Dual-Specificity Phosphatases in Regulation of Tumor-Associated Macrophage Activity
Abstract
:1. Introduction
2. Tumor-Associated Macrophages and Its Precursors in Tumor Immunity
3. DUSPs: Structure and Function
4. DUSPs Interaction with Protein Kinases in Macrophage Signaling
5. Regulation of TAM Functions by DUSPs
6. Epigenetic Regulation of DUSPs in Macrophages
- DNA Methylation
- Histone Code
- miRNA
7. Targeting DUSPs to TAM Therapeutic Modeling
8. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
Akt | aktine |
ALCAM | transmembrane glycoprotein CD166 |
AP1 | activator protein 1 |
ARG1 | arginase |
ASK1 | apoptosis signal-regulating kinase 1 |
ARG1 | arginase 1 |
ATF2 | activating transcription factor |
C3aR, C5aR | complement component 3a, 5a receptor 1 |
CD9 | tetraspanin family protein |
CHOP | C/EBP homologous protein |
CLEC5A | C-type lectin domain family 5 member A |
COX2 | COX-2 inhibitors |
CREB | cAMP response elements beta |
c-Src | Src cytoplasmic proto-oncogene-tyrosine-protein kinase |
CXCL | chemokine (C-X-C motif) ligand |
DLK | double leucine zipper kinase; MKK—MAPK kinases |
DUSP | dual-specificity phosphatases |
EGF | epidermal growth factor |
EGFR | epidermal growth factor receptor |
Elk1 | ETS Like-1 protein |
ERK | extracellular signal-regulated kinase |
FADD | Fas receptor death domain-interacting protein; MEKK, MEK kinase |
FAK | focal adhesion kinase (proteintyrosine kinase) |
FasL | ligand for Fas membrane molecule |
FasR | receptor for Fas membrane molecule |
FFA | saturated free fatty acid |
GRB2 | protein with SH2 and SH3 domains |
ICAM | intercellular adhesion molecule 1 |
IGF1R | insulin-like growth factor receptor 1 |
INFγ | interferon gamma |
IRF1 | interferon regulatory factor 1 |
ITGA6 | integrin alpha 6 |
ITGAX | integrin, alpha X, CD11c |
JNK | c-Jun N-terminal kinase |
JNK | c-Jun N-terminal kinase; MAPK, mitogen-activated protein kinase |
LITAF | lipopolysaccharide Induced TNF Factor |
LFA3 | lymphocyte function-associated antigen 3 |
LPS | lipopolysaccharides; GR, growth factors |
MEK | MAPK/ERK kinase |
MEF2 | myocyte Enhancer Factor 2 |
mF | macrophages |
MIP2 | major Intrinsic Protein 2 |
MKP | mitogen-activated protein kinase phosphatase |
MLK3 | mixed origin kinase 3, serine/threonine protein kinase |
Mmd | monocyte to macrophage differentiation associated |
MSK | mitogen and stress-activated protein kinases |
NFAT | nuclear factor of activated T-cells |
NO | nitric oxide |
PGE2 | prostaglandin E2 |
PKN2 | protein kinase N2 |
Raf | protein belonging to the serine-threonine protein kinase family; |
RAS | inactive membrane-bound small G protein; RAS-GTP, active RAS protein |
ROS | reactive oxygen species |
SOS | guanine nucleotide substitution factor |
STAT | family of proteins that are intracellular transcription factors |
SRF | serum Response Factor |
TAB1 | mitogen-activated protein kinase, regulator of MAP3K7/TAK1 kinase kinase |
TAK1 | transforming growth factor β-activated kinase 1, a member of the MAPK family |
TGF-β | transforming growth factor beta |
TNF-α | tumor necrosis factor α |
TRAF6 | TNF receptor associated factor |
TrkA | tyrosine kinase A |
UV | ultraviolet radiation |
VEGF | vascular endothelial growth factor |
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Isoforms and Cellular Localization | Inductors | Pathway | Effect of DUSPs in Macrophages |
---|---|---|---|
MAPK-specific phosphatases/typical DUSPs | |||
DUSP1 Nuclear | LPS | p38, JNK | ↓ p38 and JNK, ↓ TNF-α, IL-6, IL-10; ↑ IL-12 and IRF-1 (↑ expression of IL-12 by enhancing IRF1 expression) [56,57,58] |
IL-10 + DEX | p38 | ↓ IL-6, IL-12, p38 (↑ prolonged expression DUSP1) [59,60] | |
DEX | JNK > p38 | ↓ JNK, TNF-α, COX2, IL-1 [56,59] | |
Peptidoglycan, Zymosan, poly(I:C), Flagellin | JNK, p38 | ↓ JNK, p38, TNF-α [61] In DUSP1−/− mF ↑ p38, ↑ TNF-α, IL-10, CD86 and CD40 [62] | |
Heat shock | p38 | ↑ activity of heat shock elements (HSE) in the MKP-1 promoter, stability of MKP-1 mRNA in mF [63] | |
DUSP2 Nuclear | LPS | ERK, p38 > JNK | In DUSP2 −/− mF ↓ ERK and p38, Elk1 and NFAT-AP-1 activation ↑ JNK, ↓ TNF-α, IL-6, IL-12α, COX2, IL-1β, C5aR, C3aR + ↓ PGE2, NO [64] |
DUSP4 Nuclear | M-CSF | ERK | In DUSP4−/− mF, ↑ ERK ↓ Mmd, Csf2, expression of surface proteins CD115, CD34 [65] |
LPS | JNK, p38 | In DUSP4−/− mF ↑ JNK and p38, ↑ ARG-1, IL-6, TNFα, IL-12, PGE2 and ↓ expression of inducible nitric oxide synthase (iNOS) and IL-10, + ↑ DUSP1 as a result of increased ERK signaling [66] | |
FFA | JNK, p38 | ↓ JNK, TNF-α, IL-6, IL-12; ↓ macrophage M1 activation through JNK and p38 [67] | |
IL-4 | JNK, p38 | ↑ macrophage M2 activation [67] | |
DUSP5 Nuclear/cytoplasmic | LPS | ERK | ↓ ERK1/2, ↓ ERK1/2 phosphorylation, ↑ NF-κB activity [68] |
M-CSF | ERK | ↓ ERK1/2, block macrophage differentiation => differentiate towards to granulocytes [69] | |
DUSP6 Cytoplasmic | PKN2 | ERK | ↓ ERK1/2, IL-4, IL-10 [70] |
CCL2+LPS | ERK | ↑ ERK1/2 phosphorylation [71] | |
Hyperoxia | ERK | ↑ ERK [72] | |
DUSP7 Cytoplasmic | No information | ||
DUSP8 Nuclear/cytoplasmic | LPS | JNK | ↓ JNK, TNF-α, IL-1β, IL-6 [73,74] |
miR-21 | JNK, p38 | ↑ p38, JNK + ↑ macrophage migration and macrophage adhesion to endothelium [75] | |
DUSP9 Cytoplasmic | hypoxia/reoxygenation | JNK, p38 | ↓ JNK, p38 ↓ ASK1 phosphorylation, TRAF6, IKKβ (NF− κB pathway), K63 ubiquitination, TNF-α, IL-1β, IL-6 [76] |
DUSP10 Nuclear/cytoplasmic | LPS, peptidoglycan, poly(I:C) | JNK [77] + JNK, ERK, p38 [78] | ↓ AP-1, TNF-α, IL-6, JNK activity [77] in DUSP10−/− mF ↑ JNK, ERK, p38 phosphorylation, ↑ TNF-α, IL-6, MIP-2, ↑iNOS, ROS production [78] |
Inhibition by siRNA of pharmacological inhibitor AS077234-4 | p38 | ↓ p38, TNF-α и IL-6 [79] | |
DUSP16 Nuclear/cytoplasmic | LPS | JNK1/2 | In DUSP16−/− mF ↑ produce IL-12, IRF-1, ↑ JNK 1/2 phosphorylation [80] |
Atypical DUSPs | |||
DUSP3 Cytoplasmic | LPS | ERK | In DUSP3−/− mF ↓ ERK1/2 phosphorylation, Akt, TNF, IL-6 [81] |
DUSP11 Nuclear/cytoplasmic | LPS | TAK1 | In DUSP−/− mF, ↑ TAK1 phosphorylation (TGF-β–activated kinase 1), TNF-α, IL-6 и IL-1β [82,83] |
DUSP12 Nuclear | LPS | JNK, p38 | ↓ JNK, p38 activation, ↓ expression of AP-1, TNF-α, IL-6, IL-1β, CCL2, ↑ IL-10 [84] |
DUSP14 Cytoplasmic | No information | ||
DUSP18 Nuclear/cytoplasmic/mitochondrial intermembrane space | No information | ||
DUSP22 Nuclear | No information | ||
DUSP26 Cytoplasmic | LPS | p38, JNK | ↓ TNF-α, p38 significantly and JNK slightly [85] |
Isoform | Features in Solid Tumor | Correlation with Cancer Progression Parameters |
---|---|---|
DUSP1 | ↑ breast cancer [16,106,107] ↑ prostate cancer [108] ↓ prostate cancer [109], lung cancer by oxidation [106], head and neck squamous cell carcinoma [110] | negative correlation with OS in ovarian cancer [16] positive correlation with DFS in hepatocellular carcinoma [93] |
DUSP2 | ↓ lung, breast, colorectal, prostate, ovarian [111], ↓ ovarian carcinoma [105] ↓ bladder cancer [112] hypermethylation CpG island in head and neck cancer [113] | positive correlation with RFS in Her2+ breast cancer [97] positive correlation with OS and DMFS in colorectal cancer [98] positive correlation with OS in ovarian cancer [105] positive correlation with OS and RFS in bladder cancer [112] |
DUSP3 | ↑ cervical carcinoma, prostate cancer [114,115] ↓ non-small lung cancer [116] | positive correlation with OS for lung, kidney, sarcoma, lymphoma, and breast cancer/negative correlation with OS for lung, breast, and brain cancer for other groups [96] negative correlation with metastasis in non-small lung cancer mice model [117] |
DUSP4 | ↑ medullary thyroid carcinoma, pancreatic cancer, breast cancer, colorectal cancer, rectal cancer, melanoma [99,107,118,119] ↓ serous ovarian carcinoma [120] | negative correlation with OS and DFS in early breast cancer [95] positive correlation with RFS in colorectal cancer [99] positive correlation with OS in lung, pancreatic cancer, gastric, and clear cell renal cell cancer [121] hypermethylation predicts a negative survival factor in B-cell lymphoma [95] |
DUSP5 | ↓ colorectal cancer, prostate cancer, gastric cancer [100,102,122] hypermethylation of CpG islands in gastric cancer [122] | positive correlation with DFS and DSS in colorectal cancer [100] negative correlation with high Gleason score, biochemical recurrence and metastasis in prostate cancer [102] positive correlation with OS in gastric cancer [122] negative correlation with OS in neuroblastoma [123] |
DUSP6 | ↓ melanoma [124] ↓ esophageal cancer [125] ↓ prostate cancer [126] ↓ pancreatic cancer [127] ↑ glioblastoma [128] ↑ thyroid carcinoma [129] hypermethylation of gene promoters in pancreatic cancer [130] | positive correlation with OS, RFS in non-small cell lung cancer [131] positive correlation with OS in esophageal cancer, nasopharyngeal [132] |
DUSP7 | ↓ ovarian cancer [133] ↑ acute and myeloid leukemia [134] hypermethylation of gene promoters in ovarian cancer [104] | methylation-dependent positive correlation with PFS and OS in ovarian cancer [104] |
DUSP8 | hypermethylation of gene promoters in ovarian cancer [104] | methylation-dependent positive correlation with PFS and OS in ovarian cancer [104] |
DUSP9 | ↓ renal carcinoma [135] ↑ gastric cancer [136] hypomethylation of gene promoters in gastric cancer [136] | positive correlation in renal cancer with OS [135] |
DUSP10 | ↑ ER- breast cancer [94] ↑ prostate cancer [137] ↑ hepatocellular carcinoma, melanoma, lung cancer, colorectal cancer, prostate cancer, glioblastoma [137,138] | |
DUSP12 | ↑ sarcoma, neuroblastoma, retinoblastoma, intracranial ependymoma, chronic myeloid leukemia [139] ↑ DUSP12 positive correlate with c-met and itga, cell migration and genomic instability [138] | |
DUSP16 | ↑ hepatocellular carcinoma [137] ↑ leukemia [140] | |
DUSP18 | ↑ colon cancer [141] ↑ hepatocellular carcinoma [142] | positive correlation with OS in colon cancer [141] |
DUSP22 | ↓ breast cancer [143] ↓ colorectal cancer [101] ↓ peripheral T-cell lymphoma [144] ↓ prostate cancer [103] | positive correlation with OS in IV stage colorectal cancer [101] positive correlation with PFS and DFS in prostate cancer [103] negative correlation OS in anaplastic large cell lymphoma [145] |
DUSP26 | ↓ ovarian cancer, neuroblastoma, medulloblastoma and glioblastoma [146] ↑ thyroid carcinoma [147] ↑ for TGFβ1-promoted EMT in pancreatic, lung cancers cell lines [148] | positive correlation with DFS in neuroblastoma [149] |
Isoforms | Epigenetic Changes | Key Mechanism | Effects in Macrophages | References |
---|---|---|---|---|
DUSP4 | DNA Methylation | Efferocating ↑ DNMT3A ↓ methylation of DUSP4 promoter ↓ DUSP4 mRNA expression | ↑ PGE2, TGF-β production | [167] |
DUSP1 | Histone code | ↓ chromatin activity ↑ H3 and H4 histones acetylation ↑ mRNA DUSP1 expression | --- | [168] |
DUSP1 | Histone code | ↑ acetylation of histones H3 and H4 at the DUSP1 promoter | --- | [169] |
DUSP4 | Histone code | ↑ methylation of H3K4me3 histones | ↓ CXCL1, CXCL2, CXCL3 | [170] |
DUSP1 | miRNA | ↑ miR-127 ↓ DUSP1 mRNA expression | ↑ IL-6, TNF-α, IL-1β ↑ NOS | [171] |
DUSP1 | miRNA | miR-429, miR-200b, and miR-200c ↓ DUSP1 mRNA expression | ↑ IL-6, TNF-α, IL-1β | [172] |
DUSP6 | miRNA | ↑ miR-9 ↓ DUSP6 mRNA expression | ↓ NOS (after 6 h of CCL2 induction) ↑ TNF-α | [71] |
DUSP8 | miRNA | ↓ miR-21 ↑ DUSP8 mRNA expression | ↓ CCL2-induced migration ↓ macrophage-endothelium interaction | [16] |
DUSP8 | miRNA | ↑ Ox-LDL ↑ miR-21 ↑ DUSP8 mRNA expression | ↑ migration | [173] |
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Patysheva, M.R.; Prostakishina, E.A.; Budnitskaya, A.A.; Bragina, O.D.; Kzhyshkowska, J.G. Dual-Specificity Phosphatases in Regulation of Tumor-Associated Macrophage Activity. Int. J. Mol. Sci. 2023, 24, 17542. https://doi.org/10.3390/ijms242417542
Patysheva MR, Prostakishina EA, Budnitskaya AA, Bragina OD, Kzhyshkowska JG. Dual-Specificity Phosphatases in Regulation of Tumor-Associated Macrophage Activity. International Journal of Molecular Sciences. 2023; 24(24):17542. https://doi.org/10.3390/ijms242417542
Chicago/Turabian StylePatysheva, Marina R., Elizaveta A. Prostakishina, Arina A. Budnitskaya, Olga D. Bragina, and Julia G. Kzhyshkowska. 2023. "Dual-Specificity Phosphatases in Regulation of Tumor-Associated Macrophage Activity" International Journal of Molecular Sciences 24, no. 24: 17542. https://doi.org/10.3390/ijms242417542