C-type lectin receptors and RIG-I-like receptors: new points on the oncogenomics map

Figures & data

Table 1 Results of case-control studies investigating the association of polymorphisms of genes encoding C-type lectin receptors, RIG-I- like receptors, and proteins of their signaling pathways with various diseases, and conditions or features

Reference, population	SNP number, variant allele frequency in cases and controls	Disease or condition	Sample size	OR and 95% CI for carriers of variant allele (only positive or negative statistically significant results)
mrc1
Hattori et al^Citation13 Japanese, Afro-American populations	rs2477637 (Japanese 0.605–0.645, Afro-American 0.686–0.667)	Asthma	Japanese, 446 cases, 424 controls; Afro-American, 86 cases, 90 controls	Japanese, dominant model 1.38 (1.02–1.87) Afro-American, no association
	rs2253120 (Japanese 0.698–0.752, Afro-American 0.663–0.667)			Japanese, additive model 1.34 (1.07–1.68); dominant model 1.55 (1.16–2.09); Afro-American, no association
	rs2477631 (Japanese 0.484–0.522, Afro-American 0.238–0.267)			Japanese, no association; Afro-American, no association
	rs2477664 (Japanese 0.509–0.537, Afro-American 0.570–0.572)			Japanese, dominant model 1.47 (1.06–2.05); Afro-American, no association
	rs692527 (Japanese 0.521–0.559, Afro-American 0.581–0.389)			Japanese, additive model 1.25 (1.01–1.55), dominant model 1.39 (1.00–1.94); Afro-American, additive model 2.17 (1.40–3.37), dominant model 2.87 (1.43–5.80) recessive model 2.76 (1.34–5.70)
	rs1926736 (Japanese 0.568–0.522, Afro-American 0.855–0.861)			Japanese, additive model 0.76 (0.61–0.95), recessive model 0.61 (0.41–0.89) 0.61; Afro-American, no association
	rs691005 (Japanese 0.705–0.679, Afro-American 0.401–0.261)			Japanese, no association; Afro-American, additive model 1.81 (1.16–2.81), dominant model 2.43 (1.32–4.46)
Alter et al^Citation14 Vietnamese, Brazilian populations	rs1926736 (in Vietnamese controls 0.35, in Brazilian controls 0.32)	Leprosy	Vietnamese, 704 cases, 396 controls; Brazilian, 384 cases, 399 controls	Vietnamese, dominant model 0.76 (0.60–0.96), in the case with multibacillary leprosy, 0.71 (0.51–0.99); Brazilian, additive model, for carriers of wild-type G allele 1.34 (1.06–1.70), in the case with multibacillary leprosy, 1.42 (1.05–1.93)
	rs2437256 (in Vietnamese and Brazilian controls 0.21)			No association
	rs2478577 (in Vietnamese controls 0, in Brazilian controls 0.21)			No association
	rs2437257 (in Vietnamese controls 0, in Brazilian controls 0.21)			For carriers of wild-type G allele, dominant model 0.75 (0.54–1.05); in the case with multibacillary leprosy 0.63 (0.41–0.97)
Hattori et al^Citation15 Japanese population	rs2477637 (0.412–0.355, AG genotype 0.37–0.441, GG genotype 0.227–0.134)	Sarcoidosis	181 cases, 424 controls	No association
	rs2253120 (0.301–0.248, AG genotype 0.448–0.325, GG genotype 0.077–0.085)			No association
	rs2477631 (0.472–0.478, AC genotype 0.547–0.479, CC genotype 0.199–0.238)			No association
	rs2477664 (0.472–0.463, AT genotype 0.514–0.455, TT genotype 0.215–0.236)			No association
	rs692527 (0.492–0.441, AG genotype 0.464–0.505, GG genotype 0.26–0.189)			No association
	rs1926736 (0.453–0.478, AG genotype 0.475–0.521, AA genotype 0.215–0.217)			No association
	rs544995 (0.298–0.295, AG genotype 0.431–0.467, AA genotype 0.083–0.061)			No association
	rs554313 (0.34–0.396, AG genotype 0.492–0.462, AA genotype 0.094–0.153)			No association
	rs691005 (0.376–0.321, TC genotype 0.376–0.458, CC genotype 0.188–0.092)			Recessive model, 2.53 (1.47–4.37)
CD209
Xu et al^Citation16 Cantonese population	−116 promoter polymorphism (0.006 in controls)	NPC	444 cases, 464 controls	No association
	rs2287886 (0.275 in controls)			1.42 (1.15–1.74); for carriers of AG genotype, 1.41 (1.05–1.88), for carriers of GG genotype, 2.10 (1.23–3.59)
	−190 promoter polymorphism (in controls 0.003)			No association
	rs4804803 (in controls 0.085)			No association
	rs735239 (in controls 0.154)			1.47 (1.14–1.90); for carriers of AG genotype, 1.44 (1.05–1.98)
	rs735240 (in controls 0.222)			1.43 (1.15–1.79); for carriers of AA genotype, 2.52 (1.29–4.93)
Sakuntabhai et al^Citation17 Thai population	rs4804803 (0.093 in dengue disease patients, 0.023 in dengue fever patients, 0.116 in dengue hemorrhagic fever patients, 0.104 in controls)	Dengue disease, dengue fever, dengue hemorrhagic fever	606 cases, 696 controls	Risk of hemorrhage during dengue fever, 5.84 (2.77–12.31); risk of dengue fever, 0.204; decreased CD209 gene expression
	rs2287886 (0.292 in dengue disease patients, 0.266 in dengue fever patients, 0.301 in dengue hemorrhagic fever patients, 0.312 in controls)			No association
	DCSIGN1.in2+11 (0.066 in dengue patients, 0.019 in dengue fever patients, 0.081 in dengue hemorrhagic fever patients, 0.083 in controls)			Risk of hemorrhage during dengue fever, 4.60 (2.07–10.22); risk of dengue fever, 0.224
	DCSIGN1.ex4SF (0.007 in dengue patients, 0.003 in dengue fever patients, 0.009 in dengue hemorrhagic fever patients, 0.003 in controls)			No association
	DCSIGN1.ex4RPT (0.008 in dengue disease patients, 0.017 in dengue fever patients, 0.005 in dengue hemorrhagic fever patients, 0.006 in controls)			No association
	DCSIGN1.in5-178 (0.064 in dengue disease patients, 0.017 in dengue fever patients, 0.079 in dengue hemorrhagic fever patients, 0.079 in controls)			Risk of hemorrhage during dengue fever, 5.30 (2.25–12.46); risk of dengue fever, 0.201
