Secreted metabolome of porcine blastocysts encapsulated within in vitro 3D alginate hydrogel culture systems undergoing morphological changes provides insights into specific mechanisms involved in the initiation of porcine conceptus elongation
Sophie C. Walsh A , Jeremy R. Miles
B * , Corey D. Broeckling C , Lea A. Rempel B , Elane C. Wright-Johnson B and Angela K. Pannier A *
+ Author Affiliations
- Author Affiliations
A Department of Biological Systems Engineering, University of Nebraska-Lincoln, P.O. Box 830726, Lincoln, NE 68583, USA.
B USDA, U.S. Meat Animal Research Center, P.O. Box 166, Clay Center, NE 68933, USA.
C Bioanalysis and Omics Center, Colorado State University, Fort Collins, CO, USA.
Reproduction, Fertility and Development 35(5) 375-394 https://doi.org/10.1071/RD22210
Published online: 14 February 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Context: The exact mechanisms regulating the initiation of porcine conceptus elongation are not known due to the complexity of the uterine environment.
Aims: To identify contributing factors for initiation of conceptus elongation in vitro, this study evaluated differential metabolite abundance within media following culture of blastocysts within unmodified alginate (ALG) or Arg-Gly-Asp (RGD)-modified alginate hydrogel culture systems.
Methods: Blastocysts were harvested from pregnant gilts, encapsulated within ALG or RGD or as non-encapsulated control blastocysts (CONT), and cultured. At the termination of 96 h culture, media were separated into blastocyst media groups: non-encapsulated control blastocysts (CONT); ALG and RGD blastocysts with no morphological change (ALG− and RGD−); ALG and RGD blastocysts with morphological changes (ALG+ and RGD+) and evaluated for non-targeted metabolomic profiling by liquid chromatography (LC)–mass spectrometry (MS) techniques and gas chromatography–(GC–MS).
Key results: Analysis of variance identified 280 (LC–MS) and 1 (GC–MS) compounds that differed (P < 0.05), of which 134 (LC–MS) and 1 (GC–MS) were annotated. Metabolites abundance between ALG+ vs ALG−, RGD+ vs RGD−, and RGD+ vs ALG+ were further investigated to identify potential differences in metabolic processes during the initiation of elongation.
Conclusions: This study identified changes in phospholipid, glycosphingolipid, lipid signalling, and amino acid metabolic processes as potential RGD-independent mechanisms of elongation and identified changes in lysophosphatidylcholine and sphingolipid secretions during RGD-mediated elongation.
Implications: These results illustrate changes in phospholipid and sphingolipid metabolic processes and secretions may act as mediators of the RGD-integrin adhesion that promotes porcine conceptus elongation.
Keywords: alginate hydrogel, conceptus elongation, culture media, in vitro, metabolome, phospholipid, porcine, RGD, sphingolipid.
References
Arnhold, J, Osipov, AN, Spalteholz, H, Panasenko, OM, and Schiller, J (2002). Formation of lysophospholipids from unsaturated phosphatidylcholines under the influence of hypochlorous acid. Biochimica et Biophysica Acta (BBA) - General Subjects 1572, 91–100.| Formation of lysophospholipids from unsaturated phosphatidylcholines under the influence of hypochlorous acid.Crossref | GoogleScholarGoogle Scholar |
Asano, S, Pal, R, Tanaka, H-N, Imamura, A, Ishida, H, Suzuki, KGN, and Ando, H (2019). Development of fluorescently labeled SSEA-3, SSEA-4, and Globo-H glycosphingolipids for elucidating molecular interactions in the cell membrane. International Journal of Molecular Sciences 20, 6187–6187.
| Development of fluorescently labeled SSEA-3, SSEA-4, and Globo-H glycosphingolipids for elucidating molecular interactions in the cell membrane.Crossref | GoogleScholarGoogle Scholar |
Ashworth, CJ, Pickard, AR, Miller, SJ, Flint, APF, and Diehl, JR (1997). Comparative studies of conceptus-endometrial interactions in Large White × Landrace and Meishan gilts. Reproduction, Fertility and Development 9, 217–226.
| Comparative studies of conceptus-endometrial interactions in Large White × Landrace and Meishan gilts.Crossref | GoogleScholarGoogle Scholar |
Ashworth, MD, Ross, JW, Hu, J, White, FJ, Stein, DR, DeSilva, U, Johnson, GA, Spencer, TE, and Geisert, RD (2006). Expression of porcine endometrial prostaglandin synthase during the estrous cycle and early pregnancy, and following endocrine disruption of pregnancy. Biology of Reproduction 74, 1007–1015.
