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Phycobiliproteins extract from Spirulina protects against single-dose cadmium-induced reproductive toxicity in male mice

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Abstract

Cadmium (Cd) is known for its many toxic effects on male population such as hypogonadism and fertility difficulties, which are oftenly associated with oxidative stress. As beneficial food, Spirulina(Sp) has been proved efficient against the heavy metal toxicity. This capacity can be associated with its phycobiliproteins (PBP). In this study, the capability of PBP and Sp to treat Cd-induced oxidative damage on the testes and spermatozoa was considered. CD-1 strain mice were orally treated with either Sp or PBP for 10 days prior to single-dose Cd challenge. Sperm quality determinations and testicle histology analysis were performed. Testosterone on serum was measured using enzyme-linked immunosorbent assay (ELISA). Oxidative damage was determined. Antioxidant enzyme activity was analyzed by measuring the activity of super oxide dismutase (SOD), catalase (Cat), and glutathione peroxidase (GpX). The motility and viability of sperm decrease with Cd and improve with PBP and Sp, as the acrosomal reaction (AR) is diminished by PBPs. Testosterone levels decrease due to Cd, and only Sp maintains elevated levels. Cd increases the production of malondialdehyde in the spermatozoa, but not in testes; this production of malondialdehyde in the spermatozoa decreases in the presence of PBP. ROS only decreases with Cd, FBP, and Sp at high concentrations. Advanced oxidative protein products (AOPP) decrease with Cd and PBPs. Cat and GpX increase their activity with Cd and are altered by FBP. Cd produces vascular alterations testes. Within the seminiferous tubule, it produces areas of necrosis and apoptosis, which improve with PBPs and Sp. PBPs have a strong antioxidant activity as they show protective properties against Cd oxidative–induced toxicity on testes and sperm.

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Abbreviations

AOPP:

Assay of advanced oxidation products

APC:

Allophycocyanin

AR:

Acrosomal reaction

Cat:

Catalase

Cd:

Cadmium

C-PC:

C-Phycocyanin

ELISA:

Enzyme-linked immunosorbent assay

GABA:

Gamma-aminobutyric acid

GpX:

Glutathione peroxidase

GSH:

Dehydrogenated glutathione

MDA:

Malondialdehyde

MT:

Metallothionein

PER:

Phycoerythrin

PBP:

Phycobiliproteins

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

Sp:

Spirulina

TBARS:

Thiobarbituric acid reactive substances

TCA:

Trichloroacetic acid

References

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Acknowledgments

The authors regard their thanks to Jaramillo Ph.D. Paniagua PhD. Ramon PhD from ENCB for supporting with equipment to the realization this work.

Availability of data and materials

All data generated or analyzed during this study are included in this published article (and its supplementary information files).

Author information

Authors and Affiliations

Authors

Contributions

RIMG performed all experiments, analyzed all the data, and wrote the main manuscript (Main author PhD; student). GGS revised the manuscript and wrote introduction, MAMV designed and supervised all experiments, JMC animal manipulation support and consultant wrote the abstract, JBB supported most experiments and performed PBP extraction, and GCC main author. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Germán Chamorro-Cevallos.

Ethics declarations

Ethics approval and consent to participate

This project was approved by IRB (CEI-ENCB), according to national normativity and policy, under the title “Efecto protector de las ficobiliproteínas de Spirulina (Arthrospira) maxima en dos modelos de toxicidad reproductiva inducida por cadmio en ratón.” Register number CEI-ENCB ZOO-025-2019.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Mohamed M. Abdel-Daim

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Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Highlights

- Cd toxic effects are non-limited to oxidative stress, as it exerts aggressively, especially damaging structural and proliferative tissue in the testicles.

- Sperm quality appears to be mainly affected to oxidative stress caused by Cd.

- PBPs and Sp show great antioxidant activity against Cd-induced testicular and sperm toxicity.

- PBPs show great antioxidant activity and cellular penetration as it also interferes with spermatogenesis and acrosomal reaction.

Appendix

Appendix

Formulae used to determine PBP concentration in Sp aqueous extract

$$ PC\ \left(\frac{mg}{mL}\right)=\frac{\left[A620-0.474(A652)\right]}{5.34} $$
$$ APC\ \left(\frac{mg}{mL}\right)=\frac{\left[A652-0.208(A620)\right]}{5.09} $$
$$ PER\ \left(\frac{mg}{mL}\right)=\frac{\left[A652-2.41\left(C- PC\right)-0.89(APC)\right]}{9.62} $$

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Montaño-González, R.I., Gutiérrez-Salmeán, G., Mojica-Villegas, M.A. et al. Phycobiliproteins extract from Spirulina protects against single-dose cadmium-induced reproductive toxicity in male mice. Environ Sci Pollut Res 29, 17441–17455 (2022). https://doi.org/10.1007/s11356-021-16668-3

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  • DOI: https://doi.org/10.1007/s11356-021-16668-3

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