Macrophages inhibit migration, metabolic activity and osteogenic differentiation of human mesenchymal stem cells in vitro

Cells Tissues Organs

Volumn 195, Issue 6, 2012, Pages 473-483

  Chen, Chao ^a   Uludaǧ, Hasan ^a   Wang, Zhixiang ^a   Rezansoff, Alex ^a   Jiang, Hongxing ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Macrophages; Mesenchymal stem cells; Migration; Osteogenic differentiation

Indexed keywords

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; BONE SIALOPROTEIN; CALCIUM; INTERLEUKIN 1BETA; OSTEOCALCIN; TRANSCRIPTION FACTOR RUNX2; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BONE DEVELOPMENT; CELL METABOLISM; CELL MIGRATION; CONTROLLED STUDY; CULTURE MEDIUM; DOWN REGULATION; ENZYME ACTIVITY; FRACTURE HEALING; GENETIC MARKER; HUMAN; HUMAN CELL; IN VITRO STUDY; MACROPHAGE; MESENCHYMAL STEM CELL; MONOCYTE; OSTEOBLAST; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ALKALINE PHOSPHATASE; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL MEMBRANE; CELL MOVEMENT; CELL PROLIFERATION; CELL SHAPE; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; CYTOKINES; GENE EXPRESSION REGULATION; GENTIAN VIOLET; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MACROPHAGES; MESENCHYMAL STROMAL CELLS; MONOCYTES; OSTEOGENESIS; STAINING AND LABELING; TETRADECANOYLPHORBOL ACETATE;

EID: 84861231269     PISSN: 14226405     EISSN: 14226421     Source Type: Journal    
DOI: 10.1159/000330686     Document Type: Article

References (45)

1. Andrew, J.G., S.M. Andrew, A.J. Freemont, D.R. Marsh (1994) Inflammatory cells in normal human fracture healing. Acta Orthop Scand 65: 462-466. (Pubitemid 24331059)
2. Bertolini, D.R., G.E. Nedwin, T.S. Bringman, D.D. Smith, G.R. Mundy (1986) Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature 319: 516-518. (Pubitemid 16212936)
3. Chen, G., D.V. Goeddel (2002) TNF-R1 signaling: a beautiful pathway. Science 296: 1634-1635 (Pubitemid 34579145)
4. Cheng, P., Z.Q. Gao, Y.H. Liu, Y.X. Xue (2009) Platelet-derived growth factor BB promotes the migration of bone marrow-derived mesenchymal stem cells towards C6 glioma and up-regulates the expression of intracellular adhesion molecule-1. Neurosci Lett 451: 52-56.
5. Cho, H.H., K.K. Shin, Y.J. Kim, J.S. Song, J.M. Kim, Y.C. Bae, C.D. Kim, J.S. Jung (2010) NFkappaB activation stimulates osteogenic differentiation of mesenchymal stem cells derived from human adipose tissue by increasing TAZ expression. J Cell Physiol 223: 168-177.
6. Crowther, M., N.J. Brown, E.T. Bishop, C.E. Lewis (2001) Microenvironmental influence on macrophage regulation of angiogenesis in wounds and malignant tumors. J Leukoc Biol 70: 478-490. (Pubitemid 32954759)
7. Daigneault, M., J.A. Preston, H.M. Marriott, M.K. Whyte, D.H. Dockrell (2010) The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLoS One 5: e8668
8. DiPietro, L.A. (1995) Wound healing: the role of the macrophage and other immune cells. Shock 4: 233-240
9. Dominici, M., K. Le Blanc, I. Mueller, I. Slaper-Cortenbach, F. Marini, D. Krause, R. Deans, A. Keating, D. Prockop, E. Horwitz (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8: 315-317.
10. Gerstenfeld, L.C., T.J. Cho, T. Kon, T. Aizawa, J. Cruceta, B.D. Graves, T.A. Einhorn (2001) Impaired intramembranous bone formation during bone repair in the absence of tumor necrosis factor-alpha signaling. Cells Tissues Organs 169: 285-294. (Pubitemid 32656656)
11. Gilbert, L., X. He, P. Farmer, J. Rubin, H. Drissi, A.J. van Wijnen, J.B. Lian, G.S. Stein, M.S. Nanes (2002) Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/ AML3/Pebp2alpha A) is inhibited by tumor necrosis factor-alpha. J Biol Chem 277: 2695-2701. (Pubitemid 34953297)
12. Giuliani, N., S. Colla, F. Morandi, M. Lazzaretti, R. Sala, S. Bonomini, M. Grano, S. Colucci, M. Svaldi, V. Rizzoli (2005) Myeloma cells block RUNX2/CBFA1 activity in human bone marrow osteoblast progenitors and inhibit osteoblast formation and differentiation. Blood 106: 2472-2483. (Pubitemid 41510822)
13. Gordon, S., P.R. Taylor (2005) Monocyte and macrophage heterogeneity. Nat Rev Immunol 5: 953-964. (Pubitemid 41746764)
14. Grundnes, O., O. Reikeraas (2000) Effects of macrophage activation on bone healing. J Orthop Sci 5: 243-247. (Pubitemid 30431800)
15. Hemeda, H., M. Jakob, A.K. Ludwig, B. Giebel, S. Lang, S. Brandau (2010) Interferon-gamma and tumor necrosis factor-alpha differentially affect cytokine expression and migration properties of mesenchymal stem cells. Stem Cells Dev 19: 693-706.
16. Hess, K., A. Ushmorov, J. Fiedler, R.E. Brenner, T. Wirth (2009) TNFalpha promotes osteogenic differentiation of human mesenchymal stem cells by triggering the NF-kappaB signaling pathway. Bone 45: 367-376.
17. Ishiyama, M., Y. Miyazono, K. Sasamoto, Y. Ohkura, K. Ueno (1997) A highly water-soluble disulfonated tetrazolium salt as a chromogenic indicator for NADH as well as cell viability. Talanta 44: 1299-1305. (Pubitemid 27249311)
18. Jian, H., X. Shen, I. Liu, M. Semenov, X. He, X. Wang (2006) Smad3-dependent nuclear translocation of beta-catenin is required for TGF-beta1-induced proliferation of bone marrow-derived adult human mesenchymal stem cells. Genes Dev 20: 666-674.
19. Jones, E.A., S.E. Kinsey, A. English, R.A. Jones, L. Straszynski, D.M. Meredith, A.F. Markham, A. Jack, P. Emery, D. McGonagle (2002) Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum 46: 3349-3360. (Pubitemid 35453547)
20. Kaler, P., L. Augenlicht, L. Klampfer (2009) Macrophage-derived IL-1beta stimulates Wnt signaling and growth of colon cancer cells: a crosstalk interrupted by vitamin D3. Oncogene 28: 3892-3902.
21. Khosla, S., J.J. Westendorf, M.J. Oursler (2008) Building bone to reverse osteoporosis and repair fractures. J Clin Invest 118: 421-428 (Pubitemid 351206529)
22. Kortesidis, A., A. Zannettino, S. Isenmann, S. Shi, T. Lapidot, S. Gronthos (2005) Stromalderived factor-1 promotes the growth, survival, and development of human bone marrow stromal stem cells. Blood 105: 3793-3801. (Pubitemid 40656121)
23. Lacey, D.C., P.J. Simmons, S.E. Graves, J.A. Hamilton (2009) Proinflammatory cytokines inhibit osteogenic differentiation from stem cells: implications for bone repair during inflammation. Osteoarthritis Cartilage 17: 735-742.
24. Lai, J.J., K.P. Lai, K.H. Chuang, P. Chang, I.C. Yu, W.J. Lin, C. Chang (2009) Monocyte/macrophage androgen receptor suppresses cutaneous wound healing in mice by enhancing local TNF-alpha expression. J Clin Invest 119: 3739-3751.
25. Lange, J., A. Sapozhnikova, C. Lu, D. Hu, X. Li, T. Miclau 3rd, R.S. Marcucio (2010) Action of IL-1beta during fracture healing. J Orthop Res 28: 778-784.
26. Liang, F., V. Seyrantepe, K. Landry, R. Ahmad, A. Ahmad, N.M. Stamatos, A.V. Pshezhetsky (2006) Monocyte differentiation upregulates the expression of the lysosomal sialidase, Neu1, and triggers its targeting to the plasma membrane via major histocompatibility complex class II-positive compartments. J Biol Chem 281: 27526-27538. (Pubitemid 44401779)
27. Longobardi, L., L. O'Rear, S. Aakula, B. Johnstone, K. Shimer, A. Chytil, W.A. Horton, H.L. Moses, A. Spagnoli (2006) Effect of IGF-1 in the chondrogenesis of bone marrow mesenchymal stem cells in the presence or absence of TGF-beta signaling. J Bone Miner Res 21: 626-636.
28. Lucas, T., A. Waisman, R. Ranjan, J. Roes, T. Krieg, W. Muller, A. Roers, S.A. Eming (2010) Differential roles of macrophages in diverse phases of skin repair. J Immunol 184: 3964-3977.
29. Maes, C., L. Coenegrachts, I. Stockmans, E. Daci, A. Luttun, A. Petryk, R. Gopalakrishnan, K. Moermans, N. Smets, C.M. Verfaillie, P. Carmeliet, R. Bouillon, G. Carmeliet (2006) Placental growth factor mediates mesenchymal cell development, cartilage turnover, and bone remodeling during fracture repair. J Clin Invest 116: 1230-1242
30. Mosser, D.M., J.P. Edwards (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8: 958-969
31. Ng, F., S. Boucher, S. Koh, K.S. Sastry, L. Chase, U. Lakshmipathy, C. Choong, Z. Yang, M.C. Vemuri, M.S. Rao, V. Tanavde (2008) PDGF, TGF-beta, and FGF signaling is important for differentiation and growth of mesenchymal stem cells (MSCs): transcriptional profiling can identify markers and signaling pathways important in differentiation of MSCs into adipogenic, chondrogenic, and osteogenic lineages. Blood 112: 295-307.
32. Pasha, Z., Y. Wang, R. Sheikh, D. Zhang, T. Zhao, M. Ashraf (2008) Preconditioning enhances cell survival and differentiation of stem cells during transplantation in infarcted myocardium. Cardiovasc Res 77: 134-142. (Pubitemid 351195153)
33. Pollard, J.W. (2009) Trophic macrophages in development and disease. Nat Rev Immunol 9: 259-270.
34. Ponte, A.L., E. Marais, N. Gallay, A. Langonne, B. Delorme, O. Herault, P. Charbord, J. Domenech (2007) The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells 25: 1737-1745. (Pubitemid 47121852)
35. Santavirta, S., Y.T. Konttinen, D. Nordstrom, A. Makela, T. Sorsa, M. Hukkanen, P. Rokkanen (1992) Immunologic studies of nonunited fractures. Acta Orthop Scand 63: 579-586 (Pubitemid 23012661)
36. Song, H., K. Kwon, S. Lim, S.M. Kang, Y.G. Ko, Z. Xu, J.H. Chung, B.S. Kim, H. Lee, B. Joung, S. Park, D. Choi, Y. Jang, N.S. Chung, K.J. Yoo, K.C. Hwang (2005) Transfection of mesenchymal stem cells with the FGF-2 gene improves their survival under hypoxic conditions. Mol Cells 19: 402-407.
37. Steinert, A.F., B. Proffen, M. Kunz, C. Hendrich, S.C. Ghivizzani, U. Noth, A. Rethwilm, J. Eulert, C.H. Evans (2009) Hypertrophy is induced during the in vitro chondrogenic differentiation of human mesenchymal stem cells by bone morphogenetic protein-2 and bone morphogenetic protein-4 gene transfer. Arthritis Res Ther 11: R148.
38. Tang, Y., X. Wu, W. Lei, L. Pang, C. Wan, Z. Shi, L. Zhao, T.R. Nagy, X. Peng, J. Hu, X. Feng, W. Van Hul, M. Wan, X. Cao (2009) TGFbeta1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nat Med 15: 757-765.
39. Tsuchiya, S., Y. Kobayashi, Y. Goto, H. Okumura, S. Nakae, T. Konno, K. Tada (1982) Induction of maturation in cultured human monocytic leukemia cells by a phorbol diester. Cancer Res 42: 1530-1536. (Pubitemid 12148801)
40. van Amerongen, M.J., M.C. Harmsen, N. van Rooijen, A.H. Petersen, M.J. van Luyn (2007) Macrophage depletion impairs wound healing and increases left ventricular remodeling after myocardial injury in mice. Am J Pathol 170: 818-829. (Pubitemid 47339352)
41. Wang, L., F. Du, X. Wang (2008) TNF-alpha induces two distinct caspase-8 activation pathways. Cell 133: 693-703. (Pubitemid 351636305)
42. Wang, Q., H. Zhang, B. Zhao, H. Fei (2009) IL-1beta caused pancreatic beta-cells apoptosis is mediated in part by endoplasmic reticulum stress via the induction of endoplasmic reticulum Ca2+ release through the c-Jun Nterminal kinase pathway. Mol Cell Biochem 324: 183-190.
43. Weitzmann, M.N., C. Roggia, G. Toraldo, L. Weitzmann, R. Pacifici (2002) Increased production of IL-7 uncouples bone formation from bone resorption during estrogen deficiency. J Clin Invest 110: 1643-1650. (Pubitemid 35424242)
44. Zhou, F.H., B.K. Foster, X.F. Zhou, A.J. Cowin, C.J. Xian (2006) TNF-alpha mediates p38 MAP kinase activation and negatively regulates bone formation at the injured growth plate in rats. J Bone Miner Res 21: 1075-1088. (Pubitemid 43962836)
45. Zuk, P.A., M. Zhu, P. Ashjian, D.A. De Ugarte, J.I. Huang, H. Mizuno, Z.C. Alfonso, J.K. Fraser, P. Benhaim, M.H. Hedrick (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13: 4279-4295. (Pubitemid 35471185)