Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Acta Neuropathologica
Published in: Acta Neuropathologica 3/2004

01-03-2004 | Original Paper

Regulation of semaphorin 3A expression in neurons of the rat spinal cord and cerebral cortex after transection injury

Authors: Masayuki Hashimoto, Hidetoshi Ino, Masao Koda, Masazumi Murakami, Katsunori Yoshinaga, Masashi Yamazaki, Hideshige Moriya

Published in: Acta Neuropathologica | Issue 3/2004

Login to get access

Abstract

Semaphorin 3A (Sema3A) is a secreted repulsive axon guidance protein. It appears to play important roles in axon fasciculation, branching, neuronal migration, and tissue differentiation during embryonic development. In adults, Sema3A is expressed in spinal motoneurons and in some neurons in the brain. Here, we demonstrate changes in Sema3A expression in the spinal cord after complete transection and in the brain after spinal cord hemisection at the Th8 level in laboratory rats. Semi-quantitative reverse transcriptase-PCR analysis showed that the expression of Sema3A mRNA, which was present in the normal spinal cord, rapidly decreased after transection, reaching its lowest level 1 day after injury. Thereafter, Sema3A expression levels recovered and reached four-fifths of the normal level at 28 days. Double staining by in situ hybridization and fluorescence immunohistochemistry showed that Sema3A was expressed in NeuN-positive neurons, but not in glia in the spinal cord. Sema3A expression was up-regulated in the contralateral cerebral cortex and in the ipsilateral spinal trigeminal nucleus 1–3 days after spinal cord hemisection. It is likely that the up-regulation occurred in neurons whose descending fibers were transected. These results suggest that Sema3A is regulated differently in spinal motoneurons and brain neurons following axonal injury.
Literature
1.
Chen MS, Huber AB, Haar ME van der, Frank M, Schnell L, Spillmann AA, Christ F, Schwab ME (2000) Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403:434–439CrossRefPubMed
2.
De Winter F, Oudega M, Lankhorst AJ, Hamers FP, Blits B, Ruitenberg MJ, Pasterkamp RJ, Gispen WH, Verhaagen J (2002) Injury- induced class 3 semaphorin expression in the rat spinal cord. Exp Neurol 175:61–75
3.
Fall WM (1984) Axonal endings terminating on dendrites of identified large trigeminal nucleus oralis. Brain Res 324:335–341CrossRefPubMed
4.
Fujita H, Zhang B, Sato K, Tanaka J, Sakanaka M (2001) Expressions of neuropilin-1, neuropilin-2 and demaphorin3A mRNA in the rat brain after middle cerebral artery occlusion. Brain Res 914:1–14CrossRefPubMed
5.
Gagliardini V, Fankhauser C (1999) Semaphorin III can induce death in sensory neurons. Mol Cell Neurosci 14:301–316CrossRefPubMed
6.
Giger RJ, Wolfer DP, De Wit GMJ, Verhaagen J (1996) Anatomy of rat semaphorin III/collapsin-1 mRNA expression and relationship to developing nerve tracts during neuroembryogenesis. J Comp Neurol 375:378–392CrossRefPubMed
7.
Giger RJ, Pasterkamp J, Heijnen S, Holtmaat AJGD, Verhaagen J (1998) Anatomical distribution of the chemorepellent semaphorin III/collapsin-1 in the adult rat and human brain: predominant expression in structures of the olfactory-hippocampal pathway and the motor system. J Neurosci Res 52:27–42CrossRefPubMed
8.
Hashimoto M, Koda M, Ino H, Murakami M, Yamazaki M, Hideshige M (2003) Up-regulation of osteopontin expression in rat spinal cord microglia after traumatic injury. J Neurotrauma 20:287–296CrossRefPubMed
9.
Ikeda O, Murakami M, Ino H, Yamazaki M, Nemoto T, Koda M, Nakayama C Hideshige M (2001) Acute up-regulation of brain-derived neurotrophic factor expression resulting from experimentally induced injury in the rat spinal cord. Acta Neuropathol 100:69–74
10.
Ikeda O, Murakami M, Ino H, Yamazaki M, Koda M, Nakayama C Hideshige M (2002) Effects of brain-derived neurotrophic factor (BDNF) on compression-induced spinal cord injury: BDNF attenuates down-regulation of superoxide dismutase expression and promotes up-regulation of myelin basic protein expression. J Neuropathol Exp Neurol 61:142–153
11.
Kawakami A, Kitsukawa T, Takagi S, Fujisawa H (1996) Developmentally regulated expression of a cell surface protein, neuropilin, in the mouse nervous system. J Neurobiol 29:1–17CrossRefPubMed
12.
Kolodkin AL, Matthes DJ, Goodman CS (1993) The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75:1389–1399PubMed
13.
Kolodkin AL, Levengood DV, Rowe EG, Tai Y-T, Giger RJ, Ginty DD (1997) Neuropilin is a semaphorin III receptor. Cell 90:753–762PubMed
14.
