Mesenchymal stem cells alter macrophage immune responses to Leishmania major infection in both susceptible and resistance mice

Immunology Letters

Volumn 170, Issue , 2016, Pages 15-26

  Dameshghi, Safura ^a   Zavaran Hosseini, Ahmad ^a   Soudi, Sara ^a   Shirazi, Fatemeh Jalali ^a   Nojehdehi, Shahrzad ^b   Hashemi, Seyed Mahmoud ^c  

^a TARBIAT MODARES UNIVERSITY   (Iran)

^b STEM CELL TECHNOLOGY RESEARCH CENTER   (Iran)

^c SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Leishmania major; Macrophage; Mesenchymal stem cell; Mouse strain

Indexed keywords

INTERLEUKIN 10; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; CYTOKINE;

ADIPOSE DERIVED MESENCHYMAL STEM CELL; ADIPOSE TISSUE CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSAY; BAGG ALBINO MOUSE; C57BL 6 MOUSE; CELL ISOLATION; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GENE REPRESSION; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; LEISHMANIASIS; MACROPHAGE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PHAGOCYTOSIS; POLARIZATION; PRIORITY JOURNAL; ANIMAL; DISEASE MODEL; DISEASE PREDISPOSITION; DISEASE RESISTANCE; IMMUNOLOGY; IMMUNOPHENOTYPING; LEISHMANIA MAJOR; MESENCHYMAL STROMA CELL; METABOLISM; PARASITOLOGY; PERITONEUM MACROPHAGE; PHENOTYPE; SKIN LEISHMANIASIS;

ANIMALS; COCULTURE TECHNIQUES; CYTOKINES; DISEASE MODELS, ANIMAL; DISEASE RESISTANCE; DISEASE SUSCEPTIBILITY; FEMALE; IMMUNOPHENOTYPING; INFLAMMATION MEDIATORS; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; MACROPHAGES; MACROPHAGES, PERITONEAL; MESENCHYMAL STROMAL CELLS; MICE; NITRIC OXIDE; PHAGOCYTOSIS; PHENOTYPE;

EID: 84952690940     PISSN: 01652478     EISSN: 18790542     Source Type: Journal    
DOI: 10.1016/j.imlet.2015.12.002     Document Type: Article

References (50)

