In vivo fluorescence lifetime imaging of macrophage intracellular metabolism during wound responses in zebrafish
The function of macrophages in vitro is linked to their metabolic rewiring. However, macrophage metabolism remains poorly characterized in situ. Here, we used two-photon intensity and lifetime imaging of autofluorescent metabolic coenzymes, nicotinamide adenine dinucleotide (phosphate) (NAD(P)H) and...
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Published in | eLife Vol. 11 |
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Main Authors | , , , , , , , , , , , |
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eLife Sciences Publications Ltd
24.02.2022
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Abstract | The function of macrophages in vitro is linked to their metabolic rewiring. However, macrophage metabolism remains poorly characterized in situ. Here, we used two-photon intensity and lifetime imaging of autofluorescent metabolic coenzymes, nicotinamide adenine dinucleotide (phosphate) (NAD(P)H) and flavin adenine dinucleotide (FAD), to assess the metabolism of macrophages in the wound microenvironment. Inhibiting glycolysis reduced NAD(P)H mean lifetime and made the intracellular redox state of macrophages more oxidized, as indicated by reduced optical redox ratio. We found that TNFα+ macrophages had lower NAD(P)H mean lifetime and were more oxidized compared to TNFα- macrophages. Both infection and thermal injury induced a macrophage population with a more oxidized redox state in wounded tissues. Kinetic analysis detected temporal changes in the optical redox ratio during tissue repair, revealing a shift toward a more reduced redox state over time. Metformin reduced TNFα+ wound macrophages, made intracellular redox state more reduced and improved tissue repair. By contrast, depletion of STAT6 increased TNFα+ wound macrophages, made redox state more oxidized and impaired regeneration. Our findings suggest that autofluorescence of NAD(P)H and FAD is sensitive to dynamic changes in intracellular metabolism in tissues and can be used to probe the temporal and spatial regulation of macrophage metabolism during tissue damage and repair. |
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AbstractList | The function of macrophages in vitro is linked to their metabolic rewiring. However, macrophage metabolism remains poorly characterized in situ. Here, we used two-photon intensity and lifetime imaging of autofluorescent metabolic coenzymes, nicotinamide adenine dinucleotide (phosphate) (NAD(P)H) and flavin adenine dinucleotide (FAD), to assess the metabolism of macrophages in the wound microenvironment. Inhibiting glycolysis reduced NAD(P)H mean lifetime and made the intracellular redox state of macrophages more oxidized, as indicated by reduced optical redox ratio. We found that TNFα+ macrophages had lower NAD(P)H mean lifetime and were more oxidized compared to TNFα− macrophages. Both infection and thermal injury induced a macrophage population with a more oxidized redox state in wounded tissues. Kinetic analysis detected temporal changes in the optical redox ratio during tissue repair, revealing a shift toward a more reduced redox state over time. Metformin reduced TNFα+ wound macrophages, made intracellular redox state more reduced and improved tissue repair. By contrast, depletion of STAT6 increased TNFα+ wound macrophages, made redox state more oxidized and impaired regeneration. Our findings suggest that autofluorescence of NAD(P)H and FAD is sensitive to dynamic changes in intracellular metabolism in tissues and can be used to probe the temporal and spatial regulation