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Drosophila: A Versatile Model in Biology and Medicine
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Drosophila: A Versatile Model in Biology and Medicine

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Biology".

Deadline for manuscript submissions: closed (15 September 2024) | Viewed by 19906

Special Issue Editors

Dr. Maria Grazia Giansanti

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Guest Editor
Dipartimento di Biologia e Biotecnologie, Istituto di Biologia e Patologia Molecolari del Consiglio Nazionale delle Ricerche, Università Sapienza di Roma, Piazzale Aldo Moro 5, 00185 Rome, Italy
Interests: drosophila melanogaster; drosophila model; oncoprotein; cytokinesis
Special Issues, Collections and Topics in MDPI journals
Dr. Roberto Piergentili

E-Mail Website
Guest Editor
Dipartimento di Biologia e Biotecnologie, Istituto di Biologia e Patologia Molecolari del Consiglio Nazionale delle Ricerche (IBPM-CNR), Università Sapienza di Roma, Piazzale Aldo Moro 5, 00185 Rome, Italy
Interests: chromatin structure and function; heterochromatin; drosophila melanogaster; mitosis and male meiosis; cytokinesis; DNA repair; cancer epigenetics
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Since the year 1901, thanks to the pioneering work of the entomologist Charles W. Woodworth, Drosophila melanogaster has been pointed out as a highly suitable model organism to study processes that are conserved in all eukaryotic cells. Since then, the fruit fly has been used to study cell proliferation and metabolism, genetics, physiology, microbial pathogenesis, and life history evolution. Indeed, studies on the fruit fly have, to date, been awarded five Nobel Prizes for “Physiology or Medicine” collectively: in 1933, for discovering the role played by chromosomes in heredity (Morgan); in 1946, for the production of mutations by means of X-ray irradiation (Muller); in 1995, for the study of the genetic control of early embryonic development (Lewis, Nüsslein-Volhard, and Wieschaus); in 2011, for understanding how receptors detect microorganisms and activate innate immunity (Hoffmann); and in 2017, for unveiling the molecular mechanisms controlling the circadian rhythm (Hall, Rosbash, and Young). It is currently estimated that about 75% of known human disease genes have a recognizable, functional homologue in fruit flies, including the genes involved in important human pathologies such as Down’s syndrome, Alzheimer’s disease, autism, diabetes, and most—if not all—types of cancer. Drosophila is also a very valuable tool in the study of rare human diseases, where developing vertebrate disease models poses fundamental challenges. In addition, in recent years, Drosophila has also been effectively used for low- to high-throughput drug screens and target discovery in the context of therapeutic tests for central nervous system disorders, inflammatory disorders, cardiovascular disease, cancer, and diabetes. According to PubMed, in 2022, almost 1,800 papers had been published reporting the keywords “Drosophila melanogaster”, showing that this model system is still enormously useful, even after more than 120 years of history.

The aim of this Special Issue is to collect the most up-to-date research showing the use of the fruit fly to study human conditions. We welcome the submission of original research and review articles in this field and all contributions which provide novel insights into how Drosophila models have contributed remarkably to our understanding of human pathologies.

Dr. Maria Grazia Giansanti
Dr. Roberto Piergentili
Guest Editors

Manuscript Submission Information

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. International Journal of Molecular Sciences is an international peer-reviewed open access semimonthly journal published by MDPI.

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Keywords

  • model organism
  • human disease
  • inherited disease
  • cancer
  • neurodegeneration
  • rare disease
  • genetics

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Published Papers (10 papers)

