Participation of heparin binding proteins from the surface of Leishmania (Viannia) braziliensis promastigotes in the adhesion of parasites to Lutzomyia longipalpis cells (Lulo) in vitro

Parasites and Vectors

Volumn 5, Issue 1, 2012, Pages

  De Castro Côrtes, Luzia Monteiro ^a   De Souza Pereira, Mirian Claudia ^b   Da Silva, Franklin Souza ^a   Pereira, Bernardo Acácio Santini ^a   De Oliveira Junior, Francisco Odêncio ^a,b   De Araújo Soares, Renata Oliveira ^a   Brazil, Reginaldo Peçanha ^c   Toma, Leny ^e   Vicente, Carolina Meloni ^e   Nader, Helena Bonciani ^e   De Fátima Madeira, Maria ^d   Bello, Felio J ^f   Alves, Carlos Roberto ^a  

^a Laboratário de Biologia Molecular e Doenças Endêmicas   (Brazil)

^b Laboratário de Ultraestrutura Celular   (Brazil)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

^d Funda??o Oswaldo Cruz   (Brazil)

^e FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^f UNIVERSIDAD DEL ROSARIO   (Colombia)

Author keywords

Glycosaminoglycans; L. (V.) braziliensis; Lulo cells; Promastigotes; Surface plasmon resonance

Indexed keywords

GLYCOSAMINOGLYCAN; HEPARIN; HEPARIN BINDING PROTEIN;

ARTICLE; CELL FRACTIONATION; CELL LINE; CONTROLLED STUDY; EVIDENCE BASED MEDICINE; HOST; IN VITRO STUDY; LEISHMANIA BRAZILIENSIS; LUTZOMYIA; MICROBIAL ADHESION; NONHUMAN; PROMASTIGOTE; PROTEIN ISOLATION; SURFACE PLASMON RESONANCE;

ANIMALS; CELL ADHESION; CELL ADHESION MOLECULES; CELL MEMBRANE; CELLS, CULTURED; GENE EXPRESSION REGULATION; LEISHMANIA BRAZILIENSIS; PSYCHODIDAE;

EID: 84865232755     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/1756-3305-5-142     Document Type: Article

References (49)

