Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2021-0070
Animal Reproduction (AR)
ORIGINAL ARTICLE

Morphology and immunolocalization of aquaporins 1 and 9 in the agouti (Dasyprocta azarae) testis excurrent ducts

Bruno Cesar Schimming; Leandro Luis Martins; Fabrício Singaretti de Oliveira; Patrícia Fernanda Felipe Pinheiro; Raquel Fantin Domeniconi

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Abstract

This study investigated the morphology and immunoexpression of aquaporins (AQPs) 1 and 9 in the rete testis, efferent ducts, epididymis, and vas deferens in the Azara’s agouti (Dasyprocta azarae). For this purpose, ten adult sexually mature animals were used in histologic and immunohistochemical analyses. The Azara’s agouti rete testis was labyrinthine and lined with simple cubic epithelium. Ciliated and non-ciliated cells were observed in the epithelium of the efferent ducts. The epididymal cellular population was composed of principal, basal, apical, clear, narrow, and halo cells. The epithelium lining of vas deferens was composed of the principal and basal cells. AQPs 1 and 9 were not expressed in the rete testis. Positive reaction to AQP1 was observed at the luminal border of non-ciliated cells of the efferent ducts, and in the peritubular stroma and blood vessels in the epididymis, and vas deferens. AQP9 was immunolocalized in the epithelial cells in the efferent ducts, epididymis and vas deferens. The morphology of Azara’s agouti testis excurrent ducts is similar to that reported for other rodents such as Cuniculus paca. The immunolocalization results of the AQPs suggest that the expression of AQPs is species-specific due to differences in localization and expression when compared to studies in other mammals species. The knowledge about the expression of AQPs in Azara’s agouti testis excurrent ducts is essential to support future reproductive studies on this animal, since previous studies show that AQPs may be biomarkers of male fertility and infertility.

Keywords

aquaporins, morphology, rodents, epididymis, efferent ducts

References

Agre P. Aquaporin water channels (Nobel Lecture). Angew Chem Int Ed Engl. 2004;43(33):4278-90. http://dx.doi.org/10.1002/anie.200460804. PMid:15368374.

Andonian S, Hermo L. Principal cells of the vas deferens are involved in water transport and steroid synthesis in the adult rat. J Androl. 1999;20(1):158-76. PMid:10100486.

Arrighi S, Bosi G, Accogli G, Desantis S. Seasonal and ageing-depending changes of aquaporins 1 and 9 expression in the genital tract of buffalo bulls (Bubalus bubalis). Reprod Domest Anim. 2016;51(4):515-23. http://dx.doi.org/10.1111/rda.12713. PMid:27260501.

Arrighi S, Romanello MG, Domeneghini C. Ultrastructure of the epithelium that lines the ductuli efferentes in domestic equidae, with particular reference to spermatophagy. Acta Anat (Basel). 1994;149(3):174-84. http://dx.doi.org/10.1159/000147574. PMid:7976167.

Arrighi S, Ventriglia G, Aralla M, Zizza S, Di Summa A, Desantis S. Absorptive activities of the efferent ducts evaluated by the immunolocalization of aquaporin water channels and lectin histochemistry in adult cats. Histol Histopathol. 2010;25(4):433-44. http://dx.doi.org/10.14670/HH-25.433. PMid:20183796.

Arrighi S. Are the basal cells of the mammalian epididymis still an enigma? Reprod Fertil Dev. 2014;26(8):1061-71. http://dx.doi.org/10.1071/RD13301. PMid:24138802.

Arroyo MAM, Oliveira MF, Santos PRS, Assis AC No. Ultrastructure of the epididymis and vas deferens of agoutis at diferente stages of sexual development. Anim Reprod Sci. 2014;149(3-4):273-80. http://dx.doi.org/10.1016/j.anireprosci.2014.05.006. PMid:25028182.

Arroyo MAM, Silva FFS, Santos PRS, Silva AR, Oliveira MF, Assis-Neto AC. Ultrastructure of the spermatogenesis and spermatozoa in agoutis during sexual development. Reprod Fertil Dev. 2017;29(2):383-93. http://dx.doi.org/10.1071/RD14442. PMid:26336816.

Badran HH, Hermo LS. Expression and regulation of aquaporins 1, 8 and 9 in the testis, efferent ducts, and epididymis of adult rats and during postnatal development. J Androl. 2002;23(3):358-73. PMid:12002438.

Belleannée C, Da Silva N, Shum WWC, Brown D, Breton S. Role of purinergi signaling pathways in V-ATPase recruitment to apical membrane of acidifying epididymal clear cells. Am J Physiol Cell Physiol. 2010;298(4):C817-30. http://dx.doi.org/10.1152/ajpcell.00460.2009. PMid:20071692.

Belleannée C, Silva ND, Shum WWC, Marsolais M, Laprade R, Brown D, Breton S. Segmental expression of the Bradykinin type 2 receptor in rat efferent ducts and epididymis and its role in the regulation of aquaporin 9. Biol Reprod. 2009;80(1):134-43. http://dx.doi.org/10.1095/biolreprod.108.070797. PMid:18829705.

Belleannée C, Thimon V, Sullivan R. Region-specific gene expression in the epididymis. Cell Tissue Res. 2012;349(3):717-31. http://dx.doi.org/10.1007/s00441-012-1381-0. PMid:22427067.

Beu CCL, Orsi AM, Stefanini MA, Silva MDP, Vicentini CA. A rede testicular na cobaia. Observações morfológicas e histoquímicas. Rev Ciênc Biom. 1997;18:33-44.

Breton S, Ruan YC, Park YLJ, Kim B. Regulation of epithelial function, differentiation, and remodelling in the epididymis. Asian J Androl. 2016;18(1):3-9. http://dx.doi.org/10.4103/1008-682X.165946. PMid:26585699.

Breton S, Smith PJ, Lui B, Brown D. Acidification of the male reproductive tract by a proton pumping (H+)-ATPase. Nat Med. 1996;2(4):470-2. http://dx.doi.org/10.1038/nm0496-470. PMid:8597961.

Brown D. The discovery of water channels (Aquaporins). Ann Nutr Metab. 2017;70(Suppl 1):37-42. http://dx.doi.org/10.1159/000463061. PMid:28614812.

Carrageta DF, Bernardino RL, Soveral G, Calamita G, Alves MG, Oliveira PF. Aquaporins and male (in)fertility: expression and role throughout the male reproductive tract. Arch Biochem Biophys. 2020;679:108222. http://dx.doi.org/10.1016/j.abb.2019.108222. PMid:31816311.

Castelo TS, Souza ALP, Lima GL, Peixoto GCX, Campos LB, Oliveira MF, Silva AR. Interactions among diferentes devices and eletrical stimulus on the electroejaculation of captive agoutis (D. leporina). Reprod Domest Anim. 2015;50(3):492-6. http://dx.doi.org/10.1111/rda.12517. PMid:25800458.

Castro MM, Kim B, Hill E, Fialho MC, Puga LC, Freitas MB, Breton S, Machado-Neves M. The expression patterns of aquaporin 9, vacuolar H+-ATPase, and cytokeratin 5 in the epididymis of the common vampire bat. Histochem Cell Biol. 2017;147(1):39-48. http://dx.doi.org/10.1007/s00418-016-1477-9. PMid:27549752.

Cheung KH, Leung GPH, Leung MCT, Shum WWC, Zhou W, Wong PYD. Cell-cell interaction underlies formation of fluid in the male reproductive tract of the rat. J Gen Physiol. 2005;125(5):443-54. http://dx.doi.org/10.1085/jgp.200409205. PMid:15851503.

Clulow J, Jones RC, Hansen LA. Micropuncture and cannulation studies of fluid composition and transport in the ductuli efferent testis of the rat: comparison with the homologous metanephric proximal tubule. Exp Physiol. 1994;79(6):915-28. http://dx.doi.org/10.1113/expphysiol.1994.sp003817. PMid:7873160.

Cooper TG, Wagenfeld A, Cornwall GA, Hsia N, Chu ST, Orgebin-Crist MC, Drevet J, Vernet P, Avram C, Nieschlag E, Yeung CH. Gene and protein expression in the epididymis of infertile c-ros receptor tyrosine kinase-deficient mice. Biol Reprod. 2003;69(5):1750-62. http://dx.doi.org/10.1095/biolreprod.103.017566. PMid:12890734.

Cornwall GA, Lareyre JJ, Matusik RJ, Hinton BT, Orgebin-Crist MC. Gene expression and epididymal function. In: Robaire B, Hinton BT, editors. The epididymis: from molecules to clinical practice. New York, USA: Kluwer Academic/Plenum Publishers; 2002. p. 169-200. http://dx.doi.org/10.1007/978-1-4615-0679-9_10.

Cruceño AAM, Aguilera-Merlo CI, Chaves EM, Mohamed FH. Epididymis of viscacha (Lagostomus maximus maximus): A morphological comparative study in relation to sexual maturity. Anat Histol Embryol. 2017;46(1):73-84. http://dx.doi.org/10.1111/ahe.12240. PMid:27457370.

Da Silva N, Shum WW, Breton S. Regulation of vacuolar proton pumping ATPase-dependent luminal acidification in the epididymis. Asian J Androl. 2007;9(4):476-82. http://dx.doi.org/10.1111/j.1745-7262.2007.00299.x. PMid:17589784.

Da Silva N, Silberstein C, Beaulieu V, Piétrement C, Van Hoek NA, Brown D, Breton S. Postnatal expression of aquaporins in epithelial cells of the rat epididymis. Biol Reprod. 2006;74(2):427-38. http://dx.doi.org/10.1095/biolreprod.105.044735. PMid:16221990.

Domeniconi RF, Orsi AM, Justulin LA Jr, Beu CCL, Felisbino SL. Aquaporin 9 (AQP9) localization in the adult dog testis excurrent ducts by immunohistochemistry. Anat Rec (Hoboken). 2007;290(12):1519-25. http://dx.doi.org/10.1002/ar.20611. PMid:17957752.

Domeniconi RF, Orsi AM, Justulin LA Jr, Leme Beu CC, Felisbino SL. Immunolocalization of aquaporins 1, 2 and 7 in rete testis, efferent ducts, epididymis and vas deferens of adult dog. Cell Tissue Res. 2008;332(2):329-35. http://dx.doi.org/10.1007/s00441-008-0592-x. PMid:18340467.

Eisenberg JF, Redford KH. Mammals of the neotropics. The Central neotropics. Chicago, USA: The University of Chicago Press; 1999.

Ford J Jr, Carnes K, Hess RA. Ductuli efferentes of the male golden Syrian hamster reproductive tract. Andrology. 2014;2(4):510-20. http://dx.doi.org/10.1111/j.2047-2927.2014.00194.x. PMid:24677666.

Goyal HO, Hutto V, Robinson DD. Reexamination of the morphology of the extratesticular rete and ductuli efferents in the goat. Anat Rec. 1992;233(1):53-60. http://dx.doi.org/10.1002/ar.1092330108. PMid:1605378.

Hermo L, Dworkin J, Oko R. Role of the epithelial clear cells of the rat epididymis in the disposal of the contents of cytoplasmic droplets detached from spermatozoa. Am J Anat. 1988;183(2):107-24. http://dx.doi.org/10.1002/aja.1001830202. PMid:2849296.

Hermo L, Robaire B. Epididymal cell types and their functions. In: Robaire B, Hinton BT, editors. The epididymis: from molecules to clinical practice. New York, USA: Kluwer Academic/Plenum Publishers; 2002. p. 81-102. http://dx.doi.org/10.1007/978-1-4615-0679-9_5.

Hermo L, Schellenberg M, Liu LY, Dayanandan B, Zhang T, Mandato CA, Smith CE. Membrane domain specificity in the spatial distribution of aquaporins 5, 7, 9 and 11 in efferent ducts and epididymis of rats. J Histochem Cytochem. 2008;56(12):1121-35. http://dx.doi.org/10.1369/jhc.2008.951947. PMid:18796408.

Hess RA. The efferent ductules: structure and functions. In: Robaire B, Hinton BT, editors. The epididymis: from molecules to clinical practice. New York, USA: Kluwer Academic/Plenum Publishers; 2002. p. 49-80. http://dx.doi.org/10.1007/978-1-4615-0679-9_4.

Jones RC, Dacheux JL, Nixon B, Ecroyd HW. Role of the epididymis in sperm competition. Asian J Androl. 2007;9(4):493-9. http://dx.doi.org/10.1111/j.1745-7262.2007.00284.x. PMid:17589786.

Lange RR, Schmidt EMS. Rodentia-Roedores selvagens (capivara, cutia, paca e ouriço). In: Cubas ZS, Silva JCR, Catão-Dias JL, editors. Tratado de animais selvagens. São Paulo: Gen Roca; 2014. p. 1261-1262.

Levine N, Marsh DJ. Micropuncture studies of the electrochemical aspects of fluid and electrolyte transport in individual seminiferous tubules, the epididymis and the vas deferens in rats. J Physiol. 1971;213(3):557-70. http://dx.doi.org/10.1113/jphysiol.1971.sp009400. PMid:5551402.

Lorenzana MG, López-Wilchis R, Gómez CS, Aranzabal MCU. A light and scanning electron microscopy study of the epididymis active state of the endemic Mexican rodent Peromyscus winkelmanni (Carleton) (Rodentia: muridae). Anat Histol Embryol. 2007;36(3):230-40. http://dx.doi.org/10.1111/j.1439-0264.2006.00752.x. PMid:17535358.

Mandon M, Cyr DG. Tricellulin and its role in the epididymal epithelium of the rat. Biol Reprod. 2015;92(3):66. http://dx.doi.org/10.1095/biolreprod.114.120824. PMid:25568308.

Martinez AC, Oliveira FS, Abreu CO, Martins LL, Pauloni AP, Moreira N. Colheita de sêmen por eletroejaculação em cutia-parda (D. azarae). Pesq Vet Bras. 2013;33(1):86-8. http://dx.doi.org/10.1590/S0100-736X2013000100015.

Menezes TP, Hill E, de Alencar Moura A, Lobo MDP, Monteiro-Moreira ACO, Breton S, Machado-Neves M. Pattern of protein expression in the epididymis of Olygoryzomys nigripes (Cricetidae, Sigmodontinae). Cell Tissue Res. 2018;372(1):135-47. http://dx.doi.org/10.1007/s00441-017-2714-9. PMid:29119327.

Mollineau W, Adogwa A, Jasper N, Young K, Garcia G. The gross anatomy of the male reproductive system of a neotropical rodent: the agouti (Dasyprota leporina). Anat Histol Embryol. 2006;35(1):47-52. http://dx.doi.org/10.1111/j.1439-0264.2005.00656.x. PMid:16433673.

Mollineau WM, Adogwa AO, Garcia GW. The gross and micro-anatomy of the acessory glands of the male agouti (Dasyprocta leporina). Anat Histol Embryol. 2009;38(3):204-7. http://dx.doi.org/10.1111/j.1439-0264.2008.00922.x. PMid:19007350.

Mollineau WM, Sampson T, Adogwa AO, Garcia GW. Anatomical stages of penile erection in the agouti (Dasyprocta leporina) induced by electro-ejaculation. Anat Histol Embryol. 2012;41(5):392-4. http://dx.doi.org/10.1111/j.1439-0264.2012.01142.x. PMid:22352811.

Nakai M, Bouma J, Nie R, Zhou Q, Carnes K, Lubahn DB, Hess RA. Morphological analysis of endocytosis in efferent ductules of estrogen receptor-alpha knockout mouse. Anat Rec. 2001;263(1):10-8. http://dx.doi.org/10.1002/ar.1071. PMid:11331966.

Nicòtina PA, Romeo C, Arena S, Arena F, Maisano D, Zuccarello B. Immunoexpression of aquaporin-1 in adolescente varicocele testes: possible signficance for fluid reabsorption. Urology. 2005;65(1):149-52. http://dx.doi.org/10.1016/j.urology.2004.08.014. PMid:15667881.

Oberska P, Michalek K. Aquaporins: new markers for male (in)fertility in livestock and poultry? Anim Reprod Sci. 2021;231:106807. http://dx.doi.org/10.1016/j.anireprosci.2021.106807. PMid:34303091.

Oliveira CA, Carnes K, França LR, Hermo L, Hess RA. Aquaporin-1 and -9 are differentially regulated by oestrogen in the efferent ductule epithelium and initial segment of the epididymis. Biol Cell. 2005;97(6):385-95. http://dx.doi.org/10.1042/BC20040078. PMid:15850448.

Pelagalli A, Squillacioti C, Ali S, Liguori G, Mirabella N. Cellular distribution of aquaporins in testes of normal and cryporchid dogs: A preliminary study on dynamic roles. Anim Reprod Sci. 2019;204:22-30. http://dx.doi.org/10.1016/j.anireprosci.2019.03.001. PMid:30862405.

Pietrement C, Sun-Wada GH, Silva ND, McKee M, Marshansky V, Brown D, Futai M, Breton S. Distinct expression patterns of different subunit isoforms of the V-ATPase in the rat epididymis. Biol Reprod. 2006;74(1):185-94. http://dx.doi.org/10.1095/biolreprod.105.043752. PMid:16192400.

Praxedes ÉCG, Peixoto GCX, Maria da Silva A, Silva AR. Reproduction in agouti (Dasyprocta spp.): a review of reproductive physiology for developing assisted reproductive techniques. Anim Reprod. 2018;15(4):1181-92. http://dx.doi.org/10.21451/1984-3143-AR2018-0058. PMid:34221130.

Robaire B, Hermo L. Efferent ducts, epididymis, and vas deferens: structure, functions, and their regulation. In: Knobil E, Neill J, editors. The Physiology of Reproduction. New York, USA: Raven Press; 1988. p. 999-1080.

Robaire B, Hinton BT. The epididymis. In: Plant TM, Zeleznik AJ, editors. Knobil and Neill’s physiology of reproduction. 4th ed. San Diego, CA, USA: Elsevier; 2015. p. 691-771. http://dx.doi.org/10.1016/B978-0-12-397175-3.00017-X.

Roosen-Runge EC, Holstein AF. The human rete testis. Cell Tissue Res. 1978;189(3):409-33. http://dx.doi.org/10.1007/BF00209130. PMid:657253.

Roosen-Runge EC. The rete testis in the albino rat: its structure, development and morphological significance. Acta Anat (Basel). 1961;45(1-2):1-30. http://dx.doi.org/10.1159/000141738. PMid:14493722.

Schimming BC, Baumam C, Pinheiro P, de Matteis R, Domeniconi RF. Aquaporin 9 is expressed in the epididymis of immature and mature pigs. Reprod Domest Anim. 2017;52(4):617-24. http://dx.doi.org/10.1111/rda.12957. PMid:28370569.

Schimming BC, Machado MR, Simões K, da Cruz C, Domeniconi RF. Light microscope observation on the epididymis of paca (Agouti paca). Ital J Anat Embryol. 2013;118(1):119-27. http://dx.doi.org/10.13128/IJAE-12867. PMid:23898581.

Schimming BC, Pinheiro PFF, de Matteis R, Machado CM, Domeniconi RF. Immunolocalization of aquaporins 1 and 9 in the ram efferent ducts and epididymis. Reprod Domest Anim. 2015;50(4):617-24. http://dx.doi.org/10.1111/rda.12537. PMid:25976237.

Schimming BC, Vicentini CA. Ultrastructural features in the epididymis of the dog (Canis familiaris, L.). Anat Histol Embryol. 2001;30(6):327-32. http://dx.doi.org/10.1046/j.1439-0264.2001.00338.x. PMid:11820400.

Serre V, Robaire B. Segment-specific morphological changes in aging Brown Norway rat epididymis. Biol Reprod. 1998;58(2):497-513. http://dx.doi.org/10.1095/biolreprod58.2.497. PMid:9475407.

Setchell BP, Maddocks S, Brooks DE. Anatomy, vasculature, innervations, and fluids of the male reproductive tract. In: Knobil E, Neill JD, editors. The physiology of reproduction. New York, USA: Raven Press; 1994. p. 1063-1175.

Sharma S, Kumaran GK, Hanukoglu I. High-resolution imaging of the actin cytoskeleton and epithelial sodium channel, CFTR, and aquaporin-9 localization in the vas deferens. Mol Reprod Dev. 2020;87(2):305-19. http://dx.doi.org/10.1002/mrd.23317. PMid:31950584.

Shum WWC, Da Silva N, Brown D, Breton S. Regulation of luminal acidification in the male reproductive tract via cell-cell crosstalk. J Exp Biol. 2009;212(Pt 11):1753-61. http://dx.doi.org/10.1242/jeb.027284. PMid:19448084.

Shum WWC, Ruan YC, Da Silva N, Breton S. Establishment of cell-cell cross talk in the epididymis: control of luminal acidification. J Androl. 2011;32(6):576-86. http://dx.doi.org/10.2164/jandrol.111.012971. PMid:21441423.

Silva DCB, Fagundes NCF, Teixeira FB, Penha NEA, Santana LNS, Mendes-Oliveira AC, Lima RR. Anatomical and histological characteristics of teeth in agouti (Dasyprocta prymnolopha Wagler, 1831). Pesq Vet Bras. 2013;33(Suppl 1):51-7. http://dx.doi.org/10.1590/S0100-736X2013001300009.

Sullivan R, Mieusset R. The human epididymis: its function in sperm maturation. Hum Reprod Update. 2016;22(5):574-87. http://dx.doi.org/10.1093/humupd/dmw015. PMid:27307387.

Verkman AS, Mitra AK. Structure and function of aquaporin water channels. Am J Physiol Renal Physiol. 2000;278(1):F13-28. http://dx.doi.org/10.1152/ajprenal.2000.278.1.F13. PMid:10644652.

Verkman AS. Physiological importance of aquaporin water channels. Ann Med. 2002;34(3):192-200. http://dx.doi.org/10.1080/ann.34.3.192.200. PMid:12173689.

Viotto MJ, Orsi AM, Vicentini CA, Dias SM, Gregório EA. Ultrastructure of the rete testis in the cat (Felis domestica, L.). Anat Histol Embryol. 1993;22(2):114-22. http://dx.doi.org/10.1111/j.1439-0264.1993.tb00349.x. PMid:8346808.

Yeste M, Morató R, Rodríguez-Gil JE, Bonet S, Prieto-Martínez N. Aquaporins in the male reproductive tract and sperm: functional implications and crybiology. Reprod Domest Anim. 2017;52(Suppl 4):12-27. http://dx.doi.org/10.1111/rda.13082. PMid:29052330.
 


Submitted date:
07/20/2021

Accepted date:
10/05/2021

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