	DCSIGN1.ex6TI (0.005 in dengue disease patients, 0.003 in dengue fever patients, 0.006 in dengue hemorrhagic fever patients, 0.005 in controls)			No association
	DCSIGN1.in6-37 (0.049 in dengue disease patients, 0.023 in dengue fever patients, 0.057 in dengue hemorrhagic fever patients, 0.064 in controls)			Risk of hemorrhage during dengue fever, 2.56 (1.19–5.52); risk of dengue fever, 0.371
	DCSIGN1.2281 (0.391 in dengue disease patients, 0.42 in dengue fever patients, 0.38 in dengue hemorrhagic fever patients, 0.344 in controls)			No association
	DCSIGN1.3197 (0.112 in dengue disease patients, 0.09 in dengue fever patients, 0.119 in dengue hemorrhagic fever patients, 0.122 in controls)			No association
	DCSIGN1.3852 (0.243 in dengue disease patients, 0.24 in dengue fever patients, 0.244 in dengue hemorrhagic fever patients, 0.267 in controls)			No association
Wang et al^Citation18 Taiwanese population	rs4804803 (0.084 in dengue patients, 0.054 in dengue fever patients, 0.122 in dengue hemorrhagic fever cases, 0.028 in other non-dengue febrile illness cases, 0.038 in controls)	Dengue disease, dengue fever, dengue hemorrhagic fever	176 dengue fever cases, 135 dengue hemorrhagic fever cases, 143 patients with other non-dengue febrile illnesses, 120 controls	Risk of dengue infection, 2.34 (1.14–4.83); risk of dengue hemorrhagic fever, 3.57 (1.67–7.63); risk of hemorrhage during dengue fever, 2.44 (1.36–4.40); increased levels of TNF-α, IL-12p40, IP-10
Barreiro et al^Citation19 South African population	rs2048022 (0,434–0.483)	Tuberculosis	351 cases, 360 controls	No association
	rs1380229 (0.361–0.384)			No association
	rs650389 (0.152–0.195)			No association
	rs870384 (0.483–0.468)			No association
	rs695982 (0.321–0.277)			No association
	rs708682 (0.118–0.123)			No association
	rs715774 (0.143–0.161)			No association
	rs1433456 (0.199–0.197)			No association
	rs807131 (0.355–0.339)			No association
	rs11672183 (0.12–0.117)			No association
	rs2024628 (0.422–0.465)			No association
	rs1028184 (0.342–0.39)			No association
	rs2056773 (0.395–0.371)			No association
	rs1479067 (0.259–0.284)			No association
	rs327747 (0.258–0.292)			No association
	rs12665321 (0.142–0.129)			No association
	rs1566838 (0.465–0.458)			No association
	rs12785524 (0.39–0.424)			No association
	rs975423 (0.351–0.378)			No association
	rs914904 (0.292–0.282)			No association
	rs876287 (0.413–0.409)			No association
	rs1582598 (0.275–0.265)			No association
	rs1364198 (0.252–0.227)			No association
	rs739259 (0.361–0.39)			No association
	rs169479 (0.133–0.115)			No association
	rs4804803 (0.454–0.402)			1.48 (1.08–2.02)
	rs735239 (0.089–0.141)			For carriers of A allele, 1.85 (1.29–2.66)
	rs735240 (0.283–0.313)			No association
	rs2287886 (0.271–0.288)			No association
Vannberg et al^Citation20 Gambian, Guinean, Guinea-Bissauan, Malawian populations	rs4804803 (in Gambian population 0.48–0.54, in Guinean population 0.489–0.47, in Guinea-Bissauan population 0.475–0.504, in Malawian population 0.352–0.364)	Tuberculosis	Gambian: 678 cases, 327 controls Guinean: 151 cases, 180 controls Guinea-Bissauan: 162 cases, 141 controls Malawian: 244 cases, 295 controls	For Gambian population, 0.75 (0.61–0.94); overall, 0.86 (0.77–0.96); for cavitating tuberculosis, 0.42 (0.27–0.65)
Selvaraj et al^Citation21 South Indian population	rs4804803 (0.181–0.223)	Tuberculosis, HIV	238 HIV cases, 107 HIV+ and tuberculosis cases, 157 controls	For carriers of GG genotype, risk of tuberculosis among HIV-infected patients, 9.8 (2.2–44.3)
	rs2287886 (0.471–0.468)			No association
	rs7252229 (0.105–0.101)			No association
	rs1544767 (0.105–0.108)			No association
Nunez et al^Citation22 Spanish population	rs4804803 (0.23–0.21)	Celiac disease	103 cases, 312 controls	For carriers of GG genotype; for HLA-DQ2(−)-individuals compared with HLA-DQ2(+) individuals and controls, 3.73 (1.18–11.03)
Nunez et al^Citation23 Spanish population	rs4804803 (0.25 in Crohn’s disease patients, 0.22 in ulcerative colitis patients, 0.22 in controls)	Crohn’s disease, ulcerative colitis	515 Crohn’s disease cases, 497 ulcerative colitis cases, 731 controls	Risk of ulcerative colitis in HLA-DR3-positive patients 1.77 (1.04–3.02)
Mezger et al^Citation24 European population	rs2287886	Human CMV reactivation and disease after allogeneic stem cell transplantation	70 patients with human CMV reactivation, 59 patients with human CMV disease, 65 controls	Risk of human CMV disease, 1.88 (0.91–3.87)
	rs735240			Risk of human CMV reactivation, 2.41 (1.22–4.75); risk of human CMV disease, 2.01 (1.05–3.86)
Zheng et al^Citation25 Chinese population	rs4804803 (0.061–0.073)	Tuberculosis	237 cases, 244 controls	0.209 (0.058–0.758)
	rs735239 (0.207–0.234)			No association
Koizumi et al^Citation26 Japanese population	rs2287886	AIDS progression	104 HIV-1-positive Japanese hemophiliacs	Risk of accelerated AIDS progression: 1.95 (1.039–3.677)
	rs4804803			No association
Kashima et al^Citation27 Mixed population from different continents	rs2287886 (0.594–0.795)	HLTV-1-infection	66 cases, 33 controls	For carriers of A allele: Risk of HTLV-1-infection: 0.3758 (0.1954–0.7229) For carriers of AA genotype: Risk of HTLV-1-infection: 0.1116 (0.02168–0.5745)
	−201 promoter polymorphism (0.038–0.016)			No association
	−332 promoter polymorphism (0.03–0)			No association
	rs4804803 (0.144–0.297)			For carriers of A allele: Risk of HTLV-1-infection: 2.511 (1.218–5.179)
Ryan et al^Citation28 Irish population	rs4804803 (0.25–0.19)	HCV infection	131 cases, 79 controls	Increased risk of advanced liver disease
Chan et al^Citation29 Hong Kong population	rs4804803	SARS	585 cases with lower LDH level, 96 cases with higher LDH level	Risk of higher LDH level during SARS, 0.41 (0.20–0.86); decreased expression of CD209 gene; Sp1 and AP2 proteins bind more effectively to G allele of rs4804803
Chan et al^Citation30 Hong Kong population	rs4804803	SARS	824 cases, 471 controls	Risk of higher LDH level during SARS, 0.41 (0.20–0.86)
CLEC7A (Dectin-1)
Plantinga et al^Citation31 Dutch population	rs16910526 (0.078–0.076)	Rheumatoid arthritis	262 cases, 284 controls	Diminished TNF-α and IL-1β production in cells from homozygous and heterozygous individuals; the TLR2/Dectin-1 synergism was reduced in cells isolated from heterozygous and homozygous subjects
Cunha et al^Citation32 Italian population	rs16910526	Invasive aspergillosis	205 cases with hematopoietic stem cell transplantation	Risk of invasive aspergillosis after hematopoietic stem cell transplantation, polymorphic donor + wild-type recipient, 2.50 (1.00–6.53) Polymorphic donor + polymorphic recipient: 3.89 (1.51–9.99) Unstimulated CD14-positive monocytes from polymorphic persons display a decreased surface expression of Dectin 1 in response to β-glucan or A conidia, PBMCs from heterozygous persons showed decreased production of IL-1β, IL-6, IL-10, IL-17A, and IFN-γ
Chai et al^Citation33 Dutch and Flemish population	rs16910526 (0.19 in patients without hematopoietic transplantation with invasive aspergillosis, 0.077 in controls, 0.07 in patients with transplantation [with and without invasive aspergillosis])	Invasive aspergillosis	71 cases with invasive aspergillosis after hematopoietic stem cell transplantation, 21 cases with invasive aspergillosis without transplantation, 108 controls with transplantation	Increased risk of invasive aspergillosis in patients without hematopoietic transplantation PBMCs from variant homozygous persons had reduced proinflammatory TNF-α and IL-6 production in response to heat-killed Aspergillus fumigatus hyphae, Candida albicans blastoconidia, and live A. fumigatus conidia; monocyte-derived macrophages from polymorphic individuals had deficient expression of the Dectin 1 receptor; stimulation using β-glucan failed to generate a TNF-α response in the Dectin 1-deficient monocyte-derived macrophages from variant homozygotes
Plantinga et al^Citation34 Dutch population	rs16910526 (0.106–0.138)	Colonization with Candida spp	142 cases with hematopoietic stem cell transplantation, 138 controls	Risk of Candida spp colonization, 12.0 (2.5–57.1); risk of Candida spp colonization after transplantation, 15.5 (1.9–125.6); monocytes from the variant homozygous individuals exhibited no Dectin 1 expression on the cell surface, whereas cells from heterozygous individuals had intermediate cell surface expression; IL-1β induction by C. albicans was lower in cells from individuals bearing the polymorphism; no possibility to amplify TLR2 signaling by Dectin 1 in cells isolated from variant homozygous individuals
Plantinga et al^Citation35 East African population	I223S	Oropharyngeal candidiasis	225 cases with HIV	IFN-γ production capacity and ability to bind zymosan was markedly lower in cells from subjects bearing the polymorphism
RIG-I
Ovsyannikova et al^Citation38 US population	rs10813821	Cytokine immune response in healthy children following rubella vaccination	738 cases	Increased level of IFN-γ
	rs9650702			Increased level of IFN-γ and decreased level of GM-CSF
	rs626214			Increased level of IFN-γ
	rs592515			Increased level of IFN-γ and TNF-α
	rs6476363			Decreased level of TNF-α
	rs3739674			Decreased level of TNF-α
	rs10813829			Decreased level of TNF-α
	rs4633144			Decreased level of TNF-α
	rs3824456			Increased level of TNF-α
	rs10813831			Decreased level of GM-CSF and IL-6
Ovsyannikova et al^Citation39 US population	rs10813831	Cytokine immune response in healthy children following rubella vaccination	738 cases	Decreased rubella-specific antibody response (median antibody level)
	rs669260			Increased rubella-specific antibody response
Hu et al^Citation40 US population	rs10813831	Cytokine immune response to Newcastle disease	130 cases	Increased gene expression in Newcastle disease virus-infected cells
	rs12006123			No association
MAVS/VISA/IPS-1
Pothlichet et al^Citation50 Mixed population	rs11905552 (0.126–0.102 in Afro-American population, 0.013–0 in European-American population)	SLE	520 cases, 510 controls	For Afro-American population, probability of absence of anti-RNA-binding protein autoantibodies 2.6 (1.5–4.6); decreased level of NF-κB, IL-8, IFN-β and RANTES; significantly reduced interaction of MAVS with TRAF3
	Q198K (0.187–0.2 in African-American population, 0.128–0.155 in European-American population)			No association
Liu et al^Citation51 Chinese population	rs17857295 (0.496–0.468)	SLE	123 cases, 95 controls	Risk of SLE-related renal nephritis, 0.58 [0.34–0.97]
	rs2326369 (0.272–0.232)			Risk of SLE-related arthritis, 0.27 (0.09–0.80)
	rs7262903 (0.098–0.147)			No association
	rs7269320 (0.098–0.11)			Association with patients positive for SLE-related arthritis, 0.45 (0.21–0.94); association with patients positive for SLE-related renal nephritis, 0.42 (0.18–0.98); association with patients negative for SLE-related oral ulcer, 0.40 (0.18–0.89); association with patients negative for SLE-related photosensitivity, 0.38 (0.17–0.89)

