The role of Irf6 in tooth epithelial invagination

Developmental Biology

Volumn 365, Issue 1, 2012, Pages 61-70

  Blackburn, James ^a   Ohazama, Atsushi ^a,k   Kawasaki, Katsushige ^a   Otsuka Tanaka, Yoko ^a   Liu, Bigang ^b   Honda, Kenya ^c   Rountree, Ryan B ^d,l   Hu, Yinling ^e   Kawasaki, Maiko ^a,f   Birchmeier, Walter ^g   Schmidt Ullrich, Ruth ^g   Kinoshita, Akira ^h,i   Schutte, Brian C ⁱ   Hammond, Nigel L ^j   Dixon, Michael J ^j   Sharpe, Paul T ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF TEXAS   (United States)

^c UNIVERSITY OF TOKYO   (Japan)

^d AMGEN INC   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

^f NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^g MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^h NAGASAKI UNIVERSITY   (Japan)

ⁱ Nagasaki University ^*  (United States)

^j UNIVERSITY OF MANCHESTER   (United Kingdom)

^k SHOWA UNIVERSITY SCHOOL OF DENTISTRY   (Japan)

^l BN ImmunoTherapeutics   (United States)

more..

Author keywords

Epithelium; Ikk ; Incisor; Invagination; Irf6; Tooth development; Wnt

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 6; WNT PROTEIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; GENE; GENE MUTATION; IKKA GENE; INCISOR; IRF6 GENE; MOLECULAR MECHANICS; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TOOTH DEVELOPMENT; TOOTH EPITHELIAL INVAGINATION; UPREGULATION;

MUS;

EID: 84862788362     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.02.009     Document Type: Article

References (77)

