Aryl Hydrocarbon Receptor Modulation and Resveratrol Influence on Dnah1 Expression: Implications for Male Reproductive Health

Main Article Content

Ghadeer Sabah Bustani
Nabil Al-Humadi
Hasan F.K. Alghetaa

Abstract

Male reproductive health is intricately regulated by molecular and physiological processes, with the aryl hydrocarbon receptor (AhR) playing a crucial role. AhR is activated by various ligands and influences the onset and progression of diseases. The aim of this study was to evaluate the role of AhR on spermatogenesis in adult male rats were affected by resveratrol (RES) and CH223191, an AhR antagonist. The study include forty rats were randomly divided into four equal groups: Control group, DMSO group, RES group and AhR‾ group, the rats received respective treatments intraperitoneally twice weekly for 60 days, and various parameters related to male reproductive health were evaluated. The AhR that activation by the RES treatment were enhanced the sperm morphology, sperm acrosomal integrity and luteinizing hormone. Moreover, the Dnah1 gene expression, is has play major role in sperm morphology, was upregulated and testosterone levels were elevated by RES. On the other hand, sperm morphology, sperm acrosomal integrity, testosterone hormone levels, and Dnah1 expression were all reduced in AhR‍ rats. The testicular tissue integrity was maintained by RES, according to a histopathological analysis. These findings highlight the role of AhR in male reproductive health and suggest RES as a potential therapeutic agent.

Downloads

Download data is not yet available.

Article Details

How to Cite
Aryl Hydrocarbon Receptor Modulation and Resveratrol Influence on Dnah1 Expression: Implications for Male Reproductive Health. (2024). The Iraqi Journal of Veterinary Medicine, 48(1), 15-24. https://doi.org/10.30539/p5wv8002
Section
Articles
Author Biographies

Ghadeer Sabah Bustani, The Islamic University

Head of Department of Anesthesia Techniquesin the Islamic University Najaf

Hasan F.K. Alghetaa, Department of Physiology, Biochemistry and Pharmacology, College of Veterinary Medicine, University of Baghdad, Baghdad, Iraq

Head of Physiology, Biochemistry and Pharmacology in College of Veterinary medicine in Baghdad University

How to Cite

Aryl Hydrocarbon Receptor Modulation and Resveratrol Influence on Dnah1 Expression: Implications for Male Reproductive Health. (2024). The Iraqi Journal of Veterinary Medicine, 48(1), 15-24. https://doi.org/10.30539/p5wv8002

References

Bustani GS, Baiee FH. Semen extenders: An evaluative overview of preservative mechanisms of semen and semen extenders. Vet World. 2021;14(5):1220. https://doi.org/10.14202/vetworld.2021.1220-1233

Esakky P, Hansen DA, Drury AM, Moley KH. Cigarette smoke condensate induces aryl hydrocarbon receptor-dependent changes in gene expression in spermatocytes. Reprod. Toxicol. 2012;34(4):665–76. https://doi.org/10.1016/j.reprotox.2012.10.005

Abbott BD, Schmid JE, Pitt JA, Buckalew AR, Wood CR, Held GA, Diliberto JJ. Adverse reproductive outcomes in the transgenic Ah receptor-deficient mouse. Toxicol Appl Pharmacol. 1999;155(1):62–70. https://doi.org/10.1006/taap.1998.8601

Wang SY, Cheng YY, Liu SC, Xu YX, Gao Y, Wang CL, Wang ZG, Feng TQ, Lu GH, Song J. A synonymous mutation in IGF-1 impacts the transcription and translation process of gene expression. Mol. Ther Nucleic Acids. 2021;26:1446–65. https://doi.org/10.1016/j.omtn.2021.08.007

Alghetaa H, Mohammed A, Sultan M, Busbee P, Murphy A, Chatterjee S, et al. Resveratrol protects mice against SEB‐induced acute lung injury and mortality by miR‐193a modulation that targets TGF‐β signalling. J Cell Mol Med. 2018;22(5):2644–55. https://doi.org/10.1111/jcmm.13542

