St8sia2 deficiency plus juvenile cannabis exposure in mice synergistically affect higher cognition in adulthood

Behavioural Brain Research

Volumn 275, Issue , 2014, Pages 166-175

  Tantra, Martesa ^a,b   Kröcher, Tim ^c   Papiol, Sergi ^a,b   Winkler, Daniela ^a,b   Röckle, Iris ^c   Jatho, Jasmin ^a   Burkhardt, Hannelore ^c   Ronnenberg, Anja ^a   Gerardy Schahn, Rita ^c   Ehrenreich, Hannelore ^a,b   Hildebrandt, Herbert ^c  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b Deutsche Forschungsgemeinschaft   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Learning index; NCAM; PolySia; Reference memory; Working memory; 9 THC

Indexed keywords

DRONABINOL; NERVE CELL ADHESION MOLECULE; POLYSIALIC ACID; PROTEIN ST8SIA2; SIALYLTRANSFERASE; UNCLASSIFIED DRUG; CMP-N-ACETYLNEURAMINATE-POLY-ALPHA-2,8-SIALOSYL SIALYLTRANSFERASE; PSYCHOTROPIC AGENT;

ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; CANNABIS USE; COGNITIVE DEFECT; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; FEMALE; GENOTYPE ENVIRONMENT INTERACTION; JUVENILE ANIMAL; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; SIALYLATION; WILD TYPE; AGE; ANIMAL; BRAIN; C57BL MOUSE; CHEMICALLY INDUCED; DEFICIENCY; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; MAZE TEST; MEMORY; METABOLISM; NEWBORN; TRANSGENIC MOUSE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BRAIN; CELL ADHESION MOLECULES, NEURONAL; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRONABINOL; GENE EXPRESSION REGULATION; MALE; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PSYCHOTROPIC DRUGS; SIALYLTRANSFERASES;

EID: 84907522841     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2014.08.062     Document Type: Article

References (65)

1. Malone D.T., Hill M.N., Rubino T. Adolescent cannabis use and psychosis: epidemiology and neurodevelopmental models. Br J Pharmacol 2010, 160:511-522.
2. Schneider M. Puberty as a highly vulnerable developmental period for the consequences of cannabis exposure. Addict Biol 2008, 13:253-263.
3. Ehrenreich H., Rinn T., Kunert H.J., Moeller M.R., Poser W., Schilling L., et al. Specific attentional dysfunction in adults following early start of cannabis use. Psychopharmacology 1999, 142:295.
4. Stepniak B., Papiol S., Hammer C., Ramin A., Everts S., Hennig L., et al. Accumulated environmental risk determining the onset of schizophrenia. Lancet Psychiatry 2014, [in press].
5. Bauman A., Phongsavan P. Epidemiology of substance use in adolescence: prevalence, trends and policy implications. Drug Alcohol Depend 1999, 55:187-207.
6. von Sydow K., Lieb R., Pfister H., Höfler M., Sonntag H., Wittchen H.U. The natural course of cannabis use, abuse and dependence over four years: a longitudinal community study of adolescents and young adults. Drug Alcohol Depend 2001, 64:347-361.
7. Berghuis P., Rajnicek A.M., Morozov Y.M., Ross R.A., Mulder J., Urbán G.M., et al. Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science 2007, 316:1212-1216.
8. Harkany T., Guzman M., Galve-Roperh I., Berghuis P., Devi L.A., Mackie M. The emerging functions of endocannabinoid signaling during CNS development. Trends Pharmacol Sci 2007, 28:83-92.
9. Harkany T., Keimpema E., Barabas K., Mulder J. Endocannabinoid functions controlling neuronal specification during brain development. Mol Cell Endocrinol 2008, 286:S84-S90.
10. Lubetzki C., Charles P., Stankoff B., Hernandez P., Zalc B. Pivotal role of axonal adhesion molecules in central nervous system myelination. Neurol Neurochir Pol 2000, 34:41-44.
11. Trezza V., Cuomo V., Vanderschuren L.J. Cannabis and the developing brain: insights from behavior. Eur J Pharmacol 2008, 585:441-452.
12. Wilson R.I., Nicoll R.A. Endocannabinoid signaling in the brain. Science 2002, 296:678-682.
13. James A., James C., Thwaites T. The brain effects of cannabis in healthy adolescents and in adolescents with schizophrenia: a systematic review. Psychiatry Res 2013, 214:181-189.
14. Cha Y.M., White A.M., Kuhn C.M., Wilson W.A., Swartzwelder H.S. Differential effects of delta9-THC on learning in adolescent and adult rats. Pharmacol Biochem Behav 2006, 83:448-455.
15. Hildebrandt H., Dityatev A. Polysialic acid in brain development and synaptic plasticity. Top Curr Chem 2013, [Epub ahead of print]. 10.1007/128_2013_446.
16. Hildebrandt H., Muhlenhoff M., Oltmann-Norden I., Rockle I., Burkhardt H., Weinhold B., et al. Imbalance of neural cell adhesion molecule and polysialyltransferase alleles causes defective brain connectivity. Brain 2009, 132:2831-2838.
17. Senkov O., Tikhobrazova O., Dityatev A. PSA-NCAM: synaptic functions mediated by its interactions with proteoglycans and glutamate receptors. Int J Biochem Cell Biol 2012, 44:591-595.
18. Maness P.F., Schachner M. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 2007, 10:19-26.
19. Schnaar R.L., Gerardy-Schahn R., Hildebrandt H. Sialic acids in the brain: gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. Physiol Rev 2014, 94:461-518.
20. Angata K., Long J.M., Bukalo O., Lee W., Dityatev A., Wynshaw-Boris A., et al. Sialyltransferase ST8Sia-II assembles a subset of polysialic acid that directs hippocampal axonal targeting and promotes fear behavior. J Biol Chem 2004, 279:32603-32613.
21. Eckhardt M., Bukalo O., Chazal G., Wang L., Goridis C., Schachner M., et al. Mice deficient in the polysialyltransferase ST8SiaIV/PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity. J Neurosci 2000, 20:5234-5244.
22. Nacher J., Guirado R., Varea E., Alonso-Llosa G., Rockle I., Hildebrandt H. Divergent impact of the polysialyltransferases ST8SiaII and ST8SiaIV on polysialic acid expression in immature neurons and interneurons of the adult cerebral cortex. Neuroscience 2010, 167:825-837.
23. Oltmann-Norden I., Galuska S.P., Hildebrandt H., Geyer R., Gerardy-Schahn R., Geyer H., et al. Impact of the polysialyltransferases ST8SiaII and ST8SiaIV on polysialic acid synthesis during postnatal mouse brain development. J Biol Chem 2008, 283:1463-1471.
24. Weinhold B., Seidenfaden R., Rockle I., Muhlenhoff M., Schertzinger F., Conzelmann S., et al. Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J Biol Chem 2005, 280:42971-42977.
25. Calandreau L., Marquez C., Bisaz R., Fantin M., Sandi C. Differential impact of polysialyltransferase ST8SiaII and ST8SiaIV knockout on social interaction and aggression. Genes Brain Behav 2010, 9:958-967.
26. Krocher T., Malinovskaja K., Jurgenson M., Aonurm-Helm A., Zharkovskaya T., Kalda A., et al. Schizophrenia-like phenotype of polysialyltransferase ST8SIA2-deficient mice. Brain Struct Funct 2013, [E-pub ahead of print]. 10.1007/s00429-013-0638-z.
27. Markram K., Gerardy-Schahn R., Sandi C. Selective learning and memory impairments in mice deficient for polysialylated NCAM in adulthood. Neuroscience 2007, 144:788-796.
28. Senkov O., Sun M., Weinhold B., Gerardy-Schahn R., Schachner M., Dityatev A. Polysialylated neural cell adhesion molecule is involved in induction of long-term potentiation and memory acquisition and consolidation in a fear-conditioning paradigm. J Neurosci 2006, 26:10888-109898.
29. Higuera-Matas A., Botreau F., Miguens M., Del Olmo N., Borcel E., Pérez-Alvarez L., et al. Chronic periadolescent cannabinoid treatment enhances adult hippocampal PSA-NCAM expression in male Wistar rats but only has marginal effects on anxiety, learning and memory. Pharmacol Biochem Behav 2009, 93:482-490.
30. Mackowiak M., Chocyk A., Dudys D., Wedzony K. Activation of CB1 cannabinoid receptors impairs memory consolidation and hippocampal polysialylated neural cell adhesion molecule expression in contextual fear conditioning. Neuroscience 2009, 158:1708-1716.
31. Mackowiak M., Chocyk A., Markowicz-Kula K., Wedzony K. Acute activation of CB1 cannabinoid receptors transiently decreases PSA-NCAM expression in the dentate gyrus of the rat hippocampus. Brain Res 2007, 1148:43-52.
32. Dere E., Dahm L., Lu D., Hammerschmidt K., Ju A., Tantra M., et al. Heterozygous Ambra1 deficiency in mice: a genetic trait with autism-like behavior restricted to the female gender. Front Behav Neurosci 2014, 8:181.
33. El-Kordi A., Winkler D., Hammerschmidt K., Kastner A., Krueger D., Ronnenberg A., et al. Development of an autism severity score for mice using Nlgn4 null mutants as a construct-valid model of heritable monogenic autism. Behav Brain Res 2013, 251:41-49.
34. Kuc K.A., Gregersen B.M., Gannon K.S., Dodart J.C. Holeboard discrimination learning in mice. Genes Brain Behav 2006, 5:355-363.
35. Champagne D., Dupuy J.B., Rochford J., Poirier J. Apolipoprotein E knockout mice display procedural deficits in the Morris water maze: analysis of learning strategies in three versions of the task. Neuroscience 2002, 114:641-654.
36. Gibertini M. IL1 beta impairs relational but not procedural rodent learning in a water maze task. Adv Exp Med Biol 1996, 402:207-217.
37. Hodges H. Maze procedures: the radial-arm and water maze compared. Brain Res Cogn Brain Res 1996, 3:167-181.
38. Roullet P., Lassalle J.M. Behavioural strategies, sensorial processes and hippocampal mossy fibre distribution in radial maze performance in mice. Behav Brain Res 1992, 48:77-85.
39. Hirn M., Ghandour M.S., Deagostini-Bazin H., Goridis C. Molecular heterogeneity and structural evolution during cerebellar ontogeny detected by monoclonal antibody of the mouse cell surface antigen BSP-2. Brain Res 1983, 265:87-100.
40. Frosch M., Gorgen I., Boulnois G.J., Timmis K.N., Bitter-Suermann D. NZB mouse system for production of monoclonal antibodies to weak bacterial antigens: isolation of an IgG antibody to the polysaccharide capsules of Escherichia coli K1 and group B meningococci. Proc Natl Acad Sci USA 1985, 82:1194-1198.
41. Schiff M., Rockle I., Burkhardt H., Weinhold B., Hildebrandt H. Thalamocortical pathfinding defects precede degeneration of the reticular thalamic nucleus in polysialic acid-deficient mice. J Neurosci 2011, 31:1302-1312.
42. Stummeyer K., Dickmanns A., Muhlenhoff M., Gerardy-Schahn R., Ficner R. Crystal structure of the polysialic acid-degrading endosialidase of bacteriophage K1F. Nat Struct Mol Biol 2005, 12:90-96.
