Alpha-1 antitrypsin reduces severity of Pseudomonas pneumonia in mice and inhibits epithelial barrier disruption and Pseudomonas invasion of respiratory epithelial cells

Frontiers in Public Health

Volumn 1, Issue JUN, 2013, Pages

  Pott, Gregory B ^a,b   Scott Beard, K ^a,b   Bryan, Courtney L ^a,b   Merrick, Daniel T ^a   Shapiro, Leland ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Alpha 1 antitrypsin; Cytokines; Neutrophil elastase; Pneumonia; Pseudomonas; Sepsis

Indexed keywords

EID: 84928884471     PISSN: None     EISSN: 22962565     Source Type: Journal    
DOI: 10.3389/fpubh.2013.00019     Document Type: Article

References (76)

1. Fagon JY, Chastre J, Hance AJ, Montravers P, Novara A, Gibert C. Nosocomial pneumonia in ventilated patients: a cohort study evaluating attributable mortality and hospital stay. Am J Med (1993) 94:281-8. doi:10.1016/0002-934309390 060-3
2. Kollef MH. Epidemiology and risk factors for nosocomial pneu- monia. Emphasis on prevention. Clin Chest Med (1999) 20:653- 70. doi:10.1016/S0272-52310570 242-2
3. Klevens RM,Edwards JR,Richards CL Jr, Horan TC, Gaynes RP, Pollock DA, et al. Estimating health care-associated infections and deaths in U.S. hospitals, 2002. Public Health Rep (2007) 122: 160-6.
4. ATS. Guidelines for the man- agement of adults with hospital- acquired, ventilator-associated, and healthcare-associated pneumonia. Am J Respir Crit Care Med (2005) 171:388- 416. doi:10.1164/rccm.200405- 644ST
5. Jones RN. Microbial etiologies of hospital-acquired bacterial pneu- monia and ventilator-associated bacterial pneumonia. Clin Infect Dis (2010) 51(Suppl 1):S81-7. doi:10.1086/653053
6. Armstrong GL, Conn LA, Pin- ner RW. Trends in infectious disease mortality in the United States during the 20th cen- tury. JAMA (1999) 281:61-6. doi:10.1001/jama.281.1.61
7. Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, et al. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Soci- ety of America. Clin Infect Dis (2009) 48:1-12. doi:10.1086/59 5011
8. Scott RD. The Direct Medical Costs of Healthcare-Associated Infections in US Hospitals and the Benefits of Prevention. Atlanta: Centers for Disease Control and Prevention (2009). Available from: http://www.cdc.gov/hai/pdfs/hai/scott_costpaper.pdf .
9. O'Grady NP,Murray PR, Ames N. Preventing ventilator-associated pneumonia: does the evi- dence support the practice? JAMA (2012) 307:2534-9. doi:10.1001/jama.2012.6445 10. KollefMH, SchusterDP. The acute respiratory distress syndrome. N Engl J Med (1995) 332:27-7. doi:10.1056/NEJM19950105332 0106
10. CDC.Guidelines for prevention of nosocomial pneumonia. Centers for Disease Control and Preven- tion.MMWR Recomm Rep (1997) 46:1-79.
