Circadian Clocks pp 389-407

Part of the Handbook of Experimental Pharmacology book series (HEP, volume 217)

| Cite as

Proteomic Approaches in Circadian Biology

Abstract

Circadian clocks are endogenous oscillators that drive the rhythmic expression of a broad array of genes that orchestrate metabolism and physiology. Recent evidence indicates that posttranscriptional and posttranslational mechanisms play essential roles in modulating circadian gene expression, particularly for the molecular mechanism of the clock. In contrast to genetic technologies that have long been used to study circadian biology, proteomic approaches have so far been limited and, if applied at all, have used two-dimensional gel electrophoresis (2-DE). Here, we review the proteomics approaches applied to date in the circadian field, and we also discuss the exciting potential of using cutting-edge proteomics technology in circadian biology. Large-scale, quantitative protein abundance measurements will help to understand to what extent the circadian clock drives system wide rhythms of protein abundance downstream of transcription regulation.

Keywords

Circadian rhythm Proteomics Mass spectrometry Protein quantification Posttranslation modifications 

Abbreviations

CE-MS

Capillarity electrophoresis mass spectrometry

GC-MS

Gas chromatography mass spectrometry

LC-FT MS/MS

Liquid chromatography Fourier transformation tandem mass spectrometry

MALDI TOF MS

Matrix-assisted laser desorption/ionization time of flying mass spectrometry

MS

Mass spectrometry

SELDI

Surface-enhanced laser desorption/ionization

SPE

Solid-phase extraction

References

  1. Aebersold R, Mann M (2003) Mass spectrometry-based proteomics. Nature 422:198–207PubMedCrossRefGoogle Scholar
  2. Akhtar RA, Reddy AB, Maywood ES, Clayton JD, King VM, Smith AG, Gant TW, Hastings MH, Kyriacou CP (2002) Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr Biol 12:540–550PubMedCrossRefGoogle Scholar
  3. Albrecht U, Zheng B, Larkin D, Sun ZS, Lee CC (2001) MPer1 and mper2 are essential for normal resetting of the circadian clock. J Biol Rhythms 16:100–104PubMedCrossRefGoogle Scholar
  4. Andersen JS, Matic I, Vertegaal AC (2009) Identification of SUMO target proteins by quantitative proteomics. Methods Mol Biol 497:19–31PubMedCrossRefGoogle Scholar
  5. Araki R, Nakahara M, Fukumura R, Takahashi H, Mori K, Umeda N, Sujino M, Inouye ST, Abe M (2006) Identification of genes that express in response to light exposure and express rhythmically in a circadian manner in the mouse suprachiasmatic nucleus. Brain Res 1098:9–18PubMedCrossRefGoogle Scholar
  6. Argenzio E, Bange T, Oldrini B, Bianchi F, Peesari R, Mari S, Di Fiore PP, Mann M, Polo S (2011) Proteomic snapshot of the EGF-induced ubiquitin network. Mol Syst Biol 7:462PubMedCrossRefGoogle Scholar
  7. Asher G, Gatfield D, Stratmann M, Reinke H, Dibner C, Kreppel F, Mostoslavsky R, Alt FW, Schibler U (2008) SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134:317–328PubMedCrossRefGoogle Scholar
  8. Baggs JE, Hogenesch JB (2010) Genomics and systems approaches in the mammalian circadian clock. Curr Opin Genet Dev 20:581–587PubMedCrossRefGoogle Scholar
  9. Baker CL, Kettenbach AN, Loros JJ, Gerber SA, Dunlap JC (2009) Quantitative proteomics reveals a dynamic interactome and phase-specific phosphorylation in the Neurospora circadian clock. Mol Cell 34:354–363PubMedCrossRefGoogle Scholar
