Mitochondrial Signaling

Butow, Ronald A; Avadhani, Narayan G

doi:10.1016/s1097-2765(04)00179-0

Cited by 882Mitochondrial Function and PathologyAutophagy in Disease and TherapyMetabolism, Diabetes, and Cancer

Mitochondrial Signaling

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Butow, Ronald A, Avadhani, Narayan G·2004·Molecular Cell

DOI 10.1016/s1097-2765(04)00179-0

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Abstract

Mitochondrial retrograde signaling is a pathway of communication from mitochondria to the nucleus that influences many cellular and organismal activities under both normal and pathophysiological conditions. In yeast it is used as a sensor of mitochondrial dysfunction that initiates readjustments of carbohydrate and nitrogen metabolism. In both yeast and animal cells, retrograde signaling is linked to TOR signaling, but the precise connections are unclear. In mammalian cells, mitochondrial dysfunction sets off signaling cascades through altered Ca(2+) dynamics, which activate factors such as NFkappaB, NFAT, and ATF. Retrograde signaling also induces invasive behavior in otherwise nontumorigenic cells implying a role in tumor progression.

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In S. cerevisiae, the Rtg transcription factors were known as the model and best understood example of retrograde mitonuclear signaling.
“Whereas in S. cerevisiae the Rtg transcription factors were known as the model and best understood example of the retrograde mitonuclear signaling (Butow and Avadhani 2004; Liu and Butow 2006)”
From Mitochondrial retrograde control of transcription evolves with respiratory stress, metabolic adaptation, and virulence in budding yeasts (2026) · cites this paper as Butow and Avadhani 2004
The paper describes Rtg1p and Rtg3p as a yeast transcriptional complex that activates retrograde-response genes, and calls CIT2 a prototypical readout of that response (passages labeled Abstract; page unavailable). This supports the RTG pathway as an established example of mitochondria-to-nucleus signaling, but the passages do not establish the comparative claim that it was the best-understood example. (LLM, conf=0.78)
Experimental — accuracy not yet measured
MITF is not involved in mitonuclear signaling.
“The human homolog of Rtg3p is the microphthalmia-associated transcription factor (MITF) (Goding and Arnheiter 2019), which is not involved in mitonuclear signaling that in Metazoa evolved independently and uses different mechanisms (Butow and Avadhani 2004; Jazwinski 2014; English et al. 2020).”
From Mitochondrial retrograde control of transcription evolves with respiratory stress, metabolic adaptation, and virulence in budding yeasts (2026) · cites this paper as Butow and Avadhani 2004
The Abstract and Concluding Remarks (pages unavailable) describe yeast retrograde signaling through RTG factors and mammalian signaling through altered Ca2+ dynamics and factors such as NFκB, NFAT, and ATF. That supports a difference in the mechanisms discussed, but the copy does not say that MITF is uninvolved or that metazoan signaling evolved independently (searched: MITF, microphthalmia, metazoan signaling). (LLM, conf=0.78)
Experimental — accuracy not yet measured
Metazoan mitonuclear signaling evolved independently and uses different mechanisms.
“The human homolog of Rtg3p is the microphthalmia-associated transcription factor (MITF) (Goding and Arnheiter 2019), which is not involved in mitonuclear signaling that in Metazoa evolved independently and uses different mechanisms (Butow and Avadhani 2004; Jazwinski 2014; English et al. 2020).”
From Mitochondrial retrograde control of transcription evolves with respiratory stress, metabolic adaptation, and virulence in budding yeasts (2026) · cites this paper as Butow and Avadhani 2004
The Concluding Remarks describe different signaling machinery in yeast and mammalian cells: yeast regulatory factors versus calcium-dependent cascades activating NFκB, NFAT, and ATF. They do not say that metazoan mitonuclear signaling evolved independently; they also note a link to TOR signaling in both groups. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Replenishment of glutamate and acetyl CoA in TCA and alternative nitrogen uptake are signatures of a successful compensation for mitochondrial inefficiency via retrograde regulation.
“Nevertheless, the replenishment of glutamate and acetyl CoA in TCA and alternative nitrogen uptake are the signatures of a “successful” compensation for mitochondrial inefficiency via retrograde regulation (33), which seem to be reflected in resistant C. albicans here.”
From Divergent mitochondrial responses and metabolic signal pathways secure the azole resistance in Crabtree-positive and negative Candida species (2024) · cites this paper as [33]

