Epithelial organization and cyst lumen expansion require efficient sec13-sec31-driven secretion

Journal of Cell Science

Volumn 125, Issue 3, 2012, Pages 673-684

  Townley, Anna K ^a   Schmidt, Katy ^a,b   Hodgson, Lorna ^a   Stephens, David J ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b MAX F PERUTZ LABORATORIES   (Austria)

Author keywords

COPII; Epithelial organization; ER export

Indexed keywords

COAT PROTEIN COMPLEX II; SEC13 PROTEIN; SEC31 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL EXPANSION; CELL STRAIN CACO 2; CELL STRUCTURE; CYST; CYST LUMEN; ENZYME INHIBITION; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; IN VIVO STUDY; INTESTINE EPITHELIUM; MEMBRANE TRANSPORT; MEMBRANE VESICLE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN SECRETION; ZEBRA FISH;

ANIMALS; BASE SEQUENCE; CACO-2 CELLS; CARRIER PROTEINS; COCULTURE TECHNIQUES; COP-COATED VESICLES; EXTRACELLULAR MATRIX; GENE KNOCKDOWN TECHNIQUES; HUMANS; INTESTINAL MUCOSA; MICROSCOPY, ELECTRON, TRANSMISSION; MORPHOGENESIS; RNA, SMALL INTERFERING; VESICULAR TRANSPORT PROTEINS; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 84858139859     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.091355     Document Type: Article

References (47)

1. Abrams, E. W. and Andrew, D. J. (2005). CrebA regulates secretory activity in the Drosophila salivary gland and epidermis. Development 132, 2743-2758.
2. Antonny, B., Madden, D., Hamamoto, S., Orci, L. and Schekman, R. (2001). Dynamics of the COPII coat with GTP and stable analogues. Nat. Cell Biol. 3, 531-537.
3. Antonny, B., Gounon, P., Schekman, R. and Orci, L. (2003). Self-assembly of minimal COPII cages. EMBO Rep. 4, 419-424.
4. Aridor, M., Bannykh, S. I., Rowe, T. and Balch, W. E. (1999). Cargo can modulate COPII vesicle formation from the endoplasmic reticulum. J. Biol. Chem. 274, 4389-4399.
5. Barlowe, C., Orci, L., Yeung, T., Hosobuchi, M., Hamamoto, S., Salama, N., Rexach, M. F., Ravazzola, M., Amherdt, M. and Schekman, R. (1994). COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77, 895-907.
6. Beck, K., Hunter, I. and Engel, J. (1990). Structure and function of laminin: anatomy of a multidomain glycoprotein. FASEB J. 4, 148-160.
7. Bi, X., Mancias, J. D. and Goldberg, J. (2007). Insights into COPII coat nucleation from the structure of Sec23*Sar1 complexed with the active fragment of Sec31. Dev. Cell 13, 635-645.
8. Bornens, M. (2008). Organelle positioning and cell polarity. Nat. Rev. Mol. Cell Biol. 9, 874-886.
9. Boyadjiev, S. A., Fromme, J. C., Ben, J., Chong, S. S., Nauta, C., Hur, D. J., Zhang, G., Hamamoto, S., Schekman, R., Ravazzola, M. et al. (2006). Cranio-lenticulosutural dysplasia is caused by a SEC23A mutation leading to abnormal endoplasmicreticulum-to-Golgi trafficking. Nat. Genet. 38, 1192-1197.
10. Bryant, D. M. and Mostov, K. E. (2008). From cells to organs: building polarized tissue. Nat. Rev. Mol. Cell Biol. 9, 887-901.
11. Canty, E. G. and Kadler, K. E. (2005). Procollagen trafficking, processing and fibrillogenesis. J. Cell Sci. 118, 1341-1353.
12. d'Enfert, C., Wuestehube, L. J., Lila, T. and Schekman, R. (1991). Sec12p-dependent membrane binding of the small GTP-binding protein Sar1p promotes formation of transport vesicles from the ER. J. Cell Biol. 114, 663-670.
13. De Arcangelis, A., Neuville, P., Boukamel, R., Lefebvre, O., Kedinger, M. and Simon-Assmann, P. (1996). Inhibition of laminin alpha 1-chain expression leads to alteration of basement membrane assembly and cell differentiation. J. Cell Biol. 133, 417-430.
14. Farach-Carson, M. C. and Carson, D. D. (2007). Perlecan - a multifunctional extracellular proteoglycan scaffold. Glycobiology 17, 897-905.
15. Forster, D., Armbruster, K. and Luschnig, S. (2010). Sec24-dependent secretion drives cell-autonomous expansion of tracheal tubes in Drosophila. Curr. Biol. 20, 62-68.
16. Fromme, J. C. and Schekman, R. (2005). COPII-coated vesicles: flexible enough for large cargo? Curr. Opin. Cell Biol. 17, 345-352.
17. Fromme, J. C., Ravazzola, M., Hamamoto, S., Al-Balwi, M., Eyaid, W., Boyadjiev, S. A., Cosson, P., Schekman, R. and Orci, L. (2007). The genetic basis of a craniofacial disease provides insight into COPII coat assembly. Dev. Cell 13, 623-634.
18. Grant, D. S., Kleinman, H. K., Leblond, C. P., Inoue, S., Chung, A. E. and Martin, G. R. (1985). The basement-membrane-like matrix of the mouse EHS tumor: II. Immunohistochemical quantitation of six of its components. Am. J. Anat. 174, 387-398.
19. Grieder, N. C., Caussinus, E., Parker, D. S., Cadigan, K., Affolter, M. and Luschnig, S. (2008). gammaCOP is required for apical protein secretion and epithelial morphogenesis in Drosophila melanogaster. PLoS ONE 3, e3241.
20. Hughes, H. and Stephens, D. J. (2008). Assembly, organization, and function of the COPII coat. Histochem. Cell Biol. 129, 129-151.
21. Ivanov, A. I., Hopkins, A. M., Brown, G. T., Gerner-Smidt, K., Babbin, B. A., Parkos, C. A. and Nusrat, A. (2008). Myosin II regulates the shape of threedimensional intestinal epithelial cysts. J. Cell Sci. 121, 1803-1814.
22. Jaffe, A. B., Kaji, N., Durgan, J. and Hall, A. (2008). Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis. J. Cell Biol. 183, 625-633.
23. Jayaram, S. A., Senti, K. A., Tiklova, K., Tsarouhas, V., Hemphala, J. and Samakovlis, C. (2008). COPI vesicle transport is a common requirement for tube expansion in Drosophila. PLoS ONE 3, e1964.
24. Kedinger, M., Lefebvre, O., Duluc, I., Freund, J. N. and Simon-Assmann, P. (1998). Cellular and molecular partners involved in gut morphogenesis and differentiation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 847-856.
25. Kuehn, M. J., Herrmann, J. M. and Schekman, R. (1998). COPII-cargo interactions direct protein sorting into ER-derived transport vesicles. Nature 391, 187-190.
26. Long, K. R., Yamamoto, Y., Baker, A. L., Watkins, S. C., Coyne, C. B., Conway, J. F. and Aridor, M. (2010). Sar1 assembly regulates membrane constriction and ER export. J. Cell Biol. 190, 115-128.
27. Martin-Belmonte, F., Yu, W., Rodriguez-Fraticelli, A. E., Ewald, A. J., Werb, Z., Alonso, M. A. and Mostov, K. (2008). Cell-polarity dynamics controls the mechanism of lumen formation in epithelial morphogenesis. Curr. Biol. 18, 507-513.
28. Matsuoka, K., Orci, L., Amherdt, M., Bednarek, S. Y., Hamamoto, S., Schekman, R. and Yeung, T. (1998). COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes. Cell 93, 263-275.
29. Matsuoka, K., Schekman, R., Orci, L. and Heuser, J. E. (2001). Surface structure of the COPII-coated vesicle. Proc. Natl. Acad. Sci. USA 98, 13705-13709.
30. Mellman, I. and Nelson, W. J. (2008). Coordinated protein sorting, targeting and distribution in polarized cells. Nat. Rev. Mol. Cell Biol. 9, 833-845.
31. Mironov, A. A., Beznoussenko, G. V., Trucco, A., Lupetti, P., Smith, J. D., Geerts, W. J., Koster, A. J., Burger, K. N., Martone, M. E., Deerinck, T. J. et al. (2003). ER-to-Golgi carriers arise through direct en bloc protrusion and multistage maturation of specialized ER exit domains. Dev. Cell 5, 583-594.
32. Norum, M., Tang, E., Chavoshi, T., Schwarz, H., Linke, D., Uv, A. and Moussian, B. (2010). Trafficking through COPII stabilises cell polarity and drives secretion during Drosophila epidermal differentiation. PLoS One 5, e10802.
33. O'Brien, L. E., Jou, T. S., Pollack, A. L., Zhang, Q., Hansen, S. H., Yurchenco, P. and Mostov, K. E. (2001). Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat. Cell Biol. 3, 831-838.
34. O'Donnell, J., Maddox, K. and Stagg, S. (2010). The structure of a COPII tubule. J. Struct. Biol. 173, 358-364.
35. Rossi, M., Morita, H., Sormunen, R., Airenne, S., Kreivi, M., Wang, L., Fukai, N., Olsen, B. R., Tryggvason, K. and Soininen, R. (2003). Heparan sulfate chains of perlecan are indispensable in the lens capsule but not in the kidney. EMBO J. 22, 236-245.
36. Saito, K., Chen, M., Bard, F., Chen, S., Zhou, H., Woodley, D., Polischuk, R., Schekman, R. and Malhotra, V. (2009). TANGO1 facilitates cargo loading at endoplasmic reticulum exit sites. Cell 136, 891-902.
37. Salama, N. R., Chuang, J. S. and Schekman, R. W. (1997). Sec31 encodes an essential component of the COPII coat required for transport vesicle budding from the endoplasmic reticulum. Mol. Biol. Cell 8, 205-217.
38. Schmidt, K. and Stephens, D. J. (2010). Cargo loading at the ER. Mol. Membr. Biol. 27, 398-411.
39. Simon-Assmann, P., Lefebvre, O., Bellissent-Waydelich, A., Olsen, J., Orian-Rousseau, V. and De Arcangelis, A. (1998). The laminins: role in intestinal morphogenesis and differentiation. Ann. N. Y. Acad. Sci. 859, 46-64.
40. Stagg, S. M., Gurkan, C., Fowler, D. M., LaPointe, P., Foss, T. R., Potter, C. S., Carragher, B. and Balch, W. E. (2006). Structure of the Sec13/31 COPII coat cage. Nature 439, 234-238.
41. Stagg, S. M., LaPointe, P., Razvi, A., Gurkan, C., Potter, C. S., Carragher, B. and Balch, W. E. (2008). Structural basis for cargo regulation of COPII coat assembly. Cell 134, 474-484.
42. Timpl, R. (1996). Macromolecular organization of basement membranes. Curr. Opin. Cell Biol. 8, 618-624.
43. Townley, A. K. and Stephens, D. J. (2009). Vesicle coating and uncoating - controlling the formation of large COPII-coated carriers. F1000 Biol. Rep. 1, 65.
44. Townley, A. K., Feng, Y., Schmidt, K., Carter, D. A., Porter, R., Verkade, P. and Stephens, D. J. (2008). Efficient coupling of Sec23-Sec24 to Sec13-Sec31 drives COPII-dependent collagen secretion and is essential for normal craniofacial development. J. Cell Sci. 121, 3025-3034.
45. Tsarouhas, V., Senti, K. A., Jayaram, S. A., Tiklova, K., Hemphala, J., Adler, J. and Samakovlis, C. (2007). Sequential pulses of apical epithelial secretion and endocytosis drive airway maturation in Drosophila. Dev. Cell 13, 214-225.
46. Weston, C. A., Anova, L., Rialas, C., Prives, J. M. andWeeks, B. S. (2000). Laminin-1 activates Cdc42 in the mechanism of laminin-1-mediated neurite outgrowth. Exp. Cell Res. 260, 374-378.
47. Wilson, D. G., Phamluong, K., Li, L., Sun, M., Cao, T. C., Liu, P. S., Modrusan, Z., Sandoval, W. N., Rangell, L., Carano, R. A. et al. (2011). Global defects in collagen secretion in a Mia3/TANGO1 knockout mouse. J. Cell Biol. 193, 935-951.