Phospholipidosis in Rats Treated with Amiodarone: Serum Biochemistry and Whole Genome Micro-Array Analysis Supporting the Lipid Traffic Jam Hypothesis and the Subsequent Rise of the Biomarker BMP

Toxicologic Pathology

Volumn 40, Issue 3, 2012, Pages 491-503

  Mesens, Natalie ^a   Desmidt, Miek ^a   Verheyen, Geert R ^a   Starckx, Sofie ^a   Damsch, Siegrid ^a   Vries, Ronald de ^a   Verhemeldonck, Marc ^a   Gompel, Jacky Van ^a   Lampo, Ann ^a   Lammens, Lieve ^a  

^a JANSSEN RESEARCH FOUNDATION   (Belgium)

Author keywords

biomarkers; drug development; mechanisms of toxicity; molecular pathology; rodent pathology; toxicogenomics

Indexed keywords

ALANINE AMINOTRANSFERASE; AMIODARONE; ASPARTATE AMINOTRANSFERASE; BIOLOGICAL MARKER; BIS(MONOACYLGLYCEROL)PHOSPHATE; CHOLESTEROL; GLYCEROPHOSPHOLIPID; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PHOSPHATE; PHOSPHOLIPID; UNCLASSIFIED DRUG; DIDOCOSAHEXAENOYL BIS(MONOACYLGLYCEROL) PHOSPHATE; LYSOPHOSPHOLIPID;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BLOOD ANALYSIS; CELL MEMBRANE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOSOME; HISTOPATHOLOGY; LIPIDOSIS; LIVER; LUNG; MALE; MICROARRAY ANALYSIS; MOLECULAR PATHOLOGY; NIEMANN PICK DISEASE; NONHUMAN; ORGAN WEIGHT; PHOSPHOLIPID BLOOD LEVEL; PHOSPHOLIPID METABOLISM; PRIORITY JOURNAL; RAT; SERUM; SPLEEN; TRANSMISSION ELECTRON MICROSCOPY; URINALYSIS; URINE; WHOLE GENOME MICROARRAY ANALYSIS; ANIMAL; BLOOD; CHEMICALLY INDUCED DISORDER; DNA MICROARRAY; DRUG EFFECT; GENE EXPRESSION REGULATION; LIPID METABOLISM; LYMPHOCYTE; METABOLISM; ORGAN SIZE; PATHOLOGY; SPRAGUE DAWLEY RAT; TOXICOGENETICS;

AMIODARONE; ANIMALS; BIOLOGICAL MARKERS; CHOLESTEROL; GENE EXPRESSION REGULATION; GLYCEROPHOSPHOLIPIDS; LIPID METABOLISM; LIPIDOSES; LIVER; LUNG; LYMPHOCYTES; LYSOPHOSPHOLIPIDS; MALE; METABOLIC NETWORKS AND PATHWAYS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SIZE; PHOSPHOLIPIDS; RATS; RATS, SPRAGUE-DAWLEY; SPLEEN; TOXICOGENETICS;

EID: 84865162377     PISSN: 01926233     EISSN: 15331601     Source Type: Journal    
DOI: 10.1177/0192623311432290     Document Type: Article

References (37)

1. Abdul-Hammed M. Breiden B. Adebayo M. A. Babalola J. O. Schwarzmann G. Sandhoff K. (2010). Role of endosomal membrane lipids and NPC2 in cholesterol transfer and membrane fusion. J Lipid Res 51, 1747–60.
2. Baronas E. T. Lee J. W. Alden C. Hsieh F. Y. (2007). Biomarkers to monitor drug-induced phospholipidosis. Toxicol Appl Pharmacol 218, 72–8.
3. Beltroy E. P. Liu B. Dietschy J. M. Turley S. D. (2007). Lysosomal unesterified cholesterol content correlates with liver cell death in murine Niemann-Pick type C disease. J Lipid Res 48, 869–81.
4. Chatman L. A. Morton D. Johnson T. O. Anway S. D. (2009). A strategy for risk management of drug-induced phospholipidosis. Toxicol Pathol 37, 997–1005.
5. De Duve C. (1968). The Interaction of Drugs and Subcellular Components in Animal Cells. Little, Brown, Boston, MA.
6. Goldman I. S. Winkler M. L. Raper S. E. Barker M. E. Keung E. Goldberg H. I. Boyer T. D. (1985). Increased hepatic density and phospholipidosis due to amiodarone. Am J Roentgenol 144, 541–6.
7. Guigui B. Perrot S. Berry J. P. Fleury-Feith J. Martin N. Métreau J. M. Dhumeaux D. Zafrani E. S. (1988). Amiodarone-induced hepatic phospholipidosis: A morphological alteration independent of pseudoalcoholic liver disease. Hepatology 8, 1063–8.
8. Hein L. Lüllmann-Rauch R. Mohr K. (1990). Human accumulation potential of xenobiotics: Potential of catamphiphilic drugs to promote their accumulation via inducing lipidosis or mucopolysaccharidosis. Xenobiotica 20, 1259–67.
9. Hullin-Matsuda F. Luquain-Costaz C. Bouvier J. Delton-Vandenbroucke I. (2009). Bis(monoacylglycero)phosphate, a peculiar phospholipid to control the fate of cholesterol: Implications in pathology. Prostaglandins Leukot Essent Fatty Acids 81, 313–24.
10. Kannan R. Sarma J. S. Guha M. Venkataraman K. (1991). Amiodarone toxicity. II. Desethylamiodarone-induced phospholipidosis and ultrastructural changes during repeated administration in rats. Fundam Appl Toxicol 16, 103–9.
11. Kobayashi T. Beuchat M. H. Lindsay M. Frias S. Palmiter R. D. Sakuraba H. Parton R. G. Gruenberg J. (1999). Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport. Nat Cell Biol 1, 113–8.
12. Kobayashi T. Stang E. Fang K. S. (1998). A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392, 193–7.
13. Kolter T. Sandhoff K. (2005). Principles of lysosomal membrane digestion: Stimulation of sphingolipid degradation by sphingolipid activator proteins and anionic lysosomal lipids. Annu Rev Cell Dev Biol 21, 81–103.
14. Kolter T. Sandhoff K. (2010). Lysosomal degradation of membrane lipids. FEBS Lett 584, 1700–12.
15. Le Quintrec J. S. Le Quintrec J. L. (1991). Drug-induced myopathies. Baillière’s Clinical Rheumatology 5, 21–38.
16. Lewis J. H. Ranard R. C. Caruso A. Jackson L. K. Mullick F. Ishak K. G. Seeff L. B. Zimmerman H. J. (1988). Amiodarone hepatotoxicity: Prevalence and clinicopathologic correlations among 104 patients. Hepatology 9, 679–85.
17. Liscum L. (2000). Niemann-Pick type C mutations cause lipid traffic jam. Traffic 1, 218–25.
18. Liscum L. Sturley S. L. (2004). Intracellular trafficking of Niemann-Pick C proteins 1 and 2: Obligate components of subcellular lipid transport. Biochim Biophys Acta 1685, 22–7.
19. Lüllmann-Rauch R. (1979). Drug-induced lysosomal storage disorders. Frontiers of Biology 48, 49–130.
20. Lusa S. Blom T. S. Eskelinen E. L. Kuismanen E. Månsson J. E. Simons K. Ikonen E. (2001). Depletion of rafts in late endocytic membranes is controlled by NPC1-dependent recycling of cholesterol to the plasma membrane. J Cell Sci 114, 1893–900.
21. Matsuzawa Y. Yamamoto A. Adachi S. Nishikawa M. (1977). Studies on drug-induced lipidosis. VIII. Correlation between drug accumulation and acidic phospholipids. J Biochem 5, 1369–77.
22. Mesens N. Steemans M. Hansen E. Peeters A. Verheyen G. Vanparys P. (2009). A 96-well flow cytometric screening assay for detecting in vitro phospholipidosis-induction in the drug discovery phase. Toxicol In Vitro 23, 217–26.
23. Mesens N. Steemans M. Hansen E. Verheyen G. R. Van Goethem F. Van Gompel J. (2010). Screening for phospholipidosis induced by central nervous drugs: Comparing the predictivity of an in vitro assay to high throughput in silico assays. Toxicol In Vitro 24, 1417–25.
24. Morelli J. K. Buehrle M. Pognan F. Barone L. R. Fieles W. Ciaccio P. J. (2006). Validation of an in vitro screen for phospholipidosis using a high-content biology platform. Cell Biol Toxicol 22, 15–27.
25. Mortuza G. B. Neville W. A. Delaney J. Waterfield C. J. Camilleri P. (2003). Characterisation of a potential biomarker of phospholipidosis from amiodarone-treated rats. Biochim Biophys Acta 1631, 136–46.
26. Muller P. Y. Dieterle F. (2009). Tissue-specific, non-invasive toxicity biomarkers: Translation from preclinical safety assessment to clinical safety monitoring. Expert Opin Drug Metab Toxicol 5, 1023–38.
27. Nioi P. Perry B. K. Wang E. J. Gy Y. Z. Snyder R. D. (2007). In vitro detection of drug-induced phospholipidosis using gene expression and fluorescent phospholipid based methodologies. Toxicol Sci 99, 162–73.
28. Nonoyama T. Fukuda R. (2008). Drug-induced phospholipidosis—pathological aspects and its prediction. J Toxicol Pathol 21, 9–24.
29. Pospischil A. Walther P. Dingemanse J. (2009). Phospholipidosis in healthy subjects participating in clinical studies: Ultrastructural findings in white blood cells. Exp Toxicol Pathol 10 [Epub ahead of print].
30. Reasor M. J. Hasting K. L. Ulrich R. G. (2006). Drug-induced phospholipidosis: Issues and future directions. Expert Opin Drug Saf 5, 567–83.
31. Reasor M. J. Kacew S. (2001). Drug-induced phospholipidosis: Are there functional consequences? Exp Biol Med 226, 825–30.
32. Reasor M. J. McCloud C. M. Beard T. L. Ebert D. C. Kacew S. Gardner M. F. Aldern K. A. Hostetler K. Y. (1996). Comparative evaluation of amiodarone-induced phospholipidosis and drug accumulation in Fischer-344 and Sprague-Dawley rats. Toxicology 106, 139–47.
33. Rouser G. Kritchevsky G. Knudson A. G. Jr Simon G. (1968). Accumulation of a glycerolphospholipid in classical Niemann-Pick disease. Lipids 3, 287–90.
34. Schulze H. Kolter T. Sandhoff K. (2009). Principles of lysosomal membrane degradation: Cellular topology and biochemistry of lysosomal lipid degradation. Biochim Biophys Acta 1793, 674–83.
35. Tengstrand E. A. Miwa G. T. Hsieh F. Y. (2010). Bis(monoacylglycerol)phosphate as a non-invasive biomarker to monitor the onset and time-course of phospholipidosis with drug-induced toxicities. Expert Opin Drug Metab Toxicol 6, 555–70.
36. Tomizawa K. Sugano K. Jamada H. Horii I. (2006). Physicochemical and cell-based approach for early screening of phospholipidosis-inducing potential. J Toxicol Sci 31, 315–24.
37. Yamamoto A. Adachi S. Kitani T. Shinji Y. Seki K. (1971). Drug-induced lipidosis in human cases and in animal experiments. Accumulation of an acidic glycerophospholipid. J Biochem 69, 613–5.