TGF-β Superfamily: an Overview of Amh Signaling into Sex Determination and Differentiation in Fish

Oliveira, Marcos Antonio de; Silva Filho, Amorésio Souza; Araújo, Fabrício Eugênio

doi:10.1590/1678-4324-2023220371

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Review - Biological and Applied Sciences • Braz. arch. biol. technol. 66 • 2023 • https://doi.org/10.1590/1678-4324-2023220371 copy

TGF-β Superfamily: an Overview of Amh Signaling into Sex Determination and Differentiation in Fish

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

The decision whether the bipotential gonadal anlage will become a testis or ovary is a critical step during sex determination and differentiation in fish. This process involves a complex and coordinated genetic cascade, which result in the differentiation of the somatic cells into ovary or testis. In this context, important genes of TGF-β superfamily appears have a pivotal role in this biological process of fish development. In this review, we showed the breakthrough in the last decades that engage the Anti-Müllerian hormone (Amh) as an important effector in this decision. Here we exposed studies with different species of fishes around of world have paved the way for clarifying the role of Amh in the regulation of the germ cells proliferation, which may influence the spermatogenesis and, sex determination and differentiation decision on teleost fish.

Keywords:
Amh; cell proliferation; fish; germ cell; sex differentiation and determination

HIGHLIGHTS

• TGF-β superfamily members is crucial for cell differentiation and proliferation.

• TGF-β superfamily signaling are important to several biological system and the lack of these signaling can leads a several disorders and dysregulation of the tissue survive.

• Amh signaling have an important role during gonadal development in teleost fish.

GRAPHICAL ABSTRACT

Gene	Gene-full name	Species	References
sdY	Sexually dimorphic on the Y-chromosome	Oncorhynchus mykiss O. masou Salmon salar S. trutta Salvelinus alpinus S. fontinalis S. malma malma Hucho hucho Parahucho perryi	[⁸⁴84 Yano A, Nicol B, Jouanno E, Quillet E, Fostier A, Guyomard R, et al. The sexually dimorphic on the Y-chromosome gene (sdY) is a conserved male-specific Y-chromosome sequence in many salmonids. Evol Appl. 2013;6(3):486-96.]
sdf/gsdfY	Gonadal soma derived Factor/Gonadal soma derived factor on the Y-chromosome	Anoplopoma fimbria O. luzonensis	[¹⁶16 Myosho T, Otake H, Masuyama H, Matsuda M, Kuroki Y, Fujiyama A, et al. Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis. Genetics. 2012;191(1):163-70.] [⁸⁵85 Herpin A, Schartl M, Depincé A, Guiguen Y, Bobe J, Hua-Van A, et al. Allelic diversification after transposable element exaptation promoted gsdf as the master sex determining gene of sablefish. Genome Res. 2021;31(8):1366-80.]
gdf6Y	Growth differentiation factor 6 on the Y-chromosome	Turquoise killifish Nothobranchius furzeri	[⁴⁴44 Reichwald K, Petzold A., Koch P, Downie BR, Hartmann N, et al. Insights into sex chromosome evolution and aging from the genome of a short-lived fish. Cell. 2015;163:1527-38.]
dmy	DM-domain on the Y-chromosome	O. latipes	[⁸⁶86 Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, et al. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature. 2002;417(6888):559-63.]
dmrt1	Doublesex and mab-3 related transcription fator 1	Scatophagus argus Cynoglossus semilaevis	[⁸⁷87 Mustapha UF, Jiang D-N, Liang Z-H, Gu H-T, Yang W, Chen H-P, et al. Male-specific Dmrt1 is a candidate sex determination gene in spotted scat (Scatophagus argus). Aquaculture 2018, 495, 351-8.] [⁸⁸88 Cui Z, Liu Y, Wang W, Wang Q, Zhang N, Lin F, et al. Genome editing reveals dmrt1 as an essential male sex-determining gene in Chinese tongue sole (Cynoglossus semilaevis). Sci Rep. 2017;7:42213.]
dmrt1bY	Doublesex and mab-3 related transcription fator 1b on the Y chromosome	O. latipes, O. curvinotus	[⁸⁹89 Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A, et al. A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci U S A. 2002;99(18):11778-83.] [⁹⁰90 Matsuda M, Sato T, Toyazaki Y, Nagahama Y, Hamaguchi S, Sakaizumi M. Oryzias curvinotus has DMY, a gene that is required for male development in the medaka, O. latipes. Zoolog Sci. 2003;(2):159-61.]
sox3Y	Sry-related high mobility group-box gene 3 on the Y chromosome	O. dancena	[⁹¹91 Takehana Y, Matsuda M, Myosho T, Suster ML, Kawakami K, Shin-I T, et al. Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena. Nat Commun. 2014;5:4157.]
amhr2	Anti-Müllerian hormone receptor type 2	T. rubripes	[⁴⁵45 Kamiya T, Kai W, Tasumi S, Oka A, Matsunaga T, Mizuno N, et al. A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu). PLoS Genet. 2012;8(7):e1002798.]
amhr2by	Anti-Müllerian hormone receptor type 2 b on the Y chromosome	Perca flavescens P. altivelis	[⁴⁷47 Nakamoto M, Uchino T, Koshimizu E, Kuchiishi Y, Sekiguchi R, Wang L, et al. A Y-linked anti-Müllerian hormone type-II receptor is the sex-determining gene in ayu, Plecoglossus altivelis. PLoS Genet. 2021;17(8):e1009705.]
amhy	Y-linked anti-Müllerian hormone	O. Hatcheri O. Niloticus Sebastes schlegelii Hypoatherina tsurugae	[¹⁹19 Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK, Sakamoto T, et al. A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci U S A. 2012;109(8):2955-9.] [⁷⁰70 Liu X, Dai S, Wu J, Wei X, Zhou X, Chen M, et al. Roles of anti-Müllerian hormone and its duplicates in sex determination and germ cell proliferation of Nile tilapia. Genetics. 2022;220(3):iyab237.] [⁹²92 Song W, Xie Y, Sun M, Li X, Fitzpatrick CK, Vaux F, et al. A duplicated amh is the master sex-determining gene for Sebastes rockfish in the Northwest Pacific. Open Biol. 2021;11(7):210063.] [⁹³93 Bej DK, Miyoshi K, Hattori RS, Strüssmann CA, Yamamoto Y. A Duplicated, Truncated amh Gene Is Involved in Male Sex Determination in an Old World Silverside. G3 (Bethesda). 2017;7(8):2489-95.]
amhby	Y-linked anti-Müllerian Hormone b	E. lucius	[⁴⁶46 Pan Q, Feron R, Yano A, Guyomard R, Jouanno E, Vigouroux E, et al. Identifcation of the master sex determining gene in Northern pike (Esox lucius) reveals restricted sex chromosome differentiation. PLOS Genet. 2019;15:e1008013.]

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[1] * Correspondence: oliveira@zootecnista.com.br; Tel.: +55-19-35218661 (M.A.O.)