Characterization and role of p53 family members in the symbiont-induced morphogenesis of the Euprymna scolopes light organ

Biological Bulletin

Volumn 211, Issue 1, 2006, Pages 7-17

  Goodson, Michael S ^a   Crookes Goodson, Wendy J ^a,b   Kimbell, Jennifer R ^a,c   McFall Ngai, Margaret J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b AIR FORCE RESEARCH LABORATORY   (United States)

^c PACIFIC HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; APOPTOSIS; BACTERIUM; CEPHALOPOD; GENE EXPRESSION; HATCHING; HOST-SYMBIONT INTERACTION; IMMUNOASSAY; MORPHOGENESIS; POLYMERASE CHAIN REACTION; PROTEIN; RNA; SYMBIOSIS;

BACTERIA (MICROORGANISMS); CEPHALOPODA; EUPRYMNA SCOLOPES; VIBRIO FISCHERI;

EID: 33748328079     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.2307/4134573     Document Type: Article

References (65)

1. Aguinaldo, A. M., J. M. Turbeville, L. S. Linford, M. C. Rivera, J. R. Garey, R. A. Raff, and J. A. Lake. 1997. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387: 489-493.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
3. Ashcroft, M., and K. H. Vousden. 1999. Regulation of p53 stability. Oncogene 18: 7637-7643.
4. Boettcher, K. J., and E. G. Ruby. 1990. Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J. Bacteriol. 172: 3701-3706.
5. Boggs, K., and D. Reisman. 2006. Increased p53 transcription prior to DNA synthesis is regulated through a novel regulatory element within the p53 promoter. Oncogene 25:555-565. doi: 10.1038/sj. onc.1209076; published online: 12 September 2005.
6. Bonsing, B. A., W. E. Corver, M. C. Gorsira, M. van Vliet, P. S. Oud, C. J. Cornelisse, and G. J. Fleuren. 1997. Specificity of seven monoclonal antibodies against p53 evaluated with Western blotting, immunohistochemistry, confocal laser scanning microscopy, and flow cytometry. Cytometry 28: 11-24.
7. Bradford, M. M. 1976. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
8. Celli, J., P. Duijf, B. C. Hamel, M. Bamshad, B. Kramer, A. P. Smits, R. Newbury-Ecob, R. C. Hennekam, G. Van Buggenhout, A. van Haeringen, C. G. Woods, A. J. van Essen, R. de Waal, G. Vriend, D. A. Haber, A. Yang, F. McKeon, H.G. Brunner, and H. van Bokhoven. 1999. Heterozygous germline mutations in the p53 homolog p63 are the cause of EEC syndrome. Cell 99: 143-53.
9. Ciocan, C. M., and J. M. Rotchell. 2005. Conservation of cancer genes in the marine invertebrate Mytilus edulis. Environ. Sci. Technol. 39: 3029-3033.
10. Cox, R. L., R. E. Stephens, and C. L. Reinisch. 2003. p63/73 homologues in surf clam: novel signaling motifs and implications for control of expression. Gene 320: 49-58.
11. Derry, W. B., A. P. Putzke, and J. H. Rothman. 2001. Caenorhabditis elegans p53: role in apoptosis, meiosis, and stress resistance. Science 294: 591-595.
12. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11: 1475-1489.
13. Dobbelstein, M., S. Wienzek, C. Konig, and J. Roth. 1999. Inactivation of the p53-homologue p73 by the mdm2-oncoprotein. Oncogene 18: 2101-2106.
14. Doino, J. A., and M. J. McFall-Ngai. 1995. A transient exposure to symbiosis-competent bacteria induces light organ morphogenesis in the host squid. Biol. Bull. 189: 347-355.
