CD205 antigen targeting combined with dendritic cell recruitment factors and antigen-linked CD40L activation primes and expands significant antigen-specific antibody and CD4 + T cell responses following DNA vaccination of outbred animals

Vaccine

Volumn 30, Issue 9, 2012, Pages 1624-1635

  Njongmeta, Leo M ^a   Bray, Jocelyn ^a   Davies, Christopher J ^b   Davis, William C ^c   Howard, Chris J ^d   Hope, Jayne C ^d   Palmer, Guy H ^c   Brown, Wendy C ^c   Mwangi, Waithaka ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UTAH STATE UNIVERSITY   (United States)

^c WASHINGTON STATE UNIVERSITY   (United States)

^d INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

Author keywords

Antigen targeting; CD4 T cells; CD40L; Dendritic cell; DNA vaccine; Intradermal; Linked activation; Outbred species

Indexed keywords

CD205 ANTIGEN TARGETING VACCINE; CD40 LIGAND; DNA VACCINE; FLT3 LIGAND; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN G; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ARTICLE; CALF (BOVINE); CD4+ T LYMPHOCYTE; CELL STRAIN HEK293; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; DNA IMMUNIZATION; DRUG DOSE ESCALATION; HUMAN; HUMAN CELL; IMMUNOGENICITY; LYMPHOCYTE PROLIFERATION; MALE; NONHUMAN; OUTBREEDING; PRIORITY JOURNAL;

ANAPLASMA MARGINALE; ANIMALS; ANTIBODY FORMATION; ANTIGENS, CD; B-LYMPHOCYTES; BACTERIAL OUTER MEMBRANE PROTEINS; CATTLE; CD4-POSITIVE T-LYMPHOCYTES; CD40 LIGAND; CELL PROLIFERATION; DENDRITIC CELLS; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HEK293 CELLS; HUMANS; IMMUNOGLOBULIN G; INTERFERON-GAMMA; LECTINS, C-TYPE; LYMPHOCYTE ACTIVATION; MALE; MEMBRANE PROTEINS; RECEPTORS, CELL SURFACE; VACCINES, DNA;

EID: 84856775381     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.12.110     Document Type: Article

References (86)

