Gestational exposure to a viral mimetic poly(I:C) Results in long-lasting changes in mitochondrial function by leucocytes in the adult offspring

Mediators of Inflammation

Volumn 2013, Issue , 2013, Pages

  Giulivi, Cecilia ^a   Napoli, Eleonora ^a   Schwartzer, Jared ^a   Careaga, Milo ^a   Ashwood, Paul ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONCANAVALIN A; POLYINOSINIC POLYCYTIDYLIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ADENOSINE TRIPHOSPHATE; CYTOKINE; OXYGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTISM; BIOENERGY; CONTROLLED STUDY; ELECTRON TRANSPORT; ENVIRONMENTAL EXPOSURE; FEMALE; LEUKOCYTE FUNCTION; MALE; MITOCHONDRION; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROGENY; SCHIZOPHRENIA; SINGLE DRUG DOSE; SPLEEN CELL; ANIMAL; ANIMAL BEHAVIOR; BREEDING; C57BL MOUSE; CYTOLOGY; DISEASE MODEL; DRUG EFFECT; ENERGY METABOLISM; LEUKOCYTE; METABOLISM; PREGNANCY; PRENATAL EXPOSURE; RISK FACTOR; SOCIAL BEHAVIOR; SPLEEN; TIME;

ADENOSINE TRIPHOSPHATE; ANIMALS; AUTISTIC DISORDER; BEHAVIOR, ANIMAL; CONCANAVALIN A; CYTOKINES; DISEASE MODELS, ANIMAL; ELECTRON TRANSPORT; ENERGY METABOLISM; FEMALE; LEUKOCYTES; MALE; MATERNAL EXPOSURE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; OXYGEN; POLY I-C; PREGNANCY; PREGNANCY, ANIMAL; PRENATAL EXPOSURE DELAYED EFFECTS; RISK FACTORS; SOCIAL BEHAVIOR; SPLEEN; TIME FACTORS;

EID: 84885661909     PISSN: 09629351     EISSN: 14661861     Source Type: Journal    
DOI: 10.1155/2013/609602     Document Type: Article

References (87)

1. Baio J., Prevalence of Autism spectrum disorders-autism and Developmental Disabilities Monitoring Network, 14 Sites, United States, 2008. Morbidity and Mortality Weekly Report 2012 61 3 1 19 2-s2.0-84859394070
2. Hertz-Picciotto I., Delwiche L., The rise in autism and the role of age at diagnosis. Epidemiology 2009 20 1 84 90 2-s2.0-67349152455 10.1097/EDE.0b013e3181902d15
3. Chugani D. C., Sundram B. S., Behen M., Lee M.-L., Moore G. J., Evidence of altered energy metabolism in autistic children. Progress in Neuro-Psychopharmacology and Biological Psychiatry 1999 23 4 635 641 2-s2.0-0033136483 10.1016/S0278-5846(99)00022-6 (Pubitemid 29268408)
4. Minshew N. J., Goldstein G., Dombrowski S. M., Panchalingam K., Pettegrew J. W., A preliminary 31P MRS study of autism: evidence for undersynthesis and increased degradation of brain membranes. Biological Psychiatry 1993 33 11-12 762 773 2-s2.0-0027337120 (Pubitemid 23234627)
5. Lombard J., Autism: a mitochondrial disorder? Medical Hypotheses 1998 50 6 497 500 2-s2.0-0031748285 10.1016/S0306-9877(98)90270-5 (Pubitemid 28307912)
6. Giulivi C., Zhang Y.-F., Omanska-Klusek A., Ross-Inta C., Wong S., Hertz-Picciotto I., Tassone F., Pessah I. N., Mitochondrial dysfunction in autism. Journal of the American Medical Association 2010 304 21 2389 2396 2-s2.0-78649758904 10.1001/jama.2010.1706
7. Oliveira G., Diogo L., Grazina M., Garcia P., Ataíde A., Marques C., Miguel T., Borges L., Vicente A. M., Oliveira C. R., Mitochondrial dysfunction in autism spectrum disorders: a population-based study. Developmental Medicine and Child Neurology 2005 47 3 185 189 2-s2.0-14044258489 10.1017/S0012162205000332 (Pubitemid 40277824)
