Inhibition of neutral sphingomyelinase-2 perturbs brain sphingolipid balance and spatial memory in mice

Journal of Neuroscience Research

Volumn 88, Issue 13, 2010, Pages 2940-2951

  Tabatadze, Nino ^a   Savonenko, Alena ^a   Song, Hongjun ^a   Bandaru, Veera Venkata Ratnam ^a   Chu, Michael ^a   Haughey, Norman J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AMPA; Ceramide; Memory; NMDA; Sphingomyelinase; Synapse

Indexed keywords

AMPA RECEPTOR; CERAMIDE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POSTSYNAPTIC DENSITY PROTEIN 95; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOMYELIN PHOSPHODIESTERASE 3; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EPISODIC MEMORY; LEARNING; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPATIAL MEMORY;

ANALYSIS OF VARIANCE; ANILINE COMPOUNDS; ANIMALS; BENZYLIDENE COMPOUNDS; BRAIN; CERAMIDES; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; MASS SPECTROMETRY; MAZE LEARNING; MEMORY DISORDERS; MICE; MICE, KNOCKOUT; SPACE PERCEPTION; SPHINGOLIPIDS; SPHINGOMYELIN PHOSPHODIESTERASE;

EID: 77957220100     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22438     Document Type: Article

References (62)

1. Abulrob A, Tauskela JS, Mealing G, Brunette E, Faid K, Stanimirovic D. 2005. Protection by cholesterol-extracting cyclodextrins: a role for N-methyl-D-aspartate receptor redistribution. J Neurochem 92:1477-1486. (Pubitemid 40389216)
2. Aubin I, Adams CP, Opsahl S, Septier D, Bishop CE, Auge N, Salvayre R, Negre-Salvayre A, Goldberg M, Guenet JL, Poirier C. 2005. A deletion in the gene encoding sphingomyelin phosphodiesterase 3 (Smpd3) results in osteogenesis and dentinogenesis imperfecta in the mouse. Nat Genet 37:803-805. (Pubitemid 41077104)
3. Bajjalieh SM, Martin TF, Floor E. 1989. Synaptic vesicle ceramide kinase. A calcium-stimulated lipid kinase that co-purifies with brain synaptic vesicles. J Biol Chem 264:14354-14360. (Pubitemid 19214266)
4. Bandaru VV, McArthur JC, Sacktor N, Cutler RG, Knapp EL, Mattson MP, Haughey NJ. 2007. Associative and predictive biomarkers of dementia in HIV-1-infected patients. Neurology 68:1481-1487. (Pubitemid 46685918)
5. Bannerman DM, Good MA, Butcher SP, Ramsay M, Morris RG. 1995. Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature 378:182-186.
6. Besshoh S, Bawa D, Teves L, Wallace MC, Gurd JW. 2005. Increased phosphorylation and redistribution of NMDA receptors between synaptic lipid rafts and post-synaptic densities following transient global ischemia in the rat brain. J Neurochem 93:186-194. (Pubitemid 40463528)
7. Brann AB, Scott R, Neuberger Y, Abulafia D, Boldin S, Fainzilber M, Futerman AH. 1999. Ceramide signaling downstream of the p75 neurotrophin receptor mediates the effects of nerve growth factor on outgrowth of cultured hippocampal neurons. J Neurosci 19:8199-8206. (Pubitemid 30226739)
8. Clarke CJ, Hannun YA. 2006. Neutral sphingomyelinases and nSMase2: bridging the gaps. Biochim Biophys Acta 1758:1893-1901.
9. Claus RA, Dorer MJ, Bunck AC, Deigner HP. 2009. Inhibition of sphingomyelin hydrolysis: targeting the lipid mediator ceramide as a key regulator of cellular fate. Curr Med Chem 16:1978-2000.
10. Conrad CD, Galea LA, Kuroda Y, McEwen BS. 1996. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav Neurosci 110:1321-1334.
11. Coogan AN, O'Neill LA, O'Connor JJ. 1999. The P38 mitogen-activated protein kinase inhibitor SB203580 antagonizes the inhibitory effects of interleukin-1beta on long-term potentiation in the rat dentate gyrus in vitro. Neuroscience 93:57-69.
12. Crusio WE, Schwegler H. 2005. Learning spatial orientation tasks in the radial-maze and structural variation in the hippocampus in inbred mice. Behav Brain Funct 1:3.
13. Davis CN, Tabarean I, Gaidarova S, Behrens MM, Bartfai T. 2006. IL-1beta induces a MyD88-dependent and ceramide-mediated activation of Src in anterior hypothalamic neurons. J Neurochem 98:1379-1389.
14. Day CA, Kenworthy AK. 2009. Tracking microdomain dynamics in cell membranes. Biochim Biophys Acta 1788:245-253.
15. Dellu F, Fauchey V, Le Moal M, Simon H. 1997. Extension of a new two-trial memory task in the rat: influence of environmental context on recognition processes. Neurobiol Learn Mem 67:112-120.
16. Detre C, Kiss E, Varga Z, Ludanyi K, Paszty K, Enyedi A, Kovesdi D, Panyi G, Rajnavolgyi E, Matko J. 2006. Death or survival: membrane ceramide controls the fate and activation of antigen-specific T-cells depending on signal strength and duration. Cell Signal 18:294-306.
17. Fasano C, Miolan JP, Niel JP. 2003. Modulation by C2 ceramide of the nicotinic transmission within the coeliac ganglion in the rabbit. Neuroscience 116:753-759.
18. Frank C, Giammarioli AM, Pepponi R, Fiorentini C, Rufini S. 2004. Cholesterol perturbing agents inhibit NMDA-dependent calcium influx in rat hippocampal primary culture. FEBS Lett 566:25-29.
19. Fullekrug J, Simons K. 2004. Lipid rafts and apical membrane traffic. Ann N Y Acad Sci 1014:164-169.
20. Furukawa K, Mattson MP. 1998. The transcription factor NF-kappaB mediates increases in calcium currents and decreases in NMDA- and AMPA/kainate-induced currents induced by tumor necrosis factoralpha in hippocampal neurons. J Neurochem 70:1876-1886. (Pubitemid 28207809)
21. Haughey NJ, Cutler RG, Tamara A, McArthur JC, Vargas DL, Pardo CA, Turchan J, Nath A, Mattson MP. 2004. Perturbation of sphingolipid metabolism and ceramide production in HIV-dementia. Ann Neurol 55:257-267. (Pubitemid 38167003)
22. Hering H, Lin CC, Sheng M. 2003. Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J Neurosci 23:3262-3271. (Pubitemid 36531967)
23. Hirata H, Hibasami H, Yoshida T, Ogawa M, Matsumoto M, Morita A, Uchida A. 2001. Nerve growth factor signaling of p75 induces differentiation and ceramide-mediated apoptosis in Schwann cells cultured from degenerating nerves. Glia 36:245-258.
24. 2+-dependent neutral sphingomyelinase. Proc Natl Acad Sci U S A 97:5895-5900.
25. Inokuchi J, Mizutani A, Jimbo M, Usuki S, Yamagishi K, Mochizuki H, Muramoto K, Kobayashi K, Kuroda Y, Iwasaki K, Ohgami Y, Fujiwara M. 1997. Up-regulation of ganglioside biosynthesis, functional synapse formation, and memory retention by a synthetic ceramide analog (L-PDMP). Biochem Biophys Res Commun 237:595-600.
26. Ito A, Horigome K. 1995. Ceramide prevents neuronal programmed cell death induced by nerve growth factor deprivation. J Neurochem 65:463-466.
27. Kolmakova A, Kwiterovich P, Virgil D, Alaupovic P, Knight-Gibson C, Martin SF, Chatterjee S. 2004. Apolipoprotein C-I induces apoptosis in human aortic smooth muscle cells via recruiting neutral sphingomyelinase. Arterioscler Thromb Vasc Biol 24:264-269.
28. Lin Y, Skeberdis VA, Francesconi A, Bennett MV, Zukin RS. 2004. Postsynaptic density protein-95 regulates NMDA channel gating and surface expression. J Neurosci 24:10138-10148.
29. Luberto C, Hassler DF, Signorelli P, Okamoto Y, Sawai H, Boros E, Hazen-Martin DJ, Obeid LM, Hannun YA, Smith GK. 2002. Inhibition of tumor necrosis factor-induced cell death in MCF7 by a novel inhibitor of neutral sphingomyelinase. J Biol Chem 277:41128-41139.
30. Marchesini N, Hannun YA. 2004. Acid and neutral sphingomyelinases: roles and mechanisms of regulation. Biochem Cell Biol 82:27-44. (Pubitemid 38580872)
31. Melnikova T, Savonenko A, Wang Q, Liang X, Hand T, Wu L, Kaufmann WE, Vehmas A, Andreasson KI. 2006. Cycloxygenase-2 activity promotes cognitive deficits but not increased amyloid burden in a model of Alzheimer's disease in a sex-dimorphic pattern. Neuroscience 141:1149-1162. (Pubitemid 44128685)
32. Mizutani Y, Tamiya-Koizumi K, Irie F, Hirabayashi Y, Miwa M, Yoshida S. 2000. Cloning and expression of rat neutral sphingomyelinase: enzymological characterization and identification of essential histidine residues. Biochim Biophys Acta 1485:236-246. (Pubitemid 30314740)
33. Nakazawa K, McHugh TJ, Wilson MA, Tonegawa S. 2004. NMDA receptors, place cells and hippocampal spatial memory. Nat Rev Neurosci 5:361-372. (Pubitemid 38568497)
34. Nicol GD. 2008. Nerve growth factor, sphingomyelins, and sensitization in sensory neurons. Sheng Li Xue Bao 60:603-604.
35. 2+ from ryanodine receptor in developing cerebellar neurons. J Biol Chem 278:41259-41269.
36. Owen DM, Williamson D, Rentero C, Gaus K. 2009. Quantitative microscopy: protein dynamics and membrane organisation. Traffic 10:962-971.
37. Peng CH, Huang CN, Hsu SP, Wang CJ. 2006. Penta-acetyl geniposide induce apoptosis in C6 glioma cells by modulating the activation of neutral sphingomyelinase-induced p75 nerve growth factor receptor and protein kinase Cdelta pathway. Mol Pharmacol 70:997-1004.
38. Rao BG, Spence MW. 1976. Sphingomyelinase activity at pH 7.4 in human brain and a comparison to activity at pH 5.0. J Lipid Res 17:506-515.
39. 2+-triggered membrane fusion. J Cell Sci 119:2688-2694.
40. Rohrbough J, Rushton E, Palanker L, Woodruff E, Matthies HJ, Acharya U, Acharya JK, Broadie K. 2004. Ceramidase regulates synaptic vesicle exocytosis and trafficking. J Neurosci 24:7789-7803.
41. Savonenko A, Xu GM, Melnikova T, Morton JL, Gonzales V, Wong MP, Price DL, Tang F, Markowska AL, Borchelt DR. 2005. Episodiclike memory deficits in the APPswe/PS1dE9 mouse model of Alzheimer's disease: relationships to beta-amyloid deposition and neurotransmitter abnormalities. Neurobiol Dis 18:602-617.
42. Schneider PB, Kennedy EP. 1967. Sphingomyelinase in normal human spleens and in spleens from subjects with Niemann-Pick disease. J Lipid Res 8:202-209.
43. Schwegler H, Boldyreva M, Linke R, Wu J, Zilles K, Crusio WE. 1996. Genetic variation in the morphology of the septo-hippocampal cholinergic and GABAergic systems in mice: II. Morpho-behavioral correlations. Hippocampus 6:535-545.
44. Shaikh NA. 1994. Assessment of various techniques for the quantitative extraction of lysophospholipids from myocardial tissues. Anal Biochem 216:313-321.
45. Sipka S, Antal-Szalmas P, Szollosi I, Csipo I, Lakos G, Szegedi G. 2000. Ceramide stimulates the uptake of neutral red in human neutrophils, monocytes, and lymphocytes. Ann Hematol 79:83-85.
