Skip to main content
SpringerLink
Log in

Zinc Supplementation Reduces Testicular Cell Apoptosis in Mice and Improves Spermatogenic Dysfunction Caused by Marginal Zinc Deficiency

  • Research
  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Zinc (Zn) is an important trace element in the human body and plays an important role in growth, development, and male reproductive functions. Marginal zinc deficiency (MZD) is common in the human population and can cause spermatogenic dysfunction in males. Therefore, the aim of this study was to investigate methods to improve spermatogenic dysfunction caused by MZD and to further explore its mechanism of action. A total of 75 4-week-old male SPF ICR mice were randomly divided into five groups (control, MZD, MZD + ZnY2, MZD + ZnY4, and MZD + ZnY8, 15 mice per group). The dietary Zn content was 30 mg/kg in the control group and 10 mg/kg in the other groups. From low to high, the Zn supplementation doses administered to the three groups were 2, 4, and 8 mg/kg·bw. After 35 days, the zinc content, sperm quality, activity of spermatogenic enzymes, oxidative stress level, and apoptosis level of the testes in mice were determined. The results showed that MZD decreased the level of Zn in the serum, sperm quality, and activity of spermatogenic enzymes in mice. After Zn supplementation, the Zn level in the serum increased, sperm quality was significantly improved, and spermatogenic enzyme activity was restored. In addition, MZD reduced the content of antioxidants (copper-zinc superoxide dismutase (Cu–Zn SOD), metallothionein (MT), and glutathione (GSH) and promoted malondialdehyde (MDA) production. The apoptosis index of the testis also increased significantly in the MZD group. After Zn supplementation, the level of oxidative stress decreased, and the apoptosis index in the testis was reduced. Furthermore, quantitative real-time polymerase chain reaction (qRT–PCR) showed that the expression of B-cell lymphoma-2 (Bcl-2) mRNA and Bcl-2/BCL2-associated X (Bax) in the control group decreased in testicular cells, and their expression was restored after Zn supplementation. The results of this study indicated that Zn supplementation can reduce the level of oxidative stress and increase the ability of testicular cells to resist apoptosis, thereby improving spermatogenic dysfunction caused by MZD in mice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data Availability

All data presented in the main manuscript.

References

  1. Stefanidou M, Maravelias C, Dona A, Spiliopoulou C (2006) Zinc: a multipurpose trace element. Arch Toxicol 80(1):1–9. https://doi.org/10.1007/s00204-005-0009-5

    Article  PubMed  CAS  Google Scholar 

  2. Baltaci AK, Mogulkoc R, Baltaci SB (2019) Review: the role of zinc in the endocrine system. Pak J Pharm Sci 32(1):231–239

    PubMed  CAS  Google Scholar 

  3. Vickram S, Rohini K, Srinivasan S, Nancy VD, Archana K, Anbarasu K, Jeyanthi P, Thanigaivel S, Gulothungan G, Rajendiran N, Srikumar PS (2021) Role of Zinc (Zn) in human reproduction: a journey from initial spermatogenesis to childbirth. Int J Mol Sci 22(4). https://doi.org/10.3390/ijms22042188

  4. Prasad AS (2009) Zinc: role in immunity, oxidative stress and chronic inflammation. Curr Opin Clin Nutr Metab Care 12(6):646–652. https://doi.org/10.1097/MCO.0b013e3283312956

    Article  PubMed  CAS  Google Scholar 

  5. Wessells KR, Brown KH (2012) Estimating the global prevalence of zinc deficiency: results based on zinc availability in national food supplies and the prevalence of stunting. PLoS One 7(11):e50568. https://doi.org/10.1371/journal.pone.0050568

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  6. Caro CR, Del CCM, Arrollo J, Martinez G, Majana LS, Sarmiento-Rubiano LA (2016) Zinc deficiency: a global problem that affect the health and cognitive development. Arch Latinoam Nutr 66(3):165–175

    PubMed  CAS  Google Scholar 

  7. Jinno N, Nagata M, Takahashi T (2014) Marginal zinc deficiency negatively affects recovery from muscle injury in mice. Biol Trace Elem Res 158(1):65–72. https://doi.org/10.1007/s12011-014-9901-2

