A NOTCH3-mediated squamous cell differentiation program limits expansion of EMT-competent cells that express the ZEB transcription factors

Cancer Research

Volumn 71, Issue 21, 2011, Pages 6836-6847

  Ohashi, Shinya ^a,b,e   Natsuizaka, Mitsuteru ^a,b   Naganuma, Seiji ^a,b,f   Kagawa, Shingo ^a,b   Kimura, Sotai ^f   Itoh, Hiroshi ^f   Kalman, Ross A ^a,b   Nakagawa, Momo ^a,b   Darling, Douglas S ^g   Basu, Devraj ^a,d   Gimotty, Phyllis A ^a,b   Klein Szanto, Andres J ^c   Diehl, J Alan ^a,b   Herlyn, Meenhard ^d   Nakagawa, Hiroshi ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c FOX CHASE CANCER CENTER   (United States)

^d WISTAR INSTITUTE   (United States)

^e Kitano Hospital   (Japan)

^f UNIVERSITY OF FUKUI   (Japan)

^g UNIVERSITY OF LOUISVILLE SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MASTERMIND LIKE 1 PROTEIN; MICRORNA; MICRORNA 200; NOTCH3 RECEPTOR; PROTEIN; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ZINC FINGER E BOX BINDING PROTEIN 1; ZINC FINGER E BOX BINDING PROTEIN 2;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER INVASION; CARCINOGENESIS; CELL; CELL DIFFERENTIATION; CELL EXPANSION; CELL SUBPOPULATION; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; ESOPHAGEAL CELL; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; GENE; GENE INDUCTION; GENE TARGETING; GENETIC TRANSCRIPTION; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; MULTIGENE FAMILY; NONHUMAN; NOTCH3 GENE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR BLOCKING; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SQUAMOUS CELL; TISSUE ENGINEERING; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; CADHERINS; CARCINOMA, SQUAMOUS CELL; CELL DIVISION; CELL LINE, TUMOR; DNA-BINDING PROTEINS; EPITHELIAL-MESENCHYMAL TRANSITION; ESOPHAGEAL NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; MICE; MICE, NUDE; MICRORNAS; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; RECEPTORS, NOTCH; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; RNA INTERFERENCE; RNA, NEOPLASM; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TUMOR STEM CELL ASSAY;

EID: 80155126639     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-0846     Document Type: Article

References (50)

