Characterizing peptides in individual mammalian cells using mass spectrometry

Nature Protocols

Volumn 2, Issue 8, 2007, Pages 1987-1997

  Rubakhin, Stanislav S ^a   Sweedler, Jonathan V ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDE;

ANIMAL CELL; ARTICLE; CELL ISOLATION; CELL TYPE; CONTROLLED STUDY; HYPOPHYSIS CELL; INVERTEBRATE; MAMMAL CELL; MASS SPECTROMETRY; METHODOLOGY; NERVOUS SYSTEM; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; RAT; REFLEX; SIGNAL TRANSDUCTION;

ANIMALS; PEPTIDES; PITUITARY GLAND; RATS; SIGNAL TRANSDUCTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

ANIMALIA; INVERTEBRATA; MAMMALIA; RATTUS;

EID: 34548177101     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2007.277     Document Type: Article

References (90)

1. Garden, R.W., Shippy, S.A., Li, L., Moroz, T.P. & Sweedler, J.V. Proteolytic processing of the Aplysia egg-laying hormone prohormone. Proc. Natl. Acad. Sci. USA 95, 3972-3977 (1998).
2. Li, L., Garden, R.W. & Sweedler, J.V. Single-cell MALDI: A new tool for direct peptide profiling. Trends Biotechnol. 18, 151-160 (2000).
3. Rubakhin, S.S., Garden, R.W., Fuller, R.R. & Sweedler, J.V. Measuring the peptides in individual organelles with mass spectrometry. Nat. Biotechnol. 18, 172-175 (2000).
4. Rubakhin, S.S., Greenough, W.T. & Sweedler, J.V. Spatial profiling with MALDI MS: Distribution of neuropeptides within single neurons. Anal. Chem. 75, 5374-5380 (2003).
5. Rubakhin, S.S., Li, L., Moroz, T.P. & Sweedler, J.V. Characterization of the Aplysia californica cerebral ganglion F cluster. J. Neurophysiol. 81, 1251-1260 (1999).
6. Sweedler, J.V., Rubakhin, S.S., Churchill, J.D. & Greenough, W.T. Assaying the neuropeptides in single mammalian neurons using mass spectrometry. Program no. 326.16. 2003 Abstract Viewer/Itinerary Planner (Society for Neuroscience, Washington, DC, 2003, http://sfn.scholarone.com/itin2003/).
7. Rubakhin, S.S., Churchill, J.D., Greenough, W.T. & Sweedler, J.V. Profiling signaling peptides in single mammalian cells using mass spectrometry. Anal. Chem. 78, 7267-7272 (2006).
8. Research highlights. Biochemistry: Cell detectives. Nature 443 248-249 (2006).
9. Pacak, K., Aguilera, G., Sabban, E. & Kvetnansky, R. (eds.) Stress: Current Neuroendocrine and Genetic Approaches Vol. 1018 (New York Academy of Sciences, New York, 2004).
10. Sandman, C.A. et al. (eds.). Neuropeptides: Structure and Function in Biology and Behavior Vol. 897 (New York Academy of Sciences, New York, 1999).
11. Strand, F.L. Neuropeptides: Regulators of Physiological Proesses (MIT Press, Cambridge, MA, 1999).
12. Kastin, A.J. Handbook of Biologically Active Peptides (Academic, Amsterdam, Boston, 2006).
13. Walsh, J.H. & Dockray, G.J. Gut Peptides: Biochemistry and Physiology (Raven Press, New York, 1994).
14. Sewald, N. & Jakubke, H.-D. Peptides: Chemistry and Biology (Wiley-VCH, Weinheim, 2002).
15. Levin, E.R., Hu, R.M., Rossi, M. & Pickart, M. Arginine vasopressin stimulates atrial natriuretic peptide gene expression and secretion from rat diencephalic neurons. Endocrinology 131, 1417-1423 (1992).
16. Jensen, J. Regulatory peptides and control of food intake in non-mammalian vertebrates. Comp. Biochem. Physiol. A 128, 471-479 (2001).
17. Gundlach, A.L., Burazin, T.C. & Larm, J.A. Distribution, regulation and role of hypothalamic galanin systems: Renewed interest in a pleiotropic peptide family. Clin. Exp. Pharmacol. Physiol. 28, 100-105 (2001).
18. Okada, Y., Tsuda, Y., Bryant, S.D. & Lazarus, L.H. Endomorphins and related opioid peptides. Vitam. Horm. 65, 257-279 (2002).
