Identification of differentially expressed placental transcripts during multiple gestations in the Eurasian beaver (Castor fiber L.)
A. Lipka A B E , L. Paukszto C , M. Majewska D , J. P. Jastrzebski C , K. Myszczynski C , G. Panasiewicz A and B. Szafranska A
+ Author Affiliations
- Author Affiliations
A Department of Animal Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego Str 1A, 10-719 Olsztyn-Kortowo, Poland.
B Department of Gynecology and Obstetrics, Faculty of Medical Sciences, University of Warmia and Mazury in Olsztyn, Niepodleglosci Str 44, 10-045 Olsztyn, Poland.
C Department of Plant Physiology, Genetics and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego Str 1A, 10-719 Olsztyn-Kortowo, Poland.
D Department of Human Physiology, Faculty of Medical Sciences, University of Warmia and Mazury in Olsztyn, Warszawska Str 30, 10-082 Olsztyn, Poland.
E Corresponding author. Email: aleksandra.lipka@uwm.edu.pl
Reproduction, Fertility and Development 29(10) 2073-2084 https://doi.org/10.1071/RD16186
Submitted: 4 May 2016 Accepted: 22 December 2016 Published: 14 February 2017
Abstract
The Eurasian beaver is one of the largest rodents that, despite its high impact on the environment, is a non-model species that lacks a reference genome. Characterising genes critical for pregnancy outcome can serve as a basis for identifying mechanisms underlying effective reproduction, which is required for the success of endangered species conservation programs. In the present study, high-throughput RNA sequencing (RNA-seq) was used to analyse global changes in the Castor fiber subplacenta transcriptome during multiple pregnancy. De novo reconstruction of the C. fiber subplacenta transcriptome was used to identify genes that were differentially expressed in placentas (n = 5) from two females (in advanced twin and triple pregnancy). Analyses of the expression values revealed 124 contigs with significantly different expression; of these, 55 genes were identified using MegaBLAST. Within this group of differentially expressed genes (DEGs), 18 were upregulated and 37 were downregulated in twins. Most DEGs were associated with the following gene ontology terms: cellular process, single organism process, response to stimulus, metabolic process and biological regulation. Some genes were also assigned to the developmental process, the reproductive process or reproduction. Among this group, four genes (namely keratin 19 (Krt19) and wingless-type MMTV integration site family – member 2 (Wnt2), which were downregulated in twins, and Nik-related kinase (Nrk) and gap junction protein β2 (Gjb2), which were upregulated in twins) were assigned to placental development and nine (Krt19, Wnt2 and integrin α7 (Itga7), downregulated in twins, and Nrk, gap junction protein β6 (Gjb6), GATA binding protein 6 (Gata6), apolipoprotein A-I (ApoA1), apolipoprotein B (ApoB) and haemoglobin subunit α1 (HbA1), upregulated in twins) were assigned to embryo development. The results of the present study indicate that the number of fetuses affects the expression profile in the C. fiber subplacental transcriptome. Enhancement of transcriptomic resources for C. fiber will improve understanding of the pathways relevant to proper placental development and successful reproduction.
Additional keywords: de novo assembly, differentially expressed genes, pregnancy, RNA-seq.
References
Anders, S., and Huber, W. (2010). Differential expression analysis for sequence count data. Genome Biol. 11, R106.| Differential expression analysis for sequence count data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVahs7bI&md5=5bd2b28833da875127c6adf43696eb0cCAS |
Bolger, A. M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120.
| Trimmomatic: a flexible trimmer for Illumina sequence data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1Sqt7nP&md5=a6c0b57a945e2b659558345abad1cee0CAS |
Brown, Z. A., Schalekamp-Timmermans, S., Tiemeier, H. W., Hofman, A., Jaddoe, V. W., and Steegers, E. A. (2014). Fetal sex specific differences in human placentation: a prospective cohort study. Placenta 35, 359–364.
| Fetal sex specific differences in human placentation: a prospective cohort study.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cnisV2ksQ%3D%3D&md5=f59f1415dac7b862ca40d4bb1600f122CAS |
Buckberry, S., Bianco-Miotto, T., Bent, S. J., Dekker, G. A., and Roberts, C. T. (2014). Integrative transcriptome meta-analysis reveals widespread sex-biased gene expression at the human fetal–maternal interface. Mol. Hum. Reprod. 20, 810–819.