8. Chauhan A., Gu F., Essa M. M., Wegiel J., Kaur K., Brown W. T., Chauhan V., Brain region-specific deficit in mitochondrial electron transport chain complexes in children with autism. Journal of Neurochemistry 2011 117 2 209 220 2-s2.0-79953723451 10.1111/j.1471-4159.2011.07189.x
9. Ernster L., Schatz G., Mitochondria: a historical review. Journal of Cell Biology 1981 91 3, part 2 227s 255s 2-s2.0-0019835356 (Pubitemid 12177871)
10. West A. P., Shadel G. S., Ghosh S., Mitochondria in innate immune responses. Nature Reviews Immunology 2011 11 6 389 402 2-s2.0-79957597757 10.1038/nri2975
11. Arnoult D., Soares F., Tattoli I., Girardin S. E., Mitochondria in innate immunity. EMBO Reports 2011 12 9 901 910 2-s2.0-80052275825 10.1038/embor.2011.157
12. Cloonan S. M., Choi A. M. K., Mitochondria: commanders of innate immunity and disease? Current Opinion in Immunology 2012 24 1 32 40 2-s2.0-84857062121 10.1016/j.coi.2011.11.001
13. Fossati G., Moulding D. A., Spiller D. G., Moots R. J., White M. R. H., Edwards S. W., The mitochondrial network of human neutrophils: role in chemotaxis, phagocytosis, respiratory burst activation, and commitment to apoptosis. Journal of Immunology 2003 170 4 1964 1972 2-s2.0-0037442128 (Pubitemid 36197416)
14. Genestier A.-L., Michallet M.-C., Prévost G., Bellot G., Chalabreysse L., Peyrol S., Thivolet F., Etienne J., Lina G., Vallette F. M., Vandenesch F., Genestier L., Staphylococcus aureus Panton-Valentine leukocidin directly targets mitochondria and induces Bax-independent apoptosis of human neutrophils. Journal of Clinical Investigation 2005 115 11 3117 3127 2-s2.0-27644538026 10.1172/JCI22684 (Pubitemid 41567576)
15. Scheel-Toellner D., Wang K., Craddock R., Webb P. R., McGettrick H. M., Assi L. K., Parkes N., Clough L. E., Gulbins E., Salmon M., Lord J. M., Reactive oxygen species limit neutrophil life span by activating death receptor signaling. Blood 2004 104 8 2557 2564 2-s2.0-4944245910 10.1182/blood-2004-01- 0191 (Pubitemid 39331861)
16. Maianski N. A., Geissler J., Srinivasula S. M., Alnemri E. S., Roos D., Kuijpers T. W., Functional characterization of mitochondria in neutrophils: a role restricted to apoptosis. Cell Death and Differentiation 2004 11 2 143 153 2-s2.0-0742306781 10.1038/sj.cdd.4401320 (Pubitemid 38159638)
17. Malanski N. A., Roos D., Kuijpers T. W., Tumor necrosis factor induces a caspase-independent death pathway in human neutrophils. Blood 2003 101 5 1987 1995 2-s2.0-0037370784 10.1182/blood-2002-02-0522 (Pubitemid 36237605)
18. Burlak C., Whitney A. R., Mead D. J., Hackstadt T., DeLeo F. R., Maturation of human neutrophil phagosomes includes incorporation of molecular chaperones and endoplasmic reticulum quality control machinery. Molecular and Cellular Proteomics 2006 5 4 620 634 2-s2.0-33645721361 10.1074/mcp.M500336- MCP200
19. Pithon-Curi T. C., De Melo M. P., De Azevedo R. B., Zorn T. M. T., Curi R., Glutamine utilization by rat neutrophils: presence of phosphate- dependent glutaminase. American Journal of Physiology. Cell Physiology 1997 273 4 C1124 C1129 2-s2.0-0030718610
20. Curi R., Newsholme P., Pithon-Curi T. C., Pires-de-Melo M., Garcia C., Homem-de-Bittencourt P. I. Jr., Guimarães A. R. P., Metabolic fate of glutamine in lymphocytes, macrophages and neutrophils. Brazilian Journal of Medical and Biological Research 1999 32 1 15 21 2-s2.0-0032602636 (Pubitemid 129591668)