Levine-Fridman A, Chen L, Elferink CJ. Cytochrome P4501A1 promotes G1 phase cell cycle progression by controlling aryl hydrocarbon receptor activity. Mol Pharmacol. 2004;65(2):461–9.:https://doi.org/10.1124/mol.65.2.461

Wincent E, Bengtsson J, Bardbori AM, Alsberg T, Luecke S, Rannug U, et al. Inhibition of cytochrome P4501-dependent clearance of the endogenous agonist FICZ as a mechanism for activation of the aryl hydrocarbon receptor Proc Natl Acad Sci. 2012;109(12):4479–84. https://doi.org/10.1073/pnas.1118467109

Pinne M, Raucy JL. Cytochrome P450 Gene Regulation: Reporter Assays to Assess Aryl Hydrocarbon Receptor (HLHE76, AhR) Activation and Antagonism. In: Cytochrome P450. Springer; 2021. p. 157–74. https://doi.org/10.1007/978-1-0716-1542-3_10

Zhang J, Gao X, Yu L. Roles of histone deacetylases in acute myeloid leukemia with fusion proteins. Front Oncol. 2021;11:741746.https://doi.org/10.3389/fonc.2021.741746

Wang LT, Chiou SS, Chai CY, Hsi E, Wang SN, Huang SK, et al. Aryl hydrocarbon receptor regulates histone deacetylase 8 expression to repress tumor suppressive activity in hepatocellular carcinoma. Oncotarget. 2017;8(5):7489. https://doi.org/10.18632/oncotarget.9841

Garrison PM, Rogers JM, Brackney WR, Denison MS. Effects of histone deacetylase inhibitors on the Ah receptor gene promoter. Arch Biochem Biophys. 2000;374(2):161–71.https://doi.org/10.1006/abbi.1999.1620

Tsai CH, Li CH, Liao PL, Chang YW, Cheng YW, Kang JJ,et al. Aza-PBHA, a potent histone deacetylase inhibitor, inhibits human gastric-cancer cell migration via PKCα-mediated AHR-HDAC interactions. Biochim Biophys Acta Mol Cell Res. 2020;1867(2):118564. https://doi.org/10.1016/j.bbamcr.2019.118564

Abdulla JM, Al-Okaily BN. Histomorphometric and histopathological alterations of rat testis following exposure to hydrogen‎ peroxide: Protective role of resveratrol supplement. Iraqi J. Vet. Med.2022;46(1):17–23. https://doi.org/10.30539/ijvm.v46i1.1313

Longobardi V, Zullo G, Salzano A, De Canditiis C, Cammarano A, De Luise L, Puzio MV, Neglia G, Gasparrini B. Resveratrol prevents capacitation-like changes and improves in vitro fertilizing capability of buffalo frozen-thawed sperm. Theriogenology. 2017;88:1–8. https://doi.org/10.1016/j.theriogenology.2016.09.046

Aghetaa HFK, Dawood RA, Aladhami AK. Resveratrol Administration Ameliorates Hepatotoxicity in Mercuric Chloride-‎ Induced Liver Injury in Rats. Iraqi J. Vet. Med. 2023;47(2):1–8. https://doi.org/10.30539/ijvm.v47i2.1482

Huang Y, Zhang J, Tao Y, Ji C, Aniagu S, Jiang Y, Chen T. AHR/ROS-mediated mitochondria apoptosis contributes to benzo [a] pyrene-induced heart defects and the protective effects of resveratrol. Toxicology. 2021;462:152965. https://doi.org/10.1016/j.tox.2021.152965

Abdulla OA, Neamah W, Sultan M, Alghetaa HK, Singh N, Busbee PB, et al . The ability of AhR ligands to attenuate delayed type hypersensitivity reaction is associated with alterations in the gut microbiota. Front Immunol. 2021;12:684727.https://doi.org/10.3389/fimmu.2021.684727

