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Article ; Online: Mitochondria: Key modulators of skeletal muscle remodeling.

Quadrilatero, Joe

Seminars in cell & developmental biology

2022 Volume 143, Page(s) 1–2

MeSH term(s)	Muscle, Skeletal/metabolism ; Mitochondria
Language	English
Publishing date	2022-11-12
Publishing country	England
Document type	Editorial ; Research Support, Non-U.S. Gov't
ZDB-ID	1312473-0
ISSN	1096-3634 ; 1084-9521
ISSN (online)	1096-3634
ISSN	1084-9521
DOI	10.1016/j.semcdb.2022.10.004
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Article ; Online: Mitochondrial Apoptotic Signaling Involvement in Remodeling During Myogenesis and Skeletal Muscle Atrophy.

Rahman, Fasih Ahmad / Quadrilatero, Joe

Seminars in cell & developmental biology

2022 Volume 143, Page(s) 66–74

Abstract: Mitochondria play a major role in apoptotic signaling. In addition to its role in eliminating dysfunctional cells, mitochondrial apoptotic signaling is implicated as a key component of myogenic differentiation and skeletal muscle atrophy. For example, ... ...

Abstract	Mitochondria play a major role in apoptotic signaling. In addition to its role in eliminating dysfunctional cells, mitochondrial apoptotic signaling is implicated as a key component of myogenic differentiation and skeletal muscle atrophy. For example, the activation of cysteine-aspartic proteases (caspases; CASP's) can aid in the initial remodeling stages of myogenic differentiation by cleaving protein kinases, transcription factors, and cytoskeletal proteins. Precise regulation of these signals is needed to prevent excessive cell disassemble and subsequent cell death. During skeletal muscle atrophy, the activation of CASP's and mitochondrial derived nucleases participate in myonuclear fragmentation, a potential loss of myonuclei, and cleavage of contractile structures within skeletal muscle. The B cell leukemia/lymphoma 2 (BCL2) family of proteins play a significant role in regulating myogenesis and skeletal muscle atrophy by governing the initiating steps of mitochondrial apoptotic signaling. This review discusses the role of mitochondrial apoptotic signaling in skeletal muscle remodeling during myogenic differentiation and skeletal muscle pathological states, including aging, disuse, and muscular dystrophy.
MeSH term(s)	Humans ; Apoptosis/physiology ; Caspases/metabolism ; Muscle Development/physiology ; Muscle, Skeletal/metabolism ; Muscular Atrophy/metabolism ; Muscular Atrophy/pathology ; Mitochondria, Muscle/metabolism
Chemical Substances	Caspases (EC 3.4.22.-)
Language	English
Publishing date	2022-02-28
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1312473-0
ISSN	1096-3634 ; 1084-9521
ISSN (online)	1096-3634
ISSN	1084-9521
DOI	10.1016/j.semcdb.2022.01.011
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Article ; Online: Initiation and accumulation of loading induced changes to native collagen content and microstructural damage in the cartilaginous endplate.

Zehr, Jackie D / Quadrilatero, Joe / Callaghan, Jack P

The spine journal : official journal of the North American Spine Society

2023 Volume 24, Issue 1, Page(s) 161–171

Abstract: Background context: Injury to the cartilaginous endplate (CEP) is linked to clinically relevant low back disorders, including intervertebral disc degeneration and pain reporting. Despite this link to clinical disorders, the CEP injury pathways and the ... ...

Abstract	Background context: Injury to the cartilaginous endplate (CEP) is linked to clinically relevant low back disorders, including intervertebral disc degeneration and pain reporting. Despite this link to clinical disorders, the CEP injury pathways and the modulating effect of mechanical loading parameters on the pace of damage accumulation remains poorly understood. Purpose: This study examined the effect of cyclic loading on the initiation and accumulation of changes to native collagen content (type I, type II) and microstructural damage in the central region of cadaveric porcine CEPs. Study design: In vitro longitudinal study. Methods: One hundred fourteen porcine cervical spinal units were included (N=6 per group). The study contained a control group (no cyclic loading) and 18 experimental groups that differed by loading duration (1,000, 3,000, 5,000 cycles), joint posture (flexed, neutral), and cyclic peak compression variation (10%, 20%, 40%). Multicolor immunofluorescence staining was used to quantify loading induced changes to type I (ie, subchondral bone) and type II (ie, endplate) native collagen content (fluorescence area, fluorescence intensity) and microstructural damage (pore area [transverse plane], void area along the CEP-bone border [sagittal plane]). Results: Significant main effects of loading duration and posture were observed for fluorescence area and fluorescence intensity of type I and II collagen. In the transverse plane, type II fluorescence area significantly decreased following 1,000 cycles (-12%), but a significant change in fluorescence intensity was not observed until 3,000 cycles (-17%). Type II fluorescence area (-14%) and intensity (-10%) were both significantly less in flexed postures compared to neutral. Similar trends were observed for type I collagen in the sagittal plane sections. Generally, significant changes to fluorescence area were accompanied by the development of microstructural voids along the endplate-subchondral bone border. Conclusions: These findings demonstrate that microstructural damage beneath the endplate surface occurs before significant changes to the density of native type I and II collagen fibers. Although flexed postures were associated with greater and accelerated changes to native collagen content, the injury initiation mechanism appears similar to neutral. Clinical significance: Neutral joint postures can delay the initiation and pace of microdamage accumulation in the CEP during low-to-moderate demand lifting tasks. Furthermore, the management of peak compression exposures appeared relevant only when a neutral posture was maintained. Therefore, clinical low back injury prevention and load management efforts should consider low back posture in parallel with applied joint forces.
MeSH term(s)	Humans ; Animals ; Swine ; Longitudinal Studies ; Cartilage/metabolism ; Spine/metabolism ; Intervertebral Disc Degeneration/metabolism ; Collagen ; Intervertebral Disc/metabolism ; Weight-Bearing
Chemical Substances	Collagen (9007-34-5)
Language	English
Publishing date	2023-07-22
Publishing country	United States
Document type	Journal Article
ZDB-ID	2037072-6
ISSN	1878-1632 ; 1529-9430
ISSN (online)	1878-1632
ISSN	1529-9430
DOI	10.1016/j.spinee.2023.07.018
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Article ; Online: Indentation mechanics and native collagen content in the cartilaginous endplate: A comparison between porcine cervical and human lumbar spines.

Zehr, Jackie D / Quadrilatero, Joe / Callaghan, Jack P

Journal of the mechanical behavior of biomedical materials

2023 Volume 150, Page(s) 106334

Abstract: This study characterized the regional indentation mechanics and native collagen content in cartilaginous endplates (CEPs) from the porcine cervical spine, young human lumbar spine, and aged human lumbar spine. Seventeen endplates were included in this ... ...

Abstract	This study characterized the regional indentation mechanics and native collagen content in cartilaginous endplates (CEPs) from the porcine cervical spine, young human lumbar spine, and aged human lumbar spine. Seventeen endplates were included in this study: six porcine cervical, nine young human lumbar, and two aged human lumbar. Width and depth measurements were obtained using a digital caliper and used to size-normalize and identify the central, anterior, posterior, and lateral regions. Regional microindentation tests were performed using a serial robot, where surface locations were loaded/unloaded at 0.1 mm/s and held at a constant 10 N force for 30 s. Loading stiffness and creep displacement were obtained from force-displacement data. Immunofluorescence staining for type I and type II collagen was subsequently performed on sagittal sections of all endplate regions. 255 images were obtained from which fluorescence intensity, sub-surface void area, and cartilage thickness were measured. CEPs from the young human lumbar spine were, on average, 27% more compliant, 0.891 mm thicker, had a lower fluorescence intensity for native collagen proteins within the cartilage (-58%) and subchondral bone (-24%), and had a sub-surface void area that was 19.7 times greater than porcine cervical CEPs. Compared to aged human lumbar CEPs, young human lumbar CEPs were 57% stiffer, 0.568 mm thicker, had a higher fluorescence intensity for native collagen proteins within the cartilage (+30%) and subchondral bone (+46%), and had a sub-surface void area that was 10.6 times smaller. Although not a perfect mechanical and structural surrogate, porcine cervical CEPs provided initial conditions that may be more representative of the young and healthy human lumbar spine compared to aged human cadaveric specimens. The indentation properties presented may have further applications to finite element models of the human lumbar spine.
MeSH term(s)	Humans ; Swine ; Animals ; Aged ; Lumbar Vertebrae ; Cartilage ; Cervical Vertebrae ; Collagen ; Cadaver
Chemical Substances	Collagen (9007-34-5)
Language	English
Publishing date	2023-12-29
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	2378381-3
ISSN	1878-0180 ; 1751-6161
ISSN (online)	1878-0180
ISSN	1751-6161
DOI	10.1016/j.jmbbm.2023.106334
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Article ; Online: Emerging role of mitophagy in myoblast differentiation and skeletal muscle remodeling.

F, Ahmad Rahman / Quadrilatero, Joe

Seminars in cell & developmental biology

2021 Volume 143, Page(s) 54–65

Abstract: Mitochondrial turnover in the form of mitophagy is emerging as a central process in maintaining cellular function. The degradation of damaged mitochondria through mitophagy is particularly important in cells/tissues that exhibit high energy demands. ... ...

Abstract	Mitochondrial turnover in the form of mitophagy is emerging as a central process in maintaining cellular function. The degradation of damaged mitochondria through mitophagy is particularly important in cells/tissues that exhibit high energy demands. Skeletal muscle is one such tissue that requires precise turnover of mitochondria in several conditions in order to optimize energy production and prevent bioenergetic crisis. For instance, the formation of skeletal muscle (i.e., myogenesis) is accompanied by robust turnover of low-functioning mitochondria to eventually allow the formation of high-functioning mitochondria. In mature skeletal muscle, alterations in mitophagy-related signaling occur during exercise, aging, and various disease states. Nonetheless, several questions regarding the direct role of mitophagy in various skeletal muscle conditions remain unknown. Furthermore, given the heterogenous nature of skeletal muscle with respect to various cellular and molecular properties, and the plasticity in these properties in various conditions, the involvement and characterization of mitophagy requires more careful consideration in this tissue. Therefore, this review will highlight the known mechanisms of mitophagy in skeletal muscle, and discuss their involvement during myogenesis and various skeletal muscle conditions. This review also provides important considerations for the accurate measurement of mitophagy and interpretation of data in skeletal muscle.
MeSH term(s)	Mitophagy/physiology ; Autophagy ; Muscle, Skeletal/metabolism ; Cell Differentiation ; Myoblasts/metabolism
Language	English
Publishing date	2021-12-17
Publishing country	England
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't
ZDB-ID	1312473-0
ISSN	1096-3634 ; 1084-9521
ISSN (online)	1096-3634
ISSN	1084-9521
DOI	10.1016/j.semcdb.2021.11.026
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Article ; Online: Mitochondrial network remodeling: an important feature of myogenesis and skeletal muscle regeneration.

Rahman, Fasih Ahmad / Quadrilatero, Joe

Cellular and molecular life sciences : CMLS

2021 Volume 78, Issue 10, Page(s) 4653–4675

Abstract: The remodeling of the mitochondrial network is a critical process in maintaining cellular homeostasis and is intimately related to mitochondrial function. The interplay between the formation of new mitochondria (biogenesis) and the removal of damaged ... ...

Abstract	The remodeling of the mitochondrial network is a critical process in maintaining cellular homeostasis and is intimately related to mitochondrial function. The interplay between the formation of new mitochondria (biogenesis) and the removal of damaged mitochondria (mitophagy) provide a means for the repopulation of the mitochondrial network. Additionally, mitochondrial fission and fusion serve as a bridge between biogenesis and mitophagy. In recent years, the importance of these processes has been characterised in multiple tissue- and cell-types, and under various conditions. In skeletal muscle, the robust remodeling of the mitochondrial network is observed, particularly after injury where large portions of the tissue/cell structures are damaged. The significance of mitochondrial remodeling in regulating skeletal muscle regeneration has been widely studied, with alterations in mitochondrial remodeling processes leading to incomplete regeneration and impaired skeletal muscle function. Needless to say, important questions related to mitochondrial remodeling and skeletal muscle regeneration still remain unanswered and require further investigation. Therefore, this review will discuss the known molecular mechanisms of mitochondrial network remodeling, as well as integrate these mechanisms and discuss their relevance in myogenesis and regenerating skeletal muscle.
MeSH term(s)	Animals ; Humans ; Mitochondria/physiology ; Muscle Development ; Muscle, Skeletal/cytology ; Regeneration
Language	English
Publishing date	2021-03-22
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	1358415-7
ISSN	1420-9071 ; 1420-682X
ISSN (online)	1420-9071
ISSN	1420-682X
DOI	10.1007/s00018-021-03807-9
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Article: Mitochondrial network remodeling: an important feature of myogenesis and skeletal muscle regeneration

