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Identification of Genes Controlling Malpighian Tubule and Other Epithelial Morphogenesis in Drosophila melanogaster
Xuejun Liua, István Kissb, and Judith A. Lengyelaa Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, California 90095
b Institute of Genetics, Biological Research Center of the Hungarian Academy of Sciences, H-6701, Szeged, Hungary
Corresponding author: Judith A. Lengyel, Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, CA 90095-1606., jlengyel{at}ucla.edu (E-mail)
Communicating editor: T. SCHÜPBACH
 | ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The Drosophila Malpighian tubule is a model system for studying genetic mechanisms that control epithelial morphogenesis. From a screen of 1800 second chromosome lethal lines, by observing uric acid deposits in unfixed inviable embryos, we identified five previously described genes (barr, fas, flb, raw, and thr) and one novel gene, walrus (wal), that affect Malpighian tubule morphogenesis. Phenotypic analysis of these mutant embryos allows us to place these genes, along with other previously described genes, into a genetic pathway that controls Malpighian tubule development. Specifically, wal affects evagination of the Malpighian tubule buds, fas and thr affect bud extension, and barr, flb, raw, and thr affect tubule elongation. In addition, these genes were found to have different effects on development of other epithelial structures, such as foregut and hindgut morphogenesis. Finally, from the same screen, we identified a second novel gene, drumstick, that affects only foregut and hindgut morphogenesis.
WHILE the importance of epithelial morphogenesis in development is widely recognized, relatively little is known about its molecular basis. A few molecules, for example, members of the Rho GTPase family, have been identified that modulate the cytoskeleton and control cell shape change in culture (reviewed by 
The Malpighian tubules of the Drosophila embryo provide a useful system for investigating the genetics of epithelial morphogenesis. First, the genetic hierarchy required to establish the tubule primordia and to control their early morphogenesis has been partially elucidated. Second, the tubules constitute one of the simplest possible epithelial organs. As reviewed by
As outlined in Figure 5, the Malpighian tubules arise from the proctodeum. Overlapping expression of the tailless (tll), huckebein (hkb), fork head (fkh), and wingless (wg) genes at the posterior of the embryo is required to establish and maintain the portion of the proctodeum from which the tubules arise (
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In addition to the transcriptional regulation that defines the tubule primordia and controls early events of tubule development, cell signaling plays an important role in later steps of tubule development. Hedgehog is required for the completion of bud evagination (
To identify additional genes involved in the formation and/or morphogenesis of the Malpighian tubules, particularly genes that might regulate the cellular basis of morphogenesis (i.e., cell communication, cytoskeleton, cell junctions, and polarity), we screened a collection of lethal lines carrying P-element insertion(s) on the second chromosome (
| MATERIALS AND METHODS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Fly stocks:
We screened the collection of lethal lines with P-element insertion(s) on the second chromosome described by
Screen for mutants affecting Malpighian tubule and midgut morphogenesis:
We screened a total of 1819 lethal lines for defects in morphology of the mature Malpighian tubule by looking for abnormalities in formation of the opaque uric acid deposits that are observable in mature tubules (
Antibody staining and phenotypic analysis:
Antibody staining was performed using standard protocols (
Genetic analysis:
Information on the localization of the P element(s) in the identified lines was obtained from the Berkeley Drosophila Genome Center. The deficiency "kit" for the second chromosome from the Bloomington Drosophila Stock Center was used to localize a number of the lethal mutations from the screen. In addition, two multiply marked second chromosomes, S Sp Tft N-2G Pu and al dp b pr c px sp, were used for meiotic mapping of alleles of wal and drm, respectively. Revertant chromosomes were generated from line k14036 (wal) by P-element excision as described by
| RESULTS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Identification of seven loci affecting epithelial morphogenesis:
From a screen of over 1800 lethal lines (see MATERIALS AND METHODS), 8 lines were identified that produced lethal embryos with abnormal Malpighian tubules and various additional defects in epithelial maintenance and morphogenesis. On the basis of complementation tests among these lines and with other previously known genes and deficiencies, as well as P-element mapping and reversion studies, these 8 lines are concluded to correspond to seven loci, as described below.
Although each line contains one or two P-element insertion(s) on the second chromosome, in only three out of eight lines did the P-element map position correspond to the map position of the mutant locus giving the phenotype (see MATERIALS AND METHODS; Table 1). For lines k05115 and k14014, construction of transheterozygotes with deficiencies uncovering the site of the P insertion gave embryos with the same phenotype as homozygotes. Complementation analysis revealed that k05115 is a P-element insertion in faint little ball (flb;
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For the remaining lines, deficiencies uncovering the P insertion(s) complemented the P insert chromosomes in lethality and failed to yield embryos with defects characteristic of the homozygous line (Table 1). In a number of cases, additional complementation tests between these lines and the deficiency "kit" for the second chromosome, as well as characterization of specific defects in embryogenesis, suggested candidate genes mapping to sites different from that of the P-element insertion. In this way, four lines, k04221, k01302/k07336, and k03703, were shown to carry alleles of three previously identified genes (Table 1). k04221 is an allele of faint sausage (fas;
Two previously undescribed loci were identified. One of these has been named walrus (wal), for the head defects seen in cuticle preparations of the mutant larvae. We conclude that wal maps at the site of the P-element insertion in line k14036 on the basis of the following. First, the wal phenotype is reverted by P-element excision. Second, k14036 does not complement another lethal line, l(2)02516, which contains a P element inserted at the same cytological position (48B6-7, Table 1). Third, meiotic recombination (see MATERIALS AND METHODS) maps wal to 2-59, which corresponds roughly to the cytological position of the P element in line k14036. The fact that this line complements the only known deficiency, Df(2R)en30, reported to uncover the P-insertion site is probably due to an error in mapping of the deficiency, since l(2)02516 also complements this deficiency.
The novel locus drumstick (drm) was identified on the basis of the fact that the Malpighian tubules, though normal in morphology, are located more posteriorly in mutant than in wild-type embryos. Unlike the other mutants described here, which all affect the morphogenesis of multiple epithelial structures, the drm mutation affects only hindgut elongation and folding of the proventriculus. Although the drm mutation is lethal, it is not embryonic lethal; recombination was used to separate the drm mutation in the k11011 line from an embryonic lethal locus. Meiotic mapping placed drm between al and dp, while complementation tests with different deficiencies and translocations in this region further refined the location of drm to cytological region 23E-24A. However, as there is no available deficiency uncovering this region, we cannot determine whether the drm mutation in k11011 is a null allele. Below we describe the Malpighian tubule phenotype of the mutants identified in the screen. In addition, many of the mutants also affect development of other epithelial structures (hindgut, foregut, midgut, tracheae, etc.). These phenotypes are described in subsequent sections.
Effects on steps of Malpighian tubule morphogenesis:
Normal development of the tubules has been reviewed by
Bud evagination (and recruitment): In the early gastrula, the Malpighian tubules share the same anlage with the hindgut. At the end of germ band extension (stage 10), two pairs of buds evaginate from the proctodeum, at the junction of the hindgut and posterior midgut primordia. As shown in Figure 1A, cells continue to be recruited from the proctodeum into the Malpighian tubule primordia during germ band shortening (stage 12). This cell recruitment, which we define as part of bud evagination, is defective in wal mutant embryos: instead of being incorporated into the everting buds, many cells of the primordia remain in the proctodeum as a ring (Figure 1E). Even at later stages (14 and 15), a few Cut staining cells are observable in the ring (not shown); the cells that have been recruited into the buds, however, manage to undergo subsequent cell rearrangements. The resultant wal tubules are fairly elongated but convoluted (not shown).
Bud extension: As the tubule cells continue to be recruited into the buds during stage 12, cells already in the buds participate in another morphogenetic process, bud extension, which is completed by the end of stage 13. In this process, the cylindrical buds extend and become narrower both proximally and distally, resulting in a crescent-shaped morphology (Figure 1B). In fas mutant embryos, the tubule primordia cells appear to evert into buds, proliferate, and complete recruitment successfully; however, by the end of stage 13, the tubules have not extended, but rather remain arrested as four globules of densely packed, Cut-stained cells (Figure 1F). Thus, fas is required for the cylinder-to-crescent transition, presumably for the movement of cells toward the tubule tips, and/or for the rearrangement of cells leading to reduction in tubule diameter near the tips. A phenotype similar to that of fas embryos is seen in thr embryos, namely, that extension of the tubular buds is inhibited (Figure 1G). A difference is that while tubule extension is blocked in fas embryos, it is only retarded in thr embryos, so that the tubules in the latter embryos continue development but become arrested during elongation (described below).
