The MARCH family E3 Ubiquitin ligase K5 alters monocyte metabolism and proliferation through receptor tyrosine kinase modulation

PLoS Pathogens

Volumn 7, Issue 4, 2011, Pages

  Karki, Roshan ^a   Lang, Sabine M ^a   Means, Robert E ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE B; PROTEIN TYROSINE KINASE; UBIQUITIN PROTEIN LIGASE E3; GLUCOSE; IMMEDIATE EARLY PROTEIN; K5 PROTEIN, HUMAN HERPESVIRUS 8; LACTIC ACID; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

ANAEROBIC GLYCOLYSIS; APOPTOSIS; ARTICLE; AUTOCRINE EFFECT; CARCINOGENESIS; CELL COUNT; CELL CULTURE; CELL CYCLE; CELL DIVISION; CELL METABOLISM; CELL PROLIFERATION; DOWN REGULATION; ENDOCYTOSIS; ENZYME ACTIVATION; FLOW CYTOMETRY; GENETIC TRANSFECTION; GLUCOSE TRANSPORT; HUMAN HERPESVIRUS 8; IMMUNOBLOTTING; IMMUNOPRECIPITATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ENZYMOLOGY; HUMAN; IMMUNOLOGY; KAPOSI SARCOMA; METABOLISM; MONOCYTE; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE; VIROLOGY;

HERPESVIRIDAE; HUMAN HERPESVIRUS 8;

CELL LINE, TUMOR; CELL PROLIFERATION; DOWN-REGULATION; ENDOCYTOSIS; GLUCOSE; HERPESVIRUS 8, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; LACTIC ACID; MONOCYTES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR PROTEIN-TYROSINE KINASES; SARCOMA, KAPOSI; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 79955786075     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001331     Document Type: Article

References (66)

1. Gatenby RA, Gillies RJ, (2004) Why do cancers have high aerobic glycolysis? Nat Rev Cancer 4: 891-899.
2. DeBerardinis RJ, Cheng T, (2010) Q's next: the diverse functions of glutamine in metabolism, cell biology and cancer. Oncogene 29: 313-324.
3. Koukourakis MI, Giatromanolaki A, Harris AL, Sivridis E, (2006) Comparison of metabolic pathways between cancer cells and stromal cells in colorectal carcinomas: a metabolic survival role for tumor-associated stroma. Cancer Res 66: 632-637.
4. 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.
5. 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.
6. 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.
7. Valenti R, Huber V, Iero M, Filipazzi P, Parmiani G, et al. (2007) Tumor-released microvesicles as vehicles of immunosuppression. Cancer Res 67: 2912-2915.
8. Solinas G, Germano G, Mantovani A, Allavena P, (2009) Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation. J Leukoc Biol 86: 1065-1073.
9. Coffelt SB, Hughes R, Lewis CE, (2009) Tumor-associated macrophages: effectors of angiogenesis and tumor progression. Biochim Biophys Acta 1796: 11-18.
10. Gasperini P, Sakakibara S, Tosato G, (2008) Contribution of viral and cellular cytokines to Kaposi's sarcoma-associated herpesvirus pathogenesis. J Leukoc Biol 84: 994-1000.
11. Choi YB, Nicholas J, (2008) Autocrine and paracrine promotion of cell survival and virus replication by human herpesvirus 8 chemokines. J Virol 82: 6501-6513.
12. Liu C, Okruzhnov Y, Li H, Nicholas J, (2001) Human herpesvirus 8 (HHV-8)-encoded cytokines induce expression of and autocrine signaling by vascular endothelial growth factor (VEGF) in HHV-8-infected primary-effusion lymphoma cell lines and mediate VEGF-independent antiapoptotic effects. J Virol 75: 10933-10940.
13. Kang T, Ye FC, Gao SJ, Wang LD, (2008) Angiogenesis, Kaposi's Sarcoma and Kaposi's Sarcoma-Associated Herpesvirus. Virol Sin 23: 449-458.
14. Chung YH, Means RE, Choi JK, Lee BS, Jung JU, (2002) Kaposi's sarcoma-associated herpesvirus OX2 glycoprotein activates myeloid-lineage cells to induce inflammatory cytokine production. J Virol 76: 4688-4698.
15. Salata C, Curtarello M, Calistri A, Sartori E, Sette P, et al. (2009) vOX2 glycoprotein of human herpesvirus 8 modulates human primary macrophages activity. J Cell Physiol 219: 698-706.
16. Qin Z, Kearney P, Plaisance K, Parsons CH, (2010) Pivotal advance: Kaposi's sarcoma-associated herpesvirus (KSHV)-encoded microRNA specifically induce IL-6 and IL-10 secretion by macrophages and monocytes. J Leukoc Biol 87: 25-34.
17. West J, Damania B, (2008) Upregulation of the TLR3 pathway by Kaposi's sarcoma-associated herpesvirus during primary infection. J Virol 82: 5440-5449.
18. Rappocciolo G, Jenkins FJ, Hensler HR, Piazza P, Jais M, et al. (2006) DC-SIGN is a receptor for human herpesvirus 8 on dendritic cells and macrophages. J Immunol 176: 1741-1749.
19. Rappocciolo G, Hensler HR, Jais M, Reinhart TA, Pegu A, et al. (2008) Human herpesvirus 8 infects and replicates in primary cultures of activated B lymphocytes through DC-SIGN. J Virol 82: 4793-4806.
20. Kerur N, Veettil MV, Sharma-Walia N, Sadagopan S, Bottero V, et al. (2010) Characterization of entry and infection of monocytic THP-1 cells by Kaposi's sarcoma associated herpesvirus (KSHV): role of heparan sulfate, DC-SIGN, integrins and signaling. Virology 406: 103-116.
21. Wen KW, Damania B, (2010) Kaposi sarcoma-associated herpesvirus (KSHV): molecular biology and oncogenesis. Cancer Lett 289: 140-150.
22. Montaner S, Sodhi A, Molinolo A, Bugge TH, Sawai ET, et al. (2003) Endothelial infection with KSHV genes in vivo reveals that vGPCR initiates Kaposi's sarcomagenesis and can promote the tumorigenic potential of viral latent genes. Cancer Cell 3: 23-36.
23. Mutlu AD, Cavallin LE, Vincent L, Chiozzini C, Eroles P, et al. (2007) In vivo-restricted and reversible malignancy induced by human herpesvirus-8 KSHV: a cell and animal model of virally induced Kaposi's sarcoma. Cancer Cell 11: 245-258.
24. Dittmer D, Lagunoff M, Renne R, Staskus K, Haase A, et al. (1998) A cluster of latently expressed genes in Kaposi's sarcoma-associated herpesvirus. J Virol 72: 8309-8315.
25. 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.
26. Nathan JA, Lehner PJ, (2009) The trafficking and regulation of membrane receptors by the RING-CH ubiquitin E3 ligases. Exp Cell Res 315: 1593-1600.
27. Chang H, Dittmer DP, Shin YC, Chul SY, Hong Y, et al. (2005) Role of Notch signal transduction in Kaposi's sarcoma-associated herpesvirus gene expression. J Virol 79: 14371-14382.
28. Chang H, (2006) Notch signal transduction induces a novel profile of Kaposi's sarcoma-associated herpesvirus gene expression. J Microbiol 44: 217-225.
29. GŸnther T, Grundhoff A, (2010) The epigenetic landscape of latent Kaposi sarcoma-associated herpesvirus genomes. PLoS Pathog 6: e1000935.
30. Haque M, Ueda K, Nakano K, Hirata Y, Parravicini C, et al. (2001) Major histocompatibility complex class I molecules are down-regulated at the cell surface by the K5 protein encoded by Kaposi's sarcoma-associated herpesvirus/human herpesvirus-8. J Gen Virol 82: 1175-1180.
31. Means RE, Lang SM, Jung JU, (2007) The Kaposi's sarcoma-associated herpesvirus K5 E3 ubiquitin ligase modulates targets by multiple molecular mechanisms. J Virol 81: 6573-6583.
32. Zhivotovsky B, Orrenius S, (2009) The Warburg Effect returns to the cancer stage. Semin Cancer Biol 19: 1-3.
33. Lagunoff M, Bechtel J, Venetsanakos E, Roy AM, Abbey N, et al. (2002) De novo infection and serial transmission of Kaposi's sarcoma-associated herpesvirus in cultured endothelial cells. J Virol 76: 2440-2448.
34. 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.
35. Delgado T, Carroll PA, Punjabi AS, Margineantu D, Hockenbery DM, et al. (2010) Induction of the Warburg effect by Kaposi's sarcoma herpesvirus is required for the maintenance of latently infected endothelial cells. Proc Natl Acad Sci U S A 107: 10696-10701.
36. Elstrom RL, Bauer DE, Buzzai M, Karnauskas R, Harris MH, et al. (2004) Akt stimulates aerobic glycolysis in cancer cells. Cancer Res 64: 3892-3899.
37. Hitosugi T, Kang S, Vander Heiden MG, Chung TW, Elf S, et al. (2009) Tyrosine phosphorylation inhibits PKM2 to promote the Warburg effect and tumor growth. Sci Signal 2: ra73.
38. Dang CV, (2009) PKM2 tyrosine phosphorylation and glutamine metabolism signal a different view of the Warburg effect. Sci Signal 2: pe75.
39. Bartrons R, Caro J, (2007) Hypoxia, glucose metabolism and the Warburg's effect. J Bioenerg Biomembr 39: 223-229.
40. Brahimi-Horn MC, Chiche J, Pouysségur J, (2007) Hypoxia signalling controls metabolic demand. Curr Opin Cell Biol 19: 223-229.
41. Lu H, Forbes RA, Verma A, (2002) Hypoxia-inducible factor 1 activation by aerobic glycolysis implicates the Warburg effect in carcinogenesis. J Biol Chem 277: 23111-23115.
42. Pore N, Jiang Z, Shu HK, Bernhard E, Kao GD, et al. (2006) Akt1 activation can augment hypoxia-inducible factor-1alpha expression by increasing protein translation through a mammalian target of rapamycin-independent pathway. Mol Cancer Res 4: 471-479.
43. Zundel W, Schindler C, Haas-Kogan D, Koong A, Kaper F, et al. (2000) Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev 14: 391-396.
44. Pore N, Liu S, Haas-Kogan DA, O'Rourke DM, Maity A, (2003) PTEN mutation and epidermal growth factor receptor activation regulate vascular endothelial growth factor (VEGF) mRNA expression in human glioblastoma cells by transactivating the proximal VEGF promoter. Cancer Res 63: 236-241.
45. Zhang H, Gao P, Fukuda R, Kumar G, Krishnamachary B, et al. (2007) HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell 11: 407-420.
46. Sandau KB, Faus HG, Brüne B, (2000) Induction of hypoxia-inducible-factor 1 by nitric oxide is mediated via the PI 3K pathway. Biochem Biophys Res Commun 278: 263-267.
47. Zhong H, Chiles K, Feldser D, Laughner E, Hanrahan C, et al. (2000) Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res 60: 1541-1545.
48. Robey IF, Stephen RM, Brown KS, Baggett BK, Gatenby RA, et al. (2008) Regulation of the Warburg effect in early-passage breast cancer cells. Neoplasia 10: 745-756.
49. Penumathsa SV, Thirunavukkarasu M, Zhan L, Maulik G, Menon VP, et al. (2008) Resveratrol enhances GLUT-4 translocation to the caveolar lipid raft fractions through AMPK/Akt/eNOS signalling pathway in diabetic myocardium. J Cell Mol Med 12: 2350-2361.
50. Luo J, Manning BD, Cantley LC, (2003) Targeting the PI3K-Akt pathway in human cancer: rationale and promise. Cancer Cell 4: 257-262.
51. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, et al. (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10: 839-850.
52. Kirchhausen T, Macia E, Pelish HE, (2008) Use of dynasore, the small molecule inhibitor of dynamin, in the regulation of endocytosis. Methods Enzymol 438: 77-93.
53. Wang L, Damania B, (2008) Kaposi's sarcoma-associated herpesvirus confers a survival advantage to endothelial cells. Cancer Res 68: 4640-4648.
54. Carroll PA, Kenerson HL, Yeung RS, Lagunoff M, (2006) Latent Kaposi's sarcoma-associated herpesvirus infection of endothelial cells activates hypoxia-induced factors. J Virol 80: 10802-10812.
55. Weihua Z, Tsan R, Huang WC, Wu Q, Chiu CH, et al. (2008) Survival of cancer cells is maintained by EGFR independent of its kinase activity. Cancer Cell 13: 385-393.
56. Dittmer DP, Krown SE, (2007) Targeted therapy for Kaposi's sarcoma and Kaposi's sarcoma-associated herpesvirus. Curr Opin Oncol 19: 452-457.
57. Ikezoe T, Nishioka C, Tasaka T, Yang Y, Komatsu N, et al. (2006) The antitumor effects of sunitinib (formerly SU11248) against a variety of human hematologic malignancies: enhancement of growth inhibition via inhibition of mammalian target of rapamycin signaling. Mol Cancer Ther 5: 2522-2530.
58. Gutiérrez-Dalmau A, Sánchez-Fructuoso A, Sanz-Guajardo A, Mazuecos A, Franco A, et al. (2005) Efficacy of conversion to sirolimus in posttransplantation Kaposi's sarcoma. Transplant Proc 37: 3836-3838.
59. Stallone G, Infante B, Grandaliano G, Schena FP, Gesualdo L, (2008) Kaposi's sarcoma and mTOR: a crossroad between viral infection neoangiogenesis and immunosuppression. Transpl Int 21: 825-832.
60. Stallone G, Infante B, Pontrelli P, Ranieri E, Loverre A, et al. (2009) ID2-VEGF-related pathways in the pathogenesis of Kaposi's sarcoma: a link disrupted by rapamycin. Am J Transplant 9: 558-566.
61. Lebbé C, Euvrard S, Barrou B, Pouteil-Noble C, Garnier JL, et al. (2006) Sirolimus conversion for patients with posttransplant Kaposi's sarcoma. Am J Transplant 6: 2164-2168.
62. Murphy JE, Padilla BE, Hasdemir B, Cottrell GS, Bunnett NW, (2009) Endosomes: a legitimate platform for the signaling train. Proc Natl Acad Sci U S A 106: 17615-17622.
63. Monini P, Colombini S, Stürzl M, Goletti D, Cafaro A, et al. (1999) Reactivation and persistence of human herpesvirus-8 infection in B cells and monocytes by Th-1 cytokines increased in Kaposi's sarcoma. Blood 93: 4044-4058.
64. Blasig C, Zietz C, Haar B, Neipel F, Esser S, et al. (1997) Monocytes in Kaposi's sarcoma lesions are productively infected by human herpesvirus 8. J Virol 71: 7963-7968.
65. Jones KD, Aoki Y, Chang Y, Moore PS, Yarchoan R, et al. (1999) Involvement of interleukin-10 (IL-10) and viral IL-6 in the spontaneous growth of Kaposi's sarcoma herpesvirus-associated infected primary effusion lymphoma cells. Blood 94: 2871-2879.
66. Aoki Y, Yarchoan R, Braun J, Iwamoto A, Tosato G, (2000) Viral and cellular cytokines in AIDS-related malignant lymphomatous effusions. Blood 96: 1599-1601.