Mechanisms of immunomodulation by mammalian and viral decoy receptors: Insights from structures

Nature Reviews Immunology

Volumn 17, Issue 2, 2017, Pages 112-129

  Felix, Jan ^a,b,c   Savvides, Savvas N ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c INSTITUT DE BIOLOGIE STRUCTURALE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CHEMOKINE RECEPTOR; CYTOKINE RECEPTOR; DOUBLE STRANDED DNA; HUMAN DECOY RECEPTOR; INTERLEUKIN 1; MAMMALIAN DECOY RECEPTOR; MEMBRANE DECOY RECEPTOR; MEMBRANE RECEPTOR; UNCLASSIFIED DRUG; VIRAL DECOY RECEPTOR;

ENZYME MECHANISM; GENOME; GENOME ANALYSIS; HERPESVIRIDAE; HOST; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; IMMUNITY; IMMUNOMODULATION; INFLAMMATION; MAMMAL; MOLECULAR BIOLOGY; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; ANIMAL; IMMUNE EVASION; IMMUNOLOGY; VIRUS;

ANIMALS; HUMANS; IMMUNE EVASION; MAMMALS; RECEPTORS, CYTOKINE; VIRUSES;

EID: 85007506070     PISSN: 14741733     EISSN: 14741741     Source Type: Journal    
DOI: 10.1038/nri.2016.134     Document Type: Review

References (206)

1. Schulz O., Hammerschmidt S. I., Moschovakis G. L., & Forster R. Chemokines and chemokine receptors in lymphoid tissue dynamics. Annu. Rev. Immunol. 34, 203-242 (2016
2. Schwartz D. M., Bonelli M., Gadina M., & O'Shea J. J. Type I/II cytokines, JAKs, and new strategies for treating autoimmune diseases. Nat. Rev. Rheumatol. 12, 25-36 (2016
3. Lemmon M. A., & Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 141, 1117-1134 (2010
4. Heaney M. L., & Golde D. W. Soluble cytokine receptors. Blood 87, 847-857 (1996
5. Colotta F., et al. Interleukin 1 type II receptor: a decoy target for IL 1 that is regulated by IL 4. Science 261, 472-475 (1993
6. Afonina I. S., Muller C., Martin S. J., & Beyaert R. Proteolytic processing of interleukin 1 family cytokines: variations on a common theme. Immunity 42, 991-1004 (2015
7. Colotta F., Dower S. K., Sims J. E., & Mantovani A. The type II 'decoy' receptor: a novel regulatory pathway for interleukin 1. Immunol. Today 15, 562-566 (1994
8. Mantovani A., Locati M., Vecchi A., Sozzani S., & Allavena P. Decoy receptors: a strategy to regulate inflammatory cytokines and chemokines. Trends Immunol. 22, 328-336 (2001
9. McMahan C. J., et al. A novel IL 1 receptor, cloned from B cells by mammalian expression, is expressed in many cell types. EMBO J. 10, 2821-2832 1991
10. Arend W. P., et al. Binding of IL 1 alpha, IL 1 beta, and IL 1 receptor antagonist by soluble IL 1 receptors and levels of soluble IL 1 receptors in synovial fluids. J. Immunol. 153, 4766-4774 (1994
11. Greenfeder S. A., et al. Molecular cloning and characterization of a second subunit of the interleukin 1 receptor complex. J. Biol. Chem. 270, 13757-13765 (1995
12. Garlanda C., Dinarello C. A., & Mantovani A. The interleukin 1 family: back to the future. Immunity 39, 1003-1018 (2013
13. Orlando S., et al. Role of metalloproteases in the release of the IL 1 type II decoy receptor. J. Biol. Chem. 272, 31764-31769 (1997
14. Liu C., et al. Cloning and characterization of an alternatively processed human type II interleukin 1 receptor mRNA. J. Biol. Chem. 271, 20965-20972 (1996
15. Zheng Y., Humphry M., Maguire J. J., Bennett M. R., & Clarke M. C. Intracellular interleukin 1 receptor 2 binding prevents cleavage and activity of interleukin 1α, controlling necrosis-induced sterile inflammation. Immunity 38, 285-295 (2013
16. Smith D. E., et al. The soluble form of IL 1 receptor accessory protein enhances the ability of soluble type II IL 1 receptor to inhibit IL 1 action. Immunity 18, 87-96 (2003
17. Thomas C., Bazan J. F., & Garcia K. C. Structure of the activating IL 1 receptor signaling complex. Nat. Struct. Mol. Biol. 19, 455-457 (2012
18. Wang D., et al. Structural insights into the assembly and activation of IL 1β with its receptors. Nat. Immunol. 11, 905-911 (2010
19. Weber S., & Saftig P. Ectodomain shedding and ADAMs in development. Development 139, 3693-3709 (2012
20. Scheller J., Chalaris A., Garbers C., & Rose-John S. ADAM17: a molecular switch to control inflammation and tissue regeneration. Trends Immunol. 32, 380-387 (2011
21. Elkon R., Ugalde A. P., & Agami R. Alternative cleavage and polyadenylation: extent, regulation and function. Nat. Rev. Genet. 14, 496-506 (2013
