The KSHV K1 Protein Modulates AMPK Function to Enhance Cell Survival

PLoS Pathogens

Volumn 12, Issue 11, 2016, Pages

  Anders, Penny M ^a,b   Zhang, Zhigang ^a,b   Bhende, Prasana M ^a,b   Giffin, Louise ^a,b   Damania, Blossom ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; UNCLASSIFIED DRUG; VIRAL PROTEIN; VIRUS PROTEIN K1; K1 PROTEIN, HUMAN HERPESVIRUS 8;

ARTICLE; CELL FRACTIONATION; CELL SURVIVAL; CELL VIABILITY; CELLULAR STRESS SIGNAL; CHROMATIN IMMUNOPRECIPITATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; KAPOSI SARCOMA; MTS ASSAY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; TRYPAN BLUE ASSAY; WESTERN BLOTTING; FLUORESCENT ANTIBODY TECHNIQUE; HEK293 CELL LINE; IMMUNOPRECIPITATION; METABOLISM;

AMP-ACTIVATED PROTEIN KINASES; FLUORESCENT ANTIBODY TECHNIQUE; HEK293 CELLS; HERPESVIRUS 8, HUMAN; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICROSCOPY, CONFOCAL; VIRAL PROTEINS;

EID: 85002342296     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005985     Document Type: Article

References (68)

1. Soulier J, Grollet L, Oksenhendler E, Cacoub P, Cazals-Hatem D, Babinet P, et al. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood. 1995;86(4):1276–80. 7632932
2. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, Knowles DM, et al. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science. 1994;266(5192):1865–9. 7997879
3. Cesarman E, Chang Y, Moore PS, Said JW, Knowles DM, Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. The New England journal of medicine. 1995;332(18):1186–91. doi: 10.1056/NEJM1995050433218027700311
4. Oh JK, Weiderpass E, Infection and Cancer: Global Distribution and Burden of Diseases. Annals of global health. 2014;80(5):384–92. doi: 10.1016/j.aogh.2014.09.01325512154
5. Parkin DM, The global health burden of infection-associated cancers in the year 2002. International journal of cancer Journal international du cancer. 2006;118(12):3030–44. doi: 10.1002/ijc.2173116404738
6. Russo JJ, Bohenzky RA, Chien MC, Chen J, Yan M, Maddalena D, et al. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proceedings of the National Academy of Sciences of the United States of America. 1996;93(25):14862–7. 8962146
7. Fields BN, Howley PM, Knipe DM, Fields virology [electronic resource]. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2013.
8. Gregory SM, West JA, Dillon PJ, Hilscher C, Dittmer DP, Damania B, Toll-like receptor signaling controls reactivation of KSHV from latency. Proceedings of the National Academy of Sciences of the United States of America. 2009;106(28):11725–30. doi: 10.1073/pnas.090531610619564611
9. Bowser BS, DeWire SM, Damania B, Transcriptional regulation of the K1 gene product of Kaposi's sarcoma-associated herpesvirus. Journal of virology. 2002;76(24):12574–83. doi: 10.1128/JVI.76.24.12574-12583.200212438583
10. Chandriani S, Ganem D, Array-based transcript profiling and limiting-dilution reverse transcription-PCR analysis identify additional latent genes in Kaposi's sarcoma-associated herpesvirus. Journal of virology. 2010;84(11):5565–73. doi: 10.1128/JVI.02723-0920219929
11. Arias C, Weisburd B, Stern-Ginossar N, Mercier A, Madrid AS, Bellare P, et al. KSHV 2.0: a comprehensive annotation of the Kaposi's sarcoma-associated herpesvirus genome using next-generation sequencing reveals novel genomic and functional features. PLoS pathogens. 2014;10(1):e1003847. doi: 10.1371/journal.ppat.100384724453964
12. Lee H, Guo J, Li M, Choi JK, DeMaria M, Rosenzweig M, et al. Identification of an immunoreceptor tyrosine-based activation motif of K1 transforming protein of Kaposi's sarcoma-associated herpesvirus. Molecular and cellular biology. 1998;18(9):5219–28. 9710606
13. Lee BS, Lee SH, Feng P, Chang H, Cho NH, Jung JU, Characterization of the Kaposi's sarcoma-associated herpesvirus K1 signalosome. Journal of virology. 2005;79(19):12173–84. doi: 10.1128/JVI.79.19.12173-12184.200516160144
14. Lagunoff M, Majeti R, Weiss A, Ganem D, Deregulated signal transduction by the K1 gene product of Kaposi's sarcoma-associated herpesvirus. Proceedings of the National Academy of Sciences of the United States of America. 1999;96(10):5704–9. 10318948
15. Lee H, Veazey R, Williams K, Li M, Guo J, Neipel F, et al. Deregulation of cell growth by the K1 gene of Kaposi's sarcoma-associated herpesvirus. Nature medicine. 1998;4(4):435–40. 9546789
16. Prakash O, Tang ZY, Peng X, Coleman R, Gill J, Farr G, et al. Tumorigenesis and aberrant signaling in transgenic mice expressing the human herpesvirus-8 K1 gene. Journal of the National Cancer Institute. 2002;94(12):926–35. 12072546
17. Wang L, Dittmer DP, Tomlinson CC, Fakhari FD, Damania B, Immortalization of primary endothelial cells by the K1 protein of Kaposi's sarcoma-associated herpesvirus. Cancer research. 2006;66(7):3658–66. doi: 10.1158/0008-5472.CAN-05-368016585191
18. Tomlinson CC, Damania B, The K1 protein of Kaposi's sarcoma-associated herpesvirus activates the Akt signaling pathway. Journal of virology. 2004;78(4):1918–27. doi: 10.1128/JVI.78.4.1918-1927.200414747556
19. Wang S, Wang S, Maeng H, Young DP, Prakash O, Fayad LE, et al. K1 protein of human herpesvirus 8 suppresses lymphoma cell Fas-mediated apoptosis. Blood. 2007;109(5):2174–82. doi: 10.1182/blood-2006-02-00317817090655
20. Berkova Z, Wang S, Wise JF, Maeng H, Ji Y, Samaniego F, Mechanism of Fas signaling regulation by human herpesvirus 8 K1 oncoprotein. Journal of the National Cancer Institute. 2009;101(6):399–411. doi: 10.1093/jnci/djn51619276446
21. Hardie DG, AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol. 2007;8(10):774–85. doi: 10.1038/nrm224917712357
22. Stapleton D, Mitchelhill KI, Gao G, Widmer J, Michell BJ, Teh T, et al. Mammalian AMP-activated protein kinase subfamily. The Journal of biological chemistry. 1996;271(2):611–4. 8557660
23. Gao G, Fernandez CS, Stapleton D, Auster AS, Widmer J, Dyck JR, et al. Non-catalytic beta- and gamma-subunit isoforms of the 5'-AMP-activated protein kinase. The Journal of biological chemistry. 1996;271(15):8675–81. 8621499
24. Thornton C, Snowden MA, Carling D, Identification of a novel AMP-activated protein kinase beta subunit isoform that is highly expressed in skeletal muscle. The Journal of biological chemistry. 1998;273(20):12443–50. 9575201
25. Cheung PC, Salt IP, Davies SP, Hardie DG, Carling D, Characterization of AMP-activated protein kinase gamma-subunit isoforms and their role in AMP binding. The Biochemical journal. 2000;346Pt 3:659–69. 10698692
