A new role for mucins in immunity: Insights from gastrointestinal nematode infection

International Journal of Biochemistry and Cell Biology

Volumn 45, Issue 2, 2013, Pages 364-374

  Hasnain, Sumaira Z ^a   Gallagher, Amanda L ^b,c   Grencis, Richard K ^c   Thornton, David J ^b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Goblet cell; MUC2; Mucin; Mucus; Trichuris muris

Indexed keywords

CALCIUM ION; MUCIN; MUCIN 1; MUCIN 12; MUCIN 13; MUCIN 15; MUCIN 16; MUCIN 17; MUCIN 19; MUCIN 2; MUCIN 20; MUCIN 3A; MUCIN 3B; MUCIN 4; MUCIN 5AC; MUCIN 5B; MUCIN 6; UNCLASSIFIED DRUG;

ANTIGEN PRESENTING CELL; ENTERITIS; GASTROINTESTINAL INFECTION; GLYCOSYLATION; GOBLET CELL; HUMAN; IMMUNITY; INNATE IMMUNITY; INTESTINE EPITHELIUM; NEMATODIASIS; NONHUMAN; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN STRUCTURE; REVIEW; STRONGYLE INFECTION; TH1 CELL; TRICHINOSIS; TRICHURIASIS; TRICHURIS MURIS;

ANIMALS; GASTRIC MUCOSA; GASTROINTESTINAL DISEASES; GLYCOSYLATION; GOBLET CELLS; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNITY, INNATE; MUCINS; NEMATODE INFECTIONS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, QUATERNARY;

NEMATODA; TRICHURIS MURIS;

EID: 84872352407     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2012.10.011     Document Type: Review

References (141)

1. D. Ambort, M.E. Johansson, J.K. Gustafsson, H.E. Nilsson, A. Ermund, and B.R. Johansson Calcium and pH-dependent packing and release of the gel-forming MUC2 mucin Proceedings of the National Academy of Sciences of the United States of America 109 2012 5645 5650
2. D. Ambort, S. van der Post, M.E. Johansson, J. Mackenzie, E. Thomsson, and U. Krengel Function of the CysD domain of the gel-forming MUC2 mucin Biochemical Journal 436 2011 61 70
3. D. Artis, C.S. Potten, K.J. Else, F.D. Finkelman, and R.K. Grencis Trichuris muris: host intestinal epithelial cell hyperproliferation during chronic infection is regulated by interferon-gamma Experimental Parasitology 92 1999 144 153
4. D. Artis, M.L. Wang, S.A. Keilbaugh, W. He, M. Brenes, and G.P. Swain RELMbeta/FIZZ2 is a goblet cell-specific immune-effector molecule in the gastrointestinal tract Proceedings of the National Academy of Sciences of the United States of America 101 2004 13596 13600
5. R. Asada, A. Saito, N. Kawasaki, S. Kanemoto, H. Iwamoto, and M. Oki The endoplasmic reticulum stress transducer OASIS is involved in the terminal differentiation of goblet cells in the large intestine Journal of Biological Chemistry 287 2012 8144 8153
6. N. Asker, D. Baeckstrom, M.A. Axelsson, I. Carlstedt, and G.C. Hansson The human MUC2 mucin apoprotein appears to dimerize before O-glycosylation and shares epitopes with the 'insoluble' mucin of rat small intestine Biochemical Journal 308 Pt 3 1995 873 880
7. N. Asker, M.A. Axelsson, S.O. Olofsson, and G.C. Hansson Dimerization of the human MUC2 mucin in the endoplasmic reticulum is followed by a N-glycosylation-dependent transfer of the mono- and dimers to the Golgi apparatus Journal of Biological Chemistry 273 1998 18857 18863
8. C. Atuma, V. Strugala, A. Allen, and L. Holm The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo American Journal of Physiology: Gastrointestinal and Liver Physiology 280 2001 G922 G929
9. M.A. Axelsson, N. Asker, and G.C. Hansson O-glycosylated MUC2 monomer and dimer from LS 174T cells are water-soluble, whereas larger MUC2 species formed early during biosynthesis are insoluble and contain nonreducible intermolecular bonds Journal of Biological Chemistry 273 1998 18864 18870
10. P. Bager, J. Arnved, S. Rønborg, J. Wohlfahrt, L.K. Poulsen, and T. Westergaard Trichuris suis ova therapy for allergic rhinitis: a randomized, double-blind, placebo-controlled clinical trial Journal of Allergy and Clinical Immunology 125 1 2010 123 130
