The purpose of this article is to review our knowledge to date of collagen-proteoglycan interaction. Many topics have been taken into account in order to provide a reasonably complete picture of this highly complex subject. Basic information about collagen biology, and an overview of the current concepts and advances regarding proteoglycans, have served as a basis to elucidate collagen-proteoglycan interaction.
The bases of some methods of study have been reviewed in order to provide a fuller understanding of the results that are cited in this article.
The experimental models and biological examples discussed herein demonstrate that collagen-proteoglycan interaction is essential to the extracellular matrix resiliency. The organization of these macromolecules is critical: collagen molecules become assembled into fibrils, fibrils aggregate to form fibers, fibers associate into bundles of fibers, and proteoglycans in the ground substance play a major role in the ordering process; on the other hand, glycosaminoglycans (GAGs) are composed of repeating monomers—GAGs linked to a same protein core form a proteoglycan—which, in turn, may bind to a hyaluronic acid molecule to form a proteoglycan aggregate together with other proteoglycans. Further growth of these complex macromolecules at higher hierarchical levels occurs by interaction of collagen with proteoglycans.
A striking correlation between the tissue distribution of the genetically-distinct types of interstitial collagen and the occurrence of the different GAGs (which argues strongly in favour of a specific interaction) is demonstrated comprehensively in this review. Tissues composed of collagen type I possess small amounts of proteoglycans which contain almost exclusively dermatan sulfate; while tissues containing only collagen type II have high amounts of chondroitin sulfates. Collagen type III is the major fibrillary constituent of tissues that possess intermediate levels of proteoglycans, which contain great amounts of heparan sulfate.
The histochemical and ultrastructural equivalents of these interactions have been emphasized in order to permit an interpretation of the morphologic aspects that can contribute to distinguishing these macromolecular components when studying tissue sections either under the light microscope or by aid of electron microscopy.

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Cells of erythrocytic series in the human liver obtained from 109 embryos 28 to 49 days after ovulation and 76 fetuses between 8 to 22 weeks of gestation were investigated by light and electron microscopy. Antisera against fetal hemoglobin (Hb-F) were used in the immuno-peroxidase method to identify erythroblasts in the embryonic and fetal liver.
Immunoperoxidase staining for Hb-F revealed that most of the hemopoietic cells found in fetal hepatic parenchyma were erythrocytic in nature. The cells of the erythrocyte series consisted of large immature cells which were usually invaginating into the cytoplasm of hepatocytes, and small mature erythroblasts which tended to gather in the subendothelial spaces of the sinusoids.
The early hepatic erythroid progenitor cells observed in the intercellular spaces of the hepatocytes until 10 weeks of gestation (the early stage of hepatic hemopoiesis) distinctly differed in ultrastructure from the late hepatic erythroid progenitor cells which appeared after 10 weeks of gestation (the late stage of hepatic hemopoiesis).
These findings indicate that the progenitor cells of the erythrocytic series and the hemopoietic stem cells in the early stage of hepatic hemopoiesis are morphologically different from those in the late stage, and that the cells of erythrocytic series in the liver in the early stage differ in the course of maturation from those in the late stage.

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Presumptive hemopoietic stem cells in the human liver obtained from 109 embryos 28 to 49 days after ovulation and 76 fetuses between 8 and 22 weeks of ovulation were investigated by light and electron microscopy.
Presumptive hemopoietic stem cells in the human embryonic liver are concluded to be a series of cells that show a variegated ultrastructure. They are classified into four subtypes (type I, II, III and IV). Presumptive hemopoietic stem cells of type I are thought to differentiate from the undifferentiated mesenchymal cells that are derived from the septum transversum. Presumptive stem cells of type I, II and III transitorily appear in the liver during the early stage of hepatic hemopoiesis, and cannot be detected in late stages. With the development of the fetus, presumptive stem cells of the type IV, however, gradually increase in number. The cells of megakaryocytic, granulocytic and erythrocytic lineages originate from the presumptive stem cells of type II in the early stage of hepatic hemopoiesis, whereas the cells of the three lineages originate from the presumptive stem cells of type IV in the late stage. The presumptive hemopoietic stem cells of type IV are surmised as corresponding to the pluripotent hemopoietic stem cells (CFU-S) in laboratory animals or pluripotent hemopoietic progenitors in human bone marrow (CFU-mix).

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The resorption surface caused by osteoclasts are identified by scanning electron microscopy (SEM), but the morphological interrelation between these resorption surfaces and Howship's lacunae observed by light microscopy remains obscure, and little evidence showing that the distribution and structures of the resorption surface change according to the function of osteoclasts is available. To understand the relationship between the function of osteoclasts and the morphological evidence of bone resorption, surface structures of the parietal bones in mice, newborn to adult, were studied by SEM. The osteoclasts on the inner surface of the calvaria are considered to be involved in the growth of the skull.
The outer surface of the parietal bone was smooth, whereas the inner surface consisted of both smooth and rough areas. The rough areas were usually much larger than Howship's lacunae, which are generally thought to be of osteoclast size. These areas were composed of small and shallow concavities with oval or polygonal outlines. The borders between adjacent concavities appeared as ridges. The rough areas were very wide in the growing skull and osteoclasts were scattered on these wide rough areas. The osteoclasts were much larger than the concavities in the rough areas. During the growth of the skull, the proportion of rough areas occupying the inner surface changed parallel to the number of osteoclasts, which varied in correspondence with the growth rate of the skull. The maximum value of the proportion was about 60% at 1 week of age.
The findings suggest that the osteoclasts resorb the bone by moving along its surface, forming small concavities and leaving rough areas larger than Howship's lacunae of osteoclast size. Furthermore, they suggest that the size and distribution of the rough areas and the morphological features of the concavities in the rough areas vary depending upon the activities of the osteoclasts.

