Spatial frequency metrics for analysis of microscopic images of musculoskeletal tissues

Tehrani, Kayvan Forouhesh; Pendleton, Emily G.; Southern, William M.; Call, Jarrod A.; Mortensen, Luke J.

doi:10.1080/03008207.2020.1828381

Cited by 18 publications

(8 citation statements)

References 41 publications

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“…A greater energetic potential at the mitochondrial membrane in concert with less J O 2 could indicate a higher resistance to ATP synthesis. However, the mitochondrial network becomes highly fractured and disorganized during this time after VML injury ( Southern et al, 2019 ; Forouhesh Tehrani et al, 2021 ) and one of the determinants of mitochondrial function is its location and structural organization ( Ferreira et al, 2010 ; Glancy et al, 2015 ; Glancy et al, 2017 ). The mitochondrial network connectively has been shown to rapidly distribute changes in mitochondrial membrane potential ( Glancy et al, 2015 ; Glancy et al, 2017 ), effectively distributing energy more rapidly in a cell than would otherwise be possible via substrate diffusion alone.…”

Section: Resultsmentioning

confidence: 99%

The bioenergetic “CK Clamp” technique detects substrate-specific changes in mitochondrial respiration and membrane potential during early VML injury pathology

et al. 2023

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Volumetric muscle loss (VML) injuries are characterized by non-recoverable loss of tissue resulting in contractile and metabolic dysfunction. The characterization of metabolic dysfunction in volumetric muscle loss-injured muscle has been interpreted from permeabilized myofiber respiration experiments involving saturating ADP levels and non-physiologic ATP:ADP concentration ratios. The extent to which this testing condition obscures the analysis of mitochondrial (dys) function after volumetric muscle loss injury is unclear. An alternative approach is described that leverages the enzymatic reaction of creatine kinase and phosphocreatine to assess mitochondrial respiration and membrane potential at clamped physiologic ATP:ADP ratios, “CK Clamp.” The objective of this study was to validate the CK Clamp in volumetric muscle loss-injured muscle and to detect differences that may exist between volumetric muscle loss-injured and uninjured muscles at 1, 3, 5, 7, 10, and 14 days post-injury. Volumetric muscle loss-injured muscle maintains bioenergetic features of the CK Clamp approach, i.e., mitochondrial respiration rate (JO2) titters down and mitochondrial membrane potential is more polarized with increasing ATP:ADP ratios. Pyruvate/malate/succinate-supported JO2 was significantly less in volumetric muscle loss-injured muscle at all timepoints compared to uninjured controls (−26% to −84%, p < 0.001) and electron conductance was less at day 1 (−60%), 5 (−52%), 7 (−35%), 10 (−59%), and 14 (−41%) (p < 0.001). Palmitoyl-carnitine/malate-supported JO2 and electron conductance were less affected following volumetric muscle loss injury. volumetric muscle loss-injury also corresponded with a more polarized mitochondrial membrane potential across the clamped ATP:ADP ratios at day 1 and 10 (pyruvate and palmitoyl-carnitine, respectively) (+5%, p < 0.001). This study supports previous characterizations of metabolic dysfunction and validates the CK Clamp as a tool to investigate bioenergetics in traumatically-injured muscle.

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Section: Resultsmentioning

confidence: 99%

The bioenergetic “CK Clamp” technique detects substrate-specific changes in mitochondrial respiration and membrane potential during early VML injury pathology

et al. 2023

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“…Touching objects were split using a seed points diameter of 13.8 μm. Muscle fiber and collagen alignment ( Figure 6 ) were analyzed using a home-built 2 photon imaging system as described previously ( Forouhesh Tehrani et al, 2020 ; Pendleton et al, 2020 ). In brief, SHG images (512 × 512 pixels) of collagen and actin muscle structure were produced with linearly polarized excitation rotated at 10° intervals.…”

Section: Methodsmentioning

confidence: 99%

Nanofiber-Based Delivery of Bioactive Lipids Promotes Pro-regenerative Inflammation and Enhances Muscle Fiber Growth After Volumetric Muscle Loss

Emeterio

Hymel

Turner

et al. 2021

Front. Bioeng. Biotechnol.

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Volumetric muscle loss (VML) injuries after extremity trauma results in an important clinical challenge often associated with impaired healing, significant fibrosis, and long-term pain and functional deficits. While acute muscle injuries typically display a remarkable capacity for regeneration, critically sized VML defects present a dysregulated immune microenvironment which overwhelms innate repair mechanisms leading to chronic inflammation and pro-fibrotic signaling. In this series of studies, we developed an immunomodulatory biomaterial therapy to locally modulate the sphingosine-1-phosphate (S1P) signaling axis and resolve the persistent pro-inflammatory injury niche plaguing a critically sized VML defect. Multiparameter pseudo-temporal 2D projections of single cell cytometry data revealed subtle distinctions in the altered dynamics of specific immune subpopulations infiltrating the defect that were critical to muscle regeneration. We show that S1P receptor modulation via nanofiber delivery of Fingolimod (FTY720) was characterized by increased numbers of pro-regenerative immune subsets and coincided with an enriched pool of muscle stem cells (MuSCs) within the injured tissue. This FTY720-induced priming of the local injury milieu resulted in increased myofiber diameter and alignment across the defect space followed by enhanced revascularization and reinnervation of the injured muscle. These findings indicate that localized modulation of S1P receptor signaling via nanofiber scaffolds, which resemble the native extracellular matrix ablated upon injury, provides great potential as an immunotherapy for bolstering endogenous mechanisms of regeneration following VML injury.

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“…Skeletal tissues such as muscle and bone have periodic structural elements which can undergo substantial alterations during maturation, adaptation, injury, and regeneration. Tehrani et al 8 report a novel methodology based upon spatial frequency domain analysis of second harmonic generation (SHG) microscopic images. These Fourier-based metrics provide volumetric assessment of angular integrity and periodic consistency.…”

Section: Novel Methodologic Approachesmentioning

confidence: 99%

Cross-talk with skeletal muscle and its nexus with regenerative rehabilitation

Greising

Wang

2020

Connective Tissue Research

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Spatial frequency metrics for analysis of microscopic images of musculoskeletal tissues

Cited by 18 publications

References 41 publications

The bioenergetic “CK Clamp” technique detects substrate-specific changes in mitochondrial respiration and membrane potential during early VML injury pathology

The bioenergetic “CK Clamp” technique detects substrate-specific changes in mitochondrial respiration and membrane potential during early VML injury pathology

Nanofiber-Based Delivery of Bioactive Lipids Promotes Pro-regenerative Inflammation and Enhances Muscle Fiber Growth After Volumetric Muscle Loss

Cross-talk with skeletal muscle and its nexus with regenerative rehabilitation

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