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Looking for Missing Proteins in the Proteome of Human Spermatozoa: An Update

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Download Hi-Res ImageDownload to MS-PowerPointCite This:J. Proteome Res. 2016, 15, 11, 3998-4019
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    Looking for Missing Proteins in the Proteome of Human Spermatozoa: An Update
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    † CEA, DRF, BIG, Laboratoire de Biologie à Grande Echelle, 17 rue des martyrs, Grenoble F-38054, France
    ‡ Inserm U1038, 17, rue des Martyrs, Grenoble F-38054, France
    § Université de Grenoble, Grenoble F-38054, France
    ∥ Department of Human Protein Sciences, Faculty of Medicine, University of Geneva, 1, rue Michel-Servet, 1211 Geneva 4, Switzerland
    ⊥ CALIPHO Group, SIB-Swiss Institute of Bioinformatics, CMU, rue Michel-Servet 1, CH-1211 Geneva 4, Switzerland
    # Laboratoire de Spectrométrie de Masse BioOrganique (LSMBO), IPHC, Université de Strasbourg, CNRS UMR7178, 25 Rue Becquerel, 67087 Strasbourg, France
    ▽ Protim, Inserm U1085, Irset, Campus de Beaulieu, Rennes 35042, France
    ○ Institut de Pharmacologie et de Biologie Structurale, Université de Toulouse, CNRS, UPS, 31062 Toulouse, France
    ◆ Proteome Informatics Group, Centre Universitaire d’Informatique, Route de Drize 7, 1227 Carouge, CH, Switzerland
    Service de Médecine de la Reproduction, CHU de Nantes, 38 boulevard Jean Monnet, 44093 Nantes cedex, France
    + INSERM UMR1064, Nantes 44093, France
    □ Department of Immunology, Genetics and Pathology, Science for Life Laboratory, Uppsala University, Uppsala 751 85, Sweden
    *Y.V.: E-mail: [email protected]. Tel: +33 (0)4 38 78 26 74. Fax: (33) (0)4 38 78 50 32.
    *C.P.: E-mail: [email protected]. Tel: +33 (0)2 23 23 52 79.
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    Journal of Proteome Research

    Cite this: J. Proteome Res. 2016, 15, 11, 3998–4019
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    https://doi.org/10.1021/acs.jproteome.6b00400
    Published July 22, 2016
    Copyright © 2016 American Chemical Society
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    Abstract

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    The Chromosome-Centric Human Proteome Project (C-HPP) aims to identify “missing” proteins in the neXtProt knowledgebase. We present an in-depth proteomics analysis of the human sperm proteome to identify testis-enriched missing proteins. Using protein extraction procedures and LC–MS/MS analysis, we detected 235 proteins (PE2–PE4) for which no previous evidence of protein expression was annotated. Through LC–MS/MS and LC–PRM analysis, data mining, and immunohistochemistry, we confirmed the expression of 206 missing proteins (PE2–PE4) in line with current HPP guidelines (version 2.0). Parallel reaction monitoring acquisition and sythetic heavy labeled peptides targeted 36 ≪one-hit wonder≫ candidates selected based on prior peptide spectrum match assessment. 24 were validated with additional predicted and specifically targeted peptides. Evidence was found for 16 more missing proteins using immunohistochemistry on human testis sections. The expression pattern for some of these proteins was specific to the testis, and they could possibly be valuable markers with fertility assessment applications. Strong evidence was also found of four “uncertain” proteins (PE5); their status should be re-examined. We show how using a range of sample preparation techniques combined with MS-based analysis, expert knowledge, and complementary antibody-based techniques can produce data of interest to the community. All MS/MS data are available via ProteomeXchange under identifier PXD003947. In addition to contributing to the C-HPP, we hope these data will stimulate continued exploration of the sperm proteome.

    Copyright © 2016 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jproteome.6b00400.

    • Shotgun LC–MS/MS analyses. 2. LC–MS/MS analysis of labeled synthetic peptides and comparison of fragmentation spectra. 3. How targeted LC–PRM assays were developed (details). (PDF)

    • Supplementary Figure 1: MS/MS spectra for the 36 endogenous peptides and their synthetic reference counterparts combined with LC–PRM results for the 36 peptides, additional predicted proteotypic peptides, and their labeled synthetic counterparts. (PDF)

    • Supplementary Table 1: PSM-, peptide-, and protein-level FDR values along with the total number of expected true- and false-positives at each level for each sperm proteome data set and the combined data set (tab 1: total cell lysate followed by a 1D SDS-PAGE separation of proteins (23 gel slices), tab 2: total cell lysate, in-gel digestion of proteins, and total peptide analysis by nanoLC with long gradient runs, tab 3: total cell lysate, in-gel digestion of proteins, and peptide fractionation by high-pH reversed-phase (HpH-RP) chromatography; tabs 4 and 5: fractionation of proteins into Triton X-100-soluble and -insoluble fractions, followed by 1D SDS-PAGE separation of proteins (20 gel slices per fraction); tab 6: combined data set corresponding to the combination of results for the five proteome data sets). (XLSX)

    • Supplementary Table 2: List of proteins identified and validated with a protein-level 1% FDR for each fraction (detailed information): tab 1: total cell lysate followed by a 1D SDS-PAGE separation of proteins (23 gel slices), tab 2: total cell lysate, in-gel digestion of proteins, and total peptide analysis by nanoLC with long gradient runs, tab 3: total cell lysate, in-gel digestion of proteins, and peptide fractionation by high-pH reversed-phase (HpH-RP) chromatography; tabs 4 and 5: fractionation of proteins into Triton X-100-soluble and -insoluble fractions, followed by 1D SDS-PAGE separation of proteins (20 gel slices per fraction). (XLSX)

    • Supplementary Table 3: Missing (PE2–4) and uncertain (PE5) proteins detected in the sperm proteome: detailed information. Accession numbers, entry description, molecular weight (MW), protein length (length) number of transmembrane domains (No. TMH), subcellular location, and function (CC field) were retrieved from UniprotKB; gene names and chromosome location are as referenced in neXtProt. Coverage (protein coverage in %) and number of unique peptides mapping to missing proteins, proteins seen (yes)/not seen (not) in each of the five MS/MS data sets acquired in this study are reported. The expression annotations of the Human testis gene expression program (TGEP (5)) were also reported when available (SET: proteins produced by genes specifically expressed in the testis; PET: proteins produced by genes preferentially expressed in the testis; IE: proteins produced by genes with intermediate expression in the testis; UE: proteins produced by genes with ubiquitous expression in the testis). The ≪testis-enriched gene≫ status in the Human Protein Atlas version 15 is also provided. (XLSX)

    • Supplementary Table 4: tab 1: List of one-hit wonder missing proteins identified and selected for further spectral comparison (MS/MS) and PRM validation. tab 2: Extended list of 100 peptides selected for validation of the 36 one hit wonders and synthesized as crude labeled peptides. (XLSX)

    • Supplementary Table 5: List of 111 PE2–5 proteins for which complete data mining was performed, showing the rationale for their prioritization for subsequent antibody-based studies. Entry accession numbers (column A) and gene names (column B) were retrieved from UniProtKB, transcript abundance was retrieved from HPA (column C), phylogenetic profiles in ciliated organisms were determined by Blast analysis on UniProtKB “Reference proteomes” (column D), knockout mice phenotypes were retrieved from MGI (column E), associated publications that were not annotated in neXtProt were searched in PubMed (column F), and immunohistochemistry data was retrieved from HPA (column G). For all these criteria, a four-color grading system was adopted. Dark-green and green cells were retained as positive criteria, red cells as negative ones. Based on these criteria, a score of relevance (high/medium/low) for the implication of the proteins in spermatogenesis has been assigned (column H). The existence of a suitable antibody in HPA is reported in column I, and the list of proteins that were finally selected for IHC is provided in column J. (XLSX)

    • Supplementary Table 6: List of missing proteins for which IHC was successful, HPA antibody names, and dilutions used. (XLSX)

    • Supplementary Table 7: List of the 94 missing proteins detected in Jumeau et al. (2015) (14) and confirmed in the present study. The number of peptides identified in each study is reported in columns C and E. The protein existence (PE) status of the entries in the 2015 and 2016 neXtProt reference releases is reported in columns B and F. (XLSX)

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    Cite this: J. Proteome Res. 2016, 15, 11, 3998–4019
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    https://doi.org/10.1021/acs.jproteome.6b00400
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