The ERK5 and ERK1/2 signaling pathways play opposing regulatory roles during chondrogenesis of adult human bone marrow-derived multipotent progenitor cells

Journal of Cellular Physiology

Volumn 224, Issue 1, 2010, Pages 178-186

  Bobick, Brent E ^a,c   Matsche, Alexander I ^a   Chen, Faye H ^a   Tuan, Rocky S ^a,b  

^a NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AGGRECAN; ALCIAN BLUE; COLLAGEN TYPE 2; COLLAGEN TYPE 2A1; FIBROBLAST GROWTH FACTOR 2; LUCIFERASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE 5; PROTEOGLYCAN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SOX5; TRANSCRIPTION FACTOR SOX6; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA3; UNCLASSIFIED DRUG; MAP2K5 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1;

ADULT; AGED; ARTICLE; BONE MARROW CELL; CHONDROGENESIS; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FEMALE; GENE CONSTRUCT; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HYALINE CARTILAGE; MALE; MARKER GENE; MULTIPOTENT STEM CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REGULATORY MECHANISM; RNA TRANSCRIPTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ADULT STEM CELL; CARTILAGE; CELL CULTURE; CELL DIFFERENTIATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; MIDDLE AGED; PHOSPHORYLATION; RNA INTERFERENCE; STEM CELL; TIME;

ADULT STEM CELLS; AGED; AGED, 80 AND OVER; BONE MARROW CELLS; CARTILAGE; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROGENESIS; FEMALE; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION; HUMANS; MALE; MAP KINASE KINASE 1; MAP KINASE KINASE 5; MAP KINASE SIGNALING SYSTEM; MIDDLE AGED; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASE 7; MULTIPOTENT STEM CELLS; PHOSPHORYLATION; RNA INTERFERENCE; RNA, MESSENGER; STEM CELLS; TIME FACTORS; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA3;

EID: 77952483724     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22120     Document Type: Article

References (47)

1. Baksh D, Song L, Tuan RS. 2004. Adult mesenchymal stem cells: Characterization, differentiation, and application in cell and gene therapy. J Cell Mol Med 8:301-316. (Pubitemid 44145494)
2. Barry F, Boynton RE, Liu B, Murphy JM. 2001. Chondrogenic differentiation of mesenchymal stem cells from bone marrow: Differentiation-dependent gene expression of matrix components. Exp Cell Res 268:189-200.
3. Ben-Eliezer M, Phillip M, Gat-Yablonski G. 2007. Leptin regulates chondrogenic differentiation in ATDC5 cell-line through JAK/STAT and MAPK pathways. Endocrine 32:235-244.
4. Bobick BE, Kulyk WM. 2004. The MEK-ERK signaling pathway is a negative regulator of cartilage-specific gene expression in embryonic limb mesenchyme. J Biol Chem 279:4588-4595.
5. Bobick BE, Kulyk WM. 2006. MEK-ERK signaling plays diverse roles in the regulation of facial chondrogenesis. Exp Cell Res 312:1079-1092.
6. Bobick BE, Kulyk WM. 2008. Regulation of cartilage formation and maturation by mitogen-activated protein kinase signaling. Birth Defects Res C Embryo Today 84:131-154.
7. Bobick BE, Chen FH, Le AM, Tuan RS. 2009. Regulation of the chondrogenic phenotype in culture. Birth Defects Res C Embryo Today 87:351-371.
8. Borsch-Haubold AG, Pasquet S, Watson SP. 1998. Direct inhibition of cyclooxygenase-1 and -2 by the kinase inhibitors SB 203580 and PD 98059. SB 203580 also inhibits thromboxane synthase. J Biol Chem 273:28766-28772.
9. Browne JA, Pearson AL, Zahr RA, Niculescu-Duvaz I, Baines DL, Dockrell ME. 2008. TGF-beta activates ERK5 in human renal epithelial cells. Biochem Biophys Res Commun 373:440-444.
10. Byers BA, Mauck RL, Chiang IE, Tuan RS. 2008. Transient exposure to transforming growth factor beta 3 under serum-free conditions enhances the biomechanical and biochemical maturation of tissue-engineered cartilage. Tissue Eng Part A 14:1821-1834.
11. Chen FH, Tuan RS. 2008. Mesenchymal stem cells in arthritic diseases. Arthritis Res Ther 10:223.
12. Chen FH, Rousche KT, Tuan RS. 2006. Technology insight: Adult stem cells in cartilage regeneration and tissue engineering. Nat Clin Pract Rheumatol 2:373-382.
13. DeLise AM, Fischer L, Tuan RS. 2000. Cellular interactions and signaling in cartilage development. Osteoarthritis Cartilage 8:309-334.
14. Friedenstein AJ, Piatetzky S II, Petrakova KV. 1966. Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol 16:381-390.
15. Gould MC, Stephano JL. 2000. Inactivation of Ca(2+) action potential channels by the MEK inhibitor PD98059. Exp Cell Res 260:175-179.
16. Haleem-Smith H, Derfoul A, Okafor C, Tuli R, Olsen D, Hall DJ, Tuan RS. 2005. Optimization of high-efficiency transfection of adult human mesenchymal stem cells in vitro. Mol Biotechnol 30:9-20.
17. Hayashi M, Lee JD. 2004. Role of the BMK1/ERK5 signaling pathway: Lessons from knockout mice. J Mol Med 82:800-808.
18. Huang AH, Yeger-McKeever M, Stein A, Mauck RL. 2008. Tensile properties of engineered cartilage formed from chondrocyte- and MSC-laden hydrogels. Osteoarthritis Cartilage 16:1074-1082.
19. Kamakura S, Moriguchi T, Nishida E. 1999. Activation of the protein kinase ERK5/BMK1 by receptor tyrosine kinases. Identification and characterization of a signaling pathway to the nucleus. J Biol Chem 274:26563-26571. (Pubitemid 129520095)
20. Lee JW, Kim YH, Kim SH, Han SH, Hahn SB. 2004. Chondrogenic differentiation of mesenchymal stem cells and its clinical applications. Yonsei Med J 45:41-47. (Pubitemid 39010732)
21. Lefebvre V, Smits P. 2005. Transcriptional control of chondrocyte fate and differentiation. Birth Defects Res C Embryo Today 75:200-212.
22. Lima EG, Bian L, Ng KW, Mauck RL, Byers BA, Tuan RS, Ateshian GA, Hung CT. 2007. The beneficial effect of delayed compressive loading on tissue-engineered cartilage constructs cultured with TGF-beta3. Osteoarthritis Cartilage 15:1025-1033.
23. McMahon LA, Prendergast PJ, Campbell VA. 2008. A comparison of the involvement of p38, ERK1/2, and PI3K in growth factor-induced chondrogenic differentiation of mesenchymal stem cells. Biochem Biophys Res Commun 368: 990-995.
24. Mody N, Leitch J, Armstrong C, Dixon J, Cohen P. 2001. Effects of MAP kinase cascade inhibitors on the MKK5/ERK5 pathway. FEBS Lett 502:21-24.
25. Mueller MB, Tuan RS. 2008. Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells. Arthritis Rheum 58:1377-1388.
26. Nesti LJ, Jackson WM, Shanti RM, Koehler SM, Aragon AB, Bailey JR, Sracic MK, Freedman BA, Giuliani JR, Tuan RS. 2008. Differentiation potential of multipotent progenitor cells derived from war-traumatized muscle tissue. J Bone Joint Surg Am 90:2390-2398.
27. Nishimoto S, Nishida E. 2006. MAPK signalling: ERK5 versus ERK1/2. EMBO Rep 7:782-786.
28. Ramos-Nino ME, Scapoli L, Martinelli M, Land S, Mossman BT. 2003. Microarray analysis and RNA silencing link fra-1 to cd44 and c-met expression in mesothelioma. Cancer Res 63:3539-3545. (Pubitemid 36793033)
29. Regan CP, Li W, Boucher DM, Spatz S, Su MS, Kuida K. 2002. Erk5 null mice display multiple extraembryonic vascular and embryonic cardiovascular defects. Proc Natl Acad Sci USA 99:9248-9253.
30. Ross MH, Kaye GI, Pawlina W. 2003. Cartilage. Histology: A text and atlas with cell and molecular biology. 4 edition. Philadelphia: Lippincott Williams & Wilkins. pp 164-179.
31. Roux PP, Blenis J. 2004. ERK and p38 MAPK-activated protein kinases: A family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 68:320-344.
32. Rubinfeld H, Seger R. 2005. The ERK cascade:Aprototype of MAPK signaling. Mol Biotechnol 31:151-174.
33. Seghatoleslami MR, Roman-Blas JA, Rainville AM, Modaressi R, Danielson KG, Tuan RS. 2003. Progression of chondrogenesis in C3H10T1/2 cells is associated with prolonged and tight regulation of ERK1/2. J Cell Biochem 88:1129-1144.
34. Sekiya I, Vuoristo JT, Larson BL, Prockop DJ. 2002. In vitro cartilage formation by human adult stem cells from bone marrow stroma defines the sequence of cellular and molecular events during chondrogenesis. Proc Natl Acad Sci USA 99:4397-4402.
35. Sekiya I, Larson BL, Vuoristo JT, Reger RL, Prockop DJ. 2005. Comparison of effect of BMP-2, -4, and -6 on in vitro cartilage formation of human adult stem cells from bone marrow stroma. Cell Tissue Res 320:269-276.
36. Solchaga LA, Penick K, Porter JD, Goldberg VM, Caplan AI, Welter JF. 2005. FGF-2 enhances the mitotic and chondrogenic potentials of human adult bone marrow-derived mesenchymal stem cells. J Cell Physiol 203:398-409.
37. Song H, Jin X, Lin J. 2004. Stat3 upregulates MEK5 expression in human breast cancer cells. Oncogene 23:8301-8309.
38. Stanton LA, Underhill TM, Beier F. 2003. MAP kinases in chondrocyte differentiation. Dev Biol 263:165-175.
39. Steinert AF, Ghivizzani SC, Rethwilm A, Tuan RS, Evans CH, Noth U. 2007. Major biological obstacles for persistent cell-based regeneration of articular cartilage. Arthritis Res Ther 9:213.
40. Tew SR, Li Y, Pothacharoen P, Tweats LM, Hawkins RE, Hardingham TE. 2005. Retroviral transduction with SOX9 enhances re-expression of the chondrocyte phenotype in passaged osteoarthritic human articular chondrocytes. Osteoarthritis Cartilage 13:80-889.
41. Tuan RS, Chen FH. 2006. Cartilage. In: Battler A, Leor J, editors. Stem cell and gene-based therapy: Frontiers in regenerative medicine. London: Springer. pp 179-193.
42. Tuli R, Tuli S, Nandi S, Huang X, Manner PA, Hozack WJ, Danielson KG, Hall DJ, Tuan RS. 2003. Transforming growth factor-beta-mediated chondrogenesis of humanmesenchymal progenitor cells involves N-cadherin and mitogen-activated protein kinase and Wnt signaling cross-talk. J Biol Chem 278:41227-41236.
43. Turjanski AG, Vaque JP, Gutkind JS. 2007. MAP kinases and the control of nuclear events. Oncogene 26:3240-3253.
44. Wang X, Tournier C. 2006. Regulation of cellular functions by the ERK5 signalling pathway. Cell Signal 18:753-760.
45. Wooley PH, Grimm MJ, Radin EL. 2005. The structure and function of joints. In: Koopman WJ, Morel LW, editors. Arthritis and allied conditions: A textbook of rheumatology. 15 edition. Philadelphia: Lippincott Williams & Wilkins. pp 149-173.
46. Yan L, Carr J, Ashby PR, Murry-Tait V, Thompson C, Arthur JS. 2003. Knockout of ERK5 causes multiple defects in placental and embryonic development. BMC Dev Biol 3:11.
47. Yanai Y, Micallef MJ, Yamamoto S, Yamamoto K, Yamauchi H, Ikegami H, Kurimoto M. 2003. Expression profiling of tumor necrosis factor alpha-induced apoptosis-associated genes in human solid tumor cell lines. Anticancer Res 23:2339-2348. (Pubitemid 36897101)