Comparative Proteomic Analysis of Human Liver Tissue and Isolated Hepatocytes with a Focus on Proteins Determining Drug Exposure

Journal of Proteome Research

Volumn 14, Issue 8, 2015, Pages 3305-3314

  Vildhede, Anna ^a   Wis̈niewski, Jacek R ^b   Norén, Agneta ^a   Karlgren, Maria ^a   Artursson, Per ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

ADME proteins; CYP enzymes; drug transporters; human hepatocytes; in vitro in vivo extrapolation; membrane proteome; oxidative stress; quantitative proteomics; total protein approach; UGT enzymes

Indexed keywords

BILE SALT EXPORT PUMP; CARRIER PROTEIN; PITAVASTATIN; PROTEIN; PROTEOME; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; MEMBRANE PROTEIN; QUINOLINE DERIVATIVE;

ADULT; AGED; ARTICLE; CELL MEMBRANE; CIRCULATION; DRUG EXPOSURE; EXCISION; FEMALE; HEK293 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LIVER; LIVER CELL; LIVER CLEARANCE; LIVER MEMBRANE; LIVER RESECTION; MALE; MASS SPECTROMETRY; MITOCHONDRIAL MEMBRANE; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PARTIAL HEPATECTOMY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEOMICS; RNA TRANSLATION; TANDEM MASS SPECTROMETRY; UBIQUITINATION; WESTERN BLOTTING; CELL CULTURE; COMPARATIVE STUDY; LIQUID CHROMATOGRAPHY; METABOLISM; MIDDLE AGED; PROCEDURES; SIGNAL TRANSDUCTION; TRANSPORT AT THE CELLULAR LEVEL;

AGED; BIOLOGICAL TRANSPORT; CELLS, CULTURED; CHROMATOGRAPHY, LIQUID; FEMALE; HEPATOCYTES; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; LIVER; MALE; MEMBRANE PROTEINS; MIDDLE AGED; PROTEOME; PROTEOMICS; QUINOLINES; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

EID: 84938812314     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00334     Document Type: Article

References (58)

1. Drug-Induced Liver Injury: Premarketing Clinical Evaluation; Guidance for Industry; U.S. Food and Drug Administration: Rockville, MD, 2009.
2. Watkins, P. B. Drug safety sciences and the bottleneck in drug development Clin. Pharmacol. Ther. 2011, 89 (6) 788-790 10.1038/clpt.2011.63
3. Berger, D. R.; Ware, B. R.; Davidson, M. D.; Allsup, S. R.; Khetani, S. R. Enhancing the functional maturity of induced pluripotent stem cell-derived human hepatocytes by controlled presentation of cell-cell interactions in vitro Hepatology 2015, 61 (4) 1370-1381 10.1002/hep.27621
4. Chen, Y. F.; Tseng, C. Y.; Wang, H. W.; Kuo, H. C.; Yang, V. W.; Lee, O. K. Rapid generation of mature hepatocyte-like cells from human induced pluripotent stem cells by an efficient three-step protocol Hepatology 2012, 55 (4) 1193-1203 10.1002/hep.24790
5. Baxter, M.; Withey, S.; Harrison, S.; Segeritz, C. P.; Zhang, F.; Atkinson-Dell, R.; Rowe, C.; Gerrard, D. T.; Sison-Young, R.; Jenkins, R.; Henry, J.; Berry, A. A.; Mohamet, L.; Best, M.; Fenwick, S. W.; Malik, H.; Kitteringham, N. R.; Goldring, C. E.; Piper Hanley, K.; Vallier, L.; Hanley, N. A. Phenotypic and functional analyses show stem cell-derived hepatocyte-like cells better mimic fetal rather than adult hepatocytes J. Hepatol. 2015, 62 (3) 581-589 10.1016/j.jhep.2014.10.016
6. Sim, S. C.; Ingelman-Sundberg, M. Pharmacogenomic biomarkers: new tools in current and future drug therapy Trends Pharmacol. Sci. 2011, 32 (2) 72-81 10.1016/j.tips.2010.11.008
7. Beck, M.; Claassen, M.; Aebersold, R. Comprehensive proteomics Curr. Opin. Biotechnol. 2011, 22 (1) 3-8 10.1016/j.copbio.2010.09.002
8. Wisniewski, J. R.; Ostasiewicz, P.; Dus, K.; Zielinska, D. F.; Gnad, F.; Mann, M. Extensive quantitative remodeling of the proteome between normal colon tissue and adenocarcinoma Mol. Syst. Biol. 2012, 8, 611 10.1038/msb.2012.44
9. Wisniewski, J. R.; Hein, M. Y.; Cox, J.; Mann, M. A proteomic ruler for protein copy number and concentration estimation without spike-in standards Mol. Cell. Proteomics 2014, 13 (12) 3497-3506 10.1074/mcp.M113.037309
10. Boess, F.; Kamber, M.; Romer, S.; Gasser, R.; Muller, D.; Albertini, S.; Suter, L. Gene expression in two hepatic cell lines, cultured primary hepatocytes, and liver slices compared to the in vivo liver gene expression in rats: possible implications for toxicogenomics use of in vitro systems Toxicol. Sci. 2003, 73 (2) 386-402 10.1093/toxsci/kfg064
11. Richert, L.; Liguori, M. J.; Abadie, C.; Heyd, B.; Mantion, G.; Halkic, N.; Waring, J. F. Gene expression in human hepatocytes in suspension after isolation is similar to the liver of origin, is not affected by hepatocyte cold storage and cryopreservation, but is strongly changed after hepatocyte plating Drug Metab. Dispos. 2006, 34 (5) 870-879 10.1124/dmd.105.007708
12. Vogel, C.; Marcotte, E. M. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses Nat. Rev. Genet. 2012, 13 (4) 227-232 10.1038/nrg3185
13. Wimmer, H.; Gundacker, N. C.; Griss, J.; Haudek, V. J.; Stattner, S.; Mohr, T.; Zwickl, H.; Paulitschke, V.; Baron, D. M.; Trittner, W.; Kubicek, M.; Bayer, E.; Slany, A.; Gerner, C. Introducing the CPL/MUW proteome database: interpretation of human liver and liver cancer proteome profiles by referring to isolated primary cells Electrophoresis 2009, 30 (12) 2076-2089 10.1002/elps.200900072
14. Rowe, C.; Goldring, C. E.; Kitteringham, N. R.; Jenkins, R. E.; Lane, B. S.; Sanderson, C.; Elliott, V.; Platt, V.; Metcalfe, P.; Park, B. K. Network analysis of primary hepatocyte dedifferentiation using a shotgun proteomics approach J. Proteome Res. 2010, 9 (5) 2658-2668 10.1021/pr1001687
15. Rowe, C.; Gerrard, D. T.; Jenkins, R.; Berry, A.; Durkin, K.; Sundstrom, L.; Goldring, C. E.; Park, B. K.; Kitteringham, N. R.; Hanley, K. P.; Hanley, N. A. Proteome-wide analyses of human hepatocytes during differentiation and dedifferentiation Hepatology 2013, 58 (2) 799-809 10.1002/hep.26414
16. Musallam, L.; Ethier, C.; Haddad, P. S.; Denizeau, F.; Bilodeau, M. Resistance to Fas-induced apoptosis in hepatocytes: role of GSH depletion by cell isolation and culture Am. J. Physiol Gastrointest Liver Physiol 2002, 283 (3) G709-718 10.1152/ajpgi.00013.2002
17. Elaut, G.; Henkens, T.; Papeleu, P.; Snykers, S.; Vinken, M.; Vanhaecke, T.; Rogiers, V. Molecular mechanisms underlying the dedifferentiation process of isolated hepatocytes and their cultures Curr. Drug Metab 2006, 7 (6) 629-660
18. LeCluyse, E. L.; Alexandre, E. Isolation and culture of primary hepatocytes from resected human liver tissue Methods Mol. Biol. 2010, 640, 57-82
19. Wisniewski, J. R. Protocol to enrich and analyze plasma membrane proteins from frozen tissues Methods Mol. Biol. 2008, 432, 175-183 10.1007/978-1-59745-028-7-12
20. Wisniewski, J. R.; Zielinska, D. F.; Mann, M. Comparison of ultrafiltration units for proteomic and N-glycoproteomic analysis by the filter-aided sample preparation method Anal. Biochem. 2011, 410 (2) 307-309 10.1016/j.ab.2010.12.004
21. Wisniewski, J. R.; Zougman, A.; Nagaraj, N.; Mann, M. Universal sample preparation method for proteome analysis Nat. Methods 2009, 6 (5) 359-362 10.1038/nmeth.1322
22. Wisniewski, J. R.; Zougman, A.; Mann, M. Combination of FASP and StageTip-based fractionation allows in-depth analysis of the hippocampal membrane proteome J. Proteome Res. 2009, 8 (12) 5674-5678 10.1021/pr900748n
23. Rappsilber, J.; Ishihama, Y.; Mann, M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics Anal. Chem. 2003, 75 (3) 663-670 10.1021/ac026117i
24. Wisniewski, J. R.; Gaugaz, F. Z. Fast and sensitive total protein and Peptide assays for proteomic analysis Anal. Chem. 2015, 87 (8) 4110-4116 10.1021/ac504689z
25. Cox, J.; Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Nat. Biotechnol. 2008, 26 (12) 1367-1372 10.1038/nbt.1511
26. Wisniewski, J. R.; Rakus, D. Multi-enzyme digestion FASP and the Total Protein Approach-based absolute quantification of the Escherichia coli proteome J. Proteomics 2014, 109C, 322-331 10.1016/j.jprot.2014.07.012
27. Achour, B.; Barber, J.; Rostami-Hodjegan, A. Expression of hepatic drug-metabolizing cytochrome p450 enzymes and their intercorrelations: a meta-analysis Drug Metab. Dispos. 2014, 42 (8) 1349-1356 10.1124/dmd.114.058834
28. Achour, B.; Rostami-Hodjegan, A.; Barber, J. Protein expression of various hepatic uridine 5′-diphosphate glucuronosyltransferase (UGT) enzymes and their inter-correlations: a meta-analysis Biopharm. Drug Dispos. 2014, 35 (6) 353-361 10.1002/bdd.1906
29. Sato, Y.; Nagata, M.; Tetsuka, K.; Tamura, K.; Miyashita, A.; Kawamura, A.; Usui, T. Optimized methods for targeted peptide-based quantification of human uridine 5′-diphosphate-glucuronosyltransferases in biological specimens using liquid chromatography-tandem mass spectrometry Drug Metab. Dispos. 2014, 42 (5) 885-889 10.1124/dmd.113.056291
30. Vildhede, A.; Karlgren, M.; Svedberg, E. K.; Wisniewski, J. R.; Lai, Y.; Noren, A.; Artursson, P. Hepatic uptake of atorvastatin: influence of variability in transporter expression on uptake clearance and drug-drug interactions Drug Metab. Dispos. 2014, 42 (7) 1210-1218 10.1124/dmd.113.056309
31. Karlgren, M.; Vildhede, A.; Norinder, U.; Wisniewski, J. R.; Kimoto, E.; Lai, Y.; Haglund, U.; Artursson, P. Classification of inhibitors of hepatic organic anion transporting polypeptides (OATPs): influence of protein expression on drug-drug interactions J. Med. Chem. 2012, 55 (10) 4740-4763 10.1021/jm300212s
32. Bi, Y. A.; Qiu, X.; Rotter, C. J.; Kimoto, E.; Piotrowski, M.; Varma, M. V.; Ei-Kattan, A. F.; Lai, Y. Quantitative assessment of the contribution of sodium-dependent taurocholate co-transporting polypeptide (NTCP) to the hepatic uptake of rosuvastatin, pitavastatin and fluvastatin Biopharm. Drug Dispos. 2013, 34 (8) 452-461 10.1002/bdd.1861
33. Kimoto, E.; Yoshida, K.; Balogh, L. M.; Bi, Y. A.; Maeda, K.; El-Kattan, A.; Sugiyama, Y.; Lai, Y. Characterization of Organic Anion Transporting Polypeptide (OATP) Expression and Its Functional Contribution to the Uptake of Substrates in Human Hepatocytes Mol. Pharmaceutics 2012, 9 (12) 3535-3542 10.1021/mp300379q
34. Urdzik, J. Colorectal Cancer Liver Metastases: Effects of Chemotherapy on Liver Parenchyma and Resections. Doctoral Thesis (Comprehensive Summary), Uppsala University, Uppsala, Sweden, 2014.
35. Schroder, A.; Klein, K.; Winter, S.; Schwab, M.; Bonin, M.; Zell, A.; Zanger, U. M. Genomics of ADME gene expression: mapping expression quantitative trait loci relevant for absorption, distribution, metabolism and excretion of drugs in human liver Pharmacogenomics J. 2013, 13 (1) 12-20 10.1038/tpj.2011.44
36. Menochet, K.; Kenworthy, K. E.; Houston, J. B.; Galetin, A. Use of mechanistic modeling to assess interindividual variability and interspecies differences in active uptake in human and rat hepatocytes Drug Metab. Dispos. 2012, 40 (9) 1744-1756 10.1124/dmd.112.046193
37. Poirier, A.; Funk, C.; Scherrmann, J. M.; Lave, T. Mechanistic modeling of hepatic transport from cells to whole body: application to napsagatran and fexofenadine Mol. Pharmaceutics 2009, 6 (6) 1716-1733 10.1021/mp8002495
38. Eisenberg, E.; Levanon, E. Y. Human housekeeping genes, revisited Trends Genet. 2013, 29 (10) 569-574 10.1016/j.tig.2013.05.010
39. Wu, L.; Candille, S. I.; Choi, Y.; Xie, D.; Jiang, L.; Li-Pook-Than, J.; Tang, H.; Snyder, M. Variation and genetic control of protein abundance in humans Nature 2013, 499 (7456) 79-82 10.1038/nature12223
40. Chen, R.; Mias, G. I.; Li-Pook-Than, J.; Jiang, L.; Lam, H. Y.; Miriami, E.; Karczewski, K. J.; Hariharan, M.; Dewey, F. E.; Cheng, Y.; Clark, M. J.; Im, H.; Habegger, L.; Balasubramanian, S.; OHuallachain, M.; Dudley, J. T.; Hillenmeyer, S.; Haraksingh, R.; Sharon, D.; Euskirchen, G.; Lacroute, P.; Bettinger, K.; Boyle, A. P.; Kasowski, M.; Grubert, F.; Seki, S.; Garcia, M.; Whirl-Carrillo, M.; Gallardo, M.; Blasco, M. A.; Greenberg, P. L.; Snyder, P.; Klein, T. E.; Altman, R. B.; Butte, A. J.; Ashley, E. A.; Gerstein, M.; Nadeau, K. C.; Tang, H.; Snyder, M. Personal omics profiling reveals dynamic molecular and medical phenotypes Cell 2012, 148 (6) 1293-1307 10.1016/j.cell.2012.02.009
41. Garcea, G.; Gescher, A.; Steward, W.; Dennison, A.; Berry, D. Oxidative stress in humans following the Pringle manoeuvre Hepatobiliary Pancreat Dis Int. 2006, 5 (2) 210-214
42. Halestrap, A. P.; Clarke, S. J.; Javadov, S. A. Mitochondrial permeability transition pore opening during myocardial reperfusion - a target for cardioprotection Cardiovasc. Res. 2004, 61 (3) 372-385 10.1016/S0008-6363(03)00533-9
43. Lin, M. J.; Fine, M.; Lu, J. Y.; Hofmann, S. L.; Frazier, G.; Hilgemann, D. W. Massive palmitoylation-dependent endocytosis during reoxygenation of anoxic cardiac muscle eLife 2013, 2, e01295 10.7554/eLife.01295
44. Hilgemann, D. W.; Fine, M.; Linder, M. E.; Jennings, B. C.; Lin, M. J. Massive endocytosis triggered by surface membrane palmitoylation under mitochondrial control in BHK fibroblasts eLife 2013, 2, e01293 10.7554/eLife.01293
45. Berry, M. N.; Friend, D. S. High-yield preparation of isolated rat liver parenchymal cells: a biochemical and fine structural study J. Cell Biol. 1969, 43 (3) 506-520 10.1083/jcb.43.3.506
46. Kim, J. S.; Qian, T.; Lemasters, J. J. Mitochondrial permeability transition in the switch from necrotic to apoptotic cell death in ischemic rat hepatocytes Gastroenterology 2003, 124 (2) 494-503 10.1053/gast.2003.50059
47. Verma, R.; McDonald, H.; Yates, J. R., 3rd; Deshaies, R. J. Selective degradation of ubiquitinated Sic1 by purified 26S proteasome yields active S phase cyclin-Cdk Mol. Cell 2001, 8 (2) 439-448 10.1016/S1097-2765(01)00308-2
48. Peth, A.; Nathan, J. A.; Goldberg, A. L. The ATP costs and time required to degrade ubiquitinated proteins by the 26 S proteasome J. Biol. Chem. 2013, 288 (40) 29215-29222 10.1074/jbc.M113.482570
49. Jeffers, M.; Taylor, G. A.; Weidner, K. M.; Omura, S.; Vande Woude, G. F. Degradation of the Met tyrosine kinase receptor by the ubiquitin-proteasome pathway Mol. Cell. Biol. 1997, 17 (2) 799-808
50. Strous, G. J.; Govers, R. The ubiquitin-proteasome system and endocytosis J. Cell Sci. 1999, 112 (Pt 10) 1417-1423
51. Seglen, P. O.; Grinde, B.; Solheim, A. E. Inhibition of the lysosomal pathway of protein degradation in isolated rat hepatocytes by ammonia, methylamine, chloroquine and leupeptin Eur. J. Biochem. 1979, 95 (2) 215-225 10.1111/j.1432-1033.1979.tb12956.x
52. Giacomini, K. M.; Huang, S. M.; Tweedie, D. J.; Benet, L. Z.; Brouwer, K. L.; Chu, X.; Dahlin, A.; Evers, R.; Fischer, V.; Hillgren, K. M.; Hoffmaster, K. A.; Ishikawa, T.; Keppler, D.; Kim, R. B.; Lee, C. A.; Niemi, M.; Polli, J. W.; Sugiyama, Y.; Swaan, P. W.; Ware, J. A.; Wright, S. H.; Yee, S. W.; Zamek-Gliszczynski, M. J.; Zhang, L. Membrane transporters in drug development Nat. Rev. Drug Discovery 2010, 9 (3) 215-236 10.1038/nrd3028
53. Bow, D. A.; Perry, J. L.; Miller, D. S.; Pritchard, J. B.; Brouwer, K. L. Localization of P-gp (Abcb1) and Mrp2 (Abcc2) in freshly isolated rat hepatocytes Drug Metab. Dispos. 2007, 36 (1) 198-202 10.1124/dmd.107.018200
54. Roelofsen, H.; Bakker, C. T.; Schoemaker, B.; Heijn, M.; Jansen, P. L.; Oude Elferink, R. P. J. Redistribution of canalicular organic anion transport activity in isolated and cultured rat hepatocytes Hepatology 1995, 21 (6) 1649-1657 10.1002/hep.1840210625
55. Lundquist, P.; Loof, J.; Sohlenius-Sternbeck, A. K.; Floby, E.; Johansson, J.; Bylund, J.; Hoogstraate, J.; Afzelius, L.; Andersson, T. B. The impact of solute carrier (SLC) drug uptake transporter loss in human and rat cryopreserved hepatocytes on clearance predictions Drug Metab. Dispos. 2014, 42 (3) 469-480 10.1124/dmd.113.054676
56. Watanabe, T.; Kusuhara, H.; Maeda, K.; Kanamaru, H.; Saito, Y.; Hu, Z.; Sugiyama, Y. Investigation of the rate-determining process in the hepatic elimination of HMG-CoA reductase inhibitors in rats and humans Drug Metab. Dispos. 2010, 38 (2) 215-222 10.1124/dmd.109.030254
57. Kumar, V.; Prasad, B.; Patilea, G.; Gupta, A.; Salphati, L.; Evers, R.; Hop, C. E.; Unadkat, J. D. Quantitative Transporter Proteomics by LC-MS/MS: Addressing Methodological Issues of Plasma Membrane Isolation and Expression-activity Relationship Drug Metab. Dispos. 2014, 43 (2) 284-288 10.1124/dmd.114.061614
58. Vizcaino, J. A.; Deutsch, E. W.; Wang, R.; Csordas, A.; Reisinger, F.; Rios, D.; Dianes, J. A.; Sun, Z.; Farrah, T.; Bandeira, N.; Binz, P. A.; Xenarios, I.; Eisenacher, M.; Mayer, G.; Gatto, L.; Campos, A.; Chalkley, R. J.; Kraus, H. J.; Albar, J. P.; Martinez-Bartolome, S.; Apweiler, R.; Omenn, G. S.; Martens, L.; Jones, A. R.; Hermjakob, H. ProteomeXchange provides globally coordinated proteomics data submission and dissemination Nat. Biotechnol. 2014, 32 (3) 223-226 10.1038/nbt.2839