H1N1 influenza virus induces narcolepsy-like sleep disruption and targets sleep-wake regulatory neurons in mice

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 3, 2016, Pages E368-E377

  Tesoriero, Chiara ^a,b   Codita, Alina ^a   Zhang, Ming Dong ^a   Cherninsky, Andrij ^c   Karlsson, Håkan ^a   Grassi Zucconi, Gigliola ^b   Bertini, Giuseppe ^b   Harkany, Tibor ^a,d   Ljungberg, Karl ^a   Liljeström, Peter ^a   Hökfelt, Tomas G M ^a   Bentivoglio, Marina ^b   Kristensson, Krister ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF VERONA   (Italy)

^c TARAS SHEVCHENKO NATIONAL UNIVERSITY OF KYIV   (Ukraine)

^d Medical University of Vienna   (Austria)

Author keywords

Influenza A virus; Lateral hypothalamus; Locus coeruleus; Noradrenaline; Orexin

Indexed keywords

OREXIN; HOMEODOMAIN PROTEIN; RAG-1 PROTEIN; VIRUS ANTIGEN;

2009 H1N1 INFLUENZA; ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; BRAIN INFECTION; BRAIN STEM; CHINA; CONTROLLED STUDY; FEMALE; FINLAND; HYPOTHALAMUS; INCIDENCE; INFLUENZA A VIRUS (H1N1); MOUSE; NARCOLEPSY; NONHUMAN; PANDEMIC; PATHOGENESIS; PRIORITY JOURNAL; SLEEP WAKING CYCLE; SWITZERLAND; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; ELECTROENCEPHALOGRAPHY; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; NERVE CELL; OLFACTORY BULB; ORTHOMYXOVIRUS INFECTION; PATHOPHYSIOLOGY; PHYSIOLOGY; SLEEP; VIROLOGY; WAKEFULNESS;

ANIMALS; ANTIGENS, VIRAL; ELECTROENCEPHALOGRAPHY; HOMEODOMAIN PROTEINS; HYPOTHALAMUS; IMMUNITY, INNATE; INFLUENZA A VIRUS, H1N1 SUBTYPE; MICE; MICE, INBRED C57BL; MODELS, NEUROLOGICAL; NARCOLEPSY; NEURONS; OLFACTORY BULB; ORTHOMYXOVIRIDAE INFECTIONS; SLEEP; WAKEFULNESS;

EID: 84955153454     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1521463112     Document Type: Article

References (63)

