Neuroprotective effect of insulin-like growth factor-1: Effects on tyrosine kinase receptor (Trk) expression in dorsal root ganglion neurons with glutamate-induced excitotoxicity in vitro

Brain Research Bulletin

Volumn 97, Issue , 2013, Pages 86-95

  Li, Hao ^a,b   Dong, Haixia ^a,c   Li, Jianmin ^b   Liu, Huaxiang ^b   Liu, Zhen ^a   Li, Zhenzhong ^a  

^a SHANDONG UNIVERSITY   (China)

^b SHANDONG UNIVERSITY   (China)

^c WEIFANG MEDICAL UNIVERSITY   (China)

Author keywords

Dorsal root ganglion; Glutamate; Insulin like growth factor 1; Neurotoxicity; Tyrosine kinase receptor

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; GLUTAMIC ACID; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEUROTROPHIN 3 RECEPTOR; PROTEIN TYROSINE KINASE A; SOMATOMEDIN C;

ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; EMBRYO; EXCITOTOXICITY; GENE EXPRESSION; IN VITRO STUDY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD NERVE CELL; SPINAL GANGLION; WESTERN BLOTTING;

DORSAL ROOT GANGLION; GLUTAMATE; INSULIN-LIKE GROWTH FACTOR-1; NEUROTOXICITY; TYROSINE KINASE RECEPTOR;

ANIMALS; CELLS, CULTURED; GANGLIA, SPINAL; GLUTAMIC ACID; INSULIN-LIKE GROWTH FACTOR I; NEURONS; NEUROPROTECTIVE AGENTS; RATS; RATS, WISTAR; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, TRKA; RECEPTOR, TRKB; RECEPTOR, TRKC;

EID: 84880317325     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2013.05.014     Document Type: Article

References (60)

1. Aberg D. Role of the growth hormone/insulin-like growth factor 1 axis in neurogenesis. Endocrine Development 2010, 17:63-76.
2. Aburto M.R., Magariños M., Leon Y., Varela-Nieto I., Sanchez-Calderon H. AKT signaling mediates IGF-I survival actions on otic neural progenitors. PLoS ONE 2012, 7:e30790.
3. Akundi R.S., Zhi L., Büeler H. PINK1 enhances insulin-like growth factor-1-dependent Akt signaling and protection against apoptosis. Neurobiology of Disease 2012, 45:469-478.
4. Arboleda G., Cárdenas Y., Rodríguez Y., Morales L.C., Matheus L., Arboleda H. Differential regulation of AKT, MAPK and GSK3β during C2-ceramide-induced neuronal death. Neurotoxicology 2010, 31:687-693.
5. Areshkov P.O., Avdieiev S.S., Balynska O.V., Leroith D., Kavsan V.M. Two closely related human members of chitinase-like family, CHI3L1 and CHI3L2, activate ERK1/2 in 293 and U373 cells but have the different influence on cell proliferation. International Journal of Biological Science 2012, 8:39-48.
6. Bergman E., Fundin B.T., Ulfhake B. Effects of aging and axotomy on the expression of neurotrophin receptors in primary sensory neurons. Journal of Comparative Neurology 1999, 410:368-386.
7. 2-positive perineuronal baskets. Experimental Neurology 2011, 230:258-272.
8. Carrer H.F., Cambiasso M.J. Sexual differentiation of the brain: genes, estrogen, and neurotrophic factors. Cellular and Molecular Neurobiology 2002, 22:479-500.
9. Carroll P.V. Treatment with growth hormone and insulin-like growth factor-I in critical illness. Best Practice & Research. Clinical Endocrinology & Metabolism 2001, 15:435-451.
10. Chen M.J., Russo-Neustadt A.A. Running exercise- and antidepressant-induced increases in growth and survival-associated signaling molecules are IGF-dependent. Growth Factors 2007, 25:118-131.
11. Chirivella L., Cano-Jaimez M., Pérez-Sánchez F., Herraez L., Carretero J., Fariñas I., Burks D.J., Kirstein M. IRS2 signalling is required for the development of a subset of sensory spinal neurons. European Journal of Neuroscience 2012, 35:341-352.
12. Chung Y.H., Joo K.M., Nam R.H., Lee W.B., Lee K.H., Cha C.I. Region-specific alterations in insulin-like growth factor-I receptor in the central nervous system of nNOS knockout mice. Brain Research 2004, 1021:132-139.
13. Craner M.J., Klein J.P., Black J.A., Waxman S.G. Preferential expression of IGF-I in small DRG neurons and down-regulation following injury. Neuroreport 2002, 13:1649-1652.
14. Croci L., Barili V., Chia D., Massimino L., van Vugt R., Masserdotti G., Longhi R., Rotwein P., Consalez G.G. Local insulin-like growth factor I expression is essential for Purkinje neuron survival at birth. Cell Death and Differentiation 2011, 18:48-59.
15. Del Río P., Montiel T., Massieu L. Contribution of NMDA and non-NMDA receptors to in vivo glutamate-induced calpain activation in the rat striatum. Relation to neuronal damage. Neurochemical Research 2008, 33:1475-1483.
16. Digicaylioglu M., Garden G., Timberlake S., Fletcher L., Lipton S.A. Acute neuroprotective synergy of erythropoietin and insulin-like growth factor I. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:9855-9860.
17. Emel E., Ergün S.S., Kotan D., Gürsoy E.B., Parman Y., Zengin A., Nurten A. Effects of insulin-like growth factor-I and platelet-rich plasma on sciatic nerve crush injury in a rat model. Journal of Neurosurgery 2011, 114:522-528.
18. Ernsberger U. Role of neurotrophin signalling in the differentiation of neurons from dorsal root ganglia and sympathetic ganglia. Cell Tissue Research 2009, 336:349-384.
19. Garcia-Galloway E., Arango C., Pons S., Torres-Aleman I. Glutamate excitotoxicity attenuates insulin-like growth factor-I prosurvival signaling. Molecular and Cellular Neurosciences 2003, 24:1027-1037.
20. Genc B., Ulupinar E., Erzurumlu R.S. Differential Trk expression in explant and dissociated trigeminal ganglion cell cultures. Journal of Neurobiology 2005, 64:145-156.
21. Harada N., Zhao J., Kurihara H., Nakagata N., Okajima K. Stimulation of Fc gammaRI on primary sensory neurons increases insulin-like growth factor-I production, thereby reducing reperfusion-induced renal injury in mice. Journal of Immunology 2010, 185:1303-1310.
22. Hennigan A., O'Callaghan R.M., Kelly A.M. Neurotrophins and their receptors: roles in plasticity, neurodegeneration and neuroprotection. Biochemical Society Transactions 2007, 35:424-427.
