Reevaluating gel-forming mucins' roles in cystic fibrosis lung disease

Free Radical Biology and Medicine

Volumn 37, Issue 10, 2004, Pages 1564-1577

  Perez Vilar, Juan ^a,b   Boucher, Richard C ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Cystic fibrosis; Free radicals; Glutathione; Hypochlorous acid; Inflammation; Lung; Mucins; Mucus; Myeloperoxidase; Neutrophils

Indexed keywords

GLUTATHIONE; HYPOCHLOROUS ACID; MUCIN; MYELOPEROXIDASE;

AIRWAY; ARTICLE; CATALYSIS; CYSTIC FIBROSIS; DEHYDRATION; GEL; HUMAN; HYPOTHESIS; LUNG DISEASE; MUCUS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; RESPIRATORY TRACT MUCOSA; VISCOELASTICITY;

BACTERIAL INFECTIONS; CYSTIC FIBROSIS; GLUTATHIONE; HUMANS; HYDROGEN-ION CONCENTRATION; HYPOCHLOROUS ACID; LUNG; MUCINS; NEUTROPHILS; PEROXIDASE; SPUTUM;

BACTERIA (MICROORGANISMS);

EID: 5344221552     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2004.07.027     Document Type: Article

References (96)

1. C.E. Cross, A. van der Vliet, C.A. O'Neill, S. Louie, and B. Halliwell Oxidants, antioxidants, and respiratory tract lining fluids Environ. Health Perspect. 102 1994 185 191
2. D.J. Gendler, and A.P. Spicer Epithelial mucin genes Annu. Rev. Physiol. 57 1995 607 634
3. J. Perez-Vilar, and R.L. Hill The structure and assembly of secreted mucins J. Biol. Chem. 274 1999 31751 31754
4. J. Dekker, J.W. Rossen, H.A. Buller, and A.W. Einerhand The MUC family: an obituary Trends Biochem. Sci. 27 2002 126 131
5. Y. Chen, Y.H. Zhao, T.B. Kalaslavadi, E. Hamati, K. Nehrke, A.D. Le, D.K. Ann, and R. Wu Genome-wide search and identification of a novel gel-forming mucin MUC19/Muc19 in glandular tissues Am. J. Respir. Cell Mol. Biol. 30 2004 155 165
6. F. Escande, J.P. Aubert, N. Porchet, and M.P. Buisine Human mucin gene MUC5AC: organization of its 5′-region and central repetitive region Biochem. J. 358 2001 763 772
7. J.L. Desseyn, V. Guyonnet-Duperat, N. Porchet, J.P. Aubert, and A. Laine J. Biol. Chem. 272 1997 3168 3178
8. J. Perez-Vilar, A.E. Eckhardt, and R.L. Hill Porcine submaxillary mucin forms disulfide-bonded dimers between its carboxyl-terminal domains J. Biol. Chem. 271 1996 9845 9850
9. J. Perez-Vilar, and R.L. Hill The carboxyl-terminal 90 residues of porcine submaxillary mucin are sufficient for forming disulfide-bonded dimers J. Biol. Chem. 273 1998 6982 6988
10. J. Perez-Vilar, A.E. Eckhardt, A. DeLuca, and R.L. Hill Porcine submaxillary mucin forms disulfide-linked multimers through its amino-terminal D-domains J. Biol. Chem. 273 1998 14442 14449
11. G.J. Strous, and J. Dekker Mucin-type glycoproteins Crit. Rev. Biochem. 27 1992 57 92
12. J.A. Voynow What does mucin have to do with lung disease? Paediatr. Respir. Rev. 3 2002 98 103
13. E.R. Lillehoj, and K.C. Kim Airway mucus: its components and function Arch. Pharm. Res. 25 2002 770 780
14. J.R. Davis, A. Herrmann, W. Russell, N. Svitacheva, C. Wickstrom, and J. Carlstedt Respiratory tract mucins: structure and expression patterns Novartis Found. Symp. 248 2002 76 93
15. C. Basbaum, H. Lemjabbar, M. Longphre, D. Li, E. Gensch, and N. McNamara Control of mucin transcription by diverse injury-induced signaling pathways Am. J. Respir. Crit. Care Med. 160 1999 S44 S48
16. M.C. Rose, T.J. Nickola, and J.A. Voynow Airway mucus obstruction: mucin glycoproteins, MUC gene regulation and goblet cell hyperplasia Am. J. Respir. Cell Mol. Biol. 25 2001 533 537
17. A.D. Jackson Airway goblet-cell mucus secretion Trends Pharmacol. Sci. 22 2001 39 45
18. D.F. Rogers The airway goblet cell Int. J. Biochem. Cell Biol. 35 2003 1 6
