4.6

CiteScore

2.2

Impact Factor
  • ISSN 1674-8301
  • CN 32-1810/R
Volume 37 Issue 5
Sep.  2023
Turn off MathJax
Article Contents
Abstract
Fundings
References
Related Articles
Supplements
Yue Xiao, Yue Peng, Chi Zhang, Wei Liu, Kehan Wang, Jing Li. hucMSC-derived exosomes protect ovarian reserve and restore ovarian function in cisplatin treated mice[J]. The Journal of Biomedical Research, 2023, 37(5): 382-393. DOI: 10.7555/JBR.36.20220166
Citation: Yue Xiao, Yue Peng, Chi Zhang, Wei Liu, Kehan Wang, Jing Li. hucMSC-derived exosomes protect ovarian reserve and restore ovarian function in cisplatin treated mice[J]. The Journal of Biomedical Research, 2023, 37(5): 382-393. DOI: 10.7555/JBR.36.20220166
shu

hucMSC-derived exosomes protect ovarian reserve and restore ovarian function in cisplatin treated mice

  • State Key Laboratory of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu 210029, China

More Information
  • Corresponding author:

    Jing Li, Room B101, Xuehai Building, State Key Laboratory of Reproductive Medicine, Nanjing Medical University, 101 Longmian Avenue, Nanjing, Jiangsu 210029, China. Tel: +86-25-86869504, E-mail: ljwth@njmu.edu.cn

  • Received Date: July 24, 2022
  • Revised Date: August 27, 2022
  • Accepted Date: September 03, 2022
  • Available Online: November 09, 2022
  • Published Date: November 09, 2022
    Graphical Abstract
    • Abstract

  • Anti-cancer therapy often causes premature ovarian insufficiency and infertility as the ovarian follicle reserve is extremely sensitive to chemotherapy drugs, such as cisplatin. Various fertility preservation methods have been explored for women, especially prepubertal girls undergoing radiotherapy and chemotherapy due to cancer. In recent years, mesenchymal stem cell-derived exosomes (MSC-exos) have been reported to play an important role in tissue repair and the treatment of various diseases. In the current study, we observed that human umbilical cord-derived MSC-exos (hucMSC-exos) after short-term culture improved follicular survival and development while receiving cisplatin treatment. Moreover, intravenous injection of hucMSC-exos improved ovarian function and ameliorated inflammatory environment within the ovary. The underlying mechanism of hucMSC-exos on fertility preservation was associated with the down-regulation of p53-related apoptosis and their anti-inflammatory function. Based on these findings, we propose that hucMSC-exos may be a potential approach to improve fertility in women diagnosed with cancer.

    • FullText(HTML)

  • This work is supported by the National Key Research and Development Program of China (Grant Nos. 2018YFC1003703 and 2018YFC1004203) and the National Natural Science Foundation of China (Grant No. 31871513).

    CLC number: R711.75; R730.53, Document code: A

    The authors reported no conflict of interests.

    • References (31)
  • [1]
    Miller III JJ, Williams GF, Leissring JC. Multiple late complications of therapy with cyclophosphamide, including ovarian destruction[J]. Am J Med, 1971, 50(4): 530–535. doi: 10.1016/0002-9343(71)90341-X
    [2]
    Jayasinghe YL, Wallace WHB, Anderson RA. Ovarian function, fertility and reproductive lifespan in cancer patients[J]. Expert Rev Endocrinol Metab, 2018, 13(3): 125–136. doi: 10.1080/17446651.2018.1455498
    [3]
    Ho GY, Woodward N, Coward JIG. Cisplatin versus carboplatin: comparative review of therapeutic management in solid malignancies[J]. Crit Rev Oncol Hematol, 2016, 102: 37–46. doi: 10.1016/j.critrevonc.2016.03.014
    [4]
    Jamieson ER, Lippard SJ. Structure, recognition, and processing of cisplatin-DNA adducts[J]. Chem Rev, 1999, 99(9): 2467–2498. doi: 10.1021/cr980421n
    [5]
    Spears N, Lopes F, Stefansdottir A, et al. Ovarian damage from chemotherapy and current approaches to its protection[J]. Hum Reprod Update, 2019, 25(6): 673–693. doi: 10.1093/humupd/dmz027
    [6]
    Yang Y, Zhao Y, Liao W, et al. Acetylation of FoxO1 activates Bim expression to induce apoptosis in response to histone deacetylase inhibitor depsipeptide treatment[J]. Neoplasia, 2009, 11(4): 313–324. doi: 10.1593/neo.81358
    [7]
    Maidarti M, Anderson RA, Telfer EE. Crosstalk between PTEN/PI3K/Akt signalling and DNA damage in the oocyte: implications for primordial follicle activation, oocyte quality and ageing[J]. Cells, 2020, 9(1): 200. doi: 10.3390/cells9010200
    [8]
    Ding D, Chang Y, Shyu WC, et al. Human umbilical cord mesenchymal stem cells: a new era for stem cell therapy[J]. Cell Transplant, 2015, 24(3): 339–347. doi: 10.3727/096368915X686841
    [9]
    Shareghi-Oskoue O, Aghebati-Maleki L, Yousefi M. Transplantation of human umbilical cord mesenchymal stem cells to treat premature ovarian failure[J]. Stem Cell Res Ther, 2021, 12(1): 454. doi: 10.1186/s13287-021-02529-w
    [10]
    Yang W, Zhang J, Xu B, et al. HucMSC-derived exosomes mitigate the age-related retardation of fertility in female mice[J]. Mol Ther, 2020, 28(4): 1200–1213. doi: 10.1016/j.ymthe.2020.02.003
    [11]
    He C, Zheng S, Luo Y, Wang B, et al. Exosome theranostics: biology and translational medicine[J]. Theranostics, 2018, 8(1): 237–255. doi: 10.7150/thno.21945
    [12]
    Flaws JA, Abbud R, Mann RJ, et al. Chronically elevated luteinizing hormone depletes primordial follicles in the mouse ovary[J]. Biol Reprod, 1997, 57(5): 1233–1237. doi: 10.1095/biolreprod57.5.1233
    [13]
    Lopes, F., et al. Single and combined effects of cisplatin and doxorubicin on the human and mouse ovary in vitro[J]. Reproduction, 2020, 159(2): p. 193–204. doi: 10.1530/REP-19-0279
    [14]
    Digby JLM, Vanichapol T, Przepiorski A, et al. Evaluation of cisplatin-induced injury in human kidney organoids[J]. Am J Physiol Renal Physiol, 2020, 318(4): F971–F978. doi: 10.1152/ajprenal.00597.2019
    [15]
    Freedman BS, Brooks CR, Lam AQ, et al. Modelling kidney disease with CRISPR-mutant kidney organoids derived from human pluripotent epiblast spheroids[J]. Nat Commun, 2015, 6: 8715. doi: 10.1038/ncomms9715
    [16]
    Edlich F. BCL-2 proteins and apoptosis: Recent insights and unknowns[J]. Biochem Biophys Res Commun, 2018, 500(1): 26–34. doi: 10.1016/j.bbrc.2017.06.190
    [17]
