Magnesium protects against cisplatin-induced acute kidney injury by regulating platinum accumulation

American Journal of Physiology - Renal Physiology

Volumn 307, Issue 4, 2014, Pages

  Solanki, Malvika H ^a,b   Chatterjee, Prodyot K ^b   Gupta, Madhu ^a,b   Xue, Xiangying ^b   Plagov, Andrei ^b   Metz, Margot H ^b   Mintz, Rachel ^b   Singhal, Pravin C ^b,c   Metz, Christine N ^a,b,c  

^a Elmezzi Graduate School of Molecular Medicine   (United States)

^b FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c DONALD AND BARBARA ZUCKER SCHOOL OF MEDICINE AT HOFSTRA NORTHWELL   (United States)

Author keywords

Apoptosis; Hypomagnesemia; Inflammation; Nephrotoxicity; Oxidative stress

Indexed keywords

CISPLATIN; CREATININE; MAGNESIUM; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PLATINUM; PROTEIN P53; STAT3 PROTEIN;

ACUTE KIDNEY FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BREAST CANCER CELL LINE; CANCER PATIENT; CELL KILLING; COMPARATIVE STUDY; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DRUG EFFICACY; DRUG INDUCED DISEASE; DRUG WITHDRAWAL; EPITHELIUM CELL; FEMALE; GENE EXPRESSION; HISTOLOGY; HOMEOSTASIS; HUMAN; IN VITRO STUDY; KIDNEY CELL; KIDNEY INJURY; LUNG CANCER CELL LINE; MAGNESIUM BLOOD LEVEL; MAGNESIUM DEFICIENCY; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OVARIAN CANCER CELL LINE; OXIDATIVE STRESS; PRACTICE GUIDELINE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR CELL; UREA NITROGEN BLOOD LEVEL; VITAMIN SUPPLEMENTATION; WEIGHT REDUCTION; WESTERN BLOTTING;

APOPTOSIS; HYPOMAGNESEMIA; INFLAMMATION; NEPHROTOXICITY; OXIDATIVE STRESS;

ACUTE KIDNEY INJURY; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOOD UREA NITROGEN; CELL LINE, TUMOR; CISPLATIN; CREATININE; CYTOKINES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HUMANS; KIDNEY; LLC-PK1 CELLS; MAGNESIUM; MAGNESIUM DEFICIENCY; MICE; NEUTROPHIL INFILTRATION; OXIDATIVE STRESS; PLATINUM; STAT3 TRANSCRIPTION FACTOR; SWINE;

EID: 84906063720     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00127.2014     Document Type: Article

References (90)

