Heat shock proteins and disease control in aquatic organisms

Journal of Aquaculture Research and Development

Volumn , Issue SPEC. ISSUE 2, 2011, Pages

  Sung, Yeong Yik ^a   Macrae, Thomas H ^b  

^a UNIVERSITI MALAYSIA TERENGGANU   (Malaysia)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Aquaculture; Aquatic organisms; Disease; Heat shock proteins; Innate immunity; Molecular chaperone; Vaccine

Indexed keywords

EID: 84883643052     PISSN: None     EISSN: 21559546     Source Type: Journal    
DOI: 10.4172/2155-9546.S2-006     Document Type: Article

References (122)

1. Pockley AG, Muthana M, Calderwood SK (2008) The dual immunoregulatory roles of stress proteins. Trends Biochem Sci 33: 71-79.
2. Sung YY, MacRae TH, Sorgeloos P, Bossier P (2011) Stress Response for Disease Control in Aquaculture. Rev Aquacult 3: 120-137.
3. Pockley AG (2003) Heat shock proteins as regulators of the immune response. Lancet 362: 469-476.
4. Sun Y, MacRae TH (2005) Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci 62: 2460-2476.
5. Clegg JS, Jackson SA, Hoa NV, Sorgeloos P (2000) Thermal resistance, developmental rate and heat shock proteins in Artemia franciscana, from San Francisco Bay and Southern Vietnam. J Exp Mar Biol Ecol 252: 85-96.
6. Brown HM, Briden A, Stokell T, Griffn FJ, Cherr GN (2004) Thermotolerance and Hsp70 profles in adult and embryonic California native oysters, Ostreola conchaphila (Carpenter, 1857). J Shellfish Res 23: 135-141.
7. Brun NT, Bricelj VN, MacRae TH, Ross NW (2009) Acquisition of thermotolerance in bay scallops, Argopecten irradians irradians, via differential induction of heat shock proteins. J Exp Mar Biol Ecol 371: 77-83.
8. Basu N, Todgham AEP, Ackerman A, Bibeau MR, Nakano K, et al. (2002) Heat shock protein genes and their functional significance in fish. Gene 295: 173-183.
9. Roberts RJ, Agius C, Saliba C, Bossier P, Sung YY (2010) Heat Shock Proteins (Chaperones) in Fishes and Shellfishes and their Potential Role in Health and Welfare: A Review. J Fish Dis 33: 789-801.
10. Iwama GK, Afonso LOB, Todgham A, Ackerman P, Nakano K (2004) Are hsps suitable for indicating stressed states in fish. J Exp Biol 207: 15-19.
11. Srivastava P (2002) Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Annu Rev Immunol 20: 395-425.
12. Wieten L, van der Zee R, Spiering R, Wagenaar-Hilbers J, van Kooten P, et al. (2010) A Novel Heat-Shock Protein Coinducer Boosts Stress Protein Hsp70 to Activate T Cell Regulation of Infammation in Autoimmune Arthritis. Arthritis Rheum 62: 1026-1035.
13. Yang C, Zhang J, Li F, Ma H, Zhang Q, et al. (2008) A Toll receptor from Chinese shrimp Fenneropenaeus chinensis is responsive to Vibrio anguillarum infection. Fish Shellfish Immunol 24: 564-574.
14. Baruah K, Ranjan J, Sorgeloos P, Bossier P (2010) Efficacy of heterologous and homologous heat shock protein 70s as protective agents to Artemia franciscana challenged with Vibrio campbellii. Fish Shellfish Immunol 29: 733-739.
15. Wang L, Baruah K, Fan T, Yu M, Bossier P (2010) Infuence of heat shock proteins induction in different yeast cell wall mutants on the protection against Vibrio campbellii infection in gnotobiotically grown Artemia franciscana (Kellogg). J Fish Dis 33: 919-923.
16. Sung YY, Van Damme EJM, Sorgeloos P, Bossier P (2007) Non-lethal heat shock protects gnotobiotic Artemia franciscana larvae against virulent Vibrios. Fish Shellfsh Immunol 22: 318-326.
