Effects of Cigarette Smoke and Opium on the Expression of CD9, CD36, and CD68 at mRNA and Protein Levels in Human Macrophage Cell Line THP-1
-
Mohammad Amin Momeni-Moghaddam
,
Gholamreza Asadikaram
,
Mohammad Hadi Nematollahi
,
Mojdeh Esmaeili Tarzi
,
Sanaz Faramarz-Gaznagh
,
Abbas Mohammadpour-Gharehbagh
,
Mohammad Kazemi Arababadi
Abstract
Cigarette smoking and opium use are risk factors for coronary artery disease (CAD). It has been known that scavenger receptors such as CD36 and CD68 play critical roles in the pathogenesis of CAD. CD9, as a member of the tetraspanin, has been shown to interact with scavenger receptors. The aim of this study was to investigate the effects of these risk factors on expression levels of CD9, CD36, and CD68 on the THP-1 cell line. The THP-1 cell line treated with cigarette smoke extract (CSE( and opium, both individually and combinatory, in 24 h incubation. The protein and mRNA levels of CD9, CD36, and CD68 were evaluated by flow cytometry and quantitative reverse transcription-Polymerase Chain Reaction (qRT-PCR) techniques, respectively. CD36 and CD68 mRNA and protein expression levels were significantly increased in the cells treated with cigarette smoke extract compared to the control (p<0.001 in mRNA expression levels and p=0.016 and p=0.012 in protein expression levels, respectively). The CSE increased the level of CD9 protein expression compared to the control group (p=0.041) on the human macrophage cell line THP-1. No significant differences were observed in the CD9, CD36, and CD68 gene expression and at the protein levels between opium-treated THP-1 cells and controls. In conclusion, cigarettes by increasing the levels of CD36, CD68, and CD9 can be a risk factor in the development of many inflammatory diseases, including cardiovascular diseases, chronic obstructive pulmonary disease (COPD) and lung carcinoma.
1. Ambrose JA, Barua RS. The pathophysiology of cigarette smoking and cardiovascular disease: an update. Journal of the American college of cardiology. 2004;43(10):1731-7.
2. Messner B, Bernhard D. Smoking and cardiovascular disease: mechanisms of endothelial dysfunction and early atherogenesis. Arteriosclerosis, thrombosis, and vascular biology. 2014;34(3):509-15.
3. Lee J, Cooke JP. The role of nicotine in the pathogenesis of atherosclerosis. Atherosclerosis. 2011;215(2):281-3.
4. Mohammadi A, Darabi M, Nasry M, Saabet-Jahromi M-J, Malek-Pour-Afshar R, Sheibani H. Effect of opium addiction on lipid profile and atherosclerosis formation in hypercholesterolemic rabbits. Experimental and Toxicologic Pathology. 2009;61(2):145-9.
5. Karam GA, Reisi M, Kaseb AA, Khaksari M, Mohammadi A, Mahmoodi M. Effects of opium addiction on some serum factors in addicts with non‐insulin‐dependent diabetes mellitus. Addiction biology. 2004;9(1):53-8.
6. Azimzade SB, Gholamreza Y, Narooey S. A case-control study of effect of opium addiction on myocardial infarction. 2005.
7. Davoodi G, Sadeghian S, Akhondzadeh S, Darvish S, Alidoosti M, Amirzadegan A. Comparison of specifications, short term outcome and prognosis of acute myocardial infarction in opium dependent patients and nondependents. The Journal of Tehran University Heart Center. 2006;1(1):48-53.
8. Sadeghian S, Darvish S, Davoodi G, Salarifar M, Mahmoodian M, Fallah N, et al. The association of opium with coronary artery disease. European Journal of Cardiovascular Prevention & Rehabilitation. 2007;14(5):715-7.
9. Nabati S, Asadikaram G, Arababadi MK, Shahabinejad G, Rezaeian M, Mahmoodi M, et al. The plasma levels of the cytokines in opium-addicts and the effects of opium on the cytokines secretion by their lymphocytes. Immunology letters. 2013;152(1):42-6.
10. Bonaterra GA, Hildebrandt W, Bodens A, Sauer R, Dugi KA, Deigner H-P, et al. Increased gene expression of scavenger receptors and proinflammatory markers in peripheral blood mononuclear cells of hyperlipidemic males. Journal of Molecular Medicine. 2007;85(2):181-90.
11. Rice PJ, Kelley JL, Kogan G, Ensley HE, Kalbfleisch JH, Browder IW, et al. Human monocyte scavenger receptors are pattern recognition receptors for (1→ 3)‐β‐D‐glucans. Journal of leukocyte biology. 2002;72(1):140-6.
12. Marques P, Collado A, Escudero P, Rius C, González C, Servera E, et al. cigarette smoke increases endothelial cXcl16-leukocyte cXcr6 adhesion In Vitro and In Vivo. Potential consequences in chronic Obstructive Pulmonary Disease. Frontiers in immunology. 2017;8:1766.
13. Taylor PR, Martinez-Pomares L, Stacey M, Lin H-H, Brown GD, Gordon S. Macrophage receptors and immune recognition. Annu Rev Immunol. 2005;23:901-44.
14. O'Reilly D, Quinn CM, El-Shanawany T, Gordon S, Greaves DR. Multiple Ets factors and interferon regulatory factor-4 modulate CD68 expression in a cell type-specific manner. Journal of Biological Chemistry. 2003;278(24):21909-19.
15. Gough PJ, Raines EW. Gene therapy of apolipoprotein E–deficient mice using a novel macrophage-specific retroviral vector. Blood. 2003;101(2):485-91.
16. Li S, Lee C, Schindler C. Deletion of the murine scavenger receptor CD68. Journal of lipid research. 2011:jlr. M015412.
17. Kurushima H, Ramprasad M, Kondratenko N, Foster D, Quehenberger O, Steinberg D. Surface expression and rapid internalization of macrosialin (mouse CD68) on elicited mouse peritoneal macrophages. Journal of leukocyte biology. 2000;67(1):104-8.
18. Ramprasad MP, Fischer W, Witztum JL, Sambrano GR, Quehenberger O, Steinberg D. The 94-to 97-kDa mouse macrophage membrane protein that recognizes oxidized low density lipoprotein and phosphatidylserine-rich liposomes is identical to macrosialin, the mouse homologue of human CD68. Proceedings of the National Academy of Sciences. 1995;92(21):9580-4.
19. Miao W-M, Vasile E, Lane WS, Lawler J. CD36 associates with CD9 and integrins on human blood platelets. Blood. 2001;97(6):1689-96.
20. Huang W, Febbraio M, Silverstein RL. CD9 tetraspanin interacts with CD36 on the surface of macrophages: a possible regulatory influence on uptake of oxidized low density lipoprotein. PLoS One. 2011;6(12):e29092.
21. Gellner CA, Reynaga DD, Leslie FM. Cigarette smoke extract: A preclinical model of tobacco dependence. Current protocols in neuroscience. 2016;77(1):9.54.1-9.54.10.
22. Facchinetti F, Amadei F, Geppetti P, Tarantini F, Di Serio C, Dragotto A, et al. α, β-unsaturated aldehydes in cigarette smoke release inflammatory mediators from human macrophages. American journal of respiratory cell and molecular biology. 2007;37(5):617-23.
23. Walters MJ, Paul-Clark MJ, McMaster SK, Ito K, Adcock IM, Mitchell JA. Cigarette smoke activates human monocytes by an oxidant-AP-1 signaling pathway: implications for steroid resistance. Molecular pharmacology. 2005;68(5):1343-53.
24. Khaleghi M, Farsinejad A, Dabiri S, Asadikaram G. Induction of apoptosis by opium in some tumor cell lines. Cellular and Molecular Biology. 2016;62(11):76-80.
25. Nematollahi MH, Torkzadeh-Mahanai M, Pardakhty A, Ebrahimi Meimand HA, Asadikaram G. Ternary
complex of plasmid DNA with NLS-Mu-Mu protein and cationic niosome for biocompatible and efficient gene delivery: a comparative study with protamine and lipofectamine. Artificial cells, nanomedicine, and biotechnology.2018;46(8):1781-91.
26. Raeiszadeh M, Esmaeili-Tarzi M, Bahrampour-Juybari K, Nematollahi-mahani S, Pardakhty A, Nematollahi M, et al. Evaluation the effect of Myrtus communis L. extract on several underlying mechanisms involved in wound healing: An in vitro study. South African journal of botany. 2018;118:144-50.
27. Inoue T. Cigarette smoking as a risk factor of coronary artery disease and its effects on platelet function. Tobacco induced diseases. 2004;2(1):27.
28. Liu J, Liang Q, Frost-Pineda K, Muhammad-Kah R, Rimmer L, Roethig H, et al. Relationship between biomarkers of cigarette smoke exposure and biomarkers of inflammation, oxidative stress, and platelet activation in adult cigarette smokers. Cancer Epidemiology and Prevention Biomarkers. 2011.
29. Masoudkabir F, Sarrafzadegan N, Eisenberg MJ. Effects of opium consumption on cardiometabolic diseases. Nature reviews Cardiology. 2013;10(12):733.
30. Park YM. CD36, a scavenger receptor implicated in atherosclerosis. Experimental & molecular medicine. 2014;46(6):e99.
31. Fuhrman B, Volkova N, Aviram M. Oxidative stress increases the expression of the CD36 scavenger receptor and the cellular uptake of oxidized low-density lipoprotein in macrophages from atherosclerotic mice: protective role of antioxidants and of paraoxonase. Atherosclerosis. 2002;161(2):307-16.
32. Lee R, Margaritis M, M Channon K, Antoniades C. Evaluating oxidative stress in human cardiovascular disease: methodological aspects and considerations. Current medicinal chemistry. 2012;19(16): -2504-20.
33. Nsonwu-Anyanwu AC, Offor SJ, John II. Cigarette Smoke and Oxidative Stress Indices in Male Active Smokers. Reactive Oxygen Species. 2018;5(15):199–208-199–208.
34. Zhou M-S, Chadipiralla K, Mendez AJ, Jaimes EA, Silverstein RL, Webster K, et al. Nicotine potentiates proatherogenic effects of oxLDL by stimulating and upregulating macrophage CD36 signaling. American Journal of Physiology-Heart and Circulatory Physiology. 2013;305(4):H563-H74.
35. Ghazavi A, Mosayebi G, Solhi H, Rafiei M, Moazzeni SM. Serum markers of inflammation and oxidative stress in chronic opium (Taryak) smokers. Immunology letters. 2013;153(1-2):22-6.
36. Lee J, Taneja V, Vassallo R. Cigarette smoking and inflammation: cellular and molecular mechanisms. Journal of dental research. 2012;91(2):142-9.
37. Higuchi T, Omata F, Tsuchihashi K, Higashioka K, Koyamada R, Okada S. Current cigarette smoking is a reversible cause of elevated white blood cell count: Cross-sectional and longitudinal studies. Preventive medicine reports. 2016;4:417-22.
38. Tibuakuu M, Kamimura D, Kianoush S, DeFilippis AP, Al Rifai M, Reynolds LM, et al. The association between cigarette smoking and inflammation: The Genetic Epidemiology Network of Arteriopathy (GENOA) study. PLoS One. 2017;12(9):e0184914.
39. Lu Z, Li Y, Brinson CW, Kirkwood KL, Lopes‐Virella MF, Huang Y. CD 36 is upregulated in mice with periodontitis and metabolic syndrome and involved in macrophage gene upregulation by palmitate. Oral diseases. 2017;23(2):210-8.
40. Hashimoto R, Kakigi R, Nakamura K, Itoh S, Daida H, Okada T, et al. LPS enhances expression of CD204 through the MAPK/ERK pathway in murine bone marrow macrophages. Atherosclerosis. 2017;266:167-75.
41. Okamura DM, Pennathur S, Pasichnyk K, López-Guisa JM, Collins S, Febbraio M, et al. CD36 regulates oxidative stress and inflammation in hypercholesterolemic CKD. Journal of the American Society of Nephrology. 2009;20(3):495-505.
42. Liu J, Yang P, Zuo G, He S, Tan W, Zhang X, et al. Long-chain fatty acid activates hepatocytes through CD36 mediated oxidative stress. Lipids in health and disease. 2018;17(1):153.
43. Asadikaram G, Igder S, Jamali Z, Shahrokhi N, et al. Effects of Different Concentrations of Opium on the Secretion of Interleukin-6, Interferon-γ and Transforming Growth Factor Beta Cytokines from Jurkat Cells. Addiction & health. 2015;7(1-2):47.
44. Ayatollahi-Mousavi SA, Asadikaram G, Nakhaee N, Izadi A, Keikha N. The effects of opium addiction on the immune system function in patients with fungal infection. Addiction & health. 2016;8(4):218.
45. Peng X, Mosser DM, Adler MW, Rogers TJ, Meissler Jr JJ, Eisenstein TK. Morphine enhances interleukin‐12 and the production of other pro‐inflammatory cytokines in mouse peritoneal macrophages. Journal of leukocyte biology. 2000;68(5):723-8.
46. Martucci C, Franchi S, Lattuada D, Panerai AE, Sacerdote P. Differential involvement of RelB in morphine‐induced modulation of chemotaxis, NO, and cytokine production in murine macrophages and lymphocytes. Journal of leukocyte biology. 2007;81(1):344-54.
47. Chistiakov DA, Killingsworth MC, Myasoedova VA, et al. CD68/macrosialin: not just a histochemical marker. Laboratory Investigation. 2017;97(1):4.
48. Ramprasad MP, Terpstra V, Kondratenko N, Quehenberger O, Steinberg D. Cell surface expression of mouse macrosialin and human CD68 and their role as macrophage receptors for oxidized low density lipoprotein. Proceedings of the National Academy of Sciences. 1996;93(25):14833-8.
49. John G, Kohse K, Orasche J, Reda A, et al. The composition of cigarette smoke determines inflammatory cell recruitment to the lung in COPD mouse models. Clinical science. 2014;126(3):207-21.
50. Luo C, Lian X, Hong L, et al. High uric acid activates the ROS-AMPK pathway, impairs CD68 expression and inhibits OxLDL-induced foam-cell formation in a human monocytic cell line, THP-1. Cellular Physiology and Biochemistry. 2016;40(3-4):538-48.
51. Gottfried E, Kunz‐Schughart L, Weber A, Rehli M, Peuker A, Müller A, et al. Expression of CD68 in non‐myeloid cell types. Scandinavian journal of immunology. 2008;67(5):453-63.
52. Takeda Y, He P, Tachibana I, Zhou B, Miyado K, Kaneko H, et al. Double deficiency of tetraspanins CD9 and CD81 alters cell motility and protease production of macrophages and causes chronic obstructive pulmonary disease-like phenotype in mice. Journal of Biological Chemistry. 2008;283(38):26089-97.
53. Jin Y, Tachibana I, Takeda Y, He P, Kang S, Suzuki M, et al. Statins decrease lung inflammation in mice by upregulating tetraspanin CD9 in macrophages. PLoS One. 2013;8(9):e73706.
54. Desjardins S, Belkai E, Crete D, Cordonnier L, Scherrmann J-M, Noble F, et al. Effects of chronic morphine and morphine withdrawal on gene expression in rat peripheral blood mononuclear cells. Neuropharmacology. 2008;55(8):1347-54.
2. Messner B, Bernhard D. Smoking and cardiovascular disease: mechanisms of endothelial dysfunction and early atherogenesis. Arteriosclerosis, thrombosis, and vascular biology. 2014;34(3):509-15.
3. Lee J, Cooke JP. The role of nicotine in the pathogenesis of atherosclerosis. Atherosclerosis. 2011;215(2):281-3.
4. Mohammadi A, Darabi M, Nasry M, Saabet-Jahromi M-J, Malek-Pour-Afshar R, Sheibani H. Effect of opium addiction on lipid profile and atherosclerosis formation in hypercholesterolemic rabbits. Experimental and Toxicologic Pathology. 2009;61(2):145-9.
5. Karam GA, Reisi M, Kaseb AA, Khaksari M, Mohammadi A, Mahmoodi M. Effects of opium addiction on some serum factors in addicts with non‐insulin‐dependent diabetes mellitus. Addiction biology. 2004;9(1):53-8.
6. Azimzade SB, Gholamreza Y, Narooey S. A case-control study of effect of opium addiction on myocardial infarction. 2005.
7. Davoodi G, Sadeghian S, Akhondzadeh S, Darvish S, Alidoosti M, Amirzadegan A. Comparison of specifications, short term outcome and prognosis of acute myocardial infarction in opium dependent patients and nondependents. The Journal of Tehran University Heart Center. 2006;1(1):48-53.
8. Sadeghian S, Darvish S, Davoodi G, Salarifar M, Mahmoodian M, Fallah N, et al. The association of opium with coronary artery disease. European Journal of Cardiovascular Prevention & Rehabilitation. 2007;14(5):715-7.
9. Nabati S, Asadikaram G, Arababadi MK, Shahabinejad G, Rezaeian M, Mahmoodi M, et al. The plasma levels of the cytokines in opium-addicts and the effects of opium on the cytokines secretion by their lymphocytes. Immunology letters. 2013;152(1):42-6.
10. Bonaterra GA, Hildebrandt W, Bodens A, Sauer R, Dugi KA, Deigner H-P, et al. Increased gene expression of scavenger receptors and proinflammatory markers in peripheral blood mononuclear cells of hyperlipidemic males. Journal of Molecular Medicine. 2007;85(2):181-90.
11. Rice PJ, Kelley JL, Kogan G, Ensley HE, Kalbfleisch JH, Browder IW, et al. Human monocyte scavenger receptors are pattern recognition receptors for (1→ 3)‐β‐D‐glucans. Journal of leukocyte biology. 2002;72(1):140-6.
12. Marques P, Collado A, Escudero P, Rius C, González C, Servera E, et al. cigarette smoke increases endothelial cXcl16-leukocyte cXcr6 adhesion In Vitro and In Vivo. Potential consequences in chronic Obstructive Pulmonary Disease. Frontiers in immunology. 2017;8:1766.
13. Taylor PR, Martinez-Pomares L, Stacey M, Lin H-H, Brown GD, Gordon S. Macrophage receptors and immune recognition. Annu Rev Immunol. 2005;23:901-44.
14. O'Reilly D, Quinn CM, El-Shanawany T, Gordon S, Greaves DR. Multiple Ets factors and interferon regulatory factor-4 modulate CD68 expression in a cell type-specific manner. Journal of Biological Chemistry. 2003;278(24):21909-19.
15. Gough PJ, Raines EW. Gene therapy of apolipoprotein E–deficient mice using a novel macrophage-specific retroviral vector. Blood. 2003;101(2):485-91.
16. Li S, Lee C, Schindler C. Deletion of the murine scavenger receptor CD68. Journal of lipid research. 2011:jlr. M015412.
17. Kurushima H, Ramprasad M, Kondratenko N, Foster D, Quehenberger O, Steinberg D. Surface expression and rapid internalization of macrosialin (mouse CD68) on elicited mouse peritoneal macrophages. Journal of leukocyte biology. 2000;67(1):104-8.
18. Ramprasad MP, Fischer W, Witztum JL, Sambrano GR, Quehenberger O, Steinberg D. The 94-to 97-kDa mouse macrophage membrane protein that recognizes oxidized low density lipoprotein and phosphatidylserine-rich liposomes is identical to macrosialin, the mouse homologue of human CD68. Proceedings of the National Academy of Sciences. 1995;92(21):9580-4.
19. Miao W-M, Vasile E, Lane WS, Lawler J. CD36 associates with CD9 and integrins on human blood platelets. Blood. 2001;97(6):1689-96.
20. Huang W, Febbraio M, Silverstein RL. CD9 tetraspanin interacts with CD36 on the surface of macrophages: a possible regulatory influence on uptake of oxidized low density lipoprotein. PLoS One. 2011;6(12):e29092.
21. Gellner CA, Reynaga DD, Leslie FM. Cigarette smoke extract: A preclinical model of tobacco dependence. Current protocols in neuroscience. 2016;77(1):9.54.1-9.54.10.
22. Facchinetti F, Amadei F, Geppetti P, Tarantini F, Di Serio C, Dragotto A, et al. α, β-unsaturated aldehydes in cigarette smoke release inflammatory mediators from human macrophages. American journal of respiratory cell and molecular biology. 2007;37(5):617-23.
23. Walters MJ, Paul-Clark MJ, McMaster SK, Ito K, Adcock IM, Mitchell JA. Cigarette smoke activates human monocytes by an oxidant-AP-1 signaling pathway: implications for steroid resistance. Molecular pharmacology. 2005;68(5):1343-53.
24. Khaleghi M, Farsinejad A, Dabiri S, Asadikaram G. Induction of apoptosis by opium in some tumor cell lines. Cellular and Molecular Biology. 2016;62(11):76-80.
25. Nematollahi MH, Torkzadeh-Mahanai M, Pardakhty A, Ebrahimi Meimand HA, Asadikaram G. Ternary
complex of plasmid DNA with NLS-Mu-Mu protein and cationic niosome for biocompatible and efficient gene delivery: a comparative study with protamine and lipofectamine. Artificial cells, nanomedicine, and biotechnology.2018;46(8):1781-91.
26. Raeiszadeh M, Esmaeili-Tarzi M, Bahrampour-Juybari K, Nematollahi-mahani S, Pardakhty A, Nematollahi M, et al. Evaluation the effect of Myrtus communis L. extract on several underlying mechanisms involved in wound healing: An in vitro study. South African journal of botany. 2018;118:144-50.
27. Inoue T. Cigarette smoking as a risk factor of coronary artery disease and its effects on platelet function. Tobacco induced diseases. 2004;2(1):27.
28. Liu J, Liang Q, Frost-Pineda K, Muhammad-Kah R, Rimmer L, Roethig H, et al. Relationship between biomarkers of cigarette smoke exposure and biomarkers of inflammation, oxidative stress, and platelet activation in adult cigarette smokers. Cancer Epidemiology and Prevention Biomarkers. 2011.
29. Masoudkabir F, Sarrafzadegan N, Eisenberg MJ. Effects of opium consumption on cardiometabolic diseases. Nature reviews Cardiology. 2013;10(12):733.
30. Park YM. CD36, a scavenger receptor implicated in atherosclerosis. Experimental & molecular medicine. 2014;46(6):e99.
31. Fuhrman B, Volkova N, Aviram M. Oxidative stress increases the expression of the CD36 scavenger receptor and the cellular uptake of oxidized low-density lipoprotein in macrophages from atherosclerotic mice: protective role of antioxidants and of paraoxonase. Atherosclerosis. 2002;161(2):307-16.
32. Lee R, Margaritis M, M Channon K, Antoniades C. Evaluating oxidative stress in human cardiovascular disease: methodological aspects and considerations. Current medicinal chemistry. 2012;19(16): -2504-20.
33. Nsonwu-Anyanwu AC, Offor SJ, John II. Cigarette Smoke and Oxidative Stress Indices in Male Active Smokers. Reactive Oxygen Species. 2018;5(15):199–208-199–208.
34. Zhou M-S, Chadipiralla K, Mendez AJ, Jaimes EA, Silverstein RL, Webster K, et al. Nicotine potentiates proatherogenic effects of oxLDL by stimulating and upregulating macrophage CD36 signaling. American Journal of Physiology-Heart and Circulatory Physiology. 2013;305(4):H563-H74.
35. Ghazavi A, Mosayebi G, Solhi H, Rafiei M, Moazzeni SM. Serum markers of inflammation and oxidative stress in chronic opium (Taryak) smokers. Immunology letters. 2013;153(1-2):22-6.
36. Lee J, Taneja V, Vassallo R. Cigarette smoking and inflammation: cellular and molecular mechanisms. Journal of dental research. 2012;91(2):142-9.
37. Higuchi T, Omata F, Tsuchihashi K, Higashioka K, Koyamada R, Okada S. Current cigarette smoking is a reversible cause of elevated white blood cell count: Cross-sectional and longitudinal studies. Preventive medicine reports. 2016;4:417-22.
38. Tibuakuu M, Kamimura D, Kianoush S, DeFilippis AP, Al Rifai M, Reynolds LM, et al. The association between cigarette smoking and inflammation: The Genetic Epidemiology Network of Arteriopathy (GENOA) study. PLoS One. 2017;12(9):e0184914.
39. Lu Z, Li Y, Brinson CW, Kirkwood KL, Lopes‐Virella MF, Huang Y. CD 36 is upregulated in mice with periodontitis and metabolic syndrome and involved in macrophage gene upregulation by palmitate. Oral diseases. 2017;23(2):210-8.
40. Hashimoto R, Kakigi R, Nakamura K, Itoh S, Daida H, Okada T, et al. LPS enhances expression of CD204 through the MAPK/ERK pathway in murine bone marrow macrophages. Atherosclerosis. 2017;266:167-75.
41. Okamura DM, Pennathur S, Pasichnyk K, López-Guisa JM, Collins S, Febbraio M, et al. CD36 regulates oxidative stress and inflammation in hypercholesterolemic CKD. Journal of the American Society of Nephrology. 2009;20(3):495-505.
42. Liu J, Yang P, Zuo G, He S, Tan W, Zhang X, et al. Long-chain fatty acid activates hepatocytes through CD36 mediated oxidative stress. Lipids in health and disease. 2018;17(1):153.
43. Asadikaram G, Igder S, Jamali Z, Shahrokhi N, et al. Effects of Different Concentrations of Opium on the Secretion of Interleukin-6, Interferon-γ and Transforming Growth Factor Beta Cytokines from Jurkat Cells. Addiction & health. 2015;7(1-2):47.
44. Ayatollahi-Mousavi SA, Asadikaram G, Nakhaee N, Izadi A, Keikha N. The effects of opium addiction on the immune system function in patients with fungal infection. Addiction & health. 2016;8(4):218.
45. Peng X, Mosser DM, Adler MW, Rogers TJ, Meissler Jr JJ, Eisenstein TK. Morphine enhances interleukin‐12 and the production of other pro‐inflammatory cytokines in mouse peritoneal macrophages. Journal of leukocyte biology. 2000;68(5):723-8.
46. Martucci C, Franchi S, Lattuada D, Panerai AE, Sacerdote P. Differential involvement of RelB in morphine‐induced modulation of chemotaxis, NO, and cytokine production in murine macrophages and lymphocytes. Journal of leukocyte biology. 2007;81(1):344-54.
47. Chistiakov DA, Killingsworth MC, Myasoedova VA, et al. CD68/macrosialin: not just a histochemical marker. Laboratory Investigation. 2017;97(1):4.
48. Ramprasad MP, Terpstra V, Kondratenko N, Quehenberger O, Steinberg D. Cell surface expression of mouse macrosialin and human CD68 and their role as macrophage receptors for oxidized low density lipoprotein. Proceedings of the National Academy of Sciences. 1996;93(25):14833-8.
49. John G, Kohse K, Orasche J, Reda A, et al. The composition of cigarette smoke determines inflammatory cell recruitment to the lung in COPD mouse models. Clinical science. 2014;126(3):207-21.
50. Luo C, Lian X, Hong L, et al. High uric acid activates the ROS-AMPK pathway, impairs CD68 expression and inhibits OxLDL-induced foam-cell formation in a human monocytic cell line, THP-1. Cellular Physiology and Biochemistry. 2016;40(3-4):538-48.
51. Gottfried E, Kunz‐Schughart L, Weber A, Rehli M, Peuker A, Müller A, et al. Expression of CD68 in non‐myeloid cell types. Scandinavian journal of immunology. 2008;67(5):453-63.
52. Takeda Y, He P, Tachibana I, Zhou B, Miyado K, Kaneko H, et al. Double deficiency of tetraspanins CD9 and CD81 alters cell motility and protease production of macrophages and causes chronic obstructive pulmonary disease-like phenotype in mice. Journal of Biological Chemistry. 2008;283(38):26089-97.
53. Jin Y, Tachibana I, Takeda Y, He P, Kang S, Suzuki M, et al. Statins decrease lung inflammation in mice by upregulating tetraspanin CD9 in macrophages. PLoS One. 2013;8(9):e73706.
54. Desjardins S, Belkai E, Crete D, Cordonnier L, Scherrmann J-M, Noble F, et al. Effects of chronic morphine and morphine withdrawal on gene expression in rat peripheral blood mononuclear cells. Neuropharmacology. 2008;55(8):1347-54.
| Files | ||
| Issue | Vol 19, No 1 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijaai.v19i1.2417 | |
| PMID | 32245320 | |
| Keywords | ||
| Cigarette CD9 CD36 CD68 Coronary artery disease Opium | ||
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How to Cite
1.
Momeni-Moghaddam MA, Asadikaram G, Nematollahi MH, Esmaeili Tarzi M, Faramarz-Gaznagh S, Mohammadpour-Gharehbagh A, Kazemi Arababadi M. Effects of Cigarette Smoke and Opium on the Expression of CD9, CD36, and CD68 at mRNA and Protein Levels in Human Macrophage Cell Line THP-1. Iran J Allergy Asthma Immunol. 2020;19(1):45-55.
