-
Články
- Časopisy
- Kurzy
- Témy
- Kongresy
- Videa
- Podcasty
Degradation of Human PDZ-Proteins by Human Alphapapillomaviruses Represents an Evolutionary Adaptation to a Novel Cellular Niche
It is thought that the ability to degrade PDZ domain containing proteins is a hallmark of oncogenic papillomaviruses. However, since papillomaviruses did not evolve to be oncogenic, this hypothesis does not address the evolutionary importance of this phenotype. The present manuscript attempts to address whether HPV induced degradation of PDZ containing proteins is associated with oncogenic potential as determined by the clinical/epidemiological empirical cancer risk. Using Bayesian approaches to model trait evolution we show that it is highly unlikely for a virus to become oncogenic without first acquiring the ability to degrade PDZ proteins. Furthermore, the ability to degrade PDZ proteins allowed ancestral viruses to colonize a new cellular niche. However, in order to thrive in this new environment, these ancestral viruses had to acquire additional functions. We hypothesize that some of these additional phenotypes lead to oncogenicity. Importantly, our study illustrates the power of combining epidemiological, biochemical and evolutionary data with phylogenetic analysis in attempting to understand the relative role of specific pathogen phenotypes with host pathogenesis.
Vyšlo v časopise: Degradation of Human PDZ-Proteins by Human Alphapapillomaviruses Represents an Evolutionary Adaptation to a Novel Cellular Niche. PLoS Pathog 11(6): e32767. doi:10.1371/journal.ppat.1004980
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004980Souhrn
It is thought that the ability to degrade PDZ domain containing proteins is a hallmark of oncogenic papillomaviruses. However, since papillomaviruses did not evolve to be oncogenic, this hypothesis does not address the evolutionary importance of this phenotype. The present manuscript attempts to address whether HPV induced degradation of PDZ containing proteins is associated with oncogenic potential as determined by the clinical/epidemiological empirical cancer risk. Using Bayesian approaches to model trait evolution we show that it is highly unlikely for a virus to become oncogenic without first acquiring the ability to degrade PDZ proteins. Furthermore, the ability to degrade PDZ proteins allowed ancestral viruses to colonize a new cellular niche. However, in order to thrive in this new environment, these ancestral viruses had to acquire additional functions. We hypothesize that some of these additional phenotypes lead to oncogenicity. Importantly, our study illustrates the power of combining epidemiological, biochemical and evolutionary data with phylogenetic analysis in attempting to understand the relative role of specific pathogen phenotypes with host pathogenesis.
Zdroje
1. de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H (2004) Classification of papillomaviruses. Virology 324 : 17–27. 15183049
2. Bernard HU, Burk RD, Chen Z, van Doorslaer K, Zur Hausen H, et al. (2010) Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 401 : 70–79. doi: 10.1016/j.virol.2010.02.002 20206957
3. Schiffman M, Castle PE, Jeronimo J, Rodriguez AC, Wacholder S (2007) Human papillomavirus and cervical cancer. Lancet 370 : 890–907. 17826171
4. Bodily J, Laimins LA (2011) Persistence of human papillomavirus infection: keys to malignant progression. Trends Microbiol 19 : 33–39. doi: 10.1016/j.tim.2010.10.002 21050765
5. Burk RD, Chen Z, Van Doorslaer K (2009) Human papillomaviruses: genetic basis of carcinogenicity. Public Health Genomics 12 : 281–290. doi: 10.1159/000214919 19684441
6. Schiffman M, Herrero R, DeSalle R, Hildesheim A, Wacholder S, et al. (2005) The carcinogenicity of human papillomavirus types reflects viral evolution. Virology 337 : 76–84. 15914222
7. IARC (2012) IARC Monographs on the Evaluation of Carcinogenic Risks to Humans Volume 100B: A Review of Human Carcinogens: Biological Agents.
