{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,13]],"date-time":"2026-06-13T11:13:44Z","timestamp":1781349224463,"version":"3.54.1"},"reference-count":101,"publisher":"Springer Science and Business Media LLC","issue":"10","license":[{"start":{"date-parts":[[2023,5,12]],"date-time":"2023-05-12T00:00:00Z","timestamp":1683849600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2023,5,12]],"date-time":"2023-05-12T00:00:00Z","timestamp":1683849600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"funder":[{"DOI":"10.13039\/501100010807","name":"Firat University Scientific Research Projects Management Unit","doi-asserted-by":"publisher","award":["FF.19.16"],"award-info":[{"award-number":["FF.19.16"]}],"id":[{"id":"10.13039\/501100010807","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Reprod. Sci."],"published-print":{"date-parts":[[2023,10]]},"DOI":"10.1007\/s43032-023-01265-1","type":"journal-article","created":{"date-parts":[[2023,5,12]],"date-time":"2023-05-12T14:02:30Z","timestamp":1683900150000},"page":"3103-3122","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Activation of Nrf-2 Transcription Factor and Caspase Pathway with Royal Jelly Reduces Fluoride Induced Testicular Damage and Infertility in Rats"],"prefix":"10.1007","volume":"30","author":[{"given":"Gozde","family":"Parlak","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6243-4221","authenticated-orcid":false,"given":"Abdullah","family":"Aslan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gaffari","family":"Turk","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tuncay","family":"Kuloglu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Merve Kavak","family":"Balgetir","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ozlem","family":"Gok","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seda","family":"Beyaz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Akif Evren","family":"Parlak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Serap Dayan","family":"Cinkara","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2023,5,12]]},"reference":[{"key":"1265_CR1","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1038\/aja.2011.40","volume":"13","author":"PP Mathur","year":"2011","unstructured":"Mathur PP, D\u2019Cruz SC. The effect of environmental contaminants on testicular function. As J Andrology. 2011;13:585\u201391.","journal-title":"As J Andrology"},{"key":"1265_CR2","first-page":"20","volume":"22","author":"Y Zhang","year":"2003","unstructured":"Zhang Y. Environmental pollution threatens human fertility. Environment Rev. 2003;22:20\u20135.","journal-title":"Environment Rev"},{"key":"1265_CR3","first-page":"5614803","volume":"28","author":"AM Alhusaini","year":"2018","unstructured":"Alhusaini AM, Faddah LM, El Orabi NF, Hasan IH. Role of some natural antioxidants in the modulation of some proteins expressions against sodium fluoride \u0131nduced renal injury. Biomed Res Int. 2018;28:5614803.","journal-title":"Biomed Res Int"},{"key":"1265_CR4","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1016\/j.fct.2013.12.041","volume":"65","author":"G Yuan","year":"2014","unstructured":"Yuan G, Dai S, Yin Z, Lu H, Jia R, Xu J, Song X, Li L, Shu Y, Zhao X. Toxicological assessment of combined lead and cadmium: acute and sub-chronic toxicity study in rats. Food Chem Toxicol. 2014;65:260\u20138.","journal-title":"Food Chem Toxicol"},{"key":"1265_CR5","doi-asserted-by":"crossref","first-page":"8966","DOI":"10.1021\/acs.jafc.7b03822","volume":"65","author":"JH Zhang","year":"2017","unstructured":"Zhang JH, Zhu YC, Shi Y, Han YL, Liang C, Feng ZY, Zheng HP, Eng M, Wang JD. Fluoride-induced autophagy via the regulation of phosphorylation of mammalian targets of rapamycin in mice leydig cells. J Agric Food Chem. 2017;65:8966\u201376.","journal-title":"J Agric Food Chem"},{"key":"1265_CR6","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1007\/s00204-017-2054-2","volume":"92","author":"ZL Sun","year":"2018","unstructured":"Sun ZL, Li SJ, Yu YX, Chen HY, Ommati MM, Manthari RK, Niu RY, Wang JD. Alterations in epididymal proteomics and antioxidant activity of mice exposed to fluoride. Arch Toxic. 2018;92:169\u201380.","journal-title":"Arch Toxic"},{"key":"1265_CR7","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1016\/j.chemosphere.2018.05.153","volume":"207","author":"ZL Sun","year":"2018","unstructured":"Sun ZL, Wei RF, Luo GY, Niu RY, Wang JD. Proteomic identification of sperm from mice exposed to sodium fluoride. Chemosphere. 