Heat shock modulates neutrophil motility in zebrafish

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Lam, Pui Ying ^a   Harvie, Elizabeth A ^a   Huttenlocher, Anna ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70;

ANIMAL CELL; ARTICLE; CELL MOTILITY; CELL TYPE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; EPITHELIUM CELL; HEAT SHOCK; HEAT SHOCK RESPONSE; INNATE IMMUNITY; MACROPHAGE; NEUTROPHIL; NEUTROPHIL COUNT; NONHUMAN; PROTEIN EXPRESSION; STREPTOCOCCUS INFECTION; STREPTOCOCCUS INIAE; ZEBRA FISH;

ANIMALS; CELL MOVEMENT; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HEAT-SHOCK RESPONSE; HSP27 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; IMMUNITY, INNATE; MOLECULAR SEQUENCE DATA; NEUTROPHILS; PHENOTYPE; ZEBRAFISH;

EID: 84893180470     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084436     Document Type: Article

References (67)

1. Reynolds WW, Casterlin ME, Covert JB (1976) Behavioural fever in teleost fishes. Nature 259: 41-42. doi:10.1038/259041a0. PubMed: 1250336.
2. Covert JB, Reynolds WW (1977) Survival value of fever in fish. Nature 267: 43-45. doi:10.1038/267043a0. PubMed: 859637.
3. Gräns A, Rosengren M, Niklasson L, Axelsson M (2012) Behavioural fever boosts the inflammatory response in rainbow trout Oncorhynchus mykiss. J Fish Biol 81: 1111-1117. doi:10.1111/j.1095-8649.2012.03333.x. PubMed: 22880741.
4. Boltaña S, Rey S, Roher N, Vargas R, Huerta M et al. (2013) Behavioural fever is a synergic signal amplifying the innate immune response. Proc Biol Sci 280: 20131381. PubMed: 23843398.
5. Salanova B, Choi M, Rolle S, Wellner M, Scheidereit C et al. (2005) The effect of fever-like temperatures on neutrophil signaling. FASEB J 19: 816-818. PubMed: 15755871.
6. Kettritz R, Choi M, Salanova B, Wellner M, Rolle S et al. (2006) Fever-like temperatures affect neutrophil NF-kappaB signaling, apoptosis, and ANCA-antigen expression. J Am Soc Nephrol 17: 1345-1353. doi:10.1681/ASN. 2005090948. PubMed: 16597688.
7. Dietrich P, Dragatsis I, Xuan S, Zeitlin S, Efstratiadis A (2000) Conditional mutagenesis in mice with heat shock promoter-driven cre transgenes. Mamm Genome 11: 196-205. doi:10.1007/s003350010037. PubMed: 10723724.
8. Shoji W, Sato-Maeda M (2008) Application of heat shock promoter in transgenic zebrafish. Dev Growth Differ 50: 401-406. doi:10.1111/j.1440-169X. 2008.01038.x. PubMed: 18430027.
9. Phelps CB, Brand AH (1998) Ectopic gene expression in Drosophila using GAL4 system. Methods 14: 367-379. doi:10.1006/meth.1998.0592. PubMed: 9608508.
10. Bacaj T, Shaham S (2007) Temporal control of cell-specific transgene expression in Caenorhabditis elegans. Genetics 176: 2651-2655. doi:10.1534/genetics.107.074369. PubMed: 17603102.
11. Davis MW, Morton JJ, Carroll D, Jorgensen EM (2008) Gene activation using FLP recombinase in C. elegans. PLOS Genet 4: e1000028.
12. Colaco CA, Bailey CR, Walker KB, Keeble J (2013) Heat shock proteins: stimulators of innate and acquired immunity. Biomed Res Int 2013: 461230
13. Tsan MF, Gao B (2009) Heat shock proteins and immune system. J Leukoc Biol 85: 905-910. doi:10.1189/jlb.0109005. PubMed: 19276179.
14. Wallin RP, Lundqvist A, Moré SH, von Bonin A, Kiessling R et al. (2002) Heat-shock proteins as activators of the innate immune system. Trends Immunol 23: 130-135. doi:10.1016/S1471-4906(01)02168-8. PubMed: 11864840.
15. Tsan MF, Gao B (2004) Heat shock protein and innate immunity. Cell Mol Immunol 1: 274-279. PubMed: 16225770.
16. Todd DJ, Lee AH, Glimcher LH (2008) The endoplasmic reticulum stress response in immunity and autoimmunity. Nat Rev Immunol 8: 663-674. doi:10.1038/nrc2477. PubMed: 18670423.
