Patterns of SDF-1α and SDF-1γ mRNAs, migration pathways, and phenotypes of CXCR4-expressing neurons in the developing rat telencephalon

Journal of Comparative Neurology

Volumn 502, Issue 3, 2007, Pages 382-399

  Stumm, Ralf ^a   Kolodziej, Angela ^a   Schulz, Stefan ^a   Kohtz, Jhumku D ^b,c   Höllt, Volker ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b CHILDREN'S MEMORIAL HOSPITAL   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Cajal Retzius cell; Calretinin; Cerebral cortex; Chemokine; CXCL12; Development; Dlx; Eye; GABAergic; Interneuron; Migration; Olfactory sensory neuron; Parvalbumin; Retina; Somatostatin; Splice variant; Striatum

Indexed keywords

CALRETININ; CHEMOKINE RECEPTOR CXCR4; MESSENGER RNA; SOMATOSTATIN; STROMAL CELL DERIVED FACTOR 1; STROMAL CELL DERIVED FACTOR 1ALPHA; STROMAL CELL DERIVED FACTOR 1GAMMA; UNCLASSIFIED DRUG; ALPHA CHEMOKINE; CXCR4 PROTEIN, RAT; NERVE PROTEIN;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL MIGRATION; CELL TYPE; COMPARATIVE STUDY; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; FOREBRAIN; GABAERGIC SYSTEM; NERVE CELL; NEUROANATOMY; NEUROCHEMISTRY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; RNA ANALYSIS; TELENCEPHALON; ANIMAL; CELL MOTION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; METHODOLOGY; PHYSIOLOGY; PREGNANCY; PRENATAL DEVELOPMENT; SPRAGUE DAWLEY RAT;

ANIMALS; CELL MOVEMENT; CHEMOKINES, CXC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; NERVE TISSUE PROTEINS; NEURONS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CXCR4; RNA, MESSENGER; TELENCEPHALON;

EID: 34147112805     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21336     Document Type: Article

References (53)