of macrophage metabolism during tissue damage and repair. The function of macrophages in vitro is linked to their metabolic rewiring. However, macrophage metabolism remains poorly characterized in situ. Here, we used two-photon intensity and lifetime imaging of autofluorescent metabolic coenzymes, nicotinamide adenine dinucleotide (phosphate) (NAD(P)H) and flavin adenine dinucleotide (FAD), to assess the metabolism of macrophages in the wound microenvironment. Inhibiting glycolysis reduced NAD(P)H mean lifetime and made the intracellular redox state of macrophages more oxidized, as indicated by reduced optical redox ratio. We found that TNFα+ macrophages had lower NAD(P)H mean lifetime and were more oxidized compared to TNFα- macrophages. Both infection and thermal injury induced a macrophage population with a more oxidized redox state in wounded tissues. Kinetic analysis detected temporal changes in the optical redox ratio during tissue repair, revealing a shift toward a more reduced redox state over time. Metformin reduced TNFα+ wound macrophages, made intracellular redox state more reduced and improved tissue repair. By contrast, depletion of STAT6 increased TNFα+ wound macrophages, made redox state more oxidized and impaired regeneration. Our findings suggest that autofluorescence of NAD(P)H and FAD is sensitive to dynamic changes in intracellular metabolism in tissues and can be used to probe the temporal and spatial regulation of macrophage metabolism during tissue damage and repair. |
Author | Tweed, Kelsey E McDougal, Courtney E Huttenlocher, Anna Miskolci, Veronika Cronan, Mark R Lasarev, Michael R Walsh, Alex J Britt, Emily C Sauer, John-Demian Skala, Melissa C Zimmerman, Landon J Fan, Jing |
Author_xml | – sequence: 1 givenname: Veronika orcidid: 0000-0001-7900-4626 surname: Miskolci fullname: Miskolci, Veronika organization: Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, United States – sequence: 2 givenname: Kelsey E surname: Tweed fullname: Tweed, Kelsey E organization: Department of Biomedical Engineering, University of Wisconsin-Madison, Madison, United States – sequence: 3 givenname: Michael R orcidid: 0000-0002-1896-2705 surname: Lasarev fullname: Lasarev, Michael R organization: Department of Biostatistics & Medical Informatics, University of Wisconsin-Madison, Madison, United States – sequence: 4 givenname: Emily C surname: Britt fullname: Britt, Emily C organization: Department of Nutritional Sciences, University of Wisconsin-Madison, Madison, United States – sequence: 5 givenname: Alex J orcidid: 0000-0003-3832-8207 surname: Walsh fullname: Walsh, Alex J organization: Morgridge Institute for Research, Madison, United States – sequence: 6 givenname: Landon J surname: Zimmerman fullname: Zimmerman, Landon J organization: Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, United States – sequence: 7 givenname: Courtney E surname: McDougal fullname: McDougal, Courtney E organization: Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, United States – sequence: 8 givenname: Mark R surname: Cronan fullname: Cronan, Mark R organization: Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, United States – sequence: 9 givenname: Jing surname: Fan fullname: Fan, Jing organization: Department of Nutritional Sciences, University of Wisconsin-Madison, Madison, United States – sequence: 10 givenname: John-Demian orcidid: 0000-0001-9367-794X surname: Sauer fullname: Sauer, John-Demian organization: Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, United States – sequence: 11 givenname: Melissa C surname: Skala fullname: Skala, Melissa C organization: Department of Biomedical Engineering, University of Wisconsin-Madison, Madison, United States – sequence: 12 givenname: Anna orcidid: 0000-0001-7940-6254 surname: Huttenlocher fullname: Huttenlocher, Anna organization: Department of Pediatrics, University of Wisconsin-Madison, Madison, United States |
