Probing conformational stability and dynamics of erythroid and nonerythroid spectrin: Effects of urea and guanidine hydrochloride

PLoS ONE

Volumn 10, Issue 1, 2015, Pages

  Patra, Malay ^a   Mukhopadhyay, Chaitali ^a   Chakrabarti, Abhijit ^b  

^a UNIVERSITY OF CALCUTTA   (India)

^b SAHA INSTITUTE OF NUCLEAR PHYSICS   (India)

Author keywords

[No Author keywords available]

Indexed keywords

8 ANILINO 1 NAPHTHALENESULFONIC ACID; DIMER; GUANIDINE; MONOMER; SPECTRIN; TETRAMER; UREA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISSOCIATION; ERYTHROCYTE GHOST; HYDROGEN BOND; NONHUMAN; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STABILITY; PROTEIN SUBUNIT; PROTEIN TERTIARY STRUCTURE; PROTEIN UNFOLDING; SHEEP; ANIMAL; CHEMISTRY; DRUG EFFECTS; ERYTHROID CELL; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE;

ANIMALS; ERYTHROID CELLS; GUANIDINE; PROTEIN DENATURATION; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; SPECTRIN; UREA;

EID: 84922031922     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0116991     Document Type: Article

References (101)

1. Dobson CM, Karplus M (1999) The fundamentals of protein folding: bringing together theory and experiment. Curr Opin Struc Biol 9: 92-101. PMID: 10047588
2. Dobson CM (2003) Protein folding and misfolding. Nature 426: 884-890. PMID: 14685248
3. Lee CT, Smith KA, Hatton TA (2005) Photocontrol of protein folding: The interaction of photosensitive surfactant with Bovine serum Albumin. Biochemistry 44: 524-536. PMID: 15641777
4. Privalove PL (1996) Intermediates state in protein folding. J Mol Biol 258: 707-725. PMID: 8637003
5. Frink AL, Oberg KA, Seshadri S (1998) Discrete intermediates versus molten globule models for protein folding: characterization of partially folded intermediates of apomyoglobin. Fold Des 3: 19-25. PMID: 9502317
6. Tandford C (1968) Protein Denaturation. Adv Protein Chem 23:121-282. PMID: 4882248
7. Tandford C (1970) Protein Denaturation Part C: Theoretical models for the mechanism of denaturation. Adv Protein Chem 24: 1-95. PMID: 4912353
8. Vanzi F, Madan B, Sharp K (1998) Effect of the Protein Denaturants Urea and Guanidinium on Water Structure: A Structural and Thermodynamic Study. J Am Chem Soc 120: 10748-10753.
9. O'Brien EP, Dima RI, Brooks B, Thirumalai D (2007) Interactions between Hydrophobic and Ionic Solutes in Aqueous Guanidinium Chloride and Urea Solutions: Lessons for Protein Denaturation Mechanism. J Am Chem Soc 129: 7346-7353. PMID: 17503819
10. Ekman D, Bjorklund AK, Frey-Skott J, Elofsson A (2005) Multidomain protein in the kingdom of Life: Orphan Domains and Other Unassigned Regions J Mol Biol 348: 231-243. PMID: 15808866
11. Han JH, Bately S, Nickson AA, Teichmann SA, Clarke J (2007) The folding and evolution of multidomain protein. Nat Rev Mol Cell Biol 8: 319-330. PMID: 17356578
12. Jackson SE (1998) How do small single-domain protein fold. Fol Des 3: R81-R91. PMID: 9710577
13. Batey S, Randels LG, Steward A, Clarke J (2005) Cooperative folding of a multidomain protein. J Mol Biol 349: 1045-1059. PMID: 15913648
14. Batey S, Clarke J (2006) Apparent cooperativity in the multidomain protein depends on the relative rates of folding of the constituent domain. Proc Natl Acad Sci USA 103: 18113-18118. doi: 10.1073/ pnas.0604580103 PMID: 17108086
