The appearance of cytoplasmic cytochrome C precedes apoptosis during Drosophila salivary gland degradation
Apoptosis is an important process for organism development that functions to eliminate cell damage, maintain homeostasis, and remove obsolete tissues during morphogenesis. In mammals, apoptosis is accompanied by the release of cytochrome C (Cyt‐c) from mitochondria to the cytoplasm. However, whether...
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Published in | Insect science Vol. 31; no. 1; pp. 157 - 172 |
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Main Authors | , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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01.02.2024
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Abstract | Apoptosis is an important process for organism development that functions to eliminate cell damage, maintain homeostasis, and remove obsolete tissues during morphogenesis. In mammals, apoptosis is accompanied by the release of cytochrome C (Cyt‐c) from mitochondria to the cytoplasm. However, whether this process is conserved in the fruit fly, Drosophila melanogaster, remains controversial. In this study, we discovered that during the degradation of Drosophila salivary gland, the transcription of mitochondria apoptosis factors (MAPFs), Cyt‐c, and death‐associated APAF1‐related killer (Dark) encoding genes are all upregulated antecedent to initiator and effector caspases encoding genes. The proteins Cyt‐c and the active caspase 3 appear gradually in the cytoplasm during salivary gland degradation. Meanwhile, the Cyt‐c protein colocates with mito‐GFP, the marker indicating cytoplasmic mitochondria, and the change in mitochondrial membrane potential coincides with the appearance of Cyt‐c in the cytoplasm. Moreover, impeding or promoting 20E‐induced transcription factor E93 suppresses or enhances the staining of Cyt‐c and the active caspase 3 in the cytoplasm of salivary gland, and accordingly decreases or increases the mitochondrial membrane potential, respectively. Our research provides evidence that cytoplasmic Cyt‐c appears before apoptosis during Drosophila salivary gland degradation, shedding light on partial conserved mechanism in apoptosis between insects and mammals.
During 20‐hydroxyecdysone (20E)‐induced metamorphosis, the transcription of mitochondria apoptosis factors encoding genes (MAPFs), Cyt‐c‐d, and death‐associated APAF1‐related killer encoding gene (Dark) encoding genes are all upregulated antecedent to initiator and effector caspases encoding genes in the Drosophila salivary gland. Cyt‐c protein and the active caspase 3 appear gradually in the cytoplasm, and Cyt‐c colocates with mito‐GFP, a marker indicating cytoplasmic mitochondria. In addition, the change in mitochondrial membrane potential coincides with the appearance of cytoplasmic Cyt‐c during salivary gland degradation. Moreover, impeding or promoting 20E‐induced transcription factor E93 suppresses or enhances the accumulation of Cyt‐c and the active caspase 3 in the cytoplasm of salivary gland, and accordingly decreases or increases the mitochondrial membrane potential, respectively. The research provides evidence that cytoplasmic Cyt‐c appears before apoptosis during Drosophila salivary gland degradation, shedding light on the partial conserved mechanism in apoptosis between insects and mammals. |
