653
Views
19
CrossRef citations to date
0
Altmetric
Review Article

cAMP-dependent signal pathways in unicellular eukaryotes

Pages 23-42 | Received 27 Dec 2007, Accepted 07 Oct 2008, Published online: 01 Feb 2009

References

  • Abel, E.S., Davids, B.J., Robles, L.D., Loflin, C.E., Gillin, F.D., and Chakrabarti, R. 2001. Possible roles of protein kinase A in cell motility and excystation of the early diverging eukaryote Giardia lamblia. J. Biol. Chem. 276, 10320–10329.
  • Alexandre, S., Paindavoine, P., Hanocq-Quertier, J., Paturiaux-Hanocq, F., Tebabi, P., and Pays, E. 1996. Families of adenylate cyclase genes in Trypanosoma brucei. Mol. Biochem. Parasitol. 77, 173–182.
  • Alspaugh, J.A., Perfect, J.R., and Heitman, J. 1997. Cryptococcus neoformans mating and virulence are regulated by the G-protein alpha subunit GPA1 and cAMP. Genes Dev. 11, 3206–3217.
  • Anjard, C., Pinaud, S., Kay, R.R., and Reymond, C.D. 1992. Overexpression of Dd PK2 protein kinase causes rapid development and affects the intracellular cAMP pathway of Dictyostelium discoideum. Development. 115, 785–790.
  • Ansari, K., Martin, S., Farkasovsky, M., Ehbrecht, I.M., and Kuntzel, H. 1999. Phospholipase C binds to the receptor-like GPR1 protein and controls pseudohyphal differentiation in Saccharomyces cerevisiae. J. Biol. Chem. 274, 30052–30058.
  • Araki, T., Gamper, M., Early, A., Fukuzawa, M., Abe, T., Kawata, T., Kim, E., Firtel, R.A., and Williams, J.G. 1998. Developmentally and spatially regulated activation of a Dictyostelium STAT protein by a serpentine receptor. EMBO J. 17, 4018–4028.
  • Aubry, L., and Firtel, R. 1999. Integration of signaling networks that regulate Dictyostelium differentiation. Annu. Rev. Cell Dev. Biol. 15, 469–517.
  • Baldwin, J.M. 1994. Structure and function of receptors coupled to G proteins. Curr. Opin. Cell Biol. 6, 180–190.
  • Boy-Marcotte, E., Perrot, M., Bussereau, F., Boucherie, H., and Jacquet, M. 1998. Msn2p and Msn4p control a large number of genes induced at the diauxic transition which are repressed by cyclic AMP in Saccharomyces cerevisiae. J. Bacteriol. 180, 1044–1052.
  • Brandon, M.A., Mahadeo, D.C., and Podgorski, G.J. 2002. Galpha3 and protein kinase A represent cross–talking pathways for gene expression in Dictyostelium discoideum. Dev. Growth Differ. 44, 457–465.
  • Brandon, M.A., and Podgorski, G.J. 1997. G alpha 3 regulates the cAMP signaling system in Dictyostelium. Mol. Biol. Cell. 8, 1677–1685.
  • Carlson, G.L., and Nelson, D.L. 1996. The 44–kDa regulatory subunit of the Paramecium cAMP–dependent protein kinase lacks a dimerization domain and may have a unique autophosphorylation site sequence. J. Eukaryot. Microbiol. 43, 347–356.
  • Cases, I., and de Lorenzo, V. 1998. Expression systems and physiological control of promoter activity in bacteria. Curr. Opin. Microbiol. 1, 303–310.
  • Cassel, D., Shoubi, S., Glusman, G., Cukierman, E., Rotman, M., and Zilberstein, D. 1991. Leishmania donovani: characterization of a 38–kDa membrane protein that cross–reacts with the mammalian G-protein transducin. Exp. Parasitol. 72, 411–417.
  • Chen, M.Y., Long, Y., and Devreotes, P.N. 1997. A novel cytosolic regulator, Pianissimo, is required for chemoattractant receptor and G protein–mediated activation of the 12 transmembrane domain adenylyl cyclase in Dictyostelium. Genes Dev. 11, 3218–3231.
  • Chen, Y., Cann, M.J., Litvin, T.N., Iourgenko, V., Sinclair, M.L., Levin, L.R., and Buck, J. 2000. Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science. 289, 625–628.
  • Colombo, S., Ma, P., Cauwenberg, L., Winderickx, J., Crauwels, M., Teunissen, A., Nauwelaers, D., de Winde, J. H., Gorwa, M. F., Colavizza, D., and Thevelein, J. M. 1998. Involvement of distinct G–proteins, Gpa2 and Ras, in glucose- and intracellular acidification-induced cAMP signalling in the yeast Saccharomyces cerevisiae. EMBO J. 17, 3326–3341.
  • Cooper, D.M., Mons, N., and Karpen, J.W. 1995. Adenylyl cyclases and the interaction between calcium and cAMP signalling. Nature. 374, 421–424.
  • Dejean, L., Beauvoit, B., Alonso, A. P., Bunoust, O., Guerin, B., and Rigoulet, M. 2002. cAMP–induced modulation of the growth yield of Saccharomyces cerevisiae during respiratory and respiro– fermentative metabolism. Biochim. Biophys. Acta. 1554, 159–169.
  • Devreotes, P.N. 1994. G–protein–linked signaling pathways control the developmental program of Dictyostelium. Neuron. 12, 235–241.
  • Dyer, M., and Day, K. 2000. Expression of Plasmodium falciparum trimeric G proteins and their involvement in switching to sexual development. Mol. Biochem. Parasitol. 108, 67–78.
  • Endl, I., Konzok, A., and Nellen, W. 1996. Antagonistic effects of signal transduction by intracellular and extracellular cAMP on gene regulation in Dictyostelium. Mol. Biol. Cell. 7, 17–24.
  • Escalante, R., and Sastre, L. 2002. Regulated expression of the MADS–box transcription factor SrfA mediates activation of gene expression by protein kinase A during Dictyostelium sporulation. Mech. Dev. 117, 201–208.
  • Estruch, F. 1996. The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J. 15, 2227–2235.
  • Etchebehere, L.C., Van Bemmelen, M.X., Anjard, C., Traincard, F., Assemat, K., Reymond, C., and Veron, M. 1997. The catalytic subunit of Dictyostelium cAMP–dependent protein kinase – role of the N–terminal domain and of the C–terminal residues in catalytic activity and stability. Eur. J. Biochem. 248, 820–826.
  • Evans, T., Fawzi, A., Fraser, E.D., Brown, M. L., and Northup, J.K. 1987. Purification of a beta 35 form of the beta gamma complex common to G-proteins from human placental membranes. J. Biol. Chem. 262, 176–181.
  • Fagan, K.A., Mons, N., and Cooper, D.M. 1998. Dependence of Ca2+–inhibitable adenylyl cyclase of C6–2B glioma cells on capacitative Ca2+ entry. J. Biol. Chem. 273, 9297–9305.
  • Farber, M.D., Montagna, A.E., Paveto, C., Dollet, M., Sanchex-Moreno, M., Osuna, A., Torres, H.N., and Flawia, M.M. 1995. Adenylyl cyclase and G-proteins in Phytomonas. J. Eukaryot. Microbiol. 42, 257–260.
  • Federman, A.D., Conklin, B.R., Schrader, K.A., Reed, R.R., and Bourne, H.R. 1992. Hormonal stimulation of adenylyl cyclase through Gi–protein beta gamma subunits. Nature. 356, 159–161.
  • Fimia, G.M., and Sassone-Corsi, P. 2001. Cyclic AMP signalling. J. Cell Sci. 114, 1971–1972.
  • Fong, H.K., Amatruda, T.T. 3rd, Birren, B.W., and Simon, M.I. 1987. Distinct forms of the beta subunit of GTP–binding regulatory proteins identified by molecular cloning. Proc. Natl. Acad. Sci. 84, 3792–3796.
  • Francis, S.H., and Corbin, J.D. 1999. Cyclic nucleotide-dependent protein kinases: intracellular receptors for cAMP and cGMP action. Crit. Rev. Clin. Lab. Sci. 36, 275–328.
  • Franco, E., Manning-Cela, R., and Meza, I. 2000. Signal transduction pathways in Entamoeba histolytica: PKA activity and translocation during the interaction of trophozoites with FN. Arch. Med. Res. 31, S126–S127.
  • Franco, E., Manning-Cela, R., and Meza, I. 2002. Signal transduction in Entamoeba histolytica induced by interaction with fibronectin: presence and activation of phosphokinase A and its possible relation to invasiveness. Arch. Med. Res. 33, 389–397.
  • Gagiano, M., Bester, M., Van Dyk, D., Franken, J., Bauer, F.F., and Pretorius, I.S. 2003. Mss11p is a transcription factor regulating pseudohyphal differentiation, invasive growth and starch metabolism in Saccharomyces cerevisiae in response to nutrient availability. Mol. Microbiol. 47, 119–134.
  • Garbers, D.L. 2000. The guanylyl cyclase receptors. Zygote. 8, S24–325.
  • Garbers, D.L., Koesling, D., and Schultz, G. 1994. Guanylyl cyclase receptors. Mol. Biol. Cell. 5, 1–5.
  • Garreau, H., Hasan, R.N., Renault, G., Estruch, F., Boy-Marcotte, E., and Jacquet, M. 2000. Hyperphosphorylation of Msn2p and Msn4p in response to heat shock and the diauxic shift is inhibited by cAMP in Saccharomyces cerevisiae. Microbiology. 146, 2113–2120.
  • Gorner, W., Durchschlag, E., Martinez-Pastor, M.T., Estruch, F., Ammerer, G., Hamilton, B., Ruis, H., and Schuller, C. 1998. Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev. 12, 586–597.
  • Griffioen, G., and Thevelein, J.M. 2002. Molecular mechanisms controlling the localisation of protein kinase A. Curr. Genet. 41, 199–207.
