Cholangiocyte myosin IIB is required for localized aggregation of sodium glucose cotransporter 1 to sites of Cryptosporidium parvum cellular invasion and facilitates parasite internalization

Infection and Immunity

Volumn 78, Issue 7, 2010, Pages 2927-2936

  O'Hara, Steven P ^a   Gajdos, Gabriella B ^a   Trussoni, Christy E ^a   Splinter, Patrick L ^a   LaRusso, Nicholas F ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (5 IODO 1 NAPHTHALENESULFONYL)HEXAHYDRO 1H 1,4 DIAZEPINE; AQUAPORIN 1; BLEBBISTATIN; MYOSIN IIA; MYOSIN IIB; SMALL INTERFERING RNA; SODIUM GLUCOSE COTRANSPORTER 1;

ARTICLE; CELL CULTURE; CELL INVASION; CELL MEMBRANE; CHOLANGIOCYTE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; DRUG EFFECT; EPITHELIUM CELL; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

AQUAPORIN 1; BILE DUCTS; BLOTTING, WESTERN; CELL LINE; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; FLUORESCENT ANTIBODY TECHNIQUE; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HOST-PARASITE INTERACTIONS; HUMANS; MICROSCOPY, ELECTRON, SCANNING; NONMUSCLE MYOSIN TYPE IIA; NONMUSCLE MYOSIN TYPE IIB; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SODIUM-GLUCOSE TRANSPORTER 1;

EID: 77953938085     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00077-10     Document Type: Article

References (57)

