ACS Publications. Most Trusted. Most Cited. Most Read
My Activity
CONTENT TYPES

Ca2+ Regulation of Mitochondrial ATP Synthesis Visualized at the Single Cell Level

View Author Information
Institute of Scientific and Industrial Research, Osaka University, Japan
Research Institute for Electronic Science, Hokkaido University, Japan
§ PRESTO, Japan Science and Technology Agency, Japan
The Hakubi Project, Kyoto University, Japan
Department of Applied Chemistry, University of Tokyo, Japan
Cite this: ACS Chem. Biol. 2011, 6, 7, 709–715
Publication Date (Web):April 13, 2011
https://doi.org/10.1021/cb100313n
Copyright © 2011 American Chemical Society

    Article Views

    5858

    Altmetric

    -

    Citations

    LEARN ABOUT THESE METRICS
    Read OnlinePDF (4 MB)
    Supporting Info (2)»

    Abstract

    Abstract Image

    Intracellular Ca2+ levels play a crucial role in the control of ATP synthesis. However, the spatiotemporal correlation between ATP and Ca2+ remains unclear due to the inability to visualize these factors within same individual cells. A Förster resonance energy transfer (FRET)-based fluorescent ATP probe, named ATeam, was recently developed for ATP imaging in single living cells. However, the spectra of cyan fluorescent protein (CFP) and yellow fluorescent protein (YFP) used as the FRET donor and the acceptor, respectively, significantly overlap with the ultraviolet-excitable Ca2+ probe, fura-2. In the present work, we developed new red-shifted ATP probes, GO-ATeams, in which green fluorescent protein (GFP) and orange fluorescent protein (OFP) was used as the FRET pair to minimize spectral overlap with the fura-2 emission. The dynamics of intracellular Ca2+ and mitochondrial ATP levels in single histamine-stimulated HeLa cells were successfully visualized by using fura-2 and GO-ATeam. The experiments showed that histamine induced increases of both intracellular Ca2+ and mitochondrial ATP levels. The increment of mitochondrial ATP levels was proportional to that of Ca2+. This finding suggests that cellular Ca2+ levels might precisely control mitochondrial ATP synthesis in response to the increased ATP consumption triggered by Ca2+. In addition, GO-ATeam has several advantages over the original ATeam. The GO-ATeam signal was more stable against acidification, which would allow ATP imaging inside acidic intracellular compartments. Also, the GO-ATeam excitation wavelength is much less phototoxic to cells, making the probe suitable for long-time observation.

    Supporting Information

    ARTICLE SECTIONS
    Jump To

    This material is available free of charge via the Internet at http://pubs.acs.org.

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    This article is cited by 109 publications.

