Glutamate Secretion and Metabotropic Glutamate Receptor 1 Expression during Kaposi's Sarcoma-Associated Herpesvirus Infection Promotes Cell Proliferation

PLoS Pathogens

Volumn 10, Issue 10, 2014, Pages

  Valiya Veettil, Mohanan ^a   Dutta, Dipanjan ^a   Bottero, Virginie ^a   Bandyopadhyay, Chirosree ^a   Gjyshi, Olsi ^a   Sharma Walia, Neelam ^a   Dutta, Sujoy ^a   Chandran, Bala ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4', 6 DIAMIDINO 2 PHENYLINDOLE; COMPLEMENTARY DNA; GLUTAMIC ACID; GLUTAMINASE; HERPESVIRUS KAPOSIN A PROTEIN; LATENCY ASSOCIATED NUCLEAR ANTIGEN; LENTIVIRUS VECTOR; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR ANTAGONIST; RE1 SILENCING TRANSCRIPTION FACTOR; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VIRUS PROTEIN; GLUTAMIC ACID DERIVATIVE; METABOTROPIC GLUTAMATE RECEPTOR TYPE 1; METABOTROPIC RECEPTOR;

ARTICLE; B-CELL LYMPHOMA CELL LINE; BRDU ASSAY; CELL FRACTIONATION; CELL LYSATE; CELL PROLIFERATION; CONTROLLED STUDY; DERMAL MICROVASCULAR ENDOTHELIAL CELL; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC TRANSDUCTION; GENETIC TRANSFECTION; HERPES VIRUS INFECTION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; MRNA EXPRESSION ASSAY; MTT ASSAY; ONCOGENE C MYC; OPEN READING FRAME; PLASMID; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UBIQUITINATION; UPREGULATION; VIRAL DISEASE IMMUNOFLUORESCENCE ASSAY; WESTERN BLOTTING; B LYMPHOCYTE; CELL LINE; IMMUNOLOGY; KAPOSI SARCOMA; METABOLISM; PHYSIOLOGY; SECRETION (PROCESS); VIROLOGY; VIRUS LATENCY;

HUMAN HERPESVIRUS 8;

B-LYMPHOCYTES; CELL LINE; CELL PROLIFERATION; ENDOTHELIAL CELLS; GLUTAMATES; HERPESVIRIDAE INFECTIONS; HUMANS; RECEPTORS, METABOTROPIC GLUTAMATE; SARCOMA, KAPOSI; VIRUS LATENCY;

EID: 84908315486     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004389     Document Type: Article

References (72)

1. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, et al. (1994) Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266: 1865–1869.
2. Cesarman E, Chang Y, Moore PS, Said JW, Knowles DM, (1995) Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N Engl J Med 332: 1186–1191.
3. Soulier J, Grollet L, Oksenhendler E, Cacoub P, Cazals-Hatem D, et al. (1995) Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood 86: 1276–1280.
4. Dourmishev LA, Dourmishev AL, Palmeri D, Schwartz RA, Lukac DM, (2003) Molecular genetics of Kaposi's sarcoma-associated herpesvirus (human herpesvirus-8) epidemiology and pathogenesis. Microbiol Mol Biol Rev 67: 175–212 table of contents.
5. Ganem D, (1998) Human herpesvirus 8 and its role in the genesis of Kaposi's sarcoma. Curr Clin Top Infect Dis 18: 237–251.
6. Zhong W, Wang H, Herndier B, Ganem D, (1996) Restricted expression of Kaposi sarcoma-associated herpesvirus (human herpesvirus 8) genes in Kaposi sarcoma. Proc Natl Acad Sci U S A 93: 6641–6646.
7. Krishnan HH, Naranatt PP, Smith MS, Zeng L, Bloomer C, et al. (2004) Concurrent expression of latent and a limited number of lytic genes with immune modulation and antiapoptotic function by Kaposi's sarcoma-associated herpesvirus early during infection of primary endothelial and fibroblast cells and subsequent decline of lytic gene expression. J Virol 78: 3601–3620.
8. Naranatt PP, Krishnan HH, Svojanovsky SR, Bloomer C, Mathur S, et al. (2004) Host gene induction and transcriptional reprogramming in Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8)-infected endothelial, fibroblast, and B cells: insights into modulation events early during infection. Cancer Res 64: 72–84.
9. Cai Q, Verma SC, Lu J, Robertson ES, Molecular biology of Kaposi's sarcoma-associated herpesvirus and related oncogenesis. Adv Virus Res 78: 87–142.
10. Mesri EA, Cesarman E, Boshoff C, Kaposi's sarcoma and its associated herpesvirus. Nat Rev Cancer 10: 707–719.
11. Wen KW, Damania B, Kaposi sarcoma-associated herpesvirus (KSHV): molecular biology and oncogenesis. Cancer Lett 289: 140–150.
12. Ensoli B, Nakamura S, Salahuddin SZ, Biberfeld P, Larsson L, et al. (1989) AIDS-Kaposi's sarcoma-derived cells express cytokines with autocrine and paracrine growth effects. Science 243: 223–226.
13. Drexler HG, Meyer C, Gaidano G, Carbone A, (1999) Constitutive cytokine production by primary effusion (body cavity-based) lymphoma-derived cell lines. Leukemia 13: 634–640.
14. Oksenhendler E, Carcelain G, Aoki Y, Boulanger E, Maillard A, et al. (2000) High levels of human herpesvirus 8 viral load, human interleukin-6, interleukin-10, and C reactive protein correlate with exacerbation of multicentric castleman disease in HIV-infected patients. Blood 96: 2069–2073.
15. Asou H, Said JW, Yang R, Munker R, Park DJ, et al. (1998) Mechanisms of growth control of Kaposi's sarcoma-associated herpes virus-associated primary effusion lymphoma cells. Blood 91: 2475–2481.
16. Ensoli B, Sturzl M, (1998) Kaposi's sarcoma: a result of the interplay among inflammatory cytokines, angiogenic factors and viral agents. Cytokine Growth Factor Rev 9: 63–83.
17. Xu Y, Ganem D, (2007) Induction of chemokine production by latent Kaposi's sarcoma-associated herpesvirus infection of endothelial cells. J Gen Virol 88: 46–50.
18. Biberfeld P, Ensoli B, Sturzl M, Schulz TF, (1998) Kaposi sarcoma-associated herpesvirus/human herpesvirus 8, cytokines, growth factors and HIV in pathogenesis of Kaposi's sarcoma. Curr Opin Infect Dis 11: 97–105.
19. Castiglione M, Calafiore M, Costa L, Sortino MA, Nicoletti F, et al. (2008) Group I metabotropic glutamate receptors control proliferation, survival and differentiation of cultured neural progenitor cells isolated from the subventricular zone of adult mice. Neuropharmacology 55: 560–567.
20. Conn PJ, Pin JP, (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37: 205–237.
21. Dingledine R, Borges K, Bowie D, Traynelis SF, (1999) The glutamate receptor ion channels. Pharmacol Rev 51: 7–61.
22. Marin YE, Namkoong J, Cohen-Solal K, Shin SS, Martino JJ, et al. (2006) Stimulation of oncogenic metabotropic glutamate receptor 1 in melanoma cells activates ERK1/2 via PKCepsilon. Cell Signal 18: 1279–1286.
23. Collard CD, Park KA, Montalto MC, Alapati S, Buras JA, et al. (2002) Neutrophil-derived glutamate regulates vascular endothelial barrier function. J Biol Chem 277: 14801–14811.
24. Pacheco R, Ciruela F, Casado V, Mallol J, Gallart T, et al. (2004) Group I metabotropic glutamate receptors mediate a dual role of glutamate in T cell activation. J Biol Chem 279: 33352–33358.
