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[1]Malizia, B. A., Dodge, L. E., Penzias, A. S., and M.R. Hacker: The cumulative probability of liveborn multiples after in vitro fertilization: a cohort study of more than 10,000 women. Fertil Steril 99:393-399 (2013)
[2]Zollner, U., and J. Dietl: Perinatal risks after IVF and ICSI. J Perinat Med 41:17-22 (2013)
[3]ESHRE: Task Force on Ethics and Law Ethical issues related to multiple pregnancies in medically assisted procreation. Hum Reprod 18:1976-1979 (2003)
[4]Lukassen, H., Braat, D., Wetzels, A., Zielhuis, G., Adang, E., Scheenjes, E., and J. A. Kremer: Two cycles with single embryo transfer versus one cycle with double embryo transfer: a randomised controlled trial. Hum Reprod 20:702-708 (2005)
[5]Alpha Scientists in Reproductive medicine and ESHRE Special Interest Group of Embryology: The Istanbul consensus workshop on embryo assessment: proceedings of an expert meeting. Hum Reprod 26:1270-1283 (2011)
[6]Ebner, T., Moser, M., Sommergruber, M., and G. Tews: Selection based on morphological assessment of oocytes and embryos at different stages of preimplantation development: a review. Hum Reprod Update 9:251-262. (2003)
[7]Ziebe, S., Petersen, K., Lindenberg, S., Andersen, A. G., Gabrielsen, A., and A. N. Andersen:. Embryo morphology or cleavage stage: how to select the best embryos for transfer after in-vitro fertilization. Hum Reprod 12:1545-1549 (1997)
[8]Desai, N. N., Goldstein, J., Rowland, D. Y., and J. M. Goldfarb: Morphological evaluation of human embryos and derivation of an embryo quality scoring system specific for day 3 embryos: a preliminary study. Hum Reprod 15:2190-2196 (2000)
[9]Meseguer, M., Herrero, J., Tejera, A., Hilligsøe, K. M., Ramsing, N. B., and J. RemohÍ: The use of morphokinetics as a predictor of embryo implantation. Hum Reprod 26:2658-2671 (2011)
[10]Basile, N., Nogales, M. D., Bronet, F., Florensa, M., Riqueiros, M., Rodrigo, L., GarcÍa-Velasco, J., and M. Meseguer: Increasing the probability of selecting chromosomally normal embryos by time-lapse morphokinetics analysis. Fertil Steril 101:699-704 (2014)
[11]Wong, C. C., Loewke, K. E., Bossert, N. L., Behr, B., De Jonge, C. J., Baer, T. M., and R. A. Reijo Pera:. Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nature Biotech 28:1115-1121 (2010)
[12]Meseguer, M., Rubio, I., Cruz, M., Basile, N., Marcos, J., and A. Requena: Embryo incubation and selection in a time-lapse monitoring system improves pregnancy outcome compared with a standard incubator: a retrospective cohort study. Fertil Steril 98:1481-1489 (2012)
[13]Kulasingam, V., and E. P. Diamandis: Proteomics analysis of conditioned media from three breast cancer cell lines: a mine for biomarkers and therapeutic targets. Mol Cell Proteomics 6:1997-2011 (2007)
[14]Yao, Y. Q., Barlow, D. H., and I. L. Sargent:. Differential expression of alternatively spliced transcripts of HLA-G in human preimplantation embryos and inner cell masses. J Immunol 175:8379-8385 (2005)
[15]DomÍnguez, F., Gadea, B., Esteban, F. J., Horcajadas, J. A., Pellicer, A., and C. Simón: Comparative protein-profile analysis of implanted versus non-implanted human blastocysts. Hum Reprod 23:1993-2000 (2008)
[16]Ubaldi, F., Anniballo, R., Romano, S., Baroni, E., Albricci, L., Colamaria, S., Capalbo, A., Sapienza, F., Vajta, G., and L. Rienzi: Cumulative ongoing pregnancy rate achieved with oocyte vitrification and cleavage stage transfer without embryo selection in a standard infertility program. Hum Reprod 5:1199-1205 (2010)
