The proteome of lysosomes

Proteomics

Volumn 10, Issue 22, 2010, Pages 4053-4076

  Schröder, Bernd A ^a   Wrocklage, Christian ^b   Hasilik, Andrej ^b   Saftig, Paul ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Cell biology; Lipofuscin; Lysosome; Organellar proteomics; SLC26A11; TMEM63A

Indexed keywords

HYDROLASE; PROTEOME;

AUTOPHAGY; CONTROLLED STUDY; ENDOCYTOSIS; EUKARYOTIC CELL; HUMAN; LYSOSOME; LYSOSOME MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PURIFICATION; PROTEOMICS; REVIEW;

ANIMALS; HUMANS; LIPOFUSCIN; LYSOSOMES; MEMBRANE PROTEINS; MICE; PROTEOME; PROTEOMICS; RATS;

EUKARYOTA;

EID: 78449312361     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201000196     Document Type: Review

References (151)

1. Bainton, D. F., The discovery of lysosomes. J. Cell. Biol. 1981, 91, 66s-76s.
2. Saftig, P., Klumperman, J., Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function. Nat. Rev. Mol. Cell Biol. 2009, 10, 623-635.
3. Dice, J. F., Chaperone-mediated autophagy. Autophagy 2007, 3, 295-299.
4. Raposo, G., Marks, M. S., Cutler, D. F., Lysosome-related organelles: driving post-Golgi compartments into specialisation. Curr. Opin. Cell Biol. 2007, 19, 394-401.
5. Hasilik, A., Wrocklage, C., Schroder, B., Intracellular trafficking of lysosomal proteins and lysosomes. Int. J. Clin. Pharmacol. Ther. 2009, 47, S18-S33.
6. Ni, X., Morales, C. R., The lysosomal trafficking of acid sphingomyelinase is mediated by sortilin and mannose 6-phosphate receptor. Traffic 2006, 7, 889-902.
7. Lefrancois, S., Zeng, J., Hassan, A. J., Canuel, M., Morales, C. R., The lysosomal trafficking of sphingolipid activator proteins (SAPs) is mediated by sortilin. EMBO J. 2003, 22, 6430-6437.
8. Reczek, D., Schwake, M., Schroder, J., Hughes, H. et al., LIMP-2 is a receptor for lysosomal mannose-6-phosphate-independent targeting of beta-glucocerebrosidase. Cell 2007, 131, 770-783.
9. Bonifacino, J. S., Traub, L. M., Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 2003, 72, 395-447.
10. Fan, X., Zhang, H., Zhang, S., Bagshaw, R. D. et al., Identification of the gene encoding the enzyme deficient in mucopolysaccharidosis IIIC (Sanfilippo disease type C). Am. J. Hum. Genet. 2006, 79, 738-744.
11. Hrebicek, M., Mrazova, L., Seyrantepe, V., Durand, S. et al., Mutations in TMEM76 Cause Mucopolysaccharidosis IIIC (Sanfilippo C Syndrome). Am. J. Hum. Genet. 2006, 79, 807-819.
12. Luzio, J. P., Pryor, P. R., Bright, N. A., Lysosomes: fusion and function. Nat. Rev. Mol. Cell Biol. 2007, 8, 622-632.
13. Vellodi, A., Lysosomal storage disorders. Br. J. Haematol. 2005, 128, 413-431.
14. Jalanko, A., Braulke, T., Neuronal ceroid lipofuscinoses. Biochim. Biophys. Acta 2009, 1793, 697-709.
15. Ruivo, R., Anne, C., Sagne, C., Gasnier, B., Molecular and cellular basis of lysosomal transmembrane protein dysfunction. Biochim. Biophys. Acta 2009, 1793, 636-649.
16. Siintola, E., Topcu, M., Aula, N., Lohi, H. et al., The novel neuronal ceroid lipofuscinosis gene MFSD8 encodes a putative lysosomal transporter. Am. J. Hum. Genet. 2007, 81, 136-146.
17. Levine, B., Kroemer, G., Autophagy in the pathogenesis of disease. Cell 2008, 132, 27-42.
18. Pan, T., Kondo, S., Le, W., Jankovic, J., The role of autophagy-lysosome pathway in neurodegeneration associated with Parkinson's disease. Brain 2008, 131, 1969-1978.