17. Sung YY, Pineda C, MacRae TH, Sorgeloos P, Bossier P (2008) 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.
18. Sung YY, Ashame MF, Chen SJ, MacRae TH, Sorgeloos P, et al. (2009a) Feeding Artemia franciscana (Kellogg) larvae with bacterial heat shock protein, protects from Vibrio campbellii (Baumann) infection. J Fish Dis 32: 675-685.
19. Sung YY, Dhaene T, Defoirdt T, Boon N, MacRae TH, et al. (2009b) Ingestion of bacteria over-producing DnaK attenuates Vibrio infection of gnotobiotic Artemia franciscana larvae. Cell Stress Chaperones 14: 603-609.
20. Ryckaert J, Pasmans F, Tobback E, Duchateau L, Decostere A, et al. (2010) Heat shock proteins protect platyfsh (Xiphophorus maculatus) from Yersinia ruckeri induced mortality. Fish Shellfish Immunol 28: 228-231.
21. Marshall SH, Conejeros P, Zahr M, Olivares J, Gómez F, et al. (2007) Immunological characterization of a bacterial protein isolated from salmonid fsh naturally infected with Piscirickettsia salmonis. Vaccine 25: 2095-2102.
22. Dang W, Zhang M, Sun L (2011) Edwardsiella tarda DnaJ is a virulence-associated molecular chaperones with immunoprotective potential. Fish Shellfish Immunol 31: 182-188.
23. Mchaourab HS, Godar JA, Stewart PL (2009) Structure and mechanism of protein stability sensors: chaperone activity of small heat shock proteins. Biochem 48: 3828-3837.
24. Hilario E, Martin FJM, Bertolini MC, Fan L (2011) Crystal structures of Xanthomonas small heat shock protein provide a structural basis for an active molecular chaperone oligomer. J Mol Biol 408: 74-86.
25. Kennaway CK, Benesch JL, Gohlke U, Wang L, Robinson CV, et al. (2005) Dodecemeric structure of the small heat shock protein Acr1 from Mycobacterium tuberculosis. J Biol Chem 280: 33419-33425.
26. Laganowsky A, Benesch JLP, Landau M, Ding L, Sawaya MR, et al. (2010) Crystal structures of truncated alphaA and alphaB crystallins reveal structural mechanisms of polydispersity important for eye lens function. Protein Sci 19: 1031-1043.
27. Jehle S, Vollmar BS, Bardiaux B, Dove KK, Rajagopal P, et al. (2011) N-terminal domain of αB-crystallin provides a conformational switch for multimerization and structural heterogeneity. Proc Natl Acad Sci USA 108: 6409-6414.
28. Wu Y, MacRae TH (2010) Truncation attenuates molecular chaperoning and apoptosis inhibition by p26, a small heat shock protein from Artemia franciscana. Biochem Cell Biol 88: 937-946.
29. Chen J, Feige MJ, Franzmann TM, Bepperling A, Buchner J (2010) Regions outside the α-crystallin domain of the small heat shock protein Hsp26 are required for its dimerization. J Mol Biol 398: 122-131.
30. Franzmann TM, Wühr M, Richter K, Walter S, Buchner J (2005) The activation mechanism of Hsp26 does not require dissociation of the oligomer. J Mol Biol 350: 1083-1093.
31. Benesch JLP, Ayoub M, Robinson CV, Aquilina JA (2008) Small heat shock protein activity is regulated by variable oligomeric substructure. J Biol Chem 283: 28513-28517.
32. Takeda K, Hayashi T, Abe T, Hirano Y, Hanazono Y, et al. (2011) Dimer structure and conformational variability in the N-terminal region of an archaeal small heat shock protein, StHsp14.0. J Struct Biol 174: 92-99.
33. Ehrnsperger M, Gräber S, Gaestel M, Buchner J (1997) Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J 16: 221-229.
34. Lee GJ, Vierling E (2000) A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiol 122: 189-198.
35. Schlecht R, Erbse AH, Bukau B, Mayer MP (2011) Mechanics of Hsp70 chaperones enables differential interaction with client proteins. Nat Struct Mol Biol 18: 345-351.
