Molecular recognition in the HIV-1 Capsid/Cyclophilin A complex

Journal of Molecular Biology

Volumn 269, Issue 5, 1997, Pages 780-795

  Yoo, Sanghee ^a   Myszka, David G ^a   Yeh, Chin yah ^a   McMurray, Maureen ^a   Hill, Christopher P ^a   Sundquist, Wesley I ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Binding; Capsid; Chaperone; Cyclophilin; Human immunodeficiency virus

Indexed keywords

CAPSID PROTEIN; CYCLOPHILIN;

AMINO ACID SEQUENCE; ARTICLE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; ISOMERISM; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; STOICHIOMETRY; THERMODYNAMICS; VIRION; VIRUS CAPSID; VIRUS REPLICATION; VIRUS TYPING;

EID: 0031588011     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1051     Document Type: Article

References (98)

1. Aberham C., Weber S., Phares W. Spontaneous mutations in the human immunodeficiency virus type 1 gag gene that affect viral replication in the presence of cyclosporins. J. Virol. 70:1996;3536-3544.
2. Adachi A., Gendelman H. E., Koenig S., Folks T., Willey R., Rabson A., Martin M. A. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:1986;284-291.
3. Anderson S. K., Gallinger S., Roder J., Frey J., Young H. A., Ortaldo J. R. A cyclophilin-related protein involved in the function of natural killer cells. Proc. Natl Acad. Sci. USA. 90:1993;542-546.
4. Baker E. K., Colley N. J., Zuker C. S. The cyclophilin homolog NinaA functions as a chaperone, forming a stable complex in vivo with its protein target rhodopsin. EMBO J. 13:1994;4886-4895.
5. Billich A., Hammerschmid F., Peichl P., Wenger R., Zenke G., Quesniaux V., Rosenwirth B. Mode of action of SDZ NIM 811, a nonimmunosuppressive cyclosporin A analog with activity against human immunodeficiency virus (HIV) type 1: interference with HIV protein-cyclophilin A interactions. J. Virol. 69:1995;2451-2461.
6. Braaten D., Franke E. K., Luban J. Cyclophilin A is required for an early step in the life cycle of human immunodeficiency virus type I before the initiation of reverse transcription. J. Virol. 70:1996a;3551-3560.
7. CPZGAB but not group O HIV-1 or other primate lentiviruses. J. Virol. 70:1996b;4220-4227.
8. Braaten D., Aberham C., Franke E. K., Yin L., Phares W., Luban J. Cyclosporin A-resistant human immunodeficiency virus type 1 mutants demonstrate that Gag encodes the functional target of cyclophilin A. J. Virol. 70:1996c;5170-5176.
9. Bram R. J., Crabtree G. R. Calcium signalling in T cells stimulated by a cyclophilin B-binding protein. Nature. 371:1994;355-358.
10. Brandts J. F., Halvorson H. R., Brennan M. Consideration of the possibility that the slow step in protein denaturation reactions is due to cis-trans isomerism of proline residues. Biochemistry. 14:1975;4953-4963.
11. Brandts J. F., Lin L.-N., Wiseman T., Williston S., Yang C. P. An instrument for rapid determination of binding constants for biomolecules. Am. Lab. (Shelton, Conn). 22:1990;30-36.
12. Brooks I., Watts D. G., Soneson K. K., Hensley P. Determining confidence intervals for parameters derived from analysis of equilibrium analytical ultracentrifugation data. Methods Enzymol. 240:1994;459-478.
13. Bundle D. R., Sigurskjold B. W. Determination of accurate thermodynamics of binding by titration microcalorimetry. Methods Enzymol. 247:1994;288-305.
14. Cardenas M. E., Hemenway C., Muir R. S., Ye R., Fiorentino D., Heitman J. Immunophilins interact with calcineurin in the absence of exogenous immunosuppressive ligands. EMBO J. 13:1994;5944-5957.
15. Carrière C., Gay B., Chazal N., Morin N., Boulanger P. Sequence requirements for encapsidation of deletion mutants and chimeras of human immunodeficiency virus type 1 Gag precursor into retrovirus-like particles. J. Virol. 69:1995;2366-2377.
16. Chang H.-C. J., Lindquist S. Conservation of Hsp90 macromolecular complexes in Saccharomyces cerevisiae. J. Biol. Chem. 269:1994;24983-24988.
17. Chazal N., Carriére C., Gay B., Boulanger P. Phenotypic characterization of insertion mutants of the human immunodeficiency virus type 1 Gag precursor expressed in recombinant baculovirus-infected cells. J. Virol. 68:1994;111-122.
18. Colgan J., Yuan H. E. H., Franke E. K., Luban J. Binding of the human immunodeficiency virus type 1 Gag polyprotein to cyclophilin A is mediated by the central region of capsid and requires Gag dimerization. J. Virol. 70:1996;4299-4310.
19. Colley N. J., Baker E. K., Stamnes M. A., Zuker C. S. The cyclophilin homolog ninaA is required in the secretory pathway. Cell. 67:1991;255-263.
20. Davis E. S., Becker A., Heitman J., Hall M. N., Brennan M. B. A yeast cyclophilin gene essential for lactate metabolism at high temperature. Proc. Natl Acad. Sci. USA. 89:1992;11169-11173.
21. Di Marzo Veronese F., Copeland T. D., Oroszlan S., Gallo R. C., Sarngadharan M. G. Biochemical and immunological analysis of human immunodeficiency virus gag gene products p17 and p24. J. Virol. 62:1988;795-801.
22. Dorfman T., Göttlinger H. G. The human immunodeficiency virus type 1 capsid p2 domain confers sensitivity to the cyclophilin-binding drug SDZ NIM 811. J. Virol. 70:1996;5751-5757.
23. Dorfman T., Bukovsky A., Öhagen Å., Högland S., Göttlinger H. G. Functional domains of the capsid protein of human immunodeficiency virus type 1. J. Virol. 68:1994;8180-8187.
24. Duina A. A., Change H.-C. J., Marsh J. A., Lindquist S., Gaber R. F. A cyclophilin function in Hsp90-dependent signal transduction. Science. 274:1996;1713-1715.
25. Ehrlich L. S., Agresta B. E., Carter C. A. Assembly of recombinant human immunodeficiency virus type 1 capsid protein in vitro. J. Virol. 66:1992;4874-4883.
26. Ehrlich L. S., Agresta B. E., Gelfand C. A., Jentoft J., Carter C. A. Spectral analysis and tryptic susceptibility as probes of HIV-1 capsid protein structure. Virology. 204:1994;515-525.
27. Ferreira P. A., Nakayama T. A., Pak W. L., Travis G. H. Cyclophilin-related protein RanBP2 acts as a chaperone for red/green opsin. Nature. 383:1996;637-640.
28. Fischer G., Wittmann-Liebold B., Lang K., Kiefhaber T., Schmid F. X. Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature. 337:1989;476-478.
29. Fisher H. F., Singh N. Calorimetric methods for interpreting protein-ligand interactions. Methods Enzymol. 259:1995;194-221.
30. Franke E. K., Luban J. Cyclophilin and Gag in HIV-1 replication and pathogenesis. Cell Activation and Apoptosis in HIV Infection. 1995;Plenum Press, New York.
31. Franke E. K., Yuan H. E. H., Bossolt K. L., Goff S. P., Luban J. Specificity and sequence requirements for interactions between various retroviral Gag proteins. J. Virol. 68:1994a;5300-5303.
32. Franke E. K., Yuan H. E. H., Luban J. Specific incorporation of cyclophilin A into HIV-1 virions. Nature. 372:1994b;359-362.
33. Freeman B. C., Toft D. O., Morimoto R. I. Molecular chaperone machines: chaperone activities of the cyclophilin Cyp-40 and the steroid aporeceptor-associated protein p23. Science. 274:1996;1718-1720.
34. Freskgård P.-O., Bergenhem N., Jonsson B.-H., Svensson M., Carlsson U. Isomerase and chaperone activity of prolyl isomerase in the folding of carbonic anhydrase. Science. 258:1992;466-468.
35. Friedman J., Trahey M., Weissman I. Cloning and characterization of cyclophilin C-associated protein: a candidate natural cellular ligand for cyclophilin C. Proc. Natl. Acad. Sci. USA. 90:1993;6815-6819.
36. Gamble T., Vajdos F., Yoo S., Worthylake D., Houseweart M., Sundquist W. I., Hill C. P. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell. 87:1996;1285-1294.
37. Gelderblom H. R., Bauer P. G., Özel M., Höglund S., Niedrig M., Renz H., Morath B., Lundquist P., Nilsson Å., Mattow J., Grund C., Pauli G. Morphogenesis and morphology of human immunodeficiency virus. Aloa R. C., Curtain C. C. Membrane Interactions of HIV. 1992;Wiley-Liss, Inc. New York.
