1. School of Integrated Chinese and Western Medicine, Anhui University of Chinese Medicine,Anhui,Hefei,China,230012
2. Cancer Research Centre, Beijing Chest Hospital, Capital Medical University/Beijing Tuberculosis and Thoracic Tumor Research Institute,Beijing,China,101149
3. Department of Biochemistry and Molecular Biology, School of Integrated Chinese and Western Medicine, Anhui University of Chinese Medicine,Anhui,Hefei,China,230012
Published:2023,
Published Online:1 November 2023,
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Rui Shen, Hongyun Ruan, Shuye Lin, et al. Lysine succinylation, the metabolic bridge between cancer and immunity. [J]. Genes & Diseases 1(6):2470-2478(2023)
Rui Shen, Hongyun Ruan, Shuye Lin, et al. Lysine succinylation, the metabolic bridge between cancer and immunity. [J]. Genes & Diseases 1(6):2470-2478(2023) DOI: 10.1016/j.gendis.2022.10.028.
Lysine succinylation is a naturally occurring post-translational modification (PTM) that regulates the stability and function of proteins. It can be regulated by enzymes such as SIRT5 and SIRT7. Recently
the effect and significance of lysine succinylation in cancer and its implication in immunity have been extensively explored. Lysine succinylation is involved in the malignant phenotype of cancer cells. Abnormal regulation of lysine succinylation occurs in different cancers
and inhibitors targeting lysine succinylation regulatory enzymes can be used as potential anti-cancer strategies. Therefore
this review focused on the target protein lysine succinylation and its functions in cancer and immunity
in order to provide a reference for finding more potential clinical cancer targets in the future.
ImmunityMitochondriaSIRT5Succinyl-CoASuccinylation
1 A. Sreedhar, E.K. Wiese, T. HitosugiEnzymatic and metabolic regulation of lysine succinylation Genes Dis, 7 (2) (2020), pp. 166-171
2 W. Fischle, Y. Wang, C.D. AllisHistone and chromatin cross-talk Curr Opin Cell Biol, 15 (2) (2003), pp. 172-183
3 Z. Xie, J. Dai, L. Dai, et al.Lysine succinylation and lysine malonylation in histones Mol Cell Proteomics, 11 (5) (2012), pp. 100-107
4 Z. Zhang, M. Tan, Z. Xie, et al.Identification of lysine succinylation as a new post-translational modification Nat Chem Biol, 7 (1) (2011), pp. 58-63
5 B.T. Weinert, C. Schölz, S.A. Wagner, et al.Lysine succinylation is a frequently occurring modification in prokaryotes and eukaryotes and extensively overlaps with acetylation Cell Rep, 4 (4) (2013), pp. 842-851
6 G. Colak, Z. Xie, A.Y. Zhu, et al.Identification of lysine succinylation substrates and the succinylation regulatory enzyme CobB in Escherichia coli Mol Cell Proteomics, 12 (12) (2013), pp. 3509-3520
7 D. Listunov, B.M. Linhares, E. Kim, et al.Development of potent dimeric inhibitors of GAS41 YEATS domain Cell Chem Biol, 28 (12) (2021), pp. 1716-1727.e6
8 Y. Wang, J. Jin, M.W.H. Chung, et al.Identification of the YEATS domain of GAS41 as a pH-dependent reader of histone succinylation Proc Natl Acad Sci U S A, 115 (10) (2018), pp. 2365-2370
9 J. Huang, M.E. FraserStructural basis for the binding of succinate to succinyl-CoA synthetase Acta Crystallogr D Struct Biol, 72 (Pt 8) (2016), pp. 912-921
10 W. Kang, M. Suzuki, T. Saito, et al.Emerging role of TCA cycle-related enzymes in human diseases Int J Mol Sci, 22 (23) (2021), Article 13057
11 J.S. Burch, J.R. Marcero, J.A. Maschek, et al.Glutamine via α-ketoglutarate dehydrogenase provides succinyl-CoA for heme synthesis during erythropoiesis Blood, 132 (10) (2018), pp. 987-998
12 J. Park, Y. Chen, D.X. Tishkoff, et al.SIRT5-mediated lysine desuccinylation impacts diverse metabolic pathways Mol Cell, 50 (6) (2013), pp. 919-930
13 Y. Wang, Y.R. Guo, K. Liu, et al.KAT2A coupled with the α-KGDH complex acts as a histone H3 succinyltransferase Nature, 552 (7684) (2017), pp. 273-277
14 G. Yang, Y. Yuan, H. Yuan, et al.Histone acetyltransferase 1 is a succinyltransferase for histones and non-histones and promotes tumorigenesis EMBO Rep, 22 (2) (2021), Article e50967
15 L. Li, L. Shi, S. Yang, et al.SIRT7 is a histone desuccinylase that functionally links to chromatin compaction and genome stability Nat Commun, 7 (2016), Article 12235
16 J. Du, Y. Zhou, X. Su, et al.Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase Science, 334 (6057) (2011), pp. 806-809
17 J. Smestad, L. Erber, Y. Chen, et al.Chromatin succinylation correlates with active gene expression and is perturbed by defective TCA cycle metabolism iScience, 2 (2018), pp. 63-75
18 M. Tan, C. Peng, K.A. Anderson, et al.Lysine glutarylation is a protein posttranslational modification regulated by SIRT5 Cell Metabol, 19 (4) (2014), pp. 605-617
19 S. Trefely, C.D. Lovell, N.W. Snyder, et al.Compartmentalised acyl-CoA metabolism and roles in chromatin regulation Mol Metabol, 38 (2020), Article 100941
20 M.J. Rardin, W. He, Y. Nishida, et al.SIRT5 regulates the mitochondrial lysine succinylome and metabolic networks Cell Metabol, 18 (6) (2013), pp. 920-933
21 Z.F. Lin, H.B. Xu, J.Y. Wang, et al.SIRT5 desuccinylates and activates SOD1 to eliminate ROS Biochem Biophys Res Commun, 441 (1) (2013), pp. 191-195
22 M.J. Lukey, K.S. Greene, R.A. CerioneLysine succinylation and SIRT5 couple nutritional status to glutamine catabolism Mol Cell Oncol, 7 (3) (2020), Article 1735284
23 S.B. Hake, A. Xiao, C.D. AllisLinking the epigenetic 'language' of covalent histone modifications to cancer Br J Cancer, 90 (4) (2004), pp. 761-769
24 S. Kankotia, P.W. StacpooleDichloroacetate and cancer: new home for an orphan drug? Biochim Biophys Acta, 1846 (2) (2014), pp. 617-629
25 D. Zhu, L. Hou, B. Hu, et al.Crosstalk among proteome, acetylome and succinylome in colon cancer HCT116 cell treated with sodium dichloroacetate Sci Rep, 6 (2016), Article 37478
26 S. Mazurek, C.B. Boschek, F. Hugo, et al.Pyruvate kinase type M2 and its role in tumor growth and spreading Semin Cancer Biol, 15 (4) (2005), pp. 300-308
27 X. Ye, X. Niu, L. Gu, et al.Desuccinylation of pyruvate kinase M2 by SIRT5 contributes to antioxidant response and tumor growth Oncotarget, 8 (4) (2017), pp. 6984-6993
28 M. Xiao, H. Yang, W. Xu, et al.Inhibition of α-KG-dependent histone and DNA demethylases by fumarate and succinate that are accumulated in mutations of FH and SDH tumor suppressors Genes Dev, 26 (12) (2012), pp. 1326-1338
29 F. Zeng, H. Pang, Y. Chen, et al.First succinylome profiling of Vibrio alginolyticus reveals key role of lysine succinylation in cellular metabolism and virulence Front Cell Infect Microbiol, 10 (2020), Article 626574
