LPCLysophosphatidylcholine suppresses apoptosis and induces neurite outgrowth in PC12 cells through activation of phospholipase D2

Yun, Du-Hui;Jeon, Eun-Su;Seong, Sang-Min;Ryu, Seong-Ho;Kim, Jae-Ho
윤두희;전은수;성상민;류성호;김재호

  • Published : 20060000

Abstract

Lysophosphatidylcholine (LPC) is a bioactive lipid generated by phospholipase A2-mediated hydro - lysis of phosphatidylcholine. In the present study, we demonstrate that LPC stimulates phospholipase D2 (PLD2) activity in rat pheochromocytoma PC12 cells. Serum deprivation induced cell death of PC12 cells, as demonstrated by decreased viability, DNA frag - mentation, and increased sub-G1 fraction of cell cycle. LPC treatment protected PC12 cells partially from the cell death and induced neurite outgrowth of the cells. Overexpression of PLD2 drastically en - hanced the LPC-induced inhibition of apoptosis and neuritogenesis. Pretreatment of the cells with 1-butanol, a PLD inhibitor, completely abrogated the LPC-induced inhibition of apoptosis and neurite outgrowth in PC12 cells overexpressing PLD2. These results indicate that LPC possesses the neurotrophic effects, such as anti-apoptosis and neurite outgrowth, through activation of PLD2.

