Emergence of mass spectrometry detergents for membrane proteomics.


Journal

Analytical and bioanalytical chemistry
ISSN: 1618-2650
Titre abrégé: Anal Bioanal Chem
Pays: Germany
ID NLM: 101134327

Informations de publication

Date de publication:
Jul 2023
Historique:
received: 12 11 2022
accepted: 02 02 2023
revised: 25 01 2023
medline: 10 7 2023
pubmed: 23 2 2023
entrez: 22 2 2023
Statut: ppublish

Résumé

Detergents enable the investigation of membrane proteins by mass spectrometry. Detergent designers aim to improve underlying methodologies and are confronted with the challenge to design detergents with optimal solution and gas-phase properties. Herein, we review literature related to the optimization of detergent chemistry and handling and identify an emerging research direction: the optimization of mass spectrometry detergents for individual applications in mass spectrometry-based membrane proteomics. We provide an overview about qualitative design aspects including their relevance for the optimization of detergents in bottom-up proteomics, top-down proteomics, native mass spectrometry, and Nativeomics. In addition to established design aspects, such as charge, concentration, degradability, detergent removal, and detergent exchange, it becomes apparent that detergent heterogeneity is a promising key driver for innovation. We anticipate that rationalizing the role of detergent structures in membrane proteomics will serve as an enabling step for the analysis of challenging biological systems.

Identifiants

pubmed: 36808272
doi: 10.1007/s00216-023-04584-z
pii: 10.1007/s00216-023-04584-z
pmc: PMC10328889
doi:

Substances chimiques

Detergents 0
Membrane Proteins 0

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

3897-3909

Subventions

Organisme : Ministry of Culture and Science of the State of North Rhine-Westphalia
ID : NRW return program

Informations de copyright

© 2023. The Author(s).

Références

Mann M, Cox J. Is proteomics the new genomics? Cell. 2007:395–8.
Amiri-Dashata N, Kaushki M, Abbaszadeh H-A, Rostami-Nejad M, Rezaei-Tavirani M. Proteomics applications in health: biomarker and drug discovery and food industry. Iran J Pharm Res. 2018;17:1523–36.
Zubarev RA. The challenge of the proteome dynamic range and its implications for in-depth proteomics. Proteomics. 2013;13:723–6.
pubmed: 23307342
Overington JP, Al-Lazikani B, Hopkins AL. How many drug targets are there? Nat Rev Drug Discov. 2006;5:993–6.
pubmed: 17139284
Hauser AS, Attwood MM, Rask-Andersen M, Schiöth HB, Gloriam DE. Trends in GPCR drug discovery: new agents, targets and indications. Nat Rev Drug Discov. 2017;16:829–42.
pubmed: 29075003 pmcid: 6882681
Gulezian E, Crivello C, Bednenko J, Zafra C, Zhang Y, Colussi P, et al. Membrane protein production and formulation for drug discovery. Trends Pharmacol Sci. 2021;42:657–74.
pubmed: 34270922
Rask-Andersen M, Almén MS, Schiöth HB. Trends in the exploitation of novel drug targets. Nat Rev Drug Discov. 2011;10:579–90.
pubmed: 21804595
Speers AE, Wu CC. Proteomics of integral membrane proteins theory and application. Chem Rev. 2007;107:3687–714.
pubmed: 17683161
Savas JN, Stein BD, Wu CC, Yates JR III. Mass spectrometry accelerates membrane protein analysis. Trends Biochem Sci. 2011;36:388–96.
pubmed: 21616670 pmcid: 3222592
Zhang X. Detergents: friends not foes for high-performance membrane proteomics toward precision medicine. Proteomics. 2017;17:1600209.
Garavito RM, Ferguson-Miller S. Detergents as tools in membrane biochemistry. J Biol Chem. 2001;276:32403–6.
pubmed: 11432878
Kelleher NL, Lin HY, Valaskovic GA, Aaserud DJ, Fridriksson EK, McLafferty FW. Top down versus bottom up protein characterization by tandem high-resolution mass spectrometry. J Am Chem Soc. 1999;121:806–12.
Laganowsky A, Reading E, Hopper JTS, Robinson CV. Mass spectrometry of intact membrane protein complexes. Nat Protoc. 2013;8:639–51.
pubmed: 23471109 pmcid: 4058633
Gault J, Liko I, Landreh M, Shutin D, Bolla JR, Jefferies D, et al. Combining native and ‘omics’ mass spectrometry to identify endogenous ligands bound to membrane proteins. Nat Methods. 2020;17:505–8.
pubmed: 32371966 pmcid: 7332344
Bodzon-Kulakowska A, Bierczynska-Krzysik A, Dylag T, Drabik A, Suder P, Noga M, et al. Methods for samples preparation in proteomic research. J Chromatogr B. 2007;849:1–31.
Cherry JD, Zeineddin A, Dammer EB, Webster JA, Duong D, Seyfried NT, et al. Characterization of detergent insoluble proteome in chronic traumatic encephalopathy. J Neuropathol Exp Neurol. 2018;77:40–9.
pubmed: 29145658
Dannenmaier S, Desroches C, Schüler L, Zhang Y, Hummel J, Milanov M, et al. Quantitative proteomics identifies the universally conserved ATPase Ola1p as a positive regulator of heat shock response in Saccharomyces cerevisiae. J Biol Chem. 2021;297:101050.
pubmed: 34571008 pmcid: 8531669
Hendricks JA, Beaton N, Chernobrovkin A, Miele E, Hamza GM, Ricchiuto P, et al. Mechanistic insights into a CDK9 inhibitor via orthogonal proteomics. ACS Chem Biol. 2022;17:54–67.
pubmed: 34955012
Wu Z, Jin Y, Chen B, Gugger MK, Wilkinson-Johnson CL, Tiambeng TN, et al. Comprehensive characterization of the recombinant catalytic subunit of cAMP-dependent protein kinase by top-down mass spectrometry. J Am Soc Mass Spectrom. 2019;30:2561–70.
pubmed: 31792770 pmcid: 6922056
Li Z, Tremmel DM, Ma F, Yu Q, Ma M, Delafield DG, et al. Proteome-wide and matrisome-specific alterations during human pancreas development and maturation. Nat Commun. 2021;12:1020.
pubmed: 33589611 pmcid: 7884717
Gupta K, Donlan JAC, Hopper JTS, Uzdavinys P, Landreh M, Struwe WB, et al. The role of interfacial lipids in stabilizing membrane protein oligomers. Nature. 2017;541:421–4.
pubmed: 28077870 pmcid: 5501331
Oluwole AO, Corey RA, Brown CM, Hernández-Rocamora VM, Stansfeld PJ, Vollmer W, et al. Peptidoglycan biosynthesis is driven by lipid transfer along enzyme-substrate affinity gradients. Nat Commun. 2022;13:2278.
pubmed: 35477938 pmcid: 9046198
Allison TM, Reading E, Liko I, Baldwin AJ, Laganowsky A, Robinson CV. Quantifying the stabilizing effects of protein-ligand interactions in the gas phase. Nat Commun. 2015;6:1–10.
Yen H-Y, Liko I, Gault J, Wu D, Struwe WB, Robinson CV. Correlating glycoforms of DC-SIGN with stability using a combination of enzymatic digestion and ion mobility mass spectrometry. Angew Chem Int Ed. 2020;59:15560–4.
Bolla JR, Sauer JB, Wu D, Mehmood S, Allison TM, Robinson CV. Direct observation of the influence of cardiolipin and antibiotics on lipid II binding to MurJ. Nat Chem. 2018;10:363–71.
pubmed: 29461535 pmcid: 5912511
Patrick JW, Boone CD, Liu W, Conover GM, Liu Y, Cong X, et al. Allostery revealed within lipid binding events to membrane proteins. PNAS. 2018;115:2976–81.
pubmed: 29507234 pmcid: 5866585
Agasid MT, Sørensen L, Urner LH, Yan J, Robinson CV. The effects of sodium ions on ligand binding and conformational states of g protein-coupled receptors-insights from mass spectrometry. J Am Chem Soc. 2021;143:4085–9.
pubmed: 33711230 pmcid: 7995251
Urner LH, Ariamajd A, Weikum A. Combinatorial synthesis enables scalable designer detergents for membrane protein studies. Chem Sci. 2022;13:10299–307.
pubmed: 36277644 pmcid: 9473536
Melby JA, Roberts DS, Larson EJ, Brown KA, Bayne EF, Jin S, et al. Novel strategies to address the challenges in top-down proteomics. J Am Soc Mass Spectrom. 2021;32:1278–94.
pubmed: 33983025 pmcid: 8310706
Zhang N, Li L. Effects of common surfactants on protein digestion and matrix-assisted laser desorption/ionization mass spectrometric analysis of the digested peptides using two-layer sample preparation. Rapid Commun Mass Spectrom. 2004;18:889–96.
pubmed: 15095358
Kachuk C, Doucette AA. The benefits (and misfortunes) of SDS in top-down proteomics. J Proteomics. 2018;175:75–86.
pubmed: 28286130
Kachuk C, Faulkner M, Liu F, Doucette AA. Automated SDS depletion for mass spectrometry of intact membrane proteins though transmembrane electrophoresis. J Proteome Res. 2016;15:2634–42.
pubmed: 27376408
Kachuk C, Stephen K, Doucette A. Comparison of sodium dodecyl sulfate depletion techniques for proteome analysis by mass spectrometry. J Chromatogr A. 2015;1418:158–66.
pubmed: 26422304
Elinger D, Gabashvili A, Levin Y. Suspension trapping (S-Trap) is compatible with typical protein extraction buffers and detergents for bottom-up proteomics. J Proteome Res. 2019;18:1441–5.
pubmed: 30761899
Kim KH, Compton PD, Trans JC, Kelleher NL. Online matrix removal platform for coupling gel-based separations to whole protein electrospray ionization mass spectrometry. J Proteome Res. 2015;14:2199–206.
pubmed: 25836738 pmcid: 4419745
Yu Y-Q, Gilar M, Lee PJ, Bouvier ESP, Gebler JC. Enzyme-friendly, mass spectrometry-compatible surfactant for in-solution enzymatic digestion of proteins. Anal Chem. 2003;75:6023–8.
pubmed: 14588046
Chang Y-H, Gregorich ZR, Chen AJ, Hwang L, Guner H, Yu D, et al. New mass-spectrometry-compatible degradable surfactant for tissue proteomics. J Proteome Res. 2015;14:1587–99.
pubmed: 25589168 pmcid: 4384424
Saveliev SV, Woodroofe CC, Sabat G, Adams CM, Klaubert D, Wood K, et al. Mass spectrometry compatible surfactant for optimized in-gel protein digestion. Anal Chem. 2013;85:907–14.
pubmed: 23256507
Zhang X. Less is more: membrane protein digestion beyond urea–trypsin solution for next-level proteomics. MCP. 2015;14:2441–53.
pubmed: 26081834 pmcid: 4563727
Dapic I, Uwugiaren N, Kers J, Mohammed Y, Goodlett DR, Corthals G. Evaluation of fast and sensitive proteome profiling of FF and FFPE kidney patient tissues. Molecules. 2022;27:1137.
pubmed: 35164409 pmcid: 8838561
Brown KA, Chen B, Guardado-Alvarez TM, Z. L, Hwang L, Ayaz-Guner S, et al. A photocleavable surfactant for top-down proteomics. Nat. Methods. 2019;16:417-20.
Brown KA, Tucholski T, Eken C, Knott S, Zhu Y, Jin S, et al. High-throughput proteomics enabled by a photocleavable surfactant. Angew Chem Int Ed. 2020;59:8406–10.
Brown KA, Gugger MK, Yu Z, Moreno D, Jin S, Ge Y. Nonionic, cleavable surfactant for top-down proteomics. Anal Chem. 2023;95:1801–4.
Liu C, Si X, Yan S, Zhao X, Qian X, Ying W, et al. Development of the C12Im-Cl-assisted method for rapid sample preparation in proteomic application. Anal Methods. 2021;13:776–81.
pubmed: 33492312
Choi J-S, Park YH, Oh JH, Kim S, Kwon J, Choi Y-E. Efficient profiling of detergent-assisted membrane proteome in cyanobacteria. J Apply Phycol. 2020;32:1177–84.
Khanal DD, Tasharofi S, Azizi M, Khaledi MG. Improved protein coverage in bottom-up proteomes analysis using fluoroalcohol-mediated supramolecular biphasic systems with mixed amphiphiles for sample extraction, fractionation, and enrichment. Anal Chem. 2021;93:7430–8.
pubmed: 33970614
Pham MD, Wen T-C, Li H-C, Hsieh P-H, Chen Y-R, Chang H-C, et al. Streamlined membrane proteome preparation for shotgun proteomics analysis with Triton X-100 cloud point extraction and nanodiamond solid phase extraction. Materials. 2016;9: https://doi.org/10.3390/ma9050385 .
Rey M, Mrázek H, Pompach P, Novák P, Pelosi L, Brandolin G, et al. Effective removal of nonionic detergents in protein mass spectrometry, hydrogen/deuterium exchange, and proteomics. Anal Chem. 2010;82:5107–16.
pubmed: 20507168
Brown KA, Tucholski T, Alpert AJ, Eken C, Wesermann L, Kyrvasilis A, et al. Top-down proteomics of endogenous membrane proteins enabled by cloud point enrichment and multidimensional liquid chromatography–mass spectrometry. Anal Chem. 2020;92:15726–35.
pubmed: 33231430 pmcid: 7968110
Barrera NP, Bartolo ND, Booth PJ, Robinson CV. Micelles protect membrane complexes from solution to vacuum. Science. 2008;321:243–6.
pubmed: 18556516
Urner LH. Tailoring purification and analysis of membrane proteins with modular detergents. In: Mus-Veteau I. (eds) Heterologous Expression of Membrane Proteins. Methods in Molecular Biology, vol 2507. New York: Humana, 2022. https://doi.org/10.1007/978-1-0716-2368-8_19 .
Urner LH. Advances in membrane mimetics and mass spectrometry for understanding membrane structure and function. Curr Opin Chem Biol. 2022;69:102157.
Bolla JR, Fiorentino F, Robinson CV. Mass spectrometry informs the structure and dynamics of membrane proteins involved in lipid and drug transport. Curr Opin Struct Biol. 2021;70:53–60.
pubmed: 33964676
Agasid MT. Probing membrane protein–lipid interactions. Curr Opin Chem Biol. 2021;69:78–85.
Tamara S, den Boer MA, Heck AJR. High-resolution native mass spectrometry. Chem Rev. 2022;122:7269–326.
pubmed: 34415162
Marty MT, Hoi KK, Robinson CV. Interfacing membrane mimetics with mass spectrometry. Acc Chem Res. 2016;15:2459–67.
Keener JE, Zhang G, Marty MT. Native mass spectrometry of membrane proteins. Anal Chem. 2021;93:583–97.
pubmed: 33115234
Urner LH, Liko I, Yen H-Y, Hoi KK, Bolla JR, Gault J, et al. Modular detergents tailor the purification and structural analysis of membrane proteins including G-protein coupled receptors. Nat Commun. 2020;11:564.
pubmed: 31992701 pmcid: 6987200
SusaLippensXiaLooCampuzanoWilliams ACJLYJAIDGD. Submicrometer emitter ESI tips for native mass spectrometry of membrane proteins in ionic and nonionic detergents. J Am Soc Mass Spectrom. 2018;29:203–6.
Reading E, Liko I, Allison TM, Benesch JLP, Laganowsky A, Robinson CV. The role of the detergent micelle in preserving the structure of membrane proteins in the gas phase. Angew Chem Int Ed. 2015;54:4577–81.
Yen H-Y, Abramsson ML, Agasid MT, Lama D, Gault J, Liko I, et al. Electrospray ionization of native membrane proteins proceeds via a charge equilibration step. RSC Adv. 2022;12:9671–80.
pubmed: 35424940 pmcid: 8972943
Reading E, Walton TA, Liko I, Marty MT, Laganowsky A, Rees DC, et al. The effect of detergent, temperature, and lipid on the oligomeric state of MscL constructs: insights from mass spectrometry. Chem Biol. 2015;22:593–603.
Umbreit JN, Strominger JL. Relation of detergent HLB number to solubilization and stabilization of D-alanine carboxypeptidase from Bacillus subtilis membranes. PNAS. 1973;70:2997–3001.
pubmed: 4200727 pmcid: 427155
Nji E, Chatzikyriakidou Y, Landreh M, Drew D. An engineered thermal-shift screen reveals specific lipid preferences of eukaryotic and prokaryotic membrane proteins. Nat Commun. 2018;9:4253.
pubmed: 30315156 pmcid: 6185904
Bechara C, Robinson CV. Different modes of lipid binding to membrane proteins probed by mass spectrometry. J Am Chem Soc. 2015;137:5240–7.
pubmed: 25860341
Gupta K, Li J, Liko I, Gault J, Bechara C, Wu D, et al. Identifying key membrane protein lipid interactions using mass spectrometry. Nat Protoc. 2018;13:1106–20.
pubmed: 29700483 pmcid: 6049616
Bolla JR, Corey RA, Sahin S, Gault J, Hummer A, Hopper JTS, et al. A mass-spectrometry-based approach to distinguish annular and specific lipid binding to membrane proteins. Angew Chem Int Ed. 2020;132:3523–28.
Urner LH, Schulze M, Maier YB, Hoffmann W, Warnke S, Liko I, et al. A new azobenzene-based design strategy for detergents in membrane protein research. Chem Sci. 2020;11:3538–46.
pubmed: 34109026 pmcid: 8152689
Urner LH, Mohammadifar E, Ludwig K, Shutin D, Fiorentino F, Liko I, et al. Anionic dendritic polyglycerol for protein purification and delipidation. ACS Appl Polym Mater. 2021;3:5903–11.
Urner LH, Liko I, Pagel K, Haag R, Robinson CV. Non-ionic hybrid detergents for protein delipidation. BBA - Biomembranes. 2022;1864:183958.
pubmed: 35551920
Thota BNS, Urner LH, Haag R. Supramolecular architectures of dendritic amphiphiles in water. Chem Rev. 2015;116:2079–102.
pubmed: 26669418
Guffick C, Hsieh P-Y, Ali A, Shi W, Howard J, Chinthapalli DK, et al. Drug-dependent inhibition of nucleotide hydrolysis in the heterodimeric ABC multidrug transporter PatAB from Streptococcus pneumoniae. FEBS Lett. 2022;289:3770–88.
Kjølbye LR, Sørensen L, Yan J, Berglund NA, Ferkinghoff-Borg J, Robinson CV, et al. Lipid modulation of a class B GPCR: elucidating the modulatory role of PI(4,5)P2 lipids. J Chem Inf Model. 2022: https://doi.org/10.1021/acs.jcim.2c00635 .
Womack MD, Kendall DA, MacDonald RC. Detergent effects on enzyme activity and solubilization of lipid bilayer membranes. BBA Biomembranes. 1983;733:210–5.
pubmed: 6882760
Ilgü H, Jeckelmann J-M, Gachet MS, Boggavarapu R, Ucurum Z, Gertsch J, et al. Variation of the detergent-binding capacity and phospholipid content of membrane proteins when purified in different detergents. Biophys J. 2014;106:1660–70.
pubmed: 24739165 pmcid: 4008799
Bechara C, Nöll A, Morgner N, Degiacomi MT, Tampé R, Robinson CV. A subset of annular lipids is linked to the flippase activity of an ABC transporter. Nat Chem. 2015;7:255–62.
pubmed: 25698336
Urner LH, Maier YB, Haag R, Pagel K. Exploring the potential of dendritic oligoglycerol detergents for protein mass spectrometry. J Am Soc Mass Spectrom. 2019;30:174–80.
pubmed: 30276626
Gobet A, Zampieri V, Magnard S, Pebay-Peyroula E, Falson P, Chaptal V. The non-Newtonian behavior of detergents during concentration is increased by macromolecules, in trans, and results in their over-concentration. Biochimie. 2022: https://doi.org/10.1016/j.biochi.2022.09.004 .
Mehmood S, Marcoux J, Hopper JTS, Allison TM, Liko I, Borysik AJ, et al. Charge reduction stabilizes intact membrane protein complexes for mass spectrometry. J Am Chem Soc. 2014;136:17010–2.
pubmed: 25402655 pmcid: 4594752
Kumar S, Zhu Y, Stover L, Laganowsky A. Step toward probing the nonannular belt of membrane proteins. Anal Chem. 2022;94:13906–12.
pubmed: 36170465
Townsend JA, Keener JE, Miller ZM, Prell JS, Marty MT. Imidazole derivatives improve charge reduction and stabilization for native mass spectrometry. Anal Chem. 2019;91:14765–72.
pubmed: 31638377 pmcid: 6864253
Kaldmäe M, Österlund N, Lianoudaki D, Sahin C, Bergman P, Nyman T, et al. Gas-phase collisions with trimethylamine-N-oxide enable activation-controlled protein ion charge reduction. J Am Soc Mass Spectrom. 2019;30:1385–8.
pubmed: 31286443 pmcid: 6669196
Patrick JW, Laganowsky A. Generation of charge-reduced ions of membrane protein complexes for native ion mobility mass spectrometry studies. J Am Soc Mass Spectrom. 2019: https://doi.org/10.1007/s13361-019-02187-6 .
Gault J, Lianoudaki D, Kaldmäe M, Kronqvist N, Rising A, Johansson J, et al. Mass spectrometry reveals the direct action of a chemical chaperone. J Phys Chem Lett. 2018;9:4082–6.
pubmed: 29975538
Lyu J, Liu Y, McCabe JW, Schrecke S, Fang L, Russell DH, et al. Discovery of potent charge-reducing molecules for native ion mobility mass spectrometry studies. Anal Chem. 2020;92:11242–9.
pubmed: 32672445 pmcid: 8056390
Walker TR, Laganowsky A, Russell DH. Surface activity of amines provides evidence for the combined ESI mechanism of charge reduction for protein complexes. Anal Chem. 2022;94:10824–31.
pubmed: 35862200
Petroff JT, Tong A, Chen LJ, Dekoster GT, Khan F, Abramson J, et al. Charge reduction of membrane proteins in native mass spectrometry using alkali metal acetate salts. Anal Chem. 2020;92:6622–30.
pubmed: 32250604 pmcid: 7275249
Liko I, Hopper JTS, Allison TM, Benesch JLP, Robinson CV. Negative ions enhance survival of membrane protein complexes. J Am Soc Mass Spectrom. 2016;27:1099–104.
pubmed: 27106602 pmcid: 4869745
Chaptal V, Delolme F, Kilburg A, Magnard S, Montigny C, Picard M, et al. Quantification of detergents complexed with membrane proteins. Sci Rep. 2017;7:41751.
pubmed: 28176812 pmcid: 5297245
Kotov V, Bartels K, Veith K, Josts I, Tiruttani Subhramanyam UK, Günther C, et al. High-throughput stability screening for detergent-solubilized membrane proteins. Sci Rep. 2019;9:10379.
pubmed: 31316088 pmcid: 6637136
Yen H-Y, Hopper JT, Liko I, Allison TM, Zhu Y, Wang D, et al. Ligand binding to a G protein-coupled receptor captured in a mass spectrometer. Sci Adv. 2017;3:1–6.
Yen H-Y, Hoi KK, Liko I, Hedger G, Horrel MR, Song W, et al. PtdIns(4,5)P2 stabilizes active states of GPCRs and enhances selectivity of G-protein coupling. Nature. 2018;559:423–7.
pubmed: 29995853 pmcid: 6059376
Yen H-Y, Liko I, Song W, Kapoor P, Almeida F, Toporowska J, et al. Mass spectrometry captures biased signalling and allosteric modulation of a G-protein-coupled receptor. Nat Chem 2022: https://doi.org/10.1038/s41557-022-01041-9 .
Urner LH, Goltsche K, Selent M, Liko I, Schweder M-P, Robinson CV, et al. Dendritic oligoglycerol regioisomer mixtures and their utility for membrane protein research. Chem Eur J. 2021;27:2537–42.
pubmed: 33026114

Auteurs

Jan-Simon Behnke (JS)

Department of Chemistry and Chemical Biology, TU Dortmund University, Otto-Hahn-Str. 6, 44227, Dortmund, Germany.

Leonhard H Urner (LH)

Department of Chemistry and Chemical Biology, TU Dortmund University, Otto-Hahn-Str. 6, 44227, Dortmund, Germany. leonhard.urner@tu-dortmund.de.

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Classifications MeSH