Molecular probes for tracking lipid droplet membrane dynamics.

Lipid Droplets / metabolism Molecular Probes / chemistry Humans Membrane Proteins / metabolism Animals HeLa Cells Fluorescent Dyes / chemistry Membrane Lipids / metabolism Cell Membrane / metabolism

Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
31 Oct 2024
Historique:
received: 15 02 2024
accepted: 16 10 2024
medline: 1 11 2024
pubmed: 1 11 2024
entrez: 1 11 2024
Statut: epublish

Résumé

Lipid droplets (LDs) feature a unique monolayer lipid membrane that has not been extensively studied due to the lack of suitable molecular probes that are able to distinguish this membrane from the LD lipid core. In this work, we present a three-pronged molecular probe design strategy that combines lipophilicity-based organelle targeting with microenvironment-dependent activation and design an LD membrane labeling pro-probe called LDM. Upon activation by the HClO/ClO

Identifiants

DOI: 10.1038/s41467-024-53667-7 PMID: 39482302
pubmed: 39482302
doi: 10.1038/s41467-024-53667-7
pii: 10.1038/s41467-024-53667-7
doi:

Substances chimiques

Molecular Probes 0
Membrane Proteins 0
Fluorescent Dyes 0
Membrane Lipids 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

9413

Subventions

Organisme : National University of Singapore (NUS)
ID : NUHSRO/2020/133/Startup/08
Organisme : National University of Singapore (NUS)
ID : NUHSRO/2020/133/Startup/08
Organisme : National University of Singapore (NUS)
ID : NUHSRO/2020/133/Startup/08

Informations de copyright

© 2024. The Author(s).

