Journal of Biosciences

, Volume 20, Issue 3, pp 289–310 | Cite as

Calcium, cyclic GMP and the control of myosin II during chemotactic signal transduction ofDictyostelium

  • Peter C. Newell
Article
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Revised:

Abstract

Evidence is presented for Ca2+ and cyclic GMP being involved in signal transduction between the cell surface cyclic AMP receptors and cytoskeletal myosin II involved in chemotactic cell movement. Ca2+ is shown to be required for chemotactic aggregation of amoebae. The evidence for uptake and/or eflux of this ion being regulated by the nucleotide cyclic GMP is discussed. The connection between Ca2+, cyclic GMP and chemotactic cell movement has been explored using “streamer F” mutants. The primary defect in these mutants is in the structural gene for the cyclic GMP-specific phosphodiesterase which results in the mutants producing an abnormally prolonged peak of accumulation of cyclic GMP in response to stimulation with the chernoattractant cyclic AMP. While events associated with production and relay of cyclic AMP signals are normal, certain events associated with movement are (like the cyclic GMP response) abnormally prolonged in the mutants. These events include Ca2+ uptake, myosin II association with the cytoskeleton and inhibition of myosin heavy and light chain phosphorylation. These changes can be correlated with the amoebae becoming elongated and transiently decreasing their locomotive speed after chemotactic stimulation. Other mutants studied in which the accumulation of cyclic GMP in response to cyclic AMP stimulation was absent produced no myosin II responses.

Models are described in which cyclic GMP (directly or indirectly via Ca2+) regulates accumulation of myosin II on the cytoskeleton by inhibiting phosphorylation of the myosin heavy and light chain kinases.

Keywords

Myosin II cyclic GMP calcium myosin heavy chain kinase myosin light chain kinase 
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References

