Epigenetic regulation of SOX9 by the NF-κB signaling pathway in pancreatic cancer stem cells

Stem Cells

Volumn 31, Issue 8, 2013, Pages 1454-1466

  Sun, Lei ^a   Mathews, Lesley A ^a,b   Cabarcas, Stephanie M ^a,c   Zhang, Xiaohu ^b,d   Yang, Acong ^e   Zhang, Ying ^e   Young, Matthew R ^f   Klarmann, Kimberly D ^d   Keller, Jonathan R ^d   Farrar, William L ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c GANNON UNIVERSITY   (United States)

^d SAIC FREDERICK INC   (United States)

^e INSTITUTE OF CHINESE MATERIA MEDICA   (China)

^f NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Cancer stem cells; Epigenetic regulation; Invasion; NF B signaling; Pancreatic cancer; SOX9

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR SOX9;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CANCER STEM CELL; CELL INVASION; CELL POPULATION; CONTROLLED STUDY; CPG ISLAND; DEMETHYLATION; DNA METHYLATION; EPIGENETICS; GENE IDENTIFICATION; GENETIC REGULATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PANCREAS CANCER; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

CANCER STEM CELLS; EPIGENETIC REGULATION; INVASION; NF-ΚB SIGNALING; PANCREATIC CANCER; SOX9;

ANIMALS; CELL LINE, TUMOR; DNA METHYLATION; EPIGENOMICS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGRAFTS; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM INVASIVENESS; NF-KAPPA B; PANCREATIC NEOPLASMS; SIGNAL TRANSDUCTION; SOX9 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELA;

EID: 84883410708     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1394     Document Type: Article

References (71)

