Biology of Blood and Marrow Transplantation
Volume 15, Issue 11 , Pages 1354-1365 , November 2009

Endovenous Administration of Bone Marrow-Derived Multipotent Mesenchymal Stromal Cells Prevents Renal Failure in Diabetic Mice

  • Fernando Ezquer

      Affiliations

    • Instituto de Ciencias, Facultad de Medicina Clínica Alemana Universidad del Desarrollo, Santiago, Chile
    • ,
  • Marcelo Ezquer

      Affiliations

    • Instituto de Ciencias, Facultad de Medicina Clínica Alemana Universidad del Desarrollo, Santiago, Chile
    • Instituto de Biología y Medicina Experimental de Cuyo, IMBECU-CONYCET, Mendoza, Argentina
    • ,
  • Valeska Simon

      Affiliations

    • Instituto de Ciencias, Facultad de Medicina Clínica Alemana Universidad del Desarrollo, Santiago, Chile
    • ,
  • Fabian Pardo

      Affiliations

    • Instituto de Bioquímica, Universidad Austral de Chile, Valdivia, Chile
    • ,
  • Alejandro Yañez

      Affiliations

    • Instituto de Bioquímica, Universidad Austral de Chile, Valdivia, Chile
    • ,
  • Daniel Carpio

      Affiliations

    • Instituto de Histología y Patología, Universidad Austral de Chile, Valdivia, Chile
    • ,
  • Paulette Conget

      Affiliations

    • Instituto de Ciencias, Facultad de Medicina Clínica Alemana Universidad del Desarrollo, Santiago, Chile
    • Corresponding Author InformationCorrespondence and reprint requests: Paulette A. Conget, PhD, Av. Las Condes 12438, Lo Barnechea, Santiago, Chile 7710162.

Received 1 April 2009 ,Accepted 24 July 2009.

