CAPS and Munc13 utilize distinct PIP2-linked mechanisms to promote vesicle exocytosis

Molecular Biology of the Cell

Volumn 25, Issue 4, 2014, Pages 508-521

  Kabachinski, Greg ^a   Yamaga, Masaki ^a   Kielar Grevstad, D Michelle ^a   Bruinsma, Stephen ^a   Martin, Thomas F J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM BINDING PROTEIN; CAPS PROTEIN, RAT; ISOENZYME; NERVE PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE PHOSPHODIESTERASE; UNC13H2 PROTEIN, RAT;

AMINO ACID SEQUENCE; ANIMAL; CELL MEMBRANE; CHEMICAL STRUCTURE; CYTOPLASM; EXOCYTOSIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PC12 CELL LINE; RAT; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANSPORT AT THE CELLULAR LEVEL; TRANSPORT VESICLE; VIDEO MICROSCOPY;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; CALCIUM; CALCIUM-BINDING PROTEINS; CELL MEMBRANE; CYTOPLASM; EXOCYTOSIS; GENE EXPRESSION REGULATION; ISOENZYMES; MICROSCOPY, VIDEO; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; PC12 CELLS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHOINOSITIDE PHOSPHOLIPASE C; RATS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANSPORT VESICLES;

EID: 84894261797     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-11-0829     Document Type: Article

References (61)

1. Aikawa Y, Martin TF (2003). ARF6 regulates a plasma membrane pool of phosphatidylinositol(4,5)bisphosphate required for regulated exocytosis. J Cell Biol 162, 647-659.
2. Andrews-Zwilling YS, Kawabe H, Reim K, Varoqueaux F, Brose N (2006). Binding to Rab3A-interacting molecule RIM regulates the presynaptic recruitment of Munc13-1 and ubMunc13-2. J Biol Chem 281, 19720-19731.
3. Aoyagi K, Sugaya T, Umeda M, Yamamoto S, Terakawa S, Takahashi M (2005). The activation of exocytotic sites by the formation of phosphatidylinositol 4,5-bisphosphate microdomains at syntaxin clusters. J Biol Chem 280, 17346-17352.
4. Ashery U, Varoqueaux F, Voets T, Betz A, Thakur P, Koch H, Neher E, Brose N, Rettig J (2000). Munc13-1 acts as a priming factor for large dense-core vesicles in bovine chromaffin cells. EMBO J 19, 3586-3596.
5. Augustin I, Rosenmund C, Sudhof TC, Brose N (1999). Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 400, 457-461.
6. Bai J, Tucker WC, Chapman ER (2004). PIP2 increases the speed of response of synaptotagmin and steers its membrane-penetration activity toward the plasma membrane. Nat Struct Mol Biol 11, 36-44.
7. Basu J, Betz A, Brose N, Rosenmund C (2007). Munc13-1 C1 domain activation lowers the energy barrier for synaptic vesicle fusion. J Neurosci 27, 1200-1210.
8. Betz A, Ashery U, Rickmann M, Augustin I, Neher E, Sudhof TC, Rettig J, Brose N (1998). Munc13-1 is a presynaptic phorbol ester receptor that enhances neurotransmitter release. Neuron 21, 123-136.
9. Botelho RJ, Teruel M, Dierckman R, Anderson R, Wells A, York JD, Meyer T, Grinstein S (2000). Localized biphasic changes in phosphatidylinositol-4,5- bisphosphate at sites of phagocytosis. J Cell Biol 151, 1353-1368.
10. Costes SV, Daelemans D, Cho EH, Dobbin Z, Pavlakis G, Lockett S (2004). Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J 86, 3993-4003.
11. Daily NJ, Boswell KL, James DJ, Martin TF (2010). Novel interactions of CAPS (Ca2+-dependent activator protein for secretion) with the three neuronal SNARE proteins required for vesicle fusion. J Biol Chem 285, 35320-35329.
12. Di Paolo G, De Camilli P (2006). Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657.
13. Eberhard DA, Cooper CL, Low MG, Holz RW (1990). Evidence that the inositol phospholipids are necessary for exocytosis. Loss of inositol phospholipids and inhibition of secretion in permeabilized cells caused by a bacterial phospholipase C and removal of ATP. Biochem J 268, 15-25.
14. Flannagan RS, Jaumouille V, Grinstein S (2012). The cell biology of phagocytosis. Annu Rev Pathol 7, 61-98.
15. Grishanin RN, Klenchin VA, Loyet KM, Kowalchyk JA, Ann K, Martin TF (2002). Membrane association domains in Ca2+-dependent activator protein for secretion mediate plasma membrane and dense-core vesicle binding required for Ca2+-dependent exocytosis. J Biol Chem 277, 22025-22034.
16. Grishanin RN, Kowalchyk JA, Klenchin VA, Ann K, Earles CA, Chapman ER, Gerona RR, Martin TF (2004). CAPS acts at a prefusion step in dense-core vesicle exocytosis as a PIP2 binding protein. Neuron 43, 551-562.
17. Guan R, Dai H, Rizo J (2008). Binding of the Munc13-1 MUN domain to membrane-anchored SNARE complexes. Biochemistry 47, 1474-1481.
18. Hay JC, Fisette PL, Jenkins GH, Fukami K, Takenawa T, Anderson RA, Martin TF (1995). ATP-dependent inositide phosphorylation required for Ca(2+)-activated secretion. Nature 374, 173-177.
19. Hay JC, Martin TF (1993). Phosphatidylinositol transfer protein required for ATP-dependent priming of Ca(2+)-activated secretion. Nature 366, 572-575.
20. Henschel A, Buchholz F, Habermann B (2004). DEQOR: a web-based tool for the design and quality control of siRNAs. Nucleic Acids Res 32, W113-W120.
21. Holz RW, Hlubek MD, Sorensen SD, Fisher SK, Balla T, Ozaki S, Prestwich GD, Stuenkel EL, Bittner MA (2000). A pleckstrin homology domain specific for phosphatidylinositol 4, 5-bisphosphate (PtdIns-4,5-P2) and fused to green fluorescent protein identifies plasma membrane PtdIns-4,5-P2 as being important in exocytosis. J Biol Chem 275, 17878-17885.
22. Homma Y, Takenawa T, Emori Y, Sorimachi H, Suzuki K (1989). Tissue- and cell type-specific expression of mRNAs for four types of inositol phospholipid-specific phospholipase C. Biochem Biophys Res Commun 164, 406-412.
23. Hurley JH, Meyer T (2001). Subcellular targeting by membrane lipids. Curr Opin Cell Biol 13, 146-152.
24. Jahn R, Scheller RH (2006). SNAREs - engines for membrane fusion. Nat Rev Mol Cell Biol 7, 631-643.
25. James DJ, Khodthong C, Kowalchyk JA, Martin TF (2008). Phosphatidylinositol 4,5-bisphosphate regulates SNARE-dependent membrane fusion. J Cell Biol 182, 355-366.
26. Jockusch WJ, Speidel D, Sigler A, Sorensen JB, Varoqueaux F, Rhee JS, Brose N (2007). CAPS-1 and CAPS-2 are essential synaptic vesicle priming proteins. Cell 131, 796-808.
27. Kanemaru K, Nakahara M, Nakamura Y, Hashiguchi Y, Kouchi Z, Yamaguchi H, Oshima N, Kiyonari H, Fukami K (2010). Phospholipase C-eta2 is highly expressed in the habenula and retina. Gene Expr Patterns 10, 119-126.
28. Kasai H, Takahashi N, Tokumaru H (2012). Distinct initial SNARE configurations underlying the diversity of exocytosis. Physiol Rev 92, 1915-1964.
29. Khodthong C, Kabachinski G, James DJ, Martin TF (2011). Munc13 homology domain-1 in CAPS/UNC31 mediates SNARE binding required for priming vesicle exocytosis. Cell Metab 14, 254-263.