Références

Grabner, G. F., Xie, H., Schweiger, M. & Zechner, R. Lipolysis: cellular mechanisms for lipid mobilization from fat stores. Nat. Metab. 3, 1445–1465 (2021).
pubmed: 34799702 doi: 10.1038/s42255-021-00493-6
Roberts, M. A. & Olzmann, J. A. Protein Quality Control and Lipid Droplet Metabolism. Annu Rev. Cell Dev. Biol. 36, 115–139 (2020).
pubmed: 33021827 pmcid: 7593838 doi: 10.1146/annurev-cellbio-031320-101827
Mece, O. et al. Lipid droplet degradation by autophagy connects mitochondria metabolism to Prox1-driven expression of lymphatic genes and lymphangiogenesis. Nat. Commun. 13, 2760 (2022).
pubmed: 35589749 pmcid: 9120506 doi: 10.1038/s41467-022-30490-6
Talari, N. K. et al. Lipid-droplet associated mitochondria promote fatty-acid oxidation through a distinct bioenergetic pattern in male Wistar rats. Nat. Commun. 14, 766 (2023).
pubmed: 36765117 pmcid: 9918515 doi: 10.1038/s41467-023-36432-0
Olzmann, J. A. & Carvalho, P. Dynamics and functions of lipid droplets. Nat. Rev. Mol. Cell Biol. 20, 137–155 (2019).
pubmed: 30523332 pmcid: 6746329 doi: 10.1038/s41580-018-0085-z
Mau, K. H. T. et al. Dynamic enlargement and mobilization of lipid droplets in pluripotent cells coordinate morphogenesis during mouse peri-implantation development. Nat. Commun. 13, 3861 (2022).
pubmed: 35790717 pmcid: 9256688 doi: 10.1038/s41467-022-31323-2
Tian, H. et al. Fluorescent probes for the imaging of lipid droplets in live cells. Coordination Chemistry Reviews 427, https://doi.org/10.1016/j.ccr.2020.213577 (2021).
Chen, J. et al. Stable Super-Resolution Imaging of Lipid Droplet Dynamics through a Buffer Strategy with a Hydrogen-Bond Sensitive Fluorogenic Probe. Angew. Chem. Int Ed. Engl. 60, 25104–25113 (2021).
pubmed: 34519394 doi: 10.1002/anie.202111052
Liu, G. et al. Ultrabright organic fluorescent probe for quantifying the dynamics of cytosolic/nuclear lipid droplets. Biosensors and Bioelectronics 241, https://doi.org/10.1016/j.bios.2023.115707 (2023).
Song, C. W. et al. A rationally designed polarity–viscosity sensitive probe for imaging lipid droplets. Dyes and Pigments 171, https://doi.org/10.1016/j.dyepig.2019.107718 (2019).
Ye, Z. et al. In-Sequence High-Specificity Dual-Reporter Unlocking of Fluorescent Probe Enables the Precise Identification of Atherosclerotic Plaques. Angew. Chem. Int Ed. Engl. 61, e202204518 (2022).
pubmed: 35460326 doi: 10.1002/anie.202204518
Fan, L. et al. Lipid Droplet-Specific Fluorescent Probe for In Vivo Visualization of Polarity in Fatty Liver, Inflammation, and Cancer Models. Anal. Chem. 93, 8019–8026 (2021).
pubmed: 34037378 doi: 10.1021/acs.analchem.1c01125
Halaoui, R. & McCaffrey, L. Rewiring cell polarity signaling in cancer. Oncogene 34, 939–950 (2015).
pubmed: 24632617 doi: 10.1038/onc.2014.59
Zhanghao, K. et al. High-dimensional super-resolution imaging reveals heterogeneity and dynamics of subcellular lipid membranes. Nat. Commun. 11, 5890 (2020).
pubmed: 33208737 pmcid: 7674432 doi: 10.1038/s41467-020-19747-0
Peng, G. et al. Highly Efficient Red/NIR-Emissive Fluorescent Probe with Polarity-Sensitive Character for Visualizing Cellular Lipid Droplets and Determining Their Polarity. Anal. Chem. 94, 12095–12102 (2022).
pubmed: 36006461 doi: 10.1021/acs.analchem.2c02077
Zhang, J. et al. Mitochondrial-Targeted Delivery of Polyphenol-Mediated Antioxidases Complexes against Pyroptosis and Inflammatory Diseases. Adv. Mater. 35, e2208571 (2023).
pubmed: 36648306 doi: 10.1002/adma.202208571
Li, Y. et al. Engineering polyphenols with biological functions via polyphenol-protein interactions as additives for functional foods. Trends Food Sci. Technol. 110, 470–482 (2021).
doi: 10.1016/j.tifs.2021.02.009
Shi, D., Liu, W., Wang, G., Guo, Y. & Li, J. Small-molecule fluorescence-based probes for aging diagnosis %J. Acta Mater. Med. 1, 4–23 (2022).
