Shear forces enhance Toxoplasma gondii tachyzoite motility on vascular endothelium

mBio

Volumn 5, Issue 2, 2014, Pages

  Harker, Katherine S ^a,b   Jivan, Elizabeth ^a,b   McWhorter, Frances Y ^a,c   Liu, Wendy F ^a,c   Lodoen, Melissa B ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c University of California at Irvine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PROTEIN MIC2; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; MICROFLUIDIC ANALYSIS; NONHUMAN; PARASITE MIGRATION; PARASITE TRANSMISSION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SHEAR FLOW; SHEAR STRESS; TACHYZOITE; TOXOPLASMA GONDII; VASCULAR ENDOTHELIUM;

CELL ADHESION; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; HOST-PARASITE INTERACTIONS; HUMANS; LOCOMOTION; MICROFLUIDICS; TIME-LAPSE IMAGING; TOXOPLASMA;

EID: 84899850161     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01111-13     Document Type: Article

References (60)

1. Montoya JG, Liesenfeld O. 2004. Toxoplasmosis. Lancet 363:1965-1976. http://dx.doi.org/10.1016/S0140-6736(04)16412-X.
2. Dubey JP, Speer CA, Shen SK, Kwok OC, Blixt JA. 1997. Oocystinduced murine toxoplasmosis: life cycle, pathogenicity, and stage conversion in mice fed Toxoplasma gondii oocysts. J. Parasitol. 83:870-882. http://dx.doi.org/10.2307/3284282.
3. Lambert H, Barragan A. 2010. Modelling parasite dissemination: host cell subversion and immune evasion by Toxoplasma gondii. Cell. Microbiol. 12:292-300. http://dx.doi.org/10.1111/j.1462-5822.2009.01417.x.
4. Dubey JP. 1997. Tissue cyst tropism in Toxoplasma gondii: a comparison of tissue cyst formation in organs of cats, and rodents fed oocysts. Parasitology 115:15-20. http://dx.doi.org/10.1017/S0031182097008949.
5. Courret N, Darche S, Sonigo P, Milon G, Buzoni-Gâtel D, Tardieux I. 2006. CD11c+ and CD11b-expressing mouse leukocytes transport single Toxoplasma gondii tachyzoites to the brain. Blood 107:309-316. http:// dx.doi.org/10.1182/blood-2005-02-0666.
6. Lambert H, Hitziger N, Dellacasa I, Svensson M, Barragan A. 2006. Induction of dendritic cell migration upon Toxoplasma gondii infection potentiates parasite dissemination. Cell. Microbiol. 8:1611-1623. http:// dx.doi.org/10.1111/j.1462-5822.2006.00735.x.
7. Lambert H, Dellacasa-Lindberg I, Barragan A. 2011. Migratory responses of leukocytes infected with Toxoplasma gondii. Microbes Infect. 13:96-102. http://dx.doi.org/10.1016/j.micinf.2010.10.002.
8. Harker KS, Ueno N, Wang T, Bonhomme C, Liu W, Lodoen MB. 2013. Toxoplasma gondii modulates the dynamics of human monocyte adhesion to vascular endothelium under fluidic shear stress. J. Leukoc. Biol. 93: 789-800. http://dx.doi.org/10.1189/jlb.1012517.
9. Ueno N, Harker KS, Clarke EV, McWhorter FY, Liu WF, Tenner AJ, Lodoen MB. 2014. Real-time imaging of Toxoplasma-infected human monocytes under fluidic shear stress reveals rapid translocation of intracellular parasites across endothelial barriers. Cell. Microbiol. 16(4): 580-595. http://dx.doi.org/10.1111/cmi.12239.
10. Silveira C, Vallochi AL, Rodrigues da Silva U, Muccioli C, Holland GN, Nussenblatt RB, Belfort R, Rizzo LV. 2011. Toxoplasma gondii in the peripheral blood of patients with acute and chronic toxoplasmosis. Br. J. Ophthalmol. 95:396-400. http://dx.doi.org/10.1136/bjo.2008.148205.
11. Barragan A, Sibley LD. 2002. Transepithelial migration of Toxoplasma gondii is linked to parasite motility and virulence. J. Exp. Med. 195: 1625-1633. http://dx.doi.org/10.1084/jem.20020258.
12. Furtado JM, Bharadwaj AS, Chipps TJ, Pan Y, Ashander LM, Smith JR. 2012. Toxoplasma gondii tachyzoites cross retinal endothelium assisted by intercellular adhesion molecule-1 in vitro. Immunol. Cell Biol. 90: 912-915.
13. Sibley LD. 2010. How apicomplexan parasites move in and out of cells. Curr. Opin. Biotechnol. 21:592-598. http://dx.doi.org/10.1016/ j.copbio.2010.05.009.
