Abstract
As a persistent organic pollutant, perfluorooctane sulfonate (PFOS) and perfluorooctanoic acid (PFOA) have gained increasing research attention over recent years because of their potential risk to humans and the environment. In this paper, we investigated the reproductive toxicity of these pollutants using a C. elegans model to evaluate spermatogenesis throughout the entire developmental cycle of him-5 mutant by exposing to 0.001, 0.01, and 0.1 mmol/L PFOS or PFOA for 48 h. Experimental results suggested that PFOS and PFOA exposure led to reductions in brood size, germ cell number, spermatid size, and motility, and increases in rate of malformation spermatids. Analysis of variance (ANOVA) showed that exposure to PFOS resulted in higher levels of damage than PFOA in germ cells only in 0.001 mmol/L exposure group. RT-qPCR was used to further investigate the expression of genes associated with different stages of spermatogenesis, such as mitosis and meiosis, fibrous body-membranous organelles (FB-MOs), and sperm activation. The expression levels of wee-1.3, spe-4, spe-6, and spe-17 genes were increased, while those of puf-8, spe-10, fer-1, swm-1, try-5, and spe-15 genes were decreased. Our results suggesting that PFOS or PFOA may cause spermatogenesis damage by disrupting the mitotic proliferation, meiotic entry, formation of the MOs, fusion of the MOs and plasma membrane (PM), and pseudopods. Loss-of-function studies using puf-8 and spe-10 mutants revealed spe-10 gene was specifically involved in PFOS- or PFOA-induced reproductive toxicity via regulating one or more critical palmitoylation events, while puf-8 gene was not direct target of PFOS and PFOA, and PFOS and PFOA may act on the upstream gene of puf-8, thus affecting reproductive ability. Taken together, these results demonstrate the potential adverse impact of PFOS and PFOA exposure on spermatogenesis and provide valuable data for PFC risk assessment.
Similar content being viewed by others
Abbreviations
- PFCs:
-
Perfluorinated compounds
- PFOS:
-
Perfluorooctane sulfonate
- PFOA:
-
Perfluorooctanoic acid
- FB-MOs:
-
Fibrous body-membranous organelles
References
Abbas A et al (2018) Ecotoxicological impacts of surface water and wastewater from conventional and advanced treatment technologies on brood size, larval length, and cytochrome P450 (35A3) expression in Caenorhabditis elegans. Environ Sci Pollut Res Int 25:13868–13880. https://doi.org/10.1007/s11356-018-1605-2
Cui R, Zhang H, Guo X, Cui Q, Wang J, Dai J (2015) Proteomic analysis of cell proliferation in a human hepatic cell line (HL-7702) induced by perfluorooctane sulfonate using iTRAQ. J Hazard Mater 299:361–370
Domingo JL, Ericson-Jogsten I, Perello G, Nadal M, Van Bavel B, Karrman A (2012) Human exposure to perfluorinated compounds in Catalonia, Spain: contribution of drinking water and fish and shellfish. J Agric Food Chem 60:4408–4415
Eggert A, Cisneros-Montalvo S, Anandan S, Musilli S, Stukenborg JB, Adamsson A, Nurmio M, Toppari J (2019) The effects of perfluorooctanoic acid (PFOA) on fetal and adult rat testis. Reprod Toxicol 90:68–76
Ellis RE, Stanfield GM (2014) The regulation of spermatogenesis and sperm function in nematodes. Semin Cell Dev Biol 29:17–30
Fagbayigbo BO, Opeolu BO, Fatoki OS, Olatunji OS (2018) Validation and determination of nine PFCS in surface water and sediment samples using UPLC-QTOF-MS Environmental monitoring and assessment 190
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. https://doi.org/10.1534/genetics.105.047340
Governini L et al (2015) Chromosomal aneuploidies and DNA fragmentation of human spermatozoa from patients exposed to perfluorinated compounds. Andrologia 47:1012–1019
Henry BJ et al (2018) A critical review of the application of polymer of low concern and regulatory criteria to fluoropolymers. Integr Environ Asses 14:316–334
Hunt PR (2017) The C. elegans model in toxicity testing. J Appl Toxicol 37:50–59. https://doi.org/10.1002/jat.3357
Jeong TY, Yuk MS, Jeon J, Kim SD (2016) Multigenerational effect of perfluorooctane sulfonate (PFOS) on the individual fitness and population growth of Daphnia magna. Sci Total Environ 569-570:1553–1560. https://doi.org/10.1016/j.scitotenv.2016.06.249
