Abstract
Protein kinases C (PKCs) comprise closely related Ser/Thr kinases, ubiquitously present in animal tissues; they respond to second messengers, e.g., Ca2+ and/or diacylglycerol, to express their activities. Two PKCs have been sequenced fromGeodia cydonium, a member of the lowest multicellular animals, the sponges (Porifera). One spongeG. cydonium PKC, GCPKC1, belongs to the “novel” (Ca2+-independent) PKC (nPKC) subfamily while the second one, GCPKC2, has the hallmarks of the “conventional” (Ca2+-dependent) PKC (cPKC) subfamily. The alignment of the Ser/Thr catalytic kinase domains, of the predicted as sequences for these cDNAs with respective segments from previously reported sequences, revealed highest homology to PKCs from animals but also distant relationships to Ser/Thr kinases from protozoa, plants, and bacteria. However, a comparison of the complete structures of the sponge PKCs, which are-already-identical to those of nPKCs and cPKCs from higher metazoa, with the structures of protozoan, plant, and bacterial Ser/Thr kinases indicates that the metazoan PKCs have to be distinguished from the nonmetazoan enzymes. These data indicate that metazoan PKCs have a universal common ancestor which they share with the nonmetazoan Ser/Thr kinases with respect to the kinase domain, but they differ from them in overall structural composition.
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Ausubel FM, Brent R, Kingston RE, Moore DD, Smith JA, Seidman JG, Struhl K (1995) Current protocols in molecular biology. John Wiley and Sons, New York
Biermann B, Johnson EM, Feldman LJ (1990) Characterization and distribution of a maize cDNA encoding a peptide similar to the catalytic region of second messenger dependent protein kinases. Plant Physiol 94: 1609–1615
Blake MS, Johnston KH, Russell-Jones GJ, Gotschlich EC (1984) A rapid, sensitive method for detection of alkaline phosphatase-conjugated anti-antibody on Western blots. Anal Biochem 136: 175–179
Branden C, Tooze J (1991) Introduction to protein structure. Gerland, New York
Bürki E, Anjard C, Scholder JC, Reymond CD (1991) Isolation of two genes encoding putative protein kinases regulated duringDictyostelium discoideum development. Gene 102: 57–65
Cocco L, Martelli AM, Gilmour RS (1994) Inositol lipid cycle in the nucleus. Cell Signal 6: 481–485
Csaba G (1994) Phylogeny and ontogeny of chemical signalling: origin and development of hormone receptors. Int Rev Cytol 155: 1–48
Daum G, Eisenmann-Tappe I, Fries HW, Troppmair J, Rapp UF (1994) The ins and outs of Raf kinases. Trends Biochem Sci 19: 474–480
Disatnik MH, Winnier AR, Mochly-Rosen D, Arteaga CL (1994) Distinct responses of protein kinase C isoenzymes to c-erbB-2 activation in SKBR-3 human breast carcinoma cells. Cell Growth Differ 5: 873–880
EMBL Sequence Database, Release 40 (September 1994)
Gale MJ, Parsons M (1993) ATrypanosoma brucei gene family encoding protein kinases with catalytic domains structurally related to Nek1 and NIMA. Mol Biochem Parasitol 59: 111–121
Gorby GL, Robinson EN, Barley LR, Clemens CM, McGee ZA (1988) Microbial invasion: a covert activity? Can J Microbiol 34:507–512
Hanks SK, Quinn AM (1991) Protein kinase catalytic domain sequence database: identification of conserved features of primary structure and classification of family members. Methods Enzymol 200A:3–37
Hanks SK, Quinn AM, Hunter T (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241: 42–52
Hardie G, Hanks S (1995) The protein kinase factsbook: protein-serine kinases. Academic Press, London
Higgins DG, Sharp PM (1988) CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73: 237–244
Kikkawa U, Ogita K, Ono Y, Asaoka Y, Shearman MS, Fujii T, Ase K, Sekiguchi K, Igarashi K, Nishizuka Y (1987) The common structure and activities of four subspecies of rat brain protein kinase C family. FEBS Lett 223: 212–216
Kruse M, Mikoc A, Cetkovic H, Gamulin V, Rinkevich B, Müller IM, Müller WG (1994) Molecular evidence for the presence of a developmental gene in the lowest animals: identification of a homeobox-like gene in the marine spongeGeodia cydonium. Mech Ageing Dev 77: 43–54
Kubo K, Ohno S, Suzuki K (1987) Primary structures of human protein kinase C beta-I and beta-II differ only in their C-terminal sequences. FEBS Lett 223: 138–142
Land M, Islas-Trejo A, Freedman JH, Rubin CS (1994) Structure and expression of a novel, neuronal protein kinase C (PKCIB) fromCaenorhabditis elegans. PKCIB is expressed selectively in neurons that receive, transmit, and process environmental signals. J Biol Chem 269: 9234–9244
Lawton MA, Yamamoto RT, Hanks SK, Lamb CJ (1989) Molecular cloning of plant transcripts encoding protein kinase homologs. Proc Natl Acad Sci USA 86: 3140–3144
Levin DE, Fields O, Kunisawa R, Bishop JM, Thorner J (1990) A candidate protein kinase C gene, PKC1, is required for theS. cerevisiae cell cycle. Cell 62: 213–224
Mahoney CW, Huang KP (1994) Molecular and catalytic properties of protein kinase C. In: Kuo IF (ed) Protein kinase C. Oxford University Press, New York, pp 16–63
McLeod M, Beach D (1986) Homology between the ran 1+ gene fission yeast and protein kinases. EMBO 15: 3665–3671
Müller WEG (1995) Molecular phylogeny of metazoa [animals]: monophyletic origin. Naturwissenschaften 82: 321–329
Müller WEG, Rottmann M, Diehl-Seifert B, Kurelec B, Uhlenbruck G, Schröder HC (1987) Role of the aggregation factor in the regulation of phosphoinositide metabolism in sponges. Possible consequences on calcium efflux and on mitogenesis. J Biol Chem 262: 9850–9858
Müller WEG, Ugarkovic D, Gamulin V, Weiler E, Schröder HC (1990) Intracellular signal transduction pathways in sponges. Electron Microsc Rev 3: 97–114
Munoz-Dorado J, Inouye S, Inouye M (1991) A gene encoding a protein serine/threonine kinase is required for normal development ofM. xanthus, a gram-negative bacterium. Cell 67: 995–1006
Nishizuka Y (1988) The molecular heterogeneity of protein kinase-C and its implications for cellular regulation. Nature 334: 661–665.
PC/GENE (1995) Data Banks CD-ROM; Release 14.0. IntelliGenetics, Inc. Mountain View, CA
Pfeifer K, Frank W, Schröder HC, Gamulin V, Rinkevich B, Müller IM, Müller WEG (1993a) cDNA cloning of the polyubiquitin gene from the marine spongeGeodia cydonium which is preferentially expressed during reaggregation of cells. J Cell Science 106: 545–554
Pfeifer K, Haasemann M, Gamulin V, Bretting H, Fahrenholz F, Müller WEG (1993b) S-type lectins occur also in invertebrates: unusual subunit composition and high conservation of the carbohydrate recognition domain in the lectin genes from the marine spongeGeodia cydonium. Glycobiology 3: 179–184
Pühler G, Leffers H, Gropp F, Palm P, Klenk HP, Lottspeich F, Garrett RA, Zillig W (1989) Archaebacterial DNA-dependent RNA polymerases testify to the evolution of the eukaryotic nuclear genome. Proc Natl Acad Sci USA 86: 4569–4573
Rakow TL, Shen SS (submitted) Molecular cloning and characterization of protein kinase C from the sea urchinLytechinus pictus. (cited from: EMBL Sequence Database, Release 40) -
Rose-John S, Dietrich A, Marks F (1988) Molecular cloning of mouse protein kinase C (PKC) cDNA from Swiss 3T3 fibroblasts. Gene 74: 465–471
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467
Schäcke H, Müller WEG, Gamulin V, Rinkevich B (1994a) The Ig superfamily includes members from the lowest invertebrates to the highest invertebrates. Immunol Today 15: 497–498
Schäcke H, Schröder HC, Gamulin V, Rinkevich B, Müller IM, Müller WEG (1994b) Molecular cloning of a receptor tyrosine kinase from the marine spongeGeodia cydonium: a new member of the receptor tyrosine kinase class II family in invertebrates. Mol Membr Biol 11: 101–107
Schaeffer E, Smith D, Mardon G, Quinn W, Zuker C (1989) Isolation and characterization of two newDrosophila protein kinase C genes, including one specifically expressed in photoreceptor cells. Cell 57: 403–412
Schröder HC, Rottmann M, Wenger R, Bachmann M, Dorn A, Müller WEG (1988) Studies on protein kinases involved in regulation of nucleocytoplasmic mRNA transport. Biochem J 252: 777–790
Stabel S, Parker PJ (1991) Protein kinase C. Pharmacol Ther 51: 71–95
Takai Y, Kishimoto A, Inoue M, Nishizuka Y (1977) Studies on a cyclic nucleotide independent protein kinase and its proenzyme in mammalian tissues. J Biol Chem 252: 7603–7609
Weissmann G, Riesen W, Davidson S, Waite M (1988) Stimulus coupling in marine sponge cell aggregation: lipid metabolism and the function of exogenously added arachidonic and docosahexaenoic acids. Biochim Biophys Acta 960: 351–364
Zarkower D, Stephenson P, Sheets M, Wickens M (1986) The AAUAAA sequence is required both for cleavage and for polyadenylation of simian virus 40 pre-mRNAin vitro. Mol Cell Biol 6: 2317–2323
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Correspondence to: W.E.G. Müller
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Kruse, M., Gamulin, V., Cetkovic, H. et al. Molecular evolution of the Metazoan protein kinase C multigene family. J Mol Evol 43, 374–383 (1996). https://doi.org/10.1007/BF02339011
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DOI: https://doi.org/10.1007/BF02339011