Hypoxic conversion of SMAD7 function from an inhibitor into a promoter of cell invasion

Cancer Research

Volumn 70, Issue 14, 2010, Pages 5984-5993

  Heikkinen, Pekka T ^a,b   Nummela, Marika ^a   Jokilehto, Terhi ^a,b   Grenman, Reidar ^b,c   Kähäri, Veli Matti ^b,c   Jaakkola, Panu M ^a,b  

^a TURKU CENTRE FOR BIOTECHNOLOGY   (Finland)

^b TURKU UNIVERSITY HOSPITAL   (Finland)

^c UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

SMAD7 PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; VON HIPPEL LINDAU PROTEIN;

ARTICLE; CANCER CELL CULTURE; CARCINOMA CELL; CELL HYPOXIA; CELL INVASION; CONTROLLED STUDY; GENE ACTIVATION; GENE EXPRESSION; HUMAN; HUMAN CELL; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION;

ADULT; AGED; AGED, 80 AND OVER; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CARCINOMA, SQUAMOUS CELL; CELL HYPOXIA; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAD AND NECK NEOPLASMS; HELA CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KERATINOCYTES; MALE; MIDDLE AGED; NEOPLASM INVASIVENESS; PHOSPHORYLATION; RNA, MESSENGER; SMAD PROTEINS, RECEPTOR-REGULATED; SMAD7 PROTEIN;

EID: 77955047829     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-09-3777     Document Type: Article

References (50)

