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BMC genomics2021; 22(1); 438; doi: 10.1186/s12864-021-07758-0

Integrated proteomic and transcriptomic profiling identifies aberrant gene and protein expression in the sarcomere, mitochondrial complex I, and the extracellular matrix in Warmblood horses with myofibrillar myopathy.

Abstract: Myofibrillar myopathy in humans causes protein aggregation, degeneration, and weakness of skeletal muscle. In horses, myofibrillar myopathy is a late-onset disease of unknown origin characterized by poor performance, atrophy, myofibrillar disarray, and desmin aggregation in skeletal muscle. This study evaluated molecular and ultrastructural signatures of myofibrillar myopathy in Warmblood horses through gluteal muscle tandem-mass-tag quantitative proteomics (5 affected, 4 control), mRNA-sequencing (8 affected, 8 control), amalgamated gene ontology analyses, and immunofluorescent and electron microscopy. Results: We identified 93/1533 proteins and 47/27,690 genes that were significantly differentially expressed. The top significantly differentially expressed protein CSRP3 and three other differentially expressed proteins, including, PDLIM3, SYNPO2, and SYNPOL2, are integrally involved in Z-disc signaling, gene transcription and subsequently sarcomere integrity. Through immunofluorescent staining, both desmin aggregates and CSRP3 were localized to type 2A fibers. The highest differentially expressed gene CHAC1, whose protein product degrades glutathione, is associated with oxidative stress and apoptosis. Amalgamated transcriptomic and proteomic gene ontology analyses identified 3 enriched cellular locations; the sarcomere (Z-disc & I-band), mitochondrial complex I and the extracellular matrix which corresponded to ultrastructural Z-disc disruption and mitochondrial cristae alterations found with electron microscopy. Conclusions: A combined proteomic and transcriptomic analysis highlighted three enriched cellular locations that correspond with MFM ultrastructural pathology in Warmblood horses. Aberrant Z-disc mechano-signaling, impaired Z-disc stability, decreased mitochondrial complex I expression, and a pro-oxidative cellular environment are hypothesized to contribute to the development of myofibrillar myopathy in Warmblood horses. These molecular signatures may provide further insight into diagnostic biomarkers, treatments, and the underlying pathophysiology of MFM.
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Publication Date: 2021-06-11 PubMed ID: 34112090PubMed Central: PMC8194174DOI: 10.1186/s12864-021-07758-0Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research analyses the molecular and ultrastructural signatures of a late-onset disease known as myofibrillar myopathy in Warmblood horses. The researchers identified altered gene and protein expressions associated with this disease that may provide insights into its diagnosis, treatment, and understanding of its pathophysiology.

Introduction and Background

  • Myofibrillar myopathy, or MFM, in horses is a poorly understood disease. It is characterized by poor performance, muscle atrophy (shrinkage), muscle fiber disorder, and the accumulation of a particular muscle protein, desmin. No known cause has been established yet.
  • This disease has been parallelled to a similar condition in humans leading to skeletal muscle weakness and degeneration.

Research Methodology

  • The researchers undertook a combined approach to their study, utilizing both proteomic (studying proteins) and transcriptomic (studying gene activity) profiling.
  • Tissue samples were taken from the gluteal muscle of Warmblood horses, both healthy and those affected by MFM. Advanced techniques like tandem-mass-tag quantitative proteomics and mRNA-sequencing were used to analyze the samples.
  • Apart from this molecular profiling, researchers also studied the ultrastructural changes in the muscle fibers using electron microscopy.

Results

  • 93 proteins and 47 genes were found to be significantly differentially expressed between healthy and diseased horses.
  • Specifically, four proteins (CSRP3, PDLIM3, SYNPO2, and SYNPOL2) primarily involved in Z-disc signaling and sarcomere integrity were differently expressed. Sarcomere is the basic unit of muscle tissue, and Z-disc is an important part of it.
  • Increased expressions of desmin and CSRP3 were particularly observed in a specific type of muscle fiber (2A fibers).
  • The most significantly differentially expressed gene was CHAC1, known for its role in degrading a naturally produced antioxidant—glutathione. This suggests a state of oxidative stress and cell death (apoptosis).
  • Through electron microscopy, researchers confirmed the disruptions at Z-disc, and changes to mitochondrial cristae (interior of mitochondria)

Conclusions

  • The combined proteomic and transcriptomic approach allowed researchers to pinpoint three specific cellular locations or structures that show differences in myofibrillar myopathy affected Warmblood horses—sarcomere (Z-disc and I-band), mitochondrial complex I and the extracellular matrix.
  • These changes suggest that a complex interplay of unstable Z-disc, impaired mitochondrial function, and a pro-oxidative environment might be at play in the development of MFM.
  • This research helps in a better understanding of the pathophysiology of MFM, and might eventually aid in designing diagnostic biomarkers and therapeutic interventions.

Cite This Article

APA
Williams ZJ, Velez-Irizarry D, Gardner K, Valberg SJ. (2021). Integrated proteomic and transcriptomic profiling identifies aberrant gene and protein expression in the sarcomere, mitochondrial complex I, and the extracellular matrix in Warmblood horses with myofibrillar myopathy. BMC Genomics, 22(1), 438. https://doi.org/10.1186/s12864-021-07758-0

Publication

BMC genomics
ISSN: 1471-2164
NlmUniqueID: 100965258
Country: England
Language: English
Volume: 22
Issue: 1
Pages: 438
PII: 438

Researcher Affiliations

Williams, Zoë J
  • Large Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, 784 Wilson Road, East Lansing, MI, 48824, USA. will3084@msu.edu.
Velez-Irizarry, Deborah
  • Large Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, 784 Wilson Road, East Lansing, MI, 48824, USA.
Gardner, Keri
  • Large Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, 784 Wilson Road, East Lansing, MI, 48824, USA.
Valberg, Stephanie J
  • Large Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, 784 Wilson Road, East Lansing, MI, 48824, USA.

MeSH Terms

  • Animals
  • Extracellular Matrix / genetics
  • Horses
  • Muscle, Skeletal
  • Myopathies, Structural, Congenital
  • Proteomics
  • Sarcomeres
  • Transcriptome

Conflict of Interest Statement

The authors declare that they have no competing interests.

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