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Fucoidan protects against subacute diazinon-induced oxidative damage in cardiac, hepatic, and renal tissues

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Abstract

Fucoidans (FUC) are organic sulfated polysaccharides from natural seaweeds with multiple biological actions. The current study was performed to assess the chemoprotective, antioxidant, and anti-inflammatory effects of FUC from Laminaria japonicum against diazinon (DZN)-induced injuries to rat cardiac, hepatic, and renal tissues. Forty male Wistar rats were assigned into five groups, receiving saline, oral FUC 200 mg/kg/day, subcutaneous DZN 20 mg/kg/day, DZN plus FUC 100 mg/kg/day, or DZN plus FUC 200 mg/kg/day (each treatment was given daily for 4 weeks). Data analysis showed that DZN-intoxicated rats exhibited significantly higher (p < 0.05) serum levels of alanine transaminase, aspartate transaminase, alkaline phosphatase, urea, creatine, creatine kinase, creatine kinase-MB, lactate dehydrogenase, cholesterol, interleukin-6, and tumor necrosis factor-α, as well as lower levels of acetylcholinesterase, compared to control rats. In addition, DZN intoxication was associated with significantly higher (p < 0.05) cardiac, hepatic, and renal tissue concentrations of malondialdehyde and nitric oxide, as well as lower glutathione concentrations, and activities of glutathione peroxidase, superoxide dismutase, and catalase enzymes in comparison to control rats. Treatment with FUC (at 100 or 200 mg/kg/day) ameliorated all the aforementioned alterations in a dose-dependent manner. In conclusion, FUC from Laminaria japonicum ameliorated DZN-induced oxidative stress, pro-inflammatory effects, and injuries to the cardiac, hepatic, and renal tissues. These effects may be related to the antioxidant and anti-inflammatory effects of FUC.

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Abbreviations

AChE:

acetylcholinesterase

ALP:

alkaline phosphatase

ALT:

alanine transaminase

AST:

aspartate transaminase

CAT:

catalase

CK:

creatine kinase

DZN:

diazinon

FUC:

fucoidan

GSH-Px:

glutathione peroxidase

GSH:

reduced glutathione

IL:

interleukin

MDA:

malondialdehyde

NO:

nitric oxide

SOD:

superoxide dismutase

TNF:

tumor necrosis factor

References

  • Abdel-Daim MM (2016) Synergistic protective role of ceftriaxone and ascorbic acid against subacute diazinon-induced nephrotoxicity in rats. Cytotechnology 68:279–289

    CAS  Google Scholar 

  • Abdel-Daim MM, Abushouk AI, Alkhalf MI, Toraih EA, Fawzy MS, Ijaz H, Aleya L, Bungau SG (2018) Antagonistic effects of Spirulina platensis on diazinon-induced hemato-biochemical alterations and oxidative stress in rats. Environ Sci Pollut Res Int 25:27463–27470

    CAS  Google Scholar 

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    CAS  Google Scholar 

  • Ahmadabadi A, Akbari Z, Ahmadimoghaddam D, Larki-Harchegani A (2019) The role of ghrelin and tumor necrosis factor alpha in diazinon-induced dyslipidemia: insights into energy balance regulation. Pestic Biochem Physiol 157:138–142

    Google Scholar 

  • Ahmadi A, Heidarian E, Ghatreh-Samani K (2019) Modulatory effects of artichoke (Cynara scolymus L.) leaf extract against oxidative stress and hepatic TNF-alpha gene expression in acute diazinon-induced liver injury in rats. J Basic Clin Physiol Pharmacol 30:20180180. https://doi.org/10.1515/jbcpp-2018-0180

    Article  CAS  Google Scholar 

  • Ajibade TO, Oyagbemi AA, Omobowale TO, Asenuga ER, Afolabi JM, Adedapo AA (2016) Mitigation of diazinon-induced cardiovascular and renal dysfunction by gallic acid. Interdiscip Toxicol 9:66–77

    CAS  Google Scholar 

  • AlKahtane AA, Abushouk AI, Mohammed ET, AlNasser M, Alarifi S, Ali D, Alessia MS, Almeer RS, AlBasher G, Alkahtani S, Aleya L, Abdel-Daim MM (2019) Fucoidan alleviates microcystin-LR-induced hepatic, renal, and cardiac oxidative stress and inflammatory injuries in mice. Environ Sci Pollut Res Int https://doi.org/10.1007/s11356-019-06931-z

  • Allain CC, Poon LS, Chan CS, Richmond W, Fu PC (1974) Enzymatic determination of total serum cholesterol. Clin Chem 20:470–475

    CAS  Google Scholar 

  • Babson AL, Babson SR (1973) Kinetic colorimetric measurement of serum lactate dehydrogenase activity. Clin Chem 19:766–769

    CAS  Google Scholar 

  • Beutler E, Duron O, Kelly BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61:882–888

    CAS  Google Scholar 

  • Cakici O, Akat E (2013) Effects of oral exposure to diazinon on mice liver and kidney tissues: biometric analyses of histopathologic changes. Anal Quant Cytopathol Histopathol 35:7–16

    Google Scholar 

  • Carvalho AC, Sousa RB, Franco ÁX, Costa JVG, Neves LM, Ribeiro RA, Sutton R, Criddle DN, Soares PM, de Souza MH (2014) Protective effects of fucoidan, a P-and L-selectin inhibitor, in murine acute pancreatitis. Pancreas 43:82–87

    CAS  Google Scholar 

  • Chen J, Wang W, Zhang Q, Li F, Lei T, Luo D, Zhou H, Yang B (2013) Low molecular weight fucoidan against renal ischemia–reperfusion injury via inhibition of the MAPK signaling pathway. PLoS One 8:e56224

    CAS  Google Scholar 

  • Čolović MB, Vasić VM, Avramović NS, Gajić MM, Djurić DM, Krstić DZ (2015) In vitro evaluation of neurotoxicity potential and oxidative stress responses of diazinon and its degradation products in rat brain synaptosomes. Toxicol Lett 233:29–37

    Google Scholar 

  • Coulombe J, Favreau L (1963) A new simple semimicro method for colorimetric determination of urea. Clin Chem 9:102–108

    CAS  Google Scholar 

  • Cumashi A, Ushakova NA, Preobrazhenskaya ME, D’Incecco A, Piccoli A, Totani L, Tinari N, Morozevich GE, Berman AE, Bilan MI (2007) A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology 17:541–552

    CAS  Google Scholar 

  • Danaei GH, Memar B, Ataee R, Karami M (2019) Protective effect of thymoquinone, the main component of Nigella sativa, against diazinon cardio-toxicity in rats. Drug Chem Toxicol 42:585–591

    CAS  Google Scholar 

  • Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    CAS  Google Scholar 

  • Ezzi L, Haouas Z, Salah IB, Sakly A, Grissa I, Chakroun S, Kerkeni E, Hassine M, Mehdi M, Cheikh HB (2016) Toxicopathic changes and genotoxic effects in liver of rat following exposure to diazinon. Environ Sci Pollut Res 23:11163–11170

    CAS  Google Scholar 

  • Fischer R, Maier O (2015) Interrelation of oxidative stress and inflammation in neurodegenerative disease: role of TNF. Oxidative Med Cell Longev 2015:610813. https://doi.org/10.1155/2015/610813

    Article  CAS  Google Scholar 

  • Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem 126:131–138

    CAS  Google Scholar 

  • Hong SW, Lee HS, Jung KH, Lee H, Hong SS (2012) Protective effect of fucoidan against acetaminophen-induced liver injury. Arch Pharm Res 35:1099–1105

    CAS  Google Scholar 

  • Jia Y, Sun Y, Weng L, Li Y, Zhang Q, Zhou H, Yang B (2016) Low molecular weight fucoidan protects renal tubular cells from injury induced by albumin overload. Sci Rep 6:31759

    CAS  Google Scholar 

  • Jo M, Kim T-H, Seol D-W, Esplen JE, Dorko K, Billiar TR, Strom SC (2000) Apoptosis induced in normal human hepatocytes by tumor necrosis factor-related apoptosis-inducing ligand. Nat Med 6:564–567. https://doi.org/10.1038/75045

    Article  CAS  Google Scholar 

  • Kalimuthu S, Kim SK (2015) Fucoidan, a sulfated polysaccharides from brown algae as therapeutic target for cancer. In: Kim SK (eds) Handbook of anticancer drugs from marine origin. Springer, Cham

  • Kang KS, Kim ID, Kwon RH, Lee JY, Kang JS, Ha BJ (2008) The effects of fucoidan extracts on CCl(4)-induced liver injury. Arch Pharm Res 31:622–627

    CAS  Google Scholar 

  • Larkin DJ, Tjeerdema RS (2000) Fate and effects of diazinon. Rev Environ Contam Toxicol 166:49–82

    CAS  Google Scholar 

  • Larsen K (1972) Creatinine assay by a reaction-kinetic principle. Clin Chim Acta 41:209–217

    CAS  Google Scholar 

  • Li B, Lu F, Wei X, Zhao R (2008) Fucoidan: structure and bioactivity. Molecules 13:1671–1695

    CAS  Google Scholar 

  • Li J, Zhang Q, Li S, Dai W, Feng J, Wu L, Liu T, Chen K, Xia Y, Lu J (2017) The natural product fucoidan ameliorates hepatic ischemia–reperfusion injury in mice. Biomed Pharmacother 94:687–696

    CAS  Google Scholar 

  • Lim JD, Lee SR, Kim T, Jang SA, Kang SC, Koo HJ, Sohn E, Bak JP, Namkoong S, Kim HK, Song IS, Kim N, Sohn EH, Han J (2015) Fucoidan from Fucus vesiculosus protects against alcohol-induced liver damage by modulating inflammatory mediators in mice and HepG2 cells. Mar Drugs 13:1051–1067

    CAS  Google Scholar 

  • Mihara M, Uchiyama M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86:271–278

    CAS  Google Scholar 

  • Navarro JJ, Milena FF, Mora C, León C, Claverie F, Flores C, García J (2005) Tumor necrosis factor-α gene expression in diabetic nephropathy: relationship with urinary albumin excretion and effect of angiotensin-converting enzyme inhibition. Kidney Int 68:S98–S102

    Google Scholar 

  • Navarro-Gonzalez JF, Mora-Fernandez C (2008) The role of inflammatory cytokines in diabetic nephropathy. J Am Soc Nephrol 19:433–442

    CAS  Google Scholar 

  • Nishikimi M, Rao NA, Yagi K (1972) The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun 46:849–854

    CAS  Google Scholar 

  • Ogasawara N, Matsushima M, Kawamura N, Atsumi K, Yamaguchi T, Ochi H, Kusatsugu Y, Oyabu S, Hashimoto N, Hasegawa Y (2017) Modulation of immunological activity on macrophages induced by diazinon. Toxicology 379:22–30

    CAS  Google Scholar 

  • Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169

    CAS  Google Scholar 

  • Pakzad M, Fouladdel S, Nili-Ahmadabadi A, Pourkhalili N, Baeeri M, Azizi E, Sabzevari O, Ostad SN, Abdollahi M (2013) Sublethal exposures of diazinon alters glucose homostasis in Wistar rats: biochemical and molecular evidences of oxidative stress in adipose tissues. Pestic Biochem Physiol 105:57–61

    CAS  Google Scholar 

  • Pozharitskaya ON, Shikov AN, Faustova NM, Obluchinskaya ED, Kosman VM, Vuorela H, Makarov VG (2018) Pharmacokinetic and tissue distribution of fucoidan from Fucus vesiculosus after oral administration to rats. Mar Drugs 16:132

    Google Scholar 

  • Proskocil BJ, Grodzki ACG, Jacoby DB, Lein PJ, Fryer AD (2019) Organophosphorus pesticides induce cytokine release from differentiated human THP1 cells. Am J Respir Cell Mol Biol 61:620–630

    CAS  Google Scholar 

  • Reitman S, Frankel S (1957) A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am J Clin Pathol 28:56–63

    CAS  Google Scholar 

  • Shah MD, Iqbal M (2010) Diazinon-induced oxidative stress and renal dysfunction in rats. Food Chem Toxicol 48:3345–3353

    CAS  Google Scholar 

  • Slotkin TA, Skavicus S, Ko A, Levin ED, Seidler FJ (2019) Perinatal diazinon exposure compromises the development of acetylcholine and serotonin systems. Toxicology 424:152240. https://doi.org/10.1016/j.tox.2019.152240

    Article  CAS  Google Scholar 

  • Szasz G, Gruber W, Bernt E (1976) Creatine kinase in serum: 1 Determination of optimum reaction conditions. Clin Chem 22:650–656

    CAS  Google Scholar 

  • Thomes P, Rajendran M, Pasanban B, Rengasamy R (2010) Cardioprotective activity of Cladosiphon okamuranus fucoidan against isoproterenol induced myocardial infarction in rats. Phytomedicine 18:52–57

    CAS  Google Scholar 

  • Tietz N, Burtis C, Duncan P, Ervin K, Petitclerc C, Rinker A, Shuey D, Zygowicz E (1983) A reference method for measurement of alkaline phosphatase activity in human serum. Clin Chem 29:751–761

    CAS  Google Scholar 

  • Toledo-Ibarra G, Resendiz KD, Ventura-Ramón G, González-Jaime F, Vega-López A, Becerril-Villanueva E, Pavón L, Girón-Pérez M (2016) Oxidative damage in gills and liver in Nile tilapia (Oreochromis niloticus) exposed to diazinon. Comp Biochem Physiol A Mol Integr Physiol 200:3–8

    CAS  Google Scholar 

  • Vahidirad M, Arab-Nozari M, Mohammadi H, Zamani E, Shaki F (2018) Protective effect of captopril against diazinon induced nephrotoxicity and neurotoxicity via inhibition of ROS-NO pathway. Drug Chem Toxicol 41:287–293

    CAS  Google Scholar 

  • Voltan R, Secchiero P, Casciano F, Milani D, Zauli G, Tisato V (2016) Redox signaling and oxidative stress: cross talk with TNF-related apoptosis inducing ligand activity. Int J Biochem Cell Biol 81:364–374

    CAS  Google Scholar 

  • Wang D, Singhasemanon N, Goh KS (2017) A review of diazinon use, contamination in surface waters, and regulatory actions in California across water years 1992–2014. Environ Monit Assess 189:310

    Google Scholar 

  • Wang Y, Xing M, Cao Q, Ji A, Liang H, Song S (2019) Biological activities of fucoidan and the factors mediating its therapeutic effects: a review of recent studies. Mar Drugs 17:183

    CAS  Google Scholar 

  • Würzburg U, Hennrich N, Lang H, Prellwitz W, Neumeier D, Knedel M (1976) Determination of creatine kinase-MB in serum using inhibiting antibodies (author’s transl). Klin Wochenschr 54:357–360

    Google Scholar 

  • Yang JW, Yoon SY, Oh SJ, Kim SK, Kang KW (2006) Bifunctional effects of fucoidan on the expression of inducible nitric oxide synthase. Biochem Biophys Res Commun 346:345–350

    CAS  Google Scholar 

  • Yu X, Zhang Q, Cui W, Zeng Z, Yang W, Zhang C, Zhao H, Gao W, Wang X, Luo D (2014) Low molecular weight fucoidan alleviates cardiac dysfunction in diabetic Goto-Kakizaki rats by reducing oxidative stress and cardiomyocyte apoptosis. J Diabetes Res 2014:420929. https://doi.org/10.1155/2014/420929

    Article  Google Scholar 

  • Zhang Q, Li Z, Xu Z, Niu X, Zhang H (2003) Effects of fucoidan on chronic renal failure in rats. Planta Med 69:537–541

    CAS  Google Scholar 

Download references

Acknowledgements

The project was funded by Researchers Supporting Porject number (RSP-2019/121), King Saud University, Riyadh, Saudi.

Funding

This project was funded by the Researchers Supporting Project number (RSP-2019/121), King Saud University, Riyadh, Saudi Arabia.

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Authors and Affiliations

  1. Department of Zoology, College of Science, King Saud University, P.O. Box 2455, Riyadh, 11451, Saudi Arabia

    Mohamed M. Abdel-Daim, Mohamed S. Alyousif & Saad Alkahtani

  2. Department of Pharmacology, Faculty of Veterinary Medicine, Suez Canal University, Ismailia, 41522, Egypt

    Mohamed M. Abdel-Daim

  3. Faculty of Medicine, Ain Shams University, Cairo, Egypt

    Abdelrahman Ibrahim Abushouk

  4. Faculty of Medicine, Al-Azhar University, Damietta, Egypt

    Eshak I. Bahbah

  5. Department of Pharmacy, Faculty of Medicine and Pharmacy, University of Oradea, Oradea, Romania

    Simona G. Bungău

  6. Chrono-Environnement Laboratory, Bourgogne Franche-Comté University, UMR CNRS 6249, 25030, Besançon Cedex, France

    Lotfi Aleya

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  1. Mohamed M. Abdel-Daim
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  2. Abdelrahman Ibrahim Abushouk
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Correspondence to Mohamed M. Abdel-Daim.

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The Ethical Committee at the Faculty of Veterinary Medicine, Suez Canal University (Ismailia, Egypt) reviewed our experimental design and animal handling procedures (approval no. 201617).

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Abdel-Daim, M.M., Abushouk, A.I., Bahbah, E.I. et al. Fucoidan protects against subacute diazinon-induced oxidative damage in cardiac, hepatic, and renal tissues. Environ Sci Pollut Res 27, 11554–11564 (2020). https://doi.org/10.1007/s11356-020-07711-w

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