Hydrophobicity: An ancient damage-associated molecular pattern that initiates innate immune responses

Nature Reviews Immunology

Volumn 4, Issue 6, 2004, Pages 469-478

  Seong, Seung Yong ^a   Matzinger, Polly ^b  

^a Seoul National University College of Medicine   (South Korea)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOLOGICAL ADJUVANT; IMMUNOSTIMULATING AGENT; LIGAND; LIPOARABINOMANNAN; LIPOPOLYSACCHARIDE; PEPTIDOGLYCAN; TOLL LIKE RECEPTOR;

ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; BIOACCUMULATION; CHEMICAL STRUCTURE; EXTRACELLULAR MATRIX; HUMAN; HYDROPHOBICITY; IMMUNE RESPONSE; IMMUNITY; IMMUNOSTIMULATION; MOLECULAR BIOLOGY; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; MOLECULAR STABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; TISSUE REGENERATION; TISSUE REPAIR;

EID: 2942627626     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri1372     Document Type: Review

References (127)

1. Janeway, C. A., Jr. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 54, 1-13 (1989).
2. Matzinger, P. Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12, 991-1045 (1994).
3. Brightbill, H. D. et al. Host defense mechanisms triggered by microbial lipoproteins through Toll-like receptors. Science 285, 732-736 (1999).
4. Gallucci, S., Lolkema, M. & Matzinger, P. Natural adjuvants: endogenous activators of dendritic cells. Nature Med. 5, 1249-1255 (1999).
5. Medzhitov, R. & Janeway, C. A., Jr. Decoding the patterns of self and nonself by the innate immune system. Science 296, 298-300 (2002).
6. Janeway, C. A., Jr. & Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol. 20, 197-216 (2002).
7. Termeer, C. et al. Oligosaccharides of hyaluronan activate dendritic cells via toll-like receptor 4. J. Exp. Med. 195, 99-111 (2002).
8. Asea, A. et al. Novel signal transduction pathway utilized by extracellular HSP70: role of toll-like receptor (TLR) 2 and TLR4. J. Biol. Chem. 277, 15028-15034 (2002).
9. Guillot, L. et al. Cutting edge: the immunostimulatory activity of the lung surfactant protein-A involves Toll-like receptor 4. J. Immunol. 168, 5989-5992 (2002).
10. Shi, Y., Evans, J. E. & Rock, K. L. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425, 516-521 (2003).
11. Okamura, Y. et al. The extra domain A of fibronectin activates Toll-like receptor 4. J. Biol. Chem. 276, 10229-10233 (2001).
12. Biragyn, A. et al. Toll-like receptor 4-dependent activation of dendritic cells by β-defensin 2. Science 298, 1025-1029 (2002).
13. Peitsch, M. C., Tschopp, J., Kress, A. & Isliker, H. Antibody-independent activation of the complement system by mitochondria is mediated by cardiolipin. Biochem. J. 249, 495-500 (1988).
14. Bausinger, H. et al. Endotoxin-free heat-shock protein 70 fails to induce APC activation. Eur. J. Immunol. 32, 3708-3713 (2002).
15. Wallin, R. P. et al. Heat-shock proteins as activators of the innate immune system. Trends Immunol. 23, 130-135 (2002).
16. Dembic, Z. Immune system protects integrity of tissues. Mol. Immunol. 37, 563-569 (2000).
17. Wahl, L. M., Shankavaram, U. & Zhang, Y. Role of macrophages in vascular tissue remodelling. Transpl. Immunol. 5, 173-176 (1997).
18. Takeda, K., Kaisho, T. & Akira, S. Toll-like receptors. Annu. Rev. Immunol. 21, 335-376 (2003).
19. Sugiyama, T. & Wright, S. D. Soluble CD14 mediates efflux of phospholipids from cells. J. Immunol. 166, 826-831 (2001).
20. Wang, P. Y. & Munford, R. S. CD14-dependent internalization and metabolism of extracellular phosphatidylinositol by monocytes. J. Biol. Chem. 274, 23236-23241 (1999).
21. Callahan, M. K. et al. Phosphatidylserine expression and phagocytosis of apoptotic thymocytes during differentiation of monocytic cells. J. Leukoc. Biol. 74, 846-56 (2003).
22. Stover, A. G. et al. Structure-activity relationship of synthetic Toll-like receptor 4 agonists. J. Biol. Chem. 219, 4440-4449 (2004).
23. Bell, J. K. et al. Leucine-rich repeats and pathogen recognition in Toll-like receptors. Trends Immunol. 24, 528-533 (2003).
24. Jones, E. Y. MHC class I and class II structures. Curr. Opin. Immunol. 9, 75-79 (1997).
25. Sinha, N. & Smith-Gill, S. J. Electrostatics in protein binding and function. Curr. Protein Pept. Sci. 3, 601-614 (2002).
26. Hashimoto, M. et al. Chemical structure and immunobiological activity of lipid A from Prevotella intermedia ATCC 25611 lipopolysaccharide. FEBS Lett. 543, 98-102 (2003).
27. Steinberg, M. H. & Rodgers, G. P. Pathophysiology of sickle cell disease: role of cellular and genetic modifiers. Semin. Hematol. 38, 299-306 (2001).
28. Minton, A. P. The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media. J. Biol. Chem. 276, 10577-10580 (2001).
29. Agashe, V. R. & Hartl, F. U. Roles of molecular chaperones in cytoplasmic protein folding. Semin. Cell. Dev. Biol. 11, 15-25 (2000).
30. Ben-Zvi, A. P. & Goloubinoff, P. Mechanisms of disaggregation and refolding of stable protein aggregates by molecular chaperones. J. Struct. Biol. 135, 84-93 (2001).
31. Glotzer, J. B. et al. Activation of heat-shock response by an adenovirus is essential for virus replication. Nature 407, 207-211 (2000).
32. Kourie, J. I. & Henry, C. L. Ion channel formation and membrane-linked pathologies of misfolded hydrophobic proteins: the role of dangerous unchaperoned molecules. Clin. Exp. Pharmacol. Physiol. 29, 741-753 (2002).
33. Kuroki, Y. et al. A novel type of binding specificity to phospholipids for rat mannose-binding proteins isolated from serum and liver. FEBS Lett. 414, 387-392 (1997).
34. de Beer, M. C. et al. Apolipoprotein A-II modulates the binding and selective lipid uptake of reconstituted high density lipoprotein by scavenger receptor B1. J. Biol. Chem. 276, 15832-15839 (2001).
35. Vandivier, R. W. et al. Role of surfactant proteins A, D, and C1q in the clearance of apoptotic cells in vivo and in vitro: calreticulin and CD91 as a common collectin receptor complex. J. Immunol. 169, 3978-3986 (2002).
36. Marcel, Y. L. & Kiss, R. S. Structure-function relationships of apolipoprotein A-I: a flexible protein with dynamic lipid associations. Curr. Opin. Lipidol. 14, 151-157 (2003).
37. Borst, P., Zelcer, N. & van Helvoort, A. ABC transporters in lipid transport. Biochim. Biophys. Acta 1486, 128-144 (2000).
38. Inohara, N. & Nunez, G. NODs: intracellular proteins involved in inflammation and apoptosis. Nature Rev Immunol. 3, 371-382 (2003).
39. Krantz, D. D., Zidovetzki, R., Kagan, B. L. & Zipursky, S. L. Amphipathic β structure of a leucine-rich repeat peptide. J. Biol. Chem. 266, 16801-16807 (1991).
40. Hunter, R., Strickland, F. & Kezdy, F. The adjuvant activity of nonionic block polymer surfactants. I. The role of hydrophile-lipophile balance. J. Immunol. 127, 1244-1250 (1981).
41. Nishiguchi, M. et al. Mycoplasma fermentans lipoprotein M181Ag-induced cell activation is mediated by Toll-like receptor 2: role of N-terminal hydrophobic portion in its multiple functions. J. Immunol. 166, 2610-2616 (2001).
42. Kurt-Jones, E. A. et al. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nature Immunol. 1, 398-401 (2000).
43. Koka, R. M., Huang, E. & Lieske, J. C. Adhesion of uric acid crystals to the surface of renal epithelial cells. Am. J. Physiol. Renal Physiol. 278, F989-F998 (2000).
44. Hristova, K., Selsted, M. E. & White, S. H. Critical role of lipid composition in membrane permeabilization by rabbit neutrophil defensins. J. Biol. Chem. 272, 24224-24233 (1997).
45. Burston, S. G. & Clarke, A. R. Molecular chaperones: physical and mechanistic properties. Essays Biochem. 29, 125-136 (1995).
46. Stromer, T., Ehrnsperger, M., Gaestel, M. & Buchner, J. Analysis of the interaction of small heat shock proteins with unfolding proteins. J. Biol. Chem. 278, 18015-18021 (2003).
47. Surin, A. K., Kotova, N. V., Marchenkova, S., Marchenkov, V. V. & Semisotnov, G. V. Monomeric form of the molecular chaperone GroEL: structure, stability, and oligomerization. Bioorg. Khim. 25, 358-364 (1999) (in Russian).
48. Gorovits, B. M. & Horowitz, P. M. The chaperonin GroEL is destabilized by binding of ADP. J. Biol. Chem. 270, 28551-28556 (1995).
49. Lapcik, L., Jr, Lapcik, L., De Smedt, S., Demeester, J. & Chabrecek, P. Hyaluronan: preparation, structure, properties, and applications. Chem. Rev. 98, 2663-2684 (1998).
50. Srimal, S., Surolia, N., Balasubramanian, S. & Surolia, A. Titration calorimetric studies to elucidate the specificity of the interactions of polymyxin B with lipopolysaccharides and lipid A. Biochem. J. 315, 679-686 (1996).
51. Katz, M. et al. Lipid binding and membrane penetration of polymyxin B derivatives studied in a biomimetic vesicle system. Biochem. J. 375,405-413 (2003).
52. Thorbecke, G. J. & Benacerraf, B. Tolerance in adult rabbits by repeated non-immunogenic doses of bovine serum albumin. Immunology 13, 141-145 (1967).
53. Golub, E. S. & Weigle, W. O. Studies on the induction of immunologic unresponsiveness. 3. Antigen form and mouse strain variation. J. Immunol. 102, 389-396 (1969).
54. + T cell response to factor VII in hemophilia A, acquired hemophilia, and healthy subjects. Thromb. Haemost. 82, 509-515 (1999).
55. Saenko, E. L., Shima, M. & Sarafanov, A. G. Role of activation of the coagulation factor VIII in interaction with vWf, phospholipid, and functioning within the factor Xase complex. Trends Cardiovasc. Med. 9, 185-192 (1999).
56. Barrick, J. E. & Roberts, R. W. Sequence analysis of an artificial family of RNA-binding peptides. Protein Sci. 11, 2688-2696 (2002).
57. Heil, F. et al. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303, 1526-1529 (2004).
58. Matsumoto, M., Kikkawa, S., Kohase, M., Miyake, K. & Seya, T. Establishment of a monoclonal antibody against human Toll-like receptor 3 that blocks double-stranded RNA-mediated signaling. Biochem. Biophys. Res. Commun. 293, 1364-1369 (2002).
59. Kishore, U. & Reid, K. B. Structures and functions of mammalian collectins. Results Probl. Cell Differ. 33, 225-248 (2001).
60. Seifert, P. S. et al. Isolation and characterization of a complement-activating lipid extracted from human atherosclerotic lesions. J. Exp. Med. 172, 547-557 (1990).
61. Kairies, N. et al. The 2.0-A crystal structure of tachylectin 5A provides evidence for the common origin of the innate immunity and the blood coagulation systems. Proc. Natl Acad. Sci. USA 98, 13519-13524 (2001).
62. Retzinger, G. S., DeAnglis, A. P. & Patuto, S. J. Adsorption of fibrinogen to droplets of liquid hydrophobic phases. Functionality of the bound protein and biological implications. Arterioscler Thromb. Vasc. Biol. 18, 1948-1957 (1998).
63. Hailman, E. et al. Lipopolysaccharide (LPS)-binding protein accelerates the binding of LPS to CD14. J. Exp. Med. 179, 269-277 (1994).
