Cryptosporidium parvum invasion of biliary epithelia requires host cell tyrosine phosphorylation of cortactin via c-Src

Gastroenterology

Volumn 125, Issue 1, 2003, Pages 216-228

  Chen, Xian Ming ^a   Huang, Bing Q ^a   Splinter, Patrick L ^a   Cao, Hong ^a   Zhu, Guan ^b   McNiven, Mark A ^a   Larusso, Nicholas F ^a,c  

^a MAYO CLINIC COLLEGE OF MEDICINE   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CLATHRIN; CORTACTIN; DYNAMIN; PROTEIN TYROSINE KINASE;

ACTIN POLYMERIZATION; ARTICLE; BILE DUCT; CELL INVASION; CONTROLLED STUDY; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; ENDOCYTOSIS; EPITHELIUM CELL; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY;

EID: 0038054141     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0016-5085(03)00662-0     Document Type: Article

References (53)

1. Tzipori S, Griffiths JK. Natural history and biology of Cryptosporidium parvum. Adv Parasitol 1998;40:5-36.
2. Chen XM, Keithly JS, Paya CV, LaRusso NF. Cryptosporidiosis. N Engl J Med 2002;346:1723-1731.
3. Clark DP. New insights in human cryptosporidiosis. Clin Microbiol Rev 1999;12:554-563.
4. Chen XM, Levine SA, Tietz P, Krueger E, McNiven MA, Jefferson DM, Mahle M, LaRusso NF. Cryptosporidium parvum is cytopathic for cultured human biliary epithelia via an apoptotic mechanism. Hepatology 1998;28:906-913.
5. O'Donoghue PJ. Cryptosporidium and cryptosporidiosis in man and animals. Int J Parasitol 1995;25:139-195.
6. Finlay BB, Cossart P. Exploitation of mammalian host cell functions by bacterial pathogens. Science 1997;276:718-725.
7. Winner F, Rosengarten R, Citti C. In vitro cell invasion of Mycoplasma gallisepticum. Infect Immun 2000;68:4238-4244.
8. Rabier MJ, Tyler NK, Walker NJ, Hansen LM, Hirsh DC, Tablin F. Pasteurella multocida enters polarized epithelial cells by interacting with host F-actin. Vet Microbiol 1997;54:343-355.
9. Burns JL, Jonas M, Chi EY, Clark DK, Berger A, Griffith A. Invasion of respiratory epithelial cells by Burkholderia (Pseudomonas) cepacia. Infect Immun 1996;64:4054-4059.
10. Schramm N, Wyrick PB. Cytoskeletal requirements in Chlamydia trachomatis infection of host cells. Infect Immun 1995;63:324-332.
11. Forney JR, DeWald DB, Yang S, Speer CA, Healey MC. A role for host phosphoinositide 3-kinase and cytoskeletal remodeling during Cryptosporidium parvum infection. Infect Immun 1999;67: 844-852.
12. Chen XM, LaRusso NF. Mechanisms of attachment and internalization of Cryptosporidium parvum to biliary and intestinal epithelial cells. Gastroenterology 2000;118:368-379.
13. Elliott DA, Clark DP. Cryptosporidium parvum induces host cell actin accumulation at the host-parasite interface. Infect Immun 2000;68:2315-2322.
14. Bonnin A, Lapillonne A, Petrella T, Lopez J, Chaponnier C, Gabbiani G, Robine S, Dubremetz JF. Immunodetection of the microvillous cytoskeleton molecules villin and ezrin in the parasitophorous vacuole wall of Cryptosporidium parvum (Protozoa: Apicomplexa). Eur J Cell Biol 1999;78:794-801.
15. Aji T, Flanigan T, Marshall R, Kaetzel C, Aikawa M. Ultrastructural study of asexual development of Cryptosporidium parvum in a human intestinal cell line. J Protozool 1991;38:82S-84S.
16. Elliott DA, Coleman DJ, Lane MA, May RC, Machesky LM, Clark DP. Cryptosporidium parvum infection requires host cell actin polymerization. Infect Immun 2001;69:5940-5942.
