The treatment with the probiotic Shewanella putrefaciens Pdp11 of specimens of Solea senegalensis exposed to high stocking densities to enhance their resistance to disease

Fish and Shellfish Immunology

Volumn 41, Issue 2, 2014, Pages 209-221

  Tapia Paniagua, S T ^a   Vidal, S ^a   Lobo, C ^b   Prieto Alamo M J ^c   Jurado, J ^c   Cordero, H ^d   Cerezuela, R ^d   Garcia de la Banda I ^b   Esteban, M A ^d   Balebona, M C ^a   Morinigo M A ^a  

^a UNIVERSITY OF MÁLAGA   (Spain)

^b Centro Oceanográfico de Santander   (Spain)

^c UNIVERSITY OF CÓRDOBA   (Spain)

^d UNIVERSITY OF MURCIA   (Spain)

Author keywords

Density; Pdp11; Probiotic; Solea senegalensis; Stress

Indexed keywords

PRIMER DNA; PROBIOTIC AGENT;

ANIMAL; AQUACULTURE; CLUSTER ANALYSIS; COMPARATIVE STUDY; CROWDING (AREA); DENATURING GRADIENT GEL ELECTROPHORESIS; DISEASE RESISTANCE; DRUG EFFECTS; FLATFISH; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; GENETICS; GOBLET CELL; IMMUNOLOGY; MICROBIOLOGY; MICROFLORA; MOLECULAR CLONING; NONPARAMETRIC TEST; PHYSIOLOGICAL STRESS; PROCEDURES; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHEWANELLA PUTREFACIENS;

ANIMALS; AQUACULTURE; CLONING, MOLECULAR; CLUSTER ANALYSIS; CROWDING; DENATURING GRADIENT GEL ELECTROPHORESIS; DISEASE RESISTANCE; DNA PRIMERS; FLATFISHES; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; GOBLET CELLS; MICROBIOTA; PROBIOTICS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SHEWANELLA PUTREFACIENS; STATISTICS, NONPARAMETRIC; STRESS, PHYSIOLOGICAL;

EID: 84907710462     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2014.08.019     Document Type: Article

References (90)

