Defending against pathogens-immunological priming and its molecular basis in a sea anemone, cnidarian

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Brown, Tanya ^a   Rodriguez Lanetty, Mauricio ^a  

^a FLORIDA INTERNATIONAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANEMONE; EXPOSURE; PATHOGENESIS; SEA ANEMONE; SEASON; STRESS; THINKING; TREE OF LIFE; ANIMAL; IMMUNOLOGY; VIBRIO; VIBRIOSIS;

ANIMALS; SEA ANEMONES; VIBRIO; VIBRIO INFECTIONS;

EID: 84949033762     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep17425     Document Type: Article

References (73)

1. Janeway C., Travers P., Walport M., Capra J. Immunobiology: the immune system in health and disease. (ed. Elsevier Science Ltd./Garland Publishing) (1999).
2. Beck G., Habicht G. S. Immunity and the invertebrates-The fabulously complex immune systems of humans and other mammals evolved over hundreds of millions of years-in sometimes surprising ways. Sci. Am. 275, 60 (1996).
3. Loker E. S., Adema C. M., Zhang S. M., Kepler T. B. Invertebrate immune systems-not homogeneous, not simple, not well understood. Immunol Rev 198, 10-24 (2004).
4. Little T. J., Hultmark D., Read A. F. Invertebrate immunity and the limits of mechanistic immunology. Nature Immunol 6, 651-654 (2005).
5. Kurtz J. Memory in the innate and adaptive immune systems. Microbes and Infect. 6, 1410-1417 (2004).
6. Kurtz J., Franz K. Evidence for memory in invertebrate immunity. Nature 425, 37-38 (2003).
7. Little T. J., O'Connor B., Colegrave N., Watt K., Read A. F. Maternal transfer of strain-specific immunity in an invertebrate. Curr. Biol. 13, 489-492 (2003).
8. Roth O., Sadd B. M., Schmid-Hempel P., Kurtz J. Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum. Proc. R. Soc. B 276, 145-151 (2009).
9. Sadd B. M., Schmid-Hempel P. Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr. Biol. 16, 1206-1210 (2006).
10. Johnson K. N., van Hulten M. C. W., Barnes A. C. "Vaccination" of shrimp against viral pathogens: phenomenology and underlying mechanisms. Vaccine. 26, 4885-4892 (2008).
11. Hildemann W. H., Bigger C. H., Jokiel P. L. Characteristics of immune memory in invertebrates. Am. Zool. 19, 911-911 (1979).
12. Hildemann W. H., Jokiel P. L., Bigger C. H., Johnston I. S. Allogeneic polymorphism and alloimmune memory in the coral, Montipora verrucosa. Transplantation 30, 297-301 (1980).
13. Hildemann W. H., Raison R. L., Cheung G., Hull C. J., Akaka L., Okamoto J. Immunological specificity and memory in a scleractinian coral. Nature 270, 219-223 (1977).
14. Bigger C. H. Interspecific and intraspecific acrorhagial aggressive-behavior among sea anemones-a recognition of self and notself. Biol. Bull. 159, 117-134 (1980).
15. Saltercid L., Bigger C. H. Alloimmunity in the gorgonian coral Swiftia exerta. Biol. Bull. 181, 127-134 (1991).
16. Bourne D. G., Garren M., Work T. M., Rosenberg E., Smith G. W., Harvell C. D. Microbial disease and the coral holobiont. Trends Microbiol. 17, 554-562 (2009).
17. Richardson L. L. Coral diseases: what is really known Trends Ecol. Evol. 13, 438-443 (1998).
18. Rosenberg E., Koren O., Reshef L., Efrony R., Zilber-Rosenberg I. The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microbiol. 5, 355-362 (2007).
19. Sheridan C., Kramarsky-Winter E., Sweet M., Kushmaro A., Leal M. C. Diseases in coral aquaculture: causes, implications and preventions. Aquaculture 396, 124-135 (2013).
20. Harvell C. D. et al. Ecology-climate warming and disease risks for terrestrial and marine biota. Science. 296, 2158-2162 (2002).
21. Harvell D. et al. Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography. 20, 172-195 (2007).
22. Hoegh-Guldberg O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737-1742 (2007).
23. Burge C. A. et al. Climate change influences on marine infectious diseases: implications for management and society. Ann. Rev. Mar. Sci. 6, 249-277 (2014).
24. Weis V. M., Davy S. K., Hoegh-Guldberg O., Rodriguez-Lanetty M., Pringe J. R. Cell biology in model systems as the key to understanding corals. Trends Ecol. Evol. 23, 369-376 (2008).