Abbreviations: SNP, single nucleotide polymorphism; OR, odds ratio; CI, confidence interval; MRC, mannose receptor C; CD, cluster of differentiation; NPC, nasopharyngeal carcinoma; DC-SIGN, dendritic cell-specific intercellular adhesion molecule-3-grabbing non-integrin; TNF, tumor necrosis factor; IL, interleukin; IP, interferon-gamma inducible protein 10; HIV, human immunodeficiency virus; AIDS, acquired immunodeficiency virus; HTLV, human T-cell lymphotropic virus; HCV, hepatitis C virus; SARS, severe acute respiratory syndrome; LDH, lactate dehydrogenase; Sp, specificity protein; AP, activator protein; CLEC, C-type lectin domain, the next number is the family number 7, the next letter is the letter of family member; TLR, toll-like receptor; PBMC, peripheral blood mononuclear cell; IFN, interferon; RIG-I, retinoic acid-inducible gene I; GM-CSF, granulocyte-macrophage colony-stimulating factor; MAVS/VISA/IPS-1, mitochondrial antiviral signaling protein/virus-induced signaling adapter/induced by phosphate starvation-1; NF-κB, necrosis factor kappa B; RANTES, regulated on activation, normal T-cell expressed and secreted; TRAF, TNF receptor-associated factor; SLE, systemic lupus erythematosus.

Table 2 Polymorphisms of genes encoding C-type lectin receptors, RIG-I-like receptors, and proteins of their specific signaling pathways that have known functional consequences and may be relevant to oncogenomics

Gene	Single nucleotide polymorphism
Genes encoding CLRs
MRC1	rs1926736*
	rs2478577*
	rs2437257*
	rs691005*
	rs2477664
	rs692527
	rs2253120
	rs2477637
CD209	rs2287886*
	rs735239*
	rs4804803*
	rs735240*
CLEC7A	rs16910526*
	I223S
Genes encoding RLRs
RIG-I	rs36055726*
	rs11795404*
	rs10813831*
	rs3824456
	rs669260
	rs9650702
	rs626214
	rs592515
	rs6476363
	rs3739674
	rs10813829
	rs4633144
	rs10813821
Genes encoding proteins of CLR and RLR intracellular signaling pathways
MAVS/VISA/IPS-1	rs11905552
	rs17857295
	rs2326369
	rs7269320

Note:

* Single nucleotide polymorphisms that can be valued as the most promising for further oncogenomic investigation.

Abbreviations: PRRs, pattern recognition receptors; PAMPs, pathogen-associated molecular patterns; DAMPs, damage-associated molecular patterns; TLRs, Toll- like receptors; NLRs, NOD-like receptors; CLRs, C-type lectin receptors; RLRs, RIG- I-like receptors; SNPs, single nucleotide polymorphisms; MRC, mannose receptor C; CD, cluster of differentiation; CLEC, C-type lectin domain, the next number is the family number 7, the next letter is the letter of family member; HIV, human immunodeficiency virus; LY, lymphocyte antigen; DEC-205, dendritic and epithelial cells 205 kDa; DC- SIGN, dendritic cell-specific intercellular adhesion molecule-3-grabbing non-integrin; HCV, hepatitis C virus; CMV, cytomegalovirus; DCIR, dendritic cell immunoreceptor; RIG-I, retinoic acid-inducible gene I; EBV, Epstein–Barr virus; CARD, caspase recruitment domain; MAVS, mitochondrial antiviral signaling protein; IFIH, interferon induced with helicase C domain; MDA, melanoma differentiation-associated gene; VISA, virus- induced signaling adapter; IPS-1, induced by phosphate starvation-1.

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