36. Marcinowski M, Höller M, Feige MJ, Baerend D, Lamb DC, et al. (2011) Substrate discrimination of the chaperone BiP by autonomous and cochaperone-regulated conformational transitions. Nat Struct Mol Biol 18: 150-158.
37. Bertelsen EB, Chang L, Gestwicki JE, Zuidweg ER (2009) Solution conformation of wild type E. coli Hsp70 (DnaK) chaperone complexed with ADP and substrate. Proc Natl Acad Sci USA 106: 8471-8476.
38. Hartl FU, Hayer-Hartl K (2009) Converging concepts of proteins folding in vitro and in vivo. Nat Struct Mol Biol 16: 574-581.
39. Kabbage M, Dickman MB (2008) The BAG proteins: a ubiquitous family of chaperone regulators. Cell Mol Life Sci 65: 1390-1402.
40. Kampinga HH, Craig EA (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specifcity. Nat Rev Mol Cell Biol 11: 579-592.
41. Young JC (2010) Mechanisms of the Hsp70 chaperone system. Biochem Cell Biol 88: 291-300.
42. Böcking T, Aguet F, Harrison SC, Kirchhausen T (2011) Single-molecule analysis of a molecular disassemblase reveals the mechanism of Hsc70-driven clathrin uncoating. Nat Struct Mol Biol 18: 295-301.
43. Hagn F, Lagleder S, Retzlaff M, Rohrberg J, Demmer O, et al. (2011) Structural analysis of the interaction between Hsp90 and the tumor suppressor protein p53. Nat Struct Mol Biol 18: 1086-1093.
44. Street TO, Lavery LA, Agard DA (2011) Substrate binding drives large-scale conformation changes in the Hsp90 molecular chaperones. Mol Cell 42: 96-105.
45. Park SJ, Borin BN, Martinez-Yamout MA, Dyson HJ (2011) The client protein p53 adopts a molten globule-like state in the presence of Hsp90. Nat Struct Mol Biol 18: 537-541.
46. Pratt WB, Morishima Y, Osawa Y (2008) The Hsp90 chaperone machinery regulates signaling by modulating ligand binding clefts. J Biol Chem 283: 22885-22889.
47. Theodoraki MA, Caplan AJ (2011) Quality control and fate determination of Hsp90 client proteins. Biochim Biophys Acta (in press).
48. Taipale M, Jarosz DF, Lindquist S (2010) Hsp90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11: 515-528.
49. Krukenberg KA, Street TO, Lavery LA, Agard DA (2011) Conformational dynamics of the molecular chaperone Hsp90. Q Rev Biophys 44: 229-255.
50. Onuoha SC, Coulstock ET, Grossman JG, Jackson SE (2008) Structural studies on the co-chaperones Hop and its complexes with Hsp90. J Mol Biol 379: 732-744.
51. Cong Y, Baker ML, Jakana J, Woolford D, Miller EJ, et al. (2010) 4.0Å resolution cryo-EM structure of the mammalian chaperonin TriC/CCT reveals its unique subunit arrangement. Proc Natl Acad Sci USA 107: 4967-4972.
52. Yébenes H, Mesa P, Muňoz IG, Montoya G, Valpuesta JM (2011) Chaperonins: two rings for folding. Trends Biochem Sci 38: 424-432.
53. Speiss C, Miller EJ, McClellan, Frydman J (2006) Indentifcation of the TriC/CCT substrate binding site uncovers the function of subunit diversity in eukaryotic chaperonins. Mol Cell 24: 25-37.
54. Reissmann S, Parnot C, Booth CR, Chiu W, Frydman J (2007) Essential function of the built-in lid in the allosteric regulation of eukaryotic and archaeal chaperonins. Nat Struct Mol Biol 14: 432-440.
55. Pereira JH, Ralston CY, Douglas NR, Meyer D, Knee KM, et al. (2010) Crystal structures of a group II chaperonin reveal the open and closed states associated with the protein folding cycle. J Biol Chem 285: 27958-27966.
