Disease modeling and gene therapy of copper storage disease in canine hepatic organoids

Stem Cell Reports

Volumn 5, Issue 5, 2015, Pages 895-907

  Nantasanti, Sathidpak ^a   Spee, Bart ^a   Kruitwagen, Hedwig S ^a   Chen, Chen ^a,b   Geijsen, Niels ^a,b   Oosterhoff, Loes A ^a   Van Wolferen, Monique E ^a   Pelaez, Nicolas ^a   Fieten, Hille ^a   Wubbolts, Richard W ^c   Grinwis, Guy C ^d   Chan, Jefferson ^e   Huch, Meritxell ^b,g,h   Vries, Robert R G ^b   Clevers, Hans ^b   De Bruin, Alain ^d,f   Rothuizen, Jan ^a   Penning, Louis C ^a   Schotanus, Baukje A ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

^d UTRECHT UNIVERSITY   (Netherlands)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^g University of Cambridge   (United Kingdom)

^h UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COMMD1 PROTEIN; COPPER; IWP 2; LENTIVIRUS VECTOR; PEPTIDES AND PROTEINS; PROTEIN INHIBITOR; UNCLASSIFIED DRUG; WNT PROTEIN; NOTCH RECEPTOR; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CANINE HEPATIC ORGANOID; CANINE MODEL; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; COPPER STORAGE DISEASE; CRYOPRESERVATION; DISORDERS OF METAL METABOLISM; ENDOTHELIUM CELL; HEK293 CELL LINE; HEPATIC PROGENITOR CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER; LIVER CELL; LIVER PARENCHYMA; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; STELLATE CELL; STEM CELL CULTURE; STEM CELL EXPANSION; STORAGE DISEASE; VIRAL GENE DELIVERY SYSTEM; WNT SIGNALING PATHWAY; ADULT STEM CELL; AGONISTS; ANIMAL; CELL CULTURE; CYTOLOGY; DISEASE MODEL; DOG; GENE THERAPY; GENETICS; HEPATOLENTICULAR DEGENERATION; METABOLISM; PROCEDURES;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADULT STEM CELLS; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOGS; GENETIC THERAPY; HEPATOCYTES; HEPATOLENTICULAR DEGENERATION; RECEPTORS, NOTCH; WNT PROTEINS;

EID: 84946740896     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2015.09.002     Document Type: Article

References (48)

