Neonatal Fc receptor expression in macrophages is indispensable for IgG homeostasis

References

• Epelman S, Lavine KJ, Randolph GJ. Origin and functions of tissue macrophages. Immunity. 2014;41(1):21–35. doi:10.1016/j.immuni.2014.06.013.
   PubMed Web of Science ®Google Scholar
• Lavin Y, Mortha A, Rahman A, Merad M. Regulation of macrophage development and function in peripheral tissues. Nat Rev Immunol. 2015;15(12):731–44. doi:10.1038/nri3920.
   PubMed Web of Science ®Google Scholar
• Roberts AW, Lee BL, Deguine J, John S, Shlomchik MJ, Barton GM. Tissue-resident macrophages are locally programmed for silent clearance of apoptotic cells. Immunity. 2017;47(5):913–27. doi:10.1016/j.immuni.2017.10.006.
   PubMed Web of Science ®Google Scholar
• Iwasaki A, Medzhitov R. Control of adaptive immunity by the innate immune system. Nat Immunol. 2015;16(4):343–53. doi:10.1038/ni.3123.
   PubMed Web of Science ®Google Scholar
• Lim JP, Gleeson PA. Macropinocytosis: an endocytic pathway for internalising large gulps. Immunol Cell Biol. 2011;89(8):836–43. doi:10.1038/icb.2011.20.
   PubMed Web of Science ®Google Scholar
• Steinman RM, Brodie SE, Cohn ZA. Membrane flow during pinocytosis. A stereologic analysis. J Cell Biol. 1976;68:665–87.
   PubMed Web of Science ®Google Scholar
• Abrass CK. Measurement of the rates of basal pinocytosis of horseradish peroxidase and internalization of heat-aggregated IgG by macrophages from normal and streptozotocin-induced diabetic rats. Immunology. 1988;65:411–15.
   PubMed Web of Science ®Google Scholar
• Lee SH, Starkey PM, Gordon S. Quantitative analysis of total macrophage content in adult mouse tissues. Immunochemical studies with monoclonal antibody F4/80. J Exp Med. 1985;161:475–89.
   PubMed Web of Science ®Google Scholar
• Yu YR, O‘Koren EG, Hotten DF, Kan MJ, Kopin D, Nelson ER, Que L, Gunn MD. A protocol for the comprehensive flow cytometric analysis of immune cells in normal and inflamed murine non-lymphoid tissues. PLoS One. 2016;11(3):e0150606. doi:10.1371/journal.pone.0150606.
   PubMed Web of Science ®Google Scholar
• Challa DK, Velmurugan R, Ober RJ, Ward ES. FcRn: from molecular interactions to regulation of IgG pharmacokinetics and functions. Curr Top Microbiol Immunol. 2014;382:249–72. doi:10.1007/978-3-319-07911-0_12.
   PubMed Web of Science ®Google Scholar
• Pyzik M, Rath T, Lencer WI, Baker K, Blumberg RS. FcRn: the architect behind the immune and nonimmune functions of IgG and albumin. J Immunol. 2015;194(10):4595–603. doi:10.4049/jimmunol.1403014.
   PubMed Web of Science ®Google Scholar
• Ober RJ, Martinez C, Lai X, Zhou J, Ward ES. Exocytosis of IgG as mediated by the receptor, FcRn: an analysis at the single-molecule level. Proc Natl Acad Sci USA. 2004;101:11076–81. doi:10.1073/pnas.0402970101.
   PubMed Web of Science ®Google Scholar
• Ober RJ, Martinez C, Vaccaro C, Zhou J, Ward ES. Visualizing the site and dynamics of IgG salvage by the MHC class I-related receptor, FcRn. J Immunol. 2004;172:2021–29.
   PubMed Web of Science ®Google Scholar
• Claypool SM, Dickinson BL, Wagner JS, Johansen FE, Venu N, Borawski JA, Lencer WI, Blumberg RS. Bidirectional transepithelial IgG transport by a strongly polarized basolateral membrane Fcγ-receptor. Mol Biol Cell. 2004;15:1746–59. doi:10.1091/mbc.e03-11-0832.
   PubMed Web of Science ®Google Scholar
• Raghavan M, Gastinel LN, Bjorkman PJ. The class I major histocompatibility complex related Fc receptor shows pH-dependent stability differences correlating with immunoglobulin binding and release. Biochemistry. 1993;32:8654–60.
   PubMed Web of Science ®Google Scholar
• Kim JK, Tsen MF, Ghetie V, Ward ES. Localization of the site of the murine IgG1 molecule that is involved in binding to the murine intestinal Fc receptor. Eur J Immunol. 1994;24(10):2429–34. doi:10.1002/eji.1830241025.
   PubMed Web of Science ®Google Scholar
• Zhu X, Meng G, Dickinson BL, Li X, Mizoguchi E, Miao L, Wang Y, Robert C, Wu B, Smith PD, et al. MHC class I-related neonatal Fc receptor for IgG is functionally expressed in monocytes, intestinal macrophages, and dendritic cells. J Immunol. 2001;166:3266–76.
   PubMed Web of Science ®Google Scholar
• Akilesh S, Christianson GJ, Roopenian DC, Shaw AS. Neonatal FcR expression in bone marrow-derived cells functions to protect serum IgG from catabolism. J Immunol. 2007;179:4580–88.
   PubMed Web of Science ®Google Scholar
• Perez-Montoyo H, Vaccaro C, Hafner M, Ober RJ, Mueller W, Ward ES. Conditional deletion of the MHC Class I-related receptor, FcRn, reveals the sites of IgG homeostasis in mice. Proc Natl Acad Sci USA. 2009;106(8):2788–93. doi:10.1073/pnas.0810796106.
   PubMed Web of Science ®Google Scholar
• Kobayashi K, Qiao SW, Yoshida M, Baker K, Lencer WI, Blumberg RS. An FcRn-dependent role for anti-flagellin immunoglobulin G in pathogenesis of colitis in mice. Gastroenterology. 2009;137(5):1746–56. doi:10.1053/j.gastro.2009.07.059.
   PubMed Web of Science ®Google Scholar
• Rath T, Baker K, Dumont JA, Peters RT, Jiang H, Qiao SW, Lencer WI, Pierce GF, Blumberg RS. Fc-fusion proteins and FcRn: structural insights for longer-lasting and more effective therapeutics. Crit Rev Biotechnol. 2013;35(2):235–54. doi:10.3109/07388551.2013.834293.
   PubMed Web of Science ®Google Scholar
• Qiao SW, Kobayashi K, Johansen FE, Sollid LM, Andersen JT, Milford E, Roopenian DC, Lencer WI, Blumberg RS. Dependence of antibody-mediated presentation of antigen on FcRn. Proc Natl Acad Sci USA. 2008;105(27):9337–42. doi:10.1073/pnas.0801717105.
   PubMed Web of Science ®Google Scholar
• Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, Prinz M, Wu B, Jacobsen SE, Pollard JW, et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science. 2012;336(6077):86–90. doi:10.1126/science.1219179.
   PubMed Web of Science ®Google Scholar
• Gomez Perdiguero E, Klapproth K, Schulz C, Busch K, Azzoni E, Crozet L, Garner H, Trouillet C, de Bruijn MF, Geissmann F, et al. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature. 2015;518(7540):547–51. doi:10.1038/nature13989.
   PubMed Web of Science ®Google Scholar
• Sheng J, Ruedl C, Karjalainen K. Most tissue-resident macrophages except microglia are derived from fetal hematopoietic stem cells. Immunity. 2015;43(2):382–93. doi:10.1016/j.immuni.2015.07.016.
   PubMed Web of Science ®Google Scholar
• Van Rooijen N, Sanders A. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods. 1994;174:83–93.
   PubMed Web of Science ®Google Scholar
• Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory Fc receptors modulate in vivo cytoxicity against tumor targets. Nat Med. 2000;6(4):443–46. doi:10.1038/74704.
   PubMed Web of Science ®Google Scholar
• Baudino L, Shinohara Y, Nimmerjahn F, Furukawa J, Nakata M, Martinez-Soria E, Petry F, Ravetch JV, Nishimura S, Izui S. Crucial role of aspartic acid at position 265 in the CH2 domain for murine IgG2a and IgG2b Fc-associated effector functions. J Immunol. 2008;181:6664–69.
   PubMed Web of Science ®Google Scholar
• Roopenian DC, Christianson GJ, Sproule TJ, Brown AC, Akilesh S, Jung N, Petkova S, Avanessian L, Choi EY, Shaffer DJ, et al. The MHC class I-like IgG receptor controls perinatal IgG transport, IgG homeostasis, and fate of IgG-Fc-coupled drugs. J Immunol. 2003;170(7):3528–33.
   PubMed Web of Science ®Google Scholar
• Gu H, Marth JD, Orban PC, Mossmann H, Rajewsky K. Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting. Science. 1994;265:103–06.
   PubMed Web of Science ®Google Scholar
• Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 1999;8:265–77.
   PubMed Web of Science ®Google Scholar
• Caton ML, Smith-Raska MR, Reizis B. Notch-RBP-J signaling controls the homeostasis of CD8− dendritic cells in the spleen. J Exp Med. 2007;204(7):1653–64. doi:10.1084/jem.20062648.
   PubMed Web of Science ®Google Scholar
• Rickert RC, Roes J, Rajewsky K. B lymphocyte-specific, Cre-mediated mutagenesis in mice. Nucleic Acids Res. 1997;25:1317–18.
   PubMed Web of Science ®Google Scholar
• Kano A, Wolfgang MJ, Gao Q, Jacoby J, Chai GX, Hansen W, Iwamoto Y, Pober JS, Flavell RA, Fu XY. Endothelial cells require STAT3 for protection against endotoxin-induced inflammation. J Exp Med. 2003;198(10):1517–25. doi:10.1084/jem.20030077.
   PubMed Web of Science ®Google Scholar
• Vaccaro C, Zhou J, Ober RJ, Ward ES. Engineering the Fc region of immunoglobulin G to modulate in vivo antibody levels. Nat Biotechnol. 2005;23(10):1283–88. doi:10.1038/nbt1143.
   PubMed Web of Science ®Google Scholar
• Firan M, Bawdon R, Radu C, Ober RJ, Eaken D, Antohe F, Ghetie V, Ward ES. The MHC class I related receptor, FcRn, plays an essential role in the maternofetal transfer of gammaglobulin in humans. Int Immunol. 2001;13:993–1002.
   PubMed Web of Science ®Google Scholar
• Ades EW, Candal FJ, Swerlick RA, George VG, Summers S, Bosse DC, Lawley TJ. HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol. 1992;99:683–90.
   PubMed Web of Science ®Google Scholar
• Zhou J, Mateos F, Ober RJ, Ward ES. Conferring the binding properties of the mouse MHC class I-related receptor, FcRn, onto the human ortholog by sequential rounds of site-directed mutagenesis. J Mol Biol. 2005;345(5):1071–81. doi:10.1016/j.jmb.2004.11.014.
   PubMed Web of Science ®Google Scholar
• Abram CL, Roberge GL, Hu Y, Lowell CA. Comparative analysis of the efficiency and specificity of myeloid-Cre deleting strains using ROSA-EYFP reporter mice. J Immunol Methods. 2014;408:89–100. doi:10.1016/j.jim.2014.05.009.
   PubMed Web of Science ®Google Scholar
• Chaudhury C, Mehnaz S, Robinson JM, Hayton WL, Pearl DK, Roopenian DC, Anderson CL. The major histocompatibility complex-related Fc receptor for IgG (FcRn) binds albumin and prolongs its lifespan. J Exp Med. 2003;197:315–22.
   PubMed Web of Science ®Google Scholar
• Kim J, Bronson CL, Hayton WL, Radmacher MD, Roopenian DC, Robinson JM, Anderson CL. Albumin turnover: FcRn-mediated recycling saves as much albumin from degradation as the liver produces. Am J Physiol Gastrointest Liver Physiol. 2006;290(2):G352–G360. doi:10.1152/ajpgi.00286.2005.
   PubMed Web of Science ®Google Scholar
• Carter PJ, Lazar GA. Next generation antibody drugs: pursuit of the ‘high-hanging fruit‘. Nat Rev Drug Discov. 2018;17(3):197–223. doi:10.1038/nrd.2017.227.
   PubMed Web of Science ®Google Scholar
• Jenkins SJ, Ruckerl D, Cook PC, Jones LH, Finkelman FD, van Rooijen N, MacDonald AS, Allen JE. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science. 2011;332(6035):1284–88. doi:10.1126/science.1204351.
   PubMed Web of Science ®Google Scholar
• Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest. 2003;112(12):1796–808. doi:10.1172/JCI19246.
   PubMed Web of Science ®Google Scholar
• Ghanta S, Cuzzone DA, Torrisi JS, Albano NJ, Joseph WJ, Savetsky IL, Gardenier JC, Chang D, Zampell JC, Mehrara BJ. Regulation of inflammation and fibrosis by macrophages in lymphedema. Am J Physiol Heart Circ Physiol. 2015;308(9):H1065–H1077. doi:10.1152/ajpheart.00598.2014.
   PubMed Web of Science ®Google Scholar
• Schmidt-Supprian M, Rajewsky K. Vagaries of conditional gene targeting. Nat Immunol. 2007;8(7):665–68. doi:10.1038/ni0707-665.
   PubMed Web of Science ®Google Scholar
• Weissleder R, Nahrendorf M, Pittet MJ. Imaging macrophages with nanoparticles. Nat Mater. 2014;13(2):125–38. doi:10.1038/nmat3780.
   PubMed Web of Science ®Google Scholar
• Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, Figueiredo JL, Kohler RH, Chudnovskiy A, Waterman P, et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science. 2009;325(5940):612–16. doi:10.1126/science.1175202.
   PubMed Web of Science ®Google Scholar
• Liu L, Garcia AM, Santoro H, Zhang Y, McDonnell K, Dumont J, Bitonti A. Amelioration of experimental autoimmune myasthenia gravis in rats by neonatal FcR blockade. J Immunol. 2007;178:5390–98.
   PubMed Web of Science ®Google Scholar
• Patel DA, Puig-Canto A, Challa DK, Perez Montoyo H, Ober RJ, Ward ES. Neonatal Fc receptor blockade by Fc engineering ameliorates arthritis in a murine model. J Immunol. 2011;187(2):1015–22. doi:10.4049/jimmunol.1003780.
   PubMed Web of Science ®Google Scholar
• Challa DK, Bussmeyer U, Khan T, Montoyo HP, Bansal P, Ober RJ, Ward ES. Autoantibody depletion ameliorates disease in murine experimental autoimmune encephalomyelitis. MAbs. 2013;5(5):655–59. doi:10.4161/mabs.25439.
   PubMed Web of Science ®Google Scholar
• Kiessling P, Lledo-Garcia R, Watanabe S, Langdon G, Tran D, Bari M, Christodoulou L, Jones E, Price G, Smith B, et al. The FcRn inhibitor rozanolixizumab reduces human serum IgG concentration: A randomized phase 1 study. Sci Transl Med. 2017;9(414):1208. doi:10.1126/scitranslmed.aan1208.
   Web of Science ®Google Scholar
• Ulrichts P, Guglietta A, Dreier T, van Bragt T, Hanssens V, Hofman E, Vankerckhoven B, Verheesen P, Ongenae N, Lykhopiy V, et al. Neonatal Fc receptor antagonist efgartigimod safely and sustainably reduces IgGs in humans. J Clin Invest. 2018;128(10):4372–86. doi:10.1172/JCI97911.
   PubMed Web of Science ®Google Scholar
• Ling L, Hillson JL, Tiessen RG, Bosje T, van Iersel MP, Nix DJ, Markowitz L, Cilfone NA, Duffner J, Streisand J, et al. M281, an anti-FcRn antibody: pharmacodynamics, pharmacokinetics, and safety across the full range of IgG reduction in a first-in-human study. Clin Pharmacol Ther. 2018. doi:10.1002/cpt.1276.
   Google Scholar
• Baker K, Rath T, Pyzik M, Blumberg RS. The role of FcRn in antigen presentation. Front Immunol. 2014;5:408. doi:10.3389/fimmu.2014.00408.
   PubMed Web of Science ®Google Scholar
• Baker K, Qiao SW, Kuo TT, Aveson VG, Platzer B, Andersen JT, Sandlie I, Chen Z, de Haar C, Lencer WI, et al. Neonatal Fc receptor for IgG (FcRn) regulates cross-presentation of IgG immune complexes by CD8−CD11b+ dendritic cells. Proc Natl Acad Sci USA. 2011;108(24):9927–32. doi:10.1073/pnas.1019037108.
   PubMed Web of Science ®Google Scholar
• Baker K, Rath T, Flak MB, Arthur JC, Chen Z, Glickman JN, Zlobec I, Karamitopoulou E, Stachler MD, Odze RD, et al. Neonatal Fc receptor expression in dendritic cells mediates protective immunity against colorectal cancer. Immunity. 2013;39(6):1095–107. doi:10.1016/j.immuni.2013.11.003.
   PubMed Web of Science ®Google Scholar
• Foote J, Winter G. Antibody framework residues affecting the conformation of the hypervariable loops. J Mol Biol. 1992;224:487–99.
   PubMed Web of Science ®Google Scholar
• Amit AG, Mariuzza RA, Phillips SE, Poljak RJ. Three-dimensional structure of an antigen-antibody complex at 2.8 Å resolution. Science. 1986;233:747–53.
   PubMed Web of Science ®Google Scholar
• Gan Z, Ram S, Vaccaro C, Ober RJ, Ward ES. Analyses of the recycling receptor, FcRn, in live cells reveal novel pathways for lysosomal delivery. Traffic. 2009;10(5):600–14. doi:10.1111/j.1600-0854.2009.00887.x.
   PubMed Web of Science ®Google Scholar
• Marelli-Berg FM, Peek E, Lidington EA, Stauss HJ, Lechler RI. Isolation of endothelial cells from murine tissue. J Immunol Methods. 2000;244:205–15.
   PubMed Web of Science ®Google Scholar
• Chao J, Ward ES, Ober RJ. A software framework for the analysis of complex microscopy image data. IEEE Trans Inf Technol Biomed. 2010;14(4):1075–87. doi:10.1109/TITB.2010.2049024.
   PubMedGoogle Scholar