1. Tort L. Stress and immune modulation in fish. Dev Comp Immunol 2011, 35:1366-1375.
2. Cnaani A., Tinman S., Avidar Y., Ron M., Hulata G. Comparative study of biochemical parameters in response to stress in Oreochromis aureus, O. mossambicus and two strains of O.niloticus. Aquac Res 2004, 35(15):1434-1440.
3. Verthaak A.D. Disease prevalence in flounder (Platichthys flesus) from the Dutch Wadden Sea as indicator of environmental quality: a summary of 1988-2005 surveys. JSea Res 2013, 82:142-152.
4. Merino G.E., Piedrahita R.H., Conklin D.E. The effect of fish stocking density on the growth of California halibut (Paralichthys californicus) juveniles. Aquaculture 2007, 265:178-186.
5. Schram E., van der Heul J.W., Kamstra A., Verdegen M.C.J. Stocking density-dependent growth of Dover sole (Solea solea). Aquaculture 2006, 252:339-347.
6. Salas-Leiton E., Anguís V., Manchado M., Cañavate J.P. Growth, feeding and oxygen consumption of Senegalese sole (Solea senegalensis) juveniles stocked at different densities. Aquaculture 2008, 285:84-89.
7. Salas-Leiton E., Anguis V., Martín-Antonio B., Crespo D., Planas J.V., Infante C., et al. Effects of stocking density and feed ration on growth and gene expression in the Senegalese sole (Solea senegalensis): potential effects on the immune response. Fish Shellfish Immun 2010, 28:296-302.
8. Bailey M.T., Dowd S.E., Galley J.D., Hufnagle A.R., Allen R.G., Leyte M. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun 2011, 25:397-407.
9. Picchietti S., Mazzini M., Taddei A.R., Renna R., Fausto A.M., Mulero V., et al. Effects of administration of probiotic strains on GALT of larval gilthead seabream: immunohistochemical and ultrastructural studies. Fish Shellfish Immun 2007, 22:57-67.
10. Semova I., Carten J.D., Stombaugh J., Mackey L.C., Knight R., Farber S.A., et al. Microbiota regulate intestinal absorption and metabolism of fatty acids in the zebrafish. Cell Host Microbe 2012, 12:277-288.
11. Ringø E., Løvmo L., Kristiansen M., Bakken Y., Salinas I., Myklebust R., et al. Lacticacid bacteria vs pathogens in the gastrointestinal tract of fish: a review. Aquac Res 2010, 41:451-467.
12. Ringø E., Olsen R.E., Gifstad T.Ø., Dalmo R.A., Almund H., Hemre G.-I., et al. Prebiotics in aquaculture: a review. Aquac Nutr 2010, 16:117-136.
13. Celli J., Knodler L.A. Of microbes and membranes pathogenic subversion of host cell process. Cell Host Microbe 2008, 4:514-518.
14. Zhou Z., He S., Liu Y., Shi P., Yao B., Ring Ø.E. Do stocking densities affect the gut microbiota of gibel carp Carassius auratus gibelio cultured in ponds?. Aquac Res Dev 2011, S1:003. 10.4172/2155-9546-S1-003.
15. Rollo A., Sulpizi R., Nardi M., Silvi S., Orpianesi C., Caggiano M., et al. Live microbial feed supplement in aquaculture for improvement of stress tolerance. Fish Physiol Biochem 2006, 32:167-177.
16. Taoka Y., Maeda H., Jo J., Jeon M., Bai S.C., Lee W., et al. Growth, stress tolerance and non-specific immune response of Japanese flounder Paralichthys olivaceus to probiotics in a closed recirculating system. Fish Sci 2006, 72:310-321.
17. ® during transportation of cardinal tetra, Paracheirodon axelrodi (Schultz) in the Amazon. Aquac Res 2009, 40:157-165.
18. + probiotics. JAnim Sci 2014, 92:2017-2029.
19. Tapia-Paniagua S.T., Díaz-Rosales P., León-Rubio J.M., García de la Banda I., Lobo C., Alarcón F.J., et al. Use of the probiotic Shewanella putrefaciens Pdp11 on the culture of Senegalese sole (Solea senegalensis, Kaup 1858) and gilthead seabream (Sparus aurata L.). Aquac Int 2012, 20:1025-1039.
20. Varela J.L., Ruiz-Jarabo I., Vargas-Chacoff L., Arijo S., León-Rubio J.M., García-Millán I., et al. Dietary administration of probiotic Pdp11 promotes growth and improves stress tolerance to high stocking density in Sparus auratus. Aquaculture 2010, 309:265-271.
