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http://dx.doi.org/10.14348/molcells.2021.5016

Human Endogenous Retroviruses as Gene Expression Regulators: Insights from Animal Models into Human Diseases  

Durnaoglu, Serpen (Department of Life Sciences, College of Natural Sciences, Hanyang University)
Lee, Sun-Kyung (Department of Life Sciences, College of Natural Sciences, Hanyang University)
Ahnn, Joohong (Department of Life Sciences, College of Natural Sciences, Hanyang University)
Publication Information
Molecules and Cells / v.44, no.12, 2021 , pp. 861-878 More about this Journal
Abstract
The human genome contains many retroviral elements called human endogenous retroviruses (HERVs), resulting from the integration of retroviruses throughout evolution. HERVs once were considered inactive junk because they are not replication-competent, primarily localized in the heterochromatin, and silenced by methylation. But HERVs are now clearly shown to actively regulate gene expression in various physiological and pathological conditions such as developmental processes, immune regulation, cancers, autoimmune diseases, and neurological disorders. Recent studies report that HERVs are activated in patients suffering from coronavirus disease 2019 (COVID-19), the current pandemic caused by SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2) infection. In this review, we describe internal and external factors that influence HERV activities. We also present evidence showing the gene regulatory activity of HERV LTRs (long terminal repeats) in model organisms such as mice, rats, zebrafish, and invertebrate models of worms and flies. Finally, we discuss several molecular and cellular pathways involving various transcription factors and receptors, through which HERVs affect downstream cellular and physiological events such as epigenetic modifications, calcium influx, protein phosphorylation, and cytokine release. Understanding how HERVs participate in various physiological and pathological processes will help develop a strategy to generate effective therapeutic approaches targeting HERVs.
Keywords
cancer; COVID-19; human endogenous retrovirus; neurological disease; syncytin-1; toll-like receptor;
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1 Frank, O., Jones-Brando, L., Leib-Mosch, C., Yolken, R., and Seifarth, W. (2006). Altered transcriptional activity of human endogenous retroviruses in neuroepithelial cells after infection with Toxoplasma gondii. J. Infect. Dis. 194, 1447-1449.   DOI
2 Firouzi, R., Rolland, A., Michel, M., Jouvin-Marche, E., Hauw, J.J., Malcus-Vocanson, C., Lazarini, F., Gebuhrer, L., Seigneurin, J.M., Touraine, J.L., et al. (2003). Multiple sclerosis-associated retrovirus particles cause T lymphocyte-dependent death with brain hemorrhage in humanized SCID mice model. J. Neurovirol. 9, 79-93.   DOI
3 Hamilton, N., Clarke, A., Isles, H., Carson, E., Levraud, J.P., and Renshaw, S.A. (2021). A zebrafish reporter line reveals immune and neuronal expression of endogenous retrovirus. BioRxiv, https://doi.org/10.1101/2021.01.21.427598   DOI
4 Hanke, K., Chudak, C., Kurth, R., and Bannert, N. (2013). The Rec protein of HERV-K(HML-2) upregulates androgen receptor activity by binding to the human small glutamine-rich tetratricopeptide repeat protein (hSGT). Int. J. Cancer 132, 556-567.   DOI
5 Hayward, A., Grabherr, M., and Jern, P. (2013). Broad-scale phylogenomics provides insights into retrovirus-host evolution. Proc. Natl. Acad. Sci. U. S. A. 110, 20146-20151.   DOI
6 Herbst, H., Sauter, M., and Mueller-Lantzsch, N. (1996). Expression of human endogenous retrovirus K elements in germ cell and trophoblastic tumors. Am. J. Pathol. 149, 1727-1735.
7 Howe, K., Clark, M.D., Torroja, C.F., Torrance, J., Berthelot, C., Muffato, M., Collins, J.E., Humphray, S., McLaren, K., Matthews, L., et al. (2013). The zebrafish reference genome sequence and its relationship to the human genome. Nature 496, 498-503.   DOI
8 Huang, W., Li, S., Hu, Y., Yu, H., Luo, F., Zhang, Q., and Zhu, F. (2011). Implication of the env gene of the human endogenous retrovirus W family in the expression of BDNF and DRD3 and development of recent-onset schizophrenia. Schizophr. Bull. 37, 988-1000.   DOI
9 Huang, Y., Kim, J.K., Do, D.V., Lee, C., Penfold, C.A., Zylicz, J.J., Marioni, J.C., Hackett, J.A., and Surani, M.A. (2017). Stella modulates transcriptional and endogenous retrovirus programs during maternal-to-zygotic transition. Elife 6, e22345.   DOI
10 Jo, J.O., Kang, Y.J., Ock, M.S., Song, K.S., Jeong, M.J., Jeong, S.J., Choi, Y.H., Ko, E.J., Leem, S.H., Kim, S., et al. (2016). Expression profiles of HERV-K Env protein in normal and cancerous tissues. Genes Genomics 38, 91-107.   DOI
11 Chung, K.W., Kim, J.S., and Lee, K.S. (2020). A database of Caenorhabditis elegans locomotion and body posture phenotypes for the peripheral neuropathy model. Mol. Cells 43, 880-888.   DOI
12 Tugnet, N., Rylance, P., Roden, D., Trela, M., and Nelson, P. (2013). Human endogenous retroviruses (HERVs) and autoimmune rheumatic disease: is there a link? Open Rheumatol. J. 7, 13-21.   DOI
13 Bannert, N. and Kurth, R. (2004). Retroelements and the human genome: new perspectives on an old relation. Proc. Natl. Acad. Sci. U. S. A. 101(Suppl 2), 14572-14579.   DOI
14 C. elegans Sequencing Consortium (1998). Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282, 2012-2018.   DOI
15 Doucet-O'Hare, T.T., DiSanza, B.L., DeMarino, C., Atkinson, A.L., Rosenblum, J.S., Henderson, L.J., Johnson, K.R., Kowalak, J., Garcia-Montojo, M., Allen, S.J., et al. (2021). SMARCB1 deletion in atypical teratoid rhabdoid tumors results in human endogenous retrovirus K (HML-2) expression. Sci. Rep. 11, 12893.   DOI
16 Fuentes, D.R., Swigut, T., and Wysocka, J. (2018). Systematic perturbation of retroviral LTRs reveals widespread long-range effects on human gene regulation. Elife 7, e35989.   DOI
17 Freimanis, G., Hooley, P., Ejtehadi, H.D., Ali, H.A., Veitch, A., Rylance, P.B., Alawi, A., Axford, J., Nevill, A., Murray, P.G., et al. (2010). A role for human endogenous retrovirus-K (HML-2) in rheumatoid arthritis: investigating mechanisms of pathogenesis. Clin. Exp. Immunol. 160, 340-347.   DOI
18 Fischer, S., Echeverria, N., Cristina, J., and Moreno, P. (2016). Human endogenous retrovirus: their relationship with hematological diseases. J. Leuk. (Los Angel.) 4, 217.
19 Florl, A.R., Lower, R., Schmitz-Drager, B.J., and Schulz, W.A. (1999). DNA methylation and expression of LINE-1 and HERV-K provirus sequences in urothelial and renal cell carcinomas. Br. J. Cancer 80, 1312-1321.   DOI
20 Frank, O., Giehl, M., Zheng, C., Hehlmann, R., Leib-Mosch, C., and Seifarth, W. (2005). Human endogenous retrovirus expression profiles in samples from brains of patients with schizophrenia and bipolar disorders. J. Virol. 79, 10890-10901.   DOI
21 Fries, G.R., Walss-Bass, C., Bauer, M.E., and Teixeira, A.L. (2019). Revisiting inflammation in bipolar disorder. Pharmacol. Biochem. Behav. 177, 12-19.   DOI
22 Jennings, B.H. (2011). Drosophila - a versatile model in biology & medicine. Mater. Today (Kidlington) 14, 190-195.   DOI
23 Jonsson, M.E., Garza, R., Sharma, Y., Petri, R., Sodersten, E., Johansson, J.G., Johansson, P.A., Atacho, D.A., Pircs, K., Madsen, S., et al. (2021). Activation of endogenous retroviruses during brain development causes an inflammatory response. EMBO J. 40, e106423.
24 Jung, J., Choi, I., Ro, H., Huh, T.L., Choe, J., and Rhee, M. (2020b). march5 governs the convergence and extension movement for organization of the telencephalon and diencephalon in zebrafish embryos. Mol. Cells 43, 76-85.   DOI
25 Jung, J., Udhaya Kumar, S., Choi, I., Huh, T.L., and Rhee, M. (2019). Znf76 is associated with development of the eyes, midbrain, MHB, and hindbrain in zebrafish embryos. Anim. Cells Syst. (Seoul) 23, 26-31.   DOI
26 Chuong, E.B., Elde, N.C., and Feschotte, C. (2016). Regulatory evolution of innate immunity through co-option of endogenous retroviruses. Science 351, 1083-1087.   DOI
27 Uchida, O., Nakano, H., Koga, M., and Ohshima, Y. (2003). The C. elegans che-1 gene encodes a zinc finger transcription factor required for specification of the ASE chemosensory neurons. Development 130, 1215-1224.   DOI
28 Li, W., Lee, M.H., Henderson, L., Tyagi, R., Bachani, M., Steiner, J., Campanac, E., Hoffman, D.A., von Geldern, G., Johnson, K., et al. (2015). Human endogenous retrovirus-K contributes to motor neuron disease. Sci. Transl. Med. 7, 307ra153.   DOI
29 Fuchs, N.V., Kraft, M., Tondera, C., Hanschmann, K.M., Lower, J., and Lower, R. (2011). Expression of the human endogenous retrovirus (HERV) group HML-2/HERV-K does not depend on canonical promoter elements but is regulated by transcription factors Sp1 and Sp3. J. Virol. 85, 3436-3448.   DOI
30 Levine, E. and Lee, K.S. (2020). Microfluidic approaches for Caenorhabditis elegans research. Anim. Cells Syst. (Seoul) 24, 311-320.   DOI
31 Manghera, M., Ferguson-Parry, J., Lin, R., and Douville, R.N. (2016). NF-κB and IRF1 induce endogenous retrovirus K expression via interferon-stimulated response elements in its 5' long terminal repeat. J. Virol. 90, 9338-9349.   DOI
32 Wang, J., Xie, G., Singh, M., Ghanbarian, A.T., Rasko, T., Szvetnik, A., Cai, H., Besser, D., Prigione, A., Fuchs, N.V., et al. (2014). Primate-specific endogenous retrovirus-driven transcription defines naive-like stem cells. Nature 516, 405-409.   DOI
33 Vlisidou, I. and Wood, W. (2015). Drosophila blood cells and their role in immune responses. FEBS J. 282, 1368-1382.   DOI
34 Wallace, T.A., Downey, R.F., Seufert, C.J., Schetter, A., Dorsey, T.H., Johnson, C.A., Goldman, R., Loffredo, C.A., Yan, P., Sullivan, F.J., et al. (2014). Elevated HERV-K mRNA expression in PBMC is associated with a prostate cancer diagnosis particularly in older men and smokers. Carcinogenesis 35, 2074-2083.   DOI
35 Wang-Johanning, F., Liu, J., Rycaj, K., Huang, M., Tsai, K., Rosen, D.G., Chen, D.T., Lu, D.W., Barnhart, K.F., and Johanning, G.L. (2007). Expression of multiple human endogenous retrovirus surface envelope proteins in ovarian cancer. Int. J. Cancer 120, 81-90.   DOI
36 Turcanova, V.L., Bundgaard, B., and Hollsberg, P. (2009). Human herpesvirus-6B induces expression of the human endogenous retrovirus K18-encoded superantigen. J. Clin. Virol. 46, 15-19.   DOI
37 Katoh, I., Mirova, A., Kurata, S., Murakami, Y., Horikawa, K., Nakakuki, N., Sakai, T., Hashimoto, K., Maruyama, A., Yonaga, T., et al. (2011). Activation of the long terminal repeat of human endogenous retrovirus K by melanoma-specific transcription factor MITF-M. Neoplasia 13, 1081-1092.   DOI
38 Katsumata, K., Ikeda, H., Sato, M., Ishizu, A., Kawarada, Y., Kato, H., Wakisaka, A., Koike, T., and Yoshiki, T. (1999). Cytokine regulation of env gene expression of human endogenous retrovirus-R in human vascular endothelial cells. Clin. Immunol. 93, 75-80.   DOI
39 Montesion, M., Williams, Z.H., Subramanian, R.P., Kuperwasser, C., and Coffin, J.M. (2018). Promoter expression of HERV-K (HML-2) provirus-derived sequences is related to LTR sequence variation and polymorphic transcription factor binding sites. Retrovirology 15, 57.   DOI
40 Mayer, J., Harz, C., Sanchez, L., Pereira, G.C., Maldener, E., Heras, S.R., Ostrow, L.W., Ravits, J., Batra, R., Meese, E., et al. (2018). Transcriptional profiling of HERV-K(HML-2) in amyotrophic lateral sclerosis and potential implications for expression of HML-2 proteins. Mol. Neurodegener. 13, 39.   DOI
41 Nakagawa, K., Brusic, V., McColl, G., and Harrison, L.C. (1997). Direct evidence for the expression of multiple endogenous retroviruses in the synovial compartment in rheumatoid arthritis. Arthritis Rheum. 40, 627-638.   DOI
42 Wang, X., Wu, X., Huang, J., Li, H., Yan, Q., and Zhu, F. (2021). Human endogenous retrovirus W family envelope protein (HERV-W env) facilitates the production of TNF-α and IL-10 by inhibiting MyD88s in glial cells. Arch. Virol. 166, 1035-1045.   DOI
43 Kim, D.Y., Moon, S.H., Han, J.H., Kim, M.J., Oh, S.J., Bharti, D., Lee, S.H., Park, J.K., Rho, G.J., and Jeon, B.G. (2020). Terminal differentiation into adipocyte and growth inhibition by PPARγ activation in human A549 lung adenocarcinoma cells. Anim. Cells Syst. (Seoul) 24, 329-340.   DOI
44 Wang, T., Medynets, M., Johnson, K.R., Doucet-O'Hare, T.T., DiSanza, B., Li, W., Xu, Y., Bagnell, A., Tyagi, R., Sampson, K., et al. (2020b). Regulation of stem cell function and neuronal differentiation by HERV-K via mTOR pathway. Proc. Natl. Acad. Sci. U. S. A. 117, 17842-17853.   DOI
45 Wang, X., Liu, Z., Wang, P., Li, S., Zeng, J., Tu, X., Yan, Q., Xiao, Z., Pan, M., and Zhu, F. (2018). Syncytin-1, an endogenous retroviral protein, triggers the activation of CRP via TLR3 signal cascade in glial cells. Brain Behav. Immun. 67, 324-334.   DOI
46 Kim, Y.J., Kim, K., Seo, S.Y., Yu, J., Kim, I.H., Kim, H.J., Park, C.K., Lee, K.H., Choi, J., Song, M.S., et al. (2021). Time-sequential change in immune-related gene expression after irradiation in glioblastoma: next-generation sequencing analysis. Anim. Cells Syst. (Seoul) 25, 245-254.   DOI
47 Knossl, M., Lower, R., and Lower, J. (1999). Expression of the human endogenous retrovirus HTDV/HERV-K is enhanced by cellular transcription factor YY1. J. Virol. 73, 1254-1261.   DOI
48 Komurian-Pradel, F., Paranhos-Baccala, G., Bedin, F., Ounanian-Paraz, A., Sodoyer, M., Ott, C., Rajoharison, A., Garcia, E., Mallet, F., Mandrand, B., et al. (1999). Molecular cloning and characterization of MSRV-related sequences associated with retrovirus-like particles. Virology 260, 1-9.   DOI
49 Bergallo, M., Galliano, I., Dapra, V., Pirra, A., Montanari, P., Pavan, M., Calvi, C., Bertino, E., Coscia, A., and Tovo, P.A. (2019). Transcriptional activity of human endogenous retroviruses in response to prenatal exposure of maternal cigarette smoking. Am. J. Perinatol. 36, 1060-1065.   DOI
50 Tanaka, S. (2000). [Molecular and pathological analyses of newly established transgenic rats carrying human endogenous retrovirus gene, ERV3]. Hokkaido Igaku Zasshi 75, 105-116. Japanese.
51 Wang, Z., Wang, Y., He, Y., Zhang, N., Chang, W., and Niu, Y. (2020c). Aquaporin-1 facilitates proliferation and invasion of gastric cancer cells via GRB7-mediated ERK and Ras activation. Anim. Cells Syst. (Seoul) 24, 253-259.   DOI
52 Gutierrez, K., Dicks, N., Glanzner, W., Agellon, L., and Bordignon, V. (2015). Efficacy of the porcine species in biomedical research. Front. Genet. 6, 293.   DOI
53 Garcia-Montojo, M., Doucet-O'Hare, T., Henderson, L., and Nath, A. (2018). Human endogenous retrovirus-K (HML-2): a comprehensive review. Crit. Rev. Microbiol. 44, 715-738.   DOI
54 Galli, U.M., Sauter, M., Lecher, B., Maurer, S., Herbst, H., Roemer, K., and Mueller-Lantzsch, N. (2005). Human endogenous retrovirus rec interferes with germ cell development in mice and may cause carcinoma in situ, the predecessor lesion of germ cell tumors. Oncogene 24, 3223-3228.   DOI
55 Kuzmich, N.N., Sivak, K.V., Chubarev, V.N., Porozov, Y.B., Savateeva-Lyubimova, T.N., and Peri, F. (2017). TLR4 signaling pathway modulators as potential therapeutics in inflammation and sepsis. Vaccines (Basel) 5, 34.   DOI
56 Lee, H., Yoon, D.E., and Kim, K. (2020b). Genome editing methods in animal models. Anim. Cells Syst. (Seoul) 24, 8-16.   DOI
57 Yang, Z., Chen, S., Xue, S., Li, X., Sun, Z., Yang, Y., Hu, X., Geng, T., and Cui, H. (2018). Generation of Cas9 transgenic zebrafish and their application in establishing an ERV-deficient animal model. Biotechnol. Lett. 40, 1507-1518.   DOI
58 Young, J.M., Whiddon, J.L., Yao, Z., Kasinathan, B., Snider, L., Geng, L.N., Balog, J., Tawil, R., van der Maarel, S.M., and Tapscott, S.J. (2013). DUX4 binding to retroelements creates promoters that are active in FSHD muscle and testis. PLoS Genet. 9, e1003947.   DOI
59 Yu, H.L., Zhao, Z.K., and Zhu, F. (2013). The role of human endogenous retroviral long terminal repeat sequences in human cancer (Review). Int. J. Mol. Med. 32, 755-762.   DOI
60 Yuan, Z., Yang, Y., Zhang, N., Soto, C., Jiang, X., An, Z., and Zheng, W.J. (2021). Human endogenous retroviruses in glioblastoma multiforme. Microorganisms 9, 764.   DOI
61 Adams, M.D., Celniker, S.E., Holt, R.A., Evans, C.A., Gocayne, J.D., Amanatides, P.G., Scherer, S.E., Li, P.W., Hoskins, R.A., Galle, R.F., et al. (2000). The genome sequence of Drosophila melanogaster. Science 287, 2185-2195.   DOI
62 Meneely, P.M., Dahlberg, C.L., and Rose, J.K. (2019). Working with worms: Caenorhabditis elegans as a model organism. Curr. Protoc. Essent. Lab. Tech. 19, e35.
63 Burns, K.H. (2017). Transposable elements in cancer. Nat. Rev. Cancer 17, 415-424.   DOI
64 Lemaitre, C., Tsang, J., Bireau, C., Heidmann, T., and Dewannieux, M. (2017). A human endogenous retrovirus-derived gene that can contribute to oncogenesis by activating the ERK pathway and inducing migration and invasion. PLoS Pathog. 13, e1006451.   DOI
65 Mattera, L., Escaffit, F., Pillaire, M.J., Selves, J., Tyteca, S., Hoffmann, J.S., Gourraud, P.A., Chevillard-Briet, M., Cazaux, C., and Trouche, D. (2009). The p400/Tip60 ratio is critical for colorectal cancer cell proliferation through DNA damage response pathways. Oncogene 28, 1506-1517.   DOI
66 Menendez, L., Benigno, B.B., and McDonald, J.F. (2004). L1 and HERV-W retrotransposons are hypomethylated in human ovarian carcinomas. Mol. Cancer 3, 12.   DOI
67 Misiak, B., Stanczykiewicz, B., Kotowicz, K., Rybakowski, J.K., Samochowiec, J., and Frydecka, D. (2018). Cytokines and C-reactive protein alterations with respect to cognitive impairment in schizophrenia and bipolar disorder: a systematic review. Schizophr. Res. 192, 16-29.   DOI
68 Mitsuhashi, S., Nakagawa, S., Sasaki-Honda, M., Sakurai, H., Frith, M.C., and Mitsuhashi, H. (2021). Nanopore direct RNA sequencing detects DUX4-activated repeats and isoforms in human muscle cells. Hum. Mol. Genet. 30, 552-563.   DOI
69 Ko, E.J., Ock, M.S., Choi, Y.H., Iovanna, J.L., Mun, S., Han, K., Kim, H.S., and Cha, H.J. (2021a). Human endogenous retrovirus (HERV)-K env gene knockout affects tumorigenic characteristics of nupr1 gene in DLD-1 colorectal cancer cells. Int. J. Mol. Sci. 22, 3941.   DOI
70 Gao, Y., Yu, X.F., and Chen, T. (2021). Human endogenous retroviruses in cancer: expression, regulation and function. Oncol. Lett. 21, 121.   DOI
71 Gutierrez-Lovera, C., Vazquez-Rios, A.J., Guerra-Varela, J., Sanchez, L., and de la Fuente, M. (2017). The potential of zebrafish as a model organism for improving the translation of genetic anticancer nanomedicines. Genes (Basel) 8, 349.   DOI
72 Goldsmith, D.R., Rapaport, M.H., and Miller, B.J. (2016). A meta-analysis of blood cytokine network alterations in psychiatric patients: comparisons between schizophrenia, bipolar disorder and depression. Mol. Psychiatry 21, 1696-1709.   DOI
73 Gorrini, C., Squatrito, M., Luise, C., Syed, N., Perna, D., Wark, L., Martinato, F., Sardella, D., Verrecchia, A., Bennett, S., et al. (2007). Tip60 is a haploinsufficient tumour suppressor required for an oncogene-induced DNA damage response. Nature 448, 1063-1067.   DOI
74 Hayward, A., Cornwallis, C.K., and Jern, P. (2015). Pan-vertebrate comparative genomics unmasks retrovirus macroevolution. Proc. Natl. Acad. Sci. U. S. A. 112, 464-469.   DOI
75 Hohenadl, C., Germaier, H., Walchner, M., Hagenhofer, M., Herrmann, M., Sturzl, M., Kind, P., Hehlmann, R., Erfle, V., and Leib-Mosch, C. (1999). Transcriptional activation of endogenous retroviral sequences in human epidermal keratinocytes by UVB irradiation. J. Invest. Dermatol. 113, 587-594.   DOI
76 Kristensen, M.K. and Christensen, T. (2021). Regulation of the expression of human endogenous retroviruses: elements in fetal development and a possible role in the development of cancer and neurological diseases. APMIS 129, 241-253.   DOI
77 Durnaoglu, S., Kim, H.S., Ahnn, J., and Lee, S.K. (2020). Human Endogenous Retrovirus K (HERV-K) can drive gene expression as a promoter in Caenorhabditis elegans. BMB Rep. 53, 521-526.   DOI
78 Alqahtani, S., Promtong, P., Oliver, A.W., He, X.T., Walker, T.D., Povey, A., Hampson, L., and Hampson, I.N. (2016). Silver nanoparticles exhibit size-dependent differential toxicity and induce expression of syncytin-1 in FA-AML1 and MOLT-4 leukaemia cell lines. Mutagenesis 31, 695-702.   DOI
79 Dunn, C.A., Medstrand, P., and Mager, D.L. (2003). An endogenous retroviral long terminal repeat is the dominant promoter for human beta1,3-galactosyltransferase 5 in the colon. Proc. Natl. Acad. Sci. U. S. A. 100, 12841-12846.   DOI
80 Duperray, A., Barbe, D., Raguenez, G., Weksler, B.B., Romero, I.A., Couraud, P.O., Perron, H., and Marche, P.N. (2015). Inflammatory response of endothelial cells to a human endogenous retrovirus associated with multiple sclerosis is mediated by TLR4. Int. Immunol. 27, 545-553.   DOI
81 Escalera-Zamudio, M. and Greenwood, A.D. (2016). On the classification and evolution of endogenous retrovirus: human endogenous retroviruses may not be 'human' after all. APMIS 124, 44-51.   DOI
82 Contreras-Galindo, R., Kaplan, M.H., Leissner, P., Verjat, T., Ferlenghi, I., Bagnoli, F., Giusti, F., Dosik, M.H., Hayes, D.F., Gitlin, S.D., et al. (2008). Human endogenous retrovirus K (HML-2) elements in the plasma of people with lymphoma and breast cancer. J. Virol. 82, 9329-9336.   DOI
83 Contreras-Galindo, R., Lopez, P., Velez, R., and Yamamura, Y. (2007). HIV1 infection increases the expression of human endogenous retroviruses type K (HERV-K) in vitro. AIDS Res. Hum. Retroviruses 23, 116-122.   DOI
84 Zhou, F., Krishnamurthy, J., Wei, Y., Li, M., Hunt, K., Johanning, G.L., Cooper, L.J., and Wang-Johanning, F. (2015). Chimeric antigen receptor T cells targeting HERV-K inhibit breast cancer and its metastasis through downregulation of Ras. Oncoimmunology 4, e1047582.   DOI
85 Saito, T., Mihira, N., Matsuba, Y., Sasaguri, H., Hashimoto, S., Narasimhan, S., Zhang, B., Murayama, S., Higuchi, M., Lee, V.M.Y., et al. (2019). Humanization of the entire murine Mapt gene provides a murine model of pathological human tau propagation. J. Biol. Chem. 294, 12754-12765.   DOI
86 Stengel, S., Fiebig, U., Kurth, R., and Denner, J. (2010). Regulation of human endogenous retrovirus-K expression in melanomas by CpG methylation. Genes Chromosomes Cancer 49, 401-411.   DOI
87 Moon, Y., Moon, R., Roh, H., Chang, S., Lee, S., and Park, H. (2020). HIF-1α-dependent induction of carboxypeptidase A4 and carboxypeptidase E in hypoxic human adipose-derived stem cells. Mol. Cells 43, 945-952.   DOI
88 Yu, X., Zhu, X., Pi, W., Ling, J., Ko, L., Takeda, Y., and Tuan, D. (2005). The long terminal repeat (LTR) of ERV-9 human endogenous retrovirus binds to NF-Y in the assembly of an active LTR enhancer complex NF-Y/MZF1/GATA-2. J. Biol. Chem. 280, 35184-35194.   DOI
89 Mullins, C.S. and Linnebacher, M. (2012). Human endogenous retroviruses and cancer: causality and therapeutic possibilities. World J. Gastroenterol. 18, 6027-6035.   DOI
90 Nakkuntod, J., Sukkapan, P., Avihingsanon, Y., Mutirangura, A., and Hirankarn, N. (2013). DNA methylation of human endogenous retrovirus in systemic lupus erythematosus. J. Hum. Genet. 58, 241-249.   DOI
91 Nellaker, C., Yao, Y., Jones-Brando, L., Mallet, F., Yolken, R.H., and Karlsson, H. (2006). Transactivation of elements in the human endogenous retrovirus W family by viral infection. Retrovirology 3, 44.   DOI
92 Oh, S. and Park, J.T. (2019). Zebrafish model of KRAS-initiated pancreatic endocrine tumor. Anim. Cells Syst. (Seoul) 23, 209-218.   DOI
93 Garson, J.A., Tuke, P.W., Giraud, P., Paranhos-Baccala, G., and Perron, H. (1998). Detection of virion-associated MSRV-RNA in serum of patients with multiple sclerosis. Lancet 351, 33.   DOI
94 Nemes, K. and Fruhwald, M.C. (2018). Emerging therapeutic targets for the treatment of malignant rhabdoid tumors. Expert Opin. Ther. Targets 22, 365-379.   DOI
95 Nguyen, T.D., Davis, J., Eugenio, R.A., and Liu, Y. (2019). Female sex hormones activate human endogenous retrovirus type K through the OCT4 transcription factor in T47D breast cancer cells. AIDS Res. Hum. Retroviruses 35, 348-356.   DOI
96 Ohgaki, H. and Kleihues, P. (2005). Epidemiology and etiology of gliomas. Acta Neuropathol. 109, 93-108.   DOI
97 D'Agati, E., Pitzianti, M., Balestrieri, E., Matteucci, C., Sinibaldi Vallebona, P., and Pasini, A. (2016). First evidence of HERV-H transcriptional activity reduction after methylphenidate treatment in a young boy with ADHD. New Microbiol. 39, 237-239.
98 Dai, L., Del Valle, L., Miley, W., Whitby, D., Ochoa, A.C., Flemington, E.K., and Qin, Z. (2018). Transactivation of human endogenous retrovirus K (HERV-K) by KSHV promotes Kaposi's sarcoma development. Oncogene 37, 4534-4545.   DOI
99 Denne, M., Sauter, M., Armbruester, V., Licht, J.D., Roemer, K., and Mueller-Lantzsch, N. (2007). Physical and functional interactions of human endogenous retrovirus proteins Np9 and rec with the promyelocytic leukemia zinc finger protein. J. Virol. 81, 5607-5616.   DOI
100 Denner, J. (2016). How active are porcine endogenous retroviruses (PERVs)? Viruses 8, 215.   DOI
101 Ono, M., Kawakami, M., and Ushikubo, H. (1987). Stimulation of expression of the human endogenous retrovirus genome by female steroid hormones in human breast cancer cell line T47D. J. Virol. 61, 2059-2062.   DOI
102 Nelson, P.N. (1995). Retroviruses in rheumatic diseases. Ann. Rheum. Dis. 54, 441-442.   DOI
103 Moses, K., Ellis, M.C., and Rubin, G.M. (1989). The glass gene encodes a zinc-finger protein required by Drosophila photoreceptor cells. Nature 340, 531-536.   DOI
104 Okada, M., Ogasawara, H., Kaneko, H., Hishikawa, T., Sekigawa, I., Hashimoto, H., Maruyama, N., Kaneko, Y., and Yamamoto, N. (2002). Role of DNA methylation in transcription of human endogenous retrovirus in the pathogenesis of systemic lupus erythematosus. J. Rheumatol. 29, 1678-1682.
105 Ovejero, T., Sadones, O., Sanchez-Fito, T., Almenar-Perez, E., Espejo, J.A., Martin-Martinez, E., Nathanson, L., and Oltra, E. (2020). Activation of transposable elements in immune cells of fibromyalgia patients. Int. J. Mol. Sci. 21, 1366.   DOI
106 Padmanabhan Nair, V., Liu, H., Ciceri, G., Jungverdorben, J., Frishman, G., Tchieu, J., Cederquist, G.Y., Rothenaigner, I., Schorpp, K., Klepper, L., et al. (2021). Activation of HERV-K(HML-2) disrupts cortical patterning and neuronal differentiation by increasing NTRK3. Cell Stem Cell 28, 1566-1581.e8.   DOI
107 Perron, H., Hamdani, N., Faucard, R., Lajnef, M., Jamain, S., DabanHuard, C., Sarrazin, S., LeGuen, E., Houenou, J., Delavest, M., et al. (2012). Molecular characteristics of Human Endogenous Retrovirus type-W in schizophrenia and bipolar disorder. Transl. Psychiatry 2, e201.   DOI
108 Dhakal, S. and Lee, Y. (2019). Transient receptor potential channels and metabolism. Mol. Cells 42, 569-578.   DOI
109 Depil, S., Roche, C., Dussart, P., and Prin, L. (2002). Expression of a human endogenous retrovirus, HERV-K, in the blood cells of leukemia patients. Leukemia 16, 254-259.   DOI
110 Dewannieux, M. and Heidmann, T. (2013). Endogenous retroviruses: acquisition, amplification and taming of genome invaders. Curr. Opin. Virol. 3, 646-656.   DOI
111 Dolci, M., Favero, C., Tarantini, L., Villani, S., Bregni, M., Signorini, L., Della Valle, A., Crivelli, F., D'Alessandro, S., Ferrante, P., et al. (2020). Human endogenous retroviruses env gene expression and long terminal repeat methylation in colorectal cancer patients. Med. Microbiol. Immunol. 209, 189-199.   DOI
112 Lee, W., Mariappan, R., De, K., and Ohn, T. (2021b). Loss of MeCP2 causes subtle alteration in dendritic arborization of retinal ganglion cells. Anim. Cells Syst. (Seoul) 25, 102-109.   DOI
113 Lee, Y., Kang, H., Jin, C., Zhang, Y., Kim, Y., and Han, K. (2019b). Transcriptome analyses suggest minimal effects of Shank3 dosage on directional gene expression changes in the mouse striatum. Anim. Cells Syst. (Seoul) 23, 270-274.   DOI
114 Li, M., Radvanyi, L., Yin, B., Rycaj, K., Li, J., Chivukula, R., Lin, K., Lu, Y., Shen, J., Chang, D.Z., et al. (2017). Downregulation of human endogenous retrovirus type K (HERV-K) viral env RNA in pancreatic cancer cells decreases cell proliferation and tumor growth. Clin. Cancer Res. 23, 5892-5911.   DOI
115 Li, S., Liu, Z.C., Yin, S.J., Chen, Y.T., Yu, H.L., Zeng, J., Zhang, Q., and Zhu, F. (2013). Human endogenous retrovirus W family envelope gene activates the small conductance Ca2+-activated K+ channel in human neuroblastoma cells through CREB. Neuroscience 247, 164-174.   DOI
116 Mager, D.L. and Medstrand, P. (2005). Retroviral repeat sequences. eLS 2005 Sep 23. https://doi.org/10.1038/npg.els.0005062   DOI
117 Pi, W., Yang, Z., Wang, J., Ruan, L., Yu, X., Ling, J., Krantz, S., Isales, C., Conway, S.J., Lin, S., et al. (2004). The LTR enhancer of ERV-9 human endogenous retrovirus is active in oocytes and progenitor cells in transgenic zebrafish and humans. Proc. Natl. Acad. Sci. U. S. A. 101, 805-810.   DOI
118 Quelle, D.E., Zindy, F., Ashmun, R.A., and Sherr, C.J. (1995). Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest. Cell 83, 993-1000.   DOI
119 Lee, S.H. and Kim, E.Y. (2021). Short-term maintenance on a high-sucrose diet alleviates aging-induced sleep fragmentation in drosophila. Anim. Cells Syst. (Seoul) 2021 Nov 3 [Epub]. https://doi.org/10.1080/19768354.2021.1997801   DOI
120 Li, Z., Sheng, T., Wan, X., Liu, T., Wu, H., and Dong, J. (2010). Expression of HERV-K correlates with status of MEK-ERK and p16INK4A-CDK4 pathways in melanoma cells. Cancer Invest. 28, 1031-1037.   DOI
121 Conti, A., Rota, F., Ragni, E., Favero, C., Motta, V., Lazzari, L., Bollati, V., Fustinoni, S., and Dieci, G. (2016). Hydroquinone induces DNA hypomethylation-independent overexpression of retroelements in human leukemia and hematopoietic stem cells. Biochem. Biophys. Res. Commun. 474, 691-695.   DOI
122 Martin, M.A., Bryan, T., Rasheed, S., and Khan, A.S. (1981). Identification and cloning of endogenous retroviral sequences present in human DNA. Proc. Natl. Acad. Sci. U. S. A. 78, 4892-4896.   DOI
123 Ostrom, Q.T., Gittleman, H., Fulop, J., Liu, M., Blanda, R., Kromer, C., Wolinsky, Y., Kruchko, C., and Barnholtz-Sloan, J.S. (2015). CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2008-2012. Neuro Oncol. 17 Suppl 4, iv1-iv62.   DOI
124 Attig, J., Young, G.R., Hosie, L., Perkins, D., Encheva-Yokoya, V., Stoye, J.P., Snijders, A.P., Ternette, N., and Kassiotis, G. (2019). LTR retroelement expansion of the human cancer transcriptome and immunopeptidome revealed by de novo transcript assembly. Genome Res. 29, 1578-1590.   DOI
125 Rimal, S., Sang, J., Dhakal, S., and Lee, Y. (2020). Cucurbitacin B activates bitter-sensing gustatory receptor neurons via gustatory receptor 33a in Drosophila melanogaster. Mol. Cells 43, 530-538.   DOI
126 Rodriguez-Pinto, I., Agmon-Levin, N., Howard, A., and Shoenfeld, Y. (2014). Fibromyalgia and cytokines. Immunol. Lett. 161, 200-203.   DOI
127 Romao, M., Peracoli, J.C., Bannwart-Castro, C.F., Medeiros, L.T., Weel, I.C., Borges, V.T., Golim, M.A., and Peracoli, M.T. (2012). PP063. TLR4 expression and pro-inflammatory cytokine production by peripheral blood monocytes from preeclamptic women. Pregnancy Hypertens. 2, 276.
128 Balestrieri, E., Minutolo, A., Petrone, V., Fanelli, M., Iannetta, M., Malagnino, V., Zordan, M., Vitale, P., Charvet, B., Horvat, B., et al. (2021). Evidence of the pathogenic HERV-W envelope expression in T lymphocytes in association with the respiratory outcome of COVID-19 patients. EBioMedicine 66, 103341.   DOI
129 Anand, D., Colpo, G.D., Zeni, G., Zeni, C.P., and Teixeira, A.L. (2017). Attention-deficit/hyperactivity disorder and inflammation: what does current knowledge tell us? A systematic review. Front. Psychiatry 8, 228.
130 Schanab, O., Humer, J., Gleiss, A., Mikula, M., Sturlan, S., Grunt, S., Okamoto, I., Muster, T., Pehamberger, H., and Waltenberger, A. (2011). Expression of human endogenous retrovirus K is stimulated by ultraviolet radiation in melanoma. Pigment Cell Melanoma Res. 24, 656-665.   DOI
131 Serafino, A., Balestrieri, E., Pierimarchi, P., Matteucci, C., Moroni, G., Oricchio, E., Rasi, G., Mastino, A., Spadafora, C., Garaci, E., et al. (2009). The activation of human endogenous retrovirus K (HERV-K) is implicated in melanoma cell malignant transformation. Exp. Cell Res. 315, 849-862.   DOI
132 Siebenthall, K.T., Miller, C.P., Vierstra, J.D., Mathieu, J., Tretiakova, M., Reynolds, A., Sandstrom, R., Rynes, E., Haugen, E., Johnson, A., et al. (2019). Integrated epigenomic profiling reveals endogenous retrovirus reactivation in renal cell carcinoma. EBioMedicine 41, 427-442.   DOI
133 Rasmussen, H.B., Geny, C., Deforges, L., Perron, H., Tourtelotte, W., Heltberg, A., and Clausen, J. (1995). Expression of endogenous retroviruses in blood mononuclear cells and brain tissue from multiple sclerosis patients. Mult. Scler. 1, 82-87.   DOI
134 Sutkowski, N., Chen, G., Calderon, G., and Huber, B.T. (2004). Epstein-Barr virus latent membrane protein LMP-2A is sufficient for transactivation of the human endogenous retrovirus HERV-K18 superantigen. J. Virol. 78, 7852-7860.   DOI
135 Wang, M., Qiu, Y., Liu, H., Liang, B., Fan, B., Zhou, X., and Liu, D. (2020a). Transcription profile of human endogenous retroviruses in response to dengue virus serotype 2 infection. Virology 544, 21-30.   DOI
136 Hohn, O., Hanke, K., and Bannert, N. (2013). HERV-K(HML-2), the best preserved family of HERVs: endogenization, expression, and implications in health and disease. Front. Oncol. 3, 246.
137 Jung, G.T., Kim, K.P., and Kim, K. (2020a). How to interpret and integrate multi-omics data at systems level. Anim. Cells Syst. (Seoul) 24, 1-7.   DOI
138 Kim, S.H., Jung, H., Ahnn, J., and Lee, S.K. (2019). Calcineurin tax-6 regulates male ray development and counteracts with kin-29 kinase in Caenorhabditis elegans. Anim. Cells Syst. (Seoul) 23, 399-406.   DOI
139 Wang, X., Zhao, C., Zhang, C., Mei, X., Song, J., Sun, Y., Wu, Z., and Shi, W. (2019). Increased HERV-E clone 4-1 expression contributes to DNA hypomethylation and IL-17 release from CD4(+) T cells via miR-302d/MBD2 in systemic lupus erythematosus. Cell Commun. Signal. 17, 94.   DOI
140 Chen, T., Meng, Z., Gan, Y., Wang, X., Xu, F., Gu, Y., Xu, X., Tang, J., Zhou, H., Zhang, X., et al. (2013). The viral oncogene Np9 acts as a critical molecular switch for co-activating β-catenin, ERK, Akt and Notch1 and promoting the growth of human leukemia stem/progenitor cells. Leukemia 27, 1469-1478.   DOI
141 Balestrieri, E., Arpino, C., Matteucci, C., Sorrentino, R., Pica, F., Alessandrelli, R., Coniglio, A., Curatolo, P., Rezza, G., Macciardi, F., et al. (2012). HERVs expression in autism spectrum disorders. Plos One 7, e48831.   DOI
142 Reiche, J., Pauli, G., and Ellerbrok, H. (2010). Differential expression of human endogenous retrovirus K transcripts in primary human melanocytes and melanoma cell lines after UV irradiation. Melanoma Res. 20, 435-440.   DOI
143 Madeira, A., Burgelin, I., Perron, H., Curtin, F., Lang, A.B., and Faucard, R. (2016). MSRV envelope protein is a potent, endogenous and pathogenic agonist of human toll-like receptor 4: relevance of GNbAC1 in multiple sclerosis treatment. J. Neuroimmunol. 291, 29-38.   DOI
144 Balestrieri, E., Cipriani, C., Matteucci, C., Benvenuto, A., Coniglio, A., ArgawDenboba, A., Toschi, N., Bucci, I., Miele, M.T., Grelli, S., et al. (2019). Children with autism spectrum disorder and their mothers share abnormal expression of selected endogenous retroviruses families and cytokines. Front. Immunol. 10, 2244.   DOI
145 Bae, S., Kim, M.K., Kim, H.S., and Moon, Y.A. (2020). Arachidonic acid induces ER stress and apoptosis in HT-29 human colon cancer cells. Anim. Cells Syst. (Seoul) 24, 260-266.   DOI
146 Payer, B., Saitou, M., Barton, S.C., Thresher, R., Dixon, J.P., Zahn, D., Colledge, W.H., Carlton, M.B., Nakano, T., and Surani, M.A. (2003). Stella is a maternal effect gene required for normal early development in mice. Curr. Biol. 13, 2110-2117.   DOI
147 Perron, H., Mekaoui, L., Bernard, C., Veas, F., Stefas, I., and Leboyer, M. (2008). Endogenous retrovirus type W GAG and envelope protein antigenemia in serum of schizophrenic patients. Biol. Psychiatry 64, 1019-1023.   DOI
148 Ko, E.J., Song, K.S., Ock, M.S., Choi, Y.H., Kim, S., Kim, H.S., and Cha, H.J. (2021b). Expression profiles of human endogenous retrovirus (HERV)-K and HERV-R Env proteins in various cancers. BMB Rep. 54, 368-373.   DOI
149 Kannan, P., Buettner, R., Pratt, D.R., and Tainsky, M.A. (1991). Identification of a retinoic acid-inducible endogenous retroviral transcript in the human teratocarcinoma-derived cell line PA-1. J. Virol. 65, 6343-6348.   DOI
150 Rajagopalan, D., Tirado-Magallanes, R., Bhatia, S.S., Teo, W.S., Sian, S., Hora, S., Lee, K.K., Zhang, Y., Jadhav, S.P., Wu, Y., et al. (2018). TIP60 represses activation of endogenous retroviral elements. Nucleic Acids Res. 46, 9456-9470.   DOI
151 Santoni, F.A., Guerra, J., and Luban, J. (2012). HERV-H RNA is abundant in human embryonic stem cells and a precise marker for pluripotency. Retrovirology 9, 111.   DOI
152 Shah, M. and Woo, H.G. (2021). Molecular perspectives of SARS-CoV-2: pathology, immune evasion, and therapeutic interventions. Mol. Cells 44, 408-421.   DOI
153 Strick, R., Ackermann, S., Langbein, M., Swiatek, J., Schubert, S.W., Hashemolhosseini, S., Koscheck, T., Fasching, P.A., Schild, R.L., Beckmann, M.W., et al. (2007). Proliferation and cell-cell fusion of endometrial carcinoma are induced by the human endogenous retroviral Syncytin-1 and regulated by TGF-beta. J. Mol. Med. (Berl.) 85, 23-38.   DOI
154 Zhou, F., Li, M., Wei, Y., Lin, K., Lu, Y., Shen, J., Johanning, G.L., and Wang-Johanning, F. (2016). Activation of HERV-K Env protein is essential for tumorigenesis and metastasis of breast cancer cells. Oncotarget 7, 84093-84117.   DOI
155 Perron, H., Dougier-Reynaud, H.L., Lomparski, C., Popa, I., Firouzi, R., Bertrand, J.B., Marusic, S., Portoukalian, J., Jouvin-Marche, E., Villiers, C.L., et al. (2013). Human endogenous retrovirus protein activates innate immunity and promotes experimental allergic encephalomyelitis in mice. Plos One 8, e80128.   DOI
156 Ramsoondar, J., Vaught, T., Ball, S., Mendicino, M., Monahan, J., Jobst, P., Vance, A., Duncan, J., Wells, K., and Ayares, D. (2009). Production of transgenic pigs that express porcine endogenous retrovirus small interfering RNAs. Xenotransplantation 16, 164-180.   DOI
157 Krug, L., Chatterjee, N., Borges-Monroy, R., Hearn, S., Liao, W.W., Morrill, K., Prazak, L., Rozhkov, N., Theodorou, D., Hammell, M., et al. (2017). Retrotransposon activation contributes to neurodegeneration in a Drosophila TDP-43 model of ALS. PLoS Genet. 13, e1006635.   DOI
158 Lee, W.C., Kim, D.Y., Kim, M.J., Lee, H.J., Bharti, D., Lee, S.H., Kang, Y.H., Rho, G.J., and Jeon, B.G. (2019a). Delay of cell growth and loss of stemness by inhibition of reverse transcription in human mesenchymal stem cells derived from dental tissue. Anim. Cells Syst. (Seoul) 23, 335-345.   DOI
159 Zhang, Y., Kang, H.R., and Han, K. (2019a). Differential cell-type-expression of CYFIP1 and CYFIP2 in the adult mouse hippocampus. Anim. Cells Syst. (Seoul) 23, 380-383.   DOI
160 Zhou, Z., Li, X., Liu, Z., Huang, L., Yao, Y., Li, L., Chen, J., Zhang, R., Zhou, J., Wang, L., et al. (2020). A bromodomain-containing protein 4 (BRD4) inhibitor suppresses angiogenesis by regulating AP-1 expression. Front. Pharmacol. 11, 1043.   DOI
161 Zhang, Y., Li, T., Preissl, S., Amaral, M.L., Grinstein, J.D., Farah, E.N., Destici, E., Qiu, Y., Hu, R., Lee, A.Y., et al. (2019b). Transcriptionally active HERV-H retrotransposons demarcate topologically associating domains in human pluripotent stem cells. Nat. Genet. 51, 1380-1388.   DOI
162 Buckner, J.C., Brown, P.D., O'Neill, B.P., Meyer, F.B., Wetmore, C.J., and Uhm, J.H. (2007). Central nervous system tumors. Mayo Clin. Proc. 82, 1271-1286.   DOI
163 Tie, C.H., Fernandes, L., Conde, L., Robbez-Masson, L., Sumner, R.P., Peacock, T., Rodriguez-Plata, M.T., Mickute, G., Gifford, R., Towers, G.J., et al. (2018). KAP1 regulates endogenous retroviruses in adult human cells and contributes to innate immune control. EMBO Rep. 19, e45000.   DOI
164 Bartkowska, K., Paquin, A., Gauthier, A.S., Kaplan, D.R., and Miller, F.D. (2007). Trk signaling regulates neural precursor cell proliferation and differentiation during cortical development. Development 134, 4369-4380.   DOI
165 Blomberg, J., Nived, O., Pipkorn, R., Bengtsson, A., Erlinge, D., and Sturfelt, G. (1994). Increased antiretroviral antibody reactivity in sera from a defined population of patients with systemic lupus erythematosus. Arthritis Rheum. 37, 57-66.   DOI
166 Karimi, A., Sheervalilou, R., and Kahroba, H. (2019). A new insight on activation of human endogenous retroviruses (HERVs) in malignant melanoma upon exposure to CuSO4. Biol. Trace Elem. Res. 191, 70-74.   DOI
167 Karlsson, H., Schroder, J., Bachmann, S., Bottmer, C., and Yolken, R.H. (2004). HERV-W-related RNA detected in plasma from individuals with recent-onset schizophrenia or schizoaffective disorder. Mol. Psychiatry 9, 12-13.   DOI
168 Kassiotis, G. (2014). Endogenous retroviruses and the development of cancer. J. Immunol. 192, 1343-1349.   DOI
169 Ahmed, M.B., Islam, S.U., and Lee, Y.S. (2020). Decursin negatively regulates LPS-induced upregulation of the TLR4 and JNK signaling stimulated by the expression of PRP4 in vitro. Anim. Cells Syst. (Seoul) 24, 44-52.   DOI
170 Lee, G.Y., Sohn, J., and Lee, S.J.V. (2021a). Combinatorial approach using Caenorhabditis elegans and mammalian systems for aging research. Mol. Cells 44, 425-432.   DOI
171 Mameli, G., Erre, G.L., Caggiu, E., Mura, S., Cossu, D., Bo, M., Cadoni, M.L., Piras, A., Mundula, N., Colombo, E., et al. (2017). Identification of a HERV-K env surface peptide highly recognized in Rheumatoid Arthritis (RA) patients: a cross-sectional case-control study. Clin. Exp. Immunol. 189, 127-131.   DOI
172 Rolland, A., Jouvin-Marche, E., Viret, C., Faure, M., Perron, H., and Marche, P.N. (2006). The envelope protein of a human endogenous retrovirus-W family activates innate immunity through CD14/TLR4 and promotes Th1-like responses. J. Immunol. 176, 7636-7644.   DOI
173 Tanaka, S., Ikeda, H., Otsuka, N., Yamamoto, Y., Sugaya, T., and Yoshiki, T. (2003). Tissue specific high level expression of a full length human endogenous retrovirus genome transgene, HERV-R, under control of its own promoter in rats. Transgenic Res. 12, 319-328.   DOI
174 Walsh, N.C., Kenney, L.L., Jangalwe, S., Aryee, K.E., Greiner, D.L., Brehm, M.A., and Shultz, L.D. (2017). Humanized mouse models of clinical disease. Annu. Rev. Pathol. 12, 187-215.   DOI
175 Balada, E., Ordi-Ros, J., and Vilardell-Tarres, M. (2009). Molecular mechanisms mediated by human endogenous retroviruses (HERVs) in autoimmunity. Rev. Med. Virol. 19, 273-286.   DOI
176 Bergallo, M., Galliano, I., Montanari, P., Gambarino, S., Mareschi, K., Ferro, F., Fagioli, F., Tovo, P.A., and Ravanini, P. (2015). CMV induces HERV-K and HERV-W expression in kidney transplant recipients. J. Clin. Virol. 68, 28-31.   DOI
177 Casau, A.E., Vaughan, J.E., Lozano, G., and Levine, A.J. (1999). Germ cell expression of an isolated human endogenous retroviral long terminal repeat of the HERV-K/HTDV family in transgenic mice. J. Virol. 73, 9976-9983.   DOI
178 Cherkasova, E., Malinzak, E., Rao, S., Takahashi, Y., Senchenko, V.N., Kudryavtseva, A.V., Nickerson, M.L., Merino, M., Hong, J.A., Schrump, D.S., et al. (2011). Inactivation of the von Hippel-Lindau tumor suppressor leads to selective expression of a human endogenous retrovirus in kidney cancer. Oncogene 30, 4697-4706.   DOI
179 Chen-Plotkin, A.S., Lee, V.M.Y., and Trojanowski, J.Q. (2010). TAR DNA-binding protein 43 in neurodegenerative disease. Nat. Rev. Neurol. 6, 211-220.   DOI
180 Brodziak, A., Ziolko, E., Muc-Wierzgon, M., Nowakowska-Zajdel, E., Kokot, T., and Klakla, K. (2012). The role of human endogenous retroviruses in the pathogenesis of autoimmune diseases. Med. Sci. Monit. 18, RA80-RA88.
181 Chan, S.M., Sapir, T., Park, S.S., Rual, J.F., Contreras-Galindo, R., Reiner, O., and Markovitz, D.M. (2019). The HERV-K accessory protein Np9 controls viability and migration of teratocarcinoma cells. Plos One 14, e0212970.   DOI
182 Chen, Y., Yan, Q., Zhou, P., Li, S., and Zhu, F. (2019). HERV-W env regulates calcium influx via activating TRPC3 channel together with depressing DISC1 in human neuroblastoma cells. J. Neurovirol. 25, 101-113.   DOI
183 Lee, Y., Lee, M., Lee, S.W., Choi, N.Y., Ham, S., Lee, H.J., Ko, K., and Ko, K. (2019c). Reprogramming of spermatogonial stem cells into pluripotent stem cells in the spheroidal state. Anim. Cells Syst. (Seoul) 23, 392-398.   DOI
184 Lee, H.E., Park, S.J., Huh, J.W., Imai, H., and Kim, H.S. (2020a). Enhancer function of microRNA-3681 derived from long terminal repeats represses the activity of variable number tandem repeats in the 3' UTR of SHISA7. Mol. Cells 43, 607-618.   DOI
185 Lee, W.J., Kwun, H.J., Kim, H.S., and Jang, K.L. (2003). Activation of the human endogenous retrovirus W long terminal repeat by herpes simplex virus type 1 immediate early protein 1. Mol. Cells 15, 75-80.
186 Lee, Y., Kim, D., and Lee, C.J. (2020c). Suppressive effects of valproic acid on caudal fin regeneration in adult zebrafish. Anim. Cells Syst. (Seoul) 24, 349-358.   DOI
187 Levet, S., Medina, J., Joanou, J., Demolder, A., Queruel, N., Reant, K., Normand, M., Seffals, M., Dimier, J., Germi, R., et al. (2017). An ancestral retroviral protein identified as a therapeutic target in type-1 diabetes. JCI Insight 2, e94387.   DOI
188 Lamprecht, B., Walter, K., Kreher, S., Kumar, R., Hummel, M., Lenze, D., Kochert, K., Bouhlel, M.A., Richter, J., Soler, E., et al. (2010). Derepression of an endogenous long terminal repeat activates the CSF1R proto-oncogene in human lymphoma. Nat. Med. 16, 571-579, 1p following 579.   DOI
189 Antony, J.M., DesLauriers, A.M., Bhat, R.K., Ellestad, K.K., and Power, C. (2011). Human endogenous retroviruses and multiple sclerosis: innocent bystanders or disease determinants? Biochim. Biophys. Acta 1812, 162-176.   DOI
190 Brattas, P.L., Jonsson, M.E., Fasching, L., Nelander Wahlestedt, J., Shahsavani, M., Falk, R., Falk, A., Jern, P., Parmar, M., and Jakobsson, J. (2017). TRIM28 controls a gene regulatory network based on endogenous retroviruses in human neural progenitor cells. Cell Rep. 18, 1-11.   DOI
191 Gabriel, U., Steidler, A., Trojan, L., Michel, M.S., Seifarth, W., and Fabarius, A. (2010). Smoking increases transcription of human endogenous retroviruses in a newly established in vitro cell model and in normal urothelium. AIDS Res. Hum. Retroviruses 26, 883-888.   DOI
192 Garcia-Montojo, M. and Nath, A. (2021). HERV-W envelope expression in blood leukocytes as a marker of disease severity of COVID-19. EBioMedicine 67, 103363.   DOI
193 Gimenez-Orenga, K. and Oltra, E. (2021). Human endogenous retrovirus as therapeutic targets in neurologic disease. Pharmaceuticals (Basel) 14, 495.   DOI
194 Goering, W., Ribarska, T., and Schulz, W.A. (2011). Selective changes of retroelement expression in human prostate cancer. Carcinogenesis 32, 1484-1492.   DOI
195 Griffiths, D.J. (2001). Endogenous retroviruses in the human genome sequence. Genome Biol. 2, REVIEWS1017.   DOI
196 Groger, V., Emmer, A., Staege, M.S., and Cynis, H. (2021). Endogenous retroviruses in nervous system disorders. Pharmaceuticals (Basel) 14, 70.   DOI
197 Zhou, Y., Liu, L., Liu, Y., Zhou, P., Yan, Q., Yu, H., Chen, X., and Zhu, F. (2021). Implication of human endogenous retrovirus W family envelope in hepatocellular carcinoma promotes MEK/ERK-mediated metastatic invasiveness and doxorubicin resistance. Cell Death Discov. 7, 177.   DOI
198 Cipriani, C., Pitzianti, M.B., Matteucci, C., D'Agati, E., Miele, M.T., Rapaccini, V., Grelli, S., Curatolo, P., Sinibaldi-Vallebona, P., Pasini, A., et al. (2018). The decrease in human endogenous retrovirus-H activity runs in parallel with improvement in ADHD symptoms in patients undergoing methylphenidate therapy. Int. J. Mol. Sci. 19, 3286.   DOI
199 Cho, H., Jang, Y., Park, K.H., Choi, H., Nowakowska, A., Lee, H.J., Kim, M., Kang, M.H., Kim, J.H., Shin, H.Y., et al. (2021). Human endogenous retrovirus-enveloped baculoviral DNA vaccines against MERS-CoV and SARS-CoV2. NPJ Vaccines 6, 37.   DOI
200 Choe, S., Huh, T.L., and Rhee, M. (2020). Trim45 is essential to the development of the diencephalon and eye in zebrafish embryos. Anim. Cells Syst. (Seoul) 24, 99-106.   DOI
201 Dechaumes, A., Bertin, A., Sane, F., Levet, S., Varghese, J., Charvet, B., Gmyr, V., Kerr-Conte, J., Pierquin, J., Arunkumar, G., et al. (2020). Coxsackievirus-B4 infection can induce the expression of human endogenous retrovirus W in primary cells. Microorganisms 8, 1335.   DOI
202 Dinsmore, J.H. and Solomon, F. (1991). Inhibition of MAP2 expression affects both morphological and cell division phenotypes of neuronal differentiation. Cell 64, 817-826.   DOI
203 Etchberger, J.F., Lorch, A., Sleumer, M.C., Zapf, R., Jones, S.J., Marra, M.A., Holt, R.A., Moerman, D.G., and Hobert, O. (2007). The molecular signature and cis-regulatory architecture of a C. elegans gustatory neuron. Genes Dev. 21, 1653-1674.   DOI
204 Tovo, P.A., Garazzino, S., Dapra, V., Pruccoli, G., Calvi, C., Mignone, F., Alliaudi, C., Denina, M., Scolfaro, C., Zoppo, M., et al. (2021). COVID-19 in children: expressions of type I/II/III interferons, TRIM28, SETDB1, and endogenous retroviruses in mild and severe cases. Int. J. Mol. Sci. 22, 7481.   DOI