Increases in T cell telomere length in HIV infection after antiretroviral combination therapy for HIV-1 infection implicate distinct population dynamics in CD4+ and CD8+ T cells

Clinical Immunology

Volumn 92, Issue 1, 1999, Pages 14-24

  Kaushal, Sumesh ^a   Landay, Alan L ^b   Lederman, Michael M ^c   Connick, Elizabeth ^d   Spritzler, John ^e   Kuritzkes, Daniel R ^d   Kessler, Harold ^b   Levine, Bruce L ^a   St Louis, Daniel C ^a   June, Carl H ^a  

^a HENRY M JACKSON FOUNDATION FOR THE ADVANCEMENT OF MILITARY MEDICINE   (United States)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^e HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Antiretroviral therapy; HIV 1; Immunodeficiency; Telomerase; Telomere

Indexed keywords

LAMIVUDINE; RITONAVIR; ZIDOVUDINE;

ADULT; ANTIVIRAL ACTIVITY; ARTICLE; CLINICAL ARTICLE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LYMPHOCYTE PROLIFERATION; POPULATION DYNAMICS; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TELOMERE; VIRUS INHIBITION; VIRUS REPLICATION;

EID: 0032977717     PISSN: 15216616     EISSN: None     Source Type: Journal    
DOI: 10.1006/clim.1999.4726     Document Type: Article

References (46)