30. Kittler R, Heninger AK, Franke K, Habermann B, Buchholz F (2005). Production of endoribonuclease-prepared short interfering RNAs for gene silencing in mammalian cells. Nat Methods 2, 779-784.
31. Koch H, Hofmann K, Brose N (2000). Definition of Munc13-homology-domains and characterization of a novel ubiquitously expressed Munc13 isoform. Biochem J 349, 247-253.
32. Koch M, Holt M (2012). Coupling exo- and endocytosis: an essential role for PIP(2) at the synapse. Biochim Biophys Acta 1821, 1114-1132.
33. Kuo W, Herrick DZ, Cafiso DS (2011). Phosphatidylinositol 4,5-bisphosphate alters synaptotagmin 1 membrane docking and drives opposing bilayers closer together. Biochemistry 50, 2633-2641.
34. Lackner MR, Nurrish SJ, Kaplan JM (1999). Facilitation of synaptic transmission by EGL-30 Gqalpha and EGL-8 PLCbeta: DAG binding to UNC-13 is required to stimulate acetylcholine release. Neuron 24, 335-346.
35. Laux T, Fukami K, Thelen M, Golub T, Frey D, Caroni P (2000). GAP43, MARCKS, and CAP23 modulate PI(4,5)P(2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J Cell Biol 149, 1455-1472.
36. Lee SB, Varnai P, Balla A, Jalink K, Rhee SG, Balla T (2004). The pleckstrin homology domain of phosphoinositide-specific phospholipase Cdelta4 is not a critical determinant of the membrane localization of the enzyme. J Biol Chem 279, 24362-24371.
37. Li W, Ma C, Guan R, Xu Y, Tomchick DR, Rizo J (2011). The crystal structure of a Munc13 C-terminal module exhibits a remarkable similarity to vesicle tethering factors. Structure 19, 1443-1455.
38. Liu Y et al. (2010). Two distinct secretory vesicle-priming steps in adrenal chromaffin cells. J Cell Biol 190, 1067-1077.
39. Liu Y, Schirra C, Stevens DR, Matti U, Speidel D, Hof D, Bruns D, Brose N, Rettig J (2008). CAPS facilitates filling of the rapidly releasable pool of large dense-core vesicles. J Neurosci 28, 5594-5601.
40. Loyet KM, Kowalchyk JA, Chaudhary A, Chen J, Prestwich GD, Martin TF (1998). Specific binding of phosphatidylinositol 4,5-bisphosphate to calcium-dependent activator protein for secretion (CAPS), a potential phosphoinositide effector protein for regulated exocytosis. J Biol Chem 273, 8337-8343.
41. Lynch KL, Gerona RR, Kielar DM, Martens S, McMahon HT, Martin TF (2008). Synaptotagmin-1 utilizes membrane bending and SNARE binding to drive fusion pore expansion. Mol Biol Cell 19, 5093-5103.
42. Martin TF (2001). PI(4,5)P(2) regulation of surface membrane traffic. Curr Opin Cell Biol 13, 493-499.
43. Martin TF (2003). Tuning exocytosis for speed: fast and slow modes. Biochim Biophys Acta 1641, 157-165.
44. McLaughlin S, Murray D (2005). Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438, 605-611.
45. Milosevic I, Sorensen JB, Lang T, Krauss M, Nagy G, Haucke V, Jahn R, Neher E (2005). Plasmalemmal phosphatidylinositol-4,5-bisphosphate level regulates the releasable vesicle pool size in chromaffin cells. J Neurosci 25, 2557-2565.
46. Nakahara M, Shimozawa M, Nakamura Y, Irino Y, Morita M, Kudo Y, Fukami K (2005). A novel phospholipase C, PLC(eta)2, is a neuron-specific isozyme. J Biol Chem 280, 29128-29134.
47. Oancea E, Meyer T (1998). Protein kinase C as a molecular machine for decoding calcium and diacylglycerol signals. Cell 95, 307-318.
48. Olsen HL et al. (2003). Phosphatidylinositol 4-kinase serves as a metabolic sensor and regulates priming of secretory granules in pancreatic beta cells. Proc Natl Acad Sci USA 100, 5187-5192.
49. Pei J, Ma C, Rizo J, Grishin NV (2009). Remote homology between Munc13 MUN domain and vesicle tethering complexes. J Mol Biol 391, 509-517.
50. Rettig J, Neher E (2002). Emerging roles of presynaptic proteins in Ca++-triggered exocytosis. Science 298, 781-785.
51. Rhee JS et al. (2002). Beta phorbol ester- and diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108, 121-133.
52. Rizo J, Rosenmund C (2008). Synaptic vesicle fusion. Nat Struct Mol Biol 15, 665-674.
53. Rosenmund C, Sigler A, Augustin I, Reim K, Brose N, Rhee JS (2002). Differential control of vesicle priming and short-term plasticity by Munc13 isoforms. Neuron 33, 411-424.
54. Schramp M, Hedman A, Li W, Tan X, Anderson R (2012). PIP kinases from the cell membrane to the nucleus. Subcell Biochem 58, 25-59.
55. Shin OH et al. (2010). Munc13 C2B domain is an activity-dependent Ca2+ regulator of synaptic exocytosis. Nat Struct Mol Biol 17, 280-288.
56. Suh BC, Hille B (2008). PIP2 is a necessary cofactor for ion channel function: how and why. Annu Rev Biophys 37, 175-195.
57. van den Bogaart G, Meyenberg K, Diederichsen U, Jahn R (2012). Phosphatidylinositol 4,5-bisphosphate increases Ca2+ affinity of synaptotagmin-1 by 40-fold. J Biol Chem 287, 16447-16453.
58. van den Bogaart G et al. (2011). Membrane protein sequestering by ionic protein-lipid interactions. Nature 479, 552-555.
59. Varnai P, Thyagarajan B, Rohacs T, Balla T (2006). Rapidly inducible changes in phosphatidylinositol 4,5-bisphosphate levels influence multiple regulatory functions of the lipid in intact living cells. J Cell Biol 175, 377-382.
60. Walent JH, Porter BW, Martin TF (1992). A novel 145 kd brain cytosolic protein reconstitutes Ca(2+)-regulated secretion in permeable neuroendocrine cells. Cell 70, 765-775.
61. Zhang L, Mao YS, Janmey PA, Yin HL (2012). Phosphatidylinositol 4, 5 bisphosphate and the actin cytoskeleton. Subcell Biochem 59, 177-215.