17. Zhong L, Lu HG, Moreno SN, Docampo R. Tyrosine phosphate hydrolysis of host proteins by Trypanosoma cruzi is linked to cell invasion. FEMS Microbiol Lett 1998;161:15-20.
18. Martiny A, Vannier-Santos MA, Borges VM, Meyer-Fernandes JR, Assreuy J, Cunha e Silva NL, de Souza W. Leishmania-induced tyrosine phosphorylation in the host macrophage and its implication to infection. Eur J Cell Biol 1996;71:206-215.
19. Dluzewski AR, Garcia CR. Inhibition of invasion and intraerythrocytic development of Plasmodium falciparum by kinase inhibitors. Experientia 1996;52:621-623.
20. Barz C, Abahji TN, Trulzsch K, Heesemann J. The Yersinia Ser/Thr protein kinase YpkA/YopO directly interacts with the small GT-Pases RhoA and Rac-1. FEBS Lett 2000;482:139-143.
21. Watarai M, Kamata Y, Kozaki S, Sasakawa C. rho, a small GTP-binding protein, is essential for Shigella invasion of epithelial cells. J Exp Med 1997;185:281-292.
22. Galdiero M, Vitiello M, D'Isantom M, Peluso L, Galdiero M. Induction of tyrosine phosphorylated proteins in THP-1 cells by Salmonella typhimurium, Pasteurella haemolytica and Haemophilus influenzae porins. FEMS Immunol Med Microbiol 2001;31: 121-130.
23. Palmer LM, Reilly TJ, Utsalo SJ, Donnenberg MS. Internalization of Escherichia coli by human renal epithelial cells is associated with tyrosine phosphorylation of specific host cell proteins. Infect Immun 1997;65:2570-2575.
24. Dehio C, Prevost MC, Sansonetti PJ. Invasion of epithelial cells by Shigella flexneri induces tyrosine phosphorylation of cortactin by a pp60c-src-mediated signalling pathway. EMBO J 1995;14: 2471-2482.
25. Esen M, Grassme H, Riethmuller J, Riehle A, Fassbender K, Gulbins E. Invasion of human epithelial cells by Pseudomonas aeruginosa involves src-like tyrosine kinases p60Src and p59Fyn. Infect Immun 2001;69:281-287.
26. Verdon R, Keusch GT, Tzipori S, Grubman SA, Jefferson DM, Ward HD. An in vitro model of infection of human biliary epithelial cells by Cryptosporidium parvum. J Infect Dis 1997;175:1268-1272.
27. Campbell AT, Robertson LJ, Smith HV. Viability of Cryptosporidium parvum oocysts: correlation of in vitro excystation with inclusion or exclusion of fluorogenic vital dyes. Appl Environ Microbiol 1992;58:3488-3493.
28. McDonald V, Stables R, Warhurst DC, Barer MR, Blewett DA, Chapman HD, Connolly GM, Chiodini PL, McAdam KP. In vitro cultivation of Cryptosporidium parvum and screening for anticryptosporidial drugs. Antimicrob Agents Chemother 1990;34:1498-1500.
29. Grubman SA, Perrone RD, Lee DW, Murray SL, Rogers LC, Wolkoff LI, Mulberg AE, Cherington V, Jefferson DM. Regulation of intracellular pH by immortalized human intrahepatic biliary epithelial cell lines. Am J Physiol 1994;266:G1060-G1070.
30. MacGlashan D Jr, Miura K, Lavens-Phillips S. Pharmacology of IgE-mediated desensitization of human basophils: effects of protein kinase C and src-family kinase inhibitors. Biochem Pharmacol 2000;60:1717-1727.
31. Zhu G, Marchewka MJ, Woods KM, Upton SJ, Keithly JS. Molecular analysis of a type I fatty acid synthase in Cryptosporidium parvum. Mol Biochem Parasitol 2000;105:253-260.
32. Precious B, Young DF, Bermingham A, Fearns R, Ryan M, Randall RE. Inducible expression of the P, V, and NP genes of the paramyxovirus simian virus 5 in cell lines and an examination of NP-P and NP-V interactions. J Virol 1995;69:8001-8010.
