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Published in: Virology Journal 1/2007

Open Access 01-12-2007 | Research

Feline aminopeptidase N is not a functional receptor for avian infectious bronchitis virus

Authors: Victor C Chu, Lisa J McElroy, Jed M Aronson, Trisha J Oura, Carole E Harbison, Beverley E Bauman, Gary R Whittaker

Published in: Virology Journal | Issue 1/2007

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Abstract

Background

Coronaviruses are an important cause of infectious diseases in humans, including severe acute respiratory syndrome (SARS), and have the continued potential for emergence from animal species. A major factor in the host range of a coronavirus is its receptor utilization on host cells. In many cases, coronavirus-receptor interactions are well understood. However, a notable exception is the receptor utilization by group 3 coronaviruses, including avian infectious bronchitis virus (IBV). Feline aminopeptidase N (fAPN) serves as a functional receptor for most group 1 coronaviruses including feline infectious peritonitis virus (FIPV), canine coronavirus, transmissible gastroenteritis virus (TGEV), and human coronavirus 229E (HCoV-229E). A recent report has also suggested a role for fAPN during IBV entry (Miguel B, Pharr GT, Wang C: The role of feline aminopeptidase N as a receptor for infectious bronchitis virus. Brief review. Arch Virol 2002, 147:2047–2056.

Results

Here we show that, whereas both transient transfection and constitutive expression of fAPN on BHK-21 cells can rescue FIPV and TGEV infection in non-permissive BHK cells, fAPN expression does not rescue infection by the prototype IBV strain Mass41. To account for the previous suggestion that fAPN could serve as an IBV receptor, we show that feline cells can be infected with the prototype strain of IBV (Mass 41), but with low susceptibility compared to primary chick kidney cells. We also show that BHK-21 cells are slightly susceptible to certain IBV strains, including Ark99, Ark_DPI, CA99, and Iowa97 (<0.01% efficiency), but this level of infection is not increased by fAPN expression.

