Viral profiling identifies multiple subtypes of Kaposi’s sarcoma

mBio

Volumn 5, Issue 5, 2014, Pages

  Hosseinipour, Mina C ^a,b,c   Sweet, Kristen M ^a   Xiong, Jie ^c,d   Namarika, Dan ^e   Mwafongo, Albert ^b   Nyirenda, Michael ^f   Chiwoko, Loreen ^b   Kamwendo, Deborah ^b   Hoffman, Irving ^a,b   Lee, Jeannette ^g,h   Phiri, Sam ^e   Vahrson, Wolfgang ⁱ   Damania, Blossom ^a,c   Dittmer, Dirk P ^a,c,h  

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

^b UNC   (Malawi)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

^d The University of North Carolina at Chapel Hill   (United States)

^e KAMUZU CENTRAL HOSPITAL   (Malawi)

^f LIGHTHOUSE TRUST   (Malawi)

^g UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^h AIDS Malignancy Consortium (AMC)   (Switzerland)

ⁱ GENEDATA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; CD4 ANTIGEN; MICRORNA; VIRUS RNA; MESSENGER RNA; VIRUS DNA;

ADULT; ARTICLE; CANCER CLASSIFICATION; CROSS-SECTIONAL STUDY; FEMALE; GENE EXPRESSION PROFILING; GENE LOCUS; GENETIC TRANSCRIPTION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; KAPOSI SARCOMA; LATENT PERIOD; MAJOR CLINICAL STUDY; MALAWI; MALE; OPEN READING FRAME; REAL TIME POLYMERASE CHAIN REACTION; VIRUS GENOME; VIRUS LOAD; BODY MASS; CD4 LYMPHOCYTE COUNT; CLASSIFICATION; COMPLICATION; GENETICS; HIV INFECTIONS; ISOLATION AND PURIFICATION; METABOLISM; POLYMERASE CHAIN REACTION; SARCOMA, KAPOSI; VIROLOGY;

ADULT; BODY MASS INDEX; CD4 LYMPHOCYTE COUNT; CROSS-SECTIONAL STUDIES; DNA, VIRAL; FEMALE; HERPESVIRUS 8, HUMAN; HIV INFECTIONS; HUMANS; MALAWI; MALE; POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, VIRAL; SARCOMA, KAPOSI; VIRAL LOAD;

EID: 84908430669     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01633-14     Document Type: Article