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Cites_doi | 10.1016/j.cell.2021.02.046 10.1016/j.it.2017.03.001 10.1038/ncomms11635 10.1038/nature06887 10.1016/j.immuni.2016.02.015 10.1038/nri.2016.70 10.1016/j.immuni.2015.02.005 10.1093/nar/28.1.235 10.1371/journal.pone.0052378 10.1016/j.devcel.2017.11.003 10.3389/fonc.2019.01144 10.1038/s41467-021-24868-1 10.1038/s41536-021-00163-x 10.1073/pnas.1424089112 10.1038/s41551-020-0592-z 10.1146/annurev-immunol-081619-104850 10.12703/P6-13 10.3389/fimmu.2019.01084 10.1038/nmeth.2019 10.1089/ars.2017.7451 10.1038/s41586-021-03199-7 10.1084/jem.20151570 10.1117/1.JBO.25.7.071203 10.1038/srep21489 10.1364/BOE.6.000559 10.1146/annurev-bioeng-071811-150108 10.1016/j.cellimm.2018.01.009 10.2174/1389450118666170613081730 10.1158/0008-5472.CAN-14-0663 10.3389/fimmu.2014.00620 10.7554/eLife.07288 10.7554/eLife.45976 10.1111/cmi.12536 10.7554/eLife.30703 10.1016/j.freeradbiomed.2016.08.010 10.1016/j.jhep.2018.11.034 10.1038/sj.onc.1209597 10.3389/fphys.2018.00419 10.1016/j.neo.2019.04.004 10.1111/imcb.12237 10.1073/pnas.89.4.1271 10.1146/annurev-physiol-022516-034339 10.1007/s12195-016-0435-x 10.1038/s41598-017-03359-8 10.3389/fbioe.2021.644648 10.3389/fonc.2020.00787 10.1371/journal.pbio.2005970 10.1038/nature11986 10.1016/S0021-9258(17)30079-0 10.1364/BOE.8.002368 10.1073/pnas.1019041108 10.1016/S0021-9258(19)70779-0 10.1038/srep25086 10.1016/j.immuni.2014.06.008 10.1038/cddis.2017.374 |
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Keywords | mouse macrophages wound healing cell biology optical redox ratio immunometabolism inflammation FLIM NAD(P)H zebrafish immunology |
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References | Yaseen (bib58) 2017; 8 Krzyszczyk (bib17) 2018; 9 Wynn (bib57) 2016; 44 Murray (bib28) 2017; 79 Berman (bib1) 2000; 28 Van den Bossche (bib51) 2017; 38 Miskolci (bib25) 2019; 8 LeBert (bib20) 2018; 7 Bojarczuk (bib3) 2016; 6 Walsh (bib54) 2014; 74 Walsh (bib55) 2015; 6 Ratnayake (bib38) 2021; 591 Sauer (bib41) 2011; 108 Gillmaier (bib10) 2012; 7 Lämmermann (bib19) 2008; 453 Walsh (bib56) 2021; 5 Marjoram (bib21) 2015; 112 Martinez (bib22) 2014; 6 Team R (bib50) 2015 Blacker (bib2) 2016; 100 Caputa (bib4) 2019; 97 Heaster (bib11) 2019; 9 Hoffmann (bib14) 2020; 10 Semba (bib44) 2016; 7 Vincent (bib53) 2016; 18 Kolenc (bib16) 2019; 30 Heaster (bib12) 2021; 9 Roh-Johnson (bib39) 2017; 43 Sinclair (bib46) 2021; 6 Nguyen-Chi (bib30) 2015; 4 Stringari (bib47) 2017; 7 O’Neill (bib33) 2016; 16 Tannahill (bib49) 2013; 496 Szulczewski (bib48) 2016; 6 Miskolci (bib26) 2022 Schuiveling (bib43) 2018; 19 Datta (bib7) 2020; 25 Georgakoudi (bib9) 2012; 14 Orecchioni (bib32) 2019; 10 Schindelin (bib42) 2012; 9 Mills (bib24) 2014; 5 O’Neill (bib34) 2016; 213 Pelicano (bib35) 2006; 25 McQuin (bib23) 2018; 16 Qian (bib36) 2021; 12 Van den Bossche (bib52) 2018; 330 Jha (bib15) 2015; 42 R Core Team (bib37) 2019 Nakashima (bib29) 1980; 255 Nguyen-Chi (bib31) 2017; 8 Lakowicz (bib18) 1992; 89 Murray (bib27) 2014; 41 Chance (bib5) 1979; 254 de Oliveira (bib8) 2019; 70 Hind (bib13) 2016; 9 Ryan (bib40) 2020; 38 Cronan (bib6) 2021; 184 Sharick (bib45) 2019; 21 |
References_xml | – volume: 184 start-page: 1757 year: 2021 ident: bib6 article-title: A non-canonical type 2 immune response coordinates tuberculous granuloma formation and epithelialization publication-title: Cell doi: 10.1016/j.cell.2021.02.046 contributor: fullname: Cronan – volume: 38 start-page: 395 year: 2017 ident: bib51 article-title: Macrophage Immunometabolism: Where Are We (Going)? publication-title: Trends in Immunology doi: 10.1016/j.it.2017.03.001 contributor: fullname: Van den Bossche – volume: 7 year: 2016 ident: bib44 article-title: HIF-1α-PDK1 axis-induced active glycolysis plays an essential role in macrophage migratory capacity publication-title: Nature Communications doi: 10.1038/ncomms11635 contributor: fullname: Semba – volume: 453 start-page: 51 year: 2008 ident: bib19 article-title: Rapid leukocyte migration by integrin-independent flowing and squeezing publication-title: Nature doi: 10.1038/nature06887 contributor: fullname: Lämmermann – volume: 44 start-page: 450 year: 2016 ident: bib57 article-title: Macrophages in Tissue Repair, Regeneration, and Fibrosis publication-title: Immunity doi: 10.1016/j.immuni.2016.02.015 contributor: fullname: Wynn – volume: 16 start-page: 553 year: 2016 ident: bib33 article-title: A guide to immunometabolism for immunologists publication-title: Nature Reviews. Immunology doi: 10.1038/nri.2016.70 contributor: fullname: O’Neill – volume: 42 start-page: 419 year: 2015 ident: bib15 article-title: Network integration of parallel metabolic and transcriptional data reveals metabolic modules that regulate macrophage polarization publication-title: Immunity doi: 10.1016/j.immuni.2015.02.005 contributor: fullname: Jha – volume: 28 start-page: 235 year: 2000 ident: bib1 article-title: The Protein Data Bank publication-title: Nucleic Acids Research doi: 10.1093/nar/28.1.235 contributor: fullname: Berman – volume: 7 year: 2012 ident: bib10 article-title: Metabolic responses of primary and transformed cells to intracellular Listeria monocytogenes publication-title: PLOS ONE doi: 10.1371/journal.pone.0052378 contributor: fullname: Gillmaier – volume: 43 start-page: 549 year: 2017 ident: bib39 article-title: Macrophage-Dependent Cytoplasmic Transfer during Melanoma Invasion In Vivo publication-title: Developmental Cell doi: 10.1016/j.devcel.2017.11.003 contributor: fullname: Roh-Johnson – volume: 9 year: 2019 ident: bib11 article-title: Quantitative Spatial Analysis of Metabolic Heterogeneity Across in vivo and in vitro Tumor Models publication-title: Frontiers in Oncology doi: 10.3389/fonc.2019.01144 contributor: fullname: Heaster – volume: 12 year: 2021 ident: bib36 article-title: Label-free imaging for quality control of cardiomyocyte differentiation publication-title: Nature Communications doi: 10.1038/s41467-021-24868-1 contributor: fullname: Qian – volume: 6 year: 2021 ident: bib46 article-title: The Warburg effect is necessary to promote glycosylation in the blastema during zebrafish tail regeneration publication-title: NPJ Regenerative Medicine doi: 10.1038/s41536-021-00163-x contributor: fullname: Sinclair – volume: 112 start-page: 2770 year: 2015 ident: bib21 article-title: Epigenetic control of intestinal barrier function and inflammation in zebrafish publication-title: PNAS doi: 10.1073/pnas.1424089112 contributor: fullname: Marjoram – volume: 5 start-page: 77 year: 2021 ident: bib56 article-title: Classification of T-cell activation via autofluorescence lifetime imaging publication-title: Nature Biomedical Engineering doi: 10.1038/s41551-020-0592-z contributor: fullname: Walsh – volume: 38 start-page: 289 year: 2020 ident: bib40 article-title: Krebs Cycle Reborn in Macrophage Immunometabolism publication-title: Annual Review of Immunology doi: 10.1146/annurev-immunol-081619-104850 contributor: fullname: Ryan – volume: 6 year: 2014 ident: bib22 article-title: The M1 and