Jens R Nyengaard

Aarhus University, Aarhus, Central Jutland, Denmark

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Publications (179)679.1 Total impact

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    ABSTRACT: Balancing trophic and apoptotic cues is critical for development and regeneration of neuronal circuits. Here we identify SorCS2 as a proneurotrophin (proNT) receptor, mediating both trophic and apoptotic signals in conjunction with p75(NTR). CNS neurons, but not glia, express SorCS2 as a single-chain protein that is essential for proBDNF-induced growth cone collapse in developing dopaminergic processes. SorCS2- or p75(NTR)-deficient in mice caused reduced dopamine levels and metabolism and dopaminergic hyperinnervation of the frontal cortex. Accordingly, both knockout models displayed a paradoxical behavioral response to amphetamine reminiscent of ADHD. Contrary, in PNS glia, but not in neurons, proteolytic processing produced a two-chain SorCS2 isoform that mediated proNT-dependent Schwann cell apoptosis. Sciatic nerve injury triggered generation of two-chain SorCS2 in p75(NTR)-positive dying Schwann cells, with apoptosis being profoundly attenuated in Sorcs2(-/-) mice. In conclusion, we have demonstrated that two-chain processing of SorCS2 enables neurons and glia to respond differently to proneurotrophins.
    Neuron 06/2014; 82(5):1074-1087. · 15.77 Impact Factor
  • Molecular psychiatry 04/2014; 19(4):401. · 15.05 Impact Factor
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    ABSTRACT: The aim of this study was to establish quantitative diagnostic criteria for lymphocytic myocarditis on autopsy samples by using a stereological cell profile counting method. We quantified and compared the presence of lymphocytes and macrophages in myocardial autopsy specimens from 112 deceased individuals who had been diagnosed with myocarditis according to the Dallas criteria and 86 control subjects with morphologically normal hearts. We found the mean number to be 52.7lymphocyte profiles/mm(2) (range 3.7-946; standard deviation 131) in the myocarditis group and 9.7 (range 2.1-25.9; standard deviation 4.6) in the control group. The cut-off value for the diagnosis of myocarditis was determined by calculating sensitivity plus specificity, which reached the highest combination at 13lymphocyte profiles/mm(2) (sensitivity 68%; specificity 83%). A considerable proportion of subjects in both the myocarditis and control groups had lymphocyte profile counts below 30/mm(2), representing a diagnostic challenge due to the increased risk of creating false negative or false positive results. We found it practically impossible to obtain a reliable macrophage count. The present data add new important information on lymphocyte counts in inflamed and non-inflamed myocardium. We suggest a cut-off value in the range of 11-16lymphocyte profiles/mm(2) for a reliable diagnosis of lymphocytic myocarditis from autopsy samples. To evaluate small inflammatory changes at low lymphocyte counts, a multidisciplinary approach should be implemented, in which diagnostic tools are used ancillary to histological examination. We advise against semi-quantification of macrophages based on cell profile counting.
    Forensic science international 02/2014; 238C:9-15. · 2.10 Impact Factor
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    ABSTRACT: Stress and glucocorticoids alter glutamatergic transmission, and the outcome of stress may range from plasticity enhancing effects to noxious, maladaptive changes. We have previously demonstrated that acute stress rapidly increases glutamate release in prefrontal and frontal cortex via glucocorticoid receptor and accumulation of presynaptic SNARE complex. Here we compared the ex vivo effects of acute stress on glutamate release with those of in vitro application of corticosterone, to analyze whether acute effect of stress on glutamatergic transmission is mediated by local synaptic action of corticosterone. We found that acute stress increases both the readily releasable pool (RRP) of vesicles and depolarization-evoked glutamate release, while application in vitro of corticosterone rapidly increases the RRP, an effect dependent on synaptic receptors for the hormone, but does not induce glutamate release for up to 20 min. These findings indicate that corticosterone mediates the enhancement of glutamate release induced by acute stress, and the rapid non-genomic action of the hormone is necessary but not sufficient for this effect.Molecular Psychiatry advance online publication, 18 February 2014; doi:10.1038/mp.2014.5.
