The Selected Zinc Transporters (ZnT and ZIP) Gene Expression, Zinc, Iron and Glycogen Concentrations in Healthy Rat Testis: Effect of Aqueous Ajwain (𝘛𝘳𝘢𝘤𝘪𝘴𝘱𝘦𝘳𝘮𝘶𝘮 𝘢𝘮𝘮𝘪) Seeds Powder Extraction and High-intensity Treadmill Running
الموضوعات :Araz Nazari 1 , Abbas Ghanbari Niaki 2 , Khadijeh Nasiri 3
1 - Phd of student, Department of Exercise Physiology, Faculty of Sports Sciences, University of Mazandaran, Mazandaran, Babolsar, Iran
2 - Department of Exercise Physiology, Faculty of Sports Sciences, University of Mazandaran, Mazandaran, Babolsar, Iran
3 - Department of Exercise Physiology, Faculty of Sports Sciences, University of Mazandaran, Mazandaran, Babolsar, Iran
الکلمات المفتاحية: High-intensity exercise, aqueous extract of Ajwain seeds, Zinc transporter, Testicular tissue,
ملخص المقالة :
Zinc and iron as two important essential minerals for testis functions are controlled by Zinc transporters. It has been reported that zinc and its transporters are affected by nutrition and training. The main goals of the current experimentation were to the influences of training in combination with extraction of Ajwain seeds on rat testicular zinc and zinc transporters. Forty male rats were randomly assigned into four groups. Rats were orally received an aqueous Ajwain seed extraction (200 mg kg-1) and the saline groups were treated in the same manner. Results showed that gene expression of Znt5 had meaningfully changed in the ST group in comparison with SC (p = 0.004) and AT (p = 0.001) groups. Expression of this gene had meaningfully alteration in the AT group in comparison with ST (p = 0.036) and AC (p = 0.001) groups. Gene expression of Znt8 was also significantly increased in AT group compared to AC group (P = 0.010). Expression of Znt9 was also significantly increased in AT group in comparison with AC (P = 0.008) and ST (P = 0.026) groups. Expression of the other genes (Znt6, Zip7, Zip8, and Zip14) and also the content of Zn, Fe and glycogen did not show significant differences. The concurrent implementation of training and supplementation with the extract of Ajwain seed significantly modulated the expression levels of certain zinc transporters. These discoveries can offer new understandings into the underlying mechanisms of the effects of exercise and nutrition on testicular tissue.
1. Swain P.S., Rao S.B., Rajendran D., Dominic G., Selvaraju S., 2016. Nano zinc, an alternative to conventional zinc as animal feed supplement: A review. Animal Nutrition. 2(3), 134-141.
2. Khan M.S., Zaman S., Sajjad M., Shoaib M., Gilani G., 2011. Assessment of the level of trace element zinc in seminal plasma of males and evaluation of its role in male infertility. International Journal of Applied and Basic Medical Research. 1(2), 93.
3. Li D., Stovall D.B., Wang W., Sui G., 2020. Advances of zinc signaling studies in prostate cancer. International Journal of Molecular Sciences. 21(2), 667.
4. Parashuramulu S., Nagalakshmi D., Rao D.S., Kumar M.K., Swain P., 2015. Effect of zinc supplementation on antioxidant status and immune response in buffalo calves. Animal Nutrition and Feed Technology. 15(2), 179-188.
5. Prasad A. S., 2013. Discovery of human zinc deficiency: its impact on human health and disease. Advances in Nutrition. 4(2), 176-190.
6. Zhao C.Y., Tan S.X., Xiao X.Y., Qiu X.S., Pan J.Q., Tang Z.X., 2014. Effects of dietary zinc oxide nanoparticles on growth performance and antioxidative status in broilers. Biological Trace Element Research. 160, 361-367.
7. Parveen N., Ansari M.O., Ahmad M.F., Jameel S., Shadab G., 2017. Zinc: An element of extensive medical importance. Current Medicine Research and Practice. 7(3), 90-98.
8. Plum L.M., Rink L., Haase H., 2010. The essential toxin: impact of zinc on human health. International Journal of Environmental Research and Public Health. 7(4), 1342-1365.
9. Wong W.Y., Flik G., Groenen P.M., Swinkels D.W., Thomas C.M., Copius-Peereboom J.H., Merkus H.M., Steegers-Theunissen R.P., 2001. The impact of calcium, magnesium, zinc, and copper in blood and seminal plasma on semen parameters in men. Reproductive Toxicology. 15(2), 131-136.
10. Fallah A., Mohammad-Hasani A., Colagar A.H., 2018. Zinc is an essential element for male fertility: a review of Zn roles in men’s health, germination, sperm quality, and fertilization. Journal of Reproduction & Infertility. 19(2), 69.
