Cellular origin of Kaposi's sarcoma and Kaposi's sarcoma-associated herpesvirus-induced cell reprogramming

Trends in Cell Biology

Volumn 23, Issue 9, 2013, Pages 421-432

  Cancian, Laila ^a   Hansen, Amy ^a   Boshoff, Chris ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cell differentiation; Cell plasticity; Endothelial cells; Kaposi's sarcoma; KSHV HHV8; Oncogenic viruses

Indexed keywords

ANGIOGENIN; ANGIOPOIETIN; CYCLOOXYGENASE 2; FIBROBLAST GROWTH FACTOR; FLICE INHIBITORY PROTEIN; G PROTEIN COUPLED RECEPTOR; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HEMOSIDERIN; INTERLEUKIN 1; INTERLEUKIN 6; INTERLEUKIN 8; JANUS KINASE 2; MONOCYTE CHEMOTACTIC PROTEIN 1; PLATELET DERIVED GROWTH FACTOR; STAT3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; VIRUS LARGE T ANTIGEN;

B LYMPHOCYTE; CANCER GROWTH; CARCINOGENESIS; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL DIVISION; DENDRITIC CELL; DERMATITIS; GENE EXPRESSION; HERPES VIRUS; HISTOGENESIS; HUMAN; IMMUNE RESPONSE; IMMUNOSUPPRESSIVE TREATMENT; IN VIVO STUDY; KAPOSI SARCOMA; NUCLEAR REPROGRAMMING; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PLASTICITY; PRIORITY JOURNAL; REVIEW; TARGET CELL; TUMOR VIRUS; UPREGULATION; VIRUS GENOME; COMPLICATION; ENDOTHELIUM CELL; GENETICS; HUMAN HERPESVIRUS 8; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NEOVASCULARIZATION (PATHOLOGY); PATHOGENICITY; PATHOLOGY; VIROLOGY;

HUMAN HERPESVIRUS 8; PROSPERO;

CELL DIFFERENTIATION; ENDOTHELIAL CELLS; HERPESVIRUS 8, HUMAN; HIV INFECTIONS; HUMANS; NEOVASCULARIZATION, PATHOLOGIC; ONCOGENIC VIRUSES; SARCOMA, KAPOSI;

EID: 84882847653     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2013.04.001     Document Type: Review

References (108)

1. Kaposi M. Idiopathisches multiples Pigmentsarkomen der haut. Arch. Dermatol. Syph. 1872, 4:265-273. (in German).
2. Centers for Disease Control (CDC) Kaposi's sarcoma and Pneumocystis pneumonia among homosexual men--New York City and California. MMWR Morb. Mortal. Wkly. Rep. 1981, 30:305-308.
3. Gottlieb G.J., et al. A preliminary communication on extensively disseminated Kaposi's sarcoma in young homosexual men. Am. J. Dermatopathol. 1981, 3:111-114.
4. Franceschi S., Geddes M. Epidemiology of classic Kaposi's sarcoma, with special reference to Mediterranean population. Tumori 1995, 81:308-314.
5. Oettle A.G. Geographical and racial differences in the frequency of Kaposi's sarcoma as evidence of environmental or genetic causes. Acta Unio Int. Contra Cancrum 1962, 18:330-363.
6. Harwood A.R., et al. Kaposi's sarcoma in recipients of renal transplants. Am. J. Med. 1979, 67:759-765.
7. Friedman-Kien A.E. Disseminated Kaposi's sarcoma syndrome in young homosexual men. J. Am. Acad. Dermatol. 1981, 5:468-471.
8. Chang Y., et al. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 1994, 266:1865-1869.
9. Ensoli B., et al. Biology of Kaposi's sarcoma. Eur. J. Cancer 2001, 37:1251-1269.
10. Simpson G.R., et al. Prevalence of Kaposi's sarcoma associated herpesvirus infection measured by antibodies to recombinant capsid protein and latent immunofluorescence antigen. Lancet 1996, 348:1133-1138.
11. Kedes D.H., et al. The seroepidemiology of human herpesvirus 8 (Kaposi's sarcoma-associated herpesvirus): distribution of infection in KS risk groups and evidence for sexual transmission. Nat. Med. 1996, 2:918-924.
12. Sitas F., et al. Antibodies against human herpesvirus 8 in black South African patients with cancer. N. Engl. J. Med. 1999, 340:1863-1871.
13. Boshoff C., Weiss R. AIDS-related malignancies. Nat. Rev. Cancer 2002, 2:373-382.
14. Soerjomataram I., et al. Global burden of cancer in 2008: a systematic analysis of disability-adjusted life-years in 12 world regions. Lancet 2012, 380:1840-1850.
15. Cesarman E., et al. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N. Engl. J. Med. 1995, 332:1186-1191.
16. Soulier J., et al. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood 1995, 86:1276-1280.
17. Gill P.S., et al. Evidence for multiclonality in multicentric Kaposi's sarcoma. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:8257-8261.
18. Duprez R., et al. Evidence for a multiclonal origin of multicentric advanced lesions of Kaposi sarcoma. J. Natl. Cancer Inst. 2007, 99:1086-1094.
19. Gessain A., Duprez R. Spindle cells and their role in Kaposi's sarcoma. Int. J. Biochem. Cell Biol. 2005, 37:2457-2465.
20. Mesri E.A., et al. Kaposi's sarcoma and its associated herpesvirus. Nat. Rev. Cancer 2010, 10:707-719.
21. Boshoff C., et al. Kaposi's sarcoma-associated herpesvirus infects endothelial and spindle cells. Nat. Med. 1995, 1:1274-1278.
22. Staskus K.A., et al. Kaposi's sarcoma-associated herpesvirus gene expression in endothelial (spindle) tumor cells. J. Virol. 1997, 71:715-719.
23. Dupin N., et al. Herpesvirus-like DNA sequences in patients with Mediterranean Kaposi's sarcoma. Lancet 1995, 345:761-762.
24. Beckstead J.H., et al. Evidence for the origin of Kaposi's sarcoma from lymphatic endothelium. Am. J. Pathol. 1985, 119:294-300.
25. Regezi J.A., et al. Oral Kaposi's sarcoma: a 10-year retrospective histopathologic study. J. Oral Pathol. Med. 1993, 22:292-297.
26. Dorfman R.F. Kaposi's sarcoma: evidence supporting its origin from the lymphatic system. Lymphology 1988, 21:45-52.
27. Dupin N., et al. Distribution of human herpesvirus-8 latently infected cells in Kaposi's sarcoma, multicentric Castleman's disease, and primary effusion lymphoma. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:4546-4551.
28. Skobe M., et al. Vascular endothelial growth factor-C (VEGF-C) and its receptors KDR and flt-4 are expressed in AIDS-associated Kaposi's sarcoma. J. Invest. Dermatol. 1999, 113:1047-1053.
29. Marchio S., et al. Vascular endothelial growth factor-C stimulates the migration and proliferation of Kaposi's sarcoma cells. J. Biol. Chem. 1999, 274:27617-27622.
30. Wang H.W., et al. Kaposi sarcoma herpesvirus-induced cellular reprogramming contributes to the lymphatic endothelial gene expression in Kaposi sarcoma. Nat. Genet. 2004, 36:687-693.
31. Carroll P.A., et al. Kaposi's sarcoma-associated herpesvirus infection of blood endothelial cells induces lymphatic differentiation. Virology 2004, 328:7-18.
32. Hong Y.K., et al. Lymphatic reprogramming of blood vascular endothelium by Kaposi sarcoma-associated herpesvirus. Nat. Genet. 2004, 36:683-685.
33. Morris V.A., et al. Activation of Akt through gp130 receptor signaling is required for Kaposi's sarcoma-associated herpesvirus-induced lymphatic reprogramming of endothelial cells. J. Virol. 2008, 82:8771-8779.
34. Vart R.J., et al. Kaposi's sarcoma-associated herpesvirus-encoded interleukin-6 and G-protein-coupled receptor regulate angiopoietin-2 expression in lymphatic endothelial cells. Cancer Res. 2007, 67:4042-4051.
35. Chen D., et al. Intracellular signaling mechanisms and activities of human herpesvirus 8 interleukin-6. J. Virol. 2009, 83:722-733.
36. Morris V.A., et al. The KSHV viral IL-6 homolog is sufficient to induce blood to lymphatic endothelial cell differentiation. Virology 2012, 428:112-120.
37. Ganem D. Kaposi's sarcoma-associated herpesvirus. Fields Virology 2007, 2847-2888. Lippincott Williams & Wilkins. 5th edn. D.M.H. Knipe, M. Peter (Eds.).
38. Yoo J., et al. Kaposin-B enhances the PROX1 mRNA stability during lymphatic reprogramming of vascular endothelial cells by Kaposi's sarcoma herpes virus. PLoS Pathog. 2010, 6:e1001046.
39. McCormick C., Ganem D. The kaposin B protein of KSHV activates the p38/MK2 pathway and stabilizes cytokine mRNAs. Science 2005, 307:739-741.
40. Yoo J., et al. Opposing regulation of PROX1 by interleukin-3 receptor and NOTCH directs differential host cell fate reprogramming by Kaposi sarcoma herpes virus. PLoS Pathog. 2012, 8:e1002770.
41. Aguilar B., et al. Lymphatic reprogramming by Kaposi sarcoma herpes virus promotes the oncogenic activity of the virus-encoded G-protein-coupled receptor. Cancer Res. 2012, 72:5833-5842.
42. Cai X., et al. Kaposi's sarcoma-associated herpesvirus expresses an array of viral microRNAs in latently infected cells. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:5570-5575.
43. Samols M.A., et al. Cloning and identification of a microRNA cluster within the latency-associated region of Kaposi's sarcoma-associated herpesvirus. J. Virol. 2005, 79:9301-9305.
44. Hansen A., et al. KSHV-encoded miRNAs target MAF to induce endothelial cell reprogramming. Genes Dev. 2010, 24:195-205.
45. Pfeffer S., et al. Identification of microRNAs of the herpesvirus family. Nat. Methods 2005, 2:269-276.
46. Cullen B.R. Viral and cellular messenger RNA targets of viral microRNAs. Nature 2009, 457:421-425.
47. Hong Y.K., et al. Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate. Dev. Dyn. 2002, 225:351-357.
48. Petrova T.V., et al. Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J. 2002, 21:4593-4599.
49. Kataoka K. Multiple mechanisms and functions of maf transcription factors in the regulation of tissue-specific genes. J. Biochem. 2007, 141:775-781.
50. Eychene A., et al. A new MAFia in cancer. Nat. Rev. Cancer 2008, 8:683-693.
51. Cui W., et al. Mafs, Prox1, and Pax6 can regulate chicken betaB1-crystallin gene expression. J. Biol. Chem. 2004, 279:11088-11095.
52. Ring B.Z., et al. Regulation of mouse lens fiber cell development and differentiation by the Maf gene. Development 2000, 127:307-317.
53. Kim J.I., et al. Requirement for the c-Maf transcription factor in crystallin gene regulation and lens development. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:3781-3785.
54. Kawauchi S., et al. Regulation of lens fiber cell differentiation by transcription factor c-Maf. J. Biol. Chem. 1999, 274:19254-19260.
55. Wigle J.T., et al. Prox1 function is crucial for mouse lens-fibre elongation. Nat. Genet. 1999, 21:318-322.
56. Wigle J.T., et al. An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J. 2002, 21:1505-1513.
57. Zhou Q., et al. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 2008, 455:627-632.
58. Cheng F., et al. KSHV-initiated notch activation leads to membrane-type-1 matrix metalloproteinase-dependent lymphatic endothelial-to-mesenchymal transition. Cell Host Microbe 2011, 10:577-590.
59. Schatteman G.C., et al. Biology of bone marrow-derived endothelial cell precursors. Am. J. Physiol. Heart Circ. Physiol. 2007, 292:H1-H18.
60. Asahara T., et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ. Res. 1999, 85:221-228.
61. Browning P.J., et al. Identification and culture of Kaposi's sarcoma-like spindle cells from the peripheral blood of human immunodeficiency virus-1-infected individuals and normal controls. Blood 1994, 84:2711-2720.
62. Della Bella S., et al. Peripheral blood endothelial progenitors as potential reservoirs of Kaposi's sarcoma-associated herpesvirus. PLoS ONE 2008, 3:e1520.
63. Grundhoff A., Ganem D. Inefficient establishment of KSHV latency suggests an additional role for continued lytic replication in Kaposi sarcoma pathogenesis. J. Clin. Invest. 2004, 113:124-136.
64. Mutlu A.D., et al. 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 2007, 11:245-258.
65. Wu W., et al. KSHV/HHV-8 infection of human hematopoietic progenitor (CD34+) cells: persistence of infection during hematopoiesis in vitro and in vivo. Blood 2006, 108:141-151.
66. Taddeo A., et al. Circulating endothelial progenitor cells are increased in patients with classic Kaposi's sarcoma. J. Invest. Dermatol. 2008, 128:2125-2128.
67. Pyakurel P., et al. Lymphatic and vascular origin of Kaposi's sarcoma spindle cells during tumor development. Int. J. Cancer 2006, 119:1262-1267.
68. Webster-Cyriaque J. Development of Kaposi's sarcoma in a surgical wound. N. Engl. J. Med. 2002, 346:1207-1210.
69. Barozzi P., et al. Post-transplant Kaposi sarcoma originates from the seeding of donor-derived progenitors. Nat. Med. 2003, 9:554-561.
70. Thorley-Lawson D.A., Gross A. Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N. Engl. J. Med. 2004, 350:1328-1337.
71. Thorley-Lawson D.A., Allday M.J. The curious case of the tumour virus: 50 years of Burkitt's lymphoma. Nat. Rev. Microbiol. 2008, 6:913-924.
72. Mesri E.A., et al. Human herpesvirus-8/Kaposi's sarcoma-associated herpesvirus is a new transmissible virus that infects B cells. J. Exp. Med. 1996, 183:2385-2390.
73. Jenner R.G., et al. Kaposi's sarcoma-associated herpesvirus-infected primary effusion lymphoma has a plasma cell gene expression profile. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:10399-10404.
74. Barozzi P., et al. B cells and herpesviruses: a model of lymphoproliferation. Autoimmun. Rev. 2007, 7:132-136.
75. Ballon G., et al. Kaposi sarcoma herpesvirus (KSHV) vFLIP oncoprotein induces B cell transdifferentiation and tumorigenesis in mice. J. Clin. Invest. 2011, 121:1141-1153.
76. Dupin N., et al. HHV-8 is associated with a plasmablastic variant of Castleman disease that is linked to HHV-8-positive plasmablastic lymphoma. Blood 2000, 95:1406-1412.
77. Fehrmann F., Laimins L.A. Human papillomaviruses: targeting differentiating epithelial cells for malignant transformation. Oncogene 2003, 22:5201-5207.
78. Feller L., et al. Epithelial maturation and molecular biology of oral HPV. Infect. Agent Cancer 2009, 4:16.
79. Lin F.J., et al. Direct transcriptional regulation of neuropilin-2 by COUP-TFII modulates multiple steps in murine lymphatic vessel development. J. Clin. Invest. 2010, 120:1694-1707.
80. Niedt G.W., Prioleau P.G. Kaposi's sarcoma occurring in a dermatome previously involved by herpes zoster. J. Am. Acad. Dermatol. 1988, 18:448-451.
81. Sharma-Walia N., 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. 2010, 6:e1000777.
82. Sadagopan S., et al. 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. 2009, 83:3342-3364.
83. Sivakumar R., et al. Kaposi's sarcoma-associated herpesvirus induces sustained levels of vascular endothelial growth factors A and C early during in vitro infection of human microvascular dermal endothelial cells: biological implications. J. Virol. 2008, 82:1759-1776.
84. Ye F.C., et al. Kaposi's sarcoma-associated herpesvirus promotes angiogenesis by inducing angiopoietin-2 expression via AP-1 and Ets1. J. Virol. 2007, 81:3980-3991.
85. Bala K., et al. Kaposi's sarcoma herpesvirus K15 protein contributes to virus-induced angiogenesis by recruiting PLCgamma1 and activating NFAT1-dependent RCAN1 expression. PLoS Pathog. 2012, 8:e1002927.
86. Rabkin C.S., et al. Monoclonal origin of multicentric Kaposi's sarcoma lesions. N. Engl. J. Med. 1997, 336:988-993.
87. Tammela T., Alitalo K. Lymphangiogenesis: molecular mechanisms and future promise. Cell 2010, 140:460-476.
88. Kriehuber E., et al. Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J. Exp. Med. 2001, 194:797-808.
89. Hirakawa S., et al. Identification of vascular lineage-specific genes by transcriptional profiling of isolated blood vascular and lymphatic endothelial cells. Am. J. Pathol. 2003, 162:575-586.
90. Oliver G., Detmar M. The rediscovery of the lymphatic system: old and new insights into the development and biological function of the lymphatic vasculature. Genes Dev. 2002, 16:773-783.
91. Oliver G. Lymphatic vasculature development. Nat. Rev. Immunol. 2004, 4:35-45.
92. Karkkainen M.J., et al. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat. Immunol. 2004, 5:74-80.
93. Srinivasan R.S., et al. Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. Genes Dev. 2007, 21:2422-2432.
94. Wigle J.T., Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell 1999, 98:769-778.
95. Yaniv K., et al. Live imaging of lymphatic development in the zebrafish. Nat. Med. 2006, 12:711-716.
96. Maby-El Hajjami H., Petrova T.V. Developmental and pathological lymphangiogenesis: from models to human disease. Histochem. Cell Biol. 2008, 130:1063-1078.
97. Oliver G., Alitalo K. The lymphatic vasculature: recent progress and paradigms. Annu. Rev. Cell Dev. Biol. 2005, 21:457-483.
98. Francois M., et al. Sox18 induces development of the lymphatic vasculature in mice. Nature 2008, 456:643-647.
99. Srinivasan R.S., et al. The nuclear hormone receptor Coup-TFII is required for the initiation and early maintenance of Prox1 expression in lymphatic endothelial cells. Genes Dev. 2010, 24:696-707.
100. Oliver G., Srinivasan R.S. Endothelial cell plasticity: how to become and remain a lymphatic endothelial cell. Development 2010, 137:363-372.
101. Oliver G., Harvey N. A stepwise model of the development of lymphatic vasculature. Ann. N. Y. Acad. Sci. 2002, 979:159-165. discussion 188-196.
102. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
103. Vierbuchen T., et al. Direct conversion of fibroblasts to functional neurons by defined factors. Nature 2010, 463:1035-1041.
104. Cobaleda C., et al. Conversion of mature B cells into T cells by dedifferentiation to uncommitted progenitors. Nature 2007, 449:473-477.
105. Johnson N.C., et al. Lymphatic endothelial cell identity is reversible and its maintenance requires Prox1 activity. Genes Dev. 2008, 22:3282-3291.
106. You L.R., et al. Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature 2005, 435:98-104.
107. Grundhoff A., et al. A combined computational and microarray-based approach identifies novel microRNAs encoded by human gamma-herpesviruses. RNA 2006, 12:733-750.
108. Jenner R.G., Boshoff C. The molecular pathology of Kaposi's sarcoma-associated herpesvirus. Biochim. Biophys. Acta 2002, 1602:1-22.