degradation target of high-risk human papillomavirus E6 and the alternatively spliced isoform 18 E6. J Virol 81:4080–4090
34. 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 Virol 85:1757–1764
35. Ivanov AI, Young C, Den Beste K, Capaldo
CT, Humbert PO, Brennwald P, Parkos CA,
Nusrat A (2010) Tumor suppressor scribble
regulates assembly of tight junctions in the
intestinal
epithelium.
Am
J
Pathol
176:134–145
36. Stucke VM, Timmerman E, Vandekerckhove J,
Gevaert K, Hall A (2007) The MAGUK protein MPP7 binds to the polarity protein hDlg1
and facilitates epithelial tight junction formation. Mol Biol Cell 18:1744–1755
37. Golebiewski L, Liu H, Javier RT, Rice AP
(2011) The avian influenza virus NS1 ESEV
PDZ binding motif associates with Dlg1 and
scribble to disrupt cellular tight junctions. J
Virol 85:10639–10648
38. Ellencrona K, Syed A, Johansson M (2009)
Flavivirus NS5 associates with host-cell proteins zonula occludens-1 (ZO-1) and regulating synaptic membrane exocytosis-2 (RIMS2)
via an internal PDZ binding mechanism. Biol
Chem 390:319–323
39. Ebnet K, Kummer D, Steinbacher T, Singh A,
Nakayama M, Matis M (2018) Regulation of
cell polarity by cell adhesion receptors. Semin
Cell Dev Biol 81:2–12
40. Butler MT, Wallingford JB (2017) Planar cell
polarity in development and disease. Nat Rev
Mol Cell Biol 18:375–388
41. Schneeberger K, Roth S, Nieuwenhuis EES,
Middendorp S (2018) Intestinal epithelial cell
polarity defects in disease: lessons from microvillus inclusion disease. Dis Model Mech 11:
dmm031088.
https://doi.org/10.1242/
dmm.031088
42. Fischer E, Legue E, Doyen A, Nato F, Nicolas
JF, Torres V, Yaniv M, Pontoglio M (2006)
Defective planar cell polarity in polycystic kidney disease. Nat Genet 38:21–23
43. Medina E, Lemmers C, Lane-Guermonprez L,
Le Bivic A (2002) Role of the Crumbs complex
in the regulation of junction formation in Drosophila and mammalian epithelial cells. Biol
Cell 94:305–313
44. Yamanaka T, Horikoshi Y, Suzuki A,
Sugiyama Y, Kitamura K, Maniwa R, Nagai Y,
Yamashita A, Hirose T, Ishikawa H, Ohno S
(2001) PAR-6 regulates aPKC activity in a
novel way and mediates cell-cell contactinduced formation of the epithelial junctional
complex. Genes Cells 6:721–731
45. Yamanaka T, Ohno S (2008) Role of Lgl/Dlg/
scribble in the regulation of epithelial junction,
polarity
and
growth.
Front
Biosci
13:6693–6707
46. Nakagawa S, Huibregtse JM (2000) Human
scribble (Vartul) is targeted for ubiquitinmediated degradation by the high-risk papillomavirus E6 proteins and the E6AP ubiquitinprotein ligase. Mol Cell Biol 20:8244–8253
47. Stephens R, Lim K, Portela M, Kvansakul M,
Humbert PO, Richardson HE (2018) The
scribble cell polarity module in the regulation
of cell signaling in tissue development and
tumorigenesis. J Mol Biol 430:3585–3612
48. Arpin-Andre C, Mesnard JM (2007) The PDZ
domain-binding motif of the human T cell leukemia virus type 1 tax protein induces mislocalization of the tumor suppressor hScrib in T
cells. J Biol Chem 282:33132–33141
49. Peres E, Blin J, Ricci EP, Artesi M, Hahaut V,
Van den Broeke A, Corbin A, Gazzolo L,
Ratner L, Jalinot P, Duc Dodon M (2018)
PDZ domain-binding motif of tax sustains
T-cell proliferation in HTLV-1-infected humanized mice. PLoS Pathog 14:e1006933
50. Teoh KT, Siu YL, Chan WL, Schluter MA, Liu
CJ, Peiris JS, Bruzzone R, Margolis B, Nal B
(2010) The SARS coronavirus E protein interacts with PALS1 and alters tight junction formation and epithelial morphogenesis. Mol Biol
Cell 21:3838–3852
51. Li X, Yang H, Liu J, Schmidt MD, Gao T
(2011) Scribble-mediated membrane targeting
of PHLPP1 is required for its negative regulation of Akt. EMBO Rep 12:818–824
52. Cherian MA, Baydoun HH, Al-Saleem J,
Shkriabai N, Kvaratskhelia M, Green P, Ratner
L (2015) Akt pathway activation by human
T-cell leukemia virus type 1 tax oncoprotein. J
Biol Chem 290:26270–26281
53. Thomas M, Laura R, Hepner K, Guccione E,
Sawyers C, Lasky L, Banks L (2002) Oncogenic human papillomavirus E6 proteins target
the MAGI-2 and MAGI-3 proteins for degradation. Oncogene 21:5088–5096
54. Liu H, Golebiewski L, Dow EC, Krug RM,
Javier RT, Rice AP (2010) The ESEV
PDZ-binding motif of the avian influenza A
virus NS1 protein protects infected cells from
apoptosis by directly targeting scribble. J Virol
84:11164–11174
55. Prehaud C, Wolff N, Terrien E, Lafage M,
Megret F, Babault N, Cordier F, Tan GS,
Maitrepierre E, Menager P, Chopy D,
234
Carlos Castan ˜ o-Rodriguez et al.
34. 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 Virol 85:1757–1764
35. Ivanov AI, Young C, Den Beste K, Capaldo
CT, Humbert PO, Brennwald P, Parkos CA,
Nusrat A (2010) Tumor suppressor scribble
regulates assembly of tight junctions in the
intestinal
epithelium.
Am
J
Pathol
176:134–145
36. Stucke VM, Timmerman E, Vandekerckhove J,
Gevaert K, Hall A (2007) The MAGUK protein MPP7 binds to the polarity protein hDlg1
and facilitates epithelial tight junction formation. Mol Biol Cell 18:1744–1755
37. Golebiewski L, Liu H, Javier RT, Rice AP
(2011) The avian influenza virus NS1 ESEV
PDZ binding motif associates with Dlg1 and
scribble to disrupt cellular tight junctions. J
Virol 85:10639–10648
38. Ellencrona K, Syed A, Johansson M (2009)
Flavivirus NS5 associates with host-cell proteins zonula occludens-1 (ZO-1) and regulating synaptic membrane exocytosis-2 (RIMS2)
via an internal PDZ binding mechanism. Biol
Chem 390:319–323
39. Ebnet K, Kummer D, Steinbacher T, Singh A,
Nakayama M, Matis M (2018) Regulation of
cell polarity by cell adhesion receptors. Semin
Cell Dev Biol 81:2–12
40. Butler MT, Wallingford JB (2017) Planar cell
polarity in development and disease. Nat Rev
Mol Cell Biol 18:375–388
41. Schneeberger K, Roth S, Nieuwenhuis EES,
Middendorp S (2018) Intestinal epithelial cell
polarity defects in disease: lessons from microvillus inclusion disease. Dis Model Mech 11:
dmm031088.
https://doi.org/10.1242/
dmm.031088
42. Fischer E, Legue E, Doyen A, Nato F, Nicolas
JF, Torres V, Yaniv M, Pontoglio M (2006)
Defective planar cell polarity in polycystic kidney disease. Nat Genet 38:21–23
43. Medina E, Lemmers C, Lane-Guermonprez L,
Le Bivic A (2002) Role of the Crumbs complex
in the regulation of junction formation in Drosophila and mammalian epithelial cells. Biol
Cell 94:305–313
44. Yamanaka T, Horikoshi Y, Suzuki A,
Sugiyama Y, Kitamura K, Maniwa R, Nagai Y,
Yamashita A, Hirose T, Ishikawa H, Ohno S
(2001) PAR-6 regulates aPKC activity in a
novel way and mediates cell-cell contactinduced formation of the epithelial junctional
complex. Genes Cells 6:721–731
45. Yamanaka T, Ohno S (2008) Role of Lgl/Dlg/
scribble in the regulation of epithelial junction,
polarity
and
growth.
Front
Biosci
13:6693–6707
46. Nakagawa S, Huibregtse JM (2000) Human
scribble (Vartul) is targeted for ubiquitinmediated degradation by the high-risk papillomavirus E6 proteins and the E6AP ubiquitinprotein ligase. Mol Cell Biol 20:8244–8253
47. Stephens R, Lim K, Portela M, Kvansakul M,
Humbert PO, Richardson HE (2018) The
scribble cell polarity module in the regulation
of cell signaling in tissue development and
tumorigenesis. J Mol Biol 430:3585–3612
48. Arpin-Andre C, Mesnard JM (2007) The PDZ
domain-binding motif of the human T cell leukemia virus type 1 tax protein induces mislocalization of the tumor suppressor hScrib in T
cells. J Biol Chem 282:33132–33141
49. Peres E, Blin J, Ricci EP, Artesi M, Hahaut V,
Van den Broeke A, Corbin A, Gazzolo L,
Ratner L, Jalinot P, Duc Dodon M (2018)
PDZ domain-binding motif of tax sustains
T-cell proliferation in HTLV-1-infected humanized mice. PLoS Pathog 14:e1006933
50. Teoh KT, Siu YL, Chan WL, Schluter MA, Liu
CJ, Peiris JS, Bruzzone R, Margolis B, Nal B
(2010) The SARS coronavirus E protein interacts with PALS1 and alters tight junction formation and epithelial morphogenesis. Mol Biol
Cell 21:3838–3852
51. Li X, Yang H, Liu J, Schmidt MD, Gao T
(2011) Scribble-mediated membrane targeting
of PHLPP1 is required for its negative regulation of Akt. EMBO Rep 12:818–824
52. Cherian MA, Baydoun HH, Al-Saleem J,
Shkriabai N, Kvaratskhelia M, Green P, Ratner
L (2015) Akt pathway activation by human
T-cell leukemia virus type 1 tax oncoprotein. J
Biol Chem 290:26270–26281
53. Thomas M, Laura R, Hepner K, Guccione E,
Sawyers C, Lasky L, Banks L (2002) Oncogenic human papillomavirus E6 proteins target
the MAGI-2 and MAGI-3 proteins for degradation. Oncogene 21:5088–5096
54. Liu H, Golebiewski L, Dow EC, Krug RM,
Javier RT, Rice AP (2010) The ESEV
PDZ-binding motif of the avian influenza A
virus NS1 protein protects infected cells from
apoptosis by directly targeting scribble. J Virol
84:11164–11174
55. Prehaud C, Wolff N, Terrien E, Lafage M,
Megret F, Babault N, Cordier F, Tan GS,
Maitrepierre E, Menager P, Chopy D,
234
Carlos Castan ˜ o-Rodriguez et al.