https://doi.org/10.4081/ejh.2021.3305
Ion channels alterations in the forebrain of high-fat diet fed rats
Submitted: 12 July 2021
Accepted: 27 October 2021
Published: 23 November 2021
Accepted: 27 October 2021
Abstract Views: 1536
PDF: 860
HTML: 21
HTML: 21
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Authors
Evidence suggests that transient receptor potential (TRP) ion channels dysfunction significantly contributes to the physiopathology of metabolic and neurological disorders. Dysregulation in functions and expression in genes encoding the TRP channels cause several inherited diseases in humans (the so-called ‘TRP channelopathies’), which affect the cardiovascular, renal, skeletal, and nervous systems. This study aimed to evaluate the expression of ion channels in the forebrain of rats with diet-induced obesity (DIO). DIO rats were studied after 17 weeks under a hypercaloric diet (high-fat diet, HFD) and were compared to the control rats with a standard diet (CHOW). To determine the systemic effects of HFD exposure, we examined food intake, fat mass content, fasting glycemia, insulin levels, cholesterol, and triglycerides. qRT-PCR, Western blot, and immunochemistry analysis were performed in the frontal cortex (FC) and hippocampus (HIP). After 17 weeks of HFD, DIO rats increased their body weight significantly compared to the CHOW rats. In DIO rats, TRPC1 and TRPC6 were upregulated in the HIP, while they were downregulated in the FC. In the case of TRPM2 expression, instead was increased both in the HIP and in the FC. These could be related to the increase of proteins and nucleic acid oxidation. TRPV1 and TRPV2 gene expression showed no differences both in the FC and HIP. In general, qRT-PCR analyses were confirmed by Western blot analysis. Immunohistochemical procedures highlighted the expression of the channels in the cell body of neurons and axons, particularly for the TRPC1 and TRPC6. The alterations of TRP channel expression could be related to the activation of glial cells or the neurodegenerative process presented in the brain of the DIO rat highlighted with post synaptic protein (PSD 95) alterations. The availability of suitable animal models may be useful for studying possible pharmacological treatments to counter obesity-induced brain injury. The identified changes in DIO rats may represent the first insight to characterize the neuronal alterations occurring in obesity. Further investigations are necessary to characterize the role of TRP channels in the regulation of synaptic plasticity and obesity-related cognitive decline.
Belsky DW, Caspi A, Goldman-Mellor S, Meier MH, Ramrakha S, Poulton R, et al. Is obesity associated with a decline in intelligence quotient during the first half of the life course? Am J Epidemiol 2013;178:1461-8.
DOI: https://doi.org/10.1093/aje/kwt135
Haslam DW, James WP. Obesity. Lancet 2005;366:1197-209.
DOI: https://doi.org/10.1016/S0140-6736(05)67483-1
Bocarsly ME, Fasolino M, Kane GA, La Marca EA, Kirschen GW, Karatsoreos IN, et al. Obesity diminishes synaptic markers, alters microglial morphology, and impairs cognitive function. Proc Natl Acad Sci USA 2015;112:15731-6.
DOI: https://doi.org/10.1073/pnas.1511593112
Lodish H, Berk A, Zipursky SL, Freeman WH. Neurotransmitters, synapses, and impulse transmission. In: Lodish H, Berk A, Zipursky SL, Freeman WH, editors. Molecular Cell Biology. New York: W.H. Freeman; 2000. Section 21.4.
Gouaux E, MacKinnon R. Principles of selective ion transport in channels and pumps. Science 2005;310:1461-5.
DOI: https://doi.org/10.1126/science.1113666
Gees M, Colsoul B, Nilius B. The role of transient receptor potential cation channels in Ca2+ Signaling. Cold Spring Harb Perspect Biol 2010;2:a003962.
DOI: https://doi.org/10.1101/cshperspect.a003962
Gualdani R, Gailly P. How TRPC channels modulate hippocampal function. Int J Mol Sci 2020;21:3915.
