DOI: 10.4049/jimmunol.167.9.5231. <i>Escherichia coli</i>Braun Lipoprotein Induces a Lipopolysaccharide-Like Endotoxic Response from Primary Human Endothelial Cells

Escherichia coliBraun Lipoprotein Induces a Lipopolysaccharide-Like Endotoxic Response from Primary Human Endothelial Cells

10.4049/jimmunol.167.9.5231

Crossref journal-article

Oxford University Press (OUP)

The Journal of Immunology (286)

Abstract

AbstractAll bacteria contain proteins in which their amino-terminal cysteine residue is modified with N-acyl S-diacylglycerol functions, and peptides and proteins bearing this modification are immunomodulatory. The major outer membrane lipoprotein of Escherichia coli, the Braun lipoprotein (BLP), is the prototypical triacylated cysteinyl-modified protein. We find it is as active as LPS in stimulating human endothelial cells to an inflammatory phenotype, and a BLP-negative mutant of E. coli was less inflammatory than its parental strain. While the lipid modification was essential, the lipidated protein was more potent than a lipid-modified peptide. BLP associates with CD14, but this interaction, unlike that with LPS, was not required to elicit endothelial cell activation. BLP stimulated endothelial cell E-selectin surface expression, IL-6 secretion, and up-regulation of the same battery of cytokine mRNAs induced by LPS. Quantitative microarray analysis of 4400 genes showed the same 30 genes were induced by BLP and LPS, and that there was near complete concordance in the level of gene induction. We conclude that the lipid modification of at least one abundant Gram-negative protein is essential for endotoxic activity, but that the protein component also influences activity. The equivalent potency of BLP and LPS, and their complete concordance in the nature and extent of endothelial cell activation show that E. coli endotoxic activity is not due to just LPS. The major outer membrane protein of E. coli is a fully active endotoxic agonist for endothelial cells.

Bibliography

Neilsen, P. O., Zimmerman, G. A., & McIntyre, T. M. (2001). Escherichia coliBraun Lipoprotein Induces a Lipopolysaccharide-Like Endotoxic Response from Primary Human Endothelial Cells. The Journal of Immunology, 167(9), 5231â5239.

Authors 3

Paul O. Neilsen (first)
Guy A. Zimmerman (additional)
Thomas M. McIntyre (additional)

References 59 Referenced 40

Dates

Type	When
Created	11 years, 4 months ago (April 20, 2014, 11:19 p.m.)
Deposited	8 months ago (Jan. 2, 2025, 11:56 a.m.)
Indexed	1 month, 2 weeks ago (July 22, 2025, 7:04 a.m.)
Issued	23 years, 10 months ago (Nov. 1, 2001)
Published	23 years, 10 months ago (Nov. 1, 2001)
Published Print	23 years, 10 months ago (Nov. 1, 2001)

Funders 0

None

BibTeX

@article{Neilsen_2001, title={Escherichia coliBraun Lipoprotein Induces a Lipopolysaccharide-Like Endotoxic Response from Primary Human Endothelial Cells}, volume={167}, ISSN={1550-6606}, url={http://dx.doi.org/10.4049/jimmunol.167.9.5231}, DOI={10.4049/jimmunol.167.9.5231}, number={9}, journal={The Journal of Immunology}, publisher={Oxford University Press (OUP)}, author={Neilsen, Paul O. and Zimmerman, Guy A. and McIntyre, Thomas M.}, year={2001}, month=nov, pages={5231–5239} }