17. Costa CZ, da Rosa SE, de Camargo MM (2011) The unfolded protein response: how protein folding became a restrictive aspect for innate immunity and B lymphocytes. Scand J Immunol 73: 436-448. doi:10.1111/j.1365-3083.2010.02504.x. PubMed: 21204902.
18. Meeker ND, Trede NS (2008) Immunology and zebrafish: spawning new models of human disease. Dev Comp Immunol 32: 745-757. doi:10.1016/j.dci.2007.11.011. PubMed: 18222541.
19. Deng Q, Huttenlocher A (2012) Leukocyte migration from a fish eye's view. J Cell Sci 125: 3949-3956. doi:10.1242/jcs.093633. PubMed: 23104739.
20. Kanther M, Rawls JF (2010) Host-microbe interactions in the developing zebrafish. Curr Opin Immunol 22: 10-19. doi:10.1016/j.coi.2010.01.006. PubMed: 20153622.
21. Heiman M, Schaefer A, Gong S, Peterson JD, Day M et al. (2008) A translational profiling approach for the molecular characterization of CNS cell types. Cell 135: 738-748. doi:10.1016/j.cell.2008.10.028. PubMed: 19013281.
22. Doyle JP, Dougherty JD, Heiman M, Schmidt EF, Stevens TR et al. (2008) Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135: 749-762. doi:10.1016/j.cell.2008.10.029. PubMed: 19013282.
23. Harvie EA, Green JM, Neely MN, Huttenlocher A (2013) Innate immune response to Streptococcus iniae infection in zebrafish larvae. Infect Immun 81: 110-121. PubMed: 23090960.
24. Lam PY, Yoo SK, Green JM, Huttenlocher A (2012) The SH2-domain-containing inositol 5-phosphatase (SHIP) limits the motility of neutrophils and their recruitment to wounds in zebrafish. J Cell Sci 125: 4973-4978. doi:10.1242/jcs.106625. PubMed: 22946052.
25. Lam SH, Chua HL, Gong Z, Lam TJ, Sin YM (2004) Development and maturation of the immune system in zebrafish, Danio rerio: a gene expression profiling, in situ hybridization and immunological study. Dev Comp Immunol 28: 9-28. doi:10.1016/S0145-305X(03)00103-4. PubMed: 12962979.
26. Willett CE, Cortes A, Zuasti A, Zapata AG (1999) Early hematopoiesis and developing lymphoid organs in the zebrafish. Dev Dyn 214: 323-336. doi:10.1002/(SICI)1097-0177(199904)214:4. PubMed: 10213388.
27. Lam PY, Huttenlocher A (2013) Interstitial leukocyte migration in vivo. Curr Opin Cell Biol 25: 650-658. doi:10.1016/j.ceb.2013.05.007. PubMed: 23797028.
28. Ndong D, Chen YY, Lin YH, Vaseeharan B, Chen JC (2007) The immune response of tilapia Oreochromis mossambicus and its susceptibility to Streptococcus iniae under stress in low and high temperatures. Fish Shellfish Immunol 22: 686-694. doi:10.1016/j.fsi.2006.08.015. PubMed: 17132470.
29. Nahas GG, Tannieres ML, Lennon JF (1971) Direct measurement of leukocyte motility: effects of pH and temperature. Proc Soc Exp Biol Med 138: 350-352. doi:10.3181/00379727-138-35894. PubMed: 5125534.
30. Deng Q, Sarris M, Bennin DA, Green JM, Herbomel P et al. (2013) Localized bacterial infection induces systemic activation of neutrophils through Cxcr2 signaling in zebrafish. J Leukoc Biol 93: 761-769. doi:10.1189/jlb.1012534. PubMed: 23475575.
31. Yoo SK, Huttenlocher A (2011) Spatiotemporal photolabeling of neutrophil trafficking during inflammation in live zebrafish. J Leukoc Biol 89: 661-667. doi:10.1189/jlb.1010567. PubMed: 21248150.
32. Deng Q, Yoo SK, Cavnar PJ, Green JM, Huttenlocher A (2011) Dual roles for Rac2 in neutrophil motility and active retention in zebrafish hematopoietic tissue. Dev Cell 21: 735-745. doi:10.1016/j.devcel.2011.07.013. PubMed: 22014524.
33. Wu T, Tanguay RM (2006) Antibodies against heat shock proteins in environmental stresses and diseases: friend or foe? Cell Stress Chaperones 11: 1-12. doi:10.1379/CSC-155R.1. PubMed: 16572724.