21. Gonçalves A.T., Maita M., Futami K., Endo M., Katagiri Effects of a probiotic bacterial Lactobacillus rhamnosus dietary supplement on the crowding stress response of juvenile Nile tilapia Oreochromis niloticus. Fish Sci 2011, 77:633-642.
22. Ringø E., Myklebust R., Mayhew T.M., Olsen R.E. Bacterial translocation and pathogenesis in the digestive tract of larvae and fry. Aquaculture 2007, 268:251-264.
23. Berg R.D. Bacterial translocation from the gastrointestinal tract. Adv Exp Med Biol 1999, 473:11-30.
24. Chabrillón M., Rico S., Balebona M.C., Moriñigo M.A. Adhesion to sole, Solea senegalensis Kaup, mucus of microorganisms isolated from farmed fish, and their interaction with Photobacterium damselae subsp. piscicida. JFish Dis 2005, 28:229-237.
25. Chabrillón M., Rico R.M., Arijo S., Diaz-Rosales P., Balebona M.C., Moriñigo M.A. Interactions of microorganisms isolated from gilthead seabream, Sparus aurata L., on Vibrio harveyi, a pathogen of farmed Senegalese sole, Solea senegalensis (Kaup). JFish Dis 2005, 28:531-537.
26. Díaz-Rosales P., Arijo S., Chabrillón M., Alarcón F.J., Tapia-Paniagua S.T., Martínez Manzanares E., et al. Effects of two closely related probiotics on respiratory burst activity of Senegalese sole (Solea senegalensis, Kaup) phagocytes, and protection against Photobacterium damselae subsp. piscicida. Aquaculture 2009, 293:16-21.
27. Sáenz de Rodrigáñez M.A., Díaz-Rosales P., Chabrillón M., Smidt H., Arijo S., León-Rubio J.M., et al. Effect of dietary administration of probiotics on growth and intestine functionality of juvenile Senegalese sole (Solea senegalensis, Kaup 1858). Aquac Nutr 2009, 15:177-185.
28. García de La Banda I., Lobo C., León-Rubio J.M., Tapia-Paniagua S., Balebona M.C., Moriñigo M.A., et al. Influence of two closely related probiotics on juvenile Senegalese sole (Solea senegalensis, Kaup 1858) performance and protection against Photobacterium damselae subsp. piscicida. Aquaculture 2010, 306:281-288.
29. Salas-Leiton E., Anguis V., Martín-Antonio B., Crespo D., Planas J.V., Infante C., et al. Effects of stocking density and feed ration on growth and gene expression in the Senegalese sole (Solea senegalensis): potential effects on the immune response. Aquaculture 2010, 28:296-302.
30. Tapia-Paniagua S.T., Chabrillón M., Díaz-Rosales P., García de la Banda I., Lobo C., Balebona M.C., et al. Intestinal microbiota diversity of the flat fish Solea senegalensis (Kaup, 1858) following probiotic administration. Microb Ecol 2010, 60:310-319.
31. Kim D.H., Austin B. Innate immune responses in rainbow trout (Oncorhynchus mykiss, Walbaum) induced by probiotics. Fish Shellfish Immun 2006, 21:513-524.
32. Martínez G., Shaw E.M., Carrillo M., Zanuy S. Protein salting-out method applied to genomic DNA isolation from fish whole blood. Bioresour Tech 1998, 24:138-139.
33. Muyzer G., de Waal E.C., Uitterlinden A.G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction amplified genes for 16S rRNA. Appl Environ Microbiol 1993, 59:695-700.
34. Sanguinetti C.J., Dias-Neto E., Simpson A.J.G. Rapid silver staining and recovery of PCR products separated on polyacrylamide gels. BioTechniques 1994, 17:915-919.
35. Hicks R.E., Amann R.I., Stahl D.A. Dual staining of natural bacterioplankton with 4' 6-diamidino-2-phenylindole and fluorescent oligonucleotide probes targeting kingdom-level 16S rRNA sequences. Appl Environ Microbiol 1992, 58:2158-2163.
36. Kane M.D., Poulsen L.K., Stahl D.A. Monitoring the enrichment and isolation of sulfate-reducing bacteria by using oligonucleotide hybridization probes designed from environmentally derived 16SrRNA sequences. Appl Environ Microbiol 1993, 59:682-686.
37. Gray J.P., Herwig R.P. Phylogenetic analysis of the bacterial communities in marine sediments. Appl Environ Microbiol 1996, 62:4049-4059.
38. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. JMol Biol 1990, 215:403-410.
39. Hammer Ø., Harper D.A.T., Ryan P.D. PAST: palaeontological statistics, ver. software package for education and data analysis. Palaeontol Electrónica 2001, 4(1):9. art. 4, 178kb. http://palaeo-electronica.org/2001_1/past/issue1_01.htm.
40. Prieto-Álamo M.J., Abril N., Osuna-Jiménes I., Pueyo C. Solea senegalensis genes responding to lipopolysaccharide and copper sulphate challenges: large-scale identification by suppression substractive hybridization and absolute quantification of transcriptional profiles by real-time-PCR. Aquat Toxicol 2009, 91:312-319.
41. Osuna-Jiménez I., Williams T.D., Priéto-Álamo M.J., Abril N., Chapman J.K., Pueyo C. Immune- and stress-related transcriptomic responses of Solea senegalensis stimulated with lipopolysaccharide and copper sulphate using heterologous cDNA microarrays. Fish Shellfish Immun 2009, 26:699-706.
42. Pueyo C., Jurado J., Prieto-Alamo M.J., Monje-Casas F., Lopez-Barea J. Multiplex reverse transcription-polymerase chain reaction for determining transcriptional regulation of thioredoxin and glutaredoxin pathways. Methods Enzymol 2002, 347:441-451.
43. Jurado J., Fuentes-Almagro C.A., Prieto-Álamo M.J., Pueyo C. Alternative splicing of c-fos pre-mRNA: contribution of the rates of synthesis and degradation to the copy number of each transcript isoform and detection of a truncated c-Fos immunoreactive species. BMC Mol Biol 2007, 8:83.
44. Prieto-Álamo M.J., Cabrera-Luque J.M., Pueyo C. Absolute quantification of normal and ROS-induced patterns of gene expression: an invivo real-time PCR study in mice. Gene Expr 2003, 11:23-34.
45. Mowry R.W. The special value of methods that color both acidic and vicinal hydroxyl groups in the histochemical study of mucins. With revised directions for the colloidal iron stain, the use of Alcian blue G8x and their combinations with the periodic acid-Schiff reaction. Ann N Y Acad Sci 1963, 106:402-423.
46. Baeverfjord G., Krogdahl Å. Development and regression of soybean meal induced enteritis in Atlantic salmon, Salmo salar L., distal intestine: a comparison with the intestines of fasted fish. JFish Dis 1996, 19:375-387.
47. Bakke-McKellep A.M., Penn M.H., Salas P.M., Refstie S., Sperstad S., Landsverk T., et al. Effects of dietary soyabean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.). Br J Nutr 2007, 97:699-713.
48. Aranguren R., Tafalla C., Novoa B., Figueras A. Experimental transmission of encephalopathy and retinopathy induced by nodavirus and seabream, Sparus aurata, using different infection models. JFish Dis 2002, 25:317-324.
49. Mauri I., Romero A., Acerete L., MacKenzie S., Roher N., Callol A., et al. Changes in complement responses in gilthead seabream (Sparus aurata) and European seabass (Dicentrarchus labrax) under crowding stress, plus viral and bacterial challenges. Fish Shellfish Immun 2011, 30:182-188.
50. Austin B. Vibriosis as causal agents of zoonoses. Vet Microbiol 2010, 140:310-317.
51. Sawabe T., Kita-Tsukamoto K., Thompson F.L. Inferring the evolutionary history of vibrios by means of multilocus sequence analysis. JBacteriol 2007, 189:7932-7936.
52. Thompson F.L., Lida T., Swings J. Biodiversity of vibrios. Microbiol Mol Biol Rev 2004, 68:403-431.
53. Austin B., Zhang X.H. Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates. Lett Appl Microbiol 2006, 43:119-124.
54. Defoirdt T., Halet D., Vervaeren H., Boon N., Van de Wiele T., Sorgeloos P., et al. The bacterial storage compound poly-beta-hydroxybutyrate protects Artemia franciscana from pathogenic Vibrio campbellii. Environ Microbiol 2007, 9:445-452.
55. Zorrilla I., Arijo S., Chabrillon M., Diaz P., Martinez-Manzanares E., Balebona M.C., et al. Vibrio species isolated from diseased farmed sole, Solea senegalensis (Kaup), and evaluation of the potential virulence role of their extracellular products. JFish Dis 2003, 26:103-108.
56. Sugita H., Mizuki H., Itoi S. Diversity of siderophore-producing bacteria isolated from the intestinal tracts of fish along the Japanese coast. Aquac Res 2010, 43:481-488.
57. Holmstrom K., Gram L. Elucidation of the Vibrio anguillarum genetic response to the potential fish probiont Pseudomonas fluorescens AH2 using RNA-arbitrarily primed PCR. JBacteriol 2003, 185:831-842.
58. Patel A.K., Ahire J.J., Pawar S.P., Chaudhari B.L., Shouche Y.S., Chincholkar S.B. Evaluation of probiotic characteristics of Siderophoregenic Bacillus spp. Isolated from dairy waste. Appl Biochem Biotechnol 2010, 160:140-155.
59. Strom-Bestor M., Wiklund T. Inhibitory activity of Pseudomonas sp on Flavobacterium psychrophilum, invitro. JFish Dis 2011, 34:255-264.
60. Fromin N., Hamelin J., Tarnawski S., Roesti D., Jourdain-Miserez K., Forestier N., et al. Statistical analysis of denaturing gel electrophoresis (DGGE) fingerprinting patterns. Environ Microbiol 2002, 4:634-643.
61. Lobo C., Moreno-Ventas X., Tapia-Paniagua S., Rodríguez C., Moriñígo M.A., García de La Banda I. Dietary probiotic supplementation (Shewanella putrefaciens Pdp11) modulates gut microbiota and promotes growth and condition in Senegalese sole larviculture. Fish Physiol Biochem 2014, 40:295-309.
62. Tapia-Paniagua S.T., Díaz-Rosales P., García de la Banda I., Lobo C., Clavijo E., Balebona M.C., et al. Modulation of certain liver fatty acids in Solea senegalensis is influenced by the dietary administration of probiotic microorganisms. Aquaculture 2014, 424-425:234-238.
63. Wenderlaar Bonga S.E. The stress response in fish. Physiol Rev 1997, 7:591-625.
64. Costas B., Aragao C., Dias J., Afonso A., Conceiçao L.E.C. Interactive effects of a high-quality protein diet and high stocking density on the stress response and some innate immune parameters of Senegalese sole Solea senegalensis. Fish Physiol Biochem 2013, 9:1141-1151.
65. Michel C., Bernardet J.F., Daniel P., Chilmonczyk S., Urdaci M., de Kinkelin P. Clinical and aetiological of aspects of a summer enteritic syndrome associated with the sporulating segmented filamentous bacterium Candidatus arthromitus in farmed rainbow trout, Oncorhynchus mykiss (Walbaum). JFish Dis 2002, 25:533-543.
66. Ringø E., Jutfelt F., Kanapathippillai P., Bakken Y., Sundell K., Glette J., et al. Damaging effect of the fish pathogen Aeromonas salmonicida ssp. salmonicida on intestinal enterocytes of Atlantic salmon (Salmo salar L. Cell Tissue Res 2004, 318:305-311.
67. Liu P.C., Lin J.Y., Chuang W.H., Lee K.K. Isolation and characterization of pathogenic Vibrio harveyi (V. carchariae) from the farmed marine cobia fish Rachycentron canadum L. with gastrointestinal syndrome. World J Microbiol Biotechnol 2004, 20:495-499.
68. Ritchie J.M., Rui H.P., Zhou X.H., Iida T., Kodoma T., Ito S., et al. Inflammation and disintegration of intestinal villi in an experimental model for Vibrio parahaemolyticus-induced diarrhea. Plos Pathog 2012, 8:e1002593. 10.1371/journal.ppat.1002593.
69. Luis-Villasenor I.E., Castellanos-Cervantes T., Gomez-Gil B., Carrillo-Garcia A., Campa-Cordova A.I., Ascencio F. Probiotics in the intestinal tract of juvenile whiteleg shrimp Litopenaeus vannamei: modulation of the bacterial community. World J Microbiol Biotechnol 2013, 29:257-265.
70. Olsen R.E., Sundell K., Hansen T., Hemre G.-I., Myklebust R., Mayhew T.M., et al. Acute stress damages intestinal lining of Atlantic salmon, Salmo salar L. An electron microscopical study. Fish Physiol Biochem 2003, 26:211-221.
71. Olsen R.E., Sundell K., Mayhew T.M., Myklebust R., Ringø E. Acute stress alters intestinal function of rainbow trout, Oncorhynchus mykiss (Walbaum). Aquaculture 2005, 250:480-495.
72. Perz J.F., Craig A.S., Stratton C.W., Bodner S.J., Phillips W.E., Schaffner W. Pseudomonas putida septicemia in a special care nursery due to contaminated flush solutions prepared in a hospital pharmacy. JClin Microbiol 2005, 43:5316-5318.