19. Ramirez, A., Heimbach, A., Grundemann, J., Stiller, B. et al., Hereditary parkinsonism with dementia is caused by mutations in ATP13A2, encoding a lysosomal type 5 P-type ATPase. Nat. Genet. 2006, 38, 1184-1191.
20. Nixon, R. A., Autophagy, amyloidogenesis and Alzheimer disease. J. Cell. Sci. 2007, 120, 4081-4091.
21. Kirkegaard, T., Jaattela, M., Lysosomal involvement in cell death and cancer. Biochim. Biophys. Acta 2009, 1793, 746-754.
22. Martinet, W., De Meyer, G. R., Autophagy in atherosclerosis. Curr. Atheroscler. Rep. 2008, 10, 216-223.
23. Graham, J. M., Isolation of lysosomes from tissues and cells by differential and density gradient centrifugation. Curr. Protoc. Cell Biol. 2001, Chapter 3, Unit.
24. Graham, J., Biological Centrifugation, Bios Scientific Publishers, Oxford, UK. 2001.
25. Graham, J. M., Ford, T., Rickwood, D., Isolation of the major subcellular organelles from mouse liver using Nycodenz gradients without the use of an ultracentrifuge. Anal. Biochem. 1990, 187, 318-323.
26. Graham, J., Ford, T., Rickwood, D., The preparation of subcellular organelles from mouse liver in self-generated gradients of iodixanol. Anal. Biochem. 1994, 220, 367-373.
27. Rome, L. H., Garvin, A. J., Allietta, M. M., Neufeld, E. F., Two species of lysosomal organelles in cultured human fibroblasts. Cell 1979, 17, 143-153.
28. Diettrich, O., Gallert, F., Hasilik, A., Purification of lysosomal membrane proteins from human placenta. Eur. J. Cell Biol. 1996, 69, 99-106.
29. Beaumelle, B. D., Gibson, A., Hopkins, C. R., Isolation and preliminary characterization of the major membrane boundaries of the endocytic pathway in lymphocytes. J. Cell Biol. 1990, 111, 1811-1823.
30. Stoorvogel, W., Geuze, H. J., Strous, G. J., Sorting of endocytosed transferrin and asialoglycoprotein occurs immediately after internalization in HepG2 cells. J. Cell Biol. 1987, 104, 1261-1268.
31. Gasingirwa, M. C., Thirion, J., Costa, C., Flamion, B. et al., A method to assess the lysosomal residence of proteins in cultured cells. Anal. Biochem. 2008, 374, 31-40.
32. Arborgh, B., Ericsson, J. L., Glaumann, H., Method for the isolation of iron-loaded lysosomes from rat liver. FEBS Lett. 1973, 32, 190-194.
33. Leighton, F., Poole, B., Beaufay, H., Baudhuin, P. et al., The large-scale separation of peroxisomes, mitochondria, and lysosomes from the livers of rats injected with triton WR-1339. Improved isolation procedures, automated analysis, biochemical and morphological properties of fractions. J. Cell Biol. 1968, 37, 482-513.
34. Schieweck, O., Damme, M., Schroder, B., Hasilik, A. et al., NCU-G1 is a highly glycosylated integral membrane protein of the lysosome. Biochem. J. 2009, 422, 83-90.
35. Goldman, R., Kaplan, A., Rupture of rat liver lysosomes mediated by L-amino acid esters. Biochim. Biophys. Acta 1973, 318, 205-216.
36. Schroder, B., Elsasser, H. P., Schmidt, B., Hasilik, A., Characterisation of lipofuscin-like lysosomal inclusion bodies from human placenta. FEBS Lett. 2007, 581, 102-108.
37. Symons, L. J., Jonas, A. J., Isolation of highly purified rat liver lysosomal membranes using two Percoll gradients. Anal. Biochem. 1987, 164, 382-390.
38. Schroder, B., Wrocklage, C., Pan, C., Jager, R. et al., Integral and associated lysosomal membrane proteins. Traffic 2007, 8, 1676-1686.
39. Terman, A., Brunk, U. T., Lipofuscin. Int. J. Biochem. Cell Biol. 2004, 36, 1400-1404.
40. Seehafer, S. S., Pearce, D. A., You say lipofuscin, we say ceroid: defining autofluorescent storage material. Neurobiol. Aging 2006, 27, 576-588.
41. Strehler, B. L., Mark, D. D., Mildvan, A. S., Gee MV: Rate and magnitude of age pigment accumulation in the human myocardium. J. Gerontol. 1959, 14, 430-439.
42. Munnell, J. F., Getty, R., Rate of accumulation of cardiac lipofuscin in the aging canine. J. Gerontol. 1968, 23, 154-158.
43. Terman, A., Gustafsson, B., Brunk, U. T., The lysosomal-mitochondrial axis theory of postmitotic aging and cell death. Chem. Biol. Interact. 2006, 163, 29-37.
44. Sitte, N., Huber, M., Grune, T., Ladhoff, A. et al., Proteasome inhibition by lipofuscin/ceroid during postmitotic aging of fibroblasts. FASEB J. 2000, 14, 1490-1498.
45. Katz, M. L., Potential role of retinal pigment epithelial lipofuscin accumulation in age-related macular degeneration. Arch. Gerontol. Geriatr. 2002, 34, 359-370.
46. Goldfischer, S., Bernstein, J., Lipofuscin (aging) pigment granules of the newborn human liver. J. Cell Biol. 1969, 42, 253-261.
47. Schutt, F., Ueberle, B., Schnolzer, M., Holz, F. G., Kopitz, J., Proteome analysis of lipofuscin in human retinal pigment epithelial cells. FEBS Lett. 2002, 528, 217-221.
48. Warburton, S., Southwick, K., Hardman, R. M., Secrest, A. M. et al., Examining the proteins of functional retinal lipofuscin using proteomic analysis as a guide for understanding its origin. Mol. Vis. 2005, 11, 1122-1134.
49. Warburton, S., Davis, W. E., Southwick, K., Xin, H. et al., Proteomic and phototoxic characterization of melanolipofuscin: correlation to disease and model for its origin. Mol. Vis. 2007, 13, 318-329.
50. Kollmann, K., Mutenda, K. E., Balleininger, M., Eckermann, E. et al., Identification of novel lysosomal matrix proteins by proteome analysis. Proteomics 2005, 5, 3966-3978.
51. Qian, M., Sleat, D. E., Zheng, H., Moore, D., Lobel, P., Proteomics analysis of serum from mutant mice reveals lysosomal proteins selectively transported by each of the two mannose 6-phosphate receptors. Mol. Cell. Proteomics. 2008, 7, 58-70.
52. Journet, A., Chapel, A., Kieffer, S., Louwagie, M. et al., Towards a human repertoire of monocytic lysosomal proteins. Electrophoresis 2000, 21, 3411-3419.
53. Journet, A., Chapel, A., Kieffer, S., Roux, F., Garin, J., Proteomic analysis of human lysosomes: application to monocytic and breast cancer cells. Proteomics 2002, 2, 1026-1040.
54. Sleat, D. E., Lackland, H., Wang, Y., Sohar, I. et al., The human brain mannose 6-phosphate glycoproteome: a complex mixture composed of multiple isoforms of many soluble lysosomal proteins. Proteomics 2005, 5, 1520-1532.
55. Sleat, D. E., Wang, Y., Sohar, I., Lackland, H. et al., Identification and validation of mannose 6-phosphate glycoproteins in human plasma reveal a wide range of lysosomal and non-lysosomal proteins. Mol. Cell. Proteomics 2006, 5, 1942-1956.
56. Sleat, D. E., Zheng, H., Qian, M., Lobel, P., Identification of sites of mannose 6-phosphorylation on lysosomal proteins. Mol. Cell. Proteomics 2006, 5, 686-701.
57. Czupalla, C., Mansukoski, H., Riedl, T., Thiel, D. et al., Proteomic analysis of lysosomal acid hydrolases secreted by osteoclasts: implications for lytic enzyme transport and bone metabolism. Mol. Cell. Proteomics 2006, 5, 134-143.
58. Sleat, D. E., Zheng, H., Lobel, P., The human urine mannose 6-phosphate glycoproteome. Biochim. Biophys. Acta 2007, 1774, 368-372.
59. Sleat, D. E., Della Valle, M. C., Zheng, H., Moore, D. F., Lobel, P., The mannose 6-phosphate glycoprotein proteome. J. Proteome Res. 2008, 7, 3010-3021.
60. Sleat, D. E., Sohar, I., Lackland, H., Majercak, J., Lobel, P., Rat brain contains high levels of mannose-6-phosphorylated glycoproteins including lysosomal enzymes and palmitoyl-protein thioesterase, an enzyme implicated in infantile neuronal lipofuscinosis. J. Biol. Chem. 1996, 271, 19191-19198.
61. Zhang, H., Fan, X., Bagshaw, R. D., Zhang, L. et al., Lysosomal membranes from beige mice contain higher than normal levels of endoplasmic reticulum proteins. J. Proteome Res. 2007, 6, 240-249.
62. Gieselmann, V., Hasilik, A., von Figura, K., Processing of human cathepsin D in lysosomes in vitro. J. Biol. Chem. 1985, 260, 3215-3220.
63. Wisselaar, H. A., Kroos, M. A., Hermans, M. M., van, B. J., Reuser, A. J., Structural and functional changes of lysosomal acid alpha-glucosidase during intracellular transport and maturation. J. Biol. Chem. 1993, 268, 2223-2231.
64. Hiraiwa, M., Martin, B. M., Kishimoto, Y., Conner, G. E. et al., Lysosomal proteolysis of prosaposin, the precursor of saposins (sphingolipid activator proteins): its mechanism and inhibition by ganglioside. Arch. Biochem. Biophys. 1997, 341, 17-24.
65. Jensen, A. G., Chemali, M., Chapel, A., Kieffer-Jaquinod, S. et al., Biochemical characterization and lysosomal localization of the mannose-6-phosphate protein p76 (hypothetical protein LOC196463). Biochem. J. 2007, 402, 449-458.
66. Deuschl, F., Kollmann, K., von Figura, K., Lubke, T., Molecular characterization of the hypothetical 66.3-kDa protein in mouse: lysosomal targeting, glycosylation, processing and tissue distribution. FEBS Lett. 2006, 580, 5747-5752.
67. Lakomek, K., Dickmanns, A., Kettwig, M., Urlaub, H. et al., Initial insight into the function of the lysosomal 66.3 kDa protein from mouse by means of X-ray crystallography. BMC Struct. Biol. 2009, 9, 56.
68. Lubke, T., Lobel, P., Sleat, D. E., Proteomics of the lysosome. Biochim. Biophys. Acta 2009, 1793, 625-635.
69. Mancini, G. M., Havelaar, A. C., Verheijen, F. W., Lysosomal transport disorders. J. Inherit. Metab. Dis. 2000, 23, 278-292.
70. Sagne, C., Gasnier, B., Molecular physiology and pathophysiology of lysosomal membrane transporters. J. Inherit. Metab. Dis. 2008.
71. Winchester, B. G., Lysosomal membrane proteins. Eur. J. Paediatr. Neurol. 2001, 5, 11-19.
72. Eskelinen, E. L., Roles of LAMP-1 and LAMP-2 in lysosome biogenesis and autophagy. Mol. Aspects Med. 2006, 27, 495-502.
73. Huynh, K. K., Eskelinen, E. L., Scott, C. C., Malevanets, A. et al., LAMP proteins are required for fusion of lysosomes with phagosomes. EMBO J. 2007, 26, 313-324.
74. Verheijen, F. W., Verbeek, E., Aula, N., Beerens, C. E. et al., A new gene, encoding an anion transporter, is mutated in sialic acid storage diseases. Nat. Genet. 1999, 23, 462-465.
75. Town, M., Jean, G., Cherqui, S., Attard, M. et al., A novel gene encoding an integral membrane protein is mutated in nephropathic cystinosis. Nat. Genet. 1998, 18, 319-324.
76. Rutsch, F., Gailus, S., Miousse, I. R., Suormala, T. et al., Identification of a putative lysosomal cobalamin exporter altered in the cblF defect of vitamin B12 metabolism. Nat. Genet. 2009, 41, 234-239.
77. International Batten Disease Consortium, Isolation of a novel gene underlying Batten disease, CLN3. The International Batten Disease Consortium. Cell 1995, 82, 949-957.
78. Santoni, V., Molloy, M., Rabilloud, T., Membrane proteins and proteomics: un amour impossible? Electrophoresis 2000, 21, 1054-1070.
79. Davies, J. P., Ioannou, Y. A., Topological analysis of Niemann-Pick C1 protein reveals that the membrane orientation of the putative sterol-sensing domain is identical to those of 3-hydroxy-3-methylglutaryl-CoA reductase and sterol regulatory element binding protein cleavage-activating protein. J. Biol Chem. 2000, 275, 24367-24374.
80. Schroder, B., Hasilik, A., A protocol for combined delipidation and subfractionation of membrane proteins using organic solvents. Anal. Biochem. 2006, 357, 144-146.
81. Bagshaw, R. D., Mahuran, D. J., Callahan, J. W., A proteomic analysis of lysosomal integral membrane proteins reveals the diverse composition of the organelle. Mol. Cell. Proteomics. 2005, 4, 133-143.
82. Liu, H., Sadygov, R. G., Yates III, J. R., A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 2004, 76, 4193-4201.
83. Old, W. M., Meyer-Arendt, K., veline-Wolf, L., Pierce, K. G. et al., Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol. Cell. Proteomics. 2005, 4, 1487-1502.
84. Bantscheff, M., Schirle, M., Sweetman, G., Rick, J., Kuster, B., Quantitative mass spectrometry in proteomics: a critical review. Anal. Bioanal. Chem. 2007, 389, 1017-1031.
85. Andersen, J. S., Wilkinson, C. J., Mayor, T., Mortensen, P. et al., Proteomic characterization of the human centrosome by protein correlation profiling. Nature 2003, 426, 570-574.
86. Foster, L. J., de Hoog, C. L., Zhang, Y., Zhang, Y. et al., A mammalian organelle map by protein correlation profiling. Cell 2006, 125, 187-199.
87. Sardiello, M., Palmieri, M., di Ronza, A., Medina, D. L. et al., A gene network regulating lysosomal biogenesis and function. Science 2009, 325, 473-477.
88. Vincourt, J. B., Jullien, D., Amalric, F., Girard, J. P., Molecular and functional characterization of SLC26A11, a sodium-independent sulfate transporter from high endothelial venules. FASEB J. 2003, 17, 890-892.
89. Jonas, A. J., Jobe, H., Sulfate transport by rat liver lysosomes. J. Biol. Chem. 1990, 265, 17545-17549.
90. Boonen, M., Hamer, I., Boussac, M., Delsaute, A. F. et al., Intracellular localization of p40, a protein identified in a preparation of lysosomal membranes. Biochem. J. 2006, 395, 39-47.
91. Schröder, B., Wrocklage, C., Hasilik, A., Saftig, P., Molecular characterisation of "Transmembrane Protein 192" (TMEM192), a novel protein of the lysosomal membrane. Biol. Chem. 2010, 391, 695-704.
92. Krishnamurthy, P. C., Du, G., Fukuda, Y., Sun, D. et al., Identification of a mammalian mitochondrial porphyrin transporter. Nature 2006, 443, 586-589.
93. Jalil, Y. A., Ritz, V., Jakimenko, A., Schmitz-Salue, C. et al., Vesicular localization of the rat ATP-binding cassette half-transporter rAbcb6. Am. J. Physiol Cell Physiol 2008, 294, C579-C590.
94. Tsuchida, M., Emi, Y., Kida, Y., Sakaguchi, M., Human ABC transporter isoform B6 (ABCB6) localizes primarily in the Golgi apparatus. Biochem. Biophys. Res. Commun. 2008, 369, 369-375.
95. Paterson, J. K., Shukla, S., Black, C. M., Tachiwada, T. et al., Human ABCB6 localizes to both the outer mitochondrial membrane and the plasma membrane. Biochemistry 2007, 46, 9443-9452.
96. Garin, J., Diez, R., Kieffer, S., Dermine, J. F. et al., The phagosome proteome: insight into phagosome functions. J. Cell. Biol. 2001, 152, 165-180.
97. Jutras, I., Houde, M., Currier, N., Boulais, J. et al., Modulation of the phagosome proteome by interferon-gamma. Mol. Cell. Proteomics. 2008, 7, 697-715.
98. Shui, W., Sheu, L., Liu, J., Smart, B. et al., Membrane proteomics of phagosomes suggests a connection to autophagy. Proc. Natl. Acad. Sci. USA 2008, 105, 16952-16957.
99. Rogers, L. D., Foster, L. J., The dynamic phagosomal proteome and the contribution of the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 2007, 104, 18520-18525.
100. Desjardins, M., ER-mediated phagocytosis: a new membrane for new functions. Nat. Rev. Immunol. 2003, 3, 280-291.
101. Touret, N., Paroutis, P., Terebiznik, M., Harrison, R. E. et al., Quantitative and dynamic assessment of the contribution of the ER to phagosome formation. Cell 2005, 123, 157-170.
102. Overbye, A., Fengsrud, M., Seglen, P. O., Proteomic analysis of membrane-associated proteins from rat liver autophagosomes. Autophagy 2007, 3, 300-322.
103. Chi, A., Valencia, J. C., Hu, Z. Z., Watabe, H. et al., Proteomic and bioinformatic characterization of the biogenesis and function of melanosomes. J. Proteome Res. 2006, 5, 3135-3144.
104. Basrur, V., Yang, F., Kushimoto, T., Higashimoto, Y. et al., Proteomic analysis of early melanosomes: identification of novel melanosomal proteins. J. Proteome Res. 2003, 2, 69-79.
105. Tribl, F., Gerlach, M., Marcus, K., Asan, E. et al., "Subcellular proteomics" of neuromelanin granules isolated from the human brain. Mol. Cell. Proteomics. 2005, 4, 945-957.
106. Casey, T. M., Meade, J. L., Hewitt, E. W., Organelle proteomics: identification of the exocytic machinery associated with the natural killer cell secretory lysosome. Mol. Cell. Proteomics. 2007, 6, 767-780.
107. Schmidt, H., Gelhaus, C., Nebendahl, M., Lettau, M. et al., 2-D DIGE analyses of enriched secretory lysosomes reveal heterogeneous profiles of functionally relevant proteins in leukemic and activated human NK cells. Proteomics 2008, 8, 2911-2925.
108. Hu, Z. Z., Valencia, J. C., Huang, H., Chi, A. et al., Comparative bioinformatics analyses and profiling of lysosome-related organelle proteomes. Int. J. Mass Spectrom. 2007, 259, 147-160.
109. Sleat, D. E., Ding, L., Wang, S., Zhao, C. et al., Mass spectrometry-based protein profiling to determine the cause of lysosomal storage diseases of unknown etiology. Mol. Cell. Proteomics. 2009.
110. Sleat, D. E., Donnelly, R. J., Lackland, H., Liu, C. G. et al., Association of mutations in a lysosomal protein with classical late-infantile neuronal ceroid lipofuscinosis. Science 1997, 277, 1802-1805.
111. Naureckiene, S., Sleat, D. E., Lackland, H., Fensom, A. et al., Identification of HE1 as the second gene of Niemann-Pick C disease. Science 2000, 290, 2298-2301.
112. Ausseil, J., Loredo-Osti, J. C., Verner, A., rmond-Zwaig, C. et al., Localisation of a gene for mucopolysaccharidosis IIIC to the pericentromeric region of chromosome 8. J. Med. Genet. 2004, 41, 941-945.
113. Brookes, P. S., Pinner, A., Ramachandran, A., Coward, L. et al., High throughput two-dimensional blue-native electrophoresis: a tool for functional proteomics of mitochondria and signaling complexes. Proteomics 2002, 2, 969-977.
114. Hinton, A., Bond, S., Forgac, M., V-ATPase functions in normal and disease processes. Pflugers Arch. 2009, 457, 589-598.
115. Lange, P. F., Wartosch, L., Jentsch, T. J., Fuhrmann, J. C., ClC-7 requires Ostm1 as a beta-subunit to support bone resorption and lysosomal function. Nature 2006, 440, 220-223.
116. Okai, T., Araki, Y., Tada, M., Tateno, T. et al., Novel small GTPase subfamily capable of associating with tubulin is required for chromosome segregation. J. Cell. Sci. 2004, 117, 4705-4715.
117. Hofmann, I., Munro, S., An N-terminally acetylated Arf-like GTPase is localised to lysosomes and affects their motility. J. Cell. Sci. 2006, 119, 1494-1503.
118. Bagshaw, R. D., Callahan, J. W., Mahuran, D. J., The Arf-family protein, Arl8b, is involved in the spatial distribution of lysosomes. Biochem. Biophys. Res. Commun. 2006, 344, 1186-1191.
119. Radons, J., Faber, V., Buhrmester, H., Volker, W. et al., Stimulation of the biosynthesis of lactosamine repeats in glycoproteins in differentiating U937 cells and its suppression in the presence of NH4Cl. Eur. J. Cell Biol. 1992, 57, 184-192.
120. Chataway, T. K., Whittle, A. M., Lewis, M. D., Bindloss, C. A. et al., Two-dimensional mapping and microsequencing of lysosomal proteins from human placenta. Placenta 1998, 19, 643-654.
121. Schroder, J., Lullmann-Rauch, R., Himmerkus, N., Pleines, I. et al., Deficiency of the tetraspanin CD63 associated with kidney pathology but normal lysosomal function. Mol. Cell Biol. 2009, 29, 1083-1094.
122. Kalatzis, V., Cherqui, S., Antignac, C., Gasnier, B., Cystinosin, the protein defective in cystinosis, is a H(+)-driven lysosomal cystine transporter. EMBO J. 2001, 20, 5940-5949.
123. Morin, P., Sagne, C., Gasnier, B., Functional characterization of wild-type and mutant human sialin. EMBO J. 2004, 23, 4560-4570.
124. Miyaji, T., Echigo, N., Hiasa, M., Senoh, S. et al., Identification of a vesicular aspartate transporter. Proc. Natl. Acad. Sci. USA 2008, 105, 11720-11724.
125. Schmidt, K., Wolfe, D. M., Stiller, B., Pearce, D. A., Cd2+, Mn2+, Ni2+and Se2+toxicity to Saccharomyces cerevisiae lacking YPK9p the orthologue of human ATP13A2. Biochem. Biophys. Res. Commun. 2009, 383, 198-202.
126. Zeevi, D. A., Frumkin, A., Bach, G., TRPML and lysosomal function. Biochim. Biophys. Acta 2007, 1772, 851-858.
127. Cheng, X., Shen, D., Samie, M., Xu, H., Mucolipins: Intracellular TRPML1-3 channels. FEBS Lett. 2010.
128. Sakata, K., Yamashita, T., Maeda, M., Moriyama, Y. et al., Cloning of a lymphatic peptide/histidine transporter. Biochem. J. 2001, 356, 53-60.
129. Schmidt, S., Joost, H. G., Schurmann, A., GLUT8, the enigmatic intracellular hexose transporter. Am. J. Physiol Endocrinol. Metab. 2009, 296, E614-E618.
130. Baldwin, S. A., Yao, S. Y., Hyde, R. J., Ng, A. M. et al., Functional characterization of novel human and mouse equilibrative nucleoside transporters (hENT3 and mENT3) located in intracellular membranes. J. Biol. Chem. 2005, 280, 15880-15887.
131. Gruenheid, S., Pinner, E., Desjardins, M., Gros, P., Natural resistance to infection with intracellular pathogens: the Nramp1 protein is recruited to the membrane of the phagosome. J. Exp. Med. 1997, 185, 717-730.
132. Tabuchi, M., Yoshimori, T., Yamaguchi, K., Yoshida, T., Kishi, F., Human NRAMP2/DMT1, which mediates iron transport across endosomal membranes, is localized to late endosomes and lysosomes in HEp-2 cells. J. Biol. Chem. 2000, 275, 22220-22228.
133. Sagne, C., Agulhon, C., Ravassard, P., Darmon, M. et al., Identification and characterization of a lysosomal transporter for small neutral amino acids. Proc. Natl. Acad. Sci. USA 2001, 98, 7206-7211.
134. Falcon-Perez, J. M., Dell'Angelica, E. C., Zinc transporter 2 (SLC30A2) can suppress the vesicular zinc defect of adaptor protein 3-depleted fibroblasts by promoting zinc accumulation in lysosomes. Exp. Cell Res. 2007, 313, 1473-1483.
135. Vulevic, B., Chen, Z., Boyd, J. T., Davis, W. Jr. et al., Cloning and characterization of human adenosine 5'-triphosphate-binding cassette, sub-family A, transporter 2 (ABCA2). Cancer Res. 2001, 61, 3339-3347.
136. Chapuy, B., Panse, M., Radunski, U., Koch, R. et al., ABC transporter A3 facilitates lysosomal sequestration of imatinib and modulates susceptibility of chronic myeloid leukemia cell lines to this drug. Haematologica 2009, 94, 1528-1536.
137. Demirel, O., Waibler, Z., Kalinke, U., Grunebach, F. et al., Identification of a lysosomal peptide transport system induced during dendritic cell development. J. Biol. Chem. 2007, 282, 37836-37843.
138. Friedmann, E., Hauben, E., Maylandt, K., Schleeger, S. et al., SPPL2a and SPPL2b promote intramembrane proteolysis of TNFalpha in activated dendritic cells to trigger IL-12 production. Nat. Cell Biol. 2006, 8, 843-848.
139. Pasternak, S. H., Bagshaw, R. D., Guiral, M., Zhang, S. et al., Presenilin-1, nicastrin, amyloid precursor protein, and gamma-secretase activity are co-localized in the lysosomal membrane. J. Biol. Chem. 2003, 278, 26687-26694.
140. Ungewickell, A., Hugge, C., Kisseleva, M., Chang, S. C. et al., The identification and characterization of two phosphatidylinositol-4, 5-bisphosphate 4-phosphatases. Proc. Natl. Acad. Sci. USA 2005, 102, 18854-18859.
141. Pryor, P. R., Mullock, B. M., Bright, N. A., Lindsay, M. R. et al., Combinatorial SNARE complexes with VAMP7 or VAMP8 define different late endocytic fusion events. EMBO Rep. 2004, 5, 590-595.
142. Jarvela, I., Sainio, M., Rantamaki, T., Olkkonen, V. M. et al., Biosynthesis and intracellular targeting of the CLN3 protein defective in Batten disease. Hum. Mol. Genet. 1998, 7, 85-90.
143. Ioannou, Y. A., The structure and function of the Niemann-Pick C1 protein. Mol. Genet. Metab. 2000, 71, 175-181.
144. Zhang, D. L., Su, D., Berczi, A., Vargas, A., Asard, H., An ascorbate-reducible cytochrome b561 is localized in macrophage lysosomes. Biochim. Biophys. Acta 2006, 1760, 1903-1913.
145. Wang, L., Yu, C., Lu, Y., He, P. et al., TMEM166, a novel transmembrane protein, regulates cell autophagy and apoptosis. Apoptosis 2007, 12, 1489-1502.
146. Yu, C., Wang, L., Lv, B., Lu, Y. et al., TMEM74, a lysosome and autophagosome protein, regulates autophagy. Biochem. Biophys. Res. Commun. 2008, 369, 622-629.
147. Ihrke, G., Gray, S. R., Luzio, J. P., Endolyn is a mucin-like type I membrane protein targeted to lysosomes by its cytoplasmic tail. Biochem. J. 2000, 345, 287-296.
148. Hogue, D. L., Nash, C., Ling, V., Hobman, T. C., Lysosome-associated protein transmembrane 4 alpha (LAPTM4 alpha) requires two tandemly arranged tyrosine-based signals for sorting to lysosomes. Biochem. J. 2002, 365, 721-730.
149. Cabrita, M. A., Hobman, T. C., Hogue, D. L., King, K. M., Cass, C. E., Mouse transporter protein, a membrane protein that regulates cellular multidrug resistance, is localized to lysosomes. Cancer Res. 1999, 59, 4890-4897.
150. Pak, Y., Glowacka, W. K., Bruce, M. C., Pham, N., Rotin, D., Transport of LAPTM5 to lysosomes requires association with the ubiquitin ligase Nedd4, but not LAPTM5 ubiquitination. J. Cell. Biol. 2006, 175, 631-645.
151. He, P., Peng, Z., Luo, Y., Wang, L. et al., High-throughput functional screening for autophagy-related genes and identification of TM9SF1 as an autophagosome-inducing gene. Autophagy 2009, 5, 52-60.