"Monovalent" ligands that trigger TLR-4 and TCR are not necessarily truly monovalent

Molecular Immunology

Volumn 51, Issue 3-4, 2012, Pages 356-362

  Sigalov, Alexander B ^a  

^a SignaBlok Inc   (United States)

Author keywords

Immune signaling; Ligand valency; Lipid A; LPSL; MHC; Micelles; Receptor clustering; Surface bound; T cell receptor; TLR 4; Toll like receptor

Indexed keywords

LIGAND; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR 4;

ADAPTIVE IMMUNITY; ARTICLE; CHEMICAL PARAMETERS; INNATE IMMUNITY; MONOVALENCY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

CELL MEMBRANE; CYTOPLASM; LIGANDS; LIPID A; MODELS, MOLECULAR; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 84861224187     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2012.03.031     Document Type: Article

References (79)

1. Abastado J.P., Lone Y.C., Casrouge A., Boulot G., Kourilsky P. Dimerization of soluble major histocompatibility complex-peptide complexes is sufficient for activation of T cell hybridoma and induction of unresponsiveness. Journal of Experimental Medicine 1995, 182:439-447.
2. Adams E.J., Chien Y.H., Garcia K.C. Structure of a gammadelta T cell receptor in complex with the nonclassical MHC T22. Science 2005, 308:227-231.
3. Akira S., Takeda K. Toll-like receptor signalling. Nature Reviews Immunology 2004, 4:499-511.
4. Angelov G.S., Guillaume P., Cebecauer M., Bosshard G., Dojcinovic D., Baumgaertner P., Luescher I.F. Soluble MHC-peptide complexes containing long rigid linkers abolish CTL-mediated cytotoxicity. Journal of Immunology 2006, 176:3356-3365.
5. Bachmann M.F., Ohashi P.S. The role of T-cell receptor dimerization in T-cell activation. Immunology Today 1999, 20:568-576.
6. Bachmann M.F., Salzmann M., Oxenius A., Ohashi P.S. Formation of TCR dimers/trimers as a crucial step for T cell activation. European Journal of Immunology 1998, 28:2571-2579.
7. Berlanga O., Bori-Sanz T., James J.R., Frampton J., Davis S.J., Tomlinson M.G., Watson S.P. Glycoprotein VI oligomerization in cell lines and platelets. Journal of Thrombosis and Haemostasis 2007, 5:1026-1033.
8. Beutler B. TLR4 as the mammalian endotoxin sensor. Current Topics in Microbiology and Immunology 2002, 270:109-120.
9. Boniface J.J., Rabinowitz J.D., Wulfing C., Hampl J., Reich Z., Altman J.D., Kantor R.M., Beeson C., McConnell H.M., Davis M.M. Initiation of signal transduction through the T cell receptor requires the multivalent engagement of peptide/MHC ligands. Immunity 1998, 9:459-466.
10. Brandenburg K., Mayer H., Koch M.H., Weckesser J., Rietschel E.T., Seydel U. Influence of the supramolecular structure of free lipid A on its biological activity. European Journal of Biochemistry 1993, 218:555-563.
11. Brandenburg K., Lindner B., Schromm A., Koch M.H., Bauer J., Merkli A., Zbaeren C., Davies J.G., Seydel U. Physicochemical characteristics of triacyl lipid A partial structure OM-174 in relation to biological activity. European Journal of Biochemistry 2000, 267:3370-3377.
12. Brodsky I., Medzhitov R. Two modes of ligand recognition by TLRs. Cell 2007, 130:979-981.
13. Call M.E., Pyrdol J., Wiedmann M., Wucherpfennig K.W. The organizing principle in the formation of the T cell receptor-CD3 complex. Cell 2002, 111:967-979.
14. Cebecauer M., Guillaume P., Hozak P., Mark S., Everett H., Schneider P., Luescher I.F. Soluble MHC-peptide complexes induce rapid death of CD8+ CTL. Journal of Immunology 2005, 174:6809-6819.
15. Chan F.K. Three is better than one: pre-ligand receptor assembly in the regulation of TNF receptor signaling. Cytokine 2007, 37:101-107.
16. Chan K.F., Siegel M.R., Lenardo J.M. Signaling by the TNF receptor superfamily and T cell homeostasis. Immunity 2000, 13:419-422.
17. Cochran J.R., Cameron T.O., Stern L.J. The relationship of MHC-peptide binding and T cell activation probed using chemically defined MHC class II oligomers. Immunity 2000, 12:241-250.