21. Fukatsu K., Kudsk K. A., Zarzaur B. L., Wu Y., Hanna M. K., DeWitt R. C., TPN decreases IL-4 and IL-10 mRNA expression in lipopolysaccharide stimulated intestinal lamina propria cells but glutamine supplementation preserves the expression. Shock 2001 15 4 318 322 2-s2.0-0035316623 (Pubitemid 33596726)
22. Yassad A., Husson A., Bion A., Lavoinne A., Synthesis of interleukin 1 β and interleukin 6 by stimulated rat peritoneal macrophages: modulation by glutamine. Cytokine 2000 12 8 1288 1291 2-s2.0-0033624249 10.1006/cyto.1999. 0729 (Pubitemid 30611814)
23. Calder P. C., Yaqoob P., Glutamine and the immune system. Amino Acids 1999 17 3 227 241 2-s2.0-0033489873 (Pubitemid 30113756)
24. Newsholme P., Why is L-glutamine metabolism important to cells of the immune system in health, postinjury, surgery or infection? Journal of Nutrition 2001 131 9, supplement 2-s2.0-0034843181
25. Pithon-Curi T. C., Levada A. C., Lopes L. R., Doi S. Q., Curi R., Glutamine plays a role in superoxide production and the expression of p47phox, p22phox and gp91phox in rat neutrophils. Clinical Science 2002 103 4 403 408 2-s2.0-0036797886 (Pubitemid 35193245)
26. Hwang H. S., Davies S. S., Hill M. F., Pessah I. N., Allen P. D., Roberts L. J., Knollmann B. C., Role of ketoaldehyde protein adducts in ischemic cardiomyopathy. Circulation 2008 118 18 S288 S288
27. Gregg J. P., Lit L., Baron C. A., Hertz-Picciotto I., Walker W., Davis R. A., Croen L. A., Ozonoff S., Hansen R., Pessah I. N., Sharp F. R., Gene expression changes in children with autism. Genomics 2008 91 1 22 29 2-s2.0-37349002507 10.1016/j.ygeno.2007.09.003 (Pubitemid 350298392)
28. Onore C., Careaga M., Ashwood P., The role of immune dysfunction in the pathophysiology of autism. Brain, Behavior, and Immunity 2012 26 3 383 392 2-s2.0-84857190395 10.1016/j.bbi.2011.08.007
29. Wills S., Cabanlit M., Bennett J., Ashwood P., Amaral D., Van De Water J., Autoantibodies in Autism Spectrum Disorders (ASD). Annals of the New York Academy of Sciences 2007 1107 79 91 2-s2.0-34648820674 10.1196/annals.1381.009 (Pubitemid 47528784)
30. Napoli E., Hung C., Wong S., Giulivi C., Toxicity of the flame-retardant BDE-49 on brain mitochondria and neuronal progenitor striatal cells enhanced by a PTEN-deficient background. Toxicological Sciences 2013 132 1 196 210
31. Burgueno A. L., Cabrerizo R., Gonzales M. N., Sookoian S., Pirola C. J., Maternal high-fat intake during pregnancy programs metabolic-syndrome-related phenotypes through liver mitochondrial DNA copy number and transcriptional activity of liver PPARGC1A. Journal of Nutritional Biochemistry 2013 24 1 6 13
32. Garcia A. P., Priego T., Palou M., Sanchez J., Palou A., Pico C., Early alterations in plasma ghrelin levels in offspring of calorie-restricted rats during gestation may be linked to lower sympathetic drive to the stomach. Peptides 2013 39 59 63
33. Garay P. A., Hsiao E. Y., Patterson P. H., McAllister A. K., Maternal immune activation causes age- and region-specific changes in brain cytokines in offspring throughout development. Brain, Behavior, and Immunity 2013 31 54 68
34. Patterson P. H., Modeling autistic features in animals. Pediatric Research 2011 69 5, part 2 34R 40R 2-s2.0-79954610221 10.1203/PDR. 0b013e318212b80f