    Article  PubMed  CAS  Google Scholar 

  8. Colagar AH, Marzony ET, Chaichi MJ (2009) Zinc levels in seminal plasma are associated with sperm quality in fertile and infertile men. Nutr Res 29(2):82–88. https://doi.org/10.1016/j.nutres.2008.11.007

    Article  PubMed  CAS  Google Scholar 

  9. Merrells KJ, Blewett H, Jamieson JA, Taylor CG, Suh M (2009) Relationship between abnormal sperm morphology induced by dietary zinc deficiency and lipid composition in testes of growing rats. Br J Nutr 102(2):226–232. https://doi.org/10.1017/S0007114508159037

    Article  PubMed  CAS  Google Scholar 

  10. Allouche-Fitoussi D, Breitbart H (2020) The role of zinc in male fertility. Int J Mol Sci 21(20). https://doi.org/10.3390/ijms21207796

  11. Nishito Y, Kambe T (2018) Absorption mechanisms of iron, copper, and zinc: an overview. J Nutr Sci Vitaminol (Tokyo) 64(1):1–7. https://doi.org/10.3177/jnsv.64.1

    Article  PubMed  CAS  Google Scholar 

  12. Maret W, Sandstead HH (2006) Zinc requirements and the risks and benefits of zinc supplementation. J Trace Elem Med Biol 20(1):3–18. https://doi.org/10.1016/j.jtemb.2006.01.006

    Article  PubMed  CAS  Google Scholar 

  13. Ganger R, Garla R, Mohanty BP, Bansal MP, Garg ML (2016) Protective effects of zinc against acute arsenic toxicity by regulating antioxidant defense system and cumulative metallothionein expression. Biol Trace Elem Res 169(2):218–229. https://doi.org/10.1007/s12011-015-0400-x

    Article  PubMed  CAS  Google Scholar 

  14. Ho E, Ames BN (2002) Low intracellular zinc induces oxidative DNA damage, disrupts p53, NFkappa B, and AP1 DNA binding, and affects DNA repair in a rat glioma cell line. Proc Natl Acad Sci USA 99(26):16770–16775. https://doi.org/10.1073/pnas.222679399

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  15. Sakaguchi S, Iizuka Y, Furusawa S, Ishikawa M, Satoh S, Takayanagi M (2002) Role of Zn(2+) in oxidative stress caused by endotoxin challenge. Eur J Pharmacol 451(3):309–316. https://doi.org/10.1016/s0014-2999(02)02223-9

    Article  PubMed  CAS  Google Scholar 

  16. Zhu X, Yu C, Wu W, Shi L, Jiang C, Wang L, Ding Z, Liu Y (2022) Zinc transporter ZIP12 maintains zinc homeostasis and protects spermatogonia from oxidative stress during spermatogenesis. Reprod Biol Endocrinol 20(1):17. https://doi.org/10.1186/s12958-022-00893-7

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Chen Y, Yang J, Wang Y, Yang M, Guo M (2020) Zinc deficiency promotes testicular cell apoptosis in mice. Biol Trace Elem Res 195(1):142–149. https://doi.org/10.1007/s12011-019-01821-4

    Article  PubMed  CAS  Google Scholar 

  18. D’Arcy MS (2019) Cell death: a review of the major forms of apoptosis, necrosis and autophagy. Cell Biol Int 43(6):582–592. https://doi.org/10.1002/cbin.11137

    Article  PubMed  Google Scholar 

  19. Beigi HA, Dahan H, Tahmasbpour E, Bakhtiari KH, Shahriary A (2020) Effects of zinc deficiency on impaired spermatogenesis and male infertility: the role of oxidative stress, inflammation and apoptosis. Hum Fertil (Camb) 23(1):5–16. https://doi.org/10.1080/14647273.2018.1494390

    Article  Google Scholar 

  20. Kumari D, Nair N, Bedwal RS (2011) Testicular apoptosis after dietary zinc deficiency: ultrastructural and TUNEL studies. Syst Biol Reprod Med 57(5):233–243. https://doi.org/10.3109/19396368.2011.584500

