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MOLECULAR, CELLULAR, AND DEVELOPMENTAL BIOLOGY |
Department of Animal Sciences, 1151 Lilly Hall, Purdue University, West Lafayette, IN 47907-1151
2 Corresponding author: applegt{at}purdue.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: chicken • duck • turkey • small intestine • tight junction
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The intestinal epithelium contains a terminal bar on the apical end that consists of tight junctions (zonula occludens), intermediate junctions (zonula), and desmosomes (macula adherens; Anderson and Cereijido, 2001; Schneeberger and Lynch, 2001). The tight junctions serve as a regulated barrier in the intercellular space and maintain a fence between the apical and basolateral domains of the plasma membrane of the cell (Anderson, 2001; Schneeberger and Lynch, 2001). The protein composition of tight junctions includes claudins and occludins. The tight junctions form a flat meshwork of filaments that completely surround the basolateral side of the cell (Anderson and Cereijido, 2001). Anderson and Cereijido (2001) report 90% of substances (ions, nutrients, etc.) are absorbed via paracellular transport through pores with radii 0.003 to 0.004 µm in size. The transport of these substances is regulated by tight junctions discriminating against different ions depending on the surrounding pH. The meshwork pattern of the tight junction belt compartmentalizes the opening of specific channels via anastomosed strands increasing the junctional resistance (Gonzalez-Mariscal et al., 2001). The electrical resistance within a tissue can be a measurement of tight junction soundness. A leaky epithelium resistance can vary by 100,000-fold compared with a tight epithelium (Anderson, 2001).
Studies have shown enteric pathogens and the virulence factors associated with them can change the functionality of tight junctions (Sears, 2000). Kohler et al. (2003) reviews the potential ways the epithelial tight junction can be influenced by pathogenic microbes. The claudin proteins, for example, can be modified by pathogen-derived factors resulting in an epithelial cell line in which claudin-4 has been removed from the cell surface or the dephosphorylation of occludin proteins can occur. In either case, increased permeability of tight junctions occurs.
Bayer et al. (1975) evaluated the duodenum, jejunum, and ileum villi in 1 and 7 d posthatch broiler chicks using scanning electron microscopy. The scanning electron microscopy micrographs of the day-old chick display epithelial crevices and disruptions in the duodenum and jejunum villi surfaces. The epithelium discontinuities may be natural or artifacts from the dehydration and embedding process of the tissues. Bayer et al. (1975) did not theorize on the presence or address the potential implications of the epithelial disruptions. The crevices on the villi surface may be similar in function to the mammalian counterparts in the young neonate allowing for the passage of undigested proteins and other nutritional factors. However, the size and period of time in which the epithelial disruption is present within the chick is unknown. Adverse effects of not having a complete barrier upon placement of a flock could include either rapid transfer of pathogenic microorganisms or foodborne pathogens into circulation of the young bird.
Therefore, transmission electron microscopy was used to evaluate the tight junction formation and epithelial cell morphology in the developing small intestinal segments of the chicken, duck, and turkey. Although transmission electron microscopy will not allow the surface image of the villi to be observed, insight into formation of the tight junctions during incubation and after hatch may begin to explain the relationship to the epithelial crevices observed by Bayer et al. (1975).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Sample Processing
Five time periods were selected to evaluate tight junction formation within the jejunum with day of hatch evaluating all 3 intestinal segments. Thick sections (2.0 µm) from 1 bird per time point were cut and mounted on glass slides stained with 1% toluidine blue and 1% borate to identify the area where thin sections would be cut. After further block-trimming, thin sections (70 to 90 nm) with silver to gold interference colors were sectioned on an ultramicrotome using a 3.5-mm diamond knife (Micro Star Technologies, Huntsville, TX). Sections were mounted on Formvar, carbon-coated 100 mesh copper grids, and stained with 2% uranyl acetate and lead citrate.
