A novel ML protein from Manduca sexta may function as a key accessory protein for lipopolysaccharide signaling

Molecular Immunology

Volumn 45, Issue 10, 2008, Pages 2772-2781

  Ao, Jing qun ^a   Ling, Erjun ^a   Rao, Xiang jun ^a   Yu, Xiao Qiang ^a  

^a UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

Author keywords

Innate immunity; Lipid A; Lipopolysaccharide; Manduca sexta; MD 2; ML domain

Indexed keywords

COMPLEMENTARY DNA; GLYCOPROTEIN; INSECT PROTEIN; LIPID A; LIPOPOLYSACCHARIDE; MESSENGER RNA; PROTEIN ML; PROTEIN MSML 1; UNCLASSIFIED DRUG;

ARTICLE; BLOOD CELL; CONTROLLED STUDY; FAT BODY; GRAM NEGATIVE BACTERIUM; HEMOLYMPH; INNATE IMMUNITY; MANDUCA SEXTA; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; CLONING, MOLECULAR; DNA, COMPLEMENTARY; FAT BODY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEMOCYTES; HEMOLYMPH; HUMANS; INSECT PROTEINS; LIPID A; LIPOPOLYSACCHARIDES; MANDUCA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; RECOMBINANT PROTEINS; RNA, MESSENGER; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); INVERTEBRATA; MANDUCA SEXTA; NEGIBACTERIA;

EID: 41849092585     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2008.02.006     Document Type: Article

References (45)

1. Ao J.Q., Ling E., and Yu X.Q. A Toll receptor from Manduca sexta is in response to Escherichia coli infection. Mol. Immunol. 45 (2008) 543-552
2. Axen A., Carlsson A., Engstrom A., and Bennich H. Gloverin, an antibacterial protein from the immune hemolymph of Hyalophora pupae. Eur. J. Biochem. 247 (1997) 614-619
3. Beamer L.J., Carroll S.F., and Eisenberg D. The BPI/LBP family of proteins: a structural analysis of conserved regions. Protein Sci. 7 (1998) 906-914
4. Chaby R. Lipopolysaccharide-binding molecules: transporters, blockers and sensors. Cell. Mol. Life Sci. 61 (2004) 1697-1713
5. Dunn P.E., and Drake D. Fate of bacteria injected into naive and immunized larvae of the tobacco hornworm, Manduca sexta. J. Invertebr. Pathol. 41 (1983) 77-85
6. Ferguson A.D., Welte W., Hofmann E., Lindner B., Holst O., Coulton J.W., and Diederichs K. A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins. Structure 8 (2000) 585-592
7. Frecer V., Ho B., and Ding J.L. Interpretation of biological activity data of bacterial endotoxins by simple molecular models of mechanism of action. Eur. J. Biochem. 267 (2000) 837-852
8. Freudenberg M.A., and Galanos C. Bacterial lipopolysaccharides: structure, metabolism and mechanisms of action. Int. Rev. Immunol. 6 (1990) 207-221
9. Furukawa S., Tanaka H., Nakazawa H., Ishibashi J., Shono T., and Yamakawa M. Inducible gene expression of moricin, a unique antibacterial peptide from the silkworm (Bombyx mori). Biochem. J. 340 Pt 1 (1999) 265-271
10. Gorman M.J., Kankanala P., and Kanost M.R. Bacterial challenge stimulates innate immune responses in extra-embryonic tissues of tobacco hornworm eggs. Insect Mol. Biol. 13 (2004) 19-24
11. Hara S., and Yamakawa M. Moricin, a novel type of antibacterial peptide isolated from the silkworm, Bombyx mori. J. Biol. Chem. 270 (1995) 29923-29927
12. Hoffmann J.A., and Reichhart J.M. Drosophila innate immunity: an evolutionary perspective. Nat. Immunol. 3 (2002) 121-126
13. Imler J.L., Tauszig S., Jouanguy E., Forestier C., and Hoffmann J.A. LPS-induced immune response in Drosophila. J. Endotoxin Res. 6 (2000) 459-462
14. Inohara N., and Nunez G. ML-a conserved domain involved in innate immunity and lipid metabolism. Trends Biochem. Sci. 27 (2002) 219-221
15. Jerala R. Structural biology of the LPS recognition. Int. J. Med. Microbiol. 297 (2007) 353-363
16. Jiang H., Wang Y., and Kanost M.R. Primary structure of ribosomal proteins S3 and S7 from Manduca sexta. Insect Mol. Biol. 5 (1996) 31-38
17. Kanaya T., and Kobayashi J. Purification and characterization of an insect haemolymph protein promoting in vitro replication of the Bombyx mori nucleopolyhedrovirus. J. Gen. Virol. 81 (2000) 1135-1141
18. Kaneko T., and Silverman N. Bacterial recognition and signalling by the Drosophila IMD pathway. Cell Microbiol. 7 (2005) 461-469
19. Kaneko T., Goldman W.E., Mellroth P., Steiner H., Fukase K., Kusumoto S., Harley W., Fox A., Golenbock D., and Silverman N. Monomeric and polymeric Gram-negative peptidoglycan but not purified LPS stimulate the Drosophila IMD pathway. Immunity 20 (2004) 637-649
20. Kawaoka S., Katsuma S., Daimon T., Isono R., Omuro N., Mita K., and Shimada T. Functional analysis of four Gloverin-like genes in the silkworm, Bombyx mori. Arch. Insect Biochem. Physiol. 67 (2008) 87-96
21. Kim H.M., Park B.S., Kim J.I., Kim S.E., Lee J., Oh S.C., Enkhbayar P., Matsushima N., Lee H., Yoo O.J., and Lee J.O. Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist Eritoran. Cell 130 (2007) 906-917
22. Lee E., Linder M.E., and Gilman A.G. Expression of G-protein alpha subunits in Escherichia coli. Methods Enzymol. 237 (1994) 146-164
23. Lemaitre B., Kromer-Metzger E., Michaut L., Nicolas E., Meister M., Georgel P., Reichhart J.M., and Hoffmann J.A. A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 9465-9469
24. Lundstrom A., Liu G., Kang D., Berzins K., and Steiner H. Trichoplusia ni gloverin, an inducible immune gene encoding an antibacterial insect protein. Insect Biochem. Mol. Biol. 32 (2002) 795-801
25. Mackintosh J.A., Gooley A.A., Karuso P.H., Beattie A.J., Jardine D.R., and Veal D.A. A gloverin-like antibacterial protein is synthesized in Helicoverpa armigera following bacterial challenge. Dev. Comp. Immunol. 22 (1998) 387-399
26. Mancek-Keber M., and Jerala R. Structural similarity between the hydrophobic fluorescent probe and lipid A as a ligand of MD-2. FASEB J. 20 (2006) 1836-1842
27. Nagai Y., Akashi S., Nagafuku M., Ogata M., Iwakura Y., Akira S., Kitamura T., Kosugi A., Kimoto M., and Miyake K. Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nat. Immunol. 3 (2002) 667-672
28. Ohto U., Fukase K., Miyake K., and Satow Y. Crystal structures of human MD-2 and its complex with antiendotoxic lipid IVa. Science 316 (2007) 1632-1634
29. Oizumi Y., Hemmi H., Minami M., Asaoka A., and Yamakawa M. Isolation, gene expression and solution structure of a novel moricin analogue, antibacterial peptide from a lepidopteran insect, Spodoptera litura. Biochim. Biophys. Acta 1752 (2005) 83-92
30. Pinner R.W., Teutsch S.M., Simonsen L., Klug L.A., Graber J.M., Clarke M.J., and Berkelman R.L. Trends in infectious diseases mortality in the United States. J. Am. Med. Assoc. 275 (1996) 189-193
31. Raetz C.R., and Whitfield C. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71 (2002) 635-700
32. Saitoh S., Akashi S., Yamada T., Tanimura N., Kobayashi M., Konno K., Matsumoto F., Fukase K., Kusumoto S., Nagai Y., Kusumoto Y., Kosugi A., and Miyake K. Lipid A antagonist, lipid IVa, is distinct from lipid A in interaction with Toll-like receptor 4 (TLR4)-MD-2 and ligand-induced TLR4 oligomerization. Int. Immunol. 16 (2004) 961-969
33. Schromm A.B., Lien E., Henneke P., Chow J.C., Yoshimura A., Heine H., Latz E., Monks B.G., Schwartz D.A., Miyake K., and Golenbock D.T. Molecular genetic analysis of an endotoxin nonresponder mutant cell line: a point mutation in a conserved region of MD-2 abolishes endotoxin-induced signaling. J. Exp. Med. 194 (2001) 79-88
34. Shimazu R., Akashi S., Ogata H., Nagai Y., Fukudome K., Miyake K., and Kimoto M. MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J. Exp. Med. 189 (1999) 1777-1782
35. Stenbak C.R., Ryu J.H., Leulier F., Pili-Floury S., Parquet C., Herve M., Chaput C., Boneca I.G., Lee W.J., Lemaitre B., and Mengin-Lecreulx D. Peptidoglycan molecular requirements allowing detection by the Drosophila immune deficiency pathway. J. Immunol. 173 (2004) 7339-7348
36. Suderman R.J., Andersen S.O., Hopkins T.L., Kanost M.R., and Kramer K.J. Characterization and cDNA cloning of three major proteins from pharate pupal cuticle of Manduca sexta. Insect Biochem. Mol. Biol. 33 (2003) 331-343
37. Viriyakosol S., Tobias P.S., Kitchens R.L., and Kirkland T.N. MD-2 binds to bacterial lipopolysaccharide. J. Biol. Chem. 276 (2001) 38044-38051
38. Visintin A., Mazzoni A., Spitzer J.A., and Segal D.M. Secreted MD-2 is a large polymeric protein that efficiently confers lipopolysaccharide sensitivity to Toll-like receptor 4. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 12156-12161
39. West A.P., Koblansky A.A., and Ghosh S. Recognition and signaling by toll-like receptors. Annu. Rev. Cell Dev. Biol. 22 (2006) 409-437
40. Wright S.D., Ramos R.A., Tobias P.S., Ulevitch R.J., and Mathison J.C. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249 (1990) 1431-1433
41. Yu X.Q., and Kanost M.R. Developmental expression of Manduca sexta hemolin. Arch. Insect Biochem. Physiol. 42 (1999) 198-212
42. Yu X.Q., and Kanost M.R. Immulectin-2, a lipopolysaccharide-specific lectin from an insect, Manduca sexta, is induced in response to Gram-negative bacteria. J. Biol. Chem. 275 (2000) 37373-37381
43. Yu B., Hailman E., and Wright S.D. Lipopolysaccharide binding protein and soluble CD14 catalyze exchange of phospholipids. J. Clin. Invest. 99 (1997) 315-324
44. Yu X.Q., Gan H., and Kanost M.R. Immulectin, an inducible C-type lectin from an insect, Manduca sexta, stimulates activation of plasma prophenol oxidase. Insect Biochem. Mol. Biol. 29 (1999) 585-597
45. Yu X.Q., Tracy M.E., Ling E., Scholz F.R., and Trenczek T. A novel C-type immulectin-3 from Manduca sexta is translocated from hemolymph into the cytoplasm of hemocytes. Insect Biochem. Mol. Biol. 35 (2005) 285-295