Identification and clonal characterisation of a progenitor cell sub-population in normal human articular cartilage

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Williams, Rebecca ^a   Khan, Ilyas M ^a   Richardson, Kirsty ^a   Nelson, Larissa ^a   McCarthy, Helen E ^a   Analbelsi, Talal ^a   Singhrao, Sim K ^a   Dowthwaite, Gary P ^a   Jones, Rhiannon E ^b   Baird, Duncan M ^b   Lewis, Holly ^c   Roberts, Selwyn ^c   Shaw, Hannah M ^a   Dudhia, Jayesh ^d   Fairclough, John ^c   Briggs, Timothy ^e   Archer, Charles W ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c UNIVERSITY HOSPITAL OF WALES   (United Kingdom)

^d ROYAL VETERINARY COLLEGE   (United Kingdom)

^e ROYAL NATIONAL ORTHOPAEDIC HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; TELOMERASE; PRIMER DNA;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHROPATHY; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE CELL; CELL ADHESION; CELL ASSAY; CELL CLONE; CELL DIFFERENTIATION; CELL ISOLATION; CELL LINE; CELL SUBPOPULATION; CHILD; CHONDROGENESIS; CHONDROPATHY; CHROMOSOME SIZE; CONTROLLED STUDY; CULTURE MEDIUM; DISEASE MODEL; EMBRYO; ENZYME ACTIVITY; FEMALE; GOAT; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IN VIVO STUDY; KARYOTYPE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; NORMAL HUMAN; SCHOOL CHILD; STEM CELL EXPANSION; TELOMERE; THERAPY EFFECT; TISSUE REPAIR; CHEMISTRY; CYTOLOGY; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; METABOLISM; MIDDLE AGED; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; STEM CELL;

CAPRA HIRCUS;

ADOLESCENT; ADULT; BASE SEQUENCE; CARTILAGE, ARTICULAR; CELL DIFFERENTIATION; CELL LINE; CHILD; DNA PRIMERS; FIBRONECTINS; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; MIDDLE AGED; POLYMERASE CHAIN REACTION; STEM CELLS; TELOMERASE; TELOMERE;

EID: 78149418660     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013246     Document Type: Article

References (63)

1. Khan IM, Redman SN, Williams R, Dowthwaite GP, Oldfield SF, et al. (2007) The development of synovial joints. Curr Top Dev Biol 79: 1-36.
2. Cournil-Henrionnet C, Huselstein C, Wang Y, Galois L, Mainard D, et al. (2008) Phenotypic analysis of cell surface markers and gene expression of human mesenchymal stem cells and chondrocytes during monolayer expansion. Biorheology 45: 513-526.
3. Schnabel M, Marlovits S, Eckhoff G, Fichtel I, Gotzen L, et al. (2002) Dedifferentiation-associated changes inmorphology and gene expression in primary human articular chondrocytes in cell culture. Osteoarthritis Cartilage 10: 62-70.
4. Dell'Accio F, De Bari C, Luyten FP (2001) Molecular markers predictive of the capacity of expanded human articular chondrocytes to form stable cartilage in vivo. Arthritis Rheum 44: 1608-1619.
5. Benya PD, Shaffer JD (1982) Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 30: 215-224.
6. Jakob M, Demarteau O, Schafer D, Hintermann B, Dick W, et al. (2001) Specific growth factors during the expansion and redifferentiation of adult human articular chondrocytes enhance chondrogenesis and cartilaginous tissue formation in vitro. J Cell Biochem 81: 368-377.
7. Li Y, Tew SR, Russell AM, Gonzalez KR, Hardingham TE, et al. (2004) Transduction of passaged human articular chondrocytes with adenoviral, retroviral, and lentiviral vectors and the effects of enhanced expression of SOX9. Tissue Eng 10: 575-584.
8. Wolf F, Candrian C, Wendt D, Farhadi J, Heberer M, et al. (2008) Cartilage tissue engineering using pre-aggregated human articular chondrocytes. Eur Cell Mater 16: 92-99.
9. Peterson L, Minas T, Brittberg M, Nilsson A, Sjogren-Jansson E, et al. (2000) Two- to 9-year outcome after autologous chondrocyte transplantation of the knee. Clin Orthop Relat Res. pp 212-234.
10. Tuli R, Li WJ, Tuan RS (2003) Current state of cartilage tissue engineering. Arthritis Res Ther 5: 235-238.
11. Roberts S, McCall IW, Darby AJ, Menage J, Evans H, et al. (2003) Autologous chondrocyte implantation for cartilage repair: monitoring its success by magnetic resonance imaging and histology. Arthritis Res Ther 5: R60-73.
12. Chamberlain G, Fox J, Ashton B, Middleton J (2007) Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25: 2739-2749.
13. Yang X, Zhang W, van den Dolder J, Walboomers XF, Bian Z, et al. (2007) Multilineage potential of STRO-1+ rat dental pulp cells in vitro. J Tissue Eng Regen Med 1: 128-135.
14. Lee RH, Kim B, Choi I, Kim H, Choi HS, et al. (2004) Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol Biochem 14: 311-324.
15. Waddington RJ, Youde SJ, Lee CP, Sloan AJ (2009) Isolation of distinct progenitor stem cell populations from dental pulp. Cells Tissues Organs 189: 268-274.
16. Mareddy S, Crawford R, Brooke G, Xiao Y (2007) Clonal isolation and characterization of bone marrow stromal cells from patients with osteoarthritis. Tissue Eng 13: 819-829.
17. Montesinos JJ, Flores-Figueroa E, Castillo-Medina S, Flores-Guzman P, Hernandez-Estevez E, et al. (2009) Human mesenchymal stromal cells from adult and neonatal sources: comparative analysis of their morphology, immunophenotype, differentiation patterns and neural protein expression. Cytotherapy 11: 163-176.
18. Vidal MA, Robinson SO, Lopez MJ, Paulsen DB, Borkhsenious O, et al. (2008) Comparison of chondrogenic potential in equine mesenchymal stromal cells derived from adipose tissue and bone marrow. Vet Surg 37: 713-724.
19. Rada T, Reis RL, Gomes ME (2009) Adipose Tissue-Derived Stem Cells and Their Application in Bone and Cartilage Tissue Engineering. Tissue Eng Part B Rev.
20. Seda Tigli R, Ghosh S, Laha MM, Shevde NK, Daheron L, et al. (2009) Comparative chondrogenesis of human cell sources in 3D scaffolds. J Tissue Eng Regen Med.
21. Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU (1998) In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 238: 265-272.
