Comparative phosphoproteomic analysis of the mouse testis reveals changes in phosphopeptide abundance in response to Ppp1cc deletion

Huttlin, 2010, A tissue-specific atlas of mouse protein phosphorylation and expression, Cell, 143, 1174, 10.1016/j.cell.2010.12.001 Lundby, 2012, Quantitative maps of protein phosphorylation sites across 14 different rat organs and tissues, Nat Commun, 3, 876, 10.1038/ncomms1871 Xu, 2008, Targeted deletion of Tssk1 and 2 causes male infertility due to haploinsufficiency, Dev Biol, 319, 211, 10.1016/j.ydbio.2008.03.047 Shang, 2010, Functional transformation of the chromatoid body in mouse spermatids requires testis-specific serine/threonine kinases, J Cell Sci, 123, 331, 10.1242/jcs.059949 Spiridonov, 2005, Identification and characterization of SSTK, a serine/threonine protein kinase essential for male fertility, Mol Cell Biol, 25, 4250, 10.1128/MCB.25.10.4250-4261.2005 Kawa, 2006, Azoospermia in mice with targeted disruption of the Brek/Lmtk2 (brain-enriched kinase/lemur tyrosine kinase 2) gene, PNAS, 103, 19344, 10.1073/pnas.0603603103 Varmuza, 1999, Spermiogenesis is impaired in mice bearing a targeted mutation in the Protein Phosphatase 1cγ gene, Dev Biol, 205, 98, 10.1006/dbio.1998.9100 Bolino, 2004, Disruption of Mtmr2 produces CMT4B1-like neuropathy with myelin outfolding and impaired spermatogenesis, J Cell Biol, 167, 711, 10.1083/jcb.200407010 Forgione, 2010, Loss of protein phosphatase 1c{gamma} (PPP1CC) leads to impaired spermatogenesis associated with defects in chromatin condensation and acrosome development: an ultrastructural analysis, Reproduction, 139, 1021, 10.1530/REP-10-0063 Takizawa, 1994, Tissue distribution of isoforms of type-1 protein phosphatase PP1 in mouse tissues and its diabetic alterations, J Biochem, 116, 411, 10.1093/oxfordjournals.jbchem.a124540 Sinha, 2012, Significant expression levels of transgenic PPP1CC2 in testis and sperm are required to overcome the male infertility phenotype of Ppp1cc null mice, PLoS ONE, 7, e47623, 10.1371/journal.pone.0047623 Vijayaraghavan, 1996, Sperm motility development in the epididymis is associated with decreased glycogen synthase kinase-3 and protein phosphatase 1 activity, Biol Reprod, 54, 709, 10.1095/biolreprod54.3.709 Huang, 2002, Sperm PP1γ2 is regulated by a homologue of the yeast protein phosphatase binding protein sds221, Biol Reprod, 67, 1936, 10.1095/biolreprod.102.004093 Hrabchak, 2004, Identification of the spermatogenic zip protein Spz1 as a putative protein phosphatase-1 (PP1) regulatory protein that specifically binds the PP1cgamma2 splice variant in the mouse testis, J Biol Chem, 279, 37079, 10.1074/jbc.M403710200 Hrabchak, 2007, A testis specific isoform of endophilin B1, endophilin B1t, interacts specifically with protein phosphatase-1cgamma2 in mouse testis and is abnormally expressed in PP1cgamma null mice, Biochemistry, 46, 4635, 10.1021/bi6025837 Fardilha, 2011, Identification of the human testis protein phosphatase 1 interactome, Biochem Pharmacol, 82, 1403, 10.1016/j.bcp.2011.02.018 Henderson, 2011, New candidate targets of protein phosphatase-1c-gamma-2 in mouse testis revealed by a differential phosphoproteome analysis, Int J Androl, 34, 339, 10.1111/j.1365-2605.2010.01085.x Ruan, 2011, Ornithine decarboxylase antizyme Oaz3 modulates protein phosphatase activity, J Biol Chem, 286, 29417, 10.1074/jbc.M111.274647 Wang, 2011, PP1 forms an active complex with TLRR (lrrc67), a putative PP1 regulatory subunit, during the early stages of spermiogenesis in mice, PLoS ONE, 6, e21767, 10.1371/journal.pone.0021767 MacLeod, 2012, Tandem affinity purification in transgenic mouse embryonic stem cells identifies DDOST as a novel PPP1CC2 interacting protein, Biochemistry, 51, 9678, 10.1021/bi3010158 MacLeod, 2013, PPP1CC2 can form a kinase/phosphatase complex with the testis-specific proteins TSSK1 and TSKS in the mouse testis, Reproduction, 147, 1, 10.1530/REP-13-0224 Baker, 2010, Label-free quantitation of phosphopeptide changes during rat sperm capacitation, J Proteome Res, 9, 718, 10.1021/pr900513d Baker, 2011, Use of titanium dioxide to find phosphopeptide and total protein changes during epididymal sperm maturation, J Proteome Res, 10, 1004, 10.1021/pr1007224 Huang, 2008, Construction of a proteome profile and functional analysis of the proteins involved in the initiation of mouse spermatogenesis, J Proteome Res, 7, 3435, 10.1021/pr800179h Guo, 2011, Proteomic analysis of male 4C germ cell proteins involved in mouse meiosis, Proteomics, 11, 298, 10.1002/pmic.200900726 Varmuza, 2003, Increased recombination frequency showing evidence of loss of interference is associated with abnormal testicular histopathology, Mol Reprod Dev, 64, 499, 10.1002/mrd.10253 Keller, 2002, Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search, Anal Chem, 74, 5383, 10.1021/ac025747h Nesvizhskii, 2003, A statistical model for identifying proteins by tandem mass spectrometry, Anal Chem, 75, 4646, 10.1021/ac0341261 Beausoleil, 2006, A probability-based approach for high-throughput protein phosphorylation analysis and site localization, Nat Biotech, 24, 1285, 10.1038/nbt1240 Huang, 2008, Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources, Nat Protocols, 4, 44, 10.1038/nprot.2008.211 Huang, 2009, Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists, Nucleic Acids Res, 37, 1, 10.1093/nar/gkn923 Aranda, 2011, PSICQUIC and PSISCORE: accessing and scoring molecular interactions, Nat Methods, 8, 528, 10.1038/nmeth.1637 Brown, 2005, Online predicted human interaction database, Bioinformatics, 21, 2076, 10.1093/bioinformatics/bti273 Brown, 2007, Unequal evolutionary conservation of human protein interactions in interologous networks, Genome Biol, 8, R95, 10.1186/gb-2007-8-5-r95 Schilling, 2012, Platform-independent and label-free quantitation of proteomic data using MS1 extracted ion chromatograms in Skyline: application to protein acetylation and phosphorylation, Mol Cell Proteomics, 11, 202, 10.1074/mcp.M112.017707 Thingholm, 2008, SIMAC (sequential elution from IMAC), a phosphoproteomics strategy for the rapid separation of monophosphorylated from multiply phosphorylated peptides, Mol Cell Proteomics, 7, 661, 10.1074/mcp.M700362-MCP200 Thingholm, 2009, Enrichment and separation of mono- and multiply phosphorylated peptides using sequential elution from IMAC prior to mass spectrometric analysis, 67 Liu, 2004, A model for random sampling and estimation of relative protein abundance in shotgun proteomics, Anal Chem, 76, 4193, 10.1021/ac0498563 Ulloa, 1993, Dephosphorylation of distinct sites on microtubule-associated protein MAP1B by protein phosphatases 1, 2A and 2B, FEBS Lett, 330, 85, 10.1016/0014-5793(93)80925-K Hendrickx, 2009, Docking motif-guided mapping of the interactome of protein phosphatase-1, Chem Biol, 16, 365, 10.1016/j.chembiol.2009.02.012 Morimoto, 2002, Interaction of protein phosphatase 1 delta with nucleolin in human osteoblastic cells, J Histochem Cytochem, 50, 1187, 10.1177/002215540205000905 Tanuma, 2008, Nuclear inhibitor of protein phosphatase-1 (NIPP1) directs protein phosphatase-1 (PP1) to dephosphorylate the U2 small nuclear ribonucleoprotein particle (snRNP) component, spliceosome-associated protein 155 (Sap155), J Biol Chem, 283, 35805, 10.1074/jbc.M805468200 Chelius, 2002, Quantitative profiling of proteins in complex mixtures using liquid chromatography and mass spectrometry, J Proteome Res, 1, 317, 10.1021/pr025517j Jain, 2003, Local-pooled-error test for identifying differentially expressed genes with a small number of replicated microarrays, Bioinformatics, 19, 1945, 10.1093/bioinformatics/btg264 Colinge, 2005, Differential proteomics via probabilistic peptide identification scores, Anal Chem, 77, 596, 10.1021/ac0488513 Bollen, 2010, The extended PP1 toolkit: designed to create specificity, Trends Biochem Sci, 35, 450, 10.1016/j.tibs.2010.03.002 Egloff, 1997, Structural basis for the recognition of regulatory subunits by the catalytic subunit of protein phosphatase 1, EMBO J, 16, 1876, 10.1093/emboj/16.8.1876 Bellve, 1977, Spermatogenic cells of the prepuberal mouse: isolation and morphological characterization, J Cell Biol, 74, 68, 10.1083/jcb.74.1.68 Chakrabarti, 2007, Analysis of Ppp1cc-null mice suggests a role for PP1gamma2 in sperm morphogenesis, Biol Reprod, 76, 992, 10.1095/biolreprod.106.058610 Cagney, 2005, Human tissue profiling with multidimensional protein identification technology, J Proteome Res, 4, 1757, 10.1021/pr0500354 Baker, 2007, Identification of gene products present in Triton X-100 soluble and insoluble fractions of human spermatozoa lysates using LC–MS/MS analysis, Proteomics Clin Appl, 1, 524, 10.1002/prca.200601013 Baker, 2008, The mouse sperm proteome characterized via IPG strip prefractionation and LC–MS/MS identification, Proteomics, 8, 1720, 10.1002/pmic.200701020 de Mateo, 2011, Proteomic characterization of the human sperm nucleus, Proteomics, 11, 2714, 10.1002/pmic.201000799 Bodenmiller, 2007, Reproducible isolation of distinct, overlapping segments of the phosphoproteome, Nat Methods, 4, 231, 10.1038/nmeth1005 Ham, 2010, Novel Ser/Thr protein phosphatase 5 (PP5) regulated targets during DNA damage identified by proteomics analysis, J Proteome Res, 9, 945, 10.1021/pr9008207 Wang, 1998, Phosphorylation of spliceosomal protein SAP 155 coupled with splicing catalysis, Genes Dev, 12, 1409, 10.1101/gad.12.10.1409 Eto, 2011, The kinase DYRKIA regulates pre-mRNA splicing in spermatogonia and proliferation of spermatogonia and Sertoli cells by phosphorylating a spliceosomal component, SAP155, in postnatal murine testes, Mol Cell Biochem, 355, 217, 10.1007/s11010-011-0857-7 Yatsenko, 2013, UBE2B mRNA alterations are associated with severe oligozoospermia in infertile men, Mol Hum Reprod, 19, 388, 10.1093/molehr/gat008 Byers, 1991, Development of Sertoli cell junctional specializations and the distribution of the tight-junction-associated protein ZO-1 in the mouse testis, Am J Anat, 191, 35, 10.1002/aja.1001910104 Held, 2011, Heat-shock protein HSPA4 is required for progression of spermatogenesis, Reproduction, 142, 133, 10.1530/REP-11-0023 Dix, 1996, Targeted gene disruption of Hsp70-2 results in failed meiosis, germ cell apoptosis, and male infertility, PNAS, 93, 3264, 10.1073/pnas.93.8.3264 Liu, 2003, Hmga1 is required for normal sperm development, Mol Reprod Dev, 66, 81, 10.1002/mrd.10323 Yang, 2006, Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis, J Cell Biol, 173, 497, 10.1083/jcb.200603063 Fukuda, 2012, Phosphorylation of chromosome core components may serve as axis marks for the status of chromosomal events during mammalian meiosis, PLoS Genet, 8, e1002485, 10.1371/journal.pgen.1002485 Yang, 2005, Absence of the DNA-/RNA-binding protein MSY2 results in male and female infertility, PNAS, 102, 5755, 10.1073/pnas.0408718102 Okamura, 2012, Cell cycle gene-specific control of transcription has a critical role in proliferation of primordial germ cells, Genes Dev, 26, 2477, 10.1101/gad.202242.112 Sutherland, 2006, Disruption of Ledgf/Psip1 results in perinatal mortality and homeotic skeletal transformations, Mol Cell Biol, 26, 7201, 10.1128/MCB.00459-06 Wakayama, 2007, Heterophilic binding of the adhesion molecules poliovirus receptor and immunoglobulin superfamily 4A in the interaction between mouse spermatogenic and sertoli cells, Biol Reprod, 76, 1081, 10.1095/biolreprod.106.058974 Nagai, 2011, Mice lacking Ran binding protein 1 are viable and show male infertility, FEBS Lett, 585, 791, 10.1016/j.febslet.2011.02.002