C-Jun N-Terminal Kinase (JNK) Mediates Wnt5a-Induced Cell Motility Dependent or Independent of RhoA Pathway in Human Dental Papilla Cells

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Wang, Chenglin ^a,b   Zhao, Yuan ^a,b   Su, Yingying ^a,b   Li, Ruimin ^a,b   Lin, Yunfeng ^a,b   Zhou, Xuedong ^a,b   Ye, Ling ^a,b  

^a SICHUAN UNIVERSITY   (China)

^b SICHUAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; MYOSIN LIGHT CHAIN; PAXILLIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; STRESS ACTIVATED PROTEIN KINASE; WNT5A PROTEIN;

ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL JUNCTION; CELL MIGRATION; CELL MOTILITY; CELL MOTION; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; HUMAN; HUMAN CELL; HUMAN TISSUE; MESENCHYME CELL; ODONTOBLAST; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; TOOTH DEVELOPMENT; TOOTH PAPILLA; TOOTH PAPILLA CELL; UPREGULATION;

BETA CATENIN; CELL ADHESION; CELL MOVEMENT; CYTOSKELETON; DENTAL PAPILLA; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MYOSIN LIGHT CHAINS; PAXILLIN; PHOSPHORYLATION; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 84879739288     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069440     Document Type: Article

References (79)

1. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, et al. (2003) Cell migration: integrating signals from front to back. Science 302: 1704-1709. doi:10.1126/science.1092053. PubMed: 14657486.
2. Vicente-Manzanares M, Horwitz AR, (2011) Adhesion dynamics at a glance. J Cell Sci 124: 3923-3927. doi:10.1242/jcs.095653. PubMed: 22194302.
3. Aman A, Piotrowski T, (2010) Cell migration during morphogenesis. Dev Biol 341: 20-33. doi:10.1016/j.ydbio.2009.11.014. PubMed: 19914236.
4. Thesleff I, Hurmerinta K, (1981) Tissue interactions in tooth development. Differentiation 18: 75-88. doi:10.1111/j.1432-0436.1981.tb01107.x. PubMed: 7011890.
5. Thesleff I, Vaahtokari A, Vainio S, Jowett A, (1996) Molecular mechanisms of cell and tissue interactions during early tooth development. Anat Rec 245: 151-161. doi:10.1002/(SICI)1097-0185(199606)245:2. PubMed: 8769660.
6. Thesleff I, Vaahtokari A, Kettunen P, Aberg T, (1995) Eplthelial-Mesenchymal Signaling during Tooth Development. Connect Tissue Res 32: 9-15. doi:10.3109/03008209509013700. PubMed: 7554939.
7. Chai Y, Slavkin HC, (2003) Prospects for tooth regeneration in the 21st century: a perspective. Microsc Res Tech 60: 469-479. doi:10.1002/jemt.10287. PubMed: 12619122.
8. Wodarz A, Nusse R, (1998) Mechanisms of Wnt signaling in development. Annu Rev Cell Dev Biol 14: 59-88. doi:10.1146/annurev.cellbio.14.1.59. PubMed: 9891778.
9. Logan CY, Nusse R, (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20: 781-810. doi:10.1146/annurev.cellbio.20.010403.113126. PubMed: 15473860.
10. Yang-Snyder J, Miller JR, Brown JD, Lai CJ, Moon RT, (1996) A frizzled homolog functions in a vertebrate Wnt signaling pathway. Curr Biol 6: 1302-1306. doi:10.1016/S0960-9822(02)70716-1. PubMed: 8939578.
11. Veeman MT, Axelrod JD, Moon RT, (2003) A Second Canon Functions and Mechanisms of [beta]-Catenin-Independent Wnt Signaling. Developmental Cell 5: 367-377.
12. Topol L, Jiang X, Choi H, Garrett-Beal L, Carolan PJ, et al. (2003) Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent β-catenin degradation. J Cell Biol 162: 899-908. doi:10.1083/jcb.200303158. PubMed: 12952940.
13. Kohn AD, Moon RT, (2005) Wnt and calcium signaling: β-catenin-independent pathways. Cell Calcium 38: 439-446. doi:10.1016/j.ceca.2005.06.022. PubMed: 16099039.
14. van Amerongen R, Nusse R, (2009) Towards an integrated view of Wnt signaling in development. Development 136: 3205-3214. doi:10.1242/dev.033910. PubMed: 19736321.