2018;207:676\u201381.","journal-title":"Chemosphere"},{"key":"1265_CR8","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1136\/jmedgenet-2018-105952","volume":"56","author":"WH Liu","year":"2019","unstructured":"Liu WH, Sha YW, Li Y, Mei LB, Lin SB, Huang XJ, Lu JH, Ding L, Kong SB, Lu ZX. Loss-of-function mutations in SPEF2 cause multiple morphological abnormalities of the sperm flagella (MMAF). J Medic Gen. 2019;56:678\u201384.","journal-title":"J Medic Gen"},{"key":"1265_CR9","doi-asserted-by":"crossref","first-page":"5240","DOI":"10.1021\/acs.jafc.9b01114","volume":"67","author":"Y Liu","year":"2019","unstructured":"Liu Y, Liang C, Gao Y, Jiang SS, He YY, Han YL, Olfati A, Manthari RK, Wang JD, Zhang JH. Fluoride interferes with the sperm fertilizing ability via downregulated SPAM1, ACR, and PRSS21 expression in rat epididymis. J Agric Food Chem. 2019;67:5240\u20139.","journal-title":"J Agric Food Chem"},{"key":"1265_CR10","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1016\/j.chemosphere.2015.08.030","volume":"139","author":"BH Zhou","year":"2015","unstructured":"Zhou BH, Zhao J, Liu J, Zhang JL, Li J, Wang HW. Fluoride induced oxidative stress is involved in the morphological damage and dysfunction of liver in female mice. Chemosphere. 2015;139:504\u201311.","journal-title":"Chemosphere"},{"key":"1265_CR11","doi-asserted-by":"crossref","first-page":"628","DOI":"10.1016\/j.chemosphere.2017.12.027","volume":"194","author":"RY Niu","year":"2018","unstructured":"Niu RY, Chen HJ, Manthari RK, Sun ZL, Wang JM, Zhang JH, Wang JD. Effects of fluoride on synapse morphology and myelin damage in mouse hippocampus. Chemosphere. 2018;194:628\u201333.","journal-title":"Chemosphere"},{"key":"1265_CR12","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1007\/s00204-010-0537-5","volume":"85","author":"YM Ge","year":"2011","unstructured":"Ge YM, Niu RY, Zhang JH, Wang JD. Proteomic analysis of brain proteins of rats exposed to high fluoride and low iodine. Arch Toxic. 2011;85:27\u201333.","journal-title":"Arch Toxic"},{"key":"1265_CR13","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1002\/(SICI)1520-670X(2000)13:1<165::AID-JTRA17>3.0.CO;2-R","volume":"13","author":"JT Hindmarsh","year":"2000","unstructured":"Hindmarsh JT. Arsenic its clinical and environmental significance. J Tr Elem Exper Med. 2000;13:165\u201372.","journal-title":"J Tr Elem Exper Med"},{"key":"1265_CR14","doi-asserted-by":"crossref","first-page":"2324","DOI":"10.1016\/j.lfs.2005.04.016","volume":"77","author":"SJS Flora","year":"2005","unstructured":"Flora SJS, Bhadauria S, Pant SC, Dhaked RK. Arsenic induced blood and brain oxdative stress and its response to some thiol chelators in rats. Life Sci. 2005;77:2324\u201337.","journal-title":"Life Sci"},{"key":"1265_CR15","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1080\/01480540701380075","volume":"30","author":"M M\u0131ttal","year":"2007","unstructured":"M\u0131ttal M, Flora SJS. Vitamin E supplementation protects oxidative stress during arsenic and fluoride antagonism in male mice. Drug Chem Toxic. 2007;30:263\u201381.","journal-title":"Drug Chem Toxic"},{"key":"1265_CR16","first-page":"453","volume":"57","author":"S Gawel","year":"2004","unstructured":"Gawel S, Wardas M, Niedworok E, Wardas P. Malondialdehyde (MDA) as a lipid peroxidation marker. Wiad Lek. 2004;57:453\u20135.","journal-title":"Wiad Lek"},{"key":"1265_CR17","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/S0301-2115(98)00242-5","volume":"82","author":"MF Knapen","year":"1999","unstructured":"Knapen MF, Zusterzeel PL, Peters WH, Steegers EA. Glutathione and glutathionerelated enzymes in reproduction. A review. Europ J Obst Gynec Repr Bio. 1999;82:171\u201384.","journal-title":"Europ J Obst Gynec Repr Bio"},{"key":"1265_CR18","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.mam.2008.05.005","volume":"30","author":"SC Lu","year":"2009","unstructured":"Lu SC. Regulation of glutathione synthesis. Molec Asp Medic. 2009;30:42\u201359.","journal-title":"Molec Asp Medic"},{"key":"1265_CR19","doi-asserted-by":"crossref","unstructured":"Nandi A, Yan LJ, Jana CK, Das N. Role of catalase in oxidative stress- and age-associated degenerative diseases. Oxid Medic Cell Long. 2019;9613090.","DOI":"10.1155\/2019\/9613090"},{"key":"1265_CR20","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1016\/j.jaim.2017.07.005","volume":"9","author":"R Baskaran","year":"2018","unstructured":"Baskaran R, Priya LB, Kumar VS, Padma VV. Tinospora cordifolia extract prevents cadmium-induced oxidative stress and hepatotoxicity in experimental rats. J of Ayur Integ Medic. 2018;9:252\u20137.","journal-title":"J of Ayur Integ Medic"},{"key":"1265_CR21","doi-asserted-by":"crossref","first-page":"104514","DOI":"10.1016\/j.jff.2021.104514","volume":"82","author":"G Jianying","year":"2021","unstructured":"Jianying G, Zixu W, Yaoxing C, Jing C, Wenli T, Baochen M, Yulan D. Active components and biological functions of royal jelly. J Func Foods. 2021;82:104514.","journal-title":"J Func Foods"},{"key":"1265_CR22","first-page":"16","volume":"15","author":"E Akyol","year":"2015","unstructured":"Akyol E, Baran Y. Structure of royal jelly, importance for humans and bees. U Bee J. 2015;15:16\u201321.","journal-title":"U Bee J"},{"key":"1265_CR23","doi-asserted-by":"crossref","first-page":"382","DOI":"10.3390\/ijms21020382","volume":"21","author":"A Saboor","year":"2020","unstructured":"Saboor A, Maria GC, Filippo F, Solomon ZA, Jianke L. New insights into the biological and pharmaceutical properties of royal jelly. Int J Mol Sci. 2020;21:382.","journal-title":"Int J Mol Sci"},{"key":"1265_CR24","doi-asserted-by":"crossref","first-page":"1057","DOI":"10.1002\/hed.10318","volume":"25","author":"C Scully","year":"2003","unstructured":"Scully C, Epstein J, Sonis S. Oral mucositis: A challenging complication of radiotherapy, chemotherapy, and radiochemotherapy: Part 1, pathogenesis and prophylaxis of mucositis. Head Neck. 2003;25:1057\u201370.","journal-title":"Head Neck"},{"key":"1265_CR25","first-page":"113","volume":"9","author":"E Ghanbari","year":"2015","unstructured":"Ghanbari E, Nejati V, Najafi G, Khazaei M, Babaei M. Study on the effect of royal jelly on reproductive parameters in streptozotocin-induced diabetic rats. Int J Fert Ster. 2015;9:113\u201320.","journal-title":"Int J Fert Ster"},{"key":"1265_CR26","first-page":"219","volume":"34","author":"C Wang","year":"2018","unstructured":"Wang C, Chen Y, Manthari RK, Wang J. Abnormal spermatogenesis following sodium fluoride exposure is associated with the down regulation of CREM and ACT in the mouse testis, Toxicol. Ind Health. 2018;34:219\u201327.","journal-title":"Ind Health"},{"key":"1265_CR27","doi-asserted-by":"crossref","first-page":"778","DOI":"10.1016\/j.theriogenology.2006.10.013","volume":"67","author":"G Turk","year":"2007","unstructured":"Turk G, Atessahin A, Sonmez M, Yuce A, Ceribasi AO. Lycopene Protects against cyclosporine a-induced testicular toxicity in rats. Theriogenology. 2007;67:778\u201385.","journal-title":"Theriogenology"},{"key":"1265_CR28","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.lfs.2014.09.005","volume":"117","author":"A Aslan","year":"2014","unstructured":"Aslan A, Can MI. Milk thistle impedes the development of carbontetrachloride-induced liver damage in rats through suppression of bcl-2 and regulating caspase pathway. Life Sci. 2014;117:13\u20138.","journal-title":"Life Sci"},{"key":"1265_CR29","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1016\/0003-2697(79)90738-3","volume":"95","author":"H Ohkawa","year":"1979","unstructured":"Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979;95:351\u20138.","journal-title":"Anal Biochem"},{"key":"1265_CR30","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/0003-9861(59)90090-6","volume":"82","author":"GL Ellman","year":"1959","unstructured":"Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophysics. 1959;82:70\u20137.","journal-title":"Arch Biochem Biophysics"},{"key":"1265_CR31","first-page":"930","volume":"12","author":"M Yigit","year":"2019","unstructured":"Yigit M, Gunes A, Uguz C, Yalc\u0131n TO, T\u00f6k L, Oz A, Naz\u0131roglu M. Effects of astaxanthin on antioxidant parameters in ARPE-19 cells on oxidative stress model. Int J Ophthalmol. 2019;12:930\u20135.","journal-title":"Int J Ophthalmol"},{"key":"1265_CR32","doi-asserted-by":"crossref","unstructured":"Luck H. Catalase. In: Bergmeyer HU (ed) Methods of Enzymatic Analysis.\u00a0New York and London: Academic Press; 1965. pp. 885\u2013894.","DOI":"10.1016\/B978-0-12-395630-9.50158-4"},{"key":"1265_CR33","doi-asserted-by":"crossref","first-page":"662","DOI":"10.1016\/j.biopha.2018.06.020","volume":"105","author":"A Aslan","year":"2018","unstructured":"Aslan A, Gok O, Erman O, Kuloglu T. Ellagic acid impedes carbontetrachloride induced liver damage in rats through suppression of NF kB, bcl-2 and regulating nrf-2 and caspase pathway. Biomed Pharmather. 2018;105:662\u20139.","journal-title":"Biomed Pharmather"},{"key":"1265_CR34","unstructured":"Y\u0131lmaz I. Evaluation of apoptosis levels in germ cells in testes after experimental varicocele in adult rats and the level and duration of regression of elevated apoptosis after varicocelectomy by TUNEL method. Ministry of Health Taksim Training and Research Hospital Urology Clinic, Specialization Thesis in Medicine. 2005."},{"key":"1265_CR35","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1016\/j.jhep.2006.08.011","volume":"46","author":"J Qiu","year":"2007","unstructured":"Qiu J, Liu Z, Li Y, Xuan H, Lin Q, Li F, Wang Y, Li Z, Zhao M. Overexpression of the gene for transmembrane 4 superfamily member 4 accelerates liver damage in rats treated with CCl4. J Hepat. 2007;46:266\u201375.","journal-title":"J Hepat"},{"key":"1265_CR36","unstructured":"Can MI. The effect of thistle (Silybum marianum L.) on the caspase-3, caspase-9, bax, bcl-2 protein expression and DNA damage in rats with carbon tetrachloride (CCl4)-induced liver damage. Firat Univ. Master Thesis. 2014."},{"key":"1265_CR37","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1289\/ehp.00108961","volume":"108","author":"SH Swan","year":"2000","unstructured":"Swan SH, Elkin EP, Fenster L. The question of declining sperm density revisited: An analysis of 101 studies. Environ Health Perspect. 