ATOH1 can regulate the tumorigenicity of gastric cancer cells by inducing the differentiation of cancer stem cells

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Han, Myoung Eun ^a,b   Baek, Su Jin ^c   Kim, Seon Young ^a   Kang, Chi Dug ^a   Oh, Sae Ock ^a  

^a Pusan National University School of Medicine   (South Korea)

^b Pusan National University   (South Korea)

^c Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ATONAL HOMOLOG 1 PROTEIN; MESSENGER RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ATOH1 PROTEIN, HUMAN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; RASSF4 PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

APOPTOSIS; ARTICLE; ATOH1 GENE; CANCER STEM CELL; CARCINOGENICITY; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; GASTRIC CANCER CELL LINE; GENE OVEREXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LIVER METASTASIS; REAL TIME POLYMERASE CHAIN REACTION; STOMACH CANCER; TUMOR XENOGRAFT; WESTERN BLOTTING; ANIMAL; CARCINOGENESIS; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PROMOTER REGION; SCID MOUSE; SIGNAL TRANSDUCTION; STOMACH; STOMACH TUMOR; TUMOR CELL CULTURE; TUMOR CELL LINE; UPREGULATION;

LENTIVIRUS;

ANIMALS; APOPTOSIS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CARCINOGENESIS; CELL DIFFERENTIATION; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE, SCID; NEOPLASTIC STEM CELLS; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION; STOMACH; STOMACH NEOPLASMS; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

EID: 84929096302     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126085     Document Type: Article

References (41)

1. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, et al. (1994) A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367: 645-648.
2. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, et al. (2004) Identification of human brain tumour initiating cells. Nature 432: 396-401. PMID: 15549107
3. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100: 3983-3988. PMID: 12629218
4. O'Brien CA, Pollett A, Gallinger S, Dick JE (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445: 106-110. PMID: 17122772
5. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, et al. (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445: 111-115. PMID: 17122771
6. Han ME, Jeon TY, Hwang SH, Lee YS, Kim HJ, et al. (2011) Cancer spheres from gastric cancer patients provide an ideal model system for cancer stem cell research. Cell Mol Life Sci 68: 3589-3605. doi: 10.1007/s00018-011-0672-z PMID: 21448722
7. Li F, Tiede B, Massague J, Kang Y (2007) Beyond tumorigenesis: cancer stem cells in metastasis. Cell Res 17: 3-14. PMID: 17179981
8. Scopelliti A, Cammareri P, Catalano V, Saladino V, Todaro M, et al. (2009) Therapeutic implications of Cancer Initiating Cells. Expert Opin Biol Ther 9: 1005-1016. doi: 10.1517/14712590903066687 PMID: 19545218
9. Wang JC (2007) Evaluating therapeutic efficacy against cancer stem cells: new challenges posed by a new paradigm. Cell Stem Cell 1: 497-501. PMID: 18938746
10. Eppert K, Takenaka K, Lechman ER, Waldron L, Nilsson B, et al. (2011) Stem cell gene expression programs influence clinical outcome in human leukemia. Nat Med 17: 1086-1093. doi: 10.1038/nm.2415 PMID: 21873988
11. Vincent A, Van Seuningen I (2012) On the epigenetic origin of cancer stem cells. Biochim Biophys Acta 1826: 83-88. doi: 10.1016/j.bbcan.2012.03.009 PMID: 22495062
12. Wang Y, Cardenas H, Fang F, Condello S, Taverna P, et al. (2014) Epigenetic Targeting of Ovarian Cancer Stem Cells. Cancer Res.
13. Vermeulen L, De Sousa EMF, van der Heijden M, Cameron K, de Jong JH, et al. (2010) Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 12: 468-476. doi: 10.1038/ncb2048 PMID: 20418870
14. Bots M, Verbrugge I, Martin BP, Salmon JM, Ghisi M, et al. (2014) Differentiation therapy for the treatment of t(8;21) acute myeloid leukemia using histone deacetylase inhibitors. Blood 123: 1341-1352. doi: 10.1182/blood-2013-03-488114 PMID: 24415537
15. He LZ, Tolentino T, Grayson P, Zhong S, Warrell RP Jr., et al. (2001) Histone deacetylase inhibitors induce remission in transgenic models of therapy-resistant acute promyelocytic leukemia. J Clin Invest 108: 1321-1330. PMID: 11696577
16. Park DJ, Chumakov AM, Vuong PT, Chih DY, Gombart AF, et al. (1999) CCAAT/enhancer binding protein epsilon is a potential retinoid target gene in acute promyelocytic leukemia treatment. J Clin Invest 103: 1399-1408. PMID: 10330422
17. Truong BT, Lee YJ, Lodie TA, Park DJ, Perrotti D, et al. (2003) CCAAT/Enhancer binding proteins repress the leukemic phenotype of acute myeloid leukemia. Blood 101: 1141-1148. PMID: 12393450
18. Halmos B, Huettner CS, Kocher O, Ferenczi K, Karp DD, et al. (2002) Down-regulation and antiproliferative role of C/EBPalpha in lung cancer. Cancer Res 62: 528-534. PMID: 11809705
19. Radomska HS, Huettner CS, Zhang P, Cheng T, Scadden DT, et al. (1998) CCAAT/enhancer binding protein alpha is a regulatory switch sufficient for induction of granulocytic development from bipotential myeloid progenitors. Mol Cell Biol 18: 4301-4314. PMID: 9632814
20. Wang X, Scott E, Sawyers CL, Friedman AD (1999) C/EBPalpha bypasses granulocyte colony-stimulating factor signals to rapidly induce PU.1 gene expression, stimulate granulocytic differentiation, and limit proliferation in 32D cl3 myeloblasts. Blood 94: 560-571. PMID: 10397723
21. Choe G, Kim WH, Park JG, Kim YI (1997) Effect of suramin on differentiation of human stomach cancer cell lines. J Korean Med Sci 12: 433-442. PMID: 9364302
22. Ben-Arie N, McCall AE, Berkman S, Eichele G, Bellen HJ, et al. (1996) Evolutionary conservation of sequence and expression of the bHLH protein Atonal suggests a conserved role in neurogenesis. Hum Mol Genet 5: 1207-1216. PMID: 8872459
23. Akazawa C, Ishibashi M, Shimizu C, Nakanishi S, Kageyama R (1995) A mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. J Biol Chem 270: 8730-8738. PMID: 7721778
24. Jensen J, Pedersen EE, Galante P, Hald J, Heller RS, et al. (2000) Control of endodermal endocrine development by Hes-1. Nat Genet 24: 36-44. PMID: 10615124
25. Bossuyt W, Kazanjian A, De Geest N, Van Kelst S, De Hertogh G, et al. (2009) Atonal homolog 1 is a tumor suppressor gene. PLoS Biol 7: e39. doi: 10.1371/journal.pbio.1000039 PMID: 19243219
26. Yang Q, Bermingham NA, Finegold MJ, Zoghbi HY (2001) Requirement of Math1 for secretory cell line-age commitment in the mouse intestine. Science 294: 2155-2158. PMID: 11739954
27. VanDussen KL, Samuelson LC (2010) Mouse atonal homolog 1 directs intestinal progenitors to secretory cell rather than absorptive cell fate. Dev Biol 346: 215-223. doi: 10.1016/j.ydbio.2010.07.026 PMID: 20691176
28. Jeon TY, Han ME, Lee YW, Lee YS, Kim GH, et al. (2010) Overexpression of stathmin1 in the diffuse type of gastric cancer and its roles in proliferation and migration of gastric cancer cells. Br J Cancer 102: 710-718. doi: 10.1038/sj.bjc.6605537 PMID: 20087351
29. Lai HC, Klisch TJ, Roberts R, Zoghbi HY, Johnson JE (2011) In vivo neuronal subtype-specific targets of Atoh1 (Math1) in dorsal spinal cord. J Neurosci 31: 10859-10871. doi: 10.1523/JNEUROSCI.0445-11.2011 PMID: 21795538
30. Bossuyt W, De Geest N, Aerts S, Leenaerts I, Marynen P, et al. (2009) The atonal proneural transcription factor links differentiation and tumor formation in Drosophila. PLoS Biol 7: e40. doi: 10.1371/journal.pbio.1000040 PMID: 19243220
31. Leow CC, Romero MS, Ross S, Polakis P, Gao WQ (2004) Hath1, down-regulated in colon adenocarcinomas, inhibits proliferation and tumorigenesis of colon cancer cells. Cancer Res 64: 6050-6057. PMID: 15342386
32. Hatten ME, Alder J, Zimmerman K, Heintz N (1997) Genes involved in cerebellar cell specification and differentiation. Curr Opin Neurobiol 7: 40-47. PMID: 9039803
33. Vaillant C, Monard D (2009) SHH pathway and cerebellar development. Cerebellum 8: 291-301. doi: 10.1007/s12311-009-0094-8 PMID: 19224309
34. Pogoriler J, Millen K, Utset M, Du W (2006) Loss of cyclin D1 impairs cerebellar development and suppresses medulloblastoma formation. Development 133: 3929-3937. PMID: 16943274
35. Klisch TJ, Xi Y, Flora A, Wang L, Li W, et al. (2011) In vivo Atoh1 targetome reveals how a proneural transcription factor regulates cerebellar development. Proc Natl Acad Sci U S A 108: 3288-3293. doi: 10.1073/pnas.1100230108 PMID: 21300888
36. Forget A, Bihannic L, Cigna SM, Lefevre C, Remke M, et al. (2014) Shh signaling protects Atoh1 from degradation mediated by the E3 ubiquitin ligase Huwe1 in neural precursors. Dev Cell 29: 649-661. doi: 10.1016/j.devcel.2014.05.014 PMID: 24960692
37. Flora A, Klisch TJ, Schuster G, Zoghbi HY (2009) Deletion of Atoh1 disrupts Sonic Hedgehog signaling in the developing cerebellum and prevents medulloblastoma. Science 326: 1424-1427. doi: 10.1126/science.1181453 PMID: 19965762
38. Park ET, Oh HK, Gum JR Jr., Crawley SC, Kakar S, et al. (2006) HATH1 expression in mucinous cancers of the colorectum and related lesions. Clin Cancer Res 12: 5403-5410. PMID: 17000673
39. Zhang X, Yu H, Yang Y, Zhu R, Bai J, et al. (2010) SOX2 in gastric carcinoma, but not Hath1, is related to patients' clinicopathological features and prognosis. J Gastrointest Surg 14: 1220-1226. doi: 10.1007/s11605-010-1246-3 PMID: 20532662
40. Sekine A, Akiyama Y, Yanagihara K, Yuasa Y (2006) Hath1 up-regulates gastric mucin gene expression in gastric cells. Biochem Biophys Res Commun 344: 1166-1171. PMID: 16647036
41. Mutoh H, Sakamoto H, Hayakawa H, Arao Y, Satoh K, et al. (2006) The intestine-specific homeobox gene Cdx2 induces expression of the basic helix-loop-helix transcription factor Math1. Differentiation 74: 313-321. PMID: 16831200