1. Smith BD, Smith GL, Hurria A et al. Future of cancer incidence in the United States: Burdens upon an aging, changing nation. J Clin Oncol 2009;27:2758-2765.
2. Jemal A, Siegel R, Ward E et al. Cancer statistics, 2009. CA Cancer J Clin 2009;59:225-249.
3. Lonardo E, Hermann PC, Heeschen C. Pancreatic cancer stem cells - Update and future perspectives. Mol Oncol 2010;4:431-442.
4. Senderowicz AM, Johnson JR, Sridhara R et al. Erlotinib/gemcitabine for first-line treatment of locally advanced or metastatic adenocarcinoma of the pancreas. Oncology (Williston Park) 2007;21:1696-1706; discussion 1706-1699, 1712, 1715.
5. Duffy A, Kortmansky J, Schwartz GK et al. A phase I study of erlotinib in combination with gemcitabine and radiation in locally advanced, non-operable pancreatic adenocarcinoma. Ann Oncol 2008; 19:86-91.
6. Conroy T, Desseigne F, Ychou M et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med 2011;364: 1817-1825.
7. Klarmann GJ, Hurt EM, Mathews LA et al. Invasive prostate cancer cells are tumor initiating cells that have a stem cell-like genomic signature. Clin Exp Metastasis 2009;26:433-446.
8. Mani SA, Guo W, Liao MJ et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008;133: 704-715.
9. Huber MA, Kraut N, Beug H. Molecular requirements for epithelialmesenchymal transition during tumor progression. Curr Opin Cell Biol 2005;17:548-558.
10. Al-Hajj M, Wicha MS, Benito-Hernandez A et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003;100:3983-3988.
11. Prince ME, Sivanandan R, Kaczorowski A et al. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci USA 2007;104: 973-978.
12. Singh SK, Hawkins C, Clarke ID et al. Identification of human brain tumour initiating cells. Nature 2004;432:396-401.
13. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: Accumulating evidence and unresolved questions. Nat Rev Cancer 2008;8: 755-768.
14. Beier D, Hau P, Proescholdt M et al. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res 2007;67:4010-4015.
15. Wright MH, Calcagno AM, Salcido CD et al. Brca1 breast tumors contain distinct CD44+/CD24- and CD133+ cells with cancer stem cell characteristics. Breast Cancer Res 2008;10:R10.
16. Lee JM, Dedhar S, Kalluri R et al. The epithelial-mesenchymal transition: New insights in signaling, development, and disease. J Cell Biol 2006;172:973-981.
17. Li C, Heidt DG, Dalerba P et al. Identification of pancreatic cancer stem cells. Cancer Res 2007;67:1030-1037.
18. Sarkar FH, Li Y, Wang Z et al. Pancreatic cancer stem cells and EMT in drug resistance and metastasis. Minerva Chir 2009;64: 489-500.
19. Nakajima S, Doi R, Toyoda E et al. N-cadherin expression and epithelial-mesenchymal transition in pancreatic carcinoma. Clin Cancer Res 2004;10:4125-4133.
20. Hermann PC, Huber SL, Herrler T et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007;1:313-323.
21. Li C, Wu JJ, Hynes M et al. c-Met is a marker of pancreatic cancer stem cells and therapeutic target. Gastroenterology 2011;141: 2218-2227. e2215.
22. Mathews LA, Cabarcas SM, Hurt EM et al. Increased expression of DNA repair genes in invasive human pancreatic cancer cells. Pancreas 2011;40:730-739.
23. Ketolainen JM, Alarmo EL, Tuominen VJ et al. Parallel inhibition of cell growth and induction of cell migration and invasion in breast cancer cells by bone morphogenetic protein 4. Breast Cancer Res Treat 2010;124:377-386.
24. Belaguli NS, Aftab M, Rigi M et al. GATA6 promotes colon cancer cell invasion by regulating urokinase plasminogen activator gene expression. Neoplasia 2010;12:856-865.
25. Wang H, Leav I, Ibaragi S et al. SOX9 is expressed in human fetal prostate epithelium and enhances prostate cancer invasion. Cancer Res 2008;68:1625-1630.
26. Jaffee EM, Schutte M, Gossett J et al. Development and characterization of a cytokine-secreting pancreatic adenocarcinoma vaccine from primary tumors for use in clinical trials. Cancer J Sci Am 1998;4: 194-203.
27. Jaffee EM, Hruban RH, Biedrzycki B et al. Novel allogeneic granulocyte-macrophage colony-stimulating factor-secreting tumor vaccine for pancreatic cancer: A phase I trial of safety and immune activation. J Clin Oncol 2001;19:145-156.
28. Tomayko MM, Reynolds CP. Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother Pharmacol 1989;24: 148-154.
29. Sato N, Meijer L, Skaltsounis L et al. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 2004;10:55-63.
30. Pebay A, Wong RC, Pitson SM et al. Essential roles of sphingosine-1-phosphate and platelet-derived growth factor in the maintenance of human embryonic stem cells. Stem Cells 2005;23:1541-1548.
31. Inniss K, Moore H. Mediation of apoptosis and proliferation of human embryonic stem cells by sphingosine-1-phosphate. Stem Cells Dev 2006;15:789-796.
32. Perkins ND. The diverse and complex roles of NF-kappaB subunits in cancer. Nat Rev Cancer 2012;12:121-132.
33. Karin M, Ben-Neriah Y. Phosphorylation meets ubiquitination: The control of NF-[lsqb]kappa[rsqb]B activity. Annu Rev Immunol 2000; 18:621-663.
34. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: An emerging axis of evil in the war on cancer. Oncogene 2010;29: 4741-4751.
35. Gupta PB, Chaffer CL, Weinberg RA. Cancer stem cells: Mirage or reality? Nat Med 2009;15:1010-1012.
36. Brabletz T, Jung A, Spaderna S et al. Opinion: Migrating cancer stem cells - An integrated concept of malignant tumour progression. Nat Rev Cancer 2005;5:744-749.
37. Kucia M, Reca R, Miekus K et al. Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: Pivotal role of the SDF-1-CXCR4 axis. Stem Cells 2005;23:879-894.
