Microenvironmental Regulation of Macrophage Transcriptomic and Metabolomic Profiles in Pulmonary Hypertension Article Swipe
Min Li
,
Suzette Riddle
,
Sushil Kumar
,
Joanna M. Poczobutt
,
B.A. McKeon
,
Maria G. Frid
,
Maureen J. Ostaff
,
Julie A. Reisz
,
Travis Nemkov
,
Mehdi A. Fini
,
A. Laux
,
Cheng‐Jun Hu
,
Karim C. El Kasmi
,
Angelo D’Alessandro
,
R. Dale Brown
,
Hui Zhang
,
Kurt R. Stenmark
·
YOU?
·
· 2021
· Open Access
·
· DOI: https://doi.org/10.3389/fimmu.2021.640718
YOU?
·
· 2021
· Open Access
·
· DOI: https://doi.org/10.3389/fimmu.2021.640718
The recruitment and subsequent polarization of inflammatory monocytes/macrophages in the perivascular regions of pulmonary arteries is a key feature of pulmonary hypertension (PH). However, the mechanisms driving macrophage polarization within the adventitial microenvironment during PH progression remain unclear. We previously established that reciprocal interactions between fibroblasts and macrophages are essential in driving the activated phenotype of both cell types although the signals involved in these interactions remain undefined. We sought to test the hypothesis that adventitial fibroblasts produce a complex array of metabolites and proteins that coordinately direct metabolomic and transcriptomic re-programming of naïve macrophages to recapitulate the pathophysiologic phenotype observed in PH. Media conditioned by pulmonary artery adventitial fibroblasts isolated from pulmonary hypertensive (PH-CM) or age-matched control (CO-CM) calves were used to activate bone marrow derived macrophages. RNA-Seq and mass spectrometry-based metabolomics analyses were performed. Fibroblast conditioned medium from patients with idiopathic pulmonary arterial hypertension or controls were used to validate transcriptional findings. The microenvironment was targeted in vitro using a fibroblast-macrophage co-culture system and in vivo in a mouse model of hypoxia-induced PH. Both CO-CM and PH-CM actively, yet distinctly regulated macrophage transcriptomic and metabolomic profiles. Network integration revealed coordinated rewiring of pro-inflammatory and pro-remodeling gene regulation in concert with altered mitochondrial and intermediary metabolism in response to PH-CM. Pro-inflammation and metabolism are key regulators of macrophage phenotype in vitro , and are closely related to in vivo flow sorted lung interstitial/perivascular macrophages from hypoxic mice. Metabolic changes are accompanied by increased free NADH levels and increased expression of a metabolic sensor and transcriptional co-repressor, C-terminal binding protein 1 (CtBP1), a mechanism shared with adventitial PH-fibroblasts. Targeting the microenvironment created by both cell types with the CtBP1 inhibitor MTOB, inhibited macrophage pro-inflammatory and metabolic re-programming both in vitro and in vivo . In conclusion, coordinated transcriptional and metabolic reprogramming is a critical mechanism regulating macrophage polarization in response to the complex adventitial microenvironment in PH. Targeting the adventitial microenvironment can return activated macrophages toward quiescence and attenuate pathological remodeling that drives PH progression.
Related Topics
Concepts
Transcriptome
Macrophage polarization
Macrophage
Metabolomics
Pulmonary hypertension
Inflammation
Biology
Cell biology
Phenotype
In vivo
In vitro
Hypoxia (environmental)
Fibroblast
Chemistry
Immunology
Medicine
Bioinformatics
Internal medicine
Biochemistry
Gene expression
Gene
Genetics
Organic chemistry
Oxygen
Metadata
- Type
- article
- Language
- en
- Landing Page
- https://doi.org/10.3389/fimmu.2021.640718
- OA Status
- gold
- Cited By
- 32
- References
- 53
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W3149603318
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
-
https://openalex.org/W3149603318Canonical identifier for this work in OpenAlex
- DOI
-
https://doi.org/10.3389/fimmu.2021.640718Digital Object Identifier
- Title
-
Microenvironmental Regulation of Macrophage Transcriptomic and Metabolomic Profiles in Pulmonary HypertensionWork title
- Type
-
articleOpenAlex work type
- Language
-
enPrimary language
- Publication year
-
2021Year of publication
- Publication date
-
2021-03-31Full publication date if available
- Authors
-
Min Li, Suzette Riddle, Sushil Kumar, Joanna M. Poczobutt, B.A. McKeon, Maria G. Frid, Maureen J. Ostaff, Julie A. Reisz, Travis Nemkov, Mehdi A. Fini, A. Laux, Cheng‐Jun Hu, Karim C. El Kasmi, Angelo D’Alessandro, R. Dale Brown, Hui Zhang, Kurt R. StenmarkList of authors in order
- Landing page
-
https://doi.org/10.3389/fimmu.2021.640718Publisher landing page
- Open access
-
YesWhether a free full text is available
- OA status
-
goldOpen access status per OpenAlex
- OA URL
-
https://doi.org/10.3389/fimmu.2021.640718Direct OA link when available
- Concepts
-
Transcriptome, Macrophage polarization, Macrophage, Metabolomics, Pulmonary hypertension, Inflammation, Biology, Cell biology, Phenotype, In vivo, In vitro, Hypoxia (environmental), Fibroblast, Chemistry, Immunology, Medicine, Bioinformatics, Internal medicine, Biochemistry, Gene expression, Gene, Genetics, Organic chemistry, OxygenTop concepts (fields/topics) attached by OpenAlex
- Cited by
-
32Total citation count in OpenAlex
- Citations by year (recent)
-
2025: 6, 2024: 8, 2023: 7, 2022: 7, 2021: 4Per-year citation counts (last 5 years)
- References (count)
-
53Number of works referenced by this work
- Related works (count)
-
10Other works algorithmically related by OpenAlex
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