11. A.J. Bancroft, K.J. Else, and R.K. Grencis Low-level infection with Trichuris muris significantly affects the polarization of the CD4 response European Journal of Immunology 24 1994 3113 3118
12. R.G. Bell, L.S. Adams, and R.W. Ogden Intestinal mucus trapping in the rapid expulsion of Trichinella spiralis by rats: induction and expression analyzed by quantitative worm recovery Infection and Immunity 45 1984 267 272
13. L.A. Bobek, H. Tsai, A.R. Biesbrock, and M.J. Levine Molecular cloning, sequence, and specificity of expression of the gene encoding the low molecular weight human salivary mucin (MUC7) Journal of Biological Chemistry 268 1993 20563 20569
14. M.J. Broadhurst, J.M. Leung, V. Kashyap, J.M. McCune, U. Mahadevan, and J.H. McKerrow IL-22+ CD4+ T cells are associated with therapeutic trichuris trichiura infection in an ulcerative colitis patient Science Translational Medicine 2 2010 60ra88
15. L.S. Bruno, X. Li, L. Wang, R.V. Soares, C.C. Siqueira, and F.G. Oppenheim Two-hybrid analysis of human salivary mucin MUC7 interactions Biochimica et Biophysica Acta 1746 2005 65 72
16. V. Bryant The life cycle of Nematospiroides dubius, Baylis, 1926 (Nematoda: Heligmosomidae) Journal of Helminthology 47 1973 263 268
17. M.P. Buisine, L. Devisme, T.C. Savidge, C. Gespach, B. Gosselin, and N. Porchet Mucin gene expression in human embryonic and fetal intestine Gut 43 1998 519 524
18. M.P. Buisine, L. Devisme, M.C. Copin, M. Durand-Reville, B. Gosselin, and J.P. Aubert Developmental mucin gene expression in the human respiratory tract American Journal of Respiratory Cell and Molecular Biology 20 1999 209 218
19. Y. Chen, Y.H. Zhao, T.B. Kalaslavadi, E. Hamati, K. Nehrke, and A.D. Le Genome-wide search and identification of a novel gel-forming mucin MUC19/Muc19 in glandular tissues American Journal of Respiratory Cell and Molecular Biology 30 2004 155 165
20. E.Y. Chen, N. Yang, P.M. Quinton, and W.C. Chin A new role for bicarbonate in mucus formation American Journal of Physiology: Lung Cellular and Molecular Physiology 299 2010 L542 L549
21. L.J. Cliffe, and R.K. Grencis The Trichuris muris system: a paradigm of resistance and susceptibility to intestinal nematode infection Advances in Parasitology 57 2004 255 307
22. L.J. Cliffe, N.E. Humphreys, T.E. Lane, C.S. Potten, C. Booth, and R.K. Grencis Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion Science 308 2005 1463 1465
23. A.P. Corfield, N. Myerscough, N. Bradfield, A. Corfield Cdo, M. Gough, and J.R. Clamp Colonic mucins in ulcerative colitis: evidence for loss of sulfation Glycoconjugate Journal 13 1996 809 822
24. N.A. Croll The location of parasites within their hosts: the influence of host feeding and diet on the dispersion of adults of Nippostrongylus brasiliensis in the intestine of the rat International Journal for Parasitology 6 1976 441 448
25. R. D'Elia, M.L. DeSchoolmeester, L.A. Zeef, S.H. Wright, A.D. Pemberton, and K.J. Else Expulsion of Trichuris muris is associated with increased expression of angiogenin 4 in the gut and increased acidity of mucins within the goblet cell BMC Genomics 10 2009 492
26. C.W. Davis, and B.F. Dickey Regulated airway goblet cell mucin secretion Annual Review of Physiology 70 2008 487 512
27. P.A. Dawson, S. Huxley, B. Gardiner, T. Tran, J.L. McAuley, and S. Grimmond Reduced mucin sulfonation and impaired intestinal barrier function in the hyposulfataemic NaS1 null mouse Gut 58 2009 910 919
28. C. De Bolos, M. Garrido, and F.X. Real MUC6 apomucin shows a distinct normal tissue distribution that correlates with Lewis antigen expression in the human stomach Gastroenterology 109 1995 723 734
