Myeloid hypoxia-inducible factor-1α is essential for skeletal muscle regeneration in mice

Journal of Immunology

Volumn 191, Issue 1, 2013, Pages 407-414

  Scheerer, Nina ^a   Dehne, Nathalie ^b   Stockmann, Christian ^a   Swoboda, Sandra ^a   Baba, Hideo A ^c   Neugebauer, Agnes ^a   Johnson, Randall S ^d   Fandrey, Joachim ^a  

^a UNIVERSITY OF DUISBURG ESSEN   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY HOSPITAL ESSEN   (Germany)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 2; HYPOXIA INDUCIBLE FACTOR 1ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BONE MARROW CELL; CELL DEATH; CELL GROWTH; CELL INVASION; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE SILENCING; HYPOXIA; KNOCKOUT MOUSE; MACROPHAGE; MICROENVIRONMENT; MOUSE; MUSCLE INJURY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; SKELETAL MUSCLE REGENERATION; TISSUE REGENERATION;

ANIMALS; DOWN-REGULATION; HINDLIMB; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MUSCLE, SKELETAL; MYELOID CELLS; MYOBLASTS, SKELETAL; REGENERATION; UP-REGULATION; WOUND HEALING;

EID: 84879649706     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103779     Document Type: Article

References (35)

1. -/- mice during impaired skeletal muscle regeneration. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293: R651-R661.
2. Ten Broek, R. W., S. Grefte, and J. W. Von den Hoff. 2010. Regulatory factors and cell populations involved in skeletal muscle regeneration. J. Cell. Physiol. 224: 7-16.
3. Bondesen, B. A., S. T. Mills, K. M. Kegley, and G. K. Pavlath. 2004. The COX-2 pathway is essential during early stages of skeletal muscle regeneration. Am. J. Physiol. Cell Physiol. 287: C475-C483. (Pubitemid 38955239)
4. Chazaud, B., C. Sonnet, P. Lafuste, G. Bassez, A. C. Rimaniol, F. Poron, F. J. Authier, P. A. Dreyfus, and R. K. Gherardi. 2003. Satellite cells attract monocytes and use macrophages as a support to escape apoptosis and enhance muscle growth. J. Cell Biol. 163: 1133-1143. (Pubitemid 37541888)
5. Tidball, J. G., and M. Wehling-Henricks. 2007. Macrophages promote muscle membrane repair and muscle fibre growth and regeneration during modified muscle loading in mice in vivo. J. Physiol. 578: 327-336. (Pubitemid 44971129)
6. Tidball, J. G., and S. A. Villalta. 2010. Regulatory interactions between muscle and the immune system during muscle regeneration. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298: R1173-R1187.
7. 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. (Pubitemid 36331777)
8. Frede, S., U. Berchner-Pfannschmidt, and J. Fandrey. 2007. Regulation of hypoxia-inducible factors during inflammation. Methods Enzymol. 435: 405-419.
9. Jelkmann, W. 2004. Molecular biology of erythropoietin. Intern. Med. 43: 649-659. (Pubitemid 39264162)
10. Semenza, G. L. 2001. HIF-1 and mechanisms of hypoxia sensing. Curr. Opin. Cell Biol. 13: 167-171. (Pubitemid 32209217)
11. Kong, T., M. Scully, C. S. Shelley, and S. P. Colgan. 2007. Identification of Pur alpha as a new hypoxia response factor responsible for coordinated induction of the beta 2 integrin family. J. Immunol. 179: 1934-1941.
12. 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. (Pubitemid 350133524)
13. 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.
14. 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.
15. Stockmann, C., A. Doedens, A. Weidemann, N. Zhang, N. Takeda, J. I. Greenberg, D. A. Cheresh, and R. S. Johnson. 2008. Deletion of vascular endothelial growth factor in myeloid cells accelerates tumorigenesis. Nature 456: 814-818.
16. Crisco, J. J., K. D. Hentel, W. O. Jackson, K. Goehner, and P. Jokl. 1996. Maximal contraction lessens impact response in a muscle contusion model. J. Biomech. 29: 1291-1296. (Pubitemid 26302374)
17. Kerkweg, U., D. Schmitz, and H. de Groot. 2006. Screening for the formation of reactive oxygen species and of NO in muscle tissue and remote organs upon mechanical trauma to the mouse hind limb. Eur. Surg. Res. 38: 83-89. (Pubitemid 43876713)
18. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156-159. (Pubitemid 17064313)
19. Frede, S., C. Stockmann, P. Freitag, and J. Fandrey. 2006. Bacterial lipopolysaccharide induces HIF-1 activation in human monocytes via p44/42 MAPK and NF-kappaB. Biochem. J. 396: 517-527. (Pubitemid 44228166)
20. Richard, D. E., E. Berra, and J. Pouysségur. 1999. Angiogenesis: how a tumor adapts to hypoxia. Biochem. Biophys. Res. Commun. 266: 718-722. (Pubitemid 30042496)
21. Deasy, B. M., J. M. Feduska, T. R. Payne, Y. Li, F. Ambrosio, and J. Huard. 2009. Effect of VEGF on the regenerative capacity of muscle stem cells in dystrophic skeletal muscle. Mol. Ther. 17: 1788-1798.
22. 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 Arch. 459: 93-103.
23. 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.
24. Raes, G., R. Van den Bergh, P. De Baetselier, G. H. Ghassabeh, C. Scotton, M. Locati, A. Mantovani, and S. Sozzani. 2005. Arginase-1 and Ym1 are markers for murine, but not human, alternatively activated myeloid cells. J. Immunol. 174: 6561-, author reply 6561-6562.
25. 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.
26. Tidball, J. G. 2005. Inflammatory processes in muscle injury and repair. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288: R345-R353. (Pubitemid 40129595)
27. Smith, W. L., R. M. Garavito, and D. L. DeWitt. 1996. Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2. J. Biol. Chem. 271: 33157-33160. (Pubitemid 27010118)
28. Shen, W., Y. Li, Y. Tang, J. Cummins, and J. Huard. 2005. NS-398, a cyclooxygenase- 2-specific inhibitor, delays skeletal muscle healing by decreasing regeneration and promoting fibrosis. Am. J. Pathol. 167: 1105-1117. (Pubitemid 41416261)
29. Lee, J. J., M. Natsuizaka, S. Ohashi, G. S. Wong, M. Takaoka, C. Z. Michaylira, D. Budo, J. W. Tobias, M. Kanai, Y. Shirakawa, et al. 2010. Hypoxia activates the cyclooxygenase-2-prostaglandin E synthase axis. Carcinogenesis 31: 427-434.
30. Chu, S. H., D. F. Feng, Y. B. Ma, Z. A. Zhu, H. Zhang, and J. H. Qiu. 2009. Stabilization of hepatocyte growth factor mRNA by hypoxia-inducible factor 1. Mol. Biol. Rep. 36: 1967-1975.
31. Germani, A., A. Di Carlo, A. Mangoni, S. Straino, C. Giacinti, P. Turrini, P. Biglioli, and M. C. Capogrossi. 2003. Vascular endothelial growth factor modulates skeletal myoblast function. Am. J. Pathol. 163: 1417-1428. (Pubitemid 37175089)
32. Sonnet, C., P. Lafuste, L. Arnold, M. Brigitte, F. Poron, F. J. Authier, F. Chrétien, R. K. Gherardi, and B. Chazaud. 2006. Human macrophages rescue myoblasts and myotubes from apoptosis through a set of adhesion molecular systems. J. Cell Sci. 119: 2497-2507. (Pubitemid 44070431)
33. St Pierre, B. A., and J. G. Tidball. 1994. Differential response of macrophage subpopulations to soleus muscle reloading after rat hindlimb suspension. J. Appl. Physiol. 77: 290-297. (Pubitemid 24226148)
34. 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.
35. 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. (Pubitemid 46798150)