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J Am Soc Nephrol. Feb 2012; 23(2): 194–203.
PMCID: PMC3269181

The Renal Mononuclear Phagocytic System

Abstract

The renal mononuclear phagocytic system, conventionally composed of macrophages (Mø) and dendritic cells (DCs), plays a central role in health and disease of the kidney. Overlapping definitions of renal DCs and Mø, stemming from historically separate research tracks and the lack of experimental tools to specifically study the roles of these cells in vivo, have generated confusion and controversy, however, regarding their immunologic function in the kidney. This brief review provides an appraisal of the current state of knowledge of the renal mononuclear phagocytic system interpreted from the perspective of immunologic function. Physical characteristics, ontogeny, and known functions of the main subsets of renal mononuclear phagocytes as they relate to homeostasis, surveillance against injury and infection, and immune-mediated inflammatory injury and repair within the kidney are described. Gaps and inconsistencies in current knowledge are used to create a roadmap of key questions to be answered in future research.

The mononuclear phagocytic system in nonlymphoid organs such as the kidney is composed of diverse subsets of bone marrow–derived macrophages (Mø) and dendritic cells (DCs).1 Mø are defined as tissue-resident phagocytic cells that contribute to steady-state tissue homeostasis by clearing apoptotic material and producing growth factors. During infection, they perform antimicrobial effector functions such as phagocytosis and production of toxic metabolites and proinflammatory cytokines.1,2 DCs, however, are defined primarily by the specialized functions of antigen presentation and regulation of immune effector cells. Classically, DCs collect antigenic material in tissues and then migrate to lymph nodes for the purpose of presenting antigen to naïve T cells.1,3 As summarized in Table 1, however, Mø and DCs within the kidney exhibit additional and at times, overlapping functional properties that extend beyond these classic paradigms. Furthermore, similar to mononuclear phagocytes in skin, lung, and gut, the predominant, resident renal mononuclear phagocytes (rMoPh) simultaneously express markers traditionally associated with either Mø or DCs.47 Indeed, as discussed below, many research groups have characterized these rMoPh for over three decades as either Mø or DCs, despite growing evidence of phenotypic and functional overlap, creating a barrier to cohesive progress in the field.

Table 1.
Distinct and shared functions of macrophages and dendritic cells in the kidney

Knowledge of rMoPh began with groundbreaking studies in normal kidneys of mice and rats that identified abundant dendritiform cells within the renal interstitium. These cells were designated antigen-presenting DCs on the basis of MHC class II expression8,9 or resident Mø because of F4/80 expression.810 In addition, rare MHC class II+ globular Mø were identified in the glomerulus11,12 and subcapsular and periarterial connective tissue.13,14 Subsequently, however, multicolor flow cytometry revealed substantial overlap and heterogeneity in expression of historically defined Mø (CD11b, F4/80, and CD68) and DC (CD11c, MHC II, and CD80/86) markers by interstitial rMoPh.1519 Along with similar descriptions in normal human kidney,2022 these studies established the predominant rMoPh at steady state as networked, dendritiform, interstitial cells that coexpress multiple markers previously thought to segregate Mø from DCs. Hence, many investigators, whether originating from Mø or DC disciplines, were unknowingly studying the same predominant rMoPh, while often neglecting knowledge from the other discipline. As a result, the use of markers as surrogates for Mø or DC functions within the renal mononuclear phagocytic system (Table 1) is increasingly questioned.22 This debate has also been heightened by lack of specificity of reagents commonly used to induce loss of function of DCs or Mø (Table 2).

