Control of Stimulus-Dependent Responses in Macrophages by SWI/SNF Chromatin Remodeling Complexes

doi:10.1016/j.it.2019.12.002

Trends in Immunology

Volume 41, Issue 2, February 2020, Pages 126-140

https://doi.org/10.1016/j.it.2019.12.002 Get rights and content

Highlights

SWI/SNF chromatin remodeling complexes regulate inflammatory gene expression in macrophages through interactions with lineage-determining and stimulus-regulated transcription factors.
SWI/SNF complexes exist as three distinct variants: BAF, ncBAF, and PBAF complexes. Each variant contains both shared and unique subunits, which modulate complex localization and function through subunit-specific binding interactions.
BAF, ncBAF, and PBAF complexes are enriched at different genomic elements and colocalize with distinct transcription factors.
SWI/SNF complex variants likely regulate distinct transcriptional programs in the context of inflammatory stimulation that can be leveraged to specifically curb or promote inflammatory responses using small molecule inhibitors.
Integration of SWI/SNF complex functions can yield greater regulatory control of complex transcriptional networks.

Epigenetic regulation plays an important role in controlling the activation, timing, and resolution of innate immune responses in macrophages. Previously, SWI/SNF chromatin remodeling was found to define the kinetics and selectivity of gene activation in response to microbial ligands; however, these studies do not reflect a comprehensive understanding of SWI/SNF complex regulation. In 2018, a new variant of the SWI/SNF complex was identified with unknown function in inflammatory gene regulation. Here, we summarize the biochemical and genomic properties of SWI/SNF complex variants and the potential for increased regulatory control of innate immune transcriptional programs in light of such biochemical diversity. Finally, we review the development of SWI/SNF complex chemical inhibitors and degraders that could be used to modulate immune responses.

Section snippets

SWI/SNF: The Story So Far

In response to microbial ligands and cytokines, macrophages induce a cascade of events resulting in a transcriptional response important for macrophage activation, cytokine release, and the adaptive immune response. This highly coordinated program is executed by stimulus-regulated transcription factors (SRTFs) (see Glossary) [1]. The binding and activity of SRTFs is in turn restricted to cognate binding sites within ‘cis-regulatory elements’ made accessible by the action of myeloid

Primary versus Secondary Response Genes

Upon activation of Toll-like receptor 4 (TLR4) with lipopolysaccharide (LPS) treatment, mammalian macrophages upregulate proinflammatory genes, which can be divided into primary response genes (PRGs) and secondary response genes (SRGs) based on the requirement for new protein synthesis [19]. PRGs can be further divided into early and late PRGs by their activation kinetics. Previous studies showed that siRNA knockdown of the shared ATPases BRG1 and BRM in bone marrow-derived macrophages (BMDMs)

New Kid on the Block: The BRD9-Containing ncBAF Complex

In 2018, we and others discovered that there is a smaller, noncanonical SWI/SNF complex, also known as the ncBAF complex, that exists alongside the BAF and PBAF complexes (Figure 1) [13., 14., 15., 16.]. Mass spectrometric studies from mouse and human cells determined that the ncBAF complex contains the ATPase subunit BRG1 and the core subunits BAF155 and BAF60A, and that it uniquely incorporates BRD9 and the glioma tumor suppressor candidate region 1 (GLTSCR1) or a paralog, GLTSCR1L.

Enhancer Regulation by BAF Complexes

Using antibodies that recognize ARID1A or BAF45D, BAF complexes have been shown to be enriched at poised, active, and super enhancers, while ncBAF and PBAF complexes are more commonly found at promoters in mouse and human cells (Box 1) [14,15,18]. These data suggest that BAF complexes are important for establishing or maintaining features of enhancer architecture. Indeed, we and others have shown that loss of ARID1A, BRG1, or BAF47 results in loss of chromatin accessibility at enhancers by

Integration of SWI/SNF Complex Functions

Biochemical diversity among SWI/SNF complexes and the array of functionalities that this affords gives the advantage of greater regulatory control over gene expression programs. In mESCs, the ncBAF complex cooperates with TFs Sp5 and Kruppel-like factor 4 (KLF4) and the epigenetic reader BRD4 to regulate the stimulus-dependent program of naïve pluripotency [14]. This function is not shared by the BAF complex, which regulates chromatin accessibility at sites bound by LDTFs OCT4, SOX2, and NANOG

Pharmacological Targeting of SWI/SNF Complexes

The potential role for SWI/SNF complex in inflammatory responses makes it an attractive target for drug development; however, the biochemical properties of these large, multi-subunit complexes have made development of small molecule inhibitors particularly challenging. The development of bromodomain inhibitors directed against various bromodomain-containing SWI/SNF subunits has allowed, for the first time, the ability to probe the function of these domains in SWI/SNF complex targeting,

Translational Outlook

A mechanistic understanding of the role of SWI/SNF complexes in stimulus-dependent responses in BMDMs can lay the groundwork for a deeper understanding of the epigenetic processes that govern macrophage responses during inflammation and immune-related diseases. Indeed, macrophages can acquire different functional programs in response to inflammatory stimuli that can contribute to protection or exacerbation of disease in different contexts, including infection, sepsis, obesity, atherosclerosis,

Concluding Remarks

Previous studies demonstrated a requirement for SWI/SNF complexes in inflammatory gene induction in macrophages, but failed to delineate subunit-specific functions associated with SWI/SNF complex variants (see Outstanding Questions). Gaining insight into the potentially diverse roles of the SWI/SNF complex variants in stimulus-dependent transcription requires ChIP-seq of variant-specific subunit binding in resting and stimulated macrophages, as well as genome-wide profiling of nascent

Acknowledgments

We are thankful to Dr Helen McRae for thoughtful comments on the manuscript and to Amy Cao for help with scientific illustration. D.C.H. is supported by the National Institutes of Health (GM128943-01, CA184043-03), the V Foundation for Cancer Research (V2016-006), the Pew-Stewart Scholars Program for Cancer Research, and the Leona M. and Harry B. Helmsley Charitable Trust. J.G. is supported by the Salk Institute T32 Cancer Training Grant T32CA009370 and the NIGMS NRSA F32 GM128377-01. M.B.M. is

Glossary

Akirin: highly conserved 201-residue protein with orthologs identified throughout metazoa; functions as a transcriptional cofactor.
Assay for transposon-accessible chromatin followed by genome-wide sequencing (ATAC-seq): technique to assay chromatin accessibility; uses the Tn5 transposase to deposit DNA adapters into open chromatin, which are then amplified and sequenced by next-generation sequencing.
Bone marrow-derived macrophages (BMDMs): macrophages harvested from mouse bone marrow and

References (94)

A. Alpsoy et al.
Glioma tumor suppressor candidate region gene 1 (GLTSCR1) and its paralog GLTSCR1-like form SWI/SNF chromatin remodeling subcomplexes
J. Biol. Chem.
(2018)
D.C. Hargreaves
Control of inducible gene expression by signal-dependent transcriptional elongation
Cell
(2009)
V.R. Ramirez-Carrozzi
A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling
Cell
(2009)
D.M. Bhatt
Transcript dynamics of proinflammatory genes revealed by sequence analysis of subcellular RNA fractions
Cell
(2012)
M.J. McAndrew
Chromatin remodeler recruitment during macrophage differentiation facilitates transcription factor binding to enhancers in mature cells
J. Biol. Chem.
(2016)
R. Ostuni
Latent enhancers activated by stimulation in differentiated cells
Cell
(2013)
M.U. Kaikkonen
Remodeling of the enhancer landscape during macrophage activation is coupled to enhancer transcription
Mol. Cell
(2013)
A.J. Tong
A stringent systems approach uncovers gene-specific mechanisms regulating inflammation
Cell
(2016)
S. Yamazaki
Gene-specific requirement of a nuclear protein, IkappaB-zeta, for promoter association of inflammatory transcription regulators
J. Biol. Chem.
(2008)
S. Heinz
Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities
Mol. Cell
(2010)

S. Ghisletti

Identification and characterization of enhancers controlling the inflammatory gene expression program in macrophages

Immunity

(2010)

M. Kim

Loss of HDAC-mediated repression and gain of NF-kappaB activation underlie cytokine induction in ARID1A- and PIK3CA-mutation-driven ovarian cancer

Cell Rep.

(2016)

C. Underhill

A novel nuclear receptor corepressor complex, N-CoR, contains components of the mammalian SWI/SNF complex and the corepressor KAP-1

J. Biol. Chem.

(2000)

J.D. Brown

NF-kappaB directs dynamic super enhancer formation in inflammation and atherogenesis

Mol. Cell

(2014)

M. Stoszko

Small molecule inhibitors of BAF; a promising family of compounds in HIV-1 latency reversal

EBioMedicine

(2016)

J. Quintin

Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes

Cell Host Microbe

(2012)

V. Krasteva

The BAF53a subunit of SWI/SNF-like BAF complexes is essential for hemopoietic stem cell function

Blood

(2012)

W.A. Whyte

Master transcription factors and mediator establish super-enhancers at key cell identity genes

Cell

(2013)

J.R. Dixon

Chromatin domains: the unit of chromosome organization

Mol. Cell

(2016)

S.B. Rothbart et al.

Interpreting the language of histone and DNA modifications

Biochim. Biophys. Acta

(2014)

S. Bultman

A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes

Mol. Cell

(2000)

T.H. Chi

Sequential roles of Brg, the ATPase subunit of BAF chromatin remodeling complexes, in thymocyte development

Immunity

(2003)

C.K. Glass et al.

Molecular control of activation and priming in macrophages

Nat. Immunol.

(2016)

L. Han

Chromatin remodeling mediated by ARID1A is indispensable for normal hematopoiesis in mice

Leukemia

(2019)

V.R. Ramirez-Carrozzi

Selective and antagonistic functions of SWI/SNF and Mi-2beta nucleosome remodeling complexes during an inflammatory response

Genes Dev.

(2006)

M. Witzel

Chromatin-remodeling factor SMARCD2 regulates transcriptional networks controlling differentiation of neutrophil granulocytes

Nat. Genet.

(2017)

P. Priam

SMARCD2 subunit of SWI/SNF chromatin-remodeling complexes mediates granulopoiesis through a CEBPvarepsilon dependent mechanism

Nat. Genet.

(2017)

D.C. Hargreaves et al.

ATP-dependent chromatin remodeling: genetics, genomics and mechanisms

Cell Res.

(2011)

F. Gao

Heterozygous mutations in SMARCA2 reprogram the enhancer landscape by global retargeting of SMARCA4

Mol. Cell

(2019)

H.W. King et al.

The pioneer factor OCT4 requires the chromatin remodeller BRG1 to support gene regulatory element function in mouse embryonic stem cells

Elife

(2017)

T.W.R. Kelso

Chromatin accessibility underlies synthetic lethality of SWI/SNF subunits in ARID1A-mutant cancers

Elife

(2017)

E.L. Miller

TOP2 synergizes with BAF chromatin remodeling for both resolution and formation of facultative heterochromatin

Nat. Struct. Mol. Biol.

(2017)

X. Bao

A novel ATAC-seq approach reveals lineage-specific reinforcement of the open chromatin landscape via cooperation between BAF and p63

Genome Biol.

(2015)

C. Bossen

The chromatin remodeler Brg1 activates enhancer repertoires to establish B cell identity and modulate cell growth

Nat. Immunol.

(2015)

J. Gatchalian

A non-canonical BRD9-containing BAF chromatin remodeling complex regulates naive pluripotency in mouse embryonic stem cells

Nat. Commun.

(2018)

B.C. Michel

A non-canonical SWI/SNF complex is a synthetic lethal target in cancers driven by BAF complex perturbation

Nat. Cell Biol.

(2018)

X. Wang

BRD9 defines a SWI/SNF sub-complex and constitutes a specific vulnerability in malignant rhabdoid tumors

Nat. Commun.

(2019)

E.A. Morrison

DNA binding drives the association of BRG1/hBRM bromodomains with nucleosomes

Nat. Commun.

(2017)

J. Pan

The ATPase module of mammalian SWI/SNF family complexes mediates subcomplex identity and catalytic activity-independent genomic targeting

Nat. Genet.

(2019)

S.T. Smale et al.

Transcriptional control of inflammatory responses

Cold Spring Harb. Perspect. Biol.

(2014)

L. Escoubet-Lozach

Mechanisms establishing TLR4-responsive activation states of inflammatory response genes

PLoS Genet.

(2011)

T. Vierbuchen

AP-1 transcription factors and the BAF complex mediate signal-dependent enhancer selection

Mol. Cell

(2017)

M. Takaku

GATA3-dependent cellular reprogramming requires activation-domain dependent recruitment of a chromatin remodeler

Genome Biol.

(2016)

A. Mancino

A dual cis-regulatory code links IRF8 to constitutive and inducible gene expression in macrophages

Genes Dev.

(2015)

Y. Zhang

A switch from hBrm to Brg1 at IFNgamma-activated sequences mediates the activation of human genes

Cell Res.

(2010)

M. Huang

Chromatin-remodelling factor BRG1 selectively activates a subset of interferon-alpha-inducible genes

Nat. Cell Biol.

(2002)

Z. Ni

Apical role for BRG1 in cytokine-induced promoter assembly

Proc. Natl. Acad. Sci. U. S. A.

(2005)

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Citation Excerpt :
The immediate consequence of TF binding to enhancers and promoters is the secondary recruitment of an intermediary set of co-activators that have key roles in modifying chromatin and mediating recruitment and/or conversion of paused RNA polymerase to an active, elongating form. These include chromatin remodeling complexes (SWI/SNF) (Gatchalian et al., 2020; Lai et al., 2009), complexes with histone acetyl transferase activity (e.g., CBP and p300), histone methyltransferases (e.g., MLL proteins [Kaikkonen et al., 2013]), histone demethylases (e.g., JMJD3 [De Santa et al., 2009]), bromodomain readers of histone acetylation (e.g., Brd4 [Nicodeme et al., 2010]), and kinase activity (e.g., pTEFb) (Hargreaves et al., 2009). The concerted actions of these complexes at enhancers result in dissociation of the negative elongation factor (NELF) complex, release of PolII from its promoter-paused position, and rapid induction of gene transcription (Adelman et al., 2009).
The development and functional potential of metazoan cells is dependent on combinatorial roles of transcriptional enhancers and promoters. Macrophages provide exceptionally powerful model systems for investigation of mechanisms underlying the activation of cell-specific enhancers that drive transitions in cell fate and cell state. Here, we review recent advances that have expanded appreciation of the diversity of macrophage phenotypes in health and disease, emphasizing studies of liver, adipose tissue, and brain macrophages as paradigms for other tissue macrophages and cell types. Studies of normal tissue-resident macrophages and macrophages associated with cirrhosis, obese adipose tissue, and neurodegenerative disease illustrate the major roles of tissue environment in remodeling enhancer landscapes to specify the development and functions of distinct macrophage phenotypes. We discuss the utility of quantitative analysis of environment-dependent changes in enhancer activity states as an approach to discovery of regulatory transcription factors and upstream signaling pathways.

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Trends in Immunology

ReviewControl of Stimulus-Dependent Responses in Macrophages by SWI/SNF Chromatin Remodeling Complexes

Highlights

Section snippets

SWI/SNF: The Story So Far

Primary versus Secondary Response Genes

New Kid on the Block: The BRD9-Containing ncBAF Complex

Enhancer Regulation by BAF Complexes

Integration of SWI/SNF Complex Functions

Pharmacological Targeting of SWI/SNF Complexes

Translational Outlook

Concluding Remarks

Acknowledgments

Glossary

J. Biol. Chem.

Cell

Cell

Cell

J. Biol. Chem.

Cell

Mol. Cell

Cell

J. Biol. Chem.

Mol. Cell

Immunity

Cell Rep.

J. Biol. Chem.

Mol. Cell

EBioMedicine

Cell Host Microbe

Blood

Cell

Mol. Cell

Biochim. Biophys. Acta

Mol. Cell

Immunity

Molecular control of activation and priming in macrophages

Nat. Immunol.

Chromatin remodeling mediated by ARID1A is indispensable for normal hematopoiesis in mice

Leukemia

Selective and antagonistic functions of SWI/SNF and Mi-2beta nucleosome remodeling complexes during an inflammatory response

Genes Dev.

Chromatin-remodeling factor SMARCD2 regulates transcriptional networks controlling differentiation of neutrophil granulocytes

Nat. Genet.

SMARCD2 subunit of SWI/SNF chromatin-remodeling complexes mediates granulopoiesis through a CEBPvarepsilon dependent mechanism

Nat. Genet.

ATP-dependent chromatin remodeling: genetics, genomics and mechanisms

Cell Res.

Heterozygous mutations in SMARCA2 reprogram the enhancer landscape by global retargeting of SMARCA4

Mol. Cell

The pioneer factor OCT4 requires the chromatin remodeller BRG1 to support gene regulatory element function in mouse embryonic stem cells

Elife

Chromatin accessibility underlies synthetic lethality of SWI/SNF subunits in ARID1A-mutant cancers

Elife

TOP2 synergizes with BAF chromatin remodeling for both resolution and formation of facultative heterochromatin

Nat. Struct. Mol. Biol.

A novel ATAC-seq approach reveals lineage-specific reinforcement of the open chromatin landscape via cooperation between BAF and p63

Genome Biol.

The chromatin remodeler Brg1 activates enhancer repertoires to establish B cell identity and modulate cell growth

Nat. Immunol.

A non-canonical BRD9-containing BAF chromatin remodeling complex regulates naive pluripotency in mouse embryonic stem cells

Nat. Commun.

A non-canonical SWI/SNF complex is a synthetic lethal target in cancers driven by BAF complex perturbation

Nat. Cell Biol.

BRD9 defines a SWI/SNF sub-complex and constitutes a specific vulnerability in malignant rhabdoid tumors

Nat. Commun.

DNA binding drives the association of BRG1/hBRM bromodomains with nucleosomes

Nat. Commun.

The ATPase module of mammalian SWI/SNF family complexes mediates subcomplex identity and catalytic activity-independent genomic targeting

Nat. Genet.

Transcriptional control of inflammatory responses

Cold Spring Harb. Perspect. Biol.

Mechanisms establishing TLR4-responsive activation states of inflammatory response genes

PLoS Genet.

AP-1 transcription factors and the BAF complex mediate signal-dependent enhancer selection

Mol. Cell

GATA3-dependent cellular reprogramming requires activation-domain dependent recruitment of a chromatin remodeler

Genome Biol.

A dual cis-regulatory code links IRF8 to constitutive and inducible gene expression in macrophages

Genes Dev.

Review
Control of Stimulus-Dependent Responses in Macrophages by SWI/SNF Chromatin Remodeling Complexes