In Vivo Assessment of Cold Adaptation in Insect Larvae by Magnetic Resonance Imaging and Magnetic Resonance Spectroscopy
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{"title"=>"In vivo assessment of cold adaption in insect larvae by magnetic resonace imaging and magnetic resonance spectroscopy", "type"=>"journal", "authors"=>[{"first_name"=>"Daniel", "last_name"=>"Mietchen", "scopus_author_id"=>"7801384320"}, {"first_name"=>"Bertram", "last_name"=>"Manz", "scopus_author_id"=>"7004317805"}, {"first_name"=>"Frank", "last_name"=>"Volke", "scopus_author_id"=>"6603355970"}, {"first_name"=>"Kenneth", "last_name"=>"Storey", "scopus_author_id"=>"35598663900"}], "year"=>2008, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"57549083604", "doi"=>"10.1371/journal.pone.0003826", "pui"=>"352816318", "scopus"=>"2-s2.0-57549083604", "issn"=>"19326203"}, "id"=>"380adb5e-f6ca-3f50-be48-ca19d930af0f", "abstract"=>"Background: Temperatures below the freezing point of water and the ensuing ice crystal formation pose serious challenges to cell structure and function. Consequently, species living in seasonally cold environments have evolved a multitude of strategies to reorganize their cellular architecture and metabolism, and the underlying mechanisms are crucial to our understanding of life. In multicellular organisms, and poikilotherm animals in particular, our knowledge about these processes is almost exclusively due to invasive studies, thereby limiting the range of conclusions that can be drawn about intact living systems. Methodology: Given that non-destructive techniques like 1H Magnetic Resonance (MR) imaging and spectroscopy have proven useful for in vivo investigations of a wide range of biological systems, we aimed at evaluating their potential to observe cold adaptations in living insect larvae. Specifically, we chose two cold-hardy insect species that frequently serve as cryobiological model systems-the freeze-avoiding gall moth Epiblema scudderiana and the freeze-tolerant gall fly Eurosta solidaginis. Results: In vivo MR images were acquired from autumn-collected larvae at temperatures between 0°C and about -70°C and at spatial resolutions down to 27 μm. These images revealed three-dimensional (3D) larval anatomy at a level of detail currently not in reach of other in vivo techniques. Furthermore, they allowed visualization of the 3D distribution of the remaining liquid water and of the endogenous cryoprotectants at subzero temperatures, and temperature-weighted images of these distributions could be derived. Finally, individual fat body cells and their nuclei could be identified in intact frozen Eurosta larvae. Conclusions: These findings suggest that high resolution MR techniques provide for interesting methodological options in comparative cryobiological investigations, especially in vivo. © 2008 Mietchen et al.", "link"=>"http://www.mendeley.com/research/vivo-assessment-cold-adaption-insect-larvae-magnetic-resonace-imaging-magnetic-resonance-spectroscop", "reader_count"=>7, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Researcher"=>2, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>1, "Student > Master"=>1, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Researcher"=>2, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>1, "Student > Master"=>1, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>5}, "reader_count_by_subdiscipline"=>{"Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>5}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>1}}, "group_count"=>0}

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  • {"files"=>["https://ndownloader.figshare.com/files/452291", "https://ndownloader.figshare.com/files/452312", "https://ndownloader.figshare.com/files/452321", "https://ndownloader.figshare.com/files/452330", "https://ndownloader.figshare.com/files/452338", "https://ndownloader.figshare.com/files/452344", "https://ndownloader.figshare.com/files/452352", "https://ndownloader.figshare.com/files/452361", "https://ndownloader.figshare.com/files/452369"], "description"=>"<div><h3>Background</h3><p>Temperatures below the freezing point of water and the ensuing ice crystal formation pose serious challenges to cell structure and function. Consequently, species living in seasonally cold environments have evolved a multitude of strategies to reorganize their cellular architecture and metabolism, and the underlying mechanisms are crucial to our understanding of life. In multicellular organisms, and poikilotherm animals in particular, our knowledge about these processes is almost exclusively due to invasive studies, thereby limiting the range of conclusions that can be drawn about intact living systems.</p><h3>Methodology</h3><p>Given that non-destructive techniques like <sup>1</sup>H Magnetic Resonance (MR) imaging and spectroscopy have proven useful for <em>in vivo</em> investigations of a wide range of biological systems, we aimed at evaluating their potential to observe cold adaptations in living insect larvae. Specifically, we chose two cold-hardy insect species that frequently serve as cryobiological model systems–the freeze-avoiding gall moth <em>Epiblema scudderiana</em> and the freeze-tolerant gall fly <em>Eurosta solidaginis</em>.</p><h3>Results</h3><p><em>In vivo</em> MR images were acquired from autumn-collected larvae at temperatures between 0°C and about −70°C and at spatial resolutions down to 27 µm. These images revealed three-dimensional (3D) larval anatomy at a level of detail currently not in reach of other <em>in vivo</em> techniques. Furthermore, they allowed visualization of the 3D distribution of the remaining liquid water and of the endogenous cryoprotectants at subzero temperatures, and temperature-weighted images of these distributions could be derived. Finally, individual fat body cells and their nuclei could be identified in intact frozen <em>Eurosta</em> larvae.</p><h3>Conclusions</h3><p>These findings suggest that high resolution MR techniques provide for interesting methodological options in comparative cryobiological investigations, especially <em>in vivo</em>.</p></div>", "links"=>[], "tags"=>["adaptation", "larvae", "resonance", "imaging", "spectroscopy"], "article_id"=>149088, "categories"=>["Physics", "Cell Biology", "Developmental Biology", "Biophysics", "Biochemistry", "Evolutionary Biology", "Biotechnology", "Medicine", "Ecology"], "users"=>["Daniel Mietchen", "Bertram Manz", "Frank Volke", "Kenneth Storey"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0003826.s001", "https://dx.doi.org/10.1371/journal.pone.0003826.s002", "https://dx.doi.org/10.1371/journal.pone.0003826.s003", "https://dx.doi.org/10.1371/journal.pone.0003826.s004", "https://dx.doi.org/10.1371/journal.pone.0003826.s005", "https://dx.doi.org/10.1371/journal.pone.0003826.s006", "https://dx.doi.org/10.1371/journal.pone.0003826.s007", "https://dx.doi.org/10.1371/journal.pone.0003826.s008", "https://dx.doi.org/10.1371/journal.pone.0003826.s009"], "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_In_Vivo_Assessment_of_Cold_Adaptation_in_Insect_Larvae_by_Magnetic_Resonance_Imaging_and_Magnetic_Resonance_Spectroscopy/149088", "title"=>"<em>In Vivo</em> Assessment of Cold Adaptation in Insect Larvae by Magnetic Resonance Imaging and Magnetic Resonance Spectroscopy", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2008-12-05 02:31:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/913960"], "description"=>"<p>Relative signal intensity (from black = low to white = high; identical for all MR images in this paper, even though absolute intensities vary considerably) is given in arbitrary units but on scale across temperatures. Image resolution: 47 µm (isotropic). The images were rotated by 90° for better presentation–positioning of the larva was with head up (right), tail down (now left). The spectra are the same as in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone-0003826-g002\" target=\"_blank\">Fig. 2A</a> and repeated here to facilitate interpretation of the images. Note the image blurring at 0°C and −20°C, hinting at head and tail motion of the larva. The complete slice series of these four 3D images are given as <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone.0003826.s001\" target=\"_blank\">Movie S1</a>. This video also shows the signal contributions from the <i>Solidago twig</i>, which exhibit a different temperature dependence than the signal from the larva.</p>", "links"=>[], "tags"=>["nmr", "images", "corresponding", "spectra", "larva"], "article_id"=>584411, "categories"=>["Physics", "Cell Biology", "Developmental Biology", "Biophysics", "Biochemistry", "Evolutionary Biology", "Biotechnology", "Medicine", "Ecology"], "users"=>["Daniel Mietchen", "Bertram Manz", "Frank Volke", "Kenneth Storey"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003826.g003", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Correspondence_between_NMR_images_and_spectra_1_H_NMR_images_and_corresponding_NMR_spectra_of_an_Epiblema_larva_at_different_temperatures_/584411", "title"=>"Correspondence between NMR images and spectra: <sup>1</sup>H NMR images and corresponding NMR spectra of an <i>Epiblema</i> larva at different temperatures.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-12-05 01:13:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/914213"], "description"=>"<p>An animation of this temperature-coded composite 3D model is supplied as the supplementary video file <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone.0003826.s009\" target=\"_blank\">Movie S9</a>.</p>", "links"=>[], "tags"=>["3d", "nmr", "whole-spectrum", "images"], "article_id"=>584666, "categories"=>["Physics", "Cell Biology", "Developmental Biology", "Biophysics", "Biochemistry", "Evolutionary Biology", "Biotechnology", "Medicine", "Ecology"], "users"=>["Daniel Mietchen", "Bertram Manz", "Frank Volke", "Kenneth Storey"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003826.g006", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Temperature_weighted_imaging_3D_model_of_an_Epiblema_larva_based_on_1_H_NMR_whole_spectrum_images_cf_Fig_4_obtained_at_8722_35_176_C_brown_and_8722_70_176_C_red_/584666", "title"=>"Temperature-weighted imaging: 3D model of an <i>Epiblema</i> larva, based on <sup>1</sup>H NMR whole-spectrum images (cf. Fig. 4) obtained at −35°C (brown) and −70°C (red).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-12-05 01:17:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/913877"], "description"=>"<p>A: <i>Epiblema</i>, B: <i>Eurosta</i>. The broad peak referenced to 4.7 ppm represents hydroxyl groups (in water, glycerol and sorbitol), whereas hydrocarbon groups from glycerol and sorbitol are located around 3.6 ppm, and otherhydrocarbon groups, e.g. from lipids, around 1–2 ppm. Note that glycerol is present in both species, sorbitol only in <i>Eurosta</i>. For acquisition parameters in the images presented in this paper, see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#s2\" target=\"_blank\">Methods</a> section. C: Freezing trajectory, as extracted from the spectra above by integrating over the whole spectrum (<i>Epiblema</i>, black squares) or individual peaks (<i>Eurosta</i>, circles with upright cross for OH peak, circles with oblique cross for CH<sub>x</sub> peak, red circles for whole spectrum) at the given temperature. Signal intensity in each species was normalized to the respective value measured at −20°C. Note that the CH<sub>x</sub> peak integral does not change with temperature, while the OH peak integral does, thereby being responsible for the changes seen in the whole-spectrum trajectory in <i>Eurosta</i>. Most (if not all) of the signal loss observed in the <i>Epiblema</i> trajectory are presumably also due to the freezing of water but these contributions could not be reliably separated, since the peaks overlap in the spectrum (cf. A).</p>", "links"=>[], "tags"=>["nmr", "spectra", "larvae", "temperatures", "arbitrary", "units"], "article_id"=>584327, "categories"=>["Physics", "Cell Biology", "Developmental Biology", "Biophysics", "Biochemistry", "Evolutionary Biology", "Biotechnology", "Medicine", "Ecology"], "users"=>["Daniel Mietchen", "Bertram Manz", "Frank Volke", "Kenneth Storey"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003826.g002", "stats"=>{"downloads"=>2, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_1_H_NMR_spectra_of_insect_larvae_at_different_temperatures_intensity_in_arbitrary_units_but_on_scale_across_temperatures_/584327", "title"=>"<sup>1</sup>H NMR spectra of insect larvae at different temperatures (intensity in arbitrary units but on scale across temperatures).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-12-05 01:12:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/913811"], "description"=>"<p>(A) Photograph of an <i>Epiblema scudderiana</i> larva (head is right) in its gall, taken after the experiment. The gall was left intact throughout the experiments and only cut open afterwards to confirm the position during the NMR experiments. Normal position both in nature and in the magnet is upright. (B) Photograph of an <i>Eurosta solidaginis</i> gall before the start of the experiment. The insect was removed from the gall for the sake of increased spatial resolution. (C) Photograph taken after the experiment, indicating the positioning on the horizontal microwell plate. Note the yellowish appearance due to glycerol. All scale bars in this figure represent 5 mm.</p>", "links"=>[], "tags"=>["larvae"], "article_id"=>584267, "categories"=>["Physics", "Cell Biology", "Developmental Biology", "Biophysics", "Biochemistry", "Evolutionary Biology", "Biotechnology", "Medicine", "Ecology"], "users"=>["Daniel Mietchen", "Bertram Manz", "Frank Volke", "Kenneth Storey"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003826.g001", "stats"=>{"downloads"=>3, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Galls_and_larvae_used_in_this_experiment_/584267", "title"=>"Galls and larvae used in this experiment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-12-05 01:11:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/914098"], "description"=>"<p>The water-based 3D model is depicted in semi-transparent brown and the model based on the fat signal in red. An animation of this chemical shift-coded composite 3D model is supplied as the supplementary video file <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone.0003826.s008\" target=\"_blank\">Movie S8</a>.</p>", "links"=>[], "tags"=>["3d", "nmr", "images"], "article_id"=>584554, "categories"=>["Physics", "Cell Biology", "Developmental Biology", "Biophysics", "Biochemistry", "Evolutionary Biology", "Biotechnology", "Medicine", "Ecology"], "users"=>["Daniel Mietchen", "Bertram Manz", "Frank Volke", "Kenneth Storey"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003826.g005", "stats"=>{"downloads"=>1, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Three_dimensional_modeling_3D_model_of_a_Eurosta_larva_based_on_1_H_NMR_water_and_fat_images_cf_Fig_3_obtained_at_8722_20_176_C_/584554", "title"=>"Three-dimensional modeling: 3D model of a <i>Eurosta</i> larva, based on <sup>1</sup>H NMR water and fat images (cf. Fig. 3) obtained at −20°C.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-12-05 01:15:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/914024"], "description"=>"<p>All images have been rotated by 90°for ease of display (direction of gravity was from right to left). The images labeled “All” were acquired by using the whole spectrum (at a resolution of 27 µm), whereas the “Water” and “Fat” images only represent contributions from the hydroxyl peak at 4.7 ppm and the hydrocarbon peak at around 1 ppm, respectively (acquired at a resolution of 27 µm at −20°C and of 110 µm at −40°C; the latter were zero-filled to facilitate comparison across temperatures). The overall signal intensity of the water and fat images at a given temperature do not add up to the intensity of the whole-spectrum image because the CHESS sequences required longer echo times (for details, see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#s2\" target=\"_blank\">methods</a> section). The spectra are repeated from <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone-0003826-g002\" target=\"_blank\">Fig. 2B</a> to facilitate interpretation of the images. Note the single cells visible (with their nuclei) in all three images at −20°C and particularly in the whole-spectrum image at −40°C. Shape distortions with respect to normal anatomy of <i>Eurosta</i> larvae are due to the positioning on the cryowells, as indicated in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone-0003826-g001\" target=\"_blank\">Fig. 1C</a>, while seemingly morphological differences between the images also reflect the rescaling of the images, or movements of the animal. The complete slice series of these six 3D images are presented separately by temperature (−20°C or −40°C) and spectral coverage (All/Water/Fat) in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone.0003826.s002\" target=\"_blank\">Movies S2</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone.0003826.s003\" target=\"_blank\">S3</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone.0003826.s004\" target=\"_blank\">S4</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone.0003826.s005\" target=\"_blank\">S5</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone.0003826.s006\" target=\"_blank\">S6</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone.0003826.s007\" target=\"_blank\">S7</a>: At −20°C, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone.0003826.s002\" target=\"_blank\">Movie S2</a> covers the whole spectrum and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone.0003826.s003\" target=\"_blank\">Movie S3</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone.0003826.s004\" target=\"_blank\">Movie S4</a> the water and fat image, respectively. At −40°C, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone.0003826.s005\" target=\"_blank\">Movie S5</a> covers the whole spectrum and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone.0003826.s006\" target=\"_blank\">Movie S6</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone.0003826.s007\" target=\"_blank\">Movie S7</a> the water and hydrocarbon images, respectively. Image orientation in the movies reflects the horizontal positioning of the larva during the experiment (cf. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003826#pone-0003826-g001\" target=\"_blank\">Fig. 1C</a>).</p>", "links"=>[], "tags"=>["three-dimensional", "cryoprotectant", "nmr", "images", "corresponding", "spectra", "larva", "temperatures", "arbitrary", "units"], "article_id"=>584467, "categories"=>["Physics", "Cell Biology", "Developmental Biology", "Biophysics", "Biochemistry", "Evolutionary Biology", "Biotechnology", "Medicine", "Ecology"], "users"=>["Daniel Mietchen", "Bertram Manz", "Frank Volke", "Kenneth Storey"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003826.g004", "stats"=>{"downloads"=>3, "page_views"=>31, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Imaging_the_three_dimensional_distribution_of_water_and_cryoprotectant_in_a_living_frozen_organism_1_H_NMR_images_and_corresponding_NMR_spectra_of_an_Eurosta_larva_at_different_temperatures_intensity_in_arbitrary_units_but_on_scale_across_temperatures_/584467", "title"=>"Imaging the three-dimensional distribution of water and cryoprotectant in a living frozen organism: <sup>1</sup>H NMR images and corresponding NMR spectra of an <i>Eurosta</i> larva at different temperatures (intensity in arbitrary units but on scale across temperatures).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-12-05 01:14:27"}

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Relative Metric

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