Advances in Research Progress on the Therapeutic Function of Biliverdin

Wenya BAI; Yuan YANG; Siying HUO; Xin YANG; Jianlin SHAO

doi:10.12259/j.issn.2095-610X.S20220601

Volume 43 Issue 6

Jun. 2022

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Wenya BAI, Yuan YANG, Siying HUO, Xin YANG, Jianlin SHAO. Advances in Research Progress on the Therapeutic Function of Biliverdin[J]. Journal of Kunming Medical University, 2022, 43(6): 147-153. doi: 10.12259/j.issn.2095-610X.S20220601

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Wenya BAI, Yuan YANG, Siying HUO, Xin YANG, Jianlin SHAO. Advances in Research Progress on the Therapeutic Function of Biliverdin[J]. Journal of Kunming Medical University, 2022, 43(6): 147-153. doi: 10.12259/j.issn.2095-610X.S20220601

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Advances in Research Progress on the Therapeutic Function of Biliverdin

doi: 10.12259/j.issn.2095-610X.S20220601

Dept. of Anesthesiology，The 1st Affiliated Hospital of Kunming Medical University， Kunming Yunnan 650032，China

Received Date: 2022-03-13
Publish Date: 2022-06-25

Abstract

Abstract

Biliverdin and bilirubin are the products of heme metabolism. Many studies have found that biliverdin can continuously consume oxygen free radicals as well as activate biliverdin reductase, relying on the biliverdin-bilirubin redox recycling system. Biliverdin may play a crucial of antioxidant, anti-inflammatory, suppressing immune response, stabilizing vascular endothelial cells, regulating cell apoptosis and so on. In this review, we discussed the structure and metabolism of biliverdin/bilirubin, and mechanism of biliverdin therapeutic function in different diseases.
- Biliverdin,
- Biliverdin-bilirubin redox recycling system,
- Oxidative stress,
- Immune inflammation,
- Apoptosis

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References(55)