| Expression of porcine endometrial prostaglandin synthase during the estrous cycle and early pregnancy, and following endocrine disruption of pregnancy.Crossref | GoogleScholarGoogle Scholar |
Barnett, J, Chow, J, Ives, D, Chiou, M, Mackenzie, R, Osen, E, Nguyen, B, Tsing, S, Bach, C, Freire, J, Chan, H, Sigal, E, and Ramesha, C (1994). Purification, characterization and selective inhibition of human prostaglandin G/H synthase 1 and 2 expressed in the baculovirus system. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology 1209, 130–139.
| Purification, characterization and selective inhibition of human prostaglandin G/H synthase 1 and 2 expressed in the baculovirus system.Crossref | GoogleScholarGoogle Scholar |
Bazer, FW, and Johnson, GA (2014). Pig blastocyst–uterine interactions. Differentiation 87, 52–65.
| Pig blastocyst–uterine interactions.Crossref | GoogleScholarGoogle Scholar |
Bazer FW, Geisert RD, Thatcher WW, Roberts RM (1982) The establishment and maintenance of pregnancy. In ‘Control of pig reproduction’. (Eds DJA Cole, GR Foxcroft) pp. 227–252. (Butterworth-Heinemann)
Bazer, FW, Thatcher, WW, Martinat-Botte, F, and Terqui, M (1988). Conceptus development in Large White and prolific Chinese Meishan pigs. Reproduction 84, 37–42.
| Conceptus development in Large White and prolific Chinese Meishan pigs.Crossref | GoogleScholarGoogle Scholar |
Blomberg, LA, Long, EL, Sonstegard, TS, Van Tassell, CP, Dobrinsky, JR, and Zuelke, KA (2005). Serial analysis of gene expression during elongation of the peri-implantation porcine trophectoderm (conceptus). Physiological Genomics 20, 188–194.
| Serial analysis of gene expression during elongation of the peri-implantation porcine trophectoderm (conceptus).Crossref | GoogleScholarGoogle Scholar |
Blomberg, LA, Garrett, WM, Guillomot, M, Miles, JR, Sonstegard, TS, Van Tassell, CP, and Zuelke, KA (2006). Transcriptome profiling of the tubular porcine conceptus identifies the differential regulation of growth and developmentally associated genes. Molecular Reproduction and Development 73, 1491–1502.
| Transcriptome profiling of the tubular porcine conceptus identifies the differential regulation of growth and developmentally associated genes.Crossref | GoogleScholarGoogle Scholar |
Brandão, DO, Maddox-Hyttel, P, Løvendahl, P, Rumpf, R, Stringfellow, D, and Callesen, H (2004). Post hatching development: a novel system for extended in vitro culture of bovine embryos. Biology of Reproduction 71, 2048–2055.
| Post hatching development: a novel system for extended in vitro culture of bovine embryos.Crossref | GoogleScholarGoogle Scholar |
Broeckling, CD, Afsar, FA, Neumann, S, Ben-Hur, A, and Prenni, JE (2014). RAMClust: a novel feature clustering method enables spectral-matching-based annotation for metabolomics data. Analytical Chemistry 86, 6812–6817.
| RAMClust: a novel feature clustering method enables spectral-matching-based annotation for metabolomics data.Crossref | GoogleScholarGoogle Scholar |
Broeckling, CD, Ganna, A, Layer, M, Brown, K, Sutton, B, Ingelsson, E, Peers, G, and Prenni, JE (2016). Enabling efficient and confident annotation of LC–MS metabolomics data through MS1 spectrum and time prediction. Analytical Chemistry 88, 9226–9234.
| Enabling efficient and confident annotation of LC–MS metabolomics data through MS1 spectrum and time prediction.Crossref | GoogleScholarGoogle Scholar |
Cao, J, Shan, D, Revett, T, Li, D, Wu, L, Liu, W, Tobin, JF, and Gimeno, RE (2008). Molecular identification of a novel mammalian brain isoform of acyl-CoA:lysophospholipid acyltransferase with prominent ethanolamine lysophospholipid acylating activity, LPEAT2. Journal of Biological Chemistry 283, 19049–19057.