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Parotid and submandibular glands in human fetuses at 16, 18 and 24 weeks of gestation were studied by electron microscopy. The salivary glands of the 16 week fetus were composed of primary ducts and terminal buds. The primary duct was double layered and consisted of inner glycogen-rich ductal cells and outer myopeithelial preurscor cells. The terminal bud was a cell cluster which consisted of glycogen-rich ductal precursor cells and myoepithelial precursor cells. In the 18 week fetus, the terminal bud developed into the terminal tubule, and the formation of a lumen was evident. The terminal tubule was composed of ductal cells containing a few secretory granules and immature myoepithelial cells at the basal portion of the tubule. The differentiation of secretory activity was clearly visible in the terminal tubule of the salivary glands in the 24 week fetus. In the parotid gland of the 24 week fetus, one kind of secretory cell was found, but at the same stage, two kinds of secretory cells were distinguishable in the submandibular gland. Some mature myoepithelial cells were distinctly observed in both glands. At this stage, also, immature intercalated ducts and immature striated ducts were present. The relationship between the histogenesis of normal structures and that of tumors is also discussesed.

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The development of Ito cells in the chick embryo liver was studied using electron as well as fluorescence microscopes.
The collagen fibrils in the Disse's space can already be seen in 6-day-old chick embryos. This space contains fibroblast-like cells which should be called primitive Ito cells. They are slender cells characterized by numerous free polyribosomes. The rough endoplasmic reticulum, Golgi apparatus and 10nm microfilaments are also well developed.
The fluorescence of vitamin A and lipid droplets begin to appear in the primitive Ito cell at 9 days of incubation in both the control and vitamin A-treated animals. A special topographic relation between the lipid droplets and cell organelles is difficult to recognize. The primitive Ito cell in the Disse's space acquires the ability to produce collagen fibrils earlier than that of taking up and storing vitamin A. The Ito cells containing lipid droplets increase in number with embryonic age, and about 40-50% of perisinusoid cells have droplets of vitamin A at 21 days of incubation. The droplets are usually less than 1μm in diameter and do not fuse with each other.

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Segi's cap, a large aggregation of basal-granulated cells at the top of the intestinal villus, was studied in the proximal small intestine of bovine fetuses by histological, immunohistochemical and ultrastructural techniques. 1) Typical Segi's caps were seen in the duodenum and proximal jejunum in bovine fetuses. 2) Smaller groups of basal-granulated cells were found in the villous and partly also in the cryptal epithelium, as well as in the subepithelial lamina propria. The possible mechanism for their occurrence was discussed in connection with the fate of the cap. 3) Segi's caps were present in a neonatal calf before the suckling stage, but not in 3 or 4 week-old calves. The process of and reason for this abrupt disappearance of the caps are unknown. 4) The Segi's cap in bovine fetuses consisted mainly of argyrophil cells as demonstrated by Grimelius' and Hellerström-Hellman's silver methods. Only a few argentaffin cells were found in fetal caps using a modified Masson-Hamperl's silver method. 5) Immunohistochemically, somatostatin-, gastrin-, motilin- and secretin-immunoreactive cells were identified. 6) Four different endocrine cell types could be distinguished in the bovine Segi's cap on the basis of the ultrastructural appearance of their secretory granules.

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Cellular and ultrastructural localization of catecholamines in the dog carotid body was investigated by peroxidase-antiperoxidase method for light microscopy and by protein A-colloidal gold technique for electron microscopy, and compared with that of preproenkephalin A-related opioid peptides, i. e., Met-enkephalin-Arg⁶-Phe⁷ (Met-Enk-Arg-Phe) and Met-enkephalin-Arg⁶-Gly⁷-Leu⁸ (Met-Enk-Arg-Gly-Leu). Immunocytochemistry at the light microscopic level using consecutive semi-thin sections of Araldite-embedded tissue showed that some 30% of the chief cells contained immunoreactive noradrenaline together with Met-Enk-Arg-Phe and Met-Enk-Arg-Gly-Leu. A considerable number of chief cells exhibited immunoreactivities representing one or two of these three kinds of substances. A few chief cells showed none of the specific immunoreactivities. Immunoreactive adrenaline was not demonstrated in any cells of the dog carotid body. At the electron microscopic level, co-existence of noradrenaline with Met-Enk-Arg-Phe or Met-Enk-Arg-Gly-Leu in the same secretory granules was shown using the double labeling protein A-colloidal gold technique. Possible interactions of catecholamines and opioid peptides deserve consideration for the understanding of the chief cell's role in the carotid body chemoreceptor.

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