Visual Universitätsmedizin Mainz

Publications 2017

Lerner R, Post J, Loch S, Lutz B, Bindila L (2017) Targeting brain and peripheral plasticity of the lipidome in acute kainic acid-induced epileptic seizures in mice via quantitative mass spectrometry. Biochim Biophys Acta 1862: 255-267

Lomazzo E, König F, Abassi L, Jelinek R, Lutz B (2017) Chronic stress leads to epigenetic dysregulation in the neuropeptide-Y and cannabinoid CB1 receptor genes in the mouse cingulate cortex. Neuropharmacology 113: 301-313

Lange MD, Daldrup T, Remmers F, Szkudlarek HJ, Lesting J, Guggenhuber S, Ruehle S, Jüngling K, Seidenbecher T, Lutz B, Pape HC. (2017) Cannabinoid CB1 receptors in distinct circuits of the extended amygdala determine fear responsiveness to unpredictable threat. Mol Psychiatry  2016 Oct 4. doi: 10.1038/mp.2016.156. [Epub ahead of print]

Gutiérrez-Rodríguez A, Puente N, Elezgarai I, Ruehle S, Lutz B, Reguero L, Gerrikagoitia I, Marsicano G, Grandes P (2017) Anatomical characterization of the cannabinoid CB1 receptor in cell-type-specific mutant mouse rescue models. J Comp Neurol 525: 302-318

Moreno E, Chiarlone A, Medrano M, Puigdellívol M, Bibic L, Howell L, Resel E, Puente N, Casarejos MJ, Perucho J, Botta J, Suelves N, Ciruela F, Ginés S, Galve-Roperh I, Casadó V, Grandes P, Lutz B, Monory K, Canela EI, Lluís C, McCormick PJ, Guzmán M (2017) Singular Location and Signaling Profile of Adenosine A2A-Cannabinoid CB1 Receptor Heteromers in the Dorsal Striatum. Neuropsychopharmacology, 2017 Jan 19. doi: 10.1038/npp.2017.12. [Epub ahead of print]

Publications 2016

Vogt J, Kirischuk S, Unichenko P, Schlüter L, Pelosi A, Endle H, Yang JW, Schmarowski N, Cheng J, Thalman C, Strauss U, Prokudin A, Bharati BS, Aoki J, Chun J, Lutz B, Luhmann HJ, Nitsch R (2016) Synaptic Phospholipid Signaling Modulates Axon Outgrowth via Glutamate-dependent Ca2+-mediated Molecular Pathways. Cereb Cortex 1-15

Biedermann SV, Auer MK, Bindila L, Ende G, Lutz B, Weber-Fahr W, Gass P, Fuss J (2016) Restricted vs. unrestricted wheel running in mice: Effects on brain, behavior and endocannabinoids. Horm Behav 86: 45-54

Zimmermann T, Remmers F, Lutz B, Leschik J (2016) ESC-Derived BDNF-Overexpressing Neural Progenitors Differentially Promote Recovery in Huntington's Disease Models by Enhanced Striatal Differentiation. Stem Cell Reports 7: 693-706

Mattheus T, Kukla K, Zimmermann T, Tenzer S, Lutz B (2016) Cell Type-Specific Tandem Affinity Purification of the Mouse Hippocampal CB1 Receptor-Associated Proteome. J Proteome Res 15: 3585-3601

Schneider P, Bindila L, Schmahl C, Bohus M, Meyer-Lindenberg A, Lutz B, Spanagel R, Schneider M (2016) Adverse Social Experiences in Adolescent Rats Result in Enduring Effects on Social Competence, Pain Sensitivity and Endocannabinoid Signaling. Front Behav Neurosci 10:203

Gentile A, Fresegna D, Musella A, Sepman H, Bullitta S, De Vito F, Fantozzi R, Usiello A, Maccarrone M, Mercuri NB, Lutz B, Mandolesi G, Centonze D (2016) Interaction between interleukin-1β and type-1 cannabinoid receptor is involved in anxiety-like behavior in experimental autoimmune encephalomyelitis. J Neuroinflammation 13: 231

Busquets-Garcia A, Gomis-González M, Srivastava RK, Cutando L, Ortega-Alvaro A, Ruehle S, Remmers F, Bindila L, Bellocchio L, Marsicano G, Lutz B, Maldonado R, Ozaita A (2016) Peripheral and central CB1 cannabinoid receptors control stress-induced impairment of memory consolidation. Proc Natl Acad Sci U S A 113: 9904-9

Bindila L, Lutz B (2016) Extraction and Simultaneous Quantification of Endocannabinoids and Endocannabinoid-Like Lipids in Biological Tissues. Methods Mol Biol 1412: 9-18

Feliszek M, Bindila L, Lutz B, Zimmer A, Bilkei-Gorzo A, Schlicker E (2016) Lack of hippocampal CB1 receptor desensitization by Δ(9)-tetrahydrocannabinol in aged mice and by low doses of JZL 184. Naunyn Schmiedebergs Arch Pharmacol 389: 603-12

Jenniches I, Ternes S, Albayram O, Otte DM, Bach K, Bindila L, Michel K, Lutz B, Bilkei-Gorzo A, Zimmer A (2016) Anxiety, Stress, and Fear Response in Mice With Reduced Endocannabinoid Levels. Biol Psychiatry 79: 858-68

Guggenhuber S, Alpar A, Chen R, Schmitz N, Wickert M, Mattheus T, Harasta AE, Purrio M, Kaiser N, Elphick MR, Monory K, Kilb W, Luhmann HJ, Harkany T, Lutz B, Klugmann M (2015) Cannabinoid receptor-interacting protein Crip1a modulates CB1 receptor signaling in mouse hippocampus. Brain Struct Funct 221: 2061-74

Maroso M, Szabo GG, Kim HK, Alexander A, Bui AD, Lee SH, Lutz B, Soltesz I (2016) Cannabinoid Control of Learning and Memory through HCN Channels. Neuron 89: 1059-73

Guggenhuber S, Romo-Parra H, Bindila L, Leschik J, Lomazzo E, Remmers F, Zimmermann T, Lerner R, Klugmann M, Pape HC, Lutz B (2016) Impaired 2-AG Signaling in Hippocampal Glutamatergic Neurons: Aggravation of Anxiety-Like Behavior and Unaltered Seizure Susceptibility. Int J Neuropsychopharmacol 19: 1-13

Seifert B, Eckenstaler R, Rönicke R, Leschik J, Lutz B, Reymann K, Lessmann V, Brigadski T (2016) Amyloid-Beta Induced Changes in Vesicular Transport of BDNF in Hippocampal Neurons. Neural Plast 2016: 4145708

Ramírez-López MT, Vázquez M, Bindila L, Lomazzo E, Hofmann C, Blanco RN, Alén, Antón M, Decara J, Ouro D, Orio L, Suarez J, Lutz B, Rodríguez de Fonseca F, Gómez de Heras R (2016) Exposure to a Highly Caloric Palatable Diet During Pregestational and Gestational Periods Affects Hypothalamic and Hippocampal Endocannabinoid Levels at Birth and Induces Adiposity and Anxiety-Like Behaviors in Male Rat Offspring. Front Behav Neurosci 9:339.

