Characterization of seminal plasma proteomic alterations associated with the IVF and rescue‐ICSI pregnancy in assisted reproduction

Liu, X.; Liu, G.; Zhu, P.; Wang, Y.; Wang, J.; Zhang, W.; Wang, W.; Li, N.; Wang, X.; Zhang, C.; Liu, J.; Shen, X.; Liu, F.

doi:10.1111/andr.12687

Title: Characterization of seminal plasma proteomic alterations associated with the IVF and rescue‐ICSI pregnancy in assisted reproduction

Journal Article · 30 July 2019 · Andrology

DOI: https://doi.org/10.1111/andr.12687 · OSTI ID:1545897

Liu, X. ^[1]; Liu, G. ^[2]; Zhu, P. ^[1]; Wang, Y. ^[1]; Wang, J. ^[1]; Zhang, W. ^[1]; Wang, W. ^[1]; Li, N. ^[1]; Wang, X. ^[3]; Zhang, C. ^[1]; Liu, J. ^[1]; Shen, X. ^[4];

^[1]

Central Laboratory The Affiliated Yantai Yuhuangding Hospital of Qingdao University Yantai Shandong China
Reproductive Center Tianjin Aiwei Hospital Tianjin China
Department of Clinical Laboratory The Affiliated Yantai Yuhuangding Hospital of Qingdao University Yantai Shandong China
Reproductive Center Beijing BaoDao Obstetrics and Gynecology Hospital Beijing China

Abstract Background Seminal plasma is a promising diagnostic fluid for male infertility. In assisted reproduction, the seminal plasma‐based characteristics of normozoospermic men achieving successful clinical pregnancy through rescue intracytoplasmic sperm injection after in vitro fertilization failure remain unclear. Objective To identify potential seminal plasma proteins to contribute to a new understanding of unexplained male factor infertility. Materials and Methods An approach with isobaric tags for relative and absolute quantification labeling coupled with liquid chromatography matrix‐assisted laser desorption ionization mass spectrometry was applied to investigate differentially expressed proteins in the seminal plasma of a rescue intracytoplasmic sperm injection pregnancy group versus an in vitro fertilization pregnancy group of normozoospermic men. Result(s) The present work revealed seventy‐three differentially expressed seminal plasma proteins between the in vitro fertilization and rescue intracytoplasmic sperm injection groups. Forty‐five proteins were upregulated, and 28 proteins were downregulated in the rescue intracytoplasmic sperm injection group compared with the in vitro fertilization group. Bioinformatics analyses showed that these altered proteins were involved in various functions, including the kallikrein‐related proteolytic cascade, immune response, and heparin binding. Furthermore, the validity of the proteomic results was verified by Western blot analysis of the proteins (lactoferrin [LTF], fibronectin [FN1], creatine kinase B type [CKB], kallikrein‐2 [KLK2], aminopeptidase N [ANPEP], extracellular matrix protein 1 [ECM1], glycodelin [PAEP], alpha‐1‐antitrypsin [SERPINA1], and semenogelin‐1 [SEMG1]) and immunofluorescence. Moreover, 16% of the seminal plasma proteins identified in the present work have not been reported in previous studies. Discussion This panel of altered seminal plasma proteins associated with unexplained male factor infertility might have clinical relevance and may be useful in the diagnosis and prognosis of idiopathic infertility in in vitro fertilization. Conclusions Our work not only provides a new complementary high‐confidence dataset of seminal plasma proteins but also shines new light onto the molecular characteristics of seminal plasma from normozoospermic men with different assisted reproductive outcomes.

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Sponsoring Organization:: USDOE

OSTI ID:: 1545897

Journal Information:: Andrology, Journal Name: Andrology Journal Issue: 2 Vol. 8; ISSN 2047-2919

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: Country unknown/Code not available

Language:: English

References (58)

Semenogelin, the Main Protein of Semen Coagulum, Inhibits Human Sperm Capacitation by Interfering With the Superoxide Anion Generated During This Process de LAMIRANDE, Eve; Yoshida, Kaoru; Yoshiike, Miki Journal of Andrology, Vol. 22, Issue 4 https://doi.org/10.1002/j.1939-4640.2001.tb02228.x	journal	July 2001
Sperm Motility in Men With Spinal Cord Injuries Is Enhanced by Inactivating Cytokines in the Seminal Plasma Cohen, Daniel R.; Basu, Sarmistha; Randall, Josh M. Journal of Andrology, Vol. 25, Issue 6 https://doi.org/10.1002/j.1939-4640.2004.tb03162.x	journal	November 2004
Characterization of the osteogenic stromal cell line MN7: Identification of secreted MN7 proteins using two-dimensional polyacrylamide gel electrophoresis, western blotting, and microsequencing Mathieu, E.; Meheus, L.; Raymackers, J. Journal of Bone and Mineral Research, Vol. 9, Issue 6 https://doi.org/10.1002/jbmr.5650090616	journal	June 1994
Affinity liquid chromatography and capillary electrophoresis of seminal plasma proteins Vařilová, Tereza; Seménková, Hana; Horák, Pavel Journal of Separation Science, Vol. 29, Issue 8 https://doi.org/10.1002/jssc.200500405	journal	May 2006
Heparin-binding proteins of human seminal plasma: purification and characterization Kumar, Vijay; Hassan, Md. Imtaiyaz; Kashav, Tara Molecular Reproduction and Development, Vol. 75, Issue 12 https://doi.org/10.1002/mrd.20910	journal	December 2008
New insights into the molecular mechanisms of sperm-egg interaction Nixon, B.; Aitken, R. J.; McLaughlin, E. A. Cellular and Molecular Life Sciences, Vol. 64, Issue 14 https://doi.org/10.1007/s00018-007-6552-x	journal	April 2007
Presence, localization, and origin of clusterin in normal human spermatozoa Han, Zhijian; Wang, Zengjun; Cheng, Gong Journal of Assisted Reproduction and Genetics, Vol. 29, Issue 8 https://doi.org/10.1007/s10815-012-9779-x	journal	May 2012
Proteomic analysis of heparin-binding proteins from human seminal plasma: a step towards identification of molecular markers of male fertility Kumar, Vijay; Hassan, Md Imtaiyaz; Tomar, Anil Kumar Journal of Biosciences, Vol. 34, Issue 6 https://doi.org/10.1007/s12038-009-0104-5	journal	November 2009
The measurement of insoluble proteins using a modified Bradford assay Gotham, Simon M.; Fryer, Peter J.; Paterson, William R. Analytical Biochemistry, Vol. 173, Issue 2 https://doi.org/10.1016/0003-2697(88)90199-6	journal	September 1988
Functionally active protein C inhibitor/plasminogen activator inhibitor-3 (PCI/PAI-3) is secreted in seminal vesicles, occurs at high concentrations in human seminal plasma and complexes with prostate-specific antigen España, Francisco; Gilabert, Juan; Estellés, Amparo Thrombosis Research, Vol. 64, Issue 3 https://doi.org/10.1016/0049-3848(91)90002-E	journal	November 1991
Disordered zona pellucida–induced acrosome reaction and failure of in vitro fertilization in patients with unexplained infertility Liu, De Yi; Baker, H. W. Gordon Fertility and Sterility, Vol. 79, Issue 1 https://doi.org/10.1016/S0015-0282(02)04555-7	journal	January 2003
Effects of Human Seminal Plasma on Fertilizing Capacity of Human Spermatozoa**Supported by grants from the International Planned Parenthood Federation (to R. Y.) and the Ford Foundation (to A. L.). Kanwar, Kuldip C.; Yanagimachi, Ryuzo; Lopata, Alexander Fertility and Sterility, Vol. 31, Issue 3 https://doi.org/10.1016/S0015-0282(16)43882-3	journal	March 1979
Increased reactive oxygen species formation in semen of patients with spinal cord injury de Lamirande, Eve; Leduc, Bernard E.; Iwasaki, Akira Fertility and Sterility, Vol. 63, Issue 3 https://doi.org/10.1016/S0015-0282(16)57438-X	journal	March 1995
