Promotion of embryonic chick limb cartilage differentiation by transforming growth factor-β

Kulyk, William M.; Rodgers, Barbara J.; Greer, Karen L.; Kosher, Robert A.

doi:10.1016/0012-1606(89)90191-7

Cited by 160 publications

(103 citation statements)

References 27 publications

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“…Since seemingly parallel increases in the number of cells expressing TGF-p and collagen type I1 are observed, it may be speculated that the additional cells expressing TGF-P in fact correspond to those eventually expressing type I1 collagen, i.e., chondroprogenitor cells. A similar observation has been made in the embryonic limb bud, where the central condensing core of mesenchymal cells indeed express higher levels of TGF-(3 and later form the cartilage anlage (Kulyk et al, 1989). The mechanisms by which TGF-p influences cellular proliferation and differentiation are currently not completely understood, and are being actively studied by a large number of investigators (see review by Massague, 1990;Sporn and Roberts, 1990).…”

Section: Discussionsupporting

confidence: 57%

Effect of systemic calcium deficiency on the expression of transforming growth factor‐β in chick embryonic calvaria

Sato

Tuan

1992

Developmental Dynamics

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The developmental process of intramembranous ossification involves bone formation directly from mesenchymal differentiation without a cartilage intermediate. We have previously observed that systemic calcium deficiency in the developing chick embryo, produced by long-term shell-less culture, results in the appearance of chondrocyte-like cells in the calvarium, a parietal bone which normally develops via intramembranous ossification. This investigation aims to analyze the mechanism underlying this calcium deficiency-related, aberrant appearance of cartilage phenotype in the chick embryonic calvarium. In view of the reported involvement of transforming growth factor p (TGF-P) in osteogenesis and chondrogenesis, we have examined and compared here the expression of TGF-p in the chick embryonic calvaria of normal (in ovo development, NL), shell-less (SL), and calcium-supplemented SL (SL + Ca) embryos. TGF-f3 expression was analyzed at the mRNA level by blot and in situ cDNA hybridization, and at the protein level by immunohistochemistry and immunoblotting. The results presented here indicate that: 1) TGF-p is expressed in the chick embryonic calvarium by both periosteal cells and osteocytes, as revealed by in situ hybridization and immunohistochemistry; 2) TGF-P expression is significantly increased in SL calvarium compared to NL calvarium, at both protein and mRNA levels; 3) the number of TGF-f3 expressing cells increases in the SL calvarium, particularly along the central, subcambial core region of the bone; and 4) exogenous calcium repletion to the SL embryo affects the expression of TGF-P such that the pattern approaches that in the NL embryo. Taken together, these results indicate that altered TGF-f3 expression accompanies the aberrant appearance of cartilage phenotype caused by systemic calcium deficiency. We postulate that normal cellular differentiation along the osteogenic pathway during embryonic intramembranous ossification is crucially dependent on regulated TGF-0 expression. o 1992 Wiley-Liss, Inc.

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Section: Discussionsupporting

confidence: 57%

Effect of systemic calcium deficiency on the expression of transforming growth factor‐β in chick embryonic calvaria

Sato

Tuan

1992

Developmental Dynamics

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“…Kulyk et al (1989a) previously reported that TGF-P1 and TGF-P2 stimulate the accumulation of cartilage matrix and sulfated glycosaminoglycans by high density micromass cultures of chick limb mesenchymal cells, and also elicit a striking increase in the steadystate cytoplasmic levels of mRNAs for cartilage-characteristic type I1 collagen and aggrecan (cartilagecharacteristic sulfated proteoglycan). Furthermore, both these isoforms of TGF-(3 promote chondrogenic differentiation and cartilage-specific gene expression in low density subconfluent spot cultures of limb mesenchymal cells, which are situations in which little, or no cartilage differentiation normally occurs (Kulyk et al, 1989a). Brief exposure to these growth factors a t the initiation of culture was found to be sufficient to stimulate chondrogenesis, suggesting that TGF-P may be involved in regulating the onset of the differentiation of chick limb mesenchymal cells into chondrocytes (Kulyk et al, 1989a).…”

Section: Introductionmentioning

confidence: 97%

“…Both TGF-p1 and TGF-p2 stimulate fibroblastic, mesenchymal-like cells isolated from fetal rat muscle explants to synthesize matrix proteins characteristic of cartilage (Seyedin et al, 1985(Seyedin et al, , 1986(Seyedin et al, , 1987 and both these factors can elicit localized chondrogenesis when injected subperiosteally (Joyce et al, 1990). TGF-p1 and TGF-P2 are potent promoters of the chondrogenic differentiation of embryonic limb mesenchymal cells in vitro (Kulyk et al, 1989a;Carrington and Reddi, 1990;Schofield and Wolpert, 1990;Leonard et al, 1991) as are BMP-3 , BMP-4 (Chen et al, 1991), activin (Jiang et a]., 1993), and inhibin (Chen et al, 1993). Interestingly, while BMPs are structurally related to the TGF-Ps, one significant difference is that TGF-ps are not capable of inducing cartilage formation in vivo when explanted ectopically, as BMPs have been shown to do (Sampath et al, 1987;Wozney et al, 1988;Luyten et al, 1989;Rosen et al, 1989;Wang et al, 1990;Celeste et al, 1990).…”

Section: Introductionmentioning

confidence: 99%

“…Interestingly, while BMPs are structurally related to the TGF-Ps, one significant difference is that TGF-ps are not capable of inducing cartilage formation in vivo when explanted ectopically, as BMPs have been shown to do (Sampath et al, 1987;Wozney et al, 1988;Luyten et al, 1989;Rosen et al, 1989;Wang et al, 1990;Celeste et al, 1990). Kulyk et al (1989a) previously reported that TGF-P1 and TGF-P2 stimulate the accumulation of cartilage matrix and sulfated glycosaminoglycans by high density micromass cultures of chick limb mesenchymal cells, and also elicit a striking increase in the steadystate cytoplasmic levels of mRNAs for cartilage-characteristic type I1 collagen and aggrecan (cartilagecharacteristic sulfated proteoglycan). Furthermore, both these isoforms of TGF-(3 promote chondrogenic differentiation and cartilage-specific gene expression in low density subconfluent spot cultures of limb mesenchymal cells, which are situations in which little, or no cartilage differentiation normally occurs (Kulyk et al, 1989a).…”

Section: Introductionmentioning

confidence: 99%

“…Furthermore, both these isoforms of TGF-(3 promote chondrogenic differentiation and cartilage-specific gene expression in low density subconfluent spot cultures of limb mesenchymal cells, which are situations in which little, or no cartilage differentiation normally occurs (Kulyk et al, 1989a). Brief exposure to these growth factors a t the initiation of culture was found to be sufficient to stimulate chondrogenesis, suggesting that TGF-P may be involved in regulating the onset of the differentiation of chick limb mesenchymal cells into chondrocytes (Kulyk et al, 1989a).…”

Section: Introductionmentioning

confidence: 99%

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Transforming growth factor‐β and bone morphogenetic protein‐2 act by distinct mechanisms to promote chick limb cartilage differentiation in vitro

Roark

Greer

1994

Developmental Dynamics

Self Cite

129

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A number of studies suggest that several members of the transforming growth factor‐β (TGF‐β) family of peptide growth factors may be involved in the regulation of cartilage differentiation. It has been previously reported that TGF‐β1 and TGF‐β2 promote the chondrogenic differentiation of chick limb mesenchymal cells in high density micromass cultures (Kulyk et al. [1989a] Dev. Biol. 135:424–430). In this study we report that chick limb mesenchymal cells express mRNA for chicken TGF‐β1, TGF‐β2, and TGF‐β3 during cartilage differentiation in vitro. In addition, the time course of their expression during cartilage differentiation is consistent with their playing a role in the initiation of this differentiation process. We also report that two members of the TGF‐β family, TGF‐β3 and bone morphogenetic protein‐2 (BMP‐2), are capable of promoting the accumulation of cartilage extracellular matrix molecules by differentiating chick limb mesenchymal cells in micromass culture. Significant differences, however, were noted between the specific effects on matrix production elicited by these two growth factors which suggest that they may be acting by distinct mechanisms to regulate cartilage matrix production. TGF‐β appears to be most effective on cells which have not yet undergone cell condensation, a critical event in early cartilage differentiation, wherease BMP‐2 is most effective after cells have condensed or differentiated. These observations suggest that TGF‐β3 and BMP‐2 may be acting in a sequential manner to regulate chick limb mesenchymal cells through the different stages of cartilage differentiation. © 1994 Wiley‐Liss, Inc.

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Treatment with all-trans-retinoic acid decreases levels of endogenous TGF-?1 in the mesenchyme of the developing mouse inner ear

Frenz

Liu

2000

Teratology

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Promotion of embryonic chick limb cartilage differentiation by transforming growth factor-β

Cited by 160 publications

References 27 publications

Effect of systemic calcium deficiency on the expression of transforming growth factor‐β in chick embryonic calvaria

Effect of systemic calcium deficiency on the expression of transforming growth factor‐β in chick embryonic calvaria

Transforming growth factor‐β and bone morphogenetic protein‐2 act by distinct mechanisms to promote chick limb cartilage differentiation in vitro

Treatment with all-trans-retinoic acid decreases levels of endogenous TGF-?1 in the mesenchyme of the developing mouse inner ear

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