A novel conserved targeting motif found in ABCA transporters mediates trafficking to early post-Golgi compartments

Journal of Lipid Research

Volumn 52, Issue 8, 2011, Pages 1471-1482

  Beers, Michael F ^a   Hawkins, Arie ^a   Shuman, Henry ^a   Zhao, Ming ^a   Newitt, Jennifer L ^a   Maguire, Jean Ann ^a   Ding, Wenge ^a   Mulugeta, Surafel ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

ABCA3; ATP binding cassette, class A; Post Golgi sorting; Protein trafficking

Indexed keywords

ABC TRANSPORTER; ATP BINDING CASSETTE CLASS A PROTEIN; SURFACTANT PROTEIN C; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CELL COMPARTMENTALIZATION; CELL SELECTION; CHIMERA; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE FUNCTION; GENE MUTATION; GENETIC CONSERVATION; GENETIC TRANSFECTION; GOLGI COMPLEX; INTRACELLULAR SIGNALING; INTRACELLULAR TRANSPORT; LYSOSOME; MOLECULAR MODEL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN TARGETING;

AMINO ACID MOTIFS; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CELL LINE, TUMOR; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; HUMANS; LYSOSOMES; MICE; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MUTATION; PLASMIDS; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PULMONARY SURFACTANT-ASSOCIATED PROTEIN C; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 79960693714     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M013284     Document Type: Article

References (51)