DOI: https://doi.org/10.3390/ijms21113915
Ciardo MG, Ferrer-Montiel A. Lipids as central modulators of sensory TRP channels. Biochim Biophys Acta Biomembr 2017;1859:1615-8.
DOI: https://doi.org/10.1016/j.bbamem.2017.04.012
Schaefer M. Homo- and heteromeric assembly of TRP channel subunits. Pflugers Arch 2005;451:35-42.
DOI: https://doi.org/10.1007/s00424-005-1467-6
Sawamura S, Shirakawa H, Nakagawa T, Mori Y, Kaneko S. TRP channels in the brain: What are they there for? In: TLR Emir, editor. Neurobiology of TRP channels. Boca Raton: CRC Press/Taylor & Francis; 2017. Chapter 16.
DOI: https://doi.org/10.4324/9781315152837-16
Hayes P, Meadows HJ, Gunthorpe MJ, Harries MH, Duckworth DM, Cairns W, Harrison DC, Clarke CE, Ellington K, Prinjha RK, et al. Cloning and functional expression of a human orthologue of rat vanilloid receptor 1. Pain 2000;88:205-15.
DOI: https://doi.org/10.1016/S0304-3959(00)00353-5
Kim SR, Kim SU, Oh U, Jin BK. Transient receptor potential vanilloid subtype 1 mediates microglial cell death in vivo and in vitro via Ca2+-mediated mitochondrial damage and cytochrome c release. J Immunol 2006;177:4322-9.
DOI: https://doi.org/10.4049/jimmunol.177.7.4322
Liapi A, Wood JN. Extensive co-localization and heteromultimer formation of the vanilloid receptor-like protein TRPV2 and the capsaicin receptor TRPV1 in the adult rat cerebral cortex. Eur J Neurosci 2005;22:825-34.
DOI: https://doi.org/10.1111/j.1460-9568.2005.04270.x
Shibasaki K, Ishizaki Y, Mandadi S. Astrocytes express functional TRPV2 ion channels. Biochem Biophys Res Commun 2013;441:327-32.
DOI: https://doi.org/10.1016/j.bbrc.2013.10.046
Vennekens R, Menigoz A, Nilius, B. TRPs in the brain. Rev Physiol Biochem Pharmacol 2012;163:27-64.
DOI: https://doi.org/10.1007/112_2012_8
Tiruppathi C, Ahmmed GU, Vogel SM, Malik AB. Ca2+ signaling, TRP channels, and endothelial permeability. Microcirculation 2006;13:693-708.
DOI: https://doi.org/10.1080/10739680600930347
Authi KS. TRP channels in platelet function. In: V Flockerzi, B Nilius, editors. Transient receptor potential (TRP) channels. Handbook of experimental pharmacology, vol 179. Springer; 2007. p. 425-43.
DOI: https://doi.org/10.1007/978-3-540-34891-7_25
Dietrich A, Chubanov V, Kalwa H, Rost BR, Gudermann T. Cation channels of the transient receptor potential superfamily: their role in physiological and pathophysiological processes of smooth muscle cells. Pharmacol Ther 2006;112:744-60.
DOI: https://doi.org/10.1016/j.pharmthera.2006.05.013
Mori Y, Wakamori M, Miyakawa T, Hermosura M, Hara Y, Nishida M, et al. Transient receptor potential 1 regulates capacitative Ca2+ entry and Ca2+ release from endoplasmic reticulum in B lymphocytes. J Exp Med 2002;195:673-81.
DOI: https://doi.org/10.1084/jem.20011758
Kim SJ, Kim YS, Yuan JP, Petralia RS, Worley PF, Linden DJ. Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. Nature 2003;426:285-91.
DOI: https://doi.org/10.1038/nature02162
Shim S, Yuan JP, Kim JY, Zeng W, Huang G, Milshteyn A, et al. Peptidyl-prolyl isomerase FKBP52 controls chemotropic guidance of neuronal growth cones via regulation of TRPC1 channel opening. Neuron 2009;64:471-83.
DOI: https://doi.org/10.1016/j.neuron.2009.09.025
Qiu J, Fam Y, Ronnekleiv OK, Kelly MJ. Leptin excites proopiomelanocortin neurons via activation of TRPC channels. J Neurosci 2010;30:1560-5.
Li M, Chen C, Xhou Z, Xu S, Yu Z. TRPC1 mediated the increase in store-operated Ca2+entry is required for the proliferation of adult hippocampal neuronal progenitor cells. Cell Calcium 2012;51:486-96.
DOI: https://doi.org/10.1016/j.ceca.2012.04.014
Riccio A, Medhurst AD, Mattei C, Kelsell RE, Calver AR, Randall AD, et al. mRNA distribution analysis of human TRPC family in CNS and peripheral tissues. Brain Res Mol Brain Res 2002;109:95-104.
DOI: https://doi.org/10.1016/S0169-328X(02)00527-2
Jia Y, Zhou J, Tai Y, Wang Y. TRPC channels promote cerebellar granule neuron survival. Nat Neurosci 2007;10:559-67.
DOI: https://doi.org/10.1038/nn1870
Zhou J, Du W, Zhou K, Tai Y, Yao H, Jia Y, et al. Critical role of TRPC6 channels in the formation of excitatory synapses. Nat Neurosci 2008;11:741-3.
Li Y, Jia YC, Cui K, Li N, Zheng ZY, Wang YZ, et al. Essential role of TRPC channels in the guidance of nerve growth cones by brain-derived neurotrophic factor. Nature 2005;434:894-8.
DOI: https://doi.org/10.1038/nature03477
Zhou J, Du W, Zhou K, Tai Y, Yao H, Jia Y, et al. Critical role of TRPC6 channels in the formation of excitatory synapses. Nat Neurosci 2008;11:741-3.
Kraft R, Harteneck C. The mammalian melastatin related transient receptor potential cation channels: an overview. Pflugers Arch 2005;451:204-11.
DOI: https://doi.org/10.1007/s00424-005-1428-0
Malko P, Syed Mortadza SA, McWilliam J, Jiang LH. TRPM2 channel in microglia as a new player in neuroinflammation associated with a spectrum of central nervous system pathologies. Front Pharmacol 2019;10:239.
Bond CE, Greenfield SA. Multiple cascade effects of oxidative stress on astroglia. Glia 2007;55:1348-61.
DOI: https://doi.org/10.1002/glia.20547
Liu M, Huang W, Wu D, Priestley J V. TRPV1, but not P2X, requires cholesterol for its function and membrane expression in rat nociceptors. Eur J Neurosci 2006;24:1-6.
DOI: https://doi.org/10.1111/j.1460-9568.2006.04889.x
Zsombok A, Derbenev AV. TRP Channels as therapeutic targets in diabetes and obesity. Pharmaceuticals (Basel) 2016;9:50.
DOI: https://doi.org/10.3390/ph9030050
Micioni Di Bonaventura MV, Martinelli I, Moruzzi M, Micioni Di Bonaventura E, Giusepponi ME, Polidori C, et al. Brain alterations in high fat diet induced obesity: effects of tart cherry seeds and juice. Nutrients 2020;12:623.
DOI: https://doi.org/10.3390/nu12030623
Martinelli I, Tomassoni D, Moruzzi M, Roy P, Cifani C, Amenta F, et al. Cardiovascular changes related to metabolic syndrome: Evidence in obese Zucker rats. Int J Mol Sci 2020;21:2035.
DOI: https://doi.org/10.3390/ijms21062035
Martinelli I, Tomassoni D, Roy P, Di Cesare Mannelli L, Amenta F, Tayebati SK. Antioxidant properties of alpha-lipoic (thioctic) acid treatment on renal and heart parenchyma in a rat model of hypertension. Antioxidants (Basel) 2021;10:1006.