25. Otero C., Brown T., Rodriguez-Lanetty M. Genomic analysis shows bacterial community shifts in Aiptasia pallida between environments. Proc. 43rd Benthic Ecology Meeting. (2014). Available at: http://imageslab.fiu.edu/sites/default/files/Oteroetal2014.pdf
26. Santos S. R., Gutierrez-Rodriguez C., Coffroth M. A. Phylogenetic identification of symbiotic dinoflagellates via length heteroplasmy in domain V of chloroplast large subunit (cp23S)-ribosomal DNA sequences. Mar. Biotechnol. 5, 130-140 (2003).
27. Ben-Haim Y. et al. Vibrio coralliilyticus sp nov., a temperature-dependent pathogen of the coral Pocillopora damicornis. Int. J. Syst. Evol. Microbiol. 53, 309-315 (2003).
28. Sussman M., Willis B. L., Victor S., Bourne D. G. Coral pathogens identified for white syndrome (WS) epizootics in the Indo-Pacific. Plos One. 3, e2393 (2008).
29. Zaragoza W. J., Krediet C. J., Meyer J. L., Canas G., Ritchie K. B., Teplitski M. Outcomes of infections of sea anemone Aiptasia pallida with Vibrio spp. pathogenic to corals. Microb. Ecol. 68, 388-396 (2014).
30. Brown T., Rodriguez-Lanetty M. Molecular mechanisms underpinning immunological memory in a basal metazoan (Cnidaria). Integrative and
31. Ben-Haim Y., Zicherman-Keren M., Rosenberg E. Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl. Environ. Microbiol. 69, 4236-4242 (2003).
32. Young D., Hussell T., Dougan G. Chronic bacterial infections: living with unwanted guests. Nature Immunol. 3, 1026-1032 (2002).
33. Rinkevich B. Allorecognition and xenorecognition in reef corals: a decade of interactions. Hydrobiologia 530, 443-450 (2004).
34. Contreras-Garduno J., Rodriguez M. C., Rodriguez M. H., Alvarado-Delgado A., Lanz-Mendoza H. Cost of immune priming within generations: trade-off between infection and reproduction. Microbes Infect. 16, 261-267 (2014).
35. Bruno J. F. et al. Thermal stress and coral cover as drivers of coral disease outbreaks. Plos Biol. 5, 1220-1227 (2007).
36. Cervino J. M. et al. Relationship of Vibrio species infection and elevated temperatures to yellow blotch/band disease in Caribbean corals. Appl. Environ. Microbiol. 70, 6855-6864 (2004).
37. Ruiz-Moreno D., Vargas I. S., Olson K. E., Harrington L. C. Modeling dynamic introduction of Chikungunya Virus in the United States. PloS Negl. Trop. Dis. 6, e1918 (2012).
38. Ward J. R., Kim K., Harvell C. D. Temperature affects coral disease resistance and pathogen growth. Mar. Ecol. Prog. Ser. 329, 115-121 (2007).
39. Miller A. W., Richardson L. L. Fine structure analysis of black band disease (BBD) infected coral and coral exposed to the BBD toxins microcystin and sulfide. J Invertebr. Pathol. 109, 27-33 (2012).
40. Abdul-Careem M. F. et al. Genital HSV-2 infection induces short-term NK cell memory. Plos One. 7, e32821 (2012).
41. Ziauddin J., Schneider D. S. Where does innate immunity stop and adaptive immunity begin Cell Host Microbe. 12, 394-395 (2012).
42. Dong Y. M., Taylor H. E., Dimopoulos G. AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. Plos Biol. 4, 1137-1146 (2006).
43. Watson F. L. et al. Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309, 1874-1878 (2005).
44. Hemmrich G., Miller D. J., Bosch T. C. G. The evolution of immunity: a low-life perspective. Trends Immunol. 28, 449-454 (2007).
45. Jesus Otero-Gonzalez A. et al. Antimicrobial peptides from marine invertebrates as a new frontier for microbial infection control. Faseb J. 24, 1320-1334 (2010).
46. Mydlarz L. D., Jones L. E., Harvell C. D. Innate immunity environmental drivers and disease ecology of marine and freshwater invertebrates. Annu. Rev. Ecol. Evol. Syst. 37, 251-288 (2006).
47. Libro S., Kaluziak S. T., Vollmer S. V. RNA-seq profiles of immune related genes in the staghorn coral Acropora cervicornis infected with white band disease. Plos One 8, e81821 (2013).
48. Pinzon J. H. C., Beach-Letendre J., Weil E., Mydlarz L. D. Relationship between phylogeny and immunity suggests older Caribbean coral lineages are more resistant to disease. Plos One. 9, e104787 (2014).
49. Bolte S., Roth O., Philipp E. E. R., Saphoerster J., Rosenstiel P., Reusch T. B. H. Specific immune priming in the invasive ctenophore Mnemiopsis leidyi. Biol. Lett 9 (2013).
50. Netea M. G., Quintin J., van der Meer J. W. M. Trained immunity: a memory for innate host defense. Cell Host Microbe. 9, 355-361 (2011).
51. Cheng S. C. et al. mTOR-and HIF-1 alpha-mediated aerobic glycolysis as metabolic basis for trained immunity. Science. 345, 1579 (2014).
52. Rinkevich B. The 'immunology trap' of anthozoans. Invertebr. Surviv. J. 8, 153-161 (2011).
53. Li G. C., Werb Z. Correlation between synthesis of heat-shock proteins and development of thermotolerance in Chinese hamster fibroblasts. . Proc. Natl. Acad. Sci. USA 79, 3218-3222 (1982).
54. Lindquist S., Craig E. A. The heat-shock proteins. Annu. Rev. Genet. 22, 631-677 (1988).
55. Zugel U., Kaufmann S. H. E. Immune response against heat shock proteins in infectious diseases. Immunobiology. 201, 22-35 (1999).
56. Brown T., Bourne D., Rodriguez-Lanetty M. Transcriptional activation of c3 and hsp70 as part of the immune response of Acropora millepora to bacterial challenges. Plos One 8, e67246 (2013).
57. Kono H., Rock K. L. How dying cells alert the immune system to danger. Nat. Rev. Immunol. 8, 279-289 (2008).
58. Sanchez-Perez L. et al. Killing of normal melanocytes, combined with heat shock protein 70 and CD40L expression, cures large established melanomas. J. Immunol. 177, 4168-4177 (2006).
59. Zhang K., Zhou B., Wang Y. Y., Rao L., Zhang L. The TLR4 gene polymorphisms and susceptibility to cancer: a systematic review and meta-analysis. Eur. J. Cancer. 49, 946-954 (2013).
60. Prohaszka Z. et al. Heat shock protein 70 is a potent activator of the human complement system. Cell Stress Chaperones. 7, 17-22 (2002).
61. Baruah K., Ranjan J., Sorgeloos P., MacRae T. H., Bossier P. Priming the prophenoloxidase system of Artemia franciscana by heat shock proteins protects against Vibrio campbellii challenge. Fish Shellfish Immunol. 31, 134-141 (2011).
62. Sung Y. Y., Pineda C., MacRae T. H., Sorgeloos P., Bossier P. Exposure of gnotobiotic Artemia franciscana larvae to abiotic stress promotes heat shock protein 70 synthesis and enhances resistance to pathogenic Vibrio campbellii. Cell Stress Chaperones. 13, 59-66 (2008).
63. Sung Y. Y. et al. Ingestion of bacteria overproducing DnaK attenuates Vibrio infection of Artemia franciscana larvae. Cell Stress Chaperones. 14, 603-609 (2009).
64. Benton R., Vannice K. S., Gomez-Diaz C., Vosshall L. B. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell. 136, 149-162 (2009).
65. Croset V. et al. Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. Plos Genet. 6, e1001064 (2010).
66. Forde B. G., Roberts M. R. Glutamate receptor-like channels in plants: a role as amino acid sensors in plant defence F1000Prime Rep. 6, 12703 (2014).
67. Mousavi S. A. R., Chauvin A., Pascaud F., Kellenberger S., Farmer E. E. Glutamate receptor-like genes mediate leaf-to-leaf wound signalling. Nature. 500, 422, (2013).
68. Conus S., Simon H.-U. Cathepsins and their involvement in immune responses. Swiss Med. Wkly. 140, 4-11 (2010).
69. Matsumoto F. et al. Cathepsins are required for toll-like receptor 9 responses. Biochem. Biophys. Res. Commun. 367, 693-699 (2008).
70. Ewald S. E. et al. The ectodomain of Toll-like receptor 9 is cleaved to generate a functional receptor. Nature. 456, 658-U688 (2008).
71. Park B., Brinkmann M. M., Spooner E., Lee C. C., Kim Y. M., Ploegh H. L. Proteolytic cleavage in an endolysosomal compartment is required for activation of Toll-like receptor 9. Nature Immunology. 9, 1407-1414 (2008).
72. Polson S. W., Higgins J. L., Woodley C. M. PCR-based assay for detection of four coral pathogens. Proc. 11th Int. Coral Reef Symposium. 8, 247-251 (2008).
73. Baumgarten et al. The genome of Aiptasia, a sea anemone model for coral symbiosis. Proc. Natl. Acad. Sci. USA 112, 11893-11898 (2015).