Advertisement

Protoplasma

pp 1–14 | Cite as

Cellular elements organization in the trachea of mallard (Anas platyrhynchos) with a special reference to its local immunological role

  • Doaa M. MokhtarEmail author
  • Marwa M. Hussien
Original Article
  • 45 Downloads

Abstract

Many studies have been carried out to investigate the histological structure of the trachea in many species of birds. However, the cellular organization of the trachea in the mallard duck is still unclear. This study was performed on 12 sexually mature male Mallard duck to demonstrate the cellular organization of the trachea using light and electron microscopy. The tracheal epithelium is considered the first line of defense against airborne pathogens. The mallard trachea was lined by a pseudostratified ciliated columnar epithelium that contained many morphologically distinct cell types: ciliated, non-ciliated, basal cells that encircled by a population of sub-epithelial immune cells, fibroblasts, and telocytes (TCs). Telocytes were first recorded in duck trachea in this study and showed a wide variety of staining affinity. They presented two long telopodes that made up frequent close contacts with epithelium, tracheal cartilages, and other neighboring TCs, immune cells, blood capillaries, and nerve fibers. TCs express VEGF and S-100 protein. The immune cells include mast cells, eosinophils, basophils, lymphocytes, plasma cells, and dendritic reticular cells. The ciliated tracheal epithelium was interrupted by numerous intraepithelial mucous glands and solitary goblet cells. This mucociliary apparatus constitutes the major defense mechanism against inhaled foreign materials. The cellular organization of the duck trachea and its relation to the immunity was discussed.

Keywords

Telocytes Dendritic reticular cells Immune cells Mucous glands 

Abbreviations

DC

dendritic cell

IEL

intraepithelial lymphocyte

MC

mast cells

TCs

telocytes

TEM

transmission electron microscopy

Tps

telopodes

VEGF

vascular endothelial growth factor

Notes

Acknowledgments

This work was supported by the Faculty of Veterinary Medicine, Assiut University, Egypt

Author contributions

D. M. Mokhtar performed the electron-microscopical study, immunohistochemistry, analyzed the results, and contributed to preparing and reviewing the paper. M. M. Hussein collected the samples, performed the histological and histochemical study, analyzed the results, and contributed in preparing and reviewing the paper. The authors contributed equally to this work.

Compliance with ethical standards

Ethical approval and consent to participate

The study was approved by the Ethics Committee of Assiut University, Egypt.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

