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Role of Phospholipase D-Derived Phosphatidic Acid in Regulated Exocytosis and Neurological Disease

  • Emeline Tanguy
  • Qili Wang
  • Nicolas VitaleEmail author
Part of the Handbook of Experimental Pharmacology book series


Lipids play a vital role in numerous cellular functions starting from a structural role as major constituents of membranes to acting as signaling intracellular or extracellular entities. Accordingly, it has been known for decades that lipids, especially those coming from diet, are important to maintain normal physiological functions and good health. On the other side, the exact molecular nature of these beneficial or deleterious lipids, as well as their precise mode of action, is only starting to be unraveled. This recent improvement in our knowledge is largely resulting from novel pharmacological, molecular, cellular, and genetic tools to study lipids in vitro and in vivo. Among these important lipids, phosphatidic acid plays a unique and central role in a great variety of cellular functions. This review will focus on the proposed functions of phosphatidic acid generated by phospholipase D in the last steps of regulated exocytosis with a specific emphasis on hormonal and neurotransmitter release and its potential impact on different neurological diseases.


Exocytosis Lipid Neuroendocrine Neuron Phosphatidic acid Phospholipase D 


  1. Ahn BH, Rhim H, Kim SY, Sung YM, Lee MY, Choi JY, Wolozin B, Chang JS, Lee YH, Kwon TK, Chung KC, Yoon SH, Hahn SJ, Kim MS, Jo YH, Min DS (2002) alpha-Synuclein interacts with phospholipase D isozymes and inhibits pervanadate-induced phospholipase D activation in human embryonic kidney-293 cells. J Biol Chem 277(14):12334–12342Google Scholar
  2. Ammar MR, Humeau Y, Hanauer A, Nieswandt B, Bader MF, Vitale N (2013) The Coffin-Lowry syndrome-associated protein RSK2 regulates neurite outgrowth through phosphorylation of phospholipase D1 (PLD1) and synthesis of phosphatidic acid. J Neurosci 33(50):19470–19479Google Scholar
  3. Ammar MR, Thahouly T, Hanauer A, Stegner D, Nieswandt B, Vitale N (2015) PLD1 participates in BDNF-induced signalling in cortical neurons. Sci Rep 5:14778Google Scholar
  4. Andreyev AY, Fahy E, Guan Z, Kelly S, Li X, McDonald JG, Milne S, Myers D, Park H, Ryan A, Thompson BM, Wang E, Zhao Y, Brown HA, Merrill AH, Raetz CR, Russell DW, Subramaniam S, Dennis EA (2010) Subcellular organelle lipidomics in TLR-4-activated macrophages. J Lipid Res 51(9):2785–2797Google Scholar
  5. Audebert S, Navarro C, Nourry C, Chasserot-Golaz S, Lécine P, Bellaiche Y, Dupont JL, Premont RT, Sempéré C, Strub JM, Van Dorsselaer A, Vitale N, Borg JP (2004) Mammalian Scribble forms a tight complex with the betaPIX exchange factor. Curr Biol 14(11):987–995Google Scholar
  6. Bader MF, Holz RW, Kumakura K, Vitale N (2002) Exocytosis: the chromaffin cell as a model system. Ann N Y Acad Sci 971:178–183Google Scholar
  7. Béglé A, Tryoen-Tóth P, de Barry J, Bader MF, Vitale N (2009) ARF6 regulates the synthesis of fusogenic lipids for calcium-regulated exocytosis in neuroendocrine cells. J Biol Chem 284(8):4836–4845Google Scholar
  8. Bhattacharya M, Babwah AV, Godin C, Anborgh PH, Dale LB, Poulter MO, Ferguson SS (2004) Ral and phospholipase D2-dependent pathway for constitutive metabotropic glutamate receptor endocytosis. J Neurosci 24(40):8752–8761Google Scholar
  9. Boggs JM (1987) Lipid intermolecular hydrogen bonding: influence on structural organization and membrane function. Biochim Biophys Acta 906(3):353–404Google Scholar