Rahman, Fasih Ahmad / Quadrilatero, Joe

Cellular and molecular life sciences. 2021 May, v. 78, no. 10

2021

Abstract	The remodeling of the mitochondrial network is a critical process in maintaining cellular homeostasis and is intimately related to mitochondrial function. The interplay between the formation of new mitochondria (biogenesis) and the removal of damaged mitochondria (mitophagy) provide a means for the repopulation of the mitochondrial network. Additionally, mitochondrial fission and fusion serve as a bridge between biogenesis and mitophagy. In recent years, the importance of these processes has been characterised in multiple tissue- and cell-types, and under various conditions. In skeletal muscle, the robust remodeling of the mitochondrial network is observed, particularly after injury where large portions of the tissue/cell structures are damaged. The significance of mitochondrial remodeling in regulating skeletal muscle regeneration has been widely studied, with alterations in mitochondrial remodeling processes leading to incomplete regeneration and impaired skeletal muscle function. Needless to say, important questions related to mitochondrial remodeling and skeletal muscle regeneration still remain unanswered and require further investigation. Therefore, this review will discuss the known molecular mechanisms of mitochondrial network remodeling, as well as integrate these mechanisms and discuss their relevance in myogenesis and regenerating skeletal muscle.
Keywords	biogenesis ; homeostasis ; mitochondria ; mitophagy ; muscle development ; skeletal muscle
Language	English
Dates of publication	2021-05
Size	p. 4653-4675.
Publishing place	Springer International Publishing
Document type	Article
Note	NAL-AP-2-clean ; Review
ZDB-ID	1358415-7
ISSN	1420-9071 ; 1420-682X
ISSN (online)	1420-9071
ISSN	1420-682X
DOI	10.1007/s00018-021-03807-9
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Article ; Online: Incidence of Compression-Induced Microinjuries in the Cartilage Endplate of the Spine.

Zehr, Jackie D / Quadrilatero, Joe / Callaghan, Jack P

Spine

2022 Volume 48, Issue 9, Page(s) E122–E129

Abstract: Study design: In vitro biomechanical study.: Objective: This study investigated the incidence of microstructural endplate injuries caused by cyclic compression loading. The covarying effects of joint posture, loading duration, and peak compression ... ...

Abstract	Study design: In vitro biomechanical study. Objective: This study investigated the incidence of microstructural endplate injuries caused by cyclic compression loading. The covarying effects of joint posture, loading duration, and peak compression variation were assessed. Summary of background data: The endplate is physiologically and functionally important for the maintenance of spine health. Despite the ability to radiographically diagnose and classify macroscopic endplate injuries, the mechanical mechanisms of injury initiation and progression remain largely unknown. Methods: One hundred and fourteen porcine cervical spinal units were examined. All spinal units were exposed to preconditioning tests, followed by cyclic compression testing that differed by posture (flexed, neutral), loading duration (1000, 3000, 5000 cycles), and peak compression variation (10%, 20%, 40%). Microstructural injuries were examined via immunofluorescence staining for collagen I ( i.e. , subchondral bone) and collagen II ( i.e. , hyaline cartilage endplate). From the 678 acquired images, the incidence of node, avulsion, cartilage, and circumferential pore microinjuries were determined. The distribution of microinjuries between postures, spinal levels, and vertebrae were evaluated along with the associations of incidence and size of injuries with loading duration and variation. Results: The incidence of avulsion injuries was significantly greater in caudal endplates (92%, P =0.006). No other injuries differed between vertebrae ( P ≥0.804) and no significant differences were observed between spinal units ( P ≥0.158). With respect to posture, 100% ( P <0.001) and 90% ( P <0.001) of avulsion and node injuries, respectively, occurred in flexed postures, whereas 82% ( P <0.001) of cartilage microinjuries occurred with neutral postures. Loading duration was significantly associated with microinjury incidence ( P <0.001) and lesion size ( P ≤0.003). Conclusion: Mechanical factors such as posture did not appreciably affect the incidence of endplate injury, but microinjury types were differently distributed between flexed and neutral postures. The duration of compression was shown to have an important role in the incidence of microinjury and lesion size.
MeSH term(s)	Animals ; Swine ; Incidence ; Weight-Bearing/physiology ; Stress, Mechanical ; Spine ; Biomechanical Phenomena/physiology ; Hyaline Cartilage
Language	English
Publishing date	2022-11-02
Publishing country	United States
Document type	Journal Article
ZDB-ID	752024-4
ISSN	1528-1159 ; 0362-2436
ISSN (online)	1528-1159
ISSN	0362-2436
DOI	10.1097/BRS.0000000000004521
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Article ; Online: Autophagy displays divergent roles during intermittent amino acid starvation and toxic stress-induced senescence in cultured skeletal muscle cells.

Bloemberg, Darin / Quadrilatero, Joe

Journal of cellular physiology

2020 Volume 236, Issue 4, Page(s) 3099–3113

Abstract: Due to the ever-expanding functions attributed to autophagy, there is widespread interest in understanding its contribution to human physiology; however, its specific cellular role as a stress-response mechanism is still poorly defined. To investigate ... ...

Abstract	Due to the ever-expanding functions attributed to autophagy, there is widespread interest in understanding its contribution to human physiology; however, its specific cellular role as a stress-response mechanism is still poorly defined. To investigate autophagy's role in this regard, we repeatedly subjected cultured mouse myoblasts to two stresses with diverse impacts on autophagic flux: amino acid and serum withdrawal (Hank's balanced salt solution [HBSS]), which robustly induces autophagy, or low-level toxic stress (staurosporine, STS). We found that intermittent STS (int-STS) administration caused cell cycle arrest, development of enlarged and misshapen cells/nuclei, increased senescence-associated heterochromatic foci and senescence-associated β-galactosidase activity, and prevented myogenic differentiation. These features were not observed in cells intermittently incubated in HBSS (int-HB). While int-STS cells displayed less DNA damage (phosphorylated H2A histone family, member X content) and caspase activity when administered cisplatin, int-HB cells were protected from STS-induced cell death. Interestingly, STS-induced senescence was attenuated in autophagy related 7-deficient cells. Therefore, while repeated nutrient withdrawal did not cause senescence, autophagy was required for senescence caused by toxic stress. These results illustrate the context-dependent effects of different stressors, potentially highlighting autophagy as a distinguishing factor.
Language	English
Publishing date	2020-10-06
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	3116-1
ISSN	1097-4652 ; 0021-9541
ISSN (online)	1097-4652
ISSN	0021-9541
DOI	10.1002/jcp.30079
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Article ; Online: Mechanically induced histochemical and structural damage in the annulus fibrosus and cartilaginous endplate: a multi-colour immunofluorescence analysis.

Zehr, Jackie D / Rahman, Fasih Ahmad / Callaghan, Jack P / Quadrilatero, Joe

Cell and tissue research

2022 Volume 390, Issue 1, Page(s) 59–70

Abstract: The annulus fibrosus (AF) and endplate (EP) are collagenous spine tissues that are frequently injured due to gradual mechanical overload. Macroscopic injuries to these tissues are typically a by-product of microdamage accumulation. Many existing ... ...

Abstract	The annulus fibrosus (AF) and endplate (EP) are collagenous spine tissues that are frequently injured due to gradual mechanical overload. Macroscopic injuries to these tissues are typically a by-product of microdamage accumulation. Many existing histochemistry and biochemistry techniques are used to examine microdamage in the AF and EP; however, there are several limitations when used in isolation. Immunofluorescence may be sensitive to histochemical and structural damage and permits the simultaneous evaluation of multiple proteins-collagen I (COL I) and collagen II (COL II). This investigation characterized the histochemical and structural damage in initially healthy porcine spinal joints that were either unloaded (control) or loaded via biofidelic compression loading. The mean fluorescence area and mean fluorescence intensity of COL II significantly decreased (- 54.9 and - 44.8%, respectively) in the loaded AF (p ≤ 0.002), with no changes in COL I (p ≥ 0.471). In contrast, the EP displayed similar decreases in COL I and COL II fluorescence area (- 35.6 and - 37.7%, respectively) under loading conditions (p ≤ 0.027). A significant reduction (-31.1%) in mean fluorescence intensity was only observed for COL II (p = 0.043). The normalized area of pores was not altered on the endplate surface (p = 0.338), but a significant increase (+ 7.0%) in the void area was observed on the EP-subchondral bone interface (p = 0.002). Colocalization of COL I and COL II was minimal in all tissues (R < 0.34). In conclusion, the immunofluorescence analysis captured histochemical and structural damage in collagenous spine tissues, namely, the AF and EP.
MeSH term(s)	Animals ; Annulus Fibrosus ; Collagen ; Color ; Fluorescent Antibody Technique ; Intervertebral Disc ; Spine ; Swine
Chemical Substances	Collagen (9007-34-5)
Language	English
Publishing date	2022-07-06
Publishing country	Germany
Document type	Journal Article
ZDB-ID	125067-x
ISSN	1432-0878 ; 0302-766X
ISSN (online)	1432-0878
ISSN	0302-766X
DOI	10.1007/s00441-022-03649-2
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