    1. Eric C. Greenwald, Sohum Mehta, Jin Zhang. Genetically Encoded Fluorescent Biosensors Illuminate the Spatiotemporal Regulation of Signaling Networks. Chemical Reviews 2018, 118 (24) , 11707-11794. https://doi.org/10.1021/acs.chemrev.8b00333
    2. Taiichi Tsuyama, Jun-ichi Kishikawa, Yong-Woon Han, Yoshie Harada, Asako Tsubouchi, Hiroyuki Noji, Akira Kakizuka, Ken Yokoyama, Tadashi Uemura, and Hiromi Imamura . In Vivo Fluorescent Adenosine 5′-Triphosphate (ATP) Imaging of Drosophila melanogaster and Caenorhabditis elegans by Using a Genetically Encoded Fluorescent ATP Biosensor Optimized for Low Temperatures. Analytical Chemistry 2013, 85 (16) , 7889-7896. https://doi.org/10.1021/ac4015325
    3. Takeaki Ozawa, Hideaki Yoshimura, and Sung Bae Kim . Advances in Fluorescence and Bioluminescence Imaging. Analytical Chemistry 2013, 85 (2) , 590-609. https://doi.org/10.1021/ac3031724
    4. Yasutaka Kurishita, Takahiro Kohira, Akio Ojida, and Itaru Hamachi . Organelle-Localizable Fluorescent Chemosensors for Site-Specific Multicolor Imaging of Nucleoside Polyphosphate Dynamics in Living Cells. Journal of the American Chemical Society 2012, 134 (45) , 18779-18789. https://doi.org/10.1021/ja308754g
    5. Jungmi Choi, Naoki Matoba, Daiki Setoyama, Daiki Watanabe, Yuichiro Ohnishi, Ryuto Yasui, Yuichirou Kitai, Aki Oomachi, Yutaro Kotobuki, Yoichi Nishiya, Michael Paul Pieper, Hiromi Imamura, Motoko Yanagita, Masamichi Yamamoto. The SGLT2 inhibitor empagliflozin improves cardiac energy status via mitochondrial ATP production in diabetic mice. Communications Biology 2023, 6 (1) https://doi.org/10.1038/s42003-023-04663-y
    6. Lars Hellweg, Anna Edenhofer, Lucas Barck, Magnus-Carsten Huppertz, Michelle. S. Frei, Miroslaw Tarnawski, Andrea Bergner, Birgit Koch, Kai Johnsson, Julien Hiblot. A general method for the development of multicolor biosensors with large dynamic ranges. Nature Chemical Biology 2023, 19 (9) , 1147-1157. https://doi.org/10.1038/s41589-023-01350-1
    7. L.F. Barros, I. Ruminot, P.Y. Sandoval, A. San Martín. Enlightening brain energy metabolism. Neurobiology of Disease 2023, 184 , 106211. https://doi.org/10.1016/j.nbd.2023.106211
    8. Sonia Domínguez-Zorita, Inés Romero-Carramiñana, Fulvio Santacatterina, Pau B. Esparza-Moltó, Carolina Simó, Araceli del-Arco, Cristina Núñez de Arenas, Jorge Saiz, Coral Barbas, José M. Cuezva. IF1 ablation prevents ATP synthase oligomerization, enhances mitochondrial ATP turnover and promotes an adenosine-mediated pro-inflammatory phenotype. Cell Death & Disease 2023, 14 (7) https://doi.org/10.1038/s41419-023-05957-z
    9. Tomofumi Takenaka, Yuichiro Ohnishi, Masamichi Yamamoto, Daiki Setoyama, Haruhiko Kishima. Glycolytic System in Axons Supplement Decreased ATP Levels after Axotomy of the Peripheral Nerve. eneuro 2023, 10 (3) , ENEURO.0353-22.2023. https://doi.org/10.1523/ENEURO.0353-22.2023
    10. Yefei Wang, Ying Wang, Shixin Li, Huihui Jin, Jiayu Duan, Xiyue Lu, Yinglin Qin, Jiale Song, Xiaoshan Li, Xianglan Jin. Insights of Chinese herbal medicine for mitochondrial dysfunction in chronic cerebral hypoperfusion induced cognitive impairment: Existed evidences and potential directions. Frontiers in Pharmacology 2023, 14 https://doi.org/10.3389/fphar.2023.1138566
    11. Ruzhou Zhao, Yixin Xu, Xiaobo Wang, Xiang Zhou, Yanqi Liu, Shuai Jiang, Lin Zhang, Zhibin Yu. Withaferin A Enhances Mitochondrial Biogenesis and BNIP3-Mediated Mitophagy to Promote Rapid Adaptation to Extreme Hypoxia. Cells 2023, 12 (1) , 85. https://doi.org/10.3390/cells12010085
    12. Ning Huang, Zu-Hang Sheng. Microfluidic devices as model platforms of CNS injury-ischemia to study axonal regeneration by regulating mitochondrial transport and bioenergetic metabolism. Cell Regeneration 2022, 11 (1) https://doi.org/10.1186/s13619-022-00138-3
    13. Seyta Ley‐Ngardigal, Giulia Bertolin. Approaches to monitor ATP levels in living cells: where do we stand?. The FEBS Journal 2022, 289 (24) , 7940-7969. https://doi.org/10.1111/febs.16169
    14. Rajarshi Chakrabarti, Tak Shun Fung, Taewook Kang, Pieti W. Elonkirjo, Anu Suomalainen, Edward J. Usherwood, Henry N. Higgs. Mitochondrial dysfunction triggers actin polymerization necessary for rapid glycolytic activation. Journal of Cell Biology 2022, 221 (11) https://doi.org/10.1083/jcb.202201160
    15. Nobuhiko Nakajima, Yuichiro Ohnishi, Masamichi Yamamoto, Daiki Setoyama, Hirohiko Imai, Tomofumi Takenaka, Mari Matsumoto, Koichi Hosomi, Yoichi Saitoh, Hidemasa Furue, Haruhiko Kishima. Excess intracellular ATP causes neuropathic pain following spinal cord injury. Cellular and Molecular Life Sciences 2022, 79 (9) https://doi.org/10.1007/s00018-022-04510-z
