The role of the Notch pathway in healthy and osteoarthritic articular cartilage: From experimental models to ex vivo studies

Arthritis Research and Therapy

Volumn 13, Issue 2, 2011, Pages

  Sassi, Nadia ^a   Laadhar, Lilia ^a   Driss, Maha ^b   Kallel Sellami, Meriam ^a   Sellami, Slaheddine ^a   Makni, Sondes ^a  

^a LA RABTA HOSPITAL   (Tunisia)

^b SALAH AZAIEZ INSTITUTE   (Tunisia)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CSL; UNCLASSIFIED DRUG;

ARTICULAR CARTILAGE; BONE DEVELOPMENT; CARTILAGE CELL; CELL FUNCTION; CONTROLLED STUDY; HUMAN; NONHUMAN; OSTEOARTHRITIS; PROTEIN EXPRESSION; REVIEW; ANIMAL; CYTOLOGY; METABOLISM; PATHOLOGY;

ANIMALS; CARTILAGE, ARTICULAR; CHONDROCYTES; HUMANS; OSTEOARTHRITIS; RECEPTORS, NOTCH;

EID: 80053248917     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3255     Document Type: Review

References (77)

1. Kouri JB, Lavalle C. Do chondrocytes undergo activation and transdifferentiation during the pathogenesis of osteoarthritis? A review of the ultrastructural and immunohistochemical evidence. Histol Histopathol 2006, 21:793-802.
2. Cai SA, Fu X, Sheng Z. Dedifferentiation: a new approach in stem cell research. Bioscience 2007, 57:655-662.
3. Greenberg DA, Jin K. Turning neurogenesis up a Notch. Nat Med 2006, 12:884-885. 10.1038/nm0806-884, 16892029.
4. Yoon K, Gaiano N. Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat Neurosci 2005, 8:709-715. 10.1038/nn1475, 15917835.
5. Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, Martin RP, Schipani E, Divieti P, Bringhurst FR, Milner LA, Kronenberg HM, Scadden DT. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003, 425:841-846. 10.1038/nature02040, 14574413.
6. Tsakonas SA, Matsuno K, Fortini M. Notch signaling. Science 1995, 268:225-232. 10.1126/science.7716513, 7716513.
7. Tsakonas SA, Rand MD, Lake RJ. Notch signaling: cell fate control and signal integration in development. Science 1999, 284:770-776. 10.1126/science.284.5415.770, 10221902.
8. Hayes AJ, Dowthwaite GP, Webster SV, Archer CW. The distribution of Notch receptors and their ligands during articular cartilage development. J Anat 2003, 202:495-502. 10.1046/j.1469-7580.2003.00185.x, 1571106, 12846471.
9. Watanabe N, Tezuka Y, Matsuno K, Miyatani S, Morimura N, Yasuda M, Fujimaki R, Kuroda K, Hiraki Y, Hozumi N, Tezuka K. Suppression of differentiation and proliferation of early chondrogenic cells by Notch. J Bone Miner Metab 2003, 21:344-352. 10.1007/s00774-003-0428-4, 14586790.
10. Karlsson C, Jonsson M, Asp J. Notch and HES5 are regulated during human cartilage differentiation. Cell Tissue Res 2007, 327:539-551. 10.1007/s00441-006-0307-0, 17093926.
11. Dexter JS. The analysis of a case of continuous variation in Drosophila by a study of its linkage relations. Am Nat 1914, 48:712-758.
12. Bridges CB. Deficiency. Genetics 1917, 2:445-465. 1193728, 17245891.
13. Morgan LV. Non-criss-cross inheritance in Drosophila melanogaster. Biol Bull 1922, 42:267-274.
14. Brou C. intracellular trafficking of Notch receptors and ligands. Exp Cell Res 2009, 315:1549-1555. 10.1016/j.yexcr.2008.09.010, 18845146.
15. Talora C, Campese AF, Bellavia D, Felli MP, Vacca A, Gulino A, Screpenti I. Notch signaling and diseases: an evolutionary journey from a simple beginning to complex outcomes. Biochem Biophys Acta 2008, 1782:489-497.
