Basolateral Endocytic Recycling Requires RAB-10 and AMPH-1 Mediated Recruitment of RAB-5 GAP TBC-2 to Endosomes
When cargo is internalized from the cell surface by endocytosis, it enters a series of intracellular organelles called endosomes. Endosomes sort cargo, such that some cargos are sent to the lysosome for degradation, while others are recycled to the plasma membrane. Small GTPase proteins of the Rabs family are master regulators of endosomes, functioning by acting as molecular switches. As cargo moves through the endosomal system, it must pass from the domain controlled by one Rab-GTPase to the domain controlled by another. Little is known about how transitions along the recycling pathway are controlled. Here we analyze a group of protein interactions that act along the early-to-recycling pathway. Our work shows that RAB-5 deactivation mediated by TBC-2 and its recruiters RAB-10 and AMPH-1 is important for cargo recycling. This work provides mechanistic insight into how Rab proteins controlling different steps of trafficking interact during endocytic recycling.
Vyšlo v časopise:
Basolateral Endocytic Recycling Requires RAB-10 and AMPH-1 Mediated Recruitment of RAB-5 GAP TBC-2 to Endosomes. PLoS Genet 11(9): e32767. doi:10.1371/journal.pgen.1005514
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1005514
Souhrn
When cargo is internalized from the cell surface by endocytosis, it enters a series of intracellular organelles called endosomes. Endosomes sort cargo, such that some cargos are sent to the lysosome for degradation, while others are recycled to the plasma membrane. Small GTPase proteins of the Rabs family are master regulators of endosomes, functioning by acting as molecular switches. As cargo moves through the endosomal system, it must pass from the domain controlled by one Rab-GTPase to the domain controlled by another. Little is known about how transitions along the recycling pathway are controlled. Here we analyze a group of protein interactions that act along the early-to-recycling pathway. Our work shows that RAB-5 deactivation mediated by TBC-2 and its recruiters RAB-10 and AMPH-1 is important for cargo recycling. This work provides mechanistic insight into how Rab proteins controlling different steps of trafficking interact during endocytic recycling.
Zdroje
1. Grant BD, Donaldson JG (2009) Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10: 597–608. doi: 10.1038/nrm2755 19696797
2. Eaton S, Martin-Belmonte F (2014) Cargo sorting in the endocytic pathway: a key regulator of cell polarity and tissue dynamics. Cold Spring Harb Perspect Biol 6: a016899. doi: 10.1101/cshperspect.a016899 25125399
3. Folsch H, Mattila PE, Weisz OA (2009) Taking the scenic route: biosynthetic traffic to the plasma membrane in polarized epithelial cells. Traffic 10: 972–981. doi: 10.1111/j.1600-0854.2009.00927.x 19453969
4. Brown PS, Wang E, Aroeti B, Chapin SJ, Mostov KE, et al. (2000) Definition of distinct compartments in polarized Madin-Darby canine kidney (MDCK) cells for membrane-volume sorting, polarized sorting and apical recycling. Traffic 1: 124–140. 11208093
5. Wang E, Brown PS, Aroeti B, Chapin SJ, Mostov KE, et al. (2000) Apical and basolateral endocytic pathways of MDCK cells meet in acidic common endosomes distinct from a nearly-neutral apical recycling endosome. Traffic 1: 480–493. 11208134
6. Sobajima T, Yoshimura S, Iwano T, Kunii M, Watanabe M, et al. (2014) Rab11a is required for apical protein localisation in the intestine. Biol Open 4: 86–94. doi: 10.1242/bio.20148532 25527643
7. Casanova JE, Wang X, Kumar R, Bhartur SG, Navarre J, et al. (1999) Association of Rab25 and Rab11a with the apical recycling system of polarized Madin-Darby canine kidney cells. Mol Biol Cell 10: 47–61. 9880326
8. Sato T, Mushiake S, Kato Y, Sato K, Sato M, et al. (2007) The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 448: 366–369. 17597763
9. Grant B, Zhang Y, Paupard MC, Lin SX, Hall DH, et al. (2001) Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat Cell Biol 3: 573–579. 11389442
10. Chen CC, Schweinsberg PJ, Vashist S, Mareiniss DP, Lambie EJ, et al. (2006) RAB-10 is required for endocytic recycling in the Caenorhabditis elegans intestine. Mol Biol Cell 17: 1286–1297. 16394106
11. Shi A, Liu O, Koenig S, Banerjee R, Chen CC, et al. (2012) RAB-10-GTPase-mediated regulation of endosomal phosphatidylinositol-4,5-bisphosphate. Proc Natl Acad Sci U S A 109: E2306–2315. doi: 10.1073/pnas.1205278109 22869721
12. Lin SX, Grant B, Hirsh D, Maxfield FR (2001) Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells. Nat Cell Biol 3: 567–572. 11389441
13. Caplan S, Naslavsky N, Hartnell LM, Lodge R, Polishchuk RS, et al. (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. 12032069
14. Shi A, Chen CC, Banerjee R, Glodowski D, Audhya A, et al. (2010) EHBP-1 functions with RAB-10 during endocytic recycling in Caenorhabditis elegans. Mol Biol Cell 21: 2930–2943. doi: 10.1091/mbc.E10-02-0149 20573983
15. Guilherme A, Soriano NA, Furcinitti PS, Czech MP (2004) Role of EHD1 and EHBP1 in perinuclear sorting and insulin-regulated GLUT4 recycling in 3T3-L1 adipocytes. J Biol Chem 279: 40062–40075. 15247266
16. Brown FD, Rozelle AL, Yin HL, Balla T, Donaldson JG (2001) Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic. J Cell Biol 154: 1007–1017. 11535619
17. Babbey CM, Ahktar N, Wang E, Chen CC, Grant BD, et al. (2006) Rab10 regulates membrane transport through early endosomes of polarized Madin-Darby canine kidney cells. Mol Biol Cell 17: 3156–3175. 16641372
18. Glodowski DR, Chen CC, Schaefer H, Grant BD, Rongo C (2007) RAB-10 regulates glutamate receptor recycling in a cholesterol-dependent endocytosis pathway. Mol Biol Cell 18: 4387–4396. 17761527
19. Sasidharan N, Sumakovic M, Hannemann M, Hegermann J, Liewald JF, et al. (2012) RAB-5 and RAB-10 cooperate to regulate neuropeptide release in Caenorhabditis elegans. Proc Natl Acad Sci U S A 109: 18944–18949. doi: 10.1073/pnas.1203306109 23100538
20. Wang D, Lou J, Ouyang C, Chen W, Liu Y, et al. (2010) Ras-related protein Rab10 facilitates TLR4 signaling by promoting replenishment of TLR4 onto the plasma membrane. Proc Natl Acad Sci U S A 107: 13806–13811. doi: 10.1073/pnas.1009428107 20643919
21. Wang T, Liu Y, Xu XH, Deng CY, Wu KY, et al. (2011) Lgl1 activation of rab10 promotes axonal membrane trafficking underlying neuronal polarization. Dev Cell 21: 431–444. doi: 10.1016/j.devcel.2011.07.007 21856246
22. Deng CY, Lei WL, Xu XH, Ju XC, Liu Y, et al. (2014) JIP1 mediates anterograde transport of Rab10 cargos during neuronal polarization. J Neurosci 34: 1710–1723. doi: 10.1523/JNEUROSCI.4496-13.2014 24478353
23. Chen Y, Wang Y, Zhang J, Deng Y, Jiang L, et al. (2012) Rab10 and myosin-Va mediate insulin-stimulated GLUT4 storage vesicle translocation in adipocytes. J Cell Biol 198: 545–560. doi: 10.1083/jcb.201111091 22908308
24. Hutagalung AH, Novick PJ (2011) Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91: 119–149. doi: 10.1152/physrev.00059.2009 21248164
25. Chotard L, Mishra AK, Sylvain MA, Tuck S, Lambright DG, et al. (2010) TBC-2 regulates RAB-5/RAB-7-mediated endosomal trafficking in Caenorhabditis elegans. Mol Biol Cell 21: 2285–2296. doi: 10.1091/mbc.E09-11-0947 20462958
26. Manders EM, Stap J, Brakenhoff GJ, van Driel R, Aten JA (1992) Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. J Cell Sci 103 (Pt 3): 857–862.