11. Moraes TJ, Chow CW, Downey GP. Proteases and lung injury. Crit CareMed (2003) 31:S189-94. doi:10.1097/01.CCM.0000057842. 90746.1E
12. Parker D, Prince A. Innate immunity in the respiratory epithelium. Am J Respir Cell Mol Biol (2011) 45:189-201. doi:10.1165/rcmb.2011-0011RT
13. El Solh AA,AkinnusiME,Wiener- Kronish JP, Lynch SV, Pineda LA, Szarpa K. Persistent infection with Pseudomonas aerugi- nosa in ventilator-associated pneumonia. Am J Respir Crit Care Med (2008) 178:513- 9. doi:10.1164/rccm.200802- 239OC
14. Craig A, Mai J, Cai S, Jeyaseelan S. Neutrophil recruitment to the lungs during bacterial pneumo- nia. Infect Immun (2009) 77:568- 75. doi:10.1128/IAI.00832-08
15. Stockley RA. Role of inflammation in respiratory tract infections. Am J Med (1995) 99:S8-13. doi:10.1016/S0002- 934309980304-0
16. Hermant B, Bibert S, Concord E, Dublet B,Weidenhaupt M, Vernet T, et al. Identification of proteases involved in the proteolysis of vas- cular endothelium cadherin dur- ing neutrophil transmigration. J Biol Chem (2003) 278:14002-12. doi:10.1074/jbc.M300351200
17. Couillin I, Vasseur V, Charron S, Gasse P, Tavernier M, Guillet J, et al. IL-1R1/MyD88 signaling is critical for elastase-induced lung inflammation and emphysema. J Immunol (2009) 183:8195-202. doi:10.4049/jimmunol.0803154
18. Meyer-HoffertU,WiedowO.Neu- trophil serine proteases:mediators of innate immune responses. Curr Opin Hematol (2011) 18:19-24. doi:10.1097/MOH.0b013e328341 15d1
19. Tralau T, Meyer-Hoffert U, Schroder JM, Wiedow O. Human leukocyte elastase and cathep- sin G are specific inhibitors of C5a-dependent neutrophil enzyme release and chemo- taxis. Exp Dermatol (2004) 13:316-25. doi:10.1111/j.0906- 6705.2004.00145.x
20. Stromstedt AA, Pasupuleti M, Schmidtchen A, Malmsten M. Evaluation of strategies for improving proteolytic resistance of antimicrobial peptides by using variants of EFK17, an internal seg- ment of LL-37. Antimicrob Agents Chemother (2009) 53:593-602. doi:10.1128/AAC.00477-08
21. Lillehoj EP, Hyun SW, Kim BT, Zhang XG, Lee DI, Rowland S, et al.Muc1mucins on the cell surface are adhesion sites for Pseudomonas aeruginosa. Am J Physiol Lung Cell Mol Physiol (2001) 280:L181-7.
22. Sando L, Pearson R, Gray C, Parker P, Hawken R, Thomson PC, et al. Bovine Muc1 is a highly polymorphic gene encoding an extensively glycosylated mucin that binds bacteria. J Dairy Sci (2009) 92:5276-91. doi:10.3168/jds.2009-2216
23. Plotkowski MC, Beck G, Tournier JM, Bernardo-Filho M, Mar- ques EA, Puchelle E. Adherence of Pseudomonas aeruginosa to respiratory epithelium and the effect of leucocyte elastase. J Med Microbiol (1989) 30:285-93. doi:10.1099/00222615-30-4-285
24. Plotkowski MC, Saliba AM, Pereira SH, Cervante MP, Bajolet-Laudinat O. Pseudomonas aeruginosa selective adherence to and entry into human endothe- lial cells. Infect Immun (1994) 62:5456-63.
25. Chi E, Mehl T, Nunn D, Lory S. Interaction of Pseudomonas aerug- inosa withA549 pneumocyte cells. Infect Immun (1991) 59:822-8.
26. Lehrer RI, Ganz T. Catheli- cidins: a family of endogenous antimicrobial peptides. Curr Opin Hematol (2002) 9:18-22. doi:10.1097/00062752- 200201000-00004
27. Lee CT, Fein AM, Lippmann M, Holtzman H, Kimbel P, Wein- baum G. Elastolytic activity in pulmonary lavage fluid from patients with adult respiratory- distress syndrome. N Engl J Med (1981) 304:192-6. doi:10.1056/ NEJM198101223040402
28. Tanaka H, Sugimoto H, Yosh- ioka T, Sugimoto T. Role of granulocyte elastase in tissue injury in patients with septic shock complicated by multiple- organ failure. Ann Surg (1991) 213:81-5. doi:10.1097/00000658- 199101000-00014
29. Kieninger AN, Lipsett PA. Hospital-acquired pneumonia: pathophysiology, diagnosis, and treatment. Surg Clin North Am (2009) 89:439-61. doi:10.1016/j.suc.2008.11.001
30. Donato LJ, Jenkins SM, Smith C, Katzmann JA, Snyder MR. Reference and interpretive ranges for alpha(1)-antitrypsin quanti- tation by phenotype in adult and pediatric populations. Am J Clin Pathol (2012) 138:398- 405. doi:10.1309/AJCPMEEJK32 ACYFP
31. Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med (1999) 340:448-54. doi:10.1056/NEJM1999021134 00607
32. Blank CA, BrantlyM. Clinical fea- tures and molecular characteris- tics of alpha 1-antitrypsin deficiency.AnnAllergy (1994) 72:105- 20; quiz 120-2.
33. MinWK,Chun S,Hwang SH,Park H.No relationship between serum lipoprotein(a) and albumin con- centrations in patients with acute phase response. Ann Clin Biochem (1999) 36(Pt 5):617-21.
34. Wewers MD, Casolaro MA, Sellers SE, Swayze SC, McPhaul KM, Wittes JT, et al. Replace- ment therapy for alpha 1-antitrypsin deficiency asso- ciated with emphysema. N Engl J Med (1987) 316:1055-62. doi:10.1056/NEJM1987042331 61704
35. Sandhaus RA, Turino G. Neutrophil elastase-mediated lung disease. COPD (2013) 10(Suppl 1):60-3. doi:10. 3109/15412555.2013.764403
36. ATS. American Thoracic Soci- ety/European Respiratory Soci- ety statement: standards for the diagnosis and management of individuals with alpha-1 antit- rypsin deficiency. Am J Respir Crit Care Med (2003) 168:818-900. doi:10.1164/rccm.168.7.818
37. Cantin AM, Woods DE. Aerosolized prolastin suppresses bacterial proliferation in a model of chronic Pseudomonas aerugi- nosa lung infection. Am J Respir Crit CareMed (1999) 160:1130-5. doi:10.1164/ajrccm.160.4.9807166
38. Wiesner O, Litwiller RD, Hum- mel AM, Viss MA, McDonald CJ, Jenne DE, et al. Differ- ences between human proteinase 3 and neutrophil elastase and their murine homologues are relevant for murine model experiments. FEBS Lett (2005) 579:5305-12. doi:10.1016/j.febslet.2005.08.056
39. Dhami R, Zay K, Gilks B, Porter S,Wright JL, Churg A. Pulmonary epithelial expression of human alpha1-antitrypsin in transgenic mice results in delivery of alpha1- antitrypsin protein to the intersti- tium. J Mol Med (1999) 77:377- 85. doi:10.1007/s001090050364
40. Lewis EC,MizrahiM,ToledanoM, Defelice N,Wright JL, Churg A, et al. alpha1-Antitrypsin monother- apy induces immune tolerance during islet allograft transplan- tation in mice. Proc Natl Acad Sci USA (2008) 105:16236-41. doi:10.1073/pnas.0807627105
41. Warfel JM, Steele AD, D'agnillo F. Anthrax lethal toxin induces endothelial barrier dysfunc- tion. Am J Pathol (2005) 166:1871-81. doi:10.1016/S0002- 94401062496-0
42. Behnia M, Robertson KA, Martin WJ 2nd. Lung infec- tions: role of apoptosis in host defense and pathogenesis of disease. Chest (2000) 117:1771-7. doi:10.1378/chest.117.6.1771
43. Schaaf B, Wieghorst A, Aries SP, Dalhoff K, Braun J. Neutrophil inflammation and activation in bronchiectasis: comparison with pneumonia and idio- pathic pulmonary fbrosis. Respiration (2000) 67:52-9. doi:10.1159/000029463
44. Hotchkiss RS, Dunne WM, Swanson PE, Davis CG, Tins- ley KW, Chang KC, et al. Role of apoptosis in Pseudomonas aeruginosa pneumonia. Sci- ence (2001) 294:1783. doi:10. 1126/science.294.5548.1783a
45. Mizgerd JP. Acute lower respi- ratory tract infection. N Engl J Med (2008) 358:716-27. doi:10.1056/NEJMra074111
46. Petrache I, Fijalkowska I, Medler TR, Skirball J, Cruz P, Zhen L, et al. Alpha-1 antitrypsin inhibits caspase-3 activity, preventing lung endothelial cell apoptosis. Am J Pathol (2006a) 169:1155-66. doi:10.2353/ajpath.2006.060058
47. Petrache I, Fijalkowska I, Zhen L, Medler TR, Brown E, Cruz P, et al. A novel antiapoptotic role for alpha1-antitrypsin in the prevention of pulmonary emphy- sema. Am J Respir Crit Care Med (2006b) 173:1222-8. doi:10.1164/ rccm.200512-1842OC
48. Zhang B, Lu Y, Campbell- Thompson M, Spencer T, Wasserfall C, Atkinson M, et al. Alpha1-antitrypsin pro- tects beta-cells from apoptosis. Diabetes (2007) 56:1316-23. doi:10.2337/db06-1273
49. Pott GB, Chan ED, Dinarello CA, Shapiro L. Alpha-1-antitrypsin is an endogenous inhibitor of proinflammatory cytokine production in whole blood. J Leukoc Biol (2009) 85:886-95. doi:10.1189/jlb.0208145
50. Seki H, Fukunaga K, AritaM, Arai H, Nakanishi H, Taguchi R, et al. The anti-inflammatory and prore- solving mediator resolvin E1 pro- tects mice from bacterial pneu- monia and acute lung injury. J Immunol (2009) 184:836-43. doi:10.4049/jimmunol.0901809
51. Janciauskiene SM, Bals R, Koczulla R, Vogelmeier C, Kohn- lein T, Welte T. The discovery of alpha1-antitrypsin and its role in health and disease. Respir Med (2011) 105:1129-39. doi:10.1016/j.rmed.2011.02.002
52. Chan ED, Pott GB, Silkoff PE, Ralston AH, Bryan CL, Shapiro L. Alpha-1-antitrypsin inhibits nitric oxide production. J Leukoc Biol (2012) 92:1251-60. doi:10.1189/jlb.0212071
53. Usmani OS, Barnes PJ. Assessing and treating small airways disease in asthma and chronic obstruc- tive pulmonary disease. Ann Med (2011) 44:146-56. doi:10. 3109/07853890.2011.585656
54. Belaaouaj A, McCarthy R, Baumann M, Gao Z, Ley TJ, Abraham SN, et al. Mice lack- ing neutrophil elastase reveal impaired host defense against gram negative bacterial sep- sis. Nat Med (1998) 4:615-8. doi:10.1038/nm0598-615
55. de Lima Pimenta A, Di Mar- tino P, Le Bouder E, Hulen C, Blight MA. In vitro identification of two adherence fac- tors required for in vivo viru- lence of Pseudomonas fluorescens. Microbes Infect (2003) 5:1177-87. doi:10.1016/j.micinf.2003.09.002
56. Knappstein S, Ide T, Schmidt MA, Heusipp G. Alpha 1-antitrypsin binds to and interferes with func- tionality of EspB from atypical and typical enteropathogenic Escherichia coli strains. Infect Immun (2004) 72:4344-50. doi:10.1128/IAI.72.8.4344- 4350.2004
57. Leroy-Dudal J, Gagniere H, Cos- sard E, Carreiras F, Di Martino P. Role of alphavbeta5 integrins and vitronectin in Pseudomonas aeruginosa PAK interaction with A549 respiratory cells. Microbes Infect (2004) 6:875-81. doi:10.1016/j.micinf.2004.05.004
58. Angus AA, Lee AA, Augustin DK, Lee EJ, Evans DJ, Fleiszig SM. Pseudomonas aeruginosa induces membrane blebs in epithelial cells, which are uti- lized as a niche for intracellular replication and motility. Infect Immun (2008) 76:1992-2001. doi:10.1128/IAI.01221-07
59. Chan ED, Kaminska AM, Gill W, Chmura K, Feldman NE, Bai X, et al. Alpha-1-antitrypsin (AAT) anomalies are associated with lung disease due to rapidly growing mycobacteria and AAT inhibits Mycobacterium abscessus infection of macrophages. Scand J Infect Dis (2007a) 39:690-6. doi:10.1080/00365540701225744
60. Tilg H, Vannier E, Vachino G, Dinarello CA, Mier JW. Antiin- flammatory properties of hepatic acute phase proteins: preferen- tial induction of interleukin 1 (IL-1) receptor antagonist over IL-1 beta synthesis by human peripheral blood mononuclear cells. J Exp Med (1993) 178:1629- 36. doi:10.1084/jem.178.5.1629 7693853
61. Janciauskiene S, Moraga F, Lind- gren S. C-terminal fragment of alpha1-antitrypsin activates human monocytes to a pro- inflammatory state through interactions with the CD36 scav- enger receptor and LDL receptor. Atherosclerosis (2001) 158:41- 51. doi:10.1016/S0021-9150000 0767-X
62. Janciauskiene SM, Nita IM, Stevens T. Alpha1-antitrypsin, old dog, new tricks. Alpha1- antitrypsin exerts in vitro anti-inflammatory activ- ity in human monocytes by elevating cAMP. J Biol Chem (2007) 282:8573-82. doi:10.1074/jbc.M607976200
63. Munch J,Standker L,AdermannK, Schulz A, Schindler M,Chinnadu- rai R, et al. Discovery and opti- mization of a natural HIV-1 entry inhibitor targeting the gp41 fusion peptide. Cell (2007) 129:263-75. doi:10.1016/j.cell.2007.02.042
64. Subramaniyam D, Virtala R, Pawlowski K, Clausen IG, Warkentin S, Stevens T, et al. TNF- alpha-induced self expression in human lung endothelial cells is inhibited by native and oxidized alpha1-antitrypsin. Int J Biochem Cell Biol (2008) 40:258-71. doi:10.1016/j.biocel.2007.07.016
65. Forssmann WG, The YH, Stoll M, Adermann K, Albrecht U, Tillmann HC, et al. Short-term monotherapy in HIV-infected patients with a virus entry inhibitor against the gp41 fusion peptide. SciTransl Med (2010) 2:63re63. doi:10.1126/scitranslmed.3001697
66. Halldorsson S, Gudjonsson T, Gottfredsson M, Singh PK, Gudmundsson GH, Baldurs- son O. Azithromycin maintains airway epithelial integrity during Pseudomonas aerugi- nosa infection. Am J Respir Cell Mol Biol (2009) 42:62-8. doi:10.1165/rcmb.2008-0357OC
67. He D, Su Y, Usatyuk PV, Spannhake EW, Kogut P, Sol- way J, et al. Lysophosphatidic acid enhances pulmonary epithelial barrier integrity and protects endotoxin-induced epithelial bar- rier disruption and lung injury. J Biol Chem (2009) 284:24123- 32. doi:10.1074/jbc.M109. 007393
68. Tomashefski JF Jr, Crystal RG, Wiedemann HP,Mascha E, Stoller JK. The bronchopulmonary pathology of alpha-1 antitrypsin (AAT) deficiency: findings of the Death Review Committee of the national registry for individuals with Severe Deficiency of Alpha-1 Antitrypsin. Hum Pathol (2004) 35:1452-61. doi:10.1016/j.humpath.2004. 08.013
69. Kochanek KD, Xu J, Murphy SL, Minino AM,KungH. Deaths: pre- liminary data for 2009. Natl Vital Stat Rep (2011) 59:1-54.
70. Braun J, Dalhoff K, Schaaf B, Wood WG, Wiessmann KJ. Characterization of protein- antiproteinase imbalance in bronchoalveolar lavage from patients with pneumonia. Eur Respir J (1994) 7:127-33. doi:10.1183/09031936.94.070 10127
71. Lieberman J. Augmentation therapy reduces frequency of lung infections in antitrypsin deficiency: a new hypoth- esis with supporting data. Chest (2000) 118:1480-5. doi:10.1378/chest.118.5.1480
72. Shapiro L, Pott GB, Ralston AH. Alpha-1-antitrypsin inhibits human immunodeficiency virus type 1. FASEB J (2001) 15:115-22. doi:10.1096/fj.00-0311com
73. Chan WM, Andrews C, Dra-gan L, Fredrick D, Armstrong L, Lyons C, et al. Three novel mutations inKIF21Ahighlight the importance of the third coiled-coil stalk domain in the etiology of CFEOM1. BMC Genet (2007b) 8:26. doi:10.1186/1471-2156-8-26
74. Zhou X, Shapiro L, Felling- ham G, Willardson BM, Burton GF. HIV replication in CD4+ T lymphocytes in the pres- ence and absence of follicular dendritic cells: inhibition of replication mediated by alpha- 1-antitrypsin through altered IkappaBalpha ubiquitination. J Immunol (2011) 186:3148-55. doi:10.4049/jimmunol.1001358
75. Hubbard RC, Sellers S, Czer- ski D, Stephens L, Crystal RG. Biochemical efficacy and safety of monthly augmentation ther- apy for alpha 1-antitrypsin defi ciency. JAMA (1988) 260:1259- 64. doi:10.1001/jama.260.9.1259
76. Stoller JK, Aboussouan LS. alpha1-Antitrypsin deficiency. 5: intravenous augmentation therapy: current understand- ing. Thorax (2004) 59:708-12. doi:10.1136/thx.2003.006544