IL-10-Dependent Crosstalk between Murine Marginal Zone B Cells, Macrophages, and CD8α+ Dendritic Cells Promotes Listeria monocytogenes Infection

Liu, Dong; Yin, Xiangyun; Olyha, Sam J.; Nascimento, Manuela Sales Lima; Chen, Pei; White, Theresa L.; Gowthaman, Uthaman; Zhang, Tingting; Gertie, Jake A.; Zhang, Biyan; Xu, Lan; Yurieva, Marina; Devine, Lesley; Williams, Adam; Eisenbarth, Stephanie C.

doi:10.1016/j.immuni.2019.05.011

Cited by 26 publications

(24 citation statements)

References 74 publications

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“…Although more studies will need to be performed to examine this, these potential alternate methods of transit could impact antigen uptake and subsequently, presentation to naïve T cells. Finally, while previous studies have demonstrated a profound Batf3 cell-extrinsic effect on the induction of Lm-specific CD8 T cell responses (16,17), mice used in this study also lack Batf3 expression in CD8 T cells that may influence the T cell responses at higher infectious doses.…”

Section: Discussionmentioning

confidence: 66%

“…This is in contrast to the restoration of pathogen burden during i.v. Lm infection, where Lm-specific CD8 T cell responses were rescued in Batf3 −/− mice (16,17). Altogether, these data suggest that cDC1 may play an important role in driving effector CD8 T cell responses after foodborne InlA M Lm infection.…”

Section: Infection (Supplementarymentioning

confidence: 72%

“…infection (15). After i.v Lm infection, splenic marginal zone B cells produce IL-10, which acts on CD169 + macrophages to promote bacterial uptake and survival (16). Lm-containing CD169 + macrophages trans-infect cDC1 to mediate Lm transport to the splenic T cell zones.…”

Section: Introductionmentioning

confidence: 99%

“…infection (17). Despite these findings, cDC2 appear to play minimal roles in the generation of protective immunity to Lm, as mice lacking cDC2 do not exhibit defective CD8 T cell responses (16). Although the roles of resident cDC1 and cDC2 after i.v Lm infection have been assessed, the functions of migratory cDC in the early establishment of Lm infection and the induction of T cell responses after foodborne infection have not been extensively studied (20).…”

Section: Introductionmentioning

confidence: 99%

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Mucosal CD8 T Cell Responses Are Shaped by Batf3-DC After Foodborne Listeria monocytogenes Infection

Imperato

Romagnoli³

et al. 2020

Front. Immunol.

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While immune responses have been rigorously examined after intravenous Listeria monocytogenes (Lm) infection, less is understood about its dissemination from the intestines or the induction of adaptive immunity after more physiologic models of foodborne infection. Consequently, this study focused on early events in the intestinal mucosa and draining mesenteric lymph nodes (MLN) using foodborne infection of mice with Lm modified to invade murine intestinal epithelium (InlA M Lm). InlA M Lm trafficked intracellularly from the intestines to the MLN and were associated with Batf3independent dendritic cells (DC) in the lymphatics. Consistent with this, InlA M Lm initially disseminated from the gut to the MLN normally in Batf3 −/− mice. Activated migratory DC accumulated in the MLN by 3 days post-infection and surrounded foci of InlA M Lm. At this time Batf3 −/− mice displayed reduced InlA M Lm burdens, implicating cDC1 in maximal bacterial accumulation in the MLN. Batf3 −/− mice also exhibited profound defects in the induction and gut-homing of InlA M Lm-specific effector CD8 T cells. Restoration of pathogen burden did not rescue antigen-specific CD8 T cell responses in Batf3 −/− mice, indicating a critical role for Batf3 in generating anti-InlA M Lm immunity following foodborne infection. Collectively, these data suggest that DC play diverse, dynamic roles in the early events following foodborne InlA M Lm infection and in driving the establishment of intestinal Lm-specific effector T cells.

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Section: Discussionmentioning

confidence: 66%

Section: Infection (Supplementarymentioning

confidence: 72%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Mucosal CD8 T Cell Responses Are Shaped by Batf3-DC After Foodborne Listeria monocytogenes Infection

Imperato

Romagnoli³

et al. 2020

Front. Immunol.

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“…This regional segregation of cDC1 raises the question of the division of labor within the cDC1 population in the spleen: the red pulp cDC1 subset may be more prone to interact with innate cells, whereas the T cell zone cDC1 subset may be poised to initiate adaptive responses. Interestingly, systemic administration of poly(I:C), red blood cells, or Listeria triggers red pulp cDC1 repositioning in the marginal zone of the white pulp, and in the T cell zone where antigenbearing mature cDC1 have more chance to interact with naïve T cells (Alexandre et al, 2016;Liu et al, 2019;Idoyaga et al, 2009;Calabro et al, 2016). CCR7 is suggested to be a master regulator of the migration of red pulp cDC1 into the T cell zone (Calabro et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

NK cells orchestrate splenic cDC1 migration to potentiate antiviral protective CD8+ T cell responses

Ghilas¹,

Ambrosini²,

Cancel³

et al. 2020

Preprint

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2 Summary (150 words max):A successful immune response relies on a tightly regulated delivery of the right signals to the right cells at the right time. Here we show that innate and innate-like lymphocytes use two mechanisms to orchestrate in time and space the functions of conventional type 1 dendritic cells (cDC1) in spleen. Early after murine cytomegalovirus infection, XCL1 production by lymphocytes with innate functions attracts red pulp cDC1 near IFN--producing NK cells, generating superclusters around infected cells in the marginal zone. There, cDC1 and NK cells physically interact reinforcing their reciprocal activation. Targeted IL-12 delivery and IL-15/IL-15R transpresentation by cDC1 trigger NK cell activation and expansion. In return, activated NK cells deliver GM-CSF to cDC1, triggering their CCR7-dependent relocalization into the T cell zone. This NK cell-dependent licensing of cDC1 accelerates the priming of virusspecific CD8 + T cells. Our findings reveal a novel mechanism through which cDC1 bridge innate and adaptive immunity.

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Conventional type 1 dendritic cells induce T_H1, T_H1‐like follicular helper T cells and regulatory T cells after antigen boost via DEC205 receptor

et al. 2020

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Conventional dendritic cells (cDCs) are specialized in antigen presentation. In the mouse spleen, cDCs are classified in cDC1s and cDC2s, and express DEC205 and DCIR2 endocytic receptors, respectively. Monoclonal antibodies (mAbs) αDEC205 (αDEC) and αDCIR2 have been fused to different antigens to deliver them to cDC1s or cDC2s. We immunized mice with αDEC and αDCIR2 fused to an antigen using Poly(I:C) as adjuvant. The initial immune response was analyzed from days 3 to 6 after the immunization. We also studied the influence of a booster dose. Our results showed that antigen targeting to cDC1s promoted a pro-inflammatory T H 1 cell response. Antigen targeting to cDC2s induced T FH cells, GCs, and plasma cell differentiation. After boost, antigen targeting to cDC1s improved the T H 1 cell response and induced T H 1-like T FH cells that led to an increase in specific antibody titers and IgG class switch. Additionally, a population of regulatory T cells was also observed. Antigen targeting to cDC2s did not improve the specific antibody response after boost. Our results add new information on the immune response induced after the administration of a booster dose with αDEC and αDCIR2 fusion mAbs. These results may be useful for vaccine design using recombinant mAbs.

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IL-10-Dependent Crosstalk between Murine Marginal Zone B Cells, Macrophages, and CD8α+ Dendritic Cells Promotes Listeria monocytogenes Infection

Cited by 26 publications

References 74 publications

Mucosal CD8 T Cell Responses Are Shaped by Batf3-DC After Foodborne Listeria monocytogenes Infection

Mucosal CD8 T Cell Responses Are Shaped by Batf3-DC After Foodborne Listeria monocytogenes Infection

NK cells orchestrate splenic cDC1 migration to potentiate antiviral protective CD8+ T cell responses

Conventional type 1 dendritic cells induce T_H1, T_H1‐like follicular helper T cells and regulatory T cells after antigen boost via DEC205 receptor

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IL-10-Dependent Crosstalk between Murine Marginal Zone B Cells, Macrophages, and CD8α+ Dendritic Cells Promotes Listeria monocytogenes Infection

Cited by 26 publications

References 74 publications

Mucosal CD8 T Cell Responses Are Shaped by Batf3-DC After Foodborne Listeria monocytogenes Infection

Mucosal CD8 T Cell Responses Are Shaped by Batf3-DC After Foodborne Listeria monocytogenes Infection

NK cells orchestrate splenic cDC1 migration to potentiate antiviral protective CD8+ T cell responses

Conventional type 1 dendritic cells induce TH1, TH1‐like follicular helper T cells and regulatory T cells after antigen boost via DEC205 receptor

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Conventional type 1 dendritic cells induce T_H1, T_H1‐like follicular helper T cells and regulatory T cells after antigen boost via DEC205 receptor