Identification of the C-signal, a contact-dependent morphogen coordinating multiple developmental responses in Myxococcus xanthus

Genes and Development

Volumn 17, Issue 17, 2003, Pages 2151-2161

  Lobedanz, Sune ^a   Søgaard Andersen, Lotte ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Development; Extracellular signaling; Morphogen; Protein secretion; Proteolysis

Indexed keywords

ALCOHOL DEHYDROGENASE; C SIGNAL MORPHOGEN; MORPHOGEN; NICOTINAMIDE ADENINE DINUCLEOTIDE; PROTEIN P17; PROTEIN P25; RECOMBINANT PROTEIN; SERINE PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CSGA GENE; DEVELOPMENTAL BIOLOGY; GENE; MOLECULAR BIOLOGY; MORPHOGENESIS; MYXOCOCCUS XANTHUS; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SECRETION; PROTEIN SYNTHESIS; TEMPORAL CORTEX;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; MYXOCOCCUS XANTHUS; NAD;

BACTERIA (MICROORGANISMS); EUKARYOTA; MYXOCOCCUS XANTHUS; NEGIBACTERIA;

EID: 0041820264     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.274203     Document Type: Article

References (62)

1. Aza-Blanc, P., Ramirezweber, F., Laget, M., Schwartz, C., and Kornberg, T. 1997. Proteolysis that is inhibited by Hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell 89: 1043-1053.
2. Baker, M.E. 1994. Myxococcus xanthus C-factor, a morphogenetic paracrine signal, is similar to Escherichia coli 3-oxoacyl-[acyl-carrier-protein] reductase and human 17 β-hydroxysteroid dehydrogenase. Biochem. J. 301: 311-312.
3. Bowden, M.G. and Kaplan, H.B. 1998. The Myxococcus xanthus lipopolysaccharide O-antigen is required for social motility and multicellular development. Mol. Microbiol. 30: 275-284.
4. Brusca, J.S. and Radolf, J.D. 1994. Isolation of integral membrane proteins by phase partitioning with Triton X-114. Methods Enzymol. 228:182-193.
5. Carugo, O. and Argos, P. 1997a. NADP-dependent enzymes. I: Conserved stereochemistry of cofactor binding. Proteins 28: 10-28.
6. -. 1997b. NADP-dependent enzymes. II: Evolution of the mono- and dinucleotide binding domains. Proteins 28: 29-40.
7. Crawford, E.W. and Shimkets, L.J. 2000. The stringent response in Myxococcus xanthus is regulated by SocE and the CgsA C-signaling protein. Genes & Dev. 14: 483-492.
8. Dworkin, M. 1996. Recent advances in the social and developmental biology of the Myxobacteria. Microbiol. Rev. 60: 701-02.
9. Ellehauge, E., Nørregaard-Madsen, M., and Søgaard-Andersen, M. 1998. The FruA signal transduction protein provides a checkpoint for the temporal coordination of intercellular signals in Myxococcus xanthus development. Mol. Microbiol. 30: 807-817.
10. Fuqua, C. and Greenberg, E.P. 2002. Listening in on bacteria: Acyl-homoserine lactone signalling. Nat. Rev. Mol. Cell Biol. 3: 685-695.
11. Gill, R.E., Karlok, M., and Benton, D. 1993. Myxococcus xanthus encodes an ATP-dependent protease which is required for developmental gene transcription and intercellular signaling. J. Bacteriol. 175: 4538-4544.
12. Gronewold, T.M.A. and Kaiser, D. 2001. The act operon controls the level and time of C-signal production for Myxococcus xanthus development. Mol. Microbiol. 40: 744-756.
13. Guex, N. and Peitsch, M.C. 1997. SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling. Electrophoresis 18: 2714-2723.
14. Hodgkin, J. and Kaiser, D. 1977. Cell-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc. Natl. Acad. Sci. 74: 2938-2942.
15. Horer, S., Stoop, J., Mooibroek, H., Baumann, U., and Sassoon, J. 2001. The crystallographic structure of the mannitol 2-dehydrogenase NADP+ binary complex from Agaricus bisporus. J. Biol. Chem. 276: 27555-27561.
16. Ingham, P.A. and McMahon, A.P. 2001. Hedgehog signaling in animal development: Paradigms and principles. Genes & Dev. 15: 3059-3087.
