Human liver stem cells express UGT1A1 and improve phenotype of immunocompromised Crigler Najjar syndrome type I mice.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
21 01 2020
21 01 2020
Historique:
received:
10
04
2019
accepted:
07
01
2020
entrez:
23
1
2020
pubmed:
23
1
2020
medline:
18
12
2020
Statut:
epublish
Résumé
Crigler Najjar Syndrome type I (CNSI) is a rare recessive disorder caused by mutations in the Ugt1a1 gene. There is no permanent cure except for liver transplantation, and current therapies present several shortcomings. Since stem cell-based therapy offers a promising alternative for the treatment of this disorder, we evaluated the therapeutic potential of human liver stem cells (HLSC) in immune-compromised NOD SCID Gamma (NSG)/Ugt1
Identifiants
pubmed: 31965023
doi: 10.1038/s41598-020-57820-2
pii: 10.1038/s41598-020-57820-2
pmc: PMC6972964
doi:
Substances chimiques
UGT1A1 enzyme
EC 2.4.1.-
Glucuronosyltransferase
EC 2.4.1.17
Bilirubin
RFM9X3LJ49
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Video-Audio Media
Langues
eng
Sous-ensembles de citation
IM
Pagination
887Références
Bosma, P. J. et al. Bilirubin UDP-glucuronosyltransferase 1 is the only relevant bilirubin glucuronidating isoform in man. J. Biol. Chem. 269, 17960–17964 (1994).
pubmed: 8027054
Crigler, J. F. Jr. & Najjar, V. A. Congenital familial nonhemolytic jaundice with kernicterus. Pediatrics 10, 169–180 (1952).
pubmed: 12983120
Huang, P. W., Rozdilsky, B., Gerrard, J. W., Goluboff, N. & Holman, G. H. Crigler-Najjar syndrome in four of five siblings with postmortem findings in one. Arch Pathol 90, 536–539 passim (1970).
Fagiuoli, S., Daina, E., D’Antiga, L., Colledan, M. & Remuzzi, G. Monogenic diseases that can be cured by liver transplantation. J. Hepatol. 59, 595–612, https://doi.org/10.1016/j.jhep.2013.04.004 (2013).
doi: 10.1016/j.jhep.2013.04.004
pubmed: 23578885
Moini, M., Mistry, P. & Schilsky, M. L. Liver transplantation for inherited metabolic disorders of the liver. Curr. Opin. Organ. Transpl. 15, 269–276, https://doi.org/10.1097/MOT.0b013e3283399dbd (2010).
doi: 10.1097/MOT.0b013e3283399dbd
Tolosa, L. et al. Human neonatal hepatocyte transplantation induces long-term rescue of unconjugated hyperbilirubinemia in the Gunn rat. Liver Transpl. 21, 801–811, https://doi.org/10.1002/lt.24121 (2015).
doi: 10.1002/lt.24121
pubmed: 25821167
Maerckx, C. et al. Human liver stem/progenitor cells decrease serum bilirubin in hyperbilirubinemic Gunn rat. World J. Gastroenterol. 20, 10553–10563, https://doi.org/10.3748/wjg.v20.i30.10553 (2014).
doi: 10.3748/wjg.v20.i30.10553
pubmed: 25132775
pmcid: 4130866
Chen, Y. et al. Amelioration of Hyperbilirubinemia in Gunn Rats after Transplantation of Human Induced Pluripotent Stem Cell-Derived Hepatocytes. Stem Cell Rep. 5, 22–30, https://doi.org/10.1016/j.stemcr.2015.04.017 (2015).
doi: 10.1016/j.stemcr.2015.04.017
Spitzhorn, L. S. et al. Transplanted Human Pluripotent Stem Cell-Derived Mesenchymal Stem Cells Support Liver Regeneration in Gunn Rats. Stem Cells Dev, https://doi.org/10.1089/scd.2018.0010 (2018).
doi: 10.1089/scd.2018.0010
Fox, I. J. et al. Treatment of the Crigler-Najjar syndrome type I with hepatocyte transplantation. N. Engl. J. Med. 338, 1422–1426, https://doi.org/10.1056/NEJM199805143382004 (1998).
doi: 10.1056/NEJM199805143382004
pubmed: 9580649
Khan, A. A. et al. Treatment of Crigler-Najjar Syndrome type 1 by hepatic progenitor cell transplantation: a simple procedure for management of hyperbilirubinemia. Transpl. Proc. 40, 1148–1150, https://doi.org/10.1016/j.transproceed.2008.03.022 (2008).
doi: 10.1016/j.transproceed.2008.03.022
Herrera, M. B. et al. Isolation and characterization of a stem cell population from adult human liver. Stem Cells 24, 2840–2850, doi:2006-0114 (2006).
Herrera, M. B. et al. Human liver stem cells improve liver injury in a model of fulminant liver failure. Hepatology 57, 311–319, https://doi.org/10.1002/hep.25986 (2013).
doi: 10.1002/hep.25986
pubmed: 22829291
Navarro-Tableros, V. et al. Recellularization of rat liver scaffolds by human liver stem cells. Tissue Eng. Part. A 21, 1929–1939, https://doi.org/10.1089/ten.TEA.2014.0573 (2015).
doi: 10.1089/ten.TEA.2014.0573
pubmed: 25794768
pmcid: 4449720
Bhate, A. et al. ESRP2 controls an adult splicing programme in hepatocytes to support postnatal liver maturation. Nat. Commun. 6, 8768, https://doi.org/10.1038/ncomms9768 (2015).
doi: 10.1038/ncomms9768
pubmed: 26531099
pmcid: 4635967
Donato, M. T., Montero, S., Castell, J. V., Gomez-Lechon, M. J. & Lahoz, A. Validated assay for studying activity profiles of human liver UGTs after drug exposure: inhibition and induction studies. Anal. Bioanal. Chem. 396, 2251–2263, https://doi.org/10.1007/s00216-009-3441-1 (2010).
doi: 10.1007/s00216-009-3441-1
pubmed: 20145913
Fagoonee, S., Famulari, E. S., Silengo, L., Tolosano, E. & Altruda, F. Long Term Liver Engraftment of Functional Hepatocytes Obtained from Germline Cell-Derived Pluripotent Stem Cells. PLoS One 10, e0136762, https://doi.org/10.1371/journal.pone.0136762PONE-D-15-17850 (2015).
doi: 10.1371/journal.pone.0136762PONE-D-15-17850
pubmed: 26323094
pmcid: 4556379
Boelig, M. M. et al. The Intravenous Route of Injection Optimizes Engraftment and Survival in the Murine Model of In Utero Hematopoietic Cell Transplantation. Biol. Blood Marrow Transpl. 22, 991–999, https://doi.org/10.1016/j.bbmt.2016.01.017 (2016).
doi: 10.1016/j.bbmt.2016.01.017
Dal Ben, M., Bottin, C., Zanconati, F., Tiribelli, C. & Gazzin, S. Evaluation of region selective bilirubin-induced brain damage as a basis for a pharmacological treatment. Sci. Rep. 7, 41032, https://doi.org/10.1038/srep41032 (2017).
doi: 10.1038/srep41032
pubmed: 5244479
pmcid: 5244479
Spitalieri, P., Talarico, V. R., Murdocca, M., Novelli, G. & Sangiuolo, F. Human induced pluripotent stem cells for monogenic disease modelling and therapy. World J. Stem Cell 8, 118–135, https://doi.org/10.4252/wjsc.v8.i4.118 (2016).
doi: 10.4252/wjsc.v8.i4.118
Navarro, V., Herrine, S., Katopes, C., Colombe, B. & Spain, C. V. The effect of HLA class I (A and B) and class II (DR) compatibility on liver transplantation outcomes: an analysis of the OPTN database. Liver Transpl. 12, 652–658, https://doi.org/10.1002/lt.20680 (2006).
doi: 10.1002/lt.20680
pubmed: 16555339
Shultz, L. D. et al. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J. Immunol. 174, 6477-6489, doi:174/10/6477[pii] (2005).
Brezillon, N., Kremsdorf, D. & Weiss, M. C. Cell therapy for the diseased liver: from stem cell biology to novel models for hepatotropic human pathogens. Dis. Model. Mech. 1, 113–130, https://doi.org/10.1242/dmm.000463 (2008).
doi: 10.1242/dmm.000463
pubmed: 19048074
pmcid: 2562180
Sokal, E. M. Treating inborn errors of liver metabolism with stem cells: current clinical development. J. Inherit. Metab. Dis. 37, 535–539, https://doi.org/10.1007/s10545-014-9691-x (2014).
doi: 10.1007/s10545-014-9691-x
pubmed: 24668464
pmcid: 4088990
Ribes-Koninckx, C. et al. Clinical outcome of hepatocyte transplantation in four pediatric patients with inherited metabolic diseases. Cell Transpl. 21, 2267–2282, https://doi.org/10.3727/096368912X637505 (2012).
doi: 10.3727/096368912X637505
Lysy, P. A. et al. Liver cell transplantation for Crigler-Najjar syndrome type I: update and perspectives. World J. Gastroenterol. 14, 3464–3470 (2008).
doi: 10.3748/wjg.14.3464
Garcia, J. H., Lassen, N. A., Weiller, C., Sperling, B. & Nakagawara, J. Ischemic stroke and incomplete infarction. Stroke 27, 761–765 (1996).
doi: 10.1161/01.STR.27.4.761
Bortolussi, G. et al. Age-dependent pattern of cerebellar susceptibility to bilirubin neurotoxicity in vivo in mice. Dis. Model. Mech. 7, 1057–1068, https://doi.org/10.1242/dmm.016535 (2014).
doi: 10.1242/dmm.016535
pubmed: 4142726
pmcid: 4142726
Watchko, J. F. & Tiribelli, C. Bilirubin-induced neurologic damage–mechanisms and management approaches. N. Engl. J. Med. 369, 2021–2030, https://doi.org/10.1056/NEJMra1308124 (2013).
doi: 10.1056/NEJMra1308124
Bortolussi, G. et al. Life-long correction of hyperbilirubinemia with a neonatal liver-specific AAV-mediated gene transfer in a lethal mouse model of Crigler-Najjar Syndrome. Hum. Gene Ther. 25, 844–855, https://doi.org/10.1089/hum.2013.233 (2014).
doi: 10.1089/hum.2013.233
pubmed: 4175423
pmcid: 4175423
Ronzitti, G. et al. A translationally optimized AAV-UGT1A1 vector drives safe and long-lasting correction of Crigler-Najjar syndrome. Mol. Ther. Methods Clin. Dev. 3, 16049, https://doi.org/10.1038/mtm.2016.49 (2016).
doi: 10.1038/mtm.2016.49
pubmed: 5052023
pmcid: 5052023
Bockor, L. et al. Repeated AAV-mediated gene transfer by serotype switching enables long-lasting therapeutic levels of hUgt1a1 enzyme in a mouse model of Crigler-Najjar Syndrome Type I. Gene Ther, https://doi.org/10.1038/gt.2017.75 (2017).
doi: 10.1038/gt.2017.75
Fagoonee, S., Famulari, E. S., Silengo, L., Camussi, G. & Altruda, F. Prospects for Adult Stem Cells in the Treatment of Liver Diseases. Stem Cells Dev, https://doi.org/10.1089/scd.2016.0144 (2016).
doi: 10.1089/scd.2016.0144
Smets, F. et al. Phase I/II Trial of Liver-derived Mesenchymal Stem Cells in Pediatric Liver-based Metabolic Disorders: A Prospective, Open Label, Multicenter, Partially Randomized, Safety Study of One Cycle of Heterologous Human Adult Liver-derived Progenitor Cells (HepaStem) in Urea Cycle Disorders and Crigler-Najjar Syndrome Patients. Transplant. 103, 1903–1915, https://doi.org/10.1097/TP.0000000000002605 (2019).
doi: 10.1097/TP.0000000000002605
Herrera Sanchez, M. B. et al. Human liver stem cells and derived extracellular vesicles improve recovery in a murine model of acute kidney injury. Stem Cell Res. Ther. 5, 124, https://doi.org/10.1186/scrt514 (2014).
doi: 10.1186/scrt514
pubmed: 25384729
Fagoonee, S. et al. The RNA-binding protein ESRP1 promotes human colorectal cancer progression. Oncotarget 8, 10007–10024, https://doi.org/10.18632/oncotarget.14318 (2017).
doi: 10.18632/oncotarget.14318
pubmed: 28052020
Bortolussi, G. et al. Rescue of bilirubin-induced neonatal lethality in a mouse model of Crigler-Najjar syndrome type I by AAV9-mediated gene transfer. Faseb J. 26, 1052–1063, https://doi.org/10.1096/fj.11-195461 (2012).
doi: 10.1096/fj.11-195461
pubmed: 22094718
pmcid: 3370676
In Guide for the Care and Use of Laboratory Animals The National Academies Collection: Reports funded by National Institutes of Health (2011).
Chen, S. et al. Tissue-specific, inducible, and hormonal control of the human UDP-glucuronosyltransferase-1 (UGT1) locus. J. Biol. Chem. 280, 37547–37557, https://doi.org/10.1074/jbc.M506683200 (2005).
doi: 10.1074/jbc.M506683200
pubmed: 16155002
Porro, F., Bockor, L., De Caneva, A., Bortolussi, G. & Muro, A. F. Generation of Ugt1-deficient murine liver cell lines using TALEN technology. PLoS One 9, e104816, https://doi.org/10.1371/journal.pone.0104816 (2014).
doi: 10.1371/journal.pone.0104816
pubmed: 25118822
pmcid: 4132024