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Modulation of Immune Response by Organophosphate Pesticides: Mammals as Potential Model

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Abstract

Organophosphates (OPs) are most widely used pesticides and primarily induce toxicity by inhibition of acetylcholinesterase (AChE) in the nerve terminals of central and peripheral nervous system, leading to a variety of short-term and chronic effects in the non-target animals. In addition to acetylcholinesterase, OPs are known to potent inhibitors of serine hydrolases which are vital component of the immune system and therefore influence the immune functions. OPs induce several immunomodulatory effects in vertebrates by altering neutrophil function, macrophage production, antibody production, immunosuppression, reduced interleukin production and T cell proliferation. Immunotoxicity due to OP exposure is mediated through perturbation of the cholinergic response of lymphocytes, altering signal transduction, mutilating granule exocytosis pathway and impairing FasL/Fas pathway of natural killer cell and other immune related cells. Apoptosis of lymphocytes or immune related cells is promoted through mitochondrial pore formation and DNA fragmentation. In this review an attempt has been made to document the immunomodulatory effects of organophosphate pesticides using mammals as potential model with an additional information on the probable mechanism of immunotoxicity induced by OPs.

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References

  • Abdollahi, M., A. Ranjbar, S. Shadnia, S. Nikfar, and A. Rezaiee. 2004. Pesticides and oxidative stress: A review. Medical Science Monitor 10(6): 141–147.

    Google Scholar 

  • Adamkovicova, M., R. Toman, and M. Cabaj. 2010. Diazinon and cadmium acute testicular toxicityin rats examined by histopathological and morphometrical methods. Slovakian Journal of Animal Science 43(3): 134–140.

    Google Scholar 

  • Ader, R., D.L. Felten, and N. Cohen (eds.). 1991. Psychoneuroimmunology, 2nd ed, 27–69. San diego: Academic Press.

    Google Scholar 

  • Alberts, B., A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter. 2002. Adaptive immune system. Molecular Biology of the Cell 4: 1363–1402.

    Google Scholar 

  • Ayed-Boussema, I., K. Rjiba, N. Mnasri, A. Moussa, and H. Bacha. 2012. Genotoxicity evaluation of dimethoateto experimental mice by micronucleus, chromosome aberration tests, and comet assay. International Journal of Toxicology 31(1): 78–85.

    Article  CAS  PubMed  Google Scholar 

  • Banks, C.N., and P.J. Lein. 2012. A review of experimental evidence linking neurotoxic organophosphorus compounds and inflammation. Neurotoxicology 33(3): 575–584.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barnett, J.B., and K.E. Rodgers. 1994. Pesticides. In Immunotoxicology and Immunopharmacology. 2nd ed, ed. J.H. Dean, M.I. Luster, A.E. Munson, and I. Kimber, 191–226. New York: Raven Press.

    Google Scholar 

  • Battaglia, C.L., R.M. Gogal Jr., K. Zimmerman, and H.P. Misra. 2010. Malathion, lindane, and piperonylbutoxide, individually or in combined mixtures, induce immunotoxicity via apoptosis in murine splenocytes in vitro. International Journal of Toxicology 29(2): 209–220.

    Article  CAS  PubMed  Google Scholar 

  • Blakley, B.R., M.J. Yole, P. Brousseau, H. Boermans, and M. Fournier. 1999. Effect of chlorpyrifos on immune function in rats. Veterinary and Human Toxicology 41(3): 140–144.

    CAS  PubMed  Google Scholar 

  • Blalock, J.E. 1994. The syntax of immune–neuroendocrine communication. Immunology Today 15: 504–511.

    Article  CAS  PubMed  Google Scholar 

  • Blanco, G.A. 2011. Immune response to environmental exposure. Elsevier. https://doi.org/10.1016/b978-0-444-52272-6.00502-x.

    Article  Google Scholar 

  • Bolognesi, C. 2003. Genotoxicity of pesticides: A review of human biomonitoring studies. Mutation Research/Reviews in Mutation Research 543(3): 251–272.

