Characterization of a folding intermediate from HIV-1 ribonuclease H

Protein Science

Volumn 7, Issue 10, 1998, Pages 2164-2174

  Kern, Gunther ^a   Handel, Tracy ^a   Marqusee, Susan ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

HIV 1; Hydrogen exchange; Inhibitor; Kinetic intermediate; NMR; Protein folding; Ribonuclease H; Stopped flow

Indexed keywords

RIBONUCLEASE H;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; ENZYME ACTIVITY; ENZYME ANALYSIS; ESCHERICHIA COLI; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROCESSING; PROTEIN STABILITY;

ESCHERICHIA COLI; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 0031731890     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1002/pro.5560071014     Document Type: Article

References (62)

1. Babe LM, Rose J, Craik CS. 1992. Synthetic "interface" peptides alter dimeric assembly of the HIV 1 and 2 proteases. Protein Sci 1:1244-1253.
2. Bai Y, Milne JS, Mayne L, Englander SW. 1993. Primary structure effects on peptide group hydrogen exchange. Proteins 17:75-86.
3. Baldwin RL. 1996. On-pathway versus off-pathway folding intermediates. Fold Design 1:R1-R8.
4. Boucher W, Laue ED, Campbellburk S, Domaille PJ. 1992a. 4-Dimensional heteronuclear triple resonance NMR methods for the assignment of backbone nuclei in proteins. J Am Chem Soc 114:2262-2264.
5. Boucher W, Laue ED, Campbellburk SL, Domaille PJ. 1992b. Improved 4d-NMR experiments for the assignment of backbone nuclei in C-13/N-15 labelled proteins. J Biomol NMR 2:631-637.
6. Chamberlain AK, Handel TM, Marqusee S. 1996. Detection of rare partially folded molecules in equilibrium with the native conformation of RNase H. Nat Struct Biol 3:782-787.
7. Chen H, Hughes DD, Chan T-A, Sedat JW, Agard DA. 1996. IVE (image visualization environment): A software platform for all three-dimensional microscopy applications. J Struct Biol 116:56-60.
8. Cook KH, Schmid FX, Baldwin RL. 1979. Role of proline isomerization in folding of ribonuclease A at low temperatures. Proc Natl Acad Sci USA 76:6157-6161.
9. Crouch RJ. 1990. Ribonuclease H: From discovery to 3D structure. New Biol 2:771-777.
10. Dabora J, Marqusee S. 1996. Structure of the acid state of Escherichia coli ribonuclease H1. Biochemistry 35:11951-11958.
11. Davies JFD, Hostomska Z, Hostomsky Z, Jordan SR, Matthews DA. 1991. Crystal structure of the ribonuclease H domain of HIV-1 reverse transcriptase. Science 252:88-95.
12. Elove GA, Bhuyan AK, Roder H. 1994. Kinetic mechanism of cytochrome c folding: Involvement of the heme and its ligands. Biochemistry 33:6925-6935.
13. Elove GA, Roder H. 1991. Structure and stability of cytochrome c folding intermediates. In: Georgiou G, eds. Protein refolding. Washington, DC: American Chemical Society. pp 51-63.
14. Englander SW, Kallenbach NR. 1983. Hydrogen exchange and structural dynamics of proteins and nucleic acids. Q Rev Biophys 16:521-655.
15. Ghosh M, Howard KJ, Cameron CE, Benkovic SJ, Hughes SH, Le GS. 1995. Truncating alpha-helix E′ of p66 human immunodeficiency virus reverse transcriptase modulates RNase H function and impairs DNA strand transfer. J Biol Chem 270:7068-7076.
16. Gill SC, von Hippel PH. 1989. Calculation of protein extinction coefficients from amino acid sequence data. Analyt Biochem 182:319-326.
17. Goedken ER, Raschke TM, Marqusee S. 1997. Importance of the C-terminal helix to the stability and enzymatic activity of Escherichia coli ribonuclease H. Biochemistry 36:7256-7263.
18. Gow A, Friedrich VL Jr, Lazzarini RA. 1994. Many naturally occurring mutations of myelin proteolipid protein impair its intracellular transport. J Neurosci Res 37:574-583.
19. Grzesiek S, Bax A. 1992. Correlating backbone amide and side chain resonances in larger proteins by multiple relayed triple resonance NMR. J Am Chem Soc 114:6291-6293.
20. 2O in protein NMR. Application to sensitivity enhancement and NOE measurements. J Am Chem Soc 115:12593-12594.
21. Hall JG, Frieden C. 1989. Protein fragments as probes in the study of protein folding mechanisms: Differential effects of dihydrofolate reductase fragments on the refolding of the intact protein. Proc Natl Acad Sci 86:3060-3064.
22. Hansen J, Schulze T, Mellert W, Moelling K. 1988. Identification and characterization of HIV-specific RNase H by monoclonal antibody. Embo J 7:239-243.
23. Haruki M, Noguchi E, Nakai C, Liu YY, Oobatake M, Itaya M, Kanaya S. 1994. Investigating the role of conserved residue Asp134 in Escherichia coli ribonuclease HI by site-directed random mutagenesis. Eur J Biochem 220:623-631.
24. Houry WA, Sauder JM, Roder H, Scheraga HA. 1998. Definition of amide protection factors for early kinetic intermediates in protein folding. Proc Natl Acad Sci 95:4299-4302.
25. Hvidt A, Nielsen SO. 1966. Hydrogen exchange in proteins. Adv Protein Chem 21:288-386.
26. Jacobo MA, Ding J, Nanni RG, Clark AJ, Lu X, Tantillo C, Williams RL, Kamer G, Ferris AL, Clark P, Hizi A, Hughes SH, Arnold E. 1993. Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 Å resolution shows bent DNA. Proc Natl Acad Sci USA 90:6320-6324.
27. Jaenicke R. 1995. Folding and association versus misfolding and aggregation of proteins. Philos Trans R Soc Lond B Biol Sci 348:97-105.
28. Katayanagi K, Miyagawa M, Matsushima M, Ishikawa M, Kanaya S, Nakamura H, Ikehara M, Matsuzaki T, Morikawa K. 1992. Structural details of ribonuclease H from E. coli. J Mol Biol 223:1029-1052.
29. Keck JL, Marqusee S. 1995. Substitution of a highly basic helix/loop sequence into the RNase H domain of human immunodeficiency virus reverse transcriptase restores its Mn(2+)-dependent RNase H activity. Proc Natl Acad Sci USA 92:2740-2744.
30. Kern G, Kern D, Schmid FX, Fischer G. 1995. A kinetic analysis of the folding of human carbonic anhydrase II and its catalysis by cyclophilin. J Biol Chem 270:740-745.
31. Kiefhaber T. 1995. Kinetic traps in lysozyme folding. Proc Natl Acad Sci USA 92:9029-9033.
32. Kohlstaedt LA, Wang J, Friedman JM, Rice PA, Steitz TA. 1992. Crystal structure at 3.5 Å resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 256:1783-1790.
33. Kraulis PJ. 1989. Ansig: A program for the assignment of protein H-1 2d-NMR spectra by interactive computer graphics. J Magn Reson 84:627-633.
34. Kraulis PJ. 1991. Molscript: A program to produce both detailed and schematic plots of protein structures. J Appl Crystal 24:946-950.
35. Kraulis PJ. 1994. Protein three-dimensional structure determination and sequence-specific assignment of C-13 and N-15-separated NOE data - A novel real-space ab initio approach. J Mol Biol 243:696-718.
36. Kurada P, O'Tousa JE. 1995. Retinal degeneration caused by dominant rhodopsin mutations in Drosophila. Neuron 14:571-579.
37. Kuwajima K, Hiraoka Y, Ikeguchi M, Sugai S. 1985. Comparison of the transient folding intermediates in lysozyme and alpha-lactalbumin. Biochemistry 24:874-881.
38. Kuwajima K, Yamaya H, Miwa S, Sugai S, Nagamura T. 1987. Rapid formation of secondary structure framework in protein folding studied by stopped-flow circular dichroism. FEBS Lett 221:115-118.
39. Kuznetsov G, Bush KT, Zhang PL, Nigam SK. 1996. Perturbations in maturation of secretory proteins and their association with endoplasmic reticulum chaperones in a cell culture model for epithelial ischemia. Proc Natl Acad Sci USA 93:8584-8589.
40. Laue ED, Skilling J, Staunton J, Sibisi S, Brereton RG. 1985. Maximum entropy method in nuclear magnetic resonance spectroscopy. J Mag Res 62:437-452.
41. Liu X, Garriga P, Khorana HG. 1996. Structure and function in rhodopsin: Correct folding and misfolding in two point mutants in the intradiscal domain of rhodopsin identified in retinitis pigmentosa. Proc Natl Acad Sci USA 93:4554-4559.
42. Michaels JEA, Schimmel P, Shiba K, Miller TW. 1996. Dominant negative inhibition by fragments of a monomeric enzyme. Proc Natl Acad Sci 93: 14452-14455.
43. Oda Y, Yoshida M, Kanaya S. 1993. Role of histidine 124 in the catalytic function of ribonuclease HI from Escherichia coli. J Biol Chem 268: 88-92.
44. Oksche A, Schulein R, Rutz C, Liebenhoff U, Dickson J, Muller H, Birnbaumer M. Rosenthal W. 1996. Vasopressin V2 receptor mutants that cause X-linked nephrogenic diabetes insipidus: Analysis of expression, processing, and function. Mol Pharmacol 50:820-828.
45. Powers R, Clore GM, Bax A, Garrett DS, Stahl SJ, Wingfield PT, Gronenborn AM. 1991. Secondary structure of the ribonuclease H domain of the human immunodeficiency virus reverse transcriptase in solution using three-dimensional double and triple resonance heteronuclear magnetic resonance spectroscopy. J Mol Biol 221:1081-1090.
46. Powers R, Clore GM, Stahl SJ, Wingfield PT, Gronenborn A. 1992. Analysis of the backbone dynamics of the ribonuclease H domain of the human immunodeficiency virus reverse transcriptase using 15N relaxation measurements. Biochemistry 31:9150-9157.
47. Prusiner SB. 1997. Prion diseases and the BSE crisis. Science 278:245-251.
48. Raschke TM, Marqusee S. 1997. The kinetic folding intermediate of ribonuclease H resembles the acid molten globule and partially unfolded molecules detected under native conditions. Nat Struct Biol 4:298-304.
49. Reimer U, el Mokdad N, Schutkowski M, Fischer G. 1997. Intramolecular assistance of cis/trans isomerization of the histidine-proline moiety. Biochemistry 36:13802-13808.
50. Roder H, Colon W. 1997. Kinetic role of early intermediates in protein folding. Curr Opin Struct Biol 7:15-28.
51. Roder H, Elove GA, Englander SW. 1988. Structural characterization of folding intermediates in cytochrome c by H-exchange labeling and proton NMR. Nature 335:700-704.
52. Rodgers DW, Gamblin SJ, Harris BA, Ray S, Culp JS, Hellmig B, Woolf DJ, Debouck C, Harrison SC. 1995. The structure of unliganded reverse transcriptase from the human immunodeficiency virus type 1. Proc Natl Acad Sci USA 92:1222-1226.
53. Santoro MM, Bolen DW. 1988. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry 27:8063-8068.
54. Schatz O, Mous J, Le Grice SFJ. 1990. Inactivation of the RNase H domain of HIV-1 reverse transcriptase blocks viral infectivity. In: Papas T, ed. Gene regulation and AIDS. Houston, TX: Portfolio Publishing, pp 293-303.
55. Scholz C, Zarnt T, Kern G, Lang K, Burtscher H, Fischer G, Schmid FX. 1996. Autocatalytic folding of the folding catalyst FKBP12. J Biol Chem 271: 12703-12707.
56. Texter FL, Spencer DB, Rosenstein R, Matthews CR. 1992. Intramolecular catalysis of a proline isomerization reaction in the folding of dihydrofolate reductase. Biochemistry 31:5687-5691.
57. Tisdale M, Schulze T, Larder BA, Moelling K. 1991. Mutations within the RNase H domain of human immunodeficiency virus type 1 reverse transcriptase abolish virus infectivity. J Gen Virol 72:59-66.
58. Udgaonkar JB, Baldwin RL. 1988. NMR evidence for an early framework intermediate on the folding pathway of ribonuclease A. Nature 335:694-699.
59. 15N chemical shift referencing in biomolecular NMR. J Biomol NMR 6:135-140.
60. Yamasaki K, Ogasahara K, Yutani K, Oobatake M, Kanaya S. 1995. Folding pathway of Escherichia coli ribonuclease HI: A circular dichroism, fluorescence, and NMR study. Biochemistry 34:16552-16562.
61. Yang W, Hendrickson WA, Crouch RJ, Satow Y. 1990. Structure of ribonuclease H phased at 2 Å resolution by MAD analysis of the selenomethionyl protein. Science 249:1398-1405.
62. Zitzewitz JA, Bilsel O, Luo J, Jones BE, Matthews CR. 1995. Probing the folding mechanism of a leucine zipper peptide by stopped-flow circular dichroism spectroscopy. Biochemistry 34:12812-12819.