Interleukin 6 mediates selected effects of Notch in chondrocytes

Osteoarthritis and Cartilage

Volumn 21, Issue 11, 2013, Pages 1766-1773

  Zanotti, S ^a,b   Canalis, E ^a,b  

^a SAINT FRANCIS HOSPITAL AND MEDICAL CENTER   (United States)

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

Author keywords

Acan; Chondrocytes; Col10a1; Il6; Mmp13; Notch

Indexed keywords

5,6 DICHLOROBENZIMIDAZOLE RIBOSIDE; ADENOVIRUS VECTOR; AGGRECAN; COLLAGEN TYPE 10; COLLAGEN TYPE 2; COLLAGENASE 3; GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN G; INTERLEUKIN 6; MESSENGER RNA; NEUTRALIZING ANTIBODY; NOTCH RECEPTOR; TRANSCRIPTION FACTOR SOX9; AGC1 PROTEIN, MOUSE; MMP13 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CARTILAGE CELL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CULTURE MEDIUM; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX DETERMINATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; C57BL MOUSE; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; PHYSIOLOGY; TRANSCRIPTION INITIATION;

AGGRECANS; ANIMALS; CHONDROCYTES; FEMALE; GENE EXPRESSION REGULATION; INTERLEUKIN-6; MALE; MATRIX METALLOPROTEINASE 13; MICE; MICE, INBRED C57BL; RECEPTORS, NOTCH; RNA, MESSENGER; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION;

EID: 84884973957     PISSN: 10634584     EISSN: 15229653     Source Type: Journal    
DOI: 10.1016/j.joca.2013.08.010     Document Type: Article

References (49)

1. Zanotti S., Canalis E. Notch and the skeleton. Mol Cell Biol 2010, 30:886-896.
2. Kopan R., Ilagan M.X. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 2009, 137:216-233.
3. Kovall R.A. More complicated than it looks: assembly of Notch pathway transcription complexes. Oncogene 2008, 27:5099-5109.
4. Iso T., Sartorelli V., Poizat C., Iezzi S., Wu H.Y., Chung G., et al. HERP, a novel heterodimer partner of HES/E(spl) in Notch signaling. Mol Cell Biol 2001, 21:6080-6089.
5. Olsen B.R., Reginato A.M., Wang W. Bone development. Annu Rev Cell Dev Biol 2000, 16:191-220.
6. Marcelino J., Carpten J.D., Suwairi W.M., Gutierrez O.M., Schwartz S., Robbins C., et al. CACP, encoding a secreted proteoglycan, is mutated in camptodactyly-arthropathy-coxa vara-pericarditis syndrome. Nat Genet 1999, 23:319-322.
7. Pacifici M., Koyama E., Iwamoto M. Mechanisms of synovial joint and articular cartilage formation: recent advances, but many lingering mysteries. Birth Defects Res C Embryo Today 2005, 75:237-248.
8. Elsaid K.A., Fleming B.C., Oksendahl H.L., Machan J.T., Fadale P.D., Hulstyn M.J., et al. Decreased lubricin concentrations and markers of joint inflammation in the synovial fluid of patients with anterior cruciate ligament injury. Arthritis Rheum 2008, 58:1707-1715.
9. Ballard B.L., Antonacci J.M., Temple-Wong M.M., Hui A.Y., Schumacher B.L., Bugbee W.D., et al. Effect of tibial plateau fracture on lubrication function and composition of synovial fluid. JBone Joint Surg Am 2012, 94:e64.
10. Goldring M.B., Marcu K.B. Cartilage homeostasis in health and rheumatic diseases. Arthritis Res Ther 2009, 11:224.
11. van der Kraan P.M., van den Berg W.B. Chondrocyte hypertrophy and osteoarthritis: role in initiation and progression of cartilage degeneration?. Osteoarthr Cartil 2012, 20:223-232.
12. Fosang A.J., Rogerson F.M. Identifying the human aggrecanase. Osteoarthr Cartil 2010, 18:1109-1116.
13. Roach H.I., Yamada N., Cheung K.S., Tilley S., Clarke N.M., Oreffo R.O., et al. Association between the abnormal expression of matrix-degrading enzymes by human osteoarthritic chondrocytes and demethylation of specific CpG sites in the promoter regions. Arthritis Rheum 2005, 52:3110-3124.
14. Kapoor M., Martel-Pelletier J., Lajeunesse D., Pelletier J.P., Fahmi H. Role of proinflammatory cytokines in the pathophysiology of osteoarthritis. Nat Rev Rheumatol 2011, 7:33-42.
15. Watanabe N., Tezuka Y., Matsuno K., Miyatani S., Morimura N., Yasuda M., et al. Suppression of differentiation and proliferation of early chondrogenic cells by Notch. JBone Miner Metab 2003, 21:344-352.
16. Fujimaki R., Toyama Y., Hozumi N., Tezuka K. Involvement of Notch signaling in initiation of prechondrogenic condensation and nodule formation in limb bud micromass cultures. JBone Miner Metab 2006, 24:191-198.
17. Hilton M.J., Tu X., Wu X., Bai S., Zhao H., Kobayashi T., et al. Notch signaling maintains bone marrow mesenchymal progenitors by suppressing osteoblast differentiation. Nat Med 2008, 14:306-314.
18. Mead T.J., Yutzey K.E. Notch pathway regulation of chondrocyte differentiation and proliferation during appendicular and axial skeleton development. Proc Natl Acad Sci USA 2009, 106:14420-14425.
19. Dong Y., Jesse A.M., Kohn A., Gunnell L.M., Honjo T., Zuscik M.J., et al. RBPjkappa-dependent Notch signaling regulates mesenchymal progenitor cell proliferation and differentiation during skeletal development. Development 2010, 137:1461-1471.
20. Kohn A., Dong Y., Mirando A.J., Jesse A.M., Honjo T., Zuscik M.J., et al. Cartilage-specific RBPjkappa-dependent and -independent Notch signals regulate cartilage and bone development. Development 2012, 139:1198-1212.
21. Zanotti S., Canalis E. Notch suppresses nuclear factor of activated T cells (NFAT) transactivation and Nfatc1 expression in chondrocytes. Endocrinology 2013, 154:762-772.
22. Chen S., Tao J., Bae Y., Jiang M.M., Bertin T., Chen Y., et al. Notch gain of function inhibits chondrocyte differentiation via Rbpj-dependent suppression of Sox9. JBone Miner Res 2013, 28:649-659.
23. Karlsson C., Brantsing C., Egell S., Lindahl A. Notch1, Jagged1, and HES5 are abundantly expressed in osteoarthritis. Cells Tissues Organs 2008, 188:287-298.
24. Grogan S.P., Miyaki S., Asahara H., D'Lima D.D., Lotz M.K. Mesenchymal progenitor cell markers in human articular cartilage: normal distribution and changes in osteoarthritis. Arthritis Res Ther 2009, 11:R85.
25. Hosaka Y., Saito T., Sugita S., Hikata T., Kobayashi H., Fukai A., et al. Notch signaling in chondrocytes modulates endochondral ossification and osteoarthritis development. Proc Natl Acad Sci USA 2013, 110:1875-1880.