8. Fu L, Van Doorslaer K, Chen Z, Ristriani T, Masson M, et al. (2010) Degradation of p53 by Human Alphapapillomavirus E6 Proteins Shows a Stronger Correlation with Phylogeny than Oncogenicity. PLoS ONE 5: e12816. doi: 10.1371/journal.pone.0012816 20862247
9. Van Doorslaer K, Burk RD (2012) Association between hTERT activation by HPV E6 proteins and oncogenic risk. Virology 433 : 216–219. doi: 10.1016/j.virol.2012.08.006 22925336
10. Van Doorslaer K, Burk RD (2010) Evolution of Human Papillomavirus Carcinogenicity. Advances in Virus Research 77 : 41–62. doi: 10.1016/B978-0-12-385034-8.00002-8 20951869
11. Moody CA, Laimins LA (2010) Human papillomavirus oncoproteins: pathways to transformation. Nat Rev Cancer 10 : 550–560. doi: 10.1038/nrc2886 20592731
12. McLaughlin-Drubin ME, Munger K (2009) Oncogenic activities of human papillomaviruses. Virus Res 143 : 195–208. doi: 10.1016/j.virusres.2009.06.008 19540281
13. Klingelhutz AJ, Roman A (2012) Cellular transformation by human papillomaviruses: Lessons learned by comparing high - and low-risk viruses. Virology 424 : 77–98. doi: 10.1016/j.virol.2011.12.018 22284986
14. White EA, Kramer RE, Tan MJ, Hayes SD, Harper JW, et al. (2012) Comprehensive Analysis of Host Cellular Interactions with Human Papillomavirus E6 Proteins Identifies New E6 Binding Partners and Reflects Viral Diversity. J Virol.
15. Vande Pol SB, Klingelhutz AJ (2013) Papillomavirus E6 oncoproteins. Virology 445 : 115–137. doi: 10.1016/j.virol.2013.04.026 23711382
16. Roman A, Munger K (2013) The papillomavirus E7 proteins. Virology 445 : 138–168. doi: 10.1016/j.virol.2013.04.013 23731972
17. Pim D, Bergant M, Boon SS, Ganti K, Kranjec C, et al. (2012) Human papillomaviruses and the specificity of PDZ domain targeting. FEBS J 279 : 3530–3537. doi: 10.1111/j.1742-4658.2012.08709.x 22805590
18. Doorbar J (2006) Molecular biology of human papillomavirus infection and cervical cancer. Clin Sci (Lond) 110 : 525–541. 16597322
19. James MA, Lee JH, Klingelhutz AJ (2006) Human papillomavirus type 16 E6 activates NF-kappaB, induces cIAP-2 expression, and protects against apoptosis in a PDZ binding motif-dependent manner. J Virol 80 : 5301–5307. 16699010
20. Lee C, Laimins LA (2004) Role of the PDZ domain-binding motif of the oncoprotein E6 in the pathogenesis of human papillomavirus type 31. J Virol 78 : 12366–12377. 15507623
21. Massimi P, Gammoh N, Thomas M, Banks L (2004) HPV E6 specifically targets different cellular pools of its PDZ domain-containing tumour suppressor substrates for proteasome-mediated degradation. Oncogene 23 : 8033–8039. 15378012
22. Songyang Z, Fanning AS, Fu C, Xu J, Marfatia SM, et al. (1997) Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275 : 73–77. 8974395
23. Fournane S, Charbonnier S, Chapelle A, Kieffer B, Orfanoudakis G, et al. (2011) Surface plasmon resonance analysis of the binding of high-risk mucosal HPV E6 oncoproteins to the PDZ1 domain of the tight junction protein MAGI-1. J Mol Recognit 24 : 511–523. doi: 10.1002/jmr.1056 20842623
24. Kranjec C, Massimi P, Banks L (2014) Restoration of MAGI-1 Expression in Human Papillomavirus-Positive Tumor Cells Induces Cell Growth Arrest and Apoptosis. J Virol 88 : 7155–7169. doi: 10.1128/JVI.03247-13 24696483
25. Thomas M, Glaunsinger B, Pim D, Javier R, Banks L (2001) HPV E6 and MAGUK protein interactions: determination of the molecular basis for specific protein recognition and degradation. Oncogene 20 : 5431–5439. 11571640
26. Muench P, Hiller T, Probst S, Florea AM, Stubenrauch F, et al. (2009) Binding of PDZ proteins to HPV E6 proteins does neither correlate with epidemiological risk classification nor with the immortalization of foreskin keratinocytes. Virology 387 : 380–387. doi: 10.1016/j.virol.2009.02.018 19285702
27. Thomas M, Narayan N, Pim D, Tomaic V, Massimi P, et al. (2008) Human papillomaviruses, cervical cancer and cell polarity. Oncogene 27 : 7018–7030. doi: 10.1038/onc.2008.351 19029942
28. Dobzhansky T (1973) Nothing in biology makes sense except in the light of evolution. The American Biology Teacher 35 : 125–129.
