Annual <i>Drosophila</i> Research Conference, 2008

The Drosophila Research Conference, a yearly meeting organized by the Genetics Society of America (GSA), serves as a platform to present the latest developments in research using the Drosophila melanogaster model. The meeting provides fruit fly researchers an opportunity for interaction and exchange of ideas pertaining to their research. The 49th Annual Drosophila Research Conference took place in San Diego, California, one of the best tourist destinations famous for its great weather and miles of sandy beaches. The meeting was organized by Nanci Bonini (University of Pennsylvania, Philadelphia), Susan Celnikar (Lawrence Berkeley National Laboratory, Berkeley, California), Brian Oliver (NIDDK, NIH, HHS, Bethesda, MD), and John Tamkun (University of California, Santa Cruz). This fly meeting was attended by nearly 1,500 Drosophila researchers from all over the world, who were treated to amazing presentations in 18 platform sessions encompassing 136 talks, 13 workshops, and around 1,000 posters on a broad spectrum of biomedical topics. The meeting opened with a welcome and opening remark from Susan Celnikar. It was followed by Larry Sandler Memorial Lecture by Adam Friedman from Norbert Perrimon's group, HHMI at Harvard Medical School. The president of Drosophila board Utpal Bannerjee (University of California, Los Angeles) gave a memorial tribute to his mentor Seymour Benzer who died at the age of 86 on Nov. 30, 2007. Seymour, a highly accomplished geneticist and neurobiologist, made history by discovering that genes were structured like words. He went on to do pioneering work on the ties between genes and behavior, memory, and longevity. The historical keynote address was delivered by Antonio Garcia-Bellido, a scientist who specializes in genetic regulation of development and differentiation. A student of the noted British entomologist Sir Vincent Wigglesworth, Garcia-Bellido started his studies of cell heredity and determination as a postdoctoral fellow with Ernest Hadorn at the University of Zurich, and subsequently at Cal Tech with future Nobel Laureate Ed Lewis (1996). While at Hadorn's lab, Garcia-Bellido mastered the method of culturing imaginal disc cells of Drosophila larvae in the abdomen of sterile adult females and exploited its unique advantages for studying the properties of imaginal disc cells of mutants of the bithorax complex (BX-C). Garcia-Bellido's talk covered major landmarks of his journey through the field of Drosophila genetics and development. The first plenary session opened with the presentation of the 2008 Image Award. The Image Award is an initiative to recognize the most striking image that clearly conveys an important biological result. Eric Lecuyer (University of Toronto, Canada) received the 2008 Image Award for the image “Global Analysis of mRNA localization.” Lecuyer et al. conducted a high-resolution FISH analysis of approximately 25% of mRNAs encoded in the Drosophila genome to assess the overall variety and prevalence of mRNA localization events on a genomic level. They found that the majority of sampled mRNAs (71%) are subcellularly localized and that transcripts with similar localization patterns are often functionally related. The two runners up were S. Silver for the image “A microRNA that can activate Wingless signaling,” and G.S. Jefferis for the image “Mapping Pheromone and Fruit Odor Representations.” Interestingly, science and art came together at the San Diego meeting when another image award went to Joanne Topol, a scientist turned artist, who designed the cover of the 2008 abstract book (Fig. 1). Cover page of the abstract book of 49th Annual Drosophila Research Conference held at San Diego from April 2–6, 2008. Courtesy: Genetics Society of America (GSA). The first talk of this session was from David Bilder (University of California, Berkeley) entitled “Trafficking and polarity in the control of Drosophila growth”. Using the recently identified neoplastic tumor suppressor gene avalanche (avl) as an example, Bilder presented evidence suggesting that normal epithelial apical–basal polarity of cells and protein trafficking are both required for normal growth control. They observed that Crumbs (Crb) and Notch (N) were up-regulated in cells mutant for avl, suggesting that either avl mutant cells are defective in polarity, or are unable to degrade these proteins causing their accumulation. Further experiments revealed that proper polarity is required for proliferation control. Because N signaling targets are unaffected in avl mutant cells, they turned their attention to N trafficking and found that both exocytosis and endocytosis are important for cell polarity and for cells to exit the cell cycle. These findings open up new and exciting avenues for studying the regulation of growth and polarity in fruit flies. The next talk entitled “Ig receptor diversity