Skip to main content
Erschienen in: Journal of Neurology 1/2019

29.05.2018 | Review

Infectious agents and amyotrophic lateral sclerosis: another piece of the puzzle of motor neuron degeneration

verfasst von: David Castanedo-Vazquez, Pilar Bosque-Varela, Arancha Sainz-Pelayo, Javier Riancho

Erschienen in: Journal of Neurology | Ausgabe 1/2019

Einloggen, um Zugang zu erhalten

Abstract

Amyotrophic lateral sclerosis (ALS) is the most common neurodegenerative disease affecting motor neurons (MN). This fatal disease is characterized by progressive muscle wasting and lacks an effective treatment. ALS pathogenesis has not been elucidated yet. In a small proportion of ALS patients, the disease has a familial origin, related to mutations in specific genes, which directly result in MN degeneration. By contrast, the vast majority of cases are though to be sporadic, in which genes and environment interact leading to disease in genetically predisposed individuals. Lately, the role of the environment has gained relevance in this field and an extensive list of environmental conditions have been postulated to be involved in ALS. Among them, infectious agents, particularly viruses, have been suggested to play an important role in the pathogenesis of the disease. These agents could act by interacting with some crucial pathways in MN degeneration, such as gene processing, oxidative stress or neuroinflammation. In this article, we will review the main studies about the involvement of microorganisms in ALS, subsequently discussing their potential pathogenic effect and integrating them as another piece in the puzzle of ALS pathogenesis.
Literatur
1.
Zurück zum Zitat Zufiria M, Gil-Bea FJ, Fernandez-Torron R, Poza JJ, Munoz-Blanco JL, Rojas-Garcia R et al (2016) ALS: a bucket of genes, environment, metabolism and unknown ingredients. Prog Neurobiol 142:104–129PubMedCrossRef Zufiria M, Gil-Bea FJ, Fernandez-Torron R, Poza JJ, Munoz-Blanco JL, Rojas-Garcia R et al (2016) ALS: a bucket of genes, environment, metabolism and unknown ingredients. Prog Neurobiol 142:104–129PubMedCrossRef
2.
Zurück zum Zitat Riancho J, Lozano-Cuesta P, Santurtun A, Sanchez-Juan P, Lopez-Vega JM, Berciano J et al (2016) Amyotrophic lateral sclerosis in northern Spain 40 years later: what has changed? Neurodegener Dis 16(5–6):337–341PubMedCrossRef Riancho J, Lozano-Cuesta P, Santurtun A, Sanchez-Juan P, Lopez-Vega JM, Berciano J et al (2016) Amyotrophic lateral sclerosis in northern Spain 40 years later: what has changed? Neurodegener Dis 16(5–6):337–341PubMedCrossRef
3.
Zurück zum Zitat Hardiman O, van den Berg LH, Kiernan MC (2011) Clinical diagnosis and management of amyotrophic lateral sclerosis. Nat Rev Neurol 7(11):639–649PubMedCrossRef Hardiman O, van den Berg LH, Kiernan MC (2011) Clinical diagnosis and management of amyotrophic lateral sclerosis. Nat Rev Neurol 7(11):639–649PubMedCrossRef
4.
Zurück zum Zitat Riancho J, Berciano MT, Ruiz-Soto M, Berciano J, Landreth G, Lafarga M (2016) Retinoids and motor neuron disease: potential role in amyotrophic lateral sclerosis. J Neurol Sci 360:115–120PubMedCrossRef Riancho J, Berciano MT, Ruiz-Soto M, Berciano J, Landreth G, Lafarga M (2016) Retinoids and motor neuron disease: potential role in amyotrophic lateral sclerosis. J Neurol Sci 360:115–120PubMedCrossRef
5.
Zurück zum Zitat Al Chalabi A, Hardiman O, Kiernan MC, Chio A, Rix-Brooks B, van den Berg LH (2016) Amyotrophic lateral sclerosis: moving towards a new classification system. Lancet Neurol 15(11):1182–1194PubMedCrossRef Al Chalabi A, Hardiman O, Kiernan MC, Chio A, Rix-Brooks B, van den Berg LH (2016) Amyotrophic lateral sclerosis: moving towards a new classification system. Lancet Neurol 15(11):1182–1194PubMedCrossRef
7.
Zurück zum Zitat Al Chalabi A, Hardiman O (2013) The epidemiology of ALS: a conspiracy of genes, environment and time. Nat Rev Neurol 9(11):617–628PubMedCrossRef Al Chalabi A, Hardiman O (2013) The epidemiology of ALS: a conspiracy of genes, environment and time. Nat Rev Neurol 9(11):617–628PubMedCrossRef
9.
Zurück zum Zitat Karim S, Mirza Z, Kamal MA, Abuzenadah AM, Azhar EI, Al Qahtani MH et al (2014) The role of viruses in neurodegenerative and neurobehavioral diseases. CNS Neurol Disord Drug Targets 13(7):1213–1223PubMedCrossRef Karim S, Mirza Z, Kamal MA, Abuzenadah AM, Azhar EI, Al Qahtani MH et al (2014) The role of viruses in neurodegenerative and neurobehavioral diseases. CNS Neurol Disord Drug Targets 13(7):1213–1223PubMedCrossRef
10.
