The fission yeast β-arrestin-like protein Any1 is involved in TSC-Rheb signaling and the regulation of amino acid transporters

Journal of Cell Science

Volumn 126, Issue 17, 2013, Pages 3972-3981

  Nakase, Yukiko ^a   Nakase, Mai ^b   Kashiwazaki, Jun ^c   Murai, Tomoka ^a   Otsubo, Yoko ^d   Mabuchi, Issei ^c   Yamamoto, Masayuki ^d   Takegawa, Kaoru ^b   Matsumoto, Tomohiro ^a  

^a KYOTO UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c GAKUSHUIN UNIVERSITY   (Japan)

^d KAZUSA DNA RESEARCH INSTITUTE   (Japan)

Author keywords

Amino acid transporter; Any1; Arrestin; Schizosaccharomyces pombe; TSC; Tuberous sclerosis complex; Ubiquitin ligase

Indexed keywords

AMINO ACID; AMINO ACID TRANSPORTER; BETA ARRESTIN 1; CELL SURFACE RECEPTOR; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; NITROGEN; REGULATOR PROTEIN; RHEB PROTEIN; TARGET OF RAPAMYCIN KINASE; TUBERIN; UBIQUITIN PROTEIN LIGASE E3;

ARTICLE; CELL CYCLE PROGRESSION; CELL GROWTH; CELL INTERACTION; CELL MEMBRANE; CELL PROLIFERATION; CELLULAR DISTRIBUTION; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME REGULATION; GENE EXPRESSION; GOLGI COMPLEX; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHIZOSACCHAROMYCES POMBE; TUBEROUS SCLEROSIS; TUBEROUS SCLEROSIS COMPLEX; UBIQUITINATION; WILD TYPE;

AMINO ACID TRANSPORTER; ANY1; ARRESTIN; SCHIZOSACCHAROMYCES POMBE; TSC; TUBEROUS SCLEROSIS COMPLEX; UBIQUITIN LIGASE;

AMINO ACID TRANSPORT SYSTEMS, BASIC; ARRESTINS; CARBON-NITROGEN LIGASES; CELL CYCLE; CELL MEMBRANE; GOLGI APPARATUS; MEIOSIS; MONOMERIC GTP-BINDING PROTEINS; MULTIPROTEIN COMPLEXES; PHOSPHATIDYLINOSITOL 3-KINASES; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SIGNAL TRANSDUCTION;

EID: 84883278145     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.128355     Document Type: Article

References (50)

1. Aspuria, P. J. and Tamanoi, F. (2008). The Tsc/Rheb signaling pathway controls basic amino acid uptake via the Cat1 permease in fission yeast. Mol. Genet. Genomics 279, 441-450.
2. Crino, P. B., Nathanson, K. L. and Henske, E. P. (2006). The tuberous sclerosis complex. N. Engl. J. Med. 355, 1345-1356.
3. Danbolt, N. C. (2001). Glutamate uptake. Prog. Neurobiol. 65, 1-105.
4. Dunphy, W. G. and Kumagai, A. (1991). The cdc25 protein contains an intrinsic phosphatase activity. Cell 67, 189-196.
5. Esteban, V., Sacristán, M., Andrés, S. and Bueno, A. (2008). The Flp1/Clp1 phosphatase cooperates with HECT-type Pub1/2 protein-ubiquitin ligases in Schizosaccharomyces pombe. Cell Cycle 7, 1269-1276.
6. Fingar, D. C. and Blenis, J. (2004). Target of rapamycin (TOR): an integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene 23, 3151-3171.
7. Garami, A., Zwartkruis, F. J., Nobukuni, T., Joaquin, M., Roccio, M., Stocker, H., Kozma, S. C., Hafen, E., Bos, J. L. and Thomas, G. (2003). Insulin activation of Rheb, a mediator of mTOR/S6K/4E-BP signaling, is inhibited by TSC1 and 2. Mol. Cell 11, 1457-1466.
8. Gautier, J., Solomon, M. J., Booher, R. N., Bazan, J. F. and Kirschner, M. W. (1991). cdc25 is a specific tyrosine phosphatase that directly activates p34cdc2. Cell 67, 197-211.
9. Gietz, D., St Jean, A., Woods, R. A. and Schiestl, R. H. (1992). Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20, 1425.
10. Gómez, M. R. (1995). History of the tuberous sclerosis complex. Brain Dev. 17 Suppl, 55-57.
11. Gould, K. L. and Nurse, P. (1989). Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis. Nature 342, 39-45.
12. Inoki, K., Li, Y., Zhu, T., Wu, J. and Guan, K. L. (2002). TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat. Cell Biol. 4, 648-657.
13. Jensen, R., Sprague, G. F., Jr and Herskowitz, I. (1983). Regulation of yeast matingtype interconversion: feedback control of HO gene expression by the mating-type locus. Proc. Natl. Acad. Sci. USA 80, 3035-3039.
14. Karagiannis, J., Saleki, R. and Young, P. G. (1999). The pub1 E3 ubiquitin ligase negatively regulates leucine uptake in response to NH4 + in fission yeast. Curr. Genet. 35, 593-601.
15. Kawai, M., Nakashima, A., Ueno, M., Ushimaru, T., Aiba, K., Doi, H. and Uritani, M. (2001). Fission yeast tor1 functions in response to various stresses including nitrogen starvation, high osmolarity, and high temperature. Curr. Genet. 39, 166-174.
16. Kwiatkowski, D. J. and Short, M. P. (1994). Tuberous sclerosis. Arch. Dermatol. 130, 348-354.
17. Lin, C. H., MacGurn, J. A., Chu, T., Stefan, C. J. and Emr, S. D. (2008). Arrestinrelated ubiquitin-ligase adaptors regulate endocytosis and protein turnover at the cell surface. Cell 135, 714-725.
18. Lundgren, K., Walworth, N., Booher, R., Dembski, M., Kirschner, M. and Beach, D. (1991). mik1 and wee1 cooperate in the inhibitory tyrosine phosphorylation of cdc2. Cell 64, 1111-1122.
19. Mach, K. E., Furge, K. A. and Albright, C. F. (2000). Loss of Rhb1, a Rheb-related GTPase in fission yeast, causes growth arrest with a terminal phenotype similar to that caused by nitrogen starvation. Genetics 155, 611-622.
20. Manning, B. D. and Cantley, L. C. (2003). Rheb fills a GAP between TSC and TOR. Trends Biochem. Sci. 28, 573-576.
21. Masai, H., Miyake, T. and Arai, K.-I. (1995). hsk1+, a Schizosaccharomyces pombe gene related to Saccharomyces cerevisiae CDC7, is required for chromosomal replication. EMBO J. 14, 3094-3104.
22. Matsumoto, S., Bandyopadhyay, A., Kwiatkowski, D. J., Maitra, U. and Matsumoto, T. (2002). Role of the Tsc1-Tsc2 complex in signaling and transport across the cell membrane in the fission yeast Schizosaccharomyces pombe. Genetics 161, 1053-1063.
23. Matsuo, T., Otsubo, Y., Urano, J., Tamanoi, F. and Yamamoto, M. (2007). Loss of the TOR kinase Tor2 mimics nitrogen starvation and activates the sexual development pathway in fission yeast. Mol. Cell. Biol. 27, 3154-3164.
24. Moreno, S., Klar, A. and Nurse, P. (1991). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823.
25. Murai, T., Nakase, Y., Fukuda, K., Chikashige, Y., Tsutsumi, C., Hiraoka, Y. and Matsumoto, T. (2009). Distinctive responses to nitrogen starvation in the dominant active mutants of the fission yeast Rheb GTPase. Genetics 183, 517-527.
26. Nakamura, T., Nakamura-Kubo, M., Hirata, A. and Shimoda, C. (2001). The Schizosaccharomyces pombe spo3+ gene is required for assembly of the forespore membrane and genetically interacts with psy1+-encoding syntaxin-like protein. Mol. Biol. Cell 12, 3955-3972.
27. Nakase, Y., Fukuda, K., Chikashige, Y., Tsutsumi, C., Morita, D., Kawamoto, S., Ohnuki, M., Hiraoka, Y. and Matsumoto, T. (2006). A defect in protein farnesylation suppresses a loss of Schizosaccharomyces pombe tsc2+, a homolog of the human gene predisposing to tuberous sclerosis complex. Genetics 173, 569-578.
28. Nakase, Y., Nakamura-Kubo, M., Ye, Y., Hirata, A., Shimoda, C. and Nakamura, T. (2008). Meiotic spindle pole bodies acquire the ability to assemble the spore plasma membrane by sequential recruitment of sporulation-specific components in fission yeast. Mol. Biol. Cell 19, 2476-2487.
29. Nakase, M., Tani, M., Morita, T., Kitamoto, H. K., Kashiwazaki, J., Nakamura, T., Hosomi, A., Tanaka, N. and Takegawa, K. (2010). Mannosylinositol phosphorylceramide is a major sphingolipid component and is required for proper localization of plasma-membrane proteins in Schizosaccharomyces pombe. J. Cell Sci. 123, 1578-1587.
30. Nakase, M., Nakase, Y., Chardwiriyapreecha, S., Kakinuma, Y., Matsumoto, T. and Takegawa, K. (2012). Intracellular trafficking and ubiquitination of the Schizosaccharomyces pombe amino acid permease Aat1p. Microbiology 158, 659- 673.
31. Nefsky, B. and Beach, D. (1996). Pub1 acts as an E6-AP-like protein ubiquitiin ligase in the degradation of cdc25. EMBO J. 15, 1301-1312.
32. Nikko, E. and Pelham, H. R. (2009). Arrestin-mediated endocytosis of yeast plasma membrane transporters. Traffic 10, 1856-1867.
33. Nikko, E., Sullivan, J. A. and Pelham, H. R. (2008). Arrestin-like proteins mediate ubiquitination and endocytosis of the yeast metal transporter Smf1. EMBO Rep. 9, 1216-1221.
34. Okazaki, K., Okazaki, N., Kume, K., Jinno, S., Tanaka, K. and Okayama, H. (1990). High-frequency transformation method and library transducing vectors for cloning mammalian cDNAs by trans-complementation of Schizosaccharomyces pombe. Nucleic Acids Res. 18, 6485-6489.
35. Raught, B., Gingras, A. C. and Sonenberg, N. (2001). The target of rapamycin (TOR) proteins. Proc. Natl. Acad. Sci. USA 98, 7037-7044.
36. Russell, P. and Nurse, P. (1986). cdc25+ functions as an inducer in the mitotic control of fission yeast. Cell 45, 145-153.
37. Saito, K., Araki, Y., Kontani, K., Nishina, H. and Katada, T. (2005). Novel role of the small GTPase Rheb: its implication in endocytic pathway independent of the activation of mammalian target of rapamycin. J. Biochem. 137, 423-430.
38. Saleki, R., Jia, Z., Karagiannis, J. and Young, P. G. (1997). Tolerance of low pH in Schizosaccharomyces pombe requires a functioning pub1 ubiquitin ligase. Mol. Gen. Genet. 254, 520-528.
39. Shenoy, S. K. and Lefkowitz, R. J. (2003). Multifaceted roles of b-arrestins in the regulation of seven-membrane-spanning receptor trafficking and signalling. Biochem. J. 375, 503-515.
40. Shenoy, S. K., McDonald, P. H., Kohout, T. A. and Lefkowitz, R. J. (2001). Regulation of receptor fate by ubiquitination of activated b 2-adrenergic receptor and b-arrestin. Science 294, 1307-1313.
41. Soetens, O., De Craene, J. O. and Andre, B. (2001). Ubiquitin is required for sorting to the vacuole of the yeast general amino acid permease, Gap1. J. Biol. Chem. 276, 43949-43957.
42. Tabuchi, M., Tanaka, N., Iwahara, S. and Takegawa, K. (1997). The Schizosaccharomyces pombe gms1+ gene encodes an UDP-galactose transporter homologue required for protein galactosylation. Biochem. Biophys. Res. Commun. 232, 121-125.
43. Tanaka, K., Hao, Z., Kai, M. and Okayama, H. (2001a). Establishment and maintenance of sister chromatid cohesion in fission yeast by a unique mechanism. EMBO J. 20, 5779-5790.
44. Tanaka, N., Konomi, M., Osumi, M. and Takegawa, K. (2001b). Characterization of a Schizosaccharomyces pombe mutant deficient in UDP-galactose transport activity. Yeast 18, 903-914.
45. Thomas, P. S. (1980). Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc. Natl. Acad. Sci. USA 77, 5201-5205.
46. Urano, J., Comiso, M. J., Guo, L., Aspuria, P. J., Deniskin, R., Tabancay, A. P., Jr, Kato-Stankiewicz, J. and Tamanoi, F. (2005). Identification of novel single amino acid changes that result in hyperactivation of the unique GTPase, Rheb, in fission yeast. Mol. Microbiol. 58, 1074-1086.
47. van Slegtenhorst, M., Carr, E., Stoyanova, R., Kruger, W. D. and Henske, E. P. (2004). tsc1+ and tsc2+ regulate arginine uptake and metabolism in Schizosaccharomyces pombe. J. Biol. Chem. 279, 12706-12713.
48. Weisman, R. and Choder, M. (2001). The fission yeast TOR homolog, tor1+, is required for the response to starvation and other stresses via a conserved serine. J. Biol. Chem. 276, 7027-7032.
49. Weisman, R., Finkelstein, S. and Choder, M. (2001). Rapamycin blocks sexual development in fission yeast through inhibition of the cellular function of an FKBP12 homolog. J. Biol. Chem. 276, 24736-24742.
50. Woods, A., Sherwin, T., Sasse, R., MacRae, T. H., Baines, A. J. and Gull, K. (1989). Definition of individual components within the cytoskeleton of Trypanosoma brucei by a library of monoclonal antibodies. J. Cell Sci. 93, 491-500