SMAD2, SMAD3 and SMAD4 mutations in colorectal cancer

Cancer Research

Volumn 73, Issue 2, 2013, Pages 725-735

  Fleming, Nicholas I ^a   Jorissen, Robert N ^a   Mouradov, Dmitri ^a   Christie, Michael ^a,c   Sakthianandeswaren, Anuratha ^a   Palmieri, Michelle ^a   Day, Fiona ^a,c   Li, Shan ^a   Tsui, Cary ^a   Lipton, Lara ^a,c   Desai, Jayesh ^a   Jones, Ian T ^a   McLaughlin, Stephen ^e   Ward, Robyn L ^f   Hawkins, Nicholas J ^g   Ruszkiewicz, Andrew R ^h   Moore, James ⁱ   Zhu, Hong Jian ^d   Mariadason, John M ^b   Burgess, Antony W ^b   Busam, Dana ^j   Zhao, Qi ^k   Strausberg, Robert L ^k,l   Gibbs, Peter ^a,c   Sieber, Oliver M ^a,c   more..

^a ROYAL MELBOURNE HOSPITAL   (Australia)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e WESTERN HOSPITAL   (Australia)

^f UNIVERSITY OF NEW SOUTH WALES   (Australia)

^g UNIVERSITY OF NEW SOUTH WALES   (Australia)

^h INSTITUTE OF MEDICAL AND VETERINARY SCIENCE   (Australia)

ⁱ ROYAL ADELAIDE HOSPITAL   (Australia)

^j J CRAIG VENTER INSTITUTE   (United States)

^k JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^l LUDWIG INSTITUTE FOR CANCER RESEARCH   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ADULT; AGED; ALLELE; AMINO ACID SEQUENCE; ARTICLE; CANCER CELL CULTURE; CLINICAL FEATURE; COHORT ANALYSIS; COLORECTAL CANCER; COMPLEX FORMATION; COMPUTER ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; GENE MUTATION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MICROARRAY ANALYSIS; MISSENSE MUTATION; MUTATIONAL ANALYSIS; PATHOGENICITY; PREVALENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SMAD2 GENE; SMAD3 GENE; SMAD4 GENE; TUMOR SUPPRESSOR GENE;

ADULT; AGED; AGED, 80 AND OVER; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; FEMALE; HUMANS; LOSS OF HETEROZYGOSITY; MALE; MIDDLE AGED; MUTATION; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

EID: 84872510974     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-2706     Document Type: Article

References (50)