19. W.N. Foster Mucociliary transport and cough in humans Pulm. Pharmacol. Ther. 15 2002 277 282
20. M.R. Knowles, and R.C. Boucher Mucus clearance as a primary innate defense mechanism for mammalian airways J. Clin. Invest. 109 2002 571 577
21. J. Perez-Vilar, S.H. Randell, and R.C. Boucher C-Mannosylation of MUC5AC and MUC5B Cys subdomains Glycobiology 14 2004 325 337
22. Bell, S.L.; Xu, G.; Forstner, J.F. Role of the cystine-knot motif at the C-terminus of rat mucin protein Muc2 in dimer formation and secretion. Biochem. J. 357 203-209.
23. M.E. Lidell, M.E. Johansson, M. Morgelin, N. Asker, J.R. Gum, Y.S. Kim, and G.C. Hansson The recombinant C-terminus of the human MUC2 mucin forms dimers in Chinese-hamster ovary cells and heterodimers with full-length MUC2 in LS174T cells Biochem. J. 372 2003 335 345
24. K. Godl, M.E. Johansson, M.E. Lidell, M. Morgelin, H. Karlsson, F.J. Olson, J.R. Gum, Y.S. Kim, and G.C. Hansson The N terminus of the MUC2 mucin forms trimers that are held together within a trypsin-resistant core fragment J. Biol. Chem. 277 2002 47248 47256
25. Lidell, M.E.; Johansson M.E.; Hansson G.C. A autocatalytic cleavage in the C-terminus of the human MUC2 mucin occurs at the low pH of the late secretory pathway. J. Biol. Chem. 278 13944-13951.
26. C. Wickstrom, and I. Carlstedt N-terminal cleavage of the salivary MUC5B mucin. Analogy with the Von Willebrand propolypeptide? J. Biol. Chem. 276 2001 47116 47121
27. J. Perez-Vilar, and R.L. Hill Porcine submaxillary mucin structure and assembly Y. Inoue Y. Lee F.C. Troy Sialobiology and Other Novel Forms of Glycosylation 1999 Gakushin Publisher Osaka, Japan 207 215
28. J. Perez-Vilar, and R.L. Hill Identification of the half-cystine residues in porcine submaxillary mucin critical for multimerization through the D-domains. Roles of the CGLCG motif in the D1- and D3-domains J. Biol. Chem. 273 1998 34527 34534
29. R. Noiva Enzymatic catalysis of disulfide formation Proein Expr. Purif. 5 1994 1 13
30. J.E. Sadler Biochemistry and genetics of von Willebrand factor Annu. Rev. Biochem. 67 1998 395 424
31. T.N. Mayadas, and D.D. Wagner In vitro multimerization of von Willebrand factor is triggered by low pH. Importance of the pro-polypeptide and free sulfhydryls J. Biol. Chem. 264 1989 13497 13503
32. O.A. Weisz Acidification and protein traffic Int. Rev. Cytol. 226 2003 259 319
33. P.M. Quinton Physiological basis of cystic fibrosis: a historical perspective Physiol. Rev. 79 1999 S3 S22
34. M.H. Akabas Cystic fibrosis transmembrane conductance regulator. Structure and function of an epithelial chloride channel J. Biol. Chem. 275 2000 3729 3732
35. E.M. Schwiebert, D.J. Benos, M.E. Egan, M.J. Stutts, and W.B. Guggino CFTR is a conductance regulator as well as a chloride channel Physiol. Rev. 79 1999 S145 S166
36. R.K. Rowntree, and A. Harris The phenotypic consequences of CFTR mutations Ann. Hum. Genet. 67 2003 471 485
37. R.C. Boucher An overview of the pathogenesis of cystic fibrosis lung disease Adv. Drug Deliv. Rev. 54 2002 1359 1371
38. S.H. Donaldson, and R.C. Boucher Update on pathogenesis of cystic fibrosis lung disease Curr. Opin. Pulm. Med. 9 2003 486 491
39. H. Matsui, B.R. Grubb, R. Tarran, S.H. Randell, J.T. Gatzy, C.W. Davis, and R.C. Boucher Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airway disease Cell 95 1998 1005 1015
40. D. Worlitzsch, R. Tarran, M. Ulrich, U. Scwab, A. Cekici, K.C. Meyer, P. Birrer, G. Bellon, J. Berger, T. Weiss, K. Botzenhart, J.R. Yankaskas, S. Randell, R.C. Boucher, and G. Doring Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients J. Clin. Invest. 109 2002 317 325
