A population of selected renal cells augments renal function and extends survival in the ZSF1 model of progressive diabetic nephropathy

Cell Transplantation

Volumn 22, Issue 6, 2013, Pages 1023-1039

  Kelley, Rusty ^a   Bruce, Andrew ^a   Spencer, Tom ^a   Werdin, Eric ^a   Ilagan, Roger ^a   Choudhury, Sumana ^a   Rivera, Elias ^a   Wallace, Shay ^a   Guthrie, Kelly ^a   Jayo, Manuel ^a   Xu, Fengfeng ^b   Rao, Anjali N ^b   Humphreys, Benjamin D ^b   Presnell, Sharon ^a   Bertram, Tim ^a  

^a Tengion Inc   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Diabetes; Nephropathy; Regeneration; Renal; Survival

Indexed keywords

RENIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE REGULATION; CELL COMPOSITION; CELL POPULATION; CELL SURVIVAL; CELL TRANSPLANTATION; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC NEPHROPATHY; DISEASE COURSE; DISEASE SEVERITY; DYSLIPIDEMIA; ELECTROLYTE BALANCE; GLOMERULOSCLEROSIS; GLOMERULUS FILTRATION; HYPERTENSION; KIDNEY CELL; KIDNEY CONCENTRATING CAPACITY; KIDNEY CORTEX; KIDNEY FIBROSIS; KIDNEY FUNCTION; KIDNEY STRUCTURE; MALE; NEPHRITIS; NONHUMAN; OBESITY; PRIORITY JOURNAL; RAT; REGENERATIVE ABILITY;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BLOOD PRESSURE; CELL TRACKING; DIABETIC NEPHROPATHIES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; EPITHELIAL CELLS; FEMALE; GLOMERULAR FILTRATION RATE; KIDNEY; KIDNEY FUNCTION TESTS; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MICE; RATS; RATS, INBRED LEW; SURVIVAL ANALYSIS;

EID: 84877713628     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368912X653237     Document Type: Article

References (36)

1. Atala, A.; Bauer, S. B.; Soker, S.; Yoo, J. J.; Retik, A. B. Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet 367(9518):1241-1246; 2006.
2. Basu, J.; Genheimer, C. W.; Rivera, E. A.; Payne, R.; Mihalko, K.; Guthrie, K.; Bruce, A. T.; Robbins, N.; McCoy, D.; Sangha, N.; Ilagan, R.; Knight, T.; Spencer, T.; Wagner, B. J.; Jayo, M. J.; Jain, D.; Ludlow, J. W.; Halberstadt, C. Functional evaluation of primary renal cell/biomaterial Neo-Kidney Augment prototypes for renal tissue engineering. Cell Transplant. 20(11-12):1771-1790; 2011.
3. Benigni, A.; Morigi, M.; Remuzzi, G. Kidney regeneration. Lancet 375(9722):1310-1317; 2010.
4. Bilan, V. P.; Salah, E. M.; Bastacky, S.; Jones, H. B.; Mayers, R. M.; Zinker, B.; Poucher, S. M.; Tofovic, S. P. Diabetic nephropathy and long-term treatment effects of rosiglitazone and enalapril in obese ZSF1 rats. J. Endocrinol. 210(3):293-308; 2011.
5. Cavaglieri, R. C.; Martini, D.; Sogayar, M. C.; Noronha, I. L. Mesenchymal stem cells delivered at the subcapsule of the kidney ameliorate renal disease in the rat remnant kidney model. Transplant. Proc. 41(3):947-951; 2009.
6. Chang, Q.; Hoefs, S.; van der Kemp, A. W.; Topala, C. N.; Bindels, R. J.; Hoenderop, J. G. The β-glucuronidase klotho hydrolyzes and activates the TRPV5 channel. Science 310(5747):490-493; 2005.
7. Griffin, K. A.; Abu-Naser, M.; Abu-Amarah, I.; Picken, M.; Williamson, G. A.; Bidani, A. K. Dynamic blood pressure load and nephropathy in the ZSF1 (fa/fa cp) model of type 2 diabetes. Am. J. Physiol. Renal Physiol. 293(5):F1605- F1613; 2007.
8. Herrera, M. B.; Bussolati, B.; Bruno, S.; Morando, L.; Mauriello-Romanazzi, G.; Sanavio, F.; Stamenkovic, I.; Biancone, L.; Camussi, G. Exogenous mesenchymal stem cells localize to the kidney by means of CD44 following acute tubular injury. Kidney Int. 72(4):430-441; 2007.
9. Heyen, J. R.; Blasi, E. R.; Nikula, K.; Rocha, R.; Daust, H. A.; Frierdich, G.; Van Vleet, J. F.; De Ciechi, P.; McMahon, E. G.; Rudolph, A. E. Structural, functional, and molecular characterization of the SHHF model of heart failure. Am. J. Physiol. Heart Circ. Physiol. 283(5):H1775-H1784; 2002.
10. Humphreys, B. D.; Czerniak, S.; DiRocco, D. P.; Hasnain, W.; Cheema, R.; Bonventre, J. V. Repair of injured proximal tubule does not involve specialized progenitors. Proc. Natl. Acad. Sci. USA 108(22):9226-9231; 2011.
11. Humphreys, B. D.; Lin, S. L.; Kobayashi, A.; Hudson, T. E.; Nowlin, B. T.; Bonventre, J. V.; Valerius, M. T.; McMahon, A. P.; Duffield, J. S. Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am. J. Pathol. 176(1):85-97; 2009.
12. Humphreys, B. D.; Valerius, M. T.; Kobayashi, A.; Mugford, J. W.; Soeung, S.; Duffield, J. S.; McMahon, A. P.; Bonventre, J. V. Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2(3):284-291; 2008.
13. Imberti, B.; Morigi, M.; Tomasoni, S.; Rota, C.; Corna, D.; Longaretti, L.; Rottoli, D.; Valsecchi, F.; Benigni, A.; Wang, J.; Abbate, M.; Zoja, C.; Remuzzi, G. Insulin-like growth factor-1 sustains stem cell mediated renal repair. J. Am. Soc. Nephrol. 18(11):2921-2928; 2007.
14. Jayo, M. J.; Jain, D.; Wagner, B. J.; Bertram, T. A. Early cellular and stromal responses in regeneration versus repair of a mammalian bladder using autologous cell and biodegradable scaffold technologies. J. Urol. 180(1):392- 397; 2008.
15. Kelley, R.; Werdin, E. S.; Bruce, A. T.; Choudhury, S.; Wallace, S. M.; Ilagan, R. M.; Cox, B. R.; Tatsumi-Ficht, P.; Rivera, E. A.; Spencer, T.; Scott Rapoport, H.; Wagner, B. J.; Guthrie, K.; Jayo, M. J.; Bertram, T. A.; Presnell, S. C. Tubular cell-enriched subpopulation of primary renal cells improves survival and augments kidney function in rodent model of chronic kidney disease. Am. J. Physiol. Renal Physiol. 299(5):F1026-F1039; 2010.
16. Kunter, U.; Rong, S.; Djuric, Z.; Boor, P.; Muller-Newen, G.; Yu, D.; Floege, J. Transplanted mesenchymal stem cells accelerate glomerular healing in experimental glomerulonephritis. J. Am. Soc. Nephrol. 17(8):2202-2212; 2006.
17. Liu, B. C.; Zhang, L.; Lv, L. L.; Wang, Y. L.; Liu, D. G.; Zhang, X. L. Application of antibody array technology in the analysis of urinary cytokine profiles in patients with chronic kidney disease. Am. J. Nephrol. 26(5):483-490; 2006.
