Origin and evolution of the TKDP gene family

Chakrabarty, Anindita; Green, Jonathan A.; Roberts, R. Michael

doi:10.1016/j.gene.2005.12.033

Cited by 7 publications

(13 citation statements)

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“…For example, the trophoblast cell derived pregnancy recognition factor IFN-is produced in mammals within the Ruminantia suborder (e.g., cattle, sheep, goats), but not in unrelated species (22). Recent identification of the trophoblast kunitz domain protein (TKDP) gene family specifically expressed in ruminants (23) further supports the concept that certain genes in the reproductive system may have Genomic DNA databases at the National Center for Biotechnology Information for human, chimpanzee, dog, mouse, rat, chicken, zebrafish, and Drosophila were searched with the nucleotide sequence of the 1.5-kb bovine JY-1 cDNA. JY-1-like sequences corresponding to exon 3 were identified on human Chr 11, chimpanzee Chr 11, dog Chr 21, mouse Chr 7, and rat Chr 1 (syntenic Chrs to human Chr 11).…”

Section: Discussionmentioning

confidence: 99%

JY-1 , an oocyte-specific gene, regulates granulosa cell function and early embryonic development in cattle

Bettegowda

Yao

Sen

et al. 2007

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

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Oocyte-specific gene products play a key role in regulation of fertility in mammals. Here, we describe the discovery, molecular characterization, and function of JY-1, a bovine oocyte-expressed gene shown to regulate both function of ovarian granulosa cells and early embryogenesis in cattle and characteristics of JY-1 loci in other species. The JY-1 gene encodes for a secreted protein with multiple mRNA transcripts containing an identical ORF but differing lengths of 3 UTR. JY-1 mRNA and protein are oocyte-specific and detectable throughout folliculogenesis. Recombinant JY-1 protein regulates function of follicle-stimulating hormone-treated ovarian granulosa cells, resulting in enhanced progesterone synthesis accompanied by reduced cell numbers and estradiol production. JY-1 mRNA of maternal origin is also present in early bovine embryos, temporally regulated during the window from meiotic maturation through embryonic genome activation, and is required for blastocyst development. The JY-1 gene has three exons and is located on bovine chromosome 29. JY-1-like sequences are present on syntenic chromosomes of other vertebrate species, but lack exons 1 and 2, including the protein-coding region, suggestive of species specificity in evolution and function of this oocyte-specific gene.T he oocyte is a key regulator of multiple aspects of female fertility, including ovarian follicular development and early embryogenesis (1). The advent of oocyte genomics and EST sequencing projects have led to a dramatic increase in our understanding about the identities and functions of oocytespecific genes in female reproduction (2, 3). However, inherent species-specific differences exist in the ovulation quota, follicular waves, duration of the ovarian cycle, and number of embryonic cell cycles required for embryonic genome activation (4) between the traditional animal model (polyovulatory mouse) versus monoovulatory species such as cattle and primates, including humans. Numerous examples suggest that oocytespecific genes identified in the mouse may not have identical functions in other species. For instance, Belclare and Cambridge ewes with naturally occurring heterozygous mutations in the GDF9 gene have an increased ovulation rate and litter size (5), but mice heterozygous for the GDF9 gene disruption exhibit no obvious phenotype (6). Similarly, Inverdale and Hanna strains of sheep with homozygous mutations in BMP15 are infertile (7, 8), whereas homozygous BMP15 mutant mice are subfertile with defects in ovulation and fertilization (9). Thus, comparative genomics approaches coupled to functional studies in nontraditional model systems are needed to address dissimilarities in transcriptome composition between model organisms and provide information on existence of genes or gene families that may play important regulatory roles in fertility in nonmurine models, including the human. With this goal in mind, we previously constructed a bovine oocyte cDNA library and sequenced a number of ESTs (2). A highly abundant transcript (designat...

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Section: Discussionmentioning

confidence: 99%

JY-1 , an oocyte-specific gene, regulates granulosa cell function and early embryonic development in cattle

Bettegowda

Yao

Sen

et al. 2007

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

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“…The trophoblast Kunitz domain proteins are a family of closely related gene products uniquely expressed by trophoblast of ruminant ungulates [1,2]. Each protein is characterized by the presence of a well-conserved, carboxyl-terminal ~65 amino acid domain, typically found in the Kunitz family of serine peptidase inhibitors.…”

Section: Introductionmentioning

confidence: 99%

“…The Kunitz domain is an evolutionary conserved module, existing in C. elegans , D. melanogaster , and all known vertebrates, that generally functions as a serine peptidase inhibitor, although functions unrelated to peptidase inhibition have also been documented [3-6]. This independently folding unit is preceded by one or more "repeat" sequences of ~80 amino acids of unknown function, which have similar but not identical sequences [1,2]. TKDPs represent one of the most abundant classes of secretory proteins produced by the conceptus during the peri-implantation period and throughout gestation [1,2,7,8].…”

Section: Introductionmentioning

confidence: 99%

“…This independently folding unit is preceded by one or more "repeat" sequences of ~80 amino acids of unknown function, which have similar but not identical sequences [1,2]. TKDPs represent one of the most abundant classes of secretory proteins produced by the conceptus during the peri-implantation period and throughout gestation [1,2,7,8]. Although the function of these proteins remains unclear, their unusually high expression at the interface between the maternal and fetal systems and the presence of conserved Kunitz units at their carboxyl termini strongly suggest an important role during pregnancy that relates to the evolution of the non-invasive placental type encountered in ruminant species.…”

Section: Introductionmentioning

confidence: 99%

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Chakrabarty

Roberts

2007

BMC Mol Biol

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Background: The trophoblast Kunitz domain proteins (TKDPs) constitute a highly expressed, placenta-specific, multigene family restricted to ruminant ungulates and characterized by a Cterminal "Kunitz" domain, preceded by one or more unique N-terminal domains. TKDP-1 shares an almost identical expression pattern with interferon-tau, the "maternal recognition of pregnancy protein" in ruminants. Our goal here has been to determine whether the ovine (ov) Tkdp-1 and IFNT genes possess a similar transcriptional code.

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“…The first exon encodes the signal- and pro-peptide, the second, a single Kunitz domain and the third, a short C-terminus. However, the TKDPs have a variable number of unique N domains inserted between the signal peptide and the Kunitz domain-encoding exon [50,51]. Genes that encode multiple Kunitz domains include: hepatocyte growth factor activator inhibitor 1 and 2 , also known as SPINT1 and SPINT2 respectively (two domains), tissue factor pathway inhibitor 1 and 2 (three domains); with up to 12 domains in the Ac-KPI-1 I nematode ( Ancylostoma caninum ) protein [38,43,44].…”

Section: Introductionmentioning

confidence: 99%

The mammary gland-specific marsupial ELP and eutherian CTI share a common ancestral gene

et al. 2012

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BackgroundThe marsupial early lactation protein (ELP) gene is expressed in the mammary gland and the protein is secreted into milk during early lactation (Phase 2A). Mature ELP shares approximately 55.4% similarity with the colostrum-specific bovine colostrum trypsin inhibitor (CTI) protein. Although ELP and CTI both have a single bovine pancreatic trypsin inhibitor (BPTI)-Kunitz domain and are secreted only during the early lactation phases, their evolutionary history is yet to be investigated.ResultsTammar ELP was isolated from a genomic library and the fat-tailed dunnart and Southern koala ELP genes cloned from genomic DNA. The tammar ELP gene was expressed only in the mammary gland during late pregnancy (Phase 1) and early lactation (Phase 2A). The opossum and fat-tailed dunnart ELP and cow CTI transcripts were cloned from RNA isolated from the mammary gland and dog CTI from cells in colostrum. The putative mature ELP and CTI peptides shared 44.6%-62.2% similarity. In silico analyses identified the ELP and CTI genes in the other species examined and provided compelling evidence that they evolved from a common ancestral gene. In addition, whilst the eutherian CTI gene was conserved in the Laurasiatherian orders Carnivora and Cetartiodactyla, it had become a pseudogene in others. These data suggest that bovine CTI may be the ancestral gene of the Artiodactyla-specific, rapidly evolving chromosome 13 pancreatic trypsin inhibitor (PTI), spleen trypsin inhibitor (STI) and the five placenta-specific trophoblast Kunitz domain protein (TKDP1-5) genes.ConclusionsMarsupial ELP and eutherian CTI evolved from an ancestral therian mammal gene before the divergence of marsupials and eutherians between 130 and 160 million years ago. The retention of the ELP gene in marsupials suggests that this early lactation-specific milk protein may have an important role in the immunologically naïve young of these species.

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Origin and evolution of the TKDP gene family

Cited by 7 publications

References 22 publications

JY-1 , an oocyte-specific gene, regulates granulosa cell function and early embryonic development in cattle

JY-1 , an oocyte-specific gene, regulates granulosa cell function and early embryonic development in cattle

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The mammary gland-specific marsupial ELP and eutherian CTI share a common ancestral gene

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