41. S.S. Yoon, R.F. Hennigan, G.M. Hilliard, U.A. Ochsner, K. Parvatiyar, M.C. Kamani, H.L. Allen, T.R. Dekievit, P.R. Gardner, U. Schwab, J.J. Rowe, B.H. Iglewski, T.R. McDermott, R.P. Mason, D.J. Wozniak, R.E. Hancock, M.R. Parsek, T.L. Noah, R.C. Boucher, and D.J. Hassett Pseudomonas aeruginosa anaerobic respiration in biofilms: relationship to cystic fibrosis pathogenesis Dev. Cell 3 2002 593 603
42. J. Perez-Vilar, J.K. Sheehan, and S.H. Randell Making more MUCS Am. J. Respir. Cell Mol. Biol. 28 2003 267 270
43. C.A. Sheils, J. Kas, W. Travassos, P.G. Allen, P.A. Janmey, M.E. Wohl, and T.P. Stossel Actin filaments mediate DNA fiber formation in chronic inflammatory airway disease Am. J. Pathol. 148 1996 919 927
44. Cheng, P.W.; Boat, T.F.; Cranfill, K.; Yankaskas, J.R.; Boucher, R.C. Increased sulfation of glycoconjugates by cultured nasal epithelial cells from patients with cystic fibrosis. J. Clin. Invest. 84 68-72.
45. Y. Zhang, B. Doranz, J.R. Yankaskas, and J.F. Engelhardt Genotypic analysis of respiratory mucous sulfation defects in cystic fibrosis J. Clin. Invest. 96 1995 2997 3004
46. J. Mendicino, and S. Sangadala Synthesis of sulfated oligosaccharides by cystic fibrosis trachea epithelial cells Mol. Cell Biochem. 201 1999 141 149
47. Thomsson K.A., Carlstedt I. N.G., Karlsson H., Karlsson G., Hansson C., Different O-glycosylation of respiratory mucin glycopeptides from a patient with cystic fibrosis. Glycoconj. J. 15 823-833.
48. C.J. Reid, M.D. Burdick, M.A. Hollingsworth, and A. Harris CFTR expression does not influence glycosylation of an epitope-tagged MUC1 mucin in colon carcinoma cell lines Glycobiology 9 1999 389 398
49. D.K. Shori, H.H. Kariyawasam, R.A. Knight, M.E. Hodson, T. Genter, J. Hansen, C. Koch, and A. Kalogeridis Sulphation of the salivary mucin MG1 (MUC5B) is not correlated to the degree of its sialylation and is unaffected by cystic fibrosis Pflugers Arch. 443 2001 S50 S54
50. I. Brockhausen, F. Vavasseur, and X. Yang Biosynthesis of mucin type O-glycans: lack of correlation between glycosyltransferase and sulfotransferases activities and CFTR expression Glycoconj. J. 18 2001 685 697
51. Holmen J.M.; Karlsson N.G.; Abdullah L.H.; Randell S.H.; Sheehan J.K. Hansson G.C.; Davis C.W.; Mucins and their O-glycans from human bronchial epithelial cell cultures. Am. J. Physiol. Lung Cell Mol. Physiol. e-publication ahead of print.
52. L.H. Abdullah, J.D. Conway, J.A. Cohn, and C.W. Davis Protein kinase C and Ca2+activation of mucin secretion in airway goblet cells Am. J. Physiol. 273 1997 L201 L210
53. G. Lamblin, S. Degroote, J.M. Perini, P. Delmotte, A. Scharfman, M. Davril, J.M. Lo-Guidice, N. Houdret, V. Dumur, A. Klein, and P. Rousse Human airway mucin glycosylation: a combinatory of carbohydrate determinants which vary in cystic fibrosis Glycoconj. J. 18 2001 685 697
54. P. Delmotte, S. Degroote, M.D. Merten, I. Van Seuningen, A. Bernigaud, C. Figarella, P. Roussel, and J.M. Perini Influence of TNTalpha on the sialylation of mucins produced by a transformed cell line MM-39 derived from human tracheal gland cells Glycoconj. J. 18 2001 487 497
55. Scharfman A.; van Brussel E.; Houdret N.; Lamblin G.; Roussel P. Interactions between glycoconjugates from human respiratory airways and Pseusomonas aeruginosa. Am. J. Resp. Crit. Care Med. 154 S163-S169.
56. M. Davril, S. Degroote, P. Humbert, C. Galabert, V. Dumur, J.J. Lafitte, G. Lamblin, and P. Roussel The syalytation of bronchial mucins secreted by patients suffering from cystic fibrosis or from chronic bronchitis is related to the severity of airway infection Glycobiology 9 1999 311 321
57. R. Gupta, N. Jentoft, A.M. Jamieson, and J. Blackwell Structural analysis of purified tracheobronchial mucins Biopolymers 29 1990 347 355
58. D.J. Thornton, J.K. Sheehan, and H. Lindgren carlstedt, I. Mucus glycoproteins from cystic fibrotic sputum. Macromolecular properties and structural "architecturea" J. Biochemistry 276 1991 667 675
59. R. Gupta, and N. Jentoft The structure of tracheobronchial mucins from cystic fibrosis and control patients J. Biol. Chem. 267 1992 3160 3167
60. M.C. Rose, C.F. Brown, J.Z. Jacoby, W.S. Lynn, and B. Kaufman Biochemical properties of tracheobronchial mucins from cystic fibrosis and non-cystic fibrosis individuals Pediatr. Res. 22 1987 545 551
61. J.D. Klinger, B. Tandler, C.M. Liedtke, and T.F. Boat Proteinases of Pseudomonas Aeruginosa evoke mucin release by tracheal epithelium J. Clin. Invest. 74 1984 1669 1678
62. H.J. Jansen, C.A. Hart, J.M. Rhodes, J.R. Saunders, and J.W. Smalley A novel mucin-sulphatase activity found in Burkholderia cepacia and Pseudomonas aeruginosa J. Med. Microbiol. 48 1999 551 557
63. Voynow J.A.; Young L.R.; Wang Y.; Horger T.; Rose M.C.; Fischer B.M. Neutrophil elastase increases MUC5AC mRNA and protein expression in respiratory epithelial cells. Am. J. Physiol. 276 L835-L843.
64. M. Somerville, P.S. Richardson, A. Rutman, R. Wilson, and P.J. Cole Stimulation of secretion into human and feline airways by Pseudomonas aeruginosa proteases J. Appl. Physiol. 70 1991 2259 2267
65. M. Dawson, D. Wirtz, and J. Hanes Enhanced viscoelasticity of human cystic fibrotic sputum correlates with increasing microheterogeneity in particle transport J. Biol. Chem. 278 2003 50393 50401
66. R.D. Coakley, and R.C. Boucher Regulation and functional significance of airway surface liquid pH JOP 2 2001 294 300
67. R.D. Coakley, B.R. Grubb, A.M. Paradiso, J.T. Gatzy, L.G. Johnson, S.M. Kreda, W.K. O'Neal, and R.C. Boucher Abnormal surface liquid pH regulation by cultured cystic fibrosis bronchial epithelium Proc. Natl. Acad. Sci. USA 100 2003 16083 16088
68. H. Kopelman, P. Durie, K. Gaskin, K. Weizman, and G. Fostner Pancreatic fluid secretion and protein hyperconcentration in cystic fibrosis N. Engl. J. Med. 312 1985 329 334
69. S. von Eckardstein, T.G. Cooper, K. Rutscha, D. Meschede, J. Horst, and E. Nioeschlag Seminal fibrosis transmembrane conductance regulator (CFTR) gene mutations in men with obstructive azoospermia Fertil. Steril. 73 2000 1226 1231
70. I. Rahman, and W. MacNee Lung glutathione and oxidative stress: implications in cigarette smoke-induced airway disease Am. J. Physiol. 277 1999 L1067 L1088
71. Q. Rahman, P. Abidi, F. Afaq, D. Schiffmann, B.T. Mossman, D.W. Kamp, and M. Athar Glutathione redox system in oxidative lung injury Crit. Rev. Toxicol. 29 1999 543 568
72. A.M. Cantin, S.L. North, R.C. Hubbard, and R.G. Crystal Normal alveolar epithelial lining fluid contains high levels of glutathione J. Appl. Physiol. 63 1987 152 157
73. D.S. Boehme, J.A. Hotchkiss, and R.F. Henderson Glutathione and GSH-dependent enzymes in bronchoalveolar lavage fluid cells in response to ozone Exp. Mol. Pathol. 56 1992 37 48
74. B.J. Day, A.M. van Heeckeren, E. Min, and L.W. Velsor Role for cystic fibrosis transmembrane conductance regulator protein in a glutathione response to bronchopulmonary Pseudomonas infection Infec. Immun. 72 2004 2045 2051
75. J.H. Roum, R. Buhl, N.G. McElvany, Z. Borok, and R.G. Crystal Systematic deficiency of glutathione in cystic fibrosis J. Appl. Physiol. 75 1993 2419 2424
76. L.W. Velsor, A. van Heeckeren, and B.J. Day Antioxidant imbalance in the lungs of cystic fibrosis transmembrane conductance regulator protein mutant mice Am. J. Physiol. Lung Cell Mol. Physiol. 281 2001 L31 L38
77. L. Gao, K.J. Kim, J.R. Yankaskas, and H.J. Forman Abnormal glutathione transport in cystic fibrosis airway epithelia Am. J. Physiol. Lung Cell Mol. Physiol. 277 1999 L113 L118
78. P. Linsdell, and J.W. Hanrahan Glutathione permeability of CFTR Am. J. Physiol. 275 1998 C323 C326
79. I. Kogan, M. Ramjeesingh, C. Li, J.F. Kidd, Y. Wang, E.M. Leslie, S.P. Cole, and C.E. Bear CFTR directly mediates nucleotide-regulated glutathione flux EMBO J. 22 2003 1981 1989
80. V.M. Hudson Rethinking cystic fibrosis pathology: the critical role of abnormal reduced glutathione transport caused by CFTR Free Radic. Biol. Med. 30 2001 1440 1461
81. C.C. Winterboum Biological reactivity and biomarkers of the neutrophil oxidant, hypochlorous acid Toxicology 181/182 2002 223 227
82. M. Bilzer, and B.H. Lauterburg Glutathione metabolism in activated human neutrophils: stimulation of glutathione synthesis and consumption of glutathione by reactive oxygen species Eur. J. Clin. Invest. 21 1991 316 322
83. A. van der Vliet, M.N. Nguyen, M.K. Shigenaga, J.P. Eiserich, G.P. Marelich, and C.E. Cross Myeloperoxidase and protein oxidation in cystic fibrosis Am. J. Physiol. Lung Cell Mol. Physiol. 279 2000 L537 L546
84. J.W. Heinecke Tyrosyl radical production by myeloperoxidase: a phagocyte pathway for lipid peroxidation and dityrosine cross-linking of proteins Toxicology 177 2002 11 22
85. K. Morishita, N. Kubota, S. Asano, Y. Kaziro, and S. Nagata Molecular cloning and characterization of cDNA for human myeloperoxidase J. Biol. Chem. 262 1987 3844 3851
86. C.L. Hawkins, D.I. Pattison, and M.J. Davies Hypochlorite-induced oxidation of amino acids, peptides and proteins Amino Acids 25 2003 259 274
87. P. Verdugo Goblet cells secretion and mucogenesis Annu. Rev. Physiol. 52 1990 157 176
88. P. Verdugo Mucin exocytosis Annu. Rev. Respir. Dis. 144 1991 S33 S37
89. M.C. Rose, W.A. Voter, H. Sage, C.F. Brown, and B. Kaufman Effects of deglycosylation on the architecture of ovine submaxillary mucin glycoprotein J. Biol. Chem. 259 1984 3167 3172
90. R. Shogren, T.A. Gerken, and N. Jentoft Role of glycosylation on the conformation and chain dimensions of O-linked glycoproteins: light-scattering studies of ovine submaxillary mucin Biochemistry 28 1989 5525 5536
91. R.C. Rancourt, S. Tai, M. King, S.L. Heltshe, C. Penvari, F.J. Accurso, and C.W. White Thioredoxin liquefies and decreases the viscoelasticity of cystic fibrosis sputum Am. J. Physiol. Lung Cell Mol. Physiol. 286 2004 L931 L938
92. Y. Majoma Mucoactive medications and airway disease Paediatr. Respir. Rev. 3 2002 104 109
93. M.A. Sleigh, J.R. Blake, and N. Liron The propulsion of mucus by cilia Am. Rev. Respir. Dis. 137 1988 726 741
94. C.J. Venglarik, J. Giron-Calle, A.F. Wigley, E. Malle, N. Watanabe, and H.J. Forman Hypochlrorous acid alters bronchial epithelial cell membrane properties and prevention by extracellular glutathione J. Appl. Physiol. 95 2003 2444 2452
95. V. Brinkmann, U. Reichard, C. Goosmann, B. Fauler, Y. Uhlemann, D.S. Weiss, Y. Weinrauch, and A. Zychlinsky Neutrophil extracellular traps kill bacteria Science 303 2004 1532 1535
96. W.L. Lee, and S. Grinstein The tangled webs that neutrophils weave Science 303 2004 1477 1478