Characterization of the rabbit neonatal Fc receptor (FcRn) and analyzing the immunophenotype of the transgenic rabbits that overexpresses FcRn

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Catunda Lemos, Ana Paula ^a   Cervenak, Judit ^b   Bender, Balázs ^b   Hoffmann, Orsolya Ivett ^a   Baranyi, Mária ^b   Kerekes, Andrea ^a   Farkas, Anita ^c   Bosze, Zsuzsanna ^a   Hiripi, László ^a   Kacskovics, Imre ^b,c  

^a SZENT ISTVÁN UNIVERSITY   (Hungary)

^b ImmunoGenes Kft ^*  (Hungary)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; FC RECEPTOR; IMMUNOGLOBULIN G; FC RECEPTOR, NEONATAL; HLA ANTIGEN CLASS 1; MESSENGER RNA;

AMNION; ANIMAL CELL; ANTIBODY PRODUCTION; ARTICLE; CONTROLLED STUDY; COPY NUMBER VARIATION; FETUS; GENOMIC FRAGMENT; HEMIZYGOSITY; HOMOZYGOSITY; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOPHENOTYPING; MOLECULAR CLONING; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RABBIT; RECEPTOR BINDING; SEQUENCE ALIGNMENT; TRANSGENICS; TROPHOBLAST; YOLK SAC; AMINO ACID SEQUENCE; ANIMAL; CATTLE; CHICKEN; ENZYME IMMUNOASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PLACENTA; PREGNANCY; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; TRANSGENIC ANIMAL; WESTERN BLOTTING;

MUS; MUS MUSCULUS; ORYCTOLAGUS CUNICULUS;

AMINO ACID SEQUENCE; AMNION; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOTTING, WESTERN; CATTLE; CHICKENS; CLONING, MOLECULAR; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; IMMUNOENZYME TECHNIQUES; IMMUNOGLOBULIN G; IMMUNOPHENOTYPING; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLACENTA; PREGNANCY; RABBITS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, FC; RECEPTORS, IGG; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; YOLK SAC;

EID: 84855654982     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028869     Document Type: Article

References (72)

1. Brambell FWR, Halliday R, Morris IG, (1958) Interference by human and bovine serum and serum protein fractions with the absorption of antibodies by suckling rats and mice. Proc R Soc B 149: 1.
2. Brambell FWR, Hemmings WA, Morris IG, (1964) A theoretical model of gammaglobulin catabolism. Nature 203: 1352-1355.
3. Spiegelberg HL, Weigle WO, (1965) The Catabolism of Homologous and Heterologous 7s Gamma Globulin Fragments. J Exp Med 121: 323-338.
4. Kraehenbuhl JP, Campiche MA, (1969) Early stages of intestinal absorption of specific antibiodies in the newborn. An ultrastructural, cytochemical, and immunological study in the pig, rat, and rabbit. J Cell Biol 42: 345-365.
5. Butler JE, (1971) Transmission of immunity from mother to young. In: Hasegawa T, Hayashi M, Ebling FJG, Henderson IW, editors. Fertility and Sterility Amsterdam Excerpta Medica pp. 92-98.
6. Jones EA, Waldmann TA, (1972) The mechanism of intestinal uptake and transcellular transport of IgG in the neonatal rat. J Clin Invest 51: 2916-2927.
7. Rodewald R, Kraehenbuhl JP, (1984) Receptor-mediated transport of IgG. J Cell Biol 99: 159s-164s.
8. Simister NE, Rees AR, (1985) Isolation and characterization of an Fc receptor from neonatal rat small intestine. Eur J Immunol 15: 733-738.
9. Simister NE, Mostov KE, (1989) An Fc receptor structurally related to MHC class I antigens. Nature 337: 184-187.
10. Ward ES, Ober RJ, (2009) Chapter 4: Multitasking by exploitation of intracellular transport functions the many faces of FcRn. Adv Immunol 103: 77-115.
11. Borvak J, Richardson J, Medesan C, Antohe F, Radu C, et al. (1998) Functional expression of the MHC class I-related receptor, FcRn, in endothelial cells of mice. Int Immunol 10: 1289-1298.
12. Akilesh S, Christianson GJ, Roopenian DC, Shaw AS, (2007) Neonatal FcR Expression in Bone Marrow-Derived Cells Functions to Protect Serum IgG from Catabolism. J Immunol 179: 4580-4588.
13. Montoyo HP, Vaccaro C, Hafner M, Ober RJ, Mueller W, et al. (2009) Conditional deletion of the MHC class I-related receptor FcRn reveals the sites of IgG homeostasis in mice. Proc Natl Acad Sci U S A 106: 2788-2793.
14. Lu W, Zhao Z, Zhao Y, Yu S, Zhao Y, et al. (2007) Over-expression of the bovine FcRn in the mammary gland results in increased IgG levels in both milk and serum of transgenic mice. Immunology 122: 401-408.
15. Vidarsson G, Stemerding AM, Stapleton NM, Spliethoff SE, Janssen H, et al. (2006) FcRn: an IgG receptor on phagocytes with a novel role in phagocytosis. Blood 108: 3573-3579.
16. Qiao SW, Kobayashi K, Johansen FE, Sollid LM, Andersen JT, et al. (2008) Dependence of antibody-mediated presentation of antigen on FcRn. Proc Natl Acad Sci U S A 105: 9337-9342.
17. Mi W, Wanjie S, Lo ST, Gan Z, Pickl-Herk B, et al. (2008) Targeting the neonatal fc receptor for antigen delivery using engineered fc fragments. J Immunol 181: 7550-7561.
18. Liu X, Lu L, Yang Z, Palaniyandi S, Zeng R, et al. (2011) The Neonatal FcR-Mediated Presentation of Immune-Complexed Antigen Is Associated with Endosomal and Phagosomal pH and Antigen Stability in Macrophages and Dendritic Cells. J Immunol 186: 4674-4686.
19. Baker K, Qiao SW, Kuo TT, Aveson VG, Platzer B, et al. (2011) Neonatal Fc receptor for IgG (FcRn) regulates cross-presentation of IgG immune complexes by CD8-CD11b+ dendritic cells. Proceedings of the National Academy of Sciences of the United States of America 108: 9927-9932.
20. Brambell FWR, (1958) The passive immunity of the young mammal. Biological Reviews 33: 488-531.
21. Schlamowitz M, Hillman K, Lichtiger B, Ahearn MJ, (1975) Preparation of IgG-binding membrane vesicles from the microvillar brush border of fetal rabbit yolk sac. J Immunol 115: 296-302.
22. Andersen SB, Bjorneboe M, (1964) Gamma globulin turnover in rabbits before and during hyperimmunization. J Exp Med 119: 537-546.
23. Johanson RA, Shaw AR, Schlamowitz M, (1981) Evidence that the CH2 domain of IgG contains the recognition unit for binding by the fetal rabbit yolk sac membrane receptor. J Immunol 126: 194-199.
24. Dima S, Medesan C, Mota G, Moraru I, Sjoquist J, et al. (1983) Effect of protein A and its fragment B on the catabolic and Fc receptor sites of IgG. Eur J Immunol 13: 605-614.
25. Kim JK, Tsen MF, Ghetie V, Ward ES, (1994) Localization of the site of the murine IgG1 molecule that is involved in binding to the murine intestinal Fc receptor. Eur J Immunol 24: 2429-2434.
26. Petkova SB, Akilesh S, Sproule TJ, Christianson GJ, Al Khabbaz H, et al. (2006) Enhanced half-life of genetically engineered human IgG1 antibodies in a humanized FcRn mouse model: potential application in humorally mediated autoimmune disease. Int Immunol 18: 1759-1769.
27. Bender B, Bodrogi L, Mayer B, Schneider Z, Zhao Y, et al. (2007) Position independent and copy-number-related expression of the bovine neonatal Fc receptor alpha-chain in transgenic mice carrying a 102 kb BAC genomic fragment. Transgenic Res 16: 613-627.
28. Cervenak J, Bender B, Schneider Z, Magna M, Carstea BV, et al. (2011) Neonatal FcR Overexpression Boosts Humoral Immune Response in Transgenic Mice. J Immunol 186: 959-968.
29. Vegh A, Cervenak J, Jankovics I, Kacskovics I, (2011) FcRn overexpression in mice results in potent humoral response against weakly immunogenic antigen. mAbs 3: 173-180.
30. Schneider Z, Cervenak J, Baranyi M, Papp K, Prechl J, et al. (2011) Transgenic expression of bovine neonatal Fc receptor in mice boosts immune response and improves hybridoma production efficiency without any sign of autoimmunity. Immunol Lett 137: 62-69.
31. Kacskovics I, Cervenak J, Erdei A, Goldsby RA, Butler JE, (2011) Recent Advances Using FcRn Overexpression in Transgenic Animals to Overcome Impediments of Standard Antibody Technologies. mAbs 3: 431-439.
32. Warner CM, Paschetto MG, (2000) Analysis of mRNA levels for the MHC class I-like molecules CD1 and FcRn in preimplantation mouse embryos. Am J Reprod Immunol 43: 234-239.
33. Martin WL, West AP Jr, Gan L, Bjorkman PJ, (2001) Crystal structure at 2.8 A of an FcRn/heterodimeric Fc complex: mechanism of pH-dependent binding. Mol Cell 7: 867-877.
34. Story CM, Mikulska JE, Simister NE, (1994) A major histocompatibility complex class I-like Fc receptor cloned from human placenta: possible role in transfer of immunoglobulin G from mother to fetus. J Exp Med 180: 2377-2381.
35. Kacskovics I, Wu Z, Simister NE, Frenyo LV, Hammarstrom L, (2000) Cloning and characterization of the bovine MHC class I-like Fc receptor. J Immunol 164: 1889-1897.
36. Kacskovics I, Mayer B, Kis Z, Frenyo LV, Zhao Y, et al. (2006) Cloning and characterization of the dromedary (Camelus dromedarius) neonatal Fc receptor (drFcRn). Dev Comp Immunol 30: 1203-1215.
37. Shields RL, Namenuk AK, Hong K, Meng YG, Rae J, et al. (2001) High resolution mapping of the binding site on human IgG1 for Fc gamma RI, Fc gamma RII, Fc gamma RIII, and FcRn and design of IgG1 variants with improved binding to the Fc gamma R. J Biol Chem 276: 6591-6604.
38. Raghavan M, Chen MY, Gastinel LN, Bjorkman PJ, (1994) Investigation of the interaction between the class I MHC-related Fc receptor and its immunoglobulin G ligand. Immunity 1: 303-315.
39. Gates FT 3rd, Coligan JE, Kindt TJ, (1979) Complete amino acid sequence of rabbit beta 2-microglobulin. Biochemistry 18: 2267-2272.
40. Chaudhury C, Brooks CL, Carter DC, Robinson JM, Anderson CL, (2006) Albumin binding to FcRn: distinct from the FcRn-IgG interaction. Biochemistry 45: 4983-4990.
41. Wu Z, Simister NE, (2001) Tryptophan- and dileucine-based endocytosis signals in the neonatal Fc receptor. J Biol Chem 276: 5240-5247.
42. Wernick NL, Haucke V, Simister NE, (2005) Recognition of the tryptophan-based endocytosis signal in the neonatal Fc Receptor by the mu subunit of adaptor protein-2. J Biol Chem 280: 7309-7316.
43. Newton EE, Wu Z, Simister NE, (2005) Characterization of basolateral-targeting signals in the neonatal Fc receptor. J Cell Sci 118: 2461-2469.
44. Kuo TT, de Muinck EJ, Claypool SM, Yoshida M, Nagaishi T, et al. (2009) N-Glycan Moieties in Neonatal Fc Receptor Determine Steady-state Membrane Distribution and Directional Transport of IgG. The Journal of biological chemistry 284: 8292-8300.
45. Prasad AB, Allard MW, Green ED, (2008) Confirming the phylogeny of mammals by use of large comparative sequence data sets. Molecular Biology and Evolution 25: 1795-1808.
46. Kacskovics I, Kis Z, Mayer B, West AP Jr, Tiangco NE, et al. (2006) FcRn mediates elongated serum half-life of human IgG in cattle. Int Immunol 18: 525-536.
47. Brambell FWR, (1970) The Transmission of Passive Immunity from Mother to Young; In: Neuberger A, Tatum EL, editors. Amsterdam North-Holland Publishing Company.
48. Sonoda S, Shigematsu T, Schlamowitz M, (1973) Binding and vesiculation of rabbit IgG by rabbit yolk sac membrane. J Immunol 110: 1682-1692.
49. Meads TJ, Wild AE, (1994) Evidence that Fc gamma receptors in rabbit yolk sac endoderm do not depend upon an acid pH to effect IgG binding and transcytosis in vitro. Placenta 15: 525-539.
