Reversible phosphorylation as a molecular switch to regulate plasma membrane targeting of acylated SH4 domain proteins

Traffic

Volumn 10, Issue 8, 2009, Pages 1047-1060

  Tournaviti, Stella ^a   Pietro, Enrica San ^b   Terjung, Stefan ^b   Schafmeier, Tobias ^a   Wegehingel, Sabine ^a   Ritzerfeld, Julia ^a   Schulz, Juliane ^a   Smith, Deborah F ^c   Pepperkok, Rainer ^b   Nickel, Walter ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Endosomal recycling; Intracellular trafficking; Leishmania HASPB; Membrane targeting; SH4 domain; Src kinase; Yes

Indexed keywords

CALYCULIN A; GLUTAMIC ACID; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; HYDROPHILIC ACYLATED SURFACE PROTEIN B; MEMBRANE PROTEIN; MUTANT PROTEIN; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN; PROTEIN KINASE YES; PROTEIN SH4; PROTEIN TYROSINE KINASE; SERINE; THREONINE; UNCLASSIFIED DRUG;

ACYLATION; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BIOACCUMULATION; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOSOME; GOLGI COMPLEX; HUMAN; HUMAN CELL; LEISHMANIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; PROTEIN TRANSPORT; REGULATORY MECHANISM; RNA INTERFERENCE; WILD TYPE;

ANIMALS; ANTIGENS, PROTOZOAN; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; ENDOSOMES; ENZYME INHIBITORS; GLUTAMIC ACID; GOLGI APPARATUS; LEISHMANIA; MUTATION; OXAZOLES; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-YES; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; THREONINE;

EID: 67649882497     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2009.00921.x     Document Type: Article

References (38)

1. Parsons SJ, Parsons JT. Src family kinases, key regulators of signal transduction. Oncogene 2004;23(48):7906-7909.
2. Boggon TJ, Eck MJ. Structure and regulation of Src family kinases. Oncogene 2004;23(48):7918-7927.
3. Smotrys JE, Linder ME. Palmitoylation of intracellular signaling proteins: Regulation and function. Annu Rev Biochem 2004;73:559-587.
4. Resh MD. Fatty acylation of proteins: New insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim Biophys Acta 1999;1451(1):1-16.
5. Resh MD. Membrane targeting of lipid modified signal transduction proteins. Subcell Biochem 2004;37:217-232.
6. Linder ME, Deschenes RJ. Palmitoylation: Policing protein stability and traffic. Nat Rev Mol Cell Biol 2007;8(1):74-84.
7. Hancock JF, Paterson H, Marshall CJ. A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane. Cell 1990;63(1):133-139.
8. Mitchell DA, Vasudevan A, Linder ME, Deschenes RJ. Protein palmitoylation by a family of DHHC protein S-acyltransferases. J Lipid Res 2006;47(6):1118-1127.
9. Denny PW, Gokool S, Russell DG, Field MC, Smith DF. Acylation-dependent protein export in Leishmania. J Biol Chem 2000;275(15):11017-11025.
10. Stegmayer C, Kehlenbach A, Tournaviti S, Wegehingel S, Zehe C, Denny P, Smith DF, Schwappach B, Nickel W. Direct transport across the plasma membrane of mammalian cells of Leishmania HASPB as revealed by a CHO export mutant. J Cell Sci 2005;118(Pt3):517-527.
11. Tournaviti S, Hannemann S, Terjung S, Kitzing TM, Stegmayer C, Ritzerfeld J, Walther P, Grosse R, Nickel W, Fackler OT. SH4-domain-induced plasma membrane dynamization promotes bleb-associated cell motility. J Cell Sci 2007;120(Pt21):3820-3829.
12. McCabe JB, Berthiaume LG. N-terminal protein acylation confers localization to cholesterol, sphingolipid-enriched membranes but not to lipid rafts/caveolae. Mol Biol Cell 2001;12(11):3601-3617.
13. McCabe JB, Berthiaume LG. Functional roles for fatty acylated amino-terminal domains in subcellular localization. Mol Biol Cell 1999;10(11):3771-3786.
14. Wolven A, Okamura H, Rosenblatt Y, Resh MD. Palmitoylation of p59fyn is reversible and sufficient for plasma membrane association. Mol Biol Cell 1997;8(6):1159-1173.
15. Brown DA, London E. Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 1998;14:111-136.
16. Edidin M. The state of lipid rafts: From model membranes to cells. Annu Rev Biophys Biomol Struct 2003;32:257-283.
17. Yasuda K, Kosugi A, Hayashi F, Saitoh S, Nagafuku M, Mori Y, Ogata M, Hamaoka T. Serine 6 of Lck tyrosine kinase: A critical site for Lck myristoylation, membrane localization, and function in T lymphocytes. J Immunol 2000;165(6):3226-3231.
18. Ishihara H, Martin BL, Brautigan DL, Karaki H, Ozaki H, Kato Y, Fusetani N, Watabe S, Hashimoto K, Uemura D, Hartshorne J. Calyculin A and okadaic acid: Inhibitors of protein phosphatase activity. Biochem Biophys Res Commun 1989;159(3):871-877.
19. Resjo S, Oknianska A, Zolnierowicz S, Manganiello V, Degerman E. Phosphorylation and activation of phosphodiesterase type 3B (PDE3B) in adipocytes in response to serine/threonine phosphatase inhibitors: deactivation of PDE3B in vitro by protein phosphatase type 2A. Biochem J 1999;341(Pt3):839-845.
20. Magee T, Seabra MC. Fatty acylation and prenylation of proteins: What's hot in fat. Curr Opin Cell Biol 2005;17(2):190-196.
21. Berthiaume LG. Insider information: How palmitoylation of Ras makes it a signaling double agent. Sci STKE 2002;2002(152):PE41.
22. Denny PW, Smith DF. Rafts and sphingolipid biosynthesis in the kinetoplastid parasitic protozoa. Mol Microbiol 2004;53(3):725-733.
23. Sato I, Obata Y, Kasahara K, Nakayama Y, Fukumoto Y, Yamasaki T, Yokoyama KK, Saito T, Yamaguchi N. Differential trafficking of Src, Lyn, Yes and Fyn is specified by the state of palmitoylation in the SH4 domain. J Cell Sci 2009;122(Pt7):965-975.
24. Liang X, Lu Y, Wilkes M, Neubert TA, Resh MD. The N-terminal SH4 region of the Src family kinase Fyn is modified by methylation and heterogeneous fatty acylation: Role in membrane targeting, cell adhesion, and spreading. J Biol Chem 2004;279(9):8133-8139.
25. Roskoski R Jr. Src kinase regulation by phosphorylation and dephosphorylation. Biochem Biophys Res Commun 2005;331(1):1-14.
26. Gould KL, Hunter T. Platelet-derived growth factor induces multisite phosphorylation of pp60c-src and increases its protein-tyrosine kinase activity. Mol Cell Biol 1988;8(8):3345-3356.
27. Sandilands E, Cans C, Fincham VJ, Brunton VG, Mellor H, Prendergast GC, Norman JC, Superti-Furga G, Frame MC. RhoB and actin polymerization coordinate Src activation with endosome-mediated delivery to the membrane. Dev cell 2004;7(6):855-869.
28. de Diesbach P, Medts T, Carpentier S, D'Auria L, Van Der Smissen P, Platek A, Mettlen M, Caplanusi A, van den Hove MF, Tyteca D, Courtoy PJ. Differential subcellular membrane recruitment of Src may specify its downstream signalling. Exp Cell Res 2008;314(7):1465-1479.
29. Marchese A, Paing MM, Temple BR, Trejo J. G protein-coupled receptor sorting to endosomes and lysosomes. Annu Rev Pharmacol Toxicol 2008; 48: 601-629.
30. Innamorati G, Sadeghi H, Birnbaumer M. Phosphorylation and recycling kinetics of G protein-coupled receptors. J Recept Signal Transduct Res 1999;19(1-4):315-326.
31. Innamorati G, Sadeghi H, Eberle AN, Birnbaumer M. Phosphorylation of the V2 vasopressin receptor. J Biol Chem 1997;272(4):2486-2492.
32. Moore CA, Milano SK, Benovic JL. Regulation of receptor trafficking by GRKs and arrestins. Annu Rev Physiol 2007;69:451-482.
33. Innamorati G, Le Gouill C, Balamotis M, Birnbaumer M. The long and the short cycle. Alternative intracellular routes for trafficking of G-protein-coupled receptors. J Biol Chem 2001;276(16):13096-13103.
34. Engling A, Backhaus R, Stegmayer C, Zehe C, Seelenmeyer C, Kehlenbach A, Schwappach B, Wegehingel S, Nickel W. Biosynthetic FGF-2 is targeted to non-lipid raft microdomains following translocation to the extracellular surface of CHO cells. J Cell Sci 2002;115:3619-3631.
35. Schuck S, Honsho M, Ekroos K, Shevchenko A, Simons K. Resistance of cell membranes to different detergents. Proc Natl Acad Sci U S A 2003;100(10):5795-5800.
36. Tokuyasu KT. A technique for ultracryotomy of cell suspensions and tissues. J Cell Biol 1973;57(2):551-565.
37. Nilsson T, Pypaert M, Hoe MH, Slusarewicz P, Berger EG, Warren G. Overlapping distribution of two glycosyltransferases in the Golgi apparatus of HeLa cells. J Cell Biol 1993;120(1):5-13.
38. Lucocq J. Unbiased 3-D quantitation of ultrastructure in cell biology. Trends Cell Biol 1993;3(10):354-358.