Abstract
Oncostatin M (OSM) is a member of the interleukin-6 family of cytokines. Of these cytokines, OSM is closely related structually, genetically and functionally to leukemia inhibitory factor. However, OSM-specific biological activities have been reported in hematopoiesis and liver development. Recently, we have demonstrated OSM-specific activities in the nervous systems. In the adult central nervous system (CNS), OSM receptor (OSMR) β was observed in meningeal cells of pia mater, epithelial cells of the choroid plexus and olfactory astrocytelike glia surrounding the glomeruli of the olfactory bulb. In the CNS of neonatal mice, OSMRβ was also expressed in the ventral subnucleus of the hypoglossal nucleus, but disappeared at post-natal day (P) 14. In contrast with the CNS, OSMRβ was strongly expressed in small-sized non-peptidergic neurons of the dorsal root ganglia (DRG) and trigeminal ganglia (TG). Interestingly, all OSMRβ-positive neurons in these ganglia also expressed both TRPV1 (a vanilloid receptor) and P2X3 (a purinergic receptor). In OSM-deficient mice, TRPV1/P2X3/OSMRβ triple-positive neurons were significantly decreased. Consistent with such histological findings, OSM-deficient mice exhibited a reduction in responses to various stimuli, including mechanical and thermal stimuli. These findings suggest an important role for OSM in the development of a subset of nociceptive neurons.
Similar content being viewed by others
References
Au WW, Treloar HB, Greer CA (2002) Sublaminar organization of the mouse olfactory bulb nerve layer. J Comp Neurol 446, 68–80.
Averill S, McMahon SB, Clary DO, Reichardt LF, Priestley JV (1995) Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur J Neurosci 7, 1484–94.
Bennett DLH, Averill S, Clary DO, Priestley JV, McMahon SB (1996) Postnatal changes in the expression of the trkA high-affinity NGF receptor in primary sensory neurons. Eur J Neurosci 8, 2204–8.
Bennett DLH, Michael GJ, Ramachandran N et al. (1998) A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J Neurosci 18, 3059–72.
Brown TJ, Lioubin MN, Marquardt H (1987) Purification and characterization of cytostatic cytokines produced by activated human T lymphocytes. J Immunol 139, 2977–83.
Bruce AG, Linsley PS, Rose TM (1992) Oncostatin M. Prog Growth Factor Res 4, 157–70.
Elson GCA, Lelievre E, Guillet C et al. (2000) CLF associates with CLC to form a functional heteromeric ligand for the CNTF receptor complex. Nat Neurosci 3, 867–72.
Franceschini IA, Barnett SC (1996) Low-affinity NGF-receptor and E-N-CAM expression define two types of olfactory nerve ensheathing cells that share a common lineage. Dev Biol 173, 327–43.
Gardiner NJ, Cafferty WBJ, Slack SE, Thompson SWN (2002) Expression of gp130 and leukaemia inhibitory factor receptor subunits in adult rat sensory neurons: Regulation by nerve injury. J Neurochem 83, 100–9.
Gearing DP, Comeau MR, Friend DJ et al. (1992) The IL-6 signal transducer, gp130: An oncostatin M receptor and affinity converter for the LIF receptor. Science 255, 1434–7.
Gong Q, Bailey MS, Pixley SK, Ennis M, Liu W, Shipley MT (1994) Localization and regulation of low affinity nerve growth factor receptor expression in the rat olfactory system during developmental and regeneration. J Comp Neurol 344, 336–48.
Grenier A, Dehoux M, Boutten A et al. (1999) Oncostatin M production and regulation by human polymorphonuclear neutrophils. Blood 93, 1413–21.
Guo A, Vulchanova L, Wang J, Li X, Elde R (1999) Immunocytochemical localization of the vanilloid receptor 1 (VR1): Relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur J Neurosci 11, 946–58.
Heinrich PC, Behrmann I, Muller-Newen G, Schaper F, Graeve L (1998) Interleukin-6-type cytokine signaling through the gp130/Jak/STAT pathway. Biochem J 334, 297–314.
Hoffman RC, Moy FJ, Price V et al. (1996) Resonance assignments for oncostatin M, a 24-kDa alpha helical protein. J Biomol NMR 7, 273–82.
Ichihara M, Hara T, Kim H, Murate T, Miyajima A (1997) Oncostatin M and leukemia inhibitory factor do not use the same functional receptor in mice. Blood 90, 165–73.
Jeffery E, Price V, Gearing DP (1993) Close proximity of the genes for leukemia inhibitory factor and oncostatin M. Cytokine 5, 107–11.
Kamiya A, Kinoshita T, Ito Y et al. (1999) Fetal liver development requires a paracrine action of oncostatin M through the gp130 signal transducer. EMBO J 18, 2127–36.
Kilo S, Harding-Rose C, Hargreaves KM, Flores CM (1997) Peripheral CGRP release as a marker for neurogenic inflammation: A model system for the study of neuropeptide secretion in rat paw skin. Pain 73, 201–7.
Kishimoto T, Akira S, Narazaki M, Taga T (1995) Interleukin-6 family of cytokines and gp130. Blood 86, 1243–54.
Li M, Sendtner M, Smith A (1995) Essential function of LIF receptor in motor neurons. Nature 378, 724–7.
Lindberg RA, Juan TS-C-C, Welcher AA et al. (1998) Cloning and characterization of a specific receptor for mouse oncostation M. Mol Cell Biol 18, 3357–67.
Linsley PS, Kallestad JC, Ochs V, Neubauer M (1990) Cleavage of a hydrophilic C-terminal domain increase growth-inhibitory activity of oncostatin M. Mol Cell Biol 10, 1882–90.
Malik N, Kallestad JC, Gunderson NL et al. (1989) Molecular cloning, sequence analysis, and functional expression of a novel growth regulator, oncostatin M. Mol Cell Biol 9, 2847–53.
Malmberg AB, Yaksh TL (1992) Hyperalgesia mediated by spinal glutamate or substance P receptor blocked by spinal cyclooxygenase inhibition. Science 257, 1276–9.
Matsui T, Kinoshita T, Morikawa Y et al. (2002) K-ras mediates cytokine-induced formation of E-cadherin-based adherens junctions during liver development. EMBO J 21, 1021–30.
Mikaels A, Livet J, Westphal H, de Lapeyriere O, Ernfors P (2000) A dynamic regulation of GDNF-family receptors correlates with a specific trophic dependency of cranial motor neuron subpopulations during development. Eur J Neurosci 12, 446–56.
Miyajima A, Kinoshita T, Tanaka M, Kamiya A, Mukouyama Y, Hara T (2000) Role of oncostatin M in hematopoiesis and liver development. Cytokine Growth Factor Rev 11, 177–83.
Molliver DC, Wright DE, Leitner ML et al. (1997) IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 19, 849–61.
Morikawa Y, Tamura S, Minehata K, Donovan PJ, Miyajima A, Senba E (2004) Essential function of oncostatin M in nociceptive neurons of dorsal root ganglia. J Neurosci 24, 1941–7.
Mosley B, de Imus C, Friend D et al. (1996) Dual oncostatin M (OSM) receptors: Cloning and characterization of an alternative signaling subunit conferring. J Biol Chem 271, 32635–43.
Mukouyama Y, Hara T, Xu M et al. (1998) In vitro expansion of murine multipotential hematopoietic progenitors from the embryonic aorta-gonad-mesonephros region. Immunity 8, 105–14.
Nagy I, Miller BA, Woolf CJ (1994) NK1 and NK2 receptors contribute to C-fibre evoked slow potentials in the spinal cord. Neuroreport 5, 2105–8.
Nicola NA, Cross B, Simpson RJ (1993) The disulfide bond arrangement of leukemia inhibitory factor: Homology to oncostatin M and structural implications. Biochem Biophys Res Commun 190, 20–6.
Repovic P, Benveniste EN (2002) Prostaglandin E2 is a novel inducer of oncostatin M expression in macrophages and microglia. J Neurosci 22, 5334–43.
Rose TM, Bruce AG (1991) Oncostatin M is a member of a cytokine family that includes leukemia-inhibitory factor, granulocyte colony-stimulating factor, and interleukin 6. Proc Natl Acad Sci USA 88, 8641–5.
Senaldi G, Varnum BC, Sarmiento U et al. (1999) Novel neurotrophin-1/B cell-stimulating factor-3: A cytokine of the IL-6 family. Proc Natl Acad Sci USA 96, 11458–63.
Snider WD, McMahon SB (1998) Tackling pain at the source: New ideas about nociceptors. Neuron 20, 629–32.
Stancano L, Sakatsume M, David M et al. (1997) Beta interferon and oncostatin M activate Raf-1 and mitogen-activated protein kinase through a JAK1-dependent pathway. Mol Cell Biol 17, 3833–40.
Taga T, Kishimoto T (1997) Gp130 and the interleukin-6 family of cytokines. Annu Rev Immunol 15, 797–813.
Tamura S, Morikawa Y, Miyajima A, Senba E (2002a) Oncostatin M gene expression in hematopoietic organs. Dev Dyn 225, 327–31.
Tamura S, Morikawa Y, Tanaka M, Miyajima A, Senba E (2002b) Developmental expression pattern of oncostatin M receptor in mice. Mech Dev 115, 127–31.
Tamura S, Morikawa Y, Miyajima A, Senba E (2003a) Oncostatin M receptor β is expressed predominantly in nociceptive sensory neurons. Eur J Neurosci 17, 2287–98.
Tamura S, Morikawa Y, Senba E (2003b) Localization of oncostatin M receptor β in adult and developing central nervous system. Neuroscience 119, 991–7.
Tanaka M, Hara T, Copeland NG, Gilbert DJ, Jenkins NA, Miyajima A (1999) Reconstitution of the functional mouse oncostatin M (OSM) receptor: Molecular cloning of the mouse OSM receptor β subunit. Blood 93, 804–15.
Thoma B, Bird TA, Friend DJ, Gearing DP, Dower SK (1994) Oncostatin M and leukemia inhibitory factor trigger overlapping and different signals through partially shared receptor complexes. J Biol Chem 269, 6215–22.
Traub RJ (1996) The spinal contribution of substance P to the generation and maintenance of inflammatory hyperalgesia in the rat. Pain 67, 151–61.
Vulchanova L, Riedl MS, Shuster SJ et al. (1998) P2X3 is expressed by DRG neurons that terminate in inner lamina II. Eur J Neurosci 10, 3470–8.
Yoshimura A, Ichihara M, Kinjo I et al. (1996) Mouse oncostatin M: An immediate early gene induced by multiple cytokines through the JAK-STAT5 pathway. EMBO J 15, 1055–63.
Yu T, Scully S, Yu Y, Fox GM, Jing S, Zhou R (1998) Expression of GDNF family receptor components during development: Implications in mechanisms of interaction. J Neurosci 18, 4684–96.
Zarling JM, Shoyab M, Marquardt H, Hanson MB, Lioubin MN, Todaro GJ (1986) Oncostatin M: A growth regulator produced by differentiated histiocytic lymphoma cells. Proc Natl Acad Sci USA 83, 9739–43.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Morikawa, Y. Oncostatin M in the development of the nervous system. Anato Sci Int 80, 53–59 (2005). https://doi.org/10.1111/j.1447-073x.2005.00100.x
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1111/j.1447-073x.2005.00100.x