Smad4 decreases the population of pancreatic cancer - Initiating cells through transcriptional repression of ALDH1A1

American Journal of Pathology

Volumn 185, Issue 5, 2015, Pages 1457-1470

  Hoshino, Yukari ^a   Nishida, Jun ^a   Katsuno, Yoko ^a   Koinuma, Daizo ^a   Aoki, Taku ^b   Kokudo, Norihiro ^b   Miyazono, Kohei ^a   Ehata, Shogo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE 1A1; ALDEHYDE DEHYDROGENASE ISOENZYME 1; BONE MORPHOGENETIC PROTEIN 4; MESSENGER RNA; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ALDEHYDE DEHYDROGENASE; ALDH1A1 PROTEIN, HUMAN; SMAD4 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ARTICLE; CANCER STEM CELL; CANCER TISSUE; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; ENZYME ACTIVE SITE; ENZYME INDUCTION; ENZYME REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; PANCREAS CELL; PANCREATIC CANCER INITIATING CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; REGULATORY SEQUENCE; TRANSCRIPTION REGULATION; TRANSCRIPTION TERMINATION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GENETICS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; MOUSE; NUDE MOUSE; PANCREAS TUMOR; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; XENOGRAFT;

ALDEHYDE DEHYDROGENASE; ANIMALS; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGRAFTS; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASTIC STEM CELLS; PANCREATIC NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SMAD4 PROTEIN; TRANSCRIPTION, GENETIC; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84928019144     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2015.01.011     Document Type: Article

References (60)

1. M.F. Clarke, J.E. Dick, P.B. Dirks, C.J. Eaves, C.H. Jamieson, D.L. Jones, J. Visvader, I.L. Weissman, and G.M. Wahl Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells Cancer Res 66 2006 9339 9344
2. J.E. Russo, and J. Hilton Characterization of cytosolic aldehyde dehydrogenase from cyclophosphamide resistant L1210 cells Cancer Res 48 1988 2963 2968
3. L. Armstrong, M. Stojkovic, I. Dimmick, S. Ahmad, P. Stojkovic, N. Hole, and M. Lako Phenotypic characterization of murine primitive hematopoietic progenitor cells isolated on basis of aldehyde dehydrogenase activity Stem Cells 22 2004 1142 1151
4. D.A. Hess, L. Wirthlin, T.P. Craft, P.E. Herrbrich, S.A. Hohm, R. Lahey, W.C. Eades, M.H. Creer, and J.A. Nolta Selection based on CD133 and high aldehyde dehydrogenase activity isolates long-term reconstituting human hematopoietic stem cells Blood 107 2006 2162 2169
5. D.A. Hess, T.P. Craft, L. Wirthlin, S. Hohm, P. Zhou, W.C. Eades, M.H. Creer, M.S. Sands, and J.A. Nolta Widespread nonhematopoietic tissue distribution by transplanted human progenitor cells with high aldehyde dehydrogenase activity Stem Cells 26 2008 611 620
6. F. Jiang, Q. Qiu, A. Khanna, N.W. Todd, J. Deepak, L. Xing, H. Wang, Z. Liu, Y. Su, S.A. Stass, and R.L. Katz Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer Mol Cancer Res 7 2009 330 338
7. E.H. Huang, M.J. Hynes, T. Zhang, C. Ginestier, G. Dontu, H. Appelman, J.Z. Fields, M.S. Wicha, and B.M. Boman Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis Cancer Res 69 2009 3382 3389
8. Z.A. Rasheed, J. Yang, Q. Wang, J. Kowalski, I. Freed, C. Murter, S.M. Hong, J.B. Koorstra, N.V. Rajeshkumar, X. He, M. Goggins, C. Iacobuzio-Donahue, D.M. Berman, D. Laheru, A. Jimeno, M. Hidalgo, A. Maitra, and W. Matsui Prognostic significance of tumorigenic cells with mesenchymal features in pancreatic adenocarcinoma J Natl Cancer Inst 102 2010 340 351
9. C. Ginestier, M.H. Hur, E. Charafe-Jauffret, F. Monville, J. Dutcher, M. Brown, J. Jacquemier, P. Viens, C.G. Kleer, S. Liu, A. Schott, D. Hayes, D. Birnbaum, M.S. Wicha, and G. Dontu ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome Cell Stem Cell 1 2007 555 567
10. Y. Katsuno, S. Ehata, M. Yashiro, K. Yanagihara, K. Hirakawa, and K. Miyazono Coordinated expression of REG4 and aldehyde dehydrogenase 1 regulating tumourigenic capacity of diffuse-type gastric carcinoma-initiating cells is inhibited by TGF-β J Pathol 228 2012 391 404
11. Y. Ohi, Y. Umekita, T. Yoshioka, M. Souda, Y. Rai, Y. Sagara, and A. Tanimoto Aldehyde dehydrogenase 1 expression predicts poor prognosis in triple-negative breast cancer Histopathology 59 2011 776 780
12. C.H. Heldin, K. Miyazono, and P. ten Dijke TGF-β signalling from cell membrane to nucleus through SMAD proteins Nature 390 1997 465 471
13. B. Bierie, and H. Moses Tumour microenvironment: TGFβ: the molecular Jekyll and Hyde of cancer Nat Rev Cancer 6 2006 506 520
14. N. Bardeesy, and R.A. DePinho Pancreatic cancer biology and genetics Nat Rev Cancer 2 2002 897 909
15. A. Blackford, O.K. Serrano, C.L. Wolfgang, G. Parmigiani, S. Jones, X. Zhang, D.W. Parsons, J.C. Lin, R.J. Leary, J.R. Eshleman, M. Goggins, E.M. Jaffee, C.A. Iacobuzio-Donahue, A. Maitra, J.L. Cameron, K. Olino, R. Schulick, J. Winter, J.M. Herman, D. Laheru, A.P. Klein, B. Vogelstein, K.W. Kinzler, V.E. Velculescu, and R.H. Hruban SMAD4 gene mutations are associated with poor prognosis in pancreatic cancer Clin Cancer Res 15 2009 4674 4679
16. H. Ijichi, M. Otsuka, K. Tateishi, T. Ikenoue, T. Kawakami, F. Kanai, Y. Arakawa, N. Seki, K. Shimizu, K. Miyazono, T. Kawabe, and M. Omata Smad4-independent regulation of p21/WAF1 by transforming growth factor-β Oncogene 23 2004 1043 1051
17. K. Horiguchi, T. Shirakihara, A. Nakano, T. Imamura, K. Miyazono, and M. Saitoh Role of Ras signaling in the induction of snail by transforming growth factor-β J Biol Chem 284 2009 245 253
18. 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-β 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
19. H. Nishimori, S. Ehata, H.I. Suzuki, Y. Katsuno, and K. Miyazono Prostate cancer cells and bone stromal cells mutually interact with each other through bone morphogenetic protein-mediated signals J Biol Chem 287 2012 20037 20046
20. Y. Hoshino, Y. Katsuno, S. Ehata, and K. Miyazono Autocrine TGF-β protects breast cancer cells from apoptosis through reduction of BH3-only protein, Bim J Biochem 149 2011 55 65
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-β decreases the cancer-initiating cell population within diffuse-type gastric carcinoma cells Oncogene 30 2011 1693 1705
22. D. Koinuma, S. Tsutsumi, N. Kamimura, H. Taniguchi, K. Miyazawa, M. Sunamura, T. Imamura, K. Miyazono, and H. Aburatani Chromatin immunoprecipitation on microarray analysis of Smad2/3 binding sites reveals roles of ETS1 and TFAP2A in transforming growth factor β signaling Mol Cell Biol 29 2009 172 186
23. M. Morikawa, D. Koinuma, K. Miyazono, and C.H. Heldin Genome-wide mechanisms of Smad binding Oncogene 32 2013 1609 1615
24. Y.T. Shirai, S. Ehata, M. Yashiro, K. Yanagihara, K. Hirakawa, and K. Miyazono Bone morphogenetic protein-2 and -4 play tumor suppressive roles in human diffuse-type gastric carcinoma Am J Pathol 179 2011 2920 2930
25. K.C. Kawabata, S. Ehata, A. Komuro, K. Takeuchi, and K. Miyazono TGF-β-induced apoptosis of B-cell lymphoma Ramos cells through reduction of MS4A1/CD20 Oncogene 32 2013 2096 2106
26. C. Carbone, and D. Melisi NF-κB as a target for pancreatic cancer therapy Expert Opin Ther Targets 16 Suppl 2 2012 S1 S10
27. Y. Lu, H. Zhu, H. Shan, J. Lu, X. Chang, X. Li, X. Fan, S. Zhu, Y. Wang, Q. Guo, L. Wang, Y. Huang, M. Zhu, and Z. Wang Knockdown of Oct4 and Nanog expression inhibits the stemness of pancreatic cancer cells Cancer Lett 340 2013 113 123
28. J.E. Visvader, and G.J. Lindeman Cancer stem cells in solid tumours: accumulating evidence and unresolved questions Nat Rev Cancer 8 2008 755 768
29. C. Li, D. Heidt, P. Dalerba, C. Burant, L. Zhang, V. Adsay, M. Wicha, M. Clarke, and D. Simeone Identification of pancreatic cancer stem cells Cancer Res 67 2007 1030 1037
30. P. Hermann, S. Huber, T. Herrler, A. Aicher, J. Ellwart, M. Guba, C. Bruns, and C. Heeschen Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer Cell Stem Cell 1 2007 313 323
31. N. Bardeesy, K.H. Cheng, J.H. Berger, G.C. Chu, J. Pahler, P. Olson, A.F. Hezel, J. Horner, G.Y. Lauwers, D. Hanahan, and R.A. DePinho Smad4 is dispensable for normal pancreas development yet critical in progression and tumor biology of pancreas cancer Genes Dev 20 2006 3130 3146
32. P. Marcato, C.A. Dean, C.A. Giacomantonio, and P.W. Lee Aldehyde dehydrogenase: its role as a cancer stem cell marker comes down to the specific isoform Cell Cycle 10 2011 1378 1384
33. K.L. Woodford-Richens, A.J. Rowan, R. Poulsom, S. Bevan, R. Salovaara, L.A. Aaltonen, R.S. Houlston, N.A. Wright, and I.P. Tomlinson Comprehensive analysis of SMAD4 mutations and protein expression in juvenile polyposis: evidence for a distinct genetic pathway and polyp morphology in SMAD4 mutation carriers Am J Pathol 159 2001 1293 1300
34. M. Miyaki, T. Iijima, M. Konishi, K. Sakai, A. Ishii, M. Yasuno, T. Hishima, M. Koike, N. Shitara, T. Iwama, J. Utsunomiya, T. Kuroki, and T. Mori Higher frequency of Smad4 gene mutation in human colorectal cancer with distant metastasis Oncogene 18 1999 3098 3103
35. W. Xie, S. Bharathy, D. Kim, B.G. Haffty, D.L. Rimm, and M. Reiss Frequent alterations of Smad signaling in human head and neck squamous cell carcinomas: a tissue microarray analysis Oncol Res 14 2003 61 73