35. Schwartzer J. J., Careaga M., Onore C. E., Rushakoff J. A., Berman R. F., Ashwood P., Maternal immune activation and strain specific interactions in the development of autism-like behaviors in mice. Translational Psychiatry 2013 3 article e240
36. Tinsley J. H., Chiasson V. L., Mahajan A., Young K. J., Mitchell B. M., Toll-like receptor 3 activation during pregnancy elicits preeclampsia-like symptoms in rats. American Journal of Hypertension 2009 22 12 1314 1319 2-s2.0-70450224468 10.1038/ajh.2009.185
37. Chatterjee P., Chiasson V. L., Kopriva S. E., Young K. J., Chatterjee V., Jones K. A., Mitchell B. M., Interleukin 10 deficiency exacerbates toll-like receptor 3-induced preeclampsia-like symptoms in mice. Hypertension 2011 58 3 489 496 2-s2.0-80051946919 10.1161/HYPERTENSIONAHA.111.172114
38. Cipolla M. J., Houston E. M., Kraig R. P., Bonney E. A., Differential effects of low-dose endotoxin on the cerebral circulation during pregnancy. Reproductive Sciences 2011 18 12 1211 1221 2-s2.0-81555227076 10.1177/1933719111410712
39. Abrahams V. M., Bole-Aldo P., Kim Y. M., Straszewski-Chavez S. L., Chaiworapongsa T., Romero R., Mor G., Divergent trophoblast responses to bacterial products mediated by TLRs. Journal of Immunology 2004 173 7 4286 4296 2-s2.0-4644340557 (Pubitemid 39280656)
40. Pineda A., Verdin-Terán S. L., Camacho A., Moreno-Fierros L., Expression of toll-like receptor TLR-2, TLR-3, TLR-4 and TLR-9 is increased in placentas from patients with preeclampsia. Archives of Medical Research 2011 42 5 382 391 2-s2.0-80052761988 10.1016/j.arcmed.2011.08.003
41. Walker C. K., Anderson K. W., Milano K. M., Ye S., Tancredi D. J., Pessah I. N., Hertz-Picciotto I., Kliman H. J., Trophoblast inclusions are significantly increased in the placentas of children in families at risk for autism. Biological Psychiatry 2013 74 3 204 211 10.1016/j.biopsych.2013.03.006
42. Brown A. S., Derkits E. J., Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. American Journal of Psychiatry 2010 167 3 261 280 2-s2.0-77649167678 10.1176/appi.ajp.2009.09030361
43. Brown A. S., Patterson P. H., Maternal infection and schizophrenia: implications for prevention. Schizophrenia Bulletin 2011 37 2 284 290 2-s2.0-79952123263 10.1093/schbul/sbq146
44. Patterson P. H., Maternal infection and immune involvement in autism. Trends in Molecular Medicine 2011 17 7 389 394 2-s2.0-79959964671 10.1016/j.molmed.2011.03.001
45. Patterson P. H., Maternal infection and autism. Brain, Behavior, and Immunity 2012 26 3 393 2-s2.0-84857192192 10.1016/j.bbi.2011.09.008
46. Brown A. S., Begg M. D., Gravenstein S., Schaefer C. A., Wyatt R. J., Bresnahan M., Babulas V. P., Susser E. S., Serologic evidence of prenatal influenza in the etiology of schizophrenia. Archives of General Psychiatry 2004 61 8 774 780 2-s2.0-3543093977 10.1001/archpsyc.61.8.774 (Pubitemid 39031117)
47. Brown A. S., Hooton J., Schaefer C. A., Zhang H., Petkova E., Babulas V., Perrin M., Gorman J. M., Susser E. S., Elevated maternal interleukin-8 levels and risk of schizophrenia in adult offspring. American Journal of Psychiatry 2004 161 5 889 895 2-s2.0-2442593823 10.1176/appi.ajp.161.5.889 (Pubitemid 38625343)