29. M.S. Dehlawi, Y.R. Mahida, K. Hughes, and D. Wakelin Effects of Trichinella spiralis infection on intestinal pathology in mice lacking interleukin-4 (IL-4) or intestinal trefoil factor (ITF/TFF3) Parasitology International 55 2006 207 211
30. D. Despommier, L. Aron, and L. Turgeon Trichinella spiralis: growth of the intracellular (muscle) larva Experimental Parasitology 37 1975 108 116
31. D.D. Despommier How does Trichinella spiralis make itself at home? Parasitology Today 14 1998 318 323
32. P.G. Douch, G.B. Harrison, L.L. Buchanan, and K.S. Greer In vitro bioassay of sheep gastrointestinal mucus for nematode paralysing activity mediated by substances with some properties characteristic of SRS-A International Journal for Parasitology 13 1983 207 212
33. K.J. Else, and R.K. Grencis Helper T-cell subsets in mouse trichuriasis Parasitology Today 7 1991 313 316
34. K.J. Else, and R.K. Grencis Cellular immune responses to the murine nematode parasite Trichuris muris. I. Differential cytokine production during acute or chronic infection Immunology 72 1991 508 513
35. K.J. Else, L. Hultner, and R.K. Grencis Cellular immune responses to the murine nematode parasite Trichuris muris. II. Differential induction of TH-cell subsets in resistant versus susceptible mice Immunology 75 1992 232 237
36. K.J. Else, G.M. Entwistle, and R.K. Grencis Correlations between worm burden and markers of Th1 and Th2 cell subset induction in an inbred strain of mouse infected with Trichuris muris Parasite Immunology 15 1993 595 600
37. F. Escande, N. Porchet, A. Bernigaud, D. Petitprez, J.P. Aubert, and M.P. Buisine The mouse secreted gel-forming mucin gene cluster Biochimica et Biophysica Acta 1676 2004 240 250
38. F.D. Finkelman, T. Shea-Donohue, J. Goldhill, C.A. Sullivan, S.C. Morris, and K.B. Madden Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models Annual Review of Immunology 15 1997 505 533
39. F.D. Finkelman, T. Shea-Donohue, S.C. Morris, L. Gildea, R. Strait, and K.B. Madden Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites Immunological Reviews 201 2004 139 155
40. M.E. Forgue-Lafitte, B. Fabiani, P.P. Levy, N. Maurin, J.F. Flejou, and J. Bara Abnormal expression of M1/MUC5AC mucin in distal colon of patients with diverticulitis, ulcerative colitis and cancer International Journal of Cancer 121 2007 1543 1549
41. R.A. Forman, M.L. Deschoolmeester, R.J. Hurst, S.H. Wright, A.D. Pemberton, and K.J. Else The goblet cell is the cellular source of the anti-microbial angiogenin 4 in the large intestine post Trichuris muris infection PLoS One 7 2012 e42248
42. T. Ganz Angiogenin: an antimicrobial ribonuclease Nature Immunology 4 2003 213 214
43. W.C. Gause, J.F. Urban Jr., and M.J. Stadecker The immune response to parasitic helminths: insights from murine models Trends in Immunology 24 2003 269 277
44. T.A. Gerken Biophysical approaches to salivary mucin structure, conformation and dynamics Critical Reviews in Oral Biology and Medicine 4 1993 261 270
45. T.A. Gerken O-glycoprotein biosynthesis: site localization by Edman degradation and site prediction based on random peptide substrates Methods in Molecular Biology 842 2012 81 108
46. I.K. Gipson, and T. Inatomi Cellular origin of mucins of the ocular surface tear film Advances in Experimental Medicine and Biology 438 1998 221 227
47. R.K. Grencis, L. Hultner, and K.J. Else Host protective immunity to Trichinella spiralis in mice: activation of Th cell subsets and lymphokine secretion in mice expressing different response phenotypes Immunology 74 1991 329 332
48. R.K. Grencis Cytokine-mediated regulation of intestinal helminth infections: the Trichuris muris model Annals of Tropical Medicine and Parasitology 87 1993 643 647
49. W. Guang, H. Ding, S.J. Czinn, K.C. Kim, T.G. Blanchard, and E.P. Lillehoj Muc1 cell surface mucin attenuates epithelial inflammation in response to a common mucosal pathogen Journal of Biological Chemistry 285 2010 20547 20557
50. T.L. Gururaja, J.H. Levine, D.T. Tran, G.A. Naganagowda, K. Ramalingam, and N. Ramasubbu Candidacidal activity prompted by N-terminus histatin-like domain of human salivary mucin (MUC7)1 Biochimica et Biophysica Acta 1431 1999 107 119
51. J.K. Gustafsson, A. Ermund, M.E. Johansson, A. Schutte, G.C. Hansson, and H. Sjovall An ex vivo method for studying mucus formation, properties, and thickness in human colonic biopsies and mouse small and large intestinal explants American Journal of Physiology: Gastrointestinal and Liver Physiology 302 2012 G430 G438
52. J.K. Gustafsson, A. Ermund, D. Ambort, M.E. Johansson, H.E. Nilsson, and K. Thorell Bicarbonate and functional CFTR channel are required for proper mucin secretion and link cystic fibrosis with its mucus phenotype Journal of Experimental Medicine 209 2012 1263 1272
53. K. Hashimoto, R. Uchikawa, T. Tegoshi, K. Takeda, M. Yamada, and N. Arizono Depleted intestinal goblet cells and severe pathological changes in SCID mice infected with Heligmosomoides polygyrus Parasite Immunology 31 2009 457 465
54. S.Z. Hasnain, H. Wang, J.E. Ghia, N. Haq, Y. Deng, and A. Velcich Mucin gene deficiency in mice impairs host resistance to an enteric parasitic infection Gastroenterology 138 2010 1763 1771
55. S.Z. Hasnain, C.M. Evans, M. Roy, A.L. Gallagher, K.N. Kindrachuk, and L. Barron Muc5ac: a critical component mediating the rejection of enteric nematodes Journal of Experimental Medicine 208 2011 893 900
56. S.Z. Hasnain, D.J. Thornton, and R.K. Grencis Changes in the mucosal barrier during acute and chronic Trichuris muris infection Parasite Immunology 33 2011 45 55
57. S.Z. Hasnain, M.A. McGuckin, R.K. Grencis, and D.J. Thornton Serine protease(s) secreted by the nematode Trichuris muris degrade the mucus barrier PLOS Neglected Tropical Diseases 6 2012 e1856
58. C.K. Heazlewood, M.C. Cook, R. Eri, G.R. Price, S.B. Tauro, and D. Taupin Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis PLoS Medicine 5 2008 e54
59. M.O. Henke, G. John, C. Rheineck, S. Chillappagari, L. Naehrlich, and B.K. Rubin Serine proteases degrade airway mucins in cystic fibrosis Infection and Immunity 79 2011 3438 3444
60. D.R. Herbert, J.Q. Yang, S.P. Hogan, K. Groschwitz, M. Khodoun, and A. Munitz Intestinal epithelial cell secretion of RELM-beta protects against gastrointestinal worm infection Journal of Experimental Medicine 206 2009 2947 2957
61. A. Herrmann, J.R. Davies, G. Lindell, S. Martensson, N.H. Packer, and D.M. Swallow Studies on the "insoluble" glycoprotein complex from human colon Identification of reduction-insensitive MUC2 oligomers and C-terminal cleavage Journal of Biological Chemistry 274 1999 15828 15836
62. S.B. Ho, A.M. Roberton, L.L. Shekels, C.T. Lyftogt, G.A. Niehans, and N.W. Toribara Expression cloning of gastric mucin complementary DNA and localization of mucin gene expression Gastroenterology 109 1995 735 747
63. M.A. Hollingsworth, and B.J. Swanson Mucins in cancer: protection and control of the cell surface Nature Reviews Cancer 4 2004 45 60
64. S.D. Hurst, T. Muchamuel, D.M. Gorman, J.M. Gilbert, T. Clifford, and S. Kwan New IL-17 family members promote Th1 or Th2 responses in the lung: in vivo function of the novel cytokine IL-25 Journal of Immunology 169 2002 443 453
65. A.L. Innes, S.D. Carrington, D.J. Thornton, S. Kirkham, K. Rousseau, and R.H. Dougherty Ex vivo sputum analysis reveals impairment of protease-dependent mucus degradation by plasma proteins in acute asthma American Journal of Respiratory and Critical Care Medicine 180 2009 203 210
66. I. Iontcheva, F.G. Oppenheim, and R.F. Troxler Human salivary mucin MG1 selectively forms heterotypic complexes with amylase, proline-rich proteins, statherin, and histatins Journal of Dental Research 76 1997 734 743
67. N. Ishikawa, B.B. Shi, A.I. Khan, and Y. Nawa Reserpine-induced sulphomucin production by goblet cells in the jejunum of rats and its significance in the establishment of intestinal helminths Parasite Immunology 17 1995 581 586
68. N. Ishikawa, D. Wakelin, and Y.R. Mahida Role of T helper 2 cells in intestinal goblet cell hyperplasia in mice infected with Trichinella spiralis Gastroenterology 113 1997 542 549
69. M.E. Johansson, M. Phillipson, J. Petersson, A. Velcich, L. Holm, and G.C. Hansson The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria Proceedings of the National Academy of Sciences of the United States of America 105 2008 15064 15069
70. M.E. Johansson, K.A. Thomsson, and G.C. Hansson Proteomic analyses of the two mucus layers of the colon barrier reveal that their main component, the Muc2 mucin, is strongly bound to the Fcgbp protein Journal of Proteome Research 8 2009 3549 3557
71. M.M. Jumblatt, R.W. McKenzie, P.S. Steele, C.G. Emberts, and J.E. Jumblatt MUC7 expression in the human lacrimal gland and conjunctiva Cornea 22 2003 41 45
72. Y. Kawai, J. Yamauchi, K. Soga, M. Yamada, R. Uchikawa, and T. Tegoshi T cell-dependent and -independent expression of intestinal epithelial cell-related molecules in rats infected with the nematode Nippostrongylus brasiliensis Acta Pathologica, Microbiologica et Immunologica Scandinavica 115 2007 210 217
73. M. Kawakubo, Y. Ito, Y. Okimura, M. Kobayashi, K. Sakura, and S. Kasama Natural antibiotic function of a human gastric mucin against Helicobacter pylori infection Science 305 2004 1003 1006
74. M. Kesimer, S. Kirkham, R.J. Pickles, A.G. Henderson, N.E. Alexis, and G. Demaria Tracheobronchial air-liquid interface cell culture: a model for innate mucosal defense of the upper airways? American Journal of Physiology: Lung Cellular and Molecular Physiology 296 2009 L92 L100
75. M. Kesimer, A.M. Makhov, J.D. Griffith, P. Verdugo, and J.K. Sheehan Unpacking a gel-forming mucin: a view of MUC5B organization after granular release American Journal of Physiology: Lung Cellular and Molecular Physiology 298 2010 L15 L22
76. W.I. Khan, P. Blennerhasset, C. Ma, K.I. Matthaei, and S.M. Collins Stat6 dependent goblet cell hyperplasia during intestinal nematode infection Parasite Immunology 23 2001 39 42
77. W.I. Khan, M. Richard, H. Akiho, P.A. Blennerhasset, N.E. Humphreys, and R.K. Grencis Modulation of intestinal muscle contraction by interleukin-9 (IL-9) or IL-9 neutralization: correlation with worm expulsion in murine nematode infections Infection and Immunity 71 2003 2430 2438
78. S. Kirkham, J.K. Sheehan, D. Knight, P.S. Richardson, and D.J. Thornton Heterogeneity of airways mucus: variations in the amounts and glycoforms of the major oligomeric mucins MUC5AC and MUC5B Biochemical Journal 361 2002 537 546
79. M. Kobayashi, H. Lee, J. Nakayama, and M. Fukuda Roles of gastric mucin-type O-glycans in the pathogenesis of Helicobacter pylori infection Glycobiology 19 2009 453 461
80. M. Kondo, J. Tamaoki, K. Takeyama, J. Nakata, and A. Nagai Interleukin-13 induces goblet cell differentiation in primary cell culture from Guinea pig tracheal epithelium American Journal of Respiratory Cell and Molecular Biology 27 2002 536 541
81. J.M. Larsson, H. Karlsson, J.G. Crespo, M.E. Johansson, L. Eklund, and H. Sjovall Altered O-glycosylation profile of MUC2 mucin occurs in active ulcerative colitis and is associated with increased inflammation Inflammatory Bowel Diseases 17 2011 2299 2307
82. S.E. Levison, J.T. McLaughlin, L.A. Zeef, P. Fisher, R.K. Grencis, and J.L. Pennock Colonic transcriptional profiling in resistance and susceptibility to trichuriasis: phenotyping a chronic colitis and lessons for iatrogenic helminthosis Inflammatory Bowel Diseases 16 2010 2065 2079
83. O. Lieleg, C. Lieleg, J. Bloom, C.B. Buck, and K. Ribbeck Mucin biopolymers as broad-spectrum antiviral agents Biomacromolecules 13 2012 1724 1732
84. S. Linden, H. Nordman, J. Hedenbro, M. Hurtig, T. Boren, and I. Carlstedt Strain- and blood group-dependent binding of Helicobacter pylori to human gastric MUC5AC glycoforms Gastroenterology 123 2002 1923 1930
85. R.J. Longman, R. Poulsom, A.P. Corfield, B.F. Warren, N.A. Wright, and M.G. Thomas Alterations in the composition of the supramucosal defense barrier in relation to disease severity of ulcerative colitis Journal of Histochemistry and Cytochemistry 54 2006 1335 1348
86. K. Matsuo, H. Ota, T. Akamatsu, A. Sugiyama, and T. Katsuyama Histochemistry of the surface mucous gel layer of the human colon Gut 40 1997 782 789
87. J.R. McDermott, N.E. Humphreys, S.P. Forman, D.D. Donaldson, and R.K. Grencis Intraepithelial NK cell-derived IL-13 induces intestinal pathology associated with nematode infection Journal of Immunology 175 2005 3207 3213
88. J.R. McDole, L.W. Wheeler, K.G. McDonald, B. Wang, V. Konjufca, and K.A. Knoop Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine Nature 483 2012 345 349
89. M.A. McGuckin, R. Eri, L.A. Simms, T.H. Florin, and G. Radford-Smith Intestinal barrier dysfunction in inflammatory bowel diseases Inflammatory Bowel Diseases 15 2009 100 113
90. M.A. McGuckin, S.K. Linden, P. Sutton, and T.H. Florin Mucin dynamics and enteric pathogens Nature Reviews Microbiology 9 2011 265 278
91. G.J. McKenzie, C.L. Emson, S.E. Bell, S. Anderson, P. Fallon, and G. Zurawski Impaired development of Th2 cells in IL-13-deficient mice Immunity 9 1998 423 432
92. R. Mejias-Luque, S.K. Linden, M. Garrido, H. Tye, M. Najdovska, and B.J. Jenkins Inflammation modulates the expression of the intestinal mucins MUC2 and MUC4 in gastric tumors Oncogene 29 2010 1753 1762
93. H.R. Miller, J.F. Huntley, and G.R. Wallace Immune exclusion and mucus trapping during the rapid expulsion of Nippostrongylus brasiliensis from primed rats Immunology 44 1981 419 429
94. H.R. Miller Gastrointestinal mucus, a medium for survival and for elimination of parasitic nematodes and protozoa Parasitology 94 Suppl. 1987 S77 S100
95. D.R. Neill, S.H. Wong, A. Bellosi, R.J. Flynn, M. Daly, and T.K. Langford Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity Nature 464 2010 1367 1370
96. B.M. Ogilvie, and D.J. Hockley Effects of immunity of Nippostrongylus brasiliensis adult worms: reversible and irreversible changes in infectivity, reproduction, and morphology Journal of Parasitology 54 1968 1073 1084
97. B.M. Ogilvie, and R.J. Love Co-operation between antibodies and cells in immunity to a nematode parasite Transplantation Reviews 19 1974 147 169
98. T.S. Panesar, and N.A. Croll The location of parasites within their hosts: site selection by Trichuris muris in the laboratory mouse International Journal for Parasitology 10 1980 261 273
99. S.W. Park, G. Zhen, C. Verhaeghe, Y. Nakagami, L.T. Nguyenvu, and A.J. Barczak The protein disulfide isomerase AGR2 is essential for production of intestinal mucus Proceedings of the National Academy of Sciences of the United States of America 106 2009 6950 6955
100. N. Patel, T. Kreider, J.F. Urban Jr., and W.C. Gause Characterisation of effector mechanisms at the host:parasite interface during the immune response to tissue-dwelling intestinal nematode parasites International Journal for Parasitology 39 2009 13 21
101. J. Perez-Vilar, S.H. Randell, and R.C. Boucher C-mannosylation of MUC5AC and MUC5B Cys subdomains Glycobiology 14 2004 325 337
102. A. Phalipon, A. Cardona, J.P. Kraehenbuhl, L. Edelman, P.J. Sansonetti, and B. Corthesy Secretory component: a new role in secretory IgA-mediated immune exclusion in vivo Immunity 17 2002 107 115
103. P. Pigny, V. Guyonnet-Duperat, A.S. Hill, W.S. Pratt, S. Galiegue-Zouitina, and M.C. d'Hooge Human mucin genes assigned to 11p15.5: identification and organization of a cluster of genes Genomics 38 1996 340 352
104. D.K. Podolsky, G. Gerken, A. Eyking, and E. Cario Colitis-associated variant of TLR2 causes impaired mucosal repair because of TFF3 deficiency Gastroenterology 137 2009 209 220
105. A.E. Price, H.E. Liang, B.M. Sullivan, R.L. Reinhardt, C.J. Eisley, and D.J. Erle Systemically dispersed innate IL-13-expressing cells in type 2 immunity Proceedings of the National Academy of Sciences of the United States of America 107 2010 11489 11494
106. R.L. Pullan, and S.J. Brooker The global limits and population at risk of soil-transmitted helminth infections in 2010 Parasites & Vectors 5 2012 81
107. P.M. Quinton Cystic fibrosis: impaired bicarbonate secretion and mucoviscidosis Lancet 372 2008 415 417
108. P.M. Quinton Role of epithelial HCO3(-) transport in mucin secretion: lessons from cystic fibrosis American Journal of Physiology-Cell Physiology 299 2010 C1222 C1233
109. P.M. Quinton Birth of mucus American Journal of Physiology: Lung Cellular and Molecular Physiology 298 2010 L13 L14
110. S. Rachagani, M.P. Torres, N. Moniaux, and S.K. Batra Current status of mucins in the diagnosis and therapy of cancer Biofactors 35 2009 509 527
111. B.D. Raynal, T.E. Hardingham, J.K. Sheehan, and D.J. Thornton Calcium-dependent protein interactions in MUC5B provide reversible cross-links in salivary mucus Journal of Biological Chemistry 278 2003 28703 28710
112. S.A. Saenz, M.C. Siracusa, J.G. Perrigoue, S.P. Spencer, J.F. Urban Jr., and J.E. Tocker IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses Nature 464 2010 1362 1366
113. M. Sasaki, H. Ikeda, and Y. Nakanuma Expression profiles of MUC mucins and trefoil factor family (TFF) peptides in the intrahepatic biliary system: physiological distribution and pathological significance Progress in Histochemistry and Cytochemistry 42 2007 61 110
114. J.K. Sheehan, S. Kirkham, M. Howard, P. Woodman, S. Kutay, and C. Brazeau Identification of molecular intermediates in the assembly pathway of the MUC5AC mucin Journal of Biological Chemistry 279 2004 15698 15705
115. J.K. Sheehan, K. Oates, and I. Carlstedt Electron microscopy of cervical, gastric and bronchial mucus glycoproteins Biochemical Journal 239 1986 147 153
116. Y.H. Sheng, S.Z. Hasnain, T.H. Florin, and M.A. McGuckin Mucins in inflammatory bowel diseases and colorectal cancer Journal of Gastroenterology and Hepatology 27 2012 28 38
117. R.A. Strugnell, and O.L. Wijburg The role of secretory antibodies in infection immunity Nature Reviews Microbiology 8 2010 656 667
118. M.V. Sukhdeo, R.T. O'Grady, and S.C. Hsu The site selected by the larvae of Heligmosomoides polygyrus Journal of Helminthology 58 1984 19 23
119. R.W. Summers, D.E. Elliott, K. Qadir, J.F. Urban Jr., R. Thompson, and J.V. Weinstock Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease American Journal of Gastroenterology 98 2003 2034 2041
120. R.W. Summers, D.E. Elliott, J.F. Urban Jr., R. Thompson, and J.V. Weinstock Trichuris suis therapy in Crohn's disease Gut 54 2005 87 90
121. R.W. Summers, D.E. Elliott, J.F. Urban Jr., R.A. Thompson, and J.V. Weinstock Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial Gastroenterology 128 2005 825 832
122. R.W. Summers, D.E. Elliott, and J.V. Weinstock Therapeutic colonization with Trichuris suis Archives of Pathology and Laboratory Medicine 130 2006 1753 author reply 1753-1754
123. R.W. Summers, D.E. Elliott, and J.V. Weinstock Trichuris suis might be effective in treating allergic rhinitis Journal of Allergy and Clinical Immunology 125 2010 766 767
