Tracheobronchial epithelium in the adult rhesus monkey: A quantitative histochemical and ultrastructural study

Abstract

Previous studies of the intrapulmonary conducting airways of sheep and rabbit have demonstrated marked diversity in the epithelial populations lining them. Because studies of trachea and centriacinar regions of macaque monkeys suggested that primates may be even more diverse, the present study was designed to characterize the epithelial population throughout the airway tree of one primate species, the rhesus monkey. Trachea and intrapulmonary airways of the right cranial and middle lobes of glutaraldehyde/paraformaldehyde-infused lungs of five adult rhesus monkeys were microdissected following the axial pathway. Each branch was assigned a binary number indicating its specific location within the tree. The trachea and six generations of intrapulmonary airway from the right cranial lobe were evaluated for ultrastructure and quantitative histology as were those of the right middle lobe for quantitative carbohydrate histochemistry. Four cell types were identified throughout the tree: ciliated, mucous goblet, small mucous granule, and basal. The tallest epithelium lined the trachea; the shortest, the respiratory bronchiole. The most cells per unit length of basement membrane were in proximal intrapulmonary bronchi; the least, in the respiratory bronchiole. The nonciliated bronchiolar epithelial or Clara cell was restricted to respiratory bronchioles. Sulfomucins were present in the vast majority of surface goblet cells in the trachea and proximal bronchi. In proximal bronchi, neutral glycoconjugates predominated in glands and acidic glycoconjugates in surface epithelium. In terminal and respiratory bronchioles the ratio of acidic glycoconjugate to neutral glycoconjugate equaled that in proximal bronchi, although glands were not present. Sulfomucins were minimal in terminal airways. We conclude that the characteristics of the epithelial lining of the mammalian tracheobronchial airway tree are very species-specific. The lining of the rhesus monkey does not have the diversity in cell types in different airway generations observed in sheep and rabbit. Also, the populations lining these airways in the rhesus are very different from either the sheep or rabbit in number, proportions of different cell types, glycoconjugate content, and distribution of specific cell types.

Distribution of Clara cell secretory protein expression in the tracheobronchial airways of rhesus monkeys

“…Other investigators have reported colocalization of CCSP and mucins (8,30) in the human lung similar to what we report here in the monkey. These findings suggest CCSP expression in rhesus monkey airway epithelium is outside the classic lineage defined by TEM in distal airways by Plopper et al (23,24). When comparison is made of airways throughout the tracheobronchial tree that are identified by their branching history, immunoreactive CCSP was detected throughout the intrapulmonary airway tree from the lobar bronchus to the respiratory bronchioles.…”

An Official Research Policy Statement of the American Thoracic Society/European Respiratory Society: Standards for Quantitative Assessment of Lung Structure

“…Further subsampling may be necessary to reduce small airway samples to a practicable number. Alternatively, microdissection can be used to define and localize samples to airway generations (34,159).…”

Persistence of Serotonergic Enhancement of Airway Response in a Model of Childhood Asthma

“…Rhesus monkeys were used because they have similar lung cellular morphology, airway architecture, and immunology and undergo a similar extensive period of postnatal development compared with humans (35)(36)(37)(38)(39). In addition to possessing all of the components of the intrapulmonary conducting airways that are altered in humans with asthma, rhesus monkeys display a similar progression of asthma pathophysiology and symptoms (11,40).…”