Mesenchymal stem cells from rats with chronic kidney disease exhibit premature senescence and loss of regenerative potential

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Klinkhammer, Barbara Mara ^a   Kramann, Rafael ^a   Mallau, Monika ^a   Makowska, Anna ^a   Van Roeyen, Claudia Renate ^a   Rong, Song ^a   Buecher, Eva Bettina ^a   Boor, Peter ^a,b   Kovacova, Katarina ^a   Zok, Stephanie ^a   Denecke, Bernd ^a   Stuettgen, Esther ^a   Otten, Simon ^a   Floege, Juergen ^a   Kunter, Uta ^a  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b Physics and Informatics   (Slovakia)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BETA GALACTOSIDASE; LYMPHOCYTE ANTIBODY; THY 1 ANTIGEN; CULTURE MEDIUM; CYTOKINE; MESSENGER RNA; SIGNAL PEPTIDE;

ADENINE NEPHROPATHY; ADIPOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CELL FUNCTION; CELL ISOLATION; CELL PROLIFERATION; CELL REGENERATION; CELLULAR SECRETION; CHRONIC KIDNEY DISEASE; CONTROLLED STUDY; CULTURE MEDIUM; DISEASE SEVERITY; GLOMERULOPATHY; HEALING; IN VITRO STUDY; IN VIVO STUDY; MALE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NEPHRITIS; NONHUMAN; RAT; RENAL ARTERY; SENESCENCE; UREMIA; ANIMAL; CELL AGING; CELL CULTURE; CYTOLOGY; DISEASE MODEL; DONOR; ENZYME IMMUNOASSAY; FIBROBLAST; FISCHER 344 RAT; GENETICS; GLOMERULUS; HUMAN; IMMUNOLOGY; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PHARMACOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REGENERATION; RENAL INSUFFICIENCY, CHRONIC; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; ANTIGENS, THY-1; BLOTTING, WESTERN; CELL AGING; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; CYTOKINES; DISEASE MODELS, ANIMAL; FIBROBLASTS; HUMANS; IMMUNOENZYME TECHNIQUES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KIDNEY GLOMERULUS; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; NEPHRITIS; RATS; RATS, INBRED F344; REAL-TIME POLYMERASE CHAIN REACTION; REGENERATION; RENAL INSUFFICIENCY, CHRONIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TISSUE DONORS;

EID: 84899860592     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092115     Document Type: Article

References (52)

