Taming the symbiont for coexistence: A host PGRP neutralizes a bacterial symbiont toxin

Environmental Microbiology

Volumn 12, Issue 8, 2010, Pages 2190-2203

  Troll, Joshua V ^a,d   Bent, Eric H ^a   Pacquette, Nicholas ^b   Wier, Andrew M ^a   Goldman, William E ^c   Silverman, Neal ^b   McFall Ngai, Margaret J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF OREGON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDASE; BACTERIAL TOXIN; CARRIER PROTEIN; CYTOTOXIN; PEPTIDOGLYCAN RECOGNITION PROTEIN;

ALIIVIBRIO FISCHERI; ANIMAL; ARTICLE; CEPHALOPOD; CHEMISTRY; DRUG ANTAGONISM; EPITHELIUM; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MORPHOGENESIS; MUCUS; SECRETION; SYMBIOSIS;

ALIIVIBRIO FISCHERI; AMIDOHYDROLASES; ANIMALS; BACTERIAL TOXINS; CARRIER PROTEINS; CYTOTOXINS; DECAPODIFORMES; EPITHELIUM; MORPHOGENESIS; MUCUS; SYMBIOSIS;

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

EID: 77954364861     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2009.02121.x     Document Type: Article

References (53)

1. Adin DM, Engle JT, Goldman WE, McFall-Ngai MJ, Stabb EV. Mutations in ampG and lytic transglycosylase genes affect the net release of peptidoglycan monomers from Vibrio fischeri. J Bacteriol 2008, 191:2012-2022.
2. Aggrawal K, Silverman N. Peptidoglycan recognition in Drosophila. Biochem Soc Trans 2007, 35:1496-1500.
3. Bischoff V, Vignal C, Duvic B, Boneca IG, Hoffmann JA, Royet J. Downregulation of the Drosophila immune response by peptidoglycan-recognition proteins SC1 and SC2. Plos Pathog 2006, 2:e14.
4. Boettcher KJ, Ruby EG, McFall-Ngai MJ. Bioluminescence in the symbiotic squid Euprymna scolopes is controlled by a daily biological rhythm. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 1996, 179:65-73.
5. Charroux B, Rival T, Narbonne-Reveau K, Royet J. Bacterial detection by Drosophila peptidoglycan recognition proteins. Microbes Infect 2009, 11:631-636.
6. Cho JH, Fraser IP, Fukase K, Kusumoto S, Fujimoto Y, Stahl GL, Ezekowitz RA. Human peptidoglycan recognition protein S is an effector of neutrophil-mediated innate immunity. Blood 2005, 106:2551-2558.
7. Cloud-Hansen KA, Peterson SB, Stabb EV, Goldman WE, McFall-Ngai MJ, Handelsman J. Breaching the great wall: peptidoglycan and microbial interactions. Nat Rev Microbiol 2006, 4:710-716.
8. Cooper JE. Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J Appl Microbiology 2007, 103:1355-1365.
9. Coteur G, Mellroth P, De Lefortery C, Gillan D, Dubois P, Communi D, Steiner H. Peptidoglycan recognition proteins with amidase activity in early deuterostomes (Echinodermata). Dev Comp Immunol 2007, 31:790-804.
10. Davidson SK, Koropatnick TA, Kossmehl R, Sycuro L, McFall-Ngai MJ. NO means 'yes' in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell Microbiol 2004, 6:1139-1151.
11. Dixon M, Webb EC. Enzymes 1964, New York, NY, USA, Academic Press
12. Doino JA, McFall-Ngai MJ. A transient exposure to symbiosis-competent bacteria induces light organ morphogenesis in the host squid. Biol Bull 1995, 189:347-355.
13. Dunn AK, Millikan DS, Adin DM, Bose JL, Stabb EV. New rfp- and pES213-derived tools for analyzing symbiotic Vibrio fischeri reveal patterns of infection and lux expression in situ. Appl Environ Microbiol 2006, 72:802-810.
14. Dziarski R. Peptidoglycan recognition proteins (PGRPs). Mol Immunol 2004, 40:877-886.