    16. Maimouna D. N’Gadjaga, Stéphanie Perrinet, Michael G. Connor, Giulia Bertolin, Gaël A. Millot, Agathe Subtil. Chlamydia trachomatis development requires both host glycolysis and oxidative phosphorylation but has only minor effects on these pathways. Journal of Biological Chemistry 2022, 298 (9) , 102338. https://doi.org/10.1016/j.jbc.2022.102338
    17. Olivier Lurette, Hala Guedouari, Jordan L. Morris, Rebeca Martín-Jiménez, Julie-Pier Robichaud, Geneviève Hamel-Côté, Mehtab Khan, Nicholas Dauphinee, Nicolas Pichaud, Julien Prudent, Etienne Hebert-Chatelain. Mitochondrial matrix-localized Src kinase regulates mitochondrial morphology. Cellular and Molecular Life Sciences 2022, 79 (6) https://doi.org/10.1007/s00018-022-04325-y
    18. Tomoko Nomiyama, Daiki Setoyama, Takehiro Yasukawa, Dongchon Kang. Mitochondria metabolomics reveals a role of β-nicotinamide mononucleotide metabolism in mitochondrial DNA replication. The Journal of Biochemistry 2022, 171 (3) , 325-338. https://doi.org/10.1093/jb/mvab136
    19. Milos Mihajlovic, Mathieu Vinken. Mitochondria as the Target of Hepatotoxicity and Drug-Induced Liver Injury: Molecular Mechanisms and Detection Methods. International Journal of Molecular Sciences 2022, 23 (6) , 3315. https://doi.org/10.3390/ijms23063315
    20. A. San Martín, R. Arce-Molina, C. Aburto, F. Baeza-Lehnert, L.F. Barros, Y. Contreras-Baeza, A. Pinilla, I. Ruminot, D. Rauseo, P.Y. Sandoval. Visualizing physiological parameters in cells and tissues using genetically encoded indicators for metabolites. Free Radical Biology and Medicine 2022, 182 , 34-58. https://doi.org/10.1016/j.freeradbiomed.2022.02.012
    21. Sunan Li, Zu-Hang Sheng. Energy matters: presynaptic metabolism and the maintenance of synaptic transmission. Nature Reviews Neuroscience 2022, 23 (1) , 4-22. https://doi.org/10.1038/s41583-021-00535-8
    22. Keizo Nishikawa, Shigeto Seno, Toshitada Yoshihara, Ayako Narazaki, Yuki Sugiura, Reito Shimizu, Junichi Kikuta, Reiko Sakaguchi, Norio Suzuki, Norihiko Takeda, Hiroaki Semba, Masamichi Yamamoto, Daisuke Okuzaki, Daisuke Motooka, Yasuhiro Kobayashi, Makoto Suematsu, Haruhiko Koseki, Hideo Matsuda, Masayuki Yamamoto, Seiji Tobita, Yasuo Mori, Masaru Ishii. Osteoclasts adapt to physioxia perturbation through DNA demethylation. EMBO reports 2021, 22 (12) https://doi.org/10.15252/embr.202153035
    23. Kelly A. Chamberlain, Ning Huang, Yuxiang Xie, Francesca LiCausi, Sunan Li, Yan Li, Zu-Hang Sheng. Oligodendrocytes enhance axonal energy metabolism by deacetylation of mitochondrial proteins through transcellular delivery of SIRT2. Neuron 2021, 109 (21) , 3456-3472.e8. https://doi.org/10.1016/j.neuron.2021.08.011
    24. Jiazhou He, Masamichi Yamamoto, Kenta Sumiyama, Yumi Konagaya, Kenta Terai, Michiyuki Matsuda, Shinya Sato. Two‐photon AMPK and ATP imaging reveals the bias between rods and cones in glycolysis utility. The FASEB Journal 2021, 35 (9) https://doi.org/10.1096/fj.202101121R
    25. Martin Müller, Susanne Gerndt, Yu-Kai Chao, Themistoklis Zisis, Ong Nam Phuong Nguyen, Aaron Gerwien, Nicole Urban, Christoph Müller, Florian A. Gegenfurtner, Franz Geisslinger, Carina Ortler, Cheng-Chang Chen, Stefan Zahler, Martin Biel, Michael Schaefer, Christian Grimm, Franz Bracher, Angelika M. Vollmar, Karin Bartel. Gene editing and synthetically accessible inhibitors reveal role for TPC2 in HCC cell proliferation and tumor growth. Cell Chemical Biology 2021, 28 (8) , 1119-1131.e27. https://doi.org/10.1016/j.chembiol.2021.01.023
    26. Ning Huang, Sunan Li, Yuxiang Xie, Qi Han, Xiao-Ming Xu, Zu-Hang Sheng. Reprogramming an energetic AKT-PAK5 axis boosts axon energy supply and facilitates neuron survival and regeneration after injury and ischemia. Current Biology 2021, 31 (14) , 3098-3114.e7. https://doi.org/10.1016/j.cub.2021.04.079
    27. Aiqing Zhang, Kaya Mernitz, Chao Wu, Wei Xiong, Yaodong He, Guangyi Wang, Xin Wang, , . ATP Drives Efficient Terpene Biosynthesis in Marine Thraustochytrids. mBio 2021, 12 (3) https://doi.org/10.1128/mBio.00881-21
    28. Yuichiro Ohnishi, Masamichi Yamamoto, Yuki Sugiura, Daiki Setoyama, Haruhiko Kishima. Rostro-caudal different energy metabolism leading to differences in degeneration in spinal cord injury. Brain Communications 2021, 3 (2) https://doi.org/10.1093/braincomms/fcab058
