Quantitative peptidomics for discovery of circadian-related peptides from the rat suprachiasmatic nucleus

Journal of Proteome Research

Volumn 12, Issue 2, 2013, Pages 585-593

  Lee, Ji Eun ^a,d   Zamdborg, Leonid ^a   Southey, Bruce R ^a   Atkins, Norman ^a   Mitchell, Jennifer W ^b   Li, Mingxi ^c   Gillette, Martha U ^a,b   Kelleher, Neil L ^c   Sweedler, Jonathan V ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d Korea Institute of Science and Technology   (South Korea)

Author keywords

circadian rhythms; endogenous peptides; label free quantification; neuropeptides; quantitative peptidomic analysis; suprachiasmatic nucleus (SCN)

Indexed keywords

COCAINE AND AMPHETAMINE REGULATED TRANSCRIPT PEPTIDE; GLUCOSE REGULATED PROTEIN; HORMONE PRECURSOR; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; NEUROPEPTIDE; PROENKEPHALIN; PROENKEPHALIN A; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; FOURIER TRANSFORM MASS SPECTROMETRY; MASS SPECTROMETER; NONHUMAN; PEPTIDOMICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SUPRACHIASMATIC NUCLEUS;

EID: 84873368613     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300605p     Document Type: Article

References (70)