30 Y. Song, J. Wang, Z. Cheng, et al.Quantitative global proteome and lysine succinylome analyses provide insights into metabolic regulation and lymph node metastasis in gastric cancer Sci Rep, 7 (2017), Article 42053
31 G. Wang, J.G. Meyer, W. Cai, et al.Regulation of UCP1 and mitochondrial metabolism in brown adipose tissue by reversible succinylation Mol Cell, 74 (4) (2019), pp. 844-857.e7
32 J. Liu, Y. Shangguan, D. Tang, et al.Histone succinylation and its function on the nucleosome J Cell Mol Med, 25 (15) (2021), pp. 7101-7109
33 L. Zorro Shahidian, M. Haas, S. Le Gras, et al.Succinylation of H3K122 destabilizes nucleosomes and enhances transcription EMBO Rep, 22 (3) (2021), Article e51009
34 L. Xie, W. Liu, Q. Li, et al.First succinyl-proteome profiling of extensively drug-resistant Mycobacterium tuberculosis revealed involvement of succinylation in cellular physiology J Proteome Res, 14 (1) (2015), pp. 107-119
35 M. Lacroix, R. Riscal, G. Arena, et al.Metabolic functions of the tumor suppressor p53:implications in normal physiology, metabolic disorders, and cancer Mol Metabol, 33 (2020), pp. 2-22
36 F. Kruiswijk, C.F. Labuschagne, K.H. Vousdenp53 in survival, death and metabolic health: a lifeguard with a licence to kill Nat Rev Mol Cell Biol, 16 (7) (2015), pp. 393-405
37 Y. Liu, O. Tavana, W. Gup53 modifications: exquisite decorations of the powerful guardian J Mol Cell Biol, 11 (7) (2019), pp. 564-577
38 X. Liu, F. Rong, J. Tang, et al.Repression of p53 function by SIRT5-mediated desuccinylation at Lysine 120 in response to DNA damage Cell Death Differ, 29 (4) (2022), pp. 722-736
39 X. Gao, H. Bao, L. Liu, et al.Systematic analysis of lysine acetylome and succinylome reveals the correlation between modification of H2A.X complexes and DNA damage response in breast cancer Oncol Rep, 43 (6) (2020), pp. 1819-1830
40 C. Wang, C. Zhang, X. Li, et al.CPT1A-mediated succinylation of S100A10 increases human gastric cancer invasion J Cell Mol Med, 23 (1) (2019), pp. 293-305
41 X. Li, C. Zhang, T. Zhao, et al.Lysine-222 succinylation reduces lysosomal degradation of lactate dehydrogenase a and is increased in gastric cancer J Exp Clin Cancer Res, 39 (1) (2020), p. 172
42 Z. Guo, F. Pan, L. Peng, et al.Systematic proteome and lysine succinylome analysis reveals enhanced cell migration by hyposuccinylation in esophageal squamous cell carcinoma Mol Cell Proteomics, 20 (2021), Article 100053
43 Y.L. Negrón Abril, I.R. Fernandez, J.Y. Hong, et al.Pharmacological and genetic perturbation establish SIRT5 as a promising target in breast cancer Oncogene, 40 (9) (2021), pp. 1644-1658
44 S.M. Carlson, O. GozaniNonhistone lysine methylation in the regulation of cancer pathways Cold Spring Harb Perspect Med, 6 (11) (2016), Article a026435
45 X. Tian, S. Zhang, H.M. Liu, et al.Histone lysine-specific methyltransferases and demethylases in carcinogenesis: new targets for cancer therapy and prevention Curr Cancer Drug Targets, 13 (5) (2013), pp. 558-579
46 J. McGrath, P. TrojerTargeting histone lysine methylation in cancer Pharmacol Ther, 150 (2015), pp. 1-22
