K-ras mutation targeted to gastric tissue progenitor cells results in chronic inflammation, an altered microenvironment, and progression to intraepithelial neoplasia

Cancer Research

Volumn 70, Issue 21, 2010, Pages 8435-8445

  Okumura, Tomoyuki ^a   Ericksen, Russell E ^a   Takaishi, Shigeo ^a   Wang, Sophie S W ^a   Dubeykovskiy, Zinaida ^a   Shibata, Wataru ^a   Betz, Kelly S ^a   Muthupalani, Sureshkuma ^b   Rogers, Arlin B ^c   Fox, James G ^b   Rustgi, Anil K ^d   Wang, Timothy C ^a  

^a Columbia University Medical School ^*  (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; AMPHIREGULIN; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CYTOKERATIN 19; DOUBLECORTIN AND CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE LIKE 1; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; GAMMA INTERFERON; GREEN FLUORESCENT PROTEIN; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; INTERLEUKIN 1BETA; INTERLEUKIN 6; K RAS PROTEIN; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MOLECULAR MARKER; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VIMENTIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW; GASTROINTESTINAL DYSPLASIA; GENE MUTATION; HELICOBACTER FELIS; HELICOBACTER INFECTION; HISTOPATHOLOGY; HYPERPLASIA; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LEUKOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL; STOMACH DYSPLASIA; STOMACH EPITHELIUM; STROMA CELL; TRANSGENIC MOUSE; TUMOR MICROENVIRONMENT; UPREGULATION; Y CHROMOSOME;

ACTINS; ANIMALS; BLOTTING, WESTERN; BONE MARROW TRANSPLANTATION; CARCINOMA IN SITU; CELL PROLIFERATION; CHEMOKINES; CYTOKINES; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HELICOBACTER FELIS; HELICOBACTER INFECTIONS; HUMANS; HYPERPLASIA; IMMUNOENZYME TECHNIQUES; IN SITU HYBRIDIZATION; INFLAMMATION; KERATIN-19; MESENCHYMAL STEM CELLS; METAPLASIA; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE, SMOOTH; MUTATION; NEOPLASM INVASIVENESS; PRECANCEROUS CONDITIONS; PROTO-ONCOGENE PROTEINS; RAS PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STEM CELLS; STOMACH; STOMACH NEOPLASMS; STROMAL CELLS;

EID: 78449277432     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-1506     Document Type: Article

References (54)

