SMAD4 protein expression and cell proliferation in colorectal adenocarcinomas

Virchows Archiv

Volumn 459, Issue 5, 2011, Pages 511-519

  Handra Luca, Adriana ^a   Olschwang, Sylviane ^b,c   Fléjou, Jean François ^d,e  

^a UNIVERSITÉ PARIS 13   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c INSTITUT PAOLI CALMETTES   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e CENTRE DE RECHERCHE SAINT ANTOINE   (France)

Author keywords

Adenocarcinoma; Colon; Mismatch repair; p27; Pathology; Proliferation; SMAD4

Indexed keywords

KI 67 ANTIGEN; MISMATCH REPAIR PROTEIN; PROTEIN P27; S PHASE KINASE ASSOCIATED PROTEIN 2; SMAD4 PROTEIN;

ADULT; AGED; ARTICLE; CANCER CELL; CANCER LOCALIZATION; CANCER STAGING; CELL PROLIFERATION; COLORECTAL CARCINOMA; DISTANT METASTASIS; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TISSUE MICROARRAY; TUMOR DIFFERENTIATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; CELL PROLIFERATION; COLORECTAL NEOPLASMS; CYCLIN-DEPENDENT KINASE INHIBITOR P27; FEMALE; HUMANS; LYMPHATIC METASTASIS; MALE; MIDDLE AGED; NUCLEAR PROTEINS; S-PHASE KINASE-ASSOCIATED PROTEINS; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

EID: 80855156705     PISSN: 09456317     EISSN: 14322307     Source Type: Journal    
DOI: 10.1007/s00428-011-1152-4     Document Type: Article

References (75)

