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Chondrogenesis in the regenerating antler tip in red deer: Expression of collagen types I, IIA, IIB, and X demonstrated by in situ nucleic acid hybridization and immunocytochemistry
Author(s) -
Price Joanna S.,
Oyajobi Babatunde O.,
Nalin Andrew M.,
Frazer Astrid,
Russell R. Graham G.,
Sandell Linda J.
Publication year - 1996
Publication title -
developmental dynamics
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.634
H-Index - 141
eISSN - 1097-0177
pISSN - 1058-8388
DOI - 10.1002/(sici)1097-0177(199603)205:3<332::aid-aja12>3.0.co;2-6
Subject(s) - perichondrium , in situ hybridization , biology , chondrogenesis , endochondral ossification , cartilage , procollagen peptidase , population , immunocytochemistry , microbiology and biotechnology , anatomy , mesenchyme , messenger rna , mesenchymal stem cell , endocrinology , genetics , demography , sociology , gene
The annual regrowth of antlers in male deer is a unique example of complete boneregeneration occurring in an adult animal. Growth is initiated at the distal antler tip, which issimilar to the epiphyseal growth plate in some respects. However, there is some debate as towhether this process represents “true” endochondral ossification. As part of the characterizationof 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, typeI procollagen mRNA was observed in skin, the fibrous perichondrium, and the densely cellulararea immediately adjacent to the perichondrium. Below this area, as cells began to assume acolumnar arrangement and coincident with the appearance of a vasculature and synthesis of acartilaginous 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 wasaltered. 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. Thealternative splice form of type II procollagen mRNA (IIA), characteristic of chondroprogenitorcells (Sandell et al. [1991] J. Cell Biol. 114:1307‐1319), was expressed by a subset of cells inthe upper region of the columns, indicating that this zone contains a population ofprechondrocytic cells. Positive hybridization to type IIA was most abundant in these cells. Incontrast, transcripts for the other procollagen splice form (IIB) and type X collagen wereexpressed by chondrocytes throughout the whole of the cartilage region studied. The translationand export of type II collagen and type X collagen were confirmed by detecting specificimmunoreactivity for each. The spatial distribution of immunoreactivity for collagen types II andX was consistent with that of corresponding mRNAs. These data demonstrate for the first timethe distinct pattern of expression of genes for major cartilage matrix macromolecules, theexpression of the differentially spliced form of type II procollagen mRNA (IIA), and specificallythe colocalization of types II and X collagen in the developing antler tip. Taken together, theystrongly indicate that antler growth involves an endochondral process. © 1996 Wiley‐Liss,Inc.