Cellular and subcellular events during reorientation of the palatal shelf in hamster fetuses are described. An alteration in the morphology of the epithelial and the mesenchymal cells is observed during shelf realignment from a vertical to a horizontal plane. The mesenchymal cells elongate and subsequently appear to protrude in the medially bulging palatal shelf. Microtubules, microfilaments and close contacts are associated with elongation of the mesenchymal cells. The cells of the thickened epithelium may play a mechanical role in providing direction to the mesenchymal cells during palatal shelf reorientation. The altered morphology of the mesenchymal cells may be associated with the intrinsic shelf force implicit in Walker and Fraser′s theory of palatal shelf reorientation.

Following the publication of Dursy’s study in 1869 on the development of the secondary palate, one of the much discussed questions was how the vertical palatine processes, at first separated by the tongue, are able to move up to a horizontal position. Several possibilities were suggested and disputed regarding the mechanism underlying reorientation of the palatal shelf (see Ferguson, 1978 for details). However, the mechanism still remains unclear.

A literature review of the electron microscopic observations of palatal development in rodents and human fetuses indicates that most studies were concerned with differentiation and fate of midline epithelial cells after the palatal shelves were realigned from a vertical to a horizontal plane. However, few studies describing ultrastructural aspects of both the epithelial and the mesenchymal cells during palatal shelf reorientation have been made (Walker, 1961; Babiarz, Allenspach & Zimmerman, 1975; Innes, 1978; Ferguson, 1978). These were carried out in mice and rats and the results were conflicting.

Shah & Travill (1976 a) observed that the reorientation of palatal shelves from a vertical to a horizontal plane in hamster fetuses occurred between days 12:00 and 12:04 (12 days 4 h) of gestation. They further noted that the mode of palatal shelf reorientation in hamster fetuses resembled that in humans (Anderson & Matthiessen, 1967; Aronov, 1970) and mice (Walker & Fraser, 1956; Greene & Kochhar, 1973). The purpose of the present investigation is to study cellular and subcellular events taking place at the time of change in position of the palatal shelf from a vertical to a horizontal plane in the hamster fetus. Further, an effort will be made to relate the observations of the present study to those reported in the literature to propose a hypothetical mechanism of shelf reorientation.

Maintenance and breeding of Golden Syrian hamster have been described elsewhere (Shah & Travill, 1976a). The pregnant hamsters, in a group of five, were killed at 1 h intervals between days 12:00 and 12:04 of gestation. Half the fetuses from each litter were fixed in Bouin’s solution for light microscopy and the remainder in 3% phosphate-buffered cold glutaraldehyde for electron microscopy. Fetuses for light microscopy were processed for parafin embedding. Frontal serial sections, 7 μm thick, were stained with hematoxylin and eosin. The method for processing glutaraldehyde fixed palates for electron microscopy was similar to one described by Shah & Travill (1976b). Prior to embedding, the palates were divided into anterior, middle and posterior thirds and carefully oriented to procure 1 μm frontal sections. Thin sections were obtained from the middle third of the secondary palate and stained with methanolic uranyl acetate (Stempak & Ward, 1964) followed by lead citrate (Reynolds, 1963). The sections were observed in a Philips 300 or Hitachi HU-11E-1 electron microscope.

Light microscopy

The vertical palatal shelf (Fig. 1) was composed of mesenchymal tissue covered by one to three cell layers of epithelium (Fig. 2). Examination of serial sections revealed a focal epithelial thickening on the medial aspect of the vertical shelf. The epithelial thickening was localized and was seen only in the middle third of the secondary palate. The thickening was composed of three to five layers of cells. The palatal mesenchyme was composed of stellate cells scattered in an amorphous ground substance. An occasional cell undergoing mitosis was seen in the mesenchyme. The epithelium on the medial aspect of the vertical shelf, i.e. the prospective midline epithelium that is destined to fuse and disintegrate, showed no mitotic figures.

Fig. 1

Ventral view of hamster palate at day 12:00 of gestation. Both the lower jaw and tongue are removed. The palatal shelves are in vertical position, × 16.

