Identification of mouse MARVELD1 as a microtubule associated protein that inhibits cell cycle progression and migration
Tóm tắt
MARVEL domain-containing 1 (MARVELD1) is a newly identified nuclear protein; however its function has not been clear until now. Here, we report that mouse MARVELD1 (mMARVELD1), which is highly conserved between mice and humans, exhibits cell cycle-dependent cellular localization. In NIH3T3 cells, MARVELD1 was observed in the nucleus and at the perinuclear region during interphase, but was localized at the mitotic spindle and midbody at metaphase, and a significant fraction of mMARVELD1 translocated to the plasma membrane during anaphase. In addition, treatment of cells with colchicine, a microtubuledepolymerizing agent, resulted in translocation of mMARVELD1 to the plasma membrane, and association of mMARVELD1 and α-tubulin was confirmed by co-immunoprecipitation. Finally, overexpression of mMARVELD1 resulted in a remarkable inhibition of cell proliferation, G1-phase arrest, and reduced cell migration. These findings indicate that mMARVELD1 is a microtubule-associated protein that plays an important role in cell cycle progression and migration.
Tài liệu tham khảo
Azakir, B.A., Di Fulvio, S., Therrien, C., and Sinnreich, M. (2010). Dysferlin interacts with tubulin and microtubules in mouse skeletal muscle. PLoS One 5, e10122.
Bollimuntha, S., Cornatzer, E., and Singh, B.B. (2005). Plasma membrane localization and function of TRPC1 is dependent on its interaction with beta-tubulin in retinal epithelium cells. Vis. Neurosci. 22, 163–170.
Bordier, C. (1981). Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 256, 1604–1607.
Dasso, M. (2001). Running on Ran: nuclear transport and the mitotic spindle. Cell 104, 321–324.
D’Assoro, A.B., Lingle, W.L., and Salisbury, J.L. (2002). Centrosome amplification and the development of cancer. Oncogene 21, 6146–6153.
Downing, K.H. (2000). Structural basis for the interaction of tubulin with proteins and drugs that affect microtubule dynamics. Annu. Rev. Cell Dev. Biol. 16, 89–111.
Doxsey, S.J. (2001). Centrosomes as command centres for cellular control. Nat. Cell Biol. 3, E105–E108.
Du, D., Xu, F., Yu, L., Zhang, C., Lu, X., Yuan, H., Huang, Q., Zhang, F., Bao, H., Jia, L., et al. (2010). The tight junction protein, occludin, regulates the directional migration of epithelial cells. Dev. Cell 18, 52–63.
Giannakakou, P., Sackett, D.L., Ward, Y., Webster, K.R., Blagosklonny, M.V., and Fojo, T. (2000). p53 is associated with cellular microtubules and is transported to the nucleus by dynein. Nat. Cell Biol. 2, 709–717.
Hsu, L.C., and White, R.L. (1998). BRCA1 is associated with the cen-trosome during mitosis. Proc. Natl. Acad. Sci. USA 95, 12983–12988.
Jason, A.K., and Don, W.C. (2001). Cell cycle: Some importin news about spindle assembly. Science 291, 1718–1719.
Kahana, J.A., and Cleveland, D.W. (2001). Cell cycle: Some importin news about spindle assembly. Science 291, 1718–1719.
Khodjakov, A., and Rieder, C.L. (2001). Centrosomes enhance the fidelity of cytokinesis in vertebrates and are required for cell cycle progression. J. Cell Biol. 153, 237–242.
Kirstetter, P., Schuster, M.B., Bereshchenko, O., Moore, S., Dvinge, H., Kurz, E., Theilgaard-Mönch, K., Månsson, R., Pedersen, T.A., Pabst, T., et al. (2008). Modeling of C/EBP alpha mutant acute myeloid leukemia reveals a common expression signature of committed myeloid leukemia-initiating cells. Cancer Cell 13, 299–310.