36. K. Takaku, H. Miyoshi, A. Matsunaga, M. Oshima, N. Sasaki, and M.M. Taketo Gastric and duodenal polyps in Smad4 (Dpc4) knockout mice Cancer Res 59 1999 6113 6117
37. K. Takaku, M. Oshima, H. Miyoshi, M. Matsui, M.F. Seldin, and M.M. Taketo Intestinal tumorigenesis in compound mutant mice of both Dpc4 (Smad4) and Apc genes Cell 92 1998 645 656
38. X. Xu, B. Ehdaie, N. Ohara, T. Yoshino, and C.X. Deng Synergistic action of Smad4 and Pten in suppressing pancreatic ductal adenocarcinoma formation in mice Oncogene 29 2010 674 686
39. D.G. Duda, M. Sunamura, L.P. Lefter, T. Furukawa, T. Yokoyama, T. Yatsuoka, T. Abe, H. Inoue, F. Motoi, S. Egawa, S. Matsuno, and A. Horii Restoration of SMAD4 by gene therapy reverses the invasive phenotype in pancreatic adenocarcinoma cells Oncogene 22 2003 6857 6864
40. R.H. Xu, T.L. Sampsell-Barron, F. Gu, S. Root, R.M. Peck, G. Pan, J. Yu, J. Antosiewicz-Bourget, S. Tian, R. Stewart, and J.A. Thomson NANOG is a direct target of TGFβ/activin-mediated SMAD signaling in human ESCs Cell Stem Cell 3 2008 196 206
41. M. Sakaki-Yumoto, J. Liu, M. Ramalho-Santos, N. Yoshida, and R. Derynck Smad2 is essential for maintenance of the human and mouse primed pluripotent stem cell state J Biol Chem 288 2013 18546 18560
42. J.P. Chute, G.G. Muramoto, J. Whitesides, M. Colvin, R. Safi, N.J. Chao, and D.P. McDonnell Inhibition of aldehyde dehydrogenase and retinoid signaling induces the expansion of human hematopoietic stem cells Proc Natl Acad Sci U S A 103 2006 11707 11712
43. S.J. Dylla, L. Beviglia, I.K. Park, C. Chartier, J. Raval, L. Ngan, K. Pickell, J. Aguilar, S. Lazetic, S. Smith-Berdan, M.F. Clarke, T. Hoey, J. Lewicki, and A.L. Gurney Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy PLoS One 3 2008 e2428
44. G.G. Muramoto, J.L. Russell, R. Safi, A.B. Salter, H.A. Himburg, P. Daher, S.K. Meadows, P. Doan, R.W. Storms, N.J. Chao, D.P. McDonnell, and J.P. Chute Inhibition of aldehyde dehydrogenase expands hematopoietic stem cells with radioprotective capacity Stem Cells 28 2010 523 534
45. S.K. Kim, H. Kim, D.H. Lee, T.S. Kim, T. Kim, C. Chung, G.Y. Koh, H. Kim, and D.S. Lim Reversing the intractable nature of pancreatic cancer by selectively targeting ALDH-high, therapy-resistant cancer cells PLoS One 8 2013 e78130
46. J.S. Moreb, C. Turner, L. Sreerama, J.R. Zucali, N.E. Sladek, and M. Schweder Interleukin-1 and tumor necrosis factor α induce class 1 aldehyde dehydrogenase mRNA and protein in bone marrow cells Leuk Lymphoma 20 1995 77 84
47. X. Wang, H. Lu, T. Li, L. Yu, G. Liu, X. Peng, and J. Zhao Kruppel-like factor 8 promotes tumorigenic mammary stem cell induction by targeting miR-146a Am J Cancer Res 3 2013 356 373
48. G. Elizondo, J. Corchero, E. Sterneck, and F.J. Gonzalez Feedback inhibition of the retinaldehyde dehydrogenase gene ALDH1 by retinoic acid through retinoic acid receptor α and CCAAT/enhancer-binding protein β J Biol Chem 275 2000 39747 39753
49. X. Mu, C. Isaac, N. Greco, J. Huard, and K. Weiss Notch signaling is associated with ALDH activity and an aggressive metastatic phenotype in murine osteosarcoma cells Front Oncol 3 2013 143
50. D. Koinuma, S. Tsutsumi, N. Kamimura, T. Imamura, H. Aburatani, and K. Miyazono Promoter-wide analysis of Smad4 binding sites in human epithelial cells Cancer Sci 100 2009 2133 2142
51. K. Verschueren, J.E. Remacle, C. Collart, H. Kraft, B.S. Baker, P. Tylzanowski, L. Nelles, G. Wuytens, M.T. Su, R. Bodmer, J.C. Smith, and D. Huylebroeck SIP1, a novel zinc finger/homeodomain repressor, interacts with Smad proteins and binds to 5′-CACCT sequences in candidate target genes J Biol Chem 274 1999 20489 20498
52. E. Lonardo, P.C. Hermann, M.T. Mueller, S. Huber, A. Balic, I. Miranda-Lorenzo, S. Zagorac, S. Alcala, I. Rodriguez-Arabaolaza, J.C. Ramirez, R. Torres-Ruíz, E. Garcia, M. Hidalgo, D. Cebrián, R. Heuchel, M. Löhr, F. Berger, P. Bartenstein, A. Aicher, and C. Heeschen Nodal/Activin signaling drives self-renewal and tumorigenicity of pancreatic cancer stem cells and provides a target for combined drug therapy Cell Stem Cell 9 2011 433 446
53. B. Tang, N. Yoo, M. Vu, M. Mamura, J.S. Nam, A. Ooshima, Z. Du, P.Y. Desprez, M.R. Anver, A.M. Michalowska, J. Shih, W.T. Parks, and L.M. Wakefield Transforming growth factor-β can suppress tumorigenesis through effects on the putative cancer stem or early progenitor cell and committed progeny in a breast cancer xenograft model Cancer Res 67 2007 8643 8652
54. M. Schober, and E. Fuchs Tumor-initiating stem cells of squamous cell carcinomas and their control by TGF-β and integrin/focal adhesion kinase (FAK) signaling Proc Natl Acad Sci U S A 108 2011 10544 10549
55. S.A. Mani, W. Guo, M.J. Liao, E.N. Eaton, A. Ayyanan, A.Y. Zhou, M. Brooks, F. Reinhard, C.C. Zhang, M. Shipitsin, L.L. Campbell, K. Polyak, C. Brisken, J. Yang, and R.A. Weinberg The epithelial-mesenchymal transition generates cells with properties of stem cells Cell 133 2008 704 715
56. C. Scheel, E.N. Eaton, S.H. Li, C.L. Chaffer, F. Reinhardt, K.J. Kah, G. Bell, W. Guo, J. Rubin, A.L. Richardson, and R.A. Weinberg Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast Cell 145 2011 926 940
57. L. Cao, M. Shao, J. Schilder, T. Guise, K.S. Mohammad, and D. Matei Tissue transglutaminase links TGF-β, epithelial to mesenchymal transition and a stem cell phenotype in ovarian cancer Oncogene 31 2012 2521 2534
58. S. Peñuelas, J. Anido, R.M. Prieto-Sánchez, G. Folch, I. Barba, I. Cuartas, D. García-Dorado, M.A. Poca, J. Sahuquillo, J. Baselga, and J. Seoane TGF-β increases glioma-initiating cell self-renewal through the induction of LIF in human glioblastoma Cancer Cell 15 2009 315 327
59. H. Ikushima, T. Todo, Y. Ino, M. Takahashi, K. Miyazawa, and K. Miyazono Autocrine TGF-β signaling maintains tumorigenicity of glioma-initiating cells through Sry-related HMG-box factors Cell Stem Cell 5 2009 504 514
60. S. Ehata, Y. Yokoyama, K. Takahashi, and K. Miyazono Bi-directional roles of bone morphogenetic proteins in cancer: another molecular Jekyll and Hyde? Pathol Int 63 2013 287 296