Tumor Cell Marker PVRL4 (Nectin 4) Is an Epithelial Cell Receptor for Measles Virus
Vaccine and laboratory adapted strains of measles virus can use CD46 as a receptor to infect many human cell lines. However, wild type isolates of measles virus cannot use CD46, and they infect activated lymphocytes, dendritic cells, and macrophages via the receptor CD150/SLAM. Wild type virus can also infect epithelial cells of the respiratory tract through an unidentified receptor. We demonstrate that wild type measles virus infects primary airway epithelial cells grown in fetal calf serum and many adenocarcinoma cell lines of the lung, breast, and colon. Transfection of non-infectable adenocarcinoma cell lines with an expression vector encoding CD150/SLAM rendered them susceptible to measles virus, indicating that they were virus replication competent, but lacked a receptor for virus attachment and entry. Microarray analysis of susceptible versus non-susceptible cell lines was performed, and comparison of membrane protein gene transcripts produced a list of 11 candidate receptors. Of these, only the human tumor cell marker PVRL4 (Nectin 4) rendered cells amenable to measles virus infections. Flow cytometry confirmed that PVRL4 is highly expressed on the surfaces of susceptible lung, breast, and colon adenocarcinoma cell lines. Measles virus preferentially infected adenocarcinoma cell lines from the apical surface, although basolateral infection was observed with reduced kinetics. Confocal immune fluorescence microscopy and surface biotinylation experiments revealed that PVRL4 was expressed on both the apical and basolateral surfaces of these cell lines. Antibodies and siRNA directed against PVRL4 were able to block measles virus infections in MCF7 and NCI-H358 cancer cells. A virus binding assay indicated that PVRL4 was a bona fide receptor that supported virus attachment to the host cell. Several strains of measles virus were also shown to use PVRL4 as a receptor. Measles virus infection reduced PVRL4 surface expression in MCF7 cells, a property that is characteristic of receptor-associated viral infections.
Vyšlo v časopise:
Tumor Cell Marker PVRL4 (Nectin 4) Is an Epithelial Cell Receptor for Measles Virus. PLoS Pathog 7(8): e32767. doi:10.1371/journal.ppat.1002240
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Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1002240
Souhrn
Vaccine and laboratory adapted strains of measles virus can use CD46 as a receptor to infect many human cell lines. However, wild type isolates of measles virus cannot use CD46, and they infect activated lymphocytes, dendritic cells, and macrophages via the receptor CD150/SLAM. Wild type virus can also infect epithelial cells of the respiratory tract through an unidentified receptor. We demonstrate that wild type measles virus infects primary airway epithelial cells grown in fetal calf serum and many adenocarcinoma cell lines of the lung, breast, and colon. Transfection of non-infectable adenocarcinoma cell lines with an expression vector encoding CD150/SLAM rendered them susceptible to measles virus, indicating that they were virus replication competent, but lacked a receptor for virus attachment and entry. Microarray analysis of susceptible versus non-susceptible cell lines was performed, and comparison of membrane protein gene transcripts produced a list of 11 candidate receptors. Of these, only the human tumor cell marker PVRL4 (Nectin 4) rendered cells amenable to measles virus infections. Flow cytometry confirmed that PVRL4 is highly expressed on the surfaces of susceptible lung, breast, and colon adenocarcinoma cell lines. Measles virus preferentially infected adenocarcinoma cell lines from the apical surface, although basolateral infection was observed with reduced kinetics. Confocal immune fluorescence microscopy and surface biotinylation experiments revealed that PVRL4 was expressed on both the apical and basolateral surfaces of these cell lines. Antibodies and siRNA directed against PVRL4 were able to block measles virus infections in MCF7 and NCI-H358 cancer cells. A virus binding assay indicated that PVRL4 was a bona fide receptor that supported virus attachment to the host cell. Several strains of measles virus were also shown to use PVRL4 as a receptor. Measles virus infection reduced PVRL4 surface expression in MCF7 cells, a property that is characteristic of receptor-associated viral infections.
