Temporal Dynamics of Apoptosis-Induced Proliferation in Pupal Wing Development: Implications for Regenerative Ability DOI Creative Commons

Sara Ahmed-de-Prado,

Carlos Estella, Antonio Baonza

и другие.

bioRxiv (Cold Spring Harbor Laboratory), Год журнала: 2023, Номер unknown

Опубликована: Июль 10, 2023

Abstract The ability of animals to regenerate damaged tissue is a complex process that involves various cellular mechanisms. As age, they lose their regenerative abilities, making it essential understand the underlying mechanisms limit during aging. Drosophila melanogaster wing imaginal discs are epithelial structures can after injury. While significant research has focused on investigating responses larval stages, particularly regarding regulation and function JNK pathway, our comprehension potential pupal wings contributing decline remains limited. This study explores temporal dynamics development proliferative response triggered by induction cell death, typical response. Our results indicate apoptosis-induced proliferation be initiated as late 30 hours pupa formation (APF), when in normal circumstances ceases at around 20 APF. Furthermore, data revealed 35 APF, death alone fails induce further proliferation. Interestingly, failure reinitiating cycle beyond this time point not attributed an incapacity activate pathway. Instead, one constraining factors apoptotic-induced seems activity level ecdysone-responsive genes. Author Summary Animals have remarkable tissues, but diminishes with age. Understanding age-related abilities crucial. provide valuable model for studying regeneration. understanding In study, we investigate development, development. findings reveal occur even ceased. However, stages does occur. We found that, inability reinitiate influenced hormone ecdysone its-responsive These shed light dynamic processes involved regeneration expands interplay between proliferation, gene regeneration, providing insights future biology.

Язык: Английский

The wing imaginal disc DOI Creative Commons
Bipin Kumar Tripathi, Kenneth D. Irvine

Genetics, Год журнала: 2022, Номер 220(4)

Опубликована: Март 4, 2022

Abstract The Drosophila wing imaginal disc is a tissue of undifferentiated cells that are precursors the and most notum adult fly. first forms during embryogenesis from cluster ∼30 located in second thoracic segment, which invaginate to form sac-like structure. They undergo extensive proliferation larval stages mature ∼35,000 cells. During this time, distinct cell fates assigned different regions, develops complex morphology. Finally, pupal undergoes morphogenetic processes then differentiates notum. While bulk comprises epithelial cells, it also includes neurons glia, associated with tracheal muscle precursor relative simplicity accessibility disc, combined wealth genetic tools available Drosophila, have make premier system for identifying genes deciphering systems play crucial roles animal development. Studies discs made key contributions many areas biology, including patterning, signal transduction, growth control, regeneration, planar polarity, morphogenesis, mechanics.

Язык: Английский

Процитировано

77

Ets21C sustains a pro-regenerative transcriptional program in blastema cells of Drosophila imaginal discs DOI Creative Commons
Melanie I. Worley, Nicholas J. Everetts, Riku Yasutomi

и другие.

Current Biology, Год журнала: 2022, Номер 32(15), С. 3350 - 3364.e6

Опубликована: Июль 11, 2022

An important unanswered question in regenerative biology is to what extent regeneration accomplished by the reactivation of gene regulatory networks used during development versus activation regeneration-specific transcriptional programs. Following damage, Drosophila imaginal discs, larval precursors adult structures, can regenerate missing portions localized proliferation damage-adjacent tissue. Using single-cell transcriptomics regenerating wing we have obtained a comprehensive view transcriptome discs and identified two cell populations within blastema, Blastema1 Blastema2. Collectively, these cells upregulate multiple genes encoding secreted proteins that promote including Pvf1, upd3, asperous, Mmp1, maturation delaying factor Ilp8. Expression transcription Ets21C restricted this secretory zone; it not expressed undamaged discs. expression activated JNK/AP-1 pathway, function type 1 coherent feedforward loop with AP-1 sustain downstream genes. Without function, blastema fail maintain number genes, which leads premature differentiation severely compromised regeneration. As dispensable for normal development, observations indicate orchestrates network. We also resembling both Blastema2 scribble tumorous They express Ets21C-dependent network, eliminating reduces growth. Thus, mechanisms be co-opted tumors aberrant

Язык: Английский

Процитировано

35

Homeostasis and evolution in relation to regeneration and repair DOI
Agustina Cano‐Mártinez,

María Esther Rubio‐Ruiz,

Verónica Guarner‐Lans

и другие.

The Journal of Physiology, Год журнала: 2024, Номер 602(11), С. 2627 - 2648

Опубликована: Май 23, 2024

Homeostasis constitutes a key concept in physiology and refers to self-regulating processes that maintain internal stability when adjusting changing external conditions. It diminishes entropy constituting driving force behind evolution. Natural selection might act on homeostatic regulatory mechanisms control including homeodynamics, allostasis, hormesis homeorhesis, where different stable stationary states are reached. Regeneration is under through hormesis. Damage tissues initiates response restore the impaired equilibrium caused by mild stress using cell proliferation, differentiation death recover structure function. Repair homeorhetic change leading new state with decreased functionality fibrotic scarring without reconstruction of 3-D pattern. Mechanisms determining entrance tissue or organ regeneration repair include balance between innate adaptive immune cells relation plasticity stromal stem responses, redox balance. The regenerative reparative capacities vary species, distinct organs, at stages development ageing. Many signals pathways play crucial roles regulating protein synthesis, cellular growth, inflammation, autophagy, lysosomal function, metabolism metalloproteinase signalling. Attempts favour damaged those low proliferative rates have been made; however, there evolutionary constraint poor proliferation unfavourable environments tumour development. More research required better understand these mechanisms.

Язык: Английский

Процитировано

4

An unscheduled switch to endocycles induces a reversible senescent arrest that impairs growth of the Drosophila wing disc DOI Creative Commons
Yi-Ting Huang,

Lauren L. Hesting,

Brian R. Calvi

и другие.

PLoS Genetics, Год журнала: 2024, Номер 20(9), С. e1011387 - e1011387

Опубликована: Сен. 3, 2024

A programmed developmental switch to G / S endocycles results in tissue growth through an increase cell size. Unscheduled, induced endocycling cells (iECs) promote wound healing but also contribute cancer. Much remains unknown, however, about how these iECs affect growth. Using the D . melanogaster wing disc as model, we find that populations of initially size then subsequently undergo a heterogenous arrest causes severe undergrowth. acquired DNA damage and activated Jun N-terminal kinase (JNK) pathway, but, unlike other stressed cells, were apoptosis-resistant not eliminated from epithelium. Instead, entered JNK-dependent reversible senescent-like arrest. Senescent promoted division diploid neighbors, this compensatory proliferation did rescue Our study has uncovered unique attributes their effects on have important implications for understanding roles

Язык: Английский

Процитировано

4

An unscheduled switch to endocycles induces a reversible senescent arrest that impairs growth of theDrosophilawing disc DOI Creative Commons
Yi‐Ting Huang,

Lauren L. Hesting,

Brian R. Calvi

и другие.

bioRxiv (Cold Spring Harbor Laboratory), Год журнала: 2024, Номер unknown

Опубликована: Март 14, 2024

Summary A programmed developmental switch to G / S endocycles results in tissue growth through an increase cell size. Unscheduled, induced endocycling cells (iECs) promote wound healing but also contribute cancer. Much remains unknown, however, about how these iECs affect growth. Using the D. melanogaster wing disc as model, we find that populations of initially size then subsequently undergo a heterogenous arrest causes severe undergrowth. acquired DNA damage and activated Jun N-terminal kinase (JNK) pathway, but, unlike other stressed cells, were apoptosis-resistant not eliminated from epithelium. Instead, entered JNK-dependent reversible senescent-like arrest. Senescent promoted division diploid neighbors, this compensatory proliferation did rescue Our study has uncovered unique attributes their effects on have important implications for understanding roles

Язык: Английский

Процитировано

3

Wound Healing in Butterfly Pupal Wing Tissues: Real-Time In Vivo Imaging of Long-Range Cell Migration, Cluster Formation, and Calcium Oscillations DOI Creative Commons

Susumu Nagai,

Joji M. Otaki

Insects, Год журнала: 2025, Номер 16(2), С. 124 - 124

Опубликована: Янв. 27, 2025

Insects can repair wounds and regenerate body parts in response to physical damage. Wound healing butterfly pupal wing tissues is developmentally interesting because ectopic color patterns develop during healing, suggesting that normal damage-induced may use similar mechanisms. Here we physiologically investigated wound pattern formation using the blue pansy Junonia orithya. In puncture damage, various are formed around damage site. After wounding operation, observed hemocytes migrating over long distances along veins (lacunae) toward site, where epidermal cells cellular clusters. Calcium oscillations were at near transiently affected by ruthenium red, an inhibitor of calcium transporters channels, red caused abnormalities scales adult wings. These results suggest cell migration, cluster formation, play important roles scale development Ectopic local as a consequence evolutionary co-option process for development.

Язык: Английский

Процитировано

0

Regeneration following tissue necrosis is mediated by non-apoptotic caspase activity DOI Open Access
Jacob W Klemm,

Chloe Van Hazel,

Robin E Harris

и другие.

Опубликована: Фев. 21, 2025

Tissue necrosis is a devastating complication for many human diseases and injuries. Unfortunately, our understanding of how it impacts surrounding healthy tissue – an essential consideration when developing effective methods to treat such injuries has been limited by lack robust genetically tractable models. Our lab previously established method study necrosis-induced regeneration in the Drosophila wing imaginal disc, which revealed unique phenomenon whereby cells at distance from injury upregulate caspase activity process called Necrosis-induced Apoptosis (NiA) that vital regeneration. Here we have further investigated this phenomenon, showing NiA predominantly associated with highly regenerative pouch region shaped genetic factors present presumptive hinge. Furthermore, find proportion fail undergo apoptosis, instead surviving effector activation persist within stimulate reparative proliferation late This relies on initiator Dronc, occurs independent JNK, ROS or mitogens characterized Apoptosis-induced Proliferation (AiP) mechanism. These data reveal new means non-apoptotic Dronc signaling promotes response necrotic damage.

Язык: Английский

Процитировано

0

Regeneration following tissue necrosis is mediated by non-apoptotic caspase activity DOI Creative Commons
Jacob W Klemm,

Chloe Van Hazel,

Robin E Harris

и другие.

eLife, Год журнала: 2025, Номер 13

Опубликована: Март 5, 2025

Tissue necrosis is a devastating complication for many human diseases and injuries. Unfortunately, our understanding of how it impacts surrounding healthy tissue – an essential consideration when developing effective methods to treat such injuries has been limited by lack robust genetically tractable models. Our lab previously established method study necrosis-induced regeneration in the Drosophila wing imaginal disc, which revealed unique phenomenon whereby cells at distance from injury upregulate caspase activity process called Necrosis-induced Apoptosis (NiA) that vital regeneration. Here, we have further investigated this phenomenon, showing NiA predominantly associated with highly regenerative pouch region shaped genetic factors present presumptive hinge. Furthermore, find proportion fail undergo apoptosis, instead surviving effector activation persist within stimulate reparative proliferation late This relies on initiator Dronc, occurs independent JNK, ROS or mitogens characterized Apoptosis-induced Proliferation (AiP) mechanism. These data reveal new means non-apoptotic Dronc signaling promotes response necrotic damage.

Язык: Английский

Процитировано

0

Activation of a Src-JNK pathway in unscheduled endocycling cells of the Drosophila wing disc induces a chronic wounding response DOI Creative Commons
Yi-Ting Huang, Brian R. Calvi

bioRxiv (Cold Spring Harbor Laboratory), Год журнала: 2025, Номер unknown

Опубликована: Март 13, 2025

Abstract The endocycle is a specialized cell cycle during which cells undergo repeated G / S phases to replicate DNA without division, leading large polyploid cells. transition from mitotic an can be triggered by various stresses, results in unscheduled, or induced endocycling (iECs). While iECs beneficial for wound healing, they also detrimental impairing tissue growth promoting cancer. However, the regulation of and its role remain poorly understood. Using Drosophila wing disc as model, we previously demonstrated that iEC arrested through Jun N-Terminal Kinase (JNK)-dependent, reversible senescence-like response. it remains unclear how JNK activated impact overall structure. In this study, performed genetic screen identified Src42A-Shark-Slpr pathway upstream regulator iECs, their arrest. We found tissues recognize wounds, releasing wound-related signals induce JNK-dependent developmental delay. Similar closure, response triggers Src-JNK-mediated actomyosin remodeling, yet persist rather than being eliminated. Our findings suggest shares key signaling cytoskeletal regulatory mechanisms with healing dorsal process embryogenesis. because are retained within tissue, create unique system may serve model studying chronic wounds tumor progression. Article summary effects unscheduled endocycles on unclear. To investigate this, used switch analyzed responses at both structure levels. Surprisingly, recognized activating regeneration remodeling these resist apoptosis, cleared. This persistence disrupts normal revealing similarities between wounds. has potential novel tumorigenesis.

Язык: Английский

Процитировано

0

The early history of the eye-antennal disc ofDrosophila melanogaster DOI Open Access
Brandon P. Weasner, Justin P. Kumar

Genetics, Год журнала: 2022, Номер 221(1)

Опубликована: Апрель 23, 2022

A pair of eye-antennal imaginal discs give rise to nearly all external structures the adult Drosophila head including compound eyes, ocelli, antennae, maxillary palps, epidermis, and bristles. In earliest days research, investigators would examine thousands flies in search viable mutants whose appearance deviated from norm. The eyes are dispensable for viability perturbations their structure easy detect. As such, eye developing disc emerged as focal points studies genetics developmental biology. Since few tools were available at time, early researchers put an enormous amount thought into models that explain experimental observations-many these hypotheses remain be tested. However, "ancient" have been lost time no longer read or incorporated today's literature despite abundance field-defining discoveries contained therein. this FlyBook chapter, I will bring forgotten classics together draw connections between them modern tissue specification patterning. doing so, hope a larger appreciation contributions has made our understanding development well readers' attention important disc. Armed with toolkit sophisticated genetic molecular methods using old papers guide, we can use unravel mysteries development.

Язык: Английский

Процитировано

12