Zurück zum Zitat Babiker A, Jeudy J, Kligerman S, Khambaty M, Shah A, Bagchi S (2017) Risk of cardiovascular disease due to chronic hepatitis c infection: a review. J Clin Transl Hepatol 5(4):343–362PubMedPubMedCentral Babiker A, Jeudy J, Kligerman S, Khambaty M, Shah A, Bagchi S (2017) Risk of cardiovascular disease due to chronic hepatitis c infection: a review. J Clin Transl Hepatol 5(4):343–362PubMedPubMedCentral
12.
Zurück zum Zitat Araujo AQ (2015) Update on neurological manifestations of HTLV-1 infection. Curr Infect Dis Rep 17(2):459PubMedCrossRef Araujo AQ (2015) Update on neurological manifestations of HTLV-1 infection. Curr Infect Dis Rep 17(2):459PubMedCrossRef
14.
Zurück zum Zitat Bowen LN, Tyagi R, Li W, Alfahad T, Smith B, Wright M et al (2016) HIV-associated motor neuron disease: HERV-K activation and response to antiretroviral therapy. Neurology 87(17):1756–1762PubMedPubMedCentralCrossRef Bowen LN, Tyagi R, Li W, Alfahad T, Smith B, Wright M et al (2016) HIV-associated motor neuron disease: HERV-K activation and response to antiretroviral therapy. Neurology 87(17):1756–1762PubMedPubMedCentralCrossRef
15.
Zurück zum Zitat Rowland LP (2011) HIV-related neuromuscular diseases: nemaline myopathy, amyotrophic lateral sclerosis and bibrachial amyotrophic diplegia. Acta Myol 30(1):29–31PubMedPubMedCentral Rowland LP (2011) HIV-related neuromuscular diseases: nemaline myopathy, amyotrophic lateral sclerosis and bibrachial amyotrophic diplegia. Acta Myol 30(1):29–31PubMedPubMedCentral
16.
Zurück zum Zitat McCormick AL, Brown RH Jr, Cudkowicz ME, Al Chalabi A, Garson JA (2008) Quantification of reverse transcriptase in ALS and elimination of a novel retroviral candidate. Neurology 70(4):278–283PubMedCrossRef McCormick AL, Brown RH Jr, Cudkowicz ME, Al Chalabi A, Garson JA (2008) Quantification of reverse transcriptase in ALS and elimination of a novel retroviral candidate. Neurology 70(4):278–283PubMedCrossRef
17.
Zurück zum Zitat Verma A, Berger JR (2006) ALS syndrome in patients with HIV-1 infection. J Neurol Sci 240(1–2):59–64PubMedCrossRef Verma A, Berger JR (2006) ALS syndrome in patients with HIV-1 infection. J Neurol Sci 240(1–2):59–64PubMedCrossRef
18.
Zurück zum Zitat Bastos AF, Orsini M, Machado D, Mello MP, Nader S, Silva JG et al (2011) Amyotrophic lateral sclerosis: one or multiple causes? Neurol Int 3(1):e4PubMedPubMedCentralCrossRef Bastos AF, Orsini M, Machado D, Mello MP, Nader S, Silva JG et al (2011) Amyotrophic lateral sclerosis: one or multiple causes? Neurol Int 3(1):e4PubMedPubMedCentralCrossRef
19.
Zurück zum Zitat Louboutin JP, Strayer D (2014) Role of oxidative stress in HIV-1-associated neurocognitive disorder and protection by gene delivery of antioxidant enzymes. Antioxidants (Basel) 3(4):770–797CrossRef Louboutin JP, Strayer D (2014) Role of oxidative stress in HIV-1-associated neurocognitive disorder and protection by gene delivery of antioxidant enzymes. Antioxidants (Basel) 3(4):770–797CrossRef
20.
Zurück zum Zitat Regulier EG, Reiss K, Khalili K, Amini S, Zagury JF, Katsikis PD et al (2004) T-cell and neuronal apoptosis in HIV infection: implications for therapeutic intervention. Int Rev Immunol 23(1–2):25–59PubMedCrossRef Regulier EG, Reiss K, Khalili K, Amini S, Zagury JF, Katsikis PD et al (2004) T-cell and neuronal apoptosis in HIV infection: implications for therapeutic intervention. Int Rev Immunol 23(1–2):25–59PubMedCrossRef
21.
22.
Zurück zum Zitat Westarp ME, Ferrante P, Perron H, Bartmann P, Kornhuber HH (1995) Sporadic ALS/MND: a global neurodegeneration with retroviral involvement? J Neurol Sci 129(Suppl):145–147PubMedCrossRef Westarp ME, Ferrante P, Perron H, Bartmann P, Kornhuber HH (1995) Sporadic ALS/MND: a global neurodegeneration with retroviral involvement? J Neurol Sci 129(Suppl):145–147PubMedCrossRef
23.
Zurück zum Zitat Alkhawajah NM, Chapman KM, Moore GR, Oger J (2015) Amyotrophic lateral sclerosis presentation of a human T-lymphotropic virus type-1 myelopathy-insight into pathogenesis. APMIS 123(9):815–820PubMedCrossRef Alkhawajah NM, Chapman KM, Moore GR, Oger J (2015) Amyotrophic lateral sclerosis presentation of a human T-lymphotropic virus type-1 myelopathy-insight into pathogenesis. APMIS 123(9):815–820PubMedCrossRef
24.
Zurück zum Zitat Dekaban GA, Hudson AJ, Rice GP (1992) Absence of HTLV-I and HTLV-II proviral genome in the brains of patients with multiple sclerosis and amyotrophic lateral sclerosis. Can J Neurol Sci 19(4):458–461PubMedCrossRef Dekaban GA, Hudson AJ, Rice GP (1992) Absence of HTLV-I and HTLV-II proviral genome in the brains of patients with multiple sclerosis and amyotrophic lateral sclerosis. Can J Neurol Sci 19(4):458–461PubMedCrossRef
25.
Zurück zum Zitat Silva MT, Leite AC, Alamy AH, Chimelli L, Andrada-Serpa MJ, Araujo AQ (2005) ALS syndrome in HTLV-I infection. Neurology 65(8):1332–1333PubMedCrossRef Silva MT, Leite AC, Alamy AH, Chimelli L, Andrada-Serpa MJ, Araujo AQ (2005) ALS syndrome in HTLV-I infection. Neurology 65(8):1332–1333PubMedCrossRef
26.
Zurück zum Zitat Brutting C, Emmer A, Kornhuber ME, Staege MS (2017) Cooccurrences of putative endogenous retrovirus-associated diseases. Biomed Res Int 2017:7973165PubMedPubMedCentralCrossRef Brutting C, Emmer A, Kornhuber ME, Staege MS (2017) Cooccurrences of putative endogenous retrovirus-associated diseases. Biomed Res Int 2017:7973165PubMedPubMedCentralCrossRef
27.
Zurück zum Zitat Brown RH Jr, Al Chalabi A (2015) Endogenous retroviruses in ALS: a reawakening? Sci Transl Med 7(307):307fs40PubMedCrossRef Brown RH Jr, Al Chalabi A (2015) Endogenous retroviruses in ALS: a reawakening? Sci Transl Med 7(307):307fs40PubMedCrossRef
28.
Zurück zum Zitat Douville R, Liu J, Rothstein J, Nath A (2011) Identification of active loci of a human endogenous retrovirus in neurons of patients with amyotrophic lateral sclerosis. Ann Neurol 69(1):141–151PubMedPubMedCentralCrossRef Douville R, Liu J, Rothstein J, Nath A (2011) Identification of active loci of a human endogenous retrovirus in neurons of patients with amyotrophic lateral sclerosis. Ann Neurol 69(1):141–151PubMedPubMedCentralCrossRef
29.
Zurück zum Zitat Li W, Lee MH, Henderson L, Tyagi R, Bachani M, Steiner J et al (2015) Human endogenous retrovirus-K contributes to motor neuron disease. Sci Transl Med 7(307):307ra153PubMedPubMedCentralCrossRef Li W, Lee MH, Henderson L, Tyagi R, Bachani M, Steiner J et al (2015) Human endogenous retrovirus-K contributes to motor neuron disease. Sci Transl Med 7(307):307ra153PubMedPubMedCentralCrossRef
30.
Zurück zum Zitat Bhat RK, Rudnick W, Antony JM, Maingat F, Ellestad KK, Wheatley BM et al (2014) Human endogenous retrovirus-K(II) envelope induction protects neurons during HIV/AIDS. PLoS One 9(7):e97984PubMedPubMedCentralCrossRef Bhat RK, Rudnick W, Antony JM, Maingat F, Ellestad KK, Wheatley BM et al (2014) Human endogenous retrovirus-K(II) envelope induction protects neurons during HIV/AIDS. PLoS One 9(7):e97984PubMedPubMedCentralCrossRef
31.
Zurück zum Zitat Contreras-Galindo R, Gonzalez M, Almodovar-Camacho S, Gonzalez-Ramirez S, Lorenzo E, Yamamura Y (2006) A new real-time-RT-PCR for quantitation of human endogenous retroviruses type K (HERV-K) RNA load in plasma samples: increased HERV-K RNA titers in HIV-1 patients with HAART non-suppressive regimens. J Virol Methods 136(1–2):51–57PubMedCrossRef Contreras-Galindo R, Gonzalez M, Almodovar-Camacho S, Gonzalez-Ramirez S, Lorenzo E, Yamamura Y (2006) A new real-time-RT-PCR for quantitation of human endogenous retroviruses type K (HERV-K) RNA load in plasma samples: increased HERV-K RNA titers in HIV-1 patients with HAART non-suppressive regimens. J Virol Methods 136(1–2):51–57PubMedCrossRef
32.
