The oyster Crassostrea ariakensis is an economically important bivalve species in China, unfortunately it has suffered severe mortalities in recent years caused by rickettsia-like organism (RLO) infection. Prevention and control of this disease is a priority for the development of oyster aquaculture. Allograft inflammatory factor-1 (AIF-1) was identified as a modulator of the immune response during macrophage activation and a key gene in host immune defense reaction and inflammatory response. Therefore we investigated the functions of C. ariakensis AIF-1 (Ca-AIF1) and its antibody (anti-CaAIF1) in oyster RLO/LPS-induced disease and inflammation. Ca-AIF1 encodes a 149 amino acid protein containing two typical Ca2+ binding EF-hand motifs and shares a 48–95% amino acid sequence identity with other animal AIF-1s. Tissue-specific expression analysis indicates that Ca-AIF1 is highly expressed in hemocytes. Significant and continuous up-regulation of Ca-AIF1 is detected when hemocytes are stimulated with RLO/LPS (RLO or LPS). Treatment with recombinant Ca-AIF1 protein significantly up-regulates the expression levels of LITAF, MyD88 and TGFβ. When anti-CaAIF1 antibody is added to RLO/LPS-challenged hemocyte monolayers, a significant reduction of RLO/LPS-induced LITAF is observed at 1.5–12 h after treatment, suggesting that interference with Ca-AIF1 can suppress the inflammatory response. Furthermore, flow cytometric analysis indicated that anti-CaAIF1 administration reduces RLO/LPS-induced apoptosis and necrosis rates of hemocytes. Collectively these findings suggest that Ca-AIF1 functions as a pro-inflammatory cytokine in the oyster immune response and is a potential target for controlling RLO infection and LPS-induced inflammation.
References
[1]
Klein J (1997) Homology between immune responses in vertebrates and invertebrates: does it exist? Scand J Immunol 46: 558–564. doi: 10.1046/j.1365-3083.1997.d01-164.x
[2]
Loker ES, Adema CM, Zhang SM, Kepler TB (2004) Invertebrate immune systems—not homogeneous, not simple, not well understood. Immunol Rev 198: 10–24. doi: 10.1111/j.0105-2896.2004.0117.x
[3]
Hoffmann JA, Kafatos FC, Janeway CA, Ezekowitz RA (1999) Phylogenetic perspectives in innate immunity. Science 284: 1313–1318. doi: 10.1126/science.284.5418.1313
[4]
Aderem A, Ulevitch RJ (2000) Toll-like receptors in the induction of the innate immune response. Nature 406: 782–787. doi: 10.1038/35021228
[5]
Medzhitov R (2001) Toll-like receptors and innate immunity. Nat Rev Immunol 1: 135–145. doi: 10.1038/35100529
Wu XZ, Pan JP (2000) An intracellular prokaryotic microorganism associated with lesions in the oyster, Crassostrea ariakensis Gould. J Fish Dis 23: 409–414. doi: 10.1046/j.1365-2761.2000.00243.x
[8]
Sun J, Wu X (2004) Histology, ultrastructure, and morphogenesis of a rickettsia-like organism causing disease in the oyster, Crassostrea ariakensis Gould. J Invertebr Pathol 86: 77–86. doi: 10.1016/j.jip.2004.04.004
[9]
Chen SC, Wang PC, Tung MC, Thompson K, Adams A (2000.) A Piscirickettsia salmonis-like organism in grouper, Epinephelus melanostigma, in Taiwan. J Fish Dis 23: 415–418. doi: 10.1046/j.1365-2761.2000.00250.x
[10]
Ilan P (1977) Epitheliocystis infection in wild and cultured sea bream (Sparus aurata, Sparidae) and grey mullets (Liza ramada, Mugilidae). Aquaculture 10: 169–176. doi: 10.1016/0044-8486(77)90018-7
[11]
Fryer JL, Lannan CN (1996) Rickettsila infecions of fish. Annu Rev Fish Dis 6: 3–13.
[12]
Bonami JR, Pappalardo R (1980) Rickettsial infection in marine crustacea. Experientia 36: 180–181. doi: 10.1007/bf01953718
[13]
Federici BA, Hazard EI, Anthony DW (1974) Rickettsia-like organism causing disease in a crangonid amphipod from Florida. Appl Microbiol 28: 885–886.