References

[1]	Agnieszka Loboda, Agnieszka Jazwa, Anna Grochot-Przeczek, et al. Heme oxygenase-1 and the vascular bed: From molecular mechanisms to therapeutic opportunities[J]. Antioxid Redox Signal, 2008, 10（10）: 1767-1812.
[2]	Andrew C Bulmer,Joanne T Blanchfifield,Istvan Toth. In vitro permeability and metabolic stability of bile pigments and the effffects of hydrophilic and lipophilic modifification of biliverdin[J]. Bioorg Me Chem,2008,16(7):3616-3625. doi: 10.1016/j.bmc.2008.02.008
[3]	Daniel Hanley. Eggshell-derived Biliverdin as an Antioxidant Defense System for Birds’ Eggs[J]. Bioessays,2020,42(8):e2000133. doi: 10.1002/bies.202000133
[4]	Tao Zhang,Hehe Liu,Jiwen Wang,et al. Evidences in duck (Anas platyrhynchos) by transcriptome data for supporting the biliverdin was mainly synthesized by shell gland[J]. Poult Sci,2019,98(5):2260-2271. doi: 10.3382/ps/pey576
[5]	Ryan G. Shiels, Wenu Hewage, Josif Vidimce, et al. Bulmer. Pharmacokinetics of bilirubin -10- sulfonate and biliverdin in the rat[J]. Eur J Pharm Sci, 2021, 159期号: 105684. Ryan G Shiels,Wenu Hewage,Josif Vidimce,et al. Bulmer. Pharmacokinetics of bilirubin -10- sulfonate and biliverdin in the rat[J]. Eur J Pharm Sci,2021,159:105684.
[6]	Masakazu Sugishim, Kei Wada, Masaki Unno, et al. Bilin metabolizing enzymes: site-specifific reductions catalyzed by two different type of enzymes[J]. Curr Opin Struct Biol, 2019, 59期号: 73-80. Masakazu Sugishim,Kei Wada,Masaki Unno,et al. Bilin metabolizing enzymes:site-specifific reductions catalyzed by two different type of enzymes[J]. Curr Opin Struct Biol,2019,59:73-80.
[7]	Beibei Zhang,Natasha M. Nesbitt,Pedro José Barbosa Pereira,et al. Biochemical characterization of biliverdins IXβ/δ generated by a selective heme oxygenase[J]. Biochem J,2020,477(3):601-614. doi: 10.1042/BCJ20190810
[8]	Ryan G Shiels,Josif Vidimce,Ben Matthews,et al. Unprecedented microbial conversion of biliverdin into bilirubin-10-sulfonate[J]. Sci Rep,2019,9(1):2988. doi: 10.1038/s41598-019-39548-w
[9]	柳军,张陆勇. 胆红素及其类似物的结构与生物活性研究进展[J]. 实用肝脏病杂志,2005,8(5):307-310. doi: 10.3969/j.issn.1672-5069.2005.05.033
[10]	D Nogales,Da Lightner. On the structure of bilirubin in solution. 13C[1H] heteronuclear Overhauser effect NMR analyses in aqueous buffer and organic solvents[J]. J Biol Chem,1995,270(1):73-77. doi: 10.1074/jbc.270.1.73
[11]	何凯. 血清胆红素在慢性心力衰竭的研究进展[J]. 检验医学与临床,2018,15(19):2984-2987. doi: 10.3969/j.issn.1672-9455.2018.19.045
[12]	Haruna Takao, Kei Hirabayashi, Yuki Nishigaya, et al. A substrate-bound structure of cyanobacterial biliverdin reductase identififies stacked substrates as critical for activity[J]. Nat Commun, 2017, 8期号: 14397. Haruna Takao,Kei Hirabayashi,Yuki Nishigaya,et al. A substrate-bound structure of cyanobacterial biliverdin reductase identififies stacked substrates as critical for activity[J]. Nat Commun,2017,8:14397.
[13]	池肇春. 血红素加氧酶和胆绿素还原酶反应化学研究进展[J]. 中西医结合肝病杂志,2021,31(7):582-585.
[14]	Antony F. McDonagh. The biliverdin–bilirubin antioxidant cycle of cellular protection:Missing a wheel?[J]. Free Radic Biol Med,2010,49(5):814-820. doi: 10.1016/j.freeradbiomed.2010.06.001
[15]	Joon Nam,Yonghyun Lee,Yejin Yang,et al. Is it worth expending energy to convert biliverdin into bilirubin?[J]. Free Radic Biol Med,2018,124:232-240. doi: 10.1016/j.freeradbiomed.2018.06.010
[16]	周阳,刘慧,张华,等. 胆绿素还原酶在抗肿瘤治疗中作用的研究进展[J]. 癌症进展,2020,18(8):757-760.
[17]	Sang Jin Kim,Min Jea Shin,Dae Won Kim,et al. Tat-biliverdin reductase a exerts a protective role in oxidative stress-induced hippocampal neuronal cell damage by regulating the apoptosis and MAPK signaling[J]. Int J Mol Sci,2020,21(8):2672. doi: 10.3390/ijms21082672
[18]	Thomas Jansen,Andreas Daiber. Direct antioxidant properties of bilirubin and biliverdin. Is there a role for biliverdin reductase?[J]. Front Pharmacol,2012,3:30.