Landis, M.D., Seachrist, D.D., Montañez-Wiscovich, M.E., Danielpour, D., and Keri, R.A. (2005). Gene expression profiling of cancer progression reveals intrinsic regulation of transforming growth factor-beta signaling in ErbB2/Neu-induced tumors from transgenic mice. Oncogene 24, 5173–5190.
Liang, P., and MacRae, T.H. (1997). Molecular chaperones and the cytoskeleton. J. Cell Sci. 110, 1431–1440.
Lydersen, B.K., and Pettijohn, D.E. (1980). Human-specific nuclear protein that associates with the polar region of the mitotic apparatus: distribution in a human/hamster hybrid cell. Cell 22, 489–499.
Mimori-Kiyosue, Y., and Tsukita, S. (2003). “Search-and-capture” of microtubules through plus-end-binding proteins (+TIPs). J. Biochem. 134, 321–326.
Morris, V.B., Brammall, J., Noble, J., and Reddel, R. (2000). p53 localizes to the centrosomes and spindles of mitotic cells in the embryonic chick epiblast, human cell lines, and a human primary culture: an immunofluorescence study. Exp. Cell Res. 256, 122–130.
Nachury, M.V., Maresca, T.J., Salmon, W.C., Waterman-Storer, C.M., Heald, R., and Weis, K. (2001). Importin beta is a mitotic target of the small GTPase Ran in spindle assembly. Cell 104, 95–106.
O’Brate, A., and Giannakakou, P. (2003). The importance of p53 location: nuclear or cytoplasmic zip code? Drug Resist. Updat. 6, 313–322.
Patzke, S., Hauge, H., Sioud, M., Finne, E.F., Sivertsen, E.A., Delabie, J., Stokke, T., and Aasheim, H.C. (2005). Identification of a novel centrosome/microtubule-associated coiled-coil protein involved in cell-cycle progression and spindle organization. Oncogene 24, 1159–1173.
Raemaekers, T., Ribbeck, K., Beaudouin, J., Annaert, W., Van, C.M., Stockmans, I., Smets, N., Bouillon, R., Ellenberg, J., and Car-meliet, G. (2003). NuSAP, a novel microtubule-associated protein involved in mitotic spindle organization. J. Cell Biol. 162, 1017–1029.
Rosenblatt, J. (2005). Spindle assembly: asters part their separate ways. Nat. Cell Biol. 7, 219–222.
Sánchez-Pulido, L., Martín-Belmonte, F., Valencia, A., and Alonso, M.A. (2002). MARVEL: a conserved domain involved in membrane apposition events. Trends Biochem. Sci. 27, 599–601.
Shen, E., Lei, Y., Liu, Q., Zheng, Y., Song, C., Marc, J., Wang, Y., Sun, L., and Liang, Q. (2009). Identification and characterization of INMAP, a novel interphase nucleus and mitotic apparatus protein that is involved in spindle formation and cell cycle progression. Exp. Cell Res. 315, 1100–1116.
Shinmura, K., Bennett, R.A., Tarapore, P., and Fukasawa, K. (2007). Direct evidence for the role of centrosomally localized p53 in the regulation of centrosome duplication. Oncogene 26, 2939–2944.
Wang, S., Li, Y., Han, F., Hu, J., Yue, L., Yu, Y., Zhang, Y., He, J., Zheng, H., Shi, S., et al. (2009a). Identification and characterization of MARVELD1, a novel nuclear protein that is downregulated in multiple cancers and silenced by DNA methylation. Cancer Lett. 282, 77–86.
Wang, S., Xiao, S., He, J., Han, F., and Li, Y. (2009b). Identification of interaction between MARVELD1 and Importinβ1. Chin. J. Biochem. Mol. Biol. 25, 735–739. (In Chinese)
Wittmann, T., Wilm, M., Karsenti, E., and Vernos, I. (2000). TPX2, A novel xenopus MAP involved in spindle pole organization. J. Cell Biol. 149, 1405–1418.
Yang, C.H., Lambie, E.J., and Snyder, M. (1992). NuMA: an unusually long coiled-coil related protein in the mammalian nucleus. J. Cell Biol. 116, 1303–1317.