Murine Myeloid Dendritic Cells That Phagocytose Apoptotic T Cells Inhibit the Immune Response via NO

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Zhong, Kaili ^a   Song, Wengang ^b   Wang, Qian ^b   Wang, Chao ^c   Liu, Xi ^c   Chen, Dongwei ^c   Zhu, Zhongli ^b   Wu, Yiqing ^c   Zhang, Weijing ^a   Zhang, Minghui ^c  

^a BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^b SHANDONG PROVINCIAL HOSPITAL AFFILIATED TO SHANDONG FIRST MEDICAL UNIVERSITY   (China)

^c Tsinghua University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; STAT3 PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL TRANSFORMATION; COCULTURE; ENZYME RELEASE; ENZYME SYNTHESIS; IMMUNE DEFICIENCY; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MOUSE; MYELOID DENDRITIC CELL; NONHUMAN; PHAGOCYTOSIS; PROTEIN PHOSPHORYLATION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE;

ADAPTIVE IMMUNITY; ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; DENDRITIC CELLS; DNA PRIMERS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PHAGOCYTOSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES;

MURINAE;

EID: 84869222346     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049378     Document Type: Article

References (44)

1. Perruche S, Zhang P, Liu Y, Saas P, Bluestone JA, et al. (2008) CD3-specific antibody-induced immune tolerance involves transforming growth factor-beta from phagocytes digesting apoptotic T cells. Nat Med 14: 528-535.
2. Marguti I, Yamamoto GL, da Costa TB, Rizzo LV, de Moraes LV, (2009) Expansion of CD4+ CD25+ Foxp3+ T cells by bone marrow-derived dendritic cells. Immunology 127: 50-61.
3. Zhang M, Tang H, Guo Z, An H, Zhu X, et al. (2004) Splenic stroma drives mature dendritic cells to differentiate into regulatory dendritic cells. Nat Immunol 5: 1124-1133.
4. Zhang B, Liu R, Shi D, Liu X, Chen Y, et al. (2009) Mesenchymal stem cells induce mature dendritic cells into a novel Jagged-2-dependent regulatory dendritic cell population. Blood 113: 46-57.
5. Liu Q, Zhang C, Sun A, Zheng Y, Wang L, et al. (2009) Tumor-educated CD11bhighIalow regulatory dendritic cells suppress T cell response through arginase I. J Immunol. 182: 6207-6216.
6. Morelli AE, Larregina AT, Shufesky WJ, Zahorchak AF, Logar AJ, et al. (2003) Internalization of circulating apoptotic cells by splenic marginal zone dendritic cells: dependence on complement receptors and effect on cytokine production. Blood 101: 611-620.
7. Amarilyo G, Verbovetski I, Atallah M, Grau A, Wiser G, et al. (2010) iC3b-opsonized apoptotic cells mediate a distinct anti-inflammatory response and transcriptional NF-kappaB-dependent blockade. Eur J Immunol 40: 699-709.
8. Williams CA, Harry RA, McLeod JD, (2008) Apoptotic cells induce dendritic cell-mediated suppression via interferon-gamma-induced IDO. Immunology 124: 89-101.
9. Ren G, Su J, Zhao X, Zhang L, Zhang J, et al. (2008) Apoptotic cells induce immunosuppression through dendritic cells: critical roles of IFN-gamma and nitric oxide. J Immunol 181: 3277-3284.
10. Tang H, Guo Z, Zhang M, Wang J, Chen G, et al. (2006) Endothelial stroma programs hematopoietic stem cells to differentiate into regulatory dendritic cells through IL-10. Blood 108: 1189-1197.
11. Liu X, Tian PK, Ju DW, Zhang MH, Yao M, et al. (2003) Systemic genetic transfer of p21WAF-1 and GM-CSF utilizing of a novel oligopeptide-based EGF receptor targeting polyplex. Cancer Gene Ther 10: 529-539.
12. Bai B, Song W, Ji Y, Liu X, Tian L, et al. (2009) Microglia and microglia-like cell differentiated from DC inhibit CD4 T cell proliferation. PLoS One 4: e7869.
13. Li Q, Guo Z, Xu X, Xia S, Cao X, (2008) Pulmonary stromal cells induce the generation of regulatory DC attenuating T-cell-mediated lung inflammation. Eur J Immunol 38: 2751-2761.
14. Sen P, Wallet MA, Yi Z, Huang Y, Henderson M, et al. (2007) Apoptotic cells induce Mer tyrosine kinase-dependent blockade of NF-kappaB activation in dendritic cells. Blood 109: 653-660.
15. Cheng F, Wang HW, Cuenca A, Huang M, Ghansah T, et al. (2003) A critical role for Stat3 signaling in immune tolerance. Immunity 19: 425-436.
16. Nefedova Y, Cheng P, Gilkes D, Blaskovich M, Beg AA, et al. (2005) Activation of dendritic cells via inhibition of Jak2/STAT3 signaling. J Immunol 175: 4338-4346.
17. Wang T, Niu G, Kortylewski M, Burdelya L, Shain K, et al. (2004) Regulation of the innate and adaptive immune responses by Stat-3 signaling in tumor cells. Nat Med 10: 48-54.
18. Murray PJ, (2006) Understanding and exploiting the endogenous interleukin-10/STAT3-mediated anti-inflammatory response. Curr Opin Pharmacol 6: 379-386.
19. Kushwah R, Oliver JR, Zhang J, Siminovitch KA, Hu J, (2009) Apoptotic dendritic cells induce tolerance in mice through suppression of dendritic cell maturation and induction of antigen-specific regulatory T cells. J Immunol 183: 7104-7118.
20. Kushwah R, Wu J, Oliver JR, Jiang G, Zhang J, et al. (2010) Uptake of apoptotic DC converts immature DC into tolerogenic DC that induce differentiation of Foxp3+ Treg. Eur J Immunol 40: 1022-1035.
21. Yi Z, Li L, Matsushima GK, Earp HS, Wang B, et al. (2009) A novel role for c-Src and STAT3 in apoptotic cell-mediated MerTK-dependent immunoregulation of dendritic cells. Blood 114: 3191-3198.
22. Fransen JH, Hilbrands LB, Jacobs CW, Adema GJ, Berden JH, et al. (2009) Both early and late apoptotic blebs are taken up by DC and induce IL-6 production. Autoimmunity 42: 325-327.
23. Steinman RM, Turley S, Mellman I, Inaba K, (2000) The induction of tolerance by dendritic cells that have captured apoptotic cells. J Exp Med 191: 411-416.
24. Savill J, Dransfield I, Gregory C, Haslett C, (2002) A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2: 965-975.
25. Lleo A, Selmi C, Invernizzi P, Podda M, Gershwin ME, (2008) The consequences of apoptosis in autoimmunity. J Autoimmun 31: 257-262.
26. Walker MR, Carson BD, Nepom GT, Ziegler SF, Buckner JH, (2005) De novo generation of antigen-specific CD4+CD25+ regulatory T cells from human CD4+CD25- cells. Proc Natl Acad Sci U S A 102: 4103-4108.
27. Hutton JF, Gargett T, Sadlon TJ, Bresatz S, Brown CY, et al. (2009) Development of CD4+CD25+FoxP3+ regulatory T cells from cord blood hematopoietic progenitor cells. J Leukoc Biol 85: 445-451.
28. Yamazaki S, Dudziak D, Heidkamp GF, Fiorese C, Bonito AJ, et al. (2008) CD8+ CD205+ splenic dendritic cells are specialized to induce Foxp3+ regulatory T cells. J Immunol 181: 6923-6933.
29. Park SJ, Nakagawa T, Kitamura H, Atsumi T, Kamon H, et al. (2004) IL-6 regulates in vivo dendritic cell differentiation through STAT3 activation. J Immunol 173: 3844-3854.
30. Melillo JA, Song L, Bhagat G, Blazquez AB, Plumlee CR, et al. (2010) Dendritic cell (DC)-specific targeting reveals Stat3 as a negative regulator of DC function. J Immunol 184: 2638-2645.
31. Sun Y, Chin YE, Weisiger E, Malter C, Tawara I, et al. (2009) Cutting edge: Negative regulation of dendritic cells through acetylation of the nonhistone protein STAT-3. J Immunol 182: 5899-5903.
32. Karaghiosoff M, Neubauer H, Lassnig C, Kovarik P, Schindler H, et al. (2000) Partial impairment of cytokine responses in Tyk2-deficient mice. Immunity 13: 549-560.
33. Park SY, Baik YH, Cho JH, Kim S, Lee KS, et al. (2008) Inhibition of lipopolysaccharide-induced nitric oxide synthesis by nicotine through S6K1-p42/44 MAPK pathway and STAT3 (Ser 727) phosphorylation in Raw 264.7 cells. Cytokine 44: 126-134.
34. Huang C, Ma R, Sun S, Wei G, Fang Y, et al. (2008) JAK2-STAT3 signaling pathway mediates thrombin-induced proinflammatory actions of microglia in vitro. J Neuroimmunol 204: 118-125.
35. Tassiulas I, Park-Min KH, Hu Y, Kellerman L, Mevorach D, et al. (2007) Apoptotic cells inhibit LPS-induced cytokine and chemokine production and IFN responses in macrophages. Hum Immunol 68: 156-164.
36. Yu Z, Kone BC, (2004) The STAT3 DNA-binding domain mediates interaction with NF-kappaB p65 and iuducible nitric oxide synthase transrepression in mesangial cells. J Am Soc Nephrol 15: 585-591.
37. Lo HW, Hsu SC, Ali-Seyed M, Gunduz M, Xia W, et al. (2005) Nuclear interaction of EGFR and STAT3 in the activation of the iNOS/NO pathway. Cancer Cell 7: 575-589.
38. Shao WH, Zhen Y, Eisenberg RA, Cohen PL, (2009) The Mer receptor tyrosine kinase is expressed on discrete macrophage subpopulations and mainly uses Gas6 as its ligand for uptake of apoptotic cells. Clin Immunol 133: 138-144.
39. Thorp EB, (2010) Mechanisms of failed apoptotic cell clearance by phagocyte subsets in cardiovascular disease. Apoptosis 15: 1124-1136.
40. Wallet MA, Sen P, Flores RR, Wang Y, Yi Z, et al. (2008) MerTK is required for apoptotic cell-induced T cell tolerance. J Exp Med 205: 219-232.
41. Cao X, Tay A, Guy GR, Tan YH, (1996) Activation and association of Stat3 with Src in v-Src-transformed cell lines. Mol Cell Biol 16: 1595-1603.
42. Zhou J, Wulfkuhle J, Zhang H, Gu P, Yang Y, et al. (2007) Activation of the PTEN/mTOR/STAT3 pathway in breast cancer stem-like cells is required for viability and maintenance. Proc Natl Acad Sci U S A 104: 16158-16163.
43. Weichhart T, Costantino G, Poglitsch M, Rosner M, Zeyda M, et al. (2008) The TSC-mTOR signaling pathway regulates the innate inflammatory response. Immunity 29: 565-577.
44. Haidinger M, Poglitsch M, Geyeregger R, Kasturi S, Zeyda M, et al. (2010) A versatile role of mammalian target of rapamycin in human dendritic cell function and differentiation. J Immunol 185: 3919-3931.