Regulatory T Cells promote myositis and muscle damage in Toxoplasma gondii infection

Journal of Immunology

Volumn 198, Issue 1, 2017, Pages 352-362

  Jin, Richard M ^a   Blair, Sarah J ^a   Warunek, Jordan ^a   Heffner, Reid R ^a   Blader, Ira J ^a   Wohlfert, Elizabeth A ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DISRUPTION; CELL POPULATION; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; HOMEOSTASIS; LYMPHOCYTE FUNCTION; MACROPHAGE; MOUSE; MUSCLE INJURY; MUSCLE REGENERATION; MYOSITIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SKELETAL MUSCLE; TISSUE INJURY; TISSUE REPAIR; TOXOPLASMOSIS; ADOPTIVE TRANSFER; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; FLOW CYTOMETRY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MACROPHAGE ACTIVATION; MICROBIOLOGY; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ADOPTIVE TRANSFER; ANIMALS; CELL DIFFERENTIATION; FEMALE; FLOW CYTOMETRY; LYMPHOCYTE ACTIVATION; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; MYOSITIS; REAL-TIME POLYMERASE CHAIN REACTION; T-LYMPHOCYTES, REGULATORY; TOXOPLASMOSIS;

EID: 85006992182     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1600914     Document Type: Article

References (51)

1. Bosurgi, L., A. A. Manfredi, and P. Rovere-Querini. 2011. Macrophages in injured skeletal muscle: a perpetuum mobile causing and limiting fibrosis, prompting or restricting resolution and regeneration. Front. Immunol. 2: 62.
2. Marino, M., F. Scuderi, C. Provenzano, and E. Bartoccioni. 2011. Skeletal muscle cells: from local inflammatory response to active immunity. Gene Ther. 18: 109-116.
3. Pillon, N. J., P. J. Bilan, L. N. Fink, and A. Klip. 2013. Cross-talk between skeletal muscle and immune cells: muscle-derived mediators and metabolic implications. Am. J. Physiol. Endocrinol. Metab. 304: E453-E465.
4. 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.
5. Wiendl, H., R. Hohlfeld, and B. C. Kieseier. 2005. Immunobiology of muscle: advances in understanding an immunological microenvironment. Trends Immunol. 26: 373-380.
6. Mann, C. J., E. Perdiguero, Y. Kharraz, S. Aguilar, P. Pessina, A. L. Serrano, and P. Muñoz-Cánoves. 2011. Aberrant repair and fibrosis development in skeletal muscle. Skelet. Muscle 1: 21.
7. Rostasy, K. M., J. Schmidt, E. Bahn, T. Pfander, M. Piepkorn, E. Wilichowski, and J. Schulz-Schaeffer. 2008. Distinct inflammatory properties of late-activated macrophages in inflammatory myopathies. Acta Myol. 27: 49-53.
8. Rostasy, K. M., M. Piepkorn, H.-H. Goebel, S. Menck, F. Hanefeld, and W. J. Schulz-Schaeffer. 2004. Monocyte/macrophage differentiation in dermatomyositis and polymyositis. Muscle Nerve 30: 225-230.
9. Watson, N. B., K. M. Schneider, and P. T. Massa. 2015. SHP-1-dependent macrophage differentiation exacerbates virus-induced myositis. J. Immunol. 194: 2796-2809.
10. Rayavarapu, S., W. Coley, T. B. Kinder, and K. Nagaraju. 2013. Idiopathic inflammatory myopathies: pathogenic mechanisms of muscle weakness. Skelet. Muscle 3: 13.
11. Wang, H., D. W. Melton, L. Porter, Z. U. Sarwar, L. M. McManus, and P. K. Shireman. 2014. Altered macrophage phenotype transition impairs skeletal muscle regeneration. Am. J. Pathol. 184: 1167-1184.
12. Burzyn, D., W. Kuswanto, D. Kolodin, J. L. Shadrach, M. Cerletti, Y. Jang, E. Sefik, T. G. Tan, A. J. Wagers, C. Benoist, and D. Mathis. 2013. A special population of regulatory T cells potentiates muscle repair. Cell 155: 1282-1295.
13. Villalta, S. A., W. Rosenthal, L. Martinez, A. Kaur, T. Sparwasser, J. G. Tidball, M. Margeta, M. J. Spencer, and J. A. Bluestone. 2014. Regulatory T cells suppress muscle inflammation and injury in muscular dystrophy. Sci. Transl. Med. 6: 258ra142.
14. Mojumdar, K., F. Liang, C. Giordano, C. Lemaire, G. Danialou, T. Okazaki, J. Bourdon, M. Rafei, J. Galipeau, M. Divangahi, and B. J. Petrof. 2014. Inflammatory monocytes promote progression of Duchenne muscular dystrophy and can be therapeutically targeted via CCR2. EMBO Mol. Med. 6: 1476-1492.
15. Schmidt, J., G. Rakocevic, R. Raju, and M. C. Dalakas. 2004. Upregulated inducible co-stimulator (ICOS) and ICOS-ligand in inclusion body myositis muscle: significance for CD8+ T cell cytotoxicity. Brain 127: 1182-1190.
16. Dalakas, M. C., and R. Hohlfeld. 2003. Polymyositis and dermatomyositis. Lancet 362: 971-982.
17. Frenkel, J. K. 1988. Pathophysiology of toxoplasmosis. Parasitol. Today (Regul. Ed.) 4: 273-278.
18. Sullivan Jr., W. J., and V. Jeffers. 2012. Mechanisms of Toxoplasma gondii persistence and latency. FEMS Microbiol. Rev. 36: 717-733.
19. Suzuki, Y., F. K. Conley, and J. S. Remington. 1989. Importance of endogenous IFN-gamma for prevention of toxoplasmic encephalitis in mice. J. Immunol. 143: 2045-2050.
20. Takács, A. C., I. J. Swierzy, and C. G. K. Lüder. 2012. Interferon-γ restricts Toxoplasma gondii development in murine skeletal muscle cells via nitric oxide production and immunity-related GTPases. PLoS One 7: e45440.
21. Hunter, C. A., and L. D. Sibley. 2012. Modulation of innate immunity by Toxoplasma gondii virulence effectors. Nat. Rev. Microbiol. 10: 766-778.
22. Swierzy, I. J., M. Muhammad, J. Kroll, A. Abelmann, A. M. Tenter, and C. G. K. Lüder. 2014. Toxoplasma gondii within skeletal muscle cells: a critical interplay for food-borne parasite transmission. Int. J. Parasitol. 44: 91-98.
23. Oldenhove, G., N. Bouladoux, E. A. Wohlfert, J. A. Hall, D. Chou, L. Dos Santos, S. O'Brien, R. Blank, E. Lamb, S. Natarajan, et al. 2009. Decrease of Foxp3+ Treg cell number and acquisition of effector cell phenotype during lethal infection. Immunity 31: 772-786.
24. Yap, G., M. Pesin, and A. Sher. 2000. Cutting edge: IL-12 is required for the maintenance of IFN-gamma production in T cells mediating chronic resistance to the intracellular pathogen, Toxoplasma gondii. J. Immunol. 165: 628-631.
25. Gazzinelli, R. T., F. T. Hakim, S. Hieny, G. M. Shearer, and A. Sher. 1991. Synergistic role of CD4+ and CD8+ T lymphocytes in IFN-gamma production and protective immunity induced by an attenuated Toxoplasma gondii vaccine. J. Immunol. 146: 286-292.
26. Sturge, C. R., and F. Yarovinsky. 2014. Complex immune cell interplay in the gamma interferon response during Toxoplasma gondii infection. Infect. Immun. 82: 3090-3097.
27. Munoz, M., O. Liesenfeld, and M. M. Heimesaat. 2011. Immunology of Toxoplasma gondii. Immunol. Rev. 240: 269-285.
28. Honda, H., H. Kimura, and A. Rostami. 1990. Demonstration and phenotypic characterization of resident macrophages in rat skeletal muscle. Immunology 70: 272-277.
29. Benson, A., S. Murray, P. Divakar, N. Burnaevskiy, R. Pifer, J. Forman, and F. Yarovinsky. 2012. Microbial infection-induced expansion of effector T cells overcomes the suppressive effects of regulatory T cells via an IL-2 deprivation mechanism. J. Immunol. 188: 800-810.
30. Hall, A. O., D. P. Beiting, C. Tato, B. John, G. Oldenhove, C. G. Lombana, G. H. Pritchard, J. S. Silver, N. Bouladoux, J. S. Stumhofer, et al. 2012. The cytokines interleukin 27 and interferon-g promote distinct Treg cell populations required to limit infection-induced pathology. Immunity 37: 511-523.
31. Smigiel, K. S., E. Richards, S. Srivastava, K. R. Thomas, J. C. Dudda, K. D. Klonowski, and D. J. Campbell. 2014. CCR7 provides localized access to IL-2 and defines homeostatically distinct regulatory T cell subsets. J. Exp. Med. 211: 121-136.
32. Koch, M. A., K. R. Thomas, N. R. Perdue, K. S. Smigiel, S. Srivastava, and D. J. Campbell. 2012. T-bet(+) Treg cells undergo abortive Th1 cell differentiation due to impaired expression of IL-12 receptor b2. Immunity 37: 501-510.
33. Geissmann, F., S. Jung, and D. R. Littman. 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19: 71-82.
34. Tacke, F., F. Ginhoux, C. Jakubzick, N. van Rooijen, M. Merad, and G. J. Randolph. 2006. Immature monocytes acquire antigens from other cells in the bone marrow and present them to T cells after maturing in the periphery. J. Exp. Med. 203: 583-597.
35. Auffray, C., D. Fogg, M. Garfa, G. Elain, O. Join-Lambert, S. Kayal, S. Sarnacki, A. Cumano, G. Lauvau, and F. Geissmann. 2007. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317: 666-670.
36. Shi, C., and E. G. Pamer. 2011. Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 11: 762-774.
37. 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.
38. Lee, E. J., A. Malik, S. Pokharel, S. Ahmad, B. A. Mir, K. H. Cho, J. Kim, J. C. Kong, D.-M. Lee, K. Y. Chung, et al. 2014. Identification of genes differentially expressed in myogenin knock-down bovine muscle satellite cells during differentiation through RNA sequencing analysis. PLoS One 9: e92447.
39. Nance, J. P., K. M. Vannella, D. Worth, C. David, D. Carter, S. Noor, C. Hubeau, L. Fitz, T. E. Lane, T. A. Wynn, and E. H. Wilson. 2012. Chitinase dependent control of protozoan cyst burden in the brain. PLoS Pathog. 8: e1002990.
40. Vyas, A., S.-K. Kim, N. Giacomini, J. C. Boothroyd, and R. M. Sapolsky. 2007. Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc. Natl. Acad. Sci. USA 104: 6442-6447.
41. Hermes, G., J. W. Ajioka, K. A. Kelly, E. Mui, F. Roberts, K. Kasza, T. Mayr, M. J. Kirisits, R. Wollmann, D. J. P. Ferguson, et al. 2008. Neurological and behavioral abnormalities, ventricular dilatation, altered cellular functions, inflammation, and neuronal injury in brains of mice due to common, persistent, parasitic infection. J. Neuroinflammation 5: 48.
42. Gulinello, M., M. Acquarone, J. H. Kim, D. C. Spray, H. S. Barbosa, R. Sellers, H. B. Tanowitz, and L. M. Weiss. 2010. Acquired infection with Toxoplasma gondii in adult mice results in sensorimotor deficits but normal cognitive behavior despite widespread brain pathology. Microbes Infect. 12: 528-537.
43. Patil, V., Y. Zhao, S. Shah, B. A. Fox, L. M. Rommereim, D. J. Bzik, and G. S. Yap. 2014. Co-existence of classical and alternative activation programs in macrophages responding to Toxoplasma gondii. Int. J. Parasitol. 44: 161-164.
44. Campbell, D. J., and M. A. Koch. 2011. Phenotypical and functional specialization of FOXP3+ regulatory T cells. Nat. Rev. Immunol. 11: 119-130.
45. Koch, M. A., G. Tucker-Heard, N. R. Perdue, J. R. Killebrew, K. B. Urdahl, and D. J. Campbell. 2009. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat. Immunol. 10: 595-602.
46. Couper, K. N., P. A. Lanthier, G. Perona-Wright, L. W. Kummer, W. Chen, S. T. Smiley, M. Mohrs, and L. L. Johnson. 2009. Anti-CD25 antibody-mediated depletion of effector T cell populations enhances susceptibility of mice to acute but not chronic Toxoplasma gondii infection. J. Immunol. 182: 3985-3994.
47. Jankovic, D., M. C. Kullberg, C. G. Feng, R. S. Goldszmid, C. M. Collazo, M. Wilson, T. A. Wynn, M. Kamanaka, R. A. Flavell, and A. Sher. 2007. Conventional T-bet(+)Foxp3(-) Th1 cells are the major source of hostprotective regulatory IL-10 during intracellular protozoan infection. J. Exp. Med. 204: 273-283.
48. + regulatory T cell fate during inflammation in mice. J. Clin. Invest. 121: 4503-4515.
49. Wolf, J. R., R. R. Hirschhorn, and S. M. Steiner. 1992. Growth factor responsiveness: role of MyoD and myogenin. Exp. Cell Res. 202: 105-112.
50. Yang, Z. J. P., D. K. Broz, W. L. Noderer, J. P. Ferreira, K. W. Overton, S. L. Spencer, T. Meyer, S. J. Tapscott, L. D. Attardi, and C. L. Wang. 2015. p53 suppresses muscle differentiation at the myogenin step in response to genotoxic stress. Cell Death Differ. 22: 560-573.
51. Castiglioni, A., G. Corna, E. Rigamonti, V. Basso, M. Vezzoli, A. Monno, A. E. Almada, A. Mondino, A. J. Wagers, A. A. Manfredi, and P. Rovere-Querini. 2015. FOXP3+ T cells recruited to sites of sterile skeletal muscle injury regulate the fate of satellite cells and guide effective tissue regeneration. [Published erratum appears in 2015 PLoS One 10: e0133101]. PLoS One 10: e0128094.