Sample Measurement and Analysis
Samples were evaluated using an FEI/Philips CM-10 biotwin Transmission Electron Microscope (FEI/Philips, Hillsboro, OR) operated at 80 kV, identifying the area of interest. Only villi with attachment to the basolateral membrane were evaluated with pictures taken of the tight junctions between adjacent epithelial cells located in the bottom of the crypt and the top portion of the villus tip. Four micrographs were taken of tight junctions in the crypt and villus tip for a total of 8 observations per intestinal segment at each time point. Adobe Photoshop (Adobe Systems Inc., San Jose, CA) was used to scan negatives into the computer and to measure cell perimeter and tight junction length. The 1,200x magnification was used to measure the cell area, whereas the 20,000x magnification measured tight junction length. Identifying the tight junction locations between epithelial cells, the corresponding enterocytes involved in the tight junction were located with the perimeter outlined. Tight junction measurements were taken from the apical membrane where the tight junction began and stopped at the desmosome. For consistency, the tight junction was defined as involving the tight junction and intermediate junction. Micrographs from the crypt and villus tip were used to measure the microvilli. Six to 8 individual microvilli were measured from the tip of the microvillus to attachment on the enterocyte membrane. The tracings of the cell perimeter, tight junction length, and microvilli length were analyzed using Macintosh IPLab (BD Biosciences, San Jose, CA) and utilized the waffle-type grating calibration grid (Ladd Research, Williston, VT) to accurately compare measurements.
Statistical Analysis
Karcher et al. (2005) used a formula to determine the day of incubation in the duck and turkey relative to chicken incubation. The relative day of incubation (Table 1
) reported throughout the paper allows for species comparison. Data were compiled and analyzed based on the relative day of incubation. Only cells with 2 adjacent tight junction measurements were used in the analysis. Therefore, numbers of samples per tissue per species ranged from 1 to 8. The data were analyzed using the PROC MIXED function in SAS (SAS Institute, Cary, NC) incorporating species, tissue, position (crypt-villus axis), and day along with possible interactions in the model statement. Least squares means separations were corrected for multiple means comparison using the Tukey correction with significance set at P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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. Day –7 of incubation, the duck, turkey, and chicken had cell perimeters of 24.03 ± 4.51, 33.52 ± 5.16, and 44.16 ± 4.51 µm (mean ± SEM), respectively. The probability of differences due to species (P = 0.03) and day (P = 0.001) are significant for changes in epithelial cell perimeter. A difference between average cell perimeter was observed at 3 d post-hatch with the chicken enterocyte perimeter 48% larger than the duck or turkey. Although cell perimeter is changing in all 3 species during the time period, the cell perimeter is uniform (4-µm variance) across all species at day of hatch.
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with the probability of differences between species (P = 0.003) highly significant. The duck and turkey at d –7 had more of the cell involved in tight junctions then the chicken; however, by d – 4, the chicken had a 19% increase, whereas that of the duck and turkey decreased. On day of hatch, the percentage of enterocyte perimeter involved in tight junctions decreased in the duck, turkey, and chicken. The 3 d posthatch resulted in an increase of cell perimeter involved in tight junctions by 19% in the duck jejunum and 7% in the turkey jejunum. Chicken percentage of cell perimeter involved in tight junctions remained static at 11% during the posthatch period. Tight junction length measured in micrometers is displayed in Figure 3. The changes in tight junction length can be explained by species (P = 0.001). The turkey tight junction length decreased by 30% from d – 4 to 3 d posthatch, whereas the duck increased by 32% in the same period. Less than a 3% change in the cell perimeter involved in tight junctions in chickens, ducks, and turkeys (Figure 2) occurs 24 h after hatch. The cell perimeter uniformity, percentage involvement in tight junctions, and tight junction length are evidence of complete formation of tight junctions at day of hatch and perhaps barrier function in the 3 species.
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Evaluating cell perimeter (µm), probability of differences can be explained by the position of the enterocyte along the crypt-villus tip axis (P < 0.04; Table 2). Minimal differences between the crypt and villus epithelial cell perimeter are seen in the duodenum and jejunum in the 3 species. The chicken and duck have smaller epithelial cell perimeters in the ileal crypt compared with the villus tip at day of hatch.
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. The probability of differences can be explained by species, position (crypt or villus tip), and relative day of incubation along with all possible interactions among the 3 effects (P < 0.03). During the incubation period, the microvillus length is approximately 1 µm regardless of enterocyte position or species. The length of the crypt enterocyte microvillus remains comparable to incubation period lengths, whereas the villus tip enterocyte microvillus increases during the post-hatch period. By 3 d posthatch, the duck continues to see an increase in villus tip enterocyte microvillus length, whereas the chicken and turkey decrease to lengths found in the crypt.
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. The probability of species, tissue, and position (crypt or villus tip) as well as all interactions (P < 0.0001) can explain the differences observed. The enterocyte microvillus length in the crypts is shorter than microvillus length on the villus tip at day of hatch in all 3 segments of the small intestine and in all 3 species.
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to 10 are representative micrographs of the changing small intestine in the duck. The chicken and turkey had similar observations (data not shown) in the morphology of the intestinal enterocyte. The developing jejunum at d – 7 of incubation (Figure 5) represents the developing villi. The arrow points to a division within the crypts that will lead to a new rank of villi. The inset picture reveals the organization of the epithelium. Figure 6 is a high-magnification picture of the crypt labeling the intact tight junction, desmosome, and nucleus of an enterocyte. The duck jejunum at –4 d of incubation (Figure 7) identifies the attachment of the epithelial cell to the basal membrane with the nuclei basally located within the cell. The mitochondria are clustered toward the apical end, and the desmosomes and tight junctions are identifiable between enterocytes. At day of hatch, the duck ileum has a well-defined microvillus border (Figure 8). The goblet cells can be identified on the surface of the villus as well as migrating from the basal membrane toward the lumen. Tight junctions and mitochondria are identifiable easily defining individual enterocytes. The nuclei are basally located within the cells, and the dark, dense material within the nucleus is the nucleolus. Tight junctions are intact by day of hatch and are easily identified within the duck jejunum at d 1 and 3 posthatch (Figures 9 and 10)
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The evaluation of the tight junction as a percentage of the epithelial cell in the final days of incubation and initial days posthatch in the chicken, duck, and turkey is interesting (Figure 2
). The low percentage of cell membrane involved in tight junction formation for the chicken at all time points except d – 4 of incubation may represent either of the following: 1) the epithelium of the chicken is more developed with tight junction length (Figure 3) established early in incubation, or 2) the changing cell size during the final days of embryogenesis will dictate the percentage of the cell membrane involved in formation of the tight junction (Figure 1). The rapid increase at d – 4 is likely due to an anomaly, because only 1 cell had both sides of the tight junction measured. Therefore, the chicken mean on d – 4 does not accurately represent what is occurring during incubation. Eliminating the data point, the change in cell perimeter is greater in the duck and turkey than chicken. More likely, the cell perimeter during the final days of incubation and initial days post-hatch in the chicken is more consistent than the epithelial cells in the duck and turkey.
The parallel decrease in cell perimeter involved in tight junctions during the final days of incubation and increase after hatch in the duck and turkey is not as consistent between proliferating cells as compared with the chicken in the same time period. The measured cell perimeters had a range of 10 µm posthatch in the chicken and 20 µm in the duck and turkey, suggesting cell perimeter posthatch is more tightly controlled in the chicken. The observation of the amount of proliferating cell nuclear antigen-positive cells located along the villus by Moon and Skartvedt (1975) and Uni et al. (2000) suggest the rapid proliferation of the enterocytes in the first day after hatch results in the observed larger ranges of cell perimeter with more variation in the duck and turkey compared with the chicken. Applegate et al. (1999) demonstrated that the turkey poult enterocytes do not change migration rate just before or during the first week after hatching. Additionally, the percentage of proliferating enterocytes is much greater at hatch than 5 d posthatch, because absolute number of proliferating enterocytes does not change during this time.
To investigate the potential for intestinal segment differences as well as location differences along the crypt-villus axis, the percentage of cell perimeter involved in tight junction formation, cell perimeter size, and tight junction length at day of hatch was measured. No apparent pattern is obvious across species to explain cell perimeter differences between the crypt and villus tip position, but the probability of position to explain differences is significant (Table 2; P < 0.04). The chicken had larger enterocytes in the crypt compared with the villus tip in all 3 intestinal segments. The duck had the opposite observation, with the crypt having smaller enterocytes than the villus tip. With no significant differences in tight junction length or percentage of cell perimeter involved in tight junctions, the orchestrated development of the epithelium at day of hatch appears to be tightly regulated, although selection pressure and evolutionary differences have dictated the overall intestinal growth and maturation of these species.
The changes in the microvilli from the incubation period to posthatch have been reported by several researchers. Penttila and Gripenberg (1969) evaluated the intestinal structure of the developing chick duodenum. The microvilli have a spotty presence, with little morphological difference between 10- and 15-d enterocytes. The change in microvilli structure was reported by Overton and Shoup (1964) from d 16 to 20 of incubation with the observation that microvilli are shortest in length in the crypt and increase in length as the enterocyte migrates up the villus. Observations of the microvillus length (Figure 4) support and contradict Overton and Shoup (1964). The chicken microvillus in the crypt is longer than the villus tip until day of hatch when the microvillus length increases dramatically in the villus tip. The duck and turkey have longer microvillus on the villus tip than the crypt during the time period. The differences between Overton and Shoup (1964) observations with the current study may stem from the difference of intestinal segments evaluated (duodenum vs. jejunum).
Evaluating the 3 intestinal segments at day of hatch (Table 3) revealed the enterocyte microvillus in the crypt is shorter than the microvillus on the villus tip. The differences between position on the crypt-villus axis occurred in all 3 species. Mamajiwalla et al. (1992) reviewed the development of the chicken intestinal epithelium reporting the changes to the microvillus structure. As the enterocyte progresses up the villi from the crypt, the microvilli lengthen by membrane addition to the microvillus base. The change in the microvillus length is not surprising, because the proteins composing the brush border membrane are constantly renewed, requiring several hours to be turned over.
The interactions among species, day, and position (Figure 4) or species, tissue segment, and position (Table 3) to explain microvillus development are complicated. The body growth among the 3 species posthatch may be influenced by the length and position of microvilli along the crypt-villus tip axis dictating the uptake of nutrients. In Figure 4, the chicken and turkey microvillus length is decreasing by d 3 posthatch, whereas the duck increases, potentially contributing to the rapid body growth in the duck compared with the chicken and turkey posthatch. At day of hatch, the chicken has the longest microvillus length in the small intestinal segments, with the duck having the shortest length. The capability of increased nutrient digestion and absorption would appear to favor the chicken based on surface area of the microvillus with the duck being limited. Therefore, evaluating the interactions of microvillus development begin to convey the complexity of development.
Figures 5 to 10 depict the development of the duck small intestine during the incubation and posthatch period. Grey (1972) reports the presence of 5 ranks of developing villi, with the first 4 progressing through 3 major phases. Phase 1 occurs from d 11 to 15 of incubation. The lumen is composed of 4 distinct ridges and 4 less-distinct ridges with the developing villi present in irregular zigzag patterns. The apical surfaces of the villi are studded with short, stubby microvilli, and by d 15, the 4 ranks are identical in height, width, and a uniform zigzag pattern. Phase 2 occurs from d 15 to 17 of incubation with major changes including more prominent folding of previllus ridges with angles of the folds more acute. The contortion of the ridge broadens the base for future villi development with uniformity across the ranks of villi being lost at d 17. Finally, phase 3 occurs from d 17 to 19 of incubation. This phase is marked with true villus formation. The presence of a distinct population of cells appears on the villus crest with dense concentrations of microvilli and single-cell boundaries not easily discernible. The villi begin to develop as projections above the previllus ridges with the 4 ranks of villi growing rapidly. By d 19, the villi are first recognizable as finger-like. The fifth rank of villi originate on d 16. The villi arise from the lumen floor parallel to earlier ranks with the new villi bases later joining the ridges. The fifth-rank villi exhibit rapid growth and are prominent among the first 4 ranks of villi by d 18 to 19 of incubation. Day 19 to 20, the crest of the villi develop bulb-like swelling and by day of hatch resemble the earlier ranks. Four days after hatch, the 5 different ranks of villi cannot be differentiated within the small intestine. Uni et al. (2003) reported a similar phenomenon with 3 types of villi being identified in the last 4 d of incubation in the chicken small intestine. In fact, the description of the villi types correspond to the ranks of villi described by Grey (1972).
Figure 5 shows the presence of the first 4 ranks of villi with the origination of the fifth rank in the duck at d – 7 of incubation. The protruding bud of the fifth rank can be observed in the crypt (arrow), confirming that the formation of villi ranks occurs in the 3 avian species evaluated. The inset picture is a representative shot of the developing villi and crypt. Figure 6 identifies the nucleus, tight junction, and desmosome, which appear similar in all 3 species and were identified by Humphrey and Turk (1974) and Hodges and Michael (1975) within the chicken. Figure 7 is the duck jejunum at d – 4 before hatch surveying the enterocytes in the crypt. The nuclei are basally located in the enterocyte with the organelles arranged toward the apical end of the enterocyte. The enterocytes are attached to the basal membrane and are rectangular in appearance. Humphrey and Turk (1974) evaluated the enterocyte morphology of 4- to 7-wk-old broilers reporting the basally located nuclei and presence of organelles in the apical end of the cell. Hodges and Michael (1975) reported similar findings in 5-wk-old Leghorn chickens. Therefore, the ultrastructure of the enterocyte does not dramatically change in the final days of incubation to several weeks posthatch.
The abundance of mitochondria observed in the apical end of the enterocytes throughout the studied time period coincides with observations reported by Humphrey and Turk (1974) and Hodges and Michael (1975). In the current study, different types of mitochondria are present during the studied time points, such as rod-like, oval-shaped, and tadpole-type mitochondria (bud-like protrusion extending from the main body), as was also described by Yamauchi et al. (1992). By d 3 posthatch, all types of mitochondria were still present (Figure 10). Yamauchi et al. (1992) reported the changing of mitochondria types from day of hatch to 60 d posthatch. The suggestion has been made that different mitochondria types are responsible for differing metabolic rates with tadpole-type mitochondria having the highest rates. Future evaluation of mitochondria type within the enterocyte during incubation and posthatch growth would allow for a more accurate assessment of metabolic efficiency and functionality.
Figure 8 has 2 goblet cells identified in the ileum of the duck at day of hatch, one at the apical end of the villus tip and the other not yet exposed to the luminal side. Esmail (1988) used scanning electron microscopy to evaluate the intestinal morphology of 22-wk-old chickens and the importance of goblet cells. The duodenum had plate-like villi with a large number of goblet cells, whereas the jejunum and ileum had leaf-like villi. The jejunum had the greater amount of goblet cells compared with the ileum. The ratio for the segments was 6:2:1 estimated for the 3 segments (goblet cells per unit of intestine). The higher goblet cell number in the duodenum serves to produce mucins to form a barrier as well as buffering the acidic chyme. Lower goblet cell number in jejunum and ileum reduces the barrier layer thickness, increasing digestion and absorption.
The appearance of the goblet cell in the ileum located below several enterocytes might imply the extrusion of immature enterocytes at day of hatch. Because the avian embryo must switch from a lipid energy source to a carbohydrate energy source, the replacement of the epithelium with mature adult enterocytes would ensure the young neonate has the appropriate enzymes available. A similar phenomenon occurs in the mammalian epithelium (Trahair and Sangild, 2002). However, Penttila and Gripenberg (1969) investigated the chicken duodenum during the incubation period, finding the morphogenesis of the villi proceeded with the appearance of various enterocyte enzyme patterns. Some of these enzymes were alkaline and acid phosphotases, adenosine triphosphotase, monoamine oxides, glucose-6-phosphotase, and Leu aminopeptidase. The increase of enzyme activity along with the morphological change of the villi suggests the maturation of the enterocytes occurs in the final days of incubation before exposure to exogenous nutrient sources.
The abundant dispersion of lipid droplets (Figure 8) in the duck ileum at day of hatch was seen in the turkey and chicken, although not as inundated in the latter species. Noble and Cocchi (1990) discuss the role of lipid metabolism in the neonatal chick. During the incubation period of the chick, 80% of the yolk lipid content is mobilized and absorbed by embryonic tissues. At day of hatch, 25 to 30% of DM content of the whole embryo is lipid. During the incubation period of the 3 avian species, the lipid droplet size appears to remain the same, but at day of hatch, an accumulation of lipid is seen in the ileal tissue. A few lipid droplet inclusions are seen in the duodenum and jejunum of the 3 species, but not to the extent of the lipid accretion in the ileum. Biologically, the ileal segment is distal to the yolk sac, so lipid uptake in the small intestine at day of hatch will occur in the ileal tissue. The dramatic decrease in size and abundance observed in the ileal villus 1 d posthatch indicates a rapid mobilization and utilization of the lipid from the ileal tissue by the young neonate.
The ability of the small intestine to form a barrier relies both upon the production of mucin by the goblet cells as well as the tight junction formation between the enterocytes. The demand on the epithelium to continuously replenish while maintaining a solid barrier is counterintuitive. Watson et al. (2005) evaluated the murine small intestine epithelium in vivo. The epithelial layer was found to be discontinuous, interrupted by gaps where enterocytes were sloughed resulting in the loss of the apical brush border membrane, cytosol, and nucleus. However, the epithelial cells lost had not progressed to an entirely apoptotic state, raising the question why it would be exuviated. Based upon observations and calculations, approximately 3% of the epithelial layer along the crypt-villus axis lacks a cell. However, the presence of an unidentified fluid filling these gaps suggests other mechanisms besides tight junctions are in place to aid in maintaining barrier function. If this similar phenomenon is present within the bird, the formation of the tight junctions is vital for helping to control nutrient absorption and maintenance of a barrier function. However, the epithelial disruptions observed by Bayer et al. (1975) may not have negative connotations to the overall barrier function of the small intestine.
Overall, the morphological development in the small intestine enterocytes among the chicken, duck, and turkey is consistent. Occasional differences exist in epithelial cell perimeter in the final days of incubation but by 1 d post-hatch are very similar. The amount of the cell membrane involved in the tight junction is more consistent in the chicken than the duck and turkey during the incubation and posthatch time period evaluated. The tight junctions appear to be established by day of hatch, with little change in cell perimeter 24 h later. The tight junction architecture is likely complete at this point in time, but the lack of evaluation of the intestinal tissues for barrier functionality remains to be evaluated. Observations made among the 3 species in respect to organelle position, changes in enterocyte structure, and accumulation of lipid is consistent across the species and agrees with prior research. Evaluation of the barrier function in relation to changes of the tight junction needs to be completed to understand the integrity of the epithelium as a barrier in the final days of incubation and initial posthatch period.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Received for publication August 17, 2007. Accepted for publication November 7, 2007.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Anderson, J. M., and M. Cereijido. 2001. Introduction: Evolution of ideas on the tight junction. Pages 1–18 in Tight Junctions. 2nd ed. M. Cereijido and J. Anderson, ed. CRC Press, Boca Raton, FL.
Applegate, T. J., J. J. Dibner, M. L. Kitchell, Z. Uni, and M. S. Lilburn. 1999. Effect of turkey (Meleagridis gallopavo) breeder hen age and egg size on poult development. 2. Intestinal villus growth, enterocyte migration and proliferation of the turkey poult. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 124:381–389.[CrossRef]
Bayer, R. C., C. B. Chawan, F. H. Bird, and S. D. Musgrave. 1975. Characteristics of the absorptive surface of the small intestine of the chicken from 1 day to 14 weeks of age. Poult. Sci. 54:155–169.[Web of Science][Medline]
Burgess, D. R. 1975. Morphogenesis of intestinal villi. II. Mechanism of formation of previllous ridges. J. Embryol. Exp. Morphol. 34:723–740.[Web of Science][Medline]
Burgess, D. R. 1976. Structure of the epithelial–mesenchymal interface during early morphogenesis of the chick duodenum. Tissue Cell 8:147–158.[CrossRef][Web of Science][Medline]
Esmail, S. H. 1988. Scanning electron microscopy of intestinal villous structures and their putative relation to digestion and absorption in chickens. Reprod. Nutr. Dev. 28:1479–1487.[Medline]
Farhadi, A., A. Banan, J. Fields, and A. Keshavarzian. 2003. Intestinal barrier: An interface between health and disease. J. Gastroenterol. Hepatol. 18:479–497.[CrossRef][Web of Science][Medline]
Gheri, G., and S. Gheri Bryk. 1987. Computerized morphometric analysis of the chick embryo ileum organogenesis. Z. Mikrosk. Anat. Forsch. 101:1011–1022.[Web of Science][Medline]
Gonzalez-Mariscal, L., A. Avila, and A. Betanzos.2001. The relationship between structure and function of tight junctions. Pages 89–120 in Tight Junctions. 2nd ed. M. Cereijido and J. Anderson, ed. CRC Press, Boca Raton, FL.
Grey, R. D. 1972. Morphogenesis of intestinal villi. I. Scanning electron microscopy of the duodenal epithelium of the developing chick embryo. J. Morphol. 137:193–213.[CrossRef][Web of Science][Medline]
Hodges, R. D., and E. Michael. 1975. Structure and histochemistry of the normal intestine of the fowl. III. The fine structure of the duodenal crypt. Cell Tissue Res. 160:125–138.[Web of Science][Medline]
Humphrey, C. D., and D. E. Turk. 1974. The ultrastructure of normal chick intestinal epithelium. Poult. Sci. 53:990–1000.[Web of Science][Medline]
Karcher, D. M., J. P. McMurtry, and T. J. Applegate. 2005. Developmental changes in amniotic and allantoic fluid insulin-like growth factor (IGF)-I and -II concentrations of avian embryos. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 142:404–409.[CrossRef][Medline]
Kohler, H., B. A. McCormick, and W. A. Walker. 2003. Bacterialenterocyte crosstalk: Cellular mechanisms in health and disease. J. Pediatr. Gastroenterol. Nutr. 36:175–185.[CrossRef][Web of Science][Medline]
Konarzewski, M., C. Lilja, J. Kozlowski, and B. Lewonczuk. 1990. On the optimal growth of the alimentary tract in avian postembryonic development. J. Zool. 222:89–101.[Web of Science]
Lim, S. S., and F. N. Low. 1977. Scanning electron microscopy of the developing alimentary canal in the chick. Am. J. Anat. 150:149–173.[CrossRef][Web of Science][Medline]
Mamajiwalla, S. N., K. R. Fath, and D. R. Burgess. 1992. Development of the chicken intestinal epithelium. Curr. Top. Dev. Biol. 26:123–143.[Web of Science][Medline]
Moon, H. W., and S. M. Skartvedt. 1975. Effect of age on epithelial cell migration in small intestine of chickens. Am. J. Vet. Res. 36:213–215.[Web of Science][Medline]
Noble, R. C., and M. Cocchi. 1990. Lipid metabolism and the neonatal chicken. Prog. Lipid Res. 29:107–140.[CrossRef][Web of Science][Medline]
Noy, Y., and D. Sklan. 2001. Yolk and exogenous feed utilization in the posthatch chick. Poult. Sci. 80:1490–1495.
Overton, J., and R. Meyer. 1984. Aspects of liver and gut development in the chick. Scan. Electron Microsc. 11:737–746.
Overton, J., and J. Shoup. 1964. Fine structure of cell surface specializations in the maturing duodenal mucosa of the chick. J. Cell Biol. 21:75–85.
Penttila, A., and J. Gripenberg. 1969. Fine structure and enzyme histochemistry of developing duodenal epithelium of the chicken. Z. Anat. Entwicklungsgesch. 129:109–127.[CrossRef][Web of Science][Medline]
Schneeberger, E. E., and R. D. Lynch. 2001. Ultrastructure and immunolabeling of the tight junction. Pages 19–38 in Tight Junctions. 2nd ed. M. Cereijido and J. Anderson, ed. CRC Press, Boca Raton, FL.
Sears, C. L. 2000. Molecular physiology and pathophysiology of tight junctions. V. Assault of the tight junction by enteric pathogens. Am. J. Physiol. Gastrointest. Liver Physiol. 279:G1129–G1134.
Sell, J. L., C. R. Angel, F. J. Piquer, E. G. Mallarino, and H. A. al-Batshan. 1991. Developmental patterns of selected characteristics of the gastrointestinal tract of young turkeys. Poult. Sci. 70:1200–1205.[Web of Science][Medline]
Trahair, J. F., and P. T. Sangild. 2002. Stuyding the development of the small intestine: Philosophical and anatomical perspectives. Pages 1–54 in Biology of the Intestine in Growing Animals. 1st ed. R. Zabielski, P. C. Gregory, and B. Westrèom, ed. Elsevier, Boston, MA.
Uni, Z., A. Geyra, H. Ben-Hur, and D. Sklan. 2000. Small intestinal development in the young chick: Crypt formation and enterocyte proliferation and migration. Br. Poult. Sci. 41:544–551.[CrossRef][Web of Science][Medline]
Uni, Z., E. Tako, O. Gal-Garber, and D. Sklan. 2003. Morphological, molecular, and functional changes in the chicken small intestine of the late-term embryo. Poult. Sci. 82:1747–1754.
Watson, A. J., S. Chu, L. Sieck, O. Gerasimenko, T. Bullen, F. Campbell, M. McKenna, T. Rose, and M. H. Montrose. 2005. Epithelial barrier function in vivo is sustained despite gaps in epithelial layers. Gastroenterology 129:902–912.[CrossRef][Medline]
Yamauchi, K., S. Iida, and Y. Isshiki. 1992. Post-hatching developmental changes in the ultrastructure of the duodenal absorptive epithelial cells in 1, 10 and 60-d-old chickens, with special reference to mitochondria. Br. Poult. Sci. 33:475–488.[CrossRef][Web of Science][Medline]
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), duck (
), and turkey (•) jejunal epithelial cell perimeter (µm) comparisons during incubation and the posthatch period. Main effects of species (P = 0.03) and day (P = 0.001) are significant. Error bars indicate SEM.
