Monocytes and Macrophages as Viral Targets and Reservoirs
Abstract
:1. Introduction
2. Monocytes and Tissue Macrophages
3. Viruses Infect Monocytes and Macrophages
4. Viral Entry into Monocytes and Macrophages
5. Productive Viral Infection
6. Latent Viral Infection and Inflammation
7. Macrophages as a Target for Therapeutic Intervention
8. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
Mo | Monocyte |
Mφ | Macrophage |
MDM | Monocyte-derived macrophages |
HC | Hofbauer cells |
HIV | Human immunodeficiency virus |
HCMV | Human cytomegalovirus |
RSV | Respiratory syncytial virus |
VSV | Vesicular stomatitis virus |
dsDNA | Double stranded DNA |
ssRNA | Single stranded RNA |
CSFV | Classical swine fever virus |
EMCV | Encephalomyocarditis virus |
MHV | Mouse hepatitis virus |
ZIKV | Zika virus |
MVV | Maedi-visna virus |
EBV | Epstein-Barr virus |
KSHV | Kaposi’s sarcoma-associated herpesvirus |
HHV-6 | Human herpesvirus 6 |
VZV | Simian varicella-zoster virus |
JEV | Japanese encephalitis virus |
AIDS | Acquired immune deficiency syndrome |
CHIKV | Chikungunya alphavirus |
TMEV | Theiler’s murine encephalomyelitis virus |
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Virus | Family | Genome | Host | Disease | Model | Type of Cells | Virus Persistence and Survival in Mφ | Reaction of Mφ | Reference | |
---|---|---|---|---|---|---|---|---|---|---|
1 | Respiratory syncytial virus (RSV) | Paramyxoviridae | (−) ssRNA | Human | Bronchiolitis and pneumonia, severe acute lower-respiratory tract disease in children | -In vitro model of persistently RSV-infected Mφ-like cell line P388D1 (MφP) -RAW264.7 Mφ -Human tissue Mφ | -Murine Mφ-cell line -Human alveolar Mφ | -RSV persist in in vitro model for over 87 passages. -Alveolar Mφ support a productive RSV infection in vitro at least for 25 days. -Lack of response of infected Mφ to the IFN-beta. | -Infected Mφ produces high level of proinflammatory cytokines (class II HLA-DR, IL-1ß and TNFα—immunofluorescent staining). -Reduced cytotoxic effect in MφP cells (activation of caspase-9 along with impairment of caspase-8 activity). | [26,27,28] |
2 | Influenza virus | Orthomyxoviridae | (−) ssRNA | Human | Influenza | -Autopsies -In vitro model, BALB/c mice -Human primary Mφ | -Mouse lung Mφ -Human primary Mφ | -Low virulence persistence of influenza virus in the alveolar Mφ. -Productive replication of H5N1 virus in alveolar Mφ. | -Infected Mφ produces high level IL-1ß, IL-6, TNFα (flow cytometry). -Mφ demonstrated no cytopathic changes (visual examination of monolayers). | [29,30,31] |
3 | Vesicular stomatitis virus (VSV) | Rhabdoviridae | (−) ssRNA | Insects, cattle, horses, pigs (zoonotic virus) | Flu-like illness in infected humans | BALB/c mice | Tissue Mφ (lymph nodes, lungs, spleens, liver, muscle) | -Mφ are not the major reservoirs of VSV gRNA at late times (>60 days). -No replication in Mφ. | NS | [32] |
4 | Porcine reproductive and respiratory syndrome virus (PRRSV) | Arteriviridae | (+) ssRNA | Pig | Respiratory syndrome | Pig | Porcine alveolar Mφ | Productive replication of virus in alveolar Mφ in in vivo model. | In vitro infected Mφ are protected against complement-mediated cell lysis. | [23] |
5 | Feline coronavirus (FCoV) | Coronaviridae | (+) ssRNA | Cats | Infectious peritonitis | Specific-pathogen-free cats | Tissue Mφ | Virus persists in tissue Mφ (mostly in colon) up to 80 days after inoculation. | NS | [33] |