    Domingo IK, Latif A, Bhavsar AP. Pro-inflammatory signalling PRRopels cisplatin-induced toxicity[J]. Int J Mol Sci, 2022, 23(13): 7227. doi: 10.3390/ijms23137227
    [18]
    Morita Y, Perez GI, Paris F, et al. Oocyte apoptosis is suppressed by disruption of the acid sphingomyelinase gene or by sphingosine-1-phosphate therapy[J]. Nat Med, 2000, 6(10): 1109–1114. doi: 10.1038/80442
    [19]
    Kerr JB, Hutt KJ, Cook M, et al. Cisplatin-induced primordial follicle oocyte killing and loss of fertility are not prevented by imatinib[J]. Nat Med, 2012, 18(8): 1109–1174. doi: 10.1038/nm.2889
    [20]
    Carmely A, Meirow D, Peretz A, et al. Protective effect of the immunomodulator AS101 against cyclophosphamide-induced testicular damage in mice[J]. Hum Reprod, 2009, 24(6): 1322–1329. doi: 10.1093/humrep/den481
    [21]
    Maman E, Prokopis K, Levron J, et al. Does controlled ovarian stimulation prior to chemotherapy increase primordial follicle loss and diminish ovarian reserve? An animal study[J]. Hum Reprod, 2009, 24(1): 206–210. doi: 10.1093/humrep/den337
    [22]
    Nguyen QN, Zerafa N, Liew SH, et al. Loss of PUMA protects the ovarian reserve during DNA-damaging chemotherapy and preserves fertility[J]. Cell Death Dis, 2018, 9(6): 618. doi: 10.1038/s41419-018-0633-7
    [23]
    Bildik G, Akin N, Senbabaoglu F, et al. GnRH agonist leuprolide acetate does not confer any protection against ovarian damage induced by chemotherapy and radiation in vitro[J]. Hum Reprod, 2015, 30(12): 2912–2925. doi: 10.1093/humrep/dev257
    [24]
    Hirata Y, Takahashi M, Yamada Y, et al. trans-Fatty acids promote p53-dependent apoptosis triggered by cisplatin-induced DNA interstrand crosslinks via the Nox-RIP1-ASK1-MAPK pathway[J]. Sci Rep, 2021, 11(1): 10350. doi: 10.1038/s41598-021-89506-8
    [25]
    Yuksel A, Bildik G, Senbabaoglu F, et al. The magnitude of gonadotoxicity of chemotherapy drugs on ovarian follicles and granulosa cells varies depending upon the category of the drugs and the type of granulosa cells[J]. Hum Reprod, 2015, 30(12): 2926–2935. doi: 10.1093/humrep/dev256
    [26]
    Huang SM, Tsai CF, Chen DR, et al. p53 is a key regulator for osthole-triggered cancer pathogenesis[J]. Biomed Res Int, 2014, 2014: 175247. doi: 10.1155/2014/175247
    [27]
    Zhang J, Guan J, Niu X, et al. Exosomes released from human induced pluripotent stem cells-derived MSCs facilitate cutaneous wound healing by promoting collagen synthesis and angiogenesis[J]. J Transl Med, 2015, 13: 49. doi: 10.1186/s12967-015-0417-0
    [28]
    Zhang B, Wang M, Gong AH, et al. HucMSC-exosome mediated-Wnt4 signaling is required for cutaneous wound healing[J]. Stem Cells, 2015, 33(7): 2158–2168. doi: 10.1002/stem.1771
    [29]
    Li T, Xia M, Gao Y, et al. Human umbilical cord mesenchymal stem cells: an overview of their potential in cell-based therapy[J]. Expert Opin Biol Ther, 2015, 15(9): 1293–1306. doi: 10.1517/14712598.2015.1051528
    [30]
    Ling L, Feng X, Wei T, et al. Human amnion-derived mesenchymal stem cell (hAD-MSC) transplantation improves ovarian function in rats with premature ovarian insufficiency (POI) at least partly through a paracrine mechanism[J]. Stem Cell Res Ther, 2019, 10(1): 46. doi: 10.1186/s13287-019-1136-x
    [31]
    Rani S, Ryan AE, Griffin MD, et al. Mesenchymal stem cell-derived extracellular vesicles: toward cell-free therapeutic applications[J]. Mol Ther, 2015, 23(5): 812–823. doi: 10.1038/mt.2015.44
    • Related Articles

