Cited by 119Neurogenetic and Muscular Disorders ResearchMitochondrial Function and PathologyAmyotrophic Lateral Sclerosis Research

The DOI matches its Crossref record; 65 of the 65 references it cites were found in a registry or an index.

Motor neuron mitochondrial dysfunction in spinal muscular atrophy

Open access

Miller, Nimrod, Shi, Han, Zelikovich, Aaron S., Ma, Yong-Chao·2016·Human Molecular Genetics

DOI 10.1093/hmg/ddw262PMC PMC5179954

Open this paper in CoChat — free account Open PDF

Abstract

Spinal muscular atrophy (SMA), the leading genetic cause of infant mortality, predominantly affects high metabolic tissues including motor neurons, skeletal muscles and the heart. Although the genetic cause of SMA has been identified, mechanisms underlying tissue-specific vulnerability are not well understood. To study these mechanisms, we carried out a deep sequencing analysis of the transcriptome of spinal motor neurons in an SMA mouse model, in which we unexpectedly found changes in many genes associated with mitochondrial bioenergetics. Importantly, functional measurement of mitochondrial activities showed decreased basal and maximal mitochondrial respiration in motor neurons from SMA mice. Using a reduction-oxidation sensitive GFP and fluorescence sensors specifically targeted to mitochondria, we found increased oxidative stress level and impaired mitochondrial membrane potential in motor neurons affected by SMA. In addition, mitochondrial mobility was impaired in SMA disease conditions, with decreased retrograde transport but no effect on anterograde transport. We also found significantly increased fragmentation of the mitochondrial network in primary motor neurons from SMA mice, with no change in mitochondria density. Electron microscopy study of SMA mouse spinal cord revealed mitochondria fragmentation, edema and concentric lamellar inclusions in motor neurons affected by the disease. Intriguingly, these functional and structural deficiencies in the SMA mouse model occur during the presymptomatic stage of disease, suggesting a role in initiating SMA. Altogether, our findings reveal a critical role for mitochondrial defects in SMA pathogenesis and suggest a novel target for improving tissue health in the disease.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1093/hmg/ddw262

Cites

65 of 65 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Mitochondrial Dysfunction and Oxidative Stress in Neurodegenerative Diseases
Lin, M. T., & Beal, M. F. (2006) · Nature · doi:10.1038/nature05292 · Cited by 6,455
Identification and characterization of a spinal muscular atrophy-determining gene
Lefebvre, S., Bürglen, L., Reboullet, S., Clermont, O., Burlet, P., Viollet, L., Bénichou, B., Cruaud, C., Millasseau, P., Zeviani, M., et al. (1995) · Cell · doi:10.1016/0092-8674(95)90460-3 · Cited by 3,995
Directed differentiation of embryonic stem cells into motor neurons.
Wichterle, H., Lieberam, I., Porter, J. A., & Jessell, T. (2002) · Cell · doi:10.1016/s0092-8674(02)00835-8 · Cited by 1,792
During autophagy mitochondria elongate, are spared from degradation and sustain cell viability
Gomes, L. C., Benedetto, G. D., & Scorrano, L. (2011) · Nature Cell Biology · doi:10.1038/ncb2220 · Cited by 1,735
Mitochondrial Respiratory-Chain Diseases
DiMauro, S., & Schon, E. A. (2003) · New England Journal of Medicine · doi:10.1056/nejmra022567 · Cited by 1,672
Disruption of Fusion Results in Mitochondrial Heterogeneity and Dysfunction
Chen, H., Chomyn, A., & Chan, D. C. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m503062200 · Cited by 1,376 · cited 2×
“Increased mitochondrial fusion protects against neurodegeneration (48), while disruption of fusion leads to smaller, fragmented mitochondria that display reduced membrane potential and impaired respiration (35,49).”
Background
Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency
Cogliati, S., Frezza, C., Soriano, M. E., Varanita, T., Quintana-Cabrera, R., Corrado, M., Cipolat, S., Costa, V., Casarin, A., Gomes, L. C., et al. (2013) · Cell · doi:10.1016/j.cell.2013.08.032 · Cited by 1,265
Mitochondrial dynamics and inheritance during cell division, development and disease
Mishra, P., & Chan, D. C. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3877 · Cited by 1,076
Spinal muscular atrophy
Lunn, M. R., & Wang, C. H. (2008) · The Lancet · doi:10.1016/s0140-6736(08)60921-6 · Cited by 1,010
Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration
Sheng, Z., & Cai, Q. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3156 · Cited by 940

