Gap junction reduction in cardiomyocytes following transforming growth factor- β treatment and Trypanosoma cruzi infection

Memorias do Instituto Oswaldo Cruz

Volumn 104, Issue 8, 2009, Pages 1083-1090

  Waghabi, Mariana C ^a,b   Coutinho Silva, Robson ^b,c   Feige, Jean Jacques ^d   Higuchi, Maria de Lourdes ^e   Becker, David ^f   Burnstock, Geoffrey ^b   de Araújo Jorge, Tânia C ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^c FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^d INSERM   (France)

^e UNIVERSITY OF SÃO PAULO   (Brazil)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Chagas disease; Connexin 43; Gap junction; Heart; Transforming growth factor

Indexed keywords

TRYPANOSOMA CRUZI;

EID: 72449171585     PISSN: 00740276     EISSN: 16788060     Source Type: Journal    
DOI: 10.1590/S0074-02762009000800004     Document Type: Article

References (46)

1. Adesse D, Garzoni LR, Huang H, Tanowitz HB, Meirelles MN, Spray DC 2008. Trypanosoma cruzi induces changes in cardiac connexin43 expression. Microbes Infect 10: 21-28.
2. Araújo-Jorge TC, Waghabi MC, Hasslocher-Moreno AM, Xavier SS, Higuchi ML, Keramidas M, Bailly S, Feige JJ 2002. Implication of transforming growth factor-beta1 in Chagas disease cardiomyopathy. J Infect Dis 186: 1823-1828.
3. Araújo-Jorge TC, Waghabi MC, Soeiro MNC, Keramidas M, Bailly S, Feige JJ 2008. Pivotal role for TGF-β in infectious heart disease: the case of Trypanosoma cruzi infection and its consequent chagasic cardiomyopathy. Cytok Growth Factors Rev 19: 405-413.
4. Bastide B, Neyses L, Ganten D, Paul M, Willecke K, Traub O 1993. Gap junction protein connexin40 is preferentially expressed in vascular endothelium and conductive bundles of rat myocardium and is increased under hypertensive conditions. Circ Res 73: 1138-1149.
5. Beardslee MA, Lerner DL, Tadros PN, Laing JG, Beyer EC, Yamada KA, Kleber AG, Schuessler RB, Saffitz JE 2000. Dephosphorylation and intracellular redistribution of ventricular connexin43 during electrical uncoupling induced by ischemia. Circ Res 87: 656-662.
6. Becker DL, Davies CS 1995. Role of gap junctions in the development of the preimplantation mouse embryo. Microsc Res Tech 31: 364-374.
7. Campos de Carvalho AC, Tanowitz HB, Wittner M, Dermietzel R, Roy C, Hertzberg EL, Spray DC 1992. Gap junction distribution is altered between cardiac myocytes infected with Trypanosoma cruzi. Circ Res 70: 733-742.
8. Casado J, Davila DF, Donis JH, Torres A, Payares A, Colmenares R, Gottberg CF 1990. Electrocardiographic abnormalities and left ventricular systolic function in Chagas' heart disease. Int J Cardiol 27: 55-62.
9. Chanson M, Derouette JP, Roth I, Foglia B, Scerri I, Dudez T, Kwak BR 2005. Gap junctional communication in tissue inflammation and repair. Biochim Biophys Acta 1711: 197-207.
10. Chen X, Zhang Y 2006. Myocardial Cx43 expression in the cases of sudden death due to dilated cardiomyopathy. Forensic Sci Int 162: 170-173.
11. Coutinho-Silva R, Parsons M, Robson T, Burnstock G 2001. Changes in expression of P2 receptor in rat and mouse pancreas during development and aging. Cell Tissue Res 306: 373-383.
12. Flanders KC, Holder MG, Winokur TS 1995. Autoinduction of mRNA and protein expression for transforming growth factor-beta S in cultured cardiac cells. J Mol Cell Cardiol 27: 805-812.
13. Fortes FSA, Pecora IL, Costa V, Coutinho-Silva R, Bisaggio RC, Pires-de-Farias F, Persechini PM, Campos-de-Carvalho AC, Goldenberg RC 2004. Modulation of intercellular communication in macrophages: possible interactions between gap junctions and P2 receptors. J Cell Sci 117: 4717-4726.