[14]
Comps M, Bonami J-R, Vago C (1977) Pathology des inverte'bre's. - Mise en e'vidence d'une infection rickettsienne chez les Huitres. CR Acad Sc Paris, t 285: 427–429.
[15]
Wu XZ (2003) Advances in the research of marine-cultured animal diseases in China. In: Lee C-S, Ventura A, editors. Status of Aquaculture in China. Hawaii, USA in Honolulu: The Oceanic Institute. pp. 29–54.
[16]
Li DF, Wu XZ (2004) Purification and biological features of a rickettsia-like prokaryote from the scallop Argopecten irradians in China. Aquaculture 234: 29–40. doi: 10.1016/j.aquaculture.2003.11.019
[17]
Zhu B, Wu X (2008) Identification of outer membrane protein ompR from rickettsia-like organism and induction of immune response in Crassostrea ariakensis. Mol Immunol 45: 3198–3204. doi: 10.1016/j.molimm.2008.02.026
[18]
Zhu BJ, Wu XZ (2008) Characterization and function of CREB homologue from Crassostrea ariakensis stimulated by rickettsia-like organism. Develop Comp Immunol 32: 1572–1581. doi: 10.1016/j.dci.2008.05.012
[19]
Yang SB, Wu XZ (2009) Tolliod-like gene in Crassostrea ariakensis: Molecular cloning, structural characterization and expression by RLO stimulation. Fish Shellfish Immunol 27: 130–135. doi: 10.1016/j.fsi.2008.11.020
[20]
Luo M, Ye S, Xu T, Wu X, Yang P (2012) Molecular characterization of a novel tetraspanin from the oyster, Crassostrea ariakensis: variation, localization and relationship to oyster host defense. Fish Shellfish Immunol 33: 294–304. doi: 10.1016/j.fsi.2012.05.009
[21]
Yang SB, Wu XZ (2010) Identification and functional characterization of a human sTRAIL homolog, CasTRAIL, in an invertebrate oyster Crassostrea ariakensis. Develop Comp Immunol 34: 538–545. doi: 10.1016/j.dci.2009.12.014
[22]
Xu T, Xie J, Li J, Luo M, Ye S, et al. (2012) Identification of expressed genes in cDNA library of hemocytes from the RLO-challenged oyster, Crassostrea ariakensis Gould with special functional implication of three complement-related fragments (CaC1q1, CaC1q2 and CaC3). Fish Shellfish Immunol 32: 1106–1116. doi: 10.1016/j.fsi.2012.03.012
[23]
Xu T, Yang S, Xie J, Ye S, Luo M, et al. (2012) HMGB in mollusk Crassostrea ariakensis Gould: structure, pro-inflammatory cytokine function characterization and anti-infection role of its antibody. PLoS One 7: e50789. doi: 10.1371/journal.pone.0050789
[24]
Utans U, Arceci RJ, Yamashita Y, Russell ME (1995) Cloning and characterization of allograft inflammatory factor-1: a novel macrophage factor identified in rat cardiac allografts with chronic rejection. J Clin Invest 95: 2954–2962. doi: 10.1172/jci118003
[25]
Utans U, Quist WC, McManus BM, Wilson JE, Arceci RJ, et al. (1996) Allograft inflammatory factory-1. A cytokine-responsive macrophage molecule expressed in transplanted human hearts. Transplantation 61: 1387–1392. doi: 10.1097/00007890-199605150-00018
[26]
Utans U, Arceci RJ, Yamashita Y, Russell ME (1994) Identification, Cloning and Characterization of a Novel Gene, Allograft Inflammatory Factor-I (Aif-1), up-Regulated in Rat Cardiac Allografts with Transplant Arteriosclerosis. J Cell Biochem: 281–281.
[27]
Watano K, Iwabuchi K, Fujii S, Ishimori N, Mitsuhashi S, et al. (2001) Allograft inflammatory factor-1 augments production of interleukin-6, -10 and -12 by a mouse macrophage line. Immunology 104: 307–316. doi: 10.1046/j.1365-2567.2001.01301.x
[28]
Lacoste A, Cueff A, Poulet SA (2002) P35-sensitive caspases, MAP kinases and Rho modulate beta-adrenergic induction of apoptosis in mollusc immune cells. J Cell Sci 115: 761–768.
