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REVIEW

Airway regeneration: the role of the Clara cell secretory protein and the cells that express it

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Pages 676-687 | Published online: 02 Nov 2009

References

  • Boers JE, Ambergen AW, Thunnissen FB, . Number and proliferation of basal and parabasal cells in normal human airway epithelium. Am J Respir Crit Care Med 1998;157:2000–6.
  • Boers JE, Ambergen AW, Thunnissen FB, . Number and proliferation of clara cells in normal human airway epithelium. Am J Respir Crit Care Med 1999;159:1585–91.
  • Stripp BR, Reynolds SD, Boe IM, Lund J, Power JH, Coppens JT, . Clara cell secretory protein deficiency alters clara cell secretory apparatus and the protein composition of airway lining fluid. Am J Respir Cell Mol Biol 2002;27:170–8.
  • Stripp BR, Reynolds SD, Plopper CG, Boe IM, Lund J, . Pulmonary phenotype of CCSP/UG deficient mice: a consequence of CCSP deficiency or altered Clara cell function?. Ann NY Acad Sci 2000;923:202–9.
  • Stripp BR, Lund J, Mango GW, Doyen KC, Johnston C, Hultenby K, . Clara cell secretory protein: a determinant of PCB bioaccumulation in mammals. Am J Physiol 1996;271:L659–64.
  • Giangreco A, Reynolds SD, Stripp BR, . Terminal bronchioles harbor a unique airway stem cell population that localizes to the bronchoalveolar duct junction. Am J Pathol 2002;161:173–82.
  • Hong KU, Reynolds SD, Giangreco A, Hurley CM, Stripp BR, . Clara cell secretory protein-expressing cells of the airway neuroepithelial body microenvironment include a label-retaining subset and are critical for epithelial renewal after progenitor cell depletion. Am J Respir Cell Mol Biol 2001;24:671–81.
  • Vogel LK, Suske G, Beato M, Noren O, Sjostrom H, . Uteroglobin, an apically secreted protein of the uterine epithelium, is secreted non-polarized from MDCK cells and mainly basolaterally from Caco-2 cells. FEBS Lett 1993;330:293–6.
  • Bochskanl R, Thie M, Wirth B, Kirchner C, . Uteroglobin as progesterone-binding protein in the preimplantation uterine epithelium of the rabbit: histochemical studies. Cell Tissue Res 1988;252:625–30.
  • Kim YS, Kang D, Kwon DY, Park WY, Kim H, Lee DS, . Uteroglobin gene polymorphisms affect the progression of immunoglobulin A nephropathy by modulating the level of uteroglobin expression. Pharmacogenetics 2001;11:299–305.
  • Burmeister R, Boe IM, Nykjaer A, Jacobsen C, Moestrup SK, Verroust P, . A two-receptor pathway for catabolism of Clara cell secretory protein in the kidney. J Biol Chem 2001;276:13295–301.
  • Boers JE, Ambergen AW, Thunnissen FB, . Number and proliferation of clara cells in normal human airway epithelium. Am J Respir Crit Care Med 1999;159:1585–91.
  • Stripp BR, . Hierarchical organization of lung progenitor cells: is there an adult lung tissue stem cell? Proc Am Thorac Soc 2008;5:695–8.
  • Evans MJ, Johnson LV, Stephens RJ, Freeman G, . Renewal of the terminal bronchiolar epithelium in the rat following exposure to NO2 or O3. Lab Invest 1976;35:246–57.
  • Rawlins EL, Hogan BL, . Epithelial stem cells of the lung: privileged few or opportunities for many? Development 2006;133:2455–65.
  • Ling TY, Kuo MD, Li CL, Yu AL, Huang YH, Wu TJ, . Identification of pulmonary Oct-4+stem/progenitor cells and demonstration of their susceptibility to SARS coronavirus (SARS-CoV) infection in vitro. Proc Natl Acad Sci USA 2006;103:9530–5.
  • Kim CF, Jackson EL, Woolfenden AE, Lawrence S, Babar I, Vogel S, . Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 2005;121:823–35.
  • Hong KU, Reynolds SD, Giangreco A, Hurley CM, Stripp BR, . Clara cell secretory protein-expressing cells of the airway neuroepithelial body microenvironment include a label-retaining subset and are critical for epithelial renewal after progenitor cell depletion. Am J Respir Cell Mol Biol 2001;24:671–81.
  • Stripp BR, Maxson K, Mera R, Singh G, . Plasticity of airway cell proliferation and gene expression after acute naphthalene injury. Am J Physiol 1995;269:L791–9.
  • Giangreco A, Reynolds SD, Stripp BR, . Terminal bronchioles harbor a unique airway stem cell population that localizes to the bronchoalveolar duct junction. Am J Pathol 2002;161:173–82.
  • Rawlins EL, Okubo T, Xue Y, Brass DM, Auten RL, Hasegawa H, . The role of Scgb1a1+ Clara cells in the long-term maintenance and repair of lung airway, but not alveolar, epithelium. Cell Stem Cell 2009;4:525–34.
  • Nolen-Walston RD, Kim CF, Mazan MR, Ingenito EP, Gruntman AM, Tsai L, . Cellular kinetics and modeling of bronchioalveolar stem cell response during lung regeneration. Am J Physiol Lung Cell Mol Physiol 2008;294:L1158–65.
  • Yang Y, Iwanaga K, Raso MG, Wislez M, Hanna AE, Wieder ED, . Phosphatidylinositol 3-kinase mediates bronchioalveolar stem cell expansion in mouse models of oncogenic K-ras-induced lung cancer. PLOS One 2008;3:e2220.
  • Yanagi S, Kishimoto H, Kawahara K, Sasaki T, Sasaki M, Nishio M, . Pten controls lung morphogenesis, bronchioalveolar stem cells, and onset of lung adenocarcinomas in mice. J Clin Invest 2007;117:2929–40.
  • Zhang Y, Goss AM, Cohen ED, Kadzik R, Lepore JJ, Muthukumaraswamy K, . A Gata6-Wnt pathway required for epithelial stem cell development and airway regeneration. Nat Genet 2008;40:862–70.
  • Teisanu RM, Lagasse E, Whitesides JF, Stripp BR, . Prospective isolation of bronchiolar stem cells based upon immunophenotypic and autofluorescence characteristics. Stem Cells 2009;27:612–22.
  • McQualter JL, Brouard N, Williams B, Baird BN, Sims-Lucas S, Yuen K, . Endogenous fibroblastic progenitor cells in the adult mouse lung are highly enriched in the sca-1 positive cell fraction. Stem Cells 2009;27:623–33.
  • Giangreco A, Arwert EN, Rosewell IR, Snyder J, Watt FM, Stripp BR, . Stem cells are dispensable for lung homeostasis but restore airways after injury. Proc Natl Acad Sci USA 2009;106:9286–91.
  • Zhang Z, Zimonjic DB, Popescu NC, Wang N, Gerhard DS, Stone EM, . Human uteroglobin gene: structure, subchromosomal localization, and polymorphism. DNA Cell Biol 1997;16:73–83.
  • Wolf M, Klug J, Hackenberg R, Gessler M, Grzeschik KH, Beato M, . Human CC10, the homologue of rabbit uteroglobin: genomic cloning, chromosomal localization and expression in endometrial cell lines. Hum Mol Genet 1992;1:371–8.
  • Cassel TN, Berg T, Suske G, Nord M, . Synergistic transactivation of the differentiation-dependent lung gene Clara cell secretory protein (secretoglobin 1a1) by the basic region leucine zipper factor CCAAT/enhancer-binding protein alpha and the homeodomain factor Nkx2.1/thyroid transcription factor-1. J Biol Chem 20002;277:36970–71.
  • Nord M, Cassel TN, Braun H, Suske G, . Regulation of the Clara cell secretory protein/uteroglobin promoter in lung. Ann NY Acad Sci 2000;923:154–65.
  • Cassel TN, Suske G, Nord M, . C/EBP alpha and TTF-1 synergistically transactivate the Clara cell secretory protein gene. Ann NY Acad Sci 2000;923:300–2.
  • Harrod KS, Mounday AD, Stripp BR, Whitsett JA, . Clara cell secretory protein decreases lung inflammation after acute virus infection. Am J Physiol 1998;275:L924–30.
  • Hayashida S, Harrod KS, Whitsett JA, . Regulation and function of CCSP during pulmonary Pseudomonas aeruginosa infection in vivo. Am J Physiol Lung Cell Mol Physiol 2000;279:L452–9.
  • Yoshikawa S, Miyahara T, Reynolds SD, Stripp BR, Anghelescu M, Eyal FG, . Clara cell secretory protein and phospholipase A2 activity modulate acute ventilator-induced lung injury in mice. J Appl Physiol 2005;98:1264–71.
