Aysun ÇAĞLAR TORUN, Şerife TÜTÜNCÜ, Tuğrul ERTUĞRUL

The role of resveratrol on mast cell and chymase and tryptase expression in blunt-chesttrauma-induced acute lung injury in rats

Acute lung injury is a clinical symptom that can cause morbidity, acute respiratory failure, and risk of developing pneumonia. Mast cells are found more commonly in places where antigens can enter the body, such as skin and respiratory and digestive systems, which enables them to be among the first groups of cell to act in the defense mechanism against foreign matter entry. Resveratrol is an active substance which is found in the structure of many plants and which can be used against pathogens due to its antimicrobial effect. The aim of our study is to show the degranulation and heterogeneity of mast cells and the presence of tryptase and chymase secreted from their granules immunohistochemically in acute lung injury which occurs after blunt trauma and to research what kind of an effect resveratrol has on mast cells in this process. Twenty adult female Sprague–Dawley rats were used in the study. The rats were randomly assigned to four groups. The first group was the control group, the second was the contusion group, the third was resveratrol group, and the fourth was the treatment group in which contusion was induced following 30 mg/kg intraperitoneal resveratrol administration. In the present study, acute lung injury was created with trauma and the effects of resveratrol in this process on the distribution, heterogeneity, degranulation, and immunohistochemical characteristics of mast cells were examined. It was concluded that resveratrol, which caused a significant decrease in mast cell degranulation and increase in number following trauma, had an influential role in this process.

PDF

___

1. Rubenfeld GD, Caldwell E, Peabody E, Weaver J, Martin DP et al. Incidence and outcomes of acute lung injury. The New England Journal of Medicine 2005; 353: 1685-1693. doi: 10.1056/NEJMoa050333
2. Dowdy DW, Eid MP, Dennison CR, Mendez-Tellez PA, Herridge MS et al. Quality of life after acute respiratory distress syndrome: a meta-analysis. Intensive Care Medicine 2006; 32: 1115-1124. doi: 10.1007/s00134-006-0217-3
3. Michelet P, Couret D, Bregeon F, Perrin G, D’Journo XB et al. Early onset pneumonia in severe chest trauma: A risk factor analysis. J Trauma 2010; 68: 395-400. doi: 10.1097/ TA.0b013e3181a601cb
4. Wesson DE, Thoracic injuries. In: Grosfeld JL, O’Neill JA, Coran AG, Fonkalsrud EW, editors. Pediatric surgery. Philadelphia: Mosby Elsevier Inc 2006.
5. Stitzel JD, Gayzik FS, Hoth JJ, Mercier J, Gage HD et al. Development of a finite element-based injury metric for pulmonary contusion part I: model development and validation. Stapp Car Crash Journal 2005; 49: 271-89.
6. Knöferl MW, Liener UC, Seitz DH, Perl M, Brückner UB et al. Cardiopulmonary, histological, and inflammatory alterations after lung contusion in a novel mouse model of blunt chest trauma. Shock 2003; 19: 519-525. doi: 10.1097/01. shk.0000070739.34700.f6
7. Perl M, Hohmann C, Denk S, Kellermann P, Lu D et al. Role of activated neutrophils in chest trauma-induced septic acute lung injury. Shock 2012; 38: 98-106. doi: 10.1097/ SHK.0b013e318254be6a
8. Knöferl MW, Liener UC, Perl M, Brückner U, Kinzl L et al. Blunt chest trauma induces delayed splenic immunosuppression. Shock 2004; 22: 51-56. doi: 10.1097/SHK.0b013e31819c385c
9. Eurell JA, Frappier BL. Dellman’s Textbook of Veterinary Histology. Oxford, UK: Blackwell Publishers; 2006.
10. Krystel-Whittemore M, Dileepan KN, Wood JG. Mast cell: a multi-functional master cell. Frontiers in Immunology 2016; 6: 620. doi: 10.3389/fimmu.2015.00620
11. Wernersson S, Pejler G. Mast cell secretory granules: armed for battle. Nature Reviews Immunology 2014; 14 (7): 478-494. doi: 10.1038/nri3690
12. Galli SJ, Maurer M, Lantz CS. Mast cells as sentinels of innate immunity. Current Opinion in Immunology 1999; 11 (1): 53- 59. doi: 10.1016/s0952-7915(99)80010-7
13. Abraham SN, Malaviya R. Mast cells in infection and immunity. Infection and Immunity 1997; 65 (9): 3501-3508. doi: 10.1128/ IAI.65.9.3501-3508.1997
14. Echtenacher B, Mannel DN, Hultner L. Critical protective role of mast cells in a model of acute septic peritonitis. Nature 1996; 381: 75-77. doi: 10.1038/381075a0
15. Gartner LP, Hiatt JL. Color Textbook of Histology. China: W. B. Saunders Elsevier; 2007.
16. Frey RS, Ushio-Fukai M, Malik AB. NADPH oxidasedependent signaling in endothelial cells: role in physiology and pathophysiology. Antioxidants & Redox Signaling 2009; 11: 791-810. doi: 10.1089/ARS.2008.2220
17. Luo C, Yuan D, Zhao W, Huixin C, Gangjian L et al. Sevoflurane ameliorates intestinal ischemia-reperfusion-induced lung injury by inhibiting the synergistic action between mast cell activation and oxidative stress. Molecular Medicine Report 2015; 1082-1090. doi: 10.3892/mmr.2015.3527
18. Hermans MA, Broijl A, van Daele PL. A unique presentation of pulmonary disease in advanced systemic mastocytosis, proven by the presence of mast cells in bronchoalveolar lavage: a case report. Journals of Medical Case Report 2016; 10: 283. doi: 10.1186/s13256-016-1066-5
19. Nishino R, Fukuyama T, Watanabe Y, Harada T. Detection of respiratory allergies caused by environmental chemical allergen via measures of hyper-activation and degranulation of mast cells in lungs of NC/Nga mice. Journals of Immunotoxicology 2016; 13: 676-685. doi: 10.3109/1547691X.2016.1154904
20. Frémont L. Biological effects of resveratrol. Life Sciences 2000; 66 (8): 663-673. doi: 10.1016/s0024-3205(99)00410-5
21. Holme AL, Pervaiz S. Resveratrol in cell fate decisions. Journal of Bioenergetics and Biomembranes 2007; 39 (1): 59-63. doi: 10.1007/s10863-006-9053-y
22. Baur JA, Sinclair DA. Therapeutic potential of resveratrol: the in vivo evidence. Nature Reviews. Drug Discovery 2006; 5 (6): 493-506. doi: 10.1038/nrd2060
23. Harikumar KB, Aggarwal BB. Resveratrol: a multitargeted agent for age-associated chronic diseases. Cell Cycle 2008; 7 (8): 1020-1035. doi: 10.4161/cc.7.8.5740
24. Van der Wal SE, Vaneker M, Kox M, Braak G, VanHees HW et al. Resveratrol attenuates NF-κB-binding activity but not cytokine production in mechanically ventilated mice. Acta Anaesthesiologica Scandinavica 2014; 58: 487-494. doi: 10.1111/aas.12276
25. Das S, Das DK. Anti-inflammatory responses of resveratrol. Inflammation & Allergy Drug Targets 2007; 6 (3): 168-173. doi: 10.2174/187152807781696464
26. Sener G, Topaloğlu N, Sehirli AO, Ercan F, Gedik N. Resveratrol alleviates bleomycin-induced lung injury in rats. Pulmonary Pharmacology & Therapeutic 2007; 20 (6): 642- 649. doi: 10.1016/j.pupt.2006.07.003
27. Raghavendran K, Davidson BA, Helinski JD, Marschke CJ, Manderscheid P et al. A rat model for isolated bilateral lung contusion from blunt chest trauma. Anesthesia & Analgesia 2005; 101: 1482-14899.
