Leishmania mexicana: LACK (Leishmania homolog of receptors for activated C-kinase) is a plasminogen binding protein

Experimental Parasitology

Volumn 127, Issue 4, 2011, Pages 752-761

  Gómez Arreaza, Amaranta ^a   Acosta, Héctor ^a   Barros Álvarez, Ximena ^a   Concepción, Juan L ^a   Albericio, Fernando ^b   Avilan, Luisana ^a  

^a FACULTAD DE CIENCIAS   (Venezuela)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

LACK; Leishmania mexicana; Plasminogen

Indexed keywords

AMINOCAPROIC ACID; BINDING PROTEIN; ENOLASE; LEISHMANIA HOMOLOG OF RECEPTOR FOR ACTIVATED C KINASE; PLASMIN; PLASMINOGEN; PROTOZOAL PROTEIN; TISSUE PLASMINOGEN ACTIVATOR; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL MEMBRANE; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; LEISHMANIA MEXICANA; MICROSOME; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMINOGEN ACTIVATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, PROTOZOAN; BLOTTING, WESTERN; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNE SERA; LEISHMANIA MEXICANA; MOLECULAR STRUCTURE; MUTAGENESIS, SITE-DIRECTED; PLASMINOGEN; PROTOZOAN PROTEINS; RABBITS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

LEISHMANIA MEXICANA;

EID: 79952361927     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2011.01.008     Document Type: Article

References (58)

1. Almeida L., Vanegas G., Calcagno M., Concepción J.L., Avilan L. Plasminogen interaction with Trypanosoma cruzi. Memórias do Instituto Oswaldo Cruz 2004, 99:63-67.
2. Alvarez-Rueda N., Biron M., Le Pape P. Infectivity of Leishmania mexicana is associated with differential expression of protein kinase C-like triggered during a cell-cell contact. PLoS One 2009, 23:e7581.
3. Arnold K., Bordoli L., Kopp J., Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 2006, 22:195-201.
4. Avilan L., Calcagno M., Figuera M., Lemus L., Puig J., Rodríguez A.M. Interaction of Leishmania mexicana promastigotes with the plasminogen-plasmin system. Molecular and Biochemical Parasitology 2000, 110:183-193.
5. Bergmann S., Rohde M., Chhatwal G.S., Hammerschmidt S. Alpha-enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface. Molecular Microbiology 2001, 40:1273-1287.
6. Bergmann S., Wild D., Diekmann O., Frank R., Bracht D., Chhatwal G.S., Hammerschmidt S. Identification of a novel plasmin(ogen)-binding motif in surface displayed alpha-enolase of Streptococcus pneumoniae. Molecular Microbiology 2003, 49:411-423.
7. Bergmeyer H.U. Methods of Enzymatic Analysis 1983, Academic Press, New York.
8. Bernal D., de la Rubia J.E., Carrasco-Abad A.M., Toledo R., Mas-Coma S., Marcilla A. Identification of enolase as a plasminogen-binding protein in excretory-secretory products of Fasciola hepatica. FEBS Letters 2004, 563:203-206.
9. Besson A., Wilson T.L., Yong V.W. The anchoring protein RACK1 links protein kinase Cε to integrin β chains. The Journal of Biological Chemistry 2002, 277:22073-22084.
10. Calcagno M., Avilan L., Colasante C., Berruela L., Salmen S. Interaction of different Leishmania mexicana morphotypes with plasminogen. Parasitology Research 2002, 88:972-978.
11. Chang K.P., McGwire B.S. Molecular determinants and regulation of Leishmania virulence. Kinetoplastid Biology and Disease 2002, 1:1.
12. Coler R.N., Reed S.G. Second-generation vaccines against leishmaniasis. Trends in Parasitology 2005, 21:244-249.
13. Cuervo P., De Jesus J.B., Saboia-Vahia L., Mendonça-Lima L., Domont G.B., Cupolillo E. Proteomic characterization of the released/secreted proteins of Leishmania (Viannia) braziliensis promastigotes. Journal of Proteomics 2009, 73:79-92.
14. de la Torre-Escudero E., Manzano-Román R., Pérez-Sánchez R., Siles-Lucas M., Oleaga A. Cloning and characterization of a plasminogen-binding surface-associated enolase from Schistosoma bovis. Veterinary Parasitology 2010, 173:76-84.
15. Deutsch D.G., Mertz E.T. Plasminogen: purification from human plasma by affinity chromatography. Science 1970, 170:1095-1096.
16. Edgar R.C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004, 5:113.
17. Egea L., Aguilera L., Giménez R., Sorolla M.A., Aguilar J., Badía J., Baldoma L. Role of secreted glyceraldehyde-3-phosphate dehydrogenase in the infection mechanism of enterohemorrhagic and enteropathogenic Escherichia coli: interaction of the extracellular enzyme with human plasminogen and fibrinogen. The International Journal of Biochemistry and Cell Biology 2007, 39:1190-1203.
18. Ehinger S., Schubert W.D., Bergmann S., Hammerschmidt S., Heinz D.W. Plasmin(ogen)-binding alpha-enolase from Streptococcus pneumoniae: crystal structure and evaluation of plasmin(ogen)-binding sites. Journal of Molecular Biology 2004, 343:997-1005.
19. Gonzalez-Aseguinolaza G., Taladriz S., Marquet A., Larraga V. Molecular cloning, cell localization and binding affinity to DNA replication proteins of the p36/LACK protective antigen from Leishmania infantum. European Journal of Biochemistry 1999, 259:909-916.
20. Hurmalainen V., Edelman S., Antikainen J., Baumann M., Lähteenmäki K., Korhonen T.K. Extracellular proteins of Lactobacillus crispatus enhance activation of human plasminogen. Microbiology 2007, 153:1112-1122.
21. Jolodar A., Fischer P., Bergmann S., Büttner D.W., Hammerschmidt S., Brattig N.W. Molecular cloning of an alpha-enolase from the human filarial parasite Onchocerca volvulus that binds human plasminogen. Biochimica et Biophysica Acta 2003, 1627:111-120.
22. Jones M.N., Holt R.G. Cloning and characterization of an alpha-enolase of the oral pathogen Streptococcus mutans that binds human plasminogen. Biochemical and Biophysical Research Communications 2007, 364:924-929.
23. Kamoun-Essghaier S., Guizani I., Strub J.M., Van Dorsselaer A., Mabrouk K., Ouelhazi L., Dellagi K. Proteomic approach for characterization of immunodominant membrane-associated 30- to 36-kiloDalton fraction antigens of Leishmania infantum promastigotes, reacting with sera from Mediterranean visceral leishmaniasis patients. Clinical and Diagnostic Laboratory Immunology 2005, 2:310-320.
24. Kelly B.L., Stetson D.B., Locksley R.M. Leishmania major LACK antigen is required for efficient vertebrate parasitization. The Journal of Experimental Medicine 2003, 198:1689-1698.
25. Lähteenmäki K., Edelman S., Korhonen T.K. Bacterial metastasis: the host plasminogen system in bacterial invasion. Trends in Microbiology 2005, 13:79-85.
26. Lähteenmäki K., Kuusela P., Korhonen T.K. Bacterial plasminogen activators and receptors. FEMS Microbiology Reviews 2001, 25:531-552.
27. Launois P., Pingel S., Himmelrich H., Locksley R., Louis J. Different epitopes of the LACK protein are recognized by V beta 4 V alpha 8 CD4+ T cells in H-2b and H-2d mice susceptible to Leishmania major. Microbes and Infection 2007, 9:1260-1266.
28. Lloyd-Williams P., Albericio F., Giralt E. Chemical Approaches to the Synthesis of Peptides and Proteins 1997, CRC, Boca Raton.
29. Longstaff C. Plasminogen activation on the cell surface. Frontiers in Bioscience 2002, 7:d244-255.
30. Maldonado J., Calcagno M., Puig J., Maizo Z., Avilan L. A study of cutaneous lesions caused by Leishmania mexicana in plasminogen-deficient mice. Experimental and Molecular Pathology 2006, 80:289-294.