38. Gitti R. K., Lee B. M., Walker J., Summers M. F., Yoo S., Sundquist W. I. Structure of the amino-terminal core domain of the HIV-1 capsid protein. Science. 273:1996;231-235.
39. Haendler B., Hofer-Warbinek R., Hofer E. Complementary DNA for human T-cell cyclophilin. EMBO J. 6:1987;947-950.
40. Handschumacher R. E., Harding M. W., Rice J., Drugge R. J. Cyclophilin: a specific cytosolic binding protein for cyclosporin A. Science. 226:1984;544-547.
41. Harrison R. K., Stein R. L. Substrate specificities of the peptidyl prolyl cis-trans isomerase activities of cyclophilin and FK-506 binding protein: evidence for the existence of a family of distinct enzymes. Biochemistry. 29:1990;3813-3816.
42. Helekar S. A., Char D., Neff S., Patrick J. Prolyl isomerase requirement for the expression of functional homo-oligomeric ligand-gated ion channels. Neuron. 12:1994;179-189.
43. Henderson L. E., Bowers M. A., Sowder R. C., II, Serabyn S. A., Johnson D. G., Bess J. W. Jr, Arthur L. O., Bryant D. K., Fenselau C. Gag proteins of the highly replicative MN strain of human immunodeficiency virus type 1: posttranslational modifications, proteolytic processings, and complete amino acid seqences. J. Virol. 66:1992;1856-1865.
44. Hong S. S., Boulanger P. Assembly-defective point mutants of the human immunodeficiency virus type 1 Gag precursor phenotypically expressed in recombinant baculovirus-infected cells. J. Virol. 67:1993;2787-2798.
45. Hunter E. Macromolecular interactions in the assembly of HIV and other retroviruses. Sem. Virol. 5:1994;71-83.
46. Jackson S. E., Ferscht A. R. Folding of chymotrypsin inhibitor 2. 2. Influence of proline isomerization on the folding kinetics and thermodynamic characterization of the transition state of folding. Biochemistry. 30:1991;10436-10443.
47. Jönsson U., Fägerstam L., Ivarsson B., Johnsson B., Karlsson R., Lundh K., Löfås S., Persson B., Roos H., Rönnberg I., Sjölander S., Stenberg E., Ståhlberg R., Urbaniczky C., Östlin H., Malmqvist M. Real-time biospecific interaction analysis using surface plasmon resonance and a sensor chip technology. BioTechniques. 193:1991;620-627.
48. Jowett J., Hockley D., Nermut M. V., Jones I. M. Distinct signals in human immunodeficiency virus type 1 Pr55 necessary for RNA binding and particle formation. J. Gen. Virol. 73:1992;3079-3086.
49. Kakalis L. T., Armitage I. M. Solution conformation of a cyclophilin-bound proline isomerase substrate. Biochemistry. 33:1994;1495-1501.
50. Kallen J., Walkinshaw M. D. The X-ray structure of a tetrapeptide bound to the active site of human cyclophilin A. FEBS Leters. 300:1992;286-290.
51. Ke H. M., Zydowsky L. D., Liu J., Walsh C. T. Crystal structure of recombinant human T-cell cyclophilin A at 2.5 Å resolution. Proc. Natl Acad. Sci. USA. 88:1991;9483-9487.
52. Ke H., Mayrose D., Cao W. Crystal structure of cyclophilin A complexed with substrate Ala-Pro suggests a solvent-assisted mechanism ofcis-trans isomerization. Proc. Natl Acad. Sci. USA. 90:1993;3324-3328.
53. Koletsky A. J., Harding M. W., Handschumacher R. E. Cyclophilin: distribution and variant properties in normal and neoplastic tissues. J. Immunol. 137:1986;1054-1059.
54. Kräusslich H.-G. Morphogenesis and maturation of retroviruses. Curr. Topics Microbiol. Immunol. 214:1996.
55. Kunkel T. A., Roberts J. D., Zakour R. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154:1987;367-382.
56. Kunz J., Hall M. N. Cyclosporin A, FK506, and rapamycin: more than just immunosuppression. Trends Biochem. Sci. 18:1993;334-338.
57. Laue T. M., Shah B. D., Ridgeway T. M., Pelletier S. L. Computer-aided interpretation of analytical sedimentation data for proteins. Rowe A. J., Horton J. C. Analytical Ultracentrifugation in Biochemistry and Polymer Science. 1992;Royal Society of Chemistry, Cambridge.
58. Lilie H., Lang K., Rudolph R., Buchner J. Prolyl isomerases catalyze antibody folding in vitro. Protein Sci. 2:1993;1490-1496.
59. Liu J., Albers M. W., Chen C.-M., Schreiber S. L., Walsh C. T. Cloning, expression, and purification of human cyclophilin in Escherichia coli and assessment of the catalytic role of cysteines by site-directed mutagenesis. Proc. Natl Acad. Sci. USA. 87:1990;2304-2308.
60. Lodish H., Kong N. Cyclosporin a inhibits an initial step in folding of transferrin within the endoplasmic reticulum. J. Biol. Chem. 266:1991;14835-14838.
61. Löfås S., Johnsson B. A novel hydrogel matrix on gold surface plasmon resonance sensors for fast and efficient covalent immobilization of ligands. J. Chem. Soc. Chem. Commun. 21:1990;1526-1528.
62. Luban J., Bossolt K. L., Franke E. K., Kalpana G. V., Goff S. P. Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Cell. 73:1993;1067-1078.
63. Malmqvist M. Surface plasmon resonance for detection and measurement of antibody-antigen affinity and kinetics. Curr. Opin. Immunol. 5:1993;282-286.
64. Mammano F., Öhagen Å., Höglund S., Göttlinger H. G. Role of the major homology region of HIV-1 in virion morphogenesis. J. Virol. 68:1994;4927-4936.
65. McRorie D. K., Voelker P. J. Self-associating Systems in the Analytical Ultracentrifuge. 1993;Beckman Instruments Inc. Fullerton.
66. Momany C., Kovari L. C., Prongay A. J., Keller W., Gitti R. K., Lee B. M., Gorbalenya A. E., Tong L., McClure J., Ehrlich L. S., Summers M. F., Carter C., Rossmann M. G. Crystal structure of dimeric HIV-1 capsid protein. Nature Struct. Biol. 3:1996;763-770.
67. Morton T. A., Myszka D. G., Chaiken I. M. Interpreting complex binding kinetics from optical biosensors: a comparison of analysis by linearization, the integrated rate equation, and numerical integration. Anal. Biochem. 227:1995;176-185.
68. Myers G., Korber B., Hahn B. H., Jeang K.-T., Mellors J. W., McCutchan F. E., Henderson L. E., Pavlakis G. N. Human Retroviruses and AIDS 1995. 1995;Los Alamos National Laboratory, Los Alamos, NM.
69. O'Shannessy D. J., Winzor D. J. Interpretation of deviations from pseudo-first-order kinetic behavior in the characterization of ligand binding by biosensor technology. Anal. Biochem. 236:1996;275-283.
70. Ondek B., Hardy R. W., Baker E. K., Stamnes M. A., Shieh B.-H., Zuker C. S. Genetic dissection of cyclophilin function. J. Biol. Chem. 267:1992;16460-16466.
71. Ott D. E., Coren L. V., Johnson D. G., Sowder R. C. I., Arthur L. O., Henderson L. E. Analysis and localization of cyclophilin a found in the virions of human immunodeficiency virus type 1 MN strain. AIDS Res. Hum. Retro. 11:1995;1003-1006.
72. Ratajczak T., Carrello A., Mark P. J., Warner B. J., Simpson R. J., Moritz R. L., House A. K. The cyclophilin component of the unactivated estrogen receptor contains a tetratricopeptide repeat domain and shares identity with p59 (FKBP59). J. Biol. Chem. 268:1993;13187-13192.
73. Reicin A. S., Paik S., Berkowitz R. D., Luban J., Lowy I., Goff S. P. Linker insertion mutations in the human immunodeficiency virus type 1 gag gene: effects on virion particle assembly, release, and infectivity. J. Virol. 69:1995;642-650.
74. Rosé S., Hensley P., O'Shannessy D. J., Culp J., Debouck C., Chaiken I. Characterization of HIV-1 p24 self-association using analytical affinity chromatography. Proteins: Struct. Funct. Genet. 13:1992;112-119.
75. Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning: A Laboratory Manual. 2nd edit., 1989;Cold Spring Harbor Laboratory Press, Plainview.
76. Schmid F. X. Prolyl isomerases: role in protein folding. Advan. Protein Sci. 44:1993;25-66.
77. Schmid R. X., Baldwin R. Acid catalysis of the formation of the slow folding species of RNase a: evidence that the reaction is proline isomerization. Proc. Natl Acad. Sci. USA. 75:1978;4764-4768.
78. Schneuwly S., Shortridge R. D., Larrivee D. C., Ono T., Ozaki M., Pak W. L. Drosophila ninaA gene encodes an eye-specific cyclophilin (cyclosporin A binding protein). Proc. Natl Acad. Sci. USA. 86:1989;5390-5394.
79. Schreiber S. L., Crabtree G. R. The mechanism of action of cyclosporin A and FK506. Immunol. Today. 13:1992;136-142.
80. Shieh B.-H., Stamnes M. A., Seavello S., Harris G. L., Zuker C. S. The ninaA gene required for visual transduction in Drosophila encodes a homologue of cyclosporin A-binding protein. Nature. 338:1989;67-70.
81. Srinivasakumar N., Hammarskjöld M.-L., Rekosh D. Characterization of deletion mutations in the capsid region of human immunodeficiency virus type 1 that affect particle formation and gag-pol precursor incorporation. J. Virol. 69:1995;6106-6114.
82. Stamnes M. A., Rutherford S. L., Zuker C. S. Cyclophilins: a new family of proteins involved in intracellular folding. Trends Cell Biol. 2:1992;272-276.
83. Steinkasserer A., Harrison R., Billich A., Hammerschmid F., Werner G., Wolff B., Peichl P., Palfi G., Schnitzel W., Mlynar E., Rosenwirth B. Mode of action of SDZ NIM 811, a nonimmunosuppressive cyclosporin A analog with activity against human immunodeficiency virus type 1 (HIV-1): interference with early and late events in HIV-1 replication. J. Virol. 69:1995;814-824.
84. Studier F. W., Rosenberg A. H., Dunn J. J., Dubendorff J. W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185:1990;60-89.
85. Sykes K., Gething M.-J., Sambrook J. Proline isomerases function during heat shock. Proc. Natl Acad. Sci. USA. 90:1993;5853-5857.
86. Takahashi N., Hayano T., Suzuki M. Peptidyl-prolyl cis-trans isomerase is the cyclosporin A-binding protein cyclophilin. Nature. 337:1989;473-475.
87. Thali M., Bukovsky A., Kondo E., Rosenwirth B., Walsh C. T., Sodroski J., Göttlinger H. G. Functional association of cyclophilin A with HIV-1 virions. Nature. 372:1994;363-365.
88. von Poblotzki A., Wagner R., Niedrig M., Wanner G., Wolf H., Modrow S. Identification of a region in the Pr55 gag polyprotein essential for HIV-1 particle formation. Virology. 193:1993;981-985.
89. Walsh C. T., Zydowsky L. D., McKeon F. D. Cyclosporin A, the cyclophilin class of peptidylprolyl isomerases, and blockade of T-cell signal transduction. J. Biol. Chem. 267:1992;13115-13118.
90. Wang C.-T., Barklis E. Assembly, processing, and infectivity of human immunodeficiency virus type 1 Gag mutants. J. Virol. 67:1993;4264-4273.
91. Weisman R., Creanor J., Fantes P. A multicopy suppressor of a cell cycle defect in S. pombe encodes a heat shock-inducible 40 kDa cyclophilin-like protein. EMBO J. 15:1996;447-456.
92. Wills J., Craven R. Form, function, and use of retroviral Gag proteins. AIDS. 5:1991;639-654.
93. Wiseman T., Williston S., Brandts J. F., Lin L.-N. Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal. Biochem. 179:1989;131-137.
94. Xu Q., Leiva M. C., Fischkoff S. A., Handschumacher R. E., Lyttle C. R. Leukocyte chemotactic activity of cyclophilin. J. Biol. Chem. 267:1992;11968-11971.
95. Zhang W.-H., Hockley D. J., Nermut M. V., Morikawa Y., Jones I. M. Gag-gag interactions in the C-terminal domain of human immunodeficiency virus type 1 p24 capsid antigen are essential for Gag particle assembly. J. Gen. Virol. 77:1996;743-751.
96. Zhao Y., Ke H. Crystal structure implies that cyclophilin predominantly catalyzes the trans to cis isomerization. Biochemistry. 35:1996a;7356-7361.
97. Zhao Y., Ke H. Mechanistic implication of crystal structures of the cyclophilin-dipeptide complexes. Biochemistry. 35:1996b;7362-7368.
98. Zhao Y., Jones I. M., Hockley D. J., Nermut M. V., Roy P. Complementation of human immunodeficiency virus (HIV-1) Gag particle formation. Virology. 199:1994;403-408.