73. Iwalokun B.A., Akinsinde K.A., Lanlenhin O., Onubogu C.C. Bacteriocinogenicity and production of pyocins from Pseudomonas species isolated in Lagos, Nigeria. Afr J Biotechnol 2006, 5:1072-1077.
74. Altinok I., Kayis S., Capkin E. Pseudomonas putida infection in rainbow trout. Aquaculture 2006, 261:850-855.
75. Haldar S., Chatterjee S., Sugimoto N., Das S., Chowdhury N., Hinenoya A., et al. Identification of Vibrio campbellii isolated from diseased farm-shrimps from south India and establishment of its pathogenic potential in an Artemia model. Microbiology 2011, 157:179-188.
76. Ruwandeepika H.A.D., Defoirdt T., Bhowmick P.P., Shekar M., Bossier P., Karunasagar I. Presence of typical and atypical virulence genes in vibrio isolates belonging to the Harveyi clade. JAppl Microbiol 2010, 109:888-899.
77. Cecchini F., Iacumin L., Fontanot M., Comi G., Manzano M. Identification of the unculturable bacteria Candidatus arthromitus in the intestinal content of trouts using Dot blot and Southern blot techniques. Vet Microbiol 2012, 156:389-394.
78. Chisada S., Shimizu K., Kamada H., Matsunaga N., Okino N., Ito M. Vibrios adhere to epithelial cells in the intestinal tract of red sea bream, Pagrus major, utilizing GM4 as an attachment site. FEMS Microbiol Lett 2013, 341:18-26.
79. Finn R., Ahmad T., Coffey E.T., Brayden D.J., Baird A.W., Boyd A. Translocation of Vibrio parahaemolyticus across an invitro M cell model. FEMS Microbiol Lett 2014, 350:65-71.
80. García de la Banda I., Lobo C., Lucas L.M., Moreno-Ventas X., Mira J.R., Medina-López A., et al. Shewanella putrefaciens Pdp11 promotes welfare and confers resistance against pathogens on Solea senegalensis juveniles cultured at low and high densities. Abstracts of the V International sole Workshop, Faro (Portugal) 2011, 24.
81. Torrecillas S., Makol A., Benítez-Santana T., Caballero M.J., Montero D., Sweetman J., et al. Reduced gut bacterial translocation in European sea bass (Dicentrarchus labrax) fed mannan oligosaccharides (MOS). Fish Shellfish Immun 2011, 30:674-681.
82. Smirnov A., Perez R., Amit-Romach E., Sklan D., Uni Z. Mucin dynamics and microbial populations in chicken small intestine are changed by dietary probiotics and antibiotic growth promoter supplementation. JNutr 2005, 135:187-192.
83. Kim Y.S., Ho S.B. Industrial goblet cells and mucins in health and disease: recent insights and progress. Curr Gastroenterol Rep 2010, 12:319-330.
84. Barceló A., Claustre J., Moro F., Chayvialle J.A., Cuber J.C., Plaisancié Mucin secretion is modulated by luminal factors in the isolated vascularly perfused rat colon. Gut 2000, 46:218-224.
85. Holland J.W., Taylor G.W., Rowley A.F. The eicosanoid generating capacity of isolated cell populations from the gills of the rainbow trout, Oncorhynchus mykiss. Comp Biochem Physiol Part C 1999, 122:297-306.
86. Torrecillas S., Makol A., Betancor M.B., Montero D., Caballero M.J., Sweetman J., et al. Enhanced intestinal epithelial barrier health status on European sea bass (Dicentrarchus labrax) fed mannan oligosaccharides. Fish Shellfish Immunol 2013, 34:1485-1495.
87. Northey A., Denis D., Cirino M., Metters K.M., Nantel F. Cellular distribution of prostanoid EP receptors mRNA in the rat gastrointestinal tract. Prostagl Other Lipid Mediat 2000, 62:145-156.
88. Sherman P.M., Ossa J.C., Johnson-Henry K. Unraveling mechanisms of action of probiotics. Nutr Clin Pract 2009, 24:10-14.
89. Andrianifahanana M., Moniaux N., Baha S.K. Regulation of mucin expressions mechanistic aspects and implications for cancer and inflammatory diseases. Biochim Biophys Acta 2006, 1765:189-222.
90. Thai P., Loukoianov A., Wachi S., Wu R. Regulation of airway mucin gene expression. Annu Rev Physiol 2008, 102:1103-1116.