Cyclodextrin protects podocytes in diabetic kidney disease

Diabetes

Volumn 62, Issue 11, 2013, Pages 3817-3827

  Merscher Gomez, Sandra ^a   Guzman, Johanna ^a   Pedigo, Christopher E ^a   Lehto, Markku ^b,c   Aguillon Prada, Robier ^a   Mendez, Armando ^a   Lassenius, Mariann I ^b,c   Forsblom, Carol ^b,c   Yoo, Tae Hyun ^a   Villarreal, Rodrigo ^a   Maiguel, Dony ^a   Johnson, Kevin ^a   Goldberg, Ronald ^a   Nair, Viji ^d   Randolph, Ann ^d   Kretzler, Matthias ^d   Nelson, Robert G ^e   Burke III, George W ^a   Groop, Per Henrik ^b,c   Fornoni, Alessia ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b FOLKHÄLSAN INSTITUTE OF GENETICS   (Finland)

^c HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^d UNIVERSITY OF MICHIGAN   (United States)

^e NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 HYDROXYPROPYL BETA CYCLODEXTRIN; 3 HYDROXY 3 METHYLGLUTARYL COENZYME A; ABC TRANSPORTER A1; CREATININE; GLUCOSE; HEMOGLOBIN A1C; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INSULIN; LIPID; LOW DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN RECEPTOR; SIMVASTATIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; ATP BINDING CASSETTE, SUB FAMILY A (ABC1), MEMBER 1 PROTEIN, HUMAN; ATP-BINDING CASSETTE, SUB-FAMILY A (ABC1), MEMBER 1 PROTEIN, HUMAN; CHOLESTEROL; CYCLODEXTRIN; ABCA1 PROTEIN, HUMAN;

ADULT; ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BODY WEIGHT; CELL DAMAGE; CELL PROTECTION; CHOLESTEROL SYNTHESIS; CHOLESTEROL TRANSPORT; CLINICAL ARTICLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DIABETIC KIDNEY DISEASE; DIABETIC NEPHROPATHY; DIABETIC PATIENT; DIET RESTRICTION; DISEASE DURATION; DOWN REGULATION; DRUG EFFICACY; DRUG EXPOSURE; DRUG MEGADOSE; DRUG SAFETY; FEMALE; FOCAL GLOMERULOSCLEROSIS; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INSULIN BLOOD LEVEL; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN TREATMENT; KIDNEY BIOPSY; KIDNEY CORTEX; KIDNEY HYPERTROPHY; KIDNEY MASS; LIPID ANALYSIS; LIPID BLOOD LEVEL; LOW DRUG DOSE; MALE; MEMBRANOUS GLOMERULONEPHRITIS; METABOLIC REGULATION; MIDDLE AGED; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS ISLET; PODOCYTE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; TREATMENT DURATION; ANIMAL; BIOSYNTHESIS; BLOOD; CELL CULTURE; DRUG EFFECT; GLOMERULUS; METABOLISM; MOUSE MUTANT; PATHOLOGY; PATHOPHYSIOLOGY; DRUG EFFECTS;

ADULT; ALBUMINURIA; ANIMALS; ATP BINDING CASSETTE TRANSPORTER 1; CELLS, CULTURED; CHOLESTEROL; CYCLODEXTRINS; DIABETES MELLITUS, TYPE 1; DIABETIC NEPHROPATHIES; DOWN-REGULATION; HUMANS; ISLETS OF LANGERHANS; KIDNEY GLOMERULUS; MALE; MICE; MICE, OBESE; MIDDLE AGED; PODOCYTES;

EID: 84891688019     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-0399     Document Type: Article

References (56)

1. U.S. Renal Data System. USRDS 2011 Annual Data Report: Atlas of Chronic Kidney Disease and End-Stage Renal Disease in the United States. Bethesda, MD, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, 2011
2. Gaede P, Lund-Andersen H, Parving HH, Pedersen O. Effect of a multifactorial intervention on mortality in type 2 diabetes. N Engl J Med 2008; 358:580-591
3. Hovind P, Tarnow L, Rossing K, et al. Decreasing incidence of severe diabetic microangiopathy in type 1 diabetes. Diabetes Care 2003;26:1258- 1264
4. Somlo S, Mundel P. Getting a foothold in nephrotic syndrome. Nat Genet 2000;24:333-335
5. American Diabetes Association. Standards of medical care in diabetes- 2011. Diabetes Care 2011;34(Suppl. 1):S11-S61
6. Fioretto P, Caramori ML, Mauer M. The kidney in diabetes: dynamic pathways of injury and repair. The Camillo Golgi Lecture 2007. Diabetologia 2008;51:1347-1355
7. Steinke JM, Mauer M; International Diabetic Nephropathy Study Group. Lessons learned from studies of the natural history of diabetic nephropathy in young type 1 diabetic patients. Pediatr Endocrinol Rev 2008;5(Suppl. 4):958-963
8. Meyer TW, Bennett PH, Nelson RG. Podocyte number predicts long-term urinary albumin excretion in Pima Indians with type II diabetes and microalbuminuria. Diabetologia 1999;42:1341-1344
9. Pagtalunan ME, Miller PL, Jumping-Eagle S, et al. Podocyte loss and progressive glomerular injury in type II diabetes. J Clin Invest 1997;99:342- 348
10. Steffes MW, Schmidt D, McCrery R, Basgen JM; International Diabetic Nephropathy Study Group. Glomerular cell number in normal subjects and in type 1 diabetic patients. Kidney Int 2001;59:2104-2113
11. Verzola D, Gandolfo MT, Ferrario F, et al. Apoptosis in the kidneys of patients with type II diabetic nephropathy. Kidney Int 2007;72:1262-1272
12. White KE, Bilous RW, Marshall SM, et al. Podocyte number in normotensive type 1 diabetic patients with albuminuria. Diabetes 2002;51:3083-3089
13. Tejada T, Catanuto P, Ijaz A, et al. Failure to phosphorylate AKT in podocytes from mice with early diabetic nephropathy promotes cell death. Kidney Int 2008;73:1385-1393
14. Fornoni A, Sageshima J, Wei C, et al. Rituximab targets podocytes in recurrent focal segmental glomerulosclerosis. Sci Transl Med 2011;3:85ra46
15. Attie AD. ABCA1: at the nexus of cholesterol, HDL and atherosclerosis. Trends Biochem Sci 2007;32:172-179
16. Willer CJ, Sanna S, Jackson AU, et al. Newly identified loci that influence lipid concentrations and risk of coronary artery disease. Nat Genet 2008; 40:161-169
17. Zhou H, Tan KC, Shiu SW, Wong Y. Cellular cholesterol efflux to serum is impaired in diabetic nephropathy. Diabetes Metab Res Rev 2008;24:617-623
18. Tang C, Kanter JE, Bornfeldt KE, Leboeuf RC, Oram JF. Diabetes reduces the cholesterol exporter ABCA1 in mouse macrophages and kidneys. J Lipid Res 2010;51:1719-1728
19. Wang Z, Jiang T, Li J, et al. Regulation of renal lipid metabolism, lipid accumulation, and glomerulosclerosis in FVBdb/db mice with type 2 diabetes. Diabetes 2005;54:2328-2335
20. Proctor G, Jiang T, Iwahashi M, Wang Z, Li J, Levi M. Regulation of renal fatty acid and cholesterol metabolism, inflammation, and fibrosis in Akita and OVE26 mice with type 1 diabetes. Diabetes 2006;55:2502-2509
21. Schaefer EJ, Santos RD, Asztalos BF. Marked HDL deficiency and premature coronary heart disease. Curr Opin Lipidol 2010;21:289-297
22. Katz A, Udata C, Ott E, et al. Safety, pharmacokinetics, and pharmacodynamics of single doses of LXR-623, a novel liver X-receptor agonist, in healthy participants. J Clin Pharmacol 2009;49:643-649
23. Grefhorst A, Elzinga BM, Voshol PJ, et al. Stimulation of lipogenesis by pharmacological activation of the liver X receptor leads to production of large, triglyceride-rich very low density lipoprotein particles. J Biol Chem 2002;277:34182-34190
24. López CA, de Vries AH, Marrink SJ. Molecular mechanism of cyclodextrin mediated cholesterol extraction. PLOS Comput Biol 2011;7:e1002020
25. Christian AE, Haynes MP, Phillips MC, Rothblat GH. Use of cyclodextrins for manipulating cellular cholesterol content. J Lipid Res 1997;38:2264- 2272
26. Stella VJ, He Q. Cyclodextrins. Toxicol Pathol 2008;36:30-42
27. Berthier CC, Zhang H, Schin M, et al. Enhanced expression of Janus kinase-signal transducer and activator of transcription pathway members in human diabetic nephropathy. Diabetes 2009;58:469-477
28. Cohen CD, Frach K, Schlöndorff D, Kretzler M. Quantitative gene expression analysis in renal biopsies: a novel protocol for a high-throughput multicenter application. Kidney Int 2002;61:133-140
29. Lindenmeyer MT, Kretzler M, Boucherot A, et al. Interstitial vascular rarefaction and reduced VEGF-A expression in human diabetic nephropathy. J Am Soc Nephrol 2007;18:1765-1776
30. Johnson WE, Li C, Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 2007;8:118- 127
31. Saeed AI, Bhagabati NK, Braisted JC, et al. TM4 microarray software suite. Methods Enzymol 2006;411:134-193
32. Saeed AI, Sharov V, White J, et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003;34:374- 378
33. Saleem MA, O'Hare MJ, Reiser J, et al. A conditionally immortalized human podocyte cell line demonstrating nephrin and podocin expression. J Am Soc Nephrol 2002;13:630-638
34. Kruth HS. Histochemical detection of esterified cholesterol within human atherosclerotic lesions using the fluorescent probe filipin. Atherosclerosis 1984;51:281-292
35. Mendez AJ. Monensin and brefeldin A inhibit high density lipoproteinmediated cholesterol efflux from cholesterol-enriched cells. Implications for intracellular cholesterol transport. J Biol Chem 1995;270:5891-5900
36. Khera AV, Cuchel M, de la Llera-Moya M, et al. Cholesterol efflux capacity, high-density lipoprotein function, and atherosclerosis. N Engl J Med 2011; 364:127-135
37. Mendez AJ. Cholesterol efflux mediated by apolipoproteins is an active cellular process distinct from efflux mediated by passive diffusion. J Lipid Res 1997;38:1807-1821
38. Fornoni A, Pileggi A, Molano RD, et al. Inhibition of c-jun N terminal kinase (JNK) improves functional beta cell mass in human islets and leads to AKT and glycogen synthase kinase-3 (GSK-3) phosphorylation. Diabetologia 2008;51:298-308
39. Ramirez CM, Liv B, Taylor AM, et al. Weekly cyclodextrin administration normalizes cholesterol metabolism in nearly every organ on the Nieman- Pick Type 1C mouse and markedly prolongs life. Pediatric Res 2010;68: 309-315
40. Takahashi N, Boysen G, Li F, Li Y, Swenberg JA. Tandem mass spectrometry measurements of creatinine in mouse plasma and urine for determining glomerular filtration rate. Kidney Int 2007;71:266-271
41. Doi T, Striker LJ, Quaife C, et al. Progressive glomerulosclerosis develops in transgenic mice chronically expressing growth hormone and growth hormone releasing factor but not in those expressing insulinlike growth factor-1. Am J Pathol 1988;131:398-403
42. Van Rooyen DM, Farrell GC. SREBP-2: a link between insulin resistance, hepatic cholesterol, and inflammation in NASH. J Gastroenterol Hepatol 2011;26:789-792
43. Hudkins KL, Pichaiwong W, Wietecha T, et al. BTBR Ob/Ob mutant mice model progressive diabetic nephropathy. J Am Soc Nephrol 2010;21:1533- 1542
44. Diez-Sampedro A, Lenz O, Fornoni A. Podocytopathy in diabetes: a metabolic and endocrine disorder. Am J Kidney Dis 2011;58:637-646
45. Helfand BT, Mendez MG, Murthy SN, et al. Vimentin organization modulates the formation of lamellipodia. Mol Biol Cell 2011;22:1274-1289
46. Fackler OT, Grosse R. Cell motility through plasma membrane blebbing. J Cell Biol 2008;181:879-884
47. Coleman ML, Sahai EA, Yeo M, Bosch M, Dewar A, Olson MF. Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat Cell Biol 2001;3:339-345
48. Sebbagh M, Renvoizé C, Hamelin J, Riché N, Bertoglio J, Bréard J. Caspase- 3-mediated cleavage of ROCK I induces MLC phosphorylation and apoptotic membrane blebbing. Nat Cell Biol 2001;3:346-352
49. Qi M, Liu Y, Freeman MR, Solomon KR. Cholesterol-regulated stress fiber formation. J Cell Biochem 2009;106:1031-1040
50. Zador IZ, Deshmukh GD, Kunkel R, Johnson K, Radin NS, Shayman JA. A role for glycosphingolipid accumulation in the renal hypertrophy of streptozotocin-induced diabetes mellitus. J Clin Invest 1993;91:797-803
51. Xie X, Brown MS, Shelton JM, Richardson JA, Goldstein JL, Liang G. Amino acid substitution in NPC1 that abolishes cholesterol binding reproduces phenotype of complete NPC1 deficiency in mice. Proc Natl Acad Sci USA 2011;108:15330-15335
52. Tam J, Cinar R, Liu J, et al. Peripheral cannabinoid-1 receptor inverse agonism reduces obesity by reversing leptin resistance. Cell Metab 2012; 16:167-179
53. Maggio AB, Mueller P, Wacker J, et al. Increased pancreatic fat fraction is present in obese adolescents with metabolic syndrome. J Pediatr Gastroenterol Nutr 2012;54:720-726
54. Kruit JK, Wijesekara N, Westwell-Roper C, et al. Loss of both ABCA1 and ABCG1 results in increased disturbances in islet sterol homeostasis, inflammation, and impaired β-cell function. Diabetes 2012;61:659-664
55. Wijesekara N, Zhang LH, Kang MH, et al. miR-33a modulates ABCA1 expression, cholesterol accumulation, and insulin secretion in pancreatic islets. Diabetes 2012;61:653-658
56. Schwartz GG, Olsson AG, Abt M, et al.; dal-OUTCOMES Investigators. Effects of dalcetrapib in patients with a recent acute coronary syndrome. N Engl J Med 2012;367:2089-2099