[29]
Canesi L, Lorusso LC, Ciacci C, Betti M, Zampini M, et al. (2004) Environmental estrogens can affect the function of mussel hemocytes through rapid modulation of kinase pathways. Gen Comp Endocrinol 138: 58–69. doi: 10.1016/j.ygcen.2004.05.004
[30]
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408. doi: 10.1006/meth.2001.1262
[31]
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101–1108. doi: 10.1038/nprot.2008.73
[32]
Park JM, Greten FR, Wong A, Westrick RJ, Arthur JS, et al. (2005) Signaling pathways and genes that inhibit pathogen-induced macrophage apoptosis—CREB and NF-kappaB as key regulators. Immunity 23: 319–329. doi: 10.1016/j.immuni.2005.08.010
[33]
Tang X, Marciano DL, Leeman SE, Amar S (2005) LPS induces the interaction of a transcription factor, LPS-induced TNF-alpha factor, and STAT6(B) with effects on multiple cytokines. Proc Natl Acad Sci U S A 102: 5132–5137. doi: 10.1073/pnas.0501159102
[34]
Austin B (1988) Marine Microbiology: Cambridge University Press.
[35]
de Lorgeril J, Zenagui R, Rosa RD, Piquemal D, Bachere E (2011) Whole transcriptome profiling of successful immune response to Vibrio infections in the oyster Crassostrea gigas by digital gene expression analysis. PLoS One 6: e23142. doi: 10.1371/journal.pone.0023142
[36]
Hooper C, Day R, Slocombe R, Handlinger J, Benkendorff K (2007) Stress and immune responses in abalone: limitations in current knowledge and investigative methods based on other models. Fish Shellfish Immunol 22: 363–379. doi: 10.1016/j.fsi.2006.06.009
[37]
Rosa RD, Santini A, Fievet J, Bulet P, Destoumieux-Garzon D, et al. (2011) Big defensins, a diverse family of antimicrobial peptides that follows different patterns of expression in hemocytes of the oyster Crassostrea gigas. PLoS One 6: e25594. doi: 10.1371/journal.pone.0025594
[38]
Bachere E, Gueguen Y, Gonzalez M, de Lorgeril J, Garnier J, et al. (2004) Insights into the anti-microbial defense of marine invertebrates: the penaeid shrimps and the oyster Crassostrea gigas. Immunol Rev 198: 149–168. doi: 10.1111/j.0105-2896.2004.00115.x
[39]
Kruse M, Steffen R, Batel R, Müller IM, Müller WEG (1999) Differential expression of allograft inflammatory factor 1 and of glutathione peroxidase during auto- and allograft response in marine sponges. Journal of Cell Science 112..
[40]
Zhang L, Zhao J, Li C, Su X, Chen A, et al. (2011) Cloning and characterization of allograft inflammatory factor-1 (AIF-1) from manila clam Venerupis philippinarum. Fish & Shellfish Immunology 30: 148–153. doi: 10.1016/j.fsi.2010.09.021
[41]
De Zoysa M, Nikapitiya C, Kim Y, Oh C, Kang DH, et al. (2010) Allograft inflammatory factor-1 in disk abalone (Haliotis discus discus): molecular cloning, transcriptional regulation against immune challenge and tissue injury. Fish Shellfish Immunol 29: 319–326. doi: 10.1016/j.fsi.2010.04.006
[42]
Fujiki K, Shin DH, Nakao M, Yano T (1999) Molecular cloning of carp (Cyprinus carpio) CC chemokine, CXC chemokine receptors, allograft inflammatory factor-1, and natural killer cell enhancing factor by use of suppression subtractive hybridization. Immunogenetics 49: 909–914. doi: 10.1007/s002510050573
[43]
Miyata M, Iinuma K, Miyazaki T (2001) DNA cloning and characterization of an allograft inflammatory factor-1 homologue in red sea bream (Chrysophrys major). Aquaculture 194: 63–74. doi: 10.1016/s0044-8486(00)00517-2
[44]
Autieri MV (1996) cDNA cloning of human allograft inflammatory factor-1: tissue distribution, cytokine induction, and mRNA expression in injured rat carotid arteries. Biochem Biophys Res Commun 228: 29–37. doi: 10.1006/bbrc.1996.1612
[45]
Deininger MH, Meyermann R, Schluesener HJ (2002) The allograft inflammatory factor-1 family of proteins. FEBS Lett 514: 115–121. doi: 10.1016/s0014-5793(02)02430-4
[46]
Kuschel R, Deininger MH, Meyermann R, Bornemann A, Yablonka-Reuveni Z, et al. (2000) Allograft inflammatory factor-1 is expressed by macrophages in injured skeletal muscle and abrogates proliferation and differentiation of satellite cells. J Neuropathol Exp Neurol 59: 323–332.
