[KSCI] Korea Science Citation Index Service

http://dx.doi.org/10.12717/DR.2022.26.2.59

Differential Expressions of Aquaporin Subtypes in the Adult Mouse Testis

Mohamed, Elsayed A. (Dept. of Physiology, College of Medicine, Dong-A University)
Im, Ji Woo (Dept. of Physiology, College of Medicine, Dong-A University)
Kim, Dong-Hwan (Human Life Research Center, Dong-A University)
Bae, Hae-Rahn (Dept. of Physiology, College of Medicine, Dong-A University)

Publication Information

Development and Reproduction / v.26, no.2, 2022 , pp. 59-69 More about this Journal

Abstract

Many efforts have been made to study the expression of aquaporins (AQP) in the mammalian reproductive system, but there are not enough data available regarding their localized expression to fully understand their specific roles in male reproduction. The present study investigated the expression and localization patterns of different AQP subtypes in the adult mouse testes and testicular spermatozoa using an immunofluorescence assay. All the studied AQPs were expressed in the testes and revealed subtype-specific patterns in the intensity and localization depending on the cell types of the testes. AQP7 was the most abundant and intensive AQP subtype in the seminiferous tubules, expressing in Leydig cells and Sertoli cells as well as all stages of germ cells, especially the spermatids and testicular spermatozoa. The expression pattern of AQP3 was similar to that of AQP7, but with higher expression in the basal and lower adluminal compartments rather than the upper adluminalcompartment. AQP8 expression was limited to the spermatogonia and Leydig cells whereas AQP9 expression was exclusive to tails of the testicular spermatozoa and elongated spermatids. Taken together, the abundance and distribution of the AQPs across the different cell types in the testes indicating to their relavance in spermatogenesis, as well as in sperm maturation, transition, and function.

Keywords

Aquaporins7 (AQP7); AQP3; AQP8; AQP9; AQP1; Testes; Mouse;

Citations & Related Records

Reference

1	Sohara E, Ueda O, Tachibe T, Hani T, Jishage K, Rai T, Sasaki S, Uchida S (2007) Morphologic and functional analysis of sperm and testes in aquaporin 7 knockout mice. Fertil Steril 87:671-676. DOI
2	Squillacioti C, Mirabella N, Liguori G, Germano G, Pelagalli A (2021) Aquaporins are differentially regulated in canine cryptorchid efferent ductules and epididymis. Animals 11:1539. DOI
3	Verkman AS (2012) Aquaporins in clinical medicine. Annu Rev Med 63:303-316. DOI
4	Vicente-Carrillo A, Ekwall H, Alvarez-Rodriguez M, Rodriguez-Martinez H (2016) Membrane stress during thawing elicits redistribution of aquaporin 7 but not of aquaporin 9 in boar spermatozoa. Reprod Domest Anim 51:665-679. DOI
5	Yeung CH, Callies C, Rojek A, Nielsen S, Cooper TG (2009) Aquaporin isoforms involved in physiological volume regulation of murine spermatozoa. Biol Reprod 80:350-357. DOI
6	Yeung CH, Callies C, Tuttelmann F, Kliesch S, Cooper TG (2010) Aquaporins in the human testis and spermatozoa-identification, involvement in sperm volume regulation and clinical relevance. Int J Androl 33:629-641. DOI
7	Moretti E, Terzuoli G, Mazzi L, Iacoponi F, Collodel G (2012) Immunolocalization of aquaporin 7 in human sperm and its relationship with semen parameters. Syst Biol Reprod Med 58:129-135. DOI
8	Alves MG, Sa R, Jesus TT, Sousa M, Oliveira PF (2015) CFTR regulation of aquaporin-mediated water transport: A target in male fertility. Curr Drug Targets 16:993-1006. DOI
9	An F, Wang J (2016) Immunohistochemical study of aquaporin 1 and 2 in the reproductive tract of the Bactrian camel (Camelus bactrianus). Int J Morphol 34:1218-1222. DOI
10	Arena S, Arena F, Maisano D, Di Benedetto V, Romeo C, Nicotina PA (2011) Aquaporin-9 immunohistochemistry in varicocele testes as a consequence of hypoxia in the sperm production site. Andrologia 43:34-37. DOI
11	Arrighi S, Aralla M (2014) Immunolocalization of aquaporin water channels in the domestic cat male genital tract. Reprod Domest Anim 49:17-26. DOI
12	Azad AK, Raihan T, Ahmed J, Hakim A, Emon TH, Chowdhury PA (2021) Human aquaporins: Functional diversity and potential roles in infectious and non-infectious diseases. Front Genet 12:654865. DOI
13	Bernardino RL, Carrageta DF, Silva AM, Calamita G, Alves MG, Soveral G, Oliveira PF (2018) Estrogen modulates glycerol permeability in sertoli cells through downregulation of aquaporin-9. Cells 7:153. DOI
14	Danyu L, Ying L, Zhenwu B, Heming Y, Xuejun L (2008) Aquaporin 1 expression in the testis, epididymis and vas deferens of postnatal ICR mice. Cell Biol Int 32:532-541. DOI
15	Carrageta DF, Bernardino RL, Soveral G, Calamita G, Alves MG, Oliveira PF (2020) Aquaporins and male (in)fertility: Expression and role throughout the male reproductive tract. Arch Biochem Biophys 679:108222. DOI
16	Boj M, Chauvigne F, Cerda J (2015) Aquaporin biology of spermatogenesis and sperm physiology in mammals and teleosts. Biol Bull 229:93-108. DOI
17	Calamita G, Mazzone A, Cho YS, Valenti G, Svelto M (2001b) Expression and localization of the aquaporin-8 water channel in rat testis. Biol Reprod 64:1660-1666. DOI
18	Delporte C (2017) Aquaporins and gland secretion. Adv Exp Med Biol 969:63-79. DOI
19	Dube E, Hermo L, Chan PTK, Cyr DG (2008) Alterations in gene expression in the caput epididymides of nonobstructive azoospermic men. Biol Reprod 78:342-351. DOI
20	Elkjaer ML, Vajda Z, Nejsum LN, Kwon TH, Jensen UB, Amiry-Moghaddam M, Frokiaer J, Nielsen S (2000) Immunolocalization of AQP9 in liver, epididymis, testis, spleen, and brain. Biochem Biophys Res Commun 276:1118-1128. DOI
21	Ford J Jr, Carnes K, Hess RA (2014) Ductuli efferentes of the male Golden Syrian hamster reproductive tract. Andrology 2:510-520. DOI
22	Hermo L, Smith CE (2011) Thirsty business: Cell, region, and membrane specificity of aquaporins in the testis, efferent ducts, and epididymis and factors regulating their expression. J Androl 32:565-575. DOI
23	Klein C, Troedsson MHT, Rutllant J (2013) Region-specific expression of aquaporin subtypes in equine testis, epididymis, and ductus deferens. Anat Rec 296:1115-1126. DOI
24	Laforenza U, Pellavio G, Marchetti AL, Omes C, Todaro F, Gastaldi G (2017) Aquaporin-mediated water and hydrogen peroxide transport is involved in normal human spermatozoa functioning. Int J Mol Sci 18:66. DOI
25	Yang B, Song Y, Zhao D, Verkman AS (2005) Phenotype analysis of aquaporin-8 null mice. Am J Physiol Cell Physiol 288:C1161-C1170. DOI
26	Lu DY, Li Y, Bi ZW, Yu HM, Li XJ (2008) Expression and immunohistochemical localization of aquaporin-1 in male reproductive organs of the mouse. Anat Histol Embryol 37:1-8. DOI
27	Ma T, Song Y, Yang B, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS (2000) Nephrogenic diabetes insipidus in mice lacking aquaporin-3 water channels. Proc Natl Acad Sci USA 97:4386-4391. DOI
28	Tani T, Koyama Y, Nihei K, Hatakeyama S, Ohshiro K, Yoshida Y, Yaoita E, Sakai Y, Hatakeyama K, Yamamoto T (2001) Immunolocalization of aquaporin-8 in rat digestive organs and testis. Arch Histol Cytol 64:159-168. DOI
29	Yu L, Moriguchi T, Souma T, Takai J, Satoh H, Morito N, Engel JD, Yamamoto M (2014) GATA2 regulates body water homeostasis through maintaining aquaporin 2 expression in renal collecting ducts. Mol Cell Biol 34:1929-1941. DOI
30	Levine N, Marsh DJ (1971) 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 213:557-570. DOI
31	Ribeiro JC, Alves MG, Yeste M, Cho YS, Calamita G, Oliveira PF (2021) Aquaporins and (in) fertility: More than just water transport. BBA-Mol Basis Dis 1867:166039. DOI
32	Arnaoutova I, Cawley NX, Patel N, Kim T, Rathod T, Loh YP (2008) Aquaporin 1 is important for maintaining secretory granule biogenesis in endocrine cells. Mol Endocrinol 22:1924-1934. DOI
33	Calamita G, Mazzone A, Bizzoca A, Svelto M (2001a) Possible involvement of aquaporin-7 and -8 in rat testis development and spermatogenesis. Biochem Biophys Res Commun 288:619-625. DOI
34	Chen Q, Peng H, Lei L, Zhang Y, Kuang H, Cao Y, Shi QX, Ma T, Duan E (2011) Aquaporin3 is a sperm water channel essential for postcopulatory sperm osmoadaptation and migration. Cell Res 21:922-933. DOI
35	Domeniconi RF, Orsi AM, Justulin LA Jr, Beu CCL, Felisbino SL (2007) Aquaporin 9 (AQP9) localization in the adult dog testis excurrent ducts by immunohistochemistry. Anat Rec (Hoboken) 290:1519-1525. DOI
36	Mirabella N, Pelagalli A, Liguori G, Rashedul MA, Squillacioti C (2021) Differential abundances of AQP3 and AQP5 in reproductive tissues from dogs with and without cryptorchidism. Anim Reprod Sci 228:106735. DOI
37	Elkjaer ML, Nejsum LN, Gresz V, Kwon TH, Jensen UB, Frokiaer J, Nielsen S (2001) Immunolocalization of aquaporin-8 in rat kidney, gastrointestinal tract, testis, and airways. Am J Physiol Renal Physiol 281:F1047-F1057. DOI
38	Kageyama Y, Ishibashi K, Hayashi T, Xia G, Sasaki S, Kihara K (2001) Expression of aquaporins 7 and 8 in the developing rat testis. Andrologia 33:165-169. DOI
39	Meli R, Pirozzi C, Pelagalli A (2018) New perspectives on the potential role of aquaporins (AQPs) in the physiology of inflammation. Front Physiol 9:101.
40	Badran HH, Hermo LS (2002) 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 23:358-373.
41	Nicchia GP, Frigeri A, Nico B, Ribatti D, Svelto M (2001) Tissue distribution and membrane localization of aquaporin-9 water channel: Evidence for sex-linked differences in liver. J Histochem Cytochem 49:1547-1556. DOI
42	Saito K, Kageyama Y, Okada Y, Kawakami S, Kihara K, Ishibashi K, Sasaki S (2004) Localization of aquaporin-7 in human testis and ejaculated sperm: Possible involvement in maintenance of sperm quality. J Urol 172:2073-2076. DOI
43	Ribeiro JC, Carrageta DF, Bernardino RL, Alves MG, Oliveira PF (2022) Aquaporins and animal gamete cryopreservation: Advances and future challenges. Animals 12:359. DOI
44	Nihei K, Koyama Y, Tani T, Yaoita E, Ohshiro K, Adhikary LP, Kurosaki I, Shirai Y, Hatakeyama K, Yamamoto T (2001) Immunolocalization of aquaporin-9 in rat hepatocytes and Leydig cells. Arch Histol Cytol 64:81-88. DOI
45	Oliveira RL, Campolina-Silva GH, Nogueira JC, Mahecha GAB, Oliveira CA (2013) Differential expression and seasonal variation on aquaporins 1 and 9 in the male genital system of big fruiteating bat Artibeus lituratus. Gen Comp Endocrinol 186:116-125. DOI
46	Pastor-Soler N, Bagnis C, Sabolic I, Tyszkowski R, McKee M, Van Hoek A, Breton S, Brown D (2001) Aquaporin 9 expression along the male reproductive tract. Biol Reprod 65:384-393. DOI
47	Prieto-Martinez N, Vilagran I, Morato R, Rodriguez-Gil JE, Yeste M, Bonet S (2016) Aquaporins 7 and 11 in boar spermatozoa: Detection, localisation and relationship with sperm quality. Reprod Fertil Dev 28:663-672. DOI
48	Rato L, Socorro S, Cavaco JEB, Oliveira PF (2010) Tubular fluid secretion in the seminiferous epithelium: Ion transporters and aquaporins in Sertoli cells. J Membr Biol 236:215-224. DOI
49	Shivaraj SM, Deshmukh R, Bhat JA, Sonah H, Belanger RR (2017) Understanding aquaporin transport system in eelgrass (Zostera marina L.), an aquatic plant species. Front Plant Sci 3;8:1334.
50	Skowronski MT, Lebeck J, Rojek A, Praetorius J, Fuchtbauer EM, Frokiaer J, Nielsen S (2007) AQP7 is localized in capillaries of adipose tissue, cardiac and striated muscle: Implications in glycerol metabolism. Am J Physiol Renal Physiol 292:F956-F965. DOI