Brain structure and structural basis of neurodegenerative diseases

Jiawen Yang; Sen-Fang Sui; Zheng Liu

doi:10.52601/bpr.2022.220013

Volume 8 Issue 3

Jun. 2022

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Jiawen Yang, Sen-Fang Sui, Zheng Liu. Brain structure and structural basis of neurodegenerative diseases[J]. Biophysics Reports, 2022, 8(3): 170-181. doi: 10.52601/bpr.2022.220013

Citation:

Jiawen Yang, Sen-Fang Sui, Zheng Liu. Brain structure and structural basis of neurodegenerative diseases[J]. Biophysics Reports, 2022, 8(3): 170-181. doi: 10.52601/bpr.2022.220013

Jiawen Yang, Sen-Fang Sui, Zheng Liu. Brain structure and structural basis of neurodegenerative diseases[J]. Biophysics Reports, 2022, 8(3): 170-181. doi: 10.52601/bpr.2022.220013

Citation:

Jiawen Yang, Sen-Fang Sui, Zheng Liu. Brain structure and structural basis of neurodegenerative diseases[J]. Biophysics Reports, 2022, 8(3): 170-181. doi: 10.52601/bpr.2022.220013

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Brain structure and structural basis of neurodegenerative diseases

doi: 10.52601/bpr.2022.220013

Jiawen Yang^{1, 2},
Sen-Fang Sui^{2, 3},
Zheng Liu^{1
,
,}

1.
Cryo-electron Microscopy Center, Southern University of Science and Technology, Shenzhen 518055, Guangdong, China
2.
Department of Biology, Southern University of Science and Technology, Shenzhen 518055, Guangdong, China
3.
State Key Laboratory of Membrane Biology, Beijing Advanced Innovation Center for Structural Biology, Beijing Frontier Research Center for Biological Structure, School of Life Sciences, Tsinghua University, Beijing 100084, China

More Information

Corresponding author: liuz3@sustech.edu.cn (Z. Liu)
Received Date: 20 June 2022
Accepted Date: 07 July 2022

Available Online: 24 August 2022

Publish Date: 22 June 2022

Abstract

Abstract

The brain is one of the most complex organs in nature. In this organ, multiple neurons, neuron clusters, or multiple brain regions are interconnected to form a complex structural network where various brain functions are completed through interaction. In recent years, multiple tools and techniques have been developed to analyze the composition of different cell types in the brain and to construct the brain atlas on macroscopic, mesoscopic, and microscopic levels. Meanwhile, researchers have found that many neuropsychiatric diseases, such as Parkinson’s disease, Alzheimer’s disease, and Huntington’s disease, are closely related to abnormal changes of brain structure, which means the investigation in brain structure not only provides a new idea for understanding the pathological mechanism of the diseases, but also provides imaging markers for early diagnosis and potential treatment. This article pays attention to the research of human brain structure, reviews the research progress of human brain structure and the structural mechanism of neurodegenerative diseases, and discusses the problems and prospects in the field.
- Brain atlas,
- Brain ultrastructure,
- Neurodegenerative disease,
- Parkinson’s disease,
- Alzheimer’s disease,
- Huntington’s disease

Jiawen Yang, Sen-fang Sui and Zheng Liu declare that they have no conflict of interest.
This article does not contain any studies with human or animal subjects performed by any of the authors.

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References(98)

References

Aamodt EJ, Williams RC Jr (1984) Microtubule-associated proteins connect microtubules and neurofilaments in vitro. Biochemistry 23: 6023−6031 doi: 10.1021/bi00320a019

Abeliovich A, Gitler AD (2016) Defects in trafficking bridge Parkinson's disease pathology and genetics. Nature 539: 207−216 doi: 10.1038/nature20414

Al-Amoudi A, Norlen LP, Dubochet J (2004) Cryo-electron microscopy of vitreous sections of native biological cells and tissues. J Struct Biol 148: 131−135 doi: 10.1016/j.jsb.2004.03.010

Ando Y, Okada H, Takemura G, Suzuki K, Takada C, Tomita H, Zaikokuji R, Hotta Y, Miyazaki N, Yano H, Muraki I, Kuroda A, Fukuda H, Kawasaki Y, Okamoto H, Kawaguchi T, Watanabe T, Doi T, Yoshida T, Ushikoshi H, Yoshida S, Ogura S (2018) Brain-specific ultrastructure of capillary endothelial glycocalyx and its possible contribution for blood brain barrier. Sci Rep 8: 17523. https://doi.org/10.1038/s41598-018-35976-2

