Skip to main content
Top
Published in: Breast Cancer Research 5/2001

01-10-2001 | Review

Hypoxia and oxidative stress in breast cancer Oxidative stress - its effects on the growth, metastatic potential and response to therapy of breast cancer

Authors: Nicholas S Brown, Roy Bicknell

Published in: Breast Cancer Research | Issue 5/2001

Login to get access

Abstract

Reactive oxygen species (ROS) damage DNA, but the role of ROS in breast carcinoma may not be limited to the mutagenic activity that drives carcinoma initiation and progression. Carcinoma cells in vitro and in vivo are frequently under persistent oxidative stress. In the present review, we outline potential causes of oxygen radical generation within carcinoma cells and explore the possible impact of oxidative stress on the clinical outcome of breast carcinoma.
Literature
1.
go back to reference Wiseman H, Halliwell B: Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem J. 1996, 313: 17-29.CrossRefPubMedPubMedCentral Wiseman H, Halliwell B: Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem J. 1996, 313: 17-29.CrossRefPubMedPubMedCentral
2.
go back to reference Szatrowski TP, Nathan CF: Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 1991, 51: 794-798.PubMed Szatrowski TP, Nathan CF: Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 1991, 51: 794-798.PubMed
3.
go back to reference Toyokuni S, Okamoto K, Yodoi J, Hiai H: Persistent oxidative stress in cancer. FEBS Lett. 1995, 358: 1-3. 10.1016/0014-5793(94)01368-B.CrossRefPubMed Toyokuni S, Okamoto K, Yodoi J, Hiai H: Persistent oxidative stress in cancer. FEBS Lett. 1995, 358: 1-3. 10.1016/0014-5793(94)01368-B.CrossRefPubMed
4.
go back to reference Portakal O, Ozkaya O, Erden Inal M, Bozan B, Kosan M, Sayek I: Coenzyme Q10 concentrations and antioxidant status in tissues of breast cancer patients. Clin Biochem. 2000, 33: 279-284. 10.1016/S0009-9120(00)00067-9.CrossRefPubMed Portakal O, Ozkaya O, Erden Inal M, Bozan B, Kosan M, Sayek I: Coenzyme Q10 concentrations and antioxidant status in tissues of breast cancer patients. Clin Biochem. 2000, 33: 279-284. 10.1016/S0009-9120(00)00067-9.CrossRefPubMed
5.
go back to reference Sundaresan M, Yu Z-X, Ferrans VJ, Sulciner DJ, Gutkind JS, Irani K, Goldschmidt-Clermont PJ, Finkel T: Regulation of reactive-oxygen-species generation in fibroblasts by Rac1. Biochem J. 318: 379-382. Sundaresan M, Yu Z-X, Ferrans VJ, Sulciner DJ, Gutkind JS, Irani K, Goldschmidt-Clermont PJ, Finkel T: Regulation of reactive-oxygen-species generation in fibroblasts by Rac1. Biochem J. 318: 379-382.
6.
go back to reference Brown NS, Jones A, Fujiyama C, Harris AL, Bicknell R: Thymidine phosphorylase induces carcinoma cell oxidative stress and promotes secretion of angiogenic factors. Cancer Res. 2000, 60: 6298-6302.PubMed Brown NS, Jones A, Fujiyama C, Harris AL, Bicknell R: Thymidine phosphorylase induces carcinoma cell oxidative stress and promotes secretion of angiogenic factors. Cancer Res. 2000, 60: 6298-6302.PubMed
7.
go back to reference Sipe HJ, Jordan SJ, Hanna PM, Mason RP: The metabolism of 17 beta-estradiol by lactoperoxidase: a possible source of oxidative stress in breast cancer. Carcinogenesis. 1994, 15: 2637-2643.CrossRefPubMed Sipe HJ, Jordan SJ, Hanna PM, Mason RP: The metabolism of 17 beta-estradiol by lactoperoxidase: a possible source of oxidative stress in breast cancer. Carcinogenesis. 1994, 15: 2637-2643.CrossRefPubMed
8.
go back to reference Spitz DR, Sim JE, Ridnour LA, Galoforo SS, Lee YJ: Glucose deprivation-induced oxidative stress in human tumor cells. A fundamental defect in metabolism?. Ann N Y Acad Sci. 2000, 899: 349-362.CrossRefPubMed Spitz DR, Sim JE, Ridnour LA, Galoforo SS, Lee YJ: Glucose deprivation-induced oxidative stress in human tumor cells. A fundamental defect in metabolism?. Ann N Y Acad Sci. 2000, 899: 349-362.CrossRefPubMed
9.
go back to reference Lee YJ, Galoforo SS, Berns CM, Chen JC, Davis BH, Sim JE, Corry PM, Spitz DR: Glucose deprivation-induced cytotoxicity and alterations in mitogen-activated protein kinase activation are mediated by oxidative stress in multidrug-resistant human breast carcinoma cells. J Biol Chem. 1998, 273: 5294-5299. 10.1074/jbc.273.9.5294.CrossRefPubMed Lee YJ, Galoforo SS, Berns CM, Chen JC, Davis BH, Sim JE, Corry PM, Spitz DR: Glucose deprivation-induced cytotoxicity and alterations in mitogen-activated protein kinase activation are mediated by oxidative stress in multidrug-resistant human breast carcinoma cells. J Biol Chem. 1998, 273: 5294-5299. 10.1074/jbc.273.9.5294.CrossRefPubMed
10.
go back to reference Kundu N, Zhang S, Fulton AM: Sublethal oxidative stress inhibits tumor cell adhesion and enhances experimental metastasis of murine mammary carcinoma. Clin Exp Metastasis. 1995, 13: 16-22.CrossRefPubMed Kundu N, Zhang S, Fulton AM: Sublethal oxidative stress inhibits tumor cell adhesion and enhances experimental metastasis of murine mammary carcinoma. Clin Exp Metastasis. 1995, 13: 16-22.CrossRefPubMed
11.
go back to reference Fulton AM, Chong YC: The role of macrophage-derived TNFα in the induction of sublethal tumor cell DNA damage. Carcinogenesis. 1992, 13: 77-81.CrossRefPubMed Fulton AM, Chong YC: The role of macrophage-derived TNFα in the induction of sublethal tumor cell DNA damage. Carcinogenesis. 1992, 13: 77-81.CrossRefPubMed
12.
go back to reference Yokomizo A, Ono M, Nanri H, Makino Y, Ohga T, Wada M, Okamoto T, Yodoi J, Kuwano M, Kohno K: Cellular levels of thioredoxin associated with drug sensitivity to cisplatin, mitomycin C, doxorubicin, and etoposide. Cancer Res. 1995, 55: 4293-4296.PubMed Yokomizo A, Ono M, Nanri H, Makino Y, Ohga T, Wada M, Okamoto T, Yodoi J, Kuwano M, Kohno K: Cellular levels of thioredoxin associated with drug sensitivity to cisplatin, mitomycin C, doxorubicin, and etoposide. Cancer Res. 1995, 55: 4293-4296.PubMed
13.
go back to reference Ferlini C, Scambia G, Marone M, Distefano M, Gaggini C, Ferrandina G, Fattorossi A, Isola G, Benedetti Panici P, Mancuso S: Tamoxifen induces oxidative stress and apoptosis in oestrogen receptor-negative human cancer cell lines. Br J Cancer. 1999, 79: 257-263.CrossRefPubMedPubMedCentral Ferlini C, Scambia G, Marone M, Distefano M, Gaggini C, Ferrandina G, Fattorossi A, Isola G, Benedetti Panici P, Mancuso S: Tamoxifen induces oxidative stress and apoptosis in oestrogen receptor-negative human cancer cell lines. Br J Cancer. 1999, 79: 257-263.CrossRefPubMedPubMedCentral
14.
go back to reference Burdon RH: Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radic Biol Med. 1995, 18: 775-794. 10.1016/0891-5849(94)00198-S.CrossRefPubMed Burdon RH: Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radic Biol Med. 1995, 18: 775-794. 10.1016/0891-5849(94)00198-S.CrossRefPubMed
15.
go back to reference Wang X, Martindale JL, Liu Y, Holbrook NJ: The cellular response to oxidative stress: influences of mitogen-activated protein kinase signalling pathways on cell survival. Biochem J. 1998, 333: 291-300.CrossRefPubMedPubMedCentral Wang X, Martindale JL, Liu Y, Holbrook NJ: The cellular response to oxidative stress: influences of mitogen-activated protein kinase signalling pathways on cell survival. Biochem J. 1998, 333: 291-300.CrossRefPubMedPubMedCentral
16.
go back to reference Schiff R, Reddy P, Ahotupa M, Coronado-Heinsohn E, Grim M, Hilsenbeck SG, Lawrence R, Deneke S, Herrera R, Chamness GC, Fuqua SA, Brown PH, Osborne CK: Oxidative stress and AP-1 activity in tamoxifen-resistant breast tumors in vivo. J Natl Cancer Inst. 2000, 92: 1926-1934. 10.1093/jnci/92.23.1926.CrossRefPubMed Schiff R, Reddy P, Ahotupa M, Coronado-Heinsohn E, Grim M, Hilsenbeck SG, Lawrence R, Deneke S, Herrera R, Chamness GC, Fuqua SA, Brown PH, Osborne CK: Oxidative stress and AP-1 activity in tamoxifen-resistant breast tumors in vivo. J Natl Cancer Inst. 2000, 92: 1926-1934. 10.1093/jnci/92.23.1926.CrossRefPubMed
