Glutathione and mitochondria determine acute defense responses and adaptive processes in cadmium-induced oxidative stress and toxicity of the kidney

Archives of Toxicology

Volumn 89, Issue 12, 2015, Pages 2273-2289

  Nair, Ambily Ravindran ^a   Lee, Wing Kee ^b   Smeets, Karen ^a   Swennen, Quirine ^a   Sanchez, Amparo ^a   Thévenod, Frank ^b   Cuypers, Ann ^a  

^a HASSELT UNIVERSITY   (Belgium)

^b UNIVERSITY OF WITTEN HERDECKE   (Germany)

Author keywords

Antioxidative enzymes; Apoptosis; Metallothionein; Mitochondrial DNA content; Oxidative stress

Indexed keywords

ADENOSINE TRIPHOSPHATE; CADMIUM; COMPLEMENTARY DNA; GLUTATHIONE; GLUTATHIONE DISULFIDE; METALLOTHIONEIN I; METALLOTHIONEIN II; MITOCHONDRIAL DNA; MITOFUSIN 2; PEROXIREDOXIN 2; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE; PROTEIN BAX; PROTEIN BCL W; PROTEIN BCL XL; CADMIUM CHLORIDE; CASPASE 3; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOGENESIS; CELL CULTURE; CELL VIABILITY; CONTROLLED STUDY; FEMALE; FISCHER 344 RAT; GENE EXPRESSION; IMMORTALIZED CELL LINE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; MALE; MITOCHONDRION; NEPHROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; URINALYSIS; ANIMAL; CELL LINE; DOSE RESPONSE; DRUG EFFECTS; KIDNEY; METABOLISM; PATHOLOGY; WISTAR KYOTO RAT;

ANIMALS; APOPTOSIS; CADMIUM CHLORIDE; CASPASE 3; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GLUTATHIONE; KIDNEY; KIDNEY TUBULES, PROXIMAL; MALE; MITOCHONDRIA; OXIDATIVE STRESS; RATS; RATS, INBRED F344; RATS, INBRED WKY; REACTIVE OXYGEN SPECIES;

EID: 84949322422     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-014-1401-9     Document Type: Article

References (50)

1. Barbier O, Jacquillet G, Tauc M, Cougnon M, Poujeol P (2005) Effect of heavy metals on, and handling by, the kidney. Nephron Physiol 99(4):105–110
2. Bhat HK, Epelboym I (2004) Quantitative analysis of total mitochondrial DNA: competitive polymerase chain reaction versus real-time polymerase chain reaction. J Biochem Mol Toxicol 18(4):180–186. doi:10.1002/jbt.20024
3. Cadenas E, Davies KJ (2000) Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29(3–4):222–230
4. Cannino G, Ferruggia E, Luparello C, Rinaldi AM (2009) Cadmium and mitochondria. Mitochondrion 9(6):377–384. doi:10.1016/j.mito.2009.08.009
5. Chen Y, Shertzer HG, Schneider SN, Nebert DW, Dalton TP (2005) Glutamate cysteine ligase catalysis: dependence on ATP and modifier subunit for regulation of tissue glutathione levels. J Biol Chem 280(40):33766–33774. doi:10.1074/jbc.M504604200
6. Collino M, Patel NS, Lawrence KM et al (2005) The selective PPARgamma antagonist GW9662 reverses the protection of LPS in a model of renal ischemia-reperfusion. Kidney Int 68(2):529–536. doi:10.1111/j.1523-1755.2005.00430.x
7. Cuypers A, Plusquin M, Remans T et al (2010) Cadmium stress: an oxidative challenge. Biometals 23(5):927–940. doi:10.1007/s10534-010-9329-x
8. de Brito OM, Scorrano L (2008) Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456(7222):605–610. doi:10.1038/nature07534
9. Dikalov S (2011) Cross talk between mitochondria and NADPH oxidases. Free Radic Biol Med 51(7):1289–1301. doi:10.1016/j.freeradbiomed.2011.06.033
10. Gobe G, Crane D (2010) Mitochondria, reactive oxygen species and cadmium toxicity in the kidney. Toxicol Lett 198(1):49–55. doi:10.1016/j.toxlet.2010.04.013
11. Halliwell B (1994) Free radicals, antioxidants, and human disease: curiosity, cause, or consequence? Lancet 344(8924):721–724
12. Handschin C, Spiegelman BM (2006) Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev 27(7):728–735. doi:10.1210/er.2006-0037
13. Hiratsuka H, Katsuta O, Iwata H, Matsumoto J, Umemura T (1993) Acute toxicity of cadmium in rats with or without cadmium pretreatment. J Toxicol Sci 18(3):197–201
14. Jones DP (2006) Redefining oxidative stress. Antioxid Redox Signal 8(9–10):1865–1879. doi:10.1089/ars.2006.8.1865
15. Jones AW, Yao Z, Vicencio JM, Karkucinska-Wieckowska A, Szabadkai G (2012) PGC-1 family coactivators and cell fate: roles in cancer, neurodegeneration, cardiovascular disease and retrograde mitochondria-nucleus signalling. Mitochondrion 12(1):86–99. doi:10.1016/j.mito.2011.09.009
16. Klaassen CD, Liu J, Choudhuri S (1999) Metallothionein: an intracellular protein to protect against cadmium toxicity. Annu Rev Pharmacol Toxicol 39:267–294
17. Lee HC, Yin PH, Lu CY, Chi CW, Wei YH (2000) Increase of mitochondria and mitochondrial DNA in response to oxidative stress in human cells. Biochem J 348(Pt 2):425–432
18. 2+ uniporter. Am J Physiol Renal Physiol 288(1):F27–F39
19. Lee WK, Torchalski B, Thévenod F (2007) Cadmium-induced ceramide formation triggers calpain-dependent apoptosis in cultured kidney proximal tubule cells. Am J Physiol Cell Physiol 293(3):C839–C847
20. Lenaz G (2012) Mitochondria and reactive oxygen species. which role in physiology and pathology? Adv Exp Med Biol 942:93–136. doi:10.1007/978-94-007-2869-1_5
21. L’hoste S, Chargui A, Belfodil R et al (2009) CFTR mediates cadmium-induced apoptosis through modulation of ROS level in mouse proximal tubule cells. Free Radic Biol Med 46:1017–1031
22. Li S, Nagothu KK, Desai V et al (2009) Transgenic expression of proximal tubule peroxisome proliferator-activated receptor-alpha in mice confers protection during acute kidney injury. Kidney Int 76(10):1049–1062. doi:10.1038/ki.2009.330
23. Liesa M, Borda-d’Agua B, Medina-Gomez G et al (2008) Mitochondrial fusion is increased by the nuclear coactivator PGC-1beta. PLoS ONE 3(10):e3613. doi:10.1371/journal.pone.0003613
24. Liu J, Qu W, Kadiiska MB (2009) Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicol Appl Pharmacol 238(3):209–214. doi:10.1016/j.taap.2009.01.029
25. Lowry O, Rosebrough N, Farr A, Randall RJ (1951) Protein measurements with the Folin phenol reagent. J Biol Chem 194:265–275
26. Maret W (2011) Redox biochemistry of mammalian metallothioneins. J Biol Inorg Chem 16(7):1079–1086. doi:10.1007/s00775-011-0800-0
27. Martindale JL, Holbrook NJ (2002) Cellular response to oxidative stress: signaling for suicide and survival. J Cell Physiol 192(1):1–15. doi:10.1002/jcp.10119
28. Mishra P, Chan DC (2014) Mitochondrial dynamics and inheritance during cell division, development and disease. Nat Rev Mol Cell Biol 15(10):634–646. doi:10.1038/nrm3877
29. Nair AR, Degheselle O, Smeets K, Van Kerkhove E, Cuypers A (2013) Cadmium-induced pathologies: where is the oxidative balance lost (or not)? Int J Mol Sci 14(3):6116–6143. doi:10.3390/ijms14036116
30. Nair AR, Smeets K, Keunen E et al (2014) Renal cells exposed to cadmium in vitro and in vivo: normalising gene expression data. J Appl Toxicol (in press) doi:10.1002/jat.3047
31. Orrenius S, Gogvadze V, Zhivotovsky B (2007) Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol 47:143–183. doi:10.1146/annurev.pharmtox.47.120505.105122
32. Owen JB, Butterfield DA (2010) Measurement of oxidized/reduced glutathione ratio. Methods Mol Biol 648:269–277. doi:10.1007/978-1-60761-756-3_18
33. Queval G, Noctor G (2007) A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: application to redox profiling during Arabidopsis rosette development. Anal Biochem 363(1):58–69. doi:10.1016/j.ab.2007.01.005
34. Scarpulla RC (2008) Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev 88(2):611–638. doi:10.1152/physrev.00025.2007
35. Scarpulla RC (2011) Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochim Biophys Acta 1813(7):1269–1278. doi:10.1016/j.bbamcr.2010.09.019
36. Scarpulla RC (2012) Nucleus-encoded regulators of mitochondrial function: integration of respiratory chain expression, nutrient sensing and metabolic stress. Biochim Biophys Acta 1819(9–10):1088–1097. doi:10.1016/j.bbagrm.2011.10.011
37. Singhal RK, Anderson ME, Meister A (1987) Glutathione, a first line of defense against cadmium toxicity. FASEB J 1(3):220–223
38. Sinha K, Das J, Pal PB, Sil PC (2013) Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch Toxicol. doi:10.1007/s00204-013-1034-4
39. Small DM, Morais C, Coombes JS, Bennett NC, Johnson DW, Gobe GC (2014) Oxidative stress-induced alterations in PPARgamma and associated mitochondrial destabilisation contribute to kidney cell apoptosis. Am J Physiol Renal Physiol 307(7):F814–F822. doi:10.1152/ajprenal.00205.2014
40. Taguchi K, Motohashi H, Yamamoto M (2011) Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 16(2):123–140. doi:10.1111/j.1365-2443.2010.01473.x
41. Thévenod F (2010) Catch me if you can! Novel aspects of cadmium transport in mammalian cells. Biometals 23(5):857–875. doi:10.1007/s10534-010-9309-1
42. Thévenod F, Lee WK (2013) Toxicology of cadmium and its damage to Mammalian organs. Met Ions Life Sci 11:415–490. doi:10.1007/978-94-007-5179-8_14
43. Thijssen S, Cuypers A, Maringwa J et al (2007a) Low cadmium exposure triggers a biphasic oxidative stress response in mice kidneys. Toxicology 236(1–2):29–41. doi:10.1016/j.tox.2007.03.022
44. Thijssen S, Maringwa J, Faes C, Lambrichts I, Van Kerkhove E (2007b) Chronic exposure of mice to environmentally relevant, low doses of cadmium leads to early renal damage, not predicted by blood or urine cadmium levels. Toxicology 229(1–2):145–156
45. Trachootham D, Lu W, Ogasawara MA, Nilsa RD, Huang P (2008) Redox regulation of cell survival. Antioxid Redox Signal 10(8):1343–1374. doi:10.1089/ars.2007.1957
46. Wang Y, Fang J, Leonard SS, Rao KM (2004) Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radic Biol Med 36(11):1434–1443
47. Westermann B (2010) Mitochondrial fusion and fission in cell life and death. Nat Rev Mol Cell Biol 11(12):872–884. doi:10.1038/nrm3013
48. Woost PG, Orosz DE, Jin W et al (1996) Immortalization and characterization of proximal tubule cells derived from kidneys of spontaneously hypertensive and normotensive rats. Kidney Int 50(1):125–134
49. Zhan M, Brooks C, Liu F, Sun L, Dong Z (2013) Mitochondrial dynamics: regulatory mechanisms and emerging role in renal pathophysiology. Kidney Int 83(4):568–581. doi:10.1038/ki.2012.441
50. Zorzano A, Liesa M, Sebastian D, Segales J, Palacin M (2010) Mitochondrial fusion proteins: dual regulators of morphology and metabolism. Semin Cell Dev Biol 21(6):566–574. doi:10.1016/j.semcdb.2010.01.002