Role of AP1 and Gadkin in the traffic of secretory endo-lysosomes

Molecular Biology of the Cell

Volumn 22, Issue 12, 2011, Pages 2068-2082

  Laulagnier, Karine ^a,d   Schieber, Nicole L ^b   Maritzen, Tanja ^c   Haucke, Volker ^c   Parton, Robert G ^b   Gruenberg, Jean ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA N ACETYLHEXOSAMINIDASE; CATHEPSIN D; CHOLESTEROL; CLATHRIN; F ACTIN; GADKIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOME ENZYME; MEMBRANE PROTEIN; RAB INTERACTING LYSOSOMAL PROTEIN; RAB PROTEIN; RAB27A PROTEIN; RAB5 PROTEIN; RAB7 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR AP 2; TRANSCRIPTION FACTOR AP 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CELL MIGRATION; CONTROLLED STUDY; CROSS LINKING; DEPOLYMERIZATION; DONOR; ENDOCYTOSIS; ENDOLYSOSOME; EXOCYTOSIS; FIBROBLAST; FRACTIONATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LYSOSOME; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL;

ACTINS; ADAPTOR PROTEIN COMPLEX 1; ANIMALS; BIOLOGICAL TRANSPORT; CRICETINAE; CYTOSOL; ENDOCYTOSIS; ENDOSOMES; EXOCYTOSIS; FIBROBLASTS; HEXOSAMINIDASES; HUMANS; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; LYSOSOMES; MEMBRANE PROTEINS; RAB GTP-BINDING PROTEINS; RNA INTERFERENCE;

EID: 79959245840     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-03-0193     Document Type: Article

References (93)

1. Abrami L, Bischofberger M, Kunz B, Groux R, Van Der Goot FG (2010). Endocytosis of the anthrax toxin is mediated by clathrin, actin and unconventional adaptors. PLoS Pathog 6, e1000792.
2. Andrews NW (2000). Regulated secretion of conventional lysosomes. Trends Cell Biol 10, 316-321.
3. Andrews NW (2002). Lysosomes and the plasma membrane: trypanosomes reveal a secret relationship. J Cell Biol 158, 389-394.
4. Aniento F, Emans N, Griffiths G, Gruenberg J (1993). Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. J Cell Biol 123, 1373-1387. (Pubitemid 24012018)
5. Barral DC, Seabra MC (2004). The melanosome as a model to study organelle motility in mammals. Pigment Cell Res 17, 111-118. (Pubitemid 38419637)
6. Baust T, Anitei M, Czupalla C, Parshyna I, Bourel L, Thiele C, Krause E, Hoflack B (2008). Protein networks supporting AP-3 function in targeting lysosomal membrane proteins. Mol Biol Cell 19, 1942-1951.
7. Bensadoun A, Weinstein D (1976). Assay of proteins in the presence of interfering materials. Anal Biochem 70, 241-250.
8. Berger AC, Salazar G, Styers ML, Newell-Litwa KA, Werner E, Maue RA, Corbett AH, Faundez V (2007). The subcellular localization of the Niemann-Pick Type C proteins depends on the adaptor complex AP-3. J Cell Sci 120, 3640-3652. (Pubitemid 350120956)
9. Bonifacino JS (2004). The GGA proteins: adaptors on the move. Nat Rev Mol Cell Biol 5, 23-32.
10. Bonifacino JS, Traub LM (2003). Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72, 395-447. (Pubitemid 36930451)
11. Brachet V, Pehau-Arnaudet G, Desaymard C, Raposo G, Amigorena S (1999). Early endosomes are required for major histocompatiblity complex class II transport to peptide-loading compartments. Mol Biol Cell 10, 2891-2904. (Pubitemid 29441570)
12. Bucci C, Thomsen P, Nicoziani P, McCarthy J, van Deurs B (2000). Rab7: a key to lysosome biogenesis. Mol Biol Cell 11, 467-480. (Pubitemid 30112158)
13. Cantalupo G, Alifano P, Roberti V, Bruni CB, Bucci C (2001). Rab-interacting lysosomal protein (RILP): the Rab7 effector required for transport to lysosomes. EMBO J 20, 683-693. (Pubitemid 32167633)
14. Chapuy B, Tikkanen R, Muhlhausen C, Wenzel D, von Figura K, Honing S (2008). AP-1 and AP-3 mediate sorting of melanosomal and lysosomal membrane proteins into distinct post-Golgi trafficking pathways. Traffic 9, 1157-1172. (Pubitemid 351916890)
15. Clark R, Griffiths GM (2003). Lytic granules, secretory lysosomes and disease. Curr Opin Immunol 15, 516-521. (Pubitemid 37130191)
16. Czibener C, Sherer NM, Becker SM, Pypaert M, Hui E, Chapman ER, Mothes W, Andrews NW (2006). Ca2+ and synaptotagmin VII-dependent delivery of lysosomal membrane to nascent phagosomes. J Cell Biol 174, 997-1007.
