Silencing relaxin-3 in nucleus incertus of adult rodents: A viral vector-based approach to investigate neuropeptide function

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Callander, Gabrielle E ^a   Ma, Sherie ^a   Ganella, Despina E ^a   Wimmer, Verena C ^a   Gundlach, Andrew L ^a   Thomas, Walter G ^b   Bathgate, Ross A D ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; MESSENGER RNA; MICRORNA; MICRORNA 499; NEURON SPECIFIC NUCLEAR PROTEIN; PARVOVIRUS VECTOR; RECEPTOR; RELAXIN 3; RELAXIN 3 RECEPTOR; UNCLASSIFIED DRUG;

ADULT ANIMAL; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BRAIN NERVE CELL; BRAIN TISSUE; CONTROLLED STUDY; FOOD INTAKE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LOCOMOTION; MALE; MICROSCOPY; MOLECULAR CLONING; NISSL SUBSTANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; NUCLEUS INCERTUS; PONTINE NUCLEUS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RODENT; TRANSGENE;

ANIMALS; CELL LINE; CELL NUCLEUS; DEPENDOVIRUS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC VECTORS; HUMANS; MICE; MICRORNAS; NEURONS; NEUROPEPTIDES; RATS; RELAXIN; RNA INTERFERENCE; TRANSDUCTION, GENETIC; TRANSGENES;

MUS; RATTUS; RODENTIA;

EID: 84864462528     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042300     Document Type: Article

References (51)

