Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1989 May;9(5):2284–2288. doi: 10.1128/mcb.9.5.2284

Expression of protein kinase C genes during ontogenic development of the central nervous system.

N M Sposi 1, L Bottero 1, G Cossu 1, G Russo 1, U Testa 1, C Peschle 1
PMCID: PMC363031  PMID: 2473391

Abstract

We have analyzed the RNA expression of three protein kinase C (PKC) genes (alpha, beta, and gamma) in human and murine central nervous systems during embryonic-fetal, perinatal, and adult life. Analysis of human brain poly(A)+ RNA indicates that expression of PKC alpha and beta genes can be detected as early as 6 weeks postconception, undergoes a gradual increase until 9 weeks postconception, and reaches its highest level in the adult stage, and that the PKC gamma gene, although not expressed during embryonic and early fetal development, is abundantly expressed in the adult period. Similar developmental patterns were observed in human spinal cord and medulla oblongata. A detailed analysis of PKC gene expression during mammalian ontogeny was performed on poly(A)+ RNA from the brain cells of murine embryos at different stages of development and the brain cells of neonatal and adult mice. The ontogenetic patterns were similar to those observed for human brain. Furthermore, we observed that the expression of PKC gamma is induced in the peri- and postnatal phases. These results suggest that expression of PKC alpha, beta, and gamma genes possibly mediates the development of central neuronal functions, and expression of PKC gamma in particular may be involved in the development of peri- and postnatal functions.

Full text

PDF
2284

Images in this article

2285Image
on p.2285
2286Image
on p.2286
2286Image
on p.2286
2286Image
on p.2286
2286Image
on p.2286

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ashendel C. L. The phorbol ester receptor: a phospholipid-regulated protein kinase. Biochim Biophys Acta. 1985 Sep 9;822(2):219–242. doi: 10.1016/0304-4157(85)90009-7. [DOI] [PubMed] [Google Scholar]
  2. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berridge M. J., Irvine R. F. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature. 1984 Nov 22;312(5992):315–321. doi: 10.1038/312315a0. [DOI] [PubMed] [Google Scholar]
  4. Brandt S. J., Niedel J. E., Bell R. M., Young W. S., 3rd Distinct patterns of expression of different protein kinase C mRNAs in rat tissues. Cell. 1987 Apr 10;49(1):57–63. doi: 10.1016/0092-8674(87)90755-0. [DOI] [PubMed] [Google Scholar]
  5. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  6. Cleveland D. W., Lopata M. A., MacDonald R. J., Cowan N. J., Rutter W. J., Kirschner M. W. Number and evolutionary conservation of alpha- and beta-tubulin and cytoplasmic beta- and gamma-actin genes using specific cloned cDNA probes. Cell. 1980 May;20(1):95–105. doi: 10.1016/0092-8674(80)90238-x. [DOI] [PubMed] [Google Scholar]
  7. Coussens L., Parker P. J., Rhee L., Yang-Feng T. L., Chen E., Waterfield M. D., Francke U., Ullrich A. Multiple, distinct forms of bovine and human protein kinase C suggest diversity in cellular signaling pathways. Science. 1986 Aug 22;233(4766):859–866. doi: 10.1126/science.3755548. [DOI] [PubMed] [Google Scholar]
  8. Hashimoto T., Ase K., Sawamura S., Kikkawa U., Saito N., Tanaka C., Nishizuka Y. Postnatal development of a brain-specific subspecies of protein kinase C in rat. J Neurosci. 1988 May;8(5):1678–1683. doi: 10.1523/JNEUROSCI.08-05-01678.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hidaka H., Tanaka T., Onoda K., Hagiwara M., Watanabe M., Ohta H., Ito Y., Tsurudome M., Yoshida T. Cell type-specific expression of protein kinase C isozymes in the rabbit cerebellum. J Biol Chem. 1988 Apr 5;263(10):4523–4526. [PubMed] [Google Scholar]
  10. Housey G. M., O'Brian C. A., Johnson M. D., Kirschmeier P., Weinstein I. B. Isolation of cDNA clones encoding protein kinase C: evidence for a protein kinase C-related gene family. Proc Natl Acad Sci U S A. 1987 Feb;84(4):1065–1069. doi: 10.1073/pnas.84.4.1065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Huang F. L., Yoshida Y., Nakabayashi H., Huang K. P. Differential distribution of protein kinase C isozymes in the various regions of brain. J Biol Chem. 1987 Nov 15;262(32):15714–15720. [PubMed] [Google Scholar]
  12. Huang F. L., Yoshida Y., Nakabayashi H., Knopf J. L., Young W. S., 3rd, Huang K. P. Immunochemical identification of protein kinase C isozymes as products of discrete genes. Biochem Biophys Res Commun. 1987 Dec 31;149(3):946–952. doi: 10.1016/0006-291x(87)90500-6. [DOI] [PubMed] [Google Scholar]
  13. Inoue M., Kishimoto A., Takai Y., Nishizuka Y. Studies on a cyclic nucleotide-independent protein kinase and its proenzyme in mammalian tissues. II. Proenzyme and its activation by calcium-dependent protease from rat brain. J Biol Chem. 1977 Nov 10;252(21):7610–7616. [PubMed] [Google Scholar]
  14. Kikkawa U., Ogita K., Ono Y., Asaoka Y., Shearman M. S., Fujii T., Ase K., Sekiguchi K., Igarashi K., Nishizuka Y. The common structure and activities of four subspecies of rat brain protein kinase C family. FEBS Lett. 1987 Nov 2;223(2):212–216. doi: 10.1016/0014-5793(87)80291-0. [DOI] [PubMed] [Google Scholar]
  15. Knopf J. L., Lee M. H., Sultzman L. A., Kriz R. W., Loomis C. R., Hewick R. M., Bell R. M. Cloning and expression of multiple protein kinase C cDNAs. Cell. 1986 Aug 15;46(4):491–502. doi: 10.1016/0092-8674(86)90874-3. [DOI] [PubMed] [Google Scholar]
  16. Kuo J. F., Andersson R. G., Wise B. C., Mackerlova L., Salomonsson I., Brackett N. L., Katoh N., Shoji M., Wrenn R. W. Calcium-dependent protein kinase: widespread occurrence in various tissues and phyla of the animal kingdom and comparison of effects of phospholipid, calmodulin, and trifluoperazine. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7039–7043. doi: 10.1073/pnas.77.12.7039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Makowske M., Birnbaum M. J., Ballester R., Rosen O. M. A cDNA encoding protein kinase C identifies two species of mRNA in brain and GH3 cells. J Biol Chem. 1986 Oct 15;261(29):13389–13392. [PubMed] [Google Scholar]
