.11 mg/L), group E (1.20 ± 0.15 mg/L), and group F (1.18 ± 0.13 mg/L). Cerebral triphosphate diphosphohydrolase (NTPDase) using adenosine triphosphate (ATP) as a substrate and 5′-nucleotidase activities decreased in fish exposed to 72 h of hypoxia compared with the normoxia group, while adenosine deaminase (ADA) activity and levels of nitric oxide (NOx) metabolites were higher. Dietary supplementation with 5% and 8% caffeine prevented all alterations elicited by hypoxia, with the exception of ADA activity in the case of 5% caffeine. Based on this evidence, our findings reveal that nucleotide/nucleoside hydrolysis is modified in the brains of fish exposed to 72 h of hypoxia, contributing to inflammatory damage, which apparently is mediated by excessive ATP content in the extracellular medium and by excessive NOx production. Also, the use of a diet containing 5% and 8% caffeine prevented these alterations (except 5% of dietary caffeine on ADA activity) and can be considered an interesting approach to preventing the impairment of immune and inflammatory responses elicited by hypoxia, principally the inclusion of 8% caffeine.

Keywords

Adenosine Adenosine triphosphate 1,3,7-Trimethylxanthine Nitric oxide 

Notes

Funding information

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES)—Finance Code 001—PhD fellowships to C.F. Souza and M.D. Baldissera. A. S. Da Silva and B. Baldisserotto are funded by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) research fellowships and S.N. Descovi by an FAPERGS (Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul) undergraduate fellowship.

Compliance with ethical standards

All procedures were approved by the Ethical and Animal Welfare Committee of the Universidade do Estado de Santa Catarina (protocol 9959260218).

