Reconstructions of Centriole Formation and Ciliogenesis in Mammalian Lungs

Abstract

This study presents reconstructions of the processes of centriolar formation and ciliogenesis based on evidence found in electron micrographs of tissues and organ cultures obtained chiefly from the lungs of foetal rats. A few observations on living cultures supplement the major findings. In this material, centrioles are generated by two pathways. Those centrioles that are destined to participate in forming the achromatic figure, or to sprout transitory, rudimentary (primary) cilia, arise directly off the walls of pre-existing centrioles. In pulmonary cells of all types this direct pathway operates during interphase. The daughter centrioles are first recognizable as annular structures (procentrioles) which lengthen into cylinders through acropetal deposition of osmiophilic material in the procentriolar walls. Triplet fibres develop in these walls from singlet and doublet fibres that first appear near the procentriolar bases and thereafter extend apically. When little more than half grown, the daughter centrioles are released into the cytoplasm, where they complete their maturation. A parent centriole usually produces one daughter at a time. Exceptionally, up to 8 have been observed to develop simultaneously about 1 parent centriole. Primary cilia arise from directly produced centrioles in differentiating pulmonary cells of all types throughout the foetal period. In the bronchial epithelium they appear before the time when the ciliated border is generated. Fairly late in foetal life, centrioles destined to become kinetosomes in ciliated cells of the epithelium become assembled from masses of fibrogranular material located in the apical cytoplasm. Formation of these centrioles may be under the remote influence of the diplosomal centrioles. More certainly, the precursor material accumulates in close proximity to Golgi elements. Within the fibrogranular areas, osmiophilic granules (400-800Å) increase in size and eventually become consolidated into dense spheroidal bodies (deuterosomes), which organize the growth of procentrioles around them. When mature, the newly formed centrioles become aligned in rows beneath the apical plasma membrane. There each centriole produces satellites from its sides, a root from its base, and a cilium from its apex. Early stages in the formation of both primary cilia and those of the ciliated border are similar. In developing cilia of the ciliated border, however, the outer ciliary fibres rapidly reach the tips of the elongating shafts, and a central pair of fibres is formed (9 + 2 arrangement). In primary cilia, development of the fibres seems to lag behind the elongation of the shafts, and only the outer ciliary fibres appear (9 + 0 arrangement). The strengths and weaknesses of the proposed reconstructions of centriolar formation and ciliogenesis are discussed, and the occurrence in other living forms of similar pathways for centriolar formation is noted. Further discussion leads to an interpretation of the centriole as a semi-autonomous organelle whose replicative capacity is separable from the characteristic triplet fibre structure of its wall.