Keywords

References

  1. Alley MC, Scudiero DA, Monks A, Hursey ML, Czerwinski MJ, Fine DL, Abbott BJ, Mayo JG, Shoemaker RH, Boyd MR. Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay. Cancer Res 1988;48:589-601
  2. Arimura N, Inagaki N, Chihara K, Menager C, Nakamura N, Amano M, Iwamatsu A, Goshima Y, Kaibuchi K. Phosphorylation of collapsin response mediator protein-2 by Rhokinase. Evidence for two separate signaling pathways for growth cone collapse. J Biol Chem 2000;275:23973-80 https://doi.org/10.1074/jbc.M001032200
  3. Barde YA. Neurotrophins: a family of proteins supporting the survival of neurons. Prog Clin Biol Res 1994;390:45-56
  4. Bektas M, Barak LS, Jolly PS, Liu H, Lynch KR, Lacana E, Suhr KB, Milstien S, Spiegel S. The G protein-coupled receptor GPR4 suppresses ERK activation in a ligand-independent manner. Biochemistry 2003;42:12181-91 https://doi.org/10.1021/bi035051y
  5. Chen JS, Exton JH. Regulation of phospholipase D2 activity by protein kinase C alpha. J Biol Chem 2004;279:22076-83 https://doi.org/10.1074/jbc.M311033200
  6. Chun J. Lysophospholipids in the nervous system. Prostaglandins Other Lipid Mediat 2005;77:46-51 https://doi.org/10.1016/j.prostaglandins.2004.09.009
  7. Colley WC, Altshuller YM, Sue-Ling CK, Copeland NG, Gilbert DJ, Jenkins NA, Branch KD, Tsirka SE, Bollag RJ, Bollag WB, Frohman MA. Cloning and expression analysis of murine phospholipase D1. Biochem J 1997a;326(Pt 3):745-53 https://doi.org/10.1042/bj3260745
  8. Colley WC, Sung TC, Roll R, Jenco J, Hammond SM, Altshuller Y, Bar-Sagi D, Morris AJ, Frohman MA. Phospholipase D2, a distinct phospholipase D isoform with novel regulatory properties that provokes cytoskeletal reorganization. Curr Biol 1997b;7:191-201 https://doi.org/10.1016/S0960-9822(97)70090-3
  9. Daniels RH, Hall PS, Bokoch GM. Membrane targeting of p21-activated kinase 1 (PAK1) induces neurite outgrowth from PC12 cells. 1998;17:754-64 https://doi.org/10.1093/emboj/17.3.754
  10. Dickson BJ. Molecular mechanisms of axon guidance. Science 2002;298:1959-64 https://doi.org/10.1126/science.1072165
  11. Exton JH. Phospholipase D-structure, regulation and function. Rev Physiol Biochem Pharmacol 2002;144:1-94 https://doi.org/10.1007/BFb0116585
  12. Frohman MA, Sung TC, Morris AJ. Mammalian phospholipase D structure and regulation. Biochim Biophys Acta 1999; 1439:175-86 https://doi.org/10.1016/S1388-1981(99)00093-1
  13. Fukushima N. LPA in neural cell development. J Cell Biochem 2004;92:993-1003 https://doi.org/10.1002/jcb.20093
  14. Goodman CS. Mechanisms and molecules that control growth cone guidance. Annu Rev Neurosci 1996;19:341-77 https://doi.org/10.1146/annurev.ne.19.030196.002013
  15. Han JM, Kim JH, Lee BD, Lee SD, Kim Y, Jung YW, Lee S, Cho W, Ohba M, Kuroki T, Suh PG, Ryu SH. Phosphorylation-dependent regulation of phospholipase D2 by protein kinase C delta in rat pheochromocytoma PC12 cells. J Biol Chem 2002; 277:8290-7 https://doi.org/10.1074/jbc.M108343200
  16. Ikeno Y, Konno N, Cheon SH, Bolchi A, Ottonello S, Kitamoto K, Arioka M. Secretory phospholipases A2 induce neurite outgrowth in PC12 cells through lysophosphatidylcholine generation and activation of G2A receptor. J Biol Chem 2005; 280:28044-52 https://doi.org/10.1074/jbc.M503343200
  17. Jalink K, Eichholtz T, Postma FR, van Corven EJ, Moolenaar WH. Lysophosphatidic acid induces neuronal shape changes via a novel, receptor-mediated signaling pathway: similarity to thrombin action. Cell Growth Differ 1993;4:247-55
  18. Kim JH, Kim Y, Lee SD, Lopez I, Arnold RS, Lambeth JD, Suh PG, Ryu SH. Selective activation of phospholipase D2 by unsaturated fatty acid. FEBS Lett 1999a;454:42-6 https://doi.org/10.1016/S0014-5793(99)00745-0