43. Reagan-Shaw S., Nihal M., Ahmad N. Dose translation from animal to human studies revisited. FASEB J 2008, 22:659-661.
44. Fant R.V., Heishman S.J., Bunker E.B., Pickworth W.B. Acute and residual effects of marijuana in humans. Pharmacol Biochem Behav 1998, 60:777-784.
45. Hart C.L., van Gorp W., Haney M., Foltin R.W., Fischman M.W. Effects of acute smoked marijuana on complex cognitive performance. Neuropsychopharmacology 2001, 25:757-765.
46. Lane S.D., Cherek D.R., Tcheremissine O.V., Lieving L.M., Pietras C.J. Acute marijuana effects on human risk taking. Neuropsychopharmacology 2005, 30:800-809.
47. Schuster T., Krug M., Stalder M., Hackel N., Gerardy-Schahn R., Schachner M. Immunoelectron microscopic localization of the neural recognition molecules L1, NCAM, and its isoform NCAM180, the NCAM-associated polysialic acid, beta1 integrin and the extracellular matrix molecule tenascin-R in synapses of the adult rat hippocampus. J Neurobiol 2001, 49:142-158.
48. Schuster T., Krug M., Hassan H., Schachner M. Increase in proportion of hippocampal spine synapses expressing neural cell adhesion molecule NCAM180 following long-term potentiation. J Neurobiol 1998, 37:359-372.
49. Stoenica L., Senkov O., Gerardy-Schahn R., Weinhold B., Schachner M., Dityatev A. In vivo synaptic plasticity in the dentate gyrus of mice deficient in the neural cell adhesion molecule NCAM or its polysialic acid. Eur J Neurosci 2006, 23:2255-2264.
50. Anney R., Klei L., Pinto D., Almeida J., Bacchelli E., Baird G., et al. Individual common variants exert weak effects on the risk for autism spectrum disorders. Hum Mol Genet 2012, 21:4781-4792.
51. Anney R., Klei L., Pinto D., Regan R., Conroy J., Magalhaes T.R., et al. A genome-wide scan for common alleles affecting risk for autism. Hum Mol Genet 2010, 19:4072-4082.
52. Arai M., Yamada K., Toyota T., Obata N., Haga S., Yoshida Y., et al. Association between polymorphisms in the promoter region of the sialyltransferase 8B (SIAT8B) gene and schizophrenia. Biol Psychiatry 2006, 59:652-659.
53. Brennaman L.H., Maness P.F. NCAM in neuropsychiatric and neurodegenerative disorders. Adv Exp Med Biol 2010, 663:299-317.
54. Maziade M., Roy M.A., Chagnon Y.C., Cliche D., Fournier J.P., Montgrain N., et al. Shared and specific susceptibility loci for schizophrenia and bipolar disorder: a dense genome scan in Eastern Quebec families. Mol Psychiatry 2005, 10:486-499.
55. McAuley E.Z., Scimone A., Tiwari Y., Agahi G., Mowry B.J., Holliday E.G., et al. Identification of sialyltransferase 8 B as a generalized susceptibility gene for psychotic and mood disorders on chromosome 15q25-26. PLoS ONE 2012, 7:e38172.
56. Copeland J., Rooke S., Swift W. Changes in cannabis use among young people: impact on mental health. Curr Opin Psychiatry 2013, 26:325-329.
57. Karila L., Roux P., Rolland B., Benyamina A., Reynaud M., Aubin H.J., et al. Acute and long-term effects of cannabis use: a review. Curr Pharm Des 2013, 20:4112-4118.
58. Varvel S.A., Hamm R.J., Martin B.R., Lichtman A.H. Differential effects of delta 9-THC on spatial reference and working memory in mice. Psychopharmacology (Berl) 2001, 157:142-150.
59. Kreuz D.S., Axelrod J. Delta-9-tetrahydrocannabinol: localization in body fat. Science 1973, 179:391-393.
60. Solowij N., Michie P.T., Fox A.M. Effects of long-term cannabis use on selective attention: an event-related potential study. Pharmacol Biochem Behav 1991, 40:683-688.
61. Solowij N. Do cognitive impairments recover following cessation of cannabis use?. Life Sci 1995, 56:2119-2126.
62. Jacob W., Marsch R., Marsicano G., Lutz B., Wotjak C.T. Cannabinoid CB1 receptor deficiency increases contextual fear memory under highly aversive conditions and long-term potentiation in vivo. Neurobiol Learn Mem 2012, 98:47-55.
63. Kirkby D.L., Higgins G.A. Characterization of perforant path lesions in rodent models of memory and attention. Eur J Neurosci 1998, 10:823-838.
64. Bonfanti L., Theodosis D.T. Polysialic acid and activity-dependent synapse remodeling. Cell Adh Migr 2009, 3:43-50.
65. Gascon E., Vutskits L., Kiss J.Z. Polysialic acid-neural cell adhesion molecule in brain plasticity: from synapses to integration of new neurons. Brain Res Rev 2007, 56:101-118.