Healthy bone marrow cells reduce progression of kidney failure better than CKD bone marrow cells in rats with established chronic kidney disease

Cell Transplantation

Volumn 21, Issue 10, 2012, Pages 2299-2312

  van Koppen, Arianne ^a   Joles, Jaap A ^a   Bongartz, Lennart G ^a   van den Brandt, Jens ^b   Reichardt, Holger M ^b   Goldschmeding, Roel ^a   Nguyen, Tri Q ^a   Verhaar, Marianne C ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

Bone marrow cells (BMCs); Endothelium; Kidney; Renal hemodynamics

Indexed keywords

CREATININE; ENHANCED GREEN FLUORESCENT PROTEIN; UREA;

ANEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CHRONIC KIDNEY DISEASE; CONTROLLED STUDY; DISEASE COURSE; GLOMERULOSCLEROSIS; GLOMERULUS FILTRATION RATE; KIDNEY DISEASE; KIDNEY FAILURE; KIDNEY PLASMA FLOW; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEINURIA; RAT; SYSTOLIC BLOOD PRESSURE; TUBULAR ATROPHY;

ANIMALS; BLOOD PRESSURE; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; KIDNEY GLOMERULUS; MALE; RATS; RATS, INBRED LEW; RENAL INSUFFICIENCY, CHRONIC;

RATTUS;

EID: 84870456579     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368912X636795     Document Type: Article

References (53)

1. Alexandre, C. S.; Volpini, R. A.; Shimizu, M. H.; Sanches, T. R.; Semedo, P.; Di Jura, V. L.; Camara, N. O.; Seguro, A. C.; Andrade, L. Lineage-negative bone marrow cells protect against chronic renal failure. Stem Cells 27:682-692; 2009.
2. Attia, D. M.; Verhagen, A. M.; Stroes, E. S.; van Faassen, E. E.; Grone, H. J.; De Kimpe, S. J.; Koomans, H. A.; Braam, B.; Joles, J. A. Vitamin E alleviates renal injury, but not hypertension, during chronic nitric oxide synthase inhibition in rats. J. Am. Soc. Nephrol. 12:2585-2593; 2001.
3. Ayala-Lugo, A.; Tavares, A. M.; Paz, A. H.; Alegretti, A.; Miquelito, L.; Bock, H.; Giugliani, R.; Clausell, N.; Cirne-Lima, E.; Rohde, L. E. Age-dependent availability and functionality of bone marrow stem cells in an experimental model of acute and chronic myocardial infarction. Cell Transplant. 20:407-419; 2011.
4. Barreira, A. L.; Takiya, C. M.; Castiglione, R. C.; Maron-Gutierrez, T.; Barbosa, C. M.; Ornellas, D. S.; Verdoorn, K. S.; Pascarelli, B. M.; Borojevic, R.; Einicker-Lamas, M.; Leite, M., Jr.; Morales, M. M.; Vieyra, A. Bone marrow mononuclear cells attenuate interstitial fibrosis and stimulate the repair of tubular epithelial cells after unilateral ureteral obstruction. Cell. Physiol. Biochem. 24:585-594; 2009.
5. Bongartz, L. G.; Braam, B.; Verhaar, M. C.; Cramer, M. J.; Goldschmeding, R.; Gaillard, C. A.; Doevendans, P. A.; Joles, J. A. Transient nitric oxide reduction induces permanent cardiac systolic dysfunction and worsens kidney damage in rats with chronic kidney disease. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298:R815-R823; 2010.
6. Broekema, M.; Harmsen, M. C.; van Luyn, M. J.; Koerts, J. A.; Petersen, A. H.; van Kooten, T. G.; van Goor, H.; Navis, G.; Popa, E. R. Bone marrow-derived myofibroblasts contribute to the renal interstitial myofibroblast population and produce procollagen I after ischemia/reperfusionin rats. J. Am. Soc. Nephrol. 18:165-175; 2007.
7. Caldas, H. C.; Fernandes, I. M.; Gerbi, F.; Souza, A. C.; Baptista, M. A.; Ramalho, H. J.; Kawasaki-Oyama, R. S.; Goloni-Bertollo, E. M.; Pavarino-Bertelli, E. C.; Braile, D. M.; Abbud-Filho, M. Effect of whole bone marrow cell infusion in the progression of experimental chronic renal failure. Transplant. Proc. 40:853-855; 2008.
8. 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. 41:947-951; 2009.
9. Chade, A. R.; Zhu, X.; Lavi, R.; Krier, J. D.; Pislaru, S.; Simari, R. D.; Napoli, C.; Lerman, A.; Lerman, L. O. Endothelial progenitor cells restore renal function in chronic experimental renovascular disease. Circulation 119:547-557; 2009.
10. Choi, S.; Park, M.; Kim, J.; Hwang, S.; Park, S.; Lee, Y. The role of mesenchymal stem cells in the functional improvement of chronic renal failure. Stem Cells Dev. 18:521-529; 2009.
11. Cornacchia, F.; Fornoni, A.; Plati, A. R.; Thomas, A.; Wang, Y.; Inverardi, L.; Striker, L. J.; Striker, G. E. Glomerulosclerosis is transmitted by bone marrow-derived mesangial cell progenitors. J. Clin. Invest. 108:1649-1656; 2001.
12. Doi, K.; Leelahavanichkul, A.; Yuen, P. S.; Star, R. A. Animal models of sepsis and sepsis-induced kidney injury. J. Clin. Invest. 119:2868-2878; 2009.
13. Drewa, T.; Joachimiak, R.; Kaznica, A.; Flisinski, M.; Brymora, A.; Manitius, J. Bone marrow progenitors from animals with chronic renal failure lack capacity of in vitro proliferation. Transplant. Proc. 40:1668-1673; 2008.
14. Fadini, G. P.; Albiero, M.; Boscaro, E.; Agostini, C.; Avogaro, A. Endothelial progenitor cells as resident accessory cells for post-ischemic angiogenesis. Atherosclerosis 204:20-22; 2009.
15. Fang, T. C.; Otto, W. R.; Jeffery, R.; Hunt, T.; Alison, M. R.; Cook, H. T.; Wright, N. A.; Poulsom, R. Exogenous bone marrow cells do not rescue non-irradiated mice from acute renal tubular damage caused by HgCl2, despite establishment of chimaerism and cell proliferation in bone marrow and spleen. Cell Prolif. 41:592-606; 2008.
16. Fleck, C.; Appenroth, D.; Jonas, P.; Koch, M.; Kundt, G.; Nizze, H.; Stein, G. Suitability of 5/6 nephrectomy (5/6NX) for the induction of interstitial renal fibrosis in rats- influence of sex, strain, and surgical procedure. Exp. Toxicol. Pathol. 57:195-205; 2006.
17. Fogo, A. B. Progression versus regression of chronic kidney disease. Nephrol. Dial. Transplant. 21:281-284; 2006.
18. Go, A. S.; Chertow, G. M.; Fan, D.; McCulloch, C. E.; Hsu, C. Y. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N. Engl. J. Med. 351:1296-1305; 2004.