18. Cochran J.R., Cameron T.O., Stone J.D., Lubetsky J.B., Stern L.J. Receptor proximity, not intermolecular orientation, is critical for triggering T-cell activation. Journal of Biological Chemistry 2001, 276:28068-28074.
19. Cooper J.A., Qian H. A mechanism for SRC kinase-dependent signaling by noncatalytic receptors. Biochemistry 2008, 47:5681-5688.
20. Cullis P.R., de Kruijff B. Lipid polymorphism and the functional roles of lipids in biological membranes. Biochimica et Biophysica Acta 1979, 559:399-420.
21. Deng L., Langley R.J., Brown P.H., Xu G., Teng L., Wang Q., Gonzales M.I., Callender G.G., Nishimura M.I., Topalian S.L., Mariuzza R.A. Structural basis for the recognition of mutant self by a tumor-specific MHC class II-restricted T cell receptor. Nature Immunology 2007, 8:398-408.
22. Fahmy T.M., Bieler J.G., Schneck J.P. Probing T cell membrane organization using dimeric MHC-Ig complexes. Journal of Immunological Methods 2002, 268:93-106.
23. Fitzgerald K.A., Golenbock D.T. Immunology: The shape of things to come. Science 2007, 316:1574-1576.
24. Fukuoka S., Brandenburg K., Muller M., Lindner B., Koch M.H., Seydel U. Physico-chemical analysis of lipid A fractions of lipopolysaccharide from Erwinia carotovora in relation to bioactivity. Biochimica et Biophysica Acta 2001, 1510:185-197.
25. Garboczi D.N., Ghosh P., Utz U., Fan Q.R., Biddison W.E., Wiley D.C. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 1996, 384:134-141.
26. Garcia-Verdugo I., Sanchez-Barbero F., Soldau K., Tobias P.S., Casals C. Interaction of SP-A (surfactant protein A) with bacterial rough lipopolysaccharide (Re-LPS), and effects of SP-A on the binding of Re-LPS to CD14 and LPS-binding protein. Biochemical Journal 2005, 391:115-124.
27. Germain R.N. MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell 1994, 76:287-299.
28. Hayball J.D., Lake R.A. The immune function of MHC class II molecules mutated in the putative superdimer interface. Molecular and Cellular Biochemistry 2005, 273:1-9.
29. Herr A.B. Direct evidence of a native GPVI dimer at the platelet surface. Journal of Thrombosis and Haemostasis 2009, 7:1344-1346.
30. Hofer M., Hampton R.Y., Raetz C.R., Yu H. Aggregation behavior of lipid IVA in aqueous solutions at physiological pH. 1. Simple buffer solutions. Chemistry and Physics of Lipids 1991, 59:167-181.
31. Jin M.S., Lee J.O. Structures of the toll-like receptor family and its ligand complexes. Immunity 2008, 29:182-191.
32. Jung S.M., Tsuji K., Moroi M. Glycoprotein (GP) VI dimer as a major collagen-binding site of native platelets: direct evidence obtained with dimeric GPVI-specific Fabs. Journal of Thrombosis and Haemostasis 2009, 7:1347-1355.
33. Kiessling L.L., Gestwicki J.E., Strong L.E. Synthetic multivalent ligands as probes of signal transduction. Angewandte Chemie (International ed. in English) 2006, 45:2348-2368.
34. Kitchens R.L., Munford R.S. CD14-dependent internalization of bacterial lipopolysaccharide (LPS) is strongly influenced by LPS aggregation but not by cellular responses to LPS. Journal of Immunology 1998, 160:1920-1928.
35. Klemm J.D., Schreiber S.L., Crabtree G.R. Dimerization as a regulatory mechanism in signal transduction. Annual Review of Immunology 1998, 16:569-592.
36. Lee H.K., Dunzendorfer S., Tobias P.S. Cytoplasmic domain-mediated dimerizations of toll-like receptor 4 observed by beta-lactamase enzyme fragment complementation. Journal of Biological Chemistry 2004, 279:10564-10574.
37. Li P., Morris D.L., Willcox B.E., Steinle A., Spies T., Strong R.K. Complex structure of the activating immunoreceptor NKG2D and its MHC class I-like ligand MICA. Nature Immunology 2001, 2:443-451.
38. Lindstedt R., Monk N., Lombardi G., Lechler R. Amino acid substitutions in the putative MHC class II " dimer of dimers" interface inhibit CD4+ T cell activation. Journal of Immunology 2001, 166:800-808.