15. Dziarski R, Gupta D. Mammalian PGRPs: novel antibacterial proteins. Cell Microbiol 2006, 8:1059-1069.
16. Foster JS, McFall-Ngai MJ. Induction of apoptosis by cooperative bacteria in the morphogenesis of host epithelial tissues. Dev Genes E 1998, 208:295-303.
17. Foster JS, Apicella MA, McFall-Ngai MJ. Vibrio fischeri lipopolysaccharide induces developmental apoptosis, but not complete morphogenesis, of the Euprymna scolopes symbiotic light organ. Dev Biol 2000, 226:242-254.
18. Gage DJ. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 2004, 68:280-300.
19. Gelius E, Persson C, Karlsson J, Steiner H. A mammalian peptidoglycan recognition protein with N-acetylmuramoyl-L-alanine amidase activity. Biochem Biophys Res Commun 2003, 306:988-994.
20. Goodson MS, Kojadinovic M, Troll JV, Scheetz TE, Casavant TL, Soares MB, McFall-Ngai MJ. Identifying components of the NF-κB pathway in the beneficial Euprymna scolopes-Vibrio fischeri light organ symbiosis. Appl Environ Microbiol 2005, 71:6934-6946.
21. Gottar M, Gobert V, Michel T, Belvin M, Duyk G, Hoffmann JA. The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein. Nature 2002, 416:640-644.
22. Graf J, Ruby EG. Host-derived amino acids support the proliferation of symbiotic bacteria. Proc Natl Acad Sci USA 1998, 95:1818-1822.
23. Kaback HR. Bacterial membranes. Methods in Enzymology 1971, 99-120. Jakoby WB., New York, NY, USA, Academic Press
24. Kaneko T, Goldman WE, Mellroth P, Steiner H, Fukase K, Kusumoto S. Monomeric and polymeric gram-negative peptidoglycan but not purified LPS stimulate the Drosophila IMD pathway. Immunity 2004, 20:637-649.
25. Kelly D, Coutts AG. Early nutrition and the development of immune function in the neonate. Proc Nutr Soc 2000, 59:177-185.
26. Koropatnick TA, Engle JT, Apicella MA, Stabb EV, Goldman WE, McFall-Ngai MJ. Microbial factor-mediated development in a host-bacterial mutualism. Science 2004, 306:1186-1188.
27. Kumar S, Roychowdhury A, Ember B, Wang Q, Guan R, Mariuzza RA, Boons GJ. Selective recognition of synthetic lysine and meso-diaminopimelic acid-type peptidoglycan fragments by human peptidoglycan recognition proteins Iα and S. J Biol Chem 2005, 280:37005-37012.
28. Lamarcq LH, McFall-Ngai MJ. Induction of a gradual, reversible morphogenesis of its host's epithelial brush border by Vibrio fischeri. Infect Immun 1998, 66:777-785.
29. Lee KH, Ruby EG. Effect of the squid host on the abundance and distribution of symbiotic Vibrio fischeri in nature. Appl Environ Microbiol 1994, 60:1565-1571.
30. Luker KE, Collier JL, Kolodziej EW, Marshall GR, Goldman WE. Bordetella pertussis tracheal cytotoxin and other muramyl peptides: distinct structure-activity relationships for respiratory epithelial cytopathology. Proc Natl Acad Sci USA 1993, 90:2365-2369.
31. Luker KE, Tyler AN, Marshall GR, Goldman WE. Tracheal cytotoxin structural requirements for respiratory epithelial damage in pertussis. Mol Microbiol 1995, 16:733-743.
32. Lützner N, Pätzold B, Zoll S, Stehle T, Kalbacher H. Development of a novel fluorescent substrate for Autolysin E, a bacterial type II amidase. Biochemical Biophysical Res Comms 2009, 380:554-558.
33. McFall-Ngai MJ, Ruby EG. Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism. Science 1991, 254:1491-1494.
34. Markert S, Arndt C, Felbeck H, Becher D, Sievert SM, Hugler M. Physiological proteomics of the uncultured endosymbiont of Riftia pachyptila. Science 2007, 315:247-250.
35. Mellroth P, Steiner H. PGRP-SB1: an N-acetylmuramoyl l-alanine amidase with antibacterial activity. Biochem Biophys Res Commun 2006, 350:994-999.
36. Mellroth P, Karlsson J, Steiner H. A scavenger function for a Drosophila peptidoglycan recognition protein. J Biol Chem 2003, 278:7059-7064.
37. Melly MA, McGee ZA, Rosenthal RS. Ability of monomeric peptidoglycan fragments from Neisseria gonorrhoeae to damage human fallopian-tube mucosa. J Infect Dis 1984, 149:378-386.
38. Michel T, Reichhart JM, Hoffmann JA, Royet J. Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature 2001, 414:756-759.
39. Montgomery MK, McFall-Ngai M. Embryonic-development of the light organ of the sepiolid squid Euprymna-scolopes berry. Biological Bull 1993, 184:296-308.
40. Montgomery MK, McFall-Ngai M. Bacterial symbionts induce host organ morphogenesis during early postembryonic development of the squid Euprymna scolopes. Development 1994, 120:1719-1729.
41. Nyholm SV, McFall-Ngai MJ. Sampling the light-organ microenvironment of Euprymna scolopes: description of a population of host cells in association with the bacterial symbiont Vibrio fischeri. Biol Bull 1998, 195:89-97.
42. Nyholm SV, McFall-Ngai MJ. The winnowing: establishing the squid-vibrio symbiosis. Nat Rev Microbiol 2004, 2:632-642.
43. Nyholm SV, Stabb EV, Ruby EG, McFall-Ngai MJ. Establishment of an animal-bacterial association: recruiting symbiotic vibrios from the environment. Proc Natl Acad Sci USA 2000, 97:10231-10235.
44. Nyholm SV, Deplancke B, Gaskins HR, Apicella MA, McFall-Ngai MJ. Roles of Vibrio fischeri and nonsymbiotic bacteria in the dynamics of mucus secretion during symbiont colonization of the Euprymna scolopes light organ. Appl Environ Microbiol 2002, 68:5113-5122.
45. Ruby EG, Asato LM. Growth and flagellation of Vibrio fischeri during initiation of the sepiolid squid light organ symbiosis. Arch Microbiol 1993, 159:160-167.
46. Silverman N, Zhou R, Stoven S, Pandey N, Hultmark D, Maniatis T. A Drosophila IkappaB kinase complex required for Relish cleavage and antibacterial immunity. Genes Dev 2000, 14:2461-2471.
47. Small AL, McFall-Ngai MJ. Halide peroxidase in tissues that interact with bacteria in the host squid Euprymna scolopes. J Cell Biochem 1999, 72:445-457.
48. Steiner H. Peptidoglycan recognition proteins: on and off switches for innate immunity. Immunol Rev 2004, 198:83-96.
49. Troll JV, Adin DM, Wier AM, Paquette N, Silverman N, Goldman WE. Peptidoglycan induces loss of a nuclear peptidoglycan recognition protein during host tissue development in a beneficial animal-bacterial symbiosis. Cell Microbiol 2009, 11:1114-1127.
50. Visick KL, Foster J, Doino J, McFall-Ngai M, Ruby EG. Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J Bacteriol 2000, 182:4578-4586.
51. Wang ZM, Li X, Cocklin RR, Wang M, Fukase K, Inamura S. Human peptidoglycan recognition protein-L is an N-acetylmuramoyl-L-alanine amidase. J Biol Chem 2003, 278:49044-49052.
52. Werner T, Liu G, Kang D, Ekengren S, Steiner H, Hultmark D. A family of peptidoglycan recognition proteins in the fruit fly Drosophila melanogaster. Proc Natl Acad Sci USA 2000, 97:13772-13777.
53. Zaidman-Remy A, Herve M, Poidevin M, Pili-Floury S, Kim MS, Blanot D. The Drosophila amidase PGRP-LB modulates the immune response to bacterial infection. Immunity 2006, 24:463-473.