Neuropeptides
Volume 46, Issue 1 , Pages 19-27 , February 2012

Changes in galanin and GalR1 gene expression in discrete brain regions after transient occlusion of the middle cerebral artery in female rats

  • Lovisa Holm

      Affiliations

    • Division of Clinical Chemistry, Department of Clinical and Experimental Medicine, Faculty of Health Sciences, Linköping University, County Council of Östergötland, Linköping, Sweden
    • ,
  • Susanne Hilke

      Affiliations

    • Division of Clinical Chemistry, Department of Clinical and Experimental Medicine, Faculty of Health Sciences, Linköping University, County Council of Östergötland, Linköping, Sweden
    • ,
  • Csaba Adori

      Affiliations

    • Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden
    • ,
  • Elvar Theodorsson

      Affiliations

    • Division of Clinical Chemistry, Department of Clinical and Experimental Medicine, Faculty of Health Sciences, Linköping University, County Council of Östergötland, Linköping, Sweden
    • ,
  • Tomas Hökfelt

      Affiliations

    • Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden
    • ,
  • Annette Theodorsson

      Affiliations

    • Division of Clinical Chemistry, Department of Clinical and Experimental Medicine, Faculty of Health Sciences, Linköping University, County Council of Östergötland, Linköping, Sweden
    • Division of Neurosurgery, Department of Clinical and Experimental Medicine, Faculty of Health Sciences, Linköping University, County Council of Östergötland, Linköping, Sweden
    • Corresponding Author InformationCorresponding author at: Division of Neurosurgery, Department of Clinical and Experimental Medicine, Linköping University, SE-581 85 Linköping, Sweden. Tel.: +46 (0)101037585; fax: +46 (0)101033240.

Received 20 June 2011 ,Accepted 27 November 2011.

