The effect of 12 weeks of submaximal swimming training on MAPK and MDA biomarkers in rats exposed to tobacco-derived nitrosamine ketone

Document Type : Research Paper

Authors
Fatemeh Babaei 1
Ali Barzegari 2
Ebrahim Norian 3
Mohammad Hassan Dashti Khoidaki 2
1 (Department of physical education, Payame Noor University, PO BOX 19395-3697, Tehran, IRAN.)
2 Department of Exercise Physiology, Payame Noor University, Tehran PO Box 3697-19395, Iran.
3 Department of Exercise Physiology, Payame Noor University, Tehran PO Box 3697-19395, Iran
10.22089/spj.2022.12495.2185
Abstract
Background: The purpose of this study was to investigate the effect of 12 weeks of maximal swimming training on MAPK and MDA biomarkers in rats exposed to tobacco-derived nitrosamine ketone.
Methods:48 6-8 week old Wistar rats with a weight range of 26 ± 105 g were purchased and randomly divided into 5 control groups (8 heads), distilled water injection(10 heads),NNK injection(10 heads), swimming training.(10 heads),swimming practice + NNK injection(10 heads),were divided.The training program included12 eeks of swimming with maximum intensity (five days a week). 48 hours after the last training session, lung tissue sampling was performed and the levels of MAPK and MDA markers of lung tissue were measured by ELISA technique. One-way ANOVA and Tukey were used to analyze the data
Results :The results showed that the levels of MAPK(P = 0.001)and MDA(P = 0.000) were significant among the groups.The results of Tukey test showed that the reduction of MAPK in swimming and swimming +NNK intervention groups compared to NNK intervention group was significant(P = 0.001)(P = 0.001)and also, the rate of MDA reduction in swimming and swimming + NNK intervention groups was significant compared to NNK intervention group(0.001 = P)(001/0 = P).
Conclusion: The results of studies showed that swimming exercises can reduce the negative effects of NNK on MAPK and MDA levels to some extent, and it is possible that due to the anti-inflammatory role of swimming exercise activity can control the carcinogenic effect of NNK and protect the respiratory system in Equivalent to the carcinogen NNK.
Keywords
Swimming exercise
Lung
NNK
MAPK
MDA
  1. Xue J, Yang S, Seng S. Mechanisms of cancer induction by tobacco-specific NNK and NNN. Cancers. 2014;6(2):1138-56.
  2. Zhang D, Lei J, Ma J, Chen X, Sheng L, Jiang Z, et al. β2-adrenogenic signaling regulates NNK-induced pancreatic cancer progression via upregulation of HIF-1α. Oncotarget. 2016;7(14):17760.
  3. Lonergan PE, Tindall DJ. Androgen receptor signaling in prostate cancer development and progression. Journal of carcinogenesis. 2011;10.
  4. Wu W-K, Llewellyn OP, Bates DO, Nicholson LB, Dick AD. IL-10 regulation of macrophage VEGF production is dependent on macrophage polarisation and hypoxia. Immunobiology. 2010;215(9-10):796-803.
  5. Omomi M, Taghian F, Sharifi G-R. Investigating the effect of six weeks of aerobic exercise alone and with the consumption of ginger extract encapsulated in chitosan nanoparticles on the change of heart tissue morphology and the level of mitogen-activated protein kinase (MAPK) gene expression in rats with myocardial infarction: an experimental study. Studies in Medical Sciences. 2021;32(1):1-13.
