User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Proliferation-Independent Initiation of Biliary Cysts in Polycystic Liver Diseases

Primary tabs

download
  • Open access
  • PDF
  • 4.70 M
Beaudry, Jean-Bernard [UCL] Cordi, Sabine [UCL] Demarez, Céline [UCL] Lepreux, Sébastien [Université de Bordeaux 2] Pierreux, Christophe [UCL] Lemaigre, Frédéric [UCL]

Biliary cysts in adult patients affected by polycystic liver disease are lined by cholangiocytes that proliferate, suggesting that initiation of cyst formation depends on proliferation. Here, we challenge this view by analyzing cyst-lining cell proliferation and differentiation in Cpk mouse embryos and in livers from human fetuses affected by Autosomal Recessive Polycystic Kidney Disease (ARPKD), at early stages of cyst formation. Proliferation of fetal cholangiocyte precursors, measured by immunostaining in human and mouse livers, was low and did not differ between normal and ARPKD or Cpk livers, excluding excessive proliferation as an initiating cause of liver cysts. Instead, our analyses provide evidence that the polycystic livers exhibit increased and accelerated differentiation of hepatoblasts into cholangiocyte precursors, eventually coalescing into large biliary cysts. Lineage tracing experiments, performed in mouse embryos, indicated that the cholangiocyte precursors in Cpk mice generate cholangiocytes and periportal hepatocytes, like in wild-type animals. Therefore, contrary to current belief, cyst formation in polycystic liver disease does not necessarily depend on overproliferation. Combining our prenatal data with available data from adult livers, we propose that polycystic liver can be initiated by proliferation-independent mechanisms at a fetal stage, followed by postnatal proliferation-dependent cyst expansion.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2015
Language Anglais
Journal information "PLoS One" - Vol. 10, no. 6, p. e0132295
Peer reviewed yes
Publisher Public Library of Science
issn 1932-6203
e-issn 1932-6203
Publication status Publié
Affiliation UCL - SSS/DDUV - Institut de Duve
Links
  1. Cnossen W. R., te Morsche R. H. M., Hoischen A., Gilissen C., Chrispijn M., Venselaar H., Mehdi S., Bergmann C., Veltman J. A., Drenth J. P. H., Whole-exome sequencing reveals LRP5 mutations and canonical Wnt signaling associated with hepatic cystogenesis, 10.1073/pnas.1309438111
  2. Wills Edgar S., Roepman Ronald, Drenth Joost P.H., Polycystic liver disease: ductal plate malformation and the primary cilium, 10.1016/j.molmed.2014.01.003
  3. Masyuk Tatyana, LaRusso Nicholas, Polycystic liver disease: New insights into disease pathogenesis, 10.1002/hep.21199
  4. Onori P., Franchitto A., Mancinelli R., Carpino G., Alvaro D., Francis H., Alpini G., Gaudio E., Polycystic liver diseases, 10.1016/j.dld.2010.01.006
  5. Strazzabosco Mario, Fabris Luca, Development of the bile ducts: Essentials for the clinical hepatologist, 10.1016/j.jhep.2011.09.022
  6. Strazzabosco Mario, Somlo Stefan, Polycystic Liver Diseases: Congenital Disorders of Cholangiocyte Signaling, 10.1053/j.gastro.2011.04.030
  7. Tao B., Bu S., Yang Z., Siroky B., Kappes J. C., Kispert A., Guay-Woodford L. M., Cystin Localizes to Primary Cilia via Membrane Microdomains and a Targeting Motif, 10.1681/asn.2009020188
  8. Gallagher Anna-Rachel, Esquivel Ernie L., Briere Tiffany S., Tian Xin, Mitobe Michihiro, Menezes Luis F., Markowitz Glen S., Jain Dhanpat, Onuchic Luiz F., Somlo Stefan, Biliary and Pancreatic Dysgenesis in Mice Harboring a Mutation in Pkhd1, 10.2353/ajpath.2008.070381
  9. Woollard J.R., Punyashtiti R., Richardson S., Masyuk T.V., Whelan S., Huang B.Q., Lager D.J., vanDeursen J., Torres V.E., Gattone V.H., LaRusso N.F., Harris P.C., Ward C.J., A mouse model of autosomal recessive polycystic kidney disease with biliary duct and proximal tubule dilatation, 10.1038/sj.ki.5002294
  10. Johnson C A, Molecular pathology and genetics of congenital hepatorenal fibrocystic syndromes, 10.1136/jmg.40.5.311
  11. Masyuk Anatoliy I., Masyuk Tatyana V., LaRusso Nicholas F., Cholangiocyte primary cilia in liver health and disease, 10.1002/dvdy.21530
  12. Muchatuta Monalisa N., Gattone Vincent H., Witzmann Frank A., Blazer-Yost Bonnie L., Structural and Functional Analyses of Liver Cysts from the BALB/c-cpk Mouse Model of Polycystic Kidney Disease, 10.3181/0807-rm-215
  13. Gradilone Sergio A., Masyuk Tatyana V., Huang Bing Q., Banales Jesus M., Lehmann Guillermo L., Radtke Brynn N., Stroope Angela, Masyuk Anatoliy I., Splinter Patrick L., LaRusso Nicholas F., Activation of Trpv4 Reduces the Hyperproliferative Phenotype of Cystic Cholangiocytes From an Animal Model of ARPKD, 10.1053/j.gastro.2010.04.010
  14. Muff Melissa A, Masyuk Tatyana V, Stroope Angela J, Huang Bing Q, Splinter Patrick L, Lee Seung-Ok, LaRusso Nicholas F, Development and characterization of a cholangiocyte cell line from the PCK rat, an animal model of Autosomal Recessive Polycystic Kidney Disease, 10.1038/labinvest.3700448
  15. Sanzen Takahiro, Harada Kenichi, Yasoshima Mitsue, Kawamura Yasuhito, Ishibashi Masahiko, Nakanuma Yasuni, Polycystic Kidney Rat Is a Novel Animal Model of Caroli’s Disease Associated with Congenital Hepatic Fibrosis, 10.1016/s0002-9440(10)64116-8
  16. Raynaud Peggy, Carpentier Rodolphe, Antoniou Aline, Lemaigre Frédéric P., Biliary differentiation and bile duct morphogenesis in development and disease, 10.1016/j.biocel.2009.07.020
  17. Antoniou Aline, Raynaud Peggy, Cordi Sabine, Zong Yiwei, Tronche François, Stanger Ben Z., Jacquemin Patrick, Pierreux Christophe E., Clotman Frederic, Lemaigre Frederic P., Intrahepatic Bile Ducts Develop According to a New Mode of Tubulogenesis Regulated by the Transcription Factor SOX9, 10.1053/j.gastro.2009.02.051
  18. Carpentier Rodolphe, Suñer Regina Español, van Hul Noémi, Kopp Janel L., Beaudry Jean–Bernard, Cordi Sabine, Antoniou Aline, Raynaud Peggy, Lepreux Sébastien, Jacquemin Patrick, Leclercq Isabelle A., Sander Maike, Lemaigre Frédéric P., Embryonic Ductal Plate Cells Give Rise to Cholangiocytes, Periportal Hepatocytes, and Adult Liver Progenitor Cells, 10.1053/j.gastro.2011.06.049
  19. Hou Xiaoying, Mrug Michal, Yoder Bradley K., Lefkowitz Elliot J., Kremmidiotis Gabriel, D’Eustachio Peter, Beier David R., Guay-Woodford Lisa M., Cystin, a novel cilia-associated protein, is disrupted in the cpk mouse model of polycystic kidney disease, 10.1172/jci0214099
  20. Yoder B. K., The Polycystic Kidney Disease Proteins, Polycystin-1, Polycystin-2, Polaris, and Cystin, Are Co-Localized in Renal Cilia, 10.1097/01.asn.0000029587.47950.25
  21. GM Preminger, J Urol, 127, 556 (1982)
  22. Denamur Erick, Delezoide Anne-Lise, Alberti Corinne, Bourillon Agnès, Gubler Marie-Claire, Bouvier Raymonde, Pascaud Olivier, Elion Jacques, Grandchamp Bernard, Michel-Calemard Laurence, Missy Pascale, Zaccaria Isabelle, Le Nagard Hervé, Gerard Bénédicte, Loirat Chantal, Genotype–phenotype correlations in fetuses and neonates with autosomal recessive polycystic kidney disease, 10.1038/ki.2009.440
  23. Villeneuve Julien, Pelluard-Nehme Fanny, Combe Chantal, Carles Dominique, Chaponnier Christine, Ripoche Jean, Balabaud Charles, Bioulac-Sage Paulette, Lepreux Sébastien, Immunohistochemical study of the phenotypic change of the mesenchymal cells during portal tract maturation in normal and fibrous (ductal plate malformation) fetal liver, 10.1186/1476-5926-8-5
  24. Raynaud Peggy, Tate Joshua, Callens Céline, Cordi Sabine, Vandersmissen Patrick, Carpentier Rodolphe, Sempoux Christine, Devuyst Olivier, Pierreux Christophe E., Courtoy Pierre, Dahan Karin, Delbecque Katty, Lepreux Sébastien, Pontoglio Marco, Guay-Woodford Lisa M., Lemaigre Frédéric P., A classification of ductal plate malformations based on distinct pathogenic mechanisms of biliary dysmorphogenesis, 10.1002/hep.24292