15. Dreyfus, D. H., M. Nagasawa, E. W. Gelfand, and L. Y. Ghoda. 2005. Modulation of p53 activity by IκBα: evidence suggesting a common phylogeny between NF-κB and p53 transcription factors. BMC Immunol. 6: 12.
16. Foster, J. S., M. A. Apicella, and M. J. McFall-Ngai. 2000. Vibrio fischeri lipopolysaccharide induces developmental apoptosis, but not complete morphogenesis, of the Euprymna scolopes symbiotic light organ. Dev. Biol. 226: 242-254.
17. Giaccia, A. J., and M. B. Kastan. 1998. The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev. 12: 2973-2983.
18. Goodson, M. S., M. Kojadinovic, J. V. Troll, T. E. Scheetz, T. L. Casavant, M. B. Soares, and M. J. McFall-Ngai. 2005. Identifying components of the NF-κB pathway in the beneficial Euprymna scolopes-Vibrio fischeri light organ symbiosis. Appl. Environ. Microbiol. 71: 6934-6946.
19. Gottifredi, V., and C. Prives. 2001. Getting p53 out of the nucleus. Science 292: 1851-1852.
20. Grand, R. J., P. S. Lecane, D. Owen, M. L. Grant, S. Roberts, A. J. Levine, and P. H. Gallimore. 1995. The high levels of p53 present in adenovirus early region 1-transformed human cells do not cause up-regulation of MDM2 expression. Virology 210: 323-334.
21. Greenblatt, M. S., W. P. Bennett, M. Hollstein, and C. C. Harris. 1994. Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis. Cancer Res. 54: 4855-4878.
22. Guichon, A., and A. Zychlinsky. 1996. Apoptosis as a trigger of inflammation in Shigella-induced cell death. Biochem. Soc. Trans. 24: 1051-1054.
23. Hainaut, P., T. Hernandez, A. Robinson, P. Rodriguez-Tome, T. Flores, M. Hollstein, C. C. Harris, and R. Montesano. 1998. IARC Database of p53 gene mutations in human tumors and cell lines: updated compilation, revised formats and new visualisation tools. Nucleic Acids Res. 26: 205-213.
24. Haupt, Y., R. Maya, A. Kazaz, and M. Oren. 1997. Mdm2 promotes the rapid degradation of p53. Nature 387: 296-299.
25. Inoue, T., L. Wu, J. Stuart, and C. G. Maki. 2005. Control of p53 nuclear accumulation in stressed cells. FEBS Lett. 579: 4978-4984.
26. Ishioka, C., C. Englert, P. Winge, Y. X. Yan, M. Engelstein, and S. H. Friend. 1995. Mutational analysis of the carboxy-terminal portion of p53 using both yeast and mammalian cell assays in vivo. Oncogene 10: 1485-1492.
27. Jessen-Eller, K., J. A. Kreiling, G. S. Begley, M. E. Steele, C. W. Walker, R. E. Stephens, and C. L. Reinisch. 2002. A new invertebrate member of the p53 gene family is developmentally expressed and responds to polychlorinated biphenyls. Environ. Health Perspect. 110: 377-385.
28. Jin, S., S. Martinek, W. S. Joo, J. R. Wortman, N. Mirkovic, A. Sali, M. D. Yandell, N. P. Pavletich, M. W. Young, and A. J. Levine. 2000. Identification and characterization of a p53 homologue in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 97: 7301-7306.
29. Kaghad, M., H. Bonnet, A. Yang, L. Creancier, J. C. Biscan, A. Valent, A. Minty, P. Chalon, J. M. Lelias, X. Dumont, P. Ferrara, F. McKeon, and D. Caput. 1997. Monoallelically expressed gene related to p53 at 1p36, a region frequently deleted in neuroblastoma and other human cancers. Cell 90: 809-819.
