Use of Animal Models of Human Disease for Nonclinical Safety Assessment of Novel Pharmaceuticals

Toxicologic Pathology

Volumn 41, Issue 3, 2013, Pages 508-518

  Morgan, Sherry J ^a   Elangbam, Chandikumar S ^b   Berens, Shawn ^c   Janovitz, Evan ^d   Vitsky, Allison ^e   Zabka, Tanja ^f   Conour, Laura ^g  

^a ABBOTT LABORATORIES   (United States)

^b GLAXOSMITHKLINE   (United States)

^c ALLERGAN INC   (United States)

^d BRISTOL MYERS SQUIBB   (United States)

^e PFIZER INC   (United States)

^f GENENTECH INC   (United States)

^g PRINCETON UNIVERSITY   (United States)

Author keywords

animal models; drug development; pharmaceutical development products; preclinical research development; preclinical safety assessment risk management; safety assessment; transgenic animals

Indexed keywords

ANIMAL MODEL; ARTICLE; DRUG EFFICACY; DRUG MECHANISM; DRUG RESEARCH; DRUG SAFETY; DRUG SCREENING; DRUG SENSITIVITY; LIFESPAN; NONHUMAN; PRACTICE GUIDELINE; PRIORITY JOURNAL; RISK MANAGEMENT; TOXICITY TESTING;

ANIMALS; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; HUMANS; MICE; RATS; RISK ASSESSMENT; TOXICITY TESTS;

ANIMALIA; RODENTIA;

EID: 84875834498     PISSN: 01926233     EISSN: 15331601     Source Type: Journal    
DOI: 10.1177/0192623312457273     Document Type: Article

References (60)