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AbstractList | Apoptosis is an important process for organism development that functions to eliminate cell damage, maintain homeostasis, and remove obsolete tissues during morphogenesis. In mammals, apoptosis is accompanied by the release of cytochrome C (Cyt‐c) from mitochondria to the cytoplasm. However, whether this process is conserved in the fruit fly, Drosophila melanogaster, remains controversial. In this study, we discovered that during the degradation of Drosophila salivary gland, the transcription of mitochondria apoptosis factors (MAPFs), Cyt‐c, and death‐associated APAF1‐related killer (Dark) encoding genes are all upregulated antecedent to initiator and effector caspases encoding genes. The proteins Cyt‐c and the active caspase 3 appear gradually in the cytoplasm during salivary gland degradation. Meanwhile, the Cyt‐c protein colocates with mito‐GFP, the marker indicating cytoplasmic mitochondria, and the change in mitochondrial membrane potential coincides with the appearance of Cyt‐c in the cytoplasm. Moreover, impeding or promoting 20E‐induced transcription factor E93 suppresses or enhances the staining of Cyt‐c and the active caspase 3 in the cytoplasm of salivary gland, and accordingly decreases or increases the mitochondrial membrane potential, respectively. Our research provides evidence that cytoplasmic Cyt‐c appears before apoptosis during Drosophila salivary gland degradation, shedding light on partial conserved mechanism in apoptosis between insects and mammals. Abstract Apoptosis is an important process for organism development that functions to eliminate cell damage, maintain homeostasis, and remove obsolete tissues during morphogenesis. In mammals, apoptosis is accompanied by the release of cytochrome C (Cyt‐c) from mitochondria to the cytoplasm. However, whether this process is conserved in the fruit fly, Drosophila melanogaster , remains controversial. In this study, we discovered that during the degradation of Drosophila salivary gland, the transcription of mitochondria apoptosis factors ( MAPFs ), Cyt‐c , and death‐associated APAF1‐related killer ( Dark ) encoding genes are all upregulated antecedent to initiator and effector caspases encoding genes. The proteins Cyt‐c and the active caspase 3 appear gradually in the cytoplasm during salivary gland degradation. Meanwhile, the Cyt‐c protein colocates with mito‐GFP, the marker indicating cytoplasmic mitochondria, and the change in mitochondrial membrane potential coincides with the appearance of Cyt‐c in the cytoplasm. Moreover, impeding or promoting 20E‐induced transcription factor E93 suppresses or enhances the staining of Cyt‐c and the active caspase 3 in the cytoplasm of salivary gland, and accordingly decreases or increases the mitochondrial membrane potential, respectively. Our research provides evidence that cytoplasmic Cyt‐c appears before apoptosis during Drosophila salivary gland degradation, shedding light on partial conserved mechanism in apoptosis between insects and mammals. Apoptosis is an important process for organism development that functions to eliminate cell damage, maintain homeostasis, and remove obsolete tissues during morphogenesis. In mammals, apoptosis is accompanied by the release of cytochrome C (Cyt‐c) from mitochondria to the cytoplasm. However, whether this process is conserved in the fruit fly, Drosophila melanogaster, remains controversial. In this study, we discovered that during the degradation of Drosophila salivary gland, the transcription of mitochondria apoptosis factors (MAPFs), Cyt‐c, and death‐associated APAF1‐related killer (Dark) encoding genes are all upregulated antecedent to initiator and effector caspases encoding genes. The proteins Cyt‐c and the active caspase 3 appear gradually in the cytoplasm during salivary gland degradation. Meanwhile, the Cyt‐c protein colocates with mito‐GFP, the marker indicating cytoplasmic mitochondria, and the change in mitochondrial membrane potential coincides with the appearance of Cyt‐c in the cytoplasm. Moreover, impeding or promoting 20E‐induced transcription factor E93 suppresses or enhances the staining of Cyt‐c and the active caspase 3 in the cytoplasm of salivary gland, and accordingly decreases or increases the mitochondrial membrane potential, respectively. Our research provides evidence that cytoplasmic Cyt‐c appears before apoptosis during Drosophila salivary gland degradation, shedding light on partial conserved mechanism in apoptosis between insects and mammals. During 20‐hydroxyecdysone (20E)‐induced metamorphosis, the transcription of mitochondria apoptosis factors encoding genes (MAPFs), Cyt‐c‐d, and death‐associated APAF1‐related killer encoding gene (Dark) encoding genes are all upregulated antecedent to initiator and effector caspases encoding genes in the Drosophila salivary gland. Cyt‐c protein and the active caspase 3 appear gradually in the cytoplasm, and Cyt‐c colocates with mito‐GFP, a marker indicating cytoplasmic mitochondria. In addition, the change in mitochondrial membrane potential coincides with the appearance of cytoplasmic Cyt‐c during salivary gland degradation. Moreover, impeding or promoting 20E‐induced transcription factor E93 suppresses or enhances the accumulation of Cyt‐c and the active caspase 3 in the cytoplasm of salivary gland, and accordingly decreases or increases the mitochondrial membrane potential, respectively. The research provides evidence that cytoplasmic Cyt‐c appears before apoptosis during Drosophila salivary gland degradation, shedding light on the partial conserved mechanism in apoptosis between insects and mammals. |
Author | Qiu, Yongyu Zhao, Haigang Li, Kang Li, Sheng Dong, Renke Li, Na Deng, Ruohan Liu, Fengxin Liu, Jiali Zhang, Lidan Cao, Wenxin Long, Shihui |
Author_xml | – sequence: 1 givenname: Shihui surname: Long fullname: Long, Shihui organization: South China Normal University – sequence: 2 givenname: Wenxin surname: Cao fullname: Cao, Wenxin organization: South China Normal University – sequence: 3 givenname: Yongyu surname: Qiu fullname: Qiu, Yongyu organization: South China Normal University – sequence: 4 givenname: Ruohan surname: Deng fullname: Deng, Ruohan organization: South China Normal University – sequence: 5 givenname: Jiali surname: Liu fullname: Liu, Jiali organization: South China Normal University – sequence: 6 givenname: Lidan surname: Zhang fullname: Zhang, Lidan organization: South China Normal University – sequence: 7 givenname: Renke surname: Dong fullname: Dong, Renke organization: South China Normal University – sequence: 8 givenname: Fengxin surname: Liu fullname: Liu, Fengxin organization: South China Normal University – sequence: 9 givenname: Sheng surname: Li fullname: Li, Sheng organization: South China Normal University – sequence: 10 givenname: Haigang surname: Zhao fullname: Zhao, Haigang organization: ChemPartner PharmaTech Co., Ltd – sequence: 11 givenname: Na orcidid: 0000-0003-4202-6375 surname: Li fullname: Li, Na email: lina5hs@m.scnu.edu.cn organization: South China Normal University – sequence: 12 givenname: Kang orcidid: 0000-0002-1468-2220 surname: Li fullname: Li, Kang email: likang@m.scnu.edu.cn organization: South China Normal University |
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Cites_doi | 10.1038/cdd.2009.185 10.1016/j.ibmb.2013.11.005 10.1016/S1097-2765(00)00042-3 10.1038/cddis.2012.171 10.1038/cdd.2012.110 10.1016/S1097-2765(00)80439-6 10.1016/j.tig.2004.06.012 10.1371/journal.pone.0058499 10.1016/j.cell.2007.10.048 10.1242/dev.128.8.1443 10.1038/sj.cdd.4401918 10.1534/g3.116.037366 10.1074/jbc.M116.737072 10.1016/S1534-5807(03)00120-5 10.1083/jcb.144.4.701 10.1073/pnas.0402647101 10.1038/sj.cr.7290048 10.1083/jcb.200408054 10.1038/sj.emboj.7601745 10.1016/j.cell.2011.10.033 10.1021/bi00232a015 10.1083/jcb.200201034 10.1242/dev.117.4.1223 10.1111/1744‐7917.13135 10.1016/j.biocel.2008.12.009 10.1242/dev.124.22.4673 10.1007/s10495-015-1209-y 10.1016/j.jmb.2005.10.040 10.1006/dbio.1995.1262 10.1016/j.devcel.2004.09.018 10.1016/j.bbamcr.2013.06.014 10.1016/j.celrep.2021.109729 10.1016/S1097-2765(00)80386-X 10.1387/ijdb.150055sk 10.1093/genetics/129.2.385 10.4161/fly.3.1.7800 10.1038/sj.cdd.4401950 10.1016/0092-8674(90)90217-3 10.1111/j.1744-7917.2009.01278.x 10.1083/jcb.201303144 10.1073/pnas.0702733104 10.1073/pnas.1716897115 10.1016/j.devcel.2007.04.004 10.1083/jcb.200111107 10.1111/j.1744-7917.2011.01431.x 10.1080/15548627.2015.1134079 10.1038/sj.embor.7400773 10.1038/sj.emboj.7600920 10.1093/nar/13.2.631 10.1016/S0092-8674(00)81873-5 10.1074/jbc.M413971200 10.1016/j.cellbi.2007.03.011 10.1006/dbio.2002.0838 |
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References | 2004; 167 2004; 21 2007; 104 2017; 7 2004; 20 2009; 41 1997; 88 2000; 6 2000; 5 2010; 17 2002; 157 2004; 7 2013; 20 2002; 156 2012; 19 2007; 31 2013; 8 1995; 171 1990; 61 2021; 36 2014; 205 2000; 10 2006; 25 2007; 131 2003; 4 2009; 16 2007; 26 1985; 13 2013; 1833 2015; 59 2002; 252 2006; 13 1991; 30 2006; 7 1999; 4 1999; 144 2007; 12 2014; 45 2001; 128 2016; 12 2006; 355 1997; 124 2011; 147 2005; 280 2012; 3 1993; 117 2022 2018; 115 2016; 21 1991; 129 2009; 3 2016; 291 e_1_2_7_5_1 e_1_2_7_3_1 e_1_2_7_9_1 e_1_2_7_7_1 e_1_2_7_19_1 e_1_2_7_17_1 e_1_2_7_15_1 e_1_2_7_41_1 e_1_2_7_13_1 e_1_2_7_43_1 e_1_2_7_11_1 e_1_2_7_45_1 e_1_2_7_47_1 e_1_2_7_26_1 e_1_2_7_49_1 e_1_2_7_28_1 e_1_2_7_50_1 e_1_2_7_25_1 e_1_2_7_31_1 e_1_2_7_52_1 e_1_2_7_23_1 e_1_2_7_33_1 e_1_2_7_54_1 e_1_2_7_21_1 e_1_2_7_35_1 e_1_2_7_37_1 e_1_2_7_39_1 e_1_2_7_6_1 e_1_2_7_4_1 e_1_2_7_8_1 e_1_2_7_18_1 e_1_2_7_16_1 e_1_2_7_40_1 e_1_2_7_2_1 e_1_2_7_14_1 e_1_2_7_42_1 e_1_2_7_12_1 e_1_2_7_44_1 e_1_2_7_10_1 e_1_2_7_46_1 e_1_2_7_48_1 e_1_2_7_27_1 e_1_2_7_29_1 e_1_2_7_51_1 e_1_2_7_30_1 e_1_2_7_53_1 e_1_2_7_24_1 e_1_2_7_32_1 e_1_2_7_22_1 e_1_2_7_34_1 e_1_2_7_20_1 e_1_2_7_36_1 e_1_2_7_38_1 |
References_xml | – year: 2022 article-title: E93 promotes transcription of genes to initiate apoptosis during salivary gland metamorphosis publication-title: Insect Science – volume: 61 start-page: 85 year: 1990 end-page: 99 article-title: The 74EF early puff contains , a complex ecdysone‐inducible gene that encodes two ets‐related proteins publication-title: Cell – volume: 25 start-page: 232 year: 2006 end-page: 243 article-title: The two cytochrome C proteins can function in both respiration and caspase activation publication-title: EMBO Journal – volume: 291 start-page: 18163 year: 2016 end-page: 18175 article-title: 20‐Hydroxyecdysone (20E) Primary response gene isoforms mediate steroidogenesis autoregulation and regulate developmental timing in publication-title: Journal of Biological Chemistry – volume: 1833 start-page: 3499 year: 2013 end-page: 3506 article-title: Developmentally programmed cell death in publication-title: Biochimica Biophysica Acta – volume: 4 start-page: 757 year: 1999 end-page: 769 article-title: Control of the cell death pathway by Dapaf‐1, a Apaf‐1/CED‐4‐related caspase activator publication-title: Molecular Cell – volume: 13 start-page: 1423 year: 2006 end-page: 1433 article-title: Mechanisms of cytochrome c release from mitochondria publication-title: Cell Death and Differentiation – volume: 124 start-page: 4673 year: 1997 end-page: 4683 article-title: Steroid regulated programmed cell death during metamorphosis publication-title: Development – volume: 45 start-page: 30 year: 2014 end-page: 39 article-title: predominantly transduces 20‐hydroxyecdysone signaling to induce autophagy and caspase activity in fat body publication-title: Insect Biochemistry and Molecular Biology – volume: 4 start-page: 687 year: 2003 end-page: 697 article-title: Caspase activity and a specific cytochrome C are required for sperm differentiation in publication-title: Development Cell – volume: 129 start-page: 385 year: 1991 end-page: 397 article-title: The broad‐complex encodes a family of related proteins containing zinc fingers publication-title: Genetics – volume: 7 start-page: 933 year: 2006 end-page: 939 article-title: Cytochrome c‐d regulates developmental apoptosis in the retina publication-title: EMBO Reports – volume: 144 start-page: 701 year: 1999 end-page: 710 article-title: Altered cytochrome c display precedes apoptotic cell death in publication-title: Journal of Cell Biology – volume: 36 year: 2021 article-title: UQCRC1 engages cytochrome c for neuronal apoptotic cell death publication-title: Cell Reports – volume: 171 start-page: 85 year: 1995 end-page: 97 article-title: The gene from the 93F early puff displays stage‐ and tissue‐specific regulation by 20‐hydroxyecdysone publication-title: Developmental Biology – volume: 31 start-page: 996 year: 2007 end-page: 1001 article-title: Influence of cytochrome c on apoptosis induced by ( ) multiple nuclear polyhedrosis virus (AfMNPV) in insect cells publication-title: Cell Biology International – volume: 88 start-page: 347 year: 1997 end-page: 354 article-title: Programmed cell death in animal development publication-title: Cell – volume: 20 start-page: 218 year: 2013 end-page: 225 article-title: Identification of factors that function in salivary gland cell death during development using proteomics publication-title: Cell Death and Differentiation – volume: 26 start-page: 3144 year: 2007 end-page: 3156 article-title: Omi, a mitochondrial‐localized IAP antagonist and proapoptotic serine protease publication-title: The EMBO Journal – volume: 205 start-page: 477 year: 2014 end-page: 492 article-title: The effector caspase Dcp‐1 regulates mitochondrial dynamics and autophagic flux via SesB publication-title: The Journal of Cell Biology – volume: 17 start-page: 534 year: 2010 end-page: 539 article-title: The cleaved‐Caspase‐3 antibody is a marker of Caspase‐9‐like DRONC activity in publication-title: Cell Death and Differentiation – volume: 104 start-page: 13367 year: 2007 end-page: 13372 article-title: Local initiation of caspase activation in salivary gland programmed cell death publication-title: Proceedings of the National Academy of Sciences USA – volume: 252 start-page: 138 year: 2002 end-page: 148 article-title: Genetic mechanism for the stage‐ and tissue‐specific regulation of steroid triggered programmed cell death in publication-title: Developmental Biology – volume: 8 year: 2013 article-title: The mitochondria‐mediate apoptosis of cells induced by azadirachtin publication-title: PLoS ONE – volume: 6 start-page: 433 year: 2000 end-page: 443 article-title: directs steroid‐triggered programmed cell death in publication-title: Molecular Cell – volume: 117 start-page: 1223 year: 1993 end-page: 1237 article-title: Analysis of genetic mosaics in developing and adult tissues publication-title: Development – volume: 12 start-page: 793 year: 2007 end-page: 806 article-title: Mitochondrial disruption in apoptosis publication-title: Developmental Cell – volume: 7 start-page: 909 year: 2004 end-page: 915 article-title: caspase DRONC is required for specific developmental cell death pathways and stress‐induced apoptosis publication-title: Development Cell – volume: 131 start-page: 1137 year: 2007 end-page: 1148 article-title: Growth arrest and autophagy are required for salivary gland cell degradation in publication-title: Cell – volume: 5 start-page: 445 year: 2000 end-page: 455 article-title: A steroid‐triggered transcriptional hierarchy controls salivary gland cell death during metamorphosis publication-title: Molecular Cell – volume: 3 year: 2012 article-title: JC‐1: alternative excitation wavelengths facilitate mitochondrial membrane potential cytometry publication-title: Cell Death & Disease – volume: 7 start-page: 789 year: 2017 end-page: 799 article-title: Mutants for isocitrate dehydrogenase 3b are defective in mitochondrial function and larval cell death publication-title: G3: Genes, Genomes, Genetics – volume: 156 start-page: 1089 year: 2002 end-page: 1098 article-title: The role of cytochrome c in caspase activation in cells publication-title: Journal of Cell Biology – volume: 19 start-page: 30 year: 2012 end-page: 40 article-title: Cytochrome c and insect cell apoptosis publication-title: Insect Science – volume: 20 start-page: 384 year: 2004 end-page: 391 article-title: Gene expression systems in : a synthesis of time and space publication-title: Trends in Genetics – volume: 59 start-page: 23 year: 2015 end-page: 32 article-title: Ecdysone‐mediated programmed cell death in publication-title: International Journal of Developmental Biology – volume: 13 start-page: 1049 year: 2006 end-page: 1051 article-title: A cytochrome c‐free fly apoptosome publication-title: Cell Death and Differentiation – volume: 3 start-page: 78 year: 2009 end-page: 90 article-title: Genetic control of programmed cell death (apoptosis) in publication-title: Fly (Austin) – volume: 10 start-page: 193 year: 2000 end-page: 204 article-title: Genetic regulation of programmed cell death in publication-title: Cell Research – volume: 147 start-page: 742 year: 2011 end-page: 758 article-title: Programmed cell death in animal development and disease publication-title: Cell – volume: 355 start-page: 577 year: 2006 end-page: 589 article-title: Three‐dimensional structure of a double apoptosome formed by the Apaf‐1 related killer publication-title: Journal of Molecular Biology – volume: 41 start-page: 1430 year: 2009 end-page: 1440 article-title: Mitochondrial regulation of insect cell apoptosis: evidence for permeability transition pore‐independent cytochrome‐c release in the Sf9 cells publication-title: International Journal of Biochemistry & Cell Biology – volume: 280 start-page: 11981 year: 2005 end-page: 11986 article-title: Ecdysone‐mediated up‐regulation of the effector caspase DRICE is required for hormone‐dependent apoptosis in cells publication-title: Journal of Biological Chemistry – volume: 16 start-page: 485 year: 2009 end-page: 491 article-title: Mitochondria are involved in apoptosis induced by ultraviolet radiation in lepidopteran cell line publication-title: Insect Science – volume: 128 start-page: 1443 year: 2001 end-page: 1455 article-title: Steroid regulation of autophagic programmed cell death during development publication-title: Development – volume: 115 start-page: 139 year: 2018 end-page: 144 article-title: Antagonistic actions of juvenile hormone and 20‐hydroxyecdysone within the ring gland determine developmental transitions in publication-title: Proceedings of the National Academy of Sciences USA – volume: 167 start-page: 405 year: 2004 end-page: 410 article-title: The two cytochrome c species, DC3 and DC4, are not required for caspase activation and apoptosis in cells publication-title: Journal of Cell Biology – volume: 157 start-page: 985 year: 2002 end-page: 995 article-title: Ecdysone‐induced expression of the caspase DRONC during hormone‐dependent programmed cell death in is regulated by Broad‐Complex publication-title: Journal of Cell Biology – volume: 13 start-page: 631 year: 1985 end-page: 644 article-title: Characterization of two cytochrome c genes and their transcripts publication-title: Nucleic Acids Research – volume: 30 start-page: 4480 year: 1991 end-page: 4486 article-title: J‐aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential publication-title: Biochemistry – volume: 12 start-page: 381 year: 2016 end-page: 396 article-title: BmATG5 and BmATG6 mediate apoptosis following autophagy induced by 20‐hydroxyecdysone or starvation publication-title: Autophagy – volume: 21 start-page: 239 year: 2016 end-page: 251 article-title: Apoptosis in : which role for mitochondria? publication-title: Apoptosis – volume: 21 start-page: 8022 year: 2004 end-page: 8027 article-title: A balance between the diap1 death inhibitor and reaper and hid death inducers controls steroid‐triggered cell death in publication-title: Proceedings of the National Academy of Sciences USA – ident: e_1_2_7_19_1 doi: 10.1038/cdd.2009.185 – ident: e_1_2_7_36_1 doi: 10.1016/j.ibmb.2013.11.005 – ident: e_1_2_7_33_1 doi: 10.1016/S1097-2765(00)00042-3 – ident: e_1_2_7_44_1 doi: 10.1038/cddis.2012.171 – ident: e_1_2_7_41_1 doi: 10.1038/cdd.2012.110 – ident: e_1_2_7_26_1 doi: 10.1016/S1097-2765(00)80439-6 – ident: e_1_2_7_40_1 doi: 10.1016/j.tig.2004.06.012 – ident: e_1_2_7_22_1 doi: 10.1371/journal.pone.0058499 – ident: e_1_2_7_6_1 doi: 10.1016/j.cell.2007.10.048 – ident: e_1_2_7_31_1 doi: 10.1242/dev.128.8.1443 – ident: e_1_2_7_15_1 doi: 10.1038/sj.cdd.4401918 – ident: e_1_2_7_18_1 doi: 10.1534/g3.116.037366 – ident: e_1_2_7_34_1 doi: 10.1074/jbc.M116.737072 – ident: e_1_2_7_3_1 doi: 10.1016/S1534-5807(03)00120-5 – ident: e_1_2_7_48_1 doi: 10.1083/jcb.144.4.701 – ident: e_1_2_7_52_1 doi: 10.1073/pnas.0402647101 – ident: e_1_2_7_30_1 doi: 10.1038/sj.cr.7290048 – ident: e_1_2_7_16_1 doi: 10.1083/jcb.200408054 – ident: e_1_2_7_9_1 doi: 10.1038/sj.emboj.7601745 – ident: e_1_2_7_20_1 doi: 10.1016/j.cell.2011.10.033 – ident: e_1_2_7_45_1 doi: 10.1021/bi00232a015 – ident: e_1_2_7_8_1 doi: 10.1083/jcb.200201034 – ident: e_1_2_7_51_1 doi: 10.1242/dev.117.4.1223 – ident: e_1_2_7_54_1 doi: 10.1111/1744‐7917.13135 – ident: e_1_2_7_29_1 doi: 10.1016/j.biocel.2008.12.009 – ident: e_1_2_7_25_1 doi: 10.1242/dev.124.22.4673 – ident: e_1_2_7_10_1 doi: 10.1007/s10495-015-1209-y – ident: e_1_2_7_53_1 doi: 10.1016/j.jmb.2005.10.040 – ident: e_1_2_7_5_1 doi: 10.1006/dbio.1995.1262 – ident: e_1_2_7_11_1 doi: 10.1016/j.devcel.2004.09.018 – ident: e_1_2_7_12_1 doi: 10.1016/j.bbamcr.2013.06.014 – ident: e_1_2_7_23_1 doi: 10.1016/j.celrep.2021.109729 – ident: e_1_2_7_27_1 doi: 10.1016/S1097-2765(00)80386-X – ident: e_1_2_7_43_1 doi: 10.1387/ijdb.150055sk – ident: e_1_2_7_14_1 doi: 10.1093/genetics/129.2.385 – ident: e_1_2_7_50_1 doi: 10.4161/fly.3.1.7800 – ident: e_1_2_7_21_1 doi: 10.1038/sj.cdd.4401950 – ident: e_1_2_7_7_1 doi: 10.1016/0092-8674(90)90217-3 – ident: e_1_2_7_46_1 doi: 10.1111/j.1744-7917.2009.01278.x – ident: e_1_2_7_13_1 doi: 10.1083/jcb.201303144 – ident: e_1_2_7_47_1 doi: 10.1073/pnas.0702733104 – ident: e_1_2_7_39_1 doi: 10.1073/pnas.1716897115 – ident: e_1_2_7_2_1 doi: 10.1016/j.devcel.2007.04.004 – ident: e_1_2_7_17_1 doi: 10.1083/jcb.200111107 – ident: e_1_2_7_37_1 doi: 10.1111/j.1744-7917.2011.01431.x – ident: e_1_2_7_49_1 doi: 10.1080/15548627.2015.1134079 – ident: e_1_2_7_42_1 doi: 10.1038/sj.embor.7400773 – ident: e_1_2_7_4_1 doi: 10.1038/sj.emboj.7600920 – ident: e_1_2_7_35_1 doi: 10.1093/nar/13.2.631 – ident: e_1_2_7_24_1 doi: 10.1016/S0092-8674(00)81873-5 – ident: e_1_2_7_28_1 doi: 10.1074/jbc.M413971200 – ident: e_1_2_7_38_1 doi: 10.1016/j.cellbi.2007.03.011 – ident: e_1_2_7_32_1 doi: 10.1006/dbio.2002.0838 |
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SubjectTerms | active caspase 3 Animals Apoptosis C protein Caspase 3 Caspases - genetics Coding Cytochrome Cytochrome c Cytochromes Cytochromes c - genetics Cytochromes c - metabolism Cytoplasm Cytoplasm - metabolism Cyt‐c Degradation Drosophila Drosophila - genetics Drosophila melanogaster - genetics Exocrine glands Fruit flies Genes Homeostasis Insects Mammals Mammals - metabolism Membrane potential Membranes Mitochondria Morphogenesis Photodegradation Proteins Salivary gland Salivary glands Salivary Glands - metabolism Transcription factors |
Title | The appearance of cytoplasmic cytochrome C precedes apoptosis during Drosophila salivary gland degradation |
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