The human kallikrein protein 5 (hK5) is enzymatically active, glycosylated and forms complexes with two protease inhibitors in ovarian cancer fluids Yousef, George M.; Kapadia, Carl; Polymeris, Mary-Ellen Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression, Vol. 1628, Issue 2 https://doi.org/10.1016/S0167-4781(03)00116-7	journal	July 2003
Proteomic identification of target proteins in normal but nonfertilizing sperm Frapsauce, Cynthia; Pionneau, Cedric; Bouley, Julien Fertility and Sterility, Vol. 102, Issue 2 https://doi.org/10.1016/j.fertnstert.2014.04.039	journal	August 2014
Differences in the seminal plasma proteome are associated with oxidative stress levels in men with normal semen parameters Intasqui, Paula; Antoniassi, Mariana Pereira; Camargo, Mariana Fertility and Sterility, Vol. 104, Issue 2 https://doi.org/10.1016/j.fertnstert.2015.04.037	journal	August 2015
Association between the seminal plasma proteome and sperm functional traits Intasqui, Paula; Camargo, Mariana; Antoniassi, Mariana Pereira Fertility and Sterility, Vol. 105, Issue 3 https://doi.org/10.1016/j.fertnstert.2015.11.005	journal	March 2016
Effects of glycodelins on functional competence of spermatozoa Yeung, William S. B.; Lee, Kai-Fai; Koistinen, Riitta Journal of Reproductive Immunology, Vol. 83, Issue 1-2 https://doi.org/10.1016/j.jri.2009.04.012	journal	December 2009
TAT-peroxiredoxin 2 Fusion Protein Supplementation Improves Sperm Motility and DNA Integrity in Sperm Samples from Asthenozoospermic Men Liu, Juan; Zhu, Peng; Wang, Wen T. Journal of Urology, Vol. 195, Issue 3 https://doi.org/10.1016/j.juro.2015.11.019	journal	March 2016
ECM1 interacts with fibulin-3 and the beta 3 chain of laminin 332 through its serum albumin subdomain-like 2 domain Sercu, S.; Lambeir, A. M.; Steenackers, E. Matrix Biology, Vol. 28, Issue 3 https://doi.org/10.1016/j.matbio.2009.02.003	journal	April 2009
Roles of glycodelin in modulating sperm function Yeung, William S. B.; Lee, Kai-Fai; Koistinen, Riitta Molecular and Cellular Endocrinology, Vol. 250, Issue 1-2 https://doi.org/10.1016/j.mce.2005.12.038	journal	May 2006
Comparative analysis of the seminal plasma proteomes of oligoasthenozoospermic and normozoospermic men Giacomini, Elisa; Ura, Blendi; Giolo, Elena Reproductive BioMedicine Online, Vol. 30, Issue 5 https://doi.org/10.1016/j.rbmo.2015.01.010	journal	May 2015
An update on post-ejaculatory remodeling of the sperm surface before mammalian fertilization Gadella, B. M.; Boerke, A. Theriogenology, Vol. 85, Issue 1 https://doi.org/10.1016/j.theriogenology.2015.07.018	journal	January 2016
Simultaneous Detection of Dual Prostate Specific Antigens Using Surface-Enhanced Raman Scattering-Based Immunoassay for Accurate Diagnosis of Prostate Cancer Cheng, Ziyi; Choi, Namhyun; Wang, Rui ACS Nano, Vol. 11, Issue 5 https://doi.org/10.1021/acsnano.7b01536	journal	April 2017
Inhibition of Prostate-Specific Antigen (PSA) by α ₁ -Antichymotrypsin: Salt-Dependent Activation Mediated by a Conformational Change Hsieh, Ming-Ching; Cooperman, Barry S. Biochemistry, Vol. 41, Issue 9 https://doi.org/10.1021/bi0117450	journal	March 2002
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A. Nature Protocols, Vol. 4, Issue 1 https://doi.org/10.1038/nprot.2008.211	journal	December 2008
Large-scale gene function analysis with the PANTHER classification system Mi, Huaiyu; Muruganujan, Anushya; Casagrande, John T. Nature Protocols, Vol. 8, Issue 8 https://doi.org/10.1038/nprot.2013.092	journal	July 2013
Seminal plasma as a diagnostic fluid for male reproductive system disorders Drabovich, Andrei P.; Saraon, Punit; Jarvi, Keith Nature Reviews Urology, Vol. 11, Issue 5 https://doi.org/10.1038/nrurol.2014.74	journal	April 2014
