nach oben

Acta Neurochirurgica

Erschienen in:

01.07.2013 | Experimental Research - Brain Injury

Intraperitoneal treatment with S100B enhances hippocampal neurogenesis in juvenile mice and after experimental brain injury

verfasst von: Andrea Kleindienst, Felicitas Grünbeck, Rolf Buslei, Irene Emtmann, Michael Buchfelder

Erschienen in: Acta Neurochirurgica | Ausgabe 7/2013

Einloggen, um Zugang zu erhalten

Abstract

Background

Neurogenesis is documented in adult mammals including humans, is promoted by neurotrophic factors, and constitutes an innate repair mechanism following brain injury. The glial neurotrophic protein S100B is released following various types of brain injuries, enhances hippocampal neurogenesis and improves cognitive function following brain injury in rats when applied intrathecally. The present study was designed to elucidate whether the beneficial effect of S100B on injury-induced neurogenesis can be confirmed in mice when applied intraperitoneally (i.p.), and whether this effect is dose-dependent.

Methods

Male juvenile mice were subjected to a unilateral parietal cryolesion or sham injury, and treated with S100B at 20nM, 200nM or vehicle i.p. once daily. Hippocampal progenitor cell proliferation was quantified following labelling with bromo-deoxyuridine (BrdU, 50 mg/KG i.p.) in the germinative area of the dentate gyrus, the subgranular zone (SGZ), on day 4 as well as on cell survival and migration to the granular cell layer (GCL) on day 28. Progenitor cell differentiation was assessed following colabelling with the glial marker GFAP and the neuronal marker NeuN.

Results

S100B enhanced significantly the early progenitor cell proliferation in the SGZ as well as cell survival and migration to the GCL, and promoted neuronal differentiation. While these effects were predominately dose-dependent, 200nM S100B failed to enhance the proliferation in the SGZ on day 4 post-injury.

Conclusion

We conclude that S100B participates in hippocampal neurogenesis after injury at lower nanomolar concentrations. Therefore S100B may serve as a potential adjunct treatment to promote neuroregeneration following brain damage.

Ahlemeyer B, Beier H, Semkova I, Schaper C, Krieglstein J (2000) S-100beta protects cultured neurons against glutamate- and staurosporine-induced damage and is involved in the antiapoptotic action of the 5 HT(1A)-receptor agonist, Bay x 3702. Brain Res 858:121–128PubMedCrossRef

Baker RN, Cancilla PA, Pollock PS, Frommes SP (1971) The movement of exogenous protein in experimental cerebral edema. An electron microscopic study after freeze-injury. J Neuropathol Exp Neurol 30:668–679PubMedCrossRef

Barger SW, Van Eldik LJ, Mattson MP (1995) S100 beta protects hippocampal neurons from damage induced by glucose deprivation. Brain Res 677:167–170PubMedCrossRef

Braun H, Schafer K, Hollt V (2002) BetaIII tubulin-expressing neurons reveal enhanced neurogenesis in hippocampal and cortical structures after a contusion trauma in rats. J Neurotrauma 19:975–983PubMedCrossRef

Brewton LS, Haddad L, Azmitia EC (2001) Colchicine-induced cytoskeletal collapse and apoptosis in N-18 neuroblastoma cultures is rapidly reversed by applied S-100beta. Brain Res 912:9–16PubMedCrossRef

Chen XH, Iwata A, Nonaka M, Browne KD, Smith DH (2003) Neurogenesis and glial proliferation persist for at least one year in the subventricular zone following brain trauma in rats. J Neurotrauma 20:623–631PubMedCrossRef

Dash PK, Mach SA, Moore AN (2001) Enhanced neurogenesis in the rodent hippocampus following traumatic brain injury. J Neurosci Res 63:313–319PubMedCrossRef

Donato R (2001) S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol 33:637–668PubMedCrossRef

Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317PubMedCrossRef

10.

Fazeli MS, Errington ML, Dolphin AC, Bliss TV (1990) Extracellular proteases and S100 protein in long-term potentiation in the dentate gyrus of the anaesthetized rat. Adv Exp Med Biol 268:369–375PubMed

11.

Ghanem G, Loir B, Morandini R, Sales F, Lienard D, Eggermont A, Lejeune F (2001) On the release and half-life of S100B protein in the peripheral blood of melanoma patients. Int J Cancer 94:586–590PubMedCrossRef

12.

Goncalves DS, Lenz G, Karl J, Goncalves CA, Rodnight R (2000) Extracellular S100B protein modulates ERK in astrocyte cultures. Neuroreport 11:807–809PubMedCrossRef

13.

Green AJ, Keir G, Thompson EJ (1997) A specific and sensitive ELISA for measuring S-100b in cerebrospinal fluid. J Immunol Methods 205:35–41PubMedCrossRef

14.

Guillery RW, Herrup K (1997) Quantification without pontification: choosing a method for counting objects in sectioned tissues. J Comp Neurol 386:2–7PubMedCrossRef

15.

Heizmann CW, Fritz G, Schafer BW (2002) S100 proteins: structure, functions and pathology. Front Biosci 7:d1356–1368PubMedCrossRef

16.

Herrmann M, Curio N, Jost S, Grubich C, Ebert AD, Fork ML, Synowitz H (2001) Release of biochemical markers of damage to neuronal and glial brain tissue is associated with short and long term neuropsychological outcome after traumatic brain injury. J Neurol Neurosurg Psychiatry 70:95–100PubMedCrossRef

17.

Hu J, Ferreira A, Van Eldik LJ (1997) S100beta induces neuronal cell death through nitric oxide release from astrocytes. J Neurochem 69:2294–2301PubMedCrossRef

18.

Huttunen HJ, Kuja-Panula J, Sorci G, Agneletti AL, Donato R, Rauvala H (2000) Coregulation of neurite outgrowth and cell survival by amphoterin and S100 proteins through receptor for advanced glycation end products (RAGE) activation. J Biol Chem 275:40096–40105PubMedCrossRef

19.

Iwasaki Y, Shiojima T, Kinoshita M (1997) S100 beta prevents the death of motor neurons in newborn rats after sciatic nerve section. J Neurol Sci 151:7–12PubMedCrossRef

20.

Kawai T, Takagi N, Miyake-Takagi K, Okuyama N, Mochizuki N, Takeo S (2004) Characterization of BrdU-positive neurons induced by transient global ischemia in adult hippocampus. J Cereb Blood Flow Metab 24:548–555PubMedCrossRef

21.

Kempermann G, Gast D, Gage FH (2002) Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 52:135–143PubMedCrossRef

22.

Klein JR, Hoon DS, Nangauyan J, Okun E, Cochran AJ (1989) S-100 protein stimulates cellular proliferation. Cancer Immunol Immunother 29:133–138PubMedCrossRef

23.

Kleindienst A, Harvey HB, Rice AC, Muller C, Hamm RJ, Gaab MR, Bullock MR (2004) Intraventricular infusion of the neurotrophic protein S100B improves cognitive recovery after fluid percussion injury in the rat. J Neurotrauma 21:541–547PubMedCrossRef

24.

Kleindienst A, McGinn MJ, Harvey HB, Colello RJ, Hamm RJ, Bullock MR (2005) Enhanced hippocampal neurogenesis by intraventricular S100B infusion is associated with improved cognitive recovery after traumatic brain injury. J Neurotrauma 22:645–655PubMedCrossRef

25.

Knerlich F, Schilling L, Gorlach C, Wahl M, Ehrenreich H, Siren AL (1999) Temporal profile of expression and cellular localization of inducible nitric oxide synthase, interleukin-1beta and interleukin converting enzyme after cryogenic lesion of the rat parietal cortex. Brain Res Mol Brain Res 68:73–87PubMedCrossRef

26.

Kornack DR, Rakic P (1999) Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc Natl Acad Sci USA 96:5768–5773PubMedCrossRef

27.

Landar A, Caddell G, Chessher J, Zimmer DB (1996) Identification of an S100A1/S100B target protein: phosphoglucomutase. Cell Calcium 20:279–285PubMedCrossRef

28.

Li Y, Wang J, Sheng JG, Liu L, Barger SW, Jones RA, Van Eldik LJ, Mrak RE, Griffin WS (1998) S100 beta increases levels of beta-amyloid precursor protein and its encoding mRNA in rat neuronal cultures. J Neurochem 71:1421–1428PubMedCrossRef

29.

Lu D, Goussev A, Chen J, Pannu P, Li Y, Mahmood A, Chopp M (2004) Atorvastatin reduces neurological deficit and increases synaptogenesis, angiogenesis, and neuronal survival in rats subjected to traumatic brain injury. J Neurotrauma 21:21–32PubMedCrossRef

30.

Lu D, Mahmood A, Zhang R, Copp M (2003) Upregulation of neurogenesis and reduction in functional deficits following administration of DEtA/NONOate, a nitric oxide donor, after traumatic brain injury in rats. J Neurosurg 99:351–361PubMedCrossRef

31.

Magavi SS, Leavitt BR, Macklis JD (2000) Induction of neurogenesis in the neocortex of adult mice. Nature 405:951–955PubMedCrossRef

32.

Mahmood A, Lu D, Chopp M (2004) Intravenous administration of marrow stromal cells (MSCs) increases the expression of growth factors in rat brain after traumatic brain injury. J Neurotrauma 21:33–39PubMedCrossRef

33.

Mahmood A, Lu D, Lu M, Chopp M (2003) Treatment of traumatic brain injury in adult rats with intravenous administration of human bone marrow stromal cells. Neurosurgery 53:697–702, discussion 702–693PubMedCrossRef

34.

McAdory BS, Van Eldik LJ, Norden JJ (1998) S100B, a neurotropic protein that modulates neuronal protein phosphorylation, is upregulated during lesion-induced collateral sprouting and reactive synaptogenesis. Brain Res 813:211–217PubMedCrossRef

35.

Mello e Souza T, Rohden A, Meinhardt M, Goncalves CA, Quillfeldt JA (2000) S100B infusion into the rat hippocampus facilitates memory for the inhibitory avoidance task but not for the open-field habituation. Physiol Behav 71:29–33PubMedCrossRef

36.

Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201–211PubMed

37.

Nishi M, Kawata M, Azmitia EC (1997) S100beta promotes the extension of microtubule associated protein2 (MAP2)-immunoreactive neurites retracted after colchicine treatment in rat spinal cord culture. Neurosci Lett 229:212–214PubMedCrossRef

38.

Nottebohm F (2002) Why are some neurons replaced in adult brain? J Neurosci 22:624–628PubMed

39.

O’Dowd BS, Zhao WQ, Ng KT, Robinson SR (1997) Chicks injected with antisera to either S-100 alpha or S-100 beta protein develop amnesia for a passive avoidance task. Neurobiol Learn Mem 67:197–206PubMedCrossRef

40.

Peskind ER, Griffin WS, Akama KT, Raskind MA, Van Eldik LJ (2001) Cerebrospinal fluid S100B is elevated in the earlier stages of Alzheimer’s disease. Neurochem Int 39:409–413PubMedCrossRef

41.

Petrova TV, Hu J, Van Eldik LJ (2000) Modulation of glial activation by astrocyte-derived protein S100B: differential responses of astrocyte and microglial cultures. Brain Res 853:74–80PubMedCrossRef

42.

Pleines UE, Morganti-Kossmann MC, Rancan M, Joller H, Trentz O, Kossmann T (2001) S-100 beta reflects the extent of injury and outcome, whereas neuronal specific enolase is a better indicator of neuroinflammation in patients with severe traumatic brain injury. J Neurotrauma 18:491–498PubMedCrossRef

43.

Raabe A, Seifert V (2000) Protein S-100B as a serum marker of brain damage in severe head injury: preliminary results. Neurosurg Rev 23:136–138PubMedCrossRef

44.

Reeves RH, Yao J, Crowley MR, Buck S, Zhang X, Yarowsky P, Gearhart JD, Hilt DC (1994) Astrocytosis and axonal proliferation in the hippocampus of S100b transgenic mice. Proc Natl Acad Sci USA 91:5359–5363PubMedCrossRef

45.

Rice AC, Khaldi A, Harvey HB, Salman NJ, White F, Fillmore H, Bullock MR (2003) Proliferation and neuronal differentiation of mitotically active cells following traumatic brain injury. Exp Neurol 183:406–417PubMedCrossRef

46.

Rickmann M, Wolff JR, Meyer DL (1995) Expression of S100 protein in the vestibular nuclei during compensation of unilateral labyrinthectomy symptoms. Brain Res 688:8–14PubMedCrossRef

47.

Rustandi RR, Drohat AC, Baldisseri DM, Wilder PT, Weber DJ (1998) The Ca(2+)-dependent interaction of S100B(beta beta) with a peptide derived from p53. Biochemistry 37:1951–1960PubMedCrossRef

48.

Sargin D, Hassouna I, Sperling S, Siren AL, Ehrenreich H (2009) Uncoupling of neurodegeneration and gliosis in a murine model of juvenile cortical lesion. Glia 57:693–702PubMedCrossRef

49.

Schmidt-Hieber C, Jonas P, Bischofberger J (2004) Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429:184–187PubMedCrossRef

50.

Selinfreund RH, Barger SW, Pledger WJ, Van Eldik LJ (1991) Neurotrophic protein S100 beta stimulates glial cell proliferation. Proc Natl Acad Sci USA 88:3554–3558PubMedCrossRef

51.

Sharp FR, Liu J, Bernabeu R (2002) Neurogenesis following brain ischemia. Brain Res Dev Brain Res 134:23–30PubMedCrossRef

52.

Shashoua VE, Hesse GW, Moore BW (1984) Proteins of the brain extracellular fluid: evidence for release of S-100 protein. J Neurochem 42:1536–1541PubMedCrossRef

53.

Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372–376PubMedCrossRef

54.

Siren AL, Knerlich F, Schilling L, Kamrowski-Kruck H, Hahn A, Ehrenreich H (2000) Differential glial and vascular expression of endothelins and their receptors in rat brain after neurotrauma. Neurochem Res 25:957–969PubMedCrossRef

55.

Siren AL, Radyushkin K, Boretius S, Kammer D, Riechers CC, Natt O, Sargin D, Watanabe T, Sperling S, Michaelis T, Price J, Meyer B, Frahm J, Ehrenreich H (2006) Global brain atrophy after unilateral parietal lesion and its prevention by erythropoietin. Brain 129:480–489PubMedCrossRef

56.

Song H, Stevens CF, Gage FH (2002) Astroglia induce neurogenesis from adult neural stem cells. Nature 417:39–44PubMedCrossRef

57.

Takasawa K, Kitagawa K, Yagita Y, Sasaki T, Tanaka S, Matsushita K, Ohstuki T, Miyata T, Okano H, Hori M, Matsumoto M (2002) Increased proliferation of neural progenitor cells but reduced survival of newborn cells in the contralateral hippocampus after focal cerebral ischemia in rats. J Cereb Blood Flow Metab 22:299–307PubMedCrossRef

58.

Van Eldik LJ, Zimmer DB (1987) Secretion of S-100 from rat C6 glioma cells. Brain Res 436:367–370PubMedCrossRef

59.

Whitaker-Azmitia PM, Murphy R, Azmitia EC (1990) Stimulation of astroglial 5-HT1A receptors releases the serotonergic growth factor, protein S-100, and alters astroglial morphology. Brain Res 528:155–158PubMedCrossRef

60.

Wilder PT, Rustandi RR, Drohat AC, Weber DJ (1998) S100B(betabeta) inhibits the protein kinase C-dependent phosphorylation of a peptide derived from p53 in a Ca2 + −dependent manner. Protein Sci 7:794–798PubMedCrossRef

61.

Yagita Y, Kitagawa K, Ohtsuki T, Takasawa K, Miyata T, Okano H, Hori M, Matsumoto M (2001) Neurogenesis by progenitor cells in the ischemic adult rat hippocampus. Stroke 32:1890–1896PubMedCrossRef

62.

Yoshimura S, Takagi Y, Harada J, Teramoto T, Thomas SS, Waeber C, Bakowska JC, Breakefield XO, Moskowitz MA (2001) FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc Natl Acad Sci USA 98:5874–5879PubMedCrossRef

63.

Yoshimura S, Teramoto T, Whalen MJ, Irizarry MC, Takagi Y, Qiu J, Harada J, Waeber C, Breakefield XO, Moskowitz MA (2003) FGF-2 regulates neurogenesis and degeneration in the dentate gyrus after traumatic brain injury in mice. J Clin Invest 112:1202–1210PubMed

64.

Zimmer DB, Van Eldik LJ (1986) Identification of a molecular target for the calcium-modulated protein S100. Fructose-1,6-bisphosphate aldolase. J Biol Chem 261:11424–11428PubMed

Titel: Intraperitoneal treatment with S100B enhances hippocampal neurogenesis in juvenile mice and after experimental brain injury
verfasst von: Andrea Kleindienst
Felicitas Grünbeck
Rolf Buslei
Irene Emtmann
Michael Buchfelder
Publikationsdatum: 01.07.2013
Verlag: Springer Vienna
Erschienen in: Acta Neurochirurgica / Ausgabe 7/2013
Print ISSN: 0001-6268
Elektronische ISSN: 0942-0940
DOI: https://doi.org/10.1007/s00701-013-1720-2

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

23.04.2024 | Demenz | Nachrichten

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Intraperitoneal treatment with S100B enhances hippocampal neurogenesis in juvenile mice and after experimental brain injury

Abstract

Background

Methods

Results

Conclusion

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Demenzkranke durch Antipsychotika vielfach gefährdet

Parkinson-Therapie im Wandel – aktuelle Leitlinie im Fokus

Auf diese Krankheiten bei Geflüchteten sollten Sie vorbereitet sein

Hustenstiller lindert Agitation bei Alzheimer

Update Neurologie

Springer Medizin

Abstract

Background

Methods

Results

Conclusion

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 7/2013

Intramedullary spinal cord astrocytomas: the influence of localization and tumor extension on resectability and functional outcome

“Triple R” tonsillar technique for the management of adult Chiari I malformation: surgical note

Fluorescein-guided surgery for grade IV gliomas with a dedicated filter on the surgical microscope: preliminary results in 12 cases

Answer to: “Sodium fluorescein-guided resection under the YELLOW 560-nm surgical microscope filter in malignant brain tumor surgery—a feasibility study” (April 2013, Volume 155, Issue 4, pp 693–69)

Transfacet screw fixation of the subaxial cervical spine—how I do it?

Mitigating effects of external ventricular drain usage in the management of severe head injury

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Demenzkranke durch Antipsychotika vielfach gefährdet

Parkinson-Therapie im Wandel – aktuelle Leitlinie im Fokus

Auf diese Krankheiten bei Geflüchteten sollten Sie vorbereitet sein

Hustenstiller lindert Agitation bei Alzheimer

Update Neurologie