Limited immune-modulating activity of porcine mesenchymal stromal cells abolishes their protective efficacy in acute kidney injury

Stem Cells and Development

Volumn 19, Issue 5, 2010, Pages 719-729

  Brunswig Spickenheier, Bärbel ^a   Boche, Janna ^a   Westenfelder, Christof ^b   Peimann, Frauke ^a   Gruber, Achim D ^c   Jaquet, Kai ^d   Krause, Korff ^d   Zustin, Jozef ^a   Zander, Axel R ^a   Lange, Claudia ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d DEPARTMENT OF CARDIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; INTERLEUKIN 6; SOMATOMEDIN C; TESTIS DETERMINING FACTOR; VASCULOTROPIN A;

ALLOGENEIC STEM CELL TRANSPLANTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; AUTOLOGOUS STEM CELL TRANSPLANTATION; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE MODEL; FEMALE; HISTOPATHOLOGY; IMMUNOMODULATION; IN VITRO STUDY; KIDNEY FUNCTION; KIDNEY INJURY; MALE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MIXED LYMPHOCYTE REACTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SECRETION; RAT; RENAL PROTECTION; SPECIES DIFFERENCE; SWINE; ACUTE KIDNEY INJURY; ALLOTRANSPLANTATION; ANIMAL; BIOSYNTHESIS; HUMAN; IMMUNOLOGY; MESENCHYMAL STROMA CELL; MIXED LYMPHOCYTE CULTURE; PROCEDURES; REPERFUSION INJURY;

ANIMALIA; RATTUS; RODENTIA; SUIDAE; SUS;

ACUTE KIDNEY INJURY; ANIMALS; FEMALE; HUMANS; INTERLEUKIN-6; LYMPHOCYTE CULTURE TEST, MIXED; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; RATS; REPERFUSION INJURY; SPECIES SPECIFICITY; SWINE; TRANSPLANTATION, HOMOLOGOUS;

EID: 77952911619     PISSN: 15473287     EISSN: None     Source Type: Journal    
DOI: 10.1089/scd.2009.0494     Document Type: Article

References (49)

1. Goldberg R and P Dennen. (2008). Long-term outcomes of acute kidney injury. Adv Chronic Kidney Dis 15:297-307.
2. Lange C, F Tögel, H Ittrich, F Clayton, C Nolte-Ernsting, AR Zander and C Westenfelder. (2005). Administered mesenchymal stem cells enhance recovery from ischemia/reperfusion-induced acute renal failure in rats. Kidney Int 68:1613-1617. (Pubitemid 43169906)
3. Tögel F, Z Hu, K Weiss, J Isaac, C Lange and C Westenfelder. (2005). Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiationindependent mechanisms. Am J Physiol Renal Physiol 289:F31-F42. (Pubitemid 40863570)
4. Aggarwal S and MF Pittenger. (2005). Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105:1815-1822.
5. Haynesworth SE, MA Baber and AI Caplan. (1996). Cytokine expression by human marrow-derived mesenchymal progenitor cells in vitro: effects of dexamethasone and IL-1 alpha. J Cell Physiol 166:585-592.
6. Koç ON and HM Lazarus. (2001). Mesenchymal stem cells: heading into the clinic. Bone Marrow Transplant 27:235-239.
7. Le Blanc K and O Ringdén. (2007). Immunomodulation by mesenchymal stem cells and clinical experience. J Intern Med 262:509-525. (Pubitemid 47620502)
8. Uccelli A, L Moretta and V Pistoia. (2006). Immunoregulatory function of mesenchymal stem cells. Eur J Immunol 36:2566-2573. (Pubitemid 44608440)
9. Giordano A, U Galderisi and IR Marino. (2007). From the laboratory bench to the patient's bedside: an update on clinical trials with mesenchymal stem cells. J Cell Physiol 211:27-35.
10. Le Blanc K, F Frassoni, L Ball, F Locatelli, H Roelofs, I Lewis, E Lanino, B Sundberg, ME Bernardo, M Remberger, G Dini, RM Egeler, A Bacigalupo, W Fibbe and O Ringdén; Developmental Committee of the European Group for Blood and Marrow Transplantation. (2008). Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 371:1579-1586.
11. Imberti B, M Morigi, S Tomasoni, C Rota, D Corna, L Longaretti, D Rottoli, F Valsecchi, A Benigni, J Wang, M Abbate, C Zoja and G Remuzzi. (2007). Insulin-like growth factor-1 sustains stem cell mediated renal repair. J Am Soc Nephrol 18:2921-2928.
12. Morigi M, B Imberti, C Zoja, D Corna, S Tomasoni, M Abbate, D Rottoli, S Angioletti, A Benigni, N Perico, M Alison and G Remuzzi. (2004). Mesenchymal stem cells are renotropic, helping to repair the kidney and improve function in acute renal failure. J Am Soc Nephrol 15:1794-1804.
13. Morigi M, M Introna, B Imberti, D Corna, M Abbate, C Rota, D Rottoli, A Benigni, N Perico, C Zoja, A Rambaldi, A Remuzzi and G Remuzzi. (2008). Human bone marrow mesenchymal stem cells accelerate recovery of acute renal injury and prolong survival in mice. Stem Cells 26:2075-2082.
14. Herrera MB, B Bussolati, S Bruno, V Fonsato, GM Romanazzi and G Camussi. (2004). Mesenchymal stem cells contribute to the renal repair of acute tubular epithelial injury. Int J Mol Med 14:1035-1041.
15. Kunter U, S Rong, Z Dj uric, P Boor, G Müller-Newen, D Yu and J Floege. (2006). Transplanted mesenchymal stem cells accelerate glomerular healing in experimental glomerulonephritis. J Am Soc Nephrol 17:2202-2212.
16. Kunter U, S Rong, P Boor, F Eitner, G Müller-Newen, Z Dj uric, CR van Roeyen, A Konieczny, T Ostendorf, L Villa, M Milovanceva-Popovska, D Kerj aschki and J Floege. (2007). Mesenchymal stem cells prevent progressive experimental renal failure but maldifferentiate into glomerular adipocytes. J Am Soc Nephrol 18:1754-1764.
17. Semedo P, CG Palasio, CD Oliveira, CQ Feitoza, GM Gonçalves, MA Cenedeze, PM Wang, VP Teixeira, MA Reis, A Pacheco-Silva and NO Câmara. (2009). Early modulation of inflammation by mesenchymal stem cell after acute kidney injury. Int Immunopharmacol 9:677-682.
18. Tögel F, J Isaac, Z Hu, K Weiss and C Westenfelder. (2005). Renal SDF-1 signals mobilization and homing of CXCR4-positive cells to the kidney after ischemic injury. Kidney Int 67:1772-1784.
19. Tögel F, K Weiss, Y Yang, Z Hu, P Zhang and C Westenfelder. (2007). Vasculotropic, paracrine actions of infused mesenchymal stem cells are important to the recovery from acute kidney injury. Am J Physiol Renal Physiol 292:F1626-F1635.
20. Ittrich H, C Lange, F Tögel, AR Zander, H Dahnke, C Westenfelder, G Adam and C Nolte-Ernsting. (2007). In vivo magnetic resonance imaging of iron oxide-labeled, arteriallyinjected mesenchymal stem cells in kidneys of rats with acute ischemic kidney injury: detection and monitoring at 3T. J Magn Reson Imaging 25:1179-1191.
21. Lieberthal W and SK Nigam. (2000). Acute renal failure. II. Experimental models of acute renal failure: imperfect but indispensable. Am J Physiol Renal Physiol 278:F1-F12.
22. Behr L, M Hekmati, A Lucchini, K Houcinet, AM Faussat, N Borenstein, LH Noel, M Lelievre-Pegorier and K Laborde. (2009). Evaluation of the effect of autologous mesenchymal stem cell injection in a large-animal model of bilateral kidney ischaemia reperfusion injury. Cell Prolif 42:284-297.
23. Lange C, J Schroeder, N Stute, MV Lioznov and AR Zander. (2005). High-potential human mesenchymal stem cells. Stem Cells Dev 14:70-80.
24. Lange C, F Cakiroglu, AN Spiess, H Cappallo-Obermann, J Dierlamm and AR Zander. (2007). Accelerated and safe expansion of human mesenchymal stromal cells in animal serum-free medium for transplantation and regenerative medicine. J Cell Physiol 213:18-26.
25. Ikawa T, A Kakegawa, T Nagano, H Ando, Y Yamakoshi, T Tanabe, JP Simmer, CC Hu, M Fukae and S Oida. (2005). Porcine amelogenin is expressed from the X and Y chromosomes. J Dent Res 84:144-148.
26. Fang L, C Lange, M Engel, AR Zander and B Fehse. (2006). Sensitive balance of suppressing and activating effects of mesenchymal stem cells on T-cell proliferation. Transplantation 82:1370-1373.
27. Dominici M, K Le Blanc, I Mueller, I Slaper-Cortenbach, F Marini, D Krause, R Deans, A Keating, Dj Prockop and E Horwitz. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315-317.
28. Tögel F, A Cohen, P Zhang, Y Yang, Z Hu and C Westenfelder. (2009). Autologous and allogeneic marrow stromal cells are safe and effective for the treatment of acute kidney injury. Stem Cells Dev 18:475-485.
29. Polchert D, J Sobinsky, G Douglas, M Kidd, A Moadsiri, E Reina, K Genrich, S Mehrotra, S Setty, B Smith and A Bartholomew. (2008). IFN-gamma activation of mesenchymal stem cells for treatment and prevention of graft versus host disease. Eur J Immunol 38:1745-1755.
30. Breitbach M, T Bostani, W Roell, Y Xia, O Dewald, JM Nygren, JW Fries, K Tiemann, H Bohlen, J Hescheler, A Welz, W Bloch, SE Jacobsen and BK Fleischmann. (2007). Potential risks of bone marrow cell transplantation into infarcted hearts. Blood 110:1362-1369.
31. Lyon MB, MA Orvieto, KC Zorn, SR Tolhurst, DE Rapp, AA Mikhail, CB Brendler and AL Shalhav. (2007). Effect of renal ischemia in laparoscopic acute versus chronic solitary kidney model. Urology 69:402-406.
32. Orvieto MA, SR Tolhurst, MS Chuang, MB Lyon, CR Ritch, DE Rapp and AL Shalhav. (2005). Defining maximal renal tolerance to warm ischemia in porcine laparoscopic and open surgery model. Urology 66:1111-1115.
33. Nguyen MT and P Devarajan. (2008). Biomarkers for the early detection of acute kidney injury. Pediatr Nephrol 23:2151-2157.
34. Vaidya VS, MA Ferguson and JV Bonventre. (2008). Biomarkers of acute kidney injury. Annu Rev Pharmacol Toxicol 48:463-493.
35. Bonventre JV and A Zuk. (2004). Ischemic acute renal failure: an inflammatory disease? Kidney Int 66:480-485.
36. Lee RH, AA Pulin, MJ Seo, DJ Kota, J Ylostalo, BL Larson, L Semprun-Prieto, P Delafontaine and DJ Prockop. (2009). Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the antiinflammatory protein TSG-6. Cell Stem Cell 5:54-63.
37. Humphreys BD and JV Bonventre. (2008). Mesenchymal stem cells in acute kidney injury. Annu Rev Med 59:311-325.
38. Saalmüller A, T Pauly, BJ Höhlich and E Pfaff. (1999). Characterization of porcine T lymphocytes and their immune response against viral antigens. J Biotechnol 73:223-233.
39. Duffield JS, KM Park, LL Hsiao, VR Kelley, DT Scadden, T Ichimura and JV Bonventre. (2005). Restoration of tubular epithelial cells during repair of the postischemic kidney occurs independently of bone marrow-derived stem cells. J Clin Invest 115:1743-1755.
40. Humphreys BD, MT Valerius, A Kobayashi, JW Mugford, S Soeung, JS Duffield, AP McMahon and JV Bonventre. (2008). Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2:284-291.
41. Burne MJ, F Daniels, A El Ghandour, S Mauiyyedi, RB Colvin, MP O'Donnell and H Rabb. (2001). Identification of the CD4 (+) T cell as a major pathogenic factor in ischemic acute renal failure. J Clin Invest 108:1283-1290.
42. Ober BT, A Summerfield, C Mattlinger, KH Wiesmüller, G Jung, E Pfaff, A Saalmüller and HJ Rziha. (1998). Vaccine-induced, pseudorabies virus-specific, extrathymic CD4+CD8+ memory T-helper cells in swine. J Virol 72:4866-4873.
43. Griesemer AD, JC Lamattina, M Okumi, JD Etter, A Shimizu, DH Sachs and K Yamada. (2008). Linked suppression across an MHC-mismatched barrier in a miniature swine kidney transplantation model. J Immunol 181:4027-4036.
44. Di Nicola M, C Carlo-Stella, M Magni, M Milanesi, PD Longoni, P Matteucci, S Grisanti and AM Gianni. (2002). Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99:3838-3843.
45. Schroder K, PJ Hertzog, T Ravasi and DA Hume. (2004). Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 75:163-189.
46. McLoughlin RM, BJ Jenkins, D Grail, AS Williams, CA Fielding, CR Parker, M Ernst, N Topley and SA Jones. (2005). IL-6 transsignaling via STAT3 directs T cell infiltration in acute inflammation. Proc Natl Acad Sci USA 102:9589-9594.
47. Yokota N, M Burne-Taney, L Racusen and H Rabb. (2003). Contrasting roles for STAT4 and STAT6 signal transduction pathways in murine renal ischemia-reperfusion injury. Am J Physiol Renal Physiol 285:F319-F325.
48. Sad S, R Marcotte and TR Mosmann. (1995). Cytokine-induced differentiation of precursor mouse CD8+ T cells into cytotoxic CD8+ T cells secreting Th1 or Th2 cytokines. Immunity 2:271-279.
49. Gooch A, Doty J, Flores J, Swenson L, Toegel FE, Reiss GR, Lange C, Zander AR, Hu Z, Poole S, Zhang P and Westenfelder C. (2008). Initial report on a phase I clinical trial: Prevention and treatment of post-operative Acute Kidney Injury with allogeneic Mesenchymal Stem Cells in patients who require on-pump cardiac surgery. Cell Ther Transplant 1; doi:10. 3205/ctt-2008-en- 000028.01. [Epub ahead of print]