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The E5 protein of the human papillomavirus type 16 down-regulates HLA-I surface expression in calnexin-expressing but not in calnexin-deficient cells

Gruener, Myriam, Bravo, Ignacio G, Momburg, Frank, Alonso, Angel, Tomakidi, Pascal·2007·Virology Journal
DOI 10.1186/1743-422x-4-116PMC PMC2164959
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Abstract

The human papillomavirus type 16 E5 protein (HPV16 E5) down-regulates surface expression of HLA-I molecules. The molecular mechanisms underlying this effect are so far unknown. Here we show that HPV16 E5 down-regulates HLA-I surface expression in calnexin-containing but not in calnexin-deficient cells. Immunoprecipitation experiments reveal that calnexin and HPV16E5 can be co-precipitated and that this association depends on the presence of a wild-type first hydrophobic region of E5. When an E5 mutant (M1) in which the first putative transmembrane helix had been disrupted was used for the transfections calnexin-E5 co-precipitation was strongly impaired. In addition, we show that the M1 mutant is only able to marginally down-regulate HLA-I surface expression compared to the wild-type protein. Besides, we demonstrate that E5 forms a ternary complex with calnexin and the heavy chain of HLA-I, which is mediated by the first hydrophobic region of the E5 protein. On the basis of our results we conclude that formation of this complex is responsible for retention of HLA-I molecules in the ER of the cells.

