Chronic inflammation and oxidative stress in human carcinogenesis

A wide array of chronic inflammatory conditions predispose susceptible cells to neoplastic transformation. In general, the longer the inflammation persists, the higher the risk of cancer. A mutated cell is a sine qua non for carcinogenesis. Inflammatory processes may induce DNA mutations in cells via oxidative/nitrosative stress. This condition occurs when the generation of free radicals and active intermediates in a system exceeds the system's ability to neutralize and eliminate them. Inflammatory cells and cancer cells themselves produce free radicals and soluble mediators such as metabolites of arachidonic acid, cytokines and chemokines, which act by further producing reactive species. These, in turn, strongly recruit inflammatory cells in a vicious circle. Reactive intermediates of oxygen and nitrogen may directly oxidize DNA, or may interfere with mechanisms of DNA repair. These reactive substances may also rapidly react with proteins, carbohydrates and lipids, and the derivative products may induce a high perturbation in the intracellular and intercellular homeostasis, until DNA mutation. The main substances that link inflammation to cancer via oxidative/nitrosative stress are prostaglandins and cytokines. The effectors are represented by an imbalance between pro‐oxidant and antioxidant enzyme activities (lipoxygenase, cyclooxygenase and phospholipid hydroperoxide glutathione‐peroxidase), hydroperoxides and lipoperoxides, aldehydes and peroxinitrite. This review focalizes some of these intricate events by discussing the relationships occurring among oxidative/nitrosative/metabolic stress, inflammation and cancer. © 2007 Wiley‐Liss, Inc.

[1]  B. Halliwell,et al.  Biochemistry of oxidative stress. , 2007, Biochemical Society transactions.

[2]  D. Leibfritz,et al.  Free radicals and antioxidants in normal physiological functions and human disease. , 2007, The international journal of biochemistry & cell biology.

[3]  B. Aggarwal,et al.  Inflammation and cancer: how hot is the link? , 2006, Biochemical pharmacology.

[4]  H. Bartsch,et al.  Chronic inflammation and oxidative stress in the genesis and perpetuation of cancer: role of lipid peroxidation, DNA damage, and repair , 2006, Langenbeck's Archives of Surgery.

[5]  Chuanshu Huang,et al.  Inflammation, a Key Event in Cancer Development , 2006, Molecular Cancer Research.

[6]  M. Valko,et al.  Free radicals, metals and antioxidants in oxidative stress-induced cancer. , 2006, Chemico-biological interactions.

[7]  L. Hofseth,et al.  Identifying and defusing weapons of mass inflammation in carcinogenesis. , 2006, Biochimica et biophysica acta.

[8]  N. Geacintov,et al.  Miscoding events during DNA synthesis past the nitration-damaged base 8-nitroguanine. , 2005, Biochemistry.

[9]  M. Cronin,et al.  Metals, toxicity and oxidative stress. , 2005, Current medicinal chemistry.

[10]  M. Blaser,et al.  Mechanisms of Disease: inflammation and the origins of cancer , 2005, Nature Clinical Practice Oncology.

[11]  T. Akaike,et al.  Nitric oxide-induced nitrative stress involved in microbial pathogenesis. , 2005, Journal of pharmacological sciences.

[12]  Jian-Min Yuan,et al.  Lipid peroxidation: a novel and unifying concept of the etiology of renal cell carcinoma (United States) , 2002, Cancer Causes & Control.

[13]  W. Glasgow,et al.  Cellular proliferation and lipid metabolism: importance of lipoxygenases in modulating epidermal growth factor-dependent mitogenesis , 1994, Cancer and Metastasis Reviews.

[14]  E. Bruyneel,et al.  [Cyclooxygenase 2 and carcinogenesis]. , 2004, Bulletin du cancer.

[15]  S. Gately.  The Contributions of Cyclooxygenase-2 to Tumor Angiogenesis , 2004, Cancer and Metastasis Reviews.

[16]  D. Grignon,et al.  Role of Eicosanoids in Prostate Cancer Progression , 2004, Cancer and Metastasis Reviews.

[17]  H. Maeda,et al.  Superoxide generation mediated by 8-nitroguanosine, a highly redox-active nucleic acid derivative. , 2003, Biochemical and biophysical research communications.

[18]  Tomohiro Sawa,et al.  Chemical basis of inflammation-induced carcinogenesis. , 2003, Archives of biochemistry and biophysics.

[19]  K. Uchida,et al.  4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. , 2003, Progress in lipid research.

