Potential functions and mechanisms of lysine crotonylation modification (Kcr) in tumorigenesis and lymphatic metastasis of papillary thyroid cancer (PTC).
Humans
Thyroid Cancer, Papillary
/ metabolism
Lysine
/ metabolism
Thyroid Neoplasms
/ pathology
Lymphatic Metastasis
Carcinogenesis
/ pathology
Middle Aged
Female
Male
Gene Expression Regulation, Neoplastic
Protein Interaction Maps
Gene Ontology
Signal Transduction
Adult
Protein Processing, Post-Translational
Crotonylation
Lymphatic metastasis
Papillary thyroid cancer
Tumorigenesis
Journal
Journal of translational medicine
ISSN: 1479-5876
Titre abrégé: J Transl Med
Pays: England
ID NLM: 101190741
Informations de publication
Date de publication:
29 Sep 2024
29 Sep 2024
Historique:
received:
18
06
2024
accepted:
16
09
2024
medline:
29
9
2024
pubmed:
29
9
2024
entrez:
28
9
2024
Statut:
epublish
Résumé
To examine the putative functions and mechanisms of lysine crotonylation (Kcr) during the development and progression of papillary thyroid cancer (PTC). Samples of thyroid cancer tissues were collected and subjected to liquid chromatography-tandem mass spectrometry. Crotonylated differentially expressed proteins (DEPs) and differentially expressed Kcr sites (DEKSs) were analyzed by Motif, dynamic expression model analysis (Mfuzz), subcellular localization, Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway annotation, Go Ontology (GO) annotation, and protein-protein interaction analysis (PPI). Validation was performed by immunohistochemistry (IHC). A total of 262 crotonylated DEPs and 702 DEKSs were quantitated. First, for the tumor/normal comparison, a dynamic expression model analysis (Mfuzz) of the DEKSs revealed that clusters 1, 3, and 4 increased with the progression of thyroid cancer; however, cluster 6 showed a dramatic increase during the transition from N0-tumor to N1-tumor. Furthermore, based on GO annotation, KEGG, and PPI, the crotonylated DEPs were primarily enriched in the PI3K-Akt signaling pathway, Cell cycle, and Hippo signaling pathway. Of note, crosstalk between the proteome and Kcr proteome suggested a differential changing trend, which was enriched in Thyroid hormone synthesis, Pyruvate metabolism, TCA cycle, Cell cycle, and Apoptosis pathways. Similarly, for the LNM comparison group, the DEKSs and related DEPs were primarily enriched in Hydrogen peroxide catabolic process and Tight junction pathway. Finally, according to The Cancer Genome Atlas Program (TCGA) database, the differential expression of Kcr DEPs were associated with the prognosis of thyroid cancer, indicating the prognostic significance of these proteins. Moreover, based on the clinical validation of 47 additional samples, Kcr was highly expressed in thyroid tumor tissues compared with normal tissue (t = 9.792, P < 0.001). In addition, a positive correlation was observed between Kcr and N-cadherin (r = 0.5710, P = 0.0015). Moreover, N-cadherin expression was higher in the relatively high Kcr expression group (χ Higher Kcr expression was correlated with thyroid tumorigenesis and lymphatic metastasis, which may regulate thyroid cancer progression by Pyruvate metabolism, TCA cycle, Cell cycle, and other pathways.
Identifiants
pubmed: 39342359
doi: 10.1186/s12967-024-05651-4
pii: 10.1186/s12967-024-05651-4
doi:
Substances chimiques
Lysine
K3Z4F929H6
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
874Subventions
Organisme : the Jilin Province Science and Technology Development Project
ID : YDZJ202201ZYTS112
Organisme : the project of China-Japan Union Hospital
ID : 2023CL01
Organisme : the Project of Jilin Provincial Finance Department
ID : 2023SCZ26
Organisme : the Project of Jilin Provincial Finance Department
ID : 2023SCZ51
Informations de copyright
© 2024. The Author(s).
Références
Su Z, Bao W, Yang G, Liu J, Zhao B. SOX12 promotes thyroid cancer cell proliferation and invasion by regulating the expression of POU2F1 and POU3F1. Yonsei Med J. 2022;63:591.
pubmed: 35619584
pmcid: 9171662
doi: 10.3349/ymj.2022.63.6.591
Kang IK, Kim K, Park J, Bae JS, Kim JS. Central lymph node ratio predicts recurrence in patients with N1b papillary thyroid carcinoma. Cancers. 2022;14:3677.
pubmed: 35954338
pmcid: 9367408
doi: 10.3390/cancers14153677
Hu Y, Pan J, Shah P, Ao M, Thomas SN, Liu Y, et al. Integrated proteomic and glycoproteomic characterization of human high-grade serous ovarian carcinoma. Cell Rep. 2020;33: 108276.
pubmed: 33086064
pmcid: 7970828
doi: 10.1016/j.celrep.2020.108276
Ruiz-Andres O, Sanchez-Niño MD, Cannata-Ortiz P, Ruiz-Ortega M, Egido J, Ortiz A, et al. Histone lysine-crotonylation in acute kidney injury. Dis Models Mech. 2016. https://doi.org/10.1242/dmm.024455 .
doi: 10.1242/dmm.024455
Minguez P, Parca L, Diella F, Mende DR, Kumar R, Helmer-Citterich M, et al. Deciphering a global network of functionally associated post-translational modifications. Mol Syst Biol. 2012;8:599.
pubmed: 22806145
pmcid: 3421446
doi: 10.1038/msb.2012.31
Samanta L, Swain N, Ayaz A, Venugopal V, Agarwal A. Post-translational modifications in sperm proteome: the chemistry of proteome diversifications in the pathophysiology of male factor infertility. Biochim Biophys Acta Gen Sub. 2016;1860:1450–65.
doi: 10.1016/j.bbagen.2016.04.001
Vu LD, Gevaert K, De Smet I. Protein language: post-translational modifications talking to each other. Trends Plant Sci. 2018;23:1068–80.
pubmed: 30279071
doi: 10.1016/j.tplants.2018.09.004
Bao X, Liu Z, Zhang W, Gladysz K, Fung YME, Tian G, et al. Glutarylation of histone H4 lysine 91 regulates chromatin dynamics. Mol Cell. 2019;76:660-675.e9.
pubmed: 31542297
doi: 10.1016/j.molcel.2019.08.018
Xie Z, Zhang D, Chung D, Tang Z, Huang H, Dai L, et al. Metabolic regulation of gene expression by histone lysine β-hydroxybutyrylation. Mol Cell. 2016;62:194–206.
pubmed: 27105115
pmcid: 5540445
doi: 10.1016/j.molcel.2016.03.036
Chen Y, Sprung R, Tang Y, Ball H, Sangras B, Kim SC, et al. Lysine propionylation and butyrylation are novel post-translational modifications in histones. Mol Cell Proteomics. 2007;6:812–9.
pubmed: 17267393
doi: 10.1074/mcp.M700021-MCP200
Zhang Z, Tan M, Xie Z, Dai L, Chen Y, Zhao Y. Identification of lysine succinylation as a new post-translational modification. Nat Chem Biol. 2011;7:58–63.
pubmed: 21151122
doi: 10.1038/nchembio.495
Xu W, Wan J, Zhan J, Li X, He H, Shi Z, et al. Global profiling of crotonylation on non-histone proteins. Cell Res. 2017;27:946–9.
pubmed: 28429772
pmcid: 5518986
doi: 10.1038/cr.2017.60
Sun H, Liu X, Li F, Li W, Zhang J, Xiao Z, et al. First comprehensive proteome analysis of lysine crotonylation in seedling leaves of Nicotiana tabacum. Sci Rep. 2017;7:3013.
pubmed: 28592803
pmcid: 5462846
doi: 10.1038/s41598-017-03369-6
Yu AQ, Wang J, Jiang ST, Yuan LQ, Ma HY, Hu YM, et al. SIRT7-induced PHF5A decrotonylation regulates aging progress through alternative splicing-mediated downregulation of CDK2. Front Cell Dev Biol. 2021;9: 710479.
pubmed: 34604215
pmcid: 8484718
doi: 10.3389/fcell.2021.710479
Sabari BR, Tang Z, Huang H, Yong-Gonzalez V, Molina H, Kong HE, et al. Intracellular crotonyl-CoA stimulates transcription through p300-catalyzed histone crotonylation. Mol Cell. 2015;58:203–15.
pubmed: 25818647
pmcid: 4501262
doi: 10.1016/j.molcel.2015.02.029
Sánchez-Tilló E, De Barrios O, Siles L, Cuatrecasas M, Castells A, Postigo A. β-catenin/TCF4 complex induces the epithelial-to-mesenchymal transition (EMT)-activator ZEB1 to regulate tumor invasiveness. Proc Natl Acad Sci USA. 2011;108:19204–9.
pubmed: 22080605
pmcid: 3228467
doi: 10.1073/pnas.1108977108
Zhong J, Liu C, Zhang QH, Chen L, Shen Y-Y, Chen Y-J, et al. TGF-β1 induces HMGA1 expression: the role of HMGA1 in thyroid cancer proliferation and invasion. Int J Oncol. 2017;50:1567–78.
pubmed: 28393241
pmcid: 5403427
doi: 10.3892/ijo.2017.3958
Zhong J, Liu C, Chen Y, Zhang Q, Yang J, Kang X, et al. The association between S100A13 and HMGA1 in the modulation of thyroid cancer proliferation and invasion. J Transl Med. 2016;14:80.
pubmed: 27008379
pmcid: 4804518
doi: 10.1186/s12967-016-0824-x
Tan M, Luo H, Lee S, Jin F, Yang JS, Montellier E, et al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell. 2011;146:1016–28.
pubmed: 21925322
pmcid: 3176443
doi: 10.1016/j.cell.2011.08.008
Martinez-Moreno JM, Fontecha-Barriuso M, Martín-Sánchez D, Sánchez-Niño MD, Ruiz-Ortega M, Sanz AB, et al. The contribution of histone crotonylation to tissue health and disease: focus on kidney health. Front Pharmacol. 2020;11:393.
pubmed: 32308622
pmcid: 7145939
doi: 10.3389/fphar.2020.00393
Wu M-S, Li X-J, Liu C-Y, Xu Q, Huang J-Q, Gu S, et al. Effects of histone modification in major depressive disorder. CN. 2022;20:1261–77.
doi: 10.2174/1570159X19666210922150043
Fang Y, Xu X, Ding J, Yang L, Doan MT, Karmaus PWF, et al. Histone crotonylation promotes mesoendodermal commitment of human embryonic stem cells. Cell Stem Cell. 2021;28:748-763.e7.
pubmed: 33450185
pmcid: 8026719
doi: 10.1016/j.stem.2020.12.009
Li D, Dewey MG, Wang L, Falcinelli SD, Wong LM, Tang Y, et al. Crotonylation sensitizes IAPi-induced disruption of latent HIV by enhancing p100 cleavage into p52. iScience. 2022;25:103649.
pubmed: 35024584
doi: 10.1016/j.isci.2021.103649
Liao W, Xu N, Zhang H, Liao W, Wang Y, Wang S, et al. Persistent high glucose induced EPB41L4A-AS1 inhibits glucose uptake via GCN5 mediating crotonylation and acetylation of histones and non-histones. Clin Transl Med. 2022;12: e699.
pubmed: 35184403
pmcid: 8858623
doi: 10.1002/ctm2.699
Xu X, Zhu X, Liu F, Lu W, Wang Y, Yu J. The effects of histone crotonylation and bromodomain protein 4 on prostate cancer cell lines. Transl Androl Urol. 2021;10:900–14.
pubmed: 33718091
pmcid: 7947446
doi: 10.21037/tau-21-53
Liao M, Chu W, Sun X, Zheng W, Gao S, Li D, et al. Reduction of H3K27cr modification during DNA damage in colon cancer. Front Oncol. 2022;12: 924061.
pubmed: 35936700
pmcid: 9353715
doi: 10.3389/fonc.2022.924061
Zhang X, Chen J, Dong Q, Zhu J, Peng R, He C, et al. Lysine acylation modification landscape of Brucella abortus proteome and its virulent proteins. Front Cell Dev Biol. 2022;10: 839822.
pubmed: 35300419
pmcid: 8921143
doi: 10.3389/fcell.2022.839822
Yu H, Bu C, Liu Y, Gong T, Liu X, Liu S, et al. Global crotonylome reveals CDYL-regulated RPA1 crotonylation in homologous recombination–mediated DNA repair. Sci Adv. 2020;6:eaay4697.
pubmed: 32201722
pmcid: 7069697
doi: 10.1126/sciadv.aay4697
Zhang Y, Chen Y, Zhang Z, Tao X, Xu S, Zhang X, et al. Acox2 is a regulator of lysine crotonylation that mediates hepatic metabolic homeostasis in mice. Cell Death Dis. 2022;13:279.
pubmed: 35351852
pmcid: 8964741
doi: 10.1038/s41419-022-04725-9
Zhang D, Tang J, Xu Y, Huang X, Wang Y, Jin X, et al. Global crotonylome reveals hypoxia-mediated lamin A crotonylation regulated by HDAC6 in liver cancer. Cell Death Dis. 2022;13:717.
pubmed: 35977926
pmcid: 9385620
doi: 10.1038/s41419-022-05165-1
Qian Z, Ye J, Li J, Che Y, Yu W, Xu P, et al. Decrotonylation of AKT1 promotes AKT1 phosphorylation and activation during myogenic differentiation. J Adv Res. 2023;50:117–33.
pubmed: 36265762
doi: 10.1016/j.jare.2022.10.005
Cai W, Xu D, Zeng C, Liao F, Li R, Lin Y, et al. Modulating lysine crotonylation in cardiomyocytes improves myocardial outcomes. Circ Res. 2022;131:456–72.
pubmed: 35920168
doi: 10.1161/CIRCRESAHA.122.321054
Huang J, Tang D, Zheng F, Xu H, Dai Y. Comprehensive analysis of lysine crotonylation modification in patients with chronic renal failure. BMC Nephrol. 2021;22:310.
pubmed: 34517817
pmcid: 8439085
doi: 10.1186/s12882-021-02445-4
Liu Y, Li Y, Liang J, Sun Z, Sun C. Non-histone lysine crotonylation is involved in the regulation of white fat browning. IJMS. 2022;23:12733.
pubmed: 36361522
pmcid: 9658748
doi: 10.3390/ijms232112733
Lao Y, Cui X, Xu Z, Yan H, Zhang Z, Zhang Z, et al. Glutaryl-CoA dehydrogenase suppresses tumor progression and shapes an anti-tumor microenvironment in hepatocellular carcinoma. J Hepatol. 2024; S0168827824003696.
Hou J-Y, Cao J, Gao L-J, Zhang F-P, Shen J, Zhou L, et al. Upregulation of α enolase (ENO1) crotonylation in colorectal cancer and its promoting effect on cancer cell metastasis. Biochem Biophys Res Commun. 2021;578:77–83.
pubmed: 34547627
doi: 10.1016/j.bbrc.2021.09.027
Gao M, Wang J, Rousseaux S, Tan M, Pan L, Peng L, et al. Metabolically controlled histone H4K5 acylation/acetylation ratio drives BRD4 genomic distribution. Cell Rep. 2021;36: 109460.
pubmed: 34320364
doi: 10.1016/j.celrep.2021.109460
Liang N, Mi L, Li J, Li T, Chen J, Dionigi G, et al. Pan-cancer analysis of the oncogenic and prognostic role of PKM2: a potential target for survival and immunotherapy. BioMed Res Int. 2023;2023:1–14.
doi: 10.1155/2023/3375109
Tian J, Luo B. Identification of three prognosis-related differentially expressed lncRNAs driven by copy number variation in thyroid cancer. J Immunol Res. 2022;2022:1–18.
Gil F, Miranda-Filho A, Uribe-Perez C, Arias-Ortiz NE, Yépez-Chamorro MC, Bravo LM, et al. Impact of the management and proportion of lost to follow-up cases on cancer survival estimates for small population-based cancer registries. J Cancer Epidemiol. 2022;2022:1–10.
doi: 10.1155/2022/9068214
Neto V, Esteves-Ferreira S, Inácio I, Alves M, Dantas R, Almeida I, et al. Metabolic profile characterization of different thyroid nodules using FTIR spectroscopy: a review. Metabolites. 2022;12:53.
pubmed: 35050174
pmcid: 8777789
doi: 10.3390/metabo12010053
Walenta JH, Didier AJ, Liu X, Krämer H. The golgi-associated Hook3 protein is a member of a novel family of microtubule-binding proteins. J Cell Biol. 2001;152:923–34.
pubmed: 11238449
pmcid: 2198811
doi: 10.1083/jcb.152.5.923
Ciampi R, Giordano TJ, Wikenheiser-Brokamp K, Koenig RJ, Nikiforov YE. HOOK3-RET: a novel type of RET/PTC rearrangement in papillary thyroid carcinoma. Endocr Relat Cancer. 2007;14:445–52.
pubmed: 17639057
doi: 10.1677/ERC-07-0039
Melling N, Harutyunyan L, Hube-Magg C, Kluth M, Simon R, Lebok P, et al. High-level HOOK3 expression is an independent predictor of poor prognosis associated with genomic instability in prostate cancer. PLoS ONE. 2015;10:e0134614.
pubmed: 26230842
pmcid: 4521853
doi: 10.1371/journal.pone.0134614
Gao S, Wang S, Zhao Z, Zhang C, Liu Z, Ye P, et al. TUBB4A interacts with MYH9 to protect the nucleus during cell migration and promotes prostate cancer via GSK3β/β-catenin signalling. Nat Commun. 2022;13:2792.
pubmed: 35589707
pmcid: 9120517
doi: 10.1038/s41467-022-30409-1
Liu L, Chen C, Liu P, Li J, Pang Z, Zhu J, et al. MYH10 combines with MYH9 to recruit USP45 by deubiquitinating snail and promotes serous ovarian cancer carcinogenesis, progression, and cisplatin resistance. Adv Sci. 2023;10:2203423.
doi: 10.1002/advs.202203423
Li Q, Luo H, Dai F, Wang R, Fan X, Luo Y, et al. SAMD9 promotes postoperative recurrence of esophageal squamous cell carcinoma by stimulating MYH9-mediated GSK3 β / β -catenin signaling. Adv Sci. 2023;10:2203573.
doi: 10.1002/advs.202203573
Hu R, Cao Y, Wang Y, Zhao T, Yang K, Fan M, et al. TMEM120B strengthens breast cancer cell stemness and accelerates chemotherapy resistance via β1-integrin/FAK-TAZ-mTOR signaling axis by binding to MYH9. Breast Cancer Res. 2024;26:48.
pubmed: 38504374
pmcid: 10949598
doi: 10.1186/s13058-024-01802-z
Xu J, Wang J, He Z, Chen P, Jiang X, Chen Y, et al. LncRNA CERS6-AS1 promotes proliferation and metastasis through the upregulation of YWHAG and activation of ERK signaling in pancreatic cancer. Cell Death Dis. 2021;12:648.
pubmed: 34168120
pmcid: 8225895
doi: 10.1038/s41419-021-03921-3
Cao Z-Q, Wang Z, Leng P. Aberrant N-cadherin expression in cancer. Biomed Pharmacother. 2019;118: 109320.
pubmed: 31545265
doi: 10.1016/j.biopha.2019.109320