in insect immunity and neuronal wiring” was from Dietmar Schmucker (Harvard Medical School, Cambridge, MA). Dietmar identified a Drosophila protein (Dscam), a member of the immunoglobulin super family that is highly related to the human protein Down Syndrome Cell Adhesion Molecule (DSCAM) that can form 38,000-protein isoforms through alternative splicing and is specifically expressed on the surface of growing nerves. The extraordinary molecular diversity of the Dscam receptor, unlike other receptors expressed in the nervous system, is reminiscent of immunoglobulin receptors in the immune system. In mammals, receptor functions and signal transduction mechanisms are remarkably similar between the nervous system and the immune system. Schumucker found that the hypervariable neuronal receptor Dscam is also expressed in the immune system of flies. In fact, Drosophila immune-competent cells have the potential to express more than 18,000 isoforms of the Dscam receptor. These findings suggest an unsuspected molecular complexity of the innate immune system of insects. Artyom Kopp from the University of California, Davis talked about the cross regulatory interactions between Hox and sex determination genes and its implications for development and evolution. Steve Cohen (Temasek Life Sciences Laboratory, Singapore) talked on the different strategies by which “microRNA functions” are carried out. Cohen presented evidence that microRNAs function to “fine tune” the activity of target genes, for example, mir-8 regulates the levels and activity of its target gene atrophin. Loss of mir-8 results in elevated Atrophin activity causing apoptosis in the brain. However, reducing levels of Atrophin below the level generated by mir-8 regulation causes additional defects suggesting that mir-8 tunes the levels of Atrophin and does not completely eliminate it for its normal function. In addition, miRNAs can play essential roles by limiting errors and setting thresholds in the contexts of positive autoregulatory systems. MicroRNAs may also function by a temporal rather than spatial mechanism to clear mRNAs from the cell. Cohen summarized the computational and experimental approaches designed by his group aimed at identifying all microRNAs from the fly genome. Michael Ashburner (Cambridge University, United Kingdom) received the Thomas Hunt Morgan Medal for outstanding contributions to the field of genetics from GSA president Utpal Bannerjee at a champagne reception. Due to the broad spectrum of topics and information presented in the meeting, we will focus on some of the common themes/topics in this commentary. During early eye development, generation of dorsal (D) and ventral (V) compartments is the first lineage restriction event. The border between the dorsal and ventral compartments is known as the equator and is the site of activation of N signaling that regulates cell proliferation and differentiation of the developing eye. The members of N signaling pathway, Lobe (L) and Serrate (Ser) play an important role in ventral eye growth and development. Amit Singh (University of Dayton, Dayton, OH) and Kwang Choi (Baylor College of Medicine, Houston, TX) identified homothorax (hth), a Meis class gene which is a negative regulator of eye development, as a strong enhancer of the L mutant phenotype in a genetic modifier screen. Loss-of-function of hth, results in ectopic ventral eye enlargements, which is complementary to the L or Ser mutant phenotype of loss-of-ventral-eye. Ectopic induction of Hth was seen in loss-of-function clones of L or Ser in the ventral eye. They presented evidence that L and hth act antagonistically to each other to define the ventral boundary of the eye. The complex eye–antennal imaginal disc of Drosophila that arises from the 20–30 cell anlagen located bilaterally in the embryonic anterior, gives rise to the adult eye and the antenna. An important question is how and when the decision of division of eye–antennal disc to eye and antennal region takes places during development. During late larval and pupal development, the anterior lobe of this disc gives rise to the antenna, while the posterior lobe gives rise to the eye. Cheng-wei Wang (Y. Henry Sun's group, Academia Sinica, Taipei, Taiwan) found that the restricted expression of markers such as eyeless (ey) in the eye field and cut in the antennal field could antagonize each other for the restriction of eye and antennal identity, respectively. They put forth an interesting hypothesis that reciprocal interaction between the eye selector gene ey and antennal identity gene cut may be required to determine eye and antennal identity. The developing compound eye is an excellent model system for elucidating the molecular links between cell proliferation and tissue specification, and their role in generating the final shape and size of an organ. If this check and balance on cell proliferation is