Volume 14 Issue 4
Apr.  2024
Turn off MathJax
Article Contents
Article Navigation >  Journal of Pharmaceutical Analysis  > 2024  >  14(4): 100905
Nian-nian Li, Deng-xing Lun, Ningning Gong, Gang Meng, Xin-ying Du, He Wang, Xiangxiang Bao, Xin-yang Li, Ji-wu Song, Kewei Hu, Lala Li, Si-ying Li, Wenbo Liu, Wanping Zhu, Yunlong Zhang, Jikai Li, Ting Yao, Leming Mou, Xiaoqing Han, Furong Hao, Yongcheng Hu, Lin Liu, Hongguang Zhu, Yuyun Wu, Bin Liu. Targeting the chromatin structural changes of antitumor immunity[J]. Journal of Pharmaceutical Analysis, 2024, 14(4): 100905. doi: 10.1016/j.jpha.2023.11.012
Citation: Nian-nian Li, Deng-xing Lun, Ningning Gong, Gang Meng, Xin-ying Du, He Wang, Xiangxiang Bao, Xin-yang Li, Ji-wu Song, Kewei Hu, Lala Li, Si-ying Li, Wenbo Liu, Wanping Zhu, Yunlong Zhang, Jikai Li, Ting Yao, Leming Mou, Xiaoqing Han, Furong Hao, Yongcheng Hu, Lin Liu, Hongguang Zhu, Yuyun Wu, Bin Liu. Targeting the chromatin structural changes of antitumor immunity[J]. Journal of Pharmaceutical Analysis, 2024, 14(4): 100905. doi: 10.1016/j.jpha.2023.11.012
shu

Targeting the chromatin structural changes of antitumor immunity

doi: 10.1016/j.jpha.2023.11.012

  • a. Weifang People's Hospital, Weifang, Shandong, 261000, China;

  • b. School of Life Sciences, Nankai University, Tianjin, 300071, China;

  • c. Weifang Traditional Chinese Medicine Hospital, Weifang, Shandong, 261000, China;

  • d. Shaanxi Key Laboratory of Sericulture, Ankang University, Ankang, Shaanxi, 725000, China;

  • e. Guizhou Education University, Guiyang, 550018, China;

  • f. Guizhou Normal University, Guiyang, 550025, China;

  • g. School of Medical Imaging, Weifang Medical University, Weifang, Shandong, 261053, China;

  • h. Department of Bone and Soft Tissue Oncology, Tianjin Hospital, Tianjin, 300299, China;

  • j. Xinqiao Hospital of Army Military Medical University, Chongqing, 400038, China;

  • k. Teda Institute of Biological Sciences & Biotechnology, Nankai University, Tianjin, 300457, China

Funds:

This study was supported by the Startup Foundation for Junior Faculty, Nankai University (Grant No.: 63191439), the National Natural Science Foundation of China (Grant Nos.: 32100418 and 3210040345), The Health Commission Foundation of China (Grant No.: 2018ZX10712001-017) and the Chongqing Medical College Natural Fund (Grant Nos.: ygz2019302 and ygz2019305).

  • Received Date: Jun. 16, 2023
  • Accepted Date: Nov. 21, 2023
  • Rev Recd Date: Sep. 28, 2023
  • Publish Date: Nov. 29, 2023
    Abstract
  • Epigenomic imbalance drives abnormal transcriptional processes, promoting the onset and progression of cancer. Although defective gene regulation generally affects carcinogenesis and tumor suppression networks, tumor immunogenicity and immune cells involved in antitumor responses may also be affected by epigenomic changes, which may have significant implications for the development and application of epigenetic therapy, cancer immunotherapy, and their combinations. Herein, we focus on the impact of epigenetic regulation on tumor immune cell function and the role of key abnormal epigenetic processes, DNA methylation, histone post-translational modification, and chromatin structure in tumor immunogenicity, and introduce these epigenetic research methods. We emphasize the value of small-molecule inhibitors of epigenetic modulators in enhancing antitumor immune responses and discuss the challenges of developing treatment plans that combine epigenetic therapy and immunotherapy through the complex interaction between cancer epigenetics and cancer immunology.
    • FullText(HTML)
  • loading
    • References(277)
  • [1]
    G. Villani, Coupling between hydrogen atoms transfer and stacking interaction in adenine-thymine/guanine-cytosine complexes: a theoretical study, J. Phys. Chem. B 118 (2014) 5439-5452.
    [2]
    D. Pruss, B. Bartholomew, J. Persinger, et al., An asymmetric model for the nucleosome: a binding site for linker histones inside the DNA gyres, Science 274 (1996) 614-617.
    [3]
    X. Bai, C.C. Wong, Y. Pan, et al., Loss of YTHDF1 in gastric tumors restores sensitivity to antitumor immunity by recruiting mature dendritic cells, J. Immunother. Cancer 10 (2022), e003663.
    [4]
    T. Baubec, D.F. Colombo, C. Wirbelauer, et al., Genomic profiling of DNA methyltransferases reveals a role for DNMT3B in genic methylation, Nature 520 (2015) 243-247.
    [5]
    P. Mews, G. Egervari, R. Nativio, et al., Alcohol metabolism contributes to brain histone acetylation, Nature 574 (2019) 717-721.
    [6]
    M. Vogelauer, J. Wu, N. Suka, et al., Global histone acetylation and deacetylation in yeast, Nature 408 (2000) 495-498.
    [7]
    S.C. Elgin, Chromatin structure, DNA structure, Nature 300 (1982) 402-403.
    [8]
    C.T. Law, L. Wei, F.H. Tsang, et al., HELLS regulates chromatin remodeling and epigenetic silencing of multiple tumor suppressor genes in human hepatocellular carcinoma, Hepatology 69 (2019) 2013-2030.
    [9]
    J. Nikolich-Zugich, The twilight of immunity: emerging concepts in aging of the immune system, Nat. Immunol. 19 (2018) 10-19.
    [10]
    D.J. Simpson, A.M. McNicol, D.C. Murray, et al., Molecular pathology shows p16 methylation in nonadenomatous pituitaries from patients with Cushing’s disease, Clin. Cancer Res. 10 (2004) 1780-1788.
    [11]
    D. Alonso-Curbelo, Y.J. Ho, C. Burdziak, et al., A gene-environment-induced epigenetic program initiates tumorigenesis, Nature 590 (2021) 642-648.
    [12]
    A.P. Feinberg, R. Ohlsson, S. Henikoff, The epigenetic progenitor origin of human cancer, Nat. Rev. Genet. 7 (2006) 21-33.
    [13]
    C.B. Yoo, P.A. Jones, Epigenetic therapy of cancer: past, present and future, Nat. Rev. Drug Discov. 5 (2006) 37-50.
    [14]
    Y. Cheng, C. He, M. Wang, et al., Targeting epigenetic regulators for cancer therapy: mechanisms and advances in clinical trials, Signal Transduct. Target. Ther. 4 (2019) 62.
    [15]
    F. Lyko, The DNA methyltransferase family: a versatile toolkit for epigenetic regulation, Nat. Rev. Genet. 19 (2018) 81-92.
    [16]
    C. Stresemann, F. Lyko, Modes of action of the DNA methyltransferase inhibitors azacytidine and decitabine, Int. J. Cancer 123 (2008) 8-13.
    [17]
    D. Meilinger, K. Fellinger, S. Bultmann, et al., Np95 interacts with de novo DNA methyltransferases, Dnmt3a and Dnmt3b, and mediates epigenetic silencing of the viral CMV promoter in embryonic stem cells, EMBO Rep. 10 (2009) 1259-1264.
    [18]
    H. Saadeh, R. Schulz, Protection of CpG islands against de novo DNA methylation during oogenesis is associated with the recognition site of E2f1 and E2f2, Epigenet. Chromatin 7 (2014) 26.
    [19]
    K.P. Terracina, L.J. Graham, K.K. Payne, et al., DNA methyltransferase inhibition increases efficacy of adoptive cellular immunotherapy of murine breast cancer, Cancer Immunol. Immunother. 65 (2016) 1061-1073.
    [20]
    M. Bruno, A. Flaus, C. Stockdale, et al., Histone H2A/H2B dimer exchange by ATP-dependent chromatin remodeling activities, Mol. Cell 12 (2003) 1599-1606.
    [21]
    J. Jordano, F. Montero, E. Palacian, Relaxation of chromatin structure upon removal of histones H2A and H2B, FEBS Lett. 172 (1984) 70-74.
    [22]
    S. Eden, T. Hashimshony, I. Keshet, et al., DNA methylation models histone acetylation, Nature 394 (1998) 842.
    [23]
    S.E. Bates, Epigenetic therapies for cancer, N. Engl. J. Med. 383 (2020) 650-663.
    [24]
    M.E. Torres-Padilla, D.E. Parfitt, T. Kouzarides, et al., Histone arginine methylation regulates pluripotency in the early mouse embryo, Nature 445 (2007) 214-218.
    [25]
    A.J. Bannister, T. Kouzarides, Reversing histone methylation, Nature 436 (2005) 1103-1106.
    [26]
    S.J. Nielsen, R. Schneider, U.M. Bauer, et al., Rb targets histone H3 methylation and HP1 to promoters, Nature 412 (2001) 561-565.
    [27]
    S. Aizawa, K. Teramoto, Y. Yamamuro, Histone deacetylase 9 as a negative regulator for choline acetyltransferase gene in NG108-15 neuronal cells, Neuroscience 205 (2012) 63-72.
    [28]
    P. Kumar, S. Tripathi, K.N. Pandey, Histone deacetylase inhibitors modulate the transcriptional regulation of guanylyl cyclase/natriuretic peptide receptor-a gene: interactive roles of modified histones, histone acetyltransferase, p300, AND Sp1, J. Biol. Chem. 289 (2014) 6991-7002.
    [29]
    A. Kaidi, S.P. Jackson, Retraction Note: KAT5 tyrosine phosphorylation couples chromatin sensing to ATM signalling, Nature 568 (2019) 576.
    [30]
    K. Park, P.E. Mera, T.C. Moore, et al., Unprecedented mechanism employed by the Salmonella enterica EutT ATP: Co(I)rrinoid adenosyltransferase precludes adenosylation of incomplete co(II)rrinoids, Angew. Chem. Int. Ed. Engl. 54 (2015) 7158-7161.
    [31]
    V. Flury, N. Reveron-Gomez, N. Alcaraz, et al., Recycling of modified H2A-H2B provides short-term memory of chromatin states, Cell 186 (2023) 1050-1065.e19.
    [32]
    G. Bartolomei, M. Leutert, M. Manzo, et al., Analysis of chromatin ADP-ribosylation at the genome-wide level and at specific loci by ADPr-ChAP, Mol. Cell 61 (2016) 474-485.
    [33]
    M.B. Chandrasekharan, F. Huang, Y.C. Chen, et al., Histone H2B C-terminal helix mediates trans-histone H3K4 methylation independent of H2B ubiquitination, Mol. Cell. Biol. 30 (2010) 3216-3232.
    [34]
    H.D. Ou, S. Phan, T.J. Deerinck, et al., ChromEMT: Visualizing 3D chromatin structure and compaction in interphase and mitotic cells, Science 357 (2017), eaag0025.
    [35]
    V. Pancaldi, E. Carrillo-de-Santa-Pau, B.M. Javierre, et al., Integrating epigenomic data and 3D genomic structure with a new measure of chromatin assortativity, Genome Biol. 17 (2016) 152.
    [36]
