Tuberculosis and Respiratory Diseases

  • 제78권1호
  • /
  • Pages.8-17
  • /
  • 2015
  • /
  • 1738-3536(pISSN)
  • /
  • 2005-6184(eISSN)
대한결핵및호흡기학회 (The Korean Academy of Tuberculosis and Respiratory Diseases)
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Role of AMP-Activated Protein Kinase (AMPK) in Smoking-Induced Lung Inflammation and Emphysema

  • Lee, Jae Seung (Department of Pulmonary and Critical Care Medicine and Clinical Research Center for Chronic Obstructive Airway Diseases) ;
  • Park, Sun Joo (Department of Allergy and Clinical Immunology, Asthma Center, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Cho, You Sook (Department of Allergy and Clinical Immunology, Asthma Center, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Huh, Jin Won (Department of Pulmonary and Critical Care Medicine and Clinical Research Center for Chronic Obstructive Airway Diseases) ;
  • Oh, Yeon-Mok (Department of Pulmonary and Critical Care Medicine and Clinical Research Center for Chronic Obstructive Airway Diseases) ;
  • Lee, Sang-Do (Department of Pulmonary and Critical Care Medicine and Clinical Research Center for Chronic Obstructive Airway Diseases)
  • 투고 : 2014.07.22
  • 심사 : 2014.12.16
  • 발행 : 2015.01.30
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Background: AMP-activated protein kinase (AMPK) not only functions as an intracellular energy sensor and regulator, but is also a general sensor of oxidative stress. Furthermore, there is recent evidence that it participates in limiting acute inflammatory reactions, apoptosis and cellular senescence. Thus, it may oppose the development of chronic obstructive pulmonary disease. Methods: To investigate the role of AMPK in cigarette smoke-induced lung inflammation and emphysema we first compared cigarette smoking and polyinosinic-polycytidylic acid [poly(I:C)]-induced lung inflammation and emphysema in $AMPK{\alpha}1$-deficient ($AMPK{\alpha}1$-HT) mice and wild-type mice of the same genetic background. We then investigated the role of AMPK in the induction of interleukin-8 (IL-8) by cigarette smoke extract (CSE) in A549 cells. Results: Cigarette smoking and poly(I:C)-induced lung inflammation and emphysema were elevated in $AMPK{\alpha}1$-HT compared to wild-type mice. CSE increased AMPK activation in a CSE concentration- and time-dependent manner. 5-Aminoimidazole-4-carboxamide-1-${\beta}$-4-ribofuranoside (AICAR), an AMPK activator, decreased CSE-induced IL-8 production while Compound C, an AMPK inhibitor, increased it, as did pretreatment with an $AMPK{\alpha}1$-specific small interfering RNA. Conclusion: $AMPK{\alpha}1$-deficient mice have increased susceptibility to lung inflammation and emphysema when exposed to cigarette smoke, and AMPK appears to reduce lung inflammation and emphysema by lowering IL-8 production.

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참고문헌

  1. Global Initiative for Chronic Obstructive Lung Disease. Global strategy for the diagnosis, management, and prevention of COPD, updated 2013 [Internet]. Global Initiative for Chronic Obstructive Lung Disease; 2013 [cited 2014 Dec 1]. Available from: http://goldcopd.org.
  2. Shapiro SD. The pathogenesis of emphysema: the elastase: antielastase hypothesis 30 years later. Proc Assoc Am Physicians 1995;107:346-52.
  3. Fletcher C, Peto R. The natural history of chronic airflow obstruction. Br Med J 1977;1:1645-8. https://doi.org/10.1136/bmj.1.6077.1645
  4. Simmons MS, Connett JE, Nides MA, Lindgren PG, Kleerup EC, Murray RP, et al. Smoking reduction and the rate of decline in FEV(1): results from the Lung Health Study. Eur Respir J 2005;25:1011-7. https://doi.org/10.1183/09031936.05.00086804
  5. Falk JA, Minai OA, Mosenifar Z. Inhaled and systemic corticosteroids in chronic obstructive pulmonary disease. Proc Am Thorac Soc 2008;5:506-12. https://doi.org/10.1513/pats.200707-096ET
  6. MacNee W. Oxidative stress and chronic obstructive pulmonary disease. In: Siafakas NM, editor. European Respiratory Monograph, Vol 11. Monograph 38, Management of chronic obstructive pulmonary disease. Wakefield: European Respiratory Society; 2006. p. 100-29.
  7. Henson PM, Cosgrove GP, Vandivier RW. State of the art. Apoptosis and cell homeostasis in chronic obstructive pulmonary disease. Proc Am Thorac Soc 2006;3:512-6. https://doi.org/10.1513/pats.200603-072MS
  8. Aoshiba K, Nagai A. Senescence hypothesis for the pathogenetic mechanism of chronic obstructive pulmonary disease. Proc Am Thorac Soc 2009;6:596-601. https://doi.org/10.1513/pats.200904-017RM
  9. Ito K, Ito M, Elliott WM, Cosio B, Caramori G, Kon OM, et al. Decreased histone deacetylase activity in chronic obstructive pulmonary disease. N Engl J Med 2005;352:1967-76. https://doi.org/10.1056/NEJMoa041892
  10. Cosio MG, Saetta M, Agusti A. Immunologic aspects of chronic obstructive pulmonary disease. N Engl J Med 2009;360:2445-54. https://doi.org/10.1056/NEJMra0804752
  11. MacNee W, Tuder RM. New paradigms in the pathogenesis of chronic obstructive pulmonary disease I. Proc Am Thorac Soc 2009;6:527-31. https://doi.org/10.1513/pats.200905-027DS
  12. Kahn BB, Alquier T, Carling D, Hardie DG. AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab 2005;1:15-25. https://doi.org/10.1016/j.cmet.2004.12.003
  13. Kukidome D, Nishikawa T, Sonoda K, Imoto K, Fujisawa K, Yano M, et al. Activation of AMP-activated protein kinase reduces hyperglycemia-induced mitochondrial reactive oxygen species production and promotes mitochondrial biogenesis in human umbilical vein endothelial cells. Diabetes 2006;55:120-7. https://doi.org/10.2337/diabetes.55.01.06.db05-0943
  14. Reznick RM, Zong H, Li J, Morino K, Moore IK, Yu HJ, et al. Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metab 2007;5:151-6. https://doi.org/10.1016/j.cmet.2007.01.008
  15. Tang GJ, Wang HY, Wang JY, Lee CC, Tseng HW, Wu YL, et al. Novel role of AMP-activated protein kinase signaling in cigarette smoke induction of IL-8 in human lung epithelial cells and lung inflammation in mice. Free Radic Biol Med 2011;50:1492-502. https://doi.org/10.1016/j.freeradbiomed.2011.02.030
  16. Nerstedt A, Johansson A, Andersson CX, Cansby E, Smith U, Mahlapuu M. AMP-activated protein kinase inhibits IL-6-stimulated inflammatory response in human liver cells by suppressing phosphorylation of signal transducer and activator of transcription 3 (STAT3). Diabetologia 2010;53:2406-16. https://doi.org/10.1007/s00125-010-1856-z
  17. Myerburg MM, King JD Jr. Oyster NM, Fitch AC, Magill A, Baty CJ, et al. AMPK agonists ameliorate sodium and fluid transport and inflammation in cystic fibrosis airway epithelial cells. Am J Respir Cell Mol Biol 2010;42:676-84. https://doi.org/10.1165/2009-0147OC
  18. Zhao X, Zmijewski JW, Lorne E, Liu G, Park YJ, Tsuruta Y, et al. Activation of AMPK attenuates neutrophil proinflammatory activity and decreases the severity of acute lung injury. Am J Physiol Lung Cell Mol Physiol 2008;295:L497-504. https://doi.org/10.1152/ajplung.90210.2008
  19. Hoogendijk AJ, Pinhancos SS, van der Poll T, Wieland CW. AMP-activated protein kinase activation by 5-aminoimidazole-4-carbox-amide-1-beta-D-ribofuranoside (AICAR) reduces lipoteichoic acid-induced lung inflammation. J Biol Chem 2013;288:7047-52. https://doi.org/10.1074/jbc.M112.413138
  20. Kim TB, Kim SY, Moon KA, Park CS, Jang MK, Yun ES, et al. Five-aminoimidazole-4-carboxamide-1-beta-4-ribofuranoside attenuates poly (I:C)-induced airway inflammation in a murine model of asthma. Clin Exp Allergy 2007;37:1709-19. https://doi.org/10.1111/j.1365-2222.2007.02812.x
  21. Park CS, Bang BR, Kwon HS, Moon KA, Kim TB, Lee KY, et al. Metformin reduces airway inflammation and remodeling via activation of AMP-activated protein kinase. Biochem Pharmacol 2012;84:1660-70. https://doi.org/10.1016/j.bcp.2012.09.025
  22. Ido Y, Carling D, Ruderman N. Hyperglycemia-induced apoptosis in human umbilical vein endothelial cells: inhibition by the AMP-activated protein kinase activation. Diabetes 2002; 51:159-67. https://doi.org/10.2337/diabetes.51.1.159
  23. Jia F, Wu C, Chen Z, Lu G. AMP-activated protein kinase inhibits homocysteine-induced dysfunction and apoptosis in endothelial progenitor cells. Cardiovasc Drugs Ther 2011;25: 21-9. https://doi.org/10.1007/s10557-010-6277-1
  24. Sung JY, Woo CH, Kang YJ, Lee KY, Choi HC. AMPK induces vascular smooth muscle cell senescence via LKB1 dependent pathway. Biochem Biophys Res Commun 2011;413:143-8. https://doi.org/10.1016/j.bbrc.2011.08.071
  25. Salminen A, Kaarniranta K. AMP-activated protein kinase (AMPK) controls the aging process via an integrated signaling network. Ageing Res Rev 2012;11:230-41. https://doi.org/10.1016/j.arr.2011.12.005
  26. Wang Y, Liang Y, Vanhoutte PM. SIRT1 and AMPK in regulating mammalian senescence: a critical review and a working model. FEBS Lett 2011;585:986-94. https://doi.org/10.1016/j.febslet.2010.11.047
  27. Lee JH, Lee DS, Kim EK, Choe KH, Oh YM, Shim TS, et al. Simvastatin inhibits cigarette smoking-induced emphysema and pulmonary hypertension in rat lungs. Am J Respir Crit Care Med 2005;172:987-93. https://doi.org/10.1164/rccm.200501-041OC
  28. Thurlbeck WM. Measurement of pulmonary emphysema. Am Rev Respir Dis 1967;95:752-64.
  29. Huh JW, Kim SY, Lee JH, Lee JS, Van Ta Q, Kim M, et al. Bone marrow cells repair cigarette smoke-induced emphysema in rats. Am J Physiol Lung Cell Mol Physiol 2011;301:L255-66. https://doi.org/10.1152/ajplung.00253.2010
  30. Frankenfeld CN, Rosenbaugh MR, Fogarty BA, Lunte SM. Separation and detection of peroxynitrite and its metabolites by capillary electrophoresis with UV detection. J Chromatogr A 2006;1111:147-52. https://doi.org/10.1016/j.chroma.2005.05.027
  31. Yoshida T, Tuder RM. Pathobiology of cigarette smokeinduced chronic obstructive pulmonary disease. Physiol Rev 2007;87:1047-82. https://doi.org/10.1152/physrev.00048.2006
  32. Barnes PJ. Mediators of chronic obstructive pulmonary disease. Pharmacol Rev 2004;56:515-48. https://doi.org/10.1124/pr.56.4.2
  33. Hellermann GR, Nagy SB, Kong X, Lockey RF, Mohapatra SS. Mechanism of cigarette smoke condensate-induced acute inflammatory response in human bronchial epithelial cells. Respir Res 2002;3:22. https://doi.org/10.1186/rr172
  34. Witherden IR, Vanden Bon EJ, Goldstraw P, Ratcliffe C, Pastorino U, Tetley TD. Primary human alveolar type II epithelial cell chemokine release: effects of cigarette smoke and neutrophil elastase. Am J Respir Cell Mol Biol 2004;30:500-9. https://doi.org/10.1165/rcmb.4890
  35. Masubuchi T, Koyama S, Sato E, Takamizawa A, Kubo K, Sekiguchi M, et al. Smoke extract stimulates lung epithelial cells to release neutrophil and monocyte chemotactic activity. Am J Pathol 1998;153:1903-12. https://doi.org/10.1016/S0002-9440(10)65704-5
  36. Keatings VM, Collins PD, Scott DM, Barnes PJ. Differences in interleukin-8 and tumor necrosis factor-alpha in induced sputum from patients with chronic obstructive pulmonary disease or asthma. Am J Respir Crit Care Med 1996;153:530-4. https://doi.org/10.1164/ajrccm.153.2.8564092
  37. Aaron SD, Angel JB, Lunau M, Wright K, Fex C, Le Saux N, et al. Granulocyte inflammatory markers and airway infection during acute exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2001;163:349-55. https://doi.org/10.1164/ajrccm.163.2.2003122
  38. Park DW, Jiang S, Tadie JM, Stigler WS, Gao Y, Deshane J, et al. Activation of AMPK enhances neutrophil chemotaxis and bacterial killing. Mol Med 2013;19:387-98.
  39. Li XN, Song J, Zhang L, LeMaire SA, Hou X, Zhang C, et al. Activation of the AMPK-FOXO3 pathway reduces fatty acidinduced increase in intracellular reactive oxygen species by upregulating thioredoxin. Diabetes 2009;58:2246-57. https://doi.org/10.2337/db08-1512
  40. Xie Z, Zhang J, Wu J, Viollet B, Zou MH. Upregulation of mitochondrial uncoupling protein-2 by the AMP-activated protein kinase in endothelial cells attenuates oxidative stress in diabetes. Diabetes 2008;57:3222-30. https://doi.org/10.2337/db08-0610

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