48. Atladóttir H. Ó., Thorsen P., Østergaard L., Schendel D. E., Lemcke S., Abdallah M., Parner E. T., Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. Journal of Autism and Developmental Disorders 2010 40 12 1423 1430 2-s2.0-78549271649 10.1007/s10803-010-1006-y
49. Gilmore J. H., Jarskog L. F., Vadlamudi S., Lauder J. M., Prenatal infection and risk for schizophrenia: IL-1 β IL-6, and TNF inhibit cortical neuron dendrite development. Neuropsychopharmacology 2004 29 7 1221 1229 2-s2.0-2942683385 10.1038/sj.npp.1300446 (Pubitemid 38780645)
50. Meyer U., Feldon J., Schedlowski M., Yee B. K., Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia. Neuroscience and Biobehavioral Reviews 2005 29 6 913 947 2-s2.0-23244437953 10.1016/j.neubiorev.2004.10.012 (Pubitemid 41097394)
51. Deverman B. E., Patterson P. H., Cytokines and CNS Development. Neuron 2009 64 1 61 78 2-s2.0-70349838218 10.1016/j.neuron.2009.09.002
52. Garay P. A., McAllister A. K., Novel roles for immune molecules in neural development: implications for neurodevelopmental disorders. Frontiers in Synaptic Neuroscience 2010 2 article 136
53. Arrode-Bruses G., Bruses J. L., Maternal immune activation by poly I:C induces expression of cytokines IL-1beta and IL-13, chemokine MCP-1 and colony stimulating factor VEGF in fetal mouse brain. Journal of Neuroinflammation 2012 9 article 83
54. Burton A., Kizhner O., Brown M. B., Peltier M. R., Effect of experimental genital mycoplasmosis on gene expression in the fetal brain. Journal of Reproductive Immunology 2012 93 1 9 16 2-s2.0-84856366745 10.1016/j.jri.2011.11. 005
55. Clancy B., Finlay B. L., Darlington R. B., Anand K. J. S., Extrapolating brain development from experimental species to humans. NeuroToxicology 2007 28 5 931 937 2-s2.0-34948867658 10.1016/j.neuro.2007.01.014 (Pubitemid 47519794)
56. Jewell C. M., Lopez S. C., Irvine D. J., In situ engineering of the lymph node microenvironment via intranodal injection of adjuvant-releasing polymer particles. Proceedings of the National Academy of Sciences of the United States of America 2011 108 38 15745 15750 2-s2.0-80053161466 10.1073/pnas.1105200108
57. Rustin P., Chretien D., Bourgeron T., Gérard B., Rötig A., Saudubray J. M., Munnich A., Biochemical and molecular investigations in respiratory chain deficiencies. Clinica Chimica Acta 1994 228 1 35 51 2-s2.0-0027931039 10.1016/0009-8981(94)90055-8 (Pubitemid 24231224)
58. Hatefi Y., The mitochondrial electron transport and oxidative phosphorylation system. Annual Review of Biochemistry 1985 54 1015 1069 2-s2.0-0021891869 (Pubitemid 15073670)
59. Mandal M., Marzouk A. C., Donnelly R., Ponzio N. M., Maternal immune stimulation during pregnancy affects adaptive immunity in offspring to promote development of TH17 cells. Brain, Behavior, and Immunity 2011 25 5 863 871 2-s2.0-79957917993 10.1016/j.bbi.2010.09.011
60. Smith S. E. P., Li J., Garbett K., Mirnics K., Patterson P. H., Maternal immune activation alters fetal brain development through interleukin-6. Journal of Neuroscience 2007 27 40 10695 10702 2-s2.0-35148872226 10.1523/JNEUROSCI. 2178-07.2007 (Pubitemid 47535869)