    Molecular psychiatry 02/2014; · 15.05 Impact Factor
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    ABSTRACT: Introduction. The renin granulation of kidney arterioles is enhanced in diabetes despite the fact that the level of angiotensin II in the diabetic kidney is elevated. Therefore, the number of angiotensin II AT1-A and AT1-B receptors in afferent and efferent arteriole's renin-positive and renin-negative smooth muscle cells (SMC) was estimated. Method. Immunohistochemistry at the electron microscopic level was combined with 3D stereological sampling techniques. Results. In diabetes the enhanced downregulation of AT1-B receptors in the renin-positive than in the renin-negative SMCs in both arterioles was resulted: the significant difference in the number of AT1 (AT1-A + AT1-B) receptors between the two types of SMCs in the normal rats was further increased in diabetes and in contrast with the significant difference observed between the afferent and efferent arterioles in the normal animals, there was no such difference in diabetes. Conclusions. The enhanced downregulation of the AT1-B receptors in the renin-negative SMCs in the efferent arterioles demonstrates that the regulation of the glomerular filtration rate by the pre- and postglomerular arterioles is changed in diabetes. The enhanced downregulation of the AT1-B receptors in the renin-positive SMCs in the arterioles may result in an enhanced level of renin granulation in the arterioles.
    BioMed research international. 01/2014; 2014:947506.
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    ABSTRACT: There may be regional specialisation in structure and function across the placental surface. In Riyadh, Saudi Arabia, the length and the breadth of the placental surface at birth were highly correlated, but the breadth was more closely associated with the size of the baby. To replicate this we studied 321 pregnant Saudi women in the town of Baish. We measured the size of the newborn babies and their placentas. The association of the length and breadth of the placental surface on the baby’s body size differed in boys and girls. Among boys the breadth had a stronger association with all birth measurements except crown-heel length. This was similar to the findings in Riyadh. Placental surface length was related to crown-heel length. For each centimetre in surface length, crown-heel length increased by 0.27 cm (95% CI 0.09 to 0.44, p=0.004). Among girls placental surface breadth was related to crown-heel length, whereas surface length was related to birth weight, head and thigh circumferences. For each centimetre in surface breadth, crown-heel length increased by 0.33 cm (0.13 to 0.53, p=0.001). We conclude that, within Saudi Arabia, there are both geographical and sex differences in regional specialisation across the placental surface. In the adverse circumstances of Baish, linked to the mothers’ short stature, boys were smaller at birth than girls. Boys may have compensated for under-nutrition by increasing the depth of spiral artery invasion rather than by recruiting additional spiral arteries. Girls may have had more effective regional specialisation across the placental surface.
    Placenta 01/2014; · 3.12 Impact Factor
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    ABSTRACT: A detailed morphological description of the spectacle of the ball python (Python regius) is provided. The eyes of 21 snakes were examined by light microscopy and/or transmission electron microscopy. Additionally, eyes of nine live snakes were examined using optical coherence tomography (OCT) and Scheimpflug scanning (Pentacam). The spectacle consists of three layers: outer epithelium, stroma and inner epithelium. The outer epithelium is made up of flat basal cells overlaid by keratin, the stroma consists of organized layers of collagen fibrils with interweaving nerve fibers and blood vessels, and the inner epithelium holds squamous cells containing vesicles and microvilli. At the rim of the spectacle, there is a transition zone, where the spectacle merges with the epidermis and dermis of the periocular scales. This zone is characterized by a greater height of the basal cells of the outer epithelium and a less orderly organization of the stroma compared with the spectacle proper. The thickness of the spectacle was uniform throughout. It averaged 96 ± 10 µm in histological specimens and 108 ± 13 µm using OCT. The subspectacular space was extremely narrow in the live snakes; however, the space was visible at the periphery of the spectacle with OCT. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.