26. Sethi N., Dai X., Winter C.G., Kang Y. Tumor-derived JAGGED1 promotes osteolytic bone metastasis of breast cancer by engaging notch signaling in bone cells. Cancer Cell 2011, 19:192-205.
27. Legendre F., Dudhia J., Pujol J.P., Bogdanowicz P. JAK/STAT but not ERK1/ERK2 pathway mediates interleukin (IL)-6/soluble IL-6R down-regulation of type II collagen, aggrecan core, and link protein transcription in articular chondrocytes. Association with a down-regulation of SOX9 expression. JBiol Chem 2003, 278:2903-2912.
28. Poree B., Kypriotou M., Chadjichristos C., Beauchef G., Renard E., Legendre F., et al. Interleukin-6 (IL-6) and/or soluble IL-6 receptor down-regulation of human type II collagen gene expression in articular chondrocytes requires a decrease of Sp1.Sp3 ratio and of the binding activity of both factors to the COL2A1 promoter. JBiol Chem 2008, 283:4850-4865.
29. Novakofski K.D., Torre C.J., Fortier L.A. Interleukin-1alpha, -6, and -8 decrease Cdc42 activity resulting in loss of articular chondrocyte phenotype. JOrthop Res 2012, 30:246-251.
30. Murtaugh L.C., Stanger B.Z., Kwan K.M., Melton D.A. Notch signaling controls multiple steps of pancreatic differentiation. Proc Natl Acad Sci USA 2003, 100:14920-14925.
31. Pfander D., Cramer T., Schipani E., Johnson R.S. HIF-1alpha controls extracellular matrix synthesis by epiphyseal chondrocytes. JCell Sci 2003, 116:1819-1826.
32. Lefebvre V., Garofalo S., Zhou G., Metsaranta M., Vuorio E., de Crombrugghe B. Characterization of primary cultures of chondrocytes from type II collagen/beta-galactosidase transgenic mice. Matrix Biol 1994, 14:329-335.
33. Zanotti S., Smerdel-Ramoya A., Stadmeyer L., Durant D., Radtke F., Canalis E. Notch inhibits osteoblast differentiation and causes osteopenia. Endocrinology 2008, 149:3890-3899.
34. Zanotti S., Smerdel-Ramoya A., Canalis E. Reciprocal regulation of notch and nuclear factor of activated T-cells (NFAT)c1 transactivation in osteoblasts. JBiol Chem 2011, 286:4576-4588.
35. Zanotti S., Smerdel-Ramoya A., Canalis E. Nuclear factor of activated T-cells (NFAT)C2 inhibits Notch receptor signaling in osteoblasts. JBiol Chem 2013, 288:624-632.
36. Canalis E., Parker K., Feng J.Q., Zanotti S. Osteoblast lineage-specific effects of notch activation in the skeleton. Endocrinology 2013, 154:623-634.
37. Allen D.L., Uyenishi J.J., Cleary A.S., Mehan R.S., Lindsay S.F., Reed J.M. Calcineurin activates interleukin-6 transcription in mouse skeletal muscle invivo and in C2C12 myotubes invitro. Am J Physiol Regul Integr Comp Physiol 2010, 298:R198-R210.
38. Nye J.S., Kopan R., Axel R. An activated Notch suppresses neurogenesis and myogenesis but not gliogenesis in mammalian cells. Development 1994, 120:2421-2430.
39. Strobl L.J., Hofelmayr H., Stein C., Marschall G., Brielmeier M., Laux G., et al. Both Epstein-Barr viral nuclear antigen 2 (EBNA2) and activated Notch1 transactivate genes by interacting with the cellular protein RBP-J kappa. Immunobiology 1997, 198:299-306.
40. Tso J.Y., Sun X.H., Kao T.H., Reece K.S., Wu R. Isolation and characterization of rat and human glyceraldehyde-3-phosphate dehydrogenase cDNAs: genomic complexity and molecular evolution of the gene. Nucleic Acids Res 1985, 13:2485-2502.
41. Nakagawa O., Nakagawa M., Richardson J.A., Olson E.N., Srivastava D. HRT1, HRT2, and HRT3: a new subclass of bHLH transcription factors marking specific cardiac, somitic, and pharyngeal arch segments. Dev Biol 1999, 216:72-84.
42. Kouadjo K.E., Nishida Y., Cadrin-Girard J.F., Yoshioka M., St-Amand J. Housekeeping and tissue-specific genes in mouse tissues. BMC Genomics 2007, 8:127.
43. Bland J.M., Altman D.G. Multiple significance tests: the Bonferroni method. BMJ 1995, 310:170.
44. Sokal R.R., Rohlf F.J. Biometry 1981, 2nd edn.
45. Grogan S.P., Olee T., Hiraoka K., Lotz M.K. Repression of chondrogenesis through binding of notch signaling proteins HES-1 and HEY-1 to N-box domains in the COL2A1 enhancer site. Arthritis Rheum 2008, 58:2754-2763.
46. Canalis E., Delany A.M. Mechanisms of glucocorticoid action in bone. Ann N Y Acad Sci 2002, 966:73-81.
47. Guerne P.A., Carson D.A., Lotz M. IL-6 production by human articular chondrocytes. Modulation of its synthesis by cytokines, growth factors, and hormones invitro. JImmunol 1990, 144:499-505.
48. Wongchana W., Palaga T. Direct regulation of interleukin-6 expression by Notch signaling in macrophages. Cell Mol Immunol 2012, 9:155-162.
49. Jin S., Mutvei A.P., Chivukula I.V., Andersson E.R., Ramskold D., Sandberg R., et al. Non-canonical Notch signaling activates IL-6/JAK/STAT signaling in breast tumor cells and is controlled by p53 and IKKalpha/IKKbeta. Oncogene 2012, 10.1038/onc.2012.517.