SIV-induced terminally differentiated adaptive NK cells in lymph nodes associated with enhanced MHC-E restricted activity.
Algorithms
Animals
CD4-Positive T-Lymphocytes
/ cytology
Cell Differentiation
/ genetics
Chlorocebus aethiops
Female
Flow Cytometry
Fluorescent Antibody Technique
Humans
K562 Cells
Killer Cells, Natural
/ cytology
Lymph Nodes
/ metabolism
Lymphoid Tissue
/ cytology
Macaca
Male
NK Cell Lectin-Like Receptor Subfamily C
/ metabolism
Simian Acquired Immunodeficiency Syndrome
/ immunology
Simian Immunodeficiency Virus
/ immunology
Transcriptome
/ genetics
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
24 02 2021
24 02 2021
Historique:
received:
27
08
2020
accepted:
27
01
2021
entrez:
25
2
2021
pubmed:
26
2
2021
medline:
4
3
2021
Statut:
epublish
Résumé
Natural killer (NK) cells play a critical understudied role during HIV infection in tissues. In a natural host of SIV, the African green monkey (AGM), NK cells mediate a strong control of SIVagm infection in secondary lymphoid tissues. We demonstrate that SIVagm infection induces the expansion of terminally differentiated NKG2a
Identifiants
pubmed: 33627642
doi: 10.1038/s41467-021-21402-1
pii: 10.1038/s41467-021-21402-1
pmc: PMC7904927
doi:
Substances chimiques
Klrc2 protein, mouse
0
NK Cell Lectin-Like Receptor Subfamily C
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1282Subventions
Organisme : NIH HHS
ID : P51 OD011132
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI116379
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI143457
Pays : United States
Organisme : NIH HHS
ID : U42 OD011023
Pays : United States
Références
Martin, M. P. & Carrington, M. Immunogenetics of HIV disease. Immunol. Rev. 254, 245–264 (2013).
pubmed: 23772624
pmcid: 3703621
doi: 10.1111/imr.12071
Alter, G. & Altfeld, M. NK cells in HIV-1 infection: Evidence for their role in the control of HIV-1 infection. J. Intern. Med. 265, 29–42 (2009).
pubmed: 19093958
pmcid: 2842208
doi: 10.1111/j.1365-2796.2008.02045.x
Goulder, P. J. R. & Watkins, D. I. Impact of MHC class I diversity on immune control of immunodeficiency virus replication. Nat. Rev. Immunol. 8, 619–630 (2008).
pubmed: 18617886
pmcid: 2963026
doi: 10.1038/nri2357
Freud, A. G., Mundy-Bosse, B. L., Yu, J. & Caligiuri, M. A. The broad spectrum of human natural killer cell diversity. Immunity 47, 820–833 (2017).
pubmed: 29166586
pmcid: 5728700
doi: 10.1016/j.immuni.2017.10.008
Goodridge, J. P., Önfelt, B. & Malmberg, K.-J. Newtonian cell interactions shape natural killer cell education. Immunol. Rev. 267, 197–213 (2015).
pubmed: 26284479
pmcid: 4832384
doi: 10.1111/imr.12325
Blish, C. A. Natural killer cell diversity in viral infection: why and how much? Pathog. Immun. 1, 165–192 (2016).
pubmed: 27635417
pmcid: 5021221
doi: 10.20411/pai.v1i1.142
Strauss-Albee, D. M. et al. Human NK cell repertoire diversity reflects immune experience and correlates with viral susceptibility. Sci. Transl. Med. 7, 297ra115 (2015).
pubmed: 26203083
pmcid: 4547537
doi: 10.1126/scitranslmed.aac5722
Palgen, J.-L. et al. NK cell immune responses differ after prime and boost vaccination. J. Leukoc. Biol. 105, 1055–1073 (2019).
pubmed: 30794328
doi: 10.1002/JLB.4A1018-391RR
Reeves, R. K. et al. Antigen-specific NK cell memory in rhesus macaques. Nat. Immunol. 16, 927–932 (2015).
pubmed: 26193080
pmcid: 4545390
doi: 10.1038/ni.3227
Paust, S., Senman, B. & von Andrian, U. H. Adaptive immune responses mediated by natural killer cells. Immunol. Rev. 235, 286–296 (2010).
pubmed: 20536570
pmcid: 2911633
doi: 10.1111/j.0105-2896.2010.00906.x
Peng, H. & Tian, Z. Natural killer cell memory: progress and implications. Front. Immunol. 8, 1143 (2017).
pubmed: 28955346
pmcid: 5601391
doi: 10.3389/fimmu.2017.01143
Lucar, O., Reeves, R. K. & Jost, S. A natural impact: NK cells at the intersection of cancer and HIV disease. Front. Immunol. 10, 1850 (2019).
Luteijn, R. et al. Early viral replication in lymph nodes provides HIV with a means by which to escape NK-cell-mediated control. Eur. J. Immunol. 41, 2729–2740 (2011).
pubmed: 21630248
doi: 10.1002/eji.201040886
pmcid: 8943700
Schafer, J. L., Li, H., Evans, T. I., Estes, J. D. & Reeves, R. K. Accumulation of cytotoxic CD16+ NK cells in simian immunodeficiency virus-infected lymph nodes associated with in situ differentiation and functional anergy. J. Virol. 89, 6887–6894 (2015).
pubmed: 25903330
pmcid: 4468491
doi: 10.1128/JVI.00660-15
Freud, A. G. et al. A human CD34(+) subset resides in lymph nodes and differentiates into CD56bright natural killer cells. Immunity 22, 295–304 (2005).
pubmed: 15780987
doi: 10.1016/j.immuni.2005.01.013
Svardal, H. et al. Ancient hybridization and strong adaptation to viruses across African vervet monkey populations. Nat. Genet. 49, 1705–1713 (2017).
pubmed: 29083404
pmcid: 5709169
doi: 10.1038/ng.3980
Müller, M. C. et al. Simian immunodeficiency viruses from central and western Africa: evidence for a new species-specific lentivirus in tantalus monkeys. J. Virol. 67, 1227–1235 (1993).
pubmed: 8437214
pmcid: 237488
doi: 10.1128/jvi.67.3.1227-1235.1993
Raehtz, K., Pandrea, I. & Apetrei, C. The well-tempered SIV infection: pathogenesis of SIV infection in natural hosts in the wild, with emphasis on virus transmission and early events post-infection that may contribute to protection from disease progression. Infect. Genet. Evol. 46, 308–323 (2016).
pubmed: 27394696
pmcid: 5360191
doi: 10.1016/j.meegid.2016.07.006
Sodora, D. L. et al. Toward an AIDS vaccine: lessons from natural simian immunodeficiency virus infections of African nonhuman primate hosts. Nat. Med. 15, 861–865 (2009).
pubmed: 19661993
pmcid: 2782707
doi: 10.1038/nm.2013
Huot, N. et al. Natural killer cells migrate into and control simian immunodeficiency virus replication in lymph node follicles in African green monkeys. Nat. Med. 23, 1277–1286 (2017).
pubmed: 29035370
pmcid: 6362838
doi: 10.1038/nm.4421
Hong, J. J., Chang, K.-T. & Villinger, F. The dynamics of T and B cells in lymph node during chronic HIV infection: TFH and HIV, unhappy dance partners? Front. Immunol. 7, 522 (2016).
Wong, J. K. & Yukl, S. A. Tissue reservoirs of HIV. Curr. Opin. HIV AIDS 11, 362–370 (2016).
pubmed: 27259045
Strauss-Albee, D. M., Horowitz, A., Parham, P. & Blish, C. A. Coordinated regulation of NK receptor expression in the maturing human immune system. J. Immunol. 193, 4871–4879 (2014).
pubmed: 25288567
doi: 10.4049/jimmunol.1401821
Horowitz, A. et al. Genetic and environmental determinants of human NK cell diversity revealed by mass cytometry. Sci. Transl. Med. 5, 208ra145 (2013).
pubmed: 24154599
pmcid: 3918221
doi: 10.1126/scitranslmed.3006702
Victor, A. R. et al. Epigenetic and post-transcriptional regulation of CD16 expression during human natural killer cell development. J. Immunol. 200, 565–572 (2018).
pubmed: 29229679
doi: 10.4049/jimmunol.1701128
Sivori, S. et al. TLR/NCR/KIR: which one to use and when? Front. Immunol. 5, 105 (2014).
pubmed: 24678311
pmcid: 3958761
doi: 10.3389/fimmu.2014.00105
Jeevan-Raj, B. et al. The transcription factor Tcf1 contributes to normal NK cell development and function by limiting the expression of granzymes. Cell Rep. 20, 613–626 (2017).
pubmed: 28723565
doi: 10.1016/j.celrep.2017.06.071
Goh, W. & Huntington, N. D. Regulation of murine natural killer cell development. Front. Immunol. 8, 130 (2017).
Béziat, V., Descours, B., Parizot, C., Debré, P. & Vieillard, V. NK cell terminal differentiation: correlated stepwise decrease of NKG2A and acquisition of KIRs. PLoS ONE 5, e11966 (2010).
Luetke-Eversloh, M., Killig, M. & Romagnani, C. Signatures of human NK cell development and terminal differentiation. Front. Immunol. 4, 499 (2013).
pubmed: 24416035
pmcid: 3874559
doi: 10.3389/fimmu.2013.00499
Freud, A. G., Yu, J. & Caligiuri, M. A. Human natural killer cell development in secondary lymphoid tissues. Semin. Immunol. 26, 132–137 (2014).
pubmed: 24661538
pmcid: 4010312
doi: 10.1016/j.smim.2014.02.008
O’Sullivan, T. E., Johnson, L. R., Kang, H. H. & Sun, J. C. BNIP3- and BNIP3L-mediated mitophagy promotes the generation of natural killer cell memory. Immunity 43, 331–342 (2015).
pubmed: 26253785
pmcid: 5737626
doi: 10.1016/j.immuni.2015.07.012
Evavold, C. L. & Kagan, J. C. How Inflammasomes Inform Adaptive Immunity. J. Mol. Biol. 430, 217–237 (2018).
pubmed: 28987733
doi: 10.1016/j.jmb.2017.09.019
van den Boorn, J. G. et al. Inflammasome-dependent induction of adaptive NK cell memory. Immunity 44, 1406–1421 (2016).
pubmed: 27287410
doi: 10.1016/j.immuni.2016.05.008
Paust, S., Blish, C. A. & Reeves, R. K. Redefining memory: building the case for adaptive NK cells. J. Virol. 91, e00169-17 (2017).
Cichocki, F., Miller, J. S., Anderson, S. K. & Bryceson, Y. T. Epigenetic regulation of NK cell differentiation and effector functions. Front. Immunol. 4, 55 (2013).
Tesi, B., Schlums, H., Cichocki, F. & Bryceson, Y. T. Epigenetic regulation of adaptive NK cell diversification. Trends Immunol. 37, 451–461 (2016).
pubmed: 27160662
doi: 10.1016/j.it.2016.04.006
Wagner, J. A. & Fehniger, T. A. Human adaptive natural killer cells: beyond NKG2C. Trends Immunol. 37, 351–353 (2016).
pubmed: 27179621
pmcid: 4885776
doi: 10.1016/j.it.2016.05.001
Anfossi, N. et al. Human NK cell education by inhibitory receptors for MHC class I. Immunity 25, 331–342 (2006).
pubmed: 16901727
doi: 10.1016/j.immuni.2006.06.013
Zhang, X., Feng, J., Chen, S., Yang, H. & Dong, Z. Synergized regulation of NK cell education by NKG2A and specific Ly49 family members. Nat. Commun. 10, 1–12 (2019).
He, Y. & Tian, Z. NK cell education via nonclassical MHC and non-MHC ligands. Cell. Mol. Immunol. 14, 321–330 (2017).
pubmed: 27264685
doi: 10.1038/cmi.2016.26
Braud, V. M., Allan, D. S. J., Wilson, D. & McMichael, A. J. TAP- and tapasin-dependent HLA-E surface expression correlates with the binding of an MHC class I leader peptide. Curr. Biol. 8, 1–10 (1998).
pubmed: 9427624
doi: 10.1016/S0960-9822(98)70014-4
Michaëlsson, J. et al. A signal peptide derived from hsp60 binds HLA-E and interferes with CD94/NKG2A recognition. J. Exp. Med. 196, 1403–1414 (2002).
pubmed: 12461076
pmcid: 2194258
doi: 10.1084/jem.20020797
Pietra, G. et al. HLA-E-restricted recognition of cytomegalovirus-derived peptides by human CD8+ cytolytic T lymphocytes. Proc. Natl Acad. Sci. USA 100, 10896–10901 (2003).
pubmed: 12960383
doi: 10.1073/pnas.1834449100
pmcid: 196899
Schulte, D. et al. The HLA-E(R)/HLA-E(R) genotype affects the natural course of hepatitis C virus (HCV) infection and is associated with HLA-E-restricted recognition of an HCV-derived peptide by interferon-gamma-secreting human CD8(+) T cells. J. Infect. Dis. 200, 1397–1401 (2009).
pubmed: 19780673
doi: 10.1086/605889
Rölle, A., Jäger, D. & Momburg, F. HLA-E peptide repertoire and dimorphism—centerpieces in the adaptive NK cell puzzle? Front. Immunol. 9, 2410 (2018).
Walters, L. C. et al. Pathogen-derived HLA-E bound epitopes reveal broad primary anchor pocket tolerability and conformationally malleable peptide binding. Nat. Commun. 9, 3137 (2018).
pubmed: 30087334
pmcid: 6081459
doi: 10.1038/s41467-018-05459-z
Hansen, S. G. et al. Broadly targeted CD8+ T cell responses restricted by major histocompatibility complex E. Science 351, 714–720 (2016).
pubmed: 26797147
pmcid: 4769032
doi: 10.1126/science.aac9475
Asmal, M. et al. A signature in HIV-1 envelope leader peptide associated with transition from acute to chronic infection impacts envelope processing and infectivity. PLoS ONE 6, e23673 (2011).
da Silva, J. X. et al. Sequence variations of Env signal peptide alleles in different clinical stages of HIV infection. Peptides 32, 1800–1806 (2011).
pubmed: 21816188
doi: 10.1016/j.peptides.2011.07.014
Yolitz, J. et al. Signal peptide of HIV envelope protein impacts glycosylation and antigenicity of gp120. Proc. Natl Acad. Sci. USA 115, 2443–2448 (2018).
pubmed: 29463753
doi: 10.1073/pnas.1722627115
pmcid: 5877976
Huot, N., Bosinger, S. E., Paiardini, M., Reeves, R. K. & Müller-Trutwin, M. Lymph node cellular and viral dynamics in natural hosts and impact for HIV cure strategies. Front. Immunol. 9, 780 (2018).
pubmed: 29725327
pmcid: 5916971
doi: 10.3389/fimmu.2018.00780
Jacquelin, B. et al. Innate immune responses and rapid control of inflammation in african green monkeys treated or not with interferon-alpha during primary SIVagm infection. PLoS Pathog. 10, e1004241 (2014).
Schlums, H. et al. Cytomegalovirus infection drives adaptive epigenetic diversification of NK cells with altered signaling and effector function. Immunity 42, 443–456 (2015).
pubmed: 25786176
pmcid: 4612277
doi: 10.1016/j.immuni.2015.02.008
Cichicki, F. et al. Diversification and functional specialization of human NK cell subsets. Curr. Top. Microbiol. Immunol. 395, 63–94 (2016).
pubmed: 26472216
Wilk, A. J. & Blish, C. A. Diversification of human NK cells: Lessons from deep profiling. J. Leukoc. Biol. 103, 629–641 (2018).
pubmed: 29350874
doi: 10.1002/JLB.6RI0917-390R
Romee, R. et al. NK cell CD16 surface expression and function is regulated by a disintegrin and metalloprotease-17 (ADAM17). Blood 121, 3599–3608 (2013).
pubmed: 23487023
pmcid: 3643761
doi: 10.1182/blood-2012-04-425397
Kristensen, A. B., Kent, S. J. & Parsons, M. S. Contribution of NK cell education to both direct and anti-HIV-1 antibody-dependent NK cell functions. J. Virol. 92, e02146-17 (2018).
Rasid, O. et al. H3K4me1 supports memory-like NK cells induced by systemic inflammation. Cell Rep. 29, 3933–3945.e3 (2019).
pubmed: 31851924
doi: 10.1016/j.celrep.2019.11.043
Wu, Y., Tian, Z. & Wei, H. Developmental and functional control of natural killer cells by cytokines. Front. Immunol. 8, 930 (2017).
Wang, Y. et al. HIV-1-induced cytokines deplete homeostatic innate lymphoid cells and expand TCF7-dependent memory NK cells. Nat. Immunol. 21, 274–286 (2020).
pubmed: 32066947
pmcid: 7044076
doi: 10.1038/s41590-020-0593-9
Yang, I. et al. Modulation of major histocompatibility complex Class I molecules and major histocompatibility complex-bound immunogenic peptides induced by interferon-alpha and interferon-gamma treatment of human glioblastoma multiforme. J. Neurosurg. 100, 310–319 (2004).
pubmed: 15086239
doi: 10.3171/jns.2004.100.2.0310
Zhou, F. Molecular mechanisms of IFN-γ to up-regulate MHC class I antigen processing and presentation. Int. Rev. Immunol. 28, 239–260 (2009).
pubmed: 19811323
doi: 10.1080/08830180902978120
Kornfeld, C. et al. Antiinflammatory profiles during primary SIV infection in African green monkeys are associated with protection against AIDS. J. Clin. Invest. 115, 1389–1389 (2005).
pmcid: 1087160
Nguyen, S. et al. HLA-E upregulation on IFN-γ-activated AML blasts impairs CD94/NKG2A-dependent NK cytolysis after haplo-mismatched hematopoietic SCT. Bone Marrow Transplant. 43, 693–699 (2009).
pubmed: 19011664
doi: 10.1038/bmt.2008.380
Ploquin, M. J.-Y. et al. Distinct expression profiles of TGF-β1 signaling mediators in pathogenic SIVmac and non-pathogenic SIVagm infections. Retrovirology 3, 37 (2006).
pubmed: 16800882
pmcid: 1533859
doi: 10.1186/1742-4690-3-37
Ramsuran, V. et al. Elevated HLA-A expression impairs HIV control through inhibition of NKG2A-expressing cells. Science 359, 86–90 (2018).
pubmed: 29302013
pmcid: 5933048
doi: 10.1126/science.aam8825
Miller, J. D. et al. Analysis of HLA-E peptide-binding specificity and contact residues in bound peptide required for recognition by CD94/NKG2. J. Immunol. 171, 1369–1375 (2003).
pubmed: 12874227
doi: 10.4049/jimmunol.171.3.1369
Celik, A. A., Kraemer, T., Huyton, T., Blasczyk, R. & Bade-Döding, C. The diversity of the HLA-E-restricted peptide repertoire explains the immunological impact of the Arg107Gly mismatch. Immunogenetics 68, 29–41 (2016).
pubmed: 26552660
doi: 10.1007/s00251-015-0880-z
Hannoun, Z. et al. Identification of novel HIV-1-derived HLA-E-binding peptides. Immunol. Lett. 202, 65–72 (2018).
pubmed: 30172717
pmcid: 6291738
doi: 10.1016/j.imlet.2018.08.005
Joosten, S. A., Sullivan, L. C. & Ottenhoff, T. H. M. Characteristics of HLA-E restricted T-cell responses and their role in infectious diseases. J. Immunol. Res. 2016, 2695396 (2016).
Hammer, Q. et al. Peptide-specific recognition of human cytomegalovirus strains controls adaptive natural killer cells. Nat. Immunol. 19, 453–463 (2018).
pubmed: 29632329
doi: 10.1038/s41590-018-0082-6
Malmberg, K.-J., Beziat, V. & Ljunggren, H.-G. Spotlight on NKG2C and the human NK-cell response to CMV infection. Eur. J. Immunol. 42, 3141–3145 (2012).
pubmed: 23255011
doi: 10.1002/eji.201243050
Pupuleku, A. et al. Elusive role of the CD94/NKG2C NK cell receptor in the response to cytomegalovirus: novel experimental observations in a reporter cell system. Front. Immunol. 8, 1317 (2017).
Béziat, V. et al. CMV drives clonal expansion of NKG2C+ NK cells expressing self-specific KIRs in chronic hepatitis patients. Eur. J. Immunol. 42, 447–457 (2012).
pubmed: 22105371
doi: 10.1002/eji.201141826
Brockmeyer, C. et al. T cell receptor (TCR)-induced tyrosine phosphorylation dynamics identifies THEMIS as a new TCR signalosome component. J. Biol. Chem. 286, 7535–7547 (2011).
pubmed: 21189249
doi: 10.1074/jbc.M110.201236
Paster, W. et al. GRB2-mediated recruitment of THEMIS to LAT is essential for thymocyte development. J. Immunol. 190, 3749–3756 (2013).
pubmed: 23460737
pmcid: 3607403
doi: 10.4049/jimmunol.1203389
Choi, S. et al. THEMIS enhances TCR signaling and enables positive selection by selective inhibition of SHP-1. Nat. Immunol. 18, 433–441 (2017).
pubmed: 28250424
pmcid: 5807080
doi: 10.1038/ni.3692
Daskalaki, M. et al. Long-term efficient control of SIV infection in macaques is associated with an intact intestinal barrier. J. Med. Primatol. 46, 144–148 (2017).
pubmed: 28748664
doi: 10.1111/jmp.12294
Ram, D. R. et al. Tracking KLRC2 (NKG2C)+ memory-like NK cells in SIV+ and rhCMV+ rhesus macaques. PLoS Pathog. 14, e1007104 (2018).
pubmed: 29851983
pmcid: 5997355
doi: 10.1371/journal.ppat.1007104
Jacquelin, B. et al. Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response. J. Clin. Invest. 119, 3544–3555 (2009).
pubmed: 19959873
pmcid: 2786805
Mussil, B., Sauermann, U., Motzkus, D., Stahl-Hennig, C. & Sopper, S. Increased APOBEC3G and APOBEC3F expression is associated with low viral load and prolonged survival in simian immunodeficiency virus infected rhesus monkeys. Retrovirology 8, 77 (2011).
pubmed: 21955401
pmcid: 3192745
doi: 10.1186/1742-4690-8-77
Gnanadurai, C. W. et al. Genetic identity and biological phenotype of a transmitted/founder virus representative of nonpathogenic simian immunodeficiency virus infection in african green monkeys. J. Virol. 84, 12245–12254 (2010).
pubmed: 20881048
pmcid: 2976391
doi: 10.1128/JVI.01603-10
Diop, O. M. et al. High levels of viral replication during primary simian immunodeficiency virus SIVagm infection are rapidly and strongly controlled in African green monkeys. J. Virol. 74, 7538–7547 (2000).
pubmed: 10906207
pmcid: 112274
doi: 10.1128/JVI.74.16.7538-7547.2000
Nielsen, M. et al. Reliable prediction of T-cell epitopes using neural networks with novel sequence representations. Protein Sci. Publ. Protein Soc. 12, 1007–1017 (2003).
doi: 10.1110/ps.0239403
Lundegaard, C., Lund, O. & Nielsen, M. Accurate approximation method for prediction of class I MHC affinities for peptides of length 8, 10 and 11 using prediction tools trained on 9mers. Bioinformatics 24, 1397–1398 (2008).
pubmed: 18413329
doi: 10.1093/bioinformatics/btn128
Wu, H. L. et al. The role of MHC-E in T cell immunity is conserved among humans, rhesus macaques, and cynomolgus macaques. J. Immunol. 200, 49–60 (2018).
pubmed: 29150562
doi: 10.4049/jimmunol.1700841
Alter, G., Malenfant, J. M. & Altfeld, M. CD107a as a functional marker for the identification of natural killer cell activity. J Immunol Methods. 294, 15–22 https://doi.org/10.1016/j.jim.2004.08.008 (2004). PMID: 15604012.
doi: 10.1016/j.jim.2004.08.008
pubmed: 15604012
Aktas, E., Kucuksezer, U. C., Bilgic, S., Erten, G. & Deniz, G. Relationship between CD107a expression and cytotoxic activity. Cell Immunol. 254, 149–154 https://doi.org/10.1016/j.cellimm.2008.08.007 (2009). Epub 2008 Oct 5. PMID: 18835598.
doi: 10.1016/j.cellimm.2008.08.007
pubmed: 18835598
Webb, B. & Sali, A. Protein structure modeling with MODELLER. Methods Mol. Biol. 1137, 1–15 (2014).
pubmed: 24573470
doi: 10.1007/978-1-4939-0366-5_1
Ashkenazy, H. et al. ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules. Nucleic Acids Res. 44, W344–W350 (2016).
pubmed: 27166375
pmcid: 4987940
doi: 10.1093/nar/gkw408
Cokelaer, T., Desvillechabrol, D., Legendre, R. & Cardon, M. ‘Sequana’: a Set of Snakemake NGS pipelines. J. Open Source Softw. 2, 352 (2017).
doi: 10.21105/joss.00352
Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
pubmed: 24227677
doi: 10.1093/bioinformatics/btt656
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281
pmcid: 4302049
doi: 10.1186/s13059-014-0550-8
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 57, 289–300 (1995).
Bindea, G. et al. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25, 1091–1093 (2009).
pubmed: 19237447
pmcid: 2666812
doi: 10.1093/bioinformatics/btp101