1. Anderson SA, Eisenstat DD, Shi L, Rubenstein JL. 1997. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474-476.
2. 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.
3. Borrell V, Marin O. 2006. Meninges control tangential migration of hemderived Cajal-Retzius cells via CXCL12/CXCR4 signaling. Nat Neurosci 9:1284-1293.
4. Chalasani SH, Baribaud F, Coughlan CM, Sunshine MJ, Lee VM, Doms RW, Littman DR, Raper JA. 2003a. The chemokine stromal cell-derived factor-1 promotes the survival of embryonic retinal ganglion cells. J Neurosci 23:4601-4612.
5. Chalasani SH, Sabelko KA, Sunshine MJ, Littman DR, Raper JA. 2003b. A chemokine, SDF-1, reduces the effectiveness of multiple axonal repellents and is required for normal axon pathfinding. J Neurosci 23: 1360-1371.
6. Cobos I, Calcagnotto ME, Vilaythong AJ, Thwin MT, Noebels JL, Baraban SC, Rubenstein JL. 2005. Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat Neurosci 8:1059-1068.
7. Daniel D, Rossel M, Seki T, Konig N. 2005. Stromal cell-derived factor-1 (SDF-1) expression in embryonic mouse cerebral cortex starts in the intermediate zone close to the pallial-subpallial boundary and extends progressively towards the cortical hem. Gene Expr Patterns 5:317-322.
8. De Carlos JA, Lopez-Mascaraque L, Valverde F. 1996. Dynamics of cell migration from the lateral ganglionic eminence in the rat. J Neurosci 16:6146-6156.
9. De La Luz Sierra M, Yang F, Narazaki M, Salvucci O, Davis D, Yarchoan R, Zhang HH, Fales H, Tosato G. 2004. Differential processing of stromal-derived factor-lalpha and stromal-derived factor-1beta explains functional diversity. Blood 103:2452-2459.
10. Dziembowska M, Tham TN, Lau P, Vitry S, Lazarini F, Dubois-Dalcq M. 2005. A role for CXCR4 signaling in survival and migration of neural and oligodendrocyte precursors. Glia 50:258-269.
11. Englund C, Fink A, Lau C, Pham D, Daza RA, Bulfone A, Kowalczyk T, Hevner RF. 2005. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci 25:247-251.
12. Fonseca M, del Rio JA, Martinez A, Gomez S, Soriano E. 1995. Development of calretinin immunoreactivity in the neocortex of the rat. J Comp Neurol 361:177-192.
13. Francis F, Koulakoff A, Boucher D, Chafey P, Schaar B, Vinet MC, Friocourt G, McDonnell N, Reiner O, Kahn A, McConnell SK, Berwald-Netter Y, Denoulet P, Chelly J. 1999. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23:247-256.
14. Gleichmann M, Gillen C, Czardybon M, Bosse F, Greiner-Petter R, Auer J, Muller HW. 2000. Cloning and characterization of SDF-1gamma, a novel SDF-1 chemokine transcript with developmentally regulated expression in the nervous system. Eur J Neurosci 12:1857-1866.
15. Hevner RF, Shi L, Justice N, Hsueh Y, Sheng M, Smiga S, Bulfone A, Goffinet AM, Campagnoni AT, Rubenstein JL. 2001. Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29:353-366.
16. Hockfield S, McKay RD. 1985. Identification of major cell classes in the developing mammalian nervous system. J Neurosci 5:3310-3328.
17. Kawaguchi Y, Kondo S. 2002. Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex. J Neurocytol 31:277-287.
18. 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.
19. Kohtz JD, Lee HY, Gaiano N, Segal J, Ng E, Larson T, Baker DP, Garber EA, Williams KP, Fishell G. 2001. N-terminal fatty-acylation of sonic hedgehog enhances the induction of rodent ventral forebrain neurons. Development 128:2351-2363.
20. Kriegstein AR, Noctor SC. 2004. Patterns of neuronal migration in the embryonic cortex. Trends Neurosci 27:392-399.
21. Lavdas AA, Grigoriou M, Pachnis V, Parnavelas JG. 1999. The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J Neurosci 19:7881-7888.
22. Lazarini F, Casanova P, Tham TN, De Clercq E, Arenzana-Seisdedos F, Baleux F, Dubois-Dalcq M. 2000. Differential signalling of the chemokine receptor CXCR4 by stromal cell-derived factor 1 and the HIV glycoprotein in rat neurons and astrocytes. Eur J Neurosci 12:117-125.
23. Lee EJ, Kim IB, Lee E, Kwon SO, Oh SJ, Chun MH. 2003. Differential expression and cellular localization of doublecortin in the developing rat retina. Eur J Neurosci 17:1542-1548.
24. Lendahl U, Zimmerman LB, McKay RD. 1990. CNS stem cells express a new class of intermediate filament protein. Cell 60:585-595.
25. Lieberam I, Agalliu D, Nagasawa T, Ericson J, Jessell TM. 2005. A Cxcl12-CXCR4 chemokine signaling pathway defines the initial trajectory of mammalian motor axons. Neuron 47:667-679.
