Real-time imaging of Toxoplasma-infected human monocytes under fluidic shear stress reveals rapid translocation of intracellular parasites across endothelial barriers

Cellular Microbiology

Volumn 16, Issue 4, 2014, Pages 580-595

  Ueno, Norikiyo ^a,b   Harker, Katherine S ^a,b   Clarke, Elizabeth V ^a,b   McWhorter, Frances Y ^a,c   Liu, Wendy F ^a,c   Tenner, Andrea J ^a,b   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

CD11B ANTIGEN; CD18 ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1;

ARTICLE; BIOACCUMULATION; CELL STRUCTURE; CELL TRACKING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENDOTHELIUM; HUMAN; HUMAN CELL; LIVE CELL IMAGING; MOLECULAR IMAGING; MONOCYTE; MONOCYTE CULTURE; NONHUMAN; PARASITE LOCALIZATION; PRIMARY CELL CULTURE; PRIORITY JOURNAL; PROTEIN CONFORMATION; SHEAR STRESS; TOXOPLASMA GONDII; TOXOPLASMOSIS; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; VASCULARIZATION;

CELL MOVEMENT; ENDOTHELIAL CELLS; HUMANS; MICROSCOPY, VIDEO; MONOCYTES; OPTICAL IMAGING; PHYSICAL PHENOMENA; TIME FACTORS; TOXOPLASMA;

EID: 84896394378     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12239     Document Type: Article

References (53)

1. Abram, C.L., and Lowell, C.A. (2009) The ins and outs of leukocyte integrin signaling. Annu Rev Immunol 27: 339-362.
2. Auffray, C., Fogg, D., Garfa, M., Elain, G., Join-Lambert, O., Kayal, S., etal. (2007) Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317: 666-670.
3. Aviles, H., Stiles, J., O'Donnell, P., Orshal, J., Leid, J., Sonnenfeld, G., and Monroy, F. (2008) Kinetics of systemic cytokine and brain chemokine gene expression in murine toxoplasma infection. J Parasitol 94: 1282-1288.
4. Barragan, A., and Sibley, L.D. (2002) Transepithelial migration of Toxoplasma gondii is linked to parasite motility and virulence. J Exp Med 195: 1625-1633.
5. Barragan, A., and Sibley, L.D. (2003) Migration of Toxoplasma gondii across biological barriers. Trends Microbiol 11: 426-430.
6. Barragan, A., Brossier, F., and Sibley, L.D. (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.
7. Benson, K., Cramer, S., and Galla, H.J. (2013) Impedance-based cell monitoring: barrier properties and beyond. Fluids Barriers CNS 10: 5.
8. Bierly, A.L., Shufesky, W.J., Sukhumavasi, W., Morelli, A.E., and Denkers, E.Y. (2008) Dendritic cells expressing plasmacytoid marker PDCA-1 are Trojan horses during Toxoplasma gondii infection. J Immunol 181: 8485-8491.
9. Bobak, D.A., Frank, M.M., and Tenner, A.J. (1986) Characterization of C1q receptor expression on human phagocytic cells: effects of PDBu and fMLP. J Immunol 136: 4604-4610.
10. Carman, C.V., and Springer, T.A. (2004) A transmigratory cup in leukocyte diapedesis both through individual vascular endothelial cells and between them. J Cell Biol 167: 377-388.
11. Carman, C.V., Jun, C.D., Salas, A., and Springer, T.A. (2003) Endothelial cells proactively form microvilli-like membrane projections upon intercellular adhesion molecule 1 engagement of leukocyte LFA-1. J Immunol 171: 6135-6144.
12. Channon, J.Y., Seguin, R.M., and Kasper, L.H. (2000) Differential infectivity and division of Toxoplasma gondii in human peripheral blood leukocytes. Infect Immun 68: 4822-4826.
13. Coombes, J.L., Charsar, B.A., Han, S.J., Halkias, J., Chan, S.W., Koshy, A.A., etal. (2013) Motile invaded neutrophils in the small intestine of Toxoplasma gondii-infected mice reveal a potential mechanism for parasite spread. Proc Natl Acad Sci U S A 110: E1913-E1922.
14. Courret, N., Darche, S., Sonigo, P., Milon, G., Buzoni-Gatel, D., and Tardieux, I. (2006) CD11c- and CD11b-expressing mouse leukocytes transport single Toxoplasma gondii tachyzoites to the brain. Blood 107: 309-316.
15. Da Gama, L.M., Ribeiro-Gomes, F.L., Guimaraes, U., Jr, and Arnholdt, A.C. (2004) Reduction in adhesiveness to extracellular matrix components, modulation of adhesion molecules and in vivo migration of murine macrophages infected with Toxoplasma gondii. Microbes Infect 6: 1287-1296.
16. Dewi, B.E., Takasaki, T., and 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.
17. Dubey, J.P. (1997) Bradyzoite-induced murine toxoplasmosis: stage conversion, pathogenesis, and tissue cyst formation in mice fed bradyzoites of different strains of Toxoplasma gondii. J Eukaryot Microbiol 44: 592-602.
18. Dubey, J.P., Speer, C.A., Shen, S.K., Kwok, O.C., and Blixt, J.A. (1997) Oocyst-induced murine toxoplasmosis: life cycle, pathogenicity, and stage conversion in mice fed Toxoplasma gondii oocysts. J Parasitol 83: 870-882.
19. Dunn, J.D., Ravindran, S., Kim, S.K., and Boothroyd, J.C. (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.
20. Fan, S.T., and Edgington, T.S. (1993) Integrin regulation of leukocyte inflammatory functions. CD11b/CD18 enhancement of the tumor necrosis factor-alpha responses of monocytes. J Immunol 150: 2972-2980.
21. Furtado, J.M., Bharadwaj, A.S., Ashander, L.M., Olivas, A., and Smith, J.R. (2012) Migration of toxoplasma gondii-infected dendritic cells across human retinal vascular endothelium. Invest Ophthalmol Vis Sci 53: 6856-6862.
22. Furtado, J.M., Ashander, L.M., Mohs, K., Chipps, T.J., Appukuttan, B., and Smith, J.R. (2013) Toxoplasma gondii migration within and infection of human retina. PLoS ONE 8: e54358.
23. Gregg, B., Taylor, B.C., John, B., Tait-Wojno, E.D., Girgis, N.M., Miller, N., etal. (2013) Replication and distribution of Toxoplasma gondii in the small intestine after oral infection with tissue cysts. Infect Immun 81: 1635-1643.
24. Harker, K.S., Ueno, N., Wang, T., Bonhomme, C., Liu, W., and Lodoen, M.B. (2013) Toxoplasma gondii modulates the dynamics of human monocyte adhesion to vascular endothelium under fluidic shear stress. J Leukoc Biol 93: 789-800.
25. Herter, J., and Zarbock, A. (2013) Integrin regulation during leukocyte recruitment. J Immunol 190: 4451-4457.
26. Kinashi, T. (2005) Intracellular signalling controlling integrin activation in lymphocytes. Nat Rev Immunol 5: 546-559.
27. Kluger, M.S., Clark, P.R., Tellides, G., Gerke, V., and Pober, J.S. (2013) Claudin-5 controls intercellular barriers of human dermal microvascular but not human umbilical vein endothelial cells. Arterioscler Thromb Vasc Biol 33: 489-500.