Laywell ED, Dorries U, Bartsch U, Faissner A, Schachner M, Steindler DA (1992) Enhanced expression of the developmentally regulated extracellular matrix molecule tenascin following adult brain injury. Proc Natl Acad Sci USA 89:2634–2638PubMed
15.
Leroy T, Brown JR (1971) Projection and termination of the corticospinal tract in rodents. Exp Brain Res 13:432–450PubMed
16.
Livesey FJ, Hunt SP (1997) Netrin and netrin receptor expression in the embryonic mammalian nervous system suggests roles in retinal, striatal, nigral, and cerebellar development. Mol Cell Neurosci 8:417–429CrossRefPubMed
17.
Luo Y, Raible D, Raper JA (1993) Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75:217–227PubMed
18.
McKeon RJ, Schreiber RC, Rudge JS, Silver J (1991) Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci 11:3398–3411PubMed
19.
Messersmith EK, Leonardo ED, Shatz CJ, Tessier-Lavigne M, Goodman CS, Kolodkin AL (1995) Semaphorin III can function as a selective chemorepellent to pattern sensory projections in the spinal cord. Neuron 14:949–959PubMed
20.
Miranda JD, White LA, Marcillo AE, Willson CA, Jagid J, Whittemore SR (1999) Induction of Eph B3 after spinal cord injury. Exp Neurol 156:218–222CrossRefPubMed
21.
Pasterkamp RJ, Giger RJ, Verhaagen J (1998) Regulation of semaphorin III/collapsin-1 gene expression during peripheral nerve regeneration. Exp Neurol 153:313–327CrossRefPubMed
22.
Pasterkamp RJ, Giger RJ, Ruitenberg M-J, Holtmaat AJGD, De Wit J, De Winter F, Verhaagen J (1999) Expression of the gene encoding the chemorepellent Semaphorin III is induced in the fibroblast component of neural scar tissue formed following injuries of adult but not neonatal CNS. Mol Cell Neurosci 13:143–166PubMed
23.
Pasterkamp RJ, Anderson PN, Verhaagen J (2001) Peripheral nerve injury fails to induce growth of lesioned ascending dorsal column axons into spinal cord scar tissue expressing the axon repellent semaphorin3A. Eur J Neurosci 13:457–471CrossRefPubMed
24.
Reza JN, Gavazzi I, Cohen J (1999) Neuropilin-1 is expressed on adult mammalian dorsal root ganglion neurons and mediates semaphorin3a/collapsin-1-induced growth cone collapse by small diameter sensory afferents. Mol Cell Neurosci 14:317–326CrossRefPubMed
25.
Shirvan A, Ziv I, Fleminger G, Shina R, He Z, Brudo I, Melamed E, Barzilai A (1999) Semaphorins as mediators of neuronal apotosis. J Neurochem 73:961–971
26.
Snow DM, Lemmon V, Carrino DA, Kaplan AI, Silver J (1990) Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp Neurol 109:111–130PubMed
27.
Stichel CC, Wunderlich G, Schwab ME, Muller HW (1995) Clearance of myelin constituents and axonal sprouting in the transected postcommissural fornix of the adult rat. Eur J Neurosci 7:401–411PubMed
28.
Stoll G, Griffin JW, Li CY, Trapp BD (1989) Wallerian degeneration in the peripheral nervous system: Participation of both Schwann cells and macrophages in myelin degradation. J Neurocytol 18:671–683PubMed
29.
Takahashi T, Fournier A, Nakamura F, Wang L-H, Murakami Y, Kalb RG, Fujisawa H, Strittmatter SM (1999) Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 99:59–69PubMed
30.
Tanelian DL, Barry MA, Johnston SA, Le T, Smith GM (1997) Semaphorin III can repulse and inhibit adult sensory afferents in vivo. Nat Med 3:1398–1401PubMed
31.
Zhang Y, Winterbottom JK, Schachner M, Lieberman AR, Anderson PN (1997) Tenascin-C expression and axonal sprouting following injury to the spinal dorsal columns in the adult rat. J Neurosci Res 49:433–450CrossRefPubMed
Metadata
Title
Regulation of semaphorin 3A expression in neurons of the rat spinal cord and cerebral cortex after transection injury
Authors
Masayuki Hashimoto
Hidetoshi Ino
Masao Koda
Masazumi Murakami
Katsunori Yoshinaga
Masashi Yamazaki
Hideshige Moriya
Publication date
01-03-2004
Publisher
Springer-Verlag
Published in
Acta Neuropathologica / Issue 3/2004
Print ISSN: 0001-6322
Electronic ISSN: 1432-0533
DOI
https://doi.org/10.1007/s00401-003-0805-z

Other articles of this Issue 3/2004

Acta Neuropathologica 3/2004 Go to the issue

Regular Paper

Modulation of simian immunodeficiency virus neuropathology by dopaminergic drugs

Regular Paper

Neuropathological evaluation of the diencephalon, basal ganglia and upper brainstem in alobar holoprosencephaly

Regular Paper

Glioblastoma cells release factors that disrupt blood-brain barrier features

Regular Paper

Perinecrotic glioma proliferation and metabolic profile within an intracerebral tumor xenograft

Regular Paper

Infection of human astrocytes and glioblastoma cells with Toxoplasma gondii: monocyte chemotactic protein-1 secretion and chemokine expression in vitro

Regular Paper

Phagocytosis of Escherichia coli by amoeboid microglial cells in the developing brain