17. Inouye, M., Inouye, S., and Zusman, D.R. 1979. Gene expression during development of Myxococcus xanthus: Pattern of protein synthesis. Dev. Biol. 68:579-591.
18. Kaiser, D. 1979. Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc. Natl. Acad. Sci. 76: 5952-5956.
19. Kashefi, K. and Hartzell, P.L. 1995. Genetic suppression and phenotypic masking of a Myxococcus xanthus frzF defect. Mol. Microbiol. 15: 483-494.
20. Kim, S.K. and Kaiser, D. 1990a. C-factor: A cell-cell signaling protein required for fruiting body morphogenesis of M. xanthus. Cell 61: 19-26.
21. -. 1990b. Purification and properties of Myxococcus xanthus C-factor, an intercellular signaling protein. Proc. Natl. Acad. Sci. 87: 3635-3639.
22. -. 1991. C-factor has distinct aggregation and sporulation thresholds during Myxococcus development. J. Bacteriol. 173: 1722-1728.
23. Koradi, R., Billeter, M., and Wuthrich, K. 1996. MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graph. 14:51-55.
24. Kramer, H., Cagan, R.L., and Zipursky, S.L. 1991. Interaction of bride of sevenless membrane-bound ligand and the sevenless tyrosine-kinase receptor. Nature 352: 207-212.
25. Kroos, L. and Kaiser, D. 1987. Expression of many developmentally regulated genes in Myxococcus depends on a sequence of cell interactions. Genes & Dev. 1: 840-854.
26. Kroos, L., Kuspa, A., and Kaiser, D. 1986. A global analysis of developmentally regulated genes in Myxococcus xanthus. Dev. Biol. 117: 252-266.
27. -. 1990. Defects in fruiting body development caused by Tn5 lac insertions in Myxococcus xanthus. J. Bacteriol. 172: 484-487.
28. Kruse, T., Lobedanz, L., Berthelsen, N.M.S., and Søgaard-Andersen, L. 2001. C-signal: A cell surface-associated morphogen that induces and coordinates multicellular fruiting body morphogenesis and sporulation in M. xanthus. Mol. Microbiol. 40: 156-168.
29. Lazazzera, B.A. and Grossman, A.D. 1998. The ins and outs of peptide signaling. TIM 6: 288-294.
30. Lee, B.-U., Lee, K., Mendez, J., and Shimkets, L.J. 1995. A tactile sensory system of Myxococcus xanthus involves an extracellular NAD(P)+-containing protein. Genes & Dev. 9: 2964-2973.
31. Lee, K. and Shimkets, L.J. 1994. Cloning and characterization of the socA locus which restores development to Myxococcus xanthus C-signaling mutants. J. Bacteriol. 176: 2200-2209.
32. -. 1996. Suppression of a signaling defect during Myxococcus xanthus development. J. Bacteriol. 178: 977-984.
33. Li, S., Lee, B.-U., and Shimkets, L.J. 1992. csgA expression entrains Myxococcus xanthus development. Genes & Dev. 6: 401-410.
34. Lindahl, E., Hess, B., and van der Spoel, D. 2001. GROMACS 3.0: A package for molecular simulation and trajectory analysis. J. Mol. Mod. 7: 306-317.
35. McBride, M.J., Köhler, T., and Zusman, D.R. 1992. Methylation of FrzCD, a methyl-accepting taxis protein of Myxococcus xanthus, is correlated with factors affecting cell behaviour. J. Bacteriol. 174: 4246-4257.
36. McCleary, W.R., McBride, M.J., and Zusman, D.R. 1990. Developmental sensory transduction in Myxococcus xanthus involves methylation and demethylation of FrzCD. J. Bacteriol. 172: 4877-4887.
37. Mumm, J.S. and Kopan, R. 2000. Notch signaling: From the outside in. Dev. Biol. 228: 151-165.
38. Ogawa, M., Fujitani, S., Mao, X., Inouye, S., and Komano, T. 1996. FruA, a putative transcription factor essential for the development of Myxococus xanthus. Mol. Microbiol. 22: 757-767.
39. Oppermann, U., Filling, C., Hult, M., Shafqat, N., Wu, X., Lindh, M., Shafqat, J., Nordling, E., Kallberg, Y., Persson, B., et al. 2003. Short-chain dehydrogenases/reductases (SDR): The 2002 update. Chem. Biol. Interact. 143-144: 247-253.
40. Perego, M. and Brannigan, J.A. 2001. Pentapeptide regulation of aspartyl-phosphate phosphatases. Peptides 22: 1541-1547.