References 

  1. Agoston DV, Komoly S, Palkovits M. Selective up-regulation of neuropeptide synthesis by blocking the neuronal activity: galanin expression in septohippocampal neurons. Exp. Neurol. 1994;126:247–255
  2. Beal MF, MacGarvey U, Swartz KJ. Galanin immunoreactivity is increased in the nucleus basalis of Meynert in Alzheimer’s disease. Ann. Neurol. 1990;28:157–161
  3. Bederson JB, Pitts LH, Tsuji M, Nishimura MC, Davis RL, Bartkowski H. Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke. 1986;17:472–476
  4. Ben-Ari Y, Lazdunski M. Galanin protects hippocampal neurons from the functional effects of anoxia. Eur. J. Pharmacol. 1989;165:331–332
  5. Benveniste H. Glutamate, microdialysis, and cerebral ischemia: lost in translation?. Anesthesiology. 2009;110:422–425
  6. Bond BC, Virley DJ, Cairns NJ, Hunter AJ, Moore GB, Moss SJ, et al. The quantification of gene expression in an animal model of brain ischaemia using TaqMan real-time RT-PCR. Brain Res. Mol. Brain Res. 2002;106:101
  7. Branchek TA, Smith KE, Gerald C, Walker MW. Galanin receptor subtypes. Trends Pharmacol. Sci. 2000;21:109–117
  8. Brecht S, Buschmann T, Grimm S, Zimmermann M, Herdegen T. Persisting expression of galanin in axotomized mamillary and septal neurons of adult rats labeled for c-Jun and NADPH-diaphorase. Brain Res. Mol. Brain Res. 1997;48:7–16
  9. Burazin TC, Larm JA, Ryan MC, Gundlach AL. Galanin-R1 and -R2 receptor mRNA expression during the development of rat brain suggests differential subtype involvement in synaptic transmission and plasticity. Eur. J. Neurosci. 2000;12:2901–2917
  10. Calza L, Giardino L, Hokfelt T. Thyroid hormone-dependent regulation of galanin synthesis in neurons and glial cells after colchicine administration. Neuroendocrinology. 1998;68:428–436
  11. Ch’ng JL, Christofides ND, Anand P, Gibson SJ, Allen YS, Su HC, et al. Distribution of galanin immunoreactivity in the central nervous system and the responses of galanin-containing neuronal pathways to injury. Neuroscience. 1985;16:343–354
  12. Chan-Palay V. Galanin hyperinnervates surviving neurons of the human basal nucleus of Meynert in dementias of Alzheimer’s and Parkinson’s disease: a hypothesis for the role of galanin in accentuating cholinergic dysfunction in dementia. J. Comp. Neurol. 1988;273:543–557
  13. Cortes R, Villar MJ, Verhofstad A, Hokfelt T. Effects of central nervous system lesions on the expression of galanin: a comparative in situ hybridization and immunohistochemical study. Proc. Natl. Acad. Sci. USA. 1990;87:7742–7746
  14. Crawley JN. Functional interactions of galanin and acetylcholine: relevance to memory and Alzheimer’s disease. Behav. Brain Res. 1993;57:133–141
  15. De Michele M, Sancesario G, Toni D, Ciuffoli A, Bernardi G, Sette G. Specific expression of galanin in the peri-infarct zone after permanent focal cerebral ischemia in the rat. Regul. Pept. 2006;134:38–45
  16. Ding X, MacTavish D, Kar S, Jhamandas JH. Galanin attenuates beta-amyloid (Abeta) toxicity in rat cholinergic basal forebrain neurons. Neurobiol. Dis. 2006;21:413–420
  17. Elliott-Hunt CR, Marsh B, Bacon A, Pope R, Vanderplank P, Wynick D. Galanin acts as a neuroprotective factor to the hippocampus. Proc. Natl. Acad. Sci. USA. 2004;101:5105–5110
  18. Elliott-Hunt CR, Pope RJ, Vanderplank P, Wynick D. Activation of the galanin receptor 2 (GalR2) protects the hippocampus from neuronal damage. J. Neurochem. 2007;100:780–789
  19. Gabriel SM, Knott PJ, Haroutunian V. Alterations in cerebral cortical galanin concentrations following neurotransmitter-specific subcortical lesions in the rat. J. Neurosci. 1995;15:5526–5534