1. Albanese C., Wu K., D'Amico M., Jarrett C., Joyce D., Hughes J., Hulit J., Sakamaki T., Fu M., Ben-Ze'ev A., Bromberg J.F., Lamberti C., Verma U., Gaynor R.B., Byers S.W., Pestell R.G. IKKalpha regulates mitogenic signaling through transcriptional induction of cyclin D1 via Tcf. Mol. Biol. Cell 2003, 14:585-599.
2. Arangannal P., Muthu M.S., Nirmal L. Van der Woude syndrome: a case report. J. Indian Soc. Pedod. Prev. Dent. 2002, 20:102-103.
3. Barth A.I., Caro-Gonzalez H.Y., Nelson W.J. Role of adenomatous polyposis coli (APC) and microtubules in directional cell migration and neuronal polarization. Semin. Cell Dev. Biol. 2008, 19:245-251.
4. Bhr C., Rohwer A., Stempka L., Rincke G., Marks F., Gschwendt M. DIK, a novel protein kinase that interacts with protein kinase Cdelta. Cloning, characterization, and gene analysis. J. Biol. Chem. 2000, 275:36350-36357.
5. Bixler D., Poland C., Nance W.E. Phenotypic variation in the popliteal pterygium syndrome. Clin. Genet. 1973, 4:220-228.
6. Bonjardim C.A., Ferreira P.C., Kroon E.G. Interferons: signaling, antiviral and viral evasion. Immunol. Lett. 2009, 122:1-11.
7. Candi E., Terrinoni A., Rufini A., et al. p63 is upstream of IKK alpha in epidermal development. J. Cell Sci. 2006, 119(Pt 22):4617-4622.
8. Carayol N., Wang C.Y. IKKalpha stabilizes cytosolic beta-catenin by inhibiting both canonical and non-canonical degradation pathways. Cell. Signal. 2006, 18:1941-1946.
9. Chariot A. The NF-kappaB-independent functions of IKK subunits in immunity and cancer. Trends Cell Biol. 2009, 19:404-413.
10. Charles C., Hovorakova M., Ahn Y., et al. Regulation of tooth number by fine-tuning levels of receptor-tyrosine kinase signaling. Development 2011, 138(18):4063-4073.
11. Charoenchaikorn K., Yokomizo T., Rice D.P., Honjo T., Matsuzaki K., Shintaku Y., Imai Y., Wakamatsu A., Takahashi S., Ito Y., Takano-Yamamoto T., Thesleff I., Yamamoto M., Yamashiro T. Runx1 is involved in the fusion of the primary and the secondary palatal shelves. Dev. Biol. 2009, 326:392-402.
12. Chen L., Haider K., Ponda M., Cariappa A., Rowitch D., Pillai S. Protein kinase C-associated kinase (PKK), a novel membrane-associated, ankyrin repeat-containing protein kinase. J. Biol. Chem. 2001, 276:21737-21744.
13. Dunty W.C., Biris K.K., Chalamalasetty R.B., Taketo M.M., Lewandoski M., Yamaguchi T.P. Wnt3a/beta-catenin signaling controls posterior body development by coordinating mesoderm formation and segmentation. Development 2008, 135:85-94.
14. Ferretti E., Li B., Zewdu R., et al. A conserved Pbx-Wnt-p63-Irf6 regulatory module controls face morphogenesis by promoting epithelial apoptosis. Dev. Cell 2011, 21(4):627-641.
15. Froster-Iskenius U.G. Popliteal pterygium syndrome. J. Med. Genet. 1990, 27:320-326.
16. Goodison S., Urquidi U., Tarin D. CD44 cell adhesion molecules. J. Clin. Pathol. Mol. Pathol. 1999, 52:189-196.
17. Grosveld G.C. Gamma-secretase inhibitors: notch so bad. Nat. Med. 2009, 15:20-21.
18. Guenet J.L., Salzgeber B., Tassin M.T. Repeated epilation: a genetic epidermal syndrome in mice. J. Hered. 1979, 70:90-94.
19. Häcker H., Karin M. Regulation and function of IKK and IKK-related kinases. Sci. STKE 2006, 2006:re13.
20. Hermeking H., Benzinger A. 14-3-3 proteins in cell cycle regulation. Semin. Cancer Biol. 2006, 16:183-192.
21. Hertzog P., Forster S., Samarajiwa S. Systems biology of interferon responses. J. Interferon Cytokine Res. 2011, 31:5-11.
22. Hiscott J. Convergence of the NF-kappaB and IRF pathways in the regulation of the innate antiviral response. Cytokine Growth Factor Rev. 2007, 18:483-490.
