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. 1975 Nov;120(Pt 2):295–320.

New observations of rat airway epithelium: a quantitative and electron microscopic study.

P K Jeffery 1, L Reid 1
PMCID: PMC1231972  PMID: 1201964

Abstract

Epithelial thickness, depth of the ciliary layer and concentration of cells has been estimated at 5 levels of the rat airway (3 extrapulmonary and 2 intrapulmonary) and the ultrastructure of the cells described. Extrapulmonary airways have a pseudostratified epithelium, intrapulmonary airways a simple one. The epithelium thins progressively from upper to lower trachea while the epithelium of the lower trachea is thicker than at more peripheral airway levels, all of which are similar. The depth of the ciliary layer decreases peripherally. By electron microscopy 10 cell types could be identified - 8 epithelial and 2 'migratory'. A cell type not described previously has been found that resembles the serous cells of the submucosal glands. The salient features of each cell type are described. The upper trachea has a concentration of cells significantly higher than elsewhere, while the remaining four airway levels have about 230 cells per 10 high power fields (1-8 mm length epithelium). Ciliated cells are sparse proximally and increase in number progressively toward the periphery, while basal and migratory cells are most frequent proximally. At all levels of the airway, between 40% and 50% of cells are non-ciliated. In the upper trachea the most frequent cell type was the 'intermediate', elsewhere the 'epithelial serous' cell. Goblet cells were few at all levels, amounting to less than 1% of the total counted. The Clara cell was not restricted to the terminal bronchioles but was found as far proximally as the hilum.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Askin F. B., Kuhn C. The cellular origin of pulmonary surfactant. Lab Invest. 1971 Sep;25(3):260–268. [PubMed] [Google Scholar]
  2. Azzopardi A., Thurlbeck W. M. The histochemistry of the nonciliated bronchiolar epithelial cell. Am Rev Respir Dis. 1969 Apr;99(4):516–525. doi: 10.1164/arrd.1969.99.4P1.516. [DOI] [PubMed] [Google Scholar]
  3. BENSCH K. G., GORDON G. B., MILLER L. R. ELECTRON MICROSCOPIC AND BIOCHEMICAL STUDIES ON THE BRONCHIAL CARCINOID TUMOR. Cancer. 1965 May;18:592–602. doi: 10.1002/1097-0142(196505)18:5<592::aid-cncr2820180508>3.0.co;2-6. [DOI] [PubMed] [Google Scholar]
  4. Baskerville A. Ultrastructural studies of the normal pulmonary tissue of the pig. Res Vet Sci. 1970 Mar;11(2):150–155. [PubMed] [Google Scholar]
  5. Basset F., Poirier J., Le Crom M., Turiaf J. Etude ultrastructurale de l'épithélium bronchiolaire humain. Z Zellforsch Mikrosk Anat. 1971;116(3):425–442. [PubMed] [Google Scholar]
  6. Bensch K. G., Gordon G. B., Miller L. R. Studies on the bronchial counterpart of the Kultschitzky (argentaffin) cell and innervation of bronchial glands. J Ultrastruct Res. 1965 Jun;12(5):668–686. doi: 10.1016/s0022-5320(65)80055-7. [DOI] [PubMed] [Google Scholar]
  7. Blenkinsopp W. K. Proliferation of respiratory tract epithelium in the rat. Exp Cell Res. 1967 Apr;46(1):144–154. doi: 10.1016/0014-4827(67)90416-8. [DOI] [PubMed] [Google Scholar]
  8. Carvalheira A. F., Welsch U., Pearse A. G. Cytochemical and ultrastructural observations on the argentaffin and argyrophil cells of the gastro-intestinal tract in mammals, and their place in the APUD series of polypeptide-secreting cells. Histochemie. 1968;14(1):33–46. doi: 10.1007/BF00268031. [DOI] [PubMed] [Google Scholar]
  9. Cook R. D., King A. S. A neurite-receptor complex in the avian lung: electron microscopical observations. Experientia. 1969 Nov 15;25(11):1162–1164. doi: 10.1007/BF01900251. [DOI] [PubMed] [Google Scholar]
  10. Cutz E., Chan W., Wong V., Conen P. E. Endocrine cells in rat fetal lungs. Ultrastructural and histochemical study. Lab Invest. 1974 Apr;30(4):458–464. [PubMed] [Google Scholar]
