1,799
Views
6
CrossRef citations to date
0
Altmetric
Research Articles

Low-dose endosulfan inhibits proliferation and induces senescence and pro-inflammatory cytokine production in human lymphocytes, preferentially impacting cytotoxic cells

, , , , &
Pages 173-181 | Received 04 Mar 2019, Accepted 11 Sep 2019, Published online: 07 Oct 2019

References

  • Ahmed T, Tripathi A, Ahmed R, Das S, Suke S, Pathak R, Chakraboti A, Banerjee B. 2008. Endosulfan-induced apoptosis and glutathione depletion in human peripheral blood mononuclear cells: Attenuation by N-acetylcysteine. J Biochem Mol Toxicol. 22(5):299–304.
  • Alam S, Laughton D, Walding A, Wolstenholme A. 2006. Human peripheral blood mononuclear cells express GABAA receptor subunits. Mol Immunol. 43(9):1432–1442.
  • Antherieu S, Ledirac N, Luzy A, Lenormand P, Caron J, Rahmani R. 2007. Endosulfan decreases cell growth and apoptosis in human HaCaT keratinocytes: Partial ROS-dependent ERK1/2 mechanism. J Cell Physiol. 213(1):177–186.
  • Attaullah M, Yousuf MJ, Shaukat S, Anjum SI, Ansari MJ, Buneri ID, Tahir M, Amin M, Ahmad N, Khan SU. 2018. Serum organochlorine pesticides residues and risk of cancer: A case-control study. Saudi J Biol Sci. 25(7):1284–1290.
  • Bjurstöm H, Wang J, Wang J, Ericsson I, Bengtsson M, Liu Y, Kumar-Mendu S, Issazadeh-Navikas S, Birnir B. 2008. GABA, a natural immunomodulator of T-lymphocytes. J Neuroimmunol. 205(1–2):44–50.
  • Bulayeva N, Watson C. 2004. Xenoestrogen-induced ERK-1 and ERK-2 activation via multiple membrane-initiated signaling pathways. Environ Health Perspect. 112(15):1481–1487.
  • Campisi J, d'Adda di Fagagna F. 2007. Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Bio 8:729–740.
  • Campoy C, Jimenez M, Olea-Serrano M, Moreno Frias M, Cañabate F, Olea N, Bayés R, Molina-Font J. 2001. Analysis of organochlorine pesticides in human milk: Preliminary results. Early Human Dev. 65:183–190.
  • Canlet C, Tremblay-Franco M, Gautier R, Molina J, Métais B, Estrada F, Gamet-Payrastre L. 2013. Specific metabolic fingerprint of a dietary exposure to a very low dose of endosulfan. J. Toxicol. 2013:1.
  • Carnero A, Blanco-Aparicio C, Kondoh H, Lleonart ME, Martinez-Leal JF, Mondello C, Scovassi AI, Bisson WH, Amedei A, Roy R, et al. 2015. Disruptive chemicals, senescence and immortality. Carcinogenesis. 36(Suppl 1):S19–S37.
  • Carreño J, Rivas A, Granada A, Lopez-Espinosa J, Mariscal M, Olea N, Olea-Serrano F. 2007. Exposure of young men to organochlorine pesticides in Southern Spain. Environ Res. 103(1):55–61.
  • Dalvie M, Africa A, Solomons A, London L, Brouwer D, Kromhout H. 2009. Pesticide exposure and blood endosulfan levels after first season spray amongst farm workers in the Western Cape, South Africa. J Environ Sci Health. 44(3):271–277.
  • Dar S, Das S, Ramachandran V, Bhattacharya S, Mustafa M, Banerjee B, Verma P. 2012. Alterations in T-lymphocyte subset profiles/cytokine secretion by PBMC of systemic lupus erythematosus patients upon in vitro exposure to organochlorine pesticides. J Immunotoxicol. 9(1):85–95.
  • Desalegn B, Takasuga T, Harada K, Hitomi T, Fujii Y, Yang H, Wang P, Senevirathna S, Koizumi A. 2011. Historical trends in human dietary intakes of endosulfan and toxaphene in China, Korea and Japan. Chemosphere. 83(10):1398–1405.
  • Dionisio L, José De Rosa M, Bouzat C, Esandi M. 2011. An intrinsic GABAergic system in human lymphocytes. Neuropharmacology. 60(2–3):513–519.
  • El-Shenawy N. 2010. Effects of insecticides fenitrothion, endosulfan and abamectin on anti-oxidant parameters of isolated rat hepatocytes. Toxicol in Vitro. 24(4):1148–1157.
  • Enhui Z, Na C, Meng L, Jia L, Dan L, Yongsheng Y, Ying Z, Fu H. 2016. Isomers and their metabolites of endosulfan induced cytotoxicity and oxidative damage in SH‐SY5Y cells. Environ Toxicol. 31(4):496–504.
  • Freund A, Patil C, Campisi J. 2011. P38MAPK is a novel DNA damage response-independent regulator of the senescence-associated secretory phenotype. EMBO J. 30(8):1536–1548.
  • Fukada T, Hibi M, Yamanaka Y, Takahashi-Tezuka M, Fujitani Y, Yamaguchi T, Nakajima K, Hirano T. 1996. Two signals are necessary for cell proliferation induced by a cytokine receptor gp130: Involvement of STAT3 in anti-apoptosis. Immunity. 5(5):449–460.
  • Ghosh K, Chatterjee B, Geetha J, Kanade S. 2018. The persistent organochlorine pesticide endo-sulfan modulates multiple epigenetic regulators with oncogenic potential in MCF-7 cells. Sci Total Environ. 624:1612–1622.
  • Guo F, Zhang L, Wei J, Li Y, Shi Z, Yang Y, Zhou X, Sun Z. 2015. Endosulfan induced the arrest of the cell cycle through inhibiting the signal pathway mediated by PKCα and damaging the cytoskeleton in spermatogonial cells of mice in vitro. Toxicol Res. 4(2):508–518.
  • Han EH, Hwang YP, Kim HG, Jeong HG. 2007. Inflammatory effect of endosulfan via NF-κB activation in macrophages. Biochem Bioph Res Co 355:860–865.
  • Integrated Risk Information System (IRIS) Chemical, and Agency, U.S.E.P.A. 1994. Endosulfan (CASRN 115-29-7). USA. Retrieved from https://cfpub.epa.gov/ncea/iris/iris_documents/documents/subst/0235_summary.pdf#nameddest=rfd.
  • Kannan K, Holcombe R, Jain S, Alvarez-Hernandez X, Chervenak R, Wolf R, Glass J. 2000. Evidence for the induction of apoptosis by endosulfan in a human T-cell leukemic line. Mol Cell Biochem. 205(1–2):53–66.
  • Kim H, Kim Y, Park J, Khanal T, Choi J, Do M, Jin S, Han E, Chung Y, Jeong H. 2015. Endosulfan induces COX-2 expression via NADPH oxidase and the ROS, MAPK, and Akt pathways. Arch Toxicol. 89(11):2039–2050.
  • Kłuciński P, Hrycek A, Stasiura-Zielińska H, Kossmann S, Tustanowski J, Friedek D, Kamińska-Kołodziej B. 1996. Humoral and cellular immunity rates in chemical plant workers employed in the production of liquid pesticides. Intl J Occup Med Environ Health. 9:103–110.
  • Lecot P, Alimirah F, Desprez P, Campisi J, Wiley C. 2016. Context-dependent effects of cellular senescence in cancer development. Br J Cancer. 114(11):1180–1184.
  • Lemaire G, Mnif W, Mauvais P, Balaguer P, Rahmani R. 2006. Activation of α- and β-estrogen receptors by persistent pesticides in reporter cell lines. Life Sci. 79(12):1160–1169.
  • Li J, McMurray R. 2009. Effects of chronic exposure to DDT and TCDD on disease activity in murine systemic lupus erythematosus. Lupus. 18(11):941–949.
  • Lin M, Juan C, Chang K, Chen W, Kuo M. 2001. IL-6 inhibits apoptosis and retains oxidative DNA lesions in human gastric cancer AGS cells through up-regulation of anti-apoptotic gene mcl-1. Carcinogenesis. 22(12):1947–1953.
  • Lu Y, Morimoto K, Takeshita T, Takeuchi T, Saito T. 2000. Genotoxic effects of alpha-endosulfan and beta-endosulfan on human HepG2 cells. Environ Health Perspect. 108(6):559–561.
  • Martínez-Valenzuela C, Gómez-Arroyo S, Villalobos-Pietrini R, Waliszewski S, Calderón-Segura M, Félix-Gastélum R, Álvarez-Torres A. 2009. Genotoxic biomonitoring of agricultural workers exposed to pesticides in north of Sinaloa State. Mexico Environ Intl. 35(8):1155–1159.
  • Menezes R, Qadir T, Moin A, Fatima H, Hussain S, Madadin M, Pasha S, Al Rubaish F, Senthilkumaran S. 2017. Endosulfan poisoning: An overview. J Forensic Leg Med. 51:27–33.
  • Mrema E, Rubino F, Brambilla G, Moretto A, Tsatsakis A, Colosio C. 2013. Persistent organochlorinated pesticides and mechanisms of their toxicity. Toxicology. 307:74–88.
  • Oh H, Ghosh S. 2013. NF-κB: Roles and regulation in different CD4+ T-cell subsets. Immunol Rev. 252(1):41–51.
  • Pi N, Eng S, Nam C, Kelly B. 2016. Associations of serum organo-halogen levels and prostate cancer risk: Results from a case control study in Singapore. Chemosphere. 144:1505–1512.
  • Pratap U, Sharma H, Mohanty A, Kale P, Gopinath S, Hima L, Priyanka H, Thyaga Rajan S. 2015. Estrogen up-regulates inflammatory signals through NF-κB, IFNγ, and nitric oxide via Akt/mTOR pathway in lymph node lymphocytes of middle-aged female rats. Intl. Immunopharmacol. 29(2):591–598.
  • Rau A, Coutinho A, Avabratha K, Rau A, Warrier R. 2012. Pesticide (endosulfan) levels in the bone marrow of children with hematological malignancies. Indian Pediatr. 49(2):113–117.
  • Reed A, Dzon L, Loganathan B, Whalen M. 2004. Immunomodulation of human natural killer cell cytotoxic function by organochlorine pesticides. Hum Exp Toxicol. 23(10):463–471.
  • Schaalan M, Abdelraouf S, Mohamed W, Hassanein F. 2012. Correlation between maternal milk and infant serum levels of chlorinated pesticides (CP) and the impact of elevated CP on bleeding tendency and immune status in some infants in Egypt. J Immunotoxicol. 9(1):15–24.
  • Shah H, Bhat M, Sharma T, Banerjee B, Guleria K. 2018. Delineating potential transcriptomic association with organochlorine pesticides in the etiology of epithelial ovarian cancer. Open Biochem J. 12:16–28.
  • Silva M, Carr W. 2010. Human health risk assessment of endosulfan. II. Dietary exposure assessment. Regul Toxicol Pharm. 56(1):18–27.
  • Stockholm Convention on Persistent Organic Pollutants. United Nations Environmental Program (UNEP). 2009. Draft risk profile: Endosulfan Stockholm Convention on Persistent Organic Pollutants. Geneva. http://chm.pops.int/Default.aspx?tabid=592%0A
  • Stockholm Convention on Persistent Organic Pollutants. POPs Review Committee (POPRC). 2017. The 16 New POPs. Geneva, Switzerland. http://www.pops.int/TheConvention/ThePOPs/TheNewPOPs/tabid/2511/Default.aspx
  • Svensson B-G, Hallberg T, Nilsson A, SchüTz A, Hagmar L. 1994. Parameters of immunological competence in subjects with high consumption of fish contaminated with persistent organochlorine compounds. Int Arch Occup Environ Health. 65(6):351–358.
  • Téllez-Bañuelos M, Haramati J, Franco-Topete K, Peregrina-Sandoval J, Franco-Topete R, Zaitseva G. 2016. Chronic exposure to endosulfan induces inflammation in murine colon via β-catenin expression and IL-6 production . J Immunotoxicol. 13(6):842–849.
  • Tellez-Bañuelos M, Ortiz-Lazareno P, Santerre A, Casas-Solis J, Bravo-Cuellar A, Zaitseva G. 2011. Effects of low concentration of endosulfan on proliferation, ERK1/2 pathway, apoptosis and senescence in Nile tilapia (Oreochromis niloticus) splenocytes. Fish Shellfish Immunol. 31(6):1291–1296.
  • Tellez-Bañuelos M, Santerre A, Casas-Solis J, Bravo-Cuellar A, Zaitseva G. 2009. Oxidative stress in macrophages from spleen of Nile tilapia (Oreochromis niloticus) exposed to sublethal concentration of endosulfan. Fish Shellfish Immunol. 27(2):105–111.
  • Terry A, Benitez-Kruidenier S, DeKrey G. 2018. Effects of endosulfan isomers on cytokine and nitric oxide production by differentially activated RAW 264.7 cells. Toxicol Rep. 5:396–400.
  • Tian J, Lu Y, Zhang H, Chau C, Dang H, Kaufman D. 2004. γ-Aminobutyric acid inhibits T-cell autoimmunity and development of inflammatory responses in a mouse Type 1 diabetes model. J Immunol. 173(8):5298–5304.
  • Vaux D. 2011. Apoptogenic factors released from mitochondria. Biochim Biophys Acta. 1813(4):546–550.
  • Vine M, Stein L, Weigle K, Schroeder J, Degnan D, Tse C, Hanchette C, Backer L. 2000. Effects on immune system associated with living near a pesticide dump site. Environ Health Perspect. 108(12):1113–1124.
  • Wade M, Foster W, Younglai E, McMahon A, Leingartner K, Yagminas A, Blakey D, Fournier M, Desaulniers D, Hughes C. 2002. Effects of subchronic exposure to a complex mixture of persistent contaminants in male rats: Systemic, immune, and reproductive effects. Toxicol Sci. 67(1):131–143.
  • Wong F, Alegria H, Bidleman T. 2010. Organochlorine pesticides in soils of Mexico and the potential for soil-air exchange. Environ Pollut. 158(3):749–755.
  • Wurster A, Rodgers V, White M, Rothstein T, Grusby M. 2002. Interleukin-4-mediated protection of primary B-cells from apoptosis through Stat6-dependent up-regulation of Bcl-xL . J Biol Chem. 277(30):27169–27175.
  • Xu D, Liang D, Guo Y, Sun Y. 2018. Endosulfan causes the alterations of DNA damage response through ATM-p53 signaling pathway in human leukemia cells . Environ Pollut. 238:1048–1055.
  • Xu W, Larbi A. 2017. Markers of T-cell senescence in humans. Intl J Mol Sci. 18:1–13.
  • Yang J, Wang Z, Ma L, Shen X, Sun Y, Hu D, Sun L. 2015. The organochlorine pesticides residues in the invasive ductal breast cancer patients. Environ Toxicol Pharmacol. 40(3):698–703.
  • Zhang L, Wei J, Ren L, Zhang J, Yang M, Jing L, Wang J, Sun Z, Zhou X. 2017. Endosulfan inducing apoptosis and necroptosis through activation RIPK signaling pathway in human umbilical vascular endothelial cells. Environ Sci Pollut Res. 24(1):215–225.