Effects of TGF-β1 and Triiodothyronine on cartilage maturation: In vitro analysis using long-term high-density micromass cultures of chick embryonic limb mesenchymal cells

Journal of Orthopaedic Research

Volumn 24, Issue 11, 2006, Pages 2095-2105

  Mello, Maria A ^a   Tuan, Rocky S ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Apoptosis; Collagen type X; Hypertrophy

Indexed keywords

ALKALINE PHOSPHATASE; COLLAGEN TYPE 10; COLLAGEN TYPE 2; DNA FRAGMENT; LIOTHYRONINE; THYROID HORMONE RECEPTOR ALPHA; THYROID HORMONE RECEPTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; TRANSFORMING GROWTH FACTOR BETA1; BIOLOGICAL MARKER; MESSENGER RNA;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIFICATION; CARTILAGE CELL; CELL CULTURE; CELL DENSITY; CELL MATURATION; CELL PROLIFERATION; CELL SIZE; CELL STIMULATION; CHICK EMBRYO; CHONDROGENESIS; CONTROLLED STUDY; EMBRYO; ENCHONDRAL OSSIFICATION; ENZYME ACTIVITY; GENE EXPRESSION; HYPERTROPHY; IN VITRO STUDY; MESENCHYME CELL; MITOSIS INHIBITION; NICK END LABELING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; ANIMAL; BONE MINERALIZATION; CARTILAGE; CELL ENLARGEMENT; CYTOLOGY; DRUG COMBINATION; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIMB; MESODERM; METABOLISM; PRENATAL DEVELOPMENT;

ALKALINE PHOSPHATASE; ANIMALS; APOPTOSIS; BIOLOGICAL MARKERS; CALCIFICATION, PHYSIOLOGIC; CARTILAGE; CELL ENLARGEMENT; CELL PROLIFERATION; CELLS, CULTURED; CHICK EMBRYO; COLLAGEN TYPE X; DNA FRAGMENTATION; DRUG COMBINATIONS; EXTREMITIES; MESODERM; RNA, MESSENGER; TRANSFORMING GROWTH FACTOR BETA1; TRIIODOTHYRONINE;

EID: 33750876060     PISSN: 07360266     EISSN: None     Source Type: Journal    
DOI: 10.1002/jor.20233     Document Type: Article

References (42)

