Role of ERK/mTOR signaling in TGFβ-modulated focal adhesion kinase mRNA stability and protein synthesis in cultured rat IEC-6 intestinal epithelial cells

Cell and Tissue Research

Volumn 336, Issue 2, 2009, Pages 213-223

  Suer, Silke ^a,b   Ampasala, Dinakar ^a,b   Walsh, Mary F ^a,b   Basson, Marc D ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Extracellular signal regulated kinases (ERK); Focal adhesion kinase (FAK); Mammalian target of rapamycin (mTOR); mRNA; Rat IEC 6 intestinal epithelial cells; Transforming growth factor (TGF )

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CYCLOHEXIMIDE; DACTINOMYCIN; FOCAL ADHESION KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; RAPAMYCIN; S6 KINASE; SMAD PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL LEVEL; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; INTESTINE EPITHELIUM CELL; MODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RAT; RNA STABILITY; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSLATION INITIATION; WOUND CLOSURE;

ANIMALS; CARRIER PROTEINS; CELLS, CULTURED; ENTEROCYTES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLAVONOIDS; FOCAL ADHESION KINASE 1; MAP KINASE SIGNALING SYSTEM; PHOSPHOPROTEINS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN BIOSYNTHESIS; PROTEIN KINASES; PROTEIN STABILITY; RATS; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; RNA STABILITY; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA; WOUND HEALING;

MAMMALIA; RATTUS;

EID: 67349231247     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-009-0776-z     Document Type: Article

References (55)

1. M Agochiya VG Brunton DW Owens EK Parkinson C Paraskeva WN Keith MC Frame 1999 Increased dosage and amplification of the focal adhesion kinase gene in human cancer cells Oncogene 18 5646 5653
2. J Averous CG Proud 2006 When translation meets transformation: the mTOR story Oncogene 25 6423 6435
3. JA Barnard RD Beauchamp RJ Coffey HL Moses 1989 Regulation of intestinal epithelial cell growth by transforming growth factor type beta Proc Natl Acad Sci USA 86 1578 1582
4. JA Barnard WH Polk HL Moses RJ Coffey 1991 Production of transforming growth factor-alpha by normal rat small intestine Am J Physiol 261 C994 C1000
5. CT Basson O Kocher MD Basson A Asis JA Madri 1992 Differential modulation of vascular cell integrin and extracellular matrix expression in vitro by TGF-beta 1 correlates with reciprocal effects on cell migration J Cell Physiol 153 118 128
6. MD Basson MA Sanders R Gomez J Hatfield R Vanderheide V Thamilselvan J Zhang MF Walsh 2006 Focal adhesion kinase protein levels in gut epithelial motility Am J Physiol Gastrointest Liver Physiol 291 G491 G499
7. CA Beelman R Parker 1995 Degradation of mRNA in eukaryotes Cell 81 179 183
8. Bermudez O, Marchetti S, Pages G, Gimond C (2008) Post-translational regulation of the ERK phosphatase DUSP6/MKP3 by the mTOR pathway. Oncogene (in press)
9. F Blanchette N Rivard P Rudd F Grondin L Attisano CM Dubois 2001 Cross-talk between the p42/p44 MAP kinase and Smad pathways in transforming growth factor beta 1-induced furin gene transactivation J Biol Chem 276 33986 33994
10. V Bouchard MJ Demers S Thibodeau V Laquerre N Fujita T Tsuruo JF Beaulieu R Gauthier A Vezina L Villeneuve PH Vachon 2007 Fak/Src signaling in human intestinal epithelial cell survival and anoikis: differentiation state-specific uncoupling with the PI3-K/Akt-1 and MEK/Erk pathways J Cell Physiol 212 717 728
11. T Cai QY Lei LY Wang XL Zha 2000 TGF-beta 1 modulated the expression of alpha 5 beta 1 integrin and integrin-mediated signaling in human hepatocarcinoma cells Biochem Biophys Res Commun 274 519 525
12. JY Chow KT Quach BL Cabrera JA Cabral SE Beck JM Carethers 2007 RAS/ERK modulates TGFbeta-regulated PTEN expression in human pancreatic adenocarcinoma cells Carcinogenesis 28 2321 2327
13. C Constantinou MJ Clemens 2007 Regulation of translation factors eIF4GI and 4E-BP1 during recovery of protein synthesis from inhibition by p53 Cell Death Differ 14 576 585
14. MC Cushing PD Mariner JT Liao EA Sims KS Anseth 2008 Fibroblast growth factor represses Smad-mediated myofibroblast activation in aortic valvular interstitial cells FASEB J 22 1769 1777
15. V Golubovskaya A Kaur W Cance 2004 Cloning and characterization of the promoter region of human focal adhesion kinase gene: nuclear factor kappa B and p53 binding sites Biochim Biophys Acta 1678 111 125
16. PA Hall PJ Coates B Ansari D Hopwood 1994 Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis J Cell Sci 107 3569 3577
17. SK Hanks L Ryzhova NY Shin J Brabek 2003 Focal adhesion kinase signaling activities and their implications in the control of cell survival and motility Front Biosci 8 d982 d996
18. MT Hartsough KM Mulder 1995 Transforming growth factor beta activation of p44MAPK in proliferating cultures of epithelial cells J Biol Chem 270 7117 7124
19. T Hayashida AC Poncelet SC Hubchak HW Schnaper 1999 TGF-beta1 activates MAP kinase in human mesangial cells: a possible role in collagen expression Kidney Int 56 1710 1720
20. HW Jeong IS Kim 2004 TGF-beta1 enhances betaig-h3-mediated keratinocyte cell migration through the alpha3beta1 integrin and PI3K J Cell Biochem 92 770 780
21. M Kohno J Pouyssegur 2006 Targeting the ERK signaling pathway in cancer therapy Ann Med 38 200 211
22. M Kretzschmar J Doody I Timokhina J Massague 1999 A mechanism of repression of TGFbeta/Smad signaling by oncogenic Ras Genes Dev 13 804 816
23. SM Kutz J Hordines PJ McKeown-Longo PJ Higgins 2001 TGF-beta1-induced PAI-1 gene expression requires MEK activity and cell-to-substrate adhesion J Cell Sci 114 3905 3914
24. S Lamouille R Derynck 2007 Cell size and invasion in TGF-beta-induced epithelial to mesenchymal transition is regulated by activation of the mTOR pathway J Cell Biol 178 437 451
25. H Le Pabic A L'Helgoualc'h A Coutant UM Wewer G Baffet B Clement N Theret 2005 Involvement of the serine/threonine p70S6 kinase in TGF-beta1-induced ADAM12 expression in cultured human hepatic stellate cells J Hepatol 43 1038 1044
26. Lin MT, Kuo IH, Chen CC, Chu CY, Chen HY, Lin BR, Sureshbabu M, Shih HJ, Kuo ML (2008) Involvement of HIF-1alpha-dependent PAI-1 up-regulation in Cyr61/CCN1 induced gastric cancer cell invasion. J Biol Chem (in press)
27. L Ma Z Chen H Erdjument-Bromage P Tempst PP Pandolfi 2005 Phosphorylation and functional inactivation of TSC2 by Erk implications for tuberous sclerosis and cancer pathogenesis Cell 121 179 193
28. MC Maa JC Lee YJ Chen YJ Chen YC Lee ST Wang CC Huang NH Chow TH Leu 2007 Eps8 facilitates cellular growth and motility of colon cancer cells by increasing the expression and activity of focal adhesion kinase J Biol Chem 282 19399 19409
29. Y Mamane E Petroulakis O LeBacquer N Sonenberg 2006 mTOR, translation initiation and cancer Oncogene 25 6416 6422
30. P Mitchell D Tollervey 2000 mRNA stability in eukaryotes Curr Opin Genet Dev 10 193 198
31. SK Mitra DA Hanson DD Schlaepfer 2005 Focal adhesion kinase: in command and control of cell motility Nat Rev Mol Cell Biol 6 56 68
32. A Moustakas CH Heldin 2005 Non-Smad TGF-beta signals J Cell Sci 118 3573 3584
33. K Nakagawa S Sogo K Hioki R Tokunaga S Taketani 1998 Acquisition of cell adhesion and induction of focal adhesion kinase of human colon cancer Colo 201 cells by retinoic acid-induced differentiation Differentiation 62 249 257
34. SF Newbury 2006 Control of mRNA stability in eukaryotes Biochem Soc Trans 34 30 34
35. - symporter (NIS) mediates active iodide uptake in the intestine. Am J Physiol Cell Physiol (in press)
36. Owen CR, Yuan L, Basson MD (2008) Smad3 knockout mice exhibit impaired intestinal mucosal healing. Lab Invest (in press)
37. JT Parsons 2003 Focal adhesion kinase: the first ten years J Cell Sci 116 1409 1416
38. JT Parsons KH Martin JK Slack JM Taylor SA Weed 2000 Focal adhesion kinase: a regulator of focal adhesion dynamics and cell movement Oncogene 19 5606 5613
39. A Quaroni J Wands RL Trelstad KJ Isselbacher 1979 Epithelioid cell cultures from rat small intestine. Characterization by morphologic and immunologic criteria J Cell Biol 80 248 265
40. JM Rhoads X Niu J Odle LM Graves 2006 Role of mTOR signaling in intestinal cell migration Am J Physiol Gastrointest Liver Physiol 291 G510 G517
41. A Sanchez-Capelo 2005 Dual role for TGF-beta1 in apoptosis Cytokine Growth Factor Rev 16 15 34
42. E Sancho E Batlle H Clevers 2004 Signaling pathways in intestinal development and cancer Annu Rev Cell Dev Biol 20 695 723
43. JF Santibanez M Iglesias P Frontelo J Martinez M Quintanilla 2000 Involvement of the Ras/MAPK signaling pathway in the modulation of urokinase production and cellular invasiveness by transforming growth factor-beta(1) in transformed keratinocytes Biochem Biophys Res Commun 273 521 527
44. RS Sellers CC Capen TJ Rosol 2002 Messenger RNA stability of parathyroid hormone-related protein regulated by transforming growth factor-beta1 Mol Cell Endocrinol 188 37 46
45. A Sturm AU Dignass 2008 Epithelial restitution and wound healing in inflammatory bowel disease World J Gastroenterol 14 348 353
46. IL Szabo R Pai MK Jones GR Ehring H Kawanaka AS Tarnawski 2002 Indomethacin delays gastric restitution: association with the inhibition of focal adhesion kinase and tensin phosphorylation and reduced actin stress fibers Exp Biol Med (Maywood) 227 412 424
47. T Tanigawa R Pai T Arakawa K Higuchi AS Tarnawski 2005 TGF-beta signaling pathway: its role in gastrointestinal pathophysiology and modulation of ulcer healing J Physiol Pharmacol 56 3 13
48. A Tarnawski IL Szabo SS Husain B Soreghan 2001 Regeneration of gastric mucosa during ulcer healing is triggered by growth factors and signal transduction pathways J Physiol (Paris) 95 337 344
49. V Vaira CW Lee HL Goel S Bosari LR Languino DC Altieri 2007 Regulation of survivin expression by IGF-1/mTOR signaling Oncogene 26 2678 2684
50. MF Walsh V Thamilselvan R Grotelueschen L Farhana M Basson 2003 Absence of adhesion triggers differential FAK and SAPKp38 signals in SW620 human colon cancer cells that may inhibit adhesiveness and lead to cell death Cell Physiol Biochem 13 135 146
51. Walsh MF, Ampasala DR, Rishi AK, Basson MD (2008a) TGF-beta1 modulates focal adhesion kinase expression in rat intestinal epithelial IEC-6 cells via stimulatory and inhibitory Smad binding elements. Biochim Biophys Acta (in press)
52. MF Walsh DR Ampasala J Hatfield R Vander Heide S Suer AK Rishi MD Basson 2008 Transforming growth factor-beta stimulates intestinal epithelial focal adhesion kinase synthesis via smad- and p38-dependent mechanisms Am J Pathol 173 385 399
53. CF Yu MA Sanders MD Basson 2000 Human caco-2 motility redistributes FAK and paxillin and activates p38 MAPK in a matrix-dependent manner Am J Physiol Gastrointest Liver Physiol 278 G952 G966
54. J Yue RS Frey KM Mulder 1999 Cross-talk between the Smad1 and Ras/MEK signaling pathways for TGFbeta Oncogene 18 2033 2037
55. HM Zhang KM Keledjian JN Rao T Zou L Liu BS Marasa SR Wang L Ru ED Strauch JY Wang 2006 Induced focal adhesion kinase expression suppresses apoptosis by activating NF-kappaB signaling in intestinal epithelial cells Am J Physiol Cell Physiol 290 C1310 1320