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High prevalence of serum anti-NH2-terminal of α-enolase antibodies in patients with multiple system atrophy and corticobasal syndrome

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Abstract

Background

Hashimoto’s encephalopathy with serum anti-NH2-terminal of α-enolase (NAE) antibodies occasionally displays clinical symptoms such as cerebellar ataxia and parkinsonism. We studied the frequency of anti-NAE antibodies in patients with Parkinson-plus syndrome.

Methods

We examined the positive rates of anti-NAE antibodies in 47 patients with multiple system atrophy (MSA), 29 patients with Parkinson’s disease (PD), eight patients with corticobasal syndrome (CBS), and 18 patients with progressive supranuclear palsy (PSP) using conventional immunoblot analysis.

Results

Positive anti-NAE antibody rates of 31.9%, 10.3%, 50.0%, and 11.1% were reported in the MSA, PD, CBS, and PSP patients, respectively. The duration from onset to a wheelchair-bound state in seropositive MSA patients tended to be shorter than that in seronegative MSA patients.

Conclusions

Anti-NAE antibodies are detected in some patients clinically diagnosed with MSA and CBS. Although its pathophysiological significance remains uncertain, serum anti-NAE antibodies might represent a prognostic marker in the clinical course of MSA.

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References

  1. Fujii A, Yoneda M, Ito T, Yamamura O, Satomi S, Higa H, Kimura A, Suzuki M, Yamashita M, Yuasa T, Suzuki H, Kuriyama M (2005) Autoantibodies against the amino terminal of alpha-enolase are a useful diagnostic marker of Hashimoto’s encephalopathy. J Neuroimmunol 162:130–136

    Article  CAS  Google Scholar 

  2. Nakagawa H, Yoneda M, Fujii A, Kinomoto K, Kuriyama M (2007) Hashimoto’s encephalopathy presenting with progressive cerebellar ataxia. J Neurol Neurosurg Psychiatry 78:196–197

    Article  CAS  Google Scholar 

  3. Matsunaga A, Ikawa M, Fujii A, Nakamoto Y, Kuriyama M, Yoneda M (2013) Hashimoto’s encephalopathy as a treatable adult-onset cerebellar ataxia mimicking spinocerebellar degeneration. Eur Neurol 69:14–20

    Article  Google Scholar 

  4. Yoneda M, Fujii A, Ito A, Yokoyama H, Nakagawa H, Kuriyama M (2007) High prevalence of serum autoantibodies against the amino terminal of alpha-enolase in Hashimoto’s encephalopathy. J Neuroimmunol 185:195–200

    Article  CAS  Google Scholar 

  5. Inoue K, Kitamura J, Yoneda M, Imamura E, Tokinobu H (2012) Hashimoto’s encephalopathy presenting with micrographia as a typical feature of parkinsonism. Neurol Sci 33:395–397

    Article  CAS  Google Scholar 

  6. Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ, Wood NW, Colosimo C, Durr A, Fowler CJ, Kaufmann H, Klockgether T, Lees A, Poewe W, Quinn N, Revesz T, Robertson D, Sandroni P, Seppi K, Vidailhet M (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71:670–676

    Article  CAS  Google Scholar 

  7. Gibb WR, Lees AJ (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 51:745–752

    Article  CAS  Google Scholar 

  8. Mathew R, Bak TH, Hodges JR (2012) Diagnostic criteria for corticobasal syndrome: a comparative study. J Neurol Neurosurg Psychiatry 83:405–410

    Article  Google Scholar 

  9. Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, Goetz CG, Golbe LI, Grafman J, Growdon JH, Hallett M, Jankovic J, Quinn NP, Tolosa E, Zee DS (1996) Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 47:1–9

    Article  CAS  Google Scholar 

  10. Kishitani T, Matsunaga A, Ikawa M, Hayashi K, Yamamura O, Hamano T, Watanabe O, Tanaka K, Nakamoto Y, Yoneda M (2017) Limbic encephalitis associated with anti-NH2-terminal of alpha-enolase antibodies: a clinical subtype of Hashimoto encephalopathy. Medicine 96:e6181

    Article  CAS  Google Scholar 

  11. Dahm L, Ott C, Steiner J, Stepniak B, Teegen B, Saschenbrecker S, Hammer C, Borowski K, Begemann M, Lemke S, Rentzsch K, Probst C, Martens H, Wienands J, Spalletta G, Weissenborn K, Stocker W, Ehrenreich H (2014) Seroprevalence of autoantibodies against brain antigens in health and disease. Ann Neurol 76:82–94

    Article  CAS  Google Scholar 

  12. Mattozzi S, Sabater L, Escudero D, Arino H, Armangue T, Simabukuro M, Iizuka T, Hara M, Saiz A, Sotgiu S, Dalmau J, Graus F (2020) Hashimoto encephalopathy in the 21st century. Neurology 94:e217–e224

    Article  CAS  Google Scholar 

  13. Yoneda M, Matsunaga A, Ikawa M (2020) Reader response: Hashimoto encephalopathy in the 21st century. Neurology in press

  14. Montojo MT, Petit-Pedrol M, Graus F, Dalmau J (2015) Clinical spectrum and diagnostic value of antibodies against the potassium channel related protein complex. Neurologia 30:295–301

    Article  CAS  Google Scholar 

  15. Lebioda L, Stec B (1991) Mapping of isozymic differences in enolase. Int J Biol Macromol 13:97–100

    Article  CAS  Google Scholar 

  16. Subramanian A, Miller DM (2000) Structural analysis of alpha-enolase. Mapping the functional domains involved in down-regulation of the c-myc protooncogene. J Biol Chem 275:5958–5965

    Article  CAS  Google Scholar 

  17. Kim KS, Choi YR, Park JY, Lee JH, Kim DK, Lee SJ, Paik SR, Jou I, Park SM (2012) Proteolytic cleavage of extracellular alpha-synuclein by plasmin: implications for Parkinson disease. J Biol Chem 287:24862–24872

    Article  CAS  Google Scholar 

  18. Nakagami Y, Abe K, Nishiyama N, Matsuki N (2000) Laminin degradation by plasmin regulates long-term potentiation. J Neurosci 20:2003–2010

    Article  CAS  Google Scholar 

  19. Matsuda K (2004) Laminin and Alzheimer’s disease. Psychogeriatrics 4:S19–S38

    Article  Google Scholar 

  20. Rifkin DB, Mazzieri R, Munger JS, Noguera I, Sung J (1999) Proteolytic control of growth factor availability. APMIS 107:80–85

    Article  CAS  Google Scholar 

  21. Balsara RD, Ploplis VA (2008) Plasminogen activator inhibitor-1: the double-edged sword in apoptosis. Thromb Haemost 100:1029–1036

    Article  CAS  Google Scholar 

  22. Novak P, Williams A, Ravin P, Zurkiya O, Abduljalil A, Novak V (2012) Treatment of multiple system atrophy using intravenous immunoglobulin. BMC Neurol 12:131

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported in part by a Grant for “the Research Committee for Ataxic Diseases” of the Research on Measures for Intractable Diseases from the Ministry of Health, Labour and Welfare, Japan, and Grants-in-Aid for Scientific Research (C) (20K07923) from the Japan Society for the Promotion of Science, Japan.

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Author notes

  1. Akio Kikuchi and Makoto Yoneda contributed equally to this work.

Authors and Affiliations

  1. Department of Neurology, Tohoku University Graduate School of Medicine, 1-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi, 980-8574, Japan

    Akio Kikuchi, Takafumi Hasegawa, Takaaki Nakamura, Michinori Ezura, Naoto Sugeno, Shun Ishiyama & Masashi Aoki

  2. Faculty of Nursing and Social Welfare Sciences, Fukui Prefectural University, 4-1-1 Kenjojima, Matsuoka, Eiheiji, Fukui, 910-1195, Japan

    Makoto Yoneda

  3. Second Department of Internal Medicine, University of Fukui, Fukui, Japan

    Akiko Matsunaga, Masamichi Ikawa & Yasunari Nakamoto

  4. Department of Neurology, National Hospital Organization, Sendai Nishitaga Hospital, Sendai, Japan

    Toru Baba & Atsushi Takeda

Authors
  1. Akio Kikuchi
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  2. Makoto Yoneda
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  3. Takafumi Hasegawa
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  4. Akiko Matsunaga
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  5. Masamichi Ikawa
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  6. Takaaki Nakamura
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  7. Michinori Ezura
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  8. Toru Baba
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  9. Naoto Sugeno
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  10. Shun Ishiyama
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  11. Yasunari Nakamoto
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  12. Atsushi Takeda
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  13. Masashi Aoki
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Corresponding authors

Correspondence to Akio Kikuchi or Makoto Yoneda.

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The authors declare no financial or other conflicts of interest.

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Kikuchi, A., Yoneda, M., Hasegawa, T. et al. High prevalence of serum anti-NH2-terminal of α-enolase antibodies in patients with multiple system atrophy and corticobasal syndrome. J Neurol 268, 4291–4295 (2021). https://doi.org/10.1007/s00415-021-10553-2

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  • DOI: https://doi.org/10.1007/s00415-021-10553-2

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