Identification of SOX3 as an XX male sex reversal gene in mice and humans

Edwina Sutton, James Hughes, Stefan White, Ryohei Sekido, Jacqueline Tan, Valerie Arboleda, Nicholas Rogers, Kevin Knower, Lynn Rowley, Helen Eyre, Karine Rizzoti, Dale McAninch, Joao Goncalves, Jennie Slee, Erin Turbitt, Damien Bruno, Henrik Bengtsson, Vincent Harley, Eric Vilain, Andrew SinclairRobin Lovell-Badge, Paul Thomas*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

246 Citations (Scopus)

Abstract

Sex in mammals is genetically determined and is defined at the cellular level by sex chromosome complement (XY males and X,C females) The Y chromosome-linked gene sex-determining region Y (SRY) is believed to be the master initiator of male sex determination in almost all eutherian and metatherian mammals, functioning to upregulate expression of its direct target gene Sty-related HMG box-containing gene 9 (SOX9) Data suggest that SRY evolved from SOX3, although there is no direct functional evidence to support this hypothesis Indeed, loss-of-function mutations in SOX3 do not affect sex determination m mice or humans To further investigate Sox3 function in vivo, we generated transgenic mice overexpressing Sox3 Here, we report that in one of these transgenic lines, Sox3 was ectopically expressed in the bipotential gonad and that this led to frequent complete XX male sex reversal Further analysis indicated that Sox3 induced testis differentiation in this particular line of mice by upregulating expression of Sox9 via a similar mechanism to Sry Importantly, we also identified genomic rearrangements within the SOX3 regulatory region in three patients with XX male sex reversal Together, these data suggest that SOX3 and SRY are functionally interchangeable m sex determination and support the notion that SRY evolved from SOX3 via a regulatory mutation that led to its de novo expression in the early gonad.

Original languageEnglish
Pages (from-to)328-341
Number of pages14
JournalThe Journal of Clinical Investigation
Volume121
Issue number1
Early online date22 Dec 2010
DOIs
Publication statusPublished - 4 Jan 2011

Funding

The authors thank Peter Koopman and Josephine Bowles for sharing unpublished data and useful discussions, Terry Speed for assistance with microarray analysis, and Frank Grutzner for critical reading of the manuscript We also thank Sandra Piltz, Mizuho Mamiya, Rhonda Hutchinson, Julie Scott, and the staff of the University of Adelaide Laboratory Animal Services for technical assistance The authors also thank Tiago Rocha for patient A's clinical evaluation and the staff of Unidade de Citogenerica of Instituto Nacional de Saude Ricardo Jorge for the chromosome analysis, as well as the contribution of the patients Involved in the study We gratefully acknowledge funding support from the Australian Research Council (P Thomas), the Australian National Health and Medical Research Council (P Thomas, S White, A Sinclair, and V Harley), the UK Medical Research Council (U117512772) (R Lovell Badge), the Helen Macpherson Smith Trust (A Sinclair), the Fundacao para a Ciencia e a Tecnologia (FCT, POCTI/SAU/97/2001) and the Centro de Investigacao em Genetica Molecular Humana da Universidade Nova de Lisboa (J Goncalves), the Doris Duke Charitable Foundation (E Vilain), and the Louis Jeantet Foundation (R. Lovell Badge) Paul Thomas is a Pfizer Australia Research Fellow

Keywords

  • beta-catenin
  • testis-determining gene
  • sertoli-cells
  • retinoic acid
  • sry expression
  • mammalian sex
  • mental-retardation
  • cell precursors
  • linked hypopituitarism
  • determining region

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