Unlike Pancreatic Cancer Cells Pancreatic Cancer Associated Fibroblasts Display Minimal Gene Induction after 5-Aza-2′-Deoxycytidine

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Yu, Jun ^a   Walter, Kimberly ^a   Omura, Noriyuki ^a   Hong, Seung Mo ^a   Young, Angela ^a   Li, Ang ^a   Vincent, Audrey ^a   Goggins, Michael ^a  

^a DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; DISINTEGRIN; METALLOPROTEINASE;

ADAM12 GENE; ADULT; ARTICLE; CANCER CELL CULTURE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISINTEGRIN GENE; DNA METHYLATION; DNA SEQUENCE; FEMALE; FIBROBLAST; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC ANALYSIS; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; METALLOPROTEASE GENE; NUCLEOTIDE SEQUENCE; ONCOGENE; OUTCOME ASSESSMENT; PANCREAS CANCER; SEQUENCE ANALYSIS; UPREGULATION;

ADAM PROTEINS; AZACITIDINE; BASE SEQUENCE; BLOTTING, WESTERN; CELL LINE, TUMOR; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; FEMALE; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, NEOPLASM; GENETIC ASSOCIATION STUDIES; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE PROTEINS; MIDDLE AGED; MOLECULAR SEQUENCE DATA; PANCREATIC NEOPLASMS; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA; UP-REGULATION;

EID: 84866306531     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043456     Document Type: Article

References (72)

1. Ting AH, McGarvey KM, Baylin SB, (2006) The cancer epigenome-components and functional correlates. Genes Dev 20: 3215-3231.
2. Esteller M, (2007) Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet 8: 286-298.
3. Omura N, Goggins M, (2009) Epigenetics and epigenetic alterations in pancreatic cancer. Int J Clin Exp Pathol 2: 310-326 Epub 2008 Nov 2015.
4. Vincent A, Omura N, Hong SM, Jaffe A, Eshleman J, et al. (2011) Genome-Wide Analysis of Promoter Methylation Associated with Gene Expression Profile in Pancreatic Adenocarcinoma. Clin Cancer Res 17: 4341-4354.
5. Maegawa S, Hinkal G, Kim HS, Shen L, Zhang L, et al. (2010) Widespread and tissue specific age-related DNA methylation changes in mice. Genome Res 20: 332-340.
6. Matsubayashi H, Sato N, Brune K, Blackford AL, Hruban RH, et al. (2005) Age- and disease-related methylation of multiple genes in nonneoplastic duodenum and in duodenal juice. Clin Cancer Res 11: 573-583.
7. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, et al. (2005) Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A 102: 10604-10609.
8. Jin B, Yao B, Li JL, Fields CR, Delmas AL, et al. (2009) DNMT1 and DNMT3B modulate distinct polycomb-mediated histone modifications in colon cancer. Cancer Res 69: 7412-7421.
9. Jones PA, Liang G, (2009) Rethinking how DNA methylation patterns are maintained. Nat Rev Genet 10: 805-811.
10. Issa JP, Ahuja N, Toyota M, Bronner MP, Brentnall TA, (2001) Accelerated age-related CpG island methylation in ulcerative colitis. Cancer Res 61: 3573-3577.
11. Vincent A, Herman JM, Schulick R, Hruban R, Goggins M, (2011) Pancreatic Cancer. Lancet 378: 607-620.
12. Boyd ZS, Raja R, Johnson S, Eberhard DA, Lackner MR, (2009) A tumor sorting protocol that enables enrichment of pancreatic adenocarcinoma cells and facilitation of genetic analyses. J Mol Diagn 11: 290-297.
13. Hwang RF, Moore T, Arumugam T, Ramachandran V, Amos KD, et al. (2008) Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res 68: 918-926.
14. Chang HY, Sneddon JB, Alizadeh AA, Sood R, West RB, et al. (2004) Gene expression signature of fibroblast serum response predicts human cancer progression: similarities between tumors and wounds. PLoS Biol 2: E7.
15. Cohen SJ, Alpaugh RK, Palazzo I, Meropol NJ, Rogatko A, et al. (2008) Fibroblast activation protein and its relationship to clinical outcome in pancreatic adenocarcinoma. Pancreas 37: 154-158.
16. Finak G, Bertos N, Pepin F, Sadekova S, Souleimanova M, et al. (2008) Stromal gene expression predicts clinical outcome in breast cancer. Nat Med 14: 518-527.
17. Iacobuzio-Donahue CA, Argani P, Hempen PM, Jones J, Kern SE, (2002) The desmoplastic response to infiltrating breast carcinoma: gene expression at the site of primary invasion and implications for comparisons between tumor types. Cancer Res 62: 5351-5357.
18. Ohuchida K, Mizumoto K, Murakami M, Qian LW, Sato N, et al. (2004) Radiation to stromal fibroblasts increases invasiveness of pancreatic cancer cells through tumor-stromal interactions. Cancer Res 64: 3215-3222.
19. Kalluri R, Zeisberg M, (2006) Fibroblasts in cancer. Nat Rev Cancer 6: 392-401.
20. Fujita H, Ohuchida K, Mizumoto K, Nakata K, Yu J, et al. (2010) alpha-Smooth Muscle Actin Expressing Stroma Promotes an Aggressive Tumor Biology in Pancreatic Ductal Adenocarcinoma. Pancreas.
21. Eyden B, (2008) The myofibroblast: phenotypic characterization as a prerequisite to understanding its functions in translational medicine. J Cell Mol Med 12: 22-37.
22. Bhowmick NA, Chytil A, Plieth D, Gorska AE, Dumont N, et al. (2004) TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 303: 848-851.
23. Pietras K, Pahler J, Bergers G, Hanahan D, (2008) Functions of paracrine PDGF signaling in the proangiogenic tumor stroma revealed by pharmacological targeting. PLoS Med 5: e19.
24. Ellis LM, Hicklin DJ, (2008) VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat Rev Cancer 8: 579-591.
25. Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, et al. (2009) Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 324: 1457-1461.
26. Tian H, Callahan CA, DuPree KJ, Darbonne WC, Ahn CP, et al. (2009) Hedgehog signaling is restricted to the stromal compartment during pancreatic carcinogenesis. Proc Natl Acad Sci U S A 106: 4254-4259.
27. Walter K, Omura N, Hong SM, Griffith M, Vincent A, et al. (2010) Overexpression of smoothened activates the sonic hedgehog signaling pathway in pancreatic cancer-associated fibroblasts. Clin Cancer Res 16: 1781-1789 Epub 2010 Mar 1789.
28. Yauch RL, Gould SE, Scales SJ, Tang T, Tian H, et al. (2008) A paracrine requirement for hedgehog signalling in cancer. Nature 455: 406-410.
29. Infante JR, Matsubayashi H, Sato N, Tonascia J, Klein AP, et al. (2007) Peritumoral fibroblast SPARC expression and patient outcome with resectable pancreatic adenocarcinoma. J Clin Oncol 25: 319-325.
30. Sato N, Fukushima N, Maehara N, Matsubayashi H, Koopmann J, et al. (2003) SPARC/osteonectin is a frequent target for aberrant methylation in pancreatic adenocarcinoma and a mediator of tumor-stromal interactions. Oncogene 22: 5021-5030.
31. Bhowmick NA, Neilson EG, Moses HL, (2004) Stromal fibroblasts in cancer initiation and progression. Nature 432: 332-337.
32. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, et al. (2005) Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121: 335-348.
33. Allinen M, Beroukhim R, Cai L, Brennan C, Lahti-Domenici J, et al. (2004) Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 6: 17-32.
34. Campbell I, Polyak K, Haviv I, (2009) Clonal mutations in the cancer-associated fibroblasts: the case against genetic coevolution. Cancer Res 69: 6765-6768; discussion 6769.
35. Hu M, Yao J, Cai L, Bachman KE, van den Brule F, et al. (2005) Distinct epigenetic changes in the stromal cells of breast cancers. Nat Genet 37: 899-905 Epub 2005 Jul 2010.
36. Jiang L, Gonda TA, Gamble MV, Salas M, Seshan V, et al. (2008) Global hypomethylation of genomic DNA in cancer-associated myofibroblasts. Cancer Res 68: 9900-9908.
37. Qiu W, Hu M, Sridhar A, Opeskin K, Fox S, et al. (2008) No evidence of clonal somatic genetic alterations in cancer-associated fibroblasts from human breast and ovarian carcinomas. Nat Genet 40: 650-655.
38. Walter K, Omura N, Hong SM, Griffith M, Goggins M, (2008) Pancreatic cancer associated fibroblasts display normal allelotypes. Cancer Biol Ther 7: 882-888.
39. Sato N, Fukushima N, Maitra A, Iacobuzio-Donahue CA, van Heek NT, et al. (2004) Gene expression profiling identifies genes associated with invasive intraductal papillary mucinous neoplasms of the pancreas. Am J Pathol 164: 903-914.
40. Direkze NC, Hodivala-Dilke K, Jeffery R, Hunt T, Poulsom R, et al. (2004) Bone marrow contribution to tumor-associated myofibroblasts and fibroblasts. Cancer Res 64: 8492-8495.
41. Mishra PJ, Humeniuk R, Medina DJ, Alexe G, Mesirov JP, et al. (2008) Carcinoma-associated fibroblast-like differentiation of human mesenchymal stem cells. Cancer Res 68: 4331-4339.
42. Zeisberg EM, Potenta S, Xie L, Zeisberg M, Kalluri R, (2007) Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts. Cancer Res 67: 10123-10128.
43. Mann J, Chu DC, Maxwell A, Oakley F, Zhu NL, et al. (2010) MeCP2 controls an epigenetic pathway that promotes myofibroblast transdifferentiation and fibrosis. Gastroenterology 138: 705-714, 714 e701-704.
44. Hanson JA, Gillespie JW, Grover A, Tangrea MA, Chuaqui RF, et al. (2006) Gene promoter methylation in prostate tumor-associated stromal cells. J Natl Cancer Inst 98: 255-261.
45. Liang G, Gonzales FA, Jones PA, Orntoft TF, Thykjaer T, (2002) Analysis of gene induction in human fibroblasts and bladder cancer cells exposed to the methylation inhibitor 5-aza-2′-deoxycytidine. Cancer Res 62: 961-966.
46. Lee KM, Nguyen C, Ulrich AB, Pour PM, Ouellette MM, (2003) Immortalization with telomerase of the Nestin-positive cells of the human pancreas. Biochem Biophys Res Commun 301: 1038-1044.
47. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, et al. (2008) Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 321: 1801-1806 Epub 2008 Sep 1804.
48. Yu J, Li A, Hong SM, Hruban RH, Goggins M, (2012) MicroRNA alterations of pancreatic intraepithelial neoplasias. Clin Cancer Res 18: 981-992.
49. Kelloff GJ, Sullivan DC, Baker H, Clarke LP, Nordstrom R, et al. (2007) Workshop on imaging science development for cancer prevention and preemption. Cancer Biomark 3: 1-33.
50. Yu J, Ohuchida K, Mizumoto K, Sato N, Kayashima T, et al. (2010) MicroRNA, hsa-miR-200c, is an independent prognostic factor in pancreatic cancer and its upregulation inhibits pancreatic cancer invasion but increases cell proliferation. Mol Cancer 9: 169.
51. Omura N, Li CP, Li A, Hong SM, Walter K, et al. (2008) Genome-wide profiling of methylated promoters in pancreatic adenocarcinoma. Cancer Biol Ther 7: 1146-1156.
52. Ferguson AT, Evron E, Umbricht CB, Pandita TK, Chan TA, et al. (2000) High frequency of hypermethylation at the 14-3-3 sigma locus leads to gene silencing in breast cancer. Proc Natl Acad Sci U S A 97: 6049-6054.
53. Sun W, Liu Y, Glazer CA, Shao C, Bhan S, et al. (2010) TKTL1 is activated by promoter hypomethylation and contributes to head and neck squamous cell carcinoma carcinogenesis through increased aerobic glycolysis and HIF1alpha stabilization. Clin Cancer Res 16: 857-866.
54. Lau JC, Hanel ML, Wevrick R, (2004) Tissue-specific and imprinted epigenetic modifications of the human NDN gene. Nucleic Acids Res 32: 3376-3382.
55. Kanda M, Nomoto S, Okamura Y, Nishikawa Y, Sugimoto H, et al. (2009) Detection of metallothionein 1G as a methylated tumor suppressor gene in human hepatocellular carcinoma using a novel method of double combination array analysis. Int J Oncol 35: 477-483.
56. Iba K, Albrechtsen R, Gilpin BJ, Loechel F, Wewer UM, (1999) Cysteine-rich domain of human ADAM 12 (meltrin alpha) supports tumor cell adhesion. Am J Pathol 154: 1489-1501.
57. Sato N, Fukushima N, Maitra A, Matsubayashi H, Yeo CJ, et al. (2003) Discovery of novel targets for aberrant methylation in pancreatic carcinoma using high-throughput microarrays. Cancer Res 63: 3735-3742.
58. Di Croce L, Raker VA, Corsaro M, Fazi F, Fanelli M, et al. (2002) Methyltransferase recruitment and DNA hypermethylation of target promoters by an oncogenic transcription factor. Science 295: 1079-1082.
59. Fukushima N, Sato N, Ueki T, Rosty C, Walter KM, et al. (2002) Aberrant methylation of preproenkephalin and p16 genes in pancreatic intraepithelial neoplasia and pancreatic ductal adenocarcinoma. Am J Pathol 160: 1573-1581.
60. Sato N, Fukushima N, Chang R, Matsubayashi H, Goggins M, (2006) Differential and epigenetic gene expression profiling identifies frequent disruption of the RELN pathway in pancreatic cancers. Gastroenterology 130: 548-565.
61. Sato N, Matsubayashi H, Abe T, Fukushima N, Goggins M, (2005) Epigenetic down-regulation of CDKN1C/p57KIP2 in pancreatic ductal neoplasms identified by gene expression profiling. Clin Cancer Res 11: 4681-4688.
62. Sato N, Parker AR, Fukushima N, Miyagi Y, Iacobuzio-Donahue CA, et al. (2005) Epigenetic inactivation of TFPI-2 as a common mechanism associated with growth and invasion of pancreatic ductal adenocarcinoma. Oncogene 24: 850-858.
63. Menigatti M, Truninger K, Gebbers JO, Marbet U, Marra G, et al. (2009) Normal colorectal mucosa exhibits sex- and segment-specific susceptibility to DNA methylation at the hMLH1 and MGMT promoters. Oncogene 28: 899-909.
64. Dahl JA, Collas P, (2007) Q2ChIP, a quick and quantitative chromatin immunoprecipitation assay, unravels epigenetic dynamics of developmentally regulated genes in human carcinoma cells. Stem Cells 25: 1037-1046.
65. Freberg CT, Dahl JA, Timoskainen S, Collas P, (2007) Epigenetic reprogramming of OCT4 and NANOG regulatory regions by embryonal carcinoma cell extract. Mol Biol Cell 18: 1543-1553.
66. Kveiborg M, Albrechtsen R, Couchman JR, Wewer UM, (2008) Cellular roles of ADAM12 in health and disease. Int J Biochem Cell Biol 40: 1685-1702.
67. Frohlich C, Albrechtsen R, Dyrskjot L, Rudkjaer L, Orntoft TF, et al. (2006) Molecular profiling of ADAM12 in human bladder cancer. Clin Cancer Res 12: 7359-7368.
68. Sato N, Maitra A, Fukushima N, van Heek NT, Matsubayashi H, et al. (2003) Frequent hypomethylation of multiple genes overexpressed in pancreatic ductal adenocarcinoma. Cancer Res 63: 4158-4166.
69. Laurent L, Wong E, Li G, Huynh T, Tsirigos A, et al. (2010) Dynamic changes in the human methylome during differentiation. Genome Res 20: 320-331.
70. Kim ST, Fields PE, Flavell RA, (2007) Demethylation of a specific hypersensitive site in the Th2 locus control region. Proc Natl Acad Sci U S A 104: 17052-17057.
71. Zhu JK, (2009) Active DNA demethylation mediated by DNA glycosylases. Annu Rev Genet 43: 143-166.
72. Bender CM, Pao MM, Jones PA, (1998) Inhibition of DNA methylation by 5-aza-2′-deoxycytidine suppresses the growth of human tumor cell lines. Cancer Res 58: 95-101.