6 | Mouse hepatitis virus (MHV) | Coronaviridae | (+) ssRNA | Mouse | Model of multiple sclerosis | Mouse | Mouse peritoneal Mφ | -Mφ disseminate virus into CNS. -Mouse peritoneal Mφ are permissive for virus. Virus persists in the cells up to 8 months. | Infected Mφ express CCR1, CCR2 and CCR5 that lead to recruitment of Mφ into the CNS. | [34,35] |
7 | Classical swine fever virus (CSFV) | Flaviviridae | (+) ssRNA | Swine | Lethal fever | Pig tissue monocytes and Mφ | Tissue monocytes and Mφ | Productive replication of virus in alveolar Mφ and monocytes. | NS | [36] |
8 | Hepatitis C virus (HCV) | Flaviviridae | (+) ssRNA | Human | Hepatitis C | -Patients -Cell culture (THP-1)/tissue Mφ | -PBMC, Mφ culture (THP-1), microglial Mφ (CD68+ and CD45+) | -HCV persists in liver Mφ and lymphocytes for up to 9 years. -Productive replication of virus in a relatively non-specific manner in Mφ. | Infected Mφ/microglial cells express higher level of IL-1α, TNFα, IL-1β, IL-12, IL-18 (PCR analysis). | [37,38] |
9 | Japanese encephalitis virus (JEV), West Nile virus (WNV), Dengue virus (DENV) | Flaviviridae | (+) ssRNA | Human | Neurotropic, CNS | -Raw264.7 cells -BALB/c mice -Macaques | -Murine monocyte-derived Mφ (MDM) -Perivascular Mφ | -Productive JEV and WNV replication in murine and human Mφ. -Intracellular persistence of virus in Mφ. -Flaviviruses evade and/or subvert the Mφ response to favour survival and replication. | -Infected Mφ produce TNF-α, IL-6, IFN-α and CCL2, inducible nitric oxide synthase (iNOS) and nitrotyrosine (NT) in response to JEV in vitro (immunofluorescent staining, IFN bioassay, Cytometric Bead Array). -Both human and rodent microglia produce CCL2, CXCL9 and CXCL10 upon JEV exposure (flow cytometry). | [22,39,40] |
10 | Zika virus (ZIKV) | Flaviviridae | (+) ssRNA | Human | Foetal brain abnormalities and microcephaly, Guillain–Barré syndrome | Primary human placental Mφ | Human placental Mφ (Hofbauer cells, HC) | -Hofbauer cells are permissive to productive ZIKV infection. | Infected HCs produce high level of IFNα, IL-6, chemokines MCP-1 and IP-10 (flow cytometry). | [41] |
11 | Coxsackieviruses (CVB4, CVB3) | Picornaviridae | (+) ssRNA | Human | -Type 1 diabetes; -Myocarditis | -Human MDM; -Mouse | -MDM -Pancreas Mφ -Myocardial Mφ (activation of JAK1-STAT1 and JAK3-STAT6 pathways) | -CVB4 replicates and persist in MDM and tissue Mφ. | -CVB4-infected Mφ produce high levels of pro-inflammatory cytokines (IL-6 and TNFα—ELISA) in both M-CSF MDM and GM-CSF MDM cultures. -Virus infected pancreas Mφ showed M1 polarization (Ly-6C+/CD115+—flow cytometry). -Mφ polarization depends on gender (M1 phenotype detected in males and M2a phenotype in females). | [42,43,44] |
12 | Encephalomyocarditis virus (EMCV) | Picornaviridae | (+) ssRNA | Rodents, pigs | -Lethal acute myocarditis, fatal illness in primates and captive wild animals | -Mouse tissue Mφ -RAW264.7, naive mouse Mφ | -Tissue Mφ (brain, heart, pancreas, kidney, Peyer’s patches, spleen, lung and thymus) | -Virus persists in the thymus Mφ up to 62 days post infection. -Productive viral replication in Mφ. | EMCV activates pro-inflammatory signalling in Mφ within minutes during virus infection and type I IFNs response afterwards. | [24,45] |
