Cancer-related inflammation, the seventh hallmark of cancer: Links to genetic instability

Carcinogenesis

Volumn 30, Issue 7, 2009, Pages 1073-1081

  Colotta, Francesco ^a   Allavena, Paola ^b   Sica, Antonio ^b,c   Garlanda, Cecilia ^b   Mantovani, Alberto ^b,d  

^a NERVIANO MEDICAL SCIENCES   (Italy)

^b HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^c UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^d UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN RECEPTOR; CYCLOOXYGENASE 2; CYTOKINE; DOUBLE STRANDED DNA; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1R1; INTERLEUKIN 6; MATRIX METALLOPROTEINASE; MISMATCH REPAIR PROTEIN; PROTEIN FAT10; PROTEIN MAD2; PROTEIN MSH2; PROTEIN MSH6; PROTEIN P53; PROTEIN TIR8; REACTIVE OXYGEN METABOLITE; STAT3 PROTEIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 6; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA; UBIQUITIN; UNCLASSIFIED DRUG;

ANEUPLOIDY; BONE MARROW CELL; CANCER CELL; CANCER GROWTH; CANCER INVASION; CANCER RELATED INFLAMMATION; CARCINOGENESIS; CHROMOSOMAL INSTABILITY; CHROMOSOME SEGREGATION; CPG ISLAND; DNA SYNTHESIS; ENZYME PHOSPHORYLATION; EPIGENETICS; EXCISION REPAIR; GENE MUTATION; GENE OVEREXPRESSION; GENETIC STABILITY; HUMAN; INFLAMMATION; INFLAMMATORY CELL; INNATE IMMUNITY; INTESTINE CANCER; LEUKOCYTE ADHERENCE; LYMPHOCYTIC INFILTRATION; MALIGNANT NEOPLASTIC DISEASE; MICROSATELLITE INSTABILITY; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; ONCOGENE C MYC; PANCREATITIS; PRIORITY JOURNAL; REVIEW; SUPPRESSOR CELL; TUMOR ASSOCIATED LEUKOCYTE; ULCERATIVE COLITIS;

CELL PROLIFERATION; CYTOKINES; GENOMIC INSTABILITY; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; NEOPLASMS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 67650151005     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgp127     Document Type: Review

References (188)

1. Balkwill,F. et al. (2001) Inflammation and cancer: Back to Virchow? Lancet, 357, 539-545.
2. Coussens,L.M. et al. (2002) Inflammation and cancer. Nature, 420, 860-867.
3. Balkwill,F. et al. (2005) Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell, 7, 211-217.
4. Mantovani,A. et al. (2008) Cancer-related inflammation. Nature 454, 436-444.
5. Borrello,M.G. et al. (2005) Induction of a proinflammatory program in normal human thyrocytes by the RET/PTC1 oncogene. Proc. Natl Acad. Sci. USA, 102, 14825-14830.
6. Mantovani,A. (2009) Cancer: Inflaming metastasis. Nature, 457 36-37.
7. Rius,J. et al. (2008) NF-kappaB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1alpha. Nature, 453, 807-811.
8. Balkwill,F. (2009) Tumour necrosis factor and cancer. Nat. Rev. Cancer, 9, 361-371.
9. Hanahan,D. et al. (2000) The hallmarks of cancer. Cell, 100, 57-70.
10. Loberg,R.D. et al. (2007) Targeting CCL2 with systemic delivery of neutralizing antibodies induces prostate cancer tumor regression in vivo. Cancer Res., 67, 9417-9424.
11. Harrison,M.L. et al. (2007) Tumor necrosis factor alpha as a new target for renal cell carcinoma: Two sequential phase II trials of infliximab at standard and high dose. J. Clin. Oncol., 25, 4542-4549.
12. Karin,M. (2006) Nuclear factor-kappaB in cancer development and progression. Nature, 441, 431-436.
13. Yu,H. et al. (2007) Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat. Rev. Immunol., 7, 41-51.
14. Voronov,E. et al. (2003) IL-1 is required for tumor invasiveness and angiogenesis. Proc. Natl Acad. Sci. USA, 100, 2645-2650.