25. Skerry TM, Genever PG, (2001) Glutamate signalling in non-neuronal tissues. Trends Pharmacol Sci 22: 174–181.
26. Wang FZ, Akula SM, Pramod NP, Zeng L, Chandran B, (2001) Human herpesvirus 8 envelope glycoprotein K8.1A interaction with the target cells involves heparan sulfate. J Virol 75: 7517–7527.
27. Staskus KA, Zhong W, Gebhard K, Herndier B, Wang H, et al. (1997) Kaposi's sarcoma-associated herpesvirus gene expression in endothelial (spindle) tumor cells. J Virol 71: 715–719.
28. Judde JG, Lacoste V, Briere J, Kassa-Kelembho E, Clyti E, et al. (2000) Monoclonality or oligoclonality of human herpesvirus 8 terminal repeat sequences in Kaposi's sarcoma and other diseases. J Natl Cancer Inst 92: 729–736.
29. An FQ, Folarin HM, Compitello N, Roth J, Gerson SL, et al. (2006) Long-term-infected telomerase-immortalized endothelial cells: a model for Kaposi's sarcoma-associated herpesvirus latency in vitro and in vivo. J Virol 80: 4833–4846.
30. Nun TK, Kroll DJ, Oberlies NH, Soejarto DD, Case RJ, et al. (2007) Development of a fluorescence-based assay to screen antiviral drugs against Kaposi's sarcoma associated herpesvirus. Mol Cancer Ther 6: 2360–2370.
31. Curthoys NP, Watford M, (1995) Regulation of glutaminase activity and glutamine metabolism. Annu Rev Nutr 15: 133–159.
32. Shapiro RA, Clark VM, Curthoys NP, (1979) Inactivation of rat renal phosphate-dependent glutaminase with 6-diazo-5-oxo-L-norleucine. Evidence for interaction at the glutamine binding site. J Biol Chem 254: 2835–2838.
33. Liu J, Martin HJ, Liao G, Hayward SD, (2007) The Kaposi's sarcoma-associated herpesvirus LANA protein stabilizes and activates c-Myc. J Virol 81: 10451–10459.
34. Gao P, Tchernyshyov I, Chang TC, Lee YS, Kita K, et al. (2009) c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 458: 762–765.
35. Pollock PM, Cohen-Solal K, Sood R, Namkoong J, Martino JJ, et al. (2003) Melanoma mouse model implicates metabotropic glutamate signaling in melanocytic neoplasia. Nat Genet 34: 108–112.
36. Martino JJ, Wall BA, Mastrantoni E, Wilimczyk BJ, La Cava SN, et al. Metabotropic glutamate receptor 1 (Grm1) is an oncogene in epithelial cells. Oncogene
37. Schoenherr CJ, Anderson DJ, (1995) Silencing is golden: negative regulation in the control of neuronal gene transcription. Curr Opin Neurobiol 5: 566–571.
38. Crepaldi L, Lackner C, Corti C, Ferraguti F, (2007) Transcriptional activators and repressors for the neuron-specific expression of a metabotropic glutamate receptor. J Biol Chem 282: 17877–17889.
39. Lee HJ, Wall BA, Wangari-Talbot J, Chen S, Regulation of mGluR1 expression in human melanocytes and melanoma cells. Biochim Biophys Acta 1819: 1123–1131.
40. Guardavaccaro D, Frescas D, Dorrello NV, Peschiaroli A, Multani AS, et al. (2008) Control of chromosome stability by the beta-TrCP-REST-Mad2 axis. Nature 452: 365–369.
41. Westbrook TF, Hu G, Ang XL, Mulligan P, Pavlova NN, et al. (2008) SCFbeta-TRCP controls oncogenic transformation and neural differentiation through REST degradation. Nature 452: 370–374.
42. Sadler R, Wu L, Forghani B, Renne R, Zhong W, et al. (1999) A complex translational program generates multiple novel proteins from the latently expressed kaposin (K12) locus of Kaposi's sarcoma-associated herpesvirus. J Virol 73: 5722–5730.
43. Muralidhar S, Veytsmann G, Chandran B, Ablashi D, Doniger J, et al. (2000) Characterization of the human herpesvirus 8 (Kaposi's sarcoma-associated herpesvirus) oncogene, kaposin (ORF K12). J Clin Virol 16: 203–213.
44. Kliche S, Nagel W, Kremmer E, Atzler C, Ege A, et al. (2001) Signaling by human herpesvirus 8 kaposin A through direct membrane recruitment of cytohesin-1. Mol Cell 7: 833–843.
45. Muralidhar S, Pumfery AM, Hassani M, Sadaie MR, Kishishita M, et al. (1998) Identification of kaposin (open reading frame K12) as a human herpesvirus 8 (Kaposi's sarcoma-associated herpesvirus) transforming gene. J Virol 72: 4980–4988.
46. Chen X, Cheng L, Jia X, Zeng Y, Yao S, et al. (2009) Human immunodeficiency virus type 1 Tat accelerates Kaposi sarcoma-associated herpesvirus Kaposin A-mediated tumorigenesis of transformed fibroblasts in vitro as well as in nude and immunocompetent mice. Neoplasia 11: 1272–1284.
47. Ye ZC, Sontheimer H, (1999) Glioma cells release excitotoxic concentrations of glutamate. Cancer Res 59: 4383–4391.
48. Lyons SA, Chung WJ, Weaver AK, Ogunrinu T, Sontheimer H, (2007) Autocrine glutamate signaling promotes glioma cell invasion. Cancer Res 67: 9463–9471.
49. Sadagopan S, Sharma-Walia N, Veettil MV, Bottero V, Levine R, et al. (2009) Kaposi's sarcoma-associated herpesvirus upregulates angiogenin during infection of human dermal microvascular endothelial cells, which induces 45S rRNA synthesis, antiapoptosis, cell proliferation, migration, and angiogenesis. J Virol 83: 3342–3364.
50. Danbolt NC, (2001) Glutamate uptake. Prog Neurobiol 65: 1–105.
51. Derouiche A, Rauen T, (1995) Coincidence of L-glutamate/L-aspartate transporter (GLAST) and glutamine synthetase (GS) immunoreactions in retinal glia: evidence for coupling of GLAST and GS in transmitter clearance. J Neurosci Res 42: 131–143.
52. Rauen T, Wiessner M, (2000) Fine tuning of glutamate uptake and degradation in glial cells: common transcriptional regulation of GLAST1 and GS. Neurochem Int 37: 179–189.
53. Dang CV, Le A, Gao P, (2009) MYC-induced cancer cell energy metabolism and therapeutic opportunities. Clin Cancer Res 15: 6479–6483.
54. Majumder S, (2006) REST in good times and bad: roles in tumor suppressor and oncogenic activities. Cell Cycle 5: 1929–1935.
55. Moss AC, Jacobson GM, Walker LE, Blake NW, Marshall E, et al. (2009) SCG3 transcript in peripheral blood is a prognostic biomarker for REST-deficient small cell lung cancer. Clin Cancer Res 15: 274–283.
56. Gurrola-Diaz C, Lacroix J, Dihlmann S, Becker CM, von Knebel Doeberitz M, (2003) Reduced expression of the neuron restrictive silencer factor permits transcription of glycine receptor alpha1 subunit in small-cell lung cancer cells. Oncogene 22: 5636–5645.
57. Westbrook TF, Martin ES, Schlabach MR, Leng Y, Liang AC, et al. (2005) A genetic screen for candidate tumor suppressors identifies REST. Cell 121: 837–848.
58. Huang Y, Myers SJ, Dingledine R, (1999) Transcriptional repression by REST: recruitment of Sin3A and histone deacetylase to neuronal genes. Nat Neurosci 2: 867–872.
59. Naruse Y, Aoki T, Kojima T, Mori N, (1999) Neural restrictive silencer factor recruits mSin3 and histone deacetylase complex to repress neuron-specific target genes. Proc Natl Acad Sci U S A 96: 13691–13696.
60. Krithivas A, Young DB, Liao G, Greene D, Hayward SD, (2000) Human herpesvirus 8 LANA interacts with proteins of the mSin3 corepressor complex and negatively regulates Epstein-Barr virus gene expression in dually infected PEL cells. J Virol 74: 9637–9645.
61. Andres ME, Burger C, Peral-Rubio MJ, Battaglioli E, Anderson ME, et al. (1999) CoREST: a functional corepressor required for regulation of neural-specific gene expression. Proc Natl Acad Sci U S A 96: 9873–9878.
62. Rzeski W, Ikonomidou C, Turski L, (2002) Glutamate antagonists limit tumor growth. Biochem Pharmacol 64: 1195–1200.
63. Cavalheiro EA, Olney JW, (2001) Glutamate antagonists: deadly liaisons with cancer. Proc Natl Acad Sci U S A 98: 5947–5948.
64. Iwamoto FM, Kreisl TN, Kim L, Duic JP, Butman JA, et al. Phase 2 trial of talampanel, a glutamate receptor inhibitor, for adults with recurrent malignant gliomas. Cancer 116: 1776–1782.
65. Yip D, Le MN, Chan JL, Lee JH, Mehnert JA, et al. (2009) A phase 0 trial of riluzole in patients with resectable stage III and IV melanoma. Clin Cancer Res 15: 3896–3902.
66. Namkoong J, Shin SS, Lee HJ, Marin YE, Wall BA, et al. (2007) Metabotropic glutamate receptor 1 and glutamate signaling in human melanoma. Cancer Res 67: 2298–2305.
67. Sharma-Walia N, Paul AG, Bottero V, Sadagopan S, Veettil MV, et al. Kaposi's sarcoma associated herpes virus (KSHV) induced COX-2: a key factor in latency, inflammation, angiogenesis, cell survival and invasion. PLoS Pathog 6: e1000777.
68. Akula SM, Pramod NP, Wang FZ, Chandran B, (2002) Integrin alpha3beta1 (CD 49c/29) is a cellular receptor for Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8) entry into the target cells. Cell 108: 407–419.
69. Vart RJ, Nikitenko LL, Lagos D, Trotter MW, Cannon M, et al. (2007) Kaposi's sarcoma-associated herpesvirus-encoded interleukin-6 and G-protein-coupled receptor regulate angiopoietin-2 expression in lymphatic endothelial cells. Cancer Res 67: 4042–4051.
70. Tiscornia G, Singer O, Verma IM, (2006) Production and purification of lentiviral vectors. Nat Protoc 1: 241–245.
71. Choi KY, Chang K, Pickel JM, Badger JD, 2ndRoche KW, Expression of the metabotropic glutamate receptor 5 (mGluR5) induces melanoma in transgenic mice. Proc Natl Acad Sci U S A 108: 15219–15224.
72. Valiya Veettil M, Sadagopan S, Kerur N, Chakraborty S, Chandran B, Interaction of c-Cbl with myosin IIA regulates Bleb associated macropinocytosis of Kaposi's sarcoma-associated herpesvirus. PLoS Pathog 6: e1001238.