1. Bathgate RAD, Samuel CS, Burazin TCD, Layfield S, Claasz AA, et al. ((2002)) Human relaxin gene 3 (H3) and the equivalent mouse relaxin (M3) gene. Novel members of the relaxin peptide family. J Biol Chem 277:: 1148--1157.
2. Chan LJ, Hossain MA, Samuel CS, Separovic F, Wade JD, ((2011)) The relaxin peptide family-structure, function and clinical applications. Protein Pept Lett 18:: 220--229.
3. Wilkinson TN, Speed TP, Tregear GW, Bathgate RAD, ((2005)) Evolution of the relaxin-like peptide family. BMC Evol Biol 5:: 14.
4. Smith CM, Lawrence AJ, Sutton SW, Gundlach AL, ((2009)) Behavioral phenotyping of mixed background (129S5: B6) relaxin-3 knockout mice. Ann N Y Acad Sci 1160:: 236--241.
5. Smith CM, Shen PJ, Banerjee A, Bonaventure P, Ma S, et al. ((2010)) Distribution of relaxin-3 and RXFP3 within arousal, stress, affective, and cognitive circuits of mouse brain. J Comp Neurol 518:: 4016--4045.
6. Burazin TCD, Bathgate RAD, Macris M, Layfield S, Gundlach AL, et al. ((2002)) Restricted, but abundant, expression of the novel rat gene-3 (R3) relaxin in the dorsal tegmental region of brain. J Neurochem 82:: 1553--1557.
7. Ma S, Bonaventure P, Ferraro T, Shen PJ, Burazin TCD, et al. ((2007)) Relaxin-3 in GABA projection neurons of nucleus incertus suggests widespread influence on forebrain circuits via G-protein-coupled receptor-135 in the rat. Neuroscience 144:: 165--190.
8. Tanaka M, Iijima N, Miyamoto Y, Fukusumi S, Itoh Y, et al. ((2005)) Neurons expressing relaxin 3/INSL 7 in the nucleus incertus respond to stress. Eur J Neurosci 21:: 1659--1670.
9. Ma S, Olucha-Bordonau FE, Hossain MA, Lin F, Kuei C, et al. ((2009)) Modulation of hippocampal theta oscillations and spatial memory by relaxin-3 neurons of the nucleus incertus. Learn Mem 16:: 730--742.
10. Silvertown JD, Neschadim A, Liu HN, Shannon P, Walia JS, et al. ((2009)) Relaxin-3 and receptors in the human and rhesus brain and reproductive tissues. Regul Pept. 159:: 44--53.
11. Donizetti A, Grossi M, Pariante P, D'Aniello E, Izzo G, et al. ((2008)) Two neuron clusters in the stem of postembryonic zebrafish brain specifically express relaxin-3 gene: first evidence of nucleus incertus in fish. Dev Dyn 237:: 3864--3869.
12. Goto M, Swanson LW, Canteras NS, ((2001)) Connections of the nucleus incertus. J Comp Neurol 438:: 86--122.
13. Olucha-Bordonau FE, Teruel V, Barcia-Gonzalez J, Ruiz-Torner A, Valverde-Navarro AA, et al. ((2003)) Cytoarchitecture and efferent projections of the nucleus incertus of the rat. J Comp Neurol 464:: 62--97.
14. Bathgate RAD, Ivell R, Sanborn BM, Sherwood OD, Summers RJ, ((2006)) International Union of Pharmacology LVII: recommendations for the nomenclature of receptors for relaxin family peptides. Pharmacol Rev 58:: 7--31.
15. Liu C, Eriste E, Sutton S, Chen J, Roland B, et al. ((2003)) Identification of relaxin-3/Insl7 as an endogenous ligand for the orphan G-protein coupled receptor GPCR135. J Biol Chem 278:: 50754--64.
16. Sutton SW, Bonaventure P, Kuei C, Roland B, Chen J, et al. ((2004)) Distribution of G-protein-coupled receptor (GPCR)135 binding sites and receptor mRNA in the rat brain suggests a role for relaxin-3 in neuroendocrine and sensory processing. Neuroendocrinology 80:: 298--307.
17. Banerjee A, Shen PJ, Ma S, Bathgate RAD, Gundlach AL, ((2010)) Swim stress excitation of nucleus incertus and rapid induction of relaxin-3 expression via CRF1 activation. Neuropharmacology 58:: 145--155.
18. Tanaka M, ((2010)) Relaxin-3/insulin-like peptide 7, a neuropeptide involved in the stress response and food intake. FEBS J 277:: 4990--4997.
19. Watanabe Y, Miyamoto Y, Matsuda T, Tanaka M, ((2011)) Relaxin-3/INSL7 regulates the stress-response system in the rat hypothalamus. J Mol Neurosci 43:: 169--174.
20. McGowan BM, Stanley SA, Smith KL, White NE, Connolly MM, et al. ((2005)) Central relaxin-3 administration causes hyperphagia in male Wistar rats. Endocrinology 146:: 3295--3300.
21. McGowan BM, Stanley SA, Smith KL, Minnion JS, Donovan J, et al. ((2006)) Effects of acute and chronic relaxin-3 on food intake and energy expenditure in rats. Regul Pept. 136:: 72--77.
22. Hida T, Takahashi E, Shikata K, Hirohashi T, Sawai T, et al. ((2006)) Chronic intracerebroventricular administration of relaxin-3 increases body weight in rats. J Recept Signal Transduct Res 26:: 147--158.
23. McGowan BM, Stanley SA, White NE, Spangeus A, Patterson M, et al. ((2007)) Hypothalamic mapping of orexigenic action and Fos-like immunoreactivity following relaxin-3 administration in male Wistar rats. Am J Physiol Endocrinol Metab 292:: E913--919.