    Article  PubMed  CAS  Google Scholar 

  21. Zhang Z, Cheng Q, Liu Y, Peng C, Wang Z, Ma H, Liu D, Wang L, Wang C (2022) Zinc-enriched yeast may improve spermatogenesis by regulating steroid production and antioxidant levels in mice. Biol Trace Elem Res 200(8):3712–3722. https://doi.org/10.1007/s12011-021-02970-1

    Article  PubMed  CAS  Google Scholar 

  22. Peng C, Cheng Q, Liu Y, Zhang Z, Wang Z, Ma H, Liu D, Wang L, Wang C (2022) Marginal zinc deficiency in mice increased the number of abnormal sperm and altered the expression level of spermatogenesis-related genes. Biol Trace Elem Res 200(8):3738–3749. https://doi.org/10.1007/s12011-021-02979-6

    Article  PubMed  CAS  Google Scholar 

  23. Adamo AM, Liu X, Mathieu P, Nuttall JR, Supasai S, Oteiza PI (2019) Early developmental marginal zinc deficiency affects neurogenesis decreasing neuronal number and altering neuronal specification in the adult rat brain. Front Cell Neurosci 13:62. https://doi.org/10.3389/fncel.2019.00062

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Croxford TP, Mccormick NH, Kelleher SL (2011) Moderate zinc deficiency reduces testicular Zip6 and Zip10 abundance and impairs spermatogenesis in mice. J Nutr 141(3):359–365. https://doi.org/10.3945/jn.110.131318

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Iwaya H, Kashiwaya M, Shinoki A, Lee JS, Hayashi K, Hara H, Ishizuka S (2011) Marginal zinc deficiency exacerbates experimental colitis induced by dextran sulfate sodium in rats. J Nutr 141(6):1077–1082. https://doi.org/10.3945/jn.111.138180

    Article  PubMed  CAS  Google Scholar 

  26. China NHCO (2017) Dietary nutrient reference intake of Chinese residents. http://www.nhc.gov.cn/wjw/yingyang/201710/ef2d42ee35894a46b7726457d08d7e2d.shtml. Accessed 2023/4/20

  27. Sarkar D, Chowdhury JP, Singh SK (2016) Effect of polybrominated diphenyl ether (BDE-209) on testicular steroidogenesis and spermatogenesis through altered thyroid status in adult mice. Gen Comp Endocrinol 239:50–61. https://doi.org/10.1016/j.ygcen.2015.11.009

    Article  PubMed  CAS  Google Scholar 

  28. Duan P, Hu C, Butler HJ, Quan C, Chen W, Huang W, Tang S, Zhou W, Yuan M, Shi Y, Martin FL, Yang K (2017) 4-Nonylphenol induces disruption of spermatogenesis associated with oxidative stress-related apoptosis by targeting p53-Bcl-2/Bax-Fas/FasL signaling. Environ Toxicol 32(3):739–753. https://doi.org/10.1002/tox.22274

    Article  ADS  PubMed  CAS  Google Scholar 

  29. Menkveld R (2010) Clinical significance of the low normal sperm morphology value as proposed in the fifth edition of the WHO laboratory manual for the examination and processing of human semen. Asian J Androl 12(1):47–58. https://doi.org/10.1038/aja.2009.14

    Article  PubMed  PubMed Central  Google Scholar 

  30. Wood RJ (2000) Assessment of marginal zinc status in humans. J Nutr 130(5S Suppl):1350S-1354S. https://doi.org/10.1093/jn/130.5.1350S

    Article  PubMed  CAS  Google Scholar 

  31. Yokokawa H, Fukuda H, Saita M, Miyagami T, Takahashi Y, Hisaoka T, Naito T (2020) Serum zinc concentrations and characteristics of zinc deficiency/marginal deficiency among Japanese subjects. J Gen Fam Med 21(6):248–255. https://doi.org/10.1002/jgf2.377

