A critical review of the use of Clara cell secretory protein (CC16) as a biomarker of acute or chronic pulmonary effects

References

• Anderson SD. How does exercise cause asthma attacks?. Current Opinion in Allergy and Clinical Immunology 2006; 6: 37–42
   PubMed Web of Science ®Google Scholar
• Andersson L, Lundberg PA, Barregard L. Methodological aspects on measurement of Clara cell protein in urine as a biomarker for airway toxicity, compared with serum levels. Journal of Applied Toxicology 2007; 27: 60–66
   PubMed Web of Science ®Google Scholar
• Arsalane K, Broeckaert F, Knoops B, Wiedig M, Toubeau G, Bernard A. Clara cell specific protein (CC16) expression after acute lung inflammation induced by intratracheal lipopolysaccharide administration. American Journal of Respiratory and Critical Care Medicine 2000; 161: 1624–1630
   PubMed Web of Science ®Google Scholar
• Barbet JP, Chauveau M, Labbe S, Lockhart A. Breathing dry air causes acute epithelial damage and inflammation of the guinea pig trachea. Journal of Applied Physiology 1988; 64: 1851–1857
   Google Scholar
• Benson M, Jansson L, Adner M, Luts A, Uddman R, Cardell LO. Gene profiling reveals decreased expression of uteroglobin and other anti-inflammatory genes in nasal fluid cells from patients with intermittent allergic rhinitis. Clinical and Experimental Allergy 2005; 35: 473–478
   PubMed Web of Science ®Google Scholar
• Benson M, Fransson M, Martinsson T, Naluai AT, Uddman R, Cardell LO. Inverse relation between nasal fluid Clara Cell Protein 16 levels and symptoms and signs of rhinitis in allergen-challenged patients with intermittent allergic rhinitis. Allergy 2007; 62: 178–83
   PubMedGoogle Scholar
• Bernard A, Hermans C. Biomonitoring of early effects on the kidney or lung. The Science of the Total Environment 1997; 199: 205–211
   PubMed Web of Science ®Google Scholar
• Bernard A, Hermans C, Van Houte G. Transient increase of serum Clara cell protein (CC16) after exposure to smoke. Occupational and Environmental Medicine 1997; 54: 63–65
   PubMed Web of Science ®Google Scholar
• Bernard A, Marchandise FX, Depelchin S, Lauwerys R, Sibille Y. Clara cell protein in serum and bronchoalveolar lavage. The European Respiratory Journal 1992; 5: 1231–1238
   PubMed Web of Science ®Google Scholar
• Bernard A, Dumont X, Roels H, Lauwerys R, Dierynck I, De Ley M, Stroobant V, de Hoffmann E. The molecular mass and concentrations of protein 1 or Clara cell protein in biological fluids: A reappraisal. Clinica Chimica Acta 1993; 223: 189–191
   PubMed Web of Science ®Google Scholar
• Bernard AN, Thielemans R, Lauwerys R, Langhendries JP, Van Lierde M, Freund MM. Clara cell protein in human amniotic fluid: a potential marker of fetal lung growth. Pediatric Research 1994a; 36: 771–775
   PubMed Web of Science ®Google Scholar
• Bernard AM, Gonzalez-Lorenzo JM, Siles E, Trujillano G, Lauwerys R. Early decrease of serum Clara cell protein in silica-exposed workers. European Respiratory Journal 1994b; 7: 1932–1937
   PubMed Web of Science ®Google Scholar
• Bernard A, Carbonnelle S, Michel O, Higuet S, De Burbure C, Buchet JP, Hermans C, Dumont X, Doyle I. Lung hyperpermeability and asthma prevalence in schoolchildren: unexpected associations with the attendance at indoor chlorinated swimming pools. Occupational and Environmental Medicine 2003; 60: 385–394
   PubMed Web of Science ®Google Scholar
• Bernard A, Carbonnelle S, Nickmilder M, de Burbure C. Non-invasive biomarkers of pulmonary damage and inflammation: Application to children exposed to ozone and trichloramine. Toxicology and Applied Pharmacology 2005; 206: 185–190
