Folding and stability of transmembrane β-barrels of bacterial and human origin: Probing underlying similarities and principal differences using in vitro systems

Proceedings of the Indian National Science Academy

Volumn 81, Issue 2, 2015, Pages 463-478

  Mahalakshmi, Radhakrishnan ^a  

^a INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH BHOPAL   (India)

Author keywords

Interactions; Membrane Protein Folding; Outer Membrane Protein; Protein Kinetic Stability; Protein Lipid; Spectroscopy; VDAC

Indexed keywords

BEAM PLASMA INTERACTIONS; BIOLOGICAL MEMBRANES; ESCHERICHIA COLI; SPECTROSCOPY; STABILITY; SYSTEM STABILITY;

FUNCTIONAL CHARACTERIZATION; INTERACTION STRENGTH; MEMBRANE PROTEINS; OUTER MEMBRANE PROTEIN; PROTEIN KINETICS; REVERSIBLE FOLDING; VDAC; VOLTAGE-DEPENDENT ANION CHANNELS;

PROTEINS;

EID: 84957027340     PISSN: 03700046     EISSN: None     Source Type: Journal    
DOI: 10.16943/ptinsa/2015/v81i2/48099     Document Type: Conference Paper

References (63)

1. Anbazhagan V, Vijay N, Kleinschmidt J H and Marsh D (2008) Protein-lipid interactions with Fusobacterium nucleatum major outer membrane protein FomA: spin-label EPR and polarized infrared spectroscopy Biochemistry 47 8414-8423
2. Andersen K K, Wang H and Otzen D E (2012) A kinetic analysis of the folding and unfolding of OmpA in urea and guanidinium chloride: single and parallel pathways Biochemistry 51 8371-8383
3. Andrews B T, Capraro D T, Sulkowska J I, Onuchic J N and Jennings P A (2013) Hysteresis as a Marker for Complex, Overlapping Landscapes in Proteins J Phys Chem Lett 4 180-188
4. Booth P J and Curnow P (2009) Folding scene investigation: membrane proteins Curr Opin Struct Biol 19 8-13
5. Burgess N K, Dao T P, Stanley A M and Fleming K G (2008) Beta-barrel proteins that reside in the Escherichia coli outer membrane in vivo demonstrate varied folding behavior in vitro J Biol Chem 283 26748-26758
6. Chattopadhyay A, Mukherjee S, Rukmini R, Rawat S S and Sudha S (1997) Ionization, partitioning, and dynamics of tryptophan octyl ester: implications for membrane-bound tryptophan residues Biophys J 73 839-849
7. Chaturvedi D and Mahalakshmi R (2013) Methionine mutations of outer membrane protein X influence structural stability and beta-barrel unfolding PLoS One 8 e79351
8. Chaturvedi D and Mahalakshmi R (2014) Juxtamembrane tryptophans have distinct roles in defining the OmpX barrel-micelle boundary and facilitating protein-micelle association FEBS Lett 588 4464-4471
9. Curnow P and Booth P J (2007) Combined kinetic and thermodynamic analysis of alpha-helical membrane protein unfolding Proc Natl Acad Sci U S A 104 18970-18975
10. Durr U H, Gildenberg M and Ramamoorthy A (2012) The magic of bicelles lights up membrane protein structure Chem Rev 112 6054-6074
11. Faham S, Yang D, Bare E, Yohannan S, Whitelegge J P and Bowie J U (2004) Side-chain contributions to membrane protein structure and stability J Mol Biol 335 297-305
12. Fleming K G, Ackerman A L and Engelman D M (1997) The effect of point mutations on the free energy of transmembrane alpha-helix dimerization J Mol Biol 272 266-275
13. Grosse W, Psakis G, Mertins B, Reiss P, Windisch D, Brademann F, Burck J, Ulrich A, Koert U and Essen L O (2014) Structure-based engineering of a minimal porin reveals loopindependent channel closure Biochemistry 53 4826-4838
14. Gupta A, Chaturvedi D and Mahalakshmi R (2012) Modified CNBr cleavage protocol for efficient separation of Met-Ser containing OmpX-Om14 membrane protein fusion International Review of Biophysical Chemistry 3 147-156
15. Gupta A, Zadafiya P and Mahalakshmi R (2014) Differential Contribution of Tryptophans to the Folding and Stability of the Attachment Invasion Locus Transmembrane beta-Barrel from Yersinia pestis Sci Rep 4 6508
16. Gupta A, Iyer B R, Chaturvedi D, Maurya S R and Mahalakshmi R (2015) Thermodynamic, structural and functional properties of membrane protein inclusion bodies are analogous to purified counterparts: Case study from bacteria and humans R Soc Chem Adv 5 1227-1234
17. Hong H and Tamm L K (2004) Elastic coupling of integral membrane protein stability to lipid bilayer forces Proc Natl Acad Sci U S A 101 4065-4070
