Bone morphogenetic protein-2 and -4 play tumor suppressive roles in human diffuse-type gastric carcinoma

American Journal of Pathology

Volumn 179, Issue 6, 2011, Pages 2920-2930

  Shirai, Yo Taro ^a   Ehata, Shogo ^a   Yashiro, Masakazu ^b   Yanagihara, Kazuyoshi ^c   Hirakawa, Kosei ^b   Miyazono, Kohei ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c YASUDA WOMEN'S UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTOR 1A; PROTEIN P21; SMAD PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; CELL CYCLE ARREST; CELL PROLIFERATION; CONTROLLED STUDY; DIFFUSE TYPE GASTRIC CARCINOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; STOMACH CARCINOMA;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTORS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DISEASE PROGRESSION; MICE; MICE, INBRED BALB C; MICE, NUDE; PHOSPHORYLATION; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SMAD PROTEINS; STOMACH NEOPLASMS; TRANSFORMING GROWTH FACTOR BETA;

EID: 81255124262     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.08.022     Document Type: Article

References (50)

1. M. Yaghoobi, R. Bijarchi, and S.A. Narod Family history and the risk of gastric cancer Br J Cancer 102 2010 237 242
2. P. Lauren The two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma An attempt at a histo-clinical classification Acta Pathol Microbiol Scand 64 1965 31 49
3. K. Fukase, M. Kato, S. Kikuchi, K. Inoue, N. Uemura, S. Okamoto, S. Terao, K. Amagai, S. Hayashi, M. Asaka Japan Gast Study Group Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial Lancet 372 2008 392 397
4. D.E. Henson, C. Dittus, M. Younes, H. Nguyen, and J. Albores-Saavedra Differential trends in the intestinal and diffuse types of gastric carcinoma in the United States, 19732000: increase in the signet ring cell type Arch Pathol Lab Med 128 2004 765 770 (Pubitemid 38856886)
5. H. Ikushima, and K. Miyazono TGFbeta signalling: a complex web in cancer progression Nat Rev Cancer 10 2010 415 424
6. B. Bierie, and H.L. Moses Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer Nat Rev Cancer 6 2006 506 520 (Pubitemid 43980540)
7. Y. Suzuki, K. Montagne, A. Nishihara, T. Watabe, and K. Miyazono BMPs promote proliferation and migration of endothelial cells via stimulation of VEGF-A/VEGFR2 and angiopoietin-1/Tie2 signalling J Biochem 143 2008 199 206 (Pubitemid 351238167)
8. K. Miyazono, Y. Kamiya, and M. Morikawa Bone morphogenetic protein receptors and signal transduction J Biochem 147 2010 35 51
9. Y. Katsuno, A. Hanyu, H. Kanda, Y. Ishikawa, F. Akiyama, T. Iwase, E. Ogata, S. Ehata, K. Miyazono, and T. Imamura Bone morphogenetic protein signaling enhances invasion and bone metastasis of breast cancer cells through Smad pathway Oncogene 27 2008 6322 6333
10. E.M. Langenfeld, Y. Kong, and J. Langenfeld Bone morphogenetic protein 2 stimulation of tumor growth involves the activation of Smad-1/5 Oncogene 25 2006 685 692 (Pubitemid 43214695)
11. P.B. Yu, C.C. Hong, C. Sachidanandan, J.L. Babitt, D.Y. Deng, S.A. Hoyng, H.Y. Lin, K.D. Bloch, and R.T. Peterson Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism Nat Chem Biol 4 2008 33 41 (Pubitemid 350273653)