19. Kieffer, B.L. & Gaveriaux-Ruff, C. Exploring the opioid system by gene knockout. Prog. Neurobiol. 66, 285-306 (2002).
20. Stefano, G.B., Fricchione, G., Goumon, Y. & Esch, T. Pain, immunity, opiate and opioid compounds and health. Med. Sci. Monit. 11, MS47-MS53 (2005).
21. Hardy, J.A. & Higgins, G.A. Alzheimer's disease: The amyloid cascade hypothesis. Science 256, 184-185 (1992).
22. Taylor, A. & Jones, M.T. Chemical Communication Within the Nervous System and Its Disturbance in Disease (Pergamon, Oxford, New York, 1977).
23. Davison, A.N. & Thompson, R.H.S. The Molecular Basis of Neuropathology (Edward Arnold, London, 1981).
24. Laidlaw, J.P., Richens, A. & Oxley, J. A Textbook of Epilepsy (Churchill Livingstone, Edinburgh, New York, 1988).
25. Bradford, H.F. Chemical Neurobiology: An Introduction to Neurochemistry (W.H. Freeman, New York, 1986).
26. Ebner, K. & Singewald, N. The role of substance P in stress and anxiety responses. Amino Acids 31, 251-272 (2006).
27. Cummings, D.E. Ghrelin and the short- and long-term regulation of appetite and body weight. Physiol. Behav. 89, 71-84 (2006).
28. Crawley, J.N. & Corwin, R.L. Biological actions of cholecystokinin. Peptides 15, 731-755 (1994).
29. Charmandari, E., Tsigos, C. & Chrousos, G. Endocrinology of the stress response. Annu. Rev. Physiol. 67, 259-284 (2005).
30. Porte, D. Jr., Baskin, D.G. & Schwartz, M.W. Insulin signaling in the central nervous system: A critical role in metabolic homeostasis and disease from C. elegans to humans. Diabetes 54, 1264-1276 (2005).
31. Bach, P.H. & Baker, J.R.J. Histochemical and Immunohistochemical Techniques: Applications to Pharmacology and Toxicology (Chapman & Hall, London, 1991).
32. Pool, C.W., Buijs, R.M., Swaab, D.G. & Boer, F.W. Immunohistochemistry. in IBRO Handbook Series Vol. 3 (ed. Cuello, A.C.) xvii 501 (Wiley, Chichester, West Sussex, New York, 1983).
33. Brownstein, M.J., Saavedra, J.M., Axelrod, J., Zeman, G.H. & Carpenter, D.O. Coexistence of several putative neurotransmitters in single identified neurons of Aplysia. Proc. Natl. Acad. Sci. USA 71 4662-4665 (1974).
34. Irvine, G.B. & Williams, C.H. Neuropeptide Protocols (Humana Press, Totowa, NJ, 1997).
35. Silberring, J. & Ekman, R. Mass Spectrometry and Hyphenated Techniques in Neuropeptide Research (Wiley-Interscience, New York, 2002).
36. Michael, A.C. & Borland, L.M. Electrochemical Methods for Neuroscience (CRC Press/Taylor & Francis, Boca Raton, FL, 2007).
37. Xu, X.-H.N. (ed.) New Frontiers in Ultrasensitive Bioanalysis: Advanced Analytical Chemistry Applications in Nanobiotechnology, Single Molecule Detection, and Single Cell Analysis 308 (Wiley, Hoboken, NJ, 2007).
38. Sweedler, J.V. & Arriaga, E.A. Single cell analysis. Anal. Bioanal. Chem. 387, 1-2 (2007).
39. Baggerman, G., Cerstiaens, A., De Loof, A. & Schoofs, L. Peptidomics of the larval Drosophila melanogaster central nervous system. J. Biol. Chem. 277, 40368-40374 (2002).
40. Clynen, E. et al. Peptidomics of the pars intercerebralis-corpus cardiacum complex of the migratory locust, Locusta migratoria. Eur. J. Biochem. 268, 1929-1939 (2001).
41. Svensson, M., Skold, K., Svenningsson, P. & Andren, P.E. Peptidomics-based discovery of novel neuropeptides. J. Proteome Res. 2, 213-219 (2003).
42. Hummon, A.B. et al. From the genome to the proteome: Uncovering peptides in the Apis brain. Science 314, 647-649 (2006).
43. Husson, S.J., Clynen, E., Baggerman, G., De Loof, A. & Schoofs, L. Discovering neuropeptides in Caenorhabditis elegans by two dimensional liquid chromatography and mass spectrometry. Biochem. Biophys. Res. Commun. 335, 76-86 (2005).
44. Wei, H. et al. 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. 78, 4342-4351 (2006).
45. Fricker, L.D., Lim, J., Pan, H. & Che, F.Y. Peptidomics: Identification and quantification of endogenous peptides in neuroendocrine tissues. Mass Spectrom. Rev. 25, 327-344 (2006).
46. Hummon, A.B., Amare, A. & Sweedler, J.V. Discovering new invertebrate neuropeptides using mass spectrometry. Mass Spectrom. Rev. 25 77-98 (2006).
47. Karas, M., Bahr, U. & Giessmann, U. Matrix-assisted laser desorption ionization mass-spectrometry. Mass Spectrom. Rev. 10, 335-357 (1991).
48. Tanaka, K. et al. Protein and polymer analysis up to m/z 100,000 by laser ionisation time-of-flight mass spectometry. Rapid Commun. Mass Spectrom. 2, 151-153 (1988).
49. Hillenkamp, F., Karas, M., Beavis, R.C. & Chait, B.T. Matrix-assisted laser desorption ionization mass-spectrometry of biopolymers. Anal. Chem. 63, A1193-A1202 (1991).
50. Ong, S.E. & Mann, M. Mass spectrometry-based proteomics turns quantitative. Nat. Chem. Biol. 1, 252-262 (2005).
51. Bienvenut, W.V. et al. Matrix-assisted laser desorption/ ionization-tandem mass spectrometry with high resolution and sensitivity for identification and characterization of proteins. Proteomics 2, 868-876 (2002).
52. Medzihradszky, K.F. et al. The characteristics of peptide collision-induced dissociation using a high-performance MALDI-TOF/TOF tandem mass spectrometer. Anal. Chem. 72, 552-558 (2000).
53. Yergey, A.L. et al. De novo sequencing of peptides using MALDI/ TOF-TOF. J. Am. Soc. Mass Spectrom. 13, 784-791 (2002).
54. Suckau, D. et al. A novel MALDI LIFT-TOF/TOF mass spectrometer for proteomics. Anal. Bioanal. Chem. 376, 952-965 (2003).
55. Ma, P.W.K. et al. Characterizing the Hez-PBAN gene products in neuronal clusters with immunocytochemistry and MALDI MS. J. Insect Plysiol. 46, 221-230 (2000).
56. Jimenez, C.R. et al. Direct mass spectrometric peptide profiling and sequencing of single neurons reveals differential peptide patterns in a small neuronal network. Biochemistry 37, 2070-2076 (1998).
57. Jimenez, C.R. et al. Neuropeptide expression and processing as revealed by direct matrix-assisted laser desorption ionization mass spectrometry of single neurons. J. Neurochem. 62, 404-407 (1994).
58. Li, L. et al. Orcokinin peptides in developing and adult crustacean stomatogastric nervous systems and pericardial organs. J. Comp. Neurol. 444, 227-244 (2002).
59. Sweedler, J.V. et al. Identification and characterization of the feeding circuit-activating peptides, a novel neuropeptide family of Aplysia. J. Neurosci. 22, 7797-7808 (2002).
60. Standing, K.G. Peptide and protein de novo sequencing by mass spectrometry. Curr. Opin. Struct. Biol. 13, 595-601 (2003).
61. Nachman, R.J. et al. Occurrence of insect kinins in the flesh fly, stable fly and horn fly - mass spectrometric identification from single nerves and diuretic activity. Peptides 23, 1885-1894 (2002).
62. Jimenez, C.R. Batch introduction techniques. in Mass Spectrometry: Modified Proteins and Glycoconjugates Vol. 405 (ed. Burlingame, A.L.) 36-49 (Elsevier Academic Press, Boston, USA, 2005.
63. Glass, D.J. Experimental Design for Biologists (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 2007).
64. Townend, J. Practical Statistics for Environmental and Biological Scientists (Wiley, Chichester, New York, 2001).
65. Freshney, R.I. Culture of Animal Cells: A Manual of Basic Technique (Wiley-Liss, Hoboken, NJ, 2005).
66. Hatoya, S. et al. Isolation and charaterization of embryonic stem-like cells from canine blastocysts. Mol. Reprod. Dev. 73 298-305 (2006).
67. Jiang, X.Y. et al. Methods for isolating highly-enriched embryonic spinal cord neurons: A comparison between enzymatic and mechanical dissociations. J. Neurosci. Methods 158, 13-18 (2006).
68. Weiler, I.J. et al. Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation. Proc. Natl. Acad. Sci. USA 94, 5395-5400 (1997).
69. Murray, G.I. & Curran, S. Laser Capture Microdissection: Methods and Protocols (Humana Press, Totowa, NJ, 2005).
70. Nishino, S. The hypothalamic peptidergic system, hypocretin/orexin and vigilance control. Neuropeptides 41, 117-133 (2007).
71. Elias, C.F. et al. Chemically defined projections linking the mediobasal hypothalamus and the lateral hypothalamic area. J. Comp. Neurol. 402, 442-459 (1998).
72. Antoni, F.A. Vasopressinergic control of pituitary adrenocorticotropin secretion comes of age. Front. Neuroendocrinol. 14, 76-122 (1993).
73. Gerfen, C.R. & Young, W.S. III Distribution of striatonigral and striatopallidal peptidergic neurons in both patch and matrix compartments: An in situ hybridization histochemistry and fluorescent retrograde tracing study. Brain Res. 460, 161-167 (1988).
74. Bollheimer, L.C., Skelly, R.H., Chester, M.W., McGarry, J.D. & Rhodes, C.J. Chronic exposure to free fatty acid reduces pancreatic beta cell insulin content by increasing basal insulin secretion that is not compensated for by a corresponding increase in proinsulin biosynthesis translation. J. Clin. Invest. 101, 1094-1101 (1998).
75. Monroe, E.B. et al. Massively parallel sample preparation for the MALDI MS analyses of tissues. Anal. Chem. 78, 6826-6832 (2006).
76. Monroe, E.B., Koszczuk, B.A., Losh, J.L. & Sweedler, J.V. Measuring salty samples without adducts with MALDI MS. Int. J. Mass Spectrom. 260, 237-242 (2007).
77. Wingerd, B.D. & Stein, G. Rat Dissection Manual (Carolina Biological Supply, Burlington, NC, 1988).
78. Walker, W.F. & Homberger, D.G. Anatomy and Dissection of the Rat (W.H. Freeman, New York, 1997).
79. Miao, H., Rubakhin, S.S. & Sweedler. J.V. Subcellular analysis of o-aspartate. Anal. Chem. 77, 7190-7194 (2005).
80. Cagney, G. & Emili, A. De novo peptide sequencing and quantitative profiling of complex protein mixtures using mass-coded abundance tagging. Nat. Biotechnol. 20, 163-170 (2002).
81. n 3′ in the human FMR1 gene. J. Biol. Chem. 272, 16761-16768 (1997).
82. Hunt, D.F., Yates, J.R. III, Shabanowitz, J., Winston, S. & Hauer, C.R. Protein sequencing by tandem mass spectrometry. Proc. Natl. Acad. Sci. USA 83, 6233-6237 (1986).
83. Li, L., Garden, R.W., Romanova, E.V. & Sweedler, J.V. In situ sequencing of peptides from biological tissues and single cells using MALDI-PSD/CID analysis. Anal. Chem. 71, 5451-5458 (1999).
84. Mann, M. & Jensen, O.N. Proteomic analysis of post-translational modifications. Nat. Biotechnol. 21, 255-261 (2003).
85. Shevchenko, A. et al. Rapid 'de novo' peptide sequencing by a combination of nanoelectrospray, isotopic labeling and a quadrupole/ time-of-flight mass spectrometer. Rapid Commun. Mass Spectrom. 11, 1015-1024 (1997).
86. Shevchenko, A., Wilm, M., Vorn, O. & Mann, M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858 (1996).
87. Steen, H. & Mann, M. The ABC's (and XYZ's) of peptide sequencing. Nat. Rev. Mol. Cell Biol. 5, 699-711 (2004).
88. Li, L. et al. Cerebrin prohormone processing and distribution in Aplysia californica. J. Neurochem. 77, 1569-1580 (2001).
89. Li, L. et al. Peptide profiling of cells with multiple gene products: Combining immunochemistry and MALDI mass spectrometry with on-plate microextraction. Anal. Chem. 72, 3867-3874 (2000).
90. Li, L.J. et al. Mass spectrometric survey of interganglionically transported peptides in Aplysia. Peptides 19, 1425-1433 (1998).