DTU i isolates of Trypanosoma cruzi induce upregulation of Galectin-3 in murine myocarditis and fibrosis

Parasitology

Volumn 141, Issue 6, 2014, Pages 849-858

  Ferrer, María F ^a   Pascuale, Carla A ^b,c   Gomez, Ricardo M ^a   Leguizamón, María S ^b,c  

^a UNIVERSIDAD NACIONAL DE LA PLATA   (Argentina)

^b Universidad de Buenos Aires   (Argentina)

^c INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

Author keywords

Chagas disease; DTU; fibrosis; galectin 3; smooth muscle actin

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; GALECTIN 3; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; COLLAGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIUM ISOLATE; CARDIOMYOPATHY; CELL INFILTRATION; CONTROLLED STUDY; DISCRETE TYPING UNIT; DISEASE SEVERITY; EXTRACELLULAR MATRIX; GENOTYPE; HEART DISEASE; HEART INJURY; HEART MUSCLE FIBROSIS; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; MALE; MONONUCLEAR CELL; MORTALITY; MOUSE; MYOCARDITIS; NONHUMAN; PARASITE LOAD; PARASITEMIA; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; TRYPANOSOMA CRUZI; UPREGULATION; BACTERIUM ISOLATION; CHAGAS DISEASE; DISCRETE TYPING UNIT I; HEART FAILURE; PATHOGENESIS; QUANTITATIVE ANALYSIS; ANIMAL; DISEASE MODEL; FIBROSIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY;

MURINAE; TRYPANOSOMA CRUZI;

ANIMALS; CHAGAS CARDIOMYOPATHY; COLLAGEN; DISEASE MODELS, ANIMAL; FIBROSIS; GALECTIN 3; GENE EXPRESSION REGULATION; GENOTYPE; HUMANS; MALE; MICE; MYOCARDITIS; PARASITE LOAD; TRYPANOSOMA CRUZI; UP-REGULATION;

EID: 84898538880     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182013002254     Document Type: Article

References (68)