[17]Rienzi, L., Ubaldi, F., Anniballo, R., Cerulo, G., and E. Greco: Preincubation of human oocytes may improve fertilization and embryo quality after intracytoplasmic sperm injection. Hum Reprod 4:1014-1019 (1998)
[18]Rienzi, L., Romano, S., Albricci, L., Maggiulli, R., Capalbo, A., Baroni, E., Colamaria, S., Sapienza, F., and F. Ubaldi: Embryo development of fresh ‘versus’ vitrified metaphase II oocytes after ICSI: a prospective randomized sibling-oocyte study. Hum Reprod 25:66-73 (2010)
[19]Gardner, D. K., and WB Schoolcraft:. In-vitro culture of human blastocyst. In Jansen R., and Mortimer, D. (eds), Toward Reproductive Certainty: Fertilyty and Genetics Beyond. Parthenon Press, Carnforth, pp 378-388 (1999)
[20]Lawlor, K., Nazarian, A., Lacomis, L., Tempst, P., and J. Villanueva. Pathway-based biomarker search by high-throughput proteomics profiling of secretomes. J Proteome Res 8:1489-503 (2009)
[21]Berggård, T., Arrigoni, G., Olsson, O., Fex, M., Linse, S., and P. James: 140 mouse brain proteins identified by Ca2+-calmodulin affinity chromatography and tandem mass spectrometry. J Proteome Res 5:669-687 (2006)
[22]Solier, C., and H. Langen: Antibody-based proteomics and biomarker research - current status and limitations. Proteomics 14:774-83 (2014)
[23]R. Burns: Business research methods and statistics using SPSS. London: SAGE Publications Ltd. (2009)
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[28]Cortezzi, S. S., Garcia, J. S., Ferreira, C. R., Braga, D. P., Figueira, R. C., Iaconelli, A. Jr., Souza, G. H., Borges, E. Jr., and M. N. Eberlin: Secretome of the preimplantation human embryo by bottom-up label-free proteomics. Anal Bioanal Chem 401:1331-1339 (2011)
[29]Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M., and G. Sherlock: Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature Gen 25:25-29 (2000)
[30]Robinson, P. N., and S. Mundlos: The human phenotype ontology. Clin Gen 77:525-534 (2010)
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[33]Stark, C., Breitkreutz, B. J., Chatr-Aryamontri, A., Boucher, L., Oughtred, R., Livstone, M. S., Nixon, J., Van Auken, K., Wang, X., Shi, X., Reguly, T., Rust, J. M., Winter, A., Dolinski, K., and M. Tyers: The BioGRID Interaction Database: 2011 update. Nucl Ac Res 39:698-704 (2011)
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[36]Zentner, G. E., and S. Henikoff: Regulation of nucleosome dynamics by histone modifications. Nature Struct Mol Biol 20:259-166 (2013)
[37]Gabler, C., Kalden, J. R., and H. M. Lorenz: The putative role of apoptosis-modified histones for the induction of autoimmunity in Systemic Lupus Erythematosus. Biochem Pharmacol 66:1441-1446. (2003)
[38]Getsios S., Amargo, E. V., Dusek, R. L., Ishii, K., Sheu, L., Godsel, L. M., and K. J. Green: Coordinated expression of desmoglein 1 and desmocollin 1 regulates intercellular adhesion. Differentiation 72:419-433 (2004)
[39]Pak, S. C., Kumar, V., Tsu, C., Luke, C. J., Askew, Y. S., Mills, D. R., Brömme, D., and G. A. Silverman: SRP-2 is a cross-class inhibitor that participates in postembryonic development of the nematode Caenorhabditis elegans: initial characterization of the clade L serpins. J Biol Chem 279:15448-15459 (2004)
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Frontiers in Bioscience-Landmark (FBL) is published by IMR Press from Volume 26 Issue 5 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.