17.
go back to reference Irani K, Xia Y, Zweier JL, Sollott SJ, Der CJ, Fearon ER, Sundaresan M, Finkel T, Goldschmidt-Clermont PJ: Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science. 1997, 275: 1649-1652. 10.1126/science.275.5306.1649.CrossRefPubMed Irani K, Xia Y, Zweier JL, Sollott SJ, Der CJ, Fearon ER, Sundaresan M, Finkel T, Goldschmidt-Clermont PJ: Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science. 1997, 275: 1649-1652. 10.1126/science.275.5306.1649.CrossRefPubMed
18.
go back to reference Yin Y, Solomon G, Deng C, Barrett JC: Differential regulation of p21 by p53 and Rb in cellular response to oxidative stress. Mol Carcinog. 1999, 24: 15-24. 10.1002/(SICI)1098-2744(199901)24:1<15::AID-MC3>3.3.CO;2-P.CrossRefPubMed Yin Y, Solomon G, Deng C, Barrett JC: Differential regulation of p21 by p53 and Rb in cellular response to oxidative stress. Mol Carcinog. 1999, 24: 15-24. 10.1002/(SICI)1098-2744(199901)24:1<15::AID-MC3>3.3.CO;2-P.CrossRefPubMed
19.
go back to reference Lazo JS, Kuo SM, Woo ES, Pitt BR: The protein thiol metallothionein as an antioxidant and protectant against antineoplastic drugs. Chem Biol Interact. 1998, 111-112: 255-262. 10.1016/S0009-2797(97)00165-8.CrossRefPubMed Lazo JS, Kuo SM, Woo ES, Pitt BR: The protein thiol metallothionein as an antioxidant and protectant against antineoplastic drugs. Chem Biol Interact. 1998, 111-112: 255-262. 10.1016/S0009-2797(97)00165-8.CrossRefPubMed
21.
go back to reference Shaw M, Cohen P, Alessi DR: The activation of protein kinase B by H2O2 or heat shock is mediated by phosphoinositide 3-kinase and not by mitogen-activated protein kinase-activated protein kinase-2. Biochem J. 1998, 336: 241-246.CrossRefPubMedPubMedCentral Shaw M, Cohen P, Alessi DR: The activation of protein kinase B by H2O2 or heat shock is mediated by phosphoinositide 3-kinase and not by mitogen-activated protein kinase-activated protein kinase-2. Biochem J. 1998, 336: 241-246.CrossRefPubMedPubMedCentral
22.
go back to reference Ziemann C, Burkle A, Kahl GF, Hirsch-Ernst KI: Reactive oxygen species participate in mdr1b mRNA and P-glycoprotein over-expression in primary rat hepatocyte cultures. Carcinogenesis. 1999, 20: 407-414. 10.1093/carcin/20.3.407.CrossRefPubMed Ziemann C, Burkle A, Kahl GF, Hirsch-Ernst KI: Reactive oxygen species participate in mdr1b mRNA and P-glycoprotein over-expression in primary rat hepatocyte cultures. Carcinogenesis. 1999, 20: 407-414. 10.1093/carcin/20.3.407.CrossRefPubMed
23.
go back to reference Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez AM, Schumacker PT: Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1α during hypoxia: a mechanism of O2 sensing. J Biol Chem. 2000, 275: 25130-25138. 10.1074/jbc.M001914200.CrossRefPubMed Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez AM, Schumacker PT: Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1α during hypoxia: a mechanism of O2 sensing. J Biol Chem. 2000, 275: 25130-25138. 10.1074/jbc.M001914200.CrossRefPubMed
24.
go back to reference Richard DE, Berra E, Pouyssegur J: Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1α in vascular smooth muscle cells. J Biol Chem. 2000, 275: 26765-26771.PubMed Richard DE, Berra E, Pouyssegur J: Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1α in vascular smooth muscle cells. J Biol Chem. 2000, 275: 26765-26771.PubMed
25.
go back to reference Milligan SA, Owens MW, Grisham MB: Augmentation of cytokine-induced nitric oxide synthesis by hydrogen peroxide. Am J Physiol. 1996, 271: L114-L120.PubMed Milligan SA, Owens MW, Grisham MB: Augmentation of cytokine-induced nitric oxide synthesis by hydrogen peroxide. Am J Physiol. 1996, 271: L114-L120.PubMed