31. Marcilla A., Pérez-García A., Espert A., Bernal D., Muñoz-Antolí C., Esteban J.G., Toledo R. Echinostoma caproni: identification of enolase in excretory/secretory products, molecular cloning, and functional expression. Experimental Parasitology 2007, 117:57-64.
32. McGwire B.S., O'Connell W.A., Chang K.P., Engman D.M. Extracellular release of the glycosylphosphatidylinositol (GPI)-linked Leishmania surface metalloprotease, gp63, is independent of GPI phospholipolysis: implications for parasite virulence. The Journal of Biological Chemistry 2002, 277:8802-8809.
33. Miles L.A., Hawley S.B., Baik N., Andronicos N.M., Castellino F.J., Parmer R.J. Plasminogen receptors: the sine qua non of cell surface plasminogen activation. Frontiers in Bioscience 2005, 10:1754-1762.
34. Mottram J.C., Coombs G.H. Leishmania mexicana: subcellular distribution of enzymes in amastigotes and promastigotes. Experimental Parasitology 1985, 59:265-274.
35. Mundodi V., Kucknoor A.S., Alderete J.F. Immunogenic and plasminogen-binding surface-associated alpha-enolase of Trichomonas vaginalis. Infection and Immunity 2008, 76:523-531.
36. Naderer T., Vince J.E., McConville M.J. Surface determinants of Leishmania parasites and their role in infectivity in the mammalian host. Current Molecular Medicine 2004, 4:649-665.
37. Neer E.J., Schmidt C.J., Nambudripad R., Smith T.F. The ancient regulatory-protein family of WD-repeat proteins. Nature 1994, 371:297-300.
38. Pabón M.A., Cáceres A.J., Gualdrón M., Quiñones W., Avilán L., Concepción J.L. Purification and characterization of hexokinase from Leishmania mexicana. Parasitology Research 2007, 100:803-810.
39. Pérez H., Labrador F., Torrealba J.W. Variations in the response of five strains of mice to Leishmania mexicana. International Journal for Parasitology 1979, 9:27-32.
40. Quiñones W., Peña P., Domingo-Sananes M., Cáceres A., Michels P.A., Avilan L., Concepción J.L. Leishmania mexicana: molecular cloning and characterization of enolase. Experimental Parasitology 2007, 116:241-251.
41. Ramajo-Hernández A., Pérez-Sánchez R., Ramajo-Martín V., Oleaga A. Schistosoma bovis: plasminogen binding in adults and the identification of plasminogen-binding proteins from the worm tegument. Experimental Parasitology 2007, 115:83-91.
42. Rothberg K.G., Burdette D.L., Pfannstiel J., Jetton N., Singh R., Ruben L. The RACK1 homologue from Trypanosoma brucei is required for the onset and progression of cytokinesis. The Journal of Biological Chemistry 2006, 281:9781-9790.
43. Salay G., Dorta M.L., Santos N.M., Mortara R.A., Brodskyn C., Oliveira C.I., Barbieri C.L., Rodrigues M.M. Testing of four Leishmania vaccine candidates in a mouse model of infection with Leishmania (Viannia) braziliensis, the main causative agent of cutaneous leishmaniasis in the New World. Clinical and Vaccine Immunology 2007, 14:1173-1181.
44. Schechtman D., Mochly-Rosen D. Adaptor proteins in protein kinase C-mediated signal transduction. Oncogene 2001, 20:6339-6347.
45. Sha J., Erova T.E., Alyea R.A., Wang S., Olano J.P., Pancholi V., Chopra A.K. Surface-expressed enolase contributes to the pathogenesis of clinical isolate SSU of Aeromonas hydrophila. Journal of Bacteriology 2009, 191:3095-3107.
46. Silverman J.M., Chan S.K., Robinson D.P., Dwyer D.M., Nandan D., Foster L.J., Reiner N.E. Proteomic analysis of the secretome of Leishmania donovani. Genome Biology 2008, 9:R35.
47. Silverman J.M., Clos J., de'Oliveira C.C., Shirvani O., Fang Y., Wang C., Foster L.J., Reiner N.E. An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages. Journal of Cell Science 2010, 123:842-852.
48. Studier W. Protein production by auto-induction in high-density shaking cultures. Protein Expression and Purification 2005, 41:207-234.
49. Sun H. The interaction between pathogens and the host coagulation system. Physiology (Bethesda) 2006, 21:281-288.
50. Taladriz S., Gonzalez-Aseguinolaza G., Marquet A., Larraga V. Cloning, molecular analysis and differential cell localisation of the p36 RACK analogue antigen from the parasite protozoon Crithidia fasciculata. FEBS Letters 1999, 443:375-380.
51. Ullah H., Scappini E.L., Moon A.F., Williams L.V., Armstrong D.L., Pedersen L.C. Structure of a signal transduction regulator, RACK1, from Arabidopsis thaliana. Protein Science 2008, 17:1771-1780.
52. Urbina J.A., Concepcion J.L., Rangel S., Visbal G., Lira R. Squalene synthase as a chemotherapeutic target in Trypanosoma cruzi and Leishmania mexicana. Molecular and Biochemical Parasitology 2002, 125:35-45.
53. Vanegas G., Quiñones W., Carrasco-López C., Concepción J.L., Albericio F., Avilán L. Enolase as a plasminogen binding protein in Leishmania mexicana. Parasitology Research 2007, 101:1511-1516.
54. Vassalli J.D., Sappino A.P., Belin D. The plasminogen activator/plasmin system. The Journal of Clinical Investigation 1991, 88:1067-1072.
55. Walker M.J., McArthur J.D., McKay F., Ranson M. Is plasminogen deployed as a Streptococcus pyogenes virulence factor?. Trends in Microbiology 2005, 13:308-313.
56. Walker J.M. Nondenaturing polyacrylamidie gel electrophoresis of proteins. The Protein Protocols Handbook 2002, 57-60. Humana Press, New Jersey. J.M. Walker (Ed.).
57. Yang J., Qiu C., Xia Y., Yao L., Fu Z., Yuan C., Feng X., Lin J. Molecular cloning and functional characterization of Schistosoma japonicum enolase which is highly expressed at the schistosomulum stage. Parasitology Research 2010, 107:667-677.
58. Yao C., Li Y., Donelson J.E., Wilson M.E. Proteomic examination of Leishmania chagasi plasma membrane proteins: contrast between avirulent and virulent (metacyclic) parasite forms. Proteomics Clinical Applications 2010, 4:4-16.