  1. Berlot C H. Spudich J A and Devreotes P N 1985 Chemoattractant-elicited increases in myosin phosphorylation inDictyvstelium;Cell 43 307–314PubMedCrossRefGoogle Scholar
  2. Berlot C H, Devreotes P N and Spudich J A 1987 Chemoattractant elicited increases inDictyostelium myosin phosphorylation are due to changes in myosin localization and increases in kinase activity;J. Biol. Chem. 262 3918–3926PubMedGoogle Scholar
  3. Bohme R, Bumann J, Aeckerlc S and Malchow D 1987 A high-affinity plasma membrane CA2+-ATPase inDictyostelium Discoideum: its relation to cAMP-induced Ca2+ fluxes;Biochim. Biuphys. Acta 904 125–130CrossRefGoogle Scholar
  4. Bominaar A A, Kesbeke F, Snaarjagalska B E, Peters D J M, Schaap P and Vanhaaslert P J M 1991 Aberrant chemotaxis and differentiation inDictyostetium: Mutant fgdC with a defective regulation of receptor-stimulated phosphoinositidase-C;J. Cell Sci. 100 825–831PubMedGoogle Scholar
  5. Bumann J. Wurster B and Malchow D 1984 Attractant-induced changes and oscillations of the extracellular Ca2+ concentration in suspensions of differentiatingDictyosteliitm cells;J. Cell Biol. 98 173–178PubMedCrossRefGoogle Scholar
  6. Condeelis J, Hall A, Bresnick A, Warren V, Hock R, Bennet H and Ogihara S 1988 Actin polymerization and pseudopod extension during amoeboid chemotaxis;Cell Motility Cytoskeleton 10 77–90CrossRefGoogle Scholar
  7. Côté G P and McCrea S M 1987 Selective removal of the carboxyl-terminal tail end of theDictyosteliym myosin II heavy chain by chymotrypsin;J. Biol. Chem. 262 13033–13038PubMedGoogle Scholar
  8. Coukell M B and Cameron A M 1986 Characterization of revertants of stmF mutants ofDictyostelium discoideum: evidence that stmF is the structural gene of the cGMP-specific phosphodiesterase;Dev. Genet. 6 163–177PubMedCrossRefGoogle Scholar
  9. Cunningham K W and Fink G R 1994 Calcineurin-dependent growth control inSaccharomyces cerevisiae mutants lackingPMCl a homolog of plasma membrane Ca2+ ATPases;J. Cell Biol. 124 351–363PubMedCrossRefGoogle Scholar
  10. De Lozanne A and Spudich J A 1987 Disruption of theDictyostelium myosin heavy chain gene by homologous recombination;Science 236 1086–1091PubMedCrossRefGoogle Scholar
  11. Devreotes P N 1983 Cyclic nucleotides and cell-cell communication inDictyostelium discoideum, inAdvances in cyclic nucleotide research (eds) P Greengard and G A Robison (New York: Raven Press) Vol. 15, pp 55–96Google Scholar
  12. Egelhoff T T, Lee R J and Spudich J A 1993Dictystelium myosin heavy chain phosphorylation sites regulate myosin filament assembly and localization in vivo;Cell 75 363–371PubMedCrossRefGoogle Scholar
  13. Europe-Finner G N and Newell P C 1984 Inhibition of aggregation inDictyostelium by EGTA-induced depletion of calcium;FEMS Microbiol. Lett,21 21–25PubMedCrossRefGoogle Scholar
  14. Europe-Finner G N and Newell P C 1985 Inositol (l,4,5)trisphosphate induces cyclic GMP formation inDictyostelium discoideum;Biochem. Biophys. Res. Ctimmun. 130 1115–1122CrossRefGoogle Scholar
  15. Europe-Finner G N and Newell P C 1986 Inositol (1.4,5)trisphosphate induces calcium release from a non-mitochondrial pool in amoebae ofDictyostelium;Biochim. Biophys. Acta 887 335–340PubMedCrossRefGoogle Scholar
  16. Flaadt H, Jaworski E and Molchow D 1993a Evidence for two intracellular calcium pools inDictyostelium; the cAMP-induced calcium influx is directed into a NBD-Cl- and 25-ditert-bulyl-14-hydroquinone-sensitive pool;J. Cell Sci. 105 1131–1135PubMedGoogle Scholar
  17. Flaadt H, Jaworski E, Schlatterer C and Malchow D 1993b Cyclic AMP- and Ins 145 P3-induced Ca2+ fluxes in permeabilised cells ofDictyostelium discuideum: cGMP regulates Ca2+ entry across the plasma membrane;J. Cell Sci. 105 255–261Google Scholar
  18. Foskett J K and Wong D 1992 Calcium oscillations in parotid acinar cells induced by microsomal Ca2+-ATPase inhibitors;Am. J. Physiol. 262 656–663Google Scholar
  19. Franke J and Kessin R H 1992 The cyclic nucleotide phosphodiesterase ofDictyostelium discoideum: molecular genetics and biochemistry;Cellular Signalling 4 471–478PubMedCrossRefGoogle Scholar