13 | Theiler’s murine encephalomyelitis virus (TMEV) | Picornaviridae | (+) ssRNA | Mouse | Skeletal muscle infection and inflammation, encephalomyelitis and multiple sclerosis, epilepsy | -J774.1 Mφ -RAW264.7 Mφ cell line -C57BL/6 (B6) mouse -Primary peritoneal Mφ | Mφ cell lines, tissue Mφ | -TMEV persists in Mφ during the chronic demyelinating phase. -Productive replication of TMEV in Mφ. | -Infected Mφ in wild type animals showed M1 polarization (CD45+CD11b+Ly6c+) while muscle-infiltrating Mφ displayed an immature phenotype in SHP-1-deficient mice (flow cytometry). -Infected peritoneal Mφ produce high level of IFNα and TNFα (ELISA). -TMEV replication cause restricted induced apoptosis of Mφ. | [16,46,47,48] |
14 | Chikungunya alphavirus (CHIKV) | Togaviridae | (+) ssRNA | Human | Articular disease/ myalgia | -Cell line -Patients -Immunocompetent cynomolgus macaques | -RAW264.7 Mφ -Perivascular synovial Mφ | -Productive replication of CHIKV in RAW264.7 Mφ but in in vivo—low viral replication and release of non-infectious viral particles. -Virus persists in the cells after 18 months of chronic disease. -Mφ are the main cellular reservoirs during the late stages of CHIKV infection in vivo. | No induced apoptosis in infected RAW264.7 cells. | [19,49,50] |
15 | Sindbis virus (SINV), Mayaro virus (MAYV), O’nyong-nyong virus (ONNV) and Barmah Forest virus (BFV), Ross River virus (RRV), CHIKV | Togaviridae | (+) ssRNA | Mosquitoes, marsupials, humans | Articular disease/myalgia | -Patients -RAW 264.7 Mφ | -RAW264.7 Mφ -Perivascular synovial Mφ | -Productive viral gene expression in synovial Mφ. -RRV persist in RAW 264.7 Mφ up to 170 days in vitro. | -Infected Mφ displayed M1 polarization (CD68+) in vivo. -CHIKV infection cause induced apoptosis in vivo leading to viral dissemination into apoptotic blebs. -CHIKV-infected RAW264.7 Mφ showed high production of TNF-α, IL-6 and GM-CSF (QPCR). -RRV-infected Mφ in vitro displayed restricted cytopathic effects. | [20,51,52,53] |
16 | Avian oncoviruses | Retroviridae | ssRNA-RT | Many species | Cancer | Chicken | Tissue Mφ, MDM | -Avian leukosis viruses persist in Mφ of peripheral blood up to about 3 years. -Avian sarcoma viruses were never found in Mφ. | NS | [14] |
17 | Murine leukaemia viruses (MuLVs) | Retroviridae | ssRNA-RT | Mouse | A model for non-inflammatory degeneration of the central nervous system | BALB/c and C3H mice | Tissue Mφ | Virus infects Mφ/microglia and persists during later stages (8 weeks after infection). | NS | [15] |
18 | Ovine lentivirus OvLV | Retroviridae | ssRNA-RT | Sheep | Encephalitis and chronic pneumonitis | Lamb | Tissue Mφ | OvLV variants persist in alveolar Mφ. | NS | [54] |
19 | Human immunodeficiency virus (HIV), Simian immunodeficiency virus (SIV) | Retroviridae | ssRNA-RT | Human | Immune deficiency syndrome (AID), cancer | Human (U937, THP-1) and mouse cell lines, human and monkey, macaque tissue Mφ | MDM, monocytes, tissue Mφ | -CD14+CD16+ monocytes are permissive to productive infection. -Mφ serves as a major reservoir for HIV. -Infected Mφ escape immune response. -Infected Mφ showed impaired phagocytic activity. -Mφ dissiminate HIV to CD4+ T cells and central nervous system (“Trojan horse hypothesis”). | -Infected Mφ showed M1 polarization during early stages of infection (with high production of IFN-γ, IL-2, IL-12—ELISA). There is a shift of M1 to M2 at later stages of infection (with high production of IL-4, TGF-β and IL-10—ELISA). -HIV-1 infection enhances the survival of Mφ by upregulating antiapoptotic genes through different pathways (activation of NF-kB and PI3K signalling, delay of TNF-induced apoptosis; modulation of mitochondrial pathways; increase telomerase activity). | [18,55,56] |
20 | Maedi-visna (MVV) | Retroviridae | ssRNA-RT | Sheep | Fatal lymphoproliferative disease | Sheep | Bone marrow monocytes, PBMC | Limited virus replication in bone marrow monocytes. | NS | [57] |
21 | African swine fever virus (ASFV) | Asfarviridae | dsDNA | Pig, warthogs, bushpigs, soft ticks | Lethal haemorrhagic fever | -Pig -Porcine alveolar Mφ | -Cell culture derived from bone marrow, PBMC -Alveolar and bone marrow cells | -Virus persists in tissue Mφ. -Moderate virus replication continued for at least 3 months in alveolar and bone marrow Mφs. | -Virus caused cytotoxic effect within 2–3 days in monocytes but not in Mφ (visual examination of monolayers). -Virus leads to full morphological differentiation of Mφ (visual examination of cell morphology). | [13,58] |
22 | Bovine herpesvirus-4 (BHV-4) | Herpesviridae | dsDNA | Cattle, rabbits | Endometritis, vulvovaginitis and mastitis | Bovine Mφ cell line (BOMAC). | Cell culture | -Virus cause cell death of the majority of BOMAC cells and persists in surviving cells. | NS | [59] |
23 | Cytomegalovirus (CMV) | Herpesviridae | dsDNA | Human | Chronical inflammation, cardiovascular diseases, some types of cancers | -Murine cytomegalovirus model (MCMV), MDM/Allo-MDM | -Human monocytes -MDM | -Productive replication of CMV in human Mφ up to 16 weeks but not monocytes. -Monocytes disseminate virus in organism. | -HCMV induces specific phenotype within M1/M2 continuum (skewed towards M1). Simultaneous expression of M1-associated molecules (IL-6, TNF-α, CD86) and M2-associated molecules (IL-10 and CD163) by infected Mφ. Data analysed using PCR, flow cytometry (M1 cells were CD68+, M2—CD163+), microarray analysis for more than 2000 genes. -Decoy of induced apoptosis of infected monocytes due to prolonged expression of the anti-apoptotic molecule, Mcl-1. -Infected cells escape the cellular antiviral pro-apoptotic response due to specific cytokine/chemokine expression (the “Goldilocks” phenomenon). -Infected cells utilize EGFR receptor and integrins. | Review [17,60] |
24 | Epstein-Barr virus infection (EBV) | Herpesviridae | dsDNA | Human | Inflammation, some types of cancers | Human cancer tissues, human smears, rhesus macaques, Mφ culture (RAW 264.7 cells), Balb/c and IL-10KO mice. | MDM, tissue Mφ, submucosal monocytes, tumour-associated Mφ (TAMs) | -EBV replicates in Mφ. -Monocytes disseminate virus in organism. | -Infected Mφ produce high level of IL-8, MCP-1 due to TLR9 and TLR-2 activation (ELISA). -Monocytes produce high level of IFNα in response to EBV (ELISA). -IL-10-dependent M2 polarization of infected TAMs (ELISA). | A book [61], review [62] |
25 | Human herpesvirus 6 (HHV-6) | Herpesviridae | dsDNA | Human | Multiple sclerosis | Human | -PBMC | -Latent persistence of HHV-6 in Mφs for more than 1 month. | Selective downregulation of IL-12 in infected Mφ (ELISA), which is not dependent upon productive viral infection. | [63,64,65] |
26 | Kaposi’s sarcoma-associated herpesvirus KSHV (HHV-8) | Herpesviridae | dsDNA | Human | Cancer | -Tumour microenvironment, cell culture. -MDM -Prostate cancer samples | Tissue Mφ, RAW 264.7 cells | -HHV-8 led to production of viral proteins in intralesional Mφ, with little production of viral DNA. -Virus persists in a latent form in Mφ/monocytes. -Lytic gene expression in Mφ in prostate stroma. | KSHV miRNAs protect Mφ from cell death through the upregulation of xCT. | [66,67,68] |
27 | Murine herpesvirus 72 (MHV-72) | Herpesviridae | dsDNA | Mouse | Acute infection of lung epithelial cells | Balb/c mice | Lung mononuclear cells | Virus persists in alveolar and peritoneal lung mononuclear cells and Mφ of peripheral blood up to 8 months. | NS | [69] |
Varicella-zoster virus (VZV), simian varicella virus (SVV) | Herpesviridae | dsDNA | Human, nonhuman primates | Varicella-zoster, “multiple sclerosis-like” pathology | -Human ganglia. -Rhesus macaques. | Alveolar Mφ | -SVV IE63 proteins are present in Mφ in lymph nodes after SVV reactivation in monkeys. -SVV infects alveolar Mφ and transmit virus to T cells. | SVV-infected Mφs were CD163+ (immunofluorescence analysis) after virus reactivation but not during latency. | [70,71] | |
29 | Frog virus 3 (FV3) | Iridoviridae | dsDNA | Amphibian species | Acute systemic FV3 infection | Xenopus laevis | Peritoneal Mφ | FV3 persist in peritoneal Mφ in vitro. | No cytopathic effect on infected Mφ. | [25] |
Virus | Entry Type | Receptor(s) Used for Viral Entry/Attachment | Virus Fate | Reference | |
---|---|---|---|---|---|
1 | Respiratory syncytial virus | Macropinosome formation | Nucleolin, heparan sulphate proteoglycans | Replication | [75,81] |
2 | Influenza virus | Endocytosis, Phagocytosis | Sialic acid sugars | Replication | [76] |
3 | Vesicular stomatitis virus | endocytosis | Phosphatidylserine | No replication | [32,79] |
4 | Mouse hepatitis virus | Phagocytosis | * Sialic acid sugars and glycolipids N- * acetilneuraminic acid receptor | No replication | [34,77] |
5 | Japanese encephalitis virus, West Nile virus, Dengue virus | Phagocytosis | * DC-SIGN or * DC-SIGNR TLR-2, TLR-3 and TLR-7, RIG-I | Replication | [39,40] |
6 | Coxsackieviruses | Macropinocytosis | * CAR and IgG Fc fraction receptors (FcγRII and FcγRIII), occludin | Replication | [42,73,84] |
7 | Theiler’s murine encephalomyelitis virus | Endocytosis | Sialic acid sugars | Replication | [46,78] |
8 | Human immunodeficiency virus, Simian immunodeficiency virus | Endocytosis, macropinocytosis | Human mannose receptor C-type 1 * CD4 and a * coreceptors CXCR4 or CCR5, heparan sulphate proteoglycans | Replication | [11,85,86] |
9 | Cytomegalovirus | Endocytosis | Heparin sulphate proteoglycans following by the binding to the β1 and β3 integrins, EGFR, TLR2, TLR3 and TLR9 (murine CMV) | Replication | [17,82] |
10 | Epstein-Barr virus infection | Endocytosis | * CR2 or CD21, TLR2 and TLR3 | Replication | [82] |
11 | Human herpesvirus 6 | Endocytosis | * CD46 | Non-productive infection | [63,87] |
12 | Kaposi’s sarcoma-associated herpesvirus | * Macropinosome membrane fusion | xCT, DC-SIGN, * surface heparan sulphate, * integrin α3β1 (CD49c/29)? | Replication | [66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88] |
13 | Varicella-zoster virus, Simian varicella virus | Fusion with the plasma membrane or endocytosis | * Mannose-6-phosphate receptor, myelin-associated glycoprotein | not clear | [71,89] |
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Nikitina, E.; Larionova, I.; Choinzonov, E.; Kzhyshkowska, J. Monocytes and Macrophages as Viral Targets and Reservoirs. Int. J. Mol. Sci. 2018, 19, 2821. https://doi.org/10.3390/ijms19092821
Nikitina E, Larionova I, Choinzonov E, Kzhyshkowska J. Monocytes and Macrophages as Viral Targets and Reservoirs. International Journal of Molecular Sciences. 2018; 19(9):2821. https://doi.org/10.3390/ijms19092821
Chicago/Turabian StyleNikitina, Ekaterina, Irina Larionova, Evgeniy Choinzonov, and Julia Kzhyshkowska. 2018. "Monocytes and Macrophages as Viral Targets and Reservoirs" International Journal of Molecular Sciences 19, no. 9: 2821. https://doi.org/10.3390/ijms19092821