Show all 65 references

Sorted by citations

Microglia Function in the Central Nervous System During Health and Neurodegeneration
Colonna, M., & Butovsky, O. (2017) · Annual Review of Immunology · doi:10.1146/annurev-immunol-051116-052358 · Cited by 2,894
Huntington disease: new insights into molecular pathogenesis and therapeutic opportunities
Tabrizi, S. J., Flower, M. D., Ross, C. A., & Wild, E. J. (2020) · Nature Reviews Neurology · doi:10.1038/s41582-020-0389-4 · Cited by 568
Spinal muscular atrophy
Mercuri, E. M., Sumner, C. J., Muntoni, F., Darras, B. T., & Finkel, R. S. (2022) · Nature Reviews Disease Primers · doi:10.1038/s41572-022-00380-8 · Cited by 473
Mitochondrial dysfunction: roles in skeletal muscle atrophy
Chen, X., Ji, Y., Liu, R., Zhu, X., Wang, K., Yang, X., Liu, B., Gao, Z., Huang, Y. H., Shen, Y., et al. (2023) · Journal of Translational Medicine · doi:10.1186/s12967-023-04369-z · Cited by 362
Twenty-Five Years of Spinal Muscular Atrophy Research: From Phenotype to Genotype to Therapy, and What Comes Next
Wirth, B., Karakaya, M., Kye, M. J., & Mendoza-Ferreira, N. (2020) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-102319-103602 · Cited by 267
Advances in therapy for spinal muscular atrophy: promises and challenges
Groen, E. J. N., Talbot, K., & Gillingwater, T. H. (2018) · Nature Reviews Neurology · doi:10.1038/nrneurol.2018.4 · Cited by 241
The role of survival motor neuron protein (SMN) in protein homeostasis
Chaytow, H., Huang, Y.-T., Gillingwater, T. H., & Faller, K. M. E. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2849-1 · Cited by 240
Mitochondrial Biogenesis in Neurons: How and Where
Cardanho‐Ramos, C., & Morais, V. A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222313059 · Cited by 189
Microglia and complement mediate early corticostriatal synapse loss and cognitive dysfunction in Huntington’s disease
Wilton, D. K., Mastro, K. J., Heller, M. D., Gergits, F. W., Willing, C. R., Fahey, J. B., Frouin, A., Daggett, A., Gu, X., Kim, Y. A., et al. (2023) · Nature Medicine · doi:10.1038/s41591-023-02566-3 · Cited by 189
Safety and efficacy of olesoxime in patients with type 2 or non-ambulatory type 3 spinal muscular atrophy: a randomised, double-blind, placebo-controlled phase 2 trial
Bertini, E., Dessaud, É., Mercuri, E. M., Francesco Muntoni, A., Kirschner, J., Reid, C., Łusakowska, A., Comi, G. P., Cuisset, J., Abitbol, J., et al. (2017) · The Lancet Neurology · doi:10.1016/s1474-4422(17)30085-6 · Cited by 114
Bioenergetic status modulates motor neuron vulnerability and pathogenesis in a zebrafish model of spinal muscular atrophy
Boyd, P. J., Tu, W.-Y., Shorrock, H. K., Groen, E. J. N., Carter, R. N., Powis, R. A., Thomson, S. R., Thomson, D., Graham, L. C., Motyl, A. A. L., et al. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006744 · Cited by 98
Two-year efficacy and safety of risdiplam in patients with type 2 or non-ambulant type 3 spinal muscular atrophy (SMA)
Oskoui, M., Day, J., Deconinck, N., Mazzone, E. S., Nascimento, A., Saito, K., Vuillerot, C., Baranello, G., Goemans, N., Kirschner, J., et al. (2023) · Journal of Neurology · doi:10.1007/s00415-023-11560-1 · Cited by 95
Co-occurrence of mixed proteinopathies in late-stage Huntington’s disease
St‐Amour, I., Turgeon, A., Goupil, C., Planel, E., & Hébert, S. S. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1786-7 · Cited by 90
Real-World Outcomes in Patients with Spinal Muscular Atrophy Treated with Onasemnogene Abeparvovec Monotherapy: Findings from the RESTORE Registry
Servais, L., Day, J., Vivo, D. C. D., Kirschner, J., Mercuri, E. M., Francesco Muntoni, A., Proud, C. M., Shieh, P. B., Tizzano, E. F., Quijano-Roy, S., et al. (2024) · Journal of Neuromuscular Diseases · doi:10.3233/jnd-230122 · Cited by 81
RD-Connect, NeurOmics and EURenOmics: collaborative European initiative for rare diseases
Lochmüller, H., Badowska, D. M., Thompson, R., Knoers, N. V. A. M., Aartsma-Rus, A. M., Gut, I. G., Wood, L., Harmuth, T., Durudas, A., Graeßner, H., et al. (2018) · European Journal of Human Genetics · doi:10.1038/s41431-018-0115-5 · Cited by 72
In Vivo Imaging with Genetically Encoded Redox Biosensors
Kostyuk, A. I., Panova, A. S., Kokova, A. D., Kotova, D. A., Maltsev, D. I., Podgorny, O. V., Belousov, V. V., & Bilan, D. S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21218164 · Cited by 66
Overview of Current Drugs and Molecules in Development for Spinal Muscular Atrophy Therapy
