The TBC/RabGAP Armus Coordinates Rac1 and Rab7 Functions during Autophagy

Developmental Cell

Volumn 25, Issue 1, 2013, Pages 15-28

  Carroll, Bernadette ^a,d   Mohd Naim, Noor ^a   Maximiano, Filipe ^a,e   Frasa, Marieke A ^a,f   McCormack, Jessica ^a   Finelli, Mattea ^a,g   Thoresen, Sigrid B ^a,i   Perdios, Louis ^a   Daigaku, Reiko ^a   Francis, Richard E ^a,h   Futter, Clare ^b   Dikic, Ivan ^c   Braga, Vania M M ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c GOETHE UNIVERSITY   (Germany)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

^e Boehringer Ingelheim   (Portugal)

^f GROENE HART HOSPITAL   (Netherlands)

^g UNIVERSITY OF OXFORD   (United Kingdom)

^h Breakthrough Breast Cancer   (United Kingdom)

ⁱ UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; RAB PROTEIN; RAB7 PROTEIN; RAC1 PROTEIN;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL MIGRATION; CONTROLLED STUDY; ENDOCYTOSIS; HUMAN; HUMAN CELL; LIGHT CHAIN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STARVATION; STATISTICAL SIGNIFICANCE;

AMINO ACID SEQUENCE; AUTOPHAGY; CULTURE MEDIA; ENZYME ACTIVATION; FLUORESCENT ANTIBODY TECHNIQUE; GTPASE-ACTIVATING PROTEINS; GUANOSINE TRIPHOSPHATE; HUMANS; INFANT, NEWBORN; KERATINOCYTES; LYSOSOMES; MICROTUBULE-ASSOCIATED PROTEINS; MOLECULAR SEQUENCE DATA; PHAGOSOMES; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RAC1 GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION;

EID: 84876416302     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2013.03.005     Document Type: Article

References (56)

1. Alemu E.A., Lamark T., Torgersen K.M., Birgisdottir A.B., Larsen K.B., Jain A., Olsvik H., Øvervatn A., Kirkin V., Johansen T. ATG8 family proteins act as scaffolds for assembly of the ULK complex: sequence requirements for LC3-interacting region (LIR) motifs. J. Biol. Chem. 2012, 287:39275-39290.
2. Behrends C., Sowa M.E., Gygi S.P., Harper J.W. Network organization of the human autophagy system. Nature 2010, 466:68-76.
3. Betson M., Lozano E., Zhang J., Braga V.M.M. Rac activation upon cell-cell contact formation is dependent on signaling from the epidermal growth factor receptor. J. Biol. Chem. 2002, 277:36962-36969.
4. Braga V.M.M., Machesky L.M., Hall A., Hotchin N.A. The small GTPases Rho and Rac are required for the establishment of cadherin-dependent cell-cell contacts. J. Cell Biol. 1997, 137:1421-1431.
5. Chan E.Y., Kir S., Tooze S.A. siRNA screening of the kinome identifies ULK1 as a multidomain modulator of autophagy. J. Biol. Chem. 2007, 282:25464-25474.
6. Chen Y., Klionsky D.J. The regulation of autophagy - unanswered questions. J. Cell Sci. 2011, 124:161-170.
7. D'Souza-Schorey C., Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 2006, 7:347-358.
8. Dikic I., Johansen T., Kirkin V. Selective autophagy in cancer development and therapy. Cancer Res. 2010, 70:3431-3434.
9. Eng C.H., Abraham R.T. The autophagy conundrum in cancer: influence of tumorigenic metabolic reprogramming. Oncogene 2011, 30:4687-4696.
10. Fader C.M., Sánchez D., Furlán M., Colombo M.I. Induction of autophagy promotes fusion of multivesicular bodies with autophagic vacuoles in k562 cells. Traffic 2008, 9:230-250.
11. Frasa M.A., Maximiano F.C., Smolarczyk K., Francis R.E., Betson M.E., Lozano E., Goldenring J.R., Seabra M.C., Rak A., Ahmadian M.R., Braga V.M. Armus is a Rac1 effector that inactivates Rab7 and regulates E-cadherin degradation. Curr. Biol. 2010, 20:198-208.
12. Frasa M.A., Koessmeier K.T., Ahmadian M.R., Braga V.M. Illuminating the functional and structural repertoire of human TBC/RABGAPs. Nat. Rev. Mol. Cell Biol. 2012, 13:67-73.
13. Gulhati P., Bowen K.A., Liu J., Stevens P.D., Rychahou P.G., Chen M., Lee E.Y., Weiss H.L., O'Connor K.L., Gao T., Evers B.M. mTORC1 and mTORC2 regulate EMT, motility, and metastasis of colorectal cancer via RhoA and Rac1 signaling pathways. Cancer Res. 2011, 71:3246-3256.
14. Gutierrez M.G., Munafó D.B., Berón W., Colombo M.I. Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J. Cell Sci. 2004, 117:2687-2697.
15. Hernández-Negrete I., Carretero-Ortega J., Rosenfeldt H., Hernández-García R., Calderón-Salinas J.V., Reyes-Cruz G., Gutkind J.S., Vázquez-Prado J. P-Rex1 links mammalian target of rapamycin signaling to Rac activation and cell migration. J. Biol. Chem. 2007, 282:23708-23715.
16. Huang J., Birmingham C.L., Shahnazari S., Shiu J., Zheng Y.T., Smith A.C., Campellone K.G., Heo W.D., Gruenheid S., Meyer T., et al. Antibacterial autophagy occurs at PI(3)P-enriched domains of the endoplasmic reticulum and requires Rab1 GTPase. Autophagy 2011, 7:17-26.
17. Itoh T., Satoh M., Kanno E., Fukuda M. Screening for target Rabs of TBC (Tre-2/Bub2/Cdc16) domain-containing proteins based on their Rab-binding activity. Genes Cells 2006, 11:1023-1037.
18. Itoh T., Fujita N., Kanno E., Yamamoto A., Yoshimori T., Fukuda M. Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation. Mol. Biol. Cell 2008, 19:2916-2925.
19. Itoh T., Kanno E., Uemura T., Waguri S., Fukuda M. OATL1, a novel autophagosome-resident Rab33B-GAP, regulates autophagosomal maturation. J. Cell Biol. 2011, 192:839-853.
20. Jäger S., Bucci C., Tanida I., Ueno T., Kominami E., Saftig P., Eskelinen E.L. Role for Rab7 in maturation of late autophagic vacuoles. J. Cell Sci. 2004, 117:4837-4848.
21. Janku F., McConkey D.J., Hong D.S., Kurzrock R. Autophagy as a target for anticancer therapy. Nat. Rev. Clin. Oncol. 2011, 8:528-539.
22. Kamijo K., Ohara N., Abe M., Uchimura T., Hosoya H., Lee J.S., Miki T. Dissecting the role of Rho-mediated signaling in contractile ring formation. Mol. Biol. Cell 2006, 17:43-55.
23. Kim E.K., Yun S.J., Ha J.M., Kim Y.W., Jin I.H., Yun J., Shin H.K., Song S.H., Kim J.H., Lee J.S., et al. Selective activation of Akt1 by mammalian target of rapamycin complex 2 regulates cancer cell migration, invasion, and metastasis. Oncogene 2011, 30:2954-2963.
24. Kimura S., Noda T., Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 2007, 3:452-460.
25. Klionsky D.J. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 2007, 8:931-937.
26. Korolchuk V.I., Saiki S., Lichtenberg M., Siddiqi F.H., Roberts E.A., Imarisio S., Jahreiss L., Sarkar S., Futter M., Menzies F.M., et al. Lysosomal positioning coordinates cellular nutrient responses. Nat. Cell Biol. 2011, 13:453-460.
27. Lee J.Y., Koga H., Kawaguchi Y., Tang W., Wong E., Gao Y.S., Pandey U.B., Kaushik S., Tresse E., Lu J., et al. HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J. 2010, 29:969-980.
