Genes associated with MUC5AC expression in small airway epithelium of human smokers and non-smokers

BMC Medical Genomics

Volumn 5, Issue , 2012, Pages

  Wang, Guoqing ^a   Xu, Zhibo ^a,b   Wang, Rui ^a   Al Hijji, Mohammed ^a   Salit, Jacqueline ^a   Strulovici Barel, Yael ^a   Tilley, Ann E ^a   Mezey, Jason G ^a,c   Crystal, Ronald G ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b CHENGDU SECOND PEOPLE S HOSPITAL   (China)

^c Plant Science Building   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ION CHANNEL; MUCIN; MUCIN 5AC;

ADULT; ARTICLE; ASTHMA; BRONCHOSCOPY; BRONCHUS BIOPSY; BRONCHUS MUCOSA; BRONCHUS MUCUS; CELL DIFFERENTIATION; COHORT ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE REGULATORY NETWORK; GENOME; HUMAN; HUMAN CELL; MALE; MICROARRAY ANALYSIS; MUC5AC ASSSOCIATED CORE GENE; MUC5AC GENE; MUCUS SECRETION; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN SYNTHESIS; RNA SEQUENCE; SECRETORY GRANULE; SEQUENCE ANALYSIS; SMOKING; TRANSCRIPTOMICS; TRANSPORT VESICLE; UPREGULATION; VALIDATION STUDY;

ADULT; ASTHMA; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HUMANS; ION CHANNELS; MUCIN 5AC; MUCUS; RESPIRATORY MUCOSA; SMOKING; UP-REGULATION;

ANIMALIA;

EID: 84861871181     PISSN: None     EISSN: 17558794     Source Type: Journal    
DOI: 10.1186/1755-8794-5-21     Document Type: Article

References (76)

1. Airway mucus function and dysfunction. Fahy JV, Dickey BF, N Engl J Med 2010 363 2233 2247 10.1056/NEJMra0910061 21121836
2. Structure and function of the polymeric mucins in airways mucus. Thornton DJ, Rousseau K, McGuckin MA, Annu Rev Physiol 2008 70 459 486 10.1146/annurev.physiol.70.113006.100702 17850213
3. Respiratory tract mucin genes and mucin glycoproteins in health and disease. Rose MC, Voynow JA, Physiol Rev 2006 86 245 278 10.1152/physrev.00010. 2005 16371599
4. SPDEF is required for mouse pulmonary goblet cell differentiation and regulates a network of genes associated with mucus production. Chen G, Korfhagen TR, Xu Y, Kitzmiller J, Wert SE, Maeda Y, et al. J Clin Invest 2009 119 2914 2924 19759516
5. Sox2 is required for maintenance and differentiation of bronchiolar Clara, ciliated, and goblet cells. Tompkins DH, Besnard V, Lange AW, Wert SE, Keiser AR, Smith AN, et al. PLoS One 2009 4 8248 10.1371/journal.pone.0008248 20011520
6. Beta-catenin regulates differentiation of respiratory epithelial cells in vivo. Mucenski ML, Nation JM, Thitoff AR, Besnard V, Xu Y, Wert SE, et al. Am J Physiol Lung Cell Mol Physiol 2005 289 971 L979 10.1152/ajplung.00172.2005 16040629
7. Notch signaling controls the balance of ciliated and secretory cell fates in developing airways. Tsao PN, Vasconcelos M, Izvolsky KI, Qian J, Lu J, Cardoso WV, Development 2009 136 2297 2307 10.1242/dev.034884 19502490
8. Notch signaling promotes airway mucous metaplasia and inhibits alveolar development. Guseh JS, Bores SA, Stanger BZ, Zhou Q, Anderson WJ, Melton DA, et al. Development 2009 136 1751 1759 10.1242/dev.029249 19369400
9. Involvement of the p38 MAPK pathway in IL-13-induced mucous cell metaplasia in mouse tracheal epithelial cells. Fujisawa T, Ide K, Holtzman MJ, Suda T, Suzuki K, Kuroishi S, et al. Respirology 2008 13 191 202 10.1111/j.1440-1843.2008.01237.x 18339016
10. Threshold of biologic responses of the small airway epithelium to low levels of tobacco smoke. Strulovici-Barel Y, Omberg L, O'Mahony M, Gordon C, Hollmann C, Tilley AE, et al. Am J Respir Crit Care Med 2010 182 1524 1532 10.1164/rccm.201002-0294OC 20693378
11. The relations between structural changes in small airways and pulmonary-function tests. Cosio M, Ghezzo H, Hogg JC, Corbin R, Loveland M, Dosman J, et al. N Engl J Med 1978 298 1277 1281 10.1056/NEJM197806082982303 651978
12. Morphologic and morphometric effects of prolonged cigarette smoking on the small airways. Cosio MG, Hale KA, Niewoehner DE, Am Rev Respir Dis 1980 122 265 271 7416603
13. The nature of small-airway obstruction in chronic obstructive pulmonary disease. Hogg JC, Chu F, Utokaparch S, Woods R, Elliott WM, Buzatu L, et al. N Engl J Med 2004 350 2645 2653 10.1056/NEJMoa032158 15215480
14. Modification of gene expression of the small airway epithelium in response to cigarette smoking. Harvey BG, Heguy A, Leopold PL, Carolan BJ, Ferris B, Crystal RG, J Mol Med (Berl) 2007 85 39 53
15. Small airways in COPD. Barnes PJ, N Engl J Med 2004 350 2635 2637 10.1056/NEJMp048102 15215476
16. IL-13 and epidermal growth factor receptor have critical but distinct roles in epithelial cell mucin production. Zhen G, Park SW, Nguyenvu LT, Rodriguez MW, Barbeau R, Paquet AC, et al. Am J Respir Cell Mol Biol 2007 36 244 253 16980555
17. Regulated airway goblet cell mucin secretion. Davis CW, Dickey BF, Annu Rev Physiol 2008 70 487 512 10.1146/annurev.physiol.70.113006.100638 17988208
18. Regulation of airway mucin gene expression. Thai P, Loukoianov A, Wachi S, Wu R, Annu Rev Physiol 2008 70 405 429 10.1146/annurev.physiol.70.113006. 100441 17961085
19. Secretory cell hyperplasia and defects in Notch activity in a mouse model of leukocyte adhesion deficiency type II. Waterhouse CC, Johnson S, Phillipson M, Zbytnuik L, Petri B, Kelly M, et al. Gastroenterology 2010 138 1079 1090 10.1053/j.gastro.2009.10.049 19900444
20. Stat6-deficient mice develop airway hyperresponsiveness and peribronchial fibrosis during chronic fungal asthma. Blease K, Schuh JM, Jakubzick C, Lukacs NW, Kunkel SL, Joshi BH, et al. Am J Pathol 2002 160 481 490 10.1016/S0002-9440(10)64867-5 11839568
