Home LiteratureArticle Details
PMID: 19841138 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

AP-1 and KIF13A coordinate endosomal sorting and positioning during melanosome biogenesis.

The Journal of cell biology ·Vol. 187 ·No. 2 ·2009-10-19 ·Pages 247-64

Delevoye C, Hurbain I, Tenza D, Sibarita JB, Uzan-Gafsou S, Ohno H, Geerts WJ, Verkleij AJ, Salamero J, Marks MS, Raposo G

Abstract

Specialized cell types exploit endosomal trafficking to deliver protein cargoes to cell type-specific lysosome-related organelles (LROs), but how endosomes are specified for this function is not known. In this study, we show that the clathrin adaptor AP-1 and the kinesin motor KIF13A together create peripheral recycling endosomal subdomains in melanocytes required for cargo delivery to maturing melanosomes. In cells depleted of AP-1 or KIF13A, a subpopulation of recycling endosomes redistributes to pericentriolar clusters, resulting in sequestration of melanosomal enzymes like Tyrp1 in vacuolar endosomes and consequent inhibition of melanin synthesis and melanosome maturation. Immunocytochemistry, live cell imaging, and electron tomography reveal AP-1- and KIF13A-dependent dynamic close appositions and continuities between peripheral endosomal tubules and melanosomes. Our results reveal that LRO protein sorting is coupled to cell type-specific positioning of endosomes that facilitate endosome-LRO contacts and are required for organelle maturation.

MeSH Terms
Cell Line Endosomes/metabolism,ultrastructure Humans Kinesins/genetics,metabolism Melanosomes/metabolism,ultrastructure Microscopy, Electron RNA, Small Interfering/genetics Transcription Factor AP-1/genetics,metabolism
Chemicals
KIF13A protein, human RNA, Small Interfering Transcription Factor AP-1 Kinesins
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Delevoye Cédric
Structure and Membrane Compartments, Centre Nationale de la Recherche Scientifique, UMR 144 Institut Curie, Centre de Recherche, Paris F-75248, France.
Hurbain Ilse
Tenza Danièle
Sibarita Jean-Baptiste
Uzan-Gafsou Stéphanie
Ohno Hiroshi
Geerts Willie J C
Verkleij Arie J
Salamero Jean
Marks Michael S
Raposo Graça
References (53)
53 references, click to expand
  1. Regulation of endosomal membrane traffic by a Gadkin/AP-1/kinesin KIF5 complex.
    Proc Natl Acad Sci U S A. 2009 Sep 8;106(36):15344-9 PMID: 19706427
  2. A novel motor, KIF13A, transports mannose-6-phosphate receptor to plasma membrane through direct interaction with AP-1 complex.
    Cell. 2000 Nov 10;103(4):569-81 PMID: 11106728
  3. A Rab11-containing rapidly recycling compartment in macrophages that promotes phagocytosis.
    Proc Natl Acad Sci U S A. 2000 Jan 18;97(2):680-5 PMID: 10639139
  4. Powering membrane traffic in endocytosis and recycling.
    Nat Rev Mol Cell Biol. 2006 Dec;7(12):897-908 PMID: 17139330
  5. Functions of adaptor protein (AP)-3 and AP-1 in tyrosinase sorting from endosomes to melanosomes.
    Mol Biol Cell. 2005 Nov;16(11):5356-72 PMID: 16162817
  6. Electron tomography of early melanosomes: implications for melanogenesis and the generation of fibrillar amyloid sheets.
    Proc Natl Acad Sci U S A. 2008 Dec 16;105(50):19726-31 PMID: 19033461
  7. Evolving endosomes: how many varieties and why?
    Curr Opin Cell Biol. 2005 Aug;17(4):423-34 PMID: 15975780
  8. Endocytic recycling.
    Nat Rev Mol Cell Biol. 2004 Feb;5(2):121-32 PMID: 15040445
  9. BLOC-1 is required for cargo-specific sorting from vacuolar early endosomes toward lysosome-related organelles.
    Mol Biol Cell. 2007 Mar;18(3):768-80 PMID: 17182842
  10. Rab11 regulates recycling through the pericentriolar recycling endosome.
    J Cell Biol. 1996 Nov;135(4):913-24 PMID: 8922376
  11. Rab11A controls the biogenesis of Birbeck granules by regulating Langerin recycling and stability.
    Mol Biol Cell. 2007 Aug;18(8):3169-79 PMID: 17538027
  12. Glucose transporter 4: cycling, compartments and controversies.
    EMBO Rep. 2005 Dec;6(12):1137-42 PMID: 16319959
  13. A minimal system allowing tubulation with molecular motors pulling on giant liposomes.
    Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):5394-9 PMID: 11959994
  14. Melanosomes--dark organelles enlighten endosomal membrane transport.
    Nat Rev Mol Cell Biol. 2007 Oct;8(10):786-97 PMID: 17878918
  15. Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells.
    J Cell Biol. 2001 Feb 5;152(3):595-606 PMID: 11157985
  16. Distinct protein sorting and localization to premelanosomes, melanosomes, and lysosomes in pigmented melanocytic cells.
    J Cell Biol. 2001 Feb 19;152(4):809-24 PMID: 11266471
  17. The building BLOC(k)s of lysosomes and related organelles.
    Curr Opin Cell Biol. 2004 Aug;16(4):458-64 PMID: 15261680
  18. Visualization of TGN to endosome trafficking through fluorescently labeled MPR and AP-1 in living cells.
    Mol Biol Cell. 2003 Jan;14(1):142-55 PMID: 12529433
  19. BLOC-1 complex deficiency alters the targeting of adaptor protein complex-3 cargoes.
    Mol Biol Cell. 2006 Sep;17(9):4014-26 PMID: 16760431
  20. Disorders of lysosome-related organelle biogenesis: clinical and molecular genetics.
    Annu Rev Genomics Hum Genet. 2008;9:359-86 PMID: 18544035
  21. In migrating fibroblasts, recycling receptors are concentrated in narrow tubules in the pericentriolar area, and then routed to the plasma membrane of the leading lamella.
    J Cell Biol. 1994 Jun;125(6):1265-74 PMID: 7515888
  22. The cellular pathway of CD1e in immature and maturing dendritic cells.
    Traffic. 2005 Apr;6(4):286-302 PMID: 15752135
  23. Interactions between adaptor protein-1 of the clathrin coat and microtubules via type 1a microtubule-associated proteins.
    J Biol Chem. 2001 Aug 17;276(33):31340-8 PMID: 11418592
  24. Recycling endosomes.
    J Cell Sci. 2006 May 1;119(Pt 9):1679-81 PMID: 16636069
  25. Cell-specific ATP7A transport sustains copper-dependent tyrosinase activity in melanosomes.
    Nature. 2008 Aug 28;454(7208):1142-6 PMID: 18650808
