Traumatic injury induces stress granule formation and enhances motor dysfunctions in ALS/FTD models

Hum Mol Genet. 2018 Apr 15;27(8):1366-1381. doi: 10.1093/hmg/ddy047.

Abstract

Traumatic brain injury (TBI) has been predicted to be a predisposing factor for amyotrophic lateral sclerosis (ALS) and other neurological disorders. Despite the importance of TBI in ALS progression, the underlying cellular and molecular mechanisms are still an enigma. Here, we examined the contribution of TBI as an extrinsic factor and investigated whether TBI influences the susceptibility of developing neurodegenerative symptoms. To evaluate the effects of TBI in vivo, we applied mild to severe trauma to Drosophila and found that TBI leads to the induction of stress granules (SGs) in the brain. The degree of SGs induction directly correlates with the level of trauma. Furthermore, we observed that the level of mortality is directly proportional to the number of traumatic hits. Interestingly, trauma-induced SGs are ubiquitin, p62 and TDP-43 positive, and persistently remain over time suggesting that SGs might be aggregates and exert toxicity in our fly models. Intriguingly, TBI on animals expressing ALS-linked genes increased mortality and locomotion dysfunction suggesting that mild trauma might aggravate neurodegenerative symptoms associated with ALS. Furthermore, we found elevated levels of high molecular weight ubiquitinated proteins and p62 in animals expressing ALS-causing genes with TBI, suggesting that TBI may lead to the defects in protein degradation pathways. Finally, we observed that genetic and pharmacological induction of autophagy enhanced the clearance of SGs and promoted survival of flies in vivo. Together, our study demonstrates that trauma can induce SG formation in vivo and might enhance neurodegenerative phenotypes in the fly models of ALS.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyotrophic Lateral Sclerosis / genetics*
  • Amyotrophic Lateral Sclerosis / metabolism
  • Amyotrophic Lateral Sclerosis / pathology
  • Animals
  • Animals, Genetically Modified
  • Autophagy / genetics
  • Brain / metabolism*
  • Brain / pathology
  • Brain Injuries, Traumatic / genetics*
  • Brain Injuries, Traumatic / metabolism
  • Brain Injuries, Traumatic / pathology
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cytoplasmic Granules / metabolism*
  • Cytoplasmic Granules / pathology
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Disease Models, Animal
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics*
  • Drosophila melanogaster / metabolism
  • Frontotemporal Dementia / genetics*
  • Frontotemporal Dementia / metabolism
  • Frontotemporal Dementia / pathology
  • Humans
  • Locomotion / physiology
  • Longevity
  • Neurons / metabolism
  • Neurons / pathology
  • Protein Processing, Post-Translational*
  • TATA-Binding Protein Associated Factors / genetics
  • TATA-Binding Protein Associated Factors / metabolism
  • Transcription Factor TFIID / genetics
  • Transcription Factor TFIID / metabolism
  • Trauma Severity Indices
  • Ubiquitin / genetics
  • Ubiquitin / metabolism
  • Ubiquitination

Substances

  • Carrier Proteins
  • DNA-Binding Proteins
  • Drosophila Proteins
  • TATA-Binding Protein Associated Factors
  • TBPH protein, Drosophila
  • Taf6 protein, Drosophila
  • Transcription Factor TFIID
  • Ubiquitin
  • rin protein, Drosophila

Supplementary concepts

  • Frontotemporal Dementia With Motor Neuron Disease