  10. Bullen HE, Jia Y, Yamaryo-Botté Y, Bisio H, Zhang O, Jemelin NK, Marq JB, Carruthers V, Botté CY, Soldati-Favre D (2016) Phosphatidic acid-mediated signaling regulates microneme secretion in toxoplasma. Cell Host Microbe 19(3):349–360Google Scholar
  11. Burgess TL, Kelly RB (1987) Constitutive and regulated secretion of proteins. Annu Rev Cell Biol 3:243–293Google Scholar
  12. Caumont AS, Galas MC, Vitale N, Aunis D, Bader MF (1998) Regulated exocytosis in chromaffin cells. Translocation of ARF6 stimulates a plasma membrane-associated phospholipase D. J Biol Chem 273(3):1373–1379Google Scholar
  13. Chernomordik LV, Kozlov MM (2008) Mechanics of membrane fusion. Nat Struct Mol Biol 15(7):675–683Google Scholar
  14. Choi WS, Kim YM, Combs C, Frohman MA, Beaven MA (2002) Phospholipases D1and D2 regulate different phases of exocytosis in mast cells. J Immunol 168(11):5682–5689Google Scholar
  15. Corrotte M, Chasserot-Golaz S, Huang P, Du G, Ktistakis NT, Frohman MA, Vitale N, Bader MF, Grant NJ (2006) Dynamics and function of phospholipase D and phosphatidic acid during phagocytosis. Traffic 7(3):365–377Google Scholar
  16. Demel RA, Yin CC, Lin BZ, Hauser H (1992) Monolayer characteristics and thermal behaviour of phosphatidic acids. Chem Phys Lipids 60:209–223Google Scholar
  17. Disse J, Vitale N, Bader MF, Gerke V (2009) Phospholipase D1 is specifically required for regulated secretion of von Willebrand factor from endothelial cells. Blood 113:973–980Google Scholar
  18. Du G, Altshuller YM, Vitale N, Huang P, Chasserot-Golaz S, Morris AJ, Bader MF, Frohman MA (2003) Regulation of phospholipase D1 subcellular cycling through coordination of multiple membrane association motifs. J Cell Biol 162(2):305–315Google Scholar
  19. Escribá PV (2017) Membrane-lipid therapy: a historical perspective of membrane-targeted therapies – from lipid bilayer structure to the pathophysiological regulation of cells. Biochim Biophys Acta 1859(9 PtB):1493–1506Google Scholar
  20. Frohman MA (2015) The phospholipase D superfamily as therapeutic targets. Trends Pharmacol Sci 36(3):137–144Google Scholar
  21. Fulop T, Smith C (2006) Physiological stimulation regulates the exocytic mode through calcium activation of protein kinase C in mouse chromaffin cells. Biochem J 399(1):111–119Google Scholar
  22. Garidel P, Johann C, Blume A (1997) Nonideal mixing and phase separation in phosphatidylcholine-phosphatidic acid mixtures as a function of acyl chain length and pH. Biophys J 72(5):2196–2210Google Scholar
  23. Gasman S, Vitale N (2017) Lipid remodelling in neuroendocrine secretion. Biol Cell 109(11):381–390Google Scholar
  24. Grodnitzky JA, Syed N, Kimber MJ, Day TA, Donaldson JG, Hsu WH (2007) Somatostatin receptors signal through EFA6A-ARF6 to activate phospholipase D in clonal beta-cells. J Biol Chem 282(18):13410–13418Google Scholar
  25. Guerri C, Renau-Piqueras J (1997) Alcohol, astroglia, and brain development. Mol Neurobiol 15(1):65–81Google Scholar
  26. Guizzetti M, Catlin M, Costa LG (1997) The effects of ethanol on glial cell proliferation: relevanceto the fetal alcohol syndrome. Front Biosci 2:e93–e98Google Scholar
  27. Huang P, Altshuller YM, Hou JC, Pessin JE, Frohman MA (2005) Insulin-stimulated plasma membrane fusion of Glut4 glucose transporter-containing vesicles is regulated by phospholipase D1. Mol Biol Cell 16(6):2614–2623Google Scholar
  28. Hughes WE, Elgundi Z, Huang P, Frohman MA, Biden TJ (2004) Phospholipase D1 regulates secretagogue-stimulated insulin release in pancreatic p-cells. J Biol Chem 279:27534–27541Google Scholar
  29. Humeau Y, Vitale N, Chasserot-Golaz S, Dupont JL, Du G, Frohman MA, Bader MF, Poulain B (2001) A role for phospholipase D1 in neurotransmitter release. Proc Natl Acad Sci U S A 98(26):15300–15305Google Scholar