1. Aleksunes LM, Augustine LM, Scheffer GL, Cherrington NJ, Manautou JE. Renal xenobiotic transporters are differentially expressed in mice following cisplatin treatment. Toxicology 250: 82-88, 2008.
2. Anderson S, Eldadah B, Halter JB, Hazzard WR, Himmelfarb J, Horne FM, Kimmel PL, Molitoris BA, Murthy M, O'Hare AM, Schmader KE, High KP. Acute kidney injury in older adults. J Am Soc Nephrol 22: 28-38, 2011.
3. Aoki M, Terada T, Kajiwara M, Ogasawara K, Ikai I, Ogawa O, Katsura T, Inui K. Kidney-specific expression of human organic cation transporter 2 (OCT2/SLC22A2) is regulated by DNA methylation. Am J Physiol Renal Physiol 295: F165-F170, 2008.
4. Arnaud MJ. Update on the assessment of magnesium status. Br J Nutr Suppl 3: S24-S36, 2008.
5. Ashrafi F, Haghshenas S, Nematbakhsh M, Nasri H, Talebi A, Eshraghi-Jazi F, Pezeshki Z, Safari T. The role of magnesium supplementation in cisplatin-induced nephrotoxicity in a rat model: no nephroprotectant effect. Int J Prev Med 3: 637-643, 2012.
6. Blache D, Devaux S, Joubert O, Loreau N, Schneider M, Durand P, Prost M, Gaume V, Adrian M, Laurant P, Berthelot A. Long-term moderate magnesium-deficient diet shows relationships between blood pressure, inflammation and oxidant stress defense in aging rats. Free Radic Biol Med 41: 277-284, 2006.
7. Bodnar L, Wcislo G, Gasowska-Bodnar A, Synowiec A, Szarlej-Wcislo K, Szczylik C. Renal protection with magnesium subcarbonate and magnesium sulphate in patients with epithelial ovarian cancer after cisplatin and paclitaxel chemotherapy: a randomised phase II study. Eur J Cancer 44: 2608-2614, 2008.
8. Brooks C, Wei Q, Cho SG, Dong Z. Regulation of mitochondrial dynamics in acute kidney injury in cell culture and rodent models. J Clin Invest 119: 1275-1285, 2009.
9. Brown RC, Bidlack WR. Dietary magnesium depletion: p-nitroanisole metabolism and glucuronidation in rat hepatocytes and hepatic microsomal membranes. Proc Soc Exp Biol Med 197: 85-90, 1991.
10. Burd I, Breen K, Friedman A, Chai J, Elovitz MA. Magnesium sulfate reduces inflammation-associated brain injury in fetal mice. Am J Obstet Gynecol 202: e291-e299, 2010.
11. Cheng G, Cao Z, Xu X, van Meir EG, Lambeth JD. Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 269: 131-140, 2001.
12. Chirino YI, Pedraza-Chaverri J. Role of oxidative and nitrosative stress in cisplatin-induced nephrotoxicity. Exp Toxicol Pathol 61: 223-242, 2009.
13. Chirino YI, Sanchez-Gonzalez DJ, Martinez-Martinez CM, Cruz C, Pedraza-Chaverri J. Protective effects of apocynin against cisplatininduced oxidative stress and nephrotoxicity. Toxicology 245: 18-23, 2008.
14. Chmielinska JJ, Tejero-Taldo MI, Mak IT, Weglicki WB. Intestinal and cardiac inflammatory response shows enhanced endotoxin receptor (CD14) expression in magnesium deficiency. Mol Cell Biochem 278: 53-57, 2005.
15. Ciarimboli G, Ludwig T, Lang D, Pavenstadt H, Koepsell H, Piechota HJ, Haier J, Jaehde U, Zisowsky J, Schlatter E. Cisplatin nephrotoxicity is critically mediated via the human organic cation transporter 2. Am J Pathol 167: 1477-1484, 2005.
16. Cikos S, Bukovska A, Koppel J. Relative quantification of mRNA: comparison of methods currently used for real-time PCR data analysis. BMC Mol Biol 8: 113, 2007.
17. Cummings BS, Schnellmann RG. Cisplatin-induced renal cell apoptosis: caspase 3-dependent and-independent pathways. J Pharmacol Exp Ther 302: 8-17, 2002.
18. DeHaan RD, Yazlovitskaya EM, Persons DL. Regulation of p53 target gene expression by cisplatin-induced extracellular signal-regulated kinase. Cancer Chemother Pharmacol 48: 383-388, 2001.
19. Dickens BF, Weglicki WB, Li YS, Mak IT. Magnesium deficiency in vitro enhances free radical-induced intracellular oxidation and cytotoxicity in endothelial cells. FEBS Lett 311: 187-191, 1992.
20. Dowling O, Chatterjee PK, Gupta M, Tam Tam HB, Xue X, Lewis D, Rochelson B, Metz CN. Magnesium sulfate reduces bacterial LPS-induced inflammation at the maternal-fetal interface. Placenta 33: 392-398, 2012.
21. Duan W, Yang Y, Yi W, Yan J, Liang Z, Wang N, Li Y, Chen W, Yu S, Jin Z, Yi D. New role of JAK2/STAT3 signaling in endothelial cell oxidative stress injury and protective effect of melatonin. PLOS ONE 8: e57941, 2013.
22. Durlach J, Bac P, Durlach V, Rayssiguier Y, Bara M, Guiet-Bara A. Magnesium status and ageing: an update. Magnes Res 11: 25-42, 1998.
23. Einhorn LH. Treatment of testicular cancer: a new and improved model. J Clin Oncol 8: 1777-1781, 1990.
24. Eruslanov E, Kusmartsev S. Identification of ROS using oxidized DCFDA and flow-cytometry. Methods Mol Biol 594: 57-72, 2010.
25. Faubel S, Lewis EC, Reznikov L, Ljubanovic D, Hoke TS, Somerset H, Oh DJ, Lu L, Klein CL, Dinarello CA, Edelstein CL. Cisplatininduced acute renal failure is associated with an increase in the cytokines interleukin (IL)-1β, IL-18, IL-6, and neutrophil infiltration in the kidney. J Pharmacol Exp Ther 322: 8-15, 2007.
26. Fawcett WJ, Haxby EJ, Male DA. Magnesium: physiology and pharmacology. Br J Anaesth 83: 302-320, 1999.
27. Filipski KK, Mathijssen RH, Mikkelsen TS, Schinkel AH, Sparreboom A. Contribution of organic cation transporter 2 (OCT2) to cisplatininduced nephrotoxicity. Clin Pharmacol Ther 86: 396-402, 2009.
28. Franke RM, Kosloske AM, Lancaster CS, Filipski KK, Hu C, Zolk O, Mathijssen RH, Sparreboom A. Influence of Oct1/Oct2-deficiency on cisplatin-induced changes in urinary N-acetyl-β-D-glucosaminidase. Clin Cancer Res 16: 4198-4206, 2010.
29. Freedman AM, Mak IT, Stafford RE, Dickens BF, Cassidy MM, Muesing RA, Weglicki WB. Erythrocytes from magnesium-deficient hamsters display an enhanced susceptibility to oxidative stress. Am J Physiol Cell Physiol 262: C1371-C1375, 1992.
30. Gong H, Amemiya T, Takaya K. Retinal changes in magnesiumdeficient rats. Exp Eye Res 72: 23-32, 2001.
31. Gorboulev V, Ulzheimer JC, Akhoundova A, Ulzheimer-Teuber I, Karbach U, Quester S, Baumann C, Lang F, Busch AE, Koepsell H. Cloning and characterization of two human polyspecific organic cation transporters. DNA Cell Biol 16: 871-881, 1997.
32. 1 cells. J Biol Chem 272: 10408-10413, 1997.
33. Guerrera MP, Volpe SL, Mao JJ. Therapeutic uses of magnesium. Am Fam Physician 80: 157-162, 2009.
34. 1 cell line in studying drug-induced nephrotoxicity. Can J Physiol Pharmacol 88: 448-455, 2010.
35. Hirai S, Kaida S, Ito T, Hasebe S, Ueno M, Udagawa H, Hayashi M. [Magnesium premedication prevents cisplatin-induced nephrotoxicity in patients with esophageal and hypopharyngeal cancer]. Gan To Kagaku Ryoho 40: 743-747, 2013.
36. Ishida S, Lee J, Thiele DJ, Herskowitz I. Uptake of the anticancer drug cisplatin mediated by the copper transporter Ctr1 in yeast and mammals. Proc Natl Acad Sci USA 99: 14298-14302, 2002.