1. Agre, P., L. S. King, M. Yasui, W. B. Guggino, O. P. Ottersen, Y. Fujiyoshi, A. Engel, and S. Nielsen. 2002. Aquaporin water channels - from atomic structure to clinical medicine. J. Physiol. 542:3-16. (Pubitemid 35190266)
2. Aji, T., T. Flanigan, R. Marshall, C. Kaetzel, and M. Aikawa. 1991. Ultrastructural study of asexual development of Cryptosporidium parvum in a human intestinal cell line. J. Protozool. 38:82S-84S.
3. Bao, J., S. S. Jana, and R. S. Adelstein. 2005. Vertebrate nonmuscle myosin II isoforms rescue small interfering RNA-induced defects in COS-7 cell cytokinesis. J. Biol. Chem. 280:19594-19599.
4. Bao, J., X. Ma, C. Liu, and R. S. Adelstein. 2007. Replacement of nonmuscle myosin II-B with II-A rescues brain but not cardiac defects in mice. J. Biol. Chem. 282:22102-22111.
5. Bonnin, A., A. Lapillonne, T. Petrella, J. Lopez, C. Chaponnier, G. Gabbiani, S. Robine, and J. F. Dubremetz. 1999. Immunodetection of the microvillous cytoskeleton molecules villin and ezrin in the parasitophorous vacuole wall of Cryptosporidium parvum (Protozoa: Apicomplexa). Eur. J. Cell Biol. 78:794-801.
6. Bresnick, A. R. 1999. Molecular mechanisms of nonmuscle myosin-II regulation. Curr. Opin. Cell Biol. 11:26-33.
7. Cai, Y., N. Biais, G. Giannone, M. Tanase, G. Jiang, J. M. Hofman, C. H. Wiggins, P. Silberzan, A. Buguin, B. Ladoux, and M. P. Sheetz. 2006. Nonmuscle myosin IIA-dependent force inhibits cell spreading and drives F-actin flow. Biophys. J. 91:3907-3920. (Pubitemid 44788333)
8. Cao, C., Y. Sun, S. Healey, Z. Bi, G. Hu, S. Wan, N. Kouttab, W. Chu, and Y. Wan. 2006. EGFR-mediated expression of aquaporin-3 is involved in human skin fibroblast migration. Biochem. J. 400:225-234. (Pubitemid 44852036)
9. Cello, J. P. 1998. AIDS-related biliary tract disease. Gastrointest. Endosc. Clin. N. Am. 8:963.
10. Chan, W., G. Calderon, A. L. Swift, J. Moseley, S. Li, H. Hosoya, I. M. Arias, and D. F. Ortiz. 2005. Myosin II regulatory light chain is required for trafficking of bile salt export protein to the apical membrane in Madin-Darby canine kidney cells. J. Biol. Chem. 280:23741-23747.
11. Chen, X. M., B. Q. Huang, P. L. Splinter, H. Cao, G. Zhu, M. A. McNiven, and N. F. LaRusso. 2003. Cryptosporidium parvum invasion of biliary epithelia requires host cell tyrosine phosphorylation of cortactin via c-Src. Gastroenterology 125:216-228.
12. Chen, X. M., B. Q. Huang, P. L. Splinter, J. D. Orth, D. D. Billadeau, M. A. McNiven, and N. F. LaRusso. 2004. Cdc42 and the actin-related protein/neural Wiskott-Aldrich syndrome protein network mediate cellular invasion by Cryptosporidium parvum. Infect. Immun. 72:3011-3021.
13. Chen, X. M., J. S. Keithly, C. V. Paya, and N. F. LaRusso. 2002. Cryptosporidiosis. N. Engl. J. Med. 346:1723-1731.
14. Chen, X. M., and N. F. LaRusso. 2002. Cryptosporidiosis and the pathogenesis of AIDS-cholangiopathy. Semin. Liver Dis. 22:277-289.
15. Chen, X. M., and N. F. LaRusso. 2000. Mechanisms of attachment and internalization of Cryptosporidium parvum to biliary and intestinal epithelial cells. Gastroenterology 118:368-379.
16. Chen, X. M., S. P. O'Hara, B. Q. Huang, P. L. Splinter, J. B. Nelson, and N. F. LaRusso. 2005. Localized glucose and water influx facilitates Cryptosporidium parvum cellular invasion by means of modulation of host-cell membrane protrusion. Proc. Natl. Acad. Sci. U. S. A. 102:6338-6343.
17. Chrzanowska-Wodnicka, M., and K. Burridge. 1996. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133:1403-1415. (Pubitemid 26192339)
18. Current, W. L., and N. C. Reese. 1986. A comparison of endogenous development of three isolates of Cryptosporidium in suckling mice. J. Protozool. 33:98-108.
19. De La Cruz, E. M., and E. M. Ostap. 2004. Relating biochemistry and function in the myosin superfamily. Curr. Opin. Cell Biol. 16:61-67.
20. Elliott, D. A., and D. P. Clark. 2000. Cryptosporidium parvum induces host cell actin accumulation at the host-parasite interface. Infect. Immun. 68:2315-2322.
21. Elliott, D. A., D. J. Coleman, M. A. Lane, R. C. May, L. M. Machesky, and D. P. Clark. 2001. Cryptosporidium parvum infection requires host cell actin polymerization. Infect. Immun. 69:5940-5942.
22. Eto, M. 2009. Regulation of cellular protein phosphatase-1 (PP1) by phosphorylation of the CPI-17 family, C-kinase-activated PP1 inhibitors. J. Biol. Chem. 284:35273-35277.
23. Eto, M., T. Ohmori, M. Suzuki, K. Furuya, and F. Morita. 1995. A novel protein phosphatase-1 inhibitory protein potentiated by protein kinase C. Isolation from porcine aorta media and characterization. J. Biochem. 118:1104-1107.
24. Forney, J. R., D. B. DeWald, S. Yang, C. A. Speer, and M. C. Healey. 1999. A role for host phosphoinositide 3-kinase and cytoskeletal remodeling during Cryptosporidium parvum infection. Infect. Immun. 67:844-852.
25. Forney, J. R., D. K. Vaughan, S. Yang, and M. C. Healey. 1998. Actin-dependent motility in Cryptosporidium parvum sporozoites. J. Parasitol. 84:908-913.
26. Golomb, E., X. Ma, S. S. Jana, Y. A. Preston, S. Kawamoto, N. G. Shoham, E. Goldin, M. A. Conti, J. R. Sellers, and R. S. Adelstein. 2004. Identification and characterization of nonmuscle myosin II-C, a new member of the myosin II family. J. Biol. Chem. 279:2800-2808.
27. Grubman, S. A., R. D. Perrone, D. W. Lee, S. L. Murray, L. C. Rogers, L. I. Wolkoff, A. E. Mulberg, V. Cherington, and D. M. Jefferson. 1994. Regulation of intracellular pH by immortalized human intrahepatic biliary epithelial cell lines. Am. J. Physiol. 266:G1060-G1070.
28. Hara-Chikuma, M., and A. S. Verkman. 2006. Aquaporin-1 facilitates epithelial cell migration in kidney proximal tubule. J. Am. Soc. Nephrol. 17:39-45.
29. Hashim, A., G. Mulcahy, B. Bourke, and M. Clyne. 2006. Interaction of Cryptosporidium hominis and Cryptosporidium parvum with primary human and bovine intestinal cells. Infect. Immun. 74:99-107.
30. Heintzelman, M. B., and J. D. Schwartzman. 2001. Myosin diversity in Apicomplexa. J. Parasitol. 87:429-432.
31. Huang, B. Q., X. M. Chen, and N. F. LaRusso. 2004. Cryptosporidium parvum attachment to and internalization by human biliary epithelia in vitro: a morphologic study. J. Parasitol. 90:212-221.
32. Ivanov, A. I., M. Bachar, B. A. Babbin, R. S. Adelstein, A. Nusrat, and C. A. Parkos. 2007. A unique role for nonmuscle myosin heavy chain IIA in regulation of epithelial apical junctions. PloS ONE 2:e658.
33. Jana, S. S., S. Kawamoto, and R. S. Adelstein. 2006. A specific isoform of nonmuscle myosin II-C is required for cytokinesis in a tumor cell line. J. Biol. Chem. 281:24662-24670.
34. Jiang, J., A. L. Kolpak, and Z. Z. Bao. 2009. Myosin IIB isoform plays an essential role in the formation of two distinct types of macropinosomes. Cell Motil. Cytoskeleton 67:32-42.
35. Kovacs, M., F. Wang, A. Hu, Y. Zhang, and J. R. Sellers. 2003. Functional divergence of human cytoplasmic myosin II: kinetic characterization of the non-muscle IIA isoform. J. Biol. Chem. 278:38132-38140.
36. Lang, F., G. L. Busch, M. Ritter, H. Volkl, S. Waldegger, E. Gulbins, and D. Haussinger. 1998. Functional significance of cell volume regulatory mechanisms. Physiol. Rev. 78:247-306.
37. Loitto, V. M., T. Forslund, T. Sundqvist, K. E. Magnusson, and M. Gustafsson. 2002. Neutrophil leukocyte motility requires directed water influx. J. Leukoc. Biol. 71:212-222.
38. Lumb, R., K. Smith, P. J. O'Donoghue, and J. A. Lanser. 1988. Ultrastructure of the attachment of Cryptosporidium sporozoites to tissue culture cells. Parasitol. Res. 74:531-536.
39. Maciver, S. K. 1996. Myosin II function in non-muscle cells. Bioessays 18:179-182.
40. Marcial, M. A., and J. L. Madara. 1986. Cryptosporidium: cellular localization, structural analysis of absorptive cell-parasite membrane-membrane interactions in guinea pigs, and suggestion of protozoan transport by M cells. Gastroenterology 90:583-594.
41. Marinelli, R. A., L. Pham, P. Agre, and N. F. LaRusso. 1997. Secretin promotes osmotic water transport in rat cholangiocytes by increasing aquaporin-1 water channels in plasma membrane. Evidence for a secretin-induced vesicular translocation of aquaporin-1. J. Biol. Chem. 272:12984-12988.
42. Neco, P., D. Giner, S. Viniegra, R. Borges, A. Villarroel, and L. M. Gutierrez. 2004. New roles of myosin II during vesicle transport and fusion in chromaffin cells. J. Biol. Chem. 279:27450-27457.
43. Nelson, J. B., S. P. O'Hara, A. J. Small, P. S. Tietz, A. K. Choudhury, R. E. Pagano, X. M. Chen, and N. F. LaRusso. 2006. Cryptosporidium parvum infects human cholangiocytes via sphingolipid-enriched membrane microdomains. Cell. Microbiol. 8:1932-1945.
44. O'Hara, S. P., B. Q. Huang, X. M. Chen, J. Nelson, and N. F. LaRusso. 2005. Distribution of Cryptosporidium parvum sporozoite apical organelles during attachment to and internalization by cultured biliary epithelial cells. J. Parasitol. 91:995-999.
45. O'Hara, S. P., J. R. Yu, and J. J. Lin. 2004. A novel Cryptosporidium parvum antigen, CP2, preferentially associates with membranous structures. Parasitol. Res. 92:317-327.
46. Phillips, C. L., K. Yamakawa, and R. S. Adelstein. 1995. Cloning of the cDNA encoding human nonmuscle myosin heavy chain-B and analysis of human tissues with isoform-specific antibodies. J. Muscle Res. Cell Motil. 16:379-389.
47. Saadoun, S., M. C. Papadopoulos, M. Hara-Chikuma, and A. S. Verkman. 2005. Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434:786-792. (Pubitemid 44739524)
48. Saadoun, S., M. C. Papadopoulos, H. Watanabe, D. Yan, G. T. Manley, and A. S. Verkman. 2005. Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J. Cell Sci. 118:5691-5698. (Pubitemid 43079263)
49. Sandquist, J. C., K. I. Swenson, K. A. Demali, K. Burridge, and A. R. Means. 2006. Rho kinase differentially regulates phosphorylation of nonmuscle myosin II isoforms A and B during cell rounding and migration. J. Biol. Chem. 281:35873-35883.
50. Senba, S., M. Eto, and M. Yazawa. 1999. Identification of trimeric myosin phosphatase (PP1M) as a target for a novel PKC-potentiated protein phosphatase-1 inhibitory protein (CPI17) in porcine aorta smooth muscle. J. Biochem. 125:354-362. (Pubitemid 29112302)
51. Steimle, P. A., F. K. Fulcher, and Y. M. Patel. 2005. A novel role for myosin II in insulin-stimulated glucose uptake in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 331:1560-1565.
52. Togo, T., and R. A. Steinhardt. 2004. Nonmuscle myosin IIA and IIB have distinct functions in the exocytosis-dependent process of cell membrane repair. Mol. Biol. Cell 15:688-695.
53. Tzipori, S., and J. K. Griffiths. 1998. Natural history and biology of Cryptosporidium parvum. Adv. Parasitol. 40:5-36.
54. Tzipori, S., and H. Ward. 2002. Cryptosporidiosis: biology, pathogenesis and disease. Microbes Infect. 4:1047-1058.
55. Verkman, A. S., D. K. Binder, O. Bloch, K. Auguste, and M. C. Papadopoulos. 2006. Three distinct roles of aquaporin-4 in brain function revealed by knockout mice. Biochim. Biophys. Acta 1758:1085-1093.
56. Wetzel, D. M., J. Schmidt, M. S. Kuhlenschmidt, J. P. Dubey, and L. D. Sibley. 2005. Gliding motility leads to active cellular invasion by Cryptosporidium parvum sporozoites. Infect. Immun. 73:5379-5387.
57. Wilkinson, S., H. F. Paterson, and C. J. Marshall. 2005. Cdc42-MRCK and Rho-ROCK signalling cooperate in myosin phosphorylation and cell invasion. Nat. Cell Biol. 7:255-261.