1. Enzinger PC, Mayer RJ. Esophageal cancer. N Engl J Med 2003;349:2241-52. (Pubitemid 37485141)
2. McElhinny AS, Li JL, Wu L. Mastermind-like transcriptional co-activators: emerging roles in regulating cross talk among multiple signaling pathways. Oncogene 2008;27:5138-47.
3. Blanpain C, Lowry WE, Pasolli HA, Fuchs E. Canonical notch signaling functions as a commitment switch in the epidermal lineage. Genes Dev 2006;20:3022-35. (Pubitemid 44771736)
4. Nicolas M, Wolfer A, Raj K, Kummer JA, Mill P, van Noort M, et al. Notch1 functions as a tumor suppressor in mouse skin. Nat Genet 2003;33:416-21. (Pubitemid 36278861)
5. Lefort K, Mandinova A, Ostano P, Kolev V, Calpini V, Kolfschoten I, et al. Notch1 is a p53 target gene involved in human keratinocyte tumor suppression through negative regulation of ROCK1/2 and MRCKalpha kinases. Genes Dev 2007;21:562-77. (Pubitemid 46409471)
6. Pan Y, Lin MH, Tian X, Cheng HT, Gridley T, Shen J, et al. gamma-secretase functions through Notch signaling to maintain skin appendages but is not required for their patterning or initial morphogenesis. Dev Cell 2004;7:731-43. (Pubitemid 39462693)
7. Li T, Wen H, Brayton C, Das P, Smithson LA, Fauq A, et al. Epidermal growth factor receptor and notch pathways participate in the tumor suppressor function of gamma-secretase. J Biol Chem 2007; 282:32264-73. (Pubitemid 350106457)
8. Proweller A, Tu L, Lepore JJ, Cheng L, Lu MM, Seykora J, et al. Impaired notch signaling promotes de novo squamous cell carcinoma formation. Cancer Res 2006;66:7438-44. (Pubitemid 44289196)
9. Demehri S, Turkoz A, Kopan R. Epidermal Notch1 loss promotes skin tumorigenesis by impacting the stromal microenvironment. Cancer Cell 2009;16:55-66.
10. Ohashi S, Natsuizaka M, Yashiro-Ohtani Y, Kalman RA, Nakagawa M, Wu L, et al. NOTCH1 and NOTCH3 coordinate esophageal squamous differentiation through a CSL-dependent transcriptional network. Gastroenterology 2010;139:2113-23.
11. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest 2009;119:1420-8.
12. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 2007;7:415-28. (Pubitemid 46809165)
13. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009;139:871-90.
14. Natsuizaka M, Ohashi S, Wong GS, Ahmadi A, Kalman RA, Budo D, et al. Insulin-like growth factor-binding protein-3 promotes transforming growth factor-{beta}1-mediated epithelial-to-mesenchymal transition and motility in transformed human esophageal cells. Carcinogenesis 2010;31:1344-53.
15. Yuen HF, Chan YP, Wong ML, Kwok WK, Chan KK, Lee PY, et al. Upregulation of Twist in oesophageal squamous cell carcinoma is associated with neoplastic transformation and distant metastasis. J Clin Pathol 2007;60:510-4. (Pubitemid 46867160)
16. Usami Y, Satake S, Nakayama F, Matsumoto M, Ohnuma K, Komori T, et al. Snail-associated epithelial-mesenchymal transition promotes oesophageal squamous cell carcinoma motility and progression. J Pathol 2008;215:330-9. (Pubitemid 351956714)
17. Uchikado Y, Natsugoe S, Okumura H, Setoyama T, Matsumoto M, Ishigami S, et al. Slug Expression in the E-cadherin preserved tumors is related to prognosis in patients with esophageal squamous cell carcinoma. Clin Cancer Res 2005;11:1174-80. (Pubitemid 40175768)
18. Natsugoe S, Uchikado Y, Okumura H, Matsumoto M, Setoyama T, Tamotsu K, et al. Snail plays a key role in E-cadherin-preserved esophageal squamous cell carcinoma. Oncol Rep 2007;17: 517-23.
19. Ansieau S, Bastid J, Doreau A, Morel AP, Bouchet BP, Thomas C, et al. Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 2008; 14:79-89. (Pubitemid 351890463)
20. Zavadil J, Bottinger EP. TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 2005;24:5764-74.
21. Natsugoe S, Xiangming C, Matsumoto M, Okumura H, Nakashima S, Sakita H, et al. Smad4 and transforming growth factor beta1 expression in patients with squamous cell carcinoma of the esophagus. Clin Cancer Res 2002;8:1838-42. (Pubitemid 34633743)
22. Ansieau S, Hinkal G, Thomas C, Bastid J, Puisieux A. Early origin of cancer metastases: dissemination and evolution of premalignant cells. Cell Cycle 2008;7:3659-63.
23. Ohashi S, Natsuizaka M, Wong GS, Michaylira CZ, Grugan KD, Stairs DB, et al. Epidermal growth factor receptor and mutant p53 expand an esophageal cellular subpopulation capable of epithelial-to-mesenchymal transition through ZEB transcription factors. Cancer Res 2010;70:4174-84.
24. Liu Y, El-Naggar S, Darling DS, Higashi Y, Dean DC. Zeb1 links epithelial-mesenchymal transition and cellular senescence. Development 2008;135:579-88.
25. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A, et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 2009;11: 1487-95.
26. Brabletz S, Brabletz T. The ZEB/miR-200 feedback loop-a motor of cellular plasticity in development and cancer? EMBO Rep 2010;11: 670-7.
27. Lee JJ, Natsuizaka M, Ohashi S, Wong GS, Takaoka M, Michaylira CZ, et al. Hypoxia activates the cyclooxygenase-2-prostaglandin E synthase axis. Carcinogenesis 2010;31:427-34.