  • Related Articles

    [1]Alireza Shirpoor, Farzaneh Hosseini Gharalari, Yousef Rasmi, Elaheh Heshmati. Ginger extract attenuates ethanol-induced pulmonary histological changes and oxidative stress in rats[J]. The Journal of Biomedical Research, 2017, 31(6): 521-527. DOI: 10.7555/JBR.31.20160151
    [2]Yong-Dae Kim, Dong-Hyuk Yim, Sang-Yong Eom, Ji Yeoun Lee, Heon Kim. The effect of sunblock against oxidative stress in farmers: a pilot study[J]. The Journal of Biomedical Research, 2017, 31(4): 344-349. DOI: 10.7555/JBR.31.20160092
    [3]Iyaswamy Ashok, Rathinasamy Sheeladevi, Dapkupar Wankhar. Acute effect of aspartame-induced oxidative stress in Wistar albino rat brain[J]. The Journal of Biomedical Research, 2015, 29(5): 390-396. DOI: 10.7555/JBR.28.20120118
    [4]Tanja Stachon, Jiong Wang, Xufei Song, Achim Langenbucher, Berthold Seitz, No´ra Szentma´ry. Impact of crosslinking/riboflavin-UVA-photodynamic inactivation on viability, apoptosis and activation of human keratocytes in vitro[J]. The Journal of Biomedical Research, 2015, 29(4): 321-325. DOI: 10.7555/JBR.29.20130173
    [5]Lintao Wang, Yanyan Peng, Kaikai Shi, Haixiao Wang, Jianlei Lu, Yanli Li, Changyan Ma. Osthole inhibits proliferation of human breast cancer cells by inducing cell cycle arrest and apoptosis[J]. The Journal of Biomedical Research, 2015, 29(2): 132-138. DOI: 10.7555/JBR.27.20120115
    [6]Pengpeng Jin, Xiaoli Wang, Fei Chang, Yinyang Bai, Yingchun Li, Rong Zhou, Ling Chen. Low dose bisphenol A impairs spermatogenesis by suppressing reproductive hormone production and promoting germ cell apoptosis in adult rats[J]. The Journal of Biomedical Research, 2013, 27(2): 135-144. DOI: 10.7555/JBR.27.20120076
    [7]Xiaozheng Zhong, Xiaoyu Li, Lingling Qian, Yiming Xu, Yan Lu, Jing Zhang, Nan Li, Xudong Zhu, Jingjing Ben, Qing Yang, Qi Chen. Glycine attenuates myocardial ischemia-reperfusion injury by inhibiting myocardial apoptosis in rats[J]. The Journal of Biomedical Research, 2012, 26(5): 346-354. DOI: 10.7555/JBR.26.20110124
    [8]Lingyun Li, Jing Chi, Feng Zhou, Dandan Guo, Fang Wang, Genyan Liu, Chun Zhang, Kun Yao. Human herpesvirus 6A induces apoptosis of HSB-2 cells via a mitochondrion-related caspase pathway[J]. The Journal of Biomedical Research, 2010, 24(6): 444-451. DOI: 10.1016/S1674-8301(10)60059-0
    [9]Ling?Yan, Tiebing?Zhu, Tingting?Sun, Liansheng?Wang, Shiyang?Pan, Zhengxian?Tao, Zhijian?Yang, Kejiang?Cao. Activation?of?calcium-sensing?receptors?is?associated?with?apoptosis?in?a?model?of?simulated?cardiomyocytes?ischemia/reperfusion[J]. The Journal of Biomedical Research, 2010, 24(4): 301-307. DOI: 10.1016/S1674-8301(10)60042-5
    [10]Wei Qin, Xin Chen, Peisheng Liu. Inhibition of TGF-β1 by eNOS gene transfer provides cardiac protection after myocardial infarction[J]. The Journal of Biomedical Research, 2010, 24(2): 145-152.
    • Supplements (1)

  • Other Related Supplements

  • Cited by

    Periodical cited type(53)

    1. Pan S, Yan H, Zhu J, et al. GYY4137, as a slow-releasing H2S donor, ameliorates sodium deoxycholate-induced chronic intestinal barrier injury and gut microbiota dysbiosis. Front Pharmacol, 2024, 15: 1476407. DOI:10.3389/fphar.2024.1476407
    2. Jin YQ, Yuan H, Liu YF, et al. Role of hydrogen sulfide in health and disease. MedComm (2020), 2024, 5(9): e661. DOI:10.1002/mco2.661
    3. Sun X, Wu S, Mao C, et al. Therapeutic Potential of Hydrogen Sulfide in Ischemia and Reperfusion Injury. Biomolecules, 2024, 14(7): 740. DOI:10.3390/biom14070740
    4. Pagliaro P, Weber NC, Femminò S, et al. Gasotransmitters and noble gases in cardioprotection: unraveling molecular pathways for future therapeutic strategies. Basic Res Cardiol, 2024, 119(4): 509-544. DOI:10.1007/s00395-024-01061-1
    5. Dugbartey GJ, Juriasingani S, Richard-Mohamed M, et al. Static Cold Storage with Mitochondria-Targeted Hydrogen Sulfide Donor Improves Renal Graft Function in an Ex Vivo Porcine Model of Controlled Donation-after-Cardiac-Death Kidney Transplantation. Int J Mol Sci, 2023, 24(18): 14017. DOI:10.3390/ijms241814017
    6. Hu Q, Lukesh JC 3rd. H2S Donors with Cytoprotective Effects in Models of MI/R Injury and Chemotherapy-Induced Cardiotoxicity. Antioxidants (Basel), 2023, 12(3): 650. DOI:10.3390/antiox12030650
    7. Farzaei MH, Ramezani-Aliakbari F, Ramezani-Aliakbari M, et al. Regulatory effects of trimetazidine in cardiac ischemia/reperfusion injury. Naunyn Schmiedebergs Arch Pharmacol, 2023, 396(8): 1633-1646. DOI:10.1007/s00210-023-02469-7
    8. Khattak S, Rauf MA, Khan NH, et al. Hydrogen Sulfide Biology and Its Role in Cancer. Molecules, 2022, 27(11): 3389. DOI:10.3390/molecules27113389
    9. Zhou M, Chen JY, Chao ML, et al. S-nitrosylation of c-Jun N-terminal kinase mediates pressure overload-induced cardiac dysfunction and fibrosis. Acta Pharmacol Sin, 2022, 43(3): 602-612. DOI:10.1038/s41401-021-00674-9
    10. Zhang Y, Gong W, Xu M, et al. Necroptosis Inhibition by Hydrogen Sulfide Alleviated Hypoxia-Induced Cardiac Fibroblasts Proliferation via Sirtuin 3. Int J Mol Sci, 2021, 22(21): 11893. DOI:10.3390/ijms222111893
    11. McCook O, Denoix N, Radermacher P, et al. H2S and Oxytocin Systems in Early Life Stress and Cardiovascular Disease. J Clin Med, 2021, 10(16): 3484. DOI:10.3390/jcm10163484
    12. Testai L, Brancaleone V, Flori L, et al. Modulation of EndMT by Hydrogen Sulfide in the Prevention of Cardiovascular Fibrosis. Antioxidants (Basel), 2021, 10(6): 910. DOI:10.3390/antiox10060910
    13. Wang WL, Ge TY, Chen X, et al. Advances in the Protective Mechanism of NO, H2S, and H2 in Myocardial Ischemic Injury. Front Cardiovasc Med, 2020, 7: 588206. DOI:10.3389/fcvm.2020.588206
    14. Denoix N, McCook O, Ecker S, et al. The Interaction of the Endogenous Hydrogen Sulfide and Oxytocin Systems in Fluid Regulation and the Cardiovascular System. Antioxidants (Basel), 2020, 9(8): 748. DOI:10.3390/antiox9080748