17. Delevoye C et al. (2009). AP-1 and KIF13A coordinate endosomal sorting and positioning during melanosome biogenesis. J Cell Biol 187, 247-264.
18. Dell'Angelica EC, Shotelersuk V, Aguilar RC, Gahl WA, Bonifacino JS (1999). Altered trafficking of lysosomal proteins in Hermansky-Pudlak syndrome due to mutations in the beta 3A subunit of the AP-3 adaptor. Mol Cell 3, 11-21. (Pubitemid 29292473)
19. Denzer K, Kleijmeer MJ, Heijnen HF, Stoorvogel W, Geuze HJ (2000). Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci 113, Pt 19, 3365-3374.
20. Desnos C et al. (2003). Rab27A and its effector MyRIP link secretory granules to F-actin and control their motion towards release sites. J Cell Biol 163, 559-570. (Pubitemid 37429869)
21. Eder C (2009). Mechanisms of interleukin-1beta release. Immunobiology 214, 543-553.
22. Faundez V, Horng JT, Kelly RB (1997). ADP ribosylation factor 1 is required for synaptic vesicle budding in PC12 cells. J Cell Biol 138, 505-515. (Pubitemid 27349834)
23. Faundez V, Horng JT, Kelly RB (1998). A function for the AP3 coat complex in synaptic vesicle formation from endosomes. Cell 93, 423-432. (Pubitemid 28232086)
24. Fukuda M (2005). Versatile role of Rab27 in membrane trafficking: focus on the Rab27 effector families. J Biochem 137, 9-16.
25. Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O (2009). Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 11, 1143-1149.
26. Gieselmann V, Pohlmann R, Hasilik A, Von Figura K (1983). Biosynthesis and transport of cathepsin D in cultured human fibroblasts. J Cell Biol 97, 1-5. (Pubitemid 13076510)
27. Glickman JN, Kornfeld S (1993). Mannose 6-phosphate-independent targeting of lysosomal enzymes in I-cell disease B lymphoblasts. J Cell Biol 123, 99-108. (Pubitemid 23284866)
28. Glyvuk N, Tsytsyura Y, Geumann C, D'Hooge R, Huve J, Kratzke M, Baltes J, Boening D, Klingauf J, Schu P (2010). AP-1/sigma1B-adaptin mediates endosomal synaptic vesicle recycling, learning and memory. EMBO J 29, 1318-1330.
29. Gottardi CJ, Dunbar LA, Caplan MJ (1995). Biotinylation and assessment of membrane polarity: caveats and methodological concerns. Am J Physiol 268, F285-F295.
30. Griffiths G, McDowall A, Back R, Dubochet J (1984). On the preparation of cryosections for immunocytochemistry. J Ultrastruct Res 89, 65-78. (Pubitemid 15145723)
31. Groux-Degroote S, van Dijk SM, Wolthoorn J, Neumann S, Theos AC, De Maziere AM, Klumperman J, van Meer G, Sprong H (2008). Glycolipid-dependent sorting of melanosomal from lysosomal membrane proteins by lumenal determinants. Traffic 9, 951-963. (Pubitemid 351639498)
32. Gruenberg J (2001). The endocytic pathway: a mosaic of domains. Nat Rev Mol Cell Biol 2, 721-730.
33. Gruenberg J, Griffiths G, Howell KE (1989). Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J Cell Biol 108, 1301-1316. (Pubitemid 19097039)
34. Harter C, Mellman I (1992). Transport of the lysosomal membrane glycoprotein lgp120 (lgp-A) to lysosomes does not require appearance on the plasma membrane. J Cell Biol 117, 311-325.
35. Ihrke G, Kyttala A, Russell MR, Rous BA, Luzio JP (2004). Differential use of two AP-3-mediated pathways by lysosomal membrane proteins. Traffic 5, 946-962.
36. Isidoro C, Baccino FM, Hasilik A (1998). Human and hamster procathepsin D, although equally tagged with mannose-6-phosphate, are differentially targeted to lysosomes in transfected BHK cells. Cell Tissue Res 292, 303-310. (Pubitemid 28230217)
37. Jaiswal JK, Andrews NW, Simon SM (2002). Membrane proximal lysosomes are the major vesicles responsible for calcium-dependent exocytosis in nonsecretory cells. J Cell Biol 159, 625-635.
38. Janvier K, Bonifacino JS (2005). Role of the endocytic machinery in the sorting of lysosome-associated membrane proteins. Mol Biol Cell 16, 4231-4242. (Pubitemid 41262892)
39. Johansson M, Rocha N, Zwart W, Jordens I, Janssen L, Kuijl C, Olkkonen VM, Neefjes J (2007). Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor betalll spectrin. J Cell Biol 176, 459-471.
40. Jordens I, Fernandez-Borja M, Marsman M, Dusseljee S, Janssen L, Calafat J, Janssen H, Wubbolts R, Neefjes J (2001). The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dyneindynactin motors. Curr Biol 11, 1680-1685. (Pubitemid 33037779)
41. Klausner RD, Donaldson JG, Lippincott-Schwartz J (1992). Brefeldin A: insights into the control of membrane traffic and organelle structure. J Cell Biol 116, 1071-1080.
42. Ko DC, Gordon MD, Jin JY, Scott MP (2001). Dynamic movements of organelles containing Niemann-Pick C1 protein: NPC1 involvement in late endocytic events. Mol Biol Cell 12, 601-614. (Pubitemid 33052015)
43. Kobayashi T, Beuchat MH, Lindsay M, Frias S, Palmiter RD, Sakuraba H, Parton RG, Gruenberg J (1999). Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport. Nat Cell Biol 1, 113-118. (Pubitemid 129501953)
44. Kobayashi T, Stang E, Fang KS, de Moerloose P, Parton RG, Gruenberg J (1998). A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392, 193-197. (Pubitemid 28162794)
45. Kobayashi T, Vischer UM, Rosnoblet C, Lebrand C, Lindsay M, Parton RG, Kruithof EK, Gruenberg J (2000). The tetraspanin CD63/lamp3 cycles between endocytic and secretory compartments in human endothelial cells. Mol Biol Cell 11, 1829-1843. (Pubitemid 30307916)
46. Kroemer G, Jaattela M (2005). Lysosomes and autophagy in cell death control. Nat Rev Cancer 5, 886-897. (Pubitemid 41746033)
47. Le Borgne R, Alconada A, Bauer U, Hoflack B (1998). The mammalian AP-3 adaptor-like complex mediates the intracellular transport of lysosomal membrane glycoproteins. J Biol Chem 273, 29451-29461. (Pubitemid 28509949)
48. Lebrand C, Corti M, Goodson H, Cosson P, Cavalli V, Mayran N, Faure J, Gruenberg J (2002). Late endosome motility depends on lipids via the small GTPase Rab7. EMBO J 21, 1289-1300. (Pubitemid 34246508)
49. Lee YS et al. (2009). Silencing by small RNAs is linked to endosomal trafficking. Nat Cell Biol 11, 1150-1156.
50. Lefkir Y, Malbouyres M, Gotthardt D, Ozinsky A, Cornillon S, Bruckert F, Aderem AA, Soldati T, Cosson P, Letourneur F (2004). Involvement of the AP-1 adaptor complex in early steps of phagocytosis and macropinocytosis. Mol Biol Cell 15, 861-869. (Pubitemid 38146499)
51. Lippincott-Schwartz J, Fambrough DM (1987). Cycling of the integral membrane glycoprotein, LEP100, between plasma membrane and lysosomes: kinetic and morphological analysis. Cell 49, 669-677.
52. Liscum L, Ruggiero RM, Faust JR (1989). The intracellular transport of low density lipoprotein-derived cholesterol is defective in Niemann-Pick type C fibroblasts. J Cell Biol 108, 1625-1636. (Pubitemid 19130495)
53. Ludwig T, Griffiths G, Hoflack B (1991). Distribution of newly synthesized lysosomal enzymes in the endocytic pathway of normal rat kidney cells. J Cell Biol 115, 1561-1572. (Pubitemid 21909996)
54. Ludwig T, Munier-Lehmann H, Bauer U, Hollinshead M, Ovitt C, Lobel P, Hoflack B (1994). Differential sorting of lysosomal enzymes in mannose 6-phosphate receptor-deficient fibroblasts. EMBO J 13, 3430-3437. (Pubitemid 24246178)
55. Luzio JP, Pryor PR, Bright NA (2007). Lysosomes: fusion and function. Nat Rev Mol Cell Biol 8, 622-632. (Pubitemid 47106614)
56. Maritzen T, Haucke V (2010). Gadkin: A novel link between endosomal vesicles and microtubule tracks. Commun Integr Biol 3, 299-302.
