A TMT-based shotgun proteomics uncovers overexpression of thrombospondin 1 as a contributor in pyrrolizidine alkaloid-induced hepatic sinusoidal obstruction syndrome.


Journal

Archives of toxicology
ISSN: 1432-0738
Titre abrégé: Arch Toxicol
Pays: Germany
ID NLM: 0417615

Informations de publication

Date de publication:
07 2022
Historique:
received: 07 10 2021
accepted: 14 03 2022
pubmed: 1 4 2022
medline: 3 6 2022
entrez: 31 3 2022
Statut: ppublish

Résumé

Hepatic sinusoidal obstruction disease (HSOS) is a rare but life-threatening vascular liver disease. However, its underlying mechanism and molecular changes in HSOS are largely unknown, thus greatly hindering the development of its effective treatment. Hepatic sinusoidal endothelial cells (HSECs) are the primary and essential target for HSOS. A tandem mass tag-based shotgun proteomics study was performed using primary cultured HSECs from mice with HSOS induced by senecionine, a representative toxic pyrrolizidine alkaloid (PA). Dynamic changes in proteome were found at the initial period of damage and the essential role of thrombospondin 1 (TSP1) was highlighted in PA-induced HSOS. TSP1 over-expression was further confirmed in human HSECs and liver samples from patients with PA-induced HSOS. LSKL peptide, a known TSP1 inhibitor, protected mice from senecionine-induced HSOS. In addition, TSP1 was found to be covalently modified by dehydropyrrolizidine alkaloids in human HSECs and mouse livers upon senecionine treatment, thus to form the pyrrole-protein adduct. These findings provide useful information on early changes in HSECs upon PA treatment and uncover TSP1 overexpression as a contributor in PA-induced HSOS.

Identifiants

pubmed: 35357534
doi: 10.1007/s00204-022-03281-7
pii: 10.1007/s00204-022-03281-7
pmc: PMC9151551
doi:

Substances chimiques

Basic Helix-Loop-Helix Leucine Zipper Transcription Factors 0
Pyrrolizidine Alkaloids 0
SPZ1 protein, human 0
Thrombospondin 1 0
Thbs1 protein, mouse 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2003-2019

Subventions

Organisme : National Nature Science Foundation of China
ID : 81603384
Organisme : Shanghai Nature Science Foundation
ID : 20ZR1473300
Organisme : Shanghai Talents Development Foundation
ID : 2020099
Organisme : Xinglin Scholar Program
ID : B1-GY21-409-04-06

Informations de copyright

© 2022. The Author(s).