37. Jia Z, Wang N, Aoyagi T, Wang H, Liu H, Yang T. Amelioration of cisplatin nephrotoxicity by genetic or pharmacologic blockade of prostaglandin synthesis. Kidney Int 79: 77-88, 2011.
38. Jo SK, Cho WY, Sung SA, Kim HK, Won NH. MEK inhibitor, U0126, attenuates cisplatin-induced renal injury by decreasing inflammation and apoptosis. Kidney Int 67: 458-466, 2005.
39. Kao MC, Jan WC, Tsai PS, Wang TY, Huang CJ. Magnesium sulfate mitigates lung injury induced by bilateral lower limb ischemia-reperfusion in rats. J Surg Res 171: e97-e106, 2011.
40. Kim HJ, Lee JH, Kim SJ, Oh GS, Moon HD, Kwon KB, Park C, Park BH, Lee HK, Chung SY, Park R, So HS. Roles of NADPH oxidases in cisplatin-induced reactive oxygen species generation and ototoxicity. J Neurosci 30: 3933-3946, 2010.
41. Lajer H, Daugaard G. Cisplatin and hypomagnesemia. Cancer Treat Rev 25: 47-58, 1999.
42. Lajer H, Kristensen M, Hansen HH, Nielsen S, Frokiaer J, Ostergaard LF, Christensen S, Daugaard G, Jonassen TE. Magnesium depletion enhances cisplatin-induced nephrotoxicity. Cancer Chemother Pharmacol 56: 535-542, 2005.
43. Landon CD, Benjamin SE, Ashcraft KA, Dewhirst MW. A role for the copper transporter Ctr1 in the synergistic interaction between hyperthermia and cisplatin treatment. Int J Hyperthermia 29: 528-538, 2013.
44. Liu Y, Webb HK, Fukushima H, Micheli J, Markova S, Olson JL, Kroetz DL. Attenuation of cisplatin-induced renal injury by inhibition of soluble epoxide hydrolase involves nuclear factor kappaB signaling. J Pharmacol Exp Ther 341: 725-734, 2012.
45. Ludwig T, Riethmuller C, Gekle M, Schwerdt G, Oberleithner H. Nephrotoxicity of platinum complexes is related to basolateral organic cation transport. Kidney Int 66: 196-202, 2004.
46. Mahfouz MM, Smith TL, Kummerow FA. Changes of linoleic acid metabolism and cellular phospholipid fatty acid composition in LLC-PK cells cultured at low magnesium concentrations. Biochim Biophys Acta 1006: 70-74, 1989.
47. Malpuech-Brugere C, Nowacki W, Daveau M, Gueux E, Linard C, Rock E, Lebreton J, Mazur A, Rayssiguier Y. Inflammatory response following acute magnesium deficiency in the rat. Biochim Biophys Acta 1501: 91-98, 2000.
48. Malpuech-Brugere C, Nowacki W, Gueux E, Kuryszko J, Rock E, Rayssiguier Y, Mazur A. Accelerated thymus involution in magnesiumdeficient rats is related to enhanced apoptosis and sensitivity to oxidative stress. Br J Nutr 81: 405-411, 1999.
49. Mazur A, Maier JA, Rock E, Gueux E, Nowacki W, Rayssiguier Y. Magnesium and the inflammatory response: potential physiopathological implications. Arch Biochem Biophys 458: 48-56, 2007.
50. Miller RP, Tadagavadi RK, Ramesh G, Reeves WB. Mechanisms of cisplatin nephrotoxicity. Toxins (Basel) 2: 2490-2518, 2010.
51. Muenyi CS, States VA, Masters JH, Fan TW, Helm CW, States JC. Sodium arsenite and hyperthermia modulate cisplatin-DNA damage responses and enhance platinum accumulation in murine metastatic ovarian cancer xenograft after hyperthermic intraperitoneal chemotherapy (HIPEC). J Ovarian Res 4: 9, 2011.
52. Muraki K, Koyama R, Honma Y, Yagishita S, Shukuya T, Ohashi R, Takahashi F, Kido K, Iwakami S, Sasaki S, Iwase A, Takahashi K. Hydration with magnesium and mannitol without furosemide prevents the nephrotoxicity induced by cisplatin and pemetrexed in patients with advanced non-small cell lung cancer. J Thorac Dis 4: 562-568, 2012.
53. Nadler JL, Rude RK. Disorders of magnesium metabolism. Endocrinol Metab Clin North Am 24: 623-641, 1995.
54. Nasulewicz A, Zimowska W, Bayle D, Dzimira S, Madej J, Rayssiguier Y, Opolski A, Mazur A. Changes in gene expression in the lungs of Mg-deficient mice are related to an inflammatory process. Magnes Res 17: 259-263, 2004.
55. Nechemia-Arbely Y, Barkan D, Pizov G, Shriki A, Rose-John S, Galun E, Axelrod JH. IL-6/IL-6R axis plays a critical role in acute kidney injury. J Am Soc Nephrol 19: 1106-1115, 2008.
56. Nielsen FH. Magnesium, inflammation, and obesity in chronic disease. Nutr Rev 68: 333-340, 2010.
57. Pabla N, Dong Z. Cisplatin nephrotoxicity: mechanisms and renoprotective strategies. Kidney Int 73: 994-1007, 2008.
58. Pabla N, Murphy RF, Liu K, Dong Z. The copper transporter Ctr1 contributes to cisplatin uptake by renal tubular cells during cisplatin nephrotoxicity. Am J Physiol Renal Physiol 296: F505-F511, 2009.
59. Pan H, Shen Z, Mukhopadhyay P, Wang H, Pacher P, Qin X, Gao B. Anaphylatoxin C5a contributes to the pathogenesis of cisplatin-induced nephrotoxicity. Am J Physiol Renal Physiol 296: F496-F504, 2009.
60. Persons DL, Yazlovitskaya EM, Pelling JC. Effect of extracellular signal-regulated kinase on p53 accumulation in response to cisplatin. J Biol Chem 275: 35778-35785, 2000.
61. Polycarpe E, Arnould L, Schmitt E, Duvillard L, Ferrant E, Isambert N, Duvillard C, Beltramo JL, Chevet D, Chauffert B. Low urine osmolarity as a determinant of cisplatin-induced nephrotoxicity. Int J Cancer 111: 131-137, 2004.
62. Qiao X, Chen X, Wu D, Ding R, Wang J, Hong Q, Shi S, Li J, Xie Y, Lu Y, Wang Z. Mitochondrial pathway is responsible for aging-related increase of tubular cell apoptosis in renal ischemia/reperfusion injury. J Gerontol A Biol Sci Med Sci 60: 830-839, 2005.
63. Rayssiguier Y, Gueux E, Bussiere L, Durlach J, Mazur A. Dietary magnesium affects susceptibility of lipoproteins and tissues to peroxidation in rats. J Am Coll Nutr 12: 133-137, 1993.
64. Rayssiguier Y, Gueux E, Weiser D. Effect of magnesium deficiency on lipid metabolism in rats fed a high carbohydrate diet. J Nutr 111: 1876-1883, 1981.
65. Repetto G, del Peso A, Zurita JL. Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat Protoc 3: 1125-1131, 2009.
66. Rock E, Astier C, Lab C, Vignon X, Gueux E, Motta C, Rayssiguier Y. Dietary magnesium deficiency in rats enhances free radical production in skeletal muscle. J Nutr 125: 1205-1210, 1995.
67. Romani AM. Cellular magnesium homeostasis. Arch Biochem Biophys 512: 1-23, 2011.
68. Rosanoff A, Weaver CM, Rude RK. Suboptimal magnesium status in the United States: are the health consequences underestimated? Nutr Rev 70: 153-164, 2012.
69. Sanchez-Gonzalez PD, Lopez-Hernandez FJ, Lopez-Novoa JM, Morales AI. An integrative view of the pathophysiological events leading to cisplatin nephrotoxicity. Crit Rev Toxicol 41: 803-821, 2011.
70. Sarafian TA, Montes C, Imura T, Qi J, Coppola G, Geschwind DH, Sofroniew MV. Disruption of astrocyte STAT3 signaling decreases mitochondrial function and increases oxidative stress in vitro. PLOS ONE 5: e9532, 2010.
71. Sartori S, Nielsen I, Tassinari D, Rigolin F, Arcudi D, Abbasciano V. Changes in intracellular magnesium concentrations during cisplatin chemotherapy. Oncology 50: 230-234, 1993.
72. Scanlan BJ, Tuft B, Elfrey JE, Smith A, Zhao A, Morimoto M, Chmielinska JJ, Tejero-Taldo MI, Mak Iu T, Weglicki WB, Shea-Donohue T. Intestinal inflammation caused by magnesium deficiency alters basal and oxidative stress-induced intestinal function. Mol Cell Biochem 306: 59-69, 2007.
73. Schmitt R, Cantley LG. The impact of aging on kidney repair. Am J Physiol Renal Physiol 294: F1265-F1272, 2008.
74. Schneider V, Krieger ML, Bendas G, Jaehde U, Kalayda GV. Contribution of intracellular ATP to cisplatin resistance of tumor cells. J Biol Inorg Chem 18: 165-174, 2013.
75. 1 cells that co-express human OATP1B1 (OATP-C) and MRP2. Biochem Pharmacol 69: 415-423, 2005.
76. Standley CA, Cotton DB. Brain ionized magnesium and calcium levels during magnesium supplementation and deficiency in female Long-Evans rats. Obstet Gynecol 88: 184-188, 1996.
77. Sweet DH, Pritchard JB. The molecular biology of renal organic anion and organic cation transporters. Cell Biochem Biophys 31: 89-118, 1999.
78. Tam Tam HB, Dowling O, Xue X, Lewis D, Rochelson B, Metz CN. Magnesium sulfate ameliorates maternal and fetal inflammation in a rat model of maternal infection. Am J Obstet Gynecol 204: e361-e368, 2011.
79. 2+ deficiency induces cardiac apoptosis in the rat heart. Magnes Res 20: 208-212, 2007.
80. Teres S, Barcelo-Coblijn G, Benet M, Alvarez R, Bressani R, Halver JE, Escriba PV. Oleic acid content is responsible for the reduction in blood pressure induced by olive oil. Proc Natl Acad Sci USA 105: 13811-13816, 2008.
81. Tongyai S, Rayssiguier Y, Motta C, Gueux E, Maurois P, Heaton FW. Mechanism of increased erythrocyte membrane fluidity during magnesium deficiency in weanling rats. Am J Physiol Cell Physiol 257: C270-C276, 1989.
82. Vaquero MP. Magnesium and trace elements in the elderly: intake, status and recommendations. J Nutr Health Aging 6: 147-153, 2002.
83. Wang X, Martindale JL, Holbrook NJ. Requirement for ERK activation in cisplatin-induced apoptosis. J Biol Chem 275: 39435-39443, 2000.
84. Weglicki WB, Phillips TM, Freedman AM, Cassidy MM, Dickens BF. Magnesium-deficiency elevates circulating levels of inflammatory cytokines and endothelin. Mol Cell Biochem 110: 169-173, 1992.
85. Wei Q, Dong G, Yang T, Megyesi J, Price PM, Dong Z. Activation and involvement of p53 in cisplatin-induced nephrotoxicity. Am J Physiol Renal Physiol 293: F1282-F1291, 2007.
86. Weinstein JR, Anderson S. The aging kidney: physiological changes. Adv Chronic Kidney Dis 17: 302-307, 2010.
87. Willox JC, McAllister EJ, Sangster G, Kaye SB. Effects of magnesium supplementation in testicular cancer patients receiving cis-platin: a randomised trial. Br J Cancer 54: 19-23, 1986.
88. Wolf FI, Cittadini AR, Maier JA. Magnesium and tumors: ally or foe? Cancer Treat Rev 35: 378-382, 2009.
89. Wolf FI, Trapani V, Simonacci M, Ferre S, Maier JA. Magnesium deficiency and endothelial dysfunction: is oxidative stress involved? Magnes Res 21: 58-64, 2008.
90. Yokoo K, Murakami R, Matsuzaki T, Yoshitome K, Hamada A, Saito H. Enhanced renal accumulation of cisplatin via renal organic cation transporter deteriorates acute kidney injury in hypomagnesemic rats. Clin Exp Nephrol 13: 578-584, 2009.