11. Anagianni S., Tuschl K., 2019. Genetic disorders of manganese metabolism. Current neurology and Neuroscience Reports. 19, 1-10.
12. Balachandran R.C., Mukhopadhyay S., McBride D., Veevers J., Harrison F.E., Aschner M., Haynes E.N., Bowman A.B., 2020. Brain manganese and the balance between essential roles and neurotoxicity. Journal of Biological Chemistry. 295(19), 6312-6329.
13. Fujishiro H., Kambe T., 2022. Manganese transport in mammals by zinc transporter family proteins, ZNT and ZIP. Journal of Pharmacological Sciences. 148(1), 125-133.
14. Mukhopadhyay S., 2018. Familial manganese-induced neurotoxicity due to mutations in SLC30A10 or SLC39A14. Neurotoxicology. 64, 278-283.
15. Winslow J.W., Limesand K.H., Zhao N., 2020. The functions of ZIP8, ZIP14, and ZnT10 in the regulation of systemic manganese homeostasis. International Journal of Molecular Sciences. 21(9), 3304.
16. Kambe T., Hashimoto A., Fujimoto S., 2014. Current understanding of ZIP and ZnT zinc transporters in human health and diseases. Cellular and Molecular Life Sciences. 71, 3281-3295.
17. Chowanadisai W., Graham D.M., Keen C.L., Rucker R.B., Messerli M.A., 2013. Neurulation and neurite extension require the zinc transporter ZIP12 (slc39a12). Proceedings of the National Academy of Sciences. 110(24), 9903-9908.
18. Suzuki T., Ishihara K., Migaki H., Matsuura W., Kohda A., Okumura K., Nagao M., Yamaguchi-Iwai Y., Kambe T., 2005. Zinc transporters, ZnT5 and ZnT7, are required for the activation of alkaline phosphatases, zinc-requiring enzymes that are glycosylphosphatidylinositol-anchored to the cytoplasmic membrane. Journal of Biological Chemistry. 280(1), 637-643.
19. Fukunaka A., Kurokawa Y., Teranishi F., Sekler I., Oda K., Ackland M.L., Faundez V., Hiromura M., Masuda S., Nagao M., 2011. Tissue nonspecific alkaline phosphatase is activated via a two-step mechanism by zinc transport complexes in the early secretory pathway. Journal of Biological Chemistry. 286(18), 16363-16373.
20. Hogstrand C., Kille P., Nicholson R.I., Taylor K.M., 2009. Zinc transporters and cancer: a potential role for ZIP7 as a hub for tyrosine kinase activation. Trends in Molecular medicine. 15(3), 101-111.
21. Taylor K.M., Hiscox S., Nicholson R.I., Hogstrand C., Kille P., 2012. Protein kinase CK2 triggers cytosolic zinc signaling pathways by phosphorylation of zinc channel ZIP7. Science Signaling. 5(210), ra11-ra11.
22. Yamashita S., Miyagi C., Fukada T., Kagara N., Che Y.S., Hirano T., 2004. Zinc transporter LIVI controls epithelial-mesenchymal transition in zebrafish gastrula organizer. Nature. 429 (6989), 298-302.
23. Grubman A., Lidgerwood G.E., Duncan C., Bica L., Tan J.L., Parker S.J., Caragounis A., Meyerowitz J., Volitakis I., Moujalled D., 2014. Deregulation of subcellular biometal homeostasis through loss of the metal transporter, Zip7, in a childhood neurodegenerative disorder. Acta Neuropathologica Communications. 2(1), 1-14.
24. Song J., Kim D., Lee C.H., Lee M.S., Chun C.H., Jin E.J., 2013. MicroRNA-488 regulates zinc transporter SLC39A8/ZIP8 during pathogenesis of osteoarthritis. Journal of Biomedical Science. 20, 1-6.
25. Deng H., Qiao X., Xie T., Fu W., Li H., Zhao Y., Guo M., Feng Y., Chen L., Zhao Y., 2021. SLC-30A9 is required for Zn2+ homeostasis, Zn2+ mobilization, and mitochondrial health. Proceedings of the National Academy of Sciences. 118 (35), e2023909118.
26. Taylor K.M., Morgan H.E., Johnson A., Nicholson R.I., 2004. Structure-function analysis of HKE4, a member of the new LIV-1 subfamily of zinc transporters. Biochemical Journal. 377 (1), 131-139.
27. Myers S.A., Nield A., Chew G.S., Myers M.A., 2013. The zinc transporter, Slc39a7 (Zip7) is implicated in glycaemic control in skeletal muscle cells. PLoS One. 8(11), e79316.
28. Bellomo E.A., Meur G., Rutter G.A., 2011. Glucose regulates free cytosolic Zn2+ concentration, Slc39 (ZiP), and metallothionein gene expression in primary pancreatic islet β-cells. Journal of Biological Chemistry. 286 (29), 25778-25789.
29. Taylor K.M., Vichova P., Jordan N., Hiscox S., Hendley R., Nicholson R.I., 2008. ZIP7-mediated intracellular zinc transport contributes to aberrant growth factor signaling in antihormone-resistant breast cancer cells. Endocrinology. 149(10), 4912-4920.
30. Asif H.M., Sultana S., Akhtar N., 2014. A panoramic view on phytochemical, nutritional, ethanobotanical uses and pharmacological values of Trachyspermum ammi Linn. Asian Pacific Journal of Tropical Biomedicine. 4, S545-S553.
31. Cousins R.J., Liuzzi J.P., Lichten L.A., 2006. Mammalian zinc transport, trafficking, and signals. Journal of Biological Chemistry. 281(34), 24085-24089.
32. Liuzzi J.P., Lichten L.A., Rivera S., Blanchard R.K., Aydemir T.B., Knutson M.D., Ganz T., Cousins R.J., 2005. Interleukin-6 regulates the zinc transporter Zip14 in liver and contributes to the hypozincemia of the acute-phase response. Proceedings of the National Academy of Sciences. 102(19), 6843-6848.
33. Dashti A., Ghanbari-Niaki A., Nasiri K., Dashty H., 2024. Zinc Transporters in the Livers of Healthy Male Wistar Rats: An Investigation of the Effects of Aerobic Exercise and Supplementation with Pumpkin Seed and White Pea. Zahedan Journal of Research in Medical Sciences. 26(1), e137982.
34. Vitali L.A., Beghelli D., Nya P.C.B., Bistoni O., Cappellacci L., Damiano S., Lupidi G., Maggi F., Orsomando G., Papa F., 2016. Diverse biological effects of the essential oil from Iranian Trachyspermum ammi. Arabian Journal of Chemistry. 9(6), 775-786.
35. Ranjbaran A., Kavoosi G., Mojallal-Tabatabaei Z., Ardestani S.K., 2019. The antioxidant activity of Trachyspermum ammi essential oil and thymol in murine macrophages. Biocatalysis and Agricultural Biotechnology. 20, 101220.
36. Sauer A.K., Malijauskaite S., Meleady P., Boeckers T.M., McGourty K., Grabrucker A.M., 2022. Zinc is a key regulator of gastrointestinal development, microbiota composition and inflammation with relevance for autism spectrum disorders. Cellular and Molecular Life Sciences. 79(1), 46.
37. Zhao L., Oliver E., Maratou K., Atanur S.S., Dubois O.D., Cotroneo E., Chen C.N., Wang L., Arce C., Chabosseau P.L., 2015. The zinc transporter ZIP12 regulates the pulmonary vascular response to chronic hypoxia. Nature. 524(7565), 356-360.
38. Weaver B.P., Andrews G.K., 2012. Regulation of zinc-responsive Slc39a5 (Zip5) translation is mediated by conserved elements in the 3′-untranslated region. Biometals. 25, 319-335.
39. Fukada T., Kambe T., 2011. Molecular and genetic features of zinc transporters in physiology and pathogenesis. Metallomics. 3(7), 662-674.
40. Murray B., Rosenbloom C., 2018. Fundamentals of glycogen metabolism for coaches and athletes. Nutrition Reviews. 76(4), 243-259.
41. Holdsworth D.A., Cox P.J., Kirk T., Stradling H., Impey S.G., Clarke K., 2017. A ketone ester drink increases postexercise muscle glycogen synthesis in humans. Medicine and Science in Sports and Exercise. 49(9), 1789.
42. Flynn S., Rosales A., Hailes W., Ruby B., 2020. Males and females exhibit similar muscle glycogen recovery with varied recovery food sources. European Journal of Applied Physiology. 120, 1131-1142.
43. Poffé C., Ramaekers M., Bogaerts S., Hespel P., 2020. Exogenous ketosis impacts neither performance nor muscle glycogen breakdown in prolonged endurance exercise. Journal of applied Physiology. 128(6), 1643-1653.
44. Petit J., Eren-Koçak E., Karatas H., Magistretti P., Dalkara T., 2021. Brain glycogen metabolism: A possible link between sleep disturbances, headache and depression. Sleep Medicine Reviews. 59, 101449.
45. Khong T., Selvanayagam V., Sidhu S., Yusof A., 2017. Role of carbohydrate in central fatigue: a systematic review. Scandinavian Journal of Medicine & Science in Sports. 27(4), 376-384.
46. Ghanbari-Niaki A., Rahmati-Ahmadabad S., 2013. Effects of a fixed-intensity of endurance training and pistacia atlantica supplementation on ATP-binding cassette G4 expression. Chinese Medicine. 8(1), 1-9.