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      "doi-asserted-by": "crossref",
      "unstructured": "Arditi, M., J. Zhou, R. Dorio, G. W. Rong, S. M. Goyert, K. S. Kim. 1993. Endotoxin-mediated endothelial cell injury and activation: role of soluble CD14. Infect. Immun.\u200861: 3149",
      "DOI": "10.1128/iai.61.8.3149-3156.1993"
    },
    {
      "key": "2022123122380108200_R2",
      "doi-asserted-by": "crossref",
      "unstructured": "Pugin, J., C. C. Schurer-Maly, D. Leturcq, A. Moriarty, R. J. Ulevitch, P. S. Tobias. 1993. Lipopolysaccharide activation of human endothelial and epithelial cells is mediated by lipopolysaccharide-binding protein and soluble CD14. Proc. Natl. Acad. Sci. USA\u200890: 2744",
      "DOI": "10.1073/pnas.90.7.2744"
    },
    {
      "key": "2022123122380108200_R3",
      "doi-asserted-by": "crossref",
      "unstructured": "Frey, E. A., D. S. Miller, T. G. Jahr, A. Sundan, V. Bazil, T. Espevik, B. B. Finlay, S. D. Wright. 1992. Soluble CD14 participates in the response of cells to lipopolysaccharide. J. Exp. Med.\u2008176: 1665",
      "DOI": "10.1084/jem.176.6.1665"
    },
    {
      "key": "2022123122380108200_R4",
      "doi-asserted-by": "crossref",
      "unstructured": "Medzhitov, R., P. Preston-Hurlburt, C. A. Janeway, Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature\u2008388: 394",
      "DOI": "10.1038/41131"
    },
    {
      "key": "2022123122380108200_R5",
      "doi-asserted-by": "crossref",
      "unstructured": "Yang, R. B., M. R. Mark, A. Gray, A. Huang, M. H. Xie, M. Zhang, A. Goddard, W. I. Wood, A. L. Gurney, P. J. Godowski. 1998. Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature\u2008395: 284",
      "DOI": "10.1038/26239"
    },
    {
      "key": "2022123122380108200_R6",
      "doi-asserted-by": "crossref",
      "unstructured": "Muzio, M., G. Natoli, S. Saccani, M. Levrero, A. Mantovani. 1998. The human Toll signaling pathway: divergence of nuclear factor \u03baB and JNK/SAPK activation upstream of tumor necrosis factor receptor-associated factor 6 (TRAF6). J. Exp. Med.\u2008187: 2097",
      "DOI": "10.1084/jem.187.12.2097"
    },
    {
      "key": "2022123122380108200_R7",
      "doi-asserted-by": "crossref",
      "unstructured": "Zhang, F. X., C. J. Kirschning, R. Mancinelli, X. P. Xu, Y. Jin, E. Faure, A. Mantovani, M. Rothe, M. Muzio, M. Arditi. 1999. Bacterial lipopolysaccharide activates nuclear factor-\u03baB through interleukin-1 signaling mediators in cultured human dermal endothelial cells and mononuclear phagocytes. J. Biol. Chem.\u2008274: 7611",
      "DOI": "10.1074/jbc.274.12.7611"
    },
    {
      "key": "2022123122380108200_R8",
      "doi-asserted-by": "crossref",
      "unstructured": "Kirschning, C. J., H. Wesche, T. Merrill Ayres, M. Rothe. 1998. Human Toll-like receptor 2 confers responsiveness to bacterial lipopolysaccharide. J. Exp. Med.\u2008188: 2091",
      "DOI": "10.1084/jem.188.11.2091"
    },
    {
      "key": "2022123122380108200_R9",
      "doi-asserted-by": "crossref",
      "unstructured": "Chow, J. C., D. W. Young, D. T. Golenbock, W. J. Christ, F. Gusovsky. 1999. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J. Biol. Chem.\u2008274: 10689",
      "DOI": "10.1074/jbc.274.16.10689"
    },
    {
      "key": "2022123122380108200_R10",
      "doi-asserted-by": "crossref",
      "unstructured": "Takeuchi, O., K. Hoshino, T. Kawai, H. Sanjo, H. Takada, T. Ogawa, K. Takeda, S. Akira. 1999. Differential roles of TLR2 and TLR4 in recognition of Gram-negative and Gram-positive bacterial cell wall components. Immunity\u200811: 443",
      "DOI": "10.1016/S1074-7613(00)80119-3"
    },
    {
      "key": "2022123122380108200_R11",
      "doi-asserted-by": "crossref",
      "unstructured": "Braun, V., H. C. Wu. 1994. Lipoproteins, structure, function, biosynthesis, and model for protein export. J. M. Ghuysen, Jr, and R. Hakenbeck, Jr, eds. Bacterial Cell Wall\u2008319 Elsevier Science B. V., Amsterdam.",
      "DOI": "10.1016/S0167-7306(08)60417-2"
    },
    {
      "key": "2022123122380108200_R12",
      "doi-asserted-by": "crossref",
      "unstructured": "Muhlradt, P. F., H. Meyer, R. Jansen. 1996. Identification of S-(2, 3-dihydroxypropyl)cystein in a macrophage-activating lipopeptide from Mycoplasma fermentans. Biochemistry\u200835: 7781",
      "DOI": "10.1021/bi9602831"
    },
    {
      "key": "2022123122380108200_R13",
      "doi-asserted-by": "crossref",
      "unstructured": "Rawadi, G., S. Roman-Roman. 1996. Mycoplasma membrane lipoproteins induced proinflammatory cytokines by a mechanism distinct from that of lipopolysaccharide. Infect. Immun.\u200864: 637",
      "DOI": "10.1128/iai.64.2.637-643.1996"
    },
    {
      "key": "2022123122380108200_R14",
      "doi-asserted-by": "crossref",
      "unstructured": "Muhlradt, P. F., M. Kiess, H. Meyer, R. Sussmuth, G. Jung. 1998. Structure and specific activity of macrophage-stimulating lipopeptides from Mycoplasma\u2008hyorhinis. Infect. Immun.\u200866: 4804",
      "DOI": "10.1128/IAI.66.10.4804-4810.1998"
    },
    {
      "key": "2022123122380108200_R15",
      "doi-asserted-by": "crossref",
      "unstructured": "Melchers, F., V. Braun, C. Galanos. 1975. The lipoprotein of the outer membrane of Escherichia coli: a B-lymphocyte mitogen. J. Exp. Med.\u2008142: 473",
      "DOI": "10.1084/jem.142.2.473"
    },
    {
      "key": "2022123122380108200_R16",
      "doi-asserted-by": "crossref",
      "unstructured": "Bessler, W. G., M. Cox, A. Lex, B. Suhr, K. H. Wiesmuller, G. Jung. 1985. Synthetic lipopeptide analogs of bacterial lipoprotein are potent polyclonal activators for murine B lymphocytes. J. Immunol.\u2008135: 1900",
      "DOI": "10.4049/jimmunol.135.3.1900"
    },
    {
      "key": "2022123122380108200_R17",
      "doi-asserted-by": "crossref",
      "unstructured": "Erdile, L. F., M. A. Brandt, D. J. Warakomski, G. J. Westrack, A. Sadziene, A. G. Barbour, J. P. Mays. 1993. Role of attached lipid in immunogenicity of Borrelia burgdorferi OspA. Infect. Immun.\u200861: 81",
      "DOI": "10.1128/iai.61.1.81-90.1993"
    },
    {
      "key": "2022123122380108200_R18",
      "doi-asserted-by": "crossref",
      "unstructured": "Braun, V., K. Rehn. 1969. Chemical characterization, spatial distribution and function of a lipoprotein (murein-lipoprotein) of the E. coli cell wall: the specific effect of trypsin on the membrane structure. Eur. J. Biochem.\u200810: 426",
      "DOI": "10.1111/j.1432-1033.1969.tb00707.x"
    },
    {
      "key": "2022123122380108200_R19",
      "doi-asserted-by": "crossref",
      "unstructured": "Hoffmann, P., S. Heinle, U. F. Schade, H. Loppnow, A. J. Ulmer, H. D. Flad, G. Jung, W. G. Bessler. 1988. Stimulation of human and murine adherent cells by bacterial lipoprotein and synthetic lipopeptide analogues. Immunobiology\u2008177: 158",
      "DOI": "10.1016/S0171-2985(88)80036-6"
    },
    {
      "key": "2022123122380108200_R20",
      "doi-asserted-by": "crossref",