15. Zhou Z, Feng H, Zhou H, Zhou Y, Bai Y (2005) Design and folding of a multidomain protein. Biochemistry 44: 12107-12112. PMID: 16142908
16. Scott KA, Steward A, Fowler SB, Clarke J (2002) Titin; a multidomain protein that behaves as the sum of its parts J Mol Biol 315: 819-829. PMID: 11812150
17. Harper SL, Sriswasdi S, Tang HY, Gaetani M, Gallagher PG, et al. (2013) The common hereditary elliptocytosis -associated α-spectrin L260P mutation perturbs erythrocyte membranes by stabilizing spectrin in the closed dimer conformation. Blood 122: 3045-3053. doi: 10.1182/blood-2013-02- 487702 PMID: 23974198
18. Sriswasdi S, Harper SL, Tang HY, Gaetani M, Gallagher PG, et al. (2014) Probing large conformational rearrangements in wild-type and mutant spectrin using structural mass spectrometry. Proc Natl Acad Sci USA 111: 1801-1806. doi: 10.1073/pnas.1317620111 PMID: 24453214
19. Mohandas N, Evans E (1994) Mechanical properties of the Red cell membrane in Relation to Molecular structure and Genetic DefectsAnnu Rev Biophys Biomol Struct 23: 787-818. PMID: 7919799
20. Williamson P, Bateman J, Kozarsky K, Mattocks K, Hermanowicz N, et al. (1982) Involvement of spectrin in maintenance of phase state asymmetry in the erythrocyte membraneCell 30: 725-733. PMID: 7139713
21. Bhattacharya M, Ray S, Bhattacharya S, Chakrabarti A (2004) Chaperone activity and prodan binding at self-associating domain of erythroid spectrin. J Biol Chem 279: 55080-55088. PMID: 15492010
22. Speicher DW, Marchesi VT (1984) Erythrocyte spectrin is comprised of many homologous triple helical segments Nature 311: 177-180. PMID: 6472478
23. Pascual J, Pfuhi M, Rivas G, Pastore A, Saraste M (1996)The spectrin repeats folds into a three helix bundle in solution. FEBS Lett 383: 201-207. PMID: 8925896
24. Yan Y, Winograd E, Viel A, Cornin T, Harrison SC, et al. (1993) Crystal structure of the repetitive segment of spectrin. Science 262: 2027-2030. PMID: 8266097
25. Macdonald RI, Edwin VP (2001) Free energy of urea and of thermal unfolding shows that two tandems repeats of spectrin are thermodynamically more stable than single repeat. Biochemistry 40: 3974-3984. PMID: 11300778
26. Kusunoki H, Minasov G, Macdonald RI, Mondragon A (2004) Independent movement dimerization and stability of chicken brain α-spectrin. J Mol Biol 344: 495-511. PMID: 15522301
27. Grum VL, Dongning L, Macdonald RI, Mondragon A (1999)Structure of two repeat fragments of spectrin suggests models of flexibility Cell 98: 523-535. PMID: 10481916
28. Li Q, Fung LW (2009) Structural and dynamic study of the teramerization region of nonerythroid α- spectrin- A faraday helix revealed by site directed spin labeling electron paramagnetic resonance. Biochemistry 48: 206-215. doi: 10.1021/bi8013032 PMID: 19072330
29. Mehboob S, Jacob J, May M, Kotula L, Thiyagarajan P, et al. (2003) Structural analysis of the α-n terminal region of erythroid and nonerythroid spectrin by small angle X-ray scattering. Biochemistry 42: 14702-14710. PMID: 14661984
30. Bennett V, Davis J, Flower VE (1982) Brain spectrin: a membrane associated protein related to in structure and function of erythroid spectrin. Nature 299: 126-131. PMID: 7110333
31. Davis J, Bennett V (1983) Brain spectrin. Isolation of subunit and formation of hybrids with erythrocyte spectrin subunits. J Biol Chem 258: 7757-7766. PMID: 6863263
32. Mehboob S, Song Y, Witek M, Long F, Santarsiero BD, et al. (2010) Crystal structure of the nonerythroid spectrin α-spectrin tetramerization sites reveals the difference between erythroid and nonerythroid spectrin tetramer formation. J Biol Chem 285: 14572-14584. doi: 10.1074/jbc.M109.080028 PMID: 20228407
33. Begg GE, Morris MB Ralston GB (1997) Comparison salt dependent self-association of Brain and erythroid spectrin. Biochemistry 36: 6977-6985. PMID: 9188694
34. Diakowski W, Sikorski AF (2002) Brain spectrin exerts much stronger effects on anionic Phospholipid monolayer than erythroid spectrin. Biochim Biophys Acta 1564: 13252-13258. PMID: 12175923
35. Desilv TM, Harper AL, Kotula L, Hensley P, Curti PJ, et al. (1997) Peptide of a single motif erythroid spectrin peptide: A highly stable independent folding unitBiochemistry 36: 3991-3997. PMID: 9092829
36. Menhart N, Mitchell T, Lusitani D, Topouzian N, Fung LWM (1996) Peptides more than 106 amino acids sequence motif are needed to mimic the structural stability of spectrin. J Biol Chem 271: 30410-30416. PMID: 8940005
37. Batey S, Scott KA, Clarke J (2006) Complex folding kinetics of a multi domain protein. Biophys J 90: 2120-2130. doi: 10.1529/biophysj.105.072710 PMID: 16387757
38. Macdonald RI, Cummings JA (2004) Stabilities of folding of clustered two repeat fragments of spectrin reveal a potential hinge in the human erythroid spectrin tetramer. Proc Natl Acad Sci USA 101: 1502-1507. doi: 10.1073/pnas.0308059100 PMID: 14747656
39. An X, Zhang X, Salomao M, Guo X, Yang YW, et al. (2006) Thermal stabilities of Brain spectrin and constituent Repeats of subunits. Biochemistry 45: 13670-13676. PMID: 17087521
40. Sahr KE, Laurila P, Kotula L, Scarpa AL, Coupal E, et al. (1990) The complete c-DNA and polypeptide sequence of human erythroid alpha-spectrin. J Biol Chem 265: 4434-4443. PMID: 1689726
41. Winkelmann JC, Chang JG, Tsc WT, Scarpa AL, Marchesi VT, et al. (1990) Full length sequence of the c-DNA for human erythroid spectrin. J Biol Chem 265: 11827-11832. PMID: 2195026
42. Moon RT, MacMohan AP (1990) Generation of diversity in nonerythroid spectrins. Multiple peptides are predicted by sequence analysis of c-DNA encompassing the coding region of human nonerythroid alpha spectrin. J Biol Chem 265: 4427-4433. PMID: 2307671
43. Pantazatos DP, MacDonald RI (1997) Site-directed mutagenesis of either highly conserved Trp-22 and moderately conserved Trp-95 to a large residues the thermodynamic stability of a spectrin repeating unit. J Biol Chem 272: 21052-21059. PMID: 9261107
44. MacDonald RI, Musacchio A, Holmgren RA, Saraste M (1994) Invariant tryptophan at shielded sites promotes folding of the conformation unit of spectrin. Proc Nalt Acad Sci USA 91: 1299-1303. PMID: 8108405
45. 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. doi: 10.1110/ps. 03302003 PMID: 14573853
46. Ray S, Chakrabarti A (2004) Membrane interaction of erythroid spectrin: surface density dependent high affinity binding to phosphatidylethanolamine Mol Mem Biol 21: 93-100. PMID: 15204438