56. Douglas N, Reissmann S, Zhang J, Chen B, Jakana J, et al. (2011) Dual action of ATP hydrolysis couples lid closure to substrate release into the group II chaperonin chamber. Cell 144: 240-252.
57. Yam AY, Xia Y, Lin HJ, Burlingame A, Gerstein M, et al. (2008) Defning the TRiC/CCT interactome links chaperonin function to stabilization of newly made proteins with complex topologies. Nat Struct Mol Biol 15: 1255-1262.
58. Brackley KI, Grantham J (2009) Activities of the chaperonin containing TCP-1 (CCT): implications for cell cycle progression and cytoskeletal organisation. Cell Stress Chaperones 14: 23-31.
59. Lee JY, Cho WJ, Do JW, Kim HJ, Park JW, et al. (1996) Monoclonal antibodies raised against infectious haematopoietic necrosis virus (IHNV) G protein and a cellular 90kDa protein neutralize IHNV infection in vitro. J Gen Virol 77: 1731-1737.
60. Deane EE, Woo NYS (2011) Advances and perspectives on the regulation and expression of piscine heat shock proteins. Rev Fish Biol Fisher 21: 153-185.
61. Chen YM, Kuo CE, Wang TY, Shie PS, Wang WC, et al. (2010) Cloning of an orange-spotted grouper Epinephelus coioides heat shock protein 90AB (HSP90AB) and characterization of its expression in response to nodavirus. Fish Shellfish Immunol 28: 895-904.
62. Dong CW, Zhang YB, Zhang QY, Gui JF (2006) Differential expression of three Paralichthys olivaceus Hsp40 genes in responses to virus inflection and heat shock. Fish Shellfish Immunol 21: 146-158.
63. Forsyth RB, Candido PM, Babich SL, Iwama GK (1997) Stress protein expression in coho salmon with Bacterial Kidney Disease. J Aquat Anim Health 9: 18-25.
64. Ackerman A, Iwama GK (2001) Physiological and cellular response of juvenile rainbow trout to vibriosis. J Aquat Anim Health 13: 173-180.
65. Deane EE, Li J, Woo NYS (2004) Modulated heat shock protein expression during pathogenic Vibrio alginolyticus stress of sea bream. Dis Aquat Org 62: 205-215.
66. Wang B, Li F, Dong B, Zhang X, Zhang C, et al. (2006) Discovery of the Genes in Response to White Spot Syndrome Virus (WSSV) Infection in Fenneropenaeus chinensis through cDNA Microarray. Mar Biotechnol 8: 491-500.
67. Liu W, Qian D, Yan X (2011) Proteomic analysis of differentially expressed proteins in hemolymph of Scylla serrata response to white spot syndrome virus infection. Aquaculture 314: 53-57.
68. Cui Z, Liu Y, Luan W, Li Q, Wu D, et al. (2010) Molecular cloning and characterization of a heat shock protein 70 gene in swimming crab (Portunus trituberculatus). Fish Shellfish Immunol 28: 56-64.
69. Rungrassamee W, Leelatanawit R, Jiravanichpaisal P, Klinbunga S, Karoonuthaisiri N (2010) Expression and distribution of three heat shock protein genes under heat shock stress and under exposure to Vibrio harveyi in Penaeus monodon. Dev Comp Immunol 34: 1082-1089.
70. Somboonwiwat K, Chaikeeratisak V, Wang HC, Lo CF, Tassanakajon A (2010) Proteomic analysis of differentially expressed proteins in Penaeus monodon hemocytes after Vibrio harveyi inflection. Proteome Sci 8: 39.
71. Zhou J, Wang L, Xin Y, Wang WN, He WY, et al. (2010) Effect of temperature on antioxidant enzyme gene expression and stress protein response in white shrimp, Litopenaeus vannamei. J Thermal Biol 35: 284-289.
72. Li C, Wang L, Ning X, Chen A, Zhang L, et al. (2010) Identiflcation of two small heat shock proteins with different response profile to cadmium and pathogen stresses in Venerupis philippinarum. Cell Stress Chaperones 15: 897-904.