26. 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 U S A 99:7090-7095.
27. Ma Q, Jones D, Borghesani PR, Segal RA, Nagasawa T, Kishimoto T, Bronson RT, Springer TA. 1998. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc Natl Acad Sci U S A 95:9448-9453.
28. Marchese A, Benovic JL. 2001. Agonist-promoted ubiquitination of the G protein-coupled receptor CXCR4 mediates lysosomal sorting. J Biol Chem 276:45509-45512.
29. Marin O, Rubenstein JL. 2001. A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci 2:780-790.
30. Metin C, Baudoin JP, Rakic S, Parnavelas JG. 2006. Cell and molecular mechanisms involved in the migration of cortical interneurons. Eur J Neurosci 23:894-900.
31. Nadarajah B, Parnavelas JG. 2002. Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 3:423-432.
32. Nagasawa T, Kikutani H, Kishimoto T. 1994. Molecular cloning and structure of a pre-B-cell growth-stimulating factor. Proc Natl Acad Sci U S A 91:2305-2309.
33. Nagasawa T, Hirota S, Tachibana K, Takakura N, Nishikawa S, Kitamura Y, Yoshida N, Kikutani H, Kishimoto T. 1996. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 382:635-638.
34. Nery S, Fishell G, Corbin JG. 2002. The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat Neurosci 5:1279-1287.
35. Panganiban G, Sebring A, Nagy L, Carroll S. 1995. The development of crustacean limbs and the evolution of arthropods. Science 270:1363-1366.
36. Pujol F, Kitabgi P, Boudin H. 2005. The chemokine SDF-1 differentially regulates axonal elongation and branching in hippocampal neurons. J Cell Sci 118(Pt 5):1071-1080.
37. Quinn JC, Molinek M, Martynoga BS, Zaki PA, Faedo A, Bulfone A, Hevner RF, West JD, Price DJ. 2007. Pax6 controls cerebral cortical cell number by regulating exit from the cell cycle and specifies cortical cell identity by a cell autonomous mechanism. Dev Biol 302:50-65.
38. Schaar BT, McConnell SK. 2005. Cytoskeletal coordination during neuronal migration. Proc Natl Acad Sci U S A 102:13652-13657.
39. Shirozu M, Nakano T, Inazawa J, Tashiro K, Tada H, Shinohara T, Honjo T. 1995. Structure and chromosomal localization of the human stromal cell-derived factor 1 (SDF1) gene. Genomics 28:495-500.
40. Stumm R, Culmsee C, Schafer MK, Krieglstein J, Weihe E. 2001. Adaptive plasticity in tachykinin and tachykinin receptor expression after focal cerebral ischemia is differentially linked to gabaergic and glutamatergic cerebrocortical circuits and cerebrovenular endothelium. J Neurosci 21:798-811.
41. 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.
42. 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.
43. Stumm RK, Zhou C, Schulz S, Hollt V. 2004. Neuronal types expressing mu- and delta-opioid receptor mRNA in the rat hippocampal formation. J Comp Neurol 469:107-118.
44. Tachibana K, Hirota S, Iizasa H, Yoshida H, Kawabata K, Kataoka Y, Kitamura Y, Matsushima K, Yoshida N, Nishikawa S, Kishimoto T, Nagasawa T. 1998. The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393:591-594.
45. Tanaka D, Nakaya Y, Yanagawa Y, Obata K, Murakami F. 2003. Multimodal tangential migration of neocortical GABAergic neurons independent of GPI-anchored proteins. Development 130:5803-5813.
46. Tashiro K, Tada H, Heilker R, Shirozu M, Nakano T, Honjo T. 1993. Signal sequence trap: a cloning strategy for secreted proteins and type I membrane proteins. Science 261:600-603.
47. 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.
48. 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.
49. Tran PB, Miller RJ. 2003. Chemokine receptors: signposts to brain development and disease. Nat Rev Neurosci 4:444-455.
50. Winsky L, Isaacs KR, Jacobowitz DM. 1996. Calretinin mRNA and immunoreactivity in the medullary reticular formation of the rat: colocalization with glutamate receptors. Brain Res 741:123-133.
51. Yamazaki H, Sekiguchi M, Takamatsu M, Tanabe Y, Nakanishi S. 2004. Distinct ontogenic and regional expressions of newly identified Cajal-Retzius cell-specific genes during neocorticogenesis. Proc Natl Acad Sci U S A 101:14509-14514.
52. Zhu Y, Yu T, Zhang XC, Nagasawa T, Wu JY, Rao Y. 2002. Role of the chemokine SDF-1 as the meningeal attractant for embryonic cerebellar neurons. Nat Neurosci 5:719-720.
53. 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.