22. Murdoch AD, Grady LM, Ablett MP, Katopodi T, Meadows RS, et al. (2007) Chondrogenic differentiation of human bone marrow stem cells in transwell cultures: generation of scaffold-free cartilage. Stem Cells 25: 2786-2796.
23. Connelly JT, Wilson CG, Levenston ME (2008) Characterization of proteoglycan production and processing by chondrocytes and BMSCs in tissue engineered constructs. Osteoarthritis Cartilage 16: 1092-1100.
24. Hayes AJ, MacPherson S, Morrison H, Dowthwaite G, Archer CW (2001) The development of articular cartilage: evidence for an appositional growth mechanism. Anat Embryol (Berl) 203: 469-479.
25. Dowthwaite GP, Bishop JC, Redman SN, Khan IM, Rooney P, et al. (2004) The surface of articular cartilage contains a progenitor cell population. J Cell Sci 117: 889-897.
26. Khan IM, Bishop JC, Gilbert S, Archer CW (2009) Clonal chondroprogenitors maintain telomerase activity and Sox9 expression during extended monolayer culture and retain chondrogenic potential. Osteoarthritis Cartilage 17: 518-528.
27. Grogan SP, Barbero A, Diaz-Romero J, Cleton-Jansen AM, Soeder S, et al. (2007) Identification of markers to characterize and sort human articular chondrocytes with enhanced in vitro chondrogenic capacity. Arthritis Rheum 56: 586-595.
28. Hiraoka K, Grogan S, Olee T, Lotz M (2006) Mesenchymal progenitor cells in adult human articular cartilage. Biorheology 43: 447-454.
29. Alsalameh S, Amin R, Gemba T, Lotz M (2004) Identification of mesenchymal progenitor cells in normal and osteoarthritic human articular cartilage. Arthritis Rheum 50: 1522-1532.
30. de la Fuente R, Abad JL, Garcia-Castro J, Fernandez-Miguel G, Petriz J, et al. (2004) Dedifferentiated adult articular chondrocytes: a population of human multipotent primitive cells. Exp Cell Res 297: 313-328.
31. Diaz-Romero J, Nesic D, Grogan S, Heini P, Mainil-Varlet P (2008) Immunophenotypic changes of human articular chondrocytes during monolayer culture reflect bona fide dedifferentiation rather than amplification of progenitor cells. Journal of Cellular Physiology 214: 75-83.
32. Karlsson C, Stenhamre H, Sandstedt J, Lindahl A (2008) Neither Notch1 expression nor cellular size correlate with mesenchymal stem cell properties of adult articular chondrocytes. Cells Tissues Organs 4: 275-285.
33. Jones PH, Watt FM (1993) Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression. Cell 73: 713-724.
34. Cristofalo VJ, Allen RG, Pignolo RJ, Martin BG, Beck JC (1998) Relationship between donor age and the replicative lifespan of human cells in culture: a reevaluation. Proc Natl Acad Sci U S A 95: 10614-10619.
35. Barbero A, Grogan S, Schafer D, Heberer M, Mainil-Varlet P, et al. (2004) Age related changes in human articular chondrocyte yield, proliferation and postexpansion chondrogenic capacity. Osteoarthritis Cartilage 12: 476-484.
36. Yang R, Davies CM, Archer CW, Richards RG (2003) Immunohistochemistry of matrix markers in Technovit 9100 New-embedded undecalcified bone sections. Eur Cell Mater 6: 57-71; discussion 71.
37. Singhrao S, Müller C, Gilbert S, Duance V, Archer C (2009) An immunofluorescence method for post-embedded tissue in acrylic resin Technovit 9100 New® using fluorescein isothiocyanate secondary detection marker. Microsc Res Tech Online; ahead of press.
38. Boyle T, Griffin D (2001) The cytogenetics of pregnancy. In: Rooney D, ed. Human Cytogenetics:constitutional analysis. 3rd ed:. Oxford: Oxford University Press. pp 55-98.
39. Shaffer L, Tommerup N (2005) An International System fro Human Cytogenetic Nomenclature. In: Karger S, ed. Basel.
40. Seabright M (1972) The use of proteolytic enzymes for the mapping of structural rearrangements in the chromosomes of man. Chromosoma 36: 204-210.
41. Capper R, Britt-Compton B, Tankimanova M, Rowson J, Letsolo B, et al. (2007) The nature of telomere fusion and a definition of the critical telomere length in human cells. Genes Dev 21: 2495-2508.
42. Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphology 88: 49-92.
43. Kuznetsov SA, Krebsbach PH, Satomura K, Kerr J, Riminucci M, et al. (1997) Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J Bone Miner Res 12: 1335-1347.
44. Craig FM, Bentley G, Archer CW (1987) The spatial and temporal pattern of collagens I and II and keratan sulphate in the developing chick metatarsophalangeal joint. Development 99: 383-391.
45. Brittberg M, Peterson L (1998) Introduction of an articular cartilage classification. ICRS Newsletter 1.
46. Grogan SP, Miyaki S, Asahara H, D'Lima DD, Lotz MK (2009) Mesenchymal progenitor cell markers in human articular cartilage: normal distribution and changes in osteoarthritis. Arthritis Res Ther 11: R85.
47. Diaz-Romero J, Nesic D, Grogan SP, Heini P, Mainil-Varlet P (2008) Immunophenotypic changes of human articular chondrocytes during monolayer culture reflect bona fide dedifferentiation rather than amplification of progenitor cells. J Cell Physiol 214: 75-83.
48. Diaz-Romero J, Gaillard JP, Grogan SP, Nesic D, Trub T, et al. (2005) Immunophenotypic analysis of human articular chondrocytes: changes in surface markers associated with cell expansion in monolayer culture. J Cell Physiol 202: 731-742.
49. Kolettas E, Buluwela L, Bayliss MT, Muir HI (1995) Expression of cartilagespecific molecules is retained on long-term culture of human articular chondrocytes. J Cell Sci 108(Pt 5): 1991-1999.
50. Glowacki J, Trepman E, Folkman J (1983) Cell shape and phenotypic expression in chondrocytes. Proc Soc Exp Biol Med 172: 93-98.
51. von der Mark K, Gauss V, von der Mark H, Muller P (1977) Relationship between cell shape and type of collagen synthesised as chondrocytes lose their cartilage phenotype in culture. Nature 267: 531-532.
52. Watt FM, Dudhia J (1988) Prolonged expression of differentiated phenotype by chondrocytes cultured at low density on a composite substrate of collagen and agarose that restricts cell spreading. Differentiation 38: 140-147.
53. Archer CW, Rooney P, Wolpert L (1982) Cell shape and cartilage differentiation of early chick limb bud cells in culture. Cell Differ 11: 245-251.
54. Martin JA, Mitchell CJ, Klingelhutz AJ, Buckwalter JA (2002) Effects of telomerase and viral oncogene expression on the in vitro growth of human chondrocytes. J Gerontol A Biol Sci Med Sci 57: B48-53.
55. Blackburn EH (1991) Structure and function of telomeres. Nature 350: 569-573.
56. Martin JA, Buckwalter JA (2001) Telomere erosion and senescence in human articular cartilage chondrocytes. J Gerontol A Biol Sci Med Sci 56: B172-179.
57. Allen ND, Baird DM (2009) Telomere length maintenance in stem cell populations. Biochim Biophys Acta 1792: 324-328.
58. Archer CW, Morrison H, Pitsillides AA (1994) Cellular aspects of the development of diarthrodial joints and articular cartilage. J Anat 184(Pt 3): 447-456.
59. Ichinose S, Tagami M, Muneta T, Sekiya I (2005) Morphological examination during in vitro cartilage formation by human mesenchymal stem cells. Cell Tissue Res 322: 217-226.
60. Pelttari K, Winter A, Steck E, Goetzke K, Hennig T, et al. (2006) Premature induction of hypertrophy during in vitro chondrogenesis of human mesenchymal stem cells correlates with calcification and vascular invasion after ectopic transplantation in SCID mice. Arthritis Rheum 54: 3254-3266.
61. Koelling S, Kruegel J, Irmer M, Path JR, Sadowski B, et al. (2009) Migratory chondrogenic progenitor cells from repair tissue during the later stages of human osteoarthritis. Cell Stem Cell 4: 324-335.
62. Rooney G, McMahon S, Ritter T, Garcia Y, Moran CJ, et al. (2009) Neurotrophic Factor-Expressing Mesenchymal Stem Cells Survive Transplantation into the Contused Spinal Cord without Differentiating into Neural Cells. Tissue Eng Part A Mar 31, Epub ahead of print.
63. Tuan RS (2007) A second-generation autologous chondrocyte implantation approach to the treatment of focal articular cartilage defects. Arthritis Res Ther 9: 109.