15. Katoh M, (2005) WNT/PCP signaling pathway and human cancer (Review). Oncol Rep 14: 1583-1588. PubMed: 16273260.
16. Fuerer C, Nusse R, Ten Berge D, (2008) Wnt signalling in development and disease. EMBO Rep 9: 134-138. doi:10.1038/sj.embor.7401159. PubMed: 18188179.
17. Kikuchi A, Yamamoto H, Sato A, (2009) Selective activation mechanisms of Wnt signaling pathways. Trends Cell Biol 19: 119-129. doi:10.1016/j.tcb.2009.01.003. PubMed: 19208479.
18. Mikels AJ, Nusse R, (2006) Purified Wnt5a protein activates or inhibits β-catenin-TCF signaling depending on receptor context. PLOS Biol 4: e115. doi:10.1371/journal.pbio.0040115. PubMed: 16602827.
19. Katoh M, (2009) Transcriptional mechanisms of WNT5A based on NF-kB, Hedgehog, TGFβ, and Notch signaling cascades. Int J Mol Med 23: 763-769. PubMed: 19424602.
20. Mlodzik M, (2002) Planar cell polarization: do the same mechanisms regulate < i > Drosophila tissue polarity and vertebrate gastrulation? Trends Genet 18: 564-571. doi:10.1016/S0168-9525(02)02770-1. PubMed: 12414186.
21. Yamanaka H, Moriguchi T, Masuyama N, Kusakabe M, Hanafusa H, et al. (2002) JNK functions in the non-canonical Wnt pathway to regulate convergent extension movements in vertebrates. EMBO Rep 3: 69-75. doi:10.1093/embo-reports/kvf008. PubMed: 11751577.
22. Kim GH, Han JK, (2005) JNK and ROK[alpha] function in the noncanonical Wnt/RhoA signaling pathway to regulate Xenopus convergent extension movements. Dev Dynam 232: 958-968. doi:10.1002/dvdy.20262.
23. Pukrop T, Klemm F, Hagemann T, Gradl D, Schulz M, et al. (2006) Wnt 5a signaling is critical for macrophage-induced invasion of breast cancer cell lines. Proc Natl Acad Sci USA 103: 5454-5459. doi:10.1073/pnas.0509703103. PubMed: 16569699.
24. Weeraratna AT, Jiang Y, Hostetter G, Rosenblatt K, Duray P, et al. (2002) Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma. Cancer Cell 1: 279-288. doi:10.1016/S1535-6108(02)00045-4. PubMed: 12086864.
25. Huang CL, Liu D, Nakano J, Ishikawa S, Kontani K, et al. (2005) Wnt5a Expression Is Associated With the Tumor Proliferation and the Stromal Vascular Endothelial Growth Factor-an Expression in Non-small-Cell Lung Cancer. J Clin Oncol 23: 8765-8773. doi:10.1200/JCO.2005.02.2871. PubMed: 16314637.
26. Yamamoto H, Oue N, Sato A, Hasegawa Y, Matsubara A, et al. (2010) Wnt5a signaling is involved in the aggressiveness of prostate cancer and expression of metalloproteinase. Oncogene 29: 2036-2046. doi:10.1038/onc.2009.496. PubMed: 20101234.
27. Kremenevskaja N, Von Wasielewski R, Rao AS, Schöfl C, Andersson T, et al. (2005) Wnt-5a has tumor suppressor activity in thyroid carcinoma. Oncogene 24: 2144-2154. doi:10.1038/sj.onc.1208370. PubMed: 15735754.
28. Dejmek J, Dejmek A, Säfholm A, Sjölander A, Andersson T, (2005) Wnt-5a protein expression in primary dukes B colon cancers identifies a subgroup of patients with good prognosis. Cancer Res 65: 9142-9146. doi:10.1158/0008-5472.CAN-05-1710. PubMed: 16230369.
29. Sarkar L, Sharpe PT, (1999) Expression of Wnt signalling pathway genes during tooth development. Mech Dev 85: 197-200. doi:10.1016/S0925-4773(99)00095-7. PubMed: 10415363.
30. Lin M, Li L, Liu C, Liu H, He F, et al. (2011) Wnt5a regulates growth, patterning, and odontoblast differentiation of developing mouse tooth. Dev Dynam 240: 432-440. doi:10.1002/dvdy.22550. PubMed: 21246660.
31. Peng L, Dong G, Xu P, Ren LB, Wang CL, et al. (2010) Expression of Wnt5a in tooth germs and the related signal transduction analysis. Arch Oral Biol 55: 108-114. doi:10.1016/j.archoralbio.2009.12.002. PubMed: 20034610.
32. Peng L, Ren LB, Dong G, Wang CL, Xu P, et al. (2010) Wnt5a promotes differentiation of human dental papilla cells. Int Endod J 43: 404-412. doi:10.1111/j.1365-2591.2010.01693.x. PubMed: 20518933.
33. Wang C, Ren L, Peng L, Xu P, Dong G, et al. (2010) Effect of Wnt6 on human dental papilla cells in vitro. J Endod 36: 238-243. doi:10.1016/j.joen.2009.09.007. PubMed: 20113781.
34. Peng L, Ye L, Dong G, Ren LB, Wang CL, et al. (2009) WNT5A inhibits human dental papilla cell proliferation and migration. Biochem Biophys Res Commun 390: 1072-1078. doi:10.1016/j.bbrc.2009.10.136. PubMed: 19878652.
35. Endo Y, Wolf V, Muraiso K, Kamijo K, Soon L, et al. (2005) Wnt-3a-dependent cell motility involves RhoA activation and is specifically regulated by dishevelled-2. J Biol Chem 280: 777-786. PubMed: 15509575.
36. Even-Ram S, Artym VV, Streuli CH, (2009) Extracellular matrix protocols: Humana.
37. Block MR, Badowski C, Millon-Fremillon A, Bouvard D, Bouin AP, et al. (2008) Podosome-type adhesions and focal adhesions, so alike yet so different. Eur J Cell Biol 87: 491-506. doi:10.1016/j.ejcb.2008.02.012. PubMed: 18417250.
38. Turner CE, (2000) Paxillin and focal adhesion signalling. Nat Cell Biol 2: E231-E236. doi:10.1038/35046659. PubMed: 11146675.
39. Brown MC, Turner CE, (2004) Paxillin: adapting to change. Physiol Rev 84: 1315-1339. doi:10.1152/physrev.00002.2004. PubMed: 15383653.
40. Nakamura K, Yano H, Uchida H, Hashimoto S, Schaefer E, et al. (2000) Tyrosine phosphorylation of paxillin is involved in temporospatial regulation of paxillin-containing focal adhesion formation and F-actin organization in motile cells. J Biol Chem 275: 27155-27164. PubMed: 10823820.
41. Tsubouchi A, Sakakura J, Yagi R, Mazaki Y, Schaefer E, et al. (2002) Localized suppression of RhoA activity by Tyr31/118-phosphorylated paxillin in cell adhesion and migration. J Cell Biol 159: 673-683. doi:10.1083/jcb.200202117. PubMed: 12446743.
42. Zaidel-Bar R, Milo R, Kam Z, Geiger B, (2007) A paxillin tyrosine phosphorylation switch regulates the assembly and form of cell-matrix adhesions. J Cell Sci 120: 137-148. PubMed: 17164291.
43. Drees F, Pokutta S, Yamada S, Nelson WJ, Weis WI, (2005) β-catenin is a molecular switch that binds E-cadherin-β-catenin and regulates actin-filament assembly. Cell 123: 903-915. doi:10.1016/j.cell.2005.09.021. PubMed: 16325583.
44. Lickert H, Bauer A, Kemler R, Stappert J, (2000) Casein kinase II phosphorylation of E-cadherin increases E-cadherin/β-catenin interaction and strengthens cell-cell adhesion. J Biol Chem 275: 5090-5095. doi:10.1074/jbc.275.7.5090. PubMed: 10671552.
45. Medrek C, Landberg G, Andersson T, Leandersson K, (2009) Wnt-5a-CKIα signaling promotes β-catenin/E-cadherin complex formation and intercellular adhesion in human breast epithelial cells. J Biol Chem 284: 10968-10979. doi:10.1074/jbc.M804923200. PubMed: 19244247.
46. Kikuchi A, Yamamoto H, Sato A, Matsumoto S, (2012) Wnt5a: its signalling, functions and implication in diseases. Acta Physiol 204: 17-33. doi:10.1111/j.1748-1716.2011.02294.x. PubMed: 21518267.