73. Bao Y, Wang Q, Liu H, Lin Z (2011) A small HSP gene of bloody clam (Tegillarca granosa) involved in the immune response against Vibrio parahaemolyticus and lipopolysaccharide. Fish Shellfsh Immunol 30: 729-733.
74. Zhang L, Wang L, Zhao J, Qiu L, Song L et al. (2009) The responsive expression of heat shock protein 22 gene in zhikong scallop Chlamys farreri against a bacterial challenge. J Aquacult Res 41: 257-266.
75. Li C, Li L, Liu F, Ning X, Chen A, et al. (2011) Alternation of Venerupis philippinarum Hsp40 gene expression in response to pathogen challenge and heavy metal exposure. Fish Shellfish Immunol 30: 447-450.
76. Araya MT, Markham F, Mateo DR, McKenna P, Johnson GR, et al. (2010) Identifcation and expression of immune-related genes in hemocytes of soft-shell clams, Mya arenaria, challenged with Vibrio splendidus. Fish & Shellfish Immunology 29: 557-564.
77. Yue X, Liu B, Sun L, Tang B (2011) Cloning and characterization of a hsp70 gene from Asiatic hard clam Meretrix meretrix which is involved in the immune response against bacterial infection. Fish Shellfish Immunol 30: 791-799.
78. Song L, Wu L, Ni D, Chang Y, Xu W, et al. (2006) The cDNA cloning and mRNA expression of heat shock protein 70 gene in the haemocytes of bay scallop (Argopecten irradians, Lamarck 1819) responding to bacteria challenge and naphthalin stress. Fish Shellfish Immunol 21: 335-345.
79. Puerto M, Campos A, Prieto A, Cameán A, de Almeida AM, et al. (2011) Differential protein expression in two bivalve species; Mytilus galloprovincialis and Corbicula fuminea; exposed to Cylindrospermopsis raciborskii cells. Aquat Toxicol 101: 109-116.
80. Wang PH, Gu ZH, Wan DH, Zhang MY, Weng SP, et al. (2011) The Shrimp NF-κB Pathway Is Activated by White Spot Syndrome Virus (WSSV) 449 to Facilitate the Expression of WSSV069 (ie1), WSSV303 and WSSV371. PLoS ONE 6: e24773.
81. Sung YY, Roberts RJ, Bossier P (2011) Enhancement of Hsp70 synthesis protects common carp Cyprinus carpio L. against lethal ammonia toxicity. J Fish Dis (In press).
82. Sandilands J, Drynan KD, Roberts RJ (2010) Preliminary studies on the enhancement of storage time of chilled milt of Atlantic salmon, Salmo salar L., using an extender containing the TEX-OE heat shock-stimulating factor. Aquaculture Res 41: 568-571.
83. Yan D, Saito K, Ohmi Y, Fujie N, Ohtsuka K (2004) Paeoniforin, a novel heat shock protein-inducing compound. Cell Stress Chaperones 9: 378-389.
84. Westerheide SD, Bosman JD, Mbadugha BNA, Kawahara TLA, Matsumoto G, et al. (2004) Celastrols as Inducers of the Heat Shock Response and Cytoprotection. J Biol Chem 279: 56053-56060.
85. Ip SP, Che CT, Kong YC, Ko KM (2001) Effects of Schisandrin B pretreatment on tumor necrosis factor-a induced apoptosis and Hsp70 expression in mouse liver. Cell Stress Chaperones 6: 44-48.
86. Chiu PY, Ko KM (2004) Schisandrin B protects myocardial ischemia-reperfusion injury partly by inducing Hsp25 and Hsp70 expression in rats. Mol Cell Biochem 266: 139-144.
87. Teiten MH, Eifes S, Reuter S, Duvoix A, Dicato M, et al. (2009) Gene Expression Profling Related to Anti-infammatory Properties of Curcumin in K562 Leukemia Cells. Ann NY Acad Sci 1171: 391-398.
88. Wieten L, Broere F, van der Zee R, Koerkamp EK, Wagenaar J, et al. (2007) Cell stress induced HSP are targets of regulatory T cells: A role for HSP inducing compounds as anti-inflammatory immuno-modulators? FEBS Lett 581: 3716-3722.
89. Baruah K, Ranjan J, Sorgeloos P, MacRae TH, Bossier P (2011) Priming the prophenoloxidase system of Artemia franciscana by heat shock proteins protects against Vibrio campbellii challenge. Fish Shellfish Immunol 31: 134-141.
90. MacAry PA, Javid B, Floto RA, Smith KGC, Oehlmann KGC, et al. (2004) HSP70 peptide binding mutants separate antigen delivery from dendritic cell stimulation. Immunity 20: 95-106.
91. Wang Y, Whittall T, McGowan E, Younson J, Kelly C, et al. (2005) Identification of stimulating and inhibitory epitopes within the heat shock protein 70 molecule that modulate cytokine production and maturation of dendritic cells. J Immunol 174: 3306-3316.
92. de la Vega E, Hall MR, Degnan BM, Wilson KJ (2006) Short-term hyperthermic treatment of Penaeus monodon increases expression of heat shock protein 70 (HSP70) and reduces replication of gill associated virus (GAV). Aquaculture 253: 82-90.
93. Sung YY (2008) Protection of Artemia from vibriosis by heat shock and heat shock proteins. PhD thesis, Ghent University, Belgium. ISBN number: 978-90-5989-224-8.
94. Singh V, Aballay A (2006) Heat-shock and gene activation of HSF-1 enhance immunity to bacteria. Cell cycle 5: 2443-2446.
95. Singh V, Aballay A (2006) Heat-shock transcription factor (HSF)-1 pathway required for Caenorhabditis elegans immunity. Proc Natl Acad Sci USA 103: 13092-13097.
96. Vabulas RM, Ahmad-Nejad P, Ghose S, Kirschning CJ, Issels RD, et al. (2002) HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J Biol Chem 277: 15107-15112.
97. Gobert V, Gottar M, Matskevich AA, Rutschmann S, Royet J, et al. (2003) Dual activation of the Drosophila toll pathway by two pattern recognition receptors. Science 302: 2126-2130.
98. Kulkarni R, Behboudi S, Sharif S (2011) Insights into the role of Toll-like receptors in modulation of T cell responses. Cell Tissue Res 343: 141-152.
99. Yang LS, Yin ZX, Liao JX, Huang XD, Guo CJ, et al. (2007) A Toll receptor in shrimp. Mol Immunol 44: 1999-2008.
100. Arts JAJ, Cornelissen FHJ, Cijsouw T, Hermsen T, Savelkoul HFJ, et al. (2007) Molecular cloning and expression of a Toll-receptor in the giant tiger shrimp, Penaeus monodon. Fish Shellfish Immunol 23: 504-513.
101. Cheng TC (1981) Bivalves. In: N. A. Ratcliffe and A. F. Rowley, Editors, Invertebrate Blood Cells. Academic Press. London. 233-299.
102. Feng SY (1988) Cellular defense mechanisms of oysters and mussels. Am Fish Soc Special Publication 18: 153-168.
103. Fabbri E, Valbonesi P, Franzellitti S (2008) Hsp expression in bivalves. Inv Surv J 5: 135-161.
104. Cellura C, Toubiana M, Parrinello N, Roch P (2007) Specific expression of antimicrobial peptide and HSP70 genes in response to heat-shock and several bacterial challenges in mussels. Fish Shellfish Immunol 22: 340-350.
105. Wang Z, Wu Z, Jian J, Lu Y (2009) Cloning and expression of heat shock protein 70 gene in the haemocytes of pearl oyster (Pinctada fucata, Gould 1850) responding to bacterial challenge. Fish Shellfish Immunol 26: 639-645.
106. Polla BS, Stubbe H, Kantengwa S, Maridonneau-Parini I, Jacquier-Sarlin MR (1995) Differential induction of stress proteins and functional effects of heat shock in human phagocytes. Inflammation 19: 368-378.
107. Zhang A, Zhou X, Wang X, Zhou H (2011) Characterization of two heat shock proteins (Hsp70/Hsc70) from grass carp (Ctenopharyngodon idella): Evidence for their differential gene expression, protein synthesis and secretion in LPS-challenged peripheral blood lymphocytes. Comp Biochem Physiol Part B 159: 109-114.
108. Moseley P (2000) Stress proteins and the immune response. Int Immunopharmacol 48: 299-302.
109. Henderson B, Calderwood SK, Coates ARM, Cohen I, van Eden W, et al. (2010) Caught with their PAMPs down? The extracellular signaling actions of molecular chaperones are not due to microbial contaminants. Cell Stress Chaperones 15: 123-141.
110. Breloer M, Dorner B, More SH, Roderian T, Fleischer B, et al. (2001) Heat shock proteins as "danger signals": eukaryotic Hsp60 enhances and accelerates antigen-specifc IFN-γ production in T cells. Eur J Immunol 31: 2051-2059.
111. Fleshner M, Johnson JD (2005) Exogenous extra-cellular heat shock protein 72: releasing signal(s) and functions. Int J Hyperthermia 21: 457-471.
112. Asea A, Rehli M, Kabingu E, Boch JA, Bare O, et al. (2002) Novel signal transduction pathway utilized by extracellular HSP70: role of Toll-like receptor (TLR) 2 and TLR4. J Biol Chem 277: 15028-15034.
113. Cuellar A, Santander SP, Thomas MDC, Guzman F, Gomez A, et al. (2008) Monocyte-derived dendritic cells from chagasic patients vs healthy donors secrete differential level of IL-10 and IL-12 when stimulated with a protein fragment of Trypanosoma cruzi heat-shock protein 70. Immunol Cell Biol 86: 255-260.
114. Johnson JD, Fleshner M (2006) Releasing signals, secretory pathways, and immune function of endogenous extracellular heat shock protein 72. J Leukoc Biol 79: 425-434.
115. Cuesta A, Esteban MA, Meseguer J (2006) Cloning, distribution and up-regulation of the teleost fsh MHC class II alpha suggests a role for granulocytes as antigen-presenting cells. Mol Immunol 43: 1275-1285.
116. Grisez L, Tan Z (2005) Vaccine development for Asian aquaculture. In P. Walker, R. Lester and M.G. Bondad-Reantaso (eds). Diseases in Asian Aquaculture V, pp. 483-494. Fish Health Section, Asian Fisheries Society, Manila.
117. Plant KP, LaPatra SE, Cain KD (2009) Vaccination of rainbow trout, Oncorhynchus mykiss (Walbaum), with recombinant and DNA vaccines produced to Flavobacterium psychrophilum heat shock proteins 60 and 70. J Fish Dis 32: 521-534.
118. Wilhelm V, Soza C, Martínez R, Rosemblatt M, Burzio LO, et al. (2005) Production and immune response of recombinant Hsp60 and Hsp70 from the salmon pathogen Piscirickettsia salmonis. Biol Res 38: 69-82.
119. Sudheesh PS, LaFrentz BR, Call DR, Siems WF, LaPatra SE, et al. (2007) Identifcation of potential vaccine target antigens by immunoproteomic analysis of a virulent and a non-virulent strain of the fsh pathogen Flavobacterium psychrophilum. Dis Aquat Org 74: 37-47.
120. Rasoli M, Omar AR, Aini I, Jalilian B, Syed Hassan SH, et al. (2010) Fusion of Hsp70 gene of Mycobacterium tuberculosis to hemagglutinin (H5) gene of avian infuenza virus in DNA vaccine enhances its potency. Acta Virol 54: 33-39.
121. Suzue K, Young RA (1996) Adjuvant-free hsp70 fusion protein system elicits humoral and cellular immune responses to HIV-1 p24. J Immunol 156: 873-879.
122. Gagné, Nellie. Novel recombinant vaccine models against Infectious Salmon Anemia Virus (ISA). 2009. 27 October 2011s