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


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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).

About the authors

Yanhuan Wei

Department of Cardiology, The Affiliated Hospital of Qingdao University

Email: info@benthamscience.net

Haixia Wei

, Qingdao Chengyang People’s Hospital

Email: info@benthamscience.net

Chao Tian

Hepatopancreatobiliary Center, Beijing Tsinghua Changgung Hospital, School of Clinical Medicine, Tsinghua University

Email: info@benthamscience.net

Qinchao Wu

Department of Cardiology, The Affiliated Hospital of Qingdao University

Email: info@benthamscience.net

Daisong Li

Department of Cardiology, The Affiliated Hospital of Qingdao University

Email: info@benthamscience.net

Chao Huang

Department of Cardiology, The Affiliated Hospital of Qingdao University

Email: info@benthamscience.net

Guoliang Zhang

Department of Cardiology, The Affiliated Hospital of Qingdao University

Email: info@benthamscience.net

Ruolan Chen

Department of Cardiology, The Affiliated Hospital of Qingdao University

Email: info@benthamscience.net

Ni Wang

Department of Cardiology,, The Affiliated Hospital of Qingdao University

Email: info@benthamscience.net

Yonghong Li

Department of Cardiology, The Affiliated Hospital of Qingdao University

Email: info@benthamscience.net

Bing Li

Department of Genetics, Basic Medicine School, Qingdao University

Author for correspondence.
Email: info@benthamscience.net

Xian-Ming Chu

Department of Cardiology, The Affiliated Hospital of Qingdao University

Author for correspondence.
Email: info@benthamscience.net

References

  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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1016/j.phrs.2019.104542 PMID: 31730804
  6. Cosgriff, T.M. Doxorubicin and ventricular arrhythmia. Ann. Intern. Med., 1980, 92(3), 434-435. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1111/jnc.15112 PMID: 32618370
  28. Moon, B.; Chang, S. Exosome as a delivery vehicle for cancer therapy. Cells, 2022, 11(3), 316. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1016/j.bcp.2017.02.010 PMID: 28214518
  59. Zeuthen, T. Water-transporting proteins. J. Membr. Biol., 2010, 234(2), 57-73. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1016/j.tibs.2013.02.004 PMID: 23490039
  67. Eichler, J. Protein glycosylation. Curr. Biol., 2019, 29(7), R229-R231. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1016/j.redox.2021.102089 PMID: 34364220

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