Identification of a Novel Link between the Protein Kinase NDR1 and TGFβ Signaling in Epithelial Cells

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Pot, Isabelle ^a   Patel, Shachi ^a   Deng, Lili ^a   Chandhoke, Amrita Singh ^a   Zhang, Chi ^b   Bonni, Azad ^b,c   Bonni, Shirin ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b HARVARD MEDICAL SCHOOL   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEAR DBF2 RELATED 1; PROTEIN KINASE; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; N-MYC DOWNSTREAM-REGULATED GENE 1 PROTEIN; ONCOPROTEIN; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE; SKIL PROTEIN, HUMAN; STK38 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; BREAST CELL; CELL CYCLE ARREST; CELL NUCLEUS; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME DEGRADATION; ENZYME PURIFICATION; ENZYME REGULATION; EPITHELIUM CELL; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; ANIMAL; CELL CYCLE CHECKPOINT; CELL LINE; CELL PROLIFERATION; CYTOLOGY; GENE EXPRESSION REGULATION; METABOLISM; PHOSPHORYLATION; PROTEIN DEGRADATION;

ANIMALS; CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; CELL LINE; CELL PROLIFERATION; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA;

EID: 84879495654     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067178     Document Type: Article

References (76)

1. Massague J, (1990) The transforming growth factor-beta family. Annu Rev Cell Biol 6: 597-641.
2. Roberts AB, Sporn MB (1990) The transforming growth factor-betas. In: Sporn MB, Roberts AB, editors. Peptide growth factors and their receptors. Heidelberg: Springer-Verlag. 419-472.
3. Sporn MB, Roberts AB, (1990) TGF-beta: problems and prospects. Cell Regul 12: 875-882.
4. Wu MY, Hill CS, (2009) Tgf-beta superfamily signaling in embryonic development and homeostasis. Dev Cell 16: 329-343.
5. Blobe GC, Schiemann WP, Lodish HF, (2000) Role of transforming growth factor beta in human disease. N Engl J Med 342: 1350-1358.
6. Lan HY, (2011) Diverse roles of TGF-beta/Smads in renal fibrosis and inflammation. Int J Biol Sci 7: 1056-1067.
7. Schmierer B, Hill CS, (2007) TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility. Nat Rev Mol Cell Biol 8: 970-982.
8. Tatler AL, Jenkins G, (2012) TGF-beta Activation and Lung Fibrosis. Proc Am Thorac Soc 9: 130-136.
9. Iwano M, (2010) EMT and TGF-beta in renal fibrosis. Front Biosci (Schol Ed) 2: 229-238.
10. Galliher AJ, Neil JR, Schiemann WP, (2006) Role of transforming growth factor-beta in cancer progression. Future Oncol 2: 743-763.
11. Kim SJ, Letterio J, (2003) Transforming growth factor-beta signaling in normal and malignant hematopoiesis. Leukemia 17: 1731-1737.
12. Massague J, Blain SW, Lo RS, (2000) TGFbeta signaling in growth control, cancer, and heritable disorders. Cell 103: 295-309.
13. Rahimi RA, Leof EB, (2007) TGF-beta signaling: a tale of two responses. J Cell Biochem 102: 593-608.
14. Meulmeester E, Ten Dijke P, (2010) The dynamic roles of TGF-beta in cancer. J Pathol 223: 205-218.
15. Attisano L, Wrana JL, Lopez-Casillas F, Massague J, (1994) TGF-beta receptors and actions. Biochim Biophys Acta 1222: 71-80.
16. Huang T, David L, Mendoza V, Yang Y, Villarreal M, et al. (2011) TGF-beta signalling is mediated by two autonomously functioning TbetaRI:TbetaRII pairs. EMBO J 30: 1263-1276.
17. Massague J, Attisano L, Wrana JL, (1994) The TGF-beta family and its composite receptors. Trends Cell Biol 4: 172-178.
18. Wrana JL, Carcamo J, Attisano L, Cheifetz S, Zentella A, et al. (1992) The type II TGF-β Receptor Signals Diverse Responses in Co-Operation with the Type I Receptor. Cold Spring Harbour Symposia on Quantitative Biology. 81-86.
19. Wrana JL, Tran H, Attisano L, Arora K, Childs SR, et al. (1994) Two distinct transmembrane serine/threonine kinases from Drosophila form an activin receptor complex. Mol Cell Biol 14: 944-950.
20. Miyazono K, Suzuki H, Imamura T, (2003) Regulation of TGF-beta signaling and its roles in progression of tumors. Cancer Sci 94: 230-234.
21. Wieser R, Wrana JL, Massague J, (1995) GS domain mutations that constitutively activate TβR-I, the downstream signalling component in the TGF-β receptor complex. EMBO J 14: 2199-2208.
22. Wrana JL, Attisano L, Wieser R, Ventura F, Massague J, (1994) Mechanism of activation of the TGF-β receptor. Nature 370: 341-347.
23. Massague J, Wotton D, (2000) Transcriptional control by the TGF-beta/Smad signaling system. Embo J 19: 1745-1754.
24. Shi Y, Massague J, (2003) Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113: 685-700.
25. Abdollah S, Macias-Silva M, Tsukazaki T, Hayashi H, Attisano L, et al. (1997) TbetaRI phosphorylation of Smad2 on Ser465 and Ser467 is required for Smad2-Smad4 complex formation and signaling. J Biol Chem 272: 27678-27685.
26. Souchelnytskyi S, Tamaki K, Engstrom U, Wernstedt C, ten Dijke P, et al. (1997) Phosphorylation of Ser465 and Ser467 in the C terminus of Smad2 mediates interaction with Smad4 and is required for transforming growth factor-beta signaling. J Biol Chem 272: 28107-28115.
27. Lagna G, Hata A, Hemmati-Brivanlou A, Massagué J, (1996) Partnership between DPC4 and SMAD proteins in TGF- signalling pathways. Nature 383: 832-836.
28. Lonn P, Moren A, Raja E, Dahl M, Moustakas A, (2009) Regulating the stability of TGFbeta receptors and Smads. Cell Res 19: 21-35.
29. Feng XH, Derynck R (2005) Specificity and Versatility in TGF- Signaling Through Smads. Annu Rev Cell Dev Biol.
30. Wotton D, Massague J, (2001) Smad transcriptional corepressors in TGF beta family signaling. Curr Top Microbiol Immunol 254: 145-164.
31. Wrana JL, Attisano L (2000) The Smad pathway. Cyto Growth Factor Rev in press.
32. Luo K, (2004) Ski and SnoN: negative regulators of TGF-beta signaling. Curr Opin Genet Dev 14: 65-70.
33. Pot I, Bonni S, (2008) SnoN in TGF-beta signaling and cancer biology. Curr Mol Med 8: 319-328.
34. Pot I, Ikeuchi Y, Bonni A, Bonni S, (2010) SnoN: bridging neurobiology and cancer biology. Curr Mol Med 10: 667-673.
35. Bonni S, Bonni A, (2012) SnoN signaling in proliferating cells and postmitotic neurons. FEBS Lett 586: 1977-1983.
36. Deheuninck J, Luo K, (2009) Ski and SnoN, potent negative regulators of TGF-beta signaling. Cell Res 19: 47-57.
37. Stroschein SL, Wang W, Zhou S, Zhou Q, Luo K, (1999) Negative feedback regulation of TGF-beta signaling by the SnoN oncoprotein. Science 286: 771-774.
38. Sun Y, Liu X, Ng-Eaton E, Lodish HF, Weinberg RA, (1999) SnoN and Ski protooncoproteins are rapidly degraded in response to transforming growth factor beta signaling. Proc Natl Acad Sci U S A 96: 12442-12447.
39. Sarker KP, Kataoka H, Chan A, Netherton SJ, Pot I, et al. (2008) ING2 as a novel mediator of transforming growth factor-beta-dependent responses in epithelial cells. J Biol Chem 283: 13269-13279.
40. Sarker KP, Wilson SM, Bonni S, (2005) SnoN is a cell type-specific mediator of transforming growth factor-beta responses. J Biol Chem 280: 13037-13046.
41. Hergovich A, Stegert MR, Schmitz D, Hemmings BA, (2006) NDR kinases regulate essential cell processes from yeast to humans. Nat Rev Mol Cell Biol 7: 253-264.
42. Cornils H, Kohler RS, Hergovich A, Hemmings BA, (2011) Downstream of human NDR kinases: impacting on c-myc and p21 protein stability to control cell cycle progression. Cell Cycle 10: 1897-1904.
43. Cornils H, Kohler RS, Hergovich A, Hemmings BA, (2011) Human NDR kinases control G(1)/S cell cycle transition by directly regulating p21 stability. Mol Cell Biol 31: 1382-1395.
44. Cornils H, Stegert MR, Hergovich A, Hynx D, Schmitz D, et al. (2010) Ablation of the kinase NDR1 predisposes mice to the development of T cell lymphoma. Sci Signal 3: ra47.
45. Vichalkovski A, Gresko E, Cornils H, Hergovich A, Schmitz D, et al. (2008) NDR kinase is activated by RASSF1A/MST1 in response to Fas receptor stimulation and promotes apoptosis. Curr Biol 18: 1889-1895.
46. Ultanir SK, Hertz NT, Li G, Ge WP, Burlingame AL, et al. (2012) Chemical genetic identification of NDR1/2 kinase substrates AAK1 and Rabin8 Uncovers their roles in dendrite arborization and spine development. Neuron 73: 1127-1142.
47. Adeyinka A, Emberley E, Niu Y, Snell L, Murphy LC, et al. (2002) Analysis of gene expression in ductal carcinoma in situ of the breast. Clin Cancer Res 8: 3788-3795.
48. Hergovich A, Cornils H, Hemmings BA, (2008) Mammalian NDR protein kinases: from regulation to a role in centrosome duplication. Biochim Biophys Acta 1784: 3-15.
49. Bonni S, Wang HR, Causing CG, Kavsak P, Stroschein SL, et al. (2001) TGF-beta induces assembly of a Smad2-Smurf2 ubiquitin ligase complex that targets SnoN for degradation. Nat Cell Biol 3: 587-595.
50. Stroschein SL, Bonni S, Wrana JL, Luo K, (2001) Smad3 recruits the anaphase-promoting complex for ubiquitination and degradation of SnoN. Genes Dev 15: 2822-2836.
51. Nakatani Y, Ogryzko V, (2003) Immunoaffinity purification of mammalian protein complexes. Methods Enzymol 370: 430-444.
52. Puig O, Caspary F, Rigaut G, Rutz B, Bouveret E, et al. (2001) The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24: 218-229.
53. Barrios-Rodiles M, Brown KR, Ozdamar B, Bose R, Liu Z, et al. (2005) High-throughput mapping of a dynamic signaling network in mammalian cells. Science 307: 1621-1625.
54. Kortlever RM, Nijwening JH, Bernards R, (2008) Transforming growth factor-beta requires its target plasminogen activator inhibitor-1 for cytostatic activity. J Biol Chem 283: 24308-24313.
55. Wilkins-Port CE, Ye Q, Mazurkiewicz JE, Higgins PJ, (2009) TGF-beta1+ EGF-initiated invasive potential in transformed human keratinocytes is coupled to a plasmin/MMP-10/MMP-1-dependent collagen remodeling axis: role for PAI-1. Cancer Res 69: 4081-4091.
56. Wrana JL, Attisano L, Carcamo J, Zentella A, Doody J, et al. (1992) TGF beta signals through a heteromeric protein kinase receptor complex. Cell 71: 1003-1014.
57. Miettinen PJ, Ebner R, Lopez AR, Derynck R, (1994) TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J Cell Biol 127: 2021-2036.
58. Varelas X, Samavarchi-Tehrani P, Narimatsu M, Weiss A, Cockburn K, et al. (2010) The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-beta-SMAD pathway. Dev Cell 19: 831-844.
59. Levy L, Howell M, Das D, Harkin S, Episkopou V, et al. (2007) Arkadia activates Smad3/Smad4-dependent transcription by triggering signal-induced SnoN degradation. Mol Cell Biol 27: 6068-6083.
60. Nagano Y, Mavrakis KJ, Lee KL, Fujii T, Koinuma D, et al. (2007) Arkadia induces degradation of SnoN and c-Ski to enhance transforming growth factor-beta signaling. J Biol Chem 282: 20492-20501.
61. Wan Y, Liu X, Kirschner MW, (2001) The anaphase-promoting complex mediates TGF-beta signaling by targeting SnoN for destruction. Mol Cell 8: 1027-1039.
62. Stegmuller J, Huynh MA, Yuan Z, Konishi Y, Bonni A, (2008) TGFbeta-Smad2 signaling regulates the Cdh1-APC/SnoN pathway of axonal morphogenesis. J Neurosci 28: 1961-1969.
63. Netherton SJ, Bonni S, (2010) Suppression of TGFbeta-induced epithelial-mesenchymal transition like phenotype by a PIAS1 regulated sumoylation pathway in NMuMG epithelial cells. PLoS One 5: e13971.
64. von Both I, Silvestri C, Erdemir T, Lickert H, Walls JR, et al. (2004) Foxh1 is essential for development of the anterior heart field. Dev Cell 7: 331-345.
65. Huynh MA, Ikeuchi Y, Netherton S, de la Torre-Ubieta L, Kanadia R, et al. (2011) An isoform-specific SnoN1-FOXO1 repressor complex controls neuronal morphogenesis and positioning in the mammalian brain. Neuron 69: 930-944.
66. Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, et al. (1988) Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106: 761-771.
67. DuBridge RB, Tang P, Hsia HC, Leong PM, Miller JH, et al. (1987) Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol Cell Biol 7: 379-387.
68. Heiz M, Grunberg J, Schubiger PA, Novak-Hofer I, (2004) Hepatocyte growth factor-induced ectodomain shedding of cell adhesion molecule L1: role of the L1 cytoplasmic domain. J Biol Chem 279: 31149-31156.
69. Owens RB, (1974) Glandular epithelial cells from mice: a method for selective cultivation. J Natl Cancer Inst 52: 1375-1378.
70. Owens RB, Smith HS, Hackett AJ, (1974) Epithelial cell cultures from normal glandular tissue of mice. J Natl Cancer Inst 53: 261-269.
71. Yingling JM, Das P, Savage C, Zhang M, Padgett RW, et al. (1996) Mammalian dwarfins are phosphorylated in response to transforming growth factor beta and are implicated in control of cell growth. Proc Natl Acad Sci U S A 93: 8940-8944.
72. Hsu YH, Sarker KP, Pot I, Chan A, Netherton SJ, et al. (2006) Sumoylated SnoN represses transcription in a promoter-specific manner. J Biol Chem 281: 33008-33018.
73. Bondareva A, Downey CM, Ayres F, Liu W, Boyd SK, et al. (2009) The lysyl oxidase inhibitor, beta-aminopropionitrile, diminishes the metastatic colonization potential of circulating breast cancer cells. PLoS One 4: e5620.
74. Cailleau R, Young R, Olive M, Reeves WJ Jr, (1974) Breast tumor cell lines from pleural effusions. J Natl Cancer Inst 53: 661-674.
75. Eapen SA, Netherton SJ, Sarker KP, Deng L, Chan A, et al. (2012) Identification of a Novel Function for the Chromatin Remodeling Protein ING2 in Muscle Differentiation. PLoS One 7: e40684.
76. Scherr M, Morgan MA, Eder M, (2003) Gene silencing mediated by small interfering RNAs in mammalian cells. Curr Med Chem 10: 245-256.