  10. Bantscheff M, Schirle M, Sweetman G, Rick J, Kuster B (2007) Quantitative mass spectrometry in proteomics: a critical review. Anal Bioanal Chem 389:1017–1031PubMedCrossRefGoogle Scholar
  11. Barnard AR, Nolan PM (2008) When clocks go bad: neurobehavioural consequences of disrupted circadian timing. PLoS Genet 4:e1000040PubMedCrossRefGoogle Scholar
  12. Bass J, Takahashi JS (2010) Circadian integration of metabolism and energetics. Science 330:1349–1354PubMedCrossRefGoogle Scholar
  13. Beausoleil SA, Jedrychowski M, Schwartz D, Elias JE, Villen J, Li J, Cohn MA, Cantley LC, Gygi SP (2004) Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc Natl Acad Sci USA 101:12130–12135PubMedCrossRefGoogle Scholar
  14. Bodenmiller B, Mueller LN, Mueller M, Domon B, Aebersold R (2007) Reproducible isolation of distinct, overlapping segments of the phosphoproteome. Nat Methods 4:231–237PubMedCrossRefGoogle Scholar
  15. Brown SA, Azzi A (2013) Peripheral circadian oscillators in mammals. In: Kramer A, Merrow M (eds) Circadian clocks, vol 217, Handbook of experimental pharmacology. Springer, HeidelbergCrossRefGoogle Scholar
  16. Brown SA, Ripperger J, Kadener S, Fleury-Olela F, Vilbois F, Rosbash M, Schibler U (2005) PERIOD1-associated proteins modulate the negative limb of the mammalian circadian oscillator. Science 308:693–696PubMedCrossRefGoogle Scholar
  17. Buhr ED, Takahashi JS (2013) Molecular components of the mammalian circadian clock. In: Kramer A, Merrow M (eds) Circadian clocks, vol 217, Handbook of experimental pharmacology. Springer, HeidelbergCrossRefGoogle Scholar
  18. Cardone L, Hirayama J, Giordano F, Tamaru T, Palvimo JJ, Sassone-Corsi P (2005) Circadian clock control by SUMOylation of BMAL1. Science 309:1390–1394PubMedCrossRefGoogle Scholar
  19. Castel M, Belenky M, Cohen S, Wagner S, Schwartz WJ (1997) Light-induced c-Fos expression in the mouse suprachiasmatic nucleus: immunoelectron microscopy reveals co-localization in multiple cell types. Eur J Neurosci 9:1950–1960PubMedCrossRefGoogle Scholar
  20. Chiu JC, Vanselow JT, Kramer A, Edery I (2008) The phospho-occupancy of an atypical SLIMB-binding site on PERIOD that is phosphorylated by DOUBLETIME controls the pace of the clock. Genes Dev 22:1758–1772PubMedCrossRefGoogle Scholar
  21. Choudhary C, Mann M (2010) Decoding signalling networks by mass spectrometry-based proteomics. Nat Rev Mol Cell Biol 11:427–439PubMedCrossRefGoogle Scholar
  22. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325:834–840PubMedCrossRefGoogle Scholar
  23. Cox J, Mann M (2011) Quantitative, high-resolution proteomics for data-driven systems biology. Annu Rev Biochem 80:273–299PubMedCrossRefGoogle Scholar
  24. Dallmann R, Viola AU, Tarokh L, Cajochen C, Brown SA (2012) The human circadian metabolome. Proc Natl Acad Sci USA 109:2625–2629PubMedCrossRefGoogle Scholar
  25. Davidson AJ, Yamazaki S, Menaker M (2003) SNC: ringmaster of the circadian circus or conductor of the circadian orchestra? Novartis Found Symp 253:110–121PubMedCrossRefGoogle Scholar
  26. Deery MJ, Maywood ES, Chesham JE, Sladek M, Karp NA, Green EW, Charles PD, Reddy AB, Kyriacou CP, Lilley KS, Hastings MH (2009) Proteomic analysis reveals the role of synaptic vesicle cycling in sustaining the suprachiasmatic circadian clock. Curr Biol 19:2031–2036PubMedCrossRefGoogle Scholar
