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CC BY 4.0 · Semin Liver Dis 2022; 42(01): 061-076
DOI: 10.1055/s-0041-1733876
Review Article

Scavenger Receptors: Novel Roles in the Pathogenesis of Liver Inflammation and Cancer

Daniel A. Patten‡   *
1   National Institute for Health Research Birmingham Liver Biomedical Research Unit, Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, United Kingdom
2   Centre for Liver and Gastrointestinal Research, Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, United Kingdom
,
Alex L. Wilkinson‡   *
1   National Institute for Health Research Birmingham Liver Biomedical Research Unit, Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, United Kingdom
2   Centre for Liver and Gastrointestinal Research, Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, United Kingdom
,
Ayla O'Keeffe
1   National Institute for Health Research Birmingham Liver Biomedical Research Unit, Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, United Kingdom
2   Centre for Liver and Gastrointestinal Research, Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, United Kingdom
,
Shishir Shetty
1   National Institute for Health Research Birmingham Liver Biomedical Research Unit, Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, United Kingdom
2   Centre for Liver and Gastrointestinal Research, Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, United Kingdom
› Institutsangaben Funding Funding received from Cancer Research UK under the ID: C53575/A29959; funding received from the Wellcome Trust under MIDAS Mechanisms of Inflammatory Disease.
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Erratum zu diesem Artikel:

Erratum to: Scavenger Receptors: Novel Roles in the Pathogenesis of Liver Inflammation and CancerSemin Liver Dis 2022; 42(01): e1-e1
DOI: 10.1055/s-0041-1739050

Abstract

The scavenger receptor superfamily represents a highly diverse collection of evolutionarily-conserved receptors which are known to play key roles in host homeostasis, the most prominent of which is the clearance of unwanted endogenous macromolecules, such as oxidized low-density lipoproteins, from the systemic circulation. Members of this family have also been well characterized in their binding and internalization of a vast range of exogenous antigens and, consequently, are generally considered to be pattern recognition receptors, thus contributing to innate immunity. Several studies have implicated scavenger receptors in the pathophysiology of several inflammatory diseases, such as Alzheimer's and atherosclerosis. Hepatic resident cellular populations express a diverse complement of scavenger receptors in keeping with the liver's homeostatic functions, but there is gathering interest in the contribution of these receptors to hepatic inflammation and its complications. Here, we review the expression of scavenger receptors in the liver, their functionality in liver homeostasis, and their role in inflammatory liver disease and cancer.

Keywords

scavenger receptors - macrophages - liver sinusoidal endothelial cells - cirrhosis - hepatocellular carcinoma

* These authors contributed equally to this work.




Publikationsverlauf

Artikel online veröffentlicht:
22. September 2021

© 2021. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

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  • References

  • 1 Global World Health Organisation. Global Health Estimates 2020: deaths by cause, age, sex, by country and by region, 2000–2019. Published 2020. Accessed April 27, 2021 at: https://www.who.int/data/gho/data/themes/mortality-and-global-health-estimates/ghe-leading-causes-of-death
    PubMedGoogle Scholar
  • 2 Ibrahim SH, Hirsova P, Gores GJ. Non-alcoholic steatohepatitis pathogenesis: sublethal hepatocyte injury as a driver of liver inflammation. Gut 2018; 67 (05) 963-972
    CrossrefPubMedGoogle Scholar
  • 3 Hirschfield GM, Karlsen TH, Lindor KD, Adams DH. Primary sclerosing cholangitis. Lancet 2013; 382 (9904): 1587-1599
    CrossrefPubMedGoogle Scholar
  • 4 Tsuchida T, Friedman SL. Mechanisms of hepatic stellate cell activation. Nat Rev Gastroenterol Hepatol 2017; 14 (07) 397-411
    CrossrefPubMedGoogle Scholar
  • 5 British Liver Trust. The alarming impact of liver disease in the UK. Published 2019. Updated June 2019. Accessed July 13, 2021 at: https://britishlivertrust.org.uk/wp-content/uploads/The-alarming-impact-of-liver-disease-FINAL-June-2019.pdf
    PubMedGoogle Scholar
  • 6 Pimpin L, Cortez-Pinto H, Negro F. et al; EASL HEPAHEALTH Steering Committee. Burden of liver disease in Europe: Epidemiology and analysis of risk factors to identify prevention policies. J Hepatol 2018; 69 (03) 718-735
    CrossrefPubMedGoogle Scholar
  • 7 O'Rourke JM, Sagar VM, Shah T, Shetty S. Carcinogenesis on the background of liver fibrosis: implications for the management of hepatocellular cancer. World J Gastroenterol 2018; 24 (39) 4436-4447
    CrossrefPubMedGoogle Scholar
  • 8 Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68 (06) 394-424
    CrossrefPubMedGoogle Scholar
  • 9 Canton J, Neculai D, Grinstein S. Scavenger receptors in homeostasis and immunity. Nat Rev Immunol 2013; 13 (09) 621-634
    CrossrefPubMedGoogle Scholar
  • 10 Goldstein JL, Ho YK, Basu SK, Brown MS. Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc Natl Acad Sci U S A 1979; 76 (01) 333-337
    CrossrefPubMedGoogle Scholar
  • 11 PrabhuDas MR, Baldwin CL, Bollyky PL. et al. A consensus definitive classification of scavenger receptors and their roles in health and disease. J Immunol 2017; 198 (10) 3775-3789
    CrossrefPubMedGoogle Scholar
  • 12 Krieger M. The other side of scavenger receptors: pattern recognition for host defense. Curr Opin Lipidol 1997; 8 (05) 275-280
    CrossrefPubMedGoogle Scholar
  • 13 Yu X, Guo C, Fisher PB, Subjeck JR, Wang XY. Scavenger receptors: emerging roles in cancer biology and immunology. Adv Cancer Res 2015; 128: 309-364
    CrossrefPubMedGoogle Scholar
  • 14 Ramirez-Ortiz ZG, Pendergraft III WF, Prasad A. et al. The scavenger receptor SCARF1 mediates the clearance of apoptotic cells and prevents autoimmunity. Nat Immunol 2013; 14 (09) 917-926
    CrossrefPubMedGoogle Scholar
  • 15 Wermeling F, Chen Y, Pikkarainen T. et al. Class A scavenger receptors regulate tolerance against apoptotic cells, and autoantibodies against these receptors are predictive of systemic lupus. J Exp Med 2007; 204 (10) 2259-2265
    CrossrefPubMedGoogle Scholar
  • 16 Thanopoulou K, Fragkouli A, Stylianopoulou F, Georgopoulos S. Scavenger receptor class B type I (SR-BI) regulates perivascular macrophages and modifies amyloid pathology in an Alzheimer mouse model. Proc Natl Acad Sci U S A 2010; 107 (48) 20816-20821
