Postnatal lung development of rhesus monkey airways: Cellular expression of Clara cell secretory protein

Developmental Dynamics

Volumn 238, Issue 12, 2009, Pages 3016-3024

  Coppens, John T ^a   Plopper, Charles G ^a,b   Murphy, Shannon R ^a   Van Winkle, Laura S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bronchial epithelium; CC10; CC16; Lung; Macaca mulatta; SCGB 1A1

Indexed keywords

CLARA CELL PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LUNG DEVELOPMENT; MORPHOMETRICS; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RESPIRATORY EPITHELIUM; RHESUS MONKEY;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; EPOXY RESINS; IMMUNOHISTOCHEMISTRY; LUNG; MACACA MULATTA; MICROTOMY; PHTHALIC ANHYDRIDES; RESPIRATORY SYSTEM; UTEROGLOBIN;

MACACA MULATTA;

EID: 70949104969     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22132     Document Type: Article

References (50)

1. Asabe K, Tsuji K, Handa N, Kajiwara M, Suita S. 1998. Expression of clara cell 10-kDa protein (CC10) in congenital diaphragmatic hernia. Pediatr Surg Int 14:36-39. (Pubitemid 29056039)
2. Avadhanam KP, Plopper CG, Pinkerton KE. 1997. Mapping the distribution of pulmonary neuroepithelial bodies of the rat lung: a whole mount immunohistochemical approach. Am J Pathol 150:850-859.
3. Boers JE, Ambergen AW, Thunnissen FB. 1999. Number and proliferation of clara cells in normal human airway epithelium. Am J Respir Crit Care Med 159:1585-1591.
4. Breeze RG, Wheeldon EB. 1977. The cells of the pulmonary airways. Am Rev Respir Dis 116:705-777.
5. Cardoso WV, Stewart LG, Pinkerton KE, Ji C, Hook GE, Singh G, Katyal SL, Thurlbeck WM, Plopper CG. 1993. Secretory product expression during Clara cell differentiation in the rabbit and rat. Am J Physiol 264:L543-L552. (Pubitemid 23195773)
6. Coppens JT, Van Winkle LS, Pinkerton K, Plopper CG. 2007. Distribution of Clara cell secretory protein expression in the tracheobronchial airways of rhesus monkeys. Am J Physiol Lung Cell Mol Physiol 292:L1155-L1162. (Pubitemid 47084859)
7. Engelhardt JF. 2001. Stem cell niches in the mouse airway. Am J Respir Cell Mol Biol 24:649-652.
8. Fanucchi MV, Murphy ME, Buckpitt AR, Philpot RM, Plopper CG. 1997. Pulmonary cytochrome P450 monooxygenase and Clara cell differentiation in mice. Am J Resp Cell Mol Biol 17:302-314. (Pubitemid 127500835)
9. Hyde DM, Tyler NK, Plopper CG. 2007. Morphometry of the respiratory tract: avoiding the sampling, size, orientation, and reference traps. Toxicol Pathol 35:41-48.
10. Jeffery PK, Gaillard D, Moret S. 1992. Human airway secretory cells during development and in mature airway epithelium. Eur Respir J 5:93-104.
11. Johnston CJ, Mango GW, Finkelstein JN, Stripp BR. 1997. Altered pulmonary response to hyperoxia in Clara cell secretory protein deficient mice. Am J Respir Cell Mol Biol 17:147-155.
12. Johnston CJ, Finkelstein JN, Oberdorster G, Reynolds SD, Stripp BR. 1999. 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 25:7-21. (Pubitemid 29077326)
13. Kajekar R, Pieczarka EM, Smiley-Jewell SM, Schelegle ES, Fanucchi MV, Plopper CG. 2007. Early postnatal exposure to allergen and ozone leads to hyperinnervation of the pulmonary epithelium. Respir Physiol Neurobiol 155:55-63. (Pubitemid 46049125)
14. Kay J, editor. 1991. Blood vessels of the lung. Boca Raton: CRC Press. p 163-172.
15. Khoor A, Gray ME, Singh G, Stahlman MT. 1996. Ontogeny of Clara cell-specific protein and its mRNA: their association with neuroepithelial bodies in human fetal lung and in bronchopulmonary dysplasia. J Histochem Cytochem 44:1429-1438. (Pubitemid 27009089)
16. Larson SD, Schelegle ES, Walby WF, Gershwin LJ, Fanuccihi MV, Evans MJ, Joad JP, Tarkington BK, Hyde DM, Plopper CG. 2004. Postnatal remodeling of the neural components of the epithelial-mesenchymal trophic unit in the proximal airways of infant rhesus monkeys exposed to ozone and allergen. Toxicol Appl Pharmacol 194:211-220.
