Extracellular HSP27 mediates angiogenesis through Toll-like receptor 3

FASEB Journal

Volumn 27, Issue 10, 2013, Pages 4169-4183

  Thuringer, Dominique ^a   Jego, Gaetan ^a   Wettstein, Guillaume ^a   Terrier, Olivier ^b   Cronier, Laurent ^c   Yousfi, Nadhir ^a   Hébrard, Sophie ^a   Bouchot, André ^a   Hazoumé, Adonis ^a   Joly, Anne Laure ^a   Gleave, Martin ^d   Rosa Calatrava, Manuel ^b   Solary, Eric ^e   Garrido, Carmen ^a,f  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b UNIVERSITÉ DE LYON   (France)

^c UNIVERSITÉ DE POITIERS   (France)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e INSTITUT GUSTAVE ROUSSY   (France)

^f DIJON UNIVERSITY HOSPITAL   (France)

Author keywords

Autocrine VEGFR2 activation; Chorioallantoic membrane; Endocytosis; Microvascular endothelial cell; NF B pathway; Tubulogenesis; VEGF release

Indexed keywords

CALCIUM ION; EPIDERMAL GROWTH FACTOR RECEPTOR; I KAPPA B; INTERLEUKIN 8; RECOMBINANT HUMAN HEAT SHOCK PROTEIN 27; RECOMBINANT PROTEIN; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 2; CALCIUM; HEAT SHOCK PROTEIN 27; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TLR3 PROTEIN, HUMAN; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ANGIOGENESIS; ARTICLE; CELL INVASION; CELL MEMBRANE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENDOCYTOSIS; ENZYME ACTIVATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MICROVASCULAR ENDOTHELIAL CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; TUMOR SPHEROID; ANIMAL; CELL CULTURE; DRUG EFFECTS; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

ANIMALS; CALCIUM; CELLS, CULTURED; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HSP27 HEAT-SHOCK PROTEINS; NEOVASCULARIZATION, PHYSIOLOGIC; NF-KAPPA B; TOLL-LIKE RECEPTOR 3; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84885135776     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-226977     Document Type: Article

References (43)

