Mechanisms of protein misfolding in conformational lung diseases

Current Molecular Medicine

Volumn 12, Issue 7, 2012, Pages 850-859

  McElvaney, N G ^a   Greene, C M ^a  

^a BEAUMONT HOSPITAL   (Ireland)

Author keywords

Alpha 1 antitrypsin; Cigarette smoke; Cystic fibrosis transmembrane conductance regulator; Endoplasmic reticulum stress

Indexed keywords

ALPHA 1 ANTITRYPSIN; CELL PROTEIN; MUTANT PROTEIN; TRANSMEMBRANE CONDUCTANCE REGULATOR; UNCLASSIFIED DRUG; VALOSIN CONTAINING PROTEIN; ZAAT PROTEIN;

ALPHA 1 ANTITRYPSIN DEFICIENCY; ARTICLE; ASPERGILLUS; AUTOPHAGOSOME; CANDIDA; CAUCASIAN; CELLULAR PARAMETERS; CHEMOTAXIS; CIGARETTE SMOKING; COMPLEX FORMATION; CRYSTAL STRUCTURE; CYSTIC FIBROSIS; DISEASE ASSOCIATION; DISEASE SEVERITY; EMPHYSEMA; ENDOPLASMIC RETICULUM OVERLOAD RESPONSE; ENDOPLASMIC RETICULUM STRESS; EUROPE; GAIN OF FUNCTION MUTATION; HETEROZYGOTE; LIVER CELL; LOSS OF FUNCTION MUTATION; LUNG DISEASE; MOLECULAR MECHANICS; NORTH AMERICA; PATHOGENESIS; PATHOPHYSIOLOGY; POINT MUTATION; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MISFOLDING; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; UNFOLDED PROTEIN RESPONSE; WILD TYPE;

EID: 84863524852     PISSN: 15665240     EISSN: 18755666     Source Type: Journal    
DOI: 10.2174/156652412801318728     Document Type: Article

References (102)

1. Balch WE, Morimoto RI, Dillin A, Kelly JW. Adapting proteostasis for disease intervention. Science 2008; 319: 916-9.
2. Bouchecareilh M, Balch WE. Proteostasis: a new therapeutic paradigm for pulmonary disease. Proc Am Thorac Soc 2011; 8: 189-95.
3. Balch WE, Roth DM, Hutt DM. Emergent properties of proteostasis in managing cystic fibrosis. Cold Spring Harb Perspect Biol 2011; 3(2): pii: a004499. doi: 10.1101/cshperspect.a004499.
4. Bouchecareilh M, Conkright JJ, Balch WE. Proteostasis strategies for restoring alpha1-antitrypsin deficiency. Proc Am Thorac Soc 2010; 7: 415-22.
5. Hutt DM, Powers ET, Balch WE. The proteostasis boundary in misfolding diseases of membrane traffic. FEBS Lett 2009; 583: 2639-46.
6. Mason DY, Cramer EM, Masse JM, Crystal R, Bassot JM, Breton-Gorius J. Alpha 1-antitrypsin is present within the primary granules of human polymorphonuclear leukocytes. Am J Pathol 1991; 139: 623-8.
7. 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: 4538-46.
8. Greene CM, Miller SD, Carroll TP, et al. Anti-apoptotic effects of Z alpha1-antitrypsin in human bronchial epithelial cells. Eur Respir J 2010; 35: 1155-63.
9. Greene CM, Miller SD, Carroll T, et al. Alpha-1 antitrypsin deficiency: a conformational disease associated with lung and liver manifestations. J Inherit Metab Dis 2008; 31: 21-34.
10. Kelly E, Greene CM, Carroll TP, McElvaney NG, O'Neill SJ. Alpha-1 antitrypsin deficiency. Respir Med 2010; 104: 763-72.
11. Greene CM, Hassan T, Molloy K, McElvaney NG. The role of proteases, endoplasmic reticulum stress and SERPINA1 heterozygosity in lung disease and alpha-1 anti-trypsin deficiency. Expert Rev Respir Med 2011; 5: 395-411.
12. Greene CM, McElvaney NG. Z alpha-1 antitrypsin deficiency and the endoplasmic reticulum stress response. World J Gastrointest Pharmacol Ther 2010; 1: 94-101.
13. Lomas DA, Evans DL, Finch JT, Carrell RW. The mechanism of Z alpha 1-antitrypsin accumulation in the liver. Nature 1992; 357: 605-7.
14. Teckman JH, Perlmutter DH. Retention of mutant alpha(1)-antitrypsin Z in endoplasmic reticulum is associated with an autophagic response. Am J Physiol Gastrointest Liver Physiol 2000; 279: G961-74.
15. Lawless MW, Greene CM, Mulgrew A, Taggart CC, O'Neill SJ, McElvaney NG. Activation of endoplasmic reticulumspecific stress responses associated with the conformational disease Z alpha 1-antitrypsin deficiency. J Immunol 2004; 172: 5722-6.
16. 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: 39002-15.
17. 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: 27769-80.
18. Miller SD, Greene CM, McLean C, et al. Tauroursodeoxycholic acid inhibits apoptosis induced by Z alpha-1 antitrypsin via inhibition of Bad. Hepatology 2007; 46: 496-503.
19. Greene CM, McElvaney NG. Protein misfolding and obstructive lung disease. Proc Am Thorac Soc 2010; 7: 346-55.
20. Gaggar A, Jackson PL, Noerager BD, et al. A novel proteolytic cascade generates an extracellular matrix-derived chemoattractant in chronic neutrophilic inflammation. J Immunol 2008; 180: 5662-9.
21. Lin M, Jackson P, Tester AM, et al. Matrix metalloproteinase-8 facilitates neutrophil migration through the corneal stromal matrix by collagen degradation and production of the chemotactic peptide Pro-Gly-Pro. Am J Pathol 2008; 173: 144-53.
22. Berger M, Sorensen RU, Tosi MF, Dearborn DG, Doring G. Complement receptor expression on neutrophils at an inflammatory site, the Pseudomonas-infected lung in cystic fibrosis. J Clin Invest 1989; 84: 1302-13.
23. Rogan MP, Taggart CC, Greene CM, Murphy PG, O'Neill SJ, McElvaney NG. Loss of microbicidal activity and increased formation of biofilm due to decreased lactoferrin activity in patients with cystic fibrosis. J Infect Dis 2004; 19: 1245-53.
24. Abrahamson M, Mason RW, Hansson H, Buttle DJ, Grubb A, Ohlsson K. Human cystatin C. role of the N-terminal segment in the inhibition of human cysteine proteinases and in its inactivation by leucocyte elastase. Biochem J 1991; 273: 621-6.
25. Weldon S, McNally P, McElvaney NG, et al. Decreased levels of secretory leucoprotease inhibitor in the Pseudomonas-infected cystic fibrosis lung are due to neutrophil elastase degradation. J Immunol 2009; 183: 8148-56.
26. Guyot N, Butler MW, McNally P, et al. Elafin, an elastasespecific inhibitor, is cleaved by its cognate enzyme neutrophil elastase in sputum from individuals with cystic fibrosis. J Biol Chem 2008; 283: 32377-85.
27. Zhu YK, Liu XD, Skold CM, et al. Synergistic neutrophil elastase-cytokine interaction degrades collagen in threedimensional culture. Am J Physiol Lung Cell Mol Physiol. 2001; 281: L868-78.
28. Hartl D, Latzin P, Hordijk P, et al. Cleavage of CXCR1 on neutrophils disables bacterial killing in cystic fibrosis lung disease. Nat Med 2007; 13: 1423-30.
29. Nemoto E, Sugawara S, Tada H, Takada H, Shimauchi H, Horiuchi H. Cleavage of CD14 on human gingival fibroblasts cocultured with activated neutrophils is mediated by human leukocyte elastase resulting in down-regulation of lipopolysaccharide-induced IL-8 production. J Immunol 2000; 165: 5807-13.
30. Brodsky JL, McCracken AA. ER protein quality control and proteasome-mediated protein degradation. Semin Cell Dev Biol 1999; 10: 507-13.
31. Perlmutter DH. Autophagic disposal of the aggregation-prone protein that causes liver inflammation and carcinogenesis in alpha-1-antitrypsin deficiency. Cell Death Differ. 2009; 16: 39-45.
32. Eskelinen EL. New insights into the mechanisms of macroautophagy in mammalian cells. Int Rev Cell Mol Biol 2008; 266: 207-47.
33. Eskelinen EL, Saftig P. Autophagy: a lysosomal degradation pathway with a central role in health and disease. Biochim Biophys Acta 2009; 1793: 664-73.
34. Kundu M, Thompson CB. Autophagy: basic principles and relevance to disease. Annu Rev Pathol 2008; 3: 427-55.
35. Bergin DA, Reeves EP, Meleady P, et al. alpha-1 Antitrypsin regulates human neutrophil chemotaxis induced by soluble immune complexes and IL-8. J Clin Invest 2010; 120: 4236-50.
36. Elliott PR, Bilton D, Lomas DA. Lung polymers in Z alpha1-antitrypsin deficiency-related emphysema. Am J Respir Cell Mol Biol 1998; 18: 670-4.
37. Mulgrew AT, Taggart CC, Lawless MW, et al. Z alpha1-antitrypsin polymerizes in the lung and acts as a neutrophil chemoattractant Chest. 2004; 125: 1952-7.
38. Mahadeva R, Atkinson C, Li Z, et al. Polymers of Z alpha1-antitrypsin co-localize with neutrophils in emphysematous alveoli and are chemotactic in vivo. Am J Pathol. 2005; 166: 377-86.
39. Bottomley SP. The folding pathway of alpha1-antitrypsin: avoiding the unavoidable. Proc Am Thorac Soc 2010; 7: 404-7.
40. Krishnan B, Gierasch LM. Dynamic local unfolding in the serpin alpha-1 antitrypsin provides a mechanism for loop insertion and polymerization. Nat Struct Mol Biol 2011; 18: 222-6.
41. Baek JH, Yang WS, Lee C, Yu MH. Functional unfolding of alpha1-antitrypsin probed by hydrogen-deuterium exchange coupled with mass spectrometry. Mol Cell Proteomics 2009; 8: 1072-81.
42. Sifers RN. Intracellular processing of alpha1-antitrypsin. Proc Am Thorac Soc 2010; 7: 376-80.
43. Knaupp AS, Levina V, Robertson AL, Pearce MC, Bottomley SP. Kinetic instability of the serpin Z alpha1-antitrypsin promotes aggregation. J Mol Biol 2010; 396: 375-83.
44. Roussel BD, Irving JA, Ekeowa UI, et al. Unravelling the twists and turns of the serpinopathies. FEBS J 2011; 184: 4538-46.
45. Yamasaki M, Sendall TJ, Harris LE, Lewis GM, Huntington JA. Loop-sheet mechanism of serpin polymerization tested by reactive center loop mutations. J Biol Chem 2010; 285:30752-8.
46. Huntington JA, Whisstock JC. Molecular contortionism-on the physical limits of serpin 'loop-sheet' polymers. Biol Chem 2010; 391: 973-82.
47. Yamasaki M, Li W, Johnson DJ, Huntington JA. Crystal structure of a stable dimer reveals the molecular basis of serpin polymerization. Nature 2008; 455: 1255-8.
48. Ekeowa UI, Freeke J, Miranda E, et al. Defining the mechanism of polymerization in the serpinopathies. Proc Natl Acad Sci U S A 2010; 107: 17146-51.
49. McLean C, Greene CM, McElvaney NG. Gene targeted therapeutics for liver disease in alpha-1 antitrypsin deficiency. Biologics 2009; 3: 63-75.
50. Devlin GL, Parfrey H, Tew DJ, Lomas DA, Bottomley SP. Prevention of polymerization of M and Z alpha1-Antitrypsin (alpha1-AT) with trimethylamine N-oxide. Implications for the treatment of alpha1-at deficiency. Am J Respir Cell Mol Biol 2001; 24: 727-32.
51. Sharp LK, Mallya M, Kinghorn KJ, et al. Sugar and alcohol molecules provide a therapeutic strategy for the serpinopathies that cause dementia and cirrhosis. FEBS J 2006; 273: 2540-52.
52. Burrows JA, Willis LK, Perlmutter DH. Chemical chaperones mediate increased secretion of mutant alpha 1-antitrypsin (alpha 1-AT) Z: A potential pharmacological strategy for prevention of liver injury and emphysema in alpha 1-AT deficiency. Proc Natl Acad Sci U S A 2000; 97: 1796-801.
53. Marcus NY, Perlmutter DH. Glucosidase and mannosidase inhibitors mediate increased secretion of mutant alpha1 antitrypsin Z. J Biol Chem 2000; 275: 1987-92.
54. 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: 16891-7.
55. Hidvegi T, Ewing M, Hale P, et al. An autophagy-enhancing drug promotes degradation of mutant alpha1-antitrypsin Z and reduces hepatic fibrosis. Science 2010; 329: 229-32.
56. Mallya M, Phillips RL, Saldanha SA, et al. Small molecules block the polymerization of Z alpha1-antitrypsin and increase the clearance of intracellular aggregates. J Med Chem 2007; 50: 5357-63.
57. Chang YP, Mahadeva R, Chang WS, Lin SC, Chu YH. Small-molecule peptides inhibit Z alpha(1)-antitrypsin polymerization. J Cell Mol Med 2009; 13: 2304-16
58. Rowe SM, Miller S, Sorscher EJ. Cystic fibrosis. N Engl J Med 2005; 352: 1992-2001.
59. Lommatzsch ST, Aris R. Genetics of cystic fibrosis. Semin Respir Crit Care Med 2009; 30: 531-8.
60. Bobadilla JL, Macek M, Jr., Fine JP, Farrell PM. Cystic fibrosis: a worldwide analysis of CFTR mutations--correlation with incidence data and application to screening. Hum Mutat 2002; 19: 575-606.
61. Voynow JA, Rubin BK. Mucins, mucus, and sputum. Chest 2009; 135: 505-12.
62. Rose MC, Voynow JA. Respiratory tract mucin genes and mucin glycoproteins in health and disease. Physiol Rev 2006; 86: 245-78.
63. Roum JH, Buhl R, McElvaney NG, Borok Z, Crystal RG. Systemic deficiency of glutathione in cystic fibrosis. J Appl Physiol 1993; 75: 2419-24.
64. Greene CM, McElvaney NG. Proteases and antiproteases in chronic neutrophilic lung disease-relevance to drug discovery. Br J Pharmacol 2009; 158: 1048-58.
65. Kelly E, Greene CM, McElvaney NG. Targeting neutrophil elastase in cystic fibrosis. Expert Opin Ther Targets 2008; 12: 145-57.
66. Geraghty P, Rogan MP, Greene CM, et al. Neutrophil elastase up-regulates cathepsin B and matrix metalloprotease-2 expression. J Immunol 2007; 178: 5871-8.
67. Greene CM. How can we target pulmonary inflammation in cystic fibrosis? Open Respir Med J 2010; 4: 18-9.
68. Greene CM, Branagan P, McElvaney NG. Toll-like receptors as therapeutic targets in cystic fibrosis. Expert Opin Ther Targets 2008; 12: 1481-95.
69. Baker JM, Hudson RP, Kanelis V, et al. CFTR regulatory region interacts with NBD1 predominantly via multiple transient helices. Nat Struct Mol Biol 2007; 14: 738-45.
70. Williams KW, Scott MM, Elmquist JK. From observation to experimentation: leptin action in the mediobasal hypothalamus. Am J Clin Nutr 2009; 89: 985S-90S.
71. Riordan JR. Assembly of functional CFTR chloride channels. Annu Rev Physiol 2005; 67: 701-18.
72. Du K, Lukacs GL. Cooperative assembly and misfolding of CFTR domains in vivo. Mol Biol Cell 2009; 20: 1903-15.
73. Varga K, Jurkuvenaite A, Wakefield J, et al. Efficient intracellular processing of the endogenous cystic fibrosis transmembrane conductance regulator in epithelial cell lines. J Biol Chem 2004; 279: 22578-84.
74. Zhong X, Shen Y, Ballar P, Apostolou A, Agami R, Fang S. AAA ATPase p97/valosin-containing protein interacts with gp78, a ubiquitin ligase for endoplasmic reticulum-associated degradation. J Biol Chem 2004; 279: 45676-84.
75. Okiyoneda T, Barriere H, Bagdany M, et al. Peripheral protein quality control removes unfolded CFTR from the plasma membrane. Science 2010; 329: 805-10.
76. Cheng SH, Gregory RJ, Marshall J, et al. Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 1990; 63: 827-34.
77. Thibodeau PH, Richardson JM, 3rd, Wang W, et al. The cystic fibrosis-causing mutation deltaF508 affects multiple steps in cystic fibrosis transmembrane conductance regulator biogenesis. J Biol Chem 2010; 285: 35825-35.
78. Hoelen H, Kleizen B, Schmidt A, et al. The primary folding defect and rescue of DeltaF508 CFTR emerge during translation of the mutant domain. PLoS One 2010; 5: e15458.
79. Protasevich I, Yang Z, Wang C, et al. Thermal unfolding studies show the disease causing F508del mutation in CFTR thermodynamically destabilizes nucleotide-binding domain 1. Protein Sci 2010; 19: 1917-31.
80. Wang C, Protasevich I, Yang Z, et al. Integrated biophysical studies implicate partial unfolding of NBD1 of CFTR in the molecular pathogenesis of F508del cystic fibrosis. Protein Sci 2010; 19: 1932-47.
81. Grove DE, Rosser MF, Watkins RL, Cyr DM. Analysis of CFTR folding and degradation in transiently transfected cells. Methods Mol Biol 2011; 741: 219-32.
82. Grove DE, Fan CY, Ren HY, Cyr DM. The endoplasmic reticulum-associated Hsp40 DNAJB12 and Hsc70 cooperate to facilitate RMA1 E3-dependent degradation of nascent CFTRDeltaF508. Mol Biol Cell 2011; 22: 301-14.
83. Du K, Sharma M, Lukacs GL. The DeltaF508 cystic fibrosis mutation impairs domain-domain interactions and arrests post-translational folding of CFTR. Nat Struct Mol Biol 2005; 12: 17-25.
84. Cui L, Aleksandrov L, Chang XB, et al. Domain interdependence in the biosynthetic assembly of CFTR. J Mol Biol 2007; 365: 981-94.
85. Rosser MF, Grove DE, Chen L, Cyr DM. Assembly and misassembly of cystic fibrosis transmembrane conductance regulator: folding defects caused by deletion of F508 occur before and after the calnexin-dependent association of membrane spanning domain (MSD) 1 and MSD2. Mol Biol Cell 2008; 19: 4570-9.
86. Lewis HA, Zhao X, Wang C, et al. Impact of the deltaF508 mutation in first nucleotide-binding domain of human cystic fibrosis transmembrane conductance regulator on domain folding and structure. J Biol Chem 2005; 280: 1346-53.
87. Thibodeau PH, Brautigam CA, Machius M, Thomas PJ. Side chain and backbone contributions of Phe508 to CFTR folding. Nat Struct Mol Biol 2005; 12: 10-6.
88. Lewis HA, Wang C, Zhao X, et al. Structure and dynamics of NBD1 from CFTR characterized using crystallography and hydrogen/deuterium exchange mass spectrometry. J Mol Biol 2010; 396: 406-30.
89. Loo TW, Bartlett MC, Clarke DM. The V510D suppressor mutation stabilizes DeltaF508-CFTR at the cell surface. Biochemistry 2010; 49: 6352-7.
90. He L, Aleksandrov LA, Cui L, Jensen TJ, Nesbitt KL, Riordan JR. Restoration of domain folding and interdomain assembly by second-site suppressors of the DeltaF508 mutation in CFTR. FASEB J 2010; 24: 3103-12.
91. Peters KW, Okiyoneda T, Balch WE, et al. CFTR Folding Consortium: methods available for studies of CFTR folding and correction. Methods Mol Biol 2011; 742: 335-53.
92. Cantin AM. Cellular response to cigarette smoke and oxidants: adapting to survive. Proc Am Thorac Soc 2010; 7: 368-75.
93. Malhotra D, Thimmulappa R, Vij N, et al. Heightened endoplasmic reticulum stress in the lungs of patients with chronic obstructive pulmonary disease: the role of Nrf2-regulated proteasomal activity. Am J Respir Crit Care Med 2009; 180: 1196-207.
94. Kelsen SG, Duan X, Ji R, Perez O, Liu C, Merali S. Cigarette smoke induces an unfolded protein response in the human lung: a proteomic approach. Am J Respir Cell Mol Biol 2008; 38: 541-50.
95. Geraghty P, Wallace A, D'Armiento JM. Induction of the unfolded protein response by cigarette smoke is primarily an activating transcription factor 4-C/EBP homologous protein mediated process. Int J Chron Obstruct Pulmon Dis 2011; 6: 309-19.
96. Min T, Bodas M, Mazur S, Vij N. Critical role of proteostasisimbalance in pathogenesis of COPD and severe emphysema. J Mol Med (Berl) 2011; 89: 577-93.
97. Vij N. AAA ATPase p97/VCP: cellular functions, disease and therapeutic potential. J Cell Mol Med 2008; 12: 2511-8.
98. Bodas M, Min T, Vij N. Critical role of CFTR dependent lipidrafts in cigarette smoke induced lung epithelial injury. Am J Physiol Lung Cell Mol Physiol 2011; 300: L811-20.
99. Taggart C, Cervantes-Laurean D, Kim G, et al. Oxidation of either methionine 351 or methionine 358 in alpha 1-antitrypsin causes loss of anti-neutrophil elastase activity. J Biol Chem 2000; 275: 27258-65.
100. Alam S, Li Z, Janciauskiene S, Mahadeva R. Oxidation of Z {alpha}1-antitrypsin by Cigarette Smoke Induces Polymerization: A Novel Mechanism of Early-onset Emphysema. Am J Respir Cell Mol Biol 2011; 45(2): 261-9
101. Belcher CN, Vij N. Protein processing and inflammatory signaling in Cystic Fibrosis: challenges and therapeutic strategies. Curr Mol Med 2010; 10: 82-94.
102. Sloane PA, Rowe SM. Cystic fibrosis transmembrane conductance regulator protein repair as a therapeutic strategy in cystic fibrosis. Curr Opin Pulm Med 2010; 16: 591-7.