Deficiency of mannose-binding lectin greatly increases susceptibility to postburn infection with Pseudomonas aeruginosa

Journal of Immunology

Volumn 176, Issue 3, 2006, Pages 1769-1775

  Møller Kristensen, Mette ^a,b   Ip, W K Eddie ^a   Shi, Lei ^a,c   Gowda, Lakshmi D ^a   Hamblin, Michael R ^a   Thiel, Steffen ^b   Jensenius, Jens Chr ^b   Ezekowitz, R Alan B ^a   Takahashi, Kazue ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b AARHUS UNIVERSITY   (Denmark)

^c CENTOCOR INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT; INTERLEUKIN 6; MANNOSE BINDING LECTIN; PEPTIDE DERIVATIVE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BURN INFECTION; COMORBIDITY; CONTROLLED STUDY; DISEASE PREDISPOSITION; EFFECTOR CELL; GRAM NEGATIVE BACTERIUM; HOST; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFECTION SENSITIVITY; INFLAMMATION; INOCULATION; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SEPTICEMIA; SYMBIONT; WILD TYPE;

EID: 31144468724     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.3.1769     Document Type: Article

References (66)

1. Krutzik, S. R., P. A. Sieling, and R. L. Modlin. 2001. The role of Toll-like receptors in host defense against microbial infection. Curr. Opin. Immunol. 13: 104-108.
2. Hoffmann, J. A., F. C. Kafatos, C. A. Janeway, and R. A. Ezekowitz. 1999. Phylogenetic perspectives in innate immunity. Science 284: 1313-1318.
3. Holmskov, U., S. Thiel, and J. C. Jensenius. 2003. Collections and ficolins: humoral lectins of the innate immune defense. Annu. Rev. Immunol. 21: 547-578.
4. Fraser, I. P., H. Koziel, and R. A. Ezekowitz. 1998. The serum mannose-binding protein and the macrophage mannose receptor are pattern recognition molecules that link innate and adaptive immunity. Semin. Immunol. 10: 363-372.
5. Epstein, J., Q. Eichbaum, S. Sheriff, and R. A. Ezekowitz. 1996. The collectins in innate immunity. Curr. Opin. Immunol. 8: 29-35.
6. Ogden, C. A., A. deCathelineau, P. R. Hoffmann, D. Bratton, B. Ghebrehiwet, V. A. Fadok, and P. M. Henson. 2001. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J. Exp. Med. 194: 781-795.
7. Nauta, A. J., N. Raaschou-Jensen, A. Roos, M. R. Daha, H. O. Madsen, M. C. Borrias-Essers, L. P. Ryder, C. Koch, and P. Garred. 2003. Mannose-binding lectin engagement with late apoptotic and necrotic cells. Eur. J. Immunol. 33: 2853-2863.
8. Stuart, L. M., K. Takahashi, L. Shi, J. Savill, and R. A. Ezekowitz. 2005. Mannose-binding lectin-deficient mice display defective apoptotic cell clearance but no autoimmune phenotype. J. Immunol. 174: 3220-3226.
9. Saevarsdottir, S., T. Vikingsdottir, and H. Valdimarsson. 2004. The potential role of mannan-binding lectin in the clearance of self-components including immune complexes. Scand. J. Immunol. 60: 23-29.
10. Thiel, S., T. Vorup-Jensen, C. M. Stover, W. Schwaeble, S. B. Laursen, K. Poulsen, A. C. Willis, P. Eggleton, S. Hansen, U. Holmskov, et al. 1997. A second serine protease associated with mannan-binding lectin that activates complement. Nature 386: 506-510.
11. Matsushita, M., and T. Fujita. 1992. Activation of the classical complement pathway by mannose-binding protein in association with a novel C1s-like serine protease. J. Exp. Med. 176: 1497-1502.
12. Sparkes, B. G. 1997. Immunological responses to thermal injury. Burns 23: 106-113.
13. Schwacha, M. G. 2003. Macrophages and post-burn immune dysfunction. Burns 29: 1-14.
14. Allgöwer, M., G. A. Schoenenberger, and B. G. Sparkes. 1995. Burning the largest immune organ. Burns 21(Suppl. 1): S7-S47.
15. Pruitt, B. A., Jr., A. T. McManus, S. H. Kim, and C. W. Goodwin. 1998. Burn wound infections: current status. World J. Surg. 22; 135-145.
16. Revathi, G., J. Puri, and B. K. Jain. 1998. Bacteriology of burns. Burns 24: 347-349.
17. Song, W., K. M. Lee, H. J. Kang, D. H. Shin, and D. K. Kim. 2001. Microbiologic aspects of predominant bacteria isolated from the burn patients in Korea. Burns 27: 136-139.
18. Selsted, M. E., and A. J. Ouellette. 2005. Mammalian defensins in the antimicrobial immune response. Nat. Immunol. 6: 551-557.
19. Armstrong, D. G., and E. B. Jude. 2002. The role of matrix metalloproteinases in wound healing. J. Am. Podiatr. Med. Assoc. 92: 12-18.
20. Borregaard, N., K. Theilgaard-Mönch, J. B. Cowland, M. Ståhle, and O. E. Sørensen. 2005. Neutrophils and keratinocytes in innate immunity: cooperative actions to provide antimicrobial defense at the right time and place. J. Leukocyte Biol. 77: 439-443.
21. Arturson, G. 1979. Microvascular permeability to macromolecules in thermal injury. Acta Physiol. Scand. Suppl. 463: 111-122.
22. Ward, P. A., and G. O. Till, 1990. Pathophysiologic events related to thermal injury of skin. J. Trauma 30: S75-S79.
23. Reading, P. C., L. S. Morey, E. C. Crouch, and E. M. Anders. 1997. Cotlectin-mediated antiviral host defense of the lung: evidence from influenza virus infection of mice. J. Virol. 71: 8204-8212.
24. Shi, L., K. Takahashi, J. Dundee, S. Shahroor-Karni, S. Thiel, J. C. Jensenius, F. Gad, M. R. Hamblin, K. N. Sastry, and R. A. Ezekowitz. 2004. Mannose-binding lectin-deficient mice are susceptible to infection with Staphylococcus aureus. J. Exp. Med. 199: 1379-1390.
25. Gadjeva, M., S. R. Paludan, S. Thiel, V. Slavov, M. Ruseva, K. Eriksson, G. B. Lowhagen, L. Shi, K. Takahashi, A. Ezekowitz, and J. C. Jensenius. 2004. Mannan-binding lectin modulates the response to HSV-2 infection. Clin. Exp. Immunol. 138: 304-311.
26. Shankowsky, H. A., L. S. Callioux, and E. E. Tredget. 1994. North American survey of hydrotherapy in modern burn care. J. Burn Care Rehabil 15: 143-146.
27. Tredget, E. E., H. A. Shankowsky, R. Rennie, R. E. Burrell, and S. Logsetty. 2004. Pseudomonas infections in the thermally injured patient. Burns 30: 3-26.
28. Martin, M. A. 1993. Nosocomial infections in intensive care units: an overview of their epidemiology, outcome, and prevention. New Horiz. 1: 162-171.
29. Sadikot, R. T., T. S. Blackwell, J. W. Christman, and A. S. Prince. 2005. Pathogen-host interactions in Pseudomonas aeruginosa pneumonia. Am. J. Respir. Crit. Care Med. 171: 1209-1223.
30. Hamblin, M. R., T. Zahra, C. H. Contag, A. T. McManus, and T. Hasan. 2003. Optical monitoring and treatment of potentially lethal wound infections in vivo. J. Infect. Dis. 187: 1717-1725.
31. Vorup-Jensen, T., U. B. Jensen, H. Liu, T. Kawasaki, K. Uemura, S. Thiel, F. Dagnaes-Hansen, and T. G. Jensen. 2001. Tail-vein injection of mannan-binding lectin DNA leads to high expression levels of multimeric protein in liver. Mol. Ther. 3: 867-874.
32. Liu, H., L. Jensen, S. Hansen, S. V. Petersen, K. Takahashi, A. B. Ezekowitz, F. D. Hansen, J. C. Jensenius, and S. Thiel. 2001. Characterization and quantification of mouse mannan-binding lectins (MBL-A and MBL-C) and study of acute phase responses. Scand. J. Immunol. 53: 489-497.
33. Thiel, S., M. Møller-Kristensen, L. Jensen, and J. C. Jensenius. 2002. Assays for the functional activity of the mannan-binding lectin pathway of complement activation. Immunobiology 205: 446-454.
34. Neth, O., D. L. Jack, A. W. Dodds, H. Holzel, N. J. Klein, and M. W. Turner. 2000. Mannose-binding lectin binds to a range of clinically relevant microorganisms and promotes complement deposition. Infect. Immun. 68: 688-693.
35. Kuipers, S., P. C. Aerts, and H. van Dijk. 2003. Differential microorganism-induced mannose-binding lectin activation. FEMS Immunol. Med. Microbiol. 36: 33-39.
36. Neely, A. N., D. L. Hoover, I. A. Holder, and A. S. Cross. 1996. Circulating levels of tumour necrosis factor, interleukin 6 and proteolytic activity in a murine model of burn and infection. Burns 22: 524-530.
37. Yamada, Y., S. Endo, and K. Inada. 1996. Plasma cytokine levels in patients with severe burn injury-with reference to the relationship between infection and prognosis. Burns 22: 587-593.
38. Rumbaugh, K. P., A. N. Hamood, and J. A. Griswold. 2004. Cytokine induction by the P. aeruginosa quorum sensing system during thermal injury. J. Surg. Res. 116: 137-144.
39. Alexander, J. W., L. Gianotti, T. Pyles, M. A. Carey, and G. F. Babcock. 1991. Distribution and survival of Escherichia coli translocating from the intestine after thermal injury. Ann. Surg. 213: 558-566.
40. Eaves-Pyles, T., and J. W. Alexander. 2001. Comparison of translocation of different types of microorganisms from the intestinal tract of burned mice. Shock 16: 148-152.
41. Steinstraesser, L., Y. Oezdogan, S. C. Wang, and H. U. Steinau. 2004. Host defense peptides in burns. Burns 30: 619-627.
42. Klasen, H. J. 2000. Historical review of the use of silver in the treatment of burns. I. Early uses. Burns 26: 117-130.
43. McManus, A. T., A. D. Mason, Jr., W. F. McManus, and B. A. Pruitt, Jr. 1985. Twenty-five year review of Pseudomonas aeruginosa bacteremia in a burn center. Eur. J. Clin. Microbiol. 4: 219-223.
44. Sumiya, M., M. Super, P. Tabona, R. J. Levinsky, T. Arai, M. W. Turner, and J. A. Summerfield. 1991. Molecular basis of opsonic defect in immunodeficient children. Lancet 337: 1569-1570.
45. Steffensen, R., S. Thiel, K. Varming, C. Jersild, and J. C. Jensenius. 2000. Detection of structural gene mutations and promoter polymorphisms in the mannan-binding lectin (MBL) gene by polymerase chain reaction with sequence-specific primers. J. Immunol. Methods 241: 33-42.
46. Super, M., S. Thiel, J. Lu, R. J. Levinsky, and M. W. Turner. 1989. Association of low levels of mannan-binding protein with a common defect of opsonisation. Lancet 2: 1236-1239.
47. Madsen, H. O., M. L. Satz, B. Hogh, A. Svejgaard, and P. Garred. 1998. Different molecular events result in low protein levels of mannan-binding lectin in populations from southeast Africa and South America. J. Immunol. 161: 3169-3175.
48. Sumiya, M., and J. A. Summerfield. 1996. Mannose-binding protein, genetic variants and the risk of infection. QJM 89: 723-726.
49. Super, M., S. D. Gillies, S. Foley, K. Sastry, J. E. Schweinle, V. J. Silverman, and R. A. Ezekowitz. 1992. Distinct and overlapping functions of allelic forms of human mannose binding protein. Nat. Genet. 2: 50-55.
50. Christiansen, O. B., D. C. Kilpatrick, V. Souter, K. Varming, S. Thiel, and J. C. Jensenius. 1999. Mannan-binding lectin deficiency is associated with unexplained recurrent miscarriage. Scand. J. Immunol. 49: 193-196.
51. Peterslund, N. A., C. Koch, J. C. Jensenius, and S. Thiel. 2001. Association between deficiency of mannose-binding lectin and severe infections after chemotherapy. Lancet 358: 637-638.
52. Neth, O., I. Hann, M. W. Turner, and N. J. Klein. 2001. Deficiency of mannose-binding lectin and burden of infection in children with malignancy: a prospective study. Lancet 358: 614-618.
53. Siassi, M., W. Hohenberger, and J. Riese. 2003. Mannan-binding lectin (MBL) serum levels and post-operative infections. Biochem. Soc. Trans. 31: 774-775.
54. Ytting, H., J. C. Jensenius, I. J. Christensen, S. Thiel, and H. J. Nielsen. 2004. Increased activity of the mannan-binding lectin complement activation pathway in patients with colorectal cancer. Scand. J. Gastroenterol. 39: 674-679.
55. Mullighan, C. G., S. Heatley, K. Doherty, F. Szabo, A. Grigg, T. P. Hughes, A. P. Schwarer, J. Szer, B. D. Tait, L. Bik To, and P. G. Bardy. 2002. Mannose-binding lectin gene polymorphisms are associated with major infection following allogeneic hemopoietic stem cell transplantation. Blood 99: 3524-3529.
56. Kilpatrick, D. C., T. E. Delahooke, C. Koch, M. L. Turner, and P. C. Hayes. 2003. Mannan-binding lectin and hepatitis C infection. Clin. Exp. Immunol. 132: 92-95.
57. Bergmann, O. J., M. Christiansen, I. Laursen, P. Bang, N. E. Hansen, J. Ellegaard, C. Koch, and V. Andersen. 2003. Low levels of mannose-binding lectin do not affect occurrence of severe infections or duration of fever in acute myeloid leukaemia during remission induction therapy. Eur. J. Haematol. 70: 91-97.
58. Carlsson, M., A. G. Sjoholm, L. Eriksson, S. Thiel, J. C. Jensenius, M. Segelmark, and L. Truedsson. 2005. Deficiency of the mannan-binding lectin pathway of complement and poor outcome in cystic fibrosis: bacterial colonization may be decisive for a relationship. Clin. Exp. Immunol. 139: 306-313.
59. Neth, O., D. L. Jack, M. Johnson, N. J. Klein, and M. W. Turner. 2002. Enhancement of complement activation and opsonophagocytosis by complexes of mannose-binding lectin with mannose-binding lectin-associated serine protease after binding to Staphylococcus aureus. J. Immunol. 169: 4430-4436.
60. Childs, R. A., T. Feizi, C. T. Yuen, K. Drickamer, and M. S. Quesenberry. 1990. Differential recognition of core and terminal portions of oligosaccharide ligands by carbohydrate-recognition domains of two mannose-binding proteins. J. Biol. Chem. 265: 20770-20777.
61. Lee, R. T., Y. Ichikawa, M. Fay, K. Drickamer, M. C. Shao, and Y. C. Lee. 1991. Ligand-binding characteristics of rat serum-type mannose-binding protein (MBP-A): homology of binding site architecture with mammalian and chicken hepatic lectins. J. Biol. Chem. 266: 4810-4815.
62. Kupper, T. S., and R. C. Fuhlbrigge. 2004. Immune surveillance in the skin: mechanisms and clinical consequences. Nat. Rev. Immunol. 4: 211-222.
63. Wellmer, A., J. Gerber, J. Ragheb, G. Zysk, T. Kunst, A. Smirnov, W. Brack, and R. Nau. 2001. Effect of deficiency of tumor necrosis factor α or both of its receptors on Streptococcus pneumoniae central nervous system infection and peritonitis. Infect. Immun. 69: 6881-6886.
64. Netea, M. G., L. J. van Tits, J. H. Curfs, F. Amiot, J. F. Meis, J. W. van der Meer, and B. J. Kullberg. 1999. Increased susceptibility of TNF-α lymphotoxin-α double knockout mice to systemic candidiasis through impaired recruitment of neutrophils and phagocytosis of Candida albicans. J. Immunol. 163: 1498-1505.
65. Gardai, S. J., Y. Q. Xiao, M. Dickinson, J. A. Nick, D. R. Voelker, K. E. Greene, and P. M. Henson. 2003. By binding SIRPα or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell 115: 13-23.
66. National Nosocomial Infections Surveillance (NNIS) System Report, Data Summary from January 1992 through June 2004. October 2004. Am. J. Infect. Control 32: 470-485.