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Tracking Effects of SIL1 Increase: Taking a Closer Look Beyond the Consequences of Elevated Expression Level

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Abstract

SIL1 acts as a co-chaperone for the major ER-resident chaperone BiP and thus plays a role in many BiP-dependent cellular functions such as protein-folding control and unfolded protein response. Whereas the increase of BiP upon cellular stress conditions is a well-known phenomenon, elevation of SIL1 under stress conditions was thus far solely studied in yeast, and different studies indicated an adverse effect of SIL1 increase. This is seemingly in contrast with the beneficial effect of SIL1 increase in surviving neurons in neurodegenerative disorders such as amyotrophic lateral sclerosis and Alzheimer’s disease. Here, we addressed these controversial findings. Applying cell biological, morphological and biochemical methods, we demonstrated that SIL1 increases in various mammalian cells and neuronal tissues upon cellular stress. Investigation of heterozygous SIL1 mutant cells and tissues supported this finding. Moreover, SIL1 protein was found to be stabilized during ER stress. Increased SIL1 initiates ER stress in a concentration-dependent manner which agrees with the described adverse SIL1 effect. However, our results also suggest that protective levels are achieved by the secretion of excessive SIL1 and GRP170 and that moderately increased SIL1 also ameliorates cellular fitness under stress conditions. Our immunoprecipitation results indicate that SIL1 might act in a BiP-independent manner. Proteomic studies showed that SIL1 elevation alters the expression of proteins including crucial players in neurodegeneration, especially in Alzheimer’s disease. This finding agrees with our observation of increased SIL1 immunoreactivity in surviving neurons of Alzheimer’s disease autopsy cases and supports the assumption that SIL1 plays a protective role in neurodegenerative disorders.

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Acknowledgements

Financial support by the Ministerium für Innovation, Wissenschaft und Forschung des Landes Nordrhein-Westfalen, the Senatsverwaltung für Wirtschaft, Technologie und Forschung des Landes Berlin and the Bundesministerium für Bildung und Forschung is gratefully acknowledged. This work was also supported by a grant from the START program of RWTH Aachen University (to A. R.; grant No. 41/12) and by the German Research Foundation (DFG to R. Z.; grant no. ZA 639/1-1) as well as by the Deutsche Gesellschaft für Muskelkranke (DGM) and the IZKF Aachen (to J. W.; grant no. N5-3). We thank Mrs. Claudia Krude, Mrs. Hannelore Mader, Mrs. Astrid Knichewski, Mr. Julian Kaufmann and Mrs. Sarah Waide for expert technical assistance. Immortalized lymphoblastoid cells were kindly provided by Professor Jan Senderek (Friedrich-Baur-Institute Munich, Germany).

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Author notes

  1. Thomas Labisch and Stephan Buchkremer contributed equally to this work.

Authors and Affiliations

  1. Institute of Neuropathology, RWTH Aachen University Hospital, Pauwelsstr. 30, 52074, Aachen, Germany

    Thomas Labisch, Stephan Buchkremer, Christian Gatz, Chris Lentz, Kay Nolte, José Andrés González Coraspe, Joachim Weis & Andreas Roos

  2. Leibniz-Institut für Analytische Wissenschaften - ISAS - e.V, Otto-Hahn-Str. 6b, 44227, Dortmund, Germany

    Vietxuan Phan, Laxmikanth Kollipara, Albert Sickmann, René P. Zahedi & Andreas Roos

  3. Institute of Biochemistry and Molecular Biology, RWTH Aachen University Hospital, Pauwelsstr. 30, 52074, Aachen, Germany

    Jörg Vervoorts

  4. Department of Chemistry, College of Physical Sciences, University of Aberdeen, Aberdeen, Scotland, UK

    Albert Sickmann

  5. Medizinisches Proteom-Center (MPC), Ruhr-Universität Bochum, Bochum, Germany

    Albert Sickmann

  6. Institute of Genetic Medicine, John Walton Muscular Dystrophy Research Centre, International Centre for Life, Central Parkway, Newcastle upon Tyne, England, UK

    Stephanie Carr & Andreas Roos

Authors
  1. Thomas Labisch
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  2. Stephan Buchkremer
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  3. Vietxuan Phan
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  4. Laxmikanth Kollipara
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  5. Christian Gatz
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  6. Chris Lentz
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  7. Kay Nolte
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  8. Jörg Vervoorts
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  9. José Andrés González Coraspe
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  10. Albert Sickmann
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  11. Stephanie Carr
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  12. René P. Zahedi
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  13. Joachim Weis
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  14. Andreas Roos
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Corresponding author

Correspondence to Andreas Roos.

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Labisch, T., Buchkremer, S., Phan, V. et al. Tracking Effects of SIL1 Increase: Taking a Closer Look Beyond the Consequences of Elevated Expression Level. Mol Neurobiol 55, 2524–2546 (2018). https://doi.org/10.1007/s12035-017-0494-6

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  • DOI: https://doi.org/10.1007/s12035-017-0494-6

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