TY - JOUR
T1 - Chondrogenesis in the regenerating antler tip in red deer
T2 - Expression of collagen types I, IIA, IIB, and X demonstrated by in situ nucleic acid hybridization and immunocytochemistry
AU - Price, Joanna S.
AU - Oyajobi, Babatunde O.
AU - Nalin, Andrew M.
AU - Frazer, Astrid
AU - Russell, R. Graham G.
AU - Sandell, Linda J.
PY - 1996/3
Y1 - 1996/3
N2 - The annual regrowth of antlers in male deer is a unique example of complete bone regeneration occurring in an adult animal. Growth is initiated at the distal antler tip, which is similar to the epiphyseal growth plate in some respects. However, there is some debate as to whether this process represents 'true' endochondral ossification. As part of the characterization of the developmental process in pre-osseus antler tissue, we have studied, by in situ hybridization, the spatial expression of mRNAs for types I, II, and X collagen. Viewed in a coronal plane, type I procollagen mRNA was observed in skin, the fibrous perichondrium, and the densely cellular area immediately adjacent to the perichondrium. Below this area, as cells began to assume a columnar arrangement and coincident with the appearance of a vasculature and synthesis of a cartilaginous matrix, transcripts for types I, IIA, IIB procollagen and X collagen were detected. Further down in the cartilage zone, the pattern of type I procollagen mRNA expression was altered. Here, the signal was detected only in a morphologically distinct subpopulation of small, flattened cells within the intercellular matrix at the periphery of the columns of chondrocytes. The alternative splice form of type II procollagen mRNA (IIA), characteristic of chondroprogenitor cells (Sandell et al. [1991] J. Cell Biol. 114:1307-1319), was expressed by a subset of cells in the upper region of the columns, indicating that this zone contains a population of prechondrocytic cells. Positive hybridization to type IIA was most abundant in these cells. In contrast, transcripts for the other procollagen splice form (IIB) and type X collagen were expressed by chondrocytes throughout the whole of the cartilage region studied. The translation and export of type II collagen and type X collagen were confirmed by detecting specific immunoreactivity for each. The spatial distribution of immunoreactivity for collagen types II and X was consistent with that of corresponding mRNAs. These data demonstrate for the first time the distinct pattern of expression of genes for major cartilage matrix macromolecules, the expression of the differentially spliced form of type II procollagen mRNA (IIA), and specifically the colocalization of types II and X collagen in the developing antler tip. Taken together, they strongly indicate that antler growth involves an endochondral process.
AB - The annual regrowth of antlers in male deer is a unique example of complete bone regeneration occurring in an adult animal. Growth is initiated at the distal antler tip, which is similar to the epiphyseal growth plate in some respects. However, there is some debate as to whether this process represents 'true' endochondral ossification. As part of the characterization of the developmental process in pre-osseus antler tissue, we have studied, by in situ hybridization, the spatial expression of mRNAs for types I, II, and X collagen. Viewed in a coronal plane, type I procollagen mRNA was observed in skin, the fibrous perichondrium, and the densely cellular area immediately adjacent to the perichondrium. Below this area, as cells began to assume a columnar arrangement and coincident with the appearance of a vasculature and synthesis of a cartilaginous matrix, transcripts for types I, IIA, IIB procollagen and X collagen were detected. Further down in the cartilage zone, the pattern of type I procollagen mRNA expression was altered. Here, the signal was detected only in a morphologically distinct subpopulation of small, flattened cells within the intercellular matrix at the periphery of the columns of chondrocytes. The alternative splice form of type II procollagen mRNA (IIA), characteristic of chondroprogenitor cells (Sandell et al. [1991] J. Cell Biol. 114:1307-1319), was expressed by a subset of cells in the upper region of the columns, indicating that this zone contains a population of prechondrocytic cells. Positive hybridization to type IIA was most abundant in these cells. In contrast, transcripts for the other procollagen splice form (IIB) and type X collagen were expressed by chondrocytes throughout the whole of the cartilage region studied. The translation and export of type II collagen and type X collagen were confirmed by detecting specific immunoreactivity for each. The spatial distribution of immunoreactivity for collagen types II and X was consistent with that of corresponding mRNAs. These data demonstrate for the first time the distinct pattern of expression of genes for major cartilage matrix macromolecules, the expression of the differentially spliced form of type II procollagen mRNA (IIA), and specifically the colocalization of types II and X collagen in the developing antler tip. Taken together, they strongly indicate that antler growth involves an endochondral process.
KW - Chondrogenesis
KW - Deer antler tip
KW - Type I collagen
KW - Type X collagen
KW - Types IIA and IIB collagen
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U2 - 10.1002/(SICI)1097-0177(199603)205:3<332::AID-AJA12>3.0.CO;2-6
DO - 10.1002/(SICI)1097-0177(199603)205:3<332::AID-AJA12>3.0.CO;2-6
M3 - Article
C2 - 8850568
AN - SCOPUS:0029981207
SN - 1058-8388
VL - 205
SP - 332
EP - 347
JO - Developmental Dynamics
JF - Developmental Dynamics
IS - 3
ER -