Conclusion

We conclude that fAPN is not a functional receptor for IBV, the identity of which is currently under investigation.
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Literature
1.
go back to reference Spaan WJM, Brian D, Cavanagh D, de Groot RJ, Enjuanes L, Gorbalenya AE, Holmes KV, Masters PS, Rottier PJ, Taguchi F, Talbot P: Virus Taxonomy: Family Coronaviridae. In Eighth Report of the International Committee on Taxonomy of Viruses. 8th edition. Edited by: Fauquet CM, Mayo MA, Maniloff J, Desselberg U, Ball LA. London , Elsevier Academic Press; 2005:947-964. Spaan WJM, Brian D, Cavanagh D, de Groot RJ, Enjuanes L, Gorbalenya AE, Holmes KV, Masters PS, Rottier PJ, Taguchi F, Talbot P: Virus Taxonomy: Family Coronaviridae. In Eighth Report of the International Committee on Taxonomy of Viruses. 8th edition. Edited by: Fauquet CM, Mayo MA, Maniloff J, Desselberg U, Ball LA. London , Elsevier Academic Press; 2005:947-964.
2.
go back to reference Webster RG: Wet markets--a continuing source of severe acute respiratory syndrome and influenza? Lancet 2004,363(9404):234-236. 10.1016/S0140-6736(03)15329-9PubMedCrossRef Webster RG: Wet markets--a continuing source of severe acute respiratory syndrome and influenza? Lancet 2004,363(9404):234-236. 10.1016/S0140-6736(03)15329-9PubMedCrossRef
3.
go back to reference Makino S, Keck JG, Stohlman SA, Lai MM: High-frequency RNA recombination of murine coronaviruses. J Virol 1986,57(3):729-737.PubMedPubMedCentral Makino S, Keck JG, Stohlman SA, Lai MM: High-frequency RNA recombination of murine coronaviruses. J Virol 1986,57(3):729-737.PubMedPubMedCentral
4.
go back to reference Vijgen L, Keyaerts E, Moes E, Thoelen I, Wollants E, Lemey P, Vandamme AM, Van Ranst M: Complete genomic sequence of human coronavirus OC43: molecular clock analysis suggests a relatively recent zoonotic coronavirus transmission event. J Virol 2005,79(3):1595-1604. 10.1128/JVI.79.3.1595-1604.2005PubMedPubMedCentralCrossRef Vijgen L, Keyaerts E, Moes E, Thoelen I, Wollants E, Lemey P, Vandamme AM, Van Ranst M: Complete genomic sequence of human coronavirus OC43: molecular clock analysis suggests a relatively recent zoonotic coronavirus transmission event. J Virol 2005,79(3):1595-1604. 10.1128/JVI.79.3.1595-1604.2005PubMedPubMedCentralCrossRef
5.
go back to reference Li W, Wong SK, Li F, Kuhn JH, Huang IC, Choe H, Farzan M: Animal origins of the severe acute respiratory syndrome coronavirus: insight from ACE2-S-protein interactions. J Virol 2006,80(9):4211-4219. 10.1128/JVI.80.9.4211-4219.2006PubMedPubMedCentralCrossRef Li W, Wong SK, Li F, Kuhn JH, Huang IC, Choe H, Farzan M: Animal origins of the severe acute respiratory syndrome coronavirus: insight from ACE2-S-protein interactions. J Virol 2006,80(9):4211-4219. 10.1128/JVI.80.9.4211-4219.2006PubMedPubMedCentralCrossRef
6.
go back to reference Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, Wong BH, Wong SS, Leung SY, Chan KH, Yuen KY: Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci U S A 2005,102(39):14040-14045. 10.1073/pnas.0506735102PubMedPubMedCentralCrossRef Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, Wong BH, Wong SS, Leung SY, Chan KH, Yuen KY: Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci U S A 2005,102(39):14040-14045. 10.1073/pnas.0506735102PubMedPubMedCentralCrossRef
7.
go back to reference Luytjes W, Bredenbeek PJ, Noten AF, Horzinek MC, Spaan WJ: Sequence of mouse hepatitis virus A59 mRNA 2: indications for RNA recombination between coronaviruses and influenza C virus. Virology 1988,166(2):415-422. 10.1016/0042-6822(88)90512-0PubMedCrossRef Luytjes W, Bredenbeek PJ, Noten AF, Horzinek MC, Spaan WJ: Sequence of mouse hepatitis virus A59 mRNA 2: indications for RNA recombination between coronaviruses and influenza C virus. Virology 1988,166(2):415-422. 10.1016/0042-6822(88)90512-0PubMedCrossRef
8.
go back to reference Zhang XM, Kousoulas KG, Storz J: The hemagglutinin/esterase gene of human coronavirus strain OC43: phylogenetic relationships to bovine and murine coronaviruses and influenza C virus. Virology 1992,186(1):318-323. 10.1016/0042-6822(92)90089-8PubMedCrossRef Zhang XM, Kousoulas KG, Storz J: The hemagglutinin/esterase gene of human coronavirus strain OC43: phylogenetic relationships to bovine and murine coronaviruses and influenza C virus. Virology 1992,186(1):318-323. 10.1016/0042-6822(92)90089-8PubMedCrossRef