39. Lu Y.C., Yeh W.C., Ohashi P.S. LPS/TLR4 signal transduction pathway. Cytokine 2008, 42:145-151.
40. Ma Z., Sharp K.A., Janmey P.A., Finkel T.H. Surface-anchored monomeric agonist pMHCs alone trigger TCR with high sensitivity. PLoS Biology 2008, 6:e43.
41. Manolios N., Bonifacino J.S., Klausner R.D. Transmembrane helical interactions and the assembly of the T cell receptor complex. Science 1990, 249:274-277.
42. Maurer N. Determination of size and structure of lipid IV a vesicles by quasi-elastic light scattering and small-angle X-ray scattering. Journal of Applied Crystallography 1991, 24:832-835.
43. Minguet S., Schamel W.W. Permissive geometry model. Advances in Experimental Medicine and Biology 2008, 640:113-120.
44. Nunez Miguel R., Wong J., Westoll J.F., Brooks H.J., O'Neill L.A., Gay N.J., Bryant C.E., Monie T.P. A dimer of the Toll-like receptor 4 cytoplasmic domain provides a specific scaffold for the recruitment of signalling adaptor proteins. PLoS One 2007, 2:e788.
45. Ozinsky A., Underhill D.M., Fontenot J.D., Hajjar A.M., Smith K.D., Wilson C.B., Schroeder L., Aderem A. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:13766-13771.
46. Park B.S., Song D.H., Kim H.M., Choi B.S., Lee H., Lee J.O. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 2009, 458:1191-1195.
47. Parra-Lopez C., Calvo-Calle J.M., Cameron T.O., Vargas L.E., Salazar L.M., Patarroyo M.E., Nardin E., Stern L.J. Major histocompatibility complex and T cell interactions of a universal T cell epitope from Plasmodium falciparum circumsporozoite protein. Journal of Biological Chemistry 2006, 281:14907-14917.
48. Patrick S.M., Kim S., Braunstein N.S., Thomas J.L., Leonard E.F. Dependence of T cell activation on area of contact and density of a ligand-coated surface. Journal of Immunological Methods 2000, 241:97-108.
49. Reich Z., Boniface J.J., Lyons D.S., Borochov N., Wachtel E.J., Davis M.M. Ligand-specific oligomerization of T-cell receptor molecules. Nature 1997, 387:617-620.
50. Rietschel E.T., Brade H., Brade L., Brandenburg K., Schade U., Seydel U., Zahringer U., Galanos C., Luderitz O., Westphal O., et al. Lipid A, the endotoxic center of bacterial lipopolysaccharides: relation of chemical structure to biological activity. Progress in Clinical and Biological Research 1987, 231:25-53.
51. Rotzschke O., Falk K., Strominger J.L. Superactivation of an immune response triggered by oligomerized T cell epitopes. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:14642-14647.
52. Rubin B., Knibiehler M., Gairin J.E. Allosteric changes in the tcr/cd3 structure upon interaction with extra- or intra-cellular ligands. Scandinavian Journal of Immunology 2007, 66:228-237.
53. Saitoh S., Akashi S., Yamada T., Tanimura N., Matsumoto F., Fukase K., Kusumoto S., Kosugi A., Miyake K. Ligand-dependent toll-like receptor 4 (TLR4)-oligomerization is directly linked with TLR4-signaling. Journal of Endotoxin Research 2004, 10:257-260.
54. Schamel W.W., Reth M. Clustering models. Advances in Experimental Medicine and Biology 2008, 640:64-73.
55. Schamel W.W., Arechaga I., Risueno R.M., van Santen H.M., Cabezas P., Risco C., Valpuesta J.M., Alarcon B. Coexistence of multivalent and monovalent TCRs explains high sensitivity and wide range of response. Journal of Experimental Medicine 2005, 202:493-503.
56. Schromm A.B., Brandenburg K., Loppnow H., Zahringer U., Rietschel E.T., Carroll S.F., Koch M.H., Kusumoto S., Seydel U. The charge of endotoxin molecules influences their conformation and IL-6-inducing capacity. Journal of Immunology 1998, 161:5464-5471.
57. Schromm A.B., Brandenburg K., Loppnow H., Moran A.P., Koch M.H., Rietschel E.T., Seydel U. Biological activities of lipopolysaccharides are determined by the shape of their lipid A portion. European Journal of Biochemistry 2000, 267:2008-2013.
58. Seydel U. A biophysical view on the function and activity of endotoxins. Endotoxin in Health and Disease 1999, Marcel Dekker, New York, pp. 195-220.
