Acid-induced unfolding of didecameric keyhole limpet hemocyanin: Detection and characterizations of decameric and tetrameric intermediate states

Amino Acids

Volumn 39, Issue 3, 2010, Pages 899-910

  Varshney, Ankita ^a   Ahmad, Basir ^a   Rabbani, Gulam ^a   Kumar, Vijay ^b   Yadav, Savita ^b   Khan, Rizwan Hasan ^a  

^a ALIGARH MUSLIM UNIVERSITY   (India)

^b ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

Author keywords

Acidic pH; Decamer state; Dynamic light scattering; Keyhole limpet hemocyanin; Multimeric protein; Tetramer state

Indexed keywords

DYE; HAPTEN; IMMUNOSTIMULATING AGENT; ISOPROTEIN; KEYHOLE LIMPET HEMOCYANIN; OLIGOMER; POLYMER; TETRAMER; ACID; HEMOCYANIN; KEYHOLE-LIMPET HEMOCYANIN;

ARTICLE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; FLUORESCENCE; HYDRODYNAMICS; LIGHT SCATTERING; MOLECULAR WEIGHT; MOLLUSC; OLIGOMERIZATION; PH; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; THERMOSTABILITY; ANIMAL; CHEMISTRY; GASTROPOD; KINETICS; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

ACIDS; ANIMALS; GASTROPODA; HEMOCYANIN; HYDROGEN-ION CONCENTRATION; KINETICS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STABILITY;

MEGATHURA CRENULATA; MOLLUSCA;

EID: 77956912419     PISSN: 09394451     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00726-010-0524-4     Document Type: Article

References (66)

