Ossification of the mouse metatarsal: Differentiation and proliferation in the presence/absence of a defined growth plate
Anatomy & Morphology; bone growth; cartilage fixation; cell-proliferation; chick limb buds; chondrocyte; chondrocyte proliferation; differential growth; endochondral ossification; epiphysis; evolution; hedgehog; hypertrophic differentiation; matrix proteoglycans; rat; skeletal formation
There is significant diversity in growth plate behavior among sites within an individual skeleton and between skeletons of different species. This variation within wild-type animals is an underutilized resource for studying skeletal development. One bone that potentially exhibits the most diverse behavior is the metatarsal. While one end forms a growth plate with an epiphyseal secondary center of ossification as in other long bones, the opposite end undergoes direct ossification in a manner more similar to short bones. Although descriptions of human metatarsal/metacarpal ossification are available, a detailed comparative analysis has yet to be conducted in an animal model amenable to biomolecular analysis. Here we report an analysis of proximal and distal ossification in an age series of mouse metatarsals. Safranin 0 staining was used for qualitative and quantitative histology, and chondrocyte differentiation and proliferation were analyzed using immunohistochemistry for type X collagen and proliferative cell nuclear antigen expression. We establish that, as in the human, both growth plate formation and direct ossification occur in the mouse metatarsal, with chondrocyte populations showing distinct differentiation patterns at opposite ends of the bone. In addition, growth plate formation is characterized by a peak of proliferation in reserve zone chondrocytes that distinguishes it from both established growth plates and direct ossification. Our analysis demonstrates that the mouse metatarsal is a productive model for investigating natural variation in ossification that can further understanding of vertebrate skeletal development and evolution. (C) 2005 Wiley-Liss, Inc.
Reno P L; McBurney D L; Lovejoy C O; Horton W E
Anatomical Record Part a-Discoveries in Molecular Cellular and Evolutionary Biology
2006
2006-01
Journal Article
<a href="http://doi.org/10.1002/ar.a.20268" target="_blank" rel="noreferrer noopener">10.1002/ar.a.20268</a>
Temperature regulates limb length in homeotherms by directly modulating cartilage growth
Allen's Rule; blood-flow; body size; bone; bone growth; bone tissue culture; cartilage biology; differentiation; endoplasmic-reticulum stress; environmental-temperature; fluorescent microsphere method; mouse; plate; proliferation; Science & Technology - Other Topics; tail-length; thermoregulation
Allen's Rule documents a century-old biological observation that strong positive correlations exist among latitude, ambient temperature, and limb length in mammals. Although genetic selection for thermoregulatory adaptation is frequently presumed to be the primary basis of this phenomenon, important but frequently overlooked research has shown that appendage outgrowth is also markedly influenced by environmental temperature. Alteration of limb blood flow via vasoconstriction/vasodilation is the current default hypothesis for this growth plasticity, but here we show that tissue perfusion does not fully account for differences in extremity elongation in mice. We show that peripheral tissue temperature closely reflects housing temperature in vivo, and we demonstrate that chondrocyte proliferation and extracellular matrix volume strongly correlate with tissue temperature in metatarsals cultured without vasculature in vitro. Taken together, these data suggest that vasomotor changes likely modulate extremity growth indirectly, via their effects on appendage temperature, rather than vascular nutrient delivery. When combined with classic evolutionary theory, especially genetic assimilation, these results provide a potentially comprehensive explanation of Allen's Rule, and may substantially impact our understanding of phenotypic variation in living and extinct mammals, including humans.
Serrat M A; King D; Lovejoy C O
Proceedings of the National Academy of Sciences of the United States of America
2008
2008-12
Journal Article
<a href="http://doi.org/10.1073/pnas.0803319105" target="_blank" rel="noreferrer noopener">10.1073/pnas.0803319105</a>
Long bone histomorphogenesis of the naked mole‐rat: Histodiversity and intraspecific variation.
ONTOGENY; bone microstructure; bone modeling; endosteal bone; Heterocephalus glaber; lamellar bone; long bone growth; BONE growth; BODY temperature; HYPOTHERMIA; lamellar‐zonal bone; MORPHOGENESIS; NAKED mole rat; PERIOSTEUM; POLARIZATION microscopy; STRAINS & stresses (Mechanics)
Lacking fur, living in eusocial colonies and having the longest lifespan of any rodent, makes naked mole‐rats (NMRs) rather peculiar mammals. Although they exhibit a high degree of polymorphism, skeletal plasticity and are considered a novel model to assess the effects of delayed puberty on the skeletal system, scarce information on their morphogenesis exists. Here, we examined a large ontogenetic sample (n = 76) of subordinate individuals to assess the pattern of bone growth and bone microstructure of fore‐ and hindlimb bones by using histomorphological techniques. Over 290 undecalcified thin cross‐sections from the midshaft of the humerus, ulna, femur, and tibia from pups, juveniles and adults were analyzed with polarized light microscopy. Similar to other fossorial mammals, NMRs exhibited a systematic cortical thickening of their long bones, which clearly indicates a conserved functional adaptation to withstand the mechanical strains imposed during digging, regardless of their chisel‐tooth predominance. We describe a high histodiversity of bone matrices and the formation of secondary osteons in NMRs. The bones of pups are extremely thin‐walled and grow by periosteal bone formation coupled with considerable expansion of the medullary cavity, a process probably tightly regulated and adapted to optimize the amount of minerals destined for skeletal development, to thus allow the female breeder to produce a higher number of pups, as well as several litters. Subsequent cortical thickening in juveniles involves high amounts of endosteal bone apposition, which contrasts with the bone modeling of other mammals where a periosteal predominance exists. Adults have bone matrices predominantly consisting of parallel‐fibered bone and lamellar bone, which indicate intermediate to slow rates of osteogenesis, as well as the development of poorly vascularized lamellar‐zonal tissues separated by lines of arrested growth (LAGs) and annuli. These features reflect the low metabolism, low body temperature and slow growth rates reported for this species, as well as indicate a cyclical pattern of osteogenesis. The presence of LAGs in captive individuals was striking and indicates that postnatal osteogenesis and its consequent cortical stratification most likely represents a plesiomorphic thermometabolic strategy among endotherms which has been suggested to be regulated by endogenous rhythms. However, the generalized presence of LAGs in this and other subterranean taxa in the wild, as well as recent investigations on variability of environmental conditions in burrow systems, supports the hypothesis that underground environments experience seasonal fluctuations that may influence the postnatal osteogenesis of animals by limiting the extension of burrow systems during the unfavorable dry seasons and therefore the finding of food resources. Additionally, the intraspecific variation found in the formation of bone tissue matrices and vascularization suggested a high degree of developmental plasticity in NMRs, which may help explaining the polymorphism reported for this species. The results obtained here represent a valuable contribution to understanding the relationship of several aspects involved in the morphogenesis of the skeletal system of a mammal with extraordinary adaptations. [ABSTRACT FROM AUTHOR]
Montoya‐Sanhueza G; Bennett NC; Oosthuizen MK; Dengler‐Crish CM; Chinsamy A
Journal Of Anatomy
2021
2021-06
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journalArticle
<a href="http://doi.org/10.1111/joa.13381" target="_blank" rel="noreferrer noopener">10.1111/joa.13381</a>