    15. Pieretti JC, Junho CVC, Carneiro-Ramos MS, et al. H2S- and NO-releasing gasotransmitter platform: A crosstalk signaling pathway in the treatment of acute kidney injury. Pharmacol Res, 2020, 161: 105121. DOI:10.1016/j.phrs.2020.105121
    16. Chen LJ, Ning JZ, Cheng F, et al. Comparison of Intraperitoneal and Intratesticular GYY4137 Therapy for the Treatment of Testicular Ischemia Reperfusion Injury in Rats. Curr Med Sci, 2020, 40(2): 332-338. DOI:10.1007/s11596-020-2180-6
    17. Yurinskaya MM, Krasnov GS, Kulikova DA, et al. H2S counteracts proinflammatory effects of LPS through modulation of multiple pathways in human cells. Inflamm Res, 2020, 69(5): 481-495. DOI:10.1007/s00011-020-01329-x
    18. Kang SC, Sohn EH, Lee SR. Hydrogen Sulfide as a Potential Alternative for the Treatment of Myocardial Fibrosis. Oxid Med Cell Longev, 2020, 2020: 4105382. DOI:10.1155/2020/4105382
    19. Soo E, Marsh C, Steiner R, et al. Optimizing organs for transplantation; advancements in perfusion and preservation methods. Transplant Rev (Orlando), 2020, 34(1): 100514. DOI:10.1016/j.trre.2019.100514
    20. Zheng Q, Pan L, Ji Y. H 2S protects against diabetes-accelerated atherosclerosis by preventing the activation of NLRP3 inflammasome. J Biomed Res, 2019, 34(2): 94-102. DOI:10.7555/JBR.33.20190071
    21. Newton TD, Pluth MD. Development of a hydrolysis-based small-molecule hydrogen selenide (H2Se) donor. Chem Sci, 2019, 10(46): 10723-10727. DOI:10.1039/c9sc04616j
    22. Luo H, Song S, Chen Y, et al. Inhibitor 1 of Protein Phosphatase 1 Regulates Ca2+/Calmodulin-Dependent Protein Kinase II to Alleviate Oxidative Stress in Hypoxia-Reoxygenation Injury of Cardiomyocytes. Oxid Med Cell Longev, 2019, 2019: 2193019. DOI:10.1155/2019/2193019
    23. Maassen H, Hendriks KDW, Venema LH, et al. Hydrogen sulphide-induced hypometabolism in human-sized porcine kidneys. PLoS One, 2019, 14(11): e0225152. DOI:10.1371/journal.pone.0225152
    24. Chen Z, Tang J, Wang P, et al. GYY4137 Attenuates Sodium Deoxycholate-Induced Intestinal Barrier Injury Both In Vitro and In Vivo. Biomed Res Int, 2019, 2019: 5752323. DOI:10.1155/2019/5752323
    25. Zheng W, Liu C. The cystathionine γ-lyase/hydrogen sulfide pathway mediates the trimetazidine-induced protection of H9c2 cells against hypoxia/reoxygenation-induced apoptosis and oxidative stress. Anatol J Cardiol, 2019, 22(3): 102-111. DOI:10.14744/AnatolJCardiol.2019.83648
    26. Van Dingenen J, Pieters L, Vral A, et al. The H2S-Releasing Naproxen Derivative ATB-346 and the Slow-Release H2S Donor GYY4137 Reduce Intestinal Inflammation and Restore Transit in Postoperative Ileus. Front Pharmacol, 2019, 10: 116. DOI:10.3389/fphar.2019.00116
    27. Wang W, Liu H, Lu Y, et al. Controlled-releasing hydrogen sulfide donor based on dual-modal iron oxide nanoparticles protects myocardial tissue from ischemia-reperfusion injury. Int J Nanomedicine, 2019, 14: 875-888. DOI:10.2147/IJN.S186225
