Calcium-activated chloride channel regulator 1 (CLCA1): More than a regulator of chloride transport and mucus production

Cunningham, 1995, Cloning of an epithelial chloride channel from bovine trachea, J Biol Chem, 270, 31016, 10.1074/jbc.270.52.31016 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 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 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 Sala-Rabanal, 2015, Secreted CLCA1 modulates TMEM16A to activate Ca(2+)-dependent chloride currents in human cells, Elife, 4, 10.7554/eLife.05875 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 Zhu, 1991, Mediation of lung metastasis of murine melanomas by a lung-specific endothelial cell adhesion molecule, Proc Natl Acad Sci U S A, 88, 9568, 10.1073/pnas.88.21.9568 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 Gruber, 1998, The murine calcium-sensitive chloride channel (mCaCC) is widely expressed in secretory epithelia and in other select tissues, Histochem Cell Biol, 110, 43, 10.1007/s004180050263 Gaspar, 2000, Cloning a chloride conductance mediator from the apical membrane of porcine ileal enterocytes, Physiol Genom, 3, 101, 10.1152/physiolgenomics.2000.3.2.101 Loewen, 2002, The calcium-dependent chloride conductance mediator pCLCA1, Am J Physiol Cell Physiol, 283, 10.1152/ajpcell.00477.2001 Anton, 2005, Overexpression of eCLCA1 in small airways of horses with recurrent airway obstruction, J Histochem Cytochem, 53, 1011, 10.1369/jhc.4A6599.2005 Jeong, 2005, Cloning and expression of Ca2+-activated chloride channel from rat brain, Biochem Biophys Res Commun, 334, 569, 10.1016/j.bbrc.2005.06.122 Pauli, 2000, Molecular characteristics and functional diversity of CLCA family members, Clin Exp Pharmacol Physiol, 27, 901, 10.1046/j.1440-1681.2000.03358.x 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 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 Leverkoehne, 2000, Assignment of the murine calcium-activated chloride channel genes Clca1 and Clca3 (alias gob-5) to chromosome 3 band H2-H3 using somatic cell hybrids, Cytogenet Cell Genet, 88, 208, 10.1159/000015550 Winpenny, 2009, The CLCA gene family: putative therapeutic target for respiratory diseases, Inflamm Allergy - Drug Targets, 8, 146, 10.2174/187152809788462590 Loewen, 2005, Structure and function of CLCA proteins, Physiol Rev, 85, 1061, 10.1152/physrev.00016.2004 Loewen, 2004, pCLCA1 lacks inherent chloride channel activity in an epithelial colon carcinoma cell line, Am J Physiol Gastrointest Liver Physiol, 287, 10.1152/ajpgi.00023.2004 Mundhenk, 2006, Both cleavage products of the mCLCA3 protein are secreted soluble proteins, J Biol Chem, 281, 30072, 10.1074/jbc.M606489200 Hamann, 2009, Human ClCa1 modulates anionic conduction of calcium-dependent chloride currents, J Physiol, 587, 2255, 10.1113/jphysiol.2009.170159 Gibson, 2005, hCLCA1 and mCLCA3 are secreted non-integral membrane proteins and therefore are not ion channels, J Biol Chem, 280, 27205, 10.1074/jbc.M504654200 Greenwood, 2002, The large conductance potassium channel beta-subunit can interact with and modulate the functional properties of a calcium-activated chloride channel, CLCA1, J Biol Chem, 277, 22119, 10.1074/jbc.C200215200 Caputo, 2008, TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity, Science, 322, 590, 10.1126/science.1163518 Schroeder, 2008, Expression cloning of TMEM16A as a calcium-activated