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3-Indolepropionic acid prevented chlorpyrifos-induced hepatorenal toxicities in rats by improving anti-inflammatory, antioxidant, and pro-apoptotic responses and abating DNA damage

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Abstract

The application of chlorpyrifos (CPF), an organophosphorus pesticide to control insects, is associated with oxidative stress and reduced quality of life in humans and animals. Indole-3-propionic acid (IPA) is a by-product of tryptophan metabolism with high antioxidant capacity and has the potential to curb CPF-mediated toxicities in the hepatorenal system of rats. It is against this background that we explored the subacute exposure of CPF and the effect of IPA in the liver and kidney of thirty rats using five cohort experimental designs (n = 6) consisting of control (corn oil 2 mL/kg body weight), CPF alone (5 mg/kg), IPA alone (50 mg/kg), CPF + IPA1 (5 mg/kg + 25 mg/kg), and CPF + IPA2 (5 mg/kg + 50 mg/kg). Subsequently, we evaluated biomarkers of hepatorenal damage, oxidative and nitrosative stress, inflammation, DNA damage, and apoptosis by spectrophotometric and enzyme-linked immunosorbent assay methods. Our results showed that co-treatment with IPA decreased CPF-upregulated serum hepatic transaminases, creatinine, and urea; reversed CPF downregulation of SOD, CAT, GPx, GST, GSH, Trx, TRx-R, and TSH; and abated CPF upregulation of XO, MPO, RONS, and LPO. Co-treatment with IPA decreased CPF-upregulated IL-1β and 8-OHdG levels, caspase-9 and caspase-3 activities, and increased IL-10. In addition, IPA averts CPF-induced histological changes in the liver and kidney of rats. Our results demonstrate that co-dosing CPF-exposed rats with IPA can significantly decrease CPF-induced oxidative stress, pro-inflammatory responses, DNA damage, and subsequent pro-apoptotic responses in rats’ liver and kidneys. Therefore, supplementing tryptophan-derived endogenous IPA from exogenous sources may help avert toxicity occasioned by inadvertent exposure to harmful chemicals, including CPF-induced systemic perturbation of liver and kidney function.

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References

  • Ahmad L, Dogar MZ-u-H (2016) Insecticidal exposure may be the cause of progression of immune disorders and inflammatory diseases through dys-regulation of cytokines. Int Arch BioMedical Clin Res 2:18–27

    Article  Google Scholar 

  • Ahmad MZ, Khan A, Javed MT, Hussain I (2015) Impact of chlorpyrifos on health biomarkers of broiler chicks. Pestic Biochem Physiol 122:50–58

    Article  CAS  Google Scholar 

  • Albasher G, Almeer R, Al-Otibi FO, Al-Kubaisi N, Mahmoud AM (2019a) Ameliorative effect of Beta vulgaris root extract on chlorpyrifos-induced oxidative stress, inflammation and liver injury in rats. Biomolecules 9(7):261.https://doi.org/10.3390/biom9070261

  • Albasher G, Almeer R, Alarifi S, Alkhtani S, Farhood M, Al-Otibi FO, Alkubaisi N, Rizwana H (2019b) Nephroprotective role of Beta vulgaris L. root extract against chlorpyrifos-induced renal injury in rats. Evid Based Complement Alternat Med. https://doi.org/10.1155/2019/3595761

  • Avma AVMA (2001) 2000 report of the AVMA Panel on Euthanasia. J Am Vet Med Assoc 218:669–696

    Article  Google Scholar 

  • Bancroft JD, Gamble M (2008) Theory and practice of histological techniques. Churchill Livingston/Elsevier, China

    Google Scholar 

  • Bendheim PE, Poeggeler B, Neria E, Ziv V, Pappolla MA, Chain DG (2002) Development of indole-3-propionic acid (OXIGON) for Alzheimer’s disease. J Mol Neurosci 19:213–217

    Article  CAS  Google Scholar 

  • Bergmeyer HI, Gawehn K, Grassl M (1974) Methods of enzymatic analysis, 1. Academic Press Incorporation, New York, NY

    Google Scholar 

  • Buege JAA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310

    Article  CAS  Google Scholar 

  • Clairborne A (1995) Catalase activity. Handbook of methods for oxygen radical research. CRC Press, Boca Raton, FL

    Google Scholar 

  • Cohen J (1992) A power primer. Psychol Bull 112:155–159

    Article  CAS  Google Scholar 

  • Deng Y, Zhang Y, Lu Y, Zhao Y, Ren H (2016) Hepatotoxicity and nephrotoxicity induced by the chlorpyrifos and chlorpyrifos-methyl metabolite, 3,5,6-trichloro-2-pyridinol, in orally exposed mice. Sci Total Environ 544:507–514

    Article  CAS  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77

    Article  CAS  Google Scholar 

  • El-Wakf AM, El-Habibi ESM, Barakat NM, Attia AM et al (2018) Cardiovascular toxic effects of chlorpyrifos: a possible protective role for pomegranate extracts. Journal of Clinical Toxicology 8:374. https://doi.org/10.4172/2161-0495.1000374

  • Ezzi L, Belhadj Salah I, Haouas Z, Sakly A, Grissa I, Chakroun S, Kerkeni E, Hassine M, Mehdi M, Ben Cheikh H (2016) Histopathological and genotoxic effects of chlorpyrifos in rats. Environ Sci Pollut Res Int 23:4859–4867

    Article  CAS  Google Scholar 

  • Faul F, Erdfelder E, Lang AG, Buchner A (2007) G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 39:175–191

    Article  Google Scholar 

  • Forrester SJ, Kikuchi DS, Hernandes MS, Xu Q, Griendling KK (2018) Reactive oxygen species in metabolic and inflammatory signaling. Circ Res 122:877–902

    Article  CAS  Google Scholar 

  • Fu DJ, Li P, Song J, Zhang SY, Xie HZ (2019) Mechanisms of synergistic neurotoxicity induced by two high risk pesticide residues - chlorpyrifos and carbofuran via oxidative stress. Toxicol in Vitro 54:338–344

    Article  CAS  Google Scholar 

  • Gangemi S, Gofita E, Costa C, Teodoro M, Briguglio G, Nikitovic D, Tzanakakis G, Tsatsakis AM, Wilks MF, Spandidos DA, Fenga C (2016) Occupational and environmental exposure to pesticides and cytokine pathways in chronic diseases (Review). Int J Mol Med 38:1012–1020

    Article  CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    Article  CAS  Google Scholar 

  • Hawkins P, Prescott MJ, Carbone L, Dennison N, Johnson C, Makowska IJ, Marquardt N, Readman G, Weary DM, Golledge HD (2016) A good death? Report of the Second Newcastle Meeting on Laboratory Animal Euthanasia. Animals (Basel) 6(9):50. https://doi.org/10.3390/ani6090050

  • Huc T, Nowinski A, Drapala A, Konopelski P, Ufnal M (2018) Indole and indoxyl sulfate, gut bacteria metabolites of tryptophan, change arterial blood pressure via peripheral and central mechanisms in rats. Pharmacol Res 130:172–179

    Article  CAS  Google Scholar 

  • Iwan P, Stepniak J, Karbownik-Lewinska M (2021a) Cumulative protective effect of melatonin and indole-3-propionic acid against KIO(3)-induced lipid peroxidation in porcine thyroid. Toxics 9(5):89. https://doi.org/10.3390/toxics9050089

  • Iwan P, Stepniak J, Karbownik-Lewinska M (2021b) Pro-oxidative effect of KIO3 and protective effect of melatonin in the thyroid-comparison to other tissues. Life (Basel) 11(6):592. https://doi.org/10.3390/life11060592

  • Jog NR, Caricchio R (2014) The role of necrotic cell death in the pathogenesis of immune mediated nephropathies. Clin Immunol 153:243–253

    Article  CAS  Google Scholar 

  • Jollow DJ, Mitchell JR, Zampaglione N, Gillette JR (1974) Bromobenzene-induced liver necrosis. Protective role of glutathione and evidence for 3,4-bromobenzene oxide as the hepatotoxic metabolite. Pharmacology 11:151–169

    Article  CAS  Google Scholar 

  • Karbownik M, Garcia JJ, Lewinski A, Reiter RJ (2001) Carcinogen-induced, free radical-mediated reduction in microsomal membrane fluidity: reversal by indole-3-propionic acid. J Bioenerg Biomembr 33:73–78

    Article  CAS  Google Scholar 

  • Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8:e1000412

    Article  Google Scholar 

  • Kokushi E, Uno S, Pal S, Koyama J (2015) Effects of chlorpyrifos on the metabolome of the freshwater carp, Cyprinus carpio. Environ Toxicol 30:253–260

    Article  CAS  Google Scholar 

  • Konopelski P, Ufnal M (2018) Indoles - gut bacteria metabolites of tryptophan with pharmacotherapeutic potential. Curr Drug Metab 19:883–890

    Article  CAS  Google Scholar 

  • Konopelski P, Konop M, Gawrys-Kopczynska M, Podsadni P, Szczepanska A, Ufnal M (2019) Indole-3-propionic acid, a tryptophan-derived bacterial metabolite, reduces weight gain in rats. Nutrients 11(3):591. https://doi.org/10.3390/nu11030591

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    Article  CAS  Google Scholar 

  • Mahmoud SM, Abdel Moneim AE, Qayed MM, El-Yamany NA (2019) Potential role of N-acetylcysteine on chlorpyrifos-induced neurotoxicity in rats. Environ Sci Pollut Res Int 26:20731–20741

    Article  CAS  Google Scholar 

  • Mansour SG, Verma G, Pata RW, Martin TG, Perazella MA, Parikh CR (2017) Kidney injury and repair biomarkers in marathon runners. Am J Kidney Dis 70:252–261

    Article  CAS  Google Scholar 

  • Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175

    Article  CAS  Google Scholar 

  • Moldogazieva NT, Lutsenko SV, Terentiev AA (2018a) Reactive oxygen and nitrogen species-induced protein modifications: implication in carcinogenesis and anticancer therapy. Cancer Res 78:6040–6047

    Article  CAS  Google Scholar 

  • Moldogazieva NT, Mokhosoev IM, Feldman NB, Lutsenko SV (2018b) ROS and RNS signalling: adaptive redox switches through oxidative/nitrosative protein modifications. Free Radic Res 52:507–543

    Article  CAS  Google Scholar 

  • Nalkurthi C, Schroder WA, Melino M, Irvine KM, Nyuydzefe M, Chen W, Liu J, Teng MWL, Hill GR, Bertolino P, Blazar BR, Miller GC, Clouston AD, Zanin-Zhorov A, MacDonald KPA (2022) ROCK2 inhibition attenuates profibrogenic immune cell function to reverse thioacetamide-induced liver fibrosis. JHEP Rep 4:100386

    Article  Google Scholar 

  • Nasr HM, El-Demerdash FM, El-Nagar WA (2016) Neuro and renal toxicity induced by chlorpyrifos and abamectin in rats: toxicity of insecticide mixture. Environ Sci Pollut Res Int 23:1852–1859

    Article  CAS  Google Scholar 

  • Owumi SE, Dim UJ (2019) Manganese suppresses oxidative stress, inflammation and caspase-3 activation in rats exposed to chlorpyrifos. Toxicol Rep 6:202–209

    Article  CAS  Google Scholar 

  • Owumi SE, Elebiyo TC, Oladimeji BN (2020): Oxido-inflammatory responses and histological alterations in rat lungs exposed to petroleum product fumes. Environ Toxicol. https://doi.org/10.1002/tox.23019

  • Owumi SE, Lewu DO, Arunsi UO, Oyelere AK (2021a) Luteolin attenuates doxorubicin-induced derangements of liver and kidney by reducing oxidative and inflammatory stress to suppress apoptosis. Hum Exp Toxicol 9603271211006171

  • Owumi SE, Otunla MT, Arunsi UO, Najophe ES (2021b) 3-Indolepropionic acid upturned male reproductive function by reducing oxido-inflammatory responses and apoptosis along the hypothalamic-pituitary-gonadal axis of adult rats exposed to chlorpyrifos. Toxicology 463:152996

    Article  CAS  Google Scholar 

  • Owumi SE, Adedara IA, Oyelere AK (2022a) Indole-3-propionic acid mitigates chlorpyrifos-mediated neurotoxicity by modulating cholinergic and redox-regulatory systems, inflammatory stress, apoptotic responses and DNA damage in rats. Environ Toxicol Pharmacol 89:103786. https://doi.org/10.1016/j.etap.2021.103786

  • Owumi SE, Irozuru CE, Arunsi UO, Oyelere AK (2022b) Caffeic acid protects against DNA damage, oxidative and inflammatory mediated toxicities, and upregulated caspases activation in the hepatorenal system of rats treated with aflatoxin B1. Toxicon 207:1–12

    Article  CAS  Google Scholar 

  • Ozturk Kurt B, Konukoglu D, Kalayci R, Ozdemir S (2022) Investigation of the protective role of selenium in the changes caused by chlorpyrifos in trace elements, biochemical and hematological parameters in rats. Biol Trace Elem Res 200:228–237

    Article  CAS  Google Scholar 

  • Pal S, Kokushi E, Koyama J, Uno S, Ghosh AR (2012) Histopathological alterations in gill, liver and kidney of common carp exposed to chlorpyrifos. J Environ Sci Health B 47:180–195

    Article  CAS  Google Scholar 

  • Palmer RM, Ferrige AG, Moncada S (1987) Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327:524–526

    Article  CAS  Google Scholar 

  • Peng X, Li L, Wang X, Zhang H (2022) A machine learning-based prediction model for acute kidney injury in patients with congestive heart failure. Front Cardiovasc Med 9:842873

    Article  Google Scholar 

  • Perez-Severiano F, Santamaria A, Pedraza-Chaverri J, Medina-Campos ON, Rios C, Segovia J (2004) Increased formation of reactive oxygen species, but no changes in glutathione peroxidase activity, in striata of mice transgenic for the Huntington’s disease mutation. Neurochem Res 29:729–733

    Article  CAS  Google Scholar 

  • Pizzino G, Irrera N, Cucinotta M, Pallio G, Mannino F, Arcoraci V, Squadrito F, Altavilla D, Bitto A (2017) Oxidative stress: harms and benefits for human health. Oxid Med Cell Longev 2017:8416763. https://doi.org/10.1155/2017/8416763

  • Qi W, Reiter RJ, Tan DX, Manchester LC, Siu AW, Garcia JJ (2000) Increased levels of oxidatively damaged DNA induced by chromium(III) and H2O2: protection by melatonin and related molecules. J Pineal Res 29:54–61

    Article  CAS  Google Scholar 

  • Rotruck JT, Pope AL, Ganther HE, Swanson AB, Hafeman DG, Hoekstra WG (1973) Selenium: biochemical role as a component of glutathione peroxidase. Science 179:588–590

    Article  CAS  Google Scholar 

  • Sams C, Cocker J, Lennard MS (2004) Biotransformation of chlorpyrifos and diazinon by human liver microsomes and recombinant human cytochrome P450s (CYP). Xenobiotica 34:861–873

    Article  CAS  Google Scholar 

  • Shahzad A, Khan A, Khan MZ, Mahmood F, Gul ST, Saleemi MK (2015) Immuno-pathologic effects of oral administration of chlorpyrifos in broiler chicks. J Immunotoxicol 12:16–23

    Article  CAS  Google Scholar 

  • Singh N, Lawana V, Luo J, Phong P, Abdalla A, Palanisamy B, Rokad D, Sarkar S, Jin H, Anantharam V (2018) Organophosphate pesticide chlorpyrifos impairs STAT1 signaling to induce dopaminergic neurotoxicity: implications for mitochondria mediated oxidative stress signaling events. Neurobiol Dis 117:82–113

    Article  CAS  Google Scholar 

  • Srinivas US, Tan BWQ, Vellayappan BA, Jeyasekharan AD (2019) ROS and the DNA damage response in cancer. Redox Biol 25:101084

    Article  CAS  Google Scholar 

  • Su LJ, Zhang JH, Gomez H, Murugan R, Hong X, Xu D, Jiang F, Peng ZY (2019) Reactive oxygen species-induced lipid peroxidation in apoptosis, autophagy, and ferroptosis. Oxid Med Cell Longev 2019:5080843. https://doi.org/10.1155/2019/5080843

  • Taha MAI, Badawy MEI, Abdel-Razik RK, Younis HM, Abo-El-Saad MM (2021) Mitochondrial dysfunction and oxidative stress in liver of male albino rats after exposing to sub-chronic intoxication of chlorpyrifos, cypermethrin, and imidacloprid. Pestic Biochem Physiol 178:104938

    Article  CAS  Google Scholar 

  • Tang J, Cao Y, Rose RL, Brimfield AA, Dai D, Goldstein JA, Hodgson E (2001) Metabolism of chlorpyrifos by human cytochrome P450 isoforms and human, mouse, and rat liver microsomes. Drug Metab Dispos 29:1201–1204

    CAS  Google Scholar 

  • Tang PM, Nikolic-Paterson DJ, Lan HY (2019) Macrophages: versatile players in renal inflammation and fibrosis. Nat Rev Nephrol 15:144–158

    Article  Google Scholar 

  • Tanvir EM, Afroz R, Chowdhury M, Gan SH, Karim N, Islam MN, Khalil MI (2016) A model of chlorpyrifos distribution and its biochemical effects on the liver and kidneys of rats. Hum Exp Toxicol 35:991–1004

    Article  CAS  Google Scholar 

  • Tewari D, Sah AN, Bawari S, Nabavi SF, Dehpour AR, Shirooie S, Braidy N, Fiebich BL, Vacca RA, Nabavi SM (2021) Role of nitric oxide in neurodegeneration: function, regulation, and inhibition. Curr Neuropharmacol 19:114–126

    Article  CAS  Google Scholar 

  • Trush MA, Egner PA, Kensler TW (1994) Myeloperoxidase as a biomarker of skin irritation and inflammation. Food Chem Toxicol 32:143–147

    Article  CAS  Google Scholar 

  • Unsal V, Dalkiran T, Cicek M, Kolukcu E (2020) The role of natural antioxidants against reactive oxygen species produced by cadmium toxicity: a review. Adv Pharm Bull 10:184–202

    Article  CAS  Google Scholar 

  • Verma RS, Mehta A, Srivastava N (2007) In vivo chlorpyrifos induced oxidative stress: attenuation by antioxidant vitamins. Pestic Biochem Physiol 88:191–196

    Article  CAS  Google Scholar 

  • Wang P, Dai H, Zhang C, Tian J, Deng Y, Zhao M, Zhao M, Bing G, Zhao L (2018) Evaluation of the effects of chlorpyrifos combined with lipopolysaccharide stress on neuroinflammation and spatial memory in neonatal rats. Toxicology 410:106–115

    Article  CAS  Google Scholar 

  • Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA, Peters EC, Siuzdak G (2009) Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci U S A 106:3698–3703

    Article  CAS  Google Scholar 

  • Workman P, Aboagye EO, Balkwill F, Balmain A, Bruder G, Chaplin DJ, Double JA, Everitt J, Farningham DA, Glennie MJ, Kelland LR, Robinson V, Stratford IJ, Tozer GM, Watson S, Wedge SR, Eccles SA, Committee of the National Cancer Research I (2010) Guidelines for the welfare and use of animals in cancer research. Br J Cancer 102:1555–77

    Article  CAS  Google Scholar 

  • Xie J, Wang M, Cheng A, Zhao XX, Liu M, Zhu D, Chen S, Jia R, Yang Q, Wu Y, Zhang S, Liu Y, Yu Y, Zhang L, Sun K, Chen X (2018) Cytokine storms are primarily responsible for the rapid death of ducklings infected with duck hepatitis A virus type 1. Sci Rep 8(1):6596. https://doi.org/10.1038/s41598-018-24729-w. Erratum in: Sci Rep. 2020 Mar 24;10(1):5672