| Integrative transcriptome meta-analysis reveals widespread sex-biased gene expression at the human fetal–maternal interface.Crossref | GoogleScholarGoogle Scholar |
Burkin, H. R., Rice, M., Sarathy, A., Thompson, S., Singer, C. A., and Buxton, I. L. (2013). Integrin upregulation and localization to focal adhesion sites in pregnant human myometrium. Reprod. Sci. 20, 804–812.
| Integrin upregulation and localization to focal adhesion sites in pregnant human myometrium.Crossref | GoogleScholarGoogle Scholar |
Carter, A. M. (2000). Placental oxygen consumption. Part I: in vivo studies. A review. Placenta 21, S31–S37.
| Placental oxygen consumption. Part I: in vivo studies. A review.Crossref | GoogleScholarGoogle Scholar |
Cleal, J. K., Day, P. L., Hanson, M. A., and Lewis, R. M. (2010). Sex differences in the mRNA levels of housekeeping genes in human placenta. Placenta 31, 556–557.
| Sex differences in the mRNA levels of housekeeping genes in human placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVWru7o%3D&md5=2554c4076dbb64ed49c4e48de0473f94CAS |
Conesa, A., Götz, S., Garcia-Gomez, J. M., Terol, J., Talon, M., and Robles, M. (2005). Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676.
| Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpvFGqt70%3D&md5=f0eb182d91a46c036310171c6b2a8efeCAS |
Cross, J. C., Baczyk, D., Dobric, N., Hemberger, M., Hughes, M., Simmons, D. G., Yamamoto, H., and Kingdom, J. C. (2003). Genes, development and evolution of the placenta. Placenta 24, 123–130.
| Genes, development and evolution of the placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptlOmtw%3D%3D&md5=08b4c079ea5a521a44812f0a1d9cd439CAS |
Denda, K., Nakao-Wakabayashi, K., Okamoto, N., Kitamura, N., Ryu, J. Y., Tagawa, Y., Ichisaka, T., Yamanaka, S., and Komada, M. (2011). Nrk, an X-linked protein kinase in the germinal center kinase family, is required for placental development and fetoplacental induction of labor. J. Biol. Chem. 286, 28 802–28 810.
| Nrk, an X-linked protein kinase in the germinal center kinase family, is required for placental development and fetoplacental induction of labor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVWgsbzF&md5=a0209a0ad193b764787d0096ec456824CAS |
Du, Z.-Q., Eisley, C. J., Onteru, S. K., Madsen, O., Groenen, M. A. M., Ross, J. W., and Rothschild, M. F. (2014). Identification of species-specific novel transcripts in pig reproductive tissues using RNA-seq. Anim. Genet. 45, 198–204.
| Identification of species-specific novel transcripts in pig reproductive tissues using RNA-seq.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjvVyht74%3D&md5=29b6088f33aa515f792c21ef88384e72CAS |
Ducroz, J.-F., Stubbe, M., Saveljev, A. P., Heidecke, D., Samjaa, R., Ulevičius, A., Stubbe, A., and Durka, W. (2005). Genetic variation and population structure of the Eurasian beaver Castor fiber in Eastern Europe and Asia. J. Mammal. 86, 1059–1067.
| Genetic variation and population structure of the Eurasian beaver Castor fiber in Eastern Europe and Asia.Crossref | GoogleScholarGoogle Scholar |
Eriksson, J. G., Kajantie, E., Osmond, C., Thornburg, K., and Barker, D. J. (2010). Boys live dangerously in the womb. Am. J. Hum. Biol. 22, 330–335.
| Boys live dangerously in the womb.Crossref | GoogleScholarGoogle Scholar |
Fischer, T. V. (1971). Placentation in the American beaver (Castor canadensis). Am. J. Anat. 131, 159–183.
| Placentation in the American beaver (Castor canadensis).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE3M7ovFeqtg%3D%3D&md5=d8cb00816c11a0706001947934a2c6d6CAS |
Forsén, T., Eriksson, J. G., Tuomilehto, J., Osmond, C., and Barker, D. J. (1999). Growth in utero and during childhood among women who develop coronary heart disease: longitudinal study. BMJ 319, 1403–1407.
| Growth in utero and during childhood among women who develop coronary heart disease: longitudinal study.Crossref | GoogleScholarGoogle Scholar |
Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., di Palma, F., Birren, B. W., Nusbaum, C., Lindblad-Toh, K., Friedman, N., and Regev, A. (2011). Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat. Biotechnol. 29, 644–652.
| Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtV2hsbc%3D&md5=43827cd1bd78437a7c10243bf8f6e142CAS |
Gupta, S., Fox, N. S., Feinberg, J., Klauser, C. K., and Rebarber, A. (2015). Outcomes in twin pregnancies reduced to singleton pregnancies compared with ongoing twin pregnancies. Am. J. Obstet. Gynecol. 213, 580.e1–580.e5.
| Outcomes in twin pregnancies reduced to singleton pregnancies compared with ongoing twin pregnancies.Crossref | GoogleScholarGoogle Scholar |
Haas, B. J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P. D., Bowden, J., Couger, M. B., Eccles, D., Li, B., Lieber, M., MacManes, M. D., Ott, M., Orvis, J., Pochet, N., Strozzi, F., Weeks, N., Westerman, R., William, T., Dewey, C. N., Henschel, R., Leduc, R. D., Friedman, N., and Regev, A. (2013). De novo transcript sequence reconstruction from RNA-Seq: reference generation and analysis with Trinity. Nat. Protoc. 8, 1494–1512.
| De novo transcript sequence reconstruction from RNA-Seq: reference generation and analysis with Trinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVyrsLvF&md5=3b4fe2e991cbf90f58688d192ec6c758CAS |
Haas, J., Barzilay, E., Hourvitz, A., Dor, J., Lipitz, S., Yinon, Y., Shlomi, M., and Shulman, A. (2016). Outcome of early versus late multifetal pregnancy reduction. Reprod. Biomed. Online , .
| Outcome of early versus late multifetal pregnancy reduction.Crossref | GoogleScholarGoogle Scholar |
Halley, D. J., and Rosell, F. (2002). The beaver’s reconquest of Eurasia: status, population development and management of a conservation success. Mamm. Rev. 32, 153–178.
| The beaver’s reconquest of Eurasia: status, population development and management of a conservation success.Crossref | GoogleScholarGoogle Scholar |
Hasson, J., Shapira, A., Many, A., Jaffa, A., and Har-Toov, J. (2011). Reduction of twin pregnancy to singleton: does it improve pregnancy outcome? J. Matern. Fetal Neonatal Med. 24, 1362–1366.
| Reduction of twin pregnancy to singleton: does it improve pregnancy outcome?Crossref | GoogleScholarGoogle Scholar |
Hou, Z.-C., Sterner, K. N., Romero, R., Than, N. G., Gonzalez, J. M., Weckle, A., Xing, J., Benirschke, K., Goodman, M., and Wildman, D. E. (2012). Elephant transcriptome provides insights into the evolution of eutherian placentation. Genome Biol. Evol. 4, 713–725.
| Elephant transcriptome provides insights into the evolution of eutherian placentation.Crossref | GoogleScholarGoogle Scholar |
Jauniaux, E., Watson, A. L., Hempstock, J., Bao, Y. P., Skepper, J. N., and Burton, G. J. (2000). Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am. J. Pathol. 157, 2111–2122.
| Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsVOjtw%3D%3D&md5=55c8282a0c0ac5a3812d148ca88b4bb9CAS |
Kakinuma, H., Inomata, H., and Kitamura, N. (2005). Enhanced JNK activation by NESK without kinase activity upon caspase-mediated cleavage during apoptosis. Cell. Signal. 17, 1439–1448.
| Enhanced JNK activation by NESK without kinase activity upon caspase-mediated cleavage during apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXptVWnsbc%3D&md5=1dc5ae81ef06e77449c3ef7f3e4fdafeCAS |
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Mentjies, P., and Drummond, A. (2012). Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.
| Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar |
Kiewisz, J., Wasniewski, T., and Kmiec, Z. (2015). Participation of WNT and β-catenin in physiological and pathological endometrial changes: association with angiogenesis. Biomed. Res. Int. 2015, 854056.
