LptA assembles into rod-like oligomers involving disorder-to-order transitions

Journal of the American Society for Mass Spectrometry

Volumn 24, Issue 10, 2013, Pages 1593-1602

  Santambrogio, Carlo ^a   Sperandeo, Paola ^a   Villa, Riccardo ^b   Sobott, Frank ^c   Polissi, Alessandra ^a   Grandori, Rita ^a  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Circular dichroism; Electrospray ionization ion mobility mass spectrometry; Gram negative bacteria; Induced folding; Lipopolysaccharide; Lpt machinery

Indexed keywords

CONCENTRATION DEPENDENCE; CONFORMATIONAL CHANGE; CONFORMATIONAL STABILITIES; ELECTROSPRAYS; GRAM-NEGATIVE BACTERIA; INDUCED FOLDING; ION MOBILITY-MASS SPECTROMETRY; LIPOPOLYSACCHARIDES;

BACTERIA; DICHROISM; ELECTROSPRAY IONIZATION; MACHINERY; MASS SPECTROMETRY; OLIGOMERIZATION; OLIGOMERS; PROTEINS;

ORDER DISORDER TRANSITIONS;

ESCHERICHIA COLI LIPOPOLYSACCHARIDE; OLIGOMER; PERIPLASMIC PROTEIN; PROTEIN LPTA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL MEMBRANE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; COMPARATIVE STUDY; COMPLEX FORMATION; CONCENTRATION (PARAMETERS); CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DISORDER TO ORDER TRANSITION; ELECTROSPRAY MASS SPECTROMETRY; IN VITRO STUDY; ION MOBILITY SPECTROMETRY; MEMBRANE TRANSPORT; MOLECULAR DYNAMICS; NONHUMAN; OLIGOMERIZATION; PH; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; STOICHIOMETRY; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; THERMAL DENATURATION; THERMOSTABILITY;

CARRIER PROTEINS; CIRCULAR DICHROISM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROGEN-ION CONCENTRATION; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN FOLDING; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TEMPERATURE;

EID: 84884562035     PISSN: 10440305     EISSN: 18791123     Source Type: Journal    
DOI: 10.1007/s13361-013-0687-9     Document Type: Article

References (47)

1. Silhavy, T.J.; Kahne, D.; Walker, S.: The bacterial cell envelope. Cold Spring Harb. Perspect. Biol. 2, 1-16 (2010)
2. Nikaido, H.: Transport across the bacterial oter membrane. J. Bioenerg. Biomembr 25, 581-589 (1993) (Pubitemid 24012891)
3. Bos, M.P.; Robert, V.; Tommassen, J.: Biogenesis of the Gram-negative bacterial outer membrane. Annu. Rev. Microbiol 61, 191-214 (2007) (Pubitemid 350058206)
4. Nikaido, H.: Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev 67, 593-656 (2003) (Pubitemid 37549772)
5. Raetz, C.R.; Whitfield, C.: Lipopolysaccharide endotoxins. Ann. Rev. Biochem 71, 635-700 (2002) (Pubitemid 34800232)
6. Zhou, Z.; White, K.A.; Polissi, A.; Georgopoulos, C.; Raetz, C.R.: Function of Escherichia coli MsbA, an essential ABC family transporter, in lipid A and phospholipid biosynthesis. J. Biol. Chem 273, 12466-12475 (1998) (Pubitemid 28240620)
7. Sperandeo, P.; Dehò, G.; Polissi, A.: The lipopolysaccharide transport system of Gram-negative bacteria. Biochim. Biophys. Acta 1791, 594-602 (2009)
8. Sperandeo, P.; Villa, R.; Dehò, G.; Polissi, A.: The outer membrane of Gram-negative bacteria: lipopolysaccharide biogenesis and transport. In: Bacterial Membranes: Structural and Molecular Biology. Remaut, H.; Fronzes, R.; Eds; Horizon Scientific Press: in press (2013).
9. Narita, S.; Tokuda, H.: Biochemical characterization of an ABC transporter LptBFGC complex required for the outer membrane sorting of lipopolysaccharides. FEBS Lett 583, 2160-2164 (2009)
10. Sperandeo, P.; Lau, F.K.; Carpentieri, A.; De Castro, C.; Molinaro, A.; Dehò, G.; Silhavy, T.J.; Polissi, A.: Functional analysis of the protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. J. Bacteriol 190, 4460-4469 (2008) (Pubitemid 351898962)
11. Sperandeo, P.; Cescutti, R.; Villa, R.; Di Benedetto, C.; Candia, D.; Dehò, G.; Polissi, A.: Characterization of lptA and lptB, two essential genes implicated in lipopolysaccharide transport to the outer membrane of Escherichia coli. J. Bacteriol 189, 244-253 (2007) (Pubitemid 46036240)
12. Sperandeo, P.; Villa, R.; Martorana, A.M.; Samalikova, M.; Grandori, R.; Dehò, G.; Polissi, A.: New insights into the Lpt machinery for lipopolysaccharide transport to the cell surface: LptA-LptC interaction and LptA stability as sensors of a properly assembled transenvelope complex. J. Bacteriol 193, 1042-1053 (2011)
13. Freinkman, E.; Okuda, S.; Ruiz, N.; Kahne, D.: Regulated assembly of the transenvelope protein complex required for lipopolysaccharide export. Biochemistry 51, 4800-4806 (2012)
14. Chng, S.S.; Gronenberg, L.S.; Kahne, D.: Proteins required for lipopolysaccharide assembly in Escherichia coli form a transenvelope complex. Biochemistry 49, 4565-4567 (2010)
15. Freinkman, E.; Chng, S.S.; Kahne, D.: The complex that inserts lipopolysaccharide into the bacterial outer membrane forms a two-protein plug-and-barrel. Proc. Natl. Acad. Sci. USA 108, 2486-2491 (2011)
16. Suits, M.D.; Sperandeo, P.; Dehò, G.; Polissi, A.; Jia, Z.: Novel structure of the conserved gram-negative lipopolysaccharide transport protein A and mutagenesis analysis. J. Mol. Biol 380, 476-488 (2008)
17. Tran, A.X.; Dong, C.; Whitfield, C.: Structure and functional analysis of LptC, a conserved membrane protein involved in the lipopolysaccharide export pathway in Escherichia coli. J. Biol. Chem 285, 33529-33539 (2010)
18. Tran, A.X.; Trent, M.S.; Whitfield, C.: The LptA protein of Escherichia coli is a periplasmic lipid A-binding protein involved in the lipopolysaccharide export pathway. J. Biol. Chem 283, 20342-20349 (2008)
19. Villa, R.; Martorana, A.M.; Okuda, S.; Gourlay, L.J.; Nardini, M.; Sperandeo, P.; Dehò, G.; Bolognesi, M.; Kahne, D.; Polissi, A.: The Escherichia coli Lpt transenvelope protein complex for lipopolysaccharide export is assembled via conserved structurally homologous domains. J. Bacteriol 195, 1100-1108 (2013)
20. Okuda, S.; Freinkman, E.; Kahne, D.: Cytoplasmic ATP hydrolysis powers transport of lipopolysaccharide across the periplasm in E. coli. Science 338, 1214-1217 (2012)
21. Merten, J.A.; Schultz, K.M.; Klug, C.S.: Concentration-dependent oligomerization and oligomeric arrangement of LptA. Protein Sci 21, 211-218 (2012)
22. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685 (1970)
23. Romero, P.; Obradovic, Z.; Li, X.; Garner, E.C.; Brown, C.J.; Dunker, A.K.: Sequence complexity of disordered protein. Proteins 42, 38-48 (2001)
