Generic placeholder image

Combinatorial Chemistry & High Throughput Screening

Editor-in-Chief

ISSN (Print): 1386-2073
ISSN (Online): 1875-5402

Research Article

The Transcriptome Analysis of Circular RNAs Between the Doxorubicin- Induced Cardiomyocytes and Bone Marrow Mesenchymal Stem Cells- Derived Exosomes Treated Ones

Author(s): Yanhuan Wei, Haixia Wei, Chao Tian, Qinchao Wu, Daisong Li, Chao Huang, Guoliang Zhang, Ruolan Chen, Ni Wang, Yonghong Li, Bing Li* and Xian-Ming Chu*

Volume 27, Issue 7, 2024

Published on: 04 January, 2024

Page: [1056 - 1070] Pages: 15

DOI: 10.2174/0113862073261891231115072310

Price: $65

Abstract

Aim: To analyze the sequencing results of circular RNAs (circRNAs) in cardiomyocytes between the doxorubicin (DOX)-injured group and exosomes treatment group. Moreover, to offer potential circRNAs possibly secreted by exosomes mediating the therapeutic effect on DOX-induced cardiotoxicity for further study.

Methods: The DOX-injured group (DOX group) of cardiomyocytes was treated with DOX, while an exosomes-treated group of injured cardiomyocytes were cocultured with bone marrow mesenchymal stem cells (BMSC)-derived exosomes (BEC group). The high-throughput sequencing of circRNAs was conducted after the extraction of RNA from cardiomyocytes. The differential expression of circRNA was analyzed after identifying the number, expression, and conservative of circRNAs. Then, the target genes of differentially expressed circRNAs were predicted based on the targetscan and Miranda database. Next, the GO and KEGG enrichment analyses of target genes of circRNAs were performed. The crucial signaling pathways participating in the therapeutic process were identified. Finally, a real-time quantitative polymerase chain reaction experiment was conducted to verify the results obtained by sequencing.

Results: Thirty-two circRNAs are differentially expressed between the two groups, of which twenty-three circRNAs were elevated in the exosomes-treated group (BEC group). The GO analysis shows that target genes of differentially expressed circRNAs are mainly enriched in the intracellular signalactivity, regulation of nucleic acid-templated transcription, Golgi-related activity, and GTPase activator activity. The KEGG analysis displays that they were involved in the autophagy biological process and NOD-like receptor signaling pathway. The verification experiment suggested that mmu_circ_0000425 (ID: 116324210) was both decreased in the DOX group and elevated in BEC group, which was consistent with the result of sequencing.

Conclusion: mmu_circ_0000425 in exosomes derived from bone marrow mesenchymal stem cells (BMSC) may have a therapeutic role in alleviating doxorubicin-induced cardiotoxicity (DIC).

Keywords: Doxorubicin, cardiotoxicity, exosome, circular RNA, transcriptome analysis, non-coding RNA.