[20]  P. Elsner,et al.  Oxidative stress in malignant melanoma and non‐melanoma skin cancer , 2003, The British journal of dermatology.

[21]  C. Harris,et al.  Radical causes of cancer , 2003, Nature Reviews Cancer.

[22]  C. Nathan.  Specificity of a third kind: reactive oxygen and nitrogen intermediates in cell signaling. , 2003, The Journal of clinical investigation.

[23]  L. Marnett,et al.  Endogenous generation of reactive oxidants and electrophiles and their reactions with DNA and protein. , 2003, The Journal of clinical investigation.

[24]  K. Subbaramaiah,et al.  Cyclooxygenase 2: a molecular target for cancer prevention and treatment. , 2003, Trends in pharmacological sciences.

[25]  H. Maeda,et al.  8-Nitroguanosine formation in viral pneumonia and its implication for pathogenesis , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[26]  K. Kröncke.  Nitrosative Stress and Transcription , 2003, Biological chemistry.

[27]  M. Tang,et al.  The major lipid peroxidation product, trans-4-hydroxy-2-nonenal, preferentially forms DNA adducts at codon 249 of human p53 gene, a unique mutational hotspot in hepatocellular carcinoma. , 2002, Carcinogenesis.

[28]  Wen-Chang Chang,et al.  Involvement of reactive oxygen species in arsenite-induced downregulation of phospholipid hydroperoxide glutathione peroxidase in human epidermoid carcinoma A431 cells. , 2002, Free radical biology & medicine.

[29]  J. Shah,et al.  Cyclooxygenase‐2: A novel molecular target for the prevention and treatment of head and neck cancer , 2002, Head & neck.

[30]  A. Borchert,et al.  Regulation of enzymatic lipid peroxidation: the interplay of peroxidizing and peroxide reducing enzymes. , 2002, Free radical biology & medicine.

[31]  A. Dannenberg,et al.  A role for cyclooxygenase-2 inhibitors in the prevention and treatment of cancer. , 2002, Seminars in oncology.

[32]  Scott W. Lowe,et al.  Apoptosis A Link between Cancer Genetics and Chemotherapy , 2002, Cell.

[33]  Wen-Chang Chang,et al.  Inhibition of arachidonate metabolism in human epidermoid carcinoma a431 cells overexpressing phospholipid hydroperoxide glutathione peroxidase. , 2002, Journal of biomedical science.

[34]  Rajnish A. Gupta,et al.  Colorectal cancer prevention and treatment by inhibition of cyclooxygenase-2 , 2001, Nature Reviews Cancer.

[35]  N. Altorki,et al.  Cyclo-oxygenase 2: a pharmacological target for the prevention of cancer. , 2001, The Lancet. Oncology.

[36]  M. Benito,et al.  Activation of caspases occurs downstream from radical oxygen species production, Bcl‐xL down‐regulation, and early cytochrome C release in apoptosis induced by transforming growth factor β in rat fetal hepatocytes , 2001, Hepatology.

[37]  F. Fitzpatrick,et al.  Inflammation, carcinogenesis and cancer. , 2001, International immunopharmacology.

[38]  I. Blair.  Lipid hydroperoxide-mediated DNA damage , 2001, Experimental Gerontology.

[39]  K. Subbaramaiah,et al.  Cyclooxygenase-2: a target for the prevention and treatment of breast cancer. , 2001, Endocrine-related cancer.

[40]  J. Filep,et al.  Peroxynitrite mediates cytokine‐induced IL‐8 gene expression and production by human leukocytes , 2001, Journal of leukocyte biology.

[41]  Freya Q. Schafer,et al.  Phospholipid hydroperoxide glutathione peroxidase protects against singlet oxygen-induced cell damage of photodynamic therapy. , 2001, Free radical biology & medicine.

[42]  A. Iwamoto,et al.  Viral and cellular cytokines in AIDS-related malignant lymphomatous effusions. , 2000, Blood.

[43]  G. Bailliet,et al.  Nuclear and mitochondrial genome instability in human breast cancer. , 2000, Cancer research.

[44]  S. Zhuang,et al.  Peroxynitrite-induced apoptosis involves activation of multiple caspases in HL-60 cells. , 2000, American journal of physiology. Cell physiology.

[45]  Y. Kawamoto,et al.  4-hydroxy-2-nonenal, the end product of lipid peroxidation, is a specific inducer of cyclooxygenase-2 gene expression. , 2000, Biochemical and biophysical research communications.

[46]  H. Huang,et al.  Regulation of cyclooxygenase and 12-lipoxygenase catalysis by phospholipid hydroperoxide glutathione peroxidase in A431 cells. , 2000, Prostaglandins, leukotrienes, and essential fatty acids.

[47]  J. Jen,et al.  Facile detection of mitochondrial DNA mutations in tumors and bodily fluids. , 2000, Science.

[48]  L. Marnett,et al.  Oxyradicals and DNA damage. , 2000, Carcinogenesis.

[49]  D. Hanahan,et al.  The Hallmarks of Cancer , 2000, Cell.

[50]  E. Fosslien.  Molecular pathology of cyclooxygenase-2 in neoplasia. , 2000, Annals of clinical and laboratory science.

[51]  J. Baron,et al.  Nonsteroidal anti-inflammatory drugs and cancer prevention. , 2000, Annual review of medicine.

[52]  R. DuBois,et al.  The role of cyclooxygenases in inflammation, cancer, and development , 1999, Oncogene.

[53]  F. V. van Kuijk,et al.  Effects of mGST A4 transfection on 4-hydroxynonenal-mediated apoptosis and differentiation of K562 human erythroleukemia cells. , 1999, Archives of biochemistry and biophysics.

[54]  H. Suzuki,et al.  Inhibitory effect of phospholipid hydroperoxide glutathione peroxidase on the activity of lipoxygenases and cyclooxygenases. , 1999, Prostaglandins & other lipid mediators.

[55]  G. Kollias,et al.  Mice deficient in tumor necrosis factor-α are resistant to skin carcinogenesis , 1999, Nature Medicine.

[56]  L. Marnett,et al.  Effects of nitric oxide and nitric oxide‐derived species on prostaglandin endoperoxide synthase and prostaglandin biosynthesis , 1999, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[57]  N. Schnetz-Boutaud,et al.  Duplex DNA catalyzes the chemical rearrangement of a malondialdehyde deoxyguanosine adduct. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[58]  C C Sigman,et al.  Lipoxygenase inhibitors as potential cancer chemopreventives. , 1999, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[59]  L. Marnett.  Lipid peroxidation-DNA damage by malondialdehyde. , 1999, Mutation research.

[60]  H. Bartsch,et al.  Etheno DNA-base adducts from endogenous reactive species. , 1999, Mutation research.

[61]  T. Jabs.  Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. , 1999, Biochemical pharmacology.

[62]  S. Nishizuka,et al.  Mutations in mitochondrial control region DNA in gastric tumours of Japanese patients. , 1999, European journal of cancer.

[63]  A. Vercesi,et al.  Mitochondrial damage induced by conditions of oxidative stress. , 1999, Free radical biology & medicine.

[64]  H. Kuhn,et al.  Inverse regulation of lipid‐peroxidizing and hydroperoxyl lipid‐reducing enzymes by interleukins 4 and 13 , 1999, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[65]  K. Schnurr,et al.  Cytokine induced regulation of 15-lipoxygenase and phospholipid hydroperoxide glutathione peroxidase in mammalian cells. , 1999, Advances in experimental medicine and biology.

[66]  M. Dianzani,et al.  4-Hydroxy-2,3-nonenal as a signal for cell function and differentiation. , 1999, Acta biochimica Polonica.

[67]  Bert Vogelstein,et al.  Somatic mutations of the mitochondrial genome in human colorectal tumours , 1998, Nature Genetics.

[68]  T. Sugai,et al.  Microsatellite instability in the mitochondrial DNA of colorectal carcinomas: Evidence for mismatch repair systems in mitochondrial genome , 1998, Oncogene.

[69]  C. Bode,et al.  Induction of rat aortic smooth muscle cell growth by the lipid peroxidation product 4-hydroxy-2-nonenal. , 1998, Circulation.

[70]  I. Morita,et al.  Different substrate utilization between prostaglandin endoperoxide H synthase-1 and -2 in NIH3T3 fibroblasts. , 1998, Biochimica et biophysica acta.

[71]  N. Sata,et al.  Cytotoxicity of Peroxynitrite in Rat Pancreatic Acinar AR4–2J Cells , 1997, Pancreas.

[72]  E. Stadtman,et al.  Protein Oxidation in Aging, Disease, and Oxidative Stress* , 1997, The Journal of Biological Chemistry.

[73]  B. Ames,et al.  Oxidative Decay of DNA* , 1997, The Journal of Biological Chemistry.

