Immune–tracheal intercellular signalling coordinates the muscle injury response in Drosophila
Posted on: 25 August 2025
Preprint posted on 25 June 2025
Something SPARC’d between us and left me Breathless: Haemolymph cells turn on repair in the Drosophila tracheal system
Selected by Jonathan Townson
Categories: cell biology, developmental biology, immunology
Background
Skeletal muscles are a highly regenerative tissue that are frequently damaged through injury or stress, with small-scale damage occurring whenever physical demand is beyond a muscles comfort zone, such as during exercise that leads to a “burn” feeling or soreness afterwards. Vertebrate repair of the tissue is mediated through mobilising the vascular system to meet the metabolic demands, and through the coordination of various cell types such as macrophages and muscle stem cells (Henrot et al., 2023).
Drosophila frequently encounter natural wounding and are a powerful model organism for studying muscle injury responses . However, they lack a closed vasculature system, instead relying on a tracheal system and circulation of haemolymph. The tracheal system in Drosophila is a branched network of air-filled tubes that function to deliver oxygen to tissues, including muscle fibres (Hayashi & Kondo, 2018; Peterson & Krasnow, 2015; Sauerwald et al., 2019). The haemolymph is made up of nutrients, hormones and haemocytes, and the majority of the haemocytes are macrophage-like plasmatocytes (Banerjee et al., 2019; L. Wang et al., 2014).
In this first preprint from the Boukhatmi lab, Ammar and colleagues bridge the invertebrate and vertebrate repair mechanism by showing that, together, trachea and haemocytes coordinate the repair of damaged muscles in Drosophila.
Key findings
The team use indirect flight muscles (IFMs) in Drosophila as a model for muscle injury and repair. The IFMs are power flight through deforming the thorax to move the wings and can be injured by stabbing with a pin. They show haemocytes are recruited to injured muscle fibres where they promote extracellular matrix (ECM) remodelling and stimulate local tracheal branching to support repair of the damaged tissue.
Mhc identified as a marker of injured muscle tissue
The first challenge was to establish a reliable marker of injured muscle fibres in the IFMs. Re-expression of embryonic myosin heavy chain is an established marker of damaged fibres in vertebrates, so the team hypothesised that Myosin Heavy Chain (Mhc) expression in Drosophila may similarly indicate muscle damage.
Through immunofluorescence, they found that Mhc does localise to sites of injury; however, they showed this was not the embryonic isoform. Instead, they showed that the shorter Mhc isoform is expressed in the IFMs and is upregulated by injury (Fig. 1).
Figure 1: Immunofluorescent labelling of IFMs shows Mhc localisation to injured fibres in magenta. Different Mhc isoforms are expressed with a GFP tag showing the embryonic isoform (weeP26) is not upregulated and the long isoform (A,F,G) is not expressed, whilst the short isoform (K,L,M) is upregulated in injured fibres. Adapted from supplementary figure 1 from Ammar et al. 2025.
Haemocytes are recruited to the injury site
In mammals, macrophages are key mediators of skeletal muscle regeneration (X. Wang & Zhou, 2022), raising the possibility that Drosophila haemocytes may have an analogous role in response to injury.
The team performed immunofluorescence experiments to look at Mhc localisation and different markers of haemocytes after injury in the IFMs. They found that haemocytes are recruited to the damaged fibres, tightly attached to the tracheal cells (Fig. 2), and that some populations can persist (Pxn+ and Enh3+), whilst others are enriched and then decline over time (Hml+).
Figure 2: TOP, Immunofluorescence labelling of hameocytes using Pxn and Enh3 markers shows enrichment in injured muscles fibres (labelled by Mhc). Adapted from figure 1 in Ammar et al. 2025. BOTTOM, Enh3+ haemocytes cover the tracheal cells (A) and this coverage is increased following injury (B+D). Adapted from figure 2 in Ammar et al. 2025.
Branchless secretion from recruited haemocytes activates Breathless to mediate tracheal remodelling
Tracheal branching in response to oxygenation levels and metabolic activity has been well described during development and involves conserved signalling pathways including the ligand Branchless (Bnl), activating the Breathless (Btl) receptor (Jarecki et al., 1999; Peterson & Krasnow, 2015). Furthermore, the adult trachea has been shown to remodel to sustain adult gut regeneration through increased oxygen supply (Perochon et al., 2021; Tamamouna et al., 2021). This raises the hypothesis that a similar process may occur to repair damage in oxygen-hungry muscles.
The team observed that local hypoxia at the injury site induced tracheal branching. They further investigated if the same developmental signalling pathways mediate this response to hypoxia and found Bnl which is used reiteratively in development, is also enriched at the injury sites (Fig. 3). Furthermore, Bnl was particularly enriched surrounding haemocytes (Pxn+), and knocking down Bnl expression in haemocytes impaired tracheal invasion into the damaged tissue, without affecting haemocyte recruitment to the injury site. The secreted Bnl activates its receptor Btl on the tracheal cells, and they further showed that Btl is accumulates on the damaged fibres. This suggests that the haemocytes are responsible for the production of Bnl that turns on tracheal Btl at damaged fibres, promoting tracheal branching after tissue damage.
Figure 3: The SyHREns reporter, which labels local sites of hypoxia with GFP, shows an increase at sites of injury. Furthermore, GFP-tagged endogenous Bnl expression is detected at the injury sites. Adapted from figure 3 in Ammar et al. 2025.
Haemocytes contribute to muscle repair by remodelling the extracellular matrix
The extracellular matrix (ECM) is of critical importance in muscles and is remodelled during tracheal invasion into IFMs (Long et al., 2023; Sauerwald et al., 2019). As macrophages are also known to regulate muscle repair through ECM remodelling and haemocytes are major producers of ECM components (Banerjee et al., 2019; X. Wang & Zhou, 2022), the team hypothesised that haemocytes may contribute to the repair of IFMs through ECM remodelling.
The team first showed that Collagen IV is more abundant in the injured fibres than compared to control, and that its distribution correlated with the presence of haemocytes (Fig. 7). To determine how this may be, the team next investigated the collagen regulator SPARC (Secreted Protein, Acidic, Rich in Cysteine), which is essential for correctly integrating Collagen IV into the ECM (Duncan et al., 2020). In a neat experiment, they used a Gal4 trap line, where the Gal4 is integrated into the SPARC genomic locus to drive the expression of an RFP, thus labelling the cells which are producing SPARC. In the same experiment, they used a GFP tagged SPARC; in this way they could see the location of SPARC in the damaged tissue and which cells were producing it. With this dual reporter strategy, they showed that the haemocytes are the main source of SPARC, which was then broadly distributed along the damaged fibre (Fig. 4). Therefore, haemocytes play an active role in remodelling the ECM to promote tracheal invasion, oxidation and repair of the damaged tissue.
Figure 4: IFM injury promotes accumulation of Collagen IV (Vkg::GFP) along the injured muscle fibre (B). SPARC also accumulates and is produced by haemocytes (L and M). Adapted from figure 6 in Ammar et al. 2025.
What I like about the preprint/why I think this new work is important
I was drawn to this preprint through my enjoyment of Drosophila research and microscopy. In reading it, I really enjoyed how this preprint used the known developmental biology pathways to hypothesise and investigate the repair pathway in the IFMs. Additionally, their experiment simultaneously labelling SPARC and the cells which produced it was ingenious. In my previous preLight, I highlighted the importance of the ECM in regenerating tissue in vertebrates, here Ammar et al. have shown that the ECM is also important in repair in Drosophila. As a fly fan, I am excited to see the importance of the ECM in regeneration/repair in invertebrates and look forward to seeing more fly papers on how the ECM (and haemocytes) regulates these processes.
Future directions and questions for the authors
- Do you anticipate the short isoform of Mhc can mark damage in other types of muscle tissue? Or at other developmental stages?
- Following the recovery of the IFMs, is there a noticeable decrease in performance?
- Haemocytes also have functions in the Drosophila immune system; how do you anticipate injury repair may be impacted by infection? Similarly, is there a decrease in haemocyte recruitment at the injury site if a second injury is made elsewhere?
- Does depleting SPARC in haemocytes affect the collagen IV deposition along injured muscle fibres?
References
- Ammar, N., Josse, O., Guillou, A., Perochon, J., & Boukhatmi, H. (2025). Immune–tracheal intercellular signalling coordinates the muscle injury response in Drosophila. BioRxiv. https://doi.org/10.1101/2025.06.25.661466
- Banerjee, U., Girard, J. R., Goins, L. M., & Spratford, C. M. (2019). Drosophila as a genetic model for hematopoiesis. Genetics, 211(2), 367–417. https://doi.org/10.1534/genetics.118.300223
- Boukhatmi, H. (2021). Drosophila , an Integrative Model to Study the Features of Muscle Stem Cells in Development and Regeneration. Cells, 10(8), 2112. https://doi.org/10.3390/cells10082112
- Duncan, S., Delage, S., Chioran, A., Sirbu, O., Brown, T. J., & Ringuette, M. J. (2020). The predicted collagen-binding domains of Drosophila SPARC are essential for survival and for collagen IV distribution and assembly into basement membranes. Developmental Biology, 461(2), 197–209. https://doi.org/10.1016/j.ydbio.2020.02.011
- Hayashi, S., & Kondo, T. (2018). Development and function of the drosophila tracheal system. Genetics, 209(2), 367–380. https://doi.org/10.1534/genetics.117.300167
- Henrot, P., Blervaque, L., Dupin, I., Zysman, M., Esteves, P., Gouzi, F., Hayot, M., Pomiès, P., & Berger, P. (2023). Cellular interplay in skeletal muscle regeneration and wasting: insights from animal models. Journal of Cachexia, Sarcopenia and Muscle, 14(2), 745–757. https://doi.org/10.1002/jcsm.13103
- Jarecki, J., Johnson, E., & Krasnow, M. A. (1999). Oxygen Regulation of Airway Branching in Drosophila Is Mediated by Branchless FGF The Drosophila tracheal system is an elaborate net-work of epithelial tubes that ramifies throughout the body (Manning and Krasnow, 1993). Oxygen enters the. Cell, 99, 211–220.
- Long, A. M., Lee, G. H., Demonbreun, A. R., & McNally, E. M. (2023). Extracellular matrix contribution to disease progression and dysfunction in myopathy. American Journal of Physiology – Cell Physiology, 325(5), C1244–C1251. https://doi.org/10.1152/ajpcell.00182.2023
- Perochon, J., Yu, Y., Aughey, G. N., Medina, A. B., Southall, T. D., & Cordero, J. B. (2021). Dynamic adult tracheal plasticity drives stem cell adaptation to changes in intestinal homeostasis in Drosophila. Nature Cell Biology, 23(5), 485–496. https://doi.org/10.1038/s41556-021-00676-z
- Peterson, S. J., & Krasnow, M. A. (2015). Subcellular trafficking of FGF controls tracheal invasion of Drosophila flight muscle. Cell, 160(1–2), 313–323. https://doi.org/10.1016/j.cell.2014.11.043
- Sauerwald, J., Backer, W., Matzat, T., Schnorrer, F., & Luschnig, S. (2019). Matrix metalloproteinase 1 modulates invasive behavior of tracheal branches during entry into drosophila flight muscles. ELife, 8, 1–24. https://doi.org/10.7554/eLife.48857
- Subasi, B. S., Grabe, V., Kaltenpoth, M., Rolff, J., & Armitage, S. A. O. (2024). How frequently are insects wounded in the wild? A case study using Drosophila melanogaster. Royal Society Open Science, 11(6). https://doi.org/10.1098/rsos.240256
- Tamamouna, V., Rahman, M. M., Petersson, M., Charalambous, I., Kux, K., Mainor, H., Bolender, V., Isbilir, B., Edgar, B. A., & Pitsouli, C. (2021). Remodelling of oxygen-transporting tracheoles drives intestinal regeneration and tumorigenesis in Drosophila. Nature Cell Biology, 23(5), 497–510. https://doi.org/10.1038/s41556-021-00674-1
- Wang, L., Kounatidis, I., & Ligoxygakis, P. (2014). Drosophila as a model to study the role of blood cells in inflammation, innate immunity and cancer. Frontiers in Cellular and Infection Microbiology, 3(JAN), 1–17. https://doi.org/10.3389/fcimb.2013.00113
- Wang, X., & Zhou, L. (2022). The Many Roles of Macrophages in Skeletal Muscle Injury and Repair. Frontiers in Cell and Developmental Biology, 10(July), 1–13. https://doi.org/10.3389/fcell.2022.952249
doi: https://doi.org/10.1242/prelights.41261
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A list of preprints mentioned at the Wellcome Genome Campus Single Cell Biology 2020 meeting.
| List by | Alex Eve |
Society for Developmental Biology 79th Annual Meeting
Preprints at SDB 2020
| List by | Irepan Salvador-Martinez, Martin Estermann |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
| List by | Ana Dorrego-Rivas |
Planar Cell Polarity – PCP
This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.
| List by | Ana Dorrego-Rivas |
Cell Polarity
Recent research from the field of cell polarity is summarized in this list of preprints. It comprises of studies focusing on various forms of cell polarity ranging from epithelial polarity, planar cell polarity to front-to-rear polarity.
| List by | Yamini Ravichandran |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
| List by | Maiko Kitaoka et al. |
3D Gastruloids
A curated list of preprints related to Gastruloids (in vitro models of early development obtained by 3D aggregation of embryonic cells). Updated until July 2021.
| List by | Paul Gerald L. Sanchez and Stefano Vianello |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
| List by | Madhuja Samaddar et al. |
EDBC Alicante 2019
Preprints presented at the European Developmental Biology Congress (EDBC) in Alicante, October 23-26 2019.
| List by | Sergio Menchero et al. |
EMBL Seeing is Believing – Imaging the Molecular Processes of Life
Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019
| List by | Dey Lab |
SDB 78th Annual Meeting 2019
A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.
| List by | Alex Eve |
Lung Disease and Regeneration
This preprint list compiles highlights from the field of lung biology.
| List by | Rob Hynds |
Young Embryologist Network Conference 2019
Preprints presented at the Young Embryologist Network 2019 conference, 13 May, The Francis Crick Institute, London
| List by | Alex Eve |
Pattern formation during development
The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.
| List by | Alexa Sadier |
BSCB/BSDB Annual Meeting 2019
Preprints presented at the BSCB/BSDB Annual Meeting 2019
| List by | Dey Lab |
Zebrafish immunology
A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.
| List by | Shikha Nayar |
Also in the immunology category:
Community-driven preList – Immunology
In this community-driven preList, a group of preLighters, with expertise in different areas of immunology have worked together to create this preprint reading list.
| List by | Felipe Del Valle Batalla et al. |
Journal of Cell Science meeting ‘Imaging Cell Dynamics’
This preList highlights the preprints discussed at the JCS meeting 'Imaging Cell Dynamics'. The meeting was held from 14 - 17 May 2023 in Lisbon, Portugal and was organised by Erika Holzbaur, Jennifer Lippincott-Schwartz, Rob Parton and Michael Way.
| List by | Helen Zenner |
Fibroblasts
The advances in fibroblast biology preList explores the recent discoveries and preprints of the fibroblast world. Get ready to immerse yourself with this list created for fibroblasts aficionados and lovers, and beyond. Here, my goal is to include preprints of fibroblast biology, heterogeneity, fate, extracellular matrix, behavior, topography, single-cell atlases, spatial transcriptomics, and their matrix!
| List by | Osvaldo Contreras |
Single Cell Biology 2020
A list of preprints mentioned at the Wellcome Genome Campus Single Cell Biology 2020 meeting.
| List by | Alex Eve |
Autophagy
Preprints on autophagy and lysosomal degradation and its role in neurodegeneration and disease. Includes molecular mechanisms, upstream signalling and regulation as well as studies on pharmaceutical interventions to upregulate the process.
| List by | Sandra Malmgren Hill |
Antimicrobials: Discovery, clinical use, and development of resistance
Preprints that describe the discovery of new antimicrobials and any improvements made regarding their clinical use. Includes preprints that detail the factors affecting antimicrobial selection and the development of antimicrobial resistance.
| List by | Zhang-He Goh |