   PubMed Web of Science ®Google Scholar
• Blomberg A, Mudway I, Svensson M, Hagenbjork-Gustafsson A, Thomasson L, Helleday R, Dumont X, Forsberg B, Nordberg G, Bernard A. Clara cell protein as a biomarker for ozone-induced lung injury in humans. European Respiratory Journal 2003; 22: 883–888
   PubMed Web of Science ®Google Scholar
• Boers JE, Ambergen AW, Thunnissen FBJM. Number and proliferation of Clara cells in normal human airway epithelium. American Journal of Respiratory and Critical Care Medicine 1999; 159: 1585–1591
   PubMed Web of Science ®Google Scholar
• Bonetto G, Corradi M, Carraro S, Zanconato S, Alinovi R, Folesani G, Da Dalt L, Mutti A, Baraldi E. Longitudinal monitoring of lung injury in children after acute chlorine exposure in a swimming pool. American Journal of Respiratory and Critical Care Medicine 2006; 174: 545–9
   PubMed Web of Science ®Google Scholar
• Brigham KL, Meyrick B. Endotoxin and lung injury. American Review of Respiratory Disease 1986; 133: 913–927
   PubMed Web of Science ®Google Scholar
• Broeckaert F, Bernard A. Clara cell secretory protein (CC16): characteristics and perspectives as lung peripheral biomarker. Clinical and Experimental Allergy 2000; 30: 469–475
   PubMed Web of Science ®Google Scholar
• Broeckaert F, Clippe A, Knoops B, Hermans C, Bernard A. Clara cell secretory protein (CC16): features as a peripheral lung biomarker. Annals New York Academy of Science 2000a; 923: 68–77
   PubMed Web of Science ®Google Scholar
• Broeckaert F, Arsalane K, Hermans C, Bergamaschi E, Brustolin A, Mutti A, Bernard A. Serum clara cell protein: a sensitive biomarker of increased lung epithelium permeability caused by ambient ozone. Environmental Health Perspectives 2000b; 108: 533–537
   PubMed Web of Science ®Google Scholar
• Candelaria PV, Backer V, Laing IA, Porsbjerg C, Nepper-Christensen S, de Klerk N, Goldblatt J, Le Souef PN. Association between asthma-related phenotypes and the CC16 A38G polymorphism in an unselected population of young adult Danes. Immunogenetics 2005; 57: 25–32
   PubMed Web of Science ®Google Scholar
• Carbonnelle S, Francaux M, Doyle I, Dumont X, de Burbure C, Morel G, Michel O, Bernard A. Changes in serum pneumoproteins caused by short-term exposures to nitrogen trichloride in indoor chlorinated swimming pools. Biomarkers 2002; 7: 464–478
   PubMed Web of Science ®Google Scholar
• Cookson WO, Sharp PA, Faux JA, Hopkin JM. Linkage between immunoglobulin E responses underlying asthma and rhinitis and chromosome 11q. Lancet 1989; 1: 1292–1295
   PubMed Web of Science ®Google Scholar
• de Burbure C, Pignatti P, Corradi M, Malerba M, Clippe A, Dumont X, Moscato G, Mutti A, Bernard A. Uteroglobin-related protein 1 and clara cell protein in induced sputum of patients with asthma and rhinitis. Chest 2007; 131: 172–179
   PubMedGoogle Scholar
• Drobnic F, Freixa A, Casan P, Sanchis J, Guardino X. Assessment of chlorine exposure in swimmers during training. Medicine and Science in Sports and Exercise 1996; 28: 271–274
   PubMed Web of Science ®Google Scholar
• Gagnaire F, Azim S, Bonnet P, Hecht G, Hery M. Comparison of the sensory irritation response in mice to chlorine and nitrogen trichloride. Journal of Applied Toxicology 1994; 14: 405–409
   PubMed Web of Science ®Google Scholar
• Gao PS, Mao XQ, Kawai M, Enomoto T, Sasaki S, Tanabe O, Yoshimura K, Shaldon SR, Dake Y, Kitano H, Coull P, Shirakawa T, Hopkin JM. Negative association between asthma and variants of CC16(CC10) on chromosome 11q13 in British and Japanese populations. Human Genetics 1998; 103: 57–59
   PubMedGoogle Scholar
• Gioldassi XM, Papadimitriou H, Mikraki V, Karamanos NK. Clara cell secretory protein: determination of serum levels by an enzyme immunoassay and its importance as an indicator of bronchial asthma in children. Journal of Pharmaceutical and Biomedical Analysis 2004; 34: 823–826
   PubMedGoogle Scholar
• Halatek T, Hermans C, Broeckaert F, Wattiez R, Wiedig M, Toubeau G, Falmagne P, Bernard A. Quantification of Clara cell protein in rat and mouse biological fluids using a sensitive immunoassay. European Respiratory Journal 1998; 11: 726–733
   PubMed Web of Science ®Google Scholar
• Halatek T, Gromadzinska J, Wasowicz W, Rydzynski K. Serum clara-cell protein and β2-microglobulin as early markers of occupational exposure to nitric oxides. Inhalation Toxicology 2005a; 17: 87–97
   PubMed Web of Science ®Google Scholar
• Halatek T, Sinczuk-Walczak H, Rydzynski K. Prognostic significance of low serum levels of Clara cell phospholipid-binding protein in occupational aluminium neurotoxicity. Journal of Inorganic Biochemistry 2005b; 99: 1904–1911
   PubMed Web of Science ®Google Scholar
• Hashimoto S, Nakagawa K, Sueishi K. Monkey Clara cell 10 kDa protein (CC10): a characterization of the amino acid sequence with an evolutional comparison with humans, rabbits, rats and mice. American Journal of Respiratory Cell and Molecular Biology 1996; 15: 361–366
   PubMed Web of Science ®Google Scholar
• Haughton MA, Mason RS. Immunonephelometric assay of vitamin D-binding. protein. Clinical Chemistry 1992; 38: 1796–801
   Google Scholar
• Helenius I, Haahtela T. Allergy and asthma in elite summer sport athletes. Journal of Allergy and Clinical Immunology 2000; 106: 444–452
   PubMed Web of Science ®Google Scholar
• Helleday R, Segerstedt B, Forsberg B, Nordberg G, Svensson M, Bernard A, et al. Diurnal variation in serum levels of Clara cell protein (CC16) in humans. (Abstract). European Respiratory Journal 2003; 22(Suppl. 45)75s
   Google Scholar
• Helleday R, Segerstedt B, Forsberg B, Mudway I, Nordberg G, Bernard A, Blomberg A. Exploring the time dependence of serum clara cell protein as a biomarker of pulmonary injury in humans. Chest 2006; 130: 672–675
   PubMed Web of Science ®Google Scholar
• Hermans C, Bernard A. Lung epithelium-specific proteins. Characteristics and potential applications. State of the Art American Journal of Respiratory and Critical Care Medicine 1999; 159: 646–678
   PubMed Web of Science ®Google Scholar
• Hermans C, Aly O, Nyberg BI, Peterson C, Bernard A. Determinants of Clara cell protein (CC16) concentration in serum: a reassessment with two different immunoassays. Clinica Chimica Acta 1998; 272: 101–110
   PubMed Web of Science ®Google Scholar
• Hermans C, Knoops B, Wiedig M, Arsalane K, Toubeau G, Falmagne P, Bernard A. Clara cell protein as a marker of Clara cell damage and bronchoalveolar blood barrier permeability. European Respiratory Journal 1999; 13: 1014–1021
   PubMed Web of Science ®Google Scholar
• Hermans C, Dong P, Robin M, Jadoul M, Bernard A, Bersten AD, Doyle IR. Determinants of serum levels of surfactant proteins A and B and Clara cell protein CC16. Biomarkers 2003; 8: 461–471
   PubMed Web of Science ®Google Scholar
• Hery M, Hecht G, Gendre JC, Hubert G, Rebuffaud I. Exposure to chloramines in the atmosphere of indoor swimming pools. Annals of Occupational Hygiene 1995; 39: 427–439
   Web of Science ®Google Scholar
• Johansson S, Keen C, Stahl A, Wennergren G, Benson M. Low levels of CC16 in nasal fluid of children with birch pollen-induced rhinitis. Allergy 2005; 60: 638–642
   Google Scholar
• 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. Experimental Lung Research 1999; 25: 7–21
   PubMed Web of Science ®Google Scholar
• Jorens PG, Sibille Y, Goulding NJ, van Overveld FJ, Herman AG, Bossaert L, De Backer WA, Lauwerys R, Flower RJ, Bernard A. Potential role of Clara cell protein, an endogenous phospholipase A2 inhibitor, in acute lung injury. European Respiratory Journal 1995; 8: 1647–1653
   PubMed Web of Science ®Google Scholar
• Lagerkvist BJ, Bernard A, Blomberg A, Bergstrom E, Forsberg B, Holmstrom K, Karp K, Lundstrom NG, Segerstedt B, Svensson M, Nordberg G. Pulmonary epithelial integrity in children: relationship to ambient ozone exposure and swimming pool attendance. Environmental Health Perspectives 2004; 112: 1768–1771
   PubMed Web of Science ®Google Scholar
• Laing IA, Goldblatt J, Eber E, Hayden CM, Rye PJ, Gibson NA, Palmer LJ, Burton PR, Le Souëf PN. A polymorphism of the CC16 gene is associated with an increased risk of asthma. Medical Genetics 1998; 35: 463–467
   PubMed Web of Science ®Google Scholar
• Laing IA, Hermans C, Bernard A, Burton PR, Goldblatt J, Le Souef PN. Association between plasma CC16 levels, the A38G polymorphism, and asthma. American Journal of Respiratory and Critical Care Medicine 2000; 161: 124–127
   PubMed Web of Science ®Google Scholar
• Lesur O, Langevin S, Berthiaume Y, Légaré M, Skrobik Y, Bellemare JF, Levy B, Fortier Y, Lauzier F, Bravo G, Nickmilder M, Rousseau E, Bernard A. The prognostic value of bronchiolar epithelial Clara cell specific protein in the serum of patients with acute respiratory distress syndrome (ARDS). Intensive Care Medicine 2006; 32: 1167–1174
   PubMed Web of Science ®Google Scholar
• Mango GW, Johnston CJ, Reynolds SD, Finkelstein JN, Plopper CG, Stripp BR. Clara cell secretory protein deficiency increases oxidant stress response in conducting airways. American Journal of Physiology. Lung Cellular and Molecular Physiology 1998; 275: L348–L356
   PubMed Web of Science ®Google Scholar
• Mansur AH, Fryer AA, Hepple M, Strange RC, Spiteri MA. An association study between the Clara cell secretory protein CC16 A38G polymorphism and asthma phenotypes. Clinical and Experimental Allergy 2002; 32: 994–999
   PubMedGoogle Scholar
• Mao XQ, Shirakawa T, Kawai M, Enomoto T, Sasaki S, Dake Y, Kitano H, Hagihara A, Hopkin JM, Morimoto K. Association between asthma and an intragenic variant of CC16 on chromosome 11q13. Clinical Genetics 1998; 53: 54–56
   PubMed Web of Science ®Google Scholar
• Massin N, Bohadana AB, Wild P, Hery M, Toamain JP, Hubert G. Respiratory symptoms and bronchial responsiveness in lifeguards exposed to nitrogen trichloride in indoor swimming pools. Occupational and Environmental Medicine 1998; 55: 258–263
   PubMed Web of Science ®Google Scholar
• 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 allogenic stem-cell transplantation. Transplantation 2005; 79: 1411–1416
   PubMed Web of Science ®Google Scholar
• Michel O, Murdoch R, Bernard A. Inhaled LPS induces blood release of Clara cell specific protein (CC16) in human beings. Journal of Allergy and Clinical Immunology 2005; 115: 1143–1147
   PubMed Web of Science ®Google Scholar
• Nanson CJ, Burgess JL, Robin M, Bernard AM. Exercise alters serum pneumoprotein concentrations. Respiration Physiology 2001; 127: 259–265
   PubMedGoogle Scholar
• Needham L. 2005. Chloracne: How relevant is it to dioxin poisoning? Presentation, Dioxin. Proceedings of Organohalogen Compounds – 2005. Volume 67 (CO) 1711–1714.
   Google Scholar
• Nickmilder M, Carbonnelle S, Bernard A. House cleaning with chlorine bleach and the risks of allergic and respiratory diseases in children. Pediatric Allergy and Immunology 2007; 18: 27–35
   PubMed Web of Science ®Google Scholar
• Nomori H, Horio H, Takagi M, Kobayashi R, Hirabayashi Y. Clara cell protein correlation with hyperlipidemia. Chest 1996; 110: 680–684
   PubMed Web of Science ®Google Scholar
• 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. European Respiratory Journal 2002; 20: 1152–1161
   PubMed Web of Science ®Google Scholar
• Saadat M, Saadat I, Saboori Z, Emad A. Combination of CC16, GSTM1, and GSTT1 genetic polymorphisms is associated with asthma. Journal of Allergy and Clinical Immunology 2004; 13: 996–998
   Google Scholar
• Sengler C, Heinzmann A, Jerkic SP, Haider A, Sommerfeld C, Niggemann B, Lau S, Forster J, Schuster A, Kamin W, Bauer C, Laing I, LeSouef P, Wahn U, Deichmann K, Nickel R. Clara cell protein 16 (CC16) gene polymorphism influences the degree of airway responsiveness in asthmatic children. Journal of Allergy and Clinical Immunology 2003; 111: 515–519
   PubMedGoogle Scholar
• Sharma S, Ghosh B. Association of an intragenic microsatellite marker in the CC16 gene with asthma in the Indian population. Journal of Human Genetics 2004; 49: 677–683
   PubMedGoogle Scholar
• Shijubo N, Itoh Y, Yamaguchi T, Shibuya Y, Morita Y, Hirasawa M, Okutani R, Kawai T, Abe S. Serum and BAL Clara cell 10 kDa protein (CC10) levels and CC10-positive bronchiolar cells are decreased in smokers. European Respiratory Journal 1997; 10: 1108–1114
   PubMed Web of Science ®Google Scholar
• Shijubo N, Itoh Y, Yamaguchi T, Hirasawa M, Yamada T, Kawai T, Abe S. 1999. Serum levels of Clara cell 10-kDa protein are decreased in patients with asthma. Lung 45–52.
   Google Scholar
• Shijubo N, Itoh Y, Yamaguchi T, Abe S. Development of an enzyme-linked immunosorbent assay for Clara cell 10-kDa protein: in pursuit of clinical significance of sera in patients with asthma and sarcoidosis. Annals of the New York Academy of Science 2000; 923: 268–279
   PubMed Web of Science ®Google Scholar
• Shijubo N, Kawabata I, Sato N, Itoh Y. Clinical aspects of Clara cell 10-kDa protein/uteroglobin (secretoglobin 1A1). Current Pharmaceutical Design 2003; 9: 1139–1149
   PubMed Web of Science ®Google Scholar
• Singh G, Katyal SL. Clara cells and Clara cell 10 kD protein (CC10). American Journal of Respiratory Cell and Molecular Biology 1997; 17: 141–143
   PubMed Web of Science ®Google Scholar
• Steiner D, Jeggli S, Tschopp A, Bernard A, Oppliger A, Hilfiker S, Hotz P. Clara cell protein and surfactant protein B in garbage collectors and in wastewater workers exposed to bioaerosols. International Archives of Occupational and Environmental Health 2005; 78: 189–197
   PubMed Web of Science ®Google Scholar
• Thickett KM, McCoach JS, Gerber JM, Sadhra S, Burge PS. Occupational asthma caused by chloramines in indoor swimming-pool air. European Respiratroy Journal 2002; 19: 827–832
   PubMed Web of Science ®Google Scholar
• van Herwerden L, Harrap SB, Wong ZY, Abramson MJ, Kutin JJ, Forbes AB, Raven J, Lanigan A, Walters EH. Linkage of high-affinity IgE receptor gene with bronchial hyperreactivity, even in absence of atopy. Lancet 1995; 346: 1262–1265
   PubMed Web of Science ®Google Scholar
• van Miert E, Dumont X, Bernard A. CC16 as a marker of lung epithelial hyperpermeability in an acute model of rats exposed to mainstream smoke. Toxicology Letters 2005; 159: 115–123
   PubMed Web of Science ®Google Scholar
• van Vyve T, Chanez P, Bernard A, Bousquet J, Godard P, Lauwerijs R, Sibille Y. Protein content in bronchoalveolar lavage fluid of patients with asthma and control subjects. Journal of Allergy and Clinical Immunology 1995; 95: 60–68
   PubMed Web of Science ®Google Scholar
• Ye Q, Fujita M, Ouchi H, Inoshima I, Maeyama T, Kuwano K, Horiuchi Y, Hara N, Nakanishi Y. Serum CC-10 in inflammatory lung diseases. Respiration 2004; 71: 505–510
   PubMed Web of Science ®Google Scholar
• Yoneda K. Ultrastructural localization of phospholipases in the Clara cell of the rat bronchiole. American Journal of Pathology 1978; 93: 745–752
   PubMed Web of Science ®Google Scholar