29. Auersperg N (1964) Long-Term Cultivation of Hypodiploid Human Tumor Cells. J Natl Cancer Inst 32 : 135–163. 14114965
30. Yee C, Krishnan-Hewlett I, Baker CC, Schlegel R, Howley PM (1985) Presence and expression of human papillomavirus sequences in human cervical carcinoma cell lines. Am J Pathol 119 : 361–366. 2990217
31. Van Doorslaer K, Tan Q, Xirasagar S, Bandaru S, Gopalan V, et al. (2012) The Papillomavirus Episteme: a central resource for papillomavirus sequence data and analysis. Nucleic Acids Res.
32. Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30 : 3059–3066. 12136088
33. Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27 : 221–224. doi: 10.1093/molbev/msp259 19854763
34. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294 : 2310–2314. 11743192
35. Huelsenbeck JP, Bollback JP (2001) Empirical and hierarchical Bayesian estimation of ancestral states. Syst Biol 50 : 351–366. 12116580
36. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25 : 1253–1256. doi: 10.1093/molbev/msn083 18397919
37. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52 : 696–704. 14530136
38. Nylander JA, Wilgenbusch JC, Warren DL, Swofford DL (2008) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24 : 581–583. 17766271
39. Pagel M, Meade A (2006) Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am Nat 167 : 808–825. doi: 10.1086/503444 16685633
40. Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, et al. (2009) A review of human carcinogens—Part B: biological agents. Lancet Oncol 10 : 321–322. 19350698
41. Schiffman M, Clifford G, Buonaguro FM (2009) Classification of weakly carcinogenic human papillomavirus types: addressing the limits of epidemiology at the borderline. Infect Agent Cancer 4 : 8. doi: 10.1186/1750-9378-4-8 19486508
42. Beuming T, Skrabanek L, Niv MY, Mukherjee P, Weinstein H (2005) PDZBase: a protein-protein interaction database for PDZ-domains. Bioinformatics 21 : 827–828. 15513994
43. Ainsworth J, Thomas M, Banks L, Coutlee F, Matlashewski G (2008) Comparison of p53 and the PDZ domain containing protein MAGI-3 regulation by the E6 protein from high-risk human papillomaviruses. Virol J 5 : 67. doi: 10.1186/1743-422X-5-67 18518978
44. Massimi P, Shai A, Lambert P, Banks L (2008) HPV E6 degradation of p53 and PDZ containing substrates in an E6AP null background. Oncogene 27 : 1800–1804. 17934525
45. Currie TE, Greenhill SJ, Gray RD, Hasegawa T, Mace R (2010) Rise and fall of political complexity in island South-East Asia and the Pacific. Nature 467 : 801–804. doi: 10.1038/nature09461 20944739
46. Chi CN, Bach A, Engstrom A, Stromgaard K, Lundstrom P, et al. (2011) Biophysical characterization of the complex between human papillomavirus E6 protein and synapse-associated protein 97. J Biol Chem 286 : 3597–3606. doi: 10.1074/jbc.M110.190264 21113079
47. Thomas M, Massimi P, Navarro C, Borg JP, Banks L (2005) The hScrib/Dlg apico-basal control complex is differentially targeted by HPV-16 and HPV-18 E6 proteins. Oncogene 24 : 6222–6230. 16103886
48. Boon SS, Tomaic V, Thomas M, Roberts S, Banks L (2015) Cancer-causing human papillomavirus E6 proteins display major differences in the phospho-regulation of their PDZ interactions. J Virol 89 : 1579–1586. doi: 10.1128/JVI.01961-14 25410862
49. Fournane S, Charbonnier S, Chapelle A, Kieffer B, Orfanoudakis G, et al. (2010) Surface plasmon resonance analysis of the binding of high-risk mucosal HPV E6 oncoproteins to the PDZ1 domain of the tight junction protein MAGI-1. J Mol Recognit.