  19. Kim JH, Lee BD, Kim Y, Lee SD, Suh PG, Ryu SH. Cytosolic phospholipase A2-mediated regulation of phospholipase D2 in leukocyte cell lines. J Immunol 1999b;163:5462-70
  20. Kim KO, Lee KH, Kim YH, Park SK, Han JS. Anti-apoptotic role of phospholipase D isozymes in the glutamate-induced cell death. Exp Mol Med 2003a;35:38-45 https://doi.org/10.1038/emm.2003.6
  21. Kim SW, Hayashi M, Lo JF, Yang Y, Yoo JS, Lee JD. ADP-ribosylation factor 4 small GTPase mediates epidermal growth factor receptor-dependent phospholipase D2 activation. J Biol Chem 2003b;278:2661-8 https://doi.org/10.1074/jbc.M205819200
  22. Koch T, Brandenburg LO, Schulz S, Liang Y, Klein J, Hollt V. ADP-ribosylation factor-dependent phospholipase D2 activation is required for agonist-induced mu-opioid receptor endocytosis. J Biol Chem 2003;278:9979-85 https://doi.org/10.1074/jbc.M206709200
  23. Lee S, Kim JH, Lee CS, Kim JH, Kim Y, Heo K, Ihara Y, Goshima Y, Suh PG, Ryu SH. Collapsin response mediator protein-2 inhibits neuronal phospholipase D(2) activity by direct interaction. J Biol Chem 2002;277:6542-9 https://doi.org/10.1074/jbc.M108047200
  24. Lee S, Park JB, Kim JH, Kim Y, Kim JH, Shin KJ, Lee JS, Ha SH, Suh PG, Ryu SH. Actin directly interacts with phospholipase D, inhibiting its activity. J Biol Chem 2001;276:28252-60 https://doi.org/10.1074/jbc.M008521200
  25. Lee SD, Lee BD, Han JM, Kim JH, Kim Y, Suh PG, Ryu SH. Phospholipase D2 activity suppresses hydrogen peroxide- induced apoptosis in PC12 cells. J Neurochem 2000; 75:1053-9 https://doi.org/10.1046/j.1471-4159.2000.0751053.x
  26. Levi A, Biocca S, Cattaneo A, Calissano P. The mode of action of nerve growth factor in PC12 cells. Mol Neurobiol 1988; 2:201-26 https://doi.org/10.1007/BF02935346
  27. Liscovitch M, Czarny M, Fiucci G, Tang X. Phospholipase D: molecular and cell biology of a novel gene family. Biochem J 2000;345 Pt 3:401-15 https://doi.org/10.1042/0264-6021:3450401
  28. Lopez I, Arnold RS, Lambeth JD. Cloning and initial characterization of a human phospholipase D2 (hPLD2). ADP-ribosylation factor regulates hPLD2. J Biol Chem 1998;273:12846-52 https://doi.org/10.1074/jbc.273.21.12846
  29. Macphee CH. Lipoprotein-associated phospholipase A2: a potential new risk factor for coronary artery disease and a therapeutic target. Curr Opin Pharmacol 2001;1:121-5 https://doi.org/10.1016/S1471-4892(01)00024-8
  30. Masuda S, Murakami M, Takanezawa Y, Aoki J, Arai H, Ishikawa Y, Ishii T, Arioka M, Kudo I. Neuronal expression and neuritogenic action of group X secreted phospholipase A2. J Biol Chem 2005;280:23203-14 https://doi.org/10.1074/jbc.M500985200
  31. Meyer zu Heringdorf D, Himmel HM, Jakobs KH. Sphingosylphosphorylcholine- biological functions and mechanisms of action. Biochim Biophys Acta 2002;1582:178-89 https://doi.org/10.1016/S1388-1981(02)00154-3
  32. Moolenaar WH. Lysophospholipids in the limelight: autotaxin takes center stage. J Cell Biol 2002;158:197-9 https://doi.org/10.1083/jcb.200206094
  33. Mueller BK. Growth cone guidance: first steps towards a deeper understanding. Annu Rev Neurosci 1999;22:351-88 https://doi.org/10.1146/annurev.neuro.22.1.351
  34. Murakami N, Yokomizo T, Okuno T, Shimizu T. G2A is a proton- sensing G-protein coupled receptor antagonized by lysophosphatidylcholine. J Biol Chem 2004;279:42484-91 https://doi.org/10.1074/jbc.M406561200
  35. Nakamura F, Kalb RG, Strittmatter SM. Molecular basis of semaphorin-mediated axon guidance. J Neurobiol 2000; 44:219-29 https://doi.org/10.1002/1097-4695(200008)44:2<219::AID-NEU11>3.0.CO;2-W
  36. Park SK, Provost JJ, Bae CD, Ho WT, Exton JH. Cloning and characterization of phospholipase D from rat brain. J Biol Chem 1997;272:29263-71 https://doi.org/10.1074/jbc.272.46.29263
  37. Paves H, Saarma M. Neurotrophins as in vitro growth cone guidance molecules for embryonic sensory neurons. Cell Tissue Res 1997;290:285-97 https://doi.org/10.1007/s004410050933
  38. Prokazova NV, Zvezdina ND, Korotaeva AA. Effect of lysophosphatidylcholine on transmembrane signal transduction. Biochemistry (Mosc.) 1998;63:31-7
  39. Raper JA. Semaphorins and their receptors in vertebrates and invertebrates. Curr Opin Neurobiol 2000;10:88-94 https://doi.org/10.1016/S0959-4388(99)00057-4
  40. Reza JN, Gavazzi I, Cohen J. Neuropilin-1 is expressed on adult mammalian dorsal root ganglion neurons and mediates semaphorin3a/collapsin-1-induced growth cone collapse by small diameter sensory afferents. Mol Cell Neurosci 1999; 14:317-26 https://doi.org/10.1006/mcne.1999.0786
  41. Sato K, Malchinkhuu E, Muraki T, Ishikawa K, Hayashi K, Tosaka M, Mochiduki A, Inoue K, Tomura H, Mogi C, Nochi H, Tamoto K, Okajima F. Identification of autotaxin as a neurite retraction- inducing factor of PC12 cells in cerebrospinal fluid and its possible sources. J Neurochem 2005;92:904-14 https://doi.org/10.1111/j.1471-4159.2004.02933.x
  42. Sung TC, Altshuller YM, Morris AJ, Frohman MA. Molecular analysis of mammalian phospholipase D2. J Biol Chem 1999; 274:494-502 https://doi.org/10.1074/jbc.274.1.494
  43. Tigyi G, Miledi R. Lysophosphatidates bound to serum albumin activate membrane currents in Xenopus oocytes and neurite retraction in PC12 pheochromocytoma cells. J Biol Chem 1992;267:21360-7
  44. Tomura H, Mogi C, Sato K, Okajima F. Proton-sensing and lysolipid- sensitive G-protein-coupled receptors: a novel type of multi-functional receptors. Cell Signal 2005;17:1466-76 https://doi.org/10.1016/j.cellsig.2005.06.002
  45. Umezu-Goto M, Kishi Y, Taira A, Hama K, Dohmae N, Takio K, Yamori T, Mills GB, Inoue K, Aoki J, Arai H. Autotaxin has lysophospholipase D activity leading to tumor cell growth and motility by lysophosphatidic acid production. J Cell Biol 2002; 158:227-33 https://doi.org/10.1083/jcb.200204026
  46. Watanabe H, Yamazaki M, Miyazaki H, Arikawa C, Itoh K, Sasaki T, Maehama T, Frohman MA, Kanaho Y. Phospholipase D2 functions as a downstream signaling molecule of MAP kinase pathway in L1-stimulated neurite outgrowth of cerebellar granule neurons. J Neurochem 2004a;89:142-51 https://doi.org/10.1111/j.1471-4159.2004.02308.x
  47. Watanabe H, Yokozeki T, Yamazaki M, Miyazaki H, Sasaki T, Maehama T, Itoh K, Frohman MA, Kanaho Y. Essential role for phospholipase D2 activation downstream of ERK MAP kinase in nerve growth factor-stimulated neurite outgrowth from PC12 cells. J Biol Chem 2004b;279:37870-7 https://doi.org/10.1074/jbc.M402610200
  48. Xu Y. Sphingosylphosphorylcholine and lysophosphatdylcholine: G protein-coupled receptors and receptor-mediated signal transduction. Biochim Biophys Acta 2002;1582:81-8 https://doi.org/10.1016/S1388-1981(02)00140-3
  49. Yan JJ, Jung JS, Lee JE, Lee J, Huh SO, Kim HS, Jung KC, Cho JY, Nam JS, Suh HW, Kim YH, Song DK. Therapeutic effects of lysophosphatidylcholine in experimental sepsis. Nat Med 2004;10:161-7 https://doi.org/10.1038/nm989
  50. Yang LV, Radu CG, Wang L, Riedinger M, Witte ON. Gi-independent macrophage chemotaxis to lysophosphatidylcholine via the immunoregulatory GPCR G2A. Blood 2005; 105:1127-34 https://doi.org/10.1182/blood-2004-05-1916
  51. Zheng JQ, Wan JJ, Poo MM. Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J Neurosci 1996;16:1140-9 https://doi.org/10.1523/JNEUROSCI.16-03-01140.1996