  30. Humeau Y, Gambino F, Chelly J, Vitale N (2009) X-linked mental retardation: focus on synaptic function and plasticity. J Neurochem 109(1):1–14Google Scholar
  31. Iversen L, Mathiasen S, Larsen JB, Stamou D (2015) Membrane curvature bends the laws of physicsand chemistry. Nat Chem Biol 11(11):822–825Google Scholar
  32. Jahn R, Fasshauer D (2012) Molecular machines governing exocytosis of synaptic vesicles. Nature 490(7419):201–207Google Scholar
  33. Jang HJ, Yang YR, Kim JK, Choi JH, Seo YK, Lee YH, Lee JE, Ryu SH, Suh PG (2013) Phospholipase C-γ1 involved in brain disorders. Adv Biol Regul 53(1):51–62Google Scholar
  34. Jenco JM, Rawlingson A, Daniels B, Morris AJ (1998) Regulation of phospholipase D2: selective inhibition of mammalian phospholipase D isoenzymes by alpha- and beta-synucleins. Biochemistry 37(14):4901–4909Google Scholar
  35. Jenkins GM, Frohman MA (2005) Phospholipase D: a lipid centric review. Cell Mol Life Sci 62(19–20):2305–2316Google Scholar
  36. Jin JK, Kim NH, Min DS, Kim JI, Choi JK, Jeong BH, Choi SI, Choi EK, Carp RI, Kim YS (2005) Increased expression of phospholipase D1 in the brains of scrapie-infected mice. J Neurochem 92(3):452–461Google Scholar
  37. Jones DH, Morris JB, Morgan CP, Kondo H, Irvine RF, Cockcroft S (2000) Type I phosphatidylinositol 4-phosphate 5-kinase directly interacts with ADP-ribosylation factor 1 and is responsible for phosphatidylinositol 4,5-bisphosphate synthesis in the golgi compartment. J Biol Chem 275(18):13962–13966Google Scholar
  38. Jouhet J (2013) Importance of the hexagonal lipid phase in biological membrane organization. Front Plant Sci 4:494Google Scholar
  39. Jung AG, Labarrera C, Jansen AM, Qvortrup K, Wild K, Kjaerulff O (2010) A mutational analysis of the endophilin-A N-BAR domain performed in living flies. PLoS One 5:e9492Google Scholar
  40. Kanfer JN, Singh IN, Pettegrew JW, McCartney DG, Sorrentino G (1996) Phospholipid metabolism in Alzheimer’s disease and in a human cholinergic cell. J Lipid Mediat Cell Signal 14(1–3):361–363Google Scholar
  41. Kassas N, Tanguy E, Thahouly T, Fouillen L, Heintz D, Chasserot-Golaz S, Bader MF, Grant NJ, Vitale N (2017) Comparative characterization of phosphatidic acid sensors and their localization during frustrated phagocytosis. J Biol Chem 292(10):4266–4279Google Scholar
  42. Kim J, Min G, Bae YS, Min DS (2004a) Phospholipase D is involved in oxidative stress-induced migration of vascular smooth muscle cells via tyrosine phosphorylation and protein kinase C. Exp Mol Med 36(2):103–109Google Scholar
  43. Kim SY, Ahn BH, Min KJ, Lee YH, Joe EH, Min DS (2004b) Phospholipase D isozymes mediate epigallocatechin gallate-induced cyclooxygenase-2 expression in astrocyte cells. J Biol Chem 279(37):38125–38133Google Scholar
  44. Kim SY, Min DS, Choi JS, Choi YS, Park HJ, Sung KW, Kim J, Lee MY (2004c) Differential expression of phospholipase D isozymes in the hippocampus following kainic acid-induced seizures. J Neuropathol Exp Neurol 63:812–820Google Scholar
  45. Kim M, Moon C, Kim H, Shin MK, Min do S, Shin T (2010) Developmental levels of phospholipase D isozymes in the brain of developing rats. Acta Histochem 112(1):81–91Google Scholar
  46. Klein J (2005) Functions and pathophysiological roles of phospholipase D in the brain. J Neurochem 94(6):1473–1487Google Scholar
  47. Klein J, Holler T, Cappel E, Köppen A, Löffelholz K (1993) Release of choline from rat brain under hypoxia: contribution from phospholipase A2 but not from phospholipase D. Brain Res 630(1–2):337–340Google Scholar
