Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2022-0102
Animal Reproduction (AR)
ORIGINAL ARTICLE

Characterization of sperm motility and testosterone secretion in the taiep myelin mutant, a model of demyelination

Luz Patricia Muñoz de la Torre; Angélica Trujillo Hernández; José Ramón Eguibar; Carmen Cortés; Leticia Morales-Ledesma

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Abstract

Abstract: Presently, demyelinating diseases have been reported to affect the reproductive life of patients who suffer from them, but the progression of the alterations is unknown, especially in men. To better understand these effects, it is necessary to perform studies in animal models, such as the male taiep rat, which exhibits progressive demyelination of the central nervous system, altered kisspeptin expression at the hypothalamic level, and decreased luteinizing hormone, which could alter sperm quality and testicular diameter. Thus, the objective of the present study was to analyze the diameter of the seminiferous tubules, the sperm motility, and the testosterone levels of 90-day-old male taiep rats. The obtained results indicate that male taiep rats show an increase in testicular size accompanied by an increase in the diameter of the seminiferous tubules of the left testicle. There was also a decrease in progressive motility in sperm samples from the left epididymis of male taiep rats compared to the control group, with no changes in serum testosterone concentration. Therefore, we conclude that male taiep rats with central demyelination show altered testicular diameter and decreased motility in sperm from the left side. This type of studies serves as a basis for proposing possible reproductive strategies to improve the fertility and testicular function of men with demyelinating diseases of the central nervous system.

Keywords

demyelination, seminiferous tubules, testosterone, LH

References

Aziz NA, van der Marck MA, Pijl H, Olde Rikkert MGM, Bloem BR, Roos RAC. Weight loss in neurodegenerative disorders. J Neurol. 2008;255(12):1872-80. http://dx.doi.org/10.1007/s00415-009-0062-8. PMid:19165531.

Banczerowski P, Csaba Z, Csernus V, Gerendai I. Lesion of the insular cortex affects luteinizing hormone and testosterone secretion of rat. Brain Res. 2001;906(1-2):25-30. http://dx.doi.org/10.1016/S0006-8993(01)02540-9. PMid:11430858.

Bergamaschi R, Livieri C, Uggetti C, Candeloro E, Egitto MG, Pichiecchio A, Cosi V, Bastianello S. Brain white matter impairment in congenital adrenal hyperplasia. Arch Neurol. 2006;63(3):413-6. http://dx.doi.org/10.1001/archneur.63.3.413. PMid:16540460.

Bogaert AF. Genital asymmetry in men. Hum Reprod. 1997;12(1):68-72. http://dx.doi.org/10.1093/humrep/12.1.68. PMid:9043905.

Brown JL, Chakraborty PK. Comparison of compensatory pituitary and testicular responses to hemicastration between prepubertal and mature rats. J Androl. 1991;12(2):119-25. PMid:1904849.

Cannarella R, Condorelli RA, La Vignera S, Calogero AE. Effects of the insulin-like growth factor system on testicular differentiation and function: a review of the literature. Andrology. 2018;6(1):3-9. http://dx.doi.org/10.1111/andr.12444. PMid:29195026.

Cavalla P, Rovei V, Masera S, Vercellino M, Massobrio M, Mutani R, Revelli A. Fertility in patients with multiple sclerosis: current knowledge and future perspectives. Neurol Sci. 2006;27(4):231-9. http://dx.doi.org/10.1007/s10072-006-0676-x. PMid:16998725.

Chow S-H, Giglio W, Anesetti R, Ottenweller JE, Pogach LM, Huang HFS. The effects of testicular denervation on spermatogenesis in the sprague-dawley rat. Neuroendocrinology. 2000;72(1):37-45. http://dx.doi.org/10.1159/000054569. PMid:10940737.

D’Amico E, Zanghì A, Burgio G, Chisari CG, Condorelli RA, La Vignera S, Calogero AE, Patti F. Gonadal steroids and sperm quality in a cohort of relapsing remitting multiple sclerosis: a case-control study. Front Neurol. 2020;11:756. http://dx.doi.org/10.3389/fneur.2020.00756. PMid:32849215.

Djousse L, Knowlton B, Cupples LA, Marder K, Shoulson I, Myers RH. Weight loss in early stage of Huntington’s disease. Neurology. 2002;59(9):1325-30. http://dx.doi.org/10.1212/01.WNL.0000031791.10922.CF. PMid:12427878.