Table 2.
Features and pitfalls of commonly used strategies to induce loss of function of rMoPh

This ambiguity resulting from conventional nomenclature, now recognized and intensely debated for the mononuclear phagocytic system in general,5 dictates that functional properties are required to properly characterize the renal mononuclear phagocytic system.1 Studies on whether the predominant interstitial rMoPh isolated from kidneys perform like splenic DCs by presenting antigen and activating naïve T lymphocytes or like peritoneal Mø by killing phagocytosed microbes showed the former function.15 This finding supports other reports suggesting migratory and phagocytic properties more typical of DCs.16,23 However, these early studies could not anticipate the multitude of additional Mø and DC functions now assigned to the renal mononuclear phagocytic system2430 or the fact that functional plasticity—rather than dichotomy—might exist depending on cues provided to rMoPh from the environment.22,29,30 Moreover, the renal mononuclear phagocytic system at steady state changes dramatically during inflammation, in which resident and recruited rMoPh exhibit great heterogeneity and dynamic phenotypes.3032 In light of these shifting paradigms, we reappraise here the current knowledge of the renal mononuclear phagocytic system. We focus on identifying gaps and inconsistencies in our understanding of the ontogeny and function of rMoPh in surveillance, tolerance, and tissue cytoprotection during steady state, as well as immunity, tissue injury, and repair associated with inflammation. The emerging role for plasticity within the renal mononuclear phagocytic system is also discussed. Notably, knowledge of these topics has come primarily by studying the mouse as a model organism, and translation to humans, which has been limited,20,21 remains an important goal.

ONTOGENY OF MONONUCLEAR PHAGOCYTES OF THE KIDNEY IN STEADY STATE

During the past 10 years, studies of specific transgene reporter mice and multicolor flow cytometry of mouse kidney cell preparations reveal many characteristics of resident rMoPh during normal health. Transgene reporters of cx3cr1 (CX3CR1) and csf1r (CD115) fate map over 90% of rMoPh within the kidney at steady state.17,18,33 The large majority of CX3CR1+ cells is dendritiform rMoPh, which form a contiguous network throughout the entire renal interstitium of mice, lining the microvascular, peritubular, and periglomerular spaces.17,33,34 These predominant rMoPh are definable by a marker profile: CD11b+MHCII+CX3CR1+CD11c+/–F4/80+/–CD103 (Figure 1, CD11b+ rMoPh), which is similar to that of interstitial CD11b-like DC and tissue macrophages described in other nonlymphoid tissues.6,7,1618 Among this CD11b+ rMoPh subset, the reported frequency of expression of CD11c (either with or without F4/80 coexpression) has varied between 40% and 90%,1517,35 indicating that additional phenotypic characterization of these cells is yet required. In addition, F4/80 is reportedly expressed preferentially by medullary rMoPh at steady state.10,17

Figure 1.
Ontogeny of the renal mononuclear phagocytic system of the mouse at steady state and during inflammation. At steady state, bone marrow–resident MDPs give rise to common dendritic cell precursors (CDPs) and pre-DCs. Pre-DCs circulate to the healthy ...

The second definable rMoPh subset, representing ≤5% of steady-state interstitial rMoPh, exhibits the surface phenotype CD11bMHCII+CX3CR1CD11c+F4/80CD103+ (Figure 1, CD103+ rMoPh) and is, therefore, not visible in CX3CR1-GFP reporter mice.18 The function of this second subset in the kidney is unknown at present, but similar cells exist in skin, lung, and intestine where they perform specialized functions, including cross-presentation and induction of regulatory T cells.1,4,6,18,36 Plasmacytoid DCs, which differ ontogenically, functionally, and phenotypically from CD11b+ rMoPh and CD103+ rMoPh, are difficult to detect in normal mouse and human kidneys and may be absent.20,21 CD11b+ rMoPh within normal glomeruli are scarce, more globular-shaped, and seem to lack CD11c and F4/80.15,19,37 The rMoPh of normal human kidneys show generally similar anatomic distribution and population heterogeneity,20,21 but not all murine markers (F4/80 and CX3CR1) can be used to classify human rMoPh. To the extent that it has been characterized to date, the phenotype of the predominant human rMoPh displays the following marker profile: CD11b+CD68+BDCA-1+CD14+DC-SIGN+CD11c+MHC II+CD207.6,20,21