33. Cao H, Orth JD, Chen J, Weller SG, Heuser JE, McNiven MA. Cortactin is a component of clathrin-coated pits and participates in receptor-mediated endocytosis. Mol Cell Biol 2003;23:2162-2170.
34. McNiven MA, Kim L, Krueger EW, Orth JD, Cao H, Wong TW. Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J Cell Biol 2000;151:187-198.
35. Bendayan M. Concentration of amylase along its secretory pathway in the pancreatic acinar cell as revealed by high resolution immunocytochemistry. Histochem J 1984;16:85-108.
36. Martinez-Menarguez JA, Geuze HJ, Slot JW, Klumperman J. Vesicular tubular clusters between the ER and Golgi mediate concentration of soluble secretory proteins by exclusion from COPI-coated vesicles. Cell 1999;98:81-90.
37. Zhan X, Plourde C, Hu X, Friesel R, Maciag T. Association of fibroblast growth factor receptor-1 with c-Src correlates with association between c-Src and cortactin. J Biol Chem 1994;269: 20221-20224.
38. Cantarelli W, Takahashi A, Akeda Y, Nagayama K, Honda T. Interaction of enteropathogenic or enterohemorrhagic Escherichia coli with HeLa cells results in translocation of cortactin to the bacterial adherence site. Infect Immun 2000;68:382-386.
39. Fawaz FS, van Ooij C, Homola E, Mutka SC, Engel JN. Infection with Chlamydia trachomatis alters the tyrosine phosphorylation and/or localization of several host cell proteins including cortactin. Infect Immun 1997;65:5301-5308.
40. Mayer BJ. Signal transduction: clamping down on Src activity. Curr Biol 1997;7:R295-R298.
41. Weaver AM, Heuser JE, Karginov AV, Lee WL, Parsons JT, Cooper JA. Interaction of cortactin and N-WASp with Arp2/3 complex. Curr Biol 2002;12:1270-1278.
42. Sam-Yellowe TY. Rhaptory organellea of the Apicomplexa: their role in host cell invasion and intracellular survival. Parasitol Today 1996;12:308-316.
43. Wu H, Reynolds AB, Kanner SB, Vines RR, Parsons JT. Identification and characterization of a novel cytoskeleton-associated pp60src substrate. Mol Cell Biol 1991;11:5113-5124.
44. McNiven MA, Cao H, Pitts KR, Yoon Y. The dynamin family of mechanoenzymes: pinching in new places. Trends Biochem Sci 2000;25:115-120.
45. McNiven MA. Dynamin: a molecular motor with pinchase action. Cell 1998;94:151-154.
46. Schmid SL. Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu Rev Biochem 1997;66:511-548.
47. Henley JR, Krueger EW, Oswald BJ, McNiven MA. Dynamin-mediated internalization of caveolae. J Cell Biol 1998;141:85-99.
48. Gold ES, Underhill DM, Morrissette NS, Guo J, McNiven MA, Aderem A. Dynamin 2 is required for phagocytosis in macrophages. J Exp Med 1999;190:1849-1856.
49. DeTulleo L, Kirchhausen T. The clathrin endocytic pathway in viral. EMBO J 1998;17:4585-4593.
50. Bayer N, Schober D, Huttinger M, Blaas D, Fuchs R. Inhibition of clathrin-dependent endocytosis has multiple effects on human rhinovirus serotype 2 cell entry. J Biol Chem 2001;276:3952-3962.
51. Maruta K, Ogawa M, Miyamoto H, Izu K, Yoshida SI. Entry and intracellular localization of Legionella dumoffii in Vero cells. Microb Pathog 1998;24:65-73.
52. Huber M, Brabec M, Bayer N, Blaas D, Fuchs R. Elevated endosomal pH in HeLa cells overexpressing mutant dynamin can affect infection by pH-sensitive viruses. Traffic 2001;2:727-736.
53. Wang K, Huang S, Kapoor-Munshi A, Nemerow G. Adenovirus internalization and infection require dynamin. J Virol 1998;72: 3455-3458.