  48. Kooijman EE, Chupin V, Fuller NL, Kozlov MM, de Kruijff B, Burger KN, Rand PR (2005) Spontaneous curvature of phosphatidic acid and lysophosphatidic acid. Biochemistry 44(6):2097–2102Google Scholar
  49. Kozlovsky Y, Chernomordik LV, Kozlov MM (2002) Lipid intermediates in membrane fusion: formation, structure, and decay of hemifusion diaphragm. Biophys J 83(5):2634–2651Google Scholar
  50. Lalli G, Hall A (2005) Ral GTPases regulate neurite branching through GAP-43 and the exocyst complex. J Cell Biol 171(5):857–869Google Scholar
  51. Lam IP, Siu FK, Chu JY, Chow BK (2008) Multiple actions of secretin in the human body. Int Rev Cytol 265:159–190Google Scholar
  52. Lauwers E, Goodchild R, Verstreken P (2016) Membrane lipids in presynaptic function and disease. Neuron 90(1):11–25Google Scholar
  53. Lee MY, Kim SY, Min DS, Choi YS, Shin SL, Chun MH, Lee SB, Kim MS, Jo YH (2000) Upregulation of phospholipase D in astrocytes in response to transient forebrain ischemia. Glia 30(3):311–317Google Scholar
  54. Leung DW (2001) The structure and functions of human lysophosphatidic acid acyltransferases. Front Biosci 6(1):D944–D953Google Scholar
  55. Lewis KT, Maddipati KR, Taatjes DJ, Jena BP (2014) Neuronal porosome lipidome. J Cell MolMed 18(10):1927–1937Google Scholar
  56. Liu Y, Zhang YW, Wang X, Zhang H, You X, Liao FF, Xu H (2009) Intracellular trafficking of presenilin 1 is regulated by beta-amyloid precursor protein and phospholipase D1. J Biol Chem 284(18):12145–12152Google Scholar
  57. Ljubicic S, Bezzi P, Vitale N, Regazzi R (2009) The GTPase RalA regulates different steps of the secretory process in pancreatic beta-cells. PLoS One 4(11):e7770Google Scholar
  58. Lopez JA, Brennan AJ, Whisstock JC, Voskoboinik I, Trapani JA (2012) Protecting a serial killer: pathways for perforin trafficking and self-defence ensure sequential target cell death. Trends Immunol 33(8):406–412Google Scholar
  59. Lou X, Kim J, Hawk BJ, Shin YK (2017) α-Synuclein may cross-bridge v-SNARE and acidic phospholipids to facilitate SNARE-dependent vesicle docking. Biochem J 474(12):2039–2049Google Scholar
  60. Martens S (2010) Role of C2 domain proteins during synaptic vesicle exocytosis. Biochem Soc Trans 38:213–216Google Scholar
  61. Mateos MV, Giusto NM, Salvador GA (2012) Distinctive roles of PLD signaling elicited by oxidative stress in synaptic endings from adult and aged rats. Biochim Biophys Acta 1823(12):2136–2148Google Scholar
  62. Meyer MZ, Déliot N, Chasserot-Golaz S, Premont RT, Bader MF, Vitale N (2006) Regulation of neuroendocrine exocytosis by the ARF6 GTPase-activating protein GIT1. J Biol Chem 281(12):7919–7926Google Scholar
  63. Mima J, Wickner W (2009) Phosphoinositides and SNARE chaperones synergistically assemble and remodel SNARE complexes for membrane fusion. Proc Natl Acad Sci U S A 106(38):16191–16196Google Scholar
  64. Momboisse F, Lonchamp E, Calco V, Ceridono M, Vitale N, Bader MF, Gasman S (2009) betaPIX-activated Rac1 stimulates the activation of phospholipase D, which is associated with exocytosis in neuroendocrine cells. J Cell Sci 122(Pt 6):798–806Google Scholar
  65. Nelson RK, Frohman MA (2015) Physiological and pathophysiological roles for phospholipase D. J Lipid Res 56(12):2229–2237Google Scholar
  66. Nishida A, Emoto K, Shimizu M, Uozumi T, Yamawaki S (1994) Brain ischemia decreases phosphatidylcholine-phospholipase D but not phosphatidylinositol-phospholipase C in rats. Stroke 25(6):1247–1251Google Scholar
  67. Oh SO, Hong JH, Kim YR, Yoo HS, Lee SH, Lim K, Hwang BD, Exton JH, Park SK (2000) Regulation of phospholipase D2 by H(2)O(2) in PC12 cells. J Neurochem 75(6):2445–2454Google Scholar