57. Maritzen T, Schmidt MR, Kukhtina V, Higman VA, Strauss H, Volkmer R, Oschkinat H, Dotti CG, Haucke V (2010). A novel subtype of AP-1- binding motif within the palmitoylated trans-Golgi network/endosomal accessory protein Gadkin/gamma-BAR. J Biol Chem 285, 4074-4086.
58. Martinez I, Chakrabarti S, Hellevik T, Morehead J, Fowler K, Andrews NW (2000). Synaptotagmin VII regulates Ca(2+)-dependent exocytosis of lysosomes in fibroblasts. J Cell Biol 148, 1141-1149.
59. Mayor S, Pagano RE (2007). Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 8, 603-612. (Pubitemid 47106613)
60. Meyer C, Zizioli D, Lausmann S, Eskelinen EL, Hamann J, Saftig P, von Figura K, Schu P (2000). mu1A-adaptin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors. EMBO J 19, 2193-2203. (Pubitemid 30259000)
61. Mizuno K, Tolmachova T, Ushakov DS, Romao M, Abrink M, Ferenczi MA, Raposo G, Seabra MC (2007). Rab27b regulates mast cell granule dynamics and secretion. Traffic 8, 883-892. (Pubitemid 46971634)
62. Neubrand VE, Will RD, Mobius W, Poustka A, Wiemann S, Schu P, Dotti CG, Pepperkok R, Simpson JC (2005). Gamma-BAR, a novel AP-1-interacting protein involved in post-Golgi trafficking. EMBO J 24, 1122-1133. (Pubitemid 40516596)
63. Novak EK, Gautam R, Reddington M, Collinson LM, Copeland NG, Jenkins NA, McGarry MP, Swank RT (2002). The regulation of platelet-dense granules by Rab27a in the ashen mouse, a model of Hermansky-Pudlak and Griscelli syndromes, is granule-specific and dependent on genetic background. Blood 100, 128-135. (Pubitemid 35177437)
64. Ostrowski M et al. (2010). Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 12, 19-30; supp 1-13.
65. Parton RG, Schrotz P, Bucci C, Gruenberg J (1992). Plasticity of early endosomes. J Cell Sci 103, Pt 2335-348.
66. Peden AA, Oorschot V, Hesser BA, Austin CD, Scheller RH, Klumperman J (2004). Localization of the AP-3 adaptor complex defines a novel endosomal exit site for lysosomal membrane proteins. J Cell Biol 164, 1065-1076. (Pubitemid 38429132)
67. Pizarro-Cerda J, Payrastre B, Wang YJ, Veiga E, Yin HL, Cossart P (2007). Type II phosphatidylinositol 4-kinases promote Listeria monocytogenes entry into target cells. Cell Microbiol 9, 2381-2390. (Pubitemid 47365644)
68. Puertollano R, Aguilar RC, Gorshkova I, Crouch RJ, Bonifacino JS (2001). Sorting of mannose 6-phosphate receptors mediated by the GGAs. Science 292, 1712-1716. (Pubitemid 32506243)
69. Puri C (2009). Loss of myosin VI no insert isoform (NoI) induces a defect in clathrin-mediated endocytosis and leads to caveolar endocytosis of transferrin receptor. J Biol Chem 284, 34998-35014.
70. Rao SK, Huynh C, Proux-Gillardeaux V, Galli T, Andrews NW (2004). Identification of SNAREs involved in synaptotagmin VII-regulated lysosomal exocytosis. J Biol Chem 279, 20471-20479. (Pubitemid 38623494)
71. Raposo G, Fevrier B, Stoorvogel W, Marks MS (2002). Lysosome-related organelles: a view from immunity and pigmentation. Cell Struct Funct 27, 443-456. (Pubitemid 36267713)
72. Raposo G, Marks MS, Cutler DF (2007). Lysosome-related organelles: driving post-Golgi compartments into specialisation. Curr Opin Cell Biol 19, 394-401. (Pubitemid 47268761)
73. Raposo G, Tenza D, Mecheri S, Peronet R, Bonnerot C, Desaymard C (1997). Accumulation of major histocompatibility complex class II molecules in mast cell secretory granules and their release upon degranulation. Mol Biol Cell 8, 2631-2645. (Pubitemid 27528227)
74. Reddy A, Caler EV, Andrews NW (2001). Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes. Cell 106, 157-169. (Pubitemid 32772627)