18. Ludlow, J. W.; Kelley, R. W.; Bertram, T. A. The future of regenerative medicine: Urinary system. Tissue Eng. Part B Rev. 18(3):218-224; 2012.
19. Mensenkamp, A. R.; Hoenderop, J. G.; Bindels, R. J. Recent advances in renal tubular calcium reabsorption. Curr. Opin. Nephrol. Hypertens. 15(5):524-529; 2006.
20. Morigi, M.; Imberti, B.; Zoja, C.; Corna, D.; Tomasoni, S.; Abbate, M.; Rottoli, D.; Angioletti, S.; Benigni, A.; Perico, N.; Alison, M.; Remuzzi, G. Mesenchymal stem cells are renotropic, helping to repair the kidney and improve function in acute renal failure. J. Am. Soc. Nephrol. 15(7):1794- 1804; 2004.
21. Morigi, M.; Introna, M.; Imberti, B.; Corna, D.; Abbate, M.; Rota, C.; Rottoli, D.; Benigni, A.; Perico, N.; Zoja, C.; Rambaldi, A.; Remuzzi, A.; Remuzzi, G. Human bone marrow mesenchymal stem cells accelerate recovery of acute renal injury and prolong survival in mice. Stem Cells 26(8):2075-2082; 2008.
22. Ninichuk, V.; Khandoga, A. G.; Segerer, S.; Loetscher, P.; Schlapbach, A.; Revesz, L.; Feifel, R.; Khandoga, A.; Krombach, F.; Nelson, P. J.; Schlondorff, D.; Anders, H. J. The role of interstitial macrophages in nephropathy of type 2 diabetic db/db mice. Am. J. Pathol. 170(4):1267-1276; 2007.
23. Otto, W. R.; Wright, N. A. Mesenchymal stem cells: From experiment to clinic. Fibrogenesis Tissue Repair 4:20; 2011.
24. Prabhakar, S.; Starnes, J.; Shi, S.; Lonis, B.; Tran, R. Diabetic nephropathy is associated with oxidative stress and decreased renal nitric oxide production. J. Am. Soc. Nephrol. 18(11):2945-2952; 2007.
25. Presnell, S. C.; Bruce, A. T.; Wallace, S. M.; Choudhury, S.; Genheimer, C. W.; Cox, B.; Guthrie, K.; Werdin, E. S.; Tatsumi-Ficht, P.; Ilagan, R. M.; Kelley, R. W.; Rivera, E. A.; Ludlow, J. W.; Wagner, B. J.; Jayo, M. J.; Bertram, T. A. Isolation, characterization, and expansion methods for defined primary renal cell populations from rodent, canine, and human normal and diseased kidneys. Tissue Eng. Part C Methods 17(3):261-273; 2011.
26. Rafikova, O.; Salah, E. M.; Tofovic, S. P. Renal and metabolic effects of tempol in obese ZSF1 rats-distinct role for superoxide and hydrogen peroxide in diabetic renal injury. Metabolism 57(10):1434-1444; 2008.
27. Ruggenenti, P.; Remuzzi, G. Time to abandon microalbuminuria? Kidney Int. 70(7):1214-1222; 2006.
28. Semedo, P.; Correa-Costa, M.; Antonio Cenedeze, M.; Maria Avancini Costa Malheiros, D.; Antonia dos Reis, M.; Shimizu, M. H.; Seguro, A. C.; Pacheco-Silva, A.; Saraiva Camara, N. O. Mesenchymal stem cells attenuate renal fibrosis through immune modulation and remodeling properties in a rat remnant kidney model. Stem Cells 27(12):3063-3073; 2009.
29. Smith, S. A.; Lister, C. A.; Toseland, C. D.; Buckingham, R. E. Rosiglitazone prevents the onset of hyperglycaemia and proteinuria in the Zucker diabetic fatty rat. Diabetes Obes. Metab. 2(6):363-372; 2000.
30. + T-cells in renal fibrosis following ureteric obstruction. Kidney Int. 78(4):351-362; 2010.
31. Tofovic, S. P.; Jackson, E. K. Rat models of the metabolic syndrome. Methods Mol. Med. 86:29-46; 2003.
32. Tofovic, S. P.; Kost, Jr., C. K.; Jackson, E. K.; Bastacky, S. I. Long-term caffeine consumption exacerbates renal failure in obese, diabetic, ZSF1 [fa-fa(cp)] rats. Kidney Int. 61(4):1433-1444; 2002.
33. Tofovic, S. P.; Kusaka, H.; Jackson, E. K.; Bastacky, S. I. Renal and metabolic effects of caffeine in obese [fa/fa(cp)], diabetic, hypertensive ZSF1 rats. Ren. Fail. 23(2):159- 173; 2001.
34. Tofovic, S. P.; Kusaka, H.; Kost, Jr., C. K.; Bastacky, S. Renal function and structure in diabetic, hypertensive, obese ZDFxSHHF-hybrid rats. Ren. Fail. 22(4):387-406; 2000.
35. Togel, F.; Hu, Z.;Weiss, K.; Isaac, J.; Lange, C.;Westenfelder, C. Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiationindependent mechanisms. Am. J. Physiol. Renal Physiol. 289(1):F31-F42; 2005.
36. Zhang, X.; Jia, Y.; Jackson, E. K.; Tofovic, S. P. 2- Methoxyestradiol and 2-ethoxyestradiol retard the progression of renal disease in aged, obese, diabetic ZSF1 rats. J. Cardiovasc. Pharmacol. 49(1):56-63; 2007.