Establishment of Papillomavirus Infection is Enhanced by Promyelocytic Leukemia Protein (PML) Expression

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2004 Sep 24

PMID 15383670

Citations 151

Authors

Patricia M Day

Carl C Baker

Douglas R Lowy

John T Schiller

Affiliations

Soon will be listed here.

Abstract

Previous studies have suggested that most papillomaviruses enter the host cell via clathrin-dependent receptor-mediated endocytosis but have not addressed later steps in viral entry. To examine these events, we followed the localization of L2 and packaged DNA after entry of infectious virions or L1/L2 pseudovirions. Confocal microscopic analyses of HeLa cells showed a time-dependent uncoating of capsids in cytoplasmic vesicles and the accumulation of both L2 and viral DNA at distinct nuclear domains identified as nuclear domain 10 (ND10). Both L2 and the pseudogenome had a punctate distribution and localized to ND10 in promyelocytic leukemia protein (PML)-expressing cells, whereas L2 had a diffuse nuclear distribution in PML-/- cells. The number of pseudovirus-infected cells was an order of magnitude higher in the PML+ cells compared with the PML-/- cells, and viral genome transcription after infection with authentic bovine papillomavirus virions was similarly elevated in PML+ cells. The results identify a role for PML in the enhancement of viral infectivity in the early part of the life cycle. We propose a model in which L2 chaperones the viral genome to ND10 to efficiently initiate viral transcription.

Citing Articles

The Natural History of Cervical Cancer and the Case for MicroRNAs: Is Human Papillomavirus Infection the Whole Story?.

Palomino-Vizcaino G, Banuelos-Villegas E, Alvarez-Salas L Int J Mol Sci. 2024; 25(23.

PMID: 39684702 PMC: 11641362. DOI: 10.3390/ijms252312991.

HPV16 entry requires dynein for minus-end transport and utilizes kinesin Kif11 for plus-end transport along microtubules during mitosis.

Keiffer T, DiGiuseppe S, Guion L, Bienkowska-Haba M, Zwolinska K, Siddiqa A J Virol. 2024; 99(1):e0093724.

PMID: 39629998 PMC: 11784366. DOI: 10.1128/jvi.00937-24.

The role of HR-HPV integration in the progression of premalignant lesions into different cancer types.

Catalan-Castorena O, Garibay-Cerdenares O, Illades-Aguiar B, Rodriguez-Ruiz H, Zubillaga-Guerrero M, Leyva-Vazquez M Heliyon. 2024; 10(15):e34999.

PMID: 39170128 PMC: 11336306. DOI: 10.1016/j.heliyon.2024.e34999.

Epidemiology, Molecular Pathogenesis, Immuno-Pathogenesis, Immune Escape Mechanisms and Vaccine Evaluation for HPV-Associated Carcinogenesis.

Jain M, Yadav D, Jarouliya U, Chavda V, Yadav A, Chaurasia B Pathogens. 2023; 12(12).

PMID: 38133265 PMC: 10745624. DOI: 10.3390/pathogens12121380.

The interactions between PML nuclear bodies and small and medium size DNA viruses.

Ryabchenko B, Sroller V, Hornikova L, Lovtsov A, Forstova J, Huerfano S Virol J. 2023; 20(1):82.

PMID: 37127643 PMC: 10152602. DOI: 10.1186/s12985-023-02049-4.

References

Bousarghin L, Touze A, Sizaret P, Coursaget P . Human papillomavirus types 16, 31, and 58 use different endocytosis pathways to enter cells. J Virol. 2003; 77(6):3846-50. PMC: 149499. DOI: 10.1128/jvi.77.6.3846-3850.2003. View

Sourvinos G, Everett R . Visualization of parental HSV-1 genomes and replication compartments in association with ND10 in live infected cells. EMBO J. 2002; 21(18):4989-97. PMC: 126275. DOI: 10.1093/emboj/cdf458. View

Tang Q, Li L, Ishov A, Revol V, Epstein A, Maul G . Determination of minimum herpes simplex virus type 1 components necessary to localize transcriptionally active DNA to ND10. J Virol. 2003; 77(10):5821-8. PMC: 154000. DOI: 10.1128/jvi.77.10.5821-5828.2003. View

Culp T, Christensen N . Quantitative RT-PCR assay for HPV infection in cultured cells. J Virol Methods. 2003; 111(2):135-44. DOI: 10.1016/s0166-0934(03)00170-8. View