    Article  CAS  Google Scholar 

  • Borovikova, L.V., S. Ivanova, M. Zhang, H. Yang, G.I. Botchkina, L.R. Watkins, H. Wang, N. Abumrad, J.W. Eaton, and K.J. Tracey. 2000. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 405: 458–562.

    Article  CAS  Google Scholar 

  • Buratti, F.M., M.T. Volpe, A. Meneguz, L. Vittozzi, and E. Testai. 2003. CYP-specific bioactivation of four organophosphorothionate pesticides by human liver microsomes. Toxicology and Applied Pharmacology 86: 143–154.

    Article  CAS  Google Scholar 

  • Cabaj, M., R. Toman, M. Adamkovicova, P. Massányi, B. Siska, N. Lukac, and J. Golian. 2010. Structural changes in the rat testis caused by diazinon and selenium. Potravinarstvo 4(2): 8–16.

    Google Scholar 

  • Casale, G.P., S. Bavari, and J.J. Connolly. 1989. Inhibition of human serum complement activity by diisopropylfluorophosphate and selected anticholinesterase insecticides. Toxicological Sciences 12(3): 460–468.

    Article  CAS  Google Scholar 

  • Casale, G.P., S.D. Cohen, and R.A. DiCapua. 1983. The effects of organophosphate-induced cholinergic stimulation on the antibody response to sheep erythrocytes in inbred mice. Toxicology and Applied Pharmacology 68(2): 198–205.

    Article  CAS  PubMed  Google Scholar 

  • Casale, G.P., J.L. Vennerstrom, S. Bavari, and T.L. Wang. 1993. Inhibition of interleukin 2 driven proliferation of mouse CTLL2 cells, by selected carbamate and organophosphate insecticides and congeners of carbaryl. Immunopharmacology and Immunotoxicology 15(2–3): 199–215.

    Article  CAS  PubMed  Google Scholar 

  • Charoenying, T., T. Suriyo, A. Thiantanawat, S.C. Chaiyaroj, P. Parkpian, and J. Satayavivad. 2011. Effects of paraoxon on neuronal and lymphocytic cholinergic systems. Environmental Toxicology and Pharmacology 31(1): 119–128.

    Article  CAS  PubMed  Google Scholar 

  • Cohney, S.J., D. Sanden, N.A. Cacalano, A. Yoshimura, A. Mui, T.S. Migone, and J.A. Johnston. 1999. SOCS-3 is tyrosine phosphorylated in response to interleukin-2 and suppresses STAT5 phosphorylation and lymphocyte proliferation. Molecular and Cellular Biology 19(7): 4980–4988.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corsini, E., M. Sokooti, C.L. Galli, A. Moretto, and C. Colosio. 2013. Pesticide induced immunotoxicity in humans: A comprehensive review of the existing evidence. Toxicology 307: 123–135.

    Article  CAS  PubMed  Google Scholar 

  • Descotes, J. 2004. Importance of immunotoxicity in safety assessment: A medical toxicologist’s perspective. Toxicology Letters 149(1): 103–108.

    Article  CAS  PubMed  Google Scholar 

  • Díaz-Resendiz, K.J.G., G.A. Toledo-Ibarra, and M.I. Girón-Pérez. 2015. Modulation of immune response by organophosphorus pesticides: Fishes as a potential model in immunotoxicology. Journal of Immunology Research. 2015: Article ID 213836.http://dx.doi.org/10.1155/2015/213836.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dietert, R.R. 2008. Developmental immunotoxicology (DIT): Windows of vulnerability, immune dysfunction and safety assessment. Journal of Immunotoxicology 5: 401–412.

    Article  PubMed  Google Scholar 

  • Dimitriou, I.D., L. Clemenza, A.J. Scotter, G. Chen, F.M. Guerra, and R. Rottapel. 2008. Putting out the fire: Coordinated suppression of the innate and adaptive immune systems by SOCS1 and SOCS3 proteins. Immunological Reviews 224(1): 265–283.

    Article  CAS  PubMed  Google Scholar 

  • Esquivel-Sentíes, M.S., I. Barrera, A. Ortega, and L. Vega. 2010. Organophosphorous pesticide metabolite (DEDTP) induces changes in the activation status of human lymphocytes by modulating the interleukin 2 receptor signal transduction pathway. Toxicology and Applied Pharmacology 248(2): 122–133.

    Article  CAS  PubMed  Google Scholar 

  • Farag, A.T., A.H. Radwan, F. Sorour, A. El-Okazy, E. El-Agamy, and A.E. El-Sebae. 2010. Chlorpyrifos induced reproductive toxicity in male mice. Reproductive Toxicology 29(1): 80–88.

    Article  CAS  PubMed  Google Scholar 

  • Faustini, A., L. Settimi, and R. Pacifici. 1996. Immunological changes among farmers exposed to phenoxy herbicides: Preliminary observations. Occupational and Environmental Medicine 53: 583–585.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felten, S.Y., and D.L. Felten. 1994. Neural-immune interactions. Progress in Brain Research 100: 157–162.

    Article  CAS  PubMed  Google Scholar 

  • Fukuyama, T., T. Kosaka, Y. Tajima, H. Ueda, K. Hayashi, Y. Shutoh, and T. Harada. 2010. Prior exposure to organophosphorus and organochlorine pesticides increases the allergic potential of environmental chemical allergens in a local lymph node assay. Toxicology Letters 199(3): 347–356.

    Article  CAS  PubMed  Google Scholar 

  • Galloway, T., and R. Handy. 2003. Immunotoxicity of organophosphorous pesticides. Ecotoxicology 12(1–4): 345–363.

    Article  CAS  PubMed  Google Scholar 

  • Germolec, D.R., N.H. Adams, and M.I. Luster. 1997. The importance of enzymatic biotransformation in immunotoxicology. Reviews in Toxicology 1(7): 33–51.

    CAS  Google Scholar 

  • Gupta, R.C., D. Milatovic, and W.D. Dettbarn. 2001. Depletion of energy metabolites following acetylcholinesterase inhibitor-induced status epilepticus: Protection by antioxidants. Neurotoxicology 22(2): 271–282.

    Article  CAS  PubMed  Google Scholar 

  • Handy, R.D., H.A. Abd-El Samei, M.F.F. Bayomy, A.M. Mahran, A.M. Abdeen, and E.A. El-Elaimy. 2002. Chronic diazinon exposure: Pathologies of spleen, thymus, blood cells, and lymph nodes are modulated by dietary protein or lipid in the mouse. Toxicology 172(1): 13–34.

    Article  CAS  PubMed  Google Scholar 

  • Hermanowicz, A., and S. Kossman. 1984. Neutrophil function and infectious disease in workers occupationally exposed to phosphoorganic pesticides: Role of mononuclear-derived chemotactic factor for neutrophils. Clinical Immunology and Immunopathology 33(1): 13–22.

    Article  CAS  PubMed  Google Scholar 

  • Holladay, S.D. 1999. Prenatal immunotoxicant exposure and postnatal autoimmune disease. Environmental Health Perspectives 107(5): 687.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hoppin, J.A., M. Valcin, P.K. Henneberger, G.J. Kullman, D.M. Umbach, S.J. London, M.C. Alavanja, and D.P. Sandler. 2007. Pesticide use and chronic bronchitis among farmers in the Agricultural Health Study. American Journal of Industrial Medicine 50(12): 969–979.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jaga, K., and C. Dharmani. 2005. The epidemiology of pesticide exposure and cancer: A review. Reviews on Environmental Health 20(1): 15–38.

    Article  CAS  PubMed  Google Scholar 

  • Johnson, V.J., A.M. Rosenberg, K. Lee, and B.R. Blakley. 2002. Increased T-lymphocyte dependent antibody production in female SJL/J mice following exposure to commercial grade malathion. Toxicology 170(1): 119–129.

    Article  CAS  PubMed  Google Scholar 

  • Kawashima, K., and T. Fujii. 2000. Extraneuronal cholinergic system in lymphocytes. Pharmacology and Therapeutics 86(1): 29–48.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, A., A. Bhaskar, S. Chandra, D. Sasmal, K.M. Mukhopadhyay, and N. Sharma. 2015. Mechanism of deltamethrin induced immunotoxicity: Current and future perspectives. Receptors and Clinical Investigation 2(2): 1–7.

    Google Scholar 

  • Lasram, M.M., A.J. Lamine, I.B. Dhouib, K. Bouzid, A. Annabi, N. Belhadjhmida, M.B. Ahmed, S. El Fazaa, J. Abdelmoula, and N. Gharbi. 2014. Antioxidant and anti-inflammatory effects of N-acetylcysteine against malathion-induced liver damages and immunotoxicity in rats. Life Sciences 107(1): 50–58.

    Article  CAS  PubMed  Google Scholar 

  • Lee, C.H., M. Kamijima, H. Kim, E. Shibata, J. Ueyama, T. Suzuki, K. Takagi, I. Saito, M. Gotoh, H. Hibi, and H. Naito. 2007. 8-Hydroxydeoxyguanosine levels in human leukocyte and urine according to exposure to organophosphorus pesticides and paraoxonase 1 genotype. International Archives of Occupational and Environmental Health 80(3): 217–227.

    Article  CAS  PubMed  Google Scholar 

  • Li, Q. 2007. New mechanism of organophosphorus pesticide-induced immunotoxicity. Journal of Nippon Medical School 74(2): 92–105.

    Article  CAS  PubMed  Google Scholar 

  • Li, Q., N. Nagahara, H. Takahashi, K. Takeda, K. Okumura, and M. Minami. 2002. Organophosphorus pesticides markedly inhibit the activities of natural killer, cytotoxic T lymphocyte and lymphokine-activated killer: A proposed inhibiting mechanism via granzyme inhibition. Toxicology 172(3): 181–190.

    Article  CAS  PubMed  Google Scholar 

  • Li, Q., A. Nakadai, K. Takeda, and T. Kawada. 2004. Dimethyl 2, 2-dichlorovinyl phosphate (DDVP) markedly inhibits activities of natural killer cells, cytotoxic T lymphocytes and lymphokine-activated killer cells via the Fas-ligand/Fas pathway in perforin-knockout (PKO) mice. Toxicology 204(1): 41–50.

    Article  CAS  PubMed  Google Scholar 

  • Li, Q., A. Nakadai, M. Ishizaki, K. Morimoto, A. Ueda, A.M. Krensky, and T. Kawada. 2005. Dimethyl 2, 2-dichlorovinyl phosphate (DDVP) markedly decreases the expression of perforin, granzyme A and granulysin in human NK-92CI cell line. Toxicology 213(1): 107–116.

    Article  CAS  PubMed  Google Scholar 

  • Li, Q., and T. Kawada. 2006. The mechanism of organophosphoruspesticideinduced inhibition of cytolytic activity of killer cells. Cellular and Molecular Immunology 3(3): 171–178.

    CAS  PubMed  Google Scholar 

  • Lima, A., and L. Vega. 2005. Methyl-parathion and organophosphorous pesticide metabolites modify the activation status and interleukin-2 secretion of human peripheral blood mononuclear cells. Toxicology Letters 158(1): 30–38.

    Article  CAS  PubMed  Google Scholar 

  • Luebke, B. 2002. Pesticide-induced immunotoxicity: Are humans atrisk? Human Ecol Risk International Journal of Life Cycle Assesment 8: 293–303.

    Article  Google Scholar 

  • Luster, M.I., C. Portier, D.G. Paît, K.L. White, C. Gennings, A.E. Munson, and G.J. Rosenthal. 1992. Risk assessment in immunotoxicology I. Sensitivity and predictability of immune tests. Toxicological Sciences 18(2): 200–210.

    Article  CAS  Google Scholar 

  • Luster, M.I., and G.J. Rosenthal. 1993. Chemical agents and the immune response. Environmental Health Perspectives 100: 219.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Magnarelli, G., and T. Fonovich. 2013. Protein phosphorylation pathways disruption by pesticides. Advances in Biological Chemistry 3(05): 460.

    Article  CAS  Google Scholar 

  • Maitra, S.K., and A. Mitra. 2008. Testicular functions and serum titers of LH and testosterone in methyl parathion-fed roseringed parakeets. Ecotoxicology and Environmental Safety 71(1): 236–244.

    Article  CAS  PubMed  Google Scholar 

  • Malek, T.R. 2008. The biology of interleukin-2. Annual Review of Immunology 26: 453–479.

    Article  CAS  PubMed  Google Scholar 

  • Marx, C., M. Ehrhart-Bornstein, W.A. Scherbaum, and S.R. Bornstein. 1998. Regulation of adrenocortical function by cytokines—relevance for immune–endocrine interaction. Hormone and Metabolic Research 30: 416–420.

    Article  CAS  PubMed  Google Scholar 

  • Matin, M.A., S. Sattar, and K. Husain. 1990. Modification of malathion induced neurochemical changes by adrenalectomy in rats. Molecular and Chemical Neuropathology 13: 119–128.

    Article  CAS  PubMed  Google Scholar 

  • Mecdad, A.A., M.H. Ahmed, M.E. El Halwagy, and M.M. Afify. 2011. A study on oxidative stress biomarkers and immunomodulatory effects of pesticides in pesticide-sprayers. Egyptian Journal of Forensic Sciences 1(2): 93–98.

    Article  Google Scholar 

  • Mitra, A., and S.K. Maitra. 2004. Influences of two commonly used organophosphate pesticides, methyl parathion and phosphamidon, on the reproductive activities of female spotted munia (Lonchurapunctulata): A comparative study. In Curent Issue in Environmental and Fish Biology, ed. S. Bhattachara and S.K. Maitra. New Delhi: Daya Publishing House.

    Google Scholar 

  • Mokarizadeh, A., M.R. Faryabi, M.A. Rezvanfar, and M. Abdollahi. 2015. A comprehensive review of pesticides and the immune dysregulation: Mechanisms, evidence and consequences. Toxicology Mechanism and Methods 25(4): 258–278.

    Article  CAS  Google Scholar 

  • Monteiro, D.A., J.A. De Almeida, F.T. Rantin, and A.L. Kalinin. 2006. Oxidative stress biomarkers in the freshwater characid fish, Bryconcephalus, exposed to organophosphorus insecticide Folisuper 600 (methyl parathion). Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 143(2): 141–149.

    PubMed  Google Scholar 

  • Muller, U., P. Vogel, G. Alber, and G. Schaub. 2008. The innate immune system of mammals and insects. In Trends in Innate Immunity, vol. 15, ed. A. Egesten, A. Schmidt, and H. Herwald, 21–44. Basel: Karger Publishers.

    Google Scholar 

  • Murphy, E.C., A.M. Springer, and D.G. Roseneau. 1986. Population status of Common Guillemots Uriaaalge at a colony in western Alaska: Results and simulations. Ibis 128(3): 348–363.

    Article  Google Scholar 

  • Nakadai, A., Q. Li, and T. Kawada. 2006. Chlorpyrifos induces apoptosis in human monocyte cell line U937. Toxicology 224(3): 202–209.

    Article  CAS  PubMed  Google Scholar 

  • Orsi, L., L. Delabre, A. Monnereau, P. Delval, C. Berthou, P. Fenaux, G. Marit, P. Soubeyran, F. Huguet, N. Milpied, M. Leporrier, D. Hemon, X. Troussard, and J. Clavel. 2009. Occupational exposure to pesticides and lymphoid neoplasms among men: Results of a French case-control study. Occupationl and Environmental Medicine 66: 291–298.

    Article  CAS  Google Scholar 

  • Parrillo, J.E., and A.S. Fauci. 1979. Mechanisms of glucocorticoid action on immune processes. Annual Review 19(1): 29–201.

    Google Scholar 

  • Persson, E.C., B.I. Graubard, A.A. Evans, W.T. London, J.P. Weber, A. LeBlanc, G. Chen, W. Lin, and K.A. McGlynn. 2012. Dichlorodiphenyltrichloroethane and risk of hepatocellular carcinoma. International Journal of Cancer 131(9): 2078–2084.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prabhavathy Das, G., A. Pasha Shaik, and K. Jamil. 2006. Estimation of apoptosis and necrosis caused by pesticides in vitro on human lymphocytes using DNA diffusion assay. Drug and Chemical Toxicology 29(2): 147–156.

    Article  CAS  PubMed  Google Scholar 

  • Pruett, S.B., and J.E. Chambers. 1988. Effects of paraoxon, p-nitrophenol, phenyl saligenin cyclic phosphate, and phenol on the rat interleukin 2 system. Toxicology Letters 40(1): 11–20.

    Article  CAS  PubMed  Google Scholar 

  • Rahimi, R., and M. Abdollahi. 2007. A review on the mechanisms involved in hyperglycemia induced by organophosphorus pesticides. Pesticide Biochemistry and Physiology 88(2): 115–121.

    Article  CAS  Google Scholar 

  • Ranjbar, A., P. Pasalar, A. Sedighi, and M. Abdollahi. 2002. Induction of oxidative stress in paraquat formulating workers. Toxicology Letters 131(3): 191–194.

    Article  CAS  PubMed  Google Scholar 

  • Rodgers, K.E. 1997. Effects of oral administration of malathion on the course of disease in MRL-lpr mice. Journal of Autoimmunity 10(4): 367–373.

    Article  PubMed  Google Scholar 

  • Rodgers, K.E., and S. Xiong. 1997. Contribution of inflammatory mast cell mediators to alterations in macrophage function after malathion administration. International Journal of Immunopharmacology 19: 149–156.

    Article  CAS  PubMed  Google Scholar 

  • Rodgers, K.E., and D.D. Ellefson. 1990. Modulation of macrophage protease activity by acute administration of O, O, S trimethylphosphorothioate. Agents and Actions 29(3–4): 277–285.

    Article  CAS  PubMed  Google Scholar 

  • Rubin, R.T., S.M. O’Toole, M.E. Rhodes, L.K. Sekula, and R.K. Czambel. 1999. Hypothalamo-pituitary-adrenal cortical responses to low-dose physostigmine and arginine vasopressin administration: Sex differences between major depressives andmatched control subjects. Psychiatry Research 89: 1–20.

    Article  CAS  PubMed  Google Scholar 

  • Saleh, A.M., C. Vijayasarathy, M. Fernandez-Cabezudo, M. Taleb, and G. Petroianu. 2003a. Influence of paraoxon (POX) and parathion (PAT) on apoptosis: A possible mechanism for toxicity in low-dose exposure. Journal of Applied Toxicology 23(1): 23–29.

    Article  CAS  PubMed  Google Scholar 

  • Saleh, A.M., C. Vijayasarathy, L. Masoud, L. Kumar, A. Shahin, and A. Kambal. 2003b. Paraoxon induces apoptosis in EL4 cells via activation of mitochondrial pathways. Toxicology and Applied Pharmacology 190(1): 47–57.

    Article  CAS  PubMed  Google Scholar 

  • Sandhu, M.S., A.A. Saeed, M.S. Khilji, A. Ahmed, M.S.Z. Latif, and N. Khalid. 2013. Genotoxicity evaluation of chlorpyrifos: A gender related approach in regular toxicity testing. Journal of Toxicological Science 38(2): 237–244.

    Article  CAS  Google Scholar 

  • Sarkar, R., K.P. Mohanakumar, and M. Chowdhary. 2000. Effects of an organophosphate pesticide, quinalphos, on the hypothalamo-pituitary-gonadal axis in albino rats. Journal of Reproduction and Fertility 118(1): 29–38.

    Article  CAS  Google Scholar 

  • Schafer, M., F. Koppe, and B. Stenger. 2013. Influence of organophosphate poisoning on human dendritic cells. Chemico Biological Interaction 206: 472–478.

    Article  CAS  Google Scholar 

  • Sharma, Y., S. Bashir, M. Irshad, S.D. Gupta, and T.D. Dogra. 2005. Effects of acute dimethoate administration on antioxidant status of liver and brain of experimental rats. Toxicology 206(1): 49–57.

    Article  CAS  PubMed  Google Scholar 

  • Singh, A.K., A. Parashar, A.K. Singh, and R. Singh. 2013. Pre-natal/juvenile chlorpyrifos exposure associated with immunotoxicity in adulthood in Swiss albino mice. Journal of Immunotoxicology 10(2): 141–149.

    Article  CAS  PubMed  Google Scholar 

  • Slager, R.E., S.L. Simpson, T.D. LeVan, J.A. Poole, D.P. Sandler, and J.A. Hoppin. 2010. Rhinitis associated with pesticide use among private pesticide applicators in the agricultural health study. Journal of Toxicology and Environmental Health, Part A 73(20): 1382–1393.

    Article  CAS  Google Scholar 

  • Sobel, E.S., F. Wang, E. Butfiloski, B. Croker, and S.M. Roberts. 2006. Comparison of chlordecone effects on autoimmunity in (NZBxNZW) F 1 and BALB/c mice. Toxicology 218(2): 81–89.

    Article  CAS  PubMed  Google Scholar 

  • Sogorb, M.A., and E. Vilanova. 2002. Enzymes involved in the detoxification of organophosphorus, carbamate and pyrethroid insecticides through hydrolysis. Toxicology Letters 128(1): 215–228.

    Article  CAS  PubMed  Google Scholar 

  • Stephen, P.L.C.R.C., and B. Pruett. 1998. Immunotoxicological assessment of methyl parathion in female B6C3F1 mice. Journal of Toxicology and Environmental Health Part A 54(1): 1–20.

    Article  Google Scholar 

  • Stiller-Winkler, R., W. Hadnagy, G. Leng, E. Straube, and H. Idel. 1999. Immunological parameters in humans exposed to pesticides in the agricultural environment. Toxicology Letters 107(1): 219–224.

    Article  CAS  PubMed  Google Scholar 

  • Tarkowski, M.A.C.I.E.J., W. Lutz, and S. Birindelli. 2004. The lymphocytic cholinergic system and its modulation by organophosphorus pesticides. International Journal of Occupational Medicine and Environmental Health 17(3): 325–337.

    PubMed  Google Scholar 

  • Terry, A.V. 2012. Functional consequences of repeated organophosphate exposure: Potential non-cholinergic mechanisms. Pharmacology and Therapeutics 134(3): 355–365.

    Article  CAS  PubMed  Google Scholar 

  • Thrasher, J.D., G. Heuser, and A. Broughton. 2002. Immunological abnormalities in humans chronically exposed to chlorpyrifos. Archives of Environmental Health: An International Journal 57(3): 181–187.

    Article  CAS  Google Scholar 

  • Timofeeva, O.A., C.S. Roegge, F.J. Seidler, T.A. Slotkin, and E.D. Levin. 2008. Persistent cognitive alterations in rats after early postnatal exposure to low doses of the organophosphate pesticide, diazinon. Neurotoxicology and Teratology 30(1): 38–45.

    Article  CAS  PubMed  Google Scholar 

  • Vasilic, Z., V. Drevenkar, V. Rumenjak, B. Stengl, and Z. Frobe. 1992. Urinary excretion of diethylphosphorus metabolites in persons poisoned by quinalphos or chlorpyrifos. Archives of Environmental Contamination and Toxicology 22(4): 351–357.

    Article  CAS  PubMed  Google Scholar 

  • Vermes, I., C. Haanen, H. Steffens-Nakken, and C. Reutellingsperger. 1995. A novel assay for apoptosis flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled annexin V. Journal of Immunological Methods 184(1): 39–51.

    Article  CAS  PubMed  Google Scholar 

  • Veronesi, B., M. Ehrich, J.K. Blusztajn, M. Oortgiesen, and H. Durham. 1996. Cell culture models of interspecies selectivity to organophosphorous insecticides. Neurotoxicology 18(1): 283–297.

    Google Scholar 

  • Vial, T., B. Nicolas, and J. Descotes. 1996. Clinical immunotoxicity of pesticides. Journal of Toxicology and Environmental Health 48(3): 215–229.

    Article  CAS  PubMed  Google Scholar 

  • Voccia, I., B. Blakley, P. Brousseau, and M. Foumier. 1999. Immunotoxicity of pesticides: A review. Toxicological and Industrial Health 15: 119–132.

    Article  CAS  Google Scholar 

  • Wang, F., S.M. Roberts, E.J. Butfiloski, L. Morel, and E.S. Sobel. 2007. Acceleration of autoimmunity by organochlorine pesticides: A comparison of splenic B-cell effects of chlordecone and estradiol in (NZBxNZW) F1 mice. Toxicological Sciences 99(1): 141–152.

    Article  CAS  PubMed  Google Scholar 

  • Wang, C.Y., C.L. Wu, Y.T. Tsan, J.Y. Hsu, D.Z. Hung, and C.H. Wang. 2010. Early onset pneumonia in patients with cholinesterase inhibitor poisoning. Respirology 15(6): 961–968.

    Article  PubMed  Google Scholar 

  • Watanabe, W., H. Yoshida, A. Hirose, T. Akashi, T. Takeshita, N. Kuroki, A. Shibata, S. Hongo, S. Hashiguchi, K. Konno, and M. Kurokawa. 2013. Perinatal exposure to insecticide methamidophos suppressed production of proinflammatory cytokines responding to virus infection in lung tissues in mice. BioMed Research International. 2013: Article ID 151807. http://dx.doi.org/10.1155/2013/151807.

    Article  PubMed  PubMed Central  Google Scholar 

  • Weselak, M., T.E. Arbuckle, D.T. Wigle, and D. Krewski. 2007. In utero pesticide exposure and childhood morbidity. Environmental Research 103(1): 79–86.

    Article  CAS  PubMed  Google Scholar 

  • Wong, S., M. Fournier, D. Coderre, W. Banska, and K. Krzystyniak. 1992. Environmental immunotoxicology. Animal Biomarkers as Pollution Indicators, 167–189. Netherlands: Springer.

    Chapter  Google Scholar 

  • Xia, C., M. Wang, Q. Liang, et al. 2014. Changes in monoclonal HLADR antigen expression in acute organophosphorus pesticide-poisoned patients. Experimental and Therapeutic Medicine 7: 137–140.

    Article  CAS  PubMed  Google Scholar 

  • Yanagisawa, R., H. Takano, K.I. Inoue, E. Koike, K. Sadakane, and T. Ichinose. 2008. Effects of maternal exposure to di-(2-ethylhexyl) phthalate during fetal and/or neonatal periods on atopic dermatitis in male offspring. Environmental Health Perspectives 116(9): 1136.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhuang, S., Z. Zhang, W. Zhang, L. Bao, C. Xu, and H. Zhang. 2015. Enantioselective developmental toxicity and immunotoxicity of pyraclofos toward zebrafish (Daniorerio). Aquatic Toxicology 159: 119–126.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Authors wish to convey sincere thanks to Principal, Bankura Christian College for his support. Mr. Arup Ruidas is thankfully acknowledged for the illustrations in the review.

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Correspondence to Anindita Mitra.

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Mitra, A., Sarkar, M. & Chatterjee, C. Modulation of Immune Response by Organophosphate Pesticides: Mammals as Potential Model. Proc Zool Soc 72, 13–24 (2019). https://doi.org/10.1007/s12595-017-0256-5

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  • DOI: https://doi.org/10.1007/s12595-017-0256-5

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