Duncan ID, Bugiani M, Radcliff AB, Moran JJ, Lopez-Anido C, Duong P, August BK, Wolf NI, van der Knaap MS, Svaren J. A mutation in the Tubb4a gene leads to microtubule accumulation with hypomyelination and demyelination. Ann Neurol. 2017;81(5):690-702. http://dx.doi.org/10.1002/ana.24930. PMid:28393430.

Duncan ID, Lunn KF, Holmgren B, Urba-Holmgren R, Brignolo-Holmes L. The taiep rat: a myelin mutant with an associated oligodendrocyte microtubular defect. J Neurocytol. 1992;21(12):870-84. http://dx.doi.org/10.1007/BF01191684. PMid:1469463.

Fernandez CDB, Porto EM, Arena AC, Kempinas WDG. Effects of altered epididymal sperm transit time on sperm quality. Int J Androl. 2008;31(4):427-37. http://dx.doi.org/10.1111/j.1365-2605.2007.00788.x. PMid:17822422.

Franek G, Bieniak M, Cieślik A. Quality of life in patients with multiple sclerosis. J Neurol Neurosurg. Nurs. 2019;8(3):95-101. http://dx.doi.org/10.15225/PNN.2019.8.3.1.

Frankel AI, Chapman JC, Cook B. Testes are asymmetric in the testicular hemicastration response of the male rat. J Endocrinol. 1989;122(2):485-8. http://dx.doi.org/10.1677/joe.0.1220485. PMid:2769166.

Garduno-Robles A, Alata M, Piazza V, Cortes C, Eguibar JR, Pantano S, Hernandez VH. MRI features in a rat model of H-ABC tubulinopathy. Front Neurosci. 2020;14:555. http://dx.doi.org/10.3389/fnins.2020.00555. PMid:32581692.

Gerendai I, Halász B. Asymmetry of the neuroendocrine system. News Physiol Sci. 2001;16(2):92-5. http://dx.doi.org/10.1152/physiologyonline.2001.16.2.92. PMid:11390957.

Glazer CH, Tøttenborg SS, Giwercman A, Bräuner EV, Eisenberg ML, Vassard D, Magyari M, Pinborg A, Schmidt L, Bonde JP. Male factor infertility and risk of multiple sclerosis: a register-based cohort study. Mult Scler. 2018;24(14):1835-42. http://dx.doi.org/10.1177/1352458517734069. PMid:29027840.

Han SY, Cheong I, McLennan T, Herbison AE. Neural determinants of pulsatile Luteinizing hormone secretion in male mice. Endocrinology. 2020;161(2):bqz045. http://dx.doi.org/10.1210/endocr/bqz045. PMid:31907531.

Holmgren B, Urbá-Holmgren R, Riboni L, Vega-SaenzdeMiera EC. Sprague Dawley rat mutant with tremor, ataxia, tonic immobility episodes, epilepsy and paralysis. Lab Anim Sci. 1989;39(3):226-8. PMid:2724922.

Huo S, Xu Z, Zhang X, Zhang J, Cui S. Testicular denervation in prepuberty rat inhibits seminiferous tubule development and spermatogenesis. J Reprod Dev. 2010;56(4):370-8. http://dx.doi.org/10.1262/jrd.10-009N. PMid:20424380.

Justulin LA Jr, Ureshino RP, Zanoni M, Felisbino SL. Differential proliferative response of the ventral prostate and seminal vesicle to testosterone replacement. Cell Biol Int. 2006;30(4):354-64. http://dx.doi.org/10.1016/j.cellbi.2006.01.002. PMid:16546411.

Laoung-On J, Saenphet K, Jaikang C, Sudwan P. Effect of moringa oleifera lam. Leaf tea on sexual behavior and reproductive function in male rats. Plants. 2021;10(10):2019. http://dx.doi.org/10.3390/plants10102019. PMid:34685828.

Lee S, Miselis R, Rivier C. Anatomical and functional evidence for a neural hypothalamic-testicular pathway that is independent of the pituitary. Endocrinology. 2002;143(11):4447-54. http://dx.doi.org/10.1210/en.2002-220392. PMid:12399442.

