Neuro-inflammation, blood-brain barrier, seizures and autism

Journal of Neuroinflammation

Volumn 8, Issue , 2011, Pages

  Theoharides, Theoharis C ^a   Zhang, Bodi ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autism; Blood brain barrier; Flavonoids; Mast cells; Neuroinflammation

Indexed keywords

ANTICONVULSIVE AGENT; CORTICOTROPIN RELEASING FACTOR; FC RECEPTOR; FLAVONOID; HIGH MOBILITY GROUP B1 PROTEIN; LUTEOLIN; QUERCETIN; RUTOSIDE;

ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; AUTISM; BLOOD BRAIN BARRIER; CELL ACTIVATION; CELL DEATH; ENCEPHALITIS; HISTOPATHOLOGY; HUMAN; MAST CELL; MASTOCYTOSIS; NONHUMAN; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN EXPRESSION; SEIZURE; BRAIN; HYPERSENSITIVITY; IMMUNOLOGY; INFLAMMATION; PATHOLOGY; PATHOPHYSIOLOGY;

AUTISTIC DISORDER; BLOOD-BRAIN BARRIER; BRAIN; HUMANS; HYPERSENSITIVITY; INFLAMMATION; SEIZURES;

EID: 82255167650     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-8-168     Document Type: Article

References (75)

