The MAL protein is crucial for proper membrane condensation at the ciliary base, which is required for primary cilium elongation

Journal of Cell Science

Volumn 128, Issue 12, 2015, Pages 2261-2270

  Reales, Elena ^a   Bernabé Rubio, Miguel ^a   Casares Arias, Javier ^a   Rentero, Carles ^b   Fernández Barrera, Jaime ^a   Rangel, Laura ^a   Correas, Isabel ^a   Enrich, Carlos ^b   Andrés, Germán ^a   Alonso, Miguel A ^a  

^a CSIC   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Centrosome; Condensed membranes; MAL; Primary ciliogenesis

Indexed keywords

CAVEOLIN 1; GALECTIN 3; MAL PROTEIN; MEMBRANE PROTEIN; RAB PROTEIN; RAB8 PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN; MAL PROTEIN, HUMAN; MESSENGER RNA; MYELIN AND LYMPHOCYTE PROTEIN; SMALL INTERFERING RNA;

3' UNTRANSLATED REGION; ANIMAL CELL; APICAL MEMBRANE; ARTICLE; CELL ELONGATION; CELL MEMBRANE; CELLULAR DISTRIBUTION; CENTROSOME; CILIATED EPITHELIUM CELL; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; EXOCYTOSIS; GENE SILENCING; KINETOSOME; MDCK CELL LINE; NONHUMAN; PERICENTRIOLAR REGION; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; DOG; ELECTRON MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; HUMAN; METABOLISM; MORPHOGENESIS; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ULTRASTRUCTURE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL MEMBRANE; CELLS, CULTURED; CENTROSOME; CILIA; DOGS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MADIN DARBY CANINE KIDNEY CELLS; MICROSCOPY, ELECTRON; MORPHOGENESIS; MYELIN AND LYMPHOCYTE-ASSOCIATED PROTEOLIPID PROTEINS; RAB GTP-BINDING PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 84932100932     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.164970     Document Type: Article

References (50)

1. Angus, K. L. and Griffiths, G. M. (2013). Cell polarisation and the immunological synapse. Curr. Opin. Cell Biol. 25, 85-91.
2. Anton, O. M., Andrés-Delgado, L., Reglero-Real, N., Batista, A. and Alonso, M. A. (2011). MAL protein controls protein sorting at the supramolecular activation cluster of human T lymphocytes. J. Immunol. 186, 6345-6356.
3. Bagatolli, L. A., Sanchez, S. A., Hazlett, T. and Gratton, E. (2003). Giant vesicles, Laurdan, and two-photon fluorescence microscopy: evidence of lipid lateral separation in bilayers. Methods Enzymol. 360, 481-500.
4. Chen, J. K., Taipale, J., Cooper, M. K. and Beachy, P. A. (2002). Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev. 16, 2743-2748.
5. Cheong, K. H., Zacchetti, D., Schneeberger, E. E. and Simons, K. (1999). VIP17/MAL, a lipid raft-associated protein, is involved in apical transport in MDCK cells. Proc. Natl. Acad. Sci. USA 96, 6241-6248.
6. Chih, B., Liu, P., Chinn, Y., Chalouni, C., Komuves, L. G., Hass, P. E., Sandoval, W. and Peterson, A. S. (2011). A ciliopathy complex at the transition zone protects the cilia as a privileged membrane domain. Nat. Cell Biol. 14, 61-72.
7. Das, A. and Guo, W. (2011). Rabs and the exocyst in ciliogenesis, tubulogenesis and beyond. Trends Cell Biol. 21, 383-386.
8. Finetti, F. and Baldari, C. T. (2013). Compartmentalization of signaling by vesicular trafficking: a shared building design for the immune synapse and the primary cilium. Immunol. Rev. 251, 97-112.
9. Follit, J. A., Tuft, R. A., Fogarty, K. E. and Pazour, G. J. (2006). The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol. Biol. Cell 17, 3781-3792.
10. Francis, S. S., Sfakianos, J., Lo, B. and Mellman, I. (2011). A hierarchy of signals regulates entry of membrane proteins into the ciliary membrane domain in epithelial cells. J. Cell Biol. 193, 219-233.
11. Gaus, K., Gratton, E., Kable, E. P. W., Jones, A. S., Gelissen, I., Kritharides, L. and Jessup, W. (2003). Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc. Nat. Acad. Sci. USA 100, 15554-15559.
12. Gaus, K., Zech, T. and Harder, T. (2006). Visualizing membrane microdomains by Laurdan 2-photon microscopy. Mol. Membr. Biol. 23, 41-48.
13. Gerdes, J. M., Davis, E. E. and Katsanis, N. (2009). The vertebrate primary cilium in development, homeostasis, and disease. Cell 137, 32-45.
14. Goetz, S. C. and Anderson, K. V. (2010). The primary cilium: a signalling centre during vertebrate development. Nat. Rev. Genet. 11, 331-344.
15. Hehnly, H., Chen, C.-T., Powers, C. M., Liu, H.-L. and Doxsey, S. (2012). The centrosome regulates the Rab11-dependent recycling endosome pathway at appendages of the mother centriole. Curr. Biol. 22, 1944-1950.
16. Heider, M. R. and Munson, M. (2012). Exorcising the exocyst complex. Traffic 13, 898-907.
17. Hildebrandt, F. and Otto, E. (2005). Cilia and centrosomes: a unifying pathogenic concept for cystic kidney disease? Nat. Rev. Genet. 6, 928-940.
18. Hildebrandt, F., Benzing, T. and Katsanis, N. (2011). Ciliopathies. N. Engl. J. Med. 364, 1533-1543.
19. Hu, Q., Milenkovic, L., Jin, H., Scott, M. P., Nachury, M. V., Spiliotis, E. T. and Nelson, W. J. (2010). A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 329, 436-439.
20. Ishikawa, H. and Marshall, W. F. (2011). Ciliogenesis: building the cell's antenna. Nat. Rev. Mol. Cell Biol. 12, 222-234.
21. Kee, H. L., Dishinger, J. F., Lynne Blasius, T., Liu, C.-J., Margolis, B. and Verhey, K. J. (2012). A size-exclusion permeability barrier and nucleoporins characterize a ciliary pore complex that regulates transport into cilia. Nat. Cell Biol. 14, 431-437.
22. Knodler, A., Feng, S., Zhang, J., Zhang, X., Das, A., Peränen, J. and Guo, W. (2010). Coordination of Rab8 and Rab11 in primary ciliogenesis. Proc. Natl. Acad. Sci. USA 107, 6346-6351.
23. Kreitzer, G., Schmoranzer, J., Low, S. H., Li, X., Gan, Y., Weimbs, T., Simon, S. M. and Rodriguez-Boulan, E. (2003). Three-dimensional analysis of post-Golgi carrier exocytosis in epithelial cells. Nat. Cell Biol. 5, 126-136.
24. Lim, Y. S., Chua, C. E. L. and Tang, B. L. (2011). Rabs and other small GTPases in ciliary transport. Biol. Cell 103, 209-221.
25. Lingwood, D. and Simons, K. (2010). Lipid rafts as a membrane-organizing principle. Science 327, 46-50.
26. Lisanti, M., Le Bivic, A., Saltiel, A. and Rodriguez-Boulan, E. (1990). Preferred apical distribution of glycosyl-phosphatidylinositol (GPI) anchored proteins: a highly conserved feature of the polarized epithelial cell phenotype. J. Mem. Biol. 113, 155-167.
27. Lisanti, M. and Rodriguez-Boulan, E. (1990). Glycophospholipid membrane anchoring provides clues to the mechanism of protein sorting in polarized epithelial cells. Trends Biochem. Sci. 15, 113-118.
28. Magal, L. G., Yaffe, Y., Shepshelovich, J., Aranda, J. F., de Marco, M. C., Gaus, K., Alonso, M. A. and Hirschberg, K. (2009). Clustering and lateral concentration of raft lipids by the MAL protein. Mol. Biol. Cell 20, 3751-3762.
29. Martin-Belmonte, F., Kremer, L., Albar, J., Marazuela, M. and Alonso, M. A. (1998). Expression of the MAL gene in the thyroid: the MAL proteolipid, a component of glycolipid-enriched membranes, is apically distributed in thyroid follicles. Endocrinology 139, 2077-2084.
30. Meder, D., Shevchenko, A., Simons, K. and Füllekrug, J. (2005). Gp135/podocalyxin and NHERF-2 participate in the formation of a preapical domain during polarization of MDCK cells. J. Cell Biol. 168, 303-313.
31. Milenkovic, L., Scott, M. P. and Rohatgi, R. (2009). Lateral transport of Smoothened from the plasmamembrane to themembrane of the cilium. J.Cell Biol. 187, 365-374.
32. Millán, J. and Alonso, M. A. (1998). MAL, a novel integral membrane protein of human T lymphocytes, associates with glycosylphosphatidylinositol-anchored proteins and Src-like tyrosine kinases. Eur. J. Immunol. 28, 3675-3684.
33. Novarino, G., Akizu, N. and Gleeson, J. G. (2011). Modeling human disease in humans: the ciliopathies. Cell 147, 70-79.
34. Owen, D. M., Rentero, C., Magenau, A., Abu-Siniyeh, A. and Gaus, K. (2011). Quantitative imaging of membrane lipid order in cells and organisms. Nat. Protoc. 7, 24-35.
35. Pazour, G. J., Dickert, B. L., Vucica, Y., Seeley, E. S., Rosenbaum, J. L., Witman, G. B. and Cole, D. G. (2000). Chlamydomonas IFT88 and Its mouse homologue, polycystic kidney disease gene Tg737, are required for assembly of cilia and flagella. J. Cell Biol. 151, 709-718.
36. Puertollano, R., Martín-Belmonte, F., Millán, J., de Marco, M. C., Albar, J. P., Kremer, L. and Alonso, M. A. (1999). The MAL proteolipid is necessary for normal apical transport and accurate sorting of the influenza virus hemagglutinin in Madin-Darby canine kidney cells. J. Cell Biol. 145, 141-151.
37. Reiter, J. F. and Mostov, K. (2006). Vesicle transport, cilium formation, and membrane specialization: the origins of a sensory organelle. Proc. Natl. Acad. Sci. USA 103, 18383-18384.
38. Rentero, C., Zech, T., Quinn, C. M., Engelhardt, K., Williamson, D., Grewal, T., Jessup, W., Harder, T. and Gaus, K. (2008). Functional implications of plasma membrane condensation for T cell activation. PLoS ONE 3, e2262.
39. Rosenbaum, J. L. andWitman, G. B. (2002). Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 3, 813-825.
40. Salisbury, J. L., Suino, K. M., Busby, R. and Springett, M. (2002). Centrin-2 is required for centriole duplication in mammalian cells. Curr. Biol. 12, 1287-1292.
41. Sorokin, S. (1962). Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J. Cell Biol. 15, 363-377.
42. Takiar, V., Mistry, K., Carmosino, M., Schaeren-Wiemers, N. and Caplan, M. J. (2012). VIP17/MAL expression modulates epithelial cyst formation and ciliogenesis. Am. J. Physiol. Cell Physiol. 303, C862-C871.
43. Torkko, J. M., Manninen, A., Schuck, S. and Simons, K. (2008). Depletion of apical transport proteins perturbs epithelial cyst formation and ciliogenesis. J. Cell Sci. 121, 1193-1203.
44. Vieira, O. V., Verkade, P., Manninen, A. and Simons, K. (2005). FAPP2 is involved in the transport of apical cargo in polarized MDCK cells. J. Cell Biol. 170, 521-526.
45. Vieira, O. V., Gaus, K., Verkade, P., Fullekrug, J., Vaz, W. L. C. and Simons, K. (2006). FAPP2, cilium formation, and compartmentalization of the apical membrane in polarized Madin-Darby canine kidney (MDCK) cells. Proc. Nat. Acad. Sci. USA 103, 18556-18561.
46. Wang, G., Krishnamurthy, K. and Bieberich, E. (2009). Regulation of primary cilia formation by ceramide. J. Lipid Res. 50, 2103-2110.
47. Watnick, T. and Germino, G. (2003). From cilia to cyst. Nat. Genet. 34, 355-356.
48. Westlake, C. J., Baye, L. M., Nachury, M. V., Wright, K. J., Ervin, K. E., Phu, L., Chalouni, C., Beck, J. S., Kirkpatrick, D. S., Slusarski, D. C. et al. (2011). Primary cilia membrane assembly is initiated by Rab11 and transport protein particle II (TRAPPII) complex-dependent trafficking of Rabin8 to the centrosome. Proc. Natl. Acad. Sci. USA 108, 2759-2764.
49. Yoshimura, S.-i., Egerer, J., Fuchs, E., Haas, A. K. and Barr, F. A. (2007). Functional dissection of Rab GTPases involved in primary cilium formation. J. Cell Biol. 178, 363-369.
50. Zuo, X., Guo, W. and Lipschutz, J. H. (2009). The exocyst protein sec10 is necessary for primary ciliogenesis and cystogenesis in vitro. Mol. Biol. Cell 20, 2522-2529.