  20. Gabriel SM, Koenig JI, Kaplan LM. Galanin-like immunoreactivity is influenced by estrogen in peripubertal and adult rats. Neuroendocrinology. 1990;51:168–173
  21. Goldlust EJ, Paczynski RP, He YY, Hsu CY, Goldberg MP. Automated measurement of infarct size with scanned images of triphenyltetrazolium chloride-stained rat brains. Stroke. 1996;27:1657–1662
  22. Gubern C, Hurtado O, Rodriguez R, Morales JR, Romera VG, Moro MA, et al. Validation of housekeeping genes for quantitative real-time PCR in in-vivo and in-vitro models of cerebral ischaemia. BMC Mol. Biol. 2009;10:57
  23. Habert-Ortoli E, Amiranoff B, Loquet I, Laburthe M, Mayaux JF. Molecular cloning of a functional human galanin receptor. Proc. Natl. Acad. Sci. USA. 1994;91:9780–9783
  24. Harrison DC, Medhurst AD, Bond BC, Campbell CA, Davis RP, Philpott KL. The use of quantitative RT-PCR to measure mRNA expression in a rat model of focal ischemia–caspase-3 as a case study. Brain Res. Mol. Brain Res. 2000;75:143–149
  25. Heilig M. The NPY system in stress, anxiety and depression. Neuropeptides. 2004;38:213–224
  26. Hobson SA, Bacon A, Elliot-Hunt CR, Holmes FE, Kerr NC, Pope R, et al. Galanin acts as a trophic factor to the central and peripheral nervous systems. Cell Mol. Life Sci. 2008;65:1806–1812
  27. Holm L, Theodorsson E, Hokfelt T, Theodorsson A. Effects of intracerebroventricular galanin or a galanin receptor 2/3 agonist on the lesion induced by transient occlusion of the middle cerebral artery in female rats. Neuropeptides. 2011;45:17–23
  28. Holmes FE, Mahoney S, King VR, Bacon A, Kerr NC, Pachnis V, et al. Targeted disruption of the galanin gene reduces the number of sensory neurons and their regenerative capacity. Proc. Natl. Acad. Sci. USA. 2000;97:11563–11568
  29. Holmes PV, Blanchard DC, Blanchard RJ, Brady LS, Crawley JN. Chronic social stress increases levels of preprogalanin mRNA in the rat locus coeruleus. Pharmacol. Biochem. Behav. 1995;50:655–660
  30. Holmes PV, Crawley JN. Olfactory bulbectomy increases prepro-galanin mRNA levels in the rat locus coeruleus. Brain Res. Mol. Brain Res. 1996;36:184–188
  31. Hwang IK, Yoo KY, Kim DS, Do SG, Oh YS, Kang TC, et al. Expression and changes of galanin in neurons and microglia in the hippocampus after transient forebrain ischemia in gerbils. Brain Res. 2004;1023:193–199
  32. Hvid H, Ekstrom CT, Vienberg S, Oleksiewicz MB, Klopfleisch R. Identification of stable and oestrus cycle-independent housekeeping genes in the rat mammary gland and other tissues. Vet. J. 2010;190:103–108
  33. Hökfelt T, Wiesenfeld-Hallin Z, Villar M, Melander T. Increase of galanin-like immunoreactivity in rat dorsal root ganglion cells after peripheral axotomy. Neurosci. Lett. 1987;83:217–220
  34. Jacobowitz DM, Skofitsch G. Localization of galanin cell bodies in the brain by immunocytochemistry and in situ hybridization. In:  Hökfelt T,  Bartfai D,  Jacoboswitz D,  Ottoson D editor. Galanin – A new multifunctional peptide in the neuro-endocrine system. Wenner-Gren International Symposium Series 58. London: Macmillan Press Houndsmill; 1990;p. 69–92
  35. Johnson GD, Nogueira Araujo GM. A simple method of reducing the fading of immunofluorescence during microscopy. J. Immunol. Methods. 1981;43:349–350
  36. Kaplan LM, Gabriel SM, Koenig JI, Sunday ME, Spindel ER, Martin JB, et al. Galanin is an estrogen-inducible, secretory product of the rat anterior pituitary. Proc. Natl. Acad. Sci. USA. 1988;85:7408–7412
  37. Kerr BJ, Cafferty WB, Gupta YK, Bacon A, Wynick D, McMahon SB, et al. Galanin knockout mice reveal nociceptive deficits following peripheral nerve injury. Eur. J. Neurosci. 2000;12:793–802
  38. Kokaia M, Holmberg K, Nanobashvili A, Xu ZQ, Kokaia Z, Lendahl U, et al. Suppressed kindling epileptogenesis in mice with ectopic overexpression of galanin. Proc. Natl. Acad. Sci. USA. 2001;98:14006–14011
  39. Lee HY, Hwang IK, Kim DH, Kim JH, Kim CH, Lim BO, et al. Ischemia-related changes in galanin expression in the dentate hilar region after transient forebrain ischemia in gerbils. Exp. Anim. 2005;54:21–27
  40. Lerner JT, Sankar R, Mazarati AM. Galanin and epilepsy. EXS. 2010;102:183–194
  41. Liu HX, Brumovsky P, Schmidt R, Brown W, Payza K, Hodzic L, 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. USA. 2001;98:9960–9964
  42. 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
  43. Ma X, Tong YG, Schmidt R, Brown W, Payza K, Hodzic L, et al. Effects of galanin receptor agonists on locus coeruleus neurons. Brain Res. 2001;919:169–174
  44. Mahoney SA, Hosking R, Farrant S, Holmes FE, Jacoby AS, Shine J, et al. The second galanin receptor GalR2 plays a key role in neurite outgrowth from adult sensory neurons. J. Neurosci. 2003;23:416–421
  45. Mazarati A, Lu X, Kilk K, Langel U, Wasterlain C, Bartfai T. Galanin type 2 receptors regulate neuronal survival, susceptibility to seizures and seizure-induced neurogenesis in the dentate gyrus. Eur. J. Neurosci. 2004;19:3235–3244
  46. Mazarati AM, Hohmann JG, Bacon A, Liu H, Sankar R, Steiner RA, et al. Modulation of hippocampal excitability and seizures by galanin. J. Neurosci. 2000;20:6276–6281
  47. Mazarati AM, Liu H, Soomets U, Sankar R, Shin D, Katsumori H, et al. Galanin modulation of seizures and seizure modulation of hippocampal galanin in animal models of status epilepticus. J. Neurosci. 1998;18:10070–10077
  48. McEwen BS. Sex, stress and the hippocampus: allostasis, allostatic load and the aging process. Neurobiol. Aging. 2002;23:921
  49. Medhurst AD, Harrison DC, Read SJ, Campbell CA, Robbins MJ, Pangalos MN. The use of TaqMan RT-PCR assays for semiquantitative analysis of gene expression in CNS tissues and disease models. J. Neurosci. Methods. 2000;98:9–20
  50. Melander T, Hokfelt T, Rokaeus A. Distribution of galaninlike immunoreactivity in the rat central nervous system. J. Comp. Neurol. 1986;248:475–517
  51. Melander T, Hokfelt T, Rokaeus A, Cuello AC, Oertel WH, Verhofstad A, et al. Coexistence of galanin-like immunoreactivity with catecholamines, 5-hydroxytryptamine, GABA and neuropeptides in the rat CNS. J. Neurosci. 1986;6:3640–3654
  52. Melander T, Staines WA, Rokaeus A. Galanin-like immunoreactivity in hippocampal afferents in the rat, with special reference to cholinergic and noradrenergic inputs. Neuroscience. 1986;19:223–240
  53. Meldgaard M, Fenger C, Lambertsen KL, Pedersen MD, Ladeby R, Finsen B. Validation of two reference genes for mRNA level studies of murine disease models in neurobiology. J. Neurosci. Methods. 2006;156:101–110
  54. Mennicken F, Hoffert C, Pelletier M, Ahmad S, O’Donnell D. Restricted distribution of galanin receptor 3 (GalR3) mRNA in the adult rat central nervous system. J. Chem. Neuroanat. 2002;24:257–268
  55. Mitsukawa K, Lu X, Bartfai T. Galanin, galanin receptors, and drug targets. EXS. 2010;102:7–23
  56. Mufson EJ, Cochran E, Benzing W, Kordower JH. Galaninergic innervation of the cholinergic vertical limb of the diagonal band (Ch2) and bed nucleus of the stria terminalis in aging, Alzheimer’s disease and Down’s syndrome. Dementia. 1993;4:237–250
  57. O’Donnell D, Ahmad S, Wahlestedt C, Walker P. Expression of the novel galanin receptor subtype GALR2 in the adult rat CNS: distinct distribution from GALR1. J. Comp. Neurol. 1999;409:469–481
  58. O’Donnell, D., Mennicken, F., Hoffert, C., Hubatxch, D., Pelletier, M., Walker, P., Ahmad, S. Localization of galanin receptor subtypes in the rat CNS. Handbook of Chemical Neuroanatomy, 2003, pp. 195–244.
  59. O’Meara G, Coumis U, Ma SY, Kehr J, Mahoney S, Bacon A, et al. Galanin regulates the postnatal survival of a subset of basal forebrain cholinergic neurons. Proc. Natl. Acad. Sci. USA. 2000;97:11569–11574
  60. Pease, D.C., 1962. Buffered formaldehyde as a killing agent and primary fixative for electron microscopy. Anat. Rec. 142, 342.
  61. Pieribone VA, Xu ZQ, Zhang X, Grillner S, Bartfai T, Hokfelt T. Galanin induces a hyperpolarization of norepinephrine-containing locus coeruleus neurons in the brainstem slice. Neuroscience. 1995;64:861–874
  62. Pirondi S, Fernandez M, Schmidt R, Hokfelt T, Giardino L, Calza L. The galanin-R2 agonist AR-M1896 reduces glutamate toxicity in primary neural hippocampal cells. J. Neurochem. 2005;95:821–833
  63. Pirondi S, Giuliani A, Del Vecchio G, Giardino L, Hokfelt T, Calza L. The galanin receptor 2/3 agonist Gal2–11 protects the SN56 cells against beta-amyloid 25–35 toxicity. J. Neurosci. Res. 2010;88:1064–1073
  64. Platt JL, Michael AF. Retardation of fading and enhancement of intensity of immunofluorescence by p-phenylenediamine. J. Histochem. Cytochem. Off. J. Histochem. Soc. 1983;31:840–842
  65. Raghavendra Rao VL, Bowen KK, Dhodda VK, Song G, Franklin JL, Gavva NR, et al. Gene expression analysis of spontaneously hypertensive rat cerebral cortex following transient focal cerebral ischemia. J. Neurochem. 2002;83:1072–1086
  66. Rokaeus A, Melander T, Hokfelt T, Lundberg JM, Tatemoto K, Carlquist M, et al. A galanin-like peptide in the central nervous system and intestine of the rat. Neurosci. Lett. 1984;47:161–166
  67. Room P, Postema F, Korf J. Divergent axon collaterals of rat locus coeruleus neurons: demonstration by a fluorescent double labeling technique. Brain Res. 1981;221:219–230
  68. Seutin V, Verbanck P, Massotte L, Dresse A. Galanin decreases the activity of locus coeruleus neurons in vitro. Eur. J. Pharmacol. 1989;164:373–376
  69. Sevcik J, Finta EP, Illes P. Galanin receptors inhibit the spontaneous firing of locus coeruleus neurones and interact with mu-opioid receptors. Eur. J. Pharmacol. 1993;230:223–230
  70. Shen PJ, Larm JA, Gundlach AL. Expression and plasticity of galanin systems in cortical neurons, oligodendrocyte progenitors and proliferative zones in normal brain and after spreading depression. Eur. J. Neurosci. 2003;18:1362–1376
  71. Skofitsch G, Jacobowitz DM. Immunohistochemical mapping of galanin-like neurons in the rat central nervous system. Peptides. 1985;6:509–546
  72. Skofitsch G, Jacobowitz DM. Quantitative distribution of galanin-like immunoreactivity in the rat central nervous system. Peptides. 1986;7:609–613
  73. Sweerts BW, Jarrott B, Lawrence AJ. Expression of preprogalanin mRNA following acute and chronic restraint stress in brains of normotensive and hypertensive rats. Brain Res. Mol. Brain Res. 1999;69:113–123
  74. Tamura A, Graham DI, McCulloch J, Teasdale GM. Focal cerebral ischaemia in the rat: 1. Description of technique and early neuropathological consequences following middle cerebral artery occlusion. J. Cereb. Blood Flow Metab. 1981;1:53–60
  75. 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
  76. Thellin O, Zorzi W, Lakaye B, De Borman B, Coumans B, Hennen G, et al. Housekeeping genes as internal standards: use and limits. J. Biotechnol. 1999;75:291–295
  77. Theodorsson A, Holm L, Theodorsson E. Modern anesthesia and peroperative monitoring methods reduce per- and postoperative mortality during transient occlusion of the middle cerebral artery in rats. Brain Res. Brain Res. Protoc. 2005;14:181–190
  78. Theodorsson A, Holm L, Theodorsson E. Hypothermia-induced increase in galanin concentrations and ischemic neuroprotection in the rat brain. Neuropeptides. 2008;42:79–87
  79. Theodorsson A, Theodorsson E. Estradiol increases brain lesions in the cortex and lateral striatum after transient occlusion of the middle cerebral artery in rats: no effect of ischemia on galanin in the stroke area but decreased levels in the hippocampus. Peptides. 2005;26:2257–2264
  80. Theodorsson E, Rugarn O. Radioimmunoassay for rat galanin: immunochemical and chromatographic characterization of immunoreactivity in tissue extracts. Scand. J. Clin. Lab. Invest. 2000;60:411–418
  81. Tian YF, Zhang PB, Xiao XL, Zhang JS, Zhao JJ, Kang QY, et al. The quantification of ADAMTS expression in an animal model of cerebral ischemia using real-time PCR. Acta Anaesthesiol. Scand. 2007;51:158–164
  82. Valentino RJ, Van Bockstaele E. Convergent regulation of locus coeruleus activity as an adaptive response to stress. Eur. J. Pharmacol. 2008;583:194–203
  83. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., Speleman, F., 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, RESEARCH0034.
  84. Wang S, Gustafson EL. Galanin receptor subtypes. Drug News Perspect. 1998;11:458–468
  85. Waters SM, Krause JE. Distribution of galanin-1, -2 and -3 receptor messenger RNAs in central and peripheral rat tissues. Neuroscience. 2000;95:265–271
  86. Vila-Porcile E, Xu ZQ, Mailly P, Nagy F, Calas A, Hokfelt T, et al. Dendritic synthesis and release of the neuropeptide galanin: morphological evidence from studies on rat locus coeruleus neurons. J. Comp. Neurol. 2009;516:199–212
  87. Villar MJ, Cortes R, Theodorsson E, Wiesenfeld-Hallin Z, Schalling M, Fahrenkrug J, et al. Neuropeptide expression in rat dorsal root ganglion cells and spinal cord after peripheral nerve injury with special reference to galanin. Neuroscience. 1989;33:587–604
  88. Vrontakis ME, Peden LM, Duckworth ML, Friesen HG. Isolation and characterization of a complementary DNA (galanin) clone from estrogen-induced pituitary tumor messenger RNA. J. Biol. Chem. 1987;262:16755–16758
  89. Xu Z, Cortes R, Villar M, Morino P, Castel MN, Hokfelt T. Evidence for upregulation of galanin synthesis in rat glial cells in vivo after colchicine treatment. Neurosci. Lett. 1992;145:185–188
  90. Xu ZQ, Bartfai T, Langel U, Hokfelt T. Effects of three galanin analogs on the outward current evoked by galanin in locus coeruleus. Ann. NY Acad. Sci. 1998;863:459–465
  91. Xu ZQ, Shi TJ, Hokfelt T. Galanin/GMAP- and NPY-like immunoreactivities in locus coeruleus and noradrenergic nerve terminals in the hippocampal formation and cortex with notes on the galanin-R1 and -R2 receptors. J. Comp. Neurol. 1998;392:227–251
  92. Zamboni I, De Martino C. Buffered picric acid formaldehyde. A new rapid fixative for electron microscopy. J. Cell. Biol. 1967;35:148A
  93. Zigmond, R.E., 2001. Can galanin also be considered as growth-associated protein 3.2? Trends Neurosci. 24, 494–496 (discussion 496).
  94. Zigmond RE, Hyatt-Sachs H, Mohney RP, Schreiber RC, Shadiack AM, Sun Y, et al. Changes in neuropeptide phenotype after axotomy of adult peripheral neurons and the role of leukemia inhibitory factor. Perspect. Dev. Neurobiol. 1996;4:75–90

PII: S0143-4179(11)00103-X

doi: 10.1016/j.npep.2011.11.001

Neuropeptides
Volume 46, Issue 1 , Pages 19-27 , February 2012

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