Different Forms of MARCKS Protein Are Involved in Memory Formation in the Learning Process of Imprinting

Overview

Journal Exp Brain Res

Specialty Neurology

Date 2008 Jun 3

PMID 18516597

Citations 16

Authors

Revaz O Solomonia

David Apkhazava

Maia Nozadze

Antony P Jackson

Brian J McCabe

Gabriel Horn

Affiliations

Soon will be listed here.

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.

Citing Articles

Src-NADH dehydrogenase subunit 2 complex and recognition memory of imprinting in domestic chicks.

Chitadze L, Meparishvili M, Lagani V, Khuchua Z, McCabe B, Solomonia R PLoS One. 2024; 19(1):e0297166.

PMID: 38285689 PMC: 10824410. DOI: 10.1371/journal.pone.0297166.

Src and Memory: A Study of Filial Imprinting and Predispositions in the Domestic Chick.

Meparishvili M, Chitadze L, Lagani V, McCabe B, Solomonia R Front Physiol. 2021; 12:736999.

PMID: 34616310 PMC: 8488273. DOI: 10.3389/fphys.2021.736999.

Visual Imprinting in Birds: Behavior, Models, and Neural Mechanisms.

McCabe B Front Physiol. 2019; 10:658.

PMID: 31231236 PMC: 6558373. DOI: 10.3389/fphys.2019.00658.

Micro-RNAs, their target proteins, predispositions and the memory of filial imprinting.

Margvelani G, Meparishvili M, Kiguradze T, McCabe B, Solomonia R Sci Rep. 2018; 8(1):17444.

PMID: 30487553 PMC: 6262022. DOI: 10.1038/s41598-018-35097-w.

Effects of NMDAR Antagonist on the Regulation of P-MARCKS Protein to Aβ Oligomers Induced Neurotoxicity.

Liu Y, Zhang P, Zheng Y, Yang C, Du T, Ge M Neurochem Res. 2018; 43(10):2008-2015.

PMID: 30155805 DOI: 10.1007/s11064-018-2622-8.

References

Matus A . MARCKS for maintenance in dendritic spines. Neuron. 2005; 48(1):4-5. DOI: 10.1016/j.neuron.2005.09.013. View

McNamara R, Stumpo D, Morel L, Lewis M, Wakeland E, Blackshear P . 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 U S A. 1998; 95(24):14517-22. PMC: 24405. DOI: 10.1073/pnas.95.24.14517. View

Swierczynski S, Blackshear P . Membrane association of the myristoylated alanine-rich C kinase substrate (MARCKS) protein. Mutational analysis provides evidence for complex interactions. J Biol Chem. 1995; 270(22):13436-45. DOI: 10.1074/jbc.270.22.13436. View

Horn G, Bradley P, McCabe B . Changes in the structure of synapses associated with learning. J Neurosci. 1985; 5(12):3161-8. PMC: 6565237. View

Thelen M, Rosen A, Nairn A, Aderem A . Regulation by phosphorylation of reversible association of a myristoylated protein kinase C substrate with the plasma membrane. Nature. 1991; 351(6324):320-2. DOI: 10.1038/351320a0. View

Bredenkotter M, Braun K . Changes of neuronal responsiveness in the mediorostral neostriatum/hyperstriatum after auditory filial imprinting in the domestic chick. Neuroscience. 1997; 76(2):355-65. DOI: 10.1016/s0306-4522(96)00381-8. View

Reiner A, Perkel D, Bruce L, Butler A, Csillag A, Kuenzel W . Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol. 2004; 473(3):377-414. PMC: 2518311. DOI: 10.1002/cne.20118. View

Bolhuis J . Mechanisms of avian imprinting: a review. Biol Rev Camb Philos Soc. 1991; 66(4):303-45. DOI: 10.1111/j.1469-185x.1991.tb01145.x. View

Ramakers G, McNamara R, Lenox R, De Graan P . Differential changes in the phosphorylation of the protein kinase C substrates myristoylated alanine-rich C kinase substrate and growth-associated protein-43/B-50 following Schaffer collateral long-term potentiation and long-term depression. J Neurochem. 1999; 73(5):2175-83. View

10.

Aderem A . The MARCKS brothers: a family of protein kinase C substrates. Cell. 1992; 71(5):713-6. DOI: 10.1016/0092-8674(92)90546-o. View

11.

Solomonia R, McCabe B, Horn G . Neural cell adhesion molecules, learning, and memory in the domestic chick. Behav Neurosci. 1998; 112(3):646-55. DOI: 10.1037//0735-7044.112.3.646. View

12.

Stumpo D, Graff J, Albert K, Greengard P, Blackshear P . Molecular cloning, characterization, and expression of a cDNA encoding the "80- to 87-kDa" myristoylated alanine-rich C kinase substrate: a major cellular substrate for protein kinase C. Proc Natl Acad Sci U S A. 1989; 86(11):4012-6. PMC: 287378. DOI: 10.1073/pnas.86.11.4012. View

13.

Newton A, Johnson J . Protein kinase C: a paradigm for regulation of protein function by two membrane-targeting modules. Biochim Biophys Acta. 1998; 1376(2):155-72. DOI: 10.1016/s0304-4157(98)00003-3. View

14.

Meberg P, McCabe B, Routtenberg A . MARCKS and protein F1/GAP-43 mRNA in chick brain: effects of imprinting. Brain Res Mol Brain Res. 1996; 35(1-2):149-56. DOI: 10.1016/0169-328x(95)00200-c. View

15.

Bradley P, Horn G, Bateson P . Imprinting. An electron microscopic study of chick hyperstriatum ventrale. Exp Brain Res. 1981; 41(2):115-20. DOI: 10.1007/BF00236600. View

16.

Johnston A, Rogers L, Dodd P . [3H]MK-801 binding asymmetry in the IMHV region of dark-reared chicks is reversed by imprinting. Brain Res Bull. 1995; 37(1):5-8. DOI: 10.1016/0361-9230(94)00249-5. View

17.

Solomonia R, Morgan K, Kotorashvili A, McCabe B, Jackson A, Horn G . 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. 2003; 17(5):1073-81. DOI: 10.1046/j.1460-9568.2003.02539.x. View

18.

Ouimet C, Wang J, Walaas S, Albert K, Greengard P . Localization of the MARCKS (87 kDa) protein, a major specific substrate for protein kinase C, in rat brain. J Neurosci. 1990; 10(5):1683-98. PMC: 6570084. View

19.

Fifkova E, Morales M . Actin matrix of dendritic spines, synaptic plasticity, and long-term potentiation. Int Rev Cytol. 1992; 139:267-307. DOI: 10.1016/s0074-7696(08)61414-x. View

20.

Sheu F, McCabe B, Horn G, Routtenberg A . Learning selectively increases protein kinase C substrate phosphorylation in specific regions of the chick brain. Proc Natl Acad Sci U S A. 1993; 90(7):2705-9. PMC: 46164. DOI: 10.1073/pnas.90.7.2705. View