Quality monitoring of HIV-1-infected and uninfected peripheral blood mononuclear cell samples in a resource-limited setting

Clinical and Vaccine Immunology

Volumn 17, Issue 6, 2010, Pages 910-918

  Olemukan, Robert E ^a   Eller, Leigh Anne ^a,b   Ouma, Benson J ^a   Etonu, Ben ^a   Erima, Simon ^a   Naluyima, Prossy ^a   Kyabaggu, Denis ^a   Cox, Josephine H ^c   Sandberg, Johan K ^d   Wabwire Mangen, Fred ^a   Michael, Nelson L ^b   Robb, Merlin L ^b   De Souza, Mark S ^b,e   Eller, Michael A ^a,b,d  

^a Makerere University   (Uganda)

^b US Military HIV Research Program   (United States)

^c INTERNATIONAL AIDS VACCINE INITIATIVE   (United States)

^d KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^e ARMED FORCES RESEARCH INSTITUTE OF MEDICAL SCIENCES   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 2; STAPHYLOCOCCUS ENTEROTOXIN B;

ARTICLE; B LYMPHOCYTE; CELL FUNCTION; CELL VIABILITY; CONTROLLED STUDY; CRYOPRESERVATION; CYTOKINE PRODUCTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOPHENOTYPING; LYMPHOCYTE SUBPOPULATION; MONITORING; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; REPRODUCIBILITY; VEIN PUNCTURE;

BLOOD PRESERVATION; BLOOD SPECIMEN COLLECTION; CELL SURVIVAL; CRYOPRESERVATION; CYTOKINES; DEVELOPING COUNTRIES; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOPHENOTYPING; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE ACTIVATION; QUALITY CONTROL; TIME FACTORS; UGANDA;

EID: 77953169746     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00492-09     Document Type: Article

References (47)