Leon Chavez BA, Guevara J, Galindo S, Luna J, Ugarte A, Villegas O, Mena R, Eguibar JR, Martinez-Fong D. Regional and temporal progression of reactive astrocytosis in the brain of the myelin mutant taiep rat. Brain Res. 2001;900(1):152-5. http://dx.doi.org/10.1016/S0006-8993(01)02284-3. PMid:11325359.

Lopez‐Juarez A, Gonzalez‐Vega A, Kleinert‐Altamirano A, Piazza V, Garduno‐Robles A, Alata M, Villaseñor‐Mora C, Eguibar JR, Cortes C, Padierna LC, Hernandez VH. Auditory impairment in H‐ABC tubulinopathy. J Comp Neurol. 2021;529(5):957-68. http://dx.doi.org/10.1002/cne.24990. PMid:32681585.

Lunn KF, Fanarraga ML, Duncan ID. Myelin mutants: new models and new observations. Microsc Res Tech. 1995;32(3):183-203. http://dx.doi.org/10.1002/jemt.1070320303. PMid:8527854.

Mendes NF, Gaspar JM, Lima-Júnior JC, Donato J Jr, Velloso LA, Araújo EP. TGF-β1 down-regulation in the mediobasal hypothalamus attenuates hypothalamic inflammation and protects against diet-induced obesity. Metabolism. 2018;85:171-82. http://dx.doi.org/10.1016/j.metabol.2018.04.005. PMid:29660453.

Milosevic A, Bjelobaba I, Bozic ID, Lavrnja I, Savic D, Tesovic K, Jakovljevic M, Stojilkovic SS, Janjic MM. Testicular steroidogenesis is suppressed during experimental autoimmune encephalomyelitis in rats. Sci Rep. 2021;11(1):8996. http://dx.doi.org/10.1038/s41598-021-88305-5. PMid:33903635.

Milosevic A, Janjic MM, Lavrnja I, Savic D, Bozic ID, Tesovic K, Jakovljevic M, Pekovic S, Stojilkovic SS, Bjelobaba I. The sex-specific patterns of changes in hypothalamic-pituitary-gonadal axis during experimental autoimmune encephalomyelitis. Brain Behav Immun. 2020;89:233-44. http://dx.doi.org/10.1016/j.bbi.2020.06.025. PMid:32592862.

Muñoz de la Torre LP, Trujillo Hernández A, Eguibar JR, Cortés C, Morales-Ledesma L. Sex-specific hypothalamic expression of kisspeptin, gonadotropin releasing hormone, and kisspeptin receptor in progressive demyelination model. J Chem Neuroanat. 2022;123:102120. http://dx.doi.org/10.1016/j.jchemneu.2022.102120. PMid:35718292.

ImageJ [online]. Bethesda: NIH; 2023 [cited 2023 Oct 9]. Available at: https://imagej.net/ij/index.html.

Nurmio M, Kallio J, Adam M, Mayerhofer A, Toppari J, Jahnukainen K. Peritubular myoid cells have a role in postnatal testicular growth. Spermatogenesis. 2012;2(2):79-87. PMid:22670217.

O’Connor LT, Goetz BD, Couve E, Song J, Duncan ID. Intracellular distribution of myelin protein gene products is altered in oligodendrocytes of the taiep rat. Mol Cell Neurosci. 2000;16(4):396-407. http://dx.doi.org/10.1006/mcne.2000.0889. PMid:11085877.

O’Shaughnessy PJ, Monteiro A, Verhoeven G, De Gendt K, Abel MH. Effect of FSH on testicular morphology and spermatogenesis in gonadotrophin-deficient hypogonadal mice lacking androgen receptors. Reproduction. 2010;139(1):177-84. http://dx.doi.org/10.1530/REP-09-0377. PMid:19846485.

Oduwole OO, Huhtaniemi IT, Misrahi M. The roles of Luteinizing hormone, follicle-stimulating hormone and testosterone in spermatogenesis and folliculogenesis revisited. Int J Mol Sci. 2021;22(23):12735. http://dx.doi.org/10.3390/ijms222312735. PMid:34884539.

Pakpoor J, Goldacre R, Schmierer K, Giovannoni G, Goldacre MJ. Testicular hypofunction and multiple sclerosis risk: a record-linkage study. Ann Neurol. 2014;76(4):625-8. http://dx.doi.org/10.1002/ana.24250. PMid:25131454.