  25. Subramanian A., Tamayo P., Mootha V. K., Mukherjee S., Ebert B. L., Gillette M. A., Paulovich A., Pomeroy S. L., Golub T. R., Lander E. S., Mesirov J. P., Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles, 10.1073/pnas.0506580102
  26. Guay-Woodford L. M., Germline and somatic loss of function of the mouse cpk gene causes biliary ductal pathology that is genetically modulated, 10.1093/hmg/9.5.769
  27. Harris Peter C, Rossetti Sandro, Molecular genetics of autosomal recessive polycystic kidney disease, 10.1016/j.ymgme.2003.10.010
  28. NAGAO Shizuko, KUGITA Masanori, YOSHIHARA Daisuke, YAMAGUCHI Tamio, Animal Models for Human Polycystic Kidney Disease, 10.1538/expanim.61.477
  29. Seth A., Ye J., Yu N., Guez F., Bedford D. C., Neale G. A., Cordi S., Brindle P. K., Lemaigre F. P., Kaestner K. H., Sosa-Pineda B., Prox1 ablation in hepatic progenitors causes defective hepatocyte specification and increases biliary cell commitment, 10.1242/dev.099481
  30. Cheung Isla D., Bagnat Michel, Ma Taylur P., Datta Anirban, Evason Kimberley, Moore John C., Lawson Nathan D., Mostov Keith E., Moens Cecilia B., Stainier Didier Y.R., Regulation of intrahepatic biliary duct morphogenesis by Claudin 15-like b, 10.1016/j.ydbio.2011.10.004
  31. Moser Markus, Matthiesen Sonja, Kirfel Jutta, Schorle Hubert, Bergmann Carsten, Senderek Jan, Rudnik-Schöneborn Sabine, Zerres Klaus, Buettner Reinhard, A mouse model for cystic biliary dysgenesis in autosomal recessive polycystic kidney disease (ARPKD), 10.1002/hep.20655
  32. Masyuk Tatyana V., Masyuk Anatoliy I., Torres Vicente E., Harris Peter C., Larusso Nicholas F., Octreotide Inhibits Hepatic Cystogenesis in a Rodent Model of Polycystic Liver Disease by Reducing Cholangiocyte Adenosine 3′,5′-Cyclic Monophosphate, 10.1053/j.gastro.2006.12.039
  33. Lai Xianyin, Blazer-Yost Bonnie L., Gattone Vincent H., Muchatuta Monalisa N., Witzmann Frank A., Protein composition of liver cyst fluid from the BALB/c-cpk/+ mouse model of autosomal recessive polycystic kidney disease, 10.1002/pmic.200800379
  34. Gerdes Jantje M., Davis Erica E., Katsanis Nicholas, The Vertebrate Primary Cilium in Development, Homeostasis, and Disease, 10.1016/j.cell.2009.03.023
  35. Decaens Thomas, Godard Cécile, de Reyniès Aurélien, Rickman David S., Tronche François, Couty Jean-Pierre, Perret Christine, Colnot Sabine, Stabilization of β-catenin affects mouse embryonic liver growth and hepatoblast fate, 10.1002/hep.21952
  36. Tan Xinping, Yuan Youzhong, Zeng Gang, Apte Udayan, Thompson Michael D., Cieply Benjamin, Stolz Donna B., Michalopoulos George K., Kaestner Klaus H., Monga Satdarshan P.S., β-Catenin deletion in hepatoblasts disrupts hepatic morphogenesis and survival during mouse development, 10.1002/hep.22225
  37. Zong Y., Panikkar A., Xu J., Antoniou A., Raynaud P., Lemaigre F., Stanger B. Z., Notch signaling controls liver development by regulating biliary differentiation, 10.1242/dev.029140
  38. Yanger K., Zong Y., Maggs L. R., Shapira S. N., Maddipati R., Aiello N. M., Thung S. N., Wells R. G., Greenbaum L. E., Stanger B. Z., Robust cellular reprogramming occurs spontaneously during liver regeneration, 10.1101/gad.207803.112
  39. Overgaard C. E., Sanzone K. M., Spiczka K. S., Sheff D. R., Sandra A., Yeaman C., Deciliation Is Associated with Dramatic Remodeling of Epithelial Cell Junctions and Surface Domains, 10.1091/mbc.e08-07-0741
  40. Takashima Yasuo, Terada Maiko, Kawabata Masuyo, Suzuki Atsushi, Dynamic three-dimensional morphogenesis of intrahepatic bile ducts in mouse liver development, 10.1002/hep.27436
Bibliographic reference Beaudry, Jean-Bernard ; Cordi, Sabine ; Demarez, Céline ; Lepreux, Sébastien ; Pierreux, Christophe ; et. al. Proliferation-Independent Initiation of Biliary Cysts in Polycystic Liver Diseases. In: PLoS One, Vol. 10, no. 6, p. e0132295
Permanent URL http://hdl.handle.net/2078.1/162117