The mitochondrial import gene tomm22 is specifically required for hepatocyte survival and provides a liver regeneration model

DMM Disease Models and Mechanisms

Volumn 3, Issue 7-8, 2010, Pages 486-495

  Curado, Silvia ^a   Ober, Elke A ^b   Walsh, Susan ^c   Cortes Hernandez, Paulina ^d   Verkade, Heather ^e   Koehler, Carla M ^c   Stainier, Didier Y R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; CARRIER PROTEIN; MITOCHONDRIAL PROTEIN; MORPHOLINE; PROTEIN TOMM22; UNCLASSIFIED DRUG; MUTANT PROTEIN; TOMM22 PROTEIN, ZEBRAFISH; WNT PROTEIN; ZEBRAFISH PROTEIN;

ARTICLE; BILE DUCT; CELL CULTURE; CELL DEGENERATION; CELL DIFFERENTIATION; CELL MATURATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENE IDENTIFICATION; GENE MUTATION; GENETIC CODE; GENETIC MODEL; LIVER CELL; LIVER DISEASE; LIVER REGENERATION; MITOCHONDRIAL GENE; MITOCHONDRIAL MEMBRANE; NONHUMAN; OUTER MEMBRANE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; WILD TYPE; ZEBRA FISH; ANIMAL; ANIMAL MODEL; ANTIBODY SPECIFICITY; APOPTOSIS; CELL SURVIVAL; CYTOLOGY; DRUG EFFECTS; ENDODERM; GENE SILENCING; GENETICS; METABOLISM; MUTATION; YEAST;

DANIO RERIO; VERTEBRATA;

ANIMALS; APOPTOSIS; CELL SURVIVAL; ENDODERM; GENE KNOCKDOWN TECHNIQUES; GENES, MITOCHONDRIAL; HEPATOCYTES; LIVER REGENERATION; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; MODELS, ANIMAL; MUTANT PROTEINS; MUTATION; OLIGONUCLEOTIDES, ANTISENSE; ORGAN SPECIFICITY; PHENOTYPE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; WNT PROTEINS; YEASTS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 77954855476     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.004390     Document Type: Article

References (65)

1. Ahting, U., Floss, T., Uez, N., Schneider-Lohmar, I., Becker, L., Kling, E., Iuso, A., Bender, A., de Angelis, M. H., Gailus-Durner, V. et al. (2009). Neurological phenotype and reduced lifespan in heterozygous Tim23 knockout mice, the first mouse model of defective mitochondrial import. Biochim. Biophys. Acta 1787, 371-376.
2. Alexander, J., Stainier, D. Y. and Yelon, D. (1998). Screening mosaic F1 females for mutations affecting zebrafish heart induction and patterning. Dev. Genet. 22, 288-299.
3. Anandatheerthavarada, H. K., Sepuri, N. B. and Avadhani, N. G. (2009). Mitochondrial targeting of cytochrome P450 proteins containing NH2-terminal chimeric signals involves an unusual TOM20/TOM22 bypass mechanism. J. Biol. Chem. 284, 17352-17363.
4. Becker, T., Gebert, M., Pfanner, N. and van der Laan, M. (2009). Biogenesis of mitochondrial membrane proteins. Curr. Opin Cell Biol. 21, 484-493.
5. Bolender, N., Sickmann, A., Wagner, R., Meisinger, C. and Pfanner, N. (2008). Multiple pathways for sorting mitochondrial precursor proteins. EMBO Rep. 9, 42-49.
6. Chen, B., Dodge, M. E., Tang, W., Lu, J., Ma, Z., Fan, C. W., Wei, S., Hao, W., Kilgore, J., Williams, N. S. et al. (2009). Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat. Chem. Biol. 5, 100-107.
7. Crosnier, C., Vargesson, N., Gschmeissner, S., Ariza-McNaughton, L., Morrison, A. and Lewis, J. (2005). Delta-Notch signalling controls commitment to a secretory fate in the zebrafish intestine. Development 132, 1093-1104.
8. Curado, S., Anderson, R. M., Jungblut, B., Mumm, J., Schroeter, E. and Stainier, D. Y. (2007). Conditional targeted cell ablation in zebrafish: a new tool for regeneration studies. Dev. Dyn. 236, 1025-1035.
9. Curado, S., Stainier, D. Y. and Anderson, R. M. (2008). Nitroreductase-mediated cell/tissue ablation in zebrafish: a spatially and temporally controlled ablation method with applications in developmental and regeneration studies. Nat. Protoc. 3, 948-954.
10. Curran, S. P., Leverich, E. P., Koehler, C. M. and Larsen, P. L. (2004). Defective mitochondrial protein translocation precludes normal Caenorhabditis elegans development. J. Biol. Chem. 279, 54655-54662.
11. Daum, G., Gasser, S. M. and Schatz, G. (1982). Import of proteins into mitochondria. Energy-dependent, two-step processing of the intermembrane space enzyme cytochrome b2 by isolated yeast mitochondria. J. Biol. Chem. 257, 13075-13080.
12. Deas, T. S., Bennett, C. J., Jones, S. A., Tilgner, M., Ren, P., Behr, M. J., Stein, D. A., Iversen, P. L., Kramer, L. D., Bernard, K. A. et al. (2007). In vitro resistance selection and in vivo efficacy of morpholino oligomers against West Nile virus. Antimicrob. Agents Chemother. 51, 2470-2482.
13. Endo, T., Yamamoto, H. and Esaki, M. (2003). Functional cooperation and separation of translocators in protein import into mitochondria, the double-membrane bounded organelles. J. Cell Sci. 116, 3259-3267.
14. Farooq, M., Sulochana, K. N., Pan, X., To, J., Sheng, D., Gong, Z. and Ge, R. (2008). Histone deacetylase 3 (hdac3) is specifically required for liver development in zebrafish. Dev. Biol. 317, 336-353.
15. Fausto, N., Laird, A. D. and Webber, E. M. (1995). Liver regeneration. 2. Role of growth factors and cytokines in hepatic regeneration. FASEB J. 9, 1527-1536.
16. Fausto, N., Campbell, J. S. and Riehle, K. J. (2006). Liver regeneration. Hepatology 43, S45-S53.
17. Field, H. A., Ober, E. A., Roeser, T. and Stainier, D. Y. R. (2003). Formation of the digestive system in zebrafish. I. Liver morphogenesis. Dev. Biol. 253, 279-290.
18. Geller, B. L. (2005). Antibacterial antisense. Curr. Opin. Mol. Ther. 7, 109-113.
19. Gerloff, T., Stieger, B., Hagenbuch, B., Madon, J., Landmann, L., Roth, J., Hofmann, A. F. and Meier, P. J. (1998). The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J. Biol. Chem. 273, 10046-10050.
20. Goessling, W., North, T. E., Lord, A. M., Ceol, C., Lee, S., Weidinger, G., Bourque, C., Strijbosch, R., Haramis, A. P., Puder, M. et al. (2008). APC mutant zebrafish uncover a changing temporal requirement for wnt signaling in liver development. Dev. Biol. 320, 161-174.
21. Guo, Y., Cheong, N., Zhang, Z., De Rose, R., Deng, Y., Farber, S. A., Fernandes-Alnemri, T. and Alnemri, E. S. (2004). Tim50, a component of the mitochondrial translocator, regulates mitochondrial integrity and cell death. J. Biol. Chem. 279, 24813-24825.
22. Hayashi, T., Mizuno, N. and Kondoh, H. (2008). Determinative roles of FGF and Wnt signals in iris-derived lens regeneration in newt eye. Dev. Growth Differ. 50, 279-287.
23. Heasman, J. (2002). Morpholino oligos: making sense of antisense? Dev. Biol. 243, 209-214.
24. Her, G. M., Chiang, C. C., Chen, W. Y. and Wu, J. L. (2003). In vivo studies of liver-type fatty acid binding protein (L-FABP) gene expression in liver of transgenic zebrafish (Danio rerio). FEBS Lett. 538, 125-133.
25. Hwang, D. K., Claypool, S. M., Leuenberger, D., Tienson, H. L. and Koehler, C. M. (2007). Tim54p connects inner membrane assembly and proteolytic pathways in the mitochondrion. J. Cell Biol. 178, 1161-1175.
26. 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.
27. Kan, N. G., Junghans, D. and Izpisua Belmonte, J. C. (2009). Compensatory growth mechanisms regulated by BMP and FGF signaling mediate liver regeneration in zebrafish after partial hepatectomy. FASEB J. 23, 3516-3525.
