Global topology analysis of pancreatic zymogen granule membrane proteins

Molecular and Cellular Proteomics

Volumn 7, Issue 12, 2008, Pages 2323-2336

  Chen, Xuequn ^a   Ulintz, Peter J ^a   Simon, Eric S ^a   Williams, John A ^a   Andrews, Philip C ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MYOSIN V; PROTEINASE K; RAB PROTEIN; SYNTAXIN; UNCLASSIFIED DRUG; ZYMOGEN GRANULE MEMBRANE PROTEIN;

ARTICLE; CELL MEMBRANE; CELL VACUOLE; CONTROLLED STUDY; CYTOPLASM; ISOTOPE ANALYSIS; PANCREAS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; STATISTICAL MODEL;

AMINO ACID SEQUENCE; BLOTTING, WESTERN; CYTOPLASM; ENDOPEPTIDASE K; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PANCREAS; PEPTIDES; PROTEOMICS; REPRODUCIBILITY OF RESULTS; SECRETORY VESICLES; TRYPSIN;

EID: 58149287751     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M700575-MCP200     Document Type: Article

References (53)

1. Williams, J. A. (2001) Intracellular signaling mechanisms activated by cholecystokinin-regulating synthesis and secretion of digestive enzymes in pancreatic acinar cells. Annu. Rev. Physiol. 63, 77-97
2. Palade, G. (1975) Intracellular aspects of the process of protein synthesis. Science 189, 347-358
3. Chen, X., Walker, A. K., Strahler, J. R., Simon, E. S., Tomanicek-Volk, S. L., Nelson, B. B., Hurley, M. C., Ernst, S. A., Williams, J. A., and Andrews, P. C. (2006) Organellar proteomics: analysis of pancreatic zymogen granule membranes. Mol. Cell. Proteomics 5, 306-312
4. Antonin, W., Wagner, M., Riedel, D., Brose, N., and Jahn, R. (2002) Loss of the zymogen granule protein syncollin affects pancreatic protein synthesis and transport but not secretion. Mol. Cell. Biol. 22, 1545-1554
5. Kim, H., Melen, K., Osterberg, M., and von Heijne, G. (2006) A global topology map of the Saccharomyces cerevisiae membrane proteome. Proc. Natl. Aced. Sci. U. S. A. 103, 11142-11147
6. Daley, D. O., Rapp, M., Granseth, E., Melen, K., Drew, D., and von Heijne, G. (2005) Global topology analysis of the Escherichia coli inner membrane proteome. Science 308, 1321-1323
7. Lorenz, H., Hailey, D. W., and Lippincott-Schwartz, J. (2006) Fluorescence protease protection of GFP chimeras to reveal protein topology and subcellular localization. Nat. Methods 3, 205-210
8. Wu, C. C., MacCoss, M. J., Howell, K. E., and Yates, J. R., III (2003) A method for the comprehensive proteomic analysis of membrane proteins. Nat. Biotechnol. 21, 532-538
9. Wu, C. C., and Yates, J. R., III (2003) The application of mass spectrometry to membrane proteomics. Nat. Biotechnol. 21, 262-267
10. Chen, X., and Andrews, P. C. (2008) Purification and proteomics analysis of pancreatic zymogen granule membranes. Methods Mol. Biol. 432, 275-287
11. Perkins, D. N., Pappin, D. J., Creasy, D. M., and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence data-bases using mass spectrometry data. Electrophoresis 20, 3551-3567
12. Peng, J., Elias, J. E., Thoreen, C. C., Licklider, L. J., and Gygi, S. P. (2003) Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J. Proteome Res. 2, 43-50
13. Elias, J. E., and Gygi, S. P. (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 4, 207-214
14. Huttlin, E. L., Hegeman, A. D., Harms, A. C., and Sussman, M. R. (2007) Prediction of error associated with false-positive rate determination for peptide identification in large-scale proteomics experiments using a combined reverse and forward peptide sequence database strategy. J. Proteome Res. 6, 392-398
15. Nesvizhskii, A. I., Keller, A., Kolker, E., and Aebersold, R. (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658
16. Nesvizhskii, A. I., and Aebersold, R. (2005) Interpretation of shotgun proteomic data: the protein inference problem. Mol. Cell. Proteomics 4, 1419-1440
17. Marelli, M., Smith, J. J., Jung, S., Yi, E., Nesvizhskii, A. I., Christmas, R. H., Salaam, R. A., Tam, Y. Y., Fagarasanu, A., Goodlett, D. R., Aebersold, R., Rachubinski, R. A., and Aitchison, J. D. (2004) Quantitative mass spectrometry reveals a role for the GTPase Rho1p in actin organization on the peroxisome membrane. J. Cell Biol. 167, 1099 -1112
18. Keller, A., Nesvizhskii, A. I., Kolker, E., and Aebersold, R. (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392
19. Wagner, A. C., Wishart, M. J., Mulders, S. M., Blevins, P. M., Andrews, P. C., Lowe, A. W., and Williams, J. A. (1994) GP-3, a newly characterized glycoprotein on the inner surface of the zymogen granule membrane, undergoes regulated secretion. J. Biol. Chem. 269, 9099-9104
20. Imamura, T., Asada, M., Vogt, S. K., Rudnick, D. A., Lowe, M. E., and Muglia, L. J. (2002) Protection from pancreatitis by the zymogen granule membrane protein integral membrane-associated protein-1. J. Biol. Chem. 277, 50725-50733
21. An, S. J., Hansen, N. J., Hodel, A., Jahn, R., and Edwardson, J. M. (2000) Analysis of the association of syncollin with the membrane of the pancreatic zymogen granule. J. Biol. Chem. 275, 11306-11311
22. +V-ATPase. J. Exp. Biol. 203, 127-135
23. Stokes, D. L., Taylor, W. R., and Green, N. M. (1994) Structure, transmembrane topology and helix packing of P-type ion pumps. FEBS Lett. 346, 32-38
24. Fukuda, M. (2005) Versatile role of Rab27 in membrane trafficking: focus on the Rab27 effector families. J. Biochem. (Tokyo) 137, 9-16
25. DiNitto, J. P., Cronin, T. C., and Lambright, D. G. (2003) Membrane recognition and targeting by lipid-binding domains. Sci. STKE 2003, re16
26. Castle, A., and Castle, D. (2005) Ubiquitously expressed secretory carrier membrane proteins (SCAMPs) 1-4 mark different pathways and exhibit limited constitutive trafficking to and from the cell surface. J. Cell Sci. 118, 3769-3780
27. Hubbard, C., Singleton, D., Rauch, M., Jayasinghe, S., Cafiso, D., and Castle, D. (2000) The secretory carrier membrane protein family: structure and membrane topology. Mol. Biol. Cell 11, 2933-2947
28. Steiner, H., and Haass, C. (2000) Intramembrane proteolysis by presenilins. Nat. Rev. Mol. Cell Biol. 1, 217-224
29. Brunkan, A. L., and Goate, A. M. (2005) Presenilin function and γ-secretase activity. J. Neurochem. 93, 769-792
30. Bernsel, A., Viklund, H., Falk, J., Lindahl, E., von Heijne, G., and Elofsson, A. (2008) Prediction of membrane-protein topology from first principles. Proc. Natl. Acad. Sci. U. S. A. 105, 7177-7181
31. Schroer, T. A. (2004) Dynactin. Annu. Rev. Cell Dev. Biol. 20, 759-779
32. Wishart, M. J., Groblewski, G., Goke, B. J., Wagner, A. C., and Williams, J. A. (1994) Secretagogue regulation of pancreatic acinar cell protein phosphorylation shown by large-scale 2D-PAGE. Am. J. Physiol. 267, G676-G686
33. Schmidt, K., Dartsch, H., Linder, D., Kern, H. F., and Kleene, R. (2000) A submembranous matrix of proteoglycans on zymogen granule membranes is involved in granule formation in rat pancreatic acinar cells. J. Cell Sci. 113, 2233-2242
34. Mazella, J. (2001) Sortilin/neurotensin receptor-3: a new tool to investigate neurotensin signaling and cellular trafficking? Cell. Signal. 13, 1-6
35. Hauri, H., Appenzeller, C., Kuhn, F., and Nufer, O. (2000) Lectins and traffic in the secretory pathway. FEBS Lett. 476, 32-37
36. Rindler, M. J., Xu, C. F., Gumper, I., Smith, N. N., and Neubert, T. A. (2007) Proteomic analysis of pancreatic zymogen granules: identification of new granule proteins. J. Proteome Res. 6, 2978-2992
37. Vogel, U. S., and Thompson, R. J. (1988) Molecular structure, localization, and possible functions of the myelin-associated enzyme 2′,3′-cyclic nucleotide 3′-phosphodiestemse. J. Neurochem. 50, 1667-1677
38. Yamamoto, Y., Sokawa, Y., and Maekawa, S. (1997) Biochemical evidence for the presence of NAP-22, a novel acidic calmodulin binding protein, in the synaptic vesicles of rat brain. Neurosci. Lett. 224, 127-130
39. Kraemer, J., Schmitz, F., and Drenckhahn, D. (1999) Cytoplasmic dynein and dynactin as likely candidates for microtubule-dependent apical targeting of pancreatic zymogen granules. Eur J. Cell Biol. 78, 265-277
40. Aderem, A. (1992) The MARCKS brothers: a family of protein kinase C substrates. Cell 71, 713-716
41. Wagner, C. A., Lang, F., and Broer, S. (2001) Function and structure of heterodimeric amino acid transporters. Am. J. Physiol. 281, C1077-C1093
42. Kenny, A. J., and Maroux, S. (1982) Topology of microvillar membrance hydrolases of kidney and intestine. Physiol. Rev. 62, 91-128
43. Laudon, H., Winblad, B., and Naslund, J. (2007) The Alzheimer's disease-associated gamma-secretase complex: functional domains in the presenilin 1 protein. Physiol. Behav. 92, 115-120
44. Kalinina, E., Varlamov, O., and Fricker, L. D. (2002) Analysis of the carboxypeptidase D cytoplasmic domain: Implications in intracellular trafficking. J. Cell. Biochem. 85, 101-111
45. - cotransport: the SLC12 family. Pfluegers Arch. Eur. J. Physiol. 447, 580-593
46. Kieffer, B., Driscoll, P. C., Campbell, I. D., Willis, A. C., van der Merwe, P. A., and Davis, S. J. (1994) Three-dimensional solution structure of the extracellular region of the complement regulatory protein CD59, a new cell-surface protein domain related to snake venom neurotoxins. Biochemistry 33, 4471-4482
47. Yu, G., Nishimura, M., Arawaka, S., Levitan, D., Zhang, L., Tandon, A., Song, Y. Q., Rogaeva, E., Chen, F., Kawarai, T., Supala, A., Levesque, L., Yu, H., Yang, D. S., Holmes, E., Milman, P., Liang, Y., Zhang, D. M., Xu, D. H., Sato, C., Rogaev, E., Smith, M., Janus, C., Zhang, Y., Aebersold, R., Farrer, L. S., Sorbi, S., Bruni, A., Fraser, P., and St George-Hyslop, P. (2000) Nicastrin modulates presenilin-mediated notch/ glp-1 signal transduction and βAPP processing. Nature 407, 48-54
48. Chen, Z., Jones, L. R., O'Brian, J. J., Moorman, J. R., and Cala, S. E. (1998) Structural domains in phospholemman: a possible role for the carboxyl terminus in channel inactivation. Circ. Res. 82, 367-374
49. Spasic, D., Tolia, A., Dillen, K., Baert, V., De Strooper, B., Vrijens, S., and Annaert, W. (2006) Presenilin-1 maintains a nine-transmembrane topology throughout the secretory pathway. J. Biol. Chem. 281, 26569-26577
50. Breitwieser, G. E., McLenithan, J. C., Cortese, J. F., Shields, J. M., Oliva, M. M., Majewski, J. L., Machamer, C. E., and Yang, V. W. (1997) Colonic epithelium-enriched protein A4 is a proteolipid that exhibits ion channel characteristics. Am. J. Physiol. 272, C957-C965
51. Maecker, H. T., Todd, S. C., and Levy, S. (1997) The tetraspanin superfamily: molecular facilitators. FASEB J. 11, 428-442
52. Yokoyama, M., Matsue, H., Muramoto, K., Sasaki, M., Ono, K., and Endo, M. (1988) Isolation and characterization of sulfated glycoprotein from human pancreatic juice. Biochim. Biophys. Acta 967, 34-42
53. Hooper, N. M., Cook, S., Laine, J., and Label, D. (1997) Identification of membrane dipeptidase as a major glycosyl-phosphatidylinositol-anchored protein of the pancreatic zymogen granule membrane, and evidence for its release by phospholipase A. Biochem. J. 324, 151-157