50. Hsu EC, Lin YC, Hung CS, Huang CJ, Lee MY, et al. (2007) Suppression of hepatitis B viral gene expression by protein-tyrosine phosphatase PTPN3. J Biomed Sci 14 : 731–744. 17588219
51. Banks L, Pim D, Thomas M (2012) Human tumour viruses and the deregulation of cell polarity in cancer. Nat Rev Cancer 12 : 877–886. doi: 10.1038/nrc3400 23175122
52. Brimer N, Lyons C, Vande Pol SB (2007) Association of E6AP (UBE3A) with human papillomavirus type 11 E6 protein. Virology 358 : 303–310. 17023019
53. Brimer N, Vande Pol SB (2014) Papillomavirus E6 PDZ interactions can be replaced by repression of p53 to promote episomal human papillomavirus genome maintenance. J Virol 88 : 3027–3030. doi: 10.1128/JVI.02360-13 24352452
54. Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci U S A 95 : 5857–5864. 9600884
55. Letunic I, Doerks T, Bork P (2009) SMART 6: recent updates and new developments. Nucleic Acids Res 37: D229–232. doi: 10.1093/nar/gkn808 18978020
Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium
Článek Clearance of Pneumococcal Colonization in Infants Is Delayed through Altered Macrophage TraffickingČlánek An Model of Latency and Reactivation of Varicella Zoster Virus in Human Stem Cell-Derived NeuronsČlánek Protective mAbs and Cross-Reactive mAbs Raised by Immunization with Engineered Marburg Virus GPsČlánek Specific Cell Targeting Therapy Bypasses Drug Resistance Mechanisms in African TrypanosomiasisČlánek Peptidoglycan Branched Stem Peptides Contribute to Virulence by Inhibiting Pneumolysin ReleaseČlánek HIV Latency Is Established Directly and Early in Both Resting and Activated Primary CD4 T CellsČlánek Sequence-Specific Fidelity Alterations Associated with West Nile Virus Attenuation in Mosquitoes
Článok vyšiel v časopisePLOS Pathogens
Najčítanejšie tento týždeň
2015 Číslo 6- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
-
Všetky články tohto čísla
- Introducing “Research Matters”
- Exploring Host–Pathogen Interactions through Biological Control
- Analysis of Bottlenecks in Experimental Models of Infection
- Expected and Unexpected Features of the Newly Discovered Bat Influenza A-like Viruses
- Clearance of Pneumococcal Colonization in Infants Is Delayed through Altered Macrophage Trafficking
- Recombinant Murine Gamma Herpesvirus 68 Carrying KSHV G Protein-Coupled Receptor Induces Angiogenic Lesions in Mice
- TRIM30α Is a Negative-Feedback Regulator of the Intracellular DNA and DNA Virus-Triggered Response by Targeting STING
- Targeting Human Transmission Biology for Malaria Elimination
- Two Cdc2 Kinase Genes with Distinct Functions in Vegetative and Infectious Hyphae in
- An Model of Latency and Reactivation of Varicella Zoster Virus in Human Stem Cell-Derived Neurons
- Protective mAbs and Cross-Reactive mAbs Raised by Immunization with Engineered Marburg Virus GPs
- Virulence Factors of Induce Both the Unfolded Protein and Integrated Stress Responses in Airway Epithelial Cells
- Peptide-MHC-I from Endogenous Antigen Outnumber Those from Exogenous Antigen, Irrespective of APC Phenotype or Activation
- Specific Cell Targeting Therapy Bypasses Drug Resistance Mechanisms in African Trypanosomiasis
- An Ultrasensitive Mechanism Regulates Influenza Virus-Induced Inflammation
- The Role of Human Transportation Networks in Mediating the Genetic Structure of Seasonal Influenza in the United States
- Host Delivery of Favorite Meals for Intracellular Pathogens
- Complement-Opsonized HIV-1 Overcomes Restriction in Dendritic Cells
- Inter-Seasonal Influenza is Characterized by Extended Virus Transmission and Persistence
- A Critical Role for CLSP2 in the Modulation of Antifungal Immune Response in Mosquitoes
- Twilight, a Novel Circadian-Regulated Gene, Integrates Phototropism with Nutrient and Redox Homeostasis during Fungal Development
- Surface-Associated Lipoproteins Link Virulence to Colitogenic Activity in IL-10-Deficient Mice Independent of Their Expression Levels
- Latent Membrane Protein LMP2A Impairs Recognition of EBV-Infected Cells by CD8+ T Cells
- Bank Vole Prion Protein As an Apparently Universal Substrate for RT-QuIC-Based Detection and Discrimination of Prion Strains
- Neuronal Subtype and Satellite Cell Tropism Are Determinants of Varicella-Zoster Virus Virulence in Human Dorsal Root Ganglia Xenografts
- Molecular Basis for the Selective Inhibition of Respiratory Syncytial Virus RNA Polymerase by 2'-Fluoro-4'-Chloromethyl-Cytidine Triphosphate
- Structure of the Virulence Factor, SidC Reveals a Unique PI(4)P-Specific Binding Domain Essential for Its Targeting to the Bacterial Phagosome
- Activated Brain Endothelial Cells Cross-Present Malaria Antigen
- Fungal Morphology, Iron Homeostasis, and Lipid Metabolism Regulated by a GATA Transcription Factor in
- Peptidoglycan Branched Stem Peptides Contribute to Virulence by Inhibiting Pneumolysin Release
- A Macrophage Subversion Factor Is Shared by Intracellular and Extracellular Pathogens
- A Novel AT-Rich DNA Recognition Mechanism for Bacterial Xenogeneic Silencer MvaT
- Reovirus FAST Proteins Drive Pore Formation and Syncytiogenesis Using a Novel Helix-Loop-Helix Fusion-Inducing Lipid Packing Sensor
- The Role of ExoS in Dissemination of during Pneumonia
- IRF-5-Mediated Inflammation Limits CD8 T Cell Expansion by Inducing HIF-1α and Impairing Dendritic Cell Functions during Infection
- Discordant Impact of HLA on Viral Replicative Capacity and Disease Progression in Pediatric and Adult HIV Infection
- Crystal Structure of USP7 Ubiquitin-like Domains with an ICP0 Peptide Reveals a Novel Mechanism Used by Viral and Cellular Proteins to Target USP7
- HIV Latency Is Established Directly and Early in Both Resting and Activated Primary CD4 T Cells
- HPV16 Down-Regulates the Insulin-Like Growth Factor Binding Protein 2 to Promote Epithelial Invasion in Organotypic Cultures
- The νSaα Specific Lipoprotein Like Cluster () of . USA300 Contributes to Immune Stimulation and Invasion in Human Cells
- RSV-Induced H3K4 Demethylase KDM5B Leads to Regulation of Dendritic Cell-Derived Innate Cytokines and Exacerbates Pathogenesis
- Leukocidin A/B (LukAB) Kills Human Monocytes via Host NLRP3 and ASC when Extracellular, but Not Intracellular
- Border Patrol Gone Awry: Lung NKT Cell Activation by Exacerbates Tularemia-Like Disease
- The Curious Road from Basic Pathogen Research to Clinical Translation
- From Cell and Organismal Biology to Drugs
- Adenovirus Tales: From the Cell Surface to the Nuclear Pore Complex
- A 21st Century Perspective of Poliovirus Replication
- Is Development of a Vaccine against Feasible?