Shorrock, H. K., Gillingwater, T. H., & Groen, E. J. N. (2018) · Drugs · doi:10.1007/s40265-018-0868-8 · Cited by 62
A monocyte gene expression signature in the early clinical course of Parkinson’s disease
Schlachetzki, J. C. M., Prots, I., Tao, J., Chun, H. B., Saijo, K., Gosselin, D., Winner, B., Glass, C. K., & Winkler, J. (2018) · Scientific Reports · doi:10.1038/s41598-018-28986-7 · Cited by 58
Huntington’s disease: the coming of age
Pandey, M., & Rajamma, U. (2018) · Journal of Genetics · doi:10.1007/s12041-018-0957-1 · Cited by 56
Early alteration of epigenetic-related transcription in Huntington’s disease mouse models
Hervás-Corpión, I., Guiretti, D., Alcaráz-Iborra, M., Olivares, R., Campos‐Caro, A., Barco, Á., & Valor, L. M. (2018) · Scientific Reports · doi:10.1038/s41598-018-28185-4 · Cited by 55
Mitochondrial defects in the respiratory complex I contribute to impaired translational initiation via ROS and energy homeostasis in SMA motor neurons
Thelen, M. P., Wirth, B., & Kye, M. J. (2020) · Acta Neuropathologica Communications · doi:10.1186/s40478-020-01101-6 · Cited by 52
LCM-seq reveals unique transcriptional adaptation mechanisms of resistant neurons and identifies protective pathways in spinal muscular atrophyPreprint
Nichterwitz, S., Nijssen, J., Storvall, H., Schweingruber, C., Comley, L. H., Allodi, I., van der Lee, M., Deng, Q., Sandberg, R., & Hedlund, E. (2020) · Genome Research · doi:10.1101/gr.265017.120 · Cited by 48
Spinal muscular atrophy: Broad disease spectrum and sex-specific phenotypes
Singh, N. N., Hoffman, S., Reddi, P. P., & Singh, R. N. (2021) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2020.166063 · Cited by 52
The Role of AMPK in Neuromuscular Biology and Disease
Dial, A. G., Ng, S. Y., Manta, A., & Ljubicic, V. (2018) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2018.02.010 · Cited by 43
Mitochondrial Dysfunction in Spinal Muscular Atrophy
Zilio, E., Piano, V., & Wirth, B. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231810878 · Cited by 42
Revisiting the role of mitochondria in spinal muscular atrophy
James, R., Chaytow, H., Ledahawsky, L. M., & Gillingwater, T. H. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03819-5 · Cited by 45
Blocking p62-dependent SMN degradation ameliorates spinal muscular atrophy disease phenotypes
Rodríguez‐Muela, N., Parkhitko, A. A., Graß, T., Gibbs, R. M., Norabuena, E. M., Perrimon, N., Singh, R., & Rubin, L. L. (2018) · Journal of Clinical Investigation · doi:10.1172/jci95231 · Cited by 40
Mitochondrial stress responses in Duchenne muscular dystrophy: metabolic dysfunction or adaptive reprogramming?
Bellissimo, C. A., Garibotti, M. C., & Perry, C. G. R. (2022) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00249.2022 · Cited by 39
Advances in understanding the role of disease-associated proteins in spinal muscular atrophy
Hosseinibarkooie, S., Schneider, S. M., & Wirth, B. (2017) · Expert Review of Proteomics · doi:10.1080/14789450.2017.1345631 · Cited by 38
SMN Depleted Mice Offer a Robust and Rapid Onset Model of Nonalcoholic Fatty Liver Disease
Deguise, M., Pileggi, C. A., Repentigny, Y. D., Beauvais, A., Tierney, A., Chehadé, L., Michaud, J., Hurtado, M. L., Lamont, D. J., Atrih, A., et al. (2021) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2021.01.019 · Cited by 38
R-loop Mediated DNA Damage and Impaired DNA Repair in Spinal Muscular Atrophy
Cuartas, J., & Gangwani, L. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.826608 · Cited by 39
Mitochondrial imaging in live or fixed tissues using a luminescent iridium complex
Sorvina, A., Bader, C. A., Darby, J. R. T., Lock, M. C., Soo, J. Y., Johnson, I. R. D., Caporale, C., Voelcker, N. H., Stagni, S., Massi, M., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-24672-w · Cited by 37
Correlates of Fatigability in Patients With Spinal Muscular Atrophy
Bartels, B., de Groot, J. F., Habets, L. E., Wadman, R. I., Asselman, F., Nieuwenhuis, E. E. S., van Eijk, R. P. A., Goedee, H. S., & van der Pol, W. L. (2020) · Neurology · doi:10.1212/wnl.0000000000011230 · Cited by 37
How to Build and to Protect the Neuromuscular Junction: The Role of the Glial Cell Line-Derived Neurotrophic Factor
Stanga, S., Boido, M., & Kienlen‐Campard, P. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010136 · Cited by 39
In Search of a Cure: The Development of Therapeutics to Alter the Progression of Spinal Muscular Atrophy
Ojala, K. S., Reedich, E. J., DiDonato, C. J., & Meriney, S. D. (2021) · Brain Sciences · doi:10.3390/brainsci11020194 · Cited by 37
Survival motor neuron protein regulates oxidative stress and inflammatory response in microglia of the spinal cord in spinal muscular atrophy.
Ando, S., Osanai, D., Takahashi, K., Nakamura, S., Shimazawa, M., & Hara, H. (2020) · Journal of Pharmacological Sciences · doi:10.1016/j.jphs.2020.09.001 · Cited by 27
Magnetic resonance reveals mitochondrial dysfunction and muscle remodelling in spinal muscular atrophy
Habets, L. E., Bartels, B., Asselman, F., Hooijmans, M. T., van den Berg‐Faay, S., Nederveen, A. J., van der Pol, W. L., & Jeneson, J. A. L. (2021) · Brain · doi:10.1093/brain/awab411 · Cited by 31
The Protective Effects of Levetiracetam on a Human iPSCs-Derived Spinal Muscular Atrophy Model
Ando, S., Funato, M., Ohuchi, K., Inagaki, S., Sato, A., Seki, J., Kawase, C., Saito, T., Nishio, H., Nakamura, S., et al. (2019) · Neurochemical Research · doi:10.1007/s11064-019-02814-4 · Cited by 30
Biofluid Biomarkers in Huntington’s Disease
Rodrigues, F. B., Byrne, L. M., & Wild, E. J. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-7825-0_17 · Cited by 30
Long-term follow-up of patients with type 2 and non-ambulant type 3 spinal muscular atrophy (SMA) treated with olesoxime in the OLEOS trial
Francesco Muntoni, A., Bertini, E., Comi, G. P., Kirschner, J., Łusakowska, A., Mercuri, E. M., Scoto, M., van der Pol, W. L., Vuillerot, C., Burdeska, A., et al. (2020) · Neuromuscular Disorders · doi:10.1016/j.nmd.2020.10.008 · Cited by 29
AMPK is mitochondrial medicine for neuromuscular disorders
Mikhail, A. I., Ng, S. Y., Mattina, S. R., & Ljubicic, V. (2023) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2023.03.008 · Cited by 32
Survival Motor Neuron Protein is Released from Cells in Exosomes: A Potential Biomarker for Spinal Muscular Atrophy
Nash, L. A., McFall, E. R., Perozzo, A. M., Turner, M., Poulin, K. L., Repentigny, Y. D., Burns, J. K., McMillan, H. J., Warman‐Chardon, J., Burger, D. E., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-14313-z · Cited by 30
Developmental and degenerative cardiac defects in the Taiwanese mouse model of severe spinal muscular atrophy
Maxwell, G. K., Szunyogová, E., Shorrock, H. K., Gillingwater, T. H., & Parson, S. H. (2018) · Journal of Anatomy · doi:10.1111/joa.12793 · Cited by 33
Diminished muscle oxygen uptake and fatigue in spinal muscular atrophy
Montes, J., Goodwin, A. M., McDermott, M., Uher, D. T., Hernandez, F. M., Coutts, K., Cocchi, J., Hauschildt, M., Cornett, K., Rao, A. K., et al. (2021) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.51353 · Cited by 30
Allele-Selective Suppression of Mutant Huntingtin in Primary Human Blood Cells
Miller, J. R. C., Pfister, E. L., Liu, W., André, R., Träger, U., Kennington, L. A., Lo, K., Dijkstra, S., Macdonald, D., Ostroff, G. R., et al. (2017) · Scientific Reports · doi:10.1038/srep46740 · Cited by 27
Dysfunctional mitochondria accumulate in a skeletal muscle knockout model of Smn1, the causal gene of spinal muscular atrophy
Chemello, F., Pozzobon, M., Tsansizi, L. I., Varanita, T., Quintana–Cabrera, R., Bonesso, D., Piccoli, M., Lanfranchi, G., Giacomello, M., Scorrano, L., et al. (2023) · Cell Death and Disease · doi:10.1038/s41419-023-05573-x · Cited by 29
Muscle regulates mTOR dependent axonal local translation in motor neurons via CTRP3 secretion: implications for a neuromuscular disorder, spinal muscular atrophy
Rehorst, W. A., Thelen, M. P., Nolte, H., Türk, C., Çırak, S., Peterson, J. M., Wong, G. W., Wirth, B., Krüger, M., Winter, D., et al. (2019) · Acta Neuropathologica Communications · doi:10.1186/s40478-019-0806-3 · Cited by 27
The anti-tumor and renoprotection study of E-[c(RGDfK)2]/folic acid co-modified nanostructured lipid carrier loaded with doxorubicin hydrochloride/salvianolic acid A
Zhang, B., Zhang, Y., Dang, W., Xing, B., Yu, C., Guo, P., Pi, J., Deng, X., Qi, D., & Liu, Z. (2022) · Journal of Nanobiotechnology · doi:10.1186/s12951-022-01628-x · Cited by 26
SMN promotes mitochondrial metabolic maturation during myogenesis by regulating the MYOD-miRNA axis
Ikenaka, A., Kitagawa, Y., Yoshida, M., Lin, C., Niwa, A., Nakahata, T., & Saito, M. K. (2023) · Life Science Alliance · doi:10.26508/lsa.202201457 · Cited by 27
Microtubule-associated protein 1B dysregulates microtubule dynamics and neuronal mitochondrial transport in spinal muscular atrophy
Bora, G., Hensel, N., Rademacher, S., Koyunoğlu, D., Sunguroğlu, M., Aksu‐Menges, E., Balcı-Hayta, B., Claus, P., & Erdem‐Yurter, H. (2020) · Human Molecular Genetics · doi:10.1093/hmg/ddaa275 · Cited by 25
How Inflammation Pathways Contribute to Cell Death in Neuro-Muscular Disorders
Salucci, S., Stella, A. B., Battistelli, M., Burattini, S., Bavelloni, A., Cocco, L., Gobbi, P., & Faenza, I. (2021) · Biomolecules · doi:10.3390/biom11081109 · Cited by 26
Low-Intensity Running and High-Intensity Swimming Exercises Differentially Improve Energy Metabolism in Mice With Mild Spinal Muscular Atrophy
Houdebine, L., D’Amico, D., Bastin, J., Chali, F., Desseille, C., Rumeau, V., Soukkari, J., Oudot, C., Rouquet, T., Bariohay, B., et al. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.01258 · Cited by 23
Long Non-Coding RNA MAPK8IP1P2 Inhibits Lymphatic Metastasis of Thyroid Cancer by Activating Hippo Signaling via Sponging miR-146b-3p
Liu, X., Fu, Q., Bian, X., Fu, Y., Xin, J., Liang, N., Li, S., Zhao, Y., Li, F., Li, C., et al. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2020.600927 · Cited by 23
Quantifying mitochondrial volume density in phrenic motor neurons
Fogarty, M. J., Rana, S. D., Mantilla, C. B., & Sieck, G. C. (2021) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2021.109093 · Cited by 23
Single-cell RNA sequencing reveals dysregulation of spinal cord cell types in a severe spinal muscular atrophy mouse model
Sun, J., Qiu, J., Yang, Q., Ju, Q., Qu, R., Wang, X., Wu, L., & Xing, L. (2022) · PLoS Genetics · doi:10.1371/journal.pgen.1010392 · Cited by 25
Pathophysiology and Management of Fatigue in Neuromuscular Diseases
Torri, F., Lopriore, P., Montano, V., Siciliano, G., Mancuso, M., & Ricci, G. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24055005 · Cited by 26
Nusinersen Modulates Proteomics Profiles of Cerebrospinal Fluid in Spinal Muscular Atrophy Type 1 Patients
Bianchi, L., Sframeli, M., Vantaggiato, L., Vita, G. L., Ciranni, A., Polito, F., Oteri, R., Gitto, E., Giuseppe, F. D., Angelucci, S., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094329 · Cited by 22
Redox Imbalance in Neurological Disorders in Adults and Children
Rey, F., Berardo, C., Maghraby, E., Mauri, A., Messa, L., Esposito, L., Casili, G., Ottolenghi, S., Bonaventura, E., Cuzzocrea, S., et al. (2023) · Antioxidants · doi:10.3390/antiox12040965 · Cited by 23
Fibroblast Growth Factor 9 Stimulates Neuronal Length Through NF-kB Signaling in Striatal Cell Huntington’s Disease Models
Yusuf, I. O., Chen, H.-M., Cheng, P., Chang, C. S., Tsai, S., Chuang, J., Wu, C., Huang, B., Sun, H. S., Chen, C., et al. (2021) · Molecular Neurobiology · doi:10.1007/s12035-020-02220-w · Cited by 20
COPI-regulated mitochondria-ER contact site formation maintains axonal integrity
Maddison, D. C., Malik, B. R., Amadio, L., Bis‐Brewer, D. M., Zuchner, S. L., Peters, O. M., & Smith, G. A. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112883 · Cited by 20
Metalloprotease-mediated cleavage of PlexinD1 and its sequestration to actin rods in the motoneuron disease spinal muscular atrophy (SMA)
Rademacher, S., Verheijen, B. M., Hensel, N., Peters, M., Bora, G., Brandes, G., de Sá, R. V., Heidrich, N., Fischer, S., Brinkmann, H., et al. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx282 · Cited by 20
Vrk1 partial Knockdown in Mice Results in Reduced Brain Weight and Mild Motor Dysfunction, and Indicates Neuronal VRK1 Target Pathways
Vinograd-Byk, H., Renbaum, P., & Levy‐Lahad, E. (2018) · Scientific Reports · doi:10.1038/s41598-018-29215-x · Cited by 19
RNP Assembly Defects in Spinal Muscular Atrophy
Price, P. L., Morderer, D., & Rossoll, W. (2018) · Advances in neurobiology · doi:10.1007/978-3-319-89689-2_6 · Cited by 15
Motor unit reserve capacity in spinal muscular atrophy during fatiguing endurance performance
Habets, L. E., Bartels, B., de Groot, J. F., van der Pol, W. L., Jeneson, J. A. L., Asselman, F., van Eijk, R. P. A., & Stegeman, D. F. (2021) · Clinical Neurophysiology · doi:10.1016/j.clinph.2020.11.044 · Cited by 15
Calcium is reduced in presynaptic mitochondria of motor nerve terminals during neurotransmission in SMA mice
López-Manzaneda, M., Franco-Espín, J., Tejero, R., Cano, R., & Tabares, L. (2021) · Human Molecular Genetics · doi:10.1093/hmg/ddab065 · Cited by 16
Profilin2 regulates actin rod assembly in neuronal cells
Walter, L. M., Rademacher, S., Pich, A., & Claus, P. (2021) · Scientific Reports · doi:10.1038/s41598-021-89397-9 · Cited by 15
Smn-Deficiency Increases the Intrinsic Excitability of Motoneurons