17. Levine CR, Gewolb IH, Allen K, Welch RW, Melby JM, Pollack S, Shaffer T, Pilon AL, Davis JM. 2005. The safety, pharmacokinetics, and anti-inflammatory effects of intratracheal recombinant human Clara cell protein in premature infants with respiratory distress syndrome. Pediatr Res 58:15-21. (Pubitemid 40967423)
18. Miller LA, Hurst SD, Coffman RL, Tyler NK, Stovall MY, Chou DL, Putney LF, Gershwin LJ, Schelegle ES, Plopper CG, Hyde DM. 2005. Airway generation-specific differences in the spatial distribution of immune cells and cytokines in allergen-challenged rhesus monkeys. Clin Exp Allergy 35:894-906.
19. Nomori H, Morinaga S, Kobayashi R, Torikata C. 1994. Protein 1 and Clara cell 10-kDa protein distribution in normal and neoplastic tissues with emphasis on the respiratory system. Virchows Arch 424:517-523. (Pubitemid 24213611)
20. Plopper CG. 1983. Comparative morphologic features of bronchiolar epithelial cells: the Clara cell. Am Rev Respir Dis 128:S47-S41.
21. Plopper CG. 1990. Structural methods for studying bronchiolar epithelial cells. In: Gil J, editor. Models of lung disease, microscopy and structural methods. New York: Marcel Dekker, Inc. p 537-559.
22. Plopper CG, Hyde DM. 1992. Epithelial cells of bronchioles. In: Parent RA, editor. Comparative biology of the normal lung. Boca Raton: CRC Press. p 85-92.
23. Plopper CG, Hill LH, Mariassy AT. 1980. Ultrastructure of the nonciliated bronchiolar epithelial (Clara) cell of mammalian lung. III. A study of man with comparison of 15 mammalian species. Exp Lung Res 1:171-180.
24. Plopper C, Alley J, Serabjit-Singh C, Philpot R. 1983. Cytodifferentiation of the nonciliated bronchiolar epithelial (Clara) cell during rabbit lung maturation: an ultrastructural and morphometric study. Am J Anat 167:329-357.
25. Plopper CG, Alley JL, Weir AJ. 1986a. Differentiation of tracheal epithelium during fetal lung maturation in the rhesus monkey Macaca mulatta. Am J Anat 175:59-71.
26. Plopper CG, Weir AJ, Nishio SJ, Cranz DL, St. George JA. 1986b. Tracheal submucosal gland development in the rhesus monkey, Macaca mulatta: ultrastructure and histochemistry. Anat Embryol (Berl) 174:167-178.
27. Plopper CG, Hyde DM, Buckpitt AR. 1991. Clara cells. In: Crystal RG, West JB, editors. The lung: scientific foundations. New York: Raven Press. p 215-228.
28. Plopper CG, Macklin J, Nishio SJ, Hyde DM, Buckpitt AR. 1992. Relationship of cytochrome P-450 activity to Clara cell cytotoxicity. III. Morphometric comparison of changes in the epithelial populations of terminal bronchioles and lobar bronchi in mice, hamsters, and rats after parenteral administration of naphthalene. Lab Invest 67:553-565.
29. Plopper CG, Mango GW, Hatch GE, Wong VJ, Toskala E, Reynolds SD, Tarkington BK, Stripp BR. 2006. Elevation of susceptibility to ozone-induced acute tracheobronchial injury in transgenic mice deficient in Clara cell secretory protein. Toxicol Appl Pharmacol 15;213:74-85.
30. Ramsay PL, DeMayo FJ, Hegemier SE, Wearden ME, Smith CV, Welty SE. 2001. Clara cell secretory protein oxidation and expression in premature infants who develop bronchopulmonary dysplasia. Am J Respir Crit Care Med 164:155-161.
31. Sekhon HS, Jia Y, Raab R, Kuryatov A, Pankow JF, Whitsett JA, Lindstrom J, Spindel ER. 1999. Prenatal nicotine increases pulmonary alpha7 nicotinic receptor expression and alters fetal lung development in monkeys. J Clin Invest 103:637-647. (Pubitemid 29122416)
32. Shashikant BN, Miller TL, Welch RW, Pilon AL, Shaffer TH, Wolfson MR. 2005. Dose response to rhCC10-augmented surfactant therapy in a lamb model of infant respiratory distress syndrome: physiological, inflammatory, and kinetic profiles. J Appl Physiol 99:2204-2211.