[47]
Schluesener HJ, Seid K, Kretzschmar J, Meyermann R (1998) Allograft-inflammatory factor-1 in rat experimental autoimmune encephalomyelitis, neuritis, and uveitis: expression by activated macrophages and microglial cells. Glia 24: 244–251. doi: 10.1002/(sici)1098-1136(199810)24:2<244::aid-glia9>3.0.co;2-3
[48]
Auteri M, Carbone M, Eisen HJ (2000) Expression of allograft inflammatory Factor-1 (AIF-1) is a marker of activated human vascular smooth muscle cells and arterial injury. Transplantation 69: S231–S231. doi: 10.1097/00007890-200004271-00454
[49]
Brauner A, Hertting O, Alkstrand E, Sandberg E, Chromek M, et al. (2003) CAPD peritonitis induces the production of a novel peptide, daintain/allograft inflammatory factor-1. Perit Dial Int 23: 5–13.
[50]
Koshiba H, Kitawaki J, Teramoto M, Kitaoka Y, Ishihara H, et al. (2005) Expression of allograft inflammatory factor-1 in human eutopic endometrium and endometriosis: possible association with progression of endometriosis. J Clin Endocrinol Metab 90: 529–537. doi: 10.1210/jc.2004-0871
[51]
Kimura M, Kawahito Y, Obayashi H, Ohta M, Hara H, et al. (2007) A critical role for allograft inflammatory factor-1 in the pathogenesis of rheumatoid arthritis. J Immunol 178: 3316–3322. doi: 10.4049/jimmunol.178.5.3316
[52]
Liu S, Tan WY, Chen QR, Chen XP, Fu K, et al. (2008) Daintain/AIF-1 promotes breast cancer proliferation via activation of the NF-kappa B/cyclin D1 pathway and facilitates tumor growth. Cancer Science 99: 952–957. doi: 10.1111/j.1349-7006.2008.00787.x
[53]
Li T, Feng Z, Jia S, Wang W, Du Z, et al.. (2011) Daintain/AIF-1 promotes breast cancer cell migration by up-regulated TNF-alpha via activate p38 MAPK signaling pathway. Breast Cancer Res Treat.
[54]
Yang ZF, Ho DW, Lau CK, Lam CT, Lum CT, et al. (2005) Allograft inflammatory factor-1 (AIF-1) is crucial for the survival and pro-inflammatory activity of macrophages. Int Immunol 17: 1391–1397. doi: 10.1093/intimm/dxh316
[55]
Chen X, Kelemen SE, Autieri MV (2004) AIF-1 expression modulates proliferation of human vascular smooth muscle cells by autocrine expression of G-CSF. Arteriosclerosis Thrombosis and Vascular Biology 24: 1217–1222. doi: 10.1161/01.atv.0000130024.50058.de
[56]
Ludviksson BR, Gunnlaugsdottir B (2003) Transforming growth factor-beta as a regulator of site-specific T-cell inflammatory response. Scand J Immunol 58: 129–138. doi: 10.1046/j.1365-3083.2003.01297.x
[57]
Wang D, Noda Y, Zhou Y, Nitta A, Nabeshima T, et al. (2004) Effects of sodium houttuyfonate on phosphorylation of CaMK II, CREB and ERK 1/2 and expression of c-Fos in macrophages. Int Immunopharmacol 4: 1083–1088. doi: 10.1016/j.intimp.2004.05.008
[58]
Takano T, Kondo H, Hirono I, Saito-Taki T, Endo M, et al. (2006) Identification and characterization of a myeloid differentiation factor 88 (MyD88) cDNA and gene in Japanese flounder, Paralichthys olivaceus. Dev Comp Immunol 30: 807–816. doi: 10.1016/j.dci.2005.11.003