28. Levine B., Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008, 132:27-42.
29. Liang C., Lee J.S., Inn K.S., Gack M.U., Li Q., Roberts E.A., Vergne I., Deretic V., Feng P., Akazawa C., Jung J.U. Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat. Cell Biol. 2008, 10:776-787.
30. Longatti A., Tooze S.A. Vesicular trafficking and autophagosome formation. Cell Death Differ. 2009, 16:956-965.
31. Longatti A., Lamb C.A., Razi M., Yoshimura S., Barr F.A., Tooze S.A. TBC1D14 regulates autophagosome formation via Rab11- and ULK1-positive recycling endosomes. J. Cell Biol. 2012, 197:659-675.
32. Mack N.A., Whalley H.J., Castillo-Lluva S., Malliri A. The diverse roles of Rac signaling in tumorigenesis. Cell Cycle 2011, 10:1571-1581.
33. Moreau K., Ravikumar B., Puri C., Rubinsztein D.C. Arf6 promotes autophagosome formation via effects on phosphatidylinositol 4,5-bisphosphate and phospholipase D. J. Cell Biol. 2012, 196:483-496.
34. Mosesson Y., Mills G.B., Yarden Y. Derailed endocytosis: an emerging feature of cancer. Nat. Rev. Cancer 2008, 8:835-850.
35. Nakatogawa H., Ichimura Y., Ohsumi Y. Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 2007, 130:165-178.
36. Nishida Y., Arakawa S., Fujitani K., Yamaguchi H., Mizuta T., Kanaseki T., Komatsu M., Otsu K., Tsujimoto Y., Shimizu S. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 2009, 461:654-658.
37. Pankiv S., Alemu E.A., Brech A., Bruun J.A., Lamark T., Overvatn A., Bjørkøy G., Johansen T. FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport. J. Cell Biol. 2010, 188:253-269.
38. Peralta E.R., Martin B.C., Edinger A.L. Differential effects of TBC1D15 and mammalian Vps39 on Rab7 activation state, lysosomal morphology, and growth factor dependence. J. Biol. Chem. 2010, 285:16814-16821.
39. Popovic D., Akutsu M., Novak I., Harper J.W., Behrends C., Dikic I. Rab GTPase-activating proteins in autophagy: regulation of endocytic and autophagy pathways by direct binding to human ATG8 modifiers. Mol. Cell. Biol. 2012, 32:1733-1744.
40. Ravikumar B., Moreau K., Jahreiss L., Puri C., Rubinsztein D.C. Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat. Cell Biol. 2010, 12:747-757.
41. Ravikumar B., Sarkar S., Davies J.E., Futter M., Garcia-Arencibia M., Green-Thompson Z.W., Jimenez-Sanchez M., Korolchuk V.I., Lichtenberg M., Luo S., et al. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol. Rev. 2010, 90:1383-1435.
42. Rozenknop A., Rogov V.V., Rogova N.Y., Löhr F., Güntert P., Dikic I., Dötsch V. Characterization of the interaction of GABARAPL-1 with the LIR motif of NBR1. J. Mol. Biol. 2011, 410:477-487.
43. Saci A., Cantley L.C., Carpenter C.L. Rac1 regulates the activity of mTORC1 and mTORC2 and controls cellular size. Mol. Cell 2011, 42:50-61.
44. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 2009, 10:513-525.
45. Stinchcombe J.C., Nomoto H., Cutler D.F., Hopkins C.R. Anterograde and retrograde traffic between the rough endoplasmic reticulum and the Golgi complex. J. Cell Biol. 1995, 131:1387-1401.
46. Sun Q., Westphal W., Wong K.N., Tan I., Zhong Q. Rubicon controls endosome maturation as a Rab7 effector. Proc. Natl. Acad. Sci. USA 2010, 107:19338-19343.
47. Tooze S.A. The role of membrane proteins in mammalian autophagy. Semin. Cell Dev. Biol. 2010, 21:677-682.
48. Underwood B.R., Imarisio S., Fleming A., Rose C., Krishna G., Heard P., Quick M., Korolchuk V.I., Renna M., Sarkar S., et al. Antioxidants can inhibit basal autophagy and enhance neurodegeneration in models of polyglutamine disease. Hum. Mol. Genet. 2010, 19:3413-3429.
49. Vega F.M., Ridley A.J. Rho GTPases in cancer cell biology. FEBS Lett. 2008, 582:2093-2101.
50. Webb J.L., Ravikumar B., Atkins J., Skepper J.N., Rubinsztein D.C. Alpha-Synuclein is degraded by both autophagy and the proteasome. J. Biol. Chem. 2003, 278:25009-25013.
51. Webber J.L., Tooze S.A. Coordinated regulation of autophagy by p38alpha MAPK through mAtg9 and p38IP. EMBO J. 2010, 29:27-40.
52. Weidberg H., Shpilka T., Shvets E., Abada A., Shimron F., Elazar Z. LC3 and GATE-16 N termini mediate membrane fusion processes required for autophagosome biogenesis. Dev. Cell 2011, 20:444-454.
53. Zhang X.-M., Walsh B., Mitchell C.A., Rowe T. TBC domain family, member 15 is a novel mammalian Rab GTPase-activating protein with substrate preference for Rab7. Biochem. Biophys. Res. Commun. 2005, 335:154-161.
54. Zhu W.L., Hossain M.S., Guo D.Y., Liu S., Tong H., Khakpoor A., Casey P.J., Wang M. A role for the Rac3 GTPase in autophagy regulation. J. Biol. Chem. 2011, 286:35291-35298.
55. Zoncu R., Efeyan A., Sabatini D.M. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat. Rev. Mol. Cell Biol. 2011, 12:21-35.
56. Zoppino F.C., Militello R.D., Slavin I., Alvarez C., Colombo M.I. Autophagosome formation depends on the small GTPase Rab1 and functional ER exit sites. Traffic 2010, 11:1246-1261.