59. Seydel U., Brandenburg K., Rietschel E.T. A case for an endotoxic conformation. Progress in Clinical and Biological Research 1994, 388:17-30.
60. Seydel U., Oikawa M., Fukase K., Kusumoto S., Brandenburg K. Intrinsic conformation of lipid A is responsible for agonistic and antagonistic activity. European Journal of Biochemistry 2000, 267:3032-3039.
61. Seydel U., Hawkins L., Schromm A.B., Heine H., Scheel O., Koch M.H., Brandenburg K. The generalized endotoxic principle. European Journal of Immunology 2003, 33:1586-1592.
62. Shnyra A., Hultenby K., Lindberg A.A. Role of the physical state of Salmonella lipopolysaccharide in expression of biological and endotoxic properties. Infection and Immunity 1993, 61:5351-5360.
63. Sigalov A.B. Multichain immune recognition receptor signaling: different players, same game?. Trends in Immunology 2004, 25:583-589.
64. Sigalov A.B. The SCHOOL of nature. I. Transmembrane signaling. Self Nonself 2010, 1:4-39.
65. Sigalov A.B. The SCHOOL of nature. II. Protein order, disorder and oligomericity in transmembrane signaling. Self Nonself 2010, 1:89-102.
66. Sigalov A., Aivazian D., Stern L. Homooligomerization of the cytoplasmic domain of the T cell receptor zeta chain and of other proteins containing the immunoreceptor tyrosine-based activation motif. Biochemistry 2004, 43:2049-2061.
67. Steinle A., Li P., Morris D.L., Groh V., Lanier L.L., Strong R.K., Spies T. Interactions of human NKG2D with its ligands MICA, MICB, and homologs of the mouse RAE-1 protein family. Immunogenetics 2001, 53:279-287.
68. Strong R.K. Asymmetric ligand recognition by the activating natural killer cell receptor NKG2D, a symmetric homodimer. Molecular Immunology 2002, 38:1029-1037.
69. Sykulev Y. Changing separating distances between immune receptors as a sensitive mechanism regulating T-cell activation. Self Nonself 2010, 1:67-68.
70. Symer D.E., Dintzis R.Z., Diamond D.J., Dintzis H.M. Inhibition or activation of human T cell receptor transfectants is controlled by defined, soluble antigen arrays. Journal of Experimental Medicine 1992, 176:1421-1430.
71. Takayama K., Din Z.Z., Mukerjee P., Cooke P.H., Kirkland T.N. Physicochemical properties of the lipopolysaccharide unit that activates B lymphocytes. Journal of Biological Chemistry 1990, 265:14023-14029.
72. Takayama K., Mitchell D.H., Din Z.Z., Mukerjee P., Li C., Coleman D.L. Monomeric Re lipopolysaccharide from Escherichia coli is more active than the aggregated form in the Limulus amebocyte lysate assay and in inducing Egr-1 mRNA in murine peritoneal macrophages. Journal of Biological Chemistry 1994, 269:2241-2244.
73. Takeda K., Akira S. Toll-like receptors in innate immunity. International Immunology 2005, 17:1-14.
74. Vasan M., Wolfert M.A., Boons G.J. Agonistic and antagonistic properties of a Rhizobium sin-1 lipid A modified by an ether-linked lipid. Organic and Biomolecular Chemistry 2007, 5:2087-2097.
75. Visintin A., Latz E., Monks B.G., Espevik T., Golenbock D.T. Lysines 128 and 132 enable lipopolysaccharide binding to MD-2, leading to Toll-like receptor-4 aggregation and signal transduction. Journal of Biological Chemistry 2003, 278:48313-48320.
76. Watts T.H. T cell activation by preformed, long-lived Ia-peptide complexes. Quantitative aspects. Journal of Immunology 1988, 141:3708-3714.
77. Weiss A., Schlessinger J. Switching signals on or off by receptor dimerization. Cell 1998, 94:277-280.
78. Yu B., Wright S.D. Catalytic properties of lipopolysaccharide (LPS) binding protein Transfer of LPS to soluble CD14. Journal of Biological Chemistry 1996, 271:4100-4105.
79. Zhang H., Tay P.N., Cao W., Li W., Lu J. Integrin-nucleated Toll-like receptor (TLR) dimerization reveals subcellular targeting of TLRs and distinct mechanisms of TLR4 activation and signaling. FEBS Letters 2002, 532:171-176.