      "unstructured": "Seifert, R., G. Schultz, M. Richter-Freund, J. Metzger, K. H. Wiesmuller, G. Jung, W. G. Bessler, S. Hauschildt. 1990. Activation of superoxide formation and lysozyme release in human neutrophils by the synthetic lipopeptide Pam3Cys-Ser-(Lys)4: involvement of guanine-nucleotide-binding proteins and synergism with chemotactic peptides. Biochem. J.\u2008267: 795",
      "DOI": "10.1042/bj2670795"
    },
    {
      "key": "2022123122380108200_R21",
      "doi-asserted-by": "crossref",
      "unstructured": "Berg, M., S. Offermanns, R. Seifert, G. Schultz. 1994. Synthetic lipopeptide Pam3CysSer(Lys)4 is an effective activator of human platelets. Am. J. Physiol.\u2008266: C1684",
      "DOI": "10.1152/ajpcell.1994.266.6.C1684"
    },
    {
      "key": "2022123122380108200_R22",
      "doi-asserted-by": "crossref",
      "unstructured": "Radolf, J. D., L. L. Arndt, D. R. Akins, L. L. Curetty, M. E. Levi, Y. Shen, L. S. Davis, M. V. Norgard. 1995. Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides activate monocytes/macrophages. J. Immunol.\u2008154: 2866",
      "DOI": "10.4049/jimmunol.154.6.2866"
    },
    {
      "key": "2022123122380108200_R23",
      "doi-asserted-by": "crossref",
      "unstructured": "Sellati, T. J., L. D. Abrescia, J. D. Radolf, M. B. Furie. 1996. Outer surface lipoproteins of Borrelia burgdorferi activate vascular endothelium in vitro. Infect. Immun.\u200864: 3180",
      "DOI": "10.1128/iai.64.8.3180-3187.1996"
    },
    {
      "key": "2022123122380108200_R24",
      "doi-asserted-by": "crossref",
      "unstructured": "Sellati, T. J., D. A. Bouis, R. L. Kitchens, R. P. Darveau, J. Pugin, R. J. Ulevitch, S. C. Gangloff, S. M. Goyert, M. V. Norgard, J. D. Radolf. 1998. Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides activate monocytic cells via a CD14-dependent pathway distinct from that used by lipopolysaccharide. J. Immunol.\u2008160: 5455",
      "DOI": "10.4049/jimmunol.160.11.5455"
    },
    {
      "key": "2022123122380108200_R25",
      "doi-asserted-by": "crossref",
      "unstructured": "Sellati, T. J., M. J. Burns, M. A. Ficazzola, M. B. Furie. 1995. Borrelia burgdorferi up-regulates expression of adhesion molecules on endothelial cells and promotes transendothelial migration of neutrophils in vitro. Infect. Immun.\u200863: 4439",
      "DOI": "10.1128/iai.63.11.4439-4447.1995"
    },
    {
      "key": "2022123122380108200_R26",
      "doi-asserted-by": "crossref",
      "unstructured": "Ebnet, K., K. D. Brown, U. K. Siebenlist, M. M. Simon, S. Shaw. 1997. Borrelia burgdorferi activates nuclear factor-\u03baB and is a potent inducer of chemokine and adhesion molecule gene expression in endothelial cells and fibroblasts. J. Immunol.\u2008158: 3285",
      "DOI": "10.4049/jimmunol.158.7.3285"
    },
    {
      "key": "2022123122380108200_R27",
      "doi-asserted-by": "crossref",
      "unstructured": "Riley, B. S., N. Oppenheimer-Marks, E. J. Hansen, J. D. Radolf, M. V. Norgard. 1992. Virulent Treponema pallidum activates human vascular endothelial cells. J. Infect. Dis.\u2008165: 484",
      "DOI": "10.1093/infdis/165.3.484"
    },
    {
      "key": "2022123122380108200_R28",
      "doi-asserted-by": "crossref",
      "unstructured": "Ma, Y., J. J. Weis. 1993. Borrelia burgdorferi outer surface lipoproteins OspA and OspB possess B-cell mitogenic and cytokine-stimulatory properties. Infect. Immun.\u200861: 3843",
      "DOI": "10.1128/iai.61.9.3843-3853.1993"
    },
    {
      "key": "2022123122380108200_R29",
      "doi-asserted-by": "crossref",
      "unstructured": "Wooten, R. M., V. R. Modur, T. M. McIntyre, J. J. Weis. 1996. Borrelia burgdorferi outer membrane protein A induces nuclear translocation of nuclear factor-\u03baB and inflammatory activation in human endothelial cells. J. Immunol.\u2008157: 4584",
      "DOI": "10.4049/jimmunol.157.10.4584"
    },
    {
      "key": "2022123122380108200_R30",
      "doi-asserted-by": "crossref",
      "unstructured": "Aliprantis, A. O., R. B. Yang, M. R. Mark, S. Suggett, B. Devaux, J. D. Radolf, G. R. Klimpel, P. Godowski, A. Zychlinsky. 1999. Cell activation and apoptosis by bacterial lipoproteins through Toll-like receptor-2. Science\u2008285: 736",
      "DOI": "10.1126/science.285.5428.736"
    },
    {
      "key": "2022123122380108200_R31",
      "doi-asserted-by": "crossref",
      "unstructured": "Brightbill, H. D., D. H. Libraty, S. R. Krutzik, R. B. Yang, J. T. Belisle, J. R. Bleharski, M. Maitland, M. V. Norgard, S. E. Plevy, S. T. Smale, et al\u20081999. Host defense mechanisms triggered by microbial lipoproteins through Toll-like receptors. Science\u2008285: 732",
      "DOI": "10.1126/science.285.5428.732"
    },
    {
      "key": "2022123122380108200_R32",
      "doi-asserted-by": "crossref",
      "unstructured": "Hirschfeld, M., C. J. Kirschning, R. Schwandner, H. Wesche, J. H. Weis, R. M. Wooten, J. J. Weis. 1999. Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by Toll-like receptor. J. Immunol.\u2008163: 2382",
      "DOI": "10.4049/jimmunol.163.5.2382"
    },
    {
      "key": "2022123122380108200_R33",
      "doi-asserted-by": "crossref",
      "unstructured": "Lien, E., T. J. Sellati, A. Yoshimura, T. H. Flo, G. Rawadi, R. W. Finberg, J. D. Carroll, T. Espevik, R. R. Ingalls, J. D. Radolf, D. T. Golenbock. 1999. Toll-like receptor 2 functions as a pattern recognition receptor for diverse bacterial products. J. Biol. Chem.\u2008274: 33419",
      "DOI": "10.1074/jbc.274.47.33419"
    },
    {
      "key": "2022123122380108200_R34",
      "doi-asserted-by": "crossref",
      "unstructured": "Janeway, C. A., R. Medzhitov. 1999. Lipoproteins take their toll on the host. Curr. Biol.\u20089: R879",
      "DOI": "10.1016/S0960-9822(00)80073-1"
    },
    {
      "key": "2022123122380108200_R35",
      "doi-asserted-by": "crossref",
      "unstructured": "Faure, E., O. Equils, P. A. Sieling, L. Thomas, F. X. Zhang, C. J. Kirschning, N. Polentarutti, M. Muzio, M. Arditi. 2000. Bacterial lipopolysaccharide activates NF-\u03baB through Toll-like receptor 4 (TLR-4) in cultured human dermal endothelial cells: differential expression of TLR-4 and TLR-2 in endothelial cells. J. Biol. Chem.\u2008275: 11058",
      "DOI": "10.1074/jbc.275.15.11058"
    },
    {
      "key": "2022123122380108200_R36",
      "doi-asserted-by": "crossref",
      "unstructured": "Schwandner, R., R. Dziarski, H. Wesche, M. Rothe, C. J. Kirschning. 1999. Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by Toll-like receptor 2. J. Biol. Chem.\u2008274: 17406",
      "DOI": "10.1074/jbc.274.25.17406"
    },
    {
      "key": "2022123122380108200_R37",
      "doi-asserted-by": "crossref",
      "unstructured": "Yoshimura, A., E. Lien, R. R. Ingalls, E. Tuomanen, R. Dziarski, D. Golenbock. 1999. Cutting edge: recognition of Gram-positive bacterial cell wall components by the innate immune system occurs via Toll-like receptor 2. J. Immunol.\u2008163: 1",
      "DOI": "10.4049/jimmunol.163.1.1"
    },
    {
      "key": "2022123122380108200_R38",
      "doi-asserted-by": "crossref",
      "unstructured": "Haziot, A., N. Hijiya, K. Schultz, F. Zhang, S. C. Gangloff, S. M. Goyert. 1999. CD14 plays no major role in shock induced by Staphylococcus aureus but down-regulates TNF-\u03b1 production. J. Immunol.\u2008162: 4801",
      "DOI": "10.4049/jimmunol.162.8.4801"
    },
    {
      "key": "2022123122380108200_R39",
      "doi-asserted-by": "crossref",
      "unstructured": "Zimmerman, G. A., T. M. McIntyre, S. M. Prescott. 1985. Thrombin stimulates the adherence of neutrophils to human endothelial cells in vitro. J. Clin. Invest.\u200876: 2235",
      "DOI": "10.1172/JCI112232"
    },
    {
      "key": "2022123122380108200_R40",
      "doi-asserted-by": "crossref",
      "unstructured": "Zimmerman, G. A., T. M. McIntyre, M. Mehra, S. M. Prescott. 1990. Endothelial cell-associated platelet-activating factor: a novel mechanism for signaling intercellular adhesion. J. Cell Biol.\u2008110: 529",
      "DOI": "10.1083/jcb.110.2.529"
    },
    {
      "key": "2022123122380108200_R41",
      "doi-asserted-by": "crossref",
      "unstructured": "Inouye, S., K. Takeishi, N. Lee, M. DeMartini, A. Hirashima, M. Inouye. 1976. Lipoprotein from the outer membrane of Escherichia coli: purification, paracrystallization, and some properties of its free form. J. Bacteriol.\u2008127: 555",
      "DOI": "10.1128/jb.127.1.555-563.1976"
    },
    {
      "key": "2022123122380108200_R42",
      "doi-asserted-by": "crossref",
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      "DOI": "10.4049/jimmunol.160.11.5485"
    },
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    },
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      "DOI": "10.4049/jimmunol.162.7.3749"
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      "DOI": "10.4049/jimmunol.162.10.5666"
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      "DOI": "10.4049/jimmunol.153.6.2653"
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      "DOI": "10.4049/jimmunol.163.12.6748"
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      "key": "2022123122380108200_R52",
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      "DOI": "10.1038/nsb0298-115"
    },
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      "key": "2022123122380108200_R53",
      "doi-asserted-by": "crossref",
      "unstructured": "Braun, V., H. Rotering, J. P. Ohms, H. Hagenmaier. 1976. Conformational studies on murein-lipoprotein from the outer membrane of Escherichia coli. Eur. J. Biochem.\u200870: 601",
      "DOI": "10.1111/j.1432-1033.1976.tb11051.x"
    },
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      "doi-asserted-by": "crossref",
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      "DOI": "10.1515/bchm3.1994.375.6.407"
    },
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      "key": "2022123122380108200_R55",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1201/9781003064961-25"
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      "DOI": "10.1128/IAI.66.3.1135-1141.1998"
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      "unstructured": "Kreutz, M., U. Ackermann, S. Hauschildt, S. W. Krause, D. Riedel, W. Bessler, R. Andreesen. 1997. A comparative analysis of cytokine production and tolerance induction by bacterial lipopeptides, lipopolysaccharides and Staphylococcus\u2008aureus in human monocytes. Immunology\u200892: 396",
      "DOI": "10.1046/j.1365-2567.1997.00365.x"
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      "DOI": "10.1084/jem.166.4.1098"
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