47. Organization U.N.I.D., Handa S.S., Khanuja S.P.S., Longo G., Rakesh D.D., 2008. Extraction technologies for medicinal and aromatic plants. Earth, Environmental and Marine Sciences and Technologies.
48. Javed I., Iqbal Z., Rahman Z., Khan F., Muhammad F., Aslam B., Ali L., 2006. Comparative antihyperlipidaemic efficacy of Trachyspermum ammi extracts in albino rabbits. Pakistan Veterinary Journal. 26(1), 23.
49. Cemek M., Büyükokuroğlu M.E., Sertkaya F., Alpdağtaş S., Hazini A., Önül A., Göneş S., 2014. Effects of food color additives on antioxidant functions and bioelement contents of liver, kidney and brain tissues in rats. J Food Nutr Res. 2(10), 686-691.
50. Lo S., Russell J., Taylor A., 1970. Determination of glycogen in small tissue samples. Journal of Applied Physiology. 28(2), 234-236.
51. Kelleher S.L., McCormick N.H., Velasquez V., Lopez V., 2011. Zinc in specialized secretory tissues: roles in the pancreas, prostate, and mammary gland. Advances in Nutrition. 2(2), 101-111.
52. Yu Y.Y., Kirschke C.P., Huang L., 2007. Immunohistochemical analysis of ZnT1, 4, 5, 6, and 7 in the mouse gastrointestinal tract. Journal of Histochemistry & Cytochemistry. 55(3), 223-234.
53. Brugger D., Hanauer M., Ortner J., Windisch W.M., 2021. The response of zinc transporter gene expression of selected tissues in a pig model of subclinical zinc deficiency. The Journal of Nutritional Biochemistry. 90, 108576.
54. Boughammoura S., Ben Mimouna S., Chemek M., Ostertag A., Cohen-Solal M., Messaoudi I., 2020. Disruption of bone zinc metabolism during postnatal development of rats after early life exposure to cadmium. International Journal of Molecular Sciences. 21(4), 1218.
55. Ni H., Li C., Feng X., Cen J.N., 2011. Effects of forced running exercise on cognitive function and its relation to zinc homeostasis-related gene expression in rat hippocampus. Biological Trace Element Research. 142, 704-712.
56. Liu J., Xu C., Yu X., Zuo Q., 2021. Expression profiles of SLC39A/ZIP7, ZIP8 and ZIP14 in response to exercise-induced skeletal muscle damage. Journal of Trace Elements in Medicine and Biology. 67, 126784.
57. Barman S., Pradeep S.R., Srinivasan K., 2017. Zinc supplementation mitigates its dyshomeostasis in experimental diabetic rats by regulating the expression of zinc transporters and metallothionein. Metallomics. 9(12), 1765-1777.
58. Zhang X., Guan T., Yang B., Chi Z., Wang Z.Y., Gu H.F., 2018. A novel role for zinc transporter 8 in the facilitation of zinc accumulation and regulation of testosterone synthesis in Leydig cells of human and mouse testicles. Metabolism. 88, 40-50.
59. Noh H., Paik H.Y., Kim J., Chung J., 2014. The changes of zinc transporter ZnT gene expression in response to zinc supplementation in obese women. Biological Trace Element Research. 162, 38-45.
60. Foster M., Petocz P., Samman S., 2013. Inflammation markers predict zinc transporter gene expression in women with type 2 diabetes mellitus. The Journal of Nutritional Biochemistry. 24 (9), 1655-1661.
61. Basolo A., Poma A. M., Macerola E., Bonuccelli D., Proietti A., Salvetti A., Vignali P., Torregrossa L., Evangelisti L., Sparavelli R., 2023. Autopsy study of testicles in Covid-19: upregulation of immune-related genes and downregulation of testis-specific genes. The Journal of Clinical Endocrinology & Metabolism. 108(4), 950-961.
62. Huang L., Tepaamorndech S., 2013. The SLC30 family of zinc transporters–a review of current understanding of their biological and pathophysiological roles. Molecular Aspects of Medicine. 34(2-3), 548-560.
63. Wise T., Lunstra D., Rohrer G., Ford J., 2003. Relationships of testicular iron and ferritin concentrations with testicular weight and sperm production in boars. Journal of Animal Science. 81(2), 503-511.
64. Toebosch A., Kroos M., Grootegoed J., 1987. Transport of transferrin‐bound iron into rat Sertoli cells and spermatids. International Journal of Andrology. 10(6), 753-764.
65. Lieu P.T., Heiskala M., Peterson P.A., Yang Y., 2001. The roles of iron in health and disease. Molecular Aspects of Medicine. 22(1-2), 1-87.