  6. Schreck I, Grico N, Hansjosten I, Marquardt C, Bormann S, Seidel A, et al. The nucleotide excision repair protein XPC is essential for bulky DNA adducts to promote interleukin-6 expression via the activation of p38-SAPK. Oncogene. 2016;35(7):908-18.
  7. Chen K, Chu B-z, Liu F, Li B, Gao C-m, Li L-l, et al. New benzimidazole acridine derivative induces human colon cancer cell apoptosis in vitro via the ROS-JNK signaling pathway. Acta Pharmacologica Sinica. 2015;36(9):1074-84.
  8. Fang JY, Richardson BC. The MAPK signalling pathways and colorectal cancer. The lancet oncology. 2005;6(5):322-7.
  9. Singh S, Pillai S, Chellappan S. Nicotinic acetylcholine receptor signaling in tumor growth and metastasis. Journal of oncology. 2011;2011.
  10. Gankhuyag N, Lee K-H, Cho J-Y. The role of nitrosamine (NNK) in breast cancer carcinogenesis. Journal of mammary gland biology and neoplasia. 2017;22(3):159-70.
  11. Milevoj Kopčinović L, Domijan A-M, Posavac K, Čepelak I, Žanić Grubišić T, Rumora L. Systemic redox imbalance in stable chronic obstructive pulmonary disease. Biomarkers. 2016;21(8):692-8.
  12. Gönenç A, Özkan Y, Torun M, Şimşek B. Plasma malondialdehyde (MDA) levels in breast and lung cancer patients. Journal of clinical pharmacy and therapeutics. 2001;26(2):141-4.
  13. Liu J, Yeo HC, Overvik-Douki E, Hagen T, Doniger SJ, Chu DW, et al. Chronically and acutely exercised rats: biomarkers of oxidative stress and endogenous antioxidants. Journal of applied physiology. 2000;89(1):21-8.
  14. Hamza RZ, El-Shenawy NS. Anti-inflammatory and antioxidant role of resveratrol on nicotine-induced lung changes in male rats. Toxicology reports. 2017;4:399-407.
  15. Ghambari Z, Nabiun iM, Jalali H, Karimzadeh L. Inhibition of lung cancer Calu-6 cell line proliferation using Cdc42 gene shRNA. Journal of Cell & Tissue. 2017;8(3):261-70.
  16. Koutsokera A, Kiagia M, Saif MW, Souliotis K, Syrigos KN. Nutrition habits, physical activity, and lung cancer: an authoritative review. Clinical lung cancer. 2013;14(4):342-50.
  17. Hansen HH. Lung cancer: advances in basic and clinical research: Springer Science & Business Media; 2012.
  18. Hasani F, Gholami M, Ghazalian F. Effect of Six Weeks of Endurance Training on Tumor Volume and Muscle Myostatin Levels in Female Mice with Breast Cancer: Implications for Cachexia. Iranian Journal of Breast Diseases. 2018;11(3):44-5.
  19. Ahmadian M, Azizbeigi K, Delphan M, Atashak S. The Effect of High Intensity Interval Training on STAT-3 and Angiopoietin-1 Gene Expression, and tie-2 Protein in Mice with Breast Cancer. Iranian Journal of Breast Diseases. 2018;11(1):37-46.
  20. Zielinski MR, Muenchow M, Wallig MA, Horn PL, Woods JA. Exercise delays allogeneic tumor growth and reduces intratumoral inflammation and vascularization. Journal of applied physiology. 2004;96(6):2249-56.
  21. Murphy EA, Davis JM, Barrilleaux T, McClellan J, Steiner J, Carmichael M, et al. Benefits of exercise training on breast cancer progression and inflammation in C3 (1) SV40Tag mice. Cytokine. 2011;55(2):274-9.
  22. Williamson D, Gallagher P, Harber M, Hollon C, Trappe S. Mitogen‐activated protein kinase (MAPK) pathway activation: effects of age and acute exercise on human skeletal muscle. The Journal of physiology. 2003;547(3):977-87.