22. Thomas C. P., Andrews J. I., & Liu K. Z. Intronic polyadenylation signal sequences and alternate splicing generate human soluble Flt1 variants and regulate the abundance of soluble Flt1 in the placenta. FASEB J. 21, 3885-3895 (2007
23. Vorlova S., et al. Induction of antagonistic soluble decoy receptor tyrosine kinases by intronic polyA activation. Mol. Cell 43, 927-939 (2011
24. Kakkar R., & Lee R. T. The IL 33/ST2 pathway: therapeutic target and novel biomarker. Nat. Rev. Drug Discov. 7, 827-840 (2008
25. Peschon J. J., et al. An essential role for ectodomain shedding in mammalian development. Science 282, 1281-1284 (1998
26. Mullberg J., et al. A metalloprotease inhibitor blocks shedding of the IL 6 receptor and the p60 TNF receptor. J. Immunol. 155, 5198-5205 1995
27. Muller-Newen G., et al. Soluble IL 6 receptor potentiates the antagonistic activity of soluble gp130 on IL 6 responses. J. Immunol. 161, 6347-6355 (1998
28. Peters M., et al. The function of the soluble interleukin 6 (IL 6) receptor in vivo: sensitization of human soluble IL 6 receptor transgenic mice towards IL 6 and prolongation of the plasma half-life of IL 6. J. Exp. Med. 183, 1399-1406 (1996
29. Scheller J., Chalaris A., Schmidt-Arras D., & Rose-John S. The pro-and anti-inflammatory properties of the cytokine interleukin 6. Biochim. Biophys. Acta 1813, 878-888 (2011
30. Narazaki M., et al. Soluble forms of the interleukin 6 signal-transducing receptor component gp130 in human serum possessing a potential to inhibit signals through membrane-anchored gp130. Blood 82, 1120-1126 (1993
31. Jostock T., et al. Soluble gp130 is the natural inhibitor of soluble interleukin 6 receptor transsignaling responses. Eur. J. Biochem. 268, 160-167 (2001
32. Boulanger M. J., Chow D. C., Brevnova E. E., & Garcia K. C. Hexameric structure and assembly of the interleukin 6/IL 6 α-receptor/gp130 complex. Science 300, 2101-2104 (2003
33. Waldmann T. A. The biology of interleukin 2 and interleukin 15: implications for cancer therapy and vaccine design. Nat. Rev. Immunol. 6, 595-601 (2006
34. Dubois S., Mariner J., Waldmann T. A., & Tagaya Y. IL 15Rα recycles and presents IL 15 in trans to neighboring cells. Immunity 17, 537-547 (2002
35. Ring A. M., et al. Mechanistic and structural insight into the functional dichotomy between IL 2 and IL 15. Nat. Immunol. 13, 1187-1195 (2012
36. Mortier E., Bernard J., Plet A., & Jacques Y. Natural, proteolytic release of a soluble form of human IL 15 receptor α-chain that behaves as a specific, high affinity IL 15 antagonist. J. Immunol. 173, 1681-1688 (2004
37. Bergamaschi C., et al. Circulating IL. 15 exists as heterodimeric complex with soluble IL 15Rα in human and mouse serum. Blood 120, e1-e8 2012
38. Stonier S. W., & Schluns K. S. Trans-presentation: a novel mechanism regulating IL 15 delivery and responses. Immunol. Lett. 127, 85-92 (2010
39. Lundstrom W., et al. Soluble IL7Rα potentiates IL 7 bioactivity and promotes autoimmunity. Proc. Natl Acad. Sci. USA 110, E1761-E1770 2013
40. Hong C., et al. Activated T cells secrete an alternatively spliced form of common γ-chain that inhibits cytokine signaling and exacerbates inflammation. Immunity 40, 910-923 (2014
41. Wang X., Lupardus P., Laporte S. L., & Garcia K. C. Structural biology of shared cytokine receptors. Annu. Rev. Immunol. 27, 29-60 (2009
42. Verstraete K., et al. Structural basis of the proinflammatory signaling complex mediated by TSLP. Nat. Struct. Mol. Biol. 21, 375-382 (2014
43. McElroy C. A., et al. Structural reorganization of the interleukin 7 signaling complex. Proc. Natl Acad. Sci. USA 109, 2503-2508 (2012
44. Adamopoulos I. E., & Mellins E. D. Alternative pathways of osteoclastogenesis in inflammatory arthritis. Nat. Rev. Rheumatol. 11, 189-194 (2015
45. Johnstone R. W., Frew A. J., & Smyth M. J. The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat. Rev. Cancer 8, 782-798 (2008
46. Luan X., et al. Crystal structure of human RANKL complexed with its decoy receptor osteoprotegerin. J. Immunol. 189, 245-252 (2012
47. Nelson C. A., Warren J. T., Wang M. W., Teitelbaum S. L., & Fremont D. H. RANKL employs distinct binding modes to engage RANK and the osteoprotegerin decoy receptor. Structure 20, 1971-1982 (2012