    Article  PubMed  PubMed Central  Google Scholar 

  32. Gaulke CA, Rolshoven J, Wong CP, Hudson LG, Ho E, Sharpton TJ (2018) Marginal zinc deficiency and environmentally relevant concentrations of arsenic elicit combined effects on the gut microbiome. mSphere 3(6). https://doi.org/10.1128/mSphere.00521-18

  33. Huang YL, Supasai S, Kucera H, Gaikwad NW, Adamo AM, Mathieu P, Oteiza PI (2016) Nutritional marginal zinc deficiency disrupts placental 11beta-hydroxysteroid dehydrogenase type 2 modulation. Food Funct 7(1):84–92. https://doi.org/10.1039/c5fo01203a

    Article  PubMed  CAS  Google Scholar 

  34. Nuttall JR, Supasai S, Kha J, Vaeth BM, Mackenzie GG, Adamo AM, Oteiza PI (2015) Gestational marginal zinc deficiency impaired fetal neural progenitor cell proliferation by disrupting the ERK1/2 signaling pathway. J Nutr Biochem 26(11):1116–1123. https://doi.org/10.1016/j.jnutbio.2015.05.007

    Article  PubMed  CAS  Google Scholar 

  35. Disilvestro RA, Dardenne M, Joseph E (2021) Comparison of thymulin activity with other measures of marginal zinc deficiency. Biol Trace Elem Res 199(2):585–587. https://doi.org/10.1007/s12011-020-02159-y

    Article  PubMed  Google Scholar 

  36. Hess SY, Peerson JM, King JC, Brown KH (2007) Use of serum zinc concentration as an indicator of population zinc status. Food Nutr Bull 28(3 Suppl):S403–S429. https://doi.org/10.1177/15648265070283S303

    Article  PubMed  Google Scholar 

  37. King JC, Shames DM, Woodhouse LR (2000) Zinc homeostasis in humans. J Nutr 130(5S Suppl):1360S-1366S. https://doi.org/10.1093/jn/130.5.1360S

    Article  PubMed  CAS  Google Scholar 

  38. Dimitrova AA, Strashimirov D, Betova T, Russeva A, Alexandrova M (2008) Zinc content in the diet affects the activity of Cu/ZnSOD, lipid peroxidation and lipid profile of spontaneously hypertensive rats. Acta Biol Hung 59(3):305–314. https://doi.org/10.1556/ABiol.59.2008.3.4

    Article  PubMed  Google Scholar 

  39. Kimura T, Kambe T (2016) The functions of metallothionein and ZIP and ZnT transporters: an overview and perspective. Int J Mol Sci 17(3):336. https://doi.org/10.3390/ijms17030336

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Yu J, Fujishiro H, Miyataka H, Oyama TM, Hasegawa T, Seko Y, Miura N, Himeno S (2009) Dichotomous effects of lead acetate on the expression of metallothionein in the liver and kidney of mice. Biol Pharm Bull 32(6):1037–1042. https://doi.org/10.1248/bpb.32.1037

    Article  PubMed  CAS  Google Scholar 

  41. Justus J, Weigand E (2014) The effect of a moderate zinc deficiency and dietary fat source on the activity and expression of the Delta(3)Delta (2)-enoyl-CoA isomerase in the liver of growing rats. Biol Trace Elem Res 158(3):365–375. https://doi.org/10.1007/s12011-014-9940-8

    Article  PubMed  CAS  Google Scholar 

  42. Mahfouz RZ, du Plessis SS, Aziz N, Sharma R, Sabanegh E, Agarwal A (2010) Sperm viability, apoptosis, and intracellular reactive oxygen species levels in human spermatozoa before and after induction of oxidative stress. Fertil Steril 93(3):814–821. https://doi.org/10.1016/j.fertnstert.2008.10.068

    Article  PubMed  CAS  Google Scholar 

  43. Chia SE, Ong CN, Chua LH, Ho LM, Tay SK (2000) Comparison of zinc concentrations in blood and seminal plasma and the various sperm parameters between fertile and infertile men. J Androl 21(1):53–57