  • Dierynck I, Bernard A, Roels H, De Ley M, . The human Clara cell protein: biochemical and biological characterisation of a natural immunosuppressor. Mult Scler 1996;1:385–7.
  • Wang SZ, Rosenberger CL, Bao YX, Stark JM, Harrod KS, . Clara cell secretory protein modulates lung inflammatory and immune responses to respiratory syncytial virus infection. J Immunol 2003;171:1051–60.
  • Pilon AL, . Rationale for the development of recombinant human CC10 as a therapeutic for inflammatory and fibrotic disease. Ann NY Acad Sci 2000;923:280–99.
  • Stripp BR, Lund J, Mango GW, Doyen KC, Johnston C, Hultenby K, . Clara cell secretory protein: a determinant of PCB bioaccumulation in mammals. Am J Physiol 1996;271:L656–64.
  • Peri A, Cowan BD, Bhartiya D, Miele L, Nieman LK, Nwaeze IO, . Expression of Clara cell 10-kD gene in the human endometrium and its relationship to ovarian menstrual cycle. DNA Cell Biol 1994;13:495–503.
  • Peri A, Cordella-Miele E, Miele L, Mukherjee AB, . Tissue-specific expression of the gene coding for human Clara cell 10-kD protein, a phospholipase A2-inhibitory protein. J Clin Invest 1993;92:2099–109.
  • Rauch M, Loosfelt H, Philibert D, Milgrom E, . Mechanism of action of an antiprogesterone, RU486, in the rabbit endometrium. Effects of RU486 on the progesterone receptor and on the expression of the uteroglobin gene. Eur J Biochem 1985;148:213–8.
  • Johnston CJ, Mango GW, Finkelstein JN, Stripp BR, . Altered pulmonary response to hyperoxia in Clara cell secretory protein deficient mice. Am J Respir Cell Mol Biol 1997;17:147–55.
  • Johnston CJ, Finkelstein JN, Oberdorster G, Reynolds SD, Stripp BR, . Clara cell secretory protein-deficient mice differ from wild-type mice in inflammatory chemokine expression to oxygen and ozone, but not to endotoxin. Exp Lung Res 1999;25:7–21.
  • Mango GW, Johnston CJ, Reynolds SD, Finkelstein JN, Plopper CG, Stripp BR, . Clara cell secretory protein deficiency increases oxidant stress response in conducting airways. Am J Physiol 1998;275:L348–56.
  • Watson TM, Reynolds SD, Mango GW, Boe IM, Lund J, Stripp BR, . Altered lung gene expression in CCSP-null mice suggests immunoregulatory roles for Clara cells. Am J Physiol Lung Cell Mol Physiol 2001;281:L1523–30.
  • Reynolds SD, Reynolds PR, Pryhuber GS, Finder JD, Stripp BR, . Secretoglobins SCGB3A1 and SCGB3A2 define secretory cell subsets in mouse and human airways. Am J Respir Crit Care Med 2002;166:1498–509.
  • Wang SZ, Rosenberger CL, Espindola TM, Barrett EG, Tesfaigzi Y, Bice DE, . CCSP modulates airway dysfunction and host responses in an Ova-challenged mouse model. Am J Physiol Lung Cell Mol Physiol 2001;281:L1303–11.
  • Reynolds SD, Reynolds PR, Snyder JC, Whyte F, Paavola KJ, Stripp BR, . CCSP regulates cross talk between secretory cells and both ciliated cells and macrophages of the conducting airway. Am J Physiol Lung Cell Mol Physiol 2007;293:L114–23.
  • Zhang Z, Kundu GC, Yuan CJ, Ward JM, Lee EJ, DeMayo F, . Severe fibronectin-deposit renal glomerular disease in mice lacking uteroglobin. Science 1997;276:1408–12.
  • Kundu GC, Zhang Z, Mantile-Selvaggi G, Mandal A, Yuan CJ, Mukherjee AB, . Uteroglobin binding proteins: regulation of cellular motility and invasion in normal and cancer cells. Ann NY Acad Sci 2000;923:234–48.
  • Zhang Z, Kim SJ, Chowdhury B, Wang J, Lee YC, Tsai PC, . Interaction of uteroglobin with lipocalin-1 receptor suppresses cancer cell motility and invasion. Gene 2006;369:66–71.
  • Yang Y, Zhang Z, Mukherjee AB, Linnoila RI, . Increased susceptibility of mice lacking Clara cell 10-kDa protein to lung tumorigenesis by 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone, a potent carcinogen in cigarette smoke. J Biol Chem 2004;279:29336–40.
  • Chen J, Lam S, Pilon A, McWilliams A, Macaulay C, Szabo E, . Higher levels of the anti-inflammatory protein CC10 are associated with improvement in bronchial dysplasia and sputum cytometric assessment in individuals at high risk for lung cancer. Clin Cancer Res 2008;14:1590–7.
  • Broeckaert F, Clippe A, Knoops B, Hermans C, Bernard A, . Clara cell secretory protein (CC16): features as a peripheral lung biomarker. Ann NY Acad Sci 2000;923:68–77.
  • Broeckaert F, Arsalane K, Hermans C, Bergamaschi E, Brustolin A, Mutti A, . Serum clara cell protein: a sensitive biomarker of increased lung epithelium permeability caused by ambient ozone. Environ Health Perspect 2000;108:533–7.
  • Blomberg A, Mudway I, Svensson M, Hagenbjork-Gustafsson A, Thomasson L, Helleday R, . Clara cell protein as a biomarker for ozone-induced lung injury in humans. Eur Respir J 2003;22:883–8.
  • Helleday R, Segerstedt B, Forsberg B, Mudway I, Nordberg G, Bernard A, . Exploring the time dependence of serum clara cell protein as a biomarker of pulmonary injury in humans. Chest 2006;130:672–5.
  • Broeckaert F, Bernard A, . Clara cell secretory protein (CC16): characteristics and perspectives as lung peripheral biomarker. Clin Exp Allergy 2000;30:469–75.
  • Petrek M, Hermans C, Kolek V, Fialova J, Bernard A, . Clara cell protein (CC16) in serum and bronchoalveolar lavage fluid of subjects exposed to asbestos. Biomarkers 2002;7:58–67.
  • Broeckaert F, Clippe A, Wattiez R, Falmagne P, Bernard A, . Lung hyperpermeability, Clara-cell secretory protein (CC16), and susceptibility to ozone of five inbred strains of mice. Inhal Toxicol 2003;15:1209–30.
  • Bernard A, Hermans C, Van Houte G, . Transient increase of serum Clara cell protein (CC16) after exposure to smoke. Occup Environ Med 1997;54:63–5.
  • Bernard A, Van Houte G, . Increased Clara cell protein in serum of firefighters. Clin Chem 1996;42:1120.
  • Martin AC, Laing IA, Khoo SK, Zhang G, Rueter K, Teoh L, . Acute asthma in children: relationships among CD14 and CC16 genotypes, plasma levels, and severity. Am J Respir Crit Care Med 2006;173:617–22.
  • de Burbure C, Pignatti P, Corradi M, Malerba M, Clippe A, Dumont X, . Uteroglobin-related protein 1 and clara cell protein in induced sputum of patients with asthma and rhinitis. Chest 2007;131:172–9.
  • Sengler C, Heinzmann A, Jerkic SP, Haider A, Sommerfeld C, Niggemann B, . Clara cell protein 16 (CC16) gene polymorphism influences the degree of airway responsiveness in asthmatic children. J Allergy Clin Immunol 2003;111:515–9.
  • Laing IA, Hermans C, Bernard A, Burton PR, Goldblatt J, Le Souef PN, . Association between plasma CC16 levels, the A38G polymorphism, and asthma. Am J Respir Crit Care Med 2000;161:124–7.
  • Shijubo N, Itoh Y, Yamaguchi T, Imada A, Hirasawa M, Yamada T, . Clara cell protein-positive epithelial cells are reduced in small airways of asthmatics. Am J Respir Crit Care Med 1999;160:930–3.
  • Shijubo N, Itoh Y, Yamaguchi T, Sugaya F, Hirasawa M, Yamada T, . Serum levels of Clara cell 10-kDa protein are decreased in patients with asthma. Lung 1999;177:45–52.
  • Yang KD, Ou CY, Chang JC, Chen RF, Liu CA, Liang HM, . Infant frequent wheezing correlated to Clara cell protein 10 (CC10) polymorphism and concentration, but not allergy sensitization, in a perinatal cohort study. J Allergy Clin Immunol 2007;120:842–8.
  • Mattsson J, Remberger M, Andersson O, Sundberg B, Nord M, . Decreased serum levels of clara cell secretory protein (CC16) are associated with bronchiolitis obliterans and may permit early diagnosis in patients after allogeneic stem-cell transplantation. Transplantation 2005;79:1411–6.
  • Nord M, Schubert K, Cassel TN, Andersson O, Riise GC, . Decreased serum and bronchoalveolar lavage levels of Clara cell secretory protein (CC16) is associated with bronchiolitis obliterans syndrome and airway neutrophilia in lung transplant recipients. Transplantation 2002;73:1264–9.
  • Pilette C, Godding V, Kiss R, Delos M, Verbeken E, Decaestecker C, . Reduced epithelial expression of secretory component in small airways correlates with airflow obstruction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2001;163:185–94.
  • Bernard AM, Roels HA, Buchet JP, Lauwerys RR, . Serum Clara cell protein: an indicator of bronchial cell dysfunction caused by tobacco smoking. Environ Res 1994;66:96–104.
  • Robin M, Dong P, Hermans C, Bernard A, Bersten AD, Doyle IR, . Serum levels of CC16, SP-A and SP-B reflect tobacco-smoke exposure in asymptomatic subjects. Eur Respir J 2002;20:1152–61.
  • Macpherson H, Keir P, Webb S, Samuel K, Boyle S, Bickmore W, . Bone marrow-derived SP cells can contribute to the respiratory tract of mice in vivo. J Cell Sci 2005;118:2441–50.
  • Wong AP, Dutly AE, Sacher A, Lee H, Hwang DM, Liu M, . Targeted cell replacement with bone marrow cells for airway epithelial regeneration. Am J Physiol Lung Cell Mol Physiol 2007;293:L740–52.
  • Gomperts BN, Belperio JA, Rao PN, Randell SH, Fishbein MC, Burdick MD, . Circulating progenitor epithelial cells traffic via CXCR4/CXCL12 in response to airway injury. J Immunol 2006;176:1916–27.
  • Krause DS, Theise ND, Collector MI, Henegariu O, Hwang S, Gardner R, . Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 2001;105:369–77.
  • Rojas M, Xu J, Woods CR, Mora AL, Spears W, Roman J, . Bone marrow-derived mesenchymal stem cells in repair of the injured lung. Am J Respir Cell Mol Biol 2005;33:145–52.
  • Yamada M, Kubo H, Kobayashi S, Ishizawa K, Numasaki M, Ueda S, . Bone marrow-derived progenitor cells are important for lung repair after lipopolysaccharide-induced lung injury. J Immunol 2004;172:1266–72.
  • Ayach BB, Yoshimitsu M, Dawood F, Sun M, Arab S, Chen M, . Stem cell factor receptor induces progenitor and natural killer cell-mediated cardiac survival and repair after myocardial infarction. Proc Natl Acad Sci USA 2006;103:2304–9.
  • Fazel S, Cimini M, Chen L, Li S, Angoulvant D, Fedak P, . Cardioprotective c-kit+cells are from the bone marrow and regulate the myocardial balance of angiogenic cytokines. J Clin Invest 2006;116:1865–77.
  • Ortiz LA, Dutreil M, Fattman C, Pandey AC, Torres G, Go K, . Interleukin 1 receptor antagonist mediates the antiinflammatory and antifibrotic effect of mesenchymal stem cells during lung injury. Proc Natl Acad Sci USA 2007;104:11002–7.
  • Xu J, Woods CR, Mora AL, Joodi R, Brigham KL, Iyer S, . Prevention of endotoxin-induced systemic response by bone marrow derived mesenchymal stem cells in mice. Am J Physiol Lung Cell Mol Physiol 2007;293:L131–41.
  • Ortiz LA, Dutreil M, Fattman C, Pandey AC, Torres G, Go K, . Interleukin 1 receptor antagonist mediates the antiinflammatory and antifibrotic effect of mesenchymal stem cells during lung injury. Proc Natl Acad Sci USA 2007;104:11002–7.
  • Wong AP, Keating A, Lu WY, Duchesneau P, Wang X, Sacher A, . Identification of a bone marrow-derived epithelial-like population capable of repopulating injured mouse airway epithelium. J Clin Invest 2009;119:336–48.
  • Lagasse E, Connors H, Al-Dhalimy M, Reitsma M, Dohse M, Osborne L, . Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 2000;6:1229–34.
  • Aliotta JM, Sanchez-Guijo FM, Dooner GJ, Johnson KW, Dooner MS, Greer KA, . Alteration of marrow cell gene expression, protein production, and engraftment into lung by lung-derived microvesicles: a novel mechanism for phenotype modulation. Stem Cells 2007;25:2245–56.

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