16. Egan SE, Pierre B, Leow C. Notch receptors, partners and regulators: from conserved domains to powerful functions. Curr Top Microbiol Immunol 1998, 228:273-324.
17. Kao HY, Ordentlich P, Koyano Nakagawa N, Tang Z, Downes M, Kintner CR, Evans RM, Kadesch T. A histone desacetylase corepressor complex regulates the Notch signal transduction pathway. Genes Dev 1998, 12:2269-2277. 10.1101/gad.12.15.2269, 317043, 9694793.
18. Arias AM, Zecchini V, Brennan K. CSL-independant Notch signaling: a checkpoint in cell fate decisions during development?. Curr Opin Genet Dev 2002, 12:524-533. 10.1016/S0959-437X(02)00336-2, 12200157.
19. Fortini M. Notch and presenilin: a proteolytic mechanism emerges. Curr Opin Cell Biol 2001, 13:627-634. 10.1016/S0955-0674(00)00261-1, 11544033.
20. Schweisguth F. Regulation of Notch signaling activity. Curr Biol 2004, 14(3):129-138.
21. Fiùza UM, Arias AM. Cell and molecular biology of Notch. J Endocrinol 2007, 194:459-474.
22. Ohsako S, Hyer J, Panganiban G, Oliver I, Caudy M. Hairy function as a DNA-binding helix-loop-helix repressor of Drosophila sensory organ formation. Genes Dev 1994, 8:2743-2755. 10.1101/gad.8.22.2743, 7958930.
23. Ohtsuka T, Ishibashi M, Gradwohl G, Nakanishi S, Guillemot F, Kageyama R. Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. EMBO J 1999, 18:2196-21207. 10.1093/emboj/18.8.2196, 1171303, 10205173.
24. Iso T, Kedes L, Hamamori Y. HES and HERP families: multiple effectors of the Notch signaling pathway. J Cell Physiol 2003, 194:237-255. 10.1002/jcp.10208, 12548545.
25. Shawber C, Nofziger D, Hsieh JD, Lindsell C, Bögler O, Hayward D, Weinmaster G. Notch signaling inhibits muscle cell differentiation through a CBF1-independent pathway. Development 1996, 122:3765-3773.
26. Donna Nofziger D, Alison Miyamoto A, Karen M, Weinmaster G. Notch signaling imposes two distinct blocks in the differentiation of C2C12 myoblasts. Development 1999, 126:1689-1702.
27. Maillard I, Koch U, Dumortier A, Shestova O, Xu L, Sai H, Pross SE, Aster JC, Bhandoola A, Radtke F, Pear WS. Canonical Notch signaling is dispensable for the maintenance of adult hematopoietic stem cells. Cell Stem Cell 2008, 2:356-366. 10.1016/j.stem.2008.02.011, 18397755.
28. Baum B, Perrimon N. Spatial control of the actin cytoskeleton in Drosophila epithelial cells. Nat Cell Biol 2001, 3:883-890. 10.1038/ncb1001-883, 11584269.
29. Bear JE, Loureiro JJ, Libova I, Fassler R, Wehland J, Gertler FB. Negative regulation of fibroblast motility by Ena/VASP proteins. Cell 2000, 101:717-728. 10.1016/S0092-8674(00)80884-3, 10892743.
30. Gertler FB, Bennett RL, Clark MJ, Hoffmann FM. Drosophila Abl tyrosine kinase in embryonic CNS axons: A role in axonogenesis is revealed through dosage-sensitive interactions with disabled. Cell 1989, 58:103-113. 10.1016/0092-8674(89)90407-8, 2502313.
31. Grevengoed EE, Loureiro JJ, Jesse TL, Peifer M. Abelson kinase regulates epithelial morphogenesis in Drosophila. J Cell Biol 2001, 155:1185-1198. 10.1083/jcb.200105102, 2199330, 11756472.
32. Luo L. Trio quartet in D. melanogaster. Neuron 2000, 26:1-2. 10.1016/S0896-6273(00)81129-0, 10798384.
33. Wills Z, Bateman J, Korey CA, Comer A, Van Vactor D. The tyrosine kinase Abl and its substrate enabled collaborate with the receptor phosphatase Dlar to control motor axon guidance. Neuron 1999, 22:301-312. 10.1016/S0896-6273(00)81091-0, 10069336.
