Large-Scale Quantitative Proteomics Identifies the Ubiquitin Ligase Nedd4-1 as an Essential Regulator of Liver Regeneration

Developmental Cell

Volumn 42, Issue 6, 2017, Pages 616-625.e8

  Bachofner, Marc ^a   Speicher, Tobias ^a   Bogorad, Roman L ^b   Muzumdar, Sukalp ^a   Derrer, Carina P ^a   Hürlimann, Fabrizio ^a   Böhm, Friederike ^a   Nanni, Paolo ^c   Kockmann, Tobias ^a,c   Kachaylo, Ekaterina ^d   Meyer, Michael ^a   Padrissa Altés, Susagna ^a   Graf, Rolf ^d   Anderson, Daniel G ^b,e   Koteliansky, Victor ^f   auf dem Keller, Ulrich ^a   Werner, Sabine ^a  

^a ETH ZURICH   (Switzerland)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^e Massachusetts Institute of Technology Cambridge   (United States)

^f SKOLKOVO INSTITUTE OF SCIENCE AND TECHNOLOGY   (Russian Federation)

Author keywords

EGF; Eps15; hepatocyte; HGF; liver regeneration; Nedd4 1; proteomics; siRNA; ubiquitin

Indexed keywords

GROWTH FACTOR RECEPTOR; MITOGENIC AGENT; NANOPARTICLE; PROTEASOME; SMALL INTERFERING RNA; UBIQUITIN; UBIQUITIN PROTEIN LIGASE NEDD4; UBIQUITIN PROTEIN LIGASE NEDD4 1; UNCLASSIFIED DRUG; EPIDERMAL GROWTH FACTOR RECEPTOR; ESCRT PROTEIN; NEDD4 UBIQUITIN PROTEIN LIGASES; POLYUBIQUITIN; PROTEOME; UBIQUITIN PROTEIN LIGASE;

ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; DISEASE SEVERITY; GENE SILENCING; IN VIVO STUDY; INTERNALIZATION; LIVER CELL; LIVER FAILURE; LIVER INJURY; LIVER REGENERATION; LIVER RESECTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEOMICS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; C57BL MOUSE; DRUG EFFECTS; ENDOCYTOSIS; INJURIES; LIVER; MALE; METABOLISM; PATHOLOGY; PROCEDURES; REPRODUCIBILITY; UBIQUITINATION;

ANIMALS; ENDOCYTOSIS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; GENE KNOCKDOWN TECHNIQUES; HEPATOCYTES; LIVER; LIVER REGENERATION; MALE; MICE, INBRED C57BL; MITOGENS; POLYUBIQUITIN; PROTEOME; PROTEOMICS; RECEPTOR, EPIDERMAL GROWTH FACTOR; REPRODUCIBILITY OF RESULTS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 85030832225     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2017.07.025     Document Type: Article

References (51)