[74]  L. Marnett,et al.  Mutagenicity in Escherichia coli of the major DNA adduct derived from the endogenous mutagen malondialdehyde. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[75]  K. Honn,et al.  Apoptosis of W256 carcinosarcoma cells of the monocytoid origin induced by NDGA involves lipid peroxidation and depletion of GSH: Role of 12‐lipoxygenase in regulating tumor cell survival , 1997, Journal of cellular physiology.

[76]  D. Willoughby,et al.  The codependence of angiogenesis and chronic inflammation , 1997, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[77]  B. Van Houten,et al.  Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[78]  W. Glasgow,et al.  Modulation of epidermal growth factor signal transduction by linoleic acid metabolites. , 1997, Advances in experimental medicine and biology.

[79]  K. Dhingra,et al.  Lipid peroxidation-induced putative malondialdehyde-DNA adducts in human breast tissues. , 1996, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[80]  E. Shacter,et al.  Elevated interleukin 6 is induced by prostaglandin E2 in a murine model of inflammation: possible role of cyclooxygenase-2. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[81]  F. Rodeghiero,et al.  Interleukin-15 promotes the growth of leukemic cells of patients with B-cell chronic lymphoproliferative disorders. , 1996, Blood.

[82]  D. Wallace,et al.  Novel mitochondrial DNA deletion found in a renal cell carcinoma , 1996, Genes, chromosomes & cancer.

[83]  T. Naoe,et al.  In vitro studies on cellular and molecular mechanisms of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia: As2O3 induces NB4 cell apoptosis with downregulation of Bcl-2 expression and modulation of PML-RAR alpha/PML proteins. , 1996, Blood.

[84]  H. Ohshima,et al.  Formation of 8-nitroguanine by the reaction of guanine with peroxynitrite in vitro. , 1995, Carcinogenesis.

[85]  S. Kawanishi,et al.  Oxidative DNA damage induced by simultaneous generation of nitric oxide and superoxide , 1995, FEBS letters.

[86]  V. Fazio,et al.  Control of neoplastic cell proliferation and differentiation by restoration of 4-hydroxynonenal physiological concentrations. , 1993, Molecular aspects of medicine.

[87]  J. Williams,et al.  Elevation of interleukin-6 in response to a chronic inflammatory stimulus in mice: inhibition by indomethacin. , 1992, Blood.

[88]  B. Zachara.  Mammalian selenoproteins. , 1992, Journal of trace elements and electrolytes in health and disease.

[89]  H. Esterbauer,et al.  Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. , 1991, Free radical biology & medicine.

[90]  R. Metcalf,et al.  Mutational hotspot in the p53 gene in human hepatocellular carcinomas. , 1991, Nature.

[91]  J. Swenberg,et al.  Vinyl chloride-induced DNA adducts. II: Formation and persistence of 7-(2'-oxoethyl)guanine and N2,3-ethenoguanine in rat tissue DNA. , 1990, Carcinogenesis.

[92]  J. Minna,et al.  p53: a frequent target for genetic abnormalities in lung cancer. , 1989, Science.

[93]  J. Bos,et al.  The ras gene family and human carcinogenesis. , 1988, Mutation research.

[94]  S. Dahlén,et al.  Leukotrienes and lipoxins: structures, biosynthesis, and biological effects. , 1987, Science.

[95]  E. Cadenas,et al.  Oxidative stress: damage to intact cells and organs. , 1985, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[96]  H. Sies,et al.  1 – Oxidative Stress: Introductory Remarks , 1985 .

[97]  D. Clayton.  Transcription of the mammalian mitochondrial genome. , 1984, Annual review of biochemistry.

[98]  T. Slaga,et al.  Effects of tumor promoters and steroidal anti-inflammatory agents on skin of newborn mice in vivo and in vitro. , 1978, Journal of the National Cancer Institute.

[99]  J. Griffith,et al.  Association of a protein structure of probable membrane derivation with HeLa cell mitochondrial DNA near its origin of replication. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[100]  W. Pryor,et al.  Letter: A suggested mechanism for the production of malonaldehyde during the autoxidation of polyunsaturated fatty acids. Nonenzymatic production of prostaglandin endoperoxides during autoxidation. , 1975, The Journal of organic chemistry.

[101]  I. M. Neiman,et al.  [Inflammation and cancer]. , 1974, Patologicheskaia fiziologiia i eksperimental'naia terapiia.

[102]  R. Soberman,et al.  Specificity of a third kind : reactive oxygen and nitrogen intermediates in cell signaling , 2022 .