Podocyte hypertrophy, "adaptation" and "decompensation" associated with glomerular enlargement and glomerulosclerosis in the aging rat: Prevention by calorie restriction

Journal of the American Society of Nephrology

Volumn 16, Issue 10, 2005, Pages 2953-2966

  Wiggins, Jocelyn E ^a   Goyal, Meera ^b   Sanden, Silja K ^b   Wharram, Bryan L ^b   Shedden, Kerby A ^c   Misek, David E ^b   Kuick, Rork D ^b   Wiggins, Roger C ^b,d  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN SCHOOL OF PUBLIC HEALTH   (United States)

^d UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 4; DESMIN; NEPHRIN; PODOCALYXIN; SYNAPSIN I; TRANSCRIPTION FACTOR; VASCULOTROPIN; WT1 PROTEIN;

AGING; ARTICLE; BODY SIZE; CALORIC RESTRICTION; CELL FUNCTION; DISEASE ASSOCIATION; GLOMERULOPATHY; GLOMERULOSCLEROSIS; HYPERPLASIA; HYPERTROPHY; KIDNEY FUNCTION; NONHUMAN; OBESITY; PODOCYTE; PRIORITY JOURNAL; PROTEINURIA; ADAPTATION; AGE; ANIMAL; CALORIC INTAKE; CELL COUNT; FISCHER 344 RAT; FOCAL GLOMERULOSCLEROSIS; GLOMERULUS; PATHOLOGY; PHYSIOLOGY; RAT;

ADAPTATION, PHYSIOLOGICAL; AGE FACTORS; ANIMALS; CALORIC RESTRICTION; CELL COUNT; ENERGY INTAKE; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; HYPERTROPHY; KIDNEY GLOMERULUS; PODOCYTES; RATS; RATS, INBRED F344;

EID: 33645266951     PISSN: 10466673     EISSN: None     Source Type: Journal    
DOI: 10.1681/ASN.2005050488     Document Type: Article

References (52)