48. Ta H. M., et al. Structure-based development of a receptor activator of nuclear factor-κB ligand (RANKL) inhibitor peptide and molecular basis for osteopetrosis. Proc. Natl Acad. Sci. USA 107, 20281-20286 (2010
49. Liu C., et al. Structural and functional insights of RANKL-RANK interaction and signaling. J. Immunol. 184, 6910-6919 (2010
50. Zhan C., et al. Decoy strategies: the structure of TL1A: DcR3 complex. Structure 19, 162-171 (2011
51. Liu W., et al. Mechanistic basis for functional promiscuity in the TNF and TNF receptor superfamilies: structure of the LIGHT: DcR3 assembly. Structure 22, 1252-1262 (2014
52. Liu W., et al. Crystal structure of the complex of human FasL and its decoy receptor DcR3. Structure 24, 2016-2023 (2016
53. Dumoutier L., Lejeune D., Colau D., & Renauld J. C. Cloning and characterization of IL 22 binding protein, a natural antagonist of IL 10 related T cell-derived inducible factor/IL 22. J. Immunol. 166, 7090-7095 (2001
54. Kotenko S. V., et al. Identification, cloning, and characterization of a novel soluble receptor that binds IL 22 and neutralizes its activity. J. Immunol. 166, 7096-7103 (2001
55. Xu W., et al. A soluble class II cytokine receptor, IL 22RA2, is a naturally occurring IL 22 antagonist. Proc. Natl Acad. Sci. USA 98, 9511-9516 (2001
56. de Moura P. R., et al. Crystal structure of a soluble decoy receptor IL 22BP bound to interleukin 22. FEBS Lett. 583, 1072-1077 (2009
57. Bleicher L., et al. Crystal structure of the IL 22/IL 22R1 complex and its implications for the IL 22 signaling mechanism. FEBS Lett. 582, 2985-2992 (2008
58. Jones B. C., Logsdon N. J., & Walter M. R. Structure of IL 22 bound to its high-affinity IL 22R1 chain. Structure 16, 1333-1344 (2008
59. Bovolenta P., Esteve P., Ruiz J. M., Cisneros E., & Lopez-Rios J. Beyond Wnt inhibition: new functions of secreted Frizzled-related proteins in development and disease. J. Cell Sci. 121, 737-746 (2008
60. Lopez-Rios J., Esteve P., Ruiz J. M., & Bovolenta P. The netrin-related domain of Sfrp1 interacts with Wnt ligands and antagonizes their activity in the anterior neural plate. Neural Dev. 3, 19 (2008
61. Cruciat C. M., & Niehrs C. Secreted and transmembrane wnt inhibitors and activators. Cold Spring Harb. Perspect. Biol. 5, a015081 2013
62. Bafico A., et al. Interaction of Frizzled related protein (FRP) with Wnt ligands and the Frizzled receptor suggests alternative mechanisms for FRP inhibition of Wnt signaling. J. Biol. Chem. 274, 16180-16187 (1999
63. Dann C. E., et al. Insights into Wnt binding and signalling from the structures of two Frizzled cysteine-rich domains. Nature 412, 86-90 (2001
64. Rodriguez J., et al. SFRP1 regulates the growth of retinal ganglion cell axons through the Fz2 receptor. Nat. Neurosci. 8, 1301-1309 (2005
65. Novick D., et al. Interleukin 18 binding protein: a novel modulator of the Th1 cytokine response. Immunity 10, 127-136 (1999
66. Bufler P., et al. A complex of the IL 1 homologue IL 1F7b and IL 18 binding protein reduces IL 18 activity. Proc. Natl Acad. Sci. USA 99, 13723-13728 (2002
67. Kumar S., et al. Interleukin 1F7B (IL 1H4/IL 1F7) is processed by caspase 1 and mature IL 1F7B binds to the IL 18 receptor but does not induce IFN-γ production. Cytokine 18, 61-71 (2002
68. Tsutsumi N., et al. The structural basis for receptor recognition of human interleukin 18. Nat. Commun. 5, 5340 (2014
69. Jenkins M., Keir M., & McCune J. M. A membrane-bound Fas decoy receptor expressed by human thymocytes. J. Biol. Chem. 275, 7988-7993 (2000
70. Pan G., et al. An antagonist decoy receptor and a death domain-containing receptor for TRAIL. Science 277, 815-818 (1997
71. Pan G., Ni J., Yu G., Wei Y. F., & Dixit V. M. TRUNDD, a new member of the TRAIL receptor family that antagonizes TRAIL signalling. FEBS Lett. 424, 41-45 (1998
72. Caput D., et al. Cloning and characterization of a specific interleukin (IL)-13 binding protein structurally related to the IL 5 receptor α chain. J. Biol. Chem. 271, 16921-16926 (1996
73. Donaldson D. D., et al. The murine IL 13 receptor α2: molecular cloning, characterization, and comparison with murine IL 13 receptor α1. J. Immunol. 161, 2317-2324 (1998
74. Chen W., et al. IL 13Rα2 membrane and soluble isoforms differ in humans and mice. J. Immunol. 183, 7870-7876 (2009
75. Hershey G. K. IL 13 receptors and signaling pathways: an evolving web. J. Allergy Clin. Immunol. 111, 677-690 (2003
76. Lupardus P. J., Birnbaum M. E., & Garcia K. C. Molecular basis for shared cytokine recognition revealed in the structure of an unusually high affinity complex between IL 13 and IL 13Rα2. Structure 18, 332-342 (2010
77. LaPorte S. L., et al. Molecular and structural basis of cytokine receptor pleiotropy in the interleukin 4/13 system. Cell 132, 259-272 (2008
78. Meyer R. D., Mohammadi M., & Rahimi N. A single amino acid substitution in the activation loop defines the decoy characteristic of VEGFR 1/FLT 1. J. Biol. Chem. 281, 867-875 (2006
79. Nold-Petry C. A., et al. IL 37 requires the receptors IL 18Rα and IL 1R8 (SIGIRR) to carry out its multifaceted anti-inflammatory program upon innate signal transduction. Nat. Immunol. 16, 354-365 (2015
80. Wald D., et al. SIGIRR, a negative regulator of Toll-like receptor-interleukin 1 receptor signaling. Nat. Immunol. 4, 920-927 (2003
81. Qin J., Qian Y., Yao J., Grace C., & Li X. SIGIRR inhibits interleukin 1 receptor-and Toll-like receptor 4 mediated signaling through different mechanisms. J. Biol. Chem. 280, 25233-25241 (2005
82. Garlanda C., Anders H. J., & Mantovani A. TIR8/SIGIRR: an IL 1R/TLR family member with regulatory functions in inflammation and T cell polarization. Trends Immunol. 30, 439-446 (2009
83. Thomassen E., Renshaw B. R., & Sims J. E. Identification and characterization of SIGIRR, a molecule representing a novel subtype of the IL 1R superfamily. Cytokine 11, 389-399 (1999
84. Griffith J. W., Sokol C. L., & Luster A. D. Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu. Rev. Immunol. 32, 659-702 (2014
85. Burns J. M., et al. A novel chemokine receptor for SDF 1 and I TAC involved in cell survival, cell adhesion, and tumor development. J. Exp. Med. 203, 2201-2213 (2006
86. Nibbs R. J., & Graham G. J. Immune regulation by atypical chemokine receptors. Nat. Rev. Immunol. 13, 815-829 (2013
87. Bachelerie F., et al. International Union of Basic and Clinical Pharmacology. LXXXIX. Update on the extended family of chemokine receptors and introducing a new nomenclature for atypical chemokine receptors. Pharmacol. Rev. 66, 1-79 (2014
88. Luker K. E., Gupta M., Steele J. M., Foerster B. R., & Luker G. D. Imaging ligand-dependent activation of CXCR7. Neoplasia 11, 1022-1035 (2009
89. Borroni E. M., et al. β-Arrestin-dependent activation of the cofilin pathway is required for the scavenging activity of the atypical chemokine receptor D6. Sci. Signal. 6, ra30 2013
90. D'Amico G., et al. Uncoupling of inflammatory chemokine receptors by IL 10: generation of functional decoys. Nat. Immunol. 1, 387-391 (2000
91. Iannello A., et al. Viral strategies for evading antiviral cellular immune responses of the host. J. Leukoc. Biol. 79, 16-35 (2006
92. Speck S. H., & Ganem D. Viral latency and its regulation: lessons from the γ-herpesviruses. Cell Host Microbe 8, 100-115 (2010
93. Duffy S., Shackelton L. A., & Holmes E. C. Rates of evolutionary change in viruses: patterns and determinants. Nat. Rev. Genet. 9, 267-276 (2008
94. Odom M. R., Hendrickson R. C., & Lefkowitz E. J. Poxvirus protein evolution: family wide assessment of possible horizontal gene transfer events. Virus Res. 144, 233-249 (2009
95. Alcami A. Viral mimicry of cytokines, chemokines and their receptors. Nat. Rev. Immunol. 3, 36-50 (2003
96. McFadden G., Lalani A., Everett H., Nash P., & Xu X. Virus-encoded receptors for cytokines and chemokines. Semin. Cell Dev. Biol. 9, 359-368 (1998
97. Smith C. A., et al. A receptor for tumor necrosis factor defines an unusual family of cellular and viral proteins. Science 248 1019-1023 1990
98. Smith C. A., et al. T2 open reading frame from the Shope fibroma virus encodes a soluble form of the TNF receptor. Biochem. Biophys. Res. Commun. 176, 335-342 (1991
99. Alcami A., & Smith G. L. A soluble receptor for interleukin 1β encoded by vaccinia virus: a novel mechanism of virus modulation of the host response to infection. Cell 71, 153-167 1992
100. Spriggs M. K., et al. Vaccinia and cowpox viruses encode a novel secreted interleukin 1 binding protein. Cell 71, 145-152 (1992
101. Upton C., Mossman K., & McFadden G. Encoding of a homolog of the IFN-gamma receptor by myxoma virus. Science 258, 1369-1372 (1992