Kim, J., Zhao, K., Jiang, P., Lu, Z.-X., Wang, J., Murray, J. C., and Xing, Y. (2012). Transcriptome landscape of the human placenta. BMC Genomics 13, 115.
| Transcriptome landscape of the human placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XovVeitb0%3D&md5=dc288b299a6972ce70c022d188cf776bCAS |
Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., Jones, S. J., and Marra, M. A. (2009). Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639–1645.
| Circos: an information aesthetic for comparative genomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFCjsLvJ&md5=bac0f34dcdc2d3a75d581a905d3c5970CAS |
Langmead, B., Trapnell, C., Pop, M., and Salzberg, S. L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25–R25.10.
| Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.Crossref | GoogleScholarGoogle Scholar |
LaVoie, H. A., McCoy, G. L., and Blake, C. A. (2004). Expression of the GATA-4 and GATA-6 transcription factors in the fetal rat gonad and in the ovary during postnatal development and pregnancy. Mol. Cell. Endocrinol. 227, 31–40.
| Expression of the GATA-4 and GATA-6 transcription factors in the fetal rat gonad and in the ovary during postnatal development and pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVKrtLw%3D&md5=8c97361ed46910dc877d5f5f3b4443f0CAS |
Lenz, P. H., Roncalli, V., Hassett, R. P., Wu, L.-S., Cieslak, M. C., Hartlin, D. K., and Christie, A. E. (2014). De novo assembly of a transcriptome for Calanus finmarchicus (Crustacea, Copepoda). The dominant zooplankter of the North Atlantic Ocean. PLoS One 9, e88589.
| De novo assembly of a transcriptome for Calanus finmarchicus (Crustacea, Copepoda). The dominant zooplankter of the North Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |
Li, B., and Dewey, C. N. (2011). RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323–339.
| RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFajtLvM&md5=8aaf2cec49ad8fad78ae143eaa1a5e3aCAS |
Lin, X., Xu, Q., and Veenstra, R. D. (2014). Functional formation of heterotypic gap junction channels by connexins-40 and -43. Channels 8, 433–443.
| Functional formation of heterotypic gap junction channels by connexins-40 and -43.Crossref | GoogleScholarGoogle Scholar |
Lopez, W., Gonzalez, J., Liu, Y., Harris, A. L., and Contreras, J. E. (2013). Insights on the mechanisms of Ca(2+) regulation of connexin26 hemichannels revealed by human pathogenic mutations (D50N/Y). J. Gen. Physiol. 142, 23–35.
| Insights on the mechanisms of Ca(2+) regulation of connexin26 hemichannels revealed by human pathogenic mutations (D50N/Y).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtF2qtr7E&md5=05b1bb3228e0e2200873f0171cd31f0eCAS |
Misra, D. P., Salafia, C. M., Miller, R. K., and Charles, A. K. (2009). Non-linear and gender-specific relationships among placental growth measures and the fetoplacental weight ratio. Placenta 30, 1052–1057.
| Non-linear and gender-specific relationships among placental growth measures and the fetoplacental weight ratio.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MjotVyjtA%3D%3D&md5=d35531d80ff0802d3ad9a209a8497a7dCAS |
Moll, R., Franke, W. W., Schiller, D. L., Geiger, B., and Krepler, R. (1982). The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells. Cell 31, 11–24.
| The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhtlSjsw%3D%3D&md5=b34b5532e3dbcb2dc264bc4e50eb4062CAS |
Mossman, H. W. (1987). ‘Vertebrate Fetal Membranes.’ (MacMillan: Basingstoke, UK.)
Mossman, H. W. (1991). Classics revisited: comparative morphogenesis of the fetal membranes and accessory uterine structures. Placenta 12, 1–5.
| Classics revisited: comparative morphogenesis of the fetal membranes and accessory uterine structures.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M3jvFCjug%3D%3D&md5=d97e2e0a43474251067da33046cfa912CAS |
Müler-Schwarze, D. (2011). ‘The Beaver: Its Life and Impact.’ (Cornell University Press: Ithaca NY.)
Nolet, B. A. (1997). ‘Management of the Beaver (Castor fiber): Towards Restoration of its Former Distribution and Ecological Function in Europe.’ Council of Europe/Convention on the Conservation of European Wildlife and Natural Habitats Bern Convention Nature & Environment Series 86. (Council of Europe Publishing: Strasbourg.)
Nolet, B. A., and Rosell, F. (1998). Comeback of the beaver Castor fiber: an overview of old and new conservation problems. Biol. Conserv. 83, 165–173.
| Comeback of the beaver Castor fiber: an overview of old and new conservation problems.Crossref | GoogleScholarGoogle Scholar |
Riesgo, A., Andrade, S. C., Sharma, P. P., Novo, M., Pérez-Porro, A. R., Vahtera, V., González, V. L., Kawauchi, G. Y., and Giribet, G. (2012). Comparative description of ten transcriptomes of newly sequenced invertebrates and efficiency estimation of genomic sampling in non-model taxa. Front. Zool. 9, 33–57.
| Comparative description of ten transcriptomes of newly sequenced invertebrates and efficiency estimation of genomic sampling in non-model taxa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlsVWjsbg%3D&md5=aea415b8832f04eb28280a2c1ebeeb93CAS |
Robinson, M. D., McCarthy, D. J., and Smyth, G. K. (2010). Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140.
| Bioconductor package for differential expression analysis of digital gene expression data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1WlurvO&md5=d93e78ef4346789f93b9c53f55f6456fCAS |
Romanenko, S. A., Perelman, P. L., Trifonov, V. A., and Graphodatsky, A. S. (2012). Chromosomal evolution in Rodentia. Heredity 108, 4–16.
| Chromosomal evolution in Rodentia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38%2FmsFeiuw%3D%3D&md5=f4cbb7de8a1dde7994da8c4767ae6fa0CAS |
Ross, T. D., Coon, B. G., Yun, S., Baeyens, N., Tanaka, K., Ouyang, M., and Schwartz, M. A. (2013). Integrins in mechanotransduction. Curr. Opin. Cell Biol. 25, 613–618.
| Integrins in mechanotransduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVWgu7bJ&md5=1d659da1f65089a2ceef47f53988b595CAS |
Saben, J., Zhong, Y., McKelvey, S., Dajani, N. K., Andres, A., Badger, T. M., Gomez-Acevedo, H., and Shankar, K. (2014). A comprehensive analysis of the human placenta transcriptome. Placenta 35, 125–131.
| A comprehensive analysis of the human placenta transcriptome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVWjtbnJ&md5=3224a524944516dd4c1a7c0de36c65e4CAS |
Sedlmeier, E. M., Brunner, S., Much, D., Pagel, P., Ulbrich, S. E., Meyer, H. H., Amann-Gassner, U., Hauner, H., and Bader, B. L. (2014). Human placental transcriptome shows sexually dimorphic gene expression and responsiveness to maternal dietary n-3 long-chain polyunsaturated fatty acid intervention during pregnancy. BMC Genomics 15, 941–959.
| Human placental transcriptome shows sexually dimorphic gene expression and responsiveness to maternal dietary n-3 long-chain polyunsaturated fatty acid intervention during pregnancy.Crossref | GoogleScholarGoogle Scholar |
Senn, H., Ogden, R., Frosch, C., Syrůčková, A., Campbell-Palmer, R., Munclinger, P., Durka, W., Kraus, R. H., Saveljev, A. P., Nowak, C., Stubbe, A., Stubbe, M., Michaux, J., Lavrov, V., Samiya, R., Ulevicius, A., and Rosell, F. (2014). Nuclear and mitochondrial genetic structure in the Eurasian beaver (Castor fiber). Implications for future reintroductions. Evol. Appl. 7, 645–662.
| Nuclear and mitochondrial genetic structure in the Eurasian beaver (Castor fiber). Implications for future reintroductions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVGktr3L&md5=4bb0d3f0fb82f581672aa191de2a3431CAS |
Shi, X., He, Z., Gao, Y., Luo, Y., Gou, C., and Fang, Q. (2014). Placental expression of PHLDA2 in selective intrauterine growth restriction in monozygotic twins. Placenta 35, 428–430.