1. Lange C, Togel F, Ittrich H, Clayton F, Nolte-Ernsting C, et al. (2005) Administered mesenchymal stem cells enhance recovery from ischemia/reperfusion- induced acute renal failure in rats. Kidney Int 68: 1613-1617. (Pubitemid 43169906)
2. Togel F, Hu Z, Weiss K, Isaac J, Lange C, et al. (2005) Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. Am J Physiol Renal Physiol 289: F31-42. (Pubitemid 40863570)
3. Duffield JS, Park KM, Hsiao LL, Kelley VR, Scadden DT, et al. (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. (Pubitemid 40979713)
4. Breitbach M, Bostani T, Roell W, Xia Y, Dewald O, et al. (2007) Potential risks of bone marrow cell transplantation into infarcted hearts. Blood 110: 1362-1369. (Pubitemid 47281438)
5. Kunter U, Rong S, Boor P, Eitner F, Muller-Newen G, et al. (2007) Mesenchymal stem cells prevent progressive experimental renal failure but maldifferentiate into glomerular adipocytes. J Am Soc Nephrol 18: 1754-1764. (Pubitemid 46870312)
6. di Bonzo LV, Ferrero I, Cravanzola C, Mareschi K, Rustichell D, et al. (2008) Human mesenchymal stem cells as a two-edged sword in hepatic regenerative medicine: engraftment and hepatocyte differentiation versus profibrogenic potential. Gut 57: 223-231. (Pubitemid 351158051)
7. Choi S, Park M, Kim J, Hwang S, Park S, et al. (2009) The role of mesenchymal stem cells in the functional improvement of chronic renal failure. Stem Cells Dev 18: 521-529.
8. Cavaglieri RC, Martini D, Sogayar MC, Noronha IL (2009) Mesenchymal stem cells delivered at the subcapsule of the kidney ameliorate renal disease in the rat remnant kidney model. Transplant Proc 41: 947-951.
9. Lee SR, Lee SH, Moon JY, Park JY, Lee D, et al. Repeated administration of bone marrow-derived mesenchymal stem cells improved the protective effects on a remnant kidney model. Ren Fail 32: 840-848.
10. Li B, Morioka T, Uchiyama M, Oite T (2006) Bone marrow cell infusion ameliorates progressive glomerulosclerosis in an experimental rat model. Kidney Int 69: 323-330. (Pubitemid 43323083)
11. Kisseberth WC, Brettingen NT, Lohse JK, Sandgren EP (1999) Ubiquitous expression of marker transgenes in mice and rats. Dev Biol 214: 128-138. (Pubitemid 29463361)
12. Kunter U, Rong S, Djuric Z, Boor P, Muller-Newen G, et al. (2006) Transplanted mesenchymal stem cells accelerate glomerular healing in experimental glomerulonephritis. J Am Soc Nephrol 17: 2202-2212. (Pubitemid 44141910)
13. Kunter U, Rong S, Moeller MJ, Floege J (2011) Mesenchymal stem cells as a therapeutic approach to glomerular diseases: benefits and risks. Kidney inter, Suppl 1: 68.
14. Liu Y, Song J, Liu W, Wan Y, Chen X, et al. (2003) Growth and differentiation of rat bone marrow stromal cells: does 5-azacytidine trigger their cardiomyogenic differentiation? Cardiovasc Res 58: 460-468. (Pubitemid 36570404)
15. Hanssen L, Frye BC, Ostendorf T, Alidousty C, Djudjaj S, et al. (2011) Y-box binding protein-1 mediates profibrotic effects of calcineurin inhibitors in the kidney. J Immunol 187: 298-308.
16. Ostendorf T, van Roeyen CR, Peterson JD, Kunter U, Eitner F, et al. (2003) A fully human monoclonal antibody (CR002) identifies PDGF-D as a novel mediator of mesangioproliferative glomerulonephritis. J Am Soc Nephrol 14: 2237-2247. (Pubitemid 37052369)
17. Boor P, Konieczny A, Villa L, Schult AL, Bucher E, et al. (2007) Complement C5 mediates experimental tubulointerstitial fibrosis. J Am Soc Nephrol 18: 1508-1515. (Pubitemid 46717517)
18. Neven E, D'Haese PC (2011) Vascular calcification in chronic renal failure: what have we learned from animal studies? Circ Res 108: 249-264.
19. Ostendorf T, Kunter U, Eitner F, Loos A, Regele H, et al. (1999) VEGF(165) mediates glomerular endothelial repair. J Clin Invest 104: 913-923. (Pubitemid 29536341)
20. Eitner F, Ostendorf T, Van Roeyen C, Kitahara M, Li X, et al. (2002) Expression of a novel PDGF isoform, PDGF-C, in normal and diseased rat kidney. J Am Soc Nephrol 13: 910-917. (Pubitemid 34274087)
21. Boor P, Celec P, Martin IV, Villa L, Hodosy J, et al. (2011) The peroxisome proliferator-activated receptor-alpha agonist, BAY PP1, attenuates renal fibrosis in rats. Kidney Int 80: 1182-1197.
22. Wagner W, Horn P, Castoldi M, Diehlmann A, Bork S, et al. (2008) Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLoS One 3: e2213.
23. Sethe S, Scutt A, Stolzing A (2006) Aging of mesenchymal stem cells. Ageing Res Rev 5: 91-116. (Pubitemid 43139669)
24. Kramann R, Couson SK, Neuss S, Kunter U, Bovi M, et al. (2011) Exposure to uremic serum induces a procalcific phenotype in human mesenchymal stem cells. Arterioscler Thromb Vasc Biol 31: e45-54.
25. Semedo P, Correa-Costa M, Antonio Cenedeze M, Maria Avancini Costa Malheiros D, Antonia dos Reis M, et al. (2009) Mesenchymal stem cells attenuate renal fibrosis through immune modulation and remodeling properties in a rat remnant kidney model. Stem Cells 27: 3063-3073.
26. Yuen DA, Connelly KA, Advani A, Liao C, Kuliszewski MA, et al. 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.