1. A.A.A., Bijvoet, H., Van Hirtum, M., Vermey, D., Van Leenen, A.T., Ven Der Ploeg, W.J., Mooi, A.J., Reuser, Pathological features of glycogen storage disease type II highlighted in the knockout mouse model, J Path, (1999), 189, 416-424
2. Boelsterli U. A. (2003). Animal models of human disease in drug safety testing. J Toxicol Sci 28, 109–21.
3. Bolon B. Galbreith E. (2002). Use of genetically engineered mice in drug discovery and development: Wielding Occam’s razor to prune the product portfolio. Int J Toxicol 21, 55–64.
4. Brayton C. F. Treuting P. M. Ward J. M. (2012). Pathobiology of aging mice and GEM: Background strains and experimental design. Vet Path 49, 85–105.
5. Buchweitz J. P. Ganey P. E. Bursian S. J. Roth R. A. (2003). Underlying endotoxemia augments toxic responses to chloropromazine: Is there a relationship to drug idiosyncrasy? J Pharmacol Exp Ther 300, 460–67.
6. Bussiere J. L. Martin P. Horner M. Couch J. Flaherty M. Andrews L. Beyer J. Horvath C. (2009). Alternative strategies for toxicity testing of species-specific biopharmaceuticals. Int J Tox 28, 230–53.
7. R.M., Cabral, E., Branco, M.M.S., Rizzo, G.J., Ferreira, G.B., Gregores, V.Y., Samoto, N.J., Stopiglia, P.C., Maioka, E.T., Fioretto, V.L., Capelozzi, J.B., Borges, S., Gomes, M.A., Miglino, Cell therapy for fibrotic interstitial pulmonary disease: Experimental study, Microsc Res Tech, (2011), 74, 957-962
8. Chen T. (2010). FDA Perspective on Preclinical Animal POC & Safety Studies for Stem Cell Based Therapy. International Society for Cellular Therapy. San Francisco, CA. Available at: http://www.celltherapysociety.org/uploads/files/Translation%20Meeting/Chen_presentation.pdf.
9. Chen X. Stern D. Yan S. D. (2006). Mitochondrial dysfunction and Alzheimer’s disease. Curr Alzheimer’s Res 3, 515–20.
10. Cheung C. Akiyama T. E. Ward J. M. Nicol C. J. Feigembaum L. Vinson C. Gonzalez F. J. (2004). Diminished hepatocellular proliferation in mice humanized for the nuclear receptor peroxisome proliferator-activated receptor-α. Cancer Res 64, 3849–54.
11. Clark J. B. Palmer C. J. Shaw W. N. (1983). The diabetic Zucker Fatty rat. Proc Soc Exp Biol Med 173, 68–75.
12. Cordaro C. J. (1989). Transgenic mice as future tools in risk assessment. Risk Analysis 9, 157–68.
13. Cure P. Pileggi A. Alejandro R. (2008). Exenatide and rare adverse events. NEJM 358, 1969–70.
14. Davidson D. J. Rolfe M. (2001). Mouse models of cystic fibrosis. Trends Genet 17, S29–37.
15. EMEA (2009). European Medicines Evaluation Agency. ICH Topic M 3 (R2) Non-Clinical Safety Studies for the Conduct of Human Clinical Trials and Marketing Authorization for Pharmaceuticals. Committee for Medicinal Products for Human Use (CHMP). CPMP/ICH/286/95.
16. EMEA (2010). European Medicines Evaluation Agency. Committee for Medicinal Products for Human Use (CHMP). Reflection paper on non-clinical evaluation of drug-induced liver injury (DILI). EMEA/CHMP/SWP/150115/2006.
17. EMEA (2011). European Medicines Evaluation Agency. ICH guideline S6 (R1)—Preclinical safety evaluation of biotechnology-derived pharmaceuticals. EMA/CHMP/ICH/731268/1998.
18. Gieselmann V. (2007). Sphingolipids in physiology and pathophysiology. Acta Paed 96, 39.
19. Hard G. C. Johnson K. J. Cohen S. M. (2009). A comparison of rat chronic progressive nephropathy with human renal disease—Implications for human risk assessment. Crit Rev in Toxicol 39, 332–46.
20. Hard G. C. Khan K. N. (2004). A contemporary overview of chronic progressive nephropathy in the laboratory rat, and its significance for human risk assessment. Toxicol Pathol 32, 171–180.
21. Haskins M. E. (2007). Animal models for mucopolysaccharidosis disorders and their clinical relevance. Acta Paed 96, 56–62.
22. Health Canada. (2004). Recommendations from the Scientific Advisory Panel Sub-groups on Hepatotoxicity: Hepatotoxicity of Health Products. Document Number OoS 01; Version 6; Issue Date July 26, 2004.
23. Horinouchi K. Erlich S. Perl D. P. Ferlinz K. Bisgaier C. L. Sandhoff K. Desnick R. J. Stewart C. L. Schuchman E. H. (1995). Acid sphingomyelinase deficient mice: A model of types A and B Niemann-Pick disease. Nat Genet 10, 288–93.
24. Ionescu E. Sauter J. F. Jeanrenaud B. (1985). Abnormal oral glucose torelance in genetically obese (fa/fa) rats. Am J Physiol 248, E500–6.
25. Iyanagi T. Watanable T. Uchiyama Y. (1989). The 3-methylcholanthrene-inducible UDP-glucuronosyltransferase deficiency in the hyperbilirubinemic rat (Gunn rat) is caused by a –1 frameshift mutation. J Biol Chem 264, 31302–307.
26. S.S.J., Janssen, G.G.M., Martens, C.C.J.F., Sweep, H.A., Ross, A.A.M.M., Hermus, In Zucker Diabetic Fatty rats plasma leptin levels are correlated with plasma insulin levels rather than with body weight, Horm Metab Res, (1999), 31, 610-615
27. Jay G. W. Dermattos R. B. Weinstein E. J. Philbert M. A. Pardo I. D. Brown T. P. (2011). Animal models for Neural Diseases. Toxicol Pathol 39, 167–69.
28. Johnson-Wood K. Lee M. Motter R. Hu K. Gordon G. Barbour R. Khan K. Gordon M. Tan H. Games D. Lieberburg I. Schenk D. Seubert P. McConlogue L. (1997). Amyloid precursor protein processing and Ab42 deposition in a transgenic mouse model of Alzheimer disease. Proc Natl Acad Sci 18, 11550–555.
29. Kasiske B. L. O’Donnell M. P. Keane W. F. (1992). The Zucker rat model of obesity, insulin resistance, hyperlipidemia, and renal injury. Hypertension 19, I110–15.
30. Kempf D. J. Waring J. F. Morfitt D. C. Werner P. Ebert B. Mitten M. Nguyen B. Randolph J. T. DeGoey D. A. Klein L. L. Marsh K. M. (2006). Preclinical model for assessing the potential for unconjugated hyperbilirubinemia produced by human immunodeficiency virus protease inhibitors. Antimicrob Agents Chemother 50, 262–764.
31. Kurtz T. W. Morris R. C. Pershadsingh H. A. (1989). The Zucker fatty rat as a genetic model of obesity and hypertension. Hypertension 13, 896–901.
32. Lewis J. Dickson D. W. Lin W. L. Chisholm L. Corral A. Jones G. Yen S. H. Sahara N. Skipper L. Yager D. Eckman C. Hardy J. Hutton M. McGowan E. (2001). Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 293, 1487–491.
33. Luyendyk J. P. Maddox J. F. Cosma G. N. Ganey P. E. Cockerell G. L. Roth R. A. (2003). Modest inflammation renders ranitidine hepatotoxic. Is there a relationship to drug idiosyncrasy? Toxicol Sci 72, 202.
34. J.J.R., Nicholl, D., Wilkinson, C., Holmes, P., Steart, H., Markham, R.O., Weller, Neuropathology of human Alzheimer’s disease after immunization with amyloid β-peptide: A case report, Nature Med, (2003), 9, 448-452
35. Oddo S. Caccamo A. Shepherd J. D. Murphy M. P. Golde T. E. Kayed R. Metherate R. Mattson M. P. Akbari Y. LaFerla F. M. (2003). Triple transgenic model of Alzheimer’s disease with plaques and tangles: Intracellular AB and synaptic dysfunction. Neuron 39, 409–21.
36. D.T., Odom, R.D., Dowell, E.S., Jacobsen, W., Gordon, T.W., Danford, K.D., MacIssac, A., Rolfe, C.M., Conboy, D.K., Gifford, E., Fraenkel, Tissue-specific transcriptional regulation has diverged significantly between human and mouse, Nat Genet, (2007), 39, 730-732
37. Ohshima T. Murray G. J. Swaim W. D. Longenecker G. Quirk J. M. Cardarelli C. O. Sugimoto Y. Pastan I. Gottesman M. M. Brady R. O. Kulkarni A. B. (1997). α-Galactosidase A deficient mice: A model of Fabry disease. Proc Natl Acad Sci USA 94, 2540–44.
38. Olson H. Betton G. Robinson D. Thomas K. Monro A. Kolaja G. Lilly P. Sanders J. Sipes G. Bracken W. Dorato M. Van Deun K. Smith P. Berger B. Heller A. (2000). Concordance of the toxicity of pharmaceuticals in humans and in animals. Reg Tox Pharm 32, 56–67.
39. Ozaki K. Sano T. Tsuji N. Matsuura T. Narama I. (2010). Insulin-induced hypoglycemic peripheral motor neuropathy in spontaneously diabetic WBN/Kob rats. Comp Med 60, 282–87.
40. Palm M. (1998). The incidence of chronic progressive nephrosis in young Sprague-Dawley rats from two different breeders. Lab Anim 32, 477–82.
41. Quimby F. W. (2002). Animal models in biomedical research. In Laboratory Animal Medicine, 2nd edition (Fox J. G. Anderson L. C. Loew F. M. Quimby F. W., eds.), pp. 1185–1214. Academic Press, San Diego, CA.
42. Racusen L. C. Prozialeck D. H. Solez K. (1984). Glomerular epithelial cell changes after ischemia or dehydration: Possible role of angiotensin II. Am J Pathol 114, 157–63.
43. Rojo L. E. Fernandez J. A. Macchioni A. A. Jiminez J. M. Macchioni R. B. (2008). Neuroinflammation: Implications for the pathogenesis and molecular diagnosis of Alzheimer’s disease. Arch Med Res 39, 1–16.
44. Roth R. A. Harkema J. R. Pestka J. P. Ganey P. E. (1997). Is exposure to bacterial endotoxin a determinant of susceptibility to intoxication from xenobiotic agents? Toxicol Appl Pharmacol 147, 300–11.
45. Shively C. A. Clarkson T. B. (2009). The unique value of primate models in translational research. Am J Primatol 71, 715–21.
46. Smith E. L. Schuchman E. H. (2008). The unexpected role of acid sphingomyelinase in cell death and the pathophysiology of common diseases. FASEB 22, 3419–3431.
47. Tabata H. (2000). Peripheral neuropathy in B6C3F1 mice and SD rats induced by chronic intermittent insulin hypoglycemia. Drug Chem Toxicol 23, 485–96.
48. Tatarkiewicz K. Smith P. Sablan E. Polizzi C. Aumann D. Villescaz C. Hargrove D. Gedulin B. Lu M. Adams L. Whisenant T. Roy D. Parkes D. (2010). Exenatide does not evoke pancreatitis and attenuates chemically induced pancreatitis in normal and diabetic rodents. Amer J Physiol Endocrinol Metab 299, E1076–1086.
49. Thiele D. L. (2007). Immunological mechanisms in drug-induced liver injury. In Drug-Induced Liver Disease, 2nd ed. (Kaplowitz N. DeLeve L. D., eds.), chap. 7 pp. 115–123. Informa Health Care, New York, NY.
50. Tokuyama Y. Sturis J. DePaoli A. M. Takeda J. Stoffel M. Tang J. Sun X. Polonsky K. S. Bell G. I. (1995). Evolution of beta cell dysfunction in the male Zucker Diabetic Fatty rat. Diabetes 44, 1447–457.
51. Travlos G. S. Betz L. Hard G. C. (2007). Influence of diet or route of exposure on chronic progressive nephropathy, kidney weight, blood urea nitrogen and creatinine concentrations in 13-week toxicity studies for control F344/N male rats [abstract]. Toxicol Pathol 35, 190–91.
52. Treuting P. M. Clifford C. B. Sellers R. S. Brayton C. F. (2012). Of mice and microflora: Considerations for genetically engineered mice. Vet Path 49, 44–63.
53. Trevisan A. Nicolli A. Chiara F. (2010). Are rats the appropriate experimental model to understand age-related renal drug metabolism and toxicity? Expert Opin Drug Metab Toxicol 6, 1451–59.
54. U.S. FDA (2009a). U.S. Food and Drug Administration. Center for Drug Evaluation and Research (CDER) and Center for Biologics Evaluation and Research (CBER). Guidance for Industry: Animal Models—Essential Elements to Address Efficacy under the Animal Rule (draft). http://www.fda.gov/cber/guidelines.htm.
55. U.S. FDA (2009b). U.S. Food and Drug Administration. Center for Drug Evaluation and Research (CDER). Guidance for Industry: Drug-Induced Liver Injury (DILI)—Premarketing Clinical Evaluation. http://www.fda.gov/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/default.htm.
56. Valentine J. L. Lee S. Seaton M. J. Asgharian B. Farris G. Corton J. C. Gonzalez F. J. Medinsky M. A. (1996). Reduction of benzene metabolism and toxicity in mice that lack CYP2E1 expression. Tox Appl Pharmacol 141, 205–213.
57. Vitsky A. Hayes M. Ewing P. Ryan S. Murray J. Nickerson C. Andrews L. Thurberg B. L. (2006). Dose-responsive toxicologic pathology following administration of recombinant human acid sphingomyelinase to acid sphingomyelinase knockout mice. Abstr ACVP Meeting, Vet Path 43, 853.
58. Wong P. C. Cai H. Borchelt D. R. Price D. L. (2002). Genetically engineered mouse models of neurodegenerative diseases. Nat Neurosci 5, 633–639.
59. Xu Y. Quinn B. Witte D. Grabowski G. A. (2003). Viable mouse models of acid α-glucosidase Deficiency. Am J Path 163, 2093–2101.
60. Zeiss C. J. Ward J. M. Allore H. G. (2012). Designing phenotyping studies for genetically engineered mice. Vet Path 49, 24–31.