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Figure 1 HPV16 E5 expression down-regulates HLA-I surface molecules. HEK-293T cells were transfected either with (A) pEGFP-HPV16-E5 or empty pEGFP vector, (B) pCI-HPV16-E5-HA or empty pCI vector. HLA-I molecules were then detected by immunostaining and flow cytometry using mouse monoclonal anti-HLA-A, B, C (mAb B9.12). Differences between the HLA-I surface expression levels were assessed by Kolmogorov-Smirnov test. This statistic defines the maximum vertical deviation between the two curves (pEGFP-E5 and GFP, pCI-E5-HA and pCI) as the statistic D. The p value of each single experiment was in all cases ≤ 0.001.
Figure 1 HPV16 E5 expression down-regulates HLA-I surface molecules. HEK-293T cells were transfected either with (A) pEGFP-HPV16-E5 or empty pEGFP vector, (B) pCI-HPV16-E5-HA or empty pCI vector. HLA-I molecules were then detected by immunostaining and flow cytometry using mouse monoclonal anti-HLA-A, B, C (mAb B9.12). Differences between the HLA-I surface expression levels were assessed by Kolmogorov-Smirnov test. This statistic defines the maximum vertical deviation between the two curves (pEGFP-E5 and GFP, pCI-E5-HA and pCI) as the statistic D. The p value of each single experiment was in all cases ≤ 0.001.CC BY · PubMed Central
Figure 2 HPV16 E5 decreases HLA-I surface expression in calnexin-containing but not in calnexin-deficient cells. CEM-C7 (calnexin) and CEM-NKR (no calnexin) cells were stably transfected with pCI-HPV16-E5-HA or pCI empty vector. A) Calnexin is only expressed in CEM-C7 cells but not in CEM-NKR cells. B) E5-HA expression was analysed in each stable polyclone by immunoprecipitation and -blot using mouse monoclonal anti-HA Ab and 500 μg RIPA cell lysate. C) FACS analysis of CEM-NKR and CEM-C7 cells transfected with either the empty vector pCI or with pCI-E5-HA were stained with anti-HLA-A, B, C mAbs B9.12. E5 expression results in diminished HLA-I surface staining in cells expressing calnexin, but not in calnexin deficient cells. D) The upper part of the blot shown in A was incubated with anti-HC-10 antibodies (anti HLA-B, C). Incubation with anti-actin antibodies was performed as loading control. Columns represent average values (N = 5) and the error bars comprise the corresponding standard deviations. There were no differences between the total amounts of cellular HLA (N = 5; pKW = 0.87, Kruskal-Wallis test, and pA = 0.77, ANOVA). Molecular-mass markers (in kDa) are indicated in the left of the blots.
Figure 2 HPV16 E5 decreases HLA-I surface expression in calnexin-containing but not in calnexin-deficient cells. CEM-C7 (calnexin) and CEM-NKR (no calnexin) cells were stably transfected with pCI-HPV16-E5-HA or pCI empty vector. A) Calnexin is only expressed in CEM-C7 cells but not in CEM-NKR cells. B) E5-HA expression was analysed in each stable polyclone by immunoprecipitation and -blot using mouse monoclonal anti-HA Ab and 500 μg RIPA cell lysate. C) FACS analysis of CEM-NKR and CEM-C7 cells transfected with either the empty vector pCI or with pCI-E5-HA were stained with anti-HLA-A, B, C mAbs B9.12. E5 expression results in diminished HLA-I surface staining in cells expressing calnexin, but not in calnexin deficient cells. D) The upper part of the blot shown in A was incubated with anti-HC-10 antibodies (anti HLA-B, C). Incubation with anti-actin antibodies was performed as loading control. Columns represent average values (N = 5) and the error bars comprise the corresponding standard deviations. There were no differences between the total amounts of cellular HLA (N = 5; pKW = 0.87, Kruskal-Wallis test, and pA = 0.77, ANOVA). Molecular-mass markers (in kDa) are indicated in the left of the blots.CC BY · PubMed Central
Figure 3 Transporter activity of TAP is not influenced by HPV16 E5. Streptolysin Opermeabilized calnexin-proficient CEM-C7 and calnexin-deficient CEM-NKR cells (38) were analysed in a peptide translocation/glyosylation assay using the indicated input quantities of the radioiodinated reporter peptide TNKTRIDGQY (glycosylation consensus site underlined) in the presence or absence of ATP. The glycosylated fraction, indicative of TAP-mediated ER transport, is isolated by concanavalin A Sepharose and quantitated by γ-counting. No significant differences could be detected between HPV16 E5-expressing cells and the control cells irrespective from the presence (CEM-C7) or absence (CEM-NKR) of calnexin.
Figure 3 Transporter activity of TAP is not influenced by HPV16 E5. Streptolysin Opermeabilized calnexin-proficient CEM-C7 and calnexin-deficient CEM-NKR cells (38) were analysed in a peptide translocation/glyosylation assay using the indicated input quantities of the radioiodinated reporter peptide TNKTRIDGQY (glycosylation consensus site underlined) in the presence or absence of ATP. The glycosylated fraction, indicative of TAP-mediated ER transport, is isolated by concanavalin A Sepharose and quantitated by γ-counting. No significant differences could be detected between HPV16 E5-expressing cells and the control cells irrespective from the presence (CEM-C7) or absence (CEM-NKR) of calnexin.CC BY · PubMed Central
Figure 4 Calnexin interacts with the HPV16 E5 protein in cellular extracts. HEK-293T cells were transfected with AU1-tagged codon-optimised HPV16 E5, pCI-HPV16-E5-HA or corresponding empty vectors and lysed at 24 h posttransfection with CHAPS lysis buffer. A) Immunoblot showing the expression levels of the codon-optimised E5 gene (left panel) and of the viral E5 gene (right panel). Note the differences in the immunoreactivity signals despite the higher amount of total protein loaded in the non-optimised gene (100 μg vs 30 μg). B) Immunoprecipitations were performed using monoclonal anti-E5-tag (AU1) antibodies and proteins in the immune complexes were probed using anti-AU1 and anti-calnexin antibodies. C) Immunoprecipitations were performed using monoclonal anti-calnexin antibodies and proteins in the immune complexes were probed using anti-calnexin and anti-E5-tag (AU1) anti-bodies. D) Immunoprecipitations were performed using monoclonal anti-E5-tag (HA) antibodies and proteins in the immune complexes were probed using anti-HA and anti-calnexin antibodies. E) 2 Immunoprecipitations were performed using monoclonal anti-calnexin antibodies and proteins in the immune complexes were probed using anti-calnexin and anti-E5-tag (HA) antibodies. Molecular-mass markers in kDa are indicated at the left of the blots.
Figure 4 Calnexin interacts with the HPV16 E5 protein in cellular extracts. HEK-293T cells were transfected with AU1-tagged codon-optimised HPV16 E5, pCI-HPV16-E5-HA or corresponding empty vectors and lysed at 24 h posttransfection with CHAPS lysis buffer. A) Immunoblot showing the expression levels of the codon-optimised E5 gene (left panel) and of the viral E5 gene (right panel). Note the differences in the immunoreactivity signals despite the higher amount of total protein loaded in the non-optimised gene (100 μg vs 30 μg). B) Immunoprecipitations were performed using monoclonal anti-E5-tag (AU1) antibodies and proteins in the immune complexes were probed using anti-AU1 and anti-calnexin antibodies. C) Immunoprecipitations were performed using monoclonal anti-calnexin antibodies and proteins in the immune complexes were probed using anti-calnexin and anti-E5-tag (AU1) anti-bodies. D) Immunoprecipitations were performed using monoclonal anti-E5-tag (HA) antibodies and proteins in the immune complexes were probed using anti-HA and anti-calnexin antibodies. E) 2 Immunoprecipitations were performed using monoclonal anti-calnexin antibodies and proteins in the immune complexes were probed using anti-calnexin and anti-E5-tag (HA) antibodies. Molecular-mass markers in kDa are indicated at the left of the blots.CC BY · PubMed Central
Figure 5 Co-localization of HPV16 E5 with calnexin. HaCaT cells were transfected with AU1- tagged codon-optimised E5 or pEGFP-E5 and analysed after 24 h by confocal laser scanning microscopy using a monoclonal anti-AU1 and/or polyclonal anti-calnexin Abs.
Figure 5 Co-localization of HPV16 E5 with calnexin. HaCaT cells were transfected with AU1- tagged codon-optimised E5 or pEGFP-E5 and analysed after 24 h by confocal laser scanning microscopy using a monoclonal anti-AU1 and/or polyclonal anti-calnexin Abs.CC BY · PubMed Central
Figure 6 Transmembrane Hidden Markov Model posterior probabilities for the sequences of E5 and the mutants M1, M2 and M3. A) Amino acid sequence of the wild-type E5 protein and corresponding mutants. Aminoacids of the AU1-tag are underlined. Arrows show the position of exchanged amino acids. B) Analysis of the wild-type E5 and mutants using the TMHMM 2.0 algorithm (36, 37), showing the three hydrophobic regions predicted to be transmembrane domains, and the corresponding disruptions in the three mutants.
Figure 6 Transmembrane Hidden Markov Model posterior probabilities for the sequences of E5 and the mutants M1, M2 and M3. A) Amino acid sequence of the wild-type E5 protein and corresponding mutants. Aminoacids of the AU1-tag are underlined. Arrows show the position of exchanged amino acids. B) Analysis of the wild-type E5 and mutants using the TMHMM 2.0 algorithm (36, 37), showing the three hydrophobic regions predicted to be transmembrane domains, and the corresponding disruptions in the three mutants.CC BY · PubMed Central
Figure 7 Mutant M1 binds less calnexin than wild-type E5 protein. HEK-293T cells were transfected with either (A-C) AU1-tagged codon-optimised HPV16 E5, the mutants M1, M2 and M3 or pcDNA 3.1 empty vector as control, (D and E) pEGFP-tagged HPV16 E5, mutant pEGFPM1, mock-control or pEGFP empty vector and lysed at 24 h posttransfection with CHAPS lysis buffer. A) Similar expression levels of all HPV16 E5 and the mutants M1, M2 and M3. B) Immunoprecipitations were performed using monoclonal anti-AU1, and proteins in the immune complex were detected using anti-AU1 and anti-calnexin. C) Quantification of co-precipitated calnexin for wild-type HPV16E5 protein, the mutants M1, M2, M3 and the vector control. The wild-type expression level was set to 100%. Data shown represent six independent experiments 2 plus standard errors of the mean. P values were calculated with paired two-tailed Student's t-test. D) Similar expression levels of pEGFP-HPV16-E5 and the mutant pEGFP-M1. E) Immunoprecipitations were performed using monoclonal anti-GFP, and proteins in the immune complex were detected using anti-GFP and anti-calnexin. Molecular-mass markers in kDa are indicated at the left of the blots.
Figure 7 Mutant M1 binds less calnexin than wild-type E5 protein. HEK-293T cells were transfected with either (A-C) AU1-tagged codon-optimised HPV16 E5, the mutants M1, M2 and M3 or pcDNA 3.1 empty vector as control, (D and E) pEGFP-tagged HPV16 E5, mutant pEGFPM1, mock-control or pEGFP empty vector and lysed at 24 h posttransfection with CHAPS lysis buffer. A) Similar expression levels of all HPV16 E5 and the mutants M1, M2 and M3. B) Immunoprecipitations were performed using monoclonal anti-AU1, and proteins in the immune complex were detected using anti-AU1 and anti-calnexin. C) Quantification of co-precipitated calnexin for wild-type HPV16E5 protein, the mutants M1, M2, M3 and the vector control. The wild-type expression level was set to 100%. Data shown represent six independent experiments 2 plus standard errors of the mean. P values were calculated with paired two-tailed Student's t-test. D) Similar expression levels of pEGFP-HPV16-E5 and the mutant pEGFP-M1. E) Immunoprecipitations were performed using monoclonal anti-GFP, and proteins in the immune complex were detected using anti-GFP and anti-calnexin. Molecular-mass markers in kDa are indicated at the left of the blots.CC BY · PubMed Central
Figure 8 HPV16 E5, M2 and M3 mutants but not M1 mutant strongly co-localize with calnexin. HaCaT cells were transfected with A) AU1-tagged codon-optimised E5 or AU1- tagged codonoptimised E5 mutants M1 B), M2 C), and M3 D) and analysed after 24 h by confocal laser scanning microscopy using a monoclonal anti-AU1 and polyclonal anticalnexin antibodies.
Figure 8 HPV16 E5, M2 and M3 mutants but not M1 mutant strongly co-localize with calnexin. HaCaT cells were transfected with A) AU1-tagged codon-optimised E5 or AU1- tagged codonoptimised E5 mutants M1 B), M2 C), and M3 D) and analysed after 24 h by confocal laser scanning microscopy using a monoclonal anti-AU1 and polyclonal anticalnexin antibodies.CC BY · PubMed Central
Figure 9 HPV16 E5 forms a ternary complex with calnexin and the HLA-I heavy chain. HeLa cells were transiently transfected with AU1-tagged codon-optimised HPV16 E5, M1, or empty vector. 24 h later CHAPS lysates were immunoprecipitated with antibodies against the E5-tag (anti-AU1). Precipitated immune complexes were separated by SDS-PAGE and Western blotted using anti-calnexin and anti-HLA-B, -C mAb (HC10), respectively (band marked with *). Molecular-mass markers in kDa are indicated at the left of the blots.
Figure 9 HPV16 E5 forms a ternary complex with calnexin and the HLA-I heavy chain. HeLa cells were transiently transfected with AU1-tagged codon-optimised HPV16 E5, M1, or empty vector. 24 h later CHAPS lysates were immunoprecipitated with antibodies against the E5-tag (anti-AU1). Precipitated immune complexes were separated by SDS-PAGE and Western blotted using anti-calnexin and anti-HLA-B, -C mAb (HC10), respectively (band marked with *). Molecular-mass markers in kDa are indicated at the left of the blots.CC BY · PubMed Central
Figure 10 E5 mutant M1 down-regulates surface expression of HLA-I to a lesser extent than the E5 protein does. HEK-293T cells were transfected either with pEGFP-HPV16- E5, -M1, or empty pEGFP vector. HLA-I molecules were detected by immunostaining and flow cytometry using mouse monoclonal anti-B9.12 Ab. Results for one representative experiment out of six are shown. Statistic analysis is shown in Table 1.
Figure 10 E5 mutant M1 down-regulates surface expression of HLA-I to a lesser extent than the E5 protein does. HEK-293T cells were transfected either with pEGFP-HPV16- E5, -M1, or empty pEGFP vector. HLA-I molecules were detected by immunostaining and flow cytometry using mouse monoclonal anti-B9.12 Ab. Results for one representative experiment out of six are shown. Statistic analysis is shown in Table 1.CC BY · PubMed Central

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  55. Samorski R, Gissmann L, Osen W: Codon optimized expression of HPV 16 E6 renders target cells susceptible to E6-specific CTL recognition. Immunol Lett. 2006, 107: 41-49. 10.1016/j.imlet.2006.07.003. · DOI

Cited by

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Metadata

Authors
Gruener, M., Bravo, I. G., Momburg, F., Alonso, A., & Tomakidi, P.
Venue
Virology Journal
Publisher
Springer Science and Business Media LLC
Published
2007-10-30
Volume
4
Issue
1
ISSN
1743-422X
DOI
10.1186/1743-422x-4-116
PMC
PMC2164959
Cited by
53
References
1
Language
en

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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