1. Harley C. B., Futcher A. B., Greider C. W. Telomeres shorten during ageing of human fibroblasts. Nature. 345:1990;458-460.
2. Vaziri H., Schachter F., Uchida I., Wei L., Zhu X., Effros R., Cohen D., Harley C. B. Loss of telomeric DNA during aging of normal and trisomy 21 human lymphocytes. Am. J. Hum. Genet. 52:1993;661-667.
3. Weng N.-P., Levine B. L., June C. H., Hodes R. J. Human naive and memory T lymphocytes differ in telomeric length and replicative potential. Proc. Natl. Acad. Sci. USA. 92:1995;11091-11094.
4. Linskens M. H., Harley C. B., West M. D., Campisi J., Hayflick L. Replicative senescence and cell death. Science. 267:1995;17.
5. Effros R. B., Pawelec G. Replicative senescence of T cells: Does the Hayflick Limit lead to immune exhaustion. Immunol. Today. 18:1997;450-454.
6. Ho D. D., Neumann A. U., Perelson A. S., Chen W., Leonard J. M., Markowitz M. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature. 373:1995;123-126.
7. Wei X., Ghosh S. K., Taylor M. E., Johnson V. A., Emini E. A., Deutsch P., Lifson J. D., Bonhoeffer S., Nowak M. A., Hahn B. H., Saag M., Shaw G. M. Viral dynamics in human immunodeficiency virus type 1 infection. Nature. 373:1995;117-122.
8. von Boehmer H. Immunology. Nature. 362:1993;696-696.
9. + T cell turnover. Science. 274:1996;1543-1547.
10. Effros R. B., Allsopp R., Chiu C. P., Hausner M. A., Hirji K., Wang L., Harley C. B., VIlleponteau B., West M. D., Giorgi J. V. Shortened telomeres in the expanded CD28-CD8+ cell subset in HIV disease implicate replicative senescence in HIV pathogenesis. AIDS. 10:1996;F17-F22.
11. Palmer L. D., Weng N.-P., Levine B. L., June C. H., Lane H. C., Hodes R. J. Telomere length, telomerase activity, and replicative potential in HIV infection: Analysis of CD4+ and CD8+ T cells from HIV-discordant monozygotic twins. J. Exp. Med. 185:1997;1381-1386.
12. Wolthers K. C., Noest A. J., Otto S. A., Miedema F., de Boer R. J. Normal telomere lengths in naive and memory CD4+ T cells in HIV-1 infection: A mathematical interpretation. J. Immunol. 1998.
13. de Boer R. J., Noest A. J. T cell renewal rates, telomerase, and telomere length shortening. J. Immunol. 160:1998;5832-5837.
14. Mohri H., Bonhoeffer S., Monard S., Perelson A. S., Ho D. D. Rapid turnover of T lymphocytes in SIV-infected rhesus macaques. Science. 279:1998;1223-1227.
15. + T lymphocyte turnover in simian immunodeficiency virus-infected macaques. Proc. Natl. Acad. Sci. USA. 95:1998;6388-6393.
16. Kelleher A. D., Carr A., Zaunders J., Cooper D. A. Alterations in the immune response of human immunodeficiency virus (HIV)-infected subjects treated with an HIV-specific protease inhibitor, ritonavir. J. Infect. Dis. 173:1996;321-329.
17. Autran B., Carcelain G., Li T. S., Blanc C., Mathez D., Tubiana R., Katlama C., Debre P., Leibowitch J. Positive effects of combined antiretroviral therapy on CD4+ T cell homeostasis and function in advanced HIV disease. Science. 277:1997;112-116.
18. Pakker N. G., Notermans D. W., de Boer R. J., Roos M. T., De Wolf F., Hill A., Leonard J. M., Danner S. A., Miedema F., Schellekens P. T. Biphasic kinetics of peripheral blood T cells after triple combination therapy in HIV-1 infection: A composite of redistribution and proliferation. Nat. Med. 4:1998;208-214.
19. Fleury S., de Boer R. J., Rizzardi G. P., Wolthers K. C., Otto S. A., Welbon C. C., Graziosi C., Knabenhans C., Soudeyns H., Bart P. A., Gallant S., Corpataux J. M., Gillet M., Meylan P., Schnyder P., Meuwly J. Y., Spreen W., Glauser M. P., Miedema F., Pantaleo G. Limited CD4+ T-cell renewal in early HIV-1 infection: Effect of highly active antiretroviral therapy. Nat. Med. 4:1998;794-801.
20. Gorochov G., Neumann A. U., Kereveur A., Parizot C., Li T., Katlama C., Karmochkine M., Raguin G., Autran B., Debre P. Perturbation of CD4+ and CD8+ T-cell repertoires during progression to AIDS and regulation of the CD4+ repertoire during antiviral therapy. Nat. Med. 4:1998;215-221.
21. Connors M., Kovacs J. A., Krevat S., Gea-Banacloche J. C., Sneller M. C., Flanigan M., Metcalf J. A., Walker R. E., Falloon J., Baseler M., Feuerstein I., Masur H., Lane H. C. HIV infection induces changes in CD4+ T-cell phenotype and depletions within the CD4+ T-cell repertoire that are not immediately restored by antiviral or immune-based therapies. Nat. Med. 3:1997;533-540.
22. Hellerstein M. K., McCune J. M. T cell turnover in HIV-1 disease. Immunity. 7:1997;583-589.
23. Mackall C. L., Gress R. E. Thymic aging and T-cell regeneration. Immunol. Rev. 160:1997;91-102.
24. Kaushal S. Telomeric terminal restriction fragment (TRF). Michael N. L. Methods in Molecular Medicine. 1998;237-242 Humana Press, Totowa.
25. Oexle K. Telomere length distribution and Southern blot analysis. J. Theor. Biol. 190:1998;369-377.
26. Kim N. W., Piatyszek M. A., Prowse K. R., Harley C. B., West M. D., Ho P. L., Coviello G. M., Wright W. E., Weinrich S. L., Shay J. W. Specific association of human telomerase activity with immortal cells and cancer. Science. 266:1994;2011-2015.
27. Lederman M., Connick E., Landay A., Kuritzkes D. R., Spritzler J., St. Clair M., Kotzin B. L., Fox L., Chiozzi M. H., Leonard J. M., Rousseau F., Wade M., Roe J. D., Martinez A., Kessler H. Immunologic responses associated with 12 weeks of combination antiretroviral therapy consisting of zidovudine, lamivudine, and ritonavir: Results of AIDS Clinical Trials Group Protocol 315. J. Infect. Dis. 178:1998;70-79.
28. Hiyama K., Hirai Y., Kyoizumi S., Akiyama M., Hiyama E., Piatyszek M. A., Shay J. W., Ishioka S., Yamakido M. Activation of telomerase in human lymphocytes and hematopoietic progenitor cells. J. Immunol. 155:1995;3711-3715.
29. Monteiro J., Batliwalla F., Ostrer H., Gregersen P. K. Shortened telomeres in clonally expanded CD28-CD8+ T cells imply a replicative history that is distinct from their CD28+CD8+ counterparts. J. Immunol. 156:1996;3587-3590.
30. Rufer N., Dragowska W., Thornbury G., Roosnek E., Lansdorp P. M. Telomere length dynamics in human lymphocyte subpopulations measured by flow cytometry. Nat. Biotechnol. 16:1998;743-747.
31. Lane H. C., Depper J. M., Greene W. C., Whalen G., Waldmann T. A., Fauci A. S. Qualitative analysis of immune function in patients with the acquired immunodeficiency syndrome. N. Engl. J. Med. 313:1985;79-84.
32. Bodnar A. G., Kim N. W., Effros R. B., Chiu C. P. Mechanism of telomerase induction during T cell activation. Exp. Cell Res. 228:1996;58-64.
33. Weng N.-P., Levine B. L., June C. H., Hodes R. J. Regulated expression of telomerase activity in human T lymphocyte development and activation. J. Exp. Med. 183:1996;2471-2480.
34. Weng N.-P., Levine B. L., June C. H., Hodes R. J. Regulation of telomerase RNA template expression in human T lymphocyte development and activation. J. Immunol. 158:1997;3215-3220.
35. Sachsenberg N., Perelson A. S., Yerly S., Schockmel G. A., Leduc D., Hirschel B., Perrin L. Turnover of CD4+ and CD8+ T lymphocytes in HIV-1 infection as measured by Ki-67 antigen. J. Exp. Med. 187:1998;1295-1303.
36. Zhang Z. Q., Notermans D. W., Sedgewick G., Cavert W., Wietgrefe S., Zupancic M., Gebhard K., Henry K., Boies L., Chen Z., Jenkins M., Mills R., McDade H., Goodwin C., Schuwirth C. M., Danner S. A., Haase A. T. Kinetics of CD4+ T cell repopulation of lymphoid tissues after treatment of HIV-1 infection. Proc. Natl. Acad. Sci. USA. 95:1998;1154-1159.
37. Mackall C. L., Fleisher T. A., Brown M. R., Andrich M. P., Chen C. C., Feuerstein I. M., Horowitz M. E., Magrath I. T., Shad A. T., Steinberg S. M., Wexler L. H., Gress R. E. Age, thymopoiesis, and CD4+ T-lymphocyte regeneration after intensive chemotherapy. N. Engl. J. Med. 332:1995;143-149.
38. Jendro M. C., Ganten T., Matteson E. L., Weyand C. M., Goronzy J. J. Emergence of oligoclonal T cell populations following therapeutic T cell depletion in rheumatoid arthritis. Arthritis Rheum. 38:1995;1242-1251.
39. Storek J., Witherspoon R. P., Storb R. T cell reconstitution after bone marrow transplantation into adult patients does not resemble T cell development in early life. Bone Marrow Transplant. 16:1995;413-425.
40. Mackall C. L., Hakim F. T., Gress R. E. T-cell regeneration: All repertoires are not created equal. Immunol. Today. 18:1997;245-251.
41. Mackall C. L., Fleisher T. A., Brown M. R., Andrich M. P., Chen C. C., Feuerstein I. M., Magrath I. T., Wexler L. H., Dimitrov D. S., Gress R. E. Distinctions between CD8+ and CD4+ T-cell regenerative pathways result in prolonged T-cell subset imbalance after intensive chemotherapy. Blood. 89:1997;3700-3707.
42. McCune J. M., Loftus R., Schmidt D. K., Carroll P., Webster D., Swor-Yim L. B., Francis I. R., Gross B. H., Grant R. M. High prevalence of thymic tissue in adults with human immunodeficiency virus-1 infection. J. Clin. Invest. 101:1998;2301-2308.
43. Gomez D. E., Tejera A. M., Olivero O. A. Irreversible telomere shortening by 3′-azido-2′,3′-dideoxythymidine (AZT) treatment. Biochem. Biophys. Res. Commun. 246:1998;107-110.
44. Strahl C., Blackburn E. H. Effects of reverse transcriptase inhibitors on telomere length and telomerase activity in two immortalized human cell lines. Mol. Cell. Biol. 16:1996;53-65.
45. Douek D. C., McFarland R. D., Keiser P. H., Gage E. A., Massey J. M., Haynes B. F., Polis M. A., Haase A. T., Feinberg M. B., Sullivan J. L., Jamieson B. D., Zack J. A., Picker L. J., Koup R. A. Changes in thymic function with age and during the treatment of HIV infection. Nature. 396:1998;690-695.
46. Haynes B. F., Hale L. P., Weinhold K. J., Patel D. D., Liao H. X., Bressler P. B., Jones D. M., Demarest J. F., Gebhard-Mitchell K., Haase A. T., Bartlett J. A. Analysis of the adult thymus in reconstitution of T lymphocytes in HIV-1 infection. J. Clin. Invest. 103:1999;453-460.