TGFβ1-induced activation of ATM and p53 mediates apoptosis in a Smad7-dependent manner

Cell Cycle

Volumn 5, Issue 23, 2006, Pages 2787-2795

  Zhang, Shouting ^a   Ekman, Maria ^a   Thakur, Noopur ^a   Bu, Shizhong ^a   Davoodpour, Padideh ^a   Grimsby, Susanne ^a   Tagami, Seicchi ^a   Heldin, Carl Henrik ^a   Landström, Marene ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Apoptosis; ATM; p53; Prostate cancer; Smad

Indexed keywords

PROTEIN P53; SMAD8 PROTEIN; ATM PROTEIN; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHOSERINE; PROTEIN SERINE THREONINE KINASE; SMAD7 PROTEIN; SMAD7 PROTEIN, HUMAN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA1; TUMOR SUPPRESSOR PROTEIN;

APOPTOSIS; ARTICLE; HUMAN; HUMAN CELL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; CELL CYCLE; CYTOLOGY; DRUG EFFECT; EPITHELIUM CELL; METABOLISM; MOUSE; PROTEIN BINDING;

ANIMALS; APOPTOSIS; CELL CYCLE; CELL CYCLE PROTEINS; DNA-BINDING PROTEINS; EPITHELIAL CELLS; HUMANS; MICE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOSERINE; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RNA, SMALL INTERFERING; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 33845388985     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.5.23.3523     Document Type: Article

References (50)

1. 1 arrest, p53, and Rb. Cancer Res 1996; 56:3645-50.
2. Schuster N, Krieglstein K. Mechanisms of TGF-beta-mediated apoptosis. Cell Tissue Res 2002; 307:1-14.
3. Siegel PM, Massagué J. Cytostatic and apoptotic actions of TGF-β in homeostasis and cancer. Nat Rev Cancer 2003; 11:807-21.
4. Sanchez-Capelo A. Dual role for TGF-beta1 in apoptosis. Cytokine Growth Factor Rev 2005; 1:15-34.
5. Wakefield LM, Roberts AB. TGF-β signaling: Positive and negative effects on tumorigenesis. Curr Opin Genet Dev 2002; 1:22-9.
6. Bierie B, Moses HL. TGF-beta and cancer. Cytokine Growth Factor Rev 2005, [Epub ahead of print].
7. Thomas DA, Massagué J. TGF-β directly targets cytotoxic T cell functions during tumor evasion of immune surveillance. Cancer Cell 2005; 5:369-80.
8. Heldin CH, Miyazono K, ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 1997; 390:465-71.
9. Massagué J. How cells read TGF-β signals. Nat Rev Mol Cell Biol 2000; 1:169-78.
10. Shi Y, Massagué J. Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 2003; 113:685-700.
11. Nagarajan RP, Zhang J, Li W, Chen Y. Regulation of Smad7 promoter by direct association with Smad3 and Smad4. J Biol Chem 1999; 274:33412-18.
12. Brodin G, Ahgren A, ten Dijke P, Heldin CH, Heuchel R. Efficient TGF-beta induction of the Smad7 gene requires cooperation between AP-1, Sp1, and Smad proteins on the mouse Smad7 promoter. J Biol Chem 2000; 275:29023-30.
13. Denissova NG, Pouponnot C, Long J, He D, Liu F. Transforming growth factor β-inducible independent binding of SMAD to the Smad7 promoter. Proc Natl Acad Sci 2000; 97:6397-6402.
14. Itoh S, Landström M, Itoh F, Heldin N-E, Hermansson A, Heldin CH, ten Dijke P. Transforming growth factor TGF-β1 induced nuclear export of Smad7. J Biol Chem 1998; 273:29195-201.
15. Kavsak P, Rasmussen RK, Causing CG, Bonni S, Zhu H, Thomsen GH, Wrana JL. Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation. Mol Cell 2000; 6:1365-75.
16. Ebisawa T, Fukuchi M, Murakami G, Chiba T, Tanaka K, Imamura T, Miyazono K. Smurf1 interacts with transforming growth factor-beta type I receptor through Smad7 and induces receptor degradation. J Biol Chem 2001; 276:12477-480.
17. Edlund S, Bu S, Schuster N, Aspenström P, Heldin NE, ten Dijke P, Heldin CH, Landström M. TGF-β1-induced apoptosis of prostate cancer cells involves Smad7-dependent activation nduced of p38 by TAK1 and MKK3. Mol Biol Cell 2003; 14:529-44.
18. Hanafusa H, Ninomiya-Tsuji J, Masuyama N, Nishita M, Fujisawa J, Shibuya H, Matsumoto K, Nishida E. Involvement of the p38 mitogen-activated protein kinase pathway in transforming growth factor-beta-induced gene expression. J Biol Chem 1999; 274:27161-167.
19. Bakin AV, Rinehart C, Tomlinson AK, Arteaga CL. p38 mitogen-activated protein kinase is required for TGFbeta-mediated fibroblastic transdifferentiation and cell migration. J Cell Sci 2002; 115:3193-06.
20. Edlund S, Landstrom M, Heldin CH, Aspenstrom P. Transforming growth factor-beta-induced mobilization of actin cytoskeleton requires signaling by small GTPases Cdc42 and RhoA. Mol Biol Cell 2002; 3:902-14.
21. Yu L, Hebert MC, Zhang YE. TGF-beta receptor-activated p38 MAP kinase mediates Smad-independent TGF-beta responses. EMBO J 2002; 21:3749-59.
22. Itoh S, Thorikay M, Kowanetz M, Moustakas A, Itoh F, Heldin CH, ten Dijke P. Elucidation of Smad requirement in transforming growth factor-beta type I receptor-induced responses. J Biol Chem 2003; 278:3751-61.
23. Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 2003; 425:577-84.
24. Feng XH, Derynck R. Specificity and versatility in TGF-beta signalling through Smads. Annu Rev Cell Dev Biol 2005; 21:659-93.
25. Moustakas A, Heldin CH. Non-Smad TGF-beta signals. J Cell Sci 2005; 118:3573-84.
26. Zarubin T, Han J. Activation and signaling of the p38 MAP kinase pathway. Cell Res 2005; 1:11-8.
27. Jacks T. Lessons from the p53 mutant mouse. J Cancer Res Clin Oncol 1996; 122:319-27.
28. Bode AM, Dong Z. Post-translational modification of p53 in tumorigenesis Nat Rev Cancer 2004; 10:793-805.
29. Rogakou EP, Boon C, Redon C, Bonner WM. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 1999; 146:905-16.
30. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature 2000; 408:307-10.
31. Shen KC, Heng H, Wang Y, Lu S, Liu G, Deng CX, Brooks SC, Wang YA. ATM and p21 cooperate to suppress aneuploidy and subsequent tumor development. Cancer Res 2005; 65:8747-53.
32. Komarov PG, Komarova EA, Kondratov RV, Christov-Tselkov K, Coon JS, Chernov MV, Gudkov AV. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 1999; 285:1733-37.
33. Nakano K, Vousden KH. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 2001; 2:683-94.
34. Yu J, Zhang L, Hwang PM, Kinzler KW, Vogelstein B. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell 2001; 3:673-82.
35. Bulavin DV, Saito S, Hollander MC, Sakaguchi K, Anderson CW, Apella E, Fornace Jr AJ. Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation. EMBO J 1999; 18:6845-54.
36. She QB, Chen N, Dong Z. ERKs and p38 kinase phosphorylate p53 protein at serine 15 in response to UV radiation. J Biol Chem 2000; 275:20444-49.
37. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003; 421:499-506.
38. Sarkaria JN, Busby EC, Tibbetts RS, Roos P, Taya Y, Karnitz LM, Abraham RT. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent caffeine. Cancer Res1999; 59:4375-82.
39. Sarkaria JN, Tibbetts RS, Busby EC, Kennedy AP, Hill DE, Abraham RT. Inhibition of phosphoinositide 3-kinase related kinases by the radiosensitizing agent wortmannin. Cancer Res 1998; 58:4375-82.
40. Rubin SJ, Hallahan DE, Ashman CR, Brachman DG, Beckett MA, Virudachalam S, Yandell DW, Weichselbaum RR. Two prostate carcinoma cell lines demonstrate abnormalities in tumor suppressor genes. J Surg Oncol 1991; 46:31-6.
41. Carroll AG, Voeller HJ, Sugars L, Gelmann EP. p53 oncogene mutations in three human prostate cancer cell lines. Prostate 1993; 23:123-34.
42. Kops GJ, Weaver BA, Cleveland DW. On the road to cancer: Aneuploidy and the mitotic checkpoint. Nat Rev Cancer 2005; 10:773-85.
43. Rieder CL, Maiato H. Stuck in division or passing through: What happens when cells cannot satisfy the spindle assembly checkpoint. Dev Cell 2004; 5:637-51.
44. Landstrom M, Heldin NE, Bu S, Hermansson A, Itoh S, ten Dijke P, Heldin CH. Smad7 mediates apoptosis induced by transforming growth factor beta in prostatic carcinoma cells. Curr Biol 2000; 10:535-38.
45. Ewan KB, Henshall-Powell RL, Ravani SA, Pajares MJ, Arteaga C, Warters R, Akhurst RJ, Barcellos-Hoff MH. Transforming growth factor- beta 1 mediates cellular response to DNA damage in situ. Cancer Res 2002; 62:5627-31.
46. Barcellos-Hoff MH. Integrative radiation carcinogenesis: Interactions between cell and tissue responses to DNA damage. Semin Cancer Biol 2005; 2:138-48.
47. Franzen P, Ichijo H, Miyazono K. Different signals mediate transforming growth factor-beta 1-induced growth inhibition and extracellular matrix production in prostatic carcinoma cells. Exp Cell Res 1993; 207:1-7.
48. Brodin G, ten Dijke P, Funa K, Heldin CH, Landström M. Increased Smad expression and activation is associated with apoptosis in normal and malignant prostate after castration. Cancer Res 1999; 59:2731-38.
49. Edlund S, Lee SY, Grimsby S, Zhang S, Aspenström P, Heldin CH, Landström M. Interaction between Smad7 and β-catenin: Importance for TGF-beta-induced apoptosis. Mol Cell Biol 2005; 4:1475-88.
50. Wong HK, Fricker M, Wyttenbach A, Villunger A, Michalak EM, Strasser A, Tolkovsky AM. Mutually exclusive subsets of BH3-only proteins are activated by the p53 and c-Jun N-terminal kinase/c-Jun signaling pathways during cortical neuron apoptosis induced by arsenite. Mol Cell Biol 2005; 25:8732-47.