21. Increased airway epithelial Na+absorption produces cystic fibrosis-like lung disease in mice. Mall M, Grubb BR, Harkema JR, O'Neal WK, Boucher RC, Nat Med 2004 10 487 493 10.1038/nm1028 15077107
22. Pathobiology of cigarette smoke-induced chronic obstructive pulmonary disease. Yoshida T, Tuder RM, Physiol Rev 2007 87 1047 1082 10.1152/physrev. 00048.2006 17615396
23. Advances in mucous cell metaplasia: a plug for mucus as a therapeutic focus in chronic airway disease. Curran DR, Cohn L, Am J Respir Cell Mol Biol 2010 42 268 275 10.1165/rcmb.2009-0151TR 19520914
24. Goblet and Clara cells of human distal airways: evidence for smoking induced changes in their numbers. Lumsden AB, McLean A, Lamb D, Thorax 1984 39 844 849 10.1136/thx.39.11.844 6505991
25. Expression of ErbB receptors and mucins in the airways of long term current smokers. O'Donnell RA, Richter A, Ward J, Angco G, Mehta A, Rousseau K, et al. Thorax 2004 59 1032 1040 10.1136/thx.2004.028043 15563701
26. Overview of the secretory pathway. Lodish H, Berk A, Zipursky SL, Molecular Cell Biology W.H. Freeman, New York 2000
27. Free-radical chemistry of cigarette smoke and its toxicological implications. Church DF, Pryor WA, Environ Health Perspect 1985 64 111 126 3007083
28. Expression of genes involved in oxidative stress responses in airway epithelial cells of smokers with chronic obstructive pulmonary disease. Pierrou S, Broberg P, O'Donnell RA, Pawlowski K, Virtala R, Lindqvist E, et al. Am J Respir Crit Care Med 2007 175 577 586 10.1164/rccm.200607-931OC 17158281
29. Effect of active smoking on the human bronchial epithelium transcriptome. Chari R, Lonergan KM, Ng RT, Macaulay C, Lam WL, Lam S, BMC Genomics 2007 8 297 10.1186/1471-2164-8-297 17727719
30. Genome-wide profiling identifies epithelial cell genes associated with asthma and with treatment response to corticosteroids. Woodruff PG, Boushey HA, Dolganov GM, Barker CS, Yang YH, Donnelly S, et al. Proc Natl Acad Sci USA 2007 104 15858 15863 10.1073/pnas.0707413104 17898169
31. The zinc-finger transcription factor Klf4 is required for terminal differentiation of goblet cells in the colon. Katz JP, Perreault N, Goldstein BG, Lee CS, Labosky PA, Yang VW, et al. Development 2002 129 2619 2628 12015290
32. Relationship of epidermal growth factor receptors to goblet cell production in human bronchi. Takeyama K, Fahy JV, Nadel JA, Am J Respir Crit Care Med 2001 163 511 516 11179132
33. Frequency of driver mutations in lung adenocarcinoma from female never-smokers varies with histologic subtypes and age at diagnosis. Zhang Y, Sun Y, Pan Y, Li C, Shen L, Li Y, et al. Clin Cancer Res 2012 18 1947 1953 10.1158/1078-0432.CCR-11-2511 22317764
34. MUC5AC, cytokeratin 20 and HER2 expression and K-RAS mutations within mucinogenic growth in congenital pulmonary airway malformations. Rossi G, Gasser B, Sartori G, Migaldi M, Costantini M, Mengoli MC, et al. Histopathology 2012
35. Distinct roles of FOXA2 and FOXA3 in allergic airway disease and asthma. Park SW, Verhaeghe C, Nguyenvu LT, Barbeau R, Eisley CJ, Nakagami Y, et al. Am J Respir Crit Care Med 2009 180 603 610 10.1164/rccm.200811-1768OC 19628779
36. Bronchioloalveolar lung carcinomas: K-ras mutations are constant events in the mucinous subtype. Marchetti A, Buttitta F, Pellegrini S, Chella A, Bertacca G, Filardo A, et al. J Pathol 1996 179 254 259 10.1002/(SICI)1096- 9896(199607)179:3<254::AID-PATH589>3.0.CO;2-J 8774479
37. Regulation of mucin gene expression by CREB via a nonclassical retinoic acid signaling pathway. Kim SW, Hong JS, Ryu SH, Chung WC, Yoon JH, Koo JS, Mol Cell Biol 2007 27 6933 6947 10.1128/MCB.02385-06 17646388
38. A nonredundant role for mouse Serpinb3a in the induction of mucus production in asthma. Sivaprasad U, Askew DJ, Ericksen MB, Gibson AM, Stier MT, Brandt EB, et al. J Allergy Clin Immunol 2011 127 254 261 10.1016/j.jaci.2010. 10.009 21126757
39. Ozone and staphylococcal enterotocin B exposure induces emphysema and mucus production that is dependent upon cathepsin C expression [Abstract]. Foley JP, Bolognese BS, Long E, Salmon M, Podolin PL, Am J Respir Crit Care Med 2009