Zurück zum Zitat Li W, Li G, Steiner J, Nath A (2009) Role of Tat protein in HIV neuropathogenesis. Neurotox Res 16(3):205–220PubMedCrossRef Li W, Li G, Steiner J, Nath A (2009) Role of Tat protein in HIV neuropathogenesis. Neurotox Res 16(3):205–220PubMedCrossRef
33.
Zurück zum Zitat Wurdinger T, Gatson NN, Balaj L, Kaur B, Breakefield XO, Pegtel DM (2012) Extracellular vesicles and their convergence with viral pathways. Adv Virol 2012:767694PubMedPubMedCentralCrossRef Wurdinger T, Gatson NN, Balaj L, Kaur B, Breakefield XO, Pegtel DM (2012) Extracellular vesicles and their convergence with viral pathways. Adv Virol 2012:767694PubMedPubMedCentralCrossRef
34.
Zurück zum Zitat Ravits J (2005) Sporadic amyotrophic lateral sclerosis: a hypothesis of persistent (non-lytic) enteroviral infection. Amyotroph Lateral Scler Other Motor Neuron Disord 6(2):77–87PubMedCrossRef Ravits J (2005) Sporadic amyotrophic lateral sclerosis: a hypothesis of persistent (non-lytic) enteroviral infection. Amyotroph Lateral Scler Other Motor Neuron Disord 6(2):77–87PubMedCrossRef
35.
Zurück zum Zitat Fung G, Shi J, Deng H, Hou J, Wang C, Hong A et al (2015) Cytoplasmic translocation, aggregation, and cleavage of TDP-43 by enteroviral proteases modulate viral pathogenesis. Cell Death Differ 22(12):2087–2097PubMedPubMedCentralCrossRef Fung G, Shi J, Deng H, Hou J, Wang C, Hong A et al (2015) Cytoplasmic translocation, aggregation, and cleavage of TDP-43 by enteroviral proteases modulate viral pathogenesis. Cell Death Differ 22(12):2087–2097PubMedPubMedCentralCrossRef
36.
Zurück zum Zitat Cermelli C, Vinceti M, Beretti F, Pietrini V, Nacci G, Pietrosemoli P et al (2003) Risk of sporadic amyotrophic lateral sclerosis associated with seropositivity for herpesviruses and echovirus-7. Eur J Epidemiol 18(2):123–127PubMedCrossRef Cermelli C, Vinceti M, Beretti F, Pietrini V, Nacci G, Pietrosemoli P et al (2003) Risk of sporadic amyotrophic lateral sclerosis associated with seropositivity for herpesviruses and echovirus-7. Eur J Epidemiol 18(2):123–127PubMedCrossRef
37.
38.
Zurück zum Zitat Finnen RL, Hay TJ, Dauber B, Smiley JR, Banfield BW (2014) The herpes simplex virus 2 virion-associated ribonuclease vhs interferes with stress granule formation. J Virol 88(21):12727–12739PubMedPubMedCentralCrossRef Finnen RL, Hay TJ, Dauber B, Smiley JR, Banfield BW (2014) The herpes simplex virus 2 virion-associated ribonuclease vhs interferes with stress granule formation. J Virol 88(21):12727–12739PubMedPubMedCentralCrossRef
39.
Zurück zum Zitat Reed D, Plato C, Elizan T, Kurland LT (1966) The amyotrophic lateral sclerosis/parkinsonism-dementia complex: a ten-year follow-up on Guam. I. Epidemiologic studies. Am J Epidemiol 83(1):54–73PubMedCrossRef Reed D, Plato C, Elizan T, Kurland LT (1966) The amyotrophic lateral sclerosis/parkinsonism-dementia complex: a ten-year follow-up on Guam. I. Epidemiologic studies. Am J Epidemiol 83(1):54–73PubMedCrossRef
40.
Zurück zum Zitat TORRES J, IRIARTE LL, Kurland LT (1957) Amyotrophic lateral sclerosis among Guamanians in California. Calif Med 86(6):385–388PubMedPubMedCentral TORRES J, IRIARTE LL, Kurland LT (1957) Amyotrophic lateral sclerosis among Guamanians in California. Calif Med 86(6):385–388PubMedPubMedCentral
41.
Zurück zum Zitat Reed DM, Brody JA (1975) Amyotrophic lateral sclerosis and parkinsonism-dementia on Guam, 1945–1972. I. Descriptive epidemiology. Am J Epidemiol 101(4):287–301PubMedCrossRef Reed DM, Brody JA (1975) Amyotrophic lateral sclerosis and parkinsonism-dementia on Guam, 1945–1972. I. Descriptive epidemiology. Am J Epidemiol 101(4):287–301PubMedCrossRef
42.
Zurück zum Zitat Murch SJ, Cox PA, Banack SA (2004) A mechanism for slow release of biomagnified cyanobacterial neurotoxins and neurodegenerative disease in Guam. Proc Natl Acad Sci USA 101(33):12228–12231PubMedCrossRef Murch SJ, Cox PA, Banack SA (2004) A mechanism for slow release of biomagnified cyanobacterial neurotoxins and neurodegenerative disease in Guam. Proc Natl Acad Sci USA 101(33):12228–12231PubMedCrossRef
43.
Zurück zum Zitat Murch SJ, Cox PA, Banack SA, Steele JC, Sacks OW (2004) Occurrence of beta-methylamino-l-alanine (BMAA) in ALS/PDC patients from Guam. Acta Neurol Scand 110(4):267–269PubMedCrossRef Murch SJ, Cox PA, Banack SA, Steele JC, Sacks OW (2004) Occurrence of beta-methylamino-l-alanine (BMAA) in ALS/PDC patients from Guam. Acta Neurol Scand 110(4):267–269PubMedCrossRef
44.
Zurück zum Zitat Field NC, Metcalf JS, Caller TA, Banack SA, Cox PA, Stommel EW (2013) Linking beta-methylamino-L-alanine exposure to sporadic amyotrophic lateral sclerosis in Annapolis, MD. Toxicon 70:179–183PubMedCrossRef Field NC, Metcalf JS, Caller TA, Banack SA, Cox PA, Stommel EW (2013) Linking beta-methylamino-L-alanine exposure to sporadic amyotrophic lateral sclerosis in Annapolis, MD. Toxicon 70:179–183PubMedCrossRef
45.
Zurück zum Zitat Caller TA, Chipman JW, Field NC, Stommel EW (2013) Spatial analysis of amyotrophic lateral sclerosis in Northern New England, USA, 1997–2009. Muscle Nerve 48(2):235–241PubMedCrossRef Caller TA, Chipman JW, Field NC, Stommel EW (2013) Spatial analysis of amyotrophic lateral sclerosis in Northern New England, USA, 1997–2009. Muscle Nerve 48(2):235–241PubMedCrossRef
46.
Zurück zum Zitat Lannuzel A, Mecharles S, Tressieres B, Demoly A, Alhendi R, Hedreville-Tablon MA et al (2015) Clinical varieties and epidemiological aspects of amyotrophic lateral sclerosis in the Caribbean island of Guadeloupe: a new focus of ALS associated with Parkinsonism. Amyotroph Lateral Scler Frontotemporal Degener 16(3–4):216–223PubMedCrossRef Lannuzel A, Mecharles S, Tressieres B, Demoly A, Alhendi R, Hedreville-Tablon MA et al (2015) Clinical varieties and epidemiological aspects of amyotrophic lateral sclerosis in the Caribbean island of Guadeloupe: a new focus of ALS associated with Parkinsonism. Amyotroph Lateral Scler Frontotemporal Degener 16(3–4):216–223PubMedCrossRef
47.
Zurück zum Zitat Masseret E, Banack S, Boumediene F, Abadie E, Brient L, Pernet F et al (2013) Dietary BMAA exposure in an amyotrophic lateral sclerosis cluster from southern France. PLoS One 8(12):e83406PubMedPubMedCentralCrossRef Masseret E, Banack S, Boumediene F, Abadie E, Brient L, Pernet F et al (2013) Dietary BMAA exposure in an amyotrophic lateral sclerosis cluster from southern France. PLoS One 8(12):e83406PubMedPubMedCentralCrossRef
48.
Zurück zum Zitat Spencer PS, Roy DN, Ludolph A, Hugon J, Dwivedi MP, Schaumburg HH (1986) Lathyrism: evidence for role of the neuroexcitatory aminoacid BOAA. Lancet 2(8515):1066–1067PubMedCrossRef Spencer PS, Roy DN, Ludolph A, Hugon J, Dwivedi MP, Schaumburg HH (1986) Lathyrism: evidence for role of the neuroexcitatory aminoacid BOAA. Lancet 2(8515):1066–1067PubMedCrossRef
49.
Zurück zum Zitat Lobner D, Piana PM, Salous AK, Peoples RW (2007) Beta-N-methylamino-l-alanine enhances neurotoxicity through multiple mechanisms. Neurobiol Dis 25(2):360–366PubMedCrossRef Lobner D, Piana PM, Salous AK, Peoples RW (2007) Beta-N-methylamino-l-alanine enhances neurotoxicity through multiple mechanisms. Neurobiol Dis 25(2):360–366PubMedCrossRef
50.
Zurück zum Zitat Bradley WG, Mash DC (2009) Beyond Guam: the cyanobacteria/BMAA hypothesis of the cause of ALS and other neurodegenerative diseases. Amyotroph Lateral Scler 10(Suppl 2):7–20PubMedCrossRef Bradley WG, Mash DC (2009) Beyond Guam: the cyanobacteria/BMAA hypothesis of the cause of ALS and other neurodegenerative diseases. Amyotroph Lateral Scler 10(Suppl 2):7–20PubMedCrossRef
51.