1. Allsopp, C. E., S. J. Nicholls, and J. Langhorne. 1998. A flow cytometric method to assess antigen-specific proliferative responses of different sub-populations of fresh and cryopreserved human peripheral blood mononuclear cells. J. Immunol. Methods 214:175-186.
2. Appay, V., S. Reynard, V. Voelter, P. Romero, D. E. Speiser, and S. Leyvraz. 2006. Immuno-monitoring of CD8+ T cells in whole blood versus PBMC samples. J. Immunol. Methods 309:192-199.
3. Arroyo, M. A., W. B. Sateren, D. Serwadda, R. H. Gray, M. J. Wawer, N. K. Sewankambo, N. Kiwanuka, G. Kigozi, F. Wabwire-Mangen, M. Eller, L. A. Eller, D. L. Birx, M. L. Robb, and F. E. McCutchan. 2006. Higher HIV-1 incidence and genetic complexity along main roads in Rakai District, Uganda. J. Acquir. Immune Defic. Syndr. 43:440-445.
4. Ashmore, L. M., G. M. Shopp, and B. S. Edwards. 1989. Lymphocyte subset analysis by flow cytometry. Comparison of three different staining techniques and effects of blood storage. J. Immunol. Methods 118:209-215.
5. Baker, C. A., K. McEvers, R. Byaruhanga, R. Mulindwa, D. Atwine, J. Nantiba, N. G. Jones, I. Ssewanyana, and H. Cao. 2008. HIV subtypes induce distinct profiles of HIV-specific CD8(+) T cell responses. AIDS Res. Hum. Retroviruses 24:283-287.
6. Betts, M. R., M. C. Nason, S. M. West, S. C. De Rosa, S. A. Migueles, J. Abraham, M. M. Lederman, J. M. Benito, P. A. Goepfert, M. Connors, M. Roederer, and R. A. Koup. 2006. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107:4781-4789.
7. Boaz, M. J., P. Hayes, T. Tarragona, L. Seamons, A. Cooper, J. Birungi, P. Kitandwe, A. Semaganda, P. Kaleebu, G. Stevens, O. Anzala, B. Farah, S. Ogola, J. Indangasi, P. Mhlanga, M. Van Eeden, M. Thakar, A. Pujari, S. Mishra, N. Goonetilleke, S. Moore, A. Mahmoud, P. Sathyamoorthy, J. Mahalingam, P. R. Narayanan, V. D. Ramanathan, J. H. Cox, L. Dally, D. K. Gill, and J. Gilmour. 2009. Concordant proficiency in measurement of T-cell immunity in human immunodeficiency virus vaccine clinical trials by peripheral blood mononuclear cell and enzyme-linked immunospot assays in laboratories from three continents. Clin. Vaccine Immunol. 16:147-155.
8. Buchbinder, S. P., D. V. Mehrotra, A. Duerr, D. W. Fitzgerald, R. Mogg, D. Li, P. B. Gilbert, J. R. Lama, M. Marmor, C. Del Rio, M. J. McElrath, D. R. Casimiro, K. M. Gottesdiener, J. A. Chodakewitz, L. Corey, and M. N. Robertson. 2008. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 372:1881-1893.
9. Bull, M., D. Lee, J. Stucky, Y. L. Chiu, A. Rubin, H. Horton, and M. J. McElrath. 2007. Defining blood processing parameters for optimal detection of cryopreserved antigen-specific responses for HIV vaccine trials. J. Immunol. Methods 322:57-69.
10. Cao, H., P. Kaleebu, D. Hom, J. Flores, D. Agrawal, N. Jones, J. Serwanga, M. Okello, C. Walker, H. Sheppard, R. El-Habib, M. Klein, E. Mbidde, P. Mugyenyi, B. Walker, J. Ellner, R. Mugerwa, et al. 2003. Immunogenicity of a recombinant human immunodeficiency virus (HIV)-canarypox vaccine in HIV-seronegative Ugandan volunteers: results of the HIV Network for Prevention Trials 007 Vaccine Study. J. Infect. Dis. 187:887-895.
11. Cao, H., I. Mani, R. Vincent, R. Mugerwa, P. Mugyenyi, P. Kanki, J. Ellner, and B. D. Walker. 2000. Cellular immunity to human immunodeficiency virus type 1 (HIV-1) clades: relevance to HIV-1 vaccine trials in Uganda. J. Infect. Dis. 182:1350-1356.
12. Costantini, A., S. Mancini, S. Giuliodoro, L. Butini, C. M. Regnery, G. Silvestri, and M. Montroni. 2003. Effects of cryopreservation on lymphocyte immunophenotype and function. J. Immunol. Methods 278:145-155.
13. Cox, J. H., G. Ferrari, R. T. Bailer, and R. A. Koup. 2004. Automating procedures for processing, cryopreservation, storage, and manipulation of human peripheral blood mononuclear cells. J. Assoc. Lab. Autom. 9:16-23.
14. Currier, J. R., E. G. Kuta, E. Turk, L. B. Earhart, L. Loomis-Price, S. Janetzki, G. Ferrari, D. L. Birx, and J. H. Cox. 2002. A panel of MHC class I restricted viral peptides for use as a quality control for vaccine trial ELISPOT assays. J. Immunol. Methods 260:157-172.
15. Disis, M. L., C. dela Rosa, V. Goodell, L. Y. Kuan, J. C. Chang, K. Kuus-Reichel, T. M. Clay, H. Kim Lyerly, S. Bhatia, S. A. Ghanekar, V. C. Maino, and H. T. Maecker. 2006. Maximizing the retention of antigen specific lymphocyte function after cryopreservation. J. Immunol. Methods 308:13-18.
16. Dyer, W. B., S. L. Pett, J. S. Sullivan, S. Emery, D. A. Cooper, A. D. Kelleher, A. Lloyd, and S. R. Lewin. 2007. Substantial improvements in performance indicators achieved in a peripheral blood mononuclear cell cryopreservation quality assurance program using single donor samples. Clin. Vaccine Immunol. 14:52-59.
17. Eller, L. A., M. A. Eller, B. Ouma, P. Kataaha, D. Kyabaggu, R. Tumusiime, J. Wandege, R. Sanya, W. B. Sateren, F. Wabwire-Mangen, H. Kibuuka, M. L. Robb, N. L. Michael, and M. S. de Souza. 2008. Reference intervals in healthy adult Ugandan blood donors and their impact on conducting international vaccine trials. PLoS One 3:e3919.
18. GE Healthcare. 2007. Ficoll-Paque Plus intended use for in vitro isolation of lymphocytes. GE Healthcare, Uppsala, Sweden.
19. Guwatudde, D., F. Wabwire-Mangen, L. A. Eller, M. Eller, F. McCutchan, H. Kibuuka, M. Millard, N. Sewankambo, D. Serwadda, N. Michael, and M. Robb. 2009. Relatively low HIV infection rates in rural Uganda, but with high potential for a rise: a cohort study in Kayunga District, Uganda. PLoS One 4:e4145.
20. Harris, M., D. Serwada, N. K. Sewankambo, B. Kim, G. Kigozi, N. Kiwanuka, J. B. Philips, F. Wabwire, M. Meehen, T. Lutalo, J. R. Lane, R. Merling, R. H. Gray, M. J. Wawer, D. L. Birx, M. D. Robb, and F. E. McCutchan. 2002. Among 46 near full-length HIV type 1 genome sequences from Rakai District, Uganda, subtype D and AD recombinants predominate. AIDS Res. Hum. Retroviruses 18:1281-1290.
21. Hoelscher, M., W. E. Dowling, E. Sanders-Buell, J. K. Carr, M. E. Harris, A. Thomschke, M. L. Robb, D. L. Birx, and F. E. McCutchan. 2002. Detection of HIV-1 subtypes, recombinants, and dual infections in east Africa by a multi-region hybridization assay. AIDS 16:2055-2064.
22. Horton, H., E. P. Thomas, J. A. Stucky, I. Frank, Z. Moodie, Y. Huang, Y. L. Chiu, M. J. McElrath, and S. C. De Rosa. 2007. Optimization and validation of an 8-color intracellular cytokine staining (ICS) assay to quantify antigen-specific T cells induced by vaccination. J. Immunol. Methods 323:39-54.
23. Jeurink, P. V., Y. M. Vissers, B. Rappard, and H. F. Savelkoul. 2008. T cell responses in fresh and cryopreserved peripheral blood mononuclear cells: kinetics of cell viability, cellular subsets, proliferation, and cytokine production. Cryobiology 57:91-103.
24. Jones, N., M. Eggena, C. Baker, F. Nghania, D. Baliruno, P. Mugyenyi, F. Ssali, B. Barugahare, and H. Cao. 2006. Presence of distinct subsets of cytolytic CD8+ T cells in chronic HIV infection. AIDS Res. Hum. Retroviruses 22:1007-1013.
25. Kanof, M. E., P. D. Smith, and H. Zola. 2003. Preparation of human mononuclear cell populations and subpopulations. Curr. Protoc. Immunol. 2003(Suppl. 19):Unit 7.1.
26. Karita, E., N. Ketter, M. A. Price, K. Kayitenkore, P. Kaleebu, A. Nanvubya, O. Anzala, W. Jaoko, G. Mutua, E. Ruzagira, J. Mulenga, E. J. Sanders, M. Mwangome, S. Allen, A. Bwanika, U. Bahemuka, K. Awuondo, G. Omosa, B. Farah, P. Amornkul, J. Birungi, S. Yates, L. Stoll-Johnson, J. Gilmour, G. Stevens, E. Shutes, O. Manigart, P. Hughes, L. Dally, J. Scott, W. Stevens, P. Fast, and A. Kamali. 2009. CLSI-derived hematology and biochemistry reference intervals for healthy adults in eastern and southern Africa. PLoS One 4:e4401.
27. Kibuuka, H., D. Guwatudde, R. Kimutai, L. Maganga, L. Maboko, C. Watyema, F. Sawe, D. Shaffer, D. Matsiko, M. Millard, N. Michael, F. Wabwire-Mangen, and M. Robb. 2009. Contraceptive use in women enrolled into preventive HIV vaccine trials: experience from a phase I/II trial in east Africa. PLoS One 4:e5164.
28. Kierstead, L. S., S. Dubey, B. Meyer, T. W. Tobery, R. Mogg, V. R. Fernandez, R. Long, L. Guan, C. Gaunt, K. Collins, K. J. Sykes, D. V. Mehrotra, N. Chirmule, J. W. Shiver, and D. R. Casimiro. 2007. Enhanced rates and magnitude of immune responses detected against an HIV vaccine: effect of using an optimized process for isolating PBMC. AIDS Res. Hum. Retroviruses 23:86-92.
29. Kiwanuka, N., O. Laeyendecker, M. Robb, G. Kigozi, M. Arroyo, F. Mc-Cutchan, L. A. Eller, M. Eller, F. Makumbi, D. Birx, F. Wabwire-Mangen, D. Serwadda, N. K. Sewankambo, T. C. Quinn, M. Wawer, and R. Gray. 2008. Effect of human immunodeficiency virus type 1 (HIV-1) subtype on disease progression in persons from Rakai, Uganda, with incident HIV-1 infection. J. Infect. Dis. 197:707-713.
30. Kreher, C. R., M. T. Dittrich, R. Guerkov, B. O. Boehm, and M. Tary-Lehmann. 2003. CD4+ and CD8+ cells in cryopreserved human PBMC maintain full functionality in cytokine ELISPOT assays. J. Immunol. Methods 278:79-93.
31. Kutvirt, S. G., S. L. Lewis, and T. L. Simon. 1993. Lymphocyte phenotypes in infants are altered by separation of blood on density gradients. Br. J. Biomed. Sci. 50:321-328.
32. Kvarnström, M., M. C. Jenmalm, and C. Ekerfelt. 2004. Effect of cryopreservation on expression of Th1 and Th2 cytokines in blood mononuclear cells from patients with different cytokine profiles, analysed with three common assays: an overall decrease of interleukin-4. Cryobiology 49:157-168.
33. Lugada, E. S., J. Mermin, F. Kaharuza, E. Ulvestad, W. Were, N. Langeland, B. Asjo, S. Malamba, and R. Downing. 2004. Population-based hematologic and immunologic reference values for a healthy Ugandan population. Clin. Diagn. Lab. Immunol. 11:29-34.
34. Macey, M. G., C. J. Hyam, and A. C. Newland. 1988. Enumeration of lymphocyte sub-populations: a comparative study of whole blood and gradient centrifugation methods. Med. Lab. Sci. 45:187-191.
35. McElrath, M. J., S. C. De Rosa, Z. Moodie, S. Dubey, L. Kierstead, H. Janes, O. D. Defawe, D. K. Carter, J. Hural, R. Akondy, S. P. Buchbinder, M. N. Robertson, D. V. Mehrotra, S. G. Self, L. Corey, J. W. Shiver, and D. R. Casimiro. 2008. HIV-1 vaccine-induced immunity in the test-of-concept Step Study: a case-cohort analysis. Lancet 372:1894-1905.
36. NCCLS. 2000. How to define and determine reference intervals in the clinical laboratory; approved guideline, 2nd ed. C28-A2, Vol. 20, No. 13. National Committee for Clinical Laboratory Standards, Wayne, PA.
37. Nilsson, C., S. Aboud, K. Karlén, B. Hejdeman, W. Urassa, and G. Biberfeld. 2008. Optimal blood mononuclear cell isolation procedures for gamma interferon enzyme-linked immunospot testing of healthy Swedish and Tanzanian subjects. Clin. Vaccine Immunol. 15:585-589.
38. Owen, R. E., E. Sinclair, B. Emu, J. W. Heitman, D. F. Hirschkorn, C. L. Epling, Q. X. Tan, B. Custer, J. M. Harris, M. A. Jacobson, J. M. McCune, J. N. Martin, F. M. Hecht, S. G. Deeks, and P. J. Norris. 2007. Loss of T cell responses following long-term cryopreservation. J. Immunol. Methods 326:93-115.
39. Reimann, K. A., M. Chernoff, C. L. Wilkening, C. E. Nickerson, and A. L. Landay. 2000. Preservation of lymphocyte immunophenotype and proliferative responses in cryopreserved peripheral blood mononuclear cells from human immunodeficiency virus type 1-infected donors: implications for multicenter clinical trials. The ACTG Immunology Advanced Technology Laboratories. Clin. Diagn. Lab. Immunol. 7:352-359.
40. Riccio, E. K., I. Neves, D. M. Banic, S. Corte-Real, M. G. Alecrim, M. Morgado, C. T. Daniel-Ribeiro, and M. D. E. F. Ferreira-da-Cruz. 2002. Cryopreservation of peripheral blood mononuclear cells does not significantly affect the levels of spontaneous apoptosis after 24-h culture. Cryobiology 45:127-134.
41. Romeu, M. A., M. Mestre, L. Gonzalez, A. Valls, J. Verdaguer, M. Corominas, J. Bas, E. Massip, and E. Buendia. 1992. Lymphocyte immunophenotyping by flow cytometry in normal adults. Comparison of fresh whole blood lysis technique, Ficoll-Paque separation and cryopreservation. J. Immunol. Methods 154:7-10.
42. Sigma-Aldrich. 2003. Accuspin tubes procedure no. AST-1. Sigma-Aldrich, St. Louis, MO.
43. Tobery, T. W., S. A. Dubey, K. Anderson, D. C. Freed, K. S. Cox, J. Lin, M. T. Prokop, K. J. Sykes, R. Mogg, D. V. Mehrotra, T. M. Fu, D. R. Casimiro, and J. W. Shiver. 2006. A comparison of standard immunogenicity assays for monitoring HIV type 1 gag-specific T cell responses in Ad5 HIV type 1 gag vaccinated human subjects. AIDS Res. Hum. Retroviruses 22:1081-1090.
44. Tugume, S. B., E. M. Piwowar, T. Lutalo, P. N. Mugyenyi, R. M. Grant, F. W. Mangeni, K. Pattishall, and E. Katongole-Mbidde. 1995. Hematological reference ranges among healthy Ugandans. Clin. Diagn. Lab. Immunol. 2:233-235.
45. Weinberg, A., R. A. Betensky, L. Zhang, and G. Ray. 1998. Effect of shipment, storage, anticoagulant, and cell separation on lymphocyte proliferation assays for human immunodeficiency virus-infected patients. Clin. Diagn. Lab. Immunol. 5:804-807.
46. Weinberg, A., L. Y. Song, C. Wilkening, A. Sevin, B. Blais, R. Louzao, D. Stein, P. Defechereux, D. Durand, E. Riedel, N. Raftery, R. Jesser, B. Brown, M. F. Keller, R. Dickover, E. McFarland, and T. Fenton. 2009. Optimization and limitations of use of cryopreserved peripheral blood mononuclear cells for functional and phenotypic T-cell characterization. Clin. Vaccine Immunol. 16:1176-1186.
47. Weinberg, A., L. Zhang, D. Brown, A. Erice, B. Polsky, M. S. Hirsch, S. Owens, and K. Lamb. 2000. Viability and functional activity of cryopreserved mononuclear cells. Clin. Diagn. Lab. Immunol. 7:714-716.