Sperm phosphoproteomics: Historical perspectives and current methodologies

Expert Review of Proteomics

Volumn 9, Issue 5, 2012, Pages 533-548

  Porambo, James R ^a   Salicioni, Ana M ^b   Visconti, Pablo E ^b   Platt, Mark D ^a,c  

^a Rensselaer Polytechnic Institute   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c RENSSELAER POLYTECHNIC INSTITUTE   (United States)

Author keywords

peptide quantitation; phosphoproteomics; phosphorylation; proteomics; sperm

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; PHOSPHOPROTEIN;

AMINO ACID SEQUENCE; HUMAN; MASS SPECTROMETRY; NONHUMAN; PHOSPHOPROTEOMICS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEOMICS; REVIEW; SEMEN ANALYSIS; SPERM; SPERMATOGENESIS; SPERMATOZOON MATURATION; SPERMATOZOON MOTILITY; TESTIS FUNCTION;

FERTILIZATION; GENE EXPRESSION REGULATION; HUMANS; INFERTILITY, MALE; MALE; MASS SPECTROMETRY; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEOMICS; SPERMATOZOA;

MAMMALIA;

EID: 84870594479     PISSN: 14789450     EISSN: 17448387     Source Type: Journal    
DOI: 10.1586/epr.12.41     Document Type: Review

References (117)

1. De Jonge CJ, Barratt CLR (Eds). The Sperm Cell Production, Maturation, Fertilization, Regeneration. Cambridge University Press, NY, USA (2006).
2. Bloch D. A catalog of sperm histones. Genetics 61(1), 93-111 (1969).
3. Díez-Sánchez C, Ruiz-Pesini E, Montoya J, Pérez-Martos A, Enríquez JA, López-Pérez MJ. Mitochondria from ejaculated human spermatozoa do not synthesize proteins. FEBS Lett. 553(1-2), 205-208 (2003).
4. Aitken RJ, Nixon B, Lin M, Koppers AJ, Lee YH, Baker MA. Proteomic changes in mammalian spermatozoa during epididymal maturation. Asian J. Androl. 9(4), 554-564 (2007).
5. Roberts KP, Ensrud KM, Wooters JL, Nolan MA, Johnston DS, Hamilton DW. Epididymal secreted protein Crisp-1 and sperm function. Mol. Cell. Endocrinol. 250(1-2), 122-127 (2006).
6. O'Rand MG, Widgren EE, Hamil KG, Silva EJ, Richardson RT. Epididymal protein targets: a brief history of the development of EPPIN as a contraceptive target. J. Androl. 32(6), 698-704 (2011).
7. Vijayaraghavan S, Stephens DT, Trautman K et al. Sperm motility development in the epididymis is associated with decreased glycogen synthase kinase-3 and protein phosphatase 1 activity. Biol. Reprod. 54(3), 709-718 (1996).
8. Visconti PE, Krapf D, de la Vega-Beltrán JL, Acevedo JJ, Darszon A. Ion channels, phosphorylation and mammalian sperm capacitation. Asian J. Androl. 13(3), 395-405 (2011).
9. Cox J, Mann M. Is proteomics the new genomics? Cell 130(3), 395-398 (2007).
10. Wilkins MR, Sanchez JC, Gooley AA et al. Progress with proteome projects: why all proteins expressed by a genome should be identifed and how to do it. Biotechnol. Genet. Eng. Rev. 13, 19-50 (1996).
11. Felix K, Krekels A. Die endaminosauren einiger protamine. Hoppe-Seylers Zeitschrift Fur Physiologische Chemie 295, 107-109 (1953).
12. Ingles CJ, Dixon GH. Phosphorylation of protamine during spermatogenesis in trout testis. Proc. Natl Acad. Sci. USA 58(3), 1011-1018 (1967).
13. Garbers D, Lust W, First N, Lardy H. Effects of phosphodiesterase inhibitors and cyclic nucleotides on sperm respiration and mot i lit y. Biochemistry 10 (10), 1825-1831 (1971).
14. Hoskins DD, Casillas ER, Stephens DT. Cyclic AMP-dependent protein kinases of bovine epididymal spermatozoa. Biochem. Biophys. Res. Commun. 48(6), 1131-1138 (1972).
15. Brandt H, Hoskins DD. A cAMP-dependent phosphorylated motility protein in bovine epididymal sperm. J. Biol. Chem. 255(3), 982-987 (1980).
16. Frackelton AR Jr, Ross AH, Eisen HN. Characterization and use of monoclonal antibodies for isolation of phosphotyrosyl proteins from retrovirus-transformed cells and growth factor-stimulated cells. Mol. Cell. Biol. 3(8), 1343-1352 (1983).
17. Leyton L, Saling P. 95 kd sperm proteins bind ZP3 and serve as tyrosine kinase substrates in response to zona binding. Cell 57(7), 1123-1130 (1989).
18. Kalab P, Visconti P, Leclerc P, Kopf GS. p95, the major phosphotyrosine-containing protein in mouse spermatozoa, is a hexokinase with unique properties. J. Biol. Chem. 269(5), 3810-3817 (1994).
19. Visconti PE, Bailey JL, Moore GD, Pan D, Olds-Clarke P, Kopf GS. Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 121(4), 1129-1137 (1995).
20. Visconti PE, Moore GD, Bailey JL et al. Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development 121(4), 1139-1150 (1995).
21. Galantino-Homer HL, Visconti PE, Kopf GS. Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3́5́-monophosphate-dependent pathway. Biol. Reprod. 56(3), 707-719 (1997).
22. Leclerc P, de Lamirande E, Gagnon C. Cyclic adenosine 3, 5́monophosphate-dependent regulation of protein tyrosine phosphorylation in relation to human sperm capacitation and motility. Biol. Reprod. 55(3), 684-692 (1996).
23. Kalab P, Peknicová J, Geussová G, Moos J. Regulation of protein tyrosine phosphorylation in boar sperm through a cAMP-dependent pathway. Mol. Reprod. Dev. 51(3), 304-314 (1998).
24. Naaby-Hansen S, Flickinger CJ, Herr JC. Two-dimensional gel electrophoretic analysis of vectorially labeled surface proteins of human spermatozoa. Biol. Reprod. 56(3), 771-787 (1997).
25. Mandal A, Naaby-Hansen S, Wolkowicz MJ et al. FSP95, a testis-specifc 95-kilodalton fbrous sheath antigen that undergoes tyrosine phosphorylation in capacitated human spermatozoa. Biol. Reprod. 61(5), 1184-1197 (1999).
26. Shetty J, Diekman AB, Jayes FC et al. Differential extraction and enrichment of human sperm surface proteins in a proteome: identifcation of immunocontraceptive candidates. Electrophoresis 22(14), 3053-3066 (2001).
27. Bohring C, Krause E, Habermann B, Krause W Isolation and identifcation of sperm membrane antigens recognized by antisperm antibodies, and their possible role in immunological infertility disease. Mol. Hum. Reprod. 7(2), 113-118 (2001).
28. Ficarro S, Chertihin O, Westbrook VA et al. Phosphoproteome analysis of capacitated human sperm. Evidence of tyrosine phosphorylation of a kinase-anchoring protein 3 and valosin-containing protein/p97 during capacitation. J. Biol. Chem. 278(13), 11579-11589 (2003).
29. Arcelay E, Salicioni AM, Wertheimer E, Visconti PE. Identifcation of proteins undergoing tyrosine phosphorylation during mouse sperm capacitation. Int. J. Dev. Biol. 52(5-6), 463-472 (2008).
30. Kota V, Dhople VM, Shivaji S. Tyrosine phosphoproteome of hamster spermatozoa: role of glycerol-3-phosphate dehydrogenase 2 in sperm capacitation. Proteomics 9(7), 1809-1826 (2009).
31. Johnson SA, Hunter T Kinomics: methods for deciphering the kinome. Nat. Methods 2(1), 17-25 (2005).
32. de Lamirande E, Gagnon C. The extracellular signal-regulated kinase (ERK) pathway is involved in human sperm function and modulated by the superoxide anion. Mol. Hum. Reprod. 8(2), 124-135 (2002).
33. Luconi M, Barni T, Vannelli GB et al. Extracellular signal-regulated kinases modulate capacitation of human spermatozoa. Biol. Reprod. 58(6), 1476-1489 (1998).
34. Zhang H, Zha X, Tan Y et al. Phosphoprotein analysis using antibodies broadly reactive against phosphorylated motifs. J. Biol. Chem. 277(42), 39379-39387 (2002).
35. Harrison RA. Rapid PKA-catalysed phosphorylation of boar sperm proteins induced by the capacitating agent bicarbonate. Mol. Reprod. Dev. 67(3), 337-352 (2004).
36. Krapf D, Arcelay E, Wertheimer EV et al. Inhibition of Ser/Thr phosphatases induces capacitation-associated signaling in the presence of Src kinase inhibitors. J. Biol Chem. 285(11) 7977-7985 (2010)
37. Rotman T, Etkovitz N, Spiegel A, Rubinstein S, Breitbart H. Protein kinase A and protein kinase C(alpha)/PPP1CC2 play opposing roles in the regulation of phosphatidylinositol 3-kinase activation in bovine sperm. Reproduction 140(1), 43-56 (2010).
38. Morgan DJ, Weisenhaus M, Shum S et al. Tissue-specifc PKA inhibition using a chemical genetic approach and its application to studies on sperm capacitation. Proc Natl Acad. Sci USA 105(52), 20740-20745 (2008).
39. O'Brien ED, Krapf D, Cabada MO, Visconti PE, Arranz SE. Transmembrane adenylyl cyclase regulates amphibian sperm motility through protein kinase A activation. Dev. Biol. 350(1), 80-88 (2011).
40. Su YH, Chen SH, Zhou H, Vacquier VD. Tandem mass spectrometry identifes proteins phosphorylated by cyclic AMP-dependent protein kinase when sea urchin sperm undergo the acrosome reaction. Dev. Biol. 285(1), 116-125 (2005).
41. Jha KN, Salicioni AM, Arcelay E et al. Evidence for the involvement of proline-directed serine/threonine phosphorylation in sperm capacitation. Mol. Hum. Reprod. 12(12), 781-789 (2006).
42. Baker MA, Smith ND, Hetherington L et al. Label-free quantitation of phosphopeptide changes during rat sperm capacitation. J. Proteome Res. 9(2), 718-729 (2010).
43. Fischer E, Speier A. Darstellung der Ester. Berichte der deutschen chemischen Gesellschaft 28(3), 3252-3258 (1895).
44. Platt MD, Salicioni AM, Hunt DF, Visconti PE. Use of differential isotopic labeling and mass spectrometry to analyze capacitation-associated changes in the phosphorylation status of mouse sperm proteins. J. Proteome Res. 8(3), 1431-1440 (2009).
45. Baker MA, Smith ND, Hetherington L, Pelzing M, Condina MR, Aitken RJ. Use of titanium dioxide to fnd phosphopeptide and total protein changes during epididymal sperm maturation. J. Proteome Res. 10(3), 1004-1017 (2011).
46. Coon JJ. Collisions or electrons? Protein sequence analysis in the 21st century. Anal. Chem. 81(9), 3208-3215 (2009).
