Host cell invasion by trypanosomes requires lysosomes and microtubule/kinesin-mediated transport

Journal of Cell Biology

Volumn 134, Issue 2, 1996, Pages 349-362

  Rodríguez, Ana ^a   Samoff, Erika ^a   Rioult, Marc G ^a   Chung, Albert ^a   Andrews, Norma W ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KINESIN;

ANIMAL CELL; ARTICLE; CELL INVASION; CELL VACUOLE; CONTROLLED STUDY; FIBROBLAST; HOST CELL; LYSOSOME; MEMBRANE FUSION; MICROTUBULE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, CD; BIOLOGICAL TRANSPORT; CELLS, CULTURED; HOST-PARASITE RELATIONS; KINESIN; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; LYSOSOMES; MEMBRANE GLYCOPROTEINS; MICROSCOPY, VIDEO; MICROTUBULES; MOLECULAR SEQUENCE DATA; RATS; TRYPANOSOMA CRUZI;

EID: 0030008358     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.134.2.349     Document Type: Article

References (51)

1. Andrews, N.W. 1995. Microbial subversion of phagocytosis: lysosome recruitment during host cell invasion by Trypanosoma cruzi. Trends Cell Biol. 5: 133-137.
2. Andrews, N.W., K.S. Hong, E.S. Robbins, and V. Nussenzweig. 1987. Stage-specific surface antigens expressed during the morphogenesis of vertebrate forms of Trypanosoma cruzi. Exp. Parasitol. 64:474-484.
3. Boyles, J., and D.F. Bainton. 1981. Changes in plasma-membrane-associated filaments during endocytosis and exocytosis in polymorphonuclear leukocytes. Cell. 24:905-914.
4. Brady, S.T., K.K. Pfister, and G.S. Bloom. 1990. A monoclonal antibody against kinesin inhibits both anterograde and retrograde fast axonal transport in squid axoplasm. Proc. Natl. Acad. Sci. USA. 87:1061-1065.
5. Burkhardt, J.K., J.M. McIlvain, M.P. Sheetz, and Y. Argon. 1993. Lytic granules from cytotoxic T cells exhibit kinesin-dependent motility on microtubules in vitro. J. Cell Sci. 104:151-162.
6. 2+-signaling factor for mammalian cells. J. Biol. Chem. 270:5172-5180.
7. Cole, N.B., and J. Lippincott-Schwartz. 1995. Organization of organelles and membrane traffic by microtubules. Curr. Opin. Cell Biol. 7:55-64.
8. De Brabander, M., R. Nuydens, G. Geuens, M. Moeremans, and J. De May. 1986. The use of submicroscopic gold particles combined with video contrast enhancement as a simple molecular probe for the living cell. Cell Motil. Cytoskeleton. 6:105-113.
9. De Brabander, M., R. Nuydens, H. Geerts, and C.R. Hopkins. 1988. Dynamic behavior of the transferrin receptor followed in living epidermoid carcinoma (A431) cells with nanovid microscopy. Cell Motil. Cytoskeleton. 9:30-47.
10. Desjardins, M. 1995. Biogenesis of phagolysosomes: the 'kiss and run' hypothesis. Trends Cell Biol. 5:183-186.
11. Desjardins, M., L.A. Huber, R.G. Parton, and G. Griffiths. 1994. Biogenesis of phagolysosomes proceeds though a sequential series of interactions with the endocytic apparatus. J. Cell Biol. 124:677-688.
12. Feiguin, F., A. Ferreira, K.S. Kosik, and A. Caceres. 1994. Kinesin-mediated organelle translocation revealed by cellular manipulations. J. Cell Biol. 127: 1021-1039.
13. Granger, B., S.A. Green, C.A. Gabel, C.L. Howe, I. Mellman, and A. Helenius. 1990. Characterization and cloning of lgp 110, a lysosomal membrane glycoprotein from mouse and rat cells. J. Biol. Chem. 265:12036-12043.
14. Griffiths, G.M., and Y. Argon. 1995. Structure and biogenesis of lytic granules. Curr. Top. Microbiol. Immunol. 198:39-58.
15. Hall, B.F., P. Webster, A.K. Ma, K.A. Joiner, and N.W. Andrews. 1992. Desialylation of lysosomal membrane glycoproteins by Trypanosoma cruzi: a role for the surface neuraminidase in facilitating parasite entry into the host cell cytoplasm. J. Exp. Med. 176:313-325.
16. Hamm-Alvarez, S.F., P.Y. Preston, and M.P. Sheetz. 1993. Regulation of vesicle transport in CV-1 cells and extracts. J. Cell Sci. 106:955-966.
17. Hamm-Alvarez, S.F., B.E. Alayof, H.M. Himmel, P.Y. Kim, A.L. Crews, H.C. Strauss, and M.P. Sheetz. 1994. Coordinate depression of bradykinin receptor recycling and microtubule-dependent transport by taxol. Proc. Natl. Acad. Sci. USA. 91:7812-7816.
18. Herman, B., and D.F. Albertini. 1984. A time-lapse video intensification analysis of cytoplasmic organelle movements during endosome translocation. J. Cell Biol. 98:565-576.
19. Heuser, J.E. 1989. Changes in lysosome shape and distribution correlated with changes in cytoplasmic pH. J. Cell Biol. 108:855-864.
20. Hollenbeck, P.J., and J.A. Swanson. 1990. Radial extension of macrophage tubular lysosomes supported by kinesin. Nature (Lond.). 346:864-866.
21. Howe, C.L., B.L. Granger, M. Hull, S.A. Green, C.A. Gabel, A. Helenius, and I. Mellman. 1988. Derived protein sequence, oligosaccharides, and membrane insertion of the 120 kDa lysosomal membrane glycoprotein (lgp 120): identification of a highly conserved family of lysosomal membrane glycoproteins. Proc. Natl. Acad. Sci. USA. 85:7577-7581.
22. Hunziker, W., P. Male, and I. Mellman. 1990. Differential microtubule requirements for transcytosis in MDCK cells. EMBO (Eur. Mol. Biol. Organ.) J. 9: 3515-3525.
23. Ingold, A.L., S.A. Cohn, and J.M. Scholey. 1988. Inhibition of kinesin-driven microtubule motility by monoclonal antibodies to kinesin heavy chains. J. Cell Biol. 107:2657-2667.
24. Jaconi, M.E.E., D.P. Lew, J.L. Carpentier, K.E. Magnusson, M. Sjogren, and O. Stendahl. 1990. Cytosolic free calcium elevation mediates the phagosome-lysosome fusion during phagocytosis in human neutrophils. J. Cell Biol. 110: 1555-1564.
25. 3 and cAMP as long-range and associative messengers. Trends Neurosci. 17: 95-101.
26. Kornfeld, S., and I. Mellman. 1989. The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5:483-525.
27. Lin, S.X.H., and C.A. Collins. 1993. Regulation of the intracellular distribution of cytoplasmic dynein by serum factors and calcium. J. Cell Sci. 105:579-588.
28. Luduena, R.F., and M.C. Roach. 1991. Tubulin sulfhydryl groups as probes and targets for antimitotic and antimicrotubule agents. Pharmac. Ther. 49:133-152.
29. Matteoni, R., and T.E. Kreis. 1987. Translocation and clustering of endosomes and lysosomes depends on microtubules. J. Cell Biol. 105:1253-1265.
30. Matthies, H.J.G., R.J. Miller, and H.C. Palfrey. 1993. Calmodulin binding to and cAMP-dependent phosphorylation of kinesin light chains modulate kinesin ATPase activity. J. Biol. Chem. 268:11176-11187.
31. Ming, M., M.E. Ewen, and M.A. Pereira. 1995. Trypanosome invasion of mammalian cells requires activation of the TGFβ signaling pathway. Cell. 82:1-20.
32. Montgomery, R.R., P. Webster, and I. Mellman. 1991. Accumulation of indigestible substances reduces fusion competence of macrophage lysosomes. J. Immunol. 147:3087-3095.
33. Moreno, S.N., J. Silva, A.E. Vercesi, and R. Docampo. 1994. Cytosotic free calcium elevation in Trypanosoma cruzi is required for invasion. J. Exp. Med. 180:1535-1540.
34. Nakata, T., and N. Hirokawa. 1995. Point mutation of adenosine triphosphate-binding motif generated rigor kinesin that selectively blocks anterograde lysosome membrane transport. J. Cell Biol. 131:1039-1053.
35. Oh, Y-K., and J.A. Swanson. 1996. Different fates of phagocytosed particles after delivery into macrophage lysosomes. J. Cell Biol. 132:585-593.
36. Perou, C.M., and J. Kaplan. 1993. Chediak-Higashi syndrome is not due to a defect in microtubule-based lysosomal mobility. J. Cell Sci. 106:99-107.
37. i in individual cytolytic T cells and targets. EMBO (Eur. Mol. Biol. Organ.) J. 6:2223-2232.
38. Pryzwansky, K.B., E.K. MacRae, J.K. Spitznagel, and M.H. Cooney. 1979. Early degranulation of human neutrophils: immunocytochemical studies of surface and intracellular phagocytic events. Cell. 18:1025-1033.
39. Rabinowitz, S., H. Horstmann, S. Gordon, and G. Griffiths. 1992. Immunocytochemical characterization of the endocytic and phagolysosomal compartments in peritoneal macrophages. J. Cell Biol. 116:95-112.
40. Robinson, D.R., T. Sherwin, A. Ploubidou, E.H. Byard, and K. Gull. 1995. Microtubule polarity and dynamics in the control of organelle positioning, segregation, and cytokinesis in the trypanosome cell cycle. J. Cell Biol. 128: 1163-1172.
41. 2+ mobilization and microfilament rearrangement in host cells. J. Cell Biol. 129:1263-1273.
42. Schenkman, S., N.W. Andrews, V. Nussenzweig, and E.S. Robbins. 1988. Trypanosoma cruzi invade a mammalian epithelial cell in a polarized manner. Cell. 55:157-165.
43. Schenkman, S., E.S. Robbins, and V. Nussenzweig. 1991. Attachment of Trypanosoma cruzi to mammalian cells requires parasite energy, and invasion can be independent of the target cell cytoskeleton. Infect. Immun. 59:645-654.
44. Schroer, T.A., and M.P. Sheetz. 1991. Functions of microtubule-based motors. Annu. Rev. Physiol. 53:629-652.
45. Slot, J.W., and H.J. Geuze. 1985. A new method of preparing gold probes for multiple-labeling cytochemistry. Eur. J. Cell Biol. 38:87-93.
46. Swanson, J.A., A. Locke, P. Ansel, and P. Hollenbeck. 1992. Radial movement of lysosomes in permeabilized macrophages. J. Cell Sci. 103:202-209.
47. Tardieux, I., P. Webster, J. Ravensloot, W. Boron, J.A. Lunn, J.E. Heuser, and N.W. Andrews. 1992. Lysosome recruitment and fusion are early events required for trypanosome invasion of mammalian cells. Cell. 71:1117-1130.
48. 2+ transients. J. Exp. Med. 179:1017-1022.
49. Viitala, J., S.R. Carlsson, P.D. Siebert, and M. Fukuda. 1988. Molecular cloning of cDNAs encoding lamp A, a human lysosomal membrane glycoprotein with apparent Mr ∼ 120,000. Proc. Natl. Acad. Sci. USA. 85:3743-3747.
50. Wang, Y.L., and M.B. Goren. 1987. Differential and sequential delivery of fluorescent lysosomal probes into phagosomes in mouse peritoneal macrophages. J. Cell Biol. 104:1749-1754.
51. White, S., K. Miller, C. Hopkins, and I.S. Trowbridge. 1992. Monoclonal antibodies against defined epitopes of the human transferrin receptor cytoplasmic tail. Biochim. Biophys. Acta. 1136:28-34.