Bovine sperm plasma membrane proteomics through biotinylation and subcellular enrichment

A significant proportion of mammalian fertilization is mediated through the proteomic composition of the sperm surface. These protein constituents can present as biomarkers to control and regulate breeding of agricultural animals. Previous studies have addressed the bovine sperm cell apical plasma membrane (PM) proteome with nitrogen cavitation enrichment. Alternative workflows would enable to expand the compositional data more globally around the entire sperm's surface. We used a cell surface biotin‐labeling in combination with differential centrifugation to enrich sperm surface proteins. Using nano‐LC MS/MS, 338 proteins were confidently identified in the PM‐enriched proteome. Functional categories of sperm–egg interaction, protein turnover, metabolism as well as molecular transport, spermatogenesis, and signal transduction were represented by proteins with high quantitative signal in our study. A highly significant degree of enrichment was found for transmembrane and PM‐targeted proteins. Among them, we also report proteins previously not described on bovine sperm (CPQ, CD58, CKLF, CPVL, GLB1L3, and LPCAT2B) of which CPQ and CPVL cell surface localization was further validated. A descriptive overview of the bovine sperm PM integral and peripheral proteins is provided to complement future studies on animal reproduction and its relation to sperm cell surface. All MS data have been deposited in the ProteomeXchange with identifier PXD001096 (http://proteomecentral.proteomexchange.org/dataset/PXD001096).

[1]  Andrew R. Jones,et al.  ProteomeXchange provides globally co-ordinated proteomics data submission and dissemination , 2014, Nature Biotechnology.

[2]  T. McGraw,et al.  Specialized sorting of GLUT4 and its recruitment to the cell surface are independently regulated by distinct Rabs , 2013, Molecular biology of the cell.

[3]  M. Resh.  Covalent lipid modifications of proteins , 2013, Current Biology.

[4]  C. Pineau,et al.  Identification of sperm head proteins involved in zona pellucida binding. , 2013, Human reproduction.

[5]  R. Zubarev.  The challenge of the proteome dynamic range and its implications for in‐depth proteomics , 2013, Proteomics.

[6]  Jun Yu,et al.  In-depth proteomic analysis of the human sperm reveals complex protein compositions. , 2013, Journal of proteomics.

[7]  M. Colgrave,et al.  Comprehensive mapping of the bull sperm surface proteome , 2012, Proteomics.

[8]  R. Sullivan,et al.  Bovine sperm raft membrane associated Glioma Pathogenesis‐Related 1‐like protein 1 (GliPr1L1) is modified during the epididymal transit and is potentially involved in sperm binding to the zona pellucida , 2012, Journal of cellular physiology.

[9]  Damian Szklarczyk,et al.  STRING v9.1: protein-protein interaction networks, with increased coverage and integration , 2012, Nucleic Acids Res..

[10]  Brett Nixon,et al.  The Molecular Chaperone HSPA2 Plays a Key Role in Regulating the Expression of Sperm Surface Receptors That Mediate Sperm-Egg Recognition , 2012, PloS one.

[11]  Chaitanya A. K. Koppisetty,et al.  Sperm arylsulfatase A binds to mZP2 and mZP3 glycoproteins in a nonenzymatic manner. , 2012, Reproduction.

[12]  F. Gozzo,et al.  Proteomic analysis of the reproductive tract fluids from tropically-adapted Santa Ines rams. , 2012, Journal of proteomics.

[13]  A. Kudlicki.  The Optimal Exponent Base for emPAI Is 6.5 , 2012, PloS one.

[14]  B. Gadella,et al.  Sperm surface changes and physiological consequences induced by sperm handling and storage. , 2011, Reproduction.

[15]  S. Brunak,et al.  SignalP 4.0: discriminating signal peptides from transmembrane regions , 2011, Nature Methods.

[16]  A. Shevchenko,et al.  Human Lysophosphatidylcholine Acyltransferases 1 and 2 Are Located in Lipid Droplets Where They Catalyze the Formation of Phosphatidylcholine* , 2011, The Journal of Biological Chemistry.

[17]  B. Nixon,et al.  Glioma pathogenesis-related 1-like 1 is testis enriched, dynamically modified, and redistributed during male germ cell maturation and has a potential role in sperm-oocyte binding. , 2010, Endocrinology.

[18]  K. Toshimori,et al.  Tetraspanin family protein CD9 in the mouse sperm: unique localization, appearance, behavior and fate during fertilization , 2010, Cell and Tissue Research.

[19]  Albert J R Heck,et al.  Exploring the membrane proteome--challenges and analytical strategies. , 2010, Journal of proteomics.

[20]  B. Gadella,et al.  Sperm surface proteomics: from protein lists to biological function. , 2010, Molecular human reproduction.

[21]  Stuart J Cordwell,et al.  Technologies for plasma membrane proteomics , 2010, Proteomics.