23. Jang S.W., Okada M., Sayeed I., Xiao G., Stein D., Jin P., Ye K. Gambogic amide, a selective agonist for TrkA receptor that possesses robust neurotrophic activity, prevents neuronal cell death. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:16329-16334.
24. Johnson-Farley N.N., Patel K., Kim D., Cowen D.S. Interaction of FGF-2 with IGF-1 and BDNF in stimulating Akt, ERK, and neuronal survival in hippocampal cultures. Brain Research 2007, 1154:40-49.
25. Kimpinski K., Mearow K. Neurite growth promotion by nerve growth factor and insulin-like growth factor-1 in cultured adult sensory neurons: role of phosphoinositide 3-kinase and mitogen activated protein kinase. Journal of Neuroscience Research 2001, 486-499.
26. Kitiyanant N., Kitiyanant Y., Svendsen C.N., Thangnipon W. BDNF-, IGF-1- and GDNF-secreting human neural progenitor cells rescue amyloid β-induced toxicity in cultured rat septal neurons. Neurochemical Research 2012, 37:143-152.
27. Lawton M., Tong M., Gundogan F., Wands J.R., de la Monte S.M. Aspartyl-(asparaginyl) beta-hydroxylase, hypoxia-inducible factor-alpha and notch cross-talk in regulating neuronal motility. Oxidative Medicine and Cell Longevity 2010, 3:347-356.
28. Li H., Zhang P., Fu G., Li J., Liu H., Li Z. Alterations in tyrosine kinase receptor (Trk) expression induced by insulin-like growth factor-1 in cultured dorsal root ganglion neurons. Brain Research Bulletin 2013, 90:25-34.
29. Liu Z., Liu H., Yang X., Xu X., Zhang W., Li Z. Effects of insulin-like growth factor-1 on expression of sensory neuropeptides in cultured dorsal root ganglion neurons in the absence or presence of glutamate. International Journal of Neuroscience 2010, 120:698-702.
30. Lunetta C., Serafini M., Prelle A., Magni P., Dozio E., Ruscica M., Sassone J., Colciago C., Moggio M., Corbo M., Silani V. Impaired expression of insulin-like growth factor-1 system in skeletal muscle of amyotrophic lateral sclerosis patients. Muscle Nerve 2012, 45:200-208.
31. Lykissas M.G., Batistatou A.K., Charalabopoulos K.A., Beris A.E. The role of neurotrophins in axonal growth, guidance, and regeneration. Current Neurovascular Research 2007, 4:143-151.
32. Marshall J., Dolan B.M., Garcia E.P., Sathe S., Tang X., Mao Z., Blair L.A. Calcium channel and NMDA receptor activities differentially regulate nuclear C/EBPbeta levels to control neuronal survival. Neuron 2003, 39:625-639.
33. McCusker R.H., McCrea K., Zunich S., Dantzer R., Broussard S.R., Johnson R.W., Kelley K.W. Insulin-like growth factor-I enhances the biological activity of brain-derived neurotrophic factor on cerebrocortical neurons. Journal of Neuroimmunology 2006, 179:186-190.
34. Merighi A., Bardoni R., Salio C., Lossi L., Ferrini F., Prandini M., Zonta M., Gustincich S., Carmignoto G. Presynaptic functional trkB receptors mediate the release of excitatory neurotransmitters from primary afferent terminals in lamina II (substantia gelatinosa) of postnatal rat spinal cord. Developmental Neurobiology 2008, 68:457-475.
35. Miltiadous P., Stamatakis A., Stylianopoulou F. Neuroprotective effects of IGF-I following kainic acid-induced hippocampal degeneration in the rat. Cellular and Molecular Neurobiology 2010, 30:347-360.
36. Miura M., Sasaki M., Mizukoshi K., Shibasaki M., Izumi Y., Shimosato G., Amaya F. Peripheral sensitization caused by insulin-like growth factor 1 contributes to pain hypersensitivity after tissue injury. Pain 2011, 152:888-895.
37. Morcuende S., Matarredona E.R., Benítez-Temiño B., Muñoz-Hernández R., Pastor A.M., de la Cruz R.R. Differential regulation of the expression of neurotrophin receptors in rat extraocular motoneurons after lesion. Journal of Comparative Neurology 2011, 519:2335-2352.
38. Ness J.K., Mitchell N.E., Wood T.L. IGF-I and NT-3 signaling pathways in developing oligodendrocytes: differential regulation and activation of receptors and the downstream effector Akt. Developmental Neuroscience 2002, 24:437-445.
39. Ness J.K., Wood T.L. Insulin-like growth factor I, but not neurotrophin-3, sustains Akt activation and provides long-term protection of immature oligodendrocytes from glutamate-mediated apoptosis. Molecular and Cellular Neuroscience 2002, 20:476-488.
40. Okajima K., Harada N. Promotion of insulin-like growth factor-I production by sensory neuron stimulation; molecular mechanism(s) and therapeutic implications. Current Medicinal Chemistry 2008, 15:3095-3112.
41. Pierson C.R., Zhang W., Murakawa Y., Sima A.A. Insulin deficiency rather than hyperglycemia accounts for impaired neurotrophic responses and nerve fiber regeneration in type 1 diabetic neuropathy. Journal of Neuropathology and Experimental Neurology 2003, 62:260-271.
42. Pitts E.V., Potluri S., Hess D.M., Balice-Gordon R.J. Neurotrophin and Trk-mediated signaling in the neuromuscular system. International Anesthesiology Clinics 2006, 44:21-76.
43. Romanelli R.J., LeBeau A.P., Fulmer C.G., Lazzarino D.A., Hochberg A., Wood T.L. Insulin-like growth factor type-I receptor internalization and recycling mediate the sustained phosphorylation of Akt. Journal of Biological Chemistry 2007, 282:22513-22524.
44. Sanelli T., Ge W., Leystra-Lantz C., Strong M.J. Calcium mediated excitotoxicity in neurofilament aggregate-bearing neurons in vitro is NMDA receptor dependant. Journal of Neurological Science 2007, 256:39-51.
45. Scolnick J.A., Cui K., Duggan C.D., Xuan S., Yuan X.B., Efstratiadis A., Ngai J. Role of IGF signaling in olfactory sensory map formation and axon guidance. Neuron 2008, 57:847-857.
46. Simon M., Mann D., Coulton G., Terenghi G. Differential tyrosine kinase C mRNA distribution in extensor digitorum longus and soleus motoneurons in adult rats: effect of axotomy and neurotrophin-3 treatment. Neuroscience Letters 2002, 320:9-12.
47. Sivakumar V., Ling E.A., Lu J., Kaur C. Role of glutamate and its receptors and insulin-like growth factors in hypoxia induced periventricular white matter injury. Glia 2010, 58:507-523.
48. Stephens H.E., Belliveau A.C., Gupta J.S., Mirkovic S., Kablar B. The role of neurotrophins in the maintenance of the spinal cord motor neurons and the dorsal root ganglia proprioceptive sensory neurons. International Journal of Developmental Neuroscience 2005, 23:613-620.
49. Sullivan K.A., Kim B., Feldman E.L. Insulin-like growth factors in the peripheral nervous system. Endocrinology 2008, 149:5963-5971.
50. Sun C., Wang D., Zheng W. Hydrogen peroxide attenuates the prosurvival signaling of insulin-like growth factor-1 through two pathways. Neuroreport 2012, 23:768-773.
51. Svensson J., Diez M., Engel J., Wass C., Tivesten A., Jansson J.O., Isaksson O., Archer T., Hökfelt T., Ohlsson C. Endocrine, liver-derived IGF-I is of importance for spatial learning and memory in old mice. Journal of Endocrinology 2006, 189:617-627.
52. Takayama B., Sekiguchi M., Yabuki S., Kikuchi S., Konno S. Localization and function of insulin-like growth factor 1 in dorsal root ganglia in a rat disc herniation model. Spine 2011, 36:E75-E79.
53. Tran P.V., Fretham S.J., Wobken J., Miller B.S., Georgieff M.K. Gestational-neonatal iron deficiency suppresses and iron treatment reactivates IGF signaling in developing rat hippocampus. American Journal of Physiology. Endocrinology and Metabolism 2012, 302:E316-E324.
54. Vincent A.M., Mobley B.C., Hiller A., Feldman E.L. IGF-I prevents glutamate-induced motor neuron programmed cell death. Neurobiology of Diseases 2004, 16:407-416.
55. Vizi E.S., Kisfali M., Lorincz T. Role of nonsynaptic GluN2B-containing NMDA receptors in excitotoxicity: evidence that fluoxetine selectively inhibits these receptors and may have neuroprotective effects. Brain Research Bulletin 2013, 93:32-38.
56. Wood T.L., Loladze V., Altieri S., Gangoli N., Levison S.W., Brywe K.G., Mallard C., Hagberg H. Delayed IGF-1 administration rescues oligodendrocyte progenitors from glutamate-induced cell death and hypoxic-ischemic brain damage. Developmental Neuroscience 2007, 29:302-310.
57. Yano H., Chao M.V. Biochemical characterization of intracellular membranes bearing Trk neurotrophin receptors. Neurochemical Research 2005, 30:767-777.
58. Zhang H., Gao Y., Dai Z., Meng T., Tu S., Yan Y. IGF-1 reduces BACE-1 expression in PC12 cells via activation of PI3-K/Akt and MAPK/ERK1/2 signaling pathways. Neurochemical Research 2011, 36:49-57.
59. Zheng W.H., Quirion R. Insulin-like growth factor-1 (IGF-1) induces the activation/phosphorylation of Akt kinase and cAMP response element-binding protein (CREB) by activating different signaling pathways in PC12 cells. BMC Neuroscience 2006, 7:51.
60. Zhong J., Deng J., Huang S., Yang X., Lee W.H. High K+ and IGF-1 protect cerebellar granule neurons via distinct signaling pathways. Journal of Neuroscience Research 2004, 75:794-806.