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A Novel MSMB-Related Microprotein in the Postovulatory Egg Coats of Marsupials Stephen Frankenberg*, Jane Fenelon, Bonnie Dopheide, Geoff Shaw and Marilyn B Renfree

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A Novel MSMB-Related Microprotein in the Postovulatory Egg Coats of Marsupials Stephen Frankenberg*, Jane Fenelon, Bonnie Dopheide, Geoff Shaw and Marilyn B Renfree Frankenberg et al. BMC Evolutionary Biology 2011, 11:373 http://www.biomedcentral.com/1471-2148/11/373 RESEARCHARTICLE Open Access A novel MSMB-related microprotein in the postovulatory egg coats of marsupials Stephen Frankenberg*, Jane Fenelon, Bonnie Dopheide, Geoff Shaw and Marilyn B Renfree Abstract Background: Early marsupial conceptuses differ markedly from those of eutherian mammals, especially during cleavage and early blastocyst stages of development. Additionally, in marsupials the zona pellucida is surrounded by two acellular layers, the mucoid coat and shell, which are formed from secretions from the reproductive tract. Results: We report the identification of a novel postovulatory coat component in marsupials, which we call uterinesecreted microprotein (USM). USM belongs to a family of disulfide-rich microproteins of unconfirmed function that is found throughout deuterostomes and in some protostomes, and includes b-microseminoprotein (MSMB) and prostate-associated microseminoprotein (MSMP). We describe the evolution of this family in detail, including USM-related sequences in other vertebrates. The orthologue of USM in the tammar wallaby, USM1,is expressed by the endometrium with a dynamic temporal profile, possibly under the control of progesterone. Conclusions: USM appears to have evolved in a mammalian ancestor specifically as a component of the postovulatory coats. By analogy with the known properties of MSMB, it may have roles in regulating sperm motility/survival or in the immune system. However, its C-terminal domain is greatly truncated compared with MSMB, suggesting a divergent function. Background before birth [6], under the influence of proteases Marsupial conceptuses are surrounded by three extracel- secreted by the endometrium [7], after which attach- lular investments (reviewed [1]). The innermost layer, ment occurs. the zona pellucida, is deposited during oogenesis and A previous study [2] made substantial progress in occurs in all mammals. After ovulation and fertilisation, identifying components of the postovulatory coats of the it becomes surrounded by a thick, translucent layer brushtail possum (Trichosurus vulpecula) and the stripe- mucoid coat that is deposited during passage through faced dunnart (Sminthopsis macroura). The authors iso- the oviduct and traps non-fertilising sperm. By the time lated individual protein components by electrophoresis the conceptus arrives in the uterus, the mucoid coat has and sequenced their N-terminal regions. The short become surrounded by a thin, dense, shell coat derived sequences obtained (12-15 residues) for twelve excised mainly from secretions in the utero-tubal junction and protein bands (seven from possum and five from dun- the uterus [2-4]. During the period we define as “preli- nart) could not initially be identified due to insufficient minary blastocyst expansion”, the mucoid coat narrows bioinformatic resources for these species at the time. as it becomes compressed between the expanding zona Since that study, one band was identified as similar to τ- pellucida and the outer shell coat. During “secondary crystallin/enolase 1 and termed CP4 (coat protein 4) [8]. expansion”, the shell coat itself expands from an initial Genomes have now been sequenced from two marsu- diameter of about 200-300 μmupto~17mm,increas- pials - the South American grey short-tailed opossum ing its volume dramatically from 0.001 mm3 to > 0.250 (Monodelphis domestica) [9], and more recently the mm3 [5]. The shell coat finally ruptures approximately Australian tammar wallaby (Macropus eugenii)(in two-thirds of the way through pregnancy, or 3-8 days press). With these new resources at hand, we re-exam- ined the published protein sequences of Casey et al. [2] * Correspondence: [email protected] and identified one of them from the brushtail possum. ARC Centre of Excellence for Kangaroo Genomics and Department of We show that the gene encoding this protein, which we Zoology, University of Melbourne, Parkville, Victoria, Australia © 2011 Frankenberg et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Frankenberg et al. BMC Evolutionary Biology 2011, 11:373 Page 2 of 13 http://www.biomedcentral.com/1471-2148/11/373 call uterinesecreted microprotein (USM)isaparalogue of MSMB (b-microseminoprotein; also called PSP94, b- band 3 (~22 kDa): inhibin and IgBF). MSMB is a disulfide-rich, low mole- P Y R G Y Y D F Y cular weight protein that is a major component of semi- H F K H N D V D A nal fluid and is strongly expressed in the prostate gland F R W E L L as well as in other tissues, especially of the reproductive D H system and in mucosal membranes. Its specific function N is not known, but it may have roles in inhibition of sperm motility [10,11], suppression of immune response band 4 (~17 ka): against allogeneic sperm [12], toxin defence [13,14], pituitary-gonadal axis signalling [15-17] and suppression S D R Y A V D – P A D – D P N of prostate tumorigenesis [18-22]. Very little is known A H Y W E N L T F Y T N P K of MSMP, which is similar to MSMB but more highly E I F L N T F A V R conserved among species, apart from its expression in a prostate cancer cell line [23]. USM is similar to both band 5 (~14 kDa): MSMB and MSMP in its conserved sequence of disul- A – Y R E N L D F A T N P V G fide bond-forming cysteine residues, but most of the W Y R E N L D F A T N P V G region homologous to the C-terminal domain of MSMB E N L F A T P is absent. In this study, we examine the evolution of USM/MSMB/MSMP-related microproteins in verte- A C Y R E N L D F A T N P V G brates. We discuss how, as a component of the marsu- possum EST (accession EG617409) pial postovulatory coats, USM could provide important Figure 1 Identification of a brushtail possum coat protein clues for elucidating the roles of MSMB and other component from published sequences. Published sequences related proteins, with possible applications in prostate (boxed) of electrophoresed protein bands from possum cancer, immunity and fertility control. postovulatory coats [2] are aligned with a translation of brushtail possum expressed sequence tag (EST), GenBank accession EG617409, highlighted in blue. Aligned residues between the Results & Discussion translated EST and the major sequence of band 5 are shown in red. Identification of postovulatory coat proteins Additional residues within the sub-sequences of bands 3-5 that also Protein sequences from Casey et al [2] were used to match the EST are shown in green. In bands 3 and 5, these are one search GenBank databases using the tBLASTn algorithm residue out of phase. The approximate molecular weights indicated are those estimated by Casey et al. [2]. with low-stringency search parameters. The alignments of sequences from Casey et al [2] with an expressed sequence tag [GenBank accession EG617409] derived the third exon of another gene, WASH1. To resolve this from the reproductive tract of the brushtail possum is discrepancy and to characterise fully the genomic locus shown in Figure 1. The major sequence from Band 5 of tammar USM1, we isolated and sequenced a tammar (14 kDa) matched closely the translated possum EST, genomic BAC clone containing the gene. In a single while minor sequences from Bands 3 (22 kDa), 4 (17 assembled 89.8-kb contig of BAC sequence [GenBank kDa) and 5 also showed identity. We named this protein accession JN251945], no sequence matching the “first uterine secreted microprotein (USM). exon” of the brushtail possum EST was present in the The translated sequence of the possum EST was used 17.1 kb upstream of Exon 2, however Exon 1 as identi- to identify exons in the tammar wallaby (Macropus fied by 5’ RACE was located upstream of Exon 2, as eugenii) whole genome shotgun (WGS) database, which expected. USM2 was located downstream of USM1 in revealed an apparent four-exon structure with an open the BAC sequence and in the same orientation. USM2 reading frame spanning Exons 2-4 (Figure 2). A second, also contains exons homologous to Exons 1-4 (Figure more divergent homologue was also identified bioinfor- 3). We conclude that the “first exon” of the brushtail matically. We refer to these genes respectively as tam- possum EST represents an anomaly or an artefact of mar USM1 and USM2. Conserved exons in the cDNA library construction. Downstream of USM2 and opossum genome were identified as a homologue of in the same orientation as USM1 and USM2 in the BAC USM. sequence, we identified the first 8 exons of ELP3 (Figure Exon 1 of tammar USM1 was determined by 5’ RACE 3), which also flanks USM in the opossum genome. This anddifferedfromthatofthebrushtailpossumEST.In confirmedthatopossumUSM is orthologous to the the opossum genome, Exons 2-4 of the brushtail pos- tammar USM1/USM2 cluster. However, unlike in the sum EST map to Chromosome 1 whereas the “first tammar, no duplicate of USM was found at this locus in exon” maps to Chromosome 8, immediately upstream of the opossum. Frankenberg et al. BMC Evolutionary Biology 2011, 11:373 Page 3 of 13 http://www.biomedcentral.com/1471-2148/11/373 Exon 1 M E R L I G L M L L S T F L A L A H G Exon 2 Q C Y R G N F D I A M N S E D P R R M C L D T V Exon 3 D N K A Y K L G D T W L N S Q C Q R C S C T P M G V R C C E S H N P C A * Exon 4 Figure 2 Sequence and translation of tammar USM1 and opossum USM aligned with brushtail possum EST.
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