2000;108:961\u20136.","journal-title":"Environ Health Perspect"},{"key":"1265_CR38","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1093\/humupd\/dmx022","volume":"23","author":"L Hagai","year":"2017","unstructured":"Hagai L, Niels J, Anderson MA, Jaime M, Dan Weksler-Derri IM, Rachel P, Shanna HS. Temporal trends in sperm count: A systematic review and meta-regression analysis. Hum Repr Update. 2017;23:646\u201359.","journal-title":"Hum Repr Update"},{"key":"1265_CR39","first-page":"98","volume":"41","author":"B Spittle","year":"2008","unstructured":"Spittle B. Fluor\u0131de and fertility. Editorial Fluoride. 2008;41:98\u2013100.","journal-title":"Editorial Fluoride"},{"key":"1265_CR40","doi-asserted-by":"crossref","first-page":"1441","DOI":"10.1007\/s00204-011-0672-7","volume":"85","author":"S Zilong","year":"2011","unstructured":"Zilong S, Ruiyan N, Bin W, Zhibin J, Jinming W, Jianhai Z, Shaolin W, Jundong W. Fluoride-induced apoptosis and gene expression profiling in mice sperm in vivo. Arch Toxicol. 2011;85:1441\u201352.","journal-title":"Arch Toxicol"},{"key":"1265_CR41","first-page":"1","volume":"15","author":"A Karadeniz","year":"2009","unstructured":"Karadeniz A, Simsek N, Koc F, Alp H. The \u0131nvestigation of protective effects of the panax ginseng on oxidative damage induced by chronic fluoride toxicity in mice testis tissue. Kafkas Univ Vet Fak. 2009;15:1\u20138.","journal-title":"Kafkas Univ Vet Fak"},{"key":"1265_CR42","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1177\/0748233708089041","volume":"23","author":"RS Gupta","year":"2007","unstructured":"Gupta RS, Khan TI, Agrawal D, Kachhawa JBS. The toxic effects of sodium fluoride on the reproductive system of male rats. Toxicol Ind Health. 2007;23:507\u201313.","journal-title":"Toxicol Ind Health"},{"key":"1265_CR43","first-page":"1","volume":"11","author":"A Pervez","year":"2016","unstructured":"Pervez A, S\u0131nha MK, Yadav M. Implications of fluoride toxicity on the male reproductive system: A Review. J Moun Res. 2016;11:1\u20137.","journal-title":"J Moun Res"},{"key":"1265_CR44","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1016\/j.scitotenv.2017.12.131","volume":"624","author":"HG Mikkonen","year":"2018","unstructured":"Mikkonen HG, Dasika R, Drake JA, Wallis CJ, Clarke BO, Reichman SM. Evaluation of environmental and anthropogenic influences on ambient background metal and metalloid concen- trations in soil. Sci Total Environ. 2018;624:599\u2013610.","journal-title":"Sci Total Environ"},{"key":"1265_CR45","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1016\/S0890-6238(02)00038-2","volume":"16","author":"D Ghosh","year":"2002","unstructured":"Ghosh D, Das SS, Maiti R, Jana D, Das UB. Testicular toxicity in sodium fluoride treated rats: Association with oxidative stress. Rep Tox. 2002;16:385\u201390.","journal-title":"Rep Tox"},{"key":"1265_CR46","first-page":"568","volume":"19","author":"A Minami","year":"2016","unstructured":"Minami A, Matsushita H, Ieno D, Matsuda Y, Horii Y, Ishii A, Suzuki T. Improvement of neurological disorders in postmenopausal model rats by administration of royal jelly climacteric. J Inter Men Soc. 2016;19:568\u201373.","journal-title":"J Inter Men Soc"},{"key":"1265_CR47","doi-asserted-by":"crossref","first-page":"1149","DOI":"10.3390\/molecules24061149","volume":"24","author":"Y Pan","year":"2019","unstructured":"Pan Y, Xu J, Jin P, Yang Q, Zhu K, You M, Hu F. royal jelly ameliorates behavioral deficits, cholinergic system deficiency, and autonomic nervous dysfunction in ovariectomized cholesterol-fed rabbits. Molecules. 2019;24:1149.","journal-title":"Molecules"},{"key":"1265_CR48","doi-asserted-by":"crossref","first-page":"e0191889","DOI":"10.1371\/journal.pone.0191889","volume":"13","author":"DC Caixeta","year":"2018","unstructured":"Caixeta DC, Teixeira RR, Peixoto LG, Machado HL, Baptista NB, Souza AV, SalmenEspindola F. Adaptogenic potential of royal jelly in liver of rats exposed to chronic stress. PLoS ONE. 2018;13:e0191889.","journal-title":"PLoS ONE"},{"key":"1265_CR49","doi-asserted-by":"crossref","first-page":"606","DOI":"10.1016\/j.reprotox.2006.05.001","volume":"22","author":"SD Sarkar","year":"2006","unstructured":"Sarkar SD, Maiti R, Ghosha D. Management of fluoride induced testicular disorders by calcium and vitamin-E Co-administration in the albino rat. Reproduct Toxicol. 2006;22:606\u201312.","journal-title":"Reproduct Toxicol"},{"key":"1265_CR50","first-page":"2","volume":"22","author":"NJ Chinoy","year":"1989","unstructured":"Chinoy NJ, Ahmedabad ES. Fluoride induced biochemical changes in reproductive organs of male mice. Fluoride. 1989;22:2.","journal-title":"Fluoride"},{"key":"1265_CR51","doi-asserted-by":"crossref","first-page":"80","DOI":"10.3109\/19396368.2013.852271","volume":"60","author":"FD Kasmaie","year":"2014","unstructured":"Kasmaie FD, Malekinejad H, Khoramjouy M, Rezaei-Golmisheh A, Acyabar HJ. Royal jelly protects from taxol-\u0131nduced testicular damages via improvement of antioxidant status and up-regulation of E2f1. Syst Biol Repr Med. 2014;60:80\u20138.","journal-title":"Syst Biol Repr Med"},{"key":"1265_CR52","first-page":"155","volume":"23","author":"AA Hassan","year":"2009","unstructured":"Hassan AA. Effect of royal jelly on sexual efficiency in adult male rats, Iraqi. J Vet Sci. 2009;23:155\u201360.","journal-title":"J Vet Sci"},{"key":"1265_CR53","first-page":"174","volume":"42","author":"J Wang","year":"2009","unstructured":"Wang J, Zhang Y, Zhang H, Zhang K, Zhang Z, Lanzhou JL. Toxic effects of fluoride on reproductive ability in male rats: Sperm motility, oxidative stress, cell cycle, and testicular apoptosis. Res Rep. 2009;42:174\u20138.","journal-title":"Res Rep"},{"key":"1265_CR54","first-page":"519","volume":"14","author":"E Ghanbari","year":"2016","unstructured":"Ghanbari E, Nejati V, Khazaei M. Antioxidant and protective effects of royal jelly on histopathological changes in testis of diabetic rats. Int J Rep BioMed. 2016;14:519\u201326.","journal-title":"Int J Rep BioMed"},{"key":"1265_CR55","first-page":"e12996","volume":"50","author":"MA Mohamed","year":"2018","unstructured":"Mohamed MA, Samir AE, Alkafafy ME, Mohamed AA, Mousa AA. Protective potential of royal jelly against cadmium-induced infertility in male rats. Andrologia. 2018;50:e12996.","journal-title":"Andrologia"},{"key":"1265_CR56","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/j.cbi.2010.07.011","volume":"188","author":"O Barbier","year":"2010","unstructured":"Barbier O, Arreola-Mendoza L, Del Razoa LM. Molecular mechanisms of fl\u00fcoride toxicity. Chem-Biol Interac. 2010;188:319\u201333.","journal-title":"Chem-Biol Interac"},{"key":"1265_CR57","first-page":"116","volume":"45","author":"VR Mandava","year":"2012","unstructured":"Mandava VR, Rajendra NB. Protective effect of melatonin on fluoride-induced oxidative stress and testicular dysfunction in rats. Res Rep. 2012;45:116\u201324.","journal-title":"Res Rep"},{"key":"1265_CR58","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1007\/s00204-017-2054-2","volume":"92","author":"S Zilong","year":"2018","unstructured":"Zilong S, Sujuan L, Yuxiang Y, Hongyu C, Mohammad MO, Ram KM, Ruiyan N, Jundong W. Alterations in epididymal proteomics and antioxidant activity of mice exposed to fluoride. Arch Toxicol. 2018;92:169\u201380.","journal-title":"Arch Toxicol"},{"key":"1265_CR59","doi-asserted-by":"crossref","first-page":"268","DOI":"10.5530\/ajbls.2020.9.41","volume":"9","author":"CV Chalapathy","year":"2020","unstructured":"Chalapathy CV, Chatterjee A, Jayaramaiah U, Shivasharanappa K, Hanchinalmath JV, Patil SJ. Impact of royal jelly on infertility: A review. Asian J Biol Life Sci. 2020;9:268\u201373.","journal-title":"Asian J Biol Life Sci"},{"key":"1265_CR60","doi-asserted-by":"crossref","first-page":"1286","DOI":"10.1089\/jmf.2008.0203","volume":"12","author":"K Cavusoglu","year":"2009","unstructured":"Cavusoglu K, Yapar K, Yalcin E. Royal jelly (honey bee) is a potential antioxidant against cadmium-induced genotoxicity and oxidative stress in albino mice. J of Med Food. 2009;12:1286\u201392.","journal-title":"J of Med Food"},{"key":"1265_CR61","first-page":"183","volume":"27","author":"F Alt\u0131ndag","year":"2021","unstructured":"Alt\u0131ndag F, Ozdek U. Protective effects of chitosan and chitosan oligosaccharide on sodium fluoride-\u0131nduced testicular damage in male rats: A stereological and histopathological study. Kafkas Univ J Vet Fak. 2021;27:183\u20139.","journal-title":"Kafkas Univ J Vet Fak"},{"key":"1265_CR62","first-page":"231","volume":"9","author":"F Azad","year":"2018","unstructured":"Azad F, Nejati V, Shalizar-Jalali A, Najafi G, Rahmani F. Royal jelly protects male mice against nicotine-induced reproductive failure. Vet Res Forum. 2018;9:231\u20138.","journal-title":"Vet Res Forum"},{"key":"1265_CR63","doi-asserted-by":"crossref","first-page":"21524","DOI":"10.1007\/s11356-019-05521-3","volume":"26","author":"HG Tohamy","year":"2019","unstructured":"Tohamy HG, Dina RG, Yasser SE. Attenuation potentials of royal jelly against hydroxyurea-induced infertility through inhibiting oxidation and release of pro-inflammatory cytokines in male rats. Environ Sci Pollut Res Int. 2019;26:21524\u201334.","journal-title":"Environ Sci Pollut Res Int"},{"key":"1265_CR64","unstructured":"Connett M. Fluoride\u2019s effect on male reproductive system: Animal studies. Fluoride Action Network. 2012."},{"key":"1265_CR65","first-page":"113","volume":"9","author":"G Elham","year":"2015","unstructured":"Elham G, Nejati V, Najafi G, Khazaei M, Babaei M. Study on the effect of royal jelly on reproductive parameters in streptozotocin-induced diabetic rats. Int J of Fert Ster. 2015;9:113\u201320.","journal-title":"Int J of Fert Ster"},{"key":"1265_CR66","first-page":"141","volume":"13","author":"S Y\u0131ld\u0131r\u0131m","year":"2018","unstructured":"Y\u0131ld\u0131r\u0131m S, Belhan S, Uyar H, Huyut Z, Oto G, Saglam YS. Effects of chronically exposure to flor and 7,12-dimethylbenzanthracene (DMBA) on spermatogenesis and testicular histopathology in rats. Atat\u00fcrk Univ J Vet Sci. 2018;13:141\u20138.","journal-title":"Atat\u00fcrk Univ J Vet Sci"},{"key":"1265_CR67","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1080\/19390211.2017.1363843","volume":"15","author":"M Khazaei","year":"2018","unstructured":"Khazaei M, Ansarian A, Ghanbari E. New findings on biological actions and clinical applications of royal jelly: A review. J Dietary Suppl. 2018;15:757\u201375.","journal-title":"J Dietary Suppl"},{"key":"1265_CR68","first-page":"108","volume":"44","author":"CI Pavel","year":"2011","unstructured":"Pavel CI, Al L, Marghitas O, Bobis DS, Dezmirean IRA, Sapcaliu NMM. Biological activities of royal jelly-review, scientific papers. Animal Sci Biotechnol. 2011;44:108\u201318.","journal-title":"Animal Sci Biotechnol"},{"key":"1265_CR69","first-page":"181","volume":"22","author":"Y Sullu","year":"2006","unstructured":"Sullu Y, Kandemir B, Y\u0131ld\u0131z L, Karagoz F, Bar\u0131s S, Ayd\u0131n O. p53 and bcl-2 expression in testicular germ cell tumors, Turkish. J Pathol. 2006;22:181\u20136.","journal-title":"J Pathol"},{"key":"1265_CR70","first-page":"644","volume":"31","author":"A Aslan","year":"2021","unstructured":"Aslan A, Beyaz S, Gok O, Can MI, Parlak G, Ozercan IH, Gundogdu R. Royal jelly abrogates flouride induced oxidative damage in rat heart tissue by activating of the Nrf-2\/NF-\u039ab and Bcl-2\/Bax pathway. Tox Mech and Met. 2021;31:644\u201354.","journal-title":"Tox Mech and Met"},{"key":"1265_CR71","doi-asserted-by":"crossref","first-page":"10547","DOI":"10.1007\/s11356-021-16456-z","volume":"29","author":"A Aslan","year":"2021","unstructured":"Aslan A, Can MI, Gok O, Beyaz S, Parlak G, Ozercan IH. The inducing of caspase and bcl-2 pathway with royal jelly decreases the muscle tissue damage exposed with fluoride in rats. Envir Sci and Pol Res. 2021;29:10547\u201357.","journal-title":"Envir Sci and Pol Res"},{"key":"1265_CR72","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1002\/ijc.24064","volume":"124","author":"S Fulda","year":"2009","unstructured":"Fulda S. Tumor resistance to apoptosis. Inter J Canc. 2009;124:511\u20135.","journal-title":"Inter J Canc"},{"key":"1265_CR73","first-page":"11","volume":"1","author":"F Canpolat","year":"2016","unstructured":"Canpolat F. Cell cycle and apoptosis. Current J Dermatolog. 2016;1:11\u20137.","journal-title":"Current J Dermatolog"},{"key":"1265_CR74","doi-asserted-by":"crossref","first-page":"782","DOI":"10.1016\/j.ijbiomac.2019.01.210","volume":"128","author":"MM Abu-Serie","year":"2019","unstructured":"Abu-Serie MM, NohaH H. Two purified proteins from royal jelly with in vitro dual antihepatic damage potency, Major royal jelly protein 2 and its novel isoform X1. Int J of Biol Macr. 2019;128:782\u201395.","journal-title":"Int J of Biol Macr"},{"key":"1265_CR75","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1007\/s12011-018-1364-4","volume":"187","author":"H Wang","year":"2019","unstructured":"Wang H, Zhang R, Song Y, Li T, Ge M. Protective effect of ganoderma triterpenoids on cadmium-induced testicular toxicity in chickens. Biol Trace El Res. 2019;187:281\u201390.","journal-title":"Biol Trace El Res"},{"key":"1265_CR76","doi-asserted-by":"crossref","first-page":"24048","DOI":"10.1007\/s11356-020-08791-4","volume":"27","author":"M Arab-NozariMilad","year":"2020","unstructured":"Arab-NozariMilad M, Ebrahim M, Shokrzadeh M, Ahangar N, TalebpourAmiri F, Shaki F. Co-exposure to non-toxic levels of cadmium and fluoride induces hepatotoxicity in rats via triggering mitochondrial oxidative damage, apoptosis, and NF-kB pathways. Envir Sci Poll Res. 2020;27:24048\u201358.","journal-title":"Envir Sci Poll Res"},{"key":"1265_CR77","first-page":"36","volume":"3","author":"M Akdogan","year":"2018","unstructured":"Akdogan M, Yontem M. Cytokines, Online Turkish. J Health Sci. 2018;3:36\u201345.","journal-title":"J Health Sci"},{"key":"1265_CR78","first-page":"495","volume":"47","author":"K Ozoran","year":"1994","unstructured":"Ozoran K, Tulek N, Duzgun N. Romatoid artrit (RA) ve sitokinler: Interl\u00f6kin-1 (Il-1), nterl\u00f6kin-6 (Il-6), tumor necrosis factor alpha (TNF-a) ve interferon gama (IFN-y). J Fac Med. 1994;47:495\u2013504.","journal-title":"J Fac Med"},{"key":"1265_CR79","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1210\/endo.133.1.8319585","volume":"133","author":"SK De","year":"1993","unstructured":"De SK, Chen HL, Pace JL, Hunt JS, Terranova PF, Enders GC. Expression of tumor necrosis factor-alpha in mouse spermatogenic cells. Endocrinology. 