1. ten Dijke P, Hill CS. New insights into TGF-β-Smad signalling. Trends Biochem Sci 2004;29:265-73.
2. Massague J, Seoane J, Wotton D. Smad transcription factors. Genes Dev 2005;19:2783-810.
3. Cui W, Fowlis DJ, Bryson S, et al. TGFβ1 inhibits the formation of benign skin tumors, but enhances progression to invasive spindle carcinomas in transgenic mice. Cell 1996;86:531-42.
4. Yang YA, Dukhanina O, Tang B, et al. Lifetime exposure to a soluble TGF-β antagonist protects mice against metastasis without adverse side effects. J Clin Invest 2002;109:1607-15.
5. Muraoka-Cook RS, Kurokawa H, Koh Y, et al. Conditional overexpression of active transforming growth factor β1 in vivo accelerates metastases of transgenic mammary tumors. Cancer Res 2004;64:9002-11.
6. Siegel PM, Massague J. Cytostatic and apoptotic actions of TGF-β in homeostasis and cancer. Nat Rev Cancer 2003;3:807-21.
7. Derynck R, Akhurst RJ, Balmain A. TGF-β signaling in tumor suppression and cancer progression. Nat Genet 2001;29:117-29.
8. Moustakas A, Souchelnytskyi S, Heldin CH. Smad regulation in TGF-β signal transduction. J Cell Sci 2001;114:4359-69.
9. Nakao A, Afrakhte M, Moren A, et al. Identification of Smad7, a TGFβ-inducible antagonist of TGF-β signalling. Nature 1997;389: 631-5.
10. Hayashi H, Abdollah S, Qiu Y, et al. The MAD-related protein Smad7 associates with the TGFβ receptor and functions as an antagonist of TGFβ signaling. Cell 1997;89:1165-73.
11. Kavsak P, Rasmussen RK, Causing CG, et al. Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGFβ receptor for degradation. Mol Cell 2000;6:1365-75.
12. Shi W, Sun C, He B, et al. GADD34-1c recruited by Smad7 dephosphorylates TGFβ type I receptor. J Cell Biol 2004;164:291-300.
13. Zhu HJ, Iaria J, Sizeland AM. Smad7 differentially regulates transforming growth factor β-mediated signaling pathways. J Biol Chem 1999;274:32258-64.
14. Valdimarsdottir G, Goumans MJ, Itoh F, Itoh S, Heldin CH, ten Dijke P. Smad7 and protein phosphatase 1α are critical determinants in the duration of TGF-β/ALK1 signaling in endothelial cells. BMC Cell Biol 2006;7:16.
15. Vargesson N, Laufer E. Smad7 misexpression during embryonic angiogenesis causes vascular dilation and malformations independently of vascular smooth muscle cell function. Dev Biol 2001; 240:499-516.
16. Chi JT, Wang Z, Nuyten DS, et al. Gene expression programs in response to hypoxia: cell type specificity and prognostic significance in human cancers. PLoS Med 2006;3:e47.
17. Leivonen SK, Ala-Aho R, Koli K, Grenman R, Peltonen J, Kahari VM. Activation of Smad signaling enhances collagenase-3 (MMP-13) expression and invasion of head and neck squamous carcinoma cells. Oncogene 2006;25:2588-600.
18. Javelaud D, Delmas V, Moller M, et al. Stable overexpression of Smad7 in human melanoma cells inhibits their tumorigenicity in vitro and in vivo. Oncogene 2005;24:7624-9.
19. Azuma H, Ehata S, Miyazaki H, et al. Effect of Smad7 expression on metastasis of mouse mammary carcinoma JygMC(A) cells. J Natl Cancer Inst 2005;97:1734-46.
20. Liu X, Lee J, Cooley M, Bhogte E, Hartley S, Glick A. Smad7 but not Smad6 cooperates with oncogenic ras to cause malignant conversion in a mouse model for squamous cell carcinoma. Cancer Res 2003;63:7760-8.
21. Halder SK, Beauchamp RD, Datta PK. Smad7 induces tumorigenicity by blocking TGF-β-induced growth inhibition and apoptosis. Exp Cell Res 2005;307:231-46.
22. Gumz ML, Zou H, Kreinest PA, et al. Secreted frizzled-related protein 1 loss contributes to tumor phenotype of clear cell renal cell carcinoma. Clin Cancer Res 2007;13:4740-9.
23. Higgins JP, Shinghal R, Gill H, et al. Gene expression patterns in renal cell carcinoma assessed by complementary DNA microarray. Am J Pathol 2003;162:925-32.
24. Ginos MA, Page GP, Michalowicz BS, et al. Identification of a gene expression signature associated with recurrent disease in squamous cell carcinoma of the head and neck. Cancer Res 2004;64:55-63.
25. Pyeon D, Newton MA, Lambert PF, et al. Fundamental differences in cell cycle deregulation in human papillomavirus-positive and human papillomavirus-negative head/neck and cervical cancers. Cancer Res 2007;67:4605-19.
26. Cromer A, Carles A, Millon R, et al. Identification of genes associated with tumorigenesis and metastatic potential of hypopharyngeal cancer by microarray analysis. Oncogene 2004;23:2484-98.
27. Toruner GA, Ulger C, Alkan M, et al. Association between gene expression profile and tumor invasion in oral squamous cell carcinoma. Cancer Genet Cytogenet 2004;154:27-35.
28. Boulay JL, Mild G, Lowy A, et al. SMAD7 is a prognostic marker in patients with colorectal cancer. Int J Cancer 2003;104:446-9.
29. Kleeff J, Ishiwata T, Maruyama H, et al. The TGF-β signaling inhibitor Smad7 enhances tumorigenicity in pancreatic cancer. Oncogene 1999;18:5363-72.
30. Jungert K, Buck A, Buchholz M, et al. Smad-Sp1 complexes mediate TGFβ-induced early transcription of oncogenic Smad7 in pancreatic cancer cells. Carcinogenesis 2006;27:2392-401.
31. Halder SK, Rachakonda G, Deane NG, Datta PK. Smad7 induces hepatic metastasis in colorectal cancer. Br J Cancer 2008;99: 957-65.
32. Kim YH, Lee HS, Lee HJ, et al. Prognostic significance of the expression of Smad4 and Smad7 in human gastric carcinomas. Ann Oncol 2004;15:574-80.
33. O'Donnell RK, Kupferman M, Wei SJ, et al. Gene expression signature predicts lymphatic metastasis in squamous cell carcinoma of the oral cavity. Oncogene 2005;24:1244-51.
34. Vaupel P, Mayer A. Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev 2007;26:225-39.
35. Kaelin WG, Jr., Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 2008;30:393-402.
36. Schofield CJ, Ratcliffe PJ. Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 2004;5:343-54.
37. Kaelin WG. Proline hydroxylation and gene expression. Annu Rev Biochem 2005;74:115-28.
38. Marxsen JH, Stengel P, Doege K, et al. Hypoxia-inducible factor-1 (HIF-1) promotes its degradation by induction of HIF-α-prolyl-4- hydroxylases. Biochem J 2004;381:761-7.
39. Oncomine. http://www.compendiabio.com.
40. Jokilehto T, Rantanen K, Luukkaa M, et al. Overexpression and nuclear translocation of hypoxia-inducible factor prolyl hydroxylase PHD2 in head and neck squamous cell carcinoma is associated with tumor aggressiveness. Clin Cancer Res 2006;12:1080-7.
41. Patel B, Khaliq A, Jarvis-Evans J, McLeod D, Mackness M, Boulton M. Oxygen regulation of TGF-β1 mRNA in human hepatoma (Hep G2) cells. Biochem Mol Biol Int 1994;34:639-44.
42. Schaffer L, Scheid A, Spielmann P, et al. Oxygen-regulated expression of TGF-β3, a growth factor involved in trophoblast differentiation. Placenta 2003;24:941-50.
43. Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC. Differential roles of hypoxia-inducible factor 1α (HIF-1α) and HIF-2α in hypoxic gene regulation. Mol Cell Biol 2003;23:9361-74.
44. Stopa M, Anhuf D, Terstegen L, Gatsios P, Gressner AM, Dooley S. Participation of Smad2, Smad3, and Smad4 in transforming growth factor β (TGF-β)-induced activation of Smad7. The TGF-β response element of the promoter requires functional Smad binding element and E-box sequences for transcriptional regulation. J Biol Chem 2000;275:29308-17.
45. Kim W, Kaelin WG. The von Hippel-Lindau tumor suppressor protein: new insights into oxygen sensing and cancer. Curr Opin Genet Dev 2003;13:55-60.
46. Heikkinen PT, Nummela M, Leivonen SK, et al. Hypoxia-activated Smad3-specific dephosphorylation by PP2A. J Biol Chem 2010; 285:3740-9.
47. Javelaud D, Mohammad KS, McKenna CR, et al. Stable overexpression of Smad7 in human melanoma cells impairs bone metastasis. Cancer Res 2007;67:2317-24.
48. Dowdy SC, Mariani A, Reinholz MM, et al. Overexpression of the TGF-β antagonist Smad7 in endometrial cancer. Gynecol Oncol 2005;96:368-73.
49. Kuang C, Xiao Y, Liu X, et al. In vivo disruption of TGF-β signaling by Smad7 leads to premalignant ductal lesions in the pancreas. Proc Natl Acad Sci U S A 2006;103:1858-63.
50. Sanchez-Elsner T, Botella LM, Velasco B, Corbi A, Attisano L, Bernabeu C. Synergistic cooperation between hypoxia and transforming growth factor-β pathways on human vascular endothelial growth factor gene expression. J Biol Chem 2001;276:38527-35.