C. elegans as a model organism for human mitochondrial associated disorders
Abstract
Mitochondria are small cytoplasmic organelles whose most important function is to provide the energy required by our cells and organism to live. To maintain an adequate mitochondrial homeostasis cells possess numerous mitochondrial quality controls and protective compensatory pathways, which can be activated to cope with a certain degree of mitochondrial dysfunction. However, when the mitochondrial damage is too severe and these defensive mechanisms are not anymore sufficient to deal with it, pathological signs arise. In the past few decades numerous genetic disorders ascribed to severe mitochondrial defects have been recognized with variable onset and symptomatology ranging from neuromuscular degeneration to cancer syndromes. Unfortunately, to date, only symptomatic and no curative therapies exist for most of these devastating, life-threatening disorders. Model organisms, and especially the nematode Caenorhabditis elegans, with its sequenced and highly conserved genome, and a simple but well-characterized nervous system, have enormously contributed in the past years to gain insight into the pathogenesis and treatment of different diseases. Here, we will summarize some of the advantages offered by the nematode system to model neurodegenerative diseases associated with mitochondrial electron transport chain defects and screen for therapeutic interventions.
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The round worm Caenorhabditis elegans is used to investigate metabolic pathways and has been instrumental in elucidating key genetic regulators of metabolism in relation to lifespan.
“The round worm Caenorhabditis elegans, for instance, is used to investigate metabolic pathways and has been instrumental in elucidating key genetic regulators of metabolism in relation to lifespan (36, 293, 294).”
From Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease (2018) · cites this paper as [293]
Cites
Sequence and organization of the human mitochondrial genome
Anderson, S., Bankier, A. T., Barrell, B. G., de Bruijn, M. H. L., Coulson, A. R., Drouin, J., Eperon, I. C., Nierlich, D. P., Roe, B. A., Sanger, F., et al. (1981) · Nature · doi:10.1038/290457a0 · Cited by 9,640 · see citing works
Aging: a theory based on free radical and radiation chemistry
Harman, D. (1956) · Journal of Gerontology · doi:10.1093/geronj/11.3.298 · Cited by 8,567 · see citing works
Mitochondrial Dysfunction and Oxidative Stress in Neurodegenerative Diseases
Lin, M. T., & Beal, M. F. (2006) · Nature · doi:10.1038/nature05292 · Cited by 6,455 · see citing works
The structure of the nervous system of the nematode <i>Caenorhabditis elegans</i>
White, J. G., Southgate, E., Thomson, J. N., & Brenner, S. (1986) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1986.0056 · Cited by 5,589 · see citing works
Alberts, B., Johnson, A. D., Lewis, J. H., RAFF, M. C., Roberts, K. J., & Walter, P. (2007) · W.W. Norton eBooks · doi:10.1201/9780203833445 · Cited by 4,591 · see citing works
Wallace, D. C. (2005) · Annual Review of Genetics · doi:10.1146/annurev.genet.39.110304.095751 · Cited by 3,185 · see citing works
Mitochondrial diseases in man and mouse
Wallace, D. C. (1999) · Science · doi:10.1126/science.283.5407.1482 · Cited by 3,060 · see citing works
The Nematode Caenorhabditis elegans
Wood, W. B. (1988) · Cold Spring Harbor Laboratory eBooks · Cited by 2,821 · see citing works
Mitochondria: Dynamic Organelles in Disease, Aging, and Development
Chan, D. C. (2006) · Cell · doi:10.1016/j.cell.2006.06.010 · Cited by 1,987 · see citing works
Mitochondrial DNA mutations in human disease
Taylor, R. W., & Turnbull, D. M. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1606 · Cited by 1,866 · see citing works
Functional genomic analysis of C. elegans chromosome I by systematic RNA interference
Fraser, A. G., Kamath, R. S., Zipperlen, P., Martinez-Campos, M., Sohrmann, M., & Ahringer, J. (2000) · Nature · doi:10.1038/35042517 · Cited by 1,720 · see citing works
Bender, A., Krishnan, K. J., Morris, C. M., Taylor, G. A., Reeve, A. K., Perry, R. H., Jaros, E., Hersheson, J. S., Betts, J., Klopstock, T., et al. (2006) · Nature Genetics · doi:10.1038/ng1769 · Cited by 1,570 · see citing works
Rates of Behavior and Aging Specified by Mitochondrial Function During Development
Dillin, A., Hsu, A.-L., Arantes-Oliveira, N., Lehrer-Graiwer, J., Hsin, H., Fraser, A. G., Kamath, R. S., Ahringer, J., & Kenyon, C. (2002) · Science · doi:10.1126/science.1077780 · Cited by 1,121 · see citing works
Finding function in novel targets: C. elegans as a model organism
Kaletta, T., & Hengartner, M. O. (2006) · Nature Reviews Drug Discovery · doi:10.1038/nrd2031 · Cited by 1,091 · see citing works
Mitonuclear protein imbalance as a conserved longevity mechanism
Houtkooper, R. H., Mouchiroud, L., Ryu, D., Moullan, N., Katsyuba, E., Knott, G., Williams, R. W., & Auwerx, J. (2013) · Nature · doi:10.1038/nature12188 · Cited by 1,035 · see citing works
Mitophagy: mechanisms, pathophysiological roles, and analysis
Ding, W.-X., & Yin, X.-M. (2012) · bchm · doi:10.1515/hsz-2012-0119 · Cited by 1,032 · see citing works