  20. Gerisch G, Malchow D, Huesgen A, Nanjundiah V, Roos W and Wick U 1975 Cyclic AMP reception and cell recognition inDictyostctium discoideum: inDevelopmental Biology ICN-UCLA Symposia on Molecular and Cellular Biology (eds) II McMahon and C F Fox (New York: W A Benjamin) Vol. 2, pp 76–88Google Scholar
  21. Gerisch G. Albrecht R. De Hostos E, Wallraff E, Heizer C, Kreitmeier M and Müller-Taubenberger A 1993 Act in-associated proteins in motility and chemotaxis ofDictyostelium cells; inCell behaviour: Adhesion and motility (eds) G Jones. C Wigley and R Warn (SEB Symposium) vol. 47, pp 297–315Google Scholar
  22. Griffith L M, Downs S M and Spudich J A 1987 Myosin light chain kinase and myosin light chain phosphatase fromDictyostelium: Effects of reversible phosphorylation on myosin structure and function;J. Cell Biol. 104 1309–1323PubMedCrossRefGoogle Scholar
  23. Janssens P M W and Van Haastert P J M 1987 Molecular basis of transmembrane signal transduction inDictyostelium discoideum;Microbiol. Rev. 51 396–418PubMedGoogle Scholar
  24. Janssens P M W and De Jong C C C 1988 A magnesium-dependent guanylate cyclase in cell free preparations ofDictyostelium discoideum;Biochem. Biophys. Res. Commun. 150 405–411PubMedCrossRefGoogle Scholar
  25. Jay P Y, Pham P A, Wong S C and Elson E L 1995 A mechanical function of myosin II in cell motility;J. Cell Sci. 108 387–393PubMedGoogle Scholar
  26. Kessin R H 1988 Genetics of earlyDictyostelium discoideum development;Mycrobiol. Rev. 52 29–49Google Scholar
  27. Knecht D A and Loomis W F 1987 Antisense RNA inactivation of myosin heavy chain gene expressionin Dictyostelium discoideum;Science 236 1081–1085PubMedCrossRefGoogle Scholar
  28. Knecht D A and Loomis W F 1988 Developmental consequences of the lack of myosin heavy chain inDictyostelium discoideum;Dev. Biol. 128 178–184PubMedCrossRefGoogle Scholar
  29. Kuczmarski E R, Tafuri S R and Parysek L M 1987 Effect of heavy chain phosphorylation on the polymerization and structure ofDictyostelium myosin filaments;J. Cell Biol. 105 2989–2997PubMedCrossRefGoogle Scholar
  30. Kuczmarski E R and Spudich J A 1980 Regulation of myosin self-assembly: Phosphorylation ofDictyostelium heavy chain inhibits formation of thick filaments;Proc. Natl. Acad. Sci. USA 77 7292–7296PubMedCrossRefGoogle Scholar
  31. Liu G and Newell P C 1988 Evidence that cyclic GMP regulates myosin interaction with the cytoskeleton during chemotaxis ofDictyostelium;J. Cell Sci. 90 123–129PubMedGoogle Scholar
  32. Liu G and Newell PC 1991 Evidence that cyclic GMP may regulate the association of Myosin-II heavy chain with the cytoskeleton by inhibiting its phosphorylation;J. Cell Sci. 98 483–490PubMedGoogle Scholar
  33. Liu G and Newell P C 1993 Role of cyclic GMP in signal transduction to cytoskeletal myosin; inCell behaviour. Adhesion and motility (eds) G Jones, C Wigley and R Warn (SEB Symposium) vol. 47, pp 283–295Google Scholar
  34. Liu G and Newell P C 1994 Regulation of myosin regulatory light chain phosphorylation via cyclic GMP during chemotaxis ofDictyostelium;J. Cell Sci. 107 1737–1743PubMedGoogle Scholar
  35. Luck-Vielmetter D, Schleicher M, Grabatin B, Wippler J and Gerisch G 1990 Replacement of threonines residues by serine and alanine in a phosphorylatable heavy chain fragment ofDictyostelium myosin II;FEBS Lett. 269 239–243PubMedCrossRefGoogle Scholar
  36. Malchow D, Bohme R and Rahmsdorf H J 1981 Regulation of phosphorylation of myosin heavy chain during the chemotactic response ofDictyostelium cells;Eur. J. Biochem. 117 213–218PubMedCrossRefGoogle Scholar
  37. Malchow D, Bohme R and Gras U 1982 On the role of calcium in chemotaxis and oscillations ofDictyostelium cells;Biophys. Struct. Mech. 9 131–136PubMedCrossRefGoogle Scholar
  38. Manstein D J, Titus M A, De Lozanne A and Spudich J A 1989 Gene replacement inDictyostelium: generation of myosin null mutants;EMBO J. 8 923–932PubMedGoogle Scholar
  39. Maruta H, Baltes W, Dieter P, Marme D and Gerisch G 1983 Myosin heavy chain kinase inactivated by Ca2+/calmodulin from aggregating cells ofDictyostelium discoideum;EMBO J. 2 535–542PubMedGoogle Scholar
  40. Mason J, Rasmussen W H and Dibella F 1971 3′∶5′ AMP and Ca2+ in slime mold aggregation;Exp. Cell Res. 67 156–160PubMedCrossRefGoogle Scholar
  41. Mato J M, Krens F A, Van Haastert P J M and Konijn T M 1977 3′∶5′-Cyclic AMP-dependent 3′:5′-cyclic GMP accumulation inDictyostelium discoideum;Proc. Natl. Acad. Sci. USA 74 2348–2351PubMedCrossRefGoogle Scholar
  42. McRobbie S J and Newell P C 1983 Changes in actin associated with cytoskeleton following chemotactic stimulation ofDictyostelium discoideum;Biochem. Biophys. Res. Commun. 115 351–359PubMedCrossRefGoogle Scholar
  43. McRobbie S J and Newell P C 1984a Chemoattractant-mediated changes in cytoskeletal actin of cellular slime moulds;J. Cell Sci. 68 139–151PubMedGoogle Scholar
  44. McRobbie S J and Newell P C 1984b A new model for chemotactic signal transduction inDictyostelium discoideum;Biochem. Biophys. Res. Commun. 123 1076–1083PubMedCrossRefGoogle Scholar
  45. McRobbie S J and Newell P C 1985 Effect of cytochalasin B on cell movements and chemoattractant elicited actin changes inDictyostelium;Exp. Cell Res. 160 275–286PubMedCrossRefGoogle Scholar
  46. Menz S, Bumann J, Jaworski E and Malchow D 1991 Mutant analysis suggests that cyclic GMP mediates the cyclic AMP-induced Ca2+ uptake inDictyostelium;J. Cell Sci. 99 187–191PubMedGoogle Scholar
  47. Milne J L and Coukell M B 1989 Identification of a high-affinity Ca2+ pump associated with endocytic vesicles inDictyostelium discoideum;Exp. Cell Res. 185 21–32PubMedCrossRefGoogle Scholar
  48. Milne J L and Coukell M B 1991 A Ca2+ transport system associated with the plasma membrane ofDictyostelium discoideum in activated by different chemoattractant receptors;J. Cell Biol. 112 103–110PubMedCrossRefGoogle Scholar
  49. Nanjundiah V 1985 The evolution of communication and social behaviour inDictyostelium discoideum;Proc. Indian Acad. Sci. (Anim. Sci.) 94 639–653CrossRefGoogle Scholar
  50. Newell P C 1986a The role of actin polymerization in amoebal chemotaxis;Bioessays 5 208–211CrossRefGoogle Scholar
  51. Newell P C 1986b Receptors for cell. communication inDictyostelium; inHormones, receptors and cellular interaction in plants (eds) C M Chadwick and D R Garrod (Cambridge: Cambridge Univ. Press) pp 154–216Google Scholar
  52. Newell P C, Europe-Finner G N and Small N V 1987 Signal transduction during amoebal chemotaxis ofDictyostelium discoideum;Microbiological Sci. 4 5–11Google Scholar
  53. Newell P C, Europe-Finner G N, Small N V and Liu G 1988 Inositol phosphates, G-proteins andras genes involved in chemotactic signal transduction ofDictyostelium;J. Cell Sci. 89 123–127PubMedGoogle Scholar
  54. Newell P C and Liu G 1992 Streamer F mutants and chemotaxis ofDictyostelium;Bipessays 14 473–479CrossRefGoogle Scholar
  55. Nishikawa M, de Lanerolle P, Lincoln T M and Adelstein R S 1984 Phosphorylation of mammalian myosin light chain kinases by the catalytic subunit of cyclic AMP-dependent protein kinase and by cyclic GMP-dependent protein kinase;J. Biol. Chem. 259 8429–8436PubMedGoogle Scholar
  56. Nishikawa M, Shirakawa S and Adelstein R S 1985 Phosphorylation of smooth muscle light chain kinase by protein kinase C;J. Biol. Chem. 260 8978–8983PubMedGoogle Scholar
  57. Padh H and Brenner M 1984 Studies of the guanylate cyclase of the social amoebaDictyostelium discoideum;Arch. Biochem. Biophys. 229 73–80PubMedCrossRefGoogle Scholar
  58. Padh H, Lavasa M and Steck T L 1989 Characterization of a vacuolar proton ATPase inDictyostelium discoideum;Biochem. Biophys. Acta 982 271–278PubMedCrossRefGoogle Scholar
  59. Pasternak C, Flicker P F, Ravid S and Spudich J A 1989 Intermolecular versus intramolecular interactions ofDictyostelium myosin: Possible regulation by heavy chain phosphorylation;J. Cell Biol. 109 203–210PubMedCrossRefGoogle Scholar
  60. Pederson P L and Carafoli E 1987 Ion motive ATPase I. Ubiquity properties and significance to cell function;Trends Biochem. Sci. 12 146–150CrossRefGoogle Scholar
  61. Ravid S and Spudich J A 1989 Myosin heavy chain kinase from developedDictyostelium cells. Purification and characterization;J. Biol. Chem. 264 15144–15150PubMedGoogle Scholar
  62. Ravid S and Spudich J A 1992 Membrane-boundDictyostelium myosin heavy chain kinase: A developmentally regulated substrate-specific member of the protein kinase C family;Proc. Natl. Acad. Sci. USA 89 5877–5881PubMedCrossRefGoogle Scholar
