Drosophila melanogaster Lifespan Is Regulated by nejire Gene Expression in Peripheral Tissues and Nervous System

封面

如何引用文章

全文:

开放存取 开放存取
受限制的访问 ##reader.subscriptionAccessGranted##
受限制的访问 订阅存取

详细

Histone acetyltransferases of the CBP/p300 family play the role of transcriptional regulators and are required for a number of biological processes (cell proliferation and differentiation, organism development, regulation of stress response and metabolism). In a study on the fruit fly Drosophila melanogaster, we analyzed for the first time the effect of overexpression and knockdown of the nejire (nej) ortholog gene in various tissues (fat body, intestine, nervous system) on lifespan. The activation of nej had both a positive and a negative effect on this parameter, depending on the driver and the tissue where nej was induced, as well as the sex of the animals. The effect of increasing lifespan (by 6–15%) was found in females with conditional overexpression of nej in the intestine and constitutive overexpression of nej in the nervous system. But in other cases, a shortening of life (up to 44%), or the absence of statistically significant changes were observed. In addition, activation of nej revealed changes in the expression of stress response genes (Sod1, Gadd45, Hsp27, Hsp68, Hif1). At the same time, knockdown of nej in most variants of the experiment caused a pronounced negative effect on the Drosophila lifespan.

作者简介

L. Koval

Institute of Biology, Komi Science Center, Ural Branch, Russian Academy of Sciences

Email: amoskalev@ib.komisc.ru
Russia, 167982, Syktyvkar

E. Proshkina

Institute of Biology, Komi Science Center, Ural Branch, Russian Academy of Sciences

Email: amoskalev@ib.komisc.ru
Russia, 167982, Syktyvkar

N. Zemskaya

Institute of Biology, Komi Science Center, Ural Branch, Russian Academy of Sciences

Email: amoskalev@ib.komisc.ru
Russia, 167982, Syktyvkar

I. Solovev

Institute of Biology, Komi Science Center, Ural Branch, Russian Academy of Sciences; Pitirim Sorokin Syktyvkar State University

Email: amoskalev@ib.komisc.ru
Russia, 167982, Syktyvkar; Russia, 167001, Syktyvkar

E. Shegoleva

Institute of Biology, Komi Science Center, Ural Branch, Russian Academy of Sciences

Email: amoskalev@ib.komisc.ru
Russia, 167982, Syktyvkar

M. Shaposhnikov

Institute of Biology, Komi Science Center, Ural Branch, Russian Academy of Sciences

Email: amoskalev@ib.komisc.ru
Russia, 167982, Syktyvkar

A. Moskalev

Institute of Biology, Komi Science Center, Ural Branch, Russian Academy of Sciences; Engelhardt Institute of Molecular Biology, Russian Academy of Sciences; Laboratory of Genetics and Epigenetic of Aging, Russian Clinical Research Center for Gerontology,
Pirogov Russian National Research Medical University, Ministry of Health of the Russian Federation

编辑信件的主要联系方式.
Email: amoskalev@ib.komisc.ru
Russia, 167982, Syktyvkar; Russia, 119991, Moscow; Russia, 129226, Moscow

