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Macrophage Polarization: Learning to Manage It

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Immunology".

Deadline for manuscript submissions: closed (30 April 2022) | Viewed by 51144

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Dr. Nadia Lampiasi

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Istituto per la Ricerca e l’Innovazione Biomedica (IRIB), Consiglio Nazionale delle Ricereche (CNR), 00185 Rome, Italy
Interests: inflammation; innate immunity; macrophages; mast cells; osteoimmunology
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Dear colleagues,

Macrophages are crucial components of innate immunity. They possess high plasticity and the ability to differentiate in response to numerous stimuli. The physiological and/or pathological conditions characterize the environment in which the macrophages reside, and determine their heterogeneity. There is a plethora of different specialized functional phenotypes, among which inflammatory (M1) and reparative (M2) subtypes are proposed, which are almost exactly opposite to each other. Two key cytokines, IFN-γ and TNF-α, are responsible for M1, or classical activation, while alternate activation in M2 is mediated mainly by IL-4 and IL-13. Interestingly, microRNAs and some immunomodulators are critical regulators of macrophage polarization. The link with many human diseases and infections, including cancer, autoimmunity, and periodontitis, is to be found in the dysregulation of macrophage plasticity. Furthermore, recent studies on naturally occurring compounds emphasize their regulatory effects on macrophage polarization, suggesting that some of them could be promising for the treatment of sensitive diseases.

This Special Issue aims to cover all areas of molecular research, but is not limited to this, as it may include clinical studies with biomolecular experiments.

Dr. Nadia Lampiasi
Guest Editor

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Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. International Journal of Molecular Sciences is an international peer-reviewed open access semimonthly journal published by MDPI.

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Keywords

macrophages
macrophage plasticity
macrophage polarization
innate immunity
IFN-γ
TNF-α
immunomodulators

Related Special Issue

Macrophage Polarization: Learning to Manage It 3.0 in International Journal of Molecular Sciences (7 articles)

Published Papers (13 papers)

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Editorial

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4 pages, 776 KiB

Open AccessEditorial

Macrophage Polarization: Learning to Manage It

by Nadia Lampiasi

Int. J. Mol. Sci. 2022, 23(13), 7208; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23137208 - 29 Jun 2022

Cited by 3 | Viewed by 1839

Abstract

To date, four reviews and seven experimental articles have been published in this Special Issue [...] Full article

(This article belongs to the Special Issue Macrophage Polarization: Learning to Manage It)

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Research

Jump to: Editorial, Review

21 pages, 4404 KiB

Open AccessArticle

Dealing with Macrophage Plasticity to Address Therapeutic Challenges in Head and Neck Cancers

by Sonia Furgiuele, Géraldine Descamps, Lorena Cascarano, Ambre Boucq, Christine Dubois, Fabrice Journe and Sven Saussez

Int. J. Mol. Sci. 2022, 23(12), 6385; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23126385 - 07 Jun 2022

Cited by 7 | Viewed by 2844

Abstract

The head and neck tumor microenvironment (TME) is highly infiltrated with macrophages. More specifically, tumor-associated macrophages (TAM/M2-like) are one of the most critical components associated with poor overall survival in head and neck cancers (HNC). Two extreme states of macrophage phenotypes are described as conducting pro-inflammatory/anti-tumoral (M1) or anti-inflammatory/pro-tumoral (M2) activities. Moreover, specific metabolic pathways as well as oxidative stress responses are tightly associated with their phenotypes and functions. Hence, due to their plasticity, targeting M2 macrophages to repolarize in the M1 phenotype would be a promising cancer treatment. In this context, we evaluated macrophage infiltration in 60 HNC patients and demonstrated the high infiltration of CD68+ cells that were mainly related to CD163+ M2 macrophages. We then optimized a polarization protocol from THP1 monocytes, validated by specific gene and protein expression levels. In addition, specific actors of glutamine pathway and oxidative stress were quantified to indicate the use of glutaminolysis by M2 and the production of reactive oxygen species by M1. Finally, we evaluated and confirmed the plasticity of our model using M1 activators to repolarize M2 in M1. Overall, our study provides a complete reversible polarization protocol allowing us to further evaluate various reprogramming effectors targeting glutaminolysis and/or oxidative stress in macrophages. Full article

(This article belongs to the Special Issue Macrophage Polarization: Learning to Manage It)

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18 pages, 23492 KiB

Open AccessArticle

A Short ERAP2 That Binds IRAP Is Expressed in Macrophages Independently of Gene Variation

by Benedetta Mattorre, Silvana Caristi, Simona Donato, Emilia Volpe, Marika Faiella, Alessandro Paiardini, Rosa Sorrentino and Fabiana Paladini

Int. J. Mol. Sci. 2022, 23(9), 4961; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23094961 - 29 Apr 2022

Cited by 5 | Viewed by 2096

Abstract

The M1 zinc metalloproteases ERAP1, ERAP2, and IRAP play a role in HLA-I antigen presentation by refining the peptidome either in the ER (ERAP1 and ERAP2) or in the endosomes (IRAP). They have also been entrusted with other, although less defined, functions such as the regulation of the angiotensin system and blood pressure. In humans, ERAP1 and IRAP are commonly expressed. ERAP2 instead has evolved under balancing selection that maintains two haplotypes, one of which undergoing RNA splicing leading to nonsense-mediated decay and loss of protein. Hence, likewise in rodents, wherein the ERAP2 gene is missing, about a quarter of the human population does not express ERAP2. We report here that macrophages, but not monocytes or other mononuclear blood cells, express and secrete an ERAP2 shorter form independent of the haplotype. The generation of this “short” ERAP2 is due to an autocatalytic cleavage within a distinctive structural motif and requires an acidic micro-environment. Remarkably, ERAP2 “short” binds IRAP and the two molecules are co-expressed in the endosomes as well as in the cell membrane. Of note, the same phenomenon could be observed in some cancer cells. These data prompt us to reconsider the role of ERAP2, which might have been maintained in humans due to fulfilling a relevant function in its “short” form. Full article

(This article belongs to the Special Issue Macrophage Polarization: Learning to Manage It)

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14 pages, 963 KiB

Open AccessArticle

Accelerated Generation of Extra-Islet Insulin-Producing Cells in Diabetic Rats, Treated with Sodium Phthalhydrazide

by Musa T. Abidov, Ksenia V. Sokolova, Irina F. Gette and Irina G. Danilova

Int. J. Mol. Sci. 2022, 23(8), 4286; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23084286 - 13 Apr 2022

Cited by 2 | Viewed by 1831

Abstract

β-cells dysfunction plays an important role in the pathogenesis of type 2 diabetes (T2D), partially may be compensated by the generation of extra-islet insulin-producing cells (IPCs) in pancreatic acini and ducts. Pdx1 expression and inflammatory level are suggested to be involved in the generation of extra-islet IPCs, but the exact reasons and mechanisms of it are unclear. Macrophages are key inflammatory mediators in T2D. We studied changes in mass and characteristics of extra-islet IPCs in rats with a streptozotocin-nicotinamide model of T2D and after i.m. administration of 20 daily doses of 2 mg/kg b.w. sodium aminophthalhydrazide (APH). Previously, we found that APH modulates macrophage production and increases the proliferative activity of pancreatic β-cells. Expressions of insulin and Pdx1, as well as F4/80 (macrophage marker), were detected at the protein level by immunohistochemistry analysis, the concentration of pro- and anti-inflammatory cytokines in blood and pancreas—by ELISA. Diabetic rats treated with APH showed an increasing mass of extra-islet IPCs and the content of insulin in them. The presence of Pdx1⁺ cells in the exocrine pancreas also increased. F4/80⁺ cell reduction was accompanied by increasing TGF-β1 content. Interestingly, during the development of diabetes, the mass of β-cells decreased faster than the mass of extra-islet IPCs, and extra-islet IPCs reacted to experimental T2D differently depending on their acinar or ductal location. Full article

(This article belongs to the Special Issue Macrophage Polarization: Learning to Manage It)

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20 pages, 4097 KiB

Open AccessArticle

Statins and Bempedoic Acid: Different Actions of Cholesterol Inhibitors on Macrophage Activation

by Rebecca Linnenberger, Jessica Hoppstädter, Selina Wrublewsky, Emmanuel Ampofo and Alexandra K. Kiemer

Int. J. Mol. Sci. 2021, 22(22), 12480; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms222212480 - 19 Nov 2021

Cited by 10 | Viewed by 3231

Abstract

Statins represent the most prescribed class of drugs for the treatment of hypercholesterolemia. Effects that go beyond lipid-lowering actions have been suggested to contribute to their beneficial pharmacological properties. Whether and how statins act on macrophages has been a matter of debate. In the present study, we aimed at characterizing the impact of statins on macrophage polarization and comparing these to the effects of bempedoic acid, a recently registered drug for the treatment of hypercholesterolemia, which has been suggested to have a similar beneficial profile but fewer side effects. Treatment of primary murine macrophages with two different statins, i.e., simvastatin and cerivastatin, impaired phagocytotic activity and, concurrently, enhanced pro-inflammatory responses upon short-term lipopolysaccharide challenge, as characterized by an induction of tumor necrosis factor (TNF), interleukin (IL) 1β, and IL6. In contrast, no differences were observed under long-term inflammatory (M1) or anti-inflammatory (M2) conditions, and neither inducible NO synthase (iNOS) expression nor nitric oxide production was altered. Statin treatment led to extracellular-signal regulated kinase (ERK) activation, and the pro-inflammatory statin effects were abolished by ERK inhibition. Bempedoic acid only had a negligible impact on macrophage responses when compared with statins. Taken together, our data point toward an immunomodulatory effect of statins on macrophage polarization, which is absent upon bempedoic acid treatment. Full article

(This article belongs to the Special Issue Macrophage Polarization: Learning to Manage It)

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16 pages, 3320 KiB

Open AccessArticle

Acute Inflammatory Response in Osteoporotic Fracture Healing Augmented with Mechanical Stimulation is Regulated In Vivo through the p38-MAPK Pathway

by Simon Kwoon Ho Chow, Can Cui, Keith Yu Kin Cheng, Yu Ning Chim, Jinyu Wang, Carissa Hing Wai Wong, Ka Wai Ng, Ronald Man Yeung Wong and Wing Hoi Cheung

Int. J. Mol. Sci. 2021, 22(16), 8720; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22168720 - 13 Aug 2021

Cited by 8 | Viewed by 2781

Abstract

Low-magnitude high-frequency vibration (LMHFV) has previously been reported to modulate the acute inflammatory response of ovariectomy-induced osteoporotic fracture healing. However, the underlying mechanisms are not clear. In the present study, we investigated the effect of LMHFV on the inflammatory response and the role of the p38 MAPK mechanical signaling pathway in macrophages during the healing process. A closed femoral fracture SD rat model was used. In vivo results showed that LMHFV enhanced activation of the p38 MAPK pathway at the fracture site. The acute inflammatory response, expression of inflammatory cytokines, and callus formation were suppressed in vivo by p38 MAPK inhibition. However, LMHFV did not show direct in vitro enhancement effects on the polarization of RAW264.7 macrophage from the M1 to M2 phenotype, but instead promoted macrophage enlargement and transformation to dendritic monocytes. The present study demonstrated that p38 MAPK modulated the enhancement effects of mechanical stimulation in vivo only. LMHFV may not have exerted its enhancement effects directly on macrophage, but the exact mechanism may have taken a different pathway that requires further investigation in the various subsets of immune cells. Full article

(This article belongs to the Special Issue Macrophage Polarization: Learning to Manage It)

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13 pages, 21573 KiB

Open AccessArticle

Immunonutritional Protease Inhibitors from T. durum and A. sativa Display Metabolic Similarities When Assayed on Human Macrophage-like Cells

by Bartosz Fotschki, Aurora Garcia Tejedor, Juan Antonio Nieto Fuentes and Jose Moisés Laparra Llopis

Int. J. Mol. Sci. 2021, 22(15), 8307; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22158307 - 02 Aug 2021

Cited by 2 | Viewed by 2003

Abstract

This study evaluated the immunonutritional effects caused by protease inhibitors from Avena sativa and Triticum durum to human macrophage-like cells. Macrophages were exposed (3 h) to extracts obtained from flours, and mitochondrial-associated oxygen consumption rates and inflammatory, metabolic, and proteome adaptations were quantified. Mass spectrometry ‘m/z’ signals of the extracts obtained from T. durum and A. sativa revealed molecular weights of 18–35 kDa and 16–22 kDa, respectively, for the compounds present at highest concentrations. Extracts from T. durum exhibited lower susceptibility to degradation by gastrointestinal enzymes than those from A. sativa: 9.5% vs 20.2%. Despite their different botanical origin, both extracts increased TLR4 expression. Metabolic protein levels were indicative of a decreased glycolytic to lactate flux in cell cultures upon stimulation with A. sativa extracts, which improved mitochondrial respiration in relation to those from T. durum. Principal components analysis confirmed relative similarities between immune–metabolic events triggered by immunonutritional ingredients in T. durum and A. sativa. Collectively, immunonutritional effects help to interpret the differences between both crops, worsening or improving, macrophage immune reactivity (tolerogenicity), and better control of inflammatory processes. Full article

(This article belongs to the Special Issue Macrophage Polarization: Learning to Manage It)

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18 pages, 1324 KiB

Open AccessArticle

Cytokine/Chemokine Release Patterns and Transcriptomic Profiles of LPS/IFNγ-Activated Human Macrophages Differentiated with Heat-Killed Mycobacterium obuense, M-CSF, or GM-CSF

by Samer Bazzi, Emale El-Darzi, Tina McDowell, Helmout Modjtahedi, Satvinder Mudan, Marcel Achkar, Charles Akle, Humam Kadara and Georges M. Bahr

Int. J. Mol. Sci. 2021, 22(13), 7214; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22137214 - 05 Jul 2021

Cited by 3 | Viewed by 2977

Abstract

Macrophages (Mφs) are instrumental regulators of the immune response whereby they acquire diverse functional phenotypes following their exposure to microenvironmental cues that govern their differentiation from monocytes and their activation. The complexity and diversity of the mycobacterial cell wall have empowered mycobacteria with potent immunomodulatory capacities. A heat-killed (HK) whole-cell preparation of Mycobacterium obuense (M. obuense) has shown promise as an adjunctive immunotherapeutic agent for the treatment of cancer. Moreover, HK M. obuense has been shown to trigger the differentiation of human monocytes into a monocyte-derived macrophage (MDM) type named Mob-MDM. However, the transcriptomic profile and functional properties of Mob-MDMs remain undefined during an activation state. Here, we characterized cytokine/chemokine release patterns and transcriptomic profiles of lipopolysaccharide (LPS)/interferon γ (IFNγ)-activated human MDMs that were differentiated with HK M. obuense (Mob-MDM(LPS/IFNγ)), macrophage colony-stimulating factor M-MDM(LPS/IFNγ)), or granulocyte/macrophage colony-stimulating factor (GM-MDM(LPS/IFNγ)). Mob-MDM(LPS/IFNγ) demonstrated a unique cytokine/chemokine release pattern (interleukin (IL)-10^low, IL-12/23p40^low, IL-23p19/p40^low, chemokine (C-x-C) motif ligand (CXCL)9^low) that was distinct from those of M-MDM(LPS/IFNγ) and GM-MDM(LPS/IFNγ). Furthermore, M-MDM(LPS/IFNγ) maintained IL-10 production at significantly higher levels compared to GM-MDM(LPS/IFNγ) and Mob-MDM(LPS/IFNγ) despite being activated with M1-Mφ-activating stimuli. Comparative RNA sequencing analysis pointed to a distinct transcriptome profile for Mob-MDM(LPS/IFNγ) relative to both M-MDM(LPS/IFNγ) and GM-MDM(LPS/IFNγ) that comprised 417 transcripts. Functional gene-set enrichment analysis revealed significant overrepresentation of signaling pathways and biological processes that were uniquely related to Mob-MDM(LPS/IFNγ). Our findings lay a foundation for the potential integration of HK M. obuense in specific cell-based immunotherapeutic modalities such as adoptive transfer of Mφs (Mob-MDM(LPS/IFNγ)) for cancer treatment. Full article

(This article belongs to the Special Issue Macrophage Polarization: Learning to Manage It)

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21 pages, 5123 KiB

Open AccessArticle

Exploring the Biomaterial-Induced Secretome: Physical Bone Substitute Characteristics Influence the Cytokine Expression of Macrophages

by Mike Barbeck, Marie-Luise Schröder, Said Alkildani, Ole Jung and Ronald E. Unger

Int. J. Mol. Sci. 2021, 22(9), 4442; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22094442 - 24 Apr 2021

Cited by 12 | Viewed by 2441

Abstract

In addition to their chemical composition various physical properties of synthetic bone substitute materials have been shown to influence their regenerative potential and to influence the expression of cytokines produced by monocytes, the key cell-type responsible for tissue reaction to biomaterials in vivo. In the present study both the regenerative potential and the inflammatory response to five bone substitute materials all based on β-tricalcium phosphate (β-TCP), but which differed in their physical characteristics (i.e., granule size, granule shape and porosity) were analyzed for their effects on monocyte cytokine expression. To determine the effects of the physical characteristics of the different materials, the proliferation of primary human osteoblasts growing on the materials was analyzed. To determine the immunogenic effects of the different materials on human peripheral blood monocytes, cells cultured on the materials were evaluated for the expression of 14 pro- and anti-inflammatory cytokines, i.e., IL-6, IL-10, IL-1β, VEGF, RANTES, IL-12p40, I-CAM, IL-4, V-CAM, TNF-α, GM-CSF, MIP-1α, Il-8 and MCP-1 using a Bio-Plex^® Multiplex System. The granular shape of bone substitutes showed a significant influence on the osteoblast proliferation. Moreover, smaller pore sizes, round granular shape and larger granule size increased the expression of GM-CSF, RANTES, IL-10 and IL-12 by monocytes, while polygonal shape and the larger pore sizes increased the expression of V-CAM. The physical characteristics of a bone biomaterial can influence the proliferation rate of osteoblasts and has an influence on the cytokine gene expression of monocytes in vitro. These results indicate that the physical structure of a biomaterial has a significant effect of how cells interact with the material. Thus, specific characteristics of a material may strongly affect the regenerative potential in vivo. Full article

(This article belongs to the Special Issue Macrophage Polarization: Learning to Manage It)

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Review

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25 pages, 2496 KiB

Open AccessReview

Interactions between Macrophages and Mast Cells in the Female Reproductive System

by Nadia Lampiasi

Int. J. Mol. Sci. 2022, 23(10), 5414; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23105414 - 12 May 2022

Cited by 11 | Viewed by 3722

Abstract

Mast cells (MCs) and macrophages (Mϕs) are innate immune cells that differentiate from early common myeloid precursors and reside in all body tissues. MCs have a unique capacity to neutralize/degrade toxic proteins, and they are hypothesized as being able to adopt two alternative polarization profiles, similar to Mϕs, with distinct or even opposite roles. Mϕs are very plastic phagocytic cells that are devoted to the elimination of senescent/anomalous endogenous entities (to maintain tissue homeostasis), and to the recognition and elimination of exogenous threats. They can adopt several functional phenotypes in response to microenvironmental cues, whose extreme profiles are the inflammatory/killing phenotype (M1) and the anti-inflammatory/healing phenotype (M2). The concomitant and abundant presence of these two cell types and the partial overlap of their defensive and homeostatic functions leads to the hypothesis that their crosstalk is necessary for the optimal coordination of their functions, both under physiological and pathological conditions. This review will examine the relationship between MCs and Mϕs in some situations of homeostatic regulation (menstrual cycle, embryo implantation), and in some inflammatory conditions in the same organs (endometriosis, preeclampsia), in order to appreciate the importance of their cross-regulation. Full article

(This article belongs to the Special Issue Macrophage Polarization: Learning to Manage It)

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26 pages, 2944 KiB

Open AccessReview

Repolarization of Unbalanced Macrophages: Unmet Medical Need in Chronic Inflammation and Cancer

by Yannick Degboé, Rémy Poupot and Mary Poupot

Int. J. Mol. Sci. 2022, 23(3), 1496; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23031496 - 28 Jan 2022

Cited by 15 | Viewed by 3777

Abstract

Monocytes and their tissue counterpart macrophages (MP) constitute the front line of the immune system. Indeed, they are able to rapidly and efficiently detect both external and internal danger signals, thereby activating the immune system to eradicate the disturbing biological, chemical, or physical agents. They are also in charge of the control of the immune response and account for the repair of the damaged tissues, eventually restoring tissue homeostasis. The balance between these dual activities must be thoroughly controlled in space and time. Any sustained unbalanced response of MP leads to pathological disorders, such as chronic inflammation, or favors cancer development and progression. In this review, we take advantage of our expertise in chronic inflammation, especially in rheumatoid arthritis, and in cancer, to highlight the pivotal role of MP in the physiopathology of these disorders and to emphasize the repolarization of unbalanced MP as a promising therapeutic strategy to control these diseases. Full article

(This article belongs to the Special Issue Macrophage Polarization: Learning to Manage It)

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13 pages, 1402 KiB

Open AccessReview

Macrophage Polarity and Disease Control

by Suguru Kadomoto, Kouji Izumi and Atsushi Mizokami

Int. J. Mol. Sci. 2022, 23(1), 144; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23010144 - 23 Dec 2021

Cited by 89 | Viewed by 13268

Abstract

Macrophages are present in most human tissues and have very diverse functions. Activated macrophages are usually divided into two phenotypes, M1 macrophages and M2 macrophages, which are altered by various factors such as microorganisms, tissue microenvironment, and cytokine signals. Macrophage polarity is very important for infections, inflammatory diseases, and malignancies; its management can be key in the prevention and treatment of diseases. In this review, we assess the current state of knowledge on macrophage polarity and report on its prospects as a therapeutic target. Full article

(This article belongs to the Special Issue Macrophage Polarization: Learning to Manage It)

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30 pages, 1008 KiB

Open AccessReview

The Macrophage Iron Signature in Health and Disease

by Christina Mertens, Oriana Marques, Natalie K. Horvat, Manuela Simonetti, Martina U. Muckenthaler and Michaela Jung

Int. J. Mol. Sci. 2021, 22(16), 8457; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22168457 - 06 Aug 2021

Cited by 15 | Viewed by 5162

Abstract

Throughout life, macrophages are located in every tissue of the body, where their main roles are to phagocytose cellular debris and recycle aging red blood cells. In the tissue niche, they promote homeostasis through trophic, regulatory, and repair functions by responding to internal and external stimuli. This in turn polarizes macrophages into a broad spectrum of functional activation states, also reflected in their iron-regulated gene profile. The fast adaptation to the environment in which they are located helps to maintain tissue homeostasis under physiological conditions. Full article

(This article belongs to the Special Issue Macrophage Polarization: Learning to Manage It)

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