1. auf dem Keller, U., Overall, C.M., CLIPPER: an add-on to the Trans-Proteomic Pipeline for the automated analysis of TAILS N-terminomics data. Biol. Chem. 393 (2012), 1477–1483.
2. Azimifar, S.B., Nagaraj, N., Cox, J., Mann, M., Cell-type-resolved quantitative proteomics of murine liver. Cell Metab. 20 (2014), 1076–1087.
3. Bellet, M.M., Piobbico, D., Bartoli, D., Castelli, M., Pieroni, S., Brunacci, C., Chiacchiaretta, M., Del Sordo, R., Fallarino, F., Sidoni, A., et al. NEDD4 controls the expression of GUCD1, a protein upregulated in proliferating liver cells. Cell Cycle 13 (2014), 1902–1911.
4. Beyer, T.A., Werner, S., The cytoprotective Nrf2 transcription factor controls insulin receptor signaling in the regenerating liver. Cell Cycle 7 (2008), 874–878.
5. Boase, N.A., Kumar, S., NEDD4: the founding member of a family of ubiquitin-protein ligases. Gene 557 (2015), 113–122.
6. Böhm, F., Speicher, T., Hellerbrand, C., Dickson, C., Partanen, J.M., Ornitz, D.M., Werner, S., FGF receptors 1 and 2 control chemically induced injury and compound detoxification in regenerating livers of mice. Gastroenterology 139 (2010), 1385–1396.
7. Borowiak, M., Garratt, A.N., Wustefeld, T., Strehle, M., Trautwein, C., Birchmeier, C., Met provides essential signals for liver regeneration. Proc. Natl. Acad. Sci. USA 101 (2004), 10608–10613.
8. Bracht, T., Hagemann, S., Loscha, M., Megger, D.A., Padden, J., Eisenacher, M., Kuhlmann, K., Meyer, H.E., Baba, H.A., Sitek, B., Proteome analysis of a hepatocyte-specific BIRC5 (survivin)-knockout mouse model during liver regeneration. J. Proteome Res. 13 (2014), 2771–2782.
9. Brankatschk, B., Wichert, S.P., Johnson, S.D., Schaad, O., Rossner, M.J., Gruenberg, J., Regulation of the EGF transcriptional response by endocytic sorting. Sci. Signal., 5, 2012, ra21.
10. Choe, L., D'Ascenzo, M., Relkin, N.R., Pappin, D., Ross, P., Williamson, B., Guertin, S., Pribil, P., Lee, K.H., 8-plex quantitation of changes in cerebrospinal fluid protein expression in subjects undergoing intravenous immunoglobulin treatment for Alzheimer's disease. Proteomics 7 (2007), 3651–3660.
11. Choi, M., Chang, C.Y., Clough, T., Broudy, D., Killeen, T., MacLean, B., Vitek, O., MSstats: an R package for statistical analysis of quantitative mass spectrometry-based proteomic experiments. Bioinformatics 30 (2014), 2524–2526.
12. Chomczynski, P., Sacchi, N., Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162 (1987), 156–159.
13. Deutsch, E.W., Mendoza, L., Shteynberg, D., Farrah, T., Lam, H., Tasman, N., Sun, Z., Nilsson, E., Pratt, B., Prazen, B., et al. A guided tour of the Trans-Proteomic Pipeline. Proteomics 10 (2010), 1150–1159.
14. Edwin, F., Anderson, K., Patel, T.B., HECT domain-containing E3 ubiquitin ligase Nedd4 interacts with and ubiquitinates Sprouty2. J. Biol. Chem. 285 (2010), 255–264.
15. Emili, A., Cox, B., Tissue subcellular fractionation and protein extraction for use in mass-spectrometry-based proteomics. Nat. Protoc. 1 (2006), 1872–1878.
16. Escher, C., Reiter, L., MacLean, B., Ossola, R., Herzog, F., Chilton, J., MacCoss, M.J., Rinner, O., Using iRT, a normalized retention time for more targeted measurement of peptides. Proteomics 12 (2012), 1111–1121.
17. Fouladkou, F., Lu, C., Jiang, C., Zhou, L., She, Y., Walls, J.R., Kawabe, H., Brose, N., Henkelman, R.M., Huang, A., et al. The ubiquitin ligase Nedd4-1 is required for heart development and is a suppressor of thrombospondin-1. J. Biol. Chem. 285 (2010), 6770–6780.