    29. Vikas Pandey, Lai-Hua Xie, Zhilin Qu, Zhen Song, . Mitochondrial depolarization promotes calcium alternans: Mechanistic insights from a ventricular myocyte model. PLOS Computational Biology 2021, 17 (1) , e1008624. https://doi.org/10.1371/journal.pcbi.1008624
    30. Zhong-Lin Yang, Jian-Ning Chen, Yu-Yang Lu, Min Lu, Qin-Li Wan, Gui-Sheng Wu, Huai-Rong Luo. Inositol polyphosphate multikinase IPMK-1 regulates development through IP3/calcium signaling in Caenorhabditis elegans. Cell Calcium 2021, 93 , 102327. https://doi.org/10.1016/j.ceca.2020.102327
    31. B. Spurlock, K. Mitra. Mito-SinCe2 Approach to Analyze Mitochondrial Structure–Function Relationship in Single Cells. 2021, 415-432. https://doi.org/10.1007/978-1-0716-1262-0_27
    32. András T. Deak, Claire Jean-Quartier, Alexander I. Bondarenko, Lukas N. Groschner, Roland Malli, Wolfgang F. Graier, Markus Waldeck-Weiermair. Assessment of Mitochondrial Ca2+ Uptake. 2021, 173-191. https://doi.org/10.1007/978-1-0716-1266-8_13
    33. Zefeng Wei, Yutaka Shindo, Kohji Hotta, Kotaro Oka. RedATeam: A Genetically Encoded Red ATP Sensor and Its Application in Dual FRET Imaging With a Single Excitation Light. SSRN Electronic Journal 2021, 57 https://doi.org/10.2139/ssrn.3952828
    34. Haixin Zhao, Xin Pan. Mitochondrial Ca2+ and cell cycle regulation. 2021, 171-207. https://doi.org/10.1016/bs.ircmb.2021.02.015
    35. Kevin Richetin, Pascal Steullet, Mathieu Pachoud, Romain Perbet, Enea Parietti, Mathischan Maheswaran, Sabiha Eddarkaoui, Séverine Bégard, Catherine Pythoud, Maria Rey, Raphaëlle Caillierez, Kim Q Do, Sophie Halliez, Paola Bezzi, Luc Buée, Geneviève Leuba, Morvane Colin, Nicolas Toni, Nicole Déglon. Tau accumulation in astrocytes of the dentate gyrus induces neuronal dysfunction and memory deficits in Alzheimer’s disease. Nature Neuroscience 2020, 23 (12) , 1567-1579. https://doi.org/10.1038/s41593-020-00728-x
    36. Yves Gouriou, Muhammad Alam, Zeina Harhous, Claire Da Silva, Delphine Baetz, Sally Badawi, Etienne Lefai, Jennifer Rieusset, Annie Durand, Rania Harisseh, Abdallah Gharib, Michel Ovize, Gabriel Bidaux. ANT2-Mediated ATP Import into Mitochondria Protects against Hypoxia Lethal Injury. Cells 2020, 9 (12) , 2542. https://doi.org/10.3390/cells9122542
    37. Shinya Yamamoto, Masamichi Yamamoto, Jin Nakamura, Akiko Mii, Shigenori Yamamoto, Masahiro Takahashi, Keiichi Kaneko, Eiichiro Uchino, Yuki Sato, Shingo Fukuma, Hiromi Imamura, Michiyuki Matsuda, Motoko Yanagita. Spatiotemporal ATP Dynamics during AKI Predict Renal Prognosis. Journal of the American Society of Nephrology 2020, 31 (12) , 2855-2869. https://doi.org/10.1681/ASN.2020050580
    38. Ru-Zhou Zhao, Xiao-Bo Wang, Shuai Jiang, Ning-Yu Ru, Bo Jiao, Yun-Ying Wang, Zhi-Bin Yu. Elevated ROS depress mitochondrial oxygen utilization efficiency in cardiomyocytes during acute hypoxia. Pflügers Archiv - European Journal of Physiology 2020, 472 (11) , 1619-1630. https://doi.org/10.1007/s00424-020-02463-5
    39. Sunan Li, Gui-Jing Xiong, Ning Huang, Zu-Hang Sheng. The cross-talk of energy sensing and mitochondrial anchoring sustains synaptic efficacy by maintaining presynaptic metabolism. Nature Metabolism 2020, 2 (10) , 1077-1095. https://doi.org/10.1038/s42255-020-00289-0
    40. Naoki Matsuda, Ken-ichi Hironaka, Masashi Fujii, Takumi Wada, Katsuyuki Kunida, Haruki Inoue, Miki Eto, Daisuke Hoshino, Yasuro Furuichi, Yasuko Manabe, Nobuharu L. Fujii, Hiroyuki Noji, Hiromi Imamura, Shinya Kuroda. Monitoring and mathematical modeling of mitochondrial ATP in myotubes at single-cell level reveals two distinct population with different kinetics. Quantitative Biology 2020, 8 (3) , 228-237. https://doi.org/10.1007/s40484-020-0211-8
    41. Naemeh Pourshafie, Ester Masati, Eric Bunker, Alec R. Nickolls, Parisorn Thepmankorn, Kory Johnson, Xia Feng, Tyler Ekins, Christopher Grunseich, Kenneth H. Fischbeck. Linking epigenetic dysregulation, mitochondrial impairment, and metabolic dysfunction in SBMA motor neurons. JCI Insight 2020, 5 (13) https://doi.org/10.1172/jci.insight.136539
    42. Osamu Hashizume, Yosuke Funato, Daisuke Yamazaki, Hiroaki Miki. Excessive Mg 2+ Impairs Intestinal Homeostasis by Enhanced Production of Adenosine Triphosphate and Reactive Oxygen Species. Antioxidants & Redox Signaling 2020, 33 (1) , 20-34. https://doi.org/10.1089/ars.2019.7951
    43. Saloni Agarwal, Subramaniam Ganesh. Perinuclear mitochondrial clustering, increased ROS levels, and HIF1 are required for the activation of HSF1 by heat stress. Journal of Cell Science 2020, 133 (13) https://doi.org/10.1242/jcs.245589
