Metabolic labeling of human bone marrow mesenchymal stem cells for the quantitative analysis of their chondrogenic differentiation

Journal of Proteome Research

Volumn 11, Issue 11, 2012, Pages 5350-5361

  Rocha, Beatriz ^a   Calamia, Valentina ^a   Mateos, Jesús ^a   Fernández Puente, Patricia ^a   Blanco, Francisco J ^a,b   Ruiz Romero, Cristina ^a,b  

^a UNIVERSITY OF A CORUÑA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

bone marrow; cartilage; chondrocytes; chondrogenesis; mesenchymal stem cells; proteomics; SILAC

Indexed keywords

AMINO ACID; CYCLOPHILIN A; FIBRONECTIN; GELSOLIN; STABLE ISOTOPE; SUPEROXIDE DISMUTASE; VIMENTIN;

ADULT; AGED; ARTICLE; BONE MARROW; CARTILAGE CELL; CELL CULTURE; CELL DIFFERENTIATION; CHONDROGENESIS; CLINICAL ARTICLE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MESENCHYMAL STEM CELL; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; QUANTITATIVE ANALYSIS;

BASE SEQUENCE; BIOLOGICAL MARKERS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROCYTES; CHROMATOGRAPHY, LIQUID; DATABASES, PROTEIN; DNA PRIMERS; HUMANS; MESENCHYMAL STROMAL CELLS; PROTEOMICS; REAL-TIME POLYMERASE CHAIN REACTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84868322944     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300572r     Document Type: Article

References (50)

1. Hombach-Klonisch, S.; Panigrahi, S.; Rashedi, I.; Seifert, A.; Alberti, E.; Pocar, P.; Kurpisz, M.; Schulze-Osthoff, K.; Mackiewicz, A.; Los, M. Adult stem cells and their trans-differentiation potential - perspectives and therapeutic applications J. Mol. Med. 2008, 86 (12) 1301-14
2. Pittenger, M. F. Mesenchymal stem cells from adult bone marrow Methods Mol. Biol. 2008, 449, 27-44
3. Goldring, M. B.; Tsuchimochi, K.; Ijiri, K. The control of chondrogenesis J. Cell Biochem. 2006, 97 (1) 33-44
4. Johnstone, B.; Hering, T. M.; Caplan, A. I.; Goldberg, V. M.; Yoo, J. U. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells Exp. Cell Res. 1998, 238 (1) 265-72
5. DeLise, A. M.; Stringa, E.; Woodward, W. A.; Mello, M. A.; Tuan, R. S. Embryonic limb mesenchyme micromass culture as an in vitro model for chondrogenesis and cartilage maturation Methods Mol. Biol. 2000, 137, 359-75
6. Derfoul, A.; Perkins, G. L.; Hall, D. J.; Tuan, R. S. Glucocorticoids promote chondrogenic differentiation of adult human mesenchymal stem cells by enhancing expression of cartilage extracellular matrix genes Stem Cells 2006, 24 (6) 1487-95
7. Spagnoli, A.; O'Rear, L.; Chandler, R. L.; Granero-Molto, F.; Mortlock, D. P.; Gorska, A. E.; Weis, J. A.; Longobardi, L.; Chytil, A.; Shimer, K.; Moses, H. L. TGF-beta signaling is essential for joint morphogenesis J. Cell Biol. 2007, 177 (6) 1105-17
8. Tuli, R.; Tuli, S.; Nandi, S.; Huang, X.; Manner, P. A.; Hozack, W. J.; Danielson, K. G.; Hall, D. J.; Tuan, R. S. Transforming growth factor-beta-mediated chondrogenesis of human mesenchymal progenitor cells involves N-cadherin and mitogen-activated protein kinase and Wnt signaling cross-talk J. Biol. Chem. 2003, 278 (42) 41227-36
9. Park, H. W.; Shin, J. S.; Kim, C. W. Proteome of mesenchymal stem cells Proteomics 2007, 7 (16) 2881-94
10. Maurer, M. H. Proteomic definitions of mesenchymal stem cells Stem Cells Int. 2011, 2011, 704256
11. Cicione, C.; Diaz-Prado, S.; Muinos-Lopez, E.; Hermida-Gomez, T.; Blanco, F. J. Molecular profile and cellular characterization of human bone marrow mesenchymal stem cells: donor influence on chondrogenesis Differentiation 2010, 80 (2-3) 155-65
12. Hermida-Gomez, T.; Fuentes-Boquete, I.; Gimeno-Longas, M. J.; Muinos-Lopez, E.; Diaz-Prado, S.; de Toro, F. J.; Blanco, F. J. Bone marrow cells immunomagnetically selected for CD271+ antigen promote in vitro the repair of articular cartilage defects Tissue Eng. Part A 2011, 17 (7-8) 1169-79
13. Ong, S. E.; Mann, M. Stable isotope labeling by amino acids in cell culture for quantitative proteomics Methods Mol. Biol. 2007, 359, 37-52
14. Calamia, V.; Rocha, B.; Mateos, J.; Fernandez-Puente, P.; Ruiz-Romero, C.; Blanco, F. J. Metabolic labeling of chondrocytes for the quantitative analysis of the interleukin-1-beta-mediated modulation of their intracellular and extracellular proteomes J. Proteome Res. 2011, 10 (8) 3701-11
15. Calamia, V.; Fernandez-Puente, P.; Mateos, J. U.; Lourido, L.; Rocha, B.; Montell, E.; Verges, J.; Ruiz-Romero, C.; Blanco, F. J. Pharmacoproteomic study of three different chondroitin sulfate compounds on intracellular and extracellular human chondrocyte proteomes Mol. Cell. Proteomics 2012, 11 (6) M111.013417
16. Gimeno, M.; Maneiro, E.; Rendal, E.; Ramallal, M.; Sanjurjo, L.; Blanco, F. Cell therapy: a therapeutic alternative to treat focal cartilage lesions Transplant. Proc. 2005, 37 (9) 4080-3
17. Akiyama, H. Control of chondrogenesis by the transcription factor Sox9 Mod. Rheumatol. 2008, 18 (3) 213-9
18. Steinert, A. F.; Ghivizzani, S. C.; Rethwilm, A.; Tuan, R. S.; Evans, C. H.; Noth, U. Major biological obstacles for persistent cell-based regeneration of articular cartilage Arthritis Res. Ther. 2007, 9 (3) 213
19. Hardingham, T.; Tew, S.; Murdoch, A. Tissue engineering: chondrocytes and cartilage Arthritis Res. 2002, 4 (Suppl 3) S63-8
20. Jorgensen, C.; Noel, D. Mesenchymal stem cells in osteoarticular diseases Regen. Med. 2011, 6 (6 Suppl) 44-51
21. Li, G.; Chan, C. Y.; Wang, H.; Kung, H. F. Proteomic analysis of human mesenchymal stem cells Methods Mol. Biol. 2011, 698, 443-57
22. Sun, H. J.; Bahk, Y. Y.; Choi, Y. R.; Shim, J. H.; Han, S. H.; Lee, J. W. A proteomic analysis during serial subculture and osteogenic differentiation of human mesenchymal stem cell J. Orthop. Res. 2006, 24 (11) 2059-71
23. Choi, Y. A.; Lim, J.; Kim, K. M.; Acharya, B.; Cho, J. Y.; Bae, Y. C.; Shin, H. I.; Kim, S. Y.; Park, E. K. Secretome analysis of human BMSCs and identification of SMOC1 as an important ECM protein in osteoblast differentiation J. Proteome Res. 2010, 9 (6) 2946-56
24. Kim, S.; Min, W. K.; Chun, S.; Lee, W.; Chung, H. J.; Choi, S. J.; Yang, S. E.; Yang, Y. S.; Yoo, J. I. Protein expression profiles during osteogenic differentiation of mesenchymal stem cells derived from human umbilical cord blood Tohoku J. Exp. Med. 2010, 221 (2) 141-50
25. Lee, H. K.; Lee, B. H.; Park, S. A.; Kim, C. W. The proteomic analysis of an adipocyte differentiated from human mesenchymal stem cells using two-dimensional gel electrophoresis Proteomics 2006, 6 (4) 1223-9
26. Jeong, J. A.; Ko, K. M.; Park, H. S.; Lee, J.; Jang, C.; Jeon, C. J.; Koh, G. Y.; Kim, H. Membrane proteomic analysis of human mesenchymal stromal cells during adipogenesis Proteomics 2007, 7 (22) 4181-91
27. Ji, Y. H.; Ji, J. L.; Sun, F. Y.; Zeng, Y. Y.; He, X. H.; Zhao, J. X.; Yu, Y.; Yu, S. H.; Wu, W. Quantitative proteomics analysis of chondrogenic differentiation of C3H10T1/2 mesenchymal stem cells by iTRAQ labeling coupled with on-line two-dimensional LC/MS/MS Mol. Cell. Proteomics 2010, 9 (3) 550-64
28. De la Fuente, A.; Mateos, J.; Lesende-Rodriguez, I.; Calamia, V.; Fuentes-Boquete, I.; de Toro, F. J.; Arufe, M. C.; Blanco, F. J. Proteome analysis during chondrocyte differentiation in a new chondrogenesis model using human umbilical cord stroma mesenchymal stem cells Mol. Cell. Proteomics 2012, 11 (2) M111 010496
29. Ong, S. E.; Foster, L. J.; Mann, M. Mass spectrometric-based approaches in quantitative proteomics Methods 2003, 29 (2) 124-30
30. Schilling, O.; Overall, C. M. Proteomic discovery of protease substrates Curr. Opin. Chem. Biol. 2007, 11 (1) 36-45
31. Polacek, M.; Bruun, J. A.; Elvenes, J.; Figenschau, Y.; Martinez, I. The secretory profiles of cultured human articular chondrocytes and mesenchymal stem cells: implications for autologous cell transplantation strategies Cell Transplant. 2011, 20 (9) 1381-93
32. Ruiz-Romero, C.; Lopez-Armada, M. J.; Blanco, F. J. Proteomic characterization of human normal articular chondrocytes: a novel tool for the study of osteoarthritis and other rheumatic diseases Proteomics 2005, 5 (12) 3048-59
33. Xu, J.; Wang, W.; Ludeman, M.; Cheng, K.; Hayami, T.; Lotz, J. C.; Kapila, S. Chondrogenic differentiation of human mesenchymal stem cells in three-dimensional alginate gels Tissue Eng. Part A 2008, 14 (5) 667-80
34. Kadler, K. E.; Hill, A.; Canty-Laird, E. G. Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators Curr. Opin. Cell. Biol. 2008, 20 (5) 495-501
35. Kutsuna, T.; Inoue, H.; Takeda, H.; Takahashi, T.; Yamamoto, H.; Miura, H.; Higashiyama, S. Fibronectin regulates proteoglycan production balance in transforming growth factor-beta1-induced chondrogenesis Int. J. Mol. Med. 2011, 28 (5) 829-34
36. Connelly, J. T.; Petrie, T. A.; Garcia, A. J.; Levenston, M. E. Fibronectin- and collagen-mimetic ligands regulate bone marrow stromal cell chondrogenesis in three-dimensional hydrogels Eur. Cell Mater. 2011, 22, 168-76
37. 176-7.
38. Woods, A.; Wang, G.; Beier, F. Regulation of chondrocyte differentiation by the actin cytoskeleton and adhesive interactions J. Cell Physiol. 2007, 213 (1) 1-8
39. Djouad, F.; Delorme, B.; Maurice, M.; Bony, C.; Apparailly, F.; Louis-Plence, P.; Canovas, F.; Charbord, P.; Noel, D.; Jorgensen, C. Microenvironmental changes during differentiation of mesenchymal stem cells towards chondrocytes Arthritis Res. Ther. 2007, 9 (2) R33
40. Bobick, B. E.; Tuan, R. S.; Chen, F. H. The intermediate filament vimentin regulates chondrogenesis of adult human bone marrow-derived multipotent progenitor cells J. Cell Biochem. 2010, 109 (1) 265-76
41. Mobasheri, A.; Vannucci, S. J.; Bondy, C. A.; Carter, S. D.; Innes, J. F.; Arteaga, M. F.; Trujillo, E.; Ferraz, I.; Shakibaei, M.; Martin-Vasallo, P. Glucose transport and metabolism in chondrocytes: a key to understanding chondrogenesis, skeletal development and cartilage degradation in osteoarthritis Histol. Histopathol. 2002, 17 (4) 1239-67
42. Pattappa, G.; Heywood, H. K.; de Bruijn, J. D.; Lee, D. A. The metabolism of human mesenchymal stem cells during proliferation and differentiation J. Cell Physiol. 2011, 226 (10) 2562-70
43. Ruiz-Romero, C.; Calamia, V.; Mateos, J.; Carreira, V.; Martinez-Gomariz, M.; Fernandez, M.; Blanco, F. J. Mitochondrial dysregulation of osteoarthritic human articular chondrocytes analyzed by proteomics: a decrease in mitochondrial superoxide dismutase points to a redox imbalance Mol. Cell. Proteomics 2009, 8 (1) 172-89
44. Schedel, J.; Lowin, T.; Kujat, R.; Judex, M.; Scholmerich, J.; Nerlich, M.; Muller-Ladner, U.; Angele, P. RAP-PCR fingerprinting reveals time-dependent expression of matrix-related molecules following stem-cell based TGFbeta1-induced chondrocyte development Int. J. Mol. Med. 2011, 27 (4) 519-23
45. Wang, P.; Heitman, J. The cyclophilins Genome Biol. 2005, 6 (7) 226
46. Satoh, K.; Nigro, P.; Matoba, T.; O'Dell, M. R.; Cui, Z.; Shi, X.; Mohan, A.; Yan, C.; Abe, J.; Illig, K. A.; Berk, B. C. Cyclophilin A enhances vascular oxidative stress and the development of angiotensin II-induced aortic aneurysms Nat. Med. 2009, 15 (6) 649-56
47. Catterall, J. B.; Rowan, A. D.; Sarsfield, S.; Saklatvala, J.; Wait, R.; Cawston, T. E. Development of a novel 2D proteomics approach for the identification of proteins secreted by primary chondrocytes after stimulation by IL-1 and oncostatin M Rheumatology (Oxford) 2006, 45 (9) 1101-9
48. Ruiz-Romero, C.; Carreira, V.; Rego, I.; Remeseiro, S.; Lopez-Armada, M. J.; Blanco, F. J. Proteomic analysis of human osteoarthritic chondrocytes reveals protein changes in stress and glycolysis Proteomics 2008, 8 (3) 495-507
49. Morita, K.; Miyamoto, T.; Fujita, N.; Kubota, Y.; Ito, K.; Takubo, K.; Miyamoto, K.; Ninomiya, K.; Suzuki, T.; Iwasaki, R.; Yagi, M.; Takaishi, H.; Toyama, Y.; Suda, T. Reactive oxygen species induce chondrocyte hypertrophy in endochondral ossification J. Exp. Med. 2007, 204 (7) 1613-23
50. Kim, K. S.; Choi, H. W.; Yoon, H. E.; Kim, I. Y. Reactive oxygen species generated by NADPH oxidase 2 and 4 are required for chondrogenic differentiation J. Biol. Chem. 2010, 285 (51) 40294-302