CED-10/Rac1 Regulates Endocytic Recycling through the RAB-5 GAP TBC-2

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Rac1 is a founding member of the Rho-GTPase family and a key regulator of membrane remodeling. In the context of apoptotic cell corpse engulfment, CED-10/Rac1 acts with its bipartite guanine nucleotide exchange factor, CED-5/Dock180-CED-12/ELMO, in an evolutionarily conserved pathway to promote phagocytosis. Here we show that in the context of the Caenorhabditis elegans intestinal epithelium CED-10/Rac1, CED-5/Dock180, and CED-12/ELMO promote basolateral recycling. Furthermore, we show that CED-10 binds to the RAB-5 GTPase activating protein TBC-2, that CED-10 contributes to recruitment of TBC-2 to endosomes, and that recycling cargo is trapped in recycling endosomes in ced-12, ced-10, and tbc-2 mutants. Expression of GTPase defective RAB-5(Q78L) also traps recycling cargo. Our results indicate that down-regulation of early endosome regulator RAB-5/Rab5 by a CED-5, CED-12, CED-10, TBC-2 cascade is an important step in the transport of cargo through the basolateral recycling endosome for delivery to the plasma membrane.

Vyšlo v časopise: CED-10/Rac1 Regulates Endocytic Recycling through the RAB-5 GAP TBC-2. PLoS Genet 8(7): e32767. doi:10.1371/journal.pgen.1002785
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002785

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Zdroje

1. McGheeJD The C. elegans Research Community, editor 2007 The C. elegans intestine. WormBook doi/10.1895/wormbook.1.133.1

2. ChenCCSchweinsbergPJVashistSMareinissDPLambieEJ 2006 RAB-10 is required for endocytic recycling in the Caenorhabditis elegans intestine. Mol Biol Cell 17 1286 1297

3. ShiAPantSBalklavaZChenCCFigueroaV 2007 A novel requirement for C. elegans Alix/ALX-1 in RME-1-mediated membrane transport. Curr Biol 17 1913 1924

4. PantSSharmaMPatelKCaplanSCarrCM 2009 AMPH-1/Amphiphysin/Bin1 functions with RME-1/Ehd1 in endocytic recycling. Nat Cell Biol 11 1399 1410

5. ShiASunLBanerjeeRTobinMZhangY 2009 Regulation of endosomal clathrin and retromer-mediated endosome to Golgi retrograde transport by the J-domain protein RME-8. Embo J 28 3290 3302

6. ShiAChenCCBanerjeeRGlodowskiDAudhyaA 2010 EHBP-1 functions with RAB-10 during endocytic recycling in Caenorhabditis elegans. Mol Biol Cell. 21 2930 2943

7. GrantBDDonaldsonJG 2009 Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10 597 608

8. PanCLBaumPDGuMJorgensenEMClarkSG 2008 C. elegans AP-2 and retromer control Wnt signaling by regulating mig-14/Wntless. Dev Cell 14 132 139

9. YangPTLorenowiczMJSilhankovaMCoudreuseDYBetistMC 2008 Wnt signaling requires retromer-dependent recycling of MIG-14/Wntless in Wnt-producing cells. Dev Cell 14 140 147

10. LinSXGrantBHirshDMaxfieldFR 2001 Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells. Nat Cell Biol 3 567 572

11. CaplanSNaslavskyNHartnellLMLodgeRPolishchukRS 2002 A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane. Embo J 21 2557 2567

12. GrantBDCaplanS 2008 Mechanisms of EHD/RME-1 protein function in endocytic transport. Traffic 9 2043 2052

13. KinchenJMRavichandranKS 2007 Journey to the grave: signaling events regulating removal of apoptotic cells. J Cell Sci 120 2143 2149

14. BrugneraEHaneyLGrimsleyCLuMWalkSF 2002 Unconventional Rac-GEF activity is mediated through the Dock180-ELMO complex. Nat Cell Biol 4 574 582

15. ReddienPWHorvitzHR 2000 CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat Cell Biol 2 131 136

16. CabelloJNeukommLJGunesdoganUBurkartKCharetteSJ 2010 The Wnt pathway controls cell death engulfment, spindle orientation, and migration through CED-10/Rac. PLoS Biol 8 e1000297 doi:10.1371/journal.pbio.1000297

17. RadhakrishnaHAl-AwarOKhachikianZDonaldsonJG 1999 ARF6 requirement for Rac ruffling suggests a role for membrane trafficking in cortical actin rearrangements. J Cell Sci 112 Pt 6 855 866

18. KooTHEipperBADonaldsonJG 2007 Arf6 recruits the Rac GEF Kalirin to the plasma membrane facilitating Rac activation. BMC Cell Biol 8 29

19. PalamidessiAFrittoliEGarreMFarettaMMioneM 2008 Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. Cell 134 135 147

20. DonaldsonJGPorat-ShliomNCohenLA 2009 Clathrin-independent endocytosis: a unique platform for cell signaling and PM remodeling. Cell Signal 21 1 6

21. LundquistEAReddienPWHartwiegEHorvitzHRBargmannCI 2001 Three C. elegans Rac proteins and several alternative Rac regulators control axon guidance, cell migration and apoptotic cell phagocytosis. Development 128 4475 4488

22. NaslavskyNWeigertRDonaldsonJG 2003 Convergence of non-clathrin- and clathrin-derived endosomes involves Arf6 inactivation and changes in phosphoinositides. Mol Biol Cell 14 417 431

23. NaslavskyNWeigertRDonaldsonJG 2004 Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol Biol Cell 15 3542 3552

24. WeigertRYeungACLiJDonaldsonJG 2004 Rab22a regulates the recycling of membrane proteins internalized independently of clathrin. Mol Biol Cell 15 3758 3770

25. ClokeyGVJacobsonLA 1986 The autofluorescent “lipofuscin granules” in the intestinal cells of Caenorhabditis elegans are secondary lysosomes. Mech Ageing Dev 35 79 94

26. FrasaMAMaximianoFCSmolarczykKFrancisREBetsonME 2010 Armus is a Rac1 effector that inactivates Rab7 and regulates E-cadherin degradation. Curr Biol 20 198 208

27. ChotardLMishraAKSylvainMATuckSLambrightDG 2010 TBC-2 regulates RAB-5/RAB-7-mediated endosomal trafficking in Caenorhabditis elegans. Mol Biol Cell 21 2285 2296

28. LiWZouWZhaoDYanJZhuZ 2009 C. elegans Rab GTPase activating protein TBC-2 promotes cell corpse degradation by regulating the small GTPase RAB-5. Development 136 2445 2455

29. ChotardLSkorobogataOSylvainMAShrivastavaSRocheleauCE 2010 TBC-2 is required for embryonic yolk protein storage and larval survival during L1 diapause in Caenorhabditis elegans. PLoS ONE 5 e15662 doi:10.1371/journal.pone.0015662

30. HutagalungAHNovickPJ 2011 Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91 119 149

31. RinkJGhigoEKalaidzidisYZerialM 2005 Rab conversion as a mechanism of progression from early to late endosomes. Cell 122 735 749

32. PoteryaevDDattaSAckemaKZerialMSpangA 2010 Identification of the switch in early-to-late endosome transition. Cell 141 497 508

33. KinchenJMRavichandranKS 2010 Identification of two evolutionarily conserved genes regulating processing of engulfed apoptotic cells. Nature 464 778 782

34. NordmannMCabreraMPerzABrockerCOstrowiczC 2010 The Mon1-Ccz1 complex is the GEF of the late endosomal Rab7 homolog Ypt7. Curr Biol 20 1654 1659

35. DenekaMNeeftMPopaIvan OortMSprongH 2003 Rabaptin-5alpha/rabaptin-4 serves as a linker between rab4 and gamma(1)-adaptin in membrane recycling from endosomes. Embo J 22 2645 2657

36. HoogenraadCCPopaIFutaiKMartinez-SanchezEWulfPS 2010 Neuron specific Rab4 effector GRASP-1 coordinates membrane specialization and maturation of recycling endosomes. PLoS Biol 8 e1000283 doi:10.1371/journal.pbio.1000283

37. StenmarkHPartonRGSteele-MortimerOLutckeAGruenbergJ 1994 Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. Embo J 13 1287 1296

38. HsuVWPrekerisR 2010 Transport at the recycling endosome. Curr Opin Cell Biol 22 528 534

39. AngALTaguchiTFrancisSFolschHMurrellsLJ 2004 Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells. J Cell Biol 167 531 543

40. BabbeyCMAhktarNWangEChenCCGrantBD 2006 Rab10 regulates membrane transport through early endosomes of polarized Madin-Darby canine kidney cells. Mol Biol Cell 17 3156 3175

41. SchuckSGerlMJAngAManninenAKellerP 2007 Rab10 is involved in basolateral transport in polarized Madin-Darby canine kidney cells. Traffic 8 47 60

42. ThompsonANesslerRWiscoDAndersonEWincklerB 2007 Recycling endosomes of polarized epithelial cells actively sort apical and basolateral cargos into separate subdomains. Mol Biol Cell 18 2687 2697

43. SonnichsenBDe RenzisSNielsenERietdorfJZerialM 2000 Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol 149 901 914

44. JouTSLeungSMFungLMRuizWGNelsonWJ 2000 Selective alterations in biosynthetic and endocytic protein traffic in Madin-Darby canine kidney epithelial cells expressing mutants of the small GTPase Rac1. Mol Biol Cell 11 287 304

45. StruckhoffECLundquistEA 2003 The actin-binding protein UNC-115 is an effector of Rac signaling during axon pathfinding in C. elegans. Development 130 693 704

46. CardosoCMJordaoLVieiraOV 2010 Rab10 regulates phagosome maturation and its overexpression rescues Mycobacterium-containing phagosomes maturation. Traffic 11 221 235

47. BrennerS 1974 The genetics of Caenorhabditis elegans. Genetics 77 71 94

48. PraitisVCaseyECollarDAustinJ 2001 Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157 1217 1226

49. HermannGJSchroederLKHiebCAKershnerAMRabbittsBM 2005 Genetic analysis of lysosomal trafficking in Caenorhabditis elegans. Mol Biol Cell 16 3273 3288