Neuropeptidomics: Improvements in Mass Spectrometry Imaging Analysis and Recent Advancements

Author(s): Nhu Q. Vu, Kellen DeLaney, Lingjun Li*

Journal Name: Current Protein & Peptide Science

Volume 22 , Issue 2 , 2021


Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Abstract:

Neuropeptides are an important class of endogenous peptides in the nervous system that regulate physiological functions such as feeding, glucose homeostasis, pain, memory, reproduction, and many others. In order to understand the functional role of neuropeptides in diseases or disorders, studies investigating their dysregulation in terms of changes in abundance and localization must be carried out. As multiple neuropeptides are believed to play a functional role in each physiological process, techniques capable of global profiling multiple neuropeptides simultaneously are desired. Mass spectrometry is well-suited for this goal due to its ability to perform untargeted measurements without prior comprehensive knowledge of the analytes of interest. Mass spectrometry imaging (MSI) is particularly useful because it has the capability to image a large variety of peptides in a single experiment without labeling. Like all analytical techniques, careful sample preparation is critical to successful MSI analysis. The first half of this review focuses on recent developments in MSI sample preparation and instrumentation for analyzing neuropeptides and other biomolecules in which the sample preparation technique may be directly applicable for neuropeptide analysis. The benefit offered by incorporating these techniques is shown as improvement in a number of observable neuropeptides, enhanced signal to noise, increased spatial resolution, or a combination of these aspects. The second half of this review focuses on recent biological discoveries about neuropeptides resulting from these improvements in MSI analysis. The recent progress in neuropeptide detection and analysis methods, including the incorporation of various tissue washes, matrices, instruments, ionization sources, and computation approaches combined with the advancements in understanding neuropeptide function in a variety of model organisms, indicates the potential for the utilization of MSI analysis of neuropeptides in clinical settings.

Keywords: Mass spectrometry imaging, neuropeptide, peptide, peptidomics, MALDI, LESA, MSI.

[1]
Brown, B.E. Proctolin: a peptide transmitter candidate in insects. Life Sci., 1975, 17(8), 1241-1252.
[http://dx.doi.org/10.1016/0024-3205(75)90133-2] [PMID: 575]
[2]
Burbach, J.P. What are neuropeptides? Methods Mol. Biol., 2011, 789, 1-36.
[http://dx.doi.org/10.1007/978-1-61779-310-3_1] [PMID: 21922398]
[3]
Elphick, M.R.; Mirabeau, O.; Larhammar, D. Evolution of neuropeptide signalling systems. J. Exp. Biol., 2018, 221(Pt 3), jeb151092.
[http://dx.doi.org/10.1242/jeb.151092] [PMID: 29440283]
[4]
Shaler, T.A.; Wickham, J.N.; Sannes, K.A.; Wu, K.J.; Becker, C.H. Effect of impurities on the matrix-assisted laser desorption mass spectra of single-stranded oligodeoxynucleotides. Anal. Chem., 1996, 68(3), 576-579.
[http://dx.doi.org/10.1021/ac9502662] [PMID: 8712365]
[5]
Yang, E.; Gamberi, C.; Chaurand, P. Mapping the fly Malpighian tubule lipidome by imaging mass spectrometry. J. Mass Spectrom., 2019, 54(6), 557-566.
[http://dx.doi.org/10.1002/jms.4366] [PMID: 31038251]
[6]
Diesner, M.; Predel, R.; Neupert, S. Neuropeptide Mapping of Dimmed Cells of Adult Drosophila Brain. J. Am. Soc. Mass Spectrom., 2018, 29(5), 890-902.
[http://dx.doi.org/10.1007/s13361-017-1870-1]
[7]
Perry, C.; Chung, J.Y.; Ylaya, K.; Choi, C.H.; Simpson, A.; Matsumoto, K.T.; Smith, W.A.; Hewitt, S.M. A Buffered Alcohol-Based Fixative for Histomorphologic and Molecular Applications. J. Histochem. Cytochem., 2016, 64(7), 425-440.
[http://dx.doi.org/10.1369/0022155416649579] [PMID: 27221702]
[8]
DeLaney, K.; Buchberger, A.; Li, L. Identification, Quantitation, and Imaging of the Crustacean Peptidome. Methods Mol. Biol., 2018, 1719, 247-269.
