Classification of subcellular location by comparative proteomic analysis of native and density-shifted lysosomes

Molecular and Cellular Proteomics

Volumn 10, Issue 4, 2011, Pages

  Della Valle, Maria Cecilia ^a,b   Sleat, David E ^a,b   Zheng, Haiyan ^a   Moore, Dirk F ^c   Jadot, Michel ^d   Lobel, Peter ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

^d UNIVERSITY OF NAMUR   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; COPPER ZINC SUPEROXIDE DISMUTASE; SUCROSE; TYLOXAPOL; ABCB6 PROTEIN, RAT; BIOLOGICAL MARKER; PROTEOME; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; FUNCTIONAL PROTEOMICS; LIQUID CHROMATOGRAPHY; LIVER LYSOSOME; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; WESTERN BLOTTING; ANIMAL; CELL ORGANELLE; DISCRIMINANT ANALYSIS; ENZYME ASSAY; LIVER; LYSOSOME; MALE; METABOLISM; RAT; RELATIVE DENSITY; TANDEM MASS SPECTROMETRY; WISTAR RAT;

ANIMALIA; RATTUS;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL MARKERS; DISCRIMINANT ANALYSIS; ENZYME ASSAYS; LIVER; LYSOSOMES; MALE; ORGANELLES; PROTEOME; RATS; RATS, WISTAR; SPECIFIC GRAVITY; SUBCELLULAR FRACTIONS; SUPEROXIDE DISMUTASE; TANDEM MASS SPECTROMETRY;

EID: 79953318188     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M110.006403     Document Type: Article

References (65)

1. Lübke, T., Lobel, P., and Sleat, D. E. (2009) Proteomics of the lysosome. Biochim. Biophys. Acta 1793, 625-635
2. Journet, A., and Ferro, M. (2004) The potentials of MS-based subproteomic approaches in medical science: the case of lysosomes and breast cancer. Mass Spectrom. Rev. 23, 393-442
3. Lee, J. H., Yu, W. H., Kumar, A., Lee, S., Mohan, P. S., Peterhoff, C. M., Wolfe, D. M., Martinez-Vicente, M., Massey, A. C., Sovak, G., Uchiyama, Y., Westaway, D., Cuervo, A. M., and Nixon, R. A. (2010) Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 141, 1146-1158
4. Sidransky, E., Nalls, M. A., Aasly, J. O., Aharon-Peretz, J., Annesi, G., Barbosa, E. R., Bar-Shira, A., Berg, D., Bras, J., Brice, A., Chen, C. M., Clark, L. N., Condroyer, C., De, Marco, E. V., Dürr, A., Eblan, M. J., Fahn, S., Farrer, M. J., Fung, H. C., Gan-Or, Z., Gasser, T., Gershoni- Baruch, R., Giladi, N., Griffith, A., Gurevich, T., Januario, C., Kropp, P., Lang, A. E., Lee-Chen, G. J., Lesage, S., Marder, K., Mata, I. F., Mirelman, A., Mitsui, J., Mizuta, I., Nicoletti, G., Oliveira, C., Ottman, R., Orr-Urtreger, A., Pereira, L. V., Quattrone, A., Rogaeva, E., Rolfs, A., Rosenbaum, H., Rozenberg, R., Samii, A., Samaddar, T., Schulte, C., Sharma, M., Singleton, A., Spitz, M., Tan, E. K., Tayebi, N., Toda, T., Troiano, A. R., Tsuji, S., Wittstock, M., Wolfsberg, T. G., Wu, Y. R., Zabetian, C. P., Zhao, Y., and Ziegler, S. G. (2009) Multicenter analysis of glucocerebrosidase mutations in Parkinson's disease. N. Engl. J. Med. 361, 1651-1661
5. Sun, B., Zhou, Y., Halabisky, B., Lo, I., Cho, S. H., Mueller-Steiner, S., Devidze, N., Wang, X., Grubb, A., and Gan, L. (2008) Cystatin C-cathepsin B axis regulates amyloid beta levels and associated neuronal deficits in an animal model of Alzheimer's disease. Neuron 60, 247-257
6. Callahan, J. W., Bagshaw, R. D., and Mahuran, D. J. (2009) The integral membrane of lysosomes: its proteins and their roles in disease. J. Proteomics 72, 23-33