26. Salt I, Celler JW, Hawley SA, Prescott A, Woods A, Carling D, et al. AMP-activated protein kinase: greater AMP dependence, and preferential nuclear localization, of complexes containing the alpha2 isoform. The Biochemical journal. 1998;334 (Pt 1):177–87. 9693118
27. Warden SM, Richardson C, O'Donnell J, Jr.Stapleton D, Kemp BE, Witters LA, Post-translational modifications of the beta-1 subunit of AMP-activated protein kinase affect enzyme activity and cellular localization. The Biochemical journal. 2001;354(Pt 2):275–83. 11171104
28. Turnley AM, Stapleton D, Mann RJ, Witters LA, Kemp BE, Bartlett PF, Cellular distribution and developmental expression of AMP-activated protein kinase isoforms in mouse central nervous system. Journal of neurochemistry. 1999;72(4):1707–16. 10098881
29. Crute BE, Seefeld K, Gamble J, Kemp BE, Witters LA, Functional domains of the alpha1 catalytic subunit of the AMP-activated protein kinase. The Journal of biological chemistry. 1998;273(52):35347–54. 9857077
30. Hardie DG, Ross FA, Hawley SA, AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol. 2012;13(4):251–62. doi: 10.1038/nrm331122436748
31. Gowans GJ, Hardie DG, AMPK: a cellular energy sensor primarily regulated by AMP. Biochemical Society transactions. 2014;42(1):71–5. doi: 10.1042/BST2013024424450630
32. Hong SP, Leiper FC, Woods A, Carling D, Carlson M, Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(15):8839–43. doi: 10.1073/pnas.153313610012847291
33. Woods A, Johnstone SR, Dickerson K, Leiper FC, Fryer LG, Neumann D, et al. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Current biology: CB. 2003;13(22):2004–8. 14614828
34. Peralta C, Bartrons R, Serafin A, Blazquez C, Guzman M, Prats N, et al. Adenosine monophosphate-activated protein kinase mediates the protective effects of ischemic preconditioning on hepatic ischemia-reperfusion injury in the rat. Hepatology. 2001;34(6):1164–73. doi: 10.1053/jhep.2001.2919711732006
35. Marsin AS, Bouzin C, Bertrand L, Hue L, The stimulation of glycolysis by hypoxia in activated monocytes is mediated by AMP-activated protein kinase and inducible 6-phosphofructo-2-kinase. The Journal of biological chemistry. 2002;277(34):30778–83. doi: 10.1074/jbc.M20521320012065600
36. Lee M, Hwang JT, Lee HJ, Jung SN, Kang I, Chi SG, et al. AMP-activated protein kinase activity is critical for hypoxia-inducible factor-1 transcriptional activity and its target gene expression under hypoxic conditions in DU145 cells. The Journal of biological chemistry. 2003;278(41):39653–61. doi: 10.1074/jbc.M30610420012900407
37. Laderoute KR, Amin K, Calaoagan JM, Knapp M, Le T, Orduna J, et al. 5'-AMP-activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid-tumor microenvironments. Molecular and cellular biology. 2006;26(14):5336–47. doi: 10.1128/MCB.00166-0616809770
38. Jeon SM, Hay N, The double-edged sword of AMPK signaling in cancer and its therapeutic implications. Arch Pharm Res. 2015;38(3):346–57. doi: 10.1007/s12272-015-0549-z25575627
39. Jeon SM, Hay N, The dark face of AMPK as an essential tumor promoter. Cell Logist. 2012;2(4):197–202. doi: 10.4161/cl.2265123676995
40. Chhipa RR, Wu Y, Mohler JL, Ip C, Survival advantage of AMPK activation to androgen-independent prostate cancer cells during energy stress. Cellular signalling. 2010;22(10):1554–61. doi: 10.1016/j.cellsig.2010.05.02420570728
41. Park HU, Suy S, Danner M, Dailey V, Zhang Y, Li H, et al. AMP-activated protein kinase promotes human prostate cancer cell growth and survival. Molecular cancer therapeutics. 2009;8(4):733–41. doi: 10.1158/1535-7163.MCT-08-063119372545
42. Vucicevic L, Misirkic M, Janjetovic K, Harhaji-Trajkovic L, Prica M, Stevanovic D, et al. AMP-activated protein kinase-dependent and -independent mechanisms underlying in vitro antiglioma action of compound C. Biochemical pharmacology. 2009;77(11):1684–93. doi: 10.1016/j.bcp.2009.03.00519428322
43. Baumann P, Mandl-Weber S, Emmerich B, Straka C, Schmidmaier R, Inhibition of adenosine monophosphate-activated protein kinase induces apoptosis in multiple myeloma cells. Anticancer Drugs. 2007;18(4):405–10. doi: 10.1097/CAD.0b013e32801416b617351392
44. Yang WL, Perillo W, Liou D, Marambaud P, Wang P, AMPK inhibitor compound C suppresses cell proliferation by induction of apoptosis and autophagy in human colorectal cancer cells. J Surg Oncol. 2012;106(6):680–8. doi: 10.1002/jso.2318422674626
45. Jang T, Calaoagan JM, Kwon E, Samuelsson S, Recht L, Laderoute KR, 5'-AMP-activated protein kinase activity is elevated early during primary brain tumor development in the rat. International journal of cancer Journal international du cancer. 2011;128(9):2230–9. doi: 10.1002/ijc.2555820635388
46. Zhang Z, Chen W, Sanders MK, Brulois KF, Dittmer DP, Damania B, The K1 Protein of Kaposi's Sarcoma-Associated Herpesvirus Augments Viral Lytic Replication. Journal of virology. 2016;90(17):7657–66. doi: 10.1128/JVI.03102-1527307571
47. Hardie DG, AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes & development. 2011;25(18):1895–908.
48. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, et al. Role of AMP-activated protein kinase in mechanism of metformin action. The Journal of clinical investigation. 2001;108(8):1167–74. doi: 10.1172/JCI1350511602624
49. Accordi B, Galla L, Milani G, Curtarello M, Serafin V, Lissandron V, et al. AMPK inhibition enhances apoptosis in MLL-rearranged pediatric B-acute lymphoblastic leukemia cells. Leukemia. 2013;27(5):1019–27. doi: 10.1038/leu.2012.33823228943
50. Wen KW, Damania B, Hsp90 and Hsp40/Erdj3 are required for the expression and anti-apoptotic function of KSHV K1. Oncogene. 2010;29(24):3532–44. doi: 10.1038/onc.2010.12420418907
51. Lee BS, Alvarez X, Ishido S, Lackner AA, Jung JU, Inhibition of intracellular transport of B cell antigen receptor complexes by Kaposi's sarcoma-associated herpesvirus K1. The Journal of experimental medicine. 2000;192(1):11–21. 10880522
52. Tomlinson CC, Damania B, Critical role for endocytosis in the regulation of signaling by the Kaposi's sarcoma-associated herpesvirus K1 protein. Journal of virology. 2008;82(13):6514–23. doi: 10.1128/JVI.02637-0718434405
53. Davies SP, Carling D, Hardie DG, Tissue distribution of the AMP-activated protein kinase, and lack of activation by cyclic-AMP-dependent protein kinase, studied using a specific and sensitive peptide assay. Eur J Biochem. 1989;186(1–2):123–8. 2574667
54. Giffin L, Anders P, Damania B, Hudnall SD, Kaposi’s Sarcoma-Associated Herpesvirus: Pathogenesis and Host Immune Response. In: Viruses and Human Cancer. New York: Springer Science; 2014. p. 289–322.
55. Buzzai M, Bauer DE, Jones RG, Deberardinis RJ, Hatzivassiliou G, Elstrom RL, et al. The glucose dependence of Akt-transformed cells can be reversed by pharmacologic activation of fatty acid beta-oxidation. Oncogene. 2005;24(26):4165–73. doi: 10.1038/sj.onc.120862215806154
56. Bhatt AP, Jacobs SR, Freemerman AJ, Makowski L, Rathmell JC, Dittmer DP, et al. Dysregulation of fatty acid synthesis and glycolysis in non-Hodgkin lymphoma. Proceedings of the National Academy of Sciences of the United States of America. 2012;109(29):11818–23. doi: 10.1073/pnas.120599510922752304
57. Delgado T, Carroll PA, Punjabi AS, Margineantu D, Hockenbery DM, Lagunoff M, Induction of the Warburg effect by Kaposi's sarcoma herpesvirus is required for the maintenance of latently infected endothelial cells. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(23):10696–701. doi: 10.1073/pnas.100488210720498071
58. Bhatt AP, Bhende PM, Sin SH, Roy D, Dittmer DP, Damania B, Dual inhibition of PI3K and mTOR inhibits autocrine and paracrine proliferative loops in PI3K/Akt/mTOR-addicted lymphomas. Blood. 2010;115(22):4455–63. doi: 10.1182/blood-2009-10-25108220299510
59. Murata Y, Uehara Y, Hosoi Y, Activation of mTORC1 under nutrient starvation conditions increases cellular radiosensitivity in human liver cancer cell lines, HepG2 and HuH6. Biochemical and biophysical research communications. 2015;468(4):684–90. doi: 10.1016/j.bbrc.2015.11.01626585486
60. Friedberg JW, Sharman J, Sweetenham J, Johnston PB, Vose JM, Lacasce A, et al. Inhibition of Syk with fostamatinib disodium has significant clinical activity in non-Hodgkin lymphoma and chronic lymphocytic leukemia. Blood. 2010;115(13):2578–85. doi: 10.1182/blood-2009-08-23647119965662
61. Yanagi S, Inatome R, Ding J, Kitaguchi H, Tybulewicz VL, Yamamura H, Syk expression in endothelial cells and their morphologic defects in embryonic Syk-deficient mice. Blood. 2001;98(9):2869–71. 11675365
62. Inatome R, Yanagi S, Takano T, Yamamura H, A critical role for Syk in endothelial cell proliferation and migration. Biochemical and biophysical research communications. 2001;286(1):195–9. doi: 10.1006/bbrc.2001.535511485328
63. Chang MY, Huang DY, Ho FM, Huang KC, Lin WW, PKC-dependent human monocyte adhesion requires AMPK and Syk activation. PloS one. 2012;7(7):e40999. doi: 10.1371/journal.pone.004099922848421
64. Terry LJ, Vastag L, Rabinowitz JD, Shenk T, Human kinome profiling identifies a requirement for AMP-activated protein kinase during human cytomegalovirus infection. Proceedings of the National Academy of Sciences of the United States of America. 2012;109(8):3071–6. doi: 10.1073/pnas.120049410922315427
65. McArdle J, Moorman NJ, Munger J, HCMV targets the metabolic stress response through activation of AMPK whose activity is important for viral replication. PLoS pathogens. 2012;8(1):e1002502. doi: 10.1371/journal.ppat.100250222291597
66. Leyton L, Hott M, Acuna F, Caroca J, Nunez M, Martin C, et al. Nutraceutical activators of AMPK/Sirt1 axis inhibit viral production and protect neurons from neurodegenerative events triggered during HSV-1 infection. Virus research. 2015;205:63–72. doi: 10.1016/j.virusres.2015.05.01526031763
67. Cheng F, He M, Jung JU, Lu C, Gao SJ, Suppression of Kaposi's sarcoma-associated herpesvirus infection and replication by 5' AMP-activated protein kinase. Journal of virology. 2016.
68. Wang L, Wakisaka N, Tomlinson CC, DeWire SM, Krall S, Pagano JS, et al. The Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8) K1 protein induces expression of angiogenic and invasion factors. Cancer research. 2004;64(8):2774–81. 15087393