    R.D. Acemel, J.J. Tena, I. Irastorza-Azcarate, et al., A single three-dimensional chromatin compartment in amphioxus indicates a stepwise evolution of vertebrate Hox bimodal regulation, Nat. Genet. 48 (2016) 336-341.
    [37]
    O. Delaneau, M. Zazhytska, C. Borel, et al., Chromatin three-dimensional interactions mediate genetic effects on gene expression, Science 364 (2019), eaat8266.
    [38]
    J.A. Meinel, V. Yumiceba, A. Kunstner, et al., Disruption of the topologically associated domain at Xp21.2 is related to 46,XY gonadal dysgenesis, J. Med. Genet. (2022) 469-476.
    [39]
    R.N. Ramirez, K. Chowdhary, J. Leon, et al., FoxP3 associates with enhancer-promoter loops to regulate T(reg)-specific gene expression, Sci. Immunol. 7 (2022), eabj9836.
    [40]
    E.W. Goodpasture, Immunity to virus diseases, Am. J. Public Heath. Nation’s Heath. 26 (1936) 1163-1167.
    [41]
    A. Labani-Motlagh, M. Ashja-Mahdavi, A. Loskog, The tumor microenvironment: A milieu hindering and obstructing antitumor immune responses, Front. Immunol. 11 (2020) 940.
    [42]
    J.A. Joyce, D.T. Fearon, T cell exclusion, immune privilege, and the tumor microenvironment, Science 348 (2015) 74-80.
    [43]
    X. Chen, X. Pan, W. Zhang, et al., Epigenetic strategies synergize with PD-L1/PD-1 targeted cancer immunotherapies to enhance antitumor responses, Acta Pharm. Sin. B 10 (2020) 723-733.
    [44]
    R.V. Uzhachenko, A. Shanker, CD8+ T lymphocyte and NK cell network: Circuitry in the cytotoxic domain of immunity, Front. Immunol. 10 (2019) 1906.
    [45]
    M.G. Betjes, Clinical consequences of circulating CD28-negative T cells for solid organ transplantation, Transpl. Int. 29 (2016) 274-284.
    [46]
    E. Russo, A. Santoni, G. Bernardini, Tumor inhibition or tumor promotion? The duplicity of CXCR3 in cancer, J. Leukoc. Biol. 108 (2020) 673-685.
    [47]
    S. Magri, E. Masetto, S. Solito, et al., Correction to: Human MDSCs derived from the bone marrow maintain their functional ability but have a reduced frequency of induction in the elderly compared to pediatric donors, Immun. Ageing 17 (2020), 39.
    [48]
    J.G. Henderson, A. Opejin, A. Jones, et al., CD5 instructs extrathymic regulatory T cell development in response to self and tolerizing antigens, Immunity 42 (2015) 471-483.
    [49]
    L. Zhou, T. Mudianto, X. Ma, et al., Targeting EZH2 enhances antigen presentation, antitumor immunity, and circumvents anti-PD-1 resistance in head and neck cancer, Clin. Cancer Res. 26 (2020) 290-300.
    [50]
    C. Zhou, W.Y. Liu, F. Feng, et al., Determination and stress studies on YK-1101, a potential histone deacetylase, by HPLC-UV and HPLC-TOF/MS methods, J. Pharm. Anal. 3 (2013) 168-172.
    [51]
    M.P. Correia, A. Stojanovic, W.S. Wels, et al., Innate-like NKp30(+)CD8(+) T cells armed with TCR/CAR target tumor heterogeneity, Oncoimmunology 10 (2021), 1973783.
    [52]
    S. Liu, Z. Wang, D. Zhu, et al., Effect of Shengmai Yin on the DNA methylation status of nasopharyngeal carcinoma cell and its radioresistant strains, J. Pharm. Anal. 11 (2021) 783-790.
    [53]
    X. Gu, Y. Hua, J. Yu, et al., Epigenetic drug library screening reveals targeting DOT1L abrogates NAD(+) synthesis by reprogramming H3K79 methylation in uveal melanoma, J. Pharm. Anal. 13 (2023) 24-38.
    [54]
    Q. Liao, J. Yang, S. Ge, et al., Novel insights into histone lysine methyltransferases in cancer therapy: From epigenetic regulation to selective drugs, J. Pharm. Anal. 13 (2023) 127-141.
    [55]
    H.H. Cheung, T.L. Lee, A.J. Davis, et al., Genome-wide DNA methylation profiling reveals novel epigenetically regulated genes and non-coding RNAs in human testicular cancer, Br. J. Cancer 102 (2010) 419-427.
    [56]
    J. Manning, M. Indrova, B. Lubyova, et al., Induction of MHC class I molecule cell surface expression and epigenetic activation of antigen-processing machinery components in a murine model for human papilloma virus 16-associated tumours, Immunology 123 (2008) 218-227.
    [57]
    T. Ando, M. Nishimura, Y. Oka, Decitabine (5-Aza-2’-deoxycytidine) decreased DNA methylation and expression of MDR-1 gene in K562/ADM cells, Leukemia 14 (2000) 1915-1920.
    [58]
    A.D. Truax, M. Thakkar, S.F. Greer, Dysregulated recruitment of the histone methyltransferase EZH2 to the class II transactivator (CIITA) promoter IV in breast cancer cells, PLoS One 7 (2012), e36013.
    [59]
    S. Fulda, K.M. Debatin, 5-Aza-2’-deoxycytidine and IFN-gamma cooperate to sensitize for TRAIL-induced apoptosis by upregulating caspase-8, Oncogene 25 (2006) 5125-5133.
    [60]
    H.E. Bulut, O. Ozdemir, Y. Basimoglu-Koca, et al., Effects of a DNA demethylating agent: 5-azacytidine: On testicular morphology during mouse embryo development, Okajimas Folia Anat. Jpn 76 (1999) 47-53.
    [61]
    B. Jin, P. Zhang, H. Zou, et al., Verification of EZH2 as a druggable target in metastatic uveal melanoma, Mol. Cancer 19 (2020), 52.
    [62]
    B. Cruickshank, M. Giacomantonio, P. Marcato, et al., Dying to be noticed: Epigenetic regulation of immunogenic cell death for cancer immunotherapy, Front. Immunol. 9 (2018), 654.
    [63]
    M. Silasi, Y. You, S. Simpson, et al., Human chorionic gonadotropin modulates CXCL10 expression through histone methylation in human decidua, Sci. Rep. 10 (2020), 5785.
    [64]
    D. Peng, I. Kryczek, N. Nagarsheth, et al., Epigenetic silencing of TH1-type chemokines shapes tumour immunity and immunotherapy, Nature 527 (2015) 249-253.
    [65]
    A. Lange-Consiglio, P. Romele, M. Magatti, et al., Priming with inflammatory cytokines is not a prerequisite to increase immune-suppressive effects and responsiveness of equine amniotic mesenchymal stromal cells, Stem Cell Res. Ther. 11 (2020), 99.
    [66]
    S. Sakaguchi, K. Wing, Y. Onishi, et al., Regulatory T cells: how do they suppress immune responses?, Int. Immunol. 21 (2009) 1105-1111.
    [67]
    R. Nasrallah, C.J. Imianowski, L. Bossini-Castillo, et al., A distal enhancer at risk locus 11q13.5 promotes suppression of colitis by T(reg) cells, Nature 583 (2020) 447-452.
    [68]
    F.K. Dermani, P. Samadi, G. Rahmani, et al., PD-1/PD-L1 immune checkpoint: Potential target for cancer therapy, J. Cell Physiol. 234 (2019) 1313-1325.
    [69]
    M.L. Stone, K.B. Chiappinelli, H. Li, et al., Epigenetic therapy activates type I interferon signaling in murine ovarian cancer to reduce immunosuppression and tumor burden, Proc. Natl. Acad. Sci. USA 114 (2017) E10981-E10990.
    [70]
    D. Wang, J. Quiros, K. Mahuron, et al., Targeting EZH2 reprograms intratumoral regulatory T cells to enhance cancer immunity, Cell Rep. 23 (2018) 3262-3274.
    [71]
    J. Bullwinkel, A. Ludemann, J. Debarry, et al., Epigenotype switching at the CD14 and CD209 genes during differentiation of human monocytes to dendritic cells, Epigenetics 6 (2011) 45-51.
    [72]
    C. Giallongo, N. Parrinello, D. Tibullo, et al., Myeloid derived suppressor cells (MDSCs) are increased and exert immunosuppressive activity together with polymorphonuclear leukocytes (PMNs) in chronic myeloid leukemia patients, PLoS One 9 (2014), e101848.
    [73]
    K. Atarashi, T. Tanoue, K. Oshima, et al., Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota, Nature 500 (2013) 232-236.
    [74]
    E. Lee, E.J. Fertig, K. Jin, et al., Breast cancer cells condition lymphatic endothelial cells within pre-metastatic niches to promote metastasis, Nat. Commun. 5 (2014), 4715.
