Heme oxygenase-1-mediated autophagy protects against pulmonary endothelial cell death and development of emphysema in cadmium-treated mice

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 309, Issue 3, 2015, Pages L280-L292

  Surolia, Ranu ^a   Karki, Suman ^a   Kim, Hyunki ^b   Yu, Zhihong ^c   Kulkarni, Tejaswini ^a   Mirov, Sergey B ^d   Carter, A Brent ^a,d   Rowe, Steven M ^a,d,e   Matalon, Sadis ^c   Thannickal, Victor J ^a   Agarwal, Anupam ^d   Antony, Veena B ^a  

^a and Clinical Center   (United States)

^b University of Alabama   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e University of Alabama at Birmingham and Children's Hospital   (United States)

Author keywords

Autophagy; Cadmium induced emphysema; Heme oxygenase 1; Pulmonary endothelial cells

Indexed keywords

AUTOPHAGY PROTEIN 5; BECLIN 1; CADMIUM CHLORIDE; CASPASE 3; HEME OXYGENASE 1; MICROTUBULE ASSOCIATED PROTEIN 1; CADMIUM; HMOX1 PROTEIN, MOUSE; MEMBRANE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BACTERIAL ARTIFICIAL CHROMOSOME; CAPILLARY WALL; CELL DEATH; CELL PROTECTION; EMPHYSEMA; HISTOPATHOLOGY; LUNG ALVEOLUS; LUNG ENDOTHELIUM; LUNG FUNCTION TEST; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CELL CULTURE; CHEMICALLY INDUCED; ENDOTHELIUM CELL; ENZYMOLOGY; KNOCKOUT MOUSE; LUNG; LUNG EMPHYSEMA; PATHOLOGY; PHYSIOLOGY;

ANIMALS; AUTOPHAGY; CADMIUM; CELLS, CULTURED; ENDOTHELIAL CELLS; HEME OXYGENASE-1; LUNG; MEMBRANE PROTEINS; MICE, INBRED C57BL; MICE, KNOCKOUT; PULMONARY EMPHYSEMA;

EID: 84937616611     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00097.2015     Document Type: Article

References (78)

1. American Thoracic Society. Standards for the diagnosis and care of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med152: S77–S121, 1995.
2. Aldonyte R, Hutchinson TE, Jin B, Brantly M, Block E, Patel J, Zhang J. Endothelial alpha-1-antitrypsin attenuates cigarette smoke induced apoptosis in vitro. COPD5: 153–162, 2008.
3. Bertin G, Averbeck D. Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review). Biochimie88: 1549–1559, 2006.
4. Bracke KR, D’Hulst AI, Maes T, Moerloose KB, Demedts IK, Lebecque S, Joos GF, Brusselle GG. Cigarette smoke-induced pulmonary inflammation and emphysema are attenuated in CCR6-deficient mice. J Immunol177: 4350–4359, 2006.
5. Chargui A, Zekri S, Jacquillet G, Rubera I, Ilie M, Belaid A, Duranton C, Tauc M, Hofman P, Poujeol P, El May MV, Mograbi B. Cadmium-induced autophagy in rat kidney: an early biomarker of subtoxic exposure. Toxicol Sci121: 31–42, 2011.
6. Chen DJ, Xu YM, Du JY, Huang DY, Lau AT. Cadmium induces cytotoxicity in human bronchial epithelial cells through upregulation of eIF5A1 and NF-kappaB. Biochem Biophys Res Commun445: 95–99, 2014.
7. Chen ZH, Kim HP, Ryter SW, Choi AM. Identifying targets for COPD treatment through gene expression analyses. Int J Chron Obstruct Pulmon Dis3: 359–370, 2008.
8. Chen ZH, Lam HC, Jin Y, Kim HP, Cao J, Lee SJ, Ifedigbo E, Parameswaran H, Ryter SW, Choi AM. Autophagy protein microtubule- associated protein 1 light chain-3B (LC3B) activates extrinsic apoptosis during cigarette smoke-induced emphysema. Proc Natl Acad Sci USA107: 18880–18885, 2010.
9. Churg A, Cosio M, Wright JL. Mechanisms of cigarette smoke-induced COPD: insights from animal models. Am J Physiol Lung Cell Mol Physiol294: L612–L631, 2008.
10. Courville CA, Tidwell S, Liu B, Accurso FJ, Dransfield MT, Rowe SM. Acquired defects in CFTR-dependent beta-adrenergic sweat secretion in chronic obstructive pulmonary disease. Respir Res15: 25, 2014.
11. Dhami R, Gilks B, Xie C, Zay K, Wright JL, Churg A. Acute cigarette smoke-induced connective tissue breakdown is mediated by neutrophils and prevented by alpha1-antitrypsin. Am J Respir Cell Mol Biol22: 244–252, 2000.
12. Ding WX, Ni HM, Gao W, Yoshimori T, Stolz DB, Ron D, Yin XM. Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am J Pathol171: 513–524, 2007.
13. Dolinay T, Choi AM, Ryter SW. Heme Oxygenase-1/CO as protective mediators in cigarette smoke- induced lung cell injury and chronic obstructive pulmonary disease. Curr Pharm Biotechnol13: 769–776, 2012.
14. Dong Z, Wang L, Xu J, Li Y, Zhang Y, Zhang S, Miao J. Promotion of autophagy and inhibition of apoptosis by low concentrations of cadmium in vascular endothelial cells. Toxicol In Vitro23: 105–110, 2009.
15. Dransfield MT, Wilhelm AM, Flanagan B, Courville C, Tidwell SL, Raju SV, Gaggar A, Steele C, Tang LP, Liu B, Rowe SM. Acquired cystic fibrosis transmembrane conductance regulator dysfunction in the lower airways in COPD. Chest144: 498–506, 2013.
16. Halbert RJ, Natoli JL, Gano A, Badamgarav E, Buist AS, Mannino DM. Global burden of COPD: systematic review and meta-analysis. Eur Respir J28: 523–532, 2006.
17. Hautamaki RD, Kobayashi DK, Senior RM, Shapiro SD. Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science277: 2002–2004, 1997.
18. Hendrick DJ. Smoking, cadmium, and emphysema. Thorax59: 184–185, 2004.
19. Hewitt M, Creel A, Estell K, Davis IC, Schwiebert LM. Acute exercise decreases airway inflammation, but not responsiveness, in an allergic asthma model. Am J Respir Cell Mol Biol40: 83–89, 2009.
20. Hill-Kapturczak N, Sikorski E, Voakes C, Garcia J, Nick HS, Agarwal A. An internal enhancer regulates heme- and cadmium-mediated induction of human heme oxygenase-1. Am J Physiol Renal Physiol285: F515–F523, 2003.
21. Hogg JC. Pathophysiology of airflow limitation in chronic obstructive pulmonary disease. Lancet364: 709–721, 2004.
