Myeloid HIFs are dispensable for resolution of inflammation during skeletal muscle reg eneration

Journal of Immunology

Volumn 194, Issue 7, 2015, Pages 3389-3399

  Gondin, Julien ^a   Théret, Marine ^b,c,d,e   Duhamel, Guillaume ^a   Pegan, Katarina ^f   Mathieu, Jacques R R ^b,c,d   Peyssonnaux, Carole ^b,c,d   Cuvellier, Sylvain ^b,c,d   Latroche, Claire ^b,c,d   Chazaud, Bénédicte ^b,c,d,e   Bendahan, David ^a   Mounier, Rémi ^b,c,d,e  

^a AIX MARSEILLE UNIVERSITY   (France)

^b INSTITUT COCHIN   (France)

^c CNRS   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e UNIVERSITÉ LYON 1   (France)

^f UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; MESSENGER RNA; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INTRACELLULAR SIGNALING; MACROPHAGE; MALE; MOUSE; MUSCLE REGENERATION; MYOSITIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SKELETAL MUSCLE; ANIMAL; ANOXIA; BONE MARROW CELL; DISEASE MODEL; GENE INACTIVATION; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR IMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PHAGOCYTOSIS; PHYSIOLOGY; REGENERATION; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANOXIA; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; DISEASE MODELS, ANIMAL; GENE KNOCKOUT TECHNIQUES; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INFLAMMATION; MACROPHAGES; MAGNETIC RESONANCE IMAGING; MALE; MICE; MOLECULAR IMAGING; MUSCLE, SKELETAL; MYELOID CELLS; PHAGOCYTOSIS; PHENOTYPE; REGENERATION;

EID: 84925858150     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401420     Document Type: Article

References (56)

1. Nizet, V., and R. S. Johnson. 2009. Interdependence of hypoxic and innate immune responses. Nat. Rev. Immunol. 9: 609-617.
2. Dehne, N., and B. Brüne. 2009. HIF-1 in the inflammatory microenvironment. Exp. Cell Res. 315: 1791-1797.
3. Cane, G., A. Ginouvès, S. Marchetti, R. Buscà, J. Pouysségur, E. Berra, P. Hofman, and V. Vouret-Craviari. 2010. HIF-1alpha mediates the induction of IL-8 and VEGF expression on infection with Afa/Dr diffusely adhering E. coli and promotes EMT-like behaviour. Cell. Microbiol. 12: 640-653.
4. Kempf, V. A., M. Lebiedziejewski, K. Alitalo, J. H. Wälzlein, U. Ehehalt, J. Fiebig, S. Huber, B. Schütt, C. A. Sander, S. Müller, et al. 2005. Activation of hypoxia-inducible factor-1 in bacillary angiomatosis: evidence for a role of hypoxia-inducible factor-1 in bacterial infections. Circulation 111: 1054-1062.
5. Peyssonnaux, C., V. Datta, T. Cramer, A. Doedens, E. A. Theodorakis, R. L. Gallo, N. Hurtado-Ziola, V. Nizet, and R. S. Johnson. 2005. HIF-1alpha expression regulates the bactericidal capacity of phagocytes. J. Clin. Invest. 115: 1806-1815.
6. Patel, N. J., O. Zaborina, L. Wu, Y. Wang, D. J. Wolfgeher, V. Valuckaite, M. J. Ciancio, J. E. Kohler, O. Shevchenko, S. P. Colgan, et al. 2007. Recognition of intestinal epithelial HIF-1alpha activation by Pseudomonas aeruginosa. Am. J. Physiol. Gastrointest. Liver Physiol. 292: G134-G142.
7. Rupp, J., J. Gieffers, M. Klinger, G. van Zandbergen, R. Wrase, M. Maass, W. Solbach, J. Deiwick, and T. Hellwig-Burgel. 2007. Chlamydia pneumoniae directly interferes with HIF-1alpha stabilization in human host cells. Cell. Microbiol. 9: 2181-2191.
8. Cramer, T., Y. Yamanishi, B. E. Clausen, I. Förster, R. Pawlinski, N. Mackman, V. H. Haase, R. Jaenisch, M. Corr, V. Nizet, et al. 2003. HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell 112: 645-657.
9. Blouin, C. C., E. L. Page, G. M. Soucy, and D. E. Richard. 2004. Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1α. Blood 103: 1124-1130.
10. Jung, Y., J. S. Isaacs, S. Lee, J. Trepel, Z. G. Liu, and L. Neckers. 2003. Hypoxia-inducible factor induction by tumour necrosis factor in normoxic cells requires receptor-interacting protein-dependent nuclear factor kappa B activation. Biochem. J. 370: 1011-1017.
11. Nishi, K., T. Oda, S. Takabuchi, S. Oda, K. Fukuda, T. Adachi, G. L. Semenza, K. Shingu, and K. Hirota. 2008. LPS induces hypoxia-inducible factor 1 activation in macrophage-differentiated cells in a reactive oxygen species-dependent manner. Antioxid. Redox Signal. 10: 983-995.
12. Peyssonnaux, C., P. Cejudo-Martin, A. Doedens, A. S. Zinkernagel, R. S. Johnson, and V. Nizet. 2007. Cutting edge: essential role of hypoxia inducible factor-1alpha in development of lipopolysaccharide-induced sepsis. J. Immunol. 178: 7516-7519.
13. Eckle, T., D. Köhler, R. Lehmann, K. El Kasmi, and H. K. Eltzschig. 2008. Hypoxia-inducible factor-1 is central to cardioprotection: a new paradigm for ischemic preconditioning. Circulation 118: 166-175.
14. Morote-Garcia, J. C., P. Rosenberger, N. M. Nivillac, I. R. Coe, and H. K. Eltzschig. 2009. Hypoxia-inducible factor-dependent repression of equilibrative nucleoside transporter 2 attenuates mucosal inflammation during intestinal hypoxia. Gastroenterology 136: 607-618.
15. Rosenberger, P., J. M. Schwab, V. Mirakaj, E. Masekowsky, A. Mager, J. C. Morote-Garcia, K. Unertl, and H. K. Eltzschig. 2009. Hypoxia-inducible factor-dependent induction of netrin-1 dampens inflammation caused by hypoxia. Nat. Immunol. 10: 195-202.
16. Keely, S., L. E. Glover, C. F. MacManus, E. L. Campbell, M. M. Scully, G. T. Furuta, and S. P. Colgan. 2009. Selective induction of integrin beta1 by hypoxia-inducible factor: implications for wound healing. FASEB J. 23: 1338-1346.
17. Moon, R. B., and J. H. Richards. 1973. Determination of intracellular pH by 31P magnetic resonance. J. Biol. Chem. 248: 7276-7278.
18. Halberg, N., T. Khan, M. E. Trujillo, I. Wernstedt-Asterholm, A. D. Attie, S. Sherwani, Z. V. Wang, S. Landskroner-Eiger, S. Dineen, U. J. Magalang, et al. 2009. Hypoxia-inducible factor 1alpha induces fibrosis and insulin resistance in white adipose tissue. Mol. Cell. Biol. 29: 4467-4483.