Peterson DS, Fling BW. How changes in brain activity and connectivity are associated with motor performance in people with MS. Neuroimage Clin. 2017;17:153-62. http://dx.doi.org/10.1016/j.nicl.2017.09.019. PMid:29071209.

Reder AT, Makowiec RL, Lowy MT. Adrenal size is increased in multiple sclerosis. Arch Neurol. 1994;51(2):151-4. http://dx.doi.org/10.1001/archneur.1994.00540140057015. PMid:8304840.

Rivera VM. Multiple sclerosis in Latin Americans: genetic aspects. Curr Neurol Neurosci Rep. 2017;17(8):57. http://dx.doi.org/10.1007/s11910-017-0768-4. PMid:28639238.

Safarinejad MR. Evaluation of endocrine profile, hypothalamic-pituitary-testis axis and semen quality in multiple sclerosis. J Neuroendocrinol. 2008;20(12):1368-75. http://dx.doi.org/10.1111/j.1365-2826.2008.01791.x. PMid:19094084.

Sakakibara R. Gastrointestinal dysfunction in neuroinflammatory diseases: multiple sclerosis, neuromyelitis optica, acute autonomic ganglionopathy and related conditions. Auton Neurosci. 2021;232:102795. http://dx.doi.org/10.1016/j.autneu.2021.102795. PMid:33740560.

Song J, Goetz BD, Kirvell SL, Butt AM, Duncan ID. Selective myelin defects in the anterior medullary velum of the taiep mutant rat. Glia. 2001;33(1):1-11. http://dx.doi.org/10.1002/1098-1136(20010101)33:1<1::AID-GLIA1001>3.0.CO;2-Q. PMid:11169787.

Soto-Rodriguez G, Gonzalez-Barrios J-AA, Martinez-Fong D, Blanco-Alvarez V-MM, Eguibar JR, Ugarte A, Martinez-Perez F, Brambila E, Peña LM, Pazos-Salazar N-GG, Torres-Soto M, Garcia-Robles G, Tomas-Sanchez C, Leon-Chavez BA. Analysis of chemokines and receptors expression profile in the myelin mutant taiep rat. Oxid Med Cell Longev. 2015;2015:397310. http://dx.doi.org/10.1155/2015/397310. PMid:25883747.

Soto-Rodríguez G, Martínez-Fong D, Arroyo R, Aguilar-Alonso P, Rubio H, Eguibar JR, Ugarte A, Torres-Soto M, González-Barrios JA, Cebada J, Brambila E, Leon-Chavez BA. Nitric oxide production is associated to increased lipoperoxidation and active caspase-3 in demyelinated brain regions of the taiep rat. Adv Biosci Biotechnol. 2012;03(06):695-704. http://dx.doi.org/10.4236/abb.2012.326090.

Systat Software [online]. SigmaPlot. Illinois: Systat; 2023 [cited 2023 Oct 9]. Available at: https://systatsoftware.com/sigmaplot.

Thompson AJ, Baranzini SE, Geurts J, Hemmer B, Ciccarelli O. Multiple sclerosis. Lancet. 2018;391(10130):1622-36. http://dx.doi.org/10.1016/S0140-6736(18)30481-1. PMid:29576504.

Vihko KK, Lapolt PS, Nishimori K, Hsueh AJWW. Stimulatory effects of recombinant follicle-stimulating hormone on leydig cell function and spermatogenesis in immature hypophysectomized rats. Endocrinology. 1991;129(4):1926-32. http://dx.doi.org/10.1210/endo-129-4-1926. PMid:1915076.

Wei T, Lightman SL. The neuroendocrine axis in patients with multiple sclerosis. Brain. 1997;120(Pt 6):1067-76. http://dx.doi.org/10.1093/brain/120.6.1067. PMid:9217689.

Wu S, Wolfe A. Signaling of cytokines is important in regulation of GnRH neurons. Mol Neurobiol. 2012;45(1):119-25. http://dx.doi.org/10.1007/s12035-011-8224-y. PMid:22161498.

Zirkin BR, Papadopoulos V. Leydig cells: formation, function, and regulation. Biol Reprod. 2018;99(1):101-11. http://dx.doi.org/10.1093/biolre/ioy059. PMid:29566165.
 


Submitted date:
10/24/2022

Accepted date:
09/17/2023

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