[22]  T. Kislinger,et al.  Isolation of cell surface proteins for mass spectrometry-based proteomics , 2010, Expert review of proteomics.

[23]  J. Pei,et al.  Izumo is part of a multiprotein family whose members form large complexes on mammalian sperm , 2009, Molecular Reproduction and Development.

[24]  Sarman Singh,et al.  Proteomic analysis of heparin-binding proteins from human seminal plasma: a step towards identification of molecular markers of male fertility , 2009, Journal of Biosciences.

[25]  G. Kay,et al.  The Glycosylphosphatidylinositol-Anchored Serine Protease PRSS21 (Testisin) Imparts Murine Epididymal Sperm Cell Maturation and Fertilizing Ability1 , 2009, Biology of reproduction.

[26]  E. S. Díaz,et al.  Participation of the Human Sperm Proteasome in the Capacitation Process and Its Regulation by Protein Kinase A and Tyrosine Kinase1 , 2009, Biology of reproduction.

[27]  B. He,et al.  The Novel Epididymis-Specific Beta-Galactosidase-Like Gene Glb1l4 Is Essential in Epididymal Development and Sperm Maturation in Rats1 , 2009, Biology of reproduction.

[28]  M. Mann,et al.  MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification , 2008, Nature Biotechnology.

[29]  Brad T. Sherman,et al.  Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists , 2008, Nucleic acids research.

[30]  R. Pérez-Pé,et al.  Seminal plasma proteins and sperm resistance to stress. , 2008, Reproduction in domestic animals = Zuchthygiene.

[31]  G. Elia.  Biotinylation reagents for the study of cell surface proteins , 2008, Proteomics.

[32]  Pier Luigi Martelli,et al.  PredGPI: a GPI-anchor predictor , 2008, BMC Bioinformatics.

[33]  Y. Maeda,et al.  Biosynthesis, remodelling and functions of mammalian GPI-anchored proteins: recent progress. , 2008, Journal of biochemistry.

[34]  Wei Xu,et al.  RAB2A: A Major Subacrosomal Protein of Bovine Spermatozoa Implicated in Acrosomal Biogenesis1 , 2008, Biology of reproduction.

[35]  U. Wolfrum,et al.  Expression and compartmentalisation of the glycolytic enzymes GAPDH and pyruvate kinase in boar spermatogenesis. , 2008, Reproduction, fertility, and development.

[36]  R. Aitken,et al.  The mouse sperm proteome characterized via IPG strip prefractionation and LC‐MS/MS identification , 2008, Proteomics.

[37]  E. S. Díaz,et al.  The role of sperm proteasomes during sperm aster formation and early zygote development: implications for fertilization failure in humans. , 2008, Human reproduction.

[38]  Bindu Nanduri,et al.  Comprehensive proteomic analysis of bovine spermatozoa of varying fertility rates and identification of biomarkers associated with fertility , 2008, BMC Systems Biology.

[39]  Xin Chen,et al.  FragAnchor: A Large-Scale Predictor of Glycosylphosphatidylinositol Anchors in Eukaryote Protein Sequences by Qualitative Scoring , 2007, Genom. Proteom. Bioinform..

[40]  Christine C. Wu,et al.  Proteomics of integral membrane proteins--theory and application. , 2007, Chemical reviews.

[41]  R. Aitken,et al.  Identification of gene products present in Triton X‐100 soluble and insoluble fractions of human spermatozoa lysates using LC‐MS/MS analysis , 2007, Proteomics. Clinical applications.

[42]  Brian R. King,et al.  ngLOC: an n-gram-based Bayesian method for estimating the subcellular proteomes of eukaryotes , 2007, Genome biology.

[43]  K. Roberts,et al.  Effects of seminal plasma on cooling-induced capacitative changes in boar sperm. , 2006, Journal of andrology.

[44]  S. Gordon,et al.  A vitellogenic‐like carboxypeptidase expressed by human macrophages is localized in endoplasmic reticulum and membrane ruffles , 2006, International journal of experimental pathology.

[45]  D. Johnston,et al.  Analysis of the Human Sperm Proteome , 2005, Annals of the New York Academy of Sciences.

[46]  H. Scrable,et al.  Isolation and Proteomic Analysis of Mouse Sperm Detergent-Resistant Membrane Fractions: Evidence for Dissociation of Lipid Rafts During Capacitation1 , 2005, Biology of reproduction.

[47]  M. Mann,et al.  Exponentially Modified Protein Abundance Index (emPAI) for Estimation of Absolute Protein Amount in Proteomics by the Number of Sequenced Peptides per Protein*S , 2005, Molecular & Cellular Proteomics.

[48]  Niklaus Fankhauser,et al.  Identification of GPI anchor attachment signals by a Kohonen self-organizing map , 2005, Bioinform..