References 

  1. Zimmet P, Alberti KG, Shaw J. Global and societal implications of the diabetes epidemic. Nature. 2001;414:782–787
  2. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 2004;27:1047–1053
  3. Remuzzi G, Schieppati A, Ruggenenti P. Clinical practice. Nephropathy in patients with type 2 diabetes. N Engl J Med. 2002;346:1145–1151
  4. USRDS. The United States Renal Data System. Am J Kidney Dis. 2003;42:1–230
  5. Maisonneuve P, Agodoa L, Gellert R, et al. Distribution of primary renal diseases leading to end-stage renal failure in the United States, Europe, and Australia/New Zealand: results from an international comparative study. Am J Kidney Dis. 2000;35:157–165
  6. Chavers BM, Bilous RW, Ellis EN, Steffes MW, Mauer SM. Glomerular lesions and urinary albumin excretion in type I diabetes without overt proteinuria. N Engl J Med. 1989;320:966–970
  7. Cooper ME. Pathogenesis, prevention, and treatment of diabetic nephropathy. Lancet. 1998;352:213–219
  8. Schena FP, Gesualdo L. Pathogenetic mechanisms of diabetic nephropathy. J Am Soc Nephrol. 2005;16:S30–S33
  9. Wolfe RA, Ashby VB, Milford EL, et al. Comparison of mortality in all patients on dialysis, patients on dialysis awaiting transplantation, and recipients of a first cadaveric transplant. N Engl J Med. 1999;341:1725–1730
  10. Koya D, Hayashi K, Kitada M, Kashiwagi A, Kikkawa R, Haneda M. Effects of antioxidants in diabetes-induced oxidative stress in the glomeruli of diabetic rats. J Am Soc Nephrol. 2003;14:S250–S253
  11. Kim YH, Goyal M, Kurnit D, et al. Podocyte depletion and glomerulosclerosis have a direct relationship in the PAN-treated rat. Kidney Int. 2001;60:957–968
  12. Siu B, Saha J, Smoyer WE, Sullivan KA, Brosius FC. Reduction in podocyte density as a pathologic feature in early diabetic nephropathy in rodents: prevention by lipoic acid treatment. BMC Nephrol. 2006;7:6
  13. Chow FY, Nikolic-Paterson DJ, Ozols E, Atkins RC, Rollin BJ, Tesch GH. Monocyte chemoattractant protein-1 promotes the development of diabetic renal injury in streptozotocin-treated mice. Kidney Int. 2006;69:73–80
  14. Furuta T, Saito T, Ootaka T, et al. The role of macrophages in diabetic glomerulosclerosis. Am J Kidney Dis. 1993;21:480–485
  15. Chow FY, Nikolic-Paterson DJ, Atkins RC, Tesch GH. Macrophages in streptozotocin-induced diabetic nephropathy: potential role in renal fibrosis. Nephrol Dial Transplant. 2004;19:2987–2996
  16. Chow FY, Nikolic-Paterson DJ, Ozols E, Atkins RC, Tesch GH. Intercellular adhesion molecule-1 deficiency is protective against nephropathy in type 2 diabetic db/db mice. J Am Soc Nephrol. 2005;16:1711–1722
  17. Rodby RA, Rohde R, Evans J, Bain RP, Mulcahy WS, Lewis EJ. The study of the effect of intensity of blood pressure management on the progression of type 1 diabetic nephropathy: study design and baseline patient characteristics. Collaborative Study Group. J Am Soc Nephrol. 1995;5:1775–1781
  18. Dressler RL. Antihypertensive agents for prevention of diabetic nephropathy. Am Fam Physician. 2006;74:77–79
  19. Yamagishi S, Fukami K, Ueda S, Okuda S. Molecular mechanisms of diabetic nephropathy and its therapeutic intervention. Curr Drug Targets. 2007;8:952–959
  20. Caplan AI. The mesengenic process. Clin Plast Surg. 1994;21:429–435
  21. Herrera MB, Bussolati B, Bruno S, Fonsato V, Romanazzi GM, Camussi G. Mesenchymal stem cells contribute to the renal repair of acute tubular epithelial injury. Int J Mol Med. 2004;14:1035–1041
  22. Fang TC, Alison MR, Cook HT, Jeffery R, Wright NA, Poulsom R. Proliferation of bone marrow-derived cells contributes to regeneration after folic acid-induced acute tubular injury. J Am Soc Nephrol. 2005;16:1723–1732
  23. Wong CY, Cheong SK, Mok PL, Leong CF. Differentiation of human mesenchymal stem cells into mesangial cells in post-glomerular injury murine model. Pathology. 2008;40:52–57
  24. Sugimoto H, Mundel TM, Sund M, Xie L, Cosgrove D, Kalluri R. Bone-marrow-derived stem cells repair basement membrane collagen defects and reverse genetic kidney disease. Proc Natl Acad Sci USA. 2006;103:7321–7326
  25. Ezquer FE, Ezquer ME, Parrau DB, Carpio D, Yanez AJ, Conget PA. Systemic administration of multipotent mesenchymal stromal cells reverts hyperglycemia and prevents nephropathy in type 1 diabetic mice. Biol Blood Marrow Transplant. 2008;14:631–640
  26. Lee RH, Seo MJ, Reger RL, et al. Multipotent stromal cells from human marrow home to and promote repair of pancreatic islets and renal glomeruli in diabetic NOD/scid mice. Proc Natl Acad Sci USA. 2006;103:17438–17443
  27. Katoh M, Ohmachi Y, Kurosawa Y, Yoneda H, Tanaka N, Narita H. Effects of imidapril and captopril on streptozotocin-induced diabetic nephropathy in mice. Eur J Pharmacol. 2000;398:381–387
  28. Grover JK, Vats V, Rathi SS, Dawar R. Traditional Indian anti-diabetic plants attenuate progression of renal damage in streptozotocin induced diabetic mice. J Ethnopharmacol. 2001;76:233–238