1. Hickok NJ, Haas AR, Tuan RS. 1998. Regulation of chondrocyte differentiation and maturation. Microsc Res Tech 43:174-190.
2. Morcuende JA, Weinstein SL. 2003. Developmental skeletal anomalies. Birth Defects Res C Embryo Today 69:197-207.
3. Ballock RT, O'Keefe RJ. 2003. The biology of the growth plate. J Bone Joint Surg [Am] 85-A:715-726.
4. Kronenberg HM. 2003. Developmentel regulation of the growth plate. Nature 423:332-336.
5. Ahrens PB, Solursh M, Reiter RS. 1977. Stage-related capacity for limb chondrogenesis in cell culture. Dev Biol 60:69-82.
6. Boskey AL, Stiner D, Doty SB, et al. 1992. Studies of mineralization in tissue culture: optimal conditions for cartilage calcification. Bone Miner 16:11-36.
7. Mello MA, Tuan RS. 1999. High density micromass cultures of embryonic limb bud mesenchymal cells: an in vitro model of endochondral skeletal development. In Vitro Cell Dev Biol Anim 35:262-269.
8. Evans RM. 1988. The steroid and thyroid hormone receptor superfamily. Science 240:889-895.
9. Forrest D, Sjoberg M, Vennstrom B. 1990. Contrasting developmental and tissue-specific expression of alpha and beta thyroid hormone receptor genes. EMBO J 9:1519-1528.
10. Alini M, Kofsky Y, Poole AR. 1995. Thyroid hormone, T3, negates the inhibitory effects of TGF-β1 on growth plate chondrocytes hypertrophy [abstract]. Orthop Trans 20:471.
11. Cummings RG. 1995. Metabolic and endocrine disorders. In: Canale ST, Beaty JH, editors. Operative pediatric orthopaedics, 2nd ed. St. Louis: Mosby. p. 383-400.
12. Benjamin B, Miller P. 1938. Hypothyroidism. as a cause of disease of the hip. Am J Dis Child 55:1189-1191.
13. Puri R, Smith CS, William AJ, et al. 1985. Slipped capital femoral epiphysis and primary juvenile hypothyroidism. J Bone Joint Surg [Br] 67:14-20.
14. Robson H, Siebler T, Stevens DA, et al. 2000. Thyroid hormone acts directly on growth plate chondrocytes to promote hypertrophic differentiation and inhibit clonal expansion and cell proliferation. Endocrinology 141:3887-3897.
15. Wells D, King JD, Roe TF, et al. 1993. Review of slipped capital femoral epiphysis associated with endocrine disease. J Pediatr Orthop 13:610-614.
16. Shi Y, Massagué J. 2003. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113:685-700.
17. Massague J. 1992. Receptors for the TGF-beta family. Cell 69:1067-1070.
18. San Antonio JD, Winston BM, Tuan RS. 1987. Regulation of chondrogenesis by heparan sulfate and structurally related glycosaminoglycans. Dev Biol 123:17-24.
19. Ballock RT, Mita BC, Zhou X, et al. 1999. Expression of thyroid hormone receptor isoforms in rat growth plate cartilage in vitro. J Bone Miner Res 14:1550-1556.
20. San Antonio JD, Tuan RS. 1986. Chondrogenesis of limb bud mesenchyme in vitro: stimulation by cations. Dev Biol 115:313-324.
21. Kiernan JA. 1990. Histological & histochemical methods. New York: Pergamon Press.
22. Lev R, Spicer S. 1964. Specific staining of sulfate groups with alcian blue at low PH. J Histochem Cytochem 12:309.
23. Stringa E; Love JM, McBride SC, et al. 1997. In vitro characterization of chondrogenic cells isolated from chick embryonic muscle using peanut agglutinin affinity chromatography. Exp Cell Res 232:287-294.
24. Daumer KM, Tufan AC, Tuan RS. 2004. Long term in vitro analysis of limb cartilage development: involvement of Wnt signaling. J Cell Biochem 93:526-541.
25. Ayache N, Bournediene K, Mathy-Hartert M, et al. 2002. Expression of TGF-betas and their receptors is differentially modulated by reactive oxygen species and nitric oxide in human articular chondrocytes. Osteoarthritis Cartilage 10:344-352.
26. Derfoul A, Calberg AL, Tuan RS, et al. 2004. Differential regulation of osteogenic marker gene expression by Wnt-3a in embryonic mesenchymal multipotential progenitor cells. Differentiation 72:209-223.
27. Breur GJ, Turgai J, Vanenkevort BA, et al. 1994. Sterological and serial section analysis of chondrocytic enlargement in the proximal tibial growth plate of the rat. Anat Rec 239:255-268.
28. Jacenko O, Tuan RS. 1986. Calcium deficiency induces expression of cartilage-like phenotype in chick embryonic calvaria. Dev Biol 115:215-232.
29. Gavrieli Y, Sherman Y, Ben-Sasson SA. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493-501.
30. Ray S, Ponnathpur V, Huang Y, et al. 1994. 1-beta-D-arabinofuranosylcytosine-, mitoxantrone- and paclitaxel- induced apoptosis in HL-60 cells: improved method for detection of internucleosomal DNA fragmentation. Cancer Chemother Pharmacol 34:365-371.
31. Reginato AM, Tuan RS, Ono T, et al. 1993. Effects of calcium deficiency on chondrocyte hypertrophy and type X collagen expression in chick embryonic sternum. Dev Dyn 198:284-329.
32. Tilly JL, Hsueh AJ. 1993. Microscale autoradiographic method for the qualitative and quantitative analysis of apoptotic DNA fragmentation. J Cell Physiol 154:519-526.
33. Ballock RT, Reddi AH. 1994. Thyroxine is the serum factor that regulates morphogenesis of columnar cartilage from isolated chondrocytes in chemically defined medium. J Cell Biol 126:1311-1318.
34. Alini M, Kofsky Y, Wu W, et al. 1996. In serum-free culture thyroid hormones ran induce full expression of chondrocyte hypertrophy leading to matrix calcification. J Bone Miner Res 11:105-113.
35. Ohlsson C, Nilsson A, Isaksson O, et al. 1992. Effects of tri-iodothyronine and insuline growth factor I (IGF-I) on alkaline phosphatase activity, [3H]thymidine incorporation and IGF-I receptor mRNA in cultured rat epiphyseal chondrocytes. J Endocrinol 135:115-123.
36. Boskey AL, Stiner D, Doty SB, et al. 1992. Requirement of vitamin C for cartilage calcification in a differentiating chick limb-bud mesenchymal cell culture. Bone 12:277-282.
37. Boskey AL, Camacho NP, Mendelshon R, et al. 1992. F-T microscopic mappings of early mineralization in chick limb bud mesenchymal cell cultures. Calcif Tissue Int 51:443-448.
38. Mansfield K, Pacci B, Adams CS, et al. 2003. Induction of apoptosis in skeletal tissues: phosphate-mediated chick chondrocyte apoptosis is calcium dependent. Calcif Tissue Int 73:161-172.
39. Hatori M, Matte KJ, Teixeira CC, et al. 1995. End labeling studies of fragmented DNA in the avian growth plate: evidence of apoptosis in terminally differentiated chondrocytes. J Bone Miner Res 10:1960-1968.
40. Stanton LA, Underhill TM, Beier F. 2003. MAP kinases in chondrocyte differentiation. Devel Biol 263: 165-175.
41. Stevens DA, Hassezjian RP, Robson H, et al. 2000. Thyroid hormones regulate hypertrophic chondrocyte differentiation and expression of parathyroid hormone-related peptide and its receptor during endochondral bone formation. J Bone Miner Res 15:2431-2442.
42. Williams GR, Robson H, Shalet SM. 1998. Thyroid hormone actions on cartilage and bone: interactions with other hormones at the epiphyseal plate and effects on linear growth. J Endocrinol 157:391-403.