Intermolecular interactions in biomolecular systems examined by mass spectrometry.

With the development of electrospray and matrix-assisted laser desorption ionization, mass spectrometry (MS) evolved into a powerful tool in the field of biochemistry. Whereas MS is primarily analytical in nature, an increasing number of MS research groups employ the method to address fundamental biochemical questions. Probing the interaction of noncovalently bound molecules in the mass spectrometer is one of the most interesting MS-based experiments possible today, with the potential of making a significant contribution to the basic understanding of the structure and function of biochemical complexes. Here we review a number of current research efforts employing primarily MS techniques to investigate intermolecular interactions in biochemical systems. Examples chosen include the interaction of biomolecules with solvent molecules; interactions between nucleic-acid molecules, in particular, interactions in duplex and quadruplex structures; and interactions between proteins involved in neurodegenerative diseases. Finally we conclude by presenting a few examples of very large biomolecular assemblies in the mega-Dalton range analyzed by MS.

[1]  Marco Fioroni,et al.  Chirally directed formation of nanometer-scale proline clusters. , 2006, Journal of the American Chemical Society.

[2]  E. Pauw,et al.  G-quadruplexes in telomeric repeats are conserved in a solvent-free environment , 2006 .

[3]  Andrij Baumketner,et al.  Structure of the 21–30 fragment of amyloid β‐protein , 2006 .

[4]  H. Wincel Hydration of gas-phase protonated alkylamines, amino acids and dipeptides produced by electrospray , 2006 .

[5]  J. Sessler,et al.  Cyclo[n]pyrroles: size and site-specific binding to G-quadruplexes. , 2006, Journal of the American Chemical Society.

[6]  G. Bitan,et al.  Amyloid β‐protein monomer structure: A computational and experimental study , 2006, Protein science : a publication of the Protein Society.

[7]  M. F. Bush,et al.  Infrared spectroscopy of hydrated amino acids in the gas phase: protonated and lithiated valine. , 2006, Journal of the American Chemical Society.

[8]  R. Cooks,et al.  Serine octamers: cluster formation, reactions, and implications for biomolecule homochirality. , 2006, Angewandte Chemie.

[9]  Peter Roepstorff,et al.  Mass spectrometric analysis of protein interactions. , 2005, Current opinion in chemical biology.

[10]  E. De Pauw,et al.  Ascididemin and meridine stabilise G-quadruplexes and inhibit telomerase in vitro. , 2005, Biochimica et biophysica acta.

[11]  S. Kaufman,et al.  Electrospray ionization mass spectrometry and ion mobility analysis of the 20S proteasome complex , 2005, Journal of the American Society for Mass Spectrometry.

[12]  C. Robinson,et al.  Heptameric (L12)6/L10 rather than canonical pentameric complexes are found by tandem MS of intact ribosomes from thermophilic bacteria. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[13]  R. Heeren,et al.  Monitoring macromolecular complexes involved in the chaperonin-assisted protein folding cycle by mass spectrometry , 2005, Nature Methods.

[14]  M. Bowers,et al.  Structural motifs of DNA complexes in the gas phase , 2005 .

[15]  Michael T. Bowers,et al.  Hydration of small peptides , 2005 .

[16]  G. Bitan,et al.  Amyloid β-protein: Monomer structure and early aggregation states of Aβ42 and its Pro19 alloform , 2005 .

[17]  W. Ens,et al.  Hybrid quadrupole/time-of-flight mass spectrometers for analysis of biomolecules. , 2005, Methods in enzymology.

[18]  M. Baldwin Mass spectrometers for the analysis of biomolecules. , 2005, Methods in enzymology.

[19]  S. A. McLuckey,et al.  Collision-induced dissociation (CID) of peptides and proteins. , 2005, Methods in enzymology.

[20]  K. Breuker The study of protein–ligand interactions by mass spectrometry—a personal view , 2004 .

[21]  Jennifer C. Lee,et al.  α-Synuclein: Stable compact and extended monomeric structures and pH dependence of dimer formation , 2004, Journal of the American Society for Mass Spectrometry.

[22]  G. Hall,et al.  Comparative stability determination of oligonucleotide duplexes in gas and solution phase , 2004, Journal of the American Society for Mass Spectrometry.

[23]  R. Cooks,et al.  Chiral enrichment of serine via formation, dissociation, and soft-landing of octameric cluster ions , 2004, Journal of the American Society for Mass Spectrometry.

[24]  E. Williams,et al.  Binding energies of water to lithiated valine: Formation of solution-phase structure in vacuo , 2004, Journal of the American Society for Mass Spectrometry.

[25]  M. Jarrold,et al.  Water molecule adsorption on short alanine peptides: how short is the shortest gas-phase alanine-based helix? , 2004, Journal of the American Chemical Society.

[26]  C. Robinson,et al.  Protein-Nucleic Acid Interactions and the Expanding Role of Mass Spectrometry* , 2004, Journal of Biological Chemistry.

[27]  R. Dunbar BIRD (blackbody infrared radiative dissociation): evolution, principles, and applications. , 2004, Mass spectrometry reviews.

[28]  C. J. Carpenter,et al.  Investigation of noncovalent interactions in deprotonated peptides: structural and energetic competition between aggregation and hydration. , 2004, Journal of the American Chemical Society.

[29]  J. Straub,et al.  A molecular switch in amyloid assembly: Met35 and amyloid beta-protein oligomerization. , 2003, Journal of the American Chemical Society.

[30]  Shoujun Xu,et al.  Zwitterion formation in hydrated amino acid, dipole bound anions: How many water molecules are required? , 2003 .

[31]  K. Shin‐ya,et al.  Telomestatin-induced stabilization of the human telomeric DNA quadruplex monitored by electrospray mass spectrometry. , 2003, Chemical communications.

[32]  John B Fenn,et al.  Electrospray wings for molecular elephants (Nobel lecture). , 2003, Angewandte Chemie.

[33]  Koichi Tanaka,et al.  The origin of macromolecule ionization by laser irradiation (Nobel lecture). , 2003, Angewandte Chemie.

[34]  A. Yergey,et al.  Hydration of Alkylammonium Ions in the Gas Phase , 2003 .

[35]  T. Wyttenbach,et al.  Gas-Phase Conformations: The Ion Mobility/Ion Chromatography Method , 2003 .

[36]  D. Bohme,et al.  Mass Spectrometric Approaches to Interstellar Chemistry , 2003 .

[37]  M. Kirkitadze,et al.  Amyloid β-protein (Aβ) assembly: Aβ40 and Aβ42 oligomerize through distinct pathways , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[38]  K. J. Koch,et al.  Chiral transmission between amino acids: chirally selective amino acid substitution in the serine octamer as a possible step in homochirogenesis. , 2002, Angewandte Chemie.

[39]  Renato Zenobi,et al.  Quantitative determination of noncovalent binding interactions using soft ionization mass spectrometry , 2002 .

[40]  A. Marshall,et al.  Fourier transform ion cyclotron resonance detection: principles and experimental configurations , 2002 .

[41]  T. Wyttenbach,et al.  Design of a new electrospray ion mobility mass spectrometer , 2001 .

[42]  M. Kirkitadze,et al.  Identification and characterization of key kinetic intermediates in amyloid beta-protein fibrillogenesis. , 2001, Journal of molecular biology.

[43]  K. J. Koch,et al.  Chiroselective self-directed octamerization of serine: implications for homochirogenesis. , 2001, Analytical chemistry.

[44]  P. Hobza,et al.  Potential Energy and Free Energy Surfaces of All Ten Canonical and Methylated Nucleic Acid Base Pairs: Molecular Dynamics and Quantum Chemical ab Initio Studies , 2001 .

[45]  R. Hodyss,et al.  Salt bridge stabilization of charged zwitterionic arginine aggregates in the gas phase. , 2001, Journal of the American Chemical Society.

[46]  Christopher M. Dobson,et al.  Amyloid fibrils from muscle myoglobin , 2001, Nature.

[47]  G. Siuzdak,et al.  Mass Spectrometry of an Intact Virus. , 2001, Angewandte Chemie.

[48]  R. Griffey,et al.  Analysis of noncovalent complexes of DNA and RNA by mass spectrometry. , 2001, Chemical reviews.

[49]  R. Hodyss,et al.  Spontaneous chiral separation in noncovalent molecular clusters. , 2001, Chirality.

[50]  A. Heck,et al.  Detection of intact megaDalton protein assemblies of vanillyl‐alcohol oxidase by mass spectrometry , 2008, Protein science : a publication of the Protein Society.

[51]  P. Kebarle Gas phase ion thermochemistry based on ion-equilibria from the ionosphere to the reactive centers of enzymes , 2000 .

[52]  J. Hajdu,et al.  Electrospray time-of-flight mass spectrometry of the intact MS2 virus capsid , 2000 .

[53]  Michael T. Bowers,et al.  On the Stability of Amino Acid Zwitterions in the Gas Phase: The Influence of Derivatization, Proton Affinity, and Alkali Ion Addition , 2000 .

[54]  P. Schnier,et al.  Dissociation energies of deoxyribose nucleotide dimer anions measured using blackbody infrared radiative dissociation , 1999, Journal of the American Society for Mass Spectrometry.

[55]  A. Viggiano,et al.  Airborne mass spectrometers: four decades of atmospheric and space research at the Air Force research laboratory. , 1999, Journal of mass spectrometry : JMS.

[56]  E. Williams,et al.  Hydration of gas-phase ions formed by electrospray ionization , 1999, Journal of the American Society for Mass Spectrometry.

[57]  C. Robinson,et al.  Detection of the Intact GroEL Chaperonin Assembly by Mass Spectrometry , 1999 .

[58]  M. Jarrold Unfolding, Refolding, and Hydration of Proteins in the Gas Phase , 1999 .

[59]  P. Schnier,et al.  Blackbody infrared radiative dissociation of oligonucleotide anions , 1998, Journal of the American Society for Mass Spectrometry.

[60]  T. Schindler,et al.  FREEZE-DRIED BIOMOLECULES : FT-ICR STUDIES OF THE SPECIFIC SOLVATION OF FUNCTIONAL GROUPS AND CLATHRATE FORMATION OBSERVED BY THE SLOW EVAPORATION OF WATER FROM HYDRATED PEPTIDES AND MODEL COMPOUNDS IN THE GAS PHASE , 1998 .

[61]  P. Schnier,et al.  Activation energies for dissociation of double strand oligonucleotide anions: evidence for watson-crick base pairing in vacuo. , 1998, Journal of the American Chemical Society.

[62]  Richard D. Smith,et al.  New mass spectrometric methods for the study of noncovalent associations of biopolymers , 1997 .

[63]  M. Jarrold,et al.  Hydration of Gas-Phase Proteins: A Special Hydration Site on Gas-Phase BPTI , 1997 .

[64]  David E. Clemmer,et al.  Ion Mobility Measurements and their Applications to Clusters and Biomolecules , 1997 .

[65]  E. Williams,et al.  Hydration of gas-phase gramicidin S (M + 2H)2+ ions formed by electrospray: The transition from solution to gas-phase structure , 1997 .

[66]  M. Jarrold,et al.  HYDRATION OF GAS PHASE PROTEINS : FOLDED +5 AND UNFOLDED +7 CHARGE STATES OF CYTOCHROME C , 1997 .

[67]  P. Schnier,et al.  Binding energies of the proton-bound amino Acid dimers gly.gly, ala.ala, gly.ala, and lys.lys measured by blackbody infrared radiative dissociation. , 1997, The journal of physical chemistry. B.

[68]  J. Loo,et al.  Studying noncovalent protein complexes by electrospray ionization mass spectrometry. , 1997, Mass spectrometry reviews.

[69]  P. Kebarle,et al.  Determination of Ion−Solvent Equilibria in the Gas Phase. Hydration of Diprotonated Diamines and Bis(trimethylammonium) Alkanes , 1996 .

[70]  P. Armentrout,et al.  Gas-Phase Ion Dynamics and Chemistry , 1996 .

[71]  Charles W. Bock,et al.  Calcium Ion Coordination: A Comparison with That of Beryllium, Magnesium, and Zinc , 1996 .

[72]  P. Kebarle,et al.  DETERMINATIONS OF ION-MOLECULE EQUILIBRIA INVOLVING IONS PRODUCED BY ELECTROSPRAY. HYDRATION OF PROTONATED AMINES, DIAMINES, AND SOME SMALL PEPTIDES , 1995 .

[73]  M. Karas,et al.  Analysis of biopolymers by matrix-assisted laser desorption/ionization (MALDI) mass spectrometry , 1994 .

[74]  Michael T. Bowers,et al.  Experimental evidence for the formation of fullerenes by collisional heating of carbon rings in the gas phase , 1993, Nature.

[75]  M. Bowers,et al.  The Nonstatistical Dissociation Dynamics of Cl‐(CH3Br): Evidence for Vibrational Excitation in the Products of Gas‐Phase SN2 Reactions. , 1992 .

[76]  Michael T. Bowers,et al.  The nonstatistical dissociation dynamics of chloride(bromomethane) Cl-(CH3Br): evidence for vibrational excitation in the products of gas-phase SN2 reactions , 1991 .

[77]  D. A. Sullivan,et al.  Gas-Phase Ion and Neutral Thermochemistry , 1988 .

[78]  L. Sukhodub Interactions and Hydration of Nucleic Acid Bases in a Vacuum. Experimental Study , 1987 .

[79]  Joel F. Liebman,et al.  Evaluated Gas Phase Basicities and Proton Affinities of Molecules; Heats of Formation of Protonated Molecules , 1984 .

[80]  N. Burdett,et al.  Hydration of gas-phase ions and the measurement of boundary-layer cooling during flame sampling into a mass spectrometer , 1982 .

[81]  L. Sukhodub,et al.  Experimental studies of molecular interactions between nitrogen bases of nucleic acids , 1979, Biopolymers.

[82]  F. Lovas,et al.  Millimeter wave spectrum of glycine , 1978 .

[83]  J. Storey,et al.  Microwave spectrum and conformation of glycine , 1978 .

[84]  M. Bowers,et al.  Quantitative proton affinities, ionization potentials, and hydrogen affinities of alkylamines , 1976 .

[85]  P. Kebarle,et al.  Hydration of the alkali ions in the gas phase. Enthalpies and entropies of reactions M+(H2O)n-1 + H2O = M+(H2O)n , 1970 .

[86]  Rosalind E. Franklin,et al.  The structure of sodium thymonucleate fibres. I. The influence of water content , 1953 .