Human endogenous retrovirus-K contributes to motor neuron disease

Science Translational Medicine

Volumn 7, Issue 307, 2015, Pages

  Li, Wenxue ^a   Lee, Myoung Hwa ^a   Henderson, Lisa ^a   Tyagi, Richa ^a   Bachani, Muzna ^a   Steiner, Joseph ^a   Campanac, Emilie ^b   Hoffman, Dax A ^b   Geldern, Gloria Von ^a   Johnson, Kory ^a   Maric, Dragan ^a   Morris, H Douglas ^a   Lentz, Margaret ^c   Pak, Katherine ^d   Mammen, Andrew ^d   Ostrow, Lyle ^e   Rothstein, Jeffrey ^e   Nath, Avindra ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c National Institute of Allergy and Infectious Disease   (United States)

^d NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; VIRUS ENVELOPE PROTEIN; PROTEIN TDP-43;

AMYOTROPHIC LATERAL SCLEROSIS; ANTERIOR HORN CELL; ARTICLE; AUTOPSY; BRAIN TISSUE; CINGULATE GYRUS; CONFOCAL MICROSCOPY; CORPUS CALLOSUM; DENDRITIC SPINE; DENERVATION; DNA DAMAGE; ENDOGENOUS RETROVIRUS; FLUORESCENCE MICROSCOPY; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LONG TERMINAL REPEAT; MOTOR CORTEX; MOTOR DYSFUNCTION; MOTOR NEURON DISEASE; MUSCLE ATROPHY; NERVE DEGENERATION; NEURITE; NEUROTOXICITY; NONHUMAN; PATHOGENESIS; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; REINNERVATION; RNA SEQUENCE; TRANSGENIC ANIMAL; TRANSGENIC MOUSE; VIRUS GENOME; ANIMAL; ANIMAL BEHAVIOR; BINDING SITE; BRAIN; GENETICS; METABOLISM; MOTONEURON; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; PHYSIOLOGY; VIROLOGY; VIRUS ACTIVATION;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BEHAVIOR, ANIMAL; BINDING SITES; BRAIN; DNA-BINDING PROTEINS; ENDOGENOUS RETROVIRUSES; HUMANS; MICE, TRANSGENIC; MOTOR NEURON DISEASE; MOTOR NEURONS; NERVE DEGENERATION; PHENOTYPE; TERMINAL REPEAT SEQUENCES; VIRUS ACTIVATION;

EID: 84942938334     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aac8201     Document Type: Article

References (48)

1. J. F. Hughes, J. M. Coffin, A novel endogenous retrovirus-related element in the human genome resembles a DNA transposon: Evidence for an evolutionary link? Genomics 80, 453-455 (2002).
2. R. P. Subramanian, J. H. Wildschutte, C. Russo, J. M. Coffin, Identification, characterization, and comparative genomic distribution of the HERV-K (HML-2) group of human endogenous retroviruses. Retrovirology 8, 90 (2011).
3. R. Douville, J. Liu, J. Rothstein, A. Nath, Identification of active loci of a human endogenous retrovirus in neurons of patients with amyotrophic lateral sclerosis. Ann. Neurol. 69, 141-151 (2011).
4. D. J. L. MacGowan, S. N. Scelsa, T. E. Imperato, K.-N. Liu, P. Baron, B. Polsky, A controlled study of reverse transcriptase in serum and CSF of HIV-negative patients with ALS. Neurology 68, 1944-1946 (2007).
5. A. L. McCormick, R. H. Brown Jr., M. E. Cudkowicz, A. Al-Chalabi, J. A. Garson, Quantification of reverse transcriptase in ALS and elimination of a novel retroviral candidate. Neurology 70, 278-283 (2008).
6. A. J. Steele, A. Al-Chalabi, K. Ferrante, M. E. Cudkowicz, R. H. Brown Jr., J. A. Garson, Detection of serum reverse transcriptase activity in patients with ALS and unaffected blood relatives. Neurology 64, 454-458 (2005).
7. W. D. Andrews, P. W. Tuke, A. Al-Chalabi, P. Gaudin, S. Ijaz, M. J. Parton, J. A. Garson, Detection of reverse transcriptase activity in the serum of patients with motor neurone disease. J. Med. Virol. 61, 527-532 (2000).
8. M. V. Viola, M. Frazier, L. White, J. Brody, S. Spiegelman, RNA-instructed DNA polymerase activity in a cytoplasmic particulate fraction in brains from Guamanian patients. J. Exp. Med. 142, 483-494 (1975).
9. T. Alfahad, A. Nath, Retroviruses and amyotrophic lateral sclerosis. Antiviral Res. 99, 180-187 (2013).
10. P. Horvath, R. Barrangou, CRISPR/Cas, the immune system of bacteria and archaea. Science 327, 167-170 (2010).
11. P. Mali, K. M. Esvelt, G. M. Church, Cas9 as a versatile tool for engineering biology. Nat. Methods 10, 957-963 (2013).
12. T. V. Pospelova, Z. N. Demidenko, E. I. Bukreeva, V. A. Pospelov, A. V. Gudkov, M. V. Blagosklonny, Pseudo-DNA damage response in senescent cells. Cell Cycle 8, 4112-4118 (2009).
13. J. A. Pfister, S. R. D'Mello, Insights into the regulation of neuronal viability by nucleophosmin/B23. Exp. Biol. Med. 240, 774-786 (2015).
14. L. E. Kerr, J.-L. Birse-Archbold, D.M. Short, A. L. McGregor, I.Heron, D. C.MacDonald, J. Thompson, G. J. Carlson, J. S. Kelly, J. McCulloch, J. Sharkey, Nucleophosmin is a novel Bax chaperone that regulates apoptotic cell death. Oncogene 26, 2554-2562 (2007).
15. S.-H. I. Ou, F. Wu, D. Harrich, L. F. García-Martínez, R. B. Gaynor, Cloning and characterization of a novel cellular protein, TDP-43, that binds to human immunodeficiency virus type 1 TAR DNA sequence motifs. J. Virol. 69, 3584-3596 (1995).
16. W. Li, Y. Jin, L. Prazak, M. Hammell, J. Dubnau, Transposable elements in TDP-43-mediated neurodegenerative disorders. PLOS One 7, e44099 (2012).
17. M. J. Gonzalez-Hernandez, M. D. Swanson, R. Contreras-Galindo, S. Cookinham, S. R. King, R. J. Noel Jr., M. H. Kaplan, D. M. Markovitz, Expression of human endogenous retrovirus type K (HML-2) is activated by the Tat protein of HIV-1. J. Virol. 86, 7790-7805 (2012).
18. J. Finsterer, J.-M. Burgunder, Recent progress in the genetics of motor neuron disease. Eur. J. Med. Genet. 57, 103-112 (2014).
19. F. Osakada, E. M. Callaway, Design and generation of recombinant rabies virus vectors. Nat. Protoc. 8, 1583-1601 (2013).
20. R. K. Bhat, W. Rudnick, J. M. Antony, F. Maingat, K. K. Ellestad, B. M. Wheatley, R. R. Tönjes, C. Power, Human endogenous retrovirus-K(II) envelope induction protects neurons during HIV/AIDS. PLOS One 9, e97984 (2014).
21. S. Fischer, N. Echeverria, G. Moratorio, A. I. Landoni, G. Dighiero, J. Cristina, P. Oppezzo, P. Moreno, Human endogenous retrovirus np9 gene is over expressed in chronic lymphocytic leukemia patients. Leuk. Res. Rep. 3, 70-72 (2014).
22. M. E. Gurney, H. Pu, A. Y. Chiu, M. C. Dal Canto, C. Y. Polchow, D. D. Alexander, J. Caliendo, A. Hentati, Y. W. Kwon, H. X. Deng, et al., Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 264, 1772-1775 (1994).
23. M. Okuwaki, The structure and functions of NPM1/Nucleophsmin/B23, a multifunctional nucleolar acidic protein. J. Biochem. 143, 441-448 (2008).
24. K. Murano, M. Okuwaki, M. Hisaoka, K. Nagata, Transcription regulation of the rRNA gene by a multifunctional nucleolar protein, B23/nucleophosmin, through its histone chaperone activity. Mol. Cell. Biol. 28, 3114-3126 (2008).
25. A. R. Haeusler, C. J. Donnelly, G. Periz, E. A. J. Simko, P. G. Shaw, M.-S. Kim, N. J. Maragakis, J. C. Troncoso, A. Pandey, R. Sattler, J. D. Rothstein, J. Wang, C9orf72 nucleotide repeat structures initiate molecular cascades of disease. Nature 507, 195-200 (2014).
26. L. DesGroseillers, M. Barrette, P. Jolicoeur, Physical mapping of the paralysis-inducing determinant of a wild mouse ecotropic neurotropic retrovirus. J. Virol. 52, 356-363 (1984).
27. Y. Paquette, Z. Hanna, P. Savard, R. Brousseau, Y. Robitaille, P. Jolicoeur, Retrovirus-induced murine motor neuron disease: Mapping the determinant of spongiform degeneration within the envelope gene. Proc. Natl. Acad. Sci. U.S.A. 86, 3896-3900 (1989).
28. D. E. Dimcheff, L. G. Volkert, Y. Li, A. L. DeLucia, W. P. Lynch, Gene expression profiling of microglia infected by a highly neurovirulent murine leukemia virus: Implications for neuropathogenesis. Retrovirology 3, 26 (2006).
29. M. Kaul, S. A. Lipton, Mechanisms of neuronal injury and death in HIV-1 associated dementia. Curr. HIV Res. 4, 307-318 (2006).
30. W. Li, G. Li, J. Steiner, A. Nath, Role of Tat protein in HIV neuropathogenesis. Neurotox. Res. 16, 205-220 (2009).
31. T. J. Cohen, V. M. Y. Lee, J. Q. Trojanowski, TDP-43 functions and pathogenic mechanisms implicated in TDP-43 proteinopathies. Trends Mol. Med. 17, 659-667 (2011).
32. Y. N. Lee, P. D. Bieniasz, Reconstitution of an infectious human endogenous retrovirus. PLOS Pathog. 3, e10 (2007).
33. Y. N. Lee, M. H. Malim, P. D. Bieniasz, Hypermutation of an ancient human retrovirus by APOBEC3G. J. Virol. 82, 8762-8770 (2008).
34. L. Agoni, C. Guha, J. Lenz, Detection of human endogenous retrovirus K (HERV-K) transcripts in human prostate cancer cell lines. Front. Oncol. 3, 180 (2013).
35. A. Flockerzi, A. Ruggieri, O. Frank, M. Sauter, E. Maldener, B. Kopper, B. Wullich, W. Seifarth, N. Müller-Lantzsch, C. Leib-Mösch, E. Meese, J. Mayer, Expression patterns of transcribed human endogenous retrovirus HERV-K(HML-2) loci in human tissues and the need for a HERV Transcriptome Project. BMC Genomics 9, 354 (2008).
36. A. Freund, A. V. Orjalo, P.-Y. Desprez, J. Campisi, Inflammatory networks during cellular senescence: Causes and consequences. Trends Mol. Med. 16, 238-246 (2010).
37. A. Haase, J. Frahm, D. Matthaei, W. Hänicke, K.-D. Merboldt, FLASH imaging: Rapid NMR imaging using low flip-angle pulses. J. Magn. Reson. 213, 533-541 (2011).
38. G. Paxinos, K. B. J. Franklin, The mouse brain in stereotaxic coordinates. (Elsevier Academic Press, Amsterdam, ed. Compact 2nd, 2004).
39. A. Yamamoto, J. J. Lucas, R. Hen, Reversal of neuropathology and motor dysfunction in a conditional model of Huntington's disease. Cell 101, 57-66 (2000).
40. M. Cyr, J.-M. Beaulieu, A. Laakso, T. D. Sotnikova, W.-D. Yao, L. M. Bohn, R. R. Gainetdinov, M. G. Caron, Sustained elevation of extracellular dopamine causes motor dysfunction and selective degeneration of striatal GABAergic neurons. Proc. Natl. Acad. Sci. U.S.A. 100, 11035-11040 (2003).
41. G. A. Metz, M. E. Schwab, Behavioral characterization in a comprehensive mouse test battery reveals motor and sensory impairments in growth-associated protein-43 null mutant mice. Neuroscience 129, 563-574 (2004).
42. D. D. Thiessen, G. Lindzey, Negative geotaxis in mice: Effect of balancing practice on incline behaviour in C57BL-6J male mice. Anim. Behav. 15, 113-116 (1967).
43. C. A. Schneider, W. S. Rasband, K. W. Eliceiri, NIH image to imageJ: 25 years of image analysis. Nat. Methods 9, 671-675 (2012).
44. E. Meijering, M. Jacob, J.-C. F. Sarria, P. Steiner, H. Hirling, M. Unser, Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 58, 167-176 (2004).
45. M.-H. Lee, N. D. Amin, A. Venkatesan, T. Wang, R. Tyagi, H. C. Pant, A. Nath, Impaired neurogenesis and neurite outgrowth in an HIV-gp120 transgenic model is reversed by exercise via BDNF production and Cdk5 regulation. J. Neurovirol. 19, 418-431 (2013).
46. J. Vermeire, E. Naessens, H. Vanderstraeten, A. Landi, V. Iannucci, A. Van Nuffel, T. Taghon, M. Pizzato, B. Verhasselt, Quantification of reverse transcriptase activity by real-time PCR as a fast and accurate method for titration of HIV, lenti- And retroviral vectors. PLOS One 7, e50859 (2012).
47. M. J. Kowalczyk, A.Dánczak-Pazdrowska, B. Szramka-Pawlak, R. Zaba, W. Silny, A. Osmola-Mankowska, Expression of selected human endogenous retroviral sequences in skin and peripheral blood mononuclear cells in morphea. Arch. Med. Sci. 8, 819-825 (2012).
48. K. Ahn, H.-S. Kim, Structural and quantitative expression analyses of HERV gene family in human tissues. Mol. Cells 28, 99-103 (2009).