Mass spectrometry-based characterization of endogenous peptides and metabolites in small volume samples

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1854, Issue 7, 2015, Pages 732-740

  Ong, Ta Hsuan ^a   Tillmaand, Emily G ^a   Makurath, Monika ^a   Rubakhin, Stanislav S ^a   Sweedler, Jonathan V ^a  

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

Author keywords

Bioanalytical microanalysis; Mass spectrometry; Microenvironments; Single cell

Indexed keywords

PEPTIDE;

ANIMAL; HUMAN; MASS SPECTROMETRY; PROCEDURES;

ANIMALS; HUMANS; MASS SPECTROMETRY; PEPTIDES;

EID: 84939974291     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2015.01.008     Document Type: Review

References (103)

1. W.M. Weaver, P. Tseng, A. Kunze, M. Masaeli, A.J. Chung, J.S. Dudani, H. Kittur, R.P. Kulkarni, and D. Di Carlo Advances in high-throughput single-cell microtechnologies Curr. Opin. Biotechnol. 25 2014 114 123
2. N. Liu, L. Liu, and X. Pan Single-cell analysis of the transcriptome and its application in the characterization of stem cells and early embryos Cell. Mol. Life Sci. 71 2014 2707 2715
3. J.M. Irish, and D.B. Doxie High-dimensional single-cell cancer biology Curr. Top. Microbiol. Immunol. 377 2014 1 21
4. J.P. Junker, and A. van Oudenaarden Every cell is special: genome-wide studies add a new dimension to single-cell biology Cell 157 2014 8 11
5. L. Li, and J.V. Sweedler Peptides in the brain: mass spectrometry-based measurement approaches and challenges Annu. Rev. Anal. Chem. 1 2008 451 483
6. R. Zenobi Single-cell metabolomics: analytical and biological perspectives Science 342 2013
7. H. Gest The discovery of microorganisms by Robert Hooke and Antoni Van Leeuwenhoek, fellows of the Royal Society Notes Rec. R. Soc. Lond. 58 2004 187 201
8. S.S. Rubakhin, J.D. Churchill, W.T. Greenough, and J.V. Sweedler Profiling signaling peptides in single mammalian cells using mass spectrometry Anal. Chem. 78 2006 7267 7272
9. C. Cecala, and J.V. Sweedler Sampling techniques for single-cell electrophoresis Analyst 137 2012 2922 2929
10. T. Lapainis, and J.V. Sweedler Contributions of capillary electrophoresis to neuroscience J. Chromatogr. A 1184 2008 144 158
11. C. Cecala, S.S. Rubakhin, J.W. Mitchell, M.U. Gillette, and J.V. Sweedler A hyphenated optical trap capillary electrophoresis laser induced native fluorescence system for single-cell chemical analysis Analyst 137 2012 2965 2972
12. S.S. Rubakhin, E.V. Romanova, P. Nemes, and J.V. Sweedler Profiling metabolites and peptides in single cells Nat. Methods 8 2011 S20 S29
13. A. Amantonico, P.L. Urban, S.R. Fagerer, R.M. Balabin, and R. Zenobi Single-cell MALDI-MS as an analytical tool for studying intrapopulation metabolic heterogeneity of unicellular organisms Anal. Chem. 82 2010 7394 7400
14. L. Li, R.W. Garden, and J.V. Sweedler Single-cell MALDI: a new tool for direct peptide profiling Trends Biotechnol. 18 2000 151 160
15. S. Neupert, S.S. Rubakhin, and J.V. Sweedler Targeted single-cell microchemical analysis: MS-based peptidomics of individual paraformaldehyde-fixed and immunolabeled neurons Chem. Biol. 19 2012 1010 1019
16. S. Neupert, H.A. Johard, D.R. Nassel, and R. Predel Single-cell peptidomics of Drosophila melanogaster neurons identified by Gal4-driven fluorescence Anal. Chem. 79 2007 3690 3694
17. A. Bodzon-Kulakowska, A. Drabik, M. Marszalek, J.H. Kotlinska, and P. Suder DESI analysis of mammalian cell cultures - preparation and method optimisation J. Mass Spectrom. 49 2014 613 621
18. D. Holscher, R. Shroff, K. Knop, M. Gottschaldt, A. Crecelius, B. Schneider, D.G. Heckel, U.S. Schubert, and A. Svatos Matrix-free UV-laser desorption/ionization (LDI) mass spectrometric imaging at the single-cell level: distribution of secondary metabolites of Arabidopsis thaliana and Hypericum species Plant J. 60 2009 907 918
19. E.J. Lanni, S.J. Dunham, P. Nemes, S.S. Rubakhin, and J.V. Sweedler Biomolecular imaging with a C60-SIMS/MALDI dual Ion source hybrid mass spectrometer: instrumentation, matrix enhancement, and single cell analysis J. Am. Soc. Mass Spectrom. 25 2014 1897 1907
20. S. Parry, and N. Winograd High-resolution TOF-SIMS imaging of eukaryotic cells preserved in a trehalose matrix Anal. Chem. 77 2005 7950 7957
21. T.L. Colliver, C.L. Brummel, M.L. Pacholski, F.D. Swanek, A.G. Ewing, and N. Winograd Atomic and molecular imaging at the single-cell level with TOF-SIMS Anal. Chem. 69 1997 2225 2231
22. M.L. Heien, P.D. Piehowski, N. Winograd, and A.G. Ewing Lipid detection, identification, and imaging single cells with SIMS Methods Mol. Biol. 656 2010 85 97
23. P.J. O'Brien, M. Lee, M.E. Spilker, C.C. Zhang, Z. Yan, T.C. Nichols, W. Li, C.H. Johnson, G.J. Patti, and G. Siuzdak Monitoring metabolic responses to chemotherapy in single cells and tumors using nanostructure-initiator mass spectrometry (NIMS) imaging Cancer Metab. 1 2013 1 4
24. M. Lorenzo Tejedor, H. Mizuno, N. Tsuyama, T. Harada, and T. Masujima Direct single-cell molecular analysis of plant tissues by video mass spectrometry Anal. Sci. 25 2009 1053 1055
25. S. Date, H. Mizuno, N. Tsuyama, T. Harada, and T. Masujima Direct drug metabolism monitoring in a live single hepatic cell by video mass spectrometry Anal. Sci. 28 2012 201 203
26. S.C. Bendall, E.F. Simonds, P. Qiu, A.D. Amir el, P.O. Krutzik, R. Finck, R.V. Bruggner, R. Melamed, A. Trejo, O.I. Ornatsky, R.S. Balderas, S.K. Plevritis, K. Sachs, D. Pe'er, S.D. Tanner, and G.P. Nolan Single-cell mass cytometry of differential immune and drug responses across a human hematopoietic continuum Science 332 2011 687 696
27. D.R. Bandura, V.I. Baranov, O.I. Ornatsky, A. Antonov, R. Kinach, X. Lou, S. Pavlov, S. Vorobiev, J.E. Dick, and S.D. Tanner Mass cytometry: technique for real time single cell multitarget immunoassay based on inductively coupled plasma time-of-flight mass spectrometry Anal. Chem. 81 2009 6813 6822
28. A.J. Managh, S.L. Edwards, A. Bushell, K.J. Wood, E.K. Geissler, J.A. Hutchinson, R.W. Hutchinson, H.J. Reid, and B.L. Sharp Single cell tracking of gadolinium labeled CD4 + T cells by laser ablation inductively coupled plasma mass spectrometry Anal. Chem. 85 2013 10627 10634
29. A.S. Groombridge, S. Miyashita, S. Fujii, K. Nagasawa, T. Okahashi, M. Ohata, T. Umemura, A. Takatsu, K. Inagaki, and K. Chiba High sensitive elemental analysis of single yeast cells (Saccharomyces cerevisiae) by time-resolved inductively-coupled plasma mass spectrometry using a high efficiency cell introduction system Anal. Sci. 29 2013 597 603
30. B. Shrestha, and A. Vertes High-throughput cell and tissue analysis with enhanced molecular coverage by laser ablation electrospray ionization mass spectrometry using ion mobility separation Anal. Chem. 86 2014 4308 4315
31. J.A. Stolee, and A. Vertes Toward single-cell analysis by plume collimation in laser ablation electrospray ionization mass spectrometry Anal. Chem. 85 2013 3592 3598
32. B. Shrestha, and A. Vertes In situ metabolic profiling of single cells by laser ablation electrospray ionization mass spectrometry Anal. Chem. 81 2009 8265 8271
33. R. Trouillon, M.K. Passarelli, J. Wang, M.E. Kurczy, and A.G. Ewing Chemical analysis of single cells Anal. Chem. 85 2012 522 542
34. E.V. Romanova, J.T. Aerts, C.A. Croushore, and J.V. Sweedler Small-volume analysis of cell-cell signaling molecules in the brain Neuropsychopharmacology 39 2014 50 64
35. R. Chen, and L. Li Mass spectral imaging and profiling of neuropeptides at the organ and cellular domains Anal. Bioanal. Chem. 397 2010 3185 3193
36. A.B. Hummon, A. Amare, and J.V. Sweedler Discovering new invertebrate neuropeptides using mass spectrometry Mass Spectrom. Rev. 25 2006 77 98
37. C.R. Jiménez, K.W. Li, K. Dreisewerd, S. Spijker, R. Kingston, R.H. Bateman, A.L. Burlingame, A.B. Smit, J. van Minnen, and W.P.M. Geraerts Direct mass spectrometric peptide profiling and sequencing of single neurons reveals differential peptide patterns in a small neuronal network Biochemistry 37 1998 2070 2076
38. K.W. Li, R.M. Hoek, F. Smith, C.R. Jiménez, R.C. van der Schors, P.A. van Veelen, S. Chen, J. van der Greef, D.C. Parish, and P.R. Benjamin Direct peptide profiling by mass spectrometry of single identified neurons reveals complex neuropeptide-processing pattern J. Biol. Chem. 269 1994 30288 30292
39. C.R. Jiménez, P.A.v. Veelen, K.W. Li, W.C. Wildering, W.P.M. Geraerts, U.R. Tjaden, and J.v.d. Greef Rapid communication: neuropeptide expression and processing as revealed by direct matrix-assisted laser desorption ionization mass spectrometry of single neurons J. Neurochem. 62 1994 404 407
40. S.S. Rubakhin, R.W. Garden, R.R. Fuller, and J.V. Sweedler Measuring the peptides in individual organelles with mass spectrometry Nat. Biotechnol. 18 2000 172 175
41. S.S. Rubakhin, and J.V. Sweedler Characterizing peptides in individual mammalian cells using mass spectrometry Nat. Protoc. 2 2007 1987 1997
42. S.S. Rubakhin, and J.V. Sweedler Quantitative measurements of cell-cell signaling peptides with single-cell MALDI MS Anal. Chem. 80 2008 7128 7136
43. L. Bai, E.V. Romanova, and J.V. Sweedler Distinguishing endogenous d-amino acid-containing neuropeptides in individual neurons using tandem mass spectrometry Anal. Chem. 83 2011 2794 2800
44. J.L. Jarecki, K. Andersen, C.J. Konop, J.J. Knickelbine, M.M. Vestling, and A.O. Stretton Mapping neuropeptide expression by mass spectrometry in single dissected identified neurons from the dorsal ganglion of the nematode Ascaris suum ACS Chem. Neurosci. 1 2010 505 519
45. S. Neupert, S. Schattschneider, and R. Predel Allatotropin-related peptide in cockroaches: identification via mass spectrometric analysis of single identified neurons Peptides 30 2009 489 494
46. E.J. Lanni, S.S. Rubakhin, and J.V. Sweedler Mass spectrometry imaging and profiling of single cells J. Proteome 75 2012 5036 5051
47. M.M. Gessel, J.L. Norris, and R.M. Caprioli MALDI imaging mass spectrometry: spatial molecular analysis to enable a new age of discovery J. Proteome 107 2014 71 82
48. R.M.A. Heeren Getting the picture: the coming of age of imaging MS Int. J. Mass Spectrom. 2015 10.1016/j.ijms.2014.04.021 (in press)
49. S.S. Rubakhin, W.T. Greenough, and J.V. Sweedler Spatial profiling with MALDI MS: distribution of neuropeptides within single neurons Anal. Chem. 75 2003 5374 5380
50. W. Bouschen, O. Schulz, D. Eikel, and B. Spengler Matrix vapor deposition/recrystallization and dedicated spray preparation for high-resolution scanning microprobe matrix-assisted laser desorption/ionization imaging mass spectrometry (SMALDI-MS) of tissue and single cells Rapid Commun. Mass Spectrom. 24 2010 355 364
51. S. Guenther, A. Rompp, W. Kummer, and B. Spengler AP-MALDI imaging of neuropeptides in mouse pituitary gland with 5 μm spatial resolution and high mass accuracy Int. J. Mass Spectrom. 305 2011 228 237
