TOR complex 2 (TORC2) in Dictyostelium suppresses phagocytic nutrient capture independently of TORC1-mediated nutrient sensing

Development

Volumn 139, Issue 5, 2012, Pages 37-48

  Rosel, Daniel ^a,b   Khurana, Taruna ^a,c   Majithia, Amit ^a,d   Huang, Xiuli ^a   Bhandari, Ramanath ^a,e   Kimmel, Alan R ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b CHARLES UNIVERSITY   (Czech Republic)

^c CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

Author keywords

4E BP; Actin; Dictyostelium; FKBP12; Rapamycin; Raptor

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN SERINE THREONINE KINASE; RAPAMYCIN; RAPTOR PROTEIN; TARGET OF RAPAMYCIN KINASE; TORC1 PROTEIN; TORC2 PROTEIN; UNCLASSIFIED DRUG; PROTEIN KINASE; TOR COMPLEX 1 PROTEIN; TOR COMPLEX 2 PROTEIN;

ARTICLE; CELL FUNCTION; CELL TRANSPORT; DICTYOSTELIUM; ENZYME INACTIVATION; EXPRESSION VECTOR; GROWTH REGULATION; MACROPINOCYTOSIS; NUTRIENT SENSING; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN INTERACTION; REGULATORY MECHANISM; RNA INTERFERENCE; NUTRIENT; NUTRIENT UPTAKE; PINOCYTOSIS; PROTEIN FUNCTION;

DICTYOSTELIUM; RAPTORES;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL ADHESION; DICTYOSTELIUM; FOOD; MULTIPROTEIN COMPLEXES; PEPTIDE INITIATION FACTORS; PHAGOCYTOSIS; PHOSPHORYLATION; PINOCYTOSIS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SIROLIMUS; TIME FACTORS; TOR SERINE-THREONINE KINASES;

EID: 84856704227     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/jcs.077040     Document Type: Article

References (54)

1. Abraham, R. T. and Wiederrecht, G. J. (1996). Immunopharmacology of rapamycin. Annu. Rev. Immunol. 14, 483-510.
2. Aspuria, P. J., Sato, T. and Tamanoi, F. (2007). The TSC/Rheb/TOR signaling pathway in fission yeast and mammalian cells: temperature sensitive and constitutive active mutants of TOR. Cell Cycle 6, 1692-1695.
3. Avruch, J., Long, X., Ortiz-Vega, S., Rapley, J., Papageorgiou, A. and Dai, N. (2008). Amino Acid Regulation of TOR Complex 1. Am. J. Physiol. Endocrinol. Metab. 96, E592-E602.
4. Blaauw, M., Linskens, M. H. and van Haastert, P. J. (2000). Efficient control of gene expression by a tetracycline-dependent transactivator in single Dictyostelium discoideum cells. Gene 252, 71-82.
5. Brunn, G. J., Hudson, C. C., Sekulic, A., Williams, J. M., Hosoi, H., Houghton, P. J., Lawrence, J. C., Jr and Abraham, R. T. (1997). Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science 277, 99-101.
6. Cardelli, J. (2001). Phagocytosis and macropinocytosis in Dictyostelium: phosphoinositide- based processes, biochemically distinct. Traffic 2, 311-320.
7. Chen, M. Y., Long, Y. and Devreotes, P. N. (1997). A novel cytosolic regulator, Pianissimo, is required for chemoattractant receptor and G protein-mediated activation of the 12 transmembrane domain adenylyl cyclase in Dictyostelium. Genes Dev. 11, 3218-3231.
8. Dormann, D., Weijer, G., Dowler, S. and Weijer, C. J. (2004). In vivo analysis of 3- phosphoinositide dynamics during Dictyostelium phagocytosis and chemotaxis. J. Cell Sci. 117, 6497-6509.
9. Frias, M. A., Thoreen, C. C., Jaffe, J. D., Schroder, W., Sculley, T., Carr, S. A. and Sabatini, D. M. (2006). mSin1 is necessary for Akt/PKB phosphorylation, and its isoforms define three distinct mTORC2s. Curr. Biol. 16, 1865-1870.
10. Gangloff, Y. G., Mueller, M., Dann, S. G., Svoboda, P., Sticker, M., Spetz, J. F., Um, S. H., Brown, E. J., Cereghini, S., Thomas, G. et al. (2004). Disruption of the mouse mTOR gene leads to early postimplantation lethality and prohibits embryonic stem cell development. Mol. Cell. Biol. 24, 9508-9516.
11. Guertin, D. A., Stevens, D.M., Thoreen, C. C., Burds, A. A., Kalaany, N. Y., Moffat, J., Brown, M., Fitzgerald, K. J. and Sabatini, D. M. (2006). Ablation in mice of the mTORC components raptor, rictor, or mLST8 reveals that mTORC2 is required for signaling to Akt-FOXO and PKCalpha, but not S6K1. Dev. Cell 11, 859-871.
12. Hara, K., Maruki, Y., Long, X., Yoshino, K., Oshiro, N., Hidayat, S., Tokunaga, C., Avruch, J. and Yonezawa, K. (2002). Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 110, 177-189.
13. Heitman, J., Movva, N. R. and Hall, M. N. (1991). Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253, 905-909.
14. Huang, J. and Manning, B. D. (2009). A complex interplay between Akt, TSC2 and the two mTOR complexes. Biochem. Soc. Trans. 37, 217-222.
15. Huang, J., Dibble, C. C., Matsuzaki, M. and Manning, B. D. (2008). The TSC1-TSC2 complex is required for proper activation of mTOR complex 2. Mol. Cell Biol. 28, 4104-4115.
16. Jacinto, E., Facchinetti, V., Liu, D., Soto, N., Wei, S., Jung, S. Y., Huang, Q., Qin, J. and Su, B. (2006). SIN1/MIP1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell 127, 125-137.
17. Kamimura, Y. and Devreotes, P. N. (2010). Phosphoinositide-dependent protein kinase (PDK) activity regulates phosphatidylinositol 3,4,5-trisphosphate-dependent and -independent protein kinase B activation and chemotaxis. J. Biol. Chem. 285, 7938-7946.
18. Karbowniczek, M., Cash, T., Cheung, M., Robertson, G. P., Astrinidis, A. and Henske, E. P. (2004). Regulation of B-Raf kinase activity by tuberin and Rheb is mammalian target of rapamycin (mTOR)-independent. J. Biol. Chem. 279, 29930-29937.
19. Katoh, M., Chen, G., Roberge, E., Shaulsky, G. and Kuspa, A. (2007). Developmental commitment in Dictyostelium discoideum. Eukaryot Cell 6, 2038-2045.
20. Khurana, T., Brzostowski, J. A. and Kimmel, A. R. (2005). A Rab21/LIM-only/CHLIM complex regulates phagocytosis via both activating and inhibitory mechanisms. EMBO J. 24, 2254-2264.
21. Kim, D. H., Sarbassov, D. D., Ali, S. M., King, J. E., Latek, R. R., Erdjument- Bromage, H., Tempst, P. and Sabatini, D. M. (2002). mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110, 163-175.
22. Kim, L., Liu, J. and Kimmel, A. R. (1999). The novel tyrosine kinase ZAK1 activates GSK3 to direct cell fate specification. Cell 99, 399-408.
23. Kimmel, A. R. and Firtel, R. A. (2004). Breaking symmetries: regulation of Dictyostelium development through chemoattractant and morphogen signal-response. Curr. Opin. Genet Dev. 14, 540-549.
24. Knetsch, M. L., Tsiavaliaris, G., Zimmermann, S., Ruhl, U. and Manstein, D. J. (2002). Expression vectors for studying cytoskeletal proteins in Dictyostelium discoideum. J. Muscle Res. Cell Motil. 23, 605-611.
25. Kunz, J., Henriquez, R., Schneider, U., Deuter-Reinhard, M., Movva, N. R. and Hall, M. N. (1993). Target of rapamycin in yeast, TOR2, is an essential phosphatidylinositol kinase homolog required for G1 progression. Cell 73, 585-596.
26. Laplante, M. and Sabatini, D. M. (2009). mTOR signaling at a glance. J. Cell Sci. 122, 3589-3594.
27. Lee, S., Parent, C. A., Insall, R. and Firtel, R. A. (1999). A novel Ras-interacting protein required for chemotaxis and cyclic adenosine monophosphate signal relay in Dictyostelium. Mol. Biol. Cell 10, 2829-2845.