    CrossrefPubMedGoogle Scholar
  • 17 Rantakari P, Patten DA, Valtonen J. et al. Stabilin-1 expression defines a subset of macrophages that mediate tissue homeostasis and prevent fibrosis in chronic liver injury. Proc Natl Acad Sci U S A 2016; 113 (33) 9298-9303
    CrossrefPubMedGoogle Scholar
  • 18 Kennedy DJ, Kashyap SR. Pathogenic role of scavenger receptor CD36 in the metabolic syndrome and diabetes. Metab Syndr Relat Disord 2011; 9 (04) 239-245
    CrossrefPubMedGoogle Scholar
  • 19 El Khoury JB, Moore KJ, Means TK. et al. CD36 mediates the innate host response to β-amyloid. J Exp Med 2003; 197 (12) 1657-1666
    CrossrefPubMedGoogle Scholar
  • 20 Armengol C, Bartolí R, Sanjurjo L. et al. Role of scavenger receptors in the pathophysiology of chronic liver diseases. Crit Rev Immunol 2013; 33 (01) 57-96
    PubMedGoogle Scholar
  • 21 Sørensen KK, McCourt P, Berg T. et al. The scavenger endothelial cell: a new player in homeostasis and immunity. Am J Physiol Regul Integr Comp Physiol 2012; 303 (12) R1217-R1230
    CrossrefPubMedGoogle Scholar
  • 22 Wilkinson AL, Qurashi M, Shetty S. The role of sinusoidal endothelial cells in the axis of inflammation and cancer within the liver. Front Physiol 2020; 11: 990
    CrossrefPubMedGoogle Scholar
  • 23 Li R, Oteiza A, Sørensen KK. et al. Role of liver sinusoidal endothelial cells and stabilins in elimination of oxidized low-density lipoproteins. Am J Physiol Gastrointest Liver Physiol 2011; 300 (01) G71-G81
    CrossrefPubMedGoogle Scholar
  • 24 Politz O, Gratchev A, McCourt PA. et al. Stabilin-1 and -2 constitute a novel family of fasciclin-like hyaluronan receptor homologues. Biochem J 2002; 362 (Pt 1): 155-164
    CrossrefPubMedGoogle Scholar
  • 25 Harris EN, Cabral F. Ligand binding and signaling of HARE/Stabilin-2. Biomolecules 2019; 9 (07) 273
    CrossrefPubMedGoogle Scholar
  • 26 Witztum JL, Steinberg D. Role of oxidized low density lipoprotein in atherogenesis. J Clin Invest 1991; 88 (06) 1785-1792
    CrossrefPubMedGoogle Scholar
  • 27 Schledzewski K, Géraud C, Arnold B. et al. Deficiency of liver sinusoidal scavenger receptors stabilin-1 and -2 in mice causes glomerulofibrotic nephropathy via impaired hepatic clearance of noxious blood factors. J Clin Invest 2011; 121 (02) 703-714
    CrossrefPubMedGoogle Scholar
  • 28 Malovic I, Sørensen KK, Elvevold KH. et al. The mannose receptor on murine liver sinusoidal endothelial cells is the main denatured collagen clearance receptor. Hepatology 2007; 45 (06) 1454-1461
    CrossrefPubMedGoogle Scholar
  • 29 Smedsrød B, Melkko J, Risteli L, Risteli J. Circulating C-terminal propeptide of type I procollagen is cleared mainly via the mannose receptor in liver endothelial cells. Biochem J 1990; 271 (02) 345-350
    CrossrefPubMedGoogle Scholar
  • 30 Elvevold K, Simon-Santamaria J, Hasvold H, McCourt P, Smedsrød B, Sørensen KK. Liver sinusoidal endothelial cells depend on mannose receptor-mediated recruitment of lysosomal enzymes for normal degradation capacity. Hepatology 2008; 48 (06) 2007-2015
    CrossrefPubMedGoogle Scholar
  • 31 Rijken DC, Otter M, Kuiper J, van Berkel TJ. Receptor-mediated endocytosis of tissue-type plasminogen activator (t-PA) by liver cells. Thromb Res 1990; 10: 63-71
    CrossrefPubMedGoogle Scholar
  • 32 Martinez-Pomares L. The mannose receptor. J Leukoc Biol 2012; 92 (06) 1177-1186
    CrossrefPubMedGoogle Scholar
  • 33 Smedsrød B, Melkko J, Araki N, Sano H, Horiuchi S. Advanced glycation end products are eliminated by scavenger-receptor-mediated endocytosis in hepatic sinusoidal Kupffer and endothelial cells. Biochem J 1997; 322 (Pt 2): 567-573
    CrossrefPubMedGoogle Scholar
  • 34 Lee SJ, Evers S, Roeder D. et al. Mannose receptor-mediated regulation of serum glycoprotein homeostasis. Science 2002; 295 (5561): 1898-1901
    CrossrefPubMedGoogle Scholar
  • 35 Pombinho R, Sousa S, Cabanes D. Scavenger receptors: promiscuous players during microbial pathogenesis. Crit Rev Microbiol 2018; 44 (06) 685-700
    CrossrefPubMedGoogle Scholar
  • 36 Tripathi A, Debelius J, Brenner DA. et al. The gut-liver axis and the intersection with the microbiome. Nat Rev Gastroenterol Hepatol 2018; 15 (07) 397-411
    CrossrefPubMedGoogle Scholar
  • 37 Broadley SP, Plaumann A, Coletti R. et al. Dual-track clearance of circulating bacteria balances rapid restoration of blood sterility with induction of adaptive immunity. Cell Host Microbe 2016; 20 (01) 36-48
    CrossrefPubMedGoogle Scholar
  • 38 Ishiguro T, Naito M, Yamamoto T. et al. Role of macrophage scavenger receptors in response to Listeria monocytogenes infection in mice. Am J Pathol 2001; 158 (01) 179-188
    CrossrefPubMedGoogle Scholar
  • 39 Means TK, Mylonakis E, Tampakakis E. et al. Evolutionarily conserved recognition and innate immunity to fungal pathogens by the scavenger receptors SCARF1 and CD36. J Exp Med 2009; 206 (03) 637-653
    CrossrefPubMedGoogle Scholar
  • 40 Helmy KY, Katschke Jr KJ, Gorgani NN. et al. CRIg: a macrophage complement receptor required for phagocytosis of circulating pathogens. Cell 2006; 124 (05) 915-927
    CrossrefPubMedGoogle Scholar
  • 41 Gorgani NN, He JQ, Katschke Jr KJ. et al. Complement receptor of the Ig superfamily enhances complement-mediated phagocytosis in a subpopulation of tissue resident macrophages. J Immunol 2008; 181 (11) 7902-7908
    CrossrefPubMedGoogle Scholar
  • 42 Zeng Z, Surewaard BG, Wong CH, Geoghegan JA, Jenne CN, Kubes P. CRIg functions as a macrophage pattern recognition receptor to directly bind and capture blood-borne gram-positive bacteria. Cell Host Microbe 2016; 20 (01) 99-106
    CrossrefPubMedGoogle Scholar
  • 43 Heinsbroek SE, Taylor PR, Martinez FO, Martinez-Pomares L, Brown GD, Gordon S. Stage-specific sampling by pattern recognition receptors during Candida albicans phagocytosis. PLoS Pathog 2008; 4 (11) e1000218
    CrossrefPubMedGoogle Scholar
  • 44 Stewart CR, Stuart LM, Wilkinson K. et al. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol 2010; 11 (02) 155-161
    CrossrefPubMedGoogle Scholar
  • 45 Heit B, Kim H, Cosío G. et al. Multimolecular signaling complexes enable Syk-mediated signaling of CD36 internalization. Dev Cell 2013; 24 (04) 372-383
    CrossrefPubMedGoogle Scholar
  • 46 Triantafilou M, Gamper FG, Haston RM. et al. Membrane sorting of toll-like receptor (TLR)-2/6 and TLR2/1 heterodimers at the cell surface determines heterotypic associations with CD36 and intracellular targeting. J Biol Chem 2006; 281 (41) 31002-31011
    CrossrefPubMedGoogle Scholar