34. Todryk SM, Gough MJ, Pockley AG (2003) Facets of heat shock protein 70 show immunotherapeutic potential. Immunology 110: 1-9. doi:10.1046/j.1365-2567. 2003.01725.x. PubMed: 12941135.
35. Stocki P, Dickinson AM (2012) The immunosuppressive activity of heat shock protein 70. Autoimmune Dis 2012: 617213
36. Borges TJ, Wieten L, van Herwijnen MJ, Broere F, van der Zee R et al. (2012) The anti-inflammatory mechanisms of Hsp70. Front Immunol 3: 95. PubMed: 22566973.
37. Srivastava P (2002) Roles of heat-shock proteins in innate and adaptive immunity. Nat Rev Immunol 2: 185-194. doi:10.1038/nri749. PubMed: 11913069.
38. Senf SM, Howard TM, Ahn B, Ferreira LF, Judge AR (2013) Loss of the inducible Hsp70 delays the inflammatory response to skeletal muscle injury and severely impairs muscle regeneration. PLOS ONE 8: e62687. doi:10.1371/journal. pone.0062687. PubMed: 23626847.
39. Vinokurov M, Ostrov V, Yurinskaya M, Garbuz D, Murashev A et al. (2012) Recombinant human Hsp70 protects against lipoteichoic acid-induced inflammation manifestations at the cellular and organismal levels. Cell Stress Chaperones 17: 89-101. doi:10.1007/s12192-011-0288-0. PubMed: 21845530.
40. Vidyasagar A, Wilson NA, Djamali A (2012) Heat shock protein 27 (HSP27): biomarker of disease and therapeutic target. Fibrogenesis Tissue Repair 5: 7. doi:10.1186/1755-1536-5-7. PubMed: 22564335.
41. Benndorf R, Hayess K, Ryazantsev S, Wieske M, Behlke J et al. (1994) Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J Biol Chem 269: 20780-20784. PubMed: 8051180.
42. Miron T, Vancompernolle K, Vandekerckhove J, Wilchek M, Geiger B (1991) A 25-kD inhibitor of actin polymerization is a low molecular mass heat shock protein. J Cell Biol 114: 255-261. doi:10.1083/jcb.114.2.255. PubMed: 2071672.
43. Schneider GB, Hamano H, Cooper LF (1998) In vivo evaluation of hsp27 as an inhibitor of actin polymerization: hsp27 limits actin stress fiber and focal adhesion formation after heat shock. J Cell Physiol 177: 575-584. doi:10.1002/(SICI)1097-4652(199812)177:4. PubMed: 10092210.
44. Doshi BM, Hightower LE, Lee J (2009) The role of Hsp27 and actin in the regulation of movement in human cancer cells responding to heat shock. Cell Stress Chaperones 14: 445-457. doi:10.1007/s12192-008-0098-1. PubMed: 19224398.
45. Jog NR, Jala VR, Ward RA, Rane MJ, Haribabu B et al. (2007) Heat shock protein 27 regulates neutrophil chemotaxis and exocytosis through two independent mechanisms. J Immunol 178: 2421-2428. PubMed: 17277149.
46. Mao L, Bryantsev AL, Chechenova MB, Shelden EA (2005) Cloning, characterization, and heat stress-induced redistribution of a protein homologous to human hsp27 in the zebrafish Danio rerio. Exp Cell Res 306: 230-241. doi:10.1016/j.yexcr.2005.02.007. PubMed: 15878347.
47. Tucker NR, Shelden EA (2009) Hsp27 associates with the titin filament system in heat-shocked zebrafish cardiomyocytes. Exp Cell Res 315: 3176-3186. doi:10.1016/j.yexcr.2009.06.030. PubMed: 19580808.
48. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107: 881-891. doi:10.1016/S0092-8674(01) 00611-0. PubMed: 11779464.
49. Richardson CE, Kooistra T, Kim DH (2010) An essential role for XBP-1 in host protection against immune activation in C. elegans. Nature 463: 1092-1095. doi:10.1038/nature08762. PubMed: 20182512.
50. Martinon F, Chen X, Lee AH, Glimcher LH (2010) TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat Immunol 11: 411-418. doi:10.1038/ni.1857. PubMed: 20351694.
51. Kaser A, Lee AH, Franke A, Glickman JN, Zeissig S et al. (2008) XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 134: 743-756. doi:10.1016/j.cell.2008.07.021. PubMed: 18775308.