18. Guo, T., Kouvonen, P., Koh, C.C., Gillet, L.C., Wolski, W.E., Rost, H.L., Rosenberger, G., Collins, B.C., Blum, L.C., Gillessen, S., et al. Rapid mass spectrometric conversion of tissue biopsy samples into permanent quantitative digital proteome maps. Nat. Med. 21 (2015), 407–413.
19. Huh, C.G., Factor, V.M., Sanchez, A., Uchida, K., Conner, E.A., Thorgeirsson, S.S., Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair. Proc. Natl. Acad. Sci. USA 101 (2004), 4477–4482.
20. Keller, A., Nesvizhskii, A.I., Kolker, E., Aebersold, R., Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74 (2002), 5383–5392.
21. Kislinger, T., Cox, B., Kannan, A., Chung, C., Hu, P.Z., Ignatchenko, A., Scott, M.S., Gramolini, A.O., Morris, Q., Hallett, M.T., et al. Global survey of organ and organelle protein expression in mouse: combined proteomic and transcriptomic profiling. Cell 125 (2006), 173–186.
22. Kohjima, M., Tsai, T.H., Tackett, B.C., Thevananther, S., Li, L., Chang, B.H., Chan, L., Delayed liver regeneration after partial hepatectomy in adipose differentiation related protein-null mice. J. Hepatol. 59 (2013), 1246–1254.
23. Kohler, U.A., Kurinna, S., Schwitter, D., Marti, A., Schafer, M., Hellerbrand, C., Speicher, T., Werner, S., Activated Nrf2 impairs liver regeneration in mice by activation of genes involved in cell-cycle control and apoptosis. Hepatology 60 (2014), 670–678.
24. Lex, A., Gehlenborg, N., Strobelt, H., Vuillemot, R., Pfister, H., UpSet: visualization of intersecting sets. IEEE Trans. Vis. Comput. Graph. 20 (2014), 1983–1992.
25. Love, K.T., Mahon, K.P., Levins, C.G., Whitehead, K.A., Querbes, W., Dorkin, J.R., Qin, J., Cantley, W., Qin, L.L., Racie, T., et al. Lipid-like materials for low-dose, in vivo gene silencing. Proc. Natl. Acad. Sci. USA 107 (2010), 1864–1869.
26. MacLean, B., Tomazela, D.M., Shulman, N., Chambers, M., Finney, G.L., Frewen, B., Kern, R., Tabb, D.L., Liebler, D.C., MacCoss, M.J., Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26 (2010), 966–968.
27. Mederacke, I., Dapito, D.H., Affo, S., Uchinami, H., Schwabe, R.F., High-yield and high-purity isolation of hepatic stellate cells from normal and fibrotic mouse livers. Nat. Protoc. 10 (2015), 305–315.
28. Michalopoulos, G.K., Liver regeneration. J. Cell Physiol. 213 (2007), 286–300.
29. Michalopoulos, G.K., Liver regeneration after partial hepatectomy: critical analysis of mechanistic dilemmas. Am. J. Pathol. 176 (2010), 2–13.
30. Mosesson, Y., Shtiegman, K., Katz, M., Zwang, Y., Vereb, G., Szollosi, J., Yarden, Y., Endocytosis of receptor tyrosine kinases is driven by monoubiquitylation, not polyubiquitylation. J. Biol. Chem. 278 (2003), 21323–21326.
31. Natarajan, A., Wagner, B., Sibilia, M., The EGF receptor is required for efficient liver regeneration. Proc. Natl. Acad. Sci. USA 104 (2007), 17081–17086.
32. Nesvizhskii, A.I., Keller, A., Kolker, E., Aebersold, R., A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75 (2003), 4646–4658.
33. Padrissa-Altes, S., Bachofner, M., Bogorad, R.L., Pohlmeier, L., Rossolini, T., Böhm, F., Liebisch, G., Hellerbrand, C., Koteliansky, V., Speicher, T., et al. Control of hepatocyte proliferation and survival by Fgf receptors is essential for liver regeneration in mice. Gut 64 (2015), 1444–1453.
34. Parachoniak, C.A., Park, M., Distinct recruitment of Eps15 via its coiled-coil domain is required for efficient down-regulation of the met receptor tyrosine kinase. J. Biol. Chem. 284 (2009), 8382–8394.
35. Paranjpe, S., Bowen, W.C., Mars, W.M., Orr, A., Haynes, M.M., DeFrances, M.C., Liu, S., Tseng, G.C., Tsagianni, A., Michalopoulos, G.K., Combined systemic elimination of MET and epidermal growth factor receptor signaling completely abolishes liver regeneration and leads to liver decompensation. Hepatology 64 (2016), 1711–1724.