  29. Thirone AC, Scarlett JA, Gasparetti AL, et al. Modulation of growth hormone signal transduction in kidneys of streptozotocin-induced diabetic animals: effect of a growth hormone receptor antagonist. Diabetes. 2002;51:2270–2281
  30. Okada S, Shikata K, Matsuda M, et al. Intercellular adhesion molecule-1-deficient mice are resistant against renal injury after induction of diabetes. Diabetes. 2003;52:2586–2593
  31. Gabra BH, Sirois P. Beneficial effect of chronic treatment with the selective bradykinin B1 receptor antagonists, R-715 and R-954, in attenuating streptozotocin-diabetic thermal hyperalgesia in mice. Peptides. 2003;24:1131–1139
  32. Dogrul A, Gul H, Yildiz O, Bilgin F, Guzeldemir ME. Cannabinoids blocks tactile allodynia in diabetic mice without attenuation of its antinociceptive effect. Neurosci Lett. 2004;368:82–86
  33. Conget PA, Minguell JJ. Phenotypical and functional properties of human bone marrow mesenchymal progenitor cells. J Cell Physiol. 1999;18:67–73
  34. Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315–317
  35. Kinnaird T, Stabile E, Burnett MS, et al. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res. 2004;94:678–685
  36. Wakasugi S, Maeda S, Shimada K, et al. Structural comparisons between mouse and human prealbumin. J Biochem. 1985;98:1707–1714
  37. Benigni A, Zoja C, Zatelli C, et al. Vasopeptidase inhibitor restores the balance of vasoactives hormones in progressive nephropathy. Kidney Int. 2004;66:1959–1965
  38. Hayakawa M, Shibata M. The in vitro and in vivo inhibition of protein glycosylation and diabetic vascular basement membrane thickening by pyridoxal-5′-phosphate. J Nutr Sci Vitaminol (Tokyo). 1991;37:149–159
  39. Yanez AJ, Bertinat R, Spichiger C, et al. Novel expression of liver FBPase in Langerhans islets of human and rat pancreas. J Cell Physiol. 2005;205:19–24
  40. Duffield JS, Park KM, Hsiao LL, et al. Restoration of tubular epithelial cells during repair of the postischemic kidney occurs independently of bone marrow-derived stem cells. J Clin Invest. 2005;115:1743–1755
  41. Lin F, Moran A, Igarashi P. Intrarenal cells, not bone marrow-derived cells, are the major source for regeneration in postischemic kidney. J Clin Invest. 2005;115:1756–1764
  42. Li R, Perez N, Karumuthil-Melethil S, Vasu C. Bone marrow is a preferential homing site for autoreactive T-cells in type 1 diabetes. Diabetes. 2007;56:2251–2259
  43. Allers K, Kunkel D, Moos V, et al. Migration patterns of nonspecifically activated versus nonactivated nonhuman primate T lymphocytes: preferential homing of activated autologous CD8 + T cells in the rectal mucosa. J Immunother. 2008;31:334–344
  44. Tay YC, Wang Y, Kairaitis L, Rangan GK, Zhang C, Harris DC. Can murine diabetic nephropathy be separated from superimposed acute renal failure?. Kidney Int. 2005;68:391–398
  45. Galkina E, Ley K. Leukocyte recruitment and vascular injury in diabetic nephropathy. J Am Soc Nephrol. 2006;17:368–377
  46. Liu KD, Brakeman PR. Renal repair and recovery. Crit Care Med. 2008;36:S187–S192
  47. Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol. 2008;8:726–736
  48. Imasawa T, Utsunomiya Y, Kawamura T, et al. The potential of bone marrow-derived cells to differentiate to glomerular mesangial cells. J Am Soc Nephrol. 2001;12:1401–1409
  49. Morigi M, Imberti B, Zoja C, et al. Mesenchymal stem cells are renotropic, helping to repair the kidney and improve function in acute renal failure. J Am Soc Nephrol. 2004;15:1794–1804
  50. Semedo P, Palasio CG, Oliveira CD, et al. Early modulation of inflammation by mesenchymal stem cell after acute kidney injury. Int Immunopharmacol. 2009;[Epub ahead of print]
  51. Le Blanc K. Mesenchymal stromal cells: tissue repair and immune modulation. Cytotherapy. 2006;8:559–561
  52. McTaggart SJ, Atkinson K. Mesenchymal stem cells: immunobiology and therapeutic potential in kidney disease. Nephrology. 2007;12:44–52
  53. Togel F, Hu Z, Weiss K, Isaac J, Lange C, Westenfelder C. Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. Am J Physiol Renal Physiol. 2005;289:F31–F42
  54. Togel F, Weiss K, Yang Y, Hu Z, Zhang P, Westenfelder C. Vasculotropic, paracrine actions of infused mesenchymal stem cells are important to the recovery from acute kidney injury. Am J Physiol Renal Physiol. 2007;292:F1626–F1635
  55. Semedo P, Wang PM, Andreucci TH, et al. Mesenchymal stem cells ameliorate tissue damages triggered by renal ischemia and reperfusion injury. Transplant Proc. 2007;39:421–423
  56. Higashiyama R, Inagaki Y, Hong YY, et al. Bone marrow-derived cells express matrix metalloproteinases and contribute to regression of liver fibrosis in mice. Hepatology. 2007;45:213–222

 Financial disclosure: See Acknowledgments on page 1364.

PII: S1083-8791(09)00363-2

doi: 10.1016/j.bbmt.2009.07.022

Biology of Blood and Marrow Transplantation
Volume 15, Issue 11 , Pages 1354-1365 , November 2009

Article Tools

* Image Usage & Resolution