18. Hong H, Park S, Jimenez R H, Rinehart D and Tamm L K (2007) Role of aromatic side chains in the folding and thermodynamic stability of integral membrane proteins J Am Chem Soc 129 8320-8327
19. Hong H, Rinehart D and Tamm L K (2013) Membrane depthdependent energetic contribution of the tryptophan side chain to the stability of integral membrane proteins Biochemistry 52 4413-4421
20. Huysmans G H, Radford S E, Brockwell D J and Baldwin S A (2007) The N-terminal helix is a post-assembly clamp in the bacterial outer membrane protein PagP J Mol Biol 373 529-540
21. Huysmans G H, Baldwin S A, Brockwell D J and Radford S E (2010) The transition state for folding of an outer membrane protein Proc Natl Acad Sci U S A 107 4099-4104
22. Jefferson R E, Blois T M and Bowie J U (2013) Membrane proteins can have high kinetic stability J Am Chem Soc 135 15183-15190
23. Kelkar D A and Chattopadhyay A (2006) Membrane interfacial localization of aromatic amino acids and membrane protein function J Biosci 31 297-302
24. Khan M A, Neale C, Michaux C, Pomes R, Prive G G, Woody R W and Bishop R E (2007) Gauging a hydrocarbon ruler by an intrinsic exciton probe Biochemistry 46 4565-4579
25. Killian J A and von Heijne G (2000) How proteins adapt to a membrane-water interface Trends Biochem Sci 25 429-434
26. Kleinschmidt J H and Tamm L K (1996) Folding intermediates of a beta-barrel membrane protein. Kinetic evidence for a multi-step membrane insertion mechanism Biochemistry 35 12993-13000
27. Kleinschmidt J H, den Blaauwen T, Driessen A J and Tamm L K (1999a) Outer membrane protein A of Escherichia coli inserts and folds into lipid bilayers by a concerted mechanism Biochemistry 38 5006-5016
28. Kleinschmidt J H and Tamm L K (1999) Time-resolved distance determination by tryptophan fluorescence quenching: probing intermediates in membrane protein folding Biochemistry 38 4996-5005
29. Kleinschmidt J H, Wiener M C and Tamm L K (1999b) Outer membrane protein A of E. coli folds into detergent micelles, but not in the presence of monomeric detergent Protein Sci 8 2065-2071
30. Kleinschmidt J H and Tamm L K (2002) Secondary and tertiary structure formation of the beta-barrel membrane protein OmpA is synchronized and depends on membrane thickness J Mol Biol 324 319-330
31. Kleinschmidt J H (2006) Folding kinetics of the outer membrane proteins OmpA and FomA into phospholipid bilayers Chem Phys Lipids 141 30-47
32. Lella M and Mahalakshmi R (2013) Pro-Gly mediated conformational switch of mycobacteriophage D29 holin transmembrane domain I is lipid concentration driven Chem Commun 49 9594-9596
33. Mahalakshmi R, Raghothama S and Balaram P (2006) NMR analysis of aromatic interactions in designed peptide betahairpins J Am Chem Soc 128 1125-1138
34. Mahalakshmi R, Franzin C M, Choi J and Marassi F M (2007) NMR structural studies of the bacterial outer membrane protein OmpX in oriented lipid bilayer membranes Biochim Biophys Acta 1768 3216-3224
35. Mahalakshmi R and Marassi F M (2008) Orientation of the Escherichia coli outer membrane protein OmpX in phospholipid bilayer membranes determined by solid-State NMR Biochemistry 47 6531-6538
36. Makwana K M, Raghothama S and Mahalakshmi R (2013) Stabilizing effect of electrostatic vs. aromatic interactions in diproline nucleated peptide beta-hairpins Phys Chem Chem Phys 15 15321-15324
37. Makwana K M and Mahalakshmi R (2014a) Asymmetric contribution of aromatic interactions stems from spatial positioning of the interacting aryl pairs in beta-hairpins ChemBioChem 15 2357-2360
38. Makwana K M and Mahalakshmi R (2014b) Comparative analysis of cross strand aromatic-Phe interactions in designed peptide beta-hairpins Org Biomol Chem 12 2053-2061
39. Maurya S R, Chaturvedi D and Mahalakshmi R (2013) Modulating lipid dynamics and membrane fluidity to drive rapid folding of a transmembrane barrel Sci Rep 3 1989
40. Maurya S R and Mahalakshmi R (2013) Modulation of human mitochondrial voltage-dependent anion channel 2 (hVDAC-2) structural stability by cysteine-assisted barrel-lipid interactions J Biol Chem 288 25584-25592
41. Maurya S R and Mahalakshmi R (2014a) Cysteine residues impact the stability and micelle interaction dynamics of the human mitochondrial beta-barrel anion channel hVDAC-2 PLoS One 9 e92183
42. Maurya S R and Mahalakshmi R (2014b) Influence of proteinmicelle ratios and cysteine residues on the kinetic stability and unfolding rates of human mitochondrial VDAC-2 PLoS One 9 e87701
43. Moon C P and Fleming K G (2011) Side-chain hydrophobicity scale derived from transmembrane protein folding into lipid bilayers Proc Natl Acad Sci U S A 108 10174-10177
44. Moon C P, Kwon S and Fleming K G (2011) Overcoming hysteresis to attain reversible equilibrium folding for outer membrane phospholipase A in phospholipid bilayers J Mol Biol 413 484-494
45. Moon C P, Zaccai N R, Fleming P J, Gessmann D and Fleming K G (2013) Membrane protein thermodynamic stability may serve as the energy sink for sorting in the periplasm Proc Natl Acad Sci U S A 110 4285-4290
46. Otzen D E (2002) Protein unfolding in detergents: effect of micelle structure, ionic strength, pH, and temperature Biophys J 83 2219-2230
47. Otzen D E and Oliveberg M (2002) Burst-phase expansion of native protein prior to global unfolding in SDS J Mol Biol 315 1231-1240
48. Otzen D E and Andersen K K (2013) Folding of outer membrane proteins Arch Biochem Biophys 531 34-43
49. Parker M J and Marqusee S (1999) The cooperativity of burst phase reactions explored J Mol Biol 293 1195-1210
50. Plesniak L A, Mahalakshmi R, Rypien C, Yang Y, Racic J and Marassi F M (2011) Expression, refolding, and initial structural characterization of the Y. pestis Ail outer membrane protein in lipids Biochim Biophys Acta 1808 482-489
51. Pocanschi C L, Apell H J, Puntervoll P, Hogh B, Jensen H B, Welte W and Kleinschmidt J H (2006a) The major outer membrane protein of Fusobacterium nucleatum (FomA) folds and inserts into lipid bilayers via parallel folding pathways J Mol Biol 355 548-561
52. Pocanschi C L, Patel G J, Marsh D and Kleinschmidt J H (2006b) Curvature elasticity and refolding of OmpA in large unilamellar vesicles Biophys J 91 L75-77
53. Pocanschi C L, Popot J L and Kleinschmidt J H (2013) Folding and stability of outer membrane protein A (OmpA) from Escherichia coli in an amphipathic polymer, amphipol A8-35 Eur Biophys J 42 103-118
54. Rasmussen A, Rasmussen T, Edwards M D, Schauer D, Schumann U, Miller S and Booth I R (2007) The role of tryptophan residues in the function and stability of the mechanosensitive channel MscS from Escherichia coli Biochemistry 46 10899-10908
55. Sanchez-Ruiz J M (2010) Protein kinetic stability Biophys Chem 148 1-15
56. Sanchez K M, Gable J E, Schlamadinger D E and Kim J E (2008) Effects of tryptophan microenvironment, soluble domain, and vesicle size on the thermodynamics of membrane protein folding: lessons from the transmembrane protein OmpA Biochemistry 47 12844-12852
57. Sanchez K M, Kang G, Wu B and Kim J E (2011) Tryptophanlipid interactions in membrane protein folding probed by ultraviolet resonance Raman and fluorescence spectroscopy Biophys J 100 2121-2130
58. Sehgal P, Mogensen J E and Otzen D E (2005) Using micellar mole fractions to assess membrane protein stability in mixed micelles Biochim Biophys Acta 1716 59-68
59. Sengupta A, Mahalakshmi R, Shamala N and Balaram P (2005) Aromatic interactions in tryptophan-containing peptides: crystal structures of model tryptophan peptides and phenylalanine analogs J Pept Res 65 113-129
60. Shanmugavadivu B, Apell H J, Meins T, Zeth K and Kleinschmidt J H (2007) Correct folding of the beta-barrel of the human membrane protein VDAC requires a lipid bilayer J Mol Biol 368 66-78
61. Stanley A M and Fleming K G (2008) The process of folding proteins into membranes: challenges and progress Arch Biochem Biophys 469 46-66
62. Sun H, Greathouse D V, Andersen O S and Koeppe R E, 2nd (2008) The preference of tryptophan for membrane interfaces: insights from N-methylation of tryptophans in gramicidin channels J Biol Chem 283 22233-22243
63. Yamashita S, Lukacik P, Barnard T J, Noinaj N, Felek S, Tsang T M, Krukonis E S, Hinnebusch B J and Buchanan S K (2011) Structural insights into Ail-mediated adhesion in Yersinia pestis Structure 19 1672-1682.