References

  1. Abdelrazek HMA, Tag HM, Kilany OE, Reddy PG, Hassam AM (2017) Immuomodulatory effect of dietary turmeric supplementation on Nile tilapia (Oreochromis niloticus). Aquac Nutr 23:1048–1054CrossRefGoogle Scholar
  2. Abdel-Tawwab M, Hagras AE, Elbaghdady HAM, Monier MN (2015) Effects of dissolved oxygen and fish size on Nile tilapia, Oreochromis niloticus (L.): growth performance, whole-body composition, and innate immunity. Aquacult Int 23:1261–1274CrossRefGoogle Scholar
  3. Baldissera MD, Souza CF, Boaventura TP, Nakayama CL, Baldisserotto B, Luz RK (2018a) Purinergic signaling as a potential target of hypoxia stress-induced impairment of the immune system in freshwater catfish Lophiosilurus alexandri. Aquaculture 496:197–202CrossRefGoogle Scholar
  4. Baldissera MD, Souza CF, Doleski PH, Zeppenfeld CC, Descovi S, Da Silva AS, Baldisserotto B (2018b) Xanthine oxidase activity exerts pro-oxidative and pro-inflammatory effects in serum of silver catfish fed with a diet contaminated with aflatoxin B1. J Fish Dis 41:1153–1158CrossRefPubMedGoogle Scholar
  5. Bours MJ, Swennen EL, Di Virgilio F, Cronstein BN, Dagnelie PC (2006) Adenosine 50-triphosphate and adenosine as endogenous signalling molecules in immunity and inflammation. Pharmacol Ther 112:358–404CrossRefPubMedGoogle Scholar
  6. Boyd CE, Tucker CS (1992) Water quality and pond soil analyses for aquaculture. Auburn University, Auburn 183pGoogle Scholar
  7. Burnstock G (2016a) P2X ion channel receptors and inflammation. Purinergic Signal 12:59–67CrossRefPubMedPubMedCentralGoogle Scholar
  8. Burnstock G (2016b) An introduction to the roles of purinergic signalling in neurodegeneration, neuroprotection and neuroregeneration. Neuropharmacology 104:4–17CrossRefPubMedGoogle Scholar
  9. Colt J (2001) List of spreadsheets prepared as a complement. In: Wedemeyer GA (ed) Fish hatchery management. second ed. American Fisheries Society, BethesdaGoogle Scholar
  10. Da Silva RS, Bruno AN, Battastini AMO, Sarkis JJF, Lara DR, Bonan CD (2003) Acute caffeine treatment increased extracellular nucleotide hydrolysis from rat striatal and hippocampal synaptosomes. Neurochem Res 28:1249–1254CrossRefPubMedGoogle Scholar
  11. Gilmore KL, Doubleday ZA, Gillanders BM (2018) Testing hypoxia: physiological effects of long-term exposure in two freshwater fishes. Oecologia 186:37–47CrossRefPubMedGoogle Scholar
  12. Giusti G, Gakis C (1971) Temperature conversion factors, activation energy, relative substrate specificity and optimum pH of adenosine from human serum and tissues. Enzyme 12:417–425CrossRefPubMedGoogle Scholar
  13. Guo Z, Cui J, Li M, Liu H, Zhang M, Meng F, Shi G, Wang R, He X, Zhao Y (2018) Effect of feeding frequency on growth performance, antioxidant status, immune response and resistance to hypoxia stress challenge on juvenile dolly varden char Salvelinus malma. Aquaculture 486:197–201CrossRefGoogle Scholar
  14. Gustafson LA, Zuurbier CJ, Bassett JE, Barends JPF, van Beek JHGM, Bassingthwaighte JB, Kroll K (1999) Increased hypoxic stress decreased AMP hydrolysis in rabbit heart. Cardiovasc Res 44:333–343CrossRefPubMedGoogle Scholar
  15. Hashiguchi W, Nagatomo I, Akasaki Y, Uchida M, Tominaga M, Takigawa M (2001) Influences of caffeine to nitric oxide production and zonisamide concentration in the brain of seizure susceptible EL mice. Psychiatry Clin Neurosci 55:319–324CrossRefPubMedGoogle Scholar
  16. Hung YW, Leung YM, Lin NN, Lee TJ, Kuo JS, Tung KC, Gong CL (2015) P2 purinergic receptor activation of neuronal nitric oxide synthase and guanylyl cyclase in the dorsal facial area of the medulla increases blood flow in the common carotid arteries of cats. Neuroscience 286:231–241CrossRefPubMedGoogle Scholar