7. Sleat, D. E., Jadot, M., and Lobel, P. (2007) Lysosomal proteomics and disease. Proteomics - Clinical Applications 1, 1134-1146
8. Schröder, B. A., Wrocklage, C., Hasilik, A., and Saftig, P. (2010) The proteome of lysosomes. Proteomics 10, 4053-4076
9. de Duve, C. (1971) Tissue fractionation. Past and present. J. Cell Biol. 50, 20d-55d
10. de Duve, C., Pressman, B. C., Gianetto, R., Wattiaux, R., and Appelmans, F. (1955) Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue. Biochem. J. 60, 604-617
11. Wattiaux, R., Wibo, M., and Baudhuin, P. (1963) Influence of the injection of Triton WR-1339 on the properties of rat-liver lysosomes. In: de Reuck, A. V. S., and Cameron, M. P., eds. Ciba Foundation Symposium Lysosomes, pp. 176-200, Little, Brown, and Company, Boston
12. Sohar, I., Sleat, D. E., Jadot, M., and Lobel, P. (1999) Biochemical characterization of a lysosomal protease deficient in classical late infantile neuronal ceroid lipofuscinosis (LINCL) and development of an enzyme-based assay for diagnosis and exclusion of LINCL in human specimens and animal models. J. Neurochem. 73, 700-711 (Pubitemid 29339844)
13. Naureckiene, S., Sleat, D. E., Lackland, H., Fensom, A., Vanier, M. T., Wattiaux, R., Jadot, M., and Lobel, P. (2000) Identification of HE1 as the Second Gene of Niemann-Pick C Disease. Science 290, 2298-2301 (Pubitemid 32041569)
14. Boonen, M., Hamer, I., Boussac, M., Delsaute, A. F., Flamion, B., Garin, J., and Jadot, M. (2006) Intracellular localization of p40, a protein identified in a preparation of lysosomal membranes. Biochem. J. 395, 39-47
15. Deuschl, F., Kollmann, K., von, Figura, K., and Lübke, T. (2006) Molecular characterization of the hypothetical 66.3-kDa protein in mouse: lysosomal targeting, glycosylation, processing and tissue distribution. FEBS Lett. 580, 5747-5752 (Pubitemid 44498673)
16. Schieweck, O., Damme, M., Schröder, B., Hasilik, A., Schmidt, B., and Lübke, T. (2009) NCU-G1 is a highly glycosylated integral membrane protein of the lysosome. Biochem. J. 422, 83-90
17. Jensen, A. G., Chemali, M., Chapel, A., Kieffer-Jaquinod, S., Jadot, M., Garin, J., and Journet, A. (2007) Biochemical characterization and lysosomal localization of the mannose-6-phosphate protein p76 (hypothetical protein LOC196463). Biochem. J. 402, 449-458 (Pubitemid 46423882)
18. Leighton, F., Poole, B., Beaufay, H., Baudhuin, P., Coffey, J. W., Fowler, S., and de Duve, C. (1968) 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. 37, 482-513
19. Beaufay, H., Jacques, P., Baudhuin, P., Sellinger, O. Z., Berthet, J., and de Duve, C. (1964) Tissue fractionation studies. 18. Resolution of mitochondrial fractions from rat liver into three distinct populations of cytoplasmic particles by means of density equilibration in various gradients. Biochem. J. 92, 184-205
20. Sleat, D. E., Sohar, I., Lackland, H., Majercak, J., and Lobel, P. (1996) 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. 271, 19191-19198
21. Storrie, B., and Madden, E. A. (1990) Isolation of subcellular organelles. Methods Enzymol. 182, 203-225
22. Aebi, H. (1984) Catalase in vitro. Methods Enzymol. 105, 121-126
23. Sleat, D. E., Della Valle, M. C., Zheng, H., Moore, D. F., and Lobel, P. (2008) The Mannose 6-Phosphate Glycoprotein Proteome. J. Proteome Res. 7, 3010-3021
24. Choe, L., D'Ascenzo, M., Relkin, N. R., Pappin, D., Ross, P., Williamson, B., Guertin, S., Pribil, P., and Lee, K. H. (2007) 8-plex quantitation of changes in cerebrospinal fluid protein expression in subjects undergoing intravenous immunoglobulin treatment for Alzheimer's disease. Proteomics 7, 3651-3660
25. Craig, R., and Beavis, R. C. (2004) TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20, 1466-1467
26. Venables, W. N., and Ripley, B. D. (2002) Modern Applied Statistics with S, 4 Ed., Springer, New York
27. Bagshaw, R. D., Mahuran, D. J., and Callahan, J. W. (2005) A proteomic analysis of lysosomal integral membrane proteins reveals the diverse composition of the organelle. Mol. Cell Proteomics 4, 133-143
28. Schröder, B., Wrocklage, C., Pan, C., Jäger, R., Kösters, B., Schäfer, H., Elsässer, H. P., Mann, M., and Hasilik, A. (2007) Integral and associated lysosomal membrane proteins. Traffic 8, 1676-1686 (Pubitemid 350066680)
29. Pagliarini, D. J., Calvo, S. E., Chang, B., Sheth, S. A., Vafai, S. B., Ong, S. E., Walford, G. A., Sugiana, C., Boneh, A., Chen, W. K., Hill, D. E., Vidal, M., Evans, J. G., Thorburn, D. R., Carr, S. A., and Mootha, V. K. (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell 134, 112-123
30. Schlüter, A., Real-Chicharro, A., Gabaldón, T., Sánchez-Jiménez, F., and Pujol, A. (2010) PeroxisomeDB 2.0: an integrative view of the global peroxisomal metabolome. Nucleic Acids Res. 38, D800-805
31. Chataway, T. K., Whittle, A. M., Lewis, M. D., Bindloss, C. A., Davey, R. C., Moritz, R. L., Simpson, R. J., Hopwood, J. J., and Meikle, P. J. (1998) Two-dimensional mapping and microsequencing of lysosomal proteins from human placenta. Placenta 19, 643-654 (Pubitemid 28531936)
32. Chi, A., Valencia, J. C., Hu, Z. Z., Watabe, H., Yamaguchi, H., Mangini, N. J., Huang, H., Canfield, V. A., Cheng, K. C., Yang, F., Abe, R., Yamagishi, S., Shabanowitz, J., Hearing, V. J., Wu, C., Appella, E., and Hunt, D. F. (2006) Proteomic and bioinformatic characterization of the biogenesis and function of melanosomes. J. Proteome Res. 5, 3135-3144
33. Casey, T. M., Meade, J. L., and Hewitt, E. W. (2007) Organelle proteomics: identification of the exocytic machinery associated with the natural killer cell secretory lysosome. Mol. Cell Proteomics 6, 767-780
34. Tribl, F., Gerlach, M., Marcus, K., Asan, E., Tatschner, T., Arzberger, T., Meyer, H. E., Bringmann, G., and Riederer, P. (2005) "Subcellular proteomics" of neuromelanin granules isolated from the human brain. Mol. Cell Proteomics 4, 945-957
35. Ow, S. Y., Salim, M., Noirel, J., Evans, C., Rehman, I., and Wright, P. C. (2009) iTRAQ underestimation in simple and complex mixtures: "the good, the bad and the ugly". J. Proteome Res. 8, 5347-5355
36. Sleat, D. E., Zheng, H., Qian, M., and Lobel, P. (2006) Identification of sites of mannose 6-phosphorylation on lysosomal proteins. Mol. Cell Proteomics 5, 686-701
37. Okado-Matsumoto, A., and Fridovich, I. (2001) Subcellular Distribution of Superoxide Dismutases (SOD) in Rat Liver. Cu, Zn-SOD in mitochondria. J. Biol. Chem. 276, 38388-38393
38. Kawamata, H., and Manfredi, G. (2008) Different regulation of wild-type and mutant Cu, Zn superoxide dismutase localization in mammalian mitochondria. Hum. Mol. Genet. 17, 3303-3317
39. Islinger, M., Li, K. W., Seitz, J., Völkl, A., and Lüers, G. H. (2009) Hitchhiking of Cu/Zn superoxide dismutase to peroxisomes-evidence for a natural piggyback import mechanism in mammals. Traffic 10, 1711-1721
40. Geller, B. L., and Winge, D. R. (1982) Rat liver Cu, Zn-superoxide dismutase. Subcellular location in lysosomes. J. Biol. Chem. 257, 8945-8952
41. Rabouille, C., Strous, G. J., Crapo, J. D., Geuze, H. J., and Slot, J. W. (1993) The differential degradation of two cytosolic proteins as a tool to monitor autophagy in hepatocytes by immunocytochemistry. J. Cell Biol. 120, 897-908
42. Ellerby, L. M., Cabelli, D. E., Graden, J. A., and Valentine, J. S. (1996) Copper-zinc superoxide dismutase: Why not pH-dependent? J. Am. Chem. Soc. 118, 6556-6561
43. Harata, T., Ando, H., Iwase, A., Nagasaka, T., Mizutani, S., and Kikkawa, F. (2006) Localization of angiotensin II, the AT1 receptor, angiotensin-converting enzyme, aminopeptidase A, adipocyte-derived leucine aminopeptidase, and vascular endothelial growth factor in the human ovary throughout the menstrual cycle. Fertil. Steril. 86, 433-439
44. Toei, M., Saum, R., and Forgac, M. (2010) Regulation and isoform function of the V-ATPases. Biochemistry 49, 4715-4723
45. Okai, T., Araki, Y., Tada, M., Tateno, T., Kontani, K., and Katada, T. (2004) Novel small GTPase subfamily capable of associating with tubulin is required for chromosome segregation. J. Cell Sci. 117, 4705-4715 (Pubitemid 39433437)
46. Bagshaw, R. D., Callahan, J. W., and Mahuran, D. J. (2006) The Arf-family protein, Arl8b, is involved in the spatial distribution of lysosomes. Biochem. Biophys. Res. Commun. 344, 1186-1191
47. Hofmann, I., and Munro, S. (2006) An N-terminally acetylated Arf-like GTPase is localised to lysosomes and affects their motility. J. Cell Sci. 119, 1494-1503 (Pubitemid 43732978)
48. Kolstoe, S. E., Ridha, B. H., Bellotti, V., Wang, N., Robinson, C. V., Crutch, S. J., Keir, G., Kukkastenvehmas, R., Gallimore, J. R., Hutchinson, W. L., Hawkins, P. N., Wood, S. P., Rossor, M. N., and Pepys, M. B. (2009) Molecular dissection of Alzheimer's disease neuropathology by depletion of serum amyloid P component. Proc. Natl. Acad. Sci. U.S.A. 106, 7619-7623
49. Tennent, G. A., Lovat, L. B., and Pepys, M. B. (1995) Serum amyloid P component prevents proteolysis of the amyloid fibrils of Alzheimer disease and systemic amyloidosis. Proc. Natl. Acad. Sci. U.S.A. 92, 4299-4303
50. Sleat, D. E., Wang, Y., Sohar, I., Lackland, H., Li, Y., Li, H., Zheng, H., and Lobel, P. (2006) Identification and Validation of Mannose 6-Phosphate Glycoproteins in Human Plasma Reveal a Wide Range of Lysosomal and Non-lysosomal Proteins. Mol. Cell Proteomics 5, 1942-1956 (Pubitemid 44688202)
51. Qian, M., Sleat, D. E., Zheng, H., Moore, D., and Lobel, P. (2008) Proteomics Analysis of Serum from Mutant Mice Reveals Lysosomal Proteins Selectively Transported by Each of the Two Mannose 6-Phosphate Receptors. Mol. Cell Proteomics 7, 58-70 (Pubitemid 351248234)