[http://dx.doi.org/10.1007/978-1-4939-7537-2_17] [PMID: 29476517]
[9]
van den Pol, A.N. Neuropeptide transmission in brain circuits. Neuron, 2012, 76(1), 98-115.
[http://dx.doi.org/10.1016/j.neuron.2012.09.014] [PMID: 23040809]
[10]
Dawson, G. Measuring brain lipids. Biochim. Biophys. Acta, 2015, 1851(8), 1026-1039.
[http://dx.doi.org/10.1016/j.bbalip.2015.02.007] [PMID: 25701718]
[11]
Matsushita, S.; Masaki, N.; Sato, K.; Hayasaka, T.; Sugiyama, E.; Hui, S.P.; Chiba, H.; Mase, N.; Setou, M. Selective improvement of peptides imaging on tissue by supercritical fluid wash of lipids for matrix-assisted laser desorption/ionization mass spectrometry. Anal. Bioanal. Chem., 2017, 409(6), 1475-1480.
[http://dx.doi.org/10.1007/s00216-016-0119-3] [PMID: 27942804]
[12]
Ong, T.H.; Romanova, E.V.; Roberts-Galbraith, R.H.; Yang, N.; Zimmerman, T.A.; Collins, J.J., III; Lee, J.E.; Kelleher, N.L.; Newmark, P.A.; Sweedler, J.V. Mass Spectrometry Imaging and Identification of Peptides Associated with Cephalic Ganglia Regeneration in Schmidtea mediterranea. J. Biol. Chem., 2016, 291(15), 8109-8120.
[http://dx.doi.org/10.1074/jbc.M115.709196] [PMID: 26884331]
[13]
Rešetar Maslov, D.; Svirkova, A.; Allmaier, G.; Marchetti-Deschamann, M.; Kraljević Pavelić, S. Optimization of MALDI-TOF mass spectrometry imaging for the visualization and comparison of peptide distributions in dry-cured ham muscle fibers. Food Chem., 2019, 283, 275-286.
[http://dx.doi.org/10.1016/j.foodchem.2018.12.126] [PMID: 30722871]
[14]
van Remoortere, A.; van Zeijl, R.J.; van den Oever, N.; Franck, J.; Longuespée, R.; Wisztorski, M.; Salzet, M.; Deelder, A.M.; Fournier, I.; McDonnell, L.A. MALDI imaging and profiling MS of higher mass proteins from tissue. J. Am. Soc. Mass Spectrom., 2010, 21(11), 1922-1929.
[http://dx.doi.org/10.1016/j.jasms.2010.07.011] [PMID: 20829063]
[15]
Yang, J.; Caprioli, R.M. Matrix sublimation/recrystallization for imaging proteins by mass spectrometry at high spatial resolution. Anal. Chem., 2011, 83(14), 5728-5734.
[http://dx.doi.org/10.1021/ac200998a] [PMID: 21639088]
[16]
Buchberger, A.R.; Vu, N.Q.; Johnson, J.; DeLaney, K.; Li, L. A Simple and Effective Sample Preparation Strategy for MALDI-MS Imaging of Neuropeptide Changes in the Crustacean Brain Due to Hypoxia and Hypercapnia Stress. J. Am. Soc. Mass Spectrom., 2020, 31(5), 1058-1065.
[http://dx.doi.org/10.1021/jasms.9b00107] [PMID: 32150406]
[17]
Ogrinc Potočnik, N.; Fisher, G.L.; Prop, A.; Heeren, R.M.A. Sequencing and Identification of Endogenous Neuropeptides with Matrix-Enhanced Secondary Ion Mass Spectrometry Tandem Mass Spectrometry. Anal. Chem., 2017, 89(16), 8223-8227.
[http://dx.doi.org/10.1021/acs.analchem.7b02573] [PMID: 28753276]
[18]
Sui, P.; Watanabe, H.; Artemenko, K.; Sun, W.; Bakalkin, G.; Andersson, M.; Bergquist, J. Neuropeptide imaging in rat spinal cord with MALDI-TOF MS: Method development for the application in pain-related disease studies. Eur. J. Mass Spectrom., 2017, 23(3), 105-115.
[http://dx.doi.org/10.1177/1469066717703272] [PMID: 28657437]
[19]
Hulme, H.; Fridjonsdottir, E.; Gunnarsdottir, H.; Vallianatou, T.; Zhang, X.; Wadensten, H.; Shariatgorji, R.; Nilsson, A.; Bezard, E.; Svenningsson, P.; Andrén, P.E. Simultaneous mass spectrometry imaging of multiple neuropeptides in the brain and alterations induced by experimental parkinsonism and L-DOPA therapy. Neurobiol. Dis., 2020, 137, 104738.
[http://dx.doi.org/10.1016/j.nbd.2020.104738] [PMID: 31927144]
[20]
Reglodi, D.; Jungling, A.; Longuespée, R.; Kriegsmann, J.; Casadonte, R.; Kriegsmann, M.; Juhasz, T.; Bardosi, S.; Tamas, A.; Fulop, B.D.; Kovacs, K.; Nagy, Z.; Sparks, J.; Miseta, A.; Mazzucchelli, G.; Hashimoto, H.; Bardosi, A. Accelerated pre-senile systemic amyloidosis in PACAP knockout mice - a protective role of PACAP in age-related degenerative processes. J. Pathol., 2018, 245(4), 478-490.
[http://dx.doi.org/10.1002/path.5100] [PMID: 29774542]
[21]
Paine, M.R.L.; Ellis, S.R.; Maloney, D.; Heeren, R.M.A.; Verhaert, P.D.E.M. Digestion-Free Analysis of Peptides from 30-year-old Formalin-Fixed, Paraffin-Embedded Tissue by Mass Spectrometry Imaging. Anal. Chem., 2018, 90(15), 9272-9280.
[http://dx.doi.org/10.1021/acs.analchem.8b01838] [PMID: 29975508]
[22]
Vos, D.R.N.; Bowman, A.P.; Heeren, R.M.A.; Balluff, B.; Ellis, S.R. Class-specific depletion of lipid ion signals in tissues upon formalin fixation. Int. J. Mass Spectrom., 2019, 446, 116212.
[http://dx.doi.org/10.1016/j.ijms.2019.116212]
[23]
Yang, N.; Anapindi, K.D.B.; Romanova, E.V.; Rubakhin, S.S.; Sweedler, J.V. Improved identification and quantitation of mature endogenous peptides in the rodent hypothalamus using a rapid conductive sample heating system. Analyst (Lond.), 2017, 142(23), 4476-4485.
[http://dx.doi.org/10.1039/C7AN01358B] [PMID: 29098220]
[24]
He, M.; Stoevesandt, O. In Situ Biosynthesis of Peptide Arrays.Peptidomics: Methods and Protocols. Soloviev, M., Ed.; Humana Press: Totowa, NJ; , 2010, pp. pp 345-356.
[http://dx.doi.org/10.1007/978-1-60761-535-4_24]
[25]
Goodwin, R.J.A.; Nilsson, A.; Borg, D.; Langridge-Smith, P.R.R.; Harrison, D.J.; Mackay, C.L.; Iverson, S.L.; Andrén, P.E. Conductive carbon tape used for support and mounting of both whole animal and fragile heat-treated tissue sections for MALDI MS imaging and quantitation. J. Proteomics, 2012, 75(16), 4912-4920.
[http://dx.doi.org/10.1016/j.jprot.2012.07.006] [PMID: 22796569]
[26]
Griffiths, R.L.; Simmonds, A.L.; Swales, J.G.; Goodwin, R.J.A.; Cooper, H.J. LESA MS Imaging of Heat-Preserved and Frozen Tissue: Benefits of Multistep Static FAIMS. Anal. Chem., 2018, 90(22), 13306-13314.
[http://dx.doi.org/10.1021/acs.analchem.8b02739] [PMID: 30350618]
[27]
Smolira, A.; Wessely-Szponder, J. Importance of the matrix and the matrix/sample ratio in MALDI-TOF-MS analysis of cathelicidins obtained from porcine neutrophils. Appl. Biochem. Biotechnol., 2015, 175(4), 2050-2065.
[http://dx.doi.org/10.1007/s12010-014-1405-1] [PMID: 25432341]
[28]
Shariatgorji, M.; Nilsson, A.; Källback, P.; Karlsson, O.; Zhang, X.; Svenningsson, P.; Andren, P.E. Pyrylium Salts as Reactive Matrices for MALDI-MS Imaging of Biologically Active Primary Amines. J. Am. Soc. Mass Spectrom., 2015, 26(6), 934-939.
[http://dx.doi.org/10.1007/s13361-015-1119-9] [PMID: 25821050]
[29]
Chen, B.; OuYang, C.; Tian, Z.; Xu, M.; Li, L. A high resolution atmospheric pressure matrix-assisted laser desorption/ionization-quadrupole-orbitrap MS platform enables in situ analysis of biomolecules by multi-mode ionization and acquisition. Anal. Chim. Acta, 2018, 1007, 16-25.
[http://dx.doi.org/10.1016/j.aca.2017.12.045] [PMID: 29405984]
[30]
Li, G.; Cao, Q.; Liu, Y.; DeLaney, K.; Tian, Z.; Moskovets, E.; Li, L. Characterizing and alleviating ion suppression effects in atmospheric pressure matrix-assisted laser desorption/ionization. Rapid Commun. Mass Spectrom., 2019, 33(4), 327-335.
[http://dx.doi.org/10.1002/rcm.8358] [PMID: 30430670]
[31]
Li, G.; Ma, F.; Cao, Q.; Zheng, Z.; DeLaney, K.; Liu, R.; Li, L. Nanosecond photochemically promoted click chemistry for enhanced neuropeptide visualization and rapid protein labeling. Nat. Commun., 2019, 10(1), 4697.
[http://dx.doi.org/10.1038/s41467-019-12548-0] [PMID: 31619683]
[32]
DeLaney, K.; Li, L. Capillary electrophoresis coupled to MALDI mass spectrometry imaging with large volume sample stacking injection for improved coverage of C. borealis neuropeptidome. Analyst (Lond.), 2019, 145(1), 61-69.
[http://dx.doi.org/10.1039/C9AN01883B] [PMID: 31723949]
[33]
Lamont, L.; Baumert, M.; Ogrinc Potočnik, N.; Allen, M.; Vreeken, R.; Heeren, R.M.A.; Porta, T. Integration of Ion Mobility MSE after Fully Automated, Online, High-Resolution Liquid Extraction Surface Analysis Micro-Liquid Chromatography. Anal. Chem., 2017, 89(20), 11143-11150.
[http://dx.doi.org/10.1021/acs.analchem.7b03512] [PMID: 28945354]
[34]
Zhang, Y.; DeLaney, K.; Hui, L.; Wang, J.; Sturm, R.M.; Li, L. A Multifaceted Mass Spectrometric Method to Probe Feeding Related Neuropeptide Changes in Callinectes sapidus and Carcinus maenas. J. Am. Soc. Mass Spectrom., 2018, 29(5), 948-960.
[http://dx.doi.org/10.1007/s13361-017-1888-4] [PMID: 29435768]
[35]
Ly, A.; Ragionieri, L.; Liessem, S.; Becker, M.; Deininger, S-O.; Neupert, S.; Predel, R. Enhanced Coverage of Insect Neuropeptides in Tissue Sections by an Optimized Mass-Spectrometry-Imaging Protocol. Anal. Chem., 2019, 91(3), 1980-1988.
[http://dx.doi.org/10.1021/acs.analchem.8b04304] [PMID: 30605313]
[36]
Zimmerman, T.A.; Rubakhin, S.S.; Romanova, E.V.; Tucker, K.R.; Sweedler, J.V. MALDI mass spectrometric imaging using the stretched sample method to reveal neuropeptide distributions in aplysia nervous tissue. Anal. Chem., 2009, 81(22), 9402-9409.
[http://dx.doi.org/10.1021/ac901820v] [PMID: 19835365]
[37]
Zimmerman, T.A.; Rubakhin, S.S.; Sweedler, J.V. Mass spectrometry imaging using the stretched sample approach. Methods Mol. Biol., 2010, 656, 465-479.
[http://dx.doi.org/10.1007/978-1-60761-746-4_27] [PMID: 20680608]
[38]
Zimmerman, T.A.; Rubakhin, S.S.; Sweedler, J.V. MALDI mass spectrometry imaging of neuronal cell cultures. J. Am. Soc. Mass Spectrom., 2011, 22(5), 828-836.
[http://dx.doi.org/10.1007/s13361-011-0111-2] [PMID: 21472517]
[39]
Monroe, E.B.; Jurchen, J.C.; Koszczuk, B.A.; Losh, J.L.; Rubakhin, S.S.; Sweedler, J.V. Massively parallel sample preparation for the MALDI MS analyses of tissues. Anal. Chem., 2006, 78(19), 6826-6832.
[http://dx.doi.org/10.1021/ac060652r] [PMID: 17007502]
[40]
Zhong, M.; Lee, C.Y.; Croushore, C.A.; Sweedler, J.V. Label-free quantitation of peptide release from neurons in a microfluidic device with mass spectrometry imaging. Lab Chip, 2012, 12(11), 2037-2045.
[http://dx.doi.org/10.1039/c2lc21085a] [PMID: 22508372]
[41]
Jo, K.; Heien, M.L.; Thompson, L.B.; Zhong, M.; Nuzzo, R.G.; Sweedler, J.V. Mass spectrometric imaging of peptide release from neuronal cells within microfluidic devices. Lab Chip, 2007, 7(11), 1454-1460.
[http://dx.doi.org/10.1039/b706940e] [PMID: 17960271]
[42]
Haes, W.; Sinay, E.; Detienne, G.; Temmerman, L.; Schoofs, L.; Boonen, K. Functional neuropeptidomics in invertebrates. Biochim. Biophys. Acta Proteins Proteom., 2014, 1854, 812-826.
[43]
Yew, J.Y.; Kutz, K.K.; Dikler, S.; Messinger, L.; Li, L.; Stretton, A.O. Mass spectrometric map of neuropeptide expression in Ascaris suum. J. Comp. Neurol., 2005, 488(4), 396-413.
[http://dx.doi.org/10.1002/cne.20587] [PMID: 15973679]
[44]
Ye, H.; Hui, L.; Kellersberger, K.; Li, L. Mapping of neuropeptides in the crustacean stomatogastric nervous system by imaging mass spectrometry. J. Am. Soc. Mass Spectrom., 2013, 24(1), 134-147.
[http://dx.doi.org/10.1007/s13361-012-0502-z] [PMID: 23192703]
[45]
DeKeyser, S.S.; Kutz-Naber, K.K.; Schmidt, J.J.; Barrett-Wilt, G.A.; Li, L. Imaging mass spectrometry of neuropeptides in decapod crustacean neuronal tissues. J. Proteome Res., 2007, 6(5), 1782-1791.
[http://dx.doi.org/10.1021/pr060603v] [PMID: 17381149]
[46]
Chen, R.; Hui, L.; Sturm, R.M.; Li, L. Three dimensional mapping of neuropeptides and lipids in crustacean brain by mass spectral imaging. J. Am. Soc. Mass Spectrom., 2009, 20(6), 1068-1077.
[http://dx.doi.org/10.1016/j.jasms.2009.01.017] [PMID: 19264504]
[47]
Chen, R.; Hui, L.; Cape, S.S.; Wang, J.; Li, L. Comparative Neuropeptidomic Analysis of Food Intake via a Multi-faceted Mass Spectrometric Approach. ACS Chem. Neurosci., 2010, 1(3), 204-214.
[http://dx.doi.org/10.1021/cn900028s] [PMID: 20368756]
[48]
Adams, M.D.; Celniker, S.E.; Holt, R.A.; Evans, C.A.; Gocayne, J.D.; Amanatides, P.G.; Scherer, S.E.; Li, P.W.; Hoskins, R.A.; Galle, R.F.; George, R.A.; Lewis, S.E.; Richards, S.; Ashburner, M.; Henderson, S.N.; Sutton, G.G.; Wortman, J.R.; Yandell, M.D.; Zhang, Q.; Chen, L.X.; Brandon, R.C.; Rogers, Y.H.; Blazej, R.G.; Champe, M.; Pfeiffer, B.D.; Wan, K.H.; Doyle, C.; Baxter, E.G.; Helt, G.; Nelson, C.R.; Gabor, G.L.; Abril, J.F.; Agbayani, A.; An, H.J.; Andrews-Pfannkoch, C.; Baldwin, D.; Ballew, R.M.; Basu, A.; Baxendale, J.; Bayraktaroglu, L.; Beasley, E.M.; Beeson, K.Y.; Benos, P.V.; Berman, B.P.; Bhandari, D.; Bolshakov, S.; Borkova, D.; Botchan, M.R.; Bouck, J.; Brokstein, P.; Brottier, P.; Burtis, K.C.; Busam, D.A.; Butler, H.; Cadieu, E.; Center, A.; Chandra, I.; Cherry, J.M.; Cawley, S.; Dahlke, C.; Davenport, L.B.; Davies, P.; de Pablos, B.; Delcher, A.; Deng, Z.; Mays, A.D.; Dew, I.; Dietz, S.M.; Dodson, K.; Doup, L.E.; Downes, M.; Dugan-Rocha, S.; Dunkov, B.C.; Dunn, P.; Durbin, K.J.; Evangelista, C.C.; Ferraz, C.; Ferriera, S.; Fleischmann, W.; Fosler, C.; Gabrielian, A.E.; Garg, N.S.; Gelbart, W.M.; Glasser, K.; Glodek, A.; Gong, F.; Gorrell, J.H.; Gu, Z.; Guan, P.; Harris, M.; Harris, N.L.; Harvey, D.; Heiman, T.J.; Hernandez, J.R.; Houck, J.; Hostin, D.; Houston, K.A.; Howland, T.J.; Wei, M.H.; Ibegwam, C.; Jalali, M.; Kalush, F.; Karpen, G.H.; Ke, Z.; Kennison, J.A.; Ketchum, K.A.; Kimmel, B.E.; Kodira, C.D.; Kraft, C.; Kravitz, S.; Kulp, D.; Lai, Z.; Lasko, P.; Lei, Y.; Levitsky, A.A.; Li, J.; Li, Z.; Liang, Y.; Lin, X.; Liu, X.; Mattei, B.; McIntosh, T.C.; McLeod, M.P.; McPherson, D.; Merkulov, G.; Milshina, N.V.; Mobarry, C.; Morris, J.; Moshrefi, A.; Mount, S.M.; Moy, M.; Murphy, B.; Murphy, L.; Muzny, D.M.; Nelson, D.L.; Nelson, D.R.; Nelson, K.A.; Nixon, K.; Nusskern, D.R.; Pacleb, J.M.; Palazzolo, M.; Pittman, G.S.; Pan, S.; Pollard, J.; Puri, V.; Reese, M.G.; Reinert, K.; Remington, K.; Saunders, R.D.; Scheeler, F.; Shen, H.; Shue, B.C.; Sidén-Kiamos, I.; Simpson, M.; Skupski, M.P.; Smith, T.; Spier, E.; Spradling, A.C.; Stapleton, M.; Strong, R.; Sun, E.; Svirskas, R.; Tector, C.; Turner, R.; Venter, E.; Wang, A.H.; Wang, X.; Wang, Z.Y.; Wassarman, D.A.; Weinstock, G.M.; Weissenbach, J.; Williams, S.M.; WoodageT, ; Worley, K.C.; Wu, D.; Yang, S.; Yao, Q.A.; Ye, J.; Yeh, R.F.; Zaveri, J.S.; Zhan, M.; Zhang, G.; Zhao, Q.; Zheng, L.; Zheng, X.H.; Zhong, F.N.; Zhong, W.; Zhou, X.; Zhu, S.; Zhu, X.; Smith, H.O.; Gibbs, R.A.; Myers, E.W.; Rubin, G.M.; Venter, J.C. The genome sequence of Drosophila melanogaster. Science, 2000, 287(5461), 2185-2195.
[http://dx.doi.org/10.1126/science.287.5461.2185] [PMID: 10731132]
[49]
Enomoto, Y.; Nt An, P.; Yamaguchi, M.; Fukusaki, E.; Shimma, S. Mass Spectrometric Imaging of GABA in the Drosophila melanogaster Adult Head. Anal. Sci., 2018, 34(9), 1055-1059.
[http://dx.doi.org/10.2116/analsci.18SCN01] [PMID: 30058603]
[50]
Zhong, Y.; Shobo, A.; Hancock, M.A.; Multhaup, G. Label-free distribution of anti-amyloid D-AIP in Drosophila melanogaster: prevention of Aβ42-induced toxicity without side effects in transgenic flies. J. Neurochem., 2019, 150(1), 74-87.
[http://dx.doi.org/10.1111/jnc.14720] [PMID: 31077378]
[51]
Khalil, S.M.; Pretzel, J.; Becker, K.; Spengler, B. High-resolution AP-SMALDI mass spectrometry imaging of Drosophila melanogaster. Int. J. Mass Spectrom., 2017, 416, 1-19.
[http://dx.doi.org/10.1016/j.ijms.2017.04.001]
[52]
Pratavieira, M.; Menegasso, A.R.D.S.; Esteves, F.G.; Sato, K.U.; Malaspina, O.; Palma, M.S. MALDI Imaging Analysis of Neuropeptides in Africanized Honeybee ( Apis mellifera) Brain: Effect of Aggressiveness. J. Proteome Res., 2018, 17(7), 2358-2369.
[http://dx.doi.org/10.1021/acs.jproteome.8b00098] [PMID: 29775065]
[53]
Pratavieira, M.; da Silva Menegasso, A.R.; Garcia, A.M.C.; Dos Santos, D.S.; Gomes, P.C.; Malaspina, O.; Palma, M.S. MALDI imaging analysis of neuropeptides in the Africanized honeybee (Apis mellifera) brain: effect of ontogeny. J. Proteome Res., 2014, 13(6), 3054-3064.
[http://dx.doi.org/10.1021/pr500224b] [PMID: 24742365]
[54]
Herbert, Z.; Rauser, S.; Williams, L.; Kapan, N.; Güntner, M.; Walch, A.; Boyan, G. Developmental expression of neuromodulators in the central complex of the grasshopper Schistocerca gregaria. J. Morphol., 2010, 271(12), 1509-1526.
[http://dx.doi.org/10.1002/jmor.10895] [PMID: 20960464]
[55]
Verhaert, P.D.; Pinkse, M.W.; Strupat, K.; Conaway, M.C. Imaging of similar mass neuropeptides in neuronal tissue by enhanced resolution MALDI MS with an ion trap - Orbitrap hybrid instrument. Methods Mol. Biol., 2010, 656, 433-449.
[http://dx.doi.org/10.1007/978-1-60761-746-4_25] [PMID: 20680606]
[56]
Hanrieder, J.; Ljungdahl, A.; Fälth, M.; Mammo, S. E.; Bergquist, J.; Andersson, M. L-DOPA-induced dyskinesia is associated with regional increase of striatal dynorphin peptides as elucidated by imaging mass spectrometry. Mol. Cell. Proteomics, 2011, 10(10), M111.009308.
[57]
Minerva, L.; Boonen, K.; Menschaert, G.; Landuyt, B.; Baggerman, G.; Arckens, L. Linking mass spectrometric imaging and traditional peptidomics: a validation in the obese mouse model. Anal. Chem., 2011, 83(20), 7682-7691.
[http://dx.doi.org/10.1021/ac200888j] [PMID: 21913672]
[58]
Ikegawa, M.; Nirasawa, T.; Kakuda, N.; Miyasaka, T.; Kuzuhara, Y.; Murayama, S.; Ihara, Y. Visualization of Amyloid β Deposits in the Human Brain with Matrix-assisted Laser Desorption/Ionization Imaging Mass Spectrometry. J. Vis. Exp., 2019, 145, e57645.
[59]
González de San Román, E.; Bidmon, H-J.; Malisic, M.; Susnea, I.; Küppers, A.; Hübbers, R.; Wree, A.; Nischwitz, V.; Amunts, K.; Huesgen, P.F. Molecular composition of the human primary visual cortex profiled by multimodal mass spectrometry imaging. Brain Struct. Funct., 2018, 223(6), 2767-2783.
[http://dx.doi.org/10.1007/s00429-018-1660-y] [PMID: 29633039]
[60]
Bivehed, E.; Strömvall, R.; Bergquist, J.; Bakalkin, G.; Andersson, M. Region-specific bioconversion of dynorphin neuropeptide detected by in situ histochemistry and MALDI imaging mass spectrometry. Peptides, 2017, 87, 20-27.
[http://dx.doi.org/10.1016/j.peptides.2016.11.006] [PMID: 27840228]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 22
ISSUE: 2
Year: 2021
Published on: 15 November, 2020
Page: [158 - 169]
Pages: 12
DOI: 10.2174/1389203721666201116115708
Price: $65

Article Metrics

PDF: 32
HTML: 2