26.
go back to reference Huot J, Houle F, Marceau F, Landry J: Oxidative stress-induced actin reorganization mediated by the p38 mitogen-activated protein kinase/heat shock protein 27 pathway in vascular endothelial cells. Circ Res. 1997, 80: 383-392.CrossRefPubMed Huot J, Houle F, Marceau F, Landry J: Oxidative stress-induced actin reorganization mediated by the p38 mitogen-activated protein kinase/heat shock protein 27 pathway in vascular endothelial cells. Circ Res. 1997, 80: 383-392.CrossRefPubMed
27.
go back to reference Rust W, Kingsley K, Petnicki T, Padmanabhan S, Carper SW, Plopper GE: Heat shock protein 27 plays two distinct roles in controlling human breast cancer cell migration on laminin-5. Mol Cell Biol Res Commun. 1999, 1: 196-202. 10.1006/mcbr.1999.0130.CrossRefPubMed Rust W, Kingsley K, Petnicki T, Padmanabhan S, Carper SW, Plopper GE: Heat shock protein 27 plays two distinct roles in controlling human breast cancer cell migration on laminin-5. Mol Cell Biol Res Commun. 1999, 1: 196-202. 10.1006/mcbr.1999.0130.CrossRefPubMed
28.
go back to reference Moldovan L, Irani K, Moldovan NI, Finkel T, Goldschmidt-Clermont PJ: The actin cytoskeleton reorganization induced by Rac1 requires the production of superoxide. Antiox Redox Signal. 1999, 1: 29-43.CrossRef Moldovan L, Irani K, Moldovan NI, Finkel T, Goldschmidt-Clermont PJ: The actin cytoskeleton reorganization induced by Rac1 requires the production of superoxide. Antiox Redox Signal. 1999, 1: 29-43.CrossRef
29.
go back to reference Duffy MJ, Maguire TM, Hill A, McDermott E, O'Higgins N: Metalloproteinases: role in breast carcinogenesis, invasion and metastasis. Breast Cancer Res. 2000, 2: 252-257. 10.1186/bcr65.CrossRefPubMedPubMedCentral Duffy MJ, Maguire TM, Hill A, McDermott E, O'Higgins N: Metalloproteinases: role in breast carcinogenesis, invasion and metastasis. Breast Cancer Res. 2000, 2: 252-257. 10.1186/bcr65.CrossRefPubMedPubMedCentral
30.
go back to reference Rajagopalan S, Meng XP, Ramasamy S, Harrison DG, Galis ZS: Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability. J Clin Invest. 1996, 98: 2572-2579.CrossRefPubMedPubMedCentral Rajagopalan S, Meng XP, Ramasamy S, Harrison DG, Galis ZS: Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability. J Clin Invest. 1996, 98: 2572-2579.CrossRefPubMedPubMedCentral
31.
go back to reference Swaim MW, Pizzo SV: Methionine sulfoxide and the oxidative regulation of plasma proteinase inhibitors. J Leukoc Biol. 1988, 43: 365-379.PubMed Swaim MW, Pizzo SV: Methionine sulfoxide and the oxidative regulation of plasma proteinase inhibitors. J Leukoc Biol. 1988, 43: 365-379.PubMed
32.
go back to reference Church SL, Grant JW, Ridnour LA, Oberley LW, Swanson PE, Meltzer PS, Trent JM: Increased manganese superoxide dismutase expression suppresses the malignant phenotype of human melanoma cells. Proc Natl Acad Sci USA. 1993, 90: 3113-3117.CrossRefPubMedPubMedCentral Church SL, Grant JW, Ridnour LA, Oberley LW, Swanson PE, Meltzer PS, Trent JM: Increased manganese superoxide dismutase expression suppresses the malignant phenotype of human melanoma cells. Proc Natl Acad Sci USA. 1993, 90: 3113-3117.CrossRefPubMedPubMedCentral
Metadata
Title
Hypoxia and oxidative stress in breast cancer Oxidative stress - its effects on the growth, metastatic potential and response to therapy of breast cancer
Authors
Nicholas S Brown
Roy Bicknell
Publication date
01-10-2001
Publisher
BioMed Central
Published in
Breast Cancer Research / Issue 5/2001
Electronic ISSN: 1465-542X
DOI
https://doi.org/10.1186/bcr315

Other articles of this Issue 5/2001

Breast Cancer Research 5/2001 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine