Impact of the uremic milieu on the osteogenic potential of mesenchymal stem cells

PLoS ONE

Volumn 10, Issue 1, 2015, Pages

  Lanza, Diana ^a   Perna, Alessandra F ^a   Oliva, Adriana ^a   Vanholder, Raymond ^b   Pletinck, Anneleen ^b   Guastafierro, Salvatore ^a   Di Nunzio, Annarita ^a   Vigorito, Carmela ^a   Capasso, Giovambattista ^a   Jankowski, Vera ^c   Jankowski, Joachim ^c   Ingrosso, Diego ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b GHENT UNIVERSITY HOSPITAL   (Belgium)

^c RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 CRESYLGLUCURONIDE; 4 CRESYLSULFATE; BONE MORPHOGENETIC PROTEIN 2; CINACALCET; COLLAGEN TYPE 1; HOMOCYSTEINE; INDICAN; N(G),N(G) DIMETHYLARGININE; OSTEOCALCIN; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPONTIN; OSTEOPROTEGERIN; PARATHYROID HORMONE; UNCLASSIFIED DRUG; UREMIC TOXIN; BMP2 PROTEIN, HUMAN; CULTURE MEDIUM;

ADULT; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG EFFECT; FEMALE; HEMODIALYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MESENCHYMAL STEM CELL; OSSIFICATION; OSTEOCLASTOGENESIS; OSTEOLYSIS; STEM CELL CULTURE; THERAPY EFFECT; UREMIA; BLOOD; CASE CONTROL STUDY; CELL CULTURE; CELL SURVIVAL; CULTURE MEDIUM; DRUG EFFECTS; HEMOFILTRATION; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; SOLUBILITY; TUMOR MICROENVIRONMENT;

ADULT; BONE MORPHOGENETIC PROTEIN 2; CASE-CONTROL STUDIES; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; CELLULAR MICROENVIRONMENT; CINACALCET HYDROCHLORIDE; COLLAGEN TYPE I; CULTURE MEDIA; FEMALE; HEMOFILTRATION; HUMANS; MALE; MESENCHYMAL STROMAL CELLS; OSTEOCALCIN; OSTEOGENESIS; OSTEOPONTIN; OSTEOPROTEGERIN; RANK LIGAND; SOLUBILITY; UREMIA;

EID: 84922113035     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0116468     Document Type: Article

References (61)

