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Evaluation of metabolic reactivity in macrophages from mice with chronic sodium arsenite intake and experimental carcinogenesis
Corresponding Author(s) : Mónica A Palmieri
Cellular and Molecular Biology,
Vol. 64 No. 10: Issue 10
Abstract
Arsenic is carcinogenic to human beings, and environmental exposure to arsenic is a public health issue that affects large populations around the world. Thus, studies are needed to determine the mode of action of arsenic and to prevent harmful effects that arise from arsenic intake. In particular, knowledge of the effects of arsenic exposure in individuals who are undergoing a carcinogenesis process is lacking. The present study was performed in mice to evaluate the effect of chronic As3+ administration on peritoneal and alveolar macrophages; the As3+ was administered in drinking water over 9 months and there was a two-stage carcinogenesis process. At the end of the experiment, the number of tumors stabilized to below the control values, but the tumors showed increased malignancy. Our objective was to evaluate the systemic effects of chronic As3+ingestion in a population of macrophages that was derived from the peritoneal cavity and the broncho-alveolar trunk of cancerized mice since they are the first line of defense in the immune system. The results showed that the macrophages under all conditions retained their ability to self-regulate their metabolic reactivity. This feature was more evident in peritoneal macrophages than in alveolar macrophages. Furthermore, an increase in the number of macrophages from animals receiving higher doses of As3+ compared to untreated animals was observed. These findings indicate that certain parameters associated with two-stage skin carcinogenesis are modified by the presence of As3+ in drinking water.
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- Chilvers DC, Peterson J. Global Cycling of Arsenic. In: Lead, Mercury, Cadmium and Arsenic in the Environment. Hutchinson TC y Meema KM (eds.). Published by John Wiley & Sons Ltd., 1987; p 289.
- EPA (U.S. Environmental Protection Agency). Special Report on Inorganic Arsenic: Skin Cancer; Nutritional Essentiality. EPA 1988; 625/387/013.
- National Academy of Sciences, Washington DE. Biological Effect of Environmental Pollutants, 1977; 21-23.
- Chen CJ, Chiou HY, Huang WI, Chen SY, Hsueh YM, Tseng CH, Lin LJ, Shyu MP, Lai MS. Systemic non-carcinogenic effects and developmental toxicity of inorganic arsenic. In: Abernathy CO, Calderon RL, Chappell WR (Eds.), Arsenic Exposure and Health Effects, vol. 11. Chapman&Hall, London, 1997; pp.124–34.
- Tseng WP. Effects and dose-response relationship of skin cancer and Blackfoot disease with arsenic. Environmental Health Perspectives, 1977; 19: 109-19.
- Dakeishi M, Murata K, Grandjean P. Long-term consequences of arsenic poisoning during infancy due to contaminated milk powder. Environmental Health, 2006; 5(1): 31-7.
- von Ehrenstein OS, GuhaMazumder DN, Yuan Y, Samanta S, Balmes J, Sil A, Ghosh N, Hira-Smith M, Haque R, Purushothamam R, Lahiri S, Das S, Smith AH. Decrements in Lung Function Related to Arsenic in Drinking Water in West Bengal, India. American Journal of Epidemiology, 2005; 162(6): 533–41.
- Flora SJ. Arsenic-induced oxidative stress and its reversibility following combined administration of N-acetylcysteine and meso 2,3-dimercaptosuccinic acid in rats. Clinical and Experimental Pharmacology and Physiology, 1999; 26: 865–69.
- Pi J, Yamauchi H, Kumagai Y, Sun G, Yoshida T, Aikawa H, Hopenhayn-Rich C, Shimojo N. Evidence for induction of oxidative stress caused by chronic exposure of Chinese residents to arsenic contained in drinking water. Environmental Health Perspectives, 2002; 110: 331–36.
- Lee TC, Tanaka N, Lamb PW, Gilmer TM, Barrett JC. Induction of gene amplification by arsenic. Science, 1988; 241: 79–81.
- Mahata J, Basu A, Ghoshal S, Sarkar JN, Roy AK, Poddar G, Nandy AK, Banerjee A, Ray K, Natarajan AT, Nilsson R, Giri AK. Chromosomal aberrations and sister chromatid exchanges in individuals exposed to arsenic through drinking water in West Bengal, India.Mutation Research, 2003; 34: 133–43.
- Sakurai T, Ohta T, Fujiwara K. Inorganic arsenite alters macrophage generation from human peripheral blood monocytes. Toxicology and Applied Pharmacology, 2005; 203(2):145-53.
- Lemarie A, Morzadec C, Bourdonnay E, Fardel O, Vernhet L. Human Macrophages Constitute Targets for Immunotoxic Inorganic Arsenic. Journal of Immunology, 2006; 177:3019-3027
- Baggiolini M, Boulay F, Badwey JA, Curnutte JT. Activation of neutrophil leukocytes: chemoattactant receptors and respiratory burst. Journal of the Federation of American Societies for Experimental Biology (FASEB J), 1993; 7: 1004–10.