Bordbar H, Yahyavi SS, Noorafshan A, Aliabadi E, Naseh M. Resveratrol ameliorates bisphenol A-induced testicular toxicity in adult male rats: a stereological and functional study. Basic Clin Androl. 2023;33(1):1. https://doi.org/10.1186/s12610-022-00174-8

Cao W, Lu J, Li L, Qiu C, Qin X, Wang T, et al. Activation of the Aryl Hydrocarbon Receptor Ameliorates Acute Rejection of Rat Liver Transplantation by Regulating Treg Proliferation and PD-1 Expression. Transplantation. 2022;106(11):2172–81. https://doi.org/10.1097/TP.0000000000004205

Ngaha Njila MI, Massoma Lembè D, Koloko BL, Yong Meng G, Ebrahimi M, Awad EA, et al. Sperm parameters quality and reproductive effects of methanolic extract of Alchornea cordifolia leaves on senescent male rats. Andrologia. 2019;51(9):e13359. https://doi.org/10.1111/and.13359

Al-Ghetaa HFK. Effect of Environmental High Temperature on the Reproductive activity of Awassi Ram Lambs. Iraqi J. Vet. Med. 2012; 36(2), 244-253. https://doi.org/10.30539/iraqijvm.v36i2.502

Kaka A, Wahid H, Rosnina Y, Yimer N, Khumran AM, Sarsaifi K, et al. α-Linolenic acid supplementation in BioXcell® extender can improve the quality of post-cooling and frozen-thawed bovine sperm. Anim Reprod Sci. 2015;153:1–7. 10.1016/j.anireprosci.2014.12.001.

Mulero-Navarro S, Fernandez-Salguero PM. New trends in aryl hydrocarbon receptor biology. Front Cell Dev Biol. 2016;4:45. Doi: 10.3389/fcell.2016.00045.

Larigot L, Juricek L, Dairou J, Coumoul X. AhR signaling pathways and regulatory functions. Biochim Open. 2018;7:1–9. https://doi.org/10.1016/j.anireprosci.2014.12.001

Komulainen E, Varidaki A, Kulesskaya N, Mohammad H, Sourander C, Rauvala H, et al. Impact of JNK and its substrates on dendritic spine morphology. Cells. 2020;9(2):440. https://doi.org/10.3390/cells9020440

Shaito A, Posadino AM, Younes N, Hasan H, Halabi S, Alhababi D, et al. Potential adverse effects of resveratrol: A literature review. Int J Mol Sci. 2020;21(6). https://doi.org/10.3390/ijms21062084

Revel A, Raanani H, Younglai E, Xu J, Han R, Savouret JF, et al. Resveratrol, a natural aryl hydrocarbon receptor antagonist, protects sperm from DNA damage and apoptosis caused by benzo (a) pyrene. Reprod Toxicol. 2001;15(5):479–86. https://doi.org/10.1016/S0890-6238(01)00149-6

Alghetaa H, Mohammed A, Sultan M, Busbee P, Murphy A, Chatterjee S, et al. Resveratrol protects mice against SEB-induced acute lung injury and mortality by miR-193a modulation that targets TGF-β signalling. J Cell Mol Med. 2018;22(5):2644-2655. https://doi.org/10.1111/jcmm.13542

Barroso G, Valdespin C, Vega E, Kershenovich R, Avila R,et al . Developmental sperm contributions: fertilization and beyond. Fertility and sterility, 2009; 92(3), 835-848.‏ https://doi.org/10.1016/j.fertnstert.2009.06.030

Bustani GS, Jabbar MK, AL-Baghdady HF, Al-Dhalimy AMB. Protective effects of curcumin on testicular and sperm parameters abnormalities induced by nicotine in male rats. In: AIP Conference Proceedings. 2022; 2386(1); article id.020042. https://doi.org/10.1063/5.0066855

Hansen DA, Esakky P, Drury A, Lamb L, Moley KH. The aryl hydrocarbon receptor is important for proper seminiferous tubule architecture and sperm development in mice. Biol Reprod. 2014;90(1):1–8. https://doi.org/10.1095/biolreprod.113.108845