1. Moss R. Prospects for control of emerging infectious diseases with plasmid DNA vaccines. J Immune Based Ther Vaccines 2009, 7(1):3.
2. Jechlinger W. Optimization and delivery of plasmid DNA for vaccination. Expert Rev Vaccines 2006, 5(6):803-825.
3. Donnelly J.J., Friedman A., Martinez D., Montgomery D.L., Shiver J.W., Motzel S.L., et al. Preclinical efficacy of a prototype DNA vaccine: enhanced protection against antigenic drift in influenza virus. Nat Med 1995, 1(June (6)):583-587.
4. Wolff J.A., Malone R.W., Williams P., Chong W., Acsadi G., Jani A., et al. Direct gene transfer into mouse muscle in vivo. Science 1990, 247:1465-1468.
5. Polack F.P., Lee S.H., Permar S., Manyara E., Nousari H.G., Jeng Y., et al. Successful DNA immunization against measles: neutralizing antibody against either the hemagglutinin or fusion glycoprotein protects rhesus macaques without evidence of atypical measles. Nat Med 2000, 6(July (7)):776-781.
6. Wang R., Doolan D.L., Le T.P., Hedstrom R.C., Coonan K.M., Charoenvit Y., et al. Hoffman Induction of antigen-specific cytotoxic T lymphocytes in humans by a malaria DNA vaccine. Science 1998, 282(October (5388)):476-480.
7. Wang R., Epstein J., Baraceros F.M., Gorak E.J., Charoenvit Y., Carucci D.J., et al. Induction of CD4+ T cell-dependent CD8+ type 1 responses in humans by a malaria DNA vaccine. Proc Natl Acad Sci USA 2001, 98(August (19)):10817-10822.
8. Wang R., Epstein J., Charoenvit Y., Baraceros F.M., Rahardjo N., Gay T., et al. Induction in humans of CD8+ and CD4+ T cell and antibody responses by sequential immunization with malaria DNA and recombinant protein. J Immunol 2004, 172(May (9)):5561-5569.
9. Barouch D.H., Santra S., Tenner-Racz.K., Racz P., Kuroda M., Schmitzm J.E., et al. Potent CD4+ T cell responses elicited by a bicistronic Hiv-1 DNA vaccine expressing gp120 and GM-CSF. J Immunol 2002, 168(January (2)):562-568.
10. Manoj S., Griebel P.J., Babiuk L.A., van Drunen Littel-van den Hurk S. Targeting with bovine CD154 enhances humoral immune responses induced by a DNA vaccine in sheep. J Immunol 2003, 170:989-996.
11. Mwangi W., Brown W.C., Lewin H.A., Howard C.J., Hope J.C., Baszler T.V., et al. DNA-encoded fetal liver tyrosine kinase 3 ligand and granulocyte macrophage-colony-stimulating factor increase dendritic cell recruitment to the inoculation site and enhance antigen-specific CD4+ T cell responses induced by DNA vaccination of outbred animals. J Immunol 2002, 169(October (7)):3837-3846.
12. Mwangi W., Brown W.C., Splitter G.A., Davies C.J., Howard C.J., Hope J.C., et al. DNA vaccine construct incorporating intercellular trafficking and intracellular targeting motifs effectively primes and induces memory B and T cell responses in outbred animals. Clin Vaccine Immunol 2007, 14:304-311.
13. Zubkova I., Choi Y.H., Chang E., Pirollo K., Uren T., Watanabe H., et al. T-cell vaccines that elicit effective immune responses against HCV in chimpanzees may create greater immune pressure for viral mutation. Vaccine 2009, 27(19):2594-2602.
14. Öhlschläger P., Quetting M., Alvarez G., Dürst M., Gissmann L., Kaufmann A.M. Enhancement of immunogenicity of a therapeutic cervical cancer DNA-based vaccine by co-application of sequence-optimized genetic adjuvants. Int J Cancer 2009, 125(1):189-198.
15. Fort Dodge Animal Health Care Products. http://wwwwyethcom/animalhealth.
16. Novartis Animal Health. http://wwwahnovartiscom/aqua/en/indexshtml.
17. Memorial Sloan Kettering Cancer Center. http://wwwmskccorg/mskcc/html/52438cfm.
18. Argilaguet J.M., Pérez-Martín E., Gallardo C., Salguero F.J., Borrego B., Lacasta A., et al. Enhancing DNA immunization by targeting ASFV antigens to SLA-II bearing cells. Vaccine 2011, 29(33):5379-5385.
19. Guo A., Jin Z., Zheng Y., Hai G., Yuan G., Li H., et al. Induction of protection against porcine cysticercosis in growing pigs by DNA vaccination. Vaccine 2007, 25(1):170-175.
20. Verminnen K., Beeckman D.S.A., Sanders N.N., De Smedt S., Vanrompay D.C.G. Vaccination of turkeys against Chlamydophila psittaci through optimised DNA formulation and administration. Vaccine 2010, 28(18):3095-3105.
21. Weiss W.R., Ishii K.J., Hedstrom R.C., Sedegah M., Ichino M., Barnhart K., et al. A plasmid encoding murine granulocyte-macrophage colony-stimulating factor increases protection conferred by a malaria DNA vaccine. J Immunol 1998, 161:2325-2332.
22. Oxenius A., Zinkernagel R.M., Hengartner H. CD4+ T-cell induction and effector functions: a comparison of immunity against soluble antigens and viral infections. Adv Immunol 1998, 70:313-367.
23. Haddad D., Ramprakash J., Sedegah M., Charoenvit Y., Baumgartner R., Kumar S., et al. Plasmid vaccine expressing granulocyte-macrophage colony-stimulating factor attracts infiltrates including immature dendritic cells into injected muscles. J Immunol 2000, 165:3772-3781.
24. Galvin T.A., Muller J., Khan A.S. Effect of different promoters on immune responses elicited by HIV-1 gag/env multigenic DNA vaccine in Macaca mulatta and Macaca nemestrina. Vaccine 2000, 18:2566-2583.
25. Casares S., Inaba K., Brumeanu T.D., Steinman R.M., Bona C.A. Antigen presentation by dendritic cells after immunization with DNA encoding a major histocompatibility complex class II-restricted viral epitope. J Exp Med 1997, 186(November (9)):1481-1486.
26. Porgador A., Irvine K.R., Iwasaki A., Barber B.H., Restifo N.P., Germain R.N. Predominant role for directly transfected dendritic cells in antigen presentation to CD8+ T cells after gene gun immunization. J Exp Med 1998, 188(September (6)):1075-1082.
27. Wolff J.A., Ludtke J.J., Acsadi G., Williams P., Jani A. Long-term persistence of plasmid DNA and foreign gene expression in mouse muscle. Hum Mol Genet 1992, 1(September (6)):363-369.
28. Feltquate D.M., Heaney S., Webster R.G., Robinson H.L. Different T helper cell types and antibody isotypes generated by saline and gene gun DNA immunization. J Immunol 1997, 158:2278-2284.
29. Condon C., Watkins S.C., Celluzzi C.M., Thompson K., Falo L.D. DNA-based immunization by in vivo transfection of dendritic cells. Nat Med 1996, 2:1122-1128.
30. Steinman R.M., Kayo I., Shannon T., Philippe P., Mellman I. Antigen capture, processing, and presentation by dendritic cells: recent cell biological studies. Hum Immunol 1999, 60:562-567.
31. Banchereau J., Steinman R.M. Dendritic cells and the control of immunity. Nature 1998, 392:245-252.
32. Steinman R.M. The dendritic cell system and its role in immunogenicity. Ann Rev Immunol 1991, 9:271.
33. Ludewig B., Ehl S., Karrer U., Odermatt B., Hengartner H., Zinkernagel R.M. Dendritic cells efficiently induce protective antiviral immunity. J Virol 1998, 72:3812-3818.
34. Akbari O., Panjwani N., Garcia S., Tascon R., Lowrie D., Stockinger B. DNA vaccination: transfection and activation of dendritic cells as key events for immunity. J Exp Med 1999, 189(January (1)):169-178.
35. Nussenzweig M.C., Steinman R.M., Witmer M.D., Gutchinov B. A monoclonal antibody specific for mouse dendritic cells. Proc Natl Acad Sci USA 1982, 79(January (1)):161-165.
36. Correale P., Campoccia G., Tsang K.Y., Micheli L., Cusi M.G., Sabatino M., et al. Recruitment of dendritic cells and enhanced antigen-specific immune reactivity in cancer patients treated with hr-GM-CSF (molgramostim) and hr-IL-2: results from a phase 1b clinical trial. Eur J Cancer 2001, 37(May (7)):892-902.
37. Leachman S.A., Tigelaar R.E., Shlyankevich M., Slade M.D., Irwin M., Chang E., et al. Granulocyte-macrophage colony-stimulating factor priming plus papillomavirus E6 DNA vaccination: effects on papilloma formation and regression in the cottontail rabbit papillomavirus-rabbit model. J Virol 2000, 74(September (18)):8700-8708.
38. Tarradas J., Álvarez B., Fraile L., Rosell R., Muñoz M., Galindo-Cardiel I., et al. Immunomodulatory effect of swine CCL20 chemokine in DNA vaccination against CSFV. Vet Immunol Immunopathol 2011, 142(3-4):243-251.
39. Melkebeek V., Van den Broeck W., Verdonck F., Goddeeris B.M., Cox E. Effect of plasmid DNA encoding the porcine granulocyte-macrophage colony-stimulating factor on antigen-presenting cells in pigs. Vet Immunol Immunopathol 2008, 125(3-4):354-360.
40. Bonifaz L.B.D., Mahnke K., Rivera M., Nussenzweig M.C., Steinman R.M. Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J Exp Med 2002, 196:1627-1638.
41. Bonifaz L.C.B.D., Charalambous A., Darguste D.I., Fujii S., Soares H., Brimnes M.K., et al. In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination. J Exp Med 2004, 199:815-824.
42. Tsuji T., Matsuzaki J., Kelly M.P., Ramakrishna V., Vitale L., He L-Z., et al. Antibody-targeted NY-ESO-1 to mannose receptor or DEC-205 in vitro elicits dual human CD8+ and CD4+ T cell responses with broad antigen specificity. J Immunol 2011, 186(January (2)):1218-1227.
43. Trumpfheller C., Finke J.S., López C.B., Moran T.M., Moltedo B., Soares H., et al. Intensified and protective CD4+ T cell immunity in mice with anti-dendritic cell HIV gag fusion antibody vaccine. J Exp Med 2006, 203(March (3)):607-617.
44. Idoyaga J., Lubkin A., Fiorese C., Lahoud M.H., Caminschi I., Huang Y., et al. Comparable T helper 1 (Th1) and CD8 T-cell immunity by targeting HIV gag p24 to CD8 dendritic cells within antibodies to Langerin, DEC205, and Clec9A. Proc Natl Acad Sci USA 2011, 108(February (6)):2384-2389.
45. Wang W.W., Das D., Suresh M.R. A versatile bifunctional dendritic cell targeting vaccine vector. Mol Pharm 2008, 6(1):158-172.
46. Demangel C., Zhou J., Choo A.B.H., Shoebridge G., Halliday G.M., Britton W.J. Single chain antibody fragments for the selective targeting of antigens to dendritic cells. Mol Immunol 2005, 42(8):979-985.
47. Grossmann C., Tenbusch M., Nchinda G., Temchura V., Nabi G., Stone G., et al. Enhancement of the priming efficacy of DNA vaccines encoding dendritic cell-targeted antigens by synergistic toll-like receptor ligands. BMC Immunol 2009, 10(1):43.
48. Johnson T.S., Mahnke K., Storn V., Schönfeld K., Ring S., Nettelbeck D.M., et al. Inhibition of melanoma growth by targeting of antigen to dendritic cells via an anti-DEC-205 single-chain fragment variable molecule. Clin Cancer Res 2008, 14(December (24)):8169-8177.
49. Cheong C., Choi J-H., Vitale L., He L-Z., Trumpfheller C., Bozzacco L., et al. Improved cellular and humoral immune responses in vivo following targeting of HIV gag to dendritic cells within human anti-human DEC205 monoclonal antibody. Blood 2010, 116(November (19)):3828-3838.
50. Gurer C., Strowig T., Brilot F., Pack M., Trumpfheller C., Arrey F., et al. Targeting the nuclear antigen 1 of Epstein-Barr virus to the human endocytic receptor DEC-205 stimulates protective T-cell responses. Blood 2008, 112(August (4)):1231-1239.
51. Granelli-Piperno A., Pritsker A., Pack M., Shimeliovich I., Arrighi J-F., Park C.G., et al. Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin/CD209 is abundant on macrophages in the normal human lymph node and is not required for dendritic cell stimulation of the mixed leukocyte reaction. J Immunol 2005, 175(October (7)):4265-4273.
52. Bozzacco L., Trumpfheller C., Siegal F.P., Mehandru S., Markowitz M., Carrington M., et al. DEC-205 receptor on dendritic cells mediates presentation of HIV gag protein to CD8+ T cells in a spectrum of human MHC I haplotypes. Proc Natl Acad Sci USA 2007, 104(January (4)):1289-1294.
53. Fujii S., Liu K., Smith C., Bonito A.J., Steinman R.M. The linkage of innate to adaptive immunity via maturing dendritic cells in vivo requires CD40 ligation in addition to antigen presentation and CD80/86 co-stimulation. J Exp Med 2004, 199:1607-1618.
54. Sin J.I., Kim J.J., Zhang D., Weiner D.B. Modulation of cellular responses by plasmid CD40L: CD40L plasmid vectors enhance antigen-specific helper T cell type 1 CD4+ T cell-mediated protective immunity against herpes simplex virus type 2 in vivo. Hum Gene Ther 2001, 12:1091-1102.
55. Tripp R.A., Jones L., Anderson L.J., Brown M.P. CD40 ligand (CD154) enhances the Th1 and antibody responses to respiratory syncytial virus in the BALB/c mouse. J Immunol 2000, 164(June (11)):5913-5921.
56. Allred D.R., McGuire T.C., Palmer G.H., Leib S.R., Harkins T.M., McElwain T.F., et al. Molecular basis for surface antigen size polymorphisms and conservation of a neutralization-sensitive epitope in Anaplasma marginale. Proc Natl Acad Sci USA 1990, 87:3220-3224.
57. Barbet A.F., Palmer G.H., Myler P.J., McGuire T.C. Characterization of an immunoprotective protein complex of Anaplasma marginale by cloning and expression of the gene coding for polypeptide Am105L. Infect Immun 1987, 55(October (10)):2428-2435.
58. Palmer G.H., Rurangirwa F.R., Kocan K.M., Brown W.C. Molecular basis for vaccine development against the ehrlichial pathogen Anaplasma marginale. Parasitol Today 1999, 15(July (7)):281-286.
59. Palmer G.H., McElwain.T.F. Molecular basis for vaccine development against anaplasmosis and babesiosis. Vet Parasitol 1995, 57(1-3 Mar):233-253.
60. Brown W.C., Palmer G.H., Lewin H.A., McGuire.T.C. CD4+ T lymphocytes from calves immunized with Anaplasma marginale Major Surface Protein 1 (MSP1), a heteromeric complex of MSP1a and MSP1b, preferentially recognize the MSP1a carboxyl terminus that is conserved among strains. Infect Immun 2001, 69(November (11)):6853-6862.
61. Palmer G.H., Waghela S.D., Barbet A.F., Davis W.C., McGuire.T.C. Characterization of a neutralization-sensitive epitope on the Am 105 surface protein of Anaplasma marginale. Int J Parasitol 1987, 17(October (7)):1279-1285.
62. Brown W.C., McGuire T.C., Mwangi W., Kegerreis K.A., Macmillan H., Lewin H.A., et al. Major histocompatibility complex class II DR-restricted memory CD4+ T lymphocytes recognize conserved immunodominant epitopes of Anaplasma marginale major surface protein 1a. Infect Immun 2002, 70:5521-5532.
63. Brown W.C., Shkap V., Zhu D., McGuire T.C., Tuo W., McElwain T.F., et al. CD4+ T-lymphocyte and immunoglobulin G2 responses in calves immunized with Anaplasma marginale outer membranes and protected against homologous challenge. Infect Immun 1998, 66(November (11)):5406-5413.
64. Gliddon D.R., Hope J.C., Brooke G.P., Howard C.J. DEC-205 expression on migrating dendritic cells in afferent lymph. Immunology 2004, 111(March (3)):262-272.
65. McIlhinney R.A. Generation and use of epitope-tagged receptors. Methods Mol Biol 2004, 259:81-98.
66. Edwards C.P., Aruffo A. Current applications of COS cell based transient expression systems. Curr Opin Biotechnol 1993, 4:558-563.
67. Mazzei G.J., Edgerton M.D., Losberger C., Lecoanet-Henchoz S., Graber P., Durandy A., et al. Recombinant soluble trimeric CD40 ligand is biologically active. J Biol Chem 1995, 270:7025-7028.
68. Mertens.B.C.M., Gaidulis L. Cloning of two members of the TNF-superfamily in cattle: CD40 ligand and tumor necrosis factor alpha. Immunogenetics 1995, 42:430-431.
69. Zhuang Y., Mwangi W., Brown W.C., Davis W.C., Hope J.C., Palmer G.H. Characterization of a phenotypically unique population of CD13+ dendritic cells resident in the spleen. Clin Vaccine Immunol 2006, 13:1064-1069.
70. Mwangi W., Brown W.C., Palmer G.H. Identification of fetal liver tyrosine kinase 3 (Flt3) ligand domain required for receptor binding and function using naturally occurring ligand isoforms. J Immunol 2000, 165(12):6966-6974.
71. Mwangi W., Brown W.C., Splitter G.A., Davies C.J., Howard