Home LiteratureArticle Details
PMID: 8467810 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Depletion of casein kinase II by antisense oligonucleotide prevents neuritogenesis in neuroblastoma cells.

The EMBO journal ·Vol. 12 ·No. 4 ·1993-04-00 ·Pages 1633-40

Ulloa L, Díaz-Nido J, Avila J

Abstract

Casein kinase II is a multifunctional protein kinase which has been implicated in the regulation of cell growth and differentiation. This enzyme is much more abundant in neurons than in any other cell type. The treatment of neuroblastoma cells with an antisense oligodeoxyribonucleotide which specifically results in the depletion of casein kinase II catalytic subunits blocks neuritogenesis. Accordingly, this enzyme may perform an essential role during neurite growth in developing neurons. Casein kinase II depletion induced by antisense oligodeoxyribonucleotide is accompanied by a site-specific dephosphorylation of microtubule-associated protein MAP1B (also referred to as MAP5, MAP1.X or MAP1.2), which is paralleled by a release of MAP1B from microtubules. We therefore propose that phosphorylation by casein kinase II may be required for the proper MAP1B functioning in the promotion of the assembly of microtubules which constitute the cytoskeletal scaffolding of growing axon-like neurites.

Related Genes
MeSH Terms
Animals Base Sequence Casein Kinase II Cell Differentiation Fluorescent Antibody Technique In Vitro Techniques Mice Microtubule-Associated Proteins/metabolism Microtubules/metabolism Molecular Sequence Data Neurons/cytology Oligodeoxyribonucleotides/chemistry Oligonucleotides, Antisense Phosphorylation Protein Serine-Threonine Kinases/physiology Time Factors Tumor Cells, Cultured
Chemicals
Microtubule-Associated Proteins Oligodeoxyribonucleotides Oligonucleotides, Antisense microtubule-associated protein 1B Casein Kinase II Protein Serine-Threonine Kinases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Ulloa L
Centro de Biología Molecular (CSIC-UAM), Facultad de Ciencias, Universidad Autónoma, Madrid, Spain.
Díaz-Nido J
Avila J
References (85)
85 references, click to expand
  1. Phosphorylation of microtubule proteins in rat brain at different developmental stages: comparison with that found in neuronal cultures.
    J Neurochem. 1990 Jan;54(1):211-22 PMID: 2293611
  2. Difference in distribution of microtubule-associated proteins 5a and 5b during the development of cerebral cortex and corpus callosum in cats: dependence on phosphorylation.
    Brain Res Dev Brain Res. 1990 Nov 1;56(2):235-43 PMID: 2261685
  3. Casein kinase II. cDNA sequences, developmental expression, and tissue distribution of mRNAs for alpha, alpha', and beta subunits of the chicken enzyme.
    J Biol Chem. 1991 Feb 5;266(4):2362-8 PMID: 1989988
  4. MAP5: a novel brain microtubule-associated protein under strong developmental regulation.
    J Neurocytol. 1986 Dec;15(6):763-75 PMID: 3819779
  5. Isolation and sequencing of cDNA clones encoding alpha and beta subunits of Drosophila melanogaster casein kinase II.
    Mol Cell Biol. 1987 Oct;7(10):3409-17 PMID: 3119988
  6. Axon growth: roles of microfilaments and microtubules.
    Proc Natl Acad Sci U S A. 1970 Aug;66(4):1206-12 PMID: 5273449
  7. Casein kinase 2: an 'eminence grise' in cellular regulation?
    Biochim Biophys Acta. 1990 Sep 24;1054(3):267-84 PMID: 2207178
  8. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  9. The decreased level of casein kinase 2 in brain cortex of schizophrenic and Alzheimer's disease patients.
    FEBS Lett. 1991 Feb 11;279(1):55-7 PMID: 1995343
  10. Association of casein kinase II with microtubules.
    Exp Cell Res. 1989 Mar;181(1):263-72 PMID: 2645149
  11. Phosphorylation determines the binding of microtubule-associated protein 2 (MAP2) to microtubules in living cells.
    J Cell Biol. 1991 Aug;114(4):735-43 PMID: 1907976
  12. Regulation of casein kinase II activity by epidermal growth factor in human A-431 carcinoma cells.
    J Biol Chem. 1989 Jul 15;264(20):11958-65 PMID: 2473067
  13. Solubility properties of neuronal tubulin: evidence for labile and stable microtubules.
    Brain Res. 1984 Mar 19;295(2):255-63 PMID: 6713187
  14. Casein kinase I and II--multipotential serine protein kinases: structure, function, and regulation.
    Adv Second Messenger Phosphoprotein Res. 1991;23:123-64 PMID: 1997039
  15. Neuronal microtubule-associated proteins in the embryonic avian spinal cord.
    J Comp Neurol. 1988 May 1;271(1):44-55 PMID: 3385011
  16. Cytoplasmic and nuclear distribution of casein kinase II: characterization of the enzyme uptake by bovine adrenocortical nuclear preparation.