Butenschön J, Zimmermann T, Schmarowski N, Nitsch R, Fackelmeier B, Friedemann K, Radyushkin K, Baumgart J, Lutz B, Leschik J (2016) PSA-NCAM positive neural progenitors stably expressing BDNF promote functional recovery in a mouse model of spinal cord injury. Stem Cell Res Ther 7:11.

Jehle J, Hoyer FF, Schöne B, Pfeifer P, Schild K, Jenniches I, Bindila L, Lutz B, Lütjohann D, Zimmer A, Nickenig G (2016) Myeloid-Specific Deletion of Diacylglycerol Lipase α Inhibits Atherogenesis in ApoE-Deficient Mice. PLoS One 11:e0146267.

Publications 2015

Hoegberg BG, Lomazzo E, Lee NH, Perry DC (2015) Regulation of α4β2α5 nicotinic acetylcholinergic receptors in rat cerebral cortex in early and late adolescence: Sex differences in response to chronic nicotine. Neuropharmacology 99:347-355.

Kronfeld A, Buchholz HG, Maus S, Reuss S, Müller-Forell W, Lutz B, Schreckenberger M, Miederer I (2015) Evaluation of MRI and cannabinoid type 1 receptor PET templates constructed using DARTEL for spatial normalization of rat brains. Med Phys 42:6875.

Lutz B, Marsicano G, Maldonado R, Hillard CJ (2015) The endocannabinoid system in guarding against fear, anxiety and stress. Nat Rev Neurosci 16:705-718.

de Salas-Quiroga A, Díaz-Alonso J, García-Rincón D, Remmers F, Vega D, Gómez-Cañas M, Lutz B, Guzmán M, Galve-Roperh I (2015) Prenatal exposure to cannabinoids evokes long-lasting functional alterations by targeting CB1 receptors on developing cortical neurons. Proc Natl Acad Sci U S A 112: 13693-8

Fuss J, Steinle J, Bindila L, Auer MK, Kirchherr H, Lutz B, Gass P (2015) A runner's high depends on cannabinoid receptors in mice. Proc Natl Acad Sci USA 112:13105-8.

Jokisch V, Kroll R, Lutz B, Bindila L, Schaffelder R, Schaible T (2015) Endocannabinoid levels in newborns in relation to the mode of delivery. Am J Perinatol 32:1145-50.

Blázquez C, Chiarlone A, Bellocchio L, Resel E, Pruunsild P, García-Rincón D, Sendtner M, Timmusk T, Lutz B, Galve-Roperh I, Guzmán M (2015) The CB1 cannabinoid receptor signals striatal neuroprotection via a PI3K/Akt/mTORC1/BDNF pathway. Cell Death Differ 22:1618-29.

Duerr GD, Heinemann JC, Gestrich C, Heuft T, Klaas T, Keppel K, Roell W, Klein A, Zimmer A, Velten M, Kilic A, Bindila L, Lutz B, Dewald O (2015) Impaired border zone formation and adverse remodeling after reperfused myocardial infarction in cannabinoid CB2 receptor deficient mice. Life Sci 138:8-17.

Jenniches I, Ternes S, Albayram O, Otte DM, Bach K, Bindila L, Michel K, Lutz  B, Bilkei-Gorzo A, Zimmer A (2015) Anxiety, stress, and fear response in mice with reduced endocannabinoid levels. Biol Psychiatry 79: 858-68.

Legler A, Monory K, Lutz B (2015) Age differences in the role of the cannabinoid type 1 receptor on glutamatergic neurons in habituation and spatial memory acquisition. Life Sci 138:57-63.

Njoo C, Agarwal N, Lutz B, Kuner R (2015) The Cannabinoid Receptor CB1 interacts with the WAVE1 complex and plays a role in actin dynamics and structural plasticity in neurons. PLoS Biol 13:e1002286.

Häring M, Enk V, Aparisi Rey A, Loch S, Ruiz de Azua I, Weber T, Bartsch D, Monory K, Lutz B (2015) Cannabinoid type-1 receptor signaling in central serotonergic neurons regulates anxiety-like behavior and sociability. Front Behav Neurosci 9:235.

Piyanova A, Lomazzo E, Bindila L, Lerner R, Albayram O, Ruhl T, Lutz B, Zimmer A, Bilkei-Gorzo A (2015) Age-related changes in the endocannabinoid system in the mouse hippocampus. Mech Ageing Dev 150: 55-64.

Rivera P, Blanco E, Bindila L, Alen F, Vargas A, Rubio L, Pavón FJ, Serrano A, Lutz B, Rodríguez de Fonseca F, Suárez J (2015) Pharmacological activation of CB2 receptors counteracts the deleterious effect of ethanol on cell proliferation in the main neurogenic zones of the adult rat brain. Front Cell Neurosci 9:379.

Schneider M, Kasanetz F, Lynch DL, Friemel CM, Lassalle O, Hurst DP, Steindel F, Monory K, Schäfer C, Miederer I, Leweke FM, Schreckenberger M, Lutz B, Reggio PH, Manzoni OJ, Spanagel R (2015) Enhanced functional activity of the cannabinoid type-1 receptor mediates adolescent behavior. J Neurosci 35:13975-88.

Bilgin M, Bindila L, Graessler J, Shevchenko A (2015) Quantitative profiling of endocannabinoids in lipoproteins by LC-MS/MS. Anal Bioanal Chem 407:5125-31.

Monory K, Polack M, Remus A, Lutz B, Korte M (2015) Cannabinoid CB1 receptor calibrates excitatory synaptic balance in the mouse hippocampus. J Neurosci 35:3842-50.

Rivera P, Bindila L, Pastor A, Pérez-Martín M, Pavón FJ, Serrano A, de la Torre R, Lutz B, Rodríguez de Fonseca F, Suárez J (2015) Pharmacological blockade of the fatty acid amide hydrolase (FAAH) alters neural proliferation, apoptosis and gliosis in the rat hippocampus, hypothalamus and striatum in a negative energy context. Front Cell Neurosci 9:98.

Gestrich C, Duerr GD, Heinemann JC, Meertz A, Probst C, Roell W, Schiller W, Zimmer A, Bindila L, Lutz B, Welz A, Dewald O (2015) Activation of Endocannabinoid System Is Associated with Persistent Inflammation in Human Aortic Aneurysm. Biomed Res Int 2015:456582.

Lomazzo E, Bindila L, Remmers F, Lerner R, Schwitter C, Hoheisel U, Lutz B (2015) Therapeutic potential of inhibitors of endocannabinoid degradation for the treatment of stress-related hyperalgesia in an animal model of chronic pain. Neuropsychopharmacology 40:488-501.

Publications 2014

Sakry D, Neitz A, Singh J, Frischknecht R, Marongiu D, Binamé F, Perera SS,Endres K, Lutz B, Radyushkin K, Trotter J, Mittmann T (2014) Oligodendrocyte Precursor Cells Modulate the Neuronal Network by Activity-Dependent Ectodomain Cleavage of Glial NG2. PLoS Biol 12(11):e1001993.

Duerr GD, Heinemann JC, Suchan G, Kolobara E, Wenzel D, Geisen C, Matthey M, Passe-Tietjen K, Mahmud W, Ghanem A, Tiemann K, Alferink J, Burgdorf S, Buchalla R, Zimmer A, Lutz B, Welz A, Fleischmann BK, Dewald O (2014) The endocannabinoid-CB2 receptor axis protects the ischemic heart at the early stage of cardiomyopathy. Basic Res Cardiol 109:425.

Hebert-Chatelain E, Reguero L, Puente N, Lutz B, Chaouloff F, Rossignol R, Piazza PV, Benard G, Grandes P, Marsicano G (2014) Cannabinoid control of brain bioenergetics: Exploring the subcellular localization of the CB1 receptor. Mol Metab 3:495-504.

Hebert-Chatelain E, Reguero L, Puente N, Lutz B, Chaouloff F, Rossignol R, Piazza PV, Benard G, Grandes P, Marsicano G (2014) Studying mitochondrial CB1 receptors: Yes we can. Mol Metab 3:339.

Jergas B, Schulte K, Bindila L, Lutz B, Schlicker E (2014) O-2050 facilitates noradrenaline release and increases the CB1 receptor inverse agonistic effect of rimonabant in the guinea pig hippocampus. Naunyn Schmiedebergs Arc Pharmacol 387:621-8.

Chiarlone A, Bellocchio L, Blázquez C, Resel E, Soria-Gómez E, Cannich A, Ferrero JJ, Sagredo O, Benito C, Romero J, Sánchez-Prieto J, Lutz B, Fernández-Ruiz J, Galve-Roperh I, Guzmán M (2014) A restricted population of CB1 cannabinoid receptors with neuroprotective activity. Proc Natl Acad Sci USA 111:8257-62.

Hoyer FF, Khoury M, Slomka H, Kebschull M, Lerner R, Lutz B, Schott H, Lütjohann D, Wojtalla A, Becker A, Zimmer A, Nickenig G (2014) Inhibition of endocannabinoid-degrading enzyme fatty acid amide hydrolase increases atherosclerotic plaque vulnerability in mice. J Mol Cell Cardiol 66:126-32.

Musella A, Sepman H, Mandolesi G, Gentile A, Fresegna D, Haji N, Conrad A, Lutz B, Maccarrone M, Centonze D (2014) Pre- and postsynaptic type-1 cannabinoid receptors control the alterations of glutamate transmission in experimental autoimmune encephalomyelitis. Neuropharmacology 79:567-72.

Pryce G, Visintin C, Ramagopalan SV, Al-Izki S, De Faveri LE, Nuamah RA, Mein CA, Montpetit A, Hardcastle AJ, Kooij G, de Vries HE, Amor S, Thomas SA, Ledent C, Marsicano G, Lutz B, Thompson AJ, Selwood DL, Giovannoni G, Baker D (2014) Control of spasticity in a multiple sclerosis model using central nervous system-excluded CB1 cannabinoid receptor agonists. FASEB J 28:117-30.

Soria-Gómez E, Bellocchio L, Reguero L, Lepousez G, Martin C, Bendahmane M, Ruehle S, Remmers F, Desprez T, Matias I, Wiesner T, Cannich A, Nissant A, Wadleigh A, Pape HC, Chiarlone AP, Quarta C, Verrier D, Vincent P, Massa F, Lutz B, Guzmán M, Gurden H, Ferreira G, Lledo PM, Grandes P, Marsicano G (2014) The endocannabinoid system controls food intake via olfactory processes. Nat Neurosci 17:407-15.

Publications 2013

Bellocchio L, Soria-Gómez E, Quarta C, Metna-Laurent M, Cardinal P, Binder E, Cannich A, Delamarre A, Häring M, Martín-Fontecha M, Vega D, Leste-Lasserre T, Bartsch D, Monory K, Lutz B, Chaouloff F, Pagotto U, Guzman M, Cota D, Marsicano G (2013) Activation of the sympathetic nervous system mediates hypophagic and anxiety-like effects of CB₁ receptor blockade. Proc Natl Acad Sci U S A 110:4786-91

Dodd GT, Worth AA, Hodkinson DJ, Srivastava RK, Lutz B, Williams SR, Luckman SM (2013) Central functional response to the novel peptide cannabinoid, hemopressin. Neuropharmacology 71:27-36.

Duerr GD, Heinemann JC, Dunkel S, Zimmer A, Lutz B, Lerner R, Roell W, Mellert F, Probst C, Esmailzadeh B, Welz A, Dewald O (2013) Myocardial hypertrophy is associated with inflammation and activation of endocannabinoid system in patients with aortic valve stenosis. Life Sci 92:976-83.

Gaffal E, Cron M, Glodde N, Bald T, Kuner R, Zimmer A, Lutz B, Tüting T (2013) Cannabinoid 1 receptors in keratinocytes modulate proinflammatory chemokine secretion and attenuate contact allergic inflammation. J Immunol 190:4929-36.

Häring M, Grieb M, Monory K, Lutz B, Moreira FA (2013) Cannabinoid CB1 receptor in the modulation of stress coping behaviour in mice: the role of serotonin and different forebrain neuronal subpopulations. Neuropharmacology 65:83-89.

Lerner R, Lutz B, Bindila L (2013) Tricks and tracks in the identification and quantification of endocannabinoids. In: eLS. John Wiley & Sons, Ltd: Chichester. DOI: 10.1002/9780470015902.a0023407

Leschik J, Eckenstaler R, Nieweg K, Lichtenecker P, Brigadski T, Gottmann K, Leßmann V, Lutz B (2013) Stably BDNF-GFP expressing embryonic stem cells exhibit a BDNF release-dependent enhancement of neuronal differentiation. J Cell Sci 126:5062-73.

Meuth P, Gaburro S, Lesting J, Legler A, Herty M, Budde T, Meuth SG, Seidenbecher T, Lutz B, Pape HC (2013) Standardizing the analysis of conditioned fear in rodents: a multidimensional software approach. Genes Brain Behav 12:583-92.

Miederer I, Maus S, Zwiener I, Podoprygorina G, Meshcheryakov D, Lutz B, Schreckenberger M (2013) Evaluation of cannabinoid type 1 receptor expression in the rat brain using [(18)F]MK-9470 microPET. Eur J Nucl Med Mol Imaging 40:1739-1747.

Ruehle S, Remmers F, Romo-Parra H, Massa F, Wickert M, Wörtge S, Häring M, Kaiser N, Marsicano G, Pape HC, Lutz B (2013) Cannabinoid CB1 receptor in dorsal telencephalic glutamatergic neurons: distinctive sufficiency for hippocampus-dependent and amygdala-dependent synaptic and behavioral functions. J Neurosci 33:10264-77.

Steindel F, Lerner R, Häring M, Ruehle S, Marsicano G, Lutz B, Monory K (2013) Neuron-type specific cannabinoid-mediated G protein signalling in mouse hippocampus. J Neurochem 124:795-807.

Stumm C, Hiebel C, Hanstein R, Purrio M, Nagel H, Conrad A, Lutz B, Behl C, Clement AB (2013) Cannabinoid receptor 1 deficiency in a mouse model of Alzheimer's disease leads to enhanced cognitive impairment despite of a reduction in amyloid deposition. Neurobiol Aging 34:2574-84.

von Jonquieres G, Mersmann N, Klugmann CB, Harasta AE, Lutz B, Teahan O, Housley GD, Fröhlich D, Krämer-Albers EM, Klugmann M (2013) Glial promoter selectivity following AAV-delivery to the immature brain. PLoS One 8:e65646.

Wenzel D, Matthey M, Bindila L, Lerner R, Lutz B, Zimmer A, Fleischmann BK (2013) Endocannabinoid anandamide mediates hypoxic pulmonary vasoconstriction. Proc Natl Acad Sci U S A. 110:18710-5.

Publications 2012

Bashashati M, Storr MA, Nikas SP, Wood JT, Godlewski G, Liu J, Ho W, Keenan CM, Zhang H, Alapafuja SO, Cravatt BF, Lutz B, Mackie K, Kunos G, Patel KD, Makriyannis A, Davison JS, Sharkey KA (2012) Inhibiting fatty acid amide hydrolase normalizes endotoxin-induced enhanced gastrointestinal motility in mice. Br J Pharmacol. 165:1556-71.

Bauer M, Chicca A, Tamborrini M, Eisen D, Lerner R, Lutz B, Poetz O, Pluschke G, Gertsch J (2012) Identification and quantification of a new family of peptide endocannabinoids (Pepcans) showing negative allosteric modulation at CB1 receptors. J Biol Chem. 287(44):36944-67.

Bénard G, Massa F, Puente N, Lourenço J, Bellocchio L, Soria-Gómez E, Matias I, Delamarre A, Metna-Laurent M, Cannich A, Hebert-Chatelain E, Mulle C, Ortega-Gutiérrez S, Martín-Fontecha M, Klugmann M, Guggenhuber S, Lutz B, Gertsch J, Chaouloff F, López-Rodríguez ML, Grandes P, Rossignol R, Marsicano G (2012) Mitochondrial CB₁ receptors regulate neuronal energy metabolism. Nat Neurosci. 15:558-64.

Cardinal P, Bellocchio L, Clark S, Cannich A, Klugmann M, Lutz B, Marsicano G, Cota D (2012) Hypothalamic CB1 cannabinoid receptors regulate energy balance in mice. Endocrinology 153:4136-43.

Conzelmann A, Reif A, Jacob C, Weyers P, Lesch KP, Lutz B, Pauli P (2012) A polymorphism in the gene of the endocannabinoid-degrading enzyme FAAH (FAAH C385A) is associated with emotional-motivational reactivity. Psychopharmacology (Berl) 224,573-579.

Díaz-Alonso J, Aguado T, Wu CS, Palazuelos J, Hofmann C, Garcez P, Guillemot F, Lu HC, Lutz B, Guzmán M, Galve-Roperh I. The CB1 Cannabinoid Receptor Drives Corticospinal Motor Neuron Differentiation through the Ctip2/Satb2 Transcriptional Regulation Axis. J Neurosci 32:16651-16665.

Dubreucq S, Matias I, Cardinal P, Häring M, Lutz B, Marsicano G, Chaouloff F (2012) Genetic dissection of the role of cannabinoid type-1 receptors in the emotional consequences of repeated social stress in mice. Neuropsychopharmacology 37:1885-900.

Grabiec U, Koch M, Kallendrusch S, Kraft R, Hill K, Merkwitz C, Ghadban C, Lutz B, Straiker A, Dehghani F (2012) The endocannabinoid N-arachidonoyldopamine (NADA) exerts neuroprotective effects after excitotoxic neuronal damage via cannabinoid receptor 1 (CB1). Neuropharmacology 62:1797-807.

Häring M, Guggenhuber S, Lutz B (2012) Neuronal populations mediating the effects of endocannabinoids on stress and emotionality. Neuroscience 204:145-58.

Hons IM, Storr MA, Mackie K, Lutz B, Pittman QJ, Mawe GM, Sharkey KA (2012) Plasticity of mouse enteric synapses mediated through endocannabinoid and purinergic signaling. Neurogastroenterol Motil. 24:e113-24.

Jacob W, Marsch R, Marsicano G, Lutz B, Wotjak CT (2012) Cannabinoid CB1 receptor deficiency increases contextual fear memory under highly aversive conditions and long-term potentiation in vivo. Neurobiol Learn Mem. 98:47-55.

Pamplona FA, Ferreira J, Menezes de Lima O Jr, Duarte FS, Bento AF, Forner S, Villarinho JG, Bellochio L, Wotjak CT, Lerner R, Monory K, Lutz B, Canetti C, Matias I, Calixto JB, Marsicano G, Guimarães MZ, Takahashi RN (2012) Anti-inflammatory lipoxin A4 is an endogenous allosteric enhancer of CB1 cannabinoid receptor. Proc Natl Acad Sci U S A. 109:21134-9.

Rey AA, Purrio M, Viveros MP, Lutz B (2012) Biphasic effects of cannabinoids in anxiety responses: CB1 and GABAB receptors in the balance of GABAergic and glutamatergic neurotransmission. Neuropsychopharmacology 37:2624–2634.

Ruehle S, Rey AA, Remmers F, Lutz B (2012) The endocannabinoid system in anxiety, fear memory and habituation. J Psychopharmacol. 26:23-39.

Schulte K, Steingrüber N, Jergas B, Redmer A, Kurz CM, Buchalla R, Lutz B, Zimmer A, Schlicker E (2012) Cannabinoid CB1 receptor activation, pharmacological blockade, or genetic ablation affects the function of the muscarinic auto- and heteroreceptor. Naunyn Schmiedebergs Arch Pharmacol. 385:385-96.

Wojtalla A, Herweck F, Granzow M, Klein S, Trebicka J, Huss S, Lerner R, Lutz B, Schildberg FA, Knolle PA, Sauerbruch T, Singer MV, Zimmer A, Siegmund SV (2012) The endocannabinoid N-arachidonoyl dopamine (NADA) selectively induces oxidative stress-mediated cell death in hepatic stellate cells but not in hepatocytes. Am J Physiol Gastrointest Liver Physiol. 302:G873-87.

Publications 2011

Albayram O, Alferink J, Pitsch J, Piyanova A, Neitzert K, Poppensieker K, Mauer D, Michel K, Legler A, Becker A, Monory K, Lutz B, Zimmer A, Bilkei-Gorzo A (2011) Role of CB1 cannabinoid receptors on GABAergic neurons in brain aging. Proc Natl Acad Sci U S A. 108:11256-61.

Argaw A, Duff G, Zabouri N, Cécyre B, Chainé N, Cherif H, Tea N, Lutz B, Ptito M, Bouchard JF (2011) Concerted action of CB1 cannabinoid receptor and deleted in colorectal cancer in axon guidance. J Neurosci. 31:1489-99.

Blázquez C, Chiarlone A, Sagredo O, Aguado T, Pazos MR, Resel E, Palazuelos J, Julien B, Salazar M, Börner C, Benito C, Carrasco C, Diez-Zaera M, Paoletti P, Díaz-Hernández M, Ruiz C, Sendtner M, Lucas JJ, de Yébenes JG, Marsicano G, Monory K, Lutz B, Romero J, Alberch J, Ginés S, Kraus J, Fernández-Ruiz J, Galve-Roperh I, Guzmán M (2011) Loss of striatal type 1 cannabinoid receptors is a key pathogenic factor in Huntington's disease. Brain 134:119-36.

Carey MR, Myoga MH, McDaniels KR, Marsicano G, Lutz B, Mackie K, Regehr WG (2011) Presynaptic CB1 receptors regulate synaptic plasticity at cerebellar parallel fiber synapses. J Neurophysiol. 105:958-63.

Guggenhuber S, Monory K, Lutz B, Klugmann M (2011) AAV vector-mediated overexpression of CB1 cannabinoid receptor in pyramidal neurons of the hippocampus protects against seizure-induced excitoxicity. PLoS One 5(12):e15707.

Häring M, Kaiser N, Monory K, Lutz B (2011) Circuit specific functions of cannabinoid CB1 receptor in the balance of investigatory drive and exploration. PLoS One 6(11):e26617.

Hoyer FF, Steinmetz M, Zimmer S, Becker A, Lütjohann D, Buchalla R, Zimmer A, Nickenig G (2011) Atheroprotection via cannabinoid receptor-2 is mediated by circulating and vascular cells in vivo. J Mol Cell Cardiol. 51:1007-14.

Kamprath K, Romo-Parra H, Häring M, Gaburro S, Doengi M, Lutz B, Pape HC (2011) Short-term adaptation of conditioned fear responses through endocannabinoid signaling in the central amygdala. Neuropsychopharmacology 36:652-63.

Klugmann M, Klippenstein V, Leweke FM, Spanagel R, Schneider M (2011) Cannabinoid exposure in pubertal rats increases spontaneous ethanol consumption and NMDA receptor associated protein levels. Int J Neuropsychopharmacol. 14:505-17.

Mersmann N, Tkachev D, Jelinek R, Röth PT, Möbius W, Ruhwedel T, Rühle S, Weber-Fahr W, Sartorius A, Klugmann M (2011) Aspartoacylase-lacZ knockin mice: an engineered model of Canavan disease. PLoS One 6(5):e20336.

Remmers F, Delemarre-van de Waal HA (2011) Developmental programming of energy balance and its hypothalamic regulation. Endocr Rev. 32:272-311.

Rossi S, Furlan R, De Chiara V, Muzio L, Musella A, Motta C, Studer V, Cavasinni F, Bernardi G, Martino G, Cravatt BF, Lutz B, Maccarrone M, Centonze D (2011) Cannabinoid CB1 receptors regulate neuronal TNF-α effects in experimental autoimmune encephalomyelitis. Brain Behav Immun. 25:1242-8.

Schicho R, Bashashati M, Bawa M, McHugh D, Saur D, Hu HM, Zimmer A, Lutz B, Mackie K, Bradshaw HB, McCafferty DM, Sharkey KA, Storr M (2011) The atypical cannabinoid O-1602 protects against experimental colitis and inhibits neutrophil recruitment. Inflamm Bowel Dis. 17:1651-64.

Valor LM, Pulopulos MM, Jimenez-Minchan M, Olivares R, Lutz B, Barco A (2011) Ablation of CBP in forebrain principal neurons causes modest memory and transcriptional defects and a dramatic reduction of histone acetylation but does not affect cell viability. J Neurosci. 31:1652-63.

Publications 2010

Cluny NL, Keenan CM, Duncan M, Fox A, Lutz B, Sharkey KA (2010) Naphthalen-1-yl-(4-pentyloxynaphthalen-1-yl)methanone (SAB378), a peripherally restricted cannabinoid CB1/CB2 receptor agonist, inhibits gastrointestinal motility but has no effect on experimental colitis in mice. J Pharmacol Exp Ther 334:973-80.

Cluny NL, Vemuri VK, Chambers AP, Limebeer CL, Bedard H, Wood JT, Lutz B, Zimmer A, Parker LA, Makriyannis A, Sharkey KA (2010) A novel peripherally restricted cannabinoid receptor antagonist, AM6545, reduces food intake and body weight, but does not cause malaise, in rodents. Br J Pharmacol 161:629-42.

Dodd GT, Mancini G, Lutz B, Luckman SM. The peptide hemopressin acts through CB1 cannabinoid receptors to reduce food intake in rats and mice (2010) J Neurosci 30:7369-76.

Guggenhuber S, Monory K, Lutz B, Klugmann M (2010) AAV Vector-Mediated Overexpression of CB1 Cannabinoid Receptor in Pyramidal Neurons of the Hippocampus Protects against Seizure-Induced Excitoxicity. PLoS One 5(12):e15707.

Massa F, Mancini G, Schmidt H, Steindel F, Mackie K, Angioni C, Oliet SH, Geisslinger G, Lutz B (2010) Alterations in the hippocampal endocannabinoid system in diet-induced obese mice. J Neurosci 30:6273-81.

Quarta C, Bellocchio L, Mancini G, Mazza R, Cervino C, Braulke LJ, Fekete C, Latorre R, Nanni C, Bucci M, Clemens LE, Heldmaier G, Watanabe M, Leste-Lassere T, Maitre M, Tedesco L, Fanelli F, Reuss S, Klaus S, Srivastava RK, Monory K, Valerio A, Grandis A, De Giorgio R, Pasquali R, Nisoli E, Cota D, Lutz B, Marsicano G, Pagotto U (2010) CB1 signaling in forebrain and sympathetic neurons is a key determinant of endocannabinoid actions on energy balance. Cell Metab 11:273-85.

Storr MA, Bashashati M, Hirota C, Vemuri VK, Keenan CM, Duncan M, Lutz B, Mackie K, Makriyannis A, Macnaughton WK, Sharkey KA (2010) Differential effects of CB1 neutral antagonists and inverse agonists on gastrointestinal motility in mice. Neurogastroenterol Motil 22:787-96.

Wu CS, Zhu J, Wager-Miller J, Wang S, O'Leary D, Monory K, Lutz B, Mackie K, Lu HC. Requirement of cannabinoid CB1 receptors in cortical pyramidal neurons for appropriate development of corticothalamic and thalamocortical projections. Eur J Neurosci 32:693–706.

Publications 2009

Chung SC, Hammarsten P, Josefsson A, Stattin P, Granfors T, Egevad L, Mancini G, Lutz B, Bergh A, Fowler CJ. (2009) A high cannabinoid CB1 receptor immunoreactivity is associated with disease severity and outcome in prostate cancer. Eur J Cancer, 45:174-82.

Cluny NL, Keenan CM, Lutz B, Piomelli D, Sharkey KA (2009) The identification of peroxisome proliferator-activated receptor alpha independent effects of oleoylethanolamide on intestinal transit in mice. Neurogastroenterology and Motility 21:420-429.

Kamprath K, Plendl W, Marsicano G, Deussing JM, Wurst W, Lutz B, Wotjak CT (2009) Endocannabinoids mediate acute fear adaptation via glutamatergic neurons independently of CRH signaling. Genes Brain Behav 8:203-211.

Kodirov SA, Jasiewicz J, Amirmahani P, Psyrakis D, Bonni K, Wehrmeister M, Lutz B (2009) Endogenous cannabinoids trigger the depolarization-induced suppression of excitation in the lateral amygdala. Learn Mem 17:43-9.

Lutz B (2009) Endocannabinoid signals in the control of emotion. Curr Opin Pharmacol 9:46-52.

Moreira FA, Grieb M, Lutz B (2009) Central side-effects of therapies based on CB1 cannabinoid receptor agonists and antagonists: focus on anxiety and depression. Best Practice & Research Clinical Endocrinology & Metabolism 23:133-144.

Pernía-Andrade AJ, Kato A, Witschi R, Nyilas R, Katona I, Freund TF, Watanabe M, Filitz J, Koppert W, Schüttler J, Ji G, Neugebauer V, Marsicano G, Lutz B, Vanegas H, Zeilhofer HU (2009) Spinal endocannabinoids and CB1 receptors mediate C-fiber-induced heterosynaptic pain plasticity. Science 325:760-4.

Price DA, Seillier A, Koek W, Acosta Y, Fernandez E, Strong JR, Lutz B, Marsicano G, Roberts JL, Guiffrida A (2009) WIN55,212-2, a cannabinoid receptor agonist, protects against nigrostriatal cell loss in the MPTP mouse model of Parkinson¹s Disease. Eur J Neurosci 29:2177-2186.

Puighermanal E, Marsicano G, Busquets A, Lutz B, Maldonado R, Ozaita A (2009) Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signalling through CB1 receptors located in GABAergic neurons. Nat Neurosci 12:1152-8.

Publications 2008

Azad SC, Kurz J, Marsicano G, Lutz B, Zieglgänsberger W, Rammes G (2008) Cannabinoid receptor type 1 (CB1) receptor on GABAergic interneurons inhibits LTD in lateral amygdala. Learn Mem 15:143-52.

Hansen HH, Krutz B, Sifringer M, Stefovska V, Bittigau P, Pragst F, Marsicano G, Lutz B, Ikonomidou C (2008) Cannabinoids enhance susceptibility of immature brain to ethanol neurotoxicity. Ann Neurol 64:52-62.

Jeong WI, Osei-Hyiaman D, Park O, Liu J, Bátkai S, Mukhopadhyay P, Horiguchi N, Harvey-White J, Marsicano G, Lutz B, Gao B and Kunos G (2008) Paracrine activation of hepatic CB1 receptors by stellate cell-derived endocannabinoids mediates alcoholic fatty liver. Cell Metabol 7:227-35.

Lutz B, Monory K (2008) Soothing the seizures of children. Nat Med 14:721-2.

Moreira FA, Kaiser N, Monory K, Lutz B (2008) Reduced anxiety-like behaviour induced by genetic and pharmacological inhibition of the endocannabinoid-degrading enzyme fatty acid amide hydrolase (FAAH) is mediated by CB1 receptors. Neuropharmacology 54:141-50.

Moreira FA, Lutz B (2008) The endocannabinoid system: Emotion, learning and addiction. Addiction Biology 13:196-212.

Mulder J, Aguado T, Keimpema E, Barabás K, Ballester Rosado CJ, Nguyen L, Monory K, Marsicano G, Di Marzo V, Hurd YL, Guillemot F, Mackie K, Lutz B, Guzmán M, Lu HC, Galve-Roperh I, Harkany T. (2008) Endocannabinoid signaling controls pyramidal cell specification and long-range axon patterning. Proc Natl Acad Sci U S A 105:8760-5.

Osei-Hyiaman D, Liu J, Zhou L, Godlewski G, Harvey-White J, Jeong Wi, Bátkai S, Marsicano G, Lutz B, Buettner C, Kunos G (2008) Hepatic CB1 receptor involvement in diet-induced steatosis, altered lipid profile, and insulin and leptin resistance. J Clin Invest 118:3160-3169.

Sitz JH, Baumgärtel K, Hämmerle B, Papadopoulos C, Hekerman P, Tejedor F, Becker W, Lutz B. (2008) The Down syndrome candidate kinase DYRK1A phosphorylates the neurodegeneration-related septin SEPT4. Neuroscience 157:596-605.

Steiner M, Marsicano G, Wotjak CT, Lutz B (2008) Conditional cannabinoid receptor type 1 mutants reveal neuron subpopulation-specific effects on behavioral and neuroendocrine stress responses. Psychoneuroendocrinology 33:1165-1170.

Steiner MA, Marsicano G, Nestler EJ, Holsboer F, Lutz B, Wotjak C (2008) Antidepressant-like behavioural effects of impaired cannabinoid type 1 signalling coincide with exaggerated corticosterone secretion in mice. Psychoneuroendocrinol 33:54-67.

Storr MA, Keenan CM, Emmerdinger D, Zhang H, Yüce B, Sibaev A, Massa F, Buckley NE, Lutz B, Göke B, Brand S, Patel KD, Sharkey KA. (2008) Targeting endocannabinoid degradation protects against experimental colitis in mice: involvement of CB1 and CB2 receptors. J Mol Med 86:925-936.

Tedesco L, Valerio A, Cervino C, Cardile A, Pagano C, Vettor R, Pasquali R, Carruba MO, Marsicano G, Lutz B, Pagotto U, Nisoli E (2008) Cannabinoid type 1 receptor blockade promotes mitochondrial biogenesis through eNOS expression in white adipocytes. Diabetes 57:2028-36.

Publications 2007

Agarwal N, Pacher P, Tegeder I, Amaya F, Constantin C, Brenner GJ, Rubino T, Michalski CW, Marsicano G, Monory K, Mackie K, Marian C, Batkai B, Parolaro D, Fischer MJ, Reeh P, Kunos G, Kress M, Lutz B, Woolf CJ, Kuner R (2007) Nociceptor-specific conditional gene deletion reveals that cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors. Nat Neurosci 10:870-9.

Aguado T, Romero E, Monory K, Palazuelos J, Sendtner M, Marsicano G, Lutz B, Guzman M, Galve-Roperh I (2007) The CB1 cannabinoid receptor mediates excitotoxicity-induced neural progenitor proliferation and neurogenesis. J Biol Chem 282:23892-8.

Berghuis P, Rajnicek AM, Morozov YM, Ross RA, Mulder J, Gabriella M, Urbán GM, Monory K, Marsicano G, Matteoli M, Canty A, Irving AJ, Katona I, Yanagawa Y, Rakic P, Lutz B, Mackie K, Harkany T (2007) Hardwiring the brain: endocannabinoids control axon guidance. Science 316:1212-16.

Brenz Verca MS, Weber P, Mayer C, Graf C, Refojo D, Kühn R, Grummt I, Lutz B (2007) Development of a species-specific RNA polymerase I-based shRNA expression vector. Nucl Acids Res 35:e10.

Corbillé AG, Valjent E, Marsicano G, Ledent L, Lutz B, Hervé D, Girault JA (2007) Role of CB1 receptors in locomotor activity and striatal signaling in response to psychostimulants. J Neurosci 27:6937– 6947.

Cota D, Steiner MA, Marsicano G, Cervino C, Herman JP, Grubler Y, Stalla J, Pasquali R, Lutz B, Stalla GK, Pagotto U (2007) Requirement of cannabinoid receptor type 1 for the basal modulation of hypothalamic-pituitary-adrenal axis formation. Endocrinology 148:1574-81.

Deshmukh S, Onozuka K, Bender KJ, Bender VA, Lutz B, Mackie K, Feldman DE (2007) Postnatal development of cannabinoid receptor type 1 expression in rodent somatosensory cortex. Neuroscience 2007 145:279-87.

Häring M, Marsicano G, Lutz B, Monory K. (2007) Identification of the cannabinoid receptor type 1 in serotonergic cells of raphe nuclei in mice. Neuroscience. 2007 Mar 22; 146:1212-9.

Izzo AA, Avello G, Petrosino S, Orlando P, Morsicano G, Lutz B, Borrelli F, Papasso R, Nigam S, Papasso F, Di Marzo V (2007) Increased endocannabinoid levels reduce the development of precancerous lesions in the mouse colon. J Mol Med 86:89-98.

Lutz B (2007) The endocannabinoid system and extinction learning. Mol Neurobiol 36:92-100.

Maresz K, Pryce G, Ponomarev ED, Marsicano G, Croxford JL, Shriver LP, Ledent C, Cheng X, Carrier EJ, Mann MK, Giovannoni G, Pertwee RG, Yamamura T, Buckley NE, Hillard CJ, Lutz B, Baker D, Dittel BN. (2007) Direct suppression of CNS autoimmune inflammation via the cannabinoid receptor CB1 on neurons and CB2 on autoreactive T cells. Nat Med 13(4):492-7.

Marsch R, Foeller E, Rammes G, Bunck M, Kössl M, Holsboer F, Zieglgänsberger W, Landgraf R, Lutz B, Wotjak CT (2007) Reduced anxiety, conditioned fear, and hippocampal long-term potentiation in transient receptor potential vanilloid type 1 receptor-deficient mice. J Neurosci 27:832-9.

Monory M, Blaudzun H, Massa F, Kaiser N, Lemberger T, Schütz G, Wotjak CT, Marsicano G*, Lutz B*, (2007) Genetic dissection of behavioural and autonomic effects of Δ9-tetrahydrocannabinol in mice, PLoS Biol 5:e269. (*, equal contributions)

Steiner MA, Wanisch K, Monory K, Marsicano G, Borroni E, Bächli H, Holsboer F, Lutz B, Wotjak CT (2007) Impaired cannabinoid receptor type 1 signaling interferes with stress coping behavior in mice. The Pharmacogenomics J 8:196-208.

Yuece B, Sibaev A, Broedl U, Marsicano G, Goeke B, Lutz B, Allescher HD, Storr M (2007) Cannabinoid type 1 receptor modulates intestinal propulsion by an attenuation of intestinal motor responses within the peristaltic reflex. Neurogastroenterol Motil 19:744-753.

Publications 2006

Aguado T, Palazuelos J, Monory K, Stella N, Cravatt B, Lutz B, Marsicano G, Kokaia Z, Guzman, M, Galve-Roperh I (2006) The endocannabinoid system promotes astroglial differentiation b acting on neural progenitor cells. J Neurosci 26:1551-1561.

Barad M, Gean PW, Lutz B (2006) The role of the amygdala in the extinction of conditioned fear. Biol Psychiatry 60:322-328.

Domenici MR, Azad SC, Schierloh A, Wotjak CT, Dodt HU, Marsicano G, Zieglgänsberger W, Lutz B, Rammes G (2006) Evidence for the control of excitatory synaptic transmission by activation of cannabinoid receptor type 1 (CB1) located on presynaptic terminals of principal neurons in the cortex. J Neurosci 26:5794-9.

Kamprath C, Marsicano G, Tang J, Monory K, Bisogno T, Di Marzo V, Lutz B, Wotjak CT (2006) Cannabinoid CB1 receptor mediates fear extinction via habituation-like processes. J Neurosci 26:6677-86.

Marsicano G, Lutz B (2006) Neuromodulatory functions of the endocannabinoid system, J Endocrinol Invest 29 (3 suppl):27-46.

Massa F, Sibaev A, Marsicano G, Blauzun, Storr M, Lutz B (2006) Vanilloid receptor (TRPV1)-deficient mice show increased susceptibility to dinitrobenzene sulfonic acid-induced colitis. J Mol Med 84:142-6.

Melis M, Pillolla G, Bisogno T, Minassi A, Petrosino S, Perra S, Muntoni AL, Lutz B, Gessa GL, Marsicano G, Di Marzo V, Pistis M (2006) Protective activation of the endocannabinoid system during Ischemia in dopamine neurons, Neurobiol Dis 24:15-27.

Monory K, Massa F, Egertova M, Eder M, Blaudzun H, Westenbroek R, Kelsch W, Jacob W, Marsch R, Ekker M, Long J, Rubenstein JL, Goebbels S, Nave KA, During M, Klugmann M, Wolfel B, Dodt HU, Zieglgänsberger W, Wotjak CT, Mackie K, Elphick MR, Marsicano G, Lutz B. (2006) The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51:455-66.

Obradovic D, Gronemeyer H, Lutz B, Rein T (2006) Antagonizing actions of vitamin D3 on glucocorticoid functions in hippocampal cells. J Neurochem 96:500-509.

Pagotto U, Cervino C, Vicennati V, Marsicano G, Lutz B, Pasquali R (2006) How many sites of action for endocannabinoids to control energy metabolism? Int J Obes (Lond) 30 Suppl 1:S39-43.

Pagotto U, Marsicano G, Cota D, Lutz B, Pasquali R (2006) The emerging role of the endocannabinoid system in endocrine regulation and energy balance. Endocr Rev 27:73-100.

Sibaev A, Massa F, Yuce B, Marsicano G, Lehr HA, Lutz B, Goke B, Allescher HD, Storr M (2006) CB1 and TRPV1 receptors mediate protective effects on colonic electrophysiological properties in mice. J Mol Med 84:513-520.

Publications 2005

Aguado T, Monory K, Palazuelos J, Stella N, Cravatt B, Lutz B, Marsicano G, Kokaia Z, Guzman M, Galve-Roperh I (2005) The endocannabinoid system drives neural progenitor proliferation. FASEB J 19:1704-6.

Bayatti N, Hermann H, Lutz B, Behl C (2005) CRH-mediated induction of BDNF expression is inhibited by the activation of the cannabinoid system. Endocrinology 146:1205-1213.

Capasso R, Matias I, Lutz B, Borrelli F, Capasso F, Marsicano G, Mascolo N, Petrosino S, Monory K, Valenti M, Di Marzo V, Izzo AA (2005) Fatty acid amide hydrolase controls mouse intestinal motility in vivo. Gastroenterology 129:941-51.

Hermann H, Lutz B (2005) Coexpression of the cannabinoid receptor type 1 with the corticotropin-releasing hormone receptor type 1 in distinct regions of the adult mouse forebrain. Neurosci Lett 375:13-18.

Hölter SM, Kallnik M, Wurst W, Marsicano G, Lutz B, Wotjak CT (2005) Cannabinoid CB1 receptor is dispensable for memory extinction in an appetitively-motivated learning task. Eur J Pharmacol 510:69-74.

Massa F, Storr M, Lutz B (2005) The endocannabinoid system in the physiology and pathophysiology of the gastrointestinal tract. J Mol Med 83:944-54.

Monory K, Lutz B (2005) Pain killer without a high. Nat Med 11:378-379.

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