Calcium-activated Chloride Channel Regulator 1 (CLCA1) Controls Mucus Expansion in Colon by Proteolytic Activity

EBioMedicine - Tập 33 - Trang 134-143 - 2018
Elisabeth E.L. Nyström1, George M.H. Birchenough1, Sjoerd van der Post1, Liisa Arike1, Achim D. Gruber2, Gunnar C. Hansson1, Malin E.V. Johansson1
1Department of Medical Biochemistry, Institute of Biomedicine, University of Gothenburg, 40530 Gothenburg, Sweden
2Department of Veterinary Pathology, Freie Universität Berlin, Germany

Tài liệu tham khảo

Johansson, 2013, The gastrointestinal mucus system in health and disease, Nat Rev Gastroenterol Hepatol, 10, 352, 10.1038/nrgastro.2013.35 Sharpe, 2018, A sticky end for gastrointestinal helminths; the role of the mucus barrier, Parasite Immunol, 40, 10.1111/pim.12517 Munck, 2014, Cystic fibrosis: evidence for gut inflammation, Int J Biochem Cell Biol, 52, 180, 10.1016/j.biocel.2014.02.005 Thornton, 2008, Structure and function of the polymeric mucins in airways mucus, Annu Rev Physiol, 70, 459, 10.1146/annurev.physiol.70.113006.100702 Johansson, 2008, The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria, Proc Natl Acad Sci U S A, 105, 15064, 10.1073/pnas.0803124105 Ambort, 2012, Calcium and pH-dependent packing and release of the gel-forming MUC2 mucin, Proc Natl Acad Sci U S A, 109, 5645, 10.1073/pnas.1120269109 Birchenough, 2016, A sentinel goblet cell guards the colonic crypt by triggering Nlrp6-dependent Muc2 secretion, Science, 352, 1535, 10.1126/science.aaf7419 Johansson, 2010, Bacteria penetrate the inner mucus layer before inflammation in the dextran sulfate colitis model, PLoS ONE, 5, 10.1371/journal.pone.0012238 Johansson, 2014, Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis, Gut, 63, 281, 10.1136/gutjnl-2012-303207 Johansson, 2015, Normalization of host intestinal mucus layers requires long-term microbial colonization, Cell Host Microbe, 18, 582, 10.1016/j.chom.2015.10.007 Schutte, 2014, Microbial-induced meprin beta cleavage in MUC2 mucin and a functional CFTR channel are required to release anchored small intestinal mucus, Proc Natl Acad Sci U S A, 111, 12396, 10.1073/pnas.1407597111 Gustafsson, 2012, Bicarbonate and functional CFTR channel are required for proper mucin secretion and link cystic fibrosis with its mucus phenotype, J Exp Med, 209, 1263, 10.1084/jem.20120562 Erickson, 2015, The goblet cell protein Clca1 (alias mClca3 or Gob-5) is not required for intestinal mucus synthesis, structure and barrier function in naive or DSS-challenged mice, PLoS ONE, 10, 10.1371/journal.pone.0131991 Rodriguez-Pineiro, 2013, Studies of mucus in mouse stomach, small intestine, and colon. II. Gastrointestinal mucus proteome reveals Muc2 and Muc5ac accompanied by a set of core proteins, Am J Physiol Gastrointest Liver Physiol, 305, G348, 10.1152/ajpgi.00047.2013 Agnel, 1999, Identification of three novel members of the calcium-dependent chloride channel (CaCC) family predominantly expressed in the digestive tract and trachea, FEBS Lett, 455, 295, 10.1016/S0014-5793(99)00891-1 Gruber, 1998, Genomic cloning, molecular characterization, and functional analysis of human CLCA1, the first human member of the family of Ca2+−activated cl- channel proteins, Genomics, 54, 200, 10.1006/geno.1998.5562 Sala-Rabanal, 2015, Secreted CLCA1 modulates TMEM16A to activate Ca-dependent chloride currents in human cells, Elife, 4, 10.7554/eLife.05875 Yurtsever, 2012, Self-cleavage of human CLCA1 protein by a novel internal metalloprotease domain controls calcium-activated chloride channel activation, J Biol Chem, 287, 42138, 10.1074/jbc.M112.410282 Hamann, 2009, Human ClCa1 modulates anionic conduction of calcium-dependent chloride currents, J Physiol, 587, 2255, 10.1113/jphysiol.2009.170159 Mundhenk, 2006, Both cleavage products of the mCLCA3 protein are secreted soluble proteins, J Biol Chem, 281, 30072, 10.1074/jbc.M606489200 Bothe, 2011, The murine goblet cell protein mCLCA3 is a zinc-dependent metalloprotease with autoproteolytic activity, Mol Cells, 32, 535, 10.1007/s10059-011-0158-8 Pawlowski, 2006, Novel conserved hydrolase domain in the CLCA family of alleged calcium-activated chloride channels, Proteins, 63, 424, 10.1002/prot.20887 Patel, 2009, The role of CLCA proteins in inflammatory airway disease, Annu Rev Physiol, 71, 425, 10.1146/annurev.physiol.010908.163253 Patel, 2006, Genetic segregation of airway disease traits despite redundancy of calcium-activated chloride channel family members, Physiol Genomics, 