DRUCKEN

Lipid research

Our research projects focus on the discovery of lipid plasticity associated with pathophysiological states in various neurological diseases.

Translation of disease associated lipid changes into quantitative biological assays and their implementation for disease mechanism elucidation, lipid marker discovery and monitoring, and lipid drug targets discovery and therapy monitoring is one the major goals.

Publications

Jehle J, Eich L, Danisch M, Bagheri S, Avraamidou E, Pfeifer P, Tiyerili V, Bindila L, Lutz B, and Nickenig G (2021) The endocannabinoid 2-arachidonoylglycerol inhibits endothelial function and repair. Int J Cardiol 323:243–250.

Schuele L-L, Glasmacher S, Gertsch J, Roggan MD, Transfeld J-L, Bindila L, Lutz B, Kolbe C-C, Bilkei-Gorzo A, Zimmer A, and Leidmaa E (2021) Diacylglycerol lipase alpha in astrocytes is involved in maternal care and affective behaviors. Glia 69:377–391.

Tarragon E, Bindila L, Zimmer P, Lutz B, and Meyer J (2020) Salivary endocannabinoids as mediators in the relationship between omega-6 and  omega-3 fatty acid ratio intake from highly-processed foods and anthropometric markers of health in women. Int J Food Sci Nutr 71:235–241.

Meyer Zu Reckendorf S, Brand C, Pedro MT, Hegler J, Schilling CS, Lerner R, Bindila L, Antoniadis G, and Knöll B (2020) Lipid metabolism adaptations are reduced in human compared to murine Schwann cells following injury. Nat Commun 11:2123.

Müller-Vahl KR, Bindila L, Lutz B, Musshoff F, Skripuletz T, Baumgaertel C, and Sühs K-W (2020) Cerebrospinal fluid endocannabinoid levels in Gilles de la Tourette syndrome. Neuropsychopharmacol 45:1323–1329.

Kranaster L, Hoyer C, Mindt S, Neumaier M, Müller N, Zill P, Schwarz MJ, Moll N, Lutz B, Bindila L, Zerr I, Schmitz M, Blennow K, Zetterberg H, Haffner D, Leifheit-Nestler M, Ozbalci C, and Sartorius A (2020) The novel seizure quality index for the antidepressant outcome prediction in  electroconvulsive therapy: association with biomarkers in the cerebrospinal fluid. Eur Arch Psychiatry Clin Neurosci 270:911–919.

Jakubovski E, Pisarenko A, Fremer C, Haas M, May M, Schumacher C, Schindler C, Häckl S, Aguirre Davila L, Koch A, Brunnauer A, Cimpianu CL, Lutz B, Bindila L, and Müller-Vahl K (2020) The CANNA-TICS Study Protocol: A Randomized Multi-Center Double-Blind Placebo  Controlled Trial to Demonstrate the Efficacy and Safety of Nabiximols in the Treatment of Adults With Chronic Tic Disorders. Front psychiatry 11:575826.

Post JM, Lerner R, Schwitter C, Lutz B, Lomazzo E, and Bindila L (2020) Lipidomics and Transcriptomics in Neurological Diseases. JOVE 1–24.

Collu R, Post JM, Scherma M, Giunti E, Fratta W, Lutz B, Fadda P, and Bindila L (2020) Altered brain levels of arachidonic acid-derived inflammatory eicosanoids in a rodent model of anorexia nervosa. Biochim Biophys Acta - Mol Cell Biol Lipids 1865:158578.

Duerr GD, Heinemann JC, Kley J, Eichhorn L, Frede S, Weisheit C, Wehner S, Bindila L, Lutz B, Zimmer A, and Dewald O (2019) Myocardial maladaptation to pressure overload in CB2 receptor-deficient mice. J Mol Cell Cardiol 133:86–98.

Jehle J, Goerich H, Bindila L, Lutz B, Nickenig G, and Tiyerili V (2019) Endocannabinoid 2-arachidonoylglycerol is elevated in the coronary circulation  during acute coronary syndrome. PLoS One 14:e0227142.

Kirkedal C, Elfving B, Müller HK, Moreira FA, Bindila L, Lutz B, Wegener G, and Liebenberg N (2019) Hemisphere-dependent endocannabinoid system activity in prefrontal cortex and hippocampus of the Flinders Sensitive Line rodent model of depression. Neurochem Int 125:7–15.

