Skip to main content

Advertisement

Log in

Age-dependent changes in neuronal distribution of CacyBP/SIP: comparison to tubulin and the tau protein

  • Basic Neurosciences, Genetics and Immunology - Original Article
  • Published:
Journal of Neural Transmission Aims and scope Submit manuscript

Abstract

CacyBP/SIP was originally identified as an S100A6 (calcyclin) target and later on as a Siah-1 interacting protein. Recently, we have shown that CacyBP/SIP interacts with tubulin, which suggests its involvement in the reorganization of microtubules. In this work we examined the localization of CacyBP/SIP in cultured neurons and in brain neurons of young and aged rats, and compared this localization with that of tubulin and the tau protein. We have found that in neurons of young rats CacyBP/SIP, tubulin and tau are present in the cytoplasm and in the neuronal processes, whereas in aged animals CacyBP/SIP and tau are mainly seen in the cytoplasm of the neuronal somata. In aged rats, these changes are also accompanied by a different localization pattern of tubulin. Thus, our results show that localization of CacyBP/SIP in brain neurons is similar to that observed for tau and tubulin, which points to the involvement of CacyBP/SIP in cytoskeletal physiology.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alonso AD, Grundke-Iqbal I, Barra HS et al (1997) Abnormal phosphorylation of tau and the mechanism of Alzheimer neurofibrillary degeneration: sequestration of microtubule-associated proteins 1 and 2 and the disassembly of microtubules by the abnormal tau. Proc Natl Acad Sci USA 94:298–303

    Article  PubMed  CAS  Google Scholar 

  • Alonso AD, Zaidi T, Novak M et al (2001) Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments. Proc Natl Acad Sci USA 98:6923–6928

    Article  PubMed  CAS  Google Scholar 

  • Alonso Adel C, Li B, Grundke-Iqbal I et al (2006) Polymerization of hyperphosphorylated tau into filaments eliminates its inhibitory activity. Proc Natl Acad Sci USA 103:8864–8869

    Article  PubMed  CAS  Google Scholar 

  • Andreadis A (2005) Tau gene alternative splicing: expression pattern, regulation and modulation of unction in normal brain and neurodegenerative diseases. Biochim Biophys Acta 1739:91–103

    PubMed  CAS  Google Scholar 

  • Au KW, Kou CY, Woo AY et al (2006) Calcyclin binding protein promotes DNA synthesis and differentiation in rat neonatal cardiomyocytes. J Cell Biochem 98:555–566

    Article  PubMed  CAS  Google Scholar 

  • Avila J, Lucas JJ, Perez M et al (2004) Role of Tau in both physiological and pathological conditions. Physiol Rev 84:361–384

    Article  PubMed  CAS  Google Scholar 

  • Baas PW, Qiang L (2005) Neuronal microtubules: when the MAP is the roadblock. Trends Cell Biol 15:183–187

    Article  PubMed  CAS  Google Scholar 

  • Bendiske J, Caba E, Brown QB et al (2002) Intracellular deposition, microtubule destabilization, and transport failure: an ‘early’ pathogenic cascade leading to synaptic decline. J Neuropathol Exp Neurol 61:640–650

    PubMed  CAS  Google Scholar 

  • Brandt R, Hundelt M, Shahani N (2005) Tau alteration and neuronal degeneration in tauopathies: mechanisms and models. Bichim Biophys Acta 1739:331–354

    CAS  Google Scholar 

  • Buée L, Bussiere T, Buee-Scherrer V et al (2000) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Rev 33:95–130

    Article  PubMed  Google Scholar 

  • Charriere-Bertrand C, Nunez J (1992) Regulation of tubulin, Tau and microtubule associated protein 2 expression during mouse brain development. Neurochem Int 21:535–541

    Article  PubMed  CAS  Google Scholar 

  • Dehmelt L, Halpain S (2005) The MAP2/Tau family of microtubule-associated proteins. Genome Biol 6:204–207

    Article  PubMed  Google Scholar 

  • Desai A, Mitchison TJ (1997) Microtubule polymerisation dynamics. Ann Rev Cell Dev Biol 13:83–117

    Article  CAS  Google Scholar 

  • Drechsel DN, Hyman AA, Cobb MH et al (1992) Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol Biol Cell 3:1141–1154

    PubMed  CAS  Google Scholar 

  • Elder GA, Friedrich VL, Margita A et al (1999) Age-related atrophy of motor axons in mice deficient in the mid-sized neurofilament subunit. J Cell Biol 146:181–192

    PubMed  CAS  Google Scholar 

  • Feinstein SC, Wilson L (2005) Inability of tau to properly regulate neuronal microtubule dynamics: a loss-of-function mechanism by which tau might mediate neuronal cell death. Biochim Biophys Acta 1739:268–279

    PubMed  CAS  Google Scholar 

  • Figiel I, Dzwonek K (2007) TNF α and TNF receptor 1 expression in the mixed neuronal-glial cultures of hippocampal dentate gyrus exposed to glutamate or trimethyltin. Brain Res 1131:17–28