The role of the prostate in male fertility, health and disease Verze, Paolo; Cai, Tommaso; Lorenzetti, Stefano Nature Reviews Urology, Vol. 13, Issue 7 https://doi.org/10.1038/nrurol.2016.89	journal	June 2016
Quantitative Proteomics Analysis of Tissue Interstitial Fluid for Identification of Novel Serum Candidate Diagnostic Marker for Hepatocellular Carcinoma Sun, Wei; Xing, Baocai; Guo, Lihai Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep26499	journal	May 2016
Studies of the bulbo-urethral (Cowper's)-gland mucin and seminal gel of the boar Boursnell, J. C.; Hartree, E. F.; Briggs, P. A. Biochemical Journal, Vol. 117, Issue 5 https://doi.org/10.1042/bj1170981	journal	May 1970
Seminal Fluid Characterization for Male Fertility and Prostate Cancer: Kallikrein-Related Serine Proteases and Whole Proteome Approaches Veveris-Lowe, Tara; Kruger, Sarah; Walsh, Terry Seminars in Thrombosis and Hemostasis, Vol. 33, Issue 1 https://doi.org/10.1055/s-2006-958467	journal	February 2007
New insight into the castrated mouse epididymis based on comparative proteomics Liu, Xin; Wang, Wenjuan; Liu, FuJun Reproduction, Fertility and Development, Vol. 27, Issue 3 https://doi.org/10.1071/RD13323	journal	January 2015
The New Kallikrein-like Gene, KLK-L2 : MOLECULAR CHARACTERIZATION, MAPPING, TISSUE EXPRESSION, AND HORMONAL REGULATION Yousef, George M.; Diamandis, Eleftherios P. Journal of Biological Chemistry, Vol. 274, Issue 53 https://doi.org/10.1074/jbc.274.53.37511	journal	December 1999
Glycodelin-S in Human Seminal Plasma Reduces Cholesterol Efflux and Inhibits Capacitation of Spermatozoa Chiu, Philip C. N.; Chung, Man-Kin; Tsang, Heng-Yan Journal of Biological Chemistry, Vol. 280, Issue 27 https://doi.org/10.1074/jbc.M504103200	journal	May 2005
Human Tissue Kallikrein 5 Is a Member of a Proteolytic Cascade Pathway Involved in Seminal Clot Liquefaction and Potentially in Prostate Cancer Progression Michael, Iacovos P.; Pampalakis, Georgios; Mikolajczyk, Stephen D. Journal of Biological Chemistry, Vol. 281, Issue 18 https://doi.org/10.1074/jbc.M600326200	journal	March 2006
Verification of Male Infertility Biomarkers in Seminal Plasma by Multiplex Selected Reaction Monitoring Assay Drabovich, Andrei P.; Jarvi, Keith; Diamandis, Eleftherios P. Molecular & Cellular Proteomics, Vol. 10, Issue 12 https://doi.org/10.1074/mcp.M110.004127	journal	September 2011
The Neddylation-Cullin 2-RBX1 E3 Ligase Axis Targets Tumor Suppressor RhoB for Degradation in Liver Cancer Xu, Junfeng; Li, Lihui; Yu, Guangyang Molecular & Cellular Proteomics, Vol. 14, Issue 3 https://doi.org/10.1074/mcp.M114.045211	journal	December 2014
Towards Understanding Male Infertility After Spinal Cord Injury Using Quantitative Proteomics da Silva, Barbara Ferreira; Meng, Chen; Helm, Dominic Molecular & Cellular Proteomics, Vol. 15, Issue 4 https://doi.org/10.1074/mcp.M115.052175	journal	January 2016
A Fast Workflow for Identification and Quantification of Proteomes Ding, Chen; Jiang, Jing; Wei, Junying Molecular & Cellular Proteomics, Vol. 12, Issue 8 https://doi.org/10.1074/mcp.O112.025023	journal	May 2013
Primary Structure of a Human Glandular Kallikrein Gene Schedlich, Lynette J.; Bennetts, Bruce H.; Morris, Brian J. DNA, Vol. 6, Issue 5 https://doi.org/10.1089/dna.1987.6.429	journal	October 1987
Assisted reproductive technology in Europe, 2007: results generated from European registers by ESHRE de Mouzon, J.; Goossens, V.; Bhattacharya, S. Human Reproduction, Vol. 27, Issue 4 https://doi.org/10.1093/humrep/des023	journal	February 2012
World Health Organization reference values for human semen characteristics*‡ Cooper, Trevor G.; Noonan, Elizabeth; von Eckardstein, Sigrid Human Reproduction Update, Vol. 16, Issue 3 https://doi.org/10.1093/humupd/dmp048	journal	November 2009