Zdroje
1. EndersJFKatzSLHollowayA 1962 Development of attenuated measles-virus vaccines. A summary of recentinvestigation. Am J Dis Child 103 335 340
2. MossWJ 2009 Measles control and the prospect of eradication. Curr Top Microbiol Immunol 330 173 189
3. BlakeFGTraskJD 1921 Studies on Measles : I. Susceptibility of Monkeys to the Virus of Measles. J Exp Med 33 385 412
4. de SwartRL 2009 Measles studies in the macaque model. Curr Top Microbiol Immunol 330 55 72
5. KobuneFTakahashiHTeraoKOhkawaTAmiY 1996 Nonhuman primate models of measles. Lab Anim Sci 46 315 320
6. McChesneyMBMillerCJRotaPAZhuYDAntipaL 1997 Experimental measles. I. Pathogenesis in the normal and the immunized host. Virology 233 74 84
7. ZhuYDHeathJCollinsJGreeneTAntipaL 1997 Experimental measles. II. Infection and immunity in the rhesus macaque. Virology 233 85 92
8. BurnsteinTJensenJHWaksmanBH 1964 The Development of a Neurotropic Strain of Measles Virus in Hamsters and Mice. J Infect Dis 114 265 272
9. GriffinDEMullinixJNarayanOJohnsonRT 1974 Age dependence of viral expression: comparative pathogenesis of two rodent-adapted strains of measles virus in mice. Infect Immun 9 690 695
10. LiebertUGFinkeD 1995 Measles virus infections in rodents. Curr Top Microbiol Immunol 191 149 166
11. BlechaczBRussellSJ 2008 Measles virus as an oncolytic vector platform. Curr Gene Ther 8 162 175
12. RussellSJPengKW 2009 Measles virus for cancer therapy. Curr Top Microbiol Immunol 330 213 241
13. GriffinDE 2006 Measles Virus. Knipe D.M., editor in chief New York Lippincott, Williams, and Wilkins 1551 1585 Fields' Virology.
14. NavaratnarajahCKLeonardVHCattaneoR 2009 Measles virus glycoprotein complex assembly, receptor attachment, and cell entry. Curr Top Microbiol Immunol 329 59 76
15. HashiguchiTOseTKubotaMMaitaNKamishikiryoJ 2011 Structure of the measles virus hemagglutinin bound to its cellular receptor SLAM. Nat Struct Mol Biol 18 135 141
16. NavaratnarajahCKOezguenNRuppLKayLLeonardVH 2011 The heads of the measles virus attachment protein move to transmit the fusion-triggering signal. Nat Struct Mol Biol 18 128 134
17. YanagiYTakedaMOhnoSHashiguchiT 2009 Measles virus receptors. Curr Top Microbiol Immunol 329 13 30
18. DorigREMarcilAChopraARichardsonCD 1993 The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 75 295 305
19. NanicheDVarior-KrishnanGCervoniFWildTFRossiB 1993 Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J Virol 67 6025 6032
20. KemperCAtkinsonJP 2009 Measles virus and CD46. Curr Top Microbiol Immunol 329 31 57
21. LecouturierVFayolleJCaballeroMCarabanaJCelmaML 1996 Identification of two amino acids in the hemagglutinin glycoprotein of measles virus (MV) that govern hemadsorption, HeLa cell fusion, and CD46 downregulation: phenotypic markers that differentiate vaccine and wild-type MV strains. J Virol 70 4200 4204
22. HsuECSarangiFIorioCSidhuMSUdemSA 1998 A single amino acid change in the hemagglutinin protein of measles virus determines its ability to bind CD46 and reveals another receptor on marmoset B cells. J Virol 72 2905 2916
23. TaharaMTakedaMSekiFHashiguchiTYanagiY 2007 Multiple amino acid substitutions in hemagglutinin are necessary for wild-type measles virus to acquire the ability to use receptor CD46 efficiently. J Virol 81 2564 2572
24. KobuneFSakataHSugiuraA 1990 Marmoset lymphoblastoid cells as a sensitive host for isolation of measles virus. J Virol 64 700 705
25. ShibaharaKHottaHKatayamaYHommaM 1994 Increased binding activity of measles virus to monkey red blood cells after long-term passage in Vero cell cultures. J Gen Virol 75 Pt 12 3511 3516
26. BartzRFirschingRRimaBter MeulenVSchneider-SchauliesJ 1998 Differential receptor usage by measles virus strains. J Gen Virol 79 Pt 5 1015 1025
27. BucklandRWildTF 1997 Is CD46 the cellular receptor for measles virus? Virus Res 48 1 9
28. TatsuoHOnoNTanakaKYanagiY 2000 SLAM (CDw150) is a cellular receptor for measles virus. Nature 406 893 897
29. HsuECIorioCSarangiFKhineAARichardsonCD 2001 CDw150(SLAM) is a receptor for a lymphotropic strain of measles virus and may account for the immunosuppressive properties of this virus. Virology 279 9 21
