BMC Neuroscience | |
Social stress increases expression of hemoglobin genes in mouse prefrontal cortex | |
Paweł Lisowski1  Grzegorz R Juszczak3  Marek Wieczorek6  Alicja Majewska4  Artur H Swiergiel5  Joanna Goscik2  Adrian M Stankiewicz3  | |
[1] iPS Cell-Based Disease Modeling Group, Max-Delbrück-Center for Molecular Medicine (MDC) in the Helmholtz Association, Berlin, 13092, Germany;Faculty of Computer Science, Bialystok University of Technology, Wiejska 45A, Bialystok, 15-351, Poland;Department of Animal Behavior, Institute of Genetics and Animal Breeding, Jastrzebiec, ul. Postepu 36A, Magdalenka, 05-552, Poland;Department of Physiological Sciences, Faculty of Veterinary Medicine, Warsaw University of Life Sciences, Warsaw, Poland;Department of Human and Animal Physiology, Institute of Biology, University of Gdansk, Gdansk, 80-308, Poland;Department of Neurobiology, Faculty of Biology and Environmental Protection, University of Lodz, 90-236 Lodz, Pomorska 141/143, Poland | |
关键词: Social stress; Prefrontal cortex; Expression; Gene; Microarray; | |
Others : 1090334 DOI : 10.1186/s12868-014-0130-6 |
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received in 2014-05-10, accepted in 2014-11-18, 发布年份 2014 | |
【 摘 要 】
Background
In order to better understand the effects of social stress on the prefrontal cortex, we investigated gene expression in mice subjected to acute and repeated social encounters of different duration using microarrays.
Results
The most important finding was identification of hemoglobin genes (Hbb-b1, Hbb-b2, Hba-a1, Hba-a2, Beta-S) as potential markers of chronic social stress in mice. Expression of these genes was progressively increased in animals subjected to 8 and 13 days of repeated stress and was correlated with altered expression of Mgp (Mglap), Fbln1, 1500015O10Rik (Ecrg4), SLC16A10, and Mndal. Chronic stress increased also expression of Timp1 and Ppbp that are involved in reaction to vascular injury. Acute stress did not affect expression of hemoglobin genes but it altered expression of Fam107a (Drr1) and Agxt2l1 (Etnppl) that have been implicated in psychiatric diseases.
Conclusions
The observed up-regulation of genes associated with vascular system and brain injury suggests that stressful social encounters may affect brain function through the stress-induced dysfunction of the vascular system.
【 授权许可】
2014 Stankiewicz et al.; licensee BioMed Central Ltd.
【 预 览 】
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【 参考文献 】
- [1]Snyder BK, Roghmann KJ, Sigal LH: Stress and psychosocial factors: effects on primary cellular immune response. J Behav Med 1993, 16(2):143-161.
- [2]Lee DJ, Meehan RT, Robinson C, Smith ML, Mabry TR: Psychosocial correlates of immune responsiveness and illness episodes in US Air Force Academy cadets undergoing basic cadet training. J Psychosom Res 1995, 39(4):445-457.
- [3]Glaser R, Pearson GR, Bonneau RH, Esterling BA, Atkinson C, Kiecolt-Glaser JK: Stress and the memory T-cell response to the Epstein-Barr virus in healthy medical students. Health Psychol 1993, 12(6):435-442.
- [4]Weinberg A, Creed F: Stress and psychiatric disorder in healthcare professionals and hospital staff. Lancet 2000, 355(9203):533-537.
- [5]Dunn AJ, Swiergiel AH: The role of corticotropin-releasing factor and noradrenaline in stress-related responses, and the inter-relationships between the two systems. Eur J Pharmacol 2008, 583(2–3):186-193.
- [6]Pickering TG: Mental stress as a causal factor in the development of hypertension and cardiovascular disease. Curr Hypertens Rep 2001, 3(3):249-254.
- [7]Rozanski A, Blumenthal JA, Kaplan J: Impact of psychological factors on the pathogenesis of cardiovascular disease and implications for therapy. Circulation 1999, 99(16):2192-2217.