Rabe B, Vlachou A, Pante N, Helenius A, Kann M . Nuclear import of hepatitis B virus capsids and release of the viral genome. Proc Natl Acad Sci U S A. 2003; 100(17):9849-54. PMC: 187862. DOI: 10.1073/pnas.1730940100. View

Selinka H, Giroglou T, Nowak T, Christensen N, Sapp M . Further evidence that papillomavirus capsids exist in two distinct conformations. J Virol. 2003; 77(24):12961-7. PMC: 296061. DOI: 10.1128/jvi.77.24.12961-12967.2003. View

Buck C, Pastrana D, Lowy D, Schiller J . Efficient intracellular assembly of papillomaviral vectors. J Virol. 2003; 78(2):751-7. PMC: 368835. DOI: 10.1128/jvi.78.2.751-757.2004. View

Culp T, Christensen N . Kinetics of in vitro adsorption and entry of papillomavirus virions. Virology. 2004; 319(1):152-61. DOI: 10.1016/j.virol.2003.11.004. View

Wang J, Shiels C, Sasieni P, Wu P, Islam S, Freemont P . Promyelocytic leukemia nuclear bodies associate with transcriptionally active genomic regions. J Cell Biol. 2004; 164(4):515-26. PMC: 2171989. DOI: 10.1083/jcb.200305142. View

10.

Pastrana D, Buck C, Pang Y, Thompson C, Castle P, FitzGerald P . Reactivity of human sera in a sensitive, high-throughput pseudovirus-based papillomavirus neutralization assay for HPV16 and HPV18. Virology. 2004; 321(2):205-16. DOI: 10.1016/j.virol.2003.12.027. View

11.

Tashiro S, Muto A, Tanimoto K, Tsuchiya H, Suzuki H, Hoshino H . Repression of PML nuclear body-associated transcription by oxidative stress-activated Bach2. Mol Cell Biol. 2004; 24(8):3473-84. PMC: 381671. DOI: 10.1128/MCB.24.8.3473-3484.2004. View

12.

Yang Y, Okayama H, Howley P . Bovine papillomavirus contains multiple transforming genes. Proc Natl Acad Sci U S A. 1985; 82(4):1030-4. PMC: 397187. DOI: 10.1073/pnas.82.4.1030. View

13.

Clever J, Yamada M, Kasamatsu H . Import of simian virus 40 virions through nuclear pore complexes. Proc Natl Acad Sci U S A. 1991; 88(16):7333-7. PMC: 52289. DOI: 10.1073/pnas.88.16.7333. View

14.

Fagioli M, Alcalay M, Pandolfi P, Venturini L, Mencarelli A, Simeone A . Alternative splicing of PML transcripts predicts coexpression of several carboxy-terminally different protein isoforms. Oncogene. 1992; 7(6):1083-91. View

15.

Guldner H, Szostecki C, Grotzinger T, Will H . IFN enhance expression of Sp100, an autoantigen in primary biliary cirrhosis. J Immunol. 1992; 149(12):4067-73. View

16.

Zhou J, Stenzel D, Sun X, Frazer I . Synthesis and assembly of infectious bovine papillomavirus particles in vitro. J Gen Virol. 1993; 74 ( Pt 4):763-8. DOI: 10.1099/0022-1317-74-4-763. View

17.

Koken M, Guillemin M, Viron A, Stuurman N, de Jong L, Szostecki C . The t(15;17) translocation alters a nuclear body in a retinoic acid-reversible fashion. EMBO J. 1994; 13(5):1073-83. PMC: 394915. DOI: 10.1002/j.1460-2075.1994.tb06356.x. View

18.

Maul G, Everett R . The nuclear location of PML, a cellular member of the C3HC4 zinc-binding domain protein family, is rearranged during herpes simplex virus infection by the C3HC4 viral protein ICP0. J Gen Virol. 1994; 75 ( Pt 6):1223-33. DOI: 10.1099/0022-1317-75-6-1223. View

19.

Christensen N, Cladel N, Reed C . Postattachment neutralization of papillomaviruses by monoclonal and polyclonal antibodies. Virology. 1995; 207(1):136-42. DOI: 10.1006/viro.1995.1059. View

20.

Korioth F, Gieffers C, Maul G, Frey J . Molecular characterization of NDP52, a novel protein of the nuclear domain 10, which is redistributed upon virus infection and interferon treatment. J Cell Biol. 1995; 130(1):1-13. PMC: 2120522. DOI: 10.1083/jcb.130.1.1. View