1993;133:389\u201396.","journal-title":"Endocrinology"},{"key":"1265_CR80","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/0165-0378(93)90027-F","volume":"23","author":"JC Hutson","year":"1993","unstructured":"Hutson JC. Secretion of tumor necrosis factor alpha by testicular macrophages. J Reprod Immun. 1993;23:63\u201372.","journal-title":"J Reprod Immun"},{"key":"1265_CR81","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1210\/endo.134.1.8275970","volume":"134","author":"C Moore","year":"1994","unstructured":"Moore C, Hutson JC. Physiological relevance of tumor necrosis factor in mediating macrophage-Leydig cell interactions. Endocrinology. 1994;134:63\u20139.","journal-title":"Endocrinology"},{"key":"1265_CR82","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1006\/bbrc.1996.1077","volume":"224","author":"C Mauduit","year":"1996","unstructured":"Mauduit C, Besset V, Caussanel V, Benahmed M. Tumor necrosis factor \u03b1 receptor p55 is under hormonal (follicle-stimulating hormone) control in testicular Sertoli cells. Bioch Bioph Res Communication. 1996;224:631\u20137.","journal-title":"Bioch Bioph Res Communication"},{"key":"1265_CR83","doi-asserted-by":"crossref","first-page":"826","DOI":"10.1016\/j.chemosphere.2018.08.009","volume":"211","author":"X He","year":"2018","unstructured":"He X, Sun Z, Manthari RK, Wu P, Wang J. Fluoride altered rat\u2019s blood testis barrier by affecting the F-actin via IL-1a. Chemosphere. 2018;211:826\u201333.","journal-title":"Chemosphere"},{"key":"1265_CR84","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1016\/j.apjr.2015.07.005","volume":"4","author":"S Thangapandiyan","year":"2015","unstructured":"Thangapandiyan S, Miltonprabu S. Epigallocatechin gallate exacerbates fl\u00fcoride induced oxidative stress mediated testicular toxicity in rats through the activation of Nrf 2 signaling pathway. As Pac J Repro. 2015;4:272\u201387.","journal-title":"As Pac J Repro"},{"key":"1265_CR85","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1477-7827-2-1","volume":"2","author":"JJ Lysiak","year":"2004","unstructured":"Lysiak JJ. The role of tumor necrosis factor-alpha and interleukin-1 in the mammalian testis and their involvement in testicular torsion and autoimmune orchitis. Repr Biol Endocr. 2004;2:1\u201310.","journal-title":"Repr Biol Endocr"},{"key":"1265_CR86","doi-asserted-by":"crossref","first-page":"3979","DOI":"10.3390\/ijms19123979","volume":"19","author":"RS Almeer","year":"2018","unstructured":"Almeer RS, Soliman D, Kassab RB, AlBasher GI, Alarifi S, Alkahtani S, Ali D, Metwally D, Abdel Moneim AE. Royal jelly abrogates cadmium-induced oxidative challenge in mouse testes: Involvement of the Nrf2 pathway. Inter J Mol Sci. 2018;19:3979.","journal-title":"Inter J Mol Sci"},{"key":"1265_CR87","first-page":"1008","volume":"41","author":"Z Aslan","year":"2015","unstructured":"Aslan Z, Aksoy L. Anti-inflammatory effects of royal jelly on ethylene glycol induced renal inflammation in rats, Inter. Brazilian J. of. Urology. 2015;41:1008\u201313.","journal-title":"Urology"},{"key":"1265_CR88","doi-asserted-by":"crossref","first-page":"118382","DOI":"10.1016\/j.lfs.2020.118382","volume":"259","author":"S Kucukler","year":"2020","unstructured":"Kucukler S, Darendelioglu E, Caglayan C, Ayna A, Y\u0131ld\u0131r\u0131m S, Kandemir FM. Zingerone attenuates vancomycin-induced hepatotoxicity in rats through regulation of oxidative stress, inflammation and apoptosis. Life Sci. 2020;259:118382.","journal-title":"Life Sci"},{"key":"1265_CR89","first-page":"158","volume":"14","author":"JS Aprioku","year":"2013","unstructured":"Aprioku JS. Pharmacology of free radicals and the impact of reactive oxygen species on the testis. J of Repr & Inf. 2013;14:158.","journal-title":"J of Repr & Inf"},{"key":"1265_CR90","first-page":"111190","volume":"138","author":"FM Kandemir","year":"2020","unstructured":"Kandemir FM, Y\u0131ld\u0131r\u0131m S, Kucukler S, Caglayan C, Darendelio\u011flu E, Dortbudak MB. Protective effects of morin against acrylamide-induced hepatotoxicity and nephrotoxicity: A multi-biomarker approach. FCT. 2020;138:111190.","journal-title":"FCT"},{"key":"1265_CR91","first-page":"83","volume":"9","author":"S Comakl\u0131","year":"2020","unstructured":"Comakl\u0131 S, Ileriturk M, Kirman EM. Protective effects of rutin on oxidative DNA damage, NF-\u03baB-mediated \u0131nflammation, and apoptosis in colistin-induced testicular damage of rats. Tr J Nature Sci. 2020;9:83\u201390.","journal-title":"Tr J Nature Sci"},{"key":"1265_CR92","doi-asserted-by":"crossref","first-page":"552","DOI":"10.1007\/s12011-019-01946-6","volume":"196","author":"J Kumar","year":"2020","unstructured":"Kumar J, Haldar C, Verma R. Fluoride compromises testicular redox sensor, gap junction protein, and metabolic status: amelioration by melatonin. Biol Trace Element Res. 2020;196:552\u201364.","journal-title":"Biol Trace Element Res"},{"key":"1265_CR93","doi-asserted-by":"crossref","first-page":"80192","DOI":"10.18632\/oncotarget.19006","volume":"8","author":"Q Luo","year":"2017","unstructured":"Luo Q, Cui H, Deng H, Kuang P, Liu H, Lu Y, Fang J, Zuo Z, Deng J, Li Y, Wang X, Zhao L. Sodium fluoride induces renal inflammatory responses by activating NF-\u03baB signaling pathway and reducing antiinflammatory cytokine expression in mice. Oncotarget. 