  23. Gibala MJ, McGee SL, Garnham AP, Howlett KF, Snow RJ, Hargreaves M. Brief intense interval exercise activates AMPK and p38 MAPK signaling and increases the expression of PGC-1α in human skeletal muscle. Journal of applied physiology. 2009;106(3):929-34.
  24. Hwang I-S, Kwak Y-S. Tai chi exercise on MDA, SOD and physical fitness in breast cancer patients. Journal of Life Science. 2009;19(4):543-8.
  25. Toskulkao C, Glinsukon T. Endurance exercise and muscle damage: relationship to lipid peroxidation and scavenging enzymes in short and long distance runners. Japanese Journal of Physical Fitness and Sports Medicine. 1996;45(1):63-70.
  26. Barzegari A, Mirdar S. Investigating the Effect of One Period of Nigella Sativa Nanocapsules Consumption on the Histopathological Structure and Vascular Endothelial Growth Factor Levels of the Lung Tissue of the Rats Exposed to Nicotine-Derived Nitrosamine Ketone. Journal of Rafsanjan University of Medical Sciences. 2018;17(5):435-46.
  27. Gleeson M, Bishop N, Walsh N. Exercise immunology: Routledge; 2013.
  28. Herzog CR, Desai D, Amin S. Array CGH analysis reveals chromosomal aberrations in mouse lung adenocarcinomas induced by the human lung carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone. Biochemical and biophysical research communications. 2006;341(3):856-63.
  29. Akopyan G, Bonavida B. Understanding tobacco smoke carcinogen NNK and lung tumorigenesis. International journal of oncology. 2006;29(4):745-52.
  30. Wang C-Y, Chen C-L, Tseng Y-L, Fang Y-T, Lin Y-S, Su W-C, et al. Annexin A2 silencing induces G2 arrest of non-small cell lung cancer cells through p53-dependent and-independent mechanisms. Journal of Biological Chemistry. 2012;287(39):32512-24.
  31. Zhang BC, Gao J, Wang J, Rao ZG, Wang BC, Gao JF. Tumor-associated macrophages infiltration is associated with peritumoral lymphangiogenesis and poor prognosis in lung adenocarcinoma. Medical Oncology. 2011;28(4):1447-52.
  32. Mirdar S, S., Hedayati M, Hajizade A. The Effect of Endurance Swimming Exercise on HIF-1 Levels in Livers of Pregnant Rats Exposed to Cadmium Toxicity. Journal of Rafsanjan University of Medical Sciences. 2014;12(11):919-28.
  33. Gobatto CA, De Mello MAR, Sibuya CY, De Azevedo JRM, Dos Santos LA, Kokubun E. Maximal lactate steady state in rats submitted to swimming exercise. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 2001;130(1):21-7.
  34. Zhang N, Sun X, Sun M, Zhu S, Wang L, Ma D, et al. 4-(Methylnitrosamino)-1-(3-pyridyl)-1-butanone promotes esophageal squamous cell carcinoma growth via beta-adrenoceptors in vitro and in vivo. PloS one. 2015;10(3):e0118845.
  35. Tang J, Li Z, Lu L, Cho CH, editors. β-Adrenergic system, a backstage manipulator regulating tumour progression and drug target in cancer therapy. Seminars in cancer biology; 2013: Elsevier.
  36. Chen R-J, Chang LW, Lin P, Wang Y-J. Epigenetic effects and molecular mechanisms of tumorigenesis induced by cigarette smoke: an overview. Journal of oncology. 2011;2011.
  37. Hall JM, Couse JF, Korach KS. The multifaceted mechanisms of estradiol and estrogen receptor signaling. Journal of biological chemistry. 2001;276(40):36869-72.

 

 

  1. Mountzios G, Planchard D, Besse B, Validire P, Girard P, Devisme C, et al. Mitogen-activated protein kinase activation in lung adenocarcinoma: a comparative study between ever smokers and never smokers. Clinical cancer research. 2008;14(13):4096-102.
  2. Majidi M, Al-Wadei HA, Takahashi T, Schuller HM. Nongenomic β estrogen receptors enhance β1 adrenergic signaling induced by the nicotine-derived carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone in human small airway epithelial cells. Cancer Research. 2007;67(14):6863-71.
  3. Chen R-J, Chang C-Y, Chang LW, Siao S-H, Ho Y-S, Wu C-H, et al. The regulation of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone-induced lung tumor promotion by estradiol in female A/J mice. PloS one. 2014;9(3): e93152.
  4. Baghaiee B, Karimi P, Siahkouhian M, Pescatello LS. Moderate aerobic exercise training decreases middle-aged induced pathologic cardiac hypertrophy by improving Klotho expression, MAPK signaling pathway, and oxidative stress status in Wistar rats. Iran J Basic Med Sci. 2018;21(9):911.
  5. Junttila MR, Li SP, Westermarck J. Phosphatase‐mediated crosstalk between MAPK signaling pathways in the regulation of cell survival. The FASEB Journal. 2008;22(4):954-65.
  6. Hsieh C, Kuro-o M, Rosenblatt KP, Brobey R, Papaconstantinou J. The ASK1-Signalosome regulates p38 MAPK activity in response to levels of endogenous oxidative stress in the Klotho mouse models of aging. Aging (Albany NY). 2010;2(9):597.
  7. Standard J, Jiang Y, Yu M, Su X, Zhao Z, Xu J, et al. Reduced signaling of PI3K-Akt and RAS-MAPK pathways is the key target for weight-loss-induced cancer prevention by dietary calorie restriction and/or physical activity. The Journal of nutritional biochemistry. 2014;25(12):1317-23.
  8. Rose AJ, Hargreaves M. Exercise increases Ca2+–calmodulin‐dependent protein kinase II activity in human skeletal muscle. The Journal of physiology. 2003;553(1):303-9.
  9. Yu M, Blomstrand E, Chibalin AV, Krook A, Zierath JR. Marathon running increases ERK1/2 and p38 MAP kinase signalling to downstream targets in human skeletal muscle. The Journal of physiology. 2001;536(1):273-82.
  10. Lykkesfeldt J. Malondialdehyde as biomarker of oxidative damage to lipids caused by smoking. Clinica chimica acta. 2007;380(1-2):50-8.
  11. Tanriverdi H, Evrengul H, Kuru O, Tanriverdi S, Seleci D, Enli Y, et al. Cigarette smoking induced oxidative stress may impair endothelial function and coronary blood flow in angiographically normal coronary arteries. Circulation Journal. 2006;70(5):593-9.
  12. Munnia A, Bonassi S, Verna A, Quaglia R, Pelucco D, Ceppi M, et al. Bronchial malondialdehyde DNA adducts, tobacco smoking, and lung cancer. Free Radical Biology and Medicine. 2006;41(9):1499-505.

 

