Compensatory growth mechanisms regulated by BMP and FGF signaling mediate liver regeneration in zebrafish after partial hepatectomy

FASEB Journal

Volumn 23, Issue 10, 2009, Pages 3516-3525

  Kan, Natalia G ^a,c   Junghans, Dirk ^a,b,d   Belmonte, Juan Carlos Izpisua ^a,b  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b CENTER OF REGENERATIVE MEDICINE IN BARCELONA   (Spain)

^c BURNHAM INSTITUTE   (United States)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Danio rerio; Hepatocyte proliferation; Liver mass restoration; Liver to body weight ratio

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 1; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLOGICAL MODEL; BODY WEIGHT; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; INJURY SEVERITY; LIVER CELL; LIVER INJURY; LIVER REGENERATION; LIVER STRUCTURE; MALE; NONHUMAN; PARTIAL HEPATECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSGENIC ANIMAL; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BONE MORPHOGENETIC PROTEIN RECEPTORS; BONE MORPHOGENETIC PROTEINS; FIBROBLAST GROWTH FACTORS; HEPATECTOMY; LIVER; LIVER REGENERATION; MODELS, ANIMAL; ORGAN SIZE; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; ZEBRAFISH;

DANIO RERIO; MAMMALIA; RODENTIA; VERTEBRATA;

EID: 70349670584     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-131730     Document Type: Article

References (41)

