Harnessing the Complete Repertoire of Conventional Dendritic Cell Functions for Cancer Immunotherapy
Abstract
:1. Introduction
2. The Enigmatic Role of Plasmacytoid DCs in the DC Continuum
Subpopulation | Species | Marker | Level of Detection | Literature |
cDC1 | Mouse | CD8α (splenic, resident cDC1) | Protein; RNA | [80,86] |
CD1d | Protein | [86] | ||
CD207; Langerin | Protein; RNA | [35,37,80,82] | ||
CD24 | Protein | [30,35,82] | ||
CD103+CD11b- migratory cDC1 | Protein | [35,42] | ||
Shared | XCR1 | Protein; RNA | [30,33,42,82,86,87,88,89] | |
CADM1; TSLC1; NECL-2; IGSF4; SynCAM1; | Protein; RNA | [30,31,33,42,82,86,87,88,89] | ||
CLEC9A; DNGR-1; CD370 | Protein; RNA | [24,28,29,31,33,41,42,46,80,82,87,89,90,91] | ||
BTLA | Protein; RNA | [30,40,42,86,90] | ||
CD26 | Protein | [29,30,90] | ||
Sirpα; CD172a negative | Protein | [28,30,92] | ||
CD11c (human cDC1int) | Protein | [28,30,31,42,80,86,88] | ||
MHC-II; HLA-DR | Protein | [28,29,30,42,86] | ||
Human | CD141; BDCA-3 | Protein | [28,31,34,82,87,90,92] | |
CD103+Sirpα- migratory cDC1 | Protein | [42] | ||
cDC2 | Mouse | CD4 (lymphoid tissue) | Protein; RNA | [80,93] |
DCIR2 (lymphoid tissue) | Protein; RNA | [55] | ||
CD103+CD11b+ gut migratory cDC2 | Protein | [42] | ||
Shared | Sirpα; CD172a | Protein | [28,29,30,31,35,42,80,82,86,88,92] | |
XCR1 negative | Protein | [30] | ||
CD11b | Protein; RNA | [28,30,42,80,88] | ||
CD11c | Protein; RNA | [28,30,31,42,80,86,88] | ||
MHC-II; HLA-DR | Protein | [28,29,30,42,86] | ||
Human | CD1c; BDCA-1 | Protein; RNA | [28,31,34,80,90,91,92] | |
CD1a (skin) | Protein | [28,94] | ||
CLEC10A | Protein; RNA | [33,45] | ||
CD163 | Protein | [90,92] | ||
CD1d | Protein; RNA | [33,90] | ||
FcεRIα | Protein; RNA | [33,80,90] | ||
CD103+Sirpα+ gut migratory cDC2 | Protein | [42] | ||
Subpopulation | Species | TLRs | Level of Detection | Literature |
cDC1 | Mouse | TLR2 | Protein | [86] |
TLR4; CD284 | RNA | [80,89] | ||
TLR11 | RNA | [24,46,80,89] | ||
TLR12 | RNA | [24,46,80,86,88,95] | ||
TLR13 | Protein; RNA | [24,46,80,88] | ||
CD180; RP105 | Protein | [86] | ||
Shared | TLR3 | Protein; RNA | [42,80,87,88,89,92,96,97] | |
TLR9 | Protein; RNA | [24,46,88,89,98] | ||
Human | TLR6 | RNA | [89] | |
TLR10; CD290 | Protein | [90] | ||
cDC2 | Mouse | TLR9 | Protein; RNA | [24,46,80,88,98] |
TLR13 | Protein; RNA | [24,46,88] | ||
Shared | TLR1 | Protein; RNA | [80,86,89] | |
TLR2; CD282 | Protein; RNA | [31,80,86,89,92] | ||
TLR4; CD284 | RNA | [80,89] | ||
TLR5 | RNA | [80,89,96,98] | ||
TLR6 | Protein; RNA | [80,86,89] | ||
TLR7 | Protein; RNA | [24,46,80,88,89,91] | ||
TLR8 | Protein; RNA | [80,89,91,92] | ||
CD180; RP105 | Protein | [86,90,92] | ||
Human | - | - | - | |
Subpopulation | Species | CLRs | Level of Detection | Literature |
cDC1 | Mouse | CD207; Langerin | Protein | [35,86] |
CLEC2D | Protein | [86] | ||
CLEC4A; DCIR; CD367 | RNA | [42] | ||
Shared | DEC205; CD205; Ly75 | Protein; RNA | [24,31,35,42,46,55,82,86,88,90] | |
CLEC1A | RNA | [42] | ||
CLEC9A; DNGR-1; CD370 | Protein; RNA | [24,28,29,31,33,41,42,46,82,87,89,91] | ||
CLEC12A; MICL; KLRL1; CLL1 | Protein; RNA | [24,46,86,99] | ||
Human | CD206; MMR (skin) | Protein | [28] | |
Dectin-1; CLEC7A; CLECSF12; CD369 | Protein | [28] | ||
cDC2 | Mouse | Dectin-2; CLEC6A; CLEC4N; CLECSF10 | Protein; RNA | [55,88] |
CLEC4a2; DCIR1; CLECSF6 | RNA | [55,80,96] | ||
CLEC4a3; DCIR3 | RNA | [55] | ||
CLEC4a4; DCIR2 | Protein; RNA | [24,46,55,86,88] | ||
DCAR | RNA | [55] | ||
Shared | CLEC4A; DCIR; CD367 (subtype not defined) | Protein; RNA | [33,42,80,86,96] | |
Dectin-1; CLEC7A; CLECSF12; CD369 | Protein; RNA | [28,55,86] | ||
CLEC12A | Protein | [80,100] | ||
CLEC13A; CD302 | RNA | [96] | ||
CD209 (human gut); CD209a (mouse); DC-SIGN | Protein; RNA | [24,42,46,55,80,89,91] | ||
Human | CD206; MMR (skin) | Protein | [28,42,90] | |
CD207; Langerin | Protein; RNA | [42,91,94] | ||
CLEC5A (thymic cDC2) | RNA | [31] | ||
CLEC10A | Protein; RNA | [31,33,42,45,89] | ||
CLEC11A; CLECSF3 (CD5 low cDC2) | RNA | [91] | ||
CLEC17A (CD5 high cDC2) | RNA | [91] | ||
Subpopulation | Species | FcγRs | Level of Detection | Literature |
cDC1 | Mouse | FcγRIII; CD16 | Protein; RNA | [56,80,96] |
FcγRIV; CD16.2 | Protein | [56] | ||
Shared | FcγRI; CD64 | Protein; RNA | [30,42,56] | |
FcγRIIB; CD32b | Protein; RNA | [56,80,86,101] | ||
Human | FcγRIIA; CD32 | RNA | [102] | |
cDC2 | Mouse | FcγRIV; CD16.2 | Protein | [56] |
FcγRI; CD64 negative | Protein; RNA | [30,56,80] | ||
Shared | FcγRIIB; CD32b | Protein; RNA | [33,42,56,80,86,89,102] | |
FcγRIII; CD16; human FcγRIIIA | Protein; RNA | [80,101,102] | ||
Human | FcγRI; CD64 | Protein; RNA | [89,101] | |
FcγRIIA; CD32 | Protein; RNA | [28,31,96,101,102] | ||
Subpopulation | Species | Intracellular Sensors | Level of Detection | Literature |
cDC1 | Mouse | NLRP3; NALP3; Cryopyrin | Protein | [88] |
Shared | ||||
Human | NLRC5 | RNA | [42] | |
Caspase-1 low | RNA | [92] | ||
AIM2 | RNA | [92] | ||
PYCARD | RNA | [92] | ||
cDC2 | Mouse | NOD-1; NLRC1 | Protein; RNA | [24,46,88] |
CARD9 | Protein | [88] | ||
STING | Protein | [88] | ||
MDA5 | Protein | [88] | ||
RIG-I | Protein | [88] | ||
NLRC4 | RNA | [24,46] | ||
Shared | NLRP3; NALP3; Cryopyrin | Protein; RNA | [33,42,88,92] | |
Caspase-1 high | Protein; RNA | [42,88,92] | ||
Human | Caspase-8 | RNA | [92] | |
NAIP | RNA | [92] | ||
NLRC4 | RNA | [92] | ||
NLRP1 | RNA | [92] | ||
PYCARD | RNA | [92] | ||
Subpopulation | Species | Co-Regulatory Molecules | Level of Detection | Literature |
cDC1 | Mouse | - | - | - |
Shared | CD80 | Protein | [30,42,55,82,87] | |
CD86 | Protein; RNA | [31,33,42,55,80,82,87,89,96] | ||
CD40 | Protein; RNA | [30,42,55,89] | ||
PD-L1; CD274 | Protein | [28,30,82,87,89] | ||
Human | IDO-1 | Protein; RNA | [31,33,42,80,89,92] | |
IDO-2 | RNA | [42] | ||
cDC2 | Mouse | - | - | - |
Shared | CD80 | Protein | [30,42,55,82,87] | |
CD86 | Protein; RNA | [30,31,33,42,55,82,87,96] | ||
CD40 | Protein | [30,42,55,89] | ||
PD-L1; CD274 | Protein | [30,80,82,87,89] | ||
Human | ICOS-L | RNA | [28] | |
Subpopulation | Species | Other Interesting Molecules | Level of Detection | Literature |
cDC1 | Mouse | CD36 (Scavenger receptor) | Protein | [86,88] |
Shared | CD135; FLT3 | Protein; RNA | [28,80,91] | |
Human | TIM-3 | Protein | [90] | |
cDC2 | Mouse | Clec12A (marker for cDC2B) | Protein | [80] |
Clec10A (marker for cDC2B) | Protein | [80] | ||
ESAM (marker for cDC2A or Notch2-dependent cDC2) | Protein | [66,68,80] | ||
Shared | CD135; FLT3 | Protein; RNA | [28,80,91] | |
Human | CD36 (marker for DC3; DC2 negative) | RNA | [31,33] | |
CD163 (marker for DC3; DC2 negative) | Protein; RNA | [28,33] | ||
CD5 (marker for DC2; DC3 negative) | Protein; RNA | [90,91] | ||
CD200R (downregulating DC activity) | Protein | [90] |
3. Environmental Cues Controlling the Stimulatory and Tolerogenic Capacity of DCs
3.1. Dendritic Cells Function as Sensors for Invading Pathogens
3.2. Pathogen Recognition Receptors on DCs Regulate Antigen Sensing, Uptake and Activation
TLR Ligands | ||||
Receptor | Organism | Ligand Class | Molecules | References |
TLR2 (TLR1/TLR2; TLR2/TLR6) | M/H | Pathogenic | Lipoptroteins; Triacetylated lipopeptides; human β-defensin 3 (BD-3); Glycosylphosphatidylinositol (GPI); Zymosan; Peptidoglycan; LPS; Lipoproteine/-peptide; Glycolipide; MALP-2; Diacetylierte Lipopeptide; LTA; Zymosan | [244,245,246,247] [248,249,250,251,252,253,254,255,256,257,258] |
Endogenous | Endoplasmin; Hsp60; Hsp70; Human cardiac myosin; Urate crystals; Hyaluronan | [259,260,261,262,263,264] | ||
Synthetic | FSL-1, synthetic lipopeptides & lipoprotein analogs, triacetylated lipopeptides e.g., Pam2CSK4, Pam3CSK4, or synthetic beta-defensin 3, MALP2 | [244,245,258], [265,266,267,268] | ||
TLR3 | M/H | Pathogenic | dsRNA | [269,270,271] |
Endogenous | mRNA | [270] | ||
Synthetic | poly(I:C); poly(A:U) | [258,272,273,274] | ||
TLR4 (MD-2; CD14) | M/H | Pathogenic | Lipopolysaccharid (LPS; Gram-); Lipoteichoic acid (LTA; Gram+) | [256,275,276] |
Endogenous | β-defensin 2; Fibronectin; Fibrinogen; Hyaluronan; Surfactant protein A; Urate crystals; OxPAPC; Hsp72; Hsp70; Hsp60; HMGB1; Endoplasmin | [262,264,277,278,279,280,281,282], [259,260,283,284] | ||
Synthetic | Glycan-based agonists; Monophosphoryl Lipid A (MPL); pyrimido[5,4-b]-indoles; LPS | [268,285,286,287] | ||
TLR5 | M/H | Pathogenic | Flagellin | [248,288] |
Endogenous | Unknown | |||
Synthetic | Flagellin | [289,290] | ||
TLR7 | M/H | Pathogenic | ssRNA | [291,292,293] |
Endogenous | RNA; siRNA | [294,295] | ||
Synthetic | Imiquimod (R837); Resiquimod (R848); Gardiquimod; Loxoribine | [268,274,296,297,298,299,300,301] | ||
TLR8 | M/H | Pathogenic | TLR7 antagonist (mouse); ssRNA (human) | [292,299,302,303] |
Endogenous | Human cardiac myosin; siRNA | [295,304] | ||
Synthetic | Imiquimod (R837); Resiquimod (R848); Gardiquimod; TL8-506 | [268,274,296,297,298,299,300,301] | ||
TLR9 | M/H | Pathogenic | Unmethylated CpG DNA; dsDNA | [258,269,305,306] |
Endogenous | DNA; HMGB1 | [307,308,309] | ||
Synthetic | Diverse synthetic CpG-oligonucleotides (CpG-ODNs) | [268,274,310,311,312] | ||
TLR10 | H | Pathogenic | Non functional in mice (viral insertion); TLR2 antagonist; HIV-1 gp41 | [120,313,314] |
Endogenous | Unknown | |||
Synthetic | Unknown | |||
TLR11 | M | Pathogenic | Profilin | [95,120,315] |
Endogenous | Unknown | |||
Synthetic | Unknown | |||
TLR12 | M | Pathogenic | Profilin | [120,315,316] |
Endogenous | Unknown | |||
Synthetic | Unknown | |||
TLR13 | M | Pathogenic | Bacterial 23S rRNA | [120,123] |
Endogenous | Unknown | |||
Synthetic | Unknown | |||
CD180 | M/H | Pathogenic | Unknown | |
Endogenous | Negative regulator of TLR7 & TLR9 | [317] | ||
Synthetic | Unknown | |||
STING ligands | Organism | Ligand Class | Molecules | Literature |
Receptor | ||||
STING | M/H | Pathogenic | Bacterial cyclic di-nucleotides and cGAMP; viral DNA | [111,206,210,211] |
Endogenous | Self-DNA e.g., dead cells, DNA leaking into the cytosol following stress or tumor DNA; tumor cGAMP | [220,225,227,228] | ||
Synthetic | Cyclic dinucleotides e.g., 2′-3′-cGAMP; c-di-AMP; di-amidobenzimidazole | [301,318] | ||
RLR ligands | Organism | Ligand Class | Molecules | Literature |
Receptor | ||||
RIG-I | M/H | Pathogenic | Paramyxoviridae, Rhabdoviridae & Orthomyxoviridae; short dsRNA; dsDNA in cooperation with RNA Polymerase III; 5′-phosphorylated ssRNAs | [110,155,158,160,319] |
Endogenous | Endogeneous RNAs e.g., LINE1 | [320,321] | ||
Synthetic | poly(dA:dT); tri-phosphorylated 5′ stem-loop RNAs | [158,322,323] | ||
MDA-5 | M/H | Pathogenic | Picornaviridae; long dsRNA; ssRNA; dsDNA; NAB2; rb-dsRNA | [110,155,160,322,324] |
Endogenous | Endogeneous RNAs e.g., mitochondrial RNA and retroelement transcripts | [320,325,326,327] | ||
Synthetic | poly(I:C) | [160,322] |
4. DCs Orchestrate T Cell-Driven Immunity
4.1. The Potential of DC:T Cell-Based Vaccines and the Importance of CD4+ T Cell Help for Cancer Immunotherapy
4.2. The Priming of Naïve T Cells by DCs Is Regulated by Three Signals
4.2.1. Signal 1: pMHC Recognition by the TCR
4.2.2. Signal 2: Co-Regulatory Surface Molecules Define the Functional Phenotype of Primed T Cells
4.2.3. Signal 3: DC Cytokine Secretion Determines T Cell Polarization
5. DCs in the Tumor Microenvironment: Tipping the Scales during Anti-Cancer Immune Responses?
6. Harnessing the Potential of the Immune Systems’ Generals during Immunotherapeutic Approaches
6.1. Autologous DC Transfer Approaches for the Treatment of Malignancies
6.2. Antigen Targeting Enables the Induction of Antigen Specific T Cell Effector Modules Following Antigen Delivery to DCs In Vivo
6.2.1. The Principles of Antigen Delivery to DCs Utilizing Antigen-Coupled Targeting Antibodies In Vivo
6.2.2. Engineering of Antigen-Coupled Targeting Antibodies and Antibody-Coated Transport Vehicles
6.2.3. Factors Contributing in Rationale for DC Vaccine Design
7. Combination Therapies—Potential and Hurdles
8. Summary of DC-Based Immunotherapeutic Approaches Unleashing Anti-Tumor Immunity
9. Single Cell Omics Reshape Our Understanding of DC Biology Providing New Strategies for DC-Based Immunotherapeutic Approaches
Author Contributions
Funding
Conflicts of Interest
References
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Amon, L.; Hatscher, L.; Heger, L.; Dudziak, D.; Lehmann, C.H.K. Harnessing the Complete Repertoire of Conventional Dendritic Cell Functions for Cancer Immunotherapy. Pharmaceutics 2020, 12, 663. https://doi.org/10.3390/pharmaceutics12070663
Amon L, Hatscher L, Heger L, Dudziak D, Lehmann CHK. Harnessing the Complete Repertoire of Conventional Dendritic Cell Functions for Cancer Immunotherapy. Pharmaceutics. 2020; 12(7):663. https://doi.org/10.3390/pharmaceutics12070663
Chicago/Turabian StyleAmon, Lukas, Lukas Hatscher, Lukas Heger, Diana Dudziak, and Christian H. K. Lehmann. 2020. "Harnessing the Complete Repertoire of Conventional Dendritic Cell Functions for Cancer Immunotherapy" Pharmaceutics 12, no. 7: 663. https://doi.org/10.3390/pharmaceutics12070663
APA StyleAmon, L., Hatscher, L., Heger, L., Dudziak, D., & Lehmann, C. H. K. (2020). Harnessing the Complete Repertoire of Conventional Dendritic Cell Functions for Cancer Immunotherapy. Pharmaceutics, 12(7), 663. https://doi.org/10.3390/pharmaceutics12070663