9.
go back to reference Schwegmann-Wessels C, Herrler G: Sialic acids as receptor determinants for coronaviruses. Glycoconj J 2006,23(1-2):51-58. 10.1007/s10719-006-5437-9PubMedCrossRef Schwegmann-Wessels C, Herrler G: Sialic acids as receptor determinants for coronaviruses. Glycoconj J 2006,23(1-2):51-58. 10.1007/s10719-006-5437-9PubMedCrossRef
10.
go back to reference Yeager CL, Ashmun RA, Williams RK, Cardellichio CB, Shapiro LH, Look AT, Holmes KV: Human aminopeptidase N is a receptor for human coronavirus 229E. Nature 1992,357(6377):420-422. 10.1038/357420a0PubMedCrossRef Yeager CL, Ashmun RA, Williams RK, Cardellichio CB, Shapiro LH, Look AT, Holmes KV: Human aminopeptidase N is a receptor for human coronavirus 229E. Nature 1992,357(6377):420-422. 10.1038/357420a0PubMedCrossRef
11.
go back to reference Tresnan DB, Levis R, Holmes KV: Feline aminopeptidase N serves as a receptor for feline, canine, porcine, and human coronaviruses in serogroup I. J Virol 1996,70(12):8669-8674.PubMedPubMedCentral Tresnan DB, Levis R, Holmes KV: Feline aminopeptidase N serves as a receptor for feline, canine, porcine, and human coronaviruses in serogroup I. J Virol 1996,70(12):8669-8674.PubMedPubMedCentral
12.
go back to reference Delmas B, Gelfi J, L'Haridon R, Vogel LK, Sjostrom H, Noren O, Laude H: Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature 1992,357(6377):417-420. 10.1038/357417a0PubMedCrossRef Delmas B, Gelfi J, L'Haridon R, Vogel LK, Sjostrom H, Noren O, Laude H: Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature 1992,357(6377):417-420. 10.1038/357417a0PubMedCrossRef
13.
go back to reference Tresnan DB, Holmes KV: Feline aminopeptidase N is a receptor for all group I coronaviruses. Adv Exp Med Biol 1998, 440: 69-75.PubMedCrossRef Tresnan DB, Holmes KV: Feline aminopeptidase N is a receptor for all group I coronaviruses. Adv Exp Med Biol 1998, 440: 69-75.PubMedCrossRef
14.
go back to reference Nash TC, Buchmeier MJ: Spike glycoprotein-mediated fusion in biliary glycoprotein-independent cell-associated spread of mouse hepatitis virus infection. Virology 1996,223(1):68-78. 10.1006/viro.1996.0456PubMedCrossRef Nash TC, Buchmeier MJ: Spike glycoprotein-mediated fusion in biliary glycoprotein-independent cell-associated spread of mouse hepatitis virus infection. Virology 1996,223(1):68-78. 10.1006/viro.1996.0456PubMedCrossRef
15.
go back to reference Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, Berne MA, Somasundaran M, Sullivan JL, Luzuriaga K, Greenough TC, Choe H, Farzan M: Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 2003,426(6965):450-454. 10.1038/nature02145PubMedCrossRef Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, Berne MA, Somasundaran M, Sullivan JL, Luzuriaga K, Greenough TC, Choe H, Farzan M: Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 2003,426(6965):450-454. 10.1038/nature02145PubMedCrossRef
16.
go back to reference Winter C, Schwegmann-Wessels C, Cavanagh D, Neumann U, Herrler G: Sialic acid is a receptor determinant for infection of cells by avian Infectious bronchitis virus. J Gen Virol 2006,87(Pt 5):1209-1216. 10.1099/vir.0.81651-0PubMedCrossRef Winter C, Schwegmann-Wessels C, Cavanagh D, Neumann U, Herrler G: Sialic acid is a receptor determinant for infection of cells by avian Infectious bronchitis virus. J Gen Virol 2006,87(Pt 5):1209-1216. 10.1099/vir.0.81651-0PubMedCrossRef
17.
go back to reference Madu IG, Chu VC, Lee H, Regan AD, Bauman BE, Whittaker GR: Heparan sulfate is a selective attachment factor for the avian coronavirus IBV Beaudette. Avian Diseases Accepted for publication Madu IG, Chu VC, Lee H, Regan AD, Bauman BE, Whittaker GR: Heparan sulfate is a selective attachment factor for the avian coronavirus IBV Beaudette. Avian Diseases Accepted for publication
18.
go back to reference Beaudette FR, Hudson CB: Cultivation of the virus of infectious bronchitis: August 11-14; Columbus, OH. New Jersey Agricultural Experiment Station; 1936:51-60. Beaudette FR, Hudson CB: Cultivation of the virus of infectious bronchitis: August 11-14; Columbus, OH. New Jersey Agricultural Experiment Station; 1936:51-60.
19.