altered, then tumorigenesis and cancer may result. During early development cell proliferation is actively promoted favoring the increased ratio of undifferentiated cells to the differentiated ones. Shera Lesly (Justin Kumar's group, Indiana University, Bloomington, IN) showed that when eye specification gene function is abolished from entire eye it results in a no-eye or small eye phenotype, as was previously known. However, when eye-specification gene function is abolished in only a subset of cells using a genetic mosaic approach, there is a rescuing communication between mutant and normal cells in the early eye disc which is crucial for balancing the rates of cell proliferation and tissue determination, thereby regulating/restoring the size of the eye. She found that the N pathway mediates this balancing act. The differentiation of many cell types, including retinal pigment epithelium (RPE), is controlled by the Microphthalmia-related transcription factor (Mitf) which encodes a basic Helix-Loop-Helix Zip (bHLH-Zip) protein. The aberrant expression of Mitf is the cause of cancers like melanoma and clear cell carcinoma. Tianyi Zhang (Francesca Pignoni's group, Harvard Medical School/MEEI, Boston, MA) found that targeted overexpression of either Drosophila or mouse Mitf (dMitf or mMitf) and suppresses eye development by down-regulating two retina specification genes: eyes absent (eya) and ey. dMitf or mMitf can suppress proliferation autonomously, but induce proliferation nonautonomously. Of interest, Mitf-expressing cells often down-regulate the cell polarity gene disc large (dlg) and move out of the imaginal disc epithelium. Aditya Sen (Deborah Hursh's group, CBER/FDA, Bethesda, MD) used the SELEX (Systematic Evolution of Ligands by Exponential Enrichment) approach to determine potential targets for the pair-rule gene, Odd-paired (Opa), a homolog of the Zic (Zinc finger protein in the cerebellum) family of mammalian transcription factors, during postembryonic development results in ventral head formation defects. This is an interesting tool/method that many researchers might find useful in finding targets of their gene of interest. There are many signaling pathways involved in eye development. The JAK-STAT pathway, a well-conserved signaling cascade from vertebrates to Drosophila, is one of the important pathways involved in eye development and growth. In Drosophila, the secreted glycoprotein, Unpaired (Upd) has been shown to activate the JAK/STAT pathway. It is expressed at the central point of the posterior margin in the eye disc. Upd is important for morphogenetic furrow initiation and for long-range control of cell proliferation in the eye disc. However, how Upd is regulated in the developing eye is still unknown. Chuan-Ju Wang, (Y. Henry Sun's group) used loss-of-function and gain-of-function approaches to show that (1) Decapentaplegic (Dpp) and Hedgehog (Hh) signaling cooperate with the N signaling pathway to activate Upd expression and (2) Wingless (Wg) signaling negatively regulates Upd expression. They also identified potential binding sites of several transcriptional factors in the eye-specific enhancer region of upd. The upd gene is located in polytene band 17A. Two predicted genes, upd2 and upd3 with sequence similarity are present within 70 kb of upd. Classic mutations, described as outstretched (os), have been defined as alleles of upd. The two upd alleles, updYM55 and updYC43, cause embryonic lethality and os alleles, oso, oss, os1, result in outstretched wings, small eyes, or both. Liqun Wang (Doug Harrison's group, University of Kentucky, Lexington) identified additional mutations in the upd region that genetically separate the os and upd loci. They suggested that the upd-like genes are close to upd on the X-chromosome and show sequence similarity with upd, therefore, it is possible that os phenotypes may result from mutations in upd-like genes, disproving the long-held belief that os is an upd allele. The JAK/STAT pathway regulates growth by balancing proliferation and apoptosis. Using loss- and gain-of-function approaches, Aloma Rodrigues (Erika Bach's group, NYU School of Medicine, New York, NY) presented that cells lacking stat92E (the sole Drosophila STAT) are eliminated, most likely by cell competition, suggesting the interesting possibility that JAK/STAT signaling promotes a cell's ability to compete. Laura Ekas et al. (Erika Bach's group) reported structure function analysis of the 761 amino acid Stat92E protein. They showed that the Stat92E lacking both the N- and C-terminal domains activates a STAT-dependent luciferase reporter significantly more than wild-type Stat92E and is a gain-of-function allele. Both the N- and C-terminal domains of mammalian STATs have been shown to be critical for maximal transcriptional activation suggesting that there may be significant functional differences between Stat92E and mammalian