27. Drewa T, Joachimiak R, Kaznica A, Flisinski M, Brymora A, et al. (2008) Bone marrow progenitors from animals with chronic renal failure lack capacity of in vitro proliferation. Transplant Proc 40: 1668-1673. (Pubitemid 351853187)
28. Buemi M, Costa C, Floccari F, Coppolino G, Campo S, et al. (2010) Genomic damage in endothelial progenitor cells from uremic patients in hemodialysis. J Nephrol 23: 328-334.
29. Betjes MG, Langerak AW, van der Spek A, de Wit EA, Litjens NH (2011) Premature aging of circulating T cells in patients with end-stage renal disease. Kidney Int 80: 208-217.
30. de Groot K, Bahlmann FH, Bahlmann E, Menne J, Haller H, et al. (2005) Kidney graft function determines endothelial progenitor cell number in renal transplant recipients. Transplantation 79: 941-945. (Pubitemid 40586867)
31. de Groot K, Bahlmann FH, Sowa J, Koenig J, Menne J, et al. (2004) Uremia causes endothelial progenitor cell deficiency. Kidney Int 66: 641-646. (Pubitemid 38982006)
32. van Koppen A, Joles JA, Bongartz LG, van den Brandt J, Reichardt HM, et al. Healthy Bone Marrow Cells Reduce Progression Of Kidney Failure Better Than Ckd Bone Marrow Cells In Rats With Established Chronic Kidney Disease. Cell Transplant.
33. Yang HC, Rossini M, Ma LJ, Zuo Y, Ma J, et al. (2011) Cells Derived from Young Bone Marrow Alleviate Renal Aging. J Am Soc Nephrol.
34. Noh H, Yu MR, Kim HJ, Jeon JS, Kwon SH, et al. (2012) Uremia induces functional incompetence of bone marrow-derived stromal cells. Nephrol Dial Transplant.
35. Li Z, Liu C, Xie Z, Song P, Zhao RC, et al. (2011) Epigenetic dysregulation in mesenchymal stem cell aging and spontaneous differentiation. PLoS One 6: e20526.
36. Lo LJ, Go AS, Chertow GM, McCulloch CE, Fan D, et al. (2009) Dialysis-requiring acute renal failure increases the risk of progressive chronic kidney disease. Kidney Int 76: 893-899.
37. Urish KL, Vella JB, Okada M, Deasy BM, Tobita K, et al. (2009) Antioxidant levels represent a major determinant in the regenerative capacity of muscle stem cells. Mol Biol Cell 20: 509-520.
38. Kanda Y, Hinata T, Kang SW, Watanabe Y (2011) Reactive oxygen species mediate adipocyte differentiation in mesenchymal stem cells. Life Sci 89: 250-258.
39. Graham GJ, Wright EG, Hewick R, Wolpe SD, Wilkie NM, et al. (1990) Identification and characterization of an inhibitor of haemopoietic stem cell proliferation. Nature 344: 442-444.
40. Sugawara J, Mitsui-Saito M, Hayashi C, Hoshiai T, Senoo M, et al. (2005) Decrease and senescence of endothelial progenitor cells in patients with preeclampsia. J Clin Endocrinol Metab 90: 5329-5332. (Pubitemid 41262296)
41. Moerman EJ, Teng K, Lipschitz DA, Lecka-Czernik B (2004) Aging activates adipogenic and suppresses osteogenic programs in mesenchymal marrow stroma/stem cells: the role of PPAR-gamma2 transcription factor and TGF-beta/BMP signaling pathways. Aging Cell 3: 379-389. (Pubitemid 40246708)
42. Horn P, Bokermann G, Cholewa D, Bork S, Walenda T, et al. (2010) Impact of individual platelet lysates on isolation and growth of human mesenchymal stromal cells. Cytotherapy 12: 888-898.
43. Ball SG, Shuttleworth CA, Kielty CM (2012) Inhibition of Platelet-Derived Growth Factor Receptor Signaling Regulates Oct4 and Nanog Expression, Cell Shape and Mesenchymal Stem Cell Potency. Stem Cells.
44. Asanuma H, Vanderbrink BA, Campbell MT, Hile KL, Zhang H, et al. Arterially delivered mesenchymal stem cells prevent obstruction-induced renal fibrosis. J Surg Res 168: e51-59.
45. Ninichuk V, Gross O, Segerer S, Hoffmann R, Radomska E, et al. (2006) Multipotent mesenchymal stem cells reduce interstitial fibrosis but do not delay progression of chronic kidney disease in collagen4A3-deficient mice. Kidney Int 70: 121-129. (Pubitemid 44000128)
46. Nakanishi C, Nagaya N, Ohnishi S, Yamahara K, Takabatake S, et al. (2011) Gene and protein expression analysis of mesenchymal stem cells derived from rat adipose tissue and bone marrow. Circ J 75: 2260-2268.
47. Choi H, Lee RH, Bazhanov N, Oh JY, Prockop DJ (2011) Anti-inflammatory protein TSG-6 secreted by activated MSCs attenuates zymosan-induced mouse peritonitis by decreasing TLR2/NF-kappaB signaling in resident macrophages. Blood 118: 330-338.
48. Montzka K, Fuhrmann T, Muller-Ehmsen J, Woltje M, Brook GA (2010) Growth factor and cytokine expression of human mesenchymal stromal cells is not altered in an in vitro model of tissue damage. Cytotherapy 12: 870-880.
49. Roemeling-van Rhijn M, Reinders ME, de Klein A, Douben H, Korevaar SS, et al. (2012) Mesenchymal stem cells derived from adipose tissue are not affected by renal disease. Kidney Int 82: 748-758.
50. Krtolica A, Campisi J (2003) Integrating epithelial cancer, aging stroma and cellular senescence. Adv Gerontol 11: 109-116.
51. Salazar KD, Lankford SM, Brody AR (2009) Mesenchymal stem cells produce Wnt isoforms and TGF-beta1 that mediate proliferation and procollagen expression by lung fibroblasts. Am J Physiol Lung Cell Mol Physiol 297: L1002-1011.
52. Ohnishi S, Sumiyoshi H, Kitamura S, Nagaya N (2007) Mesenchymal stem cells attenuate cardiac fibroblast proliferation and collagen synthesis through paracrine actions. FEBS Lett 581: 3961-3966. (Pubitemid 47212103)