The building BLOC(k)s of lysosomes and related organelles

Current Opinion in Cell Biology

Volumn 16, Issue 4, 2004, Pages 458-464

  Dell'Angelica, Esteban C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

adaptor protein; AP; biogenesis of lysosome related organelles complex; BLOC; BLOC subunit; BLOS; DGC; dystrophin glycoprotein complex; F actin; filamentous actin; Hermansky Pudlak Syndrome; homotypic vacuolar protein sorting; HOPS; HPS; LAMP

Indexed keywords

GENE PRODUCT; PROTEIN SUBUNIT;

BIOGENESIS; CELL ORGANELLE; CELL STRUCTURE; CELLULAR DISTRIBUTION; GENE EXPRESSION; GENE MUTATION; HUMAN; LYSOSOME; MEMBRANE FUSION; MOLECULAR MECHANICS; NONHUMAN; OCULAR ALBINISM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW;

ANIMALS; CARRIER PROTEINS; HERMANSKI-PUDLAK SYNDROME; HUMANS; LYSOSOMES; MELANOSOMES; ORGANELLES;

EUKARYOTA; PROTISTA;

EID: 3142516226     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2004.05.001     Document Type: Review

References (50)

1. Dell'Angelica E.C., Mullins C., Caplan S., Bonifacino J.S. Lysosome-related organelles. FASEB J. 14:2000;1265-1278
2. Luzio J.P., Poupon V., Lindsay R., Mullock B.M., Piper R.C., Pryor P.R. Membrane dynamics and the biogenesis of lysosomes. Mol Membr Biol. 20:2003;141-154
3. Mullins C., Bonifacino J.S. The molecular machinery for lysosome biogenesis. Bioessays. 23:2001;333-343
4. Huizing M., Boissy R.E., Gahl W.A. Hermansky-Pudlak syndrome: vesicle formation from yeast to man. Pigment Cell Res. 15:2002;405-419
5. Suzuki T., Oiso N., Gautam R., Novak E.K., Panthier J.-J., Suprabha P.G., Vida T., Swank R.T., Spritz R.A. The mouse organellar biogenesis mutant buff results from a mutation in Vps33a, a homologue of yeast vps33 and Drosophila carnation. Proc Natl Acad Sci USA. 100:2003;1146-1150 The gene encoding mouse Vps33a is identified by positional cloning as the target of the buff mutation, which causes hypopigmentation as a result of abnormal melanosome number and size and defective platelet aggregation caused by platelet-dense granule deficiency.
6. Peterson M.R., Emr S.D. The Class C Vps complex functions at multiple stages of the vacuolar transport pathway. Traffic. 2:2001;476-486
7. Sriram V., Krishnan K.S., Mayor S. deep-orange and carnation define distinct stages in late endosomal biogenesis in Drosophila melanogaster. J Cell Biol. 161:2003;593-607
8. Richardson S.C.W., Winistorfer S.C., Poupon V., Luzio J.P., Piper R.C. Mammalian late Vps orthologues participate in early endosomal fusion and interact with the cytoskeleton. Mol Biol Cell. 15:2004;1197-1210
9. Falcón-Pérez J.M., Starcevic M.S., Gautam R., Dell'Angelica E.C. BLOC-1, a novel complex containing the pallidin and muted proteins involved in the biogenesis of melanosomes and platelet-dense granules. J Biol Chem. 277:2002;28191-28199
10. Moriyama K., Bonifacino J.S. Pallidin is a component of a multi-protein complex involved in the biogenesis of lysosome-related organelles. Traffic. 3:2002;666-677
11. Huang L., Kuo Y.-M., Gitschier J. The pallid gene encodes a novel, syntaxin 13-interacting protein involved in platelet storage pool deficiency. Nat Genet. 23:1999;329-332
12. Zhang Q., Li W., Novak E.K., Karim A., Mishra V.S., Kingsmore S.F., Roe B.A., Suzuki T., Swank R.T. The gene for the muted (mu) mouse, a model for Hermansky-Pudlak syndrome, defines a novel protein which regulates vesicle trafficking. Hum Mol Genet. 11:2002;697-706
13. Ciciotte S.L., Gwynn B., Moriyama K., Huizing M., Gahl W.A., Bonifacino J.S., Peters L.L. Cappuccino, a mouse model of Hermansky-Pudlak syndrome, encodes a novel protein that is part of the pallidin-muted complex (BLOC-1). Blood. 101:2003;4402-4407
14. Benson M.A., Newey S.E., Martin-Rendon E., Hawkes R., Blake D.J. Dysbindin, a novel coiled-coil-containing protein that interacts with the dystrobrevins in muscle and brain. J Biol Chem. 276:2001;24232-24241
15. Li W., Zhang Q., Oiso N., Novak E.K., Gautam R., O'Brien E.P., Tinsley C.L., Blake D.J., Spritz R.A., Copeland N.G., et al. Hermansky-Pudlak syndrome type 7 (HPS-7) results from mutant dysbindin, a member of the biogenesis of lysosome-related organelles complex 1 (BLOC-1). Nat Genet. 35:2003;84-89 This paper reports that dysbindin is mutated in the sandy mouse model of HPS and in one HPS patient. The study demonstrates that dysbindin is a stable component of BLOC-1 and interacts directly with the pallidin subunit of the complex. The study also shows that the mutant dysbindin protein encoded by the sandy allele fails to interact with β-dystrobrevin under conditions in which the previously published interaction between dysbindin and β-dystrobrevin [14] is reproduced.
16. Starcevic M, Dell'Angelica EC: Identification of snapin and three novel proteins (BLOS1, BLOS2 and BLOS3/reduced pigmentation) as subunits of biogenesis of lysosome-related organelles complex-1 (BLOC-1). J Biol Chem 2004, in press.
17. Zhang Q., Zhao B., Li W., Oiso N., Novak E.K., Rusiniak M.E., Gautam R., Chintala S., O'Brien E.P., Zhang Y., et al. Ru2 and Ru encode mouse orthologs of the genes mutated in human Hermansky-Pudlak syndrome types 5 and 6. Nat Genet. 33:2003;145-153 This paper reports identification of the HPS5 and HPS6 proteins by positional cloning of the genes mutated in the murine strains ruby eye 2 and ruby eye, respectively, as well as the identification of mutations in the human HPS5 and HPS6 genes in patients suffering from HPS. In addition, the study reports that the HPS5 and HPS6 proteins interact directly, and describes the presence of aberrant 'multi-melanosomal bodies' in the choroid of ruby eye and ruby eye 2 mice.
18. Di Pietro S.M., Falcón-Pérez J.M., Dell'Angelica E.C. Characterization of BLOC-2, a complex containing the Hermansky-Pudlak syndrome proteins HPS3, HPS5 and HPS6. Traffic. 5:2004;276-283
19. Gautam R., Chintala S., Li W., Zhang Q., Tan J., Novak E.K., Di Pietro S.M., Dell'Angelica E.C., Swank R.T. The Hermansky-Pudlak syndrome 3 (cocoa) protein is a component of the biogenesis of lysosome-related organelles complex-2 (BLOC-2). J Biol Chem. 279:2004;12935-12942
20. Oh J., Liu Z.-X., Feng C.H., Raposo G., Spritz R.A. The Hermansky-Pudlak syndrome (HPS) protein is part of a high-molecular-weight complex involved in biogenesis of early melanosomes. Hum Mol Genet. 9:2000;375-385
21. Chiang P.-W., Oiso N., Gautam R., Suzuki T., Swank R.T., Spritz R.A. The Hermansky-Pudlak syndrome 1 (HPS1) and HPS4 proteins are components of two complexes, BLOC-3 and BLOC-4, involved in the biogenesis of lysosome-related organelles. J Biol Chem. 278:2003;20332-20337
22. Martina J.A., Moriyama K., Bonifacino J.S. BLOC-3, a protein complex containing the Hermansky-Pudlak syndrome gene products HPS1 and HPS4. J Biol Chem. 278:2003;29376-29384
23. Nazarian R., Falcón-Pérez J.M., Dell'Angelica E.C. Biogenesis of lysosome-related organelles complex 3 (BLOC-3): a complex containing the Hermansky-Pudlak syndrome (HPS) proteins HPS1 and HPS4. Proc Natl Acad Sci USA. 100:2003;8770-8775 This paper, together with another two [21, 22], demonstrates that HPS1 and HPS4 are associated into a stable complex (BLOC-3). The paper also reports that lysosomes and late endosomes are less concentrated in the perinuclear region of BLOC-3-deficient fibroblasts than in control fibroblasts, and that a deficiency in BLOC-3 does not enhance or suppress the coat color phenotype of BLOC-1-deficient mice.
24. Jahn R., Lang T., Südhof T.C. Membrane fusion. Cell. 112:2003;519-533
25. Prekeris R., Klumperman J., Chen Y.A., Scheller R.H. Syntaxin 13 mediates cycling of plasma membrane proteins via tubulovesicular recycling endosomes. J Cell Biol. 143:1998;957-971
26. McBride H.M., Rybin V., Murphy C., Giner A., Teasdale R., Zerial M. Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and Syntaxin 13. Cell. 98:1999;377-386
27. Sun W., Yan Q., Vida T.A., Bean A.J. Hrs regulates early endosome fusion by inhibiting formation of an endosomal SNARE complex. J Cell Biol. 162:2003;125-137
28. Taunton J., Rowning B.A., Coughlin M.L., Wu M., Moon R.T., Mitchison T.J., Larabell C.A. Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP. J Cell Biol. 148:2000;519-530
29. Cordonnier M.-N., Dauzonne D., Louvard D., Coudrier E. Actin filaments and myosin Iα cooperate with microtubules for the movement of lysosomes. Mol Biol Cell. 12:2001;4013-4029
30. van Deurs B., Holm P.K., Kayser L., Sandvig K. Delivery to lysosomes in the human carcinoma cell line HEp-2 involves an actin filament-facilitated fusion between mature endosomes and preexisting lysosomes. Eur J Cell Biol. 66:1995;309-323
31. Eitzen G., Wang L., Thorngren N., Wickner W. Remodeling of organelle-bound actin is required for yeast vacuole fusion. J Cell Biol. 158:2002;669-679
32. Drengk A., Fritsch J., Schmauch C., Rühling H., Maniak M. A coat of filamentous actin prevents clustering of late-endosomal vacuoles in vivo. Curr Biol. 13:2003;1814-1819
33. Kjeken R., Egeberg M., Habermann A., Kuehnel M., Peyron P., Floetenmeyer M., Walther P., Jahraus A., Defacque H., Kuznetsov S.A., Griffiths G. Fusion between phagosomes, early and late endosomes: a role for actin in fusion between late, but not early endocytic organelles. Mol Biol Cell. 15:2004;345-358 This paper reports that late, but not early, endosomes nucleate actin, and that perturbations in actin polymerization affected homotypic fusion of late endosomes, but not of early endosomes, as evidenced by in vitro fusion assays.
34. Durbeej M., Campbell K.P. Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models. Curr Opin Genet Dev. 12:2002;349-361
35. Blake D.J., Weir A., Newey S.E., Davies K.E. Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev. 82:2002;291-329
36. Loh N.Y., Nebenius-Oosthuizen D., Blake D.J., Smith A.J.H., Davies K.E. Role of β-dystrobrevin in nonmuscle dystrophin-associated-protein-complex- like complexes in kidney and liver. Mol Cell Biol. 21:2001;7442-7448
37. Grady R.M., Grange R.W., Lau K.S., Maimone M.M., Nichol M.C., Stull J.T., Sanes J.R. Role for α-dystrobrevin in the pathogenesis of dystrophin-dependent muscular dystrophies. Nat Cell Biol. 1:1999;215-220
38. Benson M.A., Tinsley C.L., Blake D.J. Myospryn is a novel binding partner for dysbindin in muscle. J Biol Chem. 279:2004;10450-10458
39. Wixler V., Laplantine E., Geerts D., Sonnenberg A., Petersohn D., Eckes B., Paulsson M., Aumailley M. Identification of novel interaction partners for the conserved membrane proximal region of α-integrin cytoplasmic domains. FEBS Lett. 445:1999;351-355
40. Theriault L.L., Hurley L.S. Ultrastructure of developing melanosomes in C57 black and pallid mice. Dev Biol. 23:1970;261-275
41. Nguyen T., Novak E.K., Kermani M., Fluhr J., Peters L.L., Swank R.T., Wei M.L. Melanosome morphologies in murine models of Hermansky-Pudlak syndrome reflect blocks in organelle development. J Invest Dermatol. 119:2002;1156-1164
42. Boissy R.E., Zhao Y., Gahl W.A. Altered protein localization in melanocytes from Hermansky-Pudlak syndrome: support for the role of the HPS gene product in intracellular trafficking. Lab Invest. 78:1998;1037-1048
43. Gardner J.M., Wildenberg S.C., Keiper N.M., Novak E.K., Rusiniak M.E., Swank R.T., Puri N., Finger J.N., Hagiwara N., Lehman A.L., et al. The mouse pale ear (ep) mutation is the homologue of human Hermansky-Pudlak syndrome. Proc Natl Acad Sci USA. 94:1997;9238-9243
44. Suzuki T., Li W., Zhang Q., Karim A., Novak E.K., Sviderskaya E.V., Hill S.P., Bennett D.C., Levin A.V., Nieuwenhuis H.K., et al. Hermansky-Pudlak syndrome is caused by mutations in HPS4, the human homolog of the mouse light-ear gene. Nat Genet. 30:2002;321-324
45. Feng L., Novak E.K., Hartnell L.M., Bonifacino J.S., Collinson L.M., Swank R.T. The Hermansky-Pudlak syndrome 1 (HPS1) and HPS2 genes independently contribute to the production and function of platelet dense granules, melanosomes and lysosomes. Blood. 99:2002;1651-1658
46. Swank R.T., Novak E.K., McGarry M.P., Rusiniak M.E., Feng L. Mouse models of Hermansky-Pudlak syndrome: a review. Pigment Cell Res. 11:1998;60-80
47. Harada A., Takei Y., Kanai Y., Tanaka Y., Nonaka S., Hirokawa N. Golgi vesiculation and lysosome dispersion in cells lacking cytoplasmic dynein. J Cell Biol. 141:1998;51-59
48. Cantalupo G., Alifano P., Roberti V., Bruni C.B., Bucci C. Rab-interacting lysosomal protein (RILP): the Rab7 effector required for transport to lysosomes. EMBO J. 20:2001;683-693
49. Jordens I., Fernandez-Borja M., Marsman M., Dusseljee S., Janssen L., Calafat J., Janssen H., Wubbolts R., Neefjes J. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr Biol. 11:2001;1680-1685
50. Clark R.H., Stinchcombe J.C., Day A., Blott E., Booth S., Bossi G., Hamblin T., Davies E.G., Griffiths G.M. Adaptor protein 3-dependent microtubule-mediated movement of lytic granules to the immunological synapse. Nat Immunol. 4:2003;1111-1120