参考

  1. Прошкина Е.Н., Соловьёв И.А., Шапошников М.В., Москалев А.А. 2020. Ключевые молекулярные механизмы старения, биомаркеры и потенциальные интервенции. Молекуляр. биология. 54(6), 883‒921.
  2. Bradshaw P.C. (2021) Acetyl-CoA metabolism and histone acetylation in the regulation of aging and lifespan. Antioxidants (Basel). 10, 572.
  3. Santos-Rosa H., Valls E., Kouzarides T., Martinez-Balbas M. (2003) Mechanisms of P/CAF auto-acetylation. Nucl. Acids Res. 31, 4285–4292.
  4. Dutto I., Scalera C., Prosperi E. (2018) CREBBP and p300 lysine acetyl transferases in the DNA damage response. Cell Mol. Life Sci. 75, 1325–1338.
  5. Xu Y., Wan W. (2023) Acetylation in the regulation of autophagy. Autophagy. 19, 379–387.
  6. Goodman R.H., Smolik S. (2000) CBP/p300 in cell growth, transformation, and development. Genes Dev. 14, 1553–1577.
  7. Xue Y., Wen H., Shi X. (2018) CBP/p300: intramolecular and intermolecular regulations. Front. Biol. 13, 168–179.
  8. Sen P., Lan Y., Li C.Y., Sidoli S., Donahue G., Dou Z., Frederick B., Chen Q., Luense L.J., Garcia B.A., Dang W., Johnson F.B., Adams P.D., Schultz D.C., Berger S.L. (2019) Histone acetyltransferase p300 induces de novo super-enhancers to drive cellular senescence. Mol. Cell. 73, 684–698 e688.
  9. Vaziri H., West M.D., Allsopp R.C., Davison T.S., Wu Y.S., Arrowsmith C.H., Poirier G.G., Benchimol S. (1997) ATM-dependent telomere loss in aging human diploid fibroblasts and DNA damage lead to the post-translational activation of p53 protein involving poly(ADP-ribose) polymerase. EMBO J. 16, 6018–6033.
  10. Huang W.S., Kuo Y.H., Kuo H.C., Hsieh M.C., Huang C.Y., Lee K.C., Lee K.F., Shen C.H., Tung S.Y., Teng C.C. (2017) CIL-102-Induced cell cycle arrest and apoptosis in colorectal cancer cells via upregulation of p21 and GADD45. PLoS One. 12, e0168989.
  11. Li T.Y., Sleiman M.B., Li H., Gao A.W., Mottis A., Bachmann A.M., El Alam G., Li X., Goeminne L.J.E., Schoonjans K., Auwerx J. (2021) The transcriptional coactivator CBP/p300 is an evolutionarily conserved node that promotes longevity in response to mitochondrial stress. Nat. Aging. 1, 165–178.
  12. Madeo F., Carmona-Gutierrez D., Kepp O., Kroemer G. (2018) Spermidine delays aging in humans. Aging (Albany NY). 10, 2209–2211.
  13. Marek K.W., Ng N., Fetter R., Smolik S., Goodman C.S., Davis G.W. (2000) A genetic analysis of synaptic development: pre- and postsynaptic dCBP control transmitter release at the Drosophila NMJ. Neuron. 25, 537–547.
  14. Smolik S., Jones K. (2007) Drosophila dCBP is involved in establishing the DNA replication checkpoint. Mol. Cell. Biol. 27, 135–146.
  15. Taylor J.P., Taye A.A., Campbell C., Kazemi-Esfarjani P., Fischbeck K.H., Min K.T. (2003) Aberrant histone acetylation, altered transcription, and retinal degeneration in a Drosophila model of polyglutamine disease are rescued by CREB-binding protein. Genes Dev. 17, 1463–1468.
  16. Tseng A.S., Hariharan I.K. (2002) An overexpression screen in Drosophila for genes that restrict growth or cell-cycle progression in the developing eye. Genetics. 162, 229–243.
  17. Osterwalder T., Yoon K.S., White B.H., Keshishian H. (2001) A conditional tissue-specific transgene expression system using inducible GAL4. Proc. Natl. Acad. Sci. USA. 98, 12596–12601.
  18. Duffy J.B. (2002) GAL4 system in Drosophila: a fly geneticist’s Swiss army knife. Genesis. 34, 1–15.
  19. Landis G.N., Salomon M.P., Keroles D., Brookes N., Sekimura T., Tower J. (2015) The progesterone antagonist mifepristone/RU486 blocks the negative effect on life span caused by mating in female Drosophila. Aging (Albany NY). 7, 53–69.
  20. Xia B., de Belle J.S. (2016) Transgenerational programming of longevity and reproduction by post-eclosion dietary manipulation in Drosophila. Aging (Albany NY). 8, 1115–1134.
  21. Fleming T.R., O’Fallon J.R., O’Brien P.C., Harrington D.P. (1980) Modified Kolmogorov–Smirnov test procedures with application to arbitrarily right-censored data. Biometrics. 36, 607–625.
  22. Mantel N. (1966) Evaluation of survival data and two new rank order statistics arising in its consideration. Cancer Chemother. Rep. 50, 163–170.
  23. Martinez R.L.M.C., Naranjo J.D. (2012) A pretest for choosing between logrank and wilcoxon tests in the two-sample problem. Metron. 68, 111–125.
  24. Wang C., Li Q., Redden D.T., Weindruch R., Allison D.B. (2004) Statistical methods for testing effects on “maximum lifespan”. Mech. Ageing Dev. 125, 629–632.
  25. Han S.K., Lee D., Lee H., Kim D., Son H.G., Yang J.S., Lee S.V., Kim S. (2016) OASIS 2: online application for survival analysis 2 with features for the analysis of maximal lifespan and healthspan in aging research. Oncotarget. 7, 56147–56152.
  26. Kruskal W.H., Wallis W.A. (1952) Use of ranks in one-criterion variance analysis. J. Am. Stat. Assoc. 47, 583–621.
  27. Ganner A., Gerber J., Ziegler A.K., Li Y., Kandzia J., Matulenski T., Kreis S., Breves G., Klein M., Walz G., Neumann-Haefelin E. (2019) CBP-1/p300 acetyltransferase regulates SKN-1/Nrf cellular levels, nuclear localization, and activity in C. elegans. Exp. Gerontol. 126, 110690.
  28. Wang D., Kon N., Lasso G., Jiang L., Leng W., Zhu W.G., Qin J., Honig B., Gu W. (2016) Acetylation-regulated interaction between p53 and SET reveals a widespread regulatory mode. Nature. 538, 118–122.
  29. Boija A., Mahat D.B., Zare A., Holmqvist P.H., Philip P., Meyers D.J., Cole P.A., Lis J.T., Stenberg P., Mannervik M. (2017) CBP regulates recruitment and release of promoter-proximal RNA polymerase II. Mol. Cell. 68, 491–503.e495.
  30. Li Y., Zhong H., Wu M., Tan B., Zhao L., Yi Q., Xu X., Pan H., Bi Y., Yang K. (2019) Decline of p300 contributes to cell senescence and growth inhibition of hUC-MSCs through p53/p21 signaling pathway. Biochem. Biophys. Res. Commun. 515, 24–30.
  31. Ghosh R., Kaypee S., Shasmal M., Kundu T.K., Roy S., Sengupta J. (2019) Tumor suppressor p53-mediated structural reorganization of the transcriptional coactivator p300. Biochemistry. 58, 3434–3443.
  32. Xu X., Zhang C., Xu H., Wu L., Hu M., Song L. (2020) Autophagic feedback-mediated degradation of IKKα requires CHK1- and p300/CBP-dependent acetylation of p53. J. Cell Sci. 133, jcs246868.