1. Acosta-Rodriguez, E. V., Montes, C.L., Motran, C. C., Zuniga, E. I., Liu, F.T., Rabinovich, G.A. and Gruppi, A. (2004). Galectin-3 mediates IL-4-induced survival and differentiation of B cells: functional cross-talk and implications during Trypanosoma cruzi infection. Journal of Immunology 172, 493-502. doi: 10.1007/s00430-011-0192-3.
2. Andrade, S. G. and Grimaud, J. A. (1986). Chronic murine myocarditis due to Trypanosoma cruzi-an ultrastructural study and immunochemical characterization of cardiac interstitial matrix. Memórias do Instituto Oswaldo Cruz 81, 29-41. doi: 10.1590/S0074-02761986000100004.
3. Araujo-Jorge, T. C., Waghabi, M. C., Bailly, S. and Feige, J. J. (2012). The TGF-beta pathway as an emerging target for Chagas disease therapy. Clinical Pharmacology and Therapeutics 92, 613-621. doi: 10.1038/clpt2012102 [pii].
4. Bahia-Oliveira, L. M., Gomes, J. A., Rocha, M. O., Moreira, M. C., Lemos, E. M., Luz, Z. M., Pereira, M. E., Coffman, R. L., Dias, J. C., Cancado, J. R., Gazzinelli, G. and Correa-Oliveira, R. (1998). IFN-gamma in human Chagas' disease: protection or pathology? Brazilian Journal of Medical and Biological Research 31, 127-131. doi: 10.1590/S0100-879X1998000100017.
5. Bonney, K. M. and Engman, D. M. (2008). Chagas heart disease pathogenesis: one mechanism or many? Current Molecular Medicine 8, 510-518. doi: 10.2174/156652408785748004.
6. Brandariz, S., Schijman, A., Vigliano, C., Arteman, P., Viotti, R., Beldjord, C. and Levin, M. J. (1995). Detection of parasite DNA in Chagas' heart disease. Lancet 346, 1370-1371. doi: 10.1016/S0140-6736(95) 92388-8.
7. Burgos, J.M., Diez, M., Vigliano, C., Bisio, M., Risso, M., Duffy, T., Cura, C., Brusses, B., Favaloro, L., Leguizamon, M.S., Lucero, R.H., Laguens, R., Levin, M. J., Favaloro, R. and Schijman, A. G. (2010). Molecular identification of Trypanosoma cruzi discrete typing units in end-stage chronic Chagas heart disease and reactivation after heart transplantation. Clinical Infectious Disease 51, 485-495. doi: 10.1086/655680.
8. Burgos, J.M., Risso, M.G., Breniere, S.F., Barnabe, C., Campetella, O. and Leguizamon, M. S. (2013). Differential distribution of genes encoding the virulence factor trans-sialidase along Trypanosoma cruzi discrete typing units. PLoS ONE 8, e58967. doi: 10.1371/journal. pone.0058967 PONE-D-12-38981 [pii].
9. Cain, B.S., Meldrum, D.R., Dinarello, C. A., Meng, X., Joo, K. S., Banerjee, A. and Harken, A. H. (1999). Tumor necrosis factor-alpha and interleukin-1beta synergistically depress human myocardial function. Critical Care Medicine 27, 1309-1318. doi: 10.1097/00003246-199907000-00018.
10. Calvet, C. M., Melo, T. G., Garzoni, L. R., Oliveira, F. O., Neto, D. T., N. S. L.M., Meirelles, L. and Pereira, M. C. (2012). Current understanding of the Trypanosoma cruzi-cardiomyocyte interaction. Frontiers in Immunology 3, 327. doi: 10.3389/fimmu.2012.00327.
11. Campbell, D. A., Westenberger, S. J. and Sturm, N. R. (2004). The determinants of Chagas disease: connecting parasite and host genetics. Current Molecular Medicine 4, 549-562. doi: 10.2174/1566524043360249.
12. Carranza, J. C., Valadares, H. M., D'Avila, D. A., Baptista, R. P., Moreno, M., Galvao, L. M., Chiari, E., Sturm, N. R., Gontijo, E. D., Macedo, A.M. and Zingales, B. (2009). Trypanosoma cruzi maxicircle heterogeneity in Chagas disease patients from Brazil. International Journal for Parasitology 39, 963-973. doi: S0020-7519(09)00095-2 [pii] 10.1016/j. ijpara.2009.01.009.
13. Cunha-Neto, E., Rizzo, L.V., Albuquerque, F., Abel, L., Guilherme, L., Bocchi, E., Bacal, F., Carrara, D., Ianni, B., Mady, C. and Kalil, J. (1998). Cytokine production profile of heart-infiltrating T cells in Chagas' disease cardiomyopathy. Brazilian Journal of Medical and Biological Research 31, 133-137. doi: 10.1590/S0100-879X1998000100018.
14. Cunha-Neto, E., Dzau, V. J., Allen, P. D., Stamatiou, D., Benvenutti, L., Higuchi, M. L., Koyama, N. S., Silva, J. S., Kalil, J. and Liew, C. C. (2005). Cardiac gene expression profiling provides evidence for cytokinopathy as a molecular mechanism in Chagas' disease cardiomyopathy. American Journal of Pathology 167, 305-313. doi: S0002-9440(10)62976-8 [pii]10.1016/S0002-9440(10) 62976-8.
15. de Boer, R.A., Yu, L. and van Veldhuisen, D. J. (2010). Galectin-3 in cardiac remodeling and heart failure. Current Heart Failure Reports 7, 1-8. doi: 10.1007/s11897-010-0004-x.
16. Desmouliere, A., Redard, M., Darby, I. and Gabbiani, G. (1995). Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar. American Journal of Pathology 146, 56-66. doi: PMC1870783.
17. Di Noia, J.M., Buscaglia, C. A., De Marchi, C.R., Almeida, I. C. and Frasch, A. C. (2002). A Trypanosoma cruzi small surface molecule provides the first immunological evidence that Chagas' disease is due to a single parasite lineage. Journal of Experimental Medicine 195, 401-413. doi: 10.1084/jem.20011433.
18. Dutra, W. O., Menezes, C. A., Villani, F. N., da Costa, G. C., da Silveira, A. B., Reis, D. and Gollob, K.J. (2009). Cellular and genetic mechanisms involved in the generation of protective and pathogenic immune responses in human Chagas disease. Memórias do Instituto Oswaldo Cruz 104 (Suppl. 1), 208-218. doi: S0074-02762009000900027[pii].
19. Feldman, A. M. and McNamara, D. (2000). Myocarditis. New England Journal of Medicine 343, 1388-1398. doi: 10.1056/NEJM200011093431908.
20. Feliciangeli, M. D., Dujardin, J. P., Bastrenta, B., Mazzarri, M., Villegas, J., Flores, M. and Munoz, M. (2002). Is Rhodnius robustus (Hemiptera: Reduviidae) responsible for Chagas disease transmission in Western Venezuela? Tropical Medicine and International Health 7, 280-287. doi: 853 [pii].
21. Frangogiannis, N. G. (2006). Targeting the inflammatory response in healing myocardial infarcts. Current Medicinal Chemistry 13, 1877-1893. doi: 10.2174/092986706777585086.
22. Frangogiannis, N. G. (2008). The immune system and cardiac repair. Pharmacology Research 58, 88-111. doi: 10.1016/j.phrs.2008.06.007 S1043-6618(08)00108-4 [pii].
23. Freitas, J. M., Lages-Silva, E., Crema, E., Pena, S. D. and Macedo, A. M. (2005). Real time PCR strategy for the identification of major lineages of Trypanosoma cruzi directly in chronically infected human tissues. International Journal of Parasitology 35, 411-417. doi: S0020-7519 (04)00260-7 [pii] 10.1016/j.ijpara.2004.10.023.
24. Gomez, R. M., Castagnino, C. G. and Berria, M. I. (1992). Extracellular matrix remodelling after coxsackievirus B3-induced murine myocarditis. International Journal of Experimental Pathology 73, 643-653. doi: PMC2002023.
25. Gomez, R. M., Vieira, M. L., Schattner, M., Malaver, E., Watanabe, M. M., Barbosa, A. S., Abreu, P. A., de Morais, Z. M., Cifuente, J. O., Atzingen, M. V., Oliveira, T. R., Vasconcellos, S.A. and Nascimento, A. L. (2008). Putative outer membrane proteins of Leptospira interrogans stimulate human umbilical vein endothelial cells (HUVECS) and express during infection. Microbial Pathogenesis 45, 315-322. doi: S0882-4010(08)00107-1 [pii] 10.1016/j.micpath.2008.08.004.
26. Guhl, F. and Ramirez, J. D. (2011). Trypanosoma cruzi I diversity: towards the need of genetic subdivision? Acta Tropica 119, 1-4. doi: 10.1016/j.actatropica.2011.04.002 S0001-706X(11)00072-6 [pii].
27. Gurtner, G.C., Werner, S., Barrandon, Y. and Longaker, M. T. (2008). Wound repair and regeneration. Nature 453, 314-321. doi: 10.1038/nature07039 nature07039 [pii].
28. Hardison, J. L., Wrightsman, R. A., Carpenter, P.M., Lane, T.E. and Manning, J. E. (2006). The chemokines CXCL9 and CXCL10 promote a protective immune response but do not contribute to cardiac inflammation following infection with Trypanosoma cruzi. Infection and Immunity 74, 125-134. doi: 74/1/125 [pii] 10.1128/IAI.74.1.125-134.2006.
29. Haudek, S. B., Taffet, G. E., Schneider, M. D. and Mann, D. L. (2007). TNF provokes cardiomyocyte apoptosis and cardiac remodeling through activation of multiple cell death pathways. Journal of Clinical Investigation 117, 2692-2701. doi: 10.1172/JCI29134.
30. Henderson, N.C., Mackinnon, A. C., Farnworth, S. L., Poirier, F., Russo, F. P., Iredale, J. P., Haslett, C., Simpson, K. J. and Sethi, T. (2006). Galectin-3 regulates myofibroblast activation and hepatic fibrosis. Proceedings of the National Academy of Sciences USA 103, 5060-5065. doi: 0511167103 [pii] 10.1073/pnas.0511167103.
31. Henderson, N. C., Mackinnon, A. C., Farnworth, S. L., Kipari, T., Haslett, C., Iredale, J. P., Liu, F.T., Hughes, J. and Sethi, T. (2008). Galectin-3 expression and secretion links macrophages to the promotion of renal fibrosis. American Journal of Pathology 172, 288-298. doi: 10.2353/ajpath.2008. 070726 S0002-9440(10)61796-8 [pii].
32. Jaquenod De Giusti, C., Alberdi, L., Frik, J., Ferrer, M. F., Scharrig, E., Schattner, M. and Gomez, R. M. (2011). Galectin-3 is upregulated in activated glia during Junin virus-induced murine encephalitis. Neuroscience Letters 501, 163-166. doi: 10.1016/j.neulet.2011.07.007 S0304-3940(11)01040-8 [pii].
33. Junqueira, L. C., Bignolas, G. and Brentani, R. R. (1979). Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochemistry Journal 11, 447-455. doi: 10.1007/BF01002772.
34. Kaviratne, M., Hesse, M., Leusink, M., Cheever, A. W., Davies, S. J., McKerrow, J. H., Wakefield, L.M., Letterio, J. J. and Wynn, T.A. (2004). IL-13 activates a mechanism of tissue fibrosis that is completely TGF-beta independent. Journal of Immunology 173, 4020-4029. doi: 173/6/4020 [pii].
35. Kleshchenko, Y.Y., Moody, T. N., Furtak, V. A., Ochieng, J., Lima, M. F. and Villalta, F. (2004). Human galectin-3 promotes Trypanosoma cruzi adhesion to human coronary artery smooth muscle cells. Infection and Immunity 72, 6717-6721.
36. Kubota, T., McTiernan, C. F., Frye, C. S., Slawson, S.E., Lemster, B.H., Koretsky, A. P., Demetris, A. J. and Feldman, A.M. (1997). Dilated cardiomyopathy in transgenic mice with cardiac-specific overexpression of tumor necrosis factor-alpha. Circulation Research 81, 627-635. doi: 10.1161/01.RES.81.4.627.
37. Lee, C.G., Homer, R.J., Zhu, Z., Lanone, S., Wang, X., Koteliansky, V., Shipley, J. M., Gotwals, P., Noble, P., Chen, Q., Senior, R.M. and Elias, J. A. (2001). Interleukin-13 induces tissue fibrosis by selectively stimulating and activating transforming growth factor beta(1). Journal ofExperimentalMedicine 194, 809-821. doi: 10.1084/jem.194.6.809.
38. Liu, F. T. and Rabinovich, G. A. (2010). Galectins: regulators of acute and chronic inflammation. Annals of the New York Academy of Sciences 1183, 158-182. doi: 10.1111/j.1749-6632.2009.05131.x.
39. Lok, D. J., Van Der Meer, P., de la Porte, P. W., Lipsic, E., Van Wijngaarden, J., Hillege, H. L. and van Veldhuisen, D. J. (2010). Prognostic value of galectin-3, a novel marker of fibrosis, in patients with chronic heart failure: data from the DEAL-HF study. Clinical Research in Cardiology 99, 323-328. doi: 10.1007/s00392-010-0125-y.
40. Macedo, A. M., Machado, C. R., Oliveira, R. P. and Pena, S. D. (2004). Trypanosoma cruzi: genetic structure of populations and relevance of genetic variability to the pathogenesis of Chagas disease. Memórias do Instituto Oswaldo Cruz 99, 1-12. doi: S0074-02762004000100001 [pii].
41. Machado, F. S., Dutra, W. O., Esper, L., Gollob, K. J., Teixeira, M. M., Factor, S. M., Weiss, L.M., Nagajyothi, F., Tanowitz, H. B. and Garg, N.J. (2012). Current understanding of immunity to Trypanosoma cruzi infection and pathogenesis of Chagas disease. Seminars in Immuno-pathology 34, 753-770. doi: 10.1007/s00281-012-0351-7.
42. Marin-Neto, J. A., Cunha-Neto, E., Maciel, B. C. and Simoes, M. V. (2007). Pathogenesis of chronic Chagas heart disease. Circulation 115, 1109-1123. doi: 115/9/1109 [pii] 10.1161/CIRCULATIONAHA.106. 624296.
43. Miles, M. A., Feliciangeli, M. D. and de Arias, A. R. (2003). American trypanosomiasis (Chagas' disease) and the role of molecular epidemiology in guiding control strategies. British Medical Journal 326, 1444-1448. doi: 10.1136/bmj.326.7404.1444 326/7404/1444 [pii].
44. Moody, T. N., Ochieng, J. and Villalta, F. (2000). Novel mechanism that Trypanosoma cruzi uses to adhere to the extracellular matrix mediated by human galectin-3. FEBS Letters 470, 305-308.
45. PAHO (2007). Health conditions and trends. In Health in the Americas, Vol. 1, pp. 58-207. Pan American Health Organization, Washington, DC, USA.
46. Paiva, C. N., Figueiredo, R. T., Kroll-Palhares, K., Silva, A. A., Silverio, J. C., Gibaldi, D., Pyrrho Ados, S., Benjamim, C. F., Lannes-Vieira, J. and Bozza, M. T. (2009). CCL2/MCP-1 controls parasite burden, cell infiltration, and mononuclear activation during acute Trypanosoma cruzi infection. Journal of Leukocyte Biology 86, 1239-1246. doi: 10.1189/jlb.0309187 jlb.0309187 [pii].
47. Pilling, D., Fan, T., Huang, D., Kaul, B. and Gomer, R. H. (2009). Identification of markers that distinguish monocyte-derived fibrocytes from monocytes, macrophages, and fibroblasts. PLoS ONE 4, e7475. doi: 10.1371/journal.pone.0007475.
48. Ramirez, J.D., Guhl, F., Rendon, L. M., Rosas, F., Marin-Neto, J. A. and Morillo, C. A. (2010). Chagas cardiomyopathy manifestations and Trypanosoma cruzi genotypes circulating in chronic Chagasic patients. PLoS Neglected Tropical Diseases 4, e899. doi: 10.1371/journal.pntd. 0000899.
49. Rassi, A., Jr., Rassi, A. and Marin-Neto, J. A. (2010). Chagas disease. Lancet 375, 1388-1402. doi: S0140-6736(10)60061-X [pii] 10.1016/S0140-6736(10) 60061-X.
50. Risso, M.G., Garbarino, G. B., Mocetti, E., Campetella, O., Gonzalez Cappa, S.M., Buscaglia, C. A. and Leguizamon, M. S. (2004). Differential expression of a virulence factor, the trans-sialidase, by the main Trypanosoma cruzi phylogenetic lineages. Journal of Infectious Disease 189, 2250-2259. doi: 10.1086/420831 JID31720 [pii].
51. Rocha Rodrigues, D. B., dos Reis, M. A., Romano, A., Pereira, S. A., Teixeira Vde, P., Tostes, S., Jr. and Rodrigues, V., Jr. (2012). In situ expression of regulatory cytokines by heart inflammatory cells in Chagas' disease patients with heart failure. Clinical and Developmental Immunology 2012, 361730. doi: 10.1155/2012/361730.
52. Roffe, E., Rothfuchs, A.G., Santiago, H. C., Marino, A. P., Ribeiro-Gomes, F.L., Eckhaus, M., Antonelli, L. R. and Murphy, P. M. (2012). IL-10 limits parasite burden and protects against fatal myocarditis in a mouse model of Trypanosoma cruzi infection. Journal of Immunology 188, 649-660. doi: 10.4049/jimmunol.1003845 jimmunol.1003845 [pii].
53. Sato, S. and Hughes, R. C. (1994). Regulation of secretion and surface expression of Mac-2, a galactoside-binding protein of macrophages. Journal of Biological Chemistry 269, 4424-4430. doi: 10.2353/ajpath.2008. 070726.
54. Shi, Q., Liu, X., Bai, Y., Cui, C., Li, J., Li, Y., Hu, S. and Wei, Y. (2011). In vitro effects of pirfenidone on cardiac fibroblasts: proliferation, myofibroblast differentiation, migration and cytokine secretion. PLoS ONE 6, e28134. doi: 10.1371/journal.pone.0028134 PONE-D-11-15265 [pii].