1. Huang, W.; Ramsey, K. M.; Marcheva, B.; Bass, J. Circadian rhythms, sleep, and metabolism J. Clin. Invest. 2011, 121, 2133-2141
2. Reppert, S. M.; Weaver, D. R. Coordination of circadian timing in mammals Nature 2002, 418, 935-941
3. Yamaguchi, S.; Isejima, H.; Matsuo, T.; Okura, R.; Yagita, K.; Kobayashi, M.; Okamura, H. Synchronization of cellular clocks in the suprachiasmatic nucleus Science 2003, 302, 1408-1412
4. Abrahamson, E. E.; Moore, R. Y. Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections Brain Res. 2001, 916, 172-191
5. Mitchell, J. W.; Atkins, N., Jr.; Sweedler, J. V.; Gillette, M. U. Direct cellular peptidomics of hypothalamic neurons Front. Neuroendocrinol. 2011, 32, 377-386
6. Irwin, R. P.; Allen, C. N. Neuropeptide-mediated calcium signaling in the suprachiasmatic nucleus network Eur. J. Neurosci. 2010, 32, 1497-1506
7. Dardente, H.; Menet, J. S.; Challet, E.; Tournier, B. B.; Pevet, P.; Masson-Pevet, M. Daily and circadian expression of neuropeptides in the suprachiasmatic nuclei of nocturnal and diurnal rodents Brain Res. Mol. Brain Res. 2004, 124, 143-151
8. Awawdeh, L.; Lundy, F. T.; Shaw, C.; Lamey, P. J.; Linden, G. J.; Kennedy, J. G. Quantitative analysis of substance P, neurokinin A and calcitonin gene-related peptide in pulp tissue from painful and healthy human teeth Int. Endod. J. 2002, 35, 30-36
9. Chakraborty, T. R.; Tkalych, O.; Nanno, D.; Garcia, A. L.; Devi, L. A.; Salton, S. R. J. Quantification of VGF- and pro-SAAS-derived peptides in endocrine tissues and the brain, and their regulation by diet and cold stress Brain Res. 2006, 1089, 21-32
10. Wang, X. C.; Burbach, J. P.; Tenhaaf, J.; de Wied, D. Characterization and quantitation of vasopressin metabolites in the rat brain by specific radioimmunoassay and high-pressure liquid chromatography Sci. Sin. B 1986, 29, 832-843
11. Li, L.; Sweedler, J. V. Peptides in the brain: mass spectrometry-based measurement approaches and challenges Annu. Rev. Anal Chem. 2008, 1, 451-483
12. Fricker, L. D.; Lim, J.; Pan, H.; Che, F. Y. Peptidomics: identification and quantification of endogenous peptides in neuroendocrine tissues Mass Spectrom. Rev. 2006, 25, 327-344
13. Falth, M.; Skold, K.; Svensson, M.; Nilsson, A.; Fenyo, D.; Andren, P. E. Neuropeptidomics strategies for specific and sensitive identification of endogenous peptides Mol. Cell. Proteomics 2007, 6, 1188-1197
14. Svensson, M.; Skold, K.; Svenningsson, P.; Andren, P. E. Peptidomics-based discovery of novel neuropeptides J. Proteome Res. 2003, 2, 213-219
15. Lee, J. E.; Atkins, N., Jr.; Hatcher, N. G.; Zamdborg, L.; Gillette, M. U.; Sweedler, J. V.; Kelleher, N. L. Endogenous peptide discovery of the rat circadian clock: a focused study of the suprachiasmatic nucleus by ultrahigh performance tandem mass spectrometry Mol. Cell. Proteomics 2010, 9, 285-297
16. Rossbach, U.; Nilsson, A.; Falth, M.; Kultima, K.; Zhou, Q.; Hallberg, M.; Gordh, T.; Andren, P. E.; Nyberg, F. A quantitative peptidomic analysis of peptides related to the endogenous opioid and tachykinin systems in nucleus accumbens of rats following naloxone-precipitated morphine withdrawal J. Proteome Res. 2009, 8, 1091-1098
17. Kultima, K.; Nilsson, A.; Scholz, B.; Rossbach, U. L.; Falth, M.; Andren, P. E. Development and evaluation of normalization methods for label-free relative quantification of endogenous peptides Mol. Cell. Proteomics 2009, 8, 2285-2295
18. Morano, C.; Zhang, X.; Fricker, L. D. Multiple isotopic labels for quantitative mass spectrometry Anal. Chem. 2008, 80, 9298-9309
19. Scholz, B.; Alm, H.; Mattsson, A.; Nilsson, A.; Kultima, K.; Savitski, M. M.; Falth, M.; Skold, K.; Brunstrom, B.; Andren, P. E.; Dencker, L. Neuropeptidomic analysis of the embryonic Japanese quail diencephalon BMC Dev. Biol. 2010, 10, 30
20. Che, F. Y.; Fricker, L. D. Quantitative peptidomics of mouse pituitary: comparison of different stable isotopic tags J. Mass Spectrom. 2005, 40, 238-249
21. Brockmann, A.; Annangudi, S. P.; Richmond, T. A.; Ament, S. A.; Xie, F.; Southey, B. R.; Rodriguez-Zas, S. R.; Robinson, G. E.; Sweedler, J. V. Quantitative peptidomics reveal brain peptide signatures of behavior Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 2383-2388
22. Fredolini, C.; Meani, F.; Luchini, A.; Zhou, W. D.; Russo, P.; Ross, M.; Patanarut, A.; Tamburro, D.; Gambara, G.; Ornstein, D.; Odicino, F.; Ragnoli, M.; Ravaggi, A.; Novelli, F.; Collura, D.; D'Urso, L.; Muto, G.; Belluco, C.; Pecorelli, S.; Liotta, L.; Petricoin, E. F. Investigation of the ovarian and prostate cancer peptidome for candidate early detection markers using a novel nanoparticle biomarker capture technology AAPS J. 2010, 12, 504-518
23. Tinoco, A. D.; Tagore, D. M.; Saghatelian, A. Expanding the dipeptidyl peptidase 4-regulated peptidome via an optimized peptidomics platform J. Am. Chem. Soc. 2010, 132, 3819-3830
24. Bernay, B.; Gaillard, M. C.; Guryca, V.; Emadali, A.; Kuhn, L.; Bertrand, A.; Detraz, I.; Carcenac, C.; Savasta, M.; Brouillet, E.; Garin, J.; Elalouf, J. M. Discovering new bioactive neuropeptides in the striatum secretome using in vivo microdialysis and versatile proteomics Mol. Cell. Proteomics 2009, 8, 946-958
25. Liu, H.; Sadygov, R. G.; Yates, J. R., 3rd A model for random sampling and estimation of relative protein abundance in shotgun proteomics Anal. Chem. 2004, 76, 4193-4201
26. Tian, R.; Alvarez-Saavedra, M.; Cheng, H. Y.; Figeys, D. Uncovering the proteome response of the master circadian clock to light using an autoproteome system Mol. Cell. Proteomics 2011, 10, M110 007252
27. Kessner, D.; Chambers, M.; Burke, R.; Agus, D.; Mallick, P. ProteoWizard: open source software for rapid proteomics tools development Bioinformatics 2008, 24, 2534-2536
28. Geer, L. Y.; Markey, S. P.; Kowalak, J. A.; Wagner, L.; Xu, M.; Maynard, D. M.; Yang, X.; Shi, W.; Bryant, S. H. Open mass spectrometry search algorithm J. Proteome Res. 2004, 3, 958-964
29. Consortium, T. U. Reorganizing the protein space at the Universal Protein Resource (UniProt) Nucleic Acids Res. 2012, 40, D71-D75
30. Elias, J. E.; Gygi, S. P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry Nat. Methods 2007, 4, 207-214
31. R Foundation for Statistical Computing R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2011.
32. Athanas, M. Peptide and Protein Aggregated Measurements in SIEVE; VAST Scientific, Inc: Cambridge, MA, 2009.
33. Benjamini, Y.; Hochberg, Y. Controlling the false discovery rate-a practical and powerful approach to multiple testing J. R. Stat. Soc., Ser. B 1995, 57, 289-300
34. Fricker, L. D. Analysis of mouse brain peptides using mass spectrometry-based peptidomics: implications for novel functions ranging from non-classical neuropeptides to microproteins Mol. BioSyst. 2010, 6, 1355-1365
35. Fricker, L. D.; Sweedler, J. V. Fishing for the hidden peptidome in health and disease (drug abuse) AAPS J. 2010, 12, 679-682
36. Gelman, J. S.; Fricker, L. D. Hemopressin and other bioactive peptides from cytosolic proteins: are these non-classical neuropeptides? AAPS J. 2010, 12, 279-289
37. Heimann, A. S.; Gomes, I.; Dale, C. S.; Pagano, R. L.; Gupta, A.; de Souza, L. L.; Luchessi, A. D.; Castro, L. M.; Giorgi, R.; Rioli, V.; Ferro, E. S.; Devi, L. A. Hemopressin is an inverse agonist of CB1 cannabinoid receptors Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 20588-20593
