Adducins regulate remodeling of apical junctions in human epithelial cells

Molecular Biology of the Cell

Volumn 21, Issue 20, 2010, Pages 3506-3517

  Naydenov, Nayden G ^a   Ivanov, Andrei I ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADDUCIN; ALPHA ADDUCIN; BETA CATENIN; F ACTIN; GAMMA ADDUCIN; PROTEIN KINASE C; SMALL INTERFERING RNA; SPECTRIN; UNCLASSIFIED DRUG; UVOMORULIN;

ARTICLE; CELL JUNCTION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; EPITHELIUM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TIGHT JUNCTION;

ACTINS; ADHERENS JUNCTIONS; CALCIUM; CALMODULIN-BINDING PROTEINS; CELL LINE; CELL POLARITY; CYTOSKELETON; DOWN-REGULATION; ENZYME ACTIVATION; EPITHELIAL CELLS; GENE KNOCKDOWN TECHNIQUES; HUMANS; INTESTINES; PANCREAS; PROTEIN ISOFORMS; PROTEIN KINASE C; PROTEIN TRANSPORT; RNA, MESSENGER; RNA, SMALL INTERFERING; SPECTRIN; TIGHT JUNCTIONS;

EID: 77958043359     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-03-0259     Document Type: Article

References (79)

1. Abdi, K. M., and Bennett, V. (2008). Adducin promotes micrometer-scale organization of beta2-spectrin in lateral membranes of bronchial epithelial cells. Mol. Biol. Cell 19, 536-545.
2. Anderson, J. M., and Van Itallie, C. M. (2009). Physiology and function of the tight junction. Cold Spring Harbor Perspect. Biol. 1, a002584.
3. Baines, A. J. (2009). Evolution of spectrin function in cytoskeletal and membrane networks. Biochem. Soc. Trans. 37, 796-803.
4. Barkalow, K. L., Italiano, J. E., Jr., Chou, D. E., Matsuoka, Y., Bennett, V., and Hartwig, J. H. (2003). Alpha-adducin dissociates from F-actin and spectrin during platelet activation. J. Cell Biol. 161, 557-570.
5. Bennett, V., and Baines, A. J. (2001). Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol. Rev. 81, 1353-1392.
6. Bennett, V., and Healy, J. (2008). Organizing the fluid membrane bilayer: diseases linked to spectrin and ankyrin. Trends Mol. Med. 14, 28-36.
7. Bershadsky, A. (2004). Magic touch: how does cell-cell adhesion trigger actin assembly? Trends Cell Biol. 14, 589-593.
8. Bryant, D. M., and Stow, J. L. (2004). The ins and outs of E-cadherin trafficking. Trends Cell Biol. 14, 427-434.
9. Capaldo, C. T., and Macara, I. G. (2007). Depletion of E-cadherin disrupts establishment but not maintenance of cell junctions in Madin-Darby canine kidney epithelial cells. Mol. Biol. Cell 18, 189-200.
10. Cavey, M., and Lecuit, T. (2009). Molecular bases of cell-cell junctions stability and dynamics. Cold Spring Harbor Perspect Biol. 1, a002998.
11. Cereijido, M., Robbins, E. S., Dolan, W. J., Rotunno, C. A., and Sabatini, D. D. (1978). Polarized monolayers formed by epithelial cells on a permeable and translucent support. J. Cell Biol. 77, 853-880.
12. Chu, H. G., Weeks, S. K., Gilligan, D. M., and Rockey, D. D. (2008). Host alpha-adducin is redistributed and localized to the inclusion membrane in chlamydia- and chlamydophila-infected cells. Microbiology 154, 3848-3855.
13. Dong, L., Chapline, C., Mousseau, B., Fowler, L., Ramsay, K., Stevens, J. L., and Jaken, S. (1995). 35H, a sequence isolated as a protein kinase C binding protein, is a novel member of the adducin family. J. Biol. Chem. 270, 25534-25540.
14. Drenckhahn, D., and Bennett, V. (1987). Polarized distribution of Mr 210,000 and 190,000 analogs of erythrocyte ankyrin along the plasma membrane of transporting epithelia, neurons and photoreceptors. Eur. J. Cell Biol. 43, 479-486.
15. Ferrandi, M., et al. (2010). alpha- and beta-Adducin polymorphisms affect podocyte proteins and proteinuria in rodents and decline of renal function in human IgA nephropathy. J. Mol. Med. 88, 203-217.
16. Fowler, L., Dong, L., Bowes, R. C., 3rd, van de Water, B., Stevens, J. L., and Jaken, S. (1998). Transformation-sensitive changes in expression, localization, and phosphorylation of adducins in renal proximal tubule epithelial cells. Cell Growth Differ. 9, 177-184.
17. Giepmans, B. N., and van Ijzendoorn, S. C. (2009). Epithelial cell-cell junctions and plasma membrane domains. Biochim. Biophys. Acta 1788, 820-831.
18. Gonzalez-Mariscal, L., Contreras, R. G., Bolivar, J. J., Ponce, A., Chavez De Ramirez, B., and Cereijido, M. (1990). Role of calcium in tight junction formation between epithelial cells. Am. J. Physiol. 259, C978-C986.
19. Gonzalez-Mariscal, L., Tapia, R., and Chamorro, D. (2008). Crosstalk of tight junction components with signaling pathways. Biochim. Biophys. Acta 1778, 729-756.
20. Hartsock, A., and Nelson, W. J. (2008). Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim. Biophys. Acta 1778, 660-669.
21. Hong, S., Troyanovsky, R. B., and Troyanovsky, S. M. (2010). Spontaneous assembly and active disassembly balance adherens junction homeostasis. Proc. Natl. Acad. Sci. USA 107, 3528-3533.
22. Hughes, C. A., and Bennett, V. (1995). Adducin: a physical model with implications for function in assembly of spectrin-actin complexes. J. Biol. Chem. 270, 18990-18996.
23. Ivanov, A. I., Bachar, M., Babbin, B. A., Adelstein, R. S., Nusrat, A., and Parkos, C. A. (2007). A unique role for nonmuscle myosin heavy chain IIA in regulation of epithelial apical junctions. PLoS ONE 2, e658.
24. Ivanov, A. I., Hunt, D., Utech, M., Nusrat, A., and Parkos, C. A. (2005a). Differential roles for actin polymerization and a myosin II motor in assembly of the epithelial apical junctional complex. Mol. Biol. Cell 16, 2636-2650.
25. Ivanov, A. I., McCall, I. C., Parkos, C. A., and Nusrat, A. (2004a). Role for actin filament turnover and a myosin II motor in cytoskeleton-driven disassembly of the epithelial apical junctional complex. Mol. Biol. Cell 15, 2639-2651.
26. Ivanov, A. I., Nusrat, A., and Parkos, C. A. (2004b). Endocytosis of epithelial apical junctional proteins by a clathrin-mediated pathway into a unique storage compartment. Mol. Biol. Cell 15, 176-188.
27. Ivanov, A. I., Nusrat, A., and Parkos, C. A. (2005b). Endocytosis of the apical junctional complex: mechanisms and possible roles in regulation of epithelial barriers. Bioessays 27, 356-365.
28. Ivanov, A. I., Samarin, S. N., Bachar, M., Parkos, C. A., and Nusrat, A. (2009). Protein kinase C activation disrupts epithelial apical junctions via ROCK-II dependent stimulation of actomyosin contractility. BMC Cell Biol. 10, 36.
29. Ivanov, A. I., Young, C., Beste, K. D., Capaldo, C. T., Humbert, P. O., Brennwald, P., Parkos, C. A., and Nusrat, A. (2010). Tumor suppressor scribble regulates assembly of tight junctions in the intestinal epithelium. Am. J. Pathol. 176, 134-145.
30. Jackson, A. L., and Linsley, P. S. (2010). Recognizing and avoiding siRNA off-target effects for target identification and therapeutic application. Nat. Rev. Drug Discov. 9, 57-67.
31. Joshi, R., Gilligan, D. M., Otto, E., McLaughlin, T., and Bennett, V. (1991). Primary structure and domain organization of human alpha and beta adducin. J. Cell Biol. 115, 665-675.
32. Kaiser, H. W., O'Keefe, E., and Bennett, V. (1989). Adducin: Ca++-dependent association with sites of cell-cell contact. J. Cell Biol. 109, 557-569. (Pubitemid 19197018)
33. Kamei, T., Matozaki, T., Sakisaka, T., Kodama, A., Yokoyama, S., Peng, Y. F., Nakano, K., Takaishi, K., and Takai, Y. (1999). Coendocytosis of cadherin and c-Met coupled to disruption of cell-cell adhesion in MDCK cells-regulation by Rho, Rac and Rab small G proteins. Oncogene 18, 6776-6784.
34. Kimura, K., Fukata, Y., Matsuoka, Y., Bennett, V., Matsuura, Y., Okawa, K., Iwamatsu, A., and Kaibuchi, K. (1998). Regulation of the association of adducin with actin filaments by Rho-associated kinase (Rho-kinase) and myosin phosphatase. J. Biol. Chem. 273, 5542-5548.
35. Kizhatil, K., and Bennett, V. (2004). Lateral membrane biogenesis in human bronchial epithelial cells requires 190-kDa ankyrin-G. J. Biol. Chem. 279, 16706-16714.
36. Kizhatil, K., Davis, J. Q., Davis, L., Hoffman, J., Hogan, B. L., and Bennett, V. (2007a). Ankyrin-G is a molecular partner of E-cadherin in epithelial cells and early embryos. J. Biol. Chem. 282, 26552-26561.
37. Kizhatil, K., Yoon, W., Mohler, P. J., Davis, L. H., Hoffman, J. A., and Bennett, V. (2007b). Ankyrin-G and beta2-spectrin collaborate in biogenesis of lateral membrane of human bronchial epithelial cells. J. Biol. Chem. 282, 2029-2037.
38. Krendel, M., Gloushankova, N. A., Bonder, E. M., Feder, H. H., Vasiliev, J. M., and Gelfand, I. M. (1999). Myosin-dependent contractile activity of the actin cytoskeleton modulates the spatial organization of cell-cell contacts in cultured epitheliocytes. Proc. Natl. Acad. Sci. USA 96, 9666-9670.
39. Kuhlman, P. A., Hughes, C. A., Bennett, V., and Fowler, V. M. (1996). A new function for adducin. Calcium/calmodulin-regulated capping of the barbed ends of actin filaments. J. Biol. Chem. 271, 7986-7991.
40. Le Bivic, A., Real, F. X., and Rodriguez-Boulan, E. (1989). Vectorial targeting of apical and basolateral plasma membrane proteins in a human adenocarcinoma epithelial cell line. Proc. Natl. Acad. Sci. USA 86, 9313-9317.
41. Le, T. L., Yap, A. S., and Stow, J. L. (1999). Recycling of E-cadherin: a potential mechanism for regulating cadherin dynamics. J. Cell Biol. 146, 219-232.
42. Li, X., Matsuoka, Y., and Bennett, V. (1998). Adducin preferentially recruits spectrin to the fast growing ends of actin filaments in a complex requiring the MARCKS-related domain and a newly defined oligomerization domain. J. Biol. Chem. 273, 19329-19338.
43. Low, S. H., Miura, M., Roche, P. A., Valdez, A. C., Mostov, K. E., and Weimbs, T. (2000). Intracellular redirection of plasma membrane trafficking after loss of epithelial cell polarity. Mol. Biol. Cell 11, 3045-3060.
44. Ma, T. Y., Tran, D., Hoa, N., Nguyen, D., Merryfield, M., and Tarnawski, A. (2000). Mechanism of extracellular calcium regulation of intestinal epithelial tight junction permeability: role of cytoskeletal involvement. Microsc. Res. Tech. 51, 156-168.
45. Marrs, J. A., Napolitano, E. W., Murphy-Erdosh, C., Mays, R. W., Reichardt, L. F., and Nelson, W. J. (1993). Distinguishing roles of the membrane-cytoskeleton and cadherin mediated cell-cell adhesion in generating different Na+,K(+)-ATPase distributions in polarized epithelia. J. Cell Biol. 123, 149-164.
