Role of herpes simplex virus 1 γ34.5 in the regulation of IRF3 signaling

Journal of Virology

Volumn 91, Issue 23, 2017, Pages

  Manivanh, Richard ^a   Mehrbach, Jesse ^a   Knipe, David M ^b   Leib, David A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Herpes simplex virus; ICP0; ICP34.5; Innate immunity; Interferons; IRF3; Recombinant viruses; RL1; TBK1; Viral pathogenesis

Indexed keywords

AMINO ACID; BECLIN 1; CARRIER PROTEINS AND BINDING PROTEINS; INFECTED CELL PROTEIN 0; INITIATION FACTOR 2ALPHA; INTERFERON REGULATORY FACTOR 3; PHOSPHOTRANSFERASE; PROTEIN ICP 34 5; TANK BINDING KINASE 1; UNCLASSIFIED DRUG; VIRAL PROTEIN; BETA INTERFERON; GAMMA 34.5 PROTEIN, HUMAN HERPESVIRUS 1; INTERFERON; PROTEIN SERINE THREONINE KINASE; TBK1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INFECTION; CONTROLLED STUDY; EMBRYO; GENE STRUCTURE; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1 GAMMA 34 5; HUMAN; HUMAN ALPHAHERPESVIRUS 1; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS VIRULENCE; WILD TYPE; ANIMAL; CHEMISTRY; CHLOROCEBUS AETHIOPS; DRUG EFFECTS; FIBROBLAST; GENETICS; HOST PATHOGEN INTERACTION; INNATE IMMUNITY; METABOLISM; PATHOGENICITY; PHOSPHORYLATION; VERO CELL LINE; VIROLOGY;

ANIMALS; BECLIN-1; CERCOPITHECUS AETHIOPS; FIBROBLASTS; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; INTERFERONS; MICE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; VERO CELLS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 85033791187     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01156-17     Document Type: Article

References (77)

1. Virgin HW, Wherry EJ, Ahmed R. 2009. Redefining chronic viral infection. Cell 138:30-50. https://doi.org/10.1016/j.cell.2009.06.036
2. Efstathiou S, Minson AC, Field HJ, Anderson JR, Wildy P. 1986. Detection of herpes simplex virus-specific DNA sequences in latently infected mice and in humans. J Virol 57:446-455
3. Rock DL, Fraser NW. 1983. Detection of HSV-1 genome in central nervous system of latently infected mice. Nature 302:523-525. https://doi.org/10.1038/302523a0
4. Rock DL, Fraser NW. 1985. Latent herpes simplex virus type 1 DNA contains two copies of the virion DNA joint region. J Virol 55:849-852
5. Mahla RS, Reddy MC, Prasad DVR, Kumar H. 2013. Sweeten PAMPs: role of sugar complexed PAMPs in innate immunity and vaccine biology. Front Immunol 4:248. https://doi.org/10.3389/fimmu.2013.00248
6. Medzhitov R, Preston-Hurlburt P, Janeway CA. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388:394-397. https://doi.org/10.1038/41131
7. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, Golenbock DT, Coyle AJ, Liao S-M, Maniatis T. 2003. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4:491-496
8. Pomerantz JL, Baltimore D. 1999. NF-kappaB activation by a signaling complex containing TRAF2, TANK and TBK1, a novel IKK-related kinase. EMBO J 18:6694-6704. https://doi.org/10.1093/emboj/18.23.6694
9. Hiscott J, Pitha P, Genin P, Nguyen H, Heylbroeck C, Mamane Y, Algarte M, Lin R. 1999. Triggering the interferon response: the role of IRF-3 transcription factor. J Interferon Cytokine Res 19:1-13. https://doi.org/10.1089/107999099314360
10. Leonard WJ. 2001. Role of Jak kinases and STATs in cytokine signal transduction. Int J Hematol 73:271-277. https://doi.org/10.1007/BF02981951
11. Novick D, Cohen B, Rubinstein M. 1994. The human interferon alpha/beta receptor: characterization and molecular cloning. Cell 77:391-400. https://doi.org/10.1016/0092-8674(94)90154-6
12. Katze MG, He Y, Gale M. 2002. Viruses and interferon: a fight for supremacy. Nat Rev Immunol 2:675-687. https://doi.org/10.1038/nri888
13. Feng GS, Chong K, Kumar A, Williams BR. 1992. Identification of doublestranded RNA-binding domains in the interferon-induced doublestranded RNA-activated p68 kinase. Proc Natl Acad Sci U S A 89: 5447-5451. https://doi.org/10.1073/pnas.89.12.5447
14. Thomis DC, Doohan JP, Samuel CE. 1992. Mechanism of interferon action: cDNA structure, expression, and regulation of the interferon-induced, RNAdependent P1/eIF-2 alpha protein kinase from human cells. Virology 188: 33-46. https://doi.org/10.1016/0042-6822(92)90732-5
15. Lin R, Noyce RS, Collins SE, Everett RD, Mossman KL. 2004. The herpes simplex virus ICP0 RING finger domain inhibits IRF3-and IRF7-mediated activation of interferon-stimulated genes. J Virol 78:1675-1684. https://doi.org/10.1128/JVI.78.4.1675-1684.2004
16. Paladino P, Collins SE, Mossman KL. 2010. Cellular localization of the herpes simplex virus ICP0 protein dictates its ability to block IRF3-mediated innate immune responses. PLoS One 5:e10428. https://doi.org/10.1371/journal.pone.0010428
17. Wang S, Wang K, Lin R, Zheng C. 2013. Herpes simplex virus 1 serine/threonine kinase US3 hyperphosphorylates IRF3 and inhibits beta interferon production. J Virol 87:12814-12827. https://doi.org/10.1128/JVI.02355-13
18. Verpooten D, Ma Y, Hou S, Yan Z, He B. 2009. Control of TANK-binding kinase 1-mediated signaling by the gamma(1)34.5 protein of herpes simplex virus 1. J Biol Chem 284:1097-1105. https://doi.org/10.1074/jbc.M805905200
19. Ma Y, Jin H, Valyi-Nagy T, Cao Y, Yan Z, He B. 2012. Inhibition of TANK binding kinase 1 by herpes simplex virus 1 facilitates productive infection. J Virol 86:2188-2196. https://doi.org/10.1128/JVI.05376-11
20. Orvedahl A, Alexander D, Tallóczy Z, Sun Q, Wei Y, Zhang W, Burns D, Leib DA, Levine B. 2007. HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 1:23-35. https://doi.org/10.1016/j.chom.2006.12.001
21. Leib DA, Alexander DE, Cox D, Yin J, Ferguson TA. 2009. Interaction of ICP34.5 with Beclin 1 modulates herpes simplex virus type 1 pathogenesis through control of CD4+ T-cell responses. J Virol 83:12164-12171. https://doi.org/10.1128/JVI.01676-09
22. Gobeil PAM, Leib DA. 2012. Herpes simplex virus γ34.5 interferes with autophagosome maturation and antigen presentation in dendritic cells. mBio 3:e00267-e00212. https://doi.org/10.1128/mBio.00267-12
23. English L, Chemali M, Duron J, Rondeau C, Laplante A, Gingras D, Alexander D, Leib D, Norbury C, Lippé R, Desjardins M. 2009. Autophagy enhances the presentation of endogenous viral antigens on MHC class I molecules during HSV-1 infection. Nat Immunol 10:480-487. https://doi.org/10.1038/ni.1720
24. Perng GC, Ghiasi H, Slanina SM, Nesburn AB, Wechsler SL. 1996. Highdose ocular infection with a herpes simplex virus type 1 ICP34.5 deletion mutant produces no corneal disease or neurovirulence yet results in wild-type levels of spontaneous reactivation. J Virol 70:2883-2893
25. Kanai R, Zaupa C, Sgubin D, Antoszczyk SJ, Martuza RL, Wakimoto H, Rabkin SD. 2012. Effect of γ34.5 deletions on oncolytic herpes simplex virus activity in brain tumors. J Virol 86:4420-4431. https://doi.org/10.1128/JVI.00017-12
26. Broberg EK, Peltoniemi J, Nygårdas M, Vahlberg T, Röyttä M, Hukkanen V. 2004. Spread and replication of and immune response to gamma134.5-negative herpes simplex virus type 1 vectors in BALB/c mice. J Virol 78:13139-13152. https://doi.org/10.1128/JVI.78.23.13139-13152.2004
27. Mehta H, Muller J, Markovitz NS. 2010. Ultrastructural analysis of ICP34.5-herpes simplex virus 1 replication in mouse brain cells in vivo. J Virol 84:10982-10990. https://doi.org/10.1128/JVI.00337-10
28. Wilcox DR, Longnecker R. 2016. The herpes simplex virus neurovirulence factor γ34.5: revealing virus-host interactions. PLoS Pathog 12:e1005449. https://doi.org/10.1371/journal.ppat.1005449
29. Chou J, Kern ER, Whitley RJ, Roizman B. 1990. Mapping of herpes simplex virus-1 neurovirulence to gamma 134.5, a gene nonessential for growth in culture. Science 250:1262-1266. https://doi.org/10.1126/science.2173860
30. Chou J, Chen JJ, Gross M, Roizman B. 1995. Association of a M(r) 90, 000 phosphoprotein with protein kinase PKR in cells exhibiting enhanced phosphorylation of translation initiation factor eIF-2 alpha and premature shutoff of protein synthesis after infection with gamma 134.5-mutants of herpes simplex virus 1. Proc Natl Acad Sci U S A 92: 10516-10520. https://doi.org/10.1073/pnas.92.23.10516
31. Chou J, Roizman B. 1990. The herpes simplex virus 1 gene for ICP34.5, which maps in inverted repeats, is conserved in several limited-passage isolates but not in strain 17syn+. J Virol 64:1014-1020
32. He B, Gross M, Roizman B. 1997. The gamma(1)34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1alpha to dephosphorylate the alpha subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNA-activated protein kinase. Proc Natl Acad Sci U S A 94:843-848. https://doi.org/10.1073/pnas.94.3.843
33. Leib DA, Machalek MA, Williams BR, Silverman RH, Virgin HW. 2000. Specific phenotypic restoration of an attenuated virus by knockout of a host resistance gene. Proc Natl Acad Sci U S A 97:6097-6101. https://doi.org/10.1073/pnas.100415697
34. Mohr I, Gluzman Y. 1996. A herpesvirus genetic element which affects translation in the absence of the viral GADD34 function. EMBO J 15: 4759-4766
35. Mohr I, Sternberg D, Ward S, Leib D, Mulvey M, Gluzman Y. 2001. A herpes simplex virus type 1 gamma34.5 second-site suppressor mutant that exhibits enhanced growth in cultured glioblastoma cells is severely attenuated in animals. J Virol 75:5189-5196. https://doi.org/10.1128/JVI.75.11.5189-5196.2001
36. Wang Y, Yang Y, Wu S, Pan S, Zhou C, Ma Y, Ru Y, Dong S, He B, Zhang C, Cao Y. 2014. p32 is a novel target for viral protein ICP34.5 of herpes simplex virus type 1 and facilitates viral nuclear egress. J Biol Chem 289:35795-35805. https://doi.org/10.1074/jbc.M114.603845
37. Sharma S, ten Oever BR, Grandvaux N, Zhou G-P, Lin R, Hiscott J. 2003. Triggering the interferon antiviral response through an IKK-related pathway. Science 300:1148-1151. https://doi.org/10.1126/science.1081315
38. McWhirter SM, Fitzgerald KA, Rosains J, Rowe DC, Golenbock DT, Maniatis T. 2004. IFN-regulatory factor 3-dependent gene expression is defective in Tbk1-deficient mouse embryonic fibroblasts. Proc Natl Acad Sci U S A 101:233-238. https://doi.org/10.1073/pnas.2237236100
39. Lin R, Heylbroeck C, Pitha PM, Hiscott J. 1998. Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol Cell Biol 18:2986-2996. https://doi.org/10.1128/MCB.18.5.2986
40. Bolovan CA, Sawtell NM, Thompson RL. 1994. ICP34.5 mutants of herpes simplex virus type 1 strain 17syn+ are attenuated for neurovirulence in mice and for replication in confluent primary mouse embryo cell cultures. J Virol 68:48-55
41. Brown SM, Harland J, MacLean AR, Podlech J, Clements JB. 1994. Cell type and cell state determine differential in vitro growth of nonneurovirulent ICP34.5-negative herpes simplex virus types 1 and 2. J Gen Virol 75:2367-2377. https://doi.org/10.1099/0022-1317-75-9-2367
42. Melroe GT, Silva L, Schaffer PA, Knipe DM. 2007. Recruitment of activated IRF-3 and CBP/p300 to herpes simplex virus ICP0 nuclear foci: potential role in blocking IFN-beta induction. Virology 360:305-321. https://doi.org/10.1016/j.virol.2006.10.028
43. Melroe GT, DeLuca NA, Knipe DM. 2004. Herpes simplex virus 1 has multiple mechanisms for blocking virus-induced interferon production. J Virol 78:8411-8420. https://doi.org/10.1128/JVI.78.16.8411-8420.2004
44. Loret S, Guay G, Lippé R. 2008. Comprehensive characterization of extracellular herpes simplex virus type 1 virions. J Virol 82:8605-8618. https://doi.org/10.1128/JVI.00904-08
45. Mulvey M, Poppers J, Ladd A, Mohr I. 1999. A herpesvirus ribosomeassociated, RNA-binding protein confers a growth advantage upon mutants deficient in a GADD34-related function. J Virol 73:3375-3385