Early protein profile of human embryonic secretome
, Filippo Maria Ubaldi 2, Laura Rienzi 2, Cinzia Franchin 3,4, Micaela Pivato 4,5, Stefania Romano 2, Diego Guidolin 6, Raffaele De Caro 6, Alberto Ferlin 1, Luca De Toni 11 University of Padova, Department of Medicine & Andrology and Reproductive Medicine Unit, 35128, Padova, Italy
2 Genera Centre, 00197, Roma, Italy
3 University of Padova, Department of Biomedical Science, 35131, Padova, Italy
4 Proteomics Center of Padova University, 35128, Padova, Italy
5 DAFNAE, University of Padova, 35020, Legnaro (PD), Italy
6 University of Padova, Department of Molecular Medicine, 35121, Padova, Italy
Abstract
Embryos obtained by in vitro fertilization are currently assessed by morphology, but displays limitations with over 70% of embryos failing to implant. In this study, we performed HPLC-MS/MS analysis on the conditioned medium obtained from 50 human embryos at the 3rd day of in vitro culture. 70 proteins were identified in the medium of 48 embryos. Validation by protein array on two pools of 11 and 9 conditioned media, showed a protein pattern overlap with HPLC-MS/MS of respectively 72% and 78%. Unsupervised hierarchical cluster analysis on protein spectra, allowed to divide embryos into 3 clusters. The first cluster selectively lacked of proteins involved in programmed cell death. The third cluster was devoid of proteins involved in cell development. Embryos taking the shortest time to develop into 5 cell morulas, featuring lower implantation rate, significantly segregated in the third cluster (P=0.047). Multiple linear regression analysis, identified 12 predictive proteins for transfer success (P<0.0.5). Proteomics of embryo secretome aids in understanding embryo physiology and in improving assisted reproductive technology.
Keywords
- Embryo Transfer
- Proteomics
- Morphology
- Assisted Reproductive Technology
References
- [1] Malizia, B. A., Dodge, L. E., Penzias, A. S., and M.R. Hacker: The cumulative probability of liveborn multiples after in vitro fertilization: a cohort study of more than 10,000 women. Fertil Steril 99:393-399 (2013)
- [2] Zollner, U., and J. Dietl: Perinatal risks after IVF and ICSI. J Perinat Med 41:17-22 (2013)
- [3] ESHRE: Task Force on Ethics and Law Ethical issues related to multiple pregnancies in medically assisted procreation. Hum Reprod 18:1976-1979 (2003)
- [4] Lukassen, H., Braat, D., Wetzels, A., Zielhuis, G., Adang, E., Scheenjes, E., and J. A. Kremer: Two cycles with single embryo transfer versus one cycle with double embryo transfer: a randomised controlled trial. Hum Reprod 20:702-708 (2005)
- [5] Alpha Scientists in Reproductive medicine and ESHRE Special Interest Group of Embryology: The Istanbul consensus workshop on embryo assessment: proceedings of an expert meeting. Hum Reprod 26:1270-1283 (2011)
- [6] Ebner, T., Moser, M., Sommergruber, M., and G. Tews: Selection based on morphological assessment of oocytes and embryos at different stages of preimplantation development: a review. Hum Reprod Update 9:251-262. (2003)
- [7] Ziebe, S., Petersen, K., Lindenberg, S., Andersen, A. G., Gabrielsen, A., and A. N. Andersen:. Embryo morphology or cleavage stage: how to select the best embryos for transfer after in-vitro fertilization. Hum Reprod 12:1545-1549 (1997)
- [8] Desai, N. N., Goldstein, J., Rowland, D. Y., and J. M. Goldfarb: Morphological evaluation of human embryos and derivation of an embryo quality scoring system specific for day 3 embryos: a preliminary study. Hum Reprod 15:2190-2196 (2000)
