Human iPSC-derived trigeminal neurons lack constitutive TLR3-dependent immunity that protects cortical neurons from HSV-1 infection

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

Volumn 115, Issue 37, 2018, Pages E8775-E8782

  Zimmer, Bastian ^a   Ewaleifoh, Osefame ^b   Harschnitz, Oliver ^a   Lee, Yoon Seung ^c,d,e   Peneau, Camille ^c   McAlpine, Jessica L ^a   Liu, Becky ^a   Tchieu, Jason ^a   Steinbeck, Julius A ^a   Lafaille, Fabien ^c   Volpi, Stefano ^f   Notarangelo, Luigi D ^g   Casanova, Jean Laurent ^c,d,e   Zhang, Shen Ying ^c,d,e   Smith, Gregory A ^b   Studer, Lorenz ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d HÔPITAL NECKER ENFANTS MALADES   (France)

^e IMAGINE INSTITUTE   (France)

^f UNIVERSITY OF GENOA   (Italy)

^g NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Antiviral immunity; HSE; HSV 1; TG neurons; TLR3

Indexed keywords

ADENOSINE TRIPHOSPHATE; BETA INTERFERON; CAPSAICIN; CELL SURFACE MARKER; GANGLIOSIDE GD2; POLYINOSINIC POLYCYTIDYLIC ACID; TOLL LIKE RECEPTOR 3; ANTIVIRUS AGENT; TLR3 PROTEIN, HUMAN;

ARTICLE; BRAIN CELL; CELL DIFFERENTIATION; CELL FUNCTION; CONTROLLED STUDY; DISEASE EXACERBATION; EMBRYONIC STEM CELL; FEMALE; HERPES SIMPLEX ENCEPHALITIS; HUMAN; HUMAN ALPHAHERPESVIRUS 1; HUMAN CELL; IN VITRO STUDY; INDUCED PLURIPOTENT STEM CELL; LATENT VIRUS INFECTION; NONHUMAN; PRIORITY JOURNAL; PURIFICATION; TRIGEMINUS GANGLION; VIRUS CELL INTERACTION; VIRUS RESISTANCE; BRAIN CORTEX; CELL CULTURE; CHILD; CYTOLOGY; DRUG EFFECT; GENETICS; IMMUNITY; IMMUNOLOGY; METABOLISM; MUTATION; NERVE CELL; PHYSIOLOGY; VIROLOGY;

ANTIVIRAL AGENTS; CELL DIFFERENTIATION; CELLS, CULTURED; CEREBRAL CORTEX; CHILD; HERPESVIRUS 1, HUMAN; HUMANS; IMMUNITY; INDUCED PLURIPOTENT STEM CELLS; INTERFERON-BETA; MUTATION; NEURONS; POLY I-C; TOLL-LIKE RECEPTOR 3; TRIGEMINAL GANGLION;

EID: 85053030844     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1809853115     Document Type: Article

References (45)

1. Roizman B, Whitley RJ (2013) An inquiry into the molecular basis of HSV latency and reactivation. Annu Rev Microbiol 67:355–374.
2. Whitley RJ (2006) Herpes simplex encephalitis: Adolescents and adults. Antiviral Res 71:141–148.
3. Whitley RJ, et al.; Clinical Assessment (1982) Herpes simplex encephalitis. JAMA 247: 317–320.
4. Lafaille FG, et al. (2015) Deciphering human cell-autonomous anti-HSV-1 immunity in the central nervous system. Front Immunol 6:208.
5. Kennedy PG (2004) Viral encephalitis: Causes, differential diagnosis, and management. J Neurol Neurosurg Psychiatry 75(Suppl 1):i10–i15.
6. Gordon B, Selnes OA, Hart J, Jr, Hanley DF, Whitley RJ (1990) Long-term cognitive sequelae of acyclovir-treated herpes simplex encephalitis. Arch Neurol 47:646–647.
7. Bereczky-Veress B, et al. (2008) Host strain-dependent difference in susceptibility in a rat model of herpes simplex type 1 encephalitis. J Neurovirol 14:102–118.
8. Johnson RT, Mims GA (1968) Pathogenesis for viral infections of the nervous system. N Engl J Med 278:84–92.
9. Takahashi K, et al. (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–872.
10. Yu J, et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318:1917–1920.
11. Cherry AB, Daley GQ (2013) Reprogrammed cells for disease modeling and regenerative medicine. Annu Rev Med 64:277–290.
12. Osakada F, Takahashi M (2011) Neural induction and patterning in Mammalian pluripotent stem cells. CNS Neurol Disord Drug Targets 10:419–432.
13. Chambers SM, et al. (2012) Combined small-molecule inhibition accelerates developmental timing and converts human pluripotent stem cells into nociceptors. Nat Biotechnol 30:715–720.
14. Fattahi F, et al. (2016) Deriving human ENS lineages for cell therapy and drug discovery in Hirschsprung disease. Nature 531:105–109.
15. Wainger BJ, et al. (2015) Modeling pain in vitro using nociceptor neurons reprogrammed from fibroblasts. Nat Neurosci 18:17–24.
16. Hoelting L, et al. (2016) Stem cell-derived immature human dorsal root ganglia neurons to identify peripheral neurotoxicants. Stem Cells Transl Med 5:476–487.
17. Edvinsson L (2017) The trigeminovascular pathway: Role of CGRP and CGRP receptors in migraine. Headache 57:47–55.
18. Casrouge A, et al. (2006) Herpes simplex virus encephalitis in human UNC-93B deficiency. Science 314:308–312.
19. Zhang SY, et al. (2007) TLR3 deficiency in patients with herpes simplex encephalitis. Science 317:1522–1527.
20. Sancho-Shimizu V, et al. (2011) Herpes simplex encephalitis in children with autosomal recessive and dominant TRIF deficiency. J Clin Invest 121:4889–4902.
21. Herman M, et al. (2012) Heterozygous TBK1 mutations impair TLR3 immunity and underlie herpes simplex encephalitis of childhood. J Exp Med 209:1567–1582.
22. Lim HK, et al. (2014) TLR3 deficiency in herpes simplex encephalitis: High allelic heterogeneity and recurrence risk. Neurology 83:1888–1897.
23. Andersen LL, et al. (2015) Functional IRF3 deficiency in a patient with herpes simplex encephalitis. J Exp Med 212:1371–1379.
24. Zhang SY, et al. (2013) TLR3 immunity to infection in mice and humans. Curr Opin Immunol 25:19–33.
25. Lafaille FG, et al. (2012) Impaired intrinsic immunity to HSV-1 in human iPSC-derived TLR3-deficient CNS cells. Nature 491:769–773.
26. Tchieu J, et al. (2017) A modular platform for differentiation of human PSCs into all major ectodermal lineages. Cell Stem Cell 21:399–410.e7.
27. Dincer Z, et al. (2013) Specification of functional cranial placode derivatives from human pluripotent stem cells. Cell Rep 5:1387–1402.
28. McCabe KL, Sechrist JW, Bronner-Fraser M (2009) Birth of ophthalmic trigeminal neurons initiates early in the placodal ectoderm. J Comp Neurol 514:161–173.
29. Vincent M, Thiery JP (1984) A cell surface marker for neural crest and placodal cells: Further evolution in peripheral and central nervous system. Dev Biol 103:468–481.
30. Zimmer B, et al. (2016) Derivation of diverse hormone-releasing pituitary cells from human pluripotent stem cells. Stem Cell Rep 6:858–872.
31. Yuan SH, et al. (2011) Cell-surface marker signatures for the isolation of neural stem cells, glia and neurons derived from human pluripotent stem cells. PLoS One 6: e17540.
32. Marmigère F, Ernfors P (2007) Specification and connectivity of neuronal subtypes in the sensory lineage. Nat Rev Neurosci 8:114–127.
33. Guo Y, et al. (2011) Herpes simplex virus encephalitis in a patient with complete TLR3 deficiency: TLR3 is otherwise redundant in protective immunity. J Exp Med 208: 2083–2098.
34. Huffmaster NJ, Sollars PJ, Richards AL, Pickard GE, Smith GA (2015) Dynamic ubiq-uitination drives herpesvirus neuroinvasion. Proc Natl Acad Sci USA 112:12818–12823.
35. Smith G (2012) Herpesvirus transport to the nervous system and back again. Annu Rev Microbiol 66:153–176.
36. Picard C, et al. (2018) International Union of Immunological Societies: 2017 Primary Immunodeficiency Diseases Committee Report on inborn errors of immunity. J Clin Immunol 38:96–128.
37. Bousfiha A, et al. (2018) The 2017 IUIS phenotypic classification for primary immu-nodeficiencies. J Clin Immunol 38:129–143.
38. Rosato PC, Leib DA (2014) Intrinsic innate immunity fails to control herpes simplex virus and vesicular stomatitis virus replication in sensory neurons and fibroblasts. J Virol 88:9991–10001.
39. Song R, et al. (2016) Two modes of the axonal interferon response limit alpha-herpesvirus neuroinvasion. MBio 7:e02145-e15.
40. Blanchard JW, et al. (2015) Selective conversion of fibroblasts into peripheral sensory neurons. Nat Neurosci 18:25–35.
41. Chen G (2008) Splitting hESC/hiPSC Lines with EDTA in Feeder Free Conditions (StemBook, Cambridge, MA).
42. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101–1108.
43. Steinbeck JA, et al. (2016) Functional connectivity under optogenetic control allows modeling of human neuromuscular disease. Cell Stem Cell 18:134–143.
44. Calder EL, et al. (2015) Retinoic acid-mediated regulation of GLI3 enables efficient motoneuron derivation from human ESCs in the absence of extrinsic SHH activation. J Neurosci 35:11462–11481.
45. Shaner NC, et al. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22: 1567–1572.