22. Jin T, Lu J, Nordberg M. Toxicokinetics and biochemistry of cadmium with special emphasis on the role of metallothionein. Neurotoxicology19: 529–535, 1998.
23. Jin Y, Zhang S, Tao R, Huang J, He X, Qu L, Fu Z. Oral exposure of mice to cadmium (II), chromium (VI) and their mixture induce oxidativeand endoplasmic reticulum-stress mediated apoptosis in the livers. Environ Toxicol. In press.
24. Jurkuvenaite A, Benavides GA, Komarova S, Doran SF, Johnson M, Aggarwal S, Zhang J, Darley-Usmar VM, Matalon S. Upregulation of autophagy decreases chlorine gas induced mitochondrial injury and lung inflammation. Free Radic Biol Med85: 83–94, 2015.
25. Kasahara Y, Tuder RM, Cool CD, Lynch DA, Flores SC, Voelkel NF. Endothelial cell death and decreased expression of vascular endothelial growth factor and vascular endothelial growth factor receptor 2 in emphysema. Am J Respir Crit Care Med163: 737–744, 2001.
26. Kasahara Y, Tuder RM, Taraseviciene-Stewart L, Le Cras TD, Abman S, Hirth PK, Waltenberger J, Voelkel NF. Inhibition of VEGF receptors causes lung cell apoptosis and emphysema. J Clin Invest106: 1311–1319, 2000.
27. Kim HP, Wang X, Chen ZH, Lee SJ, Huang MH, Wang Y, Ryter SW, Choi AM. Autophagic proteins regulate cigarette smoke-induced apoptosis: protective role of heme oxygenase-1. Autophagy4: 887–895, 2008.
28. Kim J, Zarjou A, Traylor AM, Bolisetty S, Jaimes EA, Hull TD, George JF, Mikhail FM, Agarwal A. In vivo regulation of the heme oxygenase-1 gene in humanized transgenic mice. Kidney Int 82: 278–291, 2012.
29. Kochanek KD, Xu J, Murphy SL, Minino AM, Kung HC. Deaths: final data for 2009. National vital statistics reports: from the Centers for Disease Control and Prevention, National Center for Health Statistics. Natl Vital Stat Syst60: 1–116, 2011.
30. Konrad FM, Braun S, Ngamsri KC, Vollmer I, Reutershan J. Heme oxygenase-1 attenuates acute pulmonary inflammation by decreasing the release of segmented neutrophils from the bone marrow. Am J Physiol Lung Cell Mol Physiol307: L707–L717, 2014.
31. Kundu S, Sengupta S, Chatterjee S, Mitra S, Bhattacharyya A. Cadmium induces lung inflammation independent of lung cell proliferation: a molecular approach. J Inflamm6: 19, 2009.
32. Leberl M, Kratzer A, Taraseviciene-Stewart L. Tobacco smoke induced COPD/emphysema in the animal model-are we all on the same page? Front Physiol4: 91, 2013.
33. Li M, Xia T, Jiang CS, Li LJ, Fu JL, Zhou ZC. Cadmium directly induced the opening of membrane permeability pore of mitochondria which possibly involved in cadmium-triggered apoptosis. Toxicology194: 19–33, 2003.
34. Liebow AA. Pulmonary emphysema with special reference to vascular changes. Am Rev Respir Dis80: 67–93, 1959.
35. Lim SC, Hahm KS, Lee SH, Oh SH. Autophagy involvement in cadmium resistance through induction of multidrug resistance-associated protein and counterbalance of endoplasmic reticulum stress WI38 lung epithelial fibroblast cells. Toxicology276: 18–26, 2010.
36. Lopez de Figueroa P, Lotz M, Blanco FJ, Carames B. Autophagy activation protects from mitochondrial dysfunction in human chondrocytes. Arthritis Rheumatol67: 966–976, 2015.
37. Maestrelli P, Paska C, Saetta M, Turato G, Nowicki Y, Monti S, Formichi B, Miniati M, Fabbri LM. Decreased haem oxygenase-1 and increased inducible nitric oxide synthase in the lung of severe COPD patients. Eur Respir J21: 971–976, 2003.
38. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol8: 741–752, 2007.
39. Martinet W, Agostinis P, Vanhoecke B, Dewaele M, De Meyer GR. Autophagy in disease: a double-edged sword with therapeutic potential. Clin Sci (Lond)116: 697–712, 2009.
40. Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy3: 542–545, 2007.
41. Morissette MC, Parent J, Milot J. Alveolar epithelial and endothelial cell apoptosis in emphysema: what we know and what we need to know. Int J Chron Obstruct Pulmon Dis4: 19–31, 2009.
42. Morse D, Rosas IO. Tobacco smoke-induced lung fibrosis and emphysema. Annu Rev Physiol76: 493–513, 2014.
43. Nakahira K, Choi AM. Autophagy: a potential therapeutic target in lung diseases. Am J Physiol Lung Cell Mol Physiol305: L93–L107, 2013.
44. Nakahira K, Cloonan SM, Mizumura K, Choi AM, Ryter SW. Autophagy: a crucial moderator of redox balance, inflammation, and apoptosis in lung disease. Antioxid Redox Signal20: 474–494, 2014.
45. Nyunoya T, Mebratu Y, Contreras A, Delgado M, Chand HS, Tesfaigzi Y. Molecular processes that drive cigarette smoke-induced epithelial cell fate of the lung. Am J Respir Cell Mol Biol50: 471–482, 2014.
46. Overbeek SA, Braber S, Koelink PJ, Henricks PA, Mortaz E, LoTam Loi AT, Jackson PL, Garssen J, Wagenaar GT, Timens W, Koenderman L, Blalock JE, Kraneveld AD, Folkerts G. Cigarette smokeinduced collagen destruction; key to chronic neutrophilic airway inflammation? PLoS One8: e55612, 2013.
47. Paakko P, Kokkonen P, Anttila S, Kalliomaki PL. Cadmium and chromium as markers of smoking in human lung tissue. Environ Res49: 197–207, 1989.
48. Petrusca DN, Van Demark M, Gu Y, Justice MJ, Rogozea A, Hubbard WC, Petrache I. Smoking exposure induces human lung endothelial cell adaptation to apoptotic stress. Am J Respir Cell Mol Biol50: 513–525, 2014.
49. Raju SV, Jackson PL, Courville CA, McNicholas CM, Sloane PA, Sabbatini G, Tidwell S, Tang LP, Liu B, Fortenberry JA, Jones CW, Boydston JA, Clancy JP, Bowen LE, Accurso FJ, Blalock JE, Dransfield MT, Rowe SM. Cigarette smoke induces systemic defects in cystic fibrosis transmembrane conductance regulator function. Am J Respir Crit Care Med188: 1321–1330, 2013.
50. Raval CM, Lee PJ. Heme oxygenase-1 in lung disease. Curr Drug Targets11: 1532–1540, 2010.
51. Rennolds J, Butler S, Maloney K, Boyaka PN, Davis IC, Knoell DL, Parinandi NL, Cormet-Boyaka E. Cadmium regulates the expression of the CFTR chloride channel in human airway epithelial cells. Toxicol Sci116: 349–358, 2010.
52. Rinaldi M, Maes K, De Vleeschauwer S, Thomas D, Verbeken EK, Decramer M, Janssens W, Gayan-Ramirez GN. Long-term nose-only cigarette smoke exposure induces emphysema and mild skeletal muscle dysfunction in mice. Dis Model Mech5: 333–341, 2012.
53. Ryter SW, Lee SJ, Choi AM. Autophagy in cigarette smoke-induced chronic obstructive pulmonary disease. Expert Rev Respir Med4: 573–584, 2010.
54. Sakhatskyy P, Gabino Miranda GA, Newton J, Lee CG, Choudhary G, Vang A, Rounds S, Lu Q. Cigarette smoke-induced lung endothelial apoptosis and emphysema are associated with impairment of FAK and eIF2alpha. Microvasc Res94: 80–89, 2014.
55. Sasaki M, Chubachi S, Kameyama N, Sato M, Haraguchi M, Miyazaki M, Takahashi S, Betsuyaku T. Evaluation of cigarette smokeinduced emphysema in mice using quantitative micro-computed tomography. Am J Physiol Lung Cell Mol Physiol308: L1039–L1045, 2015.
56. Schonewolf CA, Mehta M, Schiff D, Wu H, Haffty BG, Karantza V, Jabbour SK. Autophagy inhibition by chloroquine sensitizes HT-29 colorectal cancer cells to concurrent chemoradiation. World J Gastrointest Oncol6: 74–82, 2014.
57. Segura-Valdez L, Pardo A, Gaxiola M, Uhal BD, Becerril C, Selman M. Upregulation of gelatinases A and B, collagenases 1 and 2, and increased parenchymal cell death in COPD. Chest117: 684–694, 2000.
58. Shapiro SD, Goldstein NM, Houghton AM, Kobayashi DK, Kelley D, Belaaouaj A. Neutrophil elastase contributes to cigarette smoke-induced emphysema in mice. Am J Pathol163: 2329–2335, 2003.
59. Shapiro SD, Senior Matrix metalloproteinases RM. Matrix degradation and more. Am J Respir Cell Mol Biol20: 1100–1102, 1999.
60. Shinohara T, Kaneko T, Nagashima Y, Ueda A, Tagawa A, Ishigatsubo Y. Adenovirus-mediated transfer and overexpression of heme oxygenase 1 cDNA in lungs attenuates elastase-induced pulmonary emphysema in mice. Hum Gene Ther16: 318–327, 2005.