References

  1. AL-Mussawy AM, AL-Mehanna NH, AL-Baghdady EF (2012) Histological study of the trachea in indigenous male turkey Meleagris gallopava. AL-Qadisiya J Vet Med Sci 11:2–15Google Scholar
  2. Alon T, Hemo I, Itin A, Pe’er J, Stone J, Keshet E (1995) Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat Med 1:1024–1028PubMedCrossRefPubMedCentralGoogle Scholar
  3. Bancroft JD, Gamble M (2002) Theory and practice of histological and histochemical techniques, 3rd edn. Churchill LivingstoneGoogle Scholar
  4. Bentz P-G (1985) Studies on some urban Mallard Anas platyrhynchos populations in Scandinavia. Part I: causes of death, mortality and longevity among Malmö Mallards as shown by ringing recoveries. Fauna Norvegica, Series C 8:44–56Google Scholar
  5. Bergelson JM (2003) Virus interactions with mucosal surfaces: alternative receptors, alternative pathways. Curr Opin Microbiol 6:386–391PubMedCrossRefPubMedCentralGoogle Scholar
  6. Bergelson JM (2009) Intercellular junctional proteins as receptors and barriers to virus infection and spread. Cell Host Microbe 5:517–521PubMedCrossRefPubMedCentralGoogle Scholar
  7. Cretoiu SM, Popescu LM (2014) Telocytes revisited. BioMol Concepts 5:353–369PubMedCrossRefPubMedCentralGoogle Scholar
  8. Dawicki W, Marshall JS (2007) New and emerging roles for mast cells in host defence. Curr Opin Immunol 19:31–38PubMedCrossRefPubMedCentralGoogle Scholar
  9. Donato R, Cannon BR, Sorci G, Riuzzi F, Hsu K, Weber DJ, Geczy CL (2013) Functions of S100 proteins. Curr Mol Med 13:24–57PubMedPubMedCentralCrossRefGoogle Scholar
  10. Elmberg J (2009) Are dabbling ducks major players or merely noise in freshwater ecosystems? A European perspective, with references to population limitation and density dependence. Wild fowl 2:9–23Google Scholar
  11. Erle DJ, Pabst R (2000) Intraepithelial lymphocytes in the lung. A neglected lymphocyte population. Am J Respir Cell Mol Biol 22:398–400PubMedCrossRefPubMedCentralGoogle Scholar
  12. Evans MJ, Van Winkle LS, Fanucchi MV, Plopper CG (1999) The attenuated fibroblast sheath of the respiratory tract epithelial–mesenchymal trophic unit. Am J Respir Cell Mol Biol 21:655–657PubMedCrossRefPubMedCentralGoogle Scholar
  13. Galli SJ, Maurer M, Lantz CS (1999) Mast cells as sentinels of innate immunity. Curr Opin Immunol 11:53–59PubMedCrossRefPubMedCentralGoogle Scholar
  14. Giemsa G (1904) Eine Vereinfachung und Vervollkommnung meiner Methylenblau-Eosin-Färbemethode zur Erzielung der Romanowsky-Nocht’schen Chromatinfärbung. Centralblatt für Bakteriologie I Abteilung 32:307–313Google Scholar
  15. Godfrey RWA, Severs NJ, Jeffrey PK (1992) Freeze–fracture morphology and quantification of human bronchial epithelial tight junctions. Am J Respir Cell Mol Biol 6:453–464PubMedCrossRefPubMedCentralGoogle Scholar
  16. Goto E, Kohrogi H, Hirata N, Tsumori K, Hirosako S, Hamamoto J, Fujii K, Kawano O, Ando M (2000) Human bronchial intraepithelial T lymphocytes as a distinct T cell subset: their long-term survival in SCID-Hu chimeras. Am J Respir Cell Mol Biol 22:4–14CrossRefGoogle Scholar
  17. Green AJ, Elmberg J (2014) Ecosystem services provided by water birds. Biol Rev 89:105–122PubMedCrossRefPubMedCentralGoogle Scholar
  18. Green KJ, Simpson CL (2007) Desmosomes: new perspectives on a classic. J Invest Dermatol 127:2499–2515PubMedCrossRefPubMedCentralGoogle Scholar
  19. Herard AL, Zahm JM, Pierrot D (1996) Epithelial barrier integrity during in vitro wound repair of the airway epithelium. Am J Respir Cell Mol Biol 15:624–641PubMedCrossRefPubMedCentralGoogle Scholar
