High mobility group box 1 inhibits human pulmonary artery endothelial cell migration via a toll-like receptor 4- and interferon response factor 3-dependent mechanism(s)

Journal of Biological Chemistry

Volumn 288, Issue 2, 2013, Pages 1365-1373

  Bauer, Eileen M ^a   Shapiro, Richard ^a   Billiar, Timothy R ^a   Bauer, Philip M ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEINS; ENDOTHELIAL DYSFUNCTION; HIGH-MOBILITY GROUP BOX 1 PROTEINS; HIGH-MOBILITY GROUPS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; INHIBITORY EFFECT; INTERFERON RESPONSE; NEUTRALIZING ANTIBODIES; NUCLEAR TRANSLOCATIONS; PULMONARY ARTERY ENDOTHELIAL CELLS; PULMONARY HYPERTENSION; SIGNALING PATHWAYS; TOLL-LIKE RECEPTOR 4;

ANTIBIOTICS; ANTIBODIES; GLYCOPROTEINS; INTERFERONS;

ENDOTHELIAL CELLS;

HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; MYELOID DIFFERENTIATION FACTOR 88; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 4; VASCULOTROPIN;

ARTICLE; CELL HYPOXIA; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HUMAN PULMONARY ARTERY ENDOTHELIAL CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN TRANSPORT; PULMONARY ARTERY; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL;

BLOTTING, WESTERN; CELL MOVEMENT; CELLS, CULTURED; FLUORESCENT ANTIBODY TECHNIQUE; HMGB1 PROTEIN; HUMANS; INTERFERON REGULATORY FACTOR-3; MYELOID DIFFERENTIATION FACTOR 88; PULMONARY ARTERY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; TOLL-LIKE RECEPTOR 4; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84872298261     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.434142     Document Type: Article

References (48)

1. Evankovich, J., Cho, S. W., Zhang, R., Cardinal, J., Dhupar, R., Zhang, L., Klune, J. R., Zlotnicki, J., Billiar, T., and Tsung, A. (2010) High mobility group box 1 release from hepatocytes during ischemia and reperfusion injury is mediated by decreased histone deacetylase activity. J. Biol. Chem. 285, 39888-39897
2. Park, J. S., Svetkauskaite, D., He, Q., Kim, J. Y., Strassheim, D., Ishizaka, A., and Abraham, E. (2004) Involvement of Toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J. Biol. Chem. 279, 7370-7377 (Pubitemid 38294612)
3. Park, J. S., Gamboni-Robertson, F., He, Q., Svetkauskaite, D., Kim, J. Y., Strassheim, D., Sohn, J. W., Yamada, S., Maruyama, I., Banerjee, A., Ishizaka, A., and Abraham, E. (2006) High mobility group box 1 protein interacts with multiple Toll-like receptors. Am. J. Physiol. Cell Physiol. 290, C917-924
4. Huang, W., Tang, Y., and Li, L. (2010) HMGB1, a potent proinflammatory cytokine in sepsis. Cytokine 51, 119-126
5. Ohmori, H., Luo, Y., and Kuniyasu, H. (2011) Non-histone nuclear factor HMGB1 as a therapeutic target in colorectal cancer. Expert Opin. Ther. Targets 15, 183-193
6. Sachdev, U., Cui, X., Hong, G., Namkoong, S., Karlsson, J. M., Baty, C. J., and Tzeng, E. (2012) High mobility group box 1 promotes endothelial cell angiogenic behavior in vitro and improves muscle perfusion in vivo in response to ischemic injury. J. Vasc. Surg. 55, 180-191
7. Schlueter, C., Weber, H., Meyer, B., Rogalla, P., Röser, K., Hauke, S., and Bullerdiek, J. (2005) Angiogenetic signaling through hypoxia. HMGB1: an angiogenetic switch molecule. Am. J. Pathol. 166, 1259-1263 (Pubitemid 40524448)
8. van Beijnum, J. R., Nowak-Sliwinska, P., van den Boezem, E., Hautvast, P., Buurman, W. A., and Griffioen, A. W. (March 5, 2012) Tumor angiogenesis is enforced by autocrine regulation of high-motility group box 1. Oncogene 10.1038/onc.2012.49
9. Arancibia, S. A., Beltrán, C. J., Aguirre, I. M., Silva, P., Peralta, A. L., Malinarich, F., and Hermoso, M. A. (2007) Toll-like receptors are key participants in innate immune responses. Biol. Res. 40, 97-112
10. Fitzgerald, K. A., and Chen, Z. J. (2006) Sorting out Toll signals. Cell 125, 834-836 (Pubitemid 43795201)
11. McGettrick, A. F., and O'Neill, L. A. (2010) Localisation and trafficking of Toll-like receptors: an important mode of regulation. Curr. Opin. Immunol. 22, 20-27
12. Young, K. C., Hussein, S. M., Dadiz, R., deMello, D., Devia, C., Hehre, D., and Suguihara, C. (2010) Toll-like receptor 4-deficient mice are resistant to chronic hypoxia-induced pulmonary hypertension. Exp. Lung Res. 36, 111-119
13. Poltorak, A., He, X., Smirnova, I., Liu, M. Y., Van Huffel, C., Du, X., Birdwell, D., Alejos, E., Silva, M., Galanos, C., Freudenberg, M., Ricciardi- Castagnoli, P., Layton, B., and Beutler, B. (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282, 2085-2088 (Pubitemid 29001265)
14. Abraham, E., Arcaroli, J., Carmody, A., Wang, H., and Tracey, K. J. (2000) HMG-1 as a mediator of acute lung inflammation. J. Immunol. 165, 2950-2954
15. Angus, D. C., Yang, L., Kong, L., Kellum, J. A., Delude, R. L., Tracey, K. J., and Weissfeld, L. (2007) Circulating high-mobility group box 1 (HMGB1) concentrations are elevated in both uncomplicated pneumonia and pneumonia with severe sepsis. Crit. Care Med. 35, 1061-1067 (Pubitemid 46598956)
16. Gong, Q., Xu, J. F., Yin, H., Liu, S. F., Duan, L. H., and Bian, Z. L. (2009) Protective effect of antagonist of high-mobility group box 1 on lipopolysaccharide-induced acute lung injury in mice. Scand. J. Immunol. 69, 29-35
17. Ogawa, E. N., Ishizaka, A., Tasaka, S., Koh, H., Ueno, H., Amaya, F., Ebina, M., Yamada, S., Funakoshi, Y., Soejima, J., Moriyama, K., Kotani, T., Hashimoto, S., Morisaki, H., Abraham, E., and Takeda, J. (2006) Contribution of high-mobility group box-1 to the development of ventilatorinduced lung injury. Am. J. Respir. Crit. Care Med. 174, 400-407 (Pubitemid 44223120)
18. Reiss, L. K., Uhlig, U., and Uhlig, S. (2012) Models and mechanisms of acute lung injury caused by direct insults. Eur. J. Cell Biol. 91, 590-601
19. Ueno, H., Matsuda, T., Hashimoto, S., Amaya, F., Kitamura, Y., Tanaka, M., Kobayashi, A., Maruyama, I., Yamada, S., Hasegawa, N., Soejima, J., Koh, H., and Ishizaka, A. (2004) Contributions of high mobility group box protein in experimental and clinical acute lung injury. Am. J. Respir. Crit. Care Med. 170, 1310-1316 (Pubitemid 39657195)
20. Yang, H., Ochani, M., Li, J., Qiang, X., Tanovic, M., Harris, H. E., Susarla, S. M., Ulloa, L., Wang, H., DiRaimo, R., Czura, C. J., Wang, H., Roth, J., Warren, H. S., Fink, M. P., Fenton, M. J., Andersson, U., and Tracey, K. J. (2004) Reversing established sepsis with antagonists of endogenous highmobility group box 1. Proc. Natl. Acad. Sci. U.S.A. 101, 296-301 (Pubitemid 38084244)
21. Tsung, A., Klune, J. R., Zhang, X., Jeyabalan, G., Cao, Z., Peng, X., Stolz, D. B., Geller, D. A., Rosengart, M. R., and Billiar, T. R. (2007) HMGB1 release induced by liver ischemia involves Toll-like receptor 4 dependent reactive oxygen species production and calcium-mediated signaling. J. Exp. Med. 204, 2913-2923 (Pubitemid 350179560)
22. Chavakis, E., Hain, A., Vinci, M., Carmona, G., Bianchi, M. E., Vajkoczy, P., Zeiher, A. M., Chavakis, T., and Dimmeler, S. (2007) High-mobility group box 1 activates integrin-dependent homing of endothelial progenitor cells. Circ. Res. 100, 204-212 (Pubitemid 46208720)
23. Schlueter, C., Hauke, S., Loeschke, S., Wenk, H. H., and Bullerdiek, J. (2005) HMGA1 proteins in human atherosclerotic plaques. Pathol. Res. Pract. 201, 101-107 (Pubitemid 40443823)
24. van Beijnum, J. R., Dings, R. P., van der Linden, E., Zwaans, B. M., Ramaekers, F. C., Mayo, K. H., and Griffioen, A. W. (2006) Gene expression of tumor angiogenesis dissected: specific targeting of colon cancer angiogenic vasculature. Blood 108, 2339-2348 (Pubitemid 44497518)
25. Beutler, B. (2000) Tlr4: central component of the sole mammalian LPS sensor. Curr. Opin. Immunol. 12, 20-26
26. Park, J. S., Arcaroli, J., Yum, H. K., Yang, H., Wang, H., Yang, K. Y., Choe, K. H., Strassheim, D., Pitts, T. M., Tracey, K. J., and Abraham, E. (2003) Activation of gene expression in human neutrophils by high mobility group box 1 protein. Am. J. Physiol. Cell Physiol. 284, C870-879 (Pubitemid 36336943)
27. Wang, E., Feng, Y., Zhang, M., Zou, L., Li, Y., Buys, E. S., Huang, P., Brouckaert, P., and Chao, W. (2011) Toll-like receptor 4 signaling confers cardiac protection against ischemic injury via inducible nitric oxide synthaseand soluble guanylate cyclase-dependent mechanisms. Anesthesiology 114, 603-613
28. Tsai, T. H., Chen, S. F., Huang, T. Y., Tzeng, C. F., Chiang, A. S., Kou, Y. R., Lee, T. S., and Shyue, S. K. (2011) Impaired Cd14 and Cd36 expression, bacterial clearance, and Toll-like receptor 4-MyD88 signaling in caveolin-1-deleted macrophages and mice. Shock 35, 92-99
29. DeFilippis, V. R., Robinson, B., Keck, T. M., Hansen, S. G., Nelson, J. A., and Früh, K. J. (2006) Interferon regulatory factor 3 is necessary for induction of antiviral genes during human cytomegalovirus infection. J. Virol. 80, 1032-1037 (Pubitemid 43062914)
30. Doyle, S., Vaidya, S., O'Connell, R., Dadgostar, H., Dempsey, P., Wu, T., Rao, G., Sun, R., Haberland, M., Modlin, R., and Cheng, G. (2002) IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 17, 251-263 (Pubitemid 35279547)
31. Taraseviciene-Stewart, L., Kasahara, Y., Alger, L., Hirth, P.,McMahon, G., Waltenberger, J., Voelkel, N. F., and Tuder, R. M. (2001) Inhibition of the VEGF receptor 2 combined with chronic hypoxia causes cell death-dependent pulmonary endothelial cell proliferation and severe pulmonary hypertension. FASEB J. 15, 427-438 (Pubitemid 32141434)
32. Partovian, C., Adnot, S., Raffestin, B., Louzier, V., Levame, M., Mavier, I. M., Lemarchand, P., and Eddahibi, S. (2000) Adenovirus-mediated lung vascular endothelial growth factor overexpression protects against hypoxic pulmonary hypertension in rats. Am. J. Respir. Cell Mol. Biol. 23, 762-771 (Pubitemid 32013268)
33. Pascaud, M. A., Griscelli, F., Raoul, W., Marcos, E., Opolon, P., Raffestin, B., Perricaudet, M., Adnot, S., and Eddahibi, S. (2003) Lung overexpression of angiostatin aggravates pulmonary hypertension in chronically hypoxic mice. Am. J. Respir. Cell Mol. Biol. 29, 449-457 (Pubitemid 37222682)
34. Kumar, H., Kawai, T., and Akira, S. (2011) Pathogen recognition by the innate immune system. Int. Rev. Immunol. 30, 16-34
35. Matzinger, P. (1994) Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12, 991-1045
36. Bianchi, M. E. (2007) DAMPs, PAMPs, and alarmins: all we need to know about danger. J. Leukoc. Biol. 81, 1-5
37. Klune, J. R., Dhupar, R., Cardinal, J., Billiar, T. R., and Tsung, A. (2008) HMGB1: endogenous danger signaling. Mol. Med. 14, 476-484
38. Hori, O., Brett, J., Slattery, T., Cao, R., Zhang, J., Chen, J. X., Nagashima, M., Lundh, E. R., Vijay, S., and Nitecki, D. (1995) The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin: mediation of neurite outgrowth and co-expression of rage and amphoterin in the developing nervous system. J. Biol. Chem. 270, 25752-25761
39. Tsung, A., Sahai, R., Tanaka, H., Nakao, A., Fink, M. P., Lotze, M. T., Yang, H., Li, J., Tracey, K. J., Geller, D. A., and Billiar, T. R. (2005) The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J. Exp. Med. 201, 1135-1143 (Pubitemid 40524681)
40. Maroso, M., Balosso, S., Ravizza, T., Liu, J., Aronica, E., Iyer, A. M., Rossetti, C., Molteni, M., Casalgrandi, M., Manfredi, A. A., Bianchi, M. E., and Vezzani, A. (2010) Toll-like receptor 4 and high-mobility group box-1 are involved in ictogenesis and can be targeted to reduce seizures. Nat. Med. 16, 413-419
41. Mittal, D., Saccheri, F., Vénéreau, E., Pusterla, T., Bianchi, M. E., and Rescigno, M. (2010) TLR4-mediated skin carcinogenesis is dependent on immune and radioresistant cells. EMBO J. 29, 2242-2252
42. Levy, R. M., Mollen, K. P., Prince, J. M., Kaczorowski, D. J., Vallabhaneni, R., Liu, S., Tracey, K. J., Lotze, M. T., Hackam, D. J., Fink, M. P., Vodovotz, Y., and Billiar, T. R. (2007) Systemic inflammation and remote organ injury following trauma require HMGB1. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R1538-1544 (Pubitemid 47535772)
43. Chen, J., Hartono, J. R., John, R., Bennett, M., Zhou, X. J., Wang, Y., Wu, Q., Winterberg, P. D., Nagami, G. T., and Lu, C. Y. (2011) Early interleukin 6 production by leukocytes during ischemic acute kidney injury is regulated by TLR4. Kidney Int. 80, 504-515
44. Lin, Q., Yang, X. P., Fang, D., Ren, X., Zhou, H., Fang, J., Liu, X., Zhou, S., Wen, F., Yao, X., Wang, J. M., and Su, S. B. (2011) High-mobility group box-1 mediates Toll-like receptor 4-dependent angiogenesis. Arterioscler. Thromb. Vasc. Biol. 31, 1024-1032
45. Nagata, D., Mogi, M., and Walsh, K. (2003) AMP-activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress. J. Biol. Chem. 278, 31000-31006 (Pubitemid 36994613)
46. Zhu, X. Y., Daghini, E., Chade, A. R., Lavi, R., Napoli, C., Lerman, A., and Lerman, L. O. (2008) Disparate effects of simvastatin on angiogenesis during hypoxia and inflammation. Life Sci. 83, 801-809
47. Bianchi, M. E. (2009) HMGB1 loves company. J. Leukoc. Biol. 86, 573-576
48. Ngamkitidechakul, C., and Twining, S. S. (2002) Buffered non-fermenter system for lab-scale production of secreted recombinant His-tagged proteins in Saccharomyces cerevisiae . BioTechniques 33, 1296-1300 (Pubitemid 36008186)