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<a href="http://doi.org/10.1111/joa.13381" target="_blank" rel="noreferrer noopener">http://doi.org/10.1111/joa.13381</a>
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1469-7580 0021-8782
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Long bone histomorphogenesis of the naked mole-rat: Histodiversity and intraspecific variation.
Publisher
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Journal of Anatomy
Date
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2020
2020-12-11
Subject
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bone microstructure; bone modeling; endosteal bone; Heterocephalus glaber; lamellar bone; lamellar-zonal bone; long bone growth; lamellar‐ zonal bone
Creator
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Montoya-Sanhueza G; Bennett NC; Oosthuizen MK; Dengler-Crish CM; Chinsamy A
Description
An account of the resource
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 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.
Identifier
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<a href="http://doi.org/10.1111/joa.13381" target="_blank" rel="noreferrer noopener">10.1111/joa.13381</a>
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Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
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journalArticle
2020
Bennett NC
bone microstructure
bone modeling
Chinsamy A
Dengler-Crish CM
Department of Pharmaceutical Sciences
endosteal bone
Heterocephalus glaber
January 2021 List
Journal of anatomy
journalArticle
lamellar bone
lamellar-zonal bone
lamellar‐
long bone growth
Montoya-Sanhueza G
NEOMED College of Pharmacy
Oosthuizen MK
zonal bone
-
Text
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<a href="http://doi.org/10.1111/joa.13404" target="_blank" rel="noreferrer noopener">http://doi.org/10.1111/joa.13404</a>
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Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
ISSN
1469-7580 0021-8782
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February 2021 List
NEOMED College
NEOMED College of Medicine
NEOMED Department
Department of Pharmaceutical Sciences
Dublin Core
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Title
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Bone remodeling in the longest living rodent, the naked mole-rat: Interelement variation and the effects of reproduction.
Date
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2021
2021-02-07
Subject
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Bone resorption; Heterocephalus glaber; Female breeder; Haversian systems; Secondary osteons; Secondary reconstruction
Creator
An entity primarily responsible for making the resource
Montoya-Sanhueza G;Bennett NC;Oosthuizen MK;Dengler-Crish CM;Chinsamy A
Description
An account of the resource
The pattern of bone remodeling of one of the most peculiar mammals in the world, the naked mole-rat (NMR), was assessed. NMRs are known for their long lifespans among rodents and for having low metabolic rates. We assessed long-term in vivo bone labeling of subordinate individuals, as well as the patterns of bone resorption and bone remodeling in a large sample including reproductive and non-reproductive individuals (n = 70). Over 268 undecalcified thin cross-sections from the midshaft of humerus, ulna, femur and tibia were analyzed with confocal fluorescence and polarized light microscopy. Fluorochrome analysis revealed low osteogenesis, scarce bone resorption and infrequent formation of secondary osteons (Haversian systems) (i.e., slow bone turnover), thus most likely reflecting the low metabolic rates of this species. Secondary osteons occurred regardless of reproductive status. However, considerable differences in the degree of bone remodeling were found between breeders and non-breeders. Pre-reproductive stages (subordinates) exhibited quite stable skeletal homeostasis and bone structure, although the attainment of sexual maturity and beginning of reproductive cycles in female breeders triggered a series of anabolic and catabolic processes that up-regulate bone turnover, most likely associated with the increased metabolic rates of reproduction. Furthermore, bone remodeling was more frequently found in stylopodial elements compared to zeugopodial elements. Despite the limited bone remodeling observed in NMRs, the variation in the pattern of skeletal homeostasis (interelement variation) reported here represents an important aspect to understand the skeletal dynamics of a small mammal with low metabolic rates. Given the relevance of the remodeling process among mammals, this study also permitted the comparison of such process with the well-documented histomorphology of extinct therapsids (i.e., mammalian precursors), thus evidencing that bone remodeling and its endocortical compartmentalization represent ancestral features among the lineage that gave rise to mammals. It is concluded that other factors associated with development (and not uniquely related to biomechanical loading) can also have an important role in the development of bone remodeling.
Identifier
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<a href="http://doi.org/10.1111/joa.13404" target="_blank" rel="noreferrer noopener">10.1111/joa.13404</a>
Format
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journalArticle
Publisher
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Journal Of Anatomy
2021
Bennett NC
Bone resorption
Chinsamy A
Dengler-Crish CM
Department of Pharmaceutical Sciences
February 2021 List
Female breeder
Haversian systems
Heterocephalus glaber
Journal of anatomy
journalArticle
Montoya-Sanhueza G
NEOMED College of Medicine
Oosthuizen MK
Secondary osteons
Secondary reconstruction
-
Text
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<a href="http://doi.org/" target="_blank" rel="noreferrer noopener">http://doi.org/</a>
Pages
1
ISSN
218782
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Update Year & Number
April 2021 List
NEOMED College
NEOMED College of Pharmacy
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Department of Pharmaceutical Sciences
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Title
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Bone remodeling in the longest living rodent, the naked mole‐rat: Interelement variation and the effects of reproduction.
Publisher
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Journal Of Anatomy
Date
A point or period of time associated with an event in the lifecycle of the resource
2021
2021-02-07
Creator
An entity primarily responsible for making the resource
Montoya‐Sanhueza G; Bennett NC; Oosthuizen MK; Dengler-Crish CM; Chinsamy A
Description
An account of the resource
The pattern of bone remodeling of one of the most peculiar mammals in the world, the naked mole‐rat (NMR), was assessed. NMRs are known for their long lifespans among rodents and for having low metabolic rates. We assessed long‐term <italic>in vivo</italic> bone labeling of subordinate individuals, as well as the patterns of bone resorption and bone remodeling in a large sample including reproductive and non‐reproductive individuals (<italic>n</italic> = 70). Over 268 undecalcified thin cross‐sections from the midshaft of humerus, ulna, femur and tibia were analyzed with confocal fluorescence and polarized light microscopy. Fluorochrome analysis revealed low osteogenesis, scarce bone resorption and infrequent formation of secondary osteons (Haversian systems) (i.e., slow bone turnover), thus most likely reflecting the low metabolic rates of this species. Secondary osteons occurred regardless of reproductive status. However, considerable differences in the degree of bone remodeling were found between breeders and non‐breeders. Pre‐reproductive stages (subordinates) exhibited quite stable skeletal homeostasis and bone structure, although the attainment of sexual maturity and beginning of reproductive cycles in female breeders triggered a series of anabolic and catabolic processes that up‐regulate bone turnover, most likely associated with the increased metabolic rates of reproduction. Furthermore, bone remodeling was more frequently found in stylopodial elements compared to zeugopodial elements. Despite the limited bone remodeling observed in NMRs, the variation in the pattern of skeletal homeostasis (interelement variation) reported here represents an important aspect to understand the skeletal dynamics of a small mammal with low metabolic rates. Given the relevance of the remodeling process among mammals, this study also permitted the comparison of such process with the well‐documented histomorphology of extinct therapsids (i.e., mammalian precursors), thus evidencing that bone remodeling and its endocortical compartmentalization represent ancestral features among the lineage that gave rise to mammals. It is concluded that other factors associated with development (and not uniquely related to biomechanical loading) can also have an important role in the development of bone remodeling. [ABSTRACT FROM AUTHOR]
Identifier
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<a href="http://doi.org/" target="_blank" rel="noreferrer noopener"></a>
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journalArticle
2021
April 2021 List
Bennett NC
Chinsamy A
Dengler-Crish CM
Department of Pharmaceutical Sciences
Journal of anatomy
journalArticle
Montoya‐Sanhueza G
NEOMED College of Pharmacy
Oosthuizen MK
-
Text
A resource consisting primarily of words for reading. Examples include books, letters, dissertations, poems, newspapers, articles, archives of mailing lists. Note that facsimiles or images of texts are still of the genre Text.
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<a href="http://doi.org/10.1111/joa.13381" target="_blank" rel="noreferrer noopener">http://doi.org/10.1111/joa.13381</a>
Pages
1259-1283
Issue
6
Volume
238
ISSN
218782
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<a href="http://neomed.idm.oclc.org/login?url=http://doi.org/10.1111/joa.13381" target="_blank" rel="noreferrer noopener">NEOMED Full-text Holding (if available) - Proxy DOI: 10.1111/joa.13381</a>
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Update Year & Number
July 2021 List
NEOMED College
NEOMED College of Pharmacy
NEOMED Department
Department of Pharmaceutical Sciences
Dublin Core
The Dublin Core metadata element set is common to all Omeka records, including items, files, and collections. For more information see, http://dublincore.org/documents/dces/.
Title
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Long bone histomorphogenesis of the naked mole‐rat: Histodiversity and intraspecific variation.
Publisher
An entity responsible for making the resource available
Journal Of Anatomy
Date
A point or period of time associated with an event in the lifecycle of the resource
2021
2021-06
Subject
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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)
Creator
An entity primarily responsible for making the resource
Montoya‐Sanhueza G; Bennett NC; Oosthuizen MK; Dengler‐Crish CM; Chinsamy A
Description
An account of the resource
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]
Identifier
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<a href="http://doi.org/10.1111/joa.13381" target="_blank" rel="noreferrer noopener">10.1111/joa.13381</a>
Rights
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Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
Format
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journalArticle
2021
Bennett NC
Body Temperature
bone growth
bone microstructure
bone modeling
Chinsamy A
Dengler‐Crish CM
Department of Pharmaceutical Sciences
endosteal bone
Heterocephalus glaber
hypothermia
Journal of anatomy
journalArticle
July 2021 List
lamellar bone
lamellar‐zonal bone
long bone growth
Montoya‐Sanhueza G
Morphogenesis
NAKED mole rat
NEOMED College of Medicine
ontogeny
Oosthuizen MK
Periosteum
POLARIZATION microscopy
STRAINS & stresses (Mechanics)