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Yeast Life-Span Extension by Calorie Restriction Is Independent of NAD Fluctuation
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The 14‐3‐3 Proteins Encoded by the BMH1 and BMH2 Genes are Essential in the Yeast Saccharomyces cerevisiae and Can be Replaced by a Plant Homologue
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Diminished tumorigenic phenotype after depletion of mitochondrial DNA.
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Ammonia pulses and metabolic oscillations guide yeast colony development.
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A Conserved Motif Present in a Class of Helix-Loop-Helix Proteins Activates Transcription by Direct Recruitment of the SAGA Complex
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Retrograde signaling is regulated by the dynamic interaction between Rtg2p and Mks1p
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Control of Amino Acid Permease Sorting in the Late Secretory Pathway of Saccharomyces cerevisiae by SEC13, LST4, LST7 and LST78
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The Saccharomyces cerevisiae OXA1 gene is required for the correct assembly of cytochrome c oxidase and oligomycin‐sensitive ATP synthase
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Compromised mitochondrial function leads to increased cytosolic calcium and to activation of MAP kinases
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LST8 negatively regulates amino acid biosynthesis as a component of the TOR pathway
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Structural Organization and Transcription Regulation of Nuclear Genes Encoding the Mammalian Cytochrome c Oxidase Complex
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RTG genes in yeast that function in communication between mitochondria and the nucleus are also required for expression of genes encoding peroxisomal proteins
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Mks1 in Concert with TOR Signaling Negatively Regulates RTG Target Gene Expression in S. cerevisiae
Dilova, I., Chen, C., & Powers, T. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00677-2 · Cited by 123 · see citing works
Global Transcription Analysis of Krebs Tricarboxylic Acid Cycle Mutants Reveals an Alternating Pattern of Gene Expression and Effects on Hypoxic and Oxidative Genes
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Control of Mitochondrial Respiration by NO., Effects of Low Oxygen and Respiratory State
Brookes, P. S., Kraus, D. W., Shiva, S., Doeller, J. E., Barone, M.-C., Patel, R. P., Lancaster, J. R., & Darley-Usmar, V. M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211784200 · Cited by 118 · see citing works
RTG‐dependent mitochondria to nucleus signaling is negatively regulated by the seven WD‐repeat protein Lst8p
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Expression of mtDNA and nDNA encoded respiratory chain proteins in chemically and genetically-derived Rho0 human fibroblasts: a comparison of subunit proteins in normal fibroblasts treated with ethidium bromide and fibroblasts from a patient with mtDNA depletion syndrome
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RTG-dependent Mitochondria-to-Nucleus Signaling Is Regulated by MKS1 and Is Linked to Formation of Yeast Prion [URE3]
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Localization of glucocorticoid hormone receptors in mitochondria of human cells
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Cyclic AMP‐Responsive Element Binding Protein in Brain Mitochondria
Cammarota, M., Paratcha, G., Bevilaqua, L. R., de Stein, M. L., López, M., de Iraldi, A. P., Izquierdo, I., & Medina, J. H. (1999) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1999.0722272.x · Cited by 97 · see citing works
Tumorigenicity and its suppression in cybrids of mouse and Chinese hamster cell lines.
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The role of the yeast plasma membrane SPS nutrient sensor in the metabolic response to extracellular amino acids
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Amino acids regulate the intracellular trafficking of the general amino acid permease of Saccharomyces cerevisiae
Chen, E. J., & Kaiser, C. A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.232591899 · Cited by 95 · see citing works
Origins and Consequences of Mitochondrial Variation in Vertebrate Muscle
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The Tup1-Cyc8 Protein Complex Can Shift from a Transcriptional Co-repressor to a Transcriptional Co-activator
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The basal promoter elements of murine cytochrome c oxidase subunit IV gene consist of tandemly duplicated ets motifs that bind to GABP-related transcription factors
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Self-citation
Saccharomyces cerevisiae Multidrug Resistance Gene Expression Inversely Correlates with the Status of the F0Component of the Mitochondrial ATPase
Zhang, X., & Moye-Rowley, W. S. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m106285200 · Cited by 84 · see citing works
Growing Old: Metabolic Control and Yeast Aging
Jazwinski, S. M. (2002) · Annual Review of Microbiology · doi:10.1146/annurev.micro.56.012302.160830 · Cited by 79 · see citing works
Mks1p Is Required for Negative Regulation of Retrograde Gene Expression in Saccharomyces cerevisiae but Does Not Affect Nitrogen Catabolite Repression-sensitive Gene Expression
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Calcium-regulated changes in mitochondrial phenotype in skeletal muscle cells
Freyssenet, D. G., Irrcher, I., Connor, M. K., DiCarlo, M., & Hood, D. A. (2004) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00418.2003 · Cited by 62 · see citing works
ATO3 encoding a putative outward ammonium transporter is an RTG-independent retrograde responsive gene regulated by GCN4 and the Ssy1-Ptr3-Ssy5 amino acid sensor system
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Self-citation
Tor1/2 Regulation of Retrograde Gene Expression in Saccharomyces cerevisiae Derives Indirectly as a Consequence of Alterations in Ammonia Metabolism
Tate, J. J., & Cooper, T. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301829200 · Cited by 49 · see citing works
The HAP2,3,4 transcriptional activator is required for derepression of the yeast citrate synthase gene, CIT1
Rosenkrantz, M. S., Keil, C. S., Pennell, E. A., & Devenish, L. J. (1994) · Molecular Microbiology · doi:10.1111/j.1365-2958.1994.tb00407.x · Cited by 47 · see citing works
Quinones in long‐lived clk‐1 mutants of Caenorhabditis elegans
Miyadera, H., Kano, K., Miyoshi, H., Ishii, N., Hekimi, S., & Kita, K. (2002) · FEBS Letters · doi:10.1016/s0014-5793(02)02282-2 · Cited by 46 · see citing works
Bioenergetics in cardiac hypertrophy: mitochondrial respiration as a pathological target of NO·
Dai, L., Brookes, P. S., Darley-Usmar, V. M., & Anderson, P. G. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.281.6.h2261 · Cited by 44 · see citing works
Up-regulation of nuclear genes in response to inhibition of mitochondrial DNA expression in chicken cells
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Yeast protein controlling inter-organelle communication is related to bacterial phosphatases containing the Hsp70-type ATP-binding domain
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The RAS genes: a homeostatic device in Saccharomyces cerevisiae longevity☆
Jazwinski, S. M. (1999) · Neurobiology of Aging · doi:10.1016/s0197-4580(99)00095-0 · Cited by 41 · see citing works
On suppression of tumorigenicity in hybrid and cybrid mouse cells
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Identification of RTG2 as a Modifier Gene for CTG·CAG Repeat Instability in Saccharomyces cerevisiae
Bhattacharyya, S., Rolfsmeier, M. L., Dixon, M. J., Wagoner, K., & Lahue, R. S. (2002) · Genetics · doi:10.1093/genetics/162.2.579 · Cited by 25 · see citing works

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Transcriptional paradigms in mammalian mitochondrial biogenesis and function
Scarpulla, R. C. (2008) · Physiological Reviews · doi:10.1152/physrev.00025.2007 · Cited by 1,666 · see citing works
Feedback between p21 and reactive oxygen production is necessary for cell senescence
Passos, J. F., Nelson, G., Wang, C., Richter, T., Simillion, C., Proctor, C. J., Miwa, S., Olijslagers, S., Hallinan, J., Wipat, A., et al. (2010) · Molecular Systems Biology · doi:10.1038/msb.2010.5 · Cited by 1,019 · see citing works
“Mitochondrial dysfunction including ROS production induces retrograde response, a major reprogramming of nuclear gene expression patterns, in senescent cells (Butow and Avadhani, 2004; Passos et al, 2007a, c).”
Oxidation events and skin aging
Kammeyer, A., & Luiten, R. M. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2015.01.001 · Cited by 980 · see citing works
Mitochondrial dysfunction accounts for the stochastic heterogeneity in telomere-dependent senescence
Passos, J. F., Saretzki, G., Ahmed, S., Nelson, G., Richter, T., Peters, H., Wappler, I., Birket, M. J., Harold, G., Schaeuble, K., et al. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050110 · Cited by 796 · see citing works
“Retrograde signalling includes up-regulation of mitochondrial biosynthesis via PGC-1 and PPAR-c, major metabolic and anti-apoptotic adjustments, and possible interaction with TOR signalling [27].”
BackgroundInfluential
Sirtuin regulation of mitochondria: energy production, apoptosis, and signaling
Verdin, E., Hirschey, M. D., Finley, L. W. S., & Haigis, M. C. (2010) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2010.07.003 · Cited by 661 · see citing works
Initiating Cellular Stress Responses
Bakkenist, C. J., & Kastan, M. B. (2004) · Cell · doi:10.1016/j.cell.2004.06.023 · Cited by 544 · see citing works
Reduced TOR Signaling Extends Chronological Life Span via Increased Respiration and Upregulation of Mitochondrial Gene Expression
Bonawitz, N. D., Chatenay-Lapointe, M., Pan, Y., & Shadel, G. S. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.02.009 · Cited by 422 · see citing works
Extension of Drosophila Life Span by RNAi of the Mitochondrial Respiratory Chain
Copeland, J. M., Cho, J., Lo, T., Hur, J. H., Bahadorani, S., Arabyan, T., Rabie, J., Soh, J., & Walker, D. W. (2009) · Current Biology · doi:10.1016/j.cub.2009.08.016 · Cited by 409 · see citing works
Effects of ionizing radiation on mitochondria
Kam, W. W.-Y., & Banati, R. B. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.07.024 · Cited by 386 · see citing works
Epigenetic modification of liver mitochondrial DNA is associated with histological severity of nonalcoholic fatty liver disease
Pirola, C. J., Gianotti, T. F., Burgueño, A. L., Rey-Funes, M., Loidl, C. F., Mallardi, P., Martino, J. S., Castaño, G. O., & Sookoian, S. (2013) · Gut · doi:10.1136/gutjnl-2012-302962 · Cited by 364 · see citing works
Interactions between ROS and AMP kinase activity in the regulation of PGC-1α transcription in skeletal muscle cells
Irrcher, I., Ljubicic, V., & Hood, D. A. (2009) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00267.2007 · Cited by 356 · see citing works
Nitric Oxide and Mitochondrial Signaling: From Physiology to Pathophysiology
Erusalimsky, J. D., & Moncada, S. (2007) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.107.151167 · Cited by 336 · see citing works
Mitochondria, Oxidative Stress and Innate Immunity
Chen, Y., Zhou, Z., & Min, W. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01487 · Cited by 315 · see citing works
The hallmarks of fibroblast ageing
Tigges, J., Krutmann, J., Fritsche, E., Haendeler, J., Schaal, H., Fischer, J. W., Kalfalah, F., Reinke, H., Reifenberger, G., Stühler, K., et al. (2014) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2014.03.004 · Cited by 250 · see citing works
Mitochondrial dysfunction and damage associated molecular patterns (DAMPs) in chronic inflammatory diseases
Dela Cruz, C. S., & Kang, M.-J. (2018) · Mitochondrion · doi:10.1016/j.mito.2017.12.001 · Cited by 255 · see citing works
The coordination of nuclear and mitochondrial communication during aging and calorie restriction
Finley, L. W. S., & Haigis, M. C. (2009) · Ageing Research Reviews · doi:10.1016/j.arr.2009.03.003 · Cited by 207 · see citing works
Thyroid Hormone Effects on Mitochondrial Energetics
Harper, M.-E., & Seifert, E. L. (2008) · Thyroid · doi:10.1089/thy.2007.0250 · Cited by 194 · see citing works
Mitohormesis in exercise training
Merry, T. L., & Ristow, M. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.11.032 · Cited by 176 · see citing works
The retrograde response: When mitochondrial quality control is not enough
Jazwinski, S. M. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2012.02.010 · Cited by 172 · see citing works
Senescence in Post-Mitotic Cells: A Driver of Aging?
von Zglinicki, T., Wan, T., & Miwa, S. (2021) · Antioxidants & Redox Signaling · doi:10.1089/ars.2020.8048 · Cited by 170 · see citing works
A Regulated Response to Impaired Respiration Slows Behavioral Rates and Increases Lifespan in Caenorhabditis elegans
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
Dietary restriction.; mitochondrial function and aging: From yeast to humans
Ruetenik, A., & Barrientos, A. (2015) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2015.05.005 · Cited by 139 · see citing works
Quantitative mitochondrial DNA copy number determination using droplet digital PCR with single-cell resolution
O'Hara, R., Tedone, E., Ludlow, A., Huang, E., Arosio, B., Mari, D., & Shay, J. W. (2019) · Genome Research · doi:10.1101/gr.250480.119 · Cited by 121 · see citing works
From cell senescence to age-related diseases: differential mechanisms of action of senescence-associated secretory phenotypes
Byun, H.-O., Lee, Y.-K., Kim, J.-M., & Yoon, G. (2015) · BMB Reports · doi:10.5483/bmbrep.2015.48.10.122 · Cited by 115 · see citing works
Metabolic features and regulation in cell senescence
Kwon, S. M., Hong, S. M., Lee, Y.-K., Min, S., & Yoon, G. (2019) · BMB Reports · doi:10.5483/bmbrep.2019.52.1.291 · Cited by 111 · see citing works
“restore mitochondrial function, activate an alternative energy supply, modify cellular function, and change cellular fate to death, senescence, or proliferation (42, 44-47).”
Background
Cellular and mitochondrial remodeling upon defects in iron-sulfur protein biogenesis
Hausmann, A., Samans, B., Lill, R., & Mühlenhoff, U. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m705570200 · Cited by 111 · see citing works
Mitochondrial signaling, TOR, and life span
Schieke, S. M., & Finkel, T. (2006) · Biological Chemistry · doi:10.1515/bc.2006.170 · Cited by 106 · see citing works
Metabolic-State-Dependent Remodeling of the Transcriptome in Response to Anoxia and Subsequent Reoxygenation in Saccharomyces cerevisiae
Lai, L.-C., Kosorukoff, A. L., Burke, P. V., & Kwast, K. E. (2006) · Eukaryotic Cell · doi:10.1128/ec.00107-06 · Cited by 97 · see citing works
Partial depletion of mitochondrial DNA from human skin fibroblasts induces a gene expression profile reminiscent of photoaged skin
Schroeder, P., Gremmel, T., Berneburg, M., & Krutmann, J. (2008) · Journal of Investigative Dermatology · doi:10.1038/jid.2008.57 · Cited by 85 · see citing works
Mitochondrial dysfunction induces aberrant insulin signalling and glucose utilisation in murine C2C12 myotube cells
Lim, J. H., Lee, J. I., Suh, Y. H., Kim, W., Song, J. H., & Jung, M. H. (2006) · Diabetologia · doi:10.1007/s00125-006-0278-4 · Cited by 81 · see citing works
Alcohol alters hepatic FoxO1, p53, and mitochondrial SIRT5 deacetylation function
Lieber, C. S., Leo, M. A., Wang, X., & DeCarli, L. M. (2008) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2008.06.006 · Cited by 71 · see citing works
The Retrograde Response
Jazwinski, S. M. (2014) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-394625-6.00005-2 · Cited by 67 · see citing works
Mitochondrial Matrix Ca2+ Accumulation Regulates Cytosolic NAD+/NADH Metabolism, Protein Acetylation, and Sirtuin Expression
Marcu, R., Wiczer, B. M., Neeley, C. K., & Hawkins, B. J. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.00068-14 · Cited by 62 · see citing works
Convergent mechanisms for dysregulation of mitochondrial quality control in metabolic disease: implications for mitochondrial therapeutics
Mitchell, T., Chacko, B., Ballinger, S. W., Bailey, S. M., Zhang, J., & Darley-Usmar, V. (2013) · Biochemical Society Transactions · doi:10.1042/bst20120231 · Cited by 57 · see citing works
Mitochondrial respiration and reactive oxygen species in mitochondrial aging mutants
SEDENSKY, M., & GMORGAN, P. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2006.01.004 · Cited by 57 · see citing works
The role of mitochondria in <scp>mTOR</scp>‐regulated longevity
Wei, Y., Zhang, Y., Cai, Y., & Xu, M. (2015) · Biological Reviews · doi:10.1111/brv.12103 · Cited by 56 · see citing works
Yeast growth in raffinose results in resistance to acetic acid induced programmed cell death mostly due to the activation of the mitochondrial retrograde pathway
Guaragnella, N., Ždralević, M., Lattanzio, P., Marzulli, D., Pracheil, T., Liu, Z., Passarella, S., Marra, E., & Giannattasio, S. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2013.07.017 · Cited by 52 · see citing works
Differential Roles of Transcriptional Mediator Subunits in Regulation of Multidrug Resistance Gene Expression inSaccharomyces cerevisiae
Shahi, P., Gulshan, K., Näär, A. M., & Moye-Rowley, W. S. (2010) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-10-0899 · Cited by 49 · see citing works
The TOM complex is involved in the release of superoxide anion from mitochondria
Budzińska, M., Gałgańska, H., Karachitos, A., Wojtkowska, M., & Kmita, H. (2009) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-009-9231-9 · Cited by 31 · see citing works
Proteome and cytoskeleton responses in osteosarcoma cells with reduced OXPHOS activity
Annunen‐Rasila, J., Ohlmeier, S., Tuokko, H., Veijola, J., & Majamaa, K. (2007) · PROTEOMICS · doi:10.1002/pmic.200601031 · Cited by 31 · see citing works
Mutations in Two Zinc-Cluster Proteins Activate Alternative Respiratory and Gluconeogenic Pathways and Restore Senescence in Long-Lived Respiratory Mutants ofPodospora anserina
Sellem, C. H., Bovier, E., Lorin, S., & Sainsard-Chanet, A. (2009) · Genetics · doi:10.1534/genetics.109.100834 · Cited by 27 · see citing works
The putative transcription factor CaRtg3 is involved in tolerance to cations and antifungal drugs as well as serum-induced filamentation inCandida albicans
Yan, H., Zhao, Y., & Jiang, L. (2014) · FEMS Yeast Research · doi:10.1111/1567-1364.12148 · Cited by 25 · see citing works
Role of Mitochondria in Regulating Lutein and Chlorophyll Biosynthesis in Chlorella pyrenoidosa under Heterotrophic Conditions
Liu, Z.-H., Li, T., He, Q.-Y., Sun, Z., & Jiang, Y. (2018) · Marine Drugs · doi:10.3390/md16100354 · Cited by 19 · see citing works
Investigation of regulatory factors required for alternative oxidase production in Neurospora crassa
Chae, M. S., & Nargang, F. E. (2009) · Physiologia Plantarum · doi:10.1111/j.1399-3054.2009.01239.x · Cited by 17 · see citing works
The nuclear transcription factor Rtg1p functions as a cytosolic, post-transcriptional regulator in the methylotrophic yeast Pichia pastoris
Dey, T., Krishna Rao, K., Khatun, J., & Rangarajan, P. N. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.004486 · Cited by 16 · see citing works
Divergent mitochondrial responses and metabolic signal pathways secure the azole resistance in Crabtree-positive and negative Candida species
Zhou, M., Peng, J., Ren, K., Yu, Y., Li, D., She, X., & Liu, W. (2024) · Microbiology Spectrum · doi:10.1128/spectrum.04042-23 · Cited by 13 · see citing works
Mitochondrial retrograde control of transcription evolves with respiratory stress, metabolic adaptation, and virulence in budding yeasts
Łabędzka-Dmoch, K., Bui, T. H. D., Piątkowski, J., Dilling, M., Jagiełło, P., Kabza, W., & Golik, P. (2026) · Molecular Biology and Evolution · doi:10.1093/molbev/msag005 · Cited by 1 · see citing works

Defining the momiome: Promiscuous information transfer by mobile mitochondria and the mitochondrial genome
Singh, B., Modica-Napolitano, J. S., & Singh, K. K. (2017) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2017.05.004 · Cited by 49 · see citing works
Retrograde Signaling: A New Candidate Signaling Molecule
Eckardt, N. A. (2011) · The Plant Cell · doi:10.1105/tpc.111.231113 · Cited by 5 · see citing works
How do yeast sense mitochondrial dysfunction?
Кнорре, Д. А., Соколов, С. С., Zyrina, A. N., & Severin, F. F. (2016) · Microbial Cell · doi:10.15698/mic2016.11.537 · Cited by 39 · see citing works
Specificity in signaling pathways: assembly into multimolecular signaling complexes
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ROS as Signaling Molecule Under Unfavorable Conditions
Sachdev, S., Ansari, S. A., & Ansari, M. I. (2023) · Springer eBooks · doi:10.1007/978-981-19-9884-3_11 · Cited by 1 · see citing works

Authors: Butow, R. A., & Avadhani, N. G.
Affiliations: The University of Texas Southwestern Medical Center (US)
University of Pennsylvania (US)
Corresponding author: Butow, Ronald A
ORCID: Avadhani, Narayan G
Venue: Molecular Cell
Publisher: Elsevier BV
Published: 2004-04
Volume: 14
Issue: 1
Pages: 1-15
ISSN: 1097-2765 (ISSN-L)
DOI: 10.1016/s1097-2765(04)00179-0
OpenAlex: W1548851567
Cited by: 882
References: 118
Citations by year: 2026: 35 · 2025: 27 · 2024: 26 · 2023: 27 · 2022: 29 · 2021: 25 · 2020: 34 · 2019: 35 · 2018: 32 · 2017: 37 · 2016: 32 · 2015: 48 · 2014: 46 · 2013: 51 · 2012: 54
FWCI: 3.99
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 3394 d)
Locations: Molecular Cell (publishedVersion)
PubMed (publishedVersion)
Funders: National Cancer Institute (CA 22762)
National Institute of General Medical Sciences (GM22525)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Keywords: mitochondrial retrograde signaling, mitochondrial-nuclear communication, mitochondrial dysfunction, TOR signaling, calcium dynamics, NF-κB, NFAT, ATF, tumor progression, yeast
MeSH terms: Aging, Animals, Carrier Proteins, Cell Nucleus, Gene Expression Regulation, Humans, Mitochondria, Saccharomyces cerevisiae, Transcription Factors, Signal Transduction, Phosphotransferases (Alcohol Group Acceptor), Phosphatidylinositol 3-Kinases, Saccharomyces cerevisiae Proteins, Intracellular Signaling Peptides and Proteins

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