Research progress of bile acids tolerance mechanism in lamprey biliary atresia
Received date: 2021-08-11
Revised date: 2021-09-22
Online published: 2021-11-24
Supported by
Supported by the National Natural Science Foundation of China Nos(31772884);Supported by the National Natural Science Foundation of China Nos(32070518);Liaoning Climbing Scholar, the Distinguished Professor of Liaoning No(XLYC2002093);the Program of Science and Technology of Liaoning Province No(2019-MS-218);the Project of the Educational Department of Liaoning Province No(LJ2020012);the Science and Technology Innovation Fund Research Project of Dalian City No(2018J12SN079)
Biliary atresia (BA) is a rare biliary disease in infants and young children, which is characterized by fibrosclerotic bile duct disease, leading to extrahepatic and intrahepatic bile duct obstruction or occlusion. The bile acids cannot be excreted to the intestinal tract, which causes serious damage to the liver parenchyma cells, and eventually leads to life-threatening cirrhosis and chronic liver failure. At present, the pathogenesis of biliary atresia is unknown. The sequential treatment of “first Gexi” and “later transplantation” is nowadays widely adopted in the clinic. Gossi operation (Kasai) can prolong the survival time of autologous liver by the establishment of bile drainage channel. However, it is necessary for patients to perform liver transplantation with the emergence of complications such as portal hypertension and primary cholangitis. Lampreys are the only vertebrates whose bile duct can disappear spontaneously in the process of growth and development. Lampreys have complete biliary system at the larval stage, but in the process of metamorphosis, lampreys show developmental biliary atresia, bile duct and gallbladder gradually degenerate until the whole biliary system is completely lost, and hepatocytes undergo rearrangement and fine structural changes at the same time. It has been found that lampreys can maintain normal plasma bile acid levels when the symptoms of biliary atresia are formed in during metamorphosis, so that liver cirrhosis and hepatic failure do not occur, thereby adapting to and surviving biliary atresia and cholestasis. To explore the application of bile acids tolerance in biliary atresia, we summarize the recent research progress on the mechanism of bile acids tolerance caused by biliary atresia in lampreys, and further provide a reference for the development of diagnosis and treatments of human biliary atresia.
Key words： lampreys; metamorphosis; biliary atresia; cholestasis; tolerance mechanism
Heng Yang, Yue Pang, Qingwei Li . Research progress of bile acids tolerance mechanism in lamprey biliary atresia[J]. Hereditas(Beijing), 2022 , 44(1) : 59 -67 . DOI: 10.16288/j.yczz.21-295
| [1] | Morita SY, Ikeda Y, Tsuji T, Terada T. Molecular mechanisms for protection of hepatocytes against bile salt cytotoxicity. Chem Pharm Bull (Tokyo), 2019, 67(4):333-340. |
| [2] | Nie YF, Hu J, Yan XH. Cross-talk between bile acids and intestinal microbiota in host metabolism and health. J Zhejiang Univ Sci B, 2015, 16(6):436-446. |
| [3] | Thompson MD, Moghe A, Cornuet P, Marino R, Tian JM, Wang PC, Ma XC, Abrams M, Locker J, Monga SP, Nejak-Bowen K. β-Catenin regulation of farnesoid X receptor signaling and bile acid metabolism during murine cholestasis. Hepatology, 2018, 67(3):955-971. |
| [4] | Chen HL, Liu YJ, Chen HL, Wu SH, Ni YH, Ho MC, Lai HS, Hsu WM, Hsu HY, Tseng HC, Jeng YM, Chang MH. Expression of hepatocyte transporters and nuclear receptors in children with early and late-stage biliary atresia. Pediatr Res, 2008, 63(6):667-673. |
| [5] | Wang L, Yang Y, Chen Y, Zhan JH. Early differential diagnosis methods of biliary atresia: a meta-analysis. Pediatr Surg Int, 2018, 34(4):363-380. |
| [6] | Liang J, Liu X, Wu FF, Li QW. Progress of adaptive immunity system of agnathan vertebrates. Hereditas (Beijing), 2009, 31(10):969-976. |
| [6] | 梁佼, 刘欣, 吴芬芳, 李庆伟. 无颌类脊椎动物适应性免疫系统的研究进展. 遗传, 2009, 31(10):969-976. |
| [7] | Zhu YG, Li J, Pang Y, Li QW. Lamprey: an important animal model of evolution and disease research. Hereditas (Beijing), 2020, 42(9):847-857. |
| [7] | 朱医高, 李军, 逄越, 李庆伟. 七鳃鳗:生物进化和疾病研究的重要模式动物. 遗传, 2020, 42(9):847-857. |
| [8] | Sidon EW, Youson JH. Morphological changes in the liver of the sea lamprey, Petromyzon marinus L., during metamorphosis. II. Canalicular degeneration and transformation of the hepatocytes. J Morphol, 1983, 178(3):225-246. |
| [9] | Boomer LA, Bellister SA, Stephenson LL, Hillyard SD, Khoury JD, Youson JH, Gosche JR. Cholangiocyte apoptosis is an early event during induced metamorphosis in the sea lamprey,Petromyzon marinus L. J Pediatr Surg, 2010, 45(1):114-120. |
| [10] | Sidon EW, Youson JH. Morphological changes in the liver of the sea lamprey, Petromyzon marinus L., during metamorphosis: I. Atresia of the bile ducts. J Morphol, 1983, 177(1):109-124. |
| [11] | Nikitina N, Bronner-Fraser M, Sauka-Spengler T. The sea lamprey Petromyzon marinus:a model for evolutionary and developmental biology. Cold Spring Harb Protoc, 2009, 2009(1): pdb.emo113. |
| [12] | Tetlock A, Yost CK, Stavrinides J, Manzon RG. Changes in the gut microbiome of the sea lamprey during metamorphosis. Appl Environ Microbiol, 2012, 78(21):7638-7644. |
| [13] | Suchy FJ. Biliary atresia in sea lampreys. What can it tell us about the disorder in human infants? Hepatology, 2013, 57(6):2114-2116. |
| [14] | Chung-Davidson YW, Yeh CY, Li WM. The sea lamprey as an etiological model for biliary atresia. Biomed Res Int, 2015, 2015:832943. |
| [15] | Davenport M, Gonde C, Redkar R, Koukoulis G, Tredger M, Mieli-Vergani G, Portmann B, Howard ER. Immunohistochemistry of the liver and biliary tree in extrahepatic biliary atresia. J Pediatr Surg, 2001, 36(7):1017-1025. |
| [16] | Johnson NS, Yun SS, Li WM. Investigations of novel unsaturated bile salts of male sea lamprey as potential chemical cues. J Chem Ecol, 2014, 40(10):1152-1160. |
| [17] | Cai SY, Lionarons DA, Hagey L, Soroka CJ, Mennone A, Boyer JL. Adult sea lamprey tolerates biliary atresia by altering bile salt composition and renal excretion. Hepatology, 2013, 57(6):2418-2426. |
| [18] | Yeh CY, Chung-Davidson YW, Wang HY, Li K, Li WM. Intestinal synthesis and secretion of bile salts as an adaptation to developmental biliary atresia in the sea lamprey. Proc Natl Acad Sci USA, 2012, 109(28):11419-11424. |
| [19] | Chung-Davidson YW, Wang HY, Siefkes MJ, Bryan MB, Wu H, Johnson NS, Li WM. Pheromonal bile acid 3-ketopetromyzonol sulfate primes the neuroendocrine system in sea lamprey. BMC Neurosci, 2013, 14:11. |
| [20] | Liu CJ, Huang HF, Ma F, Liu X, Li QW. Evolution of adaptive immune system in guinea-free vertebrates. Hereditas (Beijing), 2008, 30(1):13-19. |
| [20] | 刘岑杰, 黄惠芳, 马飞, 刘欣, 李庆伟. 无颌类脊椎动物适应性免疫系统的进化. 遗传, 2008, 30(1):13-19. |
| [21] | Yun SS, Scott AP, Li W. Pheromones of the male sea lamprey,Petromyzon marinus L.: structural studies on a new compound, 3-keto allocholic acid, and 3-keto petromyzonol sulfate. Steroids, 2003, 68(3):297-304. |
| [22] | Haslewood GA, Tökés L. Comparative studies of bile salts. Bile salts of the lamprey Petromyzon marinus L. Biochem J, 1969, 114(2):179-184. |
| [23] | Li WM, Scott AP, Siefkes MJ, Yan HG, Liu Q, Yun SS, Gage DA. Bile acid secreted by male sea lamprey that acts as a sex pheromone. Science, 2002, 296(5565):138-141. |
| [24] | Hoye TR, Dvornikovs V, Fine JM, Anderson KR, Jeffrey CS, Muddiman DC, Shao F, Sorensen PW, Wang JZ. Details of the structure determination of the sulfated steroids PSDS and PADS: new components of the sea lamprey (Petromyzon marinus) migratory pheromone. J Org Chem, 2007, 72(20):7544-7550. |
| [25] | Li K, Wang HY, Brant CO, Ahn SC, Li WM. Multiplex quantification of lamprey specific bile acid derivatives in environmental water using UHPLC-MS/MS. J Chromatogr B Analyt Technol Biomed Life Sci, 2011, 879(32):3879-8386. |
| [26] | Chiang JY. Regulation of bile acid synthesis: pathways, nuclear receptors, and mechanisms. J Hepatol, 2004, 40(3):539-551. |
| [27] | Midzak A, Papadopoulos V. Binding domain-driven intracellular trafficking of sterols for synthesis of steroid hormones, bile acids and oxysterols. Traffic, 2014, 15(9):895-914. |
| [28] | Björkheim I, Danielsson H, Einarsson K, Johansson G. Formation of bile acids in man: conversion of cholesterol into 5-beta-cholestane-3-alpha,7-alpha,12-alpha-triol in liver homogenates. J Clin Invest, 1968, 47(7):1573-1582. |
| [29] | Shea HC, Head DD, Setchell KDR, Russell DW. Analysis of HSD3B7 knockout mice reveals that a 3alpha-hydroxyl stereochemistry is required for bile acid function. Proc Natl Acad Sci USA, 2007, 104(28):11526-11533. |
| [30] | Venkatachalam KV, Llanos DE, Karami KJ, Malinovskii VA. Isolation, partial purification, and characterization of a novel petromyzonol sulfotransferase from Petromyzon marinus(lamprey) larval liver. J Lipid Res, 2004, 45(3):486-495. |
| [31] | Abu-Hayyeh S, Papacleovoulou G, Williamson C. Nuclear receptors, bile acids and cholesterol homeostasis series-bile acids and pregnancy. Mol Cell Endocrinol, 2013, 368(1-2):120-128. |
| [32] | Liu X, Wang Y. An overview of bile acid synthesis and its physiological and pathological functions. Hereditas (Beijing), 2019, 41(5):365-374. |
| [32] | 刘笑, 王琰. 胆汁酸的合成调控及其在生理与病理中的功能机制. 遗传, 2019, 41(5):365-374. |
| [33] | Li TG, Jahan A, Chiang JYL. Bile acids and cytokines inhibit the human cholesterol 7 alpha-hydroxylase gene via the JNK/c-jun pathway in human liver cells. Hepatology, 2006, 43(6):1202-1210. |
| [34] | Siefkes MJ, Scott AP, Zielinski B, Yun SS, Li WM. Male sea lampreys, Petromyzon marinus L., excrete a sex pheromone from gill epithelia. Biol Reprod, 2003, 69(1):125-132. |
| [35] | Chung-Davidson YW, Bussy U, Fissette SD, Scott AM, Li WM. Bile acid production is life-stage and sex-dependent and affected by primer pheromones in the sea lamprey. J Exp Biol, 2021, 224(9): jeb229476. |
| [36] | Sohail MI, Dönmez-Cakil Y, Szöllősi D, Stockner T, Chiba P. The bile salt export pump: molecular structure, study models and small-molecule drugs for the treatment of inherited BSEP deficiencies. Int J Mol Sci, 2021, 22(2):784. |
| [37] | Tran QH, Nguyen VG, Tran CM, Nguyen MN. Down- regulation of solute carrier family 10 member 1 is associated with early recurrence and poorer prognosis of hepatocellular carcinoma. Heliyon, 2021, 7(3):e06463. |
| [38] | Wang LN, Zhou Y, Wang XH, Zhang GW, Guo B, Hou XM, Ran JT, Zhang QN, Li CC, Zhao XS, Geng YC, Feng SW. Mechanism of Asbt (Slc10a2)-related bile acid malabsorption in diarrhea after pelvic radiation. Int J Radiat Biol, 2020, 96(4):510-519. |
| [39] | Hagey LR, Møller PR, Hofmann AF, Krasowski MD. Diversity of bile salts in fish and amphibians: evolution of a complex biochemical pathway. Physiol Biochem Zool, 2010, 83(2):308-321. |
| [40] | Han SY, Song HK, Cha JJ, Han JY, Kang YS, Cha DR. Farnesoid X receptor (FXR) agonist ameliorates systemic insulin resistance, dysregulation of lipid metabolism, and alterations of various organs in a type 2 diabetic kidney animal model. Acta Diabetol, 2021, 8(4):495-503. |
| [41] | Wang RX, Sheps JA, Ling V. ABC transporters, bile acids, and inflammatory stress in liver cancer. Curr Pharm Biotechnol, 2011, 12(4):636-646. |
| [42] | Slizgi JR, Lu Y, Brouwer KR, St Claire RL, Freeman KM, Pan M, Brock WJ, Brouwer KL. Inhibition of human hepatic bile acid transporters by tolvaptan and metabolites: contributing factors to drug-induced liver injury? Toxicol Sci, 2016, 149(1):237-250. |
| [43] | Sidon EW, Youson JH. Morphological changes in the liver of the sea lamprey, Petromyzon marinus L., during metamorphosis. II. Canalicular degeneration and transformation of the hepatocytes. J Morphol, 1983, 178(3):225-246. |
| [44] | Zhang YC, Hong JY, Rockwell CE, Copple BL, Jaeschke H, Klaassen CD. Effect of bile duct ligation on bile acid composition in mouse serum and liver. Liver Int, 2012, 32(1):58-69. |
| [45] | Makino I, Shinozaki K, Nakagawa S, Mashimo K. Measurement of sulfated and nonsulfated bile acids in human serum and urine. J Lipid Res, 1974, 15(2):132-138. |
| [46] | Makos BK, Youson JH. Tissue levels of bilirubin and biliverdin in the sea lamprey, Petromyzon marinus L., before and after biliary atresia. Comp Biochem Physiol A Comp Physiol, 1988, 91(4):701-710. |
| [47] | Jansen T, Hortmann M, Oelze M, Opitz B, Steven S, Schell R, Knorr M, Karbach S, Schuhmacher S, Wenzel P, Münzel T, Daiber A. 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 Mol Cell Cardiol, 2010, 49(2):186-195. |
| [48] | Sedlak TW, Saleh M, Higginson DS, Paul BD, Juluri KR, Snyder SH. Bilirubin and glutathione have complementary antioxidant and cytoprotective roles. Proc Natl Acad Sci USA, 2009, 106(13):5171-5176. |
| [49] | Bathena SPR, Thakare R, Gautam N, Mukherjee S, Olivera M, Meza J, Alnouti Y. Urinary bile acids as biomarkers for liver diseases II. Signature profiles in patients. Toxicol Sci, 2015, 143(2):308-318. |
| [50] | Faiz Kabir Uddin Ahmed A, Ohtani H, Nio M, Funaki N, Iwami D, Kumagai S, Sato E, Nagura H, Ohi R. In situ expression of fibrogenic growth factors and their receptors in biliary atresia: comparison between early and late stages. J Pathol, 2000, 192(1):73-80. |
| [51] | Youson JH, Langille RM. Proliferation and renewal of the epithelium in the intestine of young adult anadromous sea lampreys, Petromyzon marinusL. Can J Zool, 1981, 59(12):2341-2349. |
| [52] | Kao Y, Manzon RG, Sheridan MA, Youson JH. Study of the relationship between thyroid hormones and lipid metabolism during KClO4-induced metamorphosis of landlocked lamprey, Petromyzon marinus. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol, 1999, 122(3):363-373. |
| [53] | Morii M, Mezaki Y, Yamaguchi N, Yoshikawa K, Miura M, Imai K, Yoshino H, Hebiguchi T, Hebiguchi T, Senoo H. Onset of apoptosis in the cystic duct during metamorphosis of a Japanese lamprey, Lethenteron reissneri. Anat Rec (Hoboken), 2010, 293(7):1155-66. |
| [54] | Chung-Davidson YW, Ren JF, Yeh CY, Bussy U, Huerta B, Davidson PJ, Whyard S, Li WM. TGF-β Signaling plays a pivotal role during developmental biliary atresia in sea lamprey (Petromyzon marinus). Hepatol Commun, 2019, 4(2):219-234. |
| [55] | Chung-Davidson YW, Yeh CY, Bussy U, Li K, Davidson PJ, Nanlohy KG, Brown CT, Whyard S, Li WM. Hsp90 and hepatobiliary transformation during sea lamprey metamorphosis. BMC Dev Biol, 2015, 15:47. |
| [56] | Mohanty SK, Donnelly B, Temple H, Ortiz-Perez A, Mowery S, Lobeck I, Dupree P, Poling HM, McNeal M, Mourya R, Jenkins T, Bansal R, Bezerra J, Tiao G. High mobility group box 1 release by cholangiocytes governs biliary atresia pathogenesis and correlates with increases in afflicted infants. Hepatology, 2021, 74(2):864-878. |
| [57] | Sampaziotis F, Muraro D, Tysoe OC, Sawiak S, Beach TE, Godfrey EM, Upponi SS, Brevini T, Wesley BT, Garcia-Bernardo J, Mahbubani K, Canu G, Gieseck R 3rd, Berntsen NL, Mulcahy VL, Crick K, Fear C, Robinson S, Swift L, Gambardella L, Bargehr J, Ortmann D, Brown SE, Osnato A, Murphy MP, Corbett G, Gelson WTH, Mells GF, Humphreys P, Davies SE, Amin I, Gibbs P, Sinha S, Teichmann SA, Butler AJ, See TC, Melum E, Watson CJE, Saeb-Parsy K, Vallier L. Cholangiocyte organoids can repair bile ducts after transplantation in the human liver. Science, 2021, 371(6531):839-846. |
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