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Different forms of MARCKS protein are involved in memory formation in the learning process of imprinting

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Abstract

There is strong evidence that a restricted part of the chick forebrain, the IMM (formerly IMHV), stores information acquired through the learning process of visual imprinting. Twenty-four hours after imprinting training, a learning-specific increase in amount of myristoylated, alanine-rich C-kinase substrate (MARCKS) protein is known to occur in the homogenate fraction of IMM. We investigated the two components of this fraction, membrane-bound and cytoplasmic-phosphorylated MARCKS. In IMM, amount of membrane-bound MARCKS, but not of cytoplasmic-phosphorylated MARCKS, increased as chicks learned. No changes were observed for either form of MARCKS in PPN, a control forebrain region. The results indicate that there is a learning-specific increase in membrane-bound, non-phosphorylated MARCKS 24 h after training. This increase might contribute to stabilization of synaptic morphology.

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Abbreviations

ANOVA:

Analysis of variance

Df:

Degrees of freedom

MARCKS:

Myristoylated alanine-rich C-kinase substrate

m-MARCKS:

Membrane-associated MARCKS

cp-MARCKS:

Cytoplasmic-phosphorylated MARCKS

IMM:

Intermediate and medial mesopallium

P :

Probability

PKC:

Protein kinase C

PPN:

Posterior pole of the nidopallium

SEM:

Standard error of the mean

References

  • Aderem A (1992) The MARCKS brothers—a family of protein kinase C substrates. Cell 71:713–716

    Article  PubMed  CAS  Google Scholar 

  • Arbuzova A, Schmitz AAP, Vergeres G (2002) Cross-talk unfolded: MARCKS proteins. Biochem J 362:1–12

    Article  PubMed  CAS  Google Scholar 

  • Bolhuis JJ (1991) Mechanisms of avian imprinting: a review. Biol Rev 66:303–345

    Article  PubMed  CAS  Google Scholar 

  • Bolhuis JJ, Cook S, Horn G (2000) Getting better all the time: improving preference scores reflect increases in the strength of filial imprinting. Anim Behav 59:1153–1159

    Article  PubMed  Google Scholar 

  • Bradley P, Horn G, Bateson P (1981) Imprinting: an electron microscopic study of chick hyperstriatum ventrale. Exp Brain Res 41:115–120

    PubMed  CAS  Google Scholar 

  • Bredenkotter M, Braun K (1997) Changes of neuronal responsiveness in the mediorostral neostriatum/hyperstriatum after auditory filial imprinting in the domestic chick. Neuroscience 76:355–365

    Article  PubMed  CAS  Google Scholar 

  • Calabrese B, Halpain S (2005) Essential role for the PKC target MARCKS in maintaining dendritic spine morphology. Neuron 48:77–90

    Article  PubMed  CAS  Google Scholar 

  • Fifkova E, Morales M (1992) Actin matrix of dendritic spines, synaptic plasticity, and long-term potentiation. Int Rev Cytol 139:267–307

    Article  PubMed  CAS  Google Scholar 

  • Horn G (1985) Memory, imprinting and the brain. Oxford University Press, Oxford

    Google Scholar 

  • Horn G (1991) Technique for removing IMHV from the chick brain. In: Andrew RJ (ed) Neural and behavioural plasticity. The use of the domestic chick as a model. Oxford University Press, Oxford, pp 44–48

    Google Scholar 

  • Horn G (2004) Pathways of the past: the imprint of memory. Nat Rev Neurosci 5:108–120

    Article  PubMed  CAS  Google Scholar 

  • Horn G, Bradley P, McCabe BJ (1985) Changes in the structure of synapses associated with learning. J Neurosci 5:3161–3168

    PubMed  CAS  Google Scholar 

  • Johnston AN, Rogers LJ, Dodd PR (1995) [H3]MK-801 binding asymmetry in the IMHV region of dark-reared chicks is reversed by imprinting. Brain Res Bull 37:5–8

    Article  PubMed  CAS  Google Scholar 

  • Matus A (2005) MARCKS for maintenance in dendritic spines. Neuron 48:4–5

    Article  PubMed  CAS  Google Scholar 

  • McNamara RK, Hussain RJ, Simon EJ, Stumpo DJ, Blackshear PJ, Abel T, Lenox RH (2005) Effect of myristoylated alanine-rich C kinase substrate (MARCKS) overexpression on hippocampus-dependent learning and hippocampal synaptic plasticity in MARCKS transgenic mice. Hippocampus 15:675–683

    Article  PubMed  CAS  Google Scholar 

  • McNamara RK, Stumpo DJ, Morel LM, Lewis MH, Wakeland EK, Blackshear PJ, Lenox RH (1998) Effect of reduced myristoylated alanine-rich C kinase substrate expression on hippocampal mossy fiber development and spatial learning in mutant mice: transgenic rescue and interactions with gene background. Proc Natl Acad Sci USA 95:14517–14522

    Article  PubMed  CAS  Google Scholar 

  • Meberg PJ, McCabe BJ, Routtenberg A (1996) Marcks and protein f1/gap-43 messenger-RNA in chick brain—effects of imprinting. Molecular Brain Research 35:149–156

    Article  PubMed  CAS  Google Scholar 

  • Newton AC, Johnson JJ (1998) Protein kinase C: a paradigm for regulation of protein function by two membrane-targeting modules. BioChim Biophys Acta Rev Biomembranes 1376:155–172

    Article  CAS  Google Scholar 

  • Ouimet CC, Wang JKT, Walaas SI, Albert KA, Greengard P (1990) Localization of the Marcks (87-kda) protein, a major specific substrate for protein kinase-C, in rat-brain. J Neurosci 10:1683–1698

    PubMed  CAS  Google Scholar 

  • Ramakers GM, McNamara RK, Lenox RH, De Graan PN (1999) Differential changes in the phosphorylation of the protein kinase C substrates myristoylated alanini-rich C kinase substrate and growth associated protein 43/B-50 following Schaffer collateral long-term potentiation and long-term depression. J Neurochem 73:2175–2183

    PubMed  CAS  Google Scholar 

  • Reiner A et al (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377–414

    Article  PubMed  Google Scholar 

  • Sheu FS, McCabe BJ, Horn G, Routtenberg A (1993) Learning selectively increases protein kinase C substrate phorphorylation in specific regions of the chick brain. Proc Natl Acad Sci USA 90:2705–2709

    Article  PubMed  CAS  Google Scholar 

  • Sluckin W (1972) Imprinting and early learning. Methuen, London

    Google Scholar 

  • Snedecor GW, Cochran WG (1989) Statistical methods. Iowa State University Press, Ames

    Google Scholar 

  • Solomonia RO, McCabe BJ, Horn G (1998) Neural cell adhesion molecules, learning and memory. Behav Neurosci 112:646–655

    Article  PubMed  CAS  Google Scholar 

  • Solomonia RO, Morgan K, Kotorashvili A, McCabe BJ, Jackson AP, Horn G (2003) Analysis of differential gene expression supports a role for amyloid precursor protein and a protein kinase C substrate (MARCKS) in long-term memory. Eur J Neurosci 17:1073–1081

    Article  PubMed  CAS  Google Scholar 

  • Stumpo DJ, Graff JM, Albert KA, Greengard P, Blackshear PJ (1989) Molecular-cloning, characterization, and expression of a cDNA encoding the 80-kda to 87-kda myristoylated alanine-rich c-kinase substrate—a major cellular substrate for protein kinase C. Proc Natl Acad Sci USA 86:4012–4016

    Article  PubMed  CAS  Google Scholar 

  • Swierczynski SL, Blackshear PJ (1995) Membrane association of the myristoylated alanine-rich C kinase substrate (MARCKS) protein. J Biol Chem 270:13436–13445

    Article  PubMed  CAS  Google Scholar 

  • Thelen M, Rosen A, Nairn AC, Aderem A (1991) Regulation by phosphorylation of reversible association of a myristoylated protein-kinase-c substrate with the plasma-membrane. Nature 351:320–322

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are grateful to the Royal Society and the BBSRC for financial support and to Drs. P. J. Blackshear and D. J. Stumpo, National Institute of Environmental Health Sciences, Duke University, USA for the gift of anti-MARCKS antibody.

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Correspondence to Brian J. McCabe.

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Solomonia, R.O., Apkhazava, D., Nozadze, M. et al. Different forms of MARCKS protein are involved in memory formation in the learning process of imprinting. Exp Brain Res 188, 323–330 (2008). https://doi.org/10.1007/s00221-008-1428-3

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  • DOI: https://doi.org/10.1007/s00221-008-1428-3

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