23. Holland P., Willis C., Kanaly S., Glaccum M., Warren A., Charrier K., Murison J., Derry J., Virca G., Bird T., Peschon J. RIP4 is an ankyrin repeat-containing kinase essential for keratinocyte differentiation. Curr. Biol. 2002, 12:1424-1428.
24. Holtschke T., Löhler J., Kanno Y., Fehr T., Giese N., Rosenbauer F., Lou J., Knobeloch K.P., Gabriele L., Waring J.F., Bachmann M.F., Zinkernagel R.M., Morse H.C., Ozato K., Horak I. Immunodeficiency and chronic myelogenous leukemia-like syndrome in mice with a targeted mutation of the ICSBP gene. Cell 1996, 87:307-317.
25. Honda K., Yanai H., Negishi H., Asagiri M., Sato M., Mizutani T., Shimada N., Ohba Y., Takaoka A., Yoshida N., Taniguchi T. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005, 434:772-777.
26. Hoshino K., Sugiyama T., Matsumoto M., Tanaka T., Saito M., Hemmi H., Ohara O., Akira S., Kaisho T. IkappaB kinase-alpha is critical for interferon-alpha production induced by Toll-like receptors 7 and 9. Nature 2006, 440:949-953.
27. Hu Y., Baud V., Delhase M., Zhang P., Deerinck T., Ellisman M., Johnson R., Karin M. Abnormal morphogenesis but intact IKK activation in mice lacking the IKKalpha subunit of IkappaB kinase. Science 1999, 284:316-320.
28. Ingraham C.R., Kinoshita A., Kondo S., Yang B., Sajan S., Trout K.J., Malik M.I., Dunnwald M., Goudy S.L., Lovett M., Murray J.C., Schutte B.C. Abnormal skin, limb and craniofacial morphogenesis in mice deficient for interferon regulatory factor 6 (Irf6). Nat. Genet. 2006, 38:1335-1340.
29. Janssens S., Beyaert R. Functional diversity and regulation of different interleukin-1 receptor-associated kinase (IRAK) family members. Mol. Cell 2003, 11:293-302.
30. Järvinen E., Salazar-Ciudad I., Birchmeier W., Taketo M.M., Jernvall J., Thesleff I. Continuous tooth generation in mouse is induced by activated epithelial Wnt/beta-catenin signaling. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:18627-18632.
31. Jiang R., Lan Y., Chapman H.D., Shawber C., Norton C.R., Serreze D.V., Weinmaster G., Gridley T. Defects in limb, craniofacial, and thymic development in Jagged2 mutant mice. Genes Dev. 1998, 12:1046-1057.
32. Kantaputra P.N., Sumitsawan Y., Schutte B.C., Tochareontanaphol C. Van der Woude syndrome with sensorineural hearing loss, large craniofacial sinuses, dental pulp stones, and minor limb anomalies: report of a four-generation Thai family. Am. J. Med. Genet. 2002, 108:275-280.
33. Killeen M.T., Sybingco S.S. Netrin, Slit and Wnt receptors allow axons to choose the axis of migration. Dev. Biol. 2008, 323:143-151.
34. Kimura T., Kadokawa Y., Harada H., Matsumoto M., Sato M., Kashiwazaki Y., Tarutani M., Tan R.S., Takasugi T., Matsuyama T., Mak T.W., Noguchi S., Taniguchi T. Essential and non-redundant roles of p48 (ISGF3 gamma) and IRF-1 in both type I and type II interferon responses, as revealed by gene targeting studies. Genes Cells 1996, 1:115-124.
35. Klein P.S., Melton D.A. A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:8455-8459.
36. Kondo S., Schutte B.C., Richardson R.J., Bjork B.C., Knight A.S., Watanabe Y., Howard E., de Lima R.L., Daack-Hirsch S., Sander A., McDonald-McGinn D.M., Zackai E.H., Lammer E.J., Aylsworth A.S., Ardinger H.H., Lidral A.C., Pober B.R., Moreno L., Arcos-Burgos M., Valencia C., Houdayer C., Bahuau M., Moretti-Ferreira D., Richieri-Costa A., Dixon M.J., Murray J.C. Mutations in IRF6 cause Van der Woude and popliteal pterygium syndromes. Nat. Genet. 2002, 32:285-289.
37. Lamberti C., Lin K.M., Yamamoto Y., Verma U., Verma I.M., Byers S., Gaynor R.B. Regulation of beta-catenin function by the IkappaB kinases. J. Biol. Chem. 2001, 276:42276-42286.