47. Li LW, Fan LQ, Zhu WB et al. Establishment of a high-resolution 2-D reference map of human spermatozoal proteins from 12 fertile sperm-bank donors. Asian J. Androl. 9(3), 321-329 (2007).
48. Hu Q, Noll RJ, Li H, Makarov A, Hardman M, Graham Cooks R. The Orbitrap: a new mass spectrometer. J. Mass Spectrom. 40(4), 430-443 (2005).
49. Hagel P, Gerding JJ, Fieggen W, Bloemendal H. Cyanate formation in solutions of urea. I. Calculation of cyanate concentrations at different temperature and pH. Biochim. Biophys. Acta 243(3), 366-373 (1971).
50. Gerding JJ, Koppers A, Hagel P, Bloemendal H. Cyanate formation in solutions of urea. II. Effect of urea on the eye lens protein-crystallin. Biochim. Biophys. Acta 243(3), 375-379 (1971).
51. Edman P, Begg G. A protein sequenator. Eur. J. Biochem. 1(1), 80-91 (1967).
52. Sleight SB, Miranda PV, Plaskett NW et al. Isolation and proteomic analysis of mouse sperm detergent-resistant membrane fractions: evidence for dissociation of lipid rafts during capacitation. Biol. Reprod. 73(4), 721-729 (2005).
53. Krisfalusi M, Miki K, Magyar PL, O'Brien DA. Multiple glycolytic enzymes are tightly bound to the fbrous sheath of mouse spermatozoa. Biol. Reprod. 75(2), 270-278 (2006).
54. Johnston DS, Wooters J, Kopf GS, Qiu Y, Roberts KP. Analysis of the human sperm proteome. Ann. NY Acad. Sci. 1061, 190-202 (2005).
55. Haglund H. Isoelectric focusing in pH gradients-a technique for fractionation and characterization of ampholytes. Methods Biochem. Anal. 19, 1-104 (1971).
56. Baker MA, Reeves G, Hetherington L, Aitken RJ. Analysis of proteomic changes associated with sperm capacitation through the combined use of IPG-strip pre-fractionation followed by RP chromatography LC-MS/MS analysis. Proteomics 10(3), 482-495 (2010).
57. O'Farrell PH. High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250(10), 4007-4021 (1975).
58. Baker MA, Witherdin R, Hetherington L, Cunningham-Smith K, Aitken RJ. Identifcation of post-translational modifcations that occur during sperm maturation using difference in two-dimensional gel electrophoresis. Proteomics 5(4), 1003-1012 (2005).
59. Wray W, Boulikas T, Wray VP, Hancock R. Silver staining of proteins in polyacrylamide gels. Anal. Biochem. 118(1), 197-203 (1981).
60. Fujinoki M, Kawamura T, Toda T et al. Identifcation of 36-kDa fagellar phosphoproteins associated with hamster sperm motility. J. Biochem. 133(3), 361-369 (2003).
61. Staudenmann W, Hatt PD, Hoving S, Lehmann A, Kertesz M, James P. Sample handling for proteome analysis. Electrophoresis 19 (6), 901-908 (1998).
62. Tabb DL, Smith LL, Breci LA, Wysocki VH, Lin D, Yates JR 3rd. Statistical characterization of ion trap tandem mass spectra from doubly charged tryptic peptides. Anal. Chem. 75 (5), 1155-1163 (2003).
63. McCormack AL, Somogyi A, Dongré AR, Wysocki VH. Fragmentation of protonated peptides: surface-induced dissociation in conjunction with a quantum mechanical approach. Anal. Chem. 65(20), 2859-2872 (1993).
64. Quach T T, Li N, Richards DP, Zheng J, Keller BO, Li L. Development and applications of in-gel CNBr/tryptic digestion combined with mass spectrometry for the analysis of membrane proteins. J. Proteome Res. 2(5), 543-552 (2003).
65. Porath J. Immobilized metal ion affnity chromatography. Protein Expr. Purif. 3(4), 263-281 (1992).
66. Posewitz MC, Tempst P. Immobilized gallium(III) affnity chromatography of phosphopeptides. Anal. Chem. 71(14), 2883-2892 (1999).
67. Annan RS, Huddleston MJ, Verma R, Deshaies RJ, Carr SA. A multidimensional electrospray MS-based approach to phosphopeptide mapping. Anal. Chem. 73(3), 393-404 (2001).
68. Cao P, Stults JT. Phosphopeptide analysis by on-line immobilized metal-ion affnity chromatography-capillary electrophoresis-electrospray ionization mass spectrometry. J. Chromatogr. A 853(1-2), 225-235 (1999).
69. Cao P, Stults JT. Mapping the phosphorylation sites of proteins using on-line immobilized metal affnity chromatography/capillary electrophoresis/ electrospray ionization multiple stage tandem mass spectrometry. Rapid Commun. Mass Spectrom. 14(17), 1600-1606 (2000).
70. Porath J, Carlsson J, Olsson I, Belfrage G. Metal chelate affnity chromatography, a new approach to protein fractionation. Nature 258(5536), 598-599 (1975).
71. Porath J, Olin B. Immobilized metal ion affnity adsorption and immobilized metal ion affnity chromatography of biomaterials. Serum protein affnities for gel-immobilized iron and nickel ions. Biochemistry 22(7), 1621-1630 (1983).
72. Muszynska G, Andersson L, Porath J. Selective adsorption of phosphoproteins on gel-immobilized ferric chelate. Biochemistry 25(22), 6850-6853 (1986).
73. Muszynska G, Dobrowolska G, Medin A, Ekman P, Porath JO. Model studies on iron(III) ion affnity chromatography. II. Interaction of immobilized iron(III) ions with phosphorylated amino acids, peptides and proteins. J. Chromatogr. 604(1), 19-28 (1992).
74. Ficarro SB, McCleland ML, Stukenberg PT et al. Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat. Biotechnol. 20(3), 301-305 (2002).
75. Larsen MR, Thingholm TE, Jensen ON, Roepstorff P, Jørgensen TJ. Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell Proteomics 4(7), 873-886 (2005).
76. Thingholm TE, Jensen ON, Robinson PJ, Larsen MR. SIMAC (sequential elution from IMAC), a phosphoproteomics strategy for the rapid separation of monophosphorylated from multiply phosphorylated peptides. Mol. Cell Proteomics 7(4), 661-671 (2008).
77. Marouga R, David S, Hawkins E. The development of the DIGE system:2D fuorescence difference gel analysis technology. Anal. Bioanal. Chem. 382(3), 669-678 (2005).
78. Gygi SP, Rist B, Gerber SA, Turecek F, Gelb MH, Aebersold R. Quantitative analysis of complex protein mixtures using isotope-coded affnity tags. Nat. Biotechnol. 17(10), 994-999 (1999).
79. Thompson A, Schäfer J, Kuhn K et al. Tandem mass tags: a novel quantifcation strategy for comparative analysis of complex protein mixtures by MS/MS. Anal. Chem. 75(8), 1895-1904 (2003).
80. Ross PL, Huang YN, Marchese JN et al. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell Proteomics 3 (12), 1154-1169 (2004).
81. Fujinoki M, Kawamura T, Toda T et al. Identifcation of 36 kDa phosphoprotein in fbrous sheath of hamster spermatozoa. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 137(4), 509-520 (2004).
82. Lalancette C, Faure RL, Leclerc P. Identifcation of the proteins present in the bull sperm cytosolic fraction enriched in tyrosine kinase activity: a proteomic approach. Proteomics 6 (16), 4523-4540 (2006).
83. Baker MA, Aitken RJ, Hetherington L. Identifcation of SRC as a key PKA-stimulated tyrosine kinase involved in the capacitation-associated hyperactivation of murine spermatozoa. J Cell Sci. 119 (15), 3182-3192 (2006).
84. Hillenkamp F, Karas M, Beavis RC, Chait BT. Matrix-assisted laser desorption/ionization mass spectrometry of biopolymers. Anal. Chem. 63(24), 1193A-1203A (1991).
85. Marshall AG, Hendrickson CL. Highresolution mass spectrometers. Annu. Rev. Anal. Chem. (Palo Alto. Calif.) 1, 579-599 (2008).
86. McLuckey S, Goeringer D. Slow heating methods in tandem mass spectrometry. J. Mass Spectrometry, 32(5), 461-474 (1997).
87. Zheng J, Li N, Ridyard M, Dai H, Robbins SM, Li L. Simple and robust two-layer matrix/sample preparation method for MALDI MS/MS analysis of peptides. J. Proteome Res. 4(5), 1709-1716 (2005).
88. Fenn JB, Mann M, Meng CK, Wong SF, Whitehouse CM. Electrospray ionization for mass spectrometry of large biomolecules. Science 246(4926), 64-71 (1989).
89. Emmett M, Caprioli R. Micro-electrospray mass-spectrometry-ultra-high- sensitivity analysis of peptides and proteins. J. Am. Soc. Mass Spectrom., 5(7), 605-613 (1994).
90. Baker MA, Hetherington L, Reeves GM, Aitken RJ. The mouse sperm proteome characterized via IPG strip prefractionation and LC-MS/MS identifcation. Proteomics 8(8), 1720-1730 (2008).
91. Baker MA, Hetherington L, Reeves G, Müller J, Aitken RJ. The rat sperm proteome characterized via IPG strip prefractionation and LC-MS/MS identifcation. Proteomics 8(11), 2312-2321 (2008).
92. Fujinoki M, Kawamura T, Toda T et al. Identifcation of the 58-kDa phosphoprotein associated with motility initiation of hamster spermatozoa. J. Biochem. 134(4), 559-565 (2003).
93. March R. An introduction to quadrupole ion trap mass spectrometry. J. Mass Spectrom. 32(4), 351-369 (1997).
94. Brancia FL. Recent developments in ion-trap mass spectrometry and related technologies. Expert Rev. Proteomics 3(1), 143-151 (2006).
95. Craig AG, Hoeger CA, Miller CL, Goedken T, Rivier JE, Fischer WH. Monitoring protein kinase and phosphatase reactions with matrix-assisted laser desorption/ionization mass spectrometry and capillary zone electrophoresis: comparison of the detection effciency of peptide-phosphopeptide mixtures. Biol. Mass Spectrom. 23(8), 519-528 (1994).
96. Yang X, Wu H, Kobayashi T, Solaro RJ, van Breemen RB. Enhanced ionization of phosphorylated peptides during MALDI TOF mass spectrometry. Anal. Chem. 76(5), 1532-1536 (2004).
97. Asara JM, Allison J. Enhanced detection of phosphopeptides in matrix-assisted laser desorption/ionization mass spectrometry using ammonium salts. J. Am. Soc. Mass Spectrom. 10(1), 35-44 (1999).
98. Stensballe A, Jensen ON. Phosphoric acid enhances the performance of Fe(III) affnity chromatography and matrix-assisted laser desorption/ionization tandem mass spectrometry for recovery, detection and sequencing of phosphopeptides. Rapid Commun. Mass Spectrom. 18(15), 1721-1730 (2004).
99. Schwartz JC, Senko MW, Syka JE. A two-dimensional quadrupole ion trap mass spectrometer. J. Am. Soc. Mass Spectrom. 13(6), 659-669 (2002).
100. DeGnore JP, Qin J. Fragmentation of phosphopeptides in an ion trap mass spectrometer. J. Am. Soc. Mass Spectrom. 9(11), 1175-1188 (1998).
101. Syka JE, Coon JJ, Schroeder MJ, Shabanowitz J, Hunt DF. Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc. Natl Acad. Sci. USA 101(26), 9528-9533 (2004).
102. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS. Prob ability-based protein identifcation by searching sequence databases using mass spectrometry data. Electrophoresis 20(18), 3551-3567 (1999).
103. Fardilha M, Esteves SL, Korrodi-Gregório L et al. Identifcation of the human testis protein phosphatase 1 interactome. Biochem. Pharmacol. 82(10), 1403-1415 (2011).
104. Pappin DJ, Hojrup P, Bleasby AJ. Rapid identifcation of proteins by peptide-mass fngerprinting. Curr. Biol. 3(6), 327-332 (1993).
105. Chamrad DC, Körting G, Stühler K, Meyer HE, Klose J, Blüggel M. Evaluation of algorithms for protein identifcation from sequence databases using mass spectrometry data. Proteomics 4(3), 619-628 (2004).
106. Johnson RS, Martin SA, Biemann K, Stults JT, Watson JT. Novel fragmentation process of peptides by collision-induced decomposition in a tandem mass spectrometer: differentiation of leucine and isoleucine. Anal. Chem. 59 (21), 2621-2625 (1987).
107. Cottrell JS, Creasy DM. Response to: the problem with peptide presumption and low Mascot scoring. J. Proteome Res. 10(11), 5272-5273 (2011).
108. Li YF, He W, Kim YH et al. CABYR isoforms expressed in late steps of sper m io genesis bind with AKAPs and ropporin in mouse sperm fbrous sheath. Reprod. Biol. Endocrinol. 8, 101 (2010).
109. Eng JK, McCormack AL, Yates Jr. An approach to correlate tandem mass-spectral data of peptides with ami no-acid-sequences in a protein database. J. Am. Soc. Mass Spectrom. 5(11), 976-989 (1994).
110. Biemann K. Contributions of mass spectrometry to peptide and protein structure. Biomed. Environ. Mass Spectrom. 16(1-12) 99-111 (1988).
111. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J. Mol. Biol. 215(3), 403-410 (1990).
112. Salicioni A, Platt M, Visconti P. A novel testis-specifc serine-proline rich protein is present in mammalian sperm and becomes phosphorylated during capacitation. Presented at: Society for the Study of Reproduction 41st Annual Meeting. Kailua-Kona, HI, USA, 27-30 May 2008.
113. Neilson KA, Ali NA, Muralidharan S et al. Less label, more free: approaches in label-free quantitative mass spectrometry. Proteomics 11 (4), 535-553 (2011).
114. Bland JM, Altman DG. Statistics notes. The odds ratio. BMJ 320(7247), 1468 (2000).
115. Swaney DL, McAlister GC, Coon JJ. Decision tree-driven tandem mass spectrometry for shotgun proteomics. Nat. Methods 5(11), 959-964 (2008).
116. Compton PD, Strukl JV, Bai DL, Shabanowitz J, Hunt DF. Optimization of electron transfer dissociation via informed selection of reagents and operating parameters. Anal. Chem. 84(3), 1781-1785 (2012).
117. Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10 (4), 1794-1805 (2011).