28. Lachenmaier, S.M., Deli, M.A., Meissner, M., and Liesenfeld, O. (2011) Intracellular transport of Toxoplasma gondii through the blood-brain barrier. J Neuroimmunol 232: 119-130.
29. Lambert, H., Hitziger, N., Dellacasa, I., Svensson, M., and Barragan, A. (2006) Induction of dendritic cell migration upon Toxoplasma gondii infection potentiates parasite dissemination. Cell Microbiol 8: 1611-1623.
30. Lawrence, M.B., Kansas, G.S., Kunkel, E.J., and Ley, K. (1997) Threshold levels of fluid shear promote leukocyte adhesion through selectins (CD62L, P, E). J Cell Biol 136: 717-727.
31. Leon, F., Contractor, N., Fuss, I., Marth, T., Lahey, E., Iwaki, S., etal. (2006) Antibodies to complement receptor 3 treat established inflammation in murine models of colitis and a novel model of psoriasiform dermatitis. J Immunol 177: 6974-6982.
32. Ley, K., Laudanna, C., Cybulsky, M.I., and Nourshargh, S. (2007) Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7: 678-689.
33. Lim, J., and Hotchin, N.A. (2012) Signalling mechanisms of the leukocyte integrin alphaMbeta2: current and future perspectives. Biol Cell 104: 631-640.
34. Lionetti, F.J., Hunt, S.M., and Valeri, C.R. (1980) Isolation of human blood phagocytes by counterflow centrifugation elutriation. In Methods of Cell Separation. Catsimpoolas, N. (ed.). New York: Springer US, pp. 141-156.
35. Montoya, J.G., and Liesenfeld, O. (2004) Toxoplasmosis. Lancet 363: 1965-1976.
36. Morgado, P., Ong, Y.C., Boothroyd, J.C., and Lodoen, M.B. (2011) Toxoplasma gondii induces B7-2 expression through activation of JNK signal transduction. Infect Immun 79: 4401-4412.
37. Nayal, A., Webb, D.J., and Horwitz, A.F. (2004) Talin: an emerging focal point of adhesion dynamics. Curr Opin Cell Biol 16: 94-98.
38. Oxvig, C., Lu, C., and Springer, T.A. (1999) Conformational changes in tertiary structure near the ligand binding site of an integrin I domain. Proc Natl Acad Sci U S A 96: 2215-2220.
39. Papaioannou, T.G., and Stefanadis, C. (2005) Vascular wall shear stress: basic principles and methods. Hellenic J Cardiol 46: 9-15.
40. Persat, F., Mercier, C., Ficheux, D., Colomb, E., Trouillet, S., Bendridi, N., etal. (2012) A synthetic peptide derived from the parasite Toxoplasma gondii triggers human dendritic cells' migration. J Leukoc Biol 92: 1241-1250.
41. Robben, P.M., LaRegina, M., Kuziel, W.A., and Sibley, L.D. (2005) Recruitment of Gr-1+monocytes is essential for control of acute toxoplasmosis. J Exp Med 201: 1761-1769.
42. Robbins, J.R., Zeldovich, V.B., Poukchanski, A., Boothroyd, J.C., and Bakardjiev, A.I. (2012) Tissue barriers of the human placenta to infection with Toxoplasma gondii. Infect Immun 80: 418-428.
43. Schenkel, A.R., Mamdouh, Z., and Muller, W.A. (2004) Locomotion of monocytes on endothelium is a critical step during extravasation. Nat Immunol 5: 393-400.
44. Seipel, D., Oliveira, B.C., Resende, T.L., Schuindt, S.H., Pimentel, P.M., Kanashiro, M.M., and Arnholdt, A.C. (2010) Toxoplasma gondii infection positively modulates the macrophages migratory molecular complex by increasing matrix metalloproteinases, CD44 and alpha v beta 3 integrin. Vet Parasitol 169: 312-319.
45. Serbina, N.V., Jia, T., Hohl, T.M., and Pamer, E.G. (2008) Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol 26: 421-452.
46. Shaw, S.K., Ma, S., Kim, M.B., Rao, R.M., Hartman, C.U., Froio, R.M., etal. (2004) Coordinated redistribution of leukocyte LFA-1 and endothelial cell ICAM-1 accompany neutrophil transmigration. J Exp Med 200: 1571-1580.
47. Sumagin, R., Prizant, H., Lomakina, E., Waugh, R.E., and Sarelius, I.H. (2010) LFA-1 and Mac-1 define characteristically different intralumenal crawling and emigration patterns for monocytes and neutrophils in situ. J Immunol 185: 7057-7066.
48. Tardieux, I., and Menard, R. (2008) Migration of Apicomplexa across biological barriers: the Toxoplasma and Plasmodium rides. Traffic 9: 627-635.
49. Tsubota, Y., Frey, J.M., Tai, P.W., Welikson, R.E., and Raines, E.W. (2013) Monocyte ADAM17 promotes diapedesis during transendothelial migration: identification of steps and substrates targeted by metalloproteinases. J Immunol 190: 4236-4244.
50. Unno, A., Kachi, S., Batanova, T.A., Ohno, T., Elhawary, N., Kitoh, K., and Takashima, Y. (2013) Toxoplasma gondii tachyzoite-infected peripheral blood mononuclear cells are enriched in mouse lungs and liver. Exp Parasitol 134: 160-164.
51. Wang, R., Jawg, J.J., Stutzmang, N.C., Zoug, Z., and Sung, P.D. (2012) Natural killer cell-produced IFN-γ and TNF-α induce target cell cytolysis through up-regulation of ICAM-1. J Leukoc Biol 91: 299-309.
52. Weidner, J.M., Kanatani, S., Hernandez-Castaneda, M.A., Fuks, J.M., Rethi, B., Wallin, R.P., and Barragan, A. (2013) Rapid cytoskeleton remodelling in dendritic cells following invasion by Toxoplasma gondii coincides with the onset of a hypermigratory phenotype. Cell Microbiol 15: 1735-1752.
53. Zarbock, A., Ley, K., McEver, R.P., and Hidalgo, A. (2011) Leukocyte ligands for endothelial selectins: specialized glycoconjugates that mediate rolling and signaling under flow. Blood 118: 6743-6751.