61. Farina G. A., York M. R., Di Marzio M., Collins C. A., Meller S., Homey B., Rifkin I. R., Marshak-Rothstein A., Radstake T. R. D. J., Lafyatis R., Poly(I:C) drives type i IFN- and TGF Β -mediated inflammation and dermal fibrosis simulating altered gene expression in systemic sclerosis. Journal of Investigative Dermatology 2010 130 11 2583 2593 2-s2.0-77957940944 10.1038/jid.2010.200
62. Guleria I., Pollard J. W., The trophoblast is a component of the innate immune system during pregnancy. Nature Medicine 2000 6 5 589 593 2-s2.0-0034105358 10.1038/75074 (Pubitemid 30305912)
63. Koga K., Cardenas I., Aldo P., Abrahams V. M., Peng B., Fill S., Romero R., Mor G., Activation of TLR3 in the trophoblast is associated with preterm delivery. American Journal of Reproductive Immunology 2009 61 3 196 212 2-s2.0-60449092852 10.1111/j.1600-0897.2008.00682.x
64. Mor G., Romero R., Aldo P. B., Abrahams V. M., Is the trophoblast an immune regulator? The role of toll-like receptors during pregnancy. Critical Reviews in Immunology 2005 25 5 375 388 2-s2.0-30344461616 10.1615/ CritRevImmunol.v25.i5.30 (Pubitemid 43068932)
65. Suliman H. B., Welty-Wolf K. E., Carraway M. S., Schwartz D. A., Hollingsworth J. W., Piantadosi C. A., Toll-like receptor 4 mediates mitochondrial DNA damage and biogenic responses after heat-inactivated E. coli. The FASEB Journal 2005 19 11 1531 1533 2-s2.0-24644490059 10.1096/fj.04-3500fje (Pubitemid 41279021)
66. Sasai M., Shingai M., Funami K., Yoneyama M., Fujita T., Matsumoto M., Seya T., NAK-associated protein 1 participates in both the TLR3 and the cytoplasmic pathways in type I IFN induction. Journal of Immunology 2006 177 12 8676 8683 2-s2.0-33845416390 (Pubitemid 44893832)
67. Seth R. B., Sun L., Chen Z. J., Antiviral innate immunity pathways. Cell Research 2006 16 2 141 147 2-s2.0-32644456874 10.1038/sj.cr.7310019 (Pubitemid 43247969)
68. Shi H.-X., Liu X., Wang Q., Tang P.-P., Liu X.-Y., Shan Y.-F., Wang C., Mitochondrial ubiquitin ligase MARCH5 promotes TLR7 signaling by attenuating TANK action. PLoS Pathogens 2011 7 5 2-s2.0-79958042278 10.1371/journal.ppat. 1002057 e1002057
69. Carta S., Tassi S., Delfino L., Omenetti A., Raffa S., Torrisi M. R., Martini A., Gattorno M., Rubartelli A., Deficient production of IL-1 receptor antagonist and IL-6 coupled to oxidative stress in cryopyrin-associated periodic syndrome monocytes. Annals of the Rheumatic Diseases 2012 71 9 1577 1581
70. Subramanian N., Natarajan K., Clatworthy M. R., Wang Z., Germain R. N., The adaptor MAVS promotes NLRP3 mitochondrial localization and inflammasome activation. Cell 2013 153 2 348 361
71. Sweeney T. E., Suliman H. B., Hollingsworth J. W., Welty-Wolf K. E., Piantadosi C. A., A toll-like receptor 2 pathway regulates the Ppargc1a/b metabolic co-activators in mice with Staphylococcal aureus sepsis. PLoS One 2011 6 9 2-s2.0-80053151124 10.1371/journal.pone.0025249 e25249
72. Piantadosi C. A., Suliman H. B., Transcriptional control of mitochondrial biogenesis and its interface with inflammatory processes. Biochimica et Biophysica Acta 2012 1820 4 532 541 2-s2.0-84857388966 10.1016/j.bbagen.2012.01. 003
73. Bauerfeld C. P., Rastogi R., Pirockinaite G., Lee I., Hüttemann M., Monks B., Birnbaum M. J., Franchi L., Nunz G., Samavati L., TLR4-mediated AKT activation is Myd88/TRIF dependent and critical for induction of oxidative phosphorylation and mitochondrial transcription factor a in murine macrophages. Journal of Immunology 2012 188 6 2847 2857 2-s2.0-84857869690 10.4049/jimmunol.1102157
74. Sweeney T. E., Suliman H. B., Hollingsworth J. W., Piantadosi C. A., Differential regulation of the PGC family of genes in a mouse model of staphylococcus aureus sepsis. PLoS One 2010 5 7 2-s2.0-77955383048 10.1371/journal.pone.0011606 e11606
75. Oka T., Hikoso S., Yamaguchi O., Taneike M., Takeda T., Tamai T., Oyabu J., Murakawa T., Nakayama H., Nishida K., Akira S., Yamamoto A., Komuro I., Otsu K., Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure. Nature 2012 485 7397 251 255
76. Liu T. F., Brown C. M., El Gazzar M., McPhail L., Millet P., Rao A., Vachharajani V. T., Yoza B. K., McCall C. E., Fueling the flame: bioenergy couples metabolism and inflammation. Journal of Leukocyte Biology 2012 92 3 499 507
77. Fortier M.-E., Luheshi G. N., Boksa P., Effects of prenatal infection on prepulse inhibition in the rat depend on the nature of the infectious agent and the stage of pregnancy. Behavioural Brain Research 2007 181 2 270 277 2-s2.0-34250196472 10.1016/j.bbr.2007.04.016 (Pubitemid 46898665)
78. Meyer U., Nyffeler M., Engler A., Urwyler A., Schedlowski M., Knuesel I., Yee B. K., Feldon J., The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. Journal of Neuroscience 2006 26 18 4752 4762 2-s2.0-33646926705 10.1523/JNEUROSCI.0099-06. 2006 (Pubitemid 44315314)
79. Patterson P. H., Immune involvement in schizophrenia and autism: etiology, pathology and animal models. Behavioural Brain Research 2009 204 2 313 321 2-s2.0-67749114055 10.1016/j.bbr.2008.12.016
80. Serreze D. V., Hamaguchi K., Leiter E. H., Immunostimulation circumvents diabetes in NOD Lt mice. Journal of Autoimmunity 1989 2 6 759 776 2-s2.0-0024795364
81. Sobel D. O., Goyal D., Ahvazi B., Yoon J.-W., Chung Y. H., Bagg A., Harlan D. M., Low dose poly I:C prevents diabetes in the diabetes prone BB rat. Journal of Autoimmunity 1998 11 4 343 352 2-s2.0-0031723365 10.1006/jaut.1998. 0203 (Pubitemid 28428257)
82. Thomas V. A., Woda B. A., Handler E. S., Greiner D. L., Mordes J. P., Rossini A. A., Altered expression of diabetes in BB/Wor rats by exposure to viral pathogens. Diabetes 1991 40 2 255 258 2-s2.0-0025981280
83. Ewel C. H., Sobel D. O., Zeligs B. J., Bellanti J. A., Poly I:C accelerates development of diabetes mellitus in diabetes-prone BB rat. Diabetes 1992 41 8 1016 1021 2-s2.0-0026638034
84. Sobel D. O., Newsome J., Ewel C. H., Bellanti J. A., Abbassi V., Creswell K., Blair O., Poly I:C induces development of diabetes mellitus in BB rat. Diabetes 1992 41 4 515 520 2-s2.0-0026685653
85. Hamlyn J., Duhig M., McGrath J., Scott J., Modifiable risk factors for schizophrenia and autism-shared risk factors impacting on brain development. Neurobiology of Disease 2013 53 3 9
86. Napoli E., Ross-Inta C., Wong S., Hung C., Fujisawa Y., Sakaguchi D., Angelastro J., Omanska-Klusek A., Schoenfeld R., Giulivi C., Mitochondrial dysfunction in Pten haplo-insufficient mice with social deficits and repetitive behavior: interplay between Pten and p53. PLoS One 2012 7 8 e42504
87. Napoli E., Wong S., Giulivi C., Evidence of reactive oxygen species-mediated damage to mitochondrial DNA in children with typical autism. Molecular Autism 2013 4 1, article 2 10.1186/2040-2392-4-2