Leukocyte HMGB1 is required for vessel remodeling in regenerating muscles

Journal of Immunology

Volumn 192, Issue 11, 2014, Pages 5257-5264

  Campana, Lara ^a   Santarella, Francesco ^a   Esposito, Antonio ^a,b   Maugeri, Norma ^a   Rigamonti, Elena ^a   Monno, Antonella ^a   Canu, Tamara ^a   Del Maschio, Alessandro ^a,b   Bianchi, Marco E ^a   Manfredi, Angelo A ^a,b   Rovere Querini, Patrizia ^a,b  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN 2; HIGH MOBILITY GROUP B1 PROTEIN; MYOD PROTEIN; MYOGENIN; SOMATOMEDIN C; TRANSCRIPTION FACTOR PAX7;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EDEMA; FETUS LIVER; HEMATOPOIETIC SYSTEM; HYPOXIA; LEUKOCYTE; LIVER TRANSPLANTATION; MACROPHAGE; MOUSE; MOUSE MODEL; MUSCLE INJURY; MUSCLE NECROSIS; MUSCLE REGENERATION; NONHUMAN; PRIORITY JOURNAL; SATELLITE CELL;

ANGIOPOIETIN-2; ANIMALS; HMGB1 PROTEIN; LEUKOCYTES; MICE; MICE, KNOCKOUT; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; REGENERATION;

EID: 84901249389     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300938     Document Type: Article

References (47)

1. Chargé, S. B., and M. A. Rudnicki. 2004. Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84: 209-238.
2. Le Grand, F., and M. A. Rudnicki. 2007. Skeletal muscle satellite cells and adult myogenesis. Curr. Opin. Cell Biol. 19: 628-633.
3. Wagers, A. J., and I. M. Conboy. 2005. Cellular and molecular signatures of muscle regeneration: current concepts and controversies in adult myogenesis. Cell 122: 659-667.
4. Deng, B., M. Wehling-Henricks, S. A. Villalta, Y. Wang, and J. G. Tidball. 2012. IL-10 triggers changes in macrophage phenotype that promote muscle growth and regeneration. J. Immunol. 189: 3669-3680.
5. Kharraz, Y., J. Guerra, C. J. Mann, A. L. Serrano, and P. Muñoz-Cánoves. 2013. Macrophage plasticity and the role of inflammation in skeletal muscle repair. Mediators Inflamm. 2013: 491497.
6. Saclier, M., S. Cuvellier, M. Magnan, R. Mounier, and B. Chazaud. 2013. Monocyte/macrophage interactions with myogenic precursor cells during skeletal muscle regeneration. FEBS J. 280: 4118-4130.
7. Heredia, J. E., L. Mukundan, F. M. Chen, A. A. Mueller, R. C. Deo, R. M. Locksley, T. A. Rando, and A. Chawla. 2013. Type 2 innate signals stimulate fibro/adipogenic progenitors to facilitate muscle regeneration. Cell 153: 376-388.
8. Scaffidi, P., T. Misteli, and M. E. Bianchi. 2002. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418: 191-195.
9. Gardella, S., C. Andrei, D. Ferrera, L. V. Lotti, M. R. Torrisi, M. E. Bianchi, and A. Rubartelli. 2002. The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep. 3: 995-1001.
10. Bianchi, M. E., and A. A. Manfredi. 2007. High-mobility group box 1 (HMGB1) protein at the crossroads between innate and adaptive immunity. Immunol. Rev. 220: 35-46.
11. Lu, B., T. Nakamura, K. Inouye, J. Li, Y. Tang, P. Lundbäck, S. I. Valdes-Ferrer, P. S. Olofsson, T. Kalb, J. Roth, et al. 2012. Novel role of PKR in inflammasome activation and HMGB1 release. Nature 488: 670-674.
12. Bianchi, M. E. 2009. HMGB1 loves company. J. Leukoc. Biol. 86: 573-576.
13. Campana, L., L. Bosurgi, M. E. Bianchi, A. A. Manfredi, and P. Rovere-Querini. 2009. Requirement of HMGB1 for stromal cell-derived factor-1/CXCL12-dependent migration of macrophages and dendritic cells. J. Leukoc. Biol. 86: 609-615.
14. Venereau, E., M. Casalgrandi, M. Schiraldi, D. J. Antoine, A. Cattaneo, F. De Marchis, J. Liu, A. Antonelli, A. Preti, L. Raeli, et al. 2012. Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J. Exp. Med. 209: 1519-1528.
15. Yang, H., P. Lundbäck, L. Ottosson, H. Erlandsson-Harris, E. Venereau, M. E. Bianchi, Y. Al-Abed, U. Andersson, K. J. Tracey, and D. J. Antoine. 2012. Redox modification of cysteine residues regulates the cytokine activity of high mobility group box-1 (HMGB1). Mol. Med. 18: 250-259.
16. Yang, H., D. J. Antoine, U. Andersson, and K. J. Tracey. 2013. The many faces of HMGB1: molecular structure-functional activity in inflammation, apoptosis, and chemotaxis. J. Leukoc. Biol. 93: 865-873.
17. Pisetsky, D. S. 2013. The translocation of nuclear molecules during inflammation and cell death. Antioxid. Redox Signal. 20: 1117-1125.
18. Janko, C., M. Filipovic, L. E. Munoz, C. Schorn, G. Schett, I. Ivanovic-Burmazovic, and M. Herrmann. 2014. Redox modulation of HMGB1-related signaling. Antioxid. Redox Signal. 20: 1075-1085.
19. Vezzoli, M., P. Castellani, L. Campana, G. Corna, L. Bosurgi, A. A. Manfredi, M. E. Bianchi, A. Rubartelli, and P. Rovere-Querini. 2010. Redox remodeling: a candidate regulator of HMGB1 function in injured skeletal muscle. Ann. N. Y. Acad. Sci. 1209: 83-90.
20. Bonaldi, T., F. Talamo, P. Scaffidi, D. Ferrera, A. Porto, A. Bachi, A. Rubartelli, A. Agresti, and M. E. Bianchi. 2003. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J. 22: 5551-5560.
21. Vezzoli, M., P. Castellani, G. Corna, A. Castiglioni, L. Bosurgi, A. Monno, S. Brunelli, A. A. Manfredi, A. Rubartelli, and P. Rovere-Querini. 2011. Highmobility group box 1 release and redox regulation accompany regeneration and remodeling of skeletal muscle. Antioxid. Redox Signal. 15: 2161-2174.
22. Calogero, S., F. Grassi, A. Aguzzi, T. Voigtländer, P. Ferrier, S. Ferrari, and M. E. Bianchi. 1999. The lack of chromosomal protein Hmg1 does not disrupt cell growth but causes lethal hypoglycaemia in newborn mice. Nat. Genet. 22: 276-280.
23. Esposito, A., L. Campana, A. Palmisano, F. De Cobelli, T. Canu, F. Santarella, C. Colantoni, A. Monno, M. Vezzoli, G. Pezzetti, et al. 2013. Magnetic resonance imaging at 7T reveals common events in age-related sarcopenia and in the homeostatic response to muscle sterile injury. PLoS ONE 8: e59308.
24. Bosurgi, L., G. Corna, M. Vezzoli, T. Touvier, G. Cossu, A. A. Manfredi, S. Brunelli, and P. Rovere-Querini. 2012. Transplanted mesoangioblasts require macrophage IL-10 for survival in a mouse model of muscle injury. J. Immunol. 188: 6267-6277.
25. Rigamonti, E., T. Touvier, E. Clementi, A. A. Manfredi, S. Brunelli, and P. Rovere-Querini. 2013. Requirement of inducible nitric oxide synthase for skeletal muscle regeneration after acute damage. J. Immunol. 190: 1767-1777.
26. Bacci, M., A. Capobianco, A. Monno, L. Cottone, F. Di Puppo, B. Camisa, M. Mariani, C. Brignole, M. Ponzoni, S. Ferrari, et al. 2009. Macrophages are alternatively activated in patients with endometriosis and required for growth and vascularization of lesions in a mouse model of disease. Am. J. Pathol. 175: 547-556.
27. Arnold, L., A. Henry, F. Poron, Y. Baba-Amer, N. van Rooijen, A. Plonquet, R. K. Gherardi, and B. Chazaud. 2007. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med. 204: 1057-1069.
28. Brunelli, S., and P. Rovere-Querini. 2008. The immune system and the repair of skeletal muscle. Pharmacol. Res. 58: 117-121.
29. Ahluwalia, A., and A. S. Tarnawski. 2012. Critical role of hypoxia sensor - HIF-1a in VEGF gene activation. Implications for angiogenesis and tissue injury healing. Curr. Med. Chem. 19: 90-97.
30. Mitola, S., M. Belleri, C. Urbinati, D. Coltrini, B. Sparatore, M. Pedrazzi, E. Melloni, and M. Presta. 2006. Cutting edge: extracellular high mobility group box-1 protein is a proangiogenic cytokine. J. Immunol. 176: 12-15.
31. Fiedler, U., and H. G. Augustin. 2006. Angiopoietins: a link between angiogenesis and inflammation. Trends Immunol. 27: 552-558.
32. Yanai, H., A. Matsuda, J. An, R. Koshiba, J. Nishio, H. Negishi, H. Ikushima, T. Onoe, H. Ohdan, N. Yoshida, and T. Taniguchi. 2013. Conditional ablation of HMGB1 in mice reveals its protective function against endotoxemia and bacterial infection. Proc. Natl. Acad. Sci. USA 110: 20699-20704.
33. Yang, D., Q. Chen, H. Yang, K. J. Tracey, M. Bustin, and J. J. Oppenheim. 2007. High mobility group box-1 protein induces the migration and activation of human dendritic cells and acts as an alarmin. J. Leukoc. Biol. 81: 59-66.
34. Tsung, A., R. Sahai, H. Tanaka, A. Nakao, M. P. Fink, M. T. Lotze, H. Yang, J. Li, K. J. Tracey, D. A. Geller, and T. R. Billiar. 2005. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J. Exp. Med. 201: 1135-1143.
35. Wang, H., O. Bloom, M. Zhang, J. M. Vishnubhakat, M. Ombrellino, J. Che, A. Frazier, H. Yang, S. Ivanova, L. Borovikova, et al. 1999. HMG-1 as a late mediator of endotoxin lethality in mice. Science 285: 248-251.
36. Wacker, A., and H. Gerhardt. 2011. Endothelial development taking shape. Curr. Opin. Cell Biol. 23: 676-685.
37. Leslie, J. D., L. Ariza-McNaughton, A. L. Bermange, R. McAdow, S. L. Johnson, and J. Lewis. 2007. Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis. Development 134: 839-844.
38. Abou-Khalil, R., R. Mounier, and B. Chazaud. 2010. Regulation of myogenic stem cell behavior by vessel cells: the "ménage à trois" of satellite cells, periendothelial cells and endothelial cells. Cell Cycle 9: 892-896.
39. Scholz, D., S. Thomas, S. Sass, and T. Podzuweit. 2003. Angiogenesis and myogenesis as two facets of inflammatory post-ischemic tissue regeneration. Mol. Cell. Biochem. 246: 57-67.
40. Chavakis, E., A. Hain, M. Vinci, G. Carmona, M. E. Bianchi, P. Vajkoczy, A. M. Zeiher, T. Chavakis, and S. Dimmeler. 2007. High-mobility group box 1 activates integrin-dependent homing of endothelial progenitor cells. Circ. Res. 100: 204-212.
41. Zhou, X., X. Hu, J. Xie, C. Xu, W. Xu, and H. Jiang. 2012. Exogenous highmobility group box 1 protein injection improves cardiac function after myocardial infarction: involvement of Wnt signaling activation. J. Biomed. Biotechnol. 2012: 743879.
42. Gualtieri, F., C. Marinelli, D. Longo, M. Pugnaghi, P. F. Nichelli, S. Meletti, and G. Biagini. 2013. Hypoxia markers are expressed in interneurons exposed to recurrent seizures. Neuromolecular Med. 15: 133-146.
43. Gupta, P., S. Ghosh, A. Nagarajan, V. S. Mehta, and E. Sen. 2013. b-Defensin-3 negatively regulates TLR4-HMGB1 axis mediated HLA-G expression in IL-1b treated glioma cells. Cell. Signal. 25: 682-689.
44. Tafani, M., L. Schito, L. Pellegrini, L. Villanova, G. Marfe, T. Anwar, R. Rosa, M. Indelicato, M. Fini, B. Pucci, and M. A. Russo. 2011. Hypoxia-increased RAGE and P2X7R expression regulates tumor cell invasion through phosphorylation of Erk1/2 and Akt and nuclear translocation of NF-kappaB. Carcinogenesis 32: 1167-1175.
45. Sodhi, A., S. Montaner, V. Patel, M. Zohar, C. Bais, E. A. Mesri, and J. S. Gutkind. 2000. The Kaposi's sarcoma-associated herpes virus G proteincoupled receptor up-regulates vascular endothelial growth factor expression and secretion through mitogen-activated protein kinase and p38 pathways acting on hypoxia-inducible factor 1alpha. Cancer Res. 60: 4873-4880.
46. Richard, D. E., E. Berra, E. Gothié, D. Roux, and J. Pouysségur. 1999. p42/p44 mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1alpha (HIF-1alpha) and enhance the transcriptional activity of HIF-1. J. Biol. Chem. 274: 32631-32637.
47. Ke, Q., and M. Costa. 2006. Hypoxia-inducible factor-1 (HIF-1). Mol. Pharmacol. 70: 1469-1480.