1. B. Arends, B. Spee, B.A. Schotanus, T. Roskams, T.S. van den Ingh, L.C. Penning, and J. Rothuizen In vitro differentiation of liver progenitor cells derived from healthy dog livers Stem Cells Dev. 18 2009 351 358
2. -/- mice Nat. Biotechnol. 25 2007 903 910
3. A. Banas, T. Teratani, Y. Yamamoto, M. Tokuhara, F. Takeshita, G. Quinn, H. Okochi, and T. Ochiya Adipose tissue-derived mesenchymal stem cells as a source of human hepatocytes Hepatology 46 2007 219 228
4. L. Boulter, O. Govaere, T.G. Bird, S. Radulescu, P. Ramachandran, A. Pellicoro, R.A. Ridgway, S.S. Seo, B. Spee, N. Van Rooijen, and et al. Macrophage-derived Wnt opposes Notch signaling to specify hepatic progenitor cell fate in chronic liver disease Nat. Med. 18 2012 572 579
5. L. Boulter, W.Y. Lu, and S.J. Forbes Differentiation of progenitors in the liver: a matter of local choice J. Clin. Invest. 123 2013 1867 1873
6. V. Cardinale, Y. Wang, G. Carpino, C.B. Cui, M. Gatto, M. Rossi, P.B. Berloco, A. Cantafora, E. Wauthier, M.E. Furth, and et al. Multipotent stem/progenitor cells in human biliary tree give rise to hepatocytes, cholangiocytes, and pancreatic islets Hepatology 54 2011 2159 2172
7. H. Clevers, K.M. Loh, and R. Nusse Stem cell signaling. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control Science 346 2014 1248012
8. J.A. Cotruvo Jr., A.T. Aron, K.M. Ramos-Torres, and C.J. Chang Synthetic fluorescent probes for studying copper in biological systems Chem. Soc. Rev. 44 2015 4400 4414
9. D.M. Dalgetty, C.N. Medine, J.P. Iredale, and D.C. Hay Progress and future challenges in stem cell-derived liver technologies Am. J. Physiol. Gastrointest. Liver Physiol. 297 2009 G241 G248
10. A. Dhawan, J. Puppi, R.D. Hughes, and R.R. Mitry Human hepatocyte transplantation: current experience and future challenges Nat. Rev. Gastroenterol. Hepatol. 7 2010 288 298
11. A.W. Duncan, C. Dorrell, and M. Grompe Stem cells and liver regeneration Gastroenterology 137 2009 466 481
12. R. Español-Suñer, R. Carpentier, N. Van Hul, V. Legry, Y. Achouri, S. Cordi, P. Jacquemin, F. Lemaigre, and I.A. Leclercq Liver progenitor cells yield functional hepatocytes in response to chronic liver injury in mice Gastroenterology 143 2012 1564 1575.e7
13. R.P. Favier, B. Spee, B.A. Schotanus, T.S. van den Ingh, H. Fieten, B. Brinkhof, C.S. Viebahn, L.C. Penning, and J. Rothuizen COMMD1-deficient dogs accumulate copper in hepatocytes and provide a good model for chronic hepatitis and fibrosis PLoS ONE 7 2012 e42158
14. R.P. Favier, B. Spee, H. Fieten, T.S. van den Ingh, B.A. Schotanus, B. Brinkhof, J. Rothuizen, and L.C. Penning Aberrant expression of copper associated genes after copper accumulation in COMMD1-deficient dogs J. Trace Elem. Med. Biol. 29 2015 347 353
15. H. Fieten, L.C. Penning, P.A. Leegwater, and J. Rothuizen New canine models of copper toxicosis: diagnosis, treatment, and genetics Ann. N Y Acad. Sci. 1314 2014 42 48
16. M. Grompe Liver stem cells, where art thou? Cell Stem Cell 15 2014 257 258
17. J. Guo, J. Li, Y. Lu, J. Xin, L. Jiang, W. Wu, H. Cao, and Y. Qiu A novel technique for hepatic progenitor cell isolation from normal adult rat livers ASAIO J. 58 2012 73 78
18. Z. He, and M. Feng Activation, isolation, identification and culture of hepatic stem cells from porcine liver tissues Cell Prolif. 44 2011 558 566
19. M. Huch, C. Dorrell, S.F. Boj, J.H. van Es, V.S. Li, M. van de Wetering, T. Sato, K. Hamer, N. Sasaki, M.J. Finegold, and et al. In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration Nature 494 2013 247 250
20. M. Huch, H. Gehart, R. van Boxtel, K. Hamer, F. Blokzijl, M.M. Verstegen, E. Ellis, M. van Wenum, S.A. Fuchs, J. de Ligt, and et al. Long-term culture of genome-stable bipotent stem cells from adult human liver Cell 160 2015 299 312
21. R.D. Hughes, R.R. Mitry, and A. Dhawan Current status of hepatocyte transplantation Transplantation 93 2012 342 347
22. N. Ichinohe, N. Tanimizu, H. Ooe, Y. Nakamura, T. Mizuguchi, J. Kon, K. Hirata, and T. Mitaka Differentiation capacity of hepatic stem/progenitor cells isolated from D-galactosamine-treated rat livers Hepatology 57 2013 1192 1202
23. K. Kamimura, T. Kanefuji, T. Yokoo, H. Abe, T. Suda, Y. Kobayashi, G. Zhang, Y. Aoyagi, and D. Liu Safety assessment of liver-targeted hydrodynamic gene delivery in dogs PLoS ONE 9 2014 e107203
24. A. Kamiya, and Y. Inagaki Stem and progenitor cell systems in liver development and regeneration Hepatol. Res. 45 2015 29 37
25. H. Koike, and H. Taniguchi Characteristics of hepatic stem/progenitor cells in the fetal and adult liver J. Hepatobiliary Pancreat. Sci. 19 2012 587 593
26. H.S. Kruitwagen, B. Spee, C.S. Viebahn, H.B. Venema, L.C. Penning, G.C. Grinwis, R.P. Favier, T.S. van den Ingh, J. Rothuizen, and B.A. Schotanus The canine hepatic progenitor cell niche: molecular characterisation in health and disease Vet. J. 201 2014 345 352
27. F.P. Lemaigre Mechanisms of liver development: concepts for understanding liver disorders and design of novel therapies Gastroenterology 137 2009 62 79
28. W.Y. Lu, T.G. Bird, L. Boulter, A. Tsuchiya, A.M. Cole, T. Hay, R.V. Guest, D. Wojtacha, T.Y. Man, A. Mackinnon, and et al. Hepatic progenitor cells of biliary origin with liver repopulation capacity Nat. Cell Biol. 17 2015 971 983
29. M. Mata, J.F. Vera, C. Gerken, C.M. Rooney, T. Miller, C. Pfent, L.L. Wang, H.M. Wilson-Robles, and S. Gottschalk Toward immunotherapy with redirected T cells in a large animal model: ex vivo activation, expansion, and genetic modification of canine T cells J. Immunother. 37 2014 407 415
30. W.J. McCarty, O.B. Usta, M. Luitje, S.S. Bale, A. Bhushan, M. Hegde, I. Golberg, R. Jindal, and M.L. Yarmush A novel ultrathin collagen nanolayer assembly for 3-D microtissue engineering: layer-by-layer collagen deposition for long-term stable microfluidic hepatocyte culture Technology (Singap. World Sci.) 2 2014 67 74
31. E.W. Miller, L. Zeng, D.W. Domaille, and C.J. Chang Preparation and use of Coppersensor-1, a synthetic fluorophore for live-cell copper imaging Nat. Protoc. 1 2006 824 827
32. R. Nusse, C. Fuerer, W. Ching, K. Harnish, C. Logan, A. Zeng, D. ten Berge, and Y. Kalani Wnt signaling and stem cell control Cold Spring Harb. Symp. Quant. Biol. 73 2008 59 66
33. N.J. Roberts, L. Zhang, F. Janku, A. Collins, R.Y. Bai, V. Staedtke, A.W. Rusk, D. Tung, M. Miller, J. Roix, and et al. Intratumoral injection of Clostridium novyi-NT spores induces antitumor responses Sci. Transl. Med. 6 2014 249ra111
34. F.P. Russo, and M. Parola Stem cells in liver failure Best Pract. Res. Clin. Gastroenterol. 26 2012 35 45
35. P. Sancho-Bru, M. Najimi, M. Caruso, K. Pauwelyn, T. Cantz, S. Forbes, T. Roskams, M. Ott, U. Gehling, E. Sokal, and et al. Stem and progenitor cells for liver repopulation: can we standardise the process from bench to bedside? Gut 58 2009 594 603
36. I. Scheers, C. Maerckx, D.N. Khuu, S. Marcelle, A. Decottignies, M. Najimi, and E. Sokal Adult-derived human liver progenitor cells in long-term culture maintain appropriate gatekeeper mechanisms against transformation Cell Transplant. 21 2012 2241 2255
37. B.A. Schotanus, T.S. van den Ingh, L.C. Penning, J. Rothuizen, T.A. Roskams, and B. Spee Cross-species immunohistochemical investigation of the activation of the liver progenitor cell niche in different types of liver disease Liver Int. 29 2009 1241 1252
38. B.A. Schotanus, H.S. Kruitwagen, T.S. van den Ingh, M.E. van Wolferen, J. Rothuizen, L.C. Penning, and B. Spee Enhanced Wnt/β-catenin and Notch signalling in the activated canine hepatic progenitor cell niche BMC Vet. Res. 10 2014 309
39. G. Schwank, B.K. Koo, V. Sasselli, J.F. Dekkers, I. Heo, T. Demircan, N. Sasaki, S. Boymans, E. Cuppen, C.K. van der Ent, and et al. Functional repair of CFTR by CRISPR/Cas9 in intestinal stem cell organoids of cystic fibrosis patients Cell Stem Cell 13 2013 653 658
40. K. Si-Tayeb, F.P. Lemaigre, and S.A. Duncan Organogenesis and development of the liver Dev. Cell 18 2010 175 189
41. B. Spee, G. Carpino, B.A. Schotanus, A. Katoonizadeh, S. Vander Borght, E. Gaudio, and T. Roskams Characterisation of the liver progenitor cell niche in liver diseases: potential involvement of Wnt and Notch signalling Gut 59 2010 247 257
42. M.D. Thompson, and S.P. Monga WNT/beta-catenin signaling in liver health and disease Hepatology 45 2007 1298 1305
43. N. Van Hul, N. Lanthier, R. Español Suñer, J. Abarca Quinones, N. van Rooijen, and I. Leclercq Kupffer cells influence parenchymal invasion and phenotypic orientation, but not the proliferation, of liver progenitor cells in a murine model of liver injury Am. J. Pathol. 179 2011 1839 1850
44. T. Vanhaecke, and V. Rogiers Hepatocyte cultures in drug metabolism and toxicological research and testing Methods Mol. Biol. 320 2006 209 227
45. B. Wang, L. Zhao, M. Fish, C.Y. Logan, and R. Nusse Self-renewing diploid Axin2(+) cells fuel homeostatic renewal of the liver Nature 524 2015 180 185
46. K. Willert, J.D. Brown, E. Danenberg, A.W. Duncan, I.L. Weissman, T. Reya, J.R. Yates 3rd, and R. Nusse Wnt proteins are lipid-modified and can act as stem cell growth factors Nature 423 2003 448 452
47. M.I. Yovchev, P.N. Grozdanov, H. Zhou, H. Racherla, C. Guha, and M.D. Dabeva Identification of adult hepatic progenitor cells capable of repopulating injured rat liver Hepatology 47 2008 636 647
48. L. Zeng, E.W. Miller, A. Pralle, E.Y. Isacoff, and C.J. Chang A selective turn-on fluorescent sensor for imaging copper in living cells J. Am. Chem. Soc. 128 2006 10 11