Zurück zum Zitat Chernoff N, Hill DJ, Diggs DL, Faison BD, Francis BM, Lang JR et al (2017) A critical review of the postulated role of the non-essential amino acid, beta-N-methylamino-l-alanine, in neurodegenerative disease in humans. J Toxicol Environ Health B Crit Rev 20(4):1–47PubMedPubMedCentralCrossRef Chernoff N, Hill DJ, Diggs DL, Faison BD, Francis BM, Lang JR et al (2017) A critical review of the postulated role of the non-essential amino acid, beta-N-methylamino-l-alanine, in neurodegenerative disease in humans. J Toxicol Environ Health B Crit Rev 20(4):1–47PubMedPubMedCentralCrossRef
52.
Zurück zum Zitat Bradley WG (2015) The John Walton Muscular Dystrophy Research Centre in the University of Newcastle and the BMAA theory of motor neuron disease. J Neuromuscul Dis 2(s2):S77–S81PubMedPubMedCentralCrossRef Bradley WG (2015) The John Walton Muscular Dystrophy Research Centre in the University of Newcastle and the BMAA theory of motor neuron disease. J Neuromuscul Dis 2(s2):S77–S81PubMedPubMedCentralCrossRef
53.
Zurück zum Zitat Sieh W, Choi Y, Chapman NH, Craig UK, Steinbart EJ, Rothstein JH et al (2009) Identification of novel susceptibility loci for Guam neurodegenerative disease: challenges of genome scans in genetic isolates. Hum Mol Genet 18(19):3725–3738PubMedPubMedCentralCrossRef Sieh W, Choi Y, Chapman NH, Craig UK, Steinbart EJ, Rothstein JH et al (2009) Identification of novel susceptibility loci for Guam neurodegenerative disease: challenges of genome scans in genetic isolates. Hum Mol Genet 18(19):3725–3738PubMedPubMedCentralCrossRef
54.
Zurück zum Zitat Burakgazi AZ (2014) Lyme disease-induced polyradiculopathy mimicking amyotrophic lateral sclerosis. Int J Neurosci 124(11):859–862PubMedCrossRef Burakgazi AZ (2014) Lyme disease-induced polyradiculopathy mimicking amyotrophic lateral sclerosis. Int J Neurosci 124(11):859–862PubMedCrossRef
55.
Zurück zum Zitat Hemmer B, Glocker FX, Kaiser R, Lucking CH, Deuschl G (1997) Generalised motor neuron disease as an unusual manifestation of Borrelia burgdorferi infection. J Neurol Neurosurg Psychiatry 63(2):257–258PubMedPubMedCentralCrossRef Hemmer B, Glocker FX, Kaiser R, Lucking CH, Deuschl G (1997) Generalised motor neuron disease as an unusual manifestation of Borrelia burgdorferi infection. J Neurol Neurosurg Psychiatry 63(2):257–258PubMedPubMedCentralCrossRef
56.
Zurück zum Zitat Visser AE, Verduyn Lunel FM, Veldink JH, van den Berg LH (2017) No association between Borrelia burgdorferi antibodies and amyotrophic lateral sclerosis in a case-control study. Eur J Neurol 24(1):227–230PubMedCrossRef Visser AE, Verduyn Lunel FM, Veldink JH, van den Berg LH (2017) No association between Borrelia burgdorferi antibodies and amyotrophic lateral sclerosis in a case-control study. Eur J Neurol 24(1):227–230PubMedCrossRef
57.
Zurück zum Zitat Qureshi M, Bedlack RS, Cudkowicz ME (2009) Lyme disease serology in amyotrophic lateral sclerosis. Muscle Nerve 40(4):626–628PubMedCrossRef Qureshi M, Bedlack RS, Cudkowicz ME (2009) Lyme disease serology in amyotrophic lateral sclerosis. Muscle Nerve 40(4):626–628PubMedCrossRef
58.
Zurück zum Zitat Lynch SV, Pedersen O (2016) The human intestinal microbiome in health and disease. N Engl J Med 375(24):2369–2379PubMedCrossRef Lynch SV, Pedersen O (2016) The human intestinal microbiome in health and disease. N Engl J Med 375(24):2369–2379PubMedCrossRef
59.
Zurück zum Zitat Rhee SH, Pothoulakis C, Mayer EA (2009) Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat Rev Gastroenterol Hepatol 6(5):306–314PubMedCrossRef Rhee SH, Pothoulakis C, Mayer EA (2009) Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat Rev Gastroenterol Hepatol 6(5):306–314PubMedCrossRef
60.
Zurück zum Zitat Westfall S, Lomis N, Kahouli I, Dia SY, Singh SP, Prakash S (2017) Microbiome, probiotics and neurodegenerative diseases: deciphering the gut brain axis. Cell Mol Life Sci 74(20):3769–3787PubMedCrossRef Westfall S, Lomis N, Kahouli I, Dia SY, Singh SP, Prakash S (2017) Microbiome, probiotics and neurodegenerative diseases: deciphering the gut brain axis. Cell Mol Life Sci 74(20):3769–3787PubMedCrossRef
61.
Zurück zum Zitat Dobashi Y, Yoshimura H, Atarashi E, Takahashi K, Tohei A, Amao H (2013) Upregulation of superoxide dismutase activity in the intestinal tract mucosa of germ-free mice. J Vet Med Sci 75(1):49–54PubMedCrossRef Dobashi Y, Yoshimura H, Atarashi E, Takahashi K, Tohei A, Amao H (2013) Upregulation of superoxide dismutase activity in the intestinal tract mucosa of germ-free mice. J Vet Med Sci 75(1):49–54PubMedCrossRef
62.
Zurück zum Zitat Dobashi Y, Itoh K, Tohei A, Amao H (2014) Screening for intestinal microflora influencing superoxide dismutase activity in mouse cecal mucosa. J Vet Med Sci 76(3):453–456PubMedCrossRef Dobashi Y, Itoh K, Tohei A, Amao H (2014) Screening for intestinal microflora influencing superoxide dismutase activity in mouse cecal mucosa. J Vet Med Sci 76(3):453–456PubMedCrossRef
63.
Zurück zum Zitat Wu S, Yi J, Zhang YG, Zhou J, Sun J (2015) Leaky intestine and impaired microbiome in an amyotrophic lateral sclerosis mouse model. Physiol Rep 3(4):1–10CrossRef Wu S, Yi J, Zhang YG, Zhou J, Sun J (2015) Leaky intestine and impaired microbiome in an amyotrophic lateral sclerosis mouse model. Physiol Rep 3(4):1–10CrossRef
64.
Zurück zum Zitat Zhang YG, Wu S, Yi J, Xia Y, Jin D, Zhou J et al (2017) Target intestinal microbiota to alleviate disease progression in amyotrophic lateral sclerosis. Clin Ther 39(2):322–336PubMedPubMedCentralCrossRef Zhang YG, Wu S, Yi J, Xia Y, Jin D, Zhou J et al (2017) Target intestinal microbiota to alleviate disease progression in amyotrophic lateral sclerosis. Clin Ther 39(2):322–336PubMedPubMedCentralCrossRef
65.
Zurück zum Zitat Fang X, Wang X, Yang S, Meng F, Wang X, Wei H et al (2016) Evaluation of the microbial diversity in amyotrophic lateral sclerosis using high-throughput sequencing. Front Microbiol 7:1479PubMedPubMedCentral Fang X, Wang X, Yang S, Meng F, Wang X, Wei H et al (2016) Evaluation of the microbial diversity in amyotrophic lateral sclerosis using high-throughput sequencing. Front Microbiol 7:1479PubMedPubMedCentral
66.
Zurück zum Zitat Brenner D, Hiergeist A, Adis C, Mayer B, Gessner A, Ludolph AC et al (2018) The fecal microbiome of ALS patients. Neurobiol Aging 61:132–137PubMedCrossRef Brenner D, Hiergeist A, Adis C, Mayer B, Gessner A, Ludolph AC et al (2018) The fecal microbiome of ALS patients. Neurobiol Aging 61:132–137PubMedCrossRef
67.
Zurück zum Zitat Nicolson GL, Nasralla MY, Haier J, Pomfret J (2002) High frequency of systemic mycoplasmal infections in Gulf War veterans and civilians with amyotrophic lateral sclerosis (ALS). J Clin Neurosci 9(5):525–529PubMedCrossRef Nicolson GL, Nasralla MY, Haier J, Pomfret J (2002) High frequency of systemic mycoplasmal infections in Gulf War veterans and civilians with amyotrophic lateral sclerosis (ALS). J Clin Neurosci 9(5):525–529PubMedCrossRef
68.
Zurück zum Zitat Flores-Rio de la Loza LJ, Ordonez-Lozano G, Pineda-Olvera B (2005) Determination of systemic infections due to mycoplasma in patients with clinically defined amyotrophic lateral sclerosis. Rev Neurol 41(5):262–267 Flores-Rio de la Loza LJ, Ordonez-Lozano G, Pineda-Olvera B (2005) Determination of systemic infections due to mycoplasma in patients with clinically defined amyotrophic lateral sclerosis. Rev Neurol 41(5):262–267
69.
Zurück zum Zitat Hibbett DS, Taylor JW (2013) Fungal systematics: is a new age of enlightenment at hand? Nat Rev Microbiol 11(2):129–133PubMedCrossRef Hibbett DS, Taylor JW (2013) Fungal systematics: is a new age of enlightenment at hand? Nat Rev Microbiol 11(2):129–133PubMedCrossRef
70.
Zurück zum Zitat Wainwright M (2003) An alternative view of the early history of microbiology. Adv Appl Microbiol 52:333–355PubMedCrossRef Wainwright M (2003) An alternative view of the early history of microbiology. Adv Appl Microbiol 52:333–355PubMedCrossRef
71.
Zurück zum Zitat Baxi SN, Portnoy JM, Larenas-Linnemann D, Phipatanakul W (2016) Exposure and health effects of fungi on humans. J Allergy Clin Immunol Pract 4(3):396–404PubMedPubMedCentralCrossRef Baxi SN, Portnoy JM, Larenas-Linnemann D, Phipatanakul W (2016) Exposure and health effects of fungi on humans. J Allergy Clin Immunol Pract 4(3):396–404PubMedPubMedCentralCrossRef
72.
Zurück zum Zitat Pisa D, Alonso R, Carrasco L (2011) Fungal infection in a patient with multiple sclerosis. Eur J Clin Microbiol Infect Dis 30(10):1173–1180PubMedCrossRef Pisa D, Alonso R, Carrasco L (2011) Fungal infection in a patient with multiple sclerosis. Eur J Clin Microbiol Infect Dis 30(10):1173–1180PubMedCrossRef
73.
Zurück zum Zitat Pisa D, Alonso R, Juarranz A, Rabano A, Carrasco L (2015) Direct visualization of fungal infection in brains from patients with Alzheimer’s disease. J Alzheimers Dis 43(2):613–624PubMedCrossRef Pisa D, Alonso R, Juarranz A, Rabano A, Carrasco L (2015) Direct visualization of fungal infection in brains from patients with Alzheimer’s disease. J Alzheimers Dis 43(2):613–624PubMedCrossRef
74.
Zurück zum Zitat Pisa D, Alonso R, Jimenez-Jimenez FJ, Carrasco L (2013) Fungal infection in cerebrospinal fluid from some patients with multiple sclerosis. Eur J Clin Microbiol Infect Dis 32(6):795–801PubMedCrossRef Pisa D, Alonso R, Jimenez-Jimenez FJ, Carrasco L (2013) Fungal infection in cerebrospinal fluid from some patients with multiple sclerosis. Eur J Clin Microbiol Infect Dis 32(6):795–801PubMedCrossRef
75.
Zurück zum Zitat Alonso R, Pisa D, Marina AI, Morato E, Rabano A, Rodal I et al (2015) Evidence for fungal infection in cerebrospinal fluid and brain tissue from patients with amyotrophic lateral sclerosis. Int J Biol Sci 11(5):546–558PubMedPubMedCentralCrossRef Alonso R, Pisa D, Marina AI, Morato E, Rabano A, Rodal I et al (2015) Evidence for fungal infection in cerebrospinal fluid and brain tissue from patients with amyotrophic lateral sclerosis. Int J Biol Sci 11(5):546–558PubMedPubMedCentralCrossRef
76.
Zurück zum Zitat Alonso R, Pisa D, Fernandez-Fernandez AM, Rabano A, Carrasco L (2017) Fungal infection in neural tissue of patients with amyotrophic lateral sclerosis. Neurobiol Dis 108:249–260PubMedCrossRef Alonso R, Pisa D, Fernandez-Fernandez AM, Rabano A, Carrasco L (2017) Fungal infection in neural tissue of patients with amyotrophic lateral sclerosis. Neurobiol Dis 108:249–260PubMedCrossRef
77.
Zurück zum Zitat Hooten KG, Beers DR, Zhao W, Appel SH (2015) Protective and toxic neuroinflammation in amyotrophic lateral sclerosis. Neurotherapeutics 12(2):364–375PubMedPubMedCentralCrossRef Hooten KG, Beers DR, Zhao W, Appel SH (2015) Protective and toxic neuroinflammation in amyotrophic lateral sclerosis. Neurotherapeutics 12(2):364–375PubMedPubMedCentralCrossRef
78.
Zurück zum Zitat Carvalho A, Cunha C, Pasqualotto AC, Pitzurra L, Denning DW, Romani L (2010) Genetic variability of innate immunity impacts human susceptibility to fungal diseases. Int J Infect Dis 14(6):e460–e468PubMedCrossRef Carvalho A, Cunha C, Pasqualotto AC, Pitzurra L, Denning DW, Romani L (2010) Genetic variability of innate immunity impacts human susceptibility to fungal diseases. Int J Infect Dis 14(6):e460–e468PubMedCrossRef
79.
Zurück zum Zitat Harvey WT, Martz D (2007) Motor neuron disease recovery associated with IV ceftriaxone and anti-Babesia therapy. Acta Neurol Scand 115(2):129–131PubMedCrossRef Harvey WT, Martz D (2007) Motor neuron disease recovery associated with IV ceftriaxone and anti-Babesia therapy. Acta Neurol Scand 115(2):129–131PubMedCrossRef
80.
Zurück zum Zitat Robberecht W, Philips T (2013) The changing scene of amyotrophic lateral sclerosis. Nat Rev Neurosci 14(4):248–264PubMedCrossRef Robberecht W, Philips T (2013) The changing scene of amyotrophic lateral sclerosis. Nat Rev Neurosci 14(4):248–264PubMedCrossRef
Metadaten
Titel
Infectious agents and amyotrophic lateral sclerosis: another piece of the puzzle of motor neuron degeneration
verfasst von
David Castanedo-Vazquez
Pilar Bosque-Varela
Arancha Sainz-Pelayo
Javier Riancho
Publikationsdatum
29.05.2018
Verlag
Springer Berlin Heidelberg
Erschienen in
Journal of Neurology / Ausgabe 1/2019
Print ISSN: 0340-5354
Elektronische ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-018-8919-3

Weitere Artikel der Ausgabe 1/2019

Journal of Neurology 1/2019 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.