Binding of plasma membrane lipids recruits the yeast integral membrane protein Ist2 to the cortical ER

Traffic

Volumn 10, Issue 8, 2009, Pages 1084-1097

  Fischer, Marcel André ^a   Temmerman, Koen ^a   Ercan, Ebru ^a   Nickel, Walter ^a   Seedorf, Matthias ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Cortical ER; ER subdomain; Lipid binding motif, PI(4,5)P2; Plasma membrane; Sorting signal

Indexed keywords

GREEN FLUORESCENT PROTEIN; LIPOSOME; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN; PROTEIN IST2; PROTEIN TMEM16A; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOACCUMULATION; CELL MEMBRANE; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; MOLECULAR DYNAMICS; NONHUMAN; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; SECRETORY VESICLE; SIGNAL TRANSDUCTION;

ATP-BINDING CASSETTE TRANSPORTERS; CELL MEMBRANE; ENDOPLASMIC RETICULUM; GREEN FLUORESCENT PROTEINS; LIPOSOMES; MEMBRANE LIPIDS; MEMBRANE PROTEINS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN BINDING; PROTEIN SORTING SIGNALS; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 67649882496     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2009.00926.x     Document Type: Article

References (50)

1. McLaughlin S, Murray D. Plasma membrane phosphoinositide organization by protein electrostatics. Nature 2005; 438 (7068): 605-611.
2. Lemmon MA. Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 2008; 9 (2): 99-111.
3. Sheetz MP, Sable JE, Dobereiner HG. Continuous membrane-cytoskeleton adhesion requires continuous accommodation to lipid and cytoskeleton dynamics. Annu Rev Biophys Biomol Struct 2006; 35: 417-434.
4. Di Paolo G, De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature 2006; 443 (7112): 651-657.
5. Roth MG. Phosphoinositides in constitutive membrane traffic. Physiol Rev 2004; 84 (3): 699-730.
6. Behnia R, Munro S. Organelle identity and the signposts for membrane traffic. Nature 2005; 438 (7068): 597-604.
7. De Matteis MA, Godi A. PI-loting membrane traffic. Nat Cell Biol 2004; 6 (6): 487-492.
8. Gillooly DJ, Morrow IC, Lindsay M, Gould R, Bryant NJ, Gaullier JM, Parton RG, Stenmark H. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J 2000; 19 (17): 4577-4588.
9. Lindmo K, Stenmark H. Regulation of membrane traffic by phosphoinositide 3-kinases. J Cell Sci 2006; 119 (Pt 4): 605-614.
10. Maass K, Fischer MA, Seiler M, Temmerman K, Nickel W, Seedorf M. A signal comprising a basic cluster and an amphipathic α-helix interacts with lipids and is required for the transport of Ist2 to the yeast cortical ER. J Cell Sci 2009; 122: 625-635.
11. Schroeder BC, Cheng T, Jan YN, Jan LY. Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 2008; 134 (6): 1019-1029.
12. Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim WS, Park SP, Lee J, Lee B, Kim BM, Raouf R, Shin YK, Oh U. TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 2008; 455 (7217): 1210-1215.
13. Caputo A, Caci E, Ferrera L, Pedemonte N, Barsanti C, Sondo E, Pfeffer U, Ravazzolo R, Zegarra-Moran O, Galietta LJ. TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science 2008; 322 (5901): 590-594.
14. Juschke C, Ferring D, Jansen RP, Seedorf M. A novel transport pathway for a yeast plasma membrane protein encoded by a localized mRNA. Curr Biol 2004; 14 (5): 406-411.
15. Juschke C, Wachter A, Schwappach B, Seedorf M. SEC18/NSF-independent, protein-sorting pathway from the yeast cortical ER to the plasma membrane. J Cell Biol 2005; 169 (4): 613-622.
16. Pichler H, Gaigg B, Hrastnik C, Achleitner G, Kohlwein SD, Zellnig G, Perktold A, Daum G. A subfraction of the yeast endoplasmic reticulum associates with the plasma membrane and has a high capacity to synthesize lipids. Eur J Biochem 2001; 268 (8): 2351-2361.
17. Perktold A, Zechmann B, Daum G, Zellnig G. Organelle association visualized by three-dimensional ultrastructural imaging of the yeast cell. FEMS Yeast Res 2007; 7 (4): 629-638.
18. Griffith J, Mari M, De Maziere A, Reggiori F. A cryosectioning procedure for the ultrastructural analysis and the immunogold labelling of yeast Saccharomyces cerevisiae. Traffic 2008; 9 (7): 1060-1072.
19. Franz A, Maass K, Seedorf M. A complex peptide-sorting signal, but no mRNA signal, is required for the Sec-independent transport of Ist2 from the yeast ER to the plasma membrane. FEBS Lett 2007; 581 (3): 401-405.
20. Olivier C, Poirier G, Gendron P, Boisgontier A, Major F, Chartrand P. Identification of a conserved RNA motif essential for She2p recognition and mRNA localization to the yeast bud. Mol Cell Biol 2005; 25 (11): 4752-4766.
21. Jambhekar A, McDermott K, Sorber K, Shepard KA, Vale RD, Takizawa PA, DeRisi JL. Unbiased selection of localization elements reveals cis-acting determinants of mRNA bud localization in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 2005; 102 (50): 18005-18010.
22. Temmerman K, Ebert AD, Muller HM, Sinning I, Tews I, Nickel W. A direct role for phosphatidylinositol-4,5-bisphosphate in unconventional secretion of fibroblast growth factor 2. Traffic 2008; 9 (7): 1204-1217.
23. Temmerman K, Nickel W. A novel flow cytometric assay to quantify interactions between proteins and membrane lipids. J Lipid Res 2009.
24. Burd CG, Emr SD. Phosphatidylinositol(3)-phosphate signaling mediated by specific binding to RING FYVE domains. Mol Cell 1998; 2 (1): 157-162.
25. Stefan CJ, Audhya A, Emr SD. The yeast synaptojanin-like proteins control the cellular distribution of phosphatidylinositol (4,5)-bisphosphate. Mol Biol Cell 2002; 13 (2): 542-557.
26. Dowler S, Currie RA, Campbell DG, Deak M, Kular G, Downes CP, Alessi DR. Identification of pleckstrin-homology-domain-containing proteins with novel phosphoinositide-binding specificities. Biochem J 2000; 351 (Pt 1): 19-31.
27. Levine TP, Munro S. Targeting of Golgi-specific pleckstrin homology domains involves both PtdIns 4-kinase-dependent and -independent components. Curr Biol 2002; 12 (9): 695-704.
28. Lemmon MA, Ferguson KM, O'Brien R, Sigler PB, Schlessinger J. Specific and high-affinity binding of inositol phosphates to an isolated pleckstrin homology domain. Proc Natl Acad Sci U S A 1995; 92 (23): 10472-10476.
29. Kavran JM, Klein DE, Lee A, Falasca M, Isakoff SJ, Skolnik EY, Lemmon MA. Specificity and promiscuity in phosphoinositide binding by pleckstrin homology domains. J Biol Chem 1998; 273 (46): 30497-30508.
30. Votsmeier C, Gallwitz D. An acidic sequence of a putative yeast Golgi membrane protein binds COPII and facilitates ER export. EMBO J 2001; 20 (23): 6742-6750.
31. Homma K, Terui S, Minemura M, Qadota H, Anraku Y, Kanaho Y, Ohya Y. Phosphatidylinositol-4-phosphate 5-kinase localized on the plasma membrane is essential for yeast cell morphogenesis. J Biol Chem1998; 273 (25): 15779-15786.