64. Muta, T. & Takeshige, K. Essential roles of CD14 and lipopolysaccharide-binding protein for activation of toll-like receptor (TLR)2 as well as TLR4. Reconstitution of TLR2- and TLR4-activation by distinguishable ligands in LPS preparations. Eur. J. Biochem. 266, 4580-4589 (2001).
65. Yu, B., Hailman, E. & Wright, S. D. Lipopolysaccharide binding protein and soluble CD14 catalyze exchange of phospholipids. J. Clin. Invest. 99, 315-324 (1997).
66. Gregory, C. D. & Devitt, A. CD14 and apoptosis. Apoptosis 4, 11-20 (1999).
67. Schlegel, R. A., Callahan, M. K. & Williamson, P. The central role of phosphatidylsedne in the phagocytosis of apoptotic thymocytes. Ann. NY Acad. Sci. 926, 217-225 (2000).
68. van Oss, C. J. Phagocytosis as a surface phenomenon. Annu. Rev. Microbiol. 32, 19-39 (1978).
69. McEvoy, L., Williamson, P. & Schlegel, R. A. Membrane phospholipid asymmetry as a determinant of erythrocyte recognition by macrophages. Proc. Natl Acad. Sci. USA 83, 3311-3315(1986).
70. Schlegel, R. A., Krahling, S., Callahan, M. K. & Williamson, P. CD14 is a component of multiple recognition systems used by macrophages to phagocytose apoptotic lymphocytes. Cell Death Differ. 6, 583-592 (1999).
71. Thompson, D., Pepys, M. B. & Wood, S. P. The physiological structure of human C-reactive protein and its complex with phosphocholine. Structure Fold. Des. 7, 169-177 (1999).
72. Gershov, D., Kim, S., Brot, N. & Elkon, K. B. C-reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an antiinflammatory innate immune response: implications for systemic autoimmunity. J. Exp. Med. 192, 1353-1364 (2000).
73. Platt, N., da Silva, R. P. & Gordon, S. Class A scavenger receptors and the phagocytosis of apoptotic cells. Immunol. Lett. 65, 15-19 (1999).
74. Platt, N. & Gordon, S. Is the class A macrophage scavenger receptor (SR-A) multifunctional? The mouse's tale. J. Clin. Invest. 108, 649-654 (2001).
75. Janabi, M. et al. Oxidized LDL-induced NF-βB activation and subsequent expression of proinflammatory genes are defective in monocyte-derived macrophages from CD36-deficient patients. Arterioscler. Thromb. Vasc. Biol. 20, 1953-1960 (2000).
76. Krieger, M. Molecular flypaper and atherosclerosis: structure of the macrophage scavenger receptor. Trends Biochem. Sci. 17, 141-146 (1992).
77. Coraci, I. S. et al. CD36, a class B scavenger receptor, is expressed on microglia in Alzheimer's disease brains and can mediate production of reactive oxygen species in response to β-amyloid fibrils. Am. J. Pathol. 160, 101-112 (2002).
78. Terpstra, V., Bird, D. A. & Steinberg, D. Evidence that the lipid moiety of oxidized low density lipoprotein plays a role in its interaction with macrophage receptors. Proc. Natl Acad. Sci. USA 95, 1806-1811 (1998).
79. Rutschmann, S., Kilinc, A. & Ferrandon, D. Cutting edge: the toll pathway is required for resistance to Gram-positive bacterial infections in Drosophila. J. Immunol. 168, 1542-1546 (2002).
80. Kiechl, S., Wiedermann, C. J. & Willeit, J. Toll-like receptor 4 and atherogenesis. Ann. Med. 35, 164-171 (2003).
81. Muta, T. & Iwanaga, S. The role of hemolymph coagulation in innate immunity. Curr. Opin. Immunol. 8, 41-47 (1996).
82. Haziot, A. et al. Resistance to endotoxin shock and reduced dissemination of Gram-negative bacteria in CD14-deficient mice. Immunity 4, 407-414 (1996).
83. Yamada, Y., Doi, T., Hamakubo, T. & Kodama, T. Scavenger receptor family proteins: roles for atherosclerosis, host defence and disorders of the central nervous system. Cell. Mol. Life Sci. 54, 628-640 (1998).
84. Urban, B. C. et al. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 400, 73-77 (1999).
85. Finney, J. L. The Structural Basis of the Hydrophobic Interaction (ed. Bellissent-Funel, M.-C.) (IOS press, 1999).
86. Berezovskyi, I. N. & Trifono, E. Protein structure and folding: a new start. J. Biomol. Struct. Dyn. 19, 397-403 (2001).
87. Eisenberg, D. & McLachlan, A. D. Solvation energy in protein folding and binding. Nature 319, 199-203 (1986).
88. Borsos, T. Immune complex mediated activation of the classical complement pathway. Behring Inst. Mitt. 84, 93-101 (1989).
89. Storrs, S. B., Kolb, W. P. & Olson, M. S. C1q binding and C1 activation by various isolated cellular membranes. J. Immunol. 131, 416-422 (1983).
90. Martin, J. Protein folding assisted by the GroEL/GroES chaperonin system. Biochemistry (Mosc) 63, 374-381 (1998).
91. Molina, A. & Garcia-Olmedo, F. Developmental and pathogen-induced expression of three barley genes encoding lipid transfer proteins. Plant J. 4, 983-991 (1993).
92. Guiderdoni, E. et al. Inducibility by pathogen attack and developmental regulation of the rice Ltp1 gene. Plant Mol. Biol. 49, 683-699 (2002).
93. Bonas, U. & Lahaye, T. Plant disease resistance triggered by pathogen-derived molecules: refined models of specific recognition. Curr. Opin. Microbiol. 5, 44-50 (2002).
94. Niere, M., Dettloff, M., Maier, T., Ziegler, M. & Wiesner, A. Insect immune activation by apolipophorin III is correlated with the lipid-binding properties of this protein. Biochemistry 40, 11502-11508 (2001).
95. Bergner, A. et al. Crystal structure of a coagulogen, the clotting protein from horseshoe crab: a structural homologue of nerve growth factor. EMBO J. 15, 6789-6797 (1996).
96. Zhou, D. et al. Editing of Cd1d-bound lipid antigens by endosomal lipid transfer proteins. Science 303, 523-527 (2004).
97. Verjans, G. M., van Hagen, P. M., van der Kooi, A., Osterhaus, A. D. & Baarsma, G. S. Vγ9Vδ2 T cells recovered from eyes of patients with Behcet's disease recognize non-peptide prenyl pyrophosphate antigens. J. Neuroimmunol. 130, 46-54 (2002).
98. Vance, D. E. & Van den Bosch, H. Cholesterol in the year 2000. Biochim. Biophys. Acta 1529, 1-8 (2000).
99. Neuhaus, F. C. & Baddiley, J. A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol. Mol. Biol. Rev. 67, 686-723 (2003).
100. Smith, K. D. et al. Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nature Immunol. 4, 1247-1253 (2003).
101. Cheng, V. C. et al. Clinical spectrum of paradoxical deterioration during antituberculosis therapy in non-HIV-infected patients. Eur. J. Clin. Microbiol. Infect. Dis. 21, 803-809 (2002).
102. Ofori, M. F. et al. Malaria-induced acquisition of antibodies to Plasmodium falciparum variant surface antigens. Infect. Immun. 70, 2982-2988 (2002).
103. Lawrence, T., Willoughby, D. A. & Gilroy, D. W. Anti-inflammatory lipid mediators and insights into the resolution of inflammation. Nature Rev. Immunol. 2, 787-795 (2002).
104. Golenbock, D. T., Hampton, R. Y., Qureshi, N., Takayama, K. & Raetz, C. R. Lipid A-like molecules that antagonize the effects of endotoxins on human monocytes. J. Biol. Chem. 266, 19490-19498 (1991).
105. Schromm, A. B. et al. Biological activities of lipopolysaccharides are determined by the shape of their lipid A portion. Eur. J. Biochem. 267, 2008-2013 (2000).
106. Brandenburg, K. et al. Influence of the supramolecular structure of free lipid A on its biological activity. Eur. J. Biochem. 218, 555-563 (1993).
107. Seydel, U., Brandenburg, K., Koch, M. H. & Rietschel, E. T. Supramolecular structure of lipopolysaccharide and free lipid A under physiological conditions as determined by synchrotron small-angle X-ray diffraction. Eur. J. Biochem. 166, 325-332 (1989).
108. Seydel, U., Oikawa, M., Fukase, K., Kusumoto, S. & Brandenburg, K. Intrinsic conformation of lipid A is responsible for agonistic and antagonistic activity. Eur. J. Biochem. 267, 3032-3039 (2000).
109. Seydel, U. et al. The generalized endotoxic principle. Eur. J. Immunol. 33, 1586-1592 (2003).
110. Hofmann, A. F. & Roda, A. Physicochemical properties of bile acids and their relationship to biological properties: an overview of the problem. J. Lipid Res. 25, 1477-1489 (1984).
111. Pison, U., Ma, M., Neuendank, A., Weissbach, S. & Pietschmann, S. Host defence capacities of pulmonary surfactant: evidence for 'non-surfactant' functions of the surfactant system. Eur. J. Clin. Invest. 24, 586-599 (1994).
112. Hailman, E., Albers, J. J., Wollbauer, G., Tu, A. Y. & Wright, S. D. Neutralization and transfer of lipopolysaccharide by phospholipid transfer protein. J. Biol. Chem. 271, 12172-12178 (1996).
113. Vreugdenhil, A. C. et al. Lipopolysaccharide (LPS)-binding protein mediates LPS detoxification by chylomicrons. J. Immunol. 170, 1399-1405 (2003).
114. Kasravi, F. B., Brecht, W. J., Weisgraber, K. H. & Harris, H. W. Induction of cytokine tolerance requires internalization of chylomicron-bound LPS into hepatocytes. J. Surg. Res. 115, 303-309 (2003).
115. Henson, P. M., Bratton, D. L. & Fadok, V. A. The phosphatidylserine receptor: a crucial molecular switch? Nature Rev. Mol. Cell Biol. 2, 627-633 (2001).
116. 2 inhibits TNF production in murine bone marrow-derived dendritic cells. Cell. Immunol. 223, 120-132 (2003).
117. Angeli, V. et al. Peroxisome proliferator-activated receptor γ inhibits the migration of dendritic cells: consequences for the immune response. J. Immunol. 170, 5295-5301 (2003).
118. Migita, H., Satozawa, N., Un, J. H., Morser, J. & Kawai, K. RORα1 and RORα4 suppress TNF-α-induced VCAM-1 and ICAM-1 expression in human endothelial cells. FEBS Lett. 557, 269-274 (2004).
119. Sinclair, N. R. & Anderson, C. C. Co-stimulation and co-inhibition: equal partners in regulation. Scand. J. Immunol. 43, 597-603 (1996).
120. McNab, R. et al. Cell wall-anchored CshA polypeptide (259 kilodaltons) in Streptococcus gordonii forms surface fibrils that confer hydrophobic and adhesive properties. J. Bacteriol. 181, 3087-3095 (1999).
121. Ofek, I. & Doyle, R. J. Bacterial Adhesion to Cells and Tissues (Chapman and Hall, London/New York, 1994).
122. Cvitkovitch, D. G., Li, Y. H. & Ellen, R. P. Quorum sensing and biofilm formation in Streptococcal infections. J. Clin. Invest. 112, 1626-1632 (2003).
123. Chill, J. H., Quadt, S. R., Levy, R., Schreiber, G. & Anglister, J. The human type I interferon receptor: NMR structure reveals the molecular basis of ligand binding. Structure (Camb) 11, 791-802 (2003).
124. Zhao, X., Singh, M., Malashkevich, V. N. & Kim, P. S. Structural characterization of the human respiratory syncytial virus fusion protein core. Proc. Natl Acad. Sci. USA 97, 14172-14177 (2000).
125. Sauer, F. G. et al. Structural basis of chaperone function and pilus biogenesis. Science 265, 1058-1061 (1999).
126. Braig, K., Adams, P. D. & Brunger, A. T. Conformational variability in the refined structure of the chaperonin GroEL at 2.8 A resolution. Nature Struct. Biol. 2, 1083-1094 (1995).
127. Schwarz, U. S. Phase behavior of amphiphilic systems. Acta Physica Polonica B 29, 1815-1826 (1998).