Zhang, X. et al. Ratiometric fluorescent probes for capturing endogenous hypochlorous acid in the lungs of mice. Chem. Sci. 9, 8207–8212 (2018).
pubmed: 30542568 pmcid: 6240892 doi: 10.1039/C8SC03226B
Yao, L., Song, H., Yin, C. & Huo, F. An ICT-switched fluorescent probe for visualizing lipid and HClO in lipid droplets during ferroptosis. Chem. Commun. 60, 835–838 (2024).
doi: 10.1039/D3CC05679A
Yang, X. et al. Visualization of biothiols and HClO in cancer therapy via a multi-responsive fluorescent probe. Sensors and Actuators B: Chemical 347, https://doi.org/10.1016/j.snb.2021.130620 (2021).
Lu, J. et al. Assessing Early Atherosclerosis by Detecting and Imaging of Hypochlorous Acid and Phosphorylation Using Fluorescence Nanoprobe. Advanced Materials 35, https://doi.org/10.1002/adma.202307008 (2023).
Zadoorian, A., Du, X. & Yang, H. Lipid droplet biogenesis and functions in health and disease. Nat. Rev. Endocrinol. 19, 443–459 (2023).
pubmed: 37221402 doi: 10.1038/s41574-023-00845-0
Kitamura, T., Takagi, S., Naganuma, T. & Kihara, A. Mouse aldehyde dehydrogenase ALDH3B2 is localized to lipid droplets via two C-terminal tryptophan residues and lipid modification. Biochem J. 465, 79–87 (2015).
pubmed: 25286108 doi: 10.1042/BJ20140624
Schwefel, D. et al. Structural insights into the mechanism of GTPase activation in the GIMAP family. Structure 21, 550–559 (2013).
pubmed: 23454188 doi: 10.1016/j.str.2013.01.014
Cobbe, N. et al. The conserved metalloprotease invadolysin localizes to the surface of lipid droplets. J. Cell Sci. 122, 3414–3423 (2009).
pubmed: 19706689 pmcid: 2736869 doi: 10.1242/jcs.044610
Yuan, M., Lin, X., Wang, D. & Dai, J. Proteins: Neglected active ingredients in edible bird’s nest. Chin. Herb. Med. 15, 383–390 (2023).
pubmed: 37538855 pmcid: 10394320
Zhou, R. et al. Stimulated Emission Depletion (STED) Super-Resolution Imaging with an Advanced Organic Fluorescent Probe: Visualizing the Cellular Lipid Droplets at the Unprecedented Nanoscale Resolution. ACS Mater. Lett. 3, 516–524 (2021).
doi: 10.1021/acsmaterialslett.1c00143
Zhou, R. et al. A new organic molecular probe as a powerful tool for fluorescence imaging and biological study of lipid droplets. Theranostics 13, 95–105 (2023).
pubmed: 36593956 pmcid: 9800742 doi: 10.7150/thno.79052
Cao, M. et al. Structure Rigidification Promoted Ultrabright Solvatochromic Fluorescent Probes for Super-Resolution Imaging of Cytosolic and Nuclear Lipid Droplets. Anal. Chem. 94, 10676–10684 (2022).
pubmed: 35853217 doi: 10.1021/acs.analchem.2c00964
Dai, J. et al. Super-resolution dynamic tracking of cellular lipid droplets employing with a photostable deep red fluorogenic probe. Biosensors and Bioelectronics 229, https://doi.org/10.1016/j.bios.2023.115243 (2023).
Chen, Q. et al. A dual-labeling probe to track functional mitochondria-lysosome interactions in live cells. Nat. Commun. 11, 6290 (2020).
pubmed: 33293545 pmcid: 7722883 doi: 10.1038/s41467-020-20067-6
Wu, Y. & Shroff, H. Faster, sharper, and deeper: structured illumination microscopy for biological imaging. Nat. Methods 15, 1011–1019 (2018).
pubmed: 30478322 doi: 10.1038/s41592-018-0211-z
Bickel, P. E., Tansey, J. T. & Welte, M. A. PAT proteins, an ancient family of lipid droplet proteins that regulate cellular lipid stores. Biochimica et. Biophysica Acta (BBA) - Mol. Cell Biol. Lipids 1791, 419–440 (2009).
doi: 10.1016/j.bbalip.2009.04.002
Wu, Y. et al. Plin2-mediated lipid droplet mobilization accelerates exit from pluripotency by lipidomic remodeling and histone acetylation. Cell Death Differ. 29, 2316–2331 (2022).
pubmed: 35614132 pmcid: 9613632 doi: 10.1038/s41418-022-01018-8
Kong, F. et al. Traditional Chinese medicines for non-small cell lung cancer: Therapies and mechanisms. Chin. Herb. Med. 15, 509–515 (2023).
pubmed: 38094015 pmcid: 10715886
Lyu, X. et al. A gel-like condensation of Cidec generates lipid-permeable plates for lipid droplet fusion. Dev. Cell 56, 2592–2606 e2597 (2021).
pubmed: 34508658 doi: 10.1016/j.devcel.2021.08.015
Thiam, A. R., Farese, R. V. Jr. & Walther, T. C. The biophysics and cell biology of lipid droplets. Nat. Rev. Mol. Cell Biol. 14, 775–786 (2013).
pubmed: 24220094 pmcid: 4526153 doi: 10.1038/nrm3699
Tatenaka, Y. et al. Monitoring Lipid Droplet Dynamics in Living Cells by Using Fluorescent Probes. Biochemistry 58, 499–503 (2019).
pubmed: 30628446 doi: 10.1021/acs.biochem.8b01071
Honig, B. & Shapiro, L. Adhesion Protein Structure, Molecular Affinities, and Principles of Cell-Cell Recognition. Cell 181, 520–535 (2020).
pubmed: 32359436 pmcid: 7233459 doi: 10.1016/j.cell.2020.04.010
Zhou, Z. et al. Phosphorylation regulates the binding of autophagy receptors to FIP200 Claw domain for selective autophagy initiation. Nat. Commun. 12, 1570 (2021).
pubmed: 33692357 pmcid: 7946963 doi: 10.1038/s41467-021-21874-1
Liu, K. & Czaja, M. J. Regulation of lipid stores and metabolism by lipophagy. Cell Death Differ. 20, 3–11 (2013).
pubmed: 22595754 doi: 10.1038/cdd.2012.63
Nakatogawa, H. Mechanisms governing autophagosome biogenesis. Nat. Rev. Mol. Cell Biol. 21, 439–458 (2020).
pubmed: 32372019 doi: 10.1038/s41580-020-0241-0
Martínez-Reyes, I. & Chandel, N. S. Cancer metabolism: looking forward. Nat. Rev. Cancer 21, 669–680 (2021).
pubmed: 34272515 doi: 10.1038/s41568-021-00378-6
Fan, T. et al. Metabolomic and transcriptomic profiling of hepatocellular carcinomas in Hras12V transgenic mice. Cancer Med. 6, 2370–2384 (2017).
pubmed: 28941178 pmcid: 5633588 doi: 10.1002/cam4.1177
Liu, R. et al. Choline kinase alpha 2 acts as a protein kinase to promote lipolysis of lipid droplets. Mol. Cell 81, 2722–2735.e2729 (2021).
pubmed: 34077757 doi: 10.1016/j.molcel.2021.05.005
Zhou, L. et al. Coordination Among Lipid Droplets, Peroxisomes, and Mitochondria Regulates Energy Expenditure Through the CIDE-ATGL-PPARα Pathway in Adipocytes. Diabetes 67, 1935–1948 (2018).
pubmed: 29986925 doi: 10.2337/db17-1452
Wang, J. et al. An ESCRT-dependent step in fatty acid transfer from lipid droplets to mitochondria through VPS13D-TSG101 interactions. Nature Communications 12, https://doi.org/10.1038/s41467-021-21525-5 (2021).
Yu, Z. et al. In situ visualization of the cellular uptake and sub-cellular distribution of mussel oligosaccharides. Journal of Pharmaceutical Analysis 14, https://doi.org/10.1016/j.jpha.2023.12.022 (2024).
Tang, Z.-H. et al. Induction of reactive oxygen species-stimulated distinctive autophagy by chelerythrine in non-small cell lung cancer cells. Redox Biol. 12, 367–376 (2017).
pubmed: 28288416 pmcid: 5349618 doi: 10.1016/j.redox.2017.03.009
Gao, W.-Y. et al. Tanshinone IIA Downregulates Lipogenic Gene Expression and Attenuates Lipid Accumulation through the Modulation of LXRα/SREBP1 Pathway in HepG2 Cells. Biomedicines 9, https://doi.org/10.3390/biomedicines9030326 (2021).
Dean, K. M. & Palmer, A. E. Advances in fluorescence labeling strategies for dynamic cellular imaging. Nat. Chem. Biol. 10, 512–523 (2014).
pubmed: 24937069 pmcid: 4248787 doi: 10.1038/nchembio.1556
Sancho, A., Vandersmissen, I., Craps, S., Luttun, A. & Groll, J. A new strategy to measure intercellular adhesion forces in mature cell-cell contacts. Sci. Rep. 7, 46152 (2017).
pubmed: 28393890 pmcid: 5385528 doi: 10.1038/srep46152
Henne, W. M., Reese, M. L. & Goodman, J. M. The assembly of lipid droplets and their roles in challenged cells. EMBO J 37, https://doi.org/10.15252/embj.201898947 (2018).
Ramosaj, M. et al. Lipid droplet availability affects neural stem/progenitor cell metabolism and proliferation. Nat. Commun. 12, 7362 (2021).
pubmed: 34934077 pmcid: 8692608 doi: 10.1038/s41467-021-27365-7
Gerst, R., Cseresnyés, Z. & Figge, M. T. JIPipe: visual batch processing for ImageJ. Nat. Methods 20, 168–169 (2023).
pubmed: 36627450 doi: 10.1038/s41592-022-01744-4

Auteurs

Lingxiu Kong (L)

School of Pharmaceutical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong, 250117, PR China.

Qingjie Bai (Q)

School of Pharmaceutical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong, 250117, PR China.
Medical Science and Technology Innovation Center, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong, 250117, PR China.

Cuicui Li (C)

Departments of Diagnostic Radiology, Surgery, Chemical and Biomolecular Engineering, and Biomedical Engineering, Yong Loo Lin School of Medicine and College of Design and Engineering, National University of Singapore, Singapore, 119074, Singapore.
Clinical Imaging Research Centre, Centre for Translational Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, 117599, Singapore.
Nanomedicine Translational Research Program, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, 117597, Singapore.
Theranostics Center of Excellence (TCE), Yong Loo Lin School of Medicine, National University of Singapore, 11 Biopolis Way, Helios, Singapore, 138667, Singapore.

Qiqin Wang (Q)

School of Pharmaceutical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong, 250117, PR China.
College of Pharmacy, Jinan University, Guangzhou, 510632, PR China.

Yanfeng Wang (Y)

School of Pharmaceutical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong, 250117, PR China.

Xintian Shao (X)

School of Pharmaceutical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong, 250117, PR China.
Medical Science and Technology Innovation Center, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong, 250117, PR China.
Neck-Shoulder and Lumbocrural Pain Hospital, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong, 250117, PR China.

Yongchun Wei (Y)

School of Pharmaceutical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong, 250117, PR China.

Jiarao Sun (J)

School of Pharmaceutical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong, 250117, PR China.

Zhenjie Yu (Z)

School of Pharmaceutical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong, 250117, PR China.

Junling Yin (J)

Medical Science and Technology Innovation Center, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong, 250117, PR China.

Bin Shi (B)

Medical Science and Technology Innovation Center, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong, 250117, PR China.
Neck-Shoulder and Lumbocrural Pain Hospital, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong, 250117, PR China.

Hongbao Fang (H)

College of Chemistry and Materials Science, Nanjing Normal University, Nanjing, 210023, PR China.

Xiaoyuan Chen (X)

Departments of Diagnostic Radiology, Surgery, Chemical and Biomolecular Engineering, and Biomedical Engineering, Yong Loo Lin School of Medicine and College of Design and Engineering, National University of Singapore, Singapore, 119074, Singapore. chen.shawn@nus.edu.sg.
Clinical Imaging Research Centre, Centre for Translational Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, 117599, Singapore. chen.shawn@nus.edu.sg.
Nanomedicine Translational Research Program, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, 117597, Singapore. chen.shawn@nus.edu.sg.
Theranostics Center of Excellence (TCE), Yong Loo Lin School of Medicine, National University of Singapore, 11 Biopolis Way, Helios, Singapore, 138667, Singapore. chen.shawn@nus.edu.sg.
Institute of Molecular and Cell Biology, Agency for Science, Technology, and Research (A*STAR), 61 Biopolis Drive, Proteos, Singapore, 138673, Singapore. chen.shawn@nus.edu.sg.
ORCID: 0000-0002-9622-0870

Qixin Chen (Q)

School of Pharmaceutical Sciences, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong, 250117, PR China. chenqixin@sdfmu.edu.cn.
Medical Science and Technology Innovation Center, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong, 250117, PR China. chenqixin@sdfmu.edu.cn.
Departments of Diagnostic Radiology, Surgery, Chemical and Biomolecular Engineering, and Biomedical Engineering, Yong Loo Lin School of Medicine and College of Design and Engineering, National University of Singapore, Singapore, 119074, Singapore. chenqixin@sdfmu.edu.cn.
Nanomedicine Translational Research Program, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, 117597, Singapore. chenqixin@sdfmu.edu.cn.
Theranostics Center of Excellence (TCE), Yong Loo Lin School of Medicine, National University of Singapore, 11 Biopolis Way, Helios, Singapore, 138667, Singapore. chenqixin@sdfmu.edu.cn.
Institute of Molecular and Cell Biology, Agency for Science, Technology, and Research (A*STAR), 61 Biopolis Drive, Proteos, Singapore, 138673, Singapore. chenqixin@sdfmu.edu.cn.
ORCID: 0000-0002-2998-5582

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Effectiveness of Virtual Yoga for Chronic Low Back Pain: A Randomized Clinical Trial.

Hallie Tankha, Devyn Gaskins, Amanda Shallcross et al.
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH

questionsmedicales.fr › Cellules › Structures cellulaires › Espace intracellulaire › Cytoplasme › Structures cytoplasmiques › Organites › Gouttelettes lipidiques › Molecular probes for tracking lipid droplet...
questionsmedicales.fr › Actions chimiques et utilisations › Utilisations spécialisées de produits chimiques › Produits chimiques de laboratoire › Sondes moléculaires › Molecular probes for tracking lipid droplet...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Molecular probes for tracking lipid droplet...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Molecular probes for tracking lipid droplet...
questionsmedicales.fr › Eucaryotes › Animaux › Molecular probes for tracking lipid droplet...
questionsmedicales.fr › Cellules › Cellules épithéliales › Cellules HeLa › Molecular probes for tracking lipid droplet...
questionsmedicales.fr › Actions chimiques et utilisations › Utilisations spécialisées de produits chimiques › Produits chimiques de laboratoire › Indicateurs et réactifs › Luminescents › Colorants fluorescents › Molecular probes for tracking lipid droplet...
questionsmedicales.fr › Lipides › Lipides membranaires › Molecular probes for tracking lipid droplet...
questionsmedicales.fr › Cellules › Structures cellulaires › Membrane cellulaire › Molecular probes for tracking lipid droplet...