References (58)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. 2011. Global cancer statistics. CA Cancer J. Clin. 61:69-90. http://dx.doi.org/10.3322/ caac.20107.
2. Semeere AS, Busakhala N, Martin JN. 2012. Impact of antiretroviral therapy on the incidence of Kaposi's sarcoma in resource-rich and resource-limited settings. Curr. Opin. Oncol. 24:522-530. http:// dx.doi.org/10.1097/CCO.0b013e328355e14b.
3. Gopal S, Achenbach CJ, Yanik EL, Dittmer DP, Eron JJ, Engels EA. 2014. Moving forward in HIV-associated cancer. J. Clin. Oncol. 32: 876-880. http://dx.doi.org/10.1200/JCO.2013.53.1376.
4. Yanik EL, Napravnik S, Cole SR, Achenbach CJ, Gopal S, Olshan A, Dittmer DP, Kitahata MM, Mugavero MJ, Saag M, Moore RD, Mayer K, Mathews WC, Hunt PW, Rodriguez B, Eron JJ. 2013. Incidence and timing of cancer in HIV-infected individuals following initiation of combination antiretroviral therapy. Clin. Infect. Dis. 57:756 -764. http:// dx.doi.org/10.1093/cid/cit369.
5. Yanik EL, Tamburro K, Eron JJ, Damania B, Napravnik S, Dittmer DP. 2013. Recent cancer incidence trends in an observational clinical cohort of HIV-infected patients in the US, 2000-2011. Infect. Agents Cancer 8:18. http://dx.doi.org/10.1186/1750-9378-8-18.
6. Shiels MS, Pfeiffer RM, Hall HI, Li J, Goedert JJ, Morton LM, Hartge P, Engels EA. 2011. Proportions of Kaposi sarcoma, selected non- Hodgkin lymphomas, and cervical cancer in the United States occurring in persons with AIDS, 1980-2007. JAMA 305:1450 -1459. http:// dx.doi.org/10.1001/jama.2011.396.
7. Dittmer DP, Richards KL, Damania B. 2012. Treatment of Kaposi sarcoma-associated herpesvirus-associated cancers. Front. Microbiol. 3:141. http://dx.doi.org/10.3389/fmicb.2012.00141.
8. Krown SE. 2011. Treatment strategies for Kaposi sarcoma in sub-Saharan Africa: challenges and opportunities. Curr. Opin. Oncol. 23:463- 468. http://dx.doi.org/10.1097/CCO.0b013e328349428d.
9. Krown SE, Lee JY, Dittmer DP, AIDS Malignancy Consortium. 2008. More on HIV-associated Kaposi's sarcoma. N. Engl. J. Med. 358:535-536; author reply, 536. http://dx.doi.org/10.1056/NEJMc072994.
10. Nguyen HQ, Magaret AS, Kitahata MM, Van Rompaey SE, Wald A, Casper C. 2008. Persistent Kaposi sarcoma in the era of highly active antiretroviral therapy: characterizing the predictors of clinical response. AIDS 22:937-945. http://dx.doi.org/10.1097/QAD.0b013e3282ff6275.
11. Cox CM, El-Mallawany NK, Kabue M, Kovarik C, Schutze GE, Kazembe PN, Mehta PS. 2013. Clinical characteristics and outcomes of HIV-infected children diagnosed with Kaposi sarcoma in Malawi and Botswana. Pediatr. Blood Cancer 60:1274-1280. http://dx.doi.org/10.1002/ pbc.24516.
12. Letang E, Lewis JJ, Bower M, Mosam A, Borok M, Campbell TB, Naniche D, Newsom-Davis T, Shaik F, Fiorillo S, Miro JM, Schellenberg D, Easterbrook PJ. 2013. Immune reconstitution inflammatory syndrome associated with Kaposi sarcoma: higher incidence and mortality in Africa than in the UK. AIDS 27:1603-1613. http://dx.doi.org/10.1097/ QAD.0b013e328360a5a1.
13. Achenbach CJ, Harrington RD, Dhanireddy S, Crane HM, Casper C, Kitahata MM. 2012. Paradoxical immune reconstitution inflammatory syndrome in HIV-infected patients treated with combination antiretroviral therapy after AIDS-defining opportunistic infection. Clin. Infect. Dis. 54:424-433. http://dx.doi.org/10.1093/cid/cir802.
14. Bower M, Nelson M, Young AM, Thirlwell C, Newsom-Davis T, Man dalia S, Dhillon T, Holmes P, Gazzard BG, Stebbing J. 2005. Immune reconstitution inflammatory syndrome associated with Kaposi's sarcoma. J. Clin. Oncol. 23:5224 -5228. http://dx.doi.org/10.1200/ JCO.2005.14.597.
15. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, Knowles DM, Moore PS. 1994. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266:1865-1869. http:// dx.doi.org/10.1126/science.7997879.