12. S.G. Piccirillo, B.A. Reynolds, N. Zanetti, G. Lamorte, E. Binda, G. Broggi, H. Brem, A. Olivi, F. Dimeco, and A.L. Vescovi Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells Nature 444 2006 761 765 (Pubitemid 44949605)
13. H. Miyazaki, T. Watabe, T. Kitamura, and K. Miyazono BMP signals inhibit proliferation and in vivo tumor growth of androgen-insensitive prostate carcinoma cells Oncogene 23 2004 9326 9335 (Pubitemid 40069665)
14. J.C. Hardwick, L.L. Kodach, G.J. Offerhaus, and G.R. van den Brink Bone morphogenetic protein signalling in colorectal cancer Nat Rev Cancer 8 2008 806 812
15. S.A. Bleuming, X.C. He, L.L. Kodach, J.C. Hardwick, F.A. Koopman, F.J. Ten Kate, S.J. van Deventer, D.W. Hommes, M.P. Peppelenbosch, G.J. Offerhaus, L. Li, and G.R. van den Brink Bone morphogenetic protein signaling suppresses tumorigenesis at gastric epithelial transition zones in mice Cancer Res 67 2007 8149 8155 (Pubitemid 47395150)
16. H. Oshima, H. Itadani, H. Kotani, M.M. Taketo, and M. Oshima Induction of prostaglandin E2 pathway promotes gastric hamartoma development with suppression of bone morphogenetic protein signaling Cancer Res 69 2009 2729 2733
17. A. Moustakas, and C.H. Heldin Non-Smad TGF-beta signals J Cell Sci 118 2005 3573 3584
18. J.Y. Kim, D.Y. Park, G.H. Kim, K.U. Choi, C.H. Lee, G.Y. Huh, M.Y. Sol, G.A. Song, T.Y. Jeon, D.H. Kim, and M.S. Sim Smad4 expression in gastric adenoma and adenocarcinoma: frequent loss of expression in diffuse type of gastric adenocarcinoma Histol Histopathol 20 2005 543 549 (Pubitemid 40468275)
19. A. Komuro, M. Yashiro, C. Iwata, Y. Morishita, E. Johansson, Y. Matsumoto, A. Watanabe, H. Aburatani, H. Miyoshi, K. Kiyono, Y.T. Shirai, H.I. Suzuki, K. Hirakawa, M.R. Kano, and K. Miyazono Diffuse-type gastric carcinoma: progression, angiogenesis, and transforming growth factor beta signaling J Natl Cancer Inst 101 2009 592 604
20. E. Johansson, A. Komuro, C. Iwata, A. Hagiwara, Y. Fuse, A. Watanabe, Y. Morishita, H. Aburatani, K. Funa, M.R. Kano, and K. Miyazono Exogenous introduction of tissue inhibitor of metalloproteinase 2 reduces accelerated growth of TGF-beta-disrupted diffuse-type gastric carcinoma Cancer Sci 101 2010 2398 2403
21. S. Ehata, E. Johansson, R. Katayama, S. Koike, A. Watanabe, Y. Hoshino, Y. Katsuno, A. Komuro, D. Koinuma, M.R. Kano, M. Yashiro, K. Hirakawa, H. Aburatani, N. Fujita, and K. Miyazono Transforming growth factor-beta decreases the cancer-initiating cell population within diffuse-type gastric carcinoma cells Oncogene 30 2011 1693 1705
22. T. Fujihara, T. Sawada, K. Hirakawa, Y.S. Chung, M. Yashiro, T. Inoue, and M. Sowa Establishment of lymph node metastatic model for human gastric cancer in nude mice and analysis of factors associated with metastasis Clin Exp Metastasis 16 1998 389 398 (Pubitemid 28255534)
23. Y. Kato, M. Yashiro, S. Noda, M. Tendo, S. Kashiwagi, Y. Doi, T. Nishii, J. Matsuoka, Y. Fuyuhiro, O. Shinto, T. Sawada, M. Ohira, and K. Hirakawa Establishment and characterization of a new hypoxia-resistant cancer cell line, OCUM-12/Hypo, derived from a scirrhous gastric carcinoma Br J Cancer 102 2010 898 907
24. Y. Nagano, D. Koinuma, K. Miyazawa, and K. Miyazono Context-dependent regulation of the expression of c-Ski protein by Arkadia in human cancer cells J Biochem 147 2010 545 554
