Chlorpyrifos exposure reduces reproductive capacity owing to a damaging effect on gametogenesis in the nematode Caenorhabditis elegans

Journal of Applied Toxicology

Volumn 32, Issue 7, 2012, Pages 527-535

  Ruan, Qin Li ^a   Ju, Jing Juan ^a   Li, Yun Hui ^a   Li, Xiao Bo ^a   Liu, Ran ^a   Liang, Ge Yu ^a   Zhang, Juan ^a   Pu, Yue Pu ^a   Wang, Da Yong ^b   Yin, Li Hong ^a  

^a SOUTHEAST UNIVERSITY   (China)

^b MEDICAL SCHOOL OF SOUTHEAST UNIVERSITY   (China)

Author keywords

Caenorhabditis elegans; Chlorpyrifos; Oogenesis; Reproductive capacity; Spermatogenesis

Indexed keywords

CHLORPYRIFOS;

APOPTOSIS; ARTICLE; CAENORHABDITIS ELEGANS; CED 3 GENE; CED 4 GENE; CED 9 GENE; CELL ACTIVATION; CELL FUNCTION; CELL STRUCTURE; CONTROLLED STUDY; CYB 3 GENE; FER 1 GENE; FERTILITY; GAMETOGENESIS; GENE; GENE EXPRESSION; GLP 1 GENE; LARVA; MLH 1 GENE; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; PRG 1 GENE; PRIORITY JOURNAL; REPRODUCTIVE TOXICITY; SPE 10 GENE; SPE 15 GENE; SPERMATID; SPERMATOGENESIS; SPERMATOZOON MOTILITY;

ANIMALS; APOPTOSIS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHLORPYRIFOS; ENVIRONMENTAL EXPOSURE; FEMALE; FERTILIZATION; GAMETOGENESIS; GENE EXPRESSION REGULATION; GENES, HELMINTH; MALE; OOCYTES; OOGENESIS; REPRODUCTION; SPERMATIDS; SPERMATOGENESIS;

CAENORHABDITIS ELEGANS; NEMATODA; RODENTIA;

EID: 84860229943     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.1783     Document Type: Article

References (46)

1. Achanzar WE, Ward S. 1997. A nematode gene required for sperm vesicle fusion. J. Cell Sci. 110: 1073-1081.
2. Anderson GL, Boyd WA, Williams PL. 2001. Assessment of sublethal endpoints for toxicity testing with the nematode Caenorhabditis elegans. Environ. Toxicol. Chem. 20: 833-838.
3. Booth LH, O'Halloran K. 2001. A comparison of biomarker responses in the earthworm Aporrectodea caliginosa to the organophosphorus insecticides diazinon and chlorpyrifos. Environ. Toxicol. Chem. 20: 2494-2502.
4. Brenner S. 1974. Genetics of Caenorhabditis elegans. Genetics 77: 71-94.
5. Dhawan R, Dusenbery DB, Williams PL. 1999. Comparison of lethality, reproduction, and behavior as toxicological endpoints in the nematode Caenorhabditis elegans. J. Toxicol. Environ. Health A 58: 451-462.
6. Donkin SG, Williams PL. 1995. Influence of developmental stage, salts and food presence on various endpoints using Caenorhabditis elegans for aquatic toxicity testing. Environ. Toxicol. Chem. 14: 2139-2147.
7. Emmons SW. 2005. Male Development. The C. elegans Research Community, WormBook; doi/10.1895/wormbook.1.33.1; available at:.
8. Farag AT, Radwan AH, Sorour F, El-Okazy A, El-Agamy E, El-Sebae AE. 2010. Chlorpyrifos induced reproductive toxicity in male mice. Reprod. Toxicol. 29: 80-85.
9. Fraire-Zamora JJ, Cardullo RA. 2010. The physiological acquisition of amoeboid motility in nematode sperm: is the tail the only thing the sperm lost. Mol. Reprod. Dev. 77: 739-750.
10. Gilliom RJ. 2007. Pesticides in U.S. streams and groundwater. Environ. Sci. Technol. 41: 3408-3414.
11. Gleason EJ, Lindsey WC, Kroft TL, Singson AW, L'Hernault SW. 2006. spe-10 encodes a DHHC-CRD zinc-finger membrane protein required for endoplasmic reticulum/Golgi membrane morphogenesis during Caenorhabditis elegans spermatogenesis. Genetics 172: 145-158.
12. Gumienny TL, Lambie E, Hartwieg E, Horvitz HR, Hengartner MO. 1999. Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126: 1011-1022.
13. Guo YL, Yang YC, Wang DY. 2009. Induction of reproductive deficits in nematode Caenorhabditis elegans exposed to metals at different developmental stages. Reprod. Toxicol. 28: 90-95.
14. Gupta SC, Siddique HR, Mathur N, Mishra RK, Saxena DK, Chowdhuri DK. 2007. Adverse effect of organophosphate compounds, dichlorvos and chlorpyrifos in the reproductive tissues of transgenic Drosophila melanogaster: 70kDa heat shock protein as a marker of cellular damage. Toxicology 238: 1-14.
15. Hodgkin J. 2002. Exploring the envelope: systematic alteration in the sex-determination system of the nematode Caenorhabditis elegans. Genetics 162: 767-780.
16. Hope I. 1999. C. elegans: a practical approach. In Conventional Genetics, Hodgkin J (ed). Oxford University Press: Oxford; 245-271.
17. Jager T, Crommentuijn T, Van-Gestel CAM, Kooijman S. 2007. Chronic exposure to chlorpyrifos reveals two modes of action in the springtail Folsomia candida. Environ. Pollut. 145: 452-458.
18. Joshi SC, Mathur R, Gulati N. 2007. Testicular toxicity of chlorpyrifos (an organophosphate pesticide) in albino rat. Toxicol. Ind. Health 23: 439-444.
19. Kelleher JF, Mandell MA, Moulder G, Hill KL, L'Hernault SW, Barstead R, Titus MA. 2000. Myosin VI is required for asymmetric segregation of cellular components during C. elegans spermatogenesis. Cur. Biol. 10: 1489-1496.
20. Kimble J, Crittenden SL. 2005. Germline Proliferation and its Control. The C. elegans Research Community, WormBook; doi/10.1895/wormbook.1.13.1; available at:.
21. Klass M, Wolf N, Hirsh D. 1976. Development of the male reproductive system and sexual transformation in the nematode Caenorhabditis elegans. Dev. Biol. 52: 1-18.
22. Kokel D, Li Y, Qin J, Xue D. 2006. The nongenotoxic carcinogens naphthalene and para-dichlorobenzene suppress apoptosis in Caenorhabditis elegans. Nat. Chem. Biol. 2: 338-345.
23. LaMunyon CW, Ward S. 1998. Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proc. R. Soc. Lond. B. 265: 1997-2002.
24. Leung MCK, Williams PL, Benedetto A, Au C, Helmcke KJ, Aschner M, Meyer JN. 2008. Caenorhabditis elegans: an emerging model in biomedical and environmental toxicology. Toxicol. Sci. 106: 5-28.
25. L'Hernault SW. 2009. The genetics and cell biology of spermatogenesis in the nematode C. elegans. Mol. Cell. Endocrinol. 306: 59-65.
26. L'Hernault SW, Roberts TM. 1995. Cell Biology of Nematode Sperm, Epstein HF (ed.). Methods in Cell Biology. Academic Press: London; 284.
27. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using Real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25: 402-408.
28. Luo S, Kleemann GA, Shaw WM, Murphy CT. 2010. TGF-beta and insulin signaling regulate reproductive aging via oocyte and germline quality maintenance. Cell 143: 299-312.
29. Markovic M, Cupac S, Durovic R, Milinovic J, Kljajic P. 2010. Assessment of heavy metal and pesticide levels in soil and plant products from agricultural area of Belgrade, Serbia. Arch. Environ. Contam. Toxicol. 58: 341-351.
30. Nadarajan S, Govindan JA, Mc-Govern M, Hubbard EJA, Greenstein D. 2009. MSP and GLP-1/Notch signaling coordinately regulate actomyosin-dependent cytoplasmic streaming and oocyte growth in C. elegans. Development 135: 2223-2234.
31. Nelson GA, Ward S. 1980. Vesicle fusion, pseudopod extension and amoeboid motility are induced in nematode spermatids by the ionophore monensin. Cell 19: 457-464.
32. Pothof J, Van-Haaften G, Thijssen K, Kamath RS, Fraser AG, Ahringer J, Plasterk RH, Tijsterman M. 2003. Identification of genes that protect the C. elegans genome against mutations by genome-wide RNAi. Genes Dev. 17: 443-448.
33. Roberts TM, Ward S. 1982. Centripetal flow of pseudopodial surface components could propel the ameboid movement of Caenorhabditis elegans spermatozoa. J. Cell Biol. 92: 132-138.
34. Roh JY, Choi J. 2008. Ecotoxicological evaluation of chlorpyrifos exposure on the nematode Caenorhabditis elegans. Ecotoxicol. Environ. Saf. 71: 483-489.
35. Ruan QL, Ju JJ, Li YH, Liu R, Pu YP, Yin LH, Wang DY. 2009. Evaluation of pesticide toxicities with differing mechanisms using Caenorhabditis elegans. J. Toxicol. Environ. Health A 72: 746-751.
36. Shakes DC, Ward S. 1989a. Mutations that disrupt the morphogenesis and localization of a sperm-specific organelle in Caenorhabditis elegans. Dev. Biol. 134: 307-316.
37. Shakes DC, Ward S.1989b. Initiation of spermiogenesis in C. elegans: a pharmacological and genetic analysis. Dev. Biol. 134: 189-200.
38. Swain SC, Keusekotten K, Baumeister R, Sturzenbaum SR. 2004. C. elegans metallothioneins: new insights into the phenotypic effects of cadmium toxicosis. J. Mol. Biol. 341: 951-959.
39. Wang DY, Shen LL, Wang Y. 2007. The phenotypic and behavioral defects can be transferred from zinc-exposed nematodes to their progeny. Environ. Toxicol. Pharmacol. 24: 223-230.
40. Wang G, Reinke V. 2008. A C. elegans Piwi, PRG-1, regulates 21U-RNAs during spermatogenesis. Cur. Biol. 18: 861-867.
41. Ward S, Argon Y, Nelson GA. 1981. Sperm morphogenesis in wild-type and fertilization-defective mutants of Caenorhabditis elegans. J. Cell Biol. 91: 26-44.
42. Ward S, Hogan E, Nelson GA. 1983. The initiation of spermiogenesis in the nematode Caenorhabditis elegans. Dev. Biol. 98: 70-79.
43. Williams PL, Dusenbery DB. 1990. Aquatic toxicity testing using the nematode, Caenorhabditis elegans. Environ. Toxicol. Chem. 9: 1285-1290.
44. Wolke U, Jezuit EA, Priess JR. 2007. Actin-dependent cytoplasmic streaming in C. elegans oogenesis. Development 134: 2227-2236.
45. Xu H, Vanden HS, Lorson MA, Bennett KL. 2000. The cyclin B and B3 genes have distinct functions during cell division in C. elegans. East Coast Worm Meeting.
46. Zhou Z, Hartwieg E, Horvitz HR. 2001. CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 104: 43-56.