The Repetitive Domain of ScARP3d Triggers Entry of Spiroplasma citri into Cultured Cells of the Vector Circulifer haematoceps

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Béven, Laure ^a,b   Duret, Sybille ^a,b   Batailler, Brigitte ^a,b,c   Dubrana, Marie Pierre ^a,b   Saillard, Colette ^a,b   Renaudin, Joël ^a,b   Arricau Bouvery, Nathalie ^a,b  

^a Univ Bordeaux   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c University of Bordeaux   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; CYTOCHALASIN D; LATEX; SPIROPLASMA CITRI ADHESION RELATED PROTEIN 3D; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; AGGLUTINATION TEST; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL TRANSMISSION; BACTERIUM ADHERENCE; BACTERIUM CARRIER; BACTERIUM MUTANT; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL ASSAY; CELL INVASION; CIRCULIFER HAEMATOCEPS; CONTROLLED STUDY; HOST PATHOGEN INTERACTION; INTERNALIZATION; LEAFHOPPER; MOLECULAR INTERACTION; NONHUMAN; PLASMID; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; REPEAT DOMAIN; SPIROPLASMA CITRI; WILD TYPE;

ADHESINS, BACTERIAL; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL ADHESION; BINDING SITES; BLOTTING, WESTERN; CELL LINE; CELL MEMBRANE; CYTOCHALASIN D; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCYTOSIS; HEMIPTERA; HOST-PATHOGEN INTERACTIONS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; MUTATION; REPETITIVE SEQUENCES, AMINO ACID; SPIROPLASMA CITRI;

CIRCULIFER HAEMATOCEPS; HEXAPODA; SPIROPLASMA; SPIROPLASMA CITRI;

EID: 84868333562     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048606     Document Type: Article

References (50)

