Intranasal Delivery of a Methyllanthionine-Stabilized Galanin Receptor-2-Selective Agonist Reduces Acute Food Intake.


Journal

Neurotherapeutics : the journal of the American Society for Experimental NeuroTherapeutics
ISSN: 1878-7479
Titre abrégé: Neurotherapeutics
Pays: United States
ID NLM: 101290381

Informations de publication

Date de publication:
10 2021
Historique:
accepted: 30 10 2021
pubmed: 4 12 2021
medline: 31 3 2022
entrez: 3 12 2021
Statut: ppublish

Résumé

The regulatory (neuro)peptide galanin is widely distributed in the central and peripheral nervous systems, where it mediates its effects via three G protein-coupled receptors (GAL

Identifiants

pubmed: 34859381
doi: 10.1007/s13311-021-01155-x
pii: 10.1007/s13311-021-01155-x
pmc: PMC8804135
doi:

Substances chimiques

Peptides 0
Receptor, Galanin, Type 2 0
Receptors, Galanin 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2737-2752

Informations de copyright

© 2021. The Author(s).

Références

Tatemoto K, Rokaeus A, Jornvall H, McDonald TJ, Mutt V. Galanin - a novel biologically active peptide from porcine intestine. FEBS Lett 1983;164:124-128.
pubmed: 6197320 doi: 10.1016/0014-5793(83)80033-7
Lang R, Gundlach AL, Kofler B. The galanin peptide family: receptor pharmacology, pleiotropic biological actions, and implications in health and disease. Pharmacol Ther 2007;115:177-207.
pubmed: 17604107 doi: 10.1016/j.pharmthera.2007.05.009
Lang R, Gundlach AL, Holmes FE, et al. Physiology, signaling, and pharmacology of galanin peptides and receptors: three decades of emerging diversity. Pharmacol Rev 2015;67:118-175.
pubmed: 25428932 doi: 10.1124/pr.112.006536
Koller A, Bianchini R, Schlager S, Munz C, Kofler B, Wiesmayr S. The neuropeptide galanin modulates natural killer cell function. Neuropeptides 2017;64:109-115.
pubmed: 27837916 doi: 10.1016/j.npep.2016.11.002
Locker F, Lang AA, Koller A, Lang R, Bianchini R, Kofler B. Galanin modulates human and murine neutrophil activation in vitro. Acta Physiol (Oxf) 2015;213:595-602.
doi: 10.1111/apha.12444
Ramspacher A, Neudert M, Koller A, Schlager S, Kofler B, Brunner SM. Influence of the regulatory peptide galanin on cytokine expression in human monocytes. Annals of the New York Academy of Sciences 2019;1455:185-195.
pubmed: 31074091 pmcid: 6899851 doi: 10.1111/nyas.14111
Koller A, Brunner SM, Bianchini R, et al. Galanin is a potent modulator of cytokine and chemokine expression in human macrophages. Sci Rep 2019;9:7237.
pubmed: 31076613 pmcid: 6510899 doi: 10.1038/s41598-019-43704-7
Kyrkouli SE, Stanley BG, Leibowitz SF. Galanin: stimulation of feeding induced by medial hypothalamic injection of this novel peptide. European journal of pharmacology 1986;122:159-160.
pubmed: 2420618 doi: 10.1016/0014-2999(86)90175-5
Kyrkouli SE, Stanley BG, Seirafi RD, Leibowitz SF. Stimulation of feeding by galanin: anatomical localization and behavioral specificity of this peptide's effects in the brain. Peptides 1990;11:995-1001.
pubmed: 1704616 doi: 10.1016/0196-9781(90)90023-X
Crawley JN. The role of galanin in feeding behavior. Neuropeptides 1999;33:369-375.
pubmed: 10657514 doi: 10.1054/npep.1999.0049
Corwin RL, Robinson JK, Crawley JN. Galanin antagonists block galanin-induced feeding in the hypothalamus and amygdala of the rat. Eur J Neurosci 1993;5:1528-1533.
pubmed: 7506975 doi: 10.1111/j.1460-9568.1993.tb00221.x
Schick RR, Samsami S, Zimmermann JP, et al. Effect of galanin on food intake in rats: involvement of lateral and ventromedial hypothalamic sites. Am J Physiol 1993;264:R355-R361.
pubmed: 7680542
Jacoby AS, Hort YJ, Constantinescu G, Shine J, Iismaa TP. Critical role for GALR1 galanin receptor in galanin regulation of neuroendocrine function and seizure activity. Mol Brain Res 2002;107:195-200.
pubmed: 12487125 doi: 10.1016/S0169-328X(02)00451-5
Gottsch ML, Zeng H, Hohmann JG, Weinshenker D, Clifton DK, Steiner RA. Phenotypic analysis of mice deficient in the type 2 galanin receptor (GALR2). Mol Cell Biol 2005;25:4808-4811.
doi: 10.1128/MCB.25.11.4804-4811.2005
Wynick D, Bacon A. Targeted disruption of galanin: new insights from knock-out studies. Neuropeptides 2002;36:132-144.
pubmed: 12359504 doi: 10.1054/npep.2002.0888
Zorrilla EP, Brennan M, Sabino V, Lu X, Bartfai T. Galanin type 1 receptor knockout mice show altered responses to high-fat diet and glucose challenge. Physiol Behav 2007;91:479-485.
pubmed: 17223141 pmcid: 2080849 doi: 10.1016/j.physbeh.2006.11.011
Adams AC, Clapham JC, Wynick D, Speakman JR. Feeding behaviour in galanin knockout mice supports a role of galanin in fat intake and preference. Journal of neuroendocrinology 2008;20:199-206.
pubmed: 18088361 doi: 10.1111/j.1365-2826.2007.01638.x
Fuxe K, Marcellino D, Rivera A, et al. Receptor-receptor interactions within receptor mosaics. Impact on neuropsychopharmacology. Brain Res Rev 2008;58:415-452.
pubmed: 18222544
Fuxe K, Borroto-Escuela DO, Romero-Fernandez W, et al. On the existence and function of galanin receptor heteromers in the central nervous system. Front Endocrinol (Lausanne) 2012;3:127.
doi: 10.3389/fendo.2012.00127
Webling K, Runesson J, Lang A, Saar I, Kofler B, Langel U. Ala5-galanin (2-11) is a GAL2R specific galanin analogue. Neuropeptides 2016;60:75-82.
pubmed: 27592409 doi: 10.1016/j.npep.2016.08.008
Reyes-Alcaraz A, Lee YN, Son GH, et al. Development of Spexin-based Human Galanin Receptor Type II-Specific Agonists with Increased Stability in Serum and Anxiolytic Effect in Mice. Sci Rep 2016;6:21453.
pubmed: 26907960 pmcid: 4764904 doi: 10.1038/srep21453
Bedecs K, Langel U, Bartfai T. Metabolism of galanin and galanin (1-16) in isolated cerebrospinal fluid and spinal cord membranes from rat. Neuropeptides 1995;29:137-143.
pubmed: 8538874 doi: 10.1016/0143-4179(95)90015-2
Holst JJ, Bersani M, Hvidberg A, et al. On the effects of human galanin in man. Diabetologia 1993;36:653-657.
pubmed: 7689499 doi: 10.1007/BF00404076
Carey DG, Iismaa TP, Ho KY, et al. Potent effects of human galanin in man: growth hormone secretion and vagal blockade. The Journal of clinical endocrinology and metabolism 1993;77:90-93.
pubmed: 7686918
de Vries L, Reitzema-Klein CE, Meter-Arkema A, et al. Oral and pulmonary delivery of thioether-bridged angiotensin-(1-7). Peptides 2010;31:893-898.
pubmed: 20206220 doi: 10.1016/j.peptides.2010.02.015
Bosma T, Kuipers A, Bulten E, de Vries L, Rink R, Moll GN. Bacterial display and screening of posttranslationally thioether-stabilized peptides. Appl Environ Microbiol 2011;77:6794-6801.
pubmed: 21821759 pmcid: 3187086 doi: 10.1128/AEM.05550-11
Kluskens LD, Nelemans SA, Rink R, et al. Angiotensin-(1-7) with thioether bridge: an angiotensin-converting enzyme-resistant, potent angiotensin-(1-7) analog. J Pharmacol Exp Ther 2009;328:849-854.
pubmed: 19038778 doi: 10.1124/jpet.108.146431
Bosma T, Rink R, Moosmeier MA, Moll GN. Genetically Encoded Libraries of Constrained Peptides. Chembiochem 2019;20:1754-1758.
pubmed: 30794341
Kuipers A, Moll GN, Levy A, Krakovsky M, Franklin R. Cyclic angiotensin-(1–7) contributes to rehabilitation of animal performance in a rat model of cerebral stroke. Peptides 2020;123:170193.
Kuipers A, Moll GN, Wagner E, Franklin R. Efficacy of lanthionine-stabilized angiotensin-(1-7) in type I and type II diabetes mouse models. Peptides 2019;112:78-84.
pubmed: 30529303 doi: 10.1016/j.peptides.2018.10.015
Durik M, van Veghel R, Kuipers A, et al. The effect of the thioether-bridged, stabilized Angiotensin-(1–7) analogue cyclic ang-(1–7) on cardiac remodeling and endothelial function in rats with myocardial infarction. Int J Hypertens 2012;2012:536426.
Wösten-van Asperen RM, Lutter R, Specht PA, et al. Acute respiratory distress syndrome leads to reduced ratio of ACE/ACE2 activities and is prevented by angiotensin-(1-7) or an angiotensin II receptor antagonist. J Pathol 2011;225:618-627.
pubmed: 22009550 doi: 10.1002/path.2987
Nonaka N, Farr SA, Kageyama H, Shioda S, Banks WA. Delivery of galanin-like peptide to the brain: targeting with intranasal delivery and cyclodextrins. J Pharmacol Exp Ther 2008;325:513-519.
pubmed: 18270319 doi: 10.1124/jpet.107.132381
Medina G, Ji G, Gregoire S, Neugebauer V. Nasal application of neuropeptide S inhibits arthritis pain-related behaviors through an action in the amygdala. Mol Pain 2014;10:32.
pubmed: 24884567 pmcid: 4046088 doi: 10.1186/1744-8069-10-32
Meredith ME, Salameh TS, Banks WA. Intranasal Delivery of Proteins and Peptides in the Treatment of Neurodegenerative Diseases. AAPS J 2015;17:780-787.
pubmed: 25801717 pmcid: 4476983 doi: 10.1208/s12248-015-9719-7
Takenoya F, Hirako S, Wada N, et al. Regulation of Feeding Behavior and Energy Metabolism by Galanin-like Peptide (GALP): A Novel Strategy to Fight Against Obesity. Curr Pharm Des 2018;24:3926-3933.
pubmed: 30398112 doi: 10.2174/1381612824666181106111623
Rink R, Arkema-Meter A, Baudoin I, et al. To protect peptide pharmaceuticals against peptidases. J Pharmacol Toxicol Methods 2010;61:210-218.
pubmed: 20176117 doi: 10.1016/j.vascn.2010.02.010
Terzaghi BE, Sandine WE. Improved medium for lactic streptococci and their bacteriophages. Appl Microbiol 1975;29:807-813.
pubmed: 16350018 pmcid: 187084 doi: 10.1128/am.29.6.807-813.1975
Berger A, Lang R, Moritz K, et al. Galanin receptor subtype GalR2 mediates apoptosis in SH-SY5Y neuroblastoma cells. Endocrinology 2004;145:500-507.
pubmed: 14592962 doi: 10.1210/en.2003-0649
Brunner SM, Koller A, Stockinger J, et al. Validation of antibody-based tools for galanin research. Peptides 2019;120:170009.
Conklin BR, Farfel Z, Lustig KD, Julius D, Bourne HR. Substitution of three amino acids switches receptor specificity of Gq alpha to that of Gi alpha. Nature 1993;363:274-276.
pubmed: 8387644 doi: 10.1038/363274a0
Kim DK, Yun S, Son GH, et al. Coevolution of the spexin/galanin/kisspeptin family: Spexin activates galanin receptor type II and III. Endocrinology 2014;155:1864-1873.
pubmed: 24517231 doi: 10.1210/en.2013-2106
Murza A, Belleville K, Longpre JM, Sarret P, Marsault E. Stability and degradation patterns of chemically modified analogs of apelin-13 in plasma and cerebrospinal fluid. Biopolymers 2014;102:297-303.
pubmed: 24728860 doi: 10.1002/bip.22498
Kuipers A, de Boef E, Rink R, et al. NisT, the transporter of the lantibiotic nisin, can transport fully modified, dehydrated, and unmodified prenisin and fusions of the leader peptide with non-lantibiotic peptides. J Biol Chem 2004;279:22176-22182.
pubmed: 15044440 doi: 10.1074/jbc.M312789200
Kluskens LD, Kuipers A, Rink R, et al. Post-translational modification of therapeutic peptides by NisB, the dehydratase of the lantibiotic nisin. Biochemistry 2005;44:12827-12834.
pubmed: 16171398 doi: 10.1021/bi050805p
Rink R, Kluskens LD, Kuipers A, Driessen AJ, Kuipers OP, Moll GN. NisC, the cyclase of the lantibiotic nisin, can catalyze cyclization of designed nonlantibiotic peptides. Biochemistry 2007;46:13179-13189.
pubmed: 17929939 doi: 10.1021/bi700106z
Rink R, Kuipers A, de Boef E, et al. Lantibiotic structures as guidelines for the design of peptides that can be modified by lantibiotic enzymes. Biochemistry 2005;44:8873-8882.
pubmed: 15952794 doi: 10.1021/bi050081h
Rink R, Wierenga J, Kuipers A, et al. Production of dehydroamino acid-containing peptides by Lactococcus lactis. Appl Environ Microbiol 2007;73:1792-1796.
pubmed: 17261515 pmcid: 1828803 doi: 10.1128/AEM.02350-06
Gong Q, Li L, Wu X, Ma H. Pyroglutamate aminopeptidase 1 may be an indicator of cellular inflammatory response as revealed using a sensitive long-wavelength fluorescent probe. Chem Sci 2016;7:4694-4697.
pubmed: 30155117 pmcid: 6013796 doi: 10.1039/C6SC00951D
Robinson J, Smith A, Sturchler E, Tabrizifard S, Kamenecka T, McDonald P. Development of a high-throughput screening-compatible cell-based functional assay to identify small molecule probes of the galanin 3 receptor (GalR3). Assay Drug Dev Technol 2013;11:468-477.
pubmed: 24116939 pmcid: 3804082 doi: 10.1089/adt.2013.526
Schrodl F, Kaser-Eichberger A, Trost A, et al. Distribution of galanin receptors in the human eye. Exp Eye Res 2015;138:42-51.
pubmed: 26122049 doi: 10.1016/j.exer.2015.06.024
Kageyama H, Shiba K, Hirako S, et al. Anti-obesity effect of intranasal administration of galanin-like peptide (GALP) in obese mice. Sci Rep 2016;6:28200.
pubmed: 27323911 pmcid: 4914964 doi: 10.1038/srep28200
Lula I, Denadai AL, Resende JM, et al. Study of angiotensin-(1-7) vasoactive peptide and its beta-cyclodextrin inclusion complexes: complete sequence-specific NMR assignments and structural studies. Peptides 2007;28:2199-2210.
pubmed: 17904691 doi: 10.1016/j.peptides.2007.08.011
Sollenberg U, Lindström L, Bartfai T, Langel U. M871—A novel peptide antagonist selectively recognizing the galanin receptor type 2 Int J Pept Res Ther 2006;12:115–119.
Metcalf CS, Smith MD, Klein BD, McDougle DR, Zhang L, Bulaj G. Preclinical Analgesic and Safety Evaluation of the GalR2-preferring Analog, NAX 810-2. Neurochem Res 2017;42:1983-1994.
pubmed: 28382595 pmcid: 5505798 doi: 10.1007/s11064-017-2229-5
Yun S, Reyes-Alcaraz A, Lee YN, et al. Spexin-Based Galanin Receptor Type 2 Agonist for Comorbid Mood Disorders and Abnormal Body Weight. Front Neurosci 2019;13:391.
pubmed: 31057364 pmcid: 6482256 doi: 10.3389/fnins.2019.00391
Liu HX, Brumovsky P, Schmidt R, et al. Receptor subtype-specific pronociceptive and analgesic actions of galanin in the spinal cord: selective actions via GalR1 and GalR2 receptors. Proc Natl Acad Sci U S A 2001;98:9960-9964.
pubmed: 11481429 pmcid: 55560 doi: 10.1073/pnas.161293598
Lu X, Lundstrom L, Bartfai T. Galanin (2-11) binds to GalR3 in transfected cell lines: limitations for pharmacological definition of receptor subtypes. Neuropeptides 2005;39:165-167.
pubmed: 15944007 doi: 10.1016/j.npep.2004.12.013
Jurkowski W, Yazdi S, Elofsson A. Ligand binding properties of human galanin receptors. Mol Membr Biol 2013;30:206-216.
pubmed: 23237663 doi: 10.3109/09687688.2012.750384
Szczeklik A, Szewczuk A, Nowosad H, Kolaczkowska B. Serum peptidases in myocardial infarction. Br Heart J 1972;34:232-237.
pubmed: 5015019 pmcid: 458463 doi: 10.1136/hrt.34.3.232
Kim HY, Hwang JI, Moon MJ, Seong JY. A Novel Long-Acting Glucagon-Like Peptide-1 Agonist with Improved Efficacy in Insulin Secretion and beta-Cell Growth. Endocrinol Metab (Seoul) 2014;29:320-327.
doi: 10.3803/EnM.2014.29.3.320
Saar I, Runesson J, Jarv J, Kurrikoff K, Langel U. Novel galanin receptor subtype specific ligand in depression like behavior. Neurochem Res 2013;38:398-404.
pubmed: 23192661 doi: 10.1007/s11064-012-0933-8
Webling KE, Runesson J, Bartfai T, Langel U. Galanin receptors and ligands. Front Endocrinol (Lausanne) 2012;3:146.
Metcalf CS, Klein BD, McDougle DR, et al. Analgesic properties of a peripherally acting and GalR2 receptor-preferring galanin analog in inflammatory, neuropathic, and acute pain models. J Pharmacol Exp Ther 2015;352:185-193.
pubmed: 25347995 pmcid: 4279104 doi: 10.1124/jpet.114.219063
White HS, Scholl EA, Klein BD, et al. Developing novel antiepileptic drugs: characterization of NAX 5055, a systemically-active galanin analog, in epilepsy models. Neurotherapeutics 2009;6:372-380.
pubmed: 19332332 pmcid: 4402707 doi: 10.1016/j.nurt.2009.01.001
Jacoby AS, Hort YJ, Constantinescu G, Shine J, Iismaa TP. Critical role for GALR1 galanin receptor in galanin regulation of neuroendocrine function and seizure activity. Brain Res Mol Brain Res 2002;107:195-200.
pubmed: 12487125 doi: 10.1016/S0169-328X(02)00451-5
Gottsch ML, Zeng H, Hohmann JG, Weinshenker D, Clifton DK, Steiner RA. Phenotypic analysis of mice deficient in the type 2 galanin receptor (GALR2). Mol Cell Biol 2005;25:4804-4811.
pubmed: 15899880 pmcid: 1140643 doi: 10.1128/MCB.25.11.4804-4811.2005
Saar I, Runesson J, McNamara I, Jarv J, Robinson JK, Langel U. Novel galanin receptor subtype specific ligands in feeding regulation. Neurochem Int 2011;58:714-720.
pubmed: 21333705 doi: 10.1016/j.neuint.2011.02.012
Krasnow SM, Hohmann JG, Gragerov A, Clifton DK, Steiner RA. Analysis of the contribution of galanin receptors 1 and 2 to the central actions of galanin-like peptide. Neuroendocrinology 2004;79:268-277.
pubmed: 15249737 doi: 10.1159/000079632
Wraith DC, Pope R, Butzkueven H, et al. A role for galanin in human and experimental inflammatory demyelination. Proc Natl Acad Sci U S A 2009;106:15466-15471.
pubmed: 19717462 pmcid: 2732706 doi: 10.1073/pnas.0903360106
Zhang L, Yu W, Schroedter I, Kong J, Vrontakis M. Galanin transgenic mice with elevated circulating galanin levels alleviate demyelination in a cuprizone-induced MS mouse model. PLoS One 2012;7:e33901.
Garcia-Rosa S, Trivella DB, Marques VD, et al. A non-functional galanin receptor-2 in a multiple sclerosis patient. Pharmacogenomics J 2019;19:72-82.
pubmed: 30131588 doi: 10.1038/s41397-018-0032-6

Auteurs

Anneke Kuipers (A)

Lanthio Health B.V., Rozenburglaan 13B, 9727 DL, Groningen, Netherlands.

Márta Balaskó (M)

Institute for Translational Medicine, Medical School, University of Pécs, 12 Szigeti út, H-7624, Pécs, Hungary.

Erika Pétervári (E)

Institute for Translational Medicine, Medical School, University of Pécs, 12 Szigeti út, H-7624, Pécs, Hungary.

Andreas Koller (A)

Research Program for Receptor Biochemistry and Tumor Metabolism, Department of Pediatrics, University Hospital of the Paracelsus Medical University, Muellner Hauptstr. 48, 5020, Salzburg, Austria.
Research Program for Experimental Ophthalmology, Department of Ophthalmology and Optometry, University Hospital of the Paracelsus Medical University, Salzburg, Austria.

Susanne M Brunner (SM)

Research Program for Receptor Biochemistry and Tumor Metabolism, Department of Pediatrics, University Hospital of the Paracelsus Medical University, Muellner Hauptstr. 48, 5020, Salzburg, Austria.
Research Program for Experimental Ophthalmology, Department of Ophthalmology and Optometry, University Hospital of the Paracelsus Medical University, Salzburg, Austria.

Gert N Moll (GN)

Lanthio Health B.V., Rozenburglaan 13B, 9727 DL, Groningen, Netherlands.
Department of Molecular Genetics, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Nijenborgh 7, 9747 AG, Groningen, Netherlands.

Barbara Kofler (B)

Research Program for Receptor Biochemistry and Tumor Metabolism, Department of Pediatrics, University Hospital of the Paracelsus Medical University, Muellner Hauptstr. 48, 5020, Salzburg, Austria. b.kofler@salk.at.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH