Apolipoprotein A-I truncations in chagas disease are caused by cruzipain, the major cysteine protease of trypanosoma cruzi

American Journal of Pathology

Volumn 184, Issue 4, 2014, Pages 976-984

  Miao, Qianqian ^a,b   Santamaria, Cynthia ^a   Bailey, Dana ^a   Genest, Jacques ^a   Ward, Brian J ^a,b   Ndao, Momar ^a,b  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b MONTREAL GENERAL HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN A1; CRUZIPAIN; HIGH DENSITY LIPOPROTEIN; BIOLOGICAL MARKER; CYSTEINE PROTEINASE; PEPTIDE FRAGMENT;

ADIPOCYTE; AGAR GEL ELECTROPHORESIS; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MEMBRANE; CHAGAS DISEASE; CONTROLLED STUDY; DISEASE MARKER; ENZYME ACTIVITY; EPIMASTIGOTE; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; GENE CONTROL; HUMAN; HUMAN CELL; IN VITRO STUDY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; TANDEM MASS SPECTROMETRY; TRYPANOSOMA CRUZI; WESTERN BLOTTING; AMINO ACID SEQUENCE; ENZYMOLOGY; HOST PARASITE INTERACTION; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; TWO DIMENSIONAL GEL ELECTROPHORESIS;

AMINO ACID SEQUENCE; APOLIPOPROTEIN A-I; BIOLOGICAL MARKERS; BLOTTING, WESTERN; CHAGAS DISEASE; CYSTEINE ENDOPEPTIDASES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HOST-PARASITE INTERACTIONS; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TRYPANOSOMA CRUZI;

EID: 84897890418     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.12.018     Document Type: Article

References (46)

1. World Health Organization Special programme for research and training in tropical disease (TDR) Report of Scientific Group in CD 2007 World Health Organization Buenos Aires, Argentina 5
2. J. Gascon, C. Bern, and M.J. Pinazo Chagas disease in Spain, the United States and other non-endemic countries Acta Trop 115 2010 22 27
3. H.B. Tanowitz, L.M. Weiss, and S.P. Montgomery Chagas disease has now gone global PLoS Negl Trop Dis 5 2011 e1136
4. J.H. Maguire Trypanosoma S. Gorbach, J. Bartlett, N. Backlow, Infectious Diseases 2004 Lippincott Williams & Wilkins Philadelphia 2327 2334
5. J.H. Maguire Chagas' disease-can we stop the deaths? N Engl J Med 355 2006 760 761
6. E. Dias, F.S. Laranja, A. Miranda, and G. Nobrega Chagas' disease; a clinical, epidemiologic, and pathologic study Circulation 14 1956 1035 1060
7. Y.M. Gomes, V.M. Lorena, and A.O. Luquetti Diagnosis of Chagas disease: what has been achieved? what remains to be done with regard to diagnosis and follow up studies? Mem Inst Oswaldo Cruz 104 Suppl 1 2009 115 121
8. M. Ndao, T.W. Spithill, R. Caffrey, H. Li, V.N. Podust, R. Perichon, C. Santamaria, A. Ache, M. Duncan, M.R. Powell, and B.J. Ward Identification of novel diagnostic serum biomarkers for Chagas' disease in asymptomatic subjects by mass spectrometric profiling J Clin Microbiol 48 2010 1139 1149
9. J. Mishra, Q. Ma, A. Prada, M. Mitsnefes, K. Zahedi, J. Yang, J. Barasch, and P. Devarajan Identification of neutrophil gelatinase-associated lipocalin as a novel early urinary biomarker for ischemic renal injury J Am Soc Nephrol 14 2003 2534 2543
10. Q.Y. He, G.K. Lau, Y. Zhou, S.T. Yuen, M.C. Lin, H.F. Kung, and J.F. Chiu Serum biomarkers of hepatitis B virus infected liver inflammation: a proteomic study Proteomics 3 2003 666 674
11. A.R. Tall An overview of reverse cholesterol transport Eur Heart J 19 Suppl A 1998 A31 A35
12. P.J. Barter, S. Nicholls, K.A. Rye, G.M. Anantharamaiah, M. Navab, and A.M. Fogelman Antiinflammatory properties of HDL Circ Res 95 2004 764 772
13. C. Mineo, H. Deguchi, J.H. Griffin, and P.W. Shaul Endothelial and antithrombotic actions of HDL Circ Res 98 2006 1352 1364
14. A.R. Tall, and J.L. Breslow Plasma high density lipoproteins and atherogenesis 1996 Lipincott Raven Philadelphia 105 128
15. R.H. Neary, and E. Gowland Stability of free apolipoprotein A-1 concentration in serum, and its measurement in normal and hyperlipidemic subjects Clin Chem 33 1987 1163 1169
16. M.N. Palgunachari, V.K. Mishra, S. Lund-Katz, M.C. Phillips, S.O. Adeyeye, S. Alluri, G.M. Anantharamaiah, and J.P. Segrest Only the two end helixes of eight tandem amphipathic helical domains of human apo A-I have significant lipid affinity. Implications for HDL assembly Arterioscler Thromb Vasc Biol 16 1996 328 338
17. V.K. Mishra, M.N. Palgunachari, G. Datta, M.C. Phillips, S. Lund-Katz, S.O. Adeyeye, J.P. Segrest, and G.M. Anantharamaiah Studies of synthetic peptides of human apolipoprotein A-I containing tandem amphipathic alpha-helixes Biochemistry 37 1998 10313 10324
18. K.L. Gillotte, M. Zaiou, S. Lund-Katz, G.M. Anantharamaiah, P. Holvoet, A. Dhoest, M.N. Palgunachari, J.P. Segrest, K.H. Weisgraber, G.H. Rothblat, and M.C. Phillips Apolipoprotein-mediated plasma membrane microsolubilization: role of lipid affinity and membrane penetration in the efflux of cellular cholesterol and phospholipid J Biol Chem 274 1999 2021 2028
19. H.J. Pownall, Q. Pao, and J.B. Massey Isolation and specificity of rat lecithin: cholesterol acyltransferase: comparison with the human enzyme using reassembled high-density lipoproteins containing ether analogs of phosphatidylcholine Biochim Biophys Acta 833 1985 456 462
20. P.G. Frank, and Y.L. Marcel Apolipoprotein A-I: structure-function relationships J Lipid Res 41 2000 853 872
21. A.C. Murta, P.M. Persechini, S. Padron Tde, W. de Souza, J.A. Guimaraes, and J. Scharfstein Structural and functional identification of GP57/51 antigen of Trypanosoma cruzi as a cysteine proteinase Mol Biochem Parasitol 43 1990 27 38
22. P. Berasain, C. Carmona, B. Frangione, J.J. Cazzulo, and F. Goni Specific cleavage sites on human IgG subclasses by cruzipain, the major cysteine proteinase from Trypanosoma cruzi Mol Biochem Parasitol 130 2003 23 29
23. E. Del Nery, M.A. Juliano, A.P. Lima, J. Scharfstein, and L. Juliano Kininogenase activity by the major cysteinyl proteinase (cruzipain) from Trypanosoma cruzi J Biol Chem 272 1997 25713 25718
24. A.M. Canavaci, J.M. Bustamante, A.M. Padilla, C.M. Perez Brandan, L.J. Simpson, D. Xu, C.L. Boehlke, and R.L. Tarleton In vitro and in vivo high-throughput assays for the testing of anti-Trypanosoma cruzi compounds PLoS Negl Trop Dis 4 2010 e740
25. E.P. Camargo Growth and differentiation in Trypanosoma cruzi, I: origin of metacyclic trypanosomes in liquid media Rev Inst Med Trop Sao Paulo 6 1964 93 100
26. M. Berrizbeitia, M. Ndao, J. Bubis, M. Gottschalk, A. Ache, S. Lacouture, M. Medina, and B.J. Ward Purified excreted-secreted antigens from Trypanosoma cruzi trypomastigotes as tools for diagnosis of Chagas' disease J Clin Microbiol 44 2006 291 296
27. A.E. Eakin, A.A. Mills, G. Harth, J.H. McKerrow, and C.S. Craik The sequence, organization, and expression of the major cysteine protease (cruzain) from Trypanosoma cruzi J Biol Chem 267 1992 7411 7420
28. F.W. Studier Protein production by auto-induction in high density shaking cultures Protein Expr Purif 41 2005 207 234
29. J.J. Cazzulo, M.C. Cazzulo Franke, J. Martinez, and B.M. Franke de Cazzulo Some kinetic properties of a cysteine proteinase (cruzipain) from Trypanosoma cruzi Biochim Biophys Acta 1037 1990 186 191
30. G.F. Lewis, and D.J. Rader New insights into the regulation of HDL metabolism and reverse cholesterol transport Circ Res 96 2005 1221 1232
31. F. Nagajyothi, M.S. Desruisseaux, N. Thiruvur, L.M. Weiss, V.L. Braunstein, C. Albanese, M.M. Teixeira, C.J. de Almeida, M.P. Lisanti, P.E. Scherer, and H.B. Tanowitz Trypanosoma cruzi infection of cultured adipocytes results in an inflammatory phenotype Obesity (Silver Spring) 16 2008 1992 1997
32. T.P. Combs, F. Nagajyothi, S. Mukherjee, C.J. de Almeida, L.A. Jelicks, W. Schubert, Y. Lin, D.S. Jayabalan, D. Zhao, V.L. Braunstein, S. Landskroner-Eiger, A. Cordero, S.M. Factor, L.M. Weiss, M.P. Lisanti, H.B. Tanowitz, and P.E. Scherer The adipocyte as an important target cell for Trypanosoma cruzi infection J Biol Chem 280 2005 24085 24094
33. A.V. Ferreira, M. Segatto, Z. Menezes, A.M. Macedo, C. Gelape, L. de Oliveira Andrade, F. Nagajyothi, P.E. Scherer, M.M. Teixeira, and H.B. Tanowitz Evidence for Trypanosoma cruzi in adipose tissue in human chronic Chagas disease Microbes Infect 13 2011 1002 1005
34. R. Barbaras, P. Puchois, J.C. Fruchart, and G. Ailhaud Cholesterol efflux from cultured adipose cells is mediated by LpAI particles but not by LpAI: AII particles Biochem Biophys Res Commun 142 1987 63 69
35. G.R. Castro, and C.J. Fielding Early incorporation of cell-derived cholesterol into pre-beta-migrating high-density lipoprotein Biochemistry 27 1988 25 29
36. M. Kawano, T. Miida, C.J. Fielding, and P.E. Fielding Quantitation of pre beta-HDL-dependent and nonspecific components of the total efflux of cellular cholesterol and phospholipid Biochemistry 32 1993 5025 5028
37. P.E. Fielding, M. Kawano, A.L. Catapano, A. Zoppo, S. Marcovina, and C.J. Fielding Unique epitope of apolipoprotein A-I expressed in pre-beta-1 high-density lipoprotein and its role in the catalyzed efflux of cellular cholesterol Biochemistry 33 1994 6981 6985
38. S.T. Kunitake, G.C. Chen, S.F. Kung, J.W. Schilling, D.A. Hardman, and J.P. Kane Pre-beta high density lipoprotein. Unique disposition of apolipoprotein A-I increases susceptibility to proteolysis Arteriosclerosis 10 1990 25 30
39. J. Vernal, J. Munoz-Jordan, M. Muller, J.J. Cazzulo, and C. Nowicki Sequencing and heterologous expression of a cytosolic-type malate dehydrogenase of Trypanosoma brucei Mol Biochem Parasitol 117 2001 217 221
40. F. Parussini, V.G. Duschak, and J.J. Cazzulo Membrane-bound cysteine proteinase isoforms in different developmental stages of Trypanosoma cruzi Cell Mol Biol (Noisy-le-grand) 44 1998 513 519
41. J. Scharfstein, M. Schechter, M. Senna, J.M. Peralta, L. Mendonca-Previato, and M.A. Miles Trypanosoma cruzi: characterization and isolation of a 57/51,000 m.w. surface glycoprotein (GP57/51) expressed by epimastigotes and bloodstream trypomastigotes J Immunol 137 1986 1336 1341
42. J.J. Cazzulo Proteinases of Trypanosoma cruzi: potential targets for the chemotherapy of Chagas disease Curr Top Med Chem 2 2002 1261 1271
43. R.P. Prioli, I. Rosenberg, S. Shivakumar, and M.E. Pereira Specific binding of human plasma high density lipoprotein (cruzin) to Trypanosoma cruzi Mol Biochem Parasitol 28 1988 257 263
44. R.P. Prioli, I. Rosenberg, and M.E. Pereira Specific inhibition of Trypanosoma cruzi neuraminidase by the human plasma glycoprotein "cruzin" Proc Natl Acad Sci U S A 84 1987 3097 3101
45. M.S. Desruisseaux, F. Nagajyothi, M.E. Trujillo, H.B. Tanowitz, and P.E. Scherer Adipocyte, adipose tissue, and infectious disease Infect Immun 75 2007 1066 1078
46. F. Nagajyothi, L.M. Weiss, D.L. Silver, M.S. Desruisseaux, P.E. Scherer, J. Herz, and H.B. Tanowitz Trypanosoma cruzi utilizes the host low density lipoprotein receptor in invasion PLoS Negl Trop Dis 5 2011 e953