Caenorhabditis elegans: An Emerging Model in Biomedical and Environmental Toxicology
Leung, M. C. K., Williams, P. L., Benedetto, A., Au, C., Helmcke, K. J., Aschner, M., & Meyer, J. N. (2008) · Toxicological Sciences · doi:10.1093/toxsci/kfn121 · Cited by 1,027 · see citing works
A systematic RNAi screen identifies a critical role for mitochondria in C. elegans longevity
Lee, S. S., Lee, R. Y. N., Fraser, A. G., Kamath, R. S., Ahringer, J., & Ruvkun, G. (2003) · Nature Genetics · doi:10.1038/ng1056 · Cited by 969 · see citing works
Mitochondrial role in cell aging
Miquel, J., Economos, A. C., Fleming, J., & Johnson, J. E. (1980) · Experimental Gerontology · doi:10.1016/0531-5565(80)90010-8 · Cited by 937 · see citing works
Kraytsberg, Y., Kudryavtseva, E., McKee, A. C., Geula, C., Kowall, N. W., & Khrapko, K. (2006) · Nature Genetics · doi:10.1038/ng1778 · Cited by 884 · see citing works
Cellular and molecular mechanisms of mitochondrial function
Osellame, L. D., Blacker, T. S., & Duchen, M. R. (2012) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2012.05.003 · Cited by 871 · see citing works
Mitochondria, oxidative stress and neurodegeneration
Federico, A., Cardaioli, E., Pozzo, P. D., Formichi, P., Gallus, G. N., & Radi, E. (2012) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2012.05.030 · Cited by 790 · see citing works
Coordination of mitophagy and mitochondrial biogenesis during ageing in C. elegans
Palikaras, K., Lionaki, E., & Tavernarakis, N. (2015) · Nature · doi:10.1038/nature14300 · Cited by 770 · see citing works
Human mitochondrial DNA: roles of inherited and somatic mutations
Schon, E. A., DiMauro, S., & Hirano, M. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3275 · Cited by 757 · see citing works
Frataxin is Reduced in Friedreich Ataxia Patients and is Associated with Mitochondrial Membranes
Campuzano, V., Montermini, L., Lutz, Y., Cova, L., Hindelang, C., Jiralerspong, S., Trottier, Y., Kish, S. J., Faucheux, B. A., Trouillas, P., et al. (1997) · Human Molecular Genetics · doi:10.1093/hmg/6.11.1771 · Cited by 739 · see citing works
Mitochondrial disorders as windows into an ancient organelle
Vafai, S. B., & Mootha, V. K. (2012) · Nature · doi:10.1038/nature11707 · Cited by 733 · see citing works
Decline in skeletal muscle mitochondrial respiratory chain function: possible factor in ageing
Trounce, I., Byrne, E., & Marzuki, S. (1989) · The Lancet · doi:10.1016/s0140-6736(89)92143-0 · Cited by 730 · see citing works
Quality control of mitochondria: protection against neurodegeneration and ageing
Tatsuta, T., & Langer, T. (2008) · The EMBO Journal · doi:10.1038/sj.emboj.7601972 · Cited by 519 · see citing works
Cell and Molecular Biology: Concepts and Experiments
Karp, G. C., & van der Geer, P. (1984) · Cited by 517 · see citing works
Monogenic Mitochondrial Disorders
Koopman, W. J. H., Willems, P. H. G. M., & Smeitink, J. A. M. (2012) · New England Journal of Medicine · doi:10.1056/nejmra1012478 · Cited by 515 · see citing works
A systematic RNAi screen for longevity genes in C. elegansPreprint
Hamilton, B., Dong, Y., Shindo, M., Liu, W., Odell, I., Ruvkun, G., & Lee, S. S. (2005) · Genes & Development · doi:10.1101/gad.1308205 · Cited by 513 · see citing works
Mitochondrial dynamics in neurodegeneration
Itoh, K., Nakamura, K., Iijima, M., & Sesaki, H. (2012) · Trends in Cell Biology · doi:10.1016/j.tcb.2012.10.006 · Cited by 464 · see citing works
Oxidative stress and mitochondrial dysfunction in neurodegenerative diseases
Trushina, E. V., & McMurray, C. T. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2006.10.056 · Cited by 440 · see citing works
Nolden, M., Ehses, S., Koppen, M., Bernacchia, A., Rugarli, E. I., & Langer, T. (2005) · Cell · doi:10.1016/j.cell.2005.08.003 · Cited by 398 · see citing works
Rea, S. L., Ventura, N., & Johnson, T. E. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050259 · Cited by 383 · see citing works
Decline with age of the respiratory chain activity in human skeletal muscle
Boffoli, D., Scacco, S. C., Vergari, R., Solarino, G., Santacroce, G., & Papa, S. (1994) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/0925-4439(94)90061-2 · Cited by 341 · see citing works
Mitochondrial Quality Control Mediated by PINK1 and Parkin: Links to ParkinsonismPreprint
Narendra, D. P., Walker, J. E., & Youle, R. J. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a011338 · Cited by 341 · see citing works
Jovaisaite, V., Mouchiroud, L., & Auwerx, J. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.090738 · Cited by 335 · see citing works
The Nobel Prize in Physiology or Medicine
Lindsten, J., & Ringertz, N. R. (2001) · CO-PUBLISHED WITH IMPERIAL COLLEGE PRESS eBooks · doi:10.1142/9789810248543_0007 · Cited by 334 · see citing works
Mitochondrial Dysfunctions in Neurodegenerative Diseases: Relevance to Alzheimer’s Disease
Hroudová, J., Singh, N., & Fišar, Z. (2014) · BioMed Research International · doi:10.1155/2014/175062 · Cited by 319 · see citing works
Alexander, A. G., Marfil, V., & Li, C. (2014) · Frontiers in Genetics · doi:10.3389/fgene.2014.00279 · Cited by 310 · see citing works
High‐throughput screening and small animal models, where are we?
Giacomotto, J., & Ségalat, L. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.00725.x · Cited by 295 · see citing works
An antidepressant that extends lifespan in adult Caenorhabditis elegans
Petrascheck, M., Ye, X., & Buck, L. B. (2007) · Nature · doi:10.1038/nature05991 · Cited by 287 · see citing works
A small-molecule screen in C. elegans yields a new calcium channel antagonist
Kwok, T. C. Y., Ricker, N., Fraser, R., Chan, A. W., Burns, A. R., Stanley, E. F., McCourt, P., Cutler, S. R., & Roy, P. J. (2006) · Nature · doi:10.1038/nature04657 · Cited by 268 · see citing works
Impairing the Mitochondrial Fission and Fusion Balance: A New Mechanism of Neurodegeneration
Knott, A. B., & Bossy‐Wetzel, E. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1427.030 · Cited by 258 · see citing works
C. elegans in high-throughput drug discovery
O'Reilly, L. P., Luke, C., Perlmutter, D., Silverman, G., & Pak, S. C. (2013) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2013.12.001 · Cited by 251 · see citing works
Worms under stress: C. elegans stress response and its relevance to complex human disease and aging
Rodríguez, M. G., Snoek, B. L., de Bono, M., & Kammenga, J. E. (2013) · Trends in Genetics · doi:10.1016/j.tig.2013.01.010 · Cited by 219 · see citing works
Structure and function of mitochondrial supercomplexes
Dudkina, N. V., Kouřil, R., Peters, K., Braun, H., & Boekema, E. J. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2009.12.013 · Cited by 218 · see citing works
Link, C. D. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2006.06.059 · Cited by 213 · see citing works
Iron-starvation-induced mitophagy mediates lifespan extension upon mitochondrial stress in C.elegans
Schiavi, A., Maglioni, S., Palikaras, K., Shaik, A., Strappazzon, F., Brinkmann, V., Torgovnick, A., Castelein, N., De Henau, S., Braeckman, B. P., et al. (2015) · Current Biology · doi:10.1016/j.cub.2015.05.059 · Cited by 209 · see citing works
Prohibitin Ligands in Cell Death and Survival: Mode of Action and Therapeutic Potential
Thuaud, F., Ribeiro, N., Nebigil, C. G., & Désaubry, L. (2013) · Chemistry & Biology · doi:10.1016/j.chembiol.2013.02.006 · Cited by 209 · see citing works
Haynes, C. M., Fiorese, C. J., & Lin, Y. (2013) · Trends in Cell Biology · doi:10.1016/j.tcb.2013.02.002 · Cited by 209 · see citing works
Finsterer, J. (2004) · European Journal of Neurology · doi:10.1046/j.1351-5101.2003.00728.x · Cited by 206 · see citing works
Modeling human diseases in Caenorhabditis elegans
Markaki, M., & Tavernarakis, N. (2010) · Biotechnology Journal · doi:10.1002/biot.201000183 · Cited by 205 · see citing works
Gosai, S. J., Kwak, J., Luke, C., Long, O. S., King, D. E., Kovatch, K., Johnston, P., Tong, Y.-S., Lazo, J., Perlmutter, D., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015460 · Cited by 200 · see citing works
Feedback regulation via AMPK and HIF-1 mediates ROS-dependent longevity in Caenorhabditis elegans
Hwang, A. B., Ryu, E.-A., Artan, M., Chang, H., Kabir, M. H., Nam, H.-J., Lee, D.-Y., Yang, J., Kim, S., Mair, W. B., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1411199111 · Cited by 189 · see citing works
Caenorhabditis elegans MPP+ Model of Parkinson’s Disease for High-Throughput Drug Screenings
Braungart, E., Gerlach, M., Riederer, P. F., Baumeister, R., & Hoener, M. C. (2004) · Neurodegenerative Diseases · doi:10.1159/000080983 · Cited by 187 · see citing works
The role of mitochondria in inherited neurodegenerative diseases
Kwong, J. Q., Beal, M. F., & Manfredi, G. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03990.x · Cited by 180 · see citing works
Cristina, D., Cary, M., Lunceford, A., Clarke, C., & Kenyon, C. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000450 · Cited by 166 · see citing works
Mitochondrial degradation and energy metabolism
Melser, S., Lavie, J., & Bénard, G. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2015.05.010 · Cited by 163 · see citing works
Caenorhabditis elegans: A versatile platform for drug discovery
Artal‐Sanz, M., de Jong, L., & Tavernarakis, N. (2006) · Biotechnology Journal · doi:10.1002/biot.200600176 · Cited by 153 · see citing works
The role of mitochondrial DNA mutation on neurodegenerative diseases
Cha, M.-Y., Kim, D. K., & Mook‐Jung, I. (2015) · Experimental & Molecular Medicine · doi:10.1038/emm.2014.122 · Cited by 153 · see citing works
Tsang, W. Y., Sayles, L. C., Grad, L. I., Pilgrim, D. B., & Lemire, B. D. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m103999200 · Cited by 148 · see citing works
Mitochondrial DNA Mutations in Disease, Aging, and Neurodegeneration
Reeve, A. K., Krishnan, K. J., & Turnbull, D. M. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1427.016 · Cited by 146 · see citing works
Mitochondrial Disorders Overview
Chinnery, P. F. (2014) · Cited by 142 · see citing works
Ben-Yakar, A., Chronis, N., & Lu, H. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.10.010 · Cited by 138 · see citing works
A cytoprotective perspective on longevity regulation
Shore, D. E., & Ruvkun, G. (2013) · Trends in Cell Biology · doi:10.1016/j.tcb.2013.04.007 · Cited by 137 · see citing works
Lehner, B., Tischler, J., & Fraser, A. G. (2006) · Nature Protocols · doi:10.1038/nprot.2006.245 · Cited by 136 · see citing works
Grad, L. I. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddh027 · Cited by 130 · see citing works
Chakrabarti, S., Munshi, S., Banerjee, K., Thakurta, I. G., Sinha, M. S., & Bagh, M. B. (2011) · Europe PMC (PubMed Central) · Cited by 122 · see citing works
Lublin, A. L., & Link, C. D. (2012) · Drug Discovery Today Technologies · doi:10.1016/j.ddtec.2012.02.002 · Cited by 119 · see citing works
Dingley, S. D., Polyák, E., Lightfoot, R. T., Ostrovsky, J., Rao, M., Greco, T. M., Ischiropoulos, H., & Falk, M. J. (2009) · Mitochondrion · doi:10.1016/j.mito.2009.11.003 · Cited by 115 · see citing works
Medium- and high-throughput screening of neurotoxicants using C. elegans
Boyd, W. A., Smith, M. V., Kissling, G. E., & Freedman, J. H. (2009) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2008.12.004 · Cited by 114 · see citing works
The Neurodegenerative Mitochondriopathies
Swerdlow, R. H. (2009) · Journal of Alzheimer s Disease · doi:10.3233/jad-2009-1095 · Cited by 112 · see citing works
p53/CEP‐1 increases or decreases lifespan, depending on level of mitochondrial bioenergetic stress
Ventura, N., Rea, S. L., Schiavi, A., Torgovnick, A., Testi, R., & Johnson, T. E. (2009) · Aging Cell · doi:10.1111/j.1474-9726.2009.00482.x · Cited by 111 · see citing works
Metabolic pathway profiling of mitochondrial respiratory chain mutants in C. elegans
Falk, M. J., Zhang, Z., Rosenjack, J. R., Nissim, I. B., Daikhin, E., Nissim, I. B., Sedensky, M. M., Yudkoff, M., & Morgan, P. G. (2008) · Molecular Genetics and Metabolism · doi:10.1016/j.ymgme.2007.11.007 · Cited by 111 · see citing works
UPRmt-mediated cytoprotection and organismal aging
Schulz, A. M., & Haynes, C. M. (2015) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2015.03.008 · Cited by 110 · see citing works
Raamsdonk, J. M. V., Meng, Y., Camp, D., Yang, W., Jia, X., Bénard, C. Y., & Hekimi, S. (2010) · Genetics · doi:10.1534/genetics.110.115378 · Cited by 106 · see citing works
The Paradox of Mitochondrial Dysfunction and Extended Longevity
Munkácsy, E., & Rea, S. L. (2014) · Experimental Gerontology · doi:10.1016/j.exger.2014.03.016 · Cited by 101 · see citing works
Modeling Molecular and Cellular Aspects of Human Disease Using the Nematode Caenorhabditis elegans
Silverman, G. A., Luke, C. J., Bhatia, S. R., Long, O. S., Vetica, A. C., Perlmutter, D. H., & Pak, S. C. (2008) · Pediatric Research · doi:10.1203/pdr.0b013e31819009b0 · Cited by 100 · see citing works
Vázquez‐Manrique, R. P., González‐Cabo, P., Ros, S., Aziz, H., Baylis, H. A., & Palau, F. (2005) · The FASEB Journal · doi:10.1096/fj.05-4212fje · Cited by 98 · see citing works
Long-lived C. elegans Mitochondrial mutants as a model for human mitochondrial-associated diseases
Ventura, N., Rea, S. L., & Testi, R. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2006.06.060 · Cited by 89 · see citing works
Reduced expression of frataxin extends the lifespan of Caenorhabditis elegans
Ventura, N., Rea, S. L., Henderson, S. T., Condò, I., Johnson, T. E., & Testi, R. (2005) · Aging Cell · doi:10.1111/j.1474-9726.2005.00149.x · Cited by 81 · see citing works
Long-lived mitochondrial (Mit) mutants of Caenorhabditis elegans utilize a novel metabolism
Butler, J. A., Ventura, N., Johnson, T. E., & Rea, S. L. (2010) · The FASEB Journal · doi:10.1096/fj.10-162941 · Cited by 75 · see citing works
Schiavi, A., Torgovnick, A., Kell, A. M., Megalou, E. V., Castelein, N., Guccini, I., Marzocchella, L., Gelino, S., Hansen, M., Malisan, F., et al. (2012) · Experimental Gerontology · doi:10.1016/j.exger.2012.12.002 · Cited by 75 · see citing works
Teschendorf, D., & Link, C. D. (2009) · Molecular Neurodegeneration · doi:10.1186/1750-1326-4-38 · Cited by 74 · see citing works
Choe, K. P., & Strange, K. B. (2008) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00450.2008 · Cited by 73 · see citing works
C. elegans ATAD-3 Is Essential for Mitochondrial Activity and Development
Hoffmann, M., Bellancé, N., Rossignol, R., Koopman, W. J. H., Willems, P. H. G. M., Mayatepek, E., Bossinger, O., & Distelmaier, F. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007644 · Cited by 70 · see citing works
Novel interactions between mitochondrial superoxide dismutases and the electron transport chain
Suthammarak, W., Somerlot, B. H., Opheim, E., Sedensky, M. M., & Morgan, P. G. (2013) · Aging Cell · doi:10.1111/acel.12144 · Cited by 65 · see citing works
Insights on altered mitochondrial function and dynamics in the pathogenesis of neurodegeneration
McInnes, J. (2013) · Translational Neurodegeneration · doi:10.1186/2047-9158-2-12 · Cited by 64 · see citing works
Utility of Caenorhabditis elegans in high throughput neurotoxicological research
Helmcke, K. J., Ávila, D. S., & Aschner, M. (2008) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2008.11.005 · Cited by 60 · see citing works
The interplay between mitochondria and autophagy and its role in the aging process
Schiavi, A., & Ventura, N. (2014) · Experimental Gerontology · doi:10.1016/j.exger.2014.02.015 · Cited by 59 · see citing works
A High‐Throughput Screen for Chemicals that Increase the Lifespan of Caenorhabditis elegans
Petrascheck, M., Ye, X., & Buck, L. B. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04377.x · Cited by 59 · see citing works
Zarse, K., Schulz, T. J., Birringer, M., & Ristow, M. (2007) · The FASEB Journal · doi:10.1096/fj.06-6994com · Cited by 58 · see citing works
Grad, L. I., & Lemire, B. D. (2006) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2005.11.009 · Cited by 57 · see citing works
Metabolism in the Caenorhabditis elegans Mit mutants
Rea, S. L. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.06.015 · Cited by 57 · see citing works
Watching Worms Whither: Modeling Neurodegeneration in C. elegans
Wolozin, B., Gabel, C. V., Ferree, A., Guillily, M. D., & Ebata, A. (2011) · Progress in Molecular Biology and Translational Science · doi:10.1016/b978-0-12-384878-9.00015-7 · Cited by 56 · see citing works
Ventura, N., & Rea, S. L. (2007) · Biotechnology Journal · doi:10.1002/biot.200600248 · Cited by 54 · see citing works
Calap-Quintana, P., Soriano, S., Llorens, J. V., Al‐Ramahi, I., Botas, J., Moltó, M. D., & Martínez-Sebastián, M. J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0132376 · Cited by 53 · see citing works
Effects of the mitochondrial respiratory chain on longevity in C. elegans
Rabbitts, B. M., Sedensky, M. M., & Morgan, P. G. (2014) · Experimental Gerontology · doi:10.1016/j.exger.2014.03.028 · Cited by 53 · see citing works
Mitochondrial stress extends lifespan in C. elegans through neuronal hormesis
Maglioni, S., Schiavi, A., Runci, A., Shaik, A., & Ventura, N. (2014) · Experimental Gerontology · doi:10.1016/j.exger.2014.03.026 · Cited by 52 · see citing works
The early bird catches the worm: new technologies for the Caenorhabditis elegans toolkit
Xu, X., & Kim, S. K. (2011) · Nature Reviews Genetics · doi:10.1038/nrg3050 · Cited by 49 · see citing works
Neuronal responses to stress and injury in C. elegans
Kim, K. W., & Jin, Y.-S. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.05.005 · Cited by 44 · see citing works
Rapamycin reduces oxidative stress in frataxin-deficient yeast cells
Marobbio, C. M. T., Pisano, I., Porcelli, V., Lasorsa, F. M., & Palmieri, L. (2011) · Mitochondrion · doi:10.1016/j.mito.2011.07.001 · Cited by 42 · see citing works
Gatsi, R., Schulze, B., Rodríguez‐Palero, M. J., Hernando‐Rodríguez, B., Baumeister, R., & Artal‐Sanz, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0107671 · Cited by 41 · see citing works
Grad, L. I., Sayles, L. C., & Lemire, B. D. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506939102 · Cited by 41 · see citing works
Subcomplex Iλ Specifically Controls Integrated Mitochondrial Functions in Caenorhabditis elegans
Falk, M. J., Rosenjack, J. R., Polyák, E., Suthammarak, W., Chen, Z., Morgan, P. G., & Sedensky, M. M. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006607 · Cited by 35 · see citing works
Screening for Presenilin Inhibitors Using the Free-Living Nematode, Caenorhabditis elegans
Ellerbrock, B. R., Coscarelli, E. M., Gurney, M. E., & Geary, T. G. (2004) · SLAS DISCOVERY · doi:10.1177/1087057103261038 · Cited by 31 · see citing works
Maglioni, S., Arsalan, N., Franchi, L., Hurd, A. R., Opipari, A. W., Glick, G. D., & Ventura, N. (2015) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2015.05.004 · Cited by 20 · see citing works
Studying Human Disease Genes inCaenorhabditis elegans: A Molecular Genetics Laboratory Project
Cox, E. A., Grana, T. M., Harris, M. A., & Batzli, J. (2012) · CBE—Life Sciences Education · doi:10.1187/cbe-11-06-0045 · Cited by 19 · see citing works
C. elegans as a model for Friedreich Ataxia
Ventura, N., Rea, S. L., Handerson, S. T., Condò, I., Testi, R., & Johnson, T. E. (2006) · The FASEB Journal · doi:10.1096/fj.06-0505ufm · Cited by 19 · see citing works
Collaboration between mitochondria and the nucleus is key to long life in Caenorhabditis elegans
Chang, H.-W., Shtessel, L., & Lee, S. S. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2014.10.576 · Cited by 15 · see citing works
Mitochondrial Biogenesis and Dynamics in Neurodegeneration: A Causative Relationship
Nikoletopoulou, V., & Tavernarakis, N. (2013) · Neurochemical Research · doi:10.1007/s11064-013-0997-0 · Cited by 10 · see citing works
van den Ecker, D., van den Brand, M. A. M., Ariaans, G., Hoffmann, M., Bossinger, O., Mayatepek, E., Nijtmans, L. G. J., & Distelmaier, F. (2012) · Mitochondrion · doi:10.1016/j.mito.2012.01.003 · Cited by 9 · see citing works
ATP5B (ATP synthase, H+ transporting, mitochondrial F1 complex, beta polypeptide)
Bozgeyi̇k, E., Arman, K., & İğci, Y. Z. (2017) · Atlas of Genetics and Cytogenetics in Oncology and Haematology · doi:10.4267/2042/62496 · Cited by 3 · see citing works
GENETICS OF MITOCHONDRIAL DISEASES
Menzies, F. M. (2004) · Brain · doi:10.1093/brain/awh093 · Cited by 2 · see citing works
Transcription and translation of mitochondrial DNA
Taanman, J. (2003) · UCL Discovery (University College London) · Cited by 1 · see citing works
Flagged first, then by citations
2 of the 119 references couldn’t be matched to a known paper.
Cited by
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Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease
Smith, R. L., Soeters, M. R., Wüst, R. C. I., & Houtkooper, R. H. (2018) · Endocrine Reviews · doi:10.1210/er.2017-00211 · Cited by 787 · see citing works
Cell biology of the mitochondrion
van der Bliek, A. M., Sedensky, M. M., & Morgan, P. G. (2017) · Genetics · doi:10.1534/genetics.117.300262 · Cited by 388 · see citing works
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 340 · see citing works
Mitochondrial lipids in neurodegeneration
Aufschnaiter, A., Kohler, V., Diessl, J., Peselj, C., Carmona‐Gutiérrez, D., Keller, W., & Büttner, S. (2016) · Cell and Tissue Research · doi:10.1007/s00441-016-2463-1 · Cited by 85 · see citing works
Metabolomics and lipidomics in Caenorhabditis elegans using a single-sample preparation
Molenaars, M., Schomakers, B. V., Elfrink, H. L., Gao, A. W., Vervaart, M. A. T., Pras‐Raves, M. L., Luyf, A. C. M., Smith, R. L., Sterken, M. G., Kammenga, J. E., et al. (2021) · Disease Models & Mechanisms · doi:10.1242/dmm.047746 · Cited by 58 · see citing works
Luz, A. L., Godebo, T. R., Smith, L. L., Leuthner, T. C., Maurer, L. L., & Meyer, J. N. (2017) · Toxicology · doi:10.1016/j.tox.2017.05.018 · Cited by 58 · see citing works
Mitochondrial metabolism: a common link between neuroinflammation and neurodegeneration
Garabadu, D., Agrawal, N., Sharma, A., & Sharma, S. (2019) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000505 · Cited by 57 · see citing works
Soares, M. V., Mesadri, J., Gonçalves, D. F., Cordeiro, L. M., da Silva, A. F., Baptista, F. B. O., Wagner, R. C., Corte, C. L. D., Soares, F. A. A., & Ávila, D. S. (2022) · Environmental Pollution · doi:10.1016/j.envpol.2022.118856 · Cited by 44 · see citing works
Rangseekaew, P., Barros‐Rodríguez, A., ., W. P.-A., & Manzanera, M. (2022) · Biology · doi:10.3390/biology11020191 · Cited by 43 · see citing works
Witting, M. A., Hastings, J., Rodríguez, N., Joshi, C. J., Hattwell, J. P. N., Ebert, P. R., van Weeghel, M., Gao, A. W., Wakelam, M. J. O., Houtkooper, R. H., et al. (2018) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2018.00096 · Cited by 36 · see citing works
Nutritional Interventions for Mitochondrial OXPHOS Deficiencies: Mechanisms and Model Systems
Kuszak, A. J., Espey, M. G., Falk, M. J., Holmbeck, M. A., Manfredi, G., Shadel, G. S., Vernon, H. J., & Zolkipli‐Cunningham, Z. (2017) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-020117-043644 · Cited by 33 · see citing works
Maglioni, S., Schiavi, A., Melcher, M., Brinkmann, V., Luo, Z., Laromaine, A., Raimundo, N., Meyer, J. N., Distelmaier, F., & Ventura, N. (2022) · Nature Communications · doi:10.1038/s41467-022-29972-4 · Cited by 30 · see citing works
Mitochondrial bioenergetic changes during development as an indicator of C. elegans health-span
Maglioni, S., Mello, D. F., Schiavi, A., Meyer, J. N., & Ventura, N. (2019) · Aging · doi:10.18632/aging.102208 · Cited by 29 · see citing works
Translational geroscience: From invertebrate models to companion animal and human interventions
Lee, M. B., & Kaeberlein, M. R. (2018) · Translational Medicine of Aging · doi:10.1016/j.tma.2018.08.002 · Cited by 27 · see citing works
Abdel-Rahman, F., Okeremgbo, B., Alhamadah, F., Jamadar, S., Anthony, K. P., & SALEH, M. A. (2017) · Journal of Environmental Science and Health Part A · doi:10.1080/10934529.2016.1270676 · Cited by 26 · see citing works
Nguyen, T. L., & SALEH, M. A. (2019) · Journal of Environmental Science and Health Part A · doi:10.1080/10934529.2018.1562810 · Cited by 25 · see citing works
Ke, J., Yu, J.-Y., Gao, B., Hu, F., Xu, F., Yao, G., & Bao, G. (2022) · Food & Function · doi:10.1039/d2fo01795d · Cited by 24 · see citing works
C. elegans screening strategies to identify pro-longevity interventions
Maglioni, S., Arsalan, N., & Ventura, N. (2016) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2016.07.010 · Cited by 24 · see citing works
Unraveling anti-aging mystery of green tea in C. elegans: Chemical truth and multiple mechanisms
Ke, J., Li, J.-Y., Yang, Z. M., Wu, H.-Y., Yu, J.-Y., Yang, Y., Chen, C., Zhou, P., Hua, F., Wang, W., et al. (2024) · Food Chemistry · doi:10.1016/j.foodchem.2024.140510 · Cited by 23 · see citing works
Zheng, F., Chen, P., Li, H., & Aschner, M. (2020) · Toxicological Sciences · doi:10.1093/toxsci/kfaa105 · Cited by 23 · see citing works
Microfluidic devices for disease modeling in muscle tissue
Smoak, M. M., Pearce, H. A., & Mikos, A. G. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.08.059 · Cited by 21 · see citing works
Li, J., Cui, X., Ma, X., & Wang, Z. (2017) · Experimental Gerontology · doi:10.1016/j.exger.2017.01.018 · Cited by 19 · see citing works
Guerrero‐Rubio, M. A., Hernández‐García, S., García‐Carmona, F., & Gandía‐Herrero, F. (2023) · Food Research International · doi:10.1016/j.foodres.2023.112925 · Cited by 18 · see citing works
Fox, B. C., Slade, L., Torregrossa, R., Pacitti, D., Szabó, C., Etheridge, T., & Whiteman, M. (2020) · Journal of Inherited Metabolic Disease · doi:10.1002/jimd.12345 · Cited by 17 · see citing works
Traditional and novel tools to probe the mitochondrial metabolism in health and disease
Zhang, Y., & Avalos, J. L. (2017) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1373 · Cited by 17 · see citing works
Lee, M. B., Blue, B. W., Muir, M., & Kaeberlein, M. R. (2023) · GeroScience · doi:10.1007/s11357-023-00867-6 · Cited by 15 · see citing works
C. elegans to model autophagy-related human disorders
Wong, S. Q., Kumar, A. V., Mills, J., & Lapierre, L. R. (2020) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2020.01.007 · Cited by 14 · see citing works
Ji, J., Jiang, Y. G., Guo, X., Ji, R., Quan, Q., Ding, M., Li, X., & Liu, Y. (2019) · Cancer Cell International · doi:10.1186/s12935-019-0880-4 · Cited by 14 · see citing works
Thosapornvichai, T., Huangteerakul, C., Jensen, A. N., & Jensen, L. T. (2022) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2022.104000 · Cited by 11 · see citing works
Ficociello, G., Schifano, E., Nottia, M. D., Torraco, A., Carrozzo, R., Uccelletti, D., & Montanari, A. (2022) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2022.130255 · Cited by 11 · see citing works
Chen, L., Chen, G., Gai, T., Zhou, X., Zhu, J., Wang, R., Wang, X., Guo, Y., Wang, Y., & Xie, Z. (2024) · Molecules · doi:10.3390/molecules29112691 · Cited by 10 · see citing works
Detection of Mitochondrial Toxicity of Environmental Pollutants UsingCaenorhabditis elegans
Maurer, L. L., Luz, A. L., & Meyer, J. N. (2018) · Wiley eBooks · doi:10.1002/9781119329725.ch43 · Cited by 9 · see citing works
Mello, D. F., Perez, L., Bergemann, C. M., Morton, K. S., Ryde, I. T., & Meyer, J. N. (2024) · PLoS ONE · doi:10.1371/journal.pone.0306849 · Cited by 8 · see citing works
Comparative analysis of Ancylostoma ceylanicum mitochondrial genome with other Ancylostoma species
Shi, X., Wang, M., Abdullahi, A. Y., Fu, Y., Yang, F., Yu, X., Pan, W., Yan, X., Hang, J., Zhang, P., et al. (2018) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2018.04.012 · Cited by 8 · see citing works
Martorell, P., Llopis, S., Gil, J. V., Genovés, S., Ramón, D., Zacarı́as, L., & Rodrigo, M. J. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9952-1_29 · Cited by 7 · see citing works
Huang, Y., Zheng, X., Zhang, H., Ding, H., Guo, X., Yang, Y., Chen, X., Zhou, Q., & Du, A. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.02176 · Cited by 6 · see citing works
Zheng, F., Aschner, M., & Li, H. (2021) · Methods in molecular biology · doi:10.1007/978-1-0716-1514-0_3 · Cited by 6 · see citing works
Caenorhabditis elegans as a Model System for Environmental Mitotoxicants
Akinrinde, A. S., Sanchez, L. A., Maglioni, S., & Ventura, N. (2025) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-062124-012254 · Cited by 5 · see citing works
Paredes, G. F., Viehboeck, T., Markert, S., Mausz, M. A., Sato, Y., Liebeke, M., König, L., & Bulgheresi, S. (2022) · Scientific Reports · doi:10.1038/s41598-022-13235-9 · Cited by 5 · see citing works
Knockdown of Gastrin Promotes Apoptosis of Gastric Cancer Cells by Decreasing ROS Generation
Liu, Y., Zhu, J., Liu, J., Ma, X., Zhao, J., & Su, Z. (2021) · BioMed Research International · doi:10.1155/2021/5590037 · Cited by 4 · see citing works
Lack of detectable sex differences in the mitochondrial function of Caenorhabditis elegans
King, D. E., Sparling, A. C., Joyce, A. S., Ryde, I. T., deSouza, B., Ferguson, P. L., Murphy, S. K., & Meyer, J. N. (2024) · BMC Ecology and Evolution · doi:10.1186/s12862-024-02238-x · Cited by 3 · see citing works
Mitochondrial complex I deficiency-associated diseases and models
Jentsch, L., & Ventura, N. (2026) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-026-06169-2 · Cited by 2 · see citing works
Darvesh, A. S., Barnett, R. E., & Fitsanakis, V. A. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-821038-3.00028-8 · Cited by 2 · see citing works
Perlstein, E. O. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.01.08.899666 · Cited by 2 · see citing works
Sánchez-Camacho, J. V., Gómez-Chavarı́n, M., Galindo-Solano, N., Padilla-Cortés, P., Maldonado-García, J. L., Pérez‐Sánchez, G., Pavón, L., Ramírez‐Santos, J., Roldán-Roldán, G., Gómez‐López, M., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252312635 · Cited by 1 · see citing works
A novel C. elegans respirometry assay using low-cost optical oxygen sensors
Dennis, N., Gourlay, C. W., & Ezcurra, M. (2025) · Biology Methods and Protocols · doi:10.1093/biomethods/bpaf072 · Cited by 1 · see citing works
Animal Models of Mitochondrial Diseases Associated with Nuclear Gene Mutations
Averina, O. A., Kuznetsova, S. A., Permyakov, O. A., & Владимирович, С. П. (2024) · Acta Naturae · doi:10.32607/actanaturae.25442 · Cited by 1 · see citing works
Methods and models for functional studies on mtDNA mutations
Iommarini, L., Ghelli, A. M., & Díaz, F. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-819656-4.00013-9 · Cited by 1 · see citing works
González-Hunt, C. P. (2017) · DukeSpace (Duke University)
Motwani, S., Bhandari, S., Chitkara, S., Ujjainiya, R., Sengupta, S., & Mukhopadhyay, A. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.07.11.664440
King, D. E., Sparling, A. C., Joyce, A. S., Ryde, I. T., deSouza, B., Ferguson, P. L., Murphy, S. K., & Meyer, J. N. (2024) · Figshare · doi:10.6084/m9.figshare.25698146
Utilisation du modèle levure pour la recherche de voies thérapeutiques contre le syndrome de Barth
de Tilques, M. D. T. (2017) · theses.fr (ABES) · doi:10.70675/db54cf9cz39cdz47d7z9aabz808ab0c7b1c7
Ventura, N., Jentsch, L., Maglioni, S., Jerred, C., O'Hara, T., Mytilinaiou, E., Ruiz, J., Schaumkessel, Y., Schroeter, L., Jung, J., et al. (2026) · Research Square · doi:10.21203/rs.3.rs-10539896/v1
- Authors
- Maglioni, S., & Ventura, N.
- Affiliations
- Leibniz Institute of Environmental Medicine (DE)
- Corresponding author
- Ventura, Natascia
- Venue
- Mitochondrion
- Publisher
- Elsevier BV
- Published
- 2016-09
- Volume
- 30
- Pages
- 117-125
- ISSN
- 1567-7249 (ISSN-L)
- OpenAlex
- W2274068909
- Cited by
- 54
- References
- 119
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 7 · 2023: 4 · 2022: 7 · 2021: 4 · 2020: 5 · 2019: 5 · 2018: 6 · 2017: 9 · 2016: 2
- FWCI
- 0.66
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Mitochondrion (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- Caenorhabditis elegans, mitochondrial disease, mitochondrial dysfunction, mitochondrial quality control, neurodegenerative diseases, model organisms, therapeutic screening, mitochondrial homeostasis
- MeSH terms
- Animals, Disease Models, Animal, Humans, Muscular Diseases, Caenorhabditis elegans, Neurodegenerative Diseases, Mitochondrial Diseases
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