Esakky, P., Moley, K. Preventing germ cell death by inactivating aryl hydrocarbon receptor (AHR). Cell Death Dis. 2016; 7, e2116.: https://doi.org/10.1038/cddis.2016.20

Serra L, Bourdon G, Estienne A, Fréville M, Ramé C, Chevaleyre C, et al. Triazole pesticides exposure impaired steroidogenesis associated to an increase in AHR and CAR expression in testis and altered sperm parameters in chicken. Toxicol Rep. 2023; 10:409–27. https://doi.org/10.1016/j.toxrep.2023.03.005

Hashemi M, Azarnia M, Hajebrahimi Z, Ebrahimi SN. The effect of hydroalcoholic extract of Cichorium intybus leaf on aryl hydrocarbon receptor expression in the testis of Wistar rats exposed to cigarette smoke. Avicenna J Phytomed. 2023;13(1):58. Doi: 10.22038/AJP.2022.21307.

Vannucchi CI, Angrimani D de SR, Eyherabide AR, Mazzei CP, Lucio C de F, Maiorka PC, et al. Effects of intratesticular administration of zinc gluconate and dimethyl sulfoxide on clinical, endocrinological, and reproductive parameters in dogs. Theriogenology. 2015;84(7):1103–10. https://doi.org/10.1016/j.theriogenology.2015.06.005

Bordbar H, Yahyavi SS, Noorafshan A, Aliabadi E, Naseh M. Resveratrol ameliorates bisphenol A-induced testicular toxicity in adult male rats: a stereological and functional study. Basic Clin Androl. 2023;33(1):1 https://doi.org/10.1186/s12610-022-00174-8

Shin S, Jeon JH, Park D, Jang MJ, Choi JH, Choi BH, et al. trans-Resveratrol relaxes the corpus cavernosum ex vivo and enhances testosterone levels and sperm quality in vivo. Arch Pharm Res. 2008;31:83–7. https://doi.org/10.1007/s12272-008-1124-7

Korkina, Liudmila G, Wolfgang Mayer, Chiara De Luca. Meristem plant cells as a sustainable source of redox actives for skin rejuvenation. Biomolecules 2017;7(2):40 https://doi.org/10.3390/biom7020040

Sainz-Urruela C, Vera-López S, San Andrés MP, Díez-Pascual AM. Graphene-based sensors for the detection of bioactive compounds: A review. Int J Mol Sci. 2021;22(7):3316.https://doi.org/10.3390/ijms22073316

Huang B, Butler R, Miao Y, Dai Y, Wu W, et al. Dysregulation of Notch and ERα signaling in AhR−/− male mice. PNAS. 2016;113(42):11883–8. https://doi.org/10.1073/pnas.1613269113

Meng X, Zhou J, Zhao CN, Gan RY, Li HB. Health benefits and molecular mechanisms of resveratrol: a narrative review. Foods. 2020;9(3):340. https://doi.org/10.3390/foods9030340

Wu Y, Baumgarten SC, Zhou P, Stocco C. Testosterone-dependent interaction between androgen receptor and aryl hydrocarbon receptor induces liver receptor homolog 1 expression in rat granulosa cells. Mol Cell Biol. 2013;33(15):2817–28. https://doi.org/10.1128/MCB.00011-13

Morita Y, Wada-Hiraike O, Yano T, Shirane A, Hirano M, Hiraike, et al. Resveratrol promotes expression of SIRT1 and StAR in rat ovarian granulosa cells: an implicative role of SIRT1 in the ovary. RB&E. 2012;10(1):1–10. https://doi.org/10.1186/1477-7827-10-14

Elsawy H, Famurewa AC, Sedky A. Resveratrol Mitigates Diabetic Testicular Dysfunction, Endocrine Deficits, and Insulin Resistance via Suppression of Sperm-Endocrine Aberrations and Oxidative Inflammation in Rats. Andrologia. 2023;2023.https://doi.org/10.1155/2023/6385767

Wang M, Yang QY, Zhou JP, Tan HP, Hu J, Jin L, et al. Novel compound heterozygous mutations in DNAH1 cause primary infertility in Han Chinese males with multiple morphological abnormalities of the sperm flagella. Asian J Androl. 2023;25(4):512–9. 10.4103/aja202292.

Jiang C, Zhang X, Zhang H, Guo J, Zhang C, Li J, et al. Novel bi-allelic mutations in DNAH1 cause multiple morphological abnormalities of the sperm flagella resulting in male infertility. Transl Androl Urol. 2021;10(4):1656. https://doi.org/10.5534/wjmh.210119

Zhuang BJ, Xu SY, Dong L, Zhang PH, Zhuang BL, Huang XP, et al. Novel DNAH1 mutation loci lead to multiple morphological abnormalities of the sperm flagella and literature review. World J Mens Health. 2022;40(4):551. https://doi.org/10.5534/wjmh.210119

Ghafouri-Fard S, Shoorei H, Mohaqiq M, Raza SHA, Taheri M. The role of different compounds on the integrity of blood-testis barrier: A concise review based on in vitro and in vivo studies. Gene. 2021;780:145531. https://doi.org/10.1016/j.gene.2021.145531

Balci A, Ozkemahli G, Erkekoglu P, Zeybek ND, Yersal N, Kocer-Gumusel B. Histopathologic, apoptotic and autophagic, effects of prenatal bisphenol A and/or di (2-ethylhexyl) phthalate exposure on prepubertal rat testis. Environmental Science and Pollution Research. 2020;27:20104–16. https://doi.org/10.1007/s11356-020-08274-6

Assefa EG, Yan Q, Gezahegn SB, Salissou MTM, He S, Wu N, et al. Role of resveratrol on indoxyl sulfate-induced endothelial hyperpermeability via aryl hydrocarbon receptor (AHR)/Src-dependent pathway. Oxid Med Cell Longev. 2019;2019. https://doi.org/10.1155/2019/5847040

Chi KK, Zhang WH, Chen Z, Cui Y, He W, Wang SG, et al. Comparison of quercetin and resveratrol in the prevention of injury due to testicular torsion/detorsion in rats. Asian J Androl. 2016;18(6):908. https://doi.org/10.4103/1008-682X.167720

Sener TE, Atasoy BM, Cevik O, Cilingir Kaya OT, Cetinel S, et al. Effects of resveratrol against scattered radiation-induced testicular damage in rats. Turkish Journal of Biochemistry. 2020;46(4):425–33. https://doi.org/10.1515/tjb-2020-0320

Gu T, Wang N, Wu T, Ge Q, Chen L. Antioxidative stress mechanisms behind resveratrol: a multidimensional analysis. J Food Qual. 2021;2021:1–12. https://doi.org/10.1155/2021/5571733

Amin GM, Marouf BH, Namiq H. The Effects of Resveratrol Supplementation on the Quality of Life of Diabetic Patients with Neuropathy: Small Randomized Clinical Trial. IJPS. 2023;32(3):118–27. https://doi.org/10.31351/vol32iss3pp118-127

Zhang W, Ou N, Liang Z, Hu R, Song Y, Yang Y, et al. Relationship between aryl hydrocarbon receptor and spermatogenic dysfunction in male patients with varicocele. Andrologia. 2020;52(11):e13792. https://doi.org/10.1111/and.13792

Alghetaa H, Mohammed A, Singh N, Wilson K, Cai G, Putluri N, et al. Resveratrol attenuates staphylococcal enterotoxin B-activated immune cell metabolism via upregulation of miR-100 and suppression of mTOR signaling pathway. Front Pharmacol. 2023;14:1106733. https://doi.org/10.3389/fphar.2023.1106733

Lee S, Gross SE, Pfaff H, Dresen A. Waiting time, communication quality, and patient satisfaction: an analysis of moderating influences on the relationship between perceived waiting time and the satisfaction of breast cancer patients during their inpatient stay. Patient Educ Couns. 2020;103(4):819–25. https://doi.org/10.1016/j.pec.2019.11.018