Arumugam, S., Garcerá, A., Soler, R. M., & Tabares, L. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00269 · Cited by 15
Case report: Novel SCN4A variant associated with a severe congenital myasthenic syndrome/myopathy phenotype
Berghold, V. M., Koko, M., Berutti, R., & Plecko, B. (2022) · Frontiers in Pediatrics · doi:10.3389/fped.2022.944784 · Cited by 14
Autophagy in spinal muscular atrophy: from pathogenic mechanisms to therapeutic approaches
Rashid, S., & Dimitriadi, M. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1307636 · Cited by 17
The water extract of Liuwei dihuang possesses multi-protective properties on neurons and muscle tissue against deficiency of survival motor neuron protein
Tseng, Y., Jong, Y., Liang, W., Chang, F., & Lo, Y. (2017) · Phytomedicine · doi:10.1016/j.phymed.2017.08.018 · Cited by 14
Genetically Encoded Tools for Research of Cell Signaling and Metabolism under Brain Hypoxia
Kostyuk, A. I., Kokova, A. D., Podgorny, O. V., Kelmanson, I. V., Fetisova, E. S., Belousov, V. V., & Bilan, D. S. (2020) · Antioxidants · doi:10.3390/antiox9060516 · Cited by 13
Silencing SAPCD2 Represses Proliferation and Lung Metastasis of Fibrosarcoma by Activating Hippo Signaling Pathway
Zhu, B., Wu, Y., Niu, L., Wang, Y., Xue, M., Wang, H., Yang, J., Li, J., & Fan, W. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.574383 · Cited by 12
Genomic variants causing mitochondrial dysfunction are common in hereditary lower motor neuron disease
Keller, N., Paketçi, C., Altmüller, J., Fuhrmann, N., Wunderlich, G., Schrank, B., Unver, O. I., Yılmaz, S., Boostani, R., Karimiani, E. G., et al. (2021) · Human Mutation · doi:10.1002/humu.24181 · Cited by 12
Mutations of GEMIN5 are associated with coenzyme Q10 deficiency: long-term follow-up after treatment
Cascajo-Almenara, M. V., Juliá‐Palacios, N., Urreizti, R., Sánchez‐Cuesta, A., Fernández‐Ayala, D. J. M., García-Díaz, E., Oliva, C., ́Callaghan, M. D. M. O., Paredes-Fuentes, A. J., Moreno, P., et al. (2024) · European Journal of Human Genetics · doi:10.1038/s41431-023-01526-2 · Cited by 12
Spinal Cord Injury Model Mitochondria Connect Altered Function with Defects of Mitochondrion Morphology: an Ultrastructural Study
Hassanzadeh, S., Sabetvand, M., Sardar, R., Aryanpour, R., & Namjoo, Z. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03710-3 · Cited by 11
SMN regulation in SMA and in response to stress: new paradigms and therapeutic possibilities
Dominguez, C. E., Cunningham, D., & Chandler, D. S. (2017) · Human Genetics · doi:10.1007/s00439-017-1835-2 · Cited by 12
Cytoskeleton dysfunction of motor neuron in spinal muscular atrophy
Shi, T., Zhou, Z., Xiang, T., Suo, Y., Shi, X., Li, Y., Zhang, P., Dai, J., & Sheng, L. (2024) · Journal of Neurology · doi:10.1007/s00415-024-12724-3 · Cited by 10
Prolonged fasting‐induced hyperketosis, hypoglycaemia and impaired fat oxidation in child and adult patients with spinal muscular atrophy type II
Ørngreen, M. C., Andersen, A. G., Eisum, A. V., Hald, E. J., Raaschou-Pedersen, D. E. T., Løkken, N., Hoei‐Hansen, C. E., Vissing, J., Born, A. P., & van Hall, G. (2021) · Acta Paediatrica · doi:10.1111/apa.16074 · Cited by 11
Characterization of SMA type II skeletal muscle from treated patients shows OXPHOS deficiency and denervation
Grandi, F. C., Astord, S., Gidaja, E., Pezet, S., Mazzucchi, S., Chapart, M., Vasseur, S., Mamchaoui, K., & Smeriglio, P. (2024) · JCI Insight · doi:10.1172/jci.insight.180992 · Cited by 12
Genetically encoded biosensors of metabolic function for the study of neurodegeneration, a review and perspective
Zhao, M., Tanourlouee, S. B., McCracken, S., & Williams, P. R. (2025) · Neurophotonics · doi:10.1117/1.nph.12.s2.s22805 · Cited by 9
Altered Metabolism in Motor Neuron Diseases: Mechanism and Potential Therapeutic Target
Barone, C., & Qi, X. (2023) · Cells · doi:10.3390/cells12111536 · Cited by 11
Teaching An Old Drug New Tricks: Repositioning Strategies for Spinal Muscular atrophy
Hoolachan, J. M., Sutton, E. R., & Bowerman, M. (2019) · Future Neurology · doi:10.2217/fnl-2019-0006 · Cited by 10
Skeletal Muscle Mitochondrial and Autophagic Dysregulation Are Modifiable in Spinal Muscular Atrophy
Mikhail, A. I., Ng, S. Y., Xhuti, D., Lesinski, M. A., Chhor, J., Deguise, M., Repentigny, Y. D., Nederveen, J. P., Kothary, R., Tarnopolsky, M. A., et al. (2025) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.13701 · Cited by 8
The Proteome Signatures of Fibroblasts from Patients with Severe, Intermediate and Mild Spinal Muscular Atrophy Show Limited Overlap
Brown, S. J., Kline, R. A., Synowsky, S. A., Shirran, S. L., Holt, I., Sillence, K. A., Claus, P., Wirth, B., Wishart, T. M., & Fuller, H. R. (2022) · Cells · doi:10.3390/cells11172624 · Cited by 8
AAV9-mediated SMN gene therapy rescues cardiac desmin but not lamin A/C and elastin dysregulation in Smn 2B/− spinal muscular atrophy mice
Brown, S. J., Šoltić, D., Synowsky, S. A., Shirran, S. L., Chilcott, E. M., Shorrock, H. K., Gillingwater, T. H., Yáñez‐Muñoz, R. J., Schneider, B. L., Bowerman, M., et al. (2023) · Human Molecular Genetics · doi:10.1093/hmg/ddad121 · Cited by 8
Genetic Variability in Oxidative Stress, Inflammatory, and Neurodevelopmental Pathways: Impact on the Susceptibility and Course of Spinal Muscular Atrophy
Barbo, M., Koritnik, B., Leonardis, L., Blagus, T., Dolžan, V., & Ravnik‐Glavač, M. (2024) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-024-01508-y · Cited by 9
Structural and mitochondrial dendritic degenerations in old hypoglossal motor neurons
Christensen, T. A., & Fogarty, M. J. (2026) · GeroScience · doi:10.1007/s11357-025-02075-w · Cited by 6
Mitochondrial quality in aging and neurodegeneration: The emerging role of mitochondria-derived vesicles
Marzetti, E., Lorenzo, R. D., Calvani, R., Coelho‐Júnior, H. J., D’Argento, E., Pesce, V., Landi, F., Bucci, C., Guerra, F., & Picca, A. (2026) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2026.112167 · Cited by 8
Defective Expression of Mitochondrial, Vacuolar H+-ATPase and Histone Genes in a C. elegans Model of SMA
Gao, X., Xu, J., Chen, H., Xue, D., Pan, W., Zhou, C., Ma, Y. C., & Ma, L. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00410 · Cited by 6
Self-citation
Autophagy in motor neuron diseases
Rodríguez‐Muela, N. (2020) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2020.03.009 · Cited by 7
NSC Physiological Features in Spinal Muscular Atrophy: SMN Deficiency Effects on Neurogenesis
Adami, R., & Bottai, D. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232315209 · Cited by 6
Mitochondrial dysfunction could precipitate motor neuron loss in spinal muscular atrophy
Malkki, H. A. I. (2016) · Nature Reviews Neurology · doi:10.1038/nrneurol.2016.126 · Cited by 6
Mitigating aberrant Cdk5 activation alleviates mitochondrial defects and motor neuron disease symptoms in spinal muscular atrophy
Miller, N., Xu, Z., Quinlan, K. A., Ji, A., McGivern, J. V., Feng, Z., Shi, H., Ko, C., Tsai, L., Heckman, C. J., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2300308120 · Cited by 5
Self-citation
A Case Report of Systemic Intoxication Following Onabotulinum Toxin A Injections Into the Salivary Glands in a Patient With Spinal Muscular Atrophy Type 1
Kim, D. H., Elsherbini, N., Zielinski, D., & Oskoui, M. (2022) · Pediatric Neurology · doi:10.1016/j.pediatrneurol.2022.01.005 · Cited by 5
hnRNP R regulates mitochondrial movement and membrane potential in axons of motoneurons
Dithmar, S., Zare, A., Salehi, S., Briese, M., & Sendtner, M. (2024) · Neurobiology of Disease · doi:10.1016/j.nbd.2024.106454 · Cited by 5
Neuroanatomical Models of Muscle Strength and Relationship to Ambulatory Function in Spinal Muscular Atrophy
Rodriguez-Torres, R. S., Fabiano, J., Goodwin, A. M., Rao, A. K., Kinirons, S. A., Vivo, D. C. D., & Montes, J. (2020) · Journal of Neuromuscular Diseases · doi:10.3233/jnd-200550 · Cited by 5
Organ‐specific redox imbalances in spinal muscular atrophy mice are partially rescued by SMN antisense oligonucleotides
Vrettou, S., & Wirth, B. (2026) · FEBS Letters · doi:10.1002/1873-3468.70303 · Cited by 4
Comorbidities in spinal muscular atrophy and their impact on the course of the underlying disease: a real-life observational study
Błauciak, M., Ubysz, J., Wieczorek, M., & Koszewicz, M. A. (2025) · BMC Musculoskeletal Disorders · doi:10.1186/s12891-025-09133-6 · Cited by 3
Altered mitochondrial function in fibroblast cell lines derived from disease carriers of spinal muscular atrophy
James, R., Faller, K. M. E., Groen, E. J. N., Wirth, B., & Gillingwater, T. H. (2024) · Communications Medicine · doi:10.1038/s43856-024-00515-w · Cited by 3
Multi-step gene set analysis identified HTR3 family genes involving childhood acute lymphoblastic leukemia susceptibility
Liu, X., Guo, H., Kang, M., Fu, W., Li, H., Ji, H., Zhao, J., Fang, Y., Du, M., & Xue, Y. (2024) · Archives of Toxicology · doi:10.1007/s00204-024-03881-5 · Cited by 3

Authors: Miller, N., Shi, H., Zelikovich, A. S., & Ma, Y.-C.
Affiliations: Northwestern University (US)
ORCID: Miller, Nimrod
Zelikovich, Aaron S.
Venue: Human Molecular Genetics
Publisher: Oxford University Press (OUP)
Published: 2016-08-03
Volume: 25
Issue: 16
Pages: 3395-3406
ISSN: 0964-6906 (ISSN-L)
1460-2083
DOI: 10.1093/hmg/ddw262
PMC: PMC5179954
OpenAlex: W2504137115
Cited by: 119
References: 65
Citations by year: 2026: 6 · 2025: 6 · 2024: 11 · 2023: 13 · 2022: 12 · 2021: 18 · 2020: 19 · 2019: 5 · 2018: 17 · 2017: 11 · 2016: 1
FWCI: 8.22
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Human Molecular Genetics (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
HighWire Press Open Archive (submittedVersion)
Funders: Hartwell Foundation
Cure SMA
Feinberg Foundation
National Institutes of Health
National Institute of Neurological Disorders and Stroke (R01NS094564)
Topics: Health Sciences › Medicine › Genetics (clinical) › Neurogenetic and Muscular Disorders Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Health Sciences › Medicine › Clinical Neurology › Amyotrophic Lateral Sclerosis Research
Keywords: spinal muscular atrophy, motor neurons, mitochondrial dysfunction, mitochondrial respiration, oxidative stress, mitochondrial membrane potential, mitochondrial transport, mitochondrial fragmentation, presymptomatic disease, SMA mouse model, mitochondrial bioenergetics
MeSH terms: Animals, Disease Models, Animal, Humans, Microscopy, Electron, Mitochondria, Motor Neurons, Muscular Atrophy, Spinal, Myocardium, Spinal Cord, Oxidative Stress, Muscle, Skeletal, Mice, Membrane Potential, Mitochondrial, High-Throughput Nucleotide Sequencing, Transcriptome

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Motor neuron mitochondrial dysfunction in spinal muscular atrophy

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks