Unraveling the biological functions of Smad7 with mouse models

Cell and Bioscience

Volumn 1, Issue 1, 2011, Pages

  Zhu, Lu ^a   Chen, Susie ^a   Chen, Yan ^a  

^a Chinese Academy of Sciences   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA;

EID: 84862853379     PISSN: None     EISSN: 20453701     Source Type: Journal    
DOI: 10.1186/2045-3701-1-44     Document Type: Review

References (59)

1. Massague J. TGF-beta signal transduction. Annu Rev Biochem 1998, 67:753-791. 10.1146/annurev.biochem.67.1.753, 9759503.
2. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003, 113:685-700. 10.1016/S0092-8674(03)00432-X, 12809600.
3. Massague J. TGFbeta in Cancer. Cell 2008, 134:215-230. 10.1016/j.cell.2008.07.001, 18662538.
4. Imamura T, Takase M, Nishihara A, Oeda E, Hanai J, Kawabata M, Miyazono K. Smad6 inhibits signalling by the TGF-beta superfamily. Nature 1997, 389:622-626. 10.1038/39355, 9335505.
5. Nakao A, Afrakhte M, Moren A, Nakayama T, Christian JL, Heuchel R, Itoh S, Kawabata M, Heldin NE, Heldin CH, ten Dijke P. Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signalling. Nature 1997, 389:631-635. 10.1038/39369, 9335507.
6. Casellas R, Brivanlou AH. Xenopus Smad7 inhibits both the activin and BMP pathways and acts as a neural inducer. Dev Biol 1998, 198:1-12. 10.1016/S0012-1606(98)80025-0, 9640328.
7. Hayashi H, Abdollah S, Qiu Y, Cai J, Xu YY, Grinnell BW, Richardson MA, Topper JN, Gimbrone MA, Wrana JL, Falb D. The MAD-related protein Smad7 associates with the TGFbeta receptor and functions as an antagonist of TGFbeta signaling. Cell 1997, 89:1165-1173. 10.1016/S0092-8674(00)80303-7, 9215638.
8. Lebrun JJ, Takabe K, Chen Y, Vale W. Roles of pathway-specific and inhibitory Smads in activin receptor signaling. Mol Endo 1999, 13:15-23.
9. 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, 6:1365-1375. 10.1016/S1097-2765(00)00134-9, 11163210.
10. 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, 276:12477-12480. 10.1074/jbc.C100008200, 11278251.
11. Suzuki C, Murakami G, Fukuchi M, Shimanuki T, Shikauchi Y, Imamura T, Miyazono K. Smurf1 regulates the inhibitory activity of Smad7 by targeting Smad7 to the plasma membrane. J Biol Chem 2002, 277:39919-39925. 10.1074/jbc.M201901200, 12151385.
12. Shi W, Sun C, He B, Xiong W, Shi X, Yao D, Cao X. GADD34-PP1c recruited by Smad7 dephosphorylates TGFbeta type I receptor. J Cell Biol 2004, 164:291-300. 10.1083/jcb.200307151, 2172339, 14718519.
13. Yan X, Chen YG. Smad7: not only a regulator, but also a cross-talk mediator of TGF-beta signalling. Biochem J 2011, 434:1-10. 10.1042/BJ20101827, 21269274.
14. Zwijsen A, van Rooijen MA, Goumans MJ, Dewulf N, Bosman EA, ten Dijke P, Mummery CL, Huylebroeck D. Expression of the inhibitory Smad7 in early mouse development and upregulation during embryonic vasculogenesis. Dev Dyn 2000, 218:663-670. 10.1002/1097-0177(200008)218:4<663::AID-DVDY1020>3.0.CO;2-7, 10906784.
15. Zhao J, Shi W, Chen H, Warburton D. Smad7 and Smad6 differentially modulate transforming growth factor beta -induced inhibition of embryonic lung morphogenesis. J Biol Chem 2000, 275:23992-23997. 10.1074/jbc.M002433200, 10801843.
16. Han G, Li AG, Liang YY, Owens P, He W, Lu S, Yoshimatsu Y, Wang D, Ten Dijke P, Lin X, Wang XJ. Smad7-induced beta-catenin degradation alters epidermal appendage development. Dev Cell 2006, 11:301-312. 10.1016/j.devcel.2006.06.014, 16950122.
17. Iwai T, Murai J, Yoshikawa H, Tsumaki N. Smad7 Inhibits chondrocyte differentiation at multiple steps during endochondral bone formation and down-regulates p38 MAPK pathways. J Biol Chem 2008, 283:27154-27164. 10.1074/jbc.M801175200, 18644788.
18. Tang S, Snider P, Firulli AB, Conway SJ. Trigenic neural crest-restricted Smad7 over-expression results in congenital craniofacial and cardiovascular defects. Dev Biol 2010, 344:233-247. 10.1016/j.ydbio.2010.05.004, 2909335, 20457144.
19. Li R, Rosendahl A, Brodin G, Cheng AM, Ahgren A, Sundquist C, Kulkarni S, Pawson T, Heldin CH, Heuchel RL. Deletion of exon I of SMAD7 in mice results in altered B cell responses. J Immunol 2006, 176:6777-6784.
20. Chen Q, Chen H, Zheng D, Kuang C, Fang H, Zou B, Zhu W, Bu G, Jin T, Wang Z, et al. Smad7 is required for the development and function of the heart. J Biol Chem 2009, 284:292-300. 2610499, 18952608.
21. Mochizuki T, Miyazaki H, Hara T, Furuya T, Imamura T, Watabe T, Miyazono K. Roles for the MH2 domain of Smad7 in the specific inhibition of transforming growth factor-beta superfamily signaling. J Biol Chem 2004, 279:31568-31574. 10.1074/jbc.M313977200, 15148321.
22. Liu X, Chen Q, Kuang C, Zhang M, Ruan Y, Xu ZC, Wang Z, Chen Y. A 4.3 kb Smad7 promoter is able to specify gene expression during mouse development. Biochim Biophys Acta 2007, 1769:149-152. 1852475, 17306381.
23. Wynn TA. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest 2007, 117:524-529. 10.1172/JCI31487, 1804380, 17332879.
24. Dooley S, Hamzavi J, Breitkopf K, Wiercinska E, Said HM, Lorenzen J, Ten Dijke P, Gressner AM. Smad7 prevents activation of hepatic stellate cells and liver fibrosis in rats. Gastroenterology 2003, 125:178-191. 10.1016/S0016-5085(03)00666-8, 12851882.
25. Wang W, Koka V, Lan HY. Transforming growth factor-beta and Smad signalling in kidney diseases. Nephrology 2005, 10:48-56. 10.1111/j.1440-1797.2005.00334.x, 15705182.
26. Nakao A, Fujii M, Matsumura R, Kumano K, Saito Y, Miyazono K, Iwamoto I. Transient gene transfer and expression of Smad7 prevents bleomycin-induced lung fibrosis in mice. J Clin Invest 1999, 104:5-11. 10.1172/JCI6094, 408403, 10393693.
27. Fukasawa H, Yamamoto T, Togawa A, Ohashi N, Fujigaki Y, Oda T, Uchida C, Kitagawa K, Hattori T, Suzuki S, et al. Down-regulation of Smad7 expression by ubiquitin-dependent degradation contributes to renal fibrosis in obstructive nephropathy in mice. Proc Natl Acad Sci USA 2004, 101:8687-8692. 10.1073/pnas.0400035101, 423256, 15173588.
28. Chung AC, Huang XR, Zhou L, Heuchel R, Lai KN, Lan HY. Disruption of the Smad7 gene promotes renal fibrosis and inflammation in unilateral ureteral obstruction (UUO) in mice. Nephrol Dial Transplant 2009, 24:1443-1454. 10.1093/ndt/gfn699, 19096081.
29. He J, Sun X, Qian KQ, Liu X, Wang Z, Chen Y. Protection of cerulein-induced pancreatic fibrosis by pancreas-specific expression of Smad7. Biochim Biophys Acta 2009, 1792:56-60.
30. Saika S, Yamanaka O, Nishikawa-Ishida I, Kitano A, Flanders KC, Okada Y, Ohnishi Y, Nakajima Y, Ikeda K. Effect of Smad7 gene overexpression on transforming growth factor beta-induced retinal pigment fibrosis in a proliferative vitreoretinopathy mouse model. Arch Ophthalmol 2007, 125:647-654. 10.1001/archopht.125.5.647, 17502504.
31. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest 2005, 115:209-218. 546435, 15690074.
32. Dooley S, Hamzavi J, Ciuclan L, Godoy P, Ilkavets I, Ehnert S, Ueberham E, Gebhardt R, Kanzler S, Geier A, et al. Hepatocyte-specific Smad7 expression attenuates TGF-beta-mediated fibrogenesis and protects against liver damage. Gastroenterology 2008, 135:642-659. 10.1053/j.gastro.2008.04.038, 18602923.
33. Hamzavi J, Ehnert S, Godoy P, Ciuclan L, Weng H, Mertens PR, Heuchel R, Dooley S. Disruption of the Smad7 gene enhances CCI4-dependent liver damage and fibrogenesis in mice. J Cell Mol Med 2008, 12:2130-2144. 10.1111/j.1582-4934.2008.00262.x, 18266971.
34. Letterio JJ, Roberts AB. Regulation of immune responses by TGF-beta. Annu Rev Immunol 1998, 16:137-161. 10.1146/annurev.immunol.16.1.137, 9597127.
35. Li MO, Wan YY, Sanjabi S, Robertson AK, Flavell RA. Transforming growth factor-beta regulation of immune responses. Annu Rev Immunol 2006, 24:99-146. 10.1146/annurev.immunol.24.021605.090737, 16551245.
36. Hong S, Lim S, Li AG, Lee C, Lee YS, Lee EK, Park SH, Wang XJ, Kim SJ. Smad7 binds to the adaptors TAB2 and TAB3 to block recruitment of the kinase TAK1 to the adaptor TRAF2. Nat Immunol 2007, 8:504-513. 10.1038/ni1451, 17384642.
37. Ka SM, Huang XR, Lan HY, Tsai PY, Yang SM, Shui HA, Chen A. Smad7 gene therapy ameliorates an autoimmune crescentic glomerulonephritis in mice. J Am Soc Nephrol 2007, 18:1777-1788. 10.1681/ASN.2006080901, 17475816.
38. Chen HY, Huang XR, Wang W, Li JH, Heuchel RL, Chung AC, Lan HY. The protective role of Smad7 in diabetic kidney disease: mechanism and therapeutic potential. Diabetes 2011, 60:590-601. 10.2337/db10-0403, 20980457.
39. Zhu L, Wang L, Wang X, Luo X, Yang L, Zhang R, Yin H, Xie D, Pan Y, Chen Y. Hepatic deletion of Smad7 in mouse leads to spontaneous liver dysfunction and aggravates alcoholic liver injury. PLoS One 2011, 6:e17415. 10.1371/journal.pone.0017415, 3046253, 21386907.
40. Nakao A, Miike S, Hatano M, Okumura K, Tokuhisa T, Ra C, Iwamoto I. Blockade of transforming growth factor beta/Smad signaling in T cells by overexpression of Smad7 enhances antigen-induced airway inflammation and airway reactivity. J Exp Med 2000, 192:151-158. 10.1084/jem.192.2.151, 2193250, 10899902.
41. Fantini MC, Rizzo A, Fina D, Caruso R, Sarra M, Stolfi C, Becker C, Macdonald TT, Pallone F, Neurath MF, Monteleone G. Smad7 controls resistance of colitogenic T cells to regulatory T cell-mediated suppression. Gastroenterology 2009, 136:1308-1316, e1301-1303. 10.1053/j.gastro.2008.12.053, 19192480.
42. Boirivant M, Pallone F, Di Giacinto C, Fina D, Monteleone I, Marinaro M, Caruso R, Colantoni A, Palmieri G, Sanchez M, et al. Inhibition of Smad7 with a specific antisense oligonucleotide facilitates TGF-beta1-mediated suppression of colitis. Gastroenterology 2006, 131:1786-1798. 10.1053/j.gastro.2006.09.016, 17087939.
43. Monteleone G, Kumberova A, Croft NM, McKenzie C, Steer HW, MacDonald TT. Blocking Smad7 restores TGF-beta1 signaling in chronic inflammatory bowel disease. J Clin Invest 2001, 108:601-609. 209401, 11518734.
44. Kleiter I, Pedre X, Mueller AM, Poeschl P, Couillard-Despres S, Spruss T, Bogdahn U, Giegerich G, Steinbrecher A. Inhibition of Smad7, a negative regulator of TGF-beta signaling, suppresses autoimmune encephalomyelitis. J Neuroimmunol 2007, 187:61-73. 10.1016/j.jneuroim.2007.04.014, 17553571.
45. Kleiter I, Song J, Lukas D, Hasan M, Neumann B, Croxford AL, Pedre X, Hovelmeyer N, Yogev N, Mildner A, et al. Smad7 in T cells drives T helper 1 responses in multiple sclerosis and experimental autoimmune encephalomyelitis. Brain 2010, 133:1067-1081. 10.1093/brain/awq039, 2850583, 20354004.
46. Thompson CL, Plummer SJ, Acheson LS, Tucker TC, Casey G, Li L. Association of common genetic variants in SMAD7 and risk of colon cancer. Carcinogenesis 2009, 30:982-986. 10.1093/carcin/bgp086, 2691142, 19357349.
47. Slattery ML, Herrick J, Curtin K, Samowitz W, Wolff RK, Caan BJ, Duggan D, Potter JD, Peters U. Increased risk of colon cancer associated with a genetic polymorphism of SMAD7. Cancer Res 2010, 70:1479-1485. 10.1158/0008-5472.CAN-08-1792, 2925533, 20124488.
48. He W, Cao T, Smith DA, Myers TE, Wang XJ. Smads mediate signaling of the TGFbeta superfamily in normal keratinocytes but are lost during skin chemical carcinogenesis. Oncogene 2001, 20:471-483. 10.1038/sj.onc.1204117, 11313978.
49. 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, 63:7760-7768.
50. Kuang C, Xiao Y, Liu X, Stringfield TM, Zhang S, Wang Z, Chen Y. In vivo disruption of TGF-beta signaling by Smad7 leads to premalignant ductal lesions in the pancreas. Proc Natl Acad Sci USA 2006, 103:1858-1863. 10.1073/pnas.0508977103, 1413640, 16443684.
51. Halder SK, Rachakonda G, Deane NG, Datta PK. Smad7 induces hepatic metastasis in colorectal cancer. Br J Cancer 2008, 99:957-965. 10.1038/sj.bjc.6604562, 2538763, 18781153.
52. Luo X, Ding Q, Wang M, Li Z, Mao K, Sun B, Pan Y, Wang Z, Zang YQ, Chen Y. In vivo disruption of TGF-beta signaling by Smad7 in airway epithelium alleviates allergic asthma but aggravates lung carcinogenesis in mouse. PLoS One 2010, 5:e10149. 10.1371/journal.pone.0010149, 2854155, 20405019.
53. Azuma H, Ehata S, Miyazaki H, Watabe T, Maruyama O, Imamura T, Sakamoto T, Kiyama S, Kiyama Y, Ubai T, et al. Effect of Smad7 expression on metastasis of mouse mammary carcinoma JygMC(A) cells. J Natl Cancer I 2005, 97:1734-1746.
54. Javelaud D, Delmas V, Moller M, Sextius P, Andre J, Menashi S, Larue L, Mauviel A. Stable overexpression of Smad7 in human melanoma cells inhibits their tumorigenicity in vitro and in vivo. Oncogene 2005, 24:7624-7629. 10.1038/sj.onc.1208900, 16007121.
55. Rizzo A, Waldner MJ, Stolfi C, Sarra M, Fina D, Becker C, Neurath MF, Macdonald TT, Pallone F, Monteleone G, Fantini MC. Smad7 expression in T cells prevents colitis-associated cancer. Cancer Res 2011,
56. He W, Li AG, Wang D, Han S, Zheng B, Goumans MJ, Ten Dijke P, Wang XJ. Overexpression of Smad7 results in severe pathological alterations in multiple epithelial tissues. EMBO J 2002, 21:2580-2590. 10.1093/emboj/21.11.2580, 126032, 12032071.
57. Smart NG, Apelqvist AA, Gu X, Harmon EB, Topper JN, MacDonald RJ, Kim SK. Conditional expression of Smad7 in pancreatic beta cells disrupts TGF-beta signaling and induces reversible diabetes mellitus. PLoS Biol 2006, 4:e39. 10.1371/journal.pbio.0040039, 1351925, 16435884.
58. Saika S, Ikeda K, Yamanaka O, Sato M, Muragaki Y, Ohnishi Y, Ooshima A, Nakajima Y, Namikawa K, Kiyama H, et al. Transient adenoviral gene transfer of Smad7 prevents injury-induced epithelial-mesenchymal transition of lens epithelium in mice. Lab Invest 2004, 84:1259-1270. 10.1038/labinvest.3700151, 15258599.
59. Saika S, Ikeda K, Yamanaka O, Miyamoto T, Ohnishi Y, Sato M, Muragaki Y, Ooshima A, Nakajima Y, Kao WW, et al. Expression of Smad7 in mouse eyes accelerates healing of corneal tissue after exposure to alkali. Am J Pathol 2005, 166:1405-1418. 10.1016/S0002-9440(10)62358-9, 1606395, 15855641.