The transcription factor SOX30 is a key regulator of mouse spermiogenesis

Abstract

The postmeiotic development of male germ cells, also known as spermiogenesis, features the coordinated expression of a large number of spermatid-specific genes. However, only a limited number of key transcription factors have been identified and the underlying regulatory mechanisms remain largely unknown. Here, we report that SOX30, the most-divergent member of the Sry-related high-motility group box (SOX) family of transcription factors, is essential for mouse spermiogenesis. The SOX30 protein was predominantly expressed in spermatids, while its transcription was regulated by retinoic acid and by MYBL1 before and during meiosis. knockout mice arrested spermiogenesis at step 3 round spermatids, which underwent apoptosis and abnormal chromocenter formation. We also determined that SOX30 regulated the expression of hundreds of spermatid-specific protein-coding and long non-coding RNA genes. SOX30 bound to the proximal promoter of its own gene and activated its transcription. These results reveal SOX30 as a novel key regulator of spermiogenesis that regulates its own transcription to enforce and activate this meiotic regulatory pathway.

Transcription of the Sox30 Gene Is Positively Regulated by Dmrt1 in Nile Tilapia

“…Sox30 is a member of the Sox transcription factor family and exists in many animals, including teleosts and mammals [2,9,30]. It has been demonstrated in mouse that the Sox30 gene is predominantly expressed in testis and Sox30 knockout results in an abnormal spermiogenesis [7,8]. In the present study, we observed in Nile tilapia that the Sox30 gene is expressed in epithelial cells of the intratesticular efferent duct of the testis.…”

“…Sox30 is the only member of group H of the Sox family and exists widely among the animal kingdom [2,3,4,5], including human ( Homo sapiens ), mouse ( Mus musculus ), chicken ( Gallus gallus ), Nile tilapia, the channel catfish ( Ictalurus punctatus ), guppy ( Poecilia reticulata ), fathead minnow ( Pimephales promelas ), little skate ( Leucoraja erinacea ), dogfish ( Squalus acanthias ), lancelets ( Branchiotoma belcheri ), and elephant shark ( Callorhinchus milii ). Although the roles of the Sox30 protein in teleost are currently unclear, recent studies in mouse have demonstrated that Sox30 is involved in spermiogenesis and Sox30 knockout results in abnormality in germ cell development and a complete arrest of spermiogenesis [6,7,8].…”

“…In Nile tilapia, Sox30 is highly expressed in the testis at 90 days after hatching (dah) and 180 dah, especially in the sperms [4,9]. Similarly, mouse Sox30 is predominantly expressed in spermatocytes and round spermatids of the male germ cells during spermiogenesis in testis [7,8]. Previous studies reported that mouse Sox30 gene is transcriptionally regulated by retinoic acid and by the transcription factor MYBL1 [8,10].…”

“…Similarly, mouse Sox30 is predominantly expressed in spermatocytes and round spermatids of the male germ cells during spermiogenesis in testis [7,8]. Previous studies reported that mouse Sox30 gene is transcriptionally regulated by retinoic acid and by the transcription factor MYBL1 [8,10]. However, the regulatory mechanism underlying the male-biased expression of the Sox30 gene in animals remains largely unknown.…”

Role of SOX Protein Groups F and H in Lung Cancer Progression

“…The SOX30 protein (SRY-box containing gene 30), the only member of group H, has been characterized briefly only in a few species so far. SOX30 has been isolated from mice, humans and Nile tilapis, and it has been connected with mammalian spermatogonial differentiation and spermatogenesis [69][70][71][72]. Recently, it has been demonstrated that the SOX30 protein could be a novel epigenetic silenced tumor suppressor that acts through the direct regulation of p53 in human lung cancer [73,74].…”