38. Gomes, I.; Dale, C. S.; Casten, K.; Geigner, M. A.; Gozzo, F. C.; Ferro, E. S.; Heimann, A. S.; Devi, L. A. Hemoglobin-derived peptides as novel type of bioactive signaling molecules AAPS J. 2010, 12, 658-669
39. Van den Pol, A. N.; Decavel, C.; Levi, A.; Paterson, B. Hypothalamic expression of a novel gene-product, VGF-immunocytochemical analysis J. Neurosci. 1989, 9, 4122-4137
40. Fukuhara, C.; Suzuki, N.; Matsumoto, Y.; Nakayama, Y.; Aoki, K.; Tsujimoto, G.; Inouye, S. I.; Masuo, Y. Day-night variation of pituitary adenylate cyclase-activating polypeptide (PACAP) level in the rat suprachiasmatic nucleus Neurosci. Lett. 1997, 229, 49-52
41. Isobe, Y.; Muramatsu, K. Day-night differences in the contents of vasoactive intestinal peptide, gastrin-releasing peptide and Arg-vasopressin in the suprachiasmatic nucleus of rat pups during postnatal development Neurosci. Lett. 1995, 188, 45-48
42. Shinohara, K.; Tominaga, K.; Isobe, Y.; Inouye, S. T. Photic regulation of peptides located in the ventrolateral subdivision of the suprachiasmatic nucleus of the rat: daily variations of vasoactive intestinal polypeptide, gastrin-releasing peptide, and neuropeptide Y J. Neurosci. 1993, 13, 793-800
43. Tang, K.; Page, J. S.; Smith, R. D. Charge competition and the linear dynamic range of detection in electrospray ionization mass spectrometry J. Am. Soc. Mass Spectrom. 2004, 15, 1416-1423
44. Xie, F.; Liu, T.; Qian, W. J.; Petyuk, V. A.; Smith, R. D. Liquid chromatography-mass spectrometry-based quantitative proteomics J. Biol. Chem. 2011, 286, 25443-25449
45. Cutillas, P. R. Quantification of polypeptides by mass spectrometry. In Peptidomics: Methods and Applications; Soloviev, M.; Shaw, C.; Andrén, P., Eds.; John Wiley & Sons, Inc.: Hoboken, NJ, 2007; pp 291-316.
46. Kim, D. Y.; Kang, H. C.; Shin, H. C.; Lee, K. J.; Yoon, Y. W.; Han, H. C.; Na, H. S.; Hong, S. K.; Kim, Y. I. Substance P plays a critical role in photic resetting of the circadian pacemaker in the rat hypothalamus J. Neurosci. 2001, 21, 4026-4031
47. Shibata, S.; Tsuneyoshi, A.; Hamada, T.; Tominaga, K.; Watanabe, S. Effect of substance P on circadian rhythms of firing activity and the 2-deoxyglucose uptake in the rat suprachiasmatic nucleus in vitro Brain Res. 1992, 597, 257-263
48. Gamble, K. L.; Allen, G. C.; Zhou, T.; McMahon, D. G. Gastrin-releasing peptide mediates light-like resetting of the suprachiasmatic nucleus circadian pacemaker through cAMP response element-binding protein and Per1 activation J. Neurosci. 2007, 27, 12078-12087
49. McArthur, A. J.; Coogan, A. N.; Ajpru, S.; Sugden, D.; Biello, S. M.; Piggins, H. D. Gastrin-releasing peptide phase-shifts suprachiasmatic nuclei neuronal rhythms in vitro J. Neurosci. 2000, 20, 5496-5502
50. Piggins, H. D.; Cutler, D. J. The roles of vasoactive intestinal polypeptide in the mammalian circadian clock J. Endocrinol. 2003, 177, 7-15
51. Hannibal, J.; Fahrenkrug, J. Circadian rhythm regulation: a central role for the neuropeptide vasoactive intestinal polypeptide Am. J. Physiol.: Regul., Integr. Comp. Physiol. 2003, 285, R935-936
52. Reed, H. E.; Meyer-Spasche, A.; Cutler, D. J.; Coen, C. W.; Piggins, H. D. Vasoactive intestinal polypeptide (VIP) phase-shifts the rat suprachiasmatic nucleus clock in vitro Eur. J. Neurosci. 2001, 13, 839-843
53. Amare, A.; Hummon, A. B.; Southey, B. R.; Zimmerman, T. A.; Rodriguez-Zas, S. L.; Sweedler, J. V. Bridging neuropeptidomics and genomics with bioinformatics: Prediction of mammalian neuropeptide prohormone processing J. Proteome Res. 2006, 5, 1162-1167
54. Tegge, A. N.; Southey, B. R.; Sweedler, J. V.; Rodriguez-Zas, S. L. Comparative analysis of neuropeptide cleavage sites in human, mouse, rat, and cattle Mamm. Genome 2008, 19, 106-120
55. Xie, F.; London, S. E.; Southey, B. R.; Annangudi, S. P.; Amare, A.; Rodriguez-Zas, S. L.; Clayton, D. F.; Sweedler, J. V. The zebra finch neuropeptidome: prediction, detection and expression BMC Biol. 2010, 8, 28
56. Chen, D.; Buchanan, G. F.; Ding, J. M.; Hannibal, J.; Gillette, M. U. Pituitary adenylyl cyclase-activating peptide: a pivotal modulator of glutamatergic regulation of the suprachiasmatic circadian clock Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 13468-13473
57. Hannibal, J.; Ding, J. M.; Chen, D.; Fahrenkrug, J.; Larsen, P. J.; Gillette, M. U.; Mikkelsen, J. D. Pituitary adenylate cyclase activating peptide (PACAP) in the retinohypothalamic tract: a daytime regulator of the biological clock Ann. N.Y. Acad. Sci. 1998, 865, 197-206
58. Kopp, M. D.; Meissl, H.; Dehghani, F.; Korf, H. W. The pituitary adenylate cyclase-activating polypeptide modulates glutamatergic calcium signalling: investigations on rat suprachiasmatic nucleus neurons J. Neurochem. 2001, 79, 161-171
59. Colwell, C. S.; Michel, S.; Itri, J.; Rodriguez, W.; Tam, J.; Lelievre, V.; Hu, Z.; Waschek, J. A. Selective deficits in the circadian light response in mice lacking PACAP Am. J. Physiol.: Regul., Integr. Comp. Physiol. 2004, 287, R1194-1201
60. Beaule, C.; Mitchell, J. W.; Lindberg, P. T.; Damadzic, R.; Eiden, L. E.; Gillette, M. U. Temporally restricted role of retinal PACAP: integration of the phase-advancing light signal to the SCN J. Biol. Rhythms 2009, 24, 126-134
61. Belvin, M. P.; Zhou, H.; Yin, J. C. The Drosophila dCREB2 gene affects the circadian clock Neuron 1999, 22, 777-787
62. Hatcher, N. G.; Atkins, N., Jr.; Annangudi, S. P.; Forbes, A. J.; Kelleher, N. L.; Gillette, M. U.; Sweedler, J. V. Mass spectrometry-based discovery of circadian peptides Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 12527-12532
63. Vicentic, A.; Jones, D. C. The CART (cocaine- and amphetamine-regulated transcript) system in appetite and drug addiction J. Pharmacol. Exp. Ther. 2007, 320, 499-506
64. Vicentic, A.; Lakatos, A.; Hunter, R.; Philpot, K.; Dominguez, G.; Kuhar, M. J. CART peptide diurnal rhythm in brain and effect of fasting Brain Res. 2005, 1032, 111-115
65. Fliers, E.; Wiersinga, W. M.; Swaab, D. F. Physiological and pathophysiological aspects of thyrotropin-releasing hormone gene expression in the human hypothalamus Thyroid 1998, 8, 921-928
66. Jordan, D.; Veisseire, M.; Borsonchazot, F.; Mornex, R. Postnatal-development of TRH and TSH rhythms in the rat Hormone Res. 1987, 27, 216-224
67. Hong, H. K.; Chong, J. L.; Song, W.; Song, E. J.; Jyawook, A. A.; Schook, A. C.; Ko, C. H.; Takahashi, J. S. Inducible and reversible Clock gene expression in brain using the tTA system for the study of circadian behavior PLoS Genet. 2007, 3, e33
68. Isobe, Y.; Hida, H.; Nishino, H. Circadian rhythm of metabolic oscillation in suprachiasmatic nucleus depends on the mitochondrial oxidation state, reflected by cytochrome C oxidase and lactate dehydrogenase J. Neurosci. Res. 2011, 89, 929-935
69. Lopez, L.; Lorente, L.; Arias, J.; Gonzalez-Pardo, H.; Cimadevilla, J.; Arias, J. L. Changes of cytochrome oxidase activity in rat suprachiasmatic nucleus Brain Res. 1997, 769, 367-371
70. Ximenes da Silva, A.; Gendrot, G.; Serviere, J.; Lavialle, M. Daily changes of cytochrome oxidase activity within the suprachiasmatic nucleus of the Syrian hamster Neurosci. Lett. 2000, 286, 139-143