[19]	Cesare Mancuso,Pina Guido,Marzia Perluigi,et al. Inhibition of lipid peroxidation and protein oxidation by endogenous and exogenous antioxidants in rat brain microsomes in vitro[J]. Neurosci Lett,2012,518(2):101-105. doi: 10.1016/j.neulet.2012.04.062
[20]	刘颖迪,柏冰雪,任静,等. 外源性胆绿素对中波紫外线诱导的HaCaT细胞光损伤的保护作用[J]. 中华皮肤科杂志,2018,51(4):279-284. doi: 10.3760/cma.j.issn.0412-4030.2018.04.008
[21]	Manish Mishra,Joseph Fomusi Ndisang. A critical and comprehensive insight on heme oxygenase and related products including carbon monoxide,bilirubin,biliverdin and ferritin in type-1 and type-2 diabetes[J]. Curr Pharm Des,2014,20(9):1370-1391. doi: 10.2174/13816128113199990559
[22]	王娟,周华成,薄玉龙,等. 胆绿素对脑死亡致大鼠肺损伤的影响[J]. 中华麻醉学杂志,2010,30(5):615-618. doi: 10.3760/cma.j.issn.0254-1416.2010.05.032
[23]	Chirag Vasavda,Ruchita Kotharia,Adarsha P,et al. Bilirubin links heme metabolism to neuroprotection by scavenging superoxide[J]. Cell Chem Biol,2019,26(10):1450-1460. doi: 10.1016/j.chembiol.2019.07.006
[24]	Maria J Monte,Elisa Lozano,Maria A,et al. Protective role of biliverdin against bile acid-induced oxidative stress in liver cells[J]. Free Radic Biol Med,2016,97:466-477. doi: 10.1016/j.freeradbiomed.2016.06.016
[25]	张晓卉,林芳,马良娟. 外源性胆绿素对中波紫外线诱导的角质形成细胞光损伤的保护作用和机制[J]. 中华皮肤科杂志,2020,53(10):807-810.
[26]	Bingxue Bai, Yingdi Liu, Yan You, et al. Intraperitoneally administered biliverdin protects against UVB-induced skin photo-damage in hairless mice[J]. J Photochem PhotobiolB, 2015, 144期号: 35-41. Bingxue Bai,Yingdi Liu,Yan You,et al. Intraperitoneally administered biliverdin protects against UVB-induced skin photo-damage in hairless mice[J]. J Photochem PhotobiolB,2015,144:35-41.
[27]	龚睿,蒋磊,宋宁,等. 胆绿素对脂多糖诱导小鼠RAW264.7巨噬细胞NLRP3炎性体激活的作用[J]. 医学研究杂志,2017,46(10):35-39. doi: 10.11969/j.issn.1673-548X.2017.10.010
[28]	Yiting Zhang,Yan Ding,Tai Lu,et al. Biliverdin reductase-A attenuated GMH induced inflammatory response in the spleen by inhibiting toll-like receptor-4 through eNOS/NO pathway[J]. J Neuroinflammation,2018,15(1):118. doi: 10.1186/s12974-018-1155-z
[29]	Barbara Andria,Adele Bracco,Chiara Attanasio,et al. Biliverdin protects against liver ischemia reperfusion injury in swine[J]. PLoS One,2013,8(7):e69972. doi: 10.1371/journal.pone.0069972
[30]	Wenfang Tian,Ping Weng,Qiong Sheng,et al. Biliverdin protects the isolated rat lungs from ischemia-reperfusion injury via antioxidative,anti-inflammatory and anti-apoptotic effects[J]. Chin Med J (Engl),2017,130(7):859-865. doi: 10.4103/0366-6999.202735
[31]	Junjie Li,Zhiyao Zou,Jia Liu,et al. Biliverdin administration ameliorates cerebral ischemia reperfusion injury in rats and is associated with proinflammatory factor downregulation[J]. Exp Ther Med,2017,14(1):671-679. doi: 10.3892/etm.2017.4549
[32]	罗靖,高娴玲,邵建林,等. 胆绿素改善大鼠脑缺血再灌注损伤的作用机制[J]. 昆明医科大学学报,2020,41(11):1-6.
[33]	Zhiyao Zou,Jia Liu,Cheng Chang,et al. Biliverdin administration regulates the microRNA-mRNA expressional network associated with neuroprotection in cerebral ischemia reperfusion injury in rats[J]. Int J Mol Med,2019,43(3):1356-1372.
[34]	Kavita Bisht,Barbara Wegie,Jens Tampe,et al. Biliverdin modulates the expression of C5aR in response to endotoxin in part via mTOR signaling[J]. Biochem Biophys Res Commun,2014,449(1):94-99. doi: 10.1016/j.bbrc.2014.04.150
[35]	Hellíada Vasconcelos Chaves,Danielle Rocha do Val,Kátia Alves Ribeiro,et al. Heme oxygenase-1/biliverdin/carbon monoxide pathway downregulates hypernociception in rats by a mechanism dependent on cGMP/ATP-sensitive K+ channels[J]. Inflamm Res,2018,67(5):407-422. doi: 10.1007/s00011-018-1133-z
[36]	ShareeA Badseo,NicoleK Campbell,LouiseM Sullivan,et al. Suppression of human alloreactive T cells by linear tetrapyrroles; relevance for transplantation[J]. Transl Res,2016,178:81-94. doi: 10.1016/j.trsl.2016.07.011
[37]	Ferenc Zsila,György Mády. Biliverdin is the endogenous ligand of human serum α1-acid glycoprotein[J]. Biochem Biophys Res Commun,2008,372(3):503-507. doi: 10.1016/j.bbrc.2008.05.090
[38]	Ryan G Shiels,Wenu Hewage,Evan N,et al. Biliverdin and bilirubin sulfonate inhibit monosodium urate induced sterile inflammation in the rat[J]. Eur J Pharm Sci,2020,155:105546. doi: 10.1016/j.ejps.2020.105546
[39]	M Bonelli,A. Savitskaya,CW. Steiner,et al. Heme oxygenase-1 end products carbon monoxide and biliverdin ameliorate murine collagen induced arthritis[J]. Clin Exp Rheumatol,2012,30(1):73-78.
[40]	Melissa P Homsher,Michael T Astor,Michael W Butler. Immune challenges decrease biliverdin concentration in the spleen of northern Bobwhite quail,Colinus virginianus[J]. J Comp Physiol B,2018,188(3):505-515. doi: 10.1007/s00360-018-1146-5
[41]	Jessica L Baylor,Michael W Butler. Immune challenge-induced oxidative damage may be mitigated by biliverdin[J]. J Exp Biol,2019,222(Pt 6):jeb200055.
[42]	魏刚. 血红素氧合酶-1抗动脉粥样硬化作用与机制的研究进展[J]. 心血管病学进展,2018,39(1):79-83.
[43]	Atsunori Nakao,Noriko Murase,Chien Ho,et al. Biliverdin administration prevents the formation of intimal hyperplasia induced by vascular injury[J]. Circulation,2005,112(4):587-591. doi: 10.1161/CIRCULATIONAHA.104.509778
[44]	Thomas Jansen,Marcus Hortmann,Matthias Oelze,et al. Conversion of biliverdin to bilirubin by biliverdin reductase contributes to endothelial cell protection by heme oxygenase-1 evidence for direct and indirect antioxidant actions of bilirubin[J]. J Mol Cell Cardiol,2010,49(2):186-195. doi: 10.1016/j.yjmcc.2010.04.011
[45]	J. A. Moraes,P. Barcellos-de-Souza,G. Rodrigues,et al. Heme modulates smooth muscle cell proliferation and migration via NADPH oxidase:A counter-regulatory role for heme oxygenase system[J]. Atherosclerosis,2012,224(2):394-400. doi: 10.1016/j.atherosclerosis.2012.07.043
[46]	J Zheng,Da Nagda,Sa Lajud,et al. Biliverdin’s regulation of reactive oxygen species signalling leads to potent inhibition of proliferative and angiogenic pathways in head and neck cancer[J]. Br J Cancer,2014,110(8):2116-2122. doi: 10.1038/bjc.2014.98
[47]	David Stucki,Julia Steinhausen,Philipp Westhof,et al. Endogenous Carbon Monoxide Signaling Modulates Mitochondrial Function and Intracellular Glucose Utilization:Impact of the Heme Oxygenase Substrate Hemin[J]. Antioxidants (Basel),2020,9(8):652. doi: 10.3390/antiox9080652
[48]	Qian Lv,Ying Yao,Wei Wang,et al. Biliverdin protects against cisplatin-induced apoptosis of renal tubular epithelial cells[J]. Huazhong Univ Sci Technolog Med Sci,2016,36(1):48-52. doi: 10.1007/s11596-016-1540-8
[49]	孙洁芸,张鹏,杨欣颖,等. 胆绿素通过抗凋亡发挥对离体肺缺血/再灌注损伤的保护作用[J]. 中华危重病急救医学,2017,29(1):25-29.
[50]	Junjie Li,Lijia Peng,Wenya Bai,et al. Biliverdin protects against cerebral ischemia/reperfusion injury by regulating the miR-27a-3p/Rgs1 axis[J]. Neuropsychiatr Dis Treat,2021,22(17):1165-1181.
[51]	Aleš Berlec,Borut Štrukelj. A high-throughput biliverdin assay using infrared fluorescence[J]. J Vet Diagn Invest,2014,26(4):521-526. doi: 10.1177/1040638714535403
[52]	Mitja Martelanc,Lovro Žiberna,Sabina Passamonti,et al. Application of high-performance liquid chromatography combined with ultra-sensitive thermal lens spectrometric detection for simultaneous biliverdin and bilirubin assessment at trace levels in human serum[J]. Talanta,2016,154:92-98. doi: 10.1016/j.talanta.2016.03.053
[53]	Milena S. Dimitrijević,Jelena Bogdanović Pristov,Milan Žižić,et al. Biliverdin-copper complex at physiological pH[J]. Dalton Trans,2019,8(18):6061-6070.
[54]	Ruirui Xing,Qianli Zou,Chengqian Yuan,et al. Self-assembling endogenous biliverdin as a versatile near-infrared photothermal nanoagent for cancer theranostics[J]. Adv Mater,2019,31(16):e1900822. doi: 10.1002/adma.201900822
[55]	Parinaz Fathi,Hailey J Knox,Dinabandhu Sar,et al. Biodegradable biliverdin nanoparticles for efficient photoacoustic imaging[J]. ACS Nano,2019,13(7):7690-7704. doi: 10.1021/acsnano.9b01201

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