  17. Iris M, Tsou PS, Sawalha AH (2018) Caffeine inhibits STAT1 signaling and downregulates inflammatory pathways involved in autoimmunity. Clin Immunol 192:68–77CrossRefPubMedGoogle Scholar
  18. Kumar V, Kaur J, Panghal A, Kaur S, Handa V (2018) Caffeine: a boon or bane. Nutr Food Sci 48:61–75CrossRefGoogle Scholar
  19. Li M, Wang X, Qi C, Li E, Du Z, Qin JG, Chen L (2018) Metabolic response of Nile tilapia (Oreochromis niloticus) to acute and chronic hypoxia stress. Aquaculture 495:187–195CrossRefGoogle Scholar
  20. Mabrok MAE, Wahdan A (2018) The immune modulatory effect of oregano (Origanum vulgare L.) essential oil on Tilapia zillii following intraperitoneal infection with Vibrio anguillarum. Aquacult Int 26:1147–1160CrossRefGoogle Scholar
  21. Magnoni LJ, Eding E, Leguen I, Prunet P, Geurden I, Ozório ROA, Schrama JW (2018) Hypoxia, but not an electrolyte-imbalanced diet, reduces feed intake, growth and oxygen consumption in rainbow trout (Oncorhynchus mykiss). Sci Rep 8:e4965CrossRefGoogle Scholar
  22. Mahfouz ME, Hegazi MM, El-Magd MA, Kasem EA (2015) Metabolic and molecular responses in Nile tilapia, Oreochromis niloticus during short and prolonged hypoxia. Mar Freshw Behav Physiol 48:319–340CrossRefGoogle Scholar
  23. Marina N, Turovsky E, Christie IN, Hosford PS, Hadjihambi A, Korsak A, Ang R, Mastitskaya S, Sheikhbahaei S, Therapambil SM, Gourine AV (2018) Brain metabolic sensing and metabolic signaling at the level of an astrocyte. Glia 66:1185–1199CrossRefPubMedGoogle Scholar
  24. Montesinos MC, Yap JS, Desai A, Posadas I, McCrary C, Cronstein BN (2000) Reversal of the antiinflammatory effects of methotrexate by the nonselective adenosine receptor antagonists theophylline and caffeine: evidence that the antiinflammatory effects of methotrexate are mediated via multiple adenosine receptors in rat adjuvant arthritis. Arthritis Rheum 43:656–663CrossRefPubMedGoogle Scholar
  25. Motulsky HJ (2014) Common misconceptions about data analysis and statistics. Pharmacol Res Perspect 3:e00093CrossRefPubMedPubMedCentralGoogle Scholar
  26. Olson N, van der Vliet A (2011) Interactions between nitric oxide and hypoxia-inducible factor signaling pathways in inflammatory disease. Nitric Oxide 25:125–137CrossRefPubMedPubMedCentralGoogle Scholar
  27. Orbán C, Vásárhelyi Z, Bajnok A, Sava F, Toldi G (2018) Effects of caffeine and phosphodiesterase inhibitors on activation of neonatal T lymphocytes. Immunobiology 223:627–633CrossRefPubMedGoogle Scholar
  28. Pimentel VC, Zanini D, Cardoso AM, Schmatz R, Bagatini MD, Gutierres JM, Carvalho F, Gomes JL, Rubin M, Morsch VM, Moretto MB, Colino-Oliveira M, Sebastião AM, Schetinger MRC (2013) Hypoxia–ischemia alters nucleotide and nucleoside catabolism and Na+, K+-ATPase activity in the cerebral cortex of newborn rats. Neurochem Res 38:886–894CrossRefPubMedGoogle Scholar
  29. Pimentel VC, Moretto MB, Oliveira MC, Zanini D, Sebastião AM, Schetinger MRC (2015) Neuroinflammation after neonatal hypoxia–ischemia is associated with alterations in the purinergic system: adenosine deaminase 1 isoenzyme is the most predominant after insult. Mol Cell Biochem 403:169–177CrossRefPubMedGoogle Scholar
  30. Read SM, Northcote DH (1981) Minimization of variation in the response to different proteins of the Coomassie blue G dye-binding assay for protein. Anal Biochem 116:53–64CrossRefPubMedGoogle Scholar
  31. Ribeiro PAP, Miranda-Filho C, De Melo DC, Luz RK (2015) Efficiency of eugenol as anesthetic for the early life stages of Nile tilapia (Oreochromis niloticus). An Acad Bras Cienc 87:529–535CrossRefPubMedGoogle Scholar
  32. Robertson CE, Wright PA, Koblitz L, Bernier NJ (2014) Hypoxia-inducible factor-1 mediates adaptive developmental plasticity of hypoxia tolerance in zebrafish, Danio rerio. Proc Biol Sci 281:e20140637CrossRefGoogle Scholar