38. Laurikkala J., Mikkola M.L., James M., Tummers M., Mills A.A., Thesleff I. p63 regulates multiple signalling pathways required for ectodermal organogenesis and differentiation. Development 2006, 133(8):1553-1563.
39. Li Q., Verma I.M. NF-kappaB regulation in the immune system. Nat. Rev. Immunol. 2002, 2:725-734.
40. Li Q., Lu Q., Hwang J.Y., Büscher D., Lee K.F., Izpisua-Belmonte J.C., Verma I.M. IKK1-deficient mice exhibit abnormal development of skin and skeleton. Genes Dev. 1999, 13:1322-1328.
41. Liu B., Xia X., Zhu F., Park E., Carbajal S., Kiguchi K., DiGiovanni J., Fischer S.M., Hu Y. IKKalpha is required to maintain skin homeostasis and prevent skin cancer. Cancer Cell 2008, 14:212-225.
42. Liu F., Chu E.Y., Watt B., Zhang Y., Gallant N.M., Andl T., Yang S.H., Lu M.M., Piccolo S., Schmidt-Ullrich R., Taketo M.M., Morrisey E.E., Atit R., Dlugosz A.A., Millar S.E. Wnt/beta-catenin signaling directs multiple stages of tooth morphogenesis. Dev. Biol. 2008, 313:210-224.
43. Lohoff M., Mak T.W. Roles of interferon-regulatory factors in T-helper-cell differentiation. Nat. Rev. Immunol. 2005, 5:125-135.
44. Lomada D., Liu B., Coghlan L., Hu Y., Richie E.R. Thymus medulla formation and central tolerance are restored in IKKalpha-/- mice that express an IKKalpha transgene in keratin 5+ thymic epithelial cells. J. Immunol. 2007, 178:829-837.
45. Lustig B., Jerchow B., Sachs M., Weiler S., Pietsch T., Karsten U., van de Wetering M., Clevers H., Schlag P.M., Birchmeier W., Behrens J. Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol. Cell. Biol. 2002, 22:1184-1193.
46. Matsuyama T., Kimura T., Kitagawa M., Pfeffer K., Kawakami T., Watanabe N., Kündig T.M., Amakawa R., Kishihara K., Wakeham A. Targeted disruption of IRF-1 or IRF-2 results in abnormal type I IFN gene induction and aberrant lymphocyte development. Cell 1993, 75:83-97.
47. Mittrücker H.W., Matsuyama T., Grossman A., Kündig T.M., Potter J., Shahinian A., Wakeham A., Patterson B., Ohashi P.S., Mak T.W. Requirement for the transcription factor LSIRF/IRF4 for mature B and T lymphocyte function. Science 1997, 275:540-543.
48. Mucchielli M.L., Mitsiadis T.A. Correlation of asymmetric Notch2 expression and mouse incisor rotation. Mech. Dev. 2000, 91:379-382.
49. Munne P.M., Tummers M., Jarvinen E., Thesleff I., Jernvall J. Tinkering with the inductive mesenchyme: Sostdc1 uncovers the role of dental mesenchyme in limiting tooth induction. Development 2009, 136(3):393-402.
50. Nawa H., Oberoi S., Vargervik K. Taurodontism and Van der Woude syndrome. Is there an association?. Angle Orthod. 2008, 78:832-837.
51. Nicolas M., Wolfer A., Raj K., Kummer J.A., Mill P., van Noort M., Hui C.C., Clevers H., Dotto G.P., Radtke F. Notch1 functions as a tumor suppressor in mouse skin. Nat. Genet. 2003, 33:416-421.
52. Oberoi S., Vargervik K. Hypoplasia and hypodontia in Van der Woude syndrome. Cleft Palate Craniofac. J. 2005, 42:459-466.
53. Ochiai T., Shibukawa Y., Nagayama M., Mundy C., Yasuda T., Okabe T., Shimono K., Kanyama M., Hasegawa H., Maeda Y., Lanske B., Pacifici M., Koyama E. Indian hedgehog roles in post-natal TMJ development and organization. J. Dent. Res. 2010, 89:349-354.
54. Ohazama A., Hu Y., Schmidt-Ullrich R., Cao Y., Scheidereit C., Karin M., Sharpe P.T. A dual role for Ikk alpha in tooth development. Dev. Cell 2004, 6:219-227.
55. Ohazama A., Tucker A., Sharpe P.T. Organized tooth-specific cellular differentiation stimulated by BMP4. J. Dent. Res. 2005, 84:603-606.
56. Ohazama A., Johnson E.B., Ota M.S., Choi H.Y., Choi H.J., Porntaveetus T., Oommen S., Itoh N., Eto K., Gritli-Linde A., Herz J., Sharpe P.T. Lrp4 modulates extracellular integration of cell signaling pathways in development. PLoS One 2008, 3:e4092.
57. Pellón-Cárdenas O., Schweitzer J., D'Souza-Schorey C. Endocytic trafficking and Wnt/β-catenin signaling. Curr. Drug Targets 2011, 12:1216-1222.
58. Platanias L.C. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev. Immunol. 2005, 5:375-386.
59. Richardson R.J., Dixon J., Malhotra S., Hardman M.J., Knowles L., Boot-Handford R.P., Shore P., Whitmarsh A., Dixon M.J. Irf6 is a key determinant of the keratinocyte proliferation-differentiation switch. Nat. Genet. 2006, 38:1329-1334.
60. Sanz A.B., Sanchez-Niño M.D., Ramos A.M., Moreno J.A., Santamaria B., Ruiz-Ortega M., Egido J., Ortiz A. NF-kappaB in renal inflammation. J. Am. Soc. Nephrol. 2010, 21:1254-1262.
61. Sarkar L., Cobourne M., Naylor S., Smalley M., Dale T., Sharpe P.T. Wnt/Shh interactions regulate ectodermal boundary formation during mammalian tooth development. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:4520-4524.
62. Sato M., Suemori H., Hata N., Asagiri M., Ogasawara K., Nakao K., Nakaya T., Katsuki M., Noguchi S., Tanaka N., Taniguchi T. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 2000, 13:539-548.
63. Schmidt-Ullrich R., Mémet S., Lilienbaum A., Feuillard J., Raphaël M., Israel A. NF-kappaB activity in transgenic mice: developmental regulation and tissue specificity. Development 1996, 122:2117-2128.
64. Schneider E.L. Lip pits and congenital absence of second premolars: varied expression of the Lip Pits syndrome. J. Med. Genet. 1973, 10:346-349.
65. Schock F., Perrimon N. Molecular mechanisms of epithelial morphogenesis. Annu. Rev. Cell Dev. Biol. 2002, 18:463-493.
66. Shih I.M., Wang T.L. Notch signaling, gamma-secretase inhibitors, and cancer therapy. Cancer Res. 2007, 67:1879-1882.
67. Sylvie J., Ellen C., Kris V. The role of Wnt in cell signaling and cell adhesion during early vertebrate development. Front. Biosci. 2011, 17:2352-2366.
68. Takaoka A., Yanai H., Kondo S., Duncan G., Negishi H., Mizutani T., Kano S., Honda K., Ohba Y., Mak T.W., Taniguchi T. Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 2005, 434:243-249.
69. Takeda K., Takeuchi O., Tsujimura T., Itami S., Adachi O., Kawai T., Sanjo H., Yoshikawa K., Terada N., Akira S. Limb and skin abnormalities in mice lacking IKKalpha. Science 1999, 284:313-316.
70. Taniguchi T., Ogasawara K., Takaoka A., Tanaka N. IRF family of transcription factors as regulators of host defense. Annu. Rev. Immunol. 2001, 19:623-655.
71. Thesleff I. The genetic basis of tooth development and dental defects. Am. J. Med. Genet. A 2006, 140:2530-2535.
72. Thomason H.A., Zhou H., Kouwenhoven E.N., Dotto G.P., Restivo G., Nguyen B.C., Little H., Dixon M.J., van Bokhoven H., Dixon J. Cooperation between the transcription factors p63 and IRF6 is essential to prevent cleft palate in mice. J. Clin. Invest. 2010, 120:1561-1569.
73. Tucker A., Sharpe P. The cutting-edge of mammalian development; how the embryo makes teeth. Nat. Rev. Genet. 2004, 5:499-508.
74. Van der Woude A. Fistula labii inferioris congenita and its association with cleft lip and palate. Am. J. Hum. Genet. 1954, 6:244-256.
75. van Es J.H., van Gijn M.E., Riccio O., van den Born M., Vooijs M., Begthel H., Cozijnsen M., Robine S., Winton D.J., Radtke F., Clevers H. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 2005, 435:959-963.
76. Wang A.H., Kruhlak M.J., Wu J., Bertos N.R., Vezmar M., Posner B.I., Bazett-Jones D.P., Yang X.J. Regulation of histone deacetylase 4 by binding of 14-3-3 proteins. Mol. Cell. Biol. 2000, 20:6904-6912.
77. Yasuda T., Mundy C., Kinumatsu T., Shibukawa Y., Shibutani T., Grobe K., Minugh-Purvis N., Pacifici M., Koyama E. Sulfotransferase Ndst1 is needed for mandibular and TMJ development. J. Dent. Res. 2010, 89:1111-1116.