DOI: https://doi.org/10.3390/antiox10071006
O'Brien PD, Hinder LM, Callaghan BC, Feldman EL. Neurological consequences of obesity. Lancet Neurol 2017;16:465-77.
DOI: https://doi.org/10.1016/S1474-4422(17)30084-4
Levin BE, Dunn-Meynell AA. Defense of body weight against chronic caloric restriction in obesity-prone and -resistant rats. Am J Physiol Regul Integr Comp Physiol 2000;278:R231-7.
DOI: https://doi.org/10.1152/ajpregu.2000.278.1.R231
Surwit RS, Feinglos MN, McCaskill CC, Clay SL, Babyak MA, Brownlow BS, Plaisted CS, Lin PH. Metabolic and behavioral effects of a high-sucrose diet during weight loss. Am J Clin Nutr 1997;65:908-15.
DOI: https://doi.org/10.1093/ajcn/65.4.908
Levin BE, Routh VH. Role of the brain in energy balance and obesity. Am J Physiol 1996;271:R491-500.
DOI: https://doi.org/10.1152/ajpregu.1996.271.3.R491
Smani T, Shapovalov G, Skryma R, Prevarskaya N, Rosado JA. Functional and physiopathological implications of TRP channels. Biochim Biophys Acta 2015;1853:1772-82.
DOI: https://doi.org/10.1016/j.bbamcr.2015.04.016
Hong C, Jeong B, Park HJ, Chung JY, Lee JE, Kim J, et al. TRP Channels as emerging therapeutic targets for neurodegenerative diseases. Front Physiol 2020;11:238.
DOI: https://doi.org/10.3389/fphys.2020.00238
Kaneko Y, Szallasi A. Transient receptor potential (TRP) channels: a clinical perspective. Br J Pharmacol 2014;171:2474-507.
DOI: https://doi.org/10.1111/bph.12414
Wang R, Tu S, Zhang J, Shao A. Roles of TRP channels in neurological diseases. Oxid Med Cell Longev 2020;2020:7289194.
DOI: https://doi.org/10.1155/2020/7289194
Yang XL, Wang X, Shao L, Jang GT, Min JW, Mei XY, et al. TRPV1 mediates astrocyte activation and interleukin-1β release induced by hypoxic ischemia (HI). J Neuroinflammation 2019;16:114.
DOI: https://doi.org/10.1186/s12974-019-1487-3
Nedungadi T P, Dutta M, Bathina SC, Caterina MJ, Cunningham JT. Expression and Distribution of TRPV2 in rat brain. Exp Neurol 2012;237: 223-37.
DOI: https://doi.org/10.1016/j.expneurol.2012.06.017
Erac Y, Selli C, Kosova B, Akcali KC, Tosun M. Expression levels of TRPC1 and TRPC6 ion channels are reciprocally altered in aging rat aorta: implications for age-related vasospastic disorders. Age (Dordr) 2010;32:223-30.
DOI: https://doi.org/10.1007/s11357-009-9126-z
Wang J, Lu R, Yang J, Li H, He Z, Jing N, et al. TRPC6 specifically interacts with APP to inhibit its cleavage by γ-secretase and reduce Aβ production. Nat Commun 2015;6:8876.
DOI: https://doi.org/10.1038/ncomms9876
Lin Y, Chen F, Zhang J, Wang T, Wei X, Wu J, et al. Neuroprotective effect of resveratrol on ischemia/reperfusion injury in rats through TRPC6/CREB pathways. J Mol Neurosci 2013;50:504-13.
DOI: https://doi.org/10.1007/s12031-013-9977-8
Zeng C, Zhou P, Jiang T, Yuan C, Ma Y, Feng L, et al. Upregulation and diverse roles of TRPC3 and TRPC6 in synaptic reorganization of the mossy fiber pathway in temporal lobe epilepsy. Mol Neurobiol 2015;52:562-72.
DOI: https://doi.org/10.1007/s12035-014-8871-x
Tai Y, Feng S, Ge R, Du W, Zhang X, He Z, et al. TRPC6 channels promote dendritic growth via the CaMKIV-CREB pathway. J Cell Sci 2008;121:2301-7.
DOI: https://doi.org/10.1242/jcs.026906
Zhou J, Du W, Zhou K, Tai Y, Yao H, Jia Y, et al. Critical role of TRPC6 channels in the formation of excitatory synapses. Nat Neurosci 2008;11:741-3.
DOI: https://doi.org/10.1038/nn.2127
Qu C, Ding M, Zhu Y, Lu Y, Du J, Miller M, et al. Pyrazolopyrimidines as potent stimulators for transient receptor potential canonical 3/6/7 channels. J Med Chem 2017;60:4680-92.
DOI: https://doi.org/10.1021/acs.jmedchem.7b00304
Hong C, Seo H, Kwak M, Jeon J, Jang J, Jeong EM, et al. Increased TRPC5 glutathionylation contributes to striatal neuron loss in Huntington's disease. Brain 2015;138:3030-47.
DOI: https://doi.org/10.1093/brain/awv188
Bollimuntha S, Ebadi M, Singh BB. TRPC1 protects human SH-SY5Y cells against salsolinol-induced cytotoxicity by inhibiting apoptosis. Brain Res 2006;1099:141-9.
DOI: https://doi.org/10.1016/j.brainres.2006.04.104
Selvaraj S, Sun Y, Watt JA, Wang S, Lei S, Birnbaumer L, et al. Neurotoxin-induced ER stress in mouse dopaminergic neurons involves downregulation of TRPC1 and inhibition of AKT/mTOR signaling. J Clin Invest 2012;122:1354-67.
DOI: https://doi.org/10.1172/JCI61332
Weimer RM, Jorgensen EM. Controversies in synaptic vesicle exocytosis. J Cell Sci 2003;116:3661-6.
DOI: https://doi.org/10.1242/jcs.00687
Shuai Hao, Aditi Dey, Xiaolin Yu , Alexis M Stranahan. Dietary obesity reversibly induces synaptic stripping by microglia and impairs hippocampal plasticity. Brain Behav Immun 2016;51:230-9.
DOI: https://doi.org/10.1016/j.bbi.2015.08.023
Jiang L-H, Yang W, Zou J, Beech DJ. TRPM2 channel properties, functions and therapeutic potentials. Expert Opin Ther Targets 2010;14:973-88.
DOI: https://doi.org/10.1517/14728222.2010.510135
Plato CC, Galasko D, Garruto RM, Plato M, Gamst A, Craig UK, et al. ALS and PDC of Guam: forty-year follow-up. Neurology 2002;58:765-73.
DOI: https://doi.org/10.1212/WNL.58.5.765
Övey İS, Naziroğlu M. Homocysteine and cytosolic GSH depletion induce apoptosis and oxidative toxicity through cytosolic calcium overload in the hippocampus of aged mice: involvement of TRPM2 and TRPV1 channels. Neuroscience 2015;284:225-33.
DOI: https://doi.org/10.1016/j.neuroscience.2014.09.078
Ostapchenko VG, Chen M, Guzman MS, Xie YF, Lavine N, Fan J, et al. The transient receptor potential melastatin 2 (TRPM2) channel contributes to β-amyloid oligomer-related neurotoxicity and memory impairment. J Neurosci 2015;35:15157-69.
DOI: https://doi.org/10.1523/JNEUROSCI.4081-14.2015
Malko P, Syed Mortadza SA, McWilliam J, Jiang LH. TRPM2 channel in microglia as a new player in neuroinflammation associated with a spectrum of central nervous system pathologies. Front Pharmacol 2019;10:239.
DOI: https://doi.org/10.3389/fphar.2019.00239
Wang L, Wei LY, Ding R, Feng Y, Li D, Li C, et al. Predisposition to Alzheimer's and age-related brain pathologies by PM2.5 exposure: Perspective on the roles of oxidative stress and TRPM2 channel. Front Physiol 2020;11:155.
DOI: https://doi.org/10.3389/fphys.2020.00155
Miller BA, Zhang W. TRP channels as mediators of oxidative stress. Adv Exp Med Biol 2011;704:531-44.
DOI: https://doi.org/10.1007/978-94-007-0265-3_29
Tomassoni D, Martinelli I, Moruzzi M, Micioni Di Bonaventura MV, Cifani C, Amenta F, Tayebati SK. Obesity and age-related changes in the brain of the Zucker Leprfa/fa rats. Nutrients 2020;12:1356.
DOI: https://doi.org/10.3390/nu12051356
Nilius B, Szallasi A. Transient receptor potential channels as drug targets: from the science of basic research to the art of medicine. Pharmacol Rev 2014;66:676-814.
DOI: https://doi.org/10.1124/pr.113.008268
Skaper SD. Ion channels on microglia: therapeutic targets for neuroprotection. CNS Neurol Disord Drug Targets 2011;10:44-56.
DOI: https://doi.org/10.2174/187152711794488638
Echeverry S, Rodriguez MJ, Torres YP. Transient receptor potential channels in microglia: Roles in physiology and disease. Neurotox Res 2016;30:467-78.
DOI: https://doi.org/10.1007/s12640-016-9632-6
Golovina VA. Visualization of localized store-operated calcium entry in mouse astrocytes. Close proximity to the endoplasmic reticulum. J Physiol 2005;564:737-49.
DOI: https://doi.org/10.1113/jphysiol.2005.085035
Hartman RE, Kamper JE, Goyal R, Stewart JM, Longo LD. Motor and cognitive deficits in mice bred to have low or high blood pressure. Physiol Behav 2012;105:1092-7.
DOI: https://doi.org/10.1016/j.physbeh.2011.11.022
Qiu J, Fang Y, Ronnekleiv OK, Kelly MJ. Leptin excites proopiomelanocortin neurons via activation of TRPC channels. J Neurosci 2010;30:1560-5.
DOI: https://doi.org/10.1523/JNEUROSCI.4816-09.2010
Xie YF, Belrose JC, Lei G, Tymianski M, Mori Y, Macdonald JF, Jackson MF. Dependence of NMDA/GSK-3β mediated metaplasticity on TRPM2 channels at hippocampal CA3-CA1 synapses. Mol Brain 2011;4:44.
DOI: https://doi.org/10.1186/1756-6606-4-44
Lee GR, Shin MK, Yoon DJ, Kim AR, Yu R, Park NH, Han IS. Topical application of capsaicin reduces visceral adipose fat by affecting adipokine levels in high-fat diet-induced obese mice. Obesity (Silver Spring) 2013;21:115-22.
DOI: https://doi.org/10.1002/oby.20246
Shimizu T, MacEy TA, Quillinan N, Klawitter J, Oerraud ALL, Traystman RJ, Herson PS. Androgen and PARP-1 regulation of TRPM2 channels after ischemic injury. J Cereb Blood Flow Metab 2013;33:1549-55.
DOI: https://doi.org/10.1038/jcbfm.2013.105
Ethics Approval
The protocol was approved by the Ethics Committee of the University of CamerinoSupporting Agencies
This research was supported by University of Camerino, Fondo d'Ateneo di Ricerca (FAR 2019).How to Cite
Roy, P., Martinelli, I., Moruzzi, M., Maggi, F., Amantini, C., Micioni Di Bonaventura, M. V., … Tomassoni, D. (2021). Ion channels alterations in the forebrain of high-fat diet fed rats. European Journal of Histochemistry, 65(s1). https://doi.org/10.4081/ejh.2021.3305
Copyright (c) 2021 The Author(s)
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.
Similar Articles
- Federico Angelo Cazzaniga, Edoardo Bistaffa, Chiara Maria Giulia De Luca, Giuseppe Bufano, Antonio Indaco, Giorgio Giaccone, Fabio Moda, Sporadic Creutzfeldt-Jakob disease: Real-Time Quaking Induced Conversion (RT-QuIC) assay represents a major diagnostic advance , European Journal of Histochemistry: Vol. 65 No. s1 (2021): Special Collection on Advances in Neuromorphology in Health and Disease
- Lan Wang, Zhenyu Fan, Haijin Wang, Shougui Xiang, Propofol alleviates M1 polarization and neuroinflammation of microglia in a subarachnoid hemorrhage model in vitro, by targeting the miR-140-5p/TREM-1/NF-κB signaling axis , European Journal of Histochemistry: Vol. 68 No. 3 (2024)
- A. Porzionato, M. Rucinski, V. Macchi, G. Sarasin, L.K. Malendowicz, R. De Caro, ECRG4 expression in normal rat tissues: expression study and literature review , European Journal of Histochemistry: Vol. 59 No. 2 (2015)
- R. Song, W. Xu, Y. Chen, Z. Li, Y. Zeng, Y. Fu, The expression of Sirtuins 1 and 4 in peripheral blood leukocytes from patients with type 2 diabetes , European Journal of Histochemistry: Vol. 55 No. 1 (2011)
- M. Ferreira Júnior, S.A. Batista, P.V.T. Vidigal, A.A.C. Cordeiro, F.M.S. Oliveira, L.O. Prata, A.E.T. Diniz, C.M. Barral, R.C. Barbuto, A.D. Gomes, I.D. Araújo, D.M.M. Queiroz, M.V. Caliari, Infection with CagA-positive Helicobacter pylori strain containing three EPIYA C phosphorylation sites is associated with more severe gastric lesions in experimentally infected Mongolian gerbils (Meriones unguiculatus) , European Journal of Histochemistry: Vol. 59 No. 2 (2015)
- Antonio D'Amati, Roberto Tamma, Tiziana Annese, Anna Rizzi, Domenico Ribatti, Mast cells in meningiomas , European Journal of Histochemistry: Vol. 68 No. 2 (2024)
- Kazuhiko Hashimoto, Shunji Nishimura, Tomohiko Ito, Masao Akagi, Characterization of PD-1/PD-L1 immune checkpoint expression in soft tissue sarcomas , European Journal of Histochemistry: Vol. 65 No. 3 (2021)
- Y. Zhu, D. Ning, F. Wang, C. Liu, Y. Xu, X. Jia, D. Zhu, Effect of thyroxine on munc-18 and syntaxin-1 expression in dorsal hippocampus of adult-onset hypothyroid rats , European Journal of Histochemistry: Vol. 56 No. 2 (2012)
- E. Guerriero, M. Accardo, F. Capone, G. Colonna, G. Castello, S. Costantini, Assessment of the Selenoprotein M (SELM) over-expression on human hepatocellular carcinoma tissues by immunohistochemistry , European Journal of Histochemistry: Vol. 58 No. 4 (2014)
- Simon Schöfer, Sylvia Laffer, Stefanie Kirchberger, Michael Kothmayer, Renate Löhnert, Elmar E. Ebner, Klara Weipoltshammer, Martin Distel, Oliver Pusch, Christian Schöfer, Senescence-associated ß-galactosidase staining over the lifespan differs in a short- and a long-lived fish species , European Journal of Histochemistry: Vol. 68 No. 1 (2024): 1954-2024: 70 Years of Histochemical Research
<< < 1 2 3 4 5 6 7 8 9 10 > >>
You may also start an advanced similarity search for this article.