    Article  PubMed  CAS  Google Scholar 

  44. Osadchuk LV, Danilenko AD, Osadchuk AV (2021) An influence of zinc on male infertility. Urologiia 5:84–93

    Article  Google Scholar 

  45. Piechal A, Blecharz-Klin K, Pyrzanowska J, Widy-Tyszkiewicz E (2016) Influence of long-term zinc administration on spatial learning and exploratory activity in rats. Biol Trace Elem Res 172(2):408–418. https://doi.org/10.1007/s12011-015-0597-8

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Casper RF, Meriano JS, Jarvi KA, Cowan L, Lucato ML (1996) The hypo-osmotic swelling test for selection of viable sperm for intracytoplasmic sperm injection in men with complete asthenozoospermia. Fertil Steril 65(5):972–976. https://doi.org/10.1016/s0015-0282(16)58271-5

    Article  PubMed  CAS  Google Scholar 

  47. Jeyendran RS, Van der Ven HH, Perez-Pelaez M, Crabo BG, Zaneveld LJ (1984) Development of an assay to assess the functional integrity of the human sperm membrane and its relationship to other semen characteristics. J Reprod Fertil 70(1):219–228. https://doi.org/10.1530/jrf.0.0700219

    Article  PubMed  CAS  Google Scholar 

  48. Zhang B, Lin S (2009) Effects of 3,4-dichloroaniline on testicle enzymes as biological markers in rats. Biomed Environ Sci 22(1):40–43. https://doi.org/10.1016/S0895-3988(09)60020-9

    Article  MathSciNet  PubMed  CAS  Google Scholar 

  49. Hodgen GD, Sherins RJ (1973) Enzymes as markers of testicular growth and development in the rat. Endocrinology 93(4):985–989. https://doi.org/10.1210/endo-93-4-985

    Article  PubMed  CAS  Google Scholar 

  50. Turgut G, Abban G, Turgut S, Take G (2003) Effect of overdose zinc on mouse testis and its relation with sperm count and motility. Biol Trace Elem Res 96(1–3):271–279. https://doi.org/10.1385/BTER:96:1-3:271

    Article  PubMed  CAS  Google Scholar 

  51. Sirisena D, Gayashani SW, Neranjan TM, Madusanka RK, Jeong JB, Lee J (2021) A copper-zinc-superoxide dismutase (CuZnSOD) from redlip mullet, Liza haematocheila: insights to its structural characteristics, immune responses, antioxidant activity, and potent antibacterial properties. Dev Comp Immunol 123:104165. https://doi.org/10.1016/j.dci.2021.104165

    Article  PubMed  CAS  Google Scholar 

  52. Ruttkay-Nedecky B, Nejdl L, Gumulec J, Zitka O, Masarik M, Eckschlager T, Stiborova M, Adam V, Kizek R (2013) The role of metallothionein in oxidative stress. Int J Mol Sci 14(3):6044–6066. https://doi.org/10.3390/ijms14036044

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91(2):179–194. https://doi.org/10.1093/aob/mcf118

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Semercioz A, Baltaci AK, Mogulkoc R, Avunduk MC (2017) Effect of zinc and melatonin on oxidative stress and serum inhibin-B levels in a rat testicular torsion-detorsion model. Biochem Genet 55(5–6):395–409. https://doi.org/10.1007/s10528-017-9826-5

    Article  PubMed  CAS  Google Scholar 

  55. Amara S, Abdelmelek H, Garrel C, Guiraud P, Douki T, Ravanat JL, Favier A, Sakly M, Ben RK (2008) Preventive effect of zinc against cadmium-induced oxidative stress in the rat testis. J Reprod Dev 54(2):129–134. https://doi.org/10.1262/jrd.18110

    Article  PubMed  CAS  Google Scholar 

  56. Aitken RJ, Roman SD (2008) Antioxidant systems and oxidative stress in the testes. Oxid Med Cell Longev 1(1):15–24. https://doi.org/10.4161/oxim.1.1.6843

    Article  PubMed  PubMed Central  Google Scholar 

  57. Wang Z, Peng C, Zhang Y, Wang L, Yu L, Wang C (2023) Characteristics of Zn content and localization, Cu-Zn SOD, and MT levels in the tissues of marginally Zn-deficient mice. Biol Trace Elem Res 201(1):262–271. https://doi.org/10.1007/s12011-022-03119-4

    Article  PubMed  CAS  Google Scholar 

  58. Alibek K, Irving S, Sautbayeva Z, Kakpenova A, Bekmurzayeva A, Baiken Y, Imangali N, Shaimerdenova M, Mektepbayeva D, Balabiyev A, Chinybayeva A (2014) Disruption of Bcl-2 and Bcl-xL by viral proteins as a possible cause of cancer. Infect Agent Cancer 9:44. https://doi.org/10.1186/1750-9378-9-44

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Delbridge AR, Grabow S, Strasser A, Vaux DL (2016) Thirty years of BCL-2: translating cell death discoveries into novel cancer therapies. Nat Rev Cancer 16(2):99–109. https://doi.org/10.1038/nrc.2015.17

    Article  PubMed  CAS  Google Scholar 

  60. Dewson G, Ma S, Frederick P, Hockings C, Tan I, Kratina T, Kluck RM (2012) Bax dimerizes via a symmetric BH3:groove interface during apoptosis. Cell Death Differ. 19(4):661–70. https://doi.org/10.1038/cdd.2011.138

    Article  PubMed  CAS  Google Scholar 

  61. Fan TJ, Han LH, Cong RS, Liang J (2005) Caspase family proteases and apoptosis. Acta Biochim Biophys Sin (Shanghai) 37(11):719–27. https://doi.org/10.1111/j.1745-7270.2005.00108.x

  62. Xu Y, Li A, Li X, Deng X, Gao XJ (2023) Zinc deficiency induces inflammation and apoptosis via oxidative stress in the kidneys of mice. Biol Trace Elem Res 201(2):739–750. https://doi.org/10.1007/s12011-022-03166-x

    Article  PubMed  CAS  Google Scholar 

  63. Pourhassanali N, Roshan-Milani S, Kheradmand F, Motazakker M, Bagheri M, Saboory E (2016) Zinc attenuates ethanol-induced Sertoli cell toxicity and apoptosis through caspase-3 mediated pathways. Reprod Toxicol 61:97–103. https://doi.org/10.1016/j.reprotox.2016.03.041

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Thanks to all members of Professor Wang CH’s lab at the School of Public Health, Wuhan University for their generous help. We would like to thank AJE for its professional support in the help of the language polish. At the same time, thanks to the animal facilities of Wuhan University Animal Experiment Center for the maintenance of the mouse population.

Funding

This study was supported by grants from Angel Nutritech Nutrition Fund (Grant No. AF2019004).

Author information

Authors and Affiliations

  1. Department of Toxicology, School of Public Health, Wuhan University, Wuhan, 430071, Hubei Province, People’s Republic of China

    Xiangchao Zeng, Ziqiong Wang, Lu Yu, Lei Wang, Yueling Liu, Yuxin Chen & Chunhong Wang

Authors
  1. Xiangchao Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ziqiong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lu Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yueling Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yuxin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Chunhong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Chunhong Wang and Xiangchao Zeng designed this study. Ziqiong Wang, Lu Yu, Lei Wang, Yueling Liu, and Yuxin Chen raised the animals. Xiangchao Zeng and Ziqiong Wang carried out index detection and wrote the first draft. Chunhong Wang, Lu Yu, and Lei Wang edited the final paper. All authors approved the final version.

Corresponding author

Correspondence to Chunhong Wang.

Ethics declarations

Ethics Approval

This study was approved by Committee of the Ethics of Animal Experiments of the Wuhan University School of Medicine (No.: WP2020-08053).

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zeng, X., Wang, Z., Yu, L. et al. Zinc Supplementation Reduces Testicular Cell Apoptosis in Mice and Improves Spermatogenic Dysfunction Caused by Marginal Zinc Deficiency. Biol Trace Elem Res 202, 1656–1668 (2024). https://doi.org/10.1007/s12011-023-03789-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-023-03789-8

Keywords

Search

Navigation