Interaction of the Human Papillomavirus E6 Oncoprotein with Sorting Nexin 27 Modulates Endocytic Cargo Transport Pathways

PLoS Pathogens

Volumn 12, Issue 9, 2016, Pages

  Ganti, Ketaki ^a   Massimi, Paola ^a   Manzo Merino, Joaquin ^b   Tomaić, Vjekoslav ^a,c   Pim, David ^a   Playford, Martin P ^d   Lizano, Marcela ^e   Roberts, Sally ^f   Kranjec, Christian ^g   Doorbar, John ^g   Banks, Lawrence ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^b INSTITUTO NACIONAL DE CANCEROLOGÍA   (Mexico)

^c RUDER BO KOVI INSTITUTE   (Croatia)

^d NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^e UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^f UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE TRANSPORTER 1; HUMAN PAPILLOMAVIRUS E6 ONCOPROTEIN; PROTEIN E6; PROTEIN E7; SMALL INTERFERING RNA; SORTING NEXIN; SORTING NEXIN 27; UNCLASSIFIED DRUG; VIRAL PROTEIN; DNA BINDING PROTEIN; E6 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 18; ONCOPROTEIN; PROTEIN BINDING; SNX27 PROTEIN, HUMAN;

ARTICLE; AUTORADIOGRAPHY; CELL FRACTIONATION; CELL PROLIFERATION; CONTROLLED STUDY; DRUG MECHANISM; ENDOCYTOSIS; GENE EXPRESSION; GLUCOSE TRANSPORT; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS E6; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; PAPILLOMAVIRUS INFECTION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN BINDING; VIRUS CELL INTERACTION; WART VIRUS; WESTERN BLOTTING; AMINO ACID SEQUENCE; ENDOSOME; FEMALE; GENETICS; HELA CELL LINE; HUMAN PAPILLOMAVIRUS TYPE 18; METABOLISM; PDZ DOMAIN; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN TRANSPORT; UTERINE CERVIX TUMOR; VIROLOGY;

AMINO ACID SEQUENCE; DNA-BINDING PROTEINS; ENDOSOMES; FEMALE; HELA CELLS; HUMAN PAPILLOMAVIRUS 18; HUMANS; ONCOGENE PROTEINS, VIRAL; PDZ DOMAINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TRANSPORT; SORTING NEXINS; UTERINE CERVICAL NEOPLASMS;

EID: 84989876816     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005854     Document Type: Article

References (52)