STRING v10: protein–protein interaction networks, integrated over the tree of life Szklarczyk, Damian; Franceschini, Andrea; Wyder, Stefan Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1003	journal	October 2014
Involvement of Semenogelin-Derived Peptides in the Antibacterial Activity of Human Seminal Plasma1 Bourgeon, Frédéric; Evrard, Bertrand; Brillard-Bourdet, Michèle Biology of Reproduction, Vol. 70, Issue 3 https://doi.org/10.1095/biolreprod.103.022533	journal	March 2004
Purification and Characterization of the Active Precursor of a Human Sperm Motility Inhibitor Secreted by the Seminal Vesicles: Identity with Semenogelin1 Robert, Martin; Gagnon, Claude Biology of Reproduction, Vol. 55, Issue 4 https://doi.org/10.1095/biolreprod55.4.813	journal	October 1996
Enzymatic activity of prostate-specific antigen and its reactions with extracellular serine proteinase inhibitors Christensson, Anders; Laurell, Carl-Bertil; Lilja, Hans European Journal of Biochemistry, Vol. 194, Issue 3 https://doi.org/10.1111/j.1432-1033.1990.tb19466.x	journal	December 1990
Complex formation between protein C inhibitor and prostate-specific antigen in vitro and in human semen Christensson, Anders; Lilja, Hans European Journal of Biochemistry, Vol. 220, Issue 1 https://doi.org/10.1111/j.1432-1033.1994.tb18597.x	journal	February 1994
Penetration, Adhesion, and Fusion in Mammalian Sperm-Egg Interaction Primakoff, P. Science, Vol. 296, Issue 5576 https://doi.org/10.1126/science.1072029	journal	June 2002
Differential Diagnosis of Azoospermia with Proteomic Biomarkers ECM1 and TEX101 Quantified in Seminal Plasma Drabovich, A. P.; Dimitromanolakis, A.; Saraon, P. Science Translational Medicine, Vol. 5, Issue 212 https://doi.org/10.1126/scitranslmed.3006260	journal	November 2013
A kallikrein-like serine protease in prostatic fluid cleaves the predominant seminal vesicle protein. Lilja, H. Journal of Clinical Investigation, Vol. 76, Issue 5 https://doi.org/10.1172/JCI112185	journal	November 1985
Seminal vesicle-secreted proteins and their reactions during gelation and liquefaction of human semen. Lilja, H.; Oldbring, J.; Rannevik, G. Journal of Clinical Investigation, Vol. 80, Issue 2 https://doi.org/10.1172/JCI113070	journal	August 1987
iTRAQ-based analysis of sperm proteome from normozoospermic men achieving the rescue-ICSI pregnancy after the IVF failure Liu, Xin; Liu, Gensheng; Liu, Juan Clinical Proteomics, Vol. 15, Issue 1 https://doi.org/10.1186/s12014-018-9203-3	journal	August 2018
Glycodelin: A Major Lipocalin Protein of the Reproductive Axis with Diverse Actions in Cell Recognition and Differentiation Seppälä, Markku; Taylor, Robert N.; Koistinen, Hannu Endocrine Reviews, Vol. 23, Issue 4 https://doi.org/10.1210/er.2001-0026	journal	August 2002
Roles of the reproductive tract in modifications of the sperm membrane surface Kuo, Yu-Wen; Li, Sheng-Hsiang; Maeda, Kei-Ichiro Journal of Reproduction and Development, Vol. 62, Issue 4 https://doi.org/10.1262/jrd.2016-028	journal	January 2016
Effect of homologous and heterologous seminal plasma on the fertilizing ability of ejaculated bull spermatozoa assessed by penetration of zona-free bovine oocytes Henault, M. A.; Killian, G. J. Reproduction, Vol. 108, Issue 2 https://doi.org/10.1530/jrf.0.1080199	journal	November 1996
Immunosuppressive Activity of Human Seminal Plasma Lord, Edith M.; Sensabaugh, George F.; Stites, Daniel P. The Journal of Immunology, Vol. 118, Issue 5 https://doi.org/10.4049/jimmunol.118.5.1704	journal	May 1977
Seminal biomarkers for the evaluation of male infertility Bieniek, JaredM; Drabovich, AndreiP; Lo, KirkC Asian Journal of Andrology, Vol. 18, Issue 3 https://doi.org/10.4103/1008-682X.175781	journal	January 2016

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