1. Cutaneous leishmaniasis. Reithinger R, Dujardin JC, Louzir H, Pirmez C, Alexander B, Brooker S, Lancet Infect Dis 2007 7 581 596 10.1016/S1473-3099(07) 70209-8 17714672 (Pubitemid 47277438)
2. Ecologia das leishmanioses. Transmissores de leishmaniose tegumentar Americana. Rangel EF, Lainson R, Flebotomíneos do Brasil Fiocruz, Rio de Janeiro, Brazil, Rangel EF, Lainson R, 2003 291 309
3. Leishmaniasis: complexity at the host-pathogen interface. Kaye P, Scott P, Nat Rev Microbiol 2011 9 604 615 10.1038/nrmicro2608 21747391
4. New insights into the developmental biology and transmission mechanisms of Leishmania. Bates PA, Rogers ME, Curr Mol Medicine 2004 4 601 609 10.2174/1566524043360285 (Pubitemid 39172366)
5. A novel role for the peritrophic matrix in protecting Leishmania from the hydrolytic activities of the sand fly midgut. Pimenta PF, Modi GB, Pereira ST, Shahabuddin M, Sacks DL, Parasitology 1997 115 359 369 10.1017/S0031182097001510 9364562 (Pubitemid 27448510)
6. Refractory barriers in the sand fly Phlebotomus papatasi (Diptera: Psychodidae) to infection with Leishmania panamensis. Walters LL, Irons KP, Modi GB, Tesh RB, Am J Trop Med Hyg 1992 46 211 228 1539756
7. Leishmania sand fly interaction: progress and challenges. Bates PA, Curr Opin Microbiol 2008 11 340 344 10.1016/j.mib.2008.06.003 18625337
8. Down-regulation of gp63 in Leishmania amazonensis reduces its early development in Lutzomyia longipalpis. Hajmová M, Chang KP, Kolli B, Volf P, Microbes Infect 2004 6 646 649 10.1016/j.micinf.2004.03.003 15158771 (Pubitemid 38670545)
9. Differential midgut attachment of Leishmania (Viannia) braziliensis in the sand flies Lutzomyia (Nyssomyia) whitmani and Lutzomyia (Nyssomyia) intermedia. Soares RP, Margonari C, Secundino NC, Macêdo ME, da Costa SM, Rangel EF, Pimenta PF, Turco SJ, J Biomed Biotechnol 2010 2010 439174 20011070
10. The vectorial competence of Phlebotomus sergenti is specific for Leishmania tropica and is controlled by species-specific, lipophosphoglycan- mediated midgut attachment. Kamhawi S, Modi GB, Pimenta PF, Rowton E, Sacks DL, Parasitology 2000 121 Pt 1 25 33 11085222 (Pubitemid 30616108)
11. Evidence that the vectorial competence of phlebotomine sand flies for different species of Leishmania is controlled by structural polymorphisms in the surface lipophosphoglycan. Pimenta PF, Saraiva EM, Rowton E, Modi GB, Garraway LA, Beverley SM, Turco SJ, Sacks DL, Proc Natl Acad Sci USA 1994 91 9155 9159 10.1073/pnas.91.19.9155 8090785
12. Stage-specific adhesion of Leishmania promastigotes to the sandfly midgut. Pimenta PF, Turco SJ, McConville MJ, Lawyer PG, Perkins PV, Sacks DL, Science 1992 256 1812 1815 10.1126/science.1615326 1615326
13. Transmission of cutaneous leishmaniasis by sand flies is enhanced by regurgitation of fPPG. Rogers ME, Ilg T, Nikolaev AV, Ferguson MA, Bates PA, Nature 2004 430 463 467 10.1038/nature02675 15269771 (Pubitemid 38987909)
14. Lulo cell line derived from Lutzomyia longipalpis (Diptera: Psychodidae): a novel model to assay Leishmania spp. and vector interaction. Côrtes LM, Silva RM, Pereira BA, Guerra C, Zapata AC, Bello FJ, Finkelstein LC, Madeira MF, Brazil RP, Corte-Real S, Alves CR, Parasit Vectors 2011 4 216 10.1186/1756-3305-4-216 22082050
15. Surface determinants of Leishmania parasites and their role in infectivity in the mammalian host. Naderer T, Vince JE, McConville MJ, Curr Mol Med 2004 4 649 665 10.2174/1566524043360069 15357214 (Pubitemid 39172369)
16. Biosynthesis of sulfated glycosaminoglycans in the hemipteran Rhodnius prolixus. Garcia ES, Azambuja P, Nader HB, Dietrich CP, Insect Biochemistry 1986 16 347 352 10.1016/0020-1790(86)90046-6
17. Tissue specific distribution of sulfated mucopolysaccharides in mammals. Toledo OMS, Dietrich CP, Biochim Biophy Acta 1977 498 114 122 10.1016/0304-4165(77)90092-7 (Pubitemid 8117482)
18. Proteins that bind sulfated glycosaminoglycans. Jeffrey D, Esko Robert J, Linhardt, et al. Essentials of glycobiology Cold Spring Harbor Laboratory Press, Cold Spring Harbor (NY), Varki A, Cummings RD, Esko JD, 2 2009
19. Affinity-based methods for the separation of parasite proteins. Alves CR, Silva FS, Oliveira-Junior FO, Pereira BAS, Pires FA, Pereira MCS, Affinity Chromatography In Tech (in press), 2012
20. A heparin-binding activity on Leishmania amastigotes which mediates adhesion to cellular proteoglycans. Love DC, Esko JD, Mosser DM, J Cell Biol 1993 123 759 766 10.1083/jcb.123.3.759 8227137 (Pubitemid 23324931)
21. Blood meal digestion and Leishmania major infections in Phlebotomus duboscqi: effect of carbohydrates inhibiting midgut lectin activity. Volf P, Svobodova M, Dvorakova E, Med Vet Entomol 2001 15 281 286 10.1046/j.0269-283x. 2001.00308.x 11583445 (Pubitemid 32901365)
22. Heparin binds to Leishmania donovani promastigotes and inhibits protein phosphorylation. Mukhopadhyay NK, Shome K, Saha AK, Hassell JR, Glew RH, Biochem J 1989 264 517 525 2557842 (Pubitemid 20024523)
23. Leishmania donovani: cell-surface heparin receptors of promastigotes are recruited from an internal pool after trypsinization. Butcher BA, Shome K, Estes LW, Choay J, Petitou M, Sie P, Glew RH, Exp Parasitol 1990 71 49 59 10.1016/0014-4894(90)90007-Y 2162300 (Pubitemid 20323992)
24. Heparin enhances the interaction of infective Leishmania donovani promastigotes with mouse peritoneal macrophages. A fluorescence flow cytometric analysis. Butcher BA, Sklar LA, Seamer LC, Glew RH, J Immunol 1992 148 2879 2886 1573275
25. Receptors for carbohydrate ligands including heparin on the cell surface of Leishmania and other trypanosomatids. Kock NP, Gabius HJ, Schmitz J, Schotteliu J, Trop Med Int Health 1997 2 863 874 10.1046/j.1365-3156.1997.d01- 405.x 9315045 (Pubitemid 27396014)
26. Heparin binding proteins from Leishmania (Viannia) braziliensis promastigotes. Azevedo-Pereira RL, Pereira MCS, Oliveira FOR, Brazil RP, Côrtes LMC, Madeira MF, Santos ALS, Toma L, Alves CR, Vet Parasitol 2007 145 234 239 10.1016/j.vetpar.2006.12.019 17292553 (Pubitemid 46463911)
27. Leishmania (Viannia) braziliensis: insights on subcellular distribution and biochemical properties of heparin-binding proteins. De Castro Côrtes LM, de Souza Pereira MC, de Oliveira FO, Corte-Real S, da Silva FS, Pereira BA, de Fátima Madeira M, de Moraes MT, Brazil RP, Alves CR, Parasitology 2012 7 1 8
28. Protein measurement with the Folin phenol reagent. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ, J Biol Chem 1951 193 265 275 14907713
29. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Laemmli UK, Nature 1970 227 680 685 10.1038/227680a0 5432063
30. An improved silver staining procedure for schizodeme analysis in polyacrylamide gradient gels. Gonçalves AM, Nehme NS, Morel CM, Mem Inst Oswaldo Cruz 1990 85 101 106 10.1590/S0074-02761990000100017 1699112
31. Electrophoretic behavior of acidic mucopolysaccharides in diamine buffers. Dietrich CP, Dietrich SM, Anal Biochem 1976 70 645 647 10.1016/0003-2697(76)90496-6 131498
32. Arthropod-borne diseases in Italy: from a neglected matter to an emerging health problem. Romi R, Ann Ist Super Sanita 2010 46 436 443 21169676
33. The extinction of dengue through natural vulnerability of its vectors. Williams CR, Bader CA, Kearney MR, Ritchie SA, Russel RC, PLoS Negl Trop Dis 2010 4 922 10.1371/journal.pntd.0000922 21200424
34. Cell biology of Leishmania. Handman E, Adv Parasitol 1999 44 1 39 10563394 (Pubitemid 29465548)
35. Stage-specific adhesion of Leishmania promastigotes to sand fly midguts assessed using an improved comparative binding assay. Wilson R, Bates MD, Dostalova A, Jecna L, Dillon RJ, Volf P, Bates PA, PLoS Negl Trop Dis 2010 4 ii 816 20838647