52. Y. Schober, S. Guenther, B. Spengler, and A. Römpp Single cell matrix-assisted laser desorption/ionization mass spectrometry imaging Anal. Chem. 84 2012 6293 6297
53. B. Spengler, and M. Hubert Scanning microprobe matrix-assisted laser desorption ionization (SMALDI) mass spectrometry: instrumentation for sub-micrometer resolved LDI and MALDI surface analysis J. Am. Soc. Mass Spectrom. 13 2002 735 748
54. A. Zavalin, E.M. Todd, P.D. Rawhouser, J. Yang, J.L. Norris, and R.M. Caprioli Direct imaging of single cells and tissue at sub-cellular spatial resolution using transmission geometry MALDI MS J. Mass Spectrom. 47 2012 1473 1481
55. T.A. Zimmerman, S.S. Rubakhin, and J.V. Sweedler MALDI mass spectrometry imaging of neuronal cell cultures J. Am. Soc. Mass Spectrom. 22 2011 828 836
56. J. Jurchen, S. Rubakhin, and J. Sweedler MALDI-MS imaging of features smaller than the size of the laser beam J. Am. Soc. Mass Spectrom. 16 2005 1654 1659
57. J.H. Jungmann, L. MacAleese, R. Buijs, F. Giskes, A. de Snaijer, J. Visser, J. Visschers, M.J.J. Vrakking, and R.M.A. Heeren Fast, high resolution mass spectrometry imaging using a medipix pixelated detector J. Am. Soc. Mass Spectrom. 21 2010 2023 2030
58. A.F.M. Altelaar, S.L. Luxembourg, L.A. McDonnell, S.R. Piersma, and R.M.A. Heeren Imaging mass spectrometry at cellular length scales Nat. Protoc. 2 2007 1185 1196
59. S.L. Luxembourg, T.H. Mize, L.A. McDonnell, and R.M.A. Heeren High-spatial resolution mass spectrometric imaging of peptide and protein distributions on a surface Anal. Chem. 76 2004 5339 5344
60. J.H. Jungmann, L. MacAleese, J. Visser, M.J.J. Vrakking, and R.M.A. Heeren High dynamic range bio-molecular ion microscopy with the timepix detector Anal. Chem. 83 2011 7888 7894
61. J.H. Jungmann, D.F. Smith, A. Kiss, L. MacAleese, R. Buijs, and R.M.A. Heeren An in-vacuum, pixelated detection system for mass spectrometric analysis and imaging of macromolecules Int. J. Mass Spectrom. 341-342 2013 34 44
62. A.F.M. Altelaar, I.M. Taban, L.A. McDonnell, P.D.E.M. Verhaert, R.P.J. de Lange, R.A.H. Adan, W.J. Mooi, R.M.A. Heeren, and S.R. Piersma High-resolution MALDI imaging mass spectrometry allows localization of peptide distributions at cellular length scales in pituitary tissue sections Int. J. Mass Spectrom. 260 2007 203 211
63. J. Jungmann, D. Smith, L. MacAleese, I. Klinkert, J. Visser, and R.A. Heeren Biological tissue imaging with a position and time sensitive pixelated detector J. Am. Soc. Mass Spectrom. 23 2012 1679 1688
64. J. Soltwisch, G. Göritz, J.H. Jungmann, A. Kiss, D.F. Smith, S.R. Ellis, and R.M.A. Heeren MALDI mass spectrometry imaging in microscope mode with infrared lasers: bypassing the diffraction limits Anal. Chem. 86 2013 321 325
65. P.L. Urban, K. Jefimovs, A. Amantonico, S.R. Fagerer, T. Schmid, S. Madler, J. Puigmarti-Luis, N. Goedecke, and R. Zenobi High-density micro-arrays for mass spectrometry Lab Chip 10 2010 3206 3209
66. M. Pabst, S.R. Fagerer, R. Köhling, S.K. Küster, R. Steinhoff, M. Badertscher, F. Wahl, P.S. Dittrich, K. Jefimovs, and R. Zenobi Self-aliquoting microarray plates for accurate quantitative matrix-assisted laser desorption/ionization mass spectrometry Anal. Chem. 85 2013 9771 9776
67. A.J. Ibáñez, S.R. Fagerer, A.M. Schmidt, P.L. Urban, K. Jefimovs, P. Geiger, R. Dechant, M. Heinemann, and R. Zenobi Mass spectrometry-based metabolomics of single yeast cells Proc. Natl. Acad. Sci. U. S. A. 110 2013 8790 8794
68. S.R. Fagerer, T. Schmid, A.J. Ibanez, M. Pabst, R. Steinhoff, K. Jefimovs, P.L. Urban, and R. Zenobi Analysis of single algal cells by combining mass spectrometry with Raman and fluorescence mapping Analyst 138 2013 6732 6736
69. S.D. Tanner, V.I. Baranov, O.I. Ornatsky, D.R. Bandura, and T.C. George An introduction to mass cytometry: fundamentals and applications Cancer Immunol. Immunother. 62 2013 955 965
70. G.K. Behbehani, S.C. Bendall, M.R. Clutter, W.J. Fantl, and G.P. Nolan Single-cell mass cytometry adapted to measurements of the cell cycle Cytometry Part A 81A 2012 552 566
71. A. Horowitz, D.M. Strauss-Albee, M. Leipold, J. Kubo, N. Nemat-Gorgani, O.C. Dogan, C.L. Dekker, S. Mackey, H. Maecker, G.E. Swan, M.M. Davis, P.J. Norman, L.A. Guethlein, M. Desai, P. Parham, and C.A. Blish Genetic and environmental determinants of human NK cell diversity revealed by mass cytometry Sci. Transl. Med. 5 2013 (208ra145)
72. M.D. Leipold, O. Ornatsky, V. Baranov, C. Whitfield, and M. Nitz Development of mass cytometry methods for bacterial discrimination Anal. Biochem. 419 2011 1 8
73. E.W. Newell, N. Sigal, N. Nair, B.A. Kidd, H.B. Greenberg, and M.M. Davis Combinatorial tetramer staining and mass cytometry analysis facilitate T-cell epitope mapping and characterization Nat. Biotechnol. 31 2013 623 629
74. A. Han, E.W. Newell, J. Glanville, N. Fernandez-Becker, C. Khosla, Y.-h. Chien, and M.M. Davis Dietary gluten triggers concomitant activation of CD4 + and CD8 + αβ T cells and γδ T cells in celiac disease Proc. Natl. Acad. Sci. U. S. A. 110 2013 13073 13078
75. Evan W. Newell, N. Sigal, Sean C. Bendall, Garry P. Nolan, and Mark M. Davis Cytometry by time-of-flight shows combinatorial cytokine expression and virus-specific cell niches within a continuum of CD8 + T cell phenotypes Immunity 36 2012 142 152
76. G. Chen, and N.-p. Weng Analyzing the phenotypic and functional complexity of lymphocytes using CyTOF (cytometry by time-of-flight) Cell. Mol. Immunol. 9 2012 322 323
77. C.E. Dugan, and R.T. Kennedy Measurement of lipolysis products secreted by 3T3-L1 adipocytes using microfluidics Methods Enzymol. 538 2014 195 209
78. J.G. Shackman, G.M. Dahlgren, J.L. Peters, and R.T. Kennedy Perfusion and chemical monitoring of living cells on a microfluidic chip Lab Chip 5 2005 56 63
79. K.R. Reid, and R.T. Kennedy Continuous operation of microfabricated electrophoresis devices for 24 hours and application to chemical monitoring of living cells Anal. Chem. 81 2009 6837 6842
80. X. Zhong, Z. Zhang, S. Jiang, and L. Li Recent advances in coupling capillary electrophoresis-based separation techniques to ESI and MALDI-MS Electrophoresis 35 2014 1214 1225
81. P. Nemes, A.M. Knolhoff, S.S. Rubakhin, and J.V. Sweedler Metabolic differentiation of neuronal phenotypes by single-cell capillary electrophoresis-electrospray ionization-mass spectrometry Anal. Chem. 83 2011 6810 6817
82. P. Nemes, A.M. Knolhoff, S.S. Rubakhin, and J.V. Sweedler Single-cell metabolomics: changes in the metabolome of freshly isolated and cultured neurons ACS Chem. Neurosci. 3 2012 782 792
83. J. Liu, J.T. Aerts, S.S. Rubakhin, X. Zhang, and J. Sweedler Analysis of endogenous nucleotides by single cell capillary electrophoresis-mass spectrometry Analyst 139 2014 5835 5842
84. J.T. Aerts, K.R. Louis, S.R. Crandall, G. Govindaiah, C.L. Cox, and J.V. Sweedler Patch clamp electrophysiology and capillary electrophoresis-mass spectrometry metabolomics for single cell characterization Anal. Chem. 86 2014 3203 3208
85. J.S. Mellors, K. Jorabchi, L.M. Smith, and J.M. Ramsey Integrated microfluidic device for automated single cell analysis using electrophoretic separation and electrospray ionization mass spectrometry Anal. Chem. 82 2010 967 973
86. S. Mao, J. Zhang, H. Li, and J.-M. Lin Strategy for signaling molecule detection by using an integrated microfluidic device coupled with mass spectrometry to study cell-to-cell communication Anal. Chem. 85 2012 868 876