1. Milne AN, Carneiro F, O'Morain C, Offerhaus GJ. Nature meets nurture: molecular genetics of gastric cancer. Hum Genet 2009;126:615-28.
2. Chan AO, Chu KM, Huang C, et al. Association between Helicobacter pylori infection and interleukin 1β polymorphism predispose to CpG island methylation in gastric cancer. Gut 2007;56:595-7.
3. Houghton J, Stoicov C, Nomura S, et al. Gastric cancer originating from bone marrow-derived cells. Science 2004;306:1568-71.
4. Tu S, Bhagat G, Cui G, et al. Overexpression of interleukin-1β induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice. Cancer Cell 2008;14:408-19.
5. Oguma K, Oshima H, Aoki M, et al. Activated macrophages promote Wnt signaling through tumor necrosis factor-α in gastric tumor cells. EMBO J 2008;27:1671-81.
6. Lin WW, Karin M. A cytokine-mediated link between innate immunity, inflammation, and cancer. J Clin Invest 2007;117:1175-83.
7. Andreu P, Johansson M, Affara NI, et al. FcRγ activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell 2010;17:121-34.
8. Frame S, Balmain A. Integration of positive and negative growth signals during Ras pathway activation in vivo. Curr Opin Genet Dev 2000;10:106-13.
9. Abrams SI, Stanziale SF, Lunin SD, Zaremba S, Schlom J. Identification of overlapping epitopes in mutant ras oncogene peptides that activate CD4+ and CD8+ T cell responses. Eur J Immunol 1996;262:435-43.
10. Sparmann A, Bar-Sagi D. Ras-induced interleukin-8 expression plays a critical role in tumor growth and angiogenesis. Cancer Cell 2004;6:447-58.
11. Ji H, Houghton AM, Mariani TJ, et al. K-ras activation generates an inflammatory response in lung tumors. Oncogene 2006;25:2105-12.
12. Hingorani SR, Petricoin EF, Maitra A, et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 2003;4:437-50.
13. Brembeck FH, Schreiber FS, Deramaudt TB, et al. The mutant K-ras oncogene causes pancreatic periductal lymphocytic infiltration and gastric mucous neck cell hyperplasia in transgenic mice. Cancer Res 2003;63:2005-9.
14. Sparmann A, Bar-Sagi D. Ras oncogene and inflammation: partners in crime. Cell Cycle 2005;4:735-6.
15. Borrello MG, Degl'Innocenti D, Pierotti MA. Inflammation and cancer: the oncogene-driven connection. Cancer Lett 2008;267:262-70.
16. Brembeck FH, Moffett J, Wang TC, Rustgi AK. The keratin 19 promoter is potent for cell-specific targeting of genes in transgenic mice. Gastroenterology 2001;120:1720-8.
17. Calnek D, Quaroni A. Changes in keratin expression during fetal and postnatal development of intestinal epithelial cells. Biochem J 1992;285:939-46.
18. Calnek D, Quaroni A. Differential localization by in situ hybridization of distinct keratin mRNA species during intestinal epithelial cell development and differentiation. Differentiation 1993;53:95-104.
19. Giannakis M, Stappenbeck TS, Mills JC, et al. Molecular properties of adult mouse gastric and intestinal epithelial progenitors in their niches. J Biol Chem 2006;281:11292-300.
20. May R, Riehl TE, Hunt C, Sureban SM, Anant S, Houchen CW. Identification of a novel putative gastrointestinal stem cell and adenoma stem cell marker, doublecortin and CaM kinase-like-1, following radiation injury and in adenomatous polyposis coli/multiple intestinal neoplasia mice. Stem Cells 2008;26:630-7.
21. Rogers AB, Taylor NS, Whary MT, Stefanich ED, Wang TC, Fox JG. Helicobacter pylori but not high salt induces gastric intraepithelial neoplasia in B6129 mice. Cancer Res 2005;65:10709-15.
22. Rogers AB, Houghton J. Helicobacter-based mouse models of digestive system carcinogenesis. Methods Mol Biol 2009;511:267-95.
23. Wang SS, Asfaha S, Okumura T, et al. Fibroblastic colony-forming unit bone marrow cells delay progression to gastric dysplasia in a Helicobacter model of gastric carcinogenesis. Stem Cells 2009;27:2301-11.
24. Rosselot C, Spraggon L, Chia I, et al. Non-cell autonomous retinoid signaling is cruicial for renal development. Development 2010;137:283-92.
25. Oshima H, Oshima M, Inaba K, Taketo MM. Hyperplastic gastric tumors induced by activated macrophages in COX-2/mPGES-1 transgenic mice. EMBO J 2004;23:1669-78.
26. Barker N, Huch M, et al. Lgr5+ve stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell 2010;6:25-36.
27. Habbe N, Shi G, Meguid RA, et al. Spontaneous induction of murine pancreatic intraepithelial neoplasia (mPanIN) by acinar cell targeting of oncogenic K-ras in adult mice. PNAS 2008;105:18913-8.
28. Watari J, Tanaka A, Tanabe H, et al. K-ras mutations and cell kinetics in Helicobacter pylori associated gastric intestinal metaplasia: a comparison before and after eradication in patients with chronic gastritis and gastric cancer. J Clin Pathol 2007;60:921-6.
29. Hiyama T, Haruma K, Kitadai Y, et al. K-ras mutation in helicobacter pylori-associated chronic gastritis in patients with and without gastric cancer. Int J Cancer 2002;97:562-6.
30. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 2006;6:24-37.
31. Fox JG, Wang TC. Inflammation, atrophy, and gastric cancer. J Clin Invest 2007;117:60-9.
32. Balkwill F, Charles KA, Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 200;7:211-7, Review.
33. Schubbert S, Shannon K, Bollag G. Hyperactive Ras in developmental disorders and cancer. Nat Rev Cancer 2007;7:295-308, Review.
34. Ancrile B, Lim KH, Counter CM. Oncogenic Ras-induced secretion of IL6 is required for tumorigenesis. Genes Dev 2007;21:1714-9.
35. Yang G, Rosen DG, Zhang Z, et al. The chemokine growth-regulated oncogene 1 (Gro-1) links RAS signaling to the senescence of stromal fibroblasts and ovarian tumorigenesis. PNAS 2006;103:16472-7.
36. Takahashi M, Mutoh M, Shoji Y, et al. Transfection of K-rasAsp12 cDNA markedly elevates IL-1β- and lipopolysaccharide-mediated inducible nitric oxide synthase expression in rat intestinal epithelial cells. Oncogene 2003;22:7667-76.
37. Junnila S, Kokkola A, Mizuguchi T, et al. Gene expression analysis identifies over-expression of CXCL1, SPARC, SPP1, and SULF1 in gastric cancer. Genes Chromosomes Cancer 2010;49:28-39.
38. Moser B, Clark-Lewis I, Zwahlen R, Baggiollni M. Neutrophil-activating properties of the melanoma growth-stimulatory activity. J Exp Med 1990;171:1797-802.
39. Haghnegahdar H, Du J, Wang D, et al. The tumorigenic and angiogenic effects of MGSA/GRO proteins in melanoma. J Leukoc Biol 2000;67:53-62.
40. Fox JG, Feng Y, Theve EJ, et al. Gut microbes define liver cancer risk in mice exposed to chemical and viral transgenic hepatocarcinogens. Gut 2010;59:88-97.
41. Zhang Z, Sheng H, Shao J, et al. Posttranscriptional regulation of cylooxygenase-2 in rat intestinal epithelial cells. Neoplasia 2000;2:523-30.
42. Shono Y, Tanimura H, Iwahashi M, et al. Specific T-cell immunity against Ki-ras peptides in patients with pancreatic and colorectal cancers. Br J Cancer 2003;88:530-6.
43. Bristol JA, Orsini C, Lindinger P, Thalhamer J, Abrams SI. Identification of a ras oncogene peptide that contains both CD4+ and CD8+ T cell epitopes in a nested configuration and elicits both T cell subset responses by peptide or DNA immunization. Cell Immunol 2000;205:73-83.
44. Qiu Y, Zhu J, Bandi V, et al. Biopsy neutrophilia, neutrophil chemokine and receptor gene expression in severe exacerbations of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2003;168:968-75.
45. Park JY, Park KH, Bang S, et al. CXCL5 overexpression is associated with late stage gastric cancer. J Cancer Res Clin Oncol 2007;133:835-40.
46. Sieveking D, Mitchell HM, Day AS. Gastric epithelial cell CXC chemokine secretion following Helicobacter pylori infection in vitro. J Gastroenterol Hepatol 2004;19:982-7.
47. Besner G, Higashiyama S, Klagsbrun M. Isolation and characterization of a macrophage-derived heparin binding growth factor. Cell Regul 1990;1:811-9.
48. Dickson JH, Grabowska A, El-Zaatari M, Atherton J, Watson SA. Helicobacter pylori can induce heparin-binding epidermal growth factor expression via gastrin and its receptor. Cancer Res 2006;66:7524-31.
49. Shoyab M, Plowman GD, McDonald VL, Bradley JG, Todaro GJ. Structure and function of human amphiregulin: a member of the epidermal growth factor family. Science 1989;243:1074-6.
50. Toulany M, Dittmann K, Krüger M, Baumann M, Rodemann HP. Radioresistance of K-ras mutated human tumor cells is mediated through EGFR-dependent activation of PI3K-AKT pathway. Radiother Oncol 2005;76:143-50.
51. Direkze NC, Hodivala-Dilke K, Jeffery R, et al. Bone marrow contribution to tumor-associated myofibroblasts and fibroblasts. Cancer Res 2004;64:8492-5.
52. Studeny M, Marini FC, Dembinski JL, et al. Mesenchymal stem cells: potential precursors for tumor stroma and targeted-delivery vehicles for anticancer agents. J Natl Cancer Inst 2004;96:1593-603.
53. Ishii G, Sangai T, Oda T, et al. Bone-marrow-derived myofibroblasts contribute to the cancer-induced stromal reaction. Biochem Biophys Res Commun 2003;309:232-40.
54. Guo X, Oshima H, Kitmura T, et al. Stromal fibroblasts activated by tumor cells promote angiogenesis in mouse gastric cancer. J Biol Chem 2008;283:19864-71.