    28. Cao X, Zhang W, Moore PK, et al. Protective Smell of Hydrogen Sulfide and Polysulfide in Cisplatin-Induced Nephrotoxicity. Int J Mol Sci, 2019, 20(2): 313. DOI:10.3390/ijms20020313
    29. Cao X, Ding L, Xie ZZ, et al. A Review of Hydrogen Sulfide Synthesis, Metabolism, and Measurement: Is Modulation of Hydrogen Sulfide a Novel Therapeutic for Cancer?. Antioxid Redox Signal, 2019, 31(1): 1-38. DOI:10.1089/ars.2017.7058
    30. Merz T, Lukaschewski B, Wigger D, et al. Interaction of the hydrogen sulfide system with the oxytocin system in the injured mouse heart. Intensive Care Med Exp, 2018, 6(1): 41. DOI:10.1186/s40635-018-0207-0
    31. Zhang L, Wang Y, Li Y, et al. Hydrogen Sulfide (H2S)-Releasing Compounds: Therapeutic Potential in Cardiovascular Diseases. Front Pharmacol, 2018, 9: 1066. DOI:10.3389/fphar.2018.01066
    32. Zhang Y, Liu X, Zhang L, et al. Metformin Protects against H2O2-Induced Cardiomyocyte Injury by Inhibiting the miR-1a-3p/GRP94 Pathway. Mol Ther Nucleic Acids, 2018, 13: 189-197. DOI:10.1016/j.omtn.2018.09.001
    33. Corsello T, Komaravelli N, Casola A. Role of Hydrogen Sulfide in NRF2- and Sirtuin-Dependent Maintenance of Cellular Redox Balance. Antioxidants (Basel), 2018, 7(10): 129. DOI:10.3390/antiox7100129
    34. Woods JJ, Cao J, Lippert AR, et al. Characterization and Biological Activity of a Hydrogen Sulfide-Releasing Red Light-Activated Ruthenium(II) Complex. J Am Chem Soc, 2018, 140(39): 12383-12387. DOI:10.1021/jacs.8b08695
    35. Zhou X, Tang S, Hu K, et al. DL-Propargylglycine protects against myocardial injury induced by chronic intermittent hypoxia through inhibition of endoplasmic reticulum stress. Sleep Breath, 2018, 22(3): 853-863. DOI:10.1007/s11325-018-1656-0
    36. Zeng C, Jiang W, Zheng R, et al. Cardioprotection of tilianin ameliorates myocardial ischemia-reperfusion injury: Role of the apoptotic signaling pathway. PLoS One, 2018, 13(3): e0193845. DOI:10.1371/journal.pone.0193845
    37. Ning JZ, Li W, Cheng F, et al. The protective effects of GYY4137 on ipsilateral testicular injury in experimentally varicocele-induced rats. Exp Ther Med, 2018, 15(1): 433-439. DOI:10.3892/etm.2017.5417
    38. Meng G, Zhao S, Xie L, et al. Protein S-sulfhydration by hydrogen sulfide in cardiovascular system. Br J Pharmacol, 2018, 175(8): 1146-1156. DOI:10.1111/bph.13825
    39. Peng Q, Wang X, Wu K, et al. Irisin attenuates H2O2-induced apoptosis in cardiomyocytes via microRNA-19b/AKT/mTOR signaling pathway. Int J Clin Exp Pathol, 2017, 10(7): 7707-7717.
    40. Wang M, Tang W, Zhu YZ. An Update on AMPK in Hydrogen Sulfide Pharmacology. Front Pharmacol, 2017, 8: 810. DOI:10.3389/fphar.2017.00810
    41. Szabo C, Papapetropoulos A. International Union of Basic and Clinical Pharmacology. CII: Pharmacological Modulation of H2S Levels: H2S Donors and H2S Biosynthesis Inhibitors. Pharmacol Rev, 2017, 69(4): 497-564. DOI:10.1124/pr.117.014050
    42. Pang Z, Zhao W, Yao Z. Cardioprotective Effects of Nicorandil on Coronary Heart Disease Patients Undergoing Elective Percutaneous Coronary Intervention. Med Sci Monit, 2017, 23: 2924-2930. DOI:10.12659/msm.902324
    43. Sun X, Wang W, Dai J, et al. A Long-Term and Slow-Releasing Hydrogen Sulfide Donor Protects against Myocardial Ischemia/Reperfusion Injury. Sci Rep, 2017, 7(1): 3541. DOI:10.1038/s41598-017-03941-0
    44. Sun Y, Huang Y, Yu W, et al. Sulfhydration-associated phosphodiesterase 5A dimerization mediates vasorelaxant effect of hydrogen sulfide. Oncotarget, 2017, 8(19): 31888-31900. DOI:10.18632/oncotarget.16649
    45. Yuan S, Shen X, Kevil CG. Beyond a Gasotransmitter: Hydrogen Sulfide and Polysulfide in Cardiovascular Health and Immune Response. Antioxid Redox Signal, 2017, 27(10): 634-653. DOI:10.1089/ars.2017.7096
    46. Magierowski M, Magierowska K, Hubalewska-Mazgaj M, et al. Exogenous and Endogenous Hydrogen Sulfide Protects Gastric Mucosa against the Formation and Time-Dependent Development of Ischemia/Reperfusion-Induced Acute Lesions Progressing into Deeper Ulcerations. Molecules, 2017, 22(2): 295. DOI:10.3390/molecules22020295
    47. Bazhanov N, Escaffre O, Freiberg AN, et al. Broad-Range Antiviral Activity of Hydrogen Sulfide Against Highly Pathogenic RNA Viruses. Sci Rep, 2017, 7: 41029. DOI:10.1038/srep41029
    48. Cao X, Bian JS. The Role of Hydrogen Sulfide in Renal System. Front Pharmacol, 2016, 7: 385. DOI:10.3389/fphar.2016.00385
    49. Dugbartey GJ, Peppone LJ, de Graaf IA. An integrative view of cisplatin-induced renal and cardiac toxicities: Molecular mechanisms, current treatment challenges and potential protective measures. Toxicology, 2016, 371: 58-66. DOI:10.1016/j.tox.2016.10.001
    50. Haase T, Börnigen D, Müller C, et al. Systems Medicine as an Emerging Tool for Cardiovascular Genetics. Front Cardiovasc Med, 2016, 3: 27. DOI:10.3389/fcvm.2016.00027
    51. Tian XH, Liu CL, Jiang HL, et al. Cardioprotection provided by Echinatin against ischemia/reperfusion in isolated rat hearts. BMC Cardiovasc Disord, 2016, 16: 119. DOI:10.1186/s12872-016-0294-3
    52. Xu J, Tang Y, Bei Y, et al. miR-19b attenuates H2O2-induced apoptosis in rat H9C2 cardiomyocytes via targeting PTEN. Oncotarget, 2016, 7(10): 10870-8. DOI:10.18632/oncotarget.7678
    53. Singh SB, Lin HC. Hydrogen Sulfide in Physiology and Diseases of the Digestive Tract. Microorganisms, 2015, 3(4): 866-89. DOI:10.3390/microorganisms3040866

    Other cited types(0)

Catalog

    Figures(6)

    Get Citation
    PDF
    XML

    Article Metrics

    Article has an altmetric score of 1
    Article has an altmetric score of 1
    Article views (808) PDF downloads (122) Cited by(53)
    Related

    ©2023 by the Editorial Department of the Journals of Nanjing Medical University. All rights reserved.   苏ICP备05071376号-5

    Supported by: Beijing Renhe Information Technology Co., Ltd. E-mail: info@rhhz.net  Baidu Analytics

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return