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Functional equivalence of Hox gene products in the specification of the tritocerebrum during embryonic brain development of Drosophila

Frank Hirth1,*, Thomas Loop1, Boris Egger1, David F. B. Miller2, Thomas C. Kaufman2 and Heinrich Reichert1

1 Institute of Zoology, Biocenter/Pharmacenter, University of Basel, Klingelbergstrasse 50, CH-4056 Basel, Switzerland
2 Department of Biology, Howard Hughes Medical Institute, Indiana University, Jordan Hall A507, Bloomington, IN 47405-6801, USA



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  		Fig. 1. Expression of Labial and labial loss-of-function phenotype in the Drosophila embryonic brain. Laser confocal microscopy of stage 15 embryos, reconstructions of optical sections. (A,C,E) Frontal views; (B,D,F) lateral views. (A,B) Wild-type embryonic brain. Anti-HRP immunolabeling. Arrows indicate circumesophageal connectives, arrowhead indicates tritocerebral commissure. (C,D) Wild-type embryonic brain. Double immunolabeling with anti-HRP (red) and anti-Lab (green). Arrows indicate Lab expression domain, arrowhead indicates tritocerebral commissure. Same embryo as in A,B. (E,F) lab loss-of-function mutant embryonic brain. Anti-HRP immunolabeling. Arrows indicate missing circumesophageal connectives, arrowhead indicates missing tritocerebral commissure.

 


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  		Fig. 2. Reporter gene expression phenotype in the wild-type Drosophila embryonic brain. Characterization of brain-specific lab::Gal4 driver K5J2 using P{w+; lab::Gal4}K5J2-driven UAS::taulacZ reporter gene expression (Callahan and Thomas, 1994). Laser confocal microscopy of stage 15 embryos, reconstructions of optical sections. (A,C) Frontal views; (B) lateral view; (D) midline cross-section. (A,B,D) Double immunolabeling with anti-HRP (red) and anti-ß-gal (green). P{w+ lab::Gal4}K5J2-driven UAS::taulacZ reporter gene expression is seen in the cortical cytoskeleton and axons of cells in the endogenous tritocerebral Lab expression domain (arrows in A,B) of the wild-type embryonic brain. Arrowhead indicates tritocerebral commissure. Ectopic reporter gene expression is seen in a small number of cells in the deutocerebral and mandibular neuromeres. (C) Double immunolabeling with anti-Lab (red) and anti-ß-gal (green) shows that reporter gene expression occurs in the cortical cytoskeleton of the cells that also show nuclear Lab expression (arrows in C) as well as in their axons projecting along the tritocerebral commissure (arrowhead indicates the tritocerebral commissure). (D) Reporter gene expression is seen in the midline cross-section of the tritocerebral commissure (arrow).

 


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  		Fig. 3. Genetic rescue of the lab mutant brain phenotype by transgenic expression of the Lab protein in a lab-null mutant background. Laser confocal microscopy of stage 15 embryos, reconstructions of optical sections. (A,C) Frontal views’ (B,D) lateral views. (A,B) From the same preparation; (C,D) from the same preparation. (A,B) Anti-HRP immunolabeling. Arrows indicate circumesophageal connectives, arrowhead indicates tritocerebral commissure. (C,D) Double immunolabeling with anti-HRP (red) and anti-Lab (green). Arrows indicate targeted misexpression domain of Lab in the lab mutant embryonic brain (equivalent to the endogeneous expression domain of Lab in the wild-type embryonic brain). Arrowhead indicates tritocerebral commissure.

 


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  		Fig. 4. Genetic rescue of the lab mutant brain phenotype by transgenic expression of the Scr protein (A-C) or the Antp protein (D-F) in a lab-null mutant background. Laser confocal microscopy of stage 15 embryos, reconstructions of optical sections. (A,D) Frontal views, (B,C,E,F) lateral views. (B,C) From the same preparation; (E,F) from the same preparation. (A,B,D,E) Anti-HRP immunolabeling. Arrows indicate circumesophageal connectives, arrowhead indicates tritocerebral commissure. (C) Double immunolabeling with anti-HRP (red) and anti-Scr (green). Arrow indicates targeted misexpression domain of Scr in the lab mutant embryonic brain (equivalent to the endogeneous expression domain of Lab in the wild-type embryonic brain). Asterisk labels the endogenous Scr expression domain in the subesophageal ganglion. (F) Double immunolabeling with anti-HRP (red) and anti-Antp (green). Arrow indicates targeted misexpression domain of Antp in the lab mutant embryonic brain (equivalent to the endogeneous expression domain of Lab in the wild-type embryonic brain). Asterisk labels the endogenous Antp expression domain in the subesophageal ganglion and ventral nerve cord.

 


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  		Fig. 5. Genetic rescue of the lab mutant brain phenotype by transgenic expression of the Ubx protein (A-C), and failure of genetic rescue of the lab mutant brain phenotype by transgenic expression of the Abd-B protein (D-F) in a lab null mutant background. Laser confocal microscopy of stage 15 embryos, reconstructions of optical sections. (A,D) Frontal views, (B,C,E,F) lateral views. (B,C) From the same preparation; (E,F) from the same preparation. (A,B,D,E) Anti-HRP immunolabeling. Arrows indicate location of circumesophageal connectives, arrowhead indicates location of tritocerebral commissure. (C) Double immunolabeling with anti-HRP (red) and anti-Ubx (green). Arrow indicates targeted misexpression domain of Ubx in the lab mutant embryonic brain (equivalent to the endogeneous expression domain of Lab in the wild-type embryonic brain). Asterisk labels part of the endogenous Ubx expression domain in the ventral nerve cord. (D) Double immunolabeling with anti-HRP (red) and anti-Abd-B (green). Arrow indicates targeted misexpression domain of Abd-B in the lab mutant embryonic brain (equivalent to the endogeneous expression domain of Lab in the wild-type embryonic brain). The endogenous Abd-B expression domain in the ventral nerve cord is located in posterior neuromeres that are not shown.

 


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  		Fig. 6. Reporter gene expression shows genetic rescue of commissural axonal projections in the lab–/– cells of the tritocerebrum by transgenic expression of the Lab, Dfd, Antp and Ubx proteins (B-E), and failure of rescue by transgenic expression of the Abd-B protein (F); also shown is the absence of commissural axonal projections in the tritocerebral lab-null mutant domain (A). Laser confocal microscopy of stage 13-15 embryos, reconstructions of optical sections, frontal views. Immunolabeling with anti-ß-gal (green). UAS::taulacZ reporter gene expression is seen in the cortical cytoskeleton and axons of cells in tritocerebral lab mutant. Arrowheads indicate presence or absence of commissural axons of the lab–/– cells. In A, visualization of cell bodies and axonal projections was by lab::Gal4 driven UAS::taulacZ reporter gene expression in the tritocerebral lab mutant domain. In B-F, visualization of cell bodies and genetic rescue of axonal projections of the lab–/– cells was through co-expression of UAS::taulacZ reporter with UAS::Hox responders in the tritocerebral lab mutant domain by the lab::Gal4 driver. For all of the Hox gene products except Abd-B these experiments demonstrated that the rescued tritocerebral lab–/– cells were able to extend axons that projected correctly along the rescued tritocerebral commissure.

 


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  		Fig. 7. Relative rescue efficiency of Hox gene products as related to Lab. The relative efficiency of rescue of the tritocerebral brain defects in lab null mutants is shown for the Hox gene products Lab, Pb, Dfd, Scr, Antp, Ubx, Abd-A and Abd-B expressed in the lab mutant under the control of the same lab-specific cis-acting regulatory elements (see Table 1). The rescue efficiency for Lab is taken as 100% and the rescue values (the relative percentage of embryos showing a complete rescue of the tritocerebral brain defects) of the other Hox gene products are shown in percentage relative to this. The relative rescue efficiency of the Hox gene products (Lab>Pb>Dfd>Scr>AntP>Ubx>Abd-A) reflects the proximal-to-distal arrangement of their encoding loci on the chromosome.

 

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