38. Son BR, Marquez-Curtis LA, Kucia M et al. Migration of bone marrow and cord blood mesenchymal stem cells in vitro is regulated by stromal-derived factor-1-CXCR4 and hepatocyte growth factor-c-met axes and involves matrix metalloproteinases. Stem Cells 2006;24: 1254-1264.
39. Muller A, Homey B, Soto H et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001;410:50-56.
40. Vande Woude GF, Jeffers M, Cortner J et al. Met-HGF/SF: Tumorigenesis, invasion and metastasis. Ciba Found Symp 1997;212: 119-130; discussion 130-112, 148-154.
41. Shin HM, Kim MH, Kim BH et al. Inhibitory action of novel aromatic diamine compound on lipopolysaccharide-induced nuclear translocation of NF-kappaB without affecting IkappaB degradation. FEBS Lett 2004;571:50-54.
42. Lee HY, Park KS, Kim MK et al. A small compound that inhibits tumor necrosis factor-alpha-induced matrix metalloproteinase-9 upregulation. Biochem Biophys Res Commun 2005;336:716-722.
43. Friedl P, Wolf K. Tumour-cell invasion and migration: Diversity and escape mechanisms. Nat Rev Cancer 2003;3:362-374.
44. Entschladen F, Drell TL, Lang K et al. Tumour-cell migration, invasion, and metastasis: Navigation by neurotransmitters. Lancet Oncol 2004;5:254-258.
45. Gou S, Liu T, Wang C et al. Establishment of clonal colony-forming assay for propagation of pancreatic cancer cells with stem cell properties. Pancreas 2007;34:429-435.
46. Wang H, McKnight NC, Zhang T et al. SOX9 is expressed in normal prostate basal cells and regulates androgen receptor expression in prostate cancer cells. Cancer Res 2007;67:528-536.
47. De Santa Barbara P, Bonneaud N, Boizet B et al. Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Mullerian hormone gene. Mol Cell Biol 1998;18:6653-6665.
48. Guo W, Keckesova Z, Donaher JL et al. Slug and sox9 cooperatively determine the mammary stem cell state. Cell 2012;148:1015-1028.
49. Shah AN, Summy JM, Zhang J et al. Development and characterization of gemcitabine-resistant pancreatic tumor cells. Ann Surg Oncol 2007;14:3629-3637.
50. Jimeno A, Feldmann G, Suarez-Gauthier A et al. A direct pancreatic cancer xenograft model as a platform for cancer stem cell therapeutic development. Mol Cancer Ther 2009;8:310-314.
51. Christman JK. 5-Azacytidine and 5-aza-20-deoxycytidine as inhibitors of DNA methylation: Mechanistic studies and their implications for cancer therapy. Oncogene 2002;21:5483-5495.
52. Zhou L, Cheng X, Connolly BA et al. Zebularine: A novel DNA methylation inhibitor that forms a covalent complex with DNA methyltransferases. J Mol Biol 2002;321:591-599.
53. Rayet B, Gelinas C. Aberrant rel/nfkb genes and activity in human cancer. Oncogene 1999;18:6938-6947.
54. Dolcet X, Llobet D, Pallares J et al. NF-kB in development and progression of human cancer. Virchows Arch 2005;446:475-482.
55. Rajasekhar VK, Studer L, Gerald W et al. Tumour-initiating stem-like cells in human prostate cancer exhibit increased NF-kappaB signalling. Nat Commun 2011;2:162.
56. Wang Z, Banerjee S, Li Y et al. Down-regulation of notch-1 inhibits invasion by inactivation of nuclear factor-kappaB, vascular endothelial growth factor, and matrix metalloproteinase-9 in pancreatic cancer cells. Cancer Res 2006;66:2778-2784.
57. Arlt A, Vorndamm J, Breitenbroich M et al. Inhibition of NF-kappaB sensitizes human pancreatic carcinoma cells to apoptosis induced by etoposide (VP16) or doxorubicin. Oncogene 2001;20:859-868.
58. Arlt A, Gehrz A, Muerkoster S et al. Role of NF-kappaB and Akt/PI3K in the resistance of pancreatic carcinoma cell lines against gemcitabine-induced cell death. Oncogene 2003;22:3243-3251.
59. Nakanishi C, Toi M. Nuclear factor-kappaB inhibitors as sensitizers to anticancer drugs. Nat Rev Cancer 2005;5:297-309.
60. Sakai D, Suzuki T, Osumi N et al. Cooperative action of Sox9, Snail2 and PKA signaling in early neural crest development. Development 2006;133:1323-1333.
61. Wegner M, Stolt CC. From stem cells to neurons and glia: A Soxist's view of neural development. Trends Neurosci 2005;28:583-588.
62. Stolt CC, Lommes P, Sock E et al. The Sox9 transcription factor determines glial fate choice in the developing spinal cord. Genes Dev 2003;17:1677-1689.
63. Blache P, van de Wetering M, Duluc I et al. SOX9 is an intestine crypt transcription factor, is regulated by the Wnt pathway, and represses the CDX2 and MUC2 genes. J Cell Biol 2004;166:37-47.
64. Shaked H, Hofseth LJ, Chumanevich A et al. Chronic epithelial NFkappaB activation accelerates APC loss and intestinal tumor initiation through iNOS up-regulation. Proc Natl Acad Sci USA 2012;109: 14007-14012.
65. Vidal VP, Chaboissier MC, Lutzkendorf S et al. Sox9 is essential for outer root sheath differentiation and the formation of the hair stem cell compartment. Curr Biol 2005;15:1340-1351.
66. Matheu A, Collado M, Wise C et al. Oncogenicity of the developmental transcription factor Sox9. Cancer Res 2012;72:1301-1315.
67. Sun L, Cabarcas SM, Farrar WL. Radioresistance and cancer stem cells: Survival of the fittest. J Carcinog Mutagen 2011;S1:004. doi: 10.4172/2157-2518.S1-004.
68. Saito Y, Liang G, Egger G et al. Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatinmodifying drugs in human cancer cells. Cancer Cell 2006;9:435-443.
69. Bender CM, Pao MM, Jones PA. Inhibition of DNA methylation by 5-aza-20-deoxycytidine suppresses the growth of human tumor cell lines. Cancer Res 1998;58:95-101.
70. Cheng JC, Yoo CB, Weisenberger DJ et al. Preferential response of cancer cells to zebularine. Cancer Cell 2004;6:151-158.
71. Stresemann C, Brueckner B, Musch T et al. Functional diversity of DNA methyltransferase inhibitors in human cancer cell lines. Cancer Res 2006;66:2794-2800.