1. J Massague 1998 TGF-beta signal transduction Annu Rev Biochem 67 753 791 9759503 10.1146/annurev.biochem.67.1.753 1:CAS:528:DyaK1cXlsFOmsbY%3D (Pubitemid 28411144)
2. K Miyazono 2000 Positive and negative regulation of TGF-beta signalling J Cell Sci 113 1101 1109 10704361 1:CAS:528:DC%2BD3cXjtFymu7Y%3D (Pubitemid 30229527)
3. SA Hahn M Schutte AT Hoque, et al. 1996 DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1 Science 271 350 353 8553070 10.1126/science.271.5247.350 1:CAS:528:DyaK28XlsFartg%3D%3D
4. M Miyaki T Kuroki 2003 Role of Smad4 (DPC4) inactivation in human cancer Biochem Biophys Res Commun 306 799 804 12821112 10.1016/S0006-291X(03)01066-0 1:CAS:528:DC%2BD3sXkvVChtb8%3D (Pubitemid 36776201)
5. W Friedl R Kruse S Uhlhaas, et al. 1999 Frequent 4-bp deletion in exon 9 of the SMAD4/MADH4 gene in familial juvenile polyposis patients Genes Chromosomes Cancer 25 403 406 10398437 10.1002/(SICI)1098-2264(199908)25: 4<403::AID-GCC15>3.0.CO;2-P 1:CAS:528:DyaK1MXkvVOqtLs%3D (Pubitemid 29326150)
6. JR Howe S Roth JC Ringold, et al. 1998 Mutations in the SMAD4/DPC4 gene in juvenile polyposis Science 280 1086 1088 9582123 10.1126/science.280.5366. 1086 1:CAS:528:DyaK1cXjt1egsbs%3D (Pubitemid 28234951)
7. GC Blobe WP Schiemann HF Lodish 2000 Mechanisms of disease: role of transforming growth factor (beta) in human disease N Engl J Med 342 1350 1358 10793168 10.1056/NEJM200005043421807 1:CAS:528:DC%2BD3cXjtlyksrY%3D (Pubitemid 30408720)
8. RL Elliott GC Blobe 2005 Role of transforming growth factor beta in human cancer J Clin Oncol 23 2078 2093 15774796 10.1200/JCO.2005.02.047 1:CAS:528:DC%2BD2MXjt1Cku7c%3D (Pubitemid 46211385)
9. GJ Riggins KW Kinzler B Vogelstein, et al. 1997 Frequency of Smad gene mutations in human cancers Cancer Res 57 2578 2580 9205057 1:CAS:528: DyaK2sXkt12rtLw%3D (Pubitemid 27283760)
10. M Schutte RH Hruban L Hedrick, et al. 1996 DPC4 gene in various tumor types Cancer Res 56 2527 25230 8653691 1:CAS:528:DyaK28XjtlCgtb0%3D
11. S Thiagalingam C Lengauer FS Leach, et al. 1996 Evaluation of candidate tumour suppressor genes on chromosome 18 in colorectal cancers Nat Genet 13 343 346 8673134 10.1038/ng0796-343 1:CAS:528:DyaK28XktVegt7s%3D (Pubitemid 26230501)
12. M Loda B Cukor SW Tam, et al. 1997 Increased proteasome-dependent degradation of the cyclin-dependent kinase inhibitor p27 in aggressive colorectal carcinomas Nat Med 3 231 234 9018245 10.1038/nm0297-231 1:CAS:528:DyaK2sXpsFWgsQ%3D%3D (Pubitemid 27064711)
13. S Ogino T Kawasaki GJ Kirkner, et al. 2007 Loss of nuclear p27 (CDKN1B/KIP1) in colorectal cancer is correlated with microsatellite instability and CIMP Mod Pathol 20 15 22 17086168 10.1038/modpathol.3800709 1:CAS:528:DC%2BD28XhtlaktrnI (Pubitemid 44967945)
14. K Polyak JT Kato MJ Solomon, et al. 1994 p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest Genes Dev 8 9 22 8288131 10.1101/gad.8.1.9 1:CAS:528:DyaK2cXktVWku7c%3D
15. R Lloyd LA Erickson L Jin, et al. 1999 p27/kip1: a multifunctional cyclin-dependent kinase inhibitor with prognostic significance in human cancers Am J Pathol 154 313 323 10027389 10.1016/S0002-9440(10)65277-7 1:CAS:528:DyaK1MXjtVCqsb0%3D (Pubitemid 29094081)
16. D Hershko G Bornstein O Ben-Izhak, et al. 2001 Inverse relation between levels of p27(kip1) and of its ubiquitin ligase subunit SKP2 in colorectal carcinomas Cancer 91 1745 1751 11335900 10.1002/1097-0142(20010501)91:9<1745: :AID-CNCR1193>3.0.CO;2-H 1:CAS:528:DC%2BD3MXjslKns7o%3D (Pubitemid 32377961)
17. H Zhang R Kobayashi K Galakionov, et al. 1995 p19/Skp1 and p45/SKP2 are essential elements of the cyclin A-CDK2 S phase kinase Cell 82 915 925 7553852 10.1016/0092-8674(95)90271-6 1:CAS:528:DyaK2MXotlClt78%3D
