Rassf5 and Ndr kinases regulate neuronal polarity through Par3 phosphorylation in a novel pathway

Journal of Cell Science

Volumn 127, Issue 16, 2014, Pages 3463-3476

  Yang, Rui ^a,c   Kong, Eryan ^a,d   Jin, Jing ^a   Hergovich, Alexander ^b   Püschel, Andreas W ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Axon formation; Cell polarity; Ndr kinases; Par

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; NDR PROTEIN; PAR3 PROTEIN; PHOSPHOTRANSFERASE; PROTEIN; RASSF5 PROTEIN; SHORT HAIRPIN RNA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; NDR1 PROTEIN KINASE, MOUSE; NDR2 PROTEIN KINASE, MOUSE; PARD3 PROTEIN, MOUSE; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE; RASSF5 PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL POLARITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MACROGLIA; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RAT; SUBVENTRICULAR ZONE; ANIMAL; CYTOLOGY; ENZYMOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL ADHESION MOLECULES; CELL POLARITY; MICE; MICE, KNOCKOUT; NEURONS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 84906070130     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.146696     Document Type: Article

References (66)

1. Arimura, N. and Kaibuchi, K. (2007). Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat. Rev. Neurosci. 8, 194-205.
2. Banker, G. A. and Cowan, W. M. (1977). Rat hippocampal neurons in dispersed cell culture. Brain Res. 126, 397-425.
3. Barnes, A. P. and Polleux, F. (2009). Establishment of axon-dendrite polarity in developing neurons. Annu. Rev. Neurosci. 32, 347-381.
4. Bichsel, S. J., Tamaskovic, R., Stegert, M. R. and Hemmings, B. A. (2004). Mechanism of activation of NDR (nuclear Dbf2-related) protein kinase by the hMOB1 protein. J. Biol. Chem. 279, 35228-35235.
5. Calvisi, D. F., Ladu, S., Gorden, A., Farina, M., Conner, E. A., Lee, J. S., Factor, V. M. and Thorgeirsson, S. S. (2006). Ubiquitous activation of Ras and Jak/ Stat pathways in human HCC. Gastroenterology 130, 1117-1128.
6. Chen, Y. M., Wang, Q. J., Hu, H. S., Yu, P. C., Zhu, J., Drewes, G., Piwnica-Worms, H. and Luo, Z. G. (2006). Microtubule affinity-regulating kinase 2 functions downstream of the PAR-3/PAR-6/atypical PKC complex in regulating hippocampal neuronal polarity. Proc. Natl. Acad. Sci. USA 103, 8534-8539.
7. Chen, S., Chen, J., Shi, H., Wei, M., Castaneda-Castellanos, D. R., Bultje, R. S., Pei, X., Kriegstein, A. R., Zhang, M. and Shi, S. H. (2013). Regulation of microtubule stability and organization by mammalian Par3 in specifying neuronal polarity. Dev. Cell 24, 26-40.
8. Chiba, S., Amagai, Y., Homma, Y., Fukuda, M. and Mizuno, K. (2013). NDR2-mediated Rabin8 phosphorylation is crucial for ciliogenesis by switching binding specificity from phosphatidylserine to Sec15. EMBO J. 32, 874-885.
9. Cornils, H., Stegert, M. R., Hergovich, A., Hynx, D., Schmitz, D., Dirnhofer, S. and Hemmings, B. A. (2010). Ablation of the kinase NDR1 predisposes mice to the development of T cell lymphoma. Sci. Signal. 3, ra47.
10. Cornils, H., Kohler, R. S., Hergovich, A. and Hemmings, B. A. (2011a). Downstream of human NDR kinases: impacting on c-myc and p21 protein stability to control cell cycle progression. Cell Cycle 10, 1897-1904.
11. Cornils, H., Kohler, R. S., Hergovich, A. and Hemmings, B. A. (2011b). Human NDR kinases control G(1)/S cell cycle transition by directly regulating p21 stability. Mol. Cell. Biol. 31, 1382-1395.
12. de Anda, F. C., Pollarolo, G., Da Silva, J. S., Camoletto, P. G., Feiguin, F. and Dotti, C. G. (2005). Centrosome localization determines neuronal polarity. Nature 436, 704-708.
13. de Anda, F. C., Meletis, K., Ge, X., Rei, D. and Tsai, L. H. (2010). Centrosome motility is essential for initial axon formation in the neocortex. J. Neurosci. 30, 10391-10406.