Références

Bein K, Simons M (2000) Thrombospondin type 1 repeats interact with matrix metalloproteinase 2. Regulation of metalloproteinase activity. J Biol Chem. 275(41):32167–73
pubmed: 10900205 doi: 10.1074/jbc.M003834200
Breitkopf K, Sawitza I, Westhoff JH, Wickert L, Dooley S, Gressner AM (2005) Thrombospondin 1 acts as a strong promoter of transforming growth factor beta effects via two distinct mechanisms in hepatic stellate cells. Gut 54:673–681
pubmed: 15831915 pmcid: 1774498 doi: 10.1136/gut.2004.042911
Cao L, Chang H, Shi X, Peng C, He Y (2016) Keratin mediates the recognition of apoptotic and necrotic cells through dendritic cell receptor DEC205/CD205. Proc Natl Acad Sci U S A 113:13438–13443
pubmed: 27821726 pmcid: 5127327 doi: 10.1073/pnas.1609331113
Chen MY, Cai JT, Du Q (2007) Hepatic veno–occlusive disease associated with the use of Gynura segetum. Eur J Intern Med 18:609
pubmed: 18054719 doi: 10.1016/j.ejim.2007.03.006
DeLeve LD, McCuskey RS, Wang X, Hu L, McCuskey MK, Epstein RB, Kanel GC (1999) Characterization of a reproducible rat model of hepatic veno-occlusive disease. Hepatology 29(6):1779–1791
pubmed: 10347121 doi: 10.1002/hep.510290615
DeLeve LD, Wang X, Hu L, McCuskey MK, McCuskey RS (2004) Rat liver sinusoidal endothelial cell phenotype is maintained by paracrine and autocrine regulation. Am J Physiol Gastrointest Liver Physiol 287(4):G757–G763
pubmed: 15191879 doi: 10.1152/ajpgi.00017.2004
Deleve LD, Wang X, Tsai J, Kanel G, Strasberg S, Tokes ZA (2003) Sinusoidal obstruction syndrome (veno-occlusive disease) in the rat is prevented by matrix metalloproteinase inhibition. Gastroenterology 125(3):882–890
pubmed: 12949732 doi: 10.1016/S0016-5085(03)01056-4
EFSA Panel on Contaminants in the Food Chain (CONTAM), Knutsen HK, Alexander J, Barregård L, Bignami M, Brüschweiler B et al (2017) EFSA J. 15:e04908
Fu PP, Xia QS, Lin G, Chou MW (2004) Pyrrolizidine alkaloids-genotoxicity, metabolism Fu enzymes, metabolic activation, and mechanisms. Drug Metab Rev 36:1–55
pubmed: 15072438 doi: 10.1081/DMR-120028426
Helmy A (2006) Updates in the pathogenesis and therapy of hepatic sinusoidal obstruction syndrome. Aliment Pharm Ther 23:11–25
doi: 10.1111/j.1365-2036.2006.02742.x
Hessel-Pras S, Braeuning A, Guenther G, Adawy A, Enge AM, Ebmeyer J, Henderson CJ, Hengstler JG, Lampen A, Reif R (2020) The pyrrolizidine alkaloid senecionine induces CYP-dependent destruction of sinusoidal endothelial cells and cholestasis in mice. Arch Toxicol 94(1):219–229
pubmed: 31606820 doi: 10.1007/s00204-019-02582-8
Huang ZL, Jing XQ, Sheng YC, Zhang JQ, Hao ZX, Wang ZT, Ji LL (2019) (-)-Epicatechin attenuates hepatic sinusoidal obstruction syndrome by inhibiting liver oxidative and inflammatory injury. Redox Biol. 22:101117
pubmed: 30822691 pmcid: 6395886 doi: 10.1016/j.redox.2019.101117
IPCS. Environmental health criteria 80: Pyrrolizidine alkaloids. Geneva: World Health Organization. 1988.
Jefferson B, Ali M, Grant S, Frampton G, Ploof M, Andry S, DeMorrow S, McMillin M (2020) Thrombospondin-1 exacerbates acute liver failure and hepatic encephalopathy pathology in mice by activating transforming growth factor β1. Am J Pathol 190(2):347–357
pubmed: 31734229 pmcid: 7013272 doi: 10.1016/j.ajpath.2019.10.003
Kondou H, Mushiake S, Etani Y, Miyoshi Y, Michigami T, Ozono K (2003) A blocking peptide for transforming growth factor-beta1 activation prevents hepatic fibrosis in vivo. J Hepatol 39:742–748
pubmed: 14568256 doi: 10.1016/S0168-8278(03)00377-5
Kuroki H, Hayashi H, Nakagawa S, Sakamoto K, Higashi T, Nitta H, Hashimoto D, Chikamoto A, Beppu T, Baba H (2015) Effect of LSKL peptide on thrombospondin 1-mediated transforming growth factor β signal activation and liver regeneration after hepatectomy in an experimental model. Br J Surg 102:813–825
pubmed: 25866938 pmcid: 4654236 doi: 10.1002/bjs.9765
Lamé MW, Jones AD, Wilson DW, Dunston SK, Segall HJ (2000) Protein targets of monocrotaline pyrrole in pulmonary artery endothelial cells. J Biol Chem 275:29091–29099
pubmed: 10875930 doi: 10.1074/jbc.M001372200
Lamé MW, Jones AD, Wilson DW, Segall HJ (2005) Monocrotaline pyrrole targets proteins with and without cysteine residues in the cytosol and membranes of human pulmonary artery endothelial cells. Proteomics 5:4398–4413
pubmed: 16222722 doi: 10.1002/pmic.200402022
Li Y, Turpin CP, Wang S (2017) Role of thrombospondin 1 in liver diseases. Hepatol Res 47(2):186–193
pubmed: 27492250 doi: 10.1111/hepr.12787
Li YH, Tai WC, Khan I, Lu C, Lu Y, Wong WY, Chan WY, Wendy Hsiao WL, Lin G (2018) Toxicoproteomic assessment of liver responses to acute pyrrolizidine alkaloid intoxication in rats. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 36:65–83
pubmed: 29667502 doi: 10.1080/10590501.2018.1450186
Lin G, Wang JY, Li N, Li M, Gao H, Ji Y, Zhang F, Wang H, Zhou Y, Ye Y, Xu HX, Zheng J (2011) Hepatic sinusoidal obstruction syndrome associated with consumption of Gynura segetum. J Hepatol 54:666–673
pubmed: 21146894 doi: 10.1016/j.jhep.2010.07.031
Lu Y, Ma J, Song Z, Ye Y, Fu PP, Lin G (2018) The role of formation of pyrrole-ATP synthase subunit beta adduct in pyrrolizidine alkaloid-induced hepatotoxicity. Arch Toxicol 92:3403–3414
pubmed: 30244272 doi: 10.1007/s00204-018-2309-6
Lu Y, Ma J, Lin G (2019) Development of a two-layer transwell co-culture model for the in vitro investigation of pyrrolizidine alkaloid-induced hepatic sinusoidal damage. Food Chem Toxicol 129:391–398
pubmed: 31054999 doi: 10.1016/j.fct.2019.04.057
Lu Y, Wong KY, Tan C, Ma J, Feng B, Lin G (2020) Establishment of a novel CYP3A4-transduced human hepatic sinusoidal endothelial cell model and its application in screening hepatotoxicity of pyrrolizidine alkaloids. J Environ Sci Health C Toxicol Carcinog 38(2):169–185
pubmed: 32469285
Ma J, Xia Q, Fu PP, Lin G (2018) Pyrrole-protein adducts-A biomarker of pyrrolizidine alkaloid-induced hepatotoxicity. J Food Drug Anal 26:965–972
pubmed: 29976414 doi: 10.1016/j.jfda.2018.05.005
Ma J, Chen T, Wu S, Yang C, Bai M, Shu K, Li K, Zhang G, Jin Z, He F, Hermjakob H, Zhu Y (2019) iProX: an integrated proteome resource. Nucleic Acids Res 47:D1211–D1217
pmcid: 6323926 doi: 10.1093/nar/gky869
McAlister GC, Huttlin EL, Haas W, Ting L, Jedrychowski MP, Rogers JC, Kuhn K, Pike I, Grothe RA, Blethrow JD, Gygi SP (2012) Increasing the multiplexing capacity of TMTs using reporter ion isotopologues with isobaric masses. Anal Chem 84:7469–7478
pubmed: 22880955 pmcid: 3715028 doi: 10.1021/ac301572t
Nakamura K, Hatano E, Narita M, Miyagawa-Hayashino A, Koyama Y, Nagata H, Iwaisako K, Taura K, Uemoto S (2012) Sorafenib attenuates monocrotaline-induced sinusoidal obstruction syndrome in rats through suppression of JNK and MMP–9. J Hepatol 57(5):1037–1043
pubmed: 22796153 doi: 10.1016/j.jhep.2012.07.004
Narizhneva NV, Razorenova OV, Podrez EA, Chen J, Chandrasekharan UM, DiCorleto PE, Plow EF, Topol EJ, Byzova TV (2005) Thrombospondin–1 up-regulates expression of cell adhesion molecules and promotes monocyte binding to endothelium. FASEB J 19:1158–1160
pubmed: 15833768 doi: 10.1096/fj.04-3310fje
Pappireddi N, Martin L, Wühr M (2019) A review on quantitative multiplexed proteomics. Chem Biochem 20:1210–1224
Periasamy S, Hsu DZ, Chen SY, Yang SS, Chandrasekaran VR, Liu MY (2011) Therapeutic sesamol attenuates monocrotaline-induced sinusoidal obstruction syndrome in rats by inhibiting matrix metalloproteinase-9. Cell Biochem Biophys 61(2):327–336
pubmed: 21681587 doi: 10.1007/s12013-011-9215-3
Resovi A, Pinessi D, Chiorino G, Taraboletti G (2014) Current understanding of the thrombospondin–1 interactome. Matrix Biol 37:83–91
pubmed: 24476925 doi: 10.1016/j.matbio.2014.01.012
Rogers NM, Ghimire K, Calzada MJ, Isenberg JS (2017) Matricellular protein thrombospondin–1 in pulmonary hypertension: Multiple pathways to disease. Cardiovasc Res 113:858–868
pubmed: 28472457 pmcid: 5852507 doi: 10.1093/cvr/cvx094
Schultz-Cherry S, Lawler J, Murphy-Ullrich JE (1994) The type 1 repeats of thrombospondin 1 activate latent transforming growth factor-beta. J Biol Chem 269:26783–26788
pubmed: 7929414 doi: 10.1016/S0021-9258(18)47087-1
Shetty S, Lalor PF, Adams DH (2018) Liver sinusoidal endothelial cells-gatekeepers of hepatic immunity. Nat Rev Gastroenterol Hepatol 15:555–567
pubmed: 29844586 pmcid: 7096836 doi: 10.1038/s41575-018-0020-y
Thompson A, Schäfer J, Kuhn K, Kienle S, Schwarz J, Schmidt G, Neumann T, Johnstone R, Mohammed AK, Hamon C (2003) Tandem mass tags: A novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal Chem 75:1895–1904
pubmed: 12713048 doi: 10.1021/ac0262560
Venkatraman L, Tucker-Kellogg L (2013) The CD47-binding peptide of thrombospondin-1 induces defenestration of liver sinusoidal endothelial cells. Liver Int 33:1386–1397
pubmed: 23799952 pmcid: 4285809 doi: 10.1111/liv.12231
Wang ZY, Kang H, Ji LL, Yang YQ, Liu TY, Cao ZW, Morahan G, Wang ZT (2012) Proteomic characterization of the possible molecular targets of pyrrolizidine alkaloid isoline-induced hepatotoxicity. Environ Toxicol Pharmacol 34:608–617
pubmed: 22885678 doi: 10.1016/j.etap.2012.06.013
Wiktorowicz JE, Chowdhury IH, Stafford S, Choudhuri S, Dey N, Garg NJ (2019) Integrated functional analysis of the nuclear proteome of classically and alternatively activated macrophages. Mediators Inflamm 2019:3481430
pubmed: 31182931 pmcid: 6515079 doi: 10.1155/2019/3481430
Willmot FC, Robertson GW (1920) Senecio disease, or cirrhosis of the liver due to Senecio poisoning. Lancet 196:848–849
doi: 10.1016/S0140-6736(01)00020-4
Xie G, Wang X, Wang L, Wang L, Atkinson RD, Kanel GC, Gaarde WA, Deleve LD (2012) Role of differentiation of liver sinusoidal endothelial cells in progression and regression of hepatic fibrosis in rats. Gastroenterology 142:918–927
pubmed: 22178212 doi: 10.1053/j.gastro.2011.12.017
Xiong F, Jiang KY, Chen Y, Ju ZC, Yang L, Xiong AZ, Wang ZT (2020) Protein cross-linking in primary cultured mouse hepatocytes by dehydropyrrolizidine alkaloids: Structure–toxicity relationship. Toxicon 186:4–11
pubmed: 32687888 doi: 10.1016/j.toxicon.2020.07.015
Yang M, Ruan J, Fu PP, Lin G (2016) Cytotoxicity of pyrrolizidine alkaloid in human hepatic parenchymal and sinusoidal endothelial cells: Firm evidence for the reactive metabolites mediated pyrrolizidine alkaloid-induced hepatotoxicity. Chem Biol Interact 243:119–126
pubmed: 26365561 doi: 10.1016/j.cbi.2015.09.011
Yang X, Wang H, Ni HM, Xiong A, Wang Z, Sesaki H, Ding WX, Yang L (2017) Inhibition of Drp1 protects against senecionine-induced mitochondria-mediated apoptosis in primary hepatocytes and in mice. Redox Biol 12:264–273
pubmed: 28282614 pmcid: 5344326 doi: 10.1016/j.redox.2017.02.020
Zhang JQ, Sheng YC, Shi L, Zheng ZY, Chen MW, Lu B, Ji LL (2017) Quercetin and baicalein suppress monocrotaline-induced hepatic sinusoidal obstruction syndrome in rats. Eur J Pharmacol 795:160–168
pubmed: 27979702 doi: 10.1016/j.ejphar.2016.12.015
Zhang F, Zhou Y, Yang X, Xiong AZ, Wang ZT, Yang L (2019) Gynura Rhizoma containing pyrrolizidine alkaloids induces the hepatic sinusoidal obstruction syndrome in mice via upregulating fibrosis-related factors. Acta Pharmacol Sin 40:781–789
pubmed: 30367152 doi: 10.1038/s41401-018-0155-y
Zhuge YZ, Liu YL, Xie WF, Zou XP, Xu JM, Wang JY (2019) Chinese Society of Gastroenterology Committee of Hepatobiliary Disease. Expert consensus on the clinical management of pyrrolizidine alkaloid-induced hepatic sinusoidal obstruction syndrome. J Gastroenterol Hepatol. 34:634–42
pubmed: 30669184 doi: 10.1111/jgh.14612

Auteurs

Weiqian Wang (W)

The MOE Key Laboratory for Standardization of Chinese Medicines and the SATCM Key Laboratory for New Resources and Quality Evaluation of Chinese Medicines, Institute of Chinese Materia Medica, Shanghai University of Traditional Chinese Medicine, Shanghai, 201210, China.
Shanghai R and D Center for Standardization of Traditional Chinese Medicines, Shanghai, 201210, China.
Institute of Interdisciplinary Integrative Medicine Research, Shanghai University of Traditional Chinese Medicine, Shanghai, 201210, China.
National Facility for Protein Science in Shanghai, Shanghai Advanced Research Institute, Chinese Academy of Science, Shanghai, 201210, China.

Yan Chen (Y)

The MOE Key Laboratory for Standardization of Chinese Medicines and the SATCM Key Laboratory for New Resources and Quality Evaluation of Chinese Medicines, Institute of Chinese Materia Medica, Shanghai University of Traditional Chinese Medicine, Shanghai, 201210, China.
Shanghai R and D Center for Standardization of Traditional Chinese Medicines, Shanghai, 201210, China.

Yue Yin (Y)

National Facility for Protein Science in Shanghai, Shanghai Advanced Research Institute, Chinese Academy of Science, Shanghai, 201210, China.

Xunjiang Wang (X)

The MOE Key Laboratory for Standardization of Chinese Medicines and the SATCM Key Laboratory for New Resources and Quality Evaluation of Chinese Medicines, Institute of Chinese Materia Medica, Shanghai University of Traditional Chinese Medicine, Shanghai, 201210, China.

Xuanling Ye (X)

The MOE Key Laboratory for Standardization of Chinese Medicines and the SATCM Key Laboratory for New Resources and Quality Evaluation of Chinese Medicines, Institute of Chinese Materia Medica, Shanghai University of Traditional Chinese Medicine, Shanghai, 201210, China.

Kaiyuan Jiang (K)

The MOE Key Laboratory for Standardization of Chinese Medicines and the SATCM Key Laboratory for New Resources and Quality Evaluation of Chinese Medicines, Institute of Chinese Materia Medica, Shanghai University of Traditional Chinese Medicine, Shanghai, 201210, China.

Yi Zhang (Y)

The MOE Key Laboratory for Standardization of Chinese Medicines and the SATCM Key Laboratory for New Resources and Quality Evaluation of Chinese Medicines, Institute of Chinese Materia Medica, Shanghai University of Traditional Chinese Medicine, Shanghai, 201210, China.

Jiwei Zhang (J)

The MOE Key Laboratory for Standardization of Chinese Medicines and the SATCM Key Laboratory for New Resources and Quality Evaluation of Chinese Medicines, Institute of Chinese Materia Medica, Shanghai University of Traditional Chinese Medicine, Shanghai, 201210, China.

Wei Zhang (W)

Department of Gastroenterology, The Drum Tower Hospital of Nanjing, affiliated to Nanjing University Medical School, Nanjing, 210008, Jiangsu, China.

Yuzheng Zhuge (Y)

Department of Gastroenterology, The Drum Tower Hospital of Nanjing, affiliated to Nanjing University Medical School, Nanjing, 210008, Jiangsu, China.

Li Chen (L)

Department of Gastroenterology, School of Medicine, Ruijin Hospital, Shanghai JiaoTong University, Shanghai, 201801, China.

Chao Peng (C)

National Facility for Protein Science in Shanghai, Shanghai Advanced Research Institute, Chinese Academy of Science, Shanghai, 201210, China. pengchao@sari.ac.cn.

Aizhen Xiong (A)

The MOE Key Laboratory for Standardization of Chinese Medicines and the SATCM Key Laboratory for New Resources and Quality Evaluation of Chinese Medicines, Institute of Chinese Materia Medica, Shanghai University of Traditional Chinese Medicine, Shanghai, 201210, China. aizhenxiong@shutcm.edu.cn.
Shanghai R and D Center for Standardization of Traditional Chinese Medicines, Shanghai, 201210, China. aizhenxiong@shutcm.edu.cn.

Li Yang (L)

The MOE Key Laboratory for Standardization of Chinese Medicines and the SATCM Key Laboratory for New Resources and Quality Evaluation of Chinese Medicines, Institute of Chinese Materia Medica, Shanghai University of Traditional Chinese Medicine, Shanghai, 201210, China. yl7@shutcm.edu.cn.
Shanghai R and D Center for Standardization of Traditional Chinese Medicines, Shanghai, 201210, China. yl7@shutcm.edu.cn.
Institute of Interdisciplinary Integrative Medicine Research, Shanghai University of Traditional Chinese Medicine, Shanghai, 201210, China. yl7@shutcm.edu.cn.

Zhengtao Wang (Z)

The MOE Key Laboratory for Standardization of Chinese Medicines and the SATCM Key Laboratory for New Resources and Quality Evaluation of Chinese Medicines, Institute of Chinese Materia Medica, Shanghai University of Traditional Chinese Medicine, Shanghai, 201210, China.
Shanghai R and D Center for Standardization of Traditional Chinese Medicines, Shanghai, 201210, China.

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