    Journal of Morphology 12/2013; · 1.60 Impact Factor
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    ABSTRACT: Transforming growth factor (TGF)-β1 has a pivotal role in the pathogenesis of progressive kidney diseases that are characterized by fibrosis. The main intracellular signaling pathway of TGF-β1 is the Smad system, where Smad2 and Smad3 play a central role in transcriptional regulation of target genes involved in extracellular matrix (ECM) metabolism. This study analyzes the hypothesis that blockade of Smad3 attenuates the development of TGF-β1-driven renal fibrosis. This was examined in vivo in a transgenic model of TGF-β1-induced chronic kidney disease with Smad3 or without Smad3 expression and in vitro in mesangial cells and glomerular endothelial cells with Smad2/3 inhibitors or Smad3-knockdown. Electron microscopy was used for evaluation of morphological changes, real-time polymerase chain reaction for detection of RNA expression, and immunohistochemistry for localization of ECM components. Matrix metalloproteinase (MMP) level was assessed by gelatin zymography electrophoresis and located by in situ zymography. The results show TGF-β1-induced mesangial matrix expansion, tubulointerstitial fibrosis, and tubular basement membrane thickening that are attenuated by Smad3 deletion, whereas TGF-β1-induced glomerular basement membrane thickening is not shown. The amount and distribution profile of MMP-2 may suggest a role of the enzyme herein. We conclude that Smad3 targeting is not exclusively beneficial as Smad3 has diverse transcriptional regulatory effects in different cell types in the kidney.
    Physiological reports. 12/2013; 1(7):e00181.
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    ABSTRACT: Oocytes from prepubertal (PRE) or postpubertal (POST) pigs are used in, for example, somatic cell nuclear transfer and in vitro fertilization. Here we describe mitochondrial dynamics in pig oocytes of different sizes before and after in vitro maturation (IVM), isolated from PRE or POST animals. In PRE oocytes, inside-zona pellucida diameter was measured before and after IVM (μm; small: ≤110, medium: >110, large: ≥120) and used for evaluation of (1) mitochondrial numbers before maturation and (2) mitochondrial morphology and location before and after maturation in comparison with POST oocytes. Oocytes were processed for transmission electron microscopy (Acta Anat. 129:12). For assessment of mitochondrial numbers, paired dissector sections were collected at uniform intervals throughout the oocyte, and in each set of dissector sections a known area fraction was sampled for mitochondrial counting in physical dissectors (J. Microsc. 134:127). Total number of mitochondria was calculated, and oocyte volume was estimated by Cavalieri estimator (J. Microsc. 147:229). Data were analysed by ANOVA. Mitochondrial morphology was classified as elongated, round, shell-like, or compartmentalized; mitochondrial cristae as transverse or peripheral; and mitochondrial location as cortical, subcortical, or central. Before IVM, small PRE presented elongated and round mitochondria with transverse cristae; medium and large PRE presented round mitochondria with peripheral and transverse cristae; POST presented round mitochondria with peripheral cristae in all cases. After IVM, small and medium PRE had round mitochondria with peripheral cristae; medium PRE and POST had shell-like mitochondria with peripheral cristae; large PRE had compartmentalized mitochondria with peripheral cristae. Before IVM, small PRE displayed cortical mitochondrial location, whereas the location in other groups was cortical and central. After IVM, mitochondria were located centrally in some large PRE and in all POST. Mitochondrial number increased during oocyte growth proportional to the increase in oocyte volume (Table 1). Shell-like and compartmentalized mitochondria indicate (1) dividing mitochondria (increasing mitochondrial numbers during maturation), or (2) apoptosis-related mitochondrial fission (compromised oocytes after maturation). After IVM, mitochondria seemed to reach the final central position most consistently in POST. These differences may partly explain the higher developmental competence in larger PRE and POST oocytes.
    Reproduction Fertility and Development 12/2013; 26(1):189-90. · 2.58 Impact Factor
  • Jens R Nyengaard, Saleh H Alwasel
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    ABSTRACT: We provide a practical review of the opportunities made available by design-unbiased stereology to estimate cell number, total volume, mean volume and mean height in the rat stomach using enterochromaffin-like cells as an example. The second example comprises estimation of the surface area of well-defined segments of rat colon and the volumes of different layers following surgery and/or treatment which may result in the atrophy or growth of the colon. The pros and cons of the stereologic designs are discussed and the pitfalls and some solutions to these are elucidated.
    Annals of anatomy = Anatomischer Anzeiger: official organ of the Anatomische Gesellschaft 11/2013; · 1.96 Impact Factor
  • Rie Stokholm, Flemming Isidor, Jens R Nyengaard
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    ABSTRACT: The primary aim of this study was to compare the bone reaction around immediate-loaded non-splinted single implants vs. delayed loaded non-splinted single implants placed in healed ridges in the posterior mandible. Six adult Macaca Fascicularis monkeys were used in this study. The first and second premolars and the first molar were extracted in both sides of the mandible. After 3 months of healing, four implants (Replace Select Tapered; Nobel Biocare, Gothenburg, Sweden) with a moderately rough surface (TiUnite, Nobel Biocare) were placed in the edentulous areas of each monkey, two in each side. The implants had a length of 10 mm and a diameter of 3.5 mm. Four groups of varying time and occlusal loading aspects were created: (i) control group: implant placed non-loaded for 3 months; (ii) immediate loaded: implant placed and loaded immediately for 3 months; (iii) immediate loaded: implant placed and loaded immediately for 6 months; and (iv) delayed loaded: implant placed submerged for 3 months and then loaded for 3 months. At the loaded implants, after a second stage surgery, a composite crown was made directly on an abutment mounted on the implant reinsuring simultaneous occlusal contact on the implant crown and the neighboring teeth. After euthanization of the animals, histologic specimens were quantified in the light microscope. All implants were clinically, radiographically, and histologically osseointegrated at the time of euthanization and with only mild signs of inflammation in the peri-implant mucosa. The histologic marginal bone level was located on average 1.14-1.74 mm apical to the margin of the implants in the various groups. The average bone-to-implant contact (BIC) varied between 55% and 65% and the average bone density (i.e., the proportion of mineralized bone tissue from the implant surface and to a distance of 1 mm lateral to the implant) varied between 30.6% and 34.2%. No statistical significant differences between groups were observed in the above-stated histomorphometric parameters. Similar histologic and histomorphometric findings were observed in immediately and delayed loaded non-splinted implants placed in the posterior mandible of macaque monkeys.
    Clinical Oral Implants Research 10/2013; · 3.43 Impact Factor
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    ABSTRACT: Since the publication of our article it has come to our attention that our Discussion inadvertently includes some sentences taken from the following articles by DeVries et al. and Bouet et al. without appropriate citation, using quotation marks: DeVries AC, Nelson RJ, Traystman RJ, Hurn PD: Cognitive and behavioural assessment in experimental stroke research: will it prove useful. Neurosci Biobehav Rev 2001, 25:325-342. Bouet V, Boulouard M, Toutain J, Divoux D, Bernaudin M, Schumann-Bard P, Freret T: The adhesive removal test: a sensitive method to assess sensorimotor deficits in mice. Nat Protoc 2009, 4:1560-1564. The authors apologize sincerely for this oversight.
    Experimental and Translational Stroke Medicine 08/2013; 5(1):10.
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    ABSTRACT: Rodent models have been used to evaluate aspects of liver regeneration. The aim of the present study was to investigate the natural history of liver regeneration in healthy rats. A 70% partial hepatectomy was performed in 64 rats. The animals were randomised into 8 groups and evaluated on postoperative days one to eight. Hepatocyte proliferation was evaluated by immunohistochemistry using unbiased stereological principles. The mean rat body weight was 238 g (211-287). The mean weight of the resected liver was 6.3 g (5.2-7.3) and the estimated mean total liver weight was 8.9 g (7.4-10.4). Both liver weight analysis and regeneration rate showed an ascending curve, with a maximum slope on postoperative days 1-4, reaching a steady state on days 5-8. Hepatocyte proliferation (positive Ki-67 cell profiles pr. mm(2)) was high (250 cell profiles/mm(2)) on postoperative days 1-3 and tapered off on day 5. Seventy percent partial hepatectomy in healthy rats induces a rapid regenerative response and PODs 2, 4 and 8 seems optimal for assessing hepatic growth in future studies.
    International Journal of Surgery (London, England) 07/2013; · 1.44 Impact Factor
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    ABSTRACT: The podocyte depletion hypothesis has emerged as a unifying concept in glomerular pathology. According to this hypothesis podocyte depletion may be absolute (decrease in number of healthy mature podocytes), relative (fewer podocytes per unit of glomerular volume) or involve alterations to the specialized podocyte architecture (such as foot process effacement). To study and understand podocyte depletion it is important to be able to accurately and precisely count these cells. Here we present new design-based stereological methods for estimating podocyte number in individual glomeruli of known volume, and in average glomeruli. Both methods involve serial histological sectioning, triple label immunohistochemistry, laser confocal microscopy and cell counting with the optical disector/fractionator.
    Annals of anatomy = Anatomischer Anzeiger: official organ of the Anatomische Gesellschaft 05/2013; · 1.96 Impact Factor
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    ABSTRACT: BACKGROUND: Sorafenib is a multikinase inhibitor with antiangiogenic and antiproliferative properties, approved for the treatment of hepatocellular carcinoma. The effect of Sorafenib on liver regeneration in healthy rats was investigated. METHODS: Sixty Wistar rats received either Sorafenib (group S; 15 mg/kg) or placebo for 14 days prior to resection and until sacrifice. After a 70% partial hepatectomy, the rats were euthanized on post-operative days (POD) 2, 4 or 8. Hepatocyte proliferation was estimated by immunohistochemistry for Ki-67 antigen using stereological methods on sections prepared by systematic uniform random sampling. RESULTS: Seven animals (12%) died after surgery. Death rates were similar in treated rats and controls. At hepatectomy, the body weight was significantly lower in group S rats. The liver weight and regeneration rates were lower in group S rats on PODs 2, 4 and 8. Hepatocyte proliferation was significantly lower in group S animals on PODs 2 and 4. Alanine aminotransferase ALAT was significantly higher in the Sorafenib-treated group on PODs 2, 4 and 8. Alkaline phosphatase ALP and bilirubin levels were similar in the two groups, although bilirubin was elevated in group S rats on POD 8. CONCLUSION: In this rat model, Sorafenib did not increase post-hepatectomy mortality, but was associated with a significant impaired liver weight gain, regeneration rates and hepatocyte proliferation.
    HPB 03/2013; · 1.94 Impact Factor
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    ABSTRACT: Assessment of intraepidermal nerve fiber density (IENFD) has become a useful tool for the investigation of patients with suspected small-fiber neuropathy (SFN). Here, we estimate epidermal nerve fiber lengths in 12 patients with SFN and 36 healthy controls using global spatial sampling and compare the lengths with IENFD and axonal swelling ratios. Skin biopsies were analyzed on 50-μm-thick free-floating sections immunostained for the neuronal cytoplasmic marker PGP 9.5. Mean IENFD in SFN patients was 2.22 ± 1.63 mm versus 7.51 ± 2.17 mm in controls; mean length density was 112 ± 82.6 mm in SFN patients versus 565 ± 240 mm in controls (p < 0.001 for both). The correlation between the nerve fiber length and the IENFD was r = 0.16 for healthy subjects and r = 0.39 for patients, suggesting that these variables provide different quantitative information. There were significant differences in axonal swelling ratios between healthy subjects and patients, that is, per IENFD and per nerve fiber length. Together, these results suggest that, although length estimation requires more time and additional equipment, it is as effective as IENFD in differentiating SFN patients from healthy subjects. Estimating nerve fiber length may increase mechanistic understanding beyond IENFD estimation and improve efficiency in diagnosing SFN.
    Journal of neuropathology and experimental neurology. 03/2013; 72(3):186-93.
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    ABSTRACT: Xenoturbella bocki, a marine animal with a simple body plan, has recently been suggested to be sister group to the Acoelomorpha, together forming the new phylum Xenacoelomorpha. The phylogenetic position of the phylum is still under debate, either as an early branching bilaterian or as a sister group to the Ambulacraria (hemichordates and echinoderms) within the deuterostomes. Although development has been described for several species of Acoelomorpha, little is known about the life cycle of Xenoturbella. Here we report the embryonic stages of Xenoturbella, and show that it is a direct developer without a feeding larval stage. This mode of development is similar to that of the acoelomorphs, supporting the newly proposed phylum Xenacoelomorpha and suggesting that the last common ancestor of the phylum might have been a direct developer.
    Nature Communications 02/2013; 4:1537. · 10.02 Impact Factor
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    ABSTRACT: The giraffe heart has a relative mass similar to other mammals, but generates twice the blood pressure to overcome the gravitational challenge of perfusing the cerebral circulation. To provide insight as to how the giraffe left ventricle (LV) is structurally adapted to tackle such a high afterload, we performed a quantitative structural study of the LV myocardium in young and adult giraffe hearts. Tissue samples were collected from young and adult giraffe LV. Design-based stereology was used to obtain unbiased estimates of numbers and sizes of cardiomyocytes, nuclei and capillaries. The numerical density of myocyte nuclei was 120 × 10(3) mm(-3) in the adult and 504 × 10(3) mm(-3) in the young LV. The total number (N) of myocyte nuclei was 1.3 × 10(11) in the adult LV and 4.9 × 10(10) in the young LV. In the adult LV the volume per myocyte was 39.5 × 10(3) µm(3) and the number of nuclei per myocyte was 4.2. The numerical density of myocytes was 24.1 × 10(6) cm(-3) and the capillary volume fraction of the adult giraffe ventricle was 0.054. The significantly higher total number of myocyte nuclei in the adult LV, the high density of myocyte nuclei in the LV, and the number of nuclei per myocyte (which was unusually high compared to other mammalian, including human data), all suggest the presence of myocyte proliferation during growth of the animal to increase wall thickness and normalize LV wall tension as the neck lengthens and the need for higher blood pressure ensues. Anat Rec, 2013. © 2013 Wiley Periodicals, Inc.
    The Anatomical Record Advances in Integrative Anatomy and Evolutionary Biology 02/2013; · 1.34 Impact Factor
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    ABSTRACT: Glial cell-line-derived neurotrophic factor (GDNF) is a potent neurotrophic factor that has reached clinical trials for Parkinson's disease. GDNF binds to its coreceptor GFRα1 and signals through the transmembrane receptor tyrosine kinase RET, or RET independently through NCAM or syndecan-3. Whereas the GDNF signaling cascades are well described, cellular turnover and trafficking of GDNF and its receptors remain poorly characterized. Here, we find that SorLA acts as sorting receptor for the GDNF/GFRα1 complex, directing it from the cell surface to endosomes. Through this mechanism, GDNF is targeted to lysosomes and degraded while GFRα1 recycles, creating an efficient GDNF clearance pathway. The SorLA/GFRα1 complex further targets RET for endocytosis but not for degradation, affecting GDNF-induced neurotrophic activities. SorLA-deficient mice display elevated GDNF levels, altered dopaminergic function, marked hyperactivity, and reduced anxiety, all of which are phenotypes related to abnormal GDNF activity. Taken together, these findings establish SorLA as a critical regulator of GDNF activity in the CNS.
    Cell reports. 01/2013;
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    ABSTRACT: Stroke is a major cause of death and severe disability, but effective treatments are limited. Neuroglobin, a neuronal heme-globin, has been advocated as a novel pharmacological target in combating stroke and neurodegenerative disorders based on cytoprotective properties. Using thoroughly validated antibodies and oligos, we give a detailed brain anatomical characterization of transgenic mice over expressing Neuroglobin. Moreover, using permanent middle artery occlusion the effect of elevated levels of Neuroglobin on ischemic damage was studied. Lastly, the impact of mouse strain genetic background on ischemic damage was investigated. A four to five fold increase in Neuroglobin mRNA and protein expression was seen in the brain of transgenic mice. A β-actin promoter was used to drive Neuroglobin over expression, but immunohistochemistry and in situ hybridization showed over expression to be confined to primarily the cortex, hippocampus, cerebellum, and only in neurons. The level and expression pattern of endogenous Neuroglobin was unaffected by insertion of the over expressing Ngb transgene. Neuroglobin over expression resulted in a significant reduction in infarct volume 24 hours after ischemia. Immunohistochemistry showed no selective sparing of Neuroglobin expressing cells in the ischemic core or penumbra. A significant difference in infarct volume was found between mice of the same strain, but from different colonies. In contrast to some previous reports, Neuroglobin over expression is not global but confined to a few well-defined brain regions, and only in neurons. This study confirms previous reports showing a correlation between reduced infarct volume and elevated Neuroglobin levels, but underlines the need to study the likely contribution from compensatory mechanisms to the phenotype following a genetic perturbation. We also stress, that care should be taken when comparing results where different mouse strains and colonies have been used due to large genetic background contribution to the observed phenotype.
    PLoS ONE 01/2013; 8(10):e76565. · 3.73 Impact Factor

Publication Stats

3k Citations
679.10 Total Impact Points


  • 1999–2014
    • Aarhus University
      • • Department of Clinical Medicine
      • • Department of Medical Biochemistry
      • • Department of Zoophysiology
      • • Department of Dentistry
      • • Institute of Anatomy
      • • Institute of Experimental Clinical Research
      Aarhus, Central Jutland, Denmark
  • 2013
    • Vendsyssel Hospital
      Hjørring, North Denmark, Denmark
    • Danish Pain Research Center
      Aarhus, Central Jutland, Denmark
  • 2011–2013
    • Monash University (Australia)
      • • Department of Anatomy and Developmental Biology
      • • School of Biomedical Sciences
      Melbourne, Victoria, Australia
  • 2008–2013
    • University of Copenhagen
      • • Department of Neuroscience and Pharmacology
      • • Department of Clinical Veterinary Medicine and Animal Science
      København, Capital Region, Denmark
  • 2007–2011
    • Charité Universitätsmedizin Berlin
      • Institute of Clinical Pharmacology and Toxicology
      Berlin, Land Berlin, Germany
    • Freie Universität Berlin
      Berlín, Berlin, Germany
    • Shahid Sadoughi University of Medical Sciences and Health Services
      Yezd, Yazd, Iran
  • 2010
    • University of Southern Denmark
      Odense, South Denmark, Denmark
  • 2009
    • Boston University
      • Department of Medicine
      Boston, MA, United States
  • 2008–2009
    • Chongqing Medical University
      Ch’ung-ch’ing-shih, Chongqing Shi, China
  • 2006–2009
    • University of Szeged
      • Department of Pathology
      Szeged, Csongrad megye, Hungary
    • Aarhus University Hospital
      • Institute of Clinical Medicine
      Aarhus, Central Jutland, Denmark
    • University of Minnesota Twin Cities
      • Department of Pediatrics
      Minneapolis, MN, United States
  • 2004
    • Georg-August-Universität Göttingen
      • Department of Molecular Electron Cryomicroscopy
      Göttingen, Lower Saxony, Germany
  • 2003
    • Experimental Pathology Laboratories, Inc.
      Sterling, Virginia, United States
  • 2002
    • Albert Einstein College of Medicine
      • Department of Medicine
      New York City, NY, United States
  • 1997
    • University of Washington Seattle
      • Department of Pathology
      Seattle, WA, United States