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The Effect of Cerium Oxide During Pregnancy on the Development of the Testicular Tissue of Newborn NMRI Mice

  • Afsaneh Nemati
  • Ali Farhadi
  • Cyrus Jalili
  • Mohammadreza GholamiEmail author
Article
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Abstract

Cerium(IV) oxide is widely used as a catalyst in all aspects of human life and human beings are exposed to these materials. The purpose of this experimental study was to investigate the effect of CeO2 during pregnancy on alterations in the testis tissue and blood biochemical parameters in newborn mice. Pregnant NMRI mice were divided randomly into five groups (n = 6 for each group) including one control group and 4 treatment groups. Injection of CeO2 solution was administered intraperitoneally at the doses of 10, 25, 80, and 250 mg/kg.bw, respectively, on GD 7 and GD 14. At the end of treatment period, the testicular histological and biochemical parameters of 2- and 6-day-old newborns were analyzed, as well as the biochemical parameters in serum samples of 15-day-old newborns. The number of spermatogonia, Sertoli, and Leydig cells in the testis of the 2-day-old newborn and spermatogonia and Leydig cells in the testis of the 6-day-old newborns in the 250 mg/kg.bw CeO2 treatment group was significantly reduced compared with the control group (P < 0.05). Testis MDA of the 2- and 6-day-old newborns in the treated group receiving 250 mg/kg.bw of CeO2 was significantly higher than the control group (P < 0.001). There was no significant difference between serum MDA and TAC levels between the treated groups with different doses of CeO2 compared with the control group. Therefore, CeO2 given to dams during pregnancy may affect the testicular tissue and blood biochemical parameters in neonates and may be dose-dependent.

Keywords

Cerium oxide Pregnant mice Newborn Testicular tissue 

Abbreviations

bw

Body weight

Ce

Cerium

CeO2

Cerium(IV) oxide

dd

Double distilled

dpp

Days post-partum

D2

2-day-old infant

D6

6-day-old infant

°C

Degree centigrade

Fig

Figure

g

Gram

GD

Gestational day

HCL

Hydrochloric acid

h

Hour

i.p

Intraperitoneal

L

Leydig cells

μl

Microliter

MDA

Malondialdehyde concentration

μm

Micrometer

min

Minute

mm3

Cubic millimeters

mg/kg.bw

Milligrams per kilogram of body weight

ml

Milliliter

nm

Nanometer

nmol

Nanomolar

KCL

Potassium chloride

REEs

Rare earth elements

St

Sertoli cells

Sp

Spermatogonia cells

TAC

Total antioxidant capacity

TCA

Tricloric acid

TPTZ

2,4,6Tripyridyl-s-triazine

TBA

Thiobarbituric acid

V

Volume

W

Weight

Notes

Acknowledgments

Eventually, the authors of this article would like to thank Razi Herbal Medicines Research Center, Lorestan University of Medical Sciences and Kermanshah University of Medical Sciences for funding, support, and cooperation in this project.

Compliance with Ethical Standards

The study was approved by the Institutional Animal Ethics Committee of Kermanshah University of Medical Sciences, Kermanshah, Iran. Ethical clearance number for this study is IR.KUMS.REC.1397.1004.

Conflict of Interest

The authors declare that they have no conflicts of interest.

References

  1. 1.
    Chen J, Xiao HJ, Qi T, Chen DL, Long HM, Liu SH (2015) Rare earths exposure and male infertility: the injury mechanism study of rare earths on male mice and human sperm. Environ Sci Pollut Res 22(3):2076–2086CrossRefGoogle Scholar
  2. 2.
    Kawagoe M, Ishikawa K, Wang SC, Yoshikawa K, Arany S, Zhou XP, Wang JS, Ueno Y, Koizumi Y, Kameda T, Koyota S, Sugiyama T (2008) Acute effects on the lung and the liver of oral administration of cerium chloride on adult, neonatal and fetal mice. J Trace Elem Med Biol 22(1):59–65CrossRefGoogle Scholar
  3. 3.
    Nelson BC, Johnson ME, Walker ML, Riley KR, Sims CM (2016) Antioxidant Cerium Oxide Nanoparticles in Biology and Medicine.Antioxidants (Basel) 17;5(2).  https://doi.org/10.3390/antiox5020015
  4. 4.
    Nelson BC et al (2016) Antioxidant cerium oxide nanoparticles in biology and medicine. Antioxidants 5(2):15CrossRefGoogle Scholar
  5. 5.
    Falchi L et al (2016) Cerium dioxide nanoparticles did not alter the functional and morphologic characteristics of ram sperm during short-term exposure. Theriogenology 85(7):1274–1281 e3CrossRefGoogle Scholar
  6. 6.
    Niu J et al (2007) Cardioprotective effects of cerium oxide nanoparticles in a transgenic murine model of cardiomyopathy. Cardiovasc Res 73(3):549–559CrossRefGoogle Scholar
  7. 7.
    Ma JY, Mercer RR, Barger M, Schwegler-Berry D, Scabilloni J, Ma JK, Castranova V (2012) Induction of pulmonary fibrosis by cerium oxide nanoparticles. Toxicol Appl Pharmacol 262(3):255–264CrossRefGoogle Scholar
  8. 8.
    Srinivas A, Rao PJ, Selvam G, Murthy PB, Reddy PN (2011) Acute inhalation toxicity of cerium oxide nanoparticles in rats. Toxicol Lett 205(2):105–115CrossRefGoogle Scholar
  9. 9.
    Cassee FR, van Balen EC, Singh C, Green D, Muijser H, Weinstein J, Dreher K (2011) Exposure, health and ecological effects review of engineered nanoscale cerium and cerium oxide associated with its use as a fuel additive. Crit Rev Toxicol 41(3):213–229CrossRefGoogle Scholar
  10. 10.
    Zhang Z, Gao P, Qiu Y, Liu G, Feng Y, Wiesner M (2016) Transport of cerium oxide nanoparticles in saturated silica media: influences of operational parameters and aqueous chemical conditions. Sci Rep 6:34135CrossRefGoogle Scholar
  11. 11.
    Park E-J, Cho WS, Jeong J, Yi JH, Choi K, Kim Y, Park K (2010) Induction of inflammatory responses in mice treated with cerium oxide nanoparticles by intratracheal instillation. J Health Sci 56(4):387–396CrossRefGoogle Scholar
  12. 12.
    Chaudhury K, Babu K N, Singh AK, Das S, Kumar A, Seal S (2013) Mitigation of endometriosis using regenerative cerium oxide nanoparticles. Nanomedicine 9(3):439–448CrossRefGoogle Scholar
  13. 13.
    Zhao H, Cheng J, Cai J, Cheng Z, Cui Y, Gao G, Hu R, Gong X, Wang L, Hong F (2012) Liver injury and its molecular mechanisms in mice caused by exposure to cerium chloride. Arch Environ Contam Toxicol 62(1):154–164CrossRefGoogle Scholar
  14. 14.
    Das S, Singh S, Dowding JM, Oommen S, Kumar A, Sayle TXT, Saraf S, Patra CR, Vlahakis NE, Sayle DC, Self WT, Seal S (2012) The induction of angiogenesis by cerium oxide nanoparticles through the modulation of oxygen in intracellular environments. Biomaterials 33(31):7746–7755CrossRefGoogle Scholar
  15. 15.
    Courbiere B, Auffan M, Rollais R, Tassistro V, Bonnefoy A, Botta A, Rose J, Orsière T, Perrin J (2013) Ultrastructural interactions and genotoxicity assay of cerium dioxide nanoparticles on mouse oocytes. Int J Mol Sci 14(11):21613–21628CrossRefGoogle Scholar
  16. 16.
    Popov AL, Popova NR, Selezneva II, Akkizov AY, Ivanov VK (2016) Cerium oxide nanoparticles stimulate proliferation of primary mouse embryonic fibroblasts in vitro. Mater Sci Eng C 68:406–413CrossRefGoogle Scholar
  17. 17.
    Kobyliak NM, Falalyeyeva TM, Kuryk OG, Beregova TV, Bodnar PM, Zholobak NM, Shcherbakov OB, Bubnov RV, Spivak MY (2015) Antioxidative effects of cerium dioxide nanoparticles ameliorate age-related male infertility: optimistic results in rats and the review of clinical clues for integrative concept of men health and fertility. EPMA J 6(1):12CrossRefGoogle Scholar
  18. 18.
    Preaubert L et al (2016) Cerium dioxide nanoparticles affect in vitro fertilization in mice. Nanotoxicology 10(1):111–117Google Scholar
  19. 19.
    Malmir M, Soleimani Mehranjani M, Naderi Noreini S, Faraji T (2018) Protective antioxidant effects of N-acetylcysteine against impairment of spermatogenesis caused by paranonylphenol. Andrologia 50:e13114CrossRefGoogle Scholar
  20. 20.
    Milazzo J et al (2007) Comparison of conditions for cryopreservation of testicular tissue from immature mice. Hum Reprod 23(1):17–28CrossRefGoogle Scholar
  21. 21.
    Milazzo J et al (2010) Rapid screening of cryopreservation protocols for murine prepubertal testicular tissue by histology and PCNA immunostaining. J Androl 31(6):617–630CrossRefGoogle Scholar
  22. 22.
    Gholami M et al (2017) Effects of 3, 4-dihydroxyflavone on cryopreserved testicular tissue of neonatal mouse. Herb Med J 2(1):18–25Google Scholar
  23. 23.
    Howard V, Reed M (2004) Unbiased stereology: three-dimensional measurement in microscopy. Garland ScienceGoogle Scholar
  24. 24.
    Buege JA, Aust SD (1978) [30] Microsomal lipid peroxidation. In: Methods in enzymology. Elsevier, pp 302–310Google Scholar
  25. 25.
    Esterbauer H, Cheeseman KH (1990) [42] Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. In: Methods in enzymology. Elsevier, pp 407–421Google Scholar
  26. 26.
    Benzie IF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239(1):70–76CrossRefGoogle Scholar
  27. 27.
    Oral R, Bustamante P, Warnau M, D’Ambra A, Guida M, Pagano G (2010) Cytogenetic and developmental toxicity of cerium and lanthanum to sea urchin embryos. Chemosphere 81(2):194–198CrossRefGoogle Scholar
  28. 28.
    Marzec-Wróblewska U, Kamiński P, Łakota P, Ludwikowski G, Szymański M, Wasilow K, Stuczyński T, Buciński A, Jerzak L (2015) Determination of rare earth elements in human sperm and association with semen quality. Arch Environ Contam Toxicol 69(2):191–201CrossRefGoogle Scholar
  29. 29.
    Préaubert L, Tassistro V, Auffan M, Sari-Minodier I, Rose J, Courbiere B, Perrin J (2018) Very low concentration of cerium dioxide nanoparticles induce DNA damage, but no loss of vitality, in human spermatozoa. Toxicol in Vitro 50:236–241CrossRefGoogle Scholar
  30. 30.
    Garcia T, Hofmann M (2015) Regulation of germ line stem cell homeostasis. Anim Reprod 12(1):35Google Scholar
  31. 31.
    Huang P, Li J, Zhang S, Chen C, Han Y, Liu N, Xiao Y, Wang H, Zhang M, Yu Q, Liu Y, Wang W (2011) Effects of lanthanum, cerium, and neodymium on the nuclei and mitochondria of hepatocytes: accumulation and oxidative damage. Environ Toxicol Pharmacol 31(1):25–32CrossRefGoogle Scholar
  32. 32.
    Brohi RD, Wang L, Talpur HS, Wu D, Khan FA, Bhattarai D, Rehman ZU, Farmanullah F, Huo LJ (2017) Toxicity of nanoparticles on the reproductive system in animal models: a review. Front Pharmacol 8:606CrossRefGoogle Scholar
  33. 33.
    Elshaari F, Fatum A, Sheriff D (2010) Spermatozoa-a unique representation of oxygenantioxidant paradox. Acta Medica Medianae 49(1):48–53Google Scholar
  34. 34.
    Hashemitabar M, Orazizadeh M, Khorsandi L (2008) Effect of dexamethasone on Fas ligand expression in mouse testicular germ cells. ZUMS J 16(62):17–26Google Scholar
  35. 35.
    Subramanyam D, Gurunathan D, Gaayathri R, Priya VV (2018) Comparative evaluation of salivary malondialdehyde levels as a marker of lipid peroxidation in early childhood caries. Eur J Dent 12(1):67CrossRefGoogle Scholar
  36. 36.
    Barrera G, Pizzimenti S, Daga M, Dianzani C, Arcaro A, Cetrangolo GP, Giordano G, Cucci MA, Graf M, Gentile F (2018) Lipid peroxidation-derived aldehydes, 4-hydroxynonenal and malondialdehyde in aging-related disorders. Antioxidants 7(8):102CrossRefGoogle Scholar
  37. 37.
    Mikkelsen SH et al (2011) Survey on basic knowledge about exposure and potential environmental and health risks for selected nanomaterials. Danish Ministry of the EnvironmentGoogle Scholar
  38. 38.
    Rosenkranz P, Fernández-Cruz ML, Conde E, Ramírez-Fernández MB, Flores JC, Fernández M, Navas JM (2012) Effects of cerium oxide nanoparticles to fish and mammalian cell lines: an assessment of cytotoxicity and methodology. Toxicol in Vitro 26(6):888–896CrossRefGoogle Scholar
  39. 39.
    Rogers, S.N., Toxicological effects of cerium oxide nanoparticle aggregates on Caenorhabditis elegans. 2013Google Scholar
  40. 40.
    Akinmuyisitan IW, Gbore FA, Adu OA (2015) Reproductive performance of growing female rabbits (Oryctolagus cuniculus) fed diets supplemented with cerium oxide. Journal of Medical and Bioengineering 4(3): 239–243Google Scholar
  41. 41.
    Adua O, Akinmuyisitana I, Gbore F (2015) Growth performance and blood profile of female rabbits fed dietary cerium oxide. J. bio-sci 21:69–75Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Afsaneh Nemati
    • 1
  • Ali Farhadi
    • 1
  • Cyrus Jalili
    • 2
  • Mohammadreza Gholami
    • 2
    • 3
    Email author
  1. 1.Razi Herbal Medicines Research CenterLorestan University of Medical SciencesKhorramabadIran
  2. 2.Department of AnatomyKermanshah University of Medical SciencesKermanshahIran
  3. 3.Department of Anatomical Sciences, Faculty of MedicineKermanshah University of Medical SciencesKermanshahIran

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