Role for NUP62 depletion and PYK2 redistribution in dendritic retraction resulting from chronic stress

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 45, 2014, Pages 16130-16135

  Kinoshita, Yayoi ^a   Hunter, Richard G ^b,c   Gray, Jason D ^b   Mesias, Roxana ^a   McEwen, Bruce S ^c   Benson, Deanna L ^a   Kohtz, D Stave ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c UNIVERSITY OF MASSACHUSETTS BOSTON   (United States)

Author keywords

Chronic stress; Dendrite retraction; Hippocampus; Nucleoporin p62; Proline rich tyrosine kinase 2

Indexed keywords

FOCAL ADHESION KINASE 2; NUCLEOPORIN; NUCLEOPORIN P62; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; NUCLEAR PORE PROTEIN P62; NUP62 PROTEIN, MOUSE; PTK2B PROTEIN, MOUSE;

ALPHA HELIX; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL LEVEL; CELL NUCLEUS; CHRONIC STRESS; CONSENSUS SEQUENCE; CONTROLLED STUDY; CYTOPLASM; DENDRITE; EMBRYO; EMBRYO CELL; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; HIPPOCAMPAL NEURONAL CULTURE; HIPPOCAMPUS; IMMUNOFLUORESCENCE MICROSCOPY; MOUSE; NERVE FIBER; NONHUMAN; NUCLEAR PORE COMPLEX; PROTEIN CONTENT; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; RAT; ANIMAL; CHRONIC DISEASE; GENETICS; HIPPOCAMPAL CA3 REGION; HUMAN; MENTAL STRESS; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; AXONS; CA3 REGION, HIPPOCAMPAL; CHRONIC DISEASE; DENDRITES; FOCAL ADHESION KINASE 2; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; NUCLEAR PORE COMPLEX PROTEINS; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PSYCHOLOGICAL;

EID: 84909609613     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1418896111     Document Type: Article

References (53)

1. Beck M, et al. (2004) Nuclear pore complex structure and dynamics revealed by cryoelectron tomography. Science 306(5700):1387-1390.
2. Liang Y, Hetzer MW (2011) Functional interactions between nucleoporins and chromatin. Curr Opin Cell Biol 23(1):65-70.
3. Capelson M, et al. (2010) Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell 140(3):372-383.
4. Kalverda B, Pickersgill H, Shloma VV, Fornerod M (2010) Nucleoporins directly stimulate expression of developmental and cell-cycle genes inside the nucleoplasm. Cell 140(3):360-371.
5. Raices M, D'Angelo MA (2012) Nuclear pore complex composition: A new regulator of tissue-specific and developmental functions. Nat Rev Mol Cell Biol 13(11):687-699.
6. Gomez-Cavazos JS, Hetzer MW (2012) Outfits for different occasions: Tissue-specific roles of Nuclear Envelope proteins. Curr Opin Cell Biol 24(6):775-783.
7. Basel-Vanagaite L, et al. (2006) Mutated nup62 causes autosomal recessive infantile bilateral striatal necrosis. Ann Neurol 60(2):214-222.
8. Wellcome Trust Sanger Institute (2009) Alleles produced for the KOMP project by the Wellcome Trust Sanger Institute. MGI Direct Data Submission, J: 148605.
9. Watanabe Y, Gould E, Cameron HA, Daniels DC, McEwen BS (1992) Phenytoin prevents stress- and corticosterone-induced atrophy of CA3 pyramidal neurons. Hippocampus 2(4):431-435.
10. Magariños AM, Verdugo JM, McEwen BS (1997) Chronic stress alters synaptic terminal structure in hippocampus. Proc Natl Acad Sci USA 94(25):14002-14008.
11. McEwen BS (1999) Stress and hippocampal plasticity. Annu Rev Neurosci 22:105-122.
12. McEwen BS, Eiland L, Hunter RG, Miller MM (2012) Stress and anxiety: Structural plasticity and epigenetic regulation as a consequence of stress. Neuropharmacology 62(1):3-12.
13. Tochigi M, et al. (2008) Gene expression profiling of major depression and suicide in the prefrontal cortex of postmortem brains. Neurosci Res 60(2):184-191.
14. Gray JD, Rubin TG, Hunter RG, McEwen BS (2013) Hippocampal gene expression changes underlying stress sensitization and recovery. Mol Psychiatry (17): 175.
15. Heiman M, et al. (2008) A translational profiling approach for the molecular characterization of CNS cell types. Cell 135(4):738-748.
16. Hornbeck PV, et al. (2012) PhosphoSitePlus: A comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res 40(Database issue):D261-D270.
17. Blom N, Gammeltoft S, Brunak S (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294(5):1351-1362.
18. Magariños AM, Deslandes A, McEwen BS (1999) Effects of antidepressants and benzodiazepine treatments on the dendritic structure of CA3 pyramidal neurons after chronic stress. Eur J Pharmacol 371(2-3):113-122.
19. Yang S, Roselli F, Patchev AV, Yu S, Almeida OF (2013) Non-receptor-tyrosine kinases integrate fast glucocorticoid signaling in hippocampal neurons. J Biol Chem 288(33):23725-23739.
20. Li X, Dy RC, Cance WG, Graves LM, Earp HS (1999) Interactions between two cytoskeleton-associated tyrosine kinases: Calcium-dependent tyrosine kinase and focal adhesion tyrosine kinase. J Biol Chem 274(13):8917-8924.
21. Aoto H, Sasaki H, Ishino M, Sasaki T (2002) Nuclear translocation of cell adhesion kinase beta/proline-rich tyrosine kinase 2. Cell Struct Funct 27(1):47-61.
22. Corvol JC, et al. (2005) Depolarization activates ERK and proline-rich tyrosine kinase 2(PYK2) independently in different cellular compartments in hippocampal slices. J Biol Chem 280(1):660-668.
23. Roberts WG, et al. (2008) Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562, 271. Cancer Res 68(6):1935-1944.
24. Dikic I, Tokiwa G, Lev S, Courtneidge SA, Schlessinger J (1996) A role for Pyk2 and Src in linking G-protein-coupled receptors with MAP kinase activation. Nature 383(6600):547-550.
25. Kosik KS, Finch EA (1987) MAP2 and tau segregate into dendritic and axonal domains after the elaboration of morphologically distinct neurites: An immunocytochemical study of cultured rat cerebrum. J Neurosci 7(10):3142-3153.
26. Tashiro K, Hasegawa M, Ihara Y, Iwatsubo T (1997) Somatodendritic localization of phosphorylated tau in neonatal and adult rat cerebral cortex. Neuroreport 8(12):2797-2801.
27. Bradke F, Dotti CG (2000) Differentiated neurons retain the capacity to generate axons from dendrites. Curr Biol 10(22):1467-1470.
28. Schafer DP, et al. (2009) Disruption of the axon initial segment cytoskeleton is a new mechanism for neuronal injury. J Neurosci 29(42):13242-13254.
29. Kinoshita Y, Kalir T, Dottino P, Kohtz DS (2012) Nuclear distributions of NUP62 and NUP214 suggest architectural diversity and spatial patterning among nuclear pore complexes. PLoS ONE 7(4):e36137.
30. Matus A, Biou V, Brinkhaus H, Roelandse M (2007) Transfecting cultured hippocampal neurons with an actin-GFP plasmid. CSH Protoc 2007: pdb.prot4664.
31. Donohue HS, et al. (2006) Chronic restraint stress induces changes in synapse morphology in stratum lacunosum-moleculare CA1 rat hippocampus: A stereological and three-dimensional ultrastructural study. Neuroscience 140(2):597-606.
32. Hensley K, Venkova K, Christov A, Gunning W, Park J (2011) Collapsin response mediator protein-2: An emerging pathologic feature and therapeutic target for neurodisease indications. Mol Neurobiol 43(3):180-191.
33. Magariños AM, McEwen BS (1995) Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: Involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 69(1):89-98.
34. Christian KM, Miracle AD, Wellman CL, Nakazawa K (2011) Chronic stress-induced hippocampal dendritic retraction requires CA3 NMDA receptors. Neuroscience 174:26-36.
35. Huang Y, et al. (2001) CAKbeta/Pyk2 kinase is a signaling link for induction of longterm potentiation in CA1 hippocampus. Neuron 29(2):485-496.
36. Hsin H, Kim MJ, Wang CF, Sheng M (2010) Proline-rich tyrosine kinase 2 regulates hippocampal long-term depression. J Neurosci 30(36):11983-11993.
37. Faure C, Ramos M, Girault JA (2013) Pyk2 cytonuclear localization: Mechanisms and regulation by serine dephosphorylation. Cell Mol Life Sci 70(1):137-152.
38. Makio T, Lapetina DL, Wozniak RW (2013) Inheritance of yeast nuclear pore complexes requires the Nsp1p subcomplex. J Cell Biol 203(2):187-196.
39. Kinoshita Y, Kalir T, Rahaman J, Dottino P, Kohtz DS (2012) Alterations in nuclear pore architecture allow cancer cell entry into or exit from drug-resistant dormancy. Am J Pathol 180(1):375-389.
40. Echeverría PC, et al. (2009) Nuclear import of the glucocorticoid receptor-hsp90 complex through the nuclear pore complex is mediated by its interaction with Nup62 and importin beta. Mol Cell Biol 29(17):4788-4797.
41. D'Angelo MA, Raices M, Panowski SH, Hetzer MW (2009) Age-dependent deterioration of nuclear pore complexes causes a loss of nuclear integrity in postmitotic cells. Cell 136(2):284-295.
42. Solmaz SR, Chauhan R, Blobel G, Melcák I (2011) Molecular architecture of the transport channel of the nuclear pore complex. Cell 147(3):590-602.
43. Andrew CD, Warwicker J, Jones GR, Doig AJ (2002) Effect of phosphorylation on alpha-helix stability as a function of position. Biochemistry 41(6):1897-1905.
44. Lu Z, Hunter T (2009) Degradation of activated protein kinases by ubiquitination. Annu Rev Biochem 78:435-475.
45. Oh YS, et al. (2013) SMARCA3, a chromatin-remodeling factor, is required for p11-dependent antidepressant action. Cell 152(4):831-843.
46. Goslin K, Asmussen H, Banker G (1998) Rat hippocampal neurons in low-density culture. Culturing Nerve Cells, eds Banker G, Goslin K (MIT Press, Cambridge, MA), pp 339-370.
47. Chen Y, et al. (2008) NS21: Re-defined and modified supplement B27 for neuronal cultures. J Neurosci Methods 171(2):239-247.
48. Perez-Polo JR, Werbach-Perez K, Tiffany-Castiglioni E (1979) A human clonal cell line model of differentiating neurons. Dev Biol 71(2):341-355.
49. Hunter RG, et al. (2009) Regulation of kainate receptor subunit mRNA by stress and corticosteroids in the rat hippocampus. PLoS ONE 4(1):e4328.
50. Suzuki K, Bose P, Leong-Quong RY, Fujita DJ, Riabowol K (2010) REAP: A two minute cell fractionation method. BMC Res Notes 3(294):294.
51. Meijering E, et al. (2004) Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 58(2):167-176.
52. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671-675.
53. Lin K, Simossis VA, Taylor WR, Heringa J (2005) A simple and fast secondary structure prediction method using hidden neural networks. Bioinformatics 21(2):152-159.