M2 paradigm of macrophage activation: time for reassessment publication-title: F1000prime Reports doi: 10.12703/P6-13 contributor: fullname: Martinez – volume: 10 year: 2019 ident: bib32 article-title: Macrophage Polarization: Different Gene Signatures in M1(LPS+) vs. Classically and M2(LPS-) vs. Alternatively Activated Macrophages publication-title: Frontiers in Immunology doi: 10.3389/fimmu.2019.01084 contributor: fullname: Orecchioni – volume: 9 start-page: 676 year: 2012 ident: bib42 article-title: Fiji: an open-source platform for biological-image analysis publication-title: Nature Methods doi: 10.1038/nmeth.2019 contributor: fullname: Schindelin – volume: 30 start-page: 875 year: 2019 ident: bib16 article-title: Evaluating Cell Metabolism Through Autofluorescence Imaging of NAD(P)H and FAD publication-title: Antioxidants & Redox Signaling doi: 10.1089/ars.2017.7451 contributor: fullname: Kolenc – volume: 591 start-page: 281 year: 2021 ident: bib38 article-title: Macrophages provide a transient muscle stem cell niche via NAMPT secretion publication-title: Nature doi: 10.1038/s41586-021-03199-7 contributor: fullname: Ratnayake – volume: 213 start-page: 15 year: 2016 ident: bib34 article-title: Immunometabolism governs dendritic cell and macrophage function publication-title: The Journal of Experimental Medicine doi: 10.1084/jem.20151570 contributor: fullname: O’Neill – volume: 25 start-page: 1 year: 2020 ident: bib7 article-title: Fluorescence lifetime imaging microscopy: fundamentals and advances in instrumentation, analysis, and applications publication-title: Journal of Biomedical Optics doi: 10.1117/1.JBO.25.7.071203 contributor: fullname: Datta – volume: 6 year: 2016 ident: bib3 article-title: Cryptococcus neoformans Intracellular Proliferation and Capsule Size Determines Early Macrophage Control of Infection publication-title: Scientific Reports doi: 10.1038/srep21489 contributor: fullname: Bojarczuk – volume: 6 start-page: 559 year: 2015 ident: bib55 article-title: Optical metabolic imaging quantifies heterogeneous cell populations publication-title: Biomedical Optics Express doi: 10.1364/BOE.6.000559 contributor: fullname: Walsh – volume: 14 start-page: 351 year: 2012 ident: bib9 article-title: Optical imaging using endogenous contrast to assess metabolic state publication-title: Annual Review of Biomedical Engineering doi: 10.1146/annurev-bioeng-071811-150108 contributor: fullname: Georgakoudi – volume: 330 start-page: 54 year: 2018 ident: bib52 article-title: Metabolic regulation of macrophages in tissues publication-title: Cellular Immunology doi: 10.1016/j.cellimm.2018.01.009 contributor: fullname: Van den Bossche – volume: 19 start-page: 945 year: 2018 ident: bib43 article-title: Metformin, A New Era for an Old Drug in the Treatment of Immune Mediated Disease? publication-title: Current Drug Targets doi: 10.2174/1389450118666170613081730 contributor: fullname: Schuiveling – volume: 74 start-page: 5184 year: 2014 ident: bib54 article-title: Quantitative optical imaging of primary tumor organoid metabolism predicts drug response in breast cancer publication-title: Cancer Research doi: 10.1158/0008-5472.CAN-14-0663 contributor: fullname: Walsh – volume: 5 year: 2014 ident: bib24 article-title: Macrophage: SHIP of Immunity publication-title: Frontiers in Immunology doi: 10.3389/fimmu.2014.00620 contributor: fullname: Mills – volume: 4 year: 2015 ident: bib30 article-title: Identification of polarized macrophage subsets in zebrafish publication-title: eLife doi: 10.7554/eLife.07288 contributor: fullname: Nguyen-Chi – volume: 8 year: 2019 ident: bib25 article-title: Distinct inflammatory and wound healing responses to complex caudal fin injuries of larval zebrafish publication-title: eLife doi: 10.7554/eLife.45976 contributor: fullname: Miskolci – volume: 18 start-page: 591 year: 2016 ident: bib53 article-title: Macrophages mediate flagellin induced inflammasome activation and host defense in zebrafish publication-title: Cellular Microbiology doi: 10.1111/cmi.12536 contributor: fullname: Vincent – volume: 7 year: 2018 ident: bib20 article-title: Damage-induced reactive oxygen species regulate vimentin and dynamic collagen-based projections to mediate wound repair publication-title: eLife doi: 10.7554/eLife.30703 contributor: fullname: LeBert – volume: 100 start-page: 53 year: 2016 ident: bib2 article-title: Investigating mitochondrial redox state using NADH and NADPH autofluorescence publication-title: Free Radical Biology & Medicine doi: 10.1016/j.freeradbiomed.2016.08.010 contributor: fullname: Blacker – volume: 70 start-page: 710 year: 2019 ident: bib8 article-title: Metformin modulates innate immune-mediated inflammation and early progression of NAFLD-associated hepatocellular carcinoma in zebrafish publication-title: Journal of Hepatology doi: 10.1016/j.jhep.2018.11.034 contributor: fullname: de Oliveira – volume: 25 start-page: 4633 year: 2006 ident: bib35 article-title: Glycolysis inhibition for anticancer treatment publication-title: Oncogene doi: 10.1038/sj.onc.1209597 contributor: fullname: Pelicano – volume: 9 year: 2018 ident: bib17 article-title: The Role of Macrophages in Acute and Chronic Wound Healing and Interventions to Promote Pro-wound Healing Phenotypes publication-title: Frontiers in Physiology doi: 10.3389/fphys.2018.00419 contributor: fullname: Krzyszczyk – volume: 21 start-page: 615 year: 2019 ident: bib45 article-title: Cellular Metabolic Heterogeneity In Vivo Is Recapitulated in Tumor Organoids publication-title: Neoplasia (New York, N.Y.) doi: 10.1016/j.neo.2019.04.004 contributor: fullname: Sharick – volume: 97 start-page: 268 year: 2019 ident: bib4 article-title: Macrophage metabolism: a wound-healing perspective publication-title: Immunology and Cell Biology doi: 10.1111/imcb.12237 contributor: fullname: Caputa – volume: 89 start-page: 1271 year: 1992 ident: bib18 article-title: Fluorescence lifetime imaging of free and protein-bound NADH publication-title: PNAS doi: 10.1073/pnas.89.4.1271 contributor: fullname: Lakowicz – volume: 79 start-page: 541 year: 2017 ident: bib28 article-title: Macrophage Polarization publication-title: Annual Review of Physiology doi: 10.1146/annurev-physiol-022516-034339 contributor: fullname: Murray – volume: 9 start-page: 455 year: 2016 ident: bib13 article-title: Effect of M1-M2 Polarization on the Motility and Traction Stresses of Primary Human Macrophages publication-title: Cellular and Molecular Bioengineering doi: 10.1007/s12195-016-0435-x contributor: fullname: Hind – volume: 7 year: 2017 ident: bib47 article-title: Multicolor two-photon imaging of endogenous fluorophores in living tissues by wavelength mixing publication-title: Scientific Reports doi: 10.1038/s41598-017-03359-8 contributor: fullname: Stringari – volume: 9 year: 2021 ident: bib12 article-title: Intravital Metabolic Autofluorescence Imaging Captures Macrophage Heterogeneity Across Normal and Cancerous Tissue publication-title: Frontiers in Bioengineering and Biotechnology doi: 10.3389/fbioe.2021.644648 contributor: fullname: Heaster – volume: 10 year: 2020 ident: bib14 article-title: Biomechanical Contributions to Macrophage Activation in the Tumor Microenvironment publication-title: Frontiers in Oncology doi: 10.3389/fonc.2020.00787 contributor: fullname: Hoffmann – volume-title: Github year: 2022 ident: bib26 article-title: In vivo fluorescence lifetime imaging of macrophage intracellular metabolism during wound responses in zebrafish contributor: fullname: Miskolci – volume: 16 year: 2018 ident: bib23 article-title: CellProfiler 3.0: Next-generation image processing for biology publication-title: PLOS Biology doi: 10.1371/journal.pbio.2005970 contributor: fullname: McQuin – year: 2019 ident: bib37 article-title: R: A langauge and environment for statistical computing contributor: fullname: R Core Team – volume: 496 start-page: 238 year: 2013 ident: bib49 article-title: Succinate is an inflammatory signal that induces IL-1β through HIF-1α publication-title: Nature doi: 10.1038/nature11986 contributor: fullname: Tannahill – volume-title: RStudio, Inc year: 2015 ident: bib50 article-title: RStudio: Integrated Development for R contributor: fullname: Team R – volume: 254 start-page: 4764 year: 1979 ident: bib5 article-title: Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples publication-title: NADH and Flavoprotein Fluorescence Signals. J Biol Chem doi: 10.1016/S0021-9258(17)30079-0 contributor: fullname: Chance – volume: 8 start-page: 2368 year: 2017 ident: bib58 article-title: Fluorescence lifetime microscopy of NADH distinguishes alterations in cerebral metabolism in vivo publication-title: Biomedical Optics Express doi: 10.1364/BOE.8.002368 contributor: fullname: Yaseen – volume: 108 start-page: 12419 year: 2011 ident: bib41 article-title: Listeria monocytogenes engineered to activate the Nlrc4 inflammasome are severely attenuated and are poor inducers of protective immunity publication-title: PNAS doi: 10.1073/pnas.1019041108 contributor: fullname: Sauer – volume: 255 start-page: 5261 year: 1980 ident: bib29 article-title: Picosecond fluorescence lifetime of the coenzyme of D-amino acid oxidase publication-title: The Journal of Biological Chemistry doi: 10.1016/S0021-9258(19)70779-0 contributor: fullname: Nakashima – volume: 6 year: 2016 ident: bib48 article-title: In Vivo Visualization of Stromal Macrophages via label-free FLIM-based metabolite imaging publication-title: Scientific Reports doi: 10.1038/srep25086 contributor: fullname: Szulczewski – volume: 41 start-page: 14 year: 2014 ident: bib27 article-title: Macrophage activation and polarization: nomenclature and experimental guidelines publication-title: Immunity doi: 10.1016/j.immuni.2014.06.008 contributor: fullname: Murray – volume: 8 year: 2017 ident: bib31 article-title: TNF signaling and macrophages govern fin regeneration in zebrafish larvae publication-title: Cell Death & Disease doi: 10.1038/cddis.2017.374 contributor: fullname: Nguyen-Chi |
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SubjectTerms | Adenine Animals Cell Biology Coenzymes Female Flavin Flavin-adenine dinucleotide Flavin-Adenine Dinucleotide - metabolism FLIM Fluorescence Glucose Glycolysis Immunology and Inflammation immunometabolism Intracellular Kinetics Lifetime Macrophages Macrophages - metabolism Metabolism Metformin Mice Mice, Inbred C57BL Microenvironments Microscopy, Fluorescence, Multiphoton - methods NAD(P)H NADP - metabolism NADPH optical redox ratio Oxidation-Reduction Phosphorylation Proteins Redox properties Stat6 protein Thermal injury Tumor Necrosis Factor-alpha - metabolism Tumor necrosis factor-α Wound healing Wounds Wounds and Injuries - metabolism Zebrafish - metabolism |
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Title | In vivo fluorescence lifetime imaging of macrophage intracellular metabolism during wound responses in zebrafish |
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