  33. Rosemberg DB, Rico EP, Langoni AS, Spinelli JT, Pereira TC, Dias RD, Souza DO, Bonan CD, Bogo MR (2010) NTPDase family in zebrafish: nucleotide hydrolysis, molecular identification and gene expression profiles in brain, liver and heart. Comp Biochem Physiol B 155:230–240CrossRefPubMedGoogle Scholar
  34. Sakamoto W, Nishihira J, Fujie K, Mizuno S, Ozaki M, Yukawa S (2000) Coffee and fitness-coffee suppresses lipopolysaccharide-induced liver injury in rats. J Nutr Sci Vitaminol 46:316–320CrossRefPubMedGoogle Scholar
  35. Savio S, Giorgi M, Robson S (2016) Ectonucleotidases in immunobiology. Encycl Immunobiol 2:424–431CrossRefGoogle Scholar
  36. Savio LEB, Mello PA, da Silva CG, Coutinho-Silva R (2018) The P2X7 receptor in inflammatory diseases: angel or demon? Front Pharmacol 9:e52CrossRefGoogle Scholar
  37. Shin EY, Wang L, Zemskova M, Deppen J, Xu K, Strobel F (2018) Adenosine production by biomaterial-supported mesenchymal stromal cells reduces the innate inflammatory response in myocardial ischemia/reperfusion injury. J Am Heart Assoc 7:e006949PubMedPubMedCentralGoogle Scholar
  38. Souza CF, Baldissera MD, Bottari NB, Moreira KLS, da Rocha MIUM, da Veiga ML, Santos RCV, Baldisserotto B (2018) Purinergic signaling modulates the cerebral inflammatory response in experimentally infected fish with Streptococcus agalactiae: an attempt to improve the immune response. Mol Cell Biochem 443:131–138CrossRefPubMedGoogle Scholar
  39. Tatsch E, Bochi GV, Pereira RS, Kober H, Agertt VA, de Campos MM, Gomes P, Duarte MM, Moresco RN (2011) A simple and inexpensive automated technique for measurement of serum nitrite/nitrate. Clin Biochem 44:348–350CrossRefPubMedGoogle Scholar
  40. Varani K, Portaluppi F, Gessi S, Merighi S, Vincenzi F, Cattabriga E, Dalpiaz A, Bortolotti F, Belardinelli L, Borea A (2005) Caffeine intake induces an alteration in human neutrophil A2A adenosine receptors. Cell Mol Life Sci 62:2350–2358CrossRefPubMedGoogle Scholar
  41. Verdouw H, Vanechteld CJA, Deckkers EMJ (1978) Ammonia determinations based on indophenol formation with sodium salicylate. Water Res 12:399–402CrossRefGoogle Scholar
  42. Wang QF, Shen WL, Hou CC, Liu C, Wu XF, Zhu JQ (2017) Physiological responses and changes in gene expression in the large yellow croaker Larimichthys crocea following exposure to hypoxia. Chemosphere 169:418–427CrossRefPubMedGoogle Scholar
  43. Yu NY, Bieder A, Raman A, Mileti E, Katayama S, Einarsdottir E, Fredholm BB, Falk A, Tapia-Páez I, Daub CO, Kere J (2017) Acute doses of caffeine shift nervous system cell expression profiles toward promotion of neuronal projection growth. Sci Rep 7:e11458CrossRefGoogle Scholar
  44. Zhang J, Yang L, Fang Z, Kong J, Huang Q, Xu H (2018) Adenosine promotes the recovery of mice from the cuprizone-induced behavioral and morphological changes while effecting on microglia and inflammatory cytokines in the brain. J NeuroImmune Pharmacol 13:412–425CrossRefPubMedGoogle Scholar
  45. Zheng X, Dai W, Chen X, Wang K, Zhang W, Li L, Hou J (2015) Caffeine reduces hepatic lipid accumulation through regulation of lipogenesis and ER stress in zebrafish larvae. J Biomed Sci 22:e105CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of Microbiology and ParasitologyUniversidade Federal de Santa MariaSanta MariaBrazil
  2. 2.Department of Physiology and PharmacologyUniversidade Federal de Santa MariaSanta MariaBrazil
  3. 3.Postgraduate Program in Veterinary MedicineUniversidade do Oeste de Santa CatarinaXanxerêBrazil
  4. 4.Department of Animal ScienceUniversidade do Estado de Santa CatarinaChapecóBrazil

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