14. Devroe, E., Erdjument-Bromage, H., Tempst, P. and Silver, P. A. (2004). Human Mob proteins regulate the NDR1 and NDR2 serine-threonine kinases. J. Biol. Chem. 279, 24444-24451.
15. Devroe, E., Silver, P. A. and Engelman, A. (2005). HIV-1 incorporates and proteolytically processes human NDR1 and NDR2 serine-threonine kinases. Virology 331, 181-189.
16. Dotti, C. G., Sullivan, C. A. and Banker, G. A. (1988). The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8, 1454-1468.
17. Emoto, K., He, Y., Ye, B., Grueber, W. B., Adler, P. N., Jan, L. Y. and Jan, Y.-N. (2004). Control of dendritic branching and tiling by the Tricorneredkinase/ Furry signaling pathway in Drosophila sensory neurons. Cell 119, 245-256.
18. Emoto, K., Parrish, J. Z., Jan, L. Y. and Jan, Y. N. (2006). The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance. Nature 443, 210-213.
19. Funahashi, Y., Namba, T., Fujisue, S., Itoh, N., Nakamuta, S., Kato, K., Shimada, A., Xu, C., Shan, W., Nishioka, T. et al. (2013). ERK2-mediated phosphorylation of Par3 regulates neuronal polarization. J. Neurosci. 33, 13270-13285.
20. Gallegos, M. E. and Bargmann, C. I. (2004). Mechanosensory neurite termination and tiling depend on SAX-2 and the SAX-1 kinase. Neuron 44, 239-249.
21. Gärtner, A., Fornasiero, E. F., Munck, S., Vennekens, K., Seuntjens, E., Huttner, W. B., Valtorta, F. and Dotti, C. G. (2012). N-cadherin specifies first asymmetry in developing neurons. EMBO J. 31, 1893-1903.
22. Garvalov, B. K., Flynn, K. C., Neukirchen, D., Meyn, L., Teusch, N., Wu, X., Brakebusch, C., Bamburg, J. R. and Bradke, F. (2007). Cdc42 regulates cofilin during the establishment of neuronal polarity. J. Neurosci. 27, 13117-13129.
23. Harris, T. J. and Peifer, M. (2005). The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila. J. Cell Biol. 170, 813-823.
24. Harvey, K. and Tapon, N. (2007). The Salvador-Warts-Hippo pathway - an emerging tumour-suppressor network. Nat. Rev. Cancer 7, 182-191.
25. He, Y., Fang, X., Emoto, K., Jan, Y. N. and Adler, P. N. (2005). The tricornered Ser/Thr protein kinase is regulated by phosphorylation and interacts with furry during Drosophila wing hair development. Mol. Biol. Cell 16, 689-700.
26. Hergovich, A. (2011). MOB control: reviewing a conserved family of kinase regulators. Cell. Signal. 23, 1433-1440.
27. Hergovich, A., Schmitz, D. and Hemmings, B. A. (2006a). The human tumour suppressor LATS1 is activated by human MOB1 at the membrane. Biochem. Biophys. Res. Commun. 345, 50-58.
28. Hergovich, A., Stegert, M. R., Schmitz, D. and Hemmings, B. A. (2006b). NDR kinases regulate essential cell processes from yeast to humans. Nat. Rev. Mol. Cell Biol. 7, 253-264.
29. Hergovich, A., Lamla, S., Nigg, E. A. and Hemmings, B. A. (2007). Centrosome-associated NDR kinase regulates centrosome duplication. Mol. Cell 25, 625-634.
30. Hergovich, A., Kohler, R. S., Schmitz, D., Vichalkovski, A., Cornils, H. and Hemmings, B. A. (2009). The MST1 and hMOB1 tumor suppressors control human centrosome duplication by regulating NDR kinase phosphorylation. Curr. Biol. 19, 1692-1702.
31. Hesson, L., Dallol, A., Minna, J. D., Maher, E. R. and Latif, F. (2003). NORE1A, a homologue of RASSF1A tumour suppressor gene is inactivated in human cancers. Oncogene 22, 947-954.
32. Hwang, E., Ryu, K. S., Pääkkönen, K., Güntert, P., Cheong, H. K., Lim, D. S., Lee, J. O., Jeon, Y. H. and Cheong, C. (2007). Structural insight into dimeric interaction of the SARAH domains from Mst1 and RASSF family proteins in the apoptosis pathway. Proc. Natl. Acad. Sci. USA 104, 9236-9241.
33. Jan, Y. N. and Jan, L. Y. (2001). Asymmetric cell division in the Drosophila nervous system. Nat. Rev. Neurosci. 2, 772-779.
34. Kemphues, K. (2000). PARsing embryonic polarity. Cell 101, 345-348.
35. Khazaei, M. R. and Püschel, A. W. (2009). Phosphorylation of the par polarity complex protein Par3 at serine 962 is mediated by aurora a and regulates its function in neuronal polarity. J. Biol. Chem. 284, 33571-33579.
36. Khokhlatchev, A., Rabizadeh, S., Xavier, R., Nedwidek, M., Chen, T., Zhang, X. F., Seed, B. and Avruch, J. (2002). Identification of a novel Ras-regulated proapoptotic pathway. Curr. Biol. 12, 253-265.
37. Lin, Y., Khokhlatchev, A., Figeys, D. and Avruch, J. (2002). Death-associated protein 4 binds MST1 and augments MST1-induced apoptosis. J. Biol. Chem. 277, 47991-48001.
38. Lorber, B., Howe, M. L., Benowitz, L. I. and Irwin, N. (2009). Mst3b, an Ste20-like kinase, regulates axon regeneration in mature CNS and PNS pathways. Nat. Neurosci. 12, 1407-1414.
39. Moshnikova, A., Frye, J., Shay, J. W., Minna, J. D. and Khokhlatchev, A. V. (2006). The growth and tumor suppressor NORE1A is a cytoskeletal protein that suppresses growth by inhibition of the ERK pathway. J. Biol. Chem. 281, 8143-8152.
40. Moshnikova, A., Kuznetsov, S. and Khokhlatchev, A. V. (2008). Interaction of the growth and tumour suppressor NORE1A with microtubules is not required for its growth-suppressive function. BMC Res. Notes 1, 13.
41. Nakayama, M., Goto, T. M., Sugimoto, M., Nishimura, T., Shinagawa, T., Ohno, S., Amano, M. and Kaibuchi, K. (2008). Rho-kinase phosphorylates PAR-3 and disrupts PAR complex formation. Dev. Cell 14, 205-215.
42. Nishimura, T., Kato, K., Yamaguchi, T., Fukata, Y., Ohno, S. and Kaibuchi, K. (2004). Role of the PAR-3-KIF3 complex in the establishment of neuronal polarity. Nat. Cell Biol. 6, 328-334.
43. Oh, S., Lee, D., Kim, T., Kim, T. S., Oh, H. J., Hwang, C. Y., Kong, Y. Y., Kwon, K. S. and Lim, D. S. (2009). Crucial role for Mst1 and Mst2 kinases in early embryonic development of the mouse. Mol. Cell. Biol. 29, 6309-6320.
44. Ohno, S. (2001). Intercellular junctions and cellular polarity: the PAR-aPKC complex, a conserved core cassette playing fundamental roles in cell polarity. Curr. Opin. Cell Biol. 13, 641-648.
45. Ortiz-Vega, S., Khokhlatchev, A., Nedwidek, M., Zhang, X. F., Dammann, R., Pfeifer, G. P. and Avruch, J. (2002). The putative tumor suppressor RASSF1A homodimerizes and heterodimerizes with the Ras-GTP binding protein Nore1. Oncogene 21, 1381-1390.
46. Paddison, P. J., Caudy, A. A., Bernstein, E., Hannon, G. J. and Conklin, D. S. (2002). Short hairpin RNAs (shRNAs) induce sequence-specific silencing in mammalian cells. Genes Dev. 16, 948-958.
47. Pan, D. (2007). Hippo signaling in organ size control. Genes Dev. 21, 886-897.
48. Park, J., Kang, S. I., Lee, S. Y., Zhang, X. F., Kim, M. S., Beers, L. F., Lim, D. S., Avruch, J., Kim, H. S. and Lee, S. B. (2010). Tumor suppressor ras association domain family 5 (RASSF5/NORE1) mediates death receptor ligand-induced apoptosis. J. Biol. Chem. 285, 35029-35038.
49. Praskova, M., Khoklatchev, A., Ortiz-Vega, S. and Avruch, J. (2004). Regulation of the MST1 kinase by autophosphorylation, by the growth inhibitory proteins, RASSF1 and NORE1, and by Ras. Biochem. J. 381, 453-462.
50. Sakakibara, A., Sato, T., Ando, R., Noguchi, N., Masaoka, M. and Miyata, T. (2014). Dynamics of centrosome translocation and microtubule organization in neocortical neurons during distinct modes of polarization. Cereb. Cortex 24, 1301-1310.
51. Scheel, H. and Hofmann, K. (2003). A novel interaction motif, SARAH, connects three classes of tumor suppressor. Curr. Biol. 13, R899-R900.
52. Schmoranzer, J., Fawcett, J. P., Segura, M., Tan, S., Vallee, R. B., Pawson, T. and Gundersen, G. G. (2009). Par3 and dynein associate to regulate local microtubule dynamics and centrosome orientation during migration. Curr. Biol. 19, 1065-1074.
53. Schwamborn, J. C. and Püschel, A. W. (2004). The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat. Neurosci. 7, 923-929.
54. Sherwood, V., Recino, A., Jeffries, A., Ward, A. and Chalmers, A. D. (2010). The N-terminal RASSF family: a new group of Ras-association-domaincontaining proteins, with emerging links to cancer formation. Biochem. J. 425, 303-311.
55. Shi, S. H., Jan, L. Y. and Jan, Y. N. (2003). Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112, 63-75.
56. Song, H., Mak, K. K., Topol, L., Yun, K., Hu, J., Garrett, L., Chen, Y., Park, O., Chang, J., Simpson, R. M. et al. (2010). Mammalian Mst1 and Mst2 kinases play essential roles in organ size control and tumor suppression. Proc. Natl. Acad. Sci. USA 107, 1431-1436.
57. Stegert, M. R., Tamaskovic, R., Bichsel, S. J., Hergovich, A. and Hemmings, B. A. (2004). Regulation of NDR2 protein kinase by multi-site phosphorylation and the S100B calcium-binding protein. J. Biol. Chem. 279, 23806-23812.
58. Stegert, M. R., Hergovich, A., Tamaskovic, R., Bichsel, S. J. and Hemmings, B. A. (2005). Regulation of NDR protein kinase by hydrophobic motifphosphorylation mediated by the mammalian Ste20-like kinase MST3. Mol. Cell. Biol. 25, 11019-11029.
59. Ultanir, S. K., Hertz, N. T., Li, G., Ge, W. P., Burlingame, A. L., Pleasure, S. J., Shokat, K. M., Jan, L. Y. and Jan, Y. N. (2012). Chemical genetic identification of NDR1/2 kinase substrates AAK1 and Rabin8 Uncovers their roles in dendrite arborization and spine development. Neuron 73, 1127-1142.
60. van der Weyden, L., Tachibana, K. K., Gonzalez, M. A., Adams, D. J., Ng, B. L., Petty, R., Venkitaraman, A. R., Arends, M. J. and Bradley, A. (2005). The RASSF1A isoform of RASSF1 promotes microtubule stability and suppresses tumorigenesis. Mol. Cell. Biol. 25, 8356-8367.
61. Vichalkovski, A., Gresko, E., Cornils, H., Hergovich, A., Schmitz, D. and Hemmings, B. A. (2008). NDR kinase is activated by RASSF1A/MST1 in response to Fas receptor stimulation and promotes apoptosis. Curr. Biol. 18, 1889-1895.
62. Witte, H., Neukirchen, D. and Bradke, F. (2008). Microtubule stabilization specifies initial neuronal polarization. J. Cell Biol. 180, 619-632.
63. Yu, F. X. and Guan, K. L. (2013). The Hippo pathway: regulators and regulations. Genes Dev. 27, 355-371.
64. Zallen, J. A, Peckol, E. L., Tobin D. M. and Bargmann, C. I. (2000). Neuronal cell shape and neurite initiation are regulated by the Ndr kinase SAX-1, a member of the Orb6/COT-1/warts serine/threonine kinase family. Mol. Biol. Cell 11, 3177-3190.
65. Zhao, B., Tumaneng, K. and Guan, K. L. (2011). The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat. Cell Biol. 13, 877-883.
66. Zhou, D., Conrad, C., Xia, F., Park, J. S., Payer, B., Yin, Y., Lauwers, G. Y., Thasler, W., Lee, J. T., Avruch, J. et al. (2009). Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 16, 425-438.