    Biochemistry. 1990 Oct 23;29(42):9928-36 PMID: 2271631
  17. Aberrant casein kinase II in Alzheimer's disease.
    Brain Res. 1990 Jan 22;507(2):273-80 PMID: 2337767
  18. The effect of tau antisense oligonucleotides on neurite formation of cultured cerebellar macroneurons.
    J Neurosci. 1991 Jun;11(6):1515-23 PMID: 1904479
  19. Inhibition of Rous sarcoma virus replication and cell transformation by a specific oligodeoxynucleotide.
    Proc Natl Acad Sci U S A. 1978 Jan;75(1):280-4 PMID: 75545
  20. Casein kinase II is a negative regulator of c-Jun DNA binding and AP-1 activity.
    Cell. 1992 Sep 4;70(5):777-89 PMID: 1516134
  21. Casein kinase II alteration precedes tau accumulation in tangle formation.
    Am J Pathol. 1992 Feb;140(2):263-8 PMID: 1739121
  22. Microtubule protein phosphorylation in neuroblastoma cells and neurite growth.
    J Cell Sci Suppl. 1991;15:51-9 PMID: 1824107
  23. Isolation and characterization of recombinant human casein kinase II subunits alpha and beta from bacteria.
    Eur J Biochem. 1991 May 23;198(1):25-30 PMID: 2040287
  24. Protein synthesis is required for the initiation of dendritic growth in embryonic rat sympathetic neurons in vitro.
    Brain Res Dev Brain Res. 1991 Jun 21;60(2):187-96 PMID: 1716531
  25. Isolation and characterization of human cDNA clones encoding the alpha and the alpha' subunits of casein kinase II.
    Biochemistry. 1990 Sep 11;29(36):8436-47 PMID: 2174700
  26. Tubulin phosphorylation by casein kinase II is similar to that found in vivo.
    J Cell Biol. 1987 Oct;105(4):1731-9 PMID: 3478337
  27. Tubulin pools in differentiating neuroblastoma cells.
    J Cell Biol. 1981 Jun;89(3):418-23 PMID: 7251659
  28. Myc oncoproteins are phosphorylated by casein kinase II.
    EMBO J. 1989 Apr;8(4):1111-9 PMID: 2663470
  29. Ultrastructure and function of growth cones and axons of cultured nerve cells.
    J Cell Biol. 1971 Jun;49(3):614-35 PMID: 4326456
  30. Stimulation of casein kinase II by epidermal growth factor: relationship between the physiological activity of the kinase and the phosphorylation state of its beta subunit.
    Proc Natl Acad Sci U S A. 1990 Jan;87(2):821-5 PMID: 2300566
  31. In situ localization of microtubule-associated protein mRNA in the developing and adult rat brain.
    Neuron. 1989 Mar;2(3):1245-56 PMID: 2624748
  32. Characterization of proteins immunologically related to brain microtubule-associated protein MAP-1B in non-neural cells.
    J Cell Sci. 1989 Apr;92 ( Pt 4):607-20 PMID: 2689462
  33. Measurement of protein using bicinchoninic acid.
    Anal Biochem. 1985 Oct;150(1):76-85 PMID: 3843705
  34. Microtubule-associated proteins and neuronal morphogenesis.
    J Cell Sci Suppl. 1991;15:61-7 PMID: 1824108
  35. Activation of casein kinase II in response to insulin and to epidermal growth factor.
    Proc Natl Acad Sci U S A. 1987 Dec;84(24):8834-8 PMID: 3321056
  36. Differentiation of neuroblastoma cells correlates with an altered splicing pattern of tau RNA.
    FEBS Lett. 1992 Mar 24;299(1):10-4 PMID: 1544466
  37. A polymer-dependent increase in phosphorylation of beta-tubulin accompanies differentiation of a mouse neuroblastoma cell line.
    J Cell Biol. 1985 Mar;100(3):764-74 PMID: 2857724
  38. Control of isotubulin expression during neuronal differentiation of mouse neuroblastoma and teratocarcinoma cell lines.
    Dev Biol. 1987 Oct;123(2):549-58 PMID: 3653524
  39. The rate of nuclear cytoplasmic protein transport is determined by the casein kinase II site flanking the nuclear localization sequence of the SV40 T-antigen.
    EMBO J. 1991 Mar;10(3):633-9 PMID: 1848177
  40. M-phase-specific cdc2 protein kinase phosphorylates the beta subunit of casein kinase II and increases casein kinase II activity.
    Eur J Biochem. 1990 Oct 24;193(2):529-34 PMID: 2226469
  41. Human phosvitin/casein kinase type II. Molecular cloning and sequencing of full-length cDNA encoding subunit beta.
    Eur J Biochem. 1989 Jul 15;183(1):227-33 PMID: 2666134
  42. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  43. Microtubule-associated proteins (MAPs): a monoclonal antibody to MAP 1 decorates microtubules in vitro but stains stress fibers and not microtubules in vivo.
    Proc Natl Acad Sci U S A. 1985 Mar;82(5):1434-8 PMID: 3883359
  44. Cell growth stimulation by EGF: inhibition through antisense-oligodeoxynucleotides demonstrates important role of casein kinase II.
    Exp Cell Res. 1991 Dec;197(2):245-53 PMID: 1959559
  45. Casein kinase type II is involved in the inhibition by 5,6-dichloro-1-beta-D-ribofuranosylbenzimidazole of specific RNA polymerase II transcription.
    J Biol Chem. 1986 Mar 5;261(7):3414-9 PMID: 3456346
  46. The adult rat olfactory system expresses microtubule-associated proteins found in the developing brain.
    J Neurosci. 1989 Oct;9(10):3547-57 PMID: 2507752
  47. Cellular uptake and intracellular fate of antisense oligonucleotides.
    Trends Cell Biol. 1992 May;2(5):139-44 PMID: 14731968
  48. Protein serine/threonine kinases.
    Annu Rev Biochem. 1987;56:567-613 PMID: 2956925
  49. Microtubule-associated proteins characteristic of embryonic brain are found in the adult mammalian retina.
    Dev Biol. 1988 Dec;130(2):423-34 PMID: 3058539
  50. Molecular cloning of the human casein kinase II alpha subunit.
    Biochemistry. 1989 May 2;28(9):4072-6 PMID: 2752008
  51. Regulating cell growth: casein-kinase-II-dependent phosphorylation of nuclear oncoproteins.
    Cold Spring Harb Symp Quant Biol. 1988;53 Pt 1:91-5 PMID: 3076091
  52. Increase in cytoplasmic casein kinase II-type activity accompanies neurite outgrowth after DNA synthesis inhibition in NIA-103 neuroblastoma cells.
    J Neurochem. 1992 May;58(5):1820-8 PMID: 1560236
  53. Characterization in mammalian brain of a DARPP-32 serine kinase identical to casein kinase II.
    J Neurochem. 1990 Nov;55(5):1772-83 PMID: 2145398
  54. Purification and properties of calf thymus casein kinases I and II.
    J Biol Chem. 1981 Apr 10;256(7):3319-25 PMID: 6937462
  55. Casein kinase II is a predominantly nuclear enzyme.
    J Cell Biol. 1992 Jan;116(1):43-55 PMID: 1730748
  56. Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ.
    Proc Natl Acad Sci U S A. 1983 Oct;80(19):6126-30 PMID: 6577472
  57. Massive somatodendritic sprouting of cortical neurons in Alzheimer's disease.
    Brain Res. 1988 Aug 30;459(1):138-44 PMID: 3139259
  58. The inhibition of neurite outgrowth in PC12 cells by tubulin antisense oligodeoxyribonucleotides.
    Gene. 1988 Dec 10;72(1-2):297-307 PMID: 2468570
  59. Serum-stimulated cell growth causes oscillations in casein kinase II activity.
    J Biol Chem. 1989 May 5;264(13):7345-8 PMID: 2708368
  60. Nerve growth factor regulates both the phosphorylation and steady-state levels of microtubule-associated protein 1.2 (MAP1.2).
    J Cell Biol. 1988 May;106(5):1573-81 PMID: 3372590
  61. Antisense oligonucleotides as antiviral agents.
    Trends Biotechnol. 1992 May;10(5):152-8 PMID: 1368317
  62. A casein kinase II-related activity is involved in phosphorylation of microtubule-associated protein MAP-1B during neuroblastoma cell differentiation.
    J Cell Biol. 1988 Jun;106(6):2057-65 PMID: 3164313
  63. Casein kinase II is associated with neurofibrillary tangles but is not an intrinsic component of paired helical filaments.
    Brain Res. 1992 Feb 21;573(1):126-32 PMID: 1576530
  64. Identification of the major multiphosphorylation site in mammalian neurofilaments.
    Proc Natl Acad Sci U S A. 1988 Mar;85(6):1998-2002 PMID: 2450354
  65. 5,6-Dichloro-1-beta-D-ribofuranosylbenzimidazole inhibits a HeLa protein kinase that phosphorylates an RNA polymerase II-derived peptide.
    Biochem Biophys Res Commun. 1989 Mar 15;159(2):508-15 PMID: 2930526
  66. Changes in microtubule-associated protein MAP1B phosphorylation during rat brain development.
    J Neurochem. 1990 Jul;55(1):328-33 PMID: 1693946
  67. Differentiation of neuroblastoma cells in culture.
    Biol Rev Camb Philos Soc. 1975 May;50(2):129-65 PMID: 240451
  68. Immunocytochemical localization of casein kinase II during interphase and mitosis.
    J Cell Biol. 1991 Sep;114(6):1217-32 PMID: 1894695
  69. Attenuation of microtubule-associated protein 1B expression by antisense oligodeoxynucleotides inhibits initiation of neurite outgrowth.
    Neuroscience. 1993 Feb;52(3):489-96 PMID: 8450955
  70. Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons.
    Nature. 1990 Feb 1;343(6257):461-3 PMID: 2105469
  71. Regulation of axon formation by clonal lines of a neural tumor.
    Proc Natl Acad Sci U S A. 1970 May;66(1):160-7 PMID: 5273894
  72. Characterization of the catalytic subunit of casein kinase II expressed in Escherichia coli and regulation of activity.
    J Biol Chem. 1991 Mar 25;266(9):5664-9 PMID: 1900838
  73. Neurite outgrowth in peripherin-depleted PC12 cells.
    J Cell Biol. 1992 Jun;117(5):1085-92 PMID: 1577867
  74. Phosphorylation of transcriptional factors and cell-cycle-dependent proteins by casein kinase II.
    Curr Opin Cell Biol. 1991 Jun;3(3):474-83 PMID: 1654061
  75. Insulin-like growth factor I and insulin rapidly increase casein kinase II activity in BALB/c 3T3 fibroblasts.
    J Biol Chem. 1988 Nov 5;263(31):15872-5 PMID: 3053682
  76. PC12 cells express juvenile microtubule-associated proteins during nerve growth factor-induced neurite outgrowth.
    J Cell Biol. 1988 Aug;107(2):643-50 PMID: 3417766
  77. The beta subunit of casein kinase II: cloning of cDNAs from murine and porcine origin and expression of the porcine sequence as a fusion protein.
    Biochim Biophys Acta. 1991 Mar 26;1088(3):439-41 PMID: 2015307
  78. Phosphorylation of a neuronal-specific beta-tubulin isotype.
    J Biol Chem. 1990 Aug 15;265(23):13949-54 PMID: 2199448
  79. An improved purification procedure and properties of casein kinase II from brain.
    Neurochem Res. 1988 Sep;13(9):829-36 PMID: 3226465
  80. Phosphorylation of the beta subunit of casein kinase II in human A431 cells. Identification of the autophosphorylation site and a site phosphorylated by p34cdc2.
    J Biol Chem. 1991 Oct 25;266(30):20380-9 PMID: 1939094
  81. A simple fixation procedure for immunofluorescent detection of different cytoskeletal components within the same cell.
    Histochemistry. 1989;91(1):81-8 PMID: 2925451
  82. Casein kinase II as a potentially important enzyme concerned with signal transduction.
    Cold Spring Harb Symp Quant Biol. 1988;53 Pt 1:77-84 PMID: 3076090
  83. Protein kinases associated with isolated mitotic spindles from mammalian cells: identification of a casein kinase II-like enzyme.
    Second Messengers Phosphoproteins. 1992;14(1-2):39-53 PMID: 1403849
  84. Appearance and localization of phosphorylated variants of the high molecular weight neurofilament protein in NB2a/d1 cytoskeletons during differentiation.
    Brain Res Dev Brain Res. 1989 Nov 1;50(1):142-6 PMID: 2510955
  85. The p53 tumour suppressor protein is phosphorylated at serine 389 by casein kinase II.
    EMBO J. 1990 Oct;9(10):3253-60 PMID: 2145148
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1993-04-00
Pages
1633-40
Language
English
Region
England
NLM ID
8208664
PMCID
PMC413377
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]