The kynurenine pathway of tryptophan catabolism and AIDS-associated kaposi sarcoma in Africa

Journal of Acquired Immune Deficiency Syndromes

Volumn 70, Issue 3, 2015, Pages 296-303

  Byakwaga, Helen ^a,b   Hunt, Peter W ^b   Laker Oketta, Miriam ^b,c   Glidden, David V ^b   Huang, Yong ^b   Bwana, Bosco M ^a   Mocello, A Rain ^b   Bennett, John ^b   Walusansa, Victoria ^d   Dollard, Sheila C ^e   Bangsberg, David R ^f   Mbidde, Edward K ^c,g   Martin, Jeffrey N ^b  

^a MBARARA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Uganda)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MAKERERE UNIVERSITY   (Uganda)

^d UGANDA CANCER INSTITUTE   (Uganda)

^e CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

^g UGANDA VIRUS RESEARCH INSTITUTE   (Uganda)

Author keywords

Africa; HIV; Indoleamine 2 3 dioxygenase 1; Kaposi sarcoma; Kynurenine; Plasma HIV RNA; Tryptophan

Indexed keywords

CD4 ANTIGEN; INDOLEAMINE 2,3 DIOXYGENASE; KYNURENINE; TRYPTOPHAN; VIRUS RNA;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ADULT; AFRICA; AMINO ACID METABOLISM; CD4 LYMPHOCYTE COUNT; CONFERENCE PAPER; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOSTIMULATION; KAPOSI SARCOMA; LIQUID CHROMATOGRAPHY; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; TANDEM MASS SPECTROMETRY; UGANDAN; AIDS-RELATED OPPORTUNISTIC INFECTIONS; COMPLICATION; GENE EXPRESSION REGULATION; GENETICS; MALARIA; METABOLISM; SARCOMA, KAPOSI; TUBERCULOSIS; VIRUS LOAD;

ADULT; AIDS-RELATED OPPORTUNISTIC INFECTIONS; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; KYNURENINE; MALARIA; MALE; RNA, VIRAL; SARCOMA, KAPOSI; TRYPTOPHAN; TUBERCULOSIS; VIRAL LOAD;

EID: 84944452330     PISSN: 15254135     EISSN: 10779450     Source Type: Journal    
DOI: 10.1097/QAI.0000000000000747     Document Type: Conference Paper

References (58)