1. Bruey, J. M., Ducasse, C, Bonniaud, P., Ravagnan, L., Susin, S. A., Arrigo, A. P., Kroemer, G, Solary, E., and Garrido, C. (2000) Hsp27 negatively regulates cell death by interacting with cytochrome c. Nat. Cell Biol. 2, 645-652
2. Garrido, C., Brunet, M., Didelot, C., Zermati, Y, Schmitt, E., and Kroemer, G. (2006) Heat shock proteins 27 and 70: antiapoptotic proteins with tumorigenic properties. Cell Cycle 5, 2592-2601
3. Didelot, C., Schmitt, E., Brunet, M., Maingret, L., Parcellier, A, and Garrido, C. (2006) Heat shock proteins: endogenous modulators of apoptotic cell death. Handb. Exp. Pharmacol. 171-198
4. Jego, G, Hazoume, A, Seigneuric, R., and Garrido, C. (2010) Targeting heat shock proteins in cancer. Cancer Lett. 332, 275-285
5. Fanelli, M. A, Cuello Carrion, F. D., Dekker, J., Schoemaker, J., and Ciocca, D. R. (1998) Serological detection of heat shock protein hsp27 in normal and breast cancer patients. Cancer Epidemiol. Biomarkers Prev. 7, 791-795
6. Feng, J. T., Liu, Y. K, Song, H. Y, Dai, Z., Qin, L. X., Almofti, M. R., Lu, H. J., Yang, P. Y, and Tang, Z. Y. (2005) Heat-shock protein 27: a potential biomarker for hepatocellular carcinoma identified by serum proteome analysis. Proteomics 5, 4581-4588
7. De, A. K, Kodys, K. M., Yeh, B. S., and Miller-Graziano, C. (2000) Exaggerated human monocyte IL-10 concomitant to minimal TNF-a induction by heat-shock protein 27 (Hsp27) suggests Hsp27 is primarily an antiinflammatory stimulus. J. Immunol. 165, 3951-3958
8. Banerjee, S., Lin, C. F., Skinner, K. A, Schiffhauer, L. M., Peacock, J., Morrow, D., Huston, A, Shayne, M., Langstein, H. N., Miller-Graziano, C. L., Strickland, J., O'Donoghue, L., and De, A. K (2011) Heat shock protein 27 differentiates tolerogenic macrophages that may support human breast cancer progression. Cancer Res. 71, 318-327
9. Ferrara, N. (2009) Vascular endothelial growth factor. Arterioscler. Thromb. Vasc. Biol. 29, 789-791
10. Ferrara, N., Gerber, H. P., and Le Couter, J. (2003) The biology of VEGF and its receptors. Nat. Med. 9, 669-676
11. Crawford, Y., and Ferrara, N. (2009) VEGF inhibition: insights from preclinical and clinical studies. Cell Tissue Res. 335, 261-269
12. Rousseau, S., Houle, F., and Huot, J. (2000) Integrating the VEGF signals leading to actin-based motility in vascular endothelial cells. Trends Cardiovasc. Med. 10, 321-327
13. Kelly, R. J., and Rixe, O. (2009) Axitinib-a selective inhibitor of the vascular endothelial growth factor (VEGF) receptor. Target Oncol. 4, 297-305
14. Soker, S., Takashima, S., Miao, H. Q., Neufeld, G, and Klagsbrun, M. (1998) Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92, 735-745
15. Kawamura, H., Li, X., Goishi, K, Van Meeteren, L. A, Jakobsson, L., Cebe-Suarez, S., Ballmer-Hofer, K, Kjellen, L., Klagsbrun, M., and Claesson-Welsh, L. (2008) Neuropilin-1 in regulation of VEGF-induced activation of p38MAPK and endothelial cell organization. Blood 112, 3638-3649
16. Kawamura, H., Li, X., Harper, S. J., Bates, D. O., and Claesson-Welsh, L. (2008) Vascular endothelial growth factor (VEGF) - A165b is a weak in vitro agonist for VEGF receptor-2 due to lack of coreceptor binding and deficient regulation of kinase activity. Cancer Res. 68, 4683-4692
17. Doukas, J., Cutler, A. H., and Mordes, J. P. (1994) Polyinosinic: polycytidylic acid is a potent activator of endothelial cells. Am. J. Pathol. 145, 137-147
18. Fischer, S., Gerriets, T., Wessels, C., Walberer, M., Stolz, E., Zheleva, K, Hocke, A, Hippenstiel, S., and Preissner, K. T. (2007) Extracellular RNA mediates endothelial-cell permeability via vascular endothelial growth factor. Blood 110, 2457-2465
19. Fischer, S., Nishio, M., Peters, S. C., Tschernatsch, M., Weidemann, S., Heidenreich, R, Couraud, P. O., Weksler, B. B., Romero, I. A, Gerriets, T., and Preissner, K. T. (2009) Signaling mechanism of extracellular RNA in endothelial cells. FASEBJ. 23, 2100-2109
20. Paone, A, Galli, R, Gabellini, C., Lukashev, D., Starace, D., Gorlach, A, De Cesaris, P., Del Bufalo, D., Sitkovsky, M. V., Filippini, A, and Riccioli, A. (2010) Toll-like receptor 3 regulates angiogenesis and apoptosis in prostate cancer cell lines through hypoxia-inducible factor 1 alpha. Neoplasia 12, 539-549
21. Moon, S. J., Park, M. K, Oh, H. J., Lee, S. Y, Kwok, S. K, Cho, M. L., Ju, J. H., Kim, H. Y, and Park, S. H. (2010) Engagement of Toll-like receptor 3 induces vascular endothelial growth factor and interleukin-8 in human rheumatoid synovial fibroblasts. Korean J. Intern. Med. 25, 429-435
22. Koff, J. L., Shao, M. X., Ueki, I. F., and Nadel, J. A. (2008) Multiple TLRs activate EGFR via a signaling cascade to produce innate immune responses in airway epithelium. Am. J. Physiol. Lung Cell. Mol. Physiol. 294, L1068-L1075
23. Kleinman, M. E., Yamada, K, Takeda, A, Chandrasekaran, V., Nozaki, M., Baffi, J. Z., Yamasaki, S., Itaya, M., Pan, Y, Appukuttan, B., Gibbs, D., Yang, Z., Kariko, K, Ambati, B. K, Wilgus, T. A, Di Pietro, L. A, Sakurai, E., Zhang, K, Smith, J. R, Taylor, E. W., and Ambati, J. (2008) Sequenceand target-independent angiogenesis suppression by siRNA via TLR3. Nature 452, 591-597
24. Cho, W. G, Albuquerque, R. J., Kleinman, M. E., Tarallo, V., Greco, A, Nozaki, M., Ambati, B. K, De Falco, M., Alexander, J. S., Brunetti, A, De Falco, S., and Ambati, J. (2009) Small interfering RNA-induced TLR3 activation inhibits blood and lymphatic vessel growth. Proc. Natl. Acad. Sci. U. S. A. 106, 7137-7142
25. Salaun, B., Zitvogel, L., Asselin-Paturel, C., Morel, Y., Massacrier, C., Conforti, R, Chenard, M. P., Sabourin, J. C., Goubar, A, Lebecque, S., Pierres, M., Rimoldi, D., Romero, P., and Andre, F. (2011) TLR3 as a biomarker for the therapeutic efficacy of double-stranded RNA in breast cancer. Cancer Res. 71, 1607-1614
26. Pierce, J. W., Schoenleber, R, Jesmok, G, Best, J., Moore, S. A, Collins, T., and Gerritsen, M. E. (1997) Novel inhibitors of cytokine-induced IκBcα phosphorylation and endothelial cell adhesion molecule expression show anti-inflammatory effects in vivo. J. Biol. Chem. 272, 21096-21103
27. Vercammen, E., Staal, J., and Beyaert, R. (2008) Sensing of viral infection and activation of innate immunity by Toll-like receptor 3. Clin. Microbiol. Rev. 21, 13-25
28. Goutagny, N., Estornes, Y, Hasan, U., Lebecque, S., and Caux, C. (2012) Targeting pattern recognition receptors in cancer immunotherapy. Target Oncol. 7, 29-54
29. Grote, K, Schutt, H., and Schieffer, B. (2011) Toll-like receptors in angiogenesis. Scientific World J. 11, 981-991
30. Yamashita, M., Chattopadhyay, S., Fensterl, V., Zhang, Y., Sen, G. C. (2012) A TRIF-independent branch of TLR3 signaling. J. Immunol. 188, 2825-2833
31. Kim, Y. M., Brinkmann, M. M., Paquet, M. E., Ploegh, H. L. (2008) UNC93B1 delivers nucleotide-sensing toll-like receptors to endolysosomes. Nature 452, 234-239
32. Pohar, J., Pirher, N., Bencina, M., Mancek-Keber, M., Jerala, R. (2013) The role of UNC93B1 protein in surface localisation of TLR3 receptor and in cell priming to nucleic acid agonists. J. Biol. Chem. 288, 442-454
33. Wang, Y., Liu, L., Davies, D. R., and Segal, D. M. (2010) Dimerization of Toll-like receptor 3 (TLR3) is required for ligand binding. J. Biol. Chem. 285, 36836-36841
34. Piotrowicz, R. S., Hickey, E., and Levin, E. G. (1998) Heat shock protein 27 kDa expression and phosphorylation regulates endothelial cell migration. FASEB J. 12, 1481-1490
35. Evans, I. M., Britton, G., and Zachary, I. C. (2008) Vascular endothelial growth factor induces heat shock protein (HSP) 27 serine 82 phosphorylation and endothelial tubulogenesis via protein kinase D and independent of p38 kinase. Cell Signal. 20, 1375-1384
36. Winston, W. M., Sutherlin, M., Wright, A. J., Feinberg, E. H., and Hunter, C. P. (2007) Caenorhabditis elegans SID-2 is required for environmental RNA interference. Proc. Natl. Acad. Sci. U. S. A. 104, 10565-10570
37. Martin, D., Galisteo, R., and Gutkind, J. S. (2009) CXCL8/IL8 stimulates vascular endothelial growth factor (VEGF) expression and the autocrine activation of VEGFR2 in endothelial cells by activating NF-kB through the CBM (Carma3/Bcl10/Malt1) complex. J. Biol. Chem. 284, 6038-6042
38. Waugh, D. J., and Wilson, C. (2008) The interleukin-8 pathway in cancer. Clin. Cancer Res. 14, 6735-6741
39. Heidemann, J., Ogawa, H., Dwinell, M. B., Rafiee, P., Otterson, M. F., Ota, D. M., Lugering, N., Domschke, W., and Binion, D. G. (2003) Angiogenic effects of interleukin 8 (CXCL8) in human intestinal microvascular endothelial cells are mediated by CXCR2. J. Biol. Chem. 278, 8508-8515
40. Schraufstatter, I. U., Chung, J., and Burger, M. (2001) IL-8 activates endothelial cell CXCR1 and CXCR2 through Rho and Rac signaling pathways. Am. J. Physiol. Lung Cell. Mol. Physiol. 280, L1094-L1103
41. Kampinga, H. H., and Garrido, C. (2012) HSPs: Small proteins with big implications in human diseases. Int. J. Biochem. Cell Biol. 44, 1706-1710
42. Ghayour-Mobarhan, M., Saber, H., Ferns, G. A. A. (2012) The potential role of heat shock protein 27 in cardiovascular diseases. Clin. Chim. Acta 413, 15-24
43. Durupt, F., Koppers-Lalic, D., Balme, B., Budel, L., Lina, B., Thomas, L., Hoeben, R. C., Rosa-Calatrava, M. (2012) The chicken chorioallantoic membrane tumor assay as model for qualitative testing of oncolytic adenoviruses. Cancer Gene Ther. 19, 58-68