Expression of SDF-1 and CXCR4 during Reorganization of the Postnatal Dentate GyrusBerger O. · Li G. · Han S.-M. · Paredes M. · Pleasure S.J.
Department of Neurology, Programs in Neuroscience and Developmental Biology, University of California, San Francisco, Calif., USA
Do you have an account?
- Rent for 48h to view
- Buy Cloud Access for unlimited viewing via different devices
- Synchronizing in the ReadCube Cloud
- Printing and saving restrictions apply
Rental: USD 8.50
Cloud: USD 20.00
Previous studies have demonstrated that stromal cell-derived factor 1 (SDF-1) is crucial for early dentate development; however, the mouse mutants for this chemokine and its only receptor, CXCR4, are neonatally lethal, making conclusions about the role of these molecules in postnatal development difficult to sustain. Previous expression analyses have used single labeling, but the distribution of CXCR4 is complex and to determine the cell types expressing CXCR4 requires multiple marker labeling. In this study, we examined the distribution of SDF-1 and CXCR4 mRNAs during the first postnatal weeks, combining these markers with several other cell-type-specific markers. We found that SDF-1 has three sites of expression: (1) continuation of prenatal expression in the meninges; (2) expression in Cajal-Retzius cells occupying the molecular layer of the upper and lower blades of the dentate, and (3) the maturing dentate granule neurons themselves. The timing of expression in these three sites corresponds to alterations in the distribution of the primary cell types expressing CXCR4 during the same periods, notably the expression of CXCR4 in radial-glial-like GFAP-expressing dentate precursors and immature dentate granule neurons. Taken together, our data suggest potential ongoing roles for SDF-1/CXCR4 signaling in the dentate gyrus during the early postnatal period that will be tested in the future with more precise genetic approaches.
© 2007 S. Karger AG, Basel
- Abraham H, Meyer G (2003): Reelin-expressing neurons in the postnatal and adult human hippocampal formation. Hippocampus 13:715–727.
- Altman J, Bayer SA (1990a): Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J Comp Neurol 301:325–342.
- Altman J, Bayer SA (1990b): Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301:365–381.
- Altman J, Das GD (1965): Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319–335.
- Altman J, Das GD (1966): Autoradiographic and histological studies of postnatal neurogenesis. 1. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis in some brain regions. J Comp Neurol 126:337–389.
- Bagri A, Gurney T, He X, Zou YR, Littman DR, Tessier-Lavigne M, Pleasure SJ (2002): The chemokine SDF1 regulates migration of dentate granule cells. Development 129:4249–4260.
- Banisadr G, Fontanges P, Haour F, Kitabgi P, Rostene W, Melik Parsadaniantz S (2002): Neuroanatomical distribution of CXCR4 in adult rat brain and its localization in cholinergic and dopaminergic neurons. Eur J Neurosci 16:1661–1671.
- Banisadr G, Skrzydelski D, Kitabgi P, Rostene W, Parsadaniantz SM (2003): Highly regionalized distribution of stromal cell-derived factor-1/CXCL12 in adult rat brain: constitutive expression in cholinergic, dopaminergic and vasopressinergic neurons. Eur J Neurosci 18:1593–1606.
- Belmadani A, Tran PB, Ren D, Assimacopoulos S, Grove EA, Miller RJ (2005): The chemokine stromal cell-derived factor-1 regulates the migration of sensory neuron progenitors. J Neurosci 25:3995–4003.
- Blasco-Ibanez JM, Freund TF (1997): Distribution, ultrastructure, and connectivity of calretinin-immunoreactive mossy cells of the mouse dentate gyrus. Hippocampus 7:307–320.
- Brandt MD, Jessberger S, Steiner B, Kronenberg G, Reuter K, Bick-Sander A, von der Behrens W, Kempermann G (2003): Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci 24:603–613.
- Cameron HA, McKay RD (2001): Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406–417.
- Chalasani SH, Sabelko KA, Sunshine MJ, Littman DR, Raper JA (2003): A chemokine, SDF-1, reduces the effectiveness of multiple axonal repellents and is required for normal axon pathfinding. J Neurosci 23:1360–1371.
- Eckenhoff MF, Rakic P (1984): Radial organization of the hippocampal dentate gyrus: a Golgi, ultrastructural, and immunocytochemical analysis in the developing rhesus monkey. J Comp Neurol 223:1–21.
- Eckenhoff MF, Rakic P (1988): Nature and fate of proliferative cells in the hippocampal dentate gyrus during the life span of the rhesus monkey. J Neurosci 8:2729–2747.
- Forster E, Tielsch A, Saum B, Weiss KH, Johanssen C, Graus-Porta D, Muller U, Frotscher M (2002): Reelin, Disabled 1, and beta 1 integrins are required for the formation of the radial glial scaffold in the hippocampus. Proc Natl Acad Sci USA 99:13178–13183.
- Frotscher M, Haas CA, Forster E (2003): Reelin controls granule cell migration in the dentate gyrus by acting on the radial glial scaffold. Cereb Cortex 13:634–640.
- Fujise N, Liu Y, Hori N, Kosaka T (1998): Distribution of calretinin immunoreactivity in the mouse dentate gyrus. 2. Mossy cells, with special reference to their dorsoventral difference in calretinin immunoreactivity. Neuroscience 82:181–200.
- Fukuda S, Kato F, Tozuka Y, Yamaguchi M, Miyamoto Y, Hisatsune T (2003): Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J Neurosci 23:9357–9366.
- Imitola J, Raddassi K, Park KI, Mueller FJ, Nieto M, Teng YD, Frenkel D, Li J, Sidman RL, Walsh CA, Snyder EY, Khoury SJ (2004): Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc Natl Acad Sci USA 101:18117–18122.
- Jiang M, Swann JW (1997): Expression of calretinin in diverse neuronal populations during development of rat hippocampus. Neuroscience 81:1137–1154.
- Kempermann G, Jessberger S, Steiner B, Kronenberg G (2004b): Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447–452.
- Kempermann G, Wiskott L, Gage FH (2004a): Functional significance of adult neurogenesis. Curr Opin Neurobiol 14:186–191.
- Klein RS, Rubin JB, Gibson HD, DeHaan EN, Alvarez-Hernandez X, Segal RA, Luster AD (2001): SDF-1 alpha induces chemotaxis and enhances Sonic hedgehog-induced proliferation of cerebellar granule cells. Development 128:1971–1981.
- Lazarini F, Tham TN, Casanova P, Arenzana-Seisdedos F, Dubois-Dalcq M (2003): Role of the alpha-chemokine stromal cell-derived factor (SDF-1) in the developing and mature central nervous system. Glia 42:139–148.
- Li G, Pleasure SJ (2005): Morphogenesis of the dentate gyrus: what we are learning from mouse mutants. Dev Neurosci 27:93–99.
- Liu Y, Fujise N, Kosaka T (1996): Distribution of calretinin immunoreactivity in the mouse dentate gyrus. 1. General description. Exp Brain Res 108:389–403.
- Lu M, Grove EA, Miller RJ (2002): Abnormal development of the hippocampal dentate gyrus in mice lacking the CXCR4 chemokine receptor. Proc Natl Acad Sci USA 99:7090–7095.
- Ni HT, Hu S, Sheng WS, Olson JM, Cheeran MC, Chan AS, Lokensgard JR, Peterson PK (2004): High-level expression of functional chemokine receptor CXCR4 on human neural precursor cells. Brain Res Dev Brain Res 152:159–169.
- Nowakowski RS, Rakic P (1981): The site of origin and route and rate of migration of neurons to the hippocampal region of the rhesus monkey. J Comp Neurol 196:129–154.
- Peng H, Huang Y, Rose J, Erichsen D, Herek S, Fujii N, Tamamura H, Zheng J (2004): Stromal cell-derived factor 1-mediated CXCR4 signaling in rat and human cortical neural progenitor cells. J Neurosci Res 76:35–50.
- Pleasure SJ, Collins AE, Lowenstein DH (2000): Unique expression patterns of cell fate molecules delineate sequential stages of dentate gyrus development. J Neurosci 20:6095–6105.
- Rakic P, Nowakowski RS (1981): The time of origin of neurons in the hippocampal region of the rhesus monkey. J Comp Neurol 196:99–128.
- Reiss K, Mentlein R, Sievers J, Hartmann D (2002): Stromal cell-derived factor 1 is secreted by meningeal cells and acts as chemotactic factor on neuronal stem cells of the cerebellar external granular layer. Neuroscience 115:295–305.
- Rubin JB, Kung AL, Klein RS, Chan JA, Sun Y, Schmidt K, Kieran MW, Luster AD, Segal RA (2003): A small-molecule antagonist of CXCR4 inhibits intracranial growth of primary brain tumors. Proc Natl Acad Sci USA 100:13513–13518.
- Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001): Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153–7160.
- 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 410:372–376.
- Stumm RK, Rummel J, Junker V, Culmsee C, Pfeiffer M, Krieglstein J, Hollt V, Schulz S (2002): A dual role for the SDF-1/CXCR4 chemokine receptor system in adult brain: isoform-selective regulation of SDF-1 expression modulates CXCR4-dependent neuronal plasticity and cerebral leukocyte recruitment after focal ischemia. J Neurosci 22:5865–5878.
- Stumm RK, Zhou C, Ara T, Lazarini F, Dubois-Dalcq M, Nagasawa T, Hollt V, Schulz S (2003): CXCR4 regulates interneuron migration in the developing neocortex. J Neurosci 23:5123–5130.
- Tham TN, Lazarini F, Franceschini IA, Lachapelle F, Amara A, Dubois-Dalcq M (2001): Developmental pattern of expression of the alpha chemokine stromal cell-derived factor 1 in the rat central nervous system. Eur J Neurosci 13:845–856.
- Tissir F, Wang CE, Goffinet AM (2004): Expression of the chemokine receptor Cxcr4 mRNA during mouse brain development. Brain Res Dev Brain Res 149:63–71.
- Tran PB, Miller RJ (2003): Chemokine receptors in the brain: a developing story. J Comp Neurol 457:1–6.
- Tran PB, Ren D, Veldhouse TJ, Miller RJ (2004): Chemokine receptors are expressed widely by embryonic and adult neural progenitor cells. J Neurosci Res 76:20–34.
- van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002): Functional neurogenesis in the adult hippocampus. Nature 415:1030–1034.
- Vilz TO, Moepps B, Engele J, Molly S, Littman DR, Schilling K (2005): The SDF-1/CXCR4 pathway and the development of the cerebellar system. Eur J Neurosci 22:1831–1839.
- Weiss KH, Johanssen C, Tielsch A, Herz J, Deller T, Frotscher M, Forster E (2003): Malformation of the radial glial scaffold in the dentate gyrus of reeler mice, scrambler mice, and ApoER2/VLDLR-deficient mice. J Comp Neurol 460:56–65.
- Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR (1998): Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393:595–599.
Article / Publication Details
Copyright / Drug Dosage / DisclaimerCopyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.