47 H.F. Yuan, M. Zhao, L.N. Zhao, et al.PRMT5 confers lipid metabolism reprogramming, tumour growth and metastasis depending on the SIRT7-mediated desuccinylation of PRMT5 K387 in tumours Acta Pharmacol Sin, 43 (9) (2022), pp. 2373-2385
48 W. Lu, X. Che, X. Qu, et al.Succinylation regulators promote clear cell renal cell carcinoma by immune regulation and RNA N6-methyladenosine methylation Front Cell Dev Biol, 9 (2021), Article 622198
49 P.A. Marks, R. BreslowDimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug Nat Biotechnol, 25 (1) (2007), pp. 84-90
50 W. Yang, Z. Sun, C. Hua, et al.Chidamide, a histone deacetylase inhibitor-based anticancer drug, effectively reactivates latent HIV-1 provirus Microb Infect, 20 (9–10) (2018), pp. 626-634
51 M.K. Shanmugam, F. Arfuso, S. Arumugam, et al.Role of novel histone modifications in cancer Oncotarget, 9 (13) (2017), pp. 11414-11426
52 Y. SunE3 ubiquitin ligases as cancer targets and biomarkers Neoplasia, 8 (8) (2006), pp. 645-654
53 J. Liu, C. Qian, X. Cao, et al.Post-translational modification control of innate immunity Immunity, 45 (1) (2016), pp. 15-30
54 L. Deng, T. Meng, L. Chen, et al.The role of ubiquitination in tumorigenesis and targeted drug discovery Signal Transduct Targeted Ther, 5 (1) (2020), p. 11
55 M.D. Hirschey, Y. ZhaoMetabolic regulation by lysine malonylation, succinylation, and glutarylation Mol Cell Proteomics, 14 (9) (2015), pp. 2308-2315
56 C. Peng, Z. Lu, Z. Xie, et al.The first identification of lysine malonylation substrates and its regulatory enzyme Mol Cell Proteomics, 10 (12) (2011) M111.012658
57 W. Wei, A. Mao, B. Tang, et al.Large-scale identification of protein crotonylation reveals its role in multiple cellular functions J Proteome Res, 16 (4) (2017), pp. 1743-1752
58 J. Wan, H. Liu, L. MingLysine crotonylation is involved in hepatocellular carcinoma progression Biomed Pharmacother, 111 (2019), pp. 976-982
59 X. Xu, X. Zhu, F. Liu, et al.The effects of histone crotonylation and bromodomain protein 4 on prostate cancer cell lines Transl Androl Urol, 10 (2) (2021), pp. 900-914
60 S. Jiang, W. YanSuccinate in the cancer-immune cycle Cancer Lett, 390 (2017), pp. 45-47
61 M. Trauelsen, T.K. Hiron, D. Lin, et al.Extracellular succinate hyperpolarizes M2 macrophages through SUCNR1/GPR91-mediated gq signaling Cell Rep, 35 (11) (2021), Article 109246
62 J.Y. Wu, T.W. Huang, Y.T. Hsieh, et al.Cancer-derived succinate promotes macrophage polarization and cancer metastasis via succinate receptor Mol Cell, 77 (2) (2020), pp. 213-227.e5
63 X. Chen, B. Sunkel, M. Wang, et al.Succinate dehydrogenase/complex II is critical for metabolic and epigenetic regulation of T cell proliferation and inflammation Sci Immunol, 7 (70) (2022), Article eabm8161
64 D.G. Franchina, H. Kurniawan, M. Grusdat, et al.Glutathione-dependent redox balance characterizes the distinct metabolic properties of follicular and marginal zone B cells Nat Commun, 13 (1) (2022), p. 1789
65 K.E. Krueger, S. SrivastavaPosttranslational protein modifications: current implications for cancer detection, prevention, and therapeutics Mol Cell Proteomics, 5 (10) (2006), pp. 1799-1810
66 Y. Wang, J. Zhang, B. Li, et al.Advances of proteomics in novel PTM discovery: applications in cancer therapy Small Methods, 3 (5) (2019), Article 1900041
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