1. Kidney Disease: Improving Global Outcomes (KDIGO) CKD-MBD Work Group (2009) KDIGO clinical practice guideline for the diagnosis, evaluation, prevention, and treatment of Chronic Kidney Disease- Mineral and Bone Disorder (CKD-MBD). Kidney Int Suppl 113: : S1-130.
2. Almeras C, Argilés A (2009) The general picture of uremia. Semin Dial 22:329-333. doi: 10.1111/j. 1525-139X.2009.00575.x PMID: 19708976
3. Cunningham J, Locatelli F, Rodriguez M (2011) Secondary hyperparathyroidism: pathogenesis, disease progression, and therapeutic options. Clin J Am Soc Nephrol 6(4): 913. doi: 10.2215/CJN.06040710 PMID: 21454719
4. Iwasaki Y, Yamato H, Nii-Kono T, Fujieda A, Uchida M, et al. (2006) Uremic toxin and bone metabolism. J Bone Miner Metab 24(2): 172-175. doi: 10.1007/s00774-005-0667-7 PMID: 16502128
5. Tanaka H, Iwasaki Y, Yamato H, Mori Y, Komaba H, et al. (2013) p-Cresyl sulfate induces osteoblast dysfunction through activating JNK and p38 MAPK pathways. Bone 56(2):347-354. doi: 10.1016/j.bone.2013.07.002 PMID: 23851293
6. Liabeuf S, Glorieux G, Lenglet A, Diouf M, Schepers E, et al. (2013) Does p-cresylglucuronide have the same impact on mortality as other protein-bound uremic toxins? PLoS One 24; 8(6): e67168. doi: 10. 1371/journal.pone.0067168
7. Xiao ZS, Quarles LD, Chen QQ, Yu YH, Qu HP, et al. (2001) Effect of asymmetric dimethylarginine on osteoblastic differentiation. Kidney Int 60(5): 1699-1704. doi: 10.1046/j.1523-1755.2001.00011.x PMID: 11703587
8. McLean RR, Jacques PF, Selhub J, Tucker KL, Samelson EJ, et al. (2004) Homocysteine as a predictive factor for hip fracture in older persons. N Engl J Med 350(20): 2042. doi: 10.1056/NEJMoa032739 PMID: 15141042
9. Yang J, Hu X, Zhang Q, Cao H, Wang J, et al. (2012) Homocysteine level and risk of fracture: A metaanalysis and systematic review. Bone 51(3): 376-382. doi: 10.1016/j.bone.2012.05.024 PMID: 22749888
10. Nii-Kono T, Iwasaki Y, Uchida M, Fujieda A, Hosokawa A, et al. (2007) Indoxyl sulfate induces skeletal resistance to parathyroid hormone in cultured osteoblastic cells. Kidney Int 71(8): 738. doi: 10.1038/sj.ki.5002097 PMID: 17264878
11. Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, et al. (2005) Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 7(5): 393-395. doi: 10.1080/14653240500319234 PMID: 16236628
12. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, et al. (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284(5411): 143-147. doi: 10.1126/science.284.5411.143 PMID: 10102814
13. Schneider RK, Puellen A, Kramann R, Raupach K, Bornemann J, et al. (2010) The osteogenic differentiation of adult bone marrow and perinatal umbilical mesenchymal stem cells and matrix remodelling in three-dimensional collagen scaffolds. Biomaterials 31:467-480. doi: 10.1016/j.biomaterials.2009.09. 059 PMID: 19815272
14. Rodriguez JP, Gonzalez M, Rios S (2004) Cytoskeletal Organization of Human Mesenchymal Stem Cells (MSC) Changes During Their Osteogenic Differentiation. J Cell Biochem; 93: 721-731. doi: 10.1002/jcb.20234
15. Tanaka H, Mine T, Ogasa H, Taguchi T, Liang CT (2011) Expression of RANKL/OPG during bone remodeling in vivo. Biochem Biophys Res Commun 411(4):690-694. doi: 10.1016/j.bbrc.2011.07.001 PMID: 21771583
16. Kazama J (2004) Osteoprotegerin and bone mineral metabolism in renal failure. Curr Opin Nephrol Hypertens 13:411-415. doi: 10.1097/01.mnh.0000133982.40182.8a PMID: 15199291
17. Doumouchtsis KK, Kostakis AI, Doumouchtsis SK, Tziamalis MP, Tsigris C, et al. (2007) sRANKL/ osteoprotegerin complex and biochemical markers in a cohort of male and female hemodialysis patients. J Endocrinol Invest 30:762-766. doi: 10.1007/BF03350814 PMID: 17993768
18. Giachelli CM, Steitz S (2000) Osteopontin: a versatile regulator of inflammation and biomineralization. Matrix Biol 19: 615-622. doi: 10.1016/S0945-053X(00)00108-6 PMID: 11102750
19. Nemcsik J, Kiss I, Tislér A (2012) Arterial stiffness, vascular calcification and bone metabolism in chronic kidney disease. World J Nephrol 1(1): 25-34. doi: 10.5527/wjn.v1.i1.25 PMID: 24175239
20. El-Abbadi MM, Pai AS, Leaf EM, Yang HY, Bartley BA, et al. (2009) Phosphate feeding induces arterial medial calcification in uremic mice: role of serum phosphorus, fibroblast growth factor-23, and osteopontin. Kidney Int 75(12): 1297-1307. doi: 10.1038/ki.2009.83 PMID: 19322138
21. Nitta K, Ishizuka T, Horita S, Hayashi T, Ajiro A, et al. (2001) Soluble osteopontin and vascular calcification in hemodialysis patients. Nephron 89(4): 455-458. doi: 10.1159/000046119 PMID: 11721165
22. Calvo MS, Eyre DR, Gundberg CM (1996) Molecular basis and clinical application of biological markers of bone turnover. Endocr Rev 17(4): 333-368. doi: 10.1210/er.17.4.333 PMID: 8854049
23. Takano M, Okano K, Tsuruta Y, Yamashita T, Echida Y, et al. (2011) Correlation of new bone metabolic markers with conventional biomarkers in hemodialysis patients. Clin Invest Med 34(5): E267. PMID: 21968268
24. Garrett IR, Chen D, Gutierrez G, Zhao M, Escobedo A, et al. (2003) Selective inhibitors of the osteoblast proteasome stimulate bone formation in vivo and in vitro. J Clin Invest 111(11): 1771-1782. doi: 10.1172/JCI16198 PMID: 12782679
25. Costa E, Coimbra J, Catarino C, Ribeiro S, Reis F, et al. (2012) Major determinants of BMP-2 serum levels in hemodialysis patients. Ren Fail 34(10): 1355-1358. doi: 10.3109/0886022X.2012.725289 PMID: 23016911
26. Dalfino G, Simone S, Porreca S, Cosola C, Balestra C, et al. (2010) Bone morphogenetic protein-2 may represent the molecular link between oxidative stress and vascular stiffness in chronic kidney disease. Atherosclerosis 211(2): 418-423. doi: 10.1016/j.atherosclerosis.2010.04.023 PMID: 20537331
27. Ureña P, Hruby M, Ferreira A, Ang KS, de Vernejoul MC (1996) Plasma total versus bone alkaline phosphatase as markers of bone turnover in hemodialysis patients. J Am Soc Nephrol 7(3): 506-512. PMID: 8704118
28. Puchtler H, Meloan SN, Terry MS (1969) On the history and mechanism of alizarin and alizarin red S stains for calcium. J Histochem Cytochem 17(2): 110-124. doi: 10.1177/17.2.110 PMID: 4179464
29. Lievremont M, Potus J, Guillou B (1982) Use of alizarin red S for histochemical staining of Ca2+ in the mouse; some parameters of the chemical reaction in vitro. Acta Anat (Basel) 114(3): 268-280. doi: 10. 1159/000145596
30. Stanford CM, Jacobson PA, Eanes ED, Lembke LA, Midura RJ (1995) Rapidly forming apatitic mineral in an osteoblastic cell line (UMR 106-01 BSP). J Biol Chem 270(16): 9420-9428. doi: 10.1074/jbc.270.16.9420 PMID: 7721867
31. Gregory CA, Gunn WG, Peister A, Prockop DJ (2004) An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction. Anal Biochem 329(1): 77-84. doi: 10.1016/j.ab.2004.02.002 PMID: 15136169
32. Perna AF, Luciano MG, Ingrosso D, Raiola I, Pulzella P, et al. (2009) Hydrogen sulphide-generating pathways in haemodialysis patients: a study on relevant metabolites and transcriptional regulation of genes encoding for key enzymes. Nephrol Dial Transplant 24(12): 3756-3763. doi: 10.1093/ndt/ gfp378 PMID: 19654230
33. 2-induced oxidative damage-implications for the treatment of osteoporosis. Free Radic Biol Med 50(10): 1314-1323. doi: 10.1016/j.freeradbiomed.2011.02.016 PMID: 21354302
34. Liao C, Hua Y (2013) Effect of hydrogen sulfide on the expression of osteoprotegerin and receptor activator of NF-kB ligand in human periodontal ligament cells induced by tension-force stimulation. Arch Oral Biol 58:1784-1790. doi: 10.1016/j.archoralbio.2013.08.004 PMID: 24200305
35. Feigenbaum J, Neuberg C (1941) Simplified method for the preparation of aromatic sulfuric acid esters. J Am Chem Soc 63:3529-3530. doi: 10.1021/ja01857a508
36. Van der Eycken E, Terryn N, Goeman JL (2000) Sudan-β-d-glucuronides and their use for the histochemical localization of β-glucuronidase activity in transgenic plants. Plant Cell Rep 19:966-970. doi: 10.1007/s002990000219
37. Oliva A, Passaro I, Di Pasquale R, Di Feo A, Criscuolo M, et al. (2005) Ex vivo expansion of bone marrow stromal cells by platelet-rich plasma: a promising strategy in maxillo-facial surgery. Int J Immunopathol Pharmacol 18(3 Suppl):47-53. PMID: 16848987
38. Borriello A, Caldarelli I, Basile MA, Bencivenga D, Tramontano A, et al. (2011) The tyrosine kinase inhibitor dasatinib induces a marked adipogenic differentiation of human multipotent mesenchymal stromal cells. PLoS One 6(12): e28555. doi: 10.1371/journal.pone.0028555 PMID: 22164306
39. Guida L, Annunziata M, Rocci A, Contaldo M, Rullo R, et al. (2010) Biological response of human bone marrow mesenchymal stem cells to fluoride-modified titanium surfaces. Clin Oral Implants Res 21(11): 1234-1241. doi: 10.1111/j.1600-0501.2010.01929.x PMID: 20497444
40. Granéli C, Thorfve A, Ruetschi U, Brisby H, Thomsen P, et al. (2014) Novel markers of osteogenic and adipogenic differentiation of human bone marrow stromal cells identified using a quantitative proteomics approach. Stem Cell Res 12(1): 153-165. doi: 10.1016/j.scr.2013.09.009 PMID: 24239963
41. Cook DA, Fellgett SW, Pownall ME, O'Shea PJ, Genever PG, et al. (2013) Wnt-dependent osteogenic commitment of bone marrow stromal cells using a novel GSK3innodatabeta inhibitor. Stem Cell Res 12(2): 415-427. doi: 10.1016/j.scr.2013.10.002 PMID: 24382458
42. Perna AF, Ingrosso D, Satta E, Lombardi C, Galletti P, et al. (2004) Plasma Protein Aspartyl Damage Is Increased in hemodialysis Patients: Studies on Causes and Consequences. J Am Soc Nephrol 15: 2747-2754. doi: 10.1097/01.ASN.0000141041.71717.11 PMID: 15466280
43. Duranton F, Cohen G, De Smet R, Rodriguez M, Jankowski J, et al. (2012) Normal and pathologic concentrations of uremic toxins. J Am Soc Nephrol 23(7): 1258-1270. doi: 10.1681/ASN.2011121175 PMID: 22626821
44. Meert N, Schepers E, Glorieux G, Van Landschoot M, Goeman JL, et al. (2012) Novel method for simultaneous determination of p-cresylsulphate and p-cresylglucuronide: clinical data and pathophysiological implications. Nephrol Dial Transplant 27(6):2388-2396. doi: 10.1093/ndt/gfr672 PMID: 22167586
45. Huang YT, Yao CH, Way CL, Lee KV, Tsai CY, et al. (2013) Diallyl trisulfide and diallyl disulfide ameliorate cardiac dysfunction by suppressing apoptotic and enhancing survival pathways in experimental diabetic rats. J Appl Physiol 114(3): 402-410. doi: 10.1152/japplphysiol.00672.2012 PMID: 23139364
46. Kolluru GK, Shen X, Bir SC, Kevil CG (2013) Hydrogen sulfide chemical biology: pathophysiological roles and detection. Nitric Oxide 35: 5-20. doi: 10.1016/j.niox.2013.07.002 PMID: 23850632
47. Bordia A, Verma SK, Srivastava KC (1998) Effect of garlic (Allium sativum) on blood lipids, blood sugar, fibrinogen and fibrinolytic activity in patients with coronary artery disease. Prostaglandins Leukot Essent Fatty Acids 58(4): 257-263. doi: 10.1016/S0952-3278(98)90034-5 PMID: 9654398
48. Vanholder R, De Smet R, Glorieux G, Argilés A, Baurmeister U, et al. (2003) Review on uremic toxins: classification, concentration, and inter- individual variability. Kidney Int 63:1934-1943. doi: 10.1046/j. 1523-1755.2003.00924.x PMID: 12675874
49. Jankowski J, van der Giet M, Jankowski V, Schmidt S, Hemeier M, et al. (2003) Increased plasma phenylacetic acid in patients with end-stage renal failure inhibits iNOS expression. J Clin Invest 112 (2):256-64. doi: 10.1172/JCI15524 PMID: 12865413
50. Lall N, Henley-Smith CJ, De Canha MN, Oosthuizen CB, Berrington D (2013) Viability Reagent, Presto- Blue, in Comparison with Other Available Reagents, Utilized in Cytotoxicity and Antimicrobial Assays. Int J Microbiol 2013:420601. doi: 10.1155/2013/420601 PMID: 23653650
51. Boncler M, Róalski M, Krajewska U, Podsêdek A, Watala C (2014) Comparison of PrestoBlue and MTT assays of cellular viability in the assessment of anti-proliferative effects of plant extracts on human endothelial cells. J Pharmacol Toxicol Methods 69(1): 9-16. doi: 10.1016/j.vascn.2013.09.003 PMID: 24103906
52. Dawson-Saunders B, Trapp RG (1990) Basic and Clinical Biostatistics. Norwalk: Appleton & Lange. 199 p.
53. Lesaffer G, De Smet R, Lameire N, Dhondt A, Duym P, et al. (2000) Intradialytic removal of proteinbound uraemic toxins: role of solute characteristics and of dialyser membrane. Nephrol Dial Transplant 15(1):50-57. doi: 10.1093/ndt/15.1.50 PMID: 10607767
54. Kramann R, Counson 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(9): e45-54. doi: 10.1161/ATVBAHA.111.228601 PMID: 21680902
55. Chen NX, Duan D, O'Neill KD, Wolisi GO, Koczman JJ, et al. (2006) The mechanisms of uremic seruminduced expression of bone matrix proteins in bovine vascular smooth muscle cells. Kidney Int 70(6): 1046-53. doi: 10.1038/sj.ki.5001663 PMID: 16837922
56. Kawata T, Nagano N, Obi M, Miyata S, Koyama C, et al. (2008) Cinacalcet suppresses calcification of the aorta and heart in uremic rats. Kidney Int 74(10): 1270-1277. doi: 10.1038/ki.2008.407 PMID: 18813289
57. Block A, Martin KJ, de Francisco AL, Turner SA, Avram MM, et al. (2004) Cinacalcet for secondary hyperparathyroidism in patients receiving hemodialysis. N Engl J Med 350(15):1516-1525. doi: 10.1056/ NEJMoa031633 PMID: 15071126
58. Urena P, Jacobson SH, Zitt E, Vervloet M, Malberti F, et al. (2009) Cinacalcet and achievement of the NKF/K-DOQI recommended target values for bone and mineral metabolism in renal-world clinical practice- the ECHO observational study. Nephrol Dial Transplant 24(9):2852-2859. doi: 10.1093/ndt/ gfp144 PMID: 19369690
59. Li D, Shao L, Zhou H, Jiang W, Zhang W, et al. (2013) The efficacy of cinacalcet combined with conventional therapy on bone and mineral metabolism in hemodialysis patients with secondary hyperparathyroidism: a meta-analysis. Endocrine 43(1):68-77. doi: 10.1007/s12020-012-9711-2 PMID: 22669774
60. Perna AF, Sepe I, Lanza D, Capasso R, Zappavigna S, et al. (2013) Hydrogen sulfide reduces cell adhesion and relevant inflammatory triggering by preventing ADAM17-dependent TNF-α activation. J Cell Biochem 114(7): 1536-1548. doi: 10.1002/jcb.24495 PMID: 23297114
61. Liu Y, Yang R, Liu X, Zhou Y, Qu C, et al. (2014) Hydrogen sulfide maintains mesenchymal stem cell function and bone homeostasis via regulation of Ca(2+) channel sulfhydration. Cell Stem Cell 15(1):66-78. doi: 10.1016/j.stem.2014.03.005 PMID: 24726192