1. Kogan MD, Blumberg SJ, Schieve LA, Boyle CA, Perrin JM, Ghandour RM, Singh GK, Strickland BB, Trevathan E, van Dyck PC. Prevalence of parent-reported diagnosis of autism spectrum disorder among children in the US, 2007. Pediatrics 2009, 5:1395-1403.
2. Fombonne E. Epidemiology of pervasive developmental disorders. Pediatric Research 2009, 65:591-598. 10.1203/PDR.0b013e31819e7203, 19218885.
3. Volkmar FR, State M, Klin A. Autism and autism spectrum disorders: diagnostic issues for the coming decade. J Child Psychol Psychiatry 2009, 50:108-115. 10.1111/j.1469-7610.2008.02010.x, 19220594.
4. Tuchman R, Rapin I. Epilepsy in autism. Lancet Neurol 2002, 1:352-358. 10.1016/S1474-4422(02)00160-6, 12849396.
5. Trevathan E. Seizures and epilepsy among children with language regression and autistic spectrum disorders. J Child Neurol 2004, 19(Suppl 1):S49-S57.
6. Fombonne E, du Mazaubrun C. Prevalence of infantile autism in four French regions. Soc Psychiatry Psychiatr Epidemiol 1992, 27:203-210. 10.1007/BF00789007, 1411750.
7. Volkmar FR, Nelson DS. Seizure disorders in autism. J Am Acad Child Adolesc Psychiatry 1990, 29:127-129. 10.1097/00004583-199001000-00020, 2295565.
8. Clarke DF, Roberts W, Daraksan M, Dupuis A, McCabe J, Wood H, Snead OC, Weiss SK. The prevalence of autistic spectrum disorder in children surveyed in a tertiary care epilepsy clinic. Epilepsia 2005, 46:1970-1977. 10.1111/j.1528-1167.2005.00343.x, 16393164.
9. Hyde TM, Weinberger DR. Seizures and schizophrenia. Schizophr Bull 1997, 23:611-622.
10. Oblak AL, Rosene DL, Kemper TL, Bauman ML, Blatt GJ. Altered posterior cingulate cortical cyctoarchitecture, but normal density of neurons and interneurons in the posterior cingulate cortex and fusiform gyrus in autism. Autism Res 2011, 4:200-211. 10.1002/aur.188, 21360830.
11. Specchio N, Fusco L, Claps D, Vigevano F. Epileptic encephalopathy in children possibly related to immune-mediated pathogenesis. Brain Dev 2010, 32:51-56. 10.1016/j.braindev.2009.09.017, 19850427.
12. Enstrom AM, Van de Water JA, Ashwood P. Autoimmunity in autism. Curr Opin Investig Drugs 2009, 10:463-473.
13. Theoharides TC, Kempuraj D, Redwood L. Autism: an emerging 'neuroimmune disorder' in search of therapy. Exp Opinion on Pharmacotherapy 2009, 10:2127-2143.
14. Goines P, Van de Water J. The immune system's role in the biology of autism. Curr Opin Neurol 2010, 23:111-117. 10.1097/WCO.0b013e3283373514, 2898160, 20160651.
15. Wills S, Cabanlit M, Bennett J, Ashwood P, Amaral DG, Van de Water J. Detection of autoantibodies to neural cells of the cerebellum in the plasma of subjects with autism spectrum disorders. Brain Behav Immun 2009, 23:64-74. 10.1016/j.bbi.2008.07.007, 2660333, 18706993.
16. Rossi CC, Van de Water J, Rogers SJ, Amaral DG. Detection of plasma autoantibodies to brain tissue in young children with and without autism spectrum disorders. Brain Behav Immun 2011, 25:1123-1135. 10.1016/j.bbi.2011.02.011, 21420487.
17. Li X, Chauhan A, Sheikh AM, Patil S, Chauhan V, Li XM, Ji L, Brown T, Malik M. Elevated immune response in the brain of autistic patients. J Neuroimmunol 2009, 207:111-116. 10.1016/j.jneuroim.2008.12.002, 2770268, 19157572.
18. Dahlgren J, Samuelsson AM, Jansson T, Holmang A. Interleukin-6 in the maternal circulation reaches the rat fetus in mid-gestation. Pediatr Res 2006, 60:147-151. 10.1203/01.pdr.0000230026.74139.18, 16864694.
19. Smith SE, Li J, Garbett K, Mirnics K, Patterson PH. Maternal immune activation alters fetal brain development through interleukin-6. Journal of Neuroscience 2007, 27:10695-10702. 10.1523/JNEUROSCI.2178-07.2007, 2387067, 17913903.
20. Hallmayer J, Cleveland S, Torres A, Phillips J, Cohen B, Torigoe T, Miller J, Fedele A, Collins J, Smith K, Lotspeich L, Croen LA, Ozonoff S, Lajonchere C, Grether JK, Risch N. Genetic Heritability and Shared Environmental Factors Among Twin Pairs With Autism. Arch Gen Psychiatry 2011,
21. Jyonouchi H. Autism spectrum disorders and allergy: observation from a pediatric allergy/immunology clinic. Expert Rev Clin Immunol 2010, 6:397-411. 10.1586/eci.10.18, 20441426.
22. Angelidou A, Alysandratos KD, Asadi S, Zhang B, Francis K, Vasiadi M, Kalogeromitros D, Theoharides TC. Brief Report: "Allergic Symptoms" in Children with Autism Spectrum Disorders. More than Meets the Eye?. J Autism Dev Disord 2011, 41:1579-1585. 10.1007/s10803-010-1171-z, 21210299.
23. Theoharides TC, Angelidou A, Alysandratos KD, Zhang B, Asadi S, Francis K, Toniato E, Kalogeromitros D. Mast cell activation and autism. Biochim Biophys Acta 2011,
24. Kempuraj D, Asadi S, Zhang B, Manola A, Hogan J, Peterson E, Theoharides TC. Mercury induces inflammatory mediator release from human mast cells. J Neuroinflammation 2010, 7:20. 10.1186/1742-2094-7-20, 2850891, 20222982.
25. Galli SJ, Nakae S, Tsai M. Mast cells in the development of adaptive immune responses. Nat Immunol 2005, 6:135-142. 10.1038/ni1158, 15662442.
26. Theoharides TC, Alysandratos KD, Angelidou A, Delivanis DA, Sismanopoulos N, Zhang B, Asadi S, Vasiadi M, Weng Z, Miniati A, Kalogeromitros D. Mast cells and inflammation. Biochim Biophys Acta 2010,
27. Theoharides TC, Doyle R, Francis K, Conti P, Kalogeromitros D. Novel therapeutic targets for autism. Trends Pharmacol Sci 2008, 29:375-382. 10.1016/j.tips.2008.06.002, 18606459.
28. Kandere-Grzybowska K, Letourneau R, Kempuraj D, Donelan J, Poplawski S, Boucher W, Athanassiou A, Theoharides TC. IL-1 induces vesicular secretion of IL-6 without degranulation from human mast cells. J Immunol 2003, 171:4830-4836.
29. Theoharides TC, Kempuraj D, Tagen M, Conti P, Kalogeromitros D. Differential release of mast cell mediators and the pathogenesis of inflammation. Immunol Rev 2007, 217:65-78. 10.1111/j.1600-065X.2007.00519.x, 17498052.
30. Yillar DO, Kucukhuseyin C. The effects of compound 48/80, morphine, and mast cell depletion on electroshock seizure in mice. J Basic Clin Physiol Pharmacol 2008, 19:1-14. 10.1515/JBCPP.2008.19.1.1, 19024791.
31. Singh LK, Pang X, Alexacos N, Letourneau R, Theoharides TC. Acute immobilization stress triggers skin mast cell degranulation via corticotropin-releasing hormone, neurotensin and substance P: A link to neurogenic skin disorders. Brain Behav Immunity 1999, 13:225-239.
32. Antonelli T, Ferraro L, Fuxe K, Finetti S, Fournier J, Tanganelli S, De Mattei M, Tomasini MC. Neurotensin enhances endogenous extracellular glutamate levels in primary cultures of rat cortical neurons: involvement of neurotensin receptor in NMDA induced excitotoxicity. Cereb Cortex 2004, 14:466-473. 10.1093/cercor/bhh008, 15028650.
33. Shulkes A, Harris QL, Lewis SJ, Vajda JE, Jarrott B. Regional brain concentrations of neurotensin following amygdaloid kindled and cortical suprathreshold stimulation-induced seizures in the rat. Neuropeptides 1988, 11:77-81. 10.1016/0143-4179(88)90014-5, 3368040.
34. Angelidou A, Francis K, Vasiadi M, Alysandratos K-D, Zhang B, Theoharides A, Lykouras L, Kalogeromitros D, Theoharides TC. Neurotensin is increased in serum of young children with autistic disorder. J Neuroinflammation 2010, 7:48. 10.1186/1742-2094-7-48, 2936302, 20731814.
35. Ghanizadeh A. Targeting neurotensin as a potential novel approach for the treatment of autism. J Neuroinflammation 2010, 7:58. 10.1186/1742-2094-7-58, 2958902, 20920308.
36. Valent P, Akin C, Escribano L, Fodinger M, Hartmann K, Brockow K, Castells M, Sperr WR, Kluin-Nelemans HC, Hamdy NA, Lortholary O, Robyn J, van Doormaal J, Sotlar K, Hauswirth AW, Arock M, Hermine O, Hellmann A, Triggiani M, Niedoszytko M, Schwartz LB, Orfao A, Horny HP, Metcalfe DD. Standards and standardization in mastocytosis: consensus statements on diagnostics, treatment recommendations and response criteria. Eur J Clin Invest 2007, 37:435-453. 10.1111/j.1365-2362.2007.01807.x, 17537151.
37. Metcalfe DD. Mast cells and mastocytosis. Blood 2008, 112:946-956. 10.1182/blood-2007-11-078097, 2515131, 18684881.
38. Theoharides TC. Autism spectrum disorders and mastocytosis. Int J Immunopathol Pharmacol 2009, 22:859-865.
39. Brockow K, Akin C, Huber M, Metcalfe DD. IL-6 levels predict disease variant and extent of organ involvement in patients with mastocytosis. Clin Immunol 2005, 115:216-223. 10.1016/j.clim.2005.01.011, 15885646.
40. Theoharides TC, Boucher W, Spear K. Serum interleukin-6 reflects disease severity and osteoporosis in mastocytosis patients. Int Arch Allergy Immunol 2002, 128:344-350. 10.1159/000063858, 12218373.
41. Sarrot-Reynauld F, Massot C, Amblard P, Rousset H, Da Costa A, Vital-Durand D, Ninet J, Decousus H. [Systemic mastocytosis: incidence and risks of vasomotor seizures]. Rev Med Interne 1993, 14:1034. 10.1016/S0248-8663(05)80151-1, 7516568.
42. Krowchuk DP, Williford PM, Jorizzo JL, Kandt RS. Solitary mastocytoma producing symptoms mimicking those of a seizure disorder. J Child Neurol 1994, 9:451-453. 10.1177/088307389400900428, 7822745.
43. Banks WA, Erickson MA. The blood-brain barrier and immune function and dysfunction. Neurobiol Dis 2010, 37:26-32. 10.1016/j.nbd.2009.07.031, 19664708.
44. Quan N. Immune-to-brain signaling: how important are the blood-brain barrier-independent pathways?. Mol Neurobiol 2008, 37:142-152. 10.1007/s12035-008-8026-z, 2780323, 18563639.
45. Fabene PF, Navarro Mora G, Martinello M, Rossi B, Merigo F, Ottoboni L, Bach S, Angiari S, Benati D, Chakir A, Zanetti L, Schio F, Osculati A, Marzola P, Nicolato E, Homeister JW, Xia L, Lowe JB, McEver RP, Osculati F, Sbarbati A, Butcher EC, Constantin G. A role for leukocyte-endothelial adhesion mechanisms in epilepsy. Nat Med 2008, 14:1377-1383. 10.1038/nm.1878, 2710311, 19029985.
46. Ransohoff RM. Immunology: Barrier to electrical storms. Nature 2009, 457:155-156. 10.1038/457155a, 19129836.
47. Theoharides TC. Mast cells: the immune gate to the brain. Life Sci 1990, 46:607-617. 10.1016/0024-3205(90)90129-F, 2407920.
48. Gillott A, Standen PJ. Levels of anxiety and sources of stress in adults with autism. J Intellect Disabil 2007, 11:359-370. 10.1177/1744629507083585, 18029412.
49. Kinney DK, Munir KM, Crowley DJ, Miller AM. Prenatal stress and risk for autism. Neurosci Biobehav Rev 2008, 32:1519-1532. 10.1016/j.neubiorev.2008.06.004, 2632594, 18598714.
50. Esposito P, Chandler N, Kandere-Grzybowska K, Basu S, Jacobson S, Connolly R, Tutor D, Theoharides TC. Corticotropin-releasing hormone (CRH) and brain mast cells regulate blood-brain-barrier permeability induced by acute stress. J Pharmacol Exp Ther 2002, 303:1061-1066. 10.1124/jpet.102.038497, 12438528.
51. Theoharides TC, Konstantinidou A. Corticotropin-releasing hormone and the blood-brain-barrier. Front Biosci 2007, 12:1615-1628. 10.2741/2174, 17127408.
52. Rehni AK, Singh TG, Singh N, Arora S. Tramadol-induced seizurogenic effect: a possible role of opioid-dependent histamine H1 receptor activation-linked mechanism. Naunyn Schmiedebergs Arch Pharmacol 2010, 381:11-19. 10.1007/s00210-009-0476-y, 20012267.
53. Theoharides TC, Donelan J, Kandere-Grzybowska K, Konstantinidou A. The role of mast cells in migraine pathophysiology. Brain Res Rev 2005, 49:65-76. 10.1016/j.brainresrev.2004.11.006, 15960987.
54. Ottman R, Lipton RB. Comorbidity of migraine and epilepsy. Neurology 1994, 44:2105-2110.
55. Suemitsu S, Watanabe M, Yokobayashi E, Usui S, Ishikawa T, Matsumoto Y, Yamada N, Okamoto M, Kuroda S. Fcgamma receptors contribute to pyramidal cell death in the mouse hippocampus following local kainic acid injection. Neuroscience 2010, 166:819-831. 10.1016/j.neuroscience.2010.01.004, 20074624.
56. van der Kleij H, Charles N, Karimi K, Mao YK, Foster J, Janssen L, Chang Yang P, Kunze W, Rivera J, Bienenstock J. Evidence for neuronal expression of functional Fc (epsilon and gamma) receptors. The Journal of Allergy and Clinical Immunology 2010, 125:757-760. 10.1016/j.jaci.2009.10.054, 2839037, 20132972.
57. Emanuele E, Boso M, Brondino N, Pietra S, Barale F, Ucelli di Nemi S, Politi P. Increased serum levels of high mobility group box 1 protein in patients with autistic disorder. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:681-683. 10.1016/j.pnpbp.2010.03.020, 20302902.
58. Faraco G, Fossati S, Bianchi ME, Patrone M, Pedrazzi M, Sparatore B, Moroni F, Chiarugi A. High mobility group box 1 protein is released by neural cells upon different stresses and worsens ischemic neurodegeneration in vitro and in vivo. J Neurochem 2007, 103:590-603. 10.1111/j.1471-4159.2007.04788.x, 17666052.
59. Maroso M, Balosso S, Ravizza T, Liu J, Aronica E, Iyer AM, Rossetti C, Molteni M, Casalgrandi M, Manfredi AA, Bianchi ME, Vezzani A. Toll-like receptor 4 and high-mobility group box-1 are involved in ictogenesis and can be targeted to reduce seizures. Nat Med 2010, 16:413-419. 10.1038/nm.2127, 20348922.
60. Zhang B, Alysandratos KD, Angelidou A, Asadi S, Sismanopoulos N, Delivanis DA, Weng Z, Miniati A, Vasiadi M, Katsarou-Katsari A, Miao B, Leeman SE, Kalogeromitros D, Theoharides TC. Human mast cell degranulation and preformed TNF secretion require mitochondrial translocation to exocytosis sites: Relevance to atopic dermatitis. The Journal of Allergy and Clinical Immunology 2011,
61. Zhang B, Angelidou A, Alysandratos KD, Vasiadi M, Francis K, Asadi S, Theoharides A, Sideri K, Lykouras L, Kalogeromitros D, Theoharides TC. Mitochondrial DNA and anti-mitochondrial antibodies in serum of autistic children. J Neuroinflammation 2010, 7:80. 10.1186/1742-2094-7-80, 3001695, 21083929.
62. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W, Brohi K, Itagaki K, Hauser CJ. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 2010, 464:104-107. 10.1038/nature08780, 2843437, 20203610.
63. Lauritzen KH, Moldestad O, Eide L, Carlsen H, Nesse G, Storm JF, Mansuy IM, Bergersen LH, Klungland A. Mitochondrial DNA toxicity in forebrain neurons causes apoptosis, neurodegeneration, and impaired behavior. Mol Cell Biol 2010, 30:1357-1367. 10.1128/MCB.01149-09, 2832488, 20065039.
64. Frye RE, Sreenivasula S, Adams JB. Traditional and non-traditional treatments for autism spectrum disorder with seizures: an on-line survey. BMC Pediatr 2011, 11:37. 10.1186/1471-2431-11-37, 3123184, 21592359.
65. Middleton E, Kandaswami C. The impact of plant flavonoids on mammalian biology: implications for immunity, inflammation and cancer, in the flavonoids. 1993, 619-652. Barborne JB.
66. Kimata M, Shichijo M, Miura T, Serizawa I, Inagaki N, Nagai H. Effects of luteolin, quercetin and baicalein on immunoglobulin E-mediated mediator release from human cultured mast cells. Clin Exp Allergy 2000, 30:501-508. 10.1046/j.1365-2222.2000.00768.x, 10718847.
67. Jang S, Kelley KW, Johnson RW. Luteolin reduces IL-6 production in microglia by inhibiting JNK phosphorylation and activation of AP-1. Proc Natl Acad Sci USA 2008, 105:7534-7539. 10.1073/pnas.0802865105, 2396685, 18490655.
68. Meyer U, Feldon J, Dammann O. Schizophrenia and autism: both shared and disorder-specific pathogenesis via perinatal inflammation?. Pediatr Res 2011, 69:26R-33R. 10.1203/PDR.0b013e318212c196, 21289540.
69. Jang SW, Liu X, Yepes M, Shepherd KR, Miller GW, Liu Y, Wilson WD, Xiao G, Blanchi B, Sun YE, Ye K. A selective TrkB agonist with potent neurotrophic activities by 7,8-dihydroxyflavone. Proc Natl Acad Sci USA 2010, 107:2687-2692. 10.1073/pnas.0913572107, 2823863, 20133810.
70. Parker-Athill E, Luo D, Bailey A, Giunta B, Tian J, Shytle RD, Murphy T, Legradi G, Tan J. Flavonoids, a prenatal prophylaxis via targeting JAK2/STAT3 signaling to oppose IL-6/MIA associated autism. J Neuroimmunol 2009, 217:20-27. 10.1016/j.jneuroim.2009.08.012, 19766327.
71. Kempuraj D, Tagen M, Iliopoulou BP, Clemons A, Vasiadi M, Boucher W, House M, Wolferg A, Theoharides TC. Luteolin inhibits myelin basic protein-induced human mast cell activation and mast cell dependent stimulation of Jurkat T cells. Br J Pharmacol 2008, 155:1076-1084. 2597265, 18806808.
72. Sternberg Z, Chadha K, Lieberman A, Drake A, Hojnacki D, Weinstock-Guttman B, Munschauer F. Immunomodulatory responses of peripheral blood mononuclear cells from multiple sclerosis patients upon in vitro incubation with the flavonoid luteolin: additive effects of IFN-beta. J Neuroinflammation 2009, 6:28. 10.1186/1742-2094-6-28, 2768691, 19825164.
73. Kempuraj D, Madhappan B, Christodoulou S, Boucher W, Cao J, Papadopoulou N, Cetrulo CL, Theoharides TC. Flavonols inhibit proinflammatory mediator release, intracellular calcium ion levels and protein kinase C theta phosphorylation in human mast cells. Br J Pharmacol 2005, 145:934-944. 10.1038/sj.bjp.0706246, 1576204, 15912140.
74. Joshi D, Naidu PS, Singh A, Kulkarni SK. Protective effect of quercetin on alcohol abstinence-induced anxiety and convulsions. J Med Food 2005, 8:392-396. 10.1089/jmf.2005.8.392, 16176153.
75. Nassiri-Asl M, Shariati-Rad S, Zamansoltani F. Anticonvulsive effects of intracerebroventricular administration of rutin in rats. Prog Neuropsychopharmacol Biol Psychiatry 2008, 32:989-993. 10.1016/j.pnpbp.2008.01.011, 18262708.