  68. Oliveira TG, Chan RB, Tian H, Laredo M, Shui G, Staniszewski A, Zhang H, Wang L, Kim TW, Duff KE, Wenk MR, Arancio O, Di Paolo G (2010) Phospholipase d2 ablation ameliorates Alzheimer’s disease-linked synaptic dysfunction and cognitive deficits. J Neurosci 30(49):16419–16428Google Scholar
  69. Payton JE, Perrin RJ, Woods WS, George JM (2004) Structural determinants of PLD2 inhibition by alpha-synuclein. J Mol Biol 337(4):1001–1009Google Scholar
  70. Rogasevskaia TP, Coorssen JR (2015) The role of phospholipase D in regulated exocytosis. J Biol Chem 290(48):28683–28696Google Scholar
  71. Rohrbough J, Broadie K (2005) Lipid regulation of the synaptic vesicle cycle. Nat Rev Neurosci 6(2):139–150Google Scholar
  72. Schwarz K, Natarajan S, Kassas N, Vitale N, Schmitz F (2011) The synaptic ribbon is a site of phosphatidic acid generation in ribbon synapses. J Neurosci 31(44):15996–16011Google Scholar
  73. Servitja JM, Masgrau R, Pardo R, Sarri E, Picatoste F (2000) Effects of oxidative stress on phospholipid signaling in rat cultured astrocytes and brain slices. J Neurochem 75(2):788–794Google Scholar
  74. Shin EY, Ma EK, Kim CK, Kwak SJ, Kim EG (2002) Src/ERK but not phospholipase D is involved in keratinocyte growth factor-stimulated secretion of matrix metalloprotease-9 and urokinase-type plasminogen activator in SNU-16 human stomach cancer cell. J Cancer Res Clin Oncol 128(11):596–602Google Scholar
  75. Stein A, Weber G, Wahl MC, Jahn R (2009) Helical extension of the neuronal SNARE complex into the membrane. Nature 460:525–528Google Scholar
  76. Stutchfield J, Cockcroft S (1993) Correlation between secretion and phospholipase D activation in differentiated HL60 cells. Biochem J 293(Pt3):649–655Google Scholar
  77. Sun H, Xia M, Shahane SA, Jadhav A, Austin CP, Huang R (2013) Are hERG channel blockers also phospholipidosis inducers? Bioorg Med Chem Lett 23(16):4587–4590Google Scholar
  78. Tabet R, Moutin E, Becker JA, Heintz D, Fouillen L, Flatter E, Krężel W, Alunni V, Koebel P, Dembélé D, Tassone F, Bardoni B, Mandel JL, Vitale N, Muller D, Le Merrer J, Moine H (2016a) Fragile X Mental Retardation Protein (FMRP) controls diacylglycerol kinase activity in neurons. Proc Natl Acad Sci U S A 113:E3619–E3628Google Scholar
  79. Tabet R, Vitale N, Moine H (2016b) Fragile X syndrome: are signaling lipids the missing culprits? Biochimie 130:188–194Google Scholar
  80. Tanguy E, Carmon O, Wang Q, Jeandel L, Chasserot-Golaz S, Montero-Hadjadje M, Vitale N (2016) Lipids implicated in the journey of a secretory granule: from biogenesis to fusion. J Neurochem 137(6):904–912Google Scholar
  81. Taraska JW, Perrais D, Ohara-Imaizumi M, Nagamatsu S, Almers W (2003) Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells. Proc Natl Acad Sci U S A 100(4):2070–2075. Epub 21 Jan 2003Google Scholar
  82. Topham MK (2006) Signaling roles of diacylglycerol kinases. J Cell Biochem 97(3):474–484 ReviewGoogle Scholar
  83. van Kempen GT, vanderLeest HT, van den Berg RJ, Eilers P, Westerink RH (2011) Three distinct modes of exocytosis revealed by amperometry in neuroendocrine cells. Biophys J 100(4):968–977Google Scholar
  84. Vance DE, Goldfine H (2002) Konrad Bloch – a pioneer in cholesterol and fatty acid biosynthesis. Biochem Biophys Res Commun 292(5):1117–1127Google Scholar
  85. Vance JE, Vance DE (2004) Phospholipid biosynthesis in mammalian cells. Biochem Cell Biol 82(1):113–128Google Scholar
  86. Vicogne J, VollenweiderD SJR, Huang P, Frohman MA, Pessin JE (2006) Asymmetric phospholipid distribution drives in vitro reconstituted SNARE-dependent membrane fusion. Proc Natl Acad Sci U S A 103:14761–14766Google Scholar
  87. Vitale N (2010) Synthesis of fusogenic lipids through activation of phospholipase D1 by GTPases and the kinase RSK2 is required for calcium-regulated exocytosis in neuroendocrine cells. Biochem Soc Trans 38(Pt 1):167–171Google Scholar
  88. Vitale N, Caumont AS, Chasserot-Golaz S, Du G, Wu S, Sciorra VA, Morris AJ, Frohman MA, Bader MF (2001) Phospholipase D1: a key factor for the exocytotic machinery in neuroendocrine cells. EMBO J 20(10):2424–2434Google Scholar
  89. Vitale N, Chasserot-Golaz S, Bader MF (2002) Regulated secretion in chromaffin cells: an essential role for ARF6-regulated phospholipase D in the late stages of exocytosis. Ann N Y Acad Sci 971:193–200Google Scholar
  90. Vitale N, Mawet J, Camonis J, Regazzi R, Bader MF, Chasserot-Golaz S (2005) The small GTPase RalA controls exocytosis of large dense core secretory granules by interacting with ARF6-dependent phospholipase D1. J Biol Chem 280(33):29921–29928Google Scholar
  91. Vodicka P, Mo S, Tousley A, Green KM, Sapp E, Iuliano M, Sadri-Vakili G, Shaffer SA, Aronin N, DiFiglia M, Kegel-Gleason KB (2015) Mass spectrometry analysis of wild-type and knock-in Q140/Q140 Huntington’s disease mouse brains reveals changes in glycerophospholipids including alterations in phosphatidic acid and lyso-phosphatidic acid. J Huntingtons Dis 4(2):187–201Google Scholar
  92. Waselle L, Gerona RR, Vitale N, Martin TF, Bader MF, Regazzi R (2005) Role of phosphoinositide signaling in the control of insulin exocytosis. Mol Endocrinol 19(12):3097–3106. Epub 4 Aug 2005Google Scholar
  93. Williams JM, Pettitt TR, Powell W, Grove J, Savage CO, Wakelam MJ et al (2007) Antineutrophil cytoplasm antibody-stimulated neutrophil adhesion depends on diacylglycerol kinase-catalyzed phosphatidic acid formation. J Am Soc Nephrol 18(4):1112–1120Google Scholar
  94. Xie MS, Jacobs LS, Dubyak GR (1991) Activation of phospholipase D and primary granule secretion by P2-purinergic- and chemotactic peptide-receptor agaonists is induced during granulocyte differenciation of HL-60 cells. J Clin Invest 88:45–54Google Scholar
  95. Zeniou-Meyer M, Zabari N, Ashery U, Chasserot-Golaz S, Haeberlé AM, Demais V, Bailly Y, Gottfried I, Nakanishi H, Neiman AM, Du G, Frohman MA, Bader MF, Vitale N (2007) Phospholipase D1 production of phosphatidic acid at the plasma membrane promotes exocytosis of large dense-core granules at a late stage. J Biol Chem 282(30):21746–21757Google Scholar
  96. Zeniou-Meyer M, Liu Y, Béglé A, Olanich ME, Hanauer A, Becherer U, Rettig J, Bader MF, Vitale N (2008) The Coffin-Lowry syndrome-associated protein RSK2 is implicated in calcium-regulated exocytosis through the regulation of PLD1. Proc Natl Acad Sci U S A 105(24):8434–8439Google Scholar
  97. Zeniou-Meyer M, Gambino F, Ammar MR, Humeau Y, Vitale N (2010) The Coffin-Lowry syndrome-associated protein RSK2 and neurosecretion. Cell Mol Neurobiol 30(8):1401–1406Google Scholar
  98. Zhang Y, Huang P, Du G, Kanaho Y, Frohman MA, Tsirka SE (2004) Increased expression of two phospholipase D isoforms during experimentally induced hippocampal mossy fiber outgrowth. Glia 46(1):74–83Google Scholar
  99. Zhu YB, Kang K, Zhang Y, Qi C, Li G, Yin DM, Wang Y (2012) PLD1 negatively regulates dendritic branching. J Neurosci 32(23):7960–7969Google Scholar

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© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Institut des Neurosciences Cellulaires et Intégratives, CNRS UPR 3212 and Université de StrasbourgStrasbourgFrance
  2. 2.INSERMParisFrance

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