  1. Bartsch H, Petruzzelli S, De Flora S, Hietanen E, Camus A-M, Castegnaro M, et al. Carcinogen metabolism in human lung tissues and the effect of tobacco smoking: results from a case--control multicenter study on lung cancer patients. Environmental health perspectives. 1992; 98:119-24.
  2. Skrzydlewska E, Sulkowski S, Koda M, Zalewski B, Kanczuga-Koda L, Sulkowska M. Lipid peroxidation and antioxidant status in colorectal cancer. World journal of gastroenterology: WJG. 2005;11(3):403.
  3. Ermis B, Ors R, Yildirim A, Tastekin A, Kardas F, Akcay F. Influence of smoking on maternal and neonatal serum malondialdehyde, superoxide dismutase, and glutathione peroxidase levels. Annals of Clinical & Laboratory Science. 2004;34(4):405-9.
  4. Zabłocka-Słowińska K, Płaczkowska S, Skórska K, Prescha A, Pawełczyk K, Porębska I, et al. Oxidative stress in lung cancer patients is associated with altered serum markers of lipid metabolism. PloS one. 2019;14(4):e0215246.
  5. Vera-Ramirez L, Sanchez-Rovira P, Ramirez-Tortosa MC, Ramirez-Tortosa CL, Granados-Principal S, Lorente JA, et al. Free radicals in breast carcinogenesis, breast cancer progression and cancer stem cells. Biological bases to develop oxidative-based therapies. Critical reviews in oncology/hematology. 2011;80(3):347-68.
  6. Omar ME A-S, Eman R Y, Hafez F H. The antioxidant status of the plasma in patients with breast cancer undergoing chemotherapy. Open Journal of Molecular and Integrative Physiology. 2011;2011.
  7. Jayakumar R, Kanthimathi M. Dietary spices protect against hydrogen peroxide-induced DNA damage and inhibit nicotine-induced cancer cell migration. Food chemistry. 2012;134(3):1580-4.
  8. Wang M, Dhingra K, Hittelman WN, Liehr JG, De Andrade M, Li D. Lipid peroxidation-induced putative malondialdehyde-DNA adducts in human breast tissues. Cancer Epidemiology and Prevention Biomarkers. 1996;5(9):705-10.
  9. Seyed A, Farsi S, Hosseini SA, Kaka G. Antioxidant effects of swimming training and curcumin in withdrawal period of alcohol overdose in rats. Journal of Fasa University of Medical Sciences. 2018;8(3):901-10.
  10. Mirdar S, Seyedazizi R, Arzani A, Hedayati M. Effects of lead and curcumin interactions during a period of endurance training on the lung levels of vascular endothelial growth factor. 2. 2017;9(17):49-56.
  11. Ali G, Asghar T, Bahareh A. The effects of curcumin supplementation on oxidative stress induced during strenuous endurance training on the kidney and lung tissues. Scientific Journal of Kurdistan University of Medical Sciences. 2018; 23:1-11.
  12. Neumayr G, Pfister R, Hoertnagl H, Mitterbauer G, Getzner W, Ulmer H, et al. The effect of marathon cycling on renal function. International journal of sports medicine. 2003;24(02):131-7.
  13. Dehghan G, Shaghaghi M, Jafari A, Mohammadi M, Badalzadeh R. Effect of endurance training and cinnamon supplementation on post-exercise oxidative responses in rats. Molecular biology research communications. 2014;3(4):269.
  14. JAHANI GR, FIROUZRAI M, MATIN HH, Tarverdizadeh B, AZARBAIJANI M, MOVASEGHI GR, et al. The effect of continuous and regular exercise on erytrocyte antioxidative enzymes activity and stress oxidative in young soccer players. 2010.
  15. Moghaddasi M, Javanmard SH, Reisi P, Tajadini M, Taati M. The effect of regular exercise on antioxidant enzyme activities and lipid peroxidation levels in both hippocampi after occluding one carotid in rat. The Journal of Physiological Sciences. 2014;64(5):325-32.
  16. Barari A, Bashiri J, FARZANEGI P, FAYYAZINIYA V. The effect of endurance and circuit resistance training on serum superoxide dismutase and heat shock protein 70 levels in inactive college students. 2015.
  17. Daniela M, Catalina L, Ilie O, Paula M, Daniel-Andrei I, Ioana B. Effects of Exercise Training on the Autonomic Nervous System with a Focus on Anti-Inflammatory and Antioxidants Effects. Antioxidants. 2022;11(2):350.
  18. Azamian Jazi A, Emdi S, Hemati S. Effect of Six Weeks of Continuous Running on Oxidative Stress, Lipid Peroxidation and Aerobic Power in Female Survivors of Breast Cancer. The Iranian Journal of Obstetrics, Gynecology and Infertility. 2017;19(38):24-32.
  19. Wang X, Wang Z, Tang D. Aerobic exercise alleviates inflammation, oxidative stress, and apoptosis in mice with chronic obstructive pulmonary disease. International Journal of Chronic Obstructive Pulmonary Disease. 2021; 16:1369.

Fathi Bayyatiani Z, Dabidi Roshan V, Ayaz A, Hoseinzadeh M. The relationship between the pro-inflammatory markers with lipid peroxidation after water-based regular exercise and ginger supplement in breast cancer. Daneshvar Medicine. 2013;21(1):61-76.

Sport Physiology
Volume 14, Issue 56
February 2023
Pages 147-176

  • Receive Date 24 April 2022
  • Revise Date 03 October 2022
  • Accept Date 19 October 2022