Transcriptome analysis of the white body of the squid Euprymna tasmanica with emphasis on immune and hematopoietic gene discovery

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Salazar, Karla A ^a   Joffe, Nina R ^a   Dinguirard, Nathalie ^a,b   Houde, Peter ^a   Castillo, Maria G ^a  

^a NEW MEXICO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 2; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN MCL 1; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR IID; TRANSCRIPTOME;

ADULT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CPSF1 GENE; DOWN REGULATION; EUPRYMNA TASMANICA; FGFR2 GENE; GATA 2 GENE; GENE EXPRESSION REGULATION; HEMATOPOIESIS; INNATE IMMUNITY; MCL 1 GENE; NONHUMAN; RNA ANALYSIS; RNA SEQUENCE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SQUID; SYMBIOSIS; TFIID GENE; UPREGULATION; ALIIVIBRIO FISCHERI; ANIMAL; DECAPODIFORMES; GENETICS; IMMUNITY; IMMUNOLOGY; METABOLISM; MICROBIOLOGY;

BACTERIA (MICROORGANISMS); CEPHALOPODA; EUPRYMNA TASMANICA; OCTOPUS; VIBRIO FISCHERI;

ALIIVIBRIO FISCHERI; ANIMALS; DECAPODIFORMES; GENE EXPRESSION REGULATION; HEMATOPOIESIS; IMMUNITY; TRANSCRIPTOME;

EID: 84924939976     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0119949     Document Type: Article

References (100)

1. Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science. 2005;307(5717):1915-20. doi: 10.1126/science.1104816 PMID: 15790844
2. Currie CR, Scott JA, Summerbell RC, Malloch D. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature. 2007;98(6729):701-4.
3. Franche C, Lindström K, Elmeric C. Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil. 2007;321:335-59.
4. Keeney KM, Yurist-Doutsch S, Arrieta MC, Finlay BB. Effect of Antibiotics on Human Microbiota and Subsequent Disease. Annu Rev Microbiol. 2014. doi: 10.1146/annurev-micro-091313-103456.
5. McFall-Ngai M, Montgomery MK. The anatomy and morphology of the adult bacterial light organ of Euprymna scolopes Berry (Cephalopoda: Sepiolidae). The Biological Bulletin. 1990;179(3):332-9.
6. Wei SL, Young RE. Development of symbiotic bacterial bioluminescence in a nearshore cephalopod, Euprymna scolopes. Marine Biology. 1989;103(4):541-6.
7. Jones BW, Nishiguchi MK. Counterillumination in the hawaiian bobtail squid, Euprymna scolopes Berry. Marine Biology. 2004;144(6):1151-5.
8. 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(2):89-97. PMID: 9818359
9. Nyholm SV, Stewart JJ, Ruby EG, McFall-Ngai MJ. Recognition between symbiotic Vibrio fischeri and the haemocytes of Euprymna scolopes. Environ Microbiol. 2009;11(2):483-93. doi: 10.1111/j.1462-2920.2008.01788.x PMID: 19196278
10. Collins AJ, Schleicher TR, Rader BA, Nyholm SV. Understanding the role of host hemocytes in a squid/vibrio symbiosis using transcriptomics and proteomics. Front Immunol. 2012;3:91. doi: 10. 3389/fimmu.2012.00091 PMID: 22590467
11. Schleicher TR, Ver Berkmoes NC, Shah M, Nyholm SV. Colonization state influences the hemocyte proteome in a beneficial squid-vibrio symbiosis. Mol Cell Proteomics. 2014. doi: 10.1074/mcp. M113. 037259.
12. Altura MA, Heath-Heckman EA, Gillette A, Kremer N, Krachler AM, Brennan C, et al. The first engagement of partners in the Euprymna scolopes-Vibrio fischeri symbiosis is a two-step process initiated by a few environmental symbiont cells. Environ Microbiol. 2013. doi: 10.1111/1462-2920.12179.