61. Sikorski EM, Hock T, Hill-Kapturczak N, Agarwal A. The story so far: Molecular regulation of the heme oxygenase-1 gene in renal injury. Am J Physiol Renal Physiol286: F425–F441, 2004.
62. Slebos DJ, Kerstjens HA, Rutgers SR, Kauffman HF, Choi AM, Postma DS. Haem oxygenase-1 expression is diminished in alveolar macrophages of patients with COPD. Eur Respir J23: 652–653; author reply 653, 2004.
63. Sloane PA, Shastry S, Wilhelm A, Courville C, Tang LP, Backer K, Levin E, Raju SV, Li Y, Mazur M, Byan-Parker S, Grizzle W, Sorscher EJ, Dransfield MT, Rowe SM. A pharmacologic approach to acquired cystic fibrosis transmembrane conductance regulator dysfunction in smoking related lung disease. PLoS One7: e39809, 2012.
64. Snelgrove RJ, Jackson PL, Hardison MT, Noerager BD, Kinloch A, Gaggar A, Shastry S, Rowe SM, Shim YM, Hussell T, Blalock JE. A critical role for LTA4H in limiting chronic pulmonary neutrophilic inflammation. Science330: 90–94, 2010.
65. Snider GL, Lucey EC, Faris B, Jung-Legg Y, Stone PJ, Franzblau C. Cadmium-chloride-induced air-space enlargement with interstitial pulmonary fibrosis is not associated with destruction of lung elastin. Implications for the pathogenesis of human emphysema. Am Rev Respir Dis137: 918–923, 1988.
66. Sohal SS, Reid D, Soltani A, Weston S, Muller HK, Wood-Baker R, Walters EH. Changes in airway histone deacetylase2 in smokers and COPD with inhaled corticosteroids: a randomized controlled trial. PLoS One8: e64833, 2013.
67. Son YO, Pratheeshkumar P, Roy RV, Hitron JA, Wang L, Zhang Z, Shi X. Nrf2/p62 signaling in apoptosis resistance and its role in cadmiuminduced carcinogenesis. J Biol Chem289: 28660–28675, 2014.
68. Son YO, Wang X, Hitron JA, Zhang Z, Cheng S, Budhraja A, Ding S, Lee JC, Shi X. Cadmium induces autophagy through ROS-dependent activation of the LKB1-AMPK signaling in skin epidermal cells. Toxicol Appl Pharmacol255: 287–296, 2011.
69. Tetley TD. Inflammatory cells and chronic obstructive pulmonary disease. Curr Drug Targets Inflamm Allergy4: 607–618, 2005.
70. Urbanek T, Kuczmik W, Basta-Kaim A, Gabryel B. Rapamycin induces of protective autophagy in vascular endothelial cells exposed to oxygen-glucose deprivation. Brain Res1553: 1–11, 2014.
71. Vecchio D, Arezzini B, Pecorelli A, Valacchi G, Martorana PA, Gardi C. Reactivity of mouse alveolar macrophages to cigarette smoke is strain dependent. Am J Physiol Lung Cell Mol Physiol298: L704–L713, 2010.
72. Wang SH, Shih YL, Ko WC, Wei YH, Shih CM. Cadmium-induced autophagy and apoptosis are mediated by a calcium signaling pathway. Cell Mol Life Sci65: 3640–3652, 2008.
73. Wang X, Zhang J, Fu J, Wang J, Ye S, Liu W, Shao C. Role of ROS-mediated autophagy in radiation-induced bystander effect of hepatoma cells. Int J Radiat Biol91: 452–458, 2015.
74. Yamada H, Damiano VV, Tsang AL, Meranze DR, Glasgow J, Abrams WR, Weinbaum G. Neutrophil degranulation in cadmium-chloride-induced acute lung inflammation. Am J Pathol109: 145–156, 1982.
75. Yamada N, Yamaya M, Okinaga S, Nakayama K, Sekizawa K, Shibahara S, Sasaki H. Microsatellite polymorphism in the heme oxygenase- 1 gene promoter is associated with susceptibility to emphysema. Am J Hum Genet66: 187–195, 2000.
76. Yasuo M, Mizuno S, Allegood J, Kraskauskas D, Bogaard HJ, Spiegel S, Voelkel NF. Fenretinide causes emphysema, which is prevented by sphingosine 1-phosphate. PLoS One8: e53927, 2013.
77. Zhang Y, Jiang G, Sauler M, Lee PJ. Lung endothelial HO-1 targeting in vivo using lentiviral miRNA regulates apoptosis and autophagy during oxidant injury. FASEB J27: 4041–4058, 2013.
78. Zhu YK, Liu XD, Skold CM, Umino T, Wang HJ, Spurzem JR, Kohyama T, Ertl RF, Rennard SI. Synergistic neutrophil elastasecytokine interaction degrades collagen in three-dimensional culture. Am J Physiol Lung Cell Mol Physiol281: L868–L878, 2001.