  27. Dephoure N, Zhou C, Villen J, Beausoleil SA, Bakalarski CE, Elledge SJ, Gygi SP (2008) A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci USA 105:10762–10767PubMedCrossRefGoogle Scholar
  28. Duffield GE (2003) DNA microarray analyses of circadian timing: the genomic basis of biological time. J Neuroendocrinol 15:991–1002PubMedCrossRefGoogle Scholar
  29. Duong HA, Robles MS, Knutti D, Weitz CJ (2011) A molecular mechanism for circadian clock negative feedback. Science 332:1436–1439PubMedCrossRefGoogle Scholar
  30. Eckel-Mahan KL, Patel VR, Mohney RP, Vignola KS, Baldi P, Sassone-Corsi P (2012) Coordination of the transcriptome and metabolome by the circadian clock. Proc Natl Acad Sci USA 109:5541–5546PubMedCrossRefGoogle Scholar
  31. Ficarro SB, McCleland ML, Stukenberg PT, Burke DJ, Ross MM, Shabanowitz J, Hunt DF, White FM (2002) Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat Biotechnol 20:301–305PubMedCrossRefGoogle Scholar
  32. Geiger T, Cox J, Ostasiewicz P, Wisniewski JR, Mann M (2010) Super-SILAC mix for quantitative proteomics of human tumor tissue. Nat Methods 7:383–385PubMedCrossRefGoogle Scholar
  33. Geiger T, Wisniewski JR, Cox J, Zanivan S, Kruger M, Ishihama Y, Mann M (2011) Use of stable isotope labeling by amino acids in cell culture as a spike-in standard in quantitative proteomics. Nat Protoc 6:147–157PubMedCrossRefGoogle Scholar
  34. Gingras AC, Gstaiger M, Raught B, Aebersold R (2007) Analysis of protein complexes using mass spectrometry. Nat Rev Mol Cell Biol 8:645–654PubMedCrossRefGoogle Scholar
  35. Goldman BD (2001) Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J Biol Rhythms 16:283–301PubMedCrossRefGoogle Scholar
  36. Graumann J, Hubner NC, Kim JB, Ko K, Moser M, Kumar C, Cox J, Scholer H, Mann M (2008) Stable isotope labeling by amino acids in cell culture (SILAC) and proteome quantitation of mouse embryonic stem cells to a depth of 5,111 proteins. Mol Cell Proteomics 7:672–683PubMedGoogle Scholar
  37. Hanash S (2003) Disease proteomics. Nature 422:226–232PubMedCrossRefGoogle Scholar
  38. Hatcher NG, Atkins N Jr, Annangudi SP, Forbes AJ, Kelleher NL, Gillette MU, Sweedler JV (2008) Mass spectrometry-based discovery of circadian peptides. Proc Natl Acad Sci USA 105:12527–12532PubMedCrossRefGoogle Scholar
  39. Huang W, Ramsey KM, Marcheva B, Bass J (2011) Circadian rhythms, sleep, and metabolism. J Clin Invest 121:2133–2141PubMedCrossRefGoogle Scholar
  40. Hubner NC, Bird AW, Cox J, Splettstoesser B, Bandilla P, Poser I, Hyman A, Mann M (2010) Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J Cell Biol 189:739–754PubMedCrossRefGoogle Scholar
  41. Hughes ME, DiTacchio L, Hayes KR, Vollmers C, Pulivarthy S, Baggs JE, Panda S, Hogenesch JB (2009) Harmonics of circadian gene transcription in mammals. PLoS Genet 5:e1000442PubMedCrossRefGoogle Scholar
  42. Johnson CH, Mori T, Xu Y (2008) A cyanobacterial circadian clockwork. Curr Biol 18:R816–R825PubMedCrossRefGoogle Scholar
  43. Kaji H, Kamiie J, Kawakami H, Kido K, Yamauchi Y, Shinkawa T, Taoka M, Takahashi N, Isobe T (2007) Proteomics reveals N-linked glycoprotein diversity in Caenorhabditis elegans and suggests an atypical translocation mechanism for integral membrane proteins. Mol Cell Proteomics 6:2100–2109PubMedCrossRefGoogle Scholar
  44. Kamphuis W, Cailotto C, Dijk F, Bergen A, Buijs RM (2005) Circadian expression of clock genes and clock-controlled genes in the rat retina. Biochem Biophys Res Commun 330:18–26PubMedCrossRefGoogle Scholar
  45. Kim SC, Sprung R, Chen Y, Xu Y, Ball H, Pei J, Cheng T, Kho Y, Xiao H, Xiao L, Grishin NV, White M, Yang XJ, Zhao Y (2006) Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol Cell 23:607–618PubMedCrossRefGoogle Scholar
  46. Kim W, Bennett EJ, Huttlin EL, Guo A, Li J, Possemato A, Sowa ME, Rad R, Rush J, Comb MJ, Harper JW, Gygi SP (2011) Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol Cell 44(2):325–340PubMedCrossRefGoogle Scholar
  47. Kivimae S, Saez L, Young MW (2008) Activating PER repressor through a DBT-directed phosphorylation switch. PLoS Biol 6:e183PubMedCrossRefGoogle Scholar
  48. Ko CH, Takahashi JS (2006) Molecular components of the mammalian circadian clock. Hum Mol Genet 15(Spec No 2):R271–R277Google Scholar
  49. Kruger M, Moser M, Ussar S, Thievessen I, Luber CA, Forner F, Schmidt S, Zanivan S, Fassler R, Mann M (2008) SILAC mouse for quantitative proteomics uncovers kindlin-3 as an essential factor for red blood cell function. Cell 134:353–364PubMedCrossRefGoogle Scholar
  50. Lee J, Lee Y, Lee MJ, Park E, Kang SH, Chung CH, Lee KH, Kim K (2008) Dual modification of BMAL1 by SUMO2/3 and ubiquitin promotes circadian activation of the CLOCK/BMAL1 complex. Mol Cell Biol 28:6056–6065PubMedCrossRefGoogle Scholar
  51. Lee JE, Atkins N Jr, Hatcher NG, Zamdborg L, Gillette MU, Sweedler JV, Kelleher NL (2010) Endogenous peptide discovery of the rat circadian clock: a focused study of the suprachiasmatic nucleus by ultrahigh performance tandem mass spectrometry. Mol Cell Proteomics 9:285–297PubMedCrossRefGoogle Scholar
  52. Lee HM, Chen R, Kim H, Etchegaray JP, Weaver DR, Lee C (2011) The period of the circadian oscillator is primarily determined by the balance between casein kinase 1 and protein phosphatase 1. Proc Natl Acad Sci USA 108:16451–16456PubMedCrossRefGoogle Scholar
  53. Mallick P, Kuster B (2010) Proteomics: a pragmatic perspective. Nat Biotechnol 28:695–709PubMedCrossRefGoogle Scholar
  54. Martino TA, Tata N, Bjarnason GA, Straume M, Sole MJ (2007) Diurnal protein expression in blood revealed by high throughput mass spectrometry proteomics and implications for translational medicine and body time of day. Am J Physiol Regul Integr Comp Physiol 293:R1430–R1437PubMedCrossRefGoogle Scholar
  55. McCarthy JJ, Andrews JL, McDearmon EL, Campbell KS, Barber BK, Miller BH, Walker JR, Hogenesch JB, Takahashi JS, Esser KA (2007) Identification of the circadian transcriptome in adult mouse skeletal muscle. Physiol Genomics 31:86–95PubMedCrossRefGoogle Scholar
  56. Mehra A, Baker CL, Loros JJ, Dunlap JC (2009) Post-translational modifications in circadian rhythms. Trends Biochem Sci 34:483–490PubMedCrossRefGoogle Scholar
  57. Minami Y, Kasukawa T, Kakazu Y, Iigo M, Sugimoto M, Ikeda S, Yasui A, van der Horst GT, Soga T, Ueda HR (2009) Measurement of internal body time by blood metabolomics. Proc Natl Acad Sci USA 106:9890–9895PubMedCrossRefGoogle Scholar
  58. Moller M, Sparre T, Bache N, Roepstorff P, Vorum H (2007) Proteomic analysis of day-night variations in protein levels in the rat pineal gland. Proteomics 7:2009–2018PubMedCrossRefGoogle Scholar
  59. Monetti M, Nagaraj N, Sharma K, Mann M (2011) Large-scale phosphosite quantification in tissues by a spike-in SILAC method. Nat Methods 8:655–658PubMedCrossRefGoogle Scholar
  60. Nakahata Y, Kaluzova M, Grimaldi B, Sahar S, Hirayama J, Chen D, Guarente LP, Sassone-Corsi P (2008) The NAD+−dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell 134:329–340PubMedCrossRefGoogle Scholar
  61. Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, Mortensen P, Mann M (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127:635–648PubMedCrossRefGoogle Scholar
  62. Olsen JV, Vermeulen M, Santamaria A, Kumar C, Miller ML, Jensen LJ, Gnad F, Cox J, Jensen TS, Nigg EA, Brunak S, Mann M (2010) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signal 3:ra3Google Scholar
  63. Ong SE, Mann M (2006) A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat Protoc 1:2650–2660PubMedCrossRefGoogle Scholar
  64. Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, Mann M (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1:376–386PubMedCrossRefGoogle Scholar
  65. Ong SE, Mittler G, Mann M (2004) Identifying and quantifying in vivo methylation sites by heavy methyl SILAC. Nat Methods 1:119–126PubMedCrossRefGoogle Scholar
  66. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, Hogenesch JB (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109:307–320PubMedCrossRefGoogle Scholar
  67. Patel VR, Eckel-Mahan K, Sassone-Corsi P, Baldi P (2012) CircadiOmics: integrating circadian genomics, transcriptomics, proteomics and metabolomics. Nat Methods 9:772–773PubMedCrossRefGoogle Scholar
  68. Porterfield VM, Piontkivska H, Mintz EM (2007) Identification of novel light-induced genes in the suprachiasmatic nucleus. BMC Neurosci 8:98PubMedCrossRefGoogle Scholar
  69. Reddy AB (2013) Genome-wide analyses of circadian systems. In: Kramer A, Merrow M (eds) Circadian clocks, vol 217, Handbook of experimental pharmacology. Springer, HeidelbergCrossRefGoogle Scholar
  70. Reddy AB, Karp NA, Maywood ES, Sage EA, Deery M, O’Neill JS, Wong GK, Chesham J, Odell M, Lilley KS, Kyriacou CP, Hastings MH (2006) Circadian orchestration of the hepatic proteome. Curr Biol 16:1107–1115PubMedCrossRefGoogle Scholar
  71. Reischl S, Kramer A (2011) Kinases and phosphatases in the mammalian circadian clock. FEBS Lett 585:1393–1399PubMedCrossRefGoogle Scholar
  72. Robles MS, Boyault C, Knutti D, Padmanabhan K, Weitz CJ (2010) Identification of RACK1 and protein kinase Calpha as integral components of the mammalian circadian clock. Science 327:463–466PubMedCrossRefGoogle Scholar
  73. Sahar S, Zocchi L, Kinoshita C, Borrelli E, Sassone-Corsi P (2010) Regulation of BMAL1 protein stability and circadian function by GSK3beta-mediated phosphorylation. PLoS One 5:e8561PubMedCrossRefGoogle Scholar
  74. Sardiu ME, Washburn MP (2011) Building protein-protein interaction networks with proteomics and informatics tools. J Biol Chem 286:23645–23651PubMedCrossRefGoogle Scholar
  75. Schwanhausser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M (2011) Global quantification of mammalian gene expression control. Nature 473:337–342PubMedCrossRefGoogle Scholar
  76. Sewlall S, Pillay V, Danckwerts MP, Choonara YE, Ndesendo VM, du Toit LC (2010) A timely review of state-of-the-art chronopharmaceuticals synchronized with biological rhythms. Curr Drug Deliv 7:370–388PubMedCrossRefGoogle Scholar
  77. Storch KF, Lipan O, Leykin I, Viswanathan N, Davis FC, Wong WH, Weitz CJ (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417:78–83PubMedCrossRefGoogle Scholar
  78. Storch KF, Paz C, Signorovitch J, Raviola E, Pawlyk B, Li T, Weitz CJ (2007) Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell 130:730–741PubMedCrossRefGoogle Scholar
  79. Stratmann M, Schibler U (2006) Properties, entrainment, and physiological functions of mammalian peripheral oscillators. J Biol Rhythms 21:494–506PubMedCrossRefGoogle Scholar
  80. Takahashi JS, Hong HK, Ko CH, McDearmon EL (2008) The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat Rev Genet 9:764–775PubMedCrossRefGoogle Scholar
  81. Tatham MH, Matic I, Mann M, Hay RT (2011) Comparative proteomic analysis identifies a role for SUMO in protein quality control. Sci Signal 4:rs4Google Scholar
  82. ten Have S, Boulon S, Ahmad Y, Lamond AI (2011) Mass spectrometry-based immuno-precipitation proteomics - the user’s guide. Proteomics 11:1153–1159PubMedCrossRefGoogle Scholar
  83. Tian R, Alvarez-Saavedra M, Cheng HY, Figeys D (2011) Uncovering the proteome response of the master circadian clock to light using an AutoProteome system. Mol Cell Proteomics 10(M110):007252PubMedGoogle Scholar
  84. Tosini G, Menaker M (1996) Circadian rhythms in cultured mammalian retina. Science 272:419–421PubMedCrossRefGoogle Scholar
  85. Tsuji T, Hirota T, Takemori N, Komori N, Yoshitane H, Fukuda M, Matsumoto H, Fukada Y (2007) Circadian proteomics of the mouse retina. Proteomics 7:3500–3508PubMedCrossRefGoogle Scholar
  86. Ueda HR, Chen W, Adachi A, Wakamatsu H, Hayashi S, Takasugi T, Nagano M, Nakahama K, Suzuki Y, Sugano S, Iino M, Shigeyoshi Y, Hashimoto S (2002) A transcription factor response element for gene expression during circadian night. Nature 418:534–539PubMedCrossRefGoogle Scholar
  87. Vanselow K, Kramer A (2007) Role of phosphorylation in the mammalian circadian clock. Cold Spring Harb Symp Quant Biol 72:167–176PubMedCrossRefGoogle Scholar
  88. Vanselow K, Vanselow JT, Westermark PO, Reischl S, Maier B, Korte T, Herrmann A, Herzel H, Schlosser A, Kramer A (2006) Differential effects of PER2 phosphorylation: molecular basis for the human familial advanced sleep phase syndrome (FASPS). Genes Dev 20:2660–2672PubMedCrossRefGoogle Scholar
  89. Vermeulen M, Hubner NC, Mann M (2008) High confidence determination of specific protein-protein interactions using quantitative mass spectrometry. Curr Opin Biotechnol 19:331–337PubMedCrossRefGoogle Scholar
  90. Wagner SA, Beli P, Weinert BT, Nielsen ML, Cox J, Mann M, Choudhary C (2011) A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol Cell Proteomics 10(M111):013284PubMedGoogle Scholar
  91. Walther DM, Mann M (2011) Accurate quantification of more than 4000 mouse tissue proteins reveals minimal proteome changes during aging. Mol Cell Proteomics 10(M110):004523PubMedGoogle Scholar
  92. Weaver DR (1998) The suprachiasmatic nucleus: a 25-year retrospective. J Biol Rhythms 13:100–112PubMedCrossRefGoogle Scholar
  93. Wepf A, Glatter T, Schmidt A, Aebersold R, Gstaiger M (2009) Quantitative interaction proteomics using mass spectrometry. Nat Methods 6:203–205PubMedCrossRefGoogle Scholar
  94. Yates JR 3rd, Gilchrist A, Howell KE, Bergeron JJ (2005) Proteomics of organelles and large cellular structures. Nat Rev Mol Cell Biol 6:702–714PubMedCrossRefGoogle Scholar
  95. Zielinska DF, Gnad F, Wisniewski JR, Mann M (2010) Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 141:897–907PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Proteomics and Signal TransductionMax-Planck Institute of BiochemistryMartinsriedGermany

Personalised recommendations