1. Massague J. TGFb in cancer. Cell 2008;134: 215-30.
2. Abdollah S, Macias-Silva M, Tsukazaki T, Hayashi H, Attisano L, Wrana JL. TbRI phosphorylation of Smad2 on Ser465 and Ser467 is required for Smad2-Smad4 complex formation and signaling. J Biol Chem 1997;272: 27678-85.
3. Souchelnytskyi S, Tamaki K, Engstrom U, Wernstedt C, ten Dijke P, Heldin CH. 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 1997;272: 28107-15.
4. Shi Y, Hata A, Lo RS, Massague J, Pavletich NP. A structural basis for mutational inactivation of the tumour suppressor Smad4. Nature 1997;388: 87-93.
5. Chacko BM, Qin B, Correia JJ, Lam SS, de Caestecker MP, Lin K. The L3 loop and C-terminal phosphorylation jointly define Smad protein trimerization. Nat Struct Biol 2001;8: 248-53.
6. Chacko BM, Qin BY, Tiwari A, Shi G, Lam S, Hayward LJ, et al. Structural basis of heteromeric smad protein assembly in TGF-b signaling. Mol Cell 2004;15: 813-23.
7. Brown KA, Pietenpol JA, Moses HL. A tale of two proteins: differential roles and regulation of Smad2 and Smad3 in TGF-b signaling. J Cell Biochem 2007;101: 9-33.
8. Houlston R, Bevan S, Williams A, Young J, Dunlop M, Rozen P, et al. Mutations in DPC4 (SMAD4) cause juvenile polyposis syndrome, but only account for a minority of cases. Hum Mol Genet 1998;7: 1907-12.
9. Markowitz S, Wang J, Myeroff L, Parsons R, Sun L, Lutterbaugh J, et al. Inactivation of the type II TGF-b receptor in colon cancer cells with microsatellite instability. Science 1995;268: 1336-8.
10. Koyama M, Ito M, Nagai H, Emi M, Moriyama Y. Inactivation of both alleles of the DPC4/SMAD4 gene in advanced colorectal cancers: identification of seven novel somatic mutations in tumors from Japanese patients. Mutat Res 1999;406: 71-7.
11. Miyaki M, Iijima T, Konishi M, Sakai K, Ishii A, Yasuno M, et al. Higher frequency of Smad4 gene mutation in human colorectal cancer with distant metastasis. Oncogene 1999;18: 3098-103.
12. Iacobuzio-Donahue CA, Song J, Parmiagiani G, Yeo CJ, Hruban RH, Kern SE. Missense mutations of MADH4: characterization of the mutational hot spot and functional consequences in human tumors. Clin Cancer Res 2004;10: 1597-604.
13. Iacopetta BJ, Welch J, Soong R, House AK, Zhou XP, Hamelin R. Mutation of the transforming growth factor-b type II receptor gene in right-sided colorectal cancer: relationship to clinicopathological features and genetic alterations. J Pathol 1998;184: 390-5.
14. Hata A, Lo RS, Wotton D, Lagna G, Massague J. Mutations increasing autoinhibition inactivate tumour suppressors Smad2 and Smad4. Nature 1997;388: 82-7.
15. Kuang C, Chen Y. Tumor-derived C-terminal mutations of Smad4 with decreased DNA binding activity and enhanced intramolecular interaction. Oncogene 2004;23: 1021-9.
16. Wu G, Chen YG, Ozdamar B, Gyuricza CA, Chong PA, Wrana JL, et al. Structural basis of Smad2 recognition by the Smad anchor for receptor activation. Science 2000;287: 92-7.
17. Moren A, Itoh S, Moustakas A, Dijke P, Heldin CH. Functional consequences of tumorigenic missense mutations in the amino-terminal domain of Smad4. Oncogene 2000;19: 4396-404.
18. TCGA. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012;487: 330-7.
19. SjoblomT, Jones S, Wood LD, Parsons DW, Lin J, Barber TD, et al. The consensus coding sequences of human breast and colorectal cancers. Science 2006;314: 268-74.
20. Eppert K, Scherer SW, Ozcelik H, Pirone R, Hoodless P, Kim H, et al. MADR2 maps to 18q21 and encodes a TGFb-regulated MAD-related protein that is functionally mutated in colorectal carcinoma. Cell 1996;86: 543-52.
21. Hamamoto T, Beppu H, Okada H, Kawabata M, Kitamura T, Miyazono K, et al. Compound disruption of smad2 accelerates malignant progression of intestinal tumors in apc knockout mice. Cancer Res 2002;62: 5955-61.
22. Zhu Y, Richardson JA, Parada LF, Graff JM. Smad3 mutant mice develop metastatic colorectal cancer. Cell 1998;94: 703-14.
23. Sodir NM, Chen X, Park R, Nickel AE, Conti PS, Moats R, et al. Smad3 deficiency promotes tumorigenesis in the distal colon of ApcMin/+ mice. Cancer Res 2006;66: 8430-8.
24. Yau C, Mouradov D, Jorissen RN, Colella S, Mirza G, Steers G, et al. A statistical approach for detecting genomic aberrations in heterogeneous tumor samples from single nucleotide polymorphism genotyping data. Genome Biol 2010;11:R92.
25. Zhu HJ, Sizeland AM. Extracellular domain of the transforming growth factor-b receptor negatively regulates ligand-independent receptor activation. J Biol Chem 1999;274: 29220-7.
26. Wieser R, Wrana JL, Massague J. GS domain mutations that constitutively activate TbR-I, the downstream signaling component in the TGF-b receptor complex. EMBO J 1995;14: 2199-208.