Studies of the ontogeny of resident rMoPh in mice show that both major subsets derive from a common hematopoietic monocyte/Mø/DC precursor (MDP), either through a common DC precursor, which gives rise only to pre-DCs and DCs, or through circulating monocytes (Figure 1).1,18,38 Two bone marrow–derived monocyte subsets, distinguished by high or low expression of the surface protein Ly6C in mouse and expression patterns of CD14 and CD16 in humans,1 may each contribute to the resident rMoPh pool at steady state (Figure 1).18,39 However, circulating monocytes play a larger precursor role for the additional rMoPh populations that arise during inflammatory infiltration of the kidney (discussed below).35,40 Whether all rMoPh represent the progeny of MDP remains unclear, and recent studies of mouse and human hematopoeisis raise the possibility that some rMoPh originate from lymphoid progenitors.41 The development of the renal mononuclear phagocytic system commences before nephrogenesis,42 but whether vestigial, intrarenal progenitor cell niches contribute to renewal of rMoPh populations in postnatal life is unknown.1,18

The renal-derived poietins and other renal-specific factors that induce MDP lineages to rMoPh are relatively unclear. With the exception of CD103+ rMoPh, activation of both the Fms-like tyrosine kinase 3 receptor (CD135) and CD115 are required for the development and maintenance of the vast majority of rMoPh (Figure 1).18,43 Colony-stimulating factor 1 (CSF-1), the ligand for CD115, is expressed by the renal parenchyma44 and when injected, expands circulating monocytes.45 Whether the density of rMoPh in normal kidneys also increases with CSF-1 injection is unclear, but in vivo blockade of CSF-1/CD115 interactions results in depletion of most resident rMoPh.43 Systemic administration of Flt3L, the ligand for CD135, increases the density of rMoPh,46,47 but whether Flt3L is expressed within the kidney is unknown. Nevertheless, isolated kidney stromal cells secrete other trophic factors for MDPs,48 exemplifying the probable role of the renal parenchyma to differentiate the renal mononuclear phagocytic system.49

Few studies have addressed cellular turnover within the renal mononuclear phagocytic system.50 Bromodeoxyuridine (BrdU) labeling and parabiosis experiments in mice show that 10% of the predominant CD11b+ rMoPh in recipient mice becomes BrdU-positive within 12 hours. However, it requires 30 days for rMoPh from parabiotic donors to completely disappear after mice are separated. Of interest, turnover rates for CD103+ rMoPh are approximately two times as fast.18 In contrast to these experimental approaches, bone marrow transplant studies in mice suggest that repopulation of rMoPh by MDP lineages requires at least 8 weeks and possibly several months—variability that may be caused by irradiation techniques and strain of mice.19,35,51,52 In any respect, these studies together suggest that complete turnover of the renal mononuclear phagocytic system is slow at steady state.

FUNCTIONS OF rMoPh IN SURVEILLANCE, TOLERANCE, AND TISSUE CYTOPROTECTION

Surveillance, the anatomic and functional readiness to respond to environmental cues, is well described for the renal mononuclear phagocytic system, and rMoPh are often considered sentinels of the renal immune system, responding to diverse environmental cues that inform their subsequent functions. In the normal kidney, rMoPh are responsive to a range of stimuli associated with tissue perturbations such as pathogen-associated molecular patterns, damage-associated molecular patterns (DAMPs), other cell and matrix debris, immunoglobulin, complement components, oxygen tension, adenosine, cytokines, chemokines, and cell–cell contact.2429 Nonetheless, the specific protective roles of each surveillance mechanism and the possibilities that surveillance mechanisms differ by anatomic location or rMoPh subpopulation have not been extensively investigated to date. Additional studies are needed to increase understanding of how rMoPh respond to cues with varying characteristics and within different renal compartments.

Peripheral tolerance to self-antigens within the kidney that may escape central tolerance is also likely to be orchestrated by rMoPh. It is known that CD11c+ rMoPh at steady state sample self-antigens derived from tubular filtrate, renal cells, or renal matrix.16,53,54 These cells transport and present antigens to cognate T lymphocytes in renal lymph nodes, supplementing additional rMoPh-independent lymphatic transport and presentation of small filtered antigen, and promote tolerance to such antigens through mechanisms such as cross-tolerance.53,55 The intrarenal sampling, transport, and presentation of antigen occur through interstitial rMoPh, and no studies to date have shown the ability of intraglomerular rMoPh to educate T lymphocytes through antigen presentation, whether to tolerance or immunity. Interestingly, rMoPh isolated from normal kidneys on the basis of CD11c expression induce the expansion of regulatory T lymphocytes in allogeneic mixed leukocyte reactions,46 suggesting the possibility that rMoPh propagate regulatory T lymphocytes in the periphery at steady state in vivo. Aside from hypoxemia,5658 however, the cues within the kidney that may influence rMoPh to enhance or break peripheral tolerance are not well understood.54,55,59

In addition to maintaining tolerance to self-antigens, mounting evidence suggests that rMoPh at steady state also protect or lessen damage to the renal parenchyma after diverse insults through innate, anti-inflammatory responses.19,6062 This finding may reflect the innate phase response by tolerogenic rMoPh utilizing counter-regulators such as single Ig receptor-related protein,63 IFN regulatory factor 4,64 adenosine 2A receptor,65 hemeoxygenase-1,56,62 and Fc γ-receptor.66 Secretion of IL-10 by resident rMoPh is emerging as one of the key effectors of cytoprotection,61,66 raising the possibility of therapeutically augmenting this secretion by rMoPh to enhance cytoprotection.30,67 Additional research is needed to determine whether this function of the renal mononuclear phagocytic system represents an active response by rMoPh to silence insults that should not be perceived as injurious to the kidney, such as periods of brief ischemia or products from normal cellular turnover.68

FROM STEADY STATE TO INFLAMMATION

Unlike rMoPh functioning at steady state, rMoPh during inflammation exhibit highly complex and dynamic responses that can determine renal outcomes after injury.3032 Studies of mouse models of acute kidney injury induced by endotoxemia, ischemia reperfusion, acute urinary obstruction, and pyelonephritis show that resident rMoPh in the interstitium increase in size, upregulate MHC and costimulatory proteins, and secrete inflammatory mediators within hours after initiating injury.15,16,69,70 In some studies, an unknown fraction of resident rMoPh vacate the interstitium within 24–48 hours coincident with the accumulation of rMoPh in draining renal lymph nodes.16,71 During the same interval, large numbers of Ly-6C+ (inflammatory) monocytes as well as some Ly6C monocytes infiltrate the kidney and along with remaining resident rMoPh, undergo activation and differentiation to progeny rMoPh with diverse functional phenotypes (Figure 1).35,40,69 Bone marrow release of Ly-6C+ monocytes and trafficking of these cells to the injured kidney is triggered by CCR2 ligation.40,72 In glomerular inflammation, a similar influx and expansion of rMoPh, functioning primarily as Mø, is well described.73,74 Whether intraglomerular rMoPh present at the initiation of injury also migrate to renal lymph nodes for antigen presentation is unknown, but glomerular infiltration by rMoPhs with the phenotype of conventional and plasmacytoid DCs has been described in human lupus nephritis.21,75 In any respect, the degree to which inflammatory monocyte-derived rMoPh perform the repertoire of Mø and DC functions (Figure 1 and Table 1) within glomerular or tubulointerstitial compartments is not fully understood. In the following sections, we summarize current knowledge of the role of the renal mononuclear phagocytic system in active renal immunity and inflammation and their resolution.

FUNCTIONS OF rMoPh IN IMMUNITY, TISSUE INJURY, AND TISSUE REPAIR

The renal mononuclear phagocytic system plays pivotal roles in proinflammatory innate and adaptive immune responses initiated within the kidney. rMoPh resident at steady state are induced to rapidly produce proinflammatory innate cytokines (TNF, IL-6, and IL-1) and chemokines (CCL2, CCL5, CXCL10, and CXCL2) depending on environmental cues.40,70,74,76 As a result, Ly6C+ monocytes and other leukocytes are recruited into the kidney, providing a secondary and major source of innate mediators.35,40,74 This innate phase, evident during either glomerular or tubulointerstitial inflammation, shapes subsequent adaptive immune responses by rMoPh, although this progression has been more clearly described for interstitial compared with glomerular rMoPh. For example, in models of GN, resident interstitial CD11c+ rMoPh suppress T helper type 1 (Th1) lymphocytes recruited early after injury.60 With prolonged innate inflammation, likely in concert with DAMPs,7779 these CD11c+ rMoPh mature and now stimulate Th1 effectors.80,81 Studies in models of ureteral obstruction suggest that this pattern may also influence intrarenal Th17 responses orchestrated by resident interstitial rMoPh.69 Additional research is clearly needed to define the full spectrum of immune stimulatory properties of the major rMoPh subpopulations as well as any role for intraglomerular rMoPh in adaptive immune responses.

In addition to orchestrating other leukocyte populations that may induce injury, rMoPh may also directly damage the renal parenchyma. As described above, resident rMoPh elaborate damaging innate cytokines.30,40,70 In addition, recruited inflammatory monocytes35,40 that differentiate into inflammatory rMoPh also produce oxygen radicals, hydrogen peroxide, nitric oxide, IL-1, TNF-α, and other effectors of tissue injury.8286 The vast majority of reports on this acute phase of injury, whether focused on glomerular or tubulointerstitial compartments, assign responsibility for tissue damage to resident or recruited rMoPh polarized to a classically activated (M1, proinflammatory) Mø phenotype.27,30 In contrast, later fibrotic phases of injury are orchestrated by resident or recruited rMoPh polarized to an alternatively activated (M2, anti-inflammatory and wound healing) Mø phenotype.29,30,87

In contrast to their role in tissue injury, rMoPh are also associated with repair of damaged renal parenchyma during resolution of renal inflammation. Seminal studies using clodronate-containing liposomes (Table 2) to ablate rMoPh show that recruited glomerular rMoPh are required for the spontaneous repair that occurs after glomerular injury in the Thy1.1 model of mesangioproliferative GN.88 Ablation and adoptive transfer studies conducted later similarly showed that recruited rMoPh actively promote repair of injured renal tubules.67,87,8991 These reparative rMoPh clear DAMPs and other cell and matrix debris, stimulate proliferation of surviving cells through elaboration of wnt ligands, and promote angiogenesis.92 This biphasic response by recruited rMoPh to first injure and then repair renal parenchyma may reflect a process of reprogramming. After injury, resident and recruited rMoPh subpopulations exhibit distinct expression of proinflammatory, anti-inflammatory, profibrotic, and reparative factors35,40 suggestive of the presence of heterogeneous populations of rMoPh fulfilling disparate functions. Although functional heterogeneity is undoubtedly present among rMoPh at any given time after an episode of renal injury, individual rMoPh can switch from inflammatory to reparative phenotypes within the renal interstitium,30,90 a process referred to as plasticity (discussed below). Regardless of their origin, additional studies are needed to determine whether reparative rMoPh are retained after kidneys heal to comprise a long-lasting component of the renal mononuclear phagocyte system at steady state.

PLASTICITY OF FUNCTION OF rMoPh DURING RENAL INJURY AND REPAIR

As the recent study by Lee et al.90 illustrates, the ability of rMoPh to change functions over time may be an important general property of the renal mononuclear phagocytic system (Figure 2). Classic examples of rMoPh plasticity include the maturation of renal DCs to educate T lymphocytes and the polarization of renal Mø to M1 or M2 functional phenotypes in response to environmental cues.30,93 More recent studies show that bone marrow-derived Mø or rMoPh display biphasic expression of proinflammatory factors followed by anti-inflammatory and reparative factors in response to challenge with lipopolysaccharide or ischemic injury, respectively.62,92,94,95 Within the kidney, specific paracrine factors released from renal parenchymal cells, such as IL-10, DAMPs, or apoptotic bodies, initiate or augment this phenotypic reprogramming of rMoPh.90,96,97

Figure 2.
Proposed model for plasticity of rMoPh during inflammation and repair. During inflammation, rMoPh are derived from both resident and infiltrating cells. The release of DAMPs provides a proinflammatory stimulus and activates rMoPh to produce injurious ...

The plasticity of rMoPh may also represent inducible reactivation of developmental programs normally active in differentiating precursors. For example, pre-DCs are the immediate precursors for CD103+ rMoPh; however, pre-DCs can also be induced to repopulate CD11b+ rMoPh.18 The former progeny functions solely as DCs, although this finding has not been formally shown within the kidney, whereas the latter progeny clearly harbors subsets performing functions as Mø.18 The balance of poietins produced within the kidney for rMoPhs, particularly during inflammation or its resolution, may be a key driving force for this altered lineage commitment.44 Intriguingly, although no studies have been done on rMoPh per se, emerging evidence suggests that intrinsic molecular programs of plasticity governed by microRNA (miRNA)98 determine the commitment and transition of rMoPh to function as DCs or Mø. In addition, studies of bone marrow-derived Mø suggest that epigenetic chromatin modification by histone-modifying enzymes,99,100 and gene-silencing polycomb group proteins101 may be key regulators of Mø activation status. Future research on plasticity within the renal mononuclear phagocyte system may help to develop a unifying nomenclature that represents the function of rMoPh.

A ROADMAP FOR FUTURE PROGRESS

Significant progress in understanding the renal mononuclear phagocytic system has been achieved over the past three decades. Many typical DC and Mø-associated functions of the major rMoPh subsets have been described, especially in the last 5 years. As this brief review highlights, however, rMoPh may fulfill definitions and functions both of DCs and Mø, hampering definitive classification. Indeed, parallel streams of literature have been created that do not provide a fully integrated body of knowledge to this point. As a roadmap for future research, we highlight in Table 3 some of the specific areas of investigation that may yield valuable new insights. Engaging in this roadmap will require acknowledging that the complexity of the renal mononuclear phagocytic system, as with the mononuclear phagocytic system in general,5 does not fit well with simple, binary naming conventions. Specifically, historic divisions that have separated renal investigators into Mø and DC camps are falling, allowing for some key unifying conclusions to be made (Table 4) and paving the way for novel, joint approaches to better understand the role of the renal mononuclear phagocytic system in health and disease of the kidney.

Table 3.
Roadmap of key topics for future research on the renal mononuclear phagocytic system
Table 4.
Key conclusions

DISCLOSURES

None.

Acknowledgments

The authors acknowledge that many more excellent original research studies of relevance to the understanding of the renal mononuclear phagocytic system have been published than could be cited in this brief review article.

P.J.N. is supported by US National Institutes of Health (NIH) Grants DK83375, DK83375S1, and DK83912 and a Sponsored Research Agreement with Genzyme. A.J.R. is supported by the European Union (EU) FP7 Marie Curie Program MACRORIEN and TranSVIR, the EU FP7 Health Program INTRICATE, and the Austrian Vienna Science and Technology Fund. M.D.G. is supported by Science Foundation Ireland Grants SFI PI 06/IN.1/B652 and SFI SRC 09/SRC/B1794 and Health Research Board of Ireland Grant HRA HSR/2010/63. J.H. is supported by United Kingdom Medical Research Council Grants G0700330 and G0801235 and the Genzyme Renal Innovation Program. C.K. is supported by Deutsche Forschungsgemeinschaft Grants Ku1063/5, KFO228, and SFBTR57, the EU consortium INTRICATE, and the German National Academic Foundation. J.S.D. is supported by NIH Grants DK73299, DK84077, and DK8739, a Genzyme Research in Progress Award, the Nephcure Foundation, and a Sponsored Research Agreement with Regulus Therapeutics.

Footnotes

Published online ahead of print. Publication date available at www.jasn.org.

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