  11. Cutz E., Conen P. E. Ultrastructure and cytochemistry of Clara cells. Am J Pathol. 1971 Jan;62(1):127–141. [PMC free article] [PubMed] [Google Scholar]
  12. Darlington D., Rogers A. W. Epithelial lymphocytes in the small intestine of the mouse. J Anat. 1966 Oct;100(Pt 4):813–830. [PMC free article] [PubMed] [Google Scholar]
  13. Dobson C. Immunofluorescent staining of globule leucocytes in the colon of the sheep. Nature. 1966 Aug 20;211(5051):875–875. doi: 10.1038/211875a0. [DOI] [PubMed] [Google Scholar]
  14. ENDERS A. C., LYONS W. R. OBSERVATIONS ON THE FINE STRUCTURE OF LUTEIN CELLS. II. THE EFFECTS OF HYPOPHYSECTOMY AND MAMMOTROPHIC HORMONE IN THE RAT. J Cell Biol. 1964 Jul;22:127–141. doi: 10.1083/jcb.22.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. ENGSTROM H., WERSALL J. Some principles in the structure of vibratile cilia. Ann Otol Rhinol Laryngol. 1952 Dec;61(4):1027–1038. doi: 10.1177/000348945206100405. [DOI] [PubMed] [Google Scholar]
  16. Ericson L. E., Håkanson R., Larson B., Owman C., Sundler F. Fluorescence and electron microscopy of amine-storing enterochromaffin-like cells in tracheal epithelium of mouse. Z Zellforsch Mikrosk Anat. 1972;124(4):532–545. doi: 10.1007/BF00335256. [DOI] [PubMed] [Google Scholar]
  17. Etherton J. E., Conning D. M., Corrin B. Autoradiographical and morphological evidence for apocrine secretion of dipalmitoyl lecithin in the terminal bronchiole of mouse lung. Am J Anat. 1973 Sep;138(1):11–35. doi: 10.1002/aja.1001380103. [DOI] [PubMed] [Google Scholar]
  18. Etherton J. E., Conning D. M. Early incorporation of labelled palmitate into mouse lung. Experientia. 1971 May 15;27(5):554–555. doi: 10.1007/BF02147597. [DOI] [PubMed] [Google Scholar]
  19. Ewen S. W., Bussolati G., Pearse A. G. Uptake of L-dopa and L-5-hydroxytryptophan by endocrine-like cells in the rat larynx. Histochem J. 1972 Mar;4(2):103–110. doi: 10.1007/BF01004969. [DOI] [PubMed] [Google Scholar]
  20. Frasca J. M., Auerbach O., Parks V. R., Jamieson J. D. Electron microscopic observations of the bronchial epithelium of dogs. I. Control dogs. Exp Mol Pathol. 1968 Dec;9(3):363–379. doi: 10.1016/0014-4800(68)90026-9. [DOI] [PubMed] [Google Scholar]
  21. Frasca J. M., Auerbach O., Parks V. R., Stoeckenius W. Electron microscopic observations on bronchial epithelium. 1. Annulate lamellae. Exp Mol Pathol. 1967 Apr;6(2):261–273. doi: 10.1016/0014-4800(67)90062-7. [DOI] [PubMed] [Google Scholar]
  22. Gmelich J. T., Bensch K. G., Liebow A. A. Cells of Kultschitzky type in bronchioles and their relation to the origin of peripheral carcinoid tumor. Lab Invest. 1967 Jul;17(1):88–98. [PubMed] [Google Scholar]
  23. Greenwood M. F., Holland P. The mammalian respiratory tract surface. A scanning electron microscopic study. Lab Invest. 1972 Sep;27(3):296–304. [PubMed] [Google Scholar]
  24. Hage E. Electron microscopic identification of several types of endocrine cells in the bronchial epithelium of human foetuses. Z Zellforsch Mikrosk Anat. 1973 Aug 3;141(3):401–412. doi: 10.1007/BF00307413. [DOI] [PubMed] [Google Scholar]
  25. Hage E. Endocrine cells in the bronchial mucosa of human foetuses. Acta Pathol Microbiol Scand A. 1972;80(2):225–234. doi: 10.1111/j.1699-0463.1972.tb02169.x. [DOI] [PubMed] [Google Scholar]
  26. Hansell M. M., Moretti R. L. Ultrastructure of the mouse tracheal epithelium. J Morphol. 1969 Jun;128(2):159–169. doi: 10.1002/jmor.1051280203. [DOI] [PubMed] [Google Scholar]
  27. Hung K. S., Hertweck M. S., Hardy J. D., Loosli C. G. Ultrastructure of nerves and associated cells in bronchiolar epithelium of the mouse lung. J Ultrastruct Res. 1973 Jun;43(5):426–437. doi: 10.1016/s0022-5320(73)90019-1. [DOI] [PubMed] [Google Scholar]
  28. Jeffery P., Reid L. Intra-epithelial nerves in normal rat airways: a quantitative electron microscopic study. J Anat. 1973 Jan;114(Pt 1):35–45. [PMC free article] [PubMed] [Google Scholar]
  29. Jones R., Bolduc P., Reid L. Goblet cell glycoprotein and tracheal gland hypertrophy in rat airways: the effect of tobacco smoke with or without the anti-inflammatory agent phenylmethyloxadiazole. Br J Exp Pathol. 1973 Apr;54(2):229–239. [PMC free article] [PubMed] [Google Scholar]
  30. KARRER H. E. Electron microscopic study of bronchiolar epithelium of normal mouse lung; preliminary report. Exp Cell Res. 1956 Feb;10(1):237–241. doi: 10.1016/0014-4827(56)90093-3. [DOI] [PubMed] [Google Scholar]
  31. KELLAS L. M. An intra-epithelial granular cell in the uterine epithelium of some ruminant species during the pregnancy cycle. Acta Anat (Basel) 1961;44:109–130. doi: 10.1159/000141713. [DOI] [PubMed] [Google Scholar]
  32. KENT J. F. The origin, fate, and cytochemistry of the globule leucocyte of the sheep. Anat Rec. 1952 Jan;112(1):91–115. doi: 10.1002/ar.1091120107. [DOI] [PubMed] [Google Scholar]
  33. Kent J. F. Distribution and fine structure of globule leucocytes in respiratory and digestive tracts of the laboratory rat. Anat Rec. 1966 Dec;156(4):439–453. doi: 10.1002/ar.1091560408. [DOI] [PubMed] [Google Scholar]
  34. Konrádová V. The ultrastructure of the tracheal epithelium in rabbit. Folia Morphol (Praha) 1966;14(3):210–214. [PubMed] [Google Scholar]
  35. Lauweryns J. M., Cokelaere M. Hypoxia-sensitive neuro-epithelial bodies. Intrapulmonary secretory neuroreceptors, modulated by the CNS. Z Zellforsch Mikrosk Anat. 1973 Dec 21;145(4):521–540. doi: 10.1007/BF00306722. [DOI] [PubMed] [Google Scholar]
  36. Lauweryns J. M., Cokelaere M., Theunynck P. Neuro-epithelial bodies in the respiratory mucosa of various mammals. A light optical, histochemical and ultrastructural investigation. Z Zellforsch Mikrosk Anat. 1972;135(4):569–592. doi: 10.1007/BF00583438. [DOI] [PubMed] [Google Scholar]
  37. Lopez-Vidriero M. T., Charman J., Keal E., De Silva D. J., Reid L. Sputum viscosity: correlation with chemical and clinical features in chronic bronchitis. Thorax. 1973 Jul;28(4):401–408. doi: 10.1136/thx.28.4.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Luciano L., Reale E., Ruska H. Uber eine "chemorezeptive" Sinneszelle in der Trachea der Ratte. Z Zellforsch Mikrosk Anat. 1968;85(3):350–375. [PubMed] [Google Scholar]
  39. Meyrick B., Reid L. Electron microscopic aspects of surfactant secretion. Proc R Soc Med. 1973 Apr;66(4):386–387. doi: 10.1177/003591577306600434. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Meyrick B., Reid L. The alveolar brush cell in rat lung--a third pneumonocyte. J Ultrastruct Res. 1968 Apr;23(1):71–80. doi: 10.1016/s0022-5320(68)80032-2. [DOI] [PubMed] [Google Scholar]
  41. Meyrick B., Reid L. Ultrastructure of cells in the human bronchial submucosal glands. J Anat. 1970 Sep;107(Pt 2):281–299. [PMC free article] [PubMed] [Google Scholar]
  42. Moosavi H., Smith P., Heath D. The Feyrter cell in hypoxia. Thorax. 1973 Nov;28(6):729–741. doi: 10.1136/thx.28.6.729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Niden A. H. Bronchiolar and large alveolar cell in pulmonary phospholipid metabolism. Science. 1967 Dec 8;158(3806):1323–1324. doi: 10.1126/science.158.3806.1323. [DOI] [PubMed] [Google Scholar]
  44. Pearse A. G., Polak J. M. Cytochemical evidence for the neural crest origin of mammalian ultimobranchial C cells. Histochemie. 1971;27(2):96–102. doi: 10.1007/BF00284951. [DOI] [PubMed] [Google Scholar]
  45. Pearse A. G. The cytochemistry and ultrastructure of polypeptide hormone-producing cells of the APUD series and the embryologic, physiologic and pathologic implications of the concept. J Histochem Cytochem. 1969 May;17(5):303–313. doi: 10.1177/17.5.303. [DOI] [PubMed] [Google Scholar]
