Extracellular DNA in pancreatic cancer promotes cell invasion and metastasis

Cancer Research

Volumn 73, Issue 14, 2013, Pages 4256-4266

  Wen, Fushi ^a   Shen, Alex ^a   Choi, Andrew ^a   Gerner, Eugene W ^b   Shi, Jiaqi ^c  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE I; DNA; EXTRACELLULAR DNA; INTERLEUKIN 8; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CARCINOGENESIS; CELL ADHESION; CELL INVASION; CELL MIGRATION; CELL SURFACE; CONTROLLED STUDY; DNA DEGRADATION; DNA SYNTHESIS; EXTRACELLULAR MATRIX; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; IN VIVO STUDY; METASTASIS; MOUSE; NONHUMAN; PANCREAS CANCER; PANCREAS CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; DEOXYRIBONUCLEASE I; DNA, NEOPLASM; HUMANS; INTERLEUKIN-8; MICE; MICE, SCID; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PANCREATIC NEOPLASMS;

EID: 84880869520     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-3287     Document Type: Article

References (50)

1. Raimondi S, Maisonneuve P, Lowenfels AB. Epidemiology of pancreatic cancer: an overview. Nat Rev Gastroenterol Hepatol 2009; 6:699-708.
2. Barkin JS, Goldstein JA. Diagnostic and therapeutic approach to pancreatic cancer. Biomed Pharmacother 2000;54:400-9.
3. Tuveson DA, Neoptolemos JP. Understanding metastasis in pancreatic cancer: a call for new clinical approaches. Cell 2012;148: 21-3.
4. Kopfstein L, Christofori G. Metastasis: cell-autonomous mechanisms versus contributions by the tumor microenvironment. Cell Mol Life Sci 2006;63:449-68.
5. Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 2004;4:71-8.
6. Mantovani A. CANCER Inflaming metastasis. Nature 2009;457:36-7.
7. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008;454:436-44.
8. Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 2009;30:1073-81.
9. Uomo I, Miraglia S, Pastorello M. Inflammation and pancreatic ductal adenocarcinoma: a potential scenario for novel drug targets. J Pancreas 2010;11:199-202.
10. Farrow B, Evers BM. Inflammation and the development of pancreatic cancer. Surg Oncol 2002;10:153-69.
11. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002;420: 860-7.
12. Karlson BM, Ekbom A, Josefsson S, McLaughlin JK, Fraumeni JF, Nyren O. The risk of pancreatic cancer following pancreatitis: an association due to confounding? Gastroenterology 1997;113:587-92.
13. Ekbom A, McLaughlin JK, Nyren O. Pancreatitis and the risk of pancreatic-cancer. N Engl J Med 1993;329:1502.
14. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303:1532-5.
15. Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD Jr, et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci U S A 2010;107:15880-5.
16. Kessenbrock K, Krumbholz M, Schonermarck U, Back W, Gross WL, Werb Z, et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med 2009;15:623-5.
17. Bass JIF, Russo DM, Gabelloni ML, Geffner JR, Giordano M, Catalano M, et al. Extracellular DNA: a major proinflammatory component of pseudomonas aeruginosa biofilms. J Immunol 2010;184:6386-95.
18. Amulic B, Cazalet C, Hayes GL, Metzler KD, Zychlinsky A. Neutrophil function: from mechanisms to disease. Annu Rev Immunol 2012;30: 459-89.
19. Demers M, Krause DS, Schatzberg D, Martinod K, Voorhees JR, Fuchs TA, et al. Cancers predispose neutrophils to release extracellular DNA traps that contribute to cancer-associated thrombosis. Proc Natl Acad Sci U S A 2012;109:13076-81.
20. Esposito I, Menicagli M, Funel N, Bergmann F, Boggi U, Mosca F, et al. Inflammatory cells contribute to the generation of an angiogenic phenotype in pancreatic ductal adenocarcinoma. J Clin Pathol 2004;57:630-6.
21. Erkan M, Reiser-Erkan C, Michalski CW, Kleeff J. Tumor microenvironment and progression of pancreatic cancer. Exp Oncol 2010;32: 128-31.
22. Waugh DJJ, Wilson C. The interleukin-8 pathway in cancer. Clin Cancer Res 2008;14:6735-41.
23. Matsuo Y, Sawai H, Funahashi H, Takahashi H, Sakamoto M, Yamamoto M, et al. Enhanced angiogenesis due to inflammatory cytokines from pancreatic cancer cell lines and relation to metastatic potential. Pancreas 2004;28:344-52.
24. Liu N, Furukawa T, Kobari M, Tsao MS. Comparative phenotypic studies of duct epithelial cell lines derived from normal human pancreas and pancreatic carcinoma. Am J Pathol 1998;153:263-9.
25. Sylvester P. Optimization of the tetrazolium dye (MTT) colorimetric assay for cellular growth and viability. Methods Mol Biol 2011;716: 157-68.
26. Wen F, Zhou R, Shen A, Choi A, Uribe D, Shi J. The tumor suppressive role of eIF3f and its function in translation inhibition and rRNA degradation. PLoS ONE 2012;7:e34194.
27. Jiang J, Liu W, Guo X, Zhang R, Zhi Q, Ji J, et al. IRX1 influences peritoneal spreading and metastasis via inhibiting BDKRB2-dependent neovascularization on gastric cancer. Oncogene 2011;30: 4498-508.
28. Deer EL, Gonzalez-Hernandez J, Coursen JD, Shea JE, Ngatia J, Scaife CL, et al. Phenotype and genotype of pancreatic cancer cell lines. Pancreas 2010;39:425-35.
29. Sugihara S, Yamamoto T, Tanaka H, Kambara T, Hiraoka T, Miyauchi Y. Deoxyribonuclease treatment prevents blood-borne liver metastasis of cutaneously transplanted tumor-cells in mice. Br J Cancer 1993;67:66-70.
30. Hughes CS, Postovit LM, Lajoie GA. Matrigel: a complex protein mixture required for optimal growth of cell culture. Proteomics 2010;10:1886-90.
31. Delamirande G. Action of deoxyribonuclease and ribonuclease on growth of Ehrlich ascites carcinoma in mice. Nature 1961;192:52-4.
32. Salganik RI, Martynova RP, Matienko NA, Ronichevskaya GM. Effect of deoxyribonuclease on the course of lymphatic leukaemia in AKR mice. Nature 1967;214:100-2.
33. Patutina O, Mironova N, Ryabchikova E, Popova N, Nikolin V, Kaledin V, et al. Inhibition of metastasis development by daily administration of ultralow doses of RNase A and DNase I. Biochimie 2011;93:689-96.
34. Wen FS, White GJ, Van Etten HD, Xiong ZG, Hawes MC. Extracellular DNA is required for root tip resistance to fungal infection. Plant Physiol 2009;151:820-9.
35. Swarup V, Rajeswari MR. Circulating (cell-free) nucleic acids-a promising, non-invasive tool for early detection of several human diseases. Febs Lett 2007;581:795-9.
36. Shimizu N. Molecular mechanisms of the origin of micronuclei from extrachromosomal elements. Mutagenesis 2011;26:119-23.
37. Pisetsky DS, Gauley J, Ullal AJ. Microparticles as a source of extracellular DNA. Immunol Res 2011;49:227-34.
38. Chang P, Li YN, Li DH. Micronuclei levels in peripheral blood lymphocytes as a potential biomarker for pancreatic cancer risk. Carcinogenesis 2011;32:210-5.
39. Aggarwal SK, Wagner RW, McAllister PK, Rosenberg B. Cell- surfaceassociated nucleic-acid in tumorigenic cells made visible with platinum- pyrimidine complexes by electron-microscopy. Proc Natl Acad Sci U S A 1975;72:928-32.
40. Juckett DA, Rosenberg B. Actions of cis-diamminedichloroplatinum on cell-surface nucleic-acids in cancer-cells as determined by cell electrophoresis techniques. Cancer Res 1982;42:3565-73.
41. Russell JL, Golub ES. Leukemia in AKR mice-defined suppressor cell-population expressing membrane-associated DNA. Proc Natl Acad Sci U S A 1978;75:6211-4.
42. Matsuo Y, Ochi N, Sawai H, Yasuda A, Takahashi H, Funahashi H, et al. CXCL8/IL-8 and CXCL12/SDF-1 alpha co-operatively promote invasiveness and angiogenesis in pancreatic cancer. Int J Cancer 2009;124:853-61.
43. Tian J, Avalos AM, Mao SY, Chen B, Senthil K, Wu H, et al. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 2007;8: 487-96.
44. Matsuo Y, Campbell PM, Brekken RA, Sung B, Ouellette MM, Fleming JB, et al. K-Ras promotes angiogenesis mediated by immortalized human pancreatic epithelial cells through mitogen-activated protein kinase signaling pathways. Mol Cancer Res 2009;7:799-808.
45. Rial NS, Lazennec G, Prasad AR, Krouse RS, Lance P, Gerner EW. Regulation of deoxycholate induction of CXCL8 by the adenomatous polyposis coli gene in colorectal cancer. Int J Cancer 2009;124: 2270-80.
46. Mizukami Y, Jo WS, Duerr EM, Gala M, Li J, Zhang X, et al. Induction of interleukin-8 preserves the angiogenic response in HIF-1 alpha-deficient colon cancer cells. Nat Med 2005;11:992-7.
47. Arenberg DA, Kunkel SL, Polverini PJ, Glass M, Burdick MD, Strieter RM. Inhibition of interleukin-8 reduces tumorigenesis of human non- small cell lung cancer in SCID mice. J Clin Invest 1996;97:2792-802.
48. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
49. Talmadge JE, Fidler IJ. AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res 2010;70:5649-69.
50. Lefebure B, Charbonnier F, Di Fiore F, Tuech JJ, Le Pessot F, Michot F, et al. Prognostic value of circulating mutant DNA in unresectable metastatic colorectal cancer. Ann Surg 2010;251:275-80.