    [75]
    F. Veglia, E. Sanseviero, D.I. Gabrilovich, Myeloid-derived suppressor cells in the era of increasing myeloid cell diversity, Nat. Rev. Immunol. 21 (2021) 485-498.
    [76]
    A. Salminen, Activation of immunosuppressive network in the aging process, Ageing Res. Rev. 57 (2020), 100998.
    [77]
    J. Feng, H. Chang, E. Li, et al., Dynamic expression of de novo DNA methyltransferases Dnmt3a and Dnmt3b in the central nervous system, J. Neurosci. Res. 79 (2005) 734-746.
    [78]
    J. Zhenwei, G. Shuxin, Z. Yongchun, et al., Mechanisms of TET protein-mediated DNA demethylation and its role in the regulation of mouse development, Yi Chuan 37 (2015) 34-40.
    [79]
    J. Shekhawat, K. Gauba, S. Gupta, et al., Ten-eleven translocase: key regulator of the methylation landscape in cancer, J. Cancer Res. Clin. Oncol. 147 (2021) 1869-1879.
    [80]
    Y. Ogawara, I. Kitabayashi, [IDH mutations activate Hoxa9/Meis1 and hypoxia pathways in acute myeloid leukemia model mice], Rinsho Ketsueki 56 (2015) 1045-1052.
    [81]
    L.E. Lucca, D.A. Hafler, Resisting fatal attraction: a glioma oncometabolite prevents CD8+ T cell recruitment, J. Clin. Invest. 127 (2017) 1218-1220.
    [82]
    E. Sakai, A. Nakajima, A. Kaneda, Accumulation of aberrant DNA methylation during colorectal cancer development, World J. Gastroenterol. 20 (2014) 978-987.
    [83]
    Y.C. Wu, Z.Q. Ling, The role of TET family proteins and 5-hydroxymethylcytosine in human tumors, Histol. Histopathol. 29 (2014) 991-997.
    [84]
    S.S. Malik, C.T. Coey, K.M. Varney, et al., Thymine DNA glycosylase exhibits negligible affinity for nucleobases that it removes from DNA, Nucleic Acids Res. 43 (2015) 9541-9552.
    [85]
    S. Hongwei, A. Tiezhu, P. Shanhua, et al., Mammalian DNA methylation and its roles during the induced re-programming of somatic cells, Yi Chuan 36 (2014) 431-438.
    [86]
    T.Z. Wang, G. Shan, J.H. Xu, et al., Genome-scale sequence data processing and epigenetic analysis of DNA methylation, Yi Chuan 35 (2013) 685-694.
    [87]
    H.A. Kermani, M. Hosseini, M. Dadmehr, DNA-templated silver nanoclusters for DNA methylation detection, Methods Mol. Biol. 1811 (2018) 173-182.
    [88]
    A. Tramontano, F.L. Boffo, G. Russo, et al., Methylation of the suppressor gene p16INK4a: Mechanism and consequences, Biomolecules 10 (2020), 446.
    [89]
    Y. Huang, L. Chavez, X. Chang, et al., Distinct roles of the methylcytosine oxidases Tet1 and Tet2 in mouse embryonic stem cells, Proc. Natl. Acad. Sci. USA 111 (2014) 1361-1366.
    [90]
    M. Kulis, A. Merkel, S. Heath, et al., Whole-genome fingerprint of the DNA methylome during human B cell differentiation, Nat. Genet. 47 (2015) 746-756.
    [91]
    R. Schmitz, G.W. Wright, D.W. Huang, et al., Genetics and pathogenesis of diffuse large B-cell lymphoma, N Engl J. Med. 378 (2018) 1396-1407.
    [92]
    S. Orlanski, V. Labi, Y. Reizel, et al., Tissue-specific DNA demethylation is required for proper B-cell differentiation and function, Proc. Natl. Acad. Sci. USA 113 (2016) 5018-5023.
    [93]
    M. Ko, H.S. Bandukwala, J. An, et al., Ten-Eleven-Translocation 2 (TET2) negatively regulates homeostasis and differentiation of hematopoietic stem cells in mice, Proc. Natl. Acad. Sci. USA 108 (2011) 14566-14571.
    [94]
    A. Tsagaratou, E. Gonzalez-Avalos, S. Rautio, et al., TET proteins regulate the lineage specification and TCR-mediated expansion of iNKT cells, Nat. Immunol. 18 (2017) 45-53.
    [95]
    M. Li, X. Xiao, W. Zhang, et al., AFM analysis of the multiple types of molecular interactions involved in rituximab lymphoma therapy on patient tumor cells and NK cells, Cell Immunol. 290 (2014) 233-244.
    [96]
    R. Rajalingam, The impact of HLA class I-specific killer cell immunoglobulin-like receptors on antibody-dependent natural killer cell-mediated cytotoxicity and organ allograft rejection, Front. Immunol. 7 (2016), 585.
    [97]
    A. Alamri, R. Rahman, M. Zhang, et al., Semaphorin-3E produced by immature dendritic cells regulates activated natural killer cells migration, Front. Immunol. 9 (2018), 1005.
    [98]
    R.J. Gifford, J. Blomberg, J.M. Coffin, et al., Nomenclature for endogenous retrovirus (ERV) loci, Retrovirology 15 (2018), 59.
    [99]
    X. Jiang, L.G. Xu, SOX9 negatively regulates the RLR antiviral signaling by targeting MAVS, Virus Genes 58 (2022) 122-132.
    [100]
    P.T. Dean, S.B. Hooks, Pleiotropic effects of the COX-2/PGE2 axis in the glioblastoma tumor microenvironment, Front. Oncol. 12 (2022), 1116014.
    [101]
    K.N. Son, Z. Liang, H.L. Lipton, Double-stranded RNA is detected by immunofluorescence analysis in RNA and DNA virus infections, including those by negative-stranded RNA viruses, J. Virol. 89 (2015) 9383-9392.
    [102]
    G. Wang, T. Kouwaki, K. Mugikura, et al., Cytoplasmic dsRNA induces the expression of OCT3/4 and NANOG mRNAs in differentiated human cells, J. Biol. Chem. 294 (2019) 18969-18979.
    [103]
    A.A. de Jesus, Y. Hou, S. Brooks, et al., Distinct interferon signatures and cytokine patterns define additional systemic autoinflammatory diseases, J. Clin. Invest. 130 (2020) 1669-1682.
    [104]
    G. Pepin, M.P. Gantier, cGAS-STING activation in the tumor microenvironment and its role in cancer immunity, Adv. Exp. Med. Biol. 1024 (2017) 175-194.
    [105]
    C. Zhao, X.G. Zhang, C.J. Chen, et al., Maxing Shigan Decoction improves lung and colon tissue damage caused by influenza virus infection through JAK1/2-STAT1 signaling pathway, Zhongguo Zhong Yao Za Zhi 47 (2022) 5306-5315.
    [106]
    E.M. Coccia, A. Battistini, Early IFN type I response: Learning from microbial evasion strategies, Semin. Immunol. 27 (2015) 85-101.
    [107]
    W. Liang, F. Wang, Characterization of mouse CD4 TCR and its targeting antigen, Methods Mol. Biol. 2574 (2022) 221-232.
    [108]
    H. Kurumizaka, T. Kujirai, Y. Takizawa, Contributions of histone variants in nucleosome structure and function, J. Mol. Biol. 433 (2021), 166678.
    [109]
    A. Furukawa, M. Wakamori, Y. Arimura, et al., Acetylated histone H4 tail enhances histone H3 tail acetylation by altering their mutual dynamics in the nucleosome, Proc. Natl. Acad. Sci. USA 117 (2020) 19661-19663.
    [110]
    E. Toussirot, W. Abbas, K.A. Khan, et al., Imbalance between HAT and HDAC activities in the PBMCs of patients with ankylosing spondylitis or rheumatoid arthritis and influence of HDAC inhibitors on TNF alpha production, PLoS One 8 (2013), e70939.
    [111]
    S. Legartova, S. Kozubek, M. Franek, et al., Cell differentiation along multiple pathways accompanied by changes in histone acetylation status, Biochem. Cell Biol. 92 (2014) 85-93.
    [112]
    A. Newbold, G.M. Matthews, M. Bots, et al., Molecular and biologic analysis of histone deacetylase inhibitors with diverse specificities, Mol. Cancer Ther. 12 (2013) 2709-2721.
    [113]
    E. Heninger, T.E. Krueger, J.M. Lang, Augmenting antitumor immune responses with epigenetic modifying agents, Front. Immunol. 6 (2015), 29.
    [114]
    Y. Li, P. Mi, X. Chen, et al., Dynamic profiles and transcriptional preferences of histone modifications during spermiogenesis, Endocrinology 162 (2021), bqaa210.
    [115]
    J. Song, Z. Han, Y.G. Zheng, Identification and profiling of histone acetyltransferase substrates by bioorthogonal labeling, Curr. Protoc. 2 (2022), e497.
    [116]
    H.P. Chen, Y.T. Zhao, T.C. Zhao, Histone deacetylases and mechanisms of regulation of gene expression, Crit. Rev. Oncog. 20 (2015) 35-47.
    [117]
    M. Li, W. An, L. Xu, et al., The arginine methyltransferase PRMT5 and PRMT1 distinctly regulate the degradation of anti-apoptotic protein CFLAR(L) in human lung cancer cells, J. Exp. Clin. Cancer Res. 38 (2019), 64.
    [118]
    F.J. Dekker, T. van den Bosch, N.I. Martin, Small molecule inhibitors of histone acetyltransferases and deacetylases are potential drugs for inflammatory diseases, Drug Discov. Today 19 (2014) 654-660.
    [119]
    T. Kegasawa, T. Tatsumi, T. Yoshioka, et al., Soluble UL16-binding protein 2 is associated with a poor prognosis in pancreatic cancer patients, Biochem. Biophys. Res. Commun. 517 (2019) 84-88.
    [120]
    V. Skov, C.H. Riley, M. Thomassen, et al., Whole blood transcriptional profiling reveals significant down-regulation of human leukocyte antigen class I and II genes in essential thrombocythemia, polycythemia vera and myelofibrosis, Leuk. Lymphoma 54 (2013) 2269-2273.
    [121]
    I.D. Florea, C. Karaoulani, Epigenetic changes of the immune system with role in tumor development, Methods Mol. Biol. 1856 (2018) 203-218.
    [122]
    N. Arshad, M. Laurent-Rolle, W.S. Ahmed, et al., SARS-CoV-2 accessory proteins ORF7a and ORF3a use distinct mechanisms to downregulate MHC-I surface expression, bioRxiv (2022), 2022.05.17.492198.
    [123]
    M.L.M. Jongsma, G. Guarda, R.M. Spaapen, The regulatory network behind MHC class I expression, Mol. Immunol. 113 (2019) 16-21.
    [124]
    H. Kogo, M. Shimizu, Y. Negishi, et al., Suppression of murine tumour growth through CD8(+) cytotoxic T lymphocytes via activated DEC-205(+) dendritic cells by sequential administration of alpha-galactosylceramide in vivo, Immunology 151 (2017) 324-339.
    [125]
    R. Carapito, I. Aouadi, W. Ilias, et al., Natural killer group 2, member D/NKG2D ligands in hematopoietic cell transplantation, Front. Immunol. 8 (2017), 368.
    [126]
    M. Babic, C. Dimitropoulos, Q. Hammer, et al., NK cell receptor NKG2D enforces proinflammatory features and pathogenicity of Th1 and Th17 cells, J. Exp. Med. 217 (2020), e20190133.
    [127]
    T.Y. Hou, M.R. Chen, Y.C. Chou, et al., Impact of enhancer of zeste homolog 2 on T helper cell-mediated allergic rhinitis, Front. Immunol. 8 (2017), 790.
    [128]
    M. Li, Y. Fang, Histone variants: the artists of eukaryotic chromatin, Sci. China Life Sci. 58 (2015) 232-239.
    [129]
    M. Cusack, H.W. King, P. Spingardi, et al., Distinct contributions of DNA methylation and histone acetylation to the genomic occupancy of transcription factors, Genome Res. 30 (2020) 1393-1406.
    [130]
    S. Cuartero, G. Stik, R. Stadhouders, Three-dimensional genome organization in immune cell fate and function, Nat. Rev. Immunol. 23 (2023) 206-221.
    [131]
    A. Nemeckova, V. Kolackova, J. Vrana, et al., DNA replication and chromosome positioning throughout the interphase in three-dimensional space of plant nuclei, J. Exp. Bot. 71 (2020) 6262-6272.
    [132]
    W. Li, W.H. Wong, R. Jiang, DeepTACT: predicting 3D chromatin contacts via bootstrapping deep learning, Nucleic Acids Res. 47 (2019), e60.
    [133]
    C.W. Pak, M. Kosno, A.S. Holehouse, et al., Sequence determinants of intracellular phase separation by complex coacervation of a disordered protein, Mol. Cell 63 (2016) 72-85.
    [134]
    H. Luo, G. Zhu, M.A. Eshelman, et al., HOTTIP-dependent R-loop formation regulates CTCF boundary activity and TAD integrity in leukemia, Mol. Cell 82 (2022) 833-851.e11.
    [135]
    K. Shrinivas, B.R. Sabari, E.L. Coffey, et al., Enhancer features that drive formation of transcriptional condensates, Mol. Cell 75 (2019) 549-561.e7.
    [136]
    H.J. Noh, K.A. Kim, K.C. Kim, p53 down-regulates SETDB1 gene expression during paclitaxel induced-cell death, Biochem. Biophys. Res. Commun. 446 (2014) 43-48.
    [137]
    R. Galupa, E.P. Nora, R. Worsley-Hunt, et al., A conserved noncoding locus regulates random monoallelic xist expression across a topological boundary, Mol. Cell 77 (2020) 352-367.e8.
    [138]
    H. Kato, K. Igarashi, Hematopoietic cell differentiation orchestrated by transcription factor network and its related pathogenesis, Rinsho Ketsueki 59 (2018) 1872-1879.
    [139]
    R. Kulkarni, Early growth response factor 1 in aging hematopoietic stem cells and leukemia, Front. Cell Dev. Biol. 10 (2022), 925761.
    [140]
    M. Crisan, P.S. Kartalaei, C.S. Vink, et al., BMP signalling differentially regulates distinct haematopoietic stem cell types, Nat. Commun. 6 (2015), 8040.
    [141]
    F.A. Flomerfelt, R.E. Gress, Bone marrow and fetal liver radiation chimeras, Methods Mol. Biol. 1323 (2016) 109-115.
    [142]
    J.K. Manesia, M. Franch, D. Tabas-Madrid, et al., Distinct molecular signature of murine fetal liver and adult hematopoietic stem cells identify novel regulators of hematopoietic stem cell function, Stem Cells Dev. 26 (2017) 573-584.
    [143]
    B. Bartholdy, J. Lajugie, Z. Yan, et al., Mechanisms of establishment and functional significance of DNA demethylation during erythroid differentiation, Blood Adv. 2 (2018) 1833-1852.
    [144]
    K.J. Ferrari, A. Scelfo, S. Jammula, et al., Polycomb-dependent H3K27me1 and H3K27me2 regulate active transcription and enhancer fidelity, Mol. Cell 53 (2014) 49-62.
    [145]
    E.E. Khrameeva, G. Fudenberg, M.S. Gelfand, et al., History of chromosome rearrangements reflects the spatial organization of yeast chromosomes, J. Bioinform. Comput. Biol. 14 (2016), 1641002.
    [146]
    G. Sollberger, R. Streeck, F. Apel, et al., Linker histone H1.2 and H1.4 affect the neutrophil lineage determination, Elife 9 (2020), e52563.
    [147]
    H. Liu, Y. Liu, S.G. Jin, et al., TRIM28 secures skeletal stem cell fate during skeletogenesis by silencing neural gene expression and repressing GREM1/AKT/mTOR signaling axis, Cell Rep. 42 (2023), 112012.
    [148]
    C. Bronner, L. Salvi, M. Zocco, et al., Accumulation of RNA on chromatin disrupts heterochromatic silencing, Genome Res. 27 (2017) 1174-1183.
    [149]
    N. Kondoh, M. Mizuno-Kamiya, The role of immune modulatory cytokines in the tumor microenvironments of head and neck squamous cell carcinomas, Cancers 14 (2022), 2884.
    [150]
    J. Goke, X. Lu, Y.S. Chan, et al., Dynamic transcription of distinct classes of endogenous retroviral elements marks specific populations of early human embryonic cells, Cell Stem Cell 16 (2015) 135-141.
    [151]
    K.A. Giles, C.M. Gould, Q. Du, et al., Integrated epigenomic analysis stratifies chromatin remodellers into distinct functional groups, Epigenet. Chromatin 12 (2019), 12.
    [152]
    L.F. Lu, S. Li, Z.X. Wang, et al., Zebrafish NDRG1a negatively regulates IFN induction by promoting the degradation of IRF7, J. Immunol. 202 (2019) 119-130.
    [153]
    M. Yamagami, M. Otsuka, T. Kishikawa, et al., ISGF3 with reduced phosphorylation is associated with constitutive expression of interferon-induced genes in aging cells, NPJ Aging Mech. Dis. 4 (2018), 11.
    [154]
    A. Kroning, A. Furchner, D. Aulich, et al., in situ infrared ellipsometry for protein adsorption studies on ultrathin smart polymer brushes in aqueous environment, ACS Appl. Mater. Interfaces 7 (2015) 12430-12439.
    [155]
    D.H. Phanstiel, K. Van Bortle, D. Spacek, et al., Static and dynamic DNA loops form AP-1-bound activation hubs during macrophage development, Mol. Cell 67 (2017) 1037-1048.e6.
    [156]
    S. Chandra, C. Baribault, M. Lacey, et al., Myogenic differential methylation: diverse associations with chromatin structure, Biology 3 (2014) 426-451.
    [157]
    M. Xia, B. Wang, Z. Wang, et al., Epigenetic regulation of NK cell-mediated antitumor immunity, Front. Immunol. 12 (2021), 672328.
    [158]
    S. Duan, W. Guo, Z. Xu, et al., Natural killer group 2D receptor and its ligands in cancer immune escape, Mol. Cancer 18 (2019), 29.
    [159]
    T.J. Sanders, F. Ullah, A.M. Gehring, et al., Extended archaeal histone-based chromatin structure regulates global gene expression in Thermococcus kodakarensis, Front. Microbiol. 12 (2021), 681150.
    [160]
    S. Guo, Y. Zheng, D. Meng, et al., DNA and coding/non-coding RNA methylation analysis provide insights into tomato fruit ripening, Plant J. 112 (2022) 399-413.
    [161]
    D.V. Zaletaev, M.V. Nemtsova, V.V. Strelnikov, Epigenetic regulation disturbances on gene expression in imprinting diseases, Mol. Biol. 56 (2022) 3-34.
    [162]
    R. Sun, P. Zhu, Advances in measuring DNA methylation, Blood Sci. 4 (2022) 8-15.
    [163]
    S. Shen, Y. Qu, J. Zhang, The application of next generation sequencing on epigenetic study, Yi Chuan 36 (2014) 256-275.
    [164]
    R.H. Chung, C.Y. Kang, pWGBSSimla: a profile-based whole-genome bisulfite sequencing data simulator incorporating methylation QTLs, allele-specific methylations and differentially methylated regions, Bioinformatics 36 (2020) 660-665.
    [165]
    K. Gupta, R. Garg, Method for bisulfite sequencing data analysis for whole-genome level DNA methylation detection in legumes, Methods Mol. Biol. 2107 (2020) 127-145.
    [166]
    P.M. Lizardi, Q. Yan, N. Wajapeyee,DNA bisulfite sequencing for single-nucleotide-resolution DNA methylation detection, Cold Spring Harb. Protoc. 2017 (2017), pdb prot094839.
    [167]
    X. Zhou, D. Li, R.F. Lowdon, et al., methylC Track: Visual integration of single-base resolution DNA methylation data on the WashU EpiGenome Browser, Bioinformatics 30 (2014) 2206-2207.
    [168]
    R.G. Cavalcante, S. Patil, Y. Park, et al., Integrating DNA methylation and hydroxymethylation data with the mint pipeline, Cancer Res. 77 (2017) e27-e30.
    [169]
    M. De Borre, M.R. Branco, Oxidative bisulfite sequencing: An experimental and computational protocol, Methods Mol. Biol. 2198 (2021) 333-348.
    [170]
    Q. Huan, Y. Zhang, S. Wu, et al., HeteroMeth: A database of cell-to-cell heterogeneity in DNA methylation, Genomics Proteomics Bioinformatics 16 (2018) 234-243.
    [171]
    T. Kojima, B. Zhu, H. Nakano, Construction of a DNA library on microbeads using whole genome amplification, Methods Mol. Biol. 1347 (2015) 87-100.
    [172]
    S. Mukherjee, J. Hsieh, Genome-wide identification of transcription factor-binding sites in quiescent adult neural stem cells, Methods Mol. Biol. 1686 (2018) 265-286.
    [173]
    A. Peng, Z. Li, Y. Zhang, et al., The improvewment of DNA library construction in non-crosslinked chromatin immunoprecipitation coupled with next-generation sequencing, Nan Fang Yi Ke Da Xue Xue Bao 39 (2019) 692-698.
    [174]
    C. Kuscu, J.D. Eason, C. Kuscu, Technical advancements in epigenomics and applications in transplantation, Curr. Opin. Organ Transplant. 26 (2021) 23-29.
    [175]
    Z. Chu, M. Fu, J. Guo, et al., Magnetic resistance sensory system for the quantitative measurement of morphine, IEEE Trans. Biomed. Circuits Syst. 15 (2021) 171-176.
    [176]
    S. Naidoo, S. Otoo, N. Naidoo, Physical activity interventions implemented for older people in sub-Saharan Africa: protocol for a scoping review, BMJ Open 13 (2023), e071127.
    [177]
    S. Gopalan, Y. Wang, N.W. Harper, et al., Simultaneous profiling of multiple chromatin proteins in the same cells, Mol. Cell 81 (2021) 4736-4746.e5.
    [178]
    Y. Zhang, Y. Tang, Z. Sun, et al., Tn5 tagments and transposes oligos to single-stranded DNA for strand-specific RNA sequencing, Genome Res. 33 (2023) 412-426.
    [179]
    V. Rykalina, A. Shadrin, H. Lehrach, et al., qPCR-based characterization of DNA fragmentation efficiency of Tn5 transposomes, Biol. Meth. Protoc. 2 (2017), bpx001.
    [180]
    R. Wang, M. Xin, Y. Li, et al., The functions of histone modification enzymes in cancer, Curr. Protein Pept. Sci. 17 (2016) 438-445.
    [181]
    Y. Li, C.Y. Chen, A.M. Kaye, et al., The identification of cis-regulatory elements: A review from a machine learning perspective, Biosystems 138 (2015) 6-17.
    [182]
    S. Sato, Y. Arimura, T. Kujirai, et al., Biochemical analysis of nucleosome targeting by Tn5 transposase, Open Biol. 9 (2019), 190116.
    [183]
    Y. Shen, L.L. Chen, J. Gao, CharPlant: A de novo open chromatin region prediction tool for plant genomes, Genomics Proteomics Bioinformatics 19 (2021) 860-871.
    [184]
    A.O. Farrants, DNA accessibility by MNase digestions, Methods Mol. Biol. 1689 (2018) 77-82.
    [185]
    W.A.M. Hoeijmakers, R. Bartfai, Characterization of the nucleosome landscape by micrococcal nuclease-sequencing (MNase-seq), Methods Mol. Biol. 1689 (2018) 83-101.
    [186]
    R.V. Chereji, J. Ocampo, D.J. Clark, MNase-sensitive complexes in yeast: Nucleosomes and non-histone barriers, Mol. Cell 65 (2017) 565-577.e3.
    [187]
    H. Zhao, W. Zhang, T. Zhang, et al., Genome-wide MNase hypersensitivity assay unveils distinct classes of open chromatin associated with H3K27me3 and DNA methylation in Arabidopsis thaliana, Genome Biol. 21 (2020), 24.
    [188]
    H. Zhao, W. Zhang, L. Chen, et al., Proliferation of regulatory DNA elements derived from transposable elements in the maize genome, Plant Physiol. 176 (2018) 2789-2803.
    [189]
    J. Jiang, The ‘dark matter’ in the plant genomes: non-coding and unannotated DNA sequences associated with open chromatin, Curr. Opin. Plant Biol. 24 (2015) 17-23.
    [190]
    Y. Bordiya, H.G. Kang, Genome-wide analysis of chromatin accessibility in Arabidopsis infected with Pseudomonas syringae, Methods Mol. Biol. 1578 (2017) 263-272.
    [191]
    W. Gao, W.L. Ku, L. Pan, et al., Multiplex indexing approach for the detection of DNase I hypersensitive sites in single cells, Nucleic Acids Res. 49 (2021), e56.
    [192]
    M. Bajic, K.A. Maher, R.B. Deal, Identification of open chromatin regions in plant genomes using ATAC-seq, Methods Mol. Biol. 1675 (2018) 183-201.
    [193]
    D. Penkov, E. Zubkova, Y. Parfyonova, Tn5 DNA transposase in multi-omics research, Meth. Protoc. 6 (2023), 24.
    [194]
    M. Szuplewska, M. Ludwiczak, K. Lyzwa, et al., Mobility and generation of mosaic non-autonomous transposons by Tn3-derived inverted-repeat miniature elements (TIMEs), PLoS One 9 (2014), e105010.
    [195]
    C. Venturini, K.A. Hassan, P. Roy Chowdhury, et al., Sequences of two related multiple antibiotic resistance virulence plasmids sharing a unique IS26-related molecular signature isolated from different Escherichia coli pathotypes from different hosts, PLoS One 8 (2013), e78862.
    [196]
    C.J. Harmer, C.H. Pong, R.M. Hall, Insertion sequences related to ISAjo2 target pdif and dif sites and belong to a new IS family, the IS1202 family, Microb. Genom. 9 (2023), mgen000953.
    [197]
    Y.J. Liu, K. Qi, J. Zhang, et al., Firmicutes-enriched IS 1447 represents a group of IS 3-family insertion sequences exhibiting unique + 1 transcriptional slippage, Biotechnol. Biofuels 11 (2018), 300.
    [198]
    G. Blundell-Hunter, M. Tellier, R. Chalmers, Transposase subunit architecture and its relationship to genome size and the rate of transposition in prokaryotes and eukaryotes, Nucleic Acids Res. 46 (2018) 9637-9646.
    [199]
    C. Doganli, M. Sandoval, S. Thomas, et al., Assay for transposase-accessible chromatin with high-throughput sequencing (ATAC-seq) protocol for zebrafish embryos, Methods Mol. Biol. 1507 (2017) 59-66.
    [200]
    J.D. Buenrostro, P.G. Giresi, L.C. Zaba, et al., Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position, Nat. Methods 10 (2013) 1213-1218.
    [201]
    T. Suzuki, C. Ota, N. Fujino, et al., Improving the viability of tissue-resident stem cells using an organ-preservation solution, FEBS Open Bio 9 (2019) 2093-2104.
    [202]
    J.M. Belton, J. Dekker, Chromosome conformation capture (3C) in budding yeast, Cold Spring Harb. Protoc. 2015 (2015) 580-586.
    [203]
    M. Du, L. Wang, 3C-digital PCR for quantification of chromatin interactions, BMC Mol. Biol. 17 (2016), 23.
    [204]
    A. Schorg, S. Santambrogio, J.L. Platt, et al., Destruction of a distal hypoxia response element abolishes trans-activation of the PAG1 gene mediated by HIF-independent chromatin looping, Nucleic Acids Res. 43 (2015) 5810-5823.
    [205]
    Y. Ben Zouari, A. Platania, A.M. Molitor, et al., 4See: A flexible browser to explore 4C data, Front. Genet. 10 (2019), 1372.
    [206]
    R. Gabriel, I. Kutschera, C.C. Bartholomae, et al., Linear amplification mediated PCR--localization of genetic elements and characterization of unknown flanking DNA, J. Vis. Exp. (2014), e51543.
    [207]
    T.H. Kim, J. Dekker, ChIP-chip, Cold Spring Harb. Protoc. 2018 (2018), pdb.prot082636.
    [208]
    T. Pankert, T. Jegou, M. Caudron-Herger, et al., Tethering RNA to chromatin for fluorescence microscopy based analysis of nuclear organization, Methods 123 (2017) 89-101.
    [209]
    J.M. Belton, J. Dekker, Chromosome conformation capture carbon copy (5C) in budding yeast, Cold Spring Harb. Protoc. 2015 (2015) 593-598.
    [210]
    J. Cao, Q.Q. Li, Poly(A) tag library construction from 10 ng total RNA, Methods Mol. Biol. 1255 (2015) 185-194.
    [211]
    B. Jia, X. Li, W. Liu, et al., GLAPD: Whole genome based LAMP primer design for a set of target genomes, Front. Microbiol. 10 (2019), 2860.
    [212]
    J.H. Kim, K.R. Titus, W. Gong, et al., 5C-ID: Increased resolution Chromosome-Conformation-Capture-Carbon-Copy with in situ 3C and double alternating primer design, Methods 142 (2018) 39-46.
    [213]
    G. Huep, N. Kleinboelting, B. Weisshaar, An easy-to-use primer design tool to address paralogous loci and T-DNA insertion sites in the genome of Arabidopsis thaliana, Plant Methods 10 (2014), 28.
    [214]
    Z. Duan, Targeted DNase hi-C, Methods Mol. Biol. 2157 (2021) 65-83.
    [215]
    D.L. Lafontaine, L. Yang, J. Dekker, et al., Hi-C 3.0: Improved protocol for genome-wide chromosome conformation capture, Curr. Protoc. 1 (2021), e198.
    [216]
    W. Wang, L. Niu, C. Hou, Interrogating global chromatin interaction network by high-throughput chromosome conformation capture (hi-C) in plants, Methods Mol. Biol. 2484 (2022) 55-67.
    [217]
    B. Akgol Oksuz, L. Yang, S. Abraham, et al., Systematic evaluation of chromosome conformation capture assays, Nat. Methods 18 (2021) 1046-1055.
    [218]
    L. Lu, F. Jin, Easy hi-C: A low-input method for capturing genome organization, Methods Mol. Biol. 2599 (2023) 113-125.
    [219]
    H. Alinejad-Rokny, R. Ghavami Modegh, H.R. Rabiee, et al., Correction: MaxHiC: A robust background correction model to identify biologically relevant chromatin interactions in Hi-C and capture Hi-C experiments, PLoS Comput. Biol. 18 (2022), e1010515.
    [220]
    T. Ma, Z. Ye, L. Wang, Genome wide approaches to identify protein-DNA interactions, Curr. Med. Chem. 26 (2019) 7641-7654.
    [221]
    N. Yamada, W.K.M. Lai, N. Farrell, et al., Characterizing protein-DNA binding event subtypes in ChIP-exo data, Bioinformatics 35 (2019) 903-913.
    [222]
    B.E. Koch, J. Stougaard, H.P. Spaink, Spatial and temporal expression patterns of chitinase genes in developing zebrafish embryos, Gene Expr. Patterns 14 (2014) 69-77.
    [223]
    M. Masuda, Y. Li, K. Pak, et al., The promoter and multiple enhancers of the pou4f3 gene regulate expression in inner ear hair cells, Mol. Neurobiol. 54 (2017) 5414-5426.
    [224]
    T.H. Kim, J. Dekker, 4C analysis of 3C, ChIP-loop, and control libraries, Cold Spring Harb. Protoc. 2018 (2018), pdb.prot097881.
    [225]
    T.H. Kim, J. Dekker, Generation of ChIP-loop libraries, Cold Spring Harb. Protoc. 2018 (2018), pdb.prot097857.
    [226]
    M. Labajova, J. Ziarovska, K. Razna, et al., Restriction analyze of starch synthesis genes in Amaranth mutant lines, Pak. J. Biol. Sci. 17 (2014) 68-73.
    [227]
    V. Mayer, A.C. Frank, S. Preinsperger, et al., Removal of chromatin by salt-tolerant endonucleases for production of recombinant measles virus, Biotechnol. Prog. (2023), e3342.
    [228]
    D. Pose, L. Yant, DNA-binding factor target identification by chromatin immunoprecipitation (ChIP) in plants, Methods Mol. Biol. 1363 (2016) 25-35.
    [229]
    Y.M. Chan, I.M. Moustafa, J.J. Arnold, et al., Long-range communication between different functional sites in the picornaviral 3C protein, Structure 24 (2016) 509-517.
    [230]
    P.H.L. Krijger, G. Geeven, V. Bianchi, et al., 4C-seq from beginning to end: A detailed protocol for sample preparation and data analysis, Methods 170 (2020) 17-32.
    [231]
    M. Miranda, D. Noordermeer, B. Moindrot, Detection of allele-specific 3D chromatin interactions using high-resolution In-nucleus 4C-seq, Methods Mol. Biol. 2532 (2022) 15-33.
    [232]
    B. Barnwal, C.K. Mok, J. Wu, et al., A monoclonal antibody binds to threonine 49 in the non-structural 1 protein of influenza A virus and interferes with its ability to modulate viral replication, Antiviral Res. 116 (2015) 55-61.
    [233]
    G. Li, T. Sun, H. Chang, et al., Chromatin interaction analysis with updated ChIA-PET tool (V3), Genes 10 (2019), 554.
    [234]
    X. Li, O.J. Luo, P. Wang, et al., Long-read ChIA-PET for base-pair-resolution mapping of haplotype-specific chromatin interactions, Nat. Protoc. 12 (2017) 899-915.
    [235]
    J. Choy, M.J. Fullwood, Deciphering noncoding RNA and chromatin interactions: Multiplex chromatin interaction analysis by paired-end tag sequencing (mChIA-PET), Methods Mol. Biol. 1468 (2017) 63-89.
    [236]
    E.S. Kim, N. Lee, J.W. Park, et al., Kinetic characterization of on-chip DNA ligation on dendron-coated surfaces with nanoscaled lateral spacings, Nanotechnology 24 (2013), 405703.
    [237]
    Y.F. Li, M. Zhao, M. Wang, et al., An improved method of constructing degradome library suitable for sequencing using Illumina platform, Plant Methods 15 (2019), 134.
    [238]
    D. Skurnik, D. Roux, H. Aschard, et al., A comprehensive analysis of in vitro and in vivo genetic fitness of Pseudomonas aeruginosa using high-throughput sequencing of transposon libraries, PLoS Pathog. 9 (2013), e1003582.
    [239]
    M. Tasnim, T.J. Selph, J. Olcott, et al., The type IIS restriction enzyme MmeI can cut across a double-strand break, Mol. Biol. Rep. 50 (2023) 5495-5499.
    [240]
    Y.L. Orlov, O. Thierry, A.G. Bogomolov, et al., Computer methods of analysis of chromosome contacts in the cell nucleus based on sequencing technology data, Biomed. Khim. 63 (2017) 418-422.
    [241]
    V. Fernandes, K. Teles, C. Ribeiro, et al., Fat nucleosome: Role of lipids on chromatin, Prog. Lipid Res. 70 (2018) 29-34.
    [242]
    X. Wang, L. Qiu, Z. Li, et al., Understanding the multifaceted role of neutrophils in cancer and autoimmune diseases, Front. Immunol. 9 (2018), 2456.
    [243]
    M.E. Castro-Manrreza, Participation of mesenchymal stem cells in the regulation of immune response and cancer development, Bol. Med. Hosp. Infant. Mex. 73 (2016) 380-387.
    [244]
    L. Villanueva, D. Alvarez-Errico, M. Esteller, The contribution of epigenetics to cancer immunotherapy, Trends Immunol. 41 (2020) 676-691.
    [245]
    J. Borley, R. Brown, Epigenetic mechanisms and therapeutic targets of chemotherapy resistance in epithelial ovarian cancer, Ann. Med. 47 (2015) 359-369.
    [246]
    T.J. Chien, A review of the endocrine resistance in hormone-positive breast cancer, Am. J. Cancer Res. 11 (2021) 3813-3831.
    [247]
    Q. Wu, A.E. Berglund, A.B. Etame, The impact of epigenetic modifications on adaptive resistance evolution in glioblastoma, Int. J. Mol. Sci. 22 (2021), 8324.
    [248]
    M. Luo, X. Yang, H.N. Chen, et al., Drug resistance in colorectal cancer: An epigenetic overview, Biochim. Biophys. Acta Rev. Cancer 1876 (2021), 188623.
    [249]
    S. Rauscher, R. Greil, R. Geisberger, re-sensitizing tumor cells to cancer drugs with epigenetic regulators, Curr. Cancer Drug Targets 21 (2021) 353-359.
    [250]
    N. Rastgoo, J. Abdi, J. Hou, et al., Role of epigenetics-microRNA axis in drug resistance of multiple myeloma, J. Hematol. Oncol. 10 (2017), 121.
    [251]
    X. Pan, L. Zheng, Epigenetics in modulating immune functions of stromal and immune cells in the tumor microenvironment, Cell Mol. Immunol. 17 (2020) 940-953.
    [252]
    B. Frey, M. Ruckert, L. Deloch, et al., Immunomodulation by ionizing radiation-impact for design of radio-immunotherapies and for treatment of inflammatory diseases, Immunol. Rev. 280 (2017) 231-248.
    [253]
    D. Karan, Inflammasomes: Emerging central players in cancer immunology and immunotherapy, Front. Immunol. 9 (2018), 3028.
    [254]
    S. Van Lint, S. Wilgenhof, C. Heirman, et al., Optimized dendritic cell-based immunotherapy for melanoma: the TriMix-formula, Cancer Immunol. Immunother. 63 (2014) 959-967.
    [255]
    G. Petroni, L.C. Cantley, L. Santambrogio, et al., Radiotherapy as a tool to elicit clinically actionable signalling pathways in cancer, Nat. Rev. Clin. Oncol. 19 (2022) 114-131.
    [256]
    Y.N. Diep, T.J. Kim, H. Cho, et al., Nanomedicine for advanced cancer immunotherapy, J. Control Release 351 (2022) 1017-1037.
    [257]
    X. Duan, C. Chan, W. Lin, Nanoparticle-mediated immunogenic cell death enables and potentiates cancer immunotherapy, Angew. Chem. Int. Ed Engl. 58 (2019) 670-680.
    [258]
    M. Matsushita, Immunogenic cell death in hematological malignancies, Rinsho Ketsueki 62 (2021) 709-716.
    [259]
    W. Sun, S. Lv, H. Li, et al., Enhancing the anticancer efficacy of immunotherapy through combination with histone modification inhibitors, Genes 9 (2018), 633.
    [260]
    X. Zhang, X. Guo, Y. Wu, et al., Locally injectable hydrogels for tumor immunotherapy, Gels 7 (2021), 224.
    [261]
    J. Zhao, S. Cai, L. Zhang, et al., Progress, challenges, and prospects of research on the effect of gene polymorphisms on adverse reactions to opioids, Pain Ther. 11 (2022) 395-409.
    [262]
    J.S. Bowers, S.R. Bailey, M.P. Rubinstein, et al., Genomics meets immunity in pancreatic cancer: Current research and future directions for pancreatic adenocarcinoma immunotherapy, Oncol. Rev. 13 (2019), 430.
    [263]
    M.H. Saleh, L. Wang, M.S. Goldberg, Improving cancer immunotherapy with DNA methyltransferase inhibitors, Cancer Immunol. Immunother. 65 (2016) 787-796.
    [264]
    B.E. Deverman, B.M. Ravina, K.S. Bankiewicz, et al., Gene therapy for neurological disorders: progress and prospects, Nat. Rev. Drug Discov. 17 (2018), 767.
    [265]
    A. Iqubal, M.K. Iqubal, A. Khan, et al., Gene therapy, A novel therapeutic tool for neurological disorders: Current progress, challenges and future prospective, Curr. Gene Ther. 20 (2020) 184-194.
    [266]
    F.P. Manfredsson, D.C. Bloom, R.J. Mandel, Regulated protein expression for in vivo gene therapy for neurological disorders: progress, strategies, and issues, Neurobiol. Dis. 48 (2012) 212-221.
    [267]
    D.E. Biancur, K.S. Kapner, K. Yamamoto, et al., Functional genomics identifies metabolic vulnerabilities in pancreatic cancer, Cell Metab. 33 (2021) 199-210.e8.
    [268]
    R. Ding, C.C. Chao, Q. Gao, High-efficiency of genetic modification using CRISPR/Cpf1 system for engineered CAR-T cell therapy, Methods Cell Biol. 167 (2022) 1-14.
    [269]
    J. Salas-Mckee, W. Kong, W.L. Gladney, et al., CRISPR/Cas9-based genome editing in the era of CAR T cell immunotherapy, Hum. Vaccin. Immunother. 15 (2019) 1126-1132.
    [270]
    W.C. Gan, A.P.K. Ling, CRISPR/Cas9 in plant biotechnology: applications and challenges, BioTechnologia 103 (2022) 81-93.
    [271]
    R.J. Torphy, Y. Zhu, R.D. Schulick, Immunotherapy for pancreatic cancer: Barriers and breakthroughs, Ann. Gastroenterol. Surg. 2 (2018) 274-281.
    [272]
    S. Khatua, W. Zaky, The biologic era of childhood medulloblastoma and clues to novel therapies, Future Oncol. 10 (2014) 637-645.
    [273]
    J.C. Crispin, G.C. Tsokos, Cancer immunosurveillance by CD8 T cells, F1000Res 9 (2020), F1000FacultyRev-F1000FacultyR80.
    [274]
    R. Muthuswamy, A.R. McGray, S. Battaglia, et al., CXCR6 by increasing retention of memory CD8(+) T cells in the ovarian tumor microenvironment promotes immunosurveillance and control of ovarian cancer, J. Immunother. Cancer 9 (2021), e003329.
    [275]
    X. Yu, L. Zhang, A. Chaudhry, et al., Unravelling the heterogeneity and dynamic relationships of tumor-infiltrating T cells by single-cell RNA sequencing analysis, J. Leukoc. Biol. 107 (2020) 917-932.
    [276]
    F. Anari, C. Ramamurthy, M. Zibelman, Impact of tumor microenvironment composition on therapeutic responses and clinical outcomes in cancer, Future Oncol. 14 (2018) 1409-1421.
    [277]
    M. Luu, B. Schutz, M. Lauth, et al., The impact of gut microbiota-derived metabolites on the tumor immune microenvironment, Cancers 15 (2023), 1588.
    • Relative Articles
    • Supplements(0)
    • Cited By
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(1)

    Get Citation
    PDF
    XML

    Article Metrics

    Article views (225) PDF downloads(16) Cited by()
    Proportional views
    Related

    Copyright © Journal of Pharmaceutical Analysis

    E-mail: jpa2011@126.com;  jpasubmit@126.com;  jpaeditor@xjtu.edu.cn   Tel:+86-029-88960092

    Address: Western China Science and Technology Innovation Harbour, Xixian New Area, Xi’an, 712000, China

    Email alert RSS

    Supported by: Beijing Renhe Information Technology Co. Ltd    

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return