A Potential Role for the Interaction of Wolbachia Surface Proteins with the Brugia malayi Glycolytic Enzymes and Cytoskeleton in Maintenance of Endosymbiosis

PLoS Neglected Tropical Diseases

Volumn 7, Issue 4, 2013, Pages

  Melnikow, Elena ^a   Xu, Shulin ^b   Liu, Jing ^a   Bell, Aaron J ^a   Ghedin, Elodie ^c   Unnasch, Thomas R ^b   Lustigman, Sara ^a  

^a NEW YORK BLOOD CENTER   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ENOLASE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLYCOLYTIC ENZYME; MEMBRANE PROTEIN; TUBULIN;

ANIMAL EXPERIMENT; ANTIBODY AFFINITY; ARTICLE; BRUGIA MALAYI; ENDOSYMBIOSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HOST PARASITE INTERACTION; IMMUNOELECTRON MICROSCOPY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; WOLBACHIA;

EID: 84876869486     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002151     Document Type: Article

References (80)

1. Brattig NW, (2004) Pathogenesis and host responses in human onchocerciasis: impact of Onchocerca filariae and Wolbachia endobacteria. Microbes Infect 6: 113-128.
2. Shenoy RK, Suma TK, Kumaraswami V, Dhananjayan G, Rahmah N, et al. (2008) Lymphoscintigraphic evidence of lymph vessel dilation in the limbs of children with Brugia malayi infection. J Commun Dis 40: 91-100.
3. Taylor MJ, Hoerauf A, Bockarie M, (2010) Lymphatic filariasis and onchocerciasis. Lancet 376: 1175-1185.
4. Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, et al. (2008) Helminth infections: the great neglected tropical diseases. J Clin Invest 118: 1311-1321.
5. Molyneux DH, Bradley M, Hoerauf A, Kyelem D, Taylor MJ, (2003) Mass drug treatment for lymphatic filariasis and onchocerciasis. Trends Parasitol 19: 516-522.
6. Molyneux DH, Malecela MN, (2011) Neglected Tropical Diseases and the Millennium Development Goals- why the "other diseases" matter: reality versus rhetoric. Parasit Vectors 4: 234.
7. Ottesen EA, Hooper PJ, Bradley M, Biswas G, (2008) The global programme to eliminate lymphatic filariasis: health impact after 8 years. PLoS Negl Trop Dis 2: e317.
8. Prichard RK, Basáñez MG, Boatin B, McCarthy J, Garcia HH, et al. (2012) A research agenda for helminth diseases of humans: Intervention for control andelimination. PLoS Negl Trop Dis 6: e1549.
9. WHO (2010) Global programme to eliminate lymphatic filariasis. Wkly Epidemiol Rec 85: 365-372.
10. Werren JH, Baldo L, Clark ME, (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741-751.
11. Kozek WJ, (2005) What is new in the Wolbachia/Dirofilaria interaction? Vet Parasitol 133: 127-132.
12. Bandi C, Anderson TJ, Genchi C, Blaxter ML, (1998) Phylogeny of Wolbachia in filarial nematodes. Proc Biol Sci 265: 2407-2413.
13. Bandi C, Trees AJ, Brattig NW, (2001) Wolbachia in filarial nematodes: evolutionary aspects and implications for the pathogenesis and treatment of filarial diseases. Vet Parasitol 98: 215-238.
14. Bandi CT, Anderson JC (2001) The Wolbachia endosymbionts of filarial nematodes; Kennedy MW, Harnett W, editors. Wallingford, Oxon, United Kingdom: CAB International. 25-43 p.
15. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, et al. (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139: 1268-1278.
16. Ghedin E, Wang S, Spiro D, Caler E, Zhao Q, et al. (2007) Draft genome of the filarial nematode parasite Brugia malayi. Science 317: 1756-1760.
17. Foster J, Ganatra M, Kamal I, Ware J, Makarova K, et al. (2005) The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol 3: e121.
18. Slatko BE, Taylor MJ, Foster JM, (2010) The Wolbachia endosymbiont as an anti-filarial nematode target. Symbiosis 51: 55-65.
19. Wu B, Novelli J, Foster J, Vaisvila R, Conway L, et al. (2009) The heme biosynthetic pathway of the obligate Wolbachia endosymbiont of Brugia malayi as a potential anti-filarial drug target. PLoS Negl Trop Dis 3: e475.
20. Ghedin E, Daehnel K, Foster J, Slatko B, Lustigman S, (2008) The symbiotic relationship between filarial parasitic nematodes and their Wolbachia endosymbionts- a resource for a new generation of control measures. Symbiosis 46: 77-85.
21. Townson S, Hutton D, Siemienska J, Hollick L, Scanlon T, et al. (2000) Antibiotics and Wolbachia in filarial nematodes: antifilarial activity of rifampicin, oxytetracycline and chloramphenicol against Onchocerca gutturosa, Onchocerca lienalis and Brugia pahangi. Ann Trop Med Parasitol 94: 801-816.
22. Landmann F, Voronin D, Sullivan W, Taylor MJ, (2011) Anti-filarial activity of antibiotic therapy is due to extensive apoptosis after Wolbachia depletion from filarial nematodes. PLoS Pathogens 7: e1002351.
23. Hoerauf A, (2008) Filariasis: new drugs and new opportunities for lymphatic filariasis and onchocerciasis. Curr Opin Infect Dis 21: 673-681.
24. Hoerauf A, Specht S, Buttner M, Pfarr K, Mand S, et al. (2008) Wolbachia endobacteria depletion by doxycycline as antifilarial therapy has macrofilaricidal activity in onchocerciasis: a randomized placebo-controlled study. Med Microbiol Immunol 197: 295-311.
25. Rao RU, Huang Y, Abubucker S, Heinz M, Crosby SD, et al. (2012) Effects of Doxycycline on gene expression in Wolbachia and Brugia malayi adult female worms in vivo. J Biomed Sci 19: 21.
26. Bazzocchi C, Mortarino M, Grandi G, Kramer LH, Genchi C, et al. (2008) Combined ivermectin and doxycycline treatment has microfilaricidal and adulticidal activity against Dirofilaria immitis in experimentally infected dogs. Int J Parasitol 38: 1401-1410.
27. Mand S, Pfarr K, Sahoo PK, Satapathy AK, Specht S, et al. (2009) Macrofilaricidal activity and amelioration of lymphatic pathology in bancroftian filariasis after 3 weeks of doxycycline followed by single-dose diethylcarbamazine. Am J Trop Med Hyg 81: 702-711.
28. Specht S, Mand S, Marfo-Debrekyei Y, Debrah AY, Konadu P, et al. (2008) Efficacy of 2- and 4-week rifampicin treatment on the Wolbachia of Onchocerca volvulus. Parasitol Res 103: 1303-1309.
29. Specht S, Wanji S, (2009) New insights into the biology of filarial infections. J Helminthol 83: 199-202.
30. Supali T, Djuardi Y, Pfarr KM, Wibowo H, Taylor MJ, et al. (2008) Doxycycline treatment of Brugia malayi-infected persons reduces microfilaremia and adverse reactions after diethylcarbamazine and albendazole treatment. Clin Infect Dis 46: 1385-1393.
31. Hoerauf A, Nissen-Pahle K, Schmetz C, Henkle-Duhrsen K, Blaxter ML, et al. (1999) Tetracycline therapy targets intracellular bacteria in the filarial nematode Litomosoides sigmodontis and results in filarial infertility. J Clin Invest 103: 11-18.
32. Bandi C, McCall JW, Genchi C, Corona S, Venco L, et al. (1999) Effects of tetracycline on the filarial worms Brugia pahangi and Dirofilaria immitis and their bacterial endosymbionts Wolbachia. Int J Parasitol 29: 357-364.
33. Langworthy NG, Renz A, Mackenstedt U, Henkle-Duhrsen K, de Bronsvoort MB, et al. (2000) Macrofilaricidal activity of tetracycline against the filarial nematode Onchocerca ochengi: elimination of Wolbachia precedes worm death and suggests a dependent relationship. Proc Biol Sci 267: 1063-1069.
34. Taylor MJ, (2000) Wolbachia bacteria of filarial nematodes in the pathogenesis of disease and as a target for control. Trans R Soc Trop Med Hyg 94: 596-598.
35. Taylor MJ, Bandi C, Hoerauf A, (2005) Wolbachia bacterial endosymbionts of filarial nematodes. Adv Parasitol 60: 245-284.
36. Baldo L, Desjardins CA, Russell JA, Stahlhut JK, Werren JH, (2010) Accelerated microevolution in an outer membrane protein (OMP) of the intracellular bacteria Wolbachia. BMC Evol Biol 10: 48.
37. Baldo L, Lo N, Werren JH, (2005) Mosaic nature of the wolbachia surface protein. J Bacteriol 187: 5406-5418.
38. Braig HR, Zhou W, Dobson SL, O'Neill SL, (1998) Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J Bacteriol 180: 2373-2378.
39. Serbus LR, Casper-Lindley C, Landmann F, Sullivan W, (2008) The genetics and cell biology of Wolbachia-host interactions. Annu Rev Genet 42: 683-707.
40. Bennuru S, Semnani R, Meng Z, Ribeiro JM, Veenstra TD, et al. (2009) Brugia malayi excreted/secreted proteins at the host/parasite interface: stage- and gender-specific proteomic profiling. PLoS Negl Trop Dis 3: e410.
41. Melnikow E, Xu S, Liu J, Li L, Oksov Y, et al. (2011) Interaction of a Wolbachia WSP-like protein with a nuclear-encoded protein of Brugia malayi. Int J Parasitol 41: 1053-1061.
42. Turner JD, Langley RS, Johnston KL, Egerton G, Wanji S, et al. (2006) Wolbachia endosymbiotic bacteria of Brugia malayi mediate macrophage tolerance to TLR- and CD40-specific stimuli in a MyD88/TLR2-dependent manner. J Immunol 177: 1240-1249.
43. Wisniewski JR, Zougman A, Nagaraj N, Mann M, (2009) Universal sample preparation method for proteome analysis. Nat Methods 6: 359-362.
44. Kim JH, Lee S, Lee TG, Hirata M, Suh PG, et al. (2002) Phospholipase D2 directly interacts with aldolase via Its PH domain. Biochemistry 41: 3414-3421.
45. Lustigman S, Brotman B, Huima T, Prince AM, (1991) Characterization of an Onchocerca volvulus cDNA clone encoding a genus specific antigen present in infective larvae and adult worms. Mol Biochem Parasitol 45: 65-75.
46. McLaren DJ, Worms MJ, Laurence BR, Simpson MG, (1975) Micro-organisms in filarial larvae (Nematoda). Trans R Soc Trop Med Hyg 69: 509-514.
47. Kool J, Jonker N, Irth H, Niessen WM, (2011) Studying protein-protein affinity and immobilized ligand-protein affinity interactions using MS-based methods. Anal Bioanal Chem 401: 1109-1125.
48. Bonk T, Humeny A, (2001) MALDI-TOF-MS analysis of protein and DNA. Neuroscientist 7: 6-12.
49. Waingeh VF, Gustafson CD, Kozliak EI, Lowe SL, Knull HR, et al. (2006) Glycolytic enzyme interactions with yeast and skeletal muscle F-actin. Biophys J 90: 1371-1384.
50. McGarry HF, Egerton GL, Taylor MJ, (2004) Population dynamics of Wolbachia bacterial endosymbionts in Brugia malayi. Mol Biochem Parasitol 135: 57-67.
51. Jewett TJ, Sibley LD, (2003) Aldolase forms a bridge between cell surface adhesins and the actin cytoskeleton in apicomplexan parasites. Mol Cell 11: 885-894.
52. Wang SH, Zheng HJ, Dissanayake S, Cheng WF, Tao ZH, et al. (1997) Evaluation of recombinant chitinase and SXP1 antigens as antimicrofilarial vaccines. Am J Trop Med Hyg 56: 474-481.
53. Schindler R, Weichselsdorfer E, Wagner O, Bereiter-Hahn J, (2001) Aldolase-localization in cultured cells: cell-type and substrate-specific regulation of cytoskeletal associations. Biochem Cell Biol 79: 719-728.
54. Casiraghi M, McCall JW, Simoncini L, Kramer LH, Sacchi L, et al. (2002) Tetracycline treatment and sex-ratio distortion: a role for Wolbachia in the moulting of filarial nematodes? Int J Parasitol 32: 1457-1468.
55. Ferri E, Bain O, Barbuto M, Martin C, Lo N, et al. (2011) New insights into the evolution of wolbachia infections in filarial nematodes inferred from a large range of screened species. PLoS One 6: e20843.
56. Landmann F, Bain O, Martin C, Uni S, Taylor MJ, et al. (2012) Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of Wolbachia in filarial nematodes. Biology open 1: 536-547.
57. Darby AC, Armstrong SD, Bah GS, Kaur G, Hughes MA, et al. (2012) Analysis of gene expression from the Wolbachia genome of a filarial nematode supports both metabolic and defensive roles within the symbiosis. Genome Res 22: 2467-77.
58. Ferree PM, Frydman HM, Li JM, Cao J, Wieschaus E, et al. (2005) Wolbachia utilizes host microtubules and Dynein for anterior localization in the Drosophila oocyte. PLoS Pathog 1: e14.
59. Galan JE, Cossart P, (2005) Host-pathogen interactions: a diversity of themes, a variety of molecular machines. Curr Opin Microbiol 8: 1-3.
60. Heinzen RA, Grieshaber SS, Van Kirk LS, Devin CJ, (1999) Dynamics of actin-based movement by Rickettsia rickettsii in vero cells. Infect Immun 67: 4201-4207.
61. Callaini G, Riparbelli MG, Dallai R, (1994) The distribution of cytoplasmic bacteria in the early Drosophila embryo is mediated by astral microtubules. J Cell Sci 107 (Pt 3) (): 673-682.
62. Gouin E, Welch MD, Cossart P, (2005) Actin-based motility of intracellular pathogens. Curr Opin Microbiol 8: 35-45.
63. Kose H, Karr TL, (1995) Organization of Wolbachia pipientis in the Drosophila fertilized egg and embryo revealed by an anti-Wolbachia monoclonal antibody. Mech Dev 51: 275-288.
64. Tilney LG, DeRosier DJ, Tilney MS, (1992) How Listeria exploits host cell actin to form its own cytoskeleton. I. Formation of a tail and how that tail might be involved in movement. J Cell Biol 118: 71-81.
65. Landmann F, Foster JM, Slatko B, Sullivan W, (2010) Asymmetric Wolbachia segregation during early Brugia malayi embryogenesis determines its distribution in adult host tissues. PLoS Negl Trop Dis 4: e758.
66. Turner JD, Langley RS, Johnston KL, Gentil K, Ford L, et al. (2009) Wolbachia lipoprotein stimulates innate and adaptive immunity through Toll-like receptors 2 and 6 to induce disease manifestations of filariasis. J Biol Chem 284: 22364-22378.
67. Dudkina NV, Voronin DA, Kiseleva EV, (2004) Structural organization and distribution of symbiotic bacteria Wolbachia in early embryos and ovaries of Drosophila melanogaster and D. simulans. Tsitologiia 46: 208-220.
68. Aboobaker AA, Blaxter ML, (2003) Use of RNA interference to investigate gene function in the human filarial nematode parasite Brugia malayi. Mol Biochem Parasitol 129: 41-51.
69. Kotze AC, Bagnall NH, (2006) RNA interference in Haemonchus contortus: suppression of beta-tubulin gene expression in L3, L4 and adult worms in vitro. Mol Biochem Parasitol 145: 101-110.
70. Landmann F, Foster JM, Slatko BE, Sullivan W, (2012) Efficient in vitro RNA interference and immunofluorescence-based phenotype analysis in a human parasitic nematode, Brugia malayi. Parasit Vectors 5: 16.
71. Pfarr K, Heider U, Hoerauf A, (2006) RNAi mediated silencing of actin expression in adult Litomosoides sigmodontis is specific, persistent and results in a phenotype. Int J Parasitol 36: 661-669.
72. Campanella ME, Chu H, Low PS, (2005) Assembly and regulation of a glycolytic enzyme complex on the human erythrocyte membrane. Proc Natl Acad Sci U S A 102: 2402-2407.
73. Campanella ME, Chu H, Wandersee NJ, Peters LL, Mohandas N, et al. (2008) Characterization of glycolytic enzyme interactions with murine erythrocyte membranes in wild-type and membrane protein knockout mice. Blood 112: 3900-3906.
74. Walsh JL, Keith TJ, Knull HR, (1989) Glycolytic enzyme interactions with tubulin and microtubules. Biochim Biophys Acta 999: 64-70.
75. Keller A, Peltzer J, Carpentier G, Horvath I, Olah J, et al. (2007) Interactions of enolase isoforms with tubulin and microtubules during myogenesis. Biochim Biophys Acta 1770: 919-926.
76. Walsh TP, Clarke FM, Masters CJ, (1977) Modification of the kinetic parameters of aldolase on binding to the actin-containing filaments of skeletal muscle. Biochem J 165: 165-167.
77. Wang J, Tolan DR, Pagliaro L, (1997) Metabolic compartmentation in living cells: structural association of aldolase. Exp Cell Res 237: 445-451.
78. Bosch J, Buscaglia CA, Krumm B, Ingason BP, Lucas R, et al. (2007) Aldolase provides an unusual binding site for thrombospondin-related anonymous protein in the invasion machinery of the malaria parasite. Proc Natl Acad Sci U S A 104: 7015-7020.
79. Pomel S, Luk FC, Beckers CJ, (2008) Host cell egress and invasion induce marked relocations of glycolytic enzymes in Toxoplasma gondii tachyzoites. PLoS Pathog 4: e1000188.
80. Darby AC, Armstrong SD, Bah GS, Kaur G, Hughes MA, et al. (2012) Analysis of gene expression from the Wolbachia genome of a filarial nematode supports both metabolic and defensive roles within the symbiosis. Genome Research 22: 2467-2477.