Z α1-antitrypsin confers a proinflammatory phenotype that contributes to chronic obstructive pulmonary disease

American Journal of Respiratory and Critical Care Medicine

Volumn 189, Issue 8, 2014, Pages 909-931

  Alam, Samuel ^a   Li, Zhenjun ^b   Atkinson, Carl ^b   Jonigk, Danny ^c   Janciauskiene, Sabina ^d   Mahadeva, Ravi ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c Institute of Pathology   (Germany)

^d HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

COPD; ER stress; Oxidation; Polymerization; 1 antitrypsin

Indexed keywords

ALPHA 1-ANTITRYPSIN; ANIMALS; BIOLOGICAL MARKERS; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM; GLUTAMIC ACID; HUMANS; INTERLEUKIN-6; LYSINE; MACROPHAGES; MICE; MICE, TRANSGENIC; MUTATION; NEUTROPHILS; NF-KAPPA B; OXIDATIVE STRESS; PHENOTYPE; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; TOBACCO SMOKE POLLUTION; TRYPSIN INHIBITORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84898959231     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201308-1458OC     Document Type: Article

References (52)

1. Stoller JK, Aboussouan LS. A review of a1-antitrypsin deficiency. Am J Respir Crit Care Med 2012;185:246-259.
2. Eriksson S. Studies in a 1-antitrypsin deficiency. Acta Med Scand Suppl 1965;432:1-85.
3. Blanco I, de Serres FJ, Fernandez-Bustillo E, Lara B, Miravitlles M. Estimated numbers and prevalence of PIS and PIZ alleles of alpha1-antitrypsin deficiency in European countries. Eur Respir J 2006;27:77-84.
4. de Serres FJ, Blanco I, Ferná ndez-Bustillo E. Genetic epidemiology of alpha-1 antitrypsin deficiency in North America and Australia/New Zealand: Australia, Canada, New Zealand and the United States of America. Clin Genet 2003;64:382-397.
5. Lomas DA, Evans DL, Finch JT, Carrell RW. The mechanism of Z alpha 1-antitrypsin accumulation in the liver. Nature 1992;357:605-607.
6. Alam S, Mahadeva R. Cellular consequences of Z alpha-1 antitrypsin accumulation and prospects for therapy. EMJ Hepatol 2013;1:44-51.
7. Teckman JH. Liver disease in alpha-1 antitrypsin deficiency: current understanding and future therapy. COPD 2013;10:35-43.
8. Perlmutter DH. Liver injury in alpha1-antitrypsin deficiency: an aggregated protein induces mitochondrial injury. J Clin Invest 2002; 110:1579-1583.
9. Perlmutter DH. Pathogenesis of chronic liver injury and hepatocellular carcinoma in alpha-1-antitrypsin deficiency. Pediatr Res 2006;60: 233-238.
10. Laurell CB, Eriksson S. The electrophoretic alpha-1-globulin pattern of serum in alpha-1 antitrypsin deficiency. Scand J Clin Lab Invest 1963;15:132-140.
11. Snider GL, Lucey EC, Stone PJ. Pitfalls in antiprotease therapy of emphysema. Am J Respir Crit Care Med 1994;150:S131-S137. (Pubitemid 24364337)
12. Stockley RA. Cellular and biochemical mechanisms in chronic obstructive pulmonary disease. In: Calverley P, Pride N, editors. Chronic obstructive pulmonary disease. London: Chapman and Hall; 1995. pp. 93-133.
13. Silverman EK, Palmer LJ, Mosley JD, Barth M, Senter JM, Brown A, Drazen JM, Kwiatkowski DJ, Chapman HA, Campbell EJ, et al. Genomewide linkage analysis of quantitative spirometric phenotypes in severe early-onset chronic obstructive pulmonary disease. Am J Hum Genet 2002;70:1229-1239.
14. Seersholm N, Kok-Jensen A, Dirksen A. Decline in FEV1 among patients with severe hereditary alpha 1-antitrypsin deficiency type PiZ. Am J Respir Crit Care Med 1995;152:1922-1925.
15. DeMeo DL, Campbell EJ, Brantly ML, Barker AF, Eden E, McElvaney NG, Rennard SI, Stocks JM, Stoller JK, Strange C, et al. Heritability of lung function in severe alpha-1 antitrypsin deficiency. Hum Hered 2009;67:38-45.
16. Morrison HM, Kramps JA, Burnett D, Stockley RA. Lung lavage fluid from patients with alpha 1-proteinase inhibitor deficiency or chronic obstructive bronchitis: anti-elastase function and cell profile. Clin Sci (Lond) 1987;72:373-381.
17. Mulgrew AT, Taggart CC, Lawless MW, Greene CM, Brantly ML, O'Neill SJ, McElvaney NG. Z alpha1-antitrypsin polymerizes in the lung and acts as a neutrophil chemoattractant. Chest 2004;125:1952-1957.
18. Mahadeva R, Atkinson C, Li Z, Stewart S, Janciauskiene S, Kelley DG, Parmar J, Pitman R, Shapiro SD, Lomas DA. Polymers of Z alpha1-antitrypsin co-localize with neutrophils in emphysematous alveoli and are chemotactic in vivo. Am J Pathol 2005;166:377-386.
19. Hill AT, Bayley DL, Campbell EJ, Hill SL, Stockley RA. Airways inflammation in chronic bronchitis: the effects of smoking and alpha1-antitrypsin deficiency. Eur Respir J 2000;15:886-890.
20. Alam S, Li Z, Janciauskiene S, Mahadeva R. Oxidation of Z a1-antitrypsin by cigarette smoke induces polymerization: a novel mechanism of early-onset emphysema. Am J Respir Cell Mol Biol 2011;45:261-269.
21. Hautamaki RD, Kobayashi DK, Senior RM, Shapiro SD. Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science 1997;277:2002-2004.
22. Ali R, Perfumo S, della Rocca C, Amicone L, Pozzi L, McCullagh P, Millward-Sadler H, Edwards Y, Povey S, Tripodi M. Evaluation of a transgenic mouse model for alpha-1-antitrypsin (AAT) related liver disease. Ann Hum Genet 1994;58:305-320.
23. Li Z, Alam S, Wang J, Sandstrom CS, Janciauskiene S, Mahadeva R. Oxidized alpha1-antitrypsin stimulates the release of monocyte chemotactic protein-1 from lung epithelial cells: potential role in emphysema. Am J Physiol Lung Cell Mol Physiol 2009;297: L388-L400.
24. Alam S, Wang J, Janciauskiene S, Mahadeva R. Preventing and reversing the cellular consequences of Z alpha-1 antitrypsin accumulation by targeting s4A. J Hepatol 2012;57:116-124.
25. Theophile K, Jonigk D, Kreipe H, Bock O. Amplification of mRNA from laser-microdissected single or clustered cells in formalin-fixed and paraffin-embedded tissues for application in quantitative real-time PCR. Diagn Mol Pathol 2008;17:101-106.
26. Jonigk D, Golpon H, Bockmeyer CL, Maegel L, Hoeper MM, Gottlieb J, Nickel N, Hussein K, Maus U, Lehmann U, et al. Plexiform lesions in pulmonary arterial hypertension composition, architecture, and microenvironment. Am J Pathol 2011;179:167-179.
27. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 2005;5:953-964.
28. Chang YP, Mahadeva R, Chang WS, Lin SC, Chu YH. Small-molecule peptides inhibit Z alpha1-antitrypsin polymerization. J Cell Mol Med 2009;13:2304-2316.
29. Harding HP, Zyryanova AF, Ron D. Uncoupling proteostasis and development in vitro with a small molecule inhibitor of the pancreatic endoplasmic reticulum kinase, PERK. J Biol Chem 2012;287: 44338-44344.
30. Reynolds PR, Cosio MG, Hoidal Jr. Cigarette smoke-induced EGR-1 upregulates proinflammatory cytokines in pulmonary epithelial cells. Am J Respir Cell Mol Biol 2006;35:314-319.
31. Rahman I, van Schadewijk AA, Hiemstra PS, Stolk J, van Krieken JH, MacNee W, de Boer WI. Localization of gamma-glutamylcysteine synthetase messenger RNA expression in lungs of smokers and patients with chronic obstructive pulmonary disease. Free Radic Biol Med 2000;28:920-925.
32. Yoshida T, Tuder RM. Pathobiology of cigarette smoke-induced chronic obstructive pulmonary disease. Physiol Rev 2007;87: 1047-1082.
33. Ajuebor MN, Flower RJ, Hannon R, Christie M, Bowers K, Verity A, Perretti M. Endogenous monocyte chemoattractant protein-1 recruits monocytes in the zymosan peritonitis model. J Leukoc Biol 1998;63:108-116.
34. Vlahos R, Bozinovski S, Jones JE, Powell J, Gras J, Lilja A, Hansen MJ, Gualano RC, Irving L, Anderson GP. Differential protease, innate immunity, and NF-kappaB induction profiles during lung inflammation induced by subchronic cigarette smoke exposure in mice. Am J Physiol Lung Cell Mol Physiol 2006;290:L931-L945. (Pubitemid 43725055)
35. Hidvegi T, Schmidt BZ, Hale P, Perlmutter DH. Accumulation of mutant alpha1-antitrypsin Z in the endoplasmic reticulum activates caspases-4 and-12, NFkappaB, and BAP31 but not the unfolded protein response. J Biol Chem 2005;280:39002-39015.
36. Hidvegi T, Mirnics K, Hale P, Ewing M, Beckett C, Perlmutter DH. Regulator of G Signaling 16 is a marker for the distinct endoplasmic reticulum stress state associated with aggregated mutant alpha1-antitrypsin Z in the classical form of alpha1-antitrypsin deficiency. J Biol Chem 2007;282:27769-27780.
37. Malhi H, Kaufman RJ. Endoplasmic reticulum stress in liver disease. J Hepatol 2011;54:795-809.
38. Kelly E, Greene CM, Carroll TP, McElvaney NG, O'Neill SJ. Selenoprotein S/SEPS1 modifies endoplasmic reticulum stress in Z variant alpha1- antitrypsin deficiency. J Biol Chem 2009;284:16891-16897.
39. Pahl HL, Baeuerle PA. A novel signal transduction pathway from the endoplasmic reticulum to the nucleus is mediated by transcription factor NF-k B. EMBO J 1995;14:2580-2588.
40. Jorgensen E, Stinson A, Shan L, Yang J, Gietl D, Albino AP. Cigarette smoke induces endoplasmic reticulum stress and the unfolded protein response in normal and malignant human lung cells. BMC Cancer 2008;8:229.
41. Zhang K, Kaufman RJ. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008;454:455-462.
42. Rahman I, MacNee W. Role of transcription factors in inflammatory lung diseases. Thorax 1998;53:601-612.
43. Matheson NR, Wong PS, Travis J. Enzymatic inactivation of human alpha-1-proteinase inhibitor by neutrophil myeloperoxidase. Biochem Biophys Res Commun 1979;88:402-409.
44. Matheson NR, Travis J. Differential effects of oxidizing agents on human plasma alpha 1-proteinase inhibitor and human neutrophil myeloperoxidase. Biochemistry 1985;24:1941-1945.
45. Warter J, Storck D, Grosshans E, Metais P, Kuntz JL, Klumpp T. Weber-Christian syndrome associated with an alpha-1 antitrypsin deficiency. Familial investigation [in French]. Ann Med Interne (Paris) 1972;123:877-882.
46. Savige JA, Chang L, Cook L, Burdon J, Daskalakis M, Doery J. Alpha 1-antitrypsin deficiency and anti-proteinase 3 antibodies in antineutrophil cytoplasmic antibody (ANCA)-associated systemic vasculitis. Clin Exp Immunol 1995;100:194-197.
47. Wu Y, Whitman I, Molmenti E, Moore K, Hippenmeyer P, Perlmutter DH. A lag in intracellular degradation of mutant alpha 1-antitrypsin correlates with the liver disease phenotype in homozygous PiZZ alpha 1-antitrypsin deficiency. Proc Natl Acad Sci USA 1994;91: 9014-9018.
48. Hidvegi T, Ewing M, Hale P, Dippold C, Beckett C, Kemp C, Maurice N, Mukherjee A, Goldbach C, Watkins S, et al. An autophagy-enhancing drug promotes degradation of mutant alpha1-antitrypsin Z and reduces hepatic fibrosis. Science 2010;329:229-232.
49. Pan S, Huang L, McPherson J, Muzny D, Rouhani F, Brantly M, Gibbs R, Sifers RN. Single nucleotide polymorphism-mediated translational suppression of endoplasmic reticulum mannosidase I modifies the onset of end-stage liver disease in alpha1-antitrypsin deficiency. Hepatology 2009;50:275-281.
50. Carroll TP, Greene CM, O'Connor CA, Nolan AM, O'Neill SJ, McElvaney NG. Evidence for unfolded protein response activation in monocytes from individuals with alpha-1 antitrypsin deficiency. J Immunol 2010;184:4538-4546.
51. Kosmider B, Messier EM, Chu HW, Mason RJ. Human alveolar epithelial cell injury induced by cigarette smoke. PLoS ONE 2011;6: e26059.
52. Foronjy R, D'Armiento J. The effect of cigarette smoke-derived oxidants on the inflammatory response of the lung. Clin Appl Immunol Rev 2006;6:53-72.