STATs. During normal eye development in Drosophila, several gene pairs function to specify the retina. The eye specification network or retinal determination (RD) network consists of ten nuclear proteins that are woven into a complicated regulatory hierarchy. Claire Salzer (Justin Kumar's group) used retinal mosaic clones of sine oculis (so), eya, and dachshund (dac) to reexamine the regulatory relationships among the pathway members. The current model suggests that the So-Eya protein complex promotes dac expression. She found that this relationship holds true only ahead of the morphogenetic furrow and in the first few columns of developing ommatidia. However, in more posterior regions of the retina both so and eya cooperate to repress dac. Of interest, the So-Eya complex can switch between activation and repression states depending upon their localization within the developing eye field, reinforcing the need to critically examine well-characterized pathways and genes. Eyegone (eyg) encodes a Pax transcription factor and is important for Drosophila eye development. Eyg expression begins in the embryonic eye-antennal primordia (EAP) and continues to the larval eye disc. twin of eyegone (toe), a paralog of eyg in Drosophila, is located 30 kb apart from eyg on chromosome 3L. Lan-hsin Wang (Y. Henry Sun's group) dissected the eyg-toe locus to identify its eye-specific cis-regulatory elements to understand the dynamic changes in the transcriptional regulation of eyg during eye development. They identified two cis-regulatory elements, B8 and E2, which have distinctly different enhancer activities. They showed that the eyg/Pax gene is temporally regulated by these separate enhancers to achieve head and antennal development during the first and third larval instar, and eye development during the second instar. N signaling regulates eyg only during the second larval instar through the B8 enhancer. In line with the important function of eyg, Yu-Chen Tsai et al. (Y. Henry Sun's group and Gert O. Pflugfelder's group, Universität Mainz, Germany) presented that optomotor-blind (omb), a T-box transcription factor, is a negative regulator of eye development as omb mutants have enlarged eyes. Ectopic expression of omb inhibits cell proliferation, morphogenetic furrow initiation and retinal differentiation. Of interest, they found that eyg represses omb to specify eye territory. During normal eye development in Drosophila, several gene pairs function to specify the retina. Abanti Chattopadhyay (Rui Chen's group, Baylor College of Medicine, Houston, TX) presented her studies on eyg and toe gene pair. They showed that toe plays a redundant role with eyg. Rhea Dutta (Justin Kumar's group) studied the structural differences between another gene pair - teashirt (tsh) and tiptop (tio), two transcription factors that are actively involved in eye development. Using a combinatorial approach of microarray analysis and phylogenetic shadowing, Yumei Li et al. (Graeme Mardon's and Rui Chen's groups, Baylor College of Medicine, Houston, TX) have identified optix (opt) as a direct downstream target of Ey during retinal development in Drosophila. Like other known RD genes, opt is expressed before morphogenetic furrow initiation and anterior to the morphogenetic furrow in eye imaginal discs. Misexpression of Opt is sufficient to induce ectopic eye formation. The Drosophila compound eye is composed of approximately 750 ommatidia, each containing six outer photoreceptor cells (R1–R6) and two inner photoreceptor cells (R7 and R8). Drosophila R7 photoreceptors are by activation of both N signaling and receptor signaling In of R7 cells to photoreceptor the R7 cells the cell group, NY) identified the gene, which encodes an protein that transcription factor activity by with is an of N during R7 and cell development. The gene is also required for other of retinal differentiation like the differentiation of R7 cells by ectopic N activity and development of Zhang (Francesca Pignoni's group) presented the of the regulation of early expression in Drosophila eye. major proteins in the network of most cells, play a role in photoreceptor There are in and (Baylor University, TX) and Kwang Choi (Baylor College of Medicine, Houston, TX) showed that is not essential for retinal differentiation in the larval eye imaginal disc. However, all are required for localization of apical–basal polarity proteins during pupal retinal development suggesting a need to examine phenotypes in the and not differentiation. In line with this University, and Utpal Bannerjee (University of California, Los Angeles) the role of protein in eye development. While they found that larval eye development is normal in the pupal development has defects in cells, and is the only phenotype, it is clear that plays many roles in the eye. group, Research OH) presented evidence that a transcription factor that functions as a molecular switch for cell proliferation and differentiation within larval system, mediates cell of R7 cell development during group) showed that a Drosophila to the finger transcription factor, plays an role to by both negatively and during differentiation. Of interest, has recently been shown to function as a tumor is a well-characterized may be important in many biological group showed that a tumor and a growth control the specification of the David group, New University, New York, NY) the complex photoreceptor through a signaling pathway or by signaling pathway members. The protein can act of in its tumor suppressor function. They found that is required for specification, but and members of growth control are not express receptors to by one receptor group) from proteins in the of gene expression. They found that the signal does not in the but rather to identity in the genetic have been the for of of genetic in Drosophila, we have to present some of the different The RD gene cascade in Drosophila consists of ten nuclear factors and the protein There is a need to identify other genes involved in eye development. (Justin Kumar's group) followed a genetic approach to for new RD genes. of these genes within the developing eye to a in retinal development, while expression of all of these genes the of is sufficient to induce eye formation in several Drosophila eye development is regulated by control gene which is both essential and sufficient to form the eye. Rui and conducted a to identify downstream targets of ey using (1) gene expression in both and loss-of-function genetic (2) several computational approaches to a of potential direct Ey protein binding elements, and genome experiments using and to identify Ey binding sites in the fly genome. They have identified many genes with several genes that ey with other genetic such as and In the Drosophila each photoreceptors in a The mechanism photoreceptor is regulated by the N and The different photoreceptors are by several including and expression. The inner photoreceptors (R7 and in the of the shape which is by the outer photoreceptors group) reported a all known transcription factors to understand the regulatory mechanisms the determination and of outer a protein in Drosophila is required for the proper formation of the photoreceptor cell in the developing retina (University of the Sciences in identified new genes with function and involved in retinal development in a for enhancers of a loss-of-function eye phenotype in Drosophila. differentiation by the morphogenetic furrow signaling by and group, New University Medical New York, NY) presented the results of a mosaic genetic to identify mutations on the X-chromosome that the normal of photoreceptor differentiation. They with mutations that clones of cells from as retinal but the cells to to eye They mutations in members of the growth factor receptor and as as known transcription factors and genes. group, University of presented a modifier to that with the Drosophila The mutations in Drosophila complex show similar to such as eye defects and a et al. used a phenotype seen in and mutants as a for several modifier and found of the complex that to the and signaling pathways as as and genes involved in This session covered many interesting topics from immune of tumor cells, and to cell by and the mechanisms of cell in tissue group, University School of Medicine, New presented evidence that Drosophila imaginal have on the surface of the disc and increased of in the of cell by expression of the gene in the tumor growth that tumor growth. the et al. imaginal and the a similar in both to the proliferation was not In addition, presented evidence suggesting that tissue innate immune may the of and JAK-STAT Wang group, University of used molecular and strategies to which protein and the binding protein are essential to recognize the positive among the Wang showed that and could to from all of positive and may be receptors for other more complex interactions may be possible for do recognize is the innate immune is involved in activation of pathway in there a similar involved in the activation of the Drosophila immune pathway used of the mammalian in and found that it Drosophila pathway by of the receptor. with but not expression. and that receptor may induce a strong innate immune and also tissue Two on the mechanisms of cell during pupal Both University of Medical School, MA) and of presented by Germany) play a role in of cells growth before cell However, mutants to degrade and show markers for both and cell Analysis of growth in mutants suggests that they are defective at and the growth is and to defects in localization of These findings that signaling may be to cell growth and regulation of cell in to cell and cell In cells are of proliferation of cells to tissue In the Drosophila imaginal it has been shown that cells

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