chloride channel subunit, Cell, 134, 1019, 10.1016/j.cell.2008.09.003 Yang, 2008, TMEM16A confers receptor-activated calcium-dependent chloride conductance, Nature, 455, 1210, 10.1038/nature07313 Kamada, 2004, Association of the hCLCA1 gene with childhood and adult asthma, Genes Immun, 5, 540, 10.1038/sj.gene.6364124 Hegab, 2004, CLCA1 gene polymorphisms in chronic obstructive pulmonary disease, J Med Genet, 41, 10.1136/jmg.2003.012484 Ching, 2013, Secreted hCLCA1 is a signaling molecule that activates airway macrophages, PLoS One, 8, 10.1371/journal.pone.0083130 Groneberg, 2002, Expression of respiratory mucins in fatal status asthmaticus and mild asthma, Histopathology, 40, 367, 10.1046/j.1365-2559.2002.01378.x Fang, 2017, Identification of potential transcriptomic markers in developing asthma: an integrative analysis of gene expression profiles, Mol Immunol, 92, 38, 10.1016/j.molimm.2017.09.021 Singhania, 2018, Multitissue transcriptomics delineates the diversity of airway T cell functions in asthma, Am J Respir Cell Mol Biol, 58, 261, 10.1165/rcmb.2017-0162OC Poole, 2014, Dissecting childhood asthma with nasal transcriptomics distinguishes subphenotypes of disease, J Allergy Clin Immunol, 133, 670, 10.1016/j.jaci.2013.11.025 Zhou, 2001, Characterization of a calcium-activated chloride channel as a shared target of Th2 cytokine pathways and its potential involvement in asthma, Am J Respir Cell Mol Biol, 25, 486, 10.1165/ajrcmb.25.4.4578 Louten, 2012, Biomarkers of disease and treatment in murine and cynomolgus models of chronic asthma, Biomark Insights, 7, 87, 10.4137/BMI.S9776 Meldrum, 2018, Cerium dioxide nanoparticles exacerbate house dust mite induced type II airway inflammation, Part Fibre Toxicol, 15, 24, 10.1186/s12989-018-0261-5 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 Long, 2006, Gob-5 contributes to goblet cell hyperplasia and modulates pulmonary tissue inflammation, Am J Respir Cell Mol Biol, 35, 357, 10.1165/rcmb.2005-0451OC Hovenberg, 1996, Different mucins are produced by the surface epithelium and the submucosa in human trachea: identification of MUC5AC as a major mucin from the goblet cells, Biochem J, 318, 319, 10.1042/bj3180319 Song, 2013, Antibody to mCLCA3 suppresses symptoms in a mouse model of asthma, PLoS One, 8, 10.1371/journal.pone.0082367 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 Iwashita, 2012, Increased human Ca(2)(+)-activated Cl(-) channel 1 expression and mucus overproduction in airway epithelia of smokers and chronic obstructive pulmonary disease patients, Respir Res, 13, 55, 10.1186/1465-9921-13-55 Alevy, 2012, IL-13-induced airway mucus production is attenuated by MAPK13 inhibition, J Clin Investig, 122, 4555, 10.1172/JCI64896 Kerem, 1989, Identification of the cystic fibrosis gene: genetic analysis, Science, 245, 1073, 10.1126/science.2570460 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 Gray, 1994, CFTR and calcium-activated chloride currents in pancreatic duct cells of a transgenic CF mouse, Am J Physiol, 266 Rozmahel, 1996, Modulation of disease severity in cystic fibrosis transmembrane conductance regulator deficient mice by a secondary genetic factor, Nat Genet, 12, 280, 10.1038/ng0396-280 Hauber, 2003, Increased expression of interleukin-9, interleukin-9 receptor, and the calcium-activated chloride channel hCLCA1 in the upper airways of patients with cystic fibrosis, The Laryngoscope, 113, 1037, 10.1097/00005537-200306000-00022 Hauber, 2004, Expression of HCLCA1 in cystic fibrosis lungs is associated with mucus overproduction, Eur Respir J, 23, 846, 10.1183/09031936.04.00096504 Hauber, 2010, Effect of Th2 type cytokines on hCLCA1 and mucus expression in cystic fibrosis airways, J Cyst Fibros, 9, 277, 10.1016/j.jcf.2010.05.002 Plog, 2009, Genomic, tissue expression, and protein characterization of pCLCA1, a putative modulator of cystic fibrosis in the pig, J Histochem Cytochem, 57, 1169, 10.1369/jhc.2009.954594 Braun, 2010, Quantitative expression analyses of candidates for alternative anion conductance in cystic fibrosis mouse models, J Cyst Fibros, 9, 351, 10.1016/j.jcf.2010.06.003 Dietert, 2014, mCLCA3 modulates IL-17 and CXCL-1 induction and leukocyte recruitment in murine Staphylococcus aureus pneumonia, PLoS One, 9, 10.1371/journal.pone.0102606 Britto, 2015, Bactericidal/Permeability-increasing protein fold-containing family member A1 in airway host protection and respiratory disease, Am J Respir Cell Mol Biol, 52, 525, 10.1165/rcmb.2014-0297RT Erickson, 2018, Soluble mucus component CLCA1 modulates expression of leukotactic cytokines and BPIFA1 in murine alveolar macrophages but not in bone marrow-derived macrophages, Histochem Cell Biol, 149, 619, 10.1007/s00418-018-1664-y Kuperman, 2002, Direct effects of interleukin-13 on epithelial cells cause airway hyperreactivity and mucus overproduction in asthma, Nat Med, 8, 885, 10.1038/nm734 Yu, 2010, Interleukin-13 induces mucin 5AC production involving STAT6/SPDEF in human airway epithelial cells, Cell Commun Adhes, 17, 83, 10.3109/15419061.2010.551682 Hegab, 2007, Niflumic acid and AG-1478 reduce cigarette smoke-induced mucin synthesis: the role of hCLCA1, Chest, 131, 1149, 10.1378/chest.06-2031 Mertens, 2017, Cigarette smoke differentially affects IL-13-induced gene expression in human airway epithelial cells, Phys Rep, 5 Hauber, 2005, Niflumic acid and MSI-2216 reduce TNF-alpha-induced mucin expression in human airway mucosa, J Allergy Clin Immunol, 115, 266, 10.1016/j.jaci.2004.09.039 Bustin, 2001, Expression of the Ca2+-activated chloride channel genes CLCA1 and CLCA2 is downregulated in human colorectal cancer, DNA Cell Biol, 20, 331, 10.1089/10445490152122442 Yang, 2013, The transition from proliferation to differentiation in colorectal cancer is regulated by the calcium activated chloride channel A1, PLoS One, 8, 10.1371/journal.pone.0060861 Yang, 2015, Low expression of chloride channel accessory 1 predicts a poor prognosis in colorectal cancer, Cancer, 121, 1570, 10.1002/cncr.29235 Elble, 2001, Tumor suppression by a proapoptotic calcium-activated chloride channel in mammary epithelium, J Biol Chem, 276, 40510, 10.1074/jbc.M104821200 Hu, 2018, Calcium-activated chloride channel regulator 1 as a prognostic biomarker in pancreatic ductal adenocarcinoma, BMC Canc, 18, 1096, 10.1186/s12885-018-5013-2 Ostasiewicz, 2016, Quantitative analysis of gene expression in fixed colorectal carcinoma samples as a method for biomarker validation, Mol Med Rep, 13, 5084, 10.3892/mmr.2016.5200 Musrap, 2015, Comparative proteomics of ovarian cancer aggregate formation reveals an increased expression of calcium-activated chloride channel regulator 1 (CLCA1), J Biol Chem, 290, 17218, 10.1074/jbc.M115.639773 Iwanicki, 2011, Ovarian cancer spheroids use myosin-generated force to clear the mesothelium, Cancer Discov, 1, 144, 10.1158/2159-8274.CD-11-0010 Yu, 2016, High-throughput proteomics integrated with gene microarray for discovery of colorectal cancer potential biomarkers, Oncotarget, 7, 75279, 10.18632/oncotarget.12143 Li, 2017, CLCA1 suppresses colorectal cancer aggressiveness via inhibition of the Wnt/beta-catenin signaling pathway, Cell Commun Signal, 15, 38, 10.1186/s12964-017-0192-z Chen, 2018, High chloride channel accessory 1 expression predicts poor prognoses in patients with rectal cancer receiving chemoradiotherapy, Int J Med Sci, 15, 1171, 10.7150/ijms.26685 Cimino, 1997, Beta 4 integrin subunit expression is downregulated in low metastatic carcinoma variants, Cancer Detect Prev, 21, 158 Abdel-Ghany, 2003, The interacting binding domains of the beta(4) integrin and calcium-activated chloride channels (CLCAs) in metastasis, J Biol Chem, 278, 49406, 10.1074/jbc.M309086200 Abdel-Ghany, 2002, Focal adhesion kinase activated by beta(4) integrin ligation to mCLCA1 mediates early metastatic growth, J Biol Chem, 277, 34391, 10.1074/jbc.M205307200 Nystrom, 2018, Calcium-activated chloride channel regulator 1 (CLCA1) controls mucus expansion in colon by proteolytic activity, EBioMedicine, 33, 134, 10.1016/j.ebiom.2018.05.031 Pelaseyed, 2014, The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system, Immunol Rev, 260, 8, 10.1111/imr.12182 Roussa, 2010, Cellular distribution and subcellular localization of mCLCA1/2 in murine gastrointestinal epithelia, J Histochem Cytochem, 58, 653, 10.1369/jhc.2010.955211 Erickson, 2016, Role of goblet cell protein CLCA1 in murine DSS colitis, J Inflamm, 13, 5 Ritzka, 2004, The CLCA gene locus as a modulator of the gastrointestinal basic defect in cystic fibrosis, Hum Genet, 115, 483, 10.1007/s00439-004-1190-y Brouillard, 2005, Blue native/SDS-PAGE analysis reveals reduced expression of the mClCA3 protein in cystic fibrosis knock-out mice, Mol Cell Proteom, 4, 1762, 10.1074/mcp.M500098-MCP200 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 Zhou, 1994, Correction of lethal intestinal defect in a mouse model of cystic fibrosis by human CFTR, Science, 266, 1705, 10.1126/science.7527588 Dotti, 2017, Alterations in the epithelial stem cell compartment could contribute to permanent changes in the mucosa of patients with ulcerative colitis, Gut, 66, 2069, 10.1136/gutjnl-2016-312609 Strugala, 2008, Thickness and continuity of the adherent colonic mucus barrier in active and quiescent ulcerative colitis and Crohn's disease, Int J Clin Pract, 62, 762, 10.1111/j.1742-1241.2007.01665.x Vannella, 2016, Acidic chitinase primes the protective immune response to gastrointestinal nematodes, Nat Immunol, 17, 538, 10.1038/ni.3417 Knight, 2011, Novel gene expression responses in the ovine abomasal mucosa to infection with the gastric nematode Teladorsagia circumcincta, Vet Res, 42, 78, 10.1186/1297-9716-42-78 Shrestha, 2010, B cell-derived vascular endothelial growth factor A promotes lymphangiogenesis and high endothelial venule expansion in lymph nodes, J Immunol, 184, 4819, 10.4049/jimmunol.0903063 Jordan-Williams, 2016, The lymphatic endothelial mCLCA1 antibody induces proliferation and growth of lymph node lymphatic sinuses, PLoS One, 11, 10.1371/journal.pone.0156079 Furuya, 2010, Lymphatic endothelial murine chloride channel calcium-activated 1 is a ligand for leukocyte LFA-1 and Mac-1, J Immunol, 185, 5769, 10.4049/jimmunol.1002226