Osteopontin ablation ameliorates muscular dystrophy by shifting macrophages to a pro-regenerative phenotype

被引:96
作者
Capote, Joana [1 ,3 ]
Kramerova, Irina [1 ]
Martinez, Leonel [1 ]
Vetrone, Sylvia [1 ,8 ]
Barton, Elisabeth R. [6 ,7 ]
Sweeney, H. Lee [5 ,7 ]
Miceli, M. Carrie [2 ,4 ,7 ]
Spencer, Melissa J. [1 ,4 ,7 ]
机构
[1] Univ Calif Los Angeles, David Geffen Sch Med, Dept Neurol, Los Angeles, CA 90095 USA
[2] Univ Calif Los Angeles, David Geffen Sch Med, Dept Microbiol Immunol & Mol Genet, Los Angeles, CA 90095 USA
[3] Univ Calif Los Angeles, Mol Cellular & Integrat Physiol Interdept PhD Pro, Los Angeles, CA 90095 USA
[4] Univ Calif Los Angeles, Ctr Duchenne Muscular Dystrophy, Los Angeles, CA 90095 USA
[5] Univ Florida, Dept Pharmacol & Therapeut, Gainesville, FL 32610 USA
[6] Univ Florida, Dept Appl Physiol & Kinesiol, Gainesville, FL 32611 USA
[7] Univ Florida, Wellstone Muscular Dystrophy Ctr, Gainesville, FL 32610 USA
[8] Whittier Coll, Dept Biol, Whittier, CA 90608 USA
基金
美国国家卫生研究院;
关键词
ACTIVATED MACROPHAGES; MUSCLE FIBROSIS; IN-VITRO; SKELETAL; EXPRESSION; MONOCYTES; POLARIZATION; INFECTION; PATHOLOGY; SEVERITY;
D O I
10.1083/jcb.201510086
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
In the degenerative disease Duchenne muscular dystrophy, inflammatory cells enter muscles in response to repetitive muscle damage. Immune factors are required for muscle regeneration, but chronic inflammation creates a profibrotic milieu that exacerbates disease progression. Osteopontin (OPN) is an immunomodulator highly expressed in dystrophic muscles. Ablation of OPN correlates with reduced fibrosis and improved muscle strength as well as reduced natural killer T (NKT) cell counts. Here, we demonstrate that the improved dystrophic phenotype observed with OPN ablation does not result from reductions in NKT cells. OPN ablation skews macrophage polarization toward a pro-regenerative phenotype by reducing M1 and M2a and increasing M2c subsets. These changes are associated with increased expression of pro-regenerative factors insulin-like growth factor 1, leukemia inhibitory factor, and urokinase-type plasminogen activator. Furthermore, altered macrophage polarization correlated with increases in muscle weight and muscle fiber diameter, resulting in long-term improvements in muscle strength and function in mdx mice. These findings suggest that OPN ablation promotes muscle repair via macrophage secretion of pro-myogenic growth factors.
引用
收藏
页码:275 / 288
页数:14
相关论文
共 62 条
[1]  
Amalfitano A, 1996, MUSCLE NERVE, V19, P1549, DOI 10.1002/(SICI)1097-4598(199612)19:12<1549::AID-MUS4>3.0.CO
[2]  
2-A
[3]   Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis [J].
Arnold, Ludovic ;
Henry, Adeline ;
Poron, Francoise ;
Baba-Amer, Yasmine ;
van Rooijen, Nico ;
Plonquet, Anne ;
Gherardi, Romain K. ;
Chazaud, Benedicte .
JOURNAL OF EXPERIMENTAL MEDICINE, 2007, 204 (05) :1057-1069
[4]   Eta-1 (osteopontin): An early component of type-1 (cell-mediated) immunity [J].
Ashkar, S ;
Weber, GF ;
Panoutsakopoulou, V ;
Sanchirico, ME ;
Jansson, M ;
Zawaideh, S ;
Rittling, SR ;
Denhardt, DT ;
Glimcher, MJ ;
Cantor, H .
SCIENCE, 2000, 287 (5454) :860-864
[5]   DIAPHRAGM DISPLAYS EARLY AND PROGRESSIVE FUNCTIONAL DEFICITS IN DYSFERLIN-DEFICIENT MICE [J].
Barton, Elisabeth R. ;
Wang, Bing Jing ;
Brisson, Becky K. ;
Sweeney, H. Lee .
MUSCLE & NERVE, 2010, 42 (01) :22-29
[6]   Systemic administration of L-arginine benefits mdx skeletal muscle function [J].
Barton, ER ;
Morris, L ;
Kawana, M ;
Bish, LT ;
Toursel, T .
MUSCLE & NERVE, 2005, 32 (06) :751-760
[7]   Muscle-specific expression of insulin-like growth factor I counters muscle decline in mdx mice [J].
Barton, ER ;
Morris, L ;
Musaro, A ;
Rosenthal, N ;
Sweeney, HL .
JOURNAL OF CELL BIOLOGY, 2002, 157 (01) :137-147
[8]  
Bayless KJ, 1998, J CELL SCI, V111, P1165
[9]   Genetic Modifiers of Ambulation in the Cooperative International Neuromuscular Research Group Duchenne Natural History Study [J].
Bello, Luca ;
Kesari, Akanchha ;
Gordish-Dressman, Heather ;
Cnaan, Avital ;
Morgenroth, Lauren P. ;
Punetha, Jaya ;
Duong, Tina ;
Henricson, Erik K. ;
Pegoraro, Elena ;
McDonald, Craig M. ;
Hoffman, Eric P. .
ANNALS OF NEUROLOGY, 2015, 77 (04) :684-696
[10]   The role of the Th2CC chemokine ligand CCL17 in pulmonary fibrosis [J].
Belperio, JA ;
Dy, M ;
Murray, L ;
Burdick, MD ;
Xue, YY ;
Strieter, RM ;
Keane, MP .
JOURNAL OF IMMUNOLOGY, 2004, 173 (07) :4692-4698