Mesenchymal Stem Cell Therapy Mitigates Acute and Chronic Lung Damages of Sulfur Mustard Analog Exposure
-
Mahtab Tapak
,
Somaye Sadeghi
,
Tooba Ghazanfari
,
Nariman Mosaffa
,
S. Zahra Mirsanei
,
Seyed Mahmoud Masiha Hashemi
Abstract
Sulfur mustard (SM) is an established chemical weapon that can result in severe damage to parts of the body. Currently, there are no effective treatments available for SM-caused damage. We aimed to investigate the therapeutic potential of adipose-derived mesenchymal stromal cells (AD-MSCs) and conditioned medium (CM-MSCs) in acute and chronic pulmonary mouse models caused by 2-chloroethyl ethyl sulfide (CEES), an SM analog.
The mice were divided into 4 experimental groups:(1) CEES+AD-MSCs, (2) CEES+CM-MSCs, (3) CEES, and (4) control. The model observation time was divided into 7 days for the short and 6 months for the long term. AD-MSCs were injected into mice via intraperitoneal injection 24 hours after CEES exposure. The therapeutic effects of AD-MSCs on pulmonary tissue damage were assessed using histopathologic assay, measuring the neutrophil count, and bronchial alveolar lavage fluid (BALF) protein level. The levels of inflammatory and anti-inflammatory cytokines were evaluated using the enzyme-linked immunosorbent assay as the outcomes of interest.
Lung damage progression was reduced by AD-MSC treatment in mice after CEES injection into the peritoneum. The proportion of CD11b+F4/80+ macrophages in peritoneum was significantly lowered by AD-MSC treatment following CEES exposure. AD-MSC administration also reduced the level of pro-inflammatory cytokines, BALF protein, and nitric oxide levels in the peritoneal cavity.
By reducing inflammation and enhancing tissue healing, AD-MSCs and CM-MSC help prevent acute lung damage caused by CEES. The current study supports the use of a mouse model as a solid experimental foundation and indicates potential use for future cell treatment.
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2. Poursaleh Z, Harandi AA, Vahedi E, Ghanei M. Treatment for sulfur mustard lung injuries; new therapeutic approaches from acute to chronic phase. DARU J Pharm Sci. 2012;20(1):1-11.
3. Saladi R, Smith E, Persaud A. Mustard: a potential agent of chemical warfare and terrorism. Clin Exp Dermatol. 2006;31(1):1-5.
4. McGraw MD, Rioux JS, Garlick RB, Rancourt RC, White CW, Veress LA. From the cover: impairedproliferation and differentiation of the conducting airway epithelium associated with bronchiolitis obliterans after sulfur mustard inhalation injury in rats. Toxicol Sci. 2017;157(2):399-409.
5. Imani S, Salimian J, Bozorgmehr M, Vahedi E, Ghazvini A, Ghanei M, et al. Assessment of Treg/Th17 axis role in immunopathogenesis of chronic injuries of mustard lung disease. J Recept Signal Transduct. 2016;36(5):531-41.
6. Malaviya R, Sunil VR, Venosa A, Vayas KN, Heck DE, Laskin JD, et al. Inflammatory mechanisms of pulmonary injury induced by mustards. Toxicol Lett. 2016;244:2-7.
7. Korkmaz A, Yaren H, Topal T, Oter S. Molecular targets against mustard toxicity: implication of cell surface receptors, peroxynitrite production, and PARP activation. Arch Toxicol. 2006;80(10):662-70.
8. Feng Y, Xu Q, Yang Y, Shi W, Meng W, Zhang H, et al. The therapeutic effects of bone marrow-derived mesenchymal stromal cells in the acute lung injury induced by sulfur mustard. Stem Cell Res Ther. 2019;10(1):90.
9. Malaviya R, Sunil VR, Cervelli J, Anderson DR, Holmes WW, Conti ML, et al. Inflammatory effects of inhaled sulfur mustard in rat lung. Toxicol Appl Pharmacol. 2010;248(2):89-99.
10. 10. Sadeghi S, Mosaffa N, Hashemi SM, Naghizadeh MM, Ghazanfari T. The immunomodulatory effects of mesenchymal stem cells on long term pulmonary complications in an animal model exposed to a sulfur mustard analog. Int Immunopharmacol. 2020;80:105879.
11. Nejad-Moghaddam A, Ajdari S, Tahmasbpour E, Goodarzi H, Panahi Y, Ghanei M. Adipose-derived mesenchymal stem cells for treatment of airway injuries in a patient after long-term exposure to sulfur mustard. Cell J. (Yakhteh). 2017;19(1):117.
12. Darchini-Maragheh E, Balali-Mood M. Delayed complications and long-term management of sulfur mustard poisoning: recent advances by Iranian researchers (part I of II). Iran J Med Sci. 2018;43(2):103.
13. Zhou T, Yuan Z, Weng J, Pei D, Du X, He C, et al. Challenges and advances in clinical applications of mesenchymal stromal cells. J Hematol Oncol. 2021;14(1):1-24.
14. Ullah I, Subbarao RB, Rho GJ. Human mesenchymal stem cells-current trends and future prospective. Biosci Rep. 2015;35(2).
15. Reagan MR, Kaplan DL. Concise review: mesenchymal stem cell tumor-homing: detection methods in disease model systems. Stem cells. 2011;29(6):920-7.
16. Levy O, Kuai R, Siren EM, Bhere D, Milton Y, Nissar N, et al. Shattering barriers toward clinically meaningful MSC therapies. Sci Adv. 2020;6(30):eaba6884.
17. Mathias LJ, Khong SM, Spyroglou L, Payne NL, Siatskas C, Thorburn AN, et al. Alveolar macrophages are critical for the inhibition of allergic asthma by mesenchymal stromal cells. J Immun. 2013;191(12):5914-24.
18. Krasnodembskaya A, Morrison T, O'Kane C, McAuley D, Matthay M. Human mesenchymal stem cells (MSC) modulate alveolar macrophage polarization in vivo and in vitro. Eur Respir J. 2014;44(Suppl 58).
19. Zheng G, Ge M, Qiu G, Shu Q, Xu J. Mesenchymal stromal cells affect disease outcomes via macrophage polarization. Stem Cells Int. 2015
20. Braza F, Dirou S, Forest V, Sauzeau V, Hassoun D, Chesné J, et al. Mesenchymal stem cells induce suppressive macrophages through phagocytosis in a mouse model of asthma. Stem Cells. 2016;34(7):1836-45.
21. Pouya S, Heidari M, Baghaei K, Aghdaei HA, Moradi A, Namaki S, et al. Study the effects of mesenchymal stem cell conditioned medium injection in mouse model of acute colitis. Int Immunopharmacol. 2018;54:86-94.
22. Ghazanfari T, Kaboudanian Ardestani S, Varmazyar M, Eghtedar Doost M, Heidari F, Kianmehr Z, et al. A mouse model of acute and delayed complications of sulfur mustard analogue, 2-chloroethyl ethyl sulfide. Immunoregulation. 2019;2(1):9-24.
23. Hashemi SM, Hassan ZM, Pourfathollah AA, Soudi S, Shafiee A, Soleimani M. Comparative immunomodulatory properties of adipose‐derived mesenchymal stem cells conditioned media from BALB/c, C57BL/6, and DBA mouse strains. J Cell Biochem. 2013;114(4):955-65.
24. Ray A, Dittel BN. Isolation of mouse peritoneal cavity cells. J Vis Exp. 2010(35).
25. Bibak B, Gharib FG, Daneshmandi S, Abbaspour AR, Firizi MN, Ahmadabad HN. The immunomodulatory effects of abortion-prone mice decidual and serum soluble factors on macrophages and splenocytes. Eur J Obstet Gynecol Reprod Biol. 2012;165(2):331-6.
26. Namdar Ahmadabad H, Shafiei R, Hatam GR, Zolfaghari Emameh R, Aspatwar A. Cytokine profile and nitric oxide levels in peritoneal macrophages of BALB/c mice exposed to the fucose-mannose ligand of Leishmania infantum combined with glycyrrhizin. Parasit Vectors. 2020;13(1):1-7.
27. Katsura Y, Harada N, Harada S, Ishimori A, Makino F, Ito J, et al. Characteristics of alveolar macrophages from murine models of OVA-induced allergic airway inflammation and LPS-induced acute airway inflammation. Exp Lung Res. 2015;41(7):370-82.
28. Maxeiner JH, Karwot R, Hausding M, Sauer KA, Scholtes P, Finotto S. A method to enable the investigation of murine bronchial immune cells, their cytokines and mediators. Nat protocol. 2007;2(1):105-12.
29. Präbst K, Engelhardt H, Ringgeler S, Hübner H. Basic colorimetric proliferation assays: MTT, WST, and resazurin. Cell viability assays: Springer; 2017.1-17.
30. Weinberger B, Laskin JD, Sunil VR, Sinko PJ, Heck DE, Laskin DL. Sulfur mustard-induced pulmonary injury: therapeutic approaches to mitigating toxicity. Pulm Pharmacol Ther. 2011;24(1):92-9.
31. Mishra NC, Grotendorst GR, Langley RJ, Singh SP, Gundavarapu S, Weber WM, et al. Inhalation of sulfur mustard causes long-term T cell-dependent inflammation: possible role of Th17 cells in chronic lung pathology. Int immunopharmacol. 2012;13(1):101-8.
32. Beigi Harchegani A, Tahmasbpour E, Borna H, Imamy A, Ghanei M, Shahriary A. Free radical production and oxidative stress in lung tissue of patients exposed to sulfur mustard: an overview of cellular and molecular mechanisms. Chem Res Toxicol. 2018;31(4):211-22.
33. Nejad-Moghaddam A, Ajdary S, Tahmasbpour E, Rad FR, Panahi Y, Ghanei M. Immunomodulatory properties of mesenchymal stem cells can mitigate oxidative stress and inflammation process in human mustard lung. Bioch genet. 2016;54:769-83.
34. Henao Agudelo JS, Braga TT, Amano MT, Cenedeze MA, Cavinato RA, Peixoto-Santos AR, et al. Mesenchymal stromal cell-derived microvesicles regulate an internal pro-inflammatory program in activated macrophages. Front immunol. 2017;8:881.
35. Tewari-Singh N, Gu M, Agarwal C, White CW, Agarwal R. Biological and molecular mechanisms of sulfur mustard analogue-induced toxicity in JB6 and HaCaT cells: possible role of ataxia telangiectasia-mutated/ataxia telangiectasia-Rad3-related cell cycle checkpoint pathway. Chem Res Toxicol. 2010; 23(6):1034-44.
36. Stone WL, Qui M, Smith M. Lipopolysaccharide enhances the cytotoxicity of 2-chloroethyl ethyl sulfide. BMC Cell Biol. 2003;4(1):1-7.
37. Beigi Harchegani A, Khor A, Tahmasbpour E, Ghatrehsamani M, Bakhtiari Kaboutaraki H, Shahriary A. Role of oxidative stress and antioxidant therapy in acute and chronic phases of sulfur mustard injuries: a review. Cutan Ocul Toxicol. 2019;38(1):9-17.
38. Grommes J, Soehnlein O. Contribution of neutrophils to acute lung injury. Mol med. 2011;17(3):293-307.
39. Jugg B, Fairhall S, Smith A, Rutter S, Mann T, Perrott R, et al. N-acetyl-L-cysteine protects against inhaled sulfur mustard poisoning in the large swine. Clin Toxicol. 2013;51(4):216-24.
40. Potey PM, Rossi AG, Lucas CD, Dorward DA. Neutrophils in the initiation and resolution of acute pulmonary inflammation: understanding biological function and therapeutic potential. J Pathol. 2019;247(5):672-85.
41. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105(4):1815-22.
42. Mei SH, Haitsma JJ, Dos Santos CC, Deng Y, Lai PF, Slutsky AS, et al. Mesenchymal stem cells reduce inflammation while enhancing bacterial clearance and improving survival in sepsis. Am J Respir Crit Care Med. 2010;182(8):1047-57.
43. Ghazanfari T, Yaraee R, KiaSalari Z, Hedayati F, Ghasemi H, PourFarzam S, et al. Evaluation of serum levels of nitric oxide in chemical victims of Sardsht 20 years after sulfure mustard exposure. Iran j War Public Health. 2009;1(2):9-23.
44. Yan C, Wu M, Cao J, Tang H, Zhu M, Johnson PF, et al. Critical role for CCAAT/enhancer-binding protein β in immune complex-induced acute lung injury. J Immun. 2012;189(3):1480-90.
45. Korkmaz A, Tan D-X, Reiter R. Acute and delayed sulfur mustard toxicity; novel mechanisms and future studies. Interdiscip Toxicol. 2008;1(1):22-6.
46. Jost P, Svobodova H, Stetina R. Induction and repair of DNA cross-links induced by sulfur mustard in the A-549 cell line followed by a comet assay. Chem Biol Interact. 2015;237:31-7.
47. Kumar D, Tewari-Singh N, Agarwal C, Jain AK, Inturi S, Kant R, et al. Nitrogen mustard exposure of murine skin induces DNA damage, oxidative stress and activation of MAPK/Akt-AP1 pathway leading to induction of inflammatory and proteolytic mediators. Toxicol lett. 2015;235(3):161-71.
48. Laskin JD, Black AT, Jan YH, Sinko PJ, Heindel ND, Sunil V, et al. Oxidants and antioxidants in sulfur mustard–induced injury. Annals of the New York Academy of Sciences. 2010;1203(1):92-100.
49. Matthay MA. Resolution of pulmonary edema. Thirty years of progress. Am J Respir Crit Care Med. 2014;189 (11):1301-8.
50. Bain CC, Jenkins SJ. The biology of serous cavity macrophages. Cell Immunol. 2018;330:126-35.
51. Baumgarth N. The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat Rev Immunol. 2011;11(1):34-46.
52. Okabe Y, Medzhitov R. Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell. 2014;157(4):832-44.
53. Ghosn EEB, Cassado AA, Govoni GR, Fukuhara T, Yang Y, Monack DM, et al. Two physically, functionally, and developmentally distinct peritoneal macrophage subsets. Am J Respir Crit Care Med. . 2010;107(6):2568-73.
54. Tejon G, Valdivieso N, Flores-Santibañez F, Barra-Valdebenito V, Martínez V, Rosemblatt M, et al. Phenotypic and functional alterations of peritoneal macrophages in lupus-prone mice. Mol Biol Rep. 2022;49(6):4193-204.
55. Okabe Y, Medzhitov R. Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell. 2014;157(4):832-44.
2. Poursaleh Z, Harandi AA, Vahedi E, Ghanei M. Treatment for sulfur mustard lung injuries; new therapeutic approaches from acute to chronic phase. DARU J Pharm Sci. 2012;20(1):1-11.
3. Saladi R, Smith E, Persaud A. Mustard: a potential agent of chemical warfare and terrorism. Clin Exp Dermatol. 2006;31(1):1-5.
4. McGraw MD, Rioux JS, Garlick RB, Rancourt RC, White CW, Veress LA. From the cover: impairedproliferation and differentiation of the conducting airway epithelium associated with bronchiolitis obliterans after sulfur mustard inhalation injury in rats. Toxicol Sci. 2017;157(2):399-409.
5. Imani S, Salimian J, Bozorgmehr M, Vahedi E, Ghazvini A, Ghanei M, et al. Assessment of Treg/Th17 axis role in immunopathogenesis of chronic injuries of mustard lung disease. J Recept Signal Transduct. 2016;36(5):531-41.
6. Malaviya R, Sunil VR, Venosa A, Vayas KN, Heck DE, Laskin JD, et al. Inflammatory mechanisms of pulmonary injury induced by mustards. Toxicol Lett. 2016;244:2-7.
7. Korkmaz A, Yaren H, Topal T, Oter S. Molecular targets against mustard toxicity: implication of cell surface receptors, peroxynitrite production, and PARP activation. Arch Toxicol. 2006;80(10):662-70.
8. Feng Y, Xu Q, Yang Y, Shi W, Meng W, Zhang H, et al. The therapeutic effects of bone marrow-derived mesenchymal stromal cells in the acute lung injury induced by sulfur mustard. Stem Cell Res Ther. 2019;10(1):90.
9. Malaviya R, Sunil VR, Cervelli J, Anderson DR, Holmes WW, Conti ML, et al. Inflammatory effects of inhaled sulfur mustard in rat lung. Toxicol Appl Pharmacol. 2010;248(2):89-99.
10. 10. Sadeghi S, Mosaffa N, Hashemi SM, Naghizadeh MM, Ghazanfari T. The immunomodulatory effects of mesenchymal stem cells on long term pulmonary complications in an animal model exposed to a sulfur mustard analog. Int Immunopharmacol. 2020;80:105879.
11. Nejad-Moghaddam A, Ajdari S, Tahmasbpour E, Goodarzi H, Panahi Y, Ghanei M. Adipose-derived mesenchymal stem cells for treatment of airway injuries in a patient after long-term exposure to sulfur mustard. Cell J. (Yakhteh). 2017;19(1):117.
12. Darchini-Maragheh E, Balali-Mood M. Delayed complications and long-term management of sulfur mustard poisoning: recent advances by Iranian researchers (part I of II). Iran J Med Sci. 2018;43(2):103.
13. Zhou T, Yuan Z, Weng J, Pei D, Du X, He C, et al. Challenges and advances in clinical applications of mesenchymal stromal cells. J Hematol Oncol. 2021;14(1):1-24.
14. Ullah I, Subbarao RB, Rho GJ. Human mesenchymal stem cells-current trends and future prospective. Biosci Rep. 2015;35(2).
15. Reagan MR, Kaplan DL. Concise review: mesenchymal stem cell tumor-homing: detection methods in disease model systems. Stem cells. 2011;29(6):920-7.
16. Levy O, Kuai R, Siren EM, Bhere D, Milton Y, Nissar N, et al. Shattering barriers toward clinically meaningful MSC therapies. Sci Adv. 2020;6(30):eaba6884.
17. Mathias LJ, Khong SM, Spyroglou L, Payne NL, Siatskas C, Thorburn AN, et al. Alveolar macrophages are critical for the inhibition of allergic asthma by mesenchymal stromal cells. J Immun. 2013;191(12):5914-24.
18. Krasnodembskaya A, Morrison T, O'Kane C, McAuley D, Matthay M. Human mesenchymal stem cells (MSC) modulate alveolar macrophage polarization in vivo and in vitro. Eur Respir J. 2014;44(Suppl 58).
19. Zheng G, Ge M, Qiu G, Shu Q, Xu J. Mesenchymal stromal cells affect disease outcomes via macrophage polarization. Stem Cells Int. 2015
20. Braza F, Dirou S, Forest V, Sauzeau V, Hassoun D, Chesné J, et al. Mesenchymal stem cells induce suppressive macrophages through phagocytosis in a mouse model of asthma. Stem Cells. 2016;34(7):1836-45.
21. Pouya S, Heidari M, Baghaei K, Aghdaei HA, Moradi A, Namaki S, et al. Study the effects of mesenchymal stem cell conditioned medium injection in mouse model of acute colitis. Int Immunopharmacol. 2018;54:86-94.
22. Ghazanfari T, Kaboudanian Ardestani S, Varmazyar M, Eghtedar Doost M, Heidari F, Kianmehr Z, et al. A mouse model of acute and delayed complications of sulfur mustard analogue, 2-chloroethyl ethyl sulfide. Immunoregulation. 2019;2(1):9-24.
23. Hashemi SM, Hassan ZM, Pourfathollah AA, Soudi S, Shafiee A, Soleimani M. Comparative immunomodulatory properties of adipose‐derived mesenchymal stem cells conditioned media from BALB/c, C57BL/6, and DBA mouse strains. J Cell Biochem. 2013;114(4):955-65.
24. Ray A, Dittel BN. Isolation of mouse peritoneal cavity cells. J Vis Exp. 2010(35).
25. Bibak B, Gharib FG, Daneshmandi S, Abbaspour AR, Firizi MN, Ahmadabad HN. The immunomodulatory effects of abortion-prone mice decidual and serum soluble factors on macrophages and splenocytes. Eur J Obstet Gynecol Reprod Biol. 2012;165(2):331-6.
26. Namdar Ahmadabad H, Shafiei R, Hatam GR, Zolfaghari Emameh R, Aspatwar A. Cytokine profile and nitric oxide levels in peritoneal macrophages of BALB/c mice exposed to the fucose-mannose ligand of Leishmania infantum combined with glycyrrhizin. Parasit Vectors. 2020;13(1):1-7.
27. Katsura Y, Harada N, Harada S, Ishimori A, Makino F, Ito J, et al. Characteristics of alveolar macrophages from murine models of OVA-induced allergic airway inflammation and LPS-induced acute airway inflammation. Exp Lung Res. 2015;41(7):370-82.
28. Maxeiner JH, Karwot R, Hausding M, Sauer KA, Scholtes P, Finotto S. A method to enable the investigation of murine bronchial immune cells, their cytokines and mediators. Nat protocol. 2007;2(1):105-12.
29. Präbst K, Engelhardt H, Ringgeler S, Hübner H. Basic colorimetric proliferation assays: MTT, WST, and resazurin. Cell viability assays: Springer; 2017.1-17.
30. Weinberger B, Laskin JD, Sunil VR, Sinko PJ, Heck DE, Laskin DL. Sulfur mustard-induced pulmonary injury: therapeutic approaches to mitigating toxicity. Pulm Pharmacol Ther. 2011;24(1):92-9.
31. Mishra NC, Grotendorst GR, Langley RJ, Singh SP, Gundavarapu S, Weber WM, et al. Inhalation of sulfur mustard causes long-term T cell-dependent inflammation: possible role of Th17 cells in chronic lung pathology. Int immunopharmacol. 2012;13(1):101-8.
32. Beigi Harchegani A, Tahmasbpour E, Borna H, Imamy A, Ghanei M, Shahriary A. Free radical production and oxidative stress in lung tissue of patients exposed to sulfur mustard: an overview of cellular and molecular mechanisms. Chem Res Toxicol. 2018;31(4):211-22.
33. Nejad-Moghaddam A, Ajdary S, Tahmasbpour E, Rad FR, Panahi Y, Ghanei M. Immunomodulatory properties of mesenchymal stem cells can mitigate oxidative stress and inflammation process in human mustard lung. Bioch genet. 2016;54:769-83.
34. Henao Agudelo JS, Braga TT, Amano MT, Cenedeze MA, Cavinato RA, Peixoto-Santos AR, et al. Mesenchymal stromal cell-derived microvesicles regulate an internal pro-inflammatory program in activated macrophages. Front immunol. 2017;8:881.
35. Tewari-Singh N, Gu M, Agarwal C, White CW, Agarwal R. Biological and molecular mechanisms of sulfur mustard analogue-induced toxicity in JB6 and HaCaT cells: possible role of ataxia telangiectasia-mutated/ataxia telangiectasia-Rad3-related cell cycle checkpoint pathway. Chem Res Toxicol. 2010; 23(6):1034-44.
36. Stone WL, Qui M, Smith M. Lipopolysaccharide enhances the cytotoxicity of 2-chloroethyl ethyl sulfide. BMC Cell Biol. 2003;4(1):1-7.
37. Beigi Harchegani A, Khor A, Tahmasbpour E, Ghatrehsamani M, Bakhtiari Kaboutaraki H, Shahriary A. Role of oxidative stress and antioxidant therapy in acute and chronic phases of sulfur mustard injuries: a review. Cutan Ocul Toxicol. 2019;38(1):9-17.
38. Grommes J, Soehnlein O. Contribution of neutrophils to acute lung injury. Mol med. 2011;17(3):293-307.
39. Jugg B, Fairhall S, Smith A, Rutter S, Mann T, Perrott R, et al. N-acetyl-L-cysteine protects against inhaled sulfur mustard poisoning in the large swine. Clin Toxicol. 2013;51(4):216-24.
40. Potey PM, Rossi AG, Lucas CD, Dorward DA. Neutrophils in the initiation and resolution of acute pulmonary inflammation: understanding biological function and therapeutic potential. J Pathol. 2019;247(5):672-85.
41. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105(4):1815-22.
42. Mei SH, Haitsma JJ, Dos Santos CC, Deng Y, Lai PF, Slutsky AS, et al. Mesenchymal stem cells reduce inflammation while enhancing bacterial clearance and improving survival in sepsis. Am J Respir Crit Care Med. 2010;182(8):1047-57.
43. Ghazanfari T, Yaraee R, KiaSalari Z, Hedayati F, Ghasemi H, PourFarzam S, et al. Evaluation of serum levels of nitric oxide in chemical victims of Sardsht 20 years after sulfure mustard exposure. Iran j War Public Health. 2009;1(2):9-23.
44. Yan C, Wu M, Cao J, Tang H, Zhu M, Johnson PF, et al. Critical role for CCAAT/enhancer-binding protein β in immune complex-induced acute lung injury. J Immun. 2012;189(3):1480-90.
45. Korkmaz A, Tan D-X, Reiter R. Acute and delayed sulfur mustard toxicity; novel mechanisms and future studies. Interdiscip Toxicol. 2008;1(1):22-6.
46. Jost P, Svobodova H, Stetina R. Induction and repair of DNA cross-links induced by sulfur mustard in the A-549 cell line followed by a comet assay. Chem Biol Interact. 2015;237:31-7.
47. Kumar D, Tewari-Singh N, Agarwal C, Jain AK, Inturi S, Kant R, et al. Nitrogen mustard exposure of murine skin induces DNA damage, oxidative stress and activation of MAPK/Akt-AP1 pathway leading to induction of inflammatory and proteolytic mediators. Toxicol lett. 2015;235(3):161-71.
48. Laskin JD, Black AT, Jan YH, Sinko PJ, Heindel ND, Sunil V, et al. Oxidants and antioxidants in sulfur mustard–induced injury. Annals of the New York Academy of Sciences. 2010;1203(1):92-100.
49. Matthay MA. Resolution of pulmonary edema. Thirty years of progress. Am J Respir Crit Care Med. 2014;189 (11):1301-8.
50. Bain CC, Jenkins SJ. The biology of serous cavity macrophages. Cell Immunol. 2018;330:126-35.
51. Baumgarth N. The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat Rev Immunol. 2011;11(1):34-46.
52. Okabe Y, Medzhitov R. Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell. 2014;157(4):832-44.
53. Ghosn EEB, Cassado AA, Govoni GR, Fukuhara T, Yang Y, Monack DM, et al. Two physically, functionally, and developmentally distinct peritoneal macrophage subsets. Am J Respir Crit Care Med. . 2010;107(6):2568-73.
54. Tejon G, Valdivieso N, Flores-Santibañez F, Barra-Valdebenito V, Martínez V, Rosemblatt M, et al. Phenotypic and functional alterations of peritoneal macrophages in lupus-prone mice. Mol Biol Rep. 2022;49(6):4193-204.
55. Okabe Y, Medzhitov R. Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell. 2014;157(4):832-44.
| Files | ||
| Issue | Vol 23 No 5 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijaai.v23i5.16751 | |
| Keywords | ||
| Bronchoalveolar lavage fluid Conditioned medium Mesenchymal stem cell Peritoneal macrophage Sulfur mustard | ||
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How to Cite
1.
Tapak M, Sadeghi S, Ghazanfari T, Mosaffa N, Mirsanei SZ, Masiha Hashemi SM. Mesenchymal Stem Cell Therapy Mitigates Acute and Chronic Lung Damages of Sulfur Mustard Analog Exposure. Iran J Allergy Asthma Immunol. 2024;23(5):563-577.
