The dual PH domain protein Opy1 functions as a sensor and modulator of PtdIns(4,5)P2 synthesis

EMBO Journal

Volumn 31, Issue 13, 2012, Pages 2882-2894

  Ling, Yading ^a   Stefan, Christopher J ^a   MacGurn, Jason A ^a   Audhya, Anjon ^b   Emr, Scott D ^a  

^a School of Integrative Plant Sciences   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

phosphatidylinositol 4,5 bisphosphate; phosphoinositide kinase complex; tandem PH domain containing proteins

Indexed keywords

CYTOPLASM PROTEIN; MSS4 PROTEIN; OPY1 PROTEIN; PHOSPHATIDYLINOSITOL 4 PHOSPHATE KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS;

1-PHOSPHATIDYLINOSITOL 4-KINASE; CELL MEMBRANE; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

EID: 84863849284     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.127     Document Type: Article

References (47)

1. Abrams CS, Zhang J, Downes CP, Tang X, Zhao W, Rittenhouse SE (1996) Phosphopleckstrin inhibits gbetagamma-activable platelet phosphatidylinositol-4, 5-bisphosphate 3-kinase. J Biol Chem 271: 25192-25197 (Pubitemid 26337881)
2. Allam A, Marshall AJ (2005) Role of the adaptor proteins Bam32, TAPP1 and TAPP2 in lymphocyte activation. Immunol Lett 97: 7-17 (Pubitemid 40038850)
3. Audhya A, Emr SD (2002) Stt4 PI 4-kinase localizes to the plasma membrane and functions in the Pkc1-mediated MAP kinase cascade. Dev Cell 2: 593-605 (Pubitemid 34538140)
4. Audhya A, Emr SD (2003) Regulation of PI4,5P2 synthesis by nuclear-cytoplasmic shuttling of the Mss4 lipid kinase. EMBO J 22: 4223-4236 (Pubitemid 37021750)
5. Audhya A, Foti M, Emr SD (2000) Distinct roles for the yeast phosphatidylinositol 4-kinases, Stt4p and Pik1p, in secretion, cell growth, and organelle membrane dynamics. Mol Biol Cell 11: 2673-2689 (Pubitemid 30645035)
6. Baird D, Stefan C, Audhya A, Weys S, Emr SD (2008) Assembly of the PtdIns 4-kinase Stt4 complex at the plasma membrane requires Ypp1 and Efr3. J Cell Biol 183: 1061-1074
7. Behnia R, Munro S (2005) Organelle identity and the signposts for membrane traffic. Nature 438: 597-604 (Pubitemid 41740563)
8. Bertin A, McMurray MA, Thai L, Garcia 3rd G, Votin V, Grob P, Allyn T, Thorner J, Nogales E (2010) Phosphatidylinositol-4,5-bisphosphate promotes budding yeast septin filament assembly and organization. J Mol Biol 404: 711-731
9. Desrivieres S, Cooke FT, Parker PJ, Hall MN (1998) MSS4, a phosphatidylinositol-4-phosphate 5-kinase required for organization of the actin cytoskeleton in Saccharomyces cerevisiae. J Biol Chem 273: 15787-15793
10. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443: 651-657 (Pubitemid 44564702)
11. Dowler S, Currie RA, Campbell DG, Deak M, Kular G, Downes CP, Alessi DR (2000) Identification of pleckstrin-homology-domaincontaining proteins with novel phosphoinositide-binding specificities. Biochem J 351(Part 1): 19-31
12. Edlich C, Stier G, Simon B, Sattler M, Muhle-Goll C (2005) Structure and phosphatidylinositol-(3,4)-bisphosphate binding of the C-terminal PH domain of human pleckstrin. Structure 13: 277-286 (Pubitemid 40247703)
13. Edwards MC, Liegeois N, Horecka J, DePinho RA, Sprague Jr GF, Tyers M, Elledge SJ (1997) Human CPR (cell cycle progression restoration) genes impart a Far- phenotype on yeast cells. Genetics 147: 1063-1076 (Pubitemid 27467451)
14. Fairn GD, Ogata K, Botelho RJ, Stahl PD, Anderson RA, De Camilli P, Meyer T, Wodak S, Grinstein S (2009) An electrostatic switch displaces phosphatidylinositol phosphate kinases from the membrane during phagocytosis. J Cell Biol 187: 701-714
15. Foti M, Audhya A, Emr SD (2001) Sac1 lipid phosphatase and Stt4 phosphatidylinositol 4-kinase regulate a pool of phosphatidylinositol 4-phosphate that functions in the control of the actin cytoskeleton and vacuole morphology. Mol Biol Cell 12: 2396-2411 (Pubitemid 33051964)
16. Garrenton LS, Stefan CJ, McMurray MA, Emr SD, Thorner J (2010) Pheromone-induced anisotropy in yeast plasma membrane phosphatidylinositol-4,5- bisphosphate distribution is required for MAPK signaling. Proc Natl Acad Sci USA 107: 11805-11810
17. Haslam RJ, Koide HB, Hemmings BA (1993) Pleckstrin domain homology. Nature 363: 309-310
18. Haucke V (2005) Phosphoinositide regulation of clathrin-mediated endocytosis. Biochem Soc Trans 33(Part 6): 1285-1289
19. Hokin LE (1985) Receptors and phosphoinositide-generated second messengers. Annu Rev Biochem 54: 205-235
20. Homma K, Terui S, Minemura M, Qadota H, Anraku Y, Kanaho Y, Ohya Y (1998) Phosphatidylinositol-4-phosphate 5-kinase localized on the plasma membrane is essential for yeast cell morphogenesis. J Biol Chem 273: 15779-15786 (Pubitemid 28298199)
21. James DJ, Khodthong C, Kowalchyk JA, Martin TF (2008) Phosphatidylinositol 4,5-bisphosphate regulates SNARE-dependent membrane fusion. J Cell Biol 182: 355-366
22. Krauss M, Kukhtina V, Pechstein A, Haucke V (2006) Stimulation of phosphatidylinositol kinase type I-mediated phosphatidylinositol (4,5)-bisphosphate synthesis by AP-2mu-cargo complexes. Proc Natl Acad Sci USA 103: 11934-11939 (Pubitemid 44215789)
23. Kunz J, Wilson MP, Kisseleva M, Hurley JH, Majerus PW, Anderson RA (2000) The activation loop of phosphatidylinositol phosphate kinases determines signaling specificity. Mol Cell 5: 1-11 (Pubitemid 30105431)
24. Lemmon MA (2008) Membrane recognition by phospholipidbinding domains. Nat Rev Mol Cell Biol 9: 99-111
25. Ling K, Doughman RL, Firestone AJ, Bunce MW, Anderson RA (2002) Type I gamma phosphatidylinositol phosphate kinase targets and regulates focal adhesions. Nature 420: 89-93 (Pubitemid 35291445)
26. Liu J, Zuo X, Yue P, Guo W (2007) Phosphatidylinositol 4,5-bisphosphate mediates the targeting of the exocyst to the plasma membrane for exocytosis in mammalian cells. Mol Biol Cell 18: 4483-4492 (Pubitemid 350060175)
27. Logan MR, Mandato CA (2006) Regulation of the actin cytoskeleton by PIP2 in cytokinesis. Biol Cell 98: 377-388 (Pubitemid 43853424)
28. Longtine MS, McKenzie III A, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961 (Pubitemid 28328001)
29. Markus SM, Punch JJ, Lee WL (2009) Motor- and tail-dependent targeting of dynein to microtubule plus ends and the cell cortex. Curr Biol 19: 196-205
30. Martin TF (1998) Phosphoinositide lipids as signaling molecules: common themes for signal transduction, cytoskeletal regulation, and membrane trafficking. Annu Rev Cell Dev Biol 14: 231-264