18. Bosman F, Carneiro F, Hruban H, Theise N (eds) (2010) WHO classification of digestive tumours, 4th edn. IARC, Lyon
19. Edge SB, Byrd DR, Compton CC et al (eds) (2010) American Joint Committee on Cancer AJCC cancer staging manual, 7th edn. Springer, New York
20. F Jourdan N Sebbagh E Comperat, et al. 2003 Tissue microarray technology: validation in colorectal carcinoma and analysis of p53, hMLH1, and hMSH2 immunohistochemical expression Virchows Arch 443 115 121 12802583 10.1007/s00428-003-0833-z 1:CAS:528:DC%2BD3sXmsVSiu78%3D (Pubitemid 37056134)
21. J Kononen L Bubendorf A Kallioniemi, et al. 1998 Tissue microarrays for high-throughput molecular profiling of tumour specimens Nat Med 4 844 847 9662379 10.1038/nm0798-844 1:CAS:528:DyaK1cXktlKntr8%3D (Pubitemid 28331029)
22. A Handra-Luca B Ruhin C Lesty, et al. 2006 P27, SKP2, and extra-cellular signal-related kinase signalling in human salivary gland mucoepidermoid carcinoma Oral Oncol 42 1005 1010 16757206 10.1016/j.oraloncology.2005.12.022 1:CAS:528:DC%2BD28XhtFSktbrM (Pubitemid 44604459)
23. A Maitra K Molberg J Albores-Saavedra, et al. 2000 Loss of Dpc4 expression in colonic adenocarcinomas correlates with the presence of metastatic disease Am J Pathol 57 1105 1111 10.1016/S0002-9440(10)64625-1
24. A Maitra NV Adsay P Argani, et al. 2003 Multicomponent analysis of the pancreatic adenocarcinoma progression model using a pancreatic intraepithelial neoplasia tissue microarray Mod Pathol 16 902 912 13679454 10.1097/01.MP. 0000086072.56290.FB (Pubitemid 37152020)
25. A Hoos MJ Urist A Stojadinovic, et al. 2001 Validation of tissue microarrays for immunohistochemical profiling of cancer specimens using the example of human fibroblastic tumors Am J Pathol 158 1245 1251 11290542 10.1016/S0002-9440(10)64075-8 1:CAS:528:DC%2BD3MXjtVWhsLc%3D (Pubitemid 32281288)
26. V Rigau N Sebbagh S Olschwang, et al. 2003 Mirosatellite instability in colorectal carcinoma. The comparison of immunohistochemistry and molecular biology suggests a role for hMSH6 immunostaining Arch Pathol Lab Med 127 694 700 12741892 1:CAS:528:DC%2BD3sXkslKns74%3D (Pubitemid 36617287)
27. NM Lindor LJ Burgart O Leontovich, et al. 2002 Immunohistochemistry versus microsatellite instability testing in phenotyping colorectal tumours J Clin Oncol 20 1043 1048 11844828 10.1200/JCO.20.4.1043 1:CAS:528: DC%2BD38XitFOqur8%3D (Pubitemid 34141849)
28. E Montgomery M Goggins S Zhou, et al. 2001 Nuclear localization of Dpc4 (Madh4, SMAD4) in colorectal carcinomas and relation to mismatch repair/transforming growth factor-beta receptor defects Am J Pathol 158 537 542 11159190 10.1016/S0002-9440(10)63995-8 1:CAS:528:DC%2BD3MXhsFWmt7s%3D (Pubitemid 32158614)
29. SG Royce K Alsop A Haydon, et al. 2010 The role of SMAD4 in early onset colorectal cancer Colorectal Dis 12 213 219 19183329 10.1111/j.1463-1318.2009. 01779.x 1:STN:280:DC%2BC3czhsFWjsA%3D%3D
30. R Salovaara S Roth A Loukola, et al. 2002 Frequent loss of SMAD4/DPC4 protein in colorectal cancers Gut 51 56 59 12077092 10.1136/gut.51.1.56 1:CAS:528:DC%2BD38XlslOisrY%3D (Pubitemid 34717744)
31. W Xie DL Rimm Y Lin, et al. 2003 Loss of SMAD signalling in human colorectal cancer is associated with advanced disease and poor prognosis Cancer J 9 302 312 12967141 10.1097/00130404-200307000-00013 1:CAS:528: DC%2BD3sXnvVKksr4%3D
32. WQ Xu XC Jiang YY Yu, et al. 2007 Expression of TGF-beta1, TbetaRII and Smad4 in colorectal carcinoma Exp Mol Pathol 82 284 291 17289018 10.1016/j.yexmp.2006.10.011 1:CAS:528:DC%2BD2sXlt1Citbc%3D (Pubitemid 46686657)
