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Ratiometric measurement of MAM Ca2+ dynamics using a modified CalfluxVTN

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  • Eunbyul Cho

    (Pohang University of Science and Technology)

  • Youngsik Woo

    (Pohang University of Science and Technology)

  • Yeongjun Suh

    (Pohang University of Science and Technology)

  • Bo Kyoung Suh

    (Pohang University of Science and Technology)

  • Soo Jeong Kim

    (Pohang University of Science and Technology)

  • Truong Thi My Nhung

    (Pohang University of Science and Technology)

  • Jin Yeong Yoo

    (Pohang University of Science and Technology)

  • Tran Diem Nghi

    (Pohang University of Science and Technology)

  • Su Been Lee

    (Pohang University of Science and Technology)

  • Dong Jin Mun

    (Pohang University of Science and Technology)

  • Sang Ki Park

    (Pohang University of Science and Technology)

Abstract

Mitochondria-associated ER membrane (MAM) is a structure where these calcium-regulating organelles form close physical contact sites for efficient Ca2+ crosstalk. Despite the central importance of MAM Ca2+ dynamics in diverse biological processes, directly and specifically measuring Ca2+ concentrations inside MAM is technically challenging. Here, we develop MAM-Calflux, a MAM-specific BRET-based Ca2+ indicator. The successful application of the bimolecular fluorescence complementation (BiFC) concept highlights Ca2+-responsive BRET signals in MAM. The BiFC strategy imparts dual functionality as a Ca2+ indicator and quantitative structural marker specific for MAM. As a ratiometric Ca2+ indicator, MAM-Calflux estimates steady-state MAM Ca2+ levels. Finally, it enables the visualization of uneven intracellular distribution of MAM Ca2+ and the elucidation of abnormally accumulated MAM Ca2+ from the neurons of Parkinson’s disease mouse model in both steady-state and stimulated conditions. Therefore, we propose that MAM-Calflux can be a versatile tool for ratiometrically measuring dynamic inter-organellar Ca2+ communication.

Suggested Citation

  • Eunbyul Cho & Youngsik Woo & Yeongjun Suh & Bo Kyoung Suh & Soo Jeong Kim & Truong Thi My Nhung & Jin Yeong Yoo & Tran Diem Nghi & Su Been Lee & Dong Jin Mun & Sang Ki Park, 2023. "Ratiometric measurement of MAM Ca2+ dynamics using a modified CalfluxVTN," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39343-2
    DOI: 10.1038/s41467-023-39343-2
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    1. Francesca Vallese & Cristina Catoni & Domenico Cieri & Lucia Barazzuol & Omar Ramirez & Valentina Calore & Massimo Bonora & Flavia Giamogante & Paolo Pinton & Marisa Brini & Tito Calì, 2020. "An expanded palette of improved SPLICS reporters detects multiple organelle contacts in vitro and in vivo," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    2. Taufiq-Ur-Rahman & Alexander Skupin & Martin Falcke & Colin W. Taylor, 2009. "Clustering of InsP3 receptors by InsP3 retunes their regulation by InsP3 and Ca2+," Nature, Nature, vol. 458(7238), pages 655-659, April.
    3. Adam Bartok & David Weaver & Tünde Golenár & Zuzana Nichtova & Máté Katona & Száva Bánsághi & Kamil J. Alzayady & V. Kaye Thomas & Hideaki Ando & Katsuhiko Mikoshiba & Suresh K. Joseph & David I. Yule, 2019. "IP3 receptor isoforms differently regulate ER-mitochondrial contacts and local calcium transfer," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    4. Junji Suzuki & Kazunori Kanemaru & Kuniaki Ishii & Masamichi Ohkura & Yohei Okubo & Masamitsu Iino, 2014. "Imaging intraorganellar Ca2+ at subcellular resolution using CEPIA," Nature Communications, Nature, vol. 5(1), pages 1-13, September.
    5. Diego De Stefani & Anna Raffaello & Enrico Teardo & Ildikò Szabò & Rosario Rizzuto, 2011. "A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter," Nature, Nature, vol. 476(7360), pages 336-340, August.
    6. Olga Martins de Brito & Luca Scorrano, 2008. "Mitofusin 2 tethers endoplasmic reticulum to mitochondria," Nature, Nature, vol. 456(7222), pages 605-610, December.
    7. Jie Yang & Derrick Cumberbatch & Samuel Centanni & Shu-qun Shi & Danny Winder & Donna Webb & Carl Hirschie Johnson, 2016. "Coupling optogenetic stimulation with NanoLuc-based luminescence (BRET) Ca++ sensing," Nature Communications, Nature, vol. 7(1), pages 1-10, December.
    8. Souvik Modi & Guillermo López-Doménech & Elise F. Halff & Christian Covill-Cooke & Davor Ivankovic & Daniela Melandri & I. Lorena Arancibia-Cárcamo & Jemima J. Burden & Alan R. Lowe & Josef T. Kittler, 2019. "Miro clusters regulate ER-mitochondria contact sites and link cristae organization to the mitochondrial transport machinery," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    9. Radu Stoica & Kurt J. De Vos & Sébastien Paillusson & Sarah Mueller & Rosa M. Sancho & Kwok-Fai Lau & Gema Vizcay-Barrena & Wen-Lang Lin & Ya-Fei Xu & Jada Lewis & Dennis W. Dickson & Leonard Petrucel, 2014. "ER–mitochondria associations are regulated by the VAPB–PTPIP51 interaction and are disrupted by ALS/FTD-associated TDP-43," Nature Communications, Nature, vol. 5(1), pages 1-12, September.
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