go back to reference Otsuki K, Noro K, Yamamoto H, Tsubokura M: Studies on avian infectious bronchitis virus (IBV). II. Propagation of IBV in several cultured cells. Arch Virol 1979,60(2):115-122. 10.1007/BF01348027PubMedCrossRef Otsuki K, Noro K, Yamamoto H, Tsubokura M: Studies on avian infectious bronchitis virus (IBV). II. Propagation of IBV in several cultured cells. Arch Virol 1979,60(2):115-122. 10.1007/BF01348027PubMedCrossRef
20.
go back to reference Chu VC, McElroy LJ, Chu V, Bauman BE, Whittaker GR: The avian coronavirus infectious bronchitis virus undergoes direct low-pH-dependent fusion activation during entry into host cells. J Virol 2006,80(7):3180-3188. 10.1128/JVI.80.7.3180-3188.2006PubMedPubMedCentralCrossRef Chu VC, McElroy LJ, Chu V, Bauman BE, Whittaker GR: The avian coronavirus infectious bronchitis virus undergoes direct low-pH-dependent fusion activation during entry into host cells. J Virol 2006,80(7):3180-3188. 10.1128/JVI.80.7.3180-3188.2006PubMedPubMedCentralCrossRef
21.
go back to reference Miguel B, Pharr GT, Wang C: The role of feline aminopeptidase N as a receptor for infectious bronchitis virus. Brief review. Arch Virol 2002,147(11):2047-2056. 10.1007/s00705-002-0888-1PubMedCrossRef Miguel B, Pharr GT, Wang C: The role of feline aminopeptidase N as a receptor for infectious bronchitis virus. Brief review. Arch Virol 2002,147(11):2047-2056. 10.1007/s00705-002-0888-1PubMedCrossRef
22.
go back to reference Hooper NM: Families of zinc metalloproteases. FEBS Lett 1994,354(1):1-6. 10.1016/0014-5793(94)01079-XPubMedCrossRef Hooper NM: Families of zinc metalloproteases. FEBS Lett 1994,354(1):1-6. 10.1016/0014-5793(94)01079-XPubMedCrossRef
23.
go back to reference Kolb AF, Hegyi A, Siddell SG: Identification of residues critical for the human coronavirus 229E receptor function of human aminopeptidase N. J Gen Virol 1997, 78 ( Pt 11): 2795-2802.CrossRef Kolb AF, Hegyi A, Siddell SG: Identification of residues critical for the human coronavirus 229E receptor function of human aminopeptidase N. J Gen Virol 1997, 78 ( Pt 11): 2795-2802.CrossRef
24.
go back to reference Cavanagh D, Naqi SA: Infectious Bronchitis. In Diseases of Poultry. Edited by: Saif SM. Ames, Iowa , Iowa State Press; 2003:101-119. Cavanagh D, Naqi SA: Infectious Bronchitis. In Diseases of Poultry. Edited by: Saif SM. Ames, Iowa , Iowa State Press; 2003:101-119.
25.
go back to reference Chu VC, McElroy LJ, Bauman BE, Whittaker GR: Fluorescence dequenching assays of coronavirus fusion. Adv Exp Med Biol 2006, 581: 241-246.PubMedCrossRef Chu VC, McElroy LJ, Bauman BE, Whittaker GR: Fluorescence dequenching assays of coronavirus fusion. Adv Exp Med Biol 2006, 581: 241-246.PubMedCrossRef
26.
go back to reference Sommerfelt MA: Retrovirus receptors. J Gen Virol 1999, 80 ( Pt 12): 3049-3064.CrossRef Sommerfelt MA: Retrovirus receptors. J Gen Virol 1999, 80 ( Pt 12): 3049-3064.CrossRef
27.
go back to reference Vennema H, Poland A, Foley J, Pedersen NC: Feline infectious peritonitis viruses arise by mutation from endemic feline enteric coronaviruses. Virology 1998,243(1):150-157. 10.1006/viro.1998.9045PubMedCrossRef Vennema H, Poland A, Foley J, Pedersen NC: Feline infectious peritonitis viruses arise by mutation from endemic feline enteric coronaviruses. Virology 1998,243(1):150-157. 10.1006/viro.1998.9045PubMedCrossRef
28.
go back to reference Stavrinides J, Guttman DS: Mosaic evolution of the severe acute respiratory syndrome coronavirus. J Virol 2004,78(1):76-82. 10.1128/JVI.78.1.76-82.2004PubMedPubMedCentralCrossRef Stavrinides J, Guttman DS: Mosaic evolution of the severe acute respiratory syndrome coronavirus. J Virol 2004,78(1):76-82. 10.1128/JVI.78.1.76-82.2004PubMedPubMedCentralCrossRef
29.
go back to reference Sieczkarski SB, Whittaker GR: Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J Virol 2002,76(20):10455-10464. 10.1128/JVI.76.20.10455-10464.2002PubMedPubMedCentralCrossRef Sieczkarski SB, Whittaker GR: Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J Virol 2002,76(20):10455-10464. 10.1128/JVI.76.20.10455-10464.2002PubMedPubMedCentralCrossRef
Metadata
Title
Feline aminopeptidase N is not a functional receptor for avian infectious bronchitis virus
Authors
Victor C Chu
Lisa J McElroy
Jed M Aronson
Trisha J Oura
Carole E Harbison
Beverley E Bauman
Gary R Whittaker
Publication date
01-12-2007
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2007
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-4-20

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