52. Loveless, R. W., Floyd-O'Sullivan, G., Raynes, J. G., Yuen, C. T., and Feizi, T. (1992) Human serum amyloid P is a multispecific adhesive protein whose ligands include 6-phosphorylated mannose and the 3-sulphated saccharides galactose, N-acetylgalactosamine and glucuronic acid. EMBO J. 11, 813-819
53. Vargas, J. D., Herpers, B., McKie, A. T., Gledhill, S., McDonnell, J., van den Heuvel, M., Davies, K. E., and Ponting, C. P. (2003) Stromal cell-derived receptor 2 and cytochrome b561 are functional ferric reductases. Biochim. Biophys. Acta 1651, 116-123
54. Zhang, D. L., Su, D., Bérczi, A., Vargas, A., and Asard, H. (2006) An ascorbate-reducible cytochrome b561 is localized in macrophage lysosomes. Biochim. Biophys. Acta 1760, 1903-1913
55. Holland, K. A., and Holland, I. B. (2005) Adventures with ABC-proteins: highly conserved ATP-dependent transporters. Acta Microbiol. Immunol. Hung. 52, 309-322
56. Mitsuhashi, N., Miki, T., Senbongi, H., Yokoi, N., Yano, H., Miyazaki, M., Nakajima, N., Iwanaga, T., Yokoyama, Y., Shibata, T., and Seino, S. (2000) MTABC3, a novel mitochondrial ATP-binding cassette protein involved in iron homeostasis. J. Biol. Chem. 275, 17536-17540
57. Krishnamurthy, P. C., Du, G., Fukuda, Y., Sun, D., Sampath, J., Mercer, K. E., Wang, J., Sosa-Pineda, B., Murti, K. G., and Schuetz, J. D. (2006) Identification of a mammalian mitochondrial porphyrin transporter. Nature 443, 586-589
58. Paterson, J. K., Shukla, S., Black, C. M., Tachiwada, T., Garfield, S., Wincovitch, S., Ernst, D. N., Agadir, A., Li, X., Ambudkar, S. V., Szakacs, G., Akiyama, S., and Gottesman, M. M. (2007) Human ABCB6 localizes to both the outer mitochondrial membrane and the plasma membrane. Biochemistry 46, 9443-9452
59. Tsuchida, M., Emi, Y., Kida, Y., and Sakaguchi, M. (2008) Human ABC transporter isoform B6 (ABCB6) localizes primarily in the Golgi apparatus. Biochem. Biophys. Res. Commun. 369, 369-375
60. Jalil, Y. A., Ritz, V., Jakimenko, A., Schmitz-Salue, C., Siebert, H., Awuah, D., Kotthaus, A., Kietzmann, T., Ziemann, C., and Hirsch-Ernst, K. I. (2008) Vesicular localization of the rat ATP-binding cassette half-transporter rAbcb6. Am. J. Physiol. Cell Physiol 294, C579-590
61. Janckila, A. J., and Yam, L. T. (2009) Biology and clinical significance of tartrate-resistant acid phosphatases: new perspectives on an old enzyme. Calcif. Tissue Int. 85, 465-483
62. Sun, P., Sleat, D. E., Lecocq, M., Hayman, A. R., Jadot, M., and Lobel, P. (2008) Acid phosphatase 5 is responsible for removing the mannose 6-phosphate recognition marker from lysosomal proteins. Proc. Natl. Acad. Sci. U.S.A. 105, 16590-16595
63. Einstein, R., and Gabel, C. A. (1991) Cell- and ligand-specific dephosphorylation of acid hydrolases: evidence that the mannose 6-phosphatase is controlled by compartmentalization. J. Cell Biol. 112, 81-94
64. Della Valle, M. C., Sleat, D. E., Sohar, I., Wen, T., Pintar, J. E., Jadot, M., and Lobel, P. (2006) Demonstration of lysosomal localization for the mammalian ependymin-related protein using classical approaches combined with a novel density shift method. J. Biol. Chem. 281, 35436-35445
65. Gasingirwa, M. C., Thirion, J., Costa, C., Flamion, B., Lobel, P., and Jadot, M. (2008) A method to assess the lysosomal residence of proteins in cultured cells. Anal. Biochem. 374, 31-40