13. Koropatnick TA, Kimbell JR, McFall-Ngai MJ. Responses of host hemocytes during the initiation of the squid-Vibrio symbiosis. Biol Bull. 2007;212(1):29-39. PMID: 17301329
14. Cowden RR. Some cytological and cytochemical observations on the leucopoietic organs, the "white bodies" of Octupus vulgaris. Journal of Invertebrate Pathology. 1972;19(1):113-9.
15. Claes MF. Functional Morphology of the White Bodies of the Cephalopod Mollusc Sepia officinalis Acta Zoologica. 1996;77(2):173-90.
16. Moltchaniwskyj NA, Hall K, Lipinski MR, Marian JEAR, Nishiguchi M, Sakai M, et al. Ethical and welfare considerations when using cephalopods as experimental animals. Rev Fish Biol Fisheries. 2007;17:455-76.
17. Collins AJ, Nyholm SV. Obtaining hemocytes from the Hawaiian bobtail squid Euprymna scolopes and observing their adherence to symbiotic and non-symbiotic bacteria. J Vis Exp. 2010; (36:). doi: 10.3791/1714 PMID: 20190730
18. Chun CK, Scheetz TE, Bonaldo MF, Brown B, Clemens A, Crookes-Goodson WJ, et al. An annotated cDNA library of juvenile Euprymna scolopes with and without colonization by the symbiont Vibrio fischeri. BMC Genomics. 2006;7:154. doi: 10.1186/1471-2164-7-154 PMID: 16780587
19. Carter CG, Lynch KA, Moltschaniwskyj NA. Protein synthesis in a solitary benthic cephalopod, the Southern dumpling squid (Euprymna tasmanica). Comp Biochem Physiol A Mol Integr Physiol. 2009;153(2):185-90. doi: 10.1016/j.cbpa.2009.02.015 PMID: 19223018
20. Squires ZE, Wong BB, Norman MD, Stuart-Fox D. Multiple fitness benefits of polyandry in a cephalopod. PLoS One. 2012;7(5):e37074. doi: 10.1371/journal.pone.0037074 PMID: 22615896
21. Sinn DL, Moltschaniwskyj NA. Personality traits in dumpling squid (Euprymna tasmanica): contextspecific traits and their correlation with biological characteristics. J Comp Psychol. 2005;119(1):99-110. doi: 10.1037/0735-7036.119.1.99 PMID: 15740434
22. Franklin AM, Squires ZE, Stuart-Fox D. The energetic cost of mating in a promiscuous cephalopod. Biol Lett. 2012;8(5):754-6. doi: 10.1098/rsbl.2012.0556 PMID: 22809722
23. Zouari I, Salvioli A, Chialva M, Novero M, Miozzi L, Tenore GC, et al. From root to fruit: RNA-Seq analysis shows that arbuscular mycorrhizal symbiosis may affect tomato fruit metabolism. BMC Genomics. 2014;15:221. doi: 10.1186/1471-2164-15-221 PMID: 24655934
24. Rodriguez-Lanetty M, Phillips WS, Weis VM. Transcriptome analysis of a cnidarian-dinoflagellate mutualism reveals complex modulation of host gene expression. BMC Genomics. 2006;7:23. doi: 10. 1186/1471-2164-7-23 PMID: 16472376
25. Heath-Heckman EA, McFall-Ngai MJ. The occurrence of chitin in the hemocytes of invertebrates. Zoology (Jena). 2011;114(4):191-8. doi: 10.1016/j.zool.2011.02.002 PMID: 21723107
26. Mandel MJ, Schaefer AL, Brennan CA, Heath-Heckman EA, Deloney-Marino CR, McFall-Ngai MJ, et al. Squid-derived chitin oligosaccharides are a chemotactic signal during colonization by Vibrio fischeri. Appl Environ Microbiol. 2012;78(13):4620-6. doi: 10.1128/AEM.00377-12 PMID: 22522684
27. Kremer N, Philipp EE, Carpentier MC, Brennan CA, Kraemer L, Altura MA, et al. Initial symbiont contact orchestrates host-organ-wide transcriptional changes that prime tissue colonization. Cell Host Microbe. 2013;14(2):183-94. doi: 10.1016/j.chom.2013.07.006 PMID: 23954157
