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Actions of Dendritic Cells in the Kidney during Hypertension

Xiaohan Lu, Steven D. Crowley

10.1002/cphy.c210050

Source: Volume 12, Issue 4, October 2022

Published online: August 2022

Full Article on Wiley Online Library



Abstract

The immune response plays a critical role in the pathogenesis of hypertension, and immune cell populations can promote blood pressure elevation via actions in the kidney. Among these cell lineages, dendritic cells (DCs), the most potent antigen‐presenting cells, play a central role in regulating immune response during hypertension and kidney disease. DCs have different subtypes, and renal DCs are comprised of the CD103+CD11b− and CD103−CD11b+ subsets. DCs become mature and express costimulatory molecules on their surface once they encounter antigen. Isolevuglandin‐modified proteins function as antigens to activate DCs and trigger them to stimulate T cells. Activated T cells accumulate in the hypertensive kidney, release effector cytokines, promote renal oxidative stress, and promote renal salt and water retention. Individual subsets of activated T cells can secrete tumor necrosis factor‐alpha, interleukin‐17A, and interferon‐gamma, each of which has augmented the elevation of blood pressure in hypertensive models by enhancing renal sodium transport. Fms‐like tyrosine kinase 3 ligand‐dependent classical DCs are required to sustain the full hypertensive response, but C‐X3‐C chemokine receptor 1 positive DCs do not regulate blood pressure. Excess sodium enters the DC through transporters to activate DCs, whereas the ubiquitin editor A20 in dendritic cells constrains blood pressure elevation by limiting T cell activation. By contrast, activation of the salt sensing kinase, serum/glucocorticoid kinase 1 in DCs exacerbates salt‐sensitive hypertension. This article discusses recent studies illustrating mechanisms through which DC‐T cell interactions modulate levels of pro‐hypertensive mediators to regulate blood pressure via actions in the kidney. © 2022 American Physiological Society. Compr Physiol 12: 4087–4101, 2022.

Figure 1. Figure 1. Dendritic cell (DC) development is governed by a multistep differentiation cascade in the bone marrow. Myeloid precursors derive from hematopoietic stem cells and develop into common DC and myeloid progenitors. Classical/conventional DC (cDC1) and plasmacytoid DC (pDC) arise from common DC progenitors and are dependent on fms‐like tyrosine kinase 3 ligand (FLT3L). cDC continues differentiation in peripheral lymphoid tissues while pDC stays in the bone marrow and is dependent on basic helix‐loop‐helix transcription factor E2‐2. The development of cDC is regulated by several transcription factors, and cDC can be classified as cDC1 and cDC2 dependent on basic leucine zipper ATF‐like transcription factors 3 (BATF3) and interferon regulatory factor 4 (IRF4), respectively. In inflammatory conditions, monocytes differentiate into monocyte‐derived dendritic cells (mDCs) and are recruited into inflammatory sites. Another specialized subset of DCs called the Langerhans cell (LC) is resident in the epidermal layer of the skin.
Figure 2. Figure 2. Dendritic cells (DCs) develop from hematopoietic stem cells in the bone marrow and travel to the kidney. DCs are distributed throughout the renal parenchyma to encounter antigens in the kidney. After DCs engulf antigens and become activated, they home to renal lymph nodes and prime T cells in the T cell zone of the lymph node. After activation, DCs progress toward apoptosis, and their elimination helps to balance immunity and tolerance.
Figure 3. Figure 3. Hypertensive factors such as high salt, angiotensin II, and aldosterone salt activate inflammatory responses in multiple organs, including the brain, heart, blood vessel, kidney, and intestine. Antigen formation in these organs triggers the maturation of DCs that stimulate T cells to release hypertensive cytokines and increase oxidative stress. This process occurs in several target organs allowing activated immune cells to cause organ dysfunction following hypertensive stimuli.
Figure 4. Figure 4. In response to hypertensive stimuli, reactive oxygen species (ROS) are generated and facilitate the formation of neoantigens such as damage‐activated molecular patterns (DAMPs), pathogen‐activated molecular patterns (PAMPs), and isolevuglandin (IsoLG)‐modified proteins. DCs take up neoantigens and become activated, expressing high levels of CC‐chemokine receptor 7 (CCR7) and costimulatory molecules, enabling DCs to present antigen to T cells in the lymph node. CC‐chemokine ligands (CCL) for CCR7, including CCL19 and CCL21, recruit DCs from the kidney into renal lymph nodes to prime T cells. DCs release pro‐hypertensive cytokines such as IL‐1β, IL‐6, and IL‐23 to activate and polarize T cells toward pro‐inflammatory T helper cells. Activated T cells produce TNF‐α, IL‐17A, IL‐1β, and IFN‐γ, increasing sodium/fluid retention in the kidney, exacerbating BP elevation and kidney damage.
Figure 5. Figure 5. In response to hypertensive stimuli, dendritic cells (DCs) are recruited to the kidney, where they mature and are exposed to antigens. Excess sodium enters the DC through sodium transporters to activate DCs. Activation of the salt sensing kinase, serum/glucocorticoid kinase1 (SGK1), in DCs exacerbates salt‐sensitive hypertension. The NF‐κB signaling pathway is downstream of SGK1 and controls DC maturation. On this pathway, the ubiquitin editor A20 in dendritic cells limits blood pressure elevation by restraining NF‐κB‐dependent DC maturation. Innate immune signals mediate DC activation. When DCs become mature, CC‐chemokine receptor 7 (CCR7) and costimulatory molecules including CD40, CD70, CD80, CD86 are expressed on the cell surface to guide DC interactions with the T cell receptor.


Figure 1. Dendritic cell (DC) development is governed by a multistep differentiation cascade in the bone marrow. Myeloid precursors derive from hematopoietic stem cells and develop into common DC and myeloid progenitors. Classical/conventional DC (cDC1) and plasmacytoid DC (pDC) arise from common DC progenitors and are dependent on fms‐like tyrosine kinase 3 ligand (FLT3L). cDC continues differentiation in peripheral lymphoid tissues while pDC stays in the bone marrow and is dependent on basic helix‐loop‐helix transcription factor E2‐2. The development of cDC is regulated by several transcription factors, and cDC can be classified as cDC1 and cDC2 dependent on basic leucine zipper ATF‐like transcription factors 3 (BATF3) and interferon regulatory factor 4 (IRF4), respectively. In inflammatory conditions, monocytes differentiate into monocyte‐derived dendritic cells (mDCs) and are recruited into inflammatory sites. Another specialized subset of DCs called the Langerhans cell (LC) is resident in the epidermal layer of the skin.


Figure 2. Dendritic cells (DCs) develop from hematopoietic stem cells in the bone marrow and travel to the kidney. DCs are distributed throughout the renal parenchyma to encounter antigens in the kidney. After DCs engulf antigens and become activated, they home to renal lymph nodes and prime T cells in the T cell zone of the lymph node. After activation, DCs progress toward apoptosis, and their elimination helps to balance immunity and tolerance.


Figure 3. Hypertensive factors such as high salt, angiotensin II, and aldosterone salt activate inflammatory responses in multiple organs, including the brain, heart, blood vessel, kidney, and intestine. Antigen formation in these organs triggers the maturation of DCs that stimulate T cells to release hypertensive cytokines and increase oxidative stress. This process occurs in several target organs allowing activated immune cells to cause organ dysfunction following hypertensive stimuli.


Figure 4. In response to hypertensive stimuli, reactive oxygen species (ROS) are generated and facilitate the formation of neoantigens such as damage‐activated molecular patterns (DAMPs), pathogen‐activated molecular patterns (PAMPs), and isolevuglandin (IsoLG)‐modified proteins. DCs take up neoantigens and become activated, expressing high levels of CC‐chemokine receptor 7 (CCR7) and costimulatory molecules, enabling DCs to present antigen to T cells in the lymph node. CC‐chemokine ligands (CCL) for CCR7, including CCL19 and CCL21, recruit DCs from the kidney into renal lymph nodes to prime T cells. DCs release pro‐hypertensive cytokines such as IL‐1β, IL‐6, and IL‐23 to activate and polarize T cells toward pro‐inflammatory T helper cells. Activated T cells produce TNF‐α, IL‐17A, IL‐1β, and IFN‐γ, increasing sodium/fluid retention in the kidney, exacerbating BP elevation and kidney damage.


Figure 5. In response to hypertensive stimuli, dendritic cells (DCs) are recruited to the kidney, where they mature and are exposed to antigens. Excess sodium enters the DC through sodium transporters to activate DCs. Activation of the salt sensing kinase, serum/glucocorticoid kinase1 (SGK1), in DCs exacerbates salt‐sensitive hypertension. The NF‐κB signaling pathway is downstream of SGK1 and controls DC maturation. On this pathway, the ubiquitin editor A20 in dendritic cells limits blood pressure elevation by restraining NF‐κB‐dependent DC maturation. Innate immune signals mediate DC activation. When DCs become mature, CC‐chemokine receptor 7 (CCR7) and costimulatory molecules including CD40, CD70, CD80, CD86 are expressed on the cell surface to guide DC interactions with the T cell receptor.
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Article Title: Actions of Dendritic Cells in the Kidney during Hypertension
 

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Xiaohan Lu, Steven D. Crowley. Actions of Dendritic Cells in the Kidney during Hypertension. Compr Physiol 2022, 12: 4087-4101. doi: 10.1002/cphy.c210050