Chlorpyrifos induces NLRP3 inflammasome and pyroptosis/apoptosis via mitochondrial oxidative stress in human keratinocyte HaCaT cells

Toxicology

Volumn 338, Issue , 2015, Pages 37-46

  Jang, Yoonjeong ^a   Lee, Ah Young ^a   Jeong, Sang Hee ^b   Park, Kyung Hun ^c   Paik, Min Kyoung ^c   Cho, Nam Joon ^c   Kim, Ji Eun ^a   Cho, Myung Haing ^a,d  

^a Seoul National University   (South Korea)

^b Hoseo University   (South Korea)

^c National Institute of Animal Science   (South Korea)

^d Seoul National University   (South Korea)

Author keywords

Chlorpyrifos; Inflammasome; Mitochondrial oxidative stress; Pyroptosis; Skin inflammation

Indexed keywords

CHLORPYRIFOS; CRYOPYRIN; INFLAMMASOME; REACTIVE OXYGEN METABOLITE; CARRIER PROTEIN; CASPASE INHIBITOR; NLRP3 PROTEIN, HUMAN; PESTICIDE; SCAVENGER;

APOPTOSIS; ARTICLE; CELL LINE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; EPITHELIUM CELL; HUMAN; HUMAN CELL; INFLAMMATION; INNATE IMMUNITY; KERATINOCYTE; MITOCHONDRIAL MEMBRANE POTENTIAL; OXIDATIVE STRESS; PRIORITY JOURNAL; SKIN EPITHELIUM; SKIN TOXICITY; CELL SURVIVAL; DERMATITIS, CONTACT; DOSE RESPONSE; DRUG EFFECTS; IMMUNOLOGY; METABOLISM; MITOCHONDRION; PYROPTOSIS; RISK ASSESSMENT; SIGNAL TRANSDUCTION;

CARRIER PROTEINS; CASPASE INHIBITORS; CELL LINE; CELL SURVIVAL; CHLORPYRIFOS; DERMATITIS, CONTACT; DOSE-RESPONSE RELATIONSHIP, DRUG; FREE RADICAL SCAVENGERS; HUMANS; IMMUNITY, INNATE; INFLAMMASOMES; KERATINOCYTES; MITOCHONDRIA; OXIDATIVE STRESS; PESTICIDES; PYROPTOSIS; REACTIVE OXYGEN SPECIES; RISK ASSESSMENT; SIGNAL TRANSDUCTION;

EID: 84945244832     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2015.09.006     Document Type: Article

References (52)

1. Abhishek A., Ansari N.G., Shankhwar S.N., Jain A., Singh V. In vitro toxicity evaluation of low doses of pesticides in individual and mixed condition on human keratinocyte cell line. Bioinformation 2014, 10(12):716-720.
2. Arend W.P., Palmer G., Gabay C. IL1, IL18, and IL33 families of cytokines. Immunol. Rev. 2008, 223:20-38.
3. ArystaLifeScience MSDS of Chlorpyrifos 2010, 1-6. ARYSTA LifeScience South Africa (Pty) Ltd.
4. Bergsbaken T., Cookson B.T. Macrophage activation redirects yersinia-infected host cell death from apoptosis to caspase-1-dependent pyroptosis. PLoS Pathog. 2007, 3(11):e161.
5. Caicedo M.S., Desai R., McAllister K., Reddy A., Jacobs J.J., Hallab N.J. Soluble and particulate Co-Cr-Mo alloy implant metals activate the inflammasome danger signaling pathway in human macrophages: a novel mechanism for implant debris reactivity. J. Orthop. Res. 2009, 27(7):847-854.
6. Campochiaro P.A., Strauss R.W., Lu L., Hafiz G., Wolfson Y., Shah S.M., Sophie R., Mir T.A., Scholl H.P. Is there excess oxidative stress and damage in eyes of patients with retinitis pigmentosa?. Antioxid. Redox Signaling 2015, 23(7):643-648.
7. Castedo M., Ferri K., Roumier T., Métivier D., Zamzami N., Kroemer G. Quantitation of mitochondrial alterations associated with apoptosis. J. Immunol. Methods 2002, 265(1-2):39-47.
8. Chung Y.M., Kim J.S., Do Yoo Y. A novel protein, Romo1, induces ROS production in the mitochondria. Biochem. Biophys. Res. Commun. 2006, 347(3):649-655.
9. Chung S.D., Lai T.Y., Chien C.T., Yu H.J. Activating Nrf-2 signaling depresses unilateral ureteral obstruction-evoked mitochondrial stress-related autophagy, apoptosis and pyroptosis in kidney. PLoS One 2012, 7(10):e47299.
10. Contassot E., Beer H.-D., French L.E. Interleukin-1, inflammasomes, autoinflammation and the skin. Swiss Med. Wkly. 2012, 142:w13590.
11. Crumpton T., Seidler F., Slotkin T. Is oxidative stress involved in the developmental neurotoxicity of chlorpyrifos?. Dev. Brain Res. 2000, 121(2):189-195.
12. Dinnen R.D., Mao Y., Fine R.L. The use of fluorescent probes in the study of reactive oxygen species in pancreatic cancer cells. Pancreatic Cancer 2013, 321-329. Springer.
13. Ermak G., Davies K.J. Calcium and oxidative stress: from cell signaling to cell death. Mol. Immunol. 2002, 38(10):713-721.
14. Fleury C., Mignotte B., Vayssière J.-L. Mitochondrial reactive oxygen species in cell death signaling. Biochimie. 2002, 84(2-3):131-141.
15. Gavrieli Y., Sherman Y., Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 1992, 119(3):493-501.
16. Giordano G., Afsharinejad Z., Guizzetti M., Vitalone A., Kavanagh T.J., Costa L.G. Organophosphorus insecticides chlorpyrifos and diazinon and oxidative stress in neuronal cells in a genetic model of glutathione deficiency. Toxicol. Appl. Pharmacol. 2007, 219(2-3):181-189.
17. Gomez L.E. Use and Benefits of Chlorpyrifos in U.S. Agriculture 2009, 1-113. Dow AgroSciences LLC, USA.
18. Green D.R., Galluzzi L., Kroemer G. Mitochondria and the autophagy - inflammation - cell death axis in organismal aging. Science 2011, 333(6046):1109-1112.
19. Gross O., Thomas C.J., Guarda G., Tschopp J. The inflammasome: an integrated view. Immunol. Rev. 2011, 243(1):136-151.
20. Jabaut J., Ather J.L., Taracanova A., Poynter M.E., Ckless K. Mitochondria-targeted drugs enhance Nlrp3 inflammasome-dependent IL-1β secretion in association with alterations in cellular redox and energy status. Free Radical Biol. Med. 2013, 60:233-245.
21. Kasahara E., Sekiyama A., Hori M., Hara K., Takahashi N., Konishi M., Sato E.F., Matsumoto S., Okamura H., Inoue M. Mitochondrial density contributes to the immune response of macrophages to lipopolysaccharide via the MAPK pathway. FEBS Lett. 2011, 585(14):2263-2268.
22. Kepp O., Galluzzi L., Kroemer G. Mitochondrial control of the NLRP3 inflammasome. Nat. Immunol. 2011, 12:199-200.
23. Koybasi S., Senkal C.E., Sundararaj K., Spassieva S., Bielawski J., Osta W., Day T.A., Jiang J.C., Jazwinski S.M., Hannun Y.A. Defects in cell growth regulation by C18: 0-ceramide and longevity assurance gene 1 in human head and neck squamous cell carcinomas. J. Biol. Chem. 2004, 279(43):44311-44319.
24. Kupper T.S., Fuhlbrigge R.C. Immune surveillance in the skin: mechanisms and clinical consequences. Nat. Rev. Immunol. 2004, 4:211-222.
25. Kyrylkova K., Kyryachenko S., Leid M., Kioussi C. Detection of apoptosis by TUNEL assay. Odontogenesis 2012, 41-47. Springer.
26. López-Armada M.J., Riveiro-Naveira R.R., Vaamonde-García C., Valcárcel-Ares M.N. Mitochondrial dysfunction and the inflammatory response. Mitochondrion 2013, 13(2):106-118.
27. Lamkanfi M., Dixit V.M. Inflammasomes and their roles in health and disease. Annu. Rev. Cell Dev. Biol. 2012, 28:137-161.
28. Lamkanfi M., Dixit V.M. Mechanisms and functions of inflammasomes. Cell 2014, 157(5):1013-1022.
29. Lee J.E., Park J.H., Shin I.C., Koh H.C. Reactive oxygen species regulated mitochondria-mediated apoptosis in PC12 cells exposed to chlorpyrifos. Toxicol. Appl. Pharmacol. 2012, 263(2):148-162.
30. Liang H.L., Sedlic F., Bosnjak Z., Nilakantan V. SOD1 and MitoTEMPO partially prevent mitochondrial permeability transition pore opening, necrosis, and mitochondrial apoptosis after ATP depletion recovery. Free Radical Biol. Med. 2010, 49(10):1550-1560.
31. Liu M., Liu H., Dudley S.C. Reactive oxygen species originating from mitochondria regulate the cardiac sodium channel. Circ. Res. 2010, 107(8):967-974.
32. Martinon F., Tschopp J. Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 2004, 117(5):561-574.
33. Medzhitov R., Janeway C.A. Decoding the patterns of self and nonself by the innate immune system. Science 2002, 296:298-300.
34. Miao E.A., Rajan J.V., Aderem A. Caspase-1-induced pyroptotic cell death. Immunol. Rev. 2011, 243(1):206-214.
35. Muniz J.F., McCauley L., Scherer J., Lasarev M., Koshy M., Kow Y., Nazar-Stewart V., Kisby G. Biomarkers of oxidative stress and DNA damage in agricultural workers: a pilot study. Toxicol. Appl. Pharmacol. 2008, 227(1):97-107.
36. Ott M., Gogvadze V., Orrenius S., Zhivotovsky B. Mitochondria, oxidative stress and cell death. Apoptosis 2007, 12:913-922.
37. Penagos H., Ruepert C., Partanen T., Wesseling C. Pesticide patch test series for the assessment of allergic contact dermatitis among banana plantation workers in panama. Dermatitis 2004, 15(3):137-145. ISSN:1710-3568.
38. Reuter S., Gupta S.C., Chaturvedi M.M., Aggarwal B.B. Oxidative stress, inflammation, and cancer: how are they linked?. Free Radical Biol. Med. 2010, 49(11):1603-1616.
39. Sagulenko V., Thygesen S., Sester D., Idris A., Cridland J., Vajjhala P., Roberts T., Schroder K., Vince J., Hill J. AIM2 and NLRP3 inflammasomes activate both apoptotic and pyroptotic death pathways via ASC. Cell Death Differ. 2013, 20(9):1149-1160.
40. Saulsbury M.D., Heyliger S.O., Wang K., Johnson D.J. Chlorpyrifos induces oxidative stress in oligodendrocyte progenitor cells. Toxicology 2009, 259(1-2):1-9.
41. Sharpe R.M., Irvine D.S. How strong is the evidence of a link between environmental chemicals and adverse effects on human reproductive health?. BMJ: Br. Med. J. 2004, 328(7437):447.
42. Simon H.-U., Haj-Yehia A., Levi-Schaffer F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 2000, 5:415-418.
43. Tait S.W., Ichim G., Green D.R. Die another way-non-apoptotic mechanisms of cell death. J. Cell Sci. 2014, 127:2135-2144.
44. Verma R.S., Mehta A., Srivastava N. In vivo chlorpyrifos induced oxidative stress: attenuation by antioxidant vitamins. Pestic. Biochem. Physiol. 2007, 88(2):191-196.
45. Wang J., Jian X., Kan B., Song C. 2 cases of chlorpyrifos induced medicamentosa-like dermatitis. Zhonghua lao dong wei sheng zhi ye bing za zhi 2014, 32(5):384-385.
46. Watanabe H., Gaide O., Pétrilli V., Martinon F., Contassot E., Roques S., Kummer J.A., Tschopp J., French L.E. Activation of the IL-1β-processing inflammasome is involved in contact hypersensitivity. J. Invest. Dermatol. 2007, 127(8):1956-1963.
47. Waypa G.B., Marks J.D., Mack M.M., Boriboun C., Mungai P.T., Schumacker P.T. Mitochondrial reactive oxygen species trigger calcium increases during hypoxia in pulmonary arterial myocytes. Circ. Res. 2002, 91(8):719-726.
48. Wellington M., Koselny K., Sutterwala F.S., Krysan D.J. Candida albicans triggers NLRP3-mediated pyroptosis in macrophages. Eukaryot. Cell 2014, 13(2):329-340.
49. West A.P., Shadel G.S., Ghosh S. Mitochondria in innate immune responses. Nat. Rev. Immunol. 2011, 11:389-402.
50. Yu F., Wang Z., Ju B., Wang Y., Wang J., Bai D. Apoptotic effect of organophosphorus insecticide chlorpyrifos on mouse retina in vivo via oxidative stress and protection of combination of vitamins C and E. Exp. Toxicol. Pathol. 2008, 59(6):415-423.
51. Zhou R., Yazdi A.S., Menu P., Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011, 469:221-225.
52. Zou H., Li Y., Liu X., Wang X. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem. 1999, 274:11549-11556.