46. Matou-Nasri, S., Gaffney, J., Kumar, S., and Slevin, M. (2009). Oligosaccharides of hyaluronan induce angiogenesis through distinct CD44 and RHAMM-mediated signalling pathways involving Cdc2 and gamma-adducin. Int. J. Oncol. 35, 761-773.
47. Matsuoka, Y., Li, X., and Bennett, V. (1998). Adducin is an in vivo substrate for protein kinase C: phosphorylation in the MARCKS-related domain inhibits activity in promoting spectrin-actin complexes and occurs in many cells, including dendritic spines of neurons. J. Cell Biol. 142, 485-497.
48. Matsuoka, Y., Li, X., and Bennett, V. (2000). Adducin: structure, function and regulation. Cell Mol. Life Sci. 57, 884-895.
49. McNeil, E., Capaldo, C. T., and Macara, I. G. (2006). Zonula occludens-1 function in the assembly of tight junctions in Madin-Darby canine kidney epithelial cells. Mol. Biol. Cell 17, 1922-1932.
50. Mische, S. M., Mooseker, M. S., and Morrow, J. S. (1987). Erythrocyte adducin: a calmodulin-regulated actin-bundling protein that stimulates spectrin-actin binding. J. Cell Biol. 105, 2837-2845.
51. Mohandas, N., and Gallagher, P. G. (2008). Red cell membrane: past, present, and future. Blood 112, 3939-3948.
52. Nejsum, L. N., and Nelson, W. J. (2007). A molecular mechanism directly linking E-cadherin adhesion to initiation of epithelial cell surface polarity. J. Cell Biol. 178, 323-335.
53. Nelson, W. J., Shore, E. M., Wang, A. Z., and Hammerton, R. W. (1990). Identification of a membrane-cytoskeletal complex containing the cell adhesion molecule uvomorulin (E-cadherin), ankyrin, and fodrin in Madin-Darby canine kidney epithelial cells. J. Cell Biol. 110, 349-357.
54. Nelson, W. J., and Veshnock, P. J. (1986). Dynamics of membrane-skeleton (fodrin) organization during development of polarity in Madin-Darby canine kidney epithelial cells. J. Cell Biol. 103, 1751-1765.
55. Niessen, C. M., and Gottardi, C. J. (2008). Molecular components of the adherens junction. Biochim. Biophys. Acta 1778, 562-571.
56. Paris, L., Tonutti, L., Vannini, C., and Bazzoni, G. (2008). Structural organization of the tight junctions. Biochim. Biophys. Acta 1778, 646-659.
57. Pariser, H., Herradon, G., Ezquerra, L., Perez-Pinera, P., and Deuel, T. F. (2005). Pleiotrophin regulates serine phosphorylation and the cellular distribution of beta-adducin through activation of protein kinase C. Proc. Natl. Acad. Sci. USA 102, 12407-12412.
58. Perez-Moreno, M., Jamora, C., and Fuchs, E. (2003). Sticky business: orchestrating cellular signals at adherens junctions. Cell 112, 535-548. (Pubitemid 36263085)
59. Perez, T. D., Tamada, M., Sheetz, M. P., and Nelson, W. J. (2008). Immediate-early signaling induced by E-cadherin engagement and adhesion. J. Biol. Chem. 283, 5014-5022.
60. Pitelka, D. R., Taggart, B. N., and Hamamoto, S. T. (1983). Effects of extracellular calcium depletion on membrane topography and occluding junctions of mammary epithelial cells in culture. J. Cell Biol. 96, 613-624.
61. Pokutta, S., and Weis, W. I. (2007). Structure and mechanism of cadherins and catenins in cell-cell contacts. Annu. Rev. Cell Dev. Biol. 23, 237-261.
62. Pradhan, D., Lombardo, C. R., Roe, S., Rimm, D. L., and Morrow, J. S. (2001). alpha-Catenin binds directly to spectrin and facilitates spectrin-membrane assembly in vivo. J. Biol. Chem. 276, 4175-4181.