32. Audhya A, Foti M, Emr SD. Distinct roles for the yeast phosphatidylinositol 4-kinases, Stt4p and Pik1p, in secretion, cell growth, and organelle membrane dynamics. Mol Biol Cell 2000; 11 (8): 2673-2689.
33. Galindo BE, Vacquier VD. Phylogeny of the TMEM16 protein family: Some members are overexpressed in cancer. Int J Mol Med 2005; 16 (5): 919-924.
34. Nakatsukasa K, Brodsky JL. The recognition and retrotranslocation of misfolded proteins from the endoplasmic reticulum. Traffic 2008; 9 (6): 861-870.
35. Pan X, Roberts P, Chen Y, Kvam E, Shulga N, Huang K, Lemmon S, Goldfarb DS. Nucleus-vacuole junctions in Saccharomyces cerevisiae are formed through the direct interaction of Vac8p with Nvj1p. Mol Biol Cell 2000; 11 (7): 2445-2457.
36. Kvam E, Goldfarb DS. Structure and function of nucleus-vacuole junctions: Outer-nuclear-membrane targeting of Nvj1p and a role in tryptophan uptake. J Cell Sci 2006; 119 (Pt 17): 3622-3633.
37. Fehrenbacher KL, Davis D, Wu M, Boldogh I, Pon LA. Endoplasmic reticulum dynamics, inheritance, and cytoskeletal interactions in budding yeast. Mol Biol Cell 2002; 13 (3): 854-865.
38. Du Y, Walker L, Novick P, Ferro-Novick S. Ptc1p regulates cortical ER inheritance via Slt2p. EMBO J 2006; 25 (19): 4413-4422.
39. Loewen CJ, Young BP, Tavassoli S, Levine TP. Inheritance of cortical ER in yeast is required for normal septin organization. J Cell Biol 2007; 179 (3): 467-483.
40. Wiederkehr A, Du Y, Pypaert M, Ferro-Novick S, Novick P. Sec3p is needed for the spatial regulation of secretion and for the inheritance of the cortical endoplasmic reticulum. Mol Biol Cell 2003; 14 (12): 4770-4782.
41. Reinke CA, Kozik P, Glick BS. Golgi inheritance in small buds of Saccharomyces cerevisiae is linked to endoplasmic reticulum inheritance. Proc Natl Acad Sci U S A 2004; 101 (52): 18018-18023.
42. De Craene JO, Coleman J, Estrada de Martin P, Pypaert M, Anderson S, Yates JR III, Ferro-Novick S, Novick P. Rtn1p is involved in structuring the cortical endoplasmic reticulum. Mol Biol Cell 2006; 17 (7): 3009-3020.
43. Wright R, Basson M, D'Ari L, Rine J. Increased amounts of HMG-CoA reductase induce "karmellae": A proliferation of stacked membrane pairs surrounding the yeast nucleus. J Cell Biol 1988; 107 (1): 101-114.
44. Koning AJ, Roberts CJ, Wright RL. Different subcellular localization of Saccharomyces cerevisiae HMG-CoA reductase isozymes at elevated levels corresponds to distinct endoplasmic reticulum membrane proliferations. Mol Biol Cell 1996; 7 (5): 769-789.
45. Snapp EL, Hegde RS, Francolini M, Lombardo F, Colombo S, Pedrazzini E, Borgese N, Lippincott-Schwartz J. Formation of stacked ER cisternae by low affinity protein interactions. J Cell Biol 2003; 163 (2): 257-269.
46. Thomas BJ, Rothstein R. Elevated recombination rates in transcriptionally active DNA. Cell 1989; 56 (4): 619-630.
47. Sherman F. Getting started with yeast. Methods Enzymol 2002; 350: 3-41.
48. Gietz RD, Woods RA. Transformation of yeast by lithium acetate/ single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 2002; 350: 87-96.
49. van Meer G. Lipids of the Golgi membrane. Trends Cell Biol 1998; 8 (1): 29-33.
50. Frey S, Pool M, Seedorf M. Scp160p, an RNA-binding, polysome-associated protein, localizes to the endoplasmic reticulum of Saccharomyces cerevisiae in a microtubule-dependent manner. J Biol Chem 2001; 276 (19): 15905-15912.