OCRL1 engages with the F-BAR protein pacsin 2 to promote biogenesis of membrane-trafficking intermediates

Molecular Biology of the Cell

Volumn 27, Issue 1, 2016, Pages 90-107

  Billcliff, Peter G ^a   Noakes, Christopher J ^a,c   Mehta, Zenobia B ^a,b   Yan, Guanhua ^a   Mak, LokHang ^b   Woscholski, Rudiger ^b   Lowe, Martin ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c Champions Oncology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; F ACTIN; PACSIN 2; PHOSPHATASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN; PROTEIN OCRL1; PROTEIN KINASE C; SOMATOMEDIN B RECEPTOR; UNCLASSIFIED DRUG; INOSITOL POLYPHOSPHATE 5 PHOSPHATASE; NERVE PROTEIN; OCRL PROTEIN, HUMAN; PACSIN2 PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL; SCRN1 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ACTIN FILAMENT; ARTICLE; BIOGENESIS; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HYDROLYSIS; LOWE SYNDROME; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TRANS GOLGI NETWORK; ANIMAL; BIOSYNTHESIS; COS CELL LINE; ENDOCYTOSIS; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; NEPHROLITHIASIS; PATHOLOGY; PROTEIN TRANSPORT; X CHROMOSOME LINKED DISORDER;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; COS CELLS; ENDOCYTOSIS; ENDOSOMES; GENETIC DISEASES, X-LINKED; HEK293 CELLS; HELA CELLS; HUMANS; INOSITOL POLYPHOSPHATE 5-PHOSPHATASES; NEPHROLITHIASIS; NERVE TISSUE PROTEINS; OCULOCEREBRORENAL SYNDROME; PHOSPHATIDYLINOSITOLS; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN TRANSPORT; RECEPTOR, IGF TYPE 2; TRANS-GOLGI NETWORK;

EID: 84954348712     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E15-06-0329     Document Type: Article

References (73)

1. Anitei M, Hoflack B (2011). Bridging membrane and cytoskeleton dynamics in the secretory and endocytic pathways. Nat Cell Biol 14, 11-19.
2. Anitei M, Stange C, Parshina I, Baust T, Schenck A, Raposo G, Kirchhausen T, Hoflack B (2010). Protein complexes containing CYFIP/Sra/PIR121 coordinate Arf1 and Rac1 signalling during clathrin-AP-1-coated carrier biogenesis at the TGN. Nat Cell Biol 12, 330-340.
3. Arighi CN, Hartnell LM, Aguilar RC, Haft CR, Bonifacino JS (2004). Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J Cell Biol 165, 123-133.
4. Attree O, Olivos IM, Okabe I, Bailey LC, Nelson DL, Lewis RA, McInnes RR, Nussbaum RL (1992). The Lowe's oculocerebrorenal syndrome gene encodes a protein highly homologous to inositol polyphosphate-5-phosphatase. Nature 358, 239-242.
5. Balla T (2013). Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol Rev 93, 1019-1137.
6. Ben El Kadhi K, Roubinet C, Solinet S, Emery G, Carreno S (2011). The inositol 5-phosphatase dOCRL controls PI (4, 5) P2 homeostasis and is necessary for cytokinesis. Curr Biol 21, 1074-1079.
7. Billcliff PG, Lowe M (2014). Inositol lipid phosphatases in membrane trafficking and human disease. Biochem J 461, 159-175.
8. Bohdanowicz M, Balkin DM, De Camilli P, Grinstein S (2012). Recruitment of OCRL and Inpp5B to phagosomes by Rab5 and APPL1 depletes phosphoinositides and attenuates Akt signaling. Mol Biol Cell 23, 176-187.
9. Borner GH, Hein MY, Hirst J, Edgar JR, Mann M, Robinson MS (2014). Fractionation profiling: a fast and versatile approach for mapping vesicle proteomes and protein-protein interactions. Mol Biol Cell 25, 3178-3194.
10. Carlton J, Bujny M, Peter BJ, Oorschot VM, Rutherford A, Mellor H, Klumperman J, McMahon HT, Cullen PJ (2004). Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high-curvature membranes and 3-phosphoinositides. Curr Biol 14, 1791-1800.
11. Chang-Ileto B, Frere SG, Chan RB, Voronov SV, Roux A, Di Paolo G (2011). Synaptojanin 1-mediated PI (4, 5) P2 hydrolysis is modulated by membrane curvature and facilitates membrane fission. Dev Cell 20, 206-218.
12. Choudhury R, Diao A, Zhang F, Eisenberg E, Saint-Pol A, Williams C, Konstantakopoulos A, Lucocq J, Johannes L, Rabouille C, et al. (2005). Lowe syndrome protein OCRL1 interacts with clathrin and regulates protein trafficking between endosomes and the trans-Golgi network. Mol Biol Cell 16, 3467-3479.
13. Choudhury R, Noakes CJ, McKenzie E, Kox C, Lowe M (2009). Differential clathrin binding and subcellular localization of OCRL1 splice isoforms. J Biol Chem 284, 9965-9973.
14. Coon BG, Hernandez V, Madhivanan K, Mukherjee D, Hanna CB, Barinaga-Rementeria Ramirez I, Lowe M, Beales PL, Aguilar RC (2012). The Lowe syndrome protein OCRL1 is involved in primary cilia assembly. Hum Mol Genet 21, 1835-1847.
15. Coon BG, Mukherjee D, Hanna CB, Riese DJ 2nd, Lowe M, Aguilar RC (2009). Lowe syndrome patient fibroblasts display Ocrl1-specific cell migration defects that cannot be rescued by the homologous Inpp5b phosphatase. Hum Mol Genet 18, 4478-4491.
16. Cui S, Guerriero CJ, Szalinski CM, Kinlough CL, Hughey R P, Weisz OA (2010). OCRL1 function in renal epithelial membrane traffic. Am J Physiol Renal Physiol 298, F335-F345.
17. Dambournet D, Machicoane M, Chesneau L, Sachse M, Rocancourt M, El Marjou A, Formstecher E, Salomon R, Goud B, Echard A (2011). Rab35 GTPase and OCRL phosphatase remodel lipids and F-actin for successful cytokinesis. Nat Cell Biol 13, 981-988.
18. de Kreuk BJ, Anthony EC, Geerts D, Hordijk PL (2012). The F-BAR protein PACSIN2 regulates epidermal growth factor receptor internalization. J Biol Chem 287, 43438-43453.
19. de Kreuk BJ, Nethe M, Fernandez-Borja M, Anthony EC, Hensbergen PJ, Deelder AM, Plomann M, Hordijk PL (2011). The F-BAR domain protein PACSIN2 associates with Rac1 and regulates cell spreading and migration. J Cell Sci 124, 2375-2388.
20. Derivery E, Sousa C, Gautier JJ, Lombard B, Loew D, Gautreau A (2009). The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. Dev Cell 17, 712-723.
21. Diao A, Rahman D, Pappin DJ, Lucocq J, Lowe M (2003). The coiled-coil membrane protein golgin-84 is a novel rab effector required for Golgi ribbon formation. J Cell Biol 160, 201-212.
22. Di Paolo G, De Camilli P (2006). Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657.
23. Duleh SN, Welch MD (2010). WASH and the Arp2/3 complex regulate endosome shape and trafficking. Cytoskeleton (Hoboken) 67, 193-206.
24. Erdmann KS, Mao Y, McCrea HJ, Zoncu R, Lee S, Paradise S, Modregger J, Biemesderfer D, Toomre D, De Camilli P (2007). A role of the Lowe syndrome protein OCRL in early steps of the endocytic pathway. Dev Cell 13, 377-390.
25. Giridharan SS, Cai B, Vitale N, Naslavsky N, Caplan S (2013). Cooperation of MICAL-L1, Syndapin2 and phosphatidic acid in tubular recycling endosome biogenesis. Mol Biol Cell 24, 1776-1790.
26. Godi A, Pertile P, Meyers R, Marra P, Di Tullio G, Iurisci C, Luini A, Corda D, De Matteis MA (1999). ARF mediates recruitment of PtdIns-4-OH kinasebeta and stimulates synthesis of PtdIns (4, 5) P2 on the Golgi complex. Nat Cell Biol 1, 280-287.
27. Gomez TS, Billadeau DD (2009). A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev Cell 17, 699-711.
28. Grieve AG, Daniels RD, Sanchez-Heras E, Hayes MJ, Moss SE, Matter K, Lowe M, Levine TP (2011). Lowe syndrome protein OCRL1 supports maturation of polarized epithelial cells. PLoS One 6, e24044.
29. Hansen CG, Howard G, Nichols BJ (2011). Pacsin 2 is recruited to caveolae and functions in caveolar biogenesis. J Cell Sci 124, 2777-2785.
30. Harterink M, Port F, Lorenowicz MJ, McGough IJ, Silhankova M, Betist MC, van Weering JR, van Heesbeen RG, Middelkoop TC, Basler K, et al. (2011). A SNX3-dependent retromer pathway mediates retrograde transport of the Wnt sorting receptor Wntless and is required for Wnt secretion. Nat Cell Biol 13, 914-923.
31. Hirst J, Borner GH, Antrobus R, Peden AA, Hodson NA, Sahlender DA, Robinson MS (2012). Distinct and overlapping roles for AP-1 and GGAs revealed by the "knocksideways" system. Curr Biol 22, 1711-1716.
32. Hoopes RR Jr, Shrimpton AE, Knohl SJ, Hueber P, Hoppe B, Matyus J, Simckes A, Tasic V, Toenshoff B, Suchy SF, et al. (2005). Dent disease with mutations in OCRL1. Am J Hum Genet 76, 260-267.
33. Hou X, Hagemann N, Schoebel S, Blankenfeldt W, Goody RS, Erdmann KS, Itzen A (2011). A structural basis for Lowe syndrome caused by mutations in the Rab-binding domain of OCRL1. EMBO J 30, 1659-1670.
34. Hyvola N, Diao A, McKenzie E, Skippen A, Cockcroft S, Lowe M (2006). Membrane targeting and activation of the Lowe syndrome protein OCRL1 by rab GTPases. EMBO J 25, 3750-3761.
35. Kessels MM, Dong J, Leibig W, Westermann P, Qualmann B (2006). Complexes of syndapin II with dynamin II promote vesicle formation at the trans-Golgi network. J Cell Sci 119, 1504-1516.
36. Kessels MM, Qualmann B (2004). The syndapin protein family: linking membrane trafficking with the cytoskeleton. J Cell Sci 117, 3077-3086.
37. Kostan J, Salzer U, Orlova A, Toro I, Hodnik V, Senju Y, Zou J, Schreiner C, Steiner J, Merilainen J, et al. (2014). Direct interaction of actin filaments with F-BAR protein pacsin2. EMBO Rep 15, 1154-1162.
38. Kuhbacher A, Dambournet D, Echard A, Cossart P, Pizarro-Cerda J (2012). Phosphatidylinositol 5-phosphatase oculocerebrorenal syndrome of Lowe protein (OCRL) controls actin dynamics during early steps of Listeria monocytogenes infection. J Biol Chem 287, 13128-13136.
39. Luo N, West CC, Murga-Zamalloa CA, Sun L, Anderson RM, Wells CD, Weinreb RN, Travers JB, Khanna H, Sun Y (2012). OCRL localizes to the primary cilium: a new role for cilia in Lowe syndrome. Hum Mol Genet 21, 3333-3344.
40. Mak LH, Vilar R, Woscholski R (2011). Characterisation of the PTEN inhibitor VO-OHpic. J Chem Biol 3, 157-163.
41. Marion S, Mazzolini J, Herit F, Bourdoncle P, Kambou-Pene N, Hailfinger S, Sachse M, Ruland J, Benmerah A, Echard A, et al. (2012). The NF-kappaB signaling protein Bcl10 regulates actin dynamics by controlling AP1 and OCRL-bearing vesicles. Dev Cell 23, 954-967.
42. Maxfield FR, McGraw TE (2004). Endocytic recycling. Nat Rev Mol Cell Biol 5, 121-132.
43. McCrea HJ, De Camilli P (2009). Mutations in phosphoinositide metabolizing enzymes and human disease. Physiology (Bethesda) 24, 8-16.
44. McMahon HT, Boucrot E (2011). Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12, 517-533.
45. Mehta ZB, Pietka G, Lowe M (2014). The cellular and physiological functions of the Lowe syndrome protein OCRL1. Traffic 15, 471-487.
46. Miki H, Miura K, Takenawa T (1996). N-WASP, a novel actin-depolymerizing protein, regulates the cortical cytoskeletal rearrangement in a PIP2-dependent manner downstream of tyrosine kinases. EMBO J 15, 5326-5335.
47. Nandez R, Balkin DM, Messa M, Liang L, Paradise S, Czapla H, Hein MY, Duncan JS, Mann M, De Camilli P (2014). A role of OCRL in clathrincoated pit dynamics and uncoating revealed by studies of Lowe syndrome cells. Elife 3, e02975.
48. Noakes CJ, Lee G, Lowe M (2011). The PH domain proteins IPIP27A and B link OCRL1 to receptor recycling in the endocytic pathway. Mol Biol Cell 22, 606-623.
49. Pirruccello M, De Camilli P (2012). Inositol 5-phosphatases: insights from the Lowe syndrome protein OCRL. Trends Biochem Sci 37, 134-143.
50. Pirruccello M, Swan LE, Folta-Stogniew E, De Camilli P (2011). Recognition of the F&H motif by the Lowe syndrome protein OCRL. Nat Struct Mol Biol 18, 789-795.
51. Qualmann B, Koch D, Kessels MM (2011). Let's go bananas: revisiting the endocytic BAR code. EMBO J 30, 3501-3515.
52. Quan A, Robinson PJ (2014). Syndapin-a membrane remodelling and endocytic F-BAR protein. FEBS J 280, 5198-5212.
53. Rao Y, Ma Q, Vahedi-Faridi A, Sundborger A, Pechstein A, Puchkov D, Luo L, Shupliakov O, Saenger W, Haucke V (2010). Molecular basis for SH3 domain regulation of F-BAR-mediated membrane deformation. Proc Natl Acad Sci USA 107, 8213-8218.
