Trypanosoma cruzi infection induces a global host cell response in Cardiomyocytes

Infection and Immunity

Volumn 79, Issue 5, 2011, Pages 1855-1862

  Manque, Patricio A ^a,d   Probst, Christian ^c   Pereira, Mirian C S ^b   Rampazzo, Rita C P ^b,c   Ozaki, L Shozo ^a   Pavoni, Daniela P ^c   Neto, Dayse T Silva ^b   Carvalho, M Ruth ^a   Xu, Ping ^a   Serrano, Myrna G ^a   Alves, João M P ^a   Meirelles, Maria de Nazareth S L ^b   Goldenberg, Samuel ^c   Krieger, Marco A ^c   Buck, Gregory A ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c Instituto Carlos Chagas   (Brazil)

^d UNIVERSIDAD MAYOR   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS; ARTICLE; CELL CYCLE; CELL INTERACTION; CELL INVASION; CHAGAS DISEASE; CYTOSKELETON; GENE IDENTIFICATION; HEART MUSCLE CELL; HOST CELL; IMMUNE RESPONSE; IMMUNOMODULATION; INFLAMMATION; MICROARRAY ANALYSIS; NONHUMAN; OUTCOME ASSESSMENT; OXIDATIVE STRESS; PARASITE SURVIVAL; PRIORITY JOURNAL; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE;

ANIMALS; CHAGAS CARDIOMYOPATHY; GENE EXPRESSION; GENE EXPRESSION PROFILING; HOST-PARASITE INTERACTIONS; IN SITU HYBRIDIZATION; MICE; MICROARRAY ANALYSIS; MYOCYTES, CARDIAC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRYPANOSOMA CRUZI;

EID: 79955611821     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00643-10     Document Type: Article

References (61)

1. Adesse, D., et al. 2008. Trypanosoma cruzi induces changes in cardiac connexin43 expression. Microbes Infect. 10:21-28.
2. Andrade, S. G., J. A. Grimaud, and S. Stocker-Guerret. 1989. Sequential changes of the connective matrix components of the myocardium (fibronectin and laminin) and evolution of cardiac fibrosis in mice infected with Trypanosoma cruzi. Am. J. Trop. Med. Hyg. 40:252-260.
3. Barbosa, H. S., and M. N. Meirelles. 1993. The role of RCA-binding sites in the adhesion of Trypanosoma cruzi to heart muscle cells, as revealed by electron spectroscopic imaging. J. Submicrosc. Cytol. Pathol. 25:47-51.
4. Barbosa, H. S., and M. N. Meirelles. 1992. Ultrastructural detection in vitro of WGA-, RCA I-, and ConA-binding sites involved in the invasion of heart muscle cells by Trypanosoma cruzi. Parasitol. Res. 78:404-409.
5. Benarafa, C., G. P. Priebe, and E. Remold-O'Donnell. 2007. The neutrophil serine protease inhibitor serpinb1 preserves lung defense functions in Pseudomonas aeruginosa infection. J. Exp. Med. 204:1901-1909.
6. Burleigh, B. A., and A. M. Woolsey. 2002. Cell signalling and Trypanosoma cruzi invasion. Cell. Microbiol. 4:701-711.
7. Calvet, C. M., L. Toma, F. R. De Souza, M. N. Meirelles, and M. C. Pereira. 2003. Heparan sulfate proteoglycans mediate the invasion of cardiomyocytes by Trypanosoma cruzi. J. Eukaryot. Microbiol. 50:97-103.
8. Calvet, C. M., M. Meuser, D. Almeida, M. N. Meirelles, and M. C. Pereira. 2004. Trypanosoma cruzicardiomyocyte interaction: role of fibronectin in the recognition process and extracellular matrix expression in vitro and in vivo. Exp. Parasitol. 107:20-30.
9. Carmen, J. C., and A. P. Sinai. 2007. Suicide prevention: disruption of apoptotic pathways by protozoan parasites. Mol. Microbiol. 64:904-916.
10. Chuenkova, M. V., and M. P. Perrin. 2008. Trypanosoma cruzi targets AKt in host cells as an intracellular antiapoptotic strategy. Sci. Signal 17:97ra74.
11. D'Cunha, J., E. Knight, Jr., A. L. Haas, R. L. Truitt, and E. C. Borden. 1996. Immunoregulatory properties of ISG15, an interferon-induced cytokine. Proc. Natl. Acad. Sci. U. S. A. 93:211-215.
12. de Souza, E. M., et al. 2003. Host and parasite apoptosis following Trypanosoma cruzi infection in in vitro and in vivo models. Cell Tissue Res. 314:223-235.
13. Dias, W. B., et al. 2008. Endothelial cell signalling induced by trans-sialidase from Trypanosoma cruzi. Cell. Microbiol. 10:88-99.
14. Fernandes, O., et al. 1999. Populational heterogeneity of Brazilian Trypano-soma cruzi isolates revealed by the mini-exon and ribosomal spacers. Mem. Inst. Oswaldo Cruz 94(Suppl. 1):195-197.
15. Ferreira, D., M. Cortez, V. D. Atayde, and N. Yoshida. 2006. Actin cytoskeleton-dependent and -independent host cell invasion by Trypanosoma cruzi is mediated by distinct parasite surface molecules. Infect. Immun. 74:5522-5528.
16. Garg, N., V. L. Popov, and J. Papaconstantinou. 2003. Profiling gene transcription reveals a deficiency of mitochondrial oxidative phosphorylation in Trypanosoma cruzi-infected murine hearts: implications in chagasic myocarditis development. Biochim. Biophys. Acta 1638:106-120.
17. Gautier, L., L. Cope, B. M. Bolstad, and R. A. Irizarry. 2004. affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20:307-315.
18. Gentleman, R. C., et al. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5:R80.
19. Gitlin, L., et al. 2006. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavi-rus. Proc. Natl. Acad. Sci. U. S. A. 103:8459-8464.
20. Goldenberg, R. C., et al. 2009. Transcriptomic alterations in Trypanosoma cruzi-infected cardiac myocytes. Microbes Infect. 11:1140-1149.
21. Gruenheid, S., and B. B. Finlay. 2003. Microbial pathogenesis and cytoskeletal function. Nature 422:775-781.
22. Gupta, S., J. J. Wen, and N. J. Garg. 2009. Oxidative stress in Chagas disease. Interdiscip. Perspect. Infect. Dis. 2009:190354.
23. Hamilton, N. H., S. Mahalingam, J. L. Banyer, I. A. Ramshaw, and S. A. Thomson. 2004. A recombinant vaccinia virus encoding the interferon-in-ducible T-cell alpha chemoattractant is attenuated in vivo. Scand. J. Immunol. 59:246-254.
24. Higuchi, M. L., L. A. Benvenuti, M. Martins Reis, and M. Metzger. 2003. Pathophysiology of the heart in Chagas' disease: current status and new developments. Cardiovasc. Res. 60:96-107.
25. Hossain, G. S., et al. 2003. TDAG51 is induced by homocysteine, promotes detachment-mediated programmed cell death, and contributes to the development of atherosclerosis in hyperhomocysteinemia. J. Biol. Chem. 278: 30317-30327.
26. Imai, K., T. Mimori, M. Kawai, and H. Koga. 2005. Microarray analysis of host gene-expression during intracellular nests formation of Trypanosoma cruzi amastigotes. Microbiol. Immunol. 49:623-631.
27. Irizarry, R. A., et al. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249-264.
28. John, G. B., et al. 2005. The mitochondrial inner membrane protein mitofilin controls cristae morphology. Mol. Biol. Cell 16:1543-1554.
29. Kang, D. C., et al. 2004. Expression analysis and genomic characterization of human melanoma differentiation associated gene-5, mda-5: a novel type I interferon-responsive apoptosis-inducing gene. Oncogene 23:1789-1800.
30. Kohfeldt, E., T. Sasaki, W. Gohring, and R. Timpl. 1998. Nidogen-2: a new basement membrane protein with diverse binding properties. J. Mol. Biol. 282:99-109.
31. Langer, H. F., and T. Chavakis. 2009. Leukocyte-endothelial interactions in inflammation. J. Cell. Mol. Med. 13:1211-1220.
32. Liebermann, D. A., and B. Hoffman. 2007. Gadd45 in the response of he-matopoietic cells to genotoxic stress. Blood Cells Mol. Dis. 39:329-335.
33. Machado, F. S., et al. 2000. Trypanosoma cruzi-infected cardiomyocytes produce chemokines and cytokines that trigger potent nitric oxide-dependent trypanocidal activity. Circulation 102:3003-3008.
34. Malakhova, O. A., et al. 2003. Protein ISGylation modulates the JAK-STAT signaling pathway. Genes Dev. 17:455-460.
35. Malakhova, O., M. Malakhov, C. Hetherington, and D. E. Zhang. 2002. Lipopolysaccharide activates the expression of ISG15-specific protease UBP43 via interferon regulatory factor 3. J. Biol. Chem. 277:14703-14711.
36. Meirelles, M. N., T. C. de Araujo-Jorge, C. F. Miranda, W. de Souza, and H. S. Barbosa. 1986. Interaction of Trypanosoma cruzi with heart muscle cells: ultrastructural and cytochemical analysis of endocytic vacuole formation and effect upon myogenesis in vitro. Eur. J. Cell Biol. 41:198-206.
37. Melo, T. G., D. S. Almeida, M. N. Meirelles, and M. C. Pereira. 2006. Disarray of sarcomeric alpha-actinin in cardiomyocytes infected by Trypano-soma cruzi. Parasitology 133:171-178.
38. Melo, T. G., D. S. Almeida, M. N. Meirelles, and M. C. Pereira. 2004. Trypanosoma cruzi infection disrupts vinculin costameres in cardiomyocytes. Eur. J. Cell Biol. 83:531-540.
39. Melo, T. G., M. N. Meirelles, and M. C. Pereira. 2008. Trypanosoma cruzi alters adherens junctions in cardiomyocytes. Microbes Infect. 10:1405-1410.
40. Melo-Jorge, M., and M. P. Perrin. 2007. The Chagas' disease parasite Trypanosoma cruzi exploits nerve growth factor receptor Trka to infect mammalian hosts. Cell Host Microbe 1:251-261.
41. Michailowsky, V., et al. 2004. Intercellular adhesion molecule 1 deficiency leads to impaired recruitment of T lymphocytes and enhanced host susceptibility to infection with Trypanosoma cruzi. J. Immunol. 173:463-470.
42. Mondino, A., and F. Blasi. 2004. uPA and uPAR in fibrinolysis, immunity and pathology. Trends Immunol. 25:450-455.
43. Mott, A., G. Lenormand, J. Costales, J. J. Fredberg, and B. A. Burleigh. 2009. Modulation of host cell mechanics by Trypanosoma cruzi. J. Cell. Physiol. 218:315-322.
44. Mukherjee, S., et al. 2003. Microarray analysis of changes in gene expression in a murine model of chronic chagasic cardiomyopathy. Parasitol. Res. 91: 187-196.
45. Oliveira, F. O., Jr., et al. 2008. Trypanosoma cruzi heparin-binding proteins and the nature of the host cell heparan sulfate-binding domain. Microb. Pathog. 44:329-338.
46. Pereira, M. C., M. Costa, C. Chagas Filho, and M. N. Meirelles. 1993. Myofibrillar breakdown and cytoskeletal alterations in heart muscle cells during invasion by Trypanosoma cruzi: immunological and ultrastructural study. J. Submicrosc. Cytol. Pathol. 25:559-569.
47. Petersen, C. A., and B. A. Burleigh. 2003. Role for interleukin-1 beta in Trypanosoma cruzi-induced cardiomyocyte hypertrophy. Infect. Immun. 71: 4441-4447.
48. Petersen, C. A., K. A. Krumholz, J. Carmen, A. P. Sinai, and B. A. Burleigh. 2006. Trypanosoma cruzi infection and nuclear factor kappa B activation prevent apoptosis in cardiac cells. Infect. Immun. 74:1580-1587.
49. Raychaudhuri, S. K., S. P. Raychaudhuri, H. Weltman, and E. M. Farber. 2001. Effect of nerve growth factor on endothelial cell biology: proliferation and adherence molecule expression on human dermal microvascular endo-thelial cells. Arch. Dermatol. Res. 293:291-295.
50. Shigihara, T., M. Hashimoto, N. Shindo, and T. Aoki. 2008. Transcriptome profile of Trypanosoma cruzi-infected cells: simultaneous up- and down-regulation of proliferation inhibitors and promoters. Parasitol. Res. 102:715-722.
51. Silva, D. T., M. N. S. L. Meirelles, D. Almeida, J. A. Urbina, and M. C. Pereira. 2006. Cytoskeleton reassembly in cardiomyocytes infected by Trypanosoma cruzi is triggered by treatment with ergosterol biosynthesis inhibitors. Int. J. Antimicrob. Agents 27:530-537.
52. Staub, O. 2004. Ubiquitylation and isgylation: overlapping enzymatic cascades do the job. Sci. STKE 2004:pe43.
53. Talvani, A., et al. 2000. Kinetics of cytokine gene expression in experimental chagasic cardiomyopathy: tissue parasitism and endogenous IFN-gamma as important determinants of chemokine mRNA expression during infection with Trypanosoma cruzi. Microbes Infect. 2:851-866.
54. Tanowitz, H. B., et al. 2009. Perspectives on Trypanosoma cruzi-induced heart disease (Chagas disease). Prog. Cardiovasc. Dis. 51:524-539.
55. Tusher, V. G., R. Tibshirani, and G. Chu. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U. S. A. 98:5116-5121.
56. Vaena de Avalos, S., I. J. Blader, M. Fisher, J. C. Boothroyd, and B. A. Burleigh. 2002. Immediate/early response to Trypanosoma cruzi infection involves minimal modulation of host cell transcription. J. Biol. Chem. 277: 639-644.
57. Vikstrom, K. L., T. Bohlmeyer, S. M. Factor, and L. A. Leinwand. 1998. Hypertrophy, pathology, and molecular markers of cardiac pathogenesis. Circ. Res. 82:773-778.
58. WHO. 2002. The world health report, 2002. WHO, Geneva, Switzerland.
59. Williams, A. S., et al. 2009. Role of cathepsin S in ozone-induced airway hyperresponsiveness and inflammation. Pulm. Pharmacol. Ther. 22:27-32.
60. Woessner, J. F., Jr. 2002. MMPs and TIMPs-an historical perspective. Mol. Biotechnol. 22:33-49.
61. Zhan, Q., et al. 1999. Association with Cdc2 and inhibition of Cdc2/Cyclin B1 kinase activity by the p53-regulated protein Gadd45. Oncogene 18:2892-2900.