33. RE Wilentz GH Su JL Dai, et al. 2000 Immunohistochemical labeling for Dpc4 mirrors genetic status in pancreatic adenocarcinomas. A new marker of DPC4 inactivation Am J Pathol 156 37 43 10623651 10.1016/S0002-9440(10)64703-7 1:CAS:528:DC%2BD3cXns1ymtA%3D%3D (Pubitemid 30644436)
34. H Alazzouzi P Alhopuro R Salovaara, et al. 2005 SMAD4 as a prognostic marker in colorectal cancer Clin Cancer Res 11 2606 2611 15814640 10.1158/1078-0432.CCR-04-1458 1:CAS:528:DC%2BD2MXivFKis78%3D (Pubitemid 40569460)
35. P Alhopuro H Alazzouzi H Sammalkorpi, et al. 2005 SMAD4 levels and response to 5-fluorouracil in colorectal cancer Clin Cancer Res 11 6311 6316 16144935 10.1158/1078-0432.CCR-05-0244 1:CAS:528:DC%2BD2MXpslansLc%3D (Pubitemid 41262962)
36. T Tanaka T Watanabe Y Kazama, et al. 2006 Chromosome 18q deletion and Smad4 protein inactivation correlate with liver metastasis: a study matched for T- and N-classification Br J Cancer 95 1562 1567 17088901 10.1038/sj.bjc.6603460 1:CAS:528:DC%2BD28Xht1Cntr3I (Pubitemid 44863360)
37. M Miyaki T Iijima M Konishi, et al. 1999 Higher frequency of Smad4 gene mutation in human colorectal cancer with distant metastasis Oncogene 20 3098 3103 10.1038/sj.onc.1202642 (Pubitemid 29261230)
38. M Koyama M Ito H Nagai, et al. 1999 Inactivation of both alleles of the DPC4/SMAD4 gene in advanced colorectal cancers: identification of seven novel somatic mutations in tumours from Japanese patients Mutat Res 406 71 77 10479724 10.1016/S1383-5726(99)00003-5 1:CAS:528:DyaK1MXmtFOhtb8%3D (Pubitemid 29429669)
39. T Tanaka T Watanabe Y Kazama J Tanaka, et al. 2008 Loss of Smad4 protein expression and 18qLOH as molecular markers indicating lymph node metastasis in colorectal cancer-a study matched for tumor depth and pathology J Surg Oncol 97 69 73 17786972 10.1002/jso.20896 1:CAS:528:DC%2BD1cXhvVClsb0%3D
40. L Losi H Bouzourene J Benhattar 2007 Loss of Smad4 expression predicts liver metastasis in human colorectal cancer Oncol Rep 17 1095 1099 17390050 1:CAS:528:DC%2BD2sXlsVymsr0%3D
41. DS Xiao JF Wen JH Li, et al. 2006 Effect of DPC4 gene on invasion and metastasis of colorectal carcinoma cells Acta Biochim Biophys Sin (Shanghai) 38 883 892 10.1111/j.1745-7270.2006.00233.x 1:CAS:528:DC%2BD2sXht1ansr0%3D (Pubitemid 44952891)
42. B Zhang SK Halder ND Kashikar, et al. 2010 Antimetastatic role of Smad4 signaling in colorectal cancer Gastroenterology 138 969 980 19909744 10.1053/j.gastro.2009.11.004 1:CAS:528:DC%2BC3cXksVCrt78%3D
43. JL Dai RK Bansal SE Kern 1999 G1 cell cycle arrest and apoptosis induction by nuclear Smad4/Dpc4: phenotypes reversed by a tumorigenic mutation Proc Natl Acad Sci U S A 96 1427 1432 9990040 10.1073/pnas.96.4.1427 1:STN:280:DyaK1M7ksFGltA%3D%3D (Pubitemid 29098467)
44. SK Halder RD Beauchamp PK Datta 2005 Smad7 induces tumorigenicity by blocking TGF-beta-induced growth inhibition and apoptosis Exp Cell Res 307 231 246 15922743 10.1016/j.yexcr.2005.03.009 1:CAS:528:DC%2BD2MXks1Ghu7o%3D (Pubitemid 40732749)
45. I Schwarte-Waldhoff S Klein S Blass-Kampmann, et al. 1999 DPC4/SMAD4 mediated tumor suppression of colon carcinoma cells is associated with reduced urokinase expression Oncogene 18 3152 3158 10340387 10.1038/sj.onc.1202641 1:CAS:528:DyaK1MXjs1OnurY%3D (Pubitemid 29261236)
46. MW Volmer Y Radacz SA Hahn, et al. 2004 Tumour suppressor Smad4 mediates downregulation of the anti-adhesive invasion-promoting matricellular protein SPARC: landscaping activity of Smad4 as revealed by a "secretome" analysis Proteomics 4 1324 1334 15188399 10.1002/pmic.200300703 1:CAS:528:DC%2BD2cXktFCiu7s%3D (Pubitemid 38648020)
47. A Reinacher-Schick S Baldus B Romdhana, et al. 2004 Loss of Smad4 correlates with loss of the invasion suppressor E-cadherin in advanced colorectal carcinomas J Pathol 202 412 420 15095268 10.1002/path.1516 1:CAS:528:DC%2BD2cXjsFegu74%3D (Pubitemid 38456159)
48. I Schwarte-Waldhoff W Schmiegel 2002 Smad4 transcriptional pathways and angiogenesis Int J Gastrointest Cancer 31 47 59 12622415 10.1385/IJGC:31:1-3:47 1:CAS:528:DC%2BD3sXhslKrsr4%3D (Pubitemid 36335756)
49. DeVita VR, Hellman S, Rosenberg SA (eds) (2005) Cancer principles and practice of oncology, 7th edn. Lippincott Williams and Wilkins, Philadelphia
50. AV Biankin SA Biankin JG Kench, et al. 2002 Aberrant p16(INK4A) and DPC4/Smad4 expression in intraductal papillary mucinous tumours of the pancreas is associated with invasive ductal adenocarcinoma Gut 50 861 868 12010891 10.1136/gut.50.6.861 1:CAS:528:DC%2BD38XkvVGktLw%3D (Pubitemid 34539051)
51. KA Hill KL Wang SJ Stryker R Gupta DM Weinrach MS Rao 2004 Comparative analysis of cell adhesion molecules, cell cycle regulatory proteins, mismatch repair genes, cyclooxygenase-2, and DPC4 in carcinomas arising in inflammatory bowel disease and sporadic colon cancer Oncol Rep 11 951 956 15069531 1:CAS:528:DC%2BD2cXjslGksr8%3D
52. YK Kang WH Kim JJ Jang 2002 Expression of G1-S modulators (p53, p16, p27, cyclin D1, Rb) and Smad4/Dpc4 in intrahepatic cholangiocarcinoma Hum Pathol 33 877 883 12378511 10.1053/hupa.2002.127444 1:CAS:528:DC%2BD38XotlGgsLw%3D
53. L Zeng RG Rowland SM Lele, et al. 2004 Apoptosis incidence and protein expression of p53, TGF-beta receptor II, p27Kip1, and Smad4 in benign, premalignant, and malignant human prostate Hum Pathol 35 290 297 15017584 10.1016/j.humpath.2003.11.001 1:CAS:528:DC%2BD2cXitFKnur8%3D (Pubitemid 38339602)
54. J Lecanda V Ganapathy C D'Aquino-Ardalan, et al. 2009 TGFbeta prevents proteasomal degradation of the cyclin-dependent kinase inhibitor p27kip1 for cell cycle arrest Cell Cycle 8 742 756 19221482 10.4161/cc.8.5.7871 1:CAS:528:DC%2BD1MXlvFWju7g%3D
55. M Ciaparrone H Yamamoto Y Yao, et al. 1998 Localization and expression of p27KIP1 in multistage colorectal carcinogenesis Cancer Res 58 114 122 9426067 1:CAS:528:DyaK1cXitVGltg%3D%3D (Pubitemid 28027726)
56. R Palmqvist R Stenling A Oberg, et al. 1999 Prognostic significance of p27(Kip1) expression in colorectal cancer: a clinico-pathological characterization J Pathol 188 18 23 10398135 10.1002/(SICI)1096-9896(199905)188: 1<18::AID-PATH311>3.0.CO;2-T 1:STN:280:DyaK1MzlvFGltA%3D%3D (Pubitemid 29197309)
57. GV Thomas K Szigeti M Murphy, et al. 1998 Down-regulation of p27 is associated with development of colorectal adenocarcinoma metastases Am J Pathol 153 681 687 9736017 10.1016/S0002-9440(10)65610-6 1:CAS:528:DyaK1cXmtFKntbg%3D (Pubitemid 28419021)
58. Y Katayose M Kim AN Rakkar, et al. 1997 Promoting apoptosis: a novel activity associated with the cyclin-dependent kinase inhibitor p27 Cancer Res 57 5441 5445 9407946 1:CAS:528:DyaK2sXotVGnsLc%3D (Pubitemid 28006743)
59. DF Liu K Ferguson GS Cooper, et al. 1999 p27 cell-cycle inhibitor is inversely correlated with lymph node metastases in right-sided colon cancer J Clin Lab Anal 13 291 295 10633297 10.1002/(SICI)1098-2825(1999)13:6<291::AID- JCLA7>3.0.CO;2-K
60. J Yao KW Eu F Seow-Choen, et al. 2000 Down-regulation of p27 is a significant predictor of poor overall survival and may facilitate metastasis in colorectal carcinomas Int J Cancer 89 213 216 10861495 10.1002/1097- 0215(20000520)89:3<213::AID-IJC1>3.0.CO;2-L 1:STN:280: DC%2BD3czitFCjtA%3D%3D (Pubitemid 30430735)
61. M Shapira O Ben-Izhak B Bishara, et al. 2004 Alterations in the expression of the cell cycle regulatory protein cyclin kinase subunit 1 in colorectal carcinoma Cancer 100 1615 1621 15073847 10.1002/cncr.20172 1:CAS:528:DC%2BD2cXjvFygtL4%3D (Pubitemid 38456336)
62. M Shapira O Ben-Izhak S Linn, et al. 2005 The prognostic impact of the ubiquitin ligase subunits SKP2 and Cks1 in colorectal carcinoma Cancer 103 1336 1346 15717322 10.1002/cncr.20917 1:CAS:528:DC%2BD2MXjtFamsbs%3D (Pubitemid 40410727)
63. K Nakayama H Nagahama YA Minamishima, et al. 2000 Targeted disruption of SKP2 results in accumulation of cyclin E and p27 (Kip), polyploidy and centrosome duplication EMBO J 19 2069 2081 10790373 10.1093/emboj/19.9.2069 1:CAS:528:DC%2BD3cXktFWiu7o%3D (Pubitemid 30237582)
64. JQ Li F Wu T Masaki, et al. 2004 Correlation of Skp2 with carcinogenesis, invasion, metastasis, and prognosis in colorectal tumors Int J Oncol 25 87 95 15201993
65. KL Woodford-Richens AJ Rowan P Gorman, et al. 2001 SMAD4 mutations in colorectal cancer probably occur before chromosomal instability, but after divergence of the microsatellite instability pathway Proc Natl Acad Sci U S A 98 9719 9723 11481457 10.1073/pnas.171321498 1:CAS:528:DC%2BD3MXmtlCmsro%3D (Pubitemid 32769370)
66. WM Grady LL Myeroff SE Swinler, et al. 1999 Mutational inactivation of transforming growth factor beta receptor type II in microsatellite stable colon cancers Cancer Res 59 320 324 9927040 1:CAS:528:DyaK1MXntFKrug%3D%3D (Pubitemid 29048861)
67. BJ Iacopetta J Welch R Soong, et al. 1998 Mutation of the transforming growth factor-beta type II receptor gene in right-sided colorectal cancer: relationship to clinicopathological features and genetic alterations J Pathol 184 390 395 9664904 10.1002/(SICI)1096-9896(199804)184:4<390::AID- PATH1230>3.0.CO;2-Q 1:CAS:528:DyaK1cXislagu74%3D (Pubitemid 28179897)
68. R Parsons LL Myeroff B Liu, et al. 1995 Microsatellite instability and mutations of the transforming growth factor beta type II receptor gene in colorectal cancer Cancer Res 55 5548 5550 7585632 1:CAS:528:DyaK2MXps1KrtLs%3D
69. GY Locker S Hamilton J Harris, et al. 2006 ASCO 2006 update of recommendations for the use of tumor markers in gastrointestinal cancer J Clin Oncol 24 5313 5327 17060676 10.1200/JCO.2006.08.2644 1:CAS:528: DC%2BD28XhtlemurfN (Pubitemid 46631379)
70. LM McShane DG Altman W Sauerbrei Statistics Subcommittee of the NCI-EORTC Working Group on Cancer Diagnostics, et al. 2005 Reporting recommendations for neoplastic marker prognostic studies J Clin Oncol 23 9067 9072 16172462 10.1200/JCO.2004.01.0454
71. A Moren U Hellman Y Inada, et al. 2003 Differential ubiquitination defines the functional status of the tumor suppressor Smad4 J Biol Chem 278 33571 33582 12794086 10.1074/jbc.M300159200 1:CAS:528:DC%2BD3sXms1altLc%3D (Pubitemid 37055811)
72. G Nalepa M Rolfe JW Harper 2006 Drug discovery in the ubiquitin-proteasome system Nat Rev Drug Discov 5 596 613 16816840 10.1038/nrd2056 1:CAS:528:DC%2BD28XmsVagsro%3D (Pubitemid 43971194)
73. A Mani EP Gelmann 2005 The ubiquitin-proteasome pathway and its role in cancer J Clin Oncol 23 4776 4789 16034054 10.1200/JCO.2005.05.081 1:CAS:528:DC%2BD2MXotFars7o%3D (Pubitemid 46224082)
74. M Boccadoro G Morgan J Cavenagh 2005 Preclinical evaluation of the proteasome inhibitor bortezomib in cancer therapy Cancer Cell Int 5 18 15929791 10.1186/1475-2867-5-18 (Pubitemid 41460748)
75. JC Cusack 2003 Rationale for the treatment of solid tumors with the proteasome inhibitor bortezomib Cancer Treat Rev 29 21 31 12738240 10.1016/S0305-7372(03)00079-3 1:CAS:528:DC%2BD3sXjsVejsbc%3D