  • Yazdinezhad A, Abbasian M, Hojjat Hosseini S, Naserzadeh P, Agh-Atabay A-H, Hosseini M-J (2017) Protective effects of Ziziphora tenuior extract against chlorpyrifos induced liver and lung toxicity in rat: mechanistic approaches in subchronic study. Environ Toxicol 32:2191–2202

    Article  CAS  Google Scholar 

  • Zhang X, Cui W, Wang K, Chen R, Chen M, Lan K, Wei Y, Pan C, Lan X (2020) Chlorpyrifos inhibits sperm maturation and induces a decrease in mouse male fertility. Environ Res 188:109785

    Article  CAS  Google Scholar 

  • Zhang Z, Liu Q, Cai J, Yang J, Shen Q, Xu S (2017) Chlorpyrifos exposure in common carp (Cyprinus carpio L.) leads to oxidative stress and immune responses. Fish Shellfish Immunol 67:604–611

    Article  CAS  Google Scholar 

  • Zhao L, Tang G, Xiong C, Han S, Yang C, He K, Liu Q, Luo J, Luo W, Wang Y (2021) Chronic chlorpyrifos exposure induces oxidative stress, apoptosis and immune dysfunction in largemouth bass (Micropterus salmoides). Environ Pollut 282:117010

    Article  CAS  Google Scholar 

  • Zhao MW, Yang P, Zhao LL (2019a) Chlorpyrifos activates cell pyroptosis and increases susceptibility on oxidative stress-induced toxicity by miR-181/SIRT1/PGC-1alpha/Nrf2 signaling pathway in human neuroblastoma SH-SY5Y cells: implication for association between chlorpyrifos and Parkinson’s disease. Environ Toxicol 34:699–707

    Article  CAS  Google Scholar 

  • Zhao ZH, Xin FZ, Xue Y, Hu Z, Han Y, Ma F, Zhou D, Liu XL, Cui A, Liu Z, Liu Y, Gao J, Pan Q, Li Y, Fan JG (2019b) Indole-3-propionic acid inhibits gut dysbiosis and endotoxin leakage to attenuate steatohepatitis in rats. Exp Mol Med 51:1–14

    Google Scholar 

  • Zhu L, Li B, Wu R, Li W, Wang J, Wang J, Du Z, Juhasz A, Zhu L (2020): Acute toxicity, oxidative stress and DNA damage of chlorpyrifos to earthworms (Eisenia fetida): The difference between artificial and natural soils. Chemosphere 55:126982. https://doi.org/10.1016/j.chemosphere

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Acknowledgements

The authors acknowledge Mr Uche Arunsi for his technical and editorial contribution.

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Authors and Affiliations

  1. Cancer Research and Molecular Biology Laboratories, Department of Biochemistry, Faculty of Basic Medical Sciences, University of Ibadan, Room NB 302, Ibadan, 200005, Nigeria

    Solomon E. Owumi & Moses T. Otunla

  2. Nutrition and Industrial Biochemistry Research Laboratories, Department of Biochemistry, Faculty of Basic Medical Sciences, University of Ibadan, Ibadan, 200005, Nigeria

    Eseroghene S. Najophe

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  1. Solomon E. Owumi
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  2. Eseroghene S. Najophe
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  3. Moses T. Otunla
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Contributions

Conceptualization: Solomon Owumi. Project administration, data curation, analysis, investigation: Sarah Najophe, Moses Otunla, Moses Otunla, and Solomon Owumi. Validation: Solomon Owumi, Sarah Najophe, and Moses Otunla. Writing, review, and editing: Solomon Owumi, Sarah Najophe, and Moses Otunla.

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Correspondence to Solomon E. Owumi.

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The experiment was approved by the University of Ibadan Animal Care and Use Research Ethics Committee (ACUREC) UI-ACUREC/033–0521/7 and follows the United States National Academy of Sciences guidelines.

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Owumi, S.E., Najophe, E.S. & Otunla, M.T. 3-Indolepropionic acid prevented chlorpyrifos-induced hepatorenal toxicities in rats by improving anti-inflammatory, antioxidant, and pro-apoptotic responses and abating DNA damage. Environ Sci Pollut Res 29, 74377–74393 (2022). https://doi.org/10.1007/s11356-022-21075-3

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