19. Goligorsky, M. S.; Yasuda, K.; Ratliff, B. Dysfunctional endothelial progenitor cells in chronic kidney disease. J. Am. Soc. Nephrol. 21:911-919; 2010.
20. Griffin, K. A.; Picken, M. M.; Churchill, M.; Churchill, P.; Bidani, A. K. Functional and structural correlates of glomerulosclerosis after renal mass reduction in the rat. J. Am. Soc. Nephrol. 11:497-506; 2000.
21. Grunewald, M.; Avraham, I.; Dor, Y.; Bachar-Lustig, E.; Itin, A.; Jung, S.; Chimenti, S.; Landsman, L.; Abramovitch, R.; Keshet, E. VEGF-induced adult neovascularization: Recruitment, retention, and role of accessory cells. Cell 124:175-189; 2006.
22. Jie, K. E.; Zaikova, M. A.; Bergevoet, M. W.; Westerweel, P. E.; Rastmanesh, M.; Blankestijn, P. J.; Boer, W. H.; Braam, B.; Verhaar, M. C. Progenitor cells and vascular function are impaired in patients with chronic kidney disease. Nephrol. Dial. Transplant. 25:1875-1882; 2010.
23. Kahler, C. M.; Wechselberger, J.; Hilbe, W.; Gschwendtner, A.; Colleselli, D.; Niederegger, H.; Boneberg, E. M.; Spizzo, G.; Wendel, A.; Gunsilius, E.; Patsch, J. R.; Hamacher, J. Peripheral infusion of rat bone marrow derived endothelial progenitor cells leads to homing in acute lung injury. Respir. Res. 8:50; 2007.
24. Kalka, C.; Masuda, H.; Takahashi, T.; Kalka-Moll, W. M.; Silver, M.; Kearney, M.; Li, T.; Isner, J. M.; Asahara, T. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc. Natl. Acad. Sci. USA. 97:3422-3427; 2000.
25. Kang, D. H.; Kanellis, J.; Hugo, C.; Truong, L.; Anderson, S.; Kerjaschki, D.; Schreiner, G. F.; Johnson, R. J. Role of the microvascular endothelium in progressive renal disease. J. Am. Soc. Nephrol. 13:806-816; 2002.
26. 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.; Rapoport, H. S.; 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:F1026-F1039; 2010.
27. Kinomura, M.; Kitamura, S.; Tanabe, K.; Ichinose, K.; Hirokoshi, K.; Takazawa, Y.; Kitayama, H.; Nasu, T.; Sugiyama, H.; Yamasaki, Y.; Sugaya, T.; Maeshima, Y.; Makino, H. Amelioration of cisplatin-induced acute renal injury by renal progenitor-like cells derived from the adult rat kidney. Cell Transplant. 17:143-158; 2008.
28. Koeners, M. P.; Braam, B.; van der Giezen, D. M.; Goldschmeding, R.; Joles, J. A. A perinatal nitric oxide donor increases renal vascular resistance and ameliorates hypertension and glomerular injury in adult fawn-hooded hypertensive rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294:R1847-R1855; 2008.
29. Koeners, M. P.; Racasan, S.; Koomans, H. A.; Joles, J. A.; Braam, B. Nitric oxide, superoxide and renal blood flow autoregulation in SHR after perinatal l-arginine and antioxidants. Acta Physiol. 190:329-338; 2007.
30. Kraitchman, D. L.; Tatsumi, M.; Gilson, W. D.; Ishimori, T.; Kedziorek, D.; Walczak, P.; Segars, W. P.; Chen, H. H.; Fritzges, D.; Izbudak, I.; Young, R. G.; Marcelino, M.; Pittenger, M. F.; Solaiyappan, M.; Boston, R. C.; Tsui, B. M.; Wahl, R. L.; Bulte, J. W. Dynamic imaging of allogeneic mesenchymal stem cells trafficking to myocardial infarction. Circulation 112:1451-1461; 2005.
31. La Manna G.; Bianchi, F.; Cappuccilli, M.; Cenacchi, G.; Tarantino, L.; Pasquinelli, G.; Valente, S.; Della, B. E.; Cantoni, S.; Claudia, C.; Neri, F.; Tsivian, M.; Nardo, B.; Ventura, C.; Stefoni, S. Mesenchymal stem cells in renal function recovery after acute kidney injury. Use of a differentiating agent in a rat model. Cell Transplant. 20:1193-1208; 2011.
32. Levey, A. S. Measurement of renal function in chronic renal disease. Kidney Int. 38:167-184; 1990.
33. Li, B.; Morioka, T.; Uchiyama, M.; Oite, T. Bone marrow cell infusion ameliorates progressive glomerulosclerosis in an experimental rat model. Kidney Int. 69:323-330; 2006.
34. Li, J.; Deane, J. A.; Campanale, N. V.; Bertram, J. F.; Ricardo, S. D. The contribution of bone marrow-derived cells to the development of renal interstitial fibrosis. Stem Cells 25:697-706; 2007.
35. Little, M. H.; Rae, F. K. Review article: Potential cellular therapies for renal disease: Can we translate results from animal studies to the human condition? Nephrology 14:544-553; 2009.
36. 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 26:2075-2082; 2008.
37. Myers, G. L.; Miller, W. G.; Coresh, J.; Fleming, J.; Greenberg, N.; Greene, T.; Hostetter, T.; Levey, A. S.; Panteghini, M.; Welch, M.; Eckfeldt, J. H. Recommendations for improving serum creatinine measurement: A report from the Laboratory Working Group of the National Kidney Disease Education Program. Clin. Chem. 52:5-18; 2006.
38. Ostendorf, T.; Kunter, U.; Eitner, F.; Loos, A.; Regele, H.; Kerjaschki, D.; Henninger, D. D.; Janjic, N.; Floege, J. VEGF(165) mediates glomerular endothelial repair. J. Clin. Invest. 104:913-923; 1999.
39. Peters, B. A.; Diaz, L. A.; Polyak, K.; Meszler, L.; Romans, K.; Guinan, E. C.; Antin, J. H.; Myerson, D.; Hamilton, S. R.; Vogelstein, B.; Kinzler, K. W.; Lengauer, C. Contribution of bone marrow-derived endothelial cells to human tumor vasculature. Nat. Med. 11:261-262; 2005.
40. Rabelink, T. J.; de Boer, H. C.; de Koning, E. J.; van Zonneveld, A. J. Endothelial progenitor cells: More than an inflammatory response? Arterioscler. Thromb. Vasc. Biol. 24:834-838; 2004.
41. Rookmaaker, M. B.; Smits, A. M.; Tolboom, H.; Van't Woud, K.; Martens, A. C.; Goldschmeding, R.; Joles, J. A.; van Zonneveld, A. J.; Grone, H. J.; Rabelink, T. J.; Verhaar, M. C. Bone marrow-derived cells contribute to glomerular endothelial repair in experimental glomerulonephritis. Am. J. Pathol. 163:553-562; 2003.
42. Sangidorj, O.; Yang, S. H.; Jang, H. R.; Lee, J. P.; Cha, R. H.; Kim, S. M.; Lim, C. S.; Kim, Y. S. Bone marrowderived endothelial progenitor cells confer renal protection in a murine chronic renal failure model. Am. J. Physiol. Renal Physiol. 299:F325-F335; 2010.
43. Shimizu, A.; Kitamura, H.; Masuda, Y.; Ishizaki, M.; Sugisaki, Y.; Yamanaka, N. Rare glomerular capillary regeneration and subsequent capillary regression with endothelial cell apoptosis in progressive glomerulonephritis. Am. J. Pathol. 151:1231-1239; 1997.
44. Silva, G. V.; Litovsky, S.; Assad, J. A.; Sousa, A. L.; Martin, B. J.; Vela, D.; Coulter, S. C.; Lin, J.; Ober, J.; Vaughn, W. K.; Branco, R. V.; Oliveira, E. M.; He, R.; Geng, Y. J.; Willerson, J. T.; Perin, E. C. Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model. Circulation 111:150-156; 2005.
45. Tornig, J.; Amann, K.; Ritz, E.; Nichols, C.; Zeier, M.; Mall, G. Arteriolar wall thickening, capillary rarefaction and interstitial fibrosis in the heart of rats with renal failure The effects of ramipril, nifedipine and moxonidine. J. Am. Soc. Nephrol. 7:667-675; 1996.
46. Uchimura, H.; Marumo, T.; Takase, O.; Kawachi, H.; Shimizu, F.; Hayashi, M.; Saruta, T.; Hishikawa, K.; Fujita, T. Intrarenal injection of bone marrow-derived angiogenic cells reduces endothelial injury and mesangial cell activation in experimental glomerulonephritis. J. Am. Soc. Nephrol. 16:997-1004; 2005.
47. van den Brandt, J.; Wang, D.; Kwon, S. H.; Heinkelein, M.; Reichardt, H. M. Lentivirally generated eGFP-transgenic rats allow efficient cell tracking in vivo. Genesis 39:94-99; 2004.
48. Westerweel, P. E.; Hoefer, I. E.; Blankestijn, P. J.; de Bree, P.; Groeneveld, D.; van Oostrom O.; Braam, B.; Koomans, H. A.; Verhaar, M. C. End-stage renal disease causes an imbalance between endothelial and smooth muscle progenitor cells. Am. J. Physiol. Renal Physiol. 292:F1132-F1140; 2007.
49. Yang, B.; El-Nahas, A. M.; Thomas, G. L.; Haylor, J. L.; Watson, P. F.; Wagner, B.; Johnson, T. S. Caspase 3 and apoptosis in experimental chronic renal scarring. Kidney Int. 60:1765-1776; 2001.
50. Yuen, D. A.; Connelly, K. A.; Advani, A.; Liao, C.; Kuliszewski, M. A.; Trogadis, J.; Thai, K.; Advani, S. L.; Zhang, Y.; Kelly, D. J.; Leong-Poi, H.; Keating, A.; Marsden, P. A.; Stewart, D. J.; Gilbert, R. E. Culture-modified bone marrow cells attenuate cardiac and renal injury in a chronic kidney disease rat model via a novel antifibrotic mechanism. PLoS One 5:e9543; 2010.
51. Zatz, R. Haemodynamically mediated glomerular injury: The end of a 15-year-old controversy? Curr. Opin. Nephrol. Hypertens. 5:468-475; 1996.
52. Zheng, F.; Cornacchia, F.; Schulman, I.; Banerjee, A.; Cheng, Q. L.; Potier, M.; Plati, A. R.; Berho, M.; Elliot, S. J.; Li, J.; Fornoni, A.; Zang, Y. J.; Zisman, A.; Striker, L. J.; Striker, G. E. Development of albuminuria and glomerular lesions in normoglycemic B6 recipients of db/db mice bone marrow: The role of mesangial cell progenitors. Diabetes 53:2420-2427; 2004.
53. Ziegelhoeffer, T.; Fernandez, B.; Kostin, S.; Heil, M.; Voswinckel, R.; Helisch, A.; Schaper, W. Bone marrowderived cells do not incorporate into the adult growing vasculature. Circ. Res. 94:230-238; 2004.