Miro1-mediated mitochondrial positioning shapes intracellular energy gradients required for cell migration Article Swipe
Max-Hinderk Schuler
,
Agnieszka Lewandowska
,
Giuseppe Di Caprio
,
Wesley Skillern
,
Srigokul Upadhyayula
,
Tomas Kirchhausen
,
Janet M. Shaw
,
Brian Cunniff
·
YOU?
·
· 2017
· Open Access
·
· DOI: https://doi.org/10.1091/mbc.e16-10-0741
YOU?
·
· 2017
· Open Access
·
· DOI: https://doi.org/10.1091/mbc.e16-10-0741
It has long been postulated, although never directly demonstrated, that mitochondria are strategically positioned in the cytoplasm to meet local requirements for energy production. Here we show that positioning of mitochondria in mouse embryonic fibroblasts (MEFs) determines the shape of intracellular energy gradients in living cells. Specifically, the ratio of ATP to ADP was highest at perinuclear areas of dense mitochondria and gradually decreased as more-peripheral sites were approached. Furthermore, the majority of mitochondria were positioned at the ventral surface of the cell, correlating with high ATP:ADP ratios close to the ventral membrane, which rapidly decreased toward the dorsal surface. We used cells deficient for the mitochondrial Rho-GTPase 1 (Miro1), an essential mediator of microtubule-based mitochondrial motility, to study how changes in mitochondrial positioning affect cytoplasmic energy distribution and cell migration, an energy-expensive process. The mitochondrial network in Miro1 −/− MEFs was restricted to the perinuclear area, with few mitochondria present at the cell periphery. This change in mitochondrial distribution dramatically reduced the ratio of ATP to ADP at the cell cortex and disrupted events essential for cell movement, including actin dynamics, lamellipodia protrusion, and membrane ruffling. Cell adhesion status was also affected by changes in mitochondrial positioning; focal adhesion assembly and stability was decreased in Miro1 −/− MEFs compared with Miro1 +/+ MEFs. Consequently Miro1 −/− MEFs migrated slower than control cells during both collective and single-cell migration. These data establish that Miro1-mediated mitochondrial positioning at the leading edge provides localized energy production that promotes cell migration by supporting membrane protrusion and focal adhesion stability.
Related Topics
Concepts
Cell biology
Biology
Cytoplasm
Mitochondrion
Intracellular
Membrane ruffling
Lamellipodium
Focal adhesion
Cell cortex
Cell
Cell migration
Cytoskeleton
Biochemistry
Signal transduction
Metadata
- Type
- article
- Language
- en
- Landing Page
- https://doi.org/10.1091/mbc.e16-10-0741
- OA Status
- green
- Cited By
- 163
- References
- 67
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W2734745767
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
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https://openalex.org/W2734745767Canonical identifier for this work in OpenAlex
- DOI
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https://doi.org/10.1091/mbc.e16-10-0741Digital Object Identifier
- Title
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Miro1-mediated mitochondrial positioning shapes intracellular energy gradients required for cell migrationWork title
- Type
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articleOpenAlex work type
- Language
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enPrimary language
- Publication year
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2017Year of publication
- Publication date
-
2017-06-14Full publication date if available
- Authors
-
Max-Hinderk Schuler, Agnieszka Lewandowska, Giuseppe Di Caprio, Wesley Skillern, Srigokul Upadhyayula, Tomas Kirchhausen, Janet M. Shaw, Brian CunniffList of authors in order
- Landing page
-
https://doi.org/10.1091/mbc.e16-10-0741Publisher landing page
- Open access
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YesWhether a free full text is available
- OA status
-
greenOpen access status per OpenAlex
- OA URL
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https://nrs.harvard.edu/urn-3:HUL.InstRepos:34492219Direct OA link when available
- Concepts
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Cell biology, Biology, Cytoplasm, Mitochondrion, Intracellular, Membrane ruffling, Lamellipodium, Focal adhesion, Cell cortex, Cell, Cell migration, Cytoskeleton, Biochemistry, Signal transductionTop concepts (fields/topics) attached by OpenAlex
- Cited by
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163Total citation count in OpenAlex
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2025: 26, 2024: 22, 2023: 13, 2022: 21, 2021: 24Per-year citation counts (last 5 years)
- References (count)
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67Number of works referenced by this work
- Related works (count)
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10Other works algorithmically related by OpenAlex
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| abstract_inverted_index.were | 67, 74 |
| abstract_inverted_index.with | 84, 147, 210 |
| abstract_inverted_index.MEFs. | 213 |
| abstract_inverted_index.Miro1 | 138, 206, 211, 215 |
| abstract_inverted_index.These | 229 |
| abstract_inverted_index.actin | 180 |
| abstract_inverted_index.area, | 146 |
| abstract_inverted_index.areas | 57 |
| abstract_inverted_index.cell, | 82 |
| abstract_inverted_index.cells | 102, 222 |
| abstract_inverted_index.close | 88 |
| abstract_inverted_index.dense | 59 |
| abstract_inverted_index.focal | 198, 253 |
| abstract_inverted_index.local | 19 |
| abstract_inverted_index.mouse | 32 |
| abstract_inverted_index.never | 6 |
| abstract_inverted_index.ratio | 48, 163 |
| abstract_inverted_index.shape | 38 |
| abstract_inverted_index.sites | 66 |
| abstract_inverted_index.study | 118 |
| abstract_inverted_index.which | 93 |
| abstract_inverted_index.(MEFs) | 35 |
| abstract_inverted_index.affect | 124 |
| abstract_inverted_index.cells. | 45 |
| abstract_inverted_index.change | 156 |
| abstract_inverted_index.cortex | 171 |
| abstract_inverted_index.dorsal | 98 |
| abstract_inverted_index.during | 223 |
| abstract_inverted_index.energy | 22, 41, 126, 242 |
| abstract_inverted_index.events | 174 |
| abstract_inverted_index.living | 44 |
| abstract_inverted_index.ratios | 87 |
| abstract_inverted_index.slower | 219 |
| abstract_inverted_index.status | 189 |
| abstract_inverted_index.toward | 96 |
| abstract_inverted_index.ATP:ADP | 86 |
| abstract_inverted_index.changes | 120, 194 |
| abstract_inverted_index.control | 221 |
| abstract_inverted_index.highest | 54 |
| abstract_inverted_index.leading | 238 |
| abstract_inverted_index.network | 136 |
| abstract_inverted_index.present | 150 |
| abstract_inverted_index.rapidly | 94 |
| abstract_inverted_index.reduced | 161 |
| abstract_inverted_index.surface | 79 |
| abstract_inverted_index.ventral | 78, 91 |
| abstract_inverted_index.−/− | 139, 207, 216 |
| abstract_inverted_index.(Miro1), | 109 |
| abstract_inverted_index.adhesion | 188, 199, 254 |
| abstract_inverted_index.affected | 192 |
| abstract_inverted_index.although | 5 |
| abstract_inverted_index.assembly | 200 |
| abstract_inverted_index.compared | 209 |
| abstract_inverted_index.directly | 7 |
| abstract_inverted_index.majority | 71 |
| abstract_inverted_index.mediator | 112 |
| abstract_inverted_index.membrane | 185, 250 |
| abstract_inverted_index.migrated | 218 |
| abstract_inverted_index.process. | 133 |
| abstract_inverted_index.promotes | 245 |
| abstract_inverted_index.provides | 240 |
| abstract_inverted_index.surface. | 99 |
| abstract_inverted_index.cytoplasm | 16 |
| abstract_inverted_index.decreased | 63, 95, 204 |
| abstract_inverted_index.deficient | 103 |
| abstract_inverted_index.disrupted | 173 |
| abstract_inverted_index.dynamics, | 181 |
| abstract_inverted_index.embryonic | 33 |
| abstract_inverted_index.essential | 111, 175 |
| abstract_inverted_index.establish | 231 |
| abstract_inverted_index.gradients | 42 |
| abstract_inverted_index.gradually | 62 |
| abstract_inverted_index.including | 179 |
| abstract_inverted_index.localized | 241 |
| abstract_inverted_index.membrane, | 92 |
| abstract_inverted_index.migration | 247 |
| abstract_inverted_index.motility, | 116 |
| abstract_inverted_index.movement, | 178 |
| abstract_inverted_index.ruffling. | 186 |
| abstract_inverted_index.stability | 202 |
| abstract_inverted_index.Rho-GTPase | 107 |
| abstract_inverted_index.collective | 225 |
| abstract_inverted_index.determines | 36 |
| abstract_inverted_index.migration, | 130 |
| abstract_inverted_index.migration. | 228 |
| abstract_inverted_index.periphery. | 154 |
| abstract_inverted_index.positioned | 13, 75 |
| abstract_inverted_index.production | 243 |
| abstract_inverted_index.protrusion | 251 |
| abstract_inverted_index.restricted | 142 |
| abstract_inverted_index.stability. | 255 |
| abstract_inverted_index.supporting | 249 |
| abstract_inverted_index.approached. | 68 |
| abstract_inverted_index.correlating | 83 |
| abstract_inverted_index.cytoplasmic | 125 |
| abstract_inverted_index.fibroblasts | 34 |
| abstract_inverted_index.perinuclear | 56, 145 |
| abstract_inverted_index.positioning | 28, 123, 235 |
| abstract_inverted_index.postulated, | 4 |
| abstract_inverted_index.production. | 23 |
| abstract_inverted_index.protrusion, | 183 |
| abstract_inverted_index.single-cell | 227 |
| abstract_inverted_index.Consequently | 214 |
| abstract_inverted_index.Furthermore, | 69 |
| abstract_inverted_index.distribution | 127, 159 |
| abstract_inverted_index.dramatically | 160 |
| abstract_inverted_index.lamellipodia | 182 |
| abstract_inverted_index.mitochondria | 10, 30, 60, 73, 149 |
| abstract_inverted_index.positioning; | 197 |
| abstract_inverted_index.requirements | 20 |
| abstract_inverted_index.Specifically, | 46 |
| abstract_inverted_index.demonstrated, | 8 |
| abstract_inverted_index.intracellular | 40 |
| abstract_inverted_index.mitochondrial | 106, 115, 122, 135, 158, 196, 234 |
| abstract_inverted_index.strategically | 12 |
| abstract_inverted_index.Miro1-mediated | 233 |
| abstract_inverted_index.more-peripheral | 65 |
| abstract_inverted_index.energy-expensive | 132 |
| abstract_inverted_index.microtubule-based | 114 |
| cited_by_percentile_year.max | 100 |
| cited_by_percentile_year.min | 94 |
| countries_distinct_count | 1 |
| institutions_distinct_count | 8 |
| sustainable_development_goals[0].id | https://metadata.un.org/sdg/7 |
| sustainable_development_goals[0].score | 0.8700000047683716 |
| sustainable_development_goals[0].display_name | Affordable and clean energy |
| citation_normalized_percentile.value | 0.9746123 |
| citation_normalized_percentile.is_in_top_1_percent | False |
| citation_normalized_percentile.is_in_top_10_percent | True |