Kranaster L, Hoyer C, Aksay SS, Bumb JM, Müller N, Zill P, Schwarz MJ, Moll N, Lutz B, Bindila L, Zerr I, Schmitz M, Blennow K, Zetterberg H, Haffner D, Leifheit-Nestler M, Ozbalci C, Janke C, Thiel M, and Sartorius A (2019) Biomarkers for Antidepressant Efficacy of Electroconvulsive Therapy: An Exploratory  Cerebrospinal Fluid Study. Neuropsychobiology 77:13–22.

Lerner R, Cuadrado DP, Post JM, Lutz B, and Bindila L (2019) Broad lipidomic and transcriptional changes of prophylactic PEA administration in control mice. Front Neurosci 13:527.

Rivera P, Silva-Peña D, Blanco E, Vargas A, Arrabal S, Serrano A, Pavón FJ, Bindila L, Lutz B, Rodríguez de Fonseca F, and Suárez J (2019) Oleoylethanolamide restores alcohol-induced inhibition of neuronal proliferation and microglial activity in striatum. Neuropharmacology 146:184–197.

Zimmermann T, Bartsch JC, Beer A, Lomazzo E, Guggenhuber S, Lange MD, Bindila L, Pape H-C, and Lutz B (2019) Impaired anandamide/palmitoylethanolamide signaling in hippocampal glutamatergic neurons alters synaptic plasticity, learning, and emotional responses. Neuropsychopharmacol 44:1377–1388.

Baumeister D, Eich W, Lerner R, Lutz B, Bindila L, and Tesarz J (2018) Plasma Parameters of the Endocannabinoid System Are Unaltered in Fibromyalgia. Psychother Psychosom 87:377-379.

Jehle J, Schöne B, Bagheri S, Avraamidou E, Danisch M, Frank I, Pfeifer P, Bindila L, Lutz B, Lütjohann D, Zimmer A, and Nickenig G (2018) Elevated levels of 2-arachidonoylglycerol promote atherogenesis in ApoE-/- mice. PLoS One 13:e0197751.

Heide EC, Bindila L, Post JM, Malzahn D, Lutz B, Seele J, Nau R, and Ribes S (2018) Prophylactic Palmitoylethanolamide Prolongs Survival and Decreases Detrimental Inflammation in Aged Mice With Bacterial Meningitis. Front Immunol 9.

Lerner R, Post JM, Ellis SR, Naomi Vos DR, Heeren RMA, Lutz B, and Bindila L (2018) Simultaneous lipidomic and transcriptomic profiling in mouse brain punches of acute epileptic seizure model compared to controls. J Lipid Res 59:283–297.

Post JM, Loch S, Lerner R, Remmers F, Lomazzo E, Lutz B, Bindila L (2018). Antiepileptogenic effect of subchronic palmitoylethanolamide treatment in a mouse model of acute epilepsy. Front Mol Neurosci 11: 67. doi:10.3389/fnmol.2018.00067

Lerner R, Post JM, Ellis SR, Vos DRN, Heeren RMA, Lutz B, Bindila L. Simultaneous lipidomic and transcriptomic profiling in mouse brain punches of acute epileptic seizure model compared to controls. J Lipid Res. 2017 Dec 5. pii: jlr.M080093. doi: 10.1194/jlr.M080093. [Epub ahead of print]

Deis S, Srivastava RK, Ruiz de Azua I, Bindila L, Baraghithy S, Lutz B, Bab I, Tam J (2017) Age-related regulation of bone formation by the sympathetic cannabinoid CB1 receptor. Bone 108:34-42.

Fuss J, Bindila L, Wiedemann K, Auer MK, Briken P, Biedermann SV (2017) Masturbation to Orgasm Stimulates the Release of the Endocannabinoid 2-Arachidonoylglycerol in Humans. J Sex Med. 2017 Nov;14(11):1372-1379. doi: 10.1016/j.jsxm.2017.09.016.

Scott AJ, Post JM, Lerner R, Ellis SR, Lieberman J, Shirey KA, Heeren RMA, Bindila L, Ernst RK (2017) Host-based lipid inflammation drives pathogenesis in Francisella infection. Proc Natl Acad Sci U S A. 2017 Nov 6. pii: 201712887. doi: 10.1073/pnas.1712887114. [Epub ahead of print]

Ruiz de Azua I, Mancini G, Srivastava RK, Rey AA, Cardinal P, Tedesco L, Zingaretti CM, Sassmann A, Quarta C, Schwitter C, Conrad A, Wettschureck N, Vemuri VK, Makriyannis A, Hartwig J, Mendez-Lago M, Bindila L, Monory K, Giordano A, Cinti S, Marsicano G, Offermanns S, Nisoli E, Pagotto U, Cota D, Lutz B (2017) Adipocyte cannabinoid receptor CB1 regulates energy homeostasis and alternatively activated macrophages.J Clin Invest 127(11):4148-4162. doi: 10.1172/JCI83626. Epub 2017 Oct 16.

Schreiner F, Ackermann M, Michalik M, Hucklenbruch-Rother E, Bilkei-Gorzo A, Racz I, Bindila L, Lutz B, Dötsch J, Zimmer A, Woelfle J (2017) Developmental programming of somatic growth, behavior and endocannabinoid metabolism by variation of early postnatal nutrition in a cross-fostering mouse model. PLoS One 12(8):e0182754. doi: 10.1371/journal.pone.0182754. eCollection 2017.

van den Bruck R, Weil PP, Ziegenhals T, Schreiner P, Juranek S, Gödde D, Vogel S, Schuster F, Orth V, Dörner J, Pembaur D, Röper M, Störkel S, Zirngibl H, Wirth S, Jenke ACW, Postberg J, Boy N, Heringer J, Haege G, Glahn EM, Hoffmann GF, Garbade SF, Burgard P, Kölker S, Chao CM, Yahya F, Moiseenko A, Shrestha A, Ahmadvand N, Quantius J, Wilhelm J, El-Agha E, Zimmer KP, Bellusci S, Staufner C, Kölker S, Prokisch H, Hoffmann GF, Seeliger S, Müller M, Hippe A, Steinkraus H, Wauer R, Lachmann B, Hofmann SR, Hedrich CM, Zierk J, Arzideh F, Haeckel R, Rascher W, Rauh M, Metzler M, Thieme S, Bandoła J, Richter C, Ryser M, Jamal A, Ashton MP, von Bonin M, Kuhn M, Hedrich CM, Bonifacio E, Berner R, Brenner S, Hammersen J, Has C, Naumann-Bartsch N, Stachel D, Kiritsi D, Söder S, Tardieu M, Metzler M, Bruckner-Tuderman L, Schneider H, Bohne F, Langer D, Cencic R, Eggermann T, Zechner U, Pelletier J, Zepp F, Enklaar T, Prawitt D, Pech M, Weckmann M, Heinsen FA, Franke A, Happle C, Dittrich AM, Hansen G, Fuchs O, von Mutius E, Oliver BG, Kopp MV, Paret C, Russo A, Theruvath J, Keller B, El Malki K, Lehmann N, Wingerter A, Neu MA, Aslihan GA, Wagner W, Sommer C, Pietsch T, Seidmann L, Faber J, Schreiner F, Ackermann M, Michalik M, Rother E, Bilkei-Gorzo A, Racz I, Bindila L, Lutz B, Dötsch J, Zimmer A, Woelfle J, Fischer HS, Ullrich TL, Bührer C, Czernik C, Schmalisch G, Stein R, Hofmann SR, Hagenbuchner J, Kiechl-Kohlendorfer U, Obexer P, Ausserlechner MJ, Loges NT, Frommer AT, Wallmeier J, Omran H, Öner-Sieben S, Gimpfl M, Rozman J, Irmler M, Beckers J, De Angelis MH, Roscher A, Wolf E, Ensenauer R, Nemes K, Frühwald M, Hasselblatt M, Siebert R, Kordes U, Kool M, Wang H, Hardy H, Refai O, Barwick KES, Zimmerman HH, Weis J, Baple EL, Crosby AH, Cirak S, Hellmuth C, Uhl O, Standl M, Heinrich J, Thiering E, Koletzko B, Blümel L, Kerl K, Picard D, Frühwald MC, Liebau MC, Reifenberger G, Borkhardt A, Hasselblatt M, Remke M, Tews D, Wabitsch M, Fischer-Posovszky P, Westhoff MA, Nonnenmacher L, Langhans J, Schneele L, Trenkler N, Debatin KM (2017) Abstracts of the 52nd Workshop for Pediatric Research : Frankfurt, Germany. 27-28 October 2016. Mol Cell Pediatr 4(Suppl 1):5. doi: 10.1186/s40348-017-0071-0.

Ramírez-López MT, Vázquez M, Lomazzo E, Hofmann C, Blanco RN, Alén F, Antón M, Decara J, Arco R, Orio L, Suárez J, Lutz B, Gómez de Heras R, Bindila L, Rodríguez de Fonseca F (2017) A moderate diet restriction during pregnancy alters the levels of endocannabinoids and endocannabinoid-related lipids in the hypothalamus, hippocampus and olfactory bulb of rat offspring in a sex-specific manner PLoS One 12(3):e0174307. doi: 10.1371/journal.pone.0174307. eCollection 2017.

Kranaster L, Hoyer C, Aksay SS, Bumb JM, Leweke FM, Janke C, Thiel M, Lutz B, Bindila L, Sartorius A (2017) Electroconvulsive therapy enhances endocannabinoids in the cerebrospinal fluid of patients with major depression: a preliminary prospective study. Eur Arch Psychiatry Clin Neurosci doi: 10.1007/s00406-017-0789-7. [Epub ahead of print]

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(2):255-267. doi: 10.1016/j.bbalip.2016.11.008.

Ramírez-López MT, Vázquez M, Bindila L, Lomazzo E, Hofmann C, Blanco RN, Alén F, Antón M, Decara J, Arco R, Ouro D, Orio L, Suárez J, Lutz B, Gómez de Heras R, Rodríguez de Fonseca F (2016) Maternal Caloric Restriction Implemented during the Preconceptional and Pregnancy Period Alters Hypothalamic and Hippocampal Endocannabinoid Levels at Birth and Induces Overweight and Increased Adiposity at Adulthood in Male Rat Offspring. Front Behav Neurosci 10:208. eCollection 2016.

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. eCollection 2016.

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. doi: 10.1016/j.yhbeh.2016.09.007.

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(35):9904-9. doi: 10.1073/pnas.1525066113.

Bindila L, Lutz B (2016) Extraction and Simultaneous Quantification of Endocannabinoids and Endocannabinoid-Like Lipids in Biological Tissues. Methods Mol Biol 1412:9-18. doi: 10.1007/978-1-4939-3539-0_2.

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(6):603-12. doi: 10.1007/s00210-016-1226-6.

Ramírez-López MT, Vázquez M, Bindila L, Lomazzo E, Hofmann C, Blanco RN, Alén F, 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. doi: 10.3389/fnbeh.2015.00339. eCollection 2015

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(1):e0146267. doi: 10.1371/journal.pone.0146267. eCollection 2016

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. doi: 10.1155/2015/456582.

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. doi: 10.3389/fncel.2015.00379. eCollection 2015

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 U S A 112(42):13105-8. doi: 10.1073/pnas.1514996112.

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. doi: 10.1016/j.mad.2015.08.005.

Guggenhuber S, Romo-Parra H, Bindila L, Leschik J, Lomazzo E, Remmers F, Zimmermann T, Lerner R, Klugmann M, Pape HC, Lutz B (2015) Impaired 2-AG Signaling in Hippocampal Glutamatergic Neurons: Aggravation of Anxiety-Like Behavior and Unaltered Seizure Susceptibility. Int J Neuropsychopharmacol 19(2). doi: 10.1093/ijnp/pyv091

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(10):858-68. doi: 10.1016/j.biopsych.2015.03.033

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(12):1145-50. doi: 10.1055/s-0035-1549397.

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. doi: 10.3389/fncel.2015.00098. eCollection 2015

Bilgin M, Bindila L, Graessler J, Shevchenko A (2015) Quantitative profiling of endocannabinoids in lipoproteins by LC-MS/MS. Anal Bioanal Chem 407(17):5125-31. doi: 10.1007/s00216-015-8559-8.

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. doi: 10.1016/j.lfs.2014.11.005.

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.

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(2):488-501. doi: 10.1038/npp.2014.198.

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 Arch Pharmacol 387(7):621-8. doi: 10.1007/s00210-014-0991-3.

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(46):18710-5. doi: 10.1073/pnas.1308130110.

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(20-21):976-83.

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(6): 795-807.
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.

Kirsch S, Souady J, Mormann M, Bindila L, Peter-Katalinić J (2012) Ceramide Profiles of Human Serum Gangliosides GM2 and GD1a exhibit Cancer-associated Alterations. J Glycom Lipidom S2:005.

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(8): G873-87.

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.

Pamplona FA, Ferreira J, Menezes de Lima O Jr, Duarte FS, Bento AF, Forner S, Villarinho JG, Bellocchio 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(51): 21134-9.