46. Wu S, Pan S, Zhang L, Baines J, Roller R, Ames J, Yang M, Wang J, Chen D, Liu Y, Zhang C, Cao Y, He B. 2016. Herpes simplex virus 1 induces phosphorylation and reorganization of lamin A/C through the γ134.5 protein that facilitates nuclear egress. J Virol 90:10414-10422. https://doi.org/10.1128/JVI.01392-16
47. Cheng G, Yang K, He B. 2003. Dephosphorylation of eIF-2alpha mediated by the gamma(1)34.5 protein of herpes simplex virus type 1 is required for viral response to interferon but is not sufficient for efficient viral replication. J Virol 77:10154-10161. https://doi.org/10.1128/JVI.77.18.10154-10161.2003
48. Harrow S, Papanastassiou V, Harland J, Mabbs R, Petty R, Fraser M, Hadley D, Patterson J, Brown SM, Rampling R. 2004. HSV1716 injection into the brain adjacent to tumour following surgical resection of highgrade glioma: safety data and long-term survival. Gene Ther 11: 1648-1658. https://doi.org/10.1038/sj.gt.3302289
49. Tallóczy Z, Virgin HW, Levine B. 2006. PKR-dependent autophagic degradation of herpes simplex virus type 1. Autophagy 2:24-29. https://doi.org/10.4161/auto.2176
50. Tallóczy Z, Jiang W, Virgin HW, Leib DA, Scheuner D, Kaufman RJ, Eskelinen E-L, Levine B. 2002. Regulation of starvation-and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc Natl Acad Sci U S A 99:190-195. https://doi.org/10.1073/pnas.012485299
51. Liu X-Y, Wei B, Shi H-X, Shan Y-F, Wang C. 2010. Tom70 mediates activation of interferon regulatory factor 3 on mitochondria. Cell Res 20:994-1011. https://doi.org/10.1038/cr.2010.103
52. Xu C, Liu J, Hsu L-C, Luo Y, Xiang R, Chuang T-H. 2011. Functional interaction of heat shock protein 90 and Beclin 1 modulates Toll-like receptor-mediated autophagy. FASEB J 25:2700-2710. https://doi.org/10.1096/fj.10-167676
53. Zalckvar E, Berissi H, Eisenstein M, Kimchi A. 2009. Phosphorylation of Beclin 1 by DAP-kinase promotes autophagy by weakening its interactions with Bcl-2 and Bcl-XL. Autophagy 5:720-722. https://doi.org/10.4161/auto.5.5.8625
54. Zalckvar E, Berissi H, Mizrachy L, Idelchuk Y, Koren I, Eisenstein M, Sabanay H, Pinkas-Kramarski R, Kimchi A. 2009. DAP-kinase-mediated phosphorylation on the BH3 domain of beclin 1 promotes dissociation of beclin 1 from Bcl-XL and induction of autophagy. EMBO Rep 10: 285-292. https://doi.org/10.1038/embor.2008.246
55. Maiuri MC, Criollo A, Tasdemir E, Vicencio JM, Tajeddine N, Hickman JA, Geneste O, Kroemer G. 2007. BH3-only proteins and BH3 mimetics induce autophagy by competitively disrupting the interaction between Beclin 1 and Bcl-2/Bcl-X(L). Autophagy 3:374-376. https://doi.org/10.4161/auto.4237
56. Wang L, Li S, Dorf ME. 2012. NEMO binds ubiquitinated TANK-binding kinase 1 (TBK1) to regulate innate immune responses to RNA viruses. PLoS One 7:e43756. https://doi.org/10.1371/journal.pone.0043756
57. Collins SE, Noyce RS, Mossman KL. 2004. Innate cellular response to virus particle entry requires IRF3 but not virus replication. J Virol 78: 1706-1717. https://doi.org/10.1128/JVI.78.4.1706-1717.2004
58. Pitha PM, Au W-C, Lowther W, Juang Y-T, Schafer SL, Burysek L, Hiscott J, Moore PA. 1998. Role of the interferon regulatory factors (IRFs) in virus-mediated signaling and regulation of cell growth. Biochimie 80: 651-658. https://doi.org/10.1016/S0300-9084(99)80018-2
59. Rieder M, Brzózka K, Pfaller CK, Cox JH, Stitz L, Conzelmann K-K. 2011. Genetic dissection of interferon-antagonistic functions of rabies virus phosphoprotein: inhibition of interferon regulatory factor 3 activation is important for pathogenicity. J Virol 85:842-852. https://doi.org/10.1128/JVI.01427-10
60. Papanastassiou V, Rampling R, Fraser M, Petty R, Hadley D, Nicoll J, Harland J, Mabbs R, Brown M. 2002. The potential for efficacy of the modified (ICP 34.5(-)) herpes simplex virus HSV1716 following intratumoural injection into human malignant glioma: a proof of principle study. Gene Ther 9:398-406. https://doi.org/10.1038/sj.gt.3301664
61. Friedman GK, Nan L, Haas MC, Kelly VM, Moore BP, Langford CP, Xu H, Han X, Beierle EA, Markert JM, Cassady KA, Gillespie GY. 2015. γ134.5-deleted HSV-1-expressing human cytomegalovirus IRS1 gene kills human glioblastoma cells as efficiently as wild-type HSV-1 in normoxia or hypoxia. Gene Ther 22:348-355. https://doi.org/10.1038/gt.2014.107
62. Guffey MB, Parker JN, Luckett WS, Gillespie GY, Meleth S, Whitley RJ, Markert JM. 2007. Engineered herpes simplex virus expressing bacterial cytosine deaminase for experimental therapy of brain tumors. Cancer Gene Ther 14:45-56. https://doi.org/10.1038/sj.cgt.7700978
63. 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. https://doi.org/10.1128/JVI.01462-14
64. Alexander DE, Ward SL, Mizushima N, Levine B, Leib DA. 2007. Analysis of the role of autophagy in replication of herpes simplex virus in cell culture. J Virol 81:12128-12134. https://doi.org/10.1128/JVI.01356-07
65. Brown SM, Ritchie DA, Subak-Sharpe JH. 1973. Genetic studies with herpes simplex virus type 1. The isolation of temperature-sensitive mutants, their arrangement into complementation groups and recombination analysis leading to a linkage map. J Gen Virol 18:329-346
66. Ko J-K, Ma J. 2005. A rapid and efficient PCR-based mutagenesis method applicable to cell physiology study. Am J Physiol Cell Physiol 288: C1273-C1278. https://doi.org/10.1152/ajpcell.00517.2004
67. Stow ND, Stow EC. 1986. Isolation and characterization of a herpes simplex virus type 1 mutant containing a deletion within the gene encoding the immediate early polypeptide Vmw110. J Gen Virol 67: 2571-2585. https://doi.org/10.1099/0022-1317-67-12-2571
68. McCarthy AM, McMahan L, Schaffer PA. 1989. Herpes simplex virus type 1 ICP27 deletion mutants exhibit altered patterns of transcription and are DNA deficient. J Virol 63:18-27
69. Francoeur AM, Poliquin L, Stanners CP. 1987. The isolation of interferoninducing mutants of vesicular stomatitis virus with altered viral P function for the inhibition of total protein synthesis. Virology 160:236-245. https://doi.org/10.1016/0042-6822(87)90065-1
70. Miyazaki J, Takaki S, Araki K, Tashiro F, Tominaga A, Takatsu K, Yamamura K. 1989. Expression vector system based on the chicken beta-actin promoter directs efficient production of interleukin-5. Gene 79:269-277. https://doi.org/10.1016/0378-1119(89)90209-6
71. Niwa H, Yamamura K, Miyazaki J. 1991. Efficient selection for highexpression transfectants with a novel eukaryotic vector. Gene 108: 193-199. https://doi.org/10.1016/0378-1119(91)90434-D
72. Prins KC, Cárdenas WB, Basler CF. 2009. Ebola virus protein VP35 impairs the function of interferon regulatory factor-activating kinases IKKepsilon and TBK-1. J Virol 83:3069-3077. https://doi.org/10.1128/JVI.01875-08
73. Rader KA, Ackland-Berglund CE, Miller JK, Pepose JS, Leib DA. 1993. In vivo characterization of site-directed mutations in the promoter of the herpes simplex virus type 1 latency-associated transcripts. J Gen Virol 74:1859-1869. https://doi.org/10.1099/0022-1317-74-9-1859
74. Menachery VD, Pasieka TJ, Leib DA. 2010. Interferon regulatory factor 3-dependent pathways are critical for control of herpes simplex virus type 1 central nervous system infection. J Virol 84:9685-9694. https://doi.org/10.1128/JVI.00706-10
75. Mulvey M, Poppers J, Sternberg D, Mohr I. 2003. Regulation of eIF2alpha phosphorylation by different functions that act during discrete phases in the herpes simplex virus type 1 life cycle. J Virol 77:10917-10928. https://doi.org/10.1128/JVI.77.20.10917-10928.2003
76. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675. https://doi.org/10.1038/nmeth.2089
77. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A. 2012. Fiji: an opensource platform for biological-image analysis. Nat Methods 9:676-682. https://doi.org/10.1038/nmeth.2019