Insulin-like growth factor-1 lowers spreading depression susceptibility and reduces oxidative stress

Journal of Neurochemistry

Volumn 122, Issue 1, 2012, Pages 221-229

  Grinberg, Yelena Y ^a   Van Drongelen, Wim ^b   Kraig, Richard P ^a  

^a UNIVERSITY OF CHICAGO MEDICAL CENTER   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

antioxidants; hippocampus; IGF 1; migraine; reactive oxygen species; slice culture

Indexed keywords

ANTIOXIDANT; ASCORBIC ACID; HYDROGEN PEROXIDE; INSULIN; REACTIVE OXYGEN METABOLITE; SOMATOMEDIN C;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DISEASE PREDISPOSITION; ENVIRONMENTAL ENRICHMENT; FEMALE; HIPPOCAMPUS; MALE; MIGRAINE; NERVE EXCITABILITY; NEUROPROTECTION; NEWBORN; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SPREADING CORTICAL DEPRESSION;

RATTUS;

EID: 84984586109     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07763.x     Document Type: Article

References (69)

1. Blair L. A., and, Marshall J., (1997) IGF-1 modulates N and L calcium channels in a PI 3-kinase-dependent manner. Neuron 19, 421-429. (Pubitemid 27374239)
2. Brennan K. C., (2011) Turn down the lights!: an irritable occipital cortex in migraine without aura. Neurology 76, 206-207.
3. Bureš J., Burešova O., and, Křivánek J., (1974) The Mechanism and Applications of Leão's Spreading Depression of Electroencephalographic Activity, Academia, Prague.
4. Carro E., Trejo J. L., Busiguina S., and, Torres-Aleman I., (2001) Circulating insulin-like growth factor I mediates the protective effects of physical exercise against brain insults of different etiology and anatomy. J. Neurosci. 21, 5678-5684. (Pubitemid 32692166)
5. Craft S., Baker L. D., Montine T. J., et al. (2011) Intranasal insulin therapy for Alzheimer disease and amnesic mild cognitive impairment: a pilot clinical trial. Arch. Neurol. 69, 29-38.
6. Csiszar A., Labinskyy N., Perez V., et al. (2008) Endothelial function and vascular oxidative stress in long-lived GH/IGF-deficient Ames dwarf mice. Am. J. Physiol. Heart Circ. Physiol. 295, H1882-1894.
7. Darabaneanu S., Overath C. H., Rubin D., Luthje S., Sye W., Niederberger U., Gerber W. D., and, Weisser B., (2011) Aerobic exercise as a therapy option for migraine: a pilot study. Int. J. Sports Med. 32, 455-460.
8. De Kloet E. R., Oitzl M. S., and, Joels M., (1999) Stress and cognition: are corticosteroids good or bad guys? T.I.N.S. 22, 422-426. (Pubitemid 29447722)
9. Dijkhuizen R. M., Beekwilder J. P., van der Worp H. B., Berkelbach van der Sprenkel J. W., Tulleken K. A., and, Nicolay K., (1999) Correlation between tissue depolarizations and damage in focal ischemic rat brain. Brain Res. 840, 194-205. (Pubitemid 29434843)
10. Eckert M. J., and, Abraham W. C., (2010) Physiological effects of enriched environment exposure and LTP induction in the hippocampus in vivo do not transfer faithfully to in vitro slices. Learn. Mem. 17, 480-484.
11. Ekstrand J., Hellsten J., and, Tingstrom A., (2008) Environmental enrichment, exercise and corticosterone affect endothelial cell proliferation in adult rat hippocampus and prefrontal cortex. Neurosci. Lett. 442, 203-207.
12. Fletcher L., Kohli S., Sprague S. M., Scranton R. A., Lipton S. A., Parra A., Jimenez D. F., and, Digicaylioglu M., (2009) Intranasal delivery of erythropoietin plus IGF1 for acute neuroprotection in stroke. Laboratory investigation. J. Neurosurg. 111, 164-170.
13. Gagné J., Gélinas S., Martinoli M. G., Foster T. C., Ohayon M., Thompson R. F., Baudry M., and, Massicotte G., (1998) AMPA receptor properties in adult rat hippocampus following environmental enrichment. Brain Res. 799, 16-25. (Pubitemid 28351199)
14. Goldberg L. D., (2005) The cost of migraine and its treatment. Am. J. Manag. Care 11, S62-S67. (Pubitemid 40875301)
15. Gonzalez de la Vega A., Buno W., Pons S., Garcia-Calderat M. S., Garcia-Galloway E., and, Torres-Aleman I., (2001) Insulin-like growth factor I potentiates kainate receptors through a phosphatidylinositol 3-kinase dependent pathway. NeuroReport 12, 1293-1296. (Pubitemid 32374761)
16. Grinberg Y. Y., and, Kraig R. P,. (2011) Insulin-like growth factor-1 (and insulin) mitigates spreading depression susceptibility: implications for migraine therapy. Soc. Neurosci. 37, Prog #875.07.
17. Grinberg Y. Y., Milton J. G., and, Kraig R. P., (2011) Spreading depression sends microglia on Lévy flights. PLoS ONE, 6, e19294.
18. Guedes R. C., Monteiro J. S., and, Teodosio N. R., (1996) Malnutrition and brain function: experimental studies using the phenomenon of cortical spreading depression. Rev. Bras. Biol. 56 (Su 1 Pt 2), 293-301.
19. Gulati K., Ray A., Pal G., and, Vijayan V.K., (2005) Possible role of free radicals in theophylline-induced seizures in mice. Pharmacol. Biochem. Behav., 82, 241-245. (Pubitemid 41423510)
20. Herring A., Blome M., Ambree O., Sachser N., Paulus W., and, Keyvani K., (2010) Reduction of cerebral oxidative stress following environmental enrichment in mice with Alzheimer-like pathology. Brain Pathol. 20, 166-175.
21. Hu X. H., Markson L. E., Lipton R. B., Stewart W. F., and, Berger M. L., (1999) Burden of migraine in the United States: disability and economic costs. Arch. Intern. Med. 159, 813-818. (Pubitemid 29200307)
22. 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.
23. Jallali N., Ridha H., Thrasivoulou C., Butler P., and, Cowen T., (2007) Modulation of intracellular reactive oxygen species level in chondrocytes by IGF-1, FGF, and TGF-beta1. Connect. Tissue Res. 48, 149-158. (Pubitemid 46860602)
24. Kanzaki M., Zhang Y. Q., Mashima H., Li L., Shibata H., and, Kojima I., (1999) Translocation of a calcium-permeable cation channel induced by insulin-like growth factor-I. Nat. Cell Biol. 1, 165-170. (Pubitemid 129656021)
25. Kempermann G., Fabel K., Ehninger D., Babu H., Leal-Galicia P., Garthe A., and, Wolf S. A., (2010) Why and how physical activity promotes experience-induced brain plasticity. Front. Neurosci. 4, 189.
26. Kraig R. P., Mitchell H. M., Christie-Pope B., Kunkler P. E., White D. M., Tang Y. P., and, Langan G., (2010) TNF-alpha and microglial hormetic involvement in neurological health & migraine. Dose-Response 8, 389-413.
27. Kruger H., Luhmann H. J., and, Heinemann U., (1996) Repetitive spreading depression causes selective suppression of GABAergic function. NeuroReport 7, 2733-2736. (Pubitemid 26403050)
28. Kumar A., Rani A., Tchigranova O., Lee W. H., and, Foster T. C., (2011) Influence of late-life exposure to environmental enrichment or exercise on hippocampal function and CA1 senescent physiology. Neurobiol. Aging 33, 827.e1-828.e17.
29. Kunkler P. E., Hulse R. E., Schmitt M. W., Nicholson C., and, Kraig R. P., (2005) Optical current source density analysis in hippocampal organotypic culture shows that spreading depression occurs with uniquely reversing currents. J. Neurosci. 25, 3952-3961. (Pubitemid 40570428)
30. Lauritzen M., and, Kraig R. P,. (2005) Spreading depression and migraine. in The Headaches (, Olesen J., Goadsby P., Ramadan N., Tfelt-Hansen A., and, WelchK M. A., eds), 3rd edn, pp. 269-276. Lippincott-Raven, Philadelphia.
31. Liu X. F., Fawcett J. F., Hanson L. R., and, Frey W. H. 2nd, (2004) The window of opportunity for treatment of focal cerebral ischemic damage with noninvasive intranasal insulin-like growth factor-I in rats. J. Stroke Cerebrovasc. Dis. 13, 16-23. (Pubitemid 38419175)
32. Lupien S. B., Bluhm E. J., and, Ishii D. N., (2003) Systemic insulin-like growth factor-I administration prevents cognitive impairment in diabetic rats, and brain IGF regulates learning/memory in normal adult rats. J. Neurosci. Res. 74, 512-523. (Pubitemid 37352073)
33. Mack K. J., (2011) Can we help patients with chronic migraine? Neurology 76, 682-683.
34. Mies G., Iijima T., and, Hossmann K. A., (1993) Correlation between peri-infarct DC shifts and ischaemic neuronal damage in rat. NeuroReport 4, 709-711. (Pubitemid 23190898)
35. Miltiadous P., Stamatakis A., Koutsoudaki P. N., Tiniakos D. G., and, Stylianopoulou F., (2011) IGF-I ameliorates hippocampal neurodegeneration and protects against cognitive deficits in an animal model of temporal lobe epilepsy. Exp. Neurol. 231, 223-235.
36. Mitchell H. M., Levasseur V., and, Kraig R. P., (2010a) TNF-α increases spreading depression susceptibility via reduced GABAergic inhibition-implications for the transformation of episodic to chronic migraine. Soc. Neurosci. 36, Prog #346.3.
37. Mitchell H. M., White D. M., and, Kraig R. P,. (2010b) Strategies for study of neuroprotection from cold-preconditioning. J. Vis. Exp. 43, doi: 10.3791/2192.
38. Moskowitz M. A., Nozaki K., and, Kraig R. P., (1993) Neocortical spreading depression provokes the expression of c-fos protein-like immunoreactivity within trigeminal nucleus caudalis via trigeminovascular mechanisms. J. Neurosci. 13, 1167-1177. (Pubitemid 23067603)
39. Mulleners W. M., Chronicle E. P., Palmer J. E., Koehler P. J., and, Vredeveld J. W., (2001) Visual cortex excitability in migraine with and without aura. Headache 41, 565-572. (Pubitemid 32619260)
40. Muller M., Fontana A., Zbinden G., and, Gahwiler B. H., (1993) Effects of interferons and hydrogen peroxide on CA3 pyramidal cells in rat hippocampal slice cultures. Brain Res. 619, 157-162. (Pubitemid 23214317)
41. Nakamura H., Strong A. J., Dohmen C., et al. (2010) Spreading depolarizations cycle around and enlarge focal ischaemic brain lesions. Brain 133, 1994-2006.
42. Nishijima T., Piriz J., Duflot S., et al. (2010) Neuronal activity drives localized blood-brain-barrier transport of serum insulin-like growth factor-I into the CNS. Neuron 67, 834-846.
43. Palmer J. E., Chronicle E. P., Rolan P., and, Mulleners W. M., (2000) Cortical hyperexcitability is cortical underinhibition: evidence from a novel functional test of migraine patients. Cephalalgia 20, 525-532. (Pubitemid 32269469)
44. Papadia S., Soriano F. X., Léveillé F., et al. (2008) Synaptic NMDA receptor activity boosts intrinsic antioxidant defenses. Nat. Neurosci. 11, 476-487. (Pubitemid 351441886)
45. Paszek P., Jackson D. A., and, White M. R. H., (2010) Oscillatory control of signaling molecules. Curr. Opin. Genet. Dev. 20, 670-676.
46. Pérez R., García-Fernández M., Díaz- Sánchez M., Puche J. E., Delgado G., Conchillo M., Muntané J., and, Castilla-Cortázar I., (2008) Mitochondrial protection by low doses of insulin-like growth factor- I in experimental cirrhosis. World J. Gastroenterol. 14, 2731-2739.
47. van Praag H., Kempermann G., and, Gage F. H., (2000) Neural consequences of environmental enrichment. Nat. Rev. Neurosci. 1, 191-198.
48. 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:.
49. Radak Z., Chung H. Y., and, Goto S., (2008) Systemic adaptation to oxidative challenge induced by regular exercise. Free Radic. Biol. Med. 44, 153-159.
50. Ramsey M. M., Adams M. M., Ariwodola O. J., Sonntag W. E., and, Weiner J. L., (2005) Functional characterization of des-IGF-1 action at excitatory synapses in the CA1 region of rat hippocampus. J. Neurophysiol. 94, 247-254. (Pubitemid 40923244)
51. 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.
52. Rice M. E., (1999) Ascorbate compartmentalization in the CNS. Neurotox. Res. 1, 81-90.
53. Rizk N. N., Myatt-Jones J., Rafols J., and, Dunbar J. C., (2007) Insulin like growth factor-1 (IGF-1) decreases ischemia-reperfusion induced apoptosis and necrosis in diabetic rats. Endocrine 31, 66-71. (Pubitemid 350194197)
54. Somjen G. G., (2001) Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol. Rev. 81, 1065-1096. (Pubitemid 32606666)
55. Sonntag W. E., Lynch C., Thornton P., Khan A., Bennett S., and, Ingram R., (2000) The effects of growth hormone and IGF-1 deficiency on cerebrovascular and brain ageing. J. Anat. 197, 575-585. (Pubitemid 32051538)
56. Stark J., Chan C., and, George A. J. T., (2007) Oscillations in the immune system. Immunol. Rev. 216, 213-231. (Pubitemid 46426521)
57. Stockhorst U., de Fries D., Steingrueber H. J., and, Scherbaum W. A., (2004) Insulin and the CNS: effects on food intake, memory, and endocrine parameters and the role of intranasal insulin administration in humans. Physiol. Behav. 83, 47-54. (Pubitemid 39387693)
58. 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. (Pubitemid 46354128)
59. Sukhotinsky I., Dilekoz E., Wang Y., Qin T., Eikermann-Haerter K., Waeber C., and, Ayata C., (2011) Chronic daily cortical spreading depressions suppress spreading depression susceptibility. Cephalalgia 31, 1601-1608.
60. Thor H., Smith M. T., Hartzell P., Bellomo G., Jewell S. A., and, Orrenius S., (1982) The metabolism of menadione (2-methyl-1,4-naphthoquinone) by isolated hepatocytes. A study of the implications of oxidative stress in intact cells. J. Biol. Chem. 257, 12419-12425. (Pubitemid 13180138)
61. 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.
62. Waldbaum S., and, Patel M., (2010) Mitochondria, oxidative stress, and temporal lobe epilepsy. Epilepsy Res. 88, 23-45.
63. Wang Y., Paszek P., Horton C. A., Yue H., White M. R., Kell D. B., Muldoon M. R., and, Broomhead D. S., (2012) A systematic survey of the response of a model NF-KB signaling pathway to TNFα stimulation. J. Theor. Biol. 297, 127-147.
64. Welch K.M., (2005) Brain hyperexcitability: the basis for antiepileptic drugs in migraine prevention. Headache 45, S25-S32. (Pubitemid 40530181)
65. Will B., Galani R., Kelche C., and, Rosenzweig M. R., (2004) Recovery from brain injury in animals: relative efficacy of environmental enrichment, physical exercise or formal training (1990-2002). Prog. Neurobiol. 72, 167-182. (Pubitemid 38591294)
66. Xing C., Yin Y., Chang R., Gong X., He X., and, Xie Z., (2007) Effects of insulin-like growth factor 1 on synaptic excitability in cultured rat hippocampal neurons. Exp. Neurol. 205, 222-229. (Pubitemid 46617508)
67. Yanovsky Y., Brankack J., and, Haas H. L., (1995) Differences of CA3 bursting in DBA/1 and DBA/2 inbred mouse strains with divergent shuttle box performance. Neuroscience 64, 319-325.
68. Young D., Lawlor P. A., Leone P., Dragunow M., and, During M. J., (1999) Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nat. Med. 5, 448-453. (Pubitemid 29180587)
69. Zoladz P. R., and, Diamond D. M,. (2009) Linear and non-linear dose-response functions reveal a hormetic relationship between stress and learning. Dose-Response 7, 132-148.