75. Reusch U, Bernhard O, Koszinowski U, Schu P (2002). AP-1A and AP-3A lysosomal sorting functions. Traffic 3, 752-761.
76. Robinson MS (2004). Adaptable adaptors for coated vesicles. Trends Cell Biol 14, 167-174.
77. Robinson MS, Kreis TE (1992). Recruitment of coat proteins onto Golgi membranes in intact and permeabilized cells: effects of brefeldin A and G protein activators. Cell 69, 129-138.
78. Robinson MS, Sahlender DA, Foster SD (2010). Rapid inactivation of proteins by rapamycin-induced rerouting to mitochondria. Dev Cell 18, 324-331.
79. Rocha N, Kuijl C, Van Der Kant R, Janssen L, Houben D, Janssen H, Zwart W, Neefjes J (2009). Cholesterol sensor ORP1L contacts the ER protein VAP to control Rab7-RILP-p150 Glued and late endosome positioning. J Cell Biol 185, 1209-1225.
80. Rodriguez A, Webster P, Ortego J, Andrews NW (1997). Lysosomes behave as Ca2+-regulated exocytic vesicles in fibroblasts and epithelial cells. J Cell Biol 137, 93-104. (Pubitemid 27167298)
81. Rojo M, Pepperkok R, Emery G, Kellner R, Stang E, Parton RG, Gruenberg J (1997). Involvement of the transmembrane protein p23 in biosynthetic protein transport. J Cell Biol 139, 1119-1135.
82. Salazar G, Love R, Styers ML, Werner E, Peden A, Rodriguez S, Gearing M, Wainer BH, Faundez V (2004). AP-3-dependent mechanisms control the targeting of a chloride channel (ClC-3) in neuronal and non-neuronal cells. J Biol Chem 279, 25430-25439. (Pubitemid 38756800)
83. Schmidt MR, Maritzen T, Kukhtina V, Higman VA, Doglio L, Barak NN, Strauss H, Oschkinat H, Dotti CG, Haucke V (2009). Regulation of endosomal membrane traffic by a Gadkin/AP-1/kinesin KIF5 complex. Proc Natl Acad Sci USA 106, 15344-15349.
84. Stoorvogel W (1998). Analysis of the endocytic system by using horseradish peroxidase. Trends Cell Biol 8, 503-505.
85. Stoorvogel W, Kleijmeer MJ, Geuze HJ, Raposo G (2002). The biogenesis and functions of exosomes. Traffic 3, 321-330. (Pubitemid 34461042)
86. Theos AC et al. (2005). Functions of adaptor protein (AP)-3 and AP-1 in tyrosinase sorting from endosomes to melanosomes. Mol Biol Cell 16, 5356-5372. (Pubitemid 41566845)
87. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brugger B, Simons M (2008). Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319, 1244-1247. (Pubitemid 351323020)
88. Zaidi N, Maurer A, Nieke S, Kalbacher H (2008). Cathepsin D: a cellular roadmap. Biochem Biophys Res Commun 376, 5-9.
89. Zeelenberg IS et al. (2008). Targeting tumor antigens to secreted membrane vesicles in vivo induces efficient antitumor immune responses. Cancer Res 68, 1228-1235. (Pubitemid 351272243)
90. Zerial M, McBride H (2001). Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2, 107-117. (Pubitemid 33674039)
91. Zhang M, Dwyer NK, Love DC, Cooney A, Comly M, Neufeld E, Pentchev PG, Blanchette-Mackie EJ, Hanover JA (2001). Cessation of rapid late endosomal tubulovesicular trafficking in Niemann-Pick type C1 disease. Proc Natl Acad Sci USA 98, 4466-4471. (Pubitemid 32295000)
92. Zhao H, Ito Y, Chappel J, Andrews NW, Teitelbaum SL, Ross FP (2008). Synaptotagmin VII regulates bone remodeling by modulating osteoclast and osteoblast secretion. Dev Cell 14, 914-925. (Pubitemid 351757201)
93. Zhao H, Vaananen HK (2006). Pharmacological sequestration of intracellular cholesterol in late endosomes disrupts ruffled border formation in osteoclasts. J Bone Miner Res 21, 456-465.