- [8]Courtin J, Chaudun F, Rozeske RR, Karalis N, Gonzalez-Campo C, Wurtz H, Abdi A, Baufreton J, Bienvenu TC, Herry C: Prefrontal parvalbumin interneurons shape neuronal activity to drive fear expression. Nature 2014, 505(7481):92-96.
- [9]Likhtik E, Stujenske JM, Topiwala MA, Harris AZ, Gordon JA: Prefrontal entrainment of amygdala activity signals safety in learned fear and innate anxiety. Nat Neurosci 2014, 17(1):106-113.
- [10]Bourne AR, Mohan G, Stone MF, Pham MQ, Schultz CR, Meyerhoff JL, Lumley LA: Olfactory cues increase avoidance behavior and induce Fos expression in the amygdala, hippocampus and prefrontal cortex of socially defeated mice. Behav Brain Res 2013, 256:188-196.
- [11]Singh R: Signal oscillation is another reason for variability in microarray-based gene expression quantification. PLoS One 2013, 8(1):e54753.
- [12]Shippy R, Sendera TJ, Lockner R, Palaniappan C, Kaysser-Kranich T, Watts G, Alsobrook J: Performance evaluation of commercial short-oligonucleotide microarrays and the impact of noise in making cross-platform correlations. BMC Genomics 2004, 5:61.
- [13]Scherer A, Dai M, Meng F: Impact of experimental noise and annotation imprecision on data quality in microarray experiments. Methods Mol Biol 2013, 972:155-176.
- [14]LaCroix-Fralish ML, Austin JS, Zheng FY, Levitin DJ, Mogil JS: Patterns of pain: meta-analysis of microarray studies of pain. Pain 2011, 152(8):1888-1898.
- [15]Klebanov L, Qiu X, Welle S, Yakovlev A: Statistical methods and microarray data. Nat Biotechnol 2007, 25(1):25-26. author reply 26–27
- [16]van der Staay FJ, Schuurman T, Hulst M, Smits M, Prickaerts J, Kenis G, Korte SM: Effects of chronic stress: a comparison between tethered and loose sows. Physiol Behav 2010, 100(2):154-164.
- [17]Li XH, Chen JX, Yue GX, Liu YY, Zhao X, Guo XL, Liu Q, Jiang YM, Bai MH: Gene expression profile of the hippocampus of rats subjected to chronic immobilization stress. PLoS One 2013, 8(3):e57621.
- [18]Swiergiel AH, Smagin GN, Johnson LJ, Dunn AJ: The role of cytokines in the behavioral responses to endotoxin and influenza virus infection in mice: effects of acute and chronic administration of the interleukin-1-receptor antagonist (IL-1ra). Brain Res 1997, 776(1–2):96-104.
- [19]Litvin Y, Blanchard DC, Pentkowski NS, Blanchard RJ: A pinch or a lesion: a reconceptualization of biting consequences in mice. Aggress Behav 2007, 33(6):545-551.
- [20]Kudryavtseva NN, Bondar NP, Alekseyenko OV: Behavioral correlates of learned aggression in male mice. Aggress Behav 2000, 26:386-400.
- [21]Selye H: A syndrome produced by diverse nocuous agents. Nature 1936, 138:32.
- [22]Engler H, Bailey MT, Engler A, Stiner-Jones LM, Quan N, Sheridan JF: Interleukin-1 receptor type 1-deficient mice fail to develop social stress-associated glucocorticoid resistance in the spleen. Psychoneuroendocrinology 2008, 33(1):108-117.
- [23]Blanchard DC, Sakai RR, McEwen B, Weiss SM, Blanchard RJ: Subordination stress: behavioral, brain, and neuroendocrine correlates. Behav Brain Res 1993, 58(1–2):113-121.
- [24]Ling S, Jamali F: Effect of cannulation surgery and restraint stress on the plasma corticosterone concentration in the rat: application of an improved corticosterone HPLC assay. J Pharm Pharm Sci 2003, 6(2):246-251.
- [25]Paxinos G, Franklin KBJ: The Mouse Brain in Stereotaxic Coordinates. 2nd edition. Academic Press, San Diego; 2001.
- [26]Pfaffl MW: A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29(9):e45.
- [27]Hancock AA, Bush EN, Stanisic D, Kyncl JJ, Lin CT: Data normalization before statistical analysis: keeping the horse before the cart. Trends Pharmacol Sci 1988, 9(1):29-32.
- [28]Yuan JS, Reed A, Chen F, Stewart CN Jr: Statistical analysis of real-time PCR data. BMC Bioinformatics 2006, 7:85.
- [29]Datson NA, Speksnijder N, Mayer JL, Steenbergen PJ, Korobko O, Goeman J, de Kloet ER, Joels M, Lucassen PJ: The transcriptional response to chronic stress and glucocorticoid receptor blockade in the hippocampal dentate gyrus. Hippocampus 2012, 22(2):359-371.
- [30]Smyth GK: Limma: Linear Models for Microarray Data. In Bioinformatics and Computational Biology Solutions Using R and Bioconductor. Edited by Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W. Springer, New York; 2005:397-420.
- [31]Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, Holloway A, Smyth GK: A comparison of background correction methods for two-colour microarrays. Bioinformatics 2007, 23(20):2700-2707.
- [32]Smyth GK, Speed T: Normalization of cDNA microarray data. Methods 2003, 31(4):265-273.
- [33]Benjamini Y, Hochberg Y: Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc B 1995, 57(1):289-300.
- [34]Saldanha AJ: Java treeview–extensible visualization of microarray data. Bioinformatics 2004, 20(17):3246-3248.
- [35]Michener CD, Sokal RR: A quantitative approach to a problem of classification. Evolution 1957, 11:490-499.
- [36]Selye H: Thymus and adrenals in the response of the organism to injuries and intoxications. Br J Exp Pathol 1936, 17(3):234-248.
- [37]Dominguez-Gerpe L, Rey-Mendez M: Time-course of the murine lymphoid tissue involution during and following stressor exposure. Life Sci 1997, 61(10):1019-1027.
- [38]Pertsov SS: Effect of melatonin on the thymus, adrenal glands, and spleen in rats during acute stress. Bull Exp Biol Med 2006, 141(3):292-295.
- [39]Wohleb ES, Powell ND, Godbout JP, Sheridan JF: Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior. J Neurosci 2013, 33(34):13820-13833.
- [40]Hanke ML, Powell ND, Stiner LM, Bailey MT, Sheridan JF: Beta adrenergic blockade decreases the immunomodulatory effects of social disruption stress. Brain Behav Immun 2012, 26(7):1150-1159.
- [41]Maniam J, Morris MJ: The link between stress and feeding behaviour. Neuropharmacology 2012, 63(1):97-110.
- [42]Lisowski P, Juszczak GR, Goscik J, Wieczorek M, Zwierzchowski L, Swiergiel AH: Effect of chronic mild stress on hippocampal transcriptome in mice selected for high and low stress-induced analgesia and displaying different emotional behaviors. Eur Neuropsychopharmacol 2011, 21(1):45-62.
- [43]Lisowski P, Wieczorek M, Goscik J, Juszczak GR, Stankiewicz AM, Zwierzchowski L, Swiergiel AH: Effects of chronic stress on prefrontal cortex transcriptome in mice displaying different genetic backgrounds. J Mol Neurosci 2013, 50(1):33-57.
- [44]Tordera RM, Garcia-Garcia AL, Elizalde N, Segura V, Aso E, Venzala E, Ramirez MJ, Del Rio J: Chronic stress and impaired glutamate function elicit a depressive-like phenotype and common changes in gene expression in the mouse frontal cortex. Eur Neuropsychopharmacol 2011, 21(1):23-32.
- [45]Orsetti M, Di Brisco F, Canonico PL, Genazzani AA, Ghi P: Gene regulation in the frontal cortex of rats exposed to the chronic mild stress paradigm, an animal model of human depression. Eur J Neurosci 2008, 27(8):2156-2164.
- [46]Andrus BM, Blizinsky K, Vedell PT, Dennis K, Shukla PK, Schaffer DJ, Radulovic J, Churchill GA, Redei EE: Gene expression patterns in the hippocampus and amygdala of endogenous depression and chronic stress models. Mol Psychiatry 2012, 17(1):49-61.
- [47]Aso E, Ozaita A, Serra MA, Maldonado R: Genes differentially expressed in CB1 knockout mice: involvement in the depressive-like phenotype. Eur Neuropsychopharmacol 2011, 21(1):11-22.
- [48]Benatti C, Valensisi C, Blom JM, Alboni S, Montanari C, Ferrari F, Tagliafico E, Mendlewicz J, Brunello N, Tascedda F: Transcriptional profiles underlying vulnerability and resilience in rats exposed to an acute unavoidable stress. J Neurosci Res 2012, 90(11):2103-2115.
- [49]Mingmalairak S, Tohda M, Murakami Y, Matsumoto K: Possible involvement of signal transducers and activators of transcription 3 system on depression in the model mice brain. Biol Pharm Bull 2010, 33(4):636-640.
- [50]Barreto RA, Walker FR, Dunkley PR, Day TA, Smith DW: Fluoxetine prevents development of an early stress-related molecular signature in the rat infralimbic medial prefrontal cortex. Implications for depression? BMC Neurosci 2012, 13:125.
- [51]Poh KW, Yeo JF, Stohler CS, Ong WY: Comprehensive gene expression profiling in the prefrontal cortex links immune activation and neutrophil infiltration to antinociception. J Neurosci 2012, 32(1):35-45.
- [52]Richter F, Meurers BH, Zhu C, Medvedeva VP, Chesselet MF: Neurons express hemoglobin alpha- and beta-chains in rat and human brains. J Comp Neurol 2009, 515(5):538-547.
- [53]He Y, Hua Y, Lee JY, Liu W, Keep RF, Wang MM, Xi G: Brain alpha- and beta-globin expression after intracerebral hemorrhage. Transl Stroke Res 2010, 1(1):48-56.
- [54]Schelshorn DW, Schneider A, Kuschinsky W, Weber D, Kruger C, Dittgen T, Burgers HF, Sabouri F, Gassler N, Bach A, Maurer MH: Expression of hemoglobin in rodent neurons. J Cereb Blood Flow Metab 2009, 29(3):585-595.
- [55]Biagioli M, Pinto M, Cesselli D, Zaninello M, Lazarevic D, Roncaglia P, Simone R, Vlachouli C, Plessy C, Bertin N, Beltrami A, Kobayashi K, Gallo V, Santoro C, Ferrer I, Rivella S, Beltrami CA, Carninci P, Raviola E, Gustincich S: Unexpected expression of alpha- and beta-globin in mesencephalic dopaminergic neurons and glial cells. Proc Natl Acad Sci U S A 2009, 106(36):15454-15459.
- [56]Gelman JS, Sironi J, Castro LM, Ferro ES, Fricker LD: Hemopressins and other hemoglobin-derived peptides in mouse brain: comparison between brain, blood, and heart peptidome and regulation in Cpefat/fat mice. J Neurochem 2010, 113(4):871-880.
- [57]Sarlus H, Wang X, Cedazo-Minguez A, Schultzberg M, Oprica M: Chronic airway-induced allergy in mice modifies gene expression in the brain toward insulin resistance and inflammatory responses. J Neuroinflammation 2013, 10:99.
- [58]He Y, Hua Y, Liu W, Hu H, Keep RF, Xi G: Effects of cerebral ischemia on neuronal hemoglobin. J Cereb Blood Flow Metab 2009, 29(3):596-605.
- [59]Burger C, Lopez MC, Baker HV, Mandel RJ, Muzyczka N: Genome-wide analysis of aging and learning-related genes in the hippocampal dentate gyrus. Neurobiol Learn Mem 2008, 89(4):379-396.
- [60]Ince B, Guloksuz S, Altinbas K, Oral ET, Alpkan LR, Altinoz MA: Minor hemoglobins HbA2 and HbF associate with disease severity in bipolar disorder with a likely protective role of HbA2 against post-partum episodes. J Affect Disord 2013, 151(1):405-408.
- [61]Ramos-Cejudo J, Gutierrez-Fernandez M, Rodriguez-Frutos B, Exposito Alcaide M, Sanchez-Cabo F, Dopazo A, Diez-Tejedor E: Spatial and temporal gene expression differences in core and periinfarct areas in experimental stroke: a microarray analysis. PLoS One 2012, 7(12):e52121.
- [62]Choi YG, Yeo S, Hong YM, Kim SH, Lim S: Changes of gene expression profiles in the cervical spinal cord by acupuncture in an MPTP-intoxicated mouse model: microarray analysis. Gene 2011, 481(1):7-16.
- [63]Takagi Y, Aoki T, Takahashi JC, Yoshida K, Ishii A, Arakawa Y, Kikuchi T, Funaki T, Miyamoto S: Differential gene expression in relation to the clinical characteristics of human brain arteriovenous malformations. Neurol Med Chir (Tokyo) 2014, 54(3):163-175.
- [64]Price PA, Urist MR, Otawara Y: Matrix Gla protein, a new gamma-carboxyglutamic acid-containing protein which is associated with the organic matrix of bone. Biochem Biophys Res Commun 1983, 117(3):765-771.
- [65]Hale JE, Fraser JD, Price PA: The identification of matrix Gla protein in cartilage. J Biol Chem 1988, 263(12):5820-5824.
- [66]Wallin R, Cain D, Sane DC: Matrix Gla protein synthesis and gamma-carboxylation in the aortic vessel wall and proliferating vascular smooth muscle cells–a cell system which resembles the system in bone cells. Thromb Haemost 1999, 82(6):1764-1767.
- [67]Farzaneh-Far A, Proudfoot D, Weissberg PL, Shanahan CM: Matrix gla protein is regulated by a mechanism functionally related to the calcium-sensing receptor. Biochem Biophys Res Commun 2000, 277(3):736-740.
- [68]Shanahan CM, Cary NR, Metcalfe JC, Weissberg PL: High expression of genes for calcification-regulating proteins in human atherosclerotic plaques. J Clin Invest 1994, 93(6):2393-2402.
- [69]Proudfoot D, Skepper JN, Shanahan CM, Weissberg PL: Calcification of human vascular cells in vitro is correlated with high levels of matrix Gla protein and low levels of osteopontin expression. Arterioscler Thromb Vasc Biol 1998, 18(3):379-388.
- [70]Lomashvili KA, Wang X, Wallin R, O’Neill WC: Matrix Gla protein metabolism in vascular smooth muscle and role in uremic vascular calcification. J Biol Chem 2011, 286(33):28715-28722.
- [71]Mustonen E, Pohjolainen V, Aro J, Pikkarainen S, Leskinen H, Ruskoaho H, Rysa J: Upregulation of cardiac matrix Gla protein expression in response to hypertrophic stimuli. Blood Press 2009, 18(5):286-293.
- [72]Godyna S, Diaz-Ricart M, Argraves WS: Fibulin-1 mediates platelet adhesion via a bridge of fibrinogen. Blood 1996, 88(7):2569-2577.
- [73]Tran H, Tanaka A, Litvinovich SV, Medved LV, Haudenschild CC, Argraves WS: The interaction of fibulin-1 with fibrinogen. A potential role in hemostasis and thrombosis. J Biol Chem 1995, 270(33):19458-19464.
- [74]Tran H, VanDusen WJ, Argraves WS: The self-association and fibronectin-binding sites of fibulin-1 map to calcium-binding epidermal growth factor-like domains. J Biol Chem 1997, 272(36):22600-22606.
- [75]Argraves WS, Tanaka A, Smith EP, Twal WO, Argraves KM, Fan D, Haudenschild CC: Fibulin-1 and fibrinogen in human atherosclerotic lesions. Histochem Cell Biol 2009, 132(5):559-565.
- [76]Ghasemzadeh M, Kaplan ZS, Alwis I, Schoenwaelder SM, Ashworth KJ, Westein E, Hosseini E, Salem HH, Slattery R, McColl SR, Hickey MJ, Ruggeri ZM, Yuan Y, Jackson SP: The CXCR1/2 ligand NAP-2 promotes directed intravascular leukocyte migration through platelet thrombi. Blood 2013, 121(22):4555-4566.
- [77]Fujimoto M, Takagi Y, Aoki T, Hayase M, Marumo T, Gomi M, Nishimura M, Kataoka H, Hashimoto N, Nozaki K: Tissue inhibitor of metalloproteinases protect blood–brain barrier disruption in focal cerebral ischemia. J Cereb Blood Flow Metab 2008, 28(10):1674-1685.
- [78]Rosell A, Vilalta A, Garcia-Berrocoso T, Fernandez-Cadenas I, Domingues-Montanari S, Cuadrado E, Delgado P, Ribo M, Martinez-Saez E, Ortega-Aznar A, Montaner J: Brain perihematoma genomic profile following spontaneous human intracerebral hemorrhage. PLoS One 2011, 6(2):e16750.
- [79]Lijnen HR, Soloway P, Collen D: Tissue inhibitor of matrix metalloproteinases-1 impairs arterial neointima formation after vascular injury in mice. Circ Res 1999, 85(12):1186-1191.
- [80]Aoki T, Kataoka H, Moriwaki T, Nozaki K, Hashimoto N: Role of TIMP-1 and TIMP-2 in the progression of cerebral aneurysms. Stroke 2007, 38(8):2337-2345.
- [81]Yokota H, Yoshikawa M, Hirabayashi H, Nakase H, Uranishi R, Nishimura F, Sugie Y, Ishizaka S, Sakaki T: Expression of ciliary neurotrophic factor (CNTF), CNTF receptor alpha (CNTFR-alpha) following experimental intracerebral hemorrhage in rats. Neurosci Lett 2005, 377(3):170-175.
- [82]Choi JS, Kim SY, Park HJ, Cha JH, Choi YS, Chung JW, Chun MH, Lee MY: Differential regulation of ciliary neurotrophic factor and its receptor in the rat hippocampus in response to kainic acid-induced excitotoxicity. Mol Cells 2004, 17(2):292-296.
- [83]Miotke JA, MacLennan AJ, Meyer RL: Immunohistochemical localization of CNTFRalpha in adult mouse retina and optic nerve following intraorbital nerve crush: evidence for the axonal loss of a trophic factor receptor after injury. J Comp Neurol 2007, 500(2):384-400.
- [84]Ozog MA, Modha G, Church J, Reilly R, Naus CC: Co-administration of ciliary neurotrophic factor with its soluble receptor protects against neuronal death and enhances neurite outgrowth. J Biol Chem 2008, 283(10):6546-6560.
- [85]Lee N, Robitz R, Zurbrugg RJ, Karpman AM, Mahler AM, Cronier SA, Vesey R, Spearry RP, Zolotukhin S, Maclennan AJ: Conditional, genetic disruption of ciliary neurotrophic factor receptors reveals a role in adult motor neuron survival. Eur J Neurosci 2008, 27(11):2830-2837.
- [86]Podvin S, Gonzalez AM, Miller MC, Dang X, Botfield H, Donahue JE, Kurabi A, Boissaud-Cooke M, Rossi R, Leadbeater WE, Johanson CE, Coimbra R, Stopa EG, Eliceiri BP, Baird A: Esophageal cancer related gene-4 is a choroid plexus-derived injury response gene: evidence for a biphasic response in early and late brain injury. PLoS One 2011, 6(9):e24609.
- [87]Shaterian A, Kao S, Chen L, DiPietro LA, Coimbra R, Eliceiri BP, Baird A: The candidate tumor suppressor gene Ecrg4 as a wound terminating factor in cutaneous injury. Arch Dermatol Res 2013, 305(2):141-149.
- [88]Kujuro Y, Suzuki N, Kondo T: Esophageal cancer-related gene 4 is a secreted inducer of cell senescence expressed by aged CNS precursor cells. Proc Natl Acad Sci U S A 2010, 107(18):8259-8264.
- [89]Gao J, Yang H, Chen J, Fang J, Chen C, Liang R, Yang G, Wu H, Wu C, Li S: Analysis of serum metabolites for the discovery of amino acid biomarkers and the effect of galangin on cerebral ischemia. Mol Biosyst 2013, 9(9):2311-2321.
- [90]Zhang K, Kagan D, DuBois W, Robinson R, Bliskovsky V, Vass WC, Zhang S, Mock BA: Mndal, a new interferon-inducible family member, is highly polymorphic, suppresses cell growth, and may modify plasmacytoma susceptibility. Blood 2009, 114(14):2952-2960.
- [91]Kass DJ, Yu G, Loh KS, Savir A, Borczuk A, Kahloon R, Juan-Guardela B, Deiuliis G, Tedrow J, Choi J, Richards T, Kaminski N, Greenberg SM: Cytokine-like factor 1 gene expression is enriched in idiopathic pulmonary fibrosis and drives the accumulation of CD4+ T cells in murine lungs: evidence for an antifibrotic role in bleomycin injury. Am J Pathol 2012, 180(5):1963-1978.
- [92]Jia J, Dai M, Zhuang Y: E proteins are required to activate germline transcription of the TCR Vbeta8.2 gene. Eur J Immunol 2008, 38(10):2806-2820.
- [93]Vianna DM, Carrive P: Cardiovascular and behavioural responses to conditioned fear and restraint are not affected by retrograde lesions of A5 and C1 bulbospinal neurons. Neuroscience 2010, 166(4):1210-1218.
- [94]Busnardo C, Tavares RF, Resstel LB, Elias LL, Correa FM: Paraventricular nucleus modulates autonomic and neuroendocrine responses to acute restraint stress in rats. Auton Neurosci 2010, 158(1–2):51-57.
- [95]Bernatowa I, Csizmadiova Z, Kopincova J, Puzserova A: Vascular function and nitric oxide production in chronic social-stress-exposed rats with various family history of hypertension. J Physiol Pharmacol 2007, 58(3):487-501.
- [96]Snieder H, Harshfield GA, Barbeau P, Pollock DM, Pollock JS, Treiber FA: Dissecting the genetic architecture of the cardiovascular and renal stress response. Biol Psychol 2002, 61(1–2):73-95.
- [97]Skantze HB, Kaplan J, Pettersson K, Manuck S, Blomqvist N, Kyes R, Williams K, Bondjers G: Psychosocial stress causes endothelial injury in cynomolgus monkeys via beta1-adrenoceptor activation. Atherosclerosis 1998, 136(1):153-161.
- [98]Jezova D, Kristova V, Slamova J, Mlynarik M, Pirnik Z, Kiss A, Kriska M: Stress-induced rise in endothelaemia, von Willebrand factor and hypothalamic-pituitary-adrenocortical axis activation is reduced by pretreatment with pentoxifylline. J Physiol Pharmacol 2003, 54(3):329-338.
- [99]Sherwood A, Johnson K, Blumenthal JA, Hinderliter AL: Endothelial function and hemodynamic responses during mental stress. Psychosom Med 1999, 61(3):365-370.
- [100]Ghiadoni L, Donald AE, Cropley M, Mullen MJ, Oakley G, Taylor M, O’Connor G, Betteridge J, Klein N, Steptoe A, Deanfield JE: Mental stress induces transient endothelial dysfunction in humans. Circulation 2000, 102(20):2473-2478.
- [101]Bink DI, Ritz K, Aronica E, van der Weerd L, Daemen MJ: Mouse models to study the effect of cardiovascular risk factors on brain structure and cognition. J Cereb Blood Flow Metab 2013, 33(11):1666-1684.
- [102]Pires PW, Dams Ramos CM, Matin N, Dorrance AM: The effects of hypertension on the cerebral circulation. Am J Physiol Heart Circ Physiol 2013, 304(12):H1598-H1614.
- [103]Liebl C, Panhuysen M, Putz B, Trumbach D, Wurst W, Deussing JM, Muller MB, Schmidt MV: Gene expression profiling following maternal deprivation: involvement of the brain renin-angiotensin system. Front Mol Neurosci 2009, 2:1.
- [104]Veiga-da-Cunha M, Hadi F, Balligand T, Stroobant V, Van Schaftingen E: Molecular identification of hydroxylysine kinase and of ammoniophospholyases acting on 5-phosphohydroxy-L-lysine and phosphoethanolamine. J Biol Chem 2012, 287(10):7246-7255.
- [105]Schmidt MV, Schulke JP, Liebl C, Stiess M, Avrabos C, Bock J, Wochnik GM, Davies HA, Zimmermann N, Scharf SH, Trumbach D, Wurst W, Zieglgansberger W, Turck C, Holsboer F, Stewart MG, Bradke F, Eder M, Muller MB, Rein T: Tumor suppressor down-regulated in renal cell carcinoma 1 (DRR1) is a stress-induced actin bundling factor that modulates synaptic efficacy and cognition. Proc Natl Acad Sci U S A 2011, 108(41):17213-17218.
- [106]Masana M, Su YA, Liebl C, Wang XD, Jansen L, Westerholz S, Wagner KV, Labermaier C, Scharf SH, Santarelli S, Hartmann J, Schmidt MV, Rein T, Muller MB: The stress-inducible actin-interacting protein DRR1 shapes social behavior. Psychoneuroendocrinology 2014, 48:98-110.
- [107]Kim S, Choi KH, Baykiz AF, Gershenfeld HK: Suicide candidate genes associated with bipolar disorder and schizophrenia: an exploratory gene expression profiling analysis of post-mortem prefrontal cortex. BMC Genomics 2007, 8:413.
- [108]Shao L, Vawter MP: Shared gene expression alterations in schizophrenia and bipolar disorder. Biol Psychiatry 2008, 64(2):89-97.
- [109]McQuillin A, Rizig M, Gurling HM: A microarray gene expression study of the molecular pharmacology of lithium carbonate on mouse brain mRNA to understand the neurobiology of mood stabilization and treatment of bipolar affective disorder. Pharmacogenet Genomics 2007, 17(8):605-617.
- [110]Carr CP, Martins CM, Stingel AM, Lemgruber VB, Juruena MF: The role of early life stress in adult psychiatric disorders: a systematic review according to childhood trauma subtypes. J Nerv Ment Dis 2013, 201(12):1007-1020.
- [111]Lederbogen F, Haddad L, Meyer-Lindenberg A: Urban social stress–risk factor for mental disorders. The case of schizophrenia. Environ Pollut 2013, 183:2-6.
- [112]Bratlien U, Oie M, Haug E, Moller P, Andreassen OA, Lien L, Melle I: Environmental factors during adolescence associated with later development of psychotic disorders - a nested case–control study. Psychiatry Res 2014, 215(3):579-585.
- [113]Flicek P, Ahmed I, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, Fitzgerald S, Gil L, Garcia-Giron C, Gordon L, Hourlier T, Hunt S, Juettemann T, Kahari AK, Keenan S, Komorowska M, Kulesha E, Longden I, Maurel T, McLaren WM, Muffato M, Nag R, Overduin B, Pignatelli M, Pritchard B, Pritchard E: Ensembl 2013. Nucleic Acids Res 2013, 41(Database issue):D48-D55.
- [114]Paulsen SJ, Larsen LK, Jelsing J, Janssen U, Gerstmayer B, Vrang N: Gene expression profiling of individual hypothalamic nuclei from single animals using laser capture microdissection and microarrays. J Neurosci Methods 2009, 177(1):87-93.
- [115]Lauridsen JB, Johansen JL, Rekling JC, Thirstrup K, Moerk A, Sager TN: Regulation of the Bcas1 and Baiap3 transcripts in the subthalamic nucleus in mice recovering from MPTP toxicity. Neurosci Res 2011, 70(3):269-276.