1. Saglio P, (1973) Lhospital M, Laflèche D, Dupont G, Bové JM, et al (1973) Spiroplasma citri gen. and sp. nov.: a mycoplasma-like organism associated with stubborn disease of citrus. Int J Syst Bacteriol 23: 191-204.
2. Saglio P, Laflèche D, Bonisol C, Bové JM, (1971) Culture in vitro des mycoplasmes associés au stubborn des agrumes et leur observation au microscope électronique. C R Acad Sci Paris 272: 1387-1390.
3. Fletcher J, Schultz GA, Davis RE, Eastman CE, Goodman RM, (1981) Brittle root disease of horseradish: evidence for an etiological role of Spiroplasma citri. Phytopathology 71: 1073-1080.
4. Fos A, Bové JM, Lallemand J, Saillard C, Vignault JC, et al. (1986) The leafhopper Neoaliturus haematoceps is a vector of Spiroplasma citri in the mediterranean area. Ann Inst Pasteur Microbiol 137A: 97-107.
5. Liu HY, Gumpf DJ, Oldfield GN, Calavan EC, (1983) Transmission of Spiroplasma citri by Circulifer tenellus. Phytopathology 73: 582-585.
6. Rasooly R, Raccah B, Klein M, (1994) Laboratory transmission of the citrus stubborn disease agent by a leafhopper from the Circulifer tenellus complex from the Jordan valley. Phytoparasitica 22: 209-218.
7. Liu HY, Gumpf DJ, Oldfield GN, Calavan EC, (1983) The relationship of Spiroplasma citri and Circulifer tenellus. Phytopathology 73: 585-590.
8. Fletcher J, Wayadande A, Melcher U, Ye FC, (1998) The phytopathogenic mollicute-insect vector interface: a closer look. Phytopathology 88: 1351-1358.
9. Ammar E-D, Fulton D, Bai X, Meulia T, Hogenhout SA, (2004) An attachment tip and pili- like structures in insect- and plant-pathogenic spiroplasmas of the class Mollicutes. Arch Microbiol 181: 97-105.
10. Özbek E, Miller SA, Meulia T, Hogenhout SA, (2003) Infection and replication sites of Spiroplasma kunkelii (Class: Mollicutes) in midgut and Malpighian tubules of leafhopper Dalbulus maidis. J Invert Pathol 82(3): 167-175.
11. Kwon MO, Wayadande AC, Fletcher J, (1999) Spiroplasma citri movement into the intestines and salivary glands of its leafhopper vector, Circulifer tenellus. Phytopathology 89: 1144-1151.
12. Duret S, Batailler B, Danet J-L, Béven L, Renaudin J, et al. (2010) Infection of the Circulifer haematoceps cell line Ciha-1 by Spiroplasma citri: the non insect-transmissible strain 44 is impaired in invasion. Microbiology 156: 1097-1107.
13. Killiny N, Batailler B, Foissac X, Saillard C, (2006) Identification of a Spiroplasma citri hydrophilic protein associated with insect transmissibility. Microbiology 152: 1221-1230.
14. Saillard C, Carle P, Duret-Nurbel S, Henri R, Killiny N, et al. (2008) The abundant extrachromosomal content of Spiroplasma citri strain GII3-3X. BMC Genomics 9: 195-207.
15. Berho N, Duret S, Renaudin J, (2006) Absence of plasmids encoding adhesion-related proteins in non insect-transmissible strains of Spiroplasma citri. Microbiology 152: 873-886.
16. Berho N, Duret S, Danet JL, Renaudin J, (2006) Plasmid pSci6 from Spiroplasma citri GII-3 confers insect transmissility to the non-transmissible S. citri strain 44. Microbiology 152: 2703-2716.
17. Breton M, Duret S, Danet JL, Dubrana MP, Renaudin J, (2010) Sequences essential for transmission of Spiroplasma citri by its leafhopper vector, Circulifer haematoceps, revealed by plasmid curing and replacement based on incompatibility. Appl Environ Microbiol 76: 3198-3205.
18. Berg M, Melcher U, Fletcher J, (2001) Characterization of Spiroplasma citri adhesion related protein SARP1, which contains a domain of a novel family designated sarpin. Gene 275: 57-64.
19. Yu J, Wayadande AC, Fletcher J, (2000) Spiroplasma citri surface protein P89 implicated in adhesion to cells of the vector Circulifer tenellus. Phytopathology 90: 716-722.
20. Fleury B, Bergonier D, Berthelot X, Peterhans E, Frey J, et al. (2002) Characterization of P40, a cytadhesin of Mycoplasma agalactiae. Infect Immun 70: 5612-5621.
21. Vignault JC, Bové JM, Saillard C, Vogel R, Farro A, et al. (1980) Mise en culture de spiroplasmes à partir de matériel végétal et d'insectes provenant de pays circum méditerranéens et du Proche Orient. C R Acad Sci Ser III 290: 775-780.
22. Tully JG, Whitcomb RF, Clark HF, Williamson DL, (1977) Pathogenic mycoplasma: cultivation and vertebrate pathogenicity of a new spiroplasma. Science 195: 892-894.
23. Labroussaa F, Arricau-Bouvery N, Dubrana M-P, Saillard C, (2010) Entry of Spiroplasma citri into Circulifer haematoceps cells involves interaction between spiroplasma phosphoglycerate kinase and leafhopper actin Appl Environ Microbiol. 76: 1879-1886.
24. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
25. Wroblewski H, Johansson KE, Hjérten S, (1977) Purification and characterization of spiralin, the main protein of the Spiroplasma citri membrane. Biochim Biophys Acta 465: 275-289.