  • Gundersen, R.E., and Devreotes, P.N. 1990. In vivo receptor–mediated phosphorylation of a G protein in Dictyostelium. Science. 248, 591–593.
  • Hadwiger, J.A., Natarajan, K., and Firtel, R.A. 1996. Mutations in the Dictyostelium heterotrimeric G protein alpha subunit G alpha5 alter the kinetics of tip morphogenesis. Development. 122, 1215–1224.
  • Hadwiger, J.A., and Srinivasan, J. 1999. Folic acid stimulation of the Galpha4 G protein–mediated signal transduction pathway inhibits anterior prestalk cell development in Dictyostelium. Differentiation. 64, 195–204.
  • Hadwiger, J.A., Wilkie, T.M., Strathmann, M., and Firtel, R.A. 1991. Identification of Dictyostelium G alpha genes expressed during multicellular development. Proc. Natl. Acad. Sci. 88, 8213–8217.
  • Harashima, T., Heitman, J. 2002. The Galpha protein Gpa2 controls yeast differentiation by interacting with kelch repeat proteins that mimic Gbeta subunits. Mol. Cell. 10, 163–173.
  • Harwood, A.J., Hopper, N.A., Simon, M.N., Bouzid, S., Veron, M., and Williams, J.G. 1992. Multiple roles for cAMP–dependent protein kinase during Dictyostelium development. Dev. Biol. 149, 90–99.
  • Hassenzahl, D.L., Yorgey, N.K., Keedy, M.D., Price, A.R., Hall, J.A., Myzcka, C.C., and Kuruvilla, H.G. 2001. Chemorepellent signaling through the PACAP/lysozyme receptor is mediated through cAMP and PKC in Tetrahymena thermophila. J. Comp. Physiol. [A]. 187, 171–176.
  • Hereld, D., Vaughan, R., Kim, J.Y., Borleis, J., and Devreotes, P. 1994. Localization of ligand–induced phosphorylation sites to serine clusters in the C–terminal domain of the Dictyostelium cAMP receptor, cAR1. J. Biol. Chem. 269, 7036–7044.
  • Herskowitz, I. 1995. MAP kinase pathways in yeast: for mating and more. Cell. 80, 187–197.
  • Hochstrasser, M., Carlson, G.L., Walczak, C.E., and Nelson, D.L. 1996. Paramecium has two regulatory subunits of cyclic AMP–dependent protein kinase, one unique to cilia. J. Eukaryot. Microbiol. 43, 356–362.
  • Huang, Y.E., Iijima, M., Parent, C.A., Funamoto, S., Firtel, R.A., and Devreotes, P. 2003. Receptor-mediated regulation of PI3Ks confines PI(3,4,5)P3 to the leading edge of chemotaxing cells. Mol. Biol. Cell. 14, 1913–1922.
  • Hubler, L., Bradshaw-Rouse, J., and Heideman, W. 1993. Connections between the Ras–cyclic AMP pathway and G1 cyclin expression in the budding yeast Saccharomyces cerevisiae. Mol. Cell Biol. 13, 6274–6282.
  • Hurley, J.H. 1998. The adenylyl and guanylyl cyclase superfamily. Curr. Opin. Struct. Biol. 8, 770–777.
  • Hurwitz, N., Segal, M., Marbach, I., and Levitzki, A. 1995. Differential activation of yeast adenylyl cyclase by Ras1 and Ras2 depends on the conserved N terminus. Proc. Natl. Acad. Sci. 92, 11009–11013.
  • Insall, R., Kuspa, A., Lilly, P.J., Shaulsky, G., Levin, L.R., Loomis, W.F., and Devreotes, P. 1994. CRAC, a cytosolic protein containing a pleckstrin homology domain, is required for receptor and G protein–mediated activation of adenylyl cyclase in Dictyostelium. J. Cell Biol. 126, 1537–1545.
  • Isshiki, T., Mochizuki, N., Maeda, T., and Yamamoto, M. 1992. Characterization of a fission yeast gene, gpa2, that encodes a G alpha subunit involved in the monitoring of nutrition. Genes Dev. 6, 2455–2462.
  • Janetopoulos, C., Jin, T., and Devreotes, P. 2001. Receptor–mediated activation of heterotrimeric G–proteins in living cells. Science. 291, 2408–2411.
  • Kataoka, T., Broek, D., and Wigler, M. 1985. DNA sequence and characterization of the S. cerevisiae gene encoding adenylate cyclase. Cell. 43, 493–505.
  • Kendall, R.L., Yamada, R., and Bradshaw, R.A. 1990. Cotranslational amino–terminal processing. Methods Enzymol. 185, 398–407.
  • Kim, H.J., Chang, W.T., Meima, M., Gross, J.D., and Schaap, P. 1998. A novel adenylyl cyclase detected in rapidly developing mutans of Dictyostelium. J. Biol. Chem. 273, 30859–30862.
  • Kiriyama, H., Nanmori, T., Hari, K., Matsuoka, D., Fukami, Y., Kikkawa, U., and Yasuda, T. 1999. Identification of the catalytic subunit of cAMP–dependent protein kinase from the photosynthetic flagellate, Euglena gracilis Z. FEBS Lett. 450, 95–100.
  • Klein, P.S., Sun, T.J., Saxe, C.L. 3rd, Kimmel, A.R., Johnson, R.L., and Devreotes, P.N. 1988. A chemoattractant receptor controls development in Dictyostelium discoideum. Science. 241, 1467–1472.
  • Kozasa, T., Jiang, X., Hart, M.J., Sternweis, P.M., Singer, W.D., Gilman, A.G., Bollag, G., and Sternweis, P.C. 1998. p115 RhoGEF, a GTPase activating protein for Galpha12 and Galpha13. Science. 280, 2109–2111.
  • Kriebel, P.W., Barr, V.A., and Parent, C.A. 2003. Adenylyl cyclase localization regulates streaming during chemotaxis. Cell. 112, 549–560.
  • Kubler, E., Mosch, H.U., Rupp, S., and Lisanti, M.P. 1997. Gpa2p, a G–protein alpha–subunit, regulates growth and pseudohyphal development in Saccharomyces cerevisiae via a cAMP–dependent mechanism. J. Biol. Chem. 272, 20321–20323.
  • Kumagai, A., Hadwiger, J. A., Pupillo, M., and Firtel, R.A. 1991. Molecular genetic analysis of two G alpha protein subunits in Dictyostelium. J. Biol. Chem. 266, 1220–1228.
  • Kumagai, A., Pupillo, M., Gundersen, R., Miake-Lye, R., Devreotes, P.N., and Firtel, R.A. 1989. Regulation and function of G alpha protein subunits in Dictyostelium. Cell. 57, 265–275.
  • Kuruvilla, H.G., and Hennessey, T.M. 1998. Purification and characterization of a novel chemorepellent receptor from Tetrahymena thermophila. J. Membr. Biol. 162, 51–57.
  • Lee, S., Parent, C.A., Insall, R., and Firtel, R.A. 1999. A novel Ras–interacting protein required for chemotaxis and cyclic adenosine monophosphate signal relay in Dictyostelium. Mol. Biol. Cell. 10, 2829–2845.
  • Leichtling, B.H., Majerfeld, I.H., Spitz, E., Schaller, K.L., Woffendin, C., Kakinuma, S., and Rickenberg, H.V. 1984. A cytosolic cyclic AMP–dependent protein kinase in Dictyostelium discoideum. II. Developmental regulation. J. Biol. Chem. 259, 662–668.
  • Leighfield, T.A., Barbier, M., and Van Dolah, F.M. 2002. Evidence for cAMP–dependent protein kinase in the dinoflagellate, Amphidinium operculatum. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 133, 317–324.
  • Li, J., and Cox, L.S. 2000. Isolation and characterisation of a cAMP–dependent protein kinase catalytic subunit gene from Plasmodium falciparum. Mol. Biochem. Parasitol. 109, 157–163.
  • Lilly, P.J., and Devreotes, P.N. 1995. Dictyostelium requires translocation of CRAC to membranes. J. Cell Biol. 129:1659–1665.
  • Lilly, P., Wu, L., Welker, D.L., and Devreotes, P.N. 1993. A G–protein beta–subunit is essential for Dictyostelium development. Genes Dev. 7, 986–995.
  • Linder, J.U., Engel, P., Reimer, A., Kruger, T., Platner, H., Schultz, A., and Schultz, J.E. 1999. Guanyl cyclases with the topology of mammalian adenylyl cyclases and an N–terminal P–type ATPase–like domain in Paramecium, Tetrahymena and Plasmodium. EMBO J. 18, 4222–4232.
  • Linder, J.U., Hoffmann, T., Kurz, U., and Schultz, J.E. 2000. A guanylyl cyclase from Paramecium with 22 transmembrane spans. Expression of the catalytic domains and formation of chimeras with the catalytic domains of mammalian adenylyl cyclases. J. Biol. Chem. 275, 11235–11240.
  • Liu, H. 2002. Co-regulation of pathogenesis with dimorphism and phenotypic switching in Candida albicans, a commensal and a pathogen. Int. J. Med. Microbiol. 292, 299–311.
  • Lopez-Ilasaca, M. 1998. Signaling from G-protein-coupled receptors to mitogen-activated protein (MAP)-kinase cascades. Biochem. Pharmacol. 56, 269–277.
  • Lopez-Ilasaca, M., Crespo, P., Pellici, P.G., Gutkind, J. S., and Wetzker, R. 1997. Linkage of G protein-coupled receptors to the MAPK signaling pathway through PI 3-kinase gamma. Science. 275, 394–397.
  • Lorenz, M.C., Pan, X., Harashima, T., Cardenas, M.E., Xue, Y., Hirsch, J.P., and Heitman, J. 2000. The G protein-coupled receptor gpr1 is a nutrient sensor that regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Genetics. 154, 609–622.
  • Ma, P., Wera, S., Van Dijck, P., Thevelein, J.M. 1999. The PDE1-encoded low-affinity phosphodiesterase in the yeast Saccharomyces cerevisiae has a specific function in controlling agonist-induced cAMP signaling. Mol. Biol. Cell. 10, 91–104.
  • Maeda, T., Watanabe, Y., Kunitomo, H., and Yamamoto, M. 1994. Cloning of the pka1 gene encoding the catalytic subunit of the cAMP-dependent protein kinase in Schizosaccharomyces pombe. J. Biol. Chem. 269, 9632–9637.
  • Maeda, M., Aubry, L., Insall, R., Gaskins, C., Devreotes, P.N., and Firtel, R.A. 1996. Seven helix chemoattractant receptors transiently stimulate mitogen–activated protein kinase in Dictyostelium. J. Biol. Chem. 271, 3351–3354.
  • Mann, S.K., Yonemoto, W.M, Taylor, S.S., and Firtel, R.A. 1992. DdPK3, which plays essential roles during Dictyostelium development, encodes the catalytic subunit of cAMP–dependent protein kinase. Proc. Natl. Acad. Sci. 89, 10701–10705.
  • Marino, M.J., Sherman, T.G., and Wood, D.C. 2001. Partial cloning of putative G–proteins modulating mechanotransduction in the ciliate Stentor. J. Eukaryot. Microbiol. 48, 527–536.
  • Meili, R., Ellsworth, C., Lee, S., Reddy, T.B., Ma, H., and Firtel, R.A. 1999. Chemoattractant-mediated transient activation and membrane localization of Akt/PKB is required for efficient chemotaxis to cAMP in Dictyostelium. EMBO J. 18, 2092–2105.
  • Meima, M., Schaap, P. 1999. Dictyostelium development–socializing through cAMP. Semin. Cell Dev. Biol. 10, 567–576.
  • Mintzer, K.A., and Field, J. 1999. The SH3 domain of the S. cerevisiae Cdc25p binds adenylyl cyclase and facilitates Ras regulation of cAMP signalling. Cell Signal. 11, 127–135.
  • Mogi, M., and Togari, A. 2003. Activation of caspases is required for osteoblastic differentiation. J. Biol. Chem. 278, 47477–82464.
  • Mohanty, S., Lee, S., Yadava, N., Dealy, M.J., Johnson, R.S., and Firtel, R.A. 2001. Regulated protein degradation controls PKA function and cell–type differentiation in Dictyostelium. Genes Dev. 15, 1435–1448.
  • Mutzel, R., Simon, M.N., Lacombe, M.L., and Veron, M. 1988. Expression and properties of the regulatory subunit of Dictyostelium cAMP–dependent protein kinase encoded by lambda gt11 cDNA clones. Biochemistry. 27, 481–486.
  • Nakafuku, M., Obara, T., Kaibuchi, K., Miyajima, I., Miyajima, A., Itoh, H., Nakamura, S., Arai, K., Matsumoto, K., and Kaziro, Y. 1988. Isolation of a second yeast Saccharomyces cerevisiae gene (GPA2) coding for guanine nucleotide–binding regulatory protein: studies on its structure and possible functions. Proc. Natl. Acad. Sci. 85, 1374–1378.
  • Neer, E.J. 1995. Heterotrimeric G proteins: organizers of transmembrane signals. Cell. 80, 249–257.
  • Obara, T., Nakafuku, M., Yamamoto, M., and Kaziro, Y. 1991. Isolation and characterization of a gene encoding a G-protein alpha subunit from Schizosaccharomyces pombe: involvement in mating and sporulation pathways. Proc. Natl. Acad. Sci. 88, 5877–5881.
  • Okaichi, K., Cubitt, A.B., Pitt, G. S., and Firtel, R.A. 1992. Amino acid substitutions in the Dictyostelium G alpha subunit G alpha 2 produce dominant negative phenotypes and inhibit the activation of adenylyl cyclase, guanylyl cyclase, and phospholipase C. Mol. Biol. Cell. 3, 735–747.
  • Ortiz, D., del Carmen Dominguez-Robles, M., Villegas-Sepulveda, N., Meza, I. 2000. Actin induction during PMA and cAMP– dependent signal pathway activation in Entamoeba histolytica trophozoites. Cell Microbiol. 2, 391–400.
  • Ott, A., Oehme, F., Keller, H., and Schuster, S.C. 2000. Osmotic stress response in Dictyostelium is mediated by cAMP. EMBO J. 19, 5782–5792.
  • Paveto, C., Torres, H.N., Flawia, M.M., Garcia-Espitia, M., Ortega, A., and Orozco, E. 1999. Entamoeba histolytica: signaling through G proteins. Exp. Parasitol. 91, 170–175.
  • Pitt, G.S. Milona, N., Borleis, J., Lin, K.C., Reed, R.R., and Devreotes, P.N. 1992. Structurally distinct and stage–specific adenylyl cyclase genes play different roles in Dictyostelium development. Cell. 69, 305–315.
  • Primpke, G., Iassonidou, V., Nellen, W., and Wetterauer, B. 2000. Role of cAMP–dependent protein kinase during growth and early development of Dictyostelium discoideum. Dev. Biol. 221, 101–111.
  • Read, L.K., and Mikkelsen, R.B. 1991. Comparison of adenylate cyclase and cAMP–dependent protein kinase in gametocytogenic and nongametocytogenic clones of Plasmodium falciparum. J. Parasitol. 77, 346–352.
  • Renaud, F.L., Colon, I., Lebron, J., Ortiz, N., Rodriguez, F., and Cadilla, C. 1995. A novel opioid mechanism seems to modulate phagocytosis in Tetrahymena. J. Eukaryot. Microbiol. 42, 205–207.
  • Rocha, C.R., Schroppel, K., Harcus, D., Marcil, A., Dignard, D., Taylor, B.N., Thomas, D.Y., Whiteway, M., Leberer, E. 2001. Signaling through adenylyl cyclase is essential for hyphal growth and virulence in the pathogenic fungus Candida albicans. Mol. Biol. Cell. 12, 3631–3643.
  • Roelofs, J., Snippe, H., Kleineidam, R.G., and Van Haastert, P.J. 2001. Guanylate cyclase in Dictyostelium discoideum with the topology of mammalian adenylate cyclase. Biochem. J. 354, 697–706.
  • Roelofs, J., and Van Haastert, P.J. 2002. Characterization of two unusual guanylyl cyclases from Dictyostelium. J. Biol. Chem. 277, 9167–9174.
  • Ross, D.T., Raibaud, A., Florent, I.C., Sather, S., Gross, M.K., Storm, D.R., and Eisen, H. 1991. The trypanosome VSG expression site encodes adenylate cyclase and a leucine–rich putative regulatory gene. EMBO J. 10, 2047–2053.
  • Sacks, D.L., and Perkins, P.V. 1984. Identification of an infective stage of Leishmania pombe promastigotes. Science. 223, 1417–1419.
  • Sanchez, M.A., Zeoli, D., Klamo, E.M., Kavanaugh, M.P., and Landfear, S.M. 1995. A family of putative receptor–adenylate cyclases from Leishmania donovani. J. Biol. Chem. 270, 17551–17558.
  • Saxe, C.L., Klein, P., Sun, T.J., Kimmel, A.R., and Devreotes, P.N. 1988. Structure and expression of the cAMP cell–surface receptor. Dev. Genet. 9, 227–235.
  • Schadick, K., Fourcade, H.M., Boumenot, P., Seitz, J.J., Morrell, J.L., Chang, L., Gould, K.L., Partridge, J.F., Allshire, R.C., Kitagawa, K., Hieter, P., and Hoffman, C.S. 2002. Schizosaccharomyces pombe Git7p, a member of the Saccharomyces cerevisiae Sgtlp family, is required for glucose and cyclic AMP signaling, cell wall integrity, and septation. Eukaryot. Cell. 1, 558–567.
  • Schenk, P.W., Epskamp, S.J., Knetsch, M.L., Harten, V., Lagendijk, E.L., van Duijn, B., and Snaar-Jagalska, B.E. 2001. Lysophosphatidic acid– and Gbeta–dependent activation of Dictyostelium MAP kinase ERK2. Biochem. Biophys. Res. Commun. 282, 765–772.
  • Schmitt, A.P., and McEntee, K. 1996. Msn2p, a zinc finger DNA–binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. 93, 5777–5782.
  • Schultz, J.E., Klumpp, S., Benz, R., Schurhoff-Goeters, W.J., and Schmid, A. 1992. Regulation of adenylyl cyclase from Paramecium by an intrinsic potassium conductance. Science. 255, 600–603.
  • Schwartz, J.H. 2001. The many dimensions of cAMP signaling. Proc. Natl. Acad. Sci. 98, 13482–13484.
  • Seebeck, T., Gong, K., Kunz, S., Schaub, R., Shalaby, T., and Zoraghi, R. 2001. cAMP signalling in Trypanosoma brucei. Int. J. Parasitol. 31, 491–498.
  • Segall, J.E., Kuspa, A., Shaulsky, G., Ecke, M., Maeda, M., Gaskins, C., Firtel, R.A., and Loomis, W.F. 1995. A MAP kinase necessary for receptor–mediated activation of adenylyl cyclase in Dictyostelium. J. Cell Biol. 128, 405–413.
  • Shalaby, T., Liniger, M., and Seebeck, T. 2001. The regulatory subunit of a cGMP–regulated protein kinase A of Trypanosoma brucei. Eur. J. Biochem. 268, 6197–6206.
  • Shaulsky, G., Escalante, R., Fuller, D., and Loomis, W.F. 1998. A cAMP–phosphodiesterase controls PKA–dependent differentiation. Development. 125, 691–699.
  • Siman-Tov, M.M., Aly, R., Shapira, M., and Jaffe, C.L. 1996. Cloning from Leishmania major of a developmentally regulated gene, c-lpk2, for the catalytic subunit of the cAMP-dependent protein kinase. Mol. Biochem. Parasitol. 77, 201–215.
  • Siman-Tov, M.M., Ivens, A.C., and Jaffe, C.L. 2002. Molecular cloning and characterization of two new isoforms of the protein kinase A catalytic subunit from the human parasite Leishmania. Gene. 288, 65–75.
  • Simon, M.N., Pelegrini, O., Veron, M., and Kay, R.R. 1992. Mutation of protein kinase A causes heterochronic development of Dictyostelium. Nature. 356, 171–172.
  • Smith, A., Ward, M.P., and Garrett, S. 1998. Yeast PKA represses Msn2p/Msn4p–dependent gene expression to regulate growth, stress response and glycogen accumulation. EMBO J. 17, 3556–3564.
  • Snaar-Jagalska, B.E., Kesbeke, F., and van Haastert, P.J. 1988. G–proteins in the signal–transduction pathways of Dictyostelium discoideum. Dev. Genet. 9, 215–226.
  • Söderbom, F., Anjard, C., Iranfar, N., Fuller, D., and Loomis, W.F. 1999. An adenylyl cyclase that functions during late development of Dictyostelium. Development. 126, 5463–5471.
  • Soid-Raggi, L.G., and Meza, I. 1997. Partial characterization of G proteins and PLC as possible signal transduction elements during adhesion of Entamoeba histolytica to fibronectin. Arch. Med. Res. 28, 132–133.
  • Soid-Raggi, L.G., Torres-Marquez, M.E., and Meza, I. 1998. Entamoeba histolytica: identification of functional Gs and Gi proteins as possible signal transduction elements in the interaction of trophozoites with fibronectin. Exp. Parasitol. 90, 262–269.
  • Song, J., Chen, Z., Xu, P., Gingras, R., Ng, A., Leberer, E., Thomas, D. Y., and Ni, F. 2001. Molecular interactions of the Gbeta binding domain of the Ste20p/PAK family of protein kinases. An isolated but fully functional Gbeta binding domain from Ste20p is only partially folded as shown by heteronuclear NMR spectroscopy. J. Biol. Chem. 276, 41205–41212.
  • Sugimoto, K., Nukada, T., Tanabe, T., Takahashi, H., Noda, M., Minamino, N., Kangawa, K., Matsuo, H., Hirose, T., and Inayama, S. 1985. Primary structure of the beta–subunit of bovine transducin deduced from the cDNA sequence. FEBS Lett. 191, 235–240.
  • Sun, B., and Firtel, R.A. 2003. A Regulator of G protein signaling–containing kinase is important for chemotaxis and multicellular development in Dictyostelium. Mol. Biol. Cell. 14, 1727–1743.
  • Sutherland, E.W., and Rall, T.W. 1958. Fractionation and characterization of a cyclic adenine ribonucleotide formed by tissue particles. J. Biol. Chem. 232, 1077–1091.
  • Sweet, M.T., and Allis, C.D. 1993. Phosphorylation of linker histones by cAMP-dependent protein kinase in mitotic micronuclei of Tetrahymena. Chromosoma. 102, 637–647.
  • Sweet, M.T., Carlson, G., Cook, R.G., Nelson, D., and Allis, C.D. 1997. Phosphorylation of linker histones by a protein kinase A-like activity in mitotic nuclei. J. Biol. Chem. 272, 916–223.
  • Tamaki, H., Miwa, T., Shinozaki, M., Saito, M., Yun, C.W., Yamamoto, K., and Kumagai, H. 2000. GPR1 regulates filamentous growth through FLO11 in yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 267, 164–168.
  • Tamura, N., Chrisman, T.D., and Garbers, D.L. 2001. The regulation and physiological roles of the guanylyl cyclase receptors. Endocr J. 48, 611–634.
  • Tan, M., Heckmann, K., and Brunen-Nieweler, C. 2001. Analysis of micronuclear, macronuclear and cDNA sequences encoding the regulatory subunit of cAMP–dependent protein kinase of Euplotes octocarinatus: evidence for a ribosomal frameshift. J. Eukaryot. Microbiol. 48, 80–87.
  • Tang, W.J., and Gilman, A.G. 1992. Adenylyl cyclases. Cell. 70, 869–872.
  • Tang, W. J., Hurley, J. H. 1998. Catalytic mechanism and regulation of mammalian adenylyl cyclases. Mol. Pharmacol. 54, 231–240.
  • Taylor, M.C., Muhia, D.K., Baker, D.A., Mondragon, A., Schaap, P.B., and Kelly, J.M. 1999. Trypanosoma cruzi adenylyl cyclase is encoded by a complex multigene family. Mol. Biochem. Parasitol. 104, 205–217.
  • Theibert, A., and Devreotes, P.N. 1986. Surface receptor-mediated activation of adenylate cyclase in Dictyostelium. Regulation by guanine nucleotides in wild-type cells and aggregation deficient mutants. J. Biol. Chem. 261, 15121–15 125.
  • Thevelein, J.M., and de Winde, J.H. 1999. Novel sensing mechanisms and targets for the cAMP–protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 33, 904–918.
  • Toda, T., Cameron, S., Sass, P., Zoller, M., and Wigler, M. 1987. Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase. Cell. 50, 277–287.
