The novel PAR-1-binding protein MTCL1 has crucial roles in organizing microtubules in polarizing epithelial cells

Journal of Cell Science

Volumn 126, Issue 20, 2013, Pages 4671-4683

  Sato, Yoshinori ^a   Akitsu, Masashi ^a   Amano, Yoshiko ^a   Yamashita, Kazunari ^a   Ide, Mariko ^a   Shimada, Kyoko ^a   Yamashita, Akio ^a   Hirano, Hisashi ^a   Arakawa, Noriaki ^a   Maki, Takahisa ^a   Hayashi, Ikuko ^a   Ohno, Shigeo ^a   Suzuki, Atsushi ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

Cell polarity; Epithelial cells; KIAA0802; MARK; MTCL1; Non centrosomal microtubules; PAR 1

Indexed keywords

MICROTUBULE CROSSLINKING FACTOR 1; MICROTUBULE PROTEIN; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 1B; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL ACTIVITY; CELL CULTURE; CELL GROWTH; CELL SUBPOPULATION; CENTROSOME; ENZYME ACTIVITY; EPITHELIUM CELL; FEMALE; HELA CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; MDCK CELL; MICROTUBULE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; RNA INTERFERENCE;

CELL POLARITY; EPITHELIAL CELLS; KIAA0802; MARK; MTCL1; NON-CENTROSOMAL MICROTUBULES; PAR-1;

ANIMALS; CELL POLARITY; CELLS, CULTURED; DOGS; EPITHELIAL CELLS; HEK293 CELLS; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; MADIN DARBY CANINE KIDNEY CELLS; MICE; MICROTUBULES; MORPHOGENESIS; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; TRANSFECTION;

EID: 84885446277     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.127845     Document Type: Article

References (38)