Tubule elongation:
After completion of recruitment and bud extension, there is no further cell division. At this point (end of stage 13), the circumference of each of the four primitive tubules comprises about eight cells (
Hindgut morphogenesis:
In the blastoderm stage embryo, the hindgut primordium is established as a ring of cells bordering the posterior midgut primordium (
Four mutants identified in the screen, in addition to displaying defects in Malpighian tubule development and in other aspects of epithelial morphogenesis (see below), also show hindgut defects. In raw embryos, there is an extremely narrow tube, or thread, of Crb staining connecting the small intestine and rectum (Figure 2C). That this constitutes a connection (a very reduced or collapsed large intestine) between small intestine and rectum is demonstrated by the presence of a tube of visceral mesodermal cells surrounding this region, as indicated by staining with anti-Connectin (Figure 2D). In thr embryos, the hindgut is shorter and broader than normal (Figure 2F); this incomplete elongation appears similar, and may be related in cause, to the incomplete extension of Malpighian tubules seen in the same embryos.
Two defects are seen in the hindgut of fas embryos: (1) the small intestine is reduced and misshapen (Figure 2G), and (2) the cells of the large intestine are stained circumferentially with anti-Crb (Figure 2H). Since Crb is normally found only on the apical surface of epithelia (the lumen of the hindgut in this case), the uniform surface staining of cells in the fas large intestine indicates that these cells lack apical-basal polarity.
The drumstick mutation is unique among the loci identified in this screen, as drm mutant embryos show defects only in hindgut elongation (Figure 2E) and in proventriculus formation (Figure 3B, see next section). The dramatically shorter but wider hindgut in drm mutant embryos suggests a failure of convergent extension (cell rearrangement) in hindgut epithelium.
Foregut morphogenesis:
Invagination of the foregut primordium (the stomodeum) starts at the beginning of stage 10 (reviewed by
Five of the mutants identified in the screen have altered foregut morphogenesis. In barr embryos, both formation of the pharynx and folding morphogenesis of the proventriculus are incomplete (Figure 3C). In wal embryos, the esophagus is wider than normal and its epithelium highly corrugated; no proventriculus is evident (Figure 3D). In thr and fas embryos, the esophagus is shorter and the proventriculus is defective (Figure 3E and Figure F); in particular, in fas embryos, the keyhole that constitutes the beginning of proventriculus formation does not form (Figure 3F).
The defect in proventriculus formation in drm embryos is quite different from that seen in the other mutants. First, it is not associated with defects in head involution or esophagus formation, both of which appear normal in drm embryos. Second, the region of the esophagus that would form the proventriculus becomes elongated, but does not initiate either keyhole formation or folding morphogenesis (Figure 3B).
Other epithelial morphogenesis:
With the exception of the drm mutation, which has a very restricted phenotype, all of the mutants identified display defects in the development of multiple epithelial structures. The organs affected include the midgut, salivary glands, and tracheae, and the morphogenetic processes affected include germ band retraction, dorsal closure, and head involution. These defects are shown in Figure 4 and are summarized in Table 1.
| DISCUSSION |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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By screening a collection of second chromosome lethals, we have identified six loci that affect Malpighian tubule development and one locus that affects hindgut development. Five of the loci identified were known previously, and two are novel. The previously known genes all affect multiple aspects of epithelial development. Of the genes in this group that have been molecularly characterized, all are expressed globally and encode proteins required in many cell types at many stages: the EGF receptor (flb), a cell adhesion molecule (fas), and proteins required for chromatid segregation (barr, thr;
Efficacy of screen:
Although we screened specifically for Malpighian tubule defects, all of the mutants that we identified (with the exception of drm) display defects in multiple epithelial structures (e.g., tracheae, salivary glands), and/or in processes involving epithelia, such as midgut constriction, germ band retraction, dorsal closure, and head involution. Four of these six mutants with multiple epithelial defects were previously identified in a screen for embryonic lethals affecting cuticular differentiation (fas, flb, raw, and thr;
We identified only one mutation (drm) that specifically affects the gut; this mutation by itself is not embryonic lethal. Thus, future screens for novel mutants with defects specific to Malpighian tubule and/or hindgut should not be based on embryonic lethality. Instead, such screens could use antibody staining of fixed embryos or direct observation of larvae expressing markers such as green fluorescent protein.
Novel genes identified:
wal:
Mutations in this gene affect many processes of epithelial morphogenesis, including migration of the midgut endodermal epithelia over the yolk and subsequent midgut constrictions, cell recruitment from the Malpighian tubule primordia into buds, proventriculus formation, formation of the dorsal tracheal tubes, and head involution. As we did not observe obvious manifestations of cell death (such as holes seen in the cuticles of fas, barr, and thr embryos) in wal embryos, wal is likely to be required not so much for epithelial maintenance, but rather for a process common to the morphogenesis of multiple epithelia, such as cell rearrangement.
drm:
This mutation is unique among the mutants identified here, as it affects only internal organs, and of these, only the foregut and hindgut. The phenotype of drm embryos is consistent with previous studies suggesting that there is a similarity in the genetic mechanisms controlling the development of these two structures. In particular, fkh is expressed in both foregut and hindgut primordia and is required for their subsequent development (
Insights into Malpighian tubule development:
On the basis of work described here previously, Malpighian tubule morphogenesis can be divided into four steps or processes, some of which overlap (Figure 5). First, the tubule primordium is established. This requires the early and partially overlapping expression, at the posterior of the embryo, of wg and a number of genes that encode transcription factors, namely tll, hkb, and fkh. The activity of these latter genes, by a combination of activation and repression, initiates a program of gene activity that commits cells to the proctodeal fate (reviewed by
After completion of germ band extension, the tubule primordia undertake a morphogenetic process, bud evagination, which is initially controlled by Kr and wg. Kr encodes a transcription factor that is specifically expressed in the tubule primordium and is required for bud evagination (
The next step of tubule morphogenesis is bud extension. cut is expressed specifically in the tubules (under control of Kr); the tubules of cut embryos arrest early in the process of extension (
Of the genes identified affecting Malpighian tubule development in this and other studies, the largest number affect tubule elongation. This might suggest that elongation is the most complex step in tubule morphogenesis; another interpretation would be that, since elongation takes place last, it is subject to cumulative effects of derangement in processes taking place earlier.
Many genes that affect cell proliferation in the tubules also affect tubule elongation. These include: genes of the EGF signaling pathway, involved in the signaling from the tip cell that stimulates cell proliferation in the tubules (Star, rhomboid, spitz, flb, pointed, and seven up;
A number of genes have been identified that, although they do not appear to be expressed in the tubules themselves, have been shown to be required for tubule elongation. This is true for sog, which antagonizes activity of the BMP4 homolog Dpp (
The work described here, together with previous observations, associates specific genes with specific steps in Malpighian tubule development. Identifying (by genetic and molecular techniques) the genes regulated in the Malpighian tubules by Kr and cut should contribute to our understanding of mechanisms that control bud evagination and bud extension, respectively. Characterizing the gene products of the wal and rib genes is also likely to add to our understanding of the types of molecules required for the aforementioned morphogenetic processes. Finally, increased understanding of epithelial morphogenesis of other tubular organs, namely, foregut and hindgut, should be provided by investigation into the drm gene.
| ACKNOWLEDGMENTS |
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We thank John Merriam, Frank Laski, and Volker Hartenstein for helpful discussions, and Silvia Wenjuan Yu and Ronald Togelang for excellent technical assistance. This work was supported by National Institutes of Health grant HD-09948 to J. A. Lengyel and by a University of California–Los Angeles Dissertation Year Fellowship to X. Liu.
Manuscript received August 21, 1998; Accepted for publication October 26, 1998.
| LITERATURE CITED |
|---|
| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
ASHBURNER, M., 1989 Drosophila: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
BAUMANN, P. and H. SKAER, 1993 The Drosophila EGF receptor homologue (DER) is required for Malpighian tubule development. Development (Suppl.): 65–76.
BHAT, M. A., A. V. PHILP, D. M. GLOVER, and H. J. BELLEN, 1996 Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with Topoisomerase II. Cell 87:1103-1114[Medline].
BLOCHLINGER, K., R. BODMER, L. Y. JAN, and Y. N. JAN, 1990 Patterns of expression of cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos. Genes Dev. 4:1322-1331
CAMPOS-ORTEGA, J. A., and V. HARTENSTEIN, 1997 The Embryonic Development of Drosophila melanogaster. Springer-Verlag, Berlin.
D'ANDREA, R. J., R. STRATMANN, C. F. LEHNER, U. P. JOHN, and R. SAINT, 1993 The three rows gene of Drosophila melanogaster encodes a novel protein that is required for chromosome disjunction during mitosis. Mol. Biol. Cell 4:1161-1174[Abstract].
DIAZ, R., R. HARBECKE, J. SINGER, F. PIGNONI, and W. JANNING et al., 1996 Graded effect of tailless on posterior gut development: molecular basis of an allelic series of a nuclear receptor gene. Mech. Dev. 54:119-130[Medline].
EBERL, D. and A. HILLIKER, 1988 Characterization of X-linked recessive lethal mutations affecting embryonic morphogenesis in Drosophila melanogaster.. Genetics 118:109-120
FRANCOIS, V., M. SOLLOWAY, J. O'NEILL, J. EMERY, and E. BIER, 1994 Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene. Genes Dev. 8:2602-2616
GAUL, U. and D. WEIGEL, 1990 Regulation of Krüppel expression in the anlage of the Malpighian tubules in the Drosophila embryo. Mech. Dev. 33:57-67[Medline].
HÄCKER, U. and N. PERRIMON, 1998 DRhoGEF2 encodes a member of the Dbl family of oncogenes and controls cell shape changes during gastrulation in Drosophila.. Genes Dev. 12:274-284
HACOHEN, N., S. KRAMER, D. SUTHERLAND, Y. HIROMI, and M. A. KRASNOW, 1998 sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92:253-263[Medline].
HALL, A., 1998 Rho GTPases and the actin cytoskeleton. Science 279:509-514
HARBECKE, R. and W. JANNING, 1989 The segmentation gene Kruppel of Drosophila melanogaster has homeotic properties. Genes Dev. 3:114-122
HARBECKE, R. and J. LENGYEL, 1995 Genes controlling posterior gut development in the Drosophila embryo. Roux's Arch. Dev. Biol. 204:308-329.
HARTENSTEIN, V., 1993 Atlas of Drosophila Development. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
HOCH, M. and M. PANKRATZ, 1996 Control of gut development by fork head and cell signaling molecules in Drosophila.. Mech. Dev. 58:3-14[Medline].
HOCH, M., K. BROADIE, H. JACKLE, and H. SKAER, 1994 Sequential fates in a single cell are established by the neurogenic cascade in the Malpighian tubules of Drosophila.. Development 120:3439-3450[Abstract].
JACK, J. and G. MYETTE, 1997 The genes raw and ribbon are required for proper shape of tubular epithelial tissues in Drosophila.. Genetics 147:243-253[Abstract].
JANNING, W., A. LUTZ, and D. WISSEN, 1986 Clonal analysis of the blastoderm anlage of the Malpighian tubules in Drosophila melanogaster.. Roux's Arch. Dev. Biol. 195:22-32.
KERBER, B., S. FELLERT, and M. HOCH, 1998 Seven-up, the Drosophila homolog of the COUP-TF orphan receptors, controls cell proliferation in the insect kidney. Genes Dev. 12:1781-1786
KISPERT, A., B. HERRMANN, M. LEPTIN, and R. REUTER, 1994 Homologs of the mouse Brachyury gene are involved in the specification of posterior terminal structures in Drosophila, Tribolium, and Locusta.. Genes Dev. 8:2137-2150
LEKVEN, A. C., U. TEPASS, M. KESHMESHIAN, and V. HARTENSTEIN, 1998 faint sausage encodes a novel extracellular protein of the Immunoglobulin superfamily required for cell migration and the establishment of normal axonal pathways in the Drosophila nervous system. Development 125:2747-2758[Abstract].
LEPTIN, M., 1995 Drosophila gastrulation: from pattern formation to morphogenesis. Annu. Rev. Cell Dev. Biol. 11:189-212[Medline].
LIU, S. and J. JACK, 1992 Regulatory interactions and role in cell type specification of the Malpighian tubules by the cut, Krüppel, and caudal genes of Drosophila.. Dev. Biol. 150:133-143[Medline].
MEADOWS, L., D. GELL, K. BROADIE, A. GOULD, and R. WHITE, 1994 The cell adhesion molecule, connectin, and the development of the Drosophila neuromuscular system. J. Cell Sci. 107:321-328[Abstract].
NOSELLI, S., 1998 JNK signaling and morphogenesis in Drosophila.. Trends Genet. 14:33-38[Medline].
NÜSSLEIN-VOLHARD, C., 1977 A rapid method for screening eggs from single Drosophila females. Dros. Inf. Serv. 52:166.
NÜSSLEIN-VOLHARD, C., E. WIESCHAUS, and H. KLUDING, 1984 Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. I. Zygotic loci on the second chromosome. Roux's Arch. Dev. Biol. 193:267-282.
PANKRATZ, M. J. and M. HOCH, 1995 Control of epithelial morphogenesis by cell signaling and integrin molecules in the Drosophila foregut. Development 121:1885-1898[Abstract].
PHILP, A. V., J. M. AXTON, R. D. SAUNDERS, and D. M. GLOVER, 1993 Mutations in the Drosophila melanogaster gene three rows permit aspects of mitosis to continue in the absence of chromatid segregation. J. Cell Sci. 106:87-98[Abstract].
REHORN, K., H. THELEN, A. MICHELSON, and R. REUTER, 1996 A molecular aspect of hematopoiesis and endoderm development common to vertebrates and Drosophila.. Development 122:4023-4031[Abstract].
SCHEJTER, E. D. and B. Z. SHILO, 1989 The Drosophila EGF receptor homolog (DER) gene is allelic to faint little ball, a locus essential for embryonic development. Cell 56:1093-1104[Medline].
SINGER, J., R. HARBECKE, T. KUSCH, R. REUTER, and J. LENGYEL, 1996 Drosophila brachyenteron regulates gene activity and morphogenesis in the gut. Development 122:3707-3718[Abstract].
SKAER, H., 1989 Cell division in Malpighian tubule development in D. melanogaster is regulated by a single tip cell. Nature 342:566-569.
SKAER, H., 1993 The alimentary canal, pp. 941–1012 in The Development of Drosophila melanogaster, edited by M. BATE and A. MARTINEZ ARIAS. Cold Spring Harbor Laboratory Press, Plainview, NY.
SKAER, H., 1997 Morphogenesis: FGF branches out. Curr. Biol. 7:238-241.
SKAER, H. and A. MARTINEZ ARIAS, 1992 The wingless product is required for cell proliferation in the Malpighian tubule anlage of Drosophila melanogaster.. Development 116:745-754[Abstract].
STRATMANN, R. and C. LEHNER, 1996 Separation of sister chromatids in mitosis requires the Drosophila pimples product, a protein degraded after the metaphase/anaphase transition. Cell 84:25-35[Medline].
TECHNAU, G. and J. CAMPOS-ORTEGA, 1985 Fate-mapping in wild-type Drosophila melanogaster. II. Injection of horseradish peroxidase in cells of the early gastrula stage. Roux's Arch. Dev. Biol. 194:121-196.
TEPASS, U., C. THERES, and E. KNUST, 1990 crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell 61:787-799[Medline].
TÖRÖK, T., G. TICK, M. ALVARADO, and I. KISS, 1993 P-lacW insertional mutagenesis on the second chromosome of Drosophila melanogaster: isolation of lethals with different overgrowth phenotypes. Genetics 135:71-80[Abstract].
WEIGEL, D., H. BELLEN, G. JÜRGENS, and H. JÄCKLE, 1989 Primordium specific requirement of the homeotic gene fork head in the developing gut of the Drosophila embryo. Roux's Arch. Dev. Biol. 198:201-210.
WU, L. and J. LENGYEL, 1998 Role of caudal in hindgut specification and gastrulation suggests homology between Drosophila amnioproctodeal invagination and vertebrate blastopore. Development 125:2433-2442[Abstract].
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