87. A.G. Ngounou Wetie, I. Sokolowska, A.G. Woods, K.L. Wormwood, S. Dao, S. Patel, B.D. Clarkson, and C.C. Darie Automated mass spectrometry-based functional assay for the routine analysis of the secretome J. Lab. Autom. 18 2013 19 29
88. H. Skalnikova, J. Motlik, S.J. Gadher, and H. Kovarova Mapping of the secretome of primary isolates of mammalian cells, stem cells and derived cell lines Proteomics 11 2011 691 708
89. J.M. Iannacone, S. Ren, N.G. Hatcher, and J.V. Sweedler Collecting peptide release from the brain using porous polymer monolith-based solid phase extraction capillaries Anal. Chem. 81 2009 5433 5438
90. F.S. Vilim, E.C. Cropper, D.A. Price, I. Kupfermann, and K.R. Weiss Release of peptide cotransmitters in Aplysia: regulation and functional implications J. Neurosci. 16 1996 8105 8114
91. P.E. Lloyd, S. Schacher, I. Kupfermann, and K.R. Weiss Release of neuropeptides during intracellular stimulation of single identified Aplysia neurons in culture Proc. Natl. Acad. Sci. U. S. A. 83 1986 9794 9798
92. J.F. Dishinger, K.R. Reid, and R.T. Kennedy Quantitative monitoring of insulin secretion from single islets of Langerhans in parallel on a microfluidic chip Anal. Chem. 81 2009 3119 3127
93. C.E. Dugan, W.P. Cawthorn, O.A. MacDougald, and R.T. Kennedy Multiplexed microfluidic enzyme assays for simultaneous detection of lipolysis products from adipocytes Anal. Bioanal. Chem. 406 2014 4851 4859
94. D. Wei, M.J. Bailey, P. Andrew, and T. Ryhanen Electrochemical biosensors at the nanoscale Lab Chip 9 2009 2123 2131
95. H. Wei, H. Li, D. Gao, and J.-M. Lin Multi-channel microfluidic devices combined with electrospray ionization quadrupole time-of-flight mass spectrometry applied to the monitoring of glutamate release from neuronal cells Analyst 135 2010 2043 2050
96. M. Yang, T.-C. Chao, R. Nelson, and A. Ros Direct detection of peptides and proteins on a microfluidic platform with MALDI mass spectrometry Anal. Bioanal. Chem. 404 2012 1681 1689
97. S.S. Rubakhin, J.S. Page, B.R. Monroe, and J.V. Sweedler Analysis of cellular release using capillary electrophoresis and matrix assisted laser desorption/ionization-time of flight-mass spectrometry Electrophoresis 22 2001 3752 3758
98. C.A. Croushore, S.A. Supharoek, C.Y. Lee, J. Jakmunee, and J.V. Sweedler Microfluidic device for the selective chemical stimulation of neurons and characterization of peptide release with mass spectrometry Anal. Chem. 84 2012 9446 9452
99. N.G. Hatcher, T.A. Richmond, S.S. Rubakhin, and J.V. Sweedler Monitoring activity-dependent peptide release from the CNS using single-bead solid-phase extraction and MALDI TOF MS detection Anal. Chem. 77 2005 1580 1587
100. Y. Fan, S.S. Rubakhin, and J.V. Sweedler Collection of peptides released from single neurons with particle-embedded monolithic capillaries followed by detection with matrix-assisted laser desorption/ionization mass spectrometry Anal. Chem. 83 2011 9557 9563
101. Y. Fan, C.Y. Lee, S.S. Rubakhin, and J.V. Sweedler Stimulation and release from neurons via a dual capillary collection device interfaced to mass spectrometry Analyst 138 2013 6337 6346
102. M. Zhong, C.Y. Lee, C.A. Croushore, and J.V. Sweedler Label-free quantitation of peptide release from neurons in a microfluidic device with mass spectrometry imaging Lab Chip 12 2012 2037 2045
103. N.G. Hatcher, N. Atkins, S.P. Annangudi, A.J. Forbes, N.L. Kelleher, M.U. Gillette, and J.V. Sweedler Mass spectrometry-based discovery of circadian peptides Proc. Natl. Acad. Sci. U. S. A. 105 2008 12527 12532