33. Shi SR, Chaiwun B, Young L, Cote RJ, Taylor CR. 1993. Antigen retrieval technique utilizing citrate buffer or urea solution for immunohistochemical demonstration of androgen receptor in formalin-fixed paraffin sections. J Histochem Cytochem 41:1599-1604. (Pubitemid 23317103)
34. Shijubo N, Itoh Y, Yamaguchi T, Imada A, Hirasawa M, Yamada T, Kawai T, Abe S. 1999a. Clara cell protein-positive epithelial cells are reduced in small airways of asthmatics. Am J Respir Crit Care Med 160:930-933. (Pubitemid 29442033)
35. Shijubo N, Itoh Y, Yamaguchi T, Sugaya F, Hirasawa M, Yamada T, Kawai T, Abe S. 1999b. Serum levels of Clara cell 10-kDa protein are decreased in patients with asthma. Lung 177:45-52. (Pubitemid 29013440)
36. Singh G, Katyal S. 1992. Secretory proteins of Clara cells and type II cells. In: Parent RA, editor. Comparative biology of normal lung. Boca Raton: CRC Press. p 93-107.
37. Singh G, Singh J, Katyal S, Brown W, Kramps J, Paradis I, Dauber J, Macpherson T, Squeglia N. 1988. Identification, cellular localization, isolation and characterization of human Clara cell-specific 10 KD protein. J Histochem Cytochem 36:73-80. (Pubitemid 18023406)
38. Snyder JC, Reynolds SD, Hollingsworth JW, Li Z, Kaminski N, Stripp BR. 2009. Clara cells attenuate the inflammatory response through regulation of macrophage behavior. Am J Respir Cell Mol Biol [Epub ahead of print].
39. Stripp BR, Lund J, Mango GW, Doyen KC, Johnston C, Hultenby K, Nord M, Whitsett JA. 1996. Clara cell secretory protein: a determinant of PCB bioaccumulation in mammals. Am J Physiol 271:L656-L664. (Pubitemid 126757806)
40. Strum JM, Singh G, Katyal SL, McDowell EM. 1990. Immunochemical localization of Clara cell protein by light and electron microscopy in conducting airways of fetal and neonatal hamster lung. Anat Rec 227:77-86.
41. Ten Have-Opbroek AA. 1991. Lung development in the mouse embryo. Exp Lung Res 17:111-130.
42. ten Have-Opbroek AA, Otto-Verberne CJ, Dubbeldam JA, Dykman JH. 1991. The proximal border of the human respiratory unit, as shown by scanning and transmission electron microscopy and light microscopical cytochemistry. Anat Rec 229:339-354.
43. Tyler WS. 1983. Comparative subgross anatomy of lungs. Pleuras, interlobular septa, and distal airways. Am Rev Respir Dis 128:S32-S36.
44. Tyler NK, Plopper CG. 1985. Morphology of the distal conducting airways in rhesus monkey lungs. Anat Rec 211:295-303.
45. Tyler NK, Hyde DM, Hendrickx AG, Plopper CG. 1988. Morphogenesis of the respiratory bronchiole in rhesus monkey lungs. Am J Anat 182:215-223.
46. Tyler NK, Hyde DM, Hendrickx AG, Plopper CG. 1989. Cytodifferentiation of two epithelial populations of the respiratory bronchiole during fetal lung development in the rhesus monkey. Anat Rec 225:297-309.
47. Van Winkle LS, Fanucchi MV, Miller LA, Baker GL, Gershwin LJ, Schelegle ES, Hyde DM, Evans MJ, Plopper CG. 2004. Epithelial cell distribution and abundance in rhesus monkey airways during postnatal lung growth and development. J Appl Physiol 97:2355-2363.
48. Wilson DW, Plopper CG, Dungworth DL. 1984a. The response of the macaque tracheobronchial epithelium to acute ozone injury. A quantitative ultrastructural and autoradiographic study. Am J Pathol 116:193-206.
49. Wilson DW, Plopper CG, Hyde DM. 1984b. The tracheobronchial epithelium of the bonnet monkey (Macaca radiata): a quantitative ultrastructural study. Am J Anat 171:25-40.
50. Xu P, Hashimoto S, Miyazaki H, Asabe K, Shiraishi S, Sueishi K. 1998. Morphometric analysis of the immunohistochemical expression of Clara cell 10-kDa protein and surfactant apoproteins A and B in the developing bronchi and bronchioles of human fetuses and neonates. Virchows Arch 432:17-25. (Pubitemid 28065835)