54. Rbaibi Y, Cui S, Mo D, Carattino M, Rohatgi R, Satlin LM, Szalinski CM, Swanhart LM, Folsch H, Hukriede NA, Weisz OA (2012). OCRL1 modulates cilia length in renal epithelial cells. Traffic 13, 1295-1305.
55. Santiago-Tirado FH, Bretscher A (2011). Membrane-trafficking sorting hubs: cooperation between PI4P and small GTPases at the trans-Golgi network. Trends Cell Biol 21, 515-525.
56. Sasaki T, Takasuga S, Sasaki J, Kofuji S, Eguchi S, Yamazaki M, Suzuki A (2009). Mammalian phosphoinositide kinases and phosphatases. Prog Lipid Res 48, 307-343.
57. Seaman MN (2004). Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J Cell Biol 165, 111-122.
58. Senju Y, Itoh Y, Takano K, Hamada S, Suetsugu S (2011). Essential role of PACSIN2/syndapin-II in caveolae membrane sculpting. J Cell Sci 124, 2032-2040.
59. Shi A, Liu O, Koenig S, Banerjee R, Chen CC, Eimer S, Grant BD (2012). RAB-10-GTPase-mediated regulation of endosomal phosphatidylinositol-4, 5-bisphosphate. Proc Natl Acad Sci USA 109, E2306-E2315.
60. Shimada A, Takano K, Shirouzu M, Hanawa-Suetsugu K, Terada T, Toyooka K, Umehara T, Yamamoto M, Yokoyama S, Suetsugu S (2010). Mapping of the basic amino-acid residues responsible for tubulation and cellular protrusion by the EFC/F-BAR domain of pacsin2/Syndapin II. FEBS Lett 584, 1111-1118.
61. Smith CM, Chircop M (2012). Clathrin-mediated endocytic proteins are involved in regulating mitotic progression and completion. Traffic 13, 1628-1641.
62. Suchy SF, Nussbaum RL (2002). The deficiency of PIP2 5-phosphatase in Lowe syndrome affects actin polymerization. Am J Hum Genet 71, 1420-1427.
63. Sun Y, Hedman AC, Tan X, Schill NJ, Anderson RA (2013). Endosomal type Igamma PIP 5-kinase controls EGF receptor lysosomal sorting. Dev Cell 25, 144-155.
64. Swan LE, Tomasini L, Pirruccello M, Lunardi J, De Camilli P (2010). Two closely related endocytic proteins that share a common OCRL-binding motif with APPL1. Proc Natl Acad Sci USA 107, 3511-3516.
65. Takeda T, Robinson IM, Savoian MM, Griffiths JR, Whetton AD, McMahon HT, Glover DM (2013). Drosophila F-BAR protein Syndapin contributes to coupling the plasma membrane and contractile ring in cytokinesis. Open Biol 3, 130081.
66. Taylor MJ, Perrais D, Merrifield CJ (2011). A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol 9, e1000604.
67. Temkin P, Lauffer B, Jager S, Cimermancic P, Krogan NJ, von Zastrow M (2011). SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Nat Cell Biol 13, 715-721.
68. Ungewickell AJ, Majerus PW (1999). Increased levels of plasma lysosomal enzymes in patients with Lowe syndrome. Proc Natl Acad Sci USA 96, 13342-13344.
69. van Rahden VA, Brand K, Najm J, Heeren J, Pfeffer SR, Braulke T, Kutsche K (2012). The 5-phosphatase OCRL mediates retrograde transport of the mannose 6-phosphate receptor by regulating a Rac1-cofilin signalling module. Hum Mol Genet 21, 5019-5038.
70. Vicinanza M, D'Angelo G, Di Campli A, De Matteis MA (2008). Phosphoinositides as regulators of membrane trafficking in health and disease. Cell Mol Life Sci 65, 2833-2841.
71. Vicinanza M, Di Campli A, Polishchuk E, Santoro M, Di Tullio G, Godi A, Levtchenko E, De Leo MG, Polishchuk R, Sandoval L, et al. (2011). OCRL controls trafficking through early endosomes via PtdIns4, 5P (2)-dependent regulation of endosomal actin. EMBO J 30, 4970-4985.
72. Waguri S, Dewitte F, Le Borgne R, Rouille Y, Uchiyama Y, Dubremetz JF, Hoflack B (2003). Visualization of TGN to endosome trafficking through fluorescently labeled MPR and AP-1 in living cells. Mol Biol Cell 14, 142-155.
73. Watt SA, Kular G, Fleming IN, Downes C P, Lucocq JM (2002). Subcellular localization of phosphatidylinositol 4, 5-bisphosphate using the pleckstrin homology domain of phospholipase C delta1. Biochem J 363, 657-666.