16. Dittmer DP, Damania B. 2013. Kaposi sarcoma associated herpesvirus pathogenesis (KSHV)-an update. Curr. Opin. Virol. 3:238-244. http:// dx.doi.org/10.1016/j.coviro.2013.05.012.
17. Davis DA, Singer KE, Reynolds IP, Haque M, Yarchoan R. 2007. Hypoxia enhances the phosphorylation and cytotoxicity of ganciclovir and zidovudine in Kaposi's sarcoma-associated herpesvirus infected cells. Cancer Res. 67:7003-7010. http://dx.doi.org/10.1158/0008-5472.CAN- 07-0939.
18. Kedes DH, Ganem D. 1997. Sensitivity of Kaposi's sarcoma-associated herpesvirus replication to antiviral drugs. Implications for potential therapy. J. Clin. Invest. 99:2082-2086. http://dx.doi.org/10.1172/JCI119380.
19. Neyts J, De Clercq E. 1997. Antiviral drug susceptibility of human herpesvirus. Antimicrob. Agents Chemother. 41:2754-2756.
20. Dittmer D, Stoddart C, Renne R, Linquist-Stepps V, Moreno ME, Bare C, McCune JM, Ganem D. 1999. Experimental transmission of Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8) to SCID-hu Thy/Liv mice. J. Exp. Med. 190:1857-1868. http://dx.doi.org/10.1084/ jem.190.12.1857.
21. Cannon JS, Hamzeh F, Moore S, Nicholas J, Ambinder RF. 1999. Human herpesvirus 8-encoded thymidine kinase and phosphotransferase homologues confer sensitivity to ganciclovir. J. Virol. 73:4786-4793.
22. Fu DX, Tanhehco Y, Chen J, Foss CA, Fox JJ, Chong JM, Hobbs RF, Fukayama M, Sgouros G, Kowalski J, Pomper MG, Ambinder RF. 2008. Bortezomib-induced enzyme-targeted radiation therapy in herpesvirusassociated tumors. Nat. Med. 14:1118-1122. http://dx.doi.org/10.1038/ nm.1864.
23. Kurokawa M, Ghosh SK, Ramos JC, Mian AM, Toomey NL, Cabral L, Whitby D, Barber GN, Dittmer DP, Harrington WJ, Jr. 2005. Azidothymidine inhibits NF-kappaB and induces Epstein-Barr virus gene expression in Burkitt lymphoma. Blood 106:235-240. http://dx.doi.org/ 10.1182/blood-2004-09-3748.
24. Feng WH, Israel B, Raab-Traub N, Busson P, Kenney SC. 2002. Chemotherapy induces lytic EBV replication and confers ganciclovir susceptibility to EBV-positive epithelial cell tumors. Cancer Res. 62:1920-1926.
25. Krown SE, Dittmer DP, Cesarman E. 2011. Pilot study of oral valganciclovir therapy in patients with classic Kaposi sarcoma. J. Infect. Dis. 203: 1082-1086. http://dx.doi.org/10.1093/infdis/jiq177.
26. Little RF, Merced-Galindez F, Staskus K, Whitby D, Aoki Y, Humphrey R, Pluda JM, Marshall V, Walters M, Welles L, Rodriguez-Chavez IR, Pittaluga S, Tosato G, Yarchoan R. 2003. A pilot study of cidofovir in patients with Kaposi sarcoma. J. Infect. Dis. 187:149 -153. http:// dx.doi.org/10.1086/346159.
27. Uldrick TS, Polizzotto MN, Aleman K, O'Mahony D, Wyvill KM, Wang V, Marshall V, Pittaluga S, Steinberg SM, Tosato G, Whitby D, Little RF, Yarchoan R. 2011. High-dose zidovudine plus valganciclovir for Kaposi sarcoma herpesvirus-associated multicentric Castleman disease: a pilot study of virus-activated cytotoxic therapy. Blood 117:6977-6986. http://dx.doi.org/10.1182/blood-2010-11-317610.
28. Pantanowitz L, Früh K, Marconi S, Moses AV, Dezube BJ. 2008. Pathology of rituximab-induced Kaposi sarcoma flare. BMC Clin. Pathol. 8:7. http://dx.doi.org/10.1186/1472-6890-8-7.
29. Dittmer DP. 2003. Transcription profile of Kaposi's sarcoma-associated herpesvirus in primary Kaposi's sarcoma lesions as determined by realtime PCR arrays. Cancer Res. 63:2010-2015.
30. Dittmer DP. 2011. Restricted Kaposi's sarcoma (KS) herpesvirus transcription in KS lesions from patients on successful antiretroviral therapy. mBio 2(6):e00138-11. http://dx.doi.org/10.1128/mBio.00138-11.
31. Dupin N, Fisher C, Kellam P, Ariad S, Tulliez M, Franck N, van Marck E, Salmon D, Gorin I, Escande JP, Weiss RA, Alitalo K, Boshoff C. 1999. 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. 96:4546-4551. http://dx.doi.org/ 10.1073/pnas.96.8.4546.
32. Dittmer D, Lagunoff M, Renne R, Staskus K, Haase A, Ganem D. 1998. A cluster of latently expressed genes in Kaposi's sarcoma-associated herpesvirus. J. Virol. 72:8309-8315.
33. Pantanowitz L, Otis CN, Dezube BJ. 2010. Immunohistochemistry in Kaposi's sarcoma. Clin. Exp. Dermatol. 35:68 -72. http://dx.doi.org/ 10.1111/j.1365-2230.2009.03707.x.
34. Stürzl M, Brandstetter H, Roth WK. 1992. Kaposi's sarcoma: a review of gene expression and ultrastructure of KS spindle cells in vivo. AIDS Res. Hum. Retroviruses 8:1753-1763. http://dx.doi.org/10.1089/ aid.1992.8.1753.
35. Borok M, Fiorillo S, Gudza I, Putnam B, Ndemera B, White IE, Gwanzura L, Schooley RT, Campbell TB. 2010. Evaluation of plasma human herpesvirus 8 DNA as a marker of clinical outcomes during antiretroviral therapy for AIDS-related Kaposi sarcoma in Zimbabwe. Clin. Infect. Dis. 51:342-349. http://dx.doi.org/10.1086/654800.
36. Mosam A, Shaik F, Uldrick TS, Esterhuizen T, Friedland GH, Scadden DT, Aboobaker J, Coovadia HM. 2012. A randomized controlled trial of highly active antiretroviral therapy versus highly active antiretroviral therapy and chemotherapy in therapy-naive patients with HIV-associated Kaposi sarcoma in South Africa. J. Acquir. Immune Defic. Syndr. 60: 150-157. http://dx.doi.org/10.1097/QAI.0b013e318251aedd.
37. Bihl F, Mosam A, Henry LN, Chisholm JV, III, Dollard S, Gumbi P, Cassol E, Page T, Mueller N, Kiepiela P, Martin JN, Coovadia HM, Scadden DT, Brander C. 2007. Kaposi's sarcoma-associated herpesvirusspecific immune reconstitution and antiviral effect of combined HAART/ chemotherapy in HIV clade C-infected individuals with Kaposi's sarcoma. AIDS 21:1245-1252. http://dx.doi.org/10.1097/QAD.0b013e328182df03.
38. Johnston C, Orem J, Okuku F, Kalinaki M, Saracino M, Katongole- Mbidde E, Sande M, Ronald A, McAdam K, Huang ML, Drolette L, Selke S, Wald A, Corey L, Casper C. 2009. Impact of HIV infection and Kaposi sarcoma on human herpesvirus-8 mucosal replication and dissemination in Uganda. PLoS One 4:e4222. http://dx.doi.org/10.1371/ journal.pone.0004222.
39. Nasti G, Martellotta F, Berretta M, Mena M, Fasan M, Di Perri G, Talamini R, Pagano G, Montroni M, Cinelli R, Vaccher E, D'Arminio Monforte A, Tirelli U, GICAT, ICONA. 2003. Impact of highly active antiretroviral therapy on the presenting features and outcome of patients with acquired immunodeficiency syndrome-related Kaposi sarcoma. Cancer 98:2440-2446. http://dx.doi.org/10.1002/cncr.11816.
40. Martin JN, Ganem DE, Osmond DH, Page-Shafer KA, Macrae D, Kedes DH. 1998. Sexual transmission and the natural history of human herpesvirus 8 infection. N. Engl. J. Med. 338:948 -954. http://dx.doi.org/ 10.1056/NEJM199804023381403.
41. Butler LM, Dorsey G, Hladik W, Rosenthal PJ, Brander C, Neilands TB, Mbisa G, Whitby D, Kiepiela P, Mosam A, Mzolo S, Dollard SC, Martin JN. 2009. Kaposi sarcoma-associated herpesvirus (KSHV) seroprevalence in population-based samples of African children: evidence for at least 2 patterns of KSHV transmission. J. Infect. Dis. 200:430 - 438. http:// dx.doi.org/10.1086/600103.
42. Maurer T, Ponte M, Leslie K. 2007. HIV-associated Kaposi's sarcoma with a high CD4 count and a low viral load. N. Engl. J. Med. 357: 1352-1353. http://dx.doi.org/10.1056/NEJMc070508.
43. Cianfrocca M, Lee S, Von Roenn J, Tulpule A, Dezube BJ, Aboulafia DM, Ambinder RF, Lee JY, Krown SE, Sparano JA. 2010. Randomized trial of paclitaxel versus pegylated liposomal doxorubicin for advanced human immunodeficiency virus-associated Kaposi sarcoma: evidence of symptom palliation from chemotherapy. Cancer 116:3969-3977. http:// dx.doi.org/10.1002/cncr.25362.
44. Cassol E, Page T, Mosam A, Friedland G, Jack C, Lalloo U, Kopetka J, Patterson B, Esterhuizen T, Coovadia HM. 2005. Therapeutic response of HIV-1 subtype C in African patients coinfected with either Mycobacterium tuberculosis or human herpesvirus-8. J. Infect. Dis. 191:324-332. http://dx.doi.org/10.1086/427337.
45. Martín-Carbonero L, Palacios R, Valencia E, Saballs P, Sirera G, Santos I, Baldobí F, Alegre M, Goyenechea A, Pedreira J, González del Castillo J, Martínez-Lacasa J, Ocampo A, Alsina M, Santos J, Podzamczer D, González-Lahoz J, Caelyx/Kaposi's Sarcoma Spanish Group. 2008. Long-term prognosis of HIV-infected patients with Kaposi sarcoma treated with pegylated liposomal doxorubicin. Clin. Infect. Dis. 47: 410-417. http://dx.doi.org/10.1086/589865.
46. Bower M, Dalla Pria A, Coyle C, Andrews E, Tittle V, Dhoot S, Nelson M. 2014. Prospective stage-stratified approach to AIDS-related Kaposi's sarcoma. J. Clin. Oncol. 32:409 - 414. http://dx.doi.org/10.1200/ JCO.2013.51.6757.
47. Fakhari FD, Dittmer DP. 2002. Charting latency transcripts in Kaposi's sarcoma-associated herpesvirus by whole-genome real-time quantitative PCR. J. Virol. 76:6213-6223. http://dx.doi.org/10.1128/JVI.76.12.6213- 6223.2002.
48. An FQ, Folarin HM, Compitello N, Roth J, Gerson SL, McCrae KR, Fakhari FD, Dittmer DP, Renne R. 2006. Long-term-infected telomerase-immortalized endothelial cells: a model for Kaposi's sarcomaassociated herpesvirus latency in vitro and in vivo. J. Virol. 80:4833-4846. http://dx.doi.org/10.1128/JVI.80.10.4833-4846.2006.
49. Staudt MR, Kanan Y, Jeong JH, Papin JF, Hines-Boykin R, Dittmer DP. 2004. The tumor microenvironment controls primary effusion lymphoma growth in vivo. Cancer Res. 64:4790-4799. http://dx.doi.org/10.1158/ 0008-5472.CAN-03-3835.
50. Chandriani S, Ganem D. 2010. Array-based transcript profiling and limiting-dilution reverse transcription-PCR analysis identify additional latent genes in Kaposi's sarcoma-associated herpesvirus. J. Virol. 84: 5565-5573. http://dx.doi.org/10.1128/JVI.02723-09.
51. Chang HH, Ganem D. 2013. A unique herpesviral transcriptional program in KSHV-infected lymphatic endothelial cells leads to mTORC1 activation and rapamycin sensitivity. Cell Host Microbe 13:429-440. http://dx.doi.org/10.1016/j.chom.2013.03.009.
52. Wang L, Dittmer DP, Tomlinson CC, Fakhari FD, Damania B. 2006. Immortalization of primary endothelial cells by the K1 protein of Kaposi's sarcoma-associated herpesvirus. Cancer Res. 66:3658 -3666. http:// dx.doi.org/10.1158/0008-5472.CAN-05-3680.
53. Mutlu AD, Cavallin LE, Vincent L, Chiozzini C, Eroles P, Duran EM, Asgari Z, Hooper AT, La Perle KM, Hilsher C, Gao SJ, Dittmer DP, Rafii S, Mesri EA. 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. http://dx.doi.org/ 10.1016/j.ccr.2007.01.015.
54. Arias C, Weisburd B, Stern-Ginossar N, Mercier A, Madrid AS, Bellare P, Holdorf M, Weissman JS, Ganem D. 2014. 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 Pathog. 10:e1003847. http://dx.doi.org/10.1371/ journal.ppat.1003847.
55. Canny SP, Reese TA, Johnson LS, Zhang X, Kambal A, Duan E, Liu CY, Virgin HW. 2014. Pervasive transcription of a herpesvirus genome generates functionally important RNAs. mBio 5(2):e01033-13. http:// dx.doi.org/10.1128/mBio.01033-13.
56. Jenner RG, Albà MM, Boshoff C, Kellam P. 2001. Kaposi's sarcomaassociated herpesvirus latent and lytic gene expression as revealed byDNA arrays. J. Virol. 75:891-902. http://dx.doi.org/10.1128/JVI.75.2.891- 902.2001.
57. Paulose-Murphy M, Ha NK, Xiang C, Chen Y, Gillim L, Yarchoan R, Meltzer P, Bittner M, Trent J, Zeichner S. 2001. Transcription program of human herpesvirus 8 (Kaposi's sarcoma-associated herpesvirus). J. Virol. 75:4843-4853. http://dx.doi.org/10.1128/JVI.75.10.4843-4853.2001.
58. Papin J, Vahrson W, Hines-Boykin R, Dittmer DP. 2005. Real-time quantitative PCR analysis of viral transcription. Methods Mol. Biol. 292: 449-480.