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Published in final edited form as: Gene Expr Patterns. 2008 Sep 11;9(1):31–36. doi: 10.1016/j.gep.2008.09.001

Expression patterns of cadherin genes in Drosophila oogenesis

Jeremiah J Zartman 1, Jitendra S Kanodia 1, Nir Yakoby 1, Xenia Schafer 1, Colin Watson 1, Karin Schlichting 2, Christian Dahmann 2, Stanislav Y Shvartsman 1
PMCID: PMC4096819  NIHMSID: NIHMS91744  PMID: 18817893

Abstract

In Drosophila oogenesis, the follicular epithelium that envelops the oocyte is patterned by a small set of inductive signals and gives rise to an elaborate three-dimensional eggshell. Several eggshell structures provide sensitive readouts of the patterning signals, but the formation of these structures is still poorly understood. In other systems, epithelial morphogenesis is guided by the spatial patterning of cell adhesion and cytoskeleton genes. As a step towards developing a comprehensive description of patterning events leading to eggshell morphogenesis, we report the expression of Drosophila cadherins, calcium dependent adhesion molecules that are repeatedly used throughout development. We found that 9/17 of Drosophila cadherins are expressed in the follicular epithelium in dynamic patterns during oogenesis. In late oogenesis, the expression patterns of cadherin genes in the main body follicle cells is summarized using a compact set of simple geometric shapes, reflecting the integration of the EGFR and DPP inductive signals. The multi-layered composite patterning of the cadherins is hypothesized to play a key role in the formation of the eggshell. Of particular note is the complex patterning of the region of the follicular epithelium that gives rise to the dorsal appendages, which are tubular structures that serve as respiratory organs for the developing embryo.

Keywords: Drosophila, cadherin, oogenesis, gene expression, morphogenesis, adhesion, pattern formation, follicle cell, epithelium

1. Results and Discussion

Epithelial morphogenesis is characterized by the sequential execution of a core set of programmed stereotypical cell movements and shape changes, which result from the differential expression of cytoskeleton and adhesion genes (Pilot and Lecuit, 2005; Ray Keller, 2003; Schock and Perrimon, 2002; Tepass, 1999). In Drosophila oogenesis, the follicular epithelium, which surrounds the nurse cells and oocyte, serves as an established model for studying epithelial patterning and morphogenesis, amenable to live imaging and sophisticated genetic perturbations (Berg, 2005; Dorman et al., 2004; Duffy, 2002; Wu et al., 2008). Particularly striking morphogenetic events occur during the later stages of oogenesis, when the main body follicle cells (MBFCs), which encapsulate the oocyte, undergo a series of cell shape changes and movements to form and secrete an elaborate three-dimensional eggshell, including tubular structures called dorsal appendages (DAs) that project out from the main eggshell body and act as respiratory tubes for the developing embryo (Hinton, 1969; Ward and Berg, 2005; Waring, 2000).

Little is known about the expression, regulation and function of effector genes required for proper eggshell morphogenesis. As one important class of effector molecules in epithelial morphogenesis, cadherins are glycoproteins that mediate Ca+2 dependent cell-cell adhesion and contain multiple, conserved cadherin domains (Halbleib and Nelson, 2006; Tepass et al., 2000). The Drosophila genome encodes 17 cadherins (Hill et al., 2001; Hynes and Zhao, 2000) with representative members in each of the known subgroups of cadherins, excluding desmosomal cadherins (Hill et al., 2001; Tepass et al., 2000) (Table 1). Drosophila cadherins are subdivided into classical cadherins, defined by the presence of a conserved catenin-binding domain (Shotgun/DE-Cad, Cadherin-N/DN-Cad, CadN2), and nonclassical cadherins, which lack any recognizable catenin-binding domain (Fung et al., 2008; Hill et al., 2001; Tepass et al., 2000). Nonclassical cadherins consist of Fat-like cadherins (Fat, Fat2, Dachsous), seven-pass transmembrane cadherins (Starry Night/Flamingo), Calsyntenin cadherins (Calsyntenin-1), protein kinase cadherins (Ret and Cad96Ca), and currently uncategorized cadherins (Cad74A, Cad86C, Cad87A, Cad88C, Cad89D, Cad96Cb, Cad99C) (Fung et al., 2008; Hill et al., 2001).

Table 1.

Cadherin classification and expression in the Drosophila genome

Gene Subcategory Expression Selected References
Early
S<10		 Late
S>10
shotgun (shg)/
DE-Cad 		Classical + + (Godt and Tepass, 1998; Niewiadomska et al, 1999; Oda et al., 1997; Pacquelet and Rorth, 2005)
cadherin-N
(CadN)/DN-Cad 		Classical + − (Tanentzapf et al., 2000)
CadN2 Classical − − (Tepass and Harris, 2007)
starry night/
flamingo
(stan/fmi) 		Seven-pass
transmembrane		 − (Oda et al., 1997)
fat2 Fat-like + + (Castillejo-Lopez et al, 2004)
fat Fat-like − − (Castillejo-Lopez et al, 2004; Demontis et al., 2006; Saburi et al., 2008)
dachsous (ds) Fat-like − − (Tanoue and Takeichi, 2005)
calsyntenin-
l(cals) 		Calsyntenin + + (Vogt et al., 2001)
Ret oncogene
(Ret) 		Protein kinase − − (Abrescia et al., 2005; Fung et al, 2008; Sugaya et al, 1994)
Cad74A Nonclassical + + (Zartman et al.. In Press)
Cad86C Nonclassical − + (Schlichting and Dahmann, 2008)
Cad87A Nonclassical + + (Fung et al., 2008; Hill et al., 2001; Tepass et al., 2000)
Cad88C Nonclassical, − + (Demontis et al., 2006; Fung et al, 2008; Lovegrove et al., 2006)
Cad89D Nonclassical − − (Hill et al, 2001; Tepass et al., 2000)
Cad96Ca Protein kinase − − (Demontis et al., 2006)
Cad96Cb Nonclassical − − (Lovegrove et al, 2006)
Cad99C Nonclassical + + (D′Alterio et al, 2005; Schlichting et al, 2005; Schlichting et al, 2006)
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As a first step to providing a comprehensive analysis of the differential expression of potential effector molecules in the follicular epithelium, we have constructed a gene expression atlas of Drosophila cadherin genes. Nine expression patterns were identified in the follicle cells throughout all stages of oogenesis, five of which are newly reported: fat2, Cad86C, Cad87A, Cad88C and cals. Expression patterns for two genes, Cad74A and Cad99C were reported in the literature previously (D'Alterio et al., 2005; Schlichting et al., 2006; Zartman et al., In Press). Finally, expression of DE-Cad and DN-Cad were examined earlier, but later stages of mRNA expression were not previously shown explicitly (Becam et al., 2005; Godt and Tepass, 1998; Niewiadomska et al., 1999; Schnorr and Berg, 1996). Below we describe the expression patterns and group them into spatial and temporal categories.

1.1 Spatial and temporal expression of cadherin genes

Gene expression patterns of the nine detected cadherin genes can be subdivided into two temporal stages: early oogenesis, before stage 10, as defined by (Spradling, 1993), and later stages, stages 10-14, when the diversity of patterns is greater (Fig. 1 and Table 1). During early oogenesis, seven cadherins were detected: DE-Cad (Fig. 1A1 and inset), DN-Cad (Fig. 1B1), fat2 (Fig. 1C1), cals (Fig. 1D1 and inset), Cad74A (Fig. 1E1, arrows), Cad87A (Fig. 1G1) and Cad99C (D'Alterio et al., 2005; Schlichting et al., 2006) (Fig. 1I1).

Figure 1. Expression patterns of cadherin genes in Drosophila oogenesis.

Figure 1

Figure 1

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Expression of cadherin genes at stages <10 (1), Stage 10A (2), Stage 10B (3), Stages 11 (4), Stage12 (5) and Stage 13 (6) for (A) DE-Cad, (B) DN-Cad, (C) fat2, (D) calsyntenin-1 (cals), (E) Cad74A, (F) Cad86C, (G) Cad87A, (H) Cad88C, and (I) Cad99C. Inserts show expression in the earliest stages or the posterior in late stages. Dark arrows point to visible staining in the border cells. (G4): Arrow points to repression in the floor cells.

Late FC morphogenesis begins in stage 10B when the main body follicle cells (MBFCs) undergo a series of cell shape changes and movements to form the dorsal-anterior eggshell structures (Fig. 2A): the operculum, which is formed by midline cells (M), the micropyle, which is shaped by the centripetal migrating follicle cells consisting of a row of anterior follicle cells (A) and border cells (Montell et al., 1992), and dorsal appendages, which are formed by the roof (R) and floor (F) primordia, two cell populations that form the dorsal and ventral sides of each of the DAs (Dorman et al., 2004; Ward and Berg, 2005). While the patterning by EGFR and DPP signaling and the morphogenesis of the follicle cells has been studied extensively, less is known about the effectors of FC morphogenesis (Berg, 2005; Dorman et al., 2004; Horne-Badovinac and Bilder, 2005; Ward and Berg, 2005; Wu et al., 2008). Two-dimensional expression patterns are most easily categorized in stages 10-12, when the midline, floor, and roof cells have already been specified, but before significant three-dimensional shaping of the dorsal appendages occurs (Yakoby et al., under review). The dynamics of the nine expressed cadherin genes during oogenesis are discussed below.

Figure 2. Pattern classification and abstracted expression.

Figure 2

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(A) Pattern annotation scheme for the main body follicle cells (MBFCs), as proposed in (Yakoby et al., under review). Patterns have been described using three differential levels of expression: Expression not detected (no shading), basal expression (grey) and strong expression (black). (B) Abstracted expression patterns are shown as cartoons for the nine cadherin genes. Roof versus floor plus roof expression was determined by counting the number of cells between the patches (2 cells for floor plus roof, 4 for roof patterns).

1. shotgun/DE-Cad

Strong shotgun (DE-Cad) expression consistently precedes major morphogenetic movements of the FCs. DE-Cad is expressed in both the germline and the somatic follicle cells and is required for anchoring the somatic stem cell in the germarium niche (Song and Xie, 2002) and positioning the oocyte in the posterior of the egg chamber (Godt and Tepass, 1998; Gonzalez-Reyes and St Johnston, 1998). DE-Cad is also expressed in the border cells during stage 9 before border cell migration (Niewiadomska et al., 1999; Oda et al., 1997) (Fig. 1A1, arrowhead).

DE-Cad shifts from being expressed in an anterior band, corresponding to the centripetal migrating follicle cells (CMFCs) at stage 10A, to strong expression in the midline cells and weak expression in the floor and roof cells during stage 10B, when these cells apically constrict and intercalate (Fig. 1A2-5; James et al., 2002). The pattern continues to show differential DE-Cad expression in the cells forming the dorsal anterior eggshell structures during stages 11 and 12. DE-Cad is also expressed in the posterior FCs, which form the aeropyle (Fig. 1A5, inset).

2. Cadherin-N/DN-Cad

DN-Cad is expressed during early oogenesis in the FCs (Fig. 1B1). The adherens junctions contain both DN-cadherin and DE-cadherin until stage 10 (Tanentzapf et al., 2000), which is unusual because DE-Cad and DN-Cad are not usually co-expressed (Horne-Badovinac and Bilder, 2005). DN-Cad expression is not detected in the FCs after stage 9 (Fig. 1B2-6).

3. fat2

fat2 is expressed during the early stages of oogenesis, but the resolution of the assay is not sufficient to determine if it is the germline or the FCs (Fig. 1C1). Later at stage 10A, fat2 shifts from being expressed uniformly in all MBFCs and nurse cells to being expressed very strongly in the floor cells and weakly in the roof cells (Fig. 1C2-C6) with loss of expression in the other MBFCs during stages 10B-14. The transcript is found in the apical region of FCs. Fat2 shares similarity to Drosophila Fat in the extracellular domain, but lacks the PCP signaling domain found in the intracellular domain of Fat (Castillejo-Lopez et al., 2004; Saburi et al., 2008). fat2 has been implicated in tube formation throughout embryogenesis, including the trachea, salivary glands, proventriculus, and hindgut (Castillejo-Lopez et al., 2004). Based on cultured cell studies and in vivo loss-of-function analysis, Castillejo-Lopez et al. propose that fat2 does not play a role in adhesion but, perhaps due to its size, acts as a spacer for the tube lumen (Castillejo-Lopez et al., 2004).

4. calsyntenin-1 (cals)

calsyntenin-1 shows expression during stages 7-9 in the MBFCs and in the border cells during migration (Fig. 1D1 and inset). Calsyntenin-1(cals) expression is uniform during stage 10A (Fig. 1D2), but is restricted to the dorsal region at stage 10B (Fig. 1D3) with stronger expression in midline in stages 11/12 (Fig 1D4-D5). Expression is also detected in the posterior FCs during the late stages (Fig. 1D4, inset).

5. Cad74A

The expression patterns for Cad74A (Fig. 1E1-6) was published previously (Zartman et al., In Press). Cad74A is expressed in the polar cells during early oogenesis (Fig. 1E1, arrows). During late oogenesis, Cad74A is expressed in all FCs contacting the oocyte in stage 10B, except for the roof cells where high levels of the zinc-finger transcription factor Broad (Deng and Bownes, 1997; Dorman et al., 2004; Tzolovsky et al., 1999; Ward and Berg, 2005) are sufficient to repress Cad74A expression. Overexpresssion of Cad74A in the roof cells results in short, flattened DAs due to the hindered migration of roof cells, suggesting a possible role in the remodeling of the adherens junctions or modulation of the apical membrane. The Cad74A null allele shows reproducible but incompletely penetrant DA defects (Zartman et al., In Press).

6. Cad86C

Cad86C is not expressed (Fig. 1F1, 2) until stage 10B, when it is strongly detected in the roof cells and in a ventral band, corresponding to high Broad levels (Fig. 1F3-6) (Dorman et al., 2004). During stages 11 and 12, a strong hybridization signal is detected in the roof cells and the midline cells separating the roof primordia. Overexpression of Cad86C in the imaginal discs is sufficient to cause apical constriction (Schlichting and Dahmann, 2008), suggesting that it may be involved in apical constriction of the roof cells during dorsal appendage formation.

7. Cad87A

Identified as a possible vertebrate Cadherin23 homolog (Fung et al., 2008), Cad87A is expressed in the oocyte during the early stages of oogenesis (Fig. 1G1). During stage 10B, Cad87A is expressed uniformly in the FCs, with stronger expression in the dorsal anterior (Fig. 1G3). During stages 11/12, expression is particularly strong in the dorsal region except for the floor cells (Fig 1G4, arrow).

8. Cad88C

Cad88C expression is not detectable in the follicle cells up to stage 10A (Fig. 1H1, 2). In stage 10B, all follicle cells contacting the oocyte express Cad88C (Fig. 1H3). In stages 11-12, expression is confined to dorsal-anterior cells and posterior cells (Fig. 1H4-5).

9. Cad99C

The expression and function of Cad99C was previously reported and is required for microvilli morphology and the proper secretion of the vitelline membrane (D'Alterio et al., 2005; Schlichting et al., 2006). Cad99C, a homolog of Protocadherin 15 and required for microvilli morphology, is expressed in stages 4-8 in the anterior and posterior follicle cells and in the follicle cells that migrate to contact the oocyte at stage 9 (D'Alterio et al., 2005; Schlichting et al., 2006) (Fig. 1I1). However, we also find that Cad99C is repressed in the roof cells at stages 11/12 (Fig. 1I4).

1.3 Towards a spatial atlas of morphogenesis

Implementation of the morphogenetic program in several contexts has been found to be robust to the single loss-of-function perturbations of many effector proteins (Kleve et al., 2006; Lovegrove et al., 2006; Schlichting and Dahmann, 2008; Zartman et al., In Press). In the case of our recent study on Cad74A (Zartman et al., In Press), the lack of a strongly penetrant phenotype led us to hypothesize that perhaps other cadherins are expressed in similar expression patterns. In an unbiased pilot screen for expression patterns of morphogenesis genes, we found that a significant fraction (9/17) of the Drosophila cadherin superfamily is differentially expressed during Drosophila oogenesis. Our analysis of mRNA expression addresses the variety of spatial patterns but does not account for gene or protein activity, which must be examined to understand the lack of visible phenotypes in loss-of-function perturbations.

Remarkably, cadherin expression patterns are especially diverse during the later stages of oogenesis (stages 10-14). To provide abstractions of patterns, we have recently proposed an annotation system which compactly describes gene expression patterns during stages 10-12 of oogenesis (Figure 2A, B; Yakoby et al, under review). The geometric annotation terms are derived from the underlying signaling dynamics of the EGFR and BMP signaling pathways and summarize all known FC expression patterns during mid/late oogenesis (Goentoro et al., 2006; Lembong et al., In Press; Yakoby et al., under review). All expression patterns are summarized as Boolean combinations of seven primitive shapes: uniform (U), dorsal (D), midline (M), anterior (A), roof (R), floor (F), and posterior (P) (Fig. 2A). Three principle operations are performed to construct more complex patterns representing the integrate output of EGFR and DPP signaling: union (+), difference (\) or intersection (∩) (Table 2; Yakoby et al., under review).

Table 2.

Geometric annotations of cadherin patterns in the MBFCs

Gene Stage 10 A Stage 10 B Stage 11/12
DE-Cad A M ∪ D ∪ P A ∪ D ∪ P
DN-Cad - - -
fat2 U R ∪ F R ∪ F
cals U U ∪M M ∪ D
Cad74A - U \ R U \ R
Cad86C - R D \ D ∩ A
Cad87A - U ∪ D U ∪ D \ F
Cad88C U D ∪P D ∪ P
Cad99C A ∪ U A ∪ P M ∪ U \ R
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Of particular interest, several cadherins show complex overlapping dynamic expression patterns in the dorsal anterior FCs: midline, floor and roof cells, which are responsible for forming the operculum and DAs (Fig. 2B). Remarkably, no two cadherin genes share an identical expression profile, suggesting that the robustness of morphogenesis is not due to an absolute redundancy in cadherin expression.

Cad74A (stages 10B-12) and Cad99C (stages 11/12) show repression in the roof cells relative to expression in the MBFCs (Fig. 2B). DE-Cad, fat2 and cals show high expression in the floor cells and graded expression in the roof cells. Cad86C initially shows strong expression only in the roof cells whereas Cad87A shows relative repression in the floor cells. Cad88C also shows specific expression to the dorsal anterior cells. Dissecting the regulatory network that leads to such spatial pattern diversity will provide insight into how roof, floor and midline cell identities are maintained during late oogenesis. In particular, the relationship between previously mentioned cadherins and Broad, which is a zinc finger transcription factor highly expressed in the roof cells (Deng and Bownes, 1997; Dorman et al., 2004; Ward and Berg, 2005; Yakoby et al., 2008), will need to be investigated further and compared to the regulation model of Cad74A as well as the expression of other classes of effector molecules (Kleve et al., 2006; Laplante and Nilson, 2006; James et al., 2002; Zartman et al., In Press).

The expression patterns found in this study adds further weight to the possibility that a “combinatorial code” of cadherin expression may play a role in segregating and maintaining different cell sub-populations in the FCs (Foty and Steinberg, 2005; Fung et al., 2008; Lovegrove et al., 2006; Schlichting and Dahmann, 2008). For example, similar overlapping patterns for the non-classical cadherins are found in other developmental contexts (Lovegrove et al., 2006; Schlichting and Dahmann, 2008). Based on previous reports and the new patterns identified in this study, we hypothesize that the partially overlapping syn-expression of a subset of adhesion genes ensures robust morphogenesis of the dorsal appendages, providing built-in degeneracy to the epithelial folding code. Deciphering and parsing the spatial grammar of morphogenesis during DA formation will require manipulating the relative expression of sets of adhesion genes. Comparison of the relative overlaps between cadherin expression patterns in other models of morphogenesis will provide a necessary test for the universality of an epithelial folding code that converts spatial patterns of gene expression into mechanical properties and a final morphology.

3. Experimental procedures

Whole-mount in situ hybridization

cDNA clones for fat, fat2, Ret, Cad74A, Cad87A, Cad96Ca and Cad99C were gifts of M. Halfon. cDNA for dachsous came from the Drosophila Genomics Resource Center (Bloomington, IN). Primers used to amplify the remaining cadherin genes from cDNA obtained from the ovary are listed in Table 3. Products from PCR amplification were cloned using a StrataClone PCR Cloning Kit (Stratagene). For Cad88C, the underlined restriction sites (Table 3) for BamHI and Asp718 were used for cloning the PCR product into pBluescript and the clone was sequenced. Clones were designed to be between 900 – 1200 bases. Clones were then sequenced (GeneWiz) and BLASTed against the D. melanogaster genome (FlyBase) to confirm clone identity and orientation. Digoxygenin-labeled RNA probes were made from the cDNA clones. During the in situ experiments, a previously tested control probe was used to ensure the quality of in situ hybridization assay. The in situ hybridization protocol is optimized for assaying gene expression in the follicle cells and was the same as previously described (Wang et al., 2006; Yakoby et al., 2008) without an RNase treatment step. Ore R and y w were used for the in situ hybridization experiments.

Table 3.

Primers used for mRNA probe generation

Gene Forward Primer Reverse Primer
DE-Cad GCCCAATGGTCACAAGAA
CT		 CTCGTTTTGGAGCACAGTGA
DN-Cad GTCAATCGTCCGGTTCAG
TT		 CACCGATTTTCCCTCAGTGT
CadN2 TGCCAATCTCAGCGTTAC
AG		 CCATCATCCAGCGTTTTCTT
Starry night/

Flamingo 		CTTTTCGTCTCCGTCAAAG
C		 GATCGAGGGAGGCATATTGA
Calsyntenin-1 TGGCAACACCGATAATGA
AA		 CTCCTATGCATTGCGACAGA
Cad88C CGGGATCCCTTTAGCATT
CGAGAGATCG		 GGGGTACCTTTAGCCACTGAT
GCTGCTC
Cad89D CAAGCCCAATACACCGAA
CT		 ACTTTGCTAGGTCCCGGTTT
Cad86C CACTGAATCTGGACGCTG
AA		 GCCAGAAGAGCACCTTGTTC
Cad96Cb AATCTCGAGCGGATTCCT
TT		 GAGGGCCATGCTACTACTGG
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Acknowledgements

We thank M. Halfon for providing cDNA clones for several cadherin genes and the DGRC (Bloomington, IN) for cDNA clones for ds and C. Bristow for helpful comments on the manuscript. J.J.Z. is supported by the Fannie and John Hertz Foundation and the Princeton Wu fellowship. This work has been supported by the following NIH grants: P50 GM071508 and R01 GM078079 to S.Y.S.

Footnotes

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