Joensen UN, Bossi R, Leffers H, Jensen AA, Skakkebaek NE, Jorgensen N (2009) Do perfluoroalkyl compounds impair human semen quality? Environ Health Perspect 117:923–927
Kaletta T, Hengartner MO (2006) Finding function in novel targets: C-elegans as a model organism. Nat Rev Drug Discov 5:387–398
Kato H, Fujii S, Takahashi M, Matsumoto M, Hirata-Koizumi M, Ono A, Hirose A (2015) Repeated dose and reproductive/developmental toxicity of perfluorododecanoic acid in rats. Environ Toxicol 30:1244–1263
L’Hernault SW, Benian GM, Emmons RB (1993) Genetic and molecular characterization of the Caenorhabditis elegans spermatogenesis-defective gene spe-17. Genetics 134:769–780
Lamitina ST, L’Hernault SW (2002) Dominant mutations in the Caenorhabditis elegans Myt1 ortholog wee-1.3 reveal a novel domain that controls M-phase entry during spermatogenesis. Development 129:5009–5018
LaMunyon CW, Ward S (1998) Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. P Roy Soc B-Biol Sci 265:1997–2002
Lesch BJ, Page DC (2012) Genetics of germ cell development. Nat Rev Genet 13:781–794
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
Li YH, Zhang MH, Chen P, Liu R, Liang GY, Yin LH, Pu YP (2015) Effects of microcystin-LR exposure on spermiogenesis in nematode Caenorhabditis elegans. Int J Mol Sci 16:22927–22937
Liau WS, Nasri U, Elmatari D, Rothman J, LaMunyon CW (2013) Premature sperm activation and defective spermatogenesis caused by loss of spe-46 function in Caenorhabditis elegans PloS one 8
Lindim C, van Gils J, Cousins IT (2016) Europe-wide estuarine export and surface water concentrations of PFOS and PFOA Water Research 103:124–132
Liu ZY, Wang B, He RJ, Zhao YM, Miao L (2014) Calcium signaling and the MAPK cascade are required for sperm activation in Caenorhabditis elegans. Bba-Mol Cell Res 1843:299–308
Liu WW et al. (2015) Involvement of NRF2 in Perfluorooctanoic acid-induced testicular damage in male mice Biology of Reproduction 93
Liu ZY et al. (2017) Pollution pathways and release estimation of perfluorooctane sulfonate (PFOS) and perfluorooctanoic acid (PFOA) in central and eastern China Science of the Total Environment 580:1247–1256
Louis GM et al (2015) Perfluorochemicals and human semen quality: the LIFE study. Environ Health Perspect 123:57–63
Maremonti E et al (2019) Gamma radiation induces life stage-dependent reprotoxicity in Caenorhabditis elegans via impairment of spermatogenesis. Sci Total Environ 695:9
Munschy C, Marchand P, Venisseau A, Veyrand B, Zendong Z (2013) Levels and trends of the emerging contaminants HBCDs (hexabromocyclododecanes) and PFCs (perfluorinated compounds) in marine shellfish along French coasts. Chemosphere 91:233–240
Nishimura H, L’Hernault SW (2017a) Spermatogenesis. Curr Biol 27:R988–R994. https://doi.org/10.1016/j.cub.2017.07.067
Nishimura H, L’Hernault SW (2017b) Spermatogenesis. Curr Biol 27:R988–R994
Olsen GW, Burris JM, Ehresman DJ, Froehlich JW, Seacat AM, Butenhoff JL, Zobel LR (2007) Half-life of serum elimination of perfluorooctanesulfonate,perfluorohexanesulfonate, and perfluorooctanoate in retired fluorochemical production workers Environmental health perspectives 115:1298–1305 https://doi.org/10.1289/ehp.10009
Rahman MF, Peldszus S, Anderson WB (2014) Behaviour and fate of perfluoroalkyl and polyfluoroalkyl substances (PFASs) in drinking water treatment: a review. Water Res 50:318–340
Rappazzo KM, Coffman E, Hines EP (2017) Exposure to perfluorinated alkyl substances and health outcomes in children: a systematic review of the epidemiologic literature International journal of environmental research and public health 14
Raymer JH, Michael LC, Studabaker WB, Olsen GW, Sloan CS, Wilcosky T, Walmer DK (2012) Concentrations of perfluorooctane sulfonate (PFOS) and perfluorooctanoate (PFOA) and their associations with human semen quality measurements. Reprod Toxicol 33:419–427. https://doi.org/10.1016/j.reprotox.2011.05.024
Ruan QL et al (2012) Chlorpyrifos exposure reduces reproductive capacity owing to a damaging effect on gametogenesis in the nematode Caenorhabditis elegans. J Appl Toxicol 32:527–535. https://doi.org/10.1002/jat.1783
Shakes DC, Ward S (1989) Initiation of spermiogenesis in C-elegans - a pharmacological and genetic-analysis. Dev Biol 134:189–200
