Mannose-binding lectin regulates host resistance and pathology during experimental infection with Trypanosoma cruzi

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Rothfuchs, Antonio Gigliotti ^a,d   Roffê, Ester ^a   Gibson, Amanda ^a   Cheever, Allen W ^a,b   Ezekowitz, R Alan B ^c,f   Takahashi, Kazue ^c   Steindel, Mario ^e   Sher, Alan ^a   Báfica, André ^e  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d KAROLINSKA INSTITUTE   (Sweden)

^e FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^f Abide Therapeutics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 6; HYDROXYPROLINE; INTERLEUKIN 12; INTERLEUKIN 23; INTERLEUKIN 23P40; MANNOSE BINDING LECTIN; UNCLASSIFIED DRUG; INTERLEUKIN 12P40;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHAGAS DISEASE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION REGULATION; HEART MUSCLE FIBROSIS; HISTOPATHOLOGY; HOST RESISTANCE; IMMUNOPATHOLOGY; INFECTION SENSITIVITY; MALE; MBL GENE; MOUSE; MYOCARDITIS; NONHUMAN; PARASITE LOAD; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; ANIMAL; BIOSYNTHESIS; BLOOD; CARDIOMYOPATHY; DEFICIENCY; DISEASE RESISTANCE; FIBROSIS; HEART MUSCLE; HOST PARASITE INTERACTION; HUMAN; IMMUNOLOGY; METABOLISM; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; TRYPANOSOMA CRUZI;

MUS; PROTOZOA; TRYPANOSOMA CRUZI;

ANIMALS; CARDIOMYOPATHIES; CHAGAS DISEASE; DISEASE RESISTANCE; FIBROSIS; HOST-PARASITE INTERACTIONS; HUMANS; INTERLEUKIN-12 SUBUNIT P40; MANNOSE-BINDING LECTIN; MICE; MYOCARDIUM; PARASITE LOAD; TRYPANOSOMA CRUZI;

EID: 84883715816     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047835     Document Type: Article

References (54)

1. Holmskov U, Thiel S, Jensenius JC (2003) Collectins and ficolins: humoral lectins of the innate immune defense. Annu Rev Immunol 21: 547-578.
2. Super M, Thiel S, Lu J, Levinsky RJ, Turner MW (1989) Association of low levels of mannan-binding protein with a common defect of opsonisation. Lancet 2: 1236-1239.
3. Thiel S, Frederiksen PD, Jensenius JC (2006) Clinical manifestations of mannanbinding lectin deficiency. Mol Immunol 43: 86-96.
4. Ezekowitz RA (2003) Role of the mannose-binding lectin in innate immunity. J Infect Dis 187 Suppl 2: S335-339.
5. Shi L, Takahashi K, Dundee J, Shahroor-Karni S, Thiel S, et al. (2004) Mannose-binding lectin-deficient mice are susceptible to infection with Staphylococcus aureus. J Exp Med 199: 1379-1390.
6. Turner MW, Hamvas RM (2000) Mannose-binding lectin: structure, function, genetics and disease associations. Rev Immunogenet 2: 305-322.
7. Hansen S, Thiel S, Willis A, Holmskov U, Jensenius JC (2000) Purification and characterization of two mannan-binding lectins from mouse serum. J Immunol 164: 2610-2618.
8. Takahashi K, Shi L, Gowda LD, Ezekowitz RA (2005) Relative roles of complement factor 3 and mannose-binding lectin in host defense against infection. Infect Immun 73: 8188-8193.
9. Gadjeva M, Paludan SR, Thiel S, Slavov V, Ruseva M, et al. (2004) Mannanbinding lectin modulates the response to HSV-2 infection. Clin Exp Immunol 138: 304-311.
10. Held K, Thiel S, Loos M, Petry F (2008) Increased susceptibility of complement factor B/C2 double knockout mice and mannan-binding lectin knockout mice to systemic infection with Candida albicans. Mol Immunol 45: 3934-3941.
11. Ip WK, Takahashi K, Moore KJ, Stuart LM, Ezekowitz RA (2008) Mannosebinding lectin enhances Toll-like receptors 2 and 6 signaling from the phagosome. J Exp Med 205: 169-181.
12. Moller-Kristensen M, Ip WK, Shi L, Gowda LD, Hamblin MR, et al. (2006) Deficiency of mannose-binding lectin greatly increases susceptibility to postburn infection with Pseudomonas aeruginosa. J Immunol 176: 1769-1775.
13. Takahashi K, Gordon J, Liu H, Sastry KN, Epstein JE, et al. (2002) Lack of mannose-binding lectin-A enhances survival in a mouse model of acute septic peritonitis. Microbes Infect 4: 773-784.
14. Moller-Kristensen M, Wang W, Ruseva M, Thiel S, Nielsen S, et al. (2005) Mannan-binding lectin recognizes structures on ischaemic reperfused mouse kidneys and is implicated in tissue injury. Scand J Immunol 61: 426-434.
15. WHO (2002) The world health report.
16. Tarleton RL (2007) Immune system recognition of Trypanosoma cruzi. Curr Opin Immunol 19: 430-434.
17. Campos MA, Closel M, Valente EP, Cardoso JE, Akira S, et al. (2004) Impaired production of proinflammatory cytokines and host resistance to acute infection with Trypanosoma cruzi in mice lacking functional myeloid differentiation factor 88. J Immunol 172: 1711-1718.
18. Bafica A, Santiago HC, Goldszmid R, Ropert C, Gazzinelli RT, et al. (2006) Cutting edge: TLR9 and TLR2 signaling together account for MyD88- dependent control of parasitemia in Trypanosoma cruzi infection. J Immunol 177: 3515-3519.
19. Tomlinson S, Raper J (1998) Natural human immunity to trypanosomes. Parasitol Today 14: 354-359.
20. Ferreira V, Valck C, Sanchez G, Gingras A, Tzima S, et al. (2004) The classical activation pathway of the human complement system is specifically inhibited by calreticulin from Trypanosoma cruzi. J Immunol 172: 3042-3050.
21. Cestari Idos S, Krarup A, Sim RB, Inal JM, Ramirez MI (2009) Role of early lectin pathway activation in the complement-mediated killing of Trypanosoma cruzi. Mol Immunol 47: 426-437.
22. Boldt AB, Luz PR, Messias-Reason IJ (2011) MASP2 haplotypes are associated with high risk of cardiomyopathy in chronic Chagas disease. Clin Immunol 140: 63-70.
23. Weitzel T, Zulantay I, Danquah I, Hamann L, Schumann RR, et al. (2012) Mannose-binding lectin and Toll-like receptor polymorphisms and Chagas disease in Chile. Am J Trop Med Hyg 86: 229-232.
24. Sastry K, Zahedi K, Lelias JM, Whitehead AS, Ezekowitz RA (1991) Molecular characterization of the mouse mannose-binding proteins. The mannose-binding protein A but not C is an acute phase reactant. J Immunol 147: 692-697.
25. Liu H, Jensen L, Hansen S, Petersen SV, Takahashi K, et al. (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.
26. Melo RC, Brener Z (1978) Tissue tropism of different Trypanosoma cruzi strains. J Parasitol 64: 475-482.
27. Federici EE, Abelmann WH, Neva FA (1964) Chronic and Progressive Myocarditis and Myositis in C3h Mice Infected with Trypanosoma cruzi. Am J Trop Med Hyg 13: 272-280.
28. Rocha MO, Ribeiro AL, Teixeira MM (2003) Clinical management of chronic Chagas cardiomyopathy. Front Biosci 8: e44-54.
29. Uemura K, Saka M, Nakagawa T, Kawasaki N, Thiel S, et al. (2002) L-MBP is expressed in epithelial cells of mouse small intestine. J Immunol 169: 6945-6950.
30. Wagner S, Lynch NJ, Walter W, Schwaeble WJ, Loos M (2003) Differential expression of the murine mannose-binding lectins A and C in lymphoid and nonlymphoid organs and tissues. J Immunol 170: 1462-1465.
31. Rodrigues MM, Oliveira AC, Bellio M (2012) The Immune Response to Trypanosoma cruzi: Role of Toll-Like Receptors and Perspectives for Vaccine Development. J Parasitol Res 2012: 507874.
32. Monteiro AC, Schmitz V, Morrot A, de Arruda LB, Nagajyothi F, et al. (2007) Bradykinin B2 Receptors of dendritic cells, acting as sensors of kinins proteolytically released by Trypanosoma cruzi, are critical for the development of protective type-1 responses. PLoS Pathog 3: e185.
33. Teixeira MM, Gazzinelli RT, Silva JS (2002) Chemokines, inflammation and Trypanosoma cruzi infection. Trends Parasitol 18: 262-265.
34. Keller TT, van Leuven SI, Meuwese MC, Wareham NJ, Luben R, et al. (2006) Serum levels of mannose-binding lectin and the risk of future coronary artery disease in apparently healthy men and women. Arterioscler Thromb Vasc Biol 26: 2345-2350.
35. Matthijsen RA, de Winther MP, Kuipers D, van der Made I, Weber C, et al. (2009) Macrophage-specific expression of mannose-binding lectin controls atherosclerosis in low-density lipoprotein receptor-deficient mice. Circulation 119: 2188-2195.
36. Tran CT, Kjeldsen K, Haunso S, Hoiby N, Johansen HK, et al. (2007) Mannanbinding lectin is a determinant of survival in infective endocarditis. Clin Exp Immunol 148: 101-105.
37. Tambourgi DV, Kipnis TL, da Silva WD, Joiner KA, Sher A, et al. (1993) A partial cDNA clone of trypomastigote decay-accelerating factor (T-DAF), a developmentally regulated complement inhibitor of Trypanosoma cruzi, has genetic and functional similarities to the human complement inhibitor DAF. Infect Immun 61: 3656-3663.
38. Cestari Idos S, Evans-Osses I, Freitas JC, Inal JM, Ramirez MI (2008) Complement C2 receptor inhibitor trispanning confers an increased ability to resist complement-mediated lysis in Trypanosoma cruzi. J Infect Dis 198: 1276-1283.
39. Matsushita M (2010) Ficolins: complement-activating lectins involved in innate immunity. J Innate Immun 2: 24-32.
40. Kahn SJ, Wleklinski M, Ezekowitz RA, Coder D, Aruffo A, et al. (1996) The major surface glycoprotein of Trypanosoma cruzi amastigotes are ligands of the human serum mannose-binding protein. Infect Immun 64: 2649-2656.
41. Green PJ, Feizi T, Stoll MS, Thiel S, Prescott A, et al. (1994) Recognition of the major cell surface glycoconjugates of Leishmania parasites by the human serum mannan-binding protein. Mol Biochem Parasitol 66: 319-328.
42. Nogueira N, Cohn Z (1976) Trypanosoma cruzi: mechanism of entry and intracellular fate in mammalian cells. J Exp Med 143: 1402-1420.
43. Hudson L, Snary D, Morgan SJ (1984) Trypanosoma cruzi: continuous cultivation with murine cell lines. Parasitology 88 (Pt 2): 283-294.
44. Ley V, Andrews NW, Robbins ES, Nussenzweig V (1988) Amastigotes of Trypanosoma cruzi sustain an infective cycle in mammalian cells. J Exp Med 168: 649-659.
45. Scharfstein J, Morrot A (1999) A role for extracellular amastigotes in the immunopathology of Chagas disease. Mem Inst Oswaldo Cruz 94 Suppl 1: 51-63.
46. Schwaeble WJ, Lynch NJ, Clark JE, Marber M, Samani NJ, et al. (2012) Targeting of mannan-binding lectin-associated serine protease-2 confers protection from myocardial and gastrointestinal ischemia/reperfusion injury. Proc Natl Acad Sci U S A 108: 7523-7528.
47. Alonso DP, Ferreira AF, Ribolla PE, de Miranda Santos IK, do Socorro Pires e Cruz M, et al. (2007) Genotypes of the mannan-binding lectin gene and susceptibility to visceral leishmaniasis and clinical complications. J Infect Dis 195: 1212-1217.
48. Assaf A, Hoang TV, Faik I, Aebischer T, Kremsner PG, et al. (2012) Genetic evidence of functional ficolin-2 haplotype as susceptibility factor in cutaneous leishmaniasis. PLoS One 7: e34113.
49. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, et al. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18- mediated function. Immunity 9: 143-150.
50. Amato Neto V, Campos R, Higaki Y (1974) [Clinical analysis based on subsidiary tests of a patient from which was isolated, 23 years ago, the Y strain of Trypanosoma cruzi]. Rev Inst Med Trop Sao Paulo 16: 238-234.
51. Brener Z (1962) Therapeutic activity and criterion of cure on mice experimentally infected with Trypanosoma cruzi. Rev Inst Med Trop Sao Paulo 4: 389-396.
52. Scharton-Kersten TM, Wynn TA, Denkers EY, Bala S, Grunvald E, et al. (1996) In the absence of endogenous IFN-c, mice develop unimpaired IL-12 responses to Toxoplasma gondii while failing to control acute infection. J Immunol 157: 4045-4054.
53. Cummings KL, Tarleton RL (2003) Rapid quantitation of Trypanosoma cruzi in host tissue by real-time PCR. Mol Biochem Parasitol 129: 53-59.
54. Bergman I, Loxley R (1970) New spectrophotometric method for the determination of proline in tissue hydrolyzates. Anal Chem 42: 702-706.