Journal of Neural Transmission

, Volume 115, Issue 9, pp 1257–1264

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

  • Anna Filipek
  • Gabriela Schneider
  • Anna Mietelska
  • Izabela Figiel
  • Grazyna Niewiadomska
Basic Neurosciences, Genetics and Immunology - Original Article

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.

Keywords

CacyBP/SIP Tubulin Tau Aging Neuronal cytoskeleton 

Supplementary material

702_2008_62_MOESM1_ESM.ppt (72 kb)
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)

References

  1. 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 94:298–303PubMedCrossRefGoogle Scholar
  2. 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 98:6923–6928PubMedCrossRefGoogle Scholar
  3. 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 103:8864–8869PubMedCrossRefGoogle Scholar
  4. Andreadis A (2005) Tau gene alternative splicing: expression pattern, regulation and modulation of unction in normal brain and neurodegenerative diseases. Biochim Biophys Acta 1739:91–103PubMedGoogle Scholar
  5. Au KW, Kou CY, Woo AY et al (2006) Calcyclin binding protein promotes DNA synthesis and differentiation in rat neonatal cardiomyocytes. J Cell Biochem 98:555–566PubMedCrossRefGoogle Scholar
  6. Avila J, Lucas JJ, Perez M et al (2004) Role of Tau in both physiological and pathological conditions. Physiol Rev 84:361–384PubMedCrossRefGoogle Scholar
  7. Baas PW, Qiang L (2005) Neuronal microtubules: when the MAP is the roadblock. Trends Cell Biol 15:183–187PubMedCrossRefGoogle Scholar
  8. 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 61:640–650PubMedGoogle Scholar
  9. Brandt R, Hundelt M, Shahani N (2005) Tau alteration and neuronal degeneration in tauopathies: mechanisms and models. Bichim Biophys Acta 1739:331–354Google Scholar
  10. Buée L, Bussiere T, Buee-Scherrer V et al (2000) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Rev 33:95–130PubMedCrossRefGoogle Scholar
  11. Charriere-Bertrand C, Nunez J (1992) Regulation of tubulin, Tau and microtubule associated protein 2 expression during mouse brain development. Neurochem Int 21:535–541PubMedCrossRefGoogle Scholar
  12. Dehmelt L, Halpain S (2005) The MAP2/Tau family of microtubule-associated proteins. Genome Biol 6:204–207PubMedCrossRefGoogle Scholar
  13. Desai A, Mitchison TJ (1997) Microtubule polymerisation dynamics. Ann Rev Cell Dev Biol 13:83–117CrossRefGoogle Scholar
  14. 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 3:1141–1154PubMedGoogle Scholar
  15. 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 146:181–192PubMedGoogle Scholar
  16. 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 1739:268–279PubMedGoogle Scholar
  17. 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 1131:17–28PubMedCrossRefGoogle Scholar
  18. 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 277:28848–28852PubMedCrossRefGoogle Scholar
  19. 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 277:21103–21109PubMedCrossRefGoogle Scholar
  20. Filipek A, Kuznicki J (1998) Molecular cloning and expression of a mouse brain cDNA encoding a novel protein target of calcyclin. J Neurochem 70:1793–1798PubMedCrossRefGoogle Scholar
  21. Filipek A, Puzianowska M, Cieślak B et al (1993) Calcyclin-Ca2+-binding protein homologous to glial S-100 beta is present in neurones. Neuroreport 4:383–386PubMedCrossRefGoogle Scholar
  22. Filipek A, Wojda U (1996) p30, a novel protein target of mouse calcyclin (S100A6). Biochem J 320:585–587PubMedGoogle Scholar
  23. 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 24:29–39PubMedCrossRefGoogle Scholar
  24. Gundersen GG, Cook TA (1999) Microtubules and signal transduction. Curr Opin Cell Biol 11:81–94PubMedCrossRefGoogle Scholar
  25. 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. 55:963–74PubMedCrossRefGoogle Scholar
  26. Hirokawa N, Takemura R (2003) Biochemical and molecular characterization of diseases linked to motor proteins. Trends Biochem Sci 28:558–565PubMedCrossRefGoogle Scholar
  27. Howard J, Hyman AA (2007) Microtubule polymerases and depolymerases. Curr Opin Cell Biol 19:31–35PubMedCrossRefGoogle Scholar
  28. Iqbal K, Grundke-Iqbal I, Zaidi T et al (1986) Are Alzheimer neurofibrillary tangles insoluble polymers? Life Sci 38:1695–1700PubMedCrossRefGoogle Scholar
  29. Jastrzebska B, Filipek A, Nowicka D et al (2000) Calcyclin (S100A6) binding protein (CacyBP) is highly expressed in brain neurons. J Histochem Cytochem 48:1195–1202PubMedGoogle Scholar
  30. 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 27:107–114PubMedCrossRefGoogle Scholar
  31. 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 268:24374–24384PubMedGoogle Scholar
  32. Kosik KS, Shimura H (2005) Phosphorylated tau and the neurodegenerative foldopathies. Biochim Biophys Acta 1739:298–310PubMedGoogle Scholar
  33. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685PubMedCrossRefGoogle Scholar
  34. Lovestone S, McLoughlin DM (2002) Protein aggregates and dementia: is there a common toxicity? J Neurol Neurosur Psych 72:152–161CrossRefGoogle Scholar
  35. Mandelkow E, Mandelkow EM (1998) Tau in Alzheimer’s disease. Trends Cell Biol 8:425–427PubMedCrossRefGoogle Scholar
  36. 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 17:83–90CrossRefGoogle Scholar
  37. 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 7:915–926PubMedCrossRefGoogle Scholar
  38. Niewiadomska G, Baksalerska-Pazera M (2003) Age-dependent changes in axonal transport and cellular distribution of Tau1 in the rat basal forebrain neurons. NeuroRep 14:1701–1706CrossRefGoogle Scholar
  39. 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 1048:287–295CrossRefGoogle Scholar
  40. Niewiadomska G, Baksalerska-Pazera M, Riedel G (2006a) Cytoskeletal transport in the aging brain: focus on the cholinergic system. Rev Neurosci 17:581–618PubMedGoogle Scholar
  41. 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 113:1733–1746PubMedCrossRefGoogle Scholar
  42. Nowotny M, Spiechowicz M, Jastrzebska B et al (2003) Calcium-regulated interaction of Sgt1 with S100A6 (calcyclin) and other S100 proteins. J Biol Chem 278:26923–26928PubMedCrossRefGoogle Scholar
  43. Pircher TJ, Geiger JN, Zhang D et al (2001) Integrative signaling by minimal erythropoietin receptor forms and c-Kit. J Biol Chem 276:8995–9002PubMedCrossRefGoogle Scholar
  44. 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 1773:1628–1636PubMedCrossRefGoogle Scholar
  45. Schuyler SC, Pellman D (2001) Microtubule “plus-end-tracking proteins”: The end is just the beginning. Cell 105:421–424PubMedCrossRefGoogle Scholar
  46. Silva R, de Farrer M (2002) Tau neurotoxicity without the lesions: a fly challenges a tangled web. Trends Neurosci 25:327–329PubMedCrossRefGoogle Scholar
  47. Smith DS, Niethammer M, Ayala R et al (2000) Regulation of cytoplasmic dynein behaviour and microtubule organization by mammalian LIS1. Nat Cell Biol 2:767–775PubMedCrossRefGoogle Scholar
  48. Spiechowicz M, Filipek A (2005) The expression and function of Sgt1 protein in eukaryotic cells. Acta Neurobiol Exp 65:161–165Google Scholar
  49. Yang W, Ang LC, Strong MJ (2005) Tau protein aggregation in the frontal and entorhinal cortices as a function of aging. Dev Brain Res 156:127–138CrossRefGoogle Scholar
  50. 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 78:753–60PubMedCrossRefGoogle Scholar
  51. 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 38:200–208PubMedCrossRefGoogle Scholar
  52. 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 36:354–358PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Anna Filipek
    • 1
  • Gabriela Schneider
    • 1
  • Anna Mietelska
    • 1
  • Izabela Figiel
    • 1
  • Grazyna Niewiadomska
    • 1
  1. 1.Nencki Institute of Experimental BiologyWarsawPoland

Personalised recommendations