    44. Alexander I. Kostyuk, Aleksandra D. Kokova, Oleg V. Podgorny, Ilya V. Kelmanson, Elena S. Fetisova, Vsevolod V. Belousov, Dmitry S. Bilan. Genetically Encoded Tools for Research of Cell Signaling and Metabolism under Brain Hypoxia. Antioxidants 2020, 9 (6) , 516. https://doi.org/10.3390/antiox9060516
    45. Rodrigo Lerchundi, Na Huang, Christine R. Rose. Quantitative Imaging of Changes in Astrocytic and Neuronal Adenosine Triphosphate Using Two Different Variants of ATeam. Frontiers in Cellular Neuroscience 2020, 14 https://doi.org/10.3389/fncel.2020.00080
    46. Andrew D. James, Daniel A. Richardson, In-Whan Oh, Pishyaporn Sritangos, Thomas Attard, Lisa Barrett, Jason I. E. Bruce. Cutting off the fuel supply to calcium pumps in pancreatic cancer cells: role of pyruvate kinase-M2 (PKM2). British Journal of Cancer 2020, 122 (2) , 266-278. https://doi.org/10.1038/s41416-019-0675-3
    47. Giampaolo Morciano, Hiromi Imamura, Simone Patergnani, Gaia Pedriali, Carlotta Giorgi, Paolo Pinton. Measurement of ATP concentrations in mitochondria of living cells using luminescence and fluorescence approaches. 2020, 199-219. https://doi.org/10.1016/bs.mcb.2019.10.007
    48. Karla Cristine C. DOYSABAS, Mami OBA, Tomoki ISHIBASHI, Hideki SHIBATA, Hitoshi TAKEMAE, Hiroshi SHIMODA, Ronald TARIGAN, Tetsuya MIZUTANI, Atsuo IIDA, Eiichi HONDO. ATeam technology for detecting early signs of viral cytopathic effect. Journal of Veterinary Medical Science 2020, 82 (3) , 387-393. https://doi.org/10.1292/jvms.20-0021
    49. Rajat Puri, Xiu-Tang Cheng, Mei-Yao Lin, Ning Huang, Zu-Hang Sheng. Mul1 restrains Parkin-mediated mitophagy in mature neurons by maintaining ER-mitochondrial contacts. Nature Communications 2019, 10 (1) https://doi.org/10.1038/s41467-019-11636-5
    50. Jesús Gómez-Escudero, Cristina Clemente, Diego García-Weber, Rebeca Acín-Pérez, Jaime Millán, José A. Enríquez, Katie Bentley, Peter Carmeliet, Alicia G. Arroyo. PKM2 regulates endothelial cell junction dynamics and angiogenesis via ATP production. Scientific Reports 2019, 9 (1) https://doi.org/10.1038/s41598-019-50866-x
    51. Niklas J. Gerkau, Rodrigo Lerchundi, Joel S. E. Nelson, Marina Lantermann, Jan Meyer, Johannes Hirrlinger, Christine R. Rose. Relation between activity‐induced intracellular sodium transients and ATP dynamics in mouse hippocampal neurons. The Journal of Physiology 2019, 597 (23) , 5687-5705. https://doi.org/10.1113/JP278658
    52. Vitor S. Alves, Hélio S. Alves-Silva, Diego J.B. Orts, Luísa Ribeiro-Silva, Manoel Arcisio-Miranda, Fernando A. Oliveira. Calcium Signaling in Neurons and Glial Cells: Role of Cav1 channels. Neuroscience 2019, 421 , 95-111. https://doi.org/10.1016/j.neuroscience.2019.09.041
    53. Yuya Ide, Takahiro Horie, Naritatsu Saito, Shin Watanabe, Chiharu Otani, Yui Miyasaka, Yasuhide Kuwabara, Tomohiro Nishino, Tetsushi Nakao, Masataka Nishiga, Hitoo Nishi, Yasuhiro Nakashima, Fumiko Nakazeki, Satoshi Koyama, Masahiro Kimura, Shuhei Tsuji, Randolph Ruiz Rodriguez, Sijia Xu, Tomohiro Yamasaki, Toshimitsu Watanabe, Masamichi Yamamoto, Motoko Yanagita, Takeshi Kimura, Akira Kakizuka, Koh Ono. Cardioprotective Effects of VCP Modulator KUS121 in Murine and Porcine Models of Myocardial Infarction. JACC: Basic to Translational Science 2019, 4 (6) , 701-714. https://doi.org/10.1016/j.jacbts.2019.06.001
    54. Benjamin Wacquier, Valérie Voorsluijs, Laurent Combettes, Geneviève Dupont. Coding and decoding of oscillatory Ca2+ signals. Seminars in Cell & Developmental Biology 2019, 94 , 11-19. https://doi.org/10.1016/j.semcdb.2019.01.008
    55. Alexander I. Kostyuk, Aleksandra D. Demidovich, Daria A. Kotova, Vsevolod V. Belousov, Dmitry S. Bilan. Circularly Permuted Fluorescent Protein-Based Indicators: History, Principles, and Classification. International Journal of Molecular Sciences 2019, 20 (17) , 4200. https://doi.org/10.3390/ijms20174200
    56. Masamichi Yamamoto, Minsoo Kim, Hirohiko Imai, Yamato Itakura, Gen Ohtsuki. Microglia-Triggered Plasticity of Intrinsic Excitability Modulates Psychomotor Behaviors in Acute Cerebellar Inflammation. Cell Reports 2019, 28 (11) , 2923-2938.e8. https://doi.org/10.1016/j.celrep.2019.07.078
    57. Masamichi Yamamoto. Visualization of ATP dynamics during mouse exercise. Japanese Journal of Physical Fitness and Sports Medicine 2019, 68 (4) , 245-249. https://doi.org/10.7600/jspfsm.68.245