28. Lee, S., Comer, F. I., Sasaki, A., McLeod, I. X., Duong, Y., Okumura, K., Yates, J. R., 3rd, Parent, C. A. and Firtel, R. A. (2005). TOR complex 2 integrates cell movement during chemotaxis and signal relay in Dictyostelium. Mol. Biol. Cell 16, 4572-4583.
29. Liao, X. H., Buggey, J. and Kimmel, A. R. (2010). Chemotactic activation of Dictyostelium AGC-family kinases AKT and PKBR1 requires separate but coordinated functions of PDK1 and TORC2. J. Cell Sci. 123, 983-992.
30. Loewith, R., Jacinto, E., Wullschleger, S., Lorberg, A., Crespo, J. L., Bonenfant, D., Oppliger, W., Jenoe, P. and Hall, M. N. (2002). Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 10, 457-468.
31. Long, X., Spycher, C., Han, Z. S., Rose, A. M., Muller, F. and Avruch, J. (2002). TOR deficiency in C. elegans causes developmental arrest and intestinal atrophy by inhibition of mRNA translation. Curr. Biol. 12, 1448-1461.
32. Long, X., Lin, Y., Ortiz-Vega, S., Yonezawa, K. and Avruch, J. (2005). Rheb binds and regulates the mTOR kinase. Curr. Biol. 15, 702-713.
33. Maniak, M. (2001). Fluid-phase uptake and transit in axenic Dictyostelium cells. Biochim. Biophys. Acta 1525, 197-204.
34. Meili, R., Ellsworth, C., Lee, S., Reddy, T. B., Ma, H. and Firtel, R. A. (1999). Chemoattractant-mediated transient activation and membrane localization of Akt/ PKB is required for efficient chemotaxis to cAMP in Dictyostelium. EMBO J. 18, 2092-1105.
35. Murakami, M., Ichisaka, T., Maeda, M., Oshiro, N., Hara, K., Edenhofer, F., Kiyama, H., Yonezawa, K. and Yamanaka, S. (2004). mTOR is essential for growth and proliferation in early mouse embryos and embryonic stem cells. Mol. Cell. Biol. 24, 6710-6718.
36. Oldham, S., Montagne, J., Radimerski, T., Thomas, G. and Hafen, E. (2000). Genetic and biochemical characterization of dTOR, the Drosophila homolog of the target of rapamycin. Genes Dev. 14, 2689-2694.
37. Otsubo, Y. and Yamamato, M. (2008). TOR signaling in fission yeast. Crit. Rev. Biochem. Mol. Biol. 43, 277-283.
38. Pang, K. M., Lee, E. and Knecht, D. A. (1998). Use of a fusion protein between GFP and an actin-binding domain to visualize transient filamentous-actin structures. Curr. Biol. 8, 405-408.
39. Price, D. J., Grove, J. R., Calvo, V., Avruch, J. and Bierer, B. E. (1992). Rapamycininduced inhibition of the 70-kilodalton S6 protein kinase. Science 257, 973-977.
40. Rivero, F. and Maniak, M. (2006). Quantitative and microscopic methods for studying the endocytic pathway. Methods Mol. Biol. 346, 423-438.
41. Roberg, K. J., Bickel, S., Rowley, N. and Kaiser, C. A. (1997). Control of amino acid permease sorting in the late secretory pathway of Saccharomyces cerevisiae by SEC13, LST4, LST7 and LST8. Genetics 147, 1569-1584.
42. Rosel, D. and Kimmel, A. R. (2006). The COP9 signalosome regulates cell proliferation of Dictyostelium discoideum. Eur. J. Cell Biol. 85, 1023-1034.
43. Rupper, A., Lee, K., Knecht, D. and Cardelli, J. (2001). Sequential activities of phosphoinositide 3-kinase, PKB/Aakt, and Rab7 during macropinosome formation in Dictyostelium. Mol. Biol. Cell 12, 2813-2824.
44. Sarbassov, D., Ali, S. M., Sengupta, S., Sheen, J. H., Hsu, P. P., Bagley, A. F., Markhard, A. L. and Sabatini, D. M. (2006). Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol. Cell 22, 159-168.
45. Sarbassov, D. D., Ali, S. M., Kim, D. H., Guertin, D. A., Latek, R. R., Erdjument-Bromage, H., Tempst, P. and Sabatini, D. M. (2004). Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr. Biol. 14, 1296-1302.
46. Sarbassov, D. D., Guertin, D. A., Ali, S. M. and Sabatini, D. M. (2005). Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307, 1098-1101.
47. Shah, O. J., Wang, Z. and Hunter, T. (2004). Inappropriate activation of the TSC/ Rheb/mTOR/S6K cassette induces IRS1/2 depletion, insulin resistance, and cell survival deficiencies. Curr. Biol. 14, 1650-1656.
48. Sinclair, L. V., Finlay, D., Feijoo, C., Cornish, G. H., Gray, A., Ager, A., Okkenhaug, K., Hagenbeek, T. J., Spits, H. and Cantrell, D. A. (2008). Phosphatidylinositol-3-OH kinase and nutrient-sensing mTOR pathways control T lymphocyte trafficking. Nat. Immunol. 9, 513-521.
49. Soulard, A., Cohen, A. and Hall, M. N. (2009). TOR signaling in invertebrates. Curr. Opin. Cell Biol. 21, 825-836.
50. Tabancay, A. P., Jr, Gau, C. L., Machado, I. M., Uhlmann, E. J., Gutmann, D. H., Guo, L. and Tamanoi, F. (2003). Identification of dominant negative mutants of Rheb GTPase and their use to implicate the involvement of human Rheb in the activation of p70S6K. J. Biol. Chem. 278, 39921-39930.
51. Urano, J., Sato, T., Matsuo, T., Otsubo, Y., Yamamoto, M. and Tamanoi, F. (2007). Point mutations in TOR confer Rheb-independent growth in fission yeast and nutrient-independent mammalian TOR signaling in mammalian cells. Proc. Natl. Acad. Sci. USA 104, 3514-3519.
52. Weisman, R., Roitburg, I., Nahari, T. and Kupiec, M. (2005). Regulation of leucine uptake by tor1+ in Schizosaccharomyces pombe is sensitive to rapamycin. Genetics 169, 539-550.
53. Yang, Q. and Guan, K. L. (2007). Expanding mTOR signaling. Cell Res. 17, 666-681.
54. Yang, Q., Inoki, K., Ikenoue, T. and Guan, K. L. (2006). Identification of Sin1 as an essential TORC2 component required for complex formation and kinase activity. Genes Dev. 20, 2820-2832.