[49]  Christian von Mering,et al.  STRING: known and predicted protein–protein associations, integrated and transferred across organisms , 2004, Nucleic Acids Res..

[50]  C. Mukai,et al.  Glycolysis Plays a Major Role for Adenosine Triphosphate Supplementation in Mouse Sperm Flagellar Movement , 2004, Biology of reproduction.

[51]  R. Scheller,et al.  Rab14 is involved in membrane trafficking between the Golgi complex and endosomes. , 2004, Molecular biology of the cell.

[52]  N. Blom,et al.  Feature-based prediction of non-classical and leaderless protein secretion. , 2004, Protein engineering, design & selection : PEDS.

[53]  Wei Zhang,et al.  Proteomic analysis of integral plasma membrane proteins. , 2004, Analytical chemistry.

[54]  M. Wade,et al.  Acquisition of Arylsulfatase A onto the Mouse Sperm Surface During Epididymal Transit1 , 2003, Biology of reproduction.

[55]  T. Muramatsu,et al.  Basigin (CD147): a multifunctional transmembrane protein involved in reproduction, neural function, inflammation and tumor invasion. , 2003, Histology and histopathology.

[56]  M. Kong,et al.  Participation of the sperm proteasome in human fertilization. , 2003, Human reproduction.

[57]  M. Ikawa,et al.  Disruption of Mouse CD46 Causes an Accelerated Spontaneous Acrosome Reaction in Sperm , 2003, Molecular and Cellular Biology.

[58]  M. Mann,et al.  Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. , 2003, Analytical chemistry.

[59]  P. Martin-DeLeon,et al.  Mouse epididymal Spam1 (pH-20) is released in the luminal fluid with its lipid anchor. , 2003, Journal of andrology.

[60]  M. Buhr,et al.  Isolation and unique composition of purified head plasma membrane from rooster sperm. , 2002, Poultry science.

[61]  H. Yokosawa,et al.  Extracellular ubiquitination and proteasome-mediated degradation of the ascidian sperm receptor , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[62]  W. Han,et al.  [Stimulatory effect of chemokine-like factor 1 (CKLF1) on the growth of bone marrow cells]. , 2001, Zhongguo yi xue ke xue yuan xue bao. Acta Academiae Medicinae Sinicae.

[63]  R. Pérez-Pé,et al.  Seminal Plasma Proteins Revert the Cold-Shock Damage on Ram Sperm Membrane1 , 2000, Biology of reproduction.

[64]  B. Snel,et al.  STRING: a web-server to retrieve and display the repeatedly occurring neighbourhood of a gene. , 2000, Nucleic acids research.

[65]  P. Bork,et al.  Prediction of potential GPI-modification sites in proprotein sequences. , 1999, Journal of molecular biology.

[66]  J. Vera,et al.  Hexose transporter expression and function in mammalian spermatozoa: Cellular localization and transport of hexoses and vitamin C , 1998, Journal of cellular biochemistry.

[67]  Erik L. L. Sonnhammer,et al.  A Hidden Markov Model for Predicting Transmembrane Helices in Protein Sequences , 1998, ISMB.

[68]  A. Travis,et al.  Targeting of a germ cell-specific type 1 hexokinase lacking a porin-binding domain to the mitochondria as well as to the head and fibrous sheath of murine spermatozoa. , 1998, Molecular biology of the cell.

[69]  P. Primakoff,et al.  A Role for the Disintegrin Domain of Cyritestin, a Sperm Surface Protein Belonging to the ADAM Family, in Mouse Sperm–Egg Plasma Membrane Adhesion and Fusion , 1997, The Journal of cell biology.

[70]  R. Henkel,et al.  Low expression of adhesion molecules and matrix proteins in patients showing poor penetration in zona-free hamster oocytes. , 1996, Molecular human reproduction.

[71]  N. Cross.  Phosphatidylcholine enhances the acrosomal responsiveness of human sperm. , 1994, Journal of andrology.

[72]  P. Johnson,et al.  Inhibition of human spermatozoon-oocyte interaction in vitro by monoclonal antibodies to CD46 (membrane cofactor protein). , 1994, Human reproduction.

[73]  J. Atkinson,et al.  Identification and characterization of membrane cofactor protein of human spermatozoa. , 1992, Journal of immunology.

[74]  A. M. Simpson,et al.  Action of phosphatidylcholine in protecting ram sperm from cold shock , 1986 .

[75]  Y. Fujiki,et al.  Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum , 1982, The Journal of cell biology.

[76]  Brad T. Sherman,et al.  Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources , 2008, Nature Protocols.

[77]  R. Aitken,et al.  The rat sperm proteome characterized via IPG strip prefractionation and LC‐MS/MS identification , 2008, Proteomics.

[78]  P. Manjunath,et al.  Role of seminal plasma phospholipid-binding proteins in sperm membrane lipid modification that occurs during capacitation. , 2002, Journal of reproductive immunology.