28. Koehler, C. M. (2004). New developments in mitochondrial assembly. Annu. Rev. Cell Dev. Biol. 20, 309-335.
29. Kuznetsov, A. V., Usson, Y., Leverve, X. and Margreiter, R. (2004). Subcellular heterogeneity of mitochondrial function and dysfunction: evidence obtained by confocal imaging. Mol. Cell Biochem. 256-257, 359-365.
30. Lepper, C., Conway, S. J. and Fan, C. M. (2009). Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 460, 627-631.
31. Martins, P. N., Theruvath, T. P. and Neuhaus, P. (2008). Rodent models of partial hepatectomies. Liver Int. 28, 3-11.
32. McLin, V. A., Rankin, S. A. and Zorn, A. M. (2007). Repression of Wnt/beta-catenin signaling in the anterior endoderm is essential for liver and pancreas development. Development 134, 2207-2217.
33. Michalopoulos, G. K. and DeFrances, M. C. (1997). Liver regeneration. Science 276, 60-66.
34. 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.
35. Nakamura, T. and Nishina, H. (2009). Liver development: lessons from knockout mice and mutant fish. Hepatol. Res. 39, 633-644.
36. 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.
37. Nasevicius, A. and Ekker, S. C. (2000). Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26, 216-220.
38. Neupert, W. and Herrmann, J. M. (2007). Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76, 723-749.
39. Ober, E. A., Verkade, H., Field, H. A. and Stainier, D. Y. (2006). Mesodermal Wnt2b signalling positively regulates liver specification. Nature 442, 688-691.
40. Pagliarini, D. J., Calvo, S. E., Chang, B., Sheth, S. A., Vafai, S. B., Ong, S. E., Walford, G. A., Sugiana, C., Boneh, A., Chen, W. K. et al. (2008). A mitochondrial protein compendium elucidates complex I disease biology. Cell 134, 112-123.
41. Pfanner, N. and Wiedemann, N. (2002). Mitochondrial protein import: two membranes, three translocases. Curr. Opin. Cell Biol. 14, 400-411.
42. Pisharath, H., Rhee, J. M., Swanson, M. A., Leach, S. D. and Parsons, M. J. (2007). Targeted ablation of beta cells in the embryonic zebrafish pancreas using E. coli nitroreductase. Mech. Dev. 124, 218-229.
43. Polesskaya, A., Seale, P. and Rudnicki, M. A. (2003). Wnt signaling induces the myogenic specification of resident CD45+ adult stem cells during muscle regeneration. Cell 113, 841-852.
44. Rehling, P., Brandner, K. and Pfanner, N. (2004). Mitochondrial import and the twinpore translocase. Nat. Rev. Mol. Cell Biol. 5, 519-530.
45. Romano, N., Picchietti, S., Taverne-Thiele, J. J., Taverne, N., Abelli, L., Mastrolia, L., Verburg-van Kemenade, B. M. and Rombout, J. H. (1998). Distribution of macrophages during fish development: an immunohistochemical study in carp (Cyprinus carpio, L.). Anat. Embryol. 198, 31-41.
46. 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.
47. 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. USA 104, 1570-1575.
48. Sakaguchi, T. F., Sadler, K. C., Crosnier, C. and Stainier, D. Y. (2008). Endothelial signals modulate hepatocyte apicobasal polarization in zebrafish. Curr. Biol. 18, 1565-1571.
49. Saxena, R., Zucker, S. D. and Crawford, J. M. (2003). Hepatology: A Textbook of Liver Disease. Philadelphia: Saunders.
50. Shestopalov, I. A., Sinha, S. and Chen, J. K. (2007). Light-controlled gene silencing in zebrafish embryos. Nat. Chem. Biol. 3, 650-651.
51. 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.
52. Sodhi, D., Micsenyi, A., Bowen, W. C., Monga, D. K., Talavera, J. C. and Monga, S. P. (2005). Morpholino oligonucleotide-triggered beta-catenin knockdown compromises normal liver regeneration. J. Hepatol. 43, 132-141.
53. 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.
54. Stoick-Cooper, C. L., Weidinger, G., Riehle, K. J., Hubbert, C., Major, M. B., Fausto, N. and Moon, R. T. (2007). Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development 134, 479-489.
55. 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.
56. 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.
57. 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.
58. Tan, X., Yuan, Y., Zeng, G., Apte, U., Thompson, M. D., Cieply, B., Stolz, D. B., Michalopoulos, G. K., Kaestner, K. H. and Monga, S. P. (2008). Beta-catenin deletion in hepatoblasts disrupts hepatic morphogenesis and survival during mouse development. Hepatology 47, 1667-1679.
59. van der Sar, A. M., Appelmelk, B. J., Vandenbroucke-Grauls, C. M. and Bitter, W. (2004). A star with stripes: zebrafish as an infection model. Trends Microbiol. 12, 451-457.
60. Westerfield, M. (2000). The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio), 4th edn. Eugene, OR: University of Oregon Press.
61. Yu, P. B., Hong, C. C., Sachidanandan, C., Babitt, J. L., Deng, D. Y., Hoyng, S. A., Lin, H. Y., Bloch, K. D. and Peterson, R. T. (2008). Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat. Chem. Biol. 4, 33-41.
62. Zaret, K. S. and Grompe, M. (2008). Generation and regeneration of cells of the liver and pancreas. Science 322, 1490-1494.
63. Zhang, L., Theise, N., Chua, M. and Reid, L. M. (2008). The stem cell niche of human livers: symmetry between development and regeneration. Hepatology 48, 1598-1607.
64. Zhao, R. and Duncan, S. A. (2005). Embryonic development of the liver. Hepatology 41, 956-967.
65. Zhong, N., Gersch, R. P. and Hadjiargyrou, M. (2006). Wnt signaling activation during bone regeneration and the role of Dishevelled in chondrocyte proliferation and differentiation. Bone 39, 5-16.