47. Huang C, Rajfur Z, Borchers C, Schaller MD, Jacobson K, (2003) JNK phosphorylates paxillin and regulates cell migration. Nature 424: 219-223. doi:10.1038/nature01745. PubMed: 12853963.
48. Subauste MC, Von Herrath M, Benard V, Chamberlain CE, Chuang TH, et al. (2000) Rho family proteins modulate rapid apoptosis induced by cytotoxic T lymphocytes and Fas. J Biol Chem 275: 9725-9733. doi:10.1074/jbc.275.13.9725. PubMed: 10734125.
49. Amano M, Chihara K, Kimura K, Fukata Y, Nakamura N, et al. (1997) Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 275: 1308-1311. doi:10.1126/science.275.5304.1308. PubMed: 9036856.
50. Ikeda E, Hirose M, Kotobuki N, Shimaoka H, Tadokoro M, et al. (2006) Osteogenic differentiation of human dental papilla mesenchymal cells. Biochem Biophys Res Commun 342: 1257-1262. doi:10.1016/j.bbrc.2006.02.101. PubMed: 16516858.
51. Huang GTJ, Sonoyama W, Liu Y, Liu H, Wang S, et al. (2008) The hidden treasure in apical papilla: the potential role in pulp/dentin regeneration and bioroot engineering. J Endod 34: 645-651. doi:10.1016/j.joen.2008.03.001. PubMed: 18498881.
52. Sonoyama W, Liu Y, Yamaza T, Tuan RS, Wang S, et al. (2008) Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: a pilot study. J Endod 34: 166-171. doi:10.1016/j.joen.2007.11.021. PubMed: 18215674.
53. Thomas HF, Kollar EJ, (1989) Differentiation of odontoblasts in grafted recombinants of murine epithelial root sheath and dental mesenchyme. Arch Oral Biol 34: 27-35. doi:10.1016/0003-9969(89)90043-5. PubMed: 2783039.
54. Lu X, Borchers AGM, Jolicoeur C, Rayburn H, Baker JC, et al. (2004) PTK7/CCK-4 is a novel regulator of planar cell polarity in vertebrates. Nature 430: 93-98. doi:10.1038/nature02677. PubMed: 15229603.
55. Boutros M, Paricio N, Strutt DI, Mlodzik M, (1998) Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94: 109-118. doi:10.1016/S0092-8674(00)81226-X. PubMed: 9674432.
56. Bikkavilli RK, Feigin ME, Malbon CC, (2008) Gαo mediates WNT-JNK signaling through Dishevelled 1 and 3, RhoA family members, and MEKK 1 and 4 in mammalian cells. J Cell Sci 121: 234-245. doi:10.1242/jcs.021964. PubMed: 18187455.
57. Oishi I, Suzuki H, Onishi N, Takada R, Kani S, et al. (2003) The receptor tyrosine kinase Ror2 is involved in noncanonical Wnt5a/JNK signalling pathway. Genes Cells 8: 645-654. doi:10.1046/j.1365-2443.2003.00662.x. PubMed: 12839624.
58. Obara N, Suzuki Y, Takeda M, (2006) Gene expression of β-catenin is up-regulated in inner dental epithelium and enamel knots during molar tooth morphogenesis in the mouse. Cell Tissue Res 325: 197-201. doi:10.1007/s00441-005-0136-6. PubMed: 16550360.
59. Christiansen JH, Coles EG, Wilkinson DG, (2000) Molecular control of neural crest formation, migration and differentiation. Curr Opin Cell Biol 12: 719-724. doi:10.1016/S0955-0674(00)00158-7. PubMed: 11063938.
60. Kurayoshi M, Oue N, Yamamoto H, Kishida M, Inoue A, et al. (2006) Expression of Wnt-5a is correlated with aggressiveness of gastric cancer by stimulating cell migration and invasion. Cancer Res 66: 10439-10448. doi:10.1158/0008-5472.CAN-06-2359. PubMed: 17079465.
61. Kikuchi A, Yamamoto H, Sato A, Matsumoto S, (2011) Wnt5a: its signalling, functions and implication in diseases. Acta Physiol, 204: 17-33. PubMed: 21518267.
62. Biz MT, Marques MR, Crema VO, Moriscot AS, dos Santos MF, (2010) GTPases RhoA and Rac1 are important for amelogenin and DSPP expression during differentiation of ameloblasts and odontoblasts. Cell Tissue Res 340: 459-470. doi:10.1007/s00441-010-0961-0. PubMed: 20387077.
63. Marinissen MJ, Chiariello M, Tanos T, Bernard O, Narumiya S, et al. (2004) The small GTP-binding protein RhoA regulates c-jun by a ROCK-JNK signaling axis. Mol Cell 14: 29-41. doi:10.1016/S1097-2765(04)00153-4. PubMed: 15068801.
64. Wang HR, Zhang Y, Ozdamar B, Ogunjimi AA, Alexandrova E, et al. (2003) Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 302: 1775-1779. doi:10.1126/science.1090772. PubMed: 14657501.
65. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS, (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6: 483-495. doi:10.1016/S1534-5807(04)00075-9. PubMed: 15068789.
66. Watanabe N, Kato T, Fujita A, Ishizaki T, Narumiya S, (1999) Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nat Cell Biol 1: 136-143. doi:10.1038/11056. PubMed: 10559899.
67. Allen WE, Jones GE, Pollard JW, Ridley AJ, (1997) Rho, Rac and Cdc42 regulate actin organization and cell adhesion in macrophages. J Cell Sci 110: 707-720. PubMed: 9099945.
68. Banyard J, Anand-Apte B, Symons M, Zetter BR, (2000) Motility and invasion are differentially modulated by Rho family GTPases. Oncogene 19: 580-591. doi:10.1038/sj.onc.1203338. PubMed: 10698528.
69. Allen WE, Zicha D, Ridley AJ, Jones GE, (1998) A role for Cdc42 in macrophage chemotaxis. J Cell Biol 141: 1147-1157. doi:10.1083/jcb.141.5.1147. PubMed: 9606207.
70. Cox EA, Sastry SK, Huttenlocher A, (2001) Integrin-mediated adhesion regulates cell polarity and membrane protrusion through the Rho family of GTPases. Mol Biol Cell 12: 265-277. PubMed: 11179414.
71. Vial E, Sahai E, Marshall CJ, (2003) ERK-MAPK signaling coordinately regulates activity of Rac1 and RhoA for tumor cell motility. Cancer Cell 4: 67-79. doi:10.1016/S1535-6108(03)00162-4. PubMed: 12892714.
72. Pertz O, Hodgson L, Klemke RL, Hahn KM, (2006) Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 440: 1069-1072. doi:10.1038/nature04665. PubMed: 16547516.
73. Kirchner J, Kam Z, Tzur G, Bershadsky AD, Geiger B, (2003) Live-cell monitoring of tyrosine phosphorylation in focal adhesions following microtubule disruption. J Cell Sci 116: 975-986. doi:10.1242/jcs.00284. PubMed: 12584242.
74. Alberts AS, Treisman R, (1998) Activation of RhoA and SAPK/JNK signalling pathways by the RhoA-specific exchange factor mNET1. EMBO J 17: 4075-4085. doi:10.1093/emboj/17.14.4075. PubMed: 9670022.
75. Teramoto H, Crespo P, Coso OA, Igishi T, Xu N, et al. (1996) The small GTP-binding protein Rho activates c-Jun N-terminal kinases/stress-activated protein kinases in human kidney 293T cells. J Biol Chem 271: 25731-25734. doi:10.1074/jbc.271.42.25731. PubMed: 8824197.
76. Strutt DI, Weber U, Mlodzik M, (1997) The role of RhoA in tissue polarity and Frizzled signalling. Nature 387: 292-295. doi:10.1038/387292a0. PubMed: 9153394.
77. Schambony A, Wedlich D, (2007) Wnt-5A/Ror2 regulate expression of XPAPC through an alternative noncanonical signaling pathway. Dev Cell 12: 779-792. doi:10.1016/j.devcel.2007.02.016. PubMed: 17488628.
78. Nomachi A, Nishita M, Inaba D, Enomoto M, Hamasaki M, et al. (2008) Receptor tyrosine kinase Ror2 mediates Wnt5a-induced polarized cell migration by activating c-Jun N-terminal kinase via actin-binding protein filamin A. J Biol Chem 283: 27973-27981. doi:10.1074/jbc.M802325200. PubMed: 18667433.
79. Javelaud D, Laboureau J, Gabison E, Verrecchia F, Mauviel A, (2003) Disruption of basal JNK activity differentially affects key fibroblast functions important for wound healing. J Biol Chem 278: 24624-24628. doi:10.1074/jbc.M301942200. PubMed: 12730213.