1. Higgins, C. F., I. D. Hiles, G. P. Salmond, D. R. Gill, J. A. Downie, I. J. Evans, I. B. Holland, L. Gray, S. D. Buckel, and A. W. Bell. 1986. A family of related ATP-binding subunits coupled to many distinct biological processes in bacteria. Nature. 323: 448-450.
2. Bodzioch, M., E. Orso, J. Klucken, T. Langmann, A. Bottcher, W. Diederich, W. Drobnik, S. Barlage, C. Buchler, M. Porsch-Ozcurumez, et al. 1999. The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat. Genet. 22: 347-351.
3. Brooks-Wilson, A., M. Marcil, S. M. Clee, L. H. Zhang, K. Roomp, M. van Dam, L. Yu, C. Brewer, J. A. Collins, H. O. Molhuizen, et al. 1999. Mutations in ABC1 in Tangier disease and familial highdensity lipoprotein deficiency. Nat. Genet. 22: 336-345.
4. Oram, J. F., and A. M. Vaughan. 2000. ABCA1-mediated transport of cellular cholesterol and phospholipids to HDL apolipoproteins. Curr. Opin. Lipidol. 11: 253-260.
5. Cheong, N., M. Madesh, L. W. Gonzales, M. Zhao, K. Yu, P. L. Ballard, and H. Shuman. 2006. Functional and trafficking defects in ATP binding cassette A3 mutants associated with respiratory distress syndrome. J. Biol. Chem. 281: 9791-9800.
6. Cheong, N., H. Zhang, M. Madesh, M. Zhao, K. Yu, C. Dodia, A. B. Fisher, R. C. Savani, and H. Shuman. 2007. ABCA3 is critical for lamellar body biogenesis in vivo. J. Biol. Chem. 282: 23811-23817.
7. Matsumura, Y., H. Sakai, M. Sasaki, N. Ban, and N. Inagaki. 2007. ABCA3-mediated choline-phospholipids uptake into intracellular vesicles in A549 cells. FEBS Lett. 581: 3139-3144. (Pubitemid 46977352)
8. Wang, C., W. A. Wilson, S. D. Moore, B. E. Mace, N. Maeda, D. E. Schmechel, and P. M. Sullivan. 2005. Human apoE4-targeted replacement mice display synaptic deficits in the absence of neuropathology. Neurobiol. Dis. 18: 390-398.
9. Kelsell, D. P., E. E. Norgett, H. Unsworth, M. T. Teh, T. Cullup, C. A. Mein, P. J. Dopping-Hepenstal, B. A. Dale, G. Tadini, P. Fleckman, et al. 2005. Mutations in ABCA12 underlie the severe congenital skin disease harlequin ichthyosis. Am. J. Hum. Genet. 76: 794-803.
10. Albrecht, C., and E. Viturro. 2007. The ABCA subfamily--gene and protein structures, functions and associated hereditary diseases. Pflugers Arch. 453: 581-589. (Pubitemid 46192531)
11. Kaminski, W. E., A. Piehler, and J. J. Wenzel. 2006. ABC A-subfamily transporters: structure, function and disease. Biochim. Biophys. Acta. 1762: 510-524.
12. Tusnady, G. E., B. Sarkadi, I. Simon, and A. Varadi. 2006. Membrane topology of human ABC proteins. FEBS Lett. 580: 1017-1022. (Pubitemid 43185282)
13. Nothwehr, S. F., and J. I. Gordon. 1990. Targeting of proteins into the eukaryotic secretory pathway: signal peptide structure/function relationships. Bioessays. 12: 479-484.
14. Sato, T. K., M. Overduin, and S. D. Emr. 2001. Location, location, location: membrane targeting directed by PX domains. Science. 294: 1881-1885.
15. Prado, V. F., and M. A. Prado. 2002. Signals involved in targeting membrane proteins to synaptic vesicles. Cell. Mol. Neurobiol. 22: 565-577.
16. Haft, C. R., S. M.de la Luz, I. Hamer, J. L. Carpentier, and S. I. Taylor. 1998. Analysis of the juxtamembrane dileucine motif in the insulin receptor. Endocrinology. 139: 1618-1629.
17. Russo, S. J., W-J. Wang, C. Lomax, and M. F. Beers. 1999. Structural requirements for intracellular targeting of surfactant protein C. Am. J. Physiol. 277: L1034-L1044.
18. Johnson, A. L., P. Braidotti, G. G. Pietra, S. J. Russo, A. Kabore, W. J. Wang, and M. F. Beers. 2001. Post-translational processing of surfactant protein-C proprotein: targeting motifs in the NH(2)- terminal flanking domain are cleaved in late compartments. Am. J. Respir. Cell Mol. Biol. 24: 253-263.
19. Kotorashvili, A., S. J. Russo, S. Mulugeta, S. Guttentag, and M. F. Beers. 2009. Anterograde transport of surfactant protein C proprotein to distal processing compartments requires PPDY-mediated association with Nedd4 ubiquitin ligases. J. Biol. Chem. 284: 16667-16678.
20. Jakob, V., A. Schreiner, R. Tikkanen, and A. Starzinski-Powitz. 2006. Targeting of transmembrane protein shrew-1 to adherens junctions is controlled by cytoplasmic sorting motifs. Mol. Biol. Cell. 17: 3397-3408.
21. Mulugeta, S., J. M. Gray, K. L. Notarfrancesco, L. W. Gonzales, M. Koval, S. I. Feinstein, P. L. Ballard, A. B. Fisher, and H. Shuman. 2002. Identification of LBM180, a lamellar body limiting membrane protein of alveolar type II cells, as the ABC transporter protein ABCA3. J. Biol. Chem. 277: 22147-22155.
22. Mack, J. T., V. Beljanski, K. D. Tew, and D. M. Townsend. 2006. The ATP-binding cassette transporter ABCA2 as a mediator of intracellular trafficking. Biomed. Pharmacother. 60: 587-592.
23. Mulugeta, S., J. A. Maguire, J. L. Newitt, S. J. Russo, A. Kotorashvili, and M. F. Beers. 2007. Misfolded BRICHOS SP-C mutant proteins induce apoptosis via caspase-4- and cytochrome c-related mechanisms. Am. J. Physiol. Lung Cell. Mol. Physiol. 293: L720-L729.
24. Beers, M. F., and S. Mulugeta. 2006. Surfactant proteins B and C (SP-B and SP-C). In Encyclopedia of Respiratory Medicine. G. L. Laurent and S. D. Shapiro, editors. Elsevier, Oxford. 148-151.
25. Beers, M. F. 1998. Molecular processing and cellular metabolism of surfactant protein C. In Lung Surfactant: Cellular and Molecular Processing. S. A. Rooney, editor. R. G. Landes, Austin, TX. 93-124.
26. Beers, M. F., C. A. Lomax, and S. J. Russo. 1998. Synthetic processing of surfactant protein C by alevolar epithelial cells. The COOH terminus of proSP-C is required for post-translational targeting and proteolysis. J. Biol. Chem. 273: 15287-15293.
27. Kabore, A. F., W. J. Wang, S. J. Russo, and M. F. Beers. 2001. Biosynthesis of surfactant protein C: characterization of aggresome formation by EGFP chimeras containing propeptide mutants lacking conserved cysteine residues. J. Cell Sci. 114: 293-302.
28. Wang, W. J., S. Mulugeta, S. J. Russo, and M. F. Beers. 2003. Deletion of exon 4 from human surfactant protein C results in aggresome formation and generation of a dominant negative. J. Cell Sci. 116: 683-692.
29. Johansson, J. 1998. Structure and properties of surfactant protein C. Biochim. Biophys. Acta. 1408: 161-172.
30. Yamano, G., H. Funahashi, O. Kawanami, L. X. Zhao, N. Ban, Y. Uchida, T. Morohoshi, J. Ogawa, S. Shioda, and N. Inagaki. 2001. ABCA3 is a lamellar body membrane protein in human lung alveolar type II cells. FEBS Lett. 508: 221-225. (Pubitemid 33079249)
31. Parks, G. D., and R. A. Lamb. 1991. Topology of eukaryotic type II membrane proteins: importance of N-terminal positively charged residues flanking the hydrophobic domain. Cell. 64: 777-787.
32. Beltzer, J. P., K. Fiedler, C. Fuhrer, I. Geffen, C. Handschin, H. P. Wessels, and M. Spiess. 1991. Charged residues are major determinants of the transmembrane orientation of a signal-anchor sequence. J. Biol. Chem. 266: 973-978.
33. Parks, G. D., and R. A. Lamb. 1993. Role of NH2-terminal positively charged residues in establishing membrane protein topology. J. Biol. Chem. 268: 19101-19109.
34. Goder, V., and M. Spiess. 2001. Topogenesis of membrane proteins: determinants and dynamics. FEBS Lett. 504: 87-93. (Pubitemid 32787054)
35. Conkright, J. J., K. S. Apsley, E. P. Martin, R. Ridsdale, W. R. Rice, C. L. Na, B. Yang, and T. E. Weaver. 2010. Nedd4-2-mediated ubiquitination facilitates processing of surfactant protein-C. Am. J. Respir. Cell Mol. Biol. 42: 181-189.
36. Tartakoff, A. M. 1983. Perturbation of vesicular traffic with the carboxylic ionophore monensin. Cell. 32: 1026-1028. (Pubitemid 13033044)
37. ten Brinke, A., J. J. Batenburg, H. P. Haagsman, L. M. van Golde, and A. B. Vaandrager. 2002. Differential effect of brefeldin A on the palmitoylation of surfactant protein C proprotein mutants. Biochem. Biophys. Res. Commun. 290: 532-538.
38. ten Brinke, A., A. B. Vaandrager, H. P. Haagsman, A. N. Ridder, L. M. van Golde, and J. J. Batenburg. 2002. Structural requirements for palmitoylation of surfactant protein C precursor. Biochem. J. 361: 663-671.
39. Mulugeta, S., and M. F. Beers. 2003. Processing of surfactant protein C requires a type II transmembrane topology directed by juxtamembrane positively charged residues. J. Biol. Chem. 278: 47979-47986.
40. Wang, W. J., S. J. Russo, S. Mulugeta, and M. F. Beers. 2002. Biosynthesis of surfactant protein C (SP-C). Sorting of SP-C proprotein involves homomeric association via a signal anchor domain. J. Biol. Chem. 277: 19929-19937.
41. Mulugeta, S., and M. F. Beers. 2006. Surfactant protein C: its unique properties and emerging immunomodulatory role in the lung. Microbes Infect. 8: 2317-2323.
42. Beers, M. F., and S. Mulugeta. 2005. Surfactant protein C biosynthesis and its emerging role in conformational lung disease. Annu. Rev. Physiol. 67: 663-696.
43. Deborde, A., D. Gravotta, A. Lakkaraju, and E. Rodriguez-Boulan. 2008. Golgi apparatus and epithelial cell polarity. In The Golgi Apparatus. A. Mironov and M. Pavelka, editors. Springer Wien New York, Austria. 563-579.
44. Arvan, P., and J. D. Castle. 1987. Phasic release of newly synthesized secretory proteins in the unstimulated rat exocrine pancreas. J. Cell Biol. 104: 243-252.
45. Arvan, P., R. Kuliawat, D. Prabakaran, A. M. Zavacki, D. Elahi, S. Wang, and D. Pilkey. 1991. Protein discharge from immature secretory granules displays both regulated and constitutive characteristics. J. Biol. Chem. 266: 14171-14174.
46. Glombik, M. M., and H. H. Gerdes. 2000. Signal-mediated sorting of neuropeptides and prohormones: secretory granule biogenesis revisited. Biochimie. 82: 315-326.
47. Arvan, P., and D. Castle. 1998. Sorting and storage during secretory granule biogenesis: looking backward and looking forward. Biochem. J. 332: 593-610. (Pubitemid 28306683)
48. Tooze, S. A. 1998. Biogenesis of secretory granules in the trans-Golgi network of neuroendocrine and endocrine cells. Biochim. Biophys. Acta. 1404: 231-244.
49. Kirchhausen, T. 2002. Single-handed recognition of a sorting traffic motif by the GGA proteins. Nat. Struct. Biol. 9: 241-244.
50. Shiba, T., H. Takatsu, T. Nogi, N. Matsugaki, M. Kawasaki, N. Igarashi, M. Suzuki, R. Kato, T. Earnest, K. Nakayama, et al. 2002. Structural basis for recognition of acidic-cluster dileucine sequence by GGA1. Nature. 415: 937-941.
51. Rothman, J. E., and F. T. Wieland. 1996. Protein sorting by transport vesicles. Science. 272: 227-234.