19. Imtiyaz, H. Z., E. P. Williams, M. M. Hickey, S. A. Patel, A. C. Durham, L. J. Yuan, R. Hammond, P. A. Gimotty, B. Keith, and M. C. Simon. 2010. Hypoxia-inducible factor 2alpha regulates macrophage function in mouse models of acute and tumor inflammation. J. Clin. Invest. 120: 2699-2714.
20. Mosser, D. M., and J. P. Edwards. 2008. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8: 958-969.
21. Lawrence, T., and G. Natoli. 2011. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat. Rev. Immunol. 11: 750-761.
22. 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.
23. 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.
24. Shireman, P. K., V. Contreras-Shannon, O. Ochoa, B. P. Karia, J. E. Michalek, and L. M. McManus. 2007. MCP-1 deficiency causes altered inflammation with impaired skeletal muscle regeneration. J. Leukoc. Biol. 81: 775-785.
25. -/- mice following ischemic injury. Am. J. Physiol. Cell Physiol. 292: C953-C967.
26. -/- mice during impaired skeletal muscle regeneration. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293: R651-R661.
27. Lluís, F., J. Roma, M. Suelves, M. Parra, G. Aniorte, E. Gallardo, I. Illa, L. Rodríguez, S. M. Hughes, P. Carmeliet, et al. 2001. Urokinase-dependent plasminogen activation is required for efficient skeletal muscle regeneration in vivo. Blood 97: 1703-1711.
28. Saclier, M., H. Yacoub-Youssef, A. L. Mackey, L. Arnold, H. Ardjoune, M. Magnan, F. Sailhan, J. Chelly, G. K. Pavlath, R. Mounier, et al. 2013. Differentially activated macrophages orchestrate myogenic precursor cell fate during human skeletal muscle regeneration. Stem Cells 31: 384-396.
29. Varga, T., R. Mounier, P. Gogolak, S. Poliska, B. Chazaud, and L. Nagy. 2013. Tissue LyC6- macrophages are generated in the absence of circulating LyC6-monocytes and Nur77 in a model of muscle regeneration. J. Immunol. 191: 5695-5701.
30. Scheerer, N., N. Dehne, C. Stockmann, S. Swoboda, H. A. Baba, A. Neugebauer, R. S. Johnson, and J. Fandrey. 2013. Myeloid hypoxia-inducible factor-1α is essential for skeletal muscle regeneration in mice. J. Immunol. 191: 407-414.
31. Mounier, R., M. Théret, L. Arnold, S. Cuvellier, L. Bultot, O. Göransson, N. Sanz, A. Ferry, K. Sakamoto, M. Foretz, et al. 2013. AMPKα1 regulates macrophage skewing at the time of resolution of inflammation during skeletal muscle regeneration. Cell Metab. 18: 251-264.
32. Takeda, N., E. L. O'Dea, A. Doedens, J. W. Kim, A. Weidemann, C. Stockmann, M. Asagiri, M. C. Simon, A. Hoffmann, and R. S. Johnson. 2010. Differential activation and antagonistic function of HIF-alpha isoforms in macrophages are essential for NO homeostasis. Genes Dev. 24: 491-501.
33. 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.
34. Heemskerk, A. M., G. J. Strijkers, M. R. Drost, G. S. van Bochove, and K. Nicolay. 2007. Skeletal muscle degeneration and regeneration after femoral artery ligation in mice: monitoring with diffusion MR imaging. Radiology 243: 413-421.
35. Vignaud, A., C. Hourde, F. Medja, O. Agbulut, G. Butler-Browne, and A. Ferry. 2010. Impaired skeletal muscle repair after ischemia-reperfusion injury in mice. J. Biomed. Biotechnol. 2010: 724914.
36. Gondin, J., C. Vilmen, P. J. Cozzone, D. Bendahan, and G. Duhamel. 2014. High-field (11.75T) multimodal MR imaging of exercising hindlimb mouse muscles using a non-invasive combined stimulation and force measurement device. NMR Biomed. 27: 870-879.
37. Schleicher, U., and C. Bogdan. 2009. Generation, culture and flow-cytometric characterization of primary mouse macrophages. Methods Mol. Biol. 531: 203-224.
38. Mathur, S., R. S. Vohra, S. A. Germain, S. Forbes, N. D. Bryant, K. Vandenborne, and G. A. Walter. 2011. Changes in muscle T2 and tissue damage after downhill running in mdx mice. Muscle Nerve 43: 878-886.
39. Van Donkelaar, C. C., L. J. Kretzers, P. H. Bovendeerd, L. M. Lataster, K. Nicolay, J. D. Janssen, and M. R. Drost. 1999. Diffusion tensor imaging in biomechanical studies of skeletal muscle function. J. Anat. 194: 79-88.
40. Heemskerk, A. M., M. R. Drost, G. S. van Bochove, M. F. van Oosterhout, K. Nicolay, and G. J. Strijkers. 2006. DTI-based assessment of ischemia-reperfusion in mouse skeletal muscle. Magn. Reson. Med. 56: 272-281.
41. Martinez, F. O., A. Sica, A. Mantovani, and M. Locati. 2008. Macrophage activation and polarization. Front. Biosci. 13:453-461.
42. Uchida, T., F. Rossignol, M. A. Matthay, R. Mounier, S. Couette, E. Clottes, and C. Clerici. 2004. Prolonged hypoxia differentially regulates hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha expression in lung epithelial cells: implication of natural antisense HIF-1alpha. J. Biol. Chem. 279: 14871-14878.
43. Mounier, R., B. K. Pedersen, and P. Plomgaard. 2010. Muscle-specific expression of hypoxia-inducible factor in human skeletal muscle. Exp. Physiol. 95: 899-907.
44. Werno, C., H. Menrad, A. Weigert, N. Dehne, S. Goerdt, K. Schledzewski, J. Kzhyshkowska, and B. Brüne. 2010. Knockout of HIF-1α in tumor-associated macrophages enhances M2 polarization and attenuates their pro-angiogenic responses. Carcinogenesis 31: 1863-1872.
45. Shirato, K., T. Kizaki, T. Sakurai, J. E. Ogasawara, Y. Ishibashi, T. Iijima, C. Okada, I. Noguchi, K. Imaizumi, N. Taniguchi, and H. Ohno. 2009. Hypoxia-inducible factor-1alpha suppresses the expression of macrophage scavenger receptor 1. Pflugers Archiv. 459:93-103.
46. Fujisaka, S., I. Usui, M. Ikutani, A. Aminuddin, A. Takikawa, K. Tsuneyama, A. Mahmood, N. Goda, Y. Nagai, K. Takatsu, and K. Tobe. 2013. Adipose tissue hypoxia induces inflammatory M1 polarity of macrophages in an HIF-1α-dependent and HIF-1α-independent manner in obese mice. Diabetologia 56: 1403-1412.
47. Anand, R. J., S. C. Gribar, J. Li, J. W. Kohler, M. F. Branca, T. Dubowski, C. P. Sodhi, and D. J. Hackam. 2007. Hypoxia causes an increase in phagocytosis by macrophages in a HIF-1alpha-dependent manner. J. Leukoc. Biol. 82: 1257-1265.
48. Acosta-Iborra, B., A. Elorza, I. M. Olazabal, N. B. Martín-Cofreces, S. Martin-Puig, M. Miró, M. J. Calzada, J. Aragonés, F. Sánchez-Madrid, and M. O. Landázuri. 2009. Macrophage oxygen sensing modulates antigen presentation and phagocytic functions involving IFN-gamma production through the HIF-1 alpha transcription factor. J. Immunol. 182: 3155-3164.
49. Mounier, R., V. Pialoux, B. Roels, C. Thomas, G. Millet, J. Mercier, J. Coudert, N. Fellmann, and E. Clottes. 2009. Effect of intermittent hypoxic training on HIF gene expression in human skeletal muscle and leukocytes. Eur. J. Appl. Physiol. 105: 515-524.
50. Mason, S., and R. S. Johnson. 2007. The role of HIF-1 in hypoxic response in the skeletal muscle. Adv. Exp. Med. Biol. 618: 229-244.
51. Mason, S. D., R. A. Howlett, M. J. Kim, I. M. Olfert, M. C. Hogan, W. McNulty, R. P. Hickey, P. D. Wagner, C. R. Kahn, F. J. Giordano, and R. S. Johnson. 2004. Loss of skeletal muscle HIF-1alpha results in altered exercise endurance. PLoS Biol. 2: e288.
52. Dehne, N., U. Kerkweg, S. B. Flohé, B. Brüne, and J. Fandrey. 2011. Activation of hypoxia-inducible factor 1 in skeletal muscle cells after exposure to damaged muscle cell debris. Shock 35: 632-638.
53. Damon, B. M., Z. Ding, A. W. Anderson, A. S. Freyer, and J. C. Gore. 2002. Validation of diffusion tensor MRI-based muscle fiber tracking. Magn. Reson. Med. 48:97-104.
54. Ye, F., S. Mathur, M. Liu, S. E. Borst, G. A. Walter, H. L. Sweeney, and K. Vandenborne. 2013. Overexpression of insulin-like growth factor-1 attenuates skeletal muscle damage and accelerates muscle regeneration and functional recovery after disuse. Exp. Physiol. 98: 1038-1052.
55. Bryant, N.D., K. Li, M. D. Does, S. Barnes, D. F. Gochberg, T. E. Yankeelov, J. H. Park, and M. B. Damon. 2014. Multi-parametric MRI characterization of inflammation in murine skeletal muscle. NMR in Biomedicine 27: 716-725.
56. Maguire, K. K., L. Lim, S. Speedy, and T. A. Rando. 2013. Assessment of disease activity in muscular dystrophies by noninvasive imaging. J. Clin. Invest. 123: 2298-2305.