24. Li, X.; Romero, P.; Rani, M.; Dunker, A.K.; Obradovic, Z.: Predicting protein disorder for N-, C-, and internal regions. Genome Informatics 10, 30-40 (1999)
25. Lesse, A.J.; Campagnari, A.A.; Bittner, W.E.; Apicella, M.A.: Increased resolution of lipopolysaccharides and lipooligosaccharides utilizing tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis. J. Immunol. Methods 126, 109-117 (1990) (Pubitemid 20041434)
26. Hitchcock, P.J.; Brown, T.M.: Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J. Bacteriol 154, 269-277 (1983) (Pubitemid 13115445)
27. Longhi, S.; Lieutaud, P.; Canard, B.: Conformational disorder. Methods Mol. Biol 609, 307-325 (2010)
28. Kaltashov, I.A.; Abzalimov, R.R.: Do ionic charges in ESI MS provide useful information on macromolecular structure? J. Am. Soc. Mass Spectrom 19, 1239-1246 (2008)
29. Grandori, R.; Santambrogio, C.; Brocca, S.; Invernizzi, G.; Lotti, M.: Electrospray-ionization mass spectrometry as a tool for fast screening of protein structural properties. Biotechnol. J 4, 73-87 (2009)
30. Robinson, C.V.; Chung, E.W.; Kragelund, B.B.; Knudsen, J.; Aplin, R.T.; Poulsen, F.M.; Dobson, C.M.: Probing the nature of noncovalent interactions by mass spectrometry. A study of protein-CoA ligand binding and assembly. J. Am. Chem. Soc 118, 8646-8653 (1996) (Pubitemid 26318266)
31. Invernizzi, G.; Grandori, R.: Detection of the equilibrium folding intermediate of beta-lactoglobulin in the presence of trifluoroethanol by mass spectrometry. Rapid Commun. Mass Spectrom 21, 1049-1052 (2007) (Pubitemid 46426827)
32. Kelly, S.M.; Jess, T.J.; Prince, N.C.: How to study proteins by circular dichroism. Biochim. Biophys. Acta 1751, 119-139 (2005) (Pubitemid 41112231)
33. Ngounou Wetie, A.; Sokolowska, I.; Woods, A.G.; Roy, U.; Loo, J.A.; Darie, C.C.: Investigation of stable and transient protein-protein interactions: Past, present, and future. Proteomics 13, 538-557 (2013)
34. Uetrecht, C.; Rose, R.J.; van Duijn, E.; Lorenzen, K.; Heck, A.J.: Ion mobility mass spectrometry of proteins and protein assemblies. Chem. Soc. Rev 39, 1633-1655 (2010)
35. Kaddis, C.S.; Loo, J.A.: Native protein MS and ion mobility large flying proteins with ESI. Anal. Chem 79, 1778-1784 (2007) (Pubitemid 46355204)
36. Ruotolo, B.T.; Benesch, J.L.; Sandercock, A.M.; Hyung, S.J.; Robinson, C.V.: Ion mobility-mass spectrometry analysis of large protein complexes. Nat. Protoc 3, 1139-1152 (2008)
37. Woods, L.A.; Radford, S.E.; Ashcroft, A.E.: Advances in ion mobility spectrometry-mass spectrometry reveal key insights into amyloid assembly. Biochim. Biophys. Acta 1834(6), 1257-1268 (2013)
38. Brocca, S.; Testa, L.; Sobott, F.; Samalikova, M.; Natalello, A.; Papaleo, E.; Lotti, M.; De Gioia, L.; Doglia, S.M.; Alberghina, L.; Grandori, R.: Compaction properties of an intrinsically disordered protein: Sic1 and its kinase-inhibitor domain. Biophys. J 100, 2243-2252 (2011)
39. Konijnenberg, A.; Butterer, A.; Sobott, F.: Native ion mobility-mass spectrometry and related methods in structural biology. Biochim. Biophys. Acta 1834(6), 1239-1256 (2013)
40. Sobott, F.: Characterization of proteins and protein complexes by ion mobility-mass spectrometry. Chemistry Today 29, 20-24 (2011)
41. Jurneczko, E.; Barran, P.E.: How useful is ion mobility mass spectrometry for structural biology? The relationship between protein crystal structures and their collision cross sections in the gas phase. Analyst 136, 20-28 (2011)
42. Smith, D.P.; Radford, S.E.; Ashcroft, A.E.: Elongated oligomers in beta2-microglobulin amyloid assembly revealed by ion mobility spectrometry-mass spectrometry. Proc. Natl. Acad. Sci. USA 107, 6794-6798 (2010)
43. Borysik, A.J.; Robinson, C.V.: The 'sticky business' of cleaning gas-phase membrane proteins: a detergent oriented perspective. Phys. Chem.; Chem. Phys 14, 14439-14449 (2012)
44. Receveur-Brechot, V.; Bourhis, J.M.; Uversky, V.N.; Canard, B.; Longhi, S.: Assessing protein disorder and induced folding. Proteins 62, 24-45 (2006) (Pubitemid 43063003)
45. Tompa, P.: Intrinsically disordered proteins: a 10-year recap. Trends Biochem. Sci 37, 509-516 (2012)
46. Dunker, A.K.; Brown, C.J.; Lawson, J.D.; Iakoucheva, L.M.; Obradovic, Z.: Intrinsic disorder and protein function. Biochemistry 41, 6573-6582 (2002) (Pubitemid 34547347)
47. Melnik, B.S.; Povarnitsyna, T.V.; Glukhov, A.S.; Melnik, T.N.; Sarma, R.H.: SS-stabilizing proteins rationally: intrinsic disorder-based design of stabilizing disulphide bridges in GFP. J. Biomol. Struct. Dyn 29, 815-824 (2012)