| Placental expression of PHLDA2 in selective intrauterine growth restriction in monozygotic twins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXltl2ms7o%3D&md5=961e2fa95e3ca6f4787b91d972181e80CAS |
Soothill, P. W., Nicolaides, K. H., Bilardo, C. M., and Campbell, S. (1986). Relation of fetal hypoxia in growth retardation to mean blood velocity in the fetal aorta. Lancet 328, 1118–1120.
| Relation of fetal hypoxia in growth retardation to mean blood velocity in the fetal aorta.Crossref | GoogleScholarGoogle Scholar |
Steffen, K. M., Cooper, M. E., Shi, M., Caprau, D., Simhan, H. N., Dagle, J. M., Marazita, M. L., and Murray, J. C. (2007). Maternal and fetal variation in genes of cholesterol metabolism is associated with preterm delivery. J. Perinatol. 27, 672–680.
| Maternal and fetal variation in genes of cholesterol metabolism is associated with preterm delivery.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2snjtlGqsQ%3D%3D&md5=7a9ad4e06682aa529de5e86b2cf98cdcCAS |
Stewart, C. J., Crook, M. L., Lacey, J., and Louwen, K. (2011). Cytokeratin 19 expression in normal endometrium and in low-grade endometrioid adenocarcinoma of the endometrium. Int. J. Gynecol. Pathol. 30, 484–491.
| Cytokeratin 19 expression in normal endometrium and in low-grade endometrioid adenocarcinoma of the endometrium.Crossref | GoogleScholarGoogle Scholar |
Tempfer, C. B., Bancher-Todesca, D., Zeisler, H., Schatten, C., Husslein, P., and Gregg, A. R. (2000). Placental expression and serum concentrations of cytokeratin 19 in preeclampsia. Obstet. Gynecol. 95, 677–682.
| 1:CAS:528:DC%2BD3cXisFGntLk%3D&md5=45fe1ebdd524949f99fef7136ae973c1CAS |
Watson, E. D., and Cross, J. C. (2005). Development of structures and transport functions in the mouse placenta. Physiology (Bethesda) 20, 180–193.
| Development of structures and transport functions in the mouse placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXls1GgtrY%3D&md5=dd3231c5dbbc0e8691e51fdf45982ed7CAS |
Wildman, D. E., Chen, C., Erez, O., Grossman, L. I., Goodman, M., and Romero, R. (2006). Evolution of the mammalian placenta revealed by phylogenetic analysis. Proc. Natl Acad. Sci. USA 103, 3203–3208.
| Evolution of the mammalian placenta revealed by phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksF2kt7w%3D&md5=a1ea0f5a135554790f1c1b1dde9c7dceCAS |
Willey, A. (1914). Memoirs: The blastocyst and placenta of the beaver. J. Cell. Sci. s2–60, 175–249.
Wu, T. D., and Watanabe, C. K. (2005). GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21, 1859–1875.
| GMAP: a genomic mapping and alignment program for mRNA and EST sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsl2ntLw%3D&md5=1b963ac6e99fbcdc33efb8d943ae4f45CAS |
Zheng, S., Liu, J., Wu, Y., Huang, T. L., and Wang, G. (2015). Small-molecule inhibitors of Wnt signaling pathway: towards novel anticancer therapeutics. Future Med. Chem. 7, 2485–2505.
| Small-molecule inhibitors of Wnt signaling pathway: towards novel anticancer therapeutics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVeqt7fE&md5=bd206f07fffc9580ab7ddc200134a907CAS |
Zhu, F., Yuan, J. M., Zhang, Z. H., Hao, J. P., Yang, Y. Z., Hu, S. Q., Yang, F. X., Qu, L. J., and Hou, Z. C. (2015). De novo transcriptome assembly and identification of genes associated with feed conversion ratio and breast muscle yield in domestic ducks. Anim. Genet. 46, 636–645.
| De novo transcriptome assembly and identification of genes associated with feed conversion ratio and breast muscle yield in domestic ducks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvVWqs7jJ&md5=883bf1eb3ce39b139572510c37cc6c3cCAS |
Żurowski, W. (1992). Building activity of beavers. Acta Theriol. (Warsz.) 37, 403–411.
| Building activity of beavers.Crossref | GoogleScholarGoogle Scholar |