52. Hu MC, Gong HY, Lin GH, Hu SY, Chen MH et al. (2007) XBP-1, a key regulator of unfolded protein response, activates transcription of IGF1 and Akt phosphorylation in zebrafish embryonic cell line. Biochem Biophys Res Commun 359: 778-783. doi:10.1016/j.bbrc.2007.05.183. PubMed: 17560942.
53. Blechinger SR, Evans TG, Tang PT, Kuwada JY, Warren JT Jr. et al. (2002) The heat-inducible zebrafish hsp70 gene is expressed during normal lens development under non-stress conditions. Mech Dev 112: 213-215. doi:10.1016/S0925-4773(01)00652-9. PubMed: 11850198.
54. Tucker NR, Ustyugov A, Bryantsev AL, Konkel ME, Shelden EA (2009) Hsp27 is persistently expressed in zebrafish skeletal and cardiac muscle tissues but dispensable for their morphogenesis. Cell Stress Chaperones 14: 521-533. doi:10.1007/s12192-009-0105-1. PubMed: 19238587.
55. Kudo K, Xi Y, Wang Y, Song B, Chu E et al. (2010) Translational control analysis by translationally active RNA capture/microarray analysis (TrIP-Chip). Nucleic Acids Res 38: e104. doi:10.1093/nar/gkq024. PubMed: 20123731.
56. Lee CT, Zhong L, Mace TA, Repasky EA (2012) Elevation in body temperature to fever range enhances and prolongs subsequent responsiveness of macrophages to endotoxin challenge. PLOS ONE 7: e30077. doi:10.1371/journal.pone.0030077. PubMed: 22253887.
57. Halloran MC, Sato-Maeda M, Warren JT, Su F, Lele Z et al. (2000) Laser-induced gene expression in specific cells of transgenic zebrafish. Development 127: 1953-1960. PubMed: 10751183.
58. Asakawa K, Kawakami K (2008) Targeted gene expression by the Gal4-UAS system in zebrafish. Dev Growth Differ 50: 391-399. doi:10.1111/j.1440-169X. 2008.01044.x. PubMed: 18482403.
59. Faucherre A, López-Schier H (2011) Delaying Gal4-driven gene expression in the zebrafish with morpholinos and Gal80. PLOS ONE 6: e16587. doi:10.1371/journal.pone.0016587. PubMed: 21298067.
60. Wu YL, Pan X, Mudumana SP, Wang H, Kee PW et al. (2008) Development of a heat shock inducible gfp transgenic zebrafish line by using the zebrafish hsp27 promoter. Gene 408: 85-94. doi:10.1016/j.gene.2007.10.027. PubMed: 18037593.
61. Le Guyader D, Redd MJ, Colucci-Guyon E, Murayama E, Kissa K et al. (2008) Origins and unconventional behavior of neutrophils in developing zebrafish. Blood 111: 132-141. doi:10.1182/blood-2007-06-095398. PubMed: 17875807.
62. Mathias JR, Dodd ME, Walters KB, Yoo SK, Ranheim EA et al. (2009) Characterization of zebrafish larval inflammatory macrophages. Dev Comp Immunol 33: 1212-1217. doi:10.1016/j.dci.2009.07.003. PubMed: 19619578.
63. Kitaguchi T, Kawakami K, Kawahara A (2009) Transcriptional regulation of a myeloid-lineage specific gene lysozyme C during zebrafish myelopoiesis. Mech Dev 126: 314-323. doi:10.1016/j.mod.2009.06.867. PubMed: 19275935.
64. Chen CF, Chu CY, Chen TH, Lee SJ, Shen CN et al. (2011) Establishment of a transgenic zebrafish line for superficial skin ablation and functional validation of apoptosis modulators in vivo. PLOS ONE 6: e20654. doi:10.1371/journal.pone.0020654. PubMed: 21655190.
65. Yoo SK, Freisinger CM, LeBert DC, Huttenlocher A (2012) Early redox, Src family kinase, and calcium signaling integrate wound responses and tissue regeneration in zebrafish. J Cell Biol 199: 225-234. doi:10.1083/jcb.201203154. PubMed: 23045550.
66. Provost E, Rhee J, Leach SD (2007) Viral 2A peptides allow expression of multiple proteins from a single ORF in transgenic zebrafish embryos. Genesis 45: 625-629. doi:10.1002/dvg.20338. PubMed: 17941043.
67. Urasaki A, Morvan G, Kawakami K (2006) Functional dissection of the Tol2 transposable element identified the minimal cis-sequence and a highly repetitive sequence in the subterminal region essential for transposition. Genetics 174: 639-649. doi:10.1534/genetics.106.060244. PubMed: 16959904.