34. Druker BJ, Talpaz M, Resta DJ, Peng B, Buchdunger E, Ford JM, Lydon NB, Kantarjian H, Capdeville R, Ohno-Jones S, Sawyers CL. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med 2001, 344:1031-1037. 10.1056/NEJM200104053441401, 11287972.
35. Fainstein E, Marcelle C, Rosner A, Canaani E, Gale RP, Dreazen O, Smith SD, Croce CM. A new fused transcript in Philadelphia chromosome positive acute lymphocytic leukemia. Nature 1987, 330:386-388. 10.1038/330386a0, 2825022.
36. Goff SP, Gilboa E, Witte ON, Baltimore D. Structure of the Abelson murine leukemia virus genome and the homologous cellular gene: Studies with cloned viral DNA. Cell 1980, 22:777-785. 10.1016/0092-8674(80)90554-1, 6257398.
37. Giniger E. A role for Abl in Notch signaling. Neuron 1998, 20:667-681. 10.1016/S0896-6273(00)81007-7, 9581760.
38. Le Gall M, De Matter C, Giniger E. Molecular separation of two signaling pathways for the receptor Notch. Dev Biol 2008, 313:556-567. 10.1016/j.ydbio.2007.10.030, 2262048, 18062953.
39. Espinosa L, Ingles-Esteve J, Robert-Moreno A, Bigas A. IkappaBalpha and p65 regulate the cytoplasmic shuttling of nuclear corepressor: crosstalk between Notch and NFkappaB pathways. Mol Biol Cell 2003, 14:491-502. 10.1091/mbc.E02-07-0404, 149987, 12589049.
40. Vacca A, Felli MP, Palermo R, Di Mario G, Calce A, Di Giovine M, Frati L, Gulino A, Screpanti I. Notch3 and pre-TCR interaction unveils distinct NF-kappaB pathways in T-cell development and leukemia. EMBO J 2006, 25:1000-1008. 10.1038/sj.emboj.7600996, 1409728, 16498412.
41. Williams R, Nelson L, Dowthwaite GP, Evans DJ, Archer CW. Notch receptor and Notch ligands expression in developing avian cartilage. J Anat 2009, 215:159-169. 10.1111/j.1469-7580.2009.01089.x, 19490397.
42. Crowe R, Zikherman J, Niswander L. Delta 1 negatively regulates the transition from prehypertrophic chondrocytes to hypertrophic chondrocytes. Development 1999, 126:987-998.
43. Bolos V, Grego-Bessa J, de la Pompa JL. Notch signaling in development and cancer. Endocr Rev 2007, 28:339-369. 10.1210/er.2006-0046, 17409286.
44. Henson FM, Bowe EA, Daves ME. Promotion of the intrinsic damage-repair response in articular cartilage by fibroblast growth factor. Osteoarthritis Cartilage 2005, 13:537-544. 10.1016/j.joca.2005.02.007, 15922188.
45. Hardingham TE, Oldershaw R, Tew RS. Cartilage, sox9 and Notch signals in chondrogenesis. J Anat 2006, 209:469-480. 10.1111/j.1469-7580.2006.00630.x, 2100356, 17005019.
46. Hayes AJ, MacPherson S, Morrisson H, Dowthwaite GP, Archer CW. The development of articular cartilage evidence of an appositional growth mechanism. Anat Embryol 2001, 203:469-479. 10.1007/s004290100178, 11453164.
47. Oldershaw R, Murdoch A, Brennan K. The putative role of the Notch ligand, jagged1, in the mediation of the early events of human mesenchymal stem cell chondrogenesis. Int J Exp Pathol 2005, 86:47-48.
48. Kageyama R, Ohtsuka T, Hatakeyama J, Ohsawa R. Roles of bHLH genes in neural stem cell differentiation. Exp Cell Res 2005, 306:343-348. 10.1016/j.yexcr.2005.03.015, 15925590.
49. Grogan SP, Tsaiwei Olee T, Hiraoka K, Lotz MK. Notch signaling proteins Hes-1 and Hey-1 bind N-box domains in the Col2a1 enhancer site to repress chondrogenesis. Arthritis Rheum 2008, 58:2754-2763. 10.1002/art.23730, 2786215, 18759300.
50. Oldershaw R, Hardingham TE. Notch signaling during chondrogenesis of human bone marrow stem cells. Bone 2010, 46:286-293. 10.1016/j.bone.2009.04.242, 19406255.
51. Dowthwaite G, Bishop J, Redman S, Khan IM, Rooney P, Evans DJR, Haughton L, Bayram Z, Boyer S, Thomson B, Wolfe MS, Archer CW. The surface of articular cartilage contains a progenitor cell population. J Cell Sci 2004, 117:889-897. 10.1242/jcs.00912, 14762107.
52. Ustunel I, Ozenci AM, Sahin Z, Ozbey O, Acar N, Tanriover G, Celik-Ozenci C, Demir R. The immunohistochemical localization of Notch receptors and ligands in human articular cartilage, chondroprogenitor culture and ultrustructural characterestics of these progenitor cells. Acta Histochem 2008, 110:397-407. 10.1016/j.acthis.2007.12.005, 18272209.
53. Grogan SP, Miyaki S, Asahara H, D'Lima D, Lotz MK. Mesenchymal progenitor cell markers in human articular cartilage: normal distribution and changes in osteoarthritis. Arthritis Res Ther 2009, 11:R85. 10.1186/ar2719, 2714136, 19500336.
54. Laadhar L, Zitouni M, Kallel-Sellami M, Mahjoub M, Sellami S, Makni S. Physiopathology of osteoarthritis: from normal cartilage to osteoarthritic cartilage: risk factors and inflammatory mechanisms. Rev Med Interne 2007, 28:531-536. 10.1016/j.revmed.2007.01.012, 17316922.
55. Nagase H, Kashiwagi M. Aggrecanases and cartilage matrix degradation. Arthritis Res Ther 2003, 5:94-103. 10.1186/ar630, 165039, 12718749.
56. Poole AR, Kobayashi M, Yasuda T, Laverty S, Mwale F, Kojima T, Sakai T, Wahl C, El-Madawy S, Webb G, Tchetina E, Wu W. Type II collagen degradation and its regulation in articular cartilage in osteoarthritis. Ann Rheum Dis 2002, 61:78-81.
57. Van Beuningen HM, stoop R, Buma P, Takahashi N, Van Der Kraan PM, Van Den Berg WB. Phenotypic differences in murine chondrocyte cell lines from mature articular cartilage. Osteoarthritis Cartilage 2002, 10:977-986. 10.1053/joca.2002.0855, 12464558.
58. Eyre DR, McDevitt CA, Billigham MEG, Muir H. Biosynthesis of collagen and other matrix proteins by articular cartilage in experimental osteoarthritis. Biochem J 1980, 188:823-837. 1161967, 7470037.
59. Burton-Wuster N, Hui-Chou CS, Greisen HA, Lust G. Reduced deposition of in the degenerated articular cartilage of dogs with degenerative joint disease. Biochem Biophys Acta 1982, 718:74-84.
60. Miller DR, Lust G. Accumulation of procollagen in the degenerative articular cartilage of dogs with osteoarthritis. Biochem Biophys Acta 1979, 583:218-231.
61. Abbud Lozoya K, Kouri JB. A novel rat osteoarthritis model to assess apoptosis and matrix degradation. Pathol Res Pract 2000, 196:729-745.
62. Kouri Flores JB, Abbud Lozoya K, Morales RL. Kinetics of the ultrastructural changes in apoptotic chondrocytes from an osteoarthritic rat model: a window of comparison to the cellular mechanisms of apoptosis in human chondrocytes. Ultrastruct Pathol 2002, 26:33-40. 10.1080/01913120252934314, 12028657.
63. Matyas JR, Huang D, Chung M, Adams ME. Regional quantification of cartilage type II collagen and aggrecan messenger RNA in joints with early experimental osteoarthritis. Arthritis Rheum 2002, 46:1536-1543. 10.1002/art.10331, 12115184.
64. Grundmann K, Zimmermann B, Barrach HJ, Merker HJ. Behaviour of epiphyseal mouse chondrocyte populations in monolayer culture: Morphological and immunohistochemical studies. Virchows Arch A Pathol Anat Histol 1980, 389:167-187. 10.1007/BF00439484, 7456325.
65. Salvat C, Pigenet A, Humbert L, Berembaum F, Thirion S. Immature murine articular chondrocytes in primary culture: a new tool for investigating cartilage. Osteoarthritis Cartilage 2005, 13:243-249. 10.1016/j.joca.2004.11.008, 15727891.
66. Blaise R, Mahjoub M, Salvat C, Barbe U, Brou C, Corvol MT, Savouret JF, Rannou F, Berenbaum F, Bausero P. Involvement of the Notch pathway in the regulation of matrix metalloproteinase 13 and the dedifferentiation of articular chondrocytes in murine cartilage. Arthritis Rheum 2009, 60:428-439. 10.1002/art.24250, 19180482.
67. Sassi N, Laadhar L, Mahjoub M, Kallel-Sellami M, Zitouni M, Makni S, Sellami S. Expression of Notch family members in cultured murine articular chondrocytes. Biotech Histochem 2009, 84:313-320. 10.3109/10520290903054382, 19562571.
68. Svanvik T, Barreto Henriksson H, Karlsson C, Hagman M, Lindahl A, Brisby H. Human disk cells from degenerated disks and mesenchymal stem cells in co-culture result in increased matrix production. Cells Tissues Organs 2010, 191:2-11. 10.1159/000223236, 19494482.
69. Dong Y, Jesse AM, Kohn A, Gunnell LM, Honjo T, Zuscik MJ, O'Keefe RJ, Hilton MJ. RBPjk-dependent Notch signaling regulates mesenchymal progenitor cell proliferation and differentiation during skeletal development. Development 2010, 137:1461-1471. 10.1242/dev.042911, 20335360.
70. Alsalameh S, Amin R, Gemba T, Lotz M. Identification of mesenchymal progenitor cells in normal and osteoarthritic human articular cartilage. Arthritis Rheum 2004, 50:1522-1532. 10.1002/art.20269, 15146422.
71. Hiraoka K, Grogan S, Olee T, Lotz M. Mesenchymal progenitor cells in adult human articular cartilage. Biorheology 2006, 43:447-454.
72. Karlsson C, Brantsing C, Egell S, Lindahl A. Notch1, Jagged1, and HES5 are abundantly expressed in osteoarthritis. Cells Tissues Organs 2008, 188:287-298. 10.1159/000121610, 18354251.
73. Williams R, Ilyas M, Khan IK, Kirsty Richardson K, Larissa Nelson L, McCarthy H, Analbelsi T, Singhrao SK, Dowthwaite GP, Jones RE, Baird DM, Lewis H, Roberts S, Shaw HM, Dudhia J, Fairclough J, Briggs T, Archer CW. Identification and clonal characterisation of a progenitor cell sub-population in normal human articular cartilage. PLoS ONE 2010, 5:e13246. 10.1371/journal.pone.0013246, 2954799, 20976230.
74. Barbero A, Ploegert S, Herherer M, Martin I. Plasticity of clonal populations of dedifferentiated adult human articular chondrocytes. Arthritis Rheum 2003, 48:1315-1325. 10.1002/art.10950, 12746904.
75. Diaz-Romero J, Gaillard JP, Grogan SP, Nesic D, Trub T, Mainil-Varlet P. Immunophenotypic analysis of human articular chondrocytes: changes in surface markers associated with cell expansion in monolayer culture. J Cell Physiol 2005, 202:731-742. 10.1002/jcp.20164, 15389573.
76. Diaz-Romero J, Nesic D, Grogan SP, Heini P, Mainil-Varlet P. Immunophenotypic changes of human articular chondrocytes during monolayer culture reflect bona fide dedifferentiation rather than amplification of progenitor cells. J Cell Physiol 2008, 214:75-83. 10.1002/jcp.21161, 17559082.
77. De la Fuente R, Abad JL, Castro JG, Miguel GF, Petriz J, Rubio D, Abejon CV, Guillen P, Gonzalez MA, Bernada A. Dedifferentiated adult articular chondrocytes: a population of human multipotent primitive cells. Exp Cell Res 2004, 297:313-328. 10.1016/j.yexcr.2004.02.026, 15212937.