24. McGowan BM, Stanley SA, Donovan J, Thompson EL, Patterson M, et al. ((2008)) Relaxin-3 stimulates the hypothalamic-pituitary-gonadal axis. Am J Physiol Endocrinol Metab 295:: E278--286.
25. Smith CM, Hosken IT, Sutton SW, Lawrence AJ, Gundlach AL, ((2012)) Relaxin-3 null mutation mice display a circadian hypoactivity phenotype. Genes Brain Behav 11:: 94--104.
26. Kuei C, Sutton S, Bonaventure P, Pudiak C, Shelton J, et al. ((2007)) R3(BDelta23 27)R/I5 chimeric peptide, a selective antagonist for GPCR135 and GPCR142 over relaxin receptor LGR7: in vitro and in vivo characterization. J Biol Chem 282:: 25425--25435.
27. Haugaard-Kedstrom LM, Shabanpoor F, Hossain MA, Clark RJ, Ryan PJ, et al. ((2011)) Design, synthesis, and characterization of a single-chain peptide antagonist for the relaxin-3 receptor RXFP3. J Am Chem Soc 133:: 4965--4974.
28. Sutton SW, Shelton J, Smith C, Williams J, Yun S, et al. ((2009)) Metabolic and neuroendocrine responses to RXFP3 modulation in the central nervous system. Ann N Y Acad Sci 1160:: 242--249.
29. Watanabe Y, Tsujimura A, Takao K, Nishi K, Ito Y, et al. ((2011)) Relaxin-3-deficient mice showed slight alteration in anxiety-related behavior. Front Behav Neurosci 5:: 50.
30. Callander GE, Thomas WG, Bathgate RA, ((2009)) Development and optimization of microRNA against relaxin-3. Ann N Y Acad Sci 1160:: 261--264.
31. Hökfelt T, ((1991)) Neuropeptides in perspective: the last ten years. Neuron 7:: 867--879.
32. Kim KK, Adelstein RS, Kawamoto S, ((2009)) Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. J Biol Chem 284:: 31052--31061.
33. Livak KJ, Schmittgen TD, ((2001)) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:: 402--408.
34. Schmittgen TD, Livak KJ, ((2008)) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:: 1101--1108.
35. Smith CM, Shen PJ, Ma S, Sutton SW, Gundlach AL, ((2009)) Verification of a relaxin-3 knockout/LacZ reporter mouse as a model of relaxin-3 deficiency. Ann N Y Acad Sci 1160:: 259--260.
36. Cisse RS, Krebs-Kraft DL, Parent MB, ((2008)) Septal infusions of the hyperpolarization-activated cyclic nucleotide-gated channel (HCN-channel) blocker ZD7288 impair spontaneous alternation but not inhibitory avoidance. Behav Neurosci 122:: 549--556.
37. Lalonde R, ((2002)) The neurobiological basis of spontaneous alternation. Neurosci Biobehav Rev 26:: 91--104.
38. Stefani MR, Gold PE, ((1998)) Intra-septal injections of glucose and glibenclamide attenuate galanin-induced spontaneous alternation performance deficits in the rat. Brain Res 813:: 50--56.
39. Degroot A, Treit D, ((2003)) Septal GABAergic and hippocampal cholinergic systems interact in the modulation of anxiety. Neuroscience 117:: 493--501.
40. Crawley J, Goodwin FK, ((1980)) Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol Biochem Behav 13:: 167--170.
41. Hökfelt T, Broberger C, Xu ZQ, Sergeyev V, Ubink R, et al. ((2000)) Neuropeptides-an overview. Neuropharmacology 39:: 1337--1356.
42. Chauveau F, Lange MD, Jungling K, Lesting J, Seidenbecher T, et al. ((2012)) Prevention of stress-impaired fear extinction through neuropeptide S action in the lateral amygdala. Neuropsychopharmacology 37:: 1588--1599.
43. McLaughlin JP, Marton-Popovici M, Chavkin C, ((2003)) Kappa opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J Neurosci 23:: 5674--5683.
44. Miyamoto Y, Watanabe Y, Tanaka M, ((2008)) Developmental expression and serotonergic regulation of relaxin 3/INSL7 in the nucleus incertus of rat brain. Regul Pept 145:: 54--59.
45. Grimm D, Kay MA, Kleinschmidt JA, ((2003)) Helper virus-free, optically controllable, and two-plasmid-based production of adeno-associated virus vectors of serotypes 1 to 6. Mol Ther 7:: 839--850.
46. During MJ, Young D, Baer K, Lawlor P, Klugmann M, ((2003)) Development and optimization of adeno-associated virus vector transfer into the central nervous system. Methods Mol Med 76:: 221--236.
47. Zolotukhin S, Byrne BJ, Mason E, Zolotukhin I, Potter M, et al. ((1999)) Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield. Gene Ther 6:: 973--985.
48. Veldwijk MR, Topaly J, Laufs S, Hengge UR, Wenz F, et al. ((2002)) Development and optimization of a real-time quantitative PCR-based method for the titration of AAV-2 vector stocks. Mol Ther 6:: 272--278.
49. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. Amsterdam; Boston: Elsevier.
50. Ragozzino ME, Pal SN, Unick K, Stefani MR, Gold PE, ((1998)) Modulation of hippocampal acetylcholine release and spontaneous alternation scores by intrahippocampal glucose injections. J Neurosci 18:: 1595--1601.
51. Ma S, Sang Q, Lanciego JL, Gundlach AL, ((2009)) Localization of relaxin-3 in brain of Macaca fascicularis: Identification of a nucleus incertus in primate. J Comp Neurol 517:: 856--872.