Control of mitochondrial motility and distribution by the calcium signal

Mitochondria are dynamic organelles in cells. The control of mitochondrial motility by signaling mechanisms and the significance of rapid changes in motility remains elusive. In cardiac myoblasts, mitochondria were observed close to the microtubular array and displayed both short- and long-range movements along microtubules. By clamping cytoplasmic [Ca2+] ([Ca2+]c) at various levels, mitochondrial motility was found to be regulated by Ca2+ in the physiological range. Maximal movement was obtained at resting [Ca2+]c with complete arrest at 1–2 μM. Movement was fully recovered by returning to resting [Ca2+]c, and inhibition could be repeated with no apparent desensitization. The inositol 1,4,5-trisphosphate– or ryanodine receptor-mediated [Ca2+]c signal also induced a decrease in mitochondrial motility. This decrease followed the spatial and temporal pattern of the [Ca2+]c signal. Diminished mitochondrial motility in the region of the [Ca2+]c rise promotes recruitment of mitochondria to enhance local Ca2+ buffering and energy supply. This mechanism may provide a novel homeostatic circuit in calcium signaling.

• Publication year

  2004

• Venue

  Journal of Cell Biology

• Publication date

  2004-11-22

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1083/jcb.200406038PMID 15545319PMCID 2172592
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Cytoplasmic dynein regulates the subcellular distribution of mitochondria by controlling the recruitment of the fission factor dynamin-related protein-1

  2004influential reference
• Myosin V

  2004cited by this paper
• Flirting in Little Space: The ER/Mitochondria Ca2+ Liaison

  2004cited by this paper
• Myosin V: regulation by calcium, calmodulin, and the tail domain

  2004cited by this paper
• Stable Interactions between Mitochondria and Endoplasmic Reticulum Allow Rapid Accumulation of Calcium in a Subpopulation of Mitochondria*

  2003cited by this paper
• Glutamate Decreases Mitochondrial Size and Movement in Primary Forebrain Neurons

  2003cited by this paper
• Plasticity of Mitochondrial Calcium Signaling*

  2003cited by this paper
• Mechanisms of cytochrome c release by proapoptotic BCL-2 family members.

  2003cited by this paper
• Dynactin is required for bidirectional organelle transport

  2003cited by this paper
• Myosin-Va binds to and mechanochemically couples microtubules to actin filaments.

  2003cited by this paper
• Myosin Va and microtubule-based motors are required for fast axonal retrograde transport of tetanus toxin in motor neurons

  2003cited by this paper
• The molecular motor toolbox for intracellular transport.

  2003influential reference
• The Wellcome Prize Lecture

  2003cited by this paper
• Store-operated Ca2+ entry: dynamic interplay between endoplasmic reticulum, mitochondria and plasma membrane.

  2003cited by this paper
• Apoptosis--the Calcium Connection

  2003cited by this paper
• Expression of phosphatidylinositol (4,5) bisphosphate-specific pleckstrin homology domains alters direction but not the level of axonal transport of mitochondria.

  2003cited by this paper
• Structural and functional relationships between Ca 2 puffs and mitochondria in Xenopus oocytes

  2002cited by this paper
• Structural and functional relationships between Ca2+ puffs and mitochondria in Xenopus oocytes.

  2002cited by this paper
• Calcium signal compartmentalization.

  2002cited by this paper
• Old players in a new role: mitochondria-associated membranes, VDAC, and ryanodine receptors as contributors to calcium signal propagation from endoplasmic reticulum to the mitochondria.

  2002cited by this paper
• Ca2+ marks: Miniature calcium signals in single mitochondria driven by ryanodine receptors

  2002cited by this paper
• Propagation of the apoptotic signal by mitochondrial waves

  2001cited by this paper
• Circularly permuted green fluorescent proteins engineered to sense Ca2+

  2001cited by this paper
• A mitochondrial perspective on cell death.

  2001cited by this paper
• Perinuclear, perigranular and sub‐plasmalemmal mitochondria have distinct functions in the regulation of cellular calcium transport

  2001cited by this paper
• Mitochondrial Ca 2 1 Uptake Depends on the Spatial and Temporal Profile of Cytosolic Ca 2 1 Signals*

  2001cited by this paper
• Mitochondrial Ca2+ Uptake Depends on the Spatial and Temporal Profile of Cytosolic Ca2+ Signals*

  2001cited by this paper
• Immunolocalization of cytoplasmic dynein and dynactin subunits in cultured macrophages: enrichment on early endocytic organelles.

  2001cited by this paper
• ‘What nourishes me, destroys me’: towards a new mitochondrial biology

  2001cited by this paper
• High Affinity Binding of Brain Myosin-Va to F-actin Induced by Calcium in the Presence of ATP*

  2001cited by this paper
• Breaking the mitochondrial barrier

  2001cited by this paper
• Interaction of actin- and microtubule-based motors in squid axoplasm probed with antibodies to myosin V and kinesin.

  2000cited by this paper
• Mitochondria as all‐round players of the calcium game

  2000cited by this paper
• Calcium Signal Transmission between Ryanodine Receptors and Mitochondria*

  2000cited by this paper
• Chromaffin-cell stimulation triggers fast millimolar mitochondrial Ca2+ transients that modulate secretion

  2000cited by this paper
• Mitochondrial control of cell death

  2000cited by this paper
• Calcium Regulates the Association between Mitochondria and a Smooth Subdomain of the Endoplasmic Reticulum

  2000cited by this paper
• Mitochondria and calcium: from cell signalling to cell death

  2000influential reference
• Class V myosins.

  2000cited by this paper
• Dynamic mitochondria

  1999cited by this paper
• Quasi‐synaptic calcium signal transmission between endoplasmic reticulum and mitochondria

  1999cited by this paper
• Direct interaction of microtubule- and actin-based transport motors

  1999cited by this paper
• Integrating cytosolic calcium signals into mitochondrial metabolic responses

  1998cited by this paper
• Ca2+ Homeostasis in the Agonist-sensitive Internal Store: Functional Interactions Between Mitochondria and the ER Measured In Situ in Intact Cells

  1998influential reference
• A specific light chain of kinesin associates with mitochondria in cultured cells.

  1998cited by this paper
• Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria.

  1998cited by this paper
• Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses.

  1998influential reference
• Mitochondrial Regulation of Store-operated Calcium Signaling in T Lymphocytes

  1997cited by this paper
• Caffeine-induced Release of Intracellular Ca2+ from Chinese Hamster Ovary Cells Expressing Skeletal Muscle Ryanodine Receptor

  1997influential reference
• Dimerization of the Highly Conserved Light Chain Shared by Dynein and Myosin V*

  1997cited by this paper
• A Role for Calcium Influx in the Regulation of Mitochondrial Calcium in Endothelial Cells (*)

  1996cited by this paper
• Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons

  1995cited by this paper
• Decoding of cytosolic calcium oscillations in the mitochondria.

  1995cited by this paper
• KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria.

  1994cited by this paper
• Actin structure and function: roles in mitochondrial organization and morphogenesis in budding yeast and identification of the phalloidin-binding site.

  1993cited by this paper
• Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria.

  1993cited by this paper
• Immunocytochemical identification of cytoskeletal linkages to smooth muscle cell nuclei and mitochondria.

  1990cited by this paper
• Effect of microtubules and intermediate filaments on mitochondrial distribution.

  1983cited by this paper
• Organelle-cytoskeleton relationships in fibroblasts: mitochondria, Golgi apparatus, and endoplasmic reticulum in phases of movement and growth.

  1982cited by this paper
• Mitochondria are associated with microtubules and not with intermediate filaments in cultured fibroblasts.

  1982cited by this paper
• Cell Biology

  1964cited by this paper

• TRPV4 Deficiency Shifts Mitochondrial Dynamics Toward a Fragmented Morphology in Primary Microglia.

  2026cites this paper
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  2025cites this paper
• Mitochondrial position responds to glucose stimulation in a model of the pancreatic beta cell

  2025cites this paper
• The yin and yang of neuronal mitophagy: physiological functions and pathological implications in neurodevelopmental disorders

  2025cites this paper
• Miro1- a key player in β-cell function and mitochondrial dynamics under diabetes mellitus.

  2025cites this paper
• Longitudinal investigation of prostate tumor spheroid proliferation with dynamic line-field optical coherence tomography

  2025influential citation
• Mitochondrial Calcium Signaling in Hepatocyte Health and Disease.

  2025cites this paper
• The roles of mitochondria in global and local intracellular calcium signalling

  2025influential citation
• Structural-functional characterization of the MIRO1-TRAK1 complex

  2025cites this paper
• The intermediate filament protein GFAP regulates mitochondrial fission in astrocytes.

  2025cites this paper
• Death‐Associated Protein 3 Triggers Intrinsic Apoptosis via Miro1 Upon Inducing Intracellular Calcium Changes

  2025cites this paper
• Mitochondrial fission and fusion in neurodegenerative diseases:Ca2+ signalling.

  2025cites this paper
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  2025cites this paper
• Mitochondria-membranous organelle contacts at a glance.

  2025cites this paper
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  2025cites this paper
• Perinuclear mitochondrial clustering for mesenchymal-to-epithelial transition in pluripotency induction

  2025cites this paper
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  2025cites this paper
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  2024cites this paper
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  2024cites this paper
• Neuronal activity inhibits axonal mitochondrial transport in a region-specific manner

  2024cites this paper
• The genetic landscape of pediatric postural orthostatic tachycardia syndrome

  2024cites this paper
• Microtubules and Cardiovascular Diseases: Insights into Pathology and Therapeutic Strategies.

  2024cites this paper
• Absence of oncomodulin increases susceptibility to noise-induced outer hair cell death and alters mitochondrial morphology

  2024cites this paper
• Temporal dynamics of membrane contact sites

  2024cites this paper
• F-ATP synthase inhibitory factor 1 and mitochondria-organelle interactions: new insight and implications.

  2024cites this paper
• Rhodiola crenulata alleviates hypobaric hypoxia-induced brain injury by maintaining BBB integrity and balancing energy metabolism dysfunction.

  2024cites this paper
• Changes in mitochondrial distribution occur at the axon initial segment in association with neurodegeneration in Drosophila

  2024cites this paper
• Not So Rare: Diseases Based on Mutant Proteins Controlling Endoplasmic Reticulum-Mitochondria Contact (MERC) Tethering

  2024cites this paper
• Supralinear Dependence of the IP3 Receptor-to-Mitochondria Local Ca2+ Transfer on the Endoplasmic Reticulum Ca2+ Loading

  2024cites this paper
• Mitochondria during T cell aging.

  2023cites this paper
• Dynamic optical coherence tomography for cell analysis [Invited].

  2023cites this paper
• Zn2+ decoration of microtubules arrests axonal transport and displaces tau, doublecortin, and MAP2C

  2023cites this paper
• The mitochondrial permeability transition pore in Ca2+ homeostasis.

  2023cites this paper
• The Novel Role of Mitochondrial Citrate Synthase and Citrate in the Pathophysiology of Alzheimer’s Disease

  2023cites this paper
• Spatial mapping of mitochondrial networks and bioenergetics in lung cancer

  2023cites this paper
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  2023cites this paper
• Calcium-Dependent Interaction of Nitric Oxide Synthase with Cytochrome c Oxidase: Implications for Brain Bioenergetics

  2023cites this paper
• Interaction between the mitochondrial adaptor MIRO and the motor adaptor TRAK

  2023cites this paper
• Mitochondria: It is all about energy

  2023cites this paper
• Peripheral neuropathy in mitochondrial disease.

  2023cites this paper
• Unveiling OSCP as the potential therapeutic target for mitochondrial dysfunction-related diseases.

  2023cites this paper
• Unveiling microtubule dynamics in lung cancer: Recent findings and prospects for drug delivery and treatment

  2023cites this paper
• Development of primary osteoarthritis during aging in genetically diverse UM-HET3 mice

  2023influential citation
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  2022cites this paper
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  2022cites this paper
• Mitochondrial trafficking and redox/phosphorylation signaling supporting cell migration phenotypes

  2022cites this paper
• Structural and functional diversity of mitochondria in vestibular/cochlear hair cells and vestibular calyx afferents.

  2022cites this paper
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  2022cites this paper
• Capture at the ER-mitochondrial contacts licenses IP3 receptors to stimulate local Ca2+ transfer and oxidative metabolism

  2022cites this paper
• Mitochondrial dynamics involves molecular and mechanical events in motility, fusion and fission

  2022cites this paper
• Segregated cation flux by TPC2 biases Ca2+ signaling through lysosomes

  2022cites this paper
• Determinants, Maintenance and Function of Organellar pH.

  2022cites this paper
• Mitochondrial behavior when things go wrong in the axon

  2022cites this paper
• Non-conventional mitochondrial permeability transition: Its regulation by mitochondrial dynamics.

  2022cites this paper
• Nrf2 as a regulator of mitochondrial function: Energy metabolism and beyond.

  2022cites this paper
• Miro proteins and their role in mitochondrial transfer in cancer and beyond

  2022cites this paper
• The interconnections between the microtubules and mitochondrial networks in cardiocerebrovascular diseases: implications for therapy.

  2022cites this paper
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  2021cites this paper
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  2021cites this paper
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  2021cites this paper
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  2021cites this paper
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  2021cites this paper
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  2021cites this paper
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  2021cites this paper
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  2021cites this paper
• Isolation of Mitochondria-Associated ER Membranes (MAMs), Synaptic MAMs, and Glycosphingolipid Enriched Microdomains (GEMs) from Brain Tissues and Neuronal Cells.

  2021cites this paper
• Mitochondrial calcium exchange in physiology and disease.

  2021cites this paper
• PINK1: A Bridge between Mitochondria and Parkinson’s Disease

  2021cites this paper
• Motor proteins at the mitochondria–cytoskeleton interface

  2021cites this paper
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  2021cites this paper
• Multi-curvature micropatterns unveil distinct calcium and mitochondrial dynamics in neuronal networks.

  2021cites this paper
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  2021cites this paper
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  2021cites this paper
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  2021cites this paper
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  2021cites this paper
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  2021cites this paper
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  2021cites this paper
• Axonal transport dysfunction of mitochondria in traumatic brain injury: A novel therapeutic target.

  2020cites this paper
• The emerging potential of SIRT-3 in oxidative stress-inflammatory axis associated increased neuroinflammatory component for metabolically impaired neural cell.

  2020cites this paper
• Molecular Nature and Physiological Role of the Mitochondrial Calcium Uniporter Channel.

  2020cites this paper
• Introductory Chapter: Mitochondrial Alterations and Neurological Disorders

  2020cites this paper
• Keratins as regulators of colonocyte mitochondria and intestinal barrier function

  2020cites this paper
• Functional Implications of Cardiac Mitochondria Clustering

  2020cites this paper
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  2020cites this paper
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  2020cites this paper
• SAM50, a side door to the mitochondria: The case of cytotoxic proteases.

  2020cites this paper
• Review: Microtubules monitor calcium and reactive oxygen species signatures in signal transduction.

  2020cites this paper
• Identification of select G-protein coupled receptors as regulators of the ER-mitochondria contacts by drug screening

  2020influential citation
• Mitochondria-lysosome contacts regulate mitochondrial Ca2+ dynamics via lysosomal TRPML1

  2020cites this paper
• Inter and Intracellular mitochondrial trafficking in health and disease.

  2020cites this paper
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  2020cites this paper
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  2020cites this paper
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  2020cites this paper