40. Critical role of cytosolic phospholipase A2{alpha} in bronchial mucus hypersecretion in CFTR-deficient mice. Dif F, Wu YZ, Burgel PR, Ollero M, Leduc D, Aarbiou J, et al. Eur Respir J 2010 36 1120 1130 10.1183/09031936.00183409 20413542
41. The protein disulfide isomerase AGR2 is essential for production of intestinal mucus. Park SW, Zhen G, Verhaeghe C, Nakagami Y, Nguyenvu LT, Barczak AJ, et al. Proc Natl Acad Sci USA 2009 106 6950 6955 10.1073/pnas.0808722106 19359471
42. Reduced sialylation status in UDP-N-acetylglucosamine-2-epimerase/N- acetylmannosamine kinase (GNE)-deficient mice. Gagiannis D, Orthmann A, Danssmann I, Schwarzkopf M, Weidemann W, Horstkorte R, Glycoconj J 2007 24 125 130 10.1007/s10719-006-9019-7 17235685
43. Whole genome expression array profiling highlights differences in mucosal defense genes in Barrett's esophagus and esophageal adenocarcinoma. Nancarrow DJ, Clouston AD, Smithers BM, Gotley DC, Drew PA, Watson DI, et al. PLoS One 2011 6 22513 10.1371/journal.pone.0022513 21829465
44. Bi-directional protein transport between the ER and Golgi. Lee MC, Miller EA, Goldberg J, Orci L, Schekman R, Annu Rev Cell Dev Biol 2004 20 87 123 10.1146/annurev.cellbio.20.010403.105307 15473836
45. ER stress and the unfolded protein response in intestinal inflammation. McGuckin MA, Eri RD, Das I, Lourie R, Florin TH, Am J Physiol Gastrointest Liver Physiol 2010 298 820 G832 10.1152/ajpgi.00063.2010 20338921
46. Endoplasmic reticulum (ER) chaperone regulation and survival of cells compensating for deficiency in the ER stress response kinase, PERK. Yamaguchi Y, Larkin D, Lara-Lemus R, Ramos-Castaneda J, Liu M, Arvan P, J Biol Chem 2008 283 17020 17029 10.1074/jbc.M802466200 18426796
47. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Lee AH, Iwakoshi NN, Glimcher LH, Mol Cell Biol 2003 23 7448 7459 10.1128/MCB.23.21.7448-7459.2003 14559994
48. EDEM3, a soluble EDEM homolog, enhances glycoprotein endoplasmic reticulum-associated degradation and mannose trimming. Hirao K, Natsuka Y, Tamura T, Wada I, Morito D, Natsuka S, et al. J Biol Chem 2006 281 9650 9658 16431915
49. The CrebA/Creb3-like transcription factors are major and direct regulators of secretory capacity. Fox RM, Hanlon CD, Andrew DJ, J Cell Biol 2010 191 479 492 10.1083/jcb.201004062 21041443
50. Serine proteases stimulate mucous glycoprotein release from hamster tracheal ring organ culture. Niles RM, Christensen TG, Breuer R, Stone PJ, Snider GL, J Lab Clin Med 1986 108 489 497 2877041
51. Maturation of secretory granules. Kogel T, Gerdes HH, Results Probl Cell Differ 2010 50 1 20 19888562
52. Decreased basal mucus secretion by Slp2-a-deficient gastric surface mucous cells. Saegusa C, Tanaka T, Tani S, Itohara S, Mikoshiba K, Fukuda M, Genes Cells 2006 11 623 631 10.1111/j.1365-2443.2006.00964.x 16716193
53. Involvement of conventional kinesin in glucose-stimulated secretory granule movements and exocytosis in clonal pancreatic beta-cells. Varadi A, Ainscow EK, Allan VJ, Rutter GA, J Cell Sci 2002 115 4177 4189 10.1242/jcs.00083 12356920
54. Regulation of pancreatic beta-cell insulin secretion by actin cytoskeleton remodelling: role of gelsolin and cooperation with the MAPK signalling pathway. Tomas A, Yermen B, Min L, Pessin JE, Halban PA, J Cell Sci 2006 119 2156 2167 10.1242/jcs.02942 16638805
55. MUC5AC and MUC5B mucins increase in cystic fibrosis airway secretions during pulmonary exacerbation. Henke MO, John G, Germann M, Lindemann H, Rubin BK, Am J Respir Crit Care Med 2007 175 816 821 10.1164/rccm.200607-1011OC 17255563
56. Identification of pendrin as a common mediator for mucus production in bronchial asthma and chronic obstructive pulmonary disease. Nakao I, Kanaji S, Ohta S, Matsushita H, Arima K, Yuyama N, et al. J Immunol 2008 180 6262 6269 18424749
57. Structure and function of CLCA proteins. Loewen ME, Forsyth GW, Physiol Rev 2005 85 1061 1092 10.1152/physrev.00016.2004 15987802
58. A GABAergic system in airway epithelium is essential for mucus overproduction in asthma. Xiang YY, Wang S, Liu M, Hirota JA, Li J, Ju W, et al. Nat Med 2007 13 862 867 10.1038/nm1604 17589520
59. A novel method of gene transcript profiling in airway biopsy homogenates reveals increased expression of a Na+K+Cl- cotransporter (NKCC1) in asthmatic subjects. Dolganov GM, Woodruff PG, Novikov AA, Zhang Y, Ferrando RE, Szubin R, et al. Genome Res 2001 11 1473 1483 10.1101/gr.191301 11544191
60. Smoking-induced upregulation of AKR1B10 expression in the airway epithelium of healthy individuals. Wang R, Wang G, Ricard MJ, Ferris B, Strulovici-Barel Y, Salit J, et al. Chest 2010 138 1402 1410 10.1378/chest.09-2634 20705797
61. Quality control in microarray assessment of gene expression in human airway epithelium. Raman T, O'Connor TP, Hackett NR, Wang W, Harvey BG, Attiyeh MA, et al. BMC Genomics 2009 10 493 10.1186/1471-2164-10-493 19852842
62. Validation of endogenous control genes for gene expression studies on human ocular surface epithelium. Kulkarni B, Mohammed I, Hopkinson A, Dua HS, PLoS One 2011 6 22301 10.1371/journal.pone.0022301 21857920
63. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Huang D, Sherman B, Lempicki R, Nat Protoc 2009 4 44 57 19131956
64. Biologic phenotyping of the human small airway epithelial response to cigarette smoking. Tilley AE, O'Connor TP, Hackett NR, Strulovici-Barel Y, Salit J, Amoroso N, et al. PLoS One 2011 6 22798 10.1371/journal.pone.0022798 21829517
65. Novel smoking-related genes in the small airway epithelium identified by massively parallel RNA sequencing. Hackett NR, Salit J, Crystal RG, Am J Respir Crit Care Med 2010
66. Localization of TFF3, a new mucus-associated peptide of the human respiratory tract. Wiede A, Jagla W, Welte T, Kohnlein T, Busk H, Hoffmann W, Am J Respir Crit Care Med 1999 159 1330 1335 10194185
67. Tissue localization of human trefoil factors 1, 2, and 3. Madsen J, Nielsen O, Tornoe I, Thim L, Holmskov U, J Histochem Cytochem 2007 55 505 513 10.1369/jhc.6A7100.2007 17242463
68. Suppression of hath1 gene expression directly regulated by hes1 via notch sig-naling is associated with goblet cell depletion in ulcerative colitis. Zheng X, Tsuchiya K, Okamoto R, Iwasaki M, Kano Y, Sakamoto N, Nakamura T, Wata-nabe M, Inflamm Bowel Dis 2011 17 2251 2260 10.1002/ibd.21611 21987298
69. Role of fucosyltransferases in the association between apomucin and Lewis an-tigen expression in normal and malignant gastric epithelium. Lopez-Ferrer A, de BC, Barranco C, Garrido M, Isern J, Carlstedt I, Reis CA, Torrado J, Real Fx, Gut 2000 47 349 356 10.1136/gut.47.3.349 10940270
70. GeneCards: a novel functional genom-ics compendium with automated data mining and query reformulation support. Rebhan M, Chalifa-Caspi V, Prilusky J, Lancet D, Bioin-formatics 1998 14 656 664 10.1093/bioinformatics/14.8.656
71. Barrier role of actin filaments in regulated mucin secretion from airway goblet cells. Ehre C, Rossi AH, Abdullah LH, De PK, Hill S, Olsen JC, Davis CW, Am J Physiol Cell Phy-siol 2005 288 46 C56
72. SCAMP5, NBEA and AMISYN: three candi-date genes for autism involved in secretion of large dense-core vesicles. Castermans D, Volders K, Crepel A, Backx L, De VR, Freson K, Meulemans S, Vermeesch JR, Schrander-Stumpel CT, De RP, et al. Hum Mol Genet 2010 19 1368 1378 10.1093/hmg/ddq013 20071347
73. Notch inhibits expres-sion of the Kruppel-like factor 4 tumor suppressor in the intestinal epithelium. Ghaleb AM, Aggarwal G, Bialkowska AB, Nandan MO, Yang VW, Mol Cancer Res 2008 6 1920 1927 10.1158/1541-7786.MCR-08-0224 19074836
74. A novel stress-induced EDEM va-riant regulating endoplasmic reticulum-associated glycoprotein degradation. Olivari S, Galli C, Alanen H, Ruddock L, Molinari M, J Biol Chem 2005 280 2424 2428 15579471
75. Coordinate regulation of phospholipid biosynthesis and secretory pathway gene ex-pression in xBP-1(S)-induced endoplasmic reticulum biogenesis. Sriburi R, Bommiasamy H, Buldak GL, Robbins GR, Frank M, Jackowski S, Brewer JW, J Biol Chem 2007 282 7024 7034 17213183
76. Roles for UDP-GlcNAc 2-epimerase/ManNAc 6-kinase outside of sialic acid biosynthesis: modulation of sialyltransferase and BiP ex-pression, GM3 and GD3 biosynthesis, proliferation, and apoptosis, and ERK1/2 phos-phorylation. Wang Z, Sun Z, Li AV, Yarema KJ, J Biol Chem 2006 281 27016 27028 10.1074/jbc. M604903200 16847058