  46. Petrik P., Collet A. J. Quantitative electron microscopic autoradiography of in vivo incorporation of 3H-choline, 3H-leucine, 3H-acetate and 3H-galactose in non-ciliated bronchiolar (Clara) cells of mice. Am J Anat. 1974 Apr;139(4):519–533. doi: 10.1002/aja.1001390405. [DOI] [PubMed] [Google Scholar]
  47. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. RHODIN J., DALHAMN T. Electron microscopy of the tracheal ciliated mucosa in rat. Z Zellforsch Mikrosk Anat. 1956;44(4):345–412. doi: 10.1007/BF00345847. [DOI] [PubMed] [Google Scholar]
  49. Reid L. Evaluation of model systems for study of airway epithelium, cilia, and mucus. Arch Intern Med. 1970 Sep;126(3):428–434. [PubMed] [Google Scholar]
  50. Rhodin J. A. The ciliated cell. Ultrastructure and function of the human tracheal mucosa. Am Rev Respir Dis. 1966 Mar;93(3 Suppl):1–15. doi: 10.1164/arrd.1966.93.3P2.1. [DOI] [PubMed] [Google Scholar]
  51. Rosan R. C., Lauweryns J. M. Mucosal cells of the small bronchioles of prematurely born human infants (600-1700 g). Beitr Pathol. 1972;147(2):145–174. doi: 10.1016/s0005-8165(72)80025-8. [DOI] [PubMed] [Google Scholar]
  52. Rosan R. C., Lauweryns J. M. Secretory cells in the premature human lung lobule. Nature. 1971 Jul 2;232(5305):60–61. doi: 10.1038/232060a0. [DOI] [PubMed] [Google Scholar]
  53. SELZMAN H. M., LIEBELT R. A. Paneth cell granule of mouse intestine. J Cell Biol. 1962 Oct;15:136–139. doi: 10.1083/jcb.15.1.136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. STEMPAK J. G., WARD R. T. AN IMPROVED STAINING METHOD FOR ELECTRON MICROSCOPY. J Cell Biol. 1964 Sep;22:697–701. doi: 10.1083/jcb.22.3.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Smith P., Heath D., Moosavi H. The Clara cell. Thorax. 1974 Mar;29(2):147–163. doi: 10.1136/thx.29.2.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Sorokin S. P. Reconstructions of centriole formation and ciliogenesis in mammalian lungs. J Cell Sci. 1968 Jun;3(2):207–230. doi: 10.1242/jcs.3.2.207. [DOI] [PubMed] [Google Scholar]
  57. Staley M. W., Trier J. S. Morphologic heterogeneity of mouse Paneth cell granules before and after secretory stimulation. Am J Anat. 1965 Nov;117(3):365–383. doi: 10.1002/aja.1001170305. [DOI] [PubMed] [Google Scholar]
  58. Terzakis J. A., Sommers S. C., Andersson B. Neurosecretory appearing cells of human segmental bronchi. Lab Invest. 1972 Jan;26(1):127–132. [PubMed] [Google Scholar]
  59. VOLK T. L., SCARPELLI D. G. ALTERATIONS OF FINE STRUCTURE OF THE RAT ADRENAL CORTEX AFTER THE ADMINISTRATION OF TRIPARANOL. Lab Invest. 1964 Oct;13:1205–1214. [PubMed] [Google Scholar]
  60. WATSON J. H., BRINKMAN G. L. ELECTRON MICROSCOPY OF THE EPITHELIAL CELLS OF NORMAL AND BRONCHITIC HUMAN BRONCHUS. Am Rev Respir Dis. 1964 Dec;90:851–866. doi: 10.1164/arrd.1964.90.6.851. [DOI] [PubMed] [Google Scholar]
  61. Walsh C., McLelland J. Intraepithelial axons in the avian trachea. Z Zellforsch Mikrosk Anat. 1974 Feb 27;147(2):209–217. doi: 10.1007/BF00582796. [DOI] [PubMed] [Google Scholar]
  62. Whur P., Gracie M. Histochemical comparison of mast cell and globule leucocyte granules in the rat. Experientia. 1967 Aug 15;23(8):655–657. doi: 10.1007/BF02144183. [DOI] [PubMed] [Google Scholar]
  63. Whur P. Relationship of globule leucocytes to gastrointestinal nematodes in the sheep, and Nippostrongylus brasiliensis and Hymenolepis nana infections in rats. J Comp Pathol. 1966 Jan;76(1):57–65. doi: 10.1016/0021-9975(66)90048-x. [DOI] [PubMed] [Google Scholar]
  64. YOFFEY J. M. The present status of the lymphocyte problem. Lancet. 1962 Jan 27;1(7222):206–211. doi: 10.1016/s0140-6736(62)91094-2. [DOI] [PubMed] [Google Scholar]
  65. van As A., Webster I. The organization of ciliary activity and mucus transport in pulmonary airways. S Afr Med J. 1972 Mar 25;46(13):347–350. [PubMed] [Google Scholar]

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