1. Ahmad B, Ankita, Khan RH (2005) Urea induced unfolding of F isomer of human serum albumin: a case study using multiple probes. Arch Biochem Biophys 437: 159-167
2. Ahmad B, Ansari MA, Sen P, Khan RH (2006) Low versus high molecular weight polyethylene glycol induced states of stem bromelain at low pH: stabilization of molten globule and unfolded states. Biopolymers 81: 350-359
3. Andrade MA, Chacon P, Merelo JJ, Moran F (1993) Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network. Protein Eng 6: 383-390
4. Beck A, Hillen N, Dolashki A, Stevanovic S, Salvato B, Voelter W, Dolashka-Angelova P (2007) Oligosaccharide structure of a functional unit RvH1-b of Rapana venosa hemocyanin using HPLC/electrospray ionization mass spectrometry. Biochimie 89: 938-949
5. Betting DJ, Mu XY, Kafi K, McDonnel D, Rosas F, Gold DP, Timmerman JM (2009) Enhanced immune stimulation by a therapeutic lymphoma tumor antigen vaccine produced in insect cells involves mannose receptor targeting to antigen presenting cells. Vaccine 27: 250-259
6. Bonafe CF, Araujo JRV, Silva JL (1994) Intermediate states of assembly in the dissociation of gastropod hemocyanin by hydrostatic pressure. Biochemistry 33: 2651-2660
7. Chen YH, Yang JT, Martinez H (1972) Determination of the secondary structure of proteins by circular dichroism and optical rotatory dispersion. Biochemistry 11: 4120-1131
8. Cremades N, Sancho J (2008) Molten globule and native state ensemble of Helicobacter pylori flavodoxin: can crowding, osmolytes or cofactors stabilize the native conformation relative to the molten globule? Biophys J 95: 1913-1927
9. Decker H, Hellmann N, Jaenicke E, Lieb B, Meissner U, Markl J (2007) Minireview: recent progress in hemocyanin research. Integr Comp Biol 47: 631-644
10. Dolashka P, Genov N, Parvanova K, Voelter W, Geiger M, Stoeva S (1996) Rapana thomasiana grosse (gastropoda) haemocyanin: spectroscopic studies of the structure in solution and the conformational stability of the native protein and its structural subunits. Biochem J 315: 139-144
11. Dolashka-Angelova P, Schick M, Stoeva S, Voelter W (2000) Isolation and partial characterization of the N-terminal functional unit of subunit RtH1 from Rapana thomasiana grosse hemocyanin. Int J Biochem Cell Biol 32: 529-538
12. Dolashka-Angelova P, Schwarz H, Dolashki A, Beltramini M, Salvato B, Schick M, Saeed M, Voelter W (2003) Oligomeric stability of Rapana venosa hemocyanin (RvH) and its structural subunits. Biochim Biophys Acta 1646: 77-85
13. Dolashka-Angelova P, Stevanovic S, Dolashki A, Devreese B, Tzvetkova B, Voelter W, Van Beeumen J, Salvato B (2007) A challenging insight on the structural unit 1 of molluscan Rapana venosa hemocyanin. Arch Biochem Biophys 459: 50-58
14. Dolashka-Angelova P, Lieb B, Velkova L, Heilen N, Sandra K, Nikolaeva-Glomb L, Dolashki A, Galabov AS, Van Beeumen J, Stevanovic S, Voelter W, Devreese B (2009) Identification of glycosylated sites in Rapana hemocyanin by mass spectrometry and gene sequence, and their antiviral effect. Bioconjug Chem 20: 1315-1322
15. Dolashki A, Schutz J, Hristova R, Voelter W, Dolashka P (2005) Spectroscopic properties of non-glycosilated functional unit KLH2-c of keyhole limpet hemocyanin. World J Agric Sci 1: 129-136
16. Dolashki A, Velkova L, Atanasov B, Voelter W, Stevanovic S, Schwarz H, Muro PD, Dolashka-Angelova P (2008) Reversibility and ''pH-T phase diagrams'' of Rapana venosa hemocyanin and its structural subunits. Biochim Biophys Acta 1784: 1617-1624
17. Eftink MR, Ghiron CA (1982) Fluorescence quenching studies with proteins. Anal Biochem 114: 199-227
18. Gatsogiannis C, Markl J (2009) Keyhole limpet hemocyanin: the 9ÅCryoEM structure and molecular model of the KLH1 didecamer reveal the interfaces and intricate topology of 160 functional units. J Mol Biol 385: 963-983
19. Gebauer W, Harris JR, Heid H, Sueling M, Hillenbrand R, Soehngen S, Wegener-Strake A, Markl J (1994) Quaternary structure, subunits and domain patterns of two discrete forms of keyhole limpet hemocyanin: KLH1 and KLH2. Zoology 98: 51-68
20. Gebauer W, Stoeva S, Voelter W, Dainese E, Salvato B, Beltramini M, Markl J (1999a) Hemocyanin subunit organization of the gastropod Rapana thomasiana. Arch Biochem Biophys 372: 128-134
21. Gebauer W, Harris JR, Geisthardt G, Markl J (1999b) Keyhole limpet hemocyanin type 2 (KLH2): detection and immunolocalization of a labile functional unit h. J Struct Biol 128: 280-286
22. Gebauer W, Harris JR, Markl J (2002) Topology of the 10 subunits within the decamer of KLH, the hemocyanin of the marine gastropod Megathura crenulata. J Struct Biol 139: 153-159
23. Georgieva ER, Narvaez AJ, Hedin N, Graslund A (2008) Secondary structure conversions of Mycobacterium tuberculosis ribonucle-otide reductase protein R2 under varying pH and temperature conditions. Biophys Chem 137: 43-48
24. Gerber R, Tahiri-Alaoui A, Hore PJ, James W (2007) Oligomeriza-tion of the human prion protein proceeds via a molten globule intermediate. J Biol Chem 282: 6300-6337
25. Gerber R, Tahiri-Alaoui A, Hore PJ, James W (2008) Conformational pH dependence of intermediate states during oligomerization of the human prion protein. Protein Sci 17: 537-544
26. Geyer H, Wuhrer M, Resemann A, Geyer R (2005) Identification and characterization of keyhole limpet hemocyanin N-glycans mediating cross-reactivity with Schistosoma mansoni. J Biol Chem 280: 40731-40748
27. Greene LH, Wijesinha-Bettoni R, Redfield C (2006) Characterization of the molten globule of human serum retinol-binding protein using NMR spectroscopy. Biochemistry 45: 9475-9484
28. Guzman-Casado M, Parody-Morreale A, Mateo PL, Sánchez-Ruiz JM (1990) Differential scanning calorimetry of lobster haemocyanin. Eur J Biochem 188: 181-185
29. Harris JR, Markl J (1999) Keyhole limpet hemocyanin (KLH): a biomedical review. Micron 30: 597-623
30. Harris JR, Markl J (2000) Keyhole limpet hemocyanin: molecular structure of a potent marine immunoactivator: a review. Euro Urol 37(suppl 3): 24-33
31. Harris JR, Gebauer W, Adrian M, Markl J (1998) Keyhole limpet hemocyanin (KLH): slow in vitro reassociation of KLH1 and KLH2 from Immucothel. Micron 5: 329-339
32. Harris JR, Scheffler D, Gebauer W, Lehnert R, Markl J (2000) Haliotis tuberculata hemocyanin (HtH): analysis of oligomeric stability of HtH1 and HtH2 and comparison with keyhole limpet hemocyanin KLH1 and KLH2. Micron 31: 613-622
33. Hartmann H, Bongers A, Decker H (2004) Small-angle X-ray scattering based three-dimensional reconstruction of the immu-nogen KLH1 reveals different oxygen-dependent conformations. J Biol Chem 279: 2841-2845
34. Herskovits TT (1988) Recent aspects of the subunit organization and dissociation of hemocyanins. Comp Biochem Physiol B 91: 597-611
35. Hristova R, Dolashki A, Voelter W, Stevanovic S, Dolashka-Angelova P (2008) O-Diphenol oxidase activity of molluscan hemocyanins. Comp Biochem Phys Part B 149: 439-446
36. Ioannes PD, Moltedo B, Oliva H, Pacheco R, Faunes F, Ioannes AED, Becker MI (2004) Hemocyanin of the Molluscan Concholepas concholepas exhibits an unusual heterodecameric array of subunits. J Biol Chem 279: 26134-26142
37. Kather I, Jakob RP, Dobbek H, Schmid FX (2008) Increased folding stability of TEM-1 beta-lactamase by in vitro selection. J Mol Biol 383: 238-251
38. Keller H, Lieb B, Altenhein B, Gebauer D, Richter S, Stricker S, Markl J (1999) Abalone (Haliotis tuberculata) hemocyanin type 1 (HtH1). Organization of the approximately 400 kDa subunit, and amino acid sequence of its functional units f, g and h. Eur J Biochem 264: 27-38 (Pubitemid 29385864)
39. Kim JH, Lee Y, Bae YS, Kim WS, Kim K, Im HY, Kang WK, Park K, Choi HY, Lee HM, Baek SY, Lee H, Doh H, Kim BM, Kim CY, Jeon C, Jung CW (2007) Phase I/II study of immunotherapy using autologous tumor lysate-pulsed dendritic cells in patients with metastatic renal cell carcinoma. Clin Immunol 125: 257-267
40. Kuznetsova IM, Turoverov KK, Uversky VN (2003) Use of the phase diagram method to analyze the protein unfolding-refolding reactions: fishing out the "Invisible" intermediates. J Proteome Res 3: 485-494
41. Lieb B, Markl J (2004) Evolution of molluscan hemocyanins as deduced from DNA sequencing. Micron 35: 117-119
42. Lieb B, Altenhein B, Lehnert R, Gebauer W, Markl J (1999) Subunit organization of the abalone Haliotis tuberculata hemocyanin type 2 (HtH2), and the cDNA sequence encoding its functional units d, e, f, g and h. Eur J Biochem 265: 134-144 (Pubitemid 29466021)
43. Lieb B, Altenhein B, Markl J (2000) The sequence of a gastropod hemocyanin (HtH1 from Haliotis tuberculata). J Biol Chem 275: 5675-5681
44. Lieb B, Altenhein B, Markl J, Vincent A, Van Olden EV, Van Holde KE, Miller K (2001) Structures of two molluscan hemocyanin genes: significance for gene evolution. Proc Natl Acad Sci USA 98: 4546-4551
45. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin-phenol reagent. J Biol Chem 193: 265-275
46. Markl J, Savel-Niemann A, Wegener-Strake A, Sueling M, Schneider A, Gebauer W, Harris JR (1991) The role of two distinct subunit types in the architecture of keyhole limpet hemocyanin (KLH). Naturwissenschaften 78: 512-514
47. Martin A, Depoix F, Stohr M, Meissner U, Hagner-Holler S, Hammouti K, Burmester T, Heyd J, Wriggers W, Markl J (2007) Limulus polyphemus hemocyanin: 10 A structure, sequence analysis, molecular modelling and rigid-body fitting reveal the interfaces between the eight hexamers. J Mol Biol 366: 1332-1350
48. Mouche F, Zhu YX, Pulokas J, Potter CS, Carragher B (2003) Automated three-dimensional reconstruction of keyhole limpet hemocyanin type 1. J Struct Biol 144: 301-312
49. Nishimura C, Dyson HJ, Wright PE (2008) The kinetic and equilibrium molten globule intermediates of apoleghemoglobin differ in structure. J Mol Biol 378: 715-725
50. Orlova EV, Dube P, Harris JR, Beckman E, Zemlin F, Markl J, van Heel M (1997) Structure of keyhole limpet hemocyanin type 1 (KLH1) at 15 A resolution by electron cryomicroscopy and angular reconstitution. J Mol Biol 271: 417-437
51. Paci E, Greece LH, Jones RM, Smith LJ (2005) Characterization of the molten globule state of retinol-binding protein using a molecular dynamics simulation approach. FEBS J 18: 4826-4838
52. Pawar SA, Deshpande VV (2000) Characterization of acid-induced unfolding intermediates of glucose/xylose isomerase. Eur J Biochem 267: 6331-6338
53. Ramboarina S, Redfield C (2008) Probing the effect of temperature on the backbone dynamics of the human α-lactalbumin molten globule. J Am Chem Soc 130: 15318-15326
54. Riggs DR, Jackson B, Vona-Davis L, McFadden D (2002) In vitro anticancer effects of a novel immunostimulant: keyhole limpet hemocyanin. J Surg Res 108: 279-284
55. Sabbatini PJ, Ragupathi G, Hood C, Aghajanian CA, Juretzka M, Iasonos A, Hensley ML, Spassova MK, Ouerfelli O, Spriggs DR, Tew WP, Konner J, Clausen H, Abu Rustum N, Dansihefsky SJ, Livingston PO (2007) Pilot study of a heptavalent vaccine-keyhole limpet hemocyanin conjugate plus QS21 in patients with epithelial ovarian, fallopian tube, or peritoneal cancer. Clin Cancer Res 13: 4170-4177
56. Sandra K, Dolashka-Angelova P, Devreese B, Van Beeumen J (2007) New insights in Rapana venosa hemocyanin N-glycosylation resulting from on-line mass spectrometric analyses. Glycobiology 17: 141-156
57. Semisotnov GV, Rodionova NA, Razgulyaev OI, Uversky VN, Gripas AF, Gilmanshin RI (1991) Study of the ''molten globule'' intermediate state in protein folding by a hydrophobic fluorescent probe. Biopolymers 1: 119-128
58. Sohngen MS, Stahalmann A, Harris JR, Muller SA, Engel A, Markl J (1997) Mass determination, subunit organization and control of oligomerization states of keyhole limpet hemocyanin (KLH). Euro J Biochem 248: 602-614
59. Sterner R, Decker H (1994) Inversion of the Bohr effect upon oxygen binding to 24-meric tarantula hemocyanin. Proc Natl Acad Sci USA 91: 4835-4839
60. Stoeva S, Dolashka P, Bankov B, Voelter W, Salvato B, Genov N (1995) Spectroscopic properties of Callinectes sapidus hemocy-anin subunits. Spectrochim Acta 51A: 1965-1974
61. Suminoe A, Matsuzaki A, Hattori H, Koga Y, Hara T (2008) Immunotherapy with autologous dendritic cells and tumor antigens for children with refractory malignant solid tumors. Pediatr Transpl 13: 746-753
62. Van Holde KE, Miller KI (1995) Hemocyanins. Adv Protein Chem 47: 1-81
63. Van Holde KE, Miller KI, Lang WH (1992) Molluscan hemocyanins: structure and function. Adv Comp Environ Physiol 13: 257-300
64. Varshney A, Ahmad B, Khan RH (2008) Comparative studies of unfolding and binding of ligands to human serum albumin in the presence of fatty acid: spectroscopic approach. Int J Biol Macromol 42: 483-490
65. Velkova L, Dolashka-Angelova P, Dolashki A, Voelter W, Atanasov B (2009) Thermodynamic analysis and molecular modeling of Rapana venosa hemocyanin-functional unit RVH2-E. Biotechnol Biotechnol Eq 23: 601-605
66. Yang F Jr, Zhang M, Chen J, Liang Y (2006) Structural changes of alpha-lactalbumin induced by low pH and oleic acid. Biochim Biophys Acta 1764: 1389-1396