  63. Rooney E K and Gross J D 1992 ATP-driven Ca2+/H+ antiport in acid vesicles fromDictyostelium;Proc. Natl. Acad. Sci. USA 89 8025–8029PubMedCrossRefGoogle Scholar
  64. Rooney E K, Gross J D and Satre M 1994 Characterization of an intracellular Ca2+ pump inDictyostelium;Cell Calcium 16 509–522PubMedCrossRefGoogle Scholar
  65. Ross F M and Newell P C 1979 Genetics of aggregation pattern mutations in the cellular slime mouldDictyostelium discoideum;J. Gen. Microbiol. 115 289–300PubMedGoogle Scholar
  66. Ross F M and Newell P C 1981 Streamers: Chemotactic mutants ofDictyostelium discoideum with altered cyclic GMP metabolism;J. Gen. Microbiol. 127 339–350PubMedGoogle Scholar
  67. Saito M 1979 Effect of extracellular Ca2+ on the morphogenesis ofDictyostelium discoideum;Exp. Cell Res. 123 79–86PubMedCrossRefGoogle Scholar
  68. Schlatterer C and Malchow D 1993 Intracellular guanosine 5′-O-3-thiotriphosphate blocks chemotactic motility ofDictyostelium discoideum amoebae;Cell Motil. Cytoskel. 25 298–307CrossRefGoogle Scholar
  69. Segall J E 1992 Behavioral responses of streamer F mutants ofDictyostelium discoideum—Effects of cyclic GMP on cell motility;J. Cell Sci. 101 589–597PubMedGoogle Scholar
  70. Shelden E and Knecht D A 1995 Mutants lacking myosin II cannot resist forces generated during multicellular morphogenesis;J. Cell Sci. 108 1105–1115PubMedGoogle Scholar
  71. Small N V, Europe-Finner G N and Newell P C 1986 Calcium induces cyclic GMP formation inDictyostelium;FEBS Lett. 203 11–14PubMedCrossRefGoogle Scholar
  72. Tan J L and Spudich J A 1990Dictyostelium myosin light chain kinase: Purification and characterization;J. Biol. Chem. 265 13818–13824PubMedGoogle Scholar
  73. Tan J L and Spudich J A 1991 Characterization and bacterial expression of theDictyostelium myosin light chain kinase cDNA: Identification of an autoinhibitory domain;J. Biol. Chem. 266 16044–16049PubMedGoogle Scholar
  74. Unterweger N and Schlatterer C 1994 Introduction of calcium buffers into the cytosol ofDictyostelium discoideum amoebae alters cell morphology and inhibits chemotaxis;Cell Calcium (in press)Google Scholar
  75. Van Duijn B and Van Haastert P J M 1992 Independent control of locomotion and orientation duringDictyostelium discoideum chemotaxis;J. Cell Sci. 102 763–768PubMedGoogle Scholar
  76. Van Haastert P J M and Konijn T M 1982 Signal transduction in the cellular slime molds;Mol. Cell. Endocrinol. 26 1–17PubMedCrossRefGoogle Scholar
  77. Van Haastert P J M, Van Lookeren Campagne M M and Kesbeke F 1983 Multiple degradation pathways of chemoattractant mediated cyclic GMP accumulation inDictyostelium;Biochim. Biophys. Acta 756 67–71Google Scholar
  78. Wanner R and Wurster B 1990 Cyclic GMP-activated protein kinase fromDictyostelium; discoideum;Biochim. Biophys. Acta 1053 179–184PubMedCrossRefGoogle Scholar
  79. Wessels D, Soll D R, Knecht D, Loomis W F, De Lozanne A and Spudich J 1988 Cell motility and chemotaxis inDictyostelium amoebae lacking myosin heavy hain;Dev. Biol. 128 164–177PubMedCrossRefGoogle Scholar
  80. Wurster B, Schubiger K, Wick U and Gerisch G 1977 Cyclic GMP inDictyostelium discoideum; Oscillations and pulses in response to folic acid and cyclic AMP signals;FEBS Lett. 76 141–144PubMedCrossRefGoogle Scholar
  81. Yumura S and Kitanishi-Yumura T 1992 Release of myosin from the membrane-cytoskeleton ofDictyostelium discoideum mediated by heavy-chain phosphorylation at foci within the cortical actin network;J. Cell Biol. 117 1231–1239PubMedCrossRefGoogle Scholar
  82. Yumura S and Kitanishi-Yumura T 1993 A mechanism for the intracellular localization of myosin II filaments in theDictyostelium amoeba;J. Cell Sci. 105 233–242Google Scholar
  83. Zhu Q, Liu T and Clarke M 1993 Calmodulin and the contractile vacuole complex in mitotic cells ofDictyostelium discoideum;J. Cell Sci. 104 1119–1127PubMedGoogle Scholar

Copyright information

© Indian Academy of Sciences 1995

Authors and Affiliations

  • Peter C. Newell
    • 1
  1. 1.Department of BiochemistryUniversity of OxfordOxfordUK

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