47. Ray S, Chakrabarti A (2003) Erythroid spectrin in miceller detergents. Cell Motil Cytoskeleton 54: 16-28. PMID: 12451592
48. Patra M, Mitra M, Chakrabarti A, Mukhopadhyay C (2014) Binding of polarity sensitive hydrophobic ligands to erythroid and non-erythroid spectrin: fluorescence and molecular modeling studies. J Biol Mol Struct Dyn 32: 852-865. doi: 10.1080/07391102.2013.793212 PMID: 24404769
49. Gelleney JR, Gelleney JP, Weber K (1982) F-actin binding and cross linking properties of porcine brain fodrin a spectrin related molecule. J Biol Chem 257: 9781-9787. PMID: 7107591
50. Bradford MM (1976) A rapid sensitive method for the quantitation of protein utilizing the principle of dye binding. Anal Biochem 72: 9781-9786. PMID: 942051
51. Lakowicz JR (2006) Principle of fluorescence Spectroscopy. 3rd ed: Springer: Singapore.
52. Ray S, Bhattacharyya M, Chakrabarti A (2005) Conformational study of spectrin in presence of submolar concentrations of denaturants. J Fluorescence 15: 61-70. PMID: 15711878
53. Eftink MR, Ghiron CA (1981) Fluorescence quenching studies with protein. Anal Biochem 114: 199-227. PMID: 7030122
54. Lehrer SS, Leavis PC (1978) Solute quenching of protein fluorescence. Methods Enzymol 49: 222-236. PMID: 651665
55. Budzynski DM, Benight AS, LaBrake CC, Fung LWM (1992) Dynamic light scattering investigations of human erythroid spectrin. Biochemistry 31: 3653-3660. PMID: 1567821
56. Long F, Mcelheny D, Jaing S, Park S, Caffrey MS, et al. (2007) Conformational change of erythroid a-spectrin at the tetramerization site upon binding β-spectrin. Protein Sci 16: 2519-2530. doi:10. 1110/ps.073115307 PMID: 17905835
57. Pace CN (1986) Determination and analysis of urea and guanidine hydrochloride denaturation curve. Methods Enzymol 131: 266-280. PMID: 3773761
58. Pace CN (1990) Measuring and increasing protein stability. Trends Biotechnol 8: 93-98. PMID: 1367432
59. Street TO, Courtemanche N, Barrick D (2008) Protein folding and stability using denaturant. Methods Cell Biol 84: 295-325. PMID: 17964936
60. Kloss E, Barrick D (2008) Thermodynamics, kinetics, and salt dependence of folding of YopM, a Large Leucine-rich Repeat protein. J Mol Biol 383: 1195-1209. doi: 10.1016/j.jmb.2008.08.069 PMID: 18793647
61. Prajapati S, Bhakuni V, Babu KR, Jain SK (1998) Alkaline unfolding and salt induced folding liver catalase at high pH. Eur J Biochem 255: 178-184. PMID: 9692917
62. Subbarao NK, MacDonald RC (1994) Fluorescence studies of spectrin and its subunit. Cell Motil Cytoskeleton 29: 72-81. PMID: 7820859
63. Calvert R, Bennet P, Gratzer W. (1980) A conformational study of human Spectrin. Eur J Biochem 107: 363-367. PMID: 7398647
64. Yoshino H, Marchesi VT. (1984) Isolation of the subunits and the reassociation in vitro. J Biol Chem 259: 4496-4500. PMID: 6707015
65. Davis J, Bennett V (1983) Brain Spectrin. J Biol Chem 258: 7757-7766. PMID: 6863263
66. Johnson WC Jr (1988) Secondary Structure of Proteins through Circular Dichroism Spectroscopy. Annu Rev Biophys Biophys Chem 17: 145-166. PMID: 3293583
67. Parker W, Song PS (1992) Protein structures in SDS micelle protein complexes. Biophys J 61: 1435-1439. doi: 10.1016/S0006-3495(92)81949-5 PMID: 1600087
68. Dolgikh DA, Gilmanshin RI, Brazhnikov EV, Bychkova VE, Semisotnov GV, et al. (1981) Alpha-Lactalbumin: compact state with fluctuating tertiary structure. FEBS Lett 136: 311-315. PMID: 7327267
69. Bushmarina NA, Kuznetsova IM, Biktashev AV, Turoverov KK, Uversky VN (2002) Partially folded conformations in the folding pathway of bovine carbonic anhydrase II: a fluorescence spectroscopic analysis. Chembiochem 2: 813-821. PMID: 11948867
70. Povarova OI, Kuznetsova IM, Turoverov KK (2010) Differences in the pathways of protein unfolding induces by urea and Guanidine Hydrochloride: Molten globule state and aggregates. Plos One 5, e15035. doi: 10.1371/journal.pone.0015035 PMID: 21152408
71. Hawe A, Sutter M, Jiskoot W (2008) Extrinsic Fluorescent Dyes as Tools for Protein Characterization. Pharm Res 25, 1487-1499. doi: 10.1007/s11095-007-9516-9 PMID: 18172579
72. Noppert A, Gast K, Muller-Forhne M, Zirwer D, Damaschun G (1996) Reduced denatured ribonuclease A is not in a compact state. FEBS Lett 380: 179-182. PMID: 8603733
73. Sosnick R, Trewhella J (1992) Denaturated state of ribonuclease A have compact dimensions and residual secondary structure. Biochemistry 31: 8329-8330. PMID: 1525171
74. Dubin SB, Feher G, Benedek GB (1973) Study of the chemical denaturation of lysozyme by optical mixing spectroscopy. Biochemistry 12: 714-719. PMID: 4691514
75. Adel A, Nadia M, Mohamed O, Abdelhafidh G (2008) Study of thermally and chemically unfolded conformation of bovine serum albumin. Mat Sci Eng, 28: 594-600. doi: 10.1021/bm701144k PMID: 18205315
76. Franco G, Banuelos S, Falces J, Muga A, Urbaneja MM (2008) Thermodynamic characterization of nucleoplasmin unfolding: Interplay between function and stability. Biochemistry 47: 7954-7962. doi: 10.1021/bi8002555 PMID: 18597490
77. Maturicio MG (2002) Conformational Stability of Dimeric and Monomeric Forms of the C-terminal Domain of Human Immunodeficiency Virus-1 Capsid Protein. J Mol Biol 318: 519-531. PMID: 12051856
78. Hurshman Babbes AR, Powers ET, Kelly JW (2008) Quantification of the thermodynamically linked quaternary and tertiary structural stabilities of transthyretin and its disease-associated variants: The Relationship between stability and amyloidosis. Biochemistry 47, 6969-6984. doi: 10.1021/ bi800636q PMID: 18537267
79. Jaenicke R, Lillie H (2000) Folding and association of oligomeric and multimeric protein. Ad Protein Chem 53: 329-401 PMID: 10751948
80. Reddy GB, Bharadwaj S, Surolia A (1999) Thermal stabilities and mode of oligomerization of tetrameric peanut agglutinin. Biochemistry 38: 4462-4670. PMID: 10194368
81. Guidry JJ, Moczygemba CK, Stafshede PW, Steede NK, Samuel JS (2000) Reversible denaturation of oligomeric human chaperonin 10: Denatured state depends on chemical denaturant. Protein Sci 9: 2109-2117. doi: 10.1110/ps.9.11.2109 PMID: 11152122
82. Tes WT, Lecomte M, Costa FF, Garbarz M, Feo C et al. (1990) Point mutation in the beta-spectrin gene associated with alpha I/74 hereditary elliptocytosis. Implications for the mechanism of spectrin dimer self-association. J Clin Invest 86: 909-916. doi: 10.1172/JCI114792 PMID: 1975598
83. Gallagher PG, Roberts WE, Benoit L, Speicher DW, Marchesi SW, et al. (1993) Poikilocytic hereditary elliptocytosis associated with spectrin Alexandria: an alpha I/50b Kd variant that is caused by a single amino acid deletion. Blood 82: 2210-2215. PMID: 8400271
84. Ralston GB (1976) Physico-chemical characterization of the spectrin tetramer from bovine erythrocyte membranes Biochim Biophys Acta 455: 163-172. PMID: 990324
85. Mikkelsen A, Stokke BT, Elgsaeter A (1984) An electro-optic study of human erythrocyte spectrin dimers: The presence of calcium ions does not alter spectrin flexibility. Biochim Biophys Acta-Proteins 786: 95-102. PMID: 6712961
86. Morrow JS, Marchesi VT (1981) Self assembly of spectrin oligomers in vitro: a basis for a dynamic cytoskeleton. J Cell Biol 88: 463-468. PMID: 7204503
87. Liu SC, Windisch P, Kim S, Palek J (1984) Oligomeric states of spectrin in normal erythrocytes: Biochemical and electron microscopic study. Cell 37: 587-594. PMID: 6722882
88. Bhuyan AK (2002) Protein stabilization by Urea and Guanidine Hydrochloride. Biochemistry 41: 13386-13394. PMID: 12416983
89. Haque ME, Debnath D, Basak S, Chakrabarti A (1999) Structural changes in horseradish peroxidase in presence of low concentrations of urea. Eur J Biochem 259: 269-274. PMID: 9914502
90. Stepanenko OV, Verkhusha VV, Kazakov VI, Shavlovsky MM, Kuznetsova IM, et al. (2004) Comparative studies on the structure and stability of fluorescent proteins EGFP, ZFP506, Mrfp1 dimmer2 and DsRed 1Biochemistry 43: 14913-14923. PMID: 15554698
91. Dunbar J, Yennawar HP, Banerjee S, Luo J, Farber G (1997) The effect of denaturant on protein structure. Protein Science 6: 1272-1733. doi: 10.1002/pro.5560060813 PMID: 9260285
92. Pike ACW, Acharya R (1994) A structural basis for the interaction of urea with lysozyme. Protein Science 3: 706-710. doi: 10.1002/pro.5560030419 PMID: 8003989
93. Yoshino H, Marchesi VT (1985) Interaction between the subunits of human erythrocyte spectrin using a fluorescence probe. Biochim Biophys Acta 812: 786-792. PMID: 3970907
94. Schellman JA (2002) Fifty years of solvent denaturation. Biophys Chem 96: 91-101. PMID: 12034431
95. Mayo SL, Baldwin RL (1993) Guanidium chloride induction of partial unfolding in amide protein exchange in RNase A. Science 262: 873-876. PMID: 8235609
96. Breslow R, Guo T (1990) Surface tension measurements show that chaotropic salting-in denaturants are not just water-structure breakers. Proc Nalt Acad Sci USA 87: 167-169. PMID: 2153285
97. Monera OD, Kay CM, Hodges RS (1994) Protein denaturation with guanidine hydrochloride or urea provides a different estimate of stability depending on the contributions of electrostatic interactions. Protein Sci 3: 1984-1991. doi: 10.1002/pro.5560031110 PMID: 7703845
98. Myers JK, Pace CN, Scholtz JM (1995) Denaturant m values and heat capacity changes: Relation to changes in accessible surface areas of protein unfolding. Protein Sci 4: 2138-2148. doi: 10.1002/pro. 5560041020 PMID: 8535251
99. Pace CN (2000) Single surface stabilizer. Nat Struct Biol 7: 345-346. PMID: 10802723
100. Vecchio PD, Graziano G, Granata V, Barone G, Mandrich L, et al. (2002) Denaturing action of urea and guanidine hydrochloride towards two thermophilic esterases. Biochem J 367: 857-863. doi:10. 1042/BJ20020695 PMID: 12160466
101. Akhtar MS, Ahmad A, Bhakuni V (2002) Guanidinium Chloride-and Urea-Induced Unfolding of the dimeric enzyme Glucose Oxidase. Biochemistry 41: 3819-3827. PMID: 11888301