25, 502, 10.1152/physiolgenomics.00321.2005 Mundhenk, 2012, mCLCA3 does not contribute to calcium-activated chloride conductance in murine airways, Am J Respir Cell Mol Biol, 47, 87, 10.1165/rcmb.2010-0508OC Gustafsson, 2012, An ex vivo method for studying mucus formation, properties, and thickness in human colonic biopsies and mouse small and large intestinal explants, Am J Physiol Gastrointest Liver Physiol, 302, G430, 10.1152/ajpgi.00405.2011 Gustafsson, 2015, Carbachol-induced colonic mucus formation requires transport via NKCC1, K(+) channels and CFTR, Pflugers Arch, 467, 1403, 10.1007/s00424-014-1595-y Vizcaino, 2014, ProteomeXchange provides globally coordinated proteomics data submission and dissemination, Nat Biotechnol, 32, 223, 10.1038/nbt.2839 Wisniewski, 2009, Universal sample preparation method for proteome analysis, Nat Methods, 6, 359, 10.1038/nmeth.1322 van der Post, 2014, Membrane protein profiling of human colon reveals distinct regional differences, Mol Cell Proteomics, 13, 2277, 10.1074/mcp.M114.040204 Cox, 2008, MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification, Nat Biotechnol, 26, 1367, 10.1038/nbt.1511 Cox, 2011, Andromeda: a peptide search engine integrated into the MaxQuant environment, J Proteome Res, 10, 1794, 10.1021/pr101065j Bergstrom, 2016, Gram-positive bacteria are held at a distance in the colon mucus by the lectin-like protein ZG16, Proc Natl Acad Sci U S A, 113, 13833, 10.1073/pnas.1611400113 Loewen, 2002, pCLCA1 becomes a cAMP-dependent chloride conductance mediator in Caco-2 cells, Biochem Biophys Res Commun, 298, 531, 10.1016/S0006-291X(02)02498-1 Ambort, 2012, Perspectives on mucus properties and formation—lessons from the biochemical world, Cold Spring Harb Perspect Med, 2, 10.1101/cshperspect.a014159 Liu, 2015, Characterization of the effects of cl(−) channel modulators on TMEM16A and bestrophin-1 ca(2)(+) activated cl(−) channels, Pflugers Arch, 467, 1417, 10.1007/s00424-014-1572-5 Gandhi, 1998, Molecular and functional characterization of a calcium-sensitive chloride channel from mouse lung, J Biol Chem, 273, 32096, 10.1074/jbc.273.48.32096 Sala-Rabanal, 2017, Modulation of TMEM16A channel activity by the von Willebrand factor type a (VWA) domain of the calcium-activated chloride channel regulator 1 (CLCA1), J Biol Chem, 292, 9164, 10.1074/jbc.M117.788232 Leverkoehne, 2002, The murine mCLCA3 (alias gob-5) protein is located in the mucin granule membranes of intestinal, respiratory, and uterine goblet cells, J Histochem Cytochem, 50, 829, 10.1177/002215540205000609 Johansson, 2011, The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host–microbial interactions, Proc Natl Acad Sci U S A, 108, 4659, 10.1073/pnas.1006451107 Behera, 2015, Exploring the role and diversity of mucins in health and disease with special insight into non-communicable diseases, Glycoconj J, 32, 575, 10.1007/s10719-015-9606-6 Young, 2007, Amelioration of cystic fibrosis intestinal mucous disease in mice by restoration of mCLCA3, Gastroenterology, 133, 1928, 10.1053/j.gastro.2007.10.007 van der Doef, 2010, Association of the CLCA1 p.S357N variant with meconium ileus in European patients with cystic fibrosis, J Pediatr Gastroenterol Nutr, 50, 347, 10.1097/MPG.0b013e3181afce6c Knight, 2008, Innate immune response mechanisms in the intestinal epithelium: potential roles for mast cells and goblet cells in the expulsion of adult Trichinella spiralis, Parasitology, 135, 655, 10.1017/S0031182008004319 Datta, 2005, Identification of novel genes in intestinal tissue that are regulated after infection with an intestinal nematode parasite, Infect Immun, 73, 4025, 10.1128/IAI.73.7.4025-4033.2005 Gossner, 2013, Exploring the abomasal lymph node transcriptome for genes associated with resistance to the sheep nematode Teladorsagia circumcincta, Vet Res, 44, 68, 10.1186/1297-9716-44-68 Alevy, 2012, IL-13-induced airway mucus production is attenuated by MAPK13 inhibition, J Clin Invest, 122, 4555, 10.1172/JCI64896 Robichaud, 2005, Gob-5 is not essential for mucus overproduction in preclinical murine models of allergic asthma, Am J Respir Cell Mol Biol, 33, 303, 10.1165/rcmb.2004-0372OC Nakanishi, 2001, Role of gob-5 in mucus overproduction and airway hyperresponsiveness in asthma, Proc Natl Acad Sci U S A, 98, 5175, 10.1073/pnas.081510898 Thai, 2005, Differential regulation of MUC5AC/Muc5ac and hCLCA-1/mGob-5 expression in airway epithelium, Am J Respir Cell Mol Biol, 33, 523, 10.1165/rcmb.2004-0220RC