Investigation of membrane penetration depth and interactions of the amino-terminal domain of huntingtin: Refined analysis by tryptophan fluorescence measurement

European Biophysics Journal

Volumn 43, Issue 8-9, 2014, Pages 347-360

  Michalek, Matthias ^a,b   Aisenbrey, Christopher ^a   Bechinger, Burkhard ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITY OF KIEL   (Germany)

Author keywords

Huntington's disease; Lipid anchor; Peptide membrane interaction; REES; Tryptophan emission fluorescence

Indexed keywords

HUNTINGTIN; OLIGOMER; POLYGLUTAMINE; TRYPTOPHAN; NERVE PROTEIN; PEPTIDE FRAGMENT; PROTEIN BINDING;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; FLUORESCENCE ANALYSIS; GEL PERMEATION CHROMATOGRAPHY; HYDROPHOBICITY; LIPID BILAYER; LIPID COMPOSITION; LIPID MEMBRANE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; QUANTITATIVE ANALYSIS; CELL MEMBRANE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; SPECTROFLUOROMETRY;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CELL MEMBRANE; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SPECTROMETRY, FLUORESCENCE; TRYPTOPHAN;

EID: 84906046797     PISSN: 01757571     EISSN: 14321017     Source Type: Journal    
DOI: 10.1007/s00249-014-0966-9     Document Type: Article

References (39)

1. Aisenbrey C, Bechinger B, Grobner G (2008) Macromolecular crowding at membrane interfaces: adsorption and alignment of membrane peptides. J Mol Biol 375:376-385 (Pubitemid 350199664)
2. Atwal RS, Xia J, Pinchev D, Taylor J, Epand RM, Truant R (2007) Huntingtin has a membrane association signal that can modulate huntingtin aggregation, nuclear entry and toxicity. Hum Mol Genet 16:2600-2615 (Pubitemid 47617727)
3. Bechinger B, Kinder R, Helmle M, Vogt TC, Harzer U, Schinzel S (1999) Peptide structural analysis by solid-state NMR spectroscopy. Biopolymers 51:174-190 (Pubitemid 29500936)
4. Bechinger B, Aisenbrey C, Bertani P (2004) The alignment, structure and dynamics of membrane-associated polypeptides by solid-state NMR spectroscopy. Biochim Biophys Acta 1666:190-204 (Pubitemid 39425205)
5. Bolen EJ, Holloway PW (1990) Quenching of tryptophan fluorescence by brominated phospholipid. Biochemistry 29:9638-9643 (Pubitemid 20355212)
6. Chang YC, Ludescher RD (1994) Local conformation of rabbit skeletal myosin rod filaments probed by intrinsic tryptophan fluorescence. Biochemistry 33:2313-2321 (Pubitemid 24099633)
7. Chattopadhyay A, London E (1987) Parallax method for direct measurement of membrane penetration depth utilizing fluorescence quenching by spin-labeled phospholipids. Biochemistry 26:39-45
8. Chattopadhyay A, Rawat SS, Kelkar DA, Ray S, Chakrabarti A (2003) Organization and dynamics of tryptophan residues in erythroid spectrin: novel structural features of denatured spectrin revealed by the wavelength-selective fluorescence approach. Protein Sci 12:2389-2403 (Pubitemid 37310781)
9. Chen S, Wetzel R (2001) Solubilization and disaggregation of polyglutamine peptides. Protein Sci 10:887-891 (Pubitemid 32240515)
10. Christiaens B, Symoens S, Verheyden S, Engelborghs Y, Joliot A, Prochiantz A, Vandekerckhove J, Rosseneu M, Vanloo B (2002) Tryptophan fluorescence study of the interaction of penetratin peptides with model membranes. Eur J Biochem 269:2918-2926 (Pubitemid 34754020)
11. Clayton AH, Sawyer WH (1999) Tryptophan rotamer distributions in amphipathic peptides at a lipid surface. Biophys J 76:3235-3242 (Pubitemid 29269470)
12. Demchenko AP, Ladokhin AS (1988) Red-edge-excitation fluorescence spectroscopy of indole and tryptophan. Eur Biophys J 15:369-379
13. Dubreil L, Compoint JP, Marion D (1997) Interaction of puroindolines with wheat flour polar lipids determines their foaming properties. J Agric Food Chem 45:108-116 (Pubitemid 127485759)
14. Eisenberg D, Schwarz E, Komaromy M, Wall R (1984) Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J Mol Biol 179:125-142 (Pubitemid 16223392)
15. Gawrisch K, Gaede HC, Mihailescu M, White SH (2007) Hydration of POPC bilayers studied by 1H-PFG-MAS-NOESY and neutron diffraction. Eur Biophys J 36:281-291 (Pubitemid 46626216)
16. Ghosh AK, Rukmini R, Chattopadhyay A (1997) Modulation of tryptophan environment in membrane-bound melittin by negatively charged phospholipids: implications in membrane organization and function. Biochemistry 36:14291-14305 (Pubitemid 27509921)
17. Hill AV (1910) The possible effects of the aggregation of the molecules of haemoglobin on its dissociation curves. J Physiol 40:4-7
18. Huster D, Gawrisch K (1999) NOESY NMR crosspeaks between lipid headgroups and hydrocarbon chains: spin diffusion or molecular disorder? J Am Chem Soc 121:1992-1993 (Pubitemid 29132073)
19. Kegel KB, Sapp E, Yoder J, Cuiffo B, Sobin L, Kim YJ, Qin ZH, Hayden MR, Aronin N, Scott DL, Isenberg G, Goldmann WH, DiFiglia M (2005) Huntingtin associates with acidic phospholipids at the plasma membrane. J Biol Chem 280:36464-36473 (Pubitemid 41633920)
20. Ladokhin AS, Wang L, Steggles AW, Malak H, Holloway PW (1993) Fluorescence study of a temperature-induced conversion from the "loose" to the "tight" binding form of membrane-bound cytochrome b5. Biochemistry 32:6951-6956 (Pubitemid 23221627)
21. Macdonald PM, Seelig J (1988) Anion binding to neutral and positively charged lipid membranes. Biochemistry 27:6769-6775
22. McIntosh TJ, Holloway PW (1987) Determination of the depth of bromine atoms in bilayers formed from bromolipid probes. Biochemistry 26:1783-1788 (Pubitemid 17047651)
23. Michalek M, Salnikov ES, Werten S, Bechinger B (2013a) Membrane interactions of the amphipathic amino terminus of huntingtin. Biochemistry 52:847-858
24. Michalek M, Salnikov ES, Bechinger B (2013b) Structure and topology of the huntingtin 1-17 membrane anchor by a combined solution and solid-state NMR approach. Biophys J 105:699-710
25. Mosior M, McLaughlin S (1991) Peptides that mimic the pseudosubstrate region of protein kinase C bind to acidic lipids in membranes. Biophys J 60:149-159
26. Mosior M, McLaughlin S (1992) Binding of basic peptides to acidic lipids in membranes: effects of inserting alanine(s) between the basic residues. Biochemistry 31:1767-1773
27. Orr AL, Li S, Wang CE, Li H, Wang J, Rong J, Xu X, Mastroberardino PG, Greenamyre JT, Li XJ (2008) N-terminal mutant huntingtin associates with mitochondria and impairs mitochondrial trafficking. J Neurosci 28:2783-2792 (Pubitemid 351398886)
28. Pan CP, Callis PR, Barkley MD (2006) Dependence of tryptophan emission wavelength on conformation in cyclic hexapeptides. J Phys Chem B 110:7009-7016 (Pubitemid 43672174)
29. Pina DG, Johannes L, Castanho MA (2007) Shiga toxin B-subunit sequential binding to its natural receptor in lipid membranes. Biochim Biophys Acta 1768:628-636 (Pubitemid 46275602)
30. Rhoades E, Ramlall TF, Webb WW, Eliezer D (2006) Quantification of alpha-synuclein binding to lipid vesicles using fluorescence correlation spectroscopy. Biophys J 90:4692-4700 (Pubitemid 43830913)
31. Rockabrand E, Slepko N, Pantalone A, Nukala VN, Kazantsev A, Marsh JL, Sullivan PG, Steffan JS, Sensi SL, Thompson LM (2007) The first 17 amino acids of Huntingtin modulate its sub-cellular localization, aggregation and effects on calcium homeostasis. Hum Mol Genet 16:61-77 (Pubitemid 46156597)
32. Silvestro L, Gupta K, Weiser JN, Axelsen PH (1997) The concentration-dependent membrane activity of cecropin A. Biochemistry 36:11452-11460 (Pubitemid 27408628)
33. Sood R, Domanov Y, Kinnunen PK (2007) Fluorescent temporin B derivative and its binding to liposomes. J Fluoresc 17:223-234 (Pubitemid 46355030)
34. Sreerama N, Woody RW (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem 287:252-260 (Pubitemid 32006234)
35. Tam S, Geller R, Spiess C, Frydman J (2006) The chaperonin TRiC controls polyglutamine aggregation and toxicity through subunit-specific interactions. Nat Cell Biol 8:1155-1162 (Pubitemid 44473612)
36. Tam S, Spiess C, Auyeung W, Joachimiak L, Chen B, Poirier MA, Frydman J (2009) The chaperonin TRiC blocks a huntingtin sequence element that promotes the conformational switch to aggregation. Nat Struct Mol Biol 16:1279-1285
37. Thakur AK, Jayaraman M, Mishra R, Thakur M, Chellgren VM, Byeon IJ, Anjum DH, Kodali R, Creamer TP, Conway JF, Gronenborn AM, Wetzel R (2009) Polyglutamine disruption of the huntingtin exon 1 N terminus triggers a complex aggregation mechanism. Nat Struct Mol Biol 16:380-389
38. Vogt TC, Bechinger B (1999) The interactions of histidine-containing amphipathic helical peptide antibiotics with lipid bilayers. The effects of charges and pH. J Biol Chem 274:29115-29121 (Pubitemid 29477075)
39. Wieprecht T, Apostolov O, Beyermann M, Seelig J (2000) Membrane binding and pore formation of the antibacterial peptide PGLa: thermodynamic and mechanistic aspects. Biochemistry 39:442-452 (Pubitemid 30056480)