  26. An AP-1/clathrin coat plays a novel and essential role in forming the Weibel-Palade bodies of endothelial cells.
    J Cell Biol. 2005 Aug 15;170(4):627-36 PMID: 16087708
  27. EpsinR: an ENTH domain-containing protein that interacts with AP-1.
    Mol Biol Cell. 2003 Feb;14(2):625-41 PMID: 12589059
  28. Chemical composition and terminology of specialized organelles (melanosomes and melanin granules) in mammalian melanocytes.
    Nature. 1963 Mar 16;197:1082-4 PMID: 13992623
  29. mu1A-adaptin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors.
    EMBO J. 2000 May 15;19(10):2193-203 PMID: 10811610
  30. Rab38 and Rab32 control post-Golgi trafficking of melanogenic enzymes.
    J Cell Biol. 2006 Oct 23;175(2):271-81 PMID: 17043139
  31. The mechanisms of vesicle budding and fusion.
    Cell. 2004 Jan 23;116(2):153-66 PMID: 14744428
  32. SNX18 is an SNX9 paralog that acts as a membrane tubulator in AP-1-positive endosomal trafficking.
    J Cell Sci. 2008 May 1;121(Pt 9):1495-505 PMID: 18411244
  33. AP-3 mediates tyrosinase but not TRP-1 trafficking in human melanocytes.
    Mol Biol Cell. 2001 Jul;12(7):2075-85 PMID: 11452004
  34. Mannose 6-phosphate receptors regulate the formation of clathrin-coated vesicles in the TGN.
    J Cell Biol. 1997 Apr 21;137(2):335-45 PMID: 9128246
  35. The Hsp90 chaperone controls the biogenesis of L7Ae RNPs through conserved machinery.
    J Cell Biol. 2008 Feb 11;180(3):579-95 PMID: 18268104
  36. New roles for endosomes: from vesicular carriers to multi-purpose platforms.
    Nat Rev Mol Cell Biol. 2009 Apr;10(4):287-92 PMID: 19277045
  37. Secretory cytotoxic granule maturation and exocytosis require the effector protein hMunc13-4.
    Nat Immunol. 2007 Mar;8(3):257-67 PMID: 17237785
  38. Rab GTPases as coordinators of vesicle traffic.
    Nat Rev Mol Cell Biol. 2009 Aug;10(8):513-25 PMID: 19603039
  39. Sorting of Pmel17 to melanosomes through the plasma membrane by AP1 and AP2: evidence for the polarized nature of melanocytes.
    J Cell Sci. 2006 Mar 15;119(Pt 6):1080-91 PMID: 16492709
  40. A lumenal domain-dependent pathway for sorting to intralumenal vesicles of multivesicular endosomes involved in organelle morphogenesis.
    Dev Cell. 2006 Mar;10(3):343-54 PMID: 16516837
  41. Focal exocytosis of VAMP3-containing vesicles at sites of phagosome formation.
    J Cell Biol. 2000 May 1;149(3):697-706 PMID: 10791982
  42. Endocytic delivery to lysosomes mediated by concurrent fusion and kissing events in living cells.
    Curr Biol. 2005 Feb 22;15(4):360-5 PMID: 15723798
  43. Localization to mature melanosomes by virtue of cytoplasmic dileucine motifs is required for human OCA2 function.
    Mol Biol Cell. 2009 Mar;20(5):1464-77 PMID: 19116314
  44. Rab11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-golgi network.
    J Cell Biol. 2000 Dec 11;151(6):1207-20 PMID: 11121436
  45. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion.
    Nature. 1998 Jul 30;394(6692):494-8 PMID: 9697774
  46. Subcompartments of the macrophage recycling endosome direct the differential secretion of IL-6 and TNFalpha.
    J Cell Biol. 2007 Jul 2;178(1):57-69 PMID: 17606866
  47. Association of the Hermansky-Pudlak syndrome type-3 protein with clathrin.
    BMC Cell Biol. 2005 Sep 13;6:33 PMID: 16159387
  48. Deconvolution microscopy.
    Adv Biochem Eng Biotechnol. 2005;95:201-43 PMID: 16080270
  49. Computer visualization of three-dimensional image data using IMOD.
    J Struct Biol. 1996 Jan-Feb;116(1):71-6 PMID: 8742726
  50. BLOC-1 interacts with BLOC-2 and the AP-3 complex to facilitate protein trafficking on endosomes.
    Mol Biol Cell. 2006 Sep;17(9):4027-38 PMID: 16837549
  51. Hermansky-Pudlak syndrome: a disease of protein trafficking and organelle function.
    Pigment Cell Res. 2006 Feb;19(1):19-42 PMID: 16420244
  52. AP-1 and AP-3 mediate sorting of melanosomal and lysosomal membrane proteins into distinct post-Golgi trafficking pathways.
    Traffic. 2008 Jul;9(7):1157-72 PMID: 18410487
  53. Dual-axis tomography: an approach with alignment methods that preserve resolution.
    J Struct Biol. 1997 Dec;120(3):343-52 PMID: 9441937
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
1540-8140
Published
2009-10-19
Pages
247-64
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2768840
Subset
IM
Grants
NEI NIH HHS · R01 EY015625 · United States
NEI NIH HHS · R01 EY015625-06A1 · United States
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com