28. Schleicher TR, Nyholm SV. Characterizing the host and symbiont proteomes in the association between the Bobtail squid, Euprymna scolopes, and the bacterium, Vibrio fischeri. PLoS One. 2011;6(10):e25649. doi: 10.1371/journal.pone.0025649 PMID: 21998678
29. Doulatov S, Notta F, Laurenti E, Dick JE. Hematopoiesis: a human perspective. Cell Stem Cell. 2012;10(2):120-36. doi: 10.1016/j.stem.2012.01.006 PMID: 22305562
30. Iwasaki H, Akashi K. Hematopoietic developmental pathways: on cellular basis. Oncogene. 2007;26(47):6687-96. doi: 10.1038/sj.onc.1210754 PMID: 17934478
31. Bolli N, Payne EM, Rhodes J, Gjini E, Johnston AB, Guo F, et al. cpsf1 is required for definitive HSC survival in zebrafish. Blood. 2011;117(15):3996-4007. doi: 10.1182/blood-2010-08-304030 PMID: 21330472
32. Visvader JE, Crossley M, Hill J, Orkin SH, Adams JM. The C-terminal zinc finger of GATA-1 or GATA-2 is sufficient to induce megakaryocytic differentiation of an early myeloid cell line. Mol Cell Biol. 1995;15(2):634-41. PMID: 7823932
33. Tsai FY, Orkin SH. Transcription factor GATA-2 is required for proliferation/survival of early hematopoietic cells and mast cell formation, but not for erythroid and myeloid terminal differentiation. Blood. 1997;89(10):3636-43. PMID: 9160668
34. Kaufman DS, Hanson ET, Lewis RL, Auerbach R, Thomson JA. Hematopoietic colony-forming cells derived from human embryonic stem cells. Proc Natl Acad Sci U S A. 2001;98(19):10716-21. doi: 10. 1073/pnas.191362598 PMID: 11535826
35. Zhu J, Emerson SG. Hematopoietic cytokines, transcription factors and lineage commitment. Oncogene. 2002;21(21):3295-313. doi: 10.1038/sj.onc.1205318 PMID: 12032771
36. Zhang G, Fang X, Guo X, Li L, Luo R, Xu F, et al. The oyster genome reveals stress adaptation and complexity of shell formation. Nature. 2012;490(7418):49-54. doi: 10.1038/nature11413 PMID: 22992520
37. Zhang T, Qiu L, Sun Z, Wang L, Zhou Z, Liu R, et al. The specifically enhanced cellular immune responses in Pacific oyster (Crassostrea gigas) against secondary challenge with Vibrio splendidus. Dev Comp Immunol. 2014;45(1):141-50. doi: 10.1016/j.dci.2014.02.015 PMID: 24607288
38. Hart DO, Santra MK, Raha T, Green MR. Selective interaction between Trf3 and Taf3 required for early development and hematopoiesis. Dev Dyn. 2009;238(10):2540-9. doi: 10.1002/dvdy.22083 PMID: 19777587
39. Liu Z, Scannell DR, Eisen MB, Tjian R. Control of embryonic stem cell lineage commitment by core promoter factor, TAF3. Cell. 2011;146(5):720-31. doi: 10.1016/j.cell.2011.08.005 PMID: 21884934
40. Opferman JT, Iwasaki H, Ong CC, Suh H, Mizuno S, Akashi K, et al. Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science. 2005;307(5712):1101-4. doi: 10.1126/science.1106114 PMID: 15718471
41. Williams MJ. Drosophila hemopoiesis and cellular immunity. J Immunol. 2007;178(8):4711-6. PMID: 17404248
42. Sutherland DR, Yeo E, Ryan A, Mills GB, Bailey D, Baker MA. Identification of a cell-surface antigen associated with activated T lymphoblasts and activated platelets. Blood. 1991;77(1):84-93. PMID: 1984805
43. Lin M, Sutherland DR, Horsfall W, Totty N, Yeo E, Nayar R, et al. Cell surface antigen CD109 is a novel member of the alpha (2) macroglobulin/C3, C4, C5 family of thioester-containing proteins. Blood. 2002;99(5):1683-91. PMID: 11861284
44. Giesert C, Marxer A, Sutherland DR, Schuh AC, Kanz L, Buhring HJ. Antibody W7C5 defines a CD109 epitope expressed on CD34+ and CD34-hematopoietic and mesenchymal stem cell subsets. Ann N Y Acad Sci. 2003;996:227-30. PMID: 12799300
45. Hernández-Campo PM, Almeida J, Matarraz S, De Santiago M, Sánchez ML, Orfao A. Quantitative analysis of the expression of glycosylphosphatidylinositol-anchored proteins during the maturation of different hematopoietic cell compartments of normal bone marrow. Cytometry B Clin Cytom. 2007;72(1):34-42. doi: 10.1002/cyto.b.20143 PMID: 17051524
46. Wang Y, Inger M, Jiang H, Tenenbaum H, Glogauer M. CD109 plays a role in osteoclastogenesis. PLoS One. 2013;8(4):e61213. doi: 10.1371/journal.pone.0061213 PMID: 23593435
47. Castellanos-Martínez S, Prado-Alvarez M, Lobo-da-Cunha A, Azevedo C, Gestal C. Morphologic, cytometric and functional characterization of the common octopus (Octopus vulgaris) hemocytes. Dev Comp Immunol. 2014;44(1):50-8. doi: 10.1016/j.dci.2013.11.013 PMID: 24296436
48. Medzhitov R, Janeway CA. Innate immunity: the virtues of a nonclonal system of recognition. Cell. 1997;91(3):295-8. PMID: 9363937
49. Janeway CA, Medzhitov R. Innate immune recognition. Annu Rev Immunol. 2002;20:197-216. doi: 10.1146/annurev. immunol.20.083001.084359 PMID: 11861602
50. Gordon S. Pattern recognition receptors: doubling up for the innate immune response. Cell. 2002;111(7):927-30. PMID: 12507420
51. McFall-Ngai M, Nyholm SV, Castillo MG. The role of the immune system in the initiation and persistence of the Euprymna scolopes-Vibrio fischeri symbiosis. Semin Immunol. 2010;22(1):48-53. doi: 10.1016/j.smim.2009.11.003 PMID: 20036144
52. Nyholm SV, Graf J. Knowing your friends: invertebrate innate immunity fosters beneficial bacterial symbioses. Nat Rev Microbiol. 2012;10(12):815-27. doi: 10.1038/nrmicro2894 PMID: 23147708
53. Detournay O, Schnitzler CE, Poole A, Weis VM. Regulation of cnidarian-dinoflagellate mutualisms: Evidence that activation of a host TGFβ innate immune pathway promotes tolerance of the symbiont. Dev Comp Immunol. 2012;38(4):525-37. doi: 10.1016/j.dci.2012.08.008 PMID: 23010490
54. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell. 2005;122(1):107-18. doi: 10.1016/j.cell. 2005.05.007 PMID: 16009137
55. Lee YK, Mazmanian SK. Has the microbiota played a critical role in the evolution of the adaptive immune system? Science. 2010;330(6012):1768-73. doi: 10.1126/science.1195568 PMID: 21205662
56. Kvennefors EC, Leggat W, Kerr CC, Ainsworth TD, Hoegh-Guldberg O, Barnes AC. Analysis of evolutionarily conserved innate immune components in coral links immunity and symbiosis. Dev Comp Immunol. 2010;34(11):1219-29. doi: 10.1016/j.dci.2010.06.016 PMID: 20600272
57. Goodson MS, Kojadinovic M, Troll JV, Scheetz TE, Casavant TL, Soares MB, et al. Identifying components of the NF-kappaB pathway in the beneficial Euprymna scolopes-Vibrio fischeri light organ symbiosis. Appl Environ Microbiol. 2005;71(11):6934-46. doi: 10.1128/AEM.71.11.6934-6946.2005 PMID: 16269728
58. Drew BA, Burow ME, Beckman BS. MEK5/ERK5 pathway: the first fifteen years. Biochim Biophys Acta. 2012;1825(1):37-48. doi: 10.1016/j.bbcan. 2011.10.002 PMID: 22020294
59. Tada K, Okazaki T, Sakon S, Kobarai T, Kurosawa K, Yamaoka S, et al. Critical roles of TRAF2 and TRAF5 in tumor necrosis factor-induced NF-kappa B activation and protection from cell death. J Biol Chem. 2001;276(39):36530-4. doi: 10.1074/jbc. M104837200 PMID: 11479302
60. Gil J, García MA, Gomez-Puertas P, Guerra S, Rullas J, Nakano H, et al. TRAF family proteins link PKR with NF-kappa B activation. Mol Cell Biol. 2004;24(10):4502-12. PMID: 15121867
61. Oeckinghaus A, Hayden MS, Ghosh S. Crosstalk in NF-. B signaling pathways. Nat Immunol. 2011;12(8):695-708. doi: 10.1038/ni.2065 PMID: 21772278
62. Kraus ZJ, Haring JS, Bishop GA. TNF receptor-associated factor 5 is required for optimal T cell expansion and survival in response to infection. J Immunol. 2008;181(11):7800-9. PMID: 19017969
63. Castellanos-Martínez S, Arteta D, Catarino S, Gestal C. De Novo Transcriptome Sequencing of the Octopus vulgaris Hemocytes Using Illumina RNA-Seq Technology: Response to the Infection by the Gastrointestinal Parasite Aggregata octopiana. PLoS One. 2014;9(10):e107873. doi: 10.1371/journal.pone.0107873 PMID: 25329466
64. Jurica MS, Licklider LJ, Gygi SR, Grigorieff N, Moore MJ. Purification and characterization of native spliceosomes suitable for three-dimensional structural analysis. RNA. 2002;8(4):426-39. PMID: 11991638
65. Liu S, Rauhut R, Vornlocher HP, Lührmann R. The network of protein-protein interactions within the human U4/U6. U5 tri-snRNP. RNA. 2006;12(7):1418-30. doi: 10.1261/rna.55406 PMID: 16723661
66. De Arras L, Laws R, Leach SM, Pontis K, Freedman JH, Schwartz DA, et al. Comparative Genomics RNAi Screen Identifies Eftud2 as a Novel Regulator of Innate Immunity. Genetics. 2013;197(2):485-96. doi: 10.1534/genetics.113.160499 PMID: 24361939
67. Rosado CJ, Kondos S, Bull TE, Kuiper MJ, Law RH, Buckle AM, et al. The MACPF/CDC family of pore-forming toxins. Cell Microbiol. 2008;10(9):1765-74. doi: 10.1111/j.1462-5822.2008.01191.x PMID: 18564372
68. Estévez-Calvar N, Romero A, Figueras A, Novoa B. Involvement of pore-forming molecules in immune defense and development of the Mediterranean mussel (Mytilus galloprovincialis). Dev Comp Immunol. 2011;35(10):1017-31. doi: 10.1016/j.dci.2011.03.023 PMID: 21530583
69. Dreon MS, Frassa MV, Ceolín M, Ituarte S, Qiu JW, Sun J, et al. Novel animal defenses against predation: a snail egg neurotoxin combining lectin and pore-forming chains that resembles plant defense and bacteria attack toxins. PLoS One. 2013;8(5):e63782. doi: 10.1371/journal.pone.0063782 PMID: 23737950
70. Bikker FJ, Ligtenberg AJ, Nazmi K, Veerman EC, Van't Hof W, Bolscher JG, et al. Identification of the bacteria-binding peptide domain on salivary agglutinin (gp-340/DMBT1), a member of the scavenger receptor cysteine-rich superfamily. J Biol Chem. 2002;277(35):32109-15. doi: 10.1074/jbc. M203788200 PMID: 12050164
71. Madsen J, Tornøe I, Nielsen O, Lausen M, Krebs I, Mollenhauer J, et al. CRP-ductin, the mouse homologue of gp-340/deleted in malignant brain tumors 1(DMBT1), binds gram-positive and gram-negative bacteria and interacts with lung surfactant protein D. Eur J Immunol. 2003;33(8):2327-36. doi: 10.1002/eji.200323972 PMID: 12884308
72. Bikker FJ, Ligtenberg AJ, End C, Renner M, Blaich S, Lyer S, et al. Bacteria binding by DMBT1/SAG/gp-340 is confined to the VEVLXXXXW motif in its scavenger receptor cysteine-rich domains. J Biol Chem. 2004;279(46):47699-703. doi: 10.1074/jbc. M406095200 PMID: 15355985
73. Rosenstiel P, Sina C, End C, Renner M, Lyer S, Till A, et al. Regulation of DMBT1 via NOD2 and TLR4 in intestinal epithelial cells modulates bacterial recognition and invasion. J Immunol. 2007;178(12):8203-11. PMID: 17548659
74. Torti FM, Torti SV. Regulation of ferritin genes and protein. Blood. 2002;99(10):3505-16. PMID: 11986201
75. Septer AN, Wang Y, Ruby EG, Stabb EV, Dunn AK. The haem-uptake gene cluster in Vibrio fischeri is regulated by Fur and contributes to symbiotic colonization. Environ Microbiol. 2011;13(11):2855-64. doi: 10.1111/j.1462-2920.2011.02558.x PMID: 21883801
76. Kremer N, Voronin D, Charif D, Mavingui P, Mollereau B, Vavre F. Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathog. 2009;5(10):e1000630. doi: 10.1371/journal.ppat.1000630 PMID: 19851452
77. Chou CC, Gatti RA, Fuller ML, Concannon P, Wong A, Chada S, et al. Structure and expression of ferritin genes in a human promyelocytic cell line that differentiates in vitro. Mol Cell Biol. 1986;6(2):566-73. PMID: 3023856
78. Scaccabarozzi A, Arosio P, Weiss G, Valenti L, Dongiovanni P, Fracanzani AL, et al. Relationship between TNF-alpha and iron metabolism in differentiating human monocytic THP-1 cells. Br J Haematol. 2000;110(4):978-84. PMID: 11054092
79. Wang ZM, Li X, Cocklin RR, Wang M, Fukase K, Inamura S, et al. Human peptidoglycan recognition protein-L is an N-acetylmuramoyl-L-alanine amidase. J Biol Chem. 2003;278(49):49044-52. doi: 10. 1074/jbc. M307758200 PMID: 14506276
80. Troll JV, Adin DM, Wier AM, Paquette N, Silverman N, Goldman WE, et al. Peptidoglycan induces loss of a nuclear peptidoglycan recognition protein during host tissue development in a beneficial animalbacterial symbiosis. Cell Microbiol. 2009;11(7):1114-27. doi: 10.1111/j.1462-5822.2009.01315. x PMID: 19416268
81. Troll JV, Bent EH, Pacquette N, Wier AM, Goldman WE, Silverman N, et al. Taming the symbiont for coexistence: a host PGRP neutralizes a bacterial symbiont toxin. Environ Microbiol. 2010;12(8):2190-203. doi: 10.1111/j.1462-2920.2009.02121.x PMID: 21966913
82. Guan R, Roychowdhury A, Ember B, Kumar S, Boons GJ, Mariuzza RA. Structural basis for peptidoglycan binding by peptidoglycan recognition proteins. Proc Natl Acad Sci U S A. 2004;101(49):17168-73. doi: 10.1073/pnas.0407856101 PMID: 15572450
83. Mellroth P, Karlsson J, Steiner H. A scavenger function for a Drosophila peptidoglycan recognition protein. J Biol Chem. 2003;278(9):7059-64. doi: 10.1074/jbc. M208900200 PMID: 12496260
84. Lazzaro BP. Natural selection on the Drosophila antimicrobial immune system. Curr Opin Microbiol. 2008;11(3):284-9. doi: 10.1016/j.mib.2008.05.001 PMID: 18555739
85. Fujito NT, Sugimoto S, Nonaka M. Evolution of thioester-containing proteins revealed by cloning and characterization of their genes from a cnidarian sea anemone, Haliplanella lineate. Dev Comp Immunol. 2010;34(7):775-84. doi: 10.1016/j.dci.2010.02.011 PMID: 20188753
86. Sottrup-Jensen L, Stepanik TM, Kristensen T, Lønblad PB, Jones CM, Wierzbicki DM, et al. Common evolutionary origin of alpha 2-macroglobulin and complement components C3 and C4. Proc Natl Acad Sci U S A. 1985;82(1):9-13. PMID: 2578664
87. Dodds AW, Law SK. The phylogeny and evolution of the thioester bond-containing proteins C3, C4 and alpha 2-macroglobulin. Immunol Rev. 1998;166:15-26. PMID: 9914899
88. Nonaka M, Yoshizaki F. Evolution of the complement system. Mol Immunol. 2004;40(12):897-902. PMID: 14698228
89. Dishaw LJ, Smith SL, Bigger CH. Characterization of a C3-like cDNA in a coral: phylogenetic implications. Immunogenetics. 2005;57(7):535-48. doi: 10.1007/s00251-005-0005-1 PMID: 16041540
90. Castillo MG, Goodson MS, McFall-Ngai M. Identification and molecular characterization of a complement C3 molecule in a lophotrochozoan, the Hawaiian bobtail squid Euprymna scolopes. Dev Comp Immunol. 2009;33(1):69-76. doi: 10.1016/j.dci.2008.07.013 PMID: 18765250
91. Law SK, Dodds AW. The internal thioester and the covalent binding properties of the complement proteins C3 and C4. Protein Sci. 1997;6(2):263-74. doi: 10.1002/pro.5560060201 PMID: 9041627
92. Sahu A, Lambris JD. Structure and biology of complement protein C3, a connecting link between innate and acquired immunity. Immunol Rev. 2001;180:35-48. PMID: 11414361
93. Altura MA, Stabb E, Goldman W, Apicella M, McFall-Ngai MJ. Attenuation of host NO production by MAMPs potentiates development of the host in the squid-vibrio symbiosis. Cell Microbiol. 2011;13(4):527-37. doi: 10.1111/j.1462-5822.2010.01552.x. PMID: 21091598
94. Davidson SK, Koropatnick TA, Kossmehl R, Sycuro L, McFall-Ngai MJ. NO means 'yes' in the squidvibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell Microbiol. 2004;6(12):1139-51. doi: 10.1111/j.1462-5822.2004.00429.x. PMID: 15527494
95. Wier AM, Nyholm SV, Mandel MJ, Massengo-Tiassé RP, Schaefer AL, Koroleva I, et al. Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis. Proc Natl Acad Sci U S A. 2010;107(5):2259-64. doi: 10.1073/pnas. 0909712107 PMID: 20133870
96. Portela J, Duval D, Rognon A, Galinier R, Boissier J, Coustau C, et al. Evidence for specific genotypedependent immune priming in the lophotrochozoan Biomphalaria glabrata snail. J Innate Immun. 2013;5(3):261-76. doi: 10.1159/000345909 PMID: 23343530
97. Pham LN, Dionne MS, Shirasu-Hiza M, Schneider DS. A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog. 2007;3(3):e26. doi: 10.1371/journal.ppat. 0030026 PMID: 1735253
98. Mills KH. Regulatory T cells: friend or foe in immunity to infection? Nat Rev Immunol. 2004;4(11):841-55. doi: 10.1038/nri1485 PMID: 15516964
99. Di Pietro LA. Wound healing: the role of the macrophage and other immune cells. Shock. 1995;4(4):233-40. PMID: 8564549
100. Carnaud C, Lee D, Donnars O, Park SH, Beavis A, Koezuka Y, et al. Cutting edge: Cross-talk between cells of the innate immune system: NKT cells rapidly activate NK cells. J Immunol. 1999;163(9):4647-50. PMID: 10528160