1. Zur Hausen H, (2002) Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer2: 342–350. doi: 10.1038/nrc79812044010
2. Parkin DM, Bray F, (2006) Chapter 2: The burden of HPV-related cancers. Vaccine24. doi: 10.1016/j.vaccine.2006.05.111
3. Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, et al. (2009) A review of human carcinogens—Part B: biological agents. Lancet Oncol10: 321–322. Available: http://www.thelancet.com/journals/a/article/PIIS1470-2045(09)70096-8/fulltext\nhttp://www.ncbi.nlm.nih.gov/pubmed/19350698\nhttp://monographs.iarc.fr/ENG/Monographs/vol100B/mono100B.pdf. 19350698
4. Smotkin D, Wettstein FO, (1986) Transcription of human papillomavirus type 16 early genes in a cervical cancer and a cancer-derived cell line and identification of the E7 protein. Proc Natl Acad Sci U S A83: 4680–4684. doi: 10.1073/pnas.83.13.46803014503
5. Banks L, Spence P, Androphy E, Hubbert N, Matlashewski G, et al. (1987) Identification of human papillomavirus type 18 E6 polypeptide in cells derived from human cervical carcinomas. J Gen Virol68 (Pt 5): 1351–1359. 3033140
6. Yoshinouchi M, Yamada T, Kizaki M, Fen J, Koseki T, et al. (2003) In vitro and in vivo growth suppression of human papillomavirus 16-positive cervical cancer cells by E6 siRNA. Mol Ther8: 762–768. Available: http://www.ncbi.nlm.nih.gov/pubmed/14599809\nhttp://www.nature.com/mt/journal/v8/n5/pdf/mt2003237a.pdf. 14599809
7. Jones DL, Thompson DA, Münger K, (1997) Destabilization of the RB tumor suppressor protein and stabilization of p53 contribute to HPV type 16 E7-induced apoptosis. Virology239: 97–107. doi: 10.1006/viro.1997.88519426450
8. Doorbar J, (2006) Molecular biology of human papillomavirus infection and cervical cancer. Clin Sci (Lond)110: 525–541. doi: 10.1042/CS20050369
9. Noya F, Chien WM, Broker TR, Chow LT, (2001) p21cip1 degradation in differentiated keratinocytes is abrogated by costabilization with cyclin E induced by human papillomavirus E7. J Virol75: 6121–6134. doi: 10.1128/JVI.75.13.6121-6134.200111390614
10. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM, (1990) The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell63: 1129–1136. doi: 10.1016/0092-8674(90)90409-82175676
11. Thomas M, Banks L, (1998) Inhibition of Bak-induced apoptosis by HPV-18 E6. Oncogene17: 2943–2954. doi: 10.1038/sj.onc.12022239881696
12. Huibregtse JM, Scheffner M, Howley PM, (1991) A cellular protein mediates association of p53 with the E6 oncoprotein of human papillomavirus types 16 or 18. EMBO J10: 4129–4135. 1661671
13. Songyang Z, Fanning AS, Fu C, Xu J, Marfatia SM, et al. (1997) Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science275: 73–77. doi: 10.1126/science.275.5296.738974395
14. Kiyono T, Hiraiwa A, Fujita M, Hayashi Y, Akiyama T, et al. (1997) Binding of high-risk human papillomavirus E6 oncoproteins to the human homologue of the Drosophila discs large tumor suppressor protein. Proc Natl Acad Sci U S A94: 11612–11616. doi: 10.1073/pnas.94.21.116129326658
15. Watson RA, Thomas M, Banks L, Roberts S, (2003) Activity of the human papillomavirus E6 PDZ-binding motif correlates with an enhanced morphological transformation of immortalized human keratinocytes. J Cell Sci116: 4925–4934. doi: 10.1242/jcs.0080914625386
16. Nguyen ML, Nguyen MM, Lee D, Griep AE, Lambert PF, (2003) The PDZ ligand domain of the human papillomavirus type 16 E6 protein is required for E6’s induction of epithelial hyperplasia in vivo. J Virol77: 6957–6964. doi: 10.1128/JVI.77.12.6957-6964.200312768014
17. Lee C, Laimins L, (2004) Role of the PDZ domain-binding motif of the oncoprotein E6 in the pathogenesis of Human Papillomavirus Type 31. J Virol78: 12366–12377. 15507623
18. Delury C, Marsh E, James C, Boon SS, Banks L, Knight G, Roberts S, (2013) The role of protein kinase A regulation of the E6 PDZ-binding domain during the differentiation-dependent life cycle of human papillomavirus type 18. J Virol87: 9463–9472. doi: 10.1128/JVI.01234-1323804647
19. Facciuto F, Cavatorta AL, Valdano MB, Marziali F, Gardiol D, (2012) Differential expression of PDZ domain-containing proteins in human diseases—Challenging topics and novel issues. FEBS J279: 3538–3548. doi: 10.1111/j.1742-4658.2012.08699.x22776401
20. Nakagawa S, Huibregtse JM, (2000) Human scribble (Vartul) is targeted for ubiquitin-mediated degradation by the high-risk papillomavirus E6 proteins and the E6AP ubiquitin-protein ligase. Mol Cell Biol20: 8244–8253. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=86433&tool=pmcentrez&rendertype=abstract. Accessed 10 April 2015. 11027293
21. Roberts S, Delury C, Marsh E, (2012) The PDZ protein discs-large (DLG): The “Jekyll and Hyde” of the epithelial polarity proteins. FEBS J279: 3549–3558. doi: 10.1111/j.1742-4658.2012.08729.x22846345
22. Kranjec C, Banks L, (2011) A systematic analysis of human papillomavirus (HPV) E6 PDZ substrates identifies MAGI-1 as a major target of HPV type 16 (HPV-16) and HPV-18 whose loss accompanies disruption of tight junctions. J Virol85: 1757–1764. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3028909&tool=pmcentrez&rendertype=abstract. Accessed 10 April 2015. doi: 10.1128/JVI.01756-1021123374
23. Rozenblatt-Rosen O, Deo RC, Padi M, Adelmant G, Calderwood MA, et al. (2012) Interpreting cancer genomes using systematic host network perturbations by tumour virus proteins. Nature487: 491–495. doi: 10.1038/nature1128822810586
24. Belotti E, Polanowska J, Daulat AM, Audebert S, Thomé V, et al. (2013) The human PDZome: a gateway to PSD95-Disc large-zonula occludens (PDZ)-mediated functions. Mol Cell Proteomics12: 2587–2603. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3769332&tool=pmcentrez&rendertype=abstract. doi: 10.1074/mcp.O112.02102223722234
25. Suzuki A, Ohno S, (2006) The PAR-aPKC system: lessons in polarity. J Cell Sci119: 979–987. doi: 10.1242/jcs.0289816525119
26. Ivanov AI, Nusrat A, Parkos CA, (2005) Endocytosis of the apical junctional complex: Mechanisms and possible roles in regulation of epithelial barriers. BioEssays27: 356–365. doi: 10.1002/bies.2020315770686
27. Shivas JM, Morrison HA, Bilder D, Skop AR, (2010) Polarity and endocytosis: reciprocal regulation. Trends Cell Biol20: 445–452. doi: 10.1016/j.tcb.2010.04.00320493706
28. Johannes L, Popoff V, (2008) Tracing the retrograde route in protein trafficking. Cell135: 1175–1187. doi: 10.1016/j.cell.2008.12.00919109890
29. Carlton J, Bujny M, Rutherford A, Cullen P, (2005) Sorting nexins—unifying trends and new perspectives. Traffic6: 75–82. doi: 10.1111/j.1600-0854.2005.00260.x15634208
30. Cullen PJ, (2008) Endosomal sorting and signalling: an emerging role for sorting nexins. Nat Rev Mol Cell Biol9: 574–582. doi: 10.1038/nrm242718523436
31. Van Weering JRT, Verkade P, Cullen PJ, (2010) SNX-BAR proteins in phosphoinositide-mediated, tubular-based endosomal sorting. Semin Cell Dev Biol21: 371–380. doi: 10.1016/j.semcdb.2009.11.00919914387
32. Worby CA, Dixon JE, (2002) Sorting out the cellular functions of sorting nexins. Nat Rev Mol Cell Biol3: 919–931. doi: 10.1038/nrm97412461558
33. Ghai R, Collins B, (2011) PX-FERM proteins: A link between endosomal trafficking and signaling?Small GTPases2: 259–263. doi: 10.4161/sgtp.2.5.1727622292128
34. Kajii Y, Muraoka S, Hiraoka S, Fujiyama K, Umino A, et al. (2003) A developmentally regulated and psychostimulant-inducible novel rat gene mrt1 encoding PDZ-PX proteins isolated in the neocortex. Mol Psychiatry8: 434–444. doi: 10.1038/sj.mp.400125812740601
35. Cai L, Loo LS, Atlashkin V, Hanson BJ, Hong W, (2011) Deficiency of sorting nexin 27 (SNX27) leads to growth retardation and elevated levels of N-methyl-D-aspartate receptor 2C (NR2C). Mol Cell Biol31: 1734–1747. doi: 10.1128/MCB.01044-1021300787
36. Lauffer BEL, Melero C, Temkin P, Lei C, Hong W, et al. (2010) SNX27 mediates PDZ-directed sorting from endosomes to the plasma membrane. J Cell Biol190: 565–574. doi: 10.1083/jcb.20100406020733053
37. Joubert L, Hanson B, Barthet G, Sebben M, Claeysen S, et al. (2004) New sorting nexin (SNX27) and NHERF specifically interact with the 5-HT4a receptor splice variant: roles in receptor targeting. J Cell Sci117: 5367–5379. doi: 10.1242/jcs.0137915466885
38. Valdes JL, Tang J, McDermott MI, Kuo JC, Zimmerman SP, et al. (2011) Sorting nexin 27 protein regulates trafficking of a p21-activated kinase (PAK) interacting exchange factor (β-Pix)-G protein-coupled receptor kinase interacting protein (GIT) complex via a PDZ domain interaction. J Biol Chem286: 39403–39416. doi: 10.1074/jbc.M111.26080221926430
39. Temkin P, Lauffer B, Jäger S, Cimermancic P, Krogan NJ, et al. (2011) SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Nat Cell Biol13: 715–721. doi: 10.1038/ncb225221602791
40. Steinberg F, Gallon M, Winfield M, Thomas EC, Bell AJ, et al. (2013) A global analysis of SNX27-retromer assembly and cargo specificity reveals a function in glucose and metal ion transport. Nat Cell Biol15: 461–471. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4052425&tool=pmcentrez&rendertype=abstract. doi: 10.1038/ncb272123563491
41. Glaunsinger BA, Lee SS, Thomas M, Banks L, Javier R, (2000) Interactions of the PDZ-protein MAGI-1 with adenovirus E4-ORF1 and high-risk papillomavirus E6 oncoproteins. Oncogene19: 5270–5280. doi: 10.1038/sj.onc.120390611077444
42. Thomas M, Dasgupta J, Zhang Y, Chen X, Banks L, (2008) Analysis of specificity determinants in the interactions of different HPV E6 proteins with their PDZ domain-containing substrates. Virology376: 371–378. doi: 10.1016/j.virol.2008.03.02118452965
43. Zhang Y, Dasgupta J, Ma RZ, Banks L, Thomas M, et al. (2007) Structures of a human papillomavirus (HPV) E6 polypeptide bound to MAGUK proteins: mechanisms of targeting tumor suppressors by a high-risk HPV oncoprotein. J Virol81: 3618–3626. doi: 10.1128/JVI.02044-0617267502
44. Gallon M, Clairfeuille T, Steinberg F, Mas C, Ghai R, et al. (2014) A unique PDZ domain and arrestin-like fold interaction reveals mechanistic details of endocytic recycling by SNX27-retromer. Proc Natl Acad Sci U S A. Available: http://www.ncbi.nlm.nih.gov/pubmed/25136126.
45. Tomaic V, Pim D, Banks L, (2009) The stability of the human papillomavirus E6 oncoprotein is E6AP dependent. Virology393: 7–10. doi: 10.1016/j.virol.2009.07.02919700180
46. Asano T, Katagiri H, Takata K, Lin J, Ishihara et al. (1991). The role of N-glycosylation of GLUT1 for glucose transport activity. J. Biol Chem266: 24632–24636. 1761560
47. Chien MW, Lin MH, Huang SH, Fu SH, Hsu CY, et al. (2015). Glucosamine modulates T cell differentiation through downregulating N-linked glycosylation of CD25. J. Biol. Chem. 290: 29329–29344. doi: 10.1074/jbc.M115.67467126468284
48. Sheff DR, Daro EA, Hull M, Mellman I, (1999) The receptors recycling pathway contains two distinct populations of early endosomes with different sorting functions. J Cell Biol145: 123–139. doi: 10.1083/jcb.145.1.12310189373
49. Vincentelli R, Luck K, Poirson J, Polanowska J, Abdat J, et al. (2015) Quantifying domain-ligand affinities and specificities by high-throughput holdup assay. Nat Methods. Available: http://www.ncbi.nlm.nih.gov/pubmed/26053890. Accessed 10 June 2015.
50. Allen-Hoffmann B, Schlosser S, Ivarie C, Sattler C, Meisner L, O'Connor S, (2000) Normal growth and differentiation in a spontaneously immortalised near-diploid human keratinocyte cell line, NIKS. J Inv Dermatol114: 444–455.
51. Nicolaides I, Davy C, Raj K, Kranjec C, Banks L, Doorbar J, (2011) Stabilization of HPV E6 protein by PDZ proteins, and potential implications for genome maintenance. Virology414 (2): 137–145. doi: 10.1016/j.virol.2011.03.01721489588
52. Boon SS, Banks L, (2012) High-Risk Human Papillomavirus E6 Oncoproteins interact with 14-3-3 in a PDZ Binding Motif-Dependent manner. J Virol87: 1586–1595. doi: 10.1128/JVI.02074-1223175360