1. Kriz W: Podocyte is the major culprit accounting for the progression of chronic renal disease. Microsc Res Tech 57: 189-195, 2002
2. Griffin SV, Petermann AT, Durvasula RV, Shankland SJ: Podocyte proliferation and differentiation in glomerular disease: Role of cell-cycle regulatory proteins. Nephrol Dial Transplant 18[Suppl 6]: vi8-v13, 2003
3. Mundel P, Shankland SJ: Podocyte biology and response to injury. J Am Soc Nephrol 13: 3005-3015, 2002
4. Pavenstadt H, Kriz W, Kretzler, M: Cell biology of the glomerular podocyte. Physiol Rev 83: 253-307, 2003
5. Kestila M, Lenkkeri U, Mannikko M, Lamerdin J, McCready P, Putaala H, Ruotsalainen V, Morita T, Nissinen M, Herva R, Kashtan CE, Peltonen L, Holmberg C, Olsen A, Tryggvason K: Positionally cloned gene for a novel glomerular protein-nephrin-is mutated in congenital nephrotic syndrome. Mol Cell 1: 575-582, 1998
6. Boute N, Gribouval O, Roselli S, Benessy F, Lee H, Fuchshuber A, Dahan K, Gubler MC, Niaudet P, Antignac C: NPHS2, encoding the glomerular protein podocin, is mutated in autosomal recessive steroid-resistant nephrotic syndrome. Nat Genet 24: 349-354, 2000
7. Kaplan JM, Kim SH, North KN, Rennke H, Correia LA, long HQ, Mathis BJ, Rodriguez-Perez JC, Allen PG, Beggs AH, Pollak MR: Mutations in ACTN4, encoding alpha-actinin-4, cause familial focal segmental glomerulosclerosis. Nat Genet 24: 251-256, 2000
8. Laurens WE, Vanrenterghem YF, Steels PS, Van Damme BJ: A new single nephron model of focal and segmental glomerulosclerosis in the Munich-Wistar rat. Kidney Int 45: 143-149, 1994
9. Kretzler M, Koeppen-Hagemann I, Kritz W: Podocyte damage is a critical step in the development of glomerulosclerosis in the uninephrectomized- desoxycorticosterone hypertensive rat. Virchows Arch 425: 181-193, 1994
10. Kim YH, Goyal M, Kurnit D, Wharram B, Wiggins J, Holzman L, Kershaw D, Wiggins R: Podocyte depletion and glomerulosclerosis have a direct relationship in the PAN-treated rat. Kidney Int 60: 957-968, 2001
11. Schiffer M, Bitzer M, Roberts IS, Kopp JB, ten Dijke P, Mundel P, Bottinger EP: Apoptosis in podocytes induced by TGF-beta and Smad7. J Clin Invest 108: 807-816, 2001
12. Wharram BL, Goyal M, Wiggins JE, Sanden SK, Hussain S, Filipiak WE, Saunders TL, Dysko RC, Kohno K, Holzman LB, Wiggins RC: Podocyte depletion causes glomerulosclerosis: Diphtheria toxin-induced podocyte depletion in rats expressing the human diphtheria toxin receptor transgene. J Am Soc Nephrol 16: 2941-2952, 2005
13. Pagtalunan ME, Miller PL, Jumping-Eagle S, Nelson RG, Myers BD, Rennke HG, Coplon NS, Sun L, Meyer TW: Podocyte loss and progressive glomerular injury in type II diabetes. J Clin Invest 99: 342-348, 1997
14. Meyer TW, Bennett PH, Nelson RG: Podocyte number predicts long-term urinary albumin excretion in Pima Indians with type II diabetes and microalbuminuria. Diabetologia 42: 1341-1344, 1999
15. Steffes MW, Schmidt D, McCrery R, Basgen JM; International Diabetic Nephropathy Study Group: Glomerular cell number in normal subjects and in type I diabetic patients. Kidney Int 59: 2104-2113, 2001
16. White KE, Bilous RW, Marshall SM, El Nahas M, Remuzzi G, Piras G, De Cosmo S, Viberti G; the European Study for the Prevention of Renal Disease in Type I diabetes (ESPRIT): Podocyte number in normotensive type I diabetic patients with albuminuria. Diabetes 51: 3083-3089, 2002
17. Dalla Vestra M, Masiero A, Roiter AM, Saller A, Crepaldi G, Fioretto P: Is podocyte injury relevant in diabetic nephropathy? Studies in patients with type 2 diabetes. Diabetes 52: 1031-1035, 2003
18. Lemley KV, Lafayette RA, Safai M, Derby G, Blouch K, Squarer A, Myers BD: Podocytopenia and disease severity in IgA nephropathy. Kidney Int 61: 1475-1485, 2002
19. Sharif K, Goyal M, Kershaw D, Kunkel R, Wiggins R: Podocyte phenotypes as defined by expression and distribution of GLEPP1 in the developing glomerulus and in nephrotic glomeruli from MCD, CNF, and FSGS. A dedifferentiation hypothesis for the nephrotic syndrome. Exp Nephrol 6: 234-244, 1998
20. Barisoni L, Kriz W, Mundel P, D'Agati V: The dysregulated podocyte phenotype: A novel concept in the pathogenesis of collapsing idiopathic focal segmental glomerulosclerosis and HIV-associated nephropathy. J Am Soc Nephrol 10: 51-61, 1999
21. Kanno K, Kawachi H, Uchida Y, Hara M, Shimizu F, Uchiyama M: Urinary sediment podocalyxin in children with glomerular diseases. Nephron Clin Pract 95: c91-c99, 2003
22. Vogelmann SU, Nelson WJ, Myers BD, Lemley KV: Urinary excretion of viable podocytes in health and renal disease. Am J Physiol Renal Physiol 285: F40-F48, 2003
23. Floege J, Hackman B, Kliem V, Kriz W, Alpers CE, Johnson RJ, Kuhn KW, Koch KM, Brunkhorst R: Age-related glomerulosclerosis and interstitial fibrosis in Milan normotensive rats: A podocyte disease. Kidney Int 51: 230-243, 1997
24. Yu BP, Masoro EJ, McMahan CA: Nutritional influences on aging of Fischer 344 rats: I. Physical, metabolic, and longevity characteristics. J Gerontol 40: 657-670, 1985
25. Olivetti G, Anversa P, Melissari M, Loud AV: Morphometry of the renal corpuscle during postnatal growth and compensatory hypertrophy. Kidney Int 17: 438-454, 1980
26. Kaplan C, Pasternack B, Shah H, Gallo G: Age-related incidence of sclerotic glomeruli in human kidneys. Am J Pathol 80: 227-234, 1975
