2Center for Oral Biology, Aab Institute of Biomedical Sciences, and 3Department of Pediatrics, University of Rochester, Rochester, NY 14642, USA
Received on May 13; revised on August 3, 2000; accepted on August 3, 2000.
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Abstract |
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Key words: O-glycosylation/mouse development/in situ hybridization/ UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferases/epithelial-mesenchymal interactions
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Introduction |
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Prior work has focused largely on the roles played by N-linked glycans during development. Tunicamycin, an inhibitor of N-linked glycosylation, disrupts gastrulation of sea urchins (Heifetz and Lennarz, 1979) and compaction and blastocyst formation in mice (Surani, 1979
; Atienza-Samols et al., 1980
). Changes in the expression or activity of glycosyltransferases during ontogeny have been documented (e.g., Armant et al., 1986
; Granovsky et al., 1995
; Ong et al., 1998
; Fan et al., 1999
; Liu et al., 1999
). Inactivation of mouse gene Mgat1, which encodes the glycosyltransferase required to convert N-linked oligosaccharides from high-mannose precursors to their complex forms, resulted in embryonic lethality by day 10.5 (Ioffe and Stanley, 1994
; Metzler et al., 1994
). To circumvent the early embryonic lethal phenotype, Ioffe et al. (1996)
followed embryonic stem cells with an inactivated Mgat1 allele in chimeric embryos. They determined that the mutated cells did not contribute to the formation of an organized layer of bronchial epithelium, leading to the speculation that complex N-glycans are required for some aspect of cellcell recognition during the epithelialization of the lung. Mutant embryos were underdeveloped and displayed cellular disorganization of many tissues, but the timing of death, and the phenotype are most consistent with lethality due to a vascular or circulatory defect.
Recently, the role of proteoglycans in development has been explored in genetically tractable organisms (Perrimon and Bernfield, 2000). Cell surface heparan proteoglycans have been demonstrated to be essential for normal fibroblast growth factor (FGF) receptor signaling during development of Drosophila. Mutation in either the sugarless (sgl) or sulfateless (sfl) genes results in defects in the migration of mesodermal and tracheal cells during embryogenesis (Lin et al., 1999
). These genes encode UDP-glucose dehydrogenase (which is required for the formation of glucuronic acid) and heparin/heparan sulfate N-deacetylase/N-sulfotransferase respectively (specifically needed for formation of heparan sulfate). A recent study has identified the division abnormally delayed (dally) gene as a putative substrate for these enzymes (Lin et al., 1999
); dally encodes a glycosyl-phosphatidyl inositol (GPI)-linked glypican.
The products of three genes, sqv-3, sqv-7, and sqv-8, are required for proper vulval invagination in C.elegans (Herman and Horvitz, 1999). The protein product of sqv-3 is related to vertebrate ß1,4 galactosyltransferases; the predicted protein product of sqv-8 appears to encode a ß1,3 glucuronyltransferase; and the protein product of sqv-7 is similar to a family of nucleotide-sugar transporters. It is proposed that the sqv genes encode components of a glycosyltransferase pathway that are required to assemble a saccharide necessary for vulval invagination.
Other forms of O-glycans appear to play a role during metazoan development. Mutations in the rotated abdomen (rt) locus in Drosophila melanogaster affect muscle development and caused a clockwise helical rotation of the body (Martin-Blanco and Garcia-Bellido, 1996). The rt gene encodes a protein which has extensive homology to the yeast proteins PMT1 and PMT2 which are known O-mannosyltransferases. Recently, the human orthologue of the rt gene, POMT1, was identified and RNA blot analysis showed the transcript encoding the product of this gene was highly expressed in heart and skeletal muscle (Jurado et al., 1999
).
-dystroglycan, which is part of the dystrophinglycoprotein complex of muscle, has recently been demonstrated to be decorated with O-mannosyl-containing oligosaccharides (Chiba et al., 1997
). Based on inhibition studies, the O-mannosylated oligosaccharides have been implicated in
-dystroglycan-laminin interactions. Thus one possibility is that the disruption of the rt locus leads to a loss of O-mannosylation of muscle complex glycoproteins, thereby compromising muscle and body development.
In higher eukaryotes, mucin type O-glycosylation is a posttranslational event in which oligosaccharides are built step-wise. A family of enzymes, termed UDP-GalNAc:polypeptide N-Acetylgalactosaminyltransferases (ppGaNTases, EC 2.4.1.41) is responsible for the initiation of O-glycosylation; N-acetylgalactosamine (GalNAc) is transferred from the sugar donor, UDP-GalNac, in anomeric linkage to a serine or threonine of the polypeptide backbone (GalNAc
1-O-Ser/Thr). As an initial step to understand the potential roles in which this enzyme family is involved in development, we have investigated the expression pattern of seven ppGaNTases using in situ hybridization to mRNAs with in vitro transcribed, transcript-specific RNA probes. All family members whose function had been validated when these studies were initiated were chosen for examination (ppGaNTase-T1, -T2, -T3, -T4, -T5, -T7, and -T9). Several stages during murine development were studied to determine the expression patterns during development in a variety of organ systems. We show that the ppGaNTases examined each accumulate in an unique spatial and temporal pattern. These patterns indicate that this gene family may be involved in the development of multiple organ systems characterized by epithelial/mesenchymal interactions during their organogenesis. Additionally, several ppGaNTases are expressed in unique patterns in the brain, indicating involvement in development of nervous tissue.
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Results |
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Expression of ppGaNTases in developing tooth and mandible
ppGaNTase-T5 message accumulates specifically in a subset of mesenchyme at E12.5 when that tissue contains odontogenic potential (Figure 3A,B). Serial section analysis indicates expressing cells include subsets of both dental and non-dental mesenchyme (not shown). ppGaNTase-T5 expressing cells are located where a subset of cells of neural crest origin are at this stage (Chai et al., 2000). At E14.5, ppGaNTase-T5 expression is markedly reduced and ppGaNTase-T9 mRNA accumulates in neural crest cells destined to become both bone and tooth in the mandible. In contrast, ppGaNTase-T1 accumulates at higher levels in the subset of neural crest cells forming the bone, but not the tooth of the mandible (Figure 3F). The expression patterns of ppGaNTase-T9 and ppGaNTase-T1 are more spatially restricted in the developing tooth and mandible than ppGaNTase-T2 (Figure 3H and Figure 1).
Expression of ppGaNTase mRNAs in other organ systems in which epithelialmesenchymal interactions occur during development
pGaNTase-T1 accumulates in most cell types in the developing lung except airway epithelial cells of the segmented bronchi (Figure 4). ppGaNTase-T2 is more restricted to mesenchymal cells, whereas ppGaNTase-T3 is expressed in a small subset of cells whose location is consistent with neural epithelial bodies (Figure 4). All seven ppGaNTase family members examined were expressed in E16.5 intestinal epithelial cells, although at varying abundance (Figure 5 and Figure 1, E16.5). Only ppGaNTase-T2 was additionally expressed in the smooth muscle layer (Figure 5C). Similarly, expression of all seven ppGaNTases examined was detected at varying levels in E16.5 submandibular/sublingual salivary gland (Figure 6 and Figure 1, E16.5). ppGaNTase-T2 is expressed abundantly in both acinar cells and duct cells (Figure 6B). ppGaNTase-T7 and -T9 are expressed predominantly in acinar cells (Figure 6D and 6F).
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Discussion |
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The overall pattern of expression for this family of enzymes strongly indicates that ppGaNTases are not merely involved in the biosynthesis of mucin-glycoproteins as an end-product for an organ. For example, while all isoforms are clearly expressed in developing submandibular gland by E16.5 (corresponding to Theiler stage 25), the quantity of salivary mucin at this stage of development accounts for only 0.01% of the total gland protein. This is in contrast to the adult gland in which the mucin makes up 1.2% of the total protein (Denny et al., 1989). Thus, it is likely that this enzyme family is responsible for the synthesis of other O-glycans at this stage of development.
Cranial neural crest cells contribute to a variety of tissues including the intramembranous bones of the craniofacial complex and portions of the teeth (Le Douarin, 1982; Chai et al., 2000
) Peanut agglutinin (PNA), a lectin which specifically recognizes the mucin core disaccharide Galß1,3 GalNAc (Lotan et al., 1975
), has been used in numerous studies to probe for the presence of O-glycans during development. In Drosophila, peanut agglutinin labels the developing nervous system (Callaerts et al., 1995
). Later in Drosophila development peanut agglutinin also reacts with the lumen of the hindgut, salivary glands, and the Malpighian tubules (Callaerts et al., 1995
). No evidence for either fucose or sialic acid was observed in developing Drosophila. In contrast, peanut agglutinin fails to stain condensing mesenchyme associated with either developing nasal cartilage or Meckels cartilage within the mandible (Sasano et al., 1992
; Zschabitz et al., 1995
) of developing mice. However, following neuraminidase digestion, several studies report PNA reactivity in these developing craniofacial structures (Slack, 1985
; Louryan and Glineur, 1991
; Zschabitz et al., 1995
; Miyake et al., 1996
; as cited in Zschabitz, 1998
). Presumably, one or more of the ppGaNTases localized to neural crest cells and other developing structures observed in the present study are involved in the assembly of O-glycans. The future challenge lies in identifying the substrates which are decorated with O-glycans and then determining what functional role each glycosylated substrate plays during embryogenesis.
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Materials and methods |
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ppGaNTase-T1 transcripts were detected using the plasmid pBSmT1-IS. pBSmT1-IS contains nucleotides 13761676 of the mouse ppGaNTase-T1 amino acid coding region generated by PCR amplification using the primers mT1insitu+ (d(ATAGGTACCAAGCTTGTCATGGTATGGGAGGTAATCAGG)) and mT1insitu- (d(ATAGAGCTCGAGAATATTTCTGGAAGGGTGACAT)); the PCR product was cloned into the KpnI and SacI sites of pBluescript KS+.
ppGaNTase-T2 transcripts were detected using the plasmid pBSmT2-IS. pBSmT2-IS contains nucleotides 13651670 of the mouse T2 amino acid coding region. It was generated by PCR amplification using primers mT2IS-S (d(ATAGGTACCAAGCTTCTGCCTCGACACTTTGGGACACT)) and mT2IS-AS (d(ATAGAGCTCGAGGCCACACACCTCCACGCTTAGGC)); the PCR product was cloned into the KpnI and SacI sites of pBluescript KS+.
ppGaNTase-T3 transcripts were detected using the plasmid pBSmT3-IS. pBSmT3-IS contains nucleotides 16331874 of the mouse T3 amino acid coding region (Zara et al., 1996). It was generated by PCR amplification using primers mT3insitu(2)+ (d(ATAGGTACCAAGCTTCGAGTATTCTGCTCAGCGTGAA)) and mT3insitu (2)- (d(ATAGAGCTCGAGTTGGAGTAGATCTGTTGCGTCAT)); the PCR product was cloned into the KpnI and SacI sites of pBluescript KS+.
ppGaNTase-T4 transcripts were detected using the plasmid pBSmT4-IS. pBSmT4-IS contains nucleotides 14831714 of the mouse T4 amino acid coding region (Hagen et al., 1997). It was generated by PCR amplification using primers mT4IS+ (d(ATAGGTACCAAGCTTCAGATTCAATTCCGTGACTGAA)) and mT4IS-(d(ATAGAGCTCGAGCTGGTTTTTATCAAGGGCATC)); the PCR product was cloned into the KpnI and SacI sites of pBluescript KS+.
ppGaNTase-T5 transcripts were detected using the plasmid pBSmTB-IS. pBSmTB-IS contains a 212 bp region of the mouse T5 cDNA corresponding to nucleotides 25422754 of the rat T5 amino acid coding region (Ten Hagen et al., 1998). It was generated by PCR amplification using primers mTBKelIS-S (d(ATAGGTACCAAGCTTGTGTGGCGCCCATCCCTGATA)) and mTBKelIS-AS (d(ATAGAGCTCGAGGTGGTTCCGTCGGGTTACAAGCAG)); the PCR product was cloned into the KpnI and SacI sites of pBluescript KS+.
ppGaNTase-T7 transcripts were detected using the plasmid pBSrT7-IS. pBSrT7-IS contains nucleotides 17591964 of the rat T7 gene (Ten Hagen et al., 1999). It was generated by PCR amplification using primers mT5IS+ (d(ATAGGTACCAAGCTTGACCAAGGGACCCGACGGATCC) and mT5IS- (d(ATAGAGCTCGAGGATGTTATTCATCTCCCACTTCT-GAT); the PCR product was cloned into the KpnI and SacI sites of pBluescript KS+.
ppGaNTase-T9 transcripts were detected using the plasmid pBSrTa-IS. pBSrTa-IS contains nucleotides 199381 of the rat ppGaNTase-T9 amino acid coding region (Ten Hagen et al., unpublished observations). It was generated by PCR amplification using the primers mTAIS+ (d(ATAGGTACCAAGCTTGCTGAACAAAGGCTGAAGGA) and mTAIS- (d(ATAGAGCTCGAGAGAGCGATTCAGGGAGATT); the PCR product was cloned into the KpnI and SacI sites of pBluescript KS+.
Single-stranded RNA antisense and sense 33P-labeled probes were prepared with specific activities of 45 x 109 d.p.m./µg.
In situ hybridization
In situ hybridization was performed using a modification of procedures described by Wilkinson and Green (1990), and as described by McGrath et al. (1999)
. Embryos were collected from outbred ICR mice (Taconic, Germantown, NY) strain. Noon the day vaginal plugs were detected was designated as day 0.5 of gestation, post coitus (pc). Mice were anesthetized with C02 prior to cervical dislocation. Mouse embryos were fixed overnight in freshly prepared ice cold 4% paraformaldehyde in PBS. The embryos were dehydrated through ethanol into xylene and embedded in paraffin using a Tissue-Tek V.I.P. automatic processor (Miles, Mishawaka, IN). Sections (5 µm) were adhered to commercially modified glass slides (Super Frost Plus, VWR, Rochester, NY), dewaxed in xylene, rehydrated through graded ethanols, treated with proteinase K to enhance probe accessibility and with acetic anhydride to reduce nonspecific background. Sections were hybridized with probes at Tm- 15°C, washed at high stringency (Tm- 7°C) and treated with RNase A to further diminish non-specific adherence of probe. Autoradiography with NBT-2 emulsion (Eastman Kodak, Rochester, NY) was performed for 25 days. Slides were developed with D19 (Eastman Kodak), and the tissue counterstained with hematoxylin. Brightfield and darkfield grayscale images were captured with a Polaroid Digital Microscope camera (Polaroid, Cambridge, MA) and processed using Adobe Photoshop (Adobe Systems, San Jose, CA) with Image Processing Toolkit (Reindeer Games, Asheville, NC). Darkfield images were pseudocolored red and overlaid on brightfield images which were pseudocolored blue.
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Acknowledgments |
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Abbreviations |
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Footnotes |
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References |
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