  18. Minakuchi R., Takai Y., Yu B., Nishizuka Y. Widespread occurrence of calcium-activated, phospholipid-dependent protein kinase in mammalian tissues. J Biochem. 1981 May;89(5):1651–1654. doi: 10.1093/oxfordjournals.jbchem.a133362. [DOI] [PubMed] [Google Scholar]
  19. Nairn A. C., Hemmings H. C., Jr, Greengard P. Protein kinases in the brain. Annu Rev Biochem. 1985;54:931–976. doi: 10.1146/annurev.bi.54.070185.004435. [DOI] [PubMed] [Google Scholar]
  20. Nishizuka Y. Studies and perspectives of protein kinase C. Science. 1986 Jul 18;233(4761):305–312. doi: 10.1126/science.3014651. [DOI] [PubMed] [Google Scholar]
  21. Nishizuka Y. The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature. 1988 Aug 25;334(6184):661–665. doi: 10.1038/334661a0. [DOI] [PubMed] [Google Scholar]
  22. Nishizuka Y. The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature. 1984 Apr 19;308(5961):693–698. doi: 10.1038/308693a0. [DOI] [PubMed] [Google Scholar]
  23. Nishizuka Y. Turnover of inositol phospholipids and signal transduction. Science. 1984 Sep 21;225(4668):1365–1370. doi: 10.1126/science.6147898. [DOI] [PubMed] [Google Scholar]
  24. Ohno S., Kawasaki H., Imajoh S., Suzuki K., Inagaki M., Yokokura H., Sakoh T., Hidaka H. Tissue-specific expression of three distinct types of rabbit protein kinase C. Nature. 1987 Jan 8;325(7000):161–166. doi: 10.1038/325161a0. [DOI] [PubMed] [Google Scholar]
  25. Ohno S., Kawasaki H., Konno Y., Inagaki M., Hidaka H., Suzuki K. A fourth type of rabbit protein kinase C. Biochemistry. 1988 Mar 22;27(6):2083–2087. doi: 10.1021/bi00406a040. [DOI] [PubMed] [Google Scholar]
  26. Ono Y., Fujii T., Igarashi K., Kikkawa U., Ogita K., Nishizuka Y. Nucleotide sequences of cDNAs for alpha and gamma subspecies of rat brain protein kinase C. Nucleic Acids Res. 1988 Jun 10;16(11):5199–5200. doi: 10.1093/nar/16.11.5199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ono Y., Fujii T., Ogita K., Kikkawa U., Igarashi K., Nishizuka Y. Identification of three additional members of rat protein kinase C family: delta-, epsilon- and zeta-subspecies. FEBS Lett. 1987 Dec 21;226(1):125–128. doi: 10.1016/0014-5793(87)80564-1. [DOI] [PubMed] [Google Scholar]
  28. Ono Y., Kikkawa U., Ogita K., Fujii T., Kurokawa T., Asaoka Y., Sekiguchi K., Ase K., Igarashi K., Nishizuka Y. Expression and properties of two types of protein kinase C: alternative splicing from a single gene. Science. 1987 May 29;236(4805):1116–1120. doi: 10.1126/science.3576226. [DOI] [PubMed] [Google Scholar]
  29. Ono Y., Kurokawa T., Fujii T., Kawahara K., Igarashi K., Kikkawa U., Ogita K., Nishizuka Y. Two types of complementary DNAs of rat brain protein kinase C. Heterogeneity determined by alternative splicing. FEBS Lett. 1986 Oct 6;206(2):347–352. doi: 10.1016/0014-5793(86)81010-9. [DOI] [PubMed] [Google Scholar]
  30. Parker P. J., Coussens L., Totty N., Rhee L., Young S., Chen E., Stabel S., Waterfield M. D., Ullrich A. The complete primary structure of protein kinase C--the major phorbol ester receptor. Science. 1986 Aug 22;233(4766):853–859. doi: 10.1126/science.3755547. [DOI] [PubMed] [Google Scholar]
  31. Peschle C., Mavilio F., Carè A., Migliaccio G., Migliaccio A. R., Salvo G., Samoggia P., Petti S., Guerriero R., Marinucci M. Haemoglobin switching in human embryos: asynchrony of zeta----alpha and epsilon----gamma-globin switches in primitive and definite erythropoietic lineage. Nature. 1985 Jan 17;313(5999):235–238. doi: 10.1038/313235a0. [DOI] [PubMed] [Google Scholar]
  32. Saito N., Kikkawa U., Nishizuka Y., Tanaka C. Distribution of protein kinase C-like immunoreactive neurons in rat brain. J Neurosci. 1988 Feb;8(2):369–382. doi: 10.1523/JNEUROSCI.08-02-00369.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Turner R. S., Raynor R. L., Mazzei G. J., Girard P. R., Kuo J. F. Developmental studies of phospholipid-sensitive Ca2+-dependent protein kinase and its substrates and of phosphoprotein phosphatases in rat brain. Proc Natl Acad Sci U S A. 1984 May;81(10):3143–3147. doi: 10.1073/pnas.81.10.3143. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES