Persistent subclinical immune defects in HIV-1-infected children treated with antiretroviral therapy

AIDS

Volumn 29, Issue 14, 2015, Pages 1745-1756

  Van Den Heuvel, Diana ^a   Driessen, Gertjan J A ^a   Berkowska, Magdalena A ^a,b   Van Der Burg, Mirjam ^a   Langerak, Anton W ^a   Zhao, Dan ^a   Charif, Halima ^a   Hartwig, Nico G ^a,c   Van Rossum, Annemarie M C ^a   Fraaij, Pieter L A ^a   Van Dongen, Jacques J M ^a   Van Zelm, Menno C ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c SINT FRANCISCUS GASTHUIS   (Netherlands)

Author keywords

Antiretroviral therapy; B cell memory; CD4+ T cell memory; CD8+ effector T cell; Perinatal HIV infection; Persistent immune defects; V 9+V 2+ T cells

Indexed keywords

ANTIRETROVIRUS AGENT; IMMUNOGLOBULIN A; T LYMPHOCYTE RECEPTOR;

ADOLESCENT; ADULT; ARTICLE; B LYMPHOCYTE; BLOOD SAMPLING; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIVISION; CELL ISOLATION; CHILD; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; EFFECTOR CELL; FLOW CYTOMETRY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; IMMUNE DEFICIENCY; IMMUNOPHENOTYPING; INFANT; MAJOR CLINICAL STUDY; MEMORY T LYMPHOCYTE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; SEQUENCE ANALYSIS; T LYMPHOCYTE SUBPOPULATION; VIRUS LOAD; VIRUS REPLICATION; FEMALE; HIV INFECTIONS; IMMUNOLOGY; ISOLATION AND PURIFICATION; LYMPHOCYTE SUBPOPULATION; MALE; PATHOLOGY; PRESCHOOL CHILD; T LYMPHOCYTE; VIROLOGY; YOUNG ADULT;

ADOLESCENT; ANTI-RETROVIRAL AGENTS; B-LYMPHOCYTES; CHILD; CHILD, PRESCHOOL; FEMALE; FLOW CYTOMETRY; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOPHENOTYPING; INFANT; LYMPHOCYTE SUBSETS; MALE; T-LYMPHOCYTES; YOUNG ADULT;

EID: 84975118727     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0000000000000765     Document Type: Article

References (69)

1. Cohen S, Smit C, Van Rossum AM, Fraaij PL, Wolfs TF, Geelen SP, et al. Long-term response to combination antiretroviral therapy in HIV-infected children in the Netherlands registered from 1996 to 2012. AIDS 2013;27:2567-2575.
2. Duong T, Judd A, Collins IJ, Doerholt K, Lyall H, Foster C, et al. Long-term virological outcome in children on antiretroviral therapy in the UK and Ireland. AIDS 2014;28:2395-2405.
3. Van Rossum AM, Scherpbier HJ, Van Lochem EG, Pakker NG, Slieker WA, Wolthers KC, et al. Therapeutic immune reconstitution in HIV-1-infected children is independent of their age and pretreatment immune status. AIDS 2001;15:2267-2275.
4. Pakker NG, Notermans DW, De Boer RJ, Roos MT, De Wolf F, Hill A, et al. Biphasic kinetics of peripheral blood T cells after triple combination therapy in HIV-1 infection: a composite of redistribution and proliferation. Nat Med 1998;4:208-214.
5. + T lymphocytes in children on highly active antiretroviral therapy. Dutch study group for children with HIV infections. AIDS 1998;12:2155-2159.
6. Guaraldi G, Prakash M, Moecklinghoff C, Stellbrink HJ. Morbidity in older HIV-infected patients: impact of long-term antiretroviral use. AIDS Rev 2014;16:75-89.
7. Kaplan RC, Sinclair E, Landay AL, Lurain N, Sharrett AR, Gange SJ, et al. T cell activation predicts carotid artery stiffness among HIV-infected women. Atherosclerosis 2011;217:207-213.
8. Rajasuriar R, Wright E, Lewin SR. Impact of antiretroviral therapy (ART) timing on chronic immune activation/inflammation and end-organ damage. Curr Opin HIV AIDS 2015;10:35-42.
9. + T cells: an HIV evasion strategy. Cell Death Differ 2005;12(Suppl 1):859-870.
10. + T cells vary in differentiation phenotype in different persistent virus infections. Nat Med 2002;8:379-385.
11. Champagne P, Ogg GS, King AS, Knabenhans C, Ellefsen K, Nobile M, et al. Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 2001;410:106-111.
12. + T-cell polyfunctionality, proliferation, and cytotoxicity are not restored by antiretroviral therapy. J Virol 2009;83:11876-11889.
13. + T-cell differentiation towards senescence in HIV-1 infection. PLoS Biol 2004;2:E20.
14. + lymphocyte subsets during HIV infection. Clin Exp Immunol 1989;75:206-210.
15. Poles MA, Barsoum S, Yu W, Yu J, Sun P, Daly J, et al. Human immunodeficiency virus type 1 induces persistent changes in mucosal and blood gammadelta T cells despite suppressive therapy. J Virol 2003;77:10456-10467.
16. Bordon J, Evans PS, Propp N, Davis CE Jr, Redfield RR, Pauza CD. Association between longer duration of HIV-suppressive therapy and partial recovery of the V gamma 2 T cell receptor repertoire. J Infect Dis 2004;189:1482-1486.
17. Lane HC, Masur H, Edgar LC, Whalen G, Rook AH, Fauci AS. Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. N Engl J Med 1983;309:453-458.
18. De Milito A, Morch C, Sonnerborg A, Chiodi F. Loss of memory (CD27) B lymphocytes in HIV-1 infection. AIDS 2001;15:957-964.
19. Scott ME, Landay AL, Lint TF, Spear GT. In vivo decrease in the expression of complement receptor 2 on B-cells in HIV infection. AIDS 1993;7:37-41.
20. Moir S, Malaspina A, Ogwaro KM, Donoghue ET, Hallahan CW, Ehler LA, et al. HIV-1 induces phenotypic and functional perturbations of B cells in chronically infected individuals. Proc Natl Acad Sci U S A 2001;98:10362-10367.
21. Moir S, Fauci AS. B cells in HIV infection and disease. Nat Rev Immunol 2009;9:235-245.
22. Amu S, Ruffin N, Rethi B, Chiodi F. Impairment of B-cell functions during HIV-1 infection. AIDS 2013;27:2323-2334.
23. D'Orsogna LJ, Krueger RG, McKinnon EJ, French MA. Circulating memory B-cell subpopulations are affected differently by HIV infection and antiretroviral therapy. AIDS 2007;21:1747-1752.
24. Moir S, Malaspina A, Ho J, Wang W, Dipoto AC, O'Shea MA, et al. Normalization of B cell counts and subpopulations after antiretroviral therapy in chronic HIV disease. J Infect Dis 2008;197:572-579.
25. Morris L, Binley JM, Clas BA, Bonhoeffer S, Astill TP, Kost R, et al. HIV-1 antigen-specific and -nonspecific B cell responses are sensitive to combination antiretroviral therapy. J Exp Med 1998;188:233-245.
26. Titanji K, Chiodi F, Bellocco R, Schepis D, Osorio L, Tassandin C, et al. Primary HIV-1 infection sets the stage for important B lymphocyte dysfunctions. AIDS 2005;19:1947-1955.
27. Comans-Bitter WM, De Groot R, Van Den Beemd R, Neijens HJ, Hop WC, Groeneveld K, et al. Immunophenotyping of blood lymphocytes in childhood. Reference values for lymphocyte subpopulations. J Pediatr 1997;130:388-393.
28. + T cells and disease progression in HIV-1 perinatally infected children. PLoS One 2012;7:e29154.
29. Ghosh S, Feyen O, Jebran AF, Huck K, Jetzek-Zader M, Bas M, Niehues T. Memory B cell function in HIV-infected childrendecreased memory B cells despite ART. Pediatr Res 2009;66:185-190.
30. Bekker V, Scherpbier H, Pajkrt D, Jurriaans S, Zaaijer H, Kuijpers TW. Persistent humoral immune defect in highly active antiretroviral therapy-treated children with HIV-1 infection: loss of specific antibodies against attenuated vaccine strains and natural viral infection. Pediatrics 2006;118:e315-e322.
31. Romiti ML, Cancrini C, Castelli-Gattinara G, Di Cesare S, Ciaffi P, Bernardi S, et al. Kinetics of the T-cell receptor CD4 and CD8 V beta repertoire in HIV-1 vertically infected infants early treated with HAART. AIDS 2001;15:2075-2084.
32. Pensieroso S, Cagigi A, Palma P, Nilsson A, Capponi C, Freda E, et al. Timing of HAART defines the integrity of memory B cells and the longevity of humoral responses in HIV-1 verticallyinfected children. Proc Natl Acad Sci U S A 2009;106:7939-7944.
33. Palma P, Romiti ML, Cancrini C, Pensieroso S, Montesano C, Bernardi S, et al. Delayed early antiretroviral treatment is associated with an HIV-specific long-term cellular response in HIV-1 vertically infected infants. Vaccine 2008;26:5196-5201.
34. Hainaut M, Ducarme M, Schandene L, Peltier CA, Marissens D, Zissis G, et al. Age-related immune reconstitution during highly active antiretroviral therapy in human immunodeficiency virus type 1-infected children. Pediatr Infect Dis J 2003;22:62-69.
35. Cotugno N, Douagi I, Rossi P, Palma P. Suboptimal immune reconstitutioninvertically HIV infected children: a view on how HIV replication and timing of HAART initiation can impact on T and B-cell compartment. Clin Dev Immunol 2012;2012:1-11.
36. + T lymphocytes in HIV-infected individuals following antiretroviral therapy. Curr Opin Immunol 2001;13:483-488.
37. Persaud D, Patel K, Karalius B, Rainwater-Lovett K, Ziemniak C, Ellis A, et al. Influence of age at virologic control on peripheral blood human immunodeficiency virus reservoir size and serostatus in perinatally infected adolescents. JAMA Pediatr 2014;168:1138-1146.
38. Driessen GJ, Dalm VA, Van Hagen PM, Grashoff HA, Hartwig NG, Van Rossum AM, et al. Common variable immunodeficiency and idiopathic primary hypogammaglobulinemia: two different conditions within the same disease spectrum. Haematologica 2013;98:1617-1623.
39. Fraaij PL, Verweel G, Van Rossum AM, Van Lochem EG, Schutten M, Weemaes CM, et al. Sustained viral suppression and immune recovery in HIV type 1-infected children after 4 years of highly active antiretroviral therapy. Clin Infect Dis 2005;40:604-608.
40. Kalina T, Flores-Montero J, Van Der Velden VH, Martin-Ayuso M, Bottcher S, Ritgen M, et al. EuroFlow standardization of flow cytometer instrument settings and immunophenotyping protocols. Leukemia 2012;26:1986-2010.
41. Breit TM, Wolvers-Tettero IL, Van Dongen JJ. Unique selection determinant in polyclonal V delta 2-J delta 1 junctional regions of human peripheral gamma delta T lymphocytes. J Immunol 1994;152:2860-2864.
42. Van Dongen JJ, Langerak AW, Bruggemann M, Evans PA, Hummel M, Lavender FL, et al. Design and standardization of PCR primers and protocols for detection of clonal immunoglobulin and T-cell receptor gene recombinations in suspect lymphoproliferations: report of the BIOMED-2 Concerted Action BMH4-CT98-3936. Leukemia 2003;17:2257-2317.
43. Pongers-Willemse MJ, Seriu T, Stolz F, D'Aniello E, Gameiro P, Pisa P, et al. Primers and protocols for standardized detection of minimal residual disease in acute lymphoblastic leukemia using immunoglobulin and T cell receptor gene rearrangements and TAL1 deletions as PCR targets: report of the BIOMED-1 CONCERTED ACTION: investigation of minimal residual disease in acute leukemia. Leukemia 1999;13:110-118.
44. + T-cells. Leukemia 2006;20:505-513.
45. Tiller T, Meffre E, Yurasov S, Tsuiji M, Nussenzweig MC, Wardemann H. Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J Immunol Methods 2008;329:112-124.
46. Berkowska MA, Driessen GJ, Bikos V, Grosserichter-Wagener C, Stamatopoulos K, Cerutti A, et al. Human memory B cells originate from three distinct germinal center-dependent and - independent maturation pathways. Blood 2011;118:2150-2158.
47. Uduman M, Yaari G, Hershberg U, Stern JA, Shlomchik MJ, Kleinstein SH. Detecting selection in immunoglobulin sequences. Nucleic Acids Res 2011;39:W499-W504.
48. Yaari G, Uduman M, Kleinstein SH. Quantifying selection in high-throughput Immunoglobulin sequencing data sets. Nucleic Acids Res 2012;40:e134.
49. Van Zelm MC, Szczepanski T, Van Der Burg M, Van Dongen JJ. Replication history of B lymphocytes reveals homeostatic proliferation and extensive antigen-induced B cell expansion. J Exp Med 2007;204:645-655.
50. Caldwell MB, Oxtoby MJ, Simonds RJ, Lindegren ML, Rogers MF. Centers for Disease Control and Prevention. 1994 Revised classification system for human immunodeficiency virus infection in children less than 13 years of age. Official authorized addenda: human immunodeficiency virus infection codes and official guidelines for coding and reporting ICD-9-CM. MMWR 1994;43.
51. Sanquin. Normale waarden Ig's voor verschillende leeftijdsgroepen. http://www.sanquin. nl/producten-diensten/diagnostiek/vademecum/theoriehoofdstukken/afweerstoornissen [data obtained at 03-07-2013]
52. Appay V, Van Lier RA, Sallusto F, Roederer M. Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytometry A 2008;73:975-983.
53. + cell subset in HIV disease implicate replicative senescence in HIV pathogenesis. AIDS 1996;10:F17-22.
54. +CD28-cell population in the blood and lung of HIV-positive patients. J Acquir Immune Defic Syndr 1993;6:1194-1204.
55. Moir S, Ho J, Malaspina A, Wang W, Di Poto AC, O'Shea MA, et al. Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J Exp Med 2008;205:1797-1805.
56. Corbeau P, Reynes J. Immune reconstitution under antiretroviral therapy: the new challenge in HIV-1 infection. Blood 2011;117:5582-5590.
57. WHO. Antiretroviral therapy for HIV infection in infants and children: towards universal access: recommendations for a public health approach: 2010 revision. WHO Guidelines Approved by the Guidelines Review Committee; 2010.
58. + T cells in acute HIV-1 infection is mostly associated with rapid disease progression. PLoS One 2012;7:e49526.
59. Descours B, Avettand-Fenoel V, Blanc C, Samri A, Melard A, Supervie V, et al. Immune responses driven by protective human leukocyte antigen alleles from long-term nonprogressors are associated with low HIV reservoir in central memory CD4 T cells. Clin Infect Dis 2012;54:1495-1503.
60. + T-cell subsets in human immunodeficiency virus controllers: an ANRS EP36 study. J Virol 2007;81:13904-13915.
61. Fenoglio D, Poggi A, Catellani S, Battaglia F, Ferrera A, Setti M, et al. Vdelta1 T lymphocytes producing IFN-gamma and IL-17 are expanded in HIV-1-infected patients and respond to Candida albicans. Blood 2009;113:6611-6618.
62. Li H, Pauza CD. HIV envelope-mediated, CCR5/alpha4beta7-dependent killing of CD4-negative gammadelta T cells which are lost during progression to AIDS. Blood 2011;118:5824-5831.
63. Moir S, Malaspina A, Li Y, Chun TW, Lowe T, Adelsberger J, et al. B cells of HIV-1-infected patients bind virions through CD21-complement interactions and transmit infectious virus to activated T cells. J Exp Med 2000;192:637-646.
64. Xu W, Santini PA, Sullivan JS, He B, Shan M, Ball SC, et al. HIV-1 evades virus-specific IgG2 and IgA responses by targeting systemic and intestinal B cells via long-range intercellular conduits. Nat Immunol 2009;10:1008-1017.
65. Cagigi A, Nilsson A, Pensieroso S, Chiodi F. Dysfunctional B-cell responses during HIV-1 infection: implication for influenza vaccination and highly active antiretroviral therapy. Lancet Infect Dis 2010;10:499-503.
66. Bussmann BM, Reiche S, Bieniek B, Krznaric I, Ackermann F, Jassoy C. Loss of HIV-specific memory B-cells as a potential mechanism for the dysfunction of the humoral immune response against HIV. Virology 2010;397:7-13.
67. Moir S, Buckner CM, Ho J, Wang W, Chen J, Waldner AJ, et al. B cells in early and chronic HIV infection: evidence for preservation of immune function associated with early initiation of antiretroviral therapy. Blood 2010;116:5571-5579.
68. Titanji K, De Milito A, Cagigi A, Thorstensson R, Grutzmeier S, Atlas A, et al. Loss of memory B cells impairs maintenance of long-term serologic memory during HIV-1 infection. Blood 2006;108:1580-1587.
69. Fecteau JF, Cote G, Neron S. A new memory CD27-IgG+ B cell population in peripheral blood expressing VH genes with low frequency of somatic mutation. J Immunol 2006;177:3728-3736.