- Byung PL. Cellular defenses against damage from reactive oxygen species. Physiological Reviews, 1994; 74: 139–62.
- Hakim J. Reactive oxygenspecies and inflammation.ComptesRendus des Seances de la Societe de Biologie et de Ses Filiales, 1993; 187(3): 286-95.
- Forman HJ, Torres M. Redox signaling in macrophages. Molecular aspects of medicine, 2001; 22(4–5): 189–216.
- Peters SP, Cerasoli F, Albertine KH, Gee MH, Berd D, Ishihara Y. "Autoregulation” of human neutrophil activation in vitro: regulation of phorbolmyristate acetate-induced neutrophil activation by cell density. Journal of Leukocyte Biology, 1990; 47: 457–74.
- Fernández ML, Durán HA, O´Connor SE, Cabrini RL, Molinari BL. Role of distinct subpopulations of peritoneal macrophages in the regulation of reactive oxygen species release. Free Radical Biology & Medicine, 1999; 27(7/8): 797–809.
- Yuspa SH, Morgan DL. Mouse skin cells resistant to terminal differentiation associated with initiation of carcinogenesis. Nature, 1981; 293: 72-4.
- Nesnow S, Triplett LL, Slaga TJ. Mouse skin tumor initiation-promotion and complete carcinogenesis bioassays: mechanisms and biological activities of emission samples. Environmental Health Perspectives, 1983; 47: 255–68.
- Balmain A, Ramsden M, Bowden GT, Smith J. Activation of the mouse cellular Harvey-ras gene in chemically induced benign skin papillomas. Nature, 1984; 307: 658-60.
- Palmieri MA, Molinari BL. Effect of Sodium Arsenite on Mouse Skin Carcinogenesis. Toxicologic Pathology, 2015; 43: 704-714.
- Slaga TJ. SENCAR mouse skin tumorigenesis model versus other strains and stocks of mice. Environ Health Perspect, 1986; 68, 27–32.
- NIH, National Institutes of Health USA. Guide for the care and use of laboratory animals; 1996.
- Hennings H, Shores R, Mitchell P, Spangler EF, Yuspa SH. Induction of papillomas with a high probability of conversión to malignancy. Carcinogenesis, 1985; 6: 1607–10.
- Tasat DR, de Rey BM. Cytotoxic effect of uranium dioxide on rat alveolar macrophages. Environmental Research, 1987; 44: 71–81.
- Segal AW. Nitroblue-tetrazoliumtests. Lancet, 1974; 2,1248–1252.
- Molinari BL, Tasat DR, Fernández ML, Durán HA, Curiale J, Stoliar A, Cabrini RL. Automated image analysis for monitoring oxidative burst in macrophages. Analytical and Quantitative. Cytology and Histology, 2000; 22: 423–27.
- Hu J, Fang J, Dong Y, Chen SJ, Chen Z: Arsenic in cancer therapy. Anti-Cancer Drugs, 2005; 16: 119–27.
- Cheung WM, Chu PW, Kwong YL. Effects of arsenic trioxide on the cellular proliferation, apoptosis and differentiation of human neuroblastoma cells. Cancer Letters, 2007; 246(1-2): 122-28.
- Zhang XW, Yan XJ, Zhou ZR, Yang FF, Wu ZY, Sun HB, Liang WX, Song AX, Lallemand-Breitenbach V, Jeanne M, Zhang QY, Yang HY, Huang QH, Zhou GB, Tong JH, Zhang Y, Wu JH, Hu HY, Thé H, Chen SJ, Chen Z: Arsenic Trioxide Controls the Fate of the PML-RARαOncoprotein by Directly Binding PML. Science, 2010; 328: 240-43.
- Bishayi B, Sengupta M. Intracellular survival of Staphylococcus aureusdue to alteration of cellular activity in arsenic and leadintoxicated mature Swiss albino mice. Toxicology, 2003; 184: 31–39.
- Guth AM, Janssen WJ, Bosio CM, Crouch EC, Henson PM, Dow SW. Lung environment determines unique phenotype of alveolar macrophages. American Journal of Physiology-Lung Cellular and Molecular Physiology, 2009; 296(6): L936–L946.
- Müller F, Rollag H, Froland SS. Nitro blue tetrazolium reduction inmonocytes and monocyte derived macrophages. Effect of oxidative burst stimulants and interferons. ActaPathologica, Microbiologica, etImmunologicaScandinavica (APMIS), 1989; 97(6): 490–96.
- Maus UA, Janzen S, Wall G, Srivastava M, Blackwell TS, Christman JW, Seeger W, Welte T, Lohmeyer J. Resident alveolar macrophages are replaced by recruited monocytes in response to endotoxin-induced lung inflammation. American Journal of Respiratory Cell and Molecular Biology, 2006; 35: 227–35.
- Yoon HL, Marcus CB, Pfeifer RW. Induction of superoxide by 12-O-tetradecanoylphorbol-13-acetate and thapsigargin, a nonphorbol-ester-type tumor promoter, in peritoneal macrophages elicited from SenCar and B6C3F1 mice: a permissive role for the arachidonic acid cascade in signal transduction. Molecular Carcinogenesis, 1993; 7:116–125.
- Clutton SM, Townsend KMS, Walker C, Ansell JD, Wright EG. Radiation-induced genomic instability and persisting oxidative stress in primary bone marrow cultures. Carcinogenesis, 1996; 17:1633–39.
References
Chilvers DC, Peterson J. Global Cycling of Arsenic. In: Lead, Mercury, Cadmium and Arsenic in the Environment. Hutchinson TC y Meema KM (eds.). Published by John Wiley & Sons Ltd., 1987; p 289.
EPA (U.S. Environmental Protection Agency). Special Report on Inorganic Arsenic: Skin Cancer; Nutritional Essentiality. EPA 1988; 625/387/013.
National Academy of Sciences, Washington DE. Biological Effect of Environmental Pollutants, 1977; 21-23.
Chen CJ, Chiou HY, Huang WI, Chen SY, Hsueh YM, Tseng CH, Lin LJ, Shyu MP, Lai MS. Systemic non-carcinogenic effects and developmental toxicity of inorganic arsenic. In: Abernathy CO, Calderon RL, Chappell WR (Eds.), Arsenic Exposure and Health Effects, vol. 11. Chapman&Hall, London, 1997; pp.124–34.
Tseng WP. Effects and dose-response relationship of skin cancer and Blackfoot disease with arsenic. Environmental Health Perspectives, 1977; 19: 109-19.
Dakeishi M, Murata K, Grandjean P. Long-term consequences of arsenic poisoning during infancy due to contaminated milk powder. Environmental Health, 2006; 5(1): 31-7.
von Ehrenstein OS, GuhaMazumder DN, Yuan Y, Samanta S, Balmes J, Sil A, Ghosh N, Hira-Smith M, Haque R, Purushothamam R, Lahiri S, Das S, Smith AH. Decrements in Lung Function Related to Arsenic in Drinking Water in West Bengal, India. American Journal of Epidemiology, 2005; 162(6): 533–41.
Flora SJ. Arsenic-induced oxidative stress and its reversibility following combined administration of N-acetylcysteine and meso 2,3-dimercaptosuccinic acid in rats. Clinical and Experimental Pharmacology and Physiology, 1999; 26: 865–69.
Pi J, Yamauchi H, Kumagai Y, Sun G, Yoshida T, Aikawa H, Hopenhayn-Rich C, Shimojo N. Evidence for induction of oxidative stress caused by chronic exposure of Chinese residents to arsenic contained in drinking water. Environmental Health Perspectives, 2002; 110: 331–36.
Lee TC, Tanaka N, Lamb PW, Gilmer TM, Barrett JC. Induction of gene amplification by arsenic. Science, 1988; 241: 79–81.
Mahata J, Basu A, Ghoshal S, Sarkar JN, Roy AK, Poddar G, Nandy AK, Banerjee A, Ray K, Natarajan AT, Nilsson R, Giri AK. Chromosomal aberrations and sister chromatid exchanges in individuals exposed to arsenic through drinking water in West Bengal, India.Mutation Research, 2003; 34: 133–43.
Sakurai T, Ohta T, Fujiwara K. Inorganic arsenite alters macrophage generation from human peripheral blood monocytes. Toxicology and Applied Pharmacology, 2005; 203(2):145-53.
Lemarie A, Morzadec C, Bourdonnay E, Fardel O, Vernhet L. Human Macrophages Constitute Targets for Immunotoxic Inorganic Arsenic. Journal of Immunology, 2006; 177:3019-3027
Baggiolini M, Boulay F, Badwey JA, Curnutte JT. Activation of neutrophil leukocytes: chemoattactant receptors and respiratory burst. Journal of the Federation of American Societies for Experimental Biology (FASEB J), 1993; 7: 1004–10.
Byung PL. Cellular defenses against damage from reactive oxygen species. Physiological Reviews, 1994; 74: 139–62.
Hakim J. Reactive oxygenspecies and inflammation.ComptesRendus des Seances de la Societe de Biologie et de Ses Filiales, 1993; 187(3): 286-95.
Forman HJ, Torres M. Redox signaling in macrophages. Molecular aspects of medicine, 2001; 22(4–5): 189–216.
Peters SP, Cerasoli F, Albertine KH, Gee MH, Berd D, Ishihara Y. "Autoregulation” of human neutrophil activation in vitro: regulation of phorbolmyristate acetate-induced neutrophil activation by cell density. Journal of Leukocyte Biology, 1990; 47: 457–74.
Fernández ML, Durán HA, O´Connor SE, Cabrini RL, Molinari BL. Role of distinct subpopulations of peritoneal macrophages in the regulation of reactive oxygen species release. Free Radical Biology & Medicine, 1999; 27(7/8): 797–809.
Yuspa SH, Morgan DL. Mouse skin cells resistant to terminal differentiation associated with initiation of carcinogenesis. Nature, 1981; 293: 72-4.
Nesnow S, Triplett LL, Slaga TJ. Mouse skin tumor initiation-promotion and complete carcinogenesis bioassays: mechanisms and biological activities of emission samples. Environmental Health Perspectives, 1983; 47: 255–68.
Balmain A, Ramsden M, Bowden GT, Smith J. Activation of the mouse cellular Harvey-ras gene in chemically induced benign skin papillomas. Nature, 1984; 307: 658-60.
Palmieri MA, Molinari BL. Effect of Sodium Arsenite on Mouse Skin Carcinogenesis. Toxicologic Pathology, 2015; 43: 704-714.
Slaga TJ. SENCAR mouse skin tumorigenesis model versus other strains and stocks of mice. Environ Health Perspect, 1986; 68, 27–32.
NIH, National Institutes of Health USA. Guide for the care and use of laboratory animals; 1996.
Hennings H, Shores R, Mitchell P, Spangler EF, Yuspa SH. Induction of papillomas with a high probability of conversión to malignancy. Carcinogenesis, 1985; 6: 1607–10.
Tasat DR, de Rey BM. Cytotoxic effect of uranium dioxide on rat alveolar macrophages. Environmental Research, 1987; 44: 71–81.
Segal AW. Nitroblue-tetrazoliumtests. Lancet, 1974; 2,1248–1252.
Molinari BL, Tasat DR, Fernández ML, Durán HA, Curiale J, Stoliar A, Cabrini RL. Automated image analysis for monitoring oxidative burst in macrophages. Analytical and Quantitative. Cytology and Histology, 2000; 22: 423–27.
Hu J, Fang J, Dong Y, Chen SJ, Chen Z: Arsenic in cancer therapy. Anti-Cancer Drugs, 2005; 16: 119–27.
Cheung WM, Chu PW, Kwong YL. Effects of arsenic trioxide on the cellular proliferation, apoptosis and differentiation of human neuroblastoma cells. Cancer Letters, 2007; 246(1-2): 122-28.
Zhang XW, Yan XJ, Zhou ZR, Yang FF, Wu ZY, Sun HB, Liang WX, Song AX, Lallemand-Breitenbach V, Jeanne M, Zhang QY, Yang HY, Huang QH, Zhou GB, Tong JH, Zhang Y, Wu JH, Hu HY, Thé H, Chen SJ, Chen Z: Arsenic Trioxide Controls the Fate of the PML-RARαOncoprotein by Directly Binding PML. Science, 2010; 328: 240-43.
Bishayi B, Sengupta M. Intracellular survival of Staphylococcus aureusdue to alteration of cellular activity in arsenic and leadintoxicated mature Swiss albino mice. Toxicology, 2003; 184: 31–39.
Guth AM, Janssen WJ, Bosio CM, Crouch EC, Henson PM, Dow SW. Lung environment determines unique phenotype of alveolar macrophages. American Journal of Physiology-Lung Cellular and Molecular Physiology, 2009; 296(6): L936–L946.
Müller F, Rollag H, Froland SS. Nitro blue tetrazolium reduction inmonocytes and monocyte derived macrophages. Effect of oxidative burst stimulants and interferons. ActaPathologica, Microbiologica, etImmunologicaScandinavica (APMIS), 1989; 97(6): 490–96.
Maus UA, Janzen S, Wall G, Srivastava M, Blackwell TS, Christman JW, Seeger W, Welte T, Lohmeyer J. Resident alveolar macrophages are replaced by recruited monocytes in response to endotoxin-induced lung inflammation. American Journal of Respiratory Cell and Molecular Biology, 2006; 35: 227–35.
Yoon HL, Marcus CB, Pfeifer RW. Induction of superoxide by 12-O-tetradecanoylphorbol-13-acetate and thapsigargin, a nonphorbol-ester-type tumor promoter, in peritoneal macrophages elicited from SenCar and B6C3F1 mice: a permissive role for the arachidonic acid cascade in signal transduction. Molecular Carcinogenesis, 1993; 7:116–125.
Clutton SM, Townsend KMS, Walker C, Ansell JD, Wright EG. Radiation-induced genomic instability and persisting oxidative stress in primary bone marrow cultures. Carcinogenesis, 1996; 17:1633–39.