    58. Rodrigo Lerchundi, Karl W. Kafitz, Ulrike Winkler, Marcel Färfers, Johannes Hirrlinger, Christine R. Rose. FRET‐based imaging of intracellular ATP in organotypic brain slices. Journal of Neuroscience Research 2019, 97 (8) , 933-945. https://doi.org/10.1002/jnr.24361
    59. Shintaro Watanuki, Hiroshi Kobayashi, Yuriko Sorimachi, Masamichi Yamamoto, Shinichiro Okamoto, Keiyo Takubo. ATP turnover and glucose dependency in hematopoietic stem/progenitor cells are increased by proliferation and differentiation. Biochemical and Biophysical Research Communications 2019, 514 (1) , 287-294. https://doi.org/10.1016/j.bbrc.2019.04.123
    60. Brian Spurlock, Priyanka Gupta, Malay Kumar Basu, Avik Mukherjee, Anita B. Hjelmeland, Victor Darley-Usmar, Danitra Parker, McKenzie E. Foxall, Kasturi Mitra. New quantitative approach reveals heterogeneity in mitochondrial structure–function relations in tumor-initiating cells. Journal of Cell Science 2019, 132 (9) https://doi.org/10.1242/jcs.230755
    61. Jessica L. Cao, Stephanie M. Adaniya, Michael W. Cypress, Yuta Suzuki, Yoichiro Kusakari, Bong Sook Jhun, Jin O-Uchi. Role of mitochondrial Ca2+ homeostasis in cardiac muscles. Archives of Biochemistry and Biophysics 2019, 663 , 276-287. https://doi.org/10.1016/j.abb.2019.01.027
    62. Shinji Urata, Tadatsune Iida, Masamichi Yamamoto, Yu Mizushima, Chisato Fujimoto, Yu Matsumoto, Tatsuya Yamasoba, Shigeo Okabe. Cellular cartography of the organ of Corti based on optical tissue clearing and machine learning. eLife 2019, 8 https://doi.org/10.7554/eLife.40946
    63. Aditya Arya, Anamika Gangwar, Amit Kumar. Biosensors in Animal Biotechnology. 2019, 75-95. https://doi.org/10.1016/B978-0-12-818823-1.00006-5
    64. Ang Li, Jung-Hwa Cho, Brian Reid, Chun-Chih Tseng, Lian He, Peng Tan, Chao-Yuan Yeh, Ping Wu, Yuwei Li, Randall B. Widelitz, Yubin Zhou, Min Zhao, Robert H. Chow, Cheng-Ming Chuong. Calcium oscillations coordinate feather mesenchymal cell movement by SHH dependent modulation of gap junction networks. Nature Communications 2018, 9 (1) https://doi.org/10.1038/s41467-018-07661-5
    65. R. Suzuki, K. Hotta, K. Oka. Transitional correlation between inner-membrane potential and ATP levels of neuronal mitochondria. Scientific Reports 2018, 8 (1) https://doi.org/10.1038/s41598-018-21109-2
    66. Hidenobu Miyazawa, Masamichi Yamamoto, Yoshifumi Yamaguchi, Masayuki Miura. Mammalian embryos show metabolic plasticity toward the surrounding environment during neural tube closure. Genes to Cells 2018, 23 (9) , 794-802. https://doi.org/10.1111/gtc.12626
    67. Bryce A. Mendelsohn, Neal K. Bennett, Maxwell A. Darch, Katharine Yu, Mai K. Nguyen, Daniela Pucciarelli, Maxine Nelson, Max A. Horlbeck, Luke A. Gilbert, William Hyun, Martin Kampmann, Jean L. Nakamura, Ken Nakamura, . A high-throughput screen of real-time ATP levels in individual cells reveals mechanisms of energy failure. PLOS Biology 2018, 16 (8) , e2004624. https://doi.org/10.1371/journal.pbio.2004624
    68. Niamh M. C. Connolly, Pierre Theurey, Vera Adam-Vizi, Nicolas G. Bazan, Paolo Bernardi, Juan P. Bolaños, Carsten Culmsee, Valina L. Dawson, Mohanish Deshmukh, Michael R. Duchen, Heiko Düssmann, Gary Fiskum, Maria F. Galindo, Giles E. Hardingham, J. Marie Hardwick, Mika B. Jekabsons, Elizabeth A. Jonas, Joaquin Jordán, Stuart A. Lipton, Giovanni Manfredi, Mark P. Mattson, BethAnn McLaughlin, Axel Methner, Anne N. Murphy, Michael P. Murphy, David G. Nicholls, Brian M. Polster, Tullio Pozzan, Rosario Rizzuto, Jorgina Satrústegui, Ruth S. Slack, Raymond A. Swanson, Russell H. Swerdlow, Yvonne Will, Zheng Ying, Alvin Joselin, Anna Gioran, Catarina Moreira Pinho, Orla Watters, Manuela Salvucci, Irene Llorente-Folch, David S. Park, Daniele Bano, Maria Ankarcrona, Paola Pizzo, Jochen H. M. Prehn. Guidelines on experimental methods to assess mitochondrial dysfunction in cellular models of neurodegenerative diseases. Cell Death & Differentiation 2018, 25 (3) , 542-572. https://doi.org/10.1038/s41418-017-0020-4
    69. Karin Writzl, Ales Maver, Lidija Kovačič, Paula Martinez-Valero, Laura Contreras, Jorgina Satrustegui, Marco Castori, Laurence Faivre, Pablo Lapunzina, André B.P. van Kuilenburg, Slobodanka Radović, Christel Thauvin-Robinet, Borut Peterlin, Araceli del Arco, Raoul C. Hennekam. De Novo Mutations in SLC25A24 Cause a Disorder Characterized by Early Aging, Bone Dysplasia, Characteristic Face, and Early Demise. The American Journal of Human Genetics 2017, 101 (5) , 844-855. https://doi.org/10.1016/j.ajhg.2017.09.017
    70. Ulrike Winkler, Pauline Seim, Yvonne Enzbrenner, Susanne Köhler, Marit Sicker, Johannes Hirrlinger. Activity‐dependent modulation of intracellular ATP in cultured cortical astrocytes. Journal of Neuroscience Research 2017, 95 (11) , 2172-2181. https://doi.org/10.1002/jnr.24020
    71. Giampaolo Morciano, Alba Clara Sarti, Saverio Marchi, Sonia Missiroli, Simonetta Falzoni, Lizzia Raffaghello, Vito Pistoia, Carlotta Giorgi, Francesco Di Virgilio, Paolo Pinton. Use of luciferase probes to measure ATP in living cells and animals. Nature Protocols 2017, 12 (8) , 1542-1562. https://doi.org/10.1038/nprot.2017.052
    72. Masaki Nakano, Hiromi Imamura, Norio Sasaoka, Masamichi Yamamoto, Norihito Uemura, Toshiyuki Shudo, Tomohiro Fuchigami, Ryosuke Takahashi, Akira Kakizuka. ATP Maintenance via Two Types of ATP Regulators Mitigates Pathological Phenotypes in Mouse Models of Parkinson's Disease. EBioMedicine 2017, 22 , 225-241. https://doi.org/10.1016/j.ebiom.2017.07.024
    73. Valentina De Col, Philippe Fuchs, Thomas Nietzel, Marlene Elsässer, Chia Pao Voon, Alessia Candeo, Ingo Seeliger, Mark D Fricker, Christopher Grefen, Ian Max Møller, Andrea Bassi, Boon Leong Lim, Marco Zancani, Andreas J Meyer, Alex Costa, Stephan Wagner, Markus Schwarzländer. ATP sensing in living plant cells reveals tissue gradients and stress dynamics of energy physiology. eLife 2017, 6 https://doi.org/10.7554/eLife.26770
    74. Leila Heidarvand, A. Harvey Millar, Nicolas L. Taylor. Responses of the Mitochondrial Respiratory System to Low Temperature in Plants. Critical Reviews in Plant Sciences 2017, 36 (4) , 217-240. https://doi.org/10.1080/07352689.2017.1375836
    75. Gerwyn Morris, Ken Walder, Sean L. McGee, Olivia M. Dean, Susannah J. Tye, Michael Maes, Michael Berk. A model of the mitochondrial basis of bipolar disorder. Neuroscience & Biobehavioral Reviews 2017, 74 , 1-20. https://doi.org/10.1016/j.neubiorev.2017.01.014
    76. Yanfei Zhang, José L. Avalos. Traditional and novel tools to probe the mitochondrial metabolism in health and disease. WIREs Systems Biology and Medicine 2017, 9 (2) https://doi.org/10.1002/wsbm.1373
    77. Tomoki Yoshida, Soaad Alfaqaan, Norio Sasaoka, Hiromi Imamura. Application of FRET-Based Biosensor “ATeam” for Visualization of ATP Levels in the Mitochondrial Matrix of Living Mammalian Cells. 2017, 231-243. https://doi.org/10.1007/978-1-4939-6824-4_14
    78. Lauren Y. Shields, Bryce A. Mendelsohn, Ken Nakamura. Measuring ATP in Axons with FRET. 2017, 115-131. https://doi.org/10.1007/978-1-4939-6890-9_6
    79. Diana Pendin, Elisa Greotti, Konstantinos Lefkimmiatis, Tullio Pozzan. Exploring cells with targeted biosensors. Journal of General Physiology 2017, 149 (1) , 1-36. https://doi.org/10.1085/jgp.201611654
    80. Tomoki Yoshida, Akira Kakizuka, Hiromi Imamura. BTeam, a Novel BRET-based Biosensor for the Accurate Quantification of ATP Concentration within Living Cells. Scientific Reports 2016, 6 (1) https://doi.org/10.1038/srep39618
    81. Thorsten Erdmann, Kathrin Bartelheimer, Ulrich S. Schwarz. Sensitivity of small myosin II ensembles from different isoforms to mechanical load and ATP concentration. Physical Review E 2016, 94 (5) https://doi.org/10.1103/PhysRevE.94.052403
    82. David G. Nicholls. The Pancreatic β-Cell: A Bioenergetic Perspective. Physiological Reviews 2016, 96 (4) , 1385-1447. https://doi.org/10.1152/physrev.00009.2016
    83. Christine S. Gibhardt, Katharina M. Zimmermann, Xin Zhang, Vsevolod V. Belousov, Ivan Bogeski. Imaging calcium and redox signals using genetically encoded fluorescent indicators. Cell Calcium 2016, 60 (2) , 55-64. https://doi.org/10.1016/j.ceca.2016.04.008
    84. Megha Rajendran, Eric Dane, Jason Conley, Mathew Tantama. Imaging Adenosine Triphosphate (ATP). The Biological Bulletin 2016, 231 (1) , 73-84. https://doi.org/10.1086/689592
    85. Bing Zhou, Panpan Yu, Mei-Yao Lin, Tao Sun, Yanmin Chen, Zu-Hang Sheng. Facilitation of axon regeneration by enhancing mitochondrial transport and rescuing energy deficits. Journal of Cell Biology 2016, 214 (1) , 103-119. https://doi.org/10.1083/jcb.201605101
    86. Benjamin Wacquier, Laurent Combettes, Guy Tran Van Nhieu, Geneviève Dupont. Interplay Between Intracellular Ca2+ Oscillations and Ca2+-stimulated Mitochondrial Metabolism. Scientific Reports 2016, 6 (1) https://doi.org/10.1038/srep19316
    87. Veli V Uslu, Guido Grossmann. The biosensor toolbox for plant developmental biology. Current Opinion in Plant Biology 2016, 29 , 138-147. https://doi.org/10.1016/j.pbi.2015.12.001
    88. Martin Pelosse, Cécile Cottet-Rousselle, Alexei Grichine, Imre Berger, Uwe Schlattner. Genetically Encoded Fluorescent Biosensors to Explore AMPK Signaling and Energy Metabolism. 2016, 491-523. https://doi.org/10.1007/978-3-319-43589-3_20
    89. Andrew D. James, Waseema Patel, Zohra Butt, Magretta Adiamah, Raga Dakhel, Ayse Latif, Carolina Uggenti, Eileithyia Swanton, Hiromi Imamura, Ajith K. Siriwardena, Jason I.E. Bruce. The Plasma Membrane Calcium Pump in Pancreatic Cancer Cells Exhibiting the Warburg Effect Relies on Glycolytic ATP. Journal of Biological Chemistry 2015, 290 (41) , 24760-24771. https://doi.org/10.1074/jbc.M115.668707
    90. Liron Boyman, George S. B. Williams, W. J. Lederer. The growing importance of mitochondrial calcium in health and disease. Proceedings of the National Academy of Sciences 2015, 112 (36) , 11150-11151. https://doi.org/10.1073/pnas.1514284112
    91. Takahiro Shibata, Saki Yamashita, Kotoe Hirusaki, Kaoru Katoh, Yoshihiro Ohta. Isolation of mitochondria by gentle cell membrane disruption, and their subsequent characterization. Biochemical and Biophysical Research Communications 2015, 463 (4) , 563-568. https://doi.org/10.1016/j.bbrc.2015.05.095
    92. Markus Waldeck-Weiermair, Helmut Bischof, Sandra Blass, Andras Deak, Christiane Klec, Thomas Graier, Clara Roller, Rene Rost, Emrah Eroglu, Benjamin Gottschalk, Nicole Hofmann, Wolfgang Graier, Roland Malli. Generation of Red-Shifted Cameleons for Imaging Ca2+ Dynamics of the Endoplasmic Reticulum. Sensors 2015, 15 (6) , 13052-13068. https://doi.org/10.3390/s150613052
    93. Carlos B. Rueda, Javier Traba, Ignacio Amigo, Irene Llorente-Folch, Paloma González-Sánchez, Beatriz Pardo, José A. Esteban, Araceli del Arco, Jorgina Satrústegui. Mitochondrial ATP-Mg/Pi Carrier SCaMC-3/Slc25a23 Counteracts PARP-1-Dependent Fall in Mitochondrial ATP Caused by Excitotoxic Insults in Neurons. The Journal of Neuroscience 2015, 35 (8) , 3566-3581. https://doi.org/10.1523/JNEUROSCI.2702-14.2015
    94. András T. Deak, Claire Jean-Quartier, Alexander I. Bondarenko, Lukas N. Groschner, Roland Malli, Wolfgang F. Graier, Markus Waldeck-Weiermair. Assessment of Mitochondrial Ca2+ Uptake. 2015, 421-439. https://doi.org/10.1007/978-1-4939-2257-4_35
    95. Hideyuki Yaginuma, Shinnosuke Kawai, Kazuhito V. Tabata, Keisuke Tomiyama, Akira Kakizuka, Tamiki Komatsuzaki, Hiroyuki Noji, Hiromi Imamura. Diversity in ATP concentrations in a single bacterial cell population revealed by quantitative single-cell imaging. Scientific Reports 2014, 4 (1) https://doi.org/10.1038/srep06522
    96. Roberto De Michele, Francesco Carimi, Wolf B. Frommer. Mitochondrial biosensors. The International Journal of Biochemistry & Cell Biology 2014, 48 , 39-44. https://doi.org/10.1016/j.biocel.2013.12.014
    97. Adeleye J. Afolayan, Ru-Jeng Teng, Annie Eis, Ujala Rana, Katarzyna A. Broniowska, John A. Corbett, Kirkwood Pritchard, Girija G. Konduri. Inducible HSP70 regulates superoxide dismutase-2 and mitochondrial oxidative stress in the endothelial cells from developing lungs. American Journal of Physiology-Lung Cellular and Molecular Physiology 2014, 306 (4) , L351-L360. https://doi.org/10.1152/ajplung.00264.2013
    98. Neelanjan Vishnu, Muhammad Jadoon Khan, Felix Karsten, Lukas N. Groschner, Markus Waldeck-Weiermair, Rene Rost, Seth Hallström, Hiromi Imamura, Wolfgang F. Graier, Roland Malli, . ATP increases within the lumen of the endoplasmic reticulum upon intracellular Ca 2+ release. Molecular Biology of the Cell 2014, 25 (3) , 368-379. https://doi.org/10.1091/mbc.e13-07-0433
    99. Andrei I. Tarasov, Guy A. Rutter. Use of Genetically Encoded Sensors to Monitor Cytosolic ATP/ADP Ratio in Living Cells. 2014, 289-311. https://doi.org/10.1016/B978-0-12-416618-9.00015-7
    100. Takashi Tanaka, Kazuaki Nagashima, Nobuya Inagaki, Hidetaka Kioka, Seiji Takashima, Hajime Fukuoka, Hiroyuki Noji, Akira Kakizuka, Hiromi Imamura. Glucose-stimulated Single Pancreatic Islets Sustain Increased Cytosolic ATP Levels during Initial Ca2+ Influx and Subsequent Ca2+ Oscillations. Journal of Biological Chemistry 2014, 289 (4) , 2205-2216. https://doi.org/10.1074/jbc.M113.499111
    Load all citations

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    You’ve supercharged your research process with ACS and Mendeley!

    STEP 1:
    Click to create an ACS ID

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    MENDELEY PAIRING EXPIRED
    Your Mendeley pairing has expired. Please reconnect