102. Alcami A., & Smith G. L. Vaccinia, cowpox, and camelpox viruses encode soluble gamma interferon receptors with novel broad species specificity. J. Virol. 69, 4633-4639 (1995
103. Hu F. Q., Smith C. A., & Pickup D. J. Cowpox virus contains two copies of an early gene encoding a soluble secreted form of the type II TNF receptor. Virology 204, 343-356 (1994
104. Smith C. A., et al. Cowpox virus genome encodes a second soluble homologue of cellular TNF receptors, distinct from CrmB, that binds TNF but not LTα. Virology 223, 132-147 (1996
105. Loparev V. N., et al. A third distinct tumor necrosis factor receptor of orthopoxviruses. Proc. Natl Acad. Sci. USA 95, 3786-3791 (1998
106. Saraiva M., & Alcami A. CrmE, a novel soluble tumor necrosis factor receptor encoded by poxviruses. J. Virol. 75, 226-233 (2001
107. Alejo A., et al. A chemokine-binding domain in the tumor necrosis factor receptor from variola (smallpox) virus. Proc. Natl Acad. Sci. USA 103, 5995-6000 (2006
108. Graham S. C., et al. Structure of CrmE, a virus-encoded tumour necrosis factor receptor. J. Mol. Biol. 372, 660-671 (2007
109. Naismith J. H., Devine T. Q., Kohno T., & Sprang S. R. Structures of the extracellular domain of the type I tumor necrosis factor receptor. Structure 4, 1251-1262 (1996
110. Banner D. W., et al. Crystal structure of the soluble human 55 kd TNF receptor-human TNFβ complex: implications for TNF receptor activation. Cell 73, 431-445 (1993
111. Pontejo S. M., Alejo A., & Alcami A. Comparative biochemical and functional analysis of viral and human secreted tumor necrosis factor (TNF) decoy receptors. J. Biol. Chem. 290, 15973-15984 (2015
112. Panus J. F., et al. Cowpox virus encodes a fifth member of the tumor necrosis factor receptor family: a soluble, secreted CD30 homologue. Proc. Natl Acad. Sci. USA 99, 8348-8353 (2002
113. Saraiva M., Smith P., Fallon P. G., & Alcami A. Inhibition of type 1 cytokine-mediated inflammation by a soluble CD30 homologue encoded by ectromelia (mousepox) virus. J. Exp. Med. 196, 829-839 (2002
114. Kennedy M. K., Willis C. R., & Armitage R. J. Deciphering CD30 ligand biology and its role in humoral immunity. Immunology 118, 143-152 (2006
115. Xiang Y., & Moss B. IL 18 binding and inhibition of interferon γ induction by human poxvirus-encoded proteins. Proc. Natl Acad. Sci. USA 96, 11537-11542 (1999
116. Smith V. P., Bryant N. A., & Alcami A. Ectromelia, vaccinia and cowpox viruses encode secreted interleukin 18 binding proteins. J. Gen. Virol. 81, 1223-1230 (2000
117. Born T. L., et al. A poxvirus protein that binds to and inactivates IL 18, and inhibits NK cell response. J. Immunol. 164, 3246-3254 2000
118. Krumm B., Meng X., Wang Z., Xiang Y., & Deng J. A unique bivalent binding and inhibition mechanism by the yatapoxvirus interleukin 18 binding protein. PLoS Pathog. 8, e1002876 2012
119. Krumm B., Meng X., Li Y., Xiang Y., & Deng J. Structural basis for antagonism of human interleukin 18 by poxvirus interleukin 18 binding protein. Proc. Natl Acad. Sci. USA 105, 20711-20715 (2008
120. Maussang D., Bongers G., Lira S. A., & Smit M. J. in Chemokine Receptors as Drug Targets (eds Smit M. J., Lira S. A., & Leurs R.) 177-205 (Wiley-VCH Verlag GmbH, & Co. KGaA, 2010
121. Kledal T. N., Rosenkilde M. M., & Schwartz T. W. Selective recognition of the membrane-bound CX3C chemokine, fractalkine, by the human cytomegalovirus-encoded broad-spectrum receptor US28. FEBS Lett. 441, 209-214 (1998
122. Burg J. S., et al. Structural basis for chemokine recognition and activation of a viral G protein-coupled receptor. Science 347, 1113-1117 (2015
123. Venkatakrishnan A. J., et al. Molecular signatures of G protein-coupled receptors. Nature 494, 185-194 (2013
124. Rovati G. E., Capra V., & Neubig R. R. The highly conserved DRY motif of class A G protein-coupled receptors: beyond the ground state. Mol. Pharmacol. 71, 959-964 (2007
125. Nomiyama H., & Yoshie O. Functional roles of evolutionary conserved motifs and residues in vertebrate chemokine receptors. J. Leukoc. Biol. 97, 39-47 (2015
126. Rasmussen S. G., et al. Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 477, 549-555 (2011
127. Mossman K., Upton C., Buller R. M., & McFadden G. Species specificity of ectromelia virus and vaccinia virus interferon-γ binding proteins. Virology 208, 762-769 (1995
128. McNab F., Mayer-Barber K., Sher A., Wack A., & O'Garra A. Type I interferons in infectious disease. Nat. Rev. Immunol. 15, 87-103 (2015
129. Sakala I. G., et al. Poxvirus-encoded gamma interferon binding protein dampens the host immune response to infection. J. Virol. 81, 3346-3353 (2007
130. Nuara A. A., Bai H., Chen N., Buller R. M., & Walter M. R. The unique C termini of orthopoxvirus gamma interferon binding proteins are essential for ligand binding. J. Virol. 80, 10675-10682 (2006
131. Symons J. A., Alcami A., & Smith G. L. Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. Cell 81, 551-560 (1995
132. Alcami A., Symons J. A., & Smith G. L. The vaccinia virus soluble alpha/beta interferon (IFN) receptor binds to the cell surface and protects cells from the antiviral effects of IFN. J. Virol. 74, 11230-11239 (2000
133. Montanuy I., Alejo A., & Alcami A. Glycosaminoglycans mediate retention of the poxvirus type I interferon binding protein at the cell surface to locally block interferon antiviral responses. FASEB J. 25, 1960-1971 (2011
134. Nuara A. A., et al. Structure and mechanism of IFN γ antagonism by an orthopoxvirus IFN γ binding protein. Proc. Natl Acad. Sci. USA 105, 1861-1866 (2008
135. Lee C. A. Structural basis of type I interferon sequestration by a poxvirus decoy receptor. Washington PhD thesis, Washington Univ. (2011
136. Thiel D. J., et al. Observation of an unexpected third receptor molecule in the crystal structure of human interferon-γ receptor complex. Structure 8, 927-936 (2000
137. Thomas C., et al. Structural linkage between ligand discrimination and receptor activation by type I interferons. Cell 146, 621-632 (2011
138. Brunetti C. R., et al. A secreted high-affinity inhibitor of human TNF from tanapox virus. Proc. Natl Acad. Sci. USA 100, 4831-4836 (2003
139. Rahman M. M., et al. Interaction of human TNF and β2 microglobulin with tanapox virus-encoded TNF inhibitor, TPV 2L. Virology 386, 462-468 (2009
140. Yang Z., West A. P., & Bjorkman P. J. Crystal structure of TNFα complexed with a poxvirus MHC-related TNF binding protein. Nat. Struct. Mol. Biol. 16, 1189-1191 (2009
141. Strockbine L. D., et al. The Epstein-Barr virus BARF1 gene encodes a novel, soluble colony-stimulating factor 1 receptor. J. Virol. 72, 4015-4021 (1998
142. Stanley E. R., & Chitu V. CSF 1 receptor signaling in myeloid cells. Cold Spring Harb. Perspect. Biol. 6, a021857 2014
143. Tarbouriech N., Ruggiero F., de Turenne-Tessier M., Ooka T., & Burmeister W. P. Structure of the Epstein-Barr virus oncogene BARF1. J. Mol. Biol. 359, 667-678 (2006
144. Elegheert J., et al. Allosteric competitive inactivation of hematopoietic CSF 1 signaling by the viral decoy receptor BARF1. Nat. Struct. Mol. Biol. 19, 938-947 (2012
145. Felix J., et al. Structure and assembly mechanism of the signaling complex mediated by human CSF 1. Structure 23, 1621-1631 (2015
146. Lucas A., & McFadden G. Secreted immunomodulatory viral proteins as novel biotherapeutics. J. Immunol. 173, 4765-4774 (2004
147. Wang D., Bresnahan W., & Shenk T. Human cytomegalovirus encodes a highly specific RANTES decoy receptor. Proc. Natl Acad. Sci. USA 101, 16642-16647 (2004
148. Lubman O. Y., et al. Rodent herpesvirus Peru encodes a secreted chemokine decoy receptor. J. Virol. 88, 538-546 (2014
149. Lubman O. Y., & Fremont D. H. Parallel evolution of chemokine binding by structurally related herpesvirus decoy receptors. Structure 24, 57-69 (2016
150. Parry C. M., et al. A broad spectrum secreted chemokine binding protein encoded by a herpesvirus. J. Exp. Med. 191, 573-578 (2000
151. Van Berkel V., et al. Identification of a gammaherpesvirus selective chemokine binding protein that inhibits chemokine action. J. Virol. 74, 6741-6747 (2000
152. Webb L. M., Smith V. P., & Alcami A. The gammaherpesvirus chemokine binding protein can inhibit the interaction of chemokines with glycosaminoglycans. FASEB J. 18, 571-573 (2004
153. Alexander J. M., et al. Structural basis of chemokine sequestration by a herpesvirus decoy receptor. Cell 111, 343-356 (2002
154. Alexander-Brett J. M., & Fremont D. H. Dual GPCR and GAG mimicry by the M3 chemokine decoy receptor. J. Exp. Med. 204, 3157-3172 (2007
155. Nelson C. A., Epperson M. L., Singh S., Elliott J. I., & Fremont D. H. Structural conservation and functional diversity of the poxvirus immune evasion (PIE) domain superfamily. Viruses 7, 4878-4898 (2015
156. Bahar M. W., et al. Structure and function of A41, a vaccinia virus chemokine binding protein. PLoS Pathog. 4, e5 2008
157. Arnold P. L., & Fremont D. H. Structural determinants of chemokine binding by an ectromelia virus-encoded decoy receptor. J. Virol. 80, 7439-7449 (2006
158. Carfi A., Smith C. A., Smolak P. J., McGrew J., & Wiley D. C. Structure of a soluble secreted chemokine inhibitor vCCI (p35) from cowpox virus. Proc. Natl Acad. Sci. USA 96, 12379-12383 (1999
159. Zhang L., et al. Solution structure of the complex between poxvirus-encoded CC chemokine inhibitor vCCI and human MIP 1β. Proc. Natl Acad. Sci. USA 103, 13985-13990 (2006
160. Counago R. M., et al. Structures of orf virus chemokine binding protein in complex with host chemokines reveal clues to broad binding specificity. Structure 23, 1199-1213 (2015
161. Xue X., et al. Structural basis of chemokine sequestration by CrmD, a poxvirus-encoded tumor necrosis factor receptor. PLoS Pathog. 7, e1002162 2011
162. McCoy W. H. IV, Wang X., Yokoyama W. M., Hansen T. H., & Fremont D. H. Structural mechanism of ER retrieval of MHC class I by cowpox. PLoS Biol. 10, e1001432 2012
163. Deane D., et al. Orf virus encodes a novel secreted protein inhibitor of granulocyte-macrophage colony-stimulating factor and interleukin 2. J. Virol. 74, 1313-1320 (2000
164. Felix J., et al. Structural basis of GM CSF and IL 2 sequestration by the viral decoy receptor GIF. Nat. Commun. 7, 13228 (2016
165. Fernandez-Botran R., Crespo F. A., & Sun X. Soluble cytokine receptors in biological therapy. Expert Opin. Biol. Ther. 2, 585-605 (2002
166. Czajkowsky D. M., Hu J., Shao Z., & Pleass R. J. Fc fusion proteins: new developments and future perspectives. EMBO Mol. Med. 4, 1015-1028 (2012
167. Levin D., Golding B., Strome S. E., & Sauna Z. E. Fc fusion as a platform technology: potential for modulating immunogenicity. Trends Biotechnol. 33, 27-34 (2015
168. Economides A. N., et al. Cytokine traps: multi-component, high-affinity blockers of cytokine action. Nat. Med. 9, 47-52 (2003
169. Holash J., et al. VEGF-Trap: a VEGF blocker with potent antitumor effects. Proc. Natl Acad. Sci. USA 99, 11393-11398 (2002
170. Braun H., Afonina I., Mueller C., & Beyaert R 2: generation and characterization of IL 33 cytokine traps as anti-cytokine blockers. Cytokine 70, 28 2014
171. Yin H., et al. Adenovirus-mediated overexpression of soluble ST2 provides a protective effect on lipopolysaccharide-induced acute lung injury in mice. Clin. Exp. Immunol. 164, 248-255 (2011
172. Ding Y., Qin L., Kotenko S. V., Pestka S., & Bromberg J. S. A single amino acid determines the immunostimulatory activity of interleukin 10. J. Exp. Med. 191, 213-224 (2000
173. Fallon P G., & Alcami A. Pathogen-derived immunomodulatory molecules: future immunotherapeutics? Trends Immunol. 27, 470-476 2006
174. DeBruyne L. A., Li K., Bishop D. K., & Bromberg J. S. Gene transfer of virally encoded chemokine antagonists vMIP II and MC148 prolongs cardiac allograft survival and inhibits donor-specific immunity. Gene Ther. 7, 575-582 (2000
175. Liu L., et al. The viral anti-inflammatory chemokine-binding protein M-T7 reduces intimal hyperplasia after vascular injury. J. Clin. Invest. 105, 1613-1621 (2000
176. Dabbagh K., et al. Local blockade of allergic airway hyperreactivity and inflammation by the poxvirus-derived pan CC chemokine inhibitor vCCI. J. Immunol. 165, 3418-3422 (2000
177. Pyo R., et al. Inhibition of intimal hyperplasia in transgenic mice conditionally expressing the chemokine-binding protein M3. Am. J. Pathol. 164, 2289-2297 (2004
178. Viejo-Borbolla A., et al. Attenuation of TNF-driven murine ileitis by intestinal expression of the viral immunomodulator CrmD. Mucosal Immunol. 3, 633-644 (2010
179. Lucas A., et al. The serpin saga; development of a new class of virus derived anti-inflammatory protein immunotherapeutics. Adv. Exp. Med. Biol. 666, 132-156 (2009
180. Zheng D., et al. Virus-derived anti-inflammatory proteins: potential therapeutics for cancer. Trends Mol. Med. 18, 304-310 (2012
181. Lucas A., et al. Transplant vasculopathy: viral anti-inflammatory serpin regulation of atherogenesis. J. Heart Lung Transplant. 19, 1029-1038 (2000
182. Liu L., et al. Comparative analysis of plaque growth after arterial stent implant with anti-inflammatory chemokine and serine protease inhibitors treatment. J. Clin. Exp. Cardiol. 4, 274 (2013
183. Dai E., et al. Inhibition of chemokine-glycosaminoglycan interactions in donor tissue reduces mouse allograft vasculopathy and transplant rejection. PLoS ONE 5, e10510 2010
184. Levin A. M., et al. Exploiting a natural conformational switch to engineer an interleukin 2 'superkine'. Nature 484, 529-533 (2012
185. Mitra S., et al. Interleukin 2 activity can be fine tuned with engineered receptor signaling clamps. Immunity 42, 826-838 (2015
186. Moraga I., et al. Instructive roles for cytokine-receptor binding parameters in determining signaling and functional potency. Sci. Signal. 8, ra114 2015
187. Spangler J. B., Moraga I., Mendoza J. L., & Garcia K. C. Insights into cytokine-receptor interactions from cytokine engineering. Annu. Rev. Immunol. 33, 139-167 (2015
188. Skrlec K., Strukelj B., & Berlec A. Non-immunoglobulin scaffolds: a focus on their targets. Trends Biotechnol. 33, 408-418 (2015
189. Desmet J., et al. Structural basis of IL 23 antagonism by an Alphabody protein scaffold. Nat. Commun. 5, 5237 (2014
190. Xu Y., et al. Crystal structure of the entire ectodomain of gp130: insights into the molecular assembly of the tall cytokine receptor complexes. J. Biol. Chem. 285, 21214-21218 (2010
191. McElroy C. A., Dohm J. A., & Walsh S. T. Structural and biophysical studies of the human IL 7/IL 7Rα complex. Structure 17, 54-65 (2009
192. Leppnen V. M., et al. Structural determinants of growth factor binding and specificity by VEGF receptor 2. Proc. Natl Acad. Sci. USA 107, 2425-2430 (2010
193. Liu X., et al. Structural insights into the interaction of IL 33 with its receptors. Proc. Natl Acad. Sci. USA 110, 14918-14923 (2013
194. Cheng J., et al. Protection from Fas-mediated apoptosis by a soluble form of the Fas molecule. Science 263, 1759-1762 (1994
195. Wiesmann C., et al. Crystal structure at 1.7 ? resolution of VEGF in complex with domain 2 of the Flt 1 receptor. Cell 91, 695-704 (1997
196. Yoon S. I., Jones B. C., Logsdon N. J., & Walter M. R. Same structure, different function crystal structure of the Epstein-Barr virus IL 10 bound to the soluble IL 10R1 chain. Structure 13, 551-564 (2005
197. Jones B. C., et al. Crystal structure of human cytomegalovirus IL 10 bound to soluble human IL 10R1. Proc. Natl Acad. Sci. USA 99, 9404-9409 (2002
198. Kotenko S. V., Saccani S., Izotova L. S., Mirochnitchenko O. V., & Pestka S. Human cytomegalovirus harbors its own unique IL 10 homolog (cmvIL 10). Proc. Natl Acad. Sci. USA 97, 1695-1700 (2000
199. Wise L., McCaughan C., Tan C. K., Mercer A. A., & Fleming S. B. Orf virus interleukin 10 inhibits cytokine synthesis in activated human THP 1 monocytes, but only partially impairs their proliferation. J. Gen. Virol. 88, 1677-1682 (2007
200. Fleming S. B., et al. Sequence and functional analysis of a homolog of interleukin 10 encoded by the parapoxvirus orf virus. Virus Genes 21, 85-95 (2000
201. Chow D., He X., Snow A. L., Rose-John S., & Garcia K. C. Structure of an extracellular gp130 cytokine receptor signaling complex. Science 291, 2150-2155 (2001
202. Liu H., et al. Structural basis of semaphorin-plexin recognition and viral mimicry from Sema7A and A39R complexes with plexinC1. Cell 142, 749-761 (2010
203. Pieren M., et al. Crystal structure of the Orf virus NZ2 variant of vascular endothelial growth factor E: implications for receptor specificity. J. Biol. Chem. 281, 19578-19587 (2006
204. Qin L., et al. Crystal structure of the chemokine receptor CXCR4 in complex with a viral chemokine. Science 347, 1117-1122 (2015
205. Lalani A. S., et al. The purified myxoma virus gamma interferon receptor homolog M-T7 interacts with the heparin-binding domains of chemokines. J. Virol. 71, 4356-4363 (1997
206. Bryant N. A., Davis-Poynter N., Vanderplasschen A., & Alcami A. Glycoprotein G isoforms from some alphaherpesviruses function as broad-spectrum chemokine binding proteins. EMBO J. 22, 833-846 (2003