1. Thannickal TC, et al. (2000) Reduced number of hypocretin neurons in human narcolepsy. Neuron 27(3):469-474.
2. Peyron C, et al. (2000) A mutation in a case of early onset narcolepsy and a generalized absence of hypocretin peptides in human narcoleptic brains. Nat Med 6(9): 991-997.
3. Dauvilliers Y, Arnulf I, Mignot E (2007) Narcolepsy with cataplexy. Lancet 369(9560): 499-511.
4. Burgess CR, Scammell TE (2012) Narcolepsy: Neural mechanisms of sleepiness and cataplexy. J Neurosci 32(36):12305-12311.
5. Liblau RS, Vassalli A, Seifinejad A, Tafti M (2015) Hypocretin (orexin) biology and the pathophysiology of narcolepsy with cataplexy. Lancet Neurol 14(3):318-328.
6. Mignot E, et al. (2001) Complex HLA-DR and -DQ interactions confer risk of narcolepsy-cataplexy in three ethnic groups. Am J Hum Genet 68(3):686-699.
7. Hallmayer J, et al. (2009) Narcolepsy is strongly associated with the T-cell receptor alpha locus. Nat Genet 41(6):708-711.
8. Kornum BR, et al. (2011) Common variants in P2RY11 are associated with narcolepsy. Nat Genet 43(1):66-71.
9. Trowsdale J, Knight JC (2013) Major histocompatibility complex genomics and human disease. Annu Rev Genomics Hum Genet 14:301-323.
10. Kornum BR, Faraco J, Mignot E (2011) Narcolepsy with hypocretin/orexin deficiency, infections and autoimmunity of the brain. Curr Opin Neurobiol 21(6):897-903.
11. Han F, et al. (2014) HLA DQB1∗06:02 negative narcolepsy with hypocretin/orexin deficiency. Sleep 37(10):1601-1608.
12. Ollila HM, et al. (2015) HLA-DPB1 and HLA class I confer risk of and protection from narcolepsy. Am J Hum Genet 96(1):136-146.
13. Sturkenboom MC (2015) The narcolepsy-pandemic influenza story: Can the truth ever be unraveled? Vaccine 33(Suppl 2):B6-B13.
14. Partinen M, et al. (2014) Narcolepsy as an autoimmune disease: The role of H1N1 infection and vaccination. Lancet Neurol 13(6):600-613.
15. Ahmed SS, et al. (2015) Antibodies to influenza nucleoprotein cross-react with human hypocretin receptor 2. Sci Transl Med 7(294):294ra105.
16. Picchioni D, Hope CR, Harsh JR (2007) A case-control study of the environmental risk factors for narcolepsy. Neuroepidemiology 29(3-4):185-192.
17. Han F, et al. (2011) Narcolepsy onset is seasonal and increased following the 2009 H1N1 pandemic in China. Ann Neurol 70(3):410-417.
18. Winstone AM, et al. (2014) Clinical features of narcolepsy in children vaccinated with AS03 adjuvanted pandemic A/H1N1 2009 influenza vaccine in England. Dev Med Child Neurol 56(11):1117-1123.
19. Blasio BF, Iversen BG, Tomba GS (2012) Effect of vaccines and antivirals during the major 2009 A(H1N1) pandemic wave in Norway- And the influence of vaccination timing. PLoS One 7(1):e30018.
20. Fang J, Sanborn CK, Renegar KB, Majde JA, Krueger JM (1995) Influenza viral infections enhance sleep in mice. Proc Soc Exp Biol Med 210(3):242-252.
21. Walsh KB, et al. (2011) Suppression of cytokine storm with a sphingosine analog provides protection against pathogenic influenza virus. Proc Natl Acad Sci USA 108(29):12018-12023.
22. Togashi T, Matsuzono Y, Narita M, Morishima T (2004) Influenza-associated acute encephalopathy in Japanese children in 1994-2002. Virus Res 103(1-2):75-78.
23. Kristensson K (2006) Avian influenza and the brain Comments on the occasion of resurrection of the Spanish flu virus. Brain Res Bull 68(6):406-413.
24. Shinya K, et al. (2011) Subclinical brain injury caused by H5N1 influenza virus infection. J Virol 85(10):5202-5207.
25. Brown RE, Basheer R, McKenna JT, Strecker RE, McCarley RW (2012) Control of sleep and wakefulness. Physiol Rev 92(3):1087-1187.
26. Sakurai T (2007) The neural circuit of orexin (hypocretin): Maintaining sleep and wakefulness. Nat Rev Neurosci 8(3):171-181.
27. Carter ME, de Lecea L, Adamantidis A (2013) Functional wiring of hypocretin and LCNE neurons: Implications for arousal. Front Behav Neurosci 7:43.
28. Mombaerts P, et al. (1992) RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68(5):869-877.
29. Aronsson F, Robertson B, Ljunggren HG, Kristensson K (2003) Invasion and persistence of the neuroadapted influenza virus A/WSN/33 in the mouse olfactory system. Viral Immunol 16(3):415-423.
30. Bassetti C, Aldrich MS (1996) Narcolepsy. Neurol Clin 14(3):545-571.
31. Chemelli RM, et al. (1999) Narcolepsy in orexin knockout mice: Molecular genetics of sleep regulation. Cell 98(4):437-451.
32. Scammell TE, Willie JT, Guilleminault C, Siegel JM; International Working Group on Rodent Models of Narcolepsy (2009) A consensus definition of cataplexy in mouse models of narcolepsy. Sleep 32(1):111-116.
33. Tabuchi S, et al. (2014) Conditional ablation of orexin/hypocretin neurons: A new mouse model for the study of narcolepsy and orexin system function. J Neurosci 34(19):6495-6509.
34. Kalinchuk AV, McCarley RW, Porkka-Heiskanen T, Basheer R (2010) Sleep deprivation triggers inducible nitric oxide-dependent nitric oxide production in wake-active basal forebrain neurons. J Neurosci 30(40):13254-13264.
35. Jones BE, Hassani OK (2013) The role of Hcrt/Orx and MCH neurons in sleep-wake state regulation. Sleep 36(12):1769-1772.
36. Willie JT, et al. (2003) Distinct narcolepsy syndromes in Orexin receptor-2 and Orexin null mice: Molecular genetic dissection of Non-REM and REM sleep regulatory processes. Neuron 38(5):715-730.
37. Hara J, et al. (2001) Genetic ablation of orexin neurons in mice results in narcolepsy, hypophagia, and obesity. Neuron 30(2):345-354.
38. Mochizuki T, et al. (2004) Behavioral state instability in orexin knock-out mice. J Neurosci 24(28):6291-6300.
39. Sateia MJ (2014) International classification of sleep disorders-third edition: Highlights and modifications. Chest 146(5):1387-1394.
40. van Riel D, Verdijk R, Kuiken T (2015) The olfactory nerve: A shortcut for influenza and other viral diseases into the central nervous system. J Pathol 235(2):277-287.
41. van Riel D, et al. (2014) Evidence for influenza virus CNS invasion along the olfactory route in an immunocompromised infant. J Infect Dis 210(3):419-423.
42. Sakurai T, et al. (1998) Orexins and orexin receptors: A family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92(4):573-585.
43. de Lecea L, et al. (1998) The hypocretins: Hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci USA 95(1):322-327.
44. Bittencourt JC, et al. (1992) The melanin-concentrating hormone system of the rat brain: An immuno- and hybridization histochemical characterization. J Comp Neurol 319(2):218-245.
45. Shibata M, et al. (2008) Distribution of orexins-containing fibers and contents of orexins in the rat olfactory bulb. Neurosci Res 61(1):99-105.
46. Kristensson K (2011) Microbes' roadmap to neurons. Nat Rev Neurosci 12(6):345-357.
47. Shipley MT, Adamek GD (1984) The connections of the mouse olfactory bulb: A study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Brain Res Bull 12(6):669-688.
48. Panula P, Pirvola U, Auvinen S, Airaksinen MS (1989) Histamine-immunoreactive nerve fibers in the rat brain. Neuroscience 28(3):585-610.
49. Obukuro K, et al. (2013) Nitric oxide mediates selective degeneration of hypothalamic orexin neurons through dysfunction of protein disulfide isomerase. J Neurosci 33(31): 12557-12568.
50. Ayllon J, García-Sastre A (2015) The NS1 protein: A multitasking virulence factor. Curr Top Microbiol Immunol 386:73-107.
51. Brask J, Chauhan A, Hill RH, Ljunggren HG, Kristensson K (2005) Effects on synaptic activity in cultured hippocampal neurons by influenza A viral proteins. J Neurovirol 11(4):395-402.
52. Dang-Vu TT (2012) Structural changes in the narcoleptic brain and their possible relevance for clinical severity. Sleep Med 13(7):775-776.
53. Kristensson K, Nygård M, Bertini G, Bentivoglio M (2010) African trypanosome infections of the nervous system: Parasite entry and effects on sleep and synaptic functions. Prog Neurobiol 91(2):152-171.
54. Fukuyama S, Kawaoka Y (2011) The pathogenesis of influenza virus infections: The contributions of virus and host factors. Curr Opin Immunol 23(4):481-486.
55. Goto H, Kawaoka Y (1998) A novel mechanism for the acquisition of virulence by a human influenza A virus. Proc Natl Acad Sci USA 95(17):10224-10228.
56. Spesock A, et al. (2011) The virulence of 1997 H5N1 influenza viruses in the mouse model is increased by correcting a defect in their NS1 proteins. J Virol 85(14): 7048-7058.
57. Camp JV, et al. (2013) Phenotypic differences in virulence and immune response in closely related clinical isolates of influenza A 2009 H1N1 pandemic viruses in mice. PLoS One 8(2):e56602.
58. Ljungberg K, et al. (2012) Host gene expression signatures discriminate between ferrets infected with genetically similar H1N1 strains. PLoS One 7(7):e40743.
59. Boivin GA, et al. (2012) Mapping of clinical and expression quantitative trait loci in a sex-dependent effect of host susceptibility to mouse-adapted influenza H3N2/HK/1/68. J Immunol 188(8):3949-3960.
60. Horby P, Nguyen NY, Dunstan SJ, Baillie JK (2012) The role of host genetics in susceptibility to influenza: A systematic review. PLoS One 7(3):e33180.
61. Charbonnel N, et al. (2014) Immunogenetic factors affecting susceptibility of humans and rodents to hantaviruses and the clinical course of hantaviral disease in humans. Viruses 6(5):2214-2241.
62. Chapman SJ, Hill AV (2012) Human genetic susceptibility to infectious disease. Nat Rev Genet 13(3):175-188.
63. Kubinak JL, et al. (2013) Experimental viral evolution reveals major histocompatibility complex polymorphisms as the primary host factors controlling pathogen adaptation and virulence. Genes Immun 14(6):365-372.