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Research

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15 pages, 4932 KiB  
Article
The Impact of the Angiotensin-Converting Enzyme Inhibitor Lisinopril on Metabolic Rate in Drosophila melanogaster
by Denise Vecchie’, Julia M. Wolter, Jesse Perry, Patricia Jumbo-Lucioni and Maria De Luca
Int. J. Mol. Sci. 2024, 25(18), 10103; https://doi.org/10.3390/ijms251810103 - 20 Sep 2024
Cited by 1 | Viewed by 978
Abstract
Evidence suggests that angiotensin-converting enzyme inhibitors (ACEIs) may increase metabolic rate by promoting thermogenesis, potentially through enhanced fat oxidation and improved insulin. More research is, however, needed to understand this intricate process. In this study, we used 22 lines from the Drosophila Genetic [...] Read more.
Evidence suggests that angiotensin-converting enzyme inhibitors (ACEIs) may increase metabolic rate by promoting thermogenesis, potentially through enhanced fat oxidation and improved insulin. More research is, however, needed to understand this intricate process. In this study, we used 22 lines from the Drosophila Genetic Reference Panel to assess the metabolic rate of virgin female and male flies that were either fed a standard medium or received lisinopril for one week or five weeks. We demonstrated that lisinopril affects the whole-body metabolic rate in Drosophila melanogaster in a genotype-dependent manner. However, the effects of genotypes are highly context-dependent, being influenced by sex and age. Our findings also suggest that lisinopril may increase the Drosophila metabolic rate via the accumulation of a bradykinin-like peptide, which, in turn, enhances cold tolerance by upregulating Ucp4b and Ucp4c genes. Finally, we showed that knocking down Ance, the ortholog of mammalian ACE in Malpighian/renal tubules and the nervous system, leads to opposite changes in metabolic rate, and that the effect of lisinopril depends on Ance in these systems, but in a sex- and age-specific manner. In conclusion, our results regarding D. melanogaster support existing evidence of a connection between ACEI drugs and metabolic rate while offering new insights into this relationship. Full article
(This article belongs to the Special Issue Drosophila: A Versatile Model in Biology and Medicine)
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23 pages, 11416 KiB  
Article
Orthologs of NOX5 and EC-SOD/SOD3: dNox and dSod3 Impact Egg Hardening Process and Egg Laying in Reproductive Function of Drosophila melanogaster
by Eva Louise Steinmetz, Annika Scherer, Célestine Calvet and Uli Müller
Int. J. Mol. Sci. 2024, 25(11), 6138; https://doi.org/10.3390/ijms25116138 - 2 Jun 2024
Viewed by 1230
Abstract
The occurrence of ovarian dysfunction is often due to the imbalance between the formation of reactive oxygen species (ROS) and the ineffectiveness of the antioxidative defense mechanisms. Primary sources of ROS are respiratory electron transfer and the activity of NADPH oxidases (NOX) while [...] Read more.
The occurrence of ovarian dysfunction is often due to the imbalance between the formation of reactive oxygen species (ROS) and the ineffectiveness of the antioxidative defense mechanisms. Primary sources of ROS are respiratory electron transfer and the activity of NADPH oxidases (NOX) while superoxide dismutases (SOD) are the main key regulators that control the levels of ROS and reactive nitrogen species intra- and extracellularly. Because of their central role SODs are the subject of research on human ovarian dysfunction but sample acquisition is low. The high degree of cellular and molecular similarity between Drosophila melanogaster ovaries and human ovaries provides this model organism with the best conditions for analyzing the role of ROS during ovarian function. In this study we clarify the localization of the ROS-producing enzyme dNox within the ovaries of Drosophila melanogaster and by a tissue-specific knockdown we show that dNox-derived ROS are involved in the chorion hardening process. Furthermore, we analyze the dSod3 localization and show that reduced activity of dSod3 impacts egg-laying behavior but not the chorion hardening process. Full article
(This article belongs to the Special Issue Drosophila: A Versatile Model in Biology and Medicine)
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14 pages, 4520 KiB  
Article
A Novel Drosophila Model of Alzheimer’s Disease to Study Aβ Proteotoxicity in the Digestive Tract
by Greta Elovsson, Therése Klingstedt, Mikaela Brown, K. Peter R. Nilsson and Ann-Christin Brorsson
Int. J. Mol. Sci. 2024, 25(4), 2105; https://doi.org/10.3390/ijms25042105 - 9 Feb 2024
Viewed by 2476
Abstract
Amyloid-β (Aβ) proteotoxicity is associated with Alzheimer’s disease (AD) and is caused by protein aggregation, resulting in neuronal damage in the brain. In the search for novel treatments, Drosophila melanogaster has been extensively used to screen for anti-Aβ proteotoxic agents in studies where toxic [...] Read more.
Amyloid-β (Aβ) proteotoxicity is associated with Alzheimer’s disease (AD) and is caused by protein aggregation, resulting in neuronal damage in the brain. In the search for novel treatments, Drosophila melanogaster has been extensively used to screen for anti-Aβ proteotoxic agents in studies where toxic Aβ peptides are expressed in the fly brain. Since drug molecules often are administered orally there is a risk that they fail to reach the brain, due to their inability to cross the brain barrier. To circumvent this problem, we have designed a novel Drosophila model that expresses the Aβ peptides in the digestive tract. In addition, a built-in apoptotic sensor provides a fluorescent signal from the green fluorescent protein as a response to caspase activity. We found that expressing different variants of Aβ1–42 resulted in proteotoxic phenotypes such as reduced longevity, aggregate deposition, and the presence of apoptotic cells. Taken together, this gut-based Aβ-expressing fly model can be used to study the mechanisms behind Aβ proteotoxicity and to identify different substances that can modify Aβ proteotoxicity. Full article
(This article belongs to the Special Issue Drosophila: A Versatile Model in Biology and Medicine)
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13 pages, 4200 KiB  
Article
A Drosophila Model Reveals the Potential Role for mtt in Retinal Disease
by Wenfeng Chen, Wenmiao Zhong, Lingqi Yu, Xiang Lin, Jiayu Xie and Zhenxing Liu
Int. J. Mol. Sci. 2024, 25(2), 899; https://doi.org/10.3390/ijms25020899 - 11 Jan 2024
Viewed by 1369
Abstract
Congenital stationary night blindness (CSNB) is a genetically heterogeneous inherited retinal disorder, caused by over 300 mutations in 17 different genes. While there are numerous fly models available for simulating ocular diseases, most are focused on mimicking retinitis pigmentosa (RP), with animal models [...] Read more.
Congenital stationary night blindness (CSNB) is a genetically heterogeneous inherited retinal disorder, caused by over 300 mutations in 17 different genes. While there are numerous fly models available for simulating ocular diseases, most are focused on mimicking retinitis pigmentosa (RP), with animal models specifically addressing CSNB limited to mammals. Here, we present a CSNB fly model associated with the mtt gene, utilizing RNA interference (RNAi) to silence the mtt gene in fly eyes (homologous to the mammalian GRM6 gene) and construct a CSNB model. Through this approach, we observed significant defects in the eye structure and function upon reducing mtt expression in fly eyes. This manifested as disruptions in the compound eye lens structure and reduced sensitivity to light responses. These results suggest a critical role for mtt in the function of fly adult eyes. Interestingly, we found that the mtt gene is not expressed in the photoreceptor neurons of adult flies but is localized to the inner lamina neurons. In summary, these results underscore the crucial involvement of mtt in fly retinal function, providing a framework for understanding the pathogenic mechanisms of CSNB and facilitating research into potential therapeutic interventions. Full article
(This article belongs to the Special Issue Drosophila: A Versatile Model in Biology and Medicine)
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9 pages, 2284 KiB  
Communication
Tyrosine Metabolism Pathway Is Downregulated in Dopaminergic Neurons with LRRK2 Overexpression in Drosophila
by Jack Cheng, Bor-Tsang Wu, Hsin-Ping Liu and Wei-Yong Lin
Int. J. Mol. Sci. 2023, 24(21), 15587; https://doi.org/10.3390/ijms242115587 - 25 Oct 2023
Cited by 1 | Viewed by 2059
Abstract
LRRK2 mutations are the leading cause of familial Parkinson’s disease (PD) and are a significant risk factor for idiopathic PD cases. However, the molecular mechanisms underlying the degeneration of dopaminergic (DA) neurons in LRRK2 PD patients remain unclear. To determine the translatomic impact [...] Read more.
LRRK2 mutations are the leading cause of familial Parkinson’s disease (PD) and are a significant risk factor for idiopathic PD cases. However, the molecular mechanisms underlying the degeneration of dopaminergic (DA) neurons in LRRK2 PD patients remain unclear. To determine the translatomic impact of LRRK2 expression in DA neurons, we employed gene set enrichment analysis (GSEA) to analyze a translating ribosome affinity purification (TRAP) RNA-seq dataset from a DA-neuron-specific-expressing Drosophila model. We found that the tyrosine metabolism pathway, including tyrosine hydroxylase (TH), is downregulated in DA neurons with LRRK2 overexpression; in contrast, the Hippo signaling pathway is downregulated in the G2019S mutant compared to wild-type LRRK2 in the DA neurons. These results imply that the downregulation of tyrosine metabolism occurs before pronounced DA neuron loss and that LRRK2 may downregulate the tyrosine metabolism in a DA-neuron-loss-independent way. Full article
(This article belongs to the Special Issue Drosophila: A Versatile Model in Biology and Medicine)
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Review

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29 pages, 820 KiB  
Review
Decoding Nucleotide Repeat Expansion Diseases: Novel Insights from Drosophila melanogaster Studies
by Sandra Atienzar-Aroca, Marleen Kat and Arturo López-Castel
Int. J. Mol. Sci. 2024, 25(21), 11794; https://doi.org/10.3390/ijms252111794 - 2 Nov 2024
Viewed by 1494
Abstract
Drosophila melanogaster usage has provided substantial insights into the pathogenesis of several nucleotide repeat expansion diseases (NREDs), a group of genetic diseases characterized by the abnormal expansion of DNA repeats. Leveraging the genetic simplicity and manipulability of Drosophila, researchers have successfully modeled close [...] Read more.
Drosophila melanogaster usage has provided substantial insights into the pathogenesis of several nucleotide repeat expansion diseases (NREDs), a group of genetic diseases characterized by the abnormal expansion of DNA repeats. Leveraging the genetic simplicity and manipulability of Drosophila, researchers have successfully modeled close to 15 NREDs such as Huntington’s disease (HD), several spinocerebellar ataxias (SCA), and myotonic dystrophies type 1 and 2 (DM1/DM2). These models have been instrumental in characterizing the principal associated molecular mechanisms: protein aggregation, RNA toxicity, and protein function loss, thus recapitulating key features of human disease. Used in chemical and genetic screenings, they also enable us to identify promising small molecules and genetic modifiers that mitigate the toxic effects of expanded repeats. This review summarizes the close to 150 studies performed in this area during the last seven years. The relevant highlights are the achievement of the first fly-based models for some NREDs, the incorporation of new technologies such as CRISPR for developing or evaluating transgenic flies containing repeat expanded motifs, and the evaluation of less understood toxic mechanisms in NREDs such as RAN translation. Overall, Drosophila melanogaster remains a powerful platform for research in NREDs. Full article
(This article belongs to the Special Issue Drosophila: A Versatile Model in Biology and Medicine)
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14 pages, 1494 KiB  
Review
Drosophila melanogaster as an Alternative Model to Higher Organisms for In Vivo Lung Research
by Birte Ehrhardt, Thomas Roeder and Susanne Krauss-Etschmann
Int. J. Mol. Sci. 2024, 25(19), 10324; https://doi.org/10.3390/ijms251910324 - 25 Sep 2024
Viewed by 1609
Abstract
COPD and asthma are lung diseases that cause considerable burden to more than 800 million people worldwide. As both lung diseases are so far incurable, it is mandatory to understand the mechanisms underlying disease development and progression for developing novel therapeutic approaches. Exposures [...] Read more.
COPD and asthma are lung diseases that cause considerable burden to more than 800 million people worldwide. As both lung diseases are so far incurable, it is mandatory to understand the mechanisms underlying disease development and progression for developing novel therapeutic approaches. Exposures to environmental cues such as cigarette smoke in earliest life are known to increase disease risks in the individual’s own future. To explore the pathomechanisms leading to later airway disease, mammalian models are instrumental. However, such in vivo experiments are time-consuming and burdensome for the animals, which applies in particular to transgenerational studies. Along this line, the fruit fly Drosophila melanogaster comes with several advantages for research in this field. The short lifespan facilitates transgenerational studies. A high number of evolutionary conserved signaling pathways, together with a large toolbox for tissue-specific gene modification, has the potential to identify novel target genes involved in disease development. A well-defined airway microbiome could help to untangle interactions between disease development and microbiome composition. In the following article, Drosophila melanogaster is therefore presented and discussed as an alternative in vivo model to investigate airway diseases that can complement and/or replace models in higher organisms. Full article
(This article belongs to the Special Issue Drosophila: A Versatile Model in Biology and Medicine)
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Graphical abstract

17 pages, 1472 KiB  
Review
A Closer Look at Histamine in Drosophila
by Cinzia Volonté, Francesco Liguori and Susanna Amadio
Int. J. Mol. Sci. 2024, 25(8), 4449; https://doi.org/10.3390/ijms25084449 - 18 Apr 2024
Viewed by 1870
Abstract
The present work intends to provide a closer look at histamine in Drosophila. This choice is motivated firstly because Drosophila has proven over the years to be a very simple, but powerful, model organism abundantly assisting scientists in explaining not only normal [...] Read more.
The present work intends to provide a closer look at histamine in Drosophila. This choice is motivated firstly because Drosophila has proven over the years to be a very simple, but powerful, model organism abundantly assisting scientists in explaining not only normal functions, but also derangements that occur in higher organisms, not excluding humans. Secondly, because histamine has been demonstrated to be a pleiotropic master molecule in pharmacology and immunology, with increasingly recognized roles also in the nervous system. Indeed, it interacts with various neurotransmitters and controls functions such as learning, memory, circadian rhythm, satiety, energy balance, nociception, and motor circuits, not excluding several pathological conditions. In view of this, our review is focused on the knowledge that the use of Drosophila has added to the already vast histaminergic field. In particular, we have described histamine’s actions on photoreceptors sustaining the visual system and synchronizing circadian rhythms, but also on temperature preference, courtship behavior, and mechanosensory transmission. In addition, we have highlighted the pathophysiological consequences of mutations on genes involved in histamine metabolism and signaling. By promoting critical discussion and further research, our aim is to emphasize and renew the importance of histaminergic research in biomedicine through the exploitation of Drosophila, hopefully extending the scientific debate to the academic, industry, and general public audiences. Full article
(This article belongs to the Special Issue Drosophila: A Versatile Model in Biology and Medicine)
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25 pages, 7622 KiB  
Review
Mitochondrial Differentiation during Spermatogenesis: Lessons from Drosophila melanogaster
by Viktor Vedelek, Ferenc Jankovics, János Zádori and Rita Sinka
Int. J. Mol. Sci. 2024, 25(7), 3980; https://doi.org/10.3390/ijms25073980 - 3 Apr 2024
Viewed by 2355
Abstract
Numerous diseases can arise as a consequence of mitochondrial malfunction. Hence, there is a significant focus on studying the role of mitochondria in cancer, ageing, neurodegenerative diseases, and the field of developmental biology. Mitochondria could exist as discrete organelles in the cell; however, [...] Read more.
Numerous diseases can arise as a consequence of mitochondrial malfunction. Hence, there is a significant focus on studying the role of mitochondria in cancer, ageing, neurodegenerative diseases, and the field of developmental biology. Mitochondria could exist as discrete organelles in the cell; however, they have the ability to fuse, resulting in the formation of interconnected reticular structures. The dynamic changes between these forms correlate with mitochondrial function and mitochondrial health, and consequently, there is a significant scientific interest in uncovering the specific molecular constituents that govern these transitions. Moreover, the specialized mitochondria display a wide array of variable morphologies in their cristae formations. These inner mitochondrial structures are closely associated with the specific functions performed by the mitochondria. In multiple cases, the presence of mitochondrial dysfunction has been linked to male sterility, as it has been observed to cause a range of abnormal spermatogenesis and sperm phenotypes in different species. This review aims to elucidate the dynamic alterations and functions of mitochondria in germ cell development during the spermatogenesis of Drosophila melanogaster. Full article
(This article belongs to the Special Issue Drosophila: A Versatile Model in Biology and Medicine)
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21 pages, 2634 KiB  
Review
Multiple Roles of dXNP and dADD1—Drosophila Orthologs of ATRX Chromatin Remodeler
by Larisa Melnikova and Anton Golovnin
Int. J. Mol. Sci. 2023, 24(22), 16486; https://doi.org/10.3390/ijms242216486 - 18 Nov 2023
Viewed by 1812
Abstract
The Drosophila melanogaster dADD1 and dXNP proteins are orthologues of the ADD and SNF2 domains of the vertebrate ATRX (Alpha-Thalassemia with mental Retardation X-related) protein. ATRX plays a role in general molecular processes, such as regulating chromatin status and gene expression, while dADD1 [...] Read more.
The Drosophila melanogaster dADD1 and dXNP proteins are orthologues of the ADD and SNF2 domains of the vertebrate ATRX (Alpha-Thalassemia with mental Retardation X-related) protein. ATRX plays a role in general molecular processes, such as regulating chromatin status and gene expression, while dADD1 and dXNP have similar functions in the Drosophila genome. Both ATRX and dADD1/dXNP interact with various protein partners and participate in various regulatory complexes. Disruption of ATRX expression in humans leads to the development of α-thalassemia and cancer, especially glioma. However, the mechanisms that allow ATRX to regulate various cellular processes are poorly understood. Studying the functioning of dADD1/dXNP in the Drosophila model may contribute to understanding the mechanisms underlying the multifunctional action of ATRX and its connection with various cellular processes. This review provides a brief overview of the currently available information in mammals and Drosophila regarding the roles of ATRX, dXNP, and dADD1. It discusses possible mechanisms of action of complexes involving these proteins. Full article
(This article belongs to the Special Issue Drosophila: A Versatile Model in Biology and Medicine)
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