1. Baas, P. W. and Lin, S. (2011). Hooks and comets: The story of microtubule polarity orientation in the neuron. Dev. Neurobiol. 71, 403-418.
2. Bacallao, R., Antony, C., Dotti, C., Karsenti, E., Stelzer, E. H., and Simons, K. (1989). The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium. J. Cell Biol. 109, 2817-2832.
3. Bartolini, F., and Gundersen, G. G. (2006). Generation of noncentrosomal microtubule arrays. J. Cell Sci. 119, 4155-4163.
4. Bellett, G., Carter, J. M., Keynton, J., Goldspink, D., James, C., Moss, D. K., and Mogensen, M. M. (2009). Microtubule plus-end and minus-end capture at adherens junctions is involved in the assembly of apico-basal arrays in polarised epithelial cells. Cell Motil. Cytoskeleton 66, 893-908.
5. Bitan, A., Rosenbaum, I., and Abdu, U. (2012). Stable and dynamic microtubules coordinately determine and maintain Drosophila bristle shape. Development 139, 1987-1996.
6. Böhm, H., Brinkmann, V., Drab, M., Henske, A., and Kurzchalia, T. V. (1997). Mammalian homologues of C. elegans PAR-1 are asymmetrically localized in epithelial cells and may influence their polarity. Curr. Biol. 7, 603-606.
7. Bowen, J. R., Hwang, D., Bai, X., Roy, D., and Spiliotis, E. T. (2011). Septin GTPases spatially guide microtubule organization and plus end dynamics in polarizing epithelia. J. Cell Biol. 194, 187-197.
8. Bré, M. H., Kreis, T. E., and Karsenti, E. (1987). Control of microtubule nucleation and stability in Madin-Darby canine kidney cells: the occurrence of noncentrosomal, stable detyrosinated microtubules. J. Cell Biol. 105, 1283-1296.
9. Chapin, S. J., Bulinski, J. C., and Gundersen, G. G. (1991). Microtubule bundling in cells. Nature 349, 24.
10. Cohen, D., Brennwald, P. J., Rodriguez-Boulan, E., and Müsch, A. (2004). Mammalian PAR-1 determines epithelial lumen polarity by organizing the microtubule cytoskeleton. J. Cell Biol. 164, 717-727.
11. Cong, W., Hirose, T., Harita, Y., Yamashita, A., Mizuno, K., Hirano, H., and Ohno, S. (2010). ASPP2 regulates epithelial cell polarity through the PAR complex. Curr. Biol. 20, 1408-1414.
12. Cowerd, R. B., Asmar, M. M., Alderman, J. M., Alderman, E. A., Garland, A. L., Busby, W. H., Bodnar, W. M., Rusyn, I., Medoff, B. D., Tisch, R. et al. (2010). Adiponectin lowers glucose production by increasing SOGA. Am. J. Pathol. 177, 1936-1945.
13. Drewes, G., Ebneth, A., Preuss, U., Mandelkow, E. M., and Mandelkow, E. (1997). MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell 89, 297-308.
14. Grindstaff, K. K., Bacallao, R. L., and Nelson, W. J. (1998). Apiconuclear organization of microtubules does not specify protein delivery from the trans-Golgi network to different membrane domains in polarized epithelial cells. Mol. Biol. Cell 9, 685-699.
15. Hayashi, K., Suzuki, A., Hirai, S., Kurihara, Y., Hoogenraad, C. C., and Ohno, S. (2011). Maintenance of dendritic spine morphology by partitioning-defective 1b through regulation of microtubule growth. J. Neurosci. 31, 12094-12103.
16. Hotta, A., Kawakatsu, T., Nakatani, T., Sato, T., Matsui, C., Sukezane, T., Akagi, T., Hamaji, T., Grigoriev, I., Akhmanova, A. et al. (2010). Laminin-based cell adhesion anchors microtubule plus ends to the epithelial cell basal cortex through LL5alpha/beta. J. Cell Biol. 189, 901-917.
17. Jaulin, F., and Kreitzer, G. (2010). KIF17 stabilizes microtubules and contributes to epithelial morphogenesis by acting at MT plus ends with EB1 and APC. J. Cell Biol. 190, 443-460.
18. Keating, T. J., and Borisy, G. G. (1999). Centrosomal and non-centrosomal microtubules. Biol. Cell 91, 321-329.
19. Keating, T. J., Peloquin, J. G., Rodionov, V. I., Momcilovic, D., and Borisy, G. G. (1997). Microtubule release from the centrosome. Proc. Natl. Acad. Sci. USA 94, 5078-5083.
20. MacRae, T. H. (1992). Microtubule organization by cross-linking and bundling proteins. Biochim. Biophys. Acta 1160, 145-155.
21. Manning, A. L., and Compton, D. A. (2008). Structural and regulatory roles of nonmotor spindle proteins. Curr. Opin. Cell Biol. 20, 101-106.
22. Masuda-Hirata, M., Suzuki, A., Amano, Y., Yamashita, K., Ide, M., Yamanaka, T., Sakai, M., Imamura, M., and Ohno, S. (2009). Intracellular polarity protein PAR-1 regulates extracellular laminin assembly by regulating the dystroglycan complex. Genes Cells 14, 835-850.
23. Meads, T., and Schroer, T. A. (1995). Polarity and nucleation of microtubules in polarized epithelial cells. Cell Motil. Cytoskeleton 32, 273-288.
24. Mogensen, M. M., Tucker, J. B., and Stebbings, H. (1989). Microtubule polarities indicate that nucleation and capture of microtubules occurs at cell surfaces in Drosophila. J. Cell Biol. 108, 1445-1452.
25. Mogensen, M. M., Malik, A., Piel, M., Bouckson-Castaing, V., and Bornens, M. (2000). Microtubule minus-end anchorage at centrosomal and non-centrosomal sites: the role of ninein. J. Cell Sci. 113, 3013-3023.
26. Mogensen, M. M., Tucker, J. B., Mackie, J. B., Prescott, A. R., and Näthke, I. S. (2002). The adenomatous polyposis coli protein unambiguously localizes to microtubule plus ends and is involved in establishing parallel arrays of microtubule bundles in highly polarized epithelial cells. J. Cell Biol. 157, 1041-1048.
27. Mollinari, C., Kleman, J. P., Jiang, W., Schoehn, G., Hunter, T., and Margolis, R. L. (2002). PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J. Cell Biol. 157, 1175-1186.
28. Müsch, A. (2004). Microtubule organization and function in epithelial cells. Traffic 5, 1- 9.
29. Oriolo, A. S., Wald, F. A., Canessa, G., and Salas, P. J. (2007). GCP6 binds to intermediate filaments: a novel function of keratins in the organization of microtubules in epithelial cells. Mol. Biol. Cell 18, 781-794.
30. Radulescu, A. E., and Cleveland, D. W. (2010). NuMA after 30 years: the matrix revisited. Trends Cell Biol. 20, 214-222.
31. Spiliotis, E. T. (2010). Regulation of microtubule organization and functions by septin GTPases. Cytoskeleton (Hoboken) 67, 339-345.
32. Subramanian, R., Wilson-Kubalek, E. M., Arthur, C. P., Bick, M. J., Campbell, E. A., Darst, S. A., Milligan, R. A., and Kapoor, T. M. (2010). Insights into antiparallel microtubule crosslinking by PRC1, a conserved nonmotor microtubule binding protein. Cell 142, 433-443.
33. Suzuki, A., and Ohno, S. (2006). The PAR-aPKC system: lessons in polarity. J. Cell Sci. 119, 979-987.
34. Suzuki, A., Hirata, M., Kamimura, K., Maniwa, R., Yamanaka, T., Mizuno, K., Kishikawa, M., Hirose, H., Amano, Y., Izumi, N. et al. (2004). aPKC acts upstream of PAR-1b in both the establishment and maintenance of mammalian epithelial polarity. Curr. Biol. 14, 1425-1435.
35. Tanaka, J., Miwa, Y., Miyoshi, K., Ueno, A., and Inoue, H. (1999). Construction of Epstein-Barr virus-based expression vector containing mini-oriP. Biochem. Biophys. Res. Commun. 264, 938-943.
36. Vorobjev, I. A., and Nadezhdina, E. S. (1987). The centrosome and its role in the organization of microtubules. Int. Rev. Cytol. 106, 227-293.
37. Wolf, E., Kim, P. S., and Berger, B. (1997). MultiCoil: a program for predicting twoand three-stranded coiled coils. Protein Sci. 6, 1179-1189.
38. Yamashita, K., Suzuki, A., Satoh, Y., Ide, M., Amano, Y., Masuda-Hirata, M., Hayashi, Y. K., Hamada, K., Ogata, K., and Ohno, S. (2010). The 8th and 9th tandem spectrin-like repeats of utrophin cooperatively form a functional unit to interact with polarity-regulating kinase PAR-1b. Biochem. Biophys. Res. Commun. 391, 812-817.