30. Kelley, M. L., P. Winge, J. D. Heaney, R. E. Stephens, J. H. Farell, R. J. Van Beneden, C. L. Reinisch, M. P. Lesser, and C. W. Walker. 2001. Expression of homologues for p53 and p73 in the softshell clam (Mya arenaria), a naturally-occurring model for human cancer. Oncogene 20: 748-758.
31. Kimbell, J. R., and M. J. McFall-Ngai. 2004. Symbiont-induced changes in host actin during the onset of a beneficial animal-bacterial association. Appl. Environ. Microbiol. 70: 1434-1441.
32. Koropatnick, T. A., J. T. Engle, M. A. Apicella, E. V. Stabb, W. E. Goldman, and M. J. McFall-Ngai. 2004. Microbial factor-mediated development in a host-bacterial mutualism. Science 306: 1186-1188.
33. Kubbutat, M. H., S. N. Jones, and K. H. Vousden. 1997. Regulation of p53 stability by Mdm2. Nature 387: 299-303.
34. Kussie, P. H., S. Gorina, V. Marechal, B. Elenbaas, J. Moreau, A. J. Levine, and N. P. Pavletich. 1996. Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain. Science 274: 948-953.
35. Li, J. H., X. Z. Shi, S. Lv, M. Liu, and G. W. Xu. 2005. Effect of Helicobacter pylori infection on p53 expression of gastric mucosa and adenocarcinoma with microsatellite instability. World J. Gastroenterol. 11: 4363-4366.
36. Liang, X. H., M. Volkmann, R. Klein, B. Herman, and S. J. Lockett. 1993. Co-localization of the tumor-suppressor protein p53 and human papillomavirus E6 protein in human cervical carcinoma cell lines. Oncogene 8: 2645-2652.
37. McFall-Ngai, M. J., and E. G. Ruby. 1991. Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism. Science 254: 1491-1494.
38. Mills, A. A., B. Zheng, X. J. Wang, H. Vogel, D. R. Roop, and A. Bradley. 1999. p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398: 708-713.
39. Montgomery, M. K., and M. J. McFall-Ngai. 1994. Bacterial symbionts induce host organ morphogenesis during early postembryonic development of the squid Euprymna scolopes. Development 120: 1719-1729.
40. Muttray, A. F., R. L. Cox, S. St-Jean, P. van Poppelen, C. L. Reinisch, and S. A. Baldwin. 2005. Identification and phylogenetic comparison of p53 in two distinct mussel species (Mytilus). Comp. Biochem. Physiol. C Toxicol. Pharmacol. 140: 237-250.
41. Niu, G., K. L. Wright, Y. Ma, G. M. Wright, M. Huang, R. Irby, J. Briggs, J. Karras, W. D. Cress, D. Pardoll, R. Jove, J. Chen, and H. Yu. 2005. Role of Stat3 in regulating p53 expression and function. Mol. Cell Biol. 25: 7432-7440.
42. Norimatsu, M., T. Ono, A. Aoki, K. Ohishi, T. Takahashi, G. Watanabe. K. Taya, S. Sasamoto, and Y. Tamura. 1995. Lipopolysaccharide-induced apoptosis in swine lymphocytes in vivo. Infect. Immun. 63: 1122-1126.
43. Nyholm, S. V., and M. J. McFall-Ngai. 2004. The winnowing: establishing the squid-vibrio symbiosis. Nat. Rev. Microbiol. 2: 632-642.
44. Oakley, B. R., D. R. Kirsch, and N. R. Morris. 1980. A simplified ultrasensitive silver stain for detecting proteins in polyacrylamide gels. Anal. Biochem. 105: 361-363.
45. Ollmann, M., L. M. Young, C. J. Di Como, F. Karim, M. Belvin, S. Robertson, K. Whittaker, M. Demsky, W. W. Fisher, A. Buchman, G. Duyk, L. Friedman, C. Prives, and C. Kopczynski. 2000. Drosophila p53 is a structural and functional homolog of the tumor suppressor p53. Cell 101: 91-101.
46. Ozturk, Y., E. Ozer, B. Lebe, O. Bekem, and B. Buyukgebiz. 2005. Immunohistochemical evaluation of p53 expression and proliferative activity in children with Helicobacter pylori associated gastritis. J. Pediatr. Gastroenterol. Nutr. 40: 467-470.
47. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: e45.
48. Raman, V., S. A. Martensen. D. Reisman, E. Evron, W. F. Odenwald, E. Jaffee, J. Marks, and S. Sukumar. 2000. Compromised HOXA5 function can limit p53 expression in human breast tumours. Nature 405: 974-978.
49. Reisman, D., and W. T. Loging. 1998. Transcriptional regulation of the p53 tumor suppressor gene. Semin. Cancer Biol. 8: 317-324.
50. Ryan, K. M., M. K. Ernst, N. R. Rice, and K. H. Vousden. 2000. Role of NF-κB in p53-mediated programmed cell death. Nature 404: 892-897.
51. Schmale, H., and C. Bamberger. 1997. A novel protein with strong homology to the tumor suppressor p53. Oncogene 15: 1363-1367.
52. Stephens, R. E., C. W. Walker, and C. L. Reinisch. 2001. Multiple protein differences distinguish clam leukemia cells from normal hemocytes: evidence for the involvement of p53 homologues. Comp. Biochem. Physiol. C Toxicol Pharmacol. 129: 329-38.
53. Thompson, J. D., T. J. Gibson, F. Plewniak. F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882.
54. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76: 4350-4354.
55. Venot, C., M. Maratrat, C. Dureuil, E. Conseiller, L. Bracco, and L. Debussche. 1998. The requirement for the p53 proline-rich functional domain for mediation of apoptosis is correlated with specific PIG3 gene transactivation and with transcriptional repression. EMBO J. 17: 4668-4679.
56. Vogelstein, B., D. Lane, and A. J. Levine. 2000. Surfing the p53 network. Nature 408: 307-310.
57. Walker, K. K., and A. J. Levine. 1996. Identification of a novel p53 functional domain that is necessary for efficient growth suppression. Proc. Natl. Acad. Sci. USA 93: 15335-15340.
58. Webster, G. A., and N. D. Perkins. 1999. Transcriptional cross talk between NF-κB and p53. Mol. Cell Biol. 19: 3485-3495.
59. White, E., and C. Prives. 1999. DNA damage enables p53. Nature 399: 734-735, 737.
60. Yang, A., R. Schweitzer, D. Sun, M. Kaghad, N. Walker, R. T. Bronson, C. Tabin, A. Sharpe, D. Caput, C. Crum, and F. McKeon. 1999. p63 is essential for regenerative proliferation in limb, cranio-facial and epithelial development. Nature 398: 714-718.
61. Yang, A., N. Walker, R. Bronson, M. Kaghad, M. Oosterwegel, J. Bonnin, C. Vagner, H. Bonnet, P. Dikkes, A. Sharpe, F. McKeon, and D. Caput. 2000. p73-deficient mice have neurological, pheromonal and inflammatory defects but lack spontaneous tumours. Nature 404: 99-103.
62. Yang, A., M. Kaghad, D. Caput, and F. McKeon. 2002. On the shoulders of giants: p63, p73 and the rise of p53. Trends Genet. 18: 90-95.
63. Yin, Y., W. C. DeWolf, and A. Morgentaler. 1997. p53 is associated with the nuclear envelope in mouse testis. Biochem. Biophys. Res. Commun. 235: 689-694.
64. Zhang, Y., and Y. Xiong. 2001. A p53 amino-terminal nuclear export signal inhibited by DNA damage-induced phosphorylation. Science 292: 1910-1915.
65. Zychlinsky, A., K. Thirumalai, J. Arondel, J. R. Cantey, A. O. Aliprantis, and P. J. Sansonetti. 1996. In vivo apoptosis in Shigella flexneri infections. Infect. Immun. 64: 5357-5365.