  • Tolkacheva, T., McNamara, P., Piekarz, E., and Courchesne, W. 1994. Cloning of a Cryptococcus neoformans gene, GPA1, encoding a G-protein alpha-subunit homolog. Infect. Immun. 62, 2849–2856.
  • Traynor, D., Kessin, R.H., and Williams, J.G. 1992. Chemotactic sorting to cAMP in the multicellular stages of Dictyostelium development. Proc. Natl. Acad. Sci. 89, 8303–8307.
  • Ullmann, A. 1985. Catabolite repression. Biochimie. 67, 29–34.
  • Ullmann, A. 1996. Catabolite repression: a story without end. Res. Microbiol. 147, 455–458.
  • Umeki, S., and Nozawa, Y. 1996. Adenylate and guanylate cyclases in Tetrahymena. Prog. Mol. Subcell. Biol. 17, 40–60.
  • Van Es, S., Virdy, K.J., Pitt, G.S., Meima, M., Sands, T.W., Devreotes, P.N., Cotter, D.A., and Schaap, P. 1996. Adenylyl cyclase G, an osmosensor controlling germination of Dictyostelium spores. J. Biol. Chem. 271, 23623–23625.
  • Van Es, S., and Devreotes, P.N. 1999. Molecular basis of localized responses during chemotaxis in amoebae and leukocytes. Cell Mol. Life Sci. 55, 1341–1351.
  • Van Houten, J.L., Yang, W.Q., Bergeron, A. 2000. Chemosensory signal transduction in Paramecium. J. Nutr. 130, 946S–949S.
  • Veron, M., Mutzel, R., Lacombe, M.L., Simon, M.N., and Wallet, V. 1988. cAMP-dependent protein kinase from Dictyostelium discoideum. Dev. Genet. 9, 247–528.
  • Veron, M., Radzio-Andzelm, E., Tsigelny, I., Ten Eyck, L.F., and Taylor, S.S. 1993. A conserved helix motif complements the protein kinase core. Proc. Natl Acad. Sci. 90, 10618–10622.
  • Versele, M., Lemaire, K., and Thevelein, J.M. 2001. Sex and sugar in yeast: two distinct GPCR systems. EMBO Rep. 2, 574–579.
  • Wang, B., and Kuspa, A. 1997. Dictyostelium development in the absence of cAMP. Science. 277, 251–254.
  • Watkins, D.C., Northup, J.K., and Malbon, C.C. 1987. Regulation of G-proteins in differentiation. Altered ratio of alpha- to beta-subunits in 3T3-L1 cells. J. Biol. Chem. 62, 10651–10657.
  • Welton, R.M., and Hoffman, C.S. 2000. Glucose monitoring in fission yeast via the Gpa2 galpha, the git5 Gbeta and the git3 putative glucose receptor. Genetics. 156, 513–521.
  • Whiteway, M., Hougan, L., Dignard, D., Thomas, D.Y., Bell, L., Saari, G.C., Grant, F.J., O’Hara, P., and MacKay, V.L. 1989. The STE4 and STE18 genes of yeast encode potential beta and gamma subunits of the mating factor receptor–coupled G protein. Cell. 56, 467–477.
  • Wilkie, T.M., and Yokoyama, S. 1994. Evolution of the G protein alpha subunit multigene family. Soc. Gen. Physiol. 49, 249–270.
  • Wu, L., Valkema, R., Van Haastert, P.J., and Devreotes, P.N. 1995. The G protein beta subunit is essential for multiple responses to chemoattractants in Dictyostelium. J. Cell Biol. 129, 1667–1675.
  • Wu, M., Allis, C.D., Sweet, M.T., Cook, R.G., Thatcher, T.H., and Gorovsky, M.A. 1994. Four distinct and unusual linker proteins in a mitotically dividing nucleus are derived from a 71-kilodalton polyprotein, lack p34cdc2 sites, and contain protein kinase A sites. Mol. Cell Biol. 14, 10–20.
  • Xue, Y., Batlle, M., and Hirsch, J.P. 1998. GPR1 encodes a putative G protein–coupled receptor that associates with the Gpa2p Galpha subunit and functions in a Ras–independent pathway. EMBO J. 17, 1996–2007.
  • Yoshida, M., Sendai, Y., Sakuragi, N., and Hotta, Y. 2000. Analysis of a modB mutant in Dictyostelium discoideum using mRNA differential display. Plant Cell Physiol. 41, 239–243.
  • Yun, C.W., Tamaki, H., Nakayama, R., Yamamoto, K., and Kumagai, H. 1997. G–protein coupled receptor from yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 240, 287–292.
  • Yun, C.W., Tamaki, H., Nakayama, R., Yamamoto, K., and Kumagai, H. 1998. Gpr1p, a putative G–protein coupled receptor, regulates glucose-dependent cellular cAMP level in yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 252, 29–33.
  • Zhang, N., Long, Y., and Devreotes, P.N. 2001. Ggamma in Dictyostelium: its role in localization of gbetagamma to the membrane is required for chemotaxis in shallow gradients. Mol. Biol. Cell. 12, 3204–3213

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.