55. Soares, M. B., de Lima, R.S., Rocha, L. L., Vasconcelos, J. F., Rogatto, S. R., dos Santos, R. R., Iacobas, S., Goldenberg, R. C., Iacobas, D. A., Tanowitz, H. B., de Carvalho, A.C. and Spray, D. C. (2010). Gene expression changes associated with myocarditis and fibrosis in hearts of mice with chronic chagasic cardiomyopathy. Journal of Infectious Disease 202, 416-426. doi: 10.1086/653481.
56. Solana, M.E., Ferrer, M. F., Novoa, M. M., Song, W. C. and Gomez, R. M. (2012). Decay-accelerating factor 1 deficiency exacerbates Trypanosoma cruzi-induced murine chronic myositis. Muscle and Nerve 46, 582-587. doi: 10.1002/mus.23347.
57. Sun, Y. and Weber, K. T. (2000). Infarct scar: a dynamic tissue. Cardiovascular Research 46, 250-256. doi: S0008-6363(00)00032-8 [pii].
58. Tanowitz, H. B., Machado, F. S., Jelicks, L. A., Shirani, J., de Carvalho, A. C., Spray, D. C., Factor, S. M., Kirchhoff, L. V. and Weiss, L. M. (2009). Perspectives on Trypanosoma cruzi-induced heart disease (Chagas disease). Progress in Cardiovascular Disease 51, 524-539. doi: 10.1016/j.pcad.2009.02.001 S0033-0620(09)00012-7 [pii].
59. Tarleton, R. L. (2001). Parasite persistence in the aetiology of Chagas disease. International Journal of Parasitology 31, 550-554. doi: S0020-7519 (01)00158-8 [pii].
60. Tarleton, R. L. (2003). Chagas disease: a role for autoimmunity? Trends in Parasitology 19, 447-451. doi: S1471492203002228 [pii].
61. Teixeira, M. M., da Silva, F. M., Marcili, A., Umezawa, E. S., Shikanai-Yasuda, M. A., Cunha-Neto, E., Kalil, J., Stolf, N. and Stolf, A. M. (2006). Short communication: Trypanosoma cruzi lineage I in endomyocardial biopsy from a north-eastern Brazilian patient at end-stage chronic Chagasic cardiomyopathy. Tropical Medicine and International Health 11, 294-298. doi: 10.1111/j.1365-3156.2006.01575.x.
62. Turner, C. W., Lima, M. F. and Villalta, F. (2002). Trypanosoma cruzi uses a 45-kDa mucin for adhesion to mammalian cells. Biochemical and Biophysical Research Communications 290, 29-34. doi: 10.1006/bbrc.2001.6189.
63. Villalta, F., Scharfstein, J., Ashton, A. W., Tyler, K. M., Guan, F., Mukherjee, S., Lima, M. F., Alvarez, S., Weiss, L. M., Huang, H., Machado, F. S. and Tanowitz, H.B. (2009). Perspectives on the Trypanosoma cruzi-host cell receptor interactions. Parasitology Research 104, 1251-1260. doi: 10.1007/s00436-009-1383-3.
64. Vray, B., Camby, I., Vercruysse, V., Mijatovic, T., Bovin, N. V., Ricciardi-Castagnoli, P., Kaltner, H., Salmon, I., Gabius, H. J. and Kiss, R. (2004). Up-regulation of galectin-3 and its ligands by Trypanosoma cruzi infection with modulation of adhesion and migration of murine dendritic cells. Glycobiology 14, 647-657. doi: 10.1093/glycob/cwh068.
65. WHO (2002). Control of Chagas disease. Report of a WHO Expert Committee. World Health Organization Technical Report Series 905, 1-109.
66. Zhu, Z., Homer, R. J., Wang, Z., Chen, Q., Geba, G. P., Wang, J., Zhang, Y. and Elias, J. A. (1999). Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. Journal of Clinical Investigation 103, 779-788. doi: 10.1172/JCI5909.
67. Zingales, B., Andrade, S.G., Briones, M. R., Campbell, D. A., Chiari, E., Fernandes, O., Guhl, F., Lages-Silva, E., Macedo, A. M., Machado, C. R., Miles, M. A., Romanha, A. J., Sturm, N. R., Tibayrenc, M., Schijman, A. G. and Second Satellite, M. (2009). A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Memórias do Instituto Oswaldo Cruz 104, 1051-1054. doi: S0074-02762009000700021 [pii].
68. Zlochiver, S., Munoz, V., Vikstrom, K. L., Taffet, S. M., Berenfeld, O. and Jalife, J. (2008). Electrotonic myofibroblast-to-myocyte coupling increases propensity to reentrant arrhythmias in two-dimensional cardiac monolayers. Biophysical Journal 95, 4469-4480. doi: 10.1529/biophysj.108.136473.