63. Rajasekaran, S. A., Gopal, J., Espineda, C., Ryazantsev, S., Schneeberger, E. E., and Rajasekaran, A. K. (2004). HPAF-II, a cell culture model to study pancreatic epithelial cell structure and function. Pancreas 29, e77-e83.
64. Robledo, R. F., Ciciotte, S. L., Gwynn, B., Sahr, K. E., Gilligan, D. M., Mohandas, N., and Peters, L. L. (2008). Targeted deletion of alpha-adducin results in absent beta- and gamma-adducin, compensated hemolytic anemia, and lethal hydrocephalus in mice. Blood 112, 4298-4307.
65. Sahr, K. E., Lambert, A. J., Ciciotte, S. L., Mohandas, N., and Peters, L. L. (2009). Targeted deletion of the gamma-adducin gene (Add3) in mice reveals differences in alpha-adducin interactions in erythroid and nonerythroid cells. Am. J. Hematol. 84, 354-361.
66. Scott, J. A., Shewan, A. M., den Elzen, N. R., Loureiro, J. J., Gertler, F. B., and Yap, A. S. (2006). Ena/VASP proteins can regulate distinct modes of actin organization at cadherin-adhesive contacts. Mol. Biol. Cell 17, 1085-1095.
67. Shen, L., and Turner, J. R. (2005). Actin depolymerization disrupts tight junctions via caveolae-mediated endocytosis. Mol. Biol. Cell 16, 3919-3936.
68. Shewan, A. M., Maddugoda, M., Kraemer, A., Stehbens, S. J., Verma, S., Kovacs, E. M., and Yap, A. S. (2005). Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol. Biol. Cell 16, 4531-4542.
69. Smutny, M., Cox, H. L., Leerberg, J. M., Kovacs, E. M., Conti, M. A., Ferguson, C., Hamilton, N. A., Parton, R. G., Adelstein, R. S., and Yap, A. S. (2010). Myosin II isoforms identify distinct functional modules that support integrity of the epithelial zonula adherens. Nat. Cell Biol. 12, 696-702.
70. Takai, Y., and Nakanishi, H. (2003). Nectin and afadin: novel organizers of intercellular junctions. J. Cell Sci. 116, 17-27.
71. Taylor, K. A., and Taylor, D. W. (1994). Formation of two-dimensional complexes of F-actin and crosslinking proteins on lipid monolayers: demonstration of unipolar alpha-actinin-F-actin crosslinking. Biophys. J. 67, 1976-1983.
72. Thomas, G. H. (2001). Spectrin: the ghost in the machine. Bioessays 23, 152-160.
73. Troyanovsky, R. B., Sokolov, E. P., and Troyanovsky, S. M. (2006). Endocytosis of cadherin from intracellular junctions is the driving force for cadherin adhesive dimer disassembly. Mol. Biol. Cell 17, 3484-3493.
74. Tsukita, S., Furuse, M., and Itoh, M. (2001). Multifunctional strands in tight junctions. Nat. Rev. Mol. Cell Biol. 2, 285-293.
75. Turner, J. R. (2009). Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 9, 799-809.
76. van de Water, B., Tijdens, I. B., Verbrugge, A., Huigsloot, M., Dihal, A. A., Stevens, J. L., Jaken, S., and Mulder, G. J. (2000). Cleavage of the actin-capping protein alpha-adducin at Asp-Asp-Ser-Asp633-Ala by caspase-3 is preceded by its phosphorylation on serine 726 in cisplatin-induced apoptosis of renal epithelial cells. J. Biol. Chem. 275, 25805-25813.
77. Volberg, T., Geiger, B., Kartenbeck, J., and Franke, W. W. (1986). Changes in membrane-microfilament interaction in intercellular adherens junctions upon removal of extracellular Ca2+ ions. J. Cell Biol. 102, 1832-1842.
78. Yap, A. S., Crampton, M. S., and Hardin, J. (2007). Making and breaking contacts: the cellular biology of cadherin regulation. Curr. Opin. Cell Biol. 19, 508-514.
79. Yue, L., and Spradling, A. C. (1992). hu-li tai shao, a gene required for ring canal formation during Drosophila oogenesis, encodes a homolog of adducin. Genes Dev. 6, 2443-2454.