S-100-Related Proteins in Nerve Growth Factor-Induced Differentiation of PC12 Cells

  • Piotr Masiakowski
  • Eric M. Shooter

Abstract

In the development of the nervous system, more neurons are generated than are eventually found in the adult organism. The mechanisms which determine the selective neuronal survival, the acquisition and maintenance of the differentiated phenotype, and the potential for regeneration are presently under intensive study. The pioneering work on nerve growth factor (NGF) and, more recently, also other polypeptide factors, has established the key role of target-derived neurotrophic substances in these processes (for recent review, see Snider and Johnson 1989). Much effort is now focused on understanding the molecular mechanisms triggered by the interaction of neurotrophic factors with their neuronal receptors.

Keywords

Arthritis Tyrosine Leukemia Agarose Cysteine 

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References

  1. Ali SM, Geisow MJ, Burgoyne RD (1989) A role for calpactin in calcium-dependent exocytosis in adrenal chromaffin cells. Nature 340:313–315.PubMedCrossRefGoogle Scholar
  2. Barraclough R, Savin J, Dube SK, Rudland PS (1987) Molecular cloning and sequence of the gene for p9Ka, a cultured myoepithelial cell protein with strong homology to S-100, a calcium-binding protein. J Mol Biol 198:13–20.PubMedCrossRefGoogle Scholar
  3. Bar-Sagi D, Feramisco JR (1985) Microinjection of the ras oncogene protein into PC12 cells induces morphological differentiation. Cell 42:841–848.PubMedCrossRefGoogle Scholar
  4. Baudier J, Cole RD (1988) Interactions between the microtubuie-associated τ proteins and S 100b regulate τ phosphorylation by the Ca2+/calmodulin-dependent protein kinase II. J Biol Chem 263:5876–5883.PubMedGoogle Scholar
  5. Donato R (1986) S-100 proteins. Cell Calcium 7:123–145.PubMedCrossRefGoogle Scholar
  6. Ebralidze A, Tulchinsky E, Grigorian M, Afanasyeva A, Senin V, Revazova E, Lukanidin E (1989) Isolation and characterization of a gene specifically expressed in different metastatic cells and whose deduced gene product has a high degree of homology to a Ca2+-binding protein family. Genes Dev 3:1086–1093.PubMedCrossRefGoogle Scholar
  7. Edgeworth J, Freemont P, Hogg N (1989) Ionomycin-regulated phosphorylation of the myeloid calcium-binding protein pl4. Nature 342:189–192.PubMedCrossRefGoogle Scholar
  8. Feigner PL, Gadek TR, Holm M, Roman R, Chan HW, Wenz M, Northrop JP, Ringold GM, Danielsen M (1987) Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure. Proc Natl Acad Sci USA 84:7413–7417.CrossRefGoogle Scholar
  9. Fullmer CS, Wasserman RH (1981) The amino acid sequence of bovine intestinal calcium-binding protein. J Biol Chem 256:5669–5674.PubMedGoogle Scholar
  10. Gerke V, Weber K (1984) Identity of p36K phosphorylated upon Rous sarcoma virus transformation with a protein purified from brush borders: calcium-dependent binding to non-erythroid spectrin and F-actin. EMBO J 3:227–233.PubMedGoogle Scholar
  11. Gerke V, Weber K (1985a) Calcium-dependent conformational changes in the 36-kDa subunit of intestinal protein I related to the cellular 36-kDa target of Rous sarcoma virus tyrosine kinase. J Biol Chem 260:1688–1695.PubMedGoogle Scholar
  12. Gerke V, Weber K (1985b) The regulatory chain in the p36-kd substrate complex of viral tyrosine-specific protein kinases is related in sequence to the S-100 protein of glial cells. EMBO J 4:2917–2920.PubMedGoogle Scholar
  13. Glenney JR (1985) Phosphorylation of p36 in vitro with pp60810: regulation by Ca2+ and phospholipid. FEBS Lett 192:79–82.PubMedCrossRefGoogle Scholar
  14. Glenney J (1986) Phospholipid-dependent Ca2+ binding by the 36-kDa tyrosine kinase substrate (calpactin) and its 33-kDa core. J Biol Chem 261:7247–7252.PubMedGoogle Scholar
  15. Glenney JR, Tack BF (1985) Amino-terminal sequence of p36 and associated p10: identification of the site of tyrosine phosphorylation and homology with S-100. Proc Natl Acad Sci USA 82:7884–7888.PubMedCrossRefGoogle Scholar
  16. Glenney JR, Boudreau M, Galyean R, Hunter T, Tack B (1986) Association of the S-100-related calpactin I light chain with the NH2-terminal tail of the 36-kDa heavy chain. J Biol Chem 261:10485–10488.PubMedGoogle Scholar
  17. Glenney JR, Kindy MS, Zokas L (1989) Isolation of a new member of the S100 protein family: amino acid sequence, tissue, and subcellular distribution. J Cell Biol 108:569–578.PubMedCrossRefGoogle Scholar
  18. Goto K, Endo H, Fujiyoshi T (1988) Cloning of the sequences expressed abundantly in established cell lines: Identification of a cDNA clone highly homologous to S-100, a calcium binding protein. J Biochem 103:48–53.PubMedGoogle Scholar
  19. Greenberg ME, Greene LA, Ziff EB (1985) Nerve growth factor and epidermal growth factor induce rapid transient changes in proto-oncogene transcription in PC12 cells. J Biol Chem 260:14101–14110.PubMedGoogle Scholar
  20. Greenberg ME, Ziff EB, Greene LA (1986) Stimulation of neuronal acetylcholine receptors induces rapid gene transcription. Science 234:80–83.PubMedCrossRefGoogle Scholar
  21. Greene LA, Tischler AS (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci USA 73:2424–2428.PubMedCrossRefGoogle Scholar
  22. Gunning P, Leavitt J, Muscat G, Ng S-Y, Kedes L (1987) A human b-actin expression vector system directs high-level accumulation of antisense transcripts. Proc Natl Acad Sci USA 84:4831–4835.PubMedCrossRefGoogle Scholar
  23. Hashimoto S, Iwasaki C, Kuzuya H, Guroff G (1986) Regulation of nerve growth factor action on Nspl00 phosphorylation on PC12h cells by calcium. J Neurochem 46:1599–1604.PubMedCrossRefGoogle Scholar
  24. Hatanaka H, Otten U, Thoenen H (1978) Nerve growth factor mediated selective induction of ornithine decarboxylase in rat pheochromocytoma: a cyclic AMP-independent process. FEBS Lett 92:313–316.PubMedCrossRefGoogle Scholar
  25. Hofmann T, Kawakami M, Hitchman AJW, Harrison JE, Dorrington KJ (1979) The amino acid sequence of porcine intestinal calcium-binding protein. Can J Biochem 57:737–748.PubMedCrossRefGoogle Scholar
  26. Isobe T, Okuyama T (1981) The amino-acid sequence of the a subunit in bovine brain S-100a protein. EUR J Biochem 116:79–86.PubMedCrossRefGoogle Scholar
  27. Jackson-Grusby LL, Swiergiel J, Linzer DIH (1987) A growth-related mRNA in cultured mouse cells encodes a placental calcium binding protein. Nucleic Acids Res 15:6677–6690.PubMedCrossRefGoogle Scholar
  28. Johnsson N, Van PN, Söling HD, Weber K (1986) Functionally distinct serine phosphorylation sites of p36, the cellular substrate of retroviral protein kinase: differential inhibition of reassociation with p11. EMBO J 5:3455–3460.PubMedGoogle Scholar
  29. Johnsson N, Marriott G, Weber K (1988) p36, the major cytoplasmic substrate of src tyrosine protein kinase, binds to its p11 regulatory subunit via a short amino-terminal amphiphatic helix. EMBO J 7:2435–2442.PubMedGoogle Scholar
  30. Kater SB, Mattson MP, Cohan C, Connor J (1988) Calcium regulation of the neuronal growth cone. Trends Neurosci 11:315–321.PubMedCrossRefGoogle Scholar
  31. Kligman D, Marshak DR (1985) Purification and characterization of a neurite extension factor from bovine brain. Proc Natl Acad Sci USA 82:7136–7139.PubMedCrossRefGoogle Scholar
  32. Koike T, Martin DP, Johnson EM (1989) Role of Ca2+ channels in the ability of membrane depolarization to prevent neuronal death induced by the trophic-factor deprivation: evidence that levels of internal Ca2+ determine nerve growth factor dependence of sympathetic ganglion cells. Proc Natl Acad Sci USA 86:6421–6425.PubMedCrossRefGoogle Scholar
  33. Kruijer W, Schubert D, Verma IM (1985) Induction of the proto-oncogene fos by nerve growth factor. Proc Natl Acad Sci USA 82:7330–7334.PubMedCrossRefGoogle Scholar
  34. Landreth G, Cohen P, Shooter EM (1980) Ca2+ transmembrane fluxes and nerve growth factor action on a clonal cell line of rat pheochromocytoma. Nature 283:202–204.PubMedCrossRefGoogle Scholar
  35. Leonard DG, Ziff EB, Greene LA (1987) Identification and characterization of mRNAs regulated by nerve growth factor in PC12 cells. Mol Cell Biol 7:3156–3167.PubMedGoogle Scholar
  36. Masiakowski P, Shooter EM (1988) Nerve growth factor induces the genes for two proteins related to a family of calcium-binding proteins in PC12 cells. Proc Natl Acad Sci USA 85:1277–1281.PubMedCrossRefGoogle Scholar
  37. Masiakowski P, Shooter EM (1990) Changes in PC12 cell morphology induced by transfection with 42C DNA, a member of the S-100 family. J Neurosci Res (in press).Google Scholar
  38. McBurney RN, Neering IR (1987) Neuronal calcium homeostasis. Trends Neurosci 10:164–169.CrossRefGoogle Scholar
  39. Moore BW (1965) A soluble protein characteristic of the nervous system. Biochem Biophys Res Commun 19:739–744.PubMedCrossRefGoogle Scholar
  40. Morgan JI, Curran T (1986) Role of ion flux in the control of c-fos expression. Nature 322:552–555.PubMedCrossRefGoogle Scholar
  41. Odink K, Cerletti N, Brüggen J, Clerc RG, Tarcsay L, Zwadlo G, Gerhards G, Schlegl R, Sorg C (1987) Two calcium-binding proteins in infiltrate macrophages of rheumatoid arthritis. Nature 330:80–82.PubMedCrossRefGoogle Scholar
  42. Pandiella-Alonso A, Malgaroli A, Vicentini LM, Meldolesi J (1986) Early rise of cytosolic Ca2+ induced by NGF in PC12 and chromaffin cells. FEBS Lett 208:48–51.PubMedCrossRefGoogle Scholar
  43. Schubert D, LaCorbiere M, Whitlock C, Stallcup W (1978) Alterations in the surface properties of cells responsive to nerve growth factor. Nature 273:718–723.PubMedCrossRefGoogle Scholar
  44. Snider WD, Johnson EM (1989) Neurotrophic molecules. Ann Neurol 26:489–506.PubMedCrossRefGoogle Scholar
  45. Szebenyi DME, Obendorf SK, Moffat K (1981) Structure of vitamin D-dependent calcium-binding protein from bovine intestine. Nature 294:327–332.PubMedCrossRefGoogle Scholar
  46. Thompson MA, Ziff EB (1989) Structure of the gene encoding peripherin, an NGF-regulated neuronal-specific type III intermediate filament protein. Neuron 2:1043–1053.PubMedCrossRefGoogle Scholar
  47. Winningham-Major F, Staecker JL, Barger SW, Coats S, van Eldik LJ (1989) Neurite extension and neuronal survival activities of recombinant S100b proteins that differ in the content and position of cysteine residues. J Cell Biol 109:3063–3071.PubMedCrossRefGoogle Scholar
  48. Zimmer DB, van Eldik LJ (1986) Identification of a molecular target for the calcium-modulated protein S100: Fructose-l,6-bisphosphate aldolase. J Biol Chem 261:11424–11428.PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1991

Authors and Affiliations

  • Piotr Masiakowski
  • Eric M. Shooter

There are no affiliations available

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