Peptidomic analyses of mouse astrocytic cell lines and rat primary cultured astrocytes

Journal of Proteome Research

Volumn 11, Issue 8, 2012, Pages 3965-3973

  Yin, Ping ^a   Knolhoff, Ann M ^a   Rosenberg, Harry J ^b   Millet, Larry J ^b   Gillette, Martha U ^a,b   Sweedler, Jonathan V ^a,b  

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

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

Author keywords

astrocytes; Ca 2+ dependent stimulation; CE MS; glia; LC MS; peptidomics; secreted peptides

Indexed keywords

CALCIUM; ELONGATION FACTOR 1; GALECTIN 1; MACROPHAGE MIGRATION INHIBITION FACTOR; PEROXIREDOXIN 5;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN TISSUE; CELL CULTURE; CELL LINE; CELL STIMULATION; CONTROLLED STUDY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOUSE; NONHUMAN; PEPTIDOMICS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; RAT;

AMINO ACID SEQUENCE; ANIMALS; ASTROCYTES; BRADYKININ; CALCIUM IONOPHORES; CALCIUM SIGNALING; CELL LINE; IONOMYCIN; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; NEUROPEPTIDES; POTASSIUM CHLORIDE; PRIMARY CELL CULTURE; PROTEOME; PROTEOMICS; RATS; RATS, LONG-EVANS; SEROTONIN;

RATTUS;

EID: 84864634069     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr201066t     Document Type: Article

References (68)

1. Strand, F. L. Neuropeptides: general characteristics and neuropharmaceutical potential in treating CNS disorders Prog. Drug Res. 2003, 61, 1-37 (Pubitemid 37187401)
2. Miller, G. Neuroscience: the dark side of glia Science 2005, 308 (5723) 778-781
3. Volterra, A.; Meldolesi, J. Astrocytes, from brain glue to communication elements: the revolution continues Nat. Rev. Neurosci. 2005, 6, 626-640 (Pubitemid 41059337)
4. Haydon, P. G.; Carmignoto, G. Astrocyte control of synaptic transmission and neurovascular coupling Physiol. Rev. 2006, 86 (3) 1009-1031 (Pubitemid 44033387)
5. Charles, A. C.; Merrill, J. E.; Dirksen, E. R.; Sandersont, M. J. Intercellular signaling in glial cells: Calcium waves and oscillations in response to mechanical stimulation and glutamate Neuron 1991, 6 (6) 983-992
6. Hassinger, T. D.; Guthrie, P. B.; Atkinson, P. B.; Bennett, M. V. L; Kater, S. B. An extracellular signaling component in propagation of astrocytic calcium waves Proc. Natl. Acad. Sci. U.S.A. 1996, 93 (23) 13268-13273 (Pubitemid 26382805)
7. Halassaa, M. M.; Fellina, T.; Haydon, P. G. The tripartite synapse: roles for gliotransmission in health and disease Trends Mol. Med. 2007, 13 (2) 54-63 (Pubitemid 46186152)
8. Perea, G.; Navarrete, M.; Araque, A. Tripartite synapses: astrocytes process and control synaptic information Trends Neurosci. 2009, 32 (8) 421-431
9. Yang, J.-W.; Suder, P.; Silberring, J.; Lubec, G. Proteome analysis of mouse primary astrocytes Neurochem. Int. 2005, 47 (3) 159-172 (Pubitemid 40848678)
10. Yang, J.-W.; Rodrigo, R.; Felipo, V.; Lubec, G. Proteome analysis of primary neurons and astrocytes from rat cerebellum J. Proteome Res. 2005, 4 (3) 768-788 (Pubitemid 40863266)
11. Verkhratsky, A.; Steinhäuser, C. Ion channels in glial cells Brain Res. Rev. 2000, 32, 380-412 (Pubitemid 30171314)
12. Kimelberg, H. K.; MacVicar, B. A.; Sontheimer, H. Anion channels in astrocytes: biophysics, pharmacology, and function Glia 2006, 54 (7) 747-757 (Pubitemid 44629637)
13. Shibeshih Belachew, V. G. Synaptic and extrasynaptic neurotransmitter receptors in glial precursors' quest for identity Glia 2004, 48 (3) 185-196
14. Bezzi, P.; Gundersen, V.; Galbete, J. L.; Seifert, G.; Steinhäuser, C.; Pilati, E.; Volterra, A. Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate Nat. Neurosci. 2004, 7, 613-620 (Pubitemid 38691900)
15. Coco, S.; Calegari, F.; Pravettoni, E.; Pozzi, D.; Taverna, E.; Rosa, P.; Matteoli, M.; Verderio, C. Storage and release of ATP from astrocytes in culture J. Biol. Chem. 2003, 278 (2) 1354-1362 (Pubitemid 36790821)
16. Martineau, M.; Baux, G.; Mothet, J.-P. D-Serine signalling in the brain: friend and foe Trends Neurosci. 2006, 29 (8) 481-491 (Pubitemid 44118443)
17. Jourdain, P.; Bergersen, L. H.; Bhaukaurally, K.; Bezzi, P.; Santello, M.; Domercq, M.; Matute, C.; Tonello, F.; Gundersen, V.; Volterra, A. Glutamate exocytosis from astrocytes controls synaptic strength Nat. Neurosci. 2007, 10 (3) 331-339
18. Dowell, J. A.; Johnson, J. A.; Li, L. Identification of astrocyte secreted proteins with a combination of shotgun proteomics and bioinformatics J. Proteome Res. 2009, 8 (8) 4135-4143
19. Greco, T. M.; Seeholzer, S. H.; Mak, A.; Spruce, L.; Ischiropoulos, H. Quantitative mass spectrometry-based proteomics reveals the dynamic range of primary mouse astrocyte protein secretion J. Proteome Res. 2010, 9 (5) 2764-2774
20. Lafon-Cazal, M.; Adjali, O.; Galéotti, N.; Poncet, J.; Jouin, P.; Homburger, V.; Bockaert, J.; Marin, P. Proteomic analysis of astrocytic secretion in the mouse J. Biol. Chem. 2003, 278 (27) 24438-24448
21. Calegari, F.; Coco, S.; Taverna, E.; Bassetti, M.; Verderio, C.; Corradi, N.; Matteoli, M.; Rosa, P. A regulated secretory pathway in cultured hippocampal astrocytes J. Biol. Chem. 1999, 274 (32) 22539-22547
22. Kržan, M.; Stenovec, M.; Kreft, M.; Pangršič, T.; Grilc, S.; Haydon, P. G.; Zorec, R. Calcium-dependent exocytosis of atrial natriuretic peptide from astrocytes J. Neurosci. 2003, 23 (5) 1580-1583 (Pubitemid 36314711)
23. Ramamoorthy, P.; Whim, M. D. Trafficking and fusion of neuropeptide Y-containing dense-core granules in astrocytes J. Neurosci. 2008, 28 (51) 13815-13827