25. K. Yanagihara, T. Seyama, M. Tsumuraya, N. Kamada, and K. Yokoro Establishment and characterization of human signet ring cell gastric carcinoma cell lines with amplification of the c-myc oncogene Cancer Res 51 1991 381 386
26. S. Ehata, A. Hanyu, M. Fujime, Y. Katsuno, E. Fukunaga, K. Goto, Y. Ishikawa, K. Nomura, H. Yokoo, T. Shimizu, E. Ogata, K. Miyazono, K. Shimizu, and T. Imamura Ki26894, a novel transforming growth factor-beta type I receptor kinase inhibitor, inhibits in vitro invasion and in vivo bone metastasis of a human breast cancer cell line Cancer Sci 98 2007 127 133 (Pubitemid 44803931)
27. Y. Hoshino, Y. Katsuno, S. Ehata, and K. Miyazono Autocrine TGF-beta protects breast cancer cells from apoptosis through reduction of BH3-only protein, Bim J Biochem 149 2011 55 65
28. I.M. Liu, S.H. Schilling, K.A. Knouse, L. Choy, R. Derynck, and X.F. Wang TGFbeta-stimulated Smad1/5 phosphorylation requires the ALK5 L45 loop and mediates the pro-migratory TGFbeta switch EMBO J 28 2009 88 98
29. C. Kawamura, M. Kizaki, K. Yamato, H. Uchida, Y. Fukuchi, Y. Hattori, T. Koseki, T. Nishihara, and Y. Ikeda Bone morphogenetic protein-2 induces apoptosis in human myeloma cells with modulation of STAT3 Blood 96 2000 2005 2011
30. N. Fukuda, M. Saitoh, N. Kobayashi, and K. Miyazono Execution of BMP-4-induced apoptosis by p53-dependent ER dysfunction in myeloma and B-cell hybridoma cells Oncogene 25 2006 3509 3517 (Pubitemid 43901672)
31. X.Z. Wen, S. Miyake, Y. Akiyama, and Y. Yuasa BMP-2 modulates the proliferation and differentiation of normal and cancerous gastric cells Biochem Biophys Res Commun 316 2004 100 106 (Pubitemid 38299134)
32. T. Mizoi, H. Ohtani, K. Miyazono, M. Miyazawa, S. Matsuno, and H. Nagura Immunoelectron microscopic localization of transforming growth factor beta 1 and latent transforming growth factor beta 1 binding protein in human gastrointestinal carcinomas: qualitative difference between cancer cells and stromal cells Cancer Res 53 1993 183 190 (Pubitemid 23019396)
33. J.R. Howe, S. Roth, J.C. Ringold, R.W. Summers, H.J. Jarvinen, P. Sistonen, I.P. Tomlinson, R.S. Houlston, S. Bevan, F.A. Mitros, E.M. Stone, and L.A. Aaltonen Mutations in the SMAD4/DPC4 gene in juvenile polyposis Science 280 1998 1086 1088 (Pubitemid 28234951)
34. J.R. Howe, J.L. Bair, M.G. Sayed, M.E. Anderson, F.A. Mitros, G.M. Petersen, V.E. Velculescu, G. Traverso, and B. Vogelstein Germline mutations of the gene encoding bone morphogenetic protein receptor 1A in juvenile polyposis Nat Genet 28 2001 184 187 (Pubitemid 32538067)
35. L.L. Kodach, E. Wiercinska, N.F. de Miranda, S.A. Bleuming, A.R. Musler, M.P. Peppelenbosch, E. Dekker, G.R. van den Brink, C.J. van Noesel, H. Morreau, D.W. Hommes, P. Ten Dijke, G.J. Offerhaus, and J.C. Hardwick The bone morphogenetic protein pathway is inactivated in the majority of sporadic colorectal cancers Gastroenterology 134 2008 1332 1341
36. S.W. Park, S.Y. Hur, N.J. Yoo, and S.H. Lee Somatic frameshift mutations of bone morphogenic protein receptor 2 gene in gastric and colorectal cancers with microsatellite instability APMIS 118 2010 824 829
37. M. Shinohara, M. Mao, T.M. Keeley, M. El-Zaatari, H.J. Lee, K.A. Eaton, L.C. Samuelson, J.L. Merchant, J.R. Goldenring, and A. Todisco Bone morphogenetic protein signaling regulates gastric epithelial cell development and proliferation in mice Gastroenterology 139 2010 2050 2060
38. G.R. van den Brink, J.C. Hardwick, G.N. Tytgat, M.A. Brink, F.J. Ten Kate, S.J. Van Deventer, and M.P. Peppelenbosch Sonic hedgehog regulates gastric gland morphogenesis in man and mouse Gastroenterology 121 2001 317 328 (Pubitemid 32729379)
39. T. Narita, K. Saitoh, T. Kameda, A. Kuroiwa, M. Mizutani, C. Koike, H. Iba, and S. Yasugi BMPs are necessary for stomach gland formation in the chicken embryo: a study using virally induced BMP-2 and Noggin expression Development 127 2000 981 988 (Pubitemid 30162644)
40. X.Z. Wen, Y. Akiyama, S.B. Baylin, and Y. Yuasa Frequent epigenetic silencing of the bone morphogenetic protein 2 gene through methylation in gastric carcinomas Oncogene 25 2006 2666 2673
41. M. Ogawa, K. Maeda, N. Onoda, Y.S. Chung, and M. Sowa Loss of p21WAF1/CIP1 expression correlates with disease progression in gastric carcinoma Br J Cancer 75 1997 1617 1620 (Pubitemid 27229052)
42. Y. Gomyo, M. Ikeda, M. Osaki, S. Tatebe, S. Tsujitani, M. Ikeguchi, N. Kaibara, and H. Ito Expression of p21 (waf1/cip1/sdi1), but not p53 protein, is a factor in the survival of patients with advanced gastric carcinoma Cancer 79 1997 2067 2072 (Pubitemid 27227370)
43. W. Yasui, Y. Akama, H. Kuniyasu, H. Yokozaki, S. Semba, F. Shimamoto, and E. Tahara Expression of cyclin-dependent kinase inhibitor p21WAF1/CIP1 in non-neoplastic mucosa and neoplasia of the stomach: relationship with p53 status and proliferative activity J Pathol 180 1996 122 128 (Pubitemid 26370175)
44. F. Pouliot, and C. Labrie Role of Smad1 and Smad4 proteins in the induction of p21WAF1, Cip1 during bone morphogenetic protein-induced growth arrest in human breast cancer cells J Endocrinol 172 2002 187 198 (Pubitemid 34082957)
45. A. Franzen, and N.E. Heldin BMP-7-induced cell cycle arrest of anaplastic thyroid carcinoma cells via p21(CIP1) and p27(KIP1) Biochem Biophys Res Commun 285 2001 773 781 (Pubitemid 32924836)
46. G.A. Wong, V. Tang, F. El-Sabeawy, and R.H. Weiss BMP-2 inhibits proliferation of human aortic smooth muscle cells via p21Cip1/Waf1 Am J Physiol Endocrinol Metab 284 2003 E972 E979
47. S.F. Chang, T.K. Chang, H.H. Peng, Y.T. Yeh, D.Y. Lee, C.R. Yeh, J. Zhou, C.K. Cheng, C.A. Chang, and J.J. Chiu BMP-4 induction of arrest and differentiation of osteoblast-like cells via p21 CIP1 and p27 KIP1 regulation Mol Endocrinol 23 2009 1827 1838
48. Y. Park, J.W. Kim, D.S. Kim, E.B. Kim, S.J. Park, J.Y. Park, W.S. Choi, J.G. Song, H.Y. Seo, S.C. Oh, B.S. Kim, J.J. Park, Y.H. Kim, and J.S. Kim The bone morphogenesis protein-2 (BMP-2) is associated with progression to metastatic disease in gastric cancer Cancer Res Treat 40 2008 127 132
49. Y. Park, M.H. Kang, H.Y. Seo, J.M. Park, C.W. Choi, Y.H. Kim, I.S. Kim, J.S. Kim, and S.C. Oh Bone morphogenetic protein-2 levels are elevated in the patients with gastric cancer and correlate with disease progression Med Oncol 27 2010 1192 1199
50. M.H. Kang, J.S. Kim, J.E. Seo, S.C. Oh, and Y.A. Yoo BMP2 accelerates the motility and invasiveness of gastric cancer cells via activation of the phosphatidylinositol 3-kinase (PI3K)/Akt pathway Exp Cell Res 316 2010 24 37