Shinya R, Hasegawa K, Chen A, Kanzaki N, Sternberg PW (2014) Evidence of hermaphroditism and sex ratio distortion in the fungal feeding nematode Bursaphelenchus okinawaensis G3 (Bethesda, Md) 4:1907-1917 doi:https://doi.org/10.1534/g3.114.012385
Singaravelu G, Chatterjee I, Marcello MR, Singson A (2011) Isolation and in vitro activation of Caenorhabditis elegans sperm Jove-J Vis Exp
Smith JR, Stanfield GM (2011) TRY-5 is a sperm-activating protease in Caenorhabditis elegans seminal fluid. PLoS Genet 7:e1002375
Smotrys JE, Linder ME (2004) Palmitoylation of intracellular signaling proteins: regulation and function Annual review of biochemistry 73:559–587 doi:https://doi.org/10.1146/annurev.biochem.73.011303.073954
Song X et al (2018) Biomonitoring PFAAs in blood and semen samples: investigation of a potential link between PFAAs exposure and semen mobility in China. Environ Int 113:50–54. https://doi.org/10.1016/j.envint.2018.01.010
Stanfield GM, Villeneuve AM (2006) Regulation of sperm activation by SWM-1 is required for reproductive success of C-elegans males. Curr Biol 16:252–263
Subramaniam K, Seydoux G (2003) Dedifferentiation of primary spermatocytes into germ cell tumors in C-elegans lacking the pumilio-like protein PUF-8. Curr Biol 13:134–139
Sznajder-Katarzynska K, Surma M, Cieslik E, Wiczkowski W (2018) The perfluoroalkyl substances (PFASs) contamination of fruits and vegetables Food Addit Contam A 35:1776–1786
Toft G et al (2012) Exposure to perfluorinated compounds and human semen quality in arctic and European populations. Hum Reprod 27:2532–2540
Wang T, Wang YW, Liao CY, Cai YQ, Jiang GB (2009) Perspectives on the inclusion of perfluorooctane sulfonate into the Stockholm convention on persistent organic pollutants Environ Sci Technol 43:5171–5175
Wang ZY, Cousins IT, Scheringer M, Hungerbuhler K (2013) Fluorinated alternatives to long-chain perfluoroalkyl carboxylic acids (PFCAs), perfluoroalkane sulfonic acids (PFSAs) and their potential precursors. Environ Int 60:242–248
Wang Q, Zhao Z, Ruan YF, Li J, Sun HW, Zhang G (2018a) Occurrence and distribution of perfluorooctanoic acid (PFOA) and perfluorooctanesulfonic acid (PFOS) in natural forest soils: a nationwide study in China Science of the Total Environment 645:596–602
Wang YX, Zhong YX, Li JG, Zhang JQ, Lyu B, Zhao YF, Wu YN (2018b) Occurrence of perfluoroalkyl substances in matched human serum, urine, hair and nail. J Environ Sci-China 67:191–197
Ward S, Carrel JS (1979) Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 73:304–321
Yang KH, Lin YC, Fang MD, Wu CH, Panchangam C, Hong PKA, Lin CF (2013) Sorption of perfluorooctanoic acid (PFOA) onto sediment in the presence of dissolved natural organics Sep Sci Technol 48:1473–1478
Yen CA, Ruter DL, Turner CD, Pang S, Curran SP (2020) Loss of flavin adenine dinucleotide (FAD) impairs sperm function and male reproductive advantage in C. elegans eLife 9 https://doi.org/10.7554/eLife.52899
Yin JC, Liu R, Jian ZH, Yang D, Pu YP, Yin LH, Wang DY (2018) Di (2-ethylhexyl) phthalate-induced reproductive toxicity involved in dna damage-dependent oocyte apoptosis and oxidative stress in Caenorhabditis elegans. Ecotoxicol Environ Saf 163:298–306
Funding
This work was financially supported by Major Science and Technology Program for Water Pollution Control and Treatment (2014ZX07405002), National Natural Science Foundation of China grants (81872579, 81273123), Graduate Student Scientific Practice Innovation Projects in Jiangsu Province (KYCX19_0123), and Fundamental Research Fund of Central Public Welfare Research Institutions in 2019 (Innovation team project of new approach and application on substitution toxicology of environmental hormone substance).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible Editor: Mohamed M. Abdel-Daim
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOC 39 kb)
Rights and permissions
About this article
Cite this article
Yin, J., Jian, Z., Zhu, G. et al. Male reproductive toxicity involved in spermatogenesis induced by perfluorooctane sulfonate and perfluorooctanoic acid in Caenorhabditis elegans. Environ Sci Pollut Res 28, 1443–1453 (2021). https://doi.org/10.1007/s11356-020-10530-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-10530-8