36. Persaud, A., Alberts, P., Amsen, E.M., Xiong, X., Wasmuth, J., Saadon, Z., Fladd, C., Parkinson, J., Rotin, D., Comparison of substrate specificity of the ubiquitin ligases Nedd4 and Nedd4-2 using proteome arrays. Mol. Syst. Biol., 5, 2009, 333.
37. Platta, H.W., Stenmark, H., Endocytosis and signaling. Curr. Opin. Cell Biol. 23 (2011), 393–403.
38. Polo, S., Sigismund, S., Faretta, M., Guidi, M., Capua, M.R., Bossi, G., Chen, H., Camilli, D., Di Fiore, P.P., A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416 (2002), 451–455.
39. Rainer, J., Sanchez-Cabo, F., Stocker, G., Sturn, A., Trajanoski, Z., CARMAweb: comprehensive R- and bioconductor-based web service for microarray data analysis. Nucleic Acids Res. 34 (2006), W498–W503.
40. Reiter, L., Rinner, O., Picotti, P., Huttenhain, R., Beck, M., Brusniak, M.Y., Hengartner, M.O., Aebersold, R., mProphet: automated data processing and statistical validation for large-scale SRM experiments. Nat. Methods 8 (2011), 430–435.
41. Rudich, N., Zamir, G., Pappo, O., Shlomai, Z., Faroja, M., Weiss, I.D., Wald, H., Galun, E., Peled, A., Wald, O., Focal liver necrosis appears early after partial hepatectomy and is dependent on T cells and antigen delivery from the gut. Liver Int. 29 (2009), 1273–1284.
42. Sadler, K.C., Krahn, K.N., Gaur, N.A., Ukomadu, C., Liver growth in the embryo and during liver regeneration in zebrafish requires the cell cycle regulator, uhrf1. Proc. Natl. Acad. Sci. USA 104 (2007), 1570–1575.
43. Savio, M.G., Wollscheid, N., Cavallaro, E., Algisi, V., Di Fiore, P.P., Sigismund, S., Maspero, E., Polo, S., Savio, M.G., Wollscheid, N., et al. USP9X controls EGFR Fate by deubiquitinating the endocytic adaptor Eps15. Curr. Biol. 26 (2016), 173–183.
44. Schlage, P., Egli, F.E., Nanni, P., Wang, L.W., Kizhakkedathu, J.N., Apte, S.S., auf dem Keller, U., Time-resolved analysis of the matrix metalloproteinase 10 substrate degradome. Mol. Cell. Proteomics 13 (2014), 580–593.
45. Shadforth, I.P., Dunkley, T.P., Lilley, K.S., Bessant, C., i-Tracker: for quantitative proteomics using iTRAQ. BMC Genomics, 6, 2005, 145.
46. Sigismund, S., Woelk, T., Puri, C., Maspero, E., Tacchetti, C., Transidico, P., Di Fiore, P.P., Polo, S., Clathrin-independent endocytosis of ubiquitinated cargos. Proc. Natl. Acad. Sci. USA 102 (2005), 2760–2765.
47. Skarpen, E., Oksvold, M.P., Grosvik, H., Widnes, C., Huitfeldt, H.S., Altered regulation of EGF receptor signaling following a partial hepatectomy. J. Cell Physiol. 202 (2005), 707–716.
48. Sousa, L.P., Lax, I., Shen, H., Ferguson, S.M., De Camilli, P., Schlessinger, J., Suppression of EGFR endocytosis by dynamin depletion reveals that EGFR signaling occurs primarily at the plasma membrane. Proc. Natl. Acad. Sci. USA 109 (2012), 4419–4424.
49. Speicher, T., Siegenthaler, B., Bogorad, R.L., Ruppert, R., Petzold, T., Padrissa-Altes, S., Bachofner, M., Anderson, D.G., Koteliansky, V., Fassler, R., et al. Knockdown and knockout of beta1-integrin in hepatocytes impairs liver regeneration through inhibition of growth factor signalling. Nat. Commun., 5, 2014, 3862.
50. Wakabayashi, N., Shin, S., Slocum, S.L., Agoston, E.S., Wakabayashi, J., Kwak, M.K., Misra, V., Biswal, S., Yamamoto, M., Kensler, T.W., Regulation of notch1 signaling by nrf2: implications for tissue regeneration. Sci. Signal., 3, 2010, ra52.
51. Woelk, T., Oldrini, B., Maspero, E., Confalonieri, S., Cavallaro, E., Di Fiore, P.P., Polo, S., Molecular mechanisms of coupled monoubiquitination. Nat. Cell Biol. 8 (2006), 1246–1254.