27. Dennler S, Itoh S, Vivien D, ten Dijke P, Huet S, Gauthier JM. Direct binding of Smad3 and Smad4 to critical TGFb-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J 1998;17: 3091-100.
28. Lorenz WW, McCann RO, Longiaru M, Cormier MJ. Isolation and expression of a cDNA encoding Renilla reniformis luciferase. Proc Natl Acad Sci U S A 1991;88: 4438-42.
29. Ng PC, Henikoff S. Predicting deleterious amino acid substitutions. Genome Res 2001;11: 863-74.
30. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, et al. A method and server for predicting damaging missense mutations. Nat Methods 2010;7: 248-9.
31. Stone EA, Sidow A. Physicochemical constraint violation by missense substitutions mediates impairment of protein function and disease severity. Genome Res 2005;15: 978-86.
32. Capriotti E, Fariselli P, Rossi I, Casadio R. A three-state prediction of single point mutations on protein stability changes. BMC Bioinformatics 2008;9 Suppl 2:S6.
33. Yeo G, Burge CB. Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J Comput Biol 2004;11: 377-94.
34. Ihaka R, Gentleman R. R: a language for data analysis and graphics. J Comput Graph Statist 1996;5: 299-314.
35. Xiao Z, Liu X, Henis YI, Lodish HF. A distinct nuclear localization signal in the N terminus of Smad 3 determines its ligand-induced nuclear translocation. Proc Natl Acad Sci U S A 2000;97: 7853-8.
36. Matsuura I, Denissova NG, Wang G, He D, Long J, Liu F. Cyclindependent kinases regulate the antiproliferative function of Smads. Nature 2004;430: 226-31.
37. Vivian JL, Chen Y, Yee D, Schneider E, Magnuson T. An allelic series of mutations in Smad2 and Smad4 identified in a genotype-based screen of N-ethyl-N- nitrosourea-mutagenized mouse embryonic stem cells. Proc Natl Acad Sci U S A 2002;99: 15542-7.
38. Mizuide M, Hara T, Furuya T, Takeda M, Kusanagi K, Inada Y, et al. Two short segments of Smad3 are important for specific interaction of Smad3 with c-Ski and SnoN. J Biol Chem 2003;278: 531-6.
39. Ku JL, Park SH, Yoon KA, Shin YK, Kim KH, Choi JS, et al. Genetic alterations of the TGF-b signaling pathway in colorectal cancer cell lines: a novel mutation in Smad3 associated with the inactivation of TGF-b-induced transcriptional activation. Cancer Lett 2007;247: 283-92.
40. Dennler S, Huet S, Gauthier JM. A short amino-acid sequence in MH1 domain is responsible for functional differences between Smad2 and Smad3. Oncogene 1999;18: 1643-8.
41. De Bosscher K, Hill CS, Nicolas FJ. Molecular and functional consequences of Smad4 C-terminal missense mutations in colorectal tumour cells. Biochem J 2004;379: 209-16.
42. Xu J, Attisano L. Mutations in the tumor suppressors Smad2 and Smad4 inactivate transforming growth factor beta signaling by targeting Smads to the ubiquitin-proteasome pathway. Proc Natl Acad Sci U S A 2000;97: 4820-5.
43. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008;321: 1801-6.
44. Yamagata H, Matsuzaki K, Mori S, Yoshida K, Tahashi Y, Furukawa F, et al. Acceleration of Smad2 and Smad3 phosphorylation via c-JunNH (2)-terminal kinase during human colorectal carcinogenesis. Cancer Res 2005;65: 157-65.
45. Matsuzaki K, Kitano C, Murata M, Sekimoto G, Yoshida K, Uemura Y, et al. Smad2 and Smad3 phosphorylated at both linker and COOH-terminal regions transmit malignant TGF-b signal in later stages of human colorectal cancer. Cancer Res 2009;69: 5321-30.
46. Mamot C, Mild G, Reuter J, Laffer U, Metzger U, Terracciano L, et al. Infrequent mutation of the tumour-suppressor gene Smad4 in earlystage colorectal cancer. Br J Cancer 2003;88: 420-3.
47. Farhat MH, Barada KA, Tawil AN, Itani DM, Hatoum HA, Shamseddine AI. Effect of mucin production on survival in colorectal cancer: a casecontrol study. World J Gastroenterol 2008;14: 6981-5.
48. Catalano V, Loupakis F, Graziano F, Torresi U, Bisonni R, Mari D, et al. Mucinous histology predicts for poor response rate and overall survival of patients with colorectal cancer and treated with first-line oxaliplatin- and/or irinotecan-based chemotherapy. Br J Cancer 2009;100: 881-7.
49. Ogino S, Brahmandam M, Cantor M, Namgyal C, Kawasaki T, Kirkner G, et al. Distinct molecular features of colorectal carcinoma with signet ring cell component and colorectal carcinoma with mucinous component. Mod Pathol 2006;19: 59-68.
50. Hoodless PA, Tsukazaki T, Nishimatsu S, Attisano L, Wrana JL, Thomsen GH. Dominant-negative Smad2 mutants inhibit activin/Vg1 signaling and disrupt axis formation in Xenopus. Dev Biol 1999;207: 364-79.