36. Establishment and characterization of a new continuous cell line from Lutzomyia longipalpis (Diptera: Psychodidae) and its susceptibility to infections with arboviruses and Leishmania chagasi. Rey G, Ferro C, Bello F, Mem Inst Oswaldo Cruz 2000 95 103 110 10.1590/S0074-02762000000100017 10656714
37. Experimental infection of Leishmania (L.) chagasi in a cell line derived from Lutzomyia longipalpis (Diptera: Psychodidae). Bello FJ, Mejía AJ, Corena MP, Ayala M, Sarmiento L, Zú̃iga C, Palau MT, Mem Inst Oswaldo Cruz 2005 100 619 625 10.1590/S0074-02762005000600004
38. Glycosaminoglycan-binding microbial proteins in tissue adhesion and invasion: key events in microbial pathogenicity. Wadström T, Ljungh A, J Med Microbiol 1999 48 223 233 10.1099/00222615-48-3-223 10334589 (Pubitemid 29371567)
39. Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Coppi A, Tewari R, Bishop JR, Bennett BL, Lawrence R, Esko JD, Billker O, Sinnis P, Cell Host & Microbe 2007 2 316 327 10.1016/j.chom.2007.10.002 22880120 (Pubitemid 350056399)
40. Proteoglycans mediate malaria sporozoite targeting to the liver. Pradel G, Garapaty S, Frevert U, Mol Microbiol 2002 45 637 651 10.1046/j.1365-2958. 2002.03057.x 12139612 (Pubitemid 34989173)
41. Plasmodium falciparum during pregnancy: a puzzling parasite tissue adhesion tropism. Nunes MC, Scherf A, Parasitology 2007 134 1863 1869 17958921 (Pubitemid 350014549)
42. Plasmodium falciparum ookinetes require mosquito midgut chondroitin sulfate proteoglycans for cell invasion. Dinglasan RR, Alaganan A, Ghosh AK, Saito A, van Kuppevelt TH, Jacobs-Lorena M, Proc Natl Acad Sci U S A 2007 104 15882 15887 10.1073/pnas.0706340104 17873063 (Pubitemid 350035393)
43. Antiserum against perimicrovillar membranes and midgut tissue reduces the development of Trypanosoma cruzi in the insect vector, Rhodnius prolixus. Gonzalez MS, Hamedi A, Albuquerque-Cunha JM, Nogueira NF, De Souza W, Ratcliffe NA, Azambuja P, Garcia ES, Mello CB, Exp Parasitol 2006 114 297 304 10.1016/j.exppara.2006.04.009 16759654 (Pubitemid 44637215)
44. Trypanosoma cruzi heparin-binding proteins mediate the adherence of epimastigotes to the midgut epithelial cells of Rhodnius prolixus. Oliveira-Jr FOR, Alves CR, Souza-Silva F, Calvet CM, Côrtes LMC, Gonzalez MS, Toma L, Bouças RI, Nader HB, Pereira MCS, Parasitology 2012 139 735 743 10.1017/S0031182011002344 22310218
45. Surface sulfated mucopolysaccharides of primary and permanent mammalian cell lines. Dietrich CP, Montes de Oca H, Biochem Biophys Res Commun 1978 80 805 812 10.1016/0006-291X(78)91316-5 147687 (Pubitemid 8305898)
46. Functions of cell surface heparan sulfate proteoglycans. Bernfield M, Götte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M, Annu Rev Biochem 1999 68 729 777 10.1146/annurev.biochem.68.1.729 10872465 (Pubitemid 29449208)
47. Heparin-like glycosaminoglycans prevent the infection of measles virus in SLAM negative cell lines. Terao-Muto Y, Yoneda M, Seki T, Watanabe A, Tsukiyama-Kohara K, Fujita K, Kai C, Antiviral Res 2008 80 370 376 10.1016/j.antiviral.2008.08.006 18812191
48. Direct measurement of the interactions of glycosaminoglycans and a heparin decasaccharide with the malaria circumsporozoite protein. Rathore D, McCutchan TF, Garboczi DN, Toida T, Hernáiz MJ, LeBrun LA, Lang CS, Linhardt RJ, Biochemistry 2001 40 11518 11524 10.1021/bi0105476 11560500 (Pubitemid 32911294)
49. Exploring the midgut transcriptome of Phlebotomus papatasi: comparative analysis of expression profiles of sugar-fed, blood-fed and Leishmania-major- infected sandflies. Ramalho-Ortigão M, Jochim RC, Anderson JM, Lawyer PG, Pham VM, Kamhawi S, Valenzuela JG, BMC Genomics 2007 8 300 10.1186/1471-2164-8- 300 17760985 (Pubitemid 47604738)