15. Langowski,J.L. et al. (2006) IL-23 promotes tumour incidence and growth. Nature, 442, 461-465.
16. Carbia-Nagashima,A. et al. (2007) RSUME, a small RWD-containing protein, enhances SUMO conjugation and stabilizes HIF-1alpha during hypoxia. Cell, 131, 309-323.
17. Taylor,C.T. (2008) Interdependent roles for hypoxia inducible factor and nuclear factor-kappaB in hypoxic inflammation. J. Physiol., 586 4055-4059.
18. Greten,F.R. et al. (2004) IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell, 118, 285-296.
19. Pikarsky,E. et al. (2004) NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature, 431, 461-466.
20. Maeda,S. et al. (2005) IKKbeta couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell, 121, 977-990.
21. Garlanda,C. et al. (2007) Increased susceptibility to colitis-associated cancer of mice lacking TIR8, an inhibitory members of the IL-1 receptor family. Cancer Res., 67, 6017-6021.
22. Xiao,H. et al. (2007) The Toll-interleukin-1 receptor member SIGIRR regulates colonic epithelial homeostasis, inflammation, and tumorigenesis. Immunity, 26, 461-475.
23. Lech,M. et al. (2008) Tir8/Sigirr prevents murine lupus by suppressing the immunostimulatory effects of lupus autoantigens. J. Exp. Med., 205, 1879-1888.
24. Lee,H. et al. (2009) Persistently activated Stat3 maintains constitutive NF-kappaB activity in tumors. Cancer Cell, 15, 283-293.
25. Kortylewski,M. et al. (2005) Inhibiting Stat3 signaling in the hematopoietic system elicits multicomponent antitumor immunity. Nat. Med., 11, 1314-1321.
26. Becker,C. et al. (2004) TGF-beta suppresses tumor progression in colon cancer by inhibition of IL-6 trans-signaling. Immunity, 21, 491-501.
27. Gao,S.P. et al. (2007) Mutations in the EGFR kinase domain mediate STAT3 activation via IL-6 production in human lung adenocarcinomas. J. Clin. Invest., 117, 3846-3856.
28. Grivennikov,S. et al. (2008) Autocrine IL-6 signaling: A key event in tumorigenesis? Cancer Cell, 13, 7-9.
29. Lin,W.W. et al. (2007) A cytokine-mediated link between innate immunity, inflammation, and cancer. J. Clin. Invest., 117, 1175-1183.
30. Naugler,W.E. et al. (2008) The wolf in sheep's clothing: The role of interleukin-6 in immunity, inflammation and cancer. Trends Mol. Med., 14, 109-119.
31. Grivennikov,S. et al. (2009) IL-6 and stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell, 15, 103-113.
32. Bollrath,J. et al. (2009) gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis. Cancer Cell, 15, 91-102.
33. Kortylewski,M. et al. (2009) Regulation of the IL-23 and IL-12 balance by Stat3 signaling in the tumor microenvironment. Cancer Cell 15, 114-123.
34. Annunziata,C.M. et al. (2007) Frequent engagement of the classical and alternative NF-kappaB pathways by diverse genetic abnormalities in multiple myeloma. Cancer Cell, 12, 115-130.
35. Keats,J.J. et al. (2007) Promiscuous mutations activate the noncanonical NF-kappaB pathway in multiple myeloma. Cancer Cell, 12, 131-144.
36. Naugler,W.E. et al. (2007) Gender disparity in liver cancer due to sex differences in MyD88-dependent-IL-6 production. Science, 317, 121-124.
37. Rakoff-Nahoum,S. et al. (2007) Regulation of spontaneous intestinal tumorigenesis through the adaptor protein MyD88. Science 317, 124-127.
38. Moore,R.J. et al. (1999) Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat. Med., 5 828-831.
39. Popivanova,B.K. et al. (2008) Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J. Clin. Invest., 118, 560-570.
40. Kulbe,H. et al. (2007) The inflammatory cytokine tumor necrosis factor-alpha generates an autocrine tumor-promoting network in epithelial ovarian cancer cells. Cancer Res., 67, 585-592.
41. Oguma,K. et al. (2008) Activated macrophages promote Wnt signalling through tumour necrosis factor-alpha in gastric tumour cells. EMBO J., 27, 1671-1681.
42. Chang,Y.C. et al. (2008) Epigenetic control of MHC class II expression in tumor-associated macrophages by decoy receptor 3. Blood 111, 5054-5063.
43. Brown,E.R. et al. (2008) A clinical study assessing the tolerability and biological effects of infliximab, a TNF-alpha inhibitor, in patients with advanced cancer. Ann. Oncol., 19 1340-1346.
44. Giavazzi,R. et al. (1990) Interleukin 1-induced augmentation of experimental metastases from a human melanoma in nude mice. Cancer Res., 50, 4771-4775.
45. Luo,J.L. et al. (2007) Nuclear cytokine-activated IKKalpha controls prostate cancer metastasis by repressing Maspin. Nature, 446, 690-694.
46. Dinarello,C.A. (2006) The paradox of pro-inflammatory cytokines in cancer. Cancer Metastasis Rev., 25, 307-313.
47. Krelin,Y. et al. (2007) Interleukin-1beta-driven inflammation promotes the development and invasiveness of chemical carcinogen-induced tumors. Cancer Res., 67, 1062-1071.
48. Sakurai,T. et al. (2008) Hepatocyte necrosis induced by oxidative stress and IL-1 alpha release mediate carcinogen-induced compensatory proliferation and liver tumorigenesis. Cancer Cell, 14, 156-165.
49. Shchors,K. et al. (2006) The Myc-dependent angiogenic switch in tumors is mediated by interleukin 1beta. Genes Dev., 20, 2527-2538.
50. El-Omar,E.M. et al. (2000) Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature, 404, 398-402.
51. Tu,S. et al. (2008) Overexpression of interleukin-1beta induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice. Cancer Cell, 14, 408-419.
52. Zhu,P. et al. (2006) Macrophage/cancer cell interactions mediate hormone resistance by a nuclear receptor derepression pathway. Cell 124, 615-629.
53. Marhaba,R. et al. (2008) Opposing effects of fibrosarcoma cell-derived IL-1 alpha and IL-1 beta on immune response induction. Int. J. Cancer, 123, 134-145.
54. Elkabets,M. et al. (2009) Host-derived interleukin-1α is important in determining the immunogenicity of 3-methylcholantrene-tumor cells. J. immunol., 182, 4874-4881.
55. Chen,C.J. et al. (2007) Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat. Med., 13, 851-856.
56. de Visser,K.E. et al. (2006) Paradoxical roles of the immune system during cancer development. Nat. Rev. Cancer, 6, 24-37.
57. Galli,S.J. et al. (2008) Immunomodulatory mast cells: Negative, as well as positive, regulators of immunity. Nat. Rev. Immunol., 8 478-486.
58. Balkwill,F. (2004) Cancer and the chemokine network. Nat. Rev. Cancer 4, 540-550.
59. Mantovani,A. et al. (2002) Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol., 23, 549-555.
60. Sica,A. et al. (2006) Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: Potential targets of anti-cancer therapy. Eur. J. Cancer, 42, 717-727.
61. Bingle,L. et al. (2002) The role of tumour-associated macrophages in tumour progression: Implications for new anticancer therapies. J. Pathol., 196, 254-265.
62. Pollard,J.W. (2004) Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer, 4, 71-78.
63. Wyckoff,J.B. et al. (2007) Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res., 67, 2649-2656.
64. Mantovani,A. et al. (2006) Role of tumor-associated macrophages in tumor progression and invasion. Cancer Metastasis Rev., 25, 315-322.
65. Condeelis,J. et al. (2006) Macrophages: Obligate partners for tumor cell migration, invasion, and metastasis. Cell, 124, 263-266.
66. Yang,L. et al. (2008) Abrogation of TGFbeta signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer Cell, 13, 23-35.
67. Murdoch,C. et al. (2008) The role of myeloid cells in the promotion of tumour angiogenesis. Nat. Rev. Cancer, 8, 618-631.
68. Du,R. et al. (2008) HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell, 13, 206-220.
69. Seandel,M. et al. (2008) A catalytic role for proangiogenic marrow-derived cells in tumor neovascularization. Cancer Cell, 13, 181-183.
70. Ahn,G.O. et al. (2008) Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: Role of bone marrow-derived myelomonocytic cells. Cancer Cell, 13, 193-205.
71. Dineen,S.P. et al. (2008) Vascular endothelial growth factor receptor 2 mediates macrophage infiltration into orthotopic pancreatic tumors in mice. Cancer Res., 68, 4340-4346.
72. Kusmartsev,S. et al. (2008) Oxidative stress regulates expression of VEGFR1 in myeloid cells: Link to tumor-induced immune suppression in renal cell carcinoma. J. Immunol., 181, 346-353.
73. Duluc,D. et al. (2007) Tumor-associated leukemia inhibitory factor and IL-6 skew monocyte differentiation into tumor-associated macrophage-like cells. Blood, 110, 4319-4330.
74. Morandi,F. et al. (2007) Human neuroblastoma cells trigger an immunosuppressive program in monocytes by stimulating soluble HLA-G release. Cancer Res., 67, 6433-6441.
75. Robinson-Smith,T.M. et al. (2007) Macrophages mediate inflammationenhanced metastasis of ovarian tumors in mice. Cancer Res., 67, 5708-5716.
76. Stearman,R.S. et al. (2008) A macrophage gene expression signature defines a field effect in the lung tumor microenvironment. Cancer Res., 68, 34-43.
77. Lewis,C.E. et al. (2006) Distinct role of macrophages in different tumor microenvironments. Cancer Res., 66, 605-612.
78. Sierra,J.R. et al. (2008) Tumor angiogenesis and progression are enhanced by Sema4D produced by tumor-associated macrophages. J. Exp. Med., 205, 1673-1685.
79. Fischer,C. et al. (2007) Anti-PlGF inhibits growth of VEGF(R)-inhibitorresistant tumors without affecting healthy vessels. Cell, 131, 463-475.
80. Kaplan,R.N. et al. (2005) VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature, 438, 820-827.
81. Witz,I.P. (2008) Tumor-microenvironment interactions: Dangerous liaisons. Adv. Cancer Res., 100, 203-229.
82. De Palma,M. et al. (2005) Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell, 8 211-226.
83. De Palma,M. et al. (2003) Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat. Med., 9, 789-795.
84. De Palma,M. et al. (2007) Tie2-expressing monocytes: Regulation of tumor angiogenesis and therapeutic implications. Trends. Immunol., 28, 519-524.
85. De Palma,M. et al. (2008) Tumor-targeted interferon-alpha delivery by Tie2-expressing monocytes inhibits tumor growth and metastasis. Cancer Cell, 14, 299-311.
86. Sawanobori,Y. et al. (2008) Chemokine-mediated rapid turnover of myeloidderived suppressor cells in tumor-bearing mice. Blood, 111, 5457-5466.
87. Sica,A. et al. (2007) Altered macrophage differentiation and immune dysfunction in tumor development. J. Clin. Invest., 117 1155-1166.
88. Yang,L. et al. (2004) Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell, 6, 409-421.
89. Noonan,D.M. et al. (2008) Inflammation, inflammatory cells and angiogenesis: Decisions and indecisions. Cancer Metastasis Rev., 27, 31-40.
90. Shojaei,F. et al. (2007) Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells. Nat. Biotechnol. 25, 911-920.
91. Huang,B. et al. (2006) Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res., 66, 1123-1131.
92. Sinha,P. et al. (2007) Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J. Immunol., 179, 977-983.
93. Nagaraj,S. et al. (2008) Tumor escape mechanism governed by myeloidderived suppressor cells. Cancer Res., 68, 2561-2563.
94. Muller,A.J. et al. (2008) Chronic inflammation that facilitates tumor progression creates local immune suppression by inducing indoleamine 2,3 dioxygenase. Proc. Natl Acad. Sci. USA, 105, 17073-17078.
95. Allavena,P. et al. (2008) The Yin-Yang of tumor-associated macrophages in neoplastic progression and immune surveillance. Immunol. Rev., 222, 155-161.
96. Hagemann,T. et al. (2008) "Re-educating" tumor-associated macrophages by targeting NF-kappaB. J. Exp. Med., 205, 1261-1268.
97. Biswas,S.K. et al. (2006) A distinct and unique transcriptional programme expressed by tumor-associated macrophages: Defective NF-kB and enhanced IRF-3/STAT1 activation. Blood, 107, 2112-2122.
98. Tennant,D.A. et al. (2009) Metabolic transformation in cancer. Carcinogenesis, in press.
99. Shime,H. et al. (2008) Tumor-secreted lactic acid promotes IL-23/ IL-17 proinflammatory pathway. J. Immunol., 180, 7175-7183.
100. Kim,S. et al. (2009) Carcinoma produced factors activate myeloid cells via TLR2 to stimulate metastasis. Nature, 457, 102-106.
101. Loeb,L.A. et al. (2008) DNA polymerases and human disease. Nat. Rev. Genet., 9, 594-604.
102. Rajagopalan,H. et al. (2002) Tumorigenesis: RAF/RAS oncogenes and mismatch-repair status. Nature, 418, 934.
103. Nowell,P.C. (1976) The clonal evolution of tumor cell populations. Science, 194, 23-8.
104. Hakem,R. (2008) DNA-damage repair; the good, the bad, and the ugly. EMBO J., 27, 589-605.
105. Jung,Y.J. et al. (2003) IL-1beta-mediated up-regulation of HIF-1alpha via an NFkappaB/COX-2 pathway identifies HIF-1 as a critical link between inflammation and oncogenesis. FASEB J., 17, 2115-2117.
106. Sandau,K.B. et al. (2000) Induction of hypoxia-inducible-factor 1 by nitric oxide is mediated via the PI 3K pathway. Biochem. Biophys. Res. Commun., 278, 263-267.
107. Koshiji,M. et al. (2005) HIF-1alpha induces genetic instability by transcriptionally downregulating MutSalpha expression. Mol. Cell, 17, 793-803.
108. Chang,C.L. et al. (2002) Oxidative stress inactivates the human DNA mismatch repair system. Am. J. Physiol. Cell Physiol., 283 C148-C154.
109. Gasche,C. et al. (2001) Oxidative stress increases frameshift mutations in human colorectal cancer cells. Cancer Res., 61, 7444-7448.
110. Fleisher,A.S. et al. (2000) Microsatellite instability in inflammatory bowel disease-associated neoplastic lesions is associated with hypermethylation and diminished expression of the DNA mismatch repair gene, hMLH1. Cancer Res., 60, 4864-4868.
111. Mirzaee,V. et al. (2008) Helicobacter pylori infection and expression of DNA mismatch repair proteins. World J. Gastroenterol. 14, 6717-6721.
112. Brentnall,T.A. et al. (1996) Microsatellite instability in nonneoplastic mucosa from patients with chronic ulcerative colitis. Cancer Res., 56, 1237-1240.
113. Hussain,S.P. et al. (2000) Increased p53 mutation load in noncancerous colon tissue from ulcerative colitis: A cancer-prone chronic inflammatory disease. Cancer Res., 60, 3333-3337.
114. Campregher,C. et al. (2008) Activated neutrophils induce an hMSH2dependent G2/Mcheckpoint arrest and replication errors at a (CA)13-repeat in colon epithelial cells. Gut, 57, 780-787.
115. Guo,H.H. et al. (2003) Tumbling down a different pathway to genetic instability. J. Clin. Invest., 112, 1793-1795.
116. Hofseth,L.J. et al. (2003) The adaptive imbalance in base excision-repair enzymes generates microsatellite instability in chronic inflammation. J. Clin. Invest., 112, 1887-1894.
117. Ramana,C.V. et al. (1998) Activation of apurinic/apyrimidinic endonuclease in human cells by reactive oxygen species and its correlation with their adaptive response to genotoxicity of free radicals. Proc. Natl Acad. Sci. USA, 95, 5061-5066.
118. Hodge,D.R. et al. (2005) Interleukin 6 supports the maintenance of p53 tumor suppressor gene promoter methylation. Cancer Res., 65 4673-4682.
119. Crosby,M.E. et al. (2009) MicroRNA regulation of DNA repair gene expression in hypoxic stress. Cancer Res., 69, 1221-1229.
120. Rajagopalan,H. et al. (2003) The significance of unstable chromosomes in colorectal cancer. Nat. Rev. Cancer, 3, 695-701.
121. Roschke,A.V. et al. (2008) Chromosomal instability is associated with higher expression of genes implicated in epithelial-mesenchymal transition, cancer invasiveness, and metastasis and with lower expression of genes involved in cell cycle checkpoints, DNA repair, and chromatin maintenance. Neoplasia, 10, 1222-1230.
122. Tomasini,R. et al. (2008) The impact of p53 and p73 on aneuploidy and cancer. Trends Cell Biol., 18, 244-252.
123. Baek,K.H. et al. (2003) p53 deficiency and defective mitotic checkpoint in proliferating T lymphocytes increase chromosomal instability through aberrant exit from mitotic arrest. J. Leukoc. Biol., 73, 850-861.
124. Talos,F. et al. (2007) p73 suppresses polyploidy and aneuploidy in the absence of functional p53. Mol. Cell, 27, 647-659.
125. Hudson,J.D. et al. (1999) A proinflammatory cytokine inhibits p53 tumor suppressor activity. J. Exp. Med., 190, 1375-1382.
126. Calmels,S. et al. (1997) Nitric oxide induces conformational and functional modifications of wild-type p53 tumor suppressor protein. Cancer Res., 57, 3365-3369.
127. Cobbs,C.S. et al. (2003) Inactivation of wild-type p53 protein function by reactive oxygen and nitrogen species in malignant glioma cells. Cancer Res., 63, 8670-8673.
128. Ambs,S. et al. (1999) Cancer-prone oxyradical overload disease. IARC Sci. Publ., 150, 295-302.
129. Marshall,H.E. et al. (2000) Nitrosation and oxidation in the regulation of gene expression. FASEB J., 14, 1889-1900.
130. Jaiswal,M. et al. (2001) Nitric oxide in gastrointestinal epithelial cell carcinogenesis: Linking inflammation to oncogenesis. Am. J. Physiol. Gastrointest. Liver Physiol., 281, G626-G34.
131. Wink,D.A. et al. (1994) The Fpg protein, a DNA repair enzyme, is inhibited by the biomediator nitric oxide in vitro and in vivo. Carcinogenesis, 15, 2125-2129.
132. Hmadcha,A. et al. (1999) Methylation-dependent gene silencing induced by interleukin 1beta via nitric oxide production. J. Exp. Med., 190, 1595-1604.
133. Goodman,J.E. et al. (2004) Nitric oxide and p53 in cancer-prone chronic inflammation and oxyradical overload disease. Environ. Mol. Mutagen., 44, 3-9.
134. Brentnall,T.A. et al. (1994) Mutations in the p53 gene: An early marker of neoplastic progression in ulcerative colitis. Gastroenterology, 107, 369-378.
135. Burmer,G.C. et al. (1992) Neoplastic progression in ulcerative colitis: Histology, DNA content, and loss of a p53 allele. Gastroenterology, 103, 1602-1610.
136. Greeve,J. et al. (2003) Expression of activation-induced cytidine deaminase in human B-cell non-Hodgkin lymphomas. Blood, 101, 3574-3580.
137. Lossos,I.S. et al. (2004) AID is expressed in germinal center B-cell-like and activated B-cell-like diffuse large-cell lymphomas and is not correlated with intraclonal heterogeneity. Leukemia, 18 1775-1779.
138. Matsumoto,Y. et al. (2007) Helicobacter pylori infection triggers aberrant expression of activation-induced cytidine deaminase in gastric epithelium. Nat. Med., 13, 470-476.
139. Endo,Y. et al. (2007) Expression of activation-induced cytidine deaminase in human hepatocytes via NF-kappaB signaling. Oncogene, 26, 5587-5595.
140. Kou,T. et al. (2007) Expression of activation-induced cytidine deaminase in human hepatocytes during hepatocarcinogenesis. Int. J. Cancer, 120, 469-476.
141. Komori,J. et al. (2008) Activation-induced cytidine deaminase links bile duct inflammation to human cholangiocarcinoma. Hepatology 47, 888-896.
142. Endo,Y. et al. (2008) Activation-induced cytidine deaminase links between inflammation and the development of colitis-associated colorectal cancers. Gastroenterology, 135, 889-898;898, e1-e3.
143. Chesi,M. et al. (2008) AID-dependent activation of a MYC transgene induces multiple myeloma in a conditional mouse model of post-germinal center malignancies. Cancer Cell, 13, 167-180.
144. Robbiani,D.F. et al. (2008) AID is required for the chromosomal breaks in c-myc that lead to c-myc/IgH translocations. Cell, 135, 1028-1038.
145. Shen,H.M. et al. (1998) Mutation of BCL-6 gene in normal B cells by the process of somatic hypermutation of Ig genes. Science, 280, 1750-1752.
146. Singh,B. et al. (2007) Cyclooxygenase-2 expression induces genomic instability in MCF10A breast epithelial cells. J. Surg. Res., 140, 220-226.
147. Lam,M.H. et al. (2004) Chk1 is haploinsufficient for multiple functions critical to tumor suppression. Cancer Cell, 6, 45-59.
148. Golubkov,V.S. et al. (2005) Membrane type-1 matrix metalloproteinase (MT1-MMP) exhibits an important intracellular cleavage function and causes chromosome instability. J. Biol. Chem., 280 25079-25086.
149. Golubkov,V.S. et al. (2007) Proteolysis-driven oncogenesis. Cell Cycle, 6, 147-150.
150. Sternlicht,M.D. et al. (2001) How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol., 17, 463-516.
151. Sternlicht,M.D. et al. (1999) The stromal proteinase MMP3/ stromelysin-1 promotes mammary carcinogenesis. Cell, 98, 137-146.
152. Lochter,A. et al. (1997) Misregulation of stromelysin-1 expression in mouse mammary tumor cells accompanies acquisition of stromelysin-1-dependent invasive properties. J. Biol. Chem., 272, 5007-5015.
153. Matos,P. et al. (2003) Tumor-related alternatively spliced Rac1b is not regulated by Rho-GDP dissociation inhibitors and exhibits selective downstream signaling. J. Biol. Chem., 278, 50442-50448.
154. Samper,E. et al. (2003) Mitochondrial oxidative stress causes chromosomal instability of mouse embryonic fibroblasts. Aging Cell 2, 277-285.
155. Ying,L. et al. (2005) Chronic inflammation promotes retinoblastoma protein hyperphosphorylation and E2F1 activation. Cancer Res., 65, 9132-9136.
156. Ying,L. et al. (2007) Nitric oxide inactivates the retinoblastoma pathway in chronic inflammation. Cancer Res., 67, 9286-9293.
157. Hernando,E. et al. (2004) Rb inactivation promotes genomic instability by uncoupling cell cycle progression from mitotic control. Nature, 430, 797-802.
158. Lee,C.G. et al. (2003) Expression of the FAT10 gene is highly upregulated in hepatocellular carcinoma and other gastrointestinal and gynecological cancers. Oncogene, 22, 2592-2603.
159. Ren,J. et al. (2006) FAT10 plays a role in the regulation of chromosomal stability. J. Biol. Chem., 281, 11413-11421.
160. Lukasiak,S. et al. (2008) Proinflammatory cytokines cause FAT10 upregulation in cancers of liver and colon. Oncogene, 27, 6068-6074.
161. Zhang,D.W. et al. (2006) p53 negatively regulates the expression of FAT10, a gene upregulated in various cancers. Oncogene, 25 2318-2327.
162. Mills,K.D. et al. (2003) The role of DNA breaks in genomic instability and tumorigenesis. Immunol. Rev., 194, 77-95.
163. Karanjawala,Z.E. et al. (2002) Oxygen metabolism causes chromosome breaks and is associated with the neuronal apoptosis observed in DNA double-strand break repair mutants. Curr. Biol., 12, 397-402.
164. Opresko,P.L. et al. (2005) Oxidative damage in telomeric DNA disrupts recognition by TRF1 and TRF2. Nucleic Acids Res., 33 1230-1239.
165. von Zglinicki,T. et al. (2005) Telomeres as biomarkers for ageing and age-related diseases. Curr. Mol. Med., 5, 197-203.
166. San Filippo,J. et al. (2008) Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem., 77, 229-257.
167. Lieber,M.R. (2008) The mechanism of human nonhomologous DNA end joining. J. Biol. Chem., 283, 1-5.
168. Halazonetis,T.D. et al. (2008) An oncogene-induced DNA damage model for cancer development. Science, 319, 1352-1355.
169. Vafa,O. et al. (2002) c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: A mechanism for oncogene-induced genetic instability. Mol. Cell, 9, 1031-1044.
170. Dominguez-Sola,D. et al. (2007) Non-transcriptional control of DNA replication by c-Myc. Nature, 448, 445-451.
171. Taylor,W.R. et al. (1999) Mechanisms of G2 arrest in response to over-expression of p53. Mol. Biol. Cell, 10, 3607-3622.
172. Menssen,A. et al. (2007) c-MYC delays prometaphase by direct transactivation of MAD2 and BubR1: Identification of mechanisms underlying c-MYC-induced DNA damage and chromosomal instability. Cell Cycle, 6, 339-352.
173. Saintigny,Y. et al. (2001) A novel role for the Bcl-2 protein family: Specific suppression of the RAD51 recombination pathway. EMBO J., 20, 2596-2607.
174. Plo,I. et al. (2008) JAK2 stimulates homologous recombination and genetic instability: Potential implication in the heterogeneity of myeloproliferative disorders. Blood, 112, 1402-1412.
175. Bielas,J.H. et al. (2006) Human cancers express a mutator phenotype. Proc. Natl Acad. Sci. USA, 103, 18238-18242.
176. Firestein,G.S. et al. (1997) Somatic mutations in the p53 tumor suppressor gene in rheumatoid arthritis synovium. Proc. Natl Acad. Sci. USA, 94, 10895-10900.
177. Andreassi,M.G. et al. (2003) Genetic instability, DNA damage and atherosclerosis. Cell Cycle, 2, 224-227.
178. Weinberg,R.A. (2008) Coevolution in the tumor microenvironment. Nat. Genet., 40, 494-495.
179. Danish,M. et al. (2008) Genetic stability of tumor microenvironment. Cancer Biol. Ther., 7, 331-332.
180. Polyak,K. et al. (2009) Co-evolution of tumor cells and their microenvironment. Trends Genet., 25, 30-38.
181. Qiu,W. 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.
182. Apetoh,L. et al. (2007) Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med., 13, 1050-1059.
183. Shabo,I. et al. (2008) Breast cancer expression of CD163, a macrophage scavenger receptor, is related to early distant recurrence and reduced patient survival. Int. J. Cancer, 123, 780-786.
184. Tamimi,R.M. et al. (2008) Circulating colony stimulating factor-1 and breast cancer risk. Cancer Res., 68, 18-21.
185. Taskinen,M. et al. (2007) A high tumor-associated macrophage content predicts favorable outcome in follicular lymphoma patients treated with rituximab and cyclophosphamide-doxorubicin-vincristine-prednisone. Clin. Cancer Res., 13, 5784-5789.
186. Byers,R.J. et al. (2008) Clinical quantitation of immune signature in follicular lymphoma by RT-PCR-based gene expression profiling. Blood, 111, 4764-4770.
187. Liu,R. et al. (2007) The prognostic role of a gene signature from tumorigenic breast-cancer cells. N. Engl. J. Med., 356, 217-226.
188. Seike,M. et al. (2007) Use of a cytokine gene expression signature in lung adenocarcinoma and the surrounding tissue as a prognostic classifier. J. Natl Cancer Inst., 99, 1257-1269.