28. Crossmon O.A modification of mallory’s connective tissue stain with a discussion of the principles involved. The Anatomical Record 1937; 69: 31-38. doi: 10.1002/ar.1090690105
29. Enerback L. Mast cells in rat gastrointestinal mucosa: 2. dyebinding and metachromatic properties. Acta Pathologica et Microbiologica Scandinavica 1966; 66: 303-331. doi: 10.1111/ apm.1966.66.3.303
30. Böck P. Romeis Mikropische Technik. 18 th ed. München, Wien, Baltimore: Springer Spectrum; 2010 (in German).
31. John PWM. Statistical Design and Analysis of Experiments. 1 st ed. NewYork, NY, USA: Macmilllan; 1971.
32. True LD. Principles of Immunohistochemistry. 2nd ed. New York, NY, USA: Gower Medical Publishing; 1990.
33. Tutuncu S, Ertuğrul T. Immunohistochemical expression of tryptase-chymase and mast cell heterogeneity in capsaicintreated rat ovaries. International Journal of Veterinary and Animal Research 2019; 2 (2): 25-31.
34. Van der Velden J, Barker D, Barcham G, Koumoundouros E, Snibson K. Increased mast cell density and airway responses to allergic and non-allergic stimuli in a sheep model of chronic asthma. PLoS One 2012; 7 (5): e37161. doi: 10.1371/journal. pone.0037161
35. Hirata K, Sugama Y, Ikura, Y, Ohsawa M, Inoue Y et al. Enhanced mast cell chymase expression in human idiopathic interstitial pneumonia. International Journal of Molecular Medicine 2007; 19(4): 565-570.
36. Andersson CK, Shikhagaie M, Mori M, Al-Garawi A, Reed JL et al. Distal respiratory tract viral infections in young children trigger a marked increase in alveolar mast cells. ERJ Open Research 2018; 23: 4 (4). doi: 10.1183/23120541.00038-2018
37. Zanini A, Chetta A, Saetta M, Baraldo S, D’Ippolito R et al. Chymase-positive mast cells play a role in the vascular component of airway remodeling in asthma. The Journal Allergy and Clinical Immunology 2007; 120 (2): 329-333. doi: 10.1016/j.jaci.2007.04.021
38. Kosanovic D, Dahal BK, Peters DM, Seimetz M, Wygrecka M et al. Histological characterization of mast cell chymase in patients with pulmonary hypertension and chronic obstructive pulmonary disease. Pulmonary Circulation 2014; 4 (1): 128- 136. doi: 10.1086/675642
39. Kosanovic D, Luitel H, Dahal BK, Cornitescu T, Janssen W, Danser AH et al. Chymase: a multifunctional player in pulmonary hypertension associated with lung fibrosis. The Europan Respiratory Journal 2015; 46 (4): 1084-1094. doi: 10.1183/09031936.00018215
40. Payne V, Kam PC. Mast cell tryptase: a review of its physiology and clinical significance. Anaesthesia 2004; 59 (7): 695-703. doi: 10.1111/j.1365-2044.2004.03757.x
41. Gosman MM, Postma DS, Vonk JM, Rutgers B, Lodewijk M et al. Association of mast cells with lung function in chronic obstructive pulmonary disease. Respiratory Research 2008; 10 (9): 64. doi: 10.1186/1465-9921-9-64
42. Schmit D, Le DD, Heck S, Bischoff M, Tschernig T et al. Allergic airway inflammation induces migration of mast cell populations into the mouse airway. Cell and Tissue Research 2017; 69 (2): 331-340. doi: 10.1007/s00441-017-2597-9
43. Villar J, Cabrera-Benítez NE, Valladares F, García-Hernández S, Ramos-Nuez Á et al. Tryptase is involved in the development of early ventilator-induced pulmonary fibrosis in sepsisinduced lung injury. Critical Care 2015; 19: 138. doi: 10.1186/ s13054-015-0878-9
44. Andersson CK, Mori M, Bjermer L, Löfdahl CG, Erjefält JS. Alterations in lung mast cell populations in patients with chronic obstructive pulmonary disease. American Journal of Respiratory and Critical Care Medicine 2010; 181 (3): 206-217. doi: 10.1164/rccm.200906-0932OC
45. Zhao W, Gan X, Su G, Wanling G, Li S et al. The interaction between oxidative stress and mast cell activation plays a role in acute lung injuries induced by intestinal ischemia-reperfusion. The Journal of Surgical Research 2014; 187 (2): 542-552. doi: 10.1016/j.jss.2013.10.033
46. James A, Gyllfors P, Henriksson E, Dahlén SE, Adner M et al. Corticosteroid treatment selectively decreases mast cells in the smooth muscle and epithelium of asthmatic bronchi. Allergy 2012; 67 (7): 958-961. doi: 10.1111/j.1398-9995.2012.02836.x
47. Lozada A, Maegele M, Stark H, Neugebauer EM, Panula P. Traumatic brain injury results in mast cell increase and changes in regulation of central histamine receptors. Neuropathology and Applied Neurobiology 2005; 31 (2): 150-162. doi: 10.1111/j.1365-2990.2004.00622.x
48. Wilkes LK, McMenamin C, Holt PG. Postnatal maturation of mast cell subpopulations in the rat respiratory tract. Immunology 1992; 75 (3): 535-541.
49. Tomita M, Itoh H, Kobayashi T, Onitsuka T, Nawa Y. Expression of mast cell proteases in rat lung during helminth infection: mast cells express both rat mast cell protease II and tryptase in helminth infected lung. International Archives of Allergy and Immunology 1999; 120 (4): 303-309. doi: 10.1159/000024283
50. Huang X, Zhao W, Hu D, Han X, Wang H et al. Resveratrol efficiently improves pulmonary function via stabilizing mast cells in a rat intestinal injury model. Life Sciences 2017; 185: 30-37. doi: 10.1016/j.lfs.2017.07.018
51. Han SY, Bae JY, Park SH, Kim YH, Park JH et al. Resveratrol inhibits IgE-mediated basophilic mast cell degranulation and passive cutaneous anaphylaxis in mice. The Journal of Nutrition 2013; 143 (5): 632-639. doi: 10.3945/jn.112.173302
52. Catalli A, MacDonald C, Pundir P, Kulka M. Inhibitory effects of resveratrol on human mast cell degranulation, cytokine, chemokine and leukotriene release. Open Journal of Immunology 2012; 2 (4): 187-194. doi: 10.4236/oji.2012.24022
53. Bozdemir K, Şahin E, Altintoprak N, Muluk NB, Cengiz BP et al. Is resveratrol therapeutic when used to treat allergic rhinitisinitis in rats? Clinic and Investigative Medicine 2016; 39 (2): E63-72. doi: 10.25011/cim.v39i2.26482
54. Zeng H, He Y, Yu Y, Zhang J, Zeng X et al. Resveratrol improves prostate fibrosis during progression of urinary dysfunction in chronic prostatitis by mast cell suppression. Molecular Medicine Reports 2018; 17 (1): 918-924. doi: 10.3892/ mmr.2017.7960
55. Brock TG, Di Giulio C. Prolonged exposure to hyperoxia increases perivascular mast cells in rat lungs. The Journal of Histochemistry and Cytochemistry 2006; 54 (11): 1239-1246. doi: 10.1369/jhc.6A7007.2006
56. Ali Z, Kosanovic D, Kolosionek E, Schermuly RT, Graham BB et al. Enhanced inflammatory cell profiles in schistosomiasisinduced pulmonary vascular remodeling. Pulmonary Circulation 2017; 7 (1): 244-252. doi: 10.1086/690687
57. Terzi H, Duran A, Fırat T, Ocak T, Kükner T. Effect of montelukast on acute lung injury induced by intestinal ischemia and reperfusion in rats. Acta Medica Mediterranea 2014; 30: 411.
58. El-Mohandes EM, Moustafa AM, Khalaf HA, Hassan YF. The role of mast cells and macrophages in amiodarone induced pulmonary fibrosis and the possible attenuating role of atorvastatin. Biotechnic & Histochemistry 2017; 92 (7): 467- 480. doi: 10.1080/10520295.2017
59. Kilinç E, Balci CN. An Investigation of lung mast cell behavior in a rat model of migraine: implications for migraine headache. Anatolian Clinic 2018; 23 (3): 151-156. doi: 10.21673/ anadoluklin.429905
60. Possebon L, de Souza Lima Lebron I, Furlan da Silva L, Tagliaferri Paletta J, Glad BG et al. Anti-inflammatory actions of herbal medicines in a model of chronic obstructive pulmonary disease induced by cigarette smoke. Biomedicine & Pharmacotherapy 2018; 99: 591-597. doi: 10.1016/j. biopha.2018.01.106