28. Okano J, Gaslightwala I, Birnbaum MJ, Rustgi AK, Nakagawa H. Akt/ protein kinase B isoforms are differentially regulated by epidermal growth factor stimulation. J Biol Chem 2000;275:30934-42.
29. Harada H, Nakagawa H, Oyama K, Takaoka M, Andl CD, Jacobmeier B, et al. Telomerase induces immortalization of human esophageal keratinocytes without p16INK4a inactivation. Mol Cancer Res 2003;1:729-38. (Pubitemid 37025591)
30. Kim SH, Nakagawa H, Navaraj A, Naomoto Y, Klein-Szanto AJ, Rustgi AK, et al. Tumorigenic conversion of primary human esophageal epithelial cells using oncogene combinations in the absence of exogenous Ras. Cancer Res 2006;66:10415-24. (Pubitemid 44799762)
31. Okawa T, Michaylira CZ, Kalabis J, Stairs DB, Nakagawa H, Andl CD, et al. The functional interplay between EGFR overexpression, hTERT activation, and p53 mutation in esophageal epithelial cells with activation of stromal fibroblasts induces tumor development, invasion, and differentiation. Genes Dev 2007;21:2788-803. (Pubitemid 350070724)
32. Johnstone CN, Mongroo PS, Rich AS, Schupp M, Bowser MJ, Delemos AS, et al. Parvin-beta inhibits breast cancer tumorigenicity and promotes CDK9-mediated peroxisome proliferator-activated receptor gamma 1 phosphorylation. Mol Cell Biol 2008;28:687-704.
33. Takaoka M, Kim SH, Okawa T, Michaylira CZ, Stairs DB, Johnstone CN, et al. IGFBP-3 regulates esophageal tumor growth through IGF-dependent and independent mechanisms. Cancer Biol Ther 2007;6:534-40. (Pubitemid 47328327)
34. Takaoka M, Harada H, Andl CD, Oyama K, Naomoto Y, Dempsey KL, et al. Epidermal growth factor receptor regulates aberrant expression of insulin-like growth factor-binding protein 3. Cancer Res 2004;64:7711-23. (Pubitemid 39446902)
35. Darling DS, Stearman RP, Qi Y, Qiu MS, Feller JP. Expression of Zfhep/ deltaEF1 protein in palate, neural progenitors, and differentiated neurons. Gene Expr Patterns 2003;3:709-17. (Pubitemid 37451852)
36. Grugan KD, Miller CG, Yao Y, Michaylira CZ, Ohashi S, Klein-Szanto AJ, et al. Fibroblast-secreted hepatocyte growth factor plays a functional role in esophageal squamous cell carcinoma invasion. Proc Natl Acad Sci U S A 2010;107:11026-31.
37. Tetreault MP, Wang ML, Yang Y, Travis J, Yu QC, Klein-Szanto AJ, et al. Klf4 overexpression activates epithelial cytokines and inflammation- mediated esophageal squamous cell cancer in mice. Gastroenterology 2010;139:2124-34. e9.
38. Li B, Tsao SW, Li YY, Wang X, Ling MT, Wong YC, et al. Id-1 promotes tumorigenicity and metastasis of human esophageal cancer cells through activation of PI3K/AKT signaling pathway. Int J Cancer 2009;125:2576-85.
39. Vandewalle C, Van Roy F, Berx G. The role of the ZEB family of transcription factors in development and disease. Cell Mol Life Sci 2009;66:773-87.
40. Aigner K, Dampier B, Descovich L, Mikula M, Sultan A, Schreiber M, et al. The transcription factor ZEB1 (deltaEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene 2007;26:6979-88. (Pubitemid 350014612)
41. Michaylira CZ, Wong GS, Miller CG, Gutierrez CM, Nakagawa H, Hammond R, et al. Periostin, a cell adhesion molecule, facilitates invasion in the tumor microenvironment and annotates a novel tumor-invasive signature in esophageal cancer. Cancer Res 2010;70:5281-92.
42. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008;133:704-15. (Pubitemid 351636299)
43. Gibbons DL, Lin W, Creighton CJ, Rizvi ZH, Gregory PA, Goodall GJ, et al. Contextual extracellular cues promote tumor cell EMT and metastasis by regulating miR-200 family expression. Gene Dev 2009;23:2140-51.
44. Chua HL, Bhat-Nakshatri P, Clare SE, Morimiya A, Badve S, Nakshatri H. NF-kappaB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2. Oncogene 2007;26:711-24. (Pubitemid 46204250)
45. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 2008;22: 894-907. (Pubitemid 351482843)
46. Wiklund ED, Bramsen JB, Hulf T, Dyrskjot L, Ramanathan R, Hansen TB, et al. Coordinated epigenetic repression of the miR- 200 family and miR-205 in invasive bladder cancer. Int J Cancer 2011;128:1327-34.
47. Wang Z, Li Y, Kong D, Banerjee S, Ahmad A, Azmi AS, et al. Acquisition of epithelial-mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the notch signaling pathway. Cancer Res 2009;69:2400-7.
48. Maillard I, Weng AP, Carpenter AC, Rodriguez CG, Sai H, Xu L, et al. Mastermind critically regulates Notch-mediated lymphoid cell fate decisions. Blood 2004;104:1696-702. (Pubitemid 39202276)
49. Sullivan JP, Spinola M, Dodge M, Raso MG, Behrens C, Gao B, et al. Aldehyde dehydrogenase activity selects for lung adenocarcinoma stem cells dependent on notch signaling. Cancer Res 2010;70: 9937-48.
50. Pierfelice TJ, Schreck KC, Dang L, Asnaghi L, Gaiano N, Eberhart CG. Notch3 activation promotes invasive glioma formation in a tissue site-specific manner. Cancer Res 2011;71:1115-25.