  20. Hiemstra PS (2001) Epithelial antimicrobial peptides and proteins: their role in host defence and inflammation. Paediatr Respir Rev 2:306–310PubMedPubMedCentralGoogle Scholar
  21. Hsu SM, Raine L, Fanger H (1981) Use of avidin- biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577–580PubMedCrossRefPubMedCentralGoogle Scholar
  22. Hussein MM, Mokhtar DM (2018) The roles of telocytes in lung development and angiogenesis: an immunohistochemical, ultrastructural, scanning electron microscopy and morphometrical study. Dev Biol 443:137–152PubMedCrossRefPubMedCentralGoogle Scholar
  23. Huxley TH (1971) A manual of the anatomy of vertebrated animals. J. & A. Churchill, LondonGoogle Scholar
  24. Kaestner KH (2019) The intestinal stem cell niche: a central role for Foxl1-expressing subepithelial telocytes. Cell Mol Gastroenterol Hepatol 8:111–117PubMedPubMedCentralCrossRefGoogle Scholar
  25. Karnovsky MJ (1965) A formaldehyde-glutraldehyde fixative of high osmolarity for use in electron microscopy. Cell Biol 27:1A–149ACrossRefGoogle Scholar
  26. Keawcharoen J, Riel DV, Amerongen GV, Bestebroer T, Beyer WE, Lavieren RV, Osterhaus A, Fouchier R, Kuiken T (2008) Wild ducks as long-distance vectors of highly pathogenic avian influenza virus (H5N1). Emerg Infect Dis 14(4):600–607PubMedPubMedCentralCrossRefGoogle Scholar
  27. King AS, Mclelland J (1984) Birds. Their structure and function, 2nd edn. Bailliere Tindall, LondonGoogle Scholar
  28. Lali M, Ibrahim AL (1984) Scanning and transmission electron microscopy of normal chicken tracheal epithelium. Poult Sci 63:1425–1431CrossRefGoogle Scholar
  29. Lap ae Silva JR, Jones JA, Cole PJ, Poulter LW (1989) The immunological component of the cellular inflammatory infiltrate in bronchiectasis. Thorax 44(8):668–673CrossRefGoogle Scholar
  30. Lbe CS, Onyeanusi BI, Salami SO, Umosen AD, Maidawa SM (2008) Studies of the major respiratory pathways of the West African guinea fowl (Numida meleagris galeata): The Morphometric and Macroscopic Aspects. Int J Poult Sci 7(10):997–1000CrossRefGoogle Scholar
  31. McConnell RE, Higginbotham JN, Shifrin DA, Tabb DL, Coffey RJ, Tyska MJ (2009) The enterocyte microvillus is a vesicle-generating organelle. J Cell Biol 185(7):1285–1298PubMedPubMedCentralCrossRefGoogle Scholar
  32. McNamara PS, Flanagan BF, Selby AM, Hart C, Smyth RL (2004) Pro- and anti-inflammatory responses in respiratory syncytial virus bronchiolitis. Eur Respir J 23:106–112PubMedCrossRefPubMedCentralGoogle Scholar
  33. McNamara PS, Flanagan BF, Hart CA, Smyth RL (2005) Production of chemokines in the lungs of infants with severe respiratory syncytial virus bronchiolitis. J Infect Dis 191:1225–1232PubMedCrossRefPubMedCentralGoogle Scholar
  34. Mokhtar DM, Hussein MM (2019) Morphological characteristic and functional dependencies of dendritic cell in developing rabbit lung during fetal and neonatal life. Dev Biol 454:29–43PubMedCrossRefPubMedCentralGoogle Scholar
  35. Mukherjee A, Morosky SA, Shen L, Weber CR, Turner JR, Kim KS, Wang T, Coyne CB (2009) Retinoic acid-induced gene-1 (RIG-I) associates with the actin cytoskeleton via caspase activation and recruitment domain-dependent interactions. J Biol Chem 284:6486–6494PubMedPubMedCentralCrossRefGoogle Scholar
  36. Nash H (2007) Respiratory system of birds: anatomy and physiology. Pet Edu. com Drs. Foster & Smiths source for expert pet informationGoogle Scholar
  37. Nicholas BP, Skipp R, Mould S, Rennard DE, Davies CD, O’Connor R, Djukanovic R (2006) Shotgun proteomic analysis of human induced sputum. Proteomics 6:4390–4401PubMedPubMedCentralCrossRefGoogle Scholar
  38. Olah I, Nagy N (2013) Retrospection to discovery of bursal function and recognition of avian dendritic cells; past and present. Dev Comp Immunol 41:310–315PubMedCrossRefPubMedCentralGoogle Scholar
  39. Pingel H (2011) Waterfowl production for food security. Lohmann Infromat 46(2):32Google Scholar
  40. Popescu LM, Ciontea SM, Cretoiu D, Hinescu ME, Radu E, Ionescu N, Ceausu M, Gherghiceanu M, Braga RI, Vasilescu F, Zagrean L, Ardeleanu C (2005) Novel type of interstitial cell (Cajal-like) in human fallopian tube. J Cell Mol Med 9:479–523PubMedPubMedCentralCrossRefGoogle Scholar
  41. Pourlis A, Siasios A, Grivas I (2018) Morphology of the tracheal epithelium in the quail (Coturnix coturnix japonica). Asian J Anim Vet Adv 13:301–304CrossRefGoogle Scholar
  42. Reece WO (2005) Avian respiratory system morphology. In: Function Anatomy and Physiology of Domestic Animals, 3rd (ed.) edn. Lippincott Williams and Wilking, pp 230–268Google Scholar
  43. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Cell Biol 17:208–212CrossRefGoogle Scholar
  44. Roche W, Montefort RS, Baker J, Holgate ST (1993) Cell adhesion molecules and the bronchial epithelium. Am Rev Respir Dis 148:S79–S82PubMedCrossRefPubMedCentralGoogle Scholar
  45. Rusu MC, Jianu AM, Mirancea N, Didilescu AC, Mănoiu VS, Păduraru D (2012) Tracheal telocytes. J Cell Mol Med 16(2):401–405PubMedPubMedCentralCrossRefGoogle Scholar
  46. Söderquist P, Elmberg J, Gunnarsson G (2013) Longevity and migration distance differ between wild and hand-reared mallards Anas platyrhynchos in Northern Europe. Eur J Wildl Res 59:159–166CrossRefGoogle Scholar
  47. St John AL, Rathore AP, Yap H, Metcalfe DD, Vasudevan SG, Abraham SN (2011) Immune surveillance by mast cells during dengue infection promotes natural killer (NK) and NKT-cell recruitment and viral clearance. Proc Natl Acad Sci U S A 108:9190–9195PubMedPubMedCentralCrossRefGoogle Scholar
  48. Sun QW, Li S, Wang R, Han DD, Li DR, Ding Y, Yue Z (2009) Evidence for a role of mast cells in the mucosal injury induced by Newcastle disease virus. Poult Sci 88:554–561PubMedCrossRefPubMedCentralGoogle Scholar
  49. Tasbas M, Hazıroğ RM, Lu AC, O¨zcan Z (1986) A study on anatomical and histological structures of tongue and the upper respiratory passages (larynx cranialis, trachea, syrinx) in the penguin. Vet J Ank Univ 33:240–261Google Scholar
  50. Tasbas M, Hazırog RM, Lu AC, O¨zer M (1994) Morphological investigations of the respiratory system of the Denizlicock. II. Larynx, trachea, syrinx. Vet J Ank Univ 41:135–153Google Scholar
  51. Thurmon JC, Tranquilli WJ, Benson GJ (1996) Lumb & Jones Veterinary Anesthesia, 3rd edn. Lea & Febiger, LondonGoogle Scholar
  52. Vareille M, Kieninger E, Edwards MR, Regamey N (2011) The airway epithelium: soldier in the fight against respiratory viruses. Cin Microbiol Rev 24:210–229CrossRefGoogle Scholar
  53. Von Garnier C, Nicod LP (2009) Immunology taught by lung dendritic cells. Swiss Med Wkly 139:186–192Google Scholar
  54. Voynow JA, Rubin BK (2009) Mucins, mucus, and sputum. Chest 135:505–512PubMedCrossRefGoogle Scholar
  55. Witczak P, Brzezińska-Błaszczyk E (2012) Mast cells in viral infections. Postepy Hig Med Dosw 66:231–241CrossRefGoogle Scholar
  56. Ximena M, Bustamante-Marin LE (2018) Ostrowski cold spring harb cilia and mucociliary clearance. Perspect Biol 9:a028241Google Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Anatomy and Histology, Faculty of Vet. MedicineAssiut UniversityAsyutEgypt

Personalised recommendations