Distribution of Secretory Phospholipase A2 XIIA in the Brain and its Role in Lipid Metabolism and Cognition

Molecular Neurobiology

Volumn 50, Issue 1, 2014, Pages 60-75

  Ee, Sze Min ^a   Lo, Yew Long ^a,b   Shui, Guanghou ^c   Wenk, Markus R ^a   Shin, Eun Joo ^d   Kim, Hyoung Chun ^d   Ong, Wei Yi ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b SINGAPORE GENERAL HOSPITAL   (Singapore)

^c INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^d Kangwon National University   (South Korea)

Author keywords

Attention; Cognition; Electron microscopy; Lipidomics; Secretory phospholipase A2

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; ARACHIDONIC ACID; LYSOPHOSPHOLIPID; MESSENGER RNA; SECRETORY PHOSPHOLIPASE A2; SECRETORY PHOSPHOLIPASE A2 XIIA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; ATTENTION; BRAIN REGION; COGNITION; CONTROLLED STUDY; CORPUS STRIATUM; DENDRITE; ELECTRON MICROSCOPY; HIPPOCAMPUS; LIPID METABOLISM; LIPIDOMICS; MALE; NERVE ENDING; NONHUMAN; PASSIVE AVOIDANCE TEST; PREFRONTAL CORTEX; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; WORKING MEMORY; ANIMAL; ANIMAL BEHAVIOR; ANTIBODY SPECIFICITY; AVOIDANCE BEHAVIOR; BRAIN; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; SHORT TERM MEMORY; SYNAPTOSOME; WISTAR RAT;

ANIMALS; ATTENTION; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; BRAIN; COGNITION; DENDRITES; LIPID METABOLISM; MALE; MEMORY, SHORT-TERM; OLIGONUCLEOTIDES, ANTISENSE; ORGAN SPECIFICITY; PHOSPHOLIPASES A2, SECRETORY; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR;

EID: 84911002270     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-014-8635-7     Document Type: Article

References (46)

1. Titsworth WL, Liu NK, Xu XM (2008) Role of secretory phospholipase A2 in CNS inflammation: implications in traumatic spinal cord injury. CNS Neurol Disord Drug Targets 7(3):254–269
2. Farooqui AA, Horrocks LA (2004) Brain phospholipases A2: a perspective on the history. Prostaglandins Leukot Essent Fat Acids 71(3):161–169
3. Farooqui AA, Horrocks LA (2006) Phospholipase A2-generated lipid mediators in the brain: the good, the bad, and the ugly. Neuroscientist: Rev J Bringing Neurobiol Neurol Psychiatry 12(3):245–260. doi:10.1177/1073858405285923
4. Ong WY, Farooqui T, Farooqui AA (2010) Involvement of cytosolic phospholipase A2, calcium independent phospholipase A2 and plasmalogen selective phospholipase A2 in neurodegenerative and neuropsychiatric conditions. Curr Med Chem 17(25):2746–2763
5. Lambeau G, Gelb MH (2008) Biochemistry and physiology of mammalian secreted phospholipases A2. Annu Rev Biochem 77:495–520. doi:10.1146/annurev.biochem.76.062405.154007
6. Murakami M, Taketomi Y, Girard C, Yamamoto K, Lambeau G (2010) Emerging roles of secreted phospholipase A2 enzymes: lessons from transgenic and knockout mice. Biochimie 92(6):561–582
7. Fourcade O, Simon MF, Viodé C, Rugani N, Leballe F, Ragab A, Fournié B, Sarda L, Chap H (1995) Secretory phospholipase A2 generates the novel lipid mediator lysophosphatidic acid in membrane microvesicles shed from activated cells. Cell 80(6):919–927
8. Hanasaki K, Yamada K, Yamamoto S, Ishimoto Y, Saiga A, Ono T, Ikeda M, Notoya M, Kamitani S, Arita H (2002) Potent modification of low density lipoprotein by group X secretory phospholipase A2 is linked to macrophage foam cell formation. J Biol Chem 277(32):29116–29124
9. Pungercar J, Krizaj I (2007) Understanding the molecular mechanism underlying the presynaptic toxicity of secreted phospholipases A2. Toxicon 50(7):871–892
10. Lambeau G, Lazdunski M (1999) Receptors for a growing family of secreted phospholipases A2. Trends Pharmacol Sci 20(4):162–170
11. Thwin MM, Ong WY, Fong CW, Sato K, Kodama K, Farooqui AA, Gopalakrishnakone P (2003) Secretory phospholipase A2 activity in the normal and kainate injected rat brain, and inhibition by a peptide derived from python serum. Exp Brain Res Exp Hirnforsch Exp Cereb 150(4):427–433. doi:10.1007/s00221-003-1476-7
12. Cunningham TJ, Yao L, Oetinger M, Cort L, Blankenhorn EP, Greenstein JI (2006) Secreted phospholipase A2 activity in experimental autoimmune encephalomyelitis and multiple sclerosis. J Neuroinflammation 3:26. doi:10.1186/1742-2094-3-26
13. Moses GS, Jensen MD, Lue LF, Walker DG, Sun AY, Simonyi A, Sun GY (2006) Secretory PLA2-IIA: a new inflammatory factor for Alzheimer’s disease. J Neuroinflammation 3:28. doi:10.1186/1742-2094-3-28
14. Ferrini M, Nardicchi V, Mannucci R, Arcuri C, Nicoletti I, Donato R, Goracci G (2010) Effect of NGF on the subcellular localization of group IIA secretory phospholipase A2 (GIIA) in PC12 cells: role in neuritogenesis. Neurochem Res 35(12):2168–2174. doi:10.1007/s11064-010-0345-6
15. Masuda S, Yamamoto K, Hirabayashi T, Ishikawa Y, Ishii T, Kudo I, Murakami M (2008) Human group III secreted phospholipase A2 promotes neuronal outgrowth and survival. Biochem J 409(2):429–438. doi:10.1042/BJ20070844
16. Masuda S, Murakami M, Takanezawa Y, Aoki J, Arai H, Ishikawa Y, Ishii T, Arioka M, Kudo I (2005) Neuronal expression and neuritogenic action of group X secreted phospholipase A2. J Biol Chem 280(24):23203–23214. doi:10.1074/jbc.M500985200
17. Wei S, Ong WY, Thwin MM, Fong CW, Farooqui AA, Gopalakrishnakone P, Hong W (2003) Group IIA secretory phospholipase A2 stimulates exocytosis and neurotransmitter release in pheochromocytoma-12 cells and cultured rat hippocampal neurons. Neuroscience 121(4):891–898
18. Than A, Tan Y, Ong WY, Farooqui AA, Chen P (2012) Kainate receptors mediate regulated exocytosis of secretory phospholipase A2 in SH-SY5Y neuroblastoma cells. Neuro-Signals 20(2):72–85. doi:10.1159/000330414
19. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402–408
20. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37(8):911–917
21. Shui G, Stebbins JW, Lam BD, Cheong WF, Lam SM, Gregoire F, Kusonoki J, Wenk MR (2011) Comparative plasma lipidome between human and cynomolgus monkey: are plasma polar lipids good biomarkers for diabetic monkeys? PLoS ONE 6(5):e19731. doi:10.1371/journal.pone.0019731
22. Shui G, Cheong WF, Jappar IA, Hoi A, Xue Y, Fernandis AZ, Tan BK, Wenk MR (2011) Derivatization-independent cholesterol analysis in crude lipid extracts by liquid chromatography/mass spectrometry: applications to a rabbit model for atherosclerosis. J Chromatogr A 1218(28):4357–4365. doi:10.1016/j.chroma.2011.05.011
23. Birrell JM, Brown VJ (2000) Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci 20(11):4320–4324
24. Young JW, Powell SB, Geyer MA, Jeste DV, Risbrough VB (2010) The mouse attentional-set-shifting task: a method for assaying successful cognitive aging? Cogn Affect Behav Neurosci 10(2):243–251
25. Gronich J, Konieczkowski M, Gelb MH, Nemenoff RA, Sedor JR (1994) Interleukin 1 alpha causes rapid activation of cytosolic phospholipase A2 by phosphorylation in rat mesangial cells. J Clin Invest 93(3):1224–1233. doi:10.1172/JCI117076
26. Leslie CC (1997) Properties and regulation of cytosolic phospholipase A2. J Biol Chem 272(27):16709–16712
27. Gelb MH, Valentin E, Ghomashchi F, Lazdunski M, Lambeau G (2000) Cloning and recombinant expression of a structurally novel human secreted phospholipase A2. J Biol Chem 275(51):39823–39826
28. Molloy GY, Rattray M, Williams RJ (1998) Genes encoding multiple forms of phospholipase A2 are expressed in rat brain. Neurosci Lett 258(3):139–142
29. Ho IC, Arm JP, Bingham CO III, Choi A, Austen KF, Glimcher LH (2001) A novel group of phospholipase A2s preferentially expressed in type 2 helper T cells. J Biol Chem 276(21):18321–18326
30. Muñoz-Sanjuán I, Brivanlou AH (2005) Induction of ectopic olfactory structures and bone morphogenetic protein inhibition by Rossy, a group XII secreted phospholipase A2. Mol Cell Biol 25(9):3608–3619
31. Titsworth WL, Cheng X, Ke Y, Deng L, Burckardt KA, Pendleton C, Liu NK, Shao H, Cao QL, Xu XM (2009) Differential expression of sPLA2 following spinal cord injury and a functional role for sPLA2-IIA in mediating oligodendrocyte death. Glia 57(14):1521–1537. doi:10.1002/glia.20867
32. Nakashima S, Ikeno Y, Yokoyama T, Kuwana M, Bolchi A, Ottonello S, Kitamoto K, Arioka M (2003) Secretory phospholipases A2 induce neurite outgrowth in PC12 cells. Biochem J 376(Pt 3):655–666. doi:10.1042/BJ20030830
33. Williams EJ, Walsh FS, Doherty P (1994) The production of arachidonic acid can account for calcium channel activation in the second messenger pathway underlying neurite outgrowth stimulated by NCAM, N-cadherin, and L1. J Neurochem 62(3):1231–1234
34. Smalheiser NR, Dissanayake S, Kapil A (1996) Rapid regulation of neurite outgrowth and retraction by phospholipase A2-derived arachidonic acid and its metabolites. Brain Res 721(1–2):39–48
35. Ikeno Y, Konno N, Cheon SH, Bolchi A, Ottonello S, Kitamoto K, Arioka M (2005) Secretory phospholipases A2 induce neurite outgrowth in PC12 cells through lysophosphatidylcholine generation and activation of G2A receptor. J Biol Chem 280(30):28044–28052. doi:10.1074/jbc.M503343200
36. Murzyn K, Rog T, Pasenkiewicz-Gierula M (2005) Phosphatidylethanolamine-phosphatidylglycerol bilayer as a model of the inner bacterial membrane. Biophys J 88(2):1091–1103. doi:10.1529/biophysj.104.048835
37. Koduri RS, Grönroos JO, Laine VJ, Le Calvez C, Lambeau G, Nevalainen TJ, Gelb MH (2002) Bactericidal properties of human and murine groups I, II, V, X, and XII secreted phospholipases A2. J Biol Chem 277(8):5849–5857
38. Huhtinen HT, Grönroos JO, Grönroos JM, Uksila J, Gelb MH, Nevalainen TJ, Laine VJ (2006) Antibacterial effects of human group IIA and group XIIA phospholipase A2 against Helicobacter pylori in vitro. APMIS 114(2):127–130
39. Rouault M, Le Calvez C, Boilard E, Surrel F, Singer A, Ghomashchi F, Bezzine S, Scarzello S, Bollinger J, Gelb MH, Lambeau G (2007) Recombinant production and properties of binding of the full set of mouse secreted phospholipases A2 to the mouse M-type receptor. Biochemistry 46(6):1647–1662. doi:10.1021/bi062119b
40. Reynolds CP, Maurer BJ, Kolesnick RN (2004) Ceramide synthesis and metabolism as a target for cancer therapy. Cancer Lett 206(2):169–180. doi:10.1016/j.canlet.2003.08.034
41. Mocchetti I (2005) Exogenous gangliosides, neuronal plasticity and repair, and the neurotrophins. Cell Mol Life Sci: CMLS 62(19–20):2283–2294. doi:10.1007/s00018-005-5188-y
42. Goldman-Rakic PS (1990) Cellular and circuit basis of working memory in prefrontal cortex of nonhuman primates. Prog Brain Res 85:325–335, discussion 335-326
43. Puumala T, Sirviö J (1998) Changes in activities of dopamine and serotonin systems in the frontal cortex underlie poor choice accuracy and impulsivity of rats in an attention task. Neuroscience 83(2):489–499
44. de la Presa OS, Innis SM (1999) Docosahexaenoic and arachidonic acid prevent a decrease in dopaminergic and serotoninergic neurotransmitters in frontal cortex caused by a linoleic and alpha-linolenic acid deficient diet in formula-fed piglets. J Nutr 129(11):2088–2093
45. Zimmer L, Durand G, Guilloteau D, Chalon S (1999) n-3 polyunsaturated fatty acid deficiency and dopamine metabolism in the rat frontal cortex. Lipids 34:S251
46. Biederman J (2005) Attention-deficit/hyperactivity disorder: a selective overview. Biol Psychiatry 57(11):1215–1220