The crystal structure of lipopolysaccharide binding protein reveals the location of a frequent mutation that impairs innate immunity

Immunity

Volumn 39, Issue 4, 2013, Pages 647-660

  Eckert, Jana K ^a,i   Kim, Young J ^b   Kim, Jung I ^b   Gürtler, Kathleen ^a   Oh, Djin Ye ^a,j   Sur, Saubashya ^a   Lundvall, Linn ^a   Hamann, Lutz ^a   vanderPloeg, Anke ^c   Pickkers, Peter ^c   Giamarellos Bourboulis, Evangelos ^d   Kubarenko, Andriy V ^e,k   Weber, Alexander N ^e,l   Kabesch, Michael ^f,g   Kumpf, Oliver ^a   An, Hyun Jung ^h   Lee, Jie Oh ^b   Schumann, Ralf R ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^f UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^g HANNOVER MEDICAL SCHOOL   (Germany)

^h Chungnam National University   (South Korea)

ⁱ ROYAL CHILDREN'S HOSPITAL   (Australia)

^j NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^k UNIVERSITY HOSPITAL BONN   (Germany)

^l UNIVERSITY OF TÜBINGEN   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE PHASE PROTEIN; BACTERICIDAL PERMEABILITY INCREASING PROTEIN; LIPOPOLYSACCHARIDE; LIPOPOLYSACCHARIDE BINDING PROTEIN; MUTANT PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; CYTOKINE PRODUCTION; HUMAN; HYDROPHOBICITY; INNATE IMMUNITY; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; SEPSIS; SINGLE NUCLEOTIDE POLYMORPHISM;

ACUTE-PHASE PROTEINS; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BINDING SITES; BLOOD PROTEINS; CARRIER PROTEINS; CRYSTALLOGRAPHY, X-RAY; GENOTYPE; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; IMMUNITY, INNATE; LIPOPOLYSACCHARIDES; MEMBRANE GLYCOPROTEINS; MICE; MODELS, MOLECULAR; MUTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; STATIC ELECTRICITY; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84885865202     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.09.005     Document Type: Article

References (50)

1. Beamer L.J., Carroll S.F., Eisenberg D. Crystal structure of human BPI and two bound phospholipids at 2.4 angstrom resolution. Science 1997, 276:1861-1864.
2. Beamer L.J., Carroll S.F., Eisenberg D. The BPI/LBP family of proteins: a structural analysis of conserved regions. Protein Sci. 1998, 7:906-914.
3. Bingle C.D., Craven C.J. Meet the relatives: a family of BPI- and LBP-related proteins. Trends Immunol. 2004, 25:53-55.
4. Branger J., Florquin S., Knapp S., Leemans J.C., Pater J.M., Speelman P., Golenbock D.T., van der Poll T. LPS-binding protein-deficient mice have an impaired defense against Gram-negative but not Gram-positive pneumonia. Int. Immunol. 2004, 16:1605-1611.
5. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 1998, 54:905-921.
6. Canny G., Levy O. Bactericidal/permeability-increasing protein (BPI) and BPI homologs at mucosal sites. Trends Immunol. 2008, 29:541-547.
7. Chien J.W., Boeckh M.J., Hansen J.A., Clark J.G. Lipopolysaccharide binding protein promoter variants influence the risk for Gram-negative bacteremia and mortality after allogeneic hematopoietic cell transplantation. Blood 2008, 111:2462-2469.
8. Flores C., Pérez-Méndez L., Maca-Meyer N., Muriel A., Espinosa E., Blanco J., Sangüesa R., Muros M., Garcia J.G., Villar J. A common haplotype of the LBP gene predisposes to severe sepsis. Crit. Care Med. 2009, 37:2759-2766. GRECIA and Gen-SEP groups.
9. Gonzalez-Quintela A., Alonso M., Campos J., Vizcaino L., Loidi L., Gude F. Determinants of serum concentrations of lipopolysaccharide-binding protein (LBP) in the adult population: the role of obesity. PLoS ONE 2013, 8:e54600.
10. Hailman E., Lichenstein H.S., Wurfel M.M., Miller D.S., Johnson D.A., Kelley M., Busse L.A., Zukowski M.M., Wright S.D. Lipopolysaccharide (LPS)-binding protein accelerates the binding of LPS to CD14. J.Exp. Med. 1994, 179:269-277.
11. Hamann L., Alexander C., Stamme C., Zähringer U., Schumann R.R. Acute-phase concentrations of lipopolysaccharide (LPS)-binding protein inhibit innate immune cell activation by different LPS chemotypes via different mechanisms. Infect. Immun. 2005, 73:193-200.
12. Han J., Mathison J.C., Ulevitch R.J., Tobias P.S. Lipopolysaccharide (LPS) binding protein, truncated at Ile-197, binds LPS but does not transfer LPS to CD14. J.Biol. Chem. 1994, 269:8172-8175.
13. Hemmila M.R., Kim J., Sun J.M., Cannon J., Arbabi S., Minter R.M., Su G.L., Remick D.G., Wang S.C. Gene therapy with lipopolysaccharide binding protein for gram-negative pneumonia: respiratory physiology. J Trauma 2006, 61:598-605. discussion 605-596.
14. Hubacek J.A., Stüber F., Fröhlich D., Book M., Wetegrove S., Ritter M., Rothe G., Schmitz G. Gene variants of the bactericidal/permeability increasing protein and lipopolysaccharide binding protein in sepsis patients: gender-specific genetic predisposition to sepsis. Crit. Care Med. 2001, 29:557-561.
15. Hubacek J.A., Pitha J., Skodová Z., Adámková V., Podrapska I., Schmitz G., Poledne R. Polymorphisms in the lipopolysaccharide-binding protein and bactericidal/permeability-increasing protein in patients with myocardial infarction. Clin. Chem. Lab. Med. 2002, 40:1097-1100.
16. Jack R.S., Fan X., Bernheiden M., Rune G., Ehlers M., Weber A., Kirsch G., Mentel R., Fürll B., Freudenberg M., et al. Lipopolysaccharide-binding protein is required to combat a murine gram-negative bacterial infection. Nature 1997, 389:742-745.
17. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 1991, 47:110-119.
18. Knapp S., Florquin S., Golenbock D.T., van der Poll T. Pulmonary lipopolysaccharide (LPS)-binding protein inhibits the LPS-induced lung inflammation invivo. J.Immunol. 2006, 176:3189-3195.
19. Kumpf O., Giamarellos-Bourboulis E.J., Koch A., Hamann L., Mouktaroudi M., Oh D.Y., Latz E., Lorenz E., Schwartz D.A., Ferwerda B., et al. Influence of genetic variations in TLR4 and TIRAP/Mal on the course of sepsis and pneumonia and cytokine release: an observational study in three cohorts. Crit. Care 2010, 14:R103.
20. Lamping N., Hoess A., Yu B., Park T.C., Kirschning C.J., Pfeil D., Reuter D., Wright S.D., Herrmann F., Schumann R.R. Effects of site-directed mutagenesis of basic residues (Arg 94, Lys 95, Lys 99) of lipopolysaccharide (LPS)-binding protein on binding and transfer of LPS and subsequent immune cell activation. J.Immunol. 1996, 157:4648-4656.
21. Lamping N., Dettmer R., Schröder N.W., Pfeil D., Hallatschek W., Burger R., Schumann R.R. LPS-binding protein protects mice from septic shock caused by LPS or gram-negative bacteria. J.Clin. Invest. 1998, 101:2065-2071.
22. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J.Appl. Cryst. 1993, 26:283-291.
23. Le Roy D., Di Padova F., Tees R., Lengacher S., Landmann R., Glauser M.P., Calandra T., Heumann D. Monoclonal antibodies to murine lipopolysaccharide (LPS)-binding protein (LBP) protect mice from lethal endotoxemia by blocking either the binding of LPS to LBP or the presentation of LPS/LBP complexes to CD14. J.Immunol. 1999, 162:7454-7460.
24. Lee B.Y., Cho S., Shin D.H., Kim H. Genome-wide association study of copy number variations associated with pulmonary function measures in Korea Associated Resource (KARE) cohorts. Genomics 2011, 97:101-105.
25. Mathison J.C., Tobias P.S., Wolfson E., Ulevitch R.J. Plasma lipopolysaccharide (LPS)-binding protein. A key component in macrophage recognition of gram-negative LPS. J.Immunol. 1992, 149:200-206.
26. McCoy A.J., Grosse-Kunstleve R.W., Storoni L.C., Read R.J. Likelihood-enhanced fast translation functions. Acta Crystallogr. D Biol. Crystallogr. 2005, 61:458-464.
27. Medzhitov R., Janeway C.A. Innate immunity: the virtues of a nonclonal system of recognition. Cell 1997, 91:295-298.
28. Mueller M., Stamme C., Draing C., Hartung T., Seydel U., Schromm A.B. Cell activation of human macrophages by lipoteichoic acid is strongly attenuated by lipopolysaccharide-binding protein. J.Biol. Chem. 2006, 281:31448-31456.
29. Muenzer J.T., Davis C.G., Chang K., Schmidt R.E., Dunne W.M., Coopersmith C.M., Hotchkiss R.S. Characterization and modulation of the immunosuppressive phase of sepsis. Infect. Immun. 2010, 78:1582-1592.
30. Ooi C.E., Weiss J., Elsbach P., Frangione B., Mannion B. A 25-kDa NH2-terminal fragment carries all the antibacterial activities of the human neutrophil 60-kDa bactericidal/permeability-increasing protein. J.Biol. Chem. 1987, 262:14891-14894.
31. Otwinowski, Z., and Minor, W. (1997). Processing of X-ray Diffraction Data Collected in Oscillation Mode. Methods in Enzymology, Volume 276: Macromolecular Crystallography, part A, 307-326.
32. Rietschel E.T., Brade H., Holst O., Brade L., Müller-Loennies S., Mamat U., Zähringer U., Beckmann F., Seydel U., Brandenburg K., et al. Bacterial endotoxin: Chemical constitution, biological recognition, host response, and immunological detoxification. Curr. Top. Microbiol. Immunol. 1996, 216:39-81.
33. Schedel M., Pinto L.A., Schaub B., Rosenstiel P., Cherkasov D., Cameron L., Klopp N., Illig T., Vogelberg C., Weiland S.K., et al. IRF-1 gene variations influence IgE regulation and atopy. Am. J. Respir. Crit. Care Med. 2008, 177:613-621.
34. Schröder N.W.J., Heine H., Alexander C., Manukyan M., Eckert J., Hamann L., Göbel U.B., Schumann R.R. Lipopolysaccharide binding protein binds to triacylated and diacylated lipopeptides and mediates innate immune responses. J.Immunol. 2004, 173:2683-2691.
35. Schumann R.R. Old and new findings on lipopolysaccharide-binding protein: a soluble pattern-recognition molecule. Biochem. Soc. Trans. 2011, 39:989-993.
36. Schumann R.R., Leong S.R., Flaggs G.W., Gray P.W., Wright S.D., Mathison J.C., Tobias P.S., Ulevitch R.J. Structure and function of lipopolysaccharide binding protein. Science 1990, 249:1429-1431.
37. Schumann R.R., Kirschning C.J., Unbehaun A., Aberle H.P., Knope H.P., Lamping N., Ulevitch R.J., Herrmann F. The lipopolysaccharide-binding protein is a secretory class 1 acute-phase protein whose gene is transcriptionally activated by APRF/STAT/3 and other cytokine-inducible nuclear proteins. Mol. Cell. Biol. 1996, 16:3490-3503.
38. Schumann R.R., Lamping N., Hoess A. Interchangeable endotoxin-binding domains in proteins with opposite lipopolysaccharide-dependent activities. J.Immunol. 1997, 159:5599-5605.
39. Takeuchi F., Yanai K., Inomata H., Kuzuya N., Kajio H., Honjo S., Takeda N., Kaburagi Y., Yasuda K., Shirasawa S., et al. Search of type 2 diabetes susceptibility gene on chromosome 20q. Biochem. Biophys. Res. Commun. 2007, 357:1100-1106.
40. Tobias P.S., Soldau K., Ulevitch R.J. Isolation of a lipopolysaccharide-binding acute phase reactant from rabbit serum. J.Exp. Med. 1986, 164:777-793.
41. Tobias P.S., Mathison J.C., Ulevitch R.J. A family of lipopolysaccharide binding proteins involved in responses to gram-negative sepsis. J.Biol. Chem. 1988, 263:13479-13481.
42. Tsukamoto H., Fukudome K., Takao S., Tsuneyoshi N., Kimoto M. Lipopolysaccharide-binding protein-mediated Toll-like receptor 4 dimerization enables rapid signal transduction against lipopolysaccharide stimulation on membrane-associated CD14-expressing cells. Int. Immunol. 2010, 22:271-280.
43. Vollmer T., Kleesiek K., Dreier J. Lipopolysaccharide-binding protein (LBP) gene polymorphisms: rapid genotyping by real-time PCR and association with infective endocarditis. Clin. Biochem. 2009, 42:1413-1419.
44. Vreugdenhil A.C., Rousseau C.H., Hartung T., Greve J.W., van't Veer C., Buurman W.A. Lipopolysaccharide (LPS)-binding protein mediates LPS detoxification by chylomicrons. J.Immunol. 2003, 170:1399-1405.
45. Weiss J., Elsbach P., Olsson I., Odeberg H. Purification and characterization of a potent bactericidal and membrane active protein from the granules of human polymorphonuclear leukocytes. J.Biol. Chem. 1978, 253:2664-2672.
46. Wurfel M.M., Kunitake S.T., Lichenstein H., Kane J.P., Wright S.D. Lipopolysaccharide (LPS)-binding protein is carried on lipoproteins and acts as a cofactor in the neutralization of LPS. J.Exp. Med. 1994, 180:1025-1035.
47. Wurfel M.M., Monks B.G., Ingalls R.R., Dedrick R.L., Delude R., Zhou D., Lamping N., Schumann R.R., Thieringer R., Fenton M.J., et al. Targeted deletion of the lipopolysaccharide (LPS)-binding protein gene leads to profound suppression of LPS responses exvivo, whereas invivo responses remain intact. J.Exp. Med. 1997, 186:2051-2056.
48. Yang K.K., Dorner B.G., Merkel U., Ryffel B., Schütt C., Golenbock D., Freeman M.W., Jack R.S. Neutrophil influx in response to a peritoneal infection with Salmonella is delayed in lipopolysaccharide-binding protein or CD14-deficient mice. J.Immunol. 2002, 169:4475-4480.
49. Zhan Q., Yuan M., Wang X.H., Duan X.M., Yang Q.D., Xia J. Association of lipopolysaccharide-binding protein gene polymorphisms with cerebral infarction in a Chinese population. J.Thromb. Thrombolysis 2012, 34:260-268.
50. Zweigner J., Gramm H.J., Singer O.C., Wegscheider K., Schumann R.R. High concentrations of lipopolysaccharide-binding protein in serum of patients with severe sepsis or septic shock inhibit the lipopolysaccharide response in human monocytes. Blood 2001, 98:3800-3808.