Inflammatory cytokines induce a unique mineralizing phenotype in mesenchymal stem cells derived from human bone marrow

Journal of Biological Chemistry

Volumn 288, Issue 41, 2013, Pages 29494-29505

  Ferreira, Elisabeth ^a,b   Porter, Ryan M ^a,b   Wehling, Nathalie ^c   O'Sullivan, Regina P ^a   Liu, Fangjun ^a   Boskey, Adele ^d   Estok, Daniel M ^e   Harris, Mitchell B ^e   Vrahas, Mark S ^b,f   Evans, Christopher H ^a,b   Wells, James W ^a,b  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b AO FOUNDATION   (Switzerland)

^c Asklepios Stadtklinik ^*  (Germany)

^d HOSPITAL FOR SPECIAL SURGERY   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE ACTIVITY; HYDROXYAPATITE FORMATIONS; INFLAMMATORY CONDITIONS; INFLAMMATORY CYTOKINES; INFLAMMATORY MEDIATORS; MESENCHYMAL STEM CELL; PYROPHOSPHATASE ACTIVITIES; VASCULAR SMOOTH MUSCLE CELLS;

BONE; COLLAGEN; FLOWCHARTING; FOURIER TRANSFORM INFRARED SPECTROSCOPY; HYDROXYAPATITE; MINERALOGY; MUSCULOSKELETAL SYSTEM; OSTEOBLASTS; PHOSPHATASES; REPAIR; TISSUE; TISSUE ENGINEERING; TRANSMISSION ELECTRON MICROSCOPY;

CELL CULTURE;

ALKALINE PHOSPHATASE; BONE SIALOPROTEIN; DEXAMETHASONE; ECTONUCLEOTIDE PYROPHOSPHATASE; HYDROXYAPATITE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; NUCLEOTIDE PYROPHOSPHATASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; UNCLASSIFIED DRUG;

ADIPOCYTE; ADULT; AGED; ARTICLE; BIOMINERALIZATION; CARTILAGE CELL; CELL LINEAGE; CELL TYPE; CELL VACUOLE; CONTROLLED STUDY; CYTOKINE RESPONSE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EXTRACELLULAR MATRIX; FEMALE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; LIGAMENT; MALE; MESENCHYMAL STEM CELL; MYOBLAST; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; TENDON; VASCULAR SMOOTH MUSCLE;

BIOMINERALIZATION; BONE; CELL DIFFERENTIATION; INFLAMMATION; INTERLEUKIN; TISSUE ENGINEERING;

ADULT; AGED; AGED, 80 AND OVER; ALKALINE PHOSPHATASE; BLOTTING, WESTERN; BONE MARROW CELLS; CALCIUM; CELLS, CULTURED; CYTOKINES; DIPHOSPHATES; DURAPATITE; FEMALE; GENE EXPRESSION; HUMANS; INTEGRIN-BINDING SIALOPROTEIN; MALE; MESENCHYMAL STROMAL CELLS; MICROSCOPY, ELECTRON, TRANSMISSION; MIDDLE AGED; MITOGEN-ACTIVATED PROTEIN KINASES; OSTEOGENESIS; PHENOTYPE; PHOSPHORIC DIESTER HYDROLASES; PHOSPHORYLATION; PYROPHOSPHATASES; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 84885637523     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.471268     Document Type: Article

References (36)

1. Caplan, A. I., and Dennis, J. E. (2006) Mesenchymal stem cells as trophic mediators. J. Cell. Biochem. 98, 1076-1084
2. Arthur, A., Zannettino, A., and Gronthos, S. (2009) The therapeutic applications of multipotential mesenchymal/stromal stem cells in skeletal tissue repair. J. Cell. Physiol. 218, 237-245
3. Pape, H. C., Marcucio, R., Humphrey, C., Colnot, C., Knobe, M., and Harvey, E. J. (2010) Trauma-induced inflammation and fracture healing. J. Orthop. Trauma 24, 522-525
4. Bastian, O., Pillay, J., Alblas, J., Leenen, L., Koenderman, L., and Blokhuis, T. (2011) Systemic inflammation and fracture healing. J. Leukoc. Biol. 89, 669-673
5. Ni Choileain, N., and Redmond, H. P. (2006) Cell response to surgery. Arch. Surg. 141, 1132-1140
6. Wehling, N., Palmer, G. D., Pilapil, C., Liu, F., Wells, J. W., Müller, P. E., Evans, C. H., and Porter, R. M. (2009) Interleukin-1β and tumor necrosis factor α inhibit chondrogenesis by human mesenchymal stem cells through NF-kappaB-dependent pathways. Arthritis Rheum. 60, 801-812
7. Sonomoto, K., Yamaoka, K., Oshita, K., Fukuyo, S., Zhang, X., Nakano, K., Okada, Y., and Tanaka, Y. (2012) Interleukin-1β induces differentiation of human mesenchymal stem cells into osteoblasts via the Wnt-5a/receptor tyrosine kinase-like orphan receptor 2 pathway. Arthritis Rheum. 64, 3355-3363
8. Gowen, M., MacDonald, B. R., and Russell, R. G. (1988) Actions of recombinant human γ-interferon and tumor necrosis factor α on the proliferation and osteoblastic characteristics of human trabecular bone cells in vitro. Arthritis Rheum. 31, 1500-1507
9. Kuroki, T., Shingu, M., Koshihara, Y., and Nobunaga, M. (1994) Effects of cytokines on alkaline phosphatase and osteocalcin production, calcification, and calcium release by human osteoblastic cells. Br. J. Rheumatol. 33, 224-230
10. Gilbert, L., He, X., Farmer, P., Boden, S., Kozlowski, M., Rubin, J., and Nanes, M. S. (2000) Inhibition of osteoblast differentiation by tumor necrosis factor-α. Endocrinology 141, 3956-3964
11. Kaneki, H., Guo, R., Chen, D., Yao, Z., Schwarz, E. M., Zhang, Y. E., Boyce, B. F., and Xing, L. (2006) Tumor necrosis factor promotes Runx2 degradation through up-regulation of Smurf1 and Smurf2 in osteoblasts. J. Biol. Chem. 281, 4326-4333
12. Lacey, D. C., Simmons, P. J., Graves, S. E., and Hamilton, J. A. (2009) Proinflammatory cytokines inhibit osteogenic differentiation from stem cells. Implications for bone repair during inflammation. Osteoarthritis Cartilage 17, 735-742
13. Murshed, M., Harmey, D., Millán, J. L., McKee, M. D., and Karsenty, G. (2005) Unique coexpression in osteoblasts of broadly expressed genes accounts for the spatial restriction of ECM mineralization to bone. Genes Dev. 19, 1093-1104
14. Bellows, C. G., Heersche, J. N., and Aubin, J. E. (1992) Inorganic phosphate added exogenously or released from β-glycerophosphate initiates mineralization of osteoid nodules in vitro. Bone Miner. 17, 15-29
15. Fleisch, H., Russell, R. G., and Straumann, F. (1966) Effect of pyrophosphate on hydroxyapatite and its implications in calcium homeostasis. Nature 212, 901-903
16. Johnson, K. A., Hessle, L., Vaingankar, S., Wennberg, C., Mauro, S., Narisawa, S., Goding, J. W., Sano, K., Millan, J. L., and Terkeltaub, R. (2000) Osteoblast tissue-nonspecific alkaline phosphatase antagonizes and regulates PC-1. Am. J. Physiol. 279, R1365-R1377
17. Hessle, L., Johnson, K. A., Anderson, H. C., Narisawa, S., Sali, A., Goding, J. W., Terkeltaub, R., and Millan, J. L. (2002) Tissue-nonspecific alkaline phosphatase and plasma cell membrane glycoprotein-1 are central antagonistic regulators of bone mineralization. Proc. Natl. Acad. Sci. U.S.A. 99, 9445-9449
18. Johnson, K., and Terkeltaub, R. (2005) Inorganic pyrophosphate (PPi) in pathologic calcification of articular cartilage. Front. Biosci. 10, 988-997
19. Anderson, H. C. (1995) Molecular biology of matrix vesicles. Clin. Orthop. Relat. Res. 314, 266-280
20. Boskey, A. L. (1992) Mineral-matrix interactions in bone and cartilage. Clin. Orthop. Relat. Res. 281, 244-274
21. Porter, R. M., Liu, F., Pilapil, C., Betz, O. B., Vrahas, M. S., Harris, M. B., and Evans, C. H. (2009) Osteogenic potential of reamer irrigator aspirator (RIA) aspirate collected from patients undergoing hip arthroplasty. J. Orthop Res. 27, 42-49
22. Bonewald, L. F., Harris, S. E., Rosser, J., Dallas, M. R., Dallas, S. L., Camacho, N. P., Boyan, B., and Boskey, A. (2003) von Kossa staining alone is not sufficient to confirm that mineralization in vitro represents bone formation. Calcif. Tissue Int. 72, 537-547
23. Harmey, D., Hessle, L., Narisawa, S., Johnson, K. A., Terkeltaub, R., and Millán, J. L. (2004) Concerted regulation of inorganic pyrophosphate and osteopontin by akp2, enpp1, and ank. An integrated model of the pathogenesis of mineralization disorders. Am. J. Pathol. 164, 1199-1209
24. Terkeltaub, R. A., Johnson, K., Rohnow, D., Goomer, R., Burton, D., and Deftos, L. J. (1998) Bone morphogenetic proteins and bFGF exert opposing regulatory effects on PTHrP expression and inorganic pyrophosphate elaboration in immortalized murine endochondral hypertrophic chondrocytes (MCT cells). J. Bone Miner. Res. 13, 931-941
25. Yao, Z., Nakamura, H., Masuko-Hongo, K., Suzuki-Kurokawa, M., Nishioka, K., and Kato, T. (2004) Characterisation of cartilage intermediate layer protein (CILP)-induced arthropathy in mice. Ann. Rheum. Dis. 63, 252-258
26. Xiao, Z., Camalier, C. E., Nagashima, K., Chan, K. C., Lucas, D. A., de la Cruz, M. J., Gignac, M., Lockett, S., Issaq, H. J., Veenstra, T. D., Conrads, T. P., and Beck, G. R., Jr. (2007) Analysis of the extracellular matrix vesicle proteome in mineralizing osteoblasts. J. Cell. Physiol. 210, 325-335
27. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45
28. Diefenderfer, D. L., Osyczka, A. M., Garino, J. P., and Leboy, P. S. (2003) Regulation of BMP-induced transcription in cultured human bone marrow stromal cells. J. Bone Joint Surg. Am. 85, 19-28
29. Ding, J., Ghali, O., Lencel, P., Broux, O., Chauveau, C., Devedjian, J. C., Hardouin, P., and Magne, D. (2009) TNF-α and IL-1β inhibit RUNX2 and collagen expression but increase alkaline phosphatase activity and mineralization in human mesenchymal stem cells. Life Sci. 84, 499-504
30. McNamara, C. R., and Degterev, A. (2011) Small-molecule inhibitors of the PI3K signaling network. Fut. Med. Chem. 3, 549-565
31. Guardavaccaro, D., and Clevers, H. (2012) Wnt/β-catenin and MAPK signaling. Allies and enemies in different battlefields. Sci. Signal. 5, pe15
32. Scrivo, R., Vasile, M., Bartosiewicz, I., and Valesini, G. (2011) Inflammation as "common soil" of the multifactorial diseases. Autoimmun. Rev. 10, 369-374
33. Southerland, J. H., Taylor, G. W., Moss, K., Beck, J. D., and Offenbacher, S. (2006) Commonality in chronic inflammatory diseases. Periodontitis, diabetes, and coronary artery disease. Periodontology 2000 40, 130-143
34. Wei, S., Kitaura, H., Zhou, P., Ross, F. P., and Teitelbaum, S. L. (2005) IL-1 mediates TNF-induced osteoclastogenesis. J. Clin. Invest. 115, 282-290
35. Okawa, A., Nakamura, I., Goto, S., Moriya, H., Nakamura, Y., and Ikegawa, S. (1998) Mutation in Npps in a mouse model of ossification of the posterior longitudinal ligament of the spine. Nat. Genet. 19, 271-273
36. Rutsch, F., Vaingankar, S., Johnson, K., Goldfine, I., Maddux, B., Schauerte, P., Kalhoff, H., Sano, K., Boisvert, W. A., Superti-Furga, A., and Terkeltaub, R. (2001) PC-1 nucleoside triphosphate pyrophosphohydrolase deficiency in idiopathic infantile arterial calcification. Am. J. Pathol. 158, 543-554