124. L. Thim, F. Madsen, and S.S. Poulsen Effect of trefoil factors on the viscoelastic properties of mucus gels European Journal of Clinical Investigation 32 2002 519 527
125. K.A. Thomsson, J.M. Holmen-Larsson, J. Angstrom, M.E. Johansson, L. Xia, and G.C. Hansson Detailed O-glycomics of the Muc2 mucin from colon of wild-type, core 1- and core 3-transferase-deficient mice highlights differences compared with human MUC2 Glycobiology 22 2012 1128 1139
126. D.J. Thornton, N. Khan, R. Mehrotra, M. Howard, E. Veerman, and N.H. Packer Salivary mucin MG1 is comprised almost entirely of different glycosylated forms of the MUC5B gene product Glycobiology 9 1999 293 302
127. D.J. Thornton, and J.K. Sheehan From mucins to mucus: toward a more coherent understanding of this essential barrier Proceedings of the American Thoracic Society 1 2004 54 61
128. D.J. Thornton, K. Rousseau, and M.A. McGuckin Structure and function of the polymeric mucins in airways mucus Annual Review of Physiology 70 2008 459 486
129. Y. Tobisawa, Y. Imai, M. Fukuda, and H. Kawashima Sulfation of colonic mucins by N-acetylglucosamine 6-O-sulfotransferase-2 and its protective function in experimental colitis in mice Journal of Biological Chemistry 285 2010 6750 6760
130. R.F. Troxler, I. Iontcheva, F.G. Oppenheim, D.P. Nunes, and G.D. Offner Molecular characterization of a major high molecular weight mucin from human sublingual gland Glycobiology 7 1997 965 973
131. D. Tsubokawa, Y. Goso, T. Nakamura, H. Maruyama, F. Yatabe, and M. Kurihara Rapid and specific alterations of goblet cell mucin in rat airway and small intestine associated with resistance against Nippostrongylus brasiliensis reinfection Experimental Parasitology 130 2012 209 217
132. S. Vaishnava, M. Yamamoto, K.M. Severson, K.A. Ruhn, X. Yu, and O. Koren The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine Science 334 2011 255 258
133. P. Verdugo, I. Deyrup-Olsen, M. Aitken, M. Villalon, and D. Johnson Molecular mechanism of mucin secretion. I. The role of intragranular charge shielding Journal of Dental Research 66 1987 506 508
134. P. Verdugo, M. Aitken, L. Langley, and M.J. Villalon Molecular mechanism of product storage and release in mucin secretion. II. The role of extracellular Ca++ Biorheology 24 1987 625 633
135. D. Wakelin Acquired immunity to Trichuris muris in the albino laboratory mouse Parasitology 57 1967 515 524
136. X. Wei, Z. Yang, F.E. Rey, V.K. Ridaura, N.O. Davidson, and J.I. Gordon Fatty acid synthase modulates intestinal barrier function through palmitoylation of mucin 2 Cell Host Microbe 11 2012 140 152
137. R.B. Wescott, and A.C. Todd Adaptation of Nippostrongylus brasiliensis to the mouse The Journal of Parasitology 52 1966 233 236
138. L. Whittaker, N. Niu, U.A. Temann, A. Stoddard, R.A. Flavell, and A. Ray Interleukin-13 mediates a fundamental pathway for airway epithelial mucus induced by CD4 T cells and interleukin-9 American Journal of Respiratory Cell and Molecular Biology 27 2002 593 602
139. M. Wills-Karp, R. Rani, K. Dienger, I. Lewkowich, J.G. Fox, and C. Perkins Trefoil factor 2 rapidly induces interleukin 33 to promote type 2 immunity during allergic asthma and hookworm infection Journal of Experimental Medicine 209 2012 607 622
140. J. Yamauchi, Y. Kawai, M. Yamada, R. Uchikawa, T. Tegoshi, and N. Arizono Altered expression of goblet cell- and mucin glycosylation-related genes in the intestinal epithelium during infection with the nematode Nippostrongylus brasiliensis in rat Acta Pathologica, Microbiologica et Immunologica Scandinavica 114 2006 270 278
141. L. Zhu, P. Lee, D. Yu, S. Tao, and Y. Chen Cloning and characterization of human MUC19 gene American Journal of Respiratory Cell and Molecular Biology 45 2011 348 358