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Enteric neurons from postnatal Fgf2 knockout mice differ in neurite outgrowth responses

  • C.I. Hagl
    Correspondence
    Corresponding author. Tel.: +49 621 383 3772.
    Affiliations
    Clinic of Pediatric Surgery, Medical Faculty Mannheim, University of Heidelberg, Theodor-Kutzer-Ufer 1-3, 68167 Mannheim, Germany
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  • E. Wink
    Affiliations
    Clinic of Pediatric Surgery, Medical Faculty Mannheim, University of Heidelberg, Theodor-Kutzer-Ufer 1-3, 68167 Mannheim, Germany
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  • C. Weiss
    Affiliations
    Institute for Medical Statistics, Medical Faculty Mannheim, University of Heidelberg, Ludolf-Krehl-Straße 13-17, 68167 Mannheim, Germany
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  • L. Wessel
    Affiliations
    Clinic of Pediatric Surgery, Medical Faculty Mannheim, University of Heidelberg, Theodor-Kutzer-Ufer 1-3, 68167 Mannheim, Germany
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  • N. Gretz
    Affiliations
    Medical Research Center, Medical Faculty Mannheim, University of Heidelberg, Theodor-Kutzer-Ufer 1-3, 68167 Mannheim, Germany
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  • K.H. Schäfer
    Affiliations
    Clinic of Pediatric Surgery, Medical Faculty Mannheim, University of Heidelberg, Theodor-Kutzer-Ufer 1-3, 68167 Mannheim, Germany

    University of Applied Sciences, Life Science, Department of Computer Sciences and Microsystems Technology, Amerikastrasse 1, 66482 Zweibrücken, Germany
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      Abstract

      The enteric nervous system (ENS) consists of several neuronal subclasses with distinct functional properties. The formation and maintenance of these distinct populations during development and aging is dependent on the support of appropriate neurotrophic factors. During early postnatal development, the ENS has to adept continuously to changing alimentation situations, which might also affect neuronal maturation and differentiation. There is evidence that basic-fibroblast-growth-factor (Fgf2) exerts neurotrophic effects in the ENS. In this study primary myenteric plexus cultures from both wild type and Fgf2-knockout mice were investigated under the influence of Fgf2 and glial-cell-line-derived-factor (GDNF). It could be demonstrated, that the influence of neurotrophic support is decreased in the Fgf2-knockouts, while the neuronal cultures of wild type revealed a more pronounced receptiveness for trophic support. These data show that Fgf2 plays a role in the development of the ENS.

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      References

        • Bikfalvi A.
        • Klein S.
        • Pintucci G.
        • Rifkin D.B.
        Biological roles of fibroblast growth factor-2.
        Endocr. Rev. 1997; 18: 26-45
        • Borghini S.
        • Duca M.D.
        • Pini Prato A.
        • Lerone M.
        • Martucciello G.
        • Jasonni V.
        • Ravazzolo R.
        • Ceccherini I.
        Search for pathogenetic variants of the SPRY2 gene in intestinal innervation defects.
        Intern. Med. J. 2009; 39: 335-337
        • Collins S.M.
        • Hurst S.M.
        • Main C.
        • Stanley E.
        • Khan I.
        • Blennerhassett P.
        • Swain M.
        Effect of inflammation of enteric nerves. Cytokine-induced changes in neurotransmitter content and release.
        Ann. N. Y. Acad. Sci. 1992; 664: 415-424
        • Di Nardo G.
        • Blandizzi C.
        • Volta U.
        • Colucci R.
        • Stanghellini V.
        • Barbara G.
        • Del Tacca M.
        • Tonini M.
        • Corinaldesi R.
        • De Giorgio R.
        Review article: molecular, pathological and therapeutic features of human enteric neuropathies.
        Aliment. Pharmacol. Ther. 2008; 28: 25-42
        • Dono R.
        • Texido G.
        • Dussel R.
        • Ehmke H.
        • Zeller R.
        Impaired cerebral cortex development and blood pressure regulation in FGF-2-deficient mice.
        EMBO J. 1998; 17: 4213-4225
        • Edgar D.
        The expression and interactions of laminin in the developing nervous system.
        Cell Differ. Dev. 1990; 32: 377-381
        • Edgar D.
        • Timpl R.
        • Thoenen H.
        The heparin-binding domain of laminin is responsible for its effects on neurite outgrowth and neuronal survival.
        EMBO J. 1984; 3: 1463-1468
        • Fichter M.
        • Klotz M.
        • Hirschberg D.L.
        • Waldura B.
        • Schofer O.
        • Ehnert S.
        • Schwarz L.K.
        • Ginneken C.V.
        • Schäfer K.H.
        Breast milk contains relevant neurotrophic factors and cytokines for enteric nervous system development.
        Mol. Nutr. Food Res. 2011; 55: 1592-1596
        • Fu M.
        • Sato Y.
        • Lyons-Warren A.
        • Zhang B.
        • Kane M.A.
        • Napoli J.L.
        • Heuckeroth R.O.
        Vitamin A facilitates enteric nervous system precursor migration by reducing Pten accumulation.
        Development. 2010; 137: 631-640
        • Furness J.
        The Enteric Nervous System.
        Blackwell, Oxford2006
        • Gross I.
        • Armant O.
        • Benosman S.
        • de Aguilar J.L.
        • Freund J.N.
        • Kedinger M.
        • Licht J.D.
        • Gaiddon C.
        • Loeffler J.P.
        Sprouty2 inhibits BDNF-induced signaling and modulates neuronal differentiation and survival.
        Cell Death Differ. 2007; 14: 1802-1812
        • Hagl C.I.
        • Holland-Cunz S.
        • Schafer K.H.
        What do knockout models teach us about the enteric nervous system?.
        Eur. J. Pediatr. Surg. 2003; 13: 170-175
        • Hagl C.I.
        • Thil O.
        • Holland-Cunz S.
        • Faissner R.
        • Wandschneider S.
        • Schnolzer M.
        • Lohr M.
        • Schäfer K.H.
        Proteome analysis of isolated myenteric plexus reveals significant changes in protein expression during postnatal development.
        Auton. Neurosci. 2005; 122: 1-8
        • Hagl C.I.
        • Klotz M.
        • Wink E.
        • Kranzle K.
        • Holland-Cunz S.
        • Gretz N.
        • Diener M.
        • Schäfer K.H.
        Temporal and regional morphological differences as a consequence of FGF-2 deficiency are mirrored in the myenteric proteome.
        Pediatr. Surg. Int. 2008; 24: 49-60
        • Hao M.M.
        • Young H.M.
        Development of enteric neuron diversity.
        J. Cell. Mol. Med. 2009; 13: 1193-1210
        • Hausott B.
        • Vallant N.
        • Auer M.
        • Yang L.
        • Dai F.
        • Brand-Saberi B.
        • Klimaschewski L.
        Sprouty2 down-regulation promotes axon growth by adult sensory neurons.
        Mol. Cell. Neurosci. 2009; 42: 328-340
        • Hausott B.
        • Vallant N.
        • Schlick B.
        • Auer M.
        • Nimmervoll B.
        • Obermair G.J.
        • Schwarzer C.
        • Dai F.
        • Brand-Saberi B.
        • Klimaschewski L.
        Sprouty2 and -4 regulate axon outgrowth by hippocampal neurons.
        Hippocampus. 2011; 22: 434-441
        • Impagnatiello M.A.
        • Weitzer S.
        • Gannon G.
        • Compagni A.
        • Cotten M.
        • Christofori G.
        Mammalian sprouty-1 and -2 are membrane-anchored phosphoprotein inhibitors of growth factor signaling in endothelial cells.
        J. Cell Biol. 2001; 152: 1087-1098
        • Ishida M.
        • Ichihara M.
        • Mii S.
        • Jijiwa M.
        • Asai N.
        • Enomoto A.
        • Kato T.
        • Majima A.
        • Ping J.
        • Murakumo Y.
        • Takahashi M.
        Sprouty2 regulates growth and differentiation of human neuroblastoma cells through RET tyrosine kinase.
        Cancer Sci. 2007; 98: 815-821
        • Israel E.J.
        Neonatal necrotizing enterocolitis, a disease of the immature intestinal mucosal barrier.
        Acta Paediatr. Suppl. 1994; 396: 27-32
        • Iwata T.
        • Hevner R.F.
        Fibroblast growth factor signaling in development of the cerebral cortex.
        Dev. Growth Differ. 2009; 51: 299-323
        • Johnson M.S.
        • Thomson S.C.
        • Speakman J.R.
        Limits to sustained energy intake. I. Lactation in the laboratory mouse Mus musculus.
        J. Exp. Biol. 2001; 204: 1925-1935
        • Lee P.L.
        • Johnson D.E.
        • Cousens L.S.
        • Fried V.A.
        • Williams L.T.
        Purification and complementary DNA cloning of a receptor for basic fibroblast growth factor.
        Science. 1989; 245: 57-60
        • Mason I.
        Initiation to end point: the multiple roles of fibroblast growth factors in neural development.
        Nat. Rev. Neurosci. 2007; 8: 583-596
        • Mason J.M.
        • Morrison D.J.
        • Basson M.A.
        • Licht J.D.
        Sprouty proteins: multifaceted negative-feedback regulators of receptor tyrosine kinase signaling.
        Trends Cell Biol. 2006; 16: 45-54
        • Meier-Ruge W.A.
        • Ammann K.
        • Bruder E.
        • Holschneider A.M.
        • Scharli A.F.
        • Schmittenbecher P.P.
        • Stoss F.
        Updated results on intestinal neuronal dysplasia (IND B).
        Eur. J. Pediatr. Surg. 2004; 14: 384-391
        • Miyamoto R.
        • Jijiwa M.
        • Asai M.
        • Kawai K.
        • Ishida-Takagishi M.
        • Mii S.
        • Asai N.
        • Enomoto A.
        • Murakumo Y.
        • Yoshimura A.
        • Takahashi M.
        Loss of Sprouty2 partially rescues renal hypoplasia and stomach hypoganglionosis but not intestinal aganglionosis in Ret Y1062F mutant mice.
        Dev. Biol. 2010; 349: 160-168
        • Neufeld G.
        • Gospodarowicz D.
        Basic and acidic fibroblast growth factors interact with the same cell surface receptors.
        J. Biol. Chem. 1986; 261: 5631-5637
        • Newgreen D.
        • Young H.M.
        Enteric nervous system: development and developmental disturbances—part 1.
        Pediatr. Dev. Pathol. 2002; 5: 224-247
        • Nurcombe V.
        Laminin in neural development.
        Pharmacol. Ther. 1992; 56: 247-264
        • Raballo R.
        • Rhee J.
        • Lyn-Cook R.
        • Leckman J.F.
        • Schwartz M.L.
        • Vaccarino F.M.
        Basic fibroblast growth factor (Fgf2) is necessary for cell proliferation and neurogenesis in the developing cerebral cortex.
        J. Neurosci. 2000; 20: 5012-5023
        • Reuss B.
        • von Bohlen und Halbach O.
        Fibroblast growth factors and their receptors in the central nervous system.
        Cell Tissue Res. 2003; 313: 139-157
        • Schäfer K.H.
        • Mestres P.
        The GDNF-induced neurite outgrowth and neuronal survival in dissociated myenteric plexus cultures of the rat small intestine decreases postnatally.
        Exp. Brain Res. 1999; 125: 447-452
        • Schäfer K.H.
        • Saffrey M.J.
        • Burnstock G.
        • Mestres-Ventura P.
        A new method for the isolation of myenteric plexus from the newborn rat gastrointestinal tract.
        Brain Res. Brain Res. Protoc. 1997; 1: 109-113
        • Simmonds A.
        • LaGamma E.F.
        Toward improving mucosal barrier defenses: rhG-CSF plus IgG antibody.
        Indian J. Pediatr. 2006; 73: 1019-1026
        • Skaba R.
        • Frantlova M.
        • Horak J.
        Intestinal neuronal dysplasia.
        Eur. J. Gastroenterol. Hepatol. 2006; 18: 699-701
        • Taketomi T.
        • Yoshiga D.
        • Taniguchi K.
        • Kobayashi T.
        • Nonami A.
        • Kato R.
        • Sasaki M.
        • Sasaki A.
        • Ishibashi H.
        • Moriyama M.
        • Nakamura K.
        • Nishimura J.
        • Yoshimura A.
        Loss of mammalian Sprouty2 leads to enteric neuronal hyperplasia and esophageal achalasia.
        Nat. Neurosci. 2005; 8: 855-857
        • Tsang M.
        • Dawid I.B.
        Promotion and attenuation of FGF signaling through the Ras-MAPK pathway.
        Sci. STKE. 2004; (pe 17)
        • Xue J.
        • Askwith C.
        • Javed N.H.
        • Cooke H.J.
        Autonomic nervous system and secretion across the intestinal mucosal surface.
        Auton. Neurosci. 2007; 133: 55-63
        • Yoneda A.
        • Wang Y.
        • O'Briain D.S.
        • Puri P.
        Cell-adhesion molecules and fibroblast growth factor signalling in Hirschsprung's disease.
        Pediatr. Surg. Int. 2001; 17: 299-303
        • Zhou F.Q.
        • Snider W.D.
        Intracellular control of developmental and regenerative axon growth.
        Philos. Trans. R Soc. Lond. B Biol. Sci. 2006; 361: 1575-1592
        • Zhou M.
        • Sutliff R.L.
        • Paul R.J.
        • Lorenz J.N.
        • Hoying J.B.
        • Haudenschild C.C.
        • Yin M.
        • Coffin J.D.
        • Kong L.
        • Kranias E.G.
        • Luo W.
        • Boivin G.P.
        • Duffy J.J.
        • Pawlowski S.A.
        • Doetschman T.
        Fibroblast growth factor 2 control of vascular tone.
        Nat. Med. 1998; 4: 201-207

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