1. Sharma U., Singh S. Immunobiology of leishmaniasis. Indian J. Exp. Biol. 2009, 47:412-423.
2. Laufs H., Müller K., Fleischer J., Jahnke N., Jensenius J.C., Solbach W., et al. Intracellular survival of Leishmania major in neutrophil granulocytes after uptake in the absence of heat-labile serum factors. Society 2002, 70:826-835.
3. Van Zandbergen G., Klinger M., Mueller A., Dannenberg S., Gebert A., Solbach W., et al. Cutting edge: neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. J. Immunol. 2004, 173:6521-6525.
4. Culley F.J., Harris R.A., Kaye P.M., McAdam K.P., Raynes J.G. C-reactive protein binds to a novel ligand on Leishmania donovani and increases uptake into human macrophages. J. Immunol. 1996, 156:4691-4696.
5. Mosser D.M., Edelson P.J. The third component of complement (C3) is responsible for the intracellular survival of Leishmania major. Nature 1987, 327:329-331.
6. Bogdan C., Röllinghoff M. How do protozoan parasites survive inside macrophages?. Parasitol. Today 1999, 15:22-28.
7. Buates S., Matlashewski G. General suppression of macrophage gene expression during Leishmania donovani infection. J. Immunol. 2001, 166:3416-3422.
8. Menezes J.P., Almeida T.F., Petersen A.L., Guedes C.E., Mota M.S., Lima J.G., et al. Proteomic analysis reveals differentially expressed proteins in macrophages infected with Leishmania amazonensis or Leishmania major. Microbes Infect. 2013, 15:579-591.
9. Olivier M., Gregory D.J., Forget G. Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin. Microbiol. Rev. 2005, 18:293-305.
10. Liu D., Uzonna J.E. The early interaction of Leishmania with macrophages and dendritic cells and its influence on the host immune response. Front. Cell. Infect. Microbiol. 2012, 2:1-8.
11. Ghannam S., Bouffi C., Djouad F., Jorgensen C., Noël D. Immunosuppression by mesenchymal stem cells: mechanisms and clinical applications. Stem Cell Res. Ther. 2010, 1. 2.
12. Chen L., Tredget E.E., Wu P.Y.G., Wu Y. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS One 2008, 3:e1886.
13. Hass R., Otte A. Mesenchymal stem cells as all-round supporters in a normal and neoplastic microenvironment. Cell Commun. Signal. 2012, 10:26.
14. Cho D.-I., Kim M.R., Jeong H., Jeong H.C., Jeong M.H., Yoon S.H., et al. Mesenchymal stem cells reciprocally regulate the M1/M2 balance in mouse bone marrow-derived macrophages. Exp. Mol. Med. 2014, 46:e70.
15. Kim J., Hematti P. Mesenchymal stem cell-educated macrophages: a novel type of alternatively activated macrophages. Exp. Hematol. 2009, 37:1445-1453.
16. Sacks D., Noben-Trauth N. The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol. 2002, 2:845-858.
17. Krampera M., Glennie S., Dyson J., Scott D., Laylor R., Simpson E., et al. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Stem Cells 2003, 101:3722-3729.
18. Glennie S., Dyson P.J., Lam E.W., Dazzi F. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 2005, 105:2821-2827.
19. Corcione A., Benvenuto F., Ferretti E., Giunti D., Cappiello V., Cazzanti F., et al. Human mesenchymal stem cells modulate B-cell functions. Multip. Scler. 2006, 107:367-372.
20. English K., Ryan J.M., Tobin L., Murphy M.J., Barry F.P., Mahon B.P. Cell contact, prostaglandin E2 and transforming growth factor beta 1 play non-redundant roles in human mesenchymal stem cell induction of CD4+CD25Highforkhead box P3+ regulatory T cells. Clin. Exp. Immunol. 2009, 156:149-160.
21. Rasmusson I., Ringdén O., Sundberg B., Le Blanc K. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation 2003, 76:1208-1213.
22. Zhang W., Ge W., Li C., You S., Liao L., Han Q., et al. Effects of mesenchymal stem cells on differentiation, maturation, and function of human monocyte-derived dendritic cells. Stem Cells Dev. 2004, 13:263-271.
23. Bernardo M.E., Fibbe W.E. Mesenchymal stromal cells: sensors and switchers of inflammation. Cell Stem Cell 2013, 13:392-402.
24. Raghuvanshi S., Sharma P., Singh S., Van Kaer L., Das G. Mycobacterium tuberculosis evades host immunity by recruiting mesenchymal stem cells. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:21653-21658.
25. Joshi L., Chelluri L.K., Gaddam S. Mesenchymal stromal cell therapy in MDR/XDR tuberculosis: a concise review. Arch. Immunol. Ther. Exp. (Warsz) 2015, 63(6):427-433.
26. Thakur R.S., Tousif S., Awasthi V., Sanyal A., Atul P.K., Punia P., et al. Mesenchymal stem cells play an important role in host protective immune responses against malaria by modulating regulatory T cells. Eur. J. Immunol. 2013, 43:2070-2077.
27. Adutler-Lieber S., Ben-Mordechai T., Naftali-Shani N., Asher E., Loberman D., Raanani E., et al. Human macrophage regulation via interaction with cardiac adipose tissue-derived mesenchymal stromal cells. J. Cardiovasc. Pharmacol. Ther. 2012.
28. Filardy A.a., Costa-Da-Silva C.M., Guimarães-Pinto K., Ribeiro-Gomes F.L., Lopes M.F., et al. Infection with Leishmania major induces a cellular stress response in macrophages. PLoS One 2014, 9:e85715.
29. Belkaid Y., Hoffmann K.F., Mendez S., Kamhawi S., Udey M.C., Udey T.a., et al. The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure. J. Exp. Med. 2001, 194:1497-1506.
30. Kane M.M., Mosser D.M. The role of IL-10 in promoting disease progression in leishmaniasis. J. Immunol. 2001, 166:1141-1147.
31. Brandau S., Jakob M., Hemeda H., Bruderek K., Janeschik S., Bootz F., et al. Tissue-resident mesenchymal stem cells attract peripheral blood neutrophils and enhance their inflammatory activity in response to microbial challenge. J. Leukoc. Biol. 2010, 88:1005-1015.
32. Liew F.Y., Li Y., Millott S. Tumor necrosis factor-alpha synergizes with IFN-gamma in mediating killing of Leishmania major through the induction of nitric oxide. J. Immunol. 1990, 145:4306-4310.
33. Theodos C.M., Povinelli L., Molina R., Sherry B., Titus R.G. Role of tumor necrosis factor in macrophage leishmanicidal activity in vitro and resistance to cutaneous leishmaniasis in vivo. Infect. Immun. 1991, 59:2839-2842.
34. De Kossodo S., Grau G.E., Louis J.a., Müller I. Tumor necrosis factor alpha (TNF-alpha) and TNF-beta and their receptors in experimental cutaneous leishmaniasis. Infect. Immun. 1994, 62:1414-1420.
35. Oliveira C.F., Manzoni-De-Almeida D., Mello P.S., Natale C.C., Santiago H.D.C., Miranda L.D.S., et al. Characterization of chronic cutaneous lesions from TNF-receptor-1-deficient mice infected by Leishmania major. Clin. Dev. Immunol. 2012, 2012.
36. Nashleanas M., Kanaly S., Scott P. Control of Leishmania major infection in mice lacking TNF receptors. J. Immunol. 1998, 160:5506-5513.
37. Mantovani A., Biswas S.K., Galdiero M.R., Sica A., Locati M. Macrophage plasticity and polarization in tissue repair and remodelling. J. Pathol. 2013, 229:176-185.
38. Yang Y.-W., Bai H., Wang C.-B., Lin M., Wu L.-Q. Experimental study on influence of bone marrow mesenchymal stem cells on activation and function of mouse peritoneal macrophages. Zhonghua Xue Ye Xue Za Zhi 2008, 29:540-543.
39. Maggini J., Mirkin G., Bognanni I., Holmberg J., Piazzón I.M., Nepomnaschy I., et al. Mouse bone marrow-derived mesenchymal stromal cells turn activated macrophages into a regulatory-like profile. PLoS One 2010, 5.
40. Hashemi S.M., Hassan Z.M., Pourfathollah A.A., Soudi S., Shafiee A., Soleimani M. Comparative immunomodulatory properties of adipose-derived mesenchymal stem cells conditioned media from BALB/c, C57BL/6, and DBA mouse strains. J. Cell Biochem. 2013, 114:955-965.
41. Hsiao C.-H.C., Ueno N., Shao J.Q., Schroeder K.R., Moore K.C., Donelson J.E., et al. The effects of macrophage source on the mechanism of phagocytosis and intracellular survival of Leishmania. Microbes Infect. 2011, 13:1033-1044.
42. Martinez F.O., Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 2014, 6:13.
43. Lopes M.F., Costa-Da-Silva A.C., Dosreis G.A. Innate immunity to Leishmania infection: within phagocytes. Mediators Inflamm. 2014, 2014.
44. Varin A., Mukhopadhyay S., Herbein G., Gordon S. Alternative activation of macrophages by IL-4 impairs phagocytosis of pathogens but potentiates microbial-induced signalling and cytokine secretion. Blood 2010, 115:353-362.
45. Wei X.Q., Charles I.G., Smith A., Ure J., Feng G.J., Huang F.P., et al. Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 1995, 375:408-411.
46. Oliveira S.H., Fonseca S.G., Romão P.R., Ferreira S.H., Cunha F.Q. Nitric oxide mediates the microbicidal activity of eosinophils. Mem. Inst. Oswaldo Cruz 1997, 92:233-235.
47. Fonseca S.G., Romão P.R.T., Figueiredo F., Morais R.H., Lima H.C., Ferreira S.H., et al. TNF-alpha mediates the induction of nitric oxide synthase in macrophages but not in neutrophils in experimental cutaneous leishmaniasis. Eur. J. Immunol. 2003, 33:2297-2306.
48. Costa-hurtado M., Olvera A., Martínez-moliner V., Galofré-milà N., Martínez P., Dominguez J. Changes in macrophage phenotype after infection of pigs with Haemophilus parasuis strains with different levels of virulence. Infect. Immun. 2013, 81:2327-2333.
49. Muraille E., De Trez C., Pajak B., Torrentera F.A., De Baetselier P., Leo O., et al. Amastigote load and cell surface phenotype of infected cells from lesions and lymph nodes of susceptible and resistant mice infected with Leishmania major. Infect. Immun. 2003, 71:2704-2715.
50. Liu G., Abraham E. Macrophage polarization. Arter. Thromb. Vasc. Biol. 2013, 93:170-177.