| Molecular identification of a novel mammalian brain isoform of acyl-CoA:lysophospholipid acyltransferase with prominent ethanolamine lysophospholipid acylating activity, LPEAT2.Crossref | GoogleScholarGoogle Scholar |
Cebrián-Prats, A, González-Lafont, À, and Lluch, JM (2019). Unraveling the molecular details of the complete mechanism that governs the synthesis of prostaglandin G2 catalyzed by cyclooxygenase-2. ACS Omega 4, 2063–2074.
| Unraveling the molecular details of the complete mechanism that governs the synthesis of prostaglandin G2 catalyzed by cyclooxygenase-2.Crossref | GoogleScholarGoogle Scholar |
Chen, X, Zheng, X, Ali, S, Guo, M, Zhong, R, Chen, Z, Zhang, Y, Qing, H, and Deng, Y (2018). Isolation and sequencing of salsolinol synthase, an enzyme catalyzing salsolinol biosynthesis. ACS Chemical Neuroscience 9, 1388–1398.
| Isolation and sequencing of salsolinol synthase, an enzyme catalyzing salsolinol biosynthesis.Crossref | GoogleScholarGoogle Scholar |
Djoumbou Feunang, Y, Eisner, R, Knox, C, Chepelev, L, Hastings, J, Owen, G, Fahy, E, Steinbeck, C, Subramanian, S, Bolton, E, Greiner, R, and Wishart, DS (2016). ClassyFire: automated chemical classification with a comprehensive, computable taxonomy. Journal of Cheminformatics 8, 61.
| ClassyFire: automated chemical classification with a comprehensive, computable taxonomy.Crossref | GoogleScholarGoogle Scholar |
Erdreich-Epstein, A, Shimada, H, Groshen, S, Liu, M, Metelitsa, LS, Kim, KS, Stins, MF, Seeger, RC, and Durden, DL (2000). Integrins αvβ3 and αvβ5 are expressed by endothelium of high-risk neuroblastoma and their inhibition is associated with increased endogenous ceramide. Cancer Research 60, 712–721.
Erikson, DW, Burghardt, RC, Bayless, KJ, and Johnson, GA (2009). Secreted phosphoprotein 1 (SPP1, osteopontin) binds to integrin alphavbeta6 on porcine trophectoderm cells and integrin alphavbeta3 on uterine luminal epithelial cells, and promotes trophectoderm cell adhesion and migration. Biology of Reproduction 81, 814–825.
| Secreted phosphoprotein 1 (SPP1, osteopontin) binds to integrin alphavbeta6 on porcine trophectoderm cells and integrin alphavbeta3 on uterine luminal epithelial cells, and promotes trophectoderm cell adhesion and migration.Crossref | GoogleScholarGoogle Scholar |
Farooqui AA, Horrocks LA, Farooqui T (2009) Choline and ethanolamine glycerophospholipids. In ‘Handbook of neurochemistry and molecular neurobiology’. (Eds A Lajtha, G Tettamanti, G Goracci) pp. 21–38. (Springer: Boston, MA)
FASS (2010) ‘Guide for care and use of agricultural animals in research and teaching.’ 3rd edn. (FASS: Champaign, IL)
Frasor, J, Weaver, AE, Pradhan, M, and Mehta, K (2008). Synergistic up-regulation of prostaglandin E synthase expression in breast cancer cells by 17β-estradiol and proinflammatory cytokines. Endocrinology 149, 6272–6279.
| Synergistic up-regulation of prostaglandin E synthase expression in breast cancer cells by 17β-estradiol and proinflammatory cytokines.Crossref | GoogleScholarGoogle Scholar |
Garlow, JE, Ka, H, Johnson, GA, Burghardt, RC, Jaeger, LA, and Bazer, FW (2002). Analysis of osteopontin at the maternal-placental interface in pigs. Biology of Reproduction 66, 718–725.
| Analysis of osteopontin at the maternal-placental interface in pigs.Crossref | GoogleScholarGoogle Scholar |
Geisert, RD, and Schmitt, RAM (2002). Early embryonic survival in the pig: can it be improved? Journal of Animal Science 80, E54–E65.
Geisert, RD, Renegar, RH, Thatcher, WW, Roberts, RM, and Bazer, FW (1982). Establishment of pregnancy in the pig: I. Interrelationships between preimplantation development of the pig blastocyst and uterine endometrial secretions. Biology of Reproduction 27, 925–939.
| Establishment of pregnancy in the pig: I. Interrelationships between preimplantation development of the pig blastocyst and uterine endometrial secretions.Crossref | GoogleScholarGoogle Scholar |
Geisert, RD, Lucy, MC, Whyte, JJ, Ross, JW, and Mathew, DJ (2014). Cytokines from the pig conceptus: roles in conceptus development in pigs. Journal of Animal Science and Biotechnology 5, 51.
| Cytokines from the pig conceptus: roles in conceptus development in pigs.Crossref | GoogleScholarGoogle Scholar |
Geisert RD, Johnson GA, Burghardt RC (2015) Implantation and establishment of pregnancy in the pig. In ‘Regulation of implantation and establishment of pregnancy in mammals: tribute to 45 year anniversary of Roger V. Short’s “maternal recognition of pregnancy”. Vol. 216’. (Eds RD Geisert, FW Bazer) pp. 137–163. (Springer: Cham, Switzerland)
Geisert, RD, Whyte, JJ, Meyer, AE, Mathew, DJ, Juárez, MR, Lucy, MC, Prather, RS, and Spencer, TE (2017). Rapid conceptus elongation in the pig: an interleukin 1 beta 2 and estrogen-regulated phenomenon. Molecular Reproduction and Development 84, 760–774.
| Rapid conceptus elongation in the pig: an interleukin 1 beta 2 and estrogen-regulated phenomenon.Crossref | GoogleScholarGoogle Scholar |
Golczak, M, Kiser, PD, Sears, AE, Lodowski, DT, Blaner, WS, and Palczewski, K (2012). Structural basis for the acyltransferase activity of lecithin:retinol acyltransferase-like proteins. Journal of Biological Chemistry 287, 23790–23807.
| Structural basis for the acyltransferase activity of lecithin:retinol acyltransferase-like proteins.Crossref | GoogleScholarGoogle Scholar |
Hanna, VS, and Hafez, EAA (2018). Synopsis of arachidonic acid metabolism: a review. Journal of Advanced Research 11, 23–32.
| Synopsis of arachidonic acid metabolism: a review.Crossref | GoogleScholarGoogle Scholar |
Hou, D-R, Jin, Y, Nie, X-W, Zhang, M-L, Ta, N, Zhao, L-H, Yang, N, Chen, Y, Wu, Z-Q, Jiang, H-B, Li, Y-R, Sun, Q-Y, Dai, Y-F, and Li, R-F (2016). Derivation of porcine embryonic stem-like cells from in vitro-produced blastocyst-stage embryos. Scientific Reports 6, 25838.
| Derivation of porcine embryonic stem-like cells from in vitro-produced blastocyst-stage embryos.Crossref | GoogleScholarGoogle Scholar |
Humpherson, PG, Leese, HJ, and Sturmey, RG (2005). Amino acid metabolism of the porcine blastocyst. Theriogenology 64, 1852–1866.
| Amino acid metabolism of the porcine blastocyst.Crossref | GoogleScholarGoogle Scholar |
Jacob, F, Hitchins, MP, Fedier, A, Brennan, K, Nixdorf, S, Hacker, NF, Ward, R, and Heinzelmann-Schwarz, VA (2014). Expression of GBGT1 is epigenetically regulated by DNA methylation in ovarian cancer cells. BMC Molecular Biology 15, 24.
| Expression of GBGT1 is epigenetically regulated by DNA methylation in ovarian cancer cells.Crossref | GoogleScholarGoogle Scholar |
Jaeger, C, Méret, M, Schmitt, CA, and Lisec, J (2017). Compound annotation in liquid chromatography/high-resolution mass spectrometry based metabolomics: robust adduct ion determination as a prerequisite to structure prediction in electrospray ionization mass spectra. Rapid Communications in Mass Spectrometry 31, 1261–1266.
| Compound annotation in liquid chromatography/high-resolution mass spectrometry based metabolomics: robust adduct ion determination as a prerequisite to structure prediction in electrospray ionization mass spectra.Crossref | GoogleScholarGoogle Scholar |
Kiewisz, J, Krawczynski, K, Lisowski, P, Blitek, A, Zwierzchowski, L, Ziecik, AJ, and Kaczmarek, MM (2014). Global gene expression profiling of porcine endometria on Days 12 and 16 of the estrous cycle and pregnancy. Theriogenology 82, 897–909.
| Global gene expression profiling of porcine endometria on Days 12 and 16 of the estrous cycle and pregnancy.Crossref | GoogleScholarGoogle Scholar |
Kim, S, Thiessen, PA, Cheng, T, Zhang, J, Gindulyte, A, and Bolton, EE (2019). PUG-View: programmatic access to chemical annotations integrated in PubChem. Journal of Cheminformatics 11, 56.
| PUG-View: programmatic access to chemical annotations integrated in PubChem.Crossref | GoogleScholarGoogle Scholar |
Kok, K, Zwiers, KC, Boot, RG, Overkleeft, HS, Aerts, JMFG, and Artola, M (2021). Fabry disease: molecular basis, pathophysiology, diagnostics and potential therapeutic directions. Biomolecules 11, 271–271.
| Fabry disease: molecular basis, pathophysiology, diagnostics and potential therapeutic directions.Crossref | GoogleScholarGoogle Scholar |
Kuo, H-H, Lin, R-J, Hung, J-T, Hsieh, C-B, Hung, T-H, Lo, F-Y, Ho, M-Y, Yeh, C-T, Huang, Y-L, Yu, J, and Yu, AL (2017). High expression FUT1 and B3GALT5 is an independent predictor of postoperative recurrence and survival in hepatocellular carcinoma. Scientific Reports 7, 10750.
| High expression FUT1 and B3GALT5 is an independent predictor of postoperative recurrence and survival in hepatocellular carcinoma.Crossref | GoogleScholarGoogle Scholar |
Kurnik-Łucka, M, Panula, P, Bugajski, A, and Gil, K (2018). Salsolinol: an unintelligible and double-faced molecule – lessons learned from in vivo and in vitro experiments. Neurotoxicity Research 33, 485–514.
| Salsolinol: an unintelligible and double-faced molecule – lessons learned from in vivo and in vitro experiments.Crossref | GoogleScholarGoogle Scholar |
Laughlin, TD, Miles, JR, Wright-Johnson, EC, Rempel, LA, Lents, CA, and Pannier, AK (2017). Development of pre-implantation porcine blastocysts cultured within alginate hydrogel systems either supplemented with secreted phosphoprotein 1 or conjugated with Arg-Gly-Asp Peptide. Reproduction, Fertility and Development 29, 2345–2356.
| Development of pre-implantation porcine blastocysts cultured within alginate hydrogel systems either supplemented with secreted phosphoprotein 1 or conjugated with Arg-Gly-Asp Peptide.Crossref | GoogleScholarGoogle Scholar |
Liebisch, G, Vizcaíno, JA, Köfeler, H, Trötzmüller, M, Griffiths, WJ, Schmitz, G, Spener, F, and Wakelam, MJO (2013). Shorthand notation for lipid structures derived from mass spectrometry. Journal of Lipid Research 54, 1523–1530.
| Shorthand notation for lipid structures derived from mass spectrometry.Crossref | GoogleScholarGoogle Scholar |
Loupatty, FJ, Clayton, PT, Ruiter, JPN, Ofman, R, Ijlst, L, Brown, GK, Thorburn, DR, Harris, RA, Duran, M, DeSousa, C, Krywawych, S, Heales, SJR, and Wanders, RJA (2007). Mutations in the gene encoding 3-hydroxyisobutyryl-CoA hydrolase results in progressive infantile neurodegeneration. The American Journal of Human Genetics 80, 195–199.
| Mutations in the gene encoding 3-hydroxyisobutyryl-CoA hydrolase results in progressive infantile neurodegeneration.Crossref | GoogleScholarGoogle Scholar |
Markosyan, N, Dozier, BL, Lattanzio, FA, and Duffy, DM (2006). Primate granulosa cell response via prostaglandin E2 receptors increases late in the periovulatory interval. Biology of Reproduction 75, 868–876.
| Primate granulosa cell response via prostaglandin E2 receptors increases late in the periovulatory interval.Crossref | GoogleScholarGoogle Scholar |
Matsunobu, T, Okuno, T, Yokoyama, C, and Yokomizo, T (2013). Thromboxane A synthase-independent production of 12-hydroxyheptadecatrienoic acid, a BLT2 ligand. Journal of Lipid Research 54, 2979–2987.
| Thromboxane A synthase-independent production of 12-hydroxyheptadecatrienoic acid, a BLT2 ligand.Crossref | GoogleScholarGoogle Scholar |
Meiser, J, Weindl, D, and Hiller, K (2013). Complexity of dopamine metabolism. Cell Communication and Signaling 11, 34.
| Complexity of dopamine metabolism.Crossref | GoogleScholarGoogle Scholar |
Miles, JR, Freking, BA, Blomberg, LA, Vallet, JL, and Zuelke, KA (2008). Conceptus development during blastocyst elongation in lines of pigs selected for increased uterine capacity or ovulation rate. Journal of Animal Science 86, 2126–2134.
| Conceptus development during blastocyst elongation in lines of pigs selected for increased uterine capacity or ovulation rate.Crossref | GoogleScholarGoogle Scholar |
Miles, JR, Laughlin, TD, Sargus-Patino, CN, and Pannier, AK (2017). In vitro porcine blastocyst development in three-dimensional alginate hydrogels. Molecular Reproduction and Development 84, 775–787.
| In vitro porcine blastocyst development in three-dimensional alginate hydrogels.Crossref | GoogleScholarGoogle Scholar |
Miles, JR, Walsh, SC, Rempel, LA, and Pannier, AK (2022). Mechanisms regulating the initiation of porcine conceptus elongation. Molecular Reproduction and Development , .
| Mechanisms regulating the initiation of porcine conceptus elongation.Crossref | GoogleScholarGoogle Scholar |
O’Neil, EV, and Spencer, TE (2021). Insights into the lipidome and primary metabolome of the uterus from day 14 cyclic and pregnant sheep. Biology of Reproduction 105, 87–99.
| Insights into the lipidome and primary metabolome of the uterus from day 14 cyclic and pregnant sheep.Crossref | GoogleScholarGoogle Scholar |
Pellegrino, RM, Di Veroli, A, Valeri, A, Goracci, L, and Cruciani, G (2014). LC/MS lipid profiling from human serum: a new method for global lipid extraction. Analytical and Bioanalytical Chemistry 406, 7937–7948.
| LC/MS lipid profiling from human serum: a new method for global lipid extraction.Crossref | GoogleScholarGoogle Scholar |
Pfeiffer, CA, Meyer, AE, Brooks, KE, Chen, PR, Milano-Foster, J, Spate, LD, Benne, JA, Cecil, RF, Samuel, MS, Ciernia, LA, Spinka, CM, Smith, MF, Wells, KD, Spencer, TE, Prather, RS, and Geisert, RD (2020). Ablation of conceptus PTGS2 expression does not alter early conceptus development and establishment of pregnancy in the pig. Biology of Reproduction 102, 475–488.
| Ablation of conceptus PTGS2 expression does not alter early conceptus development and establishment of pregnancy in the pig.Crossref | GoogleScholarGoogle Scholar |
PigCHAMP (2020) USA 2020 – year end summary. Available at https://www.pigchamp.com/news/benchmark-magazine/articles/usa-2020-year-summary. (Vol. 2021)
Pope WF (1994) Embryonic mortality in swine. In ‘Embryonic mortality in domestic animals’. (Eds MT Zavy, RD Geisert) pp. 53–77. (CRC Press: Boca Raton, FL)
Pope, WF, and First, NL (1985). Factors affecting the survival of pig embryos. Theriogenology 23, 91–105.
| Factors affecting the survival of pig embryos.Crossref | GoogleScholarGoogle Scholar |
Ribeiro, ES, Greco, LF, Bisinotto, RS, Lima, FS, Thatcher, WW, and Santos, JE (2016). Biology of preimplantation conceptus at the onset of elongation in dairy cows. Biology of Reproduction 94, 1–18.
| Biology of preimplantation conceptus at the onset of elongation in dairy cows.Crossref | GoogleScholarGoogle Scholar |
Ross, JW, Ashworth, MD, Stein, DR, Couture, OP, Tuggle, CK, and Geisert, RD (2009). Identification of differential gene expression during porcine conceptus rapid trophoblastic elongation and attachment to uterine luminal epithelium. Physiological Genomics 36, 140–148.
| Identification of differential gene expression during porcine conceptus rapid trophoblastic elongation and attachment to uterine luminal epithelium.Crossref | GoogleScholarGoogle Scholar |
Rowley, JA, Madlambayan, G, and Mooney, DJ (1999). Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials 20, 45–53.
| Alginate hydrogels as synthetic extracellular matrix materials.Crossref | GoogleScholarGoogle Scholar |
Ryckman, AE, Brockhausen, I, and Walia, JS (2020). Metabolism of glycosphingolipids and their role in the pathophysiology of lysosomal storage disorders. International Journal of Molecular Sciences 21, 6881–6881.
| Metabolism of glycosphingolipids and their role in the pathophysiology of lysosomal storage disorders.Crossref | GoogleScholarGoogle Scholar |
Sargus-Patino, CN, Wright, EC, Plautz, SA, Miles, JR, Vallet, JL, and Pannier, AK (2014). In vitro development of preimplantation porcine embryos using alginate hydrogels as a three-dimensional extracellular matrix. Reproduction, Fertility and Development 26, 943–953.
| In vitro development of preimplantation porcine embryos using alginate hydrogels as a three-dimensional extracellular matrix.Crossref | GoogleScholarGoogle Scholar |
Shulga, YV, Topham, MK, and Epand, RM (2011). Regulation and functions of diacylglycerol kinases. Chemical Reviews 111, 6186–6208.
| Regulation and functions of diacylglycerol kinases.Crossref | GoogleScholarGoogle Scholar |
Smith, CA, Want, EJ, O’Maille, G, Abagyan, R, and Siuzdak, G (2006). XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Analytical Chemistry 78, 779–787.
| XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification.Crossref | GoogleScholarGoogle Scholar |
Suila, H, Pitkänen, V, Hirvonen, T, Heiskanen, A, Anderson, H, Laitinen, A, Natunen, S, Miller-Podraza, H, Satomaa, T, Natunen, J, Laitinen, S, and Valmu, L (2011). Are globoseries glycosphingolipids SSEA-3 and -4 markers for stem cells derived from human umbilical cord blood? Journal of Molecular Cell Biology 3, 99–107.
| Are globoseries glycosphingolipids SSEA-3 and -4 markers for stem cells derived from human umbilical cord blood?Crossref | GoogleScholarGoogle Scholar |
Sumner, LW, Amberg, A, Barrett, D, Beale, MH, Beger, R, Daykin, CA, Fan, TW-M, Fiehn, O, Goodacre, R, Griffin, JL, Hankemeier, T, Hardy, N, Harnly, J, Higashi, R, Kopka, J, Lane, AN, Lindon, JC, Marriott, P, Nicholls, AW, Reily, MD, Thaden, JJ, and Viant, MR (2007). Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI). Metabolomics 3, 211–221.
| Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI).Crossref | GoogleScholarGoogle Scholar |
Tafesse, FG, Huitema, K, Hermansson, M, van der Poel, S, van den Dikkenberg, J, Uphoff, A, Somerharju, P, and Holthuis, JCM (2007). Both sphingomyelin synthases SMS1 and SMS2 are required for sphingomyelin homeostasis and growth in human HeLa cells. Journal of Biological Chemistry 282, 17537–17547.
| Both sphingomyelin synthases SMS1 and SMS2 are required for sphingomyelin homeostasis and growth in human HeLa cells.Crossref | GoogleScholarGoogle Scholar |
Takahashi, T, and Suzuki, T (2012). Role of sulfatide in normal and pathological cells and tissues. Journal of Lipid Research 53, 1437–1450.
| Role of sulfatide in normal and pathological cells and tissues.Crossref | GoogleScholarGoogle Scholar |
Tanioka, T, Nakatani, Y, Semmyo, N, Murakami, M, and Kudo, I (2000). Molecular identification of cytosolic prostaglandin E2 synthase that is functionally coupled with cyclooxygenase-1 in immediate prostaglandin E2 biosynthesis. Journal of Biological Chemistry 275, 32775–32782.
| Molecular identification of cytosolic prostaglandin E2 synthase that is functionally coupled with cyclooxygenase-1 in immediate prostaglandin E2 biosynthesis.Crossref | GoogleScholarGoogle Scholar |
Tautenhahn, R, Böttcher, C, and Neumann, S (2008). Highly sensitive feature detection for high resolution LC/MS. BMC Bioinformatics 9, 504.
| Highly sensitive feature detection for high resolution LC/MS.Crossref | GoogleScholarGoogle Scholar |
Tsugawa, H, Kind, T, Nakabayashi, R, Yukihira, D, Tanaka, W, Cajka, T, Saito, K, Fiehn, O, and Arita, M (2016). Hydrogen rearrangement rules: computational MS/MS fragmentation and structure elucidation using MS-FINDER software. Analytical Chemistry 88, 7946–7958.
| Hydrogen rearrangement rules: computational MS/MS fragmentation and structure elucidation using MS-FINDER software.Crossref | GoogleScholarGoogle Scholar |
van der Veen, JN, Kennelly, JP, Wan, S, Vance, JE, Vance, DE, and Jacobs, RL (2017). The critical role of phosphatidylcholine and phosphatidylethanolamine metabolism in health and disease. Biochimica et Biophysica Acta (BBA) - Biomembranes 1859, 1558–1572.
| The critical role of phosphatidylcholine and phosphatidylethanolamine metabolism in health and disease.Crossref | GoogleScholarGoogle Scholar |
Vinsky, MD, Novak, S, Dixon, WT, Dyck, MK, and Foxcroft, GR (2006). Nutritional restriction in lactating primiparous sows selectively affects female embryo survival and overall litter development. Reproduction, Fertility and Development 18, 347–355.
| Nutritional restriction in lactating primiparous sows selectively affects female embryo survival and overall litter development.Crossref | GoogleScholarGoogle Scholar |
Waclawik, A, Kaczmarek, MM, Blitek, A, Kaczynski, P, and Ziecik, AJ (2017). Embryo-maternal dialogue during pregnancy establishment and implantation in the pig. Molecular Reproduction and Development 84, 842–855.
| Embryo-maternal dialogue during pregnancy establishment and implantation in the pig.Crossref | GoogleScholarGoogle Scholar |
Walsh, SC, Miles, JR, Yao, L, Broeckling, CD, Rempel, LA, Wright-Johnson, EC, and Pannier, AK (2020). Metabolic compounds within the porcine uterine environment are unique to the type of conceptus present during the early stages of blastocyst elongation. Molecular Reproduction and Development 87, 174–190.
| Metabolic compounds within the porcine uterine environment are unique to the type of conceptus present during the early stages of blastocyst elongation.Crossref | GoogleScholarGoogle Scholar |
Walsh, SC, Miles, JR, Keel, BN, Rempel, LA, Wright-Johnson, EC, Lindholm-Perry, AK, Oliver, WT, and Pannier, AK (2022). Global analysis of differential gene expression within the porcine conceptus transcriptome as it transitions through spherical, ovoid, and tubular morphologies during the initiation of elongation. Molecular Reproduction and Development 89, 175–201.
| Global analysis of differential gene expression within the porcine conceptus transcriptome as it transitions through spherical, ovoid, and tubular morphologies during the initiation of elongation.Crossref | GoogleScholarGoogle Scholar |
Watanabe, K, Ohkubo, H, Niwa, H, Tanikawa, N, Koda, N, Ito, S, and Ohmiya, Y (2003). Essential 110Cys in active site of membrane-associated prostaglandin E synthase-2. Biochemical and Biophysical Research Communications 306, 577–581.
| Essential 110Cys in active site of membrane-associated prostaglandin E synthase-2.Crossref | GoogleScholarGoogle Scholar |
Watkins, G, Douglas-Jones, A, Mansel, RE, and Jiang, WG (2005). Expression of thromboxane synthase, TBXAS1 and the thromboxane A2 receptor, TBXA2R, in human breast cancer. International Seminars in Surgical Oncology 2, 23.
| Expression of thromboxane synthase, TBXAS1 and the thromboxane A2 receptor, TBXA2R, in human breast cancer.Crossref | GoogleScholarGoogle Scholar |
Whyte, A, and Robson, T (1984). Saccharides localized by fluorescent lectins on trophectoderm and endometrium prior to implantation in pigs, sheep and equids. Placenta 5, 533–540.
| Saccharides localized by fluorescent lectins on trophectoderm and endometrium prior to implantation in pigs, sheep and equids.Crossref | GoogleScholarGoogle Scholar |
Yelich, JV, Pomp, D, and Geisert, RD (1997). Ontogeny of elongation and gene expression in the early developing porcine conceptus. Biology of Reproduction 57, 1256–1265.
| Ontogeny of elongation and gene expression in the early developing porcine conceptus.Crossref | GoogleScholarGoogle Scholar |
Zhao, Y, Chen, Y-Q, Bonacci, TM, Bredt, DS, Li, S, Bensch, WR, Moller, DE, Kowala, M, Konrad, RJ, and Cao, G (2008). Identification and characterization of a major liver lysophosphatidylcholine acyltransferase. Journal of Biological Chemistry 283, 8258–8265.
| Identification and characterization of a major liver lysophosphatidylcholine acyltransferase.Crossref | GoogleScholarGoogle Scholar |