14. Higuchi ML, Fukasawa S, De Brito T, Parzianello LC, Bellotti G, Ramires JA 1999. Different microcirculatory and interstitial matrix patterns in idiopathic dilated cardiomyopathy and Chagas' disease: a three dimensional confocal microscopy study. Heart 82: 279-285.
15. Higuchi ML, Reis MM, Aiello VD, Benvenuti LA, Gutierrez PS, Bellotti G, Pileggi F 1997. Association of an increase in CD8+ T cells with the presence of Trypanosoma cruzi antigens in chronic, human, chagasic myocarditis. Am J Trop Med Hyg 56: 485-489.
16. Hurst VIV, Goldberg PL, Minnear FL, Heimark RL, Vincent PA 1999. Rearrangement of adherens junctions by transforming growth factor-beta1: role of contraction. Am J Physiol 276: 582-595.
17. Inman GJ, Nicolas FJ, Callahan JF, Harling JD, Gaster LM, Reith AD, Laping NJ, Hill CS 2002. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5 and ALK7. Mol Pharmacol 62: 65-74.
18. Jiang L, Bardini M, Keogh A, Remedios CG, Burnstock G 2005. P2X1 receptors are closely associated with connexin43 in human ventricular myocardium. Int J of Cardiol 98: 291-297.
19. Kaprielian RR, Gunning M, Dupont E, Sheppard MN, Rothery SM, Underwood R, Pennell DJ, Fox K, Pepper J, Poole-Wilson PA, Severs NJ 1998. Downregulation of immunodetectable connexin43 and decreased gap junction size in the pathogenesis of chronic hibernation in the human left ventricle. Circulation 97: 651-660.
20. Kostin S, Rieger M, Dammer S, Hein S, Richter M, Klovekorn WP, Bauer EP, Schaper J 2003. Gap junction remodeling and altered connexin43 expression in the failing human heart. Mol Cell Biochem 242: 135-144.
21. Marin-Neto JA, Cunha-Neto E, Maciel BC, Simões MV 2007. Pathogenesis of chronic Chagas heart disease. Circulation 115: 1109-1123.
22. Meirelles MNL, Araújo-Jorge TC, Miranda CF, De Souza W, Barbosa HS 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.
23. Mori R, Power KT, Wang CM, Martin P, Becker DL 2006. Acute downregulation of connexin43 at wound sites leads to a reduced inflammatory response, enhanced keratinocyte proliferation and wound fibroblast migration. J Cell Sci 119: 5193-5203.
24. Palomino SA, Aiello VD, Higuchi ML 2000. Systematic mapping of hearts from chronic chagasic patients: the association between the occurrence of histopathological lesions and Trypanosoma cruzi antigens. Ann Trop Med Parasitol 94: 571-579.
25. Pereira MC, Singer RH, Meirelles MN 2000. Ultrastructural distribution of poly (A)+ RNA during Trypanosoma cruzi-cardiomyocyte interaction in vitro: a quantitative analysis of the total mRNA content by in situ hybridization. J Eukaryot Microbiol 47: 264-270.
26. Peters NS, Green CR, Poole-Wilson PA, Severs NJ 1993. Reduced content of connexin43 gap junctions in ventricular myocardium from hypertrophied and ischemic human hearts. Circulation 88: 864-875.
27. Reis MM, Higuchi ML, Benvenuti LA, Aiello VD, Gutierrez PS, Bellotti G, Pileggi F 1997. An in situ quantitative immunohistochemical study of cytokines and IL-2R+ in chronic human chagasic myocarditis: correlation with the presence of myocardial Trypanosoma cruzi antigens. Clin Immunol Immunopathol 83: 165-172.
28. Rodriguez-Sinovas A, Cabestrero A, Lopez D, Torre I, Morente M, Abellan A, Miro E, Ruiz-Meana M, Garcia-Dorado D 2007. The modulatory effects of connexin43 on cell death/survival beyond cell coupling. Prog Biophys Mol Biol 94: 219-232.
29. Rosendahl A, Checchin D, Fehniger TE, ten Dijke P, Heldin CH, Sideras P 2001. Activation of the TGF-beta/activin-Smad2 pathway during allergic airway inflammation. Am J Respir Cell Mol Biol 25: 60-68.
30. Rudkin GH, Yamaguchi DT, Ishida K, Peterson WJ, Bahadosingh F, Thye D, Miller TA 1996. Transforming growth factor-beta, osteogenin and bone morphogenetic protein-2 inhibit intercellular communication and alter cell proliferation in MC3T3-E1 cells. J Cell Physiol 168: 433-441.
31. Schmunis G A 2007. Epidemiology of Chagas disease in non-endemic countries: the role of international migration. Mem Inst Oswaldo Cruz 102: 75-85.
32. Sepp R, Severs NJ, Gourdie RG 1996. Altered patterns of cardiac intercellular junction distribution in hypertrophic cardiomyopathy. Heart 76: 412-417.
33. Severs NJ 2001. Gap junction remodeling and cardiac arrhythmogenesis: cause or coincidence? J Cell Mol Med 5: 355-366.
34. Severs NJ, Coppen SR, Dupont E, Yeh HI, Ko YS, Matsushita T 2004. Gap junction alterations in human cardiac disease. Cardiovasc Res 62: 368-377.
35. Severs NJ, Dupont E, Coppen SR, Halliday D, Inett E, Baylis D, Rothery S 2004. Remodelling of gap junctions and connexin expression in heart disease. Biochim Biophys Acta 1662: 138-148.
36. Silva JS, Twardzik DR, Reed SG 1991. Regulation of Trypanosoma cruzi infections in vitro and in vivo by transforming growth factor beta (TGF-beta). J Exp Med 174: 539-545.
37. Sohl G, Willecke K 2004. Gap junctions and the connexin protein family. Cardiovasc Res 62: 228-232.
38. Spach MS, Boineau JP 1997. Microfibrosis produces electrical load variations due to loss of side-to-side cell connections: a major mechanism of structural heart disease arrhythmias. Pacing Clin Electrophysiol 20: 397-413.
39. Spray DC, Burt JM 1990. Structure-activity relations of the cardiac gap junction channel. Am J Physiol 258: 195-205.
40. Tabibzadeh S 2002. Homeostasis of extracellular matrix by TGF-beta and lefty. Front Biosci 7: 1231-1246.
41. Tansey EE, Kwaku KF, Hammer PE, Cowan DB, Federman M, Levitsky S, McCully JD 2006. Reduction and redistribution of gap and adherens junction proteins after ischemia and reperfusion. Ann Thorac Surg 82: 1472-1479.
42. Uzzaman M, Honjo H, Takagishi Y, Emdad L, Magee AI, Severs NJ, Kodama I 2000. Remodeling of gap junctional coupling in hypertrophied right ventricles of rats with monocrotaline-induced pulmonary hypertension. Circ Res 86: 871-878.
43. van Zoelen EJ, Tertoolen LG 1991. Transforming growth factor-beta enhances the extent of intercellular communication between normal rat kidney cells. J Biol Chem 266: 12075-12081.
44. Waghabi MC, Keramidas M, Bailly S, Degrave W, Mendonça-Lima L, Soeiro MNC, Meirelles MN, Paciornik S, Araújo-Jorge TC, Feige JJ 2005. Uptake of host cell transforming growth factor-beta by Trypanosoma cruzi amastigotes in cardiomyocytes: potential role in parasite cycle completion. Am J Pathol 167: 993-1003.
45. Waghabi MC, Keramidas M, Calvet CM, Meuser M, Soeiro MNC, Mendonça-Lima L, Araújo-Jorge TC, Feige JJ, Bailly S 2002. Increased Trypanosoma cruzi invasion and heart fibrosis associated with high transforming growth factor beta levels in mice deficient in alpha(2)-macroglobulin. Infect Immun 70: 5115-5123.
46. Waghabi MC, Keramidas M, Calvet CM, Meuser M, Soeiro MNC, Mendonça-Lima L, Araújo-Jorge TC, Feige JJ, Bailly S 2007. SB- 431542, a transforming growth factor beta inhibitor, impairs Trypanosoma cruzi infection in cardiomyocytes and parasite cycle completion. Antimicrob Agents Chemother 51: 2905-2910.