30. ErlenhoeferCWurzerWJLofflerSSchneider-SchauliesSter MeulenV 2001 CD150 (SLAM) is a receptor for measles virus but is not involved in viral contact-mediated proliferation inhibition. J Virol 75 4499 4505
31. SchwartzbergPLMuellerKLQiHCannonsJL 2009 SLAM receptors and SAP influence lymphocyte interactions, development and function. Nat Rev Immunol 9 39 46
32. de SwartRLLudlowMde WitteLYanagiYvan AmerongenG 2007 Predominant infection of CD150+ lymphocytes and dendritic cells during measles virus infection of macaques. PLoS Pathog 3 e178
33. LeonardVHSinnPLHodgeGMiestTDevauxP 2008 Measles virus blind to its epithelial cell receptor remains virulent in rhesus monkeys but cannot cross the airway epithelium and is not shed. J Clin Invest 118 2448 2458
34. LudlowMRennickLJSarlangSSkibinskiGMcQuaidS 2010 Wild-type measles virus infection of primary epithelial cells occurs via the basolateral surface without syncytium formation or release of infectious virus. J Gen Virol 91 971 979
35. LemonKde VriesRDMesmanAWMcQuaidSvan AmerongenG 2011 Early target cells of measles virus after aerosol infection of non-human primates. PLoS Pathog 7 e1001263
36. CraigheadJE 2000 Pathology and pathogenesis of human viral disease. CraigheadJE Rubeola (Measles) Philadelphia Elsevier Inc 397 410
37. SakaguchiMYoshikawaYYamanouchiKSataTNagashimaK 1986 Growth of measles virus in epithelial and lymphoid tissues of cynomolgus monkeys. Microbiol Immunol 30 1067 1073
38. GriffinDE 2001 Measles Virus. Fields' Virology New York Lippincott, Williams, and Wilkins 1401 1442 Knipe D.M., editor in chief
39. TakeuchiKMiyajimaNNagataNTakedaMTashiroM 2003 Wild-type measles virus induces large syncytium formation in primary human small airway epithelial cells by a SLAM(CD150)-independent mechanism. Virus Res 94 11 16
40. SinnPLWilliamsGVongpunsawadSCattaneoRMcCrayPBJr 2002 Measles virus preferentially transduces the basolateral surface of well-differentiated human airway epithelia. J Virol 76 2403 2409
41. TaharaMTakedaMShiroganeYHashiguchiTOhnoS 2008 Measles virus infects both polarized epithelial and immune cells by using distinctive receptor-binding sites on its hemagglutinin. J Virol 82 4630 4637
42. TakedaM 2008 Measles virus breaks through epithelial cell barriers to achieve transmission. J Clin Invest 118 2386 2389
43. MaisnerAKlenkHHerrlerG 1998 Polarized budding of measles virus is not determined by viral surface glycoproteins. J Virol 72 5276 5278
44. HashimotoKOnoNTatsuoHMinagawaHTakedaM 2002 SLAM (CD150)-independent measles virus entry as revealed by recombinant virus expressing green fluorescent protein. J Virol 76 6743 6749
45. ShiroganeYTakedaMTaharaMIkegameSNakamuraT 2010 Epithelial-mesenchymal transition abolishes the susceptibility of polarized epithelial cell lines to measles virus. J Biol Chem 285 20882 20890
46. TakedaMTaharaMHashiguchiTSatoTAJinnouchiF 2007 A human lung carcinoma cell line supports efficient measles virus growth and syncytium formation via a SLAM- and CD46-independent mechanism. J Virol 81 12091 12096
47. BartonESForrestJCConnollyJLChappellJDLiuY 2001 Junction adhesion molecule is a receptor for reovirus. Cell 104 441 451
48. GeraghtyRJKrummenacherCCohenGHEisenbergRJSpearPG 1998 Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 280 1618 1620
49. CoyneCBShenLTurnerJRBergelsonJM 2007 Coxsackievirus entry across epithelial tight junctions requires occludin and the small GTPases Rab34 and Rab5. Cell Host Microbe 2 181 192
50. PlossAEvansMJGaysinskayaVAPanisMYouH 2009 Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457 882 886
51. HsuECSabatinosSHoedemaekerFJRoseDRRichardsonCD 1999 Use of site-specific mutagenesis and monoclonal antibodies to map regions of CD46 that interact with measles virus H protein. Virology 258 314 326
52. VongpunsawadSOezgunNBraunWCattaneoR 2004 Selectively receptor-blind measles viruses: Identification of residues necessary for SLAM- or CD46-induced fusion and their localization on a new hemagglutinin structural model. J Virol 78 302 313
53. HsuECDorigRESarangiFMarcilAIorioC 1997 Artificial mutations and natural variations in the CD46 molecules from human and monkey cells define regions important for measles virus binding. J Virol 71 6144 6154
54. RileyRCTannenbaumPLAbbottDHAtkinsonJP 2002 Cutting edge: inhibiting measles virus infection but promoting reproduction: an explanation for splicing and tissue-specific expression of CD46. J Immunol 169 5405 5409
55. BonaparteMIDimitrovASBossartKNCrameriGMungallBA 2005 Ephrin-B2 ligand is a functional receptor for Hendra virus and Nipah virus. Proc Natl Acad Sci U S A 102 10652 10657
56. NanicheDWildTFRabourdin-CombeCGerlierD 1993 Measles virus haemagglutinin induces down-regulation of gp57/67, a molecule involved in virus binding. J Gen Virol 74 Pt 6 1073 1079
57. Schneider-SchauliesJDunsterLMKobuneFRimaBter MeulenV 1995 Differential downregulation of CD46 by measles virus strains. J Virol 69 7257 7259
58. BartzRBrinckmannUDunsterLMRimaBTer MeulenV 1996 Mapping amino acids of the measles virus hemagglutinin responsible for receptor (CD46) downregulation. Virology 224 334 337
59. TanakaKMinagawaHXieMFYanagiY 2002 The measles virus hemagglutinin downregulates the cellular receptor SLAM (CD150). Arch Virol 147 195 203
60. WelsteadGGHsuECIorioCBolotinSRichardsonCD 2004 Mechanism of CD150 (SLAM) down regulation from the host cell surface by measles virus hemagglutinin protein. J Virol 78 9666 9674
61. ReymondNFabreSLecocqEAdelaideJDubreuilP 2001 Nectin4/PRR4, a new afadin-associated member of the nectin family that trans-interacts with nectin1/PRR1 through V domain interaction. J Biol Chem 276 43205 43215
62. DeryckeMSPambuccianSEGilksCBKallogerSEGhidoucheA 2010 Nectin 4 overexpression in ovarian cancer tissues and serum: potential role as a serum biomarker. Am J Clin Pathol 134 835 845
63. TakanoAIshikawaNNishinoRMasudaKYasuiW 2009 Identification of nectin-4 oncoprotein as a diagnostic and therapeutic target for lung cancer. Cancer Res 69 6694 6703
64. Fabre-LafaySGarrido-UrbaniSReymondNGoncalvesADubreuilP 2005 Nectin-4, a new serological breast cancer marker, is a substrate for tumor necrosis factor-alpha-converting enzyme (TACE)/ADAM-17. J Biol Chem 280 19543 19550
65. MengWTakeichiM 2009 Adherens junction: molecular architecture and regulation. Cold Spring Harb Perspect Biol 1 a002899
66. MendelsohnCLWimmerERacanielloVR 1989 Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 56 855 865
67. LopezMCocchiFMenottiLAvitabileEDubreuilP 2000 Nectin2alpha (PRR2alpha or HveB) and nectin2delta are low-efficiency mediators for entry of herpes simplex virus mutants carrying the Leu25Pro substitution in glycoprotein D. J Virol 74 1267 1274
68. TaylorJMLinESusmarskiNYoonMZagoA 2007 Alternative entry receptors for herpes simplex virus and their roles in disease. Cell Host Microbe 2 19 28
69. YuZAdusumilliPSEisenbergDPDarrEGhosseinRA 2007 Nectin-1 expression by squamous cell carcinoma is a predictor of herpes oncolytic sensitivity. Mol Ther 15 103 113
70. von MesslingVMilosevicDCattaneoR 2004 Tropism illuminated: lymphocyte-based pathways blazed by lethal morbillivirus through the host immune system. Proc Natl Acad Sci U S A 101 14216 14221
71. Fabre-LafaySMonvilleFGarrido-UrbaniSBerruyer-PouyetCGinestierC 2007 Nectin-4 is a new histological and serological tumor associated marker for breast cancer. BMC Cancer 7 73
72. BlumingAZZieglerJL 1971 Regression of Burkitt's lymphoma in association with measles infection. Lancet 2 105 106
73. MotaHC 1973 Infantile Hodgkin's disease: remission after measles. Br Med J 2 421
74. TaqiAMAbdurrahmanMBYakubuAMFlemingAF 1981 Regression of Hodgkin's disease after measles. Lancet 1 1112
75. ZygiertZ 1971 Hodgkin's disease: remissions after measles. Lancet 1 593
76. RichardsonCDScheidAChoppinPW 1980 Specific inhibition of paramyxovirus and myxovirus replication by oligopeptides with amino acid sequences similar to those at the N-termini of the F1 or HA2 viral polypeptides. Virology 105 205 222
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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