27. Sun L, Liu O, Desai J, Karbassi F, Sylvain MA, et al. (2012) CED-10/Rac1 regulates endocytic recycling through the RAB-5 GAP TBC-2. PLoS Genet 8: e1002785. doi: 10.1371/journal.pgen.1002785 22807685
28. Xin X, Gfeller D, Cheng J, Tonikian R, Sun L, et al. (2013) SH3 interactome conserves general function over specific form. Mol Syst Biol 9: 652. doi: 10.1038/msb.2013.9 23549480
29. Pant S, Sharma M, Patel K, Caplan S, Carr CM, et al. (2009) AMPH-1/Amphiphysin/Bin1 functions with RME-1/Ehd1 in endocytic recycling. Nat Cell Biol 11: 1399–1410. doi: 10.1038/ncb1986 19915558
30. Barr F, Lambright DG (2010) Rab GEFs and GAPs. Curr Opin Cell Biol 22: 461–470. doi: 10.1016/j.ceb.2010.04.007 20466531
31. Grosshans BL, Ortiz D, Novick P (2006) Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci U S A 103: 11821–11827. 16882731
32. Wandinger-Ness A, Zerial M (2014) Rab proteins and the compartmentalization of the endosomal system. Cold Spring Harb Perspect Biol 6: a022616. doi: 10.1101/cshperspect.a022616 25341920
33. Poteryaev D, Datta S, Ackema K, Zerial M, Spang A (2010) Identification of the switch in early-to-late endosome transition. Cell 141: 497–508. doi: 10.1016/j.cell.2010.03.011 20434987
34. Wang W, Ferro-Novick S (2002) A Ypt32p exchange factor is a putative effector of Ypt1p. Mol Biol Cell 13: 3336–3343. 12221137
35. Del Conte-Zerial P, Brusch L, Rink JC, Collinet C, Kalaidzidis Y, et al. (2008) Membrane identity and GTPase cascades regulated by toggle and cut-out switches. Mol Syst Biol 4: 206. doi: 10.1038/msb.2008.45 18628746
36. Rivera-Molina FE, Novick PJ (2009) A Rab GAP cascade defines the boundary between two Rab GTPases on the secretory pathway. Proc Natl Acad Sci U S A 106: 14408–14413. doi: 10.1073/pnas.0906536106 19666511
37. Rodal AA, Blunk AD, Akbergenova Y, Jorquera RA, Buhl LK, et al. (2011) A presynaptic endosomal trafficking pathway controls synaptic growth signaling. J Cell Biol 193: 201–217. doi: 10.1083/jcb.201009052 21464232
38. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94. 4366476
39. Sato M, Sato K, Fonarev P, Huang CJ, Liou W, et al. (2005) Caenorhabditis elegans RME-6 is a novel regulator of RAB-5 at the clathrin-coated pit. Nat Cell Biol 7: 559–569. 15895077
40. Praitis V, Casey E, Collar D, Austin J (2001) Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157: 1217–1226. 11238406
41. Mello C, Fire A (1995) DNA transformation. Methods Cell Biol 48: 451–482. 8531738
42. Clokey GV, Jacobson LA (1986) The autofluorescent "lipofuscin granules" in the intestinal cells of Caenorhabditis elegans are secondary lysosomes. Mech Ageing Dev 35: 79–94. 3736133
43. Hermann GJ, Schroeder LK, Hieb CA, Kershner AM, Rabbitts BM, et al. (2005) Genetic analysis of lysosomal trafficking in Caenorhabditis elegans. Mol Biol Cell 16: 3273–3288. 15843430
44. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, et al. (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676–682. doi: 10.1038/nmeth.2019 22743772
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2015 Číslo 9
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
Najčítanejšie v tomto čísle
- Arabidopsis AtPLC2 Is a Primary Phosphoinositide-Specific Phospholipase C in Phosphoinositide Metabolism and the Endoplasmic Reticulum Stress Response
- Bridges Meristem and Organ Primordia Boundaries through , , and during Flower Development in
- KLK5 Inactivation Reverses Cutaneous Hallmarks of Netherton Syndrome
- The Chromatin Protein DUET/MMD1 Controls Expression of the Meiotic Gene during Male Meiosis in