    Article  PubMed  CAS  Google Scholar 

  • Filipek A, Jastrzebska B, Nowotny M et al (2002a) CacyBP/SIP, a calcyclin and Siah-1-interacting protein, binds EF-hand proteins of the S100 family. J. Biol Chem 277:28848–28852

    Article  PubMed  CAS  Google Scholar 

  • Filipek A, Jastrzebska B, Nowotny M et al (2002b) Ca2+-dependent translocation of the calcyclin-binding protein in neurons and neuroblastoma NB-2a cells. J Biol Chem 277:21103–21109

    Article  PubMed  CAS  Google Scholar 

  • Filipek A, Kuznicki J (1998) Molecular cloning and expression of a mouse brain cDNA encoding a novel protein target of calcyclin. J Neurochem 70:1793–1798

    Article  PubMed  CAS  Google Scholar 

  • Filipek A, Puzianowska M, Cieślak B et al (1993) Calcyclin-Ca2+-binding protein homologous to glial S-100 beta is present in neurones. Neuroreport 4:383–386

    Article  PubMed  CAS  Google Scholar 

  • Filipek A, Wojda U (1996) p30, a novel protein target of mouse calcyclin (S100A6). Biochem J 320:585–587

    PubMed  CAS  Google Scholar 

  • Fukushima T, Zapata JM, Singha NC et al (2006) Critical function for SIP, a ubiquitin E3 ligase component of the beta-catenin degradation pathway, for thymocyte development and G1 checkpoint. Immunity 24:29–39

    Article  PubMed  CAS  Google Scholar 

  • Gundersen GG, Cook TA (1999) Microtubules and signal transduction. Curr Opin Cell Biol 11:81–94

    Article  PubMed  CAS  Google Scholar 

  • Herington JL, Bi J, Martin JD et al (2007) Beta-catenin (CTNNB1) in the mouse uterus during decidualization and the potential role of two pathways in regulating its degradation. J Histochem Cytochem. 55:963–74

    Article  PubMed  CAS  Google Scholar 

  • Hirokawa N, Takemura R (2003) Biochemical and molecular characterization of diseases linked to motor proteins. Trends Biochem Sci 28:558–565

    Article  PubMed  CAS  Google Scholar 

  • Howard J, Hyman AA (2007) Microtubule polymerases and depolymerases. Curr Opin Cell Biol 19:31–35

    Article  PubMed  CAS  Google Scholar 

  • Iqbal K, Grundke-Iqbal I, Zaidi T et al (1986) Are Alzheimer neurofibrillary tangles insoluble polymers? Life Sci 38:1695–1700

    Article  PubMed  CAS  Google Scholar 

  • Jastrzebska B, Filipek A, Nowicka D et al (2000) Calcyclin (S100A6) binding protein (CacyBP) is highly expressed in brain neurons. J Histochem Cytochem 48:1195–1202

    PubMed  CAS  Google Scholar 

  • Kinoshita K, Noetzel TL, Arnal I et al (2006) Global and local control of microtubule destabilization promoted by a catastrophe kinesin MCAK/XKCM1. J Muscle Res Cell Motil 27:107–114

    Article  PubMed  CAS  Google Scholar 

  • Köpke E, Tung YC, Shaikh S et al (1993) Microtubule-associated protein tau. Abnormal phosphorylation of a non-paired helical filament pool in Alzheimer disease. J Biol Chem 268:24374–24384

    PubMed  Google Scholar 

  • Kosik KS, Shimura H (2005) Phosphorylated tau and the neurodegenerative foldopathies. Biochim Biophys Acta 1739:298–310

    PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Lovestone S, McLoughlin DM (2002) Protein aggregates and dementia: is there a common toxicity? J Neurol Neurosur Psych 72:152–161

    Article  CAS  Google Scholar 

  • Mandelkow E, Mandelkow EM (1998) Tau in Alzheimer’s disease. Trends Cell Biol 8:425–427

    Article  PubMed  CAS  Google Scholar 

  • Mandelkow E, von Bergen M, Biernat J et al (2007) Structural principles of tau and the paired helical filaments of Alzheimer’s disease. Brain Patholol 17:83–90

    Article  CAS  Google Scholar 

  • Matsuzawa S, Reed JC (2001) Siah-1, SIP, and Ebi collaborate in a novel pathway for beta-catenin degradation linked to p53 responses. Mol Cell 7:915–926

    Article  PubMed  CAS  Google Scholar 

  • Niewiadomska G, Baksalerska-Pazera M (2003) Age-dependent changes in axonal transport and cellular distribution of Tau1 in the rat basal forebrain neurons. NeuroRep 14:1701–1706

    Article  Google Scholar 

  • Niewiadomska G, Baksalerska-Pazera M, Lenarcik I (2005) Breakdown in retrograde axonal transport and altered cellular distribution of phospho-Tau proteins during aging. Annals New York Acad Sci 1048:287–295

    Article  CAS  Google Scholar 

  • Niewiadomska G, Baksalerska-Pazera M, Riedel G (2006a) Cytoskeletal transport in the aging brain: focus on the cholinergic system. Rev Neurosci 17:581–618

    PubMed  CAS  Google Scholar 

  • Niewiadomska G, Baksalerska-Pazera M, Lenarcik I et al (2006b) Compartmental protein expression of Tau, GSK-3β and TrkA in cholinergic neurons of aged rats. J Neural Transm 113:1733–1746

    Article  PubMed  CAS  Google Scholar 

  • Nowotny M, Spiechowicz M, Jastrzebska B et al (2003) Calcium-regulated interaction of Sgt1 with S100A6 (calcyclin) and other S100 proteins. J Biol Chem 278:26923–26928

    Article  PubMed  CAS  Google Scholar 

  • Pircher TJ, Geiger JN, Zhang D et al (2001) Integrative signaling by minimal erythropoietin receptor forms and c-Kit. J Biol Chem 276:8995–9002

    Article  PubMed  CAS  Google Scholar 

  • Schneider G, Nieznanski K, Kilanczyk E et al (2007) CacyBP/SIP interacts with tubulin in neuroblastoma NB2a cells and induces formation of globular tubulin assemblies. Biochim Biophys Acta 1773:1628–1636

    Article  PubMed  CAS  Google Scholar 

  • Schuyler SC, Pellman D (2001) Microtubule “plus-end-tracking proteins”: The end is just the beginning. Cell 105:421–424

    Article  PubMed  CAS  Google Scholar 

  • Silva R, de Farrer M (2002) Tau neurotoxicity without the lesions: a fly challenges a tangled web. Trends Neurosci 25:327–329

    Article  PubMed  Google Scholar 

  • Smith DS, Niethammer M, Ayala R et al (2000) Regulation of cytoplasmic dynein behaviour and microtubule organization by mammalian LIS1. Nat Cell Biol 2:767–775

    Article  PubMed  CAS  Google Scholar 

  • Spiechowicz M, Filipek A (2005) The expression and function of Sgt1 protein in eukaryotic cells. Acta Neurobiol Exp 65:161–165

    Google Scholar 

  • Yang W, Ang LC, Strong MJ (2005) Tau protein aggregation in the frontal and entorhinal cortices as a function of aging. Dev Brain Res 156:127–138

    Article  CAS  Google Scholar 

  • Yang YJ, Liu WM, Zhou JX et al (2006) Expression and hormonal regulation of calcyclin-binding protein (CacyBP) in the mouse uterus during early pregnancy. Life Sci 78:753–60

    Article  PubMed  CAS  Google Scholar 

  • Wang JZ, Grundke-Iqbal I, Iqbal K (1996) Restoration of biological activity of Alzheimer abnormally phosphorylated tau by dephosphorylation with protein phosphatase-2A, -2B and -1. Brain Res Mol Brain Res 38:200–208

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Tan X, Peng X et al (2003) Translocation and phosphorylation of calcyclin binding protein during retinoic acid-induced neuronal differentiation of neuroblastoma SH-SY5Y cells. J Biochem Mol Biol 36:354–358

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Drs. G. Riedel and W. Leśniak for their critical reading of the manuscript. We also thank Dr. L. Sidorik for polyclonal anti-Sgt1 antibody. This work was supported by grants from the Ministry of Science and Higher Education of Poland to A. Filipek (2 P04A 01030) and G. Niewiadomska (2 PO5A 121), and by statutory funds from the Nencki Institute of Experimental Biology. G. Schneider is a recipient of a scholarship from the President of the Polish Academy of Sciences.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anna Filipek.

Electronic supplementary material

Below is the link to the electronic supplementary material.

702_2008_62_MOESM1_ESM.ppt

Specificity of the anti-Sgt1 antibody estimated by Western blotting. Rat brain extract (40 μg) prepared as described in Material and Methods, paragraph entitled “Tissue extracts preparation, SDS-PAGE and Western blot analysis” was loaded on the 10% SDS polyacrylamide gel, proteins were then blotted into nitrocellulose and incubated with anti-Sgt1 antibody. Then the blots were allowed to react with secondary antibodies conjugated to horseradish peroxidase (Sigma) and developed with ECL chemiluminescence kit (Amersham Biosciences) followed by exposition against an X-ray film. The positions of low molecular mass standard (BioRad) are indicated by arrows. (PPT 72 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Filipek, A., Schneider, G., Mietelska, A. et al. Age-dependent changes in neuronal distribution of CacyBP/SIP: comparison to tubulin and the tau protein. J Neural Transm 115, 1257–1264 (2008). https://doi.org/10.1007/s00702-008-0062-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00702-008-0062-3

Keywords

Navigation