41. Plamann, L., Kuspa, A., and Kaiser, D. 1992. Proteins that rescue A-signal-defective mutants of Myxococcus xanthus. J. Bacteriol. 174: 3311-3318.
42. Pugsley, A.P. 1993. The complete general secretory pathway in Gram-negative bacteria. Microbiol. Rev. 57: 50-108.
43. Qi, H., Rand, M.D., Wu, X., Sestan, N., Wang, W., Rakic, P., Xu, T., and Artavanis-Tsakonas, S. 1999. Processing of the Notch ligand Delta by the metalloprotease Kusbanian. Science 283: 91-94.
44. Rodriguez, J.P. and Kaiser, D. 1997. Identification and localization of the Tg1 protein, which is required for Myxococcus xanthus social motility. J. Bacteriol. 179: 4372-4381.
45. Sambrook, J., Fritsch, E.F., and Maniatis, T. 1989. Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
46. Schägger, H. and von Jagow, G. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166: 368-379.
47. Shimkets, L.J. 1986. Role of cell cohesion in Myxococcus xanthus fruiting body formation. J. Bacteriol. 166: 842-848.
48. -. 1999. Intercellular signaling during fruiting-body development of Myxococcus xanthus. Annu. Rev. Microbiol. 53: 525-549.
49. Shimkets, L.J. and Rafiee, H. 1990. CsgA, an extracellular protein essential for Myxococcus xanthus development. J. Bacteriol. 172: 5299-5306.
50. Shimkets, L.J., Gill, R.E., and Kaiser, D. 1983. Developmental cell interactions in Myxococcus xanthus and the spoC locus. Proc. Natl. Acad. Sci. 80: 1406-1410.
51. Søgaard-Andersen, L. and Kaiser, D. 1996. C factor, a cell-surface-associated intercellular signaling protein, stimulates the Frz signal transduction system in Myxococcus xanthus. Proc. Natl. Acad. Sci. 93: 2675-2679.
52. Søgaard-Andersen, L., Slack, F., Kimsey, H., and Kaiser, D. 1996. Intercellular C-signaling in Myxococcus xanthus involves a branched signal transduction pathway. Genes & Dev. 10: 740-754.
53. Spratt, B.G., Hedge, P.J., te Heesen, S., Edelman, A., and Broome-Smith, J.K. 1986. Kanamycin-resistant vectors that are analogues of plasmids pUC8, pUC9, pEMBL8 and pEMBL9. Gene 41: 337-342.
54. Sprott, G.D., Koval, S.F., and Schmaitman, C.A. 1994. Cell fractionation. In Methods for general and molecular bacteriology (eds. P. Gerhardt, R.G.A. Murray, W.A. Wood, and N.R. Kreig) pp. 72-103. American Society for Microbiology Press, Washington DC.
55. Stragier, P. and Losick, R. 1996. Molecular genetics of sporulation in Bacillus subtilis. Annu. Rev. Genet. 30: 297-341.
56. Tanaka, N., Nonaka, T., Tanabe, T., Yishimoto, T., Tsuru, D., and Mitsui, Y. 1996. Crystal structures of the binary and ternary complexes of 7-α-hydroxysteroid dehydrogenase from Escherichia coli. Biochemistry 35: 7715-7730.
57. Teleman, A.A., Strigini, M., and Cohen, S.M. 2001. Shaping morphogen gradients. Cell 105: 559-562.
58. Thomasson, B., Link, J., Stassinopoulos, A.G., Burke, N., Plamann, L., and Hartzell, P.L. 2002. Mg1A, a small GTPase, interacts with a tyrosine kinase to control type IV pili-mediated motility and development of Myxococcus xanthus. Mol. Microbiol. 46: 1399-1413.
59. van Aalten, D.M., Bywater, R., Findlay, J.B., Hendlich, M., Hooft, R.W., and Vriend, G. 1996. PRODRG, a program for generating molecular topologies and unique molecular descriptors from coordinates of small molecules. J. Comput. Aid. Mol. Des. 10: 255-262.
60. Wu, S.S. and Kaiser, D. 1996. Markerless deletions of pil genes in Myxococcus xanthus generated by counterselection with the Bacillus subtilis sacB gene. J. Bacteriol. 178: 5817-5821.
61. Yen, M.-R., Tseng, Y.-H., Nguyen, E.H., Wu, L.-F., and Saier Jr., M.H. 2002. Sequence and phylogenetic analyses of the twin-arginine targeting (Tat) protein export system. Arch. Microbiol. 177: 441-450.
62. Yoon, H.-S. and Golden, J.W. 1998. Heterocyst pattern formation controlled by a diffusible peptide. Science 282: 935-938.