  • 47 Murshid A, Borges TJ, Lang BJ, Calderwood SK. The scavenger receptor SREC-I cooperates with toll-like receptors to trigger inflammatory innate immune responses. Front Immunol 2016; 7 (226) 226
    PubMedGoogle Scholar
  • 48 Jeannin P, Bottazzi B, Sironi M. et al. Complexity and complementarity of outer membrane protein A recognition by cellular and humoral innate immunity receptors. Immunity 2005; 22 (05) 551-560
    CrossrefPubMedGoogle Scholar
  • 49 Beauvillain C, Meloni F, Sirard J-C. et al. The scavenger receptors SRA-1 and SREC-I cooperate with TLR2 in the recognition of the hepatitis C virus non-structural protein 3 by dendritic cells. J Hepatol 2010; 52 (05) 644-651
    CrossrefPubMedGoogle Scholar
  • 50 Murshid A, Gong J, Prince T, Borges TJ, Calderwood SK. Scavenger receptor SREC-I mediated entry of TLR4 into lipid microdomains and triggered inflammatory cytokine release in RAW 264.7 cells upon LPS activation. PLoS One 2015; 10 (04) e0122529
    CrossrefPubMedGoogle Scholar
  • 51 Murshid A, Gong J, Ahmad R, Borges TJ, Calderwood SK. Scavenger receptor SREC-I promotes double stranded RNA-mediated TLR3 activation in human monocytes. Immunobiology 2015; 220 (06) 823-832
    CrossrefPubMedGoogle Scholar
  • 52 Komai K, Shichita T, Ito M, Kanamori M, Chikuma S, Yoshimura A. Role of scavenger receptors as damage-associated molecular pattern receptors in Toll-like receptor activation. Int Immunol 2017; 29 (02) 59-70
    CrossrefPubMedGoogle Scholar
  • 53 Hawkes M, Li X, Crockett M. et al. CD36 deficiency attenuates experimental mycobacterial infection. BMC Infect Dis 2010; 10 (01) 299
    CrossrefPubMedGoogle Scholar
  • 54 Cha S-J, Park K, Srinivasan P. et al. CD68 acts as a major gateway for malaria sporozoite liver infection. J Exp Med 2015; 212 (09) 1391-1403
    CrossrefPubMedGoogle Scholar
  • 55 Guillot A, Tacke F. Liver macrophages: old dogmas and new insights. Hepatol Commun 2019; 3 (06) 730-743
    CrossrefPubMedGoogle Scholar
  • 56 Yao Z, Mates JM, Cheplowitz AM. et al. Blood-borne lipopolysaccharide is rapidly eliminated by liver sinusoidal endothelial cells via high-density lipoprotein. J Immunol 2016; 197 (06) 2390-2399
    CrossrefPubMedGoogle Scholar
  • 57 Ganesan LP, Mohanty S, Kim J, Clark KR, Robinson JM, Anderson CL. Rapid and efficient clearance of blood-borne virus by liver sinusoidal endothelium. PLoS Pathog 2011; 7 (09) e1002281
    CrossrefPubMedGoogle Scholar
  • 58 Mates JM, Yao Z, Cheplowitz AM. et al. Mouse liver sinusoidal endothelium eliminates HIV-like particles from blood at a rate of 100 million per minute by a second-order kinetic process. Front Immunol 2017; 8: 35
    CrossrefPubMedGoogle Scholar
  • 59 Uhrig A, Banafsche R, Kremer M. et al. Development and functional consequences of LPS tolerance in sinusoidal endothelial cells of the liver. J Leukoc Biol 2005; 77 (05) 626-633
    CrossrefPubMedGoogle Scholar
  • 60 Patten DA, Kamarajah SK, Rose JM. et al. SCARF-1 promotes adhesion of CD4+ T cells to human hepatic sinusoidal endothelium under conditions of shear stress. Sci Rep 2017; 7 (01) 17600
    CrossrefPubMedGoogle Scholar
  • 61 Øie CI, Wolfson DL, Yasunori T. et al. Liver sinusoidal endothelial cells contribute to the uptake and degradation of entero bacterial viruses. Sci Rep 2020; 10 (01) 898
    CrossrefPubMedGoogle Scholar
  • 62 Cabral F, Al-Rahem M, Skaggs J, Thomas TA, Kumar N, Wu Q, Fadda P, Yu L, Robinson JM, (Lt.) Kim J, Jarjour WN, Rajaram MVS, Harris EN, Ganesan LP. Stabilin receptors clear LPS and control systemic inflammation. Last accessed on July 23, 2021 at SSRN: https://ssrn.com/abstract=3845681 or http://dx.doi.org/10.2139/ssrn.3845681
    CrossrefPubMedGoogle Scholar
  • 63 Limmer A, Ohl J, Kurts C. et al. Efficient presentation of exogenous antigen by liver endothelial cells to CD8+ T cells results in antigen-specific T-cell tolerance. Nat Med 2000; 6 (12) 1348-1354
    CrossrefPubMedGoogle Scholar
  • 64 Schurich A, Böttcher JP, Burgdorf S. et al. Distinct kinetics and dynamics of cross-presentation in liver sinusoidal endothelial cells compared to dendritic cells. Hepatology 2009; 50 (03) 909-919
    CrossrefPubMedGoogle Scholar
  • 65 Shetty S, Lalor PF, Adams DH. Liver sinusoidal endothelial cells - gatekeepers of hepatic immunity. Nat Rev Gastroenterol Hepatol 2018; 15 (09) 555-567
    CrossrefPubMedGoogle Scholar
  • 66 Limmer A, Ohl J, Wingender G. et al. Cross-presentation of oral antigens by liver sinusoidal endothelial cells leads to CD8 T cell tolerance. Eur J Immunol 2005; 35 (10) 2970-2981
    CrossrefPubMedGoogle Scholar
  • 67 Diehl L, Schurich A, Grochtmann R, Hegenbarth S, Chen L, Knolle PA. Tolerogenic maturation of liver sinusoidal endothelial cells promotes B7-homolog 1-dependent CD8+ T cell tolerance. Hepatology 2008; 47 (01) 296-305
    CrossrefPubMedGoogle Scholar
  • 68 Berg M, Wingender G, Djandji D. et al. Cross-presentation of antigens from apoptotic tumor cells by liver sinusoidal endothelial cells leads to tumor-specific CD8+ T cell tolerance. Eur J Immunol 2006; 36 (11) 2960-2970
    CrossrefPubMedGoogle Scholar
  • 69 Höchst B, Schildberg FA, Böttcher J. et al. Liver sinusoidal endothelial cells contribute to CD8 T cell tolerance toward circulating carcinoembryonic antigen in mice. Hepatology 2012; 56 (05) 1924-1933
    CrossrefPubMedGoogle Scholar
  • 70 Fontana RJ. Acute liver failure including acetaminophen overdose. Med Clin North Am 2008; 92 (04) 761-794 , viii
    CrossrefPubMedGoogle Scholar
  • 71 Yoon E, Babar A, Choudhary M, Kutner M, Pyrsopoulos N. Acetaminophen-induced hepatotoxicity: a comprehensive update. J Clin Transl Hepatol 2016; 4 (02) 131-142
    PubMedGoogle Scholar
  • 72 Triantafyllou E, Woollard KJ, McPhail MJW, Antoniades CG, Possamai LA. The role of monocytes and macrophages in acute and acute-on-chronic liver failure. Front Immunol 2018; 9: 2948
    CrossrefPubMedGoogle Scholar
  • 73 Hiraoka A, Horiike N, Akbar SM, Michitaka K, Matsuyama T, Onji M. Soluble CD163 in patients with liver diseases: very high levels of soluble CD163 in patients with fulminant hepatic failure. J Gastroenterol 2005; 40 (01) 52-56
    CrossrefPubMedGoogle Scholar
  • 74 Møller HJ, Grønbaek H, Schiødt FV. et al; U.S. Acute Liver Failure Study Group. Soluble CD163 from activated macrophages predicts mortality in acute liver failure. J Hepatol 2007; 47 (05) 671-676
    CrossrefPubMedGoogle Scholar
  • 75 Siggaard CB, Kazankov K, Rødgaard-Hansen S. et al. Macrophage markers soluble CD163 and soluble mannose receptor are associated with liver injury in patients with paracetamol overdose. Scand J Gastroenterol 2019; 54 (05) 623-632
    CrossrefPubMedGoogle Scholar
  • 76 Grønbæk H, Rødgaard-Hansen S, Aagaard NK. et al; CANONIC study investigators of the EASL-CLIF Consortium. Macrophage activation markers predict mortality in patients with liver cirrhosis without or with acute-on-chronic liver failure (ACLF). J Hepatol 2016; 64 (04) 813-822
    CrossrefPubMedGoogle Scholar
  • 77 Nielsen MC, Hvidbjerg Gantzel R, Clària J, Trebicka J, Møller HJ, Grønbæk H. Macrophage activation markers, CD163 and CD206, in acute-on-chronic liver failure. Cells 2020; 9 (05) 1175
    CrossrefPubMedGoogle Scholar
  • 78 Zuo D, Yu X, Guo C. et al. Scavenger receptor A restrains T-cell activation and protects against concanavalin A-induced hepatic injury. Hepatology 2013; 57 (01) 228-238
    CrossrefPubMedGoogle Scholar
  • 79 Labonte AC, Sung SJ, Jennelle LT, Dandekar AP, Hahn YS. Expression of scavenger receptor-AI promotes alternative activation of murine macrophages to limit hepatic inflammation and fibrosis. Hepatology 2017; 65 (01) 32-43
    CrossrefPubMedGoogle Scholar
  • 80 Patten DA, Shetty S. More than just a removal service: scavenger receptors in leukocyte trafficking. Front Immunol 2018; 9: 2904
    CrossrefPubMedGoogle Scholar
  • 81 Patten DA, Shetty S. The role of Stabilin-1 in lymphocyte trafficking and macrophage scavenging in the liver microenvironment. Biomolecules 2019; 9 (07) 283
    CrossrefPubMedGoogle Scholar
  • 82 Irjala H, Alanen K, Grénman R, Heikkilä P, Joensuu H, Jalkanen S. Mannose receptor (MR) and common lymphatic endothelial and vascular endothelial receptor (CLEVER)-1 direct the binding of cancer cells to the lymph vessel endothelium. Cancer Res 2003; 63 (15) 4671-4676
    PubMedGoogle Scholar
  • 83 Irjala H, Elima K, Johansson EL. et al. The same endothelial receptor controls lymphocyte traffic both in vascular and lymphatic vessels. Eur J Immunol 2003; 33 (03) 815-824
    CrossrefPubMedGoogle Scholar
  • 84 Salmi M, Koskinen K, Henttinen T, Elima K, Jalkanen S. CLEVER-1 mediates lymphocyte transmigration through vascular and lymphatic endothelium. Blood 2004; 104 (13) 3849-3857
    CrossrefPubMedGoogle Scholar
  • 85 Karikoski M, Irjala H, Maksimow M. et al. Clever-1/Stabilin-1 regulates lymphocyte migration within lymphatics and leukocyte entrance to sites of inflammation. Eur J Immunol 2009; 39 (12) 3477-3487
    CrossrefPubMedGoogle Scholar
  • 86 Shetty S, Weston CJ, Adams DH, Lalor PF. A flow adhesion assay to study leucocyte recruitment to human hepatic sinusoidal endothelium under conditions of shear stress. J Vis Exp 2014; (85) 51330
    PubMedGoogle Scholar
  • 87 Shetty S, Weston CJ, Oo YH. et al. Common lymphatic endothelial and vascular endothelial receptor-1 mediates the transmigration of regulatory T cells across human hepatic sinusoidal endothelium. J Immunol 2011; 186 (07) 4147-4155
    CrossrefPubMedGoogle Scholar
  • 88 Shetty S, Bruns T, Weston CJ. et al. Recruitment mechanisms of primary and malignant B cells to the human liver. Hepatology 2012; 56 (04) 1521-1531
    CrossrefPubMedGoogle Scholar
  • 89 Patten DA, Wilson GK, Bailey D. et al. Human liver sinusoidal endothelial cells promote intracellular crawling of lymphocytes during recruitment: a new step in migration. Hepatology 2017; 65 (01) 294-309
    CrossrefPubMedGoogle Scholar
  • 90 Falkowski M, Schledzewski K, Hansen B, Goerdt S. Expression of stabilin-2, a novel fasciclin-like hyaluronan receptor protein, in murine sinusoidal endothelia, avascular tissues, and at solid/liquid interfaces. Histochem Cell Biol 2003; 120 (05) 361-369
    CrossrefPubMedGoogle Scholar
  • 91 Jung MY, Park SY, Kim IS. Stabilin-2 is involved in lymphocyte adhesion to the hepatic sinusoidal endothelium via the interaction with alphaMbeta2 integrin. J Leukoc Biol 2007; 82 (05) 1156-1165
    CrossrefPubMedGoogle Scholar
  • 92 Géraud C, Koch P-S, Zierow J. et al. GATA4-dependent organ-specific endothelial differentiation controls liver development and embryonic hematopoiesis. J Clin Invest 2017; 127 (03) 1099-1114
    CrossrefPubMedGoogle Scholar
  • 93 Shimaoka T, Nakayama T, Fukumoto N. et al. Cell surface-anchored SR-PSOX/CXC chemokine ligand 16 mediates firm adhesion of CXC chemokine receptor 6-expressing cells. J Leukoc Biol 2004; 75 (02) 267-274
    CrossrefPubMedGoogle Scholar
  • 94 Yamauchi R, Tanaka M, Kume N. et al. Upregulation of SR-PSOX/CXCL16 and recruitment of CD8+ T cells in cardiac valves during inflammatory valvular heart disease. Arterioscler Thromb Vasc Biol 2004; 24 (02) 282-287
    CrossrefPubMedGoogle Scholar
  • 95 Jiang X, Shimaoka T, Kojo S. et al. Cutting edge: critical role of CXCL16/CXCR6 in NKT cell trafficking in allograft tolerance. J Immunol 2005; 175 (04) 2051-2055
    CrossrefPubMedGoogle Scholar
  • 96 Ruth JH, Haas CS, Park CC. et al. CXCL16-mediated cell recruitment to rheumatoid arthritis synovial tissue and murine lymph nodes is dependent upon the MAPK pathway. Arthritis Rheum 2006; 54 (03) 765-778
    CrossrefPubMedGoogle Scholar
  • 97 Heydtmann M, Lalor PF, Eksteen JA, Hübscher SG, Briskin M, Adams DH. CXC chemokine ligand 16 promotes integrin-mediated adhesion of liver-infiltrating lymphocytes to cholangiocytes and hepatocytes within the inflamed human liver. J Immunol 2005; 174 (02) 1055-1062
    CrossrefPubMedGoogle Scholar
  • 98 Sato T, Thorlacius H, Johnston B. et al. Role for CXCR6 in recruitment of activated CD8+ lymphocytes to inflamed liver. J Immunol 2005; 174 (01) 277-283
    CrossrefPubMedGoogle Scholar
  • 99 Hudspeth K, Donadon M, Cimino M. et al. Human liver-resident CD56(bright)/CD16(neg) NK cells are retained within hepatic sinusoids via the engagement of CCR5 and CXCR6 pathways. J Autoimmun 2016; 66: 40-50
    CrossrefPubMedGoogle Scholar
  • 100 Stegmann KA, Robertson F, Hansi N. et al. CXCR6 marks a novel subset of T-bet(lo)Eomes(hi) natural killer cells residing in human liver. Sci Rep 2016; 6 (01) 26157
    CrossrefPubMedGoogle Scholar
  • 101 Geissmann F, Cameron TO, Sidobre S. et al. Intravascular immune surveillance by CXCR6+ NKT cells patrolling liver sinusoids. PLoS Biol 2005; 3 (04) e113
    CrossrefPubMedGoogle Scholar
  • 102 Xu H-B, Gong Y-P, Cheng J, Chu Y-W, Xiong S-D. CXCL16 participates in pathogenesis of immunological liver injury by regulating T lymphocyte infiltration in liver tissue. World J Gastroenterol 2005; 11 (32) 4979-4985
    CrossrefPubMedGoogle Scholar
  • 103 Xu H, Xu W, Chu Y, Gong Y, Jiang Z, Xiong S. Involvement of up-regulated CXC chemokine ligand 16/scavenger receptor that binds phosphatidylserine and oxidized lipoprotein in endotoxin-induced lethal liver injury via regulation of T-cell recruitment and adhesion. Infect Immun 2005; 73 (07) 4007-4016
    CrossrefPubMedGoogle Scholar
  • 104 Wang H, Shao Y, Zhang S. et al. CXCL16 deficiency attenuates acetaminophen-induced hepatotoxicity through decreasing hepatic oxidative stress and inflammation in mice. Acta Biochim Biophys Sin (Shanghai) 2017; 49 (06) 541-549
    CrossrefPubMedGoogle Scholar
  • 105 Wehr A, Tacke F. The roles of CXCL16 and CXCR6 in liver inflammation and fibrosis. Curr Pathobiol Rep 2015; 3 (04) 283-290
    CrossrefPubMedGoogle Scholar
  • 106 Piccolo P, Vetrini F, Mithbaokar P. et al. SR-A and SREC-I are Kupffer and endothelial cell receptors for helper-dependent adenoviral vectors. Mol Ther 2013; 21 (04) 767-774
    CrossrefPubMedGoogle Scholar
  • 107 Patten DA, Wilkinson AL, O'Rourke JM, Shetty S. Prognostic value and potential immunoregulatory role of SCARF1 in hepatocellular carcinoma. Front Oncol 2020; 10: 1947
    CrossrefPubMedGoogle Scholar
  • 108 Miyachi Y, Tsuchiya K, Komiya C. et al. Roles for cell-cell adhesion and contact in obesity-induced hepatic myeloid cell accumulation and glucose intolerance. Cell Rep 2017; 18 (11) 2766-2779
    CrossrefPubMedGoogle Scholar
  • 109 Shetty S, Lalor PF, Adams DH. Lymphocyte recruitment to the liver: molecular insights into the pathogenesis of liver injury and hepatitis. Toxicology 2008; 254 (03) 136-146
    CrossrefPubMedGoogle Scholar
  • 110 Furuta K, Guo Q, Pavelko KD. et al. Lipid-induced endothelial vascular cell adhesion molecule 1 promotes nonalcoholic steatohepatitis pathogenesis. J Clin Invest 2021; 131 (06) 143690
    CrossrefPubMedGoogle Scholar
  • 111 Thomas DL. Global elimination of chronic hepatitis. N Engl J Med 2019; 380 (21) 2041-2050
    CrossrefPubMedGoogle Scholar
  • 112 Jefferies M, Rauff B, Rashid H, Lam T, Rafiq S. Update on global epidemiology of viral hepatitis and preventive strategies. World J Clin Cases 2018; 6 (13) 589-599
    CrossrefPubMedGoogle Scholar
  • 113 Ringehan M, McKeating JA, Protzer U. Viral hepatitis and liver cancer. Philos Trans R Soc Lond B Biol Sci 2017; 372 (1732): 20160274
    CrossrefPubMedGoogle Scholar
  • 114 Harvey CE, Post JJ, Palladinetti P. et al. Expression of the chemokine IP-10 (CXCL10) by hepatocytes in chronic hepatitis C virus infection correlates with histological severity and lobular inflammation. J Leukoc Biol 2003; 74 (03) 360-369
    CrossrefPubMedGoogle Scholar
  • 115 Zeremski M, Petrovic LM, Talal AH. The role of chemokines as inflammatory mediators in chronic hepatitis C virus infection. J Viral Hepat 2007; 14 (10) 675-687
    CrossrefPubMedGoogle Scholar
  • 116 Li K, Li NL, Wei D, Pfeffer SR, Fan M, Pfeffer LM. Activation of chemokine and inflammatory cytokine response in hepatitis C virus-infected hepatocytes depends on Toll-like receptor 3 sensing of hepatitis C virus double-stranded RNA intermediates. Hepatology 2012; 55 (03) 666-675
    CrossrefPubMedGoogle Scholar
  • 117 Shen W-J, Azhar S, Kraemer FBSR. SR-B1: a unique multifunctional receptor for cholesterol influx and efflux. Annu Rev Physiol 2018; 80: 95-116
    CrossrefPubMedGoogle Scholar
  • 118 Pileri P, Uematsu Y, Campagnoli S. et al. Binding of hepatitis C virus to CD81. Science 1998; 282 (5390): 938-941
    CrossrefPubMedGoogle Scholar
  • 119 Scarselli E, Ansuini H, Cerino R. et al. The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J 2002; 21 (19) 5017-5025
    CrossrefPubMedGoogle Scholar
  • 120 Evans MJ, von Hahn T, Tscherne DM. et al. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 2007; 446 (7137): 801-805
    CrossrefPubMedGoogle Scholar
  • 121 Ploss A, Evans MJ, Gaysinskaya VA. et al. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 2009; 457 (7231): 882-886
    CrossrefPubMedGoogle Scholar
  • 122 Bartosch B, Vitelli A, Granier C. et al. Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J Biol Chem 2003; 278 (43) 41624-41630
    CrossrefPubMedGoogle Scholar
  • 123 Westhaus S, Deest M, Nguyen ATX. et al. Scavenger receptor class B member 1 (SCARB1) variants modulate hepatitis C virus replication cycle and viral load. J Hepatol 2017; 67 (02) 237-245
    CrossrefPubMedGoogle Scholar
  • 124 Hsu C-S, Hsu S-J, Liu W-L, Chen D-S, Kao J-H. Association of SCARB1 gene polymorphisms with virological response in chronic hepatitis C patients receiving pegylated interferon plus ribavirin therapy. Sci Rep 2016; 6 (01) 32303
    CrossrefPubMedGoogle Scholar
  • 125 Sadeghi S, Davari M, Asli E. et al. Effect of IL15 rs10833 and SCARB1 rs10846744 on virologic responses in chronic hepatitis C patients treated with pegylated interferon-α and ribavirin. Gene 2017; 630: 28-34
    CrossrefPubMedGoogle Scholar
  • 126 Sulkowski MS, Kang M, Matining R. et al; AIDS Clinical Trials Group A5277 Protocol Team. Safety and antiviral activity of the HCV entry inhibitor ITX5061 in treatment-naive HCV-infected adults: a randomized, double-blind, phase 1b study. J Infect Dis 2014; 209 (05) 658-667
    CrossrefPubMedGoogle Scholar
  • 127 Rowe IA, Tully DC, Armstrong MJ. et al. Effect of scavenger receptor class B type I antagonist ITX5061 in patients with hepatitis C virus infection undergoing liver transplantation. Liver Transpl 2016; 22 (03) 287-297
    CrossrefPubMedGoogle Scholar
  • 128 Bataller R, Brenner DA. Liver fibrosis. J Clin Invest 2005; 115 (02) 209-218
    CrossrefPubMedGoogle Scholar
  • 129 Higashi T, Friedman SL, Hoshida Y. Hepatic stellate cells as key target in liver fibrosis. Adv Drug Deliv Rev 2017; 121: 27-42
    CrossrefPubMedGoogle Scholar
  • 130 Schneiderhan W, Schmid-Kotsas A, Zhao J. et al. Oxidized low-density lipoproteins bind to the scavenger receptor, CD36, of hepatic stellate cells and stimulate extracellular matrix synthesis. Hepatology 2001; 34 (4, Pt 1): 729-737
    CrossrefPubMedGoogle Scholar
  • 131 Kang Q, Chen A. Curcumin eliminates oxidized LDL roles in activating hepatic stellate cells by suppressing gene expression of lectin-like oxidized LDL receptor-1. Lab Invest 2009; 89 (11) 1275-1290
    CrossrefPubMedGoogle Scholar
  • 132 Gieseler RK, Marquitan G, Schlattjan M. et al. Hepatocyte apoptotic bodies encasing nonstructural HCV proteins amplify hepatic stellate cell activation: implications for chronic hepatitis C. J Viral Hepat 2011; 18 (11) 760-767
    CrossrefPubMedGoogle Scholar
  • 133 Schattenberg JM, Lazarus JV, Newsome PN. et al. Disease burden and economic impact of diagnosed non-alcoholic steatohepatitis in five European countries in 2018: a cost-of-illness analysis. Liver Int 2021; 41 (06) 1227-1242
    CrossrefPubMedGoogle Scholar
  • 134 Govaere O, Martinez-Lopez N, Petersen SK. et al. Macrophage scavenger receptor 1 mediates lipid-induced inflammation in non-alcoholic fatty liver disease. bioRxiv 2020; DOI: 10.1101/2020.02.01.930115.
    CrossrefPubMedGoogle Scholar
  • 135 Qiu Y, Liu S, Chen H-T. et al. Upregulation of caveolin-1 and SR-B1 in mice with non-alcoholic fatty liver disease. Hepatobiliary Pancreat Dis Int 2013; 12 (06) 630-636
    CrossrefPubMedGoogle Scholar
  • 136 Hoekstra M, Ouweneel AB, Price J. et al. SR-BI deficiency disassociates obesity from hepatic steatosis and glucose intolerance development in high fat diet-fed mice. J Nutr Biochem 2021; 89: 108564
    CrossrefPubMedGoogle Scholar
  • 137 Rada P, González-Rodríguez Á, García-Monzón C, Valverde ÁM. Understanding lipotoxicity in NAFLD pathogenesis: is CD36 a key driver?. Cell Death Dis 2020; 11 (09) 802
    CrossrefPubMedGoogle Scholar
  • 138 Chabowski A, Żendzian-Piotrowska M, Konstantynowicz K. et al. Fatty acid transporters involved in the palmitate and oleate induced insulin resistance in primary rat hepatocytes. Acta Physiol (Oxf) 2013; 207 (02) 346-357
    CrossrefPubMedGoogle Scholar
  • 139 Li Y, Yang P, Zhao L. et al. CD36 plays a negative role in the regulation of lipophagy in hepatocytes through an AMPK-dependent pathway. J Lipid Res 2019; 60 (04) 844-855
    CrossrefPubMedGoogle Scholar
  • 140 Strauss O, Phillips A, Ruggiero K, Bartlett A, Dunbar PR. Immunofluorescence identifies distinct subsets of endothelial cells in the human liver. Sci Rep 2017; 7 (01) 44356
    CrossrefPubMedGoogle Scholar
  • 141 Kawanishi N, Mizokami T, Yada K, Suzuki K. Exercise training suppresses scavenger receptor CD36 expression in kupffer cells of nonalcoholic steatohepatitis model mice. Physiol Rep 2018; 6 (23) e13902
    CrossrefPubMedGoogle Scholar
  • 142 Niu B, He K, Li P. et al. SIRT1 upregulation protects against liver injury induced by a HFD through inhibiting CD36 and the NF‑κB pathway in mouse Kupffer cells. Mol Med Rep 2018; 18 (02) 1609-1615
    PubMedGoogle Scholar
  • 143 Couturier J, Nuotio-Antar AM, Agarwal N. et al. Lymphocytes upregulate CD36 in adipose tissue and liver. Adipocyte 2019; 8 (01) 154-163
    CrossrefPubMedGoogle Scholar
  • 144 Miquilena-Colina ME, Lima-Cabello E, Sánchez-Campos S. et al. Hepatic fatty acid translocase CD36 upregulation is associated with insulin resistance, hyperinsulinaemia and increased steatosis in non-alcoholic steatohepatitis and chronic hepatitis C. Gut 2011; 60 (10) 1394-1402
    CrossrefPubMedGoogle Scholar
  • 145 Sheedfar F, Sung MM, Aparicio-Vergara M. et al. Increased hepatic CD36 expression with age is associated with enhanced susceptibility to nonalcoholic fatty liver disease. Aging (Albany NY) 2014; 6 (04) 281-295
    CrossrefPubMedGoogle Scholar
  • 146 Zhang P, Ge Z, Wang H. et al. Prolactin improves hepatic steatosis via CD36 pathway. J Hepatol 2018; 68 (06) 1247-1255
    CrossrefPubMedGoogle Scholar
  • 147 Koonen DP, Jacobs RL, Febbraio M. et al. Increased hepatic CD36 expression contributes to dyslipidemia associated with diet-induced obesity. Diabetes 2007; 56 (12) 2863-2871
    CrossrefPubMedGoogle Scholar
  • 148 Wilson CG, Tran JL, Erion DM, Vera NB, Febbraio M, Weiss EJ. Hepatocyte-specific disruption of CD36 attenuates fatty liver and improves insulin sensitivity in HFD-fed mice. Endocrinology 2016; 157 (02) 570-585
    CrossrefPubMedGoogle Scholar
  • 149 Handberg A, Højlund K, Gastaldelli A. et al; RISC Investigators. Plasma sCD36 is associated with markers of atherosclerosis, insulin resistance and fatty liver in a nondiabetic healthy population. J Intern Med 2012; 271 (03) 294-304
    CrossrefPubMedGoogle Scholar
  • 150 Heebøll S, Poulsen MK, Ornstrup MJ. et al. Circulating sCD36 levels in patients with non-alcoholic fatty liver disease and controls. Int J Obes 2017; 41 (02) 262-267
    CrossrefPubMedGoogle Scholar
  • 151 Ma C, Han M, Heinrich B. et al. Gut microbiome-mediated bile acid metabolism regulates liver cancer via NKT cells. Science 2018; 360 (6391): eaan5931
    CrossrefPubMedGoogle Scholar
  • 152 Karikoski M, Marttila-Ichihara F, Elima K. et al. Clever-1/stabilin-1 controls cancer growth and metastasis. Clin Cancer Res 2014; 20 (24) 6452-6464
    CrossrefPubMedGoogle Scholar
  • 153 O'Rourke JM, Patten DA, Shetty S. Tumour-associated macrophages in hepatocellular carcinoma: pressing the metabolic switch to prevent T cell responses. J Hepatol 2019; 71 (02) 243-245
    CrossrefPubMedGoogle Scholar
  • 154 Yeung OWH, Lo C-M, Ling C-C. et al. Alternatively activated (M2) macrophages promote tumour growth and invasiveness in hepatocellular carcinoma. J Hepatol 2015; 62 (03) 607-616
    CrossrefPubMedGoogle Scholar
  • 155 Kuang D-M, Zhao Q, Peng C. et al. Activated monocytes in peritumoral stroma of hepatocellular carcinoma foster immune privilege and disease progression through PD-L1. J Exp Med 2009; 206 (06) 1327-1337
    CrossrefPubMedGoogle Scholar
  • 156 Biswas SK, Gangi L, Paul S. et al. A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3/STAT1 activation). Blood 2006; 107 (05) 2112-2122
    CrossrefPubMedGoogle Scholar
  • 157 Gordon S, Martinez FO. Alternative activation of macrophages: mechanism and functions. Immunity 2010; 32 (05) 593-604
    CrossrefPubMedGoogle Scholar
  • 158 Dong P, Ma L, Liu L. et al. CD86+/CD206+, diametrically polarized tumor-associated macrophages, predict hepatocellular carcinoma patient prognosis. Int J Mol Sci 2016; 17 (03) 320
    CrossrefPubMedGoogle Scholar
  • 159 Ren C-X, Leng R-X, Fan Y-G. et al. Intratumoral and peritumoral expression of CD68 and CD206 in hepatocellular carcinoma and their prognostic value. Oncol Rep 2017; 38 (02) 886-898
    CrossrefPubMedGoogle Scholar
  • 160 Sica A, Saccani A, Bottazzi B. et al. Autocrine production of IL-10 mediates defective IL-12 production and NF-κ B activation in tumor-associated macrophages. J Immunol 2000; 164 (02) 762-767
    CrossrefPubMedGoogle Scholar
  • 161 Monti P, Leone BE, Zerbi A. et al. Tumor-derived MUC1 mucins interact with differentiating monocytes and induce IL-10highIL-12low regulatory dendritic cell. J Immunol 2004; 172 (12) 7341-7349
    CrossrefPubMedGoogle Scholar
  • 162 Jaynes JM, Sable R, Ronzetti M. et al. Mannose receptor (CD206) activation in tumor-associated macrophages enhances adaptive and innate antitumor immune responses. Sci Transl Med 2020; 12 (530) eaax6337
    CrossrefPubMedGoogle Scholar
  • 163 Edin S, Wikberg ML, Dahlin AM. et al. The distribution of macrophages with a M1 or M2 phenotype in relation to prognosis and the molecular characteristics of colorectal cancer. PLoS One 2012; 7 (10) e47045
    CrossrefPubMedGoogle Scholar
  • 164 Fujimura T, Kambayashi Y, Furudate S, Kakizaki A, Aiba S. Immunomodulatory effect of bisphosphonate risedronate sodium on CD163+ arginase 1+ M2 macrophages: the development of a possible supportive therapy for angiosarcoma. Clin Dev Immunol 2013; 2013: 325412
    CrossrefPubMedGoogle Scholar
  • 165 Komohara Y, Niino D, Saito Y. et al. Clinical significance of CD163+ tumor-associated macrophages in patients with adult T-cell leukemia/lymphoma. Cancer Sci 2013; 104 (07) 945-951
    CrossrefPubMedGoogle Scholar
  • 166 Tiainen S, Tumelius R, Rilla K. et al. High numbers of macrophages, especially M2-like (CD163-positive), correlate with hyaluronan accumulation and poor outcome in breast cancer. Histopathology 2015; 66 (06) 873-883
    CrossrefPubMedGoogle Scholar
  • 167 Kristiansen M, Graversen JH, Jacobsen C. et al. Identification of the haemoglobin scavenger receptor. Nature 2001; 409 (6817): 198-201
    CrossrefPubMedGoogle Scholar
  • 168 Schaer DJ, Alayash AI, Buehler PW. Gating the radical hemoglobin to macrophages: the anti-inflammatory role of CD163, a scavenger receptor. Antioxid Redox Signal 2007; 9 (07) 991-999
    CrossrefPubMedGoogle Scholar
  • 169 Philippidis P, Mason JC, Evans BJ. et al. Hemoglobin scavenger receptor CD163 mediates interleukin-10 release and heme oxygenase-1 synthesis: antiinflammatory monocyte-macrophage responses in vitro, in resolving skin blisters in vivo, and after cardiopulmonary bypass surgery. Circ Res 2004; 94 (01) 119-126
    CrossrefPubMedGoogle Scholar
  • 170 Sierra-Filardi E, Vega MA, Sánchez-Mateos P, Corbí AL, Puig-Kröger A. Heme oxygenase-1 expression in M-CSF-polarized M2 macrophages contributes to LPS-induced IL-10 release. Immunobiology 2010; 215 (9-10): 788-795
    CrossrefPubMedGoogle Scholar
  • 171 Weis N, Weigert A, von Knethen A, Brüne B. Heme oxygenase-1 contributes to an alternative macrophage activation profile induced by apoptotic cell supernatants. Mol Biol Cell 2009; 20 (05) 1280-1288
    CrossrefPubMedGoogle Scholar
  • 172 Bover LC, Cardó-Vila M, Kuniyasu A. et al. A previously unrecognized protein-protein interaction between TWEAK and CD163: potential biological implications. J Immunol 2007; 178 (12) 8183-8194
    CrossrefPubMedGoogle Scholar
  • 173 Motomura T, Shirabe K, Mano Y. et al. Neutrophil-lymphocyte ratio reflects hepatocellular carcinoma recurrence after liver transplantation via inflammatory microenvironment. J Hepatol 2013; 58 (01) 58-64
    CrossrefPubMedGoogle Scholar
  • 174 Riabov V, Yin S, Song B. et al. Stabilin-1 is expressed in human breast cancer and supports tumor growth in mammary adenocarcinoma mouse model. Oncotarget 2016; 7 (21) 31097-31110
    CrossrefPubMedGoogle Scholar
  • 175 Hollmén M, Figueiredo CR, Jalkanen S. New tools to prevent cancer growth and spread: a ‘Clever’ approach. Br J Cancer 2020; 123 (04) 501-509
    CrossrefPubMedGoogle Scholar
  • 176 Virtakoivu R, Rannikko J, Viitala M. et al. Systemic blockade of Clever-1 elicits lymphocyte activation alongside checkpoint molecule downregulation in patients with solid tumors: Results from a Phase I/II Clinical Trial. Clin Cancer Res 2021; ; June:OF1–OF16. DOI: 10.1158/1078-0432.CCR-20-4862.
    CrossrefPubMedGoogle Scholar
  • 177 Seifert L, Deutsch M, Alothman S. et al. Dectin-1 regulates hepatic fibrosis and hepatocarcinogenesis by suppressing TLR4 signaling pathways. Cell Rep 2015; 13 (09) 1909-1921
    CrossrefPubMedGoogle Scholar
  • 178 Liu M, Luo F, Ding C. et al. Dectin-1 activation by a natural product β-glucan converts immunosuppressive macrophages into an M1-like phenotype. J Immunol 2015; 195 (10) 5055-5065
    CrossrefPubMedGoogle Scholar
  • 179 Chiba S, Ikushima H, Ueki H. et al. Recognition of tumor cells by Dectin-1 orchestrates innate immune cells for anti-tumor responses. eLife 2014; 3: e04177
    CrossrefPubMedGoogle Scholar
  • 180 Mattiola I, Tomay F, De Pizzol M. et al. The macrophage tetraspan MS4A4A enhances dectin-1-dependent NK cell-mediated resistance to metastasis. Nat Immunol 2019; 20 (08) 1012-1022
    CrossrefPubMedGoogle Scholar
  • 181 Shi B, Abrams M, Sepp-Lorenzino L. Expression of asialoglycoprotein receptor 1 in human hepatocellular carcinoma. J Histochem Cytochem 2013; 61 (12) 901-909
    CrossrefPubMedGoogle Scholar
  • 182 Witzigmann D, Quagliata L, Schenk SH, Quintavalle C, Terracciano LM, Huwyler J. Variable asialoglycoprotein receptor 1 expression in liver disease: Implications for therapeutic intervention. Hepatol Res 2016; 46 (07) 686-696
    CrossrefPubMedGoogle Scholar
  • 183 Steirer LM, Park EI, Townsend RR, Baenziger JU. The asialoglycoprotein receptor regulates levels of plasma glycoproteins terminating with sialic acid α2,6-galactose. J Biol Chem 2009; 284 (06) 3777-3783
    CrossrefPubMedGoogle Scholar
  • 184 Park EI, Mi Y, Unverzagt C, Gabius H-J, Baenziger JU. The asialoglycoprotein receptor clears glycoconjugates terminating with sialic acid α 2,6GalNAc. Proc Natl Acad Sci U S A 2005; 102 (47) 17125-17129
    CrossrefPubMedGoogle Scholar
  • 185 Gu D, Jin H, Jin G. et al. The asialoglycoprotein receptor suppresses the metastasis of hepatocellular carcinoma via LASS2-mediated inhibition of V-ATPase activity. Cancer Lett 2016; 379 (01) 107-116
    CrossrefPubMedGoogle Scholar
  • 186 Xiao Y, Chen B, Yang K. et al. Down-regulation of MARCO associates with tumor progression in hepatocellular carcinoma. Exp Cell Res 2019; 383 (02) 111542
    CrossrefPubMedGoogle Scholar
  • 187 Beattie L, Sawtell A, Mann J. et al. Bone marrow-derived and resident liver macrophages display unique transcriptomic signatures but similar biological functions. J Hepatol 2016; 65 (04) 758-768
    CrossrefPubMedGoogle Scholar
  • 188 Sun H, Song J, Weng C. et al. Association of decreased expression of the macrophage scavenger receptor MARCO with tumor progression and poor prognosis in human hepatocellular carcinoma. J Gastroenterol Hepatol 2017; 32 (05) 1107-1114
    CrossrefPubMedGoogle Scholar
  • 189 Stephen SL, Freestone K, Dunn S. et al. Scavenger receptors and their potential as therapeutic targets in the treatment of cardiovascular disease. Int J Hypertens 2010; 2010: 646929-646929
    CrossrefPubMedGoogle Scholar
  • 190 Vasquez M, Simões I, Consuegra-Fernández M, Aranda F, Lozano F, Berraondo P. Exploiting scavenger receptors in cancer immunotherapy: lessons from CD5 and SR-B1. Eur J Immunol 2017; 47 (07) 1108-1118
    CrossrefPubMedGoogle Scholar
  • 191 Enciu AM, Radu E, Popescu ID, Hinescu ME, Ceafalan LC. Targeting CD36 as biomarker for metastasis prognostic: how far from translation into clinical practice?. BioMed Res Int 2018; 2018: 7801202
    CrossrefPubMedGoogle Scholar
  • 192 Aizarani N, Saviano A, Sagar. Mailly L, Durand S, Herman JS, Pessaux P, Baumert TF, Grün D. A human liver cell atlas reveals heterogeneity and epithelial progenitors. Nature 2019; 572 (7768): 199-204
    CrossrefPubMedGoogle Scholar
  • 193 Ramachandran P, Dobie R, Wilson-Kanamori JR. et al. Resolving the fibrotic niche of human liver cirrhosis at single-cell level. Nature 2019; 575 (7783): 512-518
    CrossrefPubMedGoogle Scholar
  • 194 Dobie R, Wilson-Kanamori JR, Henderson BEP. et al. Single-cell transcriptomics uncovers zonation of function in the mesenchyme during liver fibrosis. Cell Rep 2019; 29 (07) 1832.e8-1847.e8
    CrossrefPubMedGoogle Scholar
  • 195 Wang H, Thorling CA, Liang X. et al. Diagnostic imaging and therapeutic application of nanoparticles targeting the liver. J Mater Chem B Mater Biol Med 2015; 3 (06) 939-958
    CrossrefPubMedGoogle Scholar
  • 196 Hayashi Y, Takamiya M, Jensen PB. et al. Differential nanoparticle sequestration by macrophages and scavenger endothelial cells visualized in vivo in real-time and at ultrastructural resolution. ACS Nano 2020; 14 (02) 1665-1681
    CrossrefPubMedGoogle Scholar
  • 197 Allen RJ, Mathew B, Rice KG. PEG-peptide inhibition of scavenger receptor uptake of nanoparticles by the liver. Mol Pharm 2018; 15 (09) 3881-3891
    CrossrefPubMedGoogle Scholar
  • 198 Campbell F, Bos FL, Sieber S. et al. Directing nanoparticle biodistribution through evasion and exploitation of Stab2-dependent nanoparticle uptake. ACS Nano 2018; 12 (03) 2138-2150
    CrossrefPubMedGoogle Scholar
  • 199 Arias-Alpizar G, Koch B, Hamelmann NM. et al. Stabilin-1 is required for the endothelial clearance of small anionic nanoparticles. Nanomedicine (Lond) 2021; 34: 102395
    CrossrefPubMedGoogle Scholar
  • 200 Miller CM, Donner AJ, Blank EE. et al. Stabilin-1 and Stabilin-2 are specific receptors for the cellular internalization of phosphorothioate-modified antisense oligonucleotides (ASOs) in the liver. Nucleic Acids Res 2016; 44 (06) 2782-2794
    CrossrefPubMedGoogle Scholar
  • 201 Gökirmak T, Nikan M, Wiechmann S, Prakash TP, Tanowitz M, Seth PP. Overcoming the challenges of tissue delivery for oligonucleotide therapeutics. Trends Pharmacol Sci 2021; 42 (07) 588-604
    CrossrefPubMedGoogle Scholar
  • 202 Willoughby JLS, Chan A, Sehgal A. et al. Evaluation of GalNAc-siRNA conjugate activity in pre-clinical animal models with reduced asialoglycoprotein receptor expression. Mol Ther 2018; 26 (01) 105-114
    CrossrefPubMedGoogle Scholar
  • 203 Graversen JH, Svendsen P, Dagnæs-Hansen F. et al. Targeting the hemoglobin scavenger receptor CD163 in macrophages highly increases the anti-inflammatory potency of dexamethasone. Mol Ther 2012; 20 (08) 1550-1558
    CrossrefPubMedGoogle Scholar
  • 204 Svendsen P, Graversen JH, Etzerodt A. et al. Antibody-directed glucocorticoid targeting to CD163 in M2-type macrophages attenuates fructose-induced liver inflammatory changes. Mol Ther Methods Clin Dev 2016; 4: 50-61
    CrossrefPubMedGoogle Scholar
  • 205 Etzerodt A, Tsalkitzi K, Maniecki M. et al. Specific targeting of CD163+ TAMs mobilizes inflammatory monocytes and promotes T cell-mediated tumor regression. J Exp Med 2019; 216 (10) 2394-2411
    CrossrefPubMedGoogle Scholar
  • 206 Pellicoro A, Ramachandran P, Iredale JP, Fallowfield JA. Liver fibrosis and repair: immune regulation of wound healing in a solid organ. Nat Rev Immunol 2014; 14 (03) 181-194
    CrossrefPubMedGoogle Scholar