STK31(TDRD8) is dynamically regulated throughout mouse spermatogenesis and interacts with MIWI protein

Bao, Jianqiang; Wang, Li; Lei, Jianbo; Hu, Yanqin; Liu, Yue; Shen, Hong‐Bin; Yan, Wei; Xu, Chen

doi:10.1007/s00418-011-0897-9

Cited by 24 publications

(30 citation statements)

References 46 publications

(65 reference statements)

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“…2001) and was reported to interact with MIWI, suggesting a role in miRNA biogenesis and spermatogenesis (Bao et al . 2012).…”

Section: Discussionmentioning

confidence: 99%

Identification of cell-specific targets of sumoylation during mouse spermatogenesis

Xiao¹,

Pollack²,

Andrusier³

et al. 2016

Reproduction

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Recent findings suggest diverse and potentially multiple roles of SUMO in testicular function and spermatogenesis. However, SUMO targets remain uncharacterized in the testis due to the complex multicellular nature of testicular tissue, the inability to maintain and manipulate spermatogenesis in vitro, and the technical challenges involved in identifying low-abundance endogenous SUMO targets. In this study, we performed cell-specific identification of sumoylated proteins using concentrated cell lysates prepared with de-sumoylation inhibitors from freshly purified spermatocytes and spermatids. One-hundred and twenty proteins were uniquely identified in the spermatocyte and/or spermatid fractions. The identified proteins are involved in the regulation of transcription, stress response, microRNA biogenesis, regulation of major enzymatic pathways, nuclear-cytoplasmic transport, cell cycle control, acrosome biogenesis, and other processes. Several proteins with important roles during spermatogenesis were chosen for further characterization by co-immunoprecipitation, co-localization and in-vitro sumoylation studies. GPS-SUMO software was used to identify consensus and non-consensus sumoylation sites within the amino acid sequences of the proteins. The analyses confirmed the cell-specific sumoylation and/or SUMO interaction of several novel, previously uncharacterized SUMO targets such as CDK1, RNAP II, CDC5, MILI, DDX4, TDP-43 and STK31. Furthermore, several proteins that were previously identified as SUMO targets in somatic cells (e.g., KAP1, MDC1) were identified as SUMO targets in germ cells. Many of these proteins have a unique role in spermatogenesis and during meiotic progression. This research opens a novel avenue for further studies of SUMO at the level of individual targets.

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“…2001) and was reported to interact with MIWI, suggesting a role in miRNA biogenesis and spermatogenesis (Bao et al . 2012).…”

Section: Discussionmentioning

confidence: 99%

Identification of cell-specific targets of sumoylation during mouse spermatogenesis

Xiao¹,

Pollack²,

Andrusier³

et al. 2016

Reproduction

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“…All immunofluorescent staining procedures were carried out essentially as described previously. 52 The rabbit polyclonal anti-mouse MIWI2 antibodies were generated in a company (GenScript, Piscataway, NJ, USA) by immunizing rabbits with a synthetic MIWI2 peptide (N 0 -GDGGRTFMERRGKGC-C 0 ) conjugated with a KLH adapter. The antibody dilutions used in this study were as follows: MIWI2: 1 : 500 dilution; ORF1: 1 : 1000 dilution (Rabbit, a kind gift from Dr. Alex Bortvin); IAP: 1 : 500 dilution (Rabbit, a kind gift from Dr. Bryan Cullen); gH2AX: 1 : 1000 dilution (Rabbit, Abcam, Cambridge, MA, USA).…”

Section: Discussionmentioning

confidence: 99%

Conditional inactivation of Miwi2 reveals that MIWI2 is only essential for prospermatogonial development in mice

Bao

Schuster

et al. 2014

Cell Death Differ

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The PIWI-piRNA pathway serves as a critical defense mechanism through which the genome of the male germline is protected from invasion by transposable elements (TEs). MIWI2/PIWIL4, a member of the murine PIWI subclade of the Argonaute family, has been shown to be expressed in primordial germ cells (PGCs) and prospermatogonia in fetal and prepubertal testes. Global inactivation of Miwi2 leads to male sterility due to an early meiotic arrest, which correlates with retrotransposon desuppression. However, it remains unclear whether MIWI2 functions beyond the PGC stage and whether MIWI2 has a role beyond TE suppression during male germ line development. Through conditional inactivation of Miwi2, we demonstrate herein that MIWI2 function is restricted to a narrow time window during male PGC reprograming and that Miwi2 is dispensable for postnatal male germline development and testicular function in mice. Moreover, persistent activation of LINE1 and IAP retrotransposons caused by Miwi2 inactivation is compatible with mitotic cell cycle progression of spermatogonia during the first wave of spermatogenesis, but can cause zygotene to pachytene arrest in early meiosis due to multiple defects including enhanced DNA double-strand breaks, aberrant histone modifications and altered mRNA transcriptome. Our data not only validate those from global Miwi2 KO studies, but also suggest that MIWI2 and MIWI2-associated piRNAs have functions beyond TE suppression. Cell Death and Differentiation (2014) 21, 783-796; doi:10.1038/cdd.2014; published online 24 January 2014The Argonaute family of proteins contains two subclasses, argonaute (AGO) and p-element induced wimpy testis (PIWI), both of which are highly conserved from plants to animals. 1The AGO subfamily members (for example, AGO1-4) are expressed ubiquitously in a wide range of tissues/cell types and function through associations with miRNAs and siRNAs.

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“…IP Followed by LC-MS. SPATA6 IP and LC-MS analyses were conducted as described previously with some modifications (52). Details are provided in SI Appendix, Materials and Methods.…”

Section: Methodsmentioning

confidence: 99%

Spata6is required for normal assembly of the sperm connecting piece and tight head–tail conjunction

Yuan

Stratton

Bao

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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116

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"Pinhead sperm," or "acephalic sperm," a type of human teratozoospermia, refers to the condition in which ejaculate contains mostly sperm flagella without heads. Family clustering and homogeneity of this syndrome suggests a genetic basis, but the causative genes remain largely unknown. Here we report that Spata6, an evolutionarily conserved testis-specific gene, encodes a protein required for formation of the segmented columns and the capitulum, two major structures of the sperm connecting piece essential for linking the developing flagellum to the head during late spermiogenesis. Inactivation of Spata6 in mice leads to acephalic spermatozoa and male sterility. Our proteomic analyses reveal that SPATA6 is involved in myosin-based microfilament transport through interaction with myosin subunits (e.g., MYL6).M ale gametes-spermatozoa-are produced in the testis through a process termed spermatogenesis, which can be divided into three phases: mitotic, meiotic, and haploid (1). In the mitotic phase, spermatogonial stem cells proliferate and differentiate into spermatogonia, which subsequently enter the meiotic phase and become spermatocytes. Spermatocytes undergo crossover, followed by two consecutive meiotic cell divisions to produce haploid spermatids. Spermatids then undergo a multistep differentiation process, also called spermiogenesis, to form spermatozoa. Severe disruptions in either the mitotic or the meiotic phase tend to cause azoospermia, whereas spermiogenic defects often lead to reduced sperm counts, aberrant sperm motility, and deformed spermatozoa, a condition termed oligoasthenoteratozoospermia (OAT) in humans (2, 3).OAT accounts for a significant proportion of male idiopathic infertility cases (2, 4). Numerous cases of acephalic spermatozoa have been reported in teratozoospermic patients (5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19). In these patients, the major anomaly lies in headless spermatozoa in the ejaculate, and the headless spermatozoa were initially called "pinhead sperm" because the investigators mistakenly regarded the retained cytoplasmic droplets, which are usually attached to the midprincipal piece junction of the flagella, as the heads of reduced size (8,13,14). Extensive ultrastructral studies on humans and animals with acephalic spermatozoa suggest that this condition results from defects in formation of the connecting piece of spermatozoa during late spermiogenesis, including failure for the proximal centrioles to attach normally to the caudal portion of the sperm nuclei, leading to abnormal head-midpiece alignment, or a nuclear defect that interferes with formation of the implantation fossa, the normal lodging site for the sperm proximal centriole (16). Aberrant formation of the connecting piece leads to independent development of the sperm heads and flagella, and eventually these structures become separated within the seminiferous tubules or during their transition through the seminal tract as a consequence of increased instability of the head-midpiece junction (16,18)....

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STK31(TDRD8) is dynamically regulated throughout mouse spermatogenesis and interacts with MIWI protein

Cited by 24 publications

References 46 publications

Identification of cell-specific targets of sumoylation during mouse spermatogenesis

Identification of cell-specific targets of sumoylation during mouse spermatogenesis

Conditional inactivation of Miwi2 reveals that MIWI2 is only essential for prospermatogonial development in mice

Spata6is required for normal assembly of the sperm connecting piece and tight head–tail conjunction

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