2017;8:80192\u2013207.","journal-title":"Oncotarget"},{"key":"1265_CR94","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1172\/JCI11830","volume":"107","author":"PP Tak","year":"2001","unstructured":"Tak PP, Firestein GS. NF-\u03baB: a key role in inflammatory diseases. J Clin Invest. 2001;107:7\u201311.","journal-title":"J Clin Invest"},{"key":"1265_CR95","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1038\/ncb1086","volume":"6","author":"T Bouwmeester","year":"2004","unstructured":"Bouwmeester T, Bauch A, Ruffner H, Angrand PO, Bergamini G, Croughton K, Cruciat C, Eberhard D, Gagneur J, Ghidelli S. A physical and functional map of the human TNF-\u03b1\/NF-\u03baB signal transduction pathway. Nat Cell Biol. 2004;6:97\u2013105.","journal-title":"Nat Cell Biol"},{"key":"1265_CR96","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1016\/j.smim.2014.05.004","volume":"26","author":"MS Hayden","year":"2014","unstructured":"Hayden MS, Ghosh S. Regulation of NF-\u03baB by TNF family cytokines. Semin Immunol. 2014;26:253\u201366.","journal-title":"Semin Immunol"},{"key":"1265_CR97","first-page":"624","volume":"127","author":"T Shabab","year":"2017","unstructured":"Shabab T, Khanabdali R, Moghadamtousi SZ, Kadir HA, Mohan G. Neuroinflammation pathways: A general review, Inter. J Neurosci. 2017;127:624\u201333.","journal-title":"J Neurosci"},{"key":"1265_CR98","doi-asserted-by":"crossref","first-page":"5825","DOI":"10.1038\/s41598-019-42368-7","volume":"9","author":"RS Almeer","year":"2019","unstructured":"Almeer RS, Ialbasher G, Alarif S, Alkahtani S, Ali D, Moneim AEA. Royal jelly attenuates cadmium induced nephrotoxicity in male mice. Sci Rep. 2019;9:5825.","journal-title":"Sci Rep"},{"key":"1265_CR99","doi-asserted-by":"crossref","first-page":"38658","DOI":"10.1074\/jbc.M106599200","volume":"276","author":"B Poligone","year":"2001","unstructured":"Poligone B, Baldwin AS. Positive and negative regulation of NF-\u03baB by COX-2 roles of different prostaglandins. J Biol Chem. 2001;276:38658\u201364.","journal-title":"J Biol Chem"},{"key":"1265_CR100","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1530\/REP-14-0392","volume":"149","author":"MB Frungieri","year":"2015","unstructured":"Frungieri MB, Calandra RS, Mayerhofer A, Matzkin ME. Cyclooxygenase and prostaglandins in somatic cell populations of the testis. Reproduction. 2015;149:169\u201380.","journal-title":"Reproduction"},{"key":"1265_CR101","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1111\/and.12423","volume":"48","author":"T Mostafa","year":"2016","unstructured":"Mostafa T, Rashed L, Taymour M. Seminal cyclooxygenase relationship with oxidative stress in infertile oligoasthenoteratozoospermic men with varicocele. Andrologia. 2016;48:137\u201342.","journal-title":"Andrologia"}],"container-title":["Reproductive Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s43032-023-01265-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s43032-023-01265-1\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s43032-023-01265-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,5]],"date-time":"2023-10-05T17:19:15Z","timestamp":1696526355000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s43032-023-01265-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5,12]]},"references-count":101,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2023,10]]}},"alternative-id":["1265"],"URL":"https:\/\/doi.org\/10.1007\/s43032-023-01265-1","relation":{},"ISSN":["1933-7191","1933-7205"],"issn-type":[{"value":"1933-7191","type":"print"},{"value":"1933-7205","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,5,12]]},"assertion":[{"value":"24 November 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 May 2023","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"12 May 2023","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"All rats used for this study were obtained by Firat University Experimental Animals Research Center (FUDAM, ethical committee number of this study: 02\/09\/2020, 2020\/12).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical Approval"}},{"value":"The authors declare consent to participate in this study.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Informed Consent"}},{"value":"The authors declare consent to publish this study.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for Publication"}},{"value":"No potential conflict of interest was reported by the authors.","order":5,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of Interest"}}]}}