1. Hymes KB, Cheung T, Greene JB, et al. Kaposi's sarcoma in homosexual men - A report of eight cases. Lancet. 1981;2:598-600.
2. International Collaboration on HIV and Cancer. Highly active antire-troviral therapy and incidence of cancer in human immunodeficiency virus-infected adults. J Natl Cancer Inst. 2000;92:1823-1830.
3. Franceschi S, Maso LD, Rickenbach M, et al. Kaposi sarcoma incidence in the Swiss HIV Cohort Study before and after highly active antiretroviral therapy. Br J Cancer. 2008;99:800-804.
4. Bray F, Ren JS, Masuyer E, et al. Global estimates of cancer prevalence for 27 sites in the adult population in 2008. Int J Cancer. 2013;132: 1133-1145.
5. Chang Y, Cesarman E, Pessin MS, et al. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science. 1994; 266:1865-1869.
6. Biggar RJ, Chaturvedi AK, Goedert JJ, et al. AIDS-related cancer and severity of immunosuppression in persons with AIDS. J Natl Cancer Inst. 2007;99:962-972.
7. Murray MF. Tryptophan depletion and HIV infection: a metabolic link to pathogenesis. Lancet Infect Dis. 2003;3:644-652.
8. Boasso A, Herbeuval J-P, Hardy AW, et al. HIV inhibits CD4+ T-cell proliferation by inducing indoleamine 2, 3-dioxygenase in plasmacytoid dendritic cells. Blood. 2007;109:3351-3359.
9. Byakwaga H, Boum Y, Huang Y, et al. The kynurenine pathway of tryptophan catabolism, CD4+ T-cell recovery, and mortality among HIV-infected Ugandans initiating antiretroviral therapy. J Infect Dis. 2014; 210:383-391.
10. Favre D, Mold J, Hunt PW, et al. Tryptophan catabolism by indoleamine 2, 3-dioxygenase 1 alters the balance of TH17 to regulatory T cells in HIV disease. Sci Transl Med. 2010;2:32ra36.
11. Mellor AL, Munn DH. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol. 2004;4:762-774.
12. Grant RS, Naif H, Thuruthyil SJ, et al. Induction of indoleamine 2, 3-dioxygenase in primary human macrophages by HIV-1. Redox Rep. 2000;5:105-107.
13. Munn DH, Shafizadeh E, Attwood JT, et al. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J Exp Med. 1999; 189:1363-1372.
14. Frumento G, Rotondo R, Tonetti M, et al. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2, 3-dioxygenase. J Exp Med. 2002;196: 459-468.
15. Munn DH, Zhou M, Attwood JT, et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science. 1998;281:1191-1193.
16. Katz JB, Muller AJ, Prendergast GC. Indoleamine 2, 3-dioxygenase in T-cell tolerance and tumoral immune escape. Immunol Rev. 2008;222:206-221.
17. Martin J, Laker-Oketta M, Walusana V, et al. Antiretrovirals for Kaposi's Sarcoma (ARKS): a randomized trial of protease inhibitor-based antiretroviral therapy for AIDS-associated Kaposi's sarcoma in sub-Saharan Africa. Paper presented at: 21st Conference on Retroviruses and Opportunistic Infections, March 3-6, 2014, Boston, MA.
18. Katabira ET, Kamya MR, Kalyesubula I, et al. National Antiretroviral Treatment Guidelines for Adults, Adolescents, and Children. 3rd ed: Ministry of Health; 2009. Available at: http://library.health.go.ug/publications/service-delivery-diseases-control-prevention-communicable-diseases/hivaids/national-3. Accessed August 28, 2014.
19. Schrocksnadel K, Widner B, Bergant A, et al. Longitudinal study of tryptophan degradation during and after pregnancy. Life Sci. 2003;72: 785-793.
20. Revicki DA, Sorensen S, Wu AW. Reliability and validity of physical and mental health summary scores from the Medical Outcomes Study HIV Health Survey. Med Care. 1998;36:126-137.
21. Filmer D, Pritchett L. The effect of household wealth on educational attainment: evidence from 35 countries. Popul Development Rev. 1999; 25:85-120.
22. Huang Y, Louie A, Yang Q, et al. A simple LC-MS/MS method for determination of kynurenine and tryptophan concentrations in human plasma from HIV-infected patients. Bioanalysis. 2013;5:1397-1407.
23. Pau CP, Lam LL, Spira TJ, et al. Mapping and serodiagnostic application of a dominant epitope within the human herpesvirus 8 ORF 65-encoded protein. J Clin Microbiol. 1998;36:1574-1577.
24. Spira TJ, Lam L, Dollard SC, et al. Comparison of serologic assays and PCR for diagnosis of human herpesvirus 8 infection. J Clin Microbiol. 2000;38:2174-2180.
25. Dollard SC, Nelson KE, Ness PM, et al. Possible transmission of human herpesvirus-8 by blood transfusion in a historical United States cohort. Transfusion. 2005;45:500-503.
26. Lennette ET, Blackbourn DJ, Levy JA. Antibodies to human herpesvirus type 8 in the general population and in Kaposi's sarcoma patients. Lancet. 1996;348:858-861.
27. Dollard SC, Butler LM, Jones AM, et al. Substantial regional differences in human herpesvirus 8 seroprevalence in sub-Saharan Africa: insights on the origin of the "Kaposi's sarcoma belt". Int J Cancer. 2010;127: 2395-2401.
28. Chaabna K, Bray F, Wabinga HR, et al. Kaposi sarcoma trends in Uganda and Zimbabwe: a sustained decline in incidence? Int J Cancer. 2013;133:1197-1203.
29. Jacobson LP, Jenkins FJ, Springer G, et al. Interaction of human immunodeficiency virus type 1 and human herpesvirus type 8 infections on the incidence of Kaposi's sarcoma. JInfect Dis. 2000;181:1940-1949.
30. Sullivan PS, Hanson DL, Chu SY, et al. Epidemiology of anemia in human immunodeficiency virus (HIV)-infected persons: results from the multistate adult and adolescent spectrum of HIV disease surveillance project. Blood. 1998;91:301-308.
31. Maas JJ, Dukers N, Krol A, et al. Body mass index course in asymptomatic HIV-infected homosexual men and the predictive value of a decrease of body mass index for progression to AIDS. J Acquir Immune Defic Syndr Hum Retrovirol. 1998;19:254-259.
32. Schechter MT, Hogg RS, Aylward B, et al. Higher socioeconomic status is associated with slower progression of HIV infection independent of access to health care. J Clin Epidemiol. 1994;47:59-67.
33. White IR, Royston P, Wood AM. Multiple imputation using chained equations: Issues and guidance for practice. Stat Med. 2011;30:377-399.
34. Huengsberg M, Winer JB, Gompels M, et al. Serum kynurenine-to-tryptophan ratio increases with progressive disease in HIV-infected patients. Clin Chem. 1998;44:858-862.
35. Tetsutani K, To H, Torii M, et al. Malaria parasite induces tryptophan-related immune suppression in mice. Parasitology. 2007;134:923-930.
36. Gething PW, Patil AP, Smith DL, et al. A new world malaria map: Plasmodium falciparum endemicity in 2010. Malar J. 2011;10:378.
37. World Health Organization. Global Tuberculosis Control Report 2013. Geneva. Available at: http://www.who.int/tb/publications/global-report/en/. Accessed August 28, 2014.
38. Blumenthal A, Nagalingam G, Huch JH, et al. M. tuberculosis induces potent activation of IDO-1, but this is not essential for the immunological control of infection. PLoS One. 2012;7:e37314.
39. Munn DH, Sharma MD, Hou D, et al. Expression of indoleamine 2, 3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. J Clin Invest. 2004;114:280-290.
40. Fallarino F, Grohmann U, You S, et al. The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor zeta-chain and induce a regulatory phenotype in naive T cells. J Immunol. 200;176:6752-6761.
41. Weinlich G, Murr C, Richardsen L, et al. Decreased serum tryptophan concentration predicts poor prognosis in malignant melanoma patients. Dermatology. 2007;214:8-14.
42. Suzuki Y, Suda T, Furuhashi K, et al. Increased serum kynurenine/tryptophan ratio correlates with disease progression in lung cancer. Lung Cancer. 2010;67:361-365.
43. Maby-El Hajjami H, Ame-Thomas P, Pangault C, et al. Functional alteration of the lymphoma stromal cell niche by the cytokine context: role of indoleamine-2, 3 dioxygenase. Cancer Res. 2009;69:3228-3237.
44. French PD, Harris JR, Mercey DE. The Koebner phenomenon and AIDS-related Kaposi's sarcoma. Br J Dermatol. 1994;131:746-747.
45. Monini P, Colombini S, Sturzl M, et al. Reactivation and persistence of human herpesvirus-8 infection in B cells and monocytes by Th-1 cytokines increased in Kaposi's sarcoma. Blood. 1999;93:4044-4058.
46. Ascherl G, Hohenadl C, Schatz O, et al. Infection with human immunodeficiency virus-1 increases expression of vascular endothelial cell growth factor in T cells: implications for acquired immunodeficiency syndrome-associated vasculopathy. Blood. 1999;93:4232-4241.
47. Zimmermann A, Hauka S, Maywald M, et al. Checks and balances between human cytomegalovirus replication and indoleamine-2, 3-dioxygenase. J Gen Virol. 2014;95:659-670.
48. Wacholder S, McLaughlin JK, Silverman DT, et al. Selection of controls in case-control studies. I. Principles. Am J Epidemiol. 1992;135:1019-1028.
49. Reina Ortiz M, Schreiber F, Benitez S, et al. Effects of chronic ascariasis and trichuriasis on cytokine production and gene expression in human blood: a cross-sectional study. PLoS Negl Trop Dis. 2011;5:e1157.
50. Bell LV, Else KJ. Regulation of colonic epithelial cell turnover by IDO contributes to the innate susceptibility of SCID mice to Trichuris muris infection. Parasite Immunol. 2011;33:244-249.
51. Brooker S, Kabatereine NB, Smith JL, et al. An updated atlas of human helminth infections: the example of East Africa. Int J Health Geogr. 2009;8:42.
52. Guiguet M, Boue F, Cadranel J, et al. Effect of immunodeficiency, HIV viral load, and antiretroviral therapy on the risk of individual malignancies (FHDH-ANRS CO4): a prospective cohort study. Lancet Oncol. 2009;10:1152-1159.
53. Barillari G, Sgadari C, Fiorelli V, et al. The Tat protein of human immunodeficiency virus type-1 promotes vascular cell growth and locomotion by engaging the alpha5beta1 and alphavbeta3 integrins and by mobilizing sequestered basic fibroblast growth factor. Blood. 1999;94: 663-672.
54. Maskew M, Fox MP, van Cutsem G, et al. Treatment response and mortality among patients starting antiretroviral therapy with and without Kaposi sarcoma: a cohort study. PLoS One. 2013;8:e64392.
55. Nemeth E, Rivera S, Gabayan V, et al. IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J Clin Invest. 2004;113:1271-1276.
56. Kreuzer KA, Rockstroh JK, Jelkmann W, et al. Inadequate erythropoietin response to anaemia in HIV patients: relationship to serum levels of tumour necrosis factor-alpha, interleukin-6 and their soluble receptors. Br J Haematol. 1997;96:235-239.
57. Weprin L, Zollinger R, Clausen K, et al. Kaposi's sarcoma: endoscopic observations of gastric and colon involvement. J Clin Gastroenterol. 1982;4:357-360.
58. Schmidt C. Yuan Chang and Patrick Moore: teaming up to hunt down cancer-causing viruses. J Natl Cancer Inst. 2008;100:524-529.