Insulin-like growth factor-1 abrogates microglial oxidative stress and TNF-α responses to spreading depression

Journal of Neurochemistry

Volumn 126, Issue 5, 2013, Pages 662-672

  Grinberg, Yelena Y ^a   Dibbern, Megan E ^a   Levasseur, Victoria A ^a   Kraig, Richard P ^a  

^a UNIVERSITY OF CHICAGO MEDICAL CENTER   (United States)

Author keywords

IGF 1; microglia; migraine; oxidative stress; reactive oxygen species; spreading depression

Indexed keywords

REACTIVE OXYGEN METABOLITE; SOMATOMEDIN C; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN FUNCTION; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; ENZYME ACTIVITY; FEMALE; HIPPOCAMPUS; MICROGLIA; MIGRAINE; MOLECULAR PROBE; NERVE CELL; NONHUMAN; OLIGODENDROGLIA; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; RAT; SIGNAL TRANSDUCTION; SPREADING CORTICAL DEPRESSION;

IGF-1; MICROGLIA; MIGRAINE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SPREADING DEPRESSION;

ANIMALS; CORTICAL SPREADING DEPRESSION; ELECTROPHYSIOLOGICAL PHENOMENA; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; INSULIN-LIKE GROWTH FACTOR I; MICROGLIA; MICROSCOPY, CONFOCAL; NEURONS; OLIGODENDROGLIA; ORGAN CULTURE TECHNIQUES; OXIDATIVE STRESS; PREGNANCY; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; TISSUE FIXATION; TUMOR NECROSIS FACTOR-ALPHA;

RATTUS;

EID: 84883188942     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12267     Document Type: Article

References (66)

1. Beattie E. C., Stellwagen D., Morishita W., Bresnahan J. C., Ha B. K., Von Zastrow M., Beattie M. S., and, Malenka R. C., (2002) Control of synaptic strength by glial TNFalpha. Science 295, 2282-2285.
2. Bélanger M., Allaman I., and, Magistretti P. J., (2011) Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab. 14, 724-738.
3. Brewer G. J., Torricelli J. R., Evege E. K., and, Price P. J., (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J. Neurosci. Res. 35, 567-576.
4. Buffo A., Rolando C., and, Ceruti S., (2010) Astrocytes in the damaged brain: molecular and cellular insights into their reactive response and healing potential. Biochem. Pharmacol. 79, 77-89.
5. Bureš J., Burešová O., and, Křivánek J., (1974) The mechanism and applications of Leão's spreading depression of electroencelphalographic activity. Academia, Prague.
6. Caggiano A. O., and, Kraig R. P., (1996) Eicosanoids and nitric oxide influence induction of reactive gliosis from spreading depression in microglia but not astrocytes. J. Comp. Neurol. 369, 93-108.
7. Caggiano A. O., and, Kraig R. P., (1998) Neuronal nitric oxide synthase expression is induced in neocortical astrocytes after spreading depression. J. Cereb. Blood Flow Metab. 18, 75-87.
8. Cardoso A. R., Chausse B., da Cunha F. M., Luévano-Martínez L. A., Marazzi T. B., Pessoa P. S., Queliconi B. B., and, Kowaltowski A. J., (2012) Mitochondrial compartmentalization of redox processes. Free Radic. Biol. Med. 52, 2201-2208.
9. Cipolla M. J., Pusic A. D., Grinberg Y. Y., Chapman A. C., Poynter M. E., and, Kraig R. P., (2012) Pregnant serum induces neuroinflammation and seizure activity via TNFα. Exp. Neurol. 234, 398-404.
10. Dewar D., Underhill S. M., and, Goldberg M. P., (2003) Oligodendrocytes and ischemic brain injury. J. Cereb. Blood Flow Metab. 23, 263-274.
11. Dibbern M. E., (2012) Spreading depression preferentially increases oxidative stress in microglia and astrocytes: implications for the chronification of migraine. Cornell College Thesis. www.cornellcollege.edu/ dimensions/research/Images/dibbern-the sis.pdf.
12. Dienel G. A., and, Hertz L., (2001) Glucose and lactate metabolism during brain activation. J. Neurosci. Res. 66, 824-838.
13. Dringen R., (2000) Metabolism and functions of glutathione in brain. Prog. Neurobiol. 62, 649-671.
14. Dringen R., (2005) Oxidative and antioxidative potential of brain microglial cells. Antioxid. Redox Signal. 7, 1223-1233.
15. Frank J., Pompella A., and, Biesalski H. K., (2002) Immunohistochemical detection of protein oxidation. Methods Mol. Biol. 196, 35-40.
16. Gehrmann J., Mies G., Bonnekoh P., Banati R., Iijima T., Kreutzberg G. W., and, Hossman K. A., (1993) Microglial reaction in the rat cerebral cortex induced by cortical spreading depression. Brain Pathol. 3, 11-17.
17. Grinberg Y. Y., Milton J. G., and, Kraig R. P., (2011) Spreading depression sends microglia on Lévy flights. PLoS ONE 6, e19294.
18. Grinberg Y. Y., van Drongelen W., and, Kraig R. P., (2012a) Insulin-like growth factor-1 lowers spreading depression susceptibility and reduces oxidative stress. J. Neurochem. 122, 221-229.
19. Grinberg Y. Y., Dibbern M. E., and, Kraig R. P,. (2012b) Oxidative stress from spreading depression preferentially rises in astrocytes and microglia, with the latter effect mitigated by IGF-1. Soc. Neurosci. 38, #62.11.
20. Han D., Ybanez M. D., Ahmadi S., Yeh K., and, Kaplowitz N., (2009) Redox regulation of tumor necrosis factor signaling. Antioxid. Redox Signal. 11, 2245-2263.
21. Hulse R. E., Swenson W. G., Kunkler P. E., White D. M., and, Kraig R. P., (2008) Monomeric IgG is neuroprotective via enhancing microglial recycling endocytosis and TNF-alpha. J. Neurosci. 28, 12199-12211.
22. Jander S., Schroeter M., Peters O., Witte O. W., and, Stoll G., (2001) Cortical spreading depression induces proinflammatory cytokine gene expression in the rat brain. J. Cereb. Blood Flow Metab. 21, 218-225.
23. Kishida K. T., and, Klann E., (2007) Sources and targets of reactive oxygen species in synaptic plasticity and memory. Antioxid. Redox Signal. 9, 233-244.
24. Kraig R. P., Dong L., Thisted R., and, Jaeger C. B., (1991) Spreading depression increases immunohistochemical staining of glial fibrillary acidic protein. J. Neurosci. 11, 2187-2198.
25. Kraig R. P., Mitchell H. M., Christie-Pope B., Kunkler P. E., White D. M., Tang Y. P., and, Langan G., (2010) TNF-α and microglial hormetic involvement in neurological health & migraine. Dose Response 8, 389-413.
26. Kruger H., Luhmann H. J., and, Heinemann U., (1996) Repetitive spreading depression causes selective suppression of GABAergic function. NeuroReport 7, 2733-2736.
27. Kunkler P. E., and, Kraig R. P., (1997) Reactive astrocytosis from excitotoxic injury in hippocampal organ culture parallels that seen in vivo. J. Cereb. Blood Flow Metab. 17, 26-43.
28. Kunkler P. E., Hulse R. E., and, Kraig R. P., (2004) Multiplexed cytokine protein expression profiles from spreading depression in hippocampal organotypic cultures. J. Cereb. Blood Flow Metab. 24, 829-839.
29. Lauritzen M., and, Kraig R. P,. (2005) Spreading depression and migraine, in The Headaches (, Olesen J., Goadsby P., Ramadan N., Tfelt-Hansen A., and, Welch K. M. A,., eds) 3rd edn, pp. 269-267. Lippincott-Raven, Philadelphia.
30. Leão A., (1944) Spreading depression of activity in the cerebral cortex. J. Neurophysiol. 7, 379-390.
31. Li J., Baud O., Vartanian T., Volpe J. J., and, Rosenberg P. A., (2005) Peroxynitrite generated by inducible nitric oxide synthase and NADPH oxidase mediates microglial toxicity to oligodendrocytes. Proc. Natl Acad. Sci. USA 102, 9936-9941.
32. Liu X. F., Fawcett J. R., Thorne R. G., DeFor T. A., and, Frey W. H., (2001) Intranasal administration of insulin-like growth factor-I bypasses the blood-brain barrier and protects against focal cerebral ischemic damage. J. Neurol. Sci. 187, 91-97.
33. Lovatt D., Sonnewald U., Waagepetersen H. S., et al,. (2007) The transcriptome and metabolic gene signature of protoplasmic astrocytes in the adult murine cortex. J. Neurosci. 27, 12255-12266.
34. Mack K. J., (2011) Can we help patients with chronic migraine? Neurology 76, 682-683.
35. Mendez P., Wandosell F., and, Garcia-Segura L. M., (2006) Cross-talk between estrogen receptors and insulin-like growth factor-1 receptor in the brain: cellular and molecular mechanisms. Front. Neuroendocrinol. 27, 391-403.
36. Mitchell H. M., White D. M., and, Kraig R. P,. (2010a). Strategies for study of neuroprotection from cold-preconditioning. J. Vis. Exp. 43, doi: 10.3791/2192.
37. Mitchell H. M., Levasseur V., and, Kraig R. P,. (2010b). TNF-α increases spreading depression susceptibility via reduced GABAergic inhibition-implications for the transformation of episodic to chronic migraine. Soc. Neurosci. 36, #346.3.
38. Mitchell H. M., White D. M., Domowicz M. S., and, Kraig R. P., (2011) Cold pre-conditioning neuroprotection depends on TNF-α and is enhanced by blockade of interleukin-11. J. Neurochem. 177, 187-196.
39. Moskowitz M. A., Nozaki K., and, Kraig R. P., (1993) Neocortical spreading depression provokies the expression of c-fos protein-like immunoreactivity within trigeminal nucleus caudalis via trigeminovascular mechanisms. J. Neurosci. 13, 1167-1177.
40. Murphy M. P., (2009) How mitochondria produce reactive oxygen species. Biochem. J. 417, 1-13.
41. Pellmar T. C., (1987) Peroxide alters neuronal excitability in the CA1 region of the guinea-pig hippocampus in vitro. Neuroscience 23, 447-456.
42. Pietrobon D., and, Moskowitz M. A., (2012) Pathophysiology of migraine. Annu. Rev. Physiol. 75, 365-391.
43. Pusic A. D., and, Kraig R. P,. (2011) IFN-γ from T-cells modulates susceptibility to-and transient demyelination from-spreading depression: implications for migraine therapy. Soc. Neurosci. 37, # 875.16.
44. Pusic A. D., Grinberg Y. Y., Mitchell H. M., and, Kraig R. P,. (2011) Modeling neural immune signaling of episodic and chronic migraine using spreading depression in vitro. J. Vis. Exp. 52, doi: 10.3791/2910.
45. Rasmussen B. K., Jensen R., Schroll M., and, Olesen J., (1991) Epidemiology of headache in a general population -a prevalence study. J. Clin. Epidemiol. 44, 1147-1157.
46. Scheepens A., Williams C. E., Breier B. H., Guan J., and, Gluckman P. D., (2000) A role for the somatotropic axis in neural development, injury and disease. J. Pediatr. Endocrinol. Metab. 13 (Suppl 6), 1483-1491.
47. Shoji Y., Uedono Y., Ishikura H., Takeyama N., and, Tanaka T., (1995) DNA damage induced by tumor necrosis factor-alpha in L929 cells is mediated by mitochondrial oxygen radical formation. Immunology 84, 543-548.
48. Snedecor G. W., and, Cochran W. G., (1989) Statistical Methods, 8th ed. Iowa State University Press, Ames. IA.
49. Somjen G. G., (2001) Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol. Rev. 81, 1065-1096.
50. Sorce S., and, Krause K. H., (2009) NOX enzymes in the central nervous system: from signaling to disease. Antioxid. Redox Signal. 11, 2481-2504.
51. Stellwagen D., Beattie E. C., Seo J. Y., and, Malenka R. C., (2005) Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-alpha. J. Neurosci. 25, 3219-3228.
52. Stovner L., Hagen K., Jensen R., Katsarava Z., Lipton R., Scher A., Steiner T., and, Zwart J. A., (2007) The global burden of headache: a documentation of headache prevalence and disability worldwide. Cephalalgia 27, 193-210.
53. Sugimoto K., Murakawa Y., and, Sima A. A., (2002) Expression and localization of insulin receptor in rat dorsal root ganglion and spinal cord. J. Peripher. Nerv. Syst. 7, 44-53.
54. Suh H. S., Cosenza-Nashat M., Choi N., Zhao M. L., Li J. F., Pollard J. W., Jirtle R. L., Goldstein H., and, Lee S. C., (2010) Insulin-like growth factor 2 receptor is an IFNgamma-inducible microglial protein that facilitates intracellular HIV replication: implications for HIV-induced neurocognitive disorders. Am. J. Pathol. 177, 1446-2458.
55. Tamura Y., Kataoka Y., Cui Y., and, Yamada H., (2004) Cellular proliferation in the cerebral cortex following neural excitation in rats. Neurosci. Res. 50, 129-133.
56. Thannickal V. J., and, Fanburg B. L., (2000) Reactive oxygen species in cell signaling. Am. J. Physiol. Lung Cell. Mol. Physiol. 279, L1005-L1028.
57. Thompson C. S., and, Hakim A. M., (2005) Cortical spreading depression modifies components of the inflammatory cascade. Mol. Neurobiol. 32, 51-57.
58. Thorburne S. K., and, Juurlink B. H. J., (1996) Low glutathione and high iron govern the susceptibility of oligodendroglial precursors to oxidative stress. J. Neurochem. 67, 1014-1022.
59. Ushio-Fukai M., (2009) Compartmentalization of redox signaling through NADPH oxidase-derived ROS. Antioxid. Redox Signal. 11, 1289-1299.
60. Viggiano A., Viggiano E., Valentino I., Monda M., and, De Luca B., (2011) Cortical spreading depression affects reactive oxygen species production. Brain Res. 1368, 11-18.
61. Walz W., and, Lang M. K., (1998) Immunocytochemical evidence for a distinct GFAP-negative subpopulation of astrocytes in the adult rat hippocampus. Neurosci. Lett. 257, 127-130.
62. Wang M., Tsai B., Brown J. W., and, Meldrum D. R., (2003) Insulin-like growth factor-1 in myocardial tissue: interactions with tumor necrosis factor. Crit. Care 7, 417-419.
63. Wilson J. X., (1997) Antioxidant defense of the brain: a role for astrocytes. Can. J. Physiol. Pharmacol. 75, 1149-1163.
64. Wong-Riley M. T., (1989) Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci. 12, 94-101.
65. Wong-Riley M. T., (2012) Bigenomic regulation of cytochrome C oxidase in neurons and the tight coupling between neuronal activity and energy metabolism. Adv. Exp. Med. Biol. 748, 283-304.
66. Zhou R., Tardivel A., Thorens B., Choi I., and, Tschopp J., (2009) Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat. Immunol. 11, 136-141.