14. 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. http://dx.doi.org/10.1016/S1097-2765(03)00113-8.
15. Dobrowolski JM, Sibley LD. 1996. Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84:933-939. http://dx.doi.org/10.1016/S0092-8674(00)81071-5.
16. Dobrowolski JM, Niesman IR, Sibley LD. 1997. Actin in the parasite Toxoplasma gondii is encoded by a single copy gene, ACT1 and exists primarily in a globular form. Cell Motil. Cytoskeleton 37:253-262. http:// dx.doi.org/10.1002/(SICI)1097-0169(1997)37:3 253::AIDCM7 _3.0.CO;2-7.
17. Håkansson S, Morisaki H, Heuser J, Sibley LD. 1999. Time-lapse video microscopy of gliding motility in Toxoplasma gondii reveals a novel, biphasic mechanism of cell locomotion. Mol. Biol. Cell 10:3539-3547. http://dx.doi.org/10.1091/mbc.10.11.3539.
18. Frixione E, Mondragón R, Meza I. 1996. Kinematic analysis of Toxoplasma gondii motility. Cell Motil. Cytoskeleton 34:152-163. http:// dx.doi.org/10.1002/(SICI)1097-0169(1996)34:2 152::AIDCM6 _3.3.CO;2-5.
19. Ménard R. 2001. Gliding motility and cell invasion by Apicomplexa: insights from the Plasmodium sporozoite. Cell. Microbiol. 3:63-73. http://dx.doi.org/10.1046/j.1462-5822.2001.00097.x.
20. Wetzel DM, Schmidt J, Kuhlenschmidt MS, Dubey JP, Sibley LD. 2005. Gliding motility leads to active cellular invasion by Cryptosporidium parvum sporozoites. Infect. Immun. 73:5379-5387. http://dx.doi.org/ 10.1128/IAI.73.9.5379-5387.2005.
21. Huynh MH, Carruthers VB. 2006. Toxoplasma MIC2 is a major determinant of invasion and virulence. PLoS Pathog. 2:e84. http://dx.doi.org/ 10.1371/journal.ppat.0020084.
22. Wetzel DM, Håkansson S, Hu K, Roos D, Sibley LD. 2003. Actin filament polymerization regulates gliding motility by apicomplexan parasites. Mol. Biol. Cell 14:396-406. http://dx.doi.org/10.1091/mbc.E02-08-0458.
23. Papaioannou TG, Stefanadis C. 2005. Vascular wall shear stress: basic principles and methods. Hellenic J. Cardiol. 46:9-15.
24. Alon R, Feigelson SW, Manevich E, Rose DM, Schmitz J, Overby DR, Winter E, Grabovsky V, Shinder V, Matthews BD, Sokolovsky-Eisenberg M, Ingber DE, Benoit M, Ginsberg MH. 2005. α4β1-dependent adhesion strengthening under mechanical strain is regulated by paxillin association with the α4-cytoplasmic domain. J. Cell Biol. 171: 1073-1084. http://dx.doi.org/10.1083/jcb.200503155.
25. Taubert A, Krüll M, Zahner H, Hermosilla C. 2006. Toxoplasma gondii and Neospora caninum infections of bovine endothelial cells induce endothelial adhesion molecule gene transcription and subsequent PMN adhesion. Vet. Immunol. Immunopathol. 112:272-283. http://dx.doi.org/ 10.1016/j.vetimm.2006.03.017.
26. Fischer HG, Stachelhaus S, Sahm M, Meyer HE, Reichmann G. 1998. GRA7, an excretory 29 kDa Toxoplasma gondii dense granule antigen released by infected host cells. Mol. Biochem. Parasitol. 91:251-262. http:// dx.doi.org/10.1016/S0166-6851(97)00227-2.
27. Wan KL, Carruthers VB, Sibley LD, Ajioka JW. 1997. Molecular characterisation of an expressed sequence tag locus of Toxoplasma gondii encoding the micronemal protein MIC2. Mol. Biochem. Parasitol. 84: 203-214. http://dx.doi.org/10.1016/S0166-6851(96)02796-X.
28. Carruthers VB, Sherman GD, Sibley LD. 2000. The toxoplasma adhesive protein MIC2 is proteolytically processed at multiple sites by two parasitederived proteases. J. Biol. Chem. 275:14346-14353. http://dx.doi.org/ 10.1074/jbc.275.19.14346.
29. Huynh MH, Rabenau KE, Harper JM, Beatty WL, Sibley LD, Carruthers VB. 2003. Rapid invasion of host cells by Toxoplasma requires secretion of the MIC2-M2AP adhesive protein complex. EMBO J. 22: 2082-2090. http://dx.doi.org/10.1093/emboj/cdg217.
30. Barragan A, Brossier F, Sibley LD. 2005. Transepithelial migration of Toxoplasma gondii involves an interaction of intercellular adhesion molecule 1 (ICAM-1) with the parasite adhesin MIC2. Cell. Microbiol. 7:561-568. http://dx.doi.org/10.1111/j.1462-5822.2005.00486.x.
31. Leung JM, Rould MA, Konradt C, Hunter CA, Ward GE. 2014. Disruption of TgPHIL1 alters specific parameters of Toxoplasma gondii motility measured in a quantitative, three-dimensional live motility assay. PLoS One 9:e85763. http://dx.doi.org/10.1371/journal.pone.0085763.
32. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. 2007. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7:678-689. http://dx.doi.org/10.1038/nri2156.
33. Hegge S, Münter S, Steinbüchel M, Heiss K, Engel U, Matuschewski K, Frischknecht F. 2010. Multistep adhesion of Plasmodium sporozoites. FASEB J. 24:2222-2234. http://dx.doi.org/10.1096/fj.09-148700.
34. Moriarty TJ, Shi M, Lin YP, Ebady R, Zhou H, Odisho T, Hardy PO, Salman-Dilgimen A, Wu J, Weening EH, Skare JT, Kubes P, Leong J, Chaconas G. 2012. Vascular binding of a pathogen under shear force through mechanistically distinct sequential interactions with host macromolecules. Mol. Microbiol. 86:1116-1131. http://dx.doi.org/10.1111/ mmi.12045.
35. Moriarty TJ, Norman MU, Colarusso P, Bankhead T, Kubes P, Chaconas G. 2008. Real-time high resolution 3D imaging of the Lyme disease spirochete adhering to and escaping from the vasculature of a living host. PLoS Pathog. 4:e1000090. http://dx.doi.org/10.1371/ journal.ppat.1000090.
36. Tardieux I, Ménard R. 2008. Migration of Apicomplexa across biological barriers: the Toxoplasma and Plasmodium rides. Traffic 9:627-635. http://dx.doi.org/10.1111/j.1600-0854.2008.00703.x.
37. Carruthers VB, Sibley LD. 1999. Mobilization of intracellular calcium stimulates microneme discharge in Toxoplasma gondii. Mol. Microbiol. 31:421-428. http://dx.doi.org/10.1046/j.1365-2958.1999.01174.x.
38. Wetzel DM, Chen LA, Ruiz FA, Moreno SN, Sibley LD. 2004. Calciummediated protein secretion potentiates motility in Toxoplasma gondii. J. Cell Sci. 117:5739-5748. http://dx.doi.org/10.1242/jcs.01495.
39. Fruth IA, Arrizabalaga G. 2007. Toxoplasma gondii: Induction of egress by the potassium ionophore nigericin. Int. J. Parasitol. 37:1559-1567. http://dx.doi.org/10.1016/j.ijpara.2007.05.010.
40. Carruthers VB, Håkansson S, Giddings OK, Sibley LD. 2000. Toxoplasma gondii uses sulfated proteoglycans for substrate and host cell attachment. Infect. Immun. 68:4005-4011. http://dx.doi.org/10.1128/ IAI.68.7.4005-4011.2000.
41. Soldati D, Dubremetz JF, Lebrun M. 2001. Microneme proteins: structural and functional requirements to promote adhesion and invasion by the apicomplexan parasite Toxoplasma gondii. Int. J. Parasitol. 31: 1293-1302. http://dx.doi.org/10.1016/S0020-7519(01)00257-0.
42. Friedrich N, Santos JM, Liu Y, Palma AS, Leon E, Saouros S, Kiso M, Blackman MJ, Matthews S, Feizi T, Soldati-Favre D. 2010. Members of a novel protein family containing microneme adhesive repeat domains act as sialic acid-binding lectins during host cell invasion by apicomplexan parasites. J. Biol. Chem. 285:2064-2076. http://dx.doi.org/10.1074/ jbc.M109.060988.
43. Blumenschein TM, Friedrich N, Childs RA, Saouros S, Carpenter EP, Campanero-Rhodes MA, Simpson P, Chai W, Koutroukides T, Blackman MJ, Feizi T, Soldati-Favre D, Matthews S. 2007. Atomic resolution insight into host cell recognition by Toxoplasma gondii. EMBO J. 26: 2808-2820. http://dx.doi.org/10.1038/sj.emboj.7601704.
44. Garcia-Réguet N, Lebrun M, Fourmaux MN, Mercereau-Puijalon O, Mann T, Beckers CJ, Samyn B, Van Beeumen J, Bout D, Dubremetz JF. 2000. The microneme protein MIC3 of Toxoplasma gondii is a secretory adhesin that binds to both the surface of the host cells and the surface of the parasite. Cell. Microbiol. 2:353-364. http://dx.doi.org/10.1046/j.1462-5822.2000.00064.x.
45. Cérède O, Dubremetz JF, Soête M, Deslée D, Vial H, Bout D, Lebrun M. 2005. Synergistic role of micronemal proteins in Toxoplasma gondii virulence. J. Exp. Med. 201:453-463. http://dx.doi.org/10.1084/ jem.20041672.
46. Jacquet A, Coulon L, De Nève J, Daminet V, Haumont M, Garcia L, Bollen A, Jurado M, Biemans R. 2001. The surface antigen SAG3 mediates the attachment of Toxoplasma gondii to cell-surface proteoglycans. Mol. Biochem. Parasitol. 116:35-44. http://dx.doi.org/10.1016/S0166-6851(01)00297-3.
47. Dzierszinski F, Mortuaire M, Cesbron-Delauw MF, Tomavo S. 2000. Targeted disruption of the glycosylphosphatidylinositol-anchored surface antigen SAG3 gene in Toxoplasma gondii decreases host cell adhesion and drastically reduces virulence in mice. Mol. Microbiol. 37:574-582.
48. Aird WC. 2007. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ. Res. 100:158-173. http:// dx.doi.org/10.1161/01.RES.0000255691.76142.4a.
49. Dupont CD, Christian DA, Hunter CA. 2012. Immune response and immunopathology during toxoplasmosis. Semin. Immunopathol. 34: 793-813. http://dx.doi.org/10.1007/s00281-012-0339-3.
50. Lachenmaier SM, Deli MA, Meissner M, Liesenfeld O. 2011. Intracellular transport of Toxoplasma gondii through the blood-brain barrier. J. Neuroimmunol. 232:119-130. http://dx.doi.org/10.1016/ j.jneuroim.2010.10.029.
51. Nagineni CN, Detrick B, Hooks JJ. 2000. Toxoplasma gondii infection induces gene expression and secretion of interleukin 1 (IL-1), IL-6, granulocyte-macrophage colony-stimulating factor, and intercellular adhesion molecule 1 by human retinal pigment epithelial cells. Infect. Immun. 68:407-410. http://dx.doi.org/10.1128/IAI.68.1.407-410.2000.
52. Gamble JR, Harlan JM, Klebanoff SJ, Vadas MA. 1985. Stimulation of the adherence of neutrophils to umbilical vein endothelium by human recombinant tumor necrosis factor. Proc. Natl. Acad. Sci. U. S. A. 82: 8667-8671. http://dx.doi.org/10.1073/pnas.82.24.8667.
53. Schleimer RP, Rutledge BK. 1986. Cultured human vascular endothelial cells acquire adhesiveness for neutrophils after stimulation with interleukin 1, endotoxin, and tumor-promoting phorbol diesters. J. Immunol. 136:649-654.
54. Dewi BE, Takasaki T, Kurane I. 2004. In vitro assessment of human endothelial cell permeability: effects of inflammatory cytokines and dengue virus infection. J. Virol. Methods 121:171-180. http://dx.doi.org/ 10.1016/j.jviromet.2004.06.013.
55. Morgado P, Ong YC, Boothroyd JC, Lodoen MB. 2011. Toxoplasma gondii induces B7-2 expression through activation of JNK signal transduction. Infect. Immun. 79:4401-4412. http://dx.doi.org/10.1128/IAI.05562-11.
56. Endo T, Tokuda H, Yagita K, Koyama T. 1987. Effects of extracellular potassium on acid release and motility initiation in Toxoplasma gondii. J. Protozool. 34:291-295. http://dx.doi.org/10.1111/j.1550-7408.1987.tb03177.x.
57. Kane RS, Takayama S, Ostuni E, Ingber DE, Whitesides GM. 1999. Patterning proteins and cells using soft lithography. Biomaterials 20: 2363-2376. http://dx.doi.org/10.1016/S0142-9612(99)00165-9.
58. Dunn JD, Ravindran S, Kim SK, Boothroyd JC. 2008. The Toxoplasma gondii dense granule protein GRA7 is phosphorylated upon invasion and forms an unexpected association with the rhoptry proteins ROP2 and ROP4. Infect. Immun. 76:5853-5861. http://dx.doi.org/10.1128/ IAI.01667-07.
59. Lodoen MB, Gerke C, Boothroyd JC. 2010. A highly sensitive FRETbased approach reveals secretion of the actin-binding protein toxofilin during Toxoplasma gondii infection. Cell. Microbiol. 12:55-66. http:// dx.doi.org/10.1111/j.1462-5822.2009.01378.x.
60. Khoury MK, Parker I, Aswad DW. 2010. Acquisition of chemiluminescent signals from immunoblots with a digital single-lens reflex camera. Anal. Biochem. 397:129-131. http://dx.doi.org/10.1016/ j.ab.2009.09.041.