50. Zhu X, Meng G, Dickinson BL, Li X, Mizoguchi E, et al. (2001) MHC class I-related neonatal Fc receptor for IgG is functionally expressed in monocytes, intestinal macrophages, and dendritic cells. J Immunol 166: 3266-3276.
51. Bodrogi L, Brands R, Raaben W, Seinen W, Baranyi M, et al. (2006) High level expression of tissue-nonspecific alkaline phosphatase in the milk of transgenic rabbits. Transgenic research 15: 627-636.
52. Hiripi L, Makovics F, Halter R, Baranyi M, Paul D, et al. (2003) Expression of active human blood clotting factor VIII in mammary gland of transgenic rabbits. DNA and cell biology 22: 41-45.
53. Roopenian DC, Christianson GJ, Sproule TJ, Brown AC, Akilesh S, et al. (2003) The MHC class I-like IgG receptor controls perinatal IgG transport, IgG homeostasis, and fate of IgG-Fc-coupled drugs. J Immunol 170: 3528-3533.
54. Roopenian DC, Akilesh S, (2007) FcRn: the neonatal Fc receptor comes of age. Nat Rev Immunol 7: 715-725.
55. Schneider Z, Cervenak J, Baranyi M, Papp K, Prechl J, et al. (2011) Transgenic expression of bovine neonatal Fc receptor in mice boosts immune response and improves hybridoma production efficiency without any sign of autoimmunity. Immunology Letters 137: 62-69.
56. Gan Z, Ram S, Vaccaro C, Ober RJ, Ward ES, (2009) Analyses of the recycling receptor, FcRn, in live cells reveal novel pathways for lysosomal delivery. Traffic 10: 600-614.
57. West AP Jr, Bjorkman PJ, (2000) Crystal Structure and Immunoglobulin G Binding Properties of the Human Major Histocompatibility Complex-Related Fc Receptor. Biochemistry 39: 9698-9708.
58. Vaughn DE, Milburn CM, Penny DM, Martin WL, Johnson JL, et al. (1997) Identification of critical IgG binding epitopes on the neonatal Fc receptor. J Mol Biol 274: 597-607.
59. Martin PL, Sachs C, Hoberman A, Jiao Q, Bugelski PJ, (2010) Effects of CNTO 530, an erythropoietin mimetic-IgG4 fusion protein, on embryofetal development in rats and rabbits. Birth Defects Res B Dev Reprod Toxicol 89: 87-96.
60. Pentsuk N, van der Laan JW, (2009) An interspecies comparison of placental antibody transfer: new insights into developmental toxicity testing of monoclonal antibodies. Birth Defects Res B Dev Reprod Toxicol 86: 328-344.
61. Cervenak J, Bender B, Schneider Z, Magna M, Carstea BV, et al. (2011) Neonatal FcR overexpression boosts humoral immune response in transgenic mice. Journal of immunology 186: 959-968.
62. Groves DJ, Morris BA, (2000) Veterinary sources of nonrodent monoclonal antibodies: interspecific and intraspecific hybridomas. Hybridoma 19: 201-214.
63. Popkov M, Mage RG, Alexander CB, Thundivalappil S, Barbas CF 3rd, et al. (2003) Rabbit immune repertoires as sources for therapeutic monoclonal antibodies: the impact of kappa allotype-correlated variation in cysteine content on antibody libraries selected by phage display. Journal of molecular biology 325: 325-335.
64. Mendicino M, Ramsoondar J, Phelps C, Vaught T, Ball S, et al. (2011) Generation of antibody- and B cell-deficient pigs by targeted disruption of the J-region gene segment of the heavy chain locus. Transgenic research 20: 625-641.
65. Ramsoondar J, Mendicino M, Phelps C, Vaught T, Ball S, et al. (2011) Targeted disruption of the porcine immunoglobulin kappa light chain locus. Transgenic research 20: 643-653.
66. Lonberg N, (2005) Human antibodies from transgenic animals. Nat Biotechnol 23: 1117-1125.
67. Flisikowska T, Thorey IS, Offner S, Ros F, Lifke V, et al. (2011) Efficient immunoglobulin gene disruption and targeted replacement in rabbit using zinc finger nucleases. PloS one 6: e21045.
68. Nicholas KB, Nicholas HBJ, (1997) GeneDoc: a tool for editing and annotating multiple sequence alignments.
69. Coligan JE, Kruisbeek AM, Margulies DH, Shevach EM, Strober W, (2009) Current Protocols in Immunology; Coico R, editor Hoboken, New Jersey John Wiley & Sons, Inc.
70. Schade R, Pfister C, Halatsch R, Henklein P, (1991) Polyclonal IgY antibodies from chicken egg yolk- an alternative to the production of mammalian IgG type antibodies in rabbits. ATLA 19: 403-419.
71. Rogel-Gaillard C, Piumi F, Billault A, Bourgeaux N, Save JC, et al. (2001) Construction of a rabbit bacterial artificial chromosome (BAC) library: application to the mapping of the major histocompatibility complex to position 12q.1.1. Mammalian genome: official journal of the International Mammalian Genome Society 12: 253-255.
72. Bosze Z, Hiripi L, (2011) Recombinant protein expression in milk of livestock species. In: Lorence E, editors. Recombinant gene expression: reviews and protocols 3rd edition ed: Springer.