1. Taub, R. (2004) Liver regeneration: from myth to mechanism. Nat. Rev. Mol. Cell Biol. 5, 836-847
2. Michalopoulos, G. K. (2007) Liver regeneration. J. Cell. Physiol. 213, 286-300
3. Fausto, N., Campbell, J. S., and Riehle, K. J. (2006) Liver regeneration. Hepatology 43, S45-53
4. Driever, W., Solnica-Krezel, L., Schier, A. F., Neuhauss, S. C., Malicki, J., Stemple, D. L., Stainier, D. Y., Zwartkruis, F., Abdelilah, S., Rangini, Z., Belak, J., and Boggs, C. (1996) A genetic screen for mutations affecting embryogenesis in zebrafish. Development 123, 37-46 (Pubitemid 27056734)
5. Haffter, P., Granato, M., Brand, M., Mullins, M. C., Hammerschmidt, M., Kane, D. A., Odenthal, J., van Eeden, F. J., Jiang, Y. J., Heisenberg, C. P., Kelsh, R. N., Furutani-Seiki, M., Vogelsang, E., Beuchle, D., Schach, U., Fabian, C., and Nusslein- Volhard, C. (1996) The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 123, 1-36
6. Weglarz, T. C., and Sandgren, E. P. (2000) Timing of hepatocyte entry into DNA synthesis after partial hepatectomy is cell autonomous. Proc. Natl. Acad. Sci. U. S. A. 97, 12595-12600
7. Poss, K. D., Keating, M. T., and Nechiporuk, A. (2003) Tales of regeneration in zebrafish. Dev. Dyn. 226, 202-210
8. Goessling, W., North, T. E., Lord, A. M., Ceol, C., Lee, S., Weidinger, G., Bourque, C., Strijbosch, R., Haramis, A. P., Puder, M., Clevers, H., Moon, R. T., and Zon, L. I. (2008) APC mutant zebrafish uncover a changing temporal requirement for wnt signaling in liver development. Dev. Biol. 320, 161-174
9. Sadler, K. C., Krahn, K. N., Gaur, N. A., and Ukomadu, C. (2007) Liver growth in the embryo and during liver regeneration in zebrafish requires the cell cycle regulator, uhrf1. Proc. Natl. Acad. Sci. U. S. A. 104, 1570-1575
10. Sugimoto, H., Yang, C., LeBleu, V. S., Soubasakos, M. A., Giraldo, M., Zeisberg, M., and Kalluri, R. (2007) BMP-7 functions as a novel hormone to facilitate liver regeneration. FASEB J. 21, 256-264 (Pubitemid 46052564)
11. Nakatsuka, R., Taniguchi, M., Hirata, M., Shiota, G., and Sato, K. (2007) Transient expression of bone morphogenic protein-2 in acute liver injury by carbon tetrachloride. J. Biochem. 141, 113-119
12. Sturm, J., Keese, M., Zhang, H., Bonninghoff, R., Magdeburg, R., Vajkoczy, P., Dono, R., Zeller, R., and Gretz, N. (2004) Liver regeneration in FGF-2-deficient mice: VEGF acts as potential functional substitute for FGF-2. Liver Int. 24, 161-168 (Pubitemid 38585003)
13. Steiling, H., Wustefeld, T., Bugnon, P., Brauchle, M., Fassler, R., Teupser, D., Thiery, J., Gordon, J. I., Trautwein, C., and Werner, S. (2003) Fibroblast growth factor receptor signalling is crucial for liver homeostasis and regeneration. Oncogene 22, 4380-4388 (Pubitemid 36897968)
14. Shin, D., Shin, C. H., Tucker, J., Ober, E. A., Rentzsch, F., Poss, K. D., Hammerschmidt, M., Mullins, M. C., and Stainier, D. Y. (2007) Bmp and Fgf signaling are essential for liver specification in zebrafish. Development 134, 2041-2050 (Pubitemid 46979791)
15. Pyati, U. J., Webb, A. E., and Kimelman, D. (2005) Transgenic zebrafish reveal stage-specific roles for Bmp signaling in ventral and posterior mesoderm development. Development 132, 2333-2343 (Pubitemid 40872803)
16. Lee, Y., Grill, S., Sanchez, A., Murphy-Ryan, M., and Poss, K. D. (2005) Fgf signaling instructs position-dependent growth rate during zebrafish fin regeneration. Development 132, 5173-5183 (Pubitemid 43020173)
17. Westerfield, M. (2000) The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio), 4th ed., University of Oregon Press, Eugene, OR, USA
18. Junghans, D., Hack, I., Frotscher, M., Taylor, V., and Kemler, R. (2005) Beta-catenin-mediated cell-adhesion is vital for embryonic forebrain development. Dev. Dyn. 233, 528-539 (Pubitemid 40734052)
19. Ghosh, C., Zhou, Y. L., and Collodi, P. (1994) Derivation and characterization of a zebrafish liver cell line. Cell Biol. Toxicol. 10, 167-176 (Pubitemid 24258058)
20. Michalopoulos, G. K., and DeFrances, M. C. (1997) Liver regeneration. Science 276, 60-66
21. Grisham, J. W. (1962) A morphologic study of deoxyribonucleic acid synthesis and cell proliferation in regenerating rat liver; autoradiography with thymidine-H3. Cancer Res. 22, 842-849
22. Sosa-Pineda, B., Wigle, J. T., and Oliver, G. (2000) Hepatocyte migration during liver development requires Prox1. Nat. Genet. 25, 254-255 (Pubitemid 30437306)
23. Monga, S. P., Pediaditakis, P., Mule, K., Stolz, D. B., and Michalopoulos, G. K. (2001) Changes in WNT/beta-catenin pathway during regulated growth in rat liver regeneration. Hepatology 33, 1098-1109 (Pubitemid 32378208)
24. Tan, X., Behari, J., Cieply, B., Michalopoulos, G. K., and Monga, S. P. (2006) Conditional deletion of beta-catenin reveals its role in liver growth and regeneration. Gastroenterology 131, 1561-1572 (Pubitemid 44708943)
25. Ober, E. A., Verkade, H., Field, H. A., and Stainier, D. Y. (2006) Mesodermal Wnt2b signalling positively regulates liver specification. Nature 442, 688-691 (Pubitemid 44215323)
26. Graff, J. M., Thies, R. S., Song, J. J., Celeste, A. J., and Melton, D. A. (1994) Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo. Cell 79, 169-179 (Pubitemid 2153070)
27. Amaya, E., Musci, T. J., and Kirschner, M. W. (1991) Expression of a dominant negative mutant of the FGF receptor disrupts mesoderm formation in Xenopus embryos. Cell 66, 257-270 (Pubitemid 121001364)
28. Burke, Z. D., Thowfeequ, S., and Tosh, D. (2006) Liver specification: a new role for Wnts in liver development. Curr. Biol. 16, R688-690 (Pubitemid 44691797)
29. Calmont, A., Wandzioch, E., Tremblay, K. D., Minowada, G., Kaestner, K. H., Martin, G. R., and Zaret, K. S. (2006) An FGF response pathway that mediates hepatic gene induction in embryonic endoderm cells. Dev. Cell 11, 339-348 (Pubitemid 44283941)
30. Jung, J., Zheng, M., Goldfarb, M., and Zaret, K. S. (1999) Initiation of mammalian liver development from endoderm by fibroblast growth factors. Science 284, 1998-2003 (Pubitemid 29309449)
31. Rossi, J. M., Dunn, N. R., Hogan, B. L., and Zaret, K. S. (2001) Distinct mesodermal signals, including BMPs from the septum transversum mesenchyme, are required in combination for hepatogenesis from the endoderm. Genes Dev. 15, 1998-2009
32. Zaret, K. S. (2002) Regulatory phases of early liver development: paradigms of organogenesis. Nat. Rev. Genet. 3, 499-512
33. Baruch, Y., Shoshany, G., Neufeld, G., and Enat, R. (1995) Basic fibroblast growth factor is hepatotropic for rat liver in regeneration. J. Hepatol. 23, 328-332
34. Hioki, O., Minemura, M., Shimizu, Y., Kasii, Y., Nishimori, H., Takahara, T., Higuchi, K., Yoshitake, Y., Nishikawa, K., and Watanabe, A. (1996) Expression and localization of basic fibroblast growth factor (bFGF) in the repair process of rat liver injury. J. Hepatol. 24, 217-224 (Pubitemid 26057957)
35. Itoh, N., and Ornitz, D. M. (2004) Evolution of the Fgf and Fgfr gene families. Trends Genet. 20, 563-569 (Pubitemid 39314564)
36. Poss, K. D., Shen, J., Nechiporuk, A., McMahon, G., Thisse, B., Thisse, C., and Keating, M. T. (2000) Roles for Fgf signaling during zebrafish fin regeneration. Dev. Biol. 222, 347-358 (Pubitemid 30416373)
37. Whitehead, G. G., Makino, S., Lien, C. L., and Keating, M. T. (2005) fgf20 is essential for initiating zebrafish fin regeneration. Science 310, 1957-1960
38. Thummel, R., Bai, S., Sarras, M. P., Jr., Song, P., McDermott, J., Brewer, J., Perry, M., Zhang, X., Hyde, D. R., and Godwin, A. R. (2006) Inhibition of zebrafish fin regeneration using in vivo electroporation of morpholinos against fgfr1 and msxb. Dev. Dyn. 235, 336-346 (Pubitemid 43100940)
39. Yin, V. P., Thomson, J. M., Thummel, R., Hyde, D. R., Hammond, S. M., and Poss, K. D. (2008) Fgf-dependent depletion of microRNA-133 promotes appendage regeneration in zebrafish. Genes Dev. 22, 728-733
40. Lepilina, A., Coon, A. N., Kikuchi, K., Holdway, J. E., Roberts, R. W., Burns, C. G., and Poss, K. D. (2006) A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 127, 607-619 (Pubitemid 44647426)
41. Lam, S. H., Wu, Y. L., Vega, V. B., Miller, L. D., Spitsbergen, J., Tong, Y., Zhan, H., Govindarajan, K. R., Lee, S., Mathavan, S., Murthy, K. R., Buhler, D. R., Liu, E. T., and Gong, Z. (2006) Conservation of gene expression signatures between zebrafish and human liver tumors and tumor progression. Nat. Biotechnol. 24, 73-75 (Pubitemid 43083168)