Fig. 1

Ventral view of hamster palate at day 12:00 of gestation. Both the lower jaw and tongue are removed. The palatal shelves are in vertical position, × 16.

Fig. 2

A vertical palatal shelf at day 12:00 of gestation showing thickening of the epithelium on its medial aspect (arrow). Epon thick section, × 76.

Fig. 2

A vertical palatal shelf at day 12:00 of gestation showing thickening of the epithelium on its medial aspect (arrow). Epon thick section, × 76.

Reorientation of the shelf from a vertical to a horizontal plane started in the middle third of the secondary palate (Fig. 3). In the frontal section, a medial bulge was observed above the area of epithelial thickening (Fig. 4). The prospective midline fusion epithelium showed no histological change from that of the vertical shelf. Some of the mesenchymal cells were, however, elongated and appeared to be polarized along the transverse axis of the medially bulging palatal shelf. Other mesenchymal cells were stellate or appeared to be undergoing elongation.

Fig. 3

Ventral view of hamster palate at day 12:02 of gestation. Both the lower jaw and tongue are removed. The palatal shelves are reorienting in the middle third but are still vertical in the posterior third, × 16.

Fig. 3

Ventral view of hamster palate at day 12:02 of gestation. Both the lower jaw and tongue are removed. The palatal shelves are reorienting in the middle third but are still vertical in the posterior third, × 16.

Fig. 4

A reorienting palatal shelf at day 12:02 of gestation. Some of the mesenchymal cells are elongated (arrows). Note the epithelial thickening (E). Epon thick section, × 52.

Fig. 4

A reorienting palatal shelf at day 12:02 of gestation. Some of the mesenchymal cells are elongated (arrows). Note the epithelial thickening (E). Epon thick section, × 52.

Subsequently, when the palatal shelf became horizontal (Fig. 5), the focal thickening of the epithelium was on its medial edge (Fig. 6). The mesenchymal cells were either stellate or elongated and resembled those of the vertical or reorienting shelf. However, as the opposing horizontal shelves approached one another toward the midline all mesenchymal cells were stellate.

Fig. 5

Ventral view of hamster palate at day 12:04 of gestation. Both the lower jaw and tongue are removed. The palatal shelves are horizontal, × 16.

Fig. 5

Ventral view of hamster palate at day 12:04 of gestation. Both the lower jaw and tongue are removed. The palatal shelves are horizontal, × 16.

Fig. 6

The horizontal palatal shelves at day 12:04 of gestation. The thickened epithelium is present on the medial edge of the shelves (arrows). Epon thick section. × 42.

Fig. 6

The horizontal palatal shelves at day 12:04 of gestation. The thickened epithelium is present on the medial edge of the shelves (arrows). Epon thick section. × 42.

Electron microscopy

The epithelium covering the medial aspect of the vertical palatal shelf (Fig. 7) was separated from the underlying mesenchyme by a continuous basal lamina. Numerous spaces were present between the epithelial cells. The superficial epithelial cells were flat. They were attached to one another and to the subjacent epithelial cells by desmosomes. They contained a flattened nucleus surrounded by polyribosomes, mitochondria, a few cisternae of rough endoplasmic reticula and bundles of to nofilaments. The basal cells were roughly cuboidal. Each contained a relatively large, oval or irregularly shaped nucleus, polyribosomes, a few cisternae of rough endoplasmic reticula, mitochondria, coated vesicles and a small Golgi complex.

Fig. 7

Electron micrograph of a vertical palatal shelf at day 12:00 of gestation. A continuous basal lamina (BL) separates the epithelium from the mesenchyme. Numerous spaces (ICS) are present between the superficial and the basal cells and between the latter. The superficial cell is characterized by a flat nucleus (N) surrounded by polyribosomes, mitochondria (M) and tonofilaments (Tf). The basal cell, in addition, contains a small Golgi complex (GC) and a few cisternae of rough endoplasmic reticula (RER). The nucleus (N) in the basal cell is irregular. The superficial cell is attached to the basal cell by desmosomes (D). × 13200.

Fig. 7

Electron micrograph of a vertical palatal shelf at day 12:00 of gestation. A continuous basal lamina (BL) separates the epithelium from the mesenchyme. Numerous spaces (ICS) are present between the superficial and the basal cells and between the latter. The superficial cell is characterized by a flat nucleus (N) surrounded by polyribosomes, mitochondria (M) and tonofilaments (Tf). The basal cell, in addition, contains a small Golgi complex (GC) and a few cisternae of rough endoplasmic reticula (RER). The nucleus (N) in the basal cell is irregular. The superficial cell is attached to the basal cell by desmosomes (D). × 13200.

The cells of focal epithelial thickening (Fig. 8) varied in their shapes. The cells near the basal lamina were generally cuboidal and those away were flat. A few spaces intervened between the cells of thickened epithelia which were otherwise attached to one another by desmosomes. The cells in thickened epithelium contained a spherical or oval nucleus surrounded by numerous polyribosomes, a small Golgi complex, few strands of rough endoplasmic reticula and mitochondria.

Fig. 8

Electron micrograph of a vertical palatal shelf at day 12:00 of gestation. Thickened epithelium. The cells near the basal lamina (BL) are cuboidal and those away are flat. Intercellular spaces (ICS) are few and the cells are attached to one another by desmosomes (D). The cells of thickened epithelium contain a spherical or oval nucleus (N), numerous polyribosomes, rough endoplasmic reticulum (RER) and mitochondria (M). × 8800.

Fig. 8

Electron micrograph of a vertical palatal shelf at day 12:00 of gestation. Thickened epithelium. The cells near the basal lamina (BL) are cuboidal and those away are flat. Intercellular spaces (ICS) are few and the cells are attached to one another by desmosomes (D). The cells of thickened epithelium contain a spherical or oval nucleus (N), numerous polyribosomes, rough endoplasmic reticulum (RER) and mitochondria (M). × 8800.

The mesenchymal cells were stellate and contained a large nucleus surrounded by few cytoplasmic organelles and a well developed Golgi complex.

During reorientation of the palatal shelf (Fig. 9), the basal lamina remained continuous. The spaces between the epithelial cells were increased both in number and size from that of the earlier stage. The basal cells appeared to have flattened as compared to that of the vertical shelf. Lysosomes appeared for the first time in both the superficial and the basal cells. Other cytoplasmic features remained unchanged.

Fig. 9

Electron micrograph of a reorienting palatal shelf at day 12:02 of gestation showing numerous intercellular spaces (ICS) in the epithelium. The basal lamina (BL) is intact. Lysosomes (Ly) are present in both the superficial and the basal cells, × 8800.

Fig. 9

Electron micrograph of a reorienting palatal shelf at day 12:02 of gestation showing numerous intercellular spaces (ICS) in the epithelium. The basal lamina (BL) is intact. Lysosomes (Ly) are present in both the superficial and the basal cells, × 8800.

The thickened epithelium on the reorienting palatal shelf (Fig. 10), on the other hand, showed a reduction in number and size of the spaces between its cells. Also the cells near the basal lamina were roughly columnar rather than cuboidal as seen on the vertical shelf. Other cells were flat. The Golgi complex was well developed. As in the other epithelial cells, lysosomes were recognized for the first time in the cells of the thickened epithelium.

Fig. 10

Electron micrograph of a reorienting palatal shelf at day 12:03 of gestation showing few intercellular spaces (ICS) (compare with Fig. 9) in the thickened epithelium. The basal cells (Bas) are roughly columnar (compare with Fig. 8). Mitochondria (M), Golgi complex (GC), rough endoplasmic reticulum (RER), nucleus (N), lysosome (Ly). × 8800.

Fig. 10

Electron micrograph of a reorienting palatal shelf at day 12:03 of gestation showing few intercellular spaces (ICS) (compare with Fig. 9) in the thickened epithelium. The basal cells (Bas) are roughly columnar (compare with Fig. 8). Mitochondria (M), Golgi complex (GC), rough endoplasmic reticulum (RER), nucleus (N), lysosome (Ly). × 8800.

The mesenchymal cells of reorienting palatal shelves were elongated (Fig. 11). The nuclei of the elongated cells were flattened. In addition, microtubules (Fig. 12) and condensation of microfilaments (13) were also present. Often two neighbouring elongated cells were attached to one another by close junctions (Fig. 14).

Fig. 11

Electron micrograph of a reorienting palatal shelf at day 12:02 of gestation. The elongated mesenchymal cells contain a flattened nucleus (N), polyribosomes and numerous cisternae of rough endoplasmic reticula (RER). × 8800.

Fig. 11

Electron micrograph of a reorienting palatal shelf at day 12:02 of gestation. The elongated mesenchymal cells contain a flattened nucleus (N), polyribosomes and numerous cisternae of rough endoplasmic reticula (RER). × 8800.

Fig. 12

Electron micrograph of a reorienting palatal shelf at day 12:03 of gestation. The elongated mesenchymal cell contains microtubules (arrows) which are oriented along the long axis of the cell, × 31000.

Fig. 12

Electron micrograph of a reorienting palatal shelf at day 12:03 of gestation. The elongated mesenchymal cell contains microtubules (arrows) which are oriented along the long axis of the cell, × 31000.

Fig. 13

Electron micrograph of a reorienting palatal shelf at day 12:03 of gestation. The elongated mesenchymal cell contains microfilaments (arrow) which are oriented along the long axis of the cell, × 32300.

Fig. 13

Electron micrograph of a reorienting palatal shelf at day 12:03 of gestation. The elongated mesenchymal cell contains microfilaments (arrow) which are oriented along the long axis of the cell, × 32300.

Fig. 14

Electron micrograph of a reorienting palatal shelf at day 12:03 of gestation. The two neighbouring mesenchymal cells are attached to one another by close junctions (arrows). Microfilaments (mf). × 28600.

Fig. 14

Electron micrograph of a reorienting palatal shelf at day 12:03 of gestation. The two neighbouring mesenchymal cells are attached to one another by close junctions (arrows). Microfilaments (mf). × 28600.

The epithelium covering the horizontal palatal shelf was separated from the subjacent mesenchyme by a continuous basal lamina. The spaces between the epithelial cells were reduced in number and size. The basal cells were roughly cuboidal. The cytoplasm showed an increase in organelles. The morphology and content of the thickened epithelium remained unchanged.

The mechanism by which the palatal shelf changes its position from a vertical to a horizontal plane is not understood. External factors such as muscular pressure by the tongue (Humphrey, 1969, 1971; Walker, 1969, 1971) and an alteration at the cranial base (Harris, 1967; Taylor, 1978) have been considered to be responsible for the shelf reorientation. However, palatal closure has been noted in human cases of aglossia and microglossia (see review by Shah, 1977) and no substantial alterations at the cranial base have been noted at the time of shelf reorientation (Hart, Smiley & Dixon, 1972; Diewert, 1974). Further, in vitro elevation of shelves has also been observed in the absence of the tongue and cranial base (Brinkley, Basehoar, Branch & Avery, 1975; Wee, Wolfson & Zimmerman, 1976). Thus both clinical and experimental observations seem to indicate that external factors may not be necessary for shelf elevations.

Walker & Fraser (1956) have suggested that reorientation of the palatal shelves by the mode of medial bulging may be due to an’intrinsic shelf force’. The nature of such a force, if any, is still undetermined. The contention that an increased acid mucopolysaccharide concentration in the palatal shelf at the time of elevation may provide the necessary internal shelf force (Walker, 1961; Larsson, 1962; Jacobs, 1964; Pratt, Goggins, Wilk & King, 1973; Ferguson, 1978) has been disputed (Nanda, 1971; Andrew & Zimmerman, 1971). Suggestions that the intrinsic shelf force may reside in the elastic fibers (Walker & Fraser, 1956; Clark, 1956) have been discarded by subsequent histochemical and ultrastructural observations in which no evidence of elastic fibers in the shelf tissue was found (Walker, 1961; Isaacson & Chaudhry, 1962; Frommer & Monroe, 1969). Suggestions that an increase in cellular proliferation within the palatal shelf tissue at the time of elevation may be the source of the shelf force (Schorr, 1908; Mott, Toto & Hilgers, 1969; Jelinek & Dostal, 1974; Nanda & Romeo, 1975) have also been disputed (Walker & Fraser, 1956; Cleaton-Jones, 1976). Indeed it has been recently indicated that such growth does not play a direct role in the shelf reorientation (Greene & Pratt, 1976).

The most recent hypothesis to explain the shelf reorientation through intrinsic mechanism is the molecular interactions of the contractile proteins, actin and myosin. These proteins are synthesized in the mesenchymal cells just prior to reorientation (Lessard, Wee & Zimmerman, 1974) and are represented by a cytoplasmic filament system (Babiarz et al. 1975; Innes, 1978). The results of the present study are in accordance with this hypothesis. In addition, our findings showed that there is an alteration in the morphology of both the mesenchymal and the epithelial cells during palatal shelf reorientation. The mesenchymal cells undergo elongation and appear to protrude into the medially bulging palatal shelf. The epithelial cells also flatten and appear to adapt themselves to the subjacent growth forces. These morphological alterations may be associated with the necessary power implicit in Walker & Fraser’s intrinsic force theory.

The alterations in the morphology of mesenchymal cells coincide with the appearance of microtubules and microfilaments. Microtubules play an important role in the determination of cell shape during organogenesis (Byers & Porter, 1964; Handel & Roth, 1971), and thus may have a similar role in elongation of mesenchymal cells. Presence of microfilaments in non-muscle cells is considered to be associated with cellular movement during morphogenesis (Wessels et al. 1971; Pichichero & Avers, 1973) since they contain contractile proteins (Goldman, Lazarides, Pollak & Weber, 1975). Ultrastructural identification of microfilaments in the elongated mesenchymal cells of the palate, as observed in the present study, may correspond to the contractile proteins identified by Lessard et al. (1974) and Krawczky & Gillon (1976) in mouse palate. Morphologically, however, they do not resemble the myofibrils described by Babiarz et al. (1975) and Innes (1978). The lack of resemblance may be due to differences in the areas of observation. In the present study observations were made in the middle third of the hard palate whereas the other authors observed the muscle cells in the posterior part of the palate. In any case, the presence of cytoplasmic filaments in palate mesenchyme may permit marshalling of internal stresses for movement of mesenchymal cells, and thus in general our results support the hypothesis that internal shelf force may reside in the mesenchymal cells of the palatal shelf.

Close contacts observed between the elongated mesenchymal cells during reorientation of the palatal shelves may also be important in generating internal shelf force since Dehaan (1963), Hay (1968) and Sanders (1973) have shown that such contacts play an important role in cellular movement during morphogenesis.

An interesting finding during the present study was occurrence of focal epithelial thickening on the medial aspect of the vertical palatal shelf. The cells in the thickening were closely packed. The reorientation of the palatal shelf started immediately above the thickened epithelium. A similar thickening of epithelium, however, has not been reported during mouse or human palatal development and its significance is, therefore, entirely speculative. The epithelial thickening may provide necessary guidance for the elongated mesenchymal cells to move into the medially bulging palatal shelf during the reorientation stage. The focal epithelial thickening could then act as a’mechanotactic’ pivot around which the mesenchymal cells can glide. Similar mechanotactic guidance has also been suggested during corneal development (Nelson & Revel, 1975).

In brief, the foregoing Results and Discussion indicate that reorientation of the hamster palatal shelf occurs through the mode of medial bulging and thus resembles that of humans and mice. A transient elongation of the mesenchymal cells, which subsequently appears to protrude in the medially bulging shelf, may be associated with generation of the intrinsic force for the palatal shelf realignment. Microtubules, microfilaments and close contacts are all associated with the morphological changes of the mesenchymal cells. The epithelial changes may be adaptive and guiding in nature.

The work was supported by a grant from the Medical Research Council of Canada. The author extends his gratitude to Mrs V. Koulouris and Miss Ruth Scheuing for their assistance.

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