Graphical Abstract
[1]
Zhang, Y.; Zhang, Z. The history and advances in cancer immunotherapy: Understanding the characteristics of tumor-infiltrating immune cells and their therapeutic implications. Cell. Mol. Immunol., 2020, 17(8), 807-821.
[http://dx.doi.org/10.1038/s41423-020-0488-6] [PMID: 32612154]
[2]
Deng, B.; Ma, B.; Ma, Y.; Cao, P.; Leng, X.; Huang, P.; Zhao, Y.; Ji, T.; Lu, X.; Liu, L. Doxorubicin and CpG loaded liposomal spherical nucleic acid for enhanced Cancer treatment. J. Nanobiotechnol., 2022, 20(1), 140.
[http://dx.doi.org/10.1186/s12951-022-01353-5] [PMID: 35303868]
[3]
El-Hussein, A.; Manoto, S.L.; Ombinda-Lemboumba, S.; Alrowaili, Z.A.; Mthunzi-Kufa, P. A review of chemotherapy and photodynamic therapy for lung cancer treatment. Anticancer. Agents Med. Chem., 2021, 21(2), 149-161.
[http://dx.doi.org/10.2174/18715206MTA1uNjQp3] [PMID: 32242788]
[4]
Molinaro, R.; Martinez, J.O.; Zinger, A.; De Vita, A.; Storci, G.; Arrighetti, N.; De Rosa, E.; Hartman, K.A.; Basu, N.; Taghipour, N.; Corbo, C.; Tasciotti, E. Leukocyte-mimicking nanovesicles for effective doxorubicin delivery to treat breast cancer and melanoma. Biomater. Sci., 2020, 8(1), 333-341.
[http://dx.doi.org/10.1039/C9BM01766F] [PMID: 31714542]
[5]
Benjanuwattra, J.; Siri-Angkul, N.; Chattipakorn, S.C.; Chattipakorn, N. Doxorubicin and its proarrhythmic effects: A comprehensive review of the evidence from experimental and clinical studies. Pharmacol. Res., 2020, 151, 104542.
[http://dx.doi.org/10.1016/j.phrs.2019.104542] [PMID: 31730804]
[6]
Cosgriff, T.M. Doxorubicin and ventricular arrhythmia. Ann. Intern. Med., 1980, 92(3), 434-435.
[http://dx.doi.org/10.7326/0003-4819-92-3-434_3] [PMID: 7356243]
[7]
Fang, Z.; Wei, W.; Jiang, X. Monotropein attenuates doxorubicin-induced oxidative stress, inflammation, and arrhythmia via the AKT signal pathway. Biochem. Biophys. Res. Commun., 2023, 638, 14-22.
[http://dx.doi.org/10.1016/j.bbrc.2022.11.058] [PMID: 36436337]
[8]
Ta, N.; Qu, C.; Wu, H.; Zhang, D.; Sun, T.; Li, Y.; Wang, J.; Wang, X.; Tang, T.; Chen, Q.; Liu, L. Mitochondrial outer membrane protein FUNDC2 promotes ferroptosis and contributes to doxorubicin-induced cardiomyopathy. Proc. Natl. Acad. Sci. USA, 2022, 119(36), e2117396119.
[http://dx.doi.org/10.1073/pnas.2117396119] [PMID: 36037337]
[9]
Schirone, L.; D’Ambrosio, L.; Forte, M.; Genovese, R.; Schiavon, S.; Spinosa, G.; Iacovone, G.; Valenti, V.; Frati, G.; Sciarretta, S. Mitochondria and doxorubicin-induced cardiomyopathy: A complex interplay. Cells, 2022, 11(13), 2000.
[http://dx.doi.org/10.3390/cells11132000] [PMID: 35805084]
[10]
Wallace, K.B.; Sardão, V.A.; Oliveira, P.J. Mitochondrial determinants of doxorubicin-induced cardiomyopathy. Circ. Res., 2020, 126(7), 926-941.
[http://dx.doi.org/10.1161/CIRCRESAHA.119.314681] [PMID: 32213135]
[11]
Swain, S.M.; Whaley, F.S.; Ewer, M.S. Congestive heart failure in patients treated with doxorubicin. Cancer, 2003, 97(11), 2869-2879.
[http://dx.doi.org/10.1002/cncr.11407] [PMID: 12767102]
[12]
Younis, N.N.; Salama, A.; Shaheen, M.A.; Eissa, R.G. Pachymic acid attenuated doxorubicin-induced heart failure by suppressing miR-24 and preserving cardiac junctophilin-2 in rats. Int. J. Mol. Sci., 2021, 22(19), 10710.
[http://dx.doi.org/10.3390/ijms221910710] [PMID: 34639051]
[13]
Spivak, M.; Bubnov, R.; Yemets, I.; Lazarenko, L.; Timoshok, N.; Vorobieva, A.; Mohnatyy, S.; Ulberg, Z.; Reznichenko, L.; Grusina, T.; Zhovnir, V.; Zholobak, N. Doxorubicin dose for congestive heart failure modeling and the use of general ultrasound equipment for evaluation in rats. Longitudinal in vivo study. Med. Ultrason., 2013, 15(1), 23-28.
[http://dx.doi.org/10.11152/mu.2013.2066.151.ms1ddc2] [PMID: 23486620]
[14]
Räsänen, M.; Degerman, J.; Nissinen, T.A.; Miinalainen, I.; Kerkelä, R.; Siltanen, A.; Backman, J.T.; Mervaala, E.; Hulmi, J.J.; Kivelä, R.; Alitalo, K. VEGF-B gene therapy inhibits doxorubicin-induced cardiotoxicity by endothelial protection. Proc. Natl. Acad. Sci., 2016, 113(46), 13144-13149.
[http://dx.doi.org/10.1073/pnas.1616168113] [PMID: 27799559]
[15]
Curigliano, G.; Cardinale, D.; Dent, S.; Criscitiello, C.; Aseyev, O.; Lenihan, D.; Cipolla, C.M. Cardiotoxicity of anticancer treatments: Epidemiology, detection, and management. CA Cancer J. Clin., 2016, 66(4), 309-325.
[http://dx.doi.org/10.3322/caac.21341] [PMID: 26919165]
[16]
Han, X.; Zhou, Y.; Liu, W. Precision cardio-oncology: Understanding the cardiotoxicity of cancer therapy. NPJ Precis. Oncol., 2017, 1(1), 31.
[http://dx.doi.org/10.1038/s41698-017-0034-x] [PMID: 29872712]
[17]
Zhao, L.; Qi, Y.; Xu, L.; Tao, X.; Han, X.; Yin, L.; Peng, J. MicroRNA-140-5p aggravates doxorubicin-induced cardiotoxicity by promoting myocardial oxidative stress via targeting Nrf2 and Sirt2. Redox Biol., 2018, 15, 284-296.
[http://dx.doi.org/10.1016/j.redox.2017.12.013] [PMID: 29304479]
[18]
Hou, K.; Shen, J.; Yan, J.; Zhai, C.; Zhang, J.; Pan, J.A.; Zhang, Y.; Jiang, Y.; Wang, Y.; Lin, R.Z.; Cong, H.; Gao, S.; Zong, W.X. Loss of TRIM21 alleviates cardiotoxicity by suppressing ferroptosis induced by the chemotherapeutic agent doxorubicin. EBioMedicine, 2021, 69, 103456.
[http://dx.doi.org/10.1016/j.ebiom.2021.103456] [PMID: 34233258]
[19]
He, C.; Zheng, S.; Luo, Y.; Wang, B. Exosome theranostics: Biology and translational medicine. Theranostics, 2018, 8(1), 237-255.
[http://dx.doi.org/10.7150/thno.21945] [PMID: 29290805]
[20]
Zhang, Y.; Bi, J.; Huang, J.; Tang, Y.; Du, S.; Li, P. Exosome: A review of its classification, isolation techniques, storage, diagnostic and targeted therapy applications. Int. J. Nanomedicine, 2020, 15, 6917-6934.
[http://dx.doi.org/10.2147/IJN.S264498] [PMID: 33061359]
[21]
Yang, D.; Zhang, W.; Zhang, H.; Zhang, F.; Chen, L.; Ma, L.; Larcher, L.M.; Chen, S.; Liu, N.; Zhao, Q.; Tran, P.H.L.; Chen, C.; Veedu, R.N.; Wang, T. Progress, opportunity, and perspective on exosome isolation - efforts for efficient exosome-based theranostics. Theranostics, 2020, 10(8), 3684-3707.
[http://dx.doi.org/10.7150/thno.41580] [PMID: 32206116]
[22]
Kalluri, R.; LeBleu, V.S. The biology, function, and biomedical applications of exosomes. Science, 2020, 367(6478), eaau6977.
[http://dx.doi.org/10.1126/science.aau6977] [PMID: 32029601]
[23]
Lu, M.; Yuan, S.; Li, S.; Li, L.; Liu, M.; Wan, S. the exosome-derived biomarker in atherosclerosis and its clinical application. J. Cardiovasc. Transl. Res., 2019, 12(1), 68-74.
[http://dx.doi.org/10.1007/s12265-018-9796-y] [PMID: 29802541]
[24]
Kok, V.C.; Yu, C.C. Cancer-derived exosomes: Their role in cancer biology and biomarker development. Int. J. Nanomedicine, 2020, 15, 8019-8036.
[http://dx.doi.org/10.2147/IJN.S272378] [PMID: 33116515]
[25]
Xu, Y.X.; Pu, S.D.; Li, X.; Yu, Z.W.; Zhang, Y.T.; Tong, X.W.; Shan, Y.Y.; Gao, X.Y. Exosomal ncRNAs: Novel therapeutic target and biomarker for diabetic complications. Pharmacol. Res., 2022, 178, 106135.
[http://dx.doi.org/10.1016/j.phrs.2022.106135] [PMID: 35192956]
[26]
Barile, L.; Vassalli, G. Exosomes: Therapy delivery tools and biomarkers of diseases. Pharmacol. Ther., 2017, 174, 63-78.
[http://dx.doi.org/10.1016/j.pharmthera.2017.02.020] [PMID: 28202367]
[27]
Soares Martins, T.; Trindade, D.; Vaz, M.; Campelo, I.; Almeida, M.; Trigo, G. da Cruz e Silva, O.A.B.; Henriques, A.G. Diagnostic and therapeutic potential of exosomes in Alzheimer’s disease. J. Neurochem., 2021, 156(2), 162-181.
[http://dx.doi.org/10.1111/jnc.15112] [PMID: 32618370]
[28]
Moon, B.; Chang, S. Exosome as a delivery vehicle for cancer therapy. Cells, 2022, 11(3), 316.
[http://dx.doi.org/10.3390/cells11030316] [PMID: 35159126]
[29]
Choi, H.; Kim, Y.; Mirzaaghasi, A.; Heo, J.; Kim, Y.N.; Shin, J.H.; Kim, S.; Kim, N.H.; Cho, E.S.; In Yook, J.; Yoo, T.H.; Song, E.; Kim, P.; Shin, E.C.; Chung, K.; Choi, K.; Choi, C. Exosome-based delivery of super-repressor IκBα relieves sepsis-associated organ damage and mortality. Sci. Adv., 2020, 6(15), eaaz6980.
[http://dx.doi.org/10.1126/sciadv.aaz6980] [PMID: 32285005]
[30]
Huang, X; Wu, W; Jing, D Engineered exosome as targeted lncRNA MEG3 delivery vehicles for osteosarcoma therapy. J. Control. Release, 2022, 343, 107-117.
[31]
Tian, C.; Yang, Y.; Bai, B.; Wang, S.; Liu, M.; Sun, R.C.; Yu, T.; Chu, X. Potential of exosomes as diagnostic biomarkers and therapeutic carriers for doxorubicin-induced cardiotoxicity. Int. J. Biol. Sci., 2021, 17(5), 1328-1338.
[http://dx.doi.org/10.7150/ijbs.58786] [PMID: 33867849]
[32]
Tian, C.; Yang, Y.; Li, B.; Liu, M.; He, X.; Zhao, L.; Song, X.; Yu, T.; Chu, X.M. Doxorubicin-induced cardiotoxicity may be alleviated by bone marrow mesenchymal stem cell-derived exosomal lncRNA via inhibiting inflammation. J. Inflamm. Res., 2022, 15, 4467-4486.
[http://dx.doi.org/10.2147/JIR.S358471] [PMID: 35966005]
[33]
Xiao, L.; Ma, X.X.; Luo, J.; Chung, H.K.; Kwon, M.S.; Yu, T.X.; Rao, J.N.; Kozar, R.; Gorospe, M.; Wang, J.Y. Circular RNA CircHIPK3 promotes homeostasis of the intestinal epithelium by reducing MicroRNA 29b function. Gastroenterology, 2021, 161(4), 1303-1317.e3.
[http://dx.doi.org/10.1053/j.gastro.2021.05.060] [PMID: 34116030]
[34]
Zhou, W.Y.; Cai, Z.R.; Liu, J.; Wang, D.S.; Ju, H.Q.; Xu, R.H. Circular RNA: Metabolism, functions and interactions with proteins. Mol. Cancer, 2020, 19(1), 172.
[http://dx.doi.org/10.1186/s12943-020-01286-3] [PMID: 33317550]
[35]
Altesha, M.A.; Ni, T.; Khan, A.; Liu, K.; Zheng, X. Circular RNA in cardiovascular disease. J. Cell. Physiol., 2019, 234(5), 5588-5600.
[http://dx.doi.org/10.1002/jcp.27384] [PMID: 30341894]
[36]
Wang, K.; Gao, X.Q.; Wang, T.; Zhou, L.Y. The function and therapeutic potential of circular RNA in cardiovascular diseases. Cardiovasc. Drugs Ther., 2023, 37(1), 181-198.
[http://dx.doi.org/10.1007/s10557-021-07228-5] [PMID: 34269929]
[37]
Li, H.; Xu, J.D.; Fang, X.H.; Zhu, J.N.; Yang, J.; Pan, R.; Yuan, S.J.; Zeng, N.; Yang, Z.Z.; Yang, H.; Wang, X.P.; Duan, J.Z.; Wang, S.; Luo, J.F.; Wu, S.L.; Shan, Z.X. Circular RNA circRNA_000203 aggravates cardiac hypertrophy via suppressing miR-26b-5p and miR-140-3p binding to Gata4. Cardiovasc. Res., 2020, 116(7), 1323-1334.
[http://dx.doi.org/10.1093/cvr/cvz215] [PMID: 31397837]
[38]
Gao, X.; Tian, X.; Huang, Y.; Fang, R.; Wang, G.; Li, D.; Zhang, J.; Li, T.; Yuan, R. Role of circular RNA in myocardial ischemia and ageing-related diseases. Cytokine Growth Factor Rev., 2022, 65, 1-11.
[http://dx.doi.org/10.1016/j.cytogfr.2022.04.005] [PMID: 35561533]
[39]
Davidson, S.M.; Padró, T.; Bollini, S.; Vilahur, G.; Duncker, D.J.; Evans, P.C.; Guzik, T.; Hoefer, I.E.; Waltenberger, J.; Wojta, J.; Weber, C. Progress in cardiac research: From rebooting cardiac regeneration to a complete cell atlas of the heart. Cardiovasc. Res., 2021, 117(10), 2161-2174.
[http://dx.doi.org/10.1093/cvr/cvab200] [PMID: 34114614]
[40]
Gao, Y.; Wang, J.; Zhao, F. CIRI: An efficient and unbiased algorithm for de novo circular RNA identification. Genome Biol., 2015, 16(1), 4.
[http://dx.doi.org/10.1186/s13059-014-0571-3] [PMID: 25583365]
[41]
Lewis, B.P.; Shih, I.; Jones-Rhoades, M.W.; Bartel, D.P.; Burge, C.B. Prediction of mammalian microRNA targets. Cell, 2003, 115(7), 787-798.
[http://dx.doi.org/10.1016/S0092-8674(03)01018-3] [PMID: 14697198]
[42]
Betel, D.; Wilson, M.; Gabow, A.; Marks, D.S.; Sander, C. The microRNA.org resource: Targets and expression. Nucleic Acids Res., 2008, 36(Database issue), D149-D153.
[PMID: 18158296]
[43]
Yu, G.; Wang, L.G.; Han, Y.; He, Q.Y. clusterProfiler: An R package for comparing biological themes among gene clusters. OMICS, 2012, 16(5), 284-287.
[http://dx.doi.org/10.1089/omi.2011.0118] [PMID: 22455463]
[44]
Huang, Y.; Xu, W.; Zhou, R. NLRP3 inflammasome activation and cell death. Cell. Mol. Immunol., 2021, 18(9), 2114-2127.
[http://dx.doi.org/10.1038/s41423-021-00740-6] [PMID: 34321623]
[45]
Wang, S.; Yuan, Y.H.; Chen, N.H.; Wang, H.B. The mechanisms of NLRP3 inflammasome/pyroptosis activation and their role in Parkinson’s disease. Int. Immunopharmacol., 2019, 67, 458-464.
[http://dx.doi.org/10.1016/j.intimp.2018.12.019] [PMID: 30594776]
[46]
Zhang, L; Jiang, YH; Fan, C MCC950 attenuates doxorubicin-induced myocardial injury in vivo and in vitro by inhibiting NLRP3-mediated pyroptosis. Biomed. Pharmacother., 2021, 143, 112133.
[47]
Tavakoli Dargani, Z.; Singla, D.K. Embryonic stem cell-derived exosomes inhibit doxorubicin-induced TLR4-NLRP3-mediated cell death-pyroptosis. Am. J. Physiol. Heart Circ. Physiol., 2019, 317(2), H460-H471.
[http://dx.doi.org/10.1152/ajpheart.00056.2019] [PMID: 31172809]
[48]
Zhang, J.M.; Yu, R.Q.; Wu, F.Z.; Qiao, L.; Wu, X.R.; Fu, Y.J.; Liang, Y.F.; Pang, Y.; Xie, C.Y. BMP-2 alleviates heart failure with type 2 diabetes mellitus and doxorubicin-induced AC16 cell injury by inhibiting NLRP3 inflammasome-mediated pyroptosis. Exp. Ther. Med., 2021, 22(2), 897.
[http://dx.doi.org/10.3892/etm.2021.10329] [PMID: 34257710]
[49]
Pan, J.; Zhang, H.; Lin, H.; Gao, L.; Zhang, H.; Zhang, J.; Wang, C.; Gu, J. Irisin ameliorates doxorubicin-induced cardiac perivascular fibrosis through inhibiting endothelial-to-mesenchymal transition by regulating ROS accumulation and autophagy disorder in endothelial cells. Redox Biol., 2021, 46, 102120.
[http://dx.doi.org/10.1016/j.redox.2021.102120] [PMID: 34479089]
[50]
Qu, Y.; Gao, R.; Wei, X.; Sun, X.; Yang, K.; Shi, H.; Gao, Y.; Hu, S.; Wang, Y.; Yang, J.; Sun, A.; Zhang, F.; Ge, J. Gasdermin D mediates endoplasmic reticulum stress via FAM134B to regulate cardiomyocyte autophagy and apoptosis in doxorubicin-induced cardiotoxicity. Cell Death Dis., 2022, 13(10), 901.
[http://dx.doi.org/10.1038/s41419-022-05333-3] [PMID: 36289195]
[51]
Wang, Y.; Lu, X.; Wang, X.; Qiu, Q.; Zhu, P.; Ma, L.; Ma, X.; Herrmann, J.; Lin, X.; Wang, W.; Xu, X. Atg7 -based autophagy activation reverses doxorubicin-induced cardiotoxicity. Circ. Res., 2021, 129(8), e166-e182.
[http://dx.doi.org/10.1161/CIRCRESAHA.121.319104] [PMID: 34384247]
[52]
He, Q.; Ye, A.; Ye, W.; Liao, X.; Qin, G.; Xu, Y.; Yin, Y.; Luo, H.; Yi, M.; Xian, L.; Zhang, S.; Qin, X.; Zhu, W.; Li, Y. Cancer-secreted exosomal miR-21-5p induces angiogenesis and vascular permeability by targeting KRIT1. Cell Death Dis., 2021, 12(6), 576.
[http://dx.doi.org/10.1038/s41419-021-03803-8] [PMID: 34088891]
[53]
Yang, B.; Feng, X.; Liu, H.; Tong, R.; Wu, J.; Li, C.; Yu, H.; Chen, Y.; Cheng, Q.; Chen, J.; Cai, X.; Wu, W.; Lu, Y.; Hu, J.; Liang, K.; Lv, Z.; Wu, J.; Zheng, S. High-metastatic cancer cells derived exosomal miR92a-3p promotes epithelial-mesenchymal transition and metastasis of low-metastatic cancer cells by regulating PTEN/Akt pathway in hepatocellular carcinoma. Oncogene, 2020, 39(42), 6529-6543.
[http://dx.doi.org/10.1038/s41388-020-01450-5] [PMID: 32917956]
[54]
Gao, P.; Ma, X.; Yuan, M.; Yi, Y.; Liu, G.; Wen, M.; Jiang, W.; Ji, R.; Zhu, L.; Tang, Z.; Yu, Q.; Xu, J.; Yang, R.; Xia, S.; Yang, M.; Pan, J.; Yuan, H.; An, H. E3 ligase Nedd4l promotes antiviral innate immunity by catalyzing K29-linked cysteine ubiquitination of TRAF3. Nat. Commun., 2021, 12(1), 1194.
[http://dx.doi.org/10.1038/s41467-021-21456-1] [PMID: 33608556]
[55]
Yu, B.; Hailman, E.; Wright, S.D. Lipopolysaccharide binding protein and soluble CD14 catalyze exchange of phospholipids. J. Clin. Invest., 1997, 99(2), 315-324.
[http://dx.doi.org/10.1172/JCI119160] [PMID: 9006000]
[56]
Segatori, L.; Paukstelis, P.J.; Gilbert, H.F.; Georgiou, G. Engineered DsbC chimeras catalyze both protein oxidation and disulfide-bond isomerization in Escherichia coli: Reconciling two competing pathways. Proc. Natl. Acad. Sci., 2004, 101(27), 10018-10023.
[http://dx.doi.org/10.1073/pnas.0403003101] [PMID: 15220477]
[57]
Zhang, Y.; Hagenbuch, B. Protein-protein interactions of drug uptake transporters that are important for liver and kidney. Biochem. Pharmacol., 2019, 168, 384-391.
[http://dx.doi.org/10.1016/j.bcp.2019.07.026] [PMID: 31381872]
[58]
Rives, M.L.; Javitch, J.A.; Wickenden, A.D. Potentiating SLC transporter activity: Emerging drug discovery opportunities. Biochem. Pharmacol., 2017, 135, 1-11.
[http://dx.doi.org/10.1016/j.bcp.2017.02.010] [PMID: 28214518]
[59]
Zeuthen, T. Water-transporting proteins. J. Membr. Biol., 2010, 234(2), 57-73.
[http://dx.doi.org/10.1007/s00232-009-9216-y] [PMID: 20091162]
[60]
Raabe, V.; Lai, L.; Morales, J.; Xu, Y.; Rouphael, N.; Davey, R.T.; Mulligan, M.J. Cellular and humoral immunity to Ebola Zaire glycoprotein and viral vector proteins following immunization with recombinant vesicular stomatitis virus-based Ebola vaccine (rVSVΔG-ZEBOV-GP). Vaccine, 2023, 41(8), 1513-1523.
[http://dx.doi.org/10.1016/j.vaccine.2023.01.059] [PMID: 36725433]
[61]
Raja, V.; Sobana, S.; Mercy, C.S.A.; Cotto, B.; Bora, D.P.; Natarajaseenivasan, K. Heterologous DNA prime-protein boost immunization with RecA and FliD offers cross-clade protection against leptospiral infection. Sci. Rep., 2018, 8(1), 6447.
[http://dx.doi.org/10.1038/s41598-018-24674-8] [PMID: 29691454]
[62]
Kundu, K.; Garg, R.; Kumar, S.; Mandal, M.; Tomley, F.M.; Blake, D.P.; Banerjee, P.S. Humoral and cytokine response elicited during immunisation with recombinant Immune Mapped protein-1 (EtIMP-1) and oocysts of Eimeria tenella. Vet. Parasitol., 2017, 244, 44-53.
[http://dx.doi.org/10.1016/j.vetpar.2017.07.025] [PMID: 28917316]
[63]
Leone, M.; Pagnani, A. Predicting protein functions with message passing algorithms. Bioinformatics, 2005, 21(2), 239-247.
[http://dx.doi.org/10.1093/bioinformatics/bth491] [PMID: 15377508]
[64]
Weigt, M.; White, R.A.; Szurmant, H.; Hoch, J.A.; Hwa, T. Identification of direct residue contacts in protein–protein interaction by message passing. Proc. Natl. Acad. Sci., 2009, 106(1), 67-72.
[http://dx.doi.org/10.1073/pnas.0805923106] [PMID: 19116270]
[65]
Iqbal, M.; Freitas, A.A.; Johnson, C.G.; Vergassola, M. Message-passing algorithms for the prediction of protein domain interactions from protein–protein interaction data. Bioinformatics, 2008, 24(18), 2064-2070.
[http://dx.doi.org/10.1093/bioinformatics/btn366] [PMID: 18641010]
[66]
Clarke, S.G. Protein methylation at the surface and buried deep: Thinking outside the histone box. Trends Biochem. Sci., 2013, 38(5), 243-252.
[http://dx.doi.org/10.1016/j.tibs.2013.02.004] [PMID: 23490039]
[67]
Eichler, J. Protein glycosylation. Curr. Biol., 2019, 29(7), R229-R231.
[http://dx.doi.org/10.1016/j.cub.2019.01.003] [PMID: 30939300]
[68]
Mevissen, T.E.T.; Komander, D. Mechanisms of deubiquitinase specificity and regulation. Annu. Rev. Biochem., 2017, 86(1), 159-192.
[http://dx.doi.org/10.1146/annurev-biochem-061516-044916] [PMID: 28498721]
[69]
Baeza, J.; Smallegan, M.J.; Denu, J.M. Mechanisms and dynamics of protein acetylation in mitochondria. Trends Biochem. Sci., 2016, 41(3), 231-244.
[http://dx.doi.org/10.1016/j.tibs.2015.12.006] [PMID: 26822488]
[70]
Xu, Y.; Wu, W.; Han, Q.; Wang, Y.; Li, C.; Zhang, P.; Xu, H. Post-translational modification control of RNA-binding protein hnRNPK function. Open Biol., 2019, 9(3), 180239.
[http://dx.doi.org/10.1098/rsob.180239] [PMID: 30836866]
[71]
Yang, X.; Qian, K. Protein O-GlcNAcylation: Emerging mechanisms and functions. Nat. Rev. Mol. Cell Biol., 2017, 18(7), 452-465.
[http://dx.doi.org/10.1038/nrm.2017.22] [PMID: 28488703]
[72]
Magadum, A.; Singh, N.; Kurian, A.A.; Sharkar, M.T.K.; Chepurko, E.; Zangi, L. Ablation of a single N-glycosylation site in human FSTL 1 induces cardiomyocyte proliferation and cardiac regeneration. Mol. Ther. Nucleic Acids, 2018, 13, 133-143.
[http://dx.doi.org/10.1016/j.omtn.2018.08.021] [PMID: 30290305]
[73]
Chen, Y.; Dorn, G.W., II PINK1-phosphorylated mitofusin 2 is a Parkin receptor for culling damaged mitochondria. Science, 2013, 340(6131), 471-475.
[http://dx.doi.org/10.1126/science.1231031] [PMID: 23620051]
[74]
Fukuda, R.; Gunawan, F.; Beisaw, A.; Jimenez-Amilburu, V.; Maischein, H.M.; Kostin, S.; Kawakami, K.; Stainier, D.Y.R. Proteolysis regulates cardiomyocyte maturation and tissue integration. Nat. Commun., 2017, 8(1), 14495.
[http://dx.doi.org/10.1038/ncomms14495] [PMID: 28211472]
[75]
Li, D.; Yang, Y.; Wang, S.; He, X.; Liu, M.; Bai, B.; Tian, C.; Sun, R.; Yu, T.; Chu, X. Role of acetylation in doxorubicin-induced cardiotoxicity. Redox Biol., 2021, 46, 102089.
[http://dx.doi.org/10.1016/j.redox.2021.102089] [PMID: 34364220]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy