Chronic inhibition of brain phospholipase A2 in adult rats impairs the survival of newborn mature neurons in the hippocampus

Journal of Neural Transmission

Volumn 122, Issue 5, 2015, Pages 619-628

  Schaeffer, Evelin L ^a   Gattaz, Wagner F ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Adult neurogenesis; Alzheimer disease; Hippocampus; Phospholipase A2; Rat

Indexed keywords

PHOSPHOLIPASE A2; PHOSPHOLIPASE A2 INHIBITOR; ARACHIDONIC ACID DERIVATIVE; BROXURIDINE; CELL NUCLEUS ANTIGEN; METHYL ARACHIDONYLFLUOROPHOSPHONATE; NERVE PROTEIN; NEUN PROTEIN, RAT; PHOSPHONIC ACID DERIVATIVE;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; ENZYME INHIBITION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; ANIMAL; DRUG EFFECTS; INFUSION PUMP; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; WISTAR RAT;

ANIMALS; ANTIGENS, NUCLEAR; ARACHIDONIC ACIDS; BROMODEOXYURIDINE; CELL COUNT; CELL SURVIVAL; DENTATE GYRUS; IMMUNOHISTOCHEMISTRY; INFUSION PUMPS, IMPLANTABLE; MALE; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; ORGANOPHOSPHONATES; PHOSPHOLIPASE A2 INHIBITORS; PHOSPHOLIPASES A2; RATS, WISTAR;

EID: 84928680471     PISSN: 03009564     EISSN: 14351463     Source Type: Journal    
DOI: 10.1007/s00702-014-1305-0     Document Type: Article

References (63)

1. Altman J, Bayer SA (1990) Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301:365–381
2. Arioka M, Cheon SH, Ikeno Y, Nakashima S, Kitamoto K (2005) A novel neurotrophic role of secretory phospholipases A2 for cerebellar granule neurons. FEBS Lett 579:2693–2701
3. Balsinde J, Dennis EA (1996) Distinct roles in signal transduction for each of the phospholipase A2 enzymes present in P388D1 macrophages. J Biol Chem 271:6758–6765
4. Basselin M, Ramadan E, Rapoport SI (2012) Imaging brain signal transduction and metabolism via arachidonic and docosahexaenoic acid in animals and humans. Brain Res Bull 87:154–171
5. Bédard A, Parent A (2004) Evidence of newly generated neurons in the human olfactory bulb. Brain Res Dev Brain Res 151:159–168
6. Bosetti F, Weerasinghe GR (2003) The expression of brain cyclooxygenase-2 is down-regulated in the cytosolic phospholipase A2 knockout mouse. J Neurochem 87:1471–1477
7. Chen J, Engle SJ, Seilhamer JJ, Tischfield JA (1994) Cloning and recombinant expression of a novel human low molecular weight Ca(2 +)-dependent phospholipase A2. J Biol Chem 269:2365–2368
8. Chin TY, Hwang HM, Chueh SH (2002) Distinct effects of different calcium-mobilizing agents on cell death in NG108-15 neuroblastoma X glioma cells. Mol Pharmacol 61:486–494
9. Dennis EA, Cao J, Hsu YH, Magrioti V, Kokotos G (2011) Phospholipase A2 enzymes: physical structure, biological function, disease implication, chemical inhibition, and therapeutic intervention. Chem Rev 111:6130–6185
10. Di Giorgio AM, Hou Y, Zhao X, Zhang B, Lyeth BG, Russell MJ (2008) Dimethyl sulfoxide provides neuroprotection in a traumatic brain injury model. Restor Neurol Neurosci 26:501–507
11. Ehninger D, Kempermann G (2008) Neurogenesis in the adult hippocampus. Cell Tissue Res 331:243–250
12. Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7–19
13. Forlenza OV, Mendes CT, Marie SK, Gattaz WF (2007a) Inhibition of phospholipase A2 reduces neurite outgrowth and neuronal viability. Prostaglandins Leukot Essent Fatty Acids 76:47–55
14. Forlenza OV, Schaeffer EL, Gattaz WF (2007b) The role of phospholipase A2 in neuronal homeostasis and memory formation: implications for the pathogenesis of Alzheimer’s disease. J Neural Transm 114:231–238
15. Gattaz WF, Maras A, Cairns NJ, Levy R, Förstl H (1995) Decreased phospholipase A2 activity in Alzheimer brains. Biol Psychiatry 37:13–17
16. Gattaz WF, Cairns NJ, Levy R, Förstl H, Braus DF, Maras A (1996) Decreased phospholipase A2 activity in the brain and in platelets of patients with Alzheimer’s disease. Eur Arch Psychiatry Clin Neurosci 246:129–131
17. 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 275:39823–39826
18. Gratzner HG (1982) Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218:474–475
19. Gundersen HJ, Jensen EB (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147(Pt 3):229–263
20. 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 280:28044–28052
21. Jin K, Peel AL, Mao XO, Xie L, Cottrell BA, Henshall DC, Greenberg DA (2004) Increased hippocampal neurogenesis in Alzheimer’s disease. Proc Natl Acad Sci USA 101:343–347
22. Kishimoto K, Matsumura K, Kataoka Y, Morii H, Watanabe Y (1999) Localization of cytosolic phospholipase A2 messenger RNA mainly in neurons in the rat brain. Neuroscience 92:1061–1077
23. Kolko M, Christoffersen NR, Varoqui H, Bazan NG (2005) Expression and induction of secretory phospholipase A2 group IB in brain. Cell Mol Neurobiol 25:1107–1122
24. Kolko M, Christoffersen NR, Barreiro SG, Miller ML, Pizza AJ, Bazan NG (2006) Characterization and location of secretory phospholipase A2 groups IIE, V, and X in the rat brain. J Neurosci Res 83:874–882
25. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027–2033
26. Kurusu S, Matsui K, Watanabe T, Tsunou T, Kawaminami M (2008) The cytotoxic effect of bromoenol lactone, a calcium-independent phospholipase A2 inhibitor, on rat cortical neurons in culture. Cell Mol Neurobiol 28:1109–1118
27. Lapuente Chala C, Rengifo Valbuena CA, Avila Rodríguez MF, Céspedes Rubio A (2013) Regulatory effect of dimethyl sulfoxide (DMSO) on astrocytic reactivity in a murine model of cerebral infarction by arterial embolization. Colomb Med (Cali) 44:31–36
28. Larsson Forsell PK, Kennedy BP, Claesson HE (1999) The human calcium-independent phospholipase A2 gene multiple enzymes with distinct properties from a single gene. Eur J Biochem 262:575–585
29. Lautens LL, Chiou XG, Sharp JD, Young WS 3rd, Sprague DL, Ross LS, Felder CC (1998) Cytosolic phospholipase A2 (cPLA2) distribution in murine brain and functional studies indicate that cPLA2 does not participate in muscarinic receptor-mediated signaling in neurons. Brain Res 809:18–30
30. Li B, Yamamori H, Tatebayashi Y, Shafit-Zagardo B, Tanimukai H, Chen S, Iqbal K, Grundke-Iqbal I (2008) Failure of neuronal maturation in Alzheimer disease dentate gyrus. J Neuropathol Exp Neurol 67:78–84
31. Lio YC, Reynolds LJ, Balsinde J, Dennis EA (1996) Irreversible inhibition of Ca(2 +)-independent phospholipase A2 by methyl arachidonyl fluorophosphonate. Biochim Biophys Acta 1302:55–60
32. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
33. Ma MT, Nevalainen TJ, Yeo JF, Ong WY (2010) Expression profile of multiple secretory phospholipase A(2) isoforms in the rat CNS: enriched expression of sPLA(2)-IIA in brainstem and spinal cord. J Chem Neuroanat 39:242–247
34. Mancuso DJ, Jenkins CM, Gross RW (2000) The genomic organization, complete mRNA sequence, cloning, and expression of a novel human intracellular membrane-associated calcium-independent phospholipase A(2). J Biol Chem 275:9937–9945
35. 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 280:23203–23214
36. 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 409:429–438
37. Molloy GY, Rattray M, Williams RJ (1998) Genes encoding multiple forms of phospholipase A2 are expressed in rat brain. Neurosci Lett 258:139–142
38. Moser MB, Moser EI (1998) Functional differentiation in the hippocampus. Hippocampus 8:608–619
39. 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
40. Owada Y, Tominaga T, Yoshimoto T, Kondo H (1994) Molecular cloning of rat cDNA for cytosolic phospholipase A2 and the increased gene expression in the dentate gyrus following transient forebrain ischemia. Brain Res Mol Brain Res 25:364–368
41. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic, San Diego
42. Pencea V, Bingaman KD, Freedman LJ, Luskin MB (2001) Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp Neurol 172:1–16
43. Perry EK, Johnson M, Ekonomou A, Perry RH, Ballard C, Attems J (2012) Neurogenic abnormalities in Alzheimer’s disease differ between stages of neurogenesis and are partly related to cholinergic pathology. Neurobiol Dis 47:155–162
44. Pickard RT, Strifler BA, Kramer RM, Sharp JD (1999) Molecular cloning of two new human paralogs of 85-kDa cytosolic phospholipase A2. J Biol Chem 274:8823–8831
45. Reif A, Schmitt A, Fritzen S, Chourbaji S, Bartsch C, Urani A, Wycislo M, Mössner R, Sommer C, Gass P, Lesch KP (2004) Differential effect of endothelial nitric oxide synthase (NOS-III) on the regulation of adult neurogenesis and behaviour. Eur J Neurosci 20:885–895
46. Ross BM, Moszczynska A, Erlich J, Kish SJ (1998) Phospholipid-metabolizing enzymes in Alzheimer’s disease: increased lysophospholipid acyltransferase activity and decreased phospholipase A2 activity. J Neurochem 70:786–793
47. Schaeffer EL, Gattaz WF (2005) Inhibition of calcium-independent phospholipase A2 activity in rat hippocampus impairs acquisition of short- and long-term memory. Psychopharmacology 181:392–400
48. Schaeffer EL, Kühn F, Schmitt A, Gattaz WF, Gruber O, Schneider-Axmann T, Falkai P, Schmitt A (2013) Increased cell proliferation in the rat anterior cingulate cortex following neonatal hypoxia: relevance to schizophrenia. J Neural Transm 120:187–195
49. Shapiro EM, Gonzalez-Perez O, Manuel García-Verdugo J, Alvarez-Buylla A, Koretsky AP (2006) Magnetic resonance imaging of the migration of neuronal precursors generated in the adult rodent brain. Neuroimage 32:1150–1157
50. Sharp JD, White DL (1993) Cytosolic PLA2: mRNA levels and potential for transcriptional regulation. J Lipid Mediat 8:183–189
51. Shinzawa K, Sumi H, Ikawa M, Matsuoka Y, Okabe M, Sakoda S, Tsujimoto Y (2008) Neuroaxonal dystrophy caused by group VIA phospholipase A2 deficiency in mice: a model of human neurodegenerative disease. J Neurosci 28:2212–2220
52. 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 721:39–48
53. Song C, Chang XJ, Bean KM, Proia MS, Knopf JL, Kriz RW (1999) Molecular characterization of cytosolic phospholipase A2-beta. J Biol Chem 274:17063–17067
54. Suzuki N, Ishizaki J, Yokota Y, Higashino K, Ono T, Ikeda M, Fujii N, Kawamoto K, Hanasaki K (2000) Structures, enzymatic properties, and expression of novel human and mouse secretory phospholipase A(2)s. J Biol Chem 275:5785–5793
55. Talbot K, Young RA, Jolly-Tornetta C, Lee VM, Trojanowski JQ, Wolf BA (2000) A frontal variant of Alzheimer’s disease exhibits decreased calcium-independent phospholipase A2 activity in the prefrontal cortex. Neurochem Int 37:17–31
56. Tanaka H, Takeya R, Sumimoto H (2000) A novel intracellular membrane-bound calcium-independent phospholipase A(2). Biochem Biophys Res Commun 272:320–326
57. Tojima T, Ito E (2004) Signal transduction cascades underlying de novo protein synthesis required for neuronal morphogenesis in differentiating neurons. Prog Neurobiol 72:183–193
58. Underwood KW, Song C, Kriz RW, Chang XJ, Knopf JL, Lin LL (1998) A novel calcium-independent phospholipase A2, cPLA2-gamma, that is prenylated and contains homology to cPLA2. J Biol Chem 273:21926–21932
59. Valentin E, Ghomashchi F, Gelb MH, Lazdunski M, Lambeau G (2000) Novel human secreted phospholipase A(2) with homology to the group III bee venom enzyme. J Biol Chem 275:7492–7496
60. West MJ (2012) Basic stereology for biologists and neuroscientists. Cold Spring Harbor, New York
61. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482–497
62. Yang H, Siddiqi NJ, Alhomida AS, Ong WY (2013) Expression and localization of sPLA2-III in the rat CNS. Neurochem Res 38:753–760
63. Yun DH, Jeon ES, Sung SM, Ryu SH, Kim JH (2006) Lysophosphatidylcholine suppresses apoptosis and induces neurite outgrowth in PC12 cells through activation of phospholipase D2. Exp Mol Med 38:375–384