27. Brandis A, Bianchi G, Reale E, Helmchen U, Kuhn K: Age-dependant glomerulosclerosis and proteinuria occurring in rats of the Milan normotensive strain and not in rats of the Milan hypertensive strain. Lab Invest 55: 234-243, 1986
28. Kleinknecht C, Laouari D, Hinglais N, Habib R, Dodu C, Lacour B, Broyer M: Role of amount and nature of carbohydrates in the course of experimental renal fail-ure. Kidney Int 30: 687-693, 1986
29. Tapp DC, Wortham WG, Addison JF, Hammonds DN, Barnes JL, Venkatachalam MA: Food restriction retards body growth and prevents end-stage renal pathology in remnant kidneys of rats regardless of protein intake. Lab Invest 60: 184-195, 1989
30. Keenan KP, Coleman JB, McCoy CL, Hoe CM, Soper KA, Laroque P: Chronic nephropathy in ad libitum overfed Sprague-Dawley rats and its early attenuation by increasing degrees of dietary (caloric) restriction to control growth. Toxicol Pathol 28: 788-798, 2000
31. Sanden SK, Wiggins JE, Goyal M, Riggs LK, Wiggins RC: Evaluation of a thick and thin section method for estimation of podocyte number, glomerular volume and glomerular volume per podocyte in rat kidney with Wilms' tumor-1 protein used as a podocyte nuclear marker. J Am Soc Nephrol 14: 2484-2493, 2003
32. Downer G, Phan SH, Wiggins RC: Analysis of renal fibrosis in a rabbit model of crescentic nephritis. J Clin Invest 82: 998-1006, 1988
33. Giordano TJ, Shedden KA, Schwartz DR, Kuick R, Taylor JM, Lee N, Misek DE, Greenson JK, Kardia SL, Beer DG, Rennert G, Cho KR, Gruber SB, Fearon ER, Hanash S: Organ-specific molecular classification of primary lung, colon, and ovarian adenocarcinomas using gene expression profiles. Am J Pathol 159: 1231-1238, 2001
34. Kwok JB, Kapoor R, Gotoda T, Iwamoto Y, Iizuka Y, Yamada N, Isaacs KE, Kushwaha VV, Church WB, Schofield PR, Kapoor V: A missense mutation in kynurenine aminotransferase-1 in spontaneously hypertensive rats. J Biol Chem 277: 35779-35782, 2002
35. Okada K, Ishikawa N, Fujimori K, Goryo M, Ikeda M, Sasaki J, Watanabe D, Takasuga A, Hirano T, Sugimoto Y: Abnormal development of nephrons in claudin-16-defective Japanese black cattle. J Vet Med Sci 67: 171-178, 2005
36. Ruf RG, Schultheiss M, Lichtenberger A, Karle SM, Zalewski I, Mucha B, Everding AS, Neuhaus T, Patzer L, Plank C, Haas JP, Ozaltin F, Imm A, Fuchshuber A, Bakkaloglu A, Hildebrandt F; APN Study Group: Prevalence of WT1 mutations in a large cohort of patients with steroid-resistant and steroid-sensitive nephrotic syndrome. Kidney Int 66: 564-570, 2004
37. Quaggin SE: Transcriptional regulation of podocyte specification and differentiation. Microsc Res Tech 57: 208-211, 2002
38. Thomas PE, Wharram BL, Goyal M, Wiggins JE, Holzman LB, Wiggins RC: GLEPP1, a renal glomerular epithelial cell (podocyte) membrane protein-tyrosine phosphatase. Identification, molecular cloning, and characterization in rabbit. J Biol Chem 269: 19953-19962, 1994
39. Hudson BG: The molecular basis of Goodpasture and Alport syndromes: Beacons for the discovery of the collagen IV family. J Am Soc Nephrol 15: 2514-2527, 2004
40. Kerjaschki D, Sharkey DJ, Farquhar MG: Identification and characterization of podocalyxin - The major sialo-protein of the renal glomerular epithelial cell. J Cell Biol 98: 1591-1596, 1984
41. Eremina V, Quaggin SE: The role of VEGF-A in glomerular development and function. Curr Opin Nephrol Hypertens 13: 9-15, 2004
42. Mundel P, Heid HW, Mundel TM, Kruger M, Reiser J, Kriz W: Synaptopodin: An actin-associated protein in telencephalic dendrites and renal podocytes. J Cell Biol 139: 193-204, 1997
43. Ricono JM, Xu YC, Arar M, Jin DC, Barnes JL, Abboud HE: Morphological insights into the origin of glomerular endothelial and mesangial cells and their precursors. J Histochem Cytochem 51: 141-150, 2003
44. Dean DJ, Gazdag AC, Wetter TJ, Cartee GD: Comparison of the effects of 20 days and 15 months of calorie restriction on male Fischer 344 rats. Aging 10: 303-307, 1998
45. Fogo A, Ichikawa I: Evidence for a pathogenic linkage between glomerular hypertrophy and sclerosis. Am J Kidney Dis 17: 666-669, 1991
46. Fogo AB: Glomerular hypertension, abnormal glomerular growth, and progression of renal diseases. Kidney Int Suppl 75: S15-S21, 2000
47. US Renal Data System: USRDS 2000 Annual Data Report: Atlas of End-Stage Renal Disease in the United States, Bethesda, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, 2000. Available: http://www.usrds.org/adr_2000.htm. Accessed August 5, 2005
48. Bhathena DB: Glomerular basement membrane length to podocyte ratio in human nephronopenia: Implications for focal segmental glomerulosclerosis. Am J Kidney Dis 41: 1179-1188, 2003
49. Yang CW, Striker LJ, Kopchick JJ, Chen WY, Pesce CM, Peten EP, Striker GE: Glomerulosclerosis in mice transgenic for native or mutated bovine growth hormone gene. Kidney Int Suppl 39: S90-S94, 1993
50. Cusumano AM, Bodkin NL, Hansen BC, Iotti R, Owens J, Klotman PE, Kopp JB: Glomerular hypertrophy is associated with hyperinsulinemia and precedes overt diabetes in aging rhesus monkeys. Am J Kidney Dis 40:1075-1085, 2002
51. Kambham N, Markowitz GS, Valeri AM, Lin J, D'Agati VD: Obesity-related glomerulopathy: An emerging epidemic. Kidney Int 59: 1498-1509, 2001
52. Iseki K, Ikemiya Y, Kinjo K, Inoue T, Iseki C, Takishita S: Body mass index and the risk of development of end stage renal disease in a screened cohort. Kidney Int 65: 1870-1876, 2004