  33. Wondisford A.R., Xiong L., Chang E., Meng S., Meyers D.J., Li M., Cole P.A., He L. (2014) Control of Foxo1 gene expression by co-activator P300. J. Biol. Chem. 289, 4326–4333.
  34. Wu J., Jiang Z., Zhang H., Liang W., Huang W., Zhang H., Li Y., Wang Z., Wang J., Jia Y., Liu B., Wu H. (2018) Sodium butyrate attenuates diabetes-induced aortic endothelial dysfunction via P300-mediated transcriptional activation of Nrf2. Free Radic. Biol. Med. 124, 454–465.
  35. Xu D., Zalmas L.P., La Thangue N.B. (2008) A transcription cofactor required for the heat-shock response. EMBO Rep. 9, 662–669.
  36. Ruas J.L., Berchner-Pfannschmidt U., Malik S., Gradin K., Fandrey J., Roeder R.G., Pereira T., Poellinger L. (2010) Complex regulation of the transactivation function of hypoxia-inducible factor-1 alpha by direct interaction with two distinct domains of the CREB-binding protein/p300. J. Biol. Chem. 285, 2601–2609.
  37. Barrett L.N., Westerheide S.D. (2022) The CBP-1/p300 lysine acetyltransferase regulates the heat shock response in C. elegans. Front. Aging. 3, 861761.
  38. Hunt G., Boija A., Mannervik M. (2022) p300/CBP sustains Polycomb silencing by non-enzymatic functions. Mol. Cell. 82, 3580–3597 e3589.
  39. Siebold A.P., Banerjee R., Tie F., Kiss D.L., Moskowitz J., Harte P.J. (2010) Polycomb repressive complex 2 and Trithorax modulate Drosophila longevity and stress resistance. Proc. Natl. Acad. Sci. USA. 107, 169–174.
  40. Dasari V., Srivastava S., Khan S., Mishra R.K. (2018) Epigenetic factors Polycomb (Pc) and Suppressor of zeste (Su(z)2) negatively regulate longevity in Drosophila melanogaster. Biogerontology. 19, 33–45.
  41. Sharma S., Poetz F., Bruer M., Ly-Hartig T.B., Schott J., Séraphin B., Stoecklin G. (2016) Acetylation-dependent control of global Poly(A) RNA degradation by CBP/p300 and HDAC1/2. Mol. Cell. 63, 927–938.
  42. Ansari M.S.Z., Stagni V., Iuzzolino A., Rotili D., Mai A., Del Bufalo D., Lavia P., Degrassi F., Trisciuoglio D. (2023) Pharmacological targeting of CBP/p300 drives a redox/autophagy axis leading to senescence-induced growth arrest in non-small cell lung cancer cells. Cancer Gene Ther. 30, 124–136.
  43. Solovev I., Shaposhnikov M., Kudryavtseva A., Moskalev A. (2018) Drosophila melanogaster as a model for studying the epigenetic basis of aging. In: Epigenetics of Aging and Longevity. 4. Eds Moskalev A., Vaiserman A.M. Boston: Acad. Press, pp. 293–307.
  44. Lee I.H., Finkel T. (2009) Regulation of autophagy by the p300 acetyltransferase. J. Biol. Chem. 284, 6322–6328.
  45. Wan W., You Z., Xu Y., Zhou L., Guan Z., Peng C., Wong C.C.L., Su H., Zhou T., Xia H., Liu W. (2017) mTORC1 phosphorylates acetyltransferase p300 to regulate autophagy and lipogenesis. Mol. Cell. 68, 323–335.e326.
  46. Hao Y., Ren Z., Yu L., Zhu G., Zhang P., Zhu J., Cao S. (2022) p300 arrests intervertebral disc degeneration by regulating the FOXO3/Sirt1/Wnt/β-catenin axis. Aging Cell. 21, e13677.
  47. Chen X., Li Y., Wang C., Tang Y., Mok S.A., Tsai R.M., Rojas J.C., Karydas A., Miller B.L., Boxer A.L., Gestwicki J.E., Arkin M., Cuervo A.M., Gan L. (2020) Promoting tau secretion and propagation by hyperactive p300/CBP via autophagy-lysosomal pathway in tauopathy. Mol. Neurodegener. 15, 2.
  48. Auwerx J., Li T.Y. (2020) A conserved role of CBP/p300 in mitochondrial stress response and longevity. FASEB J. 34, 1.https://doi.org/10.1096/fasebj.2020.34.s1.00128
  49. Hung H.C., Maurer C., Kay S.A., Weber F. (2007) Circadian transcription depends on limiting amounts of the transcription co-activator nejire/CBP. J. Biol. Chem. 282, 31349–31357.
  50. Lakshmanan M.D., Shaheer K. (2020) Endocrine disrupting chemicals may deregulate DNA repair through estrogen receptor mediated seizing of CBP/p300 acetylase. J. Endocrinol. Invest. 43, 1189–1196.
  51. Tezil T., Chamoli M., Ng C.P., Simon R.P., Butler V.J., Jung M., Andersen J., Kao A.W., Verdin E. (2019) Lifespan-increasing drug nordihydroguaiaretic acid inhibits p300 and activates autophagy. NPJ Aging Mech. Dis. 5, 7.
  52. Rao X., Tang P., Li Y., Fu G., Chen S., Xu X., Zhou Y., Li X., Zhang L., Mo S., Cai S., Peng J., Zhang Z., Gao J., Hua G. (2021) CBP/P300 Inhibitors mitigate radiation-induced GI syndrome by promoting intestinal stem cell-mediated crypt regeneration. Int. J. Radiat. Oncol. Biol. Phys. 110, 1210–1221.
  53. McCarroll S.A., Murphy C.T., Zou S., Pletcher S.D., Chin C.S., Jan Y.N., Kenyon C., Bargmann C.I., Li H. (2004) Comparing genomic expression patterns across species identifies shared transcriptional profile in aging. Nat. Genet. 36, 197–204.
  54. Landis G.N., Hilsabeck T.A.U., Bell H.S., Ronnen-Oron T., Wang L., Doherty D.V., Tejawinata F.I., Erickson K., Vu W., Promislow D.E.L., Kapahi P., Tower J. (2021) Mifepristone increases life span of virgin female Drosophila on regular and high-fat diet without reducing food intake. Front. Genet. 12, 751647.
  55. Kirfel P., Vilcinskas A., Skaljac M. (2020) Lysine acetyltransferase p300/CBP plays an important role in reproduction, embryogenesis and longevity of the pea aphid Acyrthosiphon pisum. Insects. 11, 265.
  56. Cai H., Dhondt I., Vandemeulebroucke L., Vlaeminck C., Rasulova M., Braeckman B.P. (2019) CBP-1 acts in GABAergic neurons to double life span in axenically cultured Caenorhabditis elegans. J. Gerontol. A Biol. Sci. Med. Sci. 74, 1198–1205.
  57. Bedford D.C., Kasper L.H., Wang R., Chang Y., Green D.R., Brindle P.K. (2011) Disrupting the CH1 domain structure in the acetyltransferases CBP and p300 results in lean mice with increased metabolic control. Cell Metab. 14, 219–230.
  58. Yao W., Wang T., Huang F. (2018) p300/CBP as a key nutritional sensor for hepatic energy homeostasis and liver fibrosis. Biomed. Res. Int. 2018, 8168791.
  59. Lai K.K.Y., Hu X., Chosa K., Nguyen C., Lin D.P., Lai K.K., Kato N., Higuchi Y., Highlander S.K., Melendez E., Eriguchi Y., Fueger P.T., Ouellette A.J., Chimge N.O., Ono M., Kahn M. (2021) P300 serine 89: a critical signaling integrator and its effects on intestinal homeostasis and repair. Cancers (Basel). 13(6), 1288.
  60. Lipinski M., Del Blanco B., Barco A. (2019) CBP/p300 in brain development and plasticity: disentangling the KAT’s cradle. Curr. Opin. Neurobiol. 59, 1–8.
  61. Lin W.H., Baines R.A. (2019) Myocyte enhancer factor-2 and p300 interact to regulate the expression of homeostatic regulator Pumilio in Drosophila. Eur. J. Neurosci. 50, 1727–1740.
  62. Caccamo A., Maldonado M.A., Bokov A.F., Majumder S., Oddo S. (2010) CBP gene transfer increases BDNF levels and ameliorates learning and memory deficits in a mouse model of Alzheimer’s disease. Proc. Natl. Acad. Sci. USA. 107, 22687–22692.
  63. Song H., Moon M., Choe H.K., Han D.H., Jang C., Kim A., Cho S., Kim K., Mook-Jung I. (2015) Aβ-Induced degradation of BMAL1 and CBP leads to circadian rhythm disruption in Alzheimer’s disease. Mol. Neurodegener. 10, 13.
  64. Iyer N.G., Özdag H., Caldas C. (2004) p300/CBP and cancer. Oncogene. 23, 4225–4231.
  65. Wang F., Marshall C.B., Ikura M. (2013) Transcriptional/epigenetic regulator CBP/p300 in tumorigenesis: structural and functional versatility in target recognition. Cell. Mol. Life Sci. 70, 3989–4008.
  66. Waddell A.R., Huang H., Liao D. (2021) CBP/p300: critical co-activators for nuclear steroid hormone receptors and emerging therapeutic targets in prostate and breast cancers. Cancers (Basel). 13(12), 2872.
  67. Chen Q., Yang B., Liu X., Zhang X.D., Zhang L., Liu T. (2022) Histone acetyltransferases CBP/p300 in tumorigenesis and CBP/p300 inhibitors as promising novel anticancer agents. Theranostics. 12, 4935–4948.
  68. Ghosh A.K. (2020) p300 in cardiac development and accelerated cardiac aging. Aging Dis. 11, 916–926.
  69. Lazar A.G., Vlad M.L., Manea A., Simionescu M., Manea S.A. (2021) Activated histone acetyltransferase p300/CBP-related signalling pathways mediate up-regulation of NADPH oxidase, inflammation, and fibrosis in diabetic kidney. Antioxidants (Basel). 10, 1356.
  70. Xiong Y., Zhang M., Li Y. (2020) Recent advances in the development of CBP/p300 bromodomain inhibitors. Curr. Med. Chem. 27, 5583–5598.
  71. He Z.X., Wei B.F., Zhang X., Gong Y.P., Ma L.Y., Zhao W. (2021) Current development of CBP/p300 inhibitors in the last decade. Eur. J. Med. Chem. 209, 112861.
  72. Valor L.M., Viosca J., Lopez-Atalaya J.P., Barco A. (2013) Lysine acetyltransferases CBP and p300 as therapeutic targets in cognitive and neurodegenerative disorders. Curr. Pharm. Des. 19, 5051–5064.
  73. Singh A.K., Neo S.H., Liwang C., Pang K.K.L., Leng J.C.K., Sinha S.H., Shetty M.S., Vasudevan M., Rao V.J., Joshi I., Eswaramoorthy M., Pavon M.V., Sheila A.R., Navakkode S., Kundu T.K., Sajikumar S. (2022) Glucose derived carbon nanosphere (CSP) conjugated TTK21, an activator of the histone acetyltransferases CBP/p300, ameliorates amyloid-beta 1–42 induced deficits in plasticity and associativity in hippocampal CA1 pyramidal neurons. Aging Cell. 21, e13675.

补充文件

附件文件
动作
1. JATS XML
下载
2.

下载 (103KB)
索引源数据
3.

下载 (168KB)
索引源数据
4.

下载 (170KB)
索引源数据
5.

下载 (210KB)
索引源数据
6.

下载 (177KB)
索引源数据
7.

下载 (192KB)
索引源数据
8.

下载 (204KB)
索引源数据
9.

下载 (196KB)
索引源数据
10.

下载 (198KB)
索引源数据
11.

下载 (192KB)
索引源数据
12.

下载 (207KB)
索引源数据

版权所有 © Л.А. Коваль, Е.Н. Прошкина, Н.В. Земская, И.А. Соловьёв, Е.В. Щеголева, М.В. Шапошников, А.А. Москалев, 2023

##common.cookie##