- [9] Meseguer, M., Herrero, J., Tejera, A., Hilligsøe, K. M., Ramsing, N. B., and J. RemohÍ: The use of morphokinetics as a predictor of embryo implantation. Hum Reprod 26:2658-2671 (2011)
- [10] Basile, N., Nogales, M. D., Bronet, F., Florensa, M., Riqueiros, M., Rodrigo, L., GarcÍa-Velasco, J., and M. Meseguer: Increasing the probability of selecting chromosomally normal embryos by time-lapse morphokinetics analysis. Fertil Steril 101:699-704 (2014)
- [11] Wong, C. C., Loewke, K. E., Bossert, N. L., Behr, B., De Jonge, C. J., Baer, T. M., and R. A. Reijo Pera:. Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nature Biotech 28:1115-1121 (2010)
- [12] Meseguer, M., Rubio, I., Cruz, M., Basile, N., Marcos, J., and A. Requena: Embryo incubation and selection in a time-lapse monitoring system improves pregnancy outcome compared with a standard incubator: a retrospective cohort study. Fertil Steril 98:1481-1489 (2012)
- [13] Kulasingam, V., and E. P. Diamandis: Proteomics analysis of conditioned media from three breast cancer cell lines: a mine for biomarkers and therapeutic targets. Mol Cell Proteomics 6:1997-2011 (2007)
- [14] Yao, Y. Q., Barlow, D. H., and I. L. Sargent:. Differential expression of alternatively spliced transcripts of HLA-G in human preimplantation embryos and inner cell masses. J Immunol 175:8379-8385 (2005)
- [15] DomÍnguez, F., Gadea, B., Esteban, F. J., Horcajadas, J. A., Pellicer, A., and C. Simón: Comparative protein-profile analysis of implanted versus non-implanted human blastocysts. Hum Reprod 23:1993-2000 (2008)
- [16] Ubaldi, F., Anniballo, R., Romano, S., Baroni, E., Albricci, L., Colamaria, S., Capalbo, A., Sapienza, F., Vajta, G., and L. Rienzi: Cumulative ongoing pregnancy rate achieved with oocyte vitrification and cleavage stage transfer without embryo selection in a standard infertility program. Hum Reprod 5:1199-1205 (2010)
- [17] Rienzi, L., Ubaldi, F., Anniballo, R., Cerulo, G., and E. Greco: Preincubation of human oocytes may improve fertilization and embryo quality after intracytoplasmic sperm injection. Hum Reprod 4:1014-1019 (1998)
- [18] Rienzi, L., Romano, S., Albricci, L., Maggiulli, R., Capalbo, A., Baroni, E., Colamaria, S., Sapienza, F., and F. Ubaldi: Embryo development of fresh ‘versus’ vitrified metaphase II oocytes after ICSI: a prospective randomized sibling-oocyte study. Hum Reprod 25:66-73 (2010)
- [19] Gardner, D. K., and WB Schoolcraft:. In-vitro culture of human blastocyst. In Jansen R., and Mortimer, D. (eds), Toward Reproductive Certainty: Fertilyty and Genetics Beyond. Parthenon Press, Carnforth, pp 378-388 (1999)
- [20] Lawlor, K., Nazarian, A., Lacomis, L., Tempst, P., and J. Villanueva. Pathway-based biomarker search by high-throughput proteomics profiling of secretomes. J Proteome Res 8:1489-503 (2009)
- [21] Berggård, T., Arrigoni, G., Olsson, O., Fex, M., Linse, S., and P. James: 140 mouse brain proteins identified by Ca2+-calmodulin affinity chromatography and tandem mass spectrometry. J Proteome Res 5:669-687 (2006)
- [22] Solier, C., and H. Langen: Antibody-based proteomics and biomarker research - current status and limitations. Proteomics 14:774-83 (2014)
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- [27] Holewinski, R. J., Jin, Z., Powell, M. J., Maust, M. D., and J. E. Van Eyk: A fast and reproducible method for albumin isolation and depletion from serum and cerebrospinal fluid. Proteomics 13:743-750 (2013)
- [28] Cortezzi, S. S., Garcia, J. S., Ferreira, C. R., Braga, D. P., Figueira, R. C., Iaconelli, A. Jr., Souza, G. H., Borges, E. Jr., and M. N. Eberlin: Secretome of the preimplantation human embryo by bottom-up label-free proteomics. Anal Bioanal Chem 401:1331-1339 (2011)
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- [30] Robinson, P. N., and S. Mundlos: The human phenotype ontology. Clin Gen 77:525-534 (2010)
- [31] Kanehisa, M., Goto, S., Furumichi, M., Tanabe, M., and Hirakawa, M:. KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucl Ac Res 38:D355-D336 (2010)
- [32] Matthews, L., Gopinath, G., Gillespie, M., Caudy, M., Croft, D., de Bono, B., Garapati, P., Hemish, J., Hermjakob, H., Jassal, B., Kanapin, A., Lewis, S., Mahajan, S., May, B., Schmidt, E., Vastrik, I., Wu, G., Birney, E., Stein, L., and P. D’Eustachio: Reactome knowledgebase of human biological pathways and processes. Nucl Ac Res 37:D619-D622 (2009)
- [33] Stark, C., Breitkreutz, B. J., Chatr-Aryamontri, A., Boucher, L., Oughtred, R., Livstone, M. S., Nixon, J., Van Auken, K., Wang, X., Shi, X., Reguly, T., Rust, J. M., Winter, A., Dolinski, K., and M. Tyers: The BioGRID Interaction Database: 2011 update. Nucl Ac Res 39:698-704 (2011)
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- [37] Gabler, C., Kalden, J. R., and H. M. Lorenz: The putative role of apoptosis-modified histones for the induction of autoimmunity in Systemic Lupus Erythematosus. Biochem Pharmacol 66:1441-1446. (2003)
- [38] Getsios S., Amargo, E. V., Dusek, R. L., Ishii, K., Sheu, L., Godsel, L. M., and K. J. Green: Coordinated expression of desmoglein 1 and desmocollin 1 regulates intercellular adhesion. Differentiation 72:419-433 (2004)
- [39] Pak, S. C., Kumar, V., Tsu, C., Luke, C. J., Askew, Y. S., Mills, D. R., Brömme, D., and G. A. Silverman: SRP-2 is a cross-class inhibitor that participates in postembryonic development of the nematode Caenorhabditis elegans: initial characterization of the clade L serpins. J Biol Chem 279:15448-15459 (2004)
- [40] Lee Motoyama, J. P., Kim-Motoyama, H., Kim, P., Nakagama, H., Miyagawa, K., and K. Suzuki: Identification of dermcidin in human gestational tissue and characterization of its proteolytic activity. Biochem Biophysl Res Commun 357:828-833 (2007)
- [41] Buhimschi, C. S., Bhandari, V., Dulay, A. T., Nayeri, U. A., Abdel-Razeq, S. S., Pettker, C. M., Thung, S., Zhao, G., Han, Y. W., Bizzarro, M., and I. A. Buhimschi IA: Proteomics mapping of cord blood identifies haptoglobin “switch-on” pattern as biomarker of early-onset neonatal sepsis in preterm newborns. PLoS One 6:e26111 (2011)
- [42] Hamatani, T., Ko, M. Sh., Yamada, M., Kuji, N., Mizusawa, Y., Shoji, M., Hada, T., Asada, H., Maruyama, T., and Y. Yoshimura: Global gene expression profiling of preimplantation embryos. Hum Cell 19:98-117 (2006)
- [43] Nyalwidhe, J., Burch, T., Bocca, S., Cazares, L., Green-Mitchell, S., Cooke, M., Birdsall, P., Basu, G., Semmes, O. J., and S. Oehninger: The search for biomarkers of human embryo developmental potential in IVF: a comprehensive proteomic approach. Mol Hum Reprod 19:250-263 (2013)
- [44] Katz-Jaffe, M. G., Schoolcraft, W. B., and D. K. Gardner: Analysis of protein expression (secretome) by human and mouse preimplantation embryos. Fertil Steril 86:678–685 (2006)
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