Degradation of Human PDZ-Proteins by Human Alphapapillomaviruses Represents an Evolutionary Adaptation to a Novel Cellular Niche

English version České info

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.1004980

Souhrn

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