E6020: a synthetic Toll-like receptor 4 agonist as a vaccine adjuvant

References

• Glauser MP, Zanetti G, Baumgartner JD, Cohen J. Septic shock: pathogenesis. Lancet338, 732–736 (1991).
   PubMed Web of Science ®Google Scholar
• Rietschel ET, Kirikae T, Schade F et al. Bacterial endotoxin: molecular relationships of structure to activity and function. FASEB J.8, 217–225 (1994).
   PubMed Web of Science ®Google Scholar
• Schletter J, Heine H, Ulmer AJ, Rietschel ET. Molecular mechanisms of endotoxin activity. Arch. Microbiol.164, 383–389 (1995).
   PubMed Web of Science ®Google Scholar
• Zahringer U, Lindner B, Rietschel ET. Molecular structure of lipid A, the endotoxic center of bacterial lipopolysaccharides. Adv. Carbohydr. Chem. Biochem.50, 211–276 (1994).
   PubMed Web of Science ®Google Scholar
• Galanos C, Luderitz O, Rietschel ET et al. Synthetic and natural Escherichia coli free lipid A express identical endotoxic activities. Eur. J. Biochem.148, 1–5 (1985).
   PubMedGoogle Scholar
• Hoffmann JA, Kafatos FC, Janeway CA Jr, Ezekowitz RAB. Phylogenetic perspectives in innate immunity. Science284, 1313–1318 (1999).
   PubMed Web of Science ®Google Scholar
• Chow JC, Young DW, Golenbock DT, Christ WJ, Gusovsky F. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J. Biol. Chem.274, 10689–10692 (1999).
   PubMed Web of Science ®Google Scholar
• Poltorak A, He X, Smirnova I et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science282, 2085–2088 (1998).
   PubMed Web of Science ®Google Scholar
• Hoshino K, Takeuchi O, Kawai T et al. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol.162, 3749–3752 (1999).
   PubMed Web of Science ®Google Scholar
• Ulevitch RJ, Tobias PS. Receptor-dependent mechanisms of cell stimulation by bacterial endotoxin. Annu. Rev. Immunol.13, 437–457 (1995).
   PubMed Web of Science ®Google Scholar
• Shimazu R, Akashi S, Ogata H et al. MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J. Exp. Med.189, 1777–1782 (1999).
   Google Scholar
• Akashi S, Nagai Y, Ogata H et al. Human MD-2 confers on mouse Toll-like receptor 4 species-specific lipopolysaccharide recognition. Internat. Immun.13, 1595–1599 (2001).
   Google Scholar
• Ohto U, Fukase K, Miyake K, Satow Y. Crystal structures of human MD-2 and its complex with antiendotoxic lipid IVa. Science316, 1632-1634 (2007).
   Google Scholar
• Pedron T, Girard R, Eustache J et al. New synthetic analogs of lipid A as lipopolysaccharide agonists or antagonists of B lymphocyte activation. Inter. Immunol.4, 533–540 (1992).
   PubMed Web of Science ®Google Scholar
• Zahringer U, Lindner B, Rietschel ET. Chemical structure of lipid A: recent advances in structural analysis of biologically active molecules. In: Endotoxin in Health and Disease. Brade H, Opal SM, Vogel SN, Morrison DC (Eds). Marcel Dekker Inc., NY, USA 93–114 (1999).
   Google Scholar
• Kusumoto S, Fukase K Oikawa M. The chemical synthesis of lipid A. In: Endotoxin in Health and Disease. Brade H, Opal SM, Vogel SN, Morrison DC (Eds). Marcel Dekker Inc., NY, USA 243–256 (1999).
   Google Scholar
• Evans JT, Cluff CW, Johnson DA, Lacy MJ, Persing DH, Baldridge JR. Enhancement of antigen-specific immunity via the TLR4 ligands MPL™ and Ribi.529. Expert Rev. Vaccines2, 219–229 (2003).
   PubMedGoogle Scholar
• Johnson DA, Keegan DS, Sowell CG et al. 3-O-desacyl monophosphoryl lipid A derivatives. J. Med. Chem.42, 4640–4649 (1999).
   PubMed Web of Science ®Google Scholar
• Cluff CW, Baldridge JR, Stöver AG et al. Synthetic Toll-like receptor 4 agonists stimulate innate resistance to infectious challenge. Infect. Immun.73, 3044–3052 (2005).
   PubMed Web of Science ®Google Scholar
• Schromm AB, Brandenburg K, Loppnow H et al. The charge of endotoxin molecules influences their conformation and interleukin-6 inducing capacity. J. Immunol.161, 5464–5471 (1998).
   PubMed Web of Science ®Google Scholar
• Schromm AB, Brandenburg K, Loppnow H et al. Biological activities of lipopolysaccharides are determined by the shape of their lipid A portion. Eur. J. Biochem.267, 2008–2013 (2000).
   PubMedGoogle Scholar
• Schumann RR, Leong SR, Flaggs GW et al. Structure and function of lipopolysaccharide binding protein. Science249, 1429–1431 (1990).
   PubMed Web of Science ®Google Scholar
• Wright SD, Ramos RA, Tobias PS, Ulevitch RJ, Mathison JC. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science249, 1431–1433 (1990).
   PubMed Web of Science ®Google Scholar
• Gutsmann T, Haberer N, Carroll SF, Seydel U, Wiese A. Interaction between lipopolysaccharide (LPS), LPS-binding protein (LBP), and planar membranes. Biol. Chem.382, 425–434 (2001).
   PubMed Web of Science ®Google Scholar
• Blunck R, Scheel O, Müller M, Brandenburg K, Seitzer U, Seydel U. New insights into endotoxin-induced activation of macrophages: Involvement of a K+ channel in transmembrane signalling. J. Immunol.166, 1009–1015 (2001).
   PubMed Web of Science ®Google Scholar
• Krisovitch SM, Regen SL. Nearest-neighbor recognition in phosopholipid membranes: a molecular-level approach to the study of membrane suprastructure. J. Am. Chem. Soc.114, 9828–9835 (1992).
   Web of Science ®Google Scholar
• Davidson SMK, Regen SL. Nearest-neighbor recognition in phospholipid membranes. Chem. Rev.97, 1269–1279 (1997).
   PubMed Web of Science ®Google Scholar
• Brandenburg K, Garidel P, Howe J et al. What can calorimetry tell us about changes of three-dimensional aggregate structures of phospholipid and glycolipids? Thermochim. Acta445, 133–145 (2006).
   Web of Science ®Google Scholar
• Seydel U, Hawkins L, Schromm AB et al. The generalized endotoxic principle. Eur. J. Immunol.33, 1586–1592 (2003).
   PubMed Web of Science ®Google Scholar
• Brandenburg K, Hawkins L, Garidel P et al. Structural polymorphism and endotoxic activity of synthetic phospholipid-like amphiphiles. Biochem.43, 4039–4046 (2004).
   PubMed Web of Science ®Google Scholar
• Brandenburg K, Mayer H, Koch MHJ, Weckesser J, Rietschel ET, Seydel U. Influence of the supramolecular structure of free lipid A on its biological activity. Eur. J. Biochem.218, 555–563 (1993).
   PubMedGoogle Scholar
• Hawkins LD, Ishizaka ST, McGuinness P et al. A novel class of endotoxin receptor agonists with simplified structure, Toll-like receptor 4-dependent immunostimulatory action, and adjuvant activity. J. Pharmacol. Exp. Ther.300(2), 655–661 (2002).
   PubMed Web of Science ®Google Scholar
• Yoneyama M, Kikuchi M, Natsukawa T et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol.5(7), 730–737 (2004).
   PubMed Web of Science ®Google Scholar
• Girardin SE, Boneca IG, Viala J et al. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem.278(11), 8869–8872 (2003).
   PubMed Web of Science ®Google Scholar
• Hayashi F, Smith KD, Ozinsky A et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature410(6832), 1099–1103 (2001).
   PubMed Web of Science ®Google Scholar
• Kurt-Jones EA, Popova L, Kwinn L et al. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol.1(5), 398–401 (2001).
   Web of Science ®Google Scholar
• Ohashi K, Burkart V, Flohe S, Kolb H. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the Toll-like receptor-4 complex. J. Immunol.164(2), 558–561 (2000).
   PubMed Web of Science ®Google Scholar
• Okamura Y, Watari M, Jerud ES et al. The extra domain A of fibronectin activates Toll-like receptor 4. J. Biol. Chem.276(13), 10229–10233 (2001).
   PubMed Web of Science ®Google Scholar
• Zhang FX, Kirschning CJ, Mancinelli R et al. Bacterial lipopolysaccharide activates nuclear factor-κB through interleukin-1 signaling mediators in cultured human dermal endothelial cells and mononuclear phagocytes. J. Biol. Chem.274(12), 7611–7614 (1999).
   PubMed Web of Science ®Google Scholar
• Fitzgerald KA, Rowe DC, Barnes BJ et al. LPS-TLR4 signaling to IRF-3/7 and NFκB involves the Toll adapters TRAM and TRIF. J. Exp. Med.198(7), 1043–1055 (2003).
   PubMed Web of Science ®Google Scholar
• Mata-Haro V, Cekic C, Martin M, Chilton PM, Casella CR, Mitchell TC. The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science316, 1628–1632 (2007).
   Google Scholar
• Ganley-Leal LM, Liu X, Wetzler LM. Toll-like receptor 2-mediated human B cell differentiation. Clin. Immunol.120(3), 272–284 (2006).
   PubMed Web of Science ®Google Scholar
• Cooper CL, Davis HL, Morris ML et al. CPG 7909, an immunostimulatory TLR9 agonist oligodeoxynucleotide, as adjuvant to Engerix-B® HBV vaccine in healthy adults: a double-blind Phase I/II study. J. Clin. Immunol.24(6), 693–701 (2004).
   PubMed Web of Science ®Google Scholar
• Vandepapeliere P, Rehermann B, Koutsoukos M et al. Potent enhancement of cellular and humoral immune responses against recombinant hepatitis B antigens using AS02A adjuvant in healthy adults. Vaccine23(20), 2591–601 (2005).
   PubMed Web of Science ®Google Scholar
• Dai J, Megjugorac NJ, Amrute SB, Fitzgerald-Bocarsly P. Regulation of IFN regulatory factor-7 and IFN-α production by enveloped virus and lipopolysaccharide in human plasmacytoid dendritic cells. J. Immunol.173(3), 1535–1548 (2004).
   PubMed Web of Science ®Google Scholar
• Caramalho I, Lopes-Carvalho T, Ostler D, Zelenay S, Haury M, Demengeot J. Regulatory T cells selectively express Toll-like receptors and are activated by lipopolysaccharide. J. Exp. Med.197(4), 403–411 (2003).
   PubMed Web of Science ®Google Scholar
• Pasare C, Medzhitov R. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science299(5609), 1033–1036 (2003).
   PubMed Web of Science ®Google Scholar
• Seya T, Akazawa T, Tsumita T, Matsumoto M. Role of toll-like receptors in adjuvant-augmented immune therapies. Evid. Based Complement. Alternat. Med.3(1), 31–38 (2006).
   Google Scholar
• Golenbock DT, Hampton RY, Qureshi N, Takayama K, Raetz CRH. Lipid A-like molecules that antagonize the effects of endotoxins on human monocytes. J. Biol. Chem.266, 19490–19498 (1991).
   Google Scholar
• Rose JR, Christ WJ, Bristol JR, Kawata T, Rossignol DP. Agonistic and antagonistic activities of bacterially derived rhodobacter sphaeroides lipid A: comparison with activities of synthetic material of the proposed structure of analogs. Infect. Immun.63, 833–839 (1995).
   Google Scholar
• Peng S. Signaling in B cells via Toll-like receptors. Curr. Opin. Immunol.17(3), 230–236 (2005).
   Google Scholar
• Kadowaki N, Ho S, Antonenko S et al. Subsets of human dendritic cell precursors express different Toll-like receptors and respond to different microbial antigens. J. Exp. Med.194(6), 863–869 (2001).
   PubMed Web of Science ®Google Scholar
• Krug A, Towarowski Britsch S et al. Toll-like receptor expression reveals CpG DNA as a unique microbial stimulus for plasmacytoid dendritic cells which synergizes with CD40 ligand to induce high amounts of IL-12. Eur. J. Immunol.31, 3026–3037 (2001).
   PubMed Web of Science ®Google Scholar
• Steinman L. A brief history of Th17, the first major revision in the Th1/Th2 hypothesis of T cell-mediated tissue damage. Nat. Med.13(2), 139–145 (2007).
   PubMed Web of Science ®Google Scholar
• Sakaguchi S, Ono M, Setoguchi R et al. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol. Rev.212, 8–27 (2006).
   PubMed Web of Science ®Google Scholar
• Gavin AL, Hoebe K, Duong B et al. Adjuvant-enhanced antibody responses in the absence of Toll-like receptor signaling. Science314(5807), 1936–1938 (2006).
   PubMed Web of Science ®Google Scholar
• Manetti R, Parronchi P, Giudizi MG et al. Natural killer cell stimulatory factor (interleukin 12 [IL-12]) induces T helper type 1 (Th1)-specific immune responses and inhibits the development of IL-4-producing Th cells. J. Exp. Med.177(4), 1199–1204 (1993).
   PubMed Web of Science ®Google Scholar
• Przetak M, Chow J, Cheng H, Rose J, Hawkins LD, Ishizaka ST. Novel synthetic LPS receptor agonists boost systemic and mucosal antibody responses in mice. Vaccine21(9–10), 961–970 (2003).
   PubMed Web of Science ®Google Scholar
• Li H, Nookala S, Re F. Aluminum hydroxide adjuvants activated caspase-1 and induce IL-1 and IL-18 release. J. Immunol.178, 5471–5276 (2007).
   Google Scholar
• Franz S, Kobzik L, Kim Y-D et al. Toll4 (TLR4) expression in cardiac myocytes in normal and failing myocardium. J. Clin. Invest.104, 271–280 (1999).
   PubMed Web of Science ®Google Scholar
• de Kleijn D, Pasterkamp G. Toll-like receptors in cardiovascular diseases. Cardiovasc. Res.60, 58–67 (2003).
   PubMed Web of Science ®Google Scholar
• Sukkar MB, Kie S, Khorasani NM et al. Toll-like receptor 2, 3, 4 expression and function in human airway smooth muscle. J. Allergy Clin. Immunol.118, 641–648 (2006).
   PubMed Web of Science ®Google Scholar
• Morris GE, Whyte MKB, Martin GF, Jose PJ, Dower SK, Sabroe I. Agonists of Toll-like receptors 2 and 4 activate airway smooth muscle via mononuclear leukocytes. Am. J. Respir. Crit. Care Med.171, 814–822 (2005).
   PubMed Web of Science ®Google Scholar
• Sha Q, Truong-Tran AQ, Plitt JR, Beck LA, Schleimer RP. Activation of airway epithelial cells by Toll-like receptor agonists. Am. J. Respir. Cell Mol. Biol.31, 358–364 (2004).
   PubMed Web of Science ®Google Scholar
• Armstrong L, Medford ARL, Uppington KM et al. Expression of Toll-like receptor-2 and -4 on alveolar epithelial cells. Am. J. Respir. Cell Mol. Biol.31, 241–245 (2004).
   PubMed Web of Science ®Google Scholar
• Moscatello DK, Ramirez G, Wong AJ. A naturally occurring mutant human epidermal growth factor receptor as a target for peptide vaccine immunotherapy of tumors. Cancer Res.57(8), 1419–1424 (1997).
   PubMed Web of Science ®Google Scholar