26. Davis RE, Dally EL, Jomantiene R, Zhao Y, Roe B, et al. (2005) Cryptic plasmid pSKU146 from the wall-less plant pathogen Spiroplasma kunkelii encodes an adhesin and components of a type IV translocation-related conjugation system. Plasmid 53: 179-190.
27. Breton M, Duret S, Arricau-Bouvery N, Béven L, Renaudin J, (2008) Characterizing the replication and stability regions of Spiroplasma citri plasmids identifies a novel replication protein and expands the genetic toolbox for plant pathogenic spiroplasmas. Microbiology 154: 3232-3244.
28. Alexeev D, Kostrjukova E, Aliper A, Popenko A, Bazaleev N, et al. (2012) Application of Spiroplasma melliferum proteogenomic profiling for the discovery of virulence factors and pathogenicity mechanisms in host-associated spiroplasmas. J Proteome Res 11: 224-236.
29. Dramsi S, Dehoux P, Cossart P, (1993) Common features of gram-positive bacterial proteins involved in cell recognition. Mol Microbiol 9: 1119-1121.
30. Minion FC, Adams C, Hsu T, (2000) R1 region of P97 mediates adherence of Mycoplasma hyopneumoniae to swine cilia. Infect Immun 68: 3056-3060.
31. Cote JP, Mourez M, (2011) Structure-function analysis of the TibA self-associating autotransporter reveals a modular organization. Infect Immun 79: 1826-1832.
32. Castano S, Blaudez D, Desbat B, Dufourcq J, Wroblewski H, (2002) Secondary structure of spiralin in solution, at the air/water interface, and its interaction with lipid monolayers. Biochim Biophys Acta 1562: 45-56.
33. Fletcher J, Wills JW, Denman SE, (1989) Identification of surface-proteins of Spiroplasma citri with protease and antibody probes. Curr Microbiol 19: 383-391.
34. Lecuit M, Ohayon H, Braun L, Mengaud J, Cossart P, (1997) Internalin of Listeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization. Infect Immun 65: 5309-5319.
35. Sun JN, Solis NV, Phan QT, Bajwa JS, Kashleva H, et al. (2010) Host cell invasion and virulence mediated by Candida albicans Ssa1. PLoS Pathog 6: e1001181.
36. Vadia S, Arnett E, Haghighat AC, Wilson-Kubalek EM, Tweten RK, et al. (2011) The pore-forming toxin listeriolysin O mediates a novel entry pathway of L. monocytogenes into human hepatocytes. PLoS Pathog 7: e1002356.
37. McKee ML, O'Brien AD, (1996) Truncated enterohemorrhagic Escherichia coli (EHEC) O157: H7 intimin (EaeA) fusion proteins promote adherence of EHEC strains to HEp-2 cells. Infect Immun 64: 2225-2233.
38. Wang H, Min G, Glockshuber R, Sun TT, Kong XP, (2009) Uropathogenic E. coli adhesin-induced host cell receptor conformational changes: implications in transmembrane signaling transduction. J Mol Biol 392: 352-361.
39. Thumbikat P, Berry RE, Zhou G, Billips BK, Yaggie RE, et al. (2009) Bacteria-induced uroplakin signaling mediates bladder response to infection. PLoS Pathog 5: e1000415.
40. Baker RP, Wijetilaka R, Urban S, (2006) Two Plasmodium rhomboid proteases preferentially cleave different adhesins implicated in all invasive stages of malaria. PLoS Pathog 2: e113.
41. Dersch P, Isberg RR, (2000) An immunoglobulin superfamily-like domain unique to the Yersinia pseudotuberculosis invasin protein is required for stimulation of bacterial uptake via integrin receptors. Infect Immun 68: 2930-2938.
42. Wells CL, van de Westerlo EM, Jechorek RP, Haines HM, Erlandsen SL, (1998) Cytochalasin-induced actin disruption of polarized enterocytes can augment internalization of bacteria. Infect Immun 66: 2410-2419.
43. Murai M, Seki K, Sakurada J, Usui A, Masuda S, (1993) Effects of cytochalasins B and D on Staphylococcus aureus adherence to and ingestion by mouse renal cells from primary culture. Microbiol Immunol 37: 69-73.
44. Burnett TA, Dinkla K, Rohde M, Chhatwal GS, Uphoff C, et al. (2006) P159 is a proteolytically processed, surface adhesin of Mycoplasma hyopneumoniae: defined domains of P159 bind heparin and promote adherence to eukaryote cells. Mol Microbiol 60: 669-686.
45. Zhang Q, Young TF, Ross RF, (1995) Identification and characterization of a Mycoplasma hyopneumoniae adhesin. Infect Immun 63: 1013-1019.
46. Wilton J, Jenkins C, Cordwell SJ, Falconer L, Minion FC, et al. (2009) Mhp493 (P216) is a proteolytically processed, cilium and heparin binding protein of Mycoplasma hyopneumoniae. Mol Microbiol 71: 566-582.
47. Deutscher AT, Tacchi JL, Minion FC, Padula MP, Crossett B, et al. (2012) Mycoplasma hyopneumoniae surface proteins Mhp385 and Mhp384 bind host cilia and glycosaminoglycans and are endoproteolytically processed by proteases that recognize different cleavage motifs. J Proteome Res 11: 1924-1936.
48. Killiny N, Castroviejo M, Saillard C, (2005) Spiroplasma citri spiralin acts in vitro as a lectin binding to glycoproteins from its insect vector Circulifer haematoceps. Phytopathology 95: 541-548.
49. Veiga E, Cossart P, (2006) The role of clathrin-dependent endocytosis in bacterial internalization. Trends Cell Biol 16: 499-504.
50. Marchler-Bauer A, Bryant SH, (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32: 327-331.