46. Smith AR, Visioli F, Frei B, Hagen TM. 2006. Age-related changes in endothelial nitric oxide synthase phosphorylation and nitric oxide dependent vasodilation: evidence for a novel mechanism involving sphingomyelinase and ceramide-activated phosphatase 2A. Aging Cell 5:391-400.
47. Stahelin RV. 2009. Lipid binding domains: more than simple lipid effectors. J Lipid Res 50(Suppl):S299-S304.
48. Steele RJ, Morris RG. 1999. Delay-dependent impairment of a matching-to-place task with chronic and intrahippocampal infusion of the NMDA-antagonist D-AP5. Hippocampus 9:118-136.
49. Stoffel W, Jenke B, Block B, Zumbansen M, Koebke J. 2005. Neutral sphingomyelinase 2 (smpd3) in the control of postnatal growth and development. Proc Natl Acad Sci U S A 102:4554-4559.
50. Stoffel W, Jenke B, Holz B, Binczek E, Gunter RH, Knifka J, Koebke J, Niehoff A. 2007. Neutral sphingomyelinase (SMPD3) deficiency causes a novel form of chondrodysplasia and dwarfism that is rescued by Col2A1-driven smpd3 transgene expression. Am J Pathol 171:153-161.
51. Swartz KJ. 2008. Sensing voltage across lipid membranes. Nature 456: 891-897.
52. Tabarean IV, Korn H, Bartfai T. 2006. Interleukin-1beta induces hyperpolarization and modulates synaptic inhibition in preoptic and anterior hypothalamic neurons. Neuroscience 141:1685-1695.
53. Takahashi E, Inanami O, Asanuma T, Kuwabara M. 2006. Effects of ceramide inhibition on radiation-induced apoptosis in human leukemia MOLT-4 cells. J Radiat Res 47:19-25. (Pubitemid 43788495)
54. Tomiuk S, Hofmann K, Nix M, Zumbansen M, Stoffel W. 1998. Cloned mammalian neutral sphingomyelinase: functions in sphingolipid signaling? Proc Natl Acad Sci U S A 95:3638-3643.
55. van Blitterswijk WJ, van der Luit AH, Veldman RJ, Verheij M, Borst J. 2003. Ceramide: second messenger or modulator of membrane structure and dynamics? Biochem J 369:199-211.
56. Walton KA, Gugiu BG, Thomas M, Basseri RJ, Eliav DR, Salomon RG, Berliner JA. 2006. A role for neutral sphingomyelinase activation in the inhibition of LPS action by phospholipid oxidation products. J Lipid Res 47:1967-1974. (Pubitemid 44401984)
57. Wheeler D, Knapp E, Bandaru VV, Wang Y, Knorr D, Poirier C, Mattson MP, Geiger JD, Haughey NJ. 2009. Tumor necrosis factor-alpha-induced neutral sphingomyelinase-2 modulates synaptic plasticity by controlling the membrane insertion of NMDA receptors. J Neurochem 109:1237-1249.
58. Yamagishi K, Mishima K, Ohgami Y, Iwasaki K, Jimbo M, Masuda H, Igarashi Y, Inokuchi J, Fujiwara M. 2003. A synthetic ceramide analog ameliorates spatial cognition deficit and stimulates biosynthesis of brain gangliosides in rats with cerebral ischemia. Eur J Pharmacol 462:53-60.
59. Yang SN. 2000. Ceramide-induced sustained depression of synaptic currents mediated by ionotropic glutamate receptors in the hippocampus: an essential role of postsynaptic protein phosphatases. Neuroscience 96:253-258.
60. + current in ceramide-induced caspase activation and apoptosis in cultured cortical neurons. J Neurochem 73:933-941.
61. Zhang YH, Nicol GD. 2004. NGF-mediated sensitization of the excitability of rat sensory neurons is prevented by a blocking antibody to the p75 neurotrophin receptor. Neurosci Lett 366:187-192.
62. + current in rat sensory neurons. J Physiol 544:385-402.