24. 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 (2) 327-344
25. Wei, H.; Nolkrantz, K.; Parkin, M. C.; Chisolm, C. N.; O'Callaghan, J. P.; Kennedy, R. T. Identification and quantification of neuropeptides in brain tissue by capillary liquid chromatography coupled off-Line to MALDI-TOF and MALDI-TOF/TOF-MS Anal. Chem. 2006, 78 (13) 4342-4351
26. Svensson, M.; Sköld, K.; Svenningsson, P.; Andren, P. E. Peptidomics-based discovery of novel neuropeptides J. Proteome Res. 2003, 2 (2) 213-219 (Pubitemid 37099058)
27. Bora, A.; Annangudi, S. P.; Millet, L. J.; Rubakhin, S. S.; Forbes, A. J.; Kelleher, N. L.; Gillette, M. U.; Sweedler, J. V. Neuropeptidomics of the supraoptic rat nucleus J. Proteome Res. 2008, 7 (11) 4992-5003
28. Hatcher, N. G.; Atkins, N.; 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
29. Rubakhin, S. S.; Romanova, E. V.; Nemes, P.; Sweedler, J. V. Profiling metabolites and peptides in single cells Nat. Methods 2011, 8 (4s) S20-S29
30. Rubakhin, S. S.; Sweedler, J. V. Quantitative measurements of cell-cell signaling peptides with single-cell MALDI MS Anal. Chem. 2008, 80 (18) 7128-7136
31. Millet, L. J.; Bora, A.; Sweedler, J. V.; Gillette, M. U. Direct cellular peptidomics of supraoptic magnocellular and hippocampal neurons in low-density cocultures ACS Chem. Neurosci. 2009, 1 (1) 36-48
32. Gelman, J. S.; Sironi, J.; Castro, L. M.; Ferro, E. S.; Fricker, L. D. Peptidomic Analysis of Human Cell Lines J. Proteome Res. 2011, 10 (4) 1583-1592
33. 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. Biosys. 2010, 6 (8) 1355-1365
34. Dircksen, H.; Neupert, S.; Predel, R.; Verleyen, P.; Huybrechts, J.; Strauss, J.; Hauser, F.; Stafflinger, E.; Schneider, M.; Pauwels, K.; Schoofs, L.; Grimmelikhuijzen, C. J. P. Genomics, transcriptomics, and peptidomics of Daphnia pulex neuropeptides and protein hormones J. Proteome Res. 2011, 10 (10) 4478-4504
35. Li, L.; Sweedler, J. V. Peptides in the brain: mass spectrometry-based measurement approaches and challenges Annu. Rev. Anal. Chem. 2008, 1 (1) 451-483
36. Venance, L.; Stella, N.; Glowinski, J.; Giaume, C. Mechanism involved in initiation and propagation of receptor-induced intercellular calcium signaling in cultured rat astrocytes J. Neurosci. 1997, 17 (6) 1981-1992 (Pubitemid 27106757)
37. Jeftinija, S. D.; Jeftinija, K. V.; Stefanovic, G.; Liu, F. Neuroligand-evoked calcium-dependent release of excitatory amino acids from cultured astrocytes J. Neurochem. 1996, 66 (2) 676-684 (Pubitemid 26037318)
38. Morgan, A. C. A.; Chang, H.-Y.; Liu, J. S. H.; Hua, L. L.; Lee, S. C. High extracellular potassium modulates nitric oxide synthase expression in human astrocytes J. Neurochem. 2000, 74 (5) 1903-1912 (Pubitemid 30217645)
39. i and calmodulin Am. J. Physiol.: Cell Physiol. 1999, 277 (4) C823-C832
40. + concentration J. Neurochem. 1994, 62 (2) 489-495 (Pubitemid 24041314)
41. Haak, L. L.; Heller, H. C.; van den Pol, A. N. Metabotropic glutamate receptor activation modulates kainate and serotonin calcium response in astrocytes J. Neurosci. 1997, 17 (5) 1825-1837 (Pubitemid 27089827)
42. Jalonen, T. O.; Margraf, R. R.; Wielt, D. B.; Charniga, C. J.; Linne, M. L.; Kimelberg, H. K. Serotonin induces inward potassium and calcium currents in rat cortical astrocytes Brain Res. 1997, 758 (1-2) 69-82 (Pubitemid 27310644)
43. Anderson, E. J.; McFarland, D.; Kimelberg, H. K. Serotonin uptake by astrocytes in situ Glia 1992, 6 (2) 154-158
44. Parpura, V.; Basarsky, T. A.; Liu, F.; Jeftinij, K.; Jeftinija, S.; Haydon, P. G. Glutamate-mediated astrocyte-neuron signalling Nature 1994, 369, 744-747 (Pubitemid 24225363)
45. Alliota, F.; Pessac, B. Astrocytic cell clones derived from established cultures of 8-day postnatal mouse cerebella Brain Res. 1984, 306 (1-2) 283-291 (Pubitemid 14090466)
46. Dowell, J. A.; Heyden, W. V.; Li, L. Rat neuropeptidomics by LC-MS/MS and MALDI-FTMS: enhanced dissection and extraction techniques coupled with 2D RP-RP HPLC J. Proteome Res. 2006, 5 (12) 3368-3375 (Pubitemid 44904328)
47. Yin, P.; Hou, X.; Romanova, E. V.; Sweedler, J. V.; Merighi, A. Neuropeptidomics: mass spectrometry-based qualitative and quantitative analysis Methods Mol. Biol. 2011, 789, 223-236
48. Lapainis, T.; Rubakhin, S. S.; Sweedler, J. V. Capillary electrophoresis with electrospray ionization mass spectrometric detection for single-cell metabolomics Anal. Chem. 2009, 81 (14) 5858-5864
49. Knolhoff, A. M.; Nemes, P.; Rubakhin, S. S.; Sweedler, J. V. MS-based methodologies for single-cell metabolite detection and identification. In Methodologies for Metabolomics: Experimental Strategies and Techniques; Lutz, N.; Wevers, R.; Sweedler, J. V., Eds.: Cambridge University Press: New York, 2012.
50. Nemes, P.; Knolhoff, A. M.; Rubakhin, S. S.; Sweedler, J. V. Metabolic differentiation of neuronal phenotypes by single-cell capillary electrophoresis-electrospray ionization-mass spectrometry Anal. Chem. 2011, 83, 6810-6817
51. Squires, L. N.; Talbot, K. N.; Rubakhin, S. S.; Sweedler, J. V. Serotonin catabolism in the central and enteric nervous systems of rats upon induction of serotonin syndrome J. Neurochem. 2007, 103 (1) 174-180 (Pubitemid 47404206)
52. Cahoy, J. D.; Emery, B.; Kaushal, A.; Foo, L. C.; Zamanian, J. L.; Christopherson, K. S.; Xing, Y.; Lubischer, J. L.; Krieg, P. A.; Krupenko, S. A.; Thompson, W. J.; Barres, B. A. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function J. Neurosci. 2008, 28 (1) 264-278
53. Vilijn, M. H.; Vaysse, P. J.; Zukin, R. S.; Kessler, J. A. Expression of preproenkephalin mRNA by cultured astrocytes and neurons Proc. Natl. Acad. Sci. U.S.A. 1988, 85 (17) 6551-6555
54. Shinoda, H.; Marini, A. M.; Cosi, C.; Schwartz, J. P. Brain region and gene specificity of neuropeptide gene expression in cultured astrocytes Science 1989, 245 (4916) 415-417 (Pubitemid 19203367)
55. Shinoda, H.; Marini, A. M.; Schwartz, J. P. Developmental expression of the proenkephalin and prosomatostatin genes in cultured cortical and cerebellar astrocytes Dev. Brain Res. 1992, 67 (2) 205-210
56. Vilijn, M.-H.; Das, B.; Kessler, J. A.; Flicker, L. D. Cultured astrocytes and neurons synthesize and secrete carboxypeptidase E, a neuropeptide-processing enzyme J. Neurochem. 1989, 53 (5) 1487-1493 (Pubitemid 19267017)
57. Rhodes, C. H.; Xu, R. Y.; Angeletti, R. H. Peptidylglycine alpha-amidating monooxygenase (PAM) in Schwann cells and glia as well as neurons J. Histochem. Cytochem. 1990, 38 (9) 1301-11 (Pubitemid 20266129)
58. Klein, R. S.; Fricker, L. D. Cultured astrocytes express mRNA for peptidylglycine-α-amidating monooxygenase, a neuropeptide processing enzyme Brain Res. 1992, 596 (1-2) 202-208
59. Ubink, R.; Calza, L.; Hökfelt, T. 'Neuro'-peptides in glia: Focus on NPY and galanin Trends Neurosci. 2003, 26 (11) 604-609 (Pubitemid 37338368)
60. Gelman, J.; Fricker, L. Hemopressin and other bioactive peptides from cytosolic proteins: are these non-classical neuropeptides? AAPS J. 2010, 12 (3) 279-289
61. Mo, X. Y.; Cascio, P.; Lemerise, K.; Goldberg, A. L.; Rock, K. Distinct proteolytic processes generate the C and N termini of MHC class I-binding peptides J. Immunol. 1999, 163 (11) 5851-5859
62. Vosler, P.; Brennan, C.; Chen, J. Calpain-mediated signaling mechanisms in neuronal injury and neurodegeneration Mol. Neurobiol. 2008, 38 (1) 78-100
63. Shields, D. C.; Tyor, W. R.; Deibler, G. E.; Hogan, E. L.; Banik, N. L. Increased calpain expression in activated glial and inflammatory cells in experimental allergic encephalomyelitis Proc. Natl. Acad. Sci. U.S.A. 1998, 95 (10) 5768-5772 (Pubitemid 28224171)
64. Chatila, T.; Silverman, L.; Miller, R.; Geha, R. Mechanisms of T cell activation by the calcium ionophore ionomycin J. Immunol. 1989, 143 (4) 1283-1289 (Pubitemid 19211362)
65. 2+ from intracellular stores in response to ionomycin in oocytes of the frog Xenopus laevis J. Physiol. (London) 1992, 458 (1) 307-318 (Pubitemid 23024595)
66. Wise, T. N.; Fishbain, D. A.; Holder-Perkins, V. Painful physical symptoms in depression: a clinical challenge Pain Med. 2007, 8 (s2) S75-S82
67. 2+ increases in cultured astrocytes from three different brain regions Neurochem. Int. 2000, 36 (4-5) 427-434 (Pubitemid 30101584)
68. Camby, I.; Le Mercier, M.; Lefranc, F.; Kiss, R. Galectin-1: a small protein with major functions Glycobiology 2006, 16 (11) 137R-157R (Pubitemid 44530693)