31. Nakano-Kobayashi A, Yamazaki M, Unoki T, Hongu T, Murata C, Taguchi R, Katada T, Frohman MA, Yokozeki T, Kanaho Y (2007) Role of activation of PIP5Kgamma661 by AP-2 complex in synaptic vesicle endocytosis. EMBO J 26: 1105-1116
32. Parrish WR, Stefan CJ, Emr SD (2004) Essential role for the myotubularin-related phosphatase Ymr1p and the synaptojanin-like phosphatases Sjl2p and Sjl3p in regulation of phosphatidylinositol 3-phosphate in yeast. Mol Biol Cell 15: 3567-3579 (Pubitemid 38989697)
33. Pruyne D, Bretscher A (2000a) Polarization of cell growth in yeast. J Cell Sci 113(Part 4): 571-585
34. Pruyne D, Bretscher A (2000b) Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J Cell Sci 113(Part 3): 365-375 (Pubitemid 30116643)
35. Sikorski RS, Hieter P (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27
36. Smaczynska-de II R, Costa R, Ayscough KR (2008) Yeast Arf3p modulates plasma membrane PtdIns(4,5)P2 levels to facilitate endocytosis. Traffic 9: 559-573 (Pubitemid 351351615)
37. Stefan CJ, Audhya A, Emr SD (2002) The yeast synaptojanin-like proteins control the cellular distribution of phosphatidylinositol (4,5)-bisphosphate. Mol Biol Cell 13: 542-557 (Pubitemid 34165082)
38. Stefan CJ, Manford AG, Baird D, Yamada-Hanff J, Mao Y, Emr SD (2011) Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell 144: 389-401
39. Sun Y, Carroll S, Kaksonen M, Toshima JY, Drubin DG (2007) PtdIns(4,5)P2 turnover is required for multiple stages during clathrin- and actin-dependent endocytic internalization. J Cell Biol 177: 355-367 (Pubitemid 46658645)
40. Szentpetery Z, Balla A, Kim YJ, Lemmon MA, Balla T (2009) Live cell imaging with protein domains capable of recognizing phosphatidylinositol 4,5-bisphosphate; a comparative study. BMC Cell Biol 10: 67
41. Vicinanza M, D'Angelo G, Di Campli A, De Matteis MA (2008) Function and dysfunction of the PI system in membrane trafficking. EMBO J 27: 2457-2470
42. Walther TC, Brickner JH, Aguilar PS, Bernales S, Pantoja C,Walter P (2006) Eisosomes mark static sites of endocytosis. Nature 439: 998-1003 (Pubitemid 43292420)
43. Wang DS, Shaw R, Winkelmann JC, Shaw G (1994) Binding of PH domains of beta-adrenergic receptor kinase and beta-spectrin to WD40/beta-transducin repeat containing regions of the beta-subunit of trimeric G-proteins. Biochem Biophys Res Commun 203: 29-35
44. Wullschleger S, Wasserman DH, Gray A, Sakamoto K, Alessi DR (2011) Role of TAPP1 and TAPP2 adaptor binding to PtdIns(3,4)P2 in regulating insulin sensitivity defined by knock-in analysis. Biochem J 434: 265-274
45. Yao L, Kawakami Y, Kawakami T (1994) The pleckstrin homology domain of Bruton tyrosine kinase interacts with protein kinase C. Proc Natl Acad Sci USA 91: 9175-9179
46. Yin HL, Janmey PA (2003) Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 65: 761-789 (Pubitemid 38249176)
47. Yu JW, Mendrola JM, Audhya A, Singh S, Keleti D, DeWald DB, Murray D, Emr SD, Lemmon MA (2004) Genome-wide analysis of membrane targeting by S. cerevisiae pleckstrin homology domains. Mol Cell 13: 677-688 (Pubitemid 38368125)