- Waterborne Viruses: A Barrier to Safe Drinking Water
- Battling Phages: How Bacteria Defend against Viral Attack
- Archaea in and on the Human Body: Health Implications and Future Directions
- Degradation of Human PDZ-Proteins by Human Alphapapillomaviruses Represents an Evolutionary Adaptation to a Novel Cellular Niche
- Natural Variants of the KPC-2 Carbapenemase have Evolved Increased Catalytic Efficiency for Ceftazidime Hydrolysis at the Cost of Enzyme Stability
- Potent Cell-Intrinsic Immune Responses in Dendritic Cells Facilitate HIV-1-Specific T Cell Immunity in HIV-1 Elite Controllers
- The Mammalian Cell Cycle Regulates Parvovirus Nuclear Capsid Assembly
- Host Reticulocytes Provide Metabolic Reservoirs That Can Be Exploited by Malaria Parasites
- The Proteome of the Isolated Containing Vacuole Reveals a Complex Trafficking Platform Enriched for Retromer Components
- NK-, NKT- and CD8-Derived IFNγ Drives Myeloid Cell Activation and Erythrophagocytosis, Resulting in Trypanosomosis-Associated Acute Anemia
- Successes and Challenges on the Road to Cure Hepatitis C
- BRCA1 Regulates IFI16 Mediated Nuclear Innate Sensing of Herpes Viral DNA and Subsequent Induction of the Innate Inflammasome and Interferon-β Responses
- A Structural and Functional Comparison Between Infectious and Non-Infectious Autocatalytic Recombinant PrP Conformers
- Phosphorylation of the Peptidoglycan Synthase PonA1 Governs the Rate of Polar Elongation in Mycobacteria
- Human Immunodeficiency Virus Type 1 Nef Inhibits Autophagy through Transcription Factor EB Sequestration
- Sequence-Specific Fidelity Alterations Associated with West Nile Virus Attenuation in Mosquitoes
- EBV BART MicroRNAs Target Multiple Pro-apoptotic Cellular Genes to Promote Epithelial Cell Survival
- Single-Cell and Single-Cycle Analysis of HIV-1 Replication
- TRIM32 Senses and Restricts Influenza A Virus by Ubiquitination of PB1 Polymerase
- The Herpes Simplex Virus Protein pUL31 Escorts Nucleocapsids to Sites of Nuclear Egress, a Process Coordinated by Its N-Terminal Domain
- Host Transcriptional Response to Influenza and Other Acute Respiratory Viral Infections – A Prospective Cohort Study
- PLOS Pathogens
- Archív čísel
- Aktuálne číslo
- Informácie o časopise
Najčítanejšie v tomto čísle- HIV Latency Is Established Directly and Early in Both Resting and Activated Primary CD4 T Cells
- Battling Phages: How Bacteria Defend against Viral Attack
- A 21st Century Perspective of Poliovirus Replication
- Adenovirus Tales: From the Cell Surface to the Nuclear Pore Complex
Prihlásenie#ADS_BOTTOM_SCRIPTS#Zabudnuté hesloZadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
- Časopisy