Balestrino R, Schapira AHV (2020) Parkinson disease. Eur J Neurol 27: 27−42 doi: 10.1111/ene.14108

Bäuerlein FJB, Saha I, Mishra A, Kalemanov M, Martínez-Sánchez A, Klein R, Dudanova I, Hipp MS, Hartl FU, Baumeister W, Fernández-Busnadiego R (2017) In situ architecture and cellular interactions of polyQ inclusions. Cell 171: 179−187 doi: 10.1016/j.cell.2017.08.009

Bolós M, Pallas-Bazarra N, Terreros-Roncal J, Perea JR, Jurado-Arjona J, Ávila J, Llorens-Martín M (2017) Soluble Tau has devastating effects on the structural plasticity of hippocampal granule neurons. Transl Psychiatry 7: 1267. https://doi.org/10.1038/s41398-017-0013-6

Briggman KL, Helmstaedter M, Denk W (2011) Wiring specificity in the direction-selectivity circuit of the retina. Nature 471: 183−188 doi: 10.1038/nature09818

Brunello CA, Merezhko M, Uronen RL, Huttunen HJ (2020) Mechanisms of secretion and spreading of pathological tau protein. Cell Mol Life Sci 77: 1721−1744 doi: 10.1007/s00018-019-03349-1

Bullen A, Taylor RR, Kachar B, Moores C, Fleck RA, Forge A (2014) Inner ear tissue preservation by rapid freezing: improving fixation by high-pressure freezing and hybrid methods. Hear Res 315: 49−60 doi: 10.1016/j.heares.2014.06.006

Burgunder J-M (2015) Huntington’s disease: a tutorial review. Chin J Nerv Ment Dis 41: 577−591

Canter RG, Penney J, Tsai LH (2016) The road to restoring neural circuits for the treatment of Alzheimer's disease. Nature 539: 187−196 doi: 10.1038/nature20412

Carew TJ (2000) Behavioral neurobiology: the cellular organization of natural behavior. Sinauer Associates, Inc.

Chan SL, Tan EK (2017) Targeting LRRK2 in Parkinson's disease: an update on recent developments. Expert Opin Ther Targets 21: 601−610 doi: 10.1080/14728222.2017.1323881

Chandra A, Dervenoulas G, Politis M (2019) Magnetic resonance imaging in Alzheimer's disease and mild cognitive impairment. J Neurol 266: 1293−1302 doi: 10.1007/s00415-018-9016-3

Chen J, Marks E, Lai B, Zhang Z, Duce JA, Lam LQ, Volitakis I, Bush AI, Hersch S, Fox JH (2013) Iron accumulates in Huntington's disease neurons: protection by deferoxamine. PLoS One 8: e77023. https://doi.org/10.1371/journal.pone.0077023

Chen L, Wu Z, Hu D, Wang Y, Zhao F, Zhong T, Lin W, Wang L, Li G (2022) A 4D infant brain volumetric atlas based on the UNC/UMN baby connectome project (BCP) cohort. Neuroimage 253: 119097. https://doi.org/10.1016/j.neuroimage.2022.119097

Chen WW, Zhang X, Huang WJ (2016) Role of neuroinflammation in neurodegenerative diseases (Review). Mol Med Rep 13: 3391−3396 doi: 10.3892/mmr.2016.4948

Daneman R, Prat A (2015) The blood-brain barrier. Cold Spring Harb Perspect Biol 7: a020412. https://doi.org/10.1101/cshperspect.a020412

Deniston CK, Salogiannis J, Mathea S, Snead DM, Lahiri I, Matyszewski M, Donosa O, Watanabe R, Böhning J, Shiau AK, Knapp S, Villa E, Reck-Peterson SL, Leschziner AE (2020) Structure of LRRK2 in Parkinson's disease and model for microtubule interaction. Nature 588: 344−349 doi: 10.1038/s41586-020-2673-2

El Hajj H, Savage JC, Bisht K, Parent M, Vallières L, Rivest S, Tremblay M (2019) Ultrastructural evidence of microglial heterogeneity in Alzheimer's disease amyloid pathology. J Neuroinflammation 16: 87. https://doi.org/10.1186/s12974-019-1473-9

Femminella GD, Thayanandan T, Calsolaro V, Komici K, Rengo G, Corbi G, Ferrara N (2018) Imaging and molecular mechanisms of Alzheimer's disease: a review. Int J Mol Sci 19: 3702. https://doi.org/10.3390/ijms19123702

Fernandez-Moran H (1953) A diamond knife for ultrathin sectioning. Exp Cell Res 5: 255−256 doi: 10.1016/0014-4827(53)90112-8

Finkbeiner S (2011) Huntington's disease. Cold Spring Harb Perspect Biol 3: a007476. https://doi.org/10.1101/cshperspect.a007476

Fitzpatrick AWP, Falcon B, He S, Murzin AG, Murshudov G, Garringer HJ, Crowther RA, Ghetti B, Goedert M, Scheres SHW (2017) Cryo-EM structures of tau filaments from Alzheimer's disease. Nature 547: 185−190 doi: 10.1038/nature23002

Friedmann D, Pun A, Adams EL, Lui JH, Kebschull JM, Grutzner SM, Castagnola C, Tessier-Lavigne M, Luo L (2020) Mapping mesoscale axonal projections in the mouse brain using a 3D convolutional network. Proc Natl Acad Sci USA 117: 11068−11075 doi: 10.1073/pnas.1918465117

Gan ZY, Callegari S, Cobbold SA, Cotton TR, Mlodzianoski MJ, Schubert AF, Geoghegan ND, Rogers KL, Leis A, Dewson G, Glukhova A, Komander D (2022) Activation mechanism of PINK1. Nature 602: 328−335 doi: 10.1038/s41586-021-04340-2

Glasser MF, Coalson TS, Robinson EC, Hacker CD, Harwell J, Yacoub E, Ugurbil K, Andersson J, Beckmann CF, Jenkinson M, Smith SM, Van Essen DC (2016) A multi-modal parcellation of human cerebral cortex. Nature 536: 171−178 doi: 10.1038/nature18933

Goedert M, Spillantini MG, Del Tredici K, Braak H (2013) 100 years of Lewy pathology. Nat Rev Neurol 9: 13−24

Goh AM, Wibawa P, Loi SM, Walterfang M, Velakoulis D, Looi JC (2018) Huntington's disease: neuropsychiatric manifestations of Huntington's disease. Australas Psychiatry 26: 366−375 doi: 10.1177/1039856218791036

Gómez-Benito M, Granado N, García-Sanz P, Michel A, Dumoulin M, Moratalla R (2020) Modeling Parkinson's disease with the alpha-synuclein protein. Front Pharmacol 11: 356. https://doi.org/10.3389/fphar.2020.00356

Gong H, Xu D, Yuan J, Li X, Guo C, Peng J, Li Y, Schwarz LA, Li A, Hu B, Xiong B, Sun Q, Zhang Y, Liu J, Zhong Q, Xu T, Zeng S, Luo Q (2016) High-throughput dual-colour precision imaging for brain-wide connectome with cytoarchitectonic landmarks at the cellular level. Nat Commun 7: 12142. https://doi.org/10.1038/ncomms12142

Gremer L, Schölzel D, Schenk C, Reinartz E, Labahn J, Ravelli RBG, Tusche M, Lopez-Iglesias C, Hoyer W, Heise H, Willbold D, Schröder GF (2017) Fibril structure of amyloid-β(1-42) by cryo-electron microscopy. Science 358: 116−119 doi: 10.1126/science.aao2825

Guo Q, Bin H, Cheng J, Seefelder M, Engler T, Pfeifer G, Oeckl P, Otto M, Moser F, Maurer M, Pautsch A, Baumeister W, Fernández-Busnadiego R, Kochanek S (2018) The cryo-electron microscopy structure of huntingtin. Nature 555: 117−120 doi: 10.1038/nature25502

Henderson MX, Trojanowski JQ, Lee VM (2019) α-Synuclein pathology in Parkinson's disease and related α-synucleinopathies. Neurosci Lett 709: 134316. https://doi.org/10.1016/j.neulet.2019.134316

Henmar S, Simonsen EB, Berg RW (2020) What are the gray and white matter volumes of the human spinal cord? J Neurophysiol 124: 1792−1797

Jarrell TA, Wang Y, Bloniarz AE, Brittin CA, Xu M, Thomson JN, Albertson DG, Hall DH, Emmons SW (2012) The connectome of a decision-making neural network. Science 337: 437−444 doi: 10.1126/science.1221762

Jia L, Du Y, Chu L, Zhang Z, Li F, Lyu D, Li Y, Li Y, Zhu M, Jiao H, Song Y, Shi Y, Zhang H, Gong M, Wei C, Tang Y, Fang B, Guo D, Wang F, Zhou A, Chu C, Zuo X, Yu Y, Yuan Q, Wang W, Li F, Shi S, Yang H, Zhou C, Liao Z, Lv Y, Li Y, Kan M, Zhao H, Wang S, Yang S, Li H, Liu Z, Wang Q, Qin W, Jia J (2020) Prevalence, risk factors, and management of dementia and mild cognitive impairment in adults aged 60 years or older in China: a cross-sectional study. Lancet Public Health 5: e661−e671 doi: 10.1016/S2468-2667(20)30185-7

Jucker M, Walker LC (2013) Self-propagation of pathogenic protein aggregates in neurodegenerative diseases. Nature 501: 45−51 doi: 10.1038/nature12481

Kalia LV, Lang AE (2015) Parkinson's disease. Lancet 386: 896−912 doi: 10.1016/S0140-6736(14)61393-3

Ke PC, Zhou R, Serpell LC, Riek R, Knowles TPJ, Lashuel HA, Gazit E, Hamley IW, Davis TP, Fändrich M, Otzen DE, Chapman MR, Dobson CM, Eisenberg DS, Mezzenga R (2020) Half a century of amyloids: past, present and future. Chem Soc Rev 49: 5473−5509 doi: 10.1039/C9CS00199A

Kegel-Gleason KB (2013) Huntingtin interactions with membrane phospholipids: strategic targets for therapeutic intervention? J Huntingtons Dis 2: 239-250

Kim MS, Kim Y, Choi H, Kim W, Park S, Lee D, Kim DK, Kim HJ, Choi H, Hyun DW, Lee JY, Choi EY, Lee DS, Bae JW, Mook-Jung I (2020) Transfer of a healthy microbiota reduces amyloid and tau pathology in an Alzheimer's disease animal model. Gut 69: 283−294 doi: 10.1136/gutjnl-2018-317431

Kim S, Sakaie K, Blümcke I, Jones S, Lowe MJ (2021) Whole-brain, ultra-high spatial resolution ex vivo MRI with off-the-shelf components. Magn Reson Imaging 76: 39−48 doi: 10.1016/j.mri.2020.11.002

Knudsen EI (2020) Evolution of neural processing for visual perception in vertebrates. J Comp Neurol 528: 2888−2901 doi: 10.1002/cne.24871

König IR, Fuchs O, Hansen G, von Mutius E, Kopp MV (2017) What is precision medicine? Eur Respir J 50: 1700391. https://doi.org/10.1183/13993003.00391-2017

Korogod N, Petersen CC, Knott GW (2015) Ultrastructural analysis of adult mouse neocortex comparing aldehyde perfusion with cryo fixation. Elife 4: e05793. https://doi.org/10.7554/eLife.05793

Krueger M, Härtig W, Reichenbach A, Bechmann I, Michalski D (2013) Blood-brain barrier breakdown after embolic stroke in rats occurs without ultrastructural evidence for disrupting tight junctions. PLoS One 8: e56419. https://doi.org/10.1371/journal.pone.0056419

Latta H, Hartmann JF (1950) Use of a glass edge in thin sectioning for electron microscopy. Proc Soc Exp Biol Med 74: 436−439 doi: 10.3181/00379727-74-17931

Lehrer J (2009) Neuroscience: making connections. Nature 457: 524−527 doi: 10.1038/457524a

Li A, Gong H, Zhang B, Wang Q, Yan C, Wu J, Liu Q, Zeng S, Luo Q (2010) Micro-optical sectioning tomography to obtain a high-resolution atlas of the mouse brain. Science 330: 1404−1408 doi: 10.1126/science.1191776

Li H, Li SH, Yu ZX, Shelbourne P, Li XJ (2001) Huntingtin aggregate-associated axonal degeneration is an early pathological event in Huntington's disease mice. J Neurosci 21: 8473−8481 doi: 10.1523/JNEUROSCI.21-21-08473.2001

Li Q, Weiland A, Chen X, Lan X, Han X, Durham F, Liu X, Wan J, Ziai WC, Hanley DF, Wang J (2018a) Ultrastructural characteristics of neuronal death and white matter injury in mouse brain tissues after intracerebral hemorrhage: coexistence of ferroptosis, autophagy, and necrosis. Front Neurol 9: 581. https://doi.org/10.3389/fneur.2018.00581

Li X, Yu B, Sun Q, Zhang Y, Ren M, Zhang X, Li A, Yuan J, Madisen L, Luo Q, Zeng H, Gong H, Qiu Z (2018b) Generation of a whole-brain atlas for the cholinergic system and mesoscopic projectome analysis of basal forebrain cholinergic neurons. Proc Natl Acad Sci USA 115: 415−420 doi: 10.1073/pnas.1703601115

Liu YT, Tao CL, Zhang X, Xia W, Shi DQ, Qi L, Xu C, Sun R, Li XW, Lau PM, Zhou ZH, Bi GQ (2020) Mesophasic organization of GABA(A) receptors in hippocampal inhibitory synapses. Nat Neurosci 23: 1589−1596 doi: 10.1038/s41593-020-00729-w

Livingston G, Huntley J, Sommerlad A, Ames D, Ballard C, Banerjee S, Brayne C, Burns A, Cohen-Mansfield J, Cooper C, Costafreda SG, Dias A, Fox N, Gitlin LN, Howard R, Kales HC, Kivimäki M, Larson EB, Ogunniyi A, Orgeta V, Ritchie K, Rockwood K, Sampson EL, Samus Q, Schneider LS, Selbæk G, Teri L, Mukadam N (2020) Dementia prevention, intervention, and care: 2020 report of the Lancet Commission. Lancet 396: 413−446 doi: 10.1016/S0140-6736(20)30367-6

Logothetis NK (2008) What we can do and what we cannot do with fMRI. Nature 453: 869−878 doi: 10.1038/nature06976

Michalski D, Grosche J, Pelz J, Schneider D, Weise C, Bauer U, Kacza J, Gärtner U, Hobohm C, Härtig W (2010) A novel quantification of blood-brain barrier damage and histochemical typing after embolic stroke in rats. Brain Res 1359: 186−200 doi: 10.1016/j.brainres.2010.08.045

Mikula S, Denk W (2015) High-resolution whole-brain staining for electron microscopic circuit reconstruction. Nat Methods 12: 541−546 doi: 10.1038/nmeth.3361

Milanesi L, Sheynis T, Xue WF, Orlova EV, Hellewell AL, Jelinek R, Hewitt EW, Radford SE, Saibil HR (2012) Direct three-dimensional visualization of membrane disruption by amyloid fibrils. Proc Natl Acad Sci USA 109: 20455−20460 doi: 10.1073/pnas.1206325109

Monfrini E, Di Fonzo A (2017) Leucine-rich repeat kinase (LRRK2) genetics and Parkinson's disease. Adv Neurobiol 14: 3−30

Muller HR (1957) Freeze-drying as a fixation technic for plant cells. J Ultrastruct Res 1: 109−137 doi: 10.1016/S0022-5320(57)80001-X

Nakamura S (1993) Huntington's disease-advances in gene mapping. Nihon Rinsho 51: 2481−2487

Nixon RA, Wegiel J, Kumar A, Yu WH, Peterhoff C, Cataldo A, Cuervo AM (2005) Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J Neuropathol Exp Neurol 64: 113−122 doi: 10.1093/jnen/64.2.113

Oh SW, Harris JA, Ng L, Winslow B, Cain N, Mihalas S, Wang Q, Lau C, Kuan L, Henry AM, Mortrud MT, Ouellette B, Nguyen TN, Sorensen SA, Slaughterbeck CR, Wakeman W, Li Y, Feng D, Ho A, Nicholas E, Hirokawa KE, Bohn P, Joines KM, Peng H, Hawrylycz MJ, Phillips JW, Hohmann JG, Wohnoutka P, Gerfen CR, Koch C, Bernard A, Dang C, Jones AR, Zeng H (2014) A mesoscale connectome of the mouse brain. Nature 508: 207−214 doi: 10.1038/nature13186

Pieri L, Madiona K, Bousset L, Melki R (2012) Fibrillar α-synuclein and huntingtin exon 1 assemblies are toxic to the cells. Biophys J 102: 2894−2905 doi: 10.1016/j.bpj.2012.04.050

Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, Pike B, Root H, Rubenstein J, Boyer R, Stenroos ES, Chandrasekharappa S, Athanassiadou A, Papapetropoulos T, Johnson WG, Lazzarini AM, Duvoisin RC, Di Iorio G, Golbe LI, Nussbaum RL (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276: 2045−2047 doi: 10.1126/science.276.5321.2045

Porter KR, Blum J (1953) A study in microtomy for electron microscopy. Anat Rec 117: 685−710 doi: 10.1002/ar.1091170403

Rastogi S, Sharma V, Bharti PS, Rani K, Modi GP, Nikolajeff F, Kumar S (2021) The evolving landscape of exosomes in neurodegenerative diseases: exosomes characteristics and a promising role in early diagnosis. Int J Mol Sci 22(1): 440. https://doi.org/10.3390/ijms22010440

Rodríguez JM, Murphy K, Stanton C, Ross RP, Kober OI, Juge N, Avershina E, Rudi K, Narbad A, Jenmalm MC, Marchesi JR, Collado MC (2015) The composition of the gut microbiota throughout life, with an emphasis on early life. Microb Ecol Health Dis 26: 26050. https://doi.org/10.3402/mehd.v26.26050

Roostaei T, Nazeri A, Sahraian MA, Minagar A (2014) The human cerebellum: a review of physiologic neuroanatomy. Neurol Clin 32: 859−869 doi: 10.1016/j.ncl.2014.07.013

Rosas HD, Chen YI, Doros G, Salat DH, Chen NK, Kwong KK, Bush A, Fox J, Hersch SM (2012) Alterations in brain transition metals in Huntington disease: an evolving and intricate story. Arch Neurol 69: 887−893

Ross CA, Poirier MA (2004) Protein aggregation and neurodegenerative disease. Nat Med 10(Suppl): S10−S17

Sanchez-Varo R, Trujillo-Estrada L, Sanchez-Mejias E, Torres M, Baglietto-Vargas D, Moreno-Gonzalez I, De Castro V, Jimenez S, Ruano D, Vizuete M, Davila JC, Garcia-Verdugo JM, Jimenez AJ, Vitorica J, Gutierrez A (2012) Abnormal accumulation of autophagic vesicles correlates with axonal and synaptic pathology in young Alzheimer's mice hippocampus. Acta Neuropathol 123: 53−70 doi: 10.1007/s00401-011-0896-x

Santos Armentia E, Martín Noguerol T, Suárez Vega V (2019) Advanced magnetic resonance imaging techniques for tumors of the head and neck. Radiologia (Engl Ed) 61: 191−203 doi: 10.1016/j.rxeng.2019.03.005

Saudou F, Humbert S (2016) The Biology of Huntingtin. Neuron 89: 910−926 doi: 10.1016/j.neuron.2016.02.003

Saygin AP, Sereno MI (2008) Retinotopy and attention in human occipital, temporal, parietal, and frontal cortex. Cereb Cortex 18: 2158−2168 doi: 10.1093/cercor/bhm242

Schapira AH, Cooper JM, Dexter D, Jenner P, Clark JB, Marsden CD (1989) Mitochondrial complex I deficiency in Parkinson's disease. Lancet 1: 1269

Schellenberg GD, Montine TJ (2012) The genetics and neuropathology of Alzheimer's disease. Acta Neuropathol 124: 305−323 doi: 10.1007/s00401-012-0996-2

Schubert AF, Gladkova C, Pardon E, Wagstaff JL, Freund SMV, Steyaert J, Maslen SL, Komander D (2017) Structure of PINK1 in complex with its substrate ubiquitin. Nature 552: 51−56 doi: 10.1038/nature24645

Selkoe DJ, Hardy J (2016) The amyloid hypothesis of Alzheimer's disease at 25 years. EMBO Mol Med 8: 595−608 doi: 10.15252/emmm.201606210

Shahmoradian SH, Lewis AJ, Genoud C, Hench J, Moors TE, Navarro PP, Castaño-Díez D, Schweighauser G, Graff-Meyer A, Goldie KN, Sütterlin R, Huisman E, Ingrassia A, Gier Y, Rozemuller AJM, Wang J, Paepe A, Erny J, Staempfli A, Hoernschemeyer J, Großerüschkamp F, Niedieker D, El-Mashtoly SF, Quadri M, Van IWFJ, Bonifati V, Gerwert K, Bohrmann B, Frank S, Britschgi M, Stahlberg H, Van de Berg WDJ, Lauer ME (2019) Lewy pathology in Parkinson's disease consists of crowded organelles and lipid membranes. Nat Neurosci 22: 1099−1109 doi: 10.1038/s41593-019-0423-2

Shampo MA, Kyle RA (1997) Ernst Ruska-inventor of the electron microscope. Mayo Clin Proc 72: 148. https://doi.org/10.4065/72.2.148

Shapson-Coe A, Januszewski M, Berger DR, Pope A, Wu Y, Blakely T, Schalek RL, Li PH. , Wang S, Maitin-Shepard J, Karlupia N, Dorkenwald S, Sjostedt E, Leavitt L, Lee D, Bailey L, Fitzmaurice A, Kar R, Field B, Wu H, Wagner-Carena J, Aley D, Lau J, Lin Z, Wei D, Pfister H, Peleg A, Jain V, Lichtman JW (2021) A connectomic study of a petascale fragment of human cerebral cortex. bioRxiv. https://doi.org/10.1101/2021.05.29.446289

Sjostrand FS (1953) The ultrastructure of the innersegments of the retinal rods of the guinea pig eye as revealed by electron microscopy. J Cell Comp Physiol 42: 45−70 doi: 10.1002/jcp.1030420104

Sporns O, Tononi G, Kötter R (2005) The human connectome: a structural description of the human brain. PLoS Comput Biol 1: e42. https://doi.org/10.1371/journal.pcbi.0010042

Taylor JP, Brown RH, Jr., Cleveland DW (2016) Decoding ALS: from genes to mechanism. Nature 539: 197−206 doi: 10.1038/nature20413

Trempe JF, Sauvé V, Grenier K, Seirafi M, Tang MY, Ménade M, Al-Abdul-Wahid S, Krett J, Wong K, Kozlov G, Nagar B, Fon EA, Gehring K (2013) Structure of parkin reveals mechanisms for ubiquitin ligase activation. Science 340: 1451−1455 doi: 10.1126/science.1237908

Trinkaus VA, Riera-Tur I, Martínez-Sánchez A, Bäuerlein FJB, Guo Q, Arzberger T, Baumeister W, Dudanova I, Hipp MS, Hartl FU, Fernández-Busnadiego R (2021) In situ architecture of neuronal α-Synuclein inclusions. Nat Commun 12: 2110. https://doi.org/10.1038/s41467-021-22108-0

Van Essen DC, Ugurbil K (2012) The future of the human connectome. Neuroimage 62: 1299−1310 doi: 10.1016/j.neuroimage.2012.01.032

Volpe JJ (2009) Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 8: 110−124 doi: 10.1016/S1474-4422(08)70294-1

Watanabe R, Buschauer R, Böhning J, Audagnotto M, Lasker K, Lu TW, Boassa D, Taylor S, Villa E (2020) The in situ structure of parkinson's disease-linked LRRK2. Cell 182: 1508−1518 doi: 10.1016/j.cell.2020.08.004

Wohlgemuth MJ, Moss CF (2016) Midbrain auditory selectivity to natural sounds. Proc Natl Acad Sci USA 113: 2508−2513 doi: 10.1073/pnas.1517451113

Wyss-Coray T (2016) Ageing, neurodegeneration and brain rejuvenation. Nature 539: 180−186 doi: 10.1038/nature20411

Xiaoyan Xue XG, Min Li, Minhuan Luo (2015) Research progress on the pathogenesis of neurodegenerative diseases. Chin J Gerontol 35: 3149−3152

Yousaf T, Dervenoulas G, Politis M (2018) Advances in MRI methodology. Int Rev Neurobiol 141: 31−76

Zhang B, Wu L-L, Wu Y-Y, Pan LJ, Lou SS, Kong (2016) The Application of highpressure freezing-freeze substitution technique in ultrastructure of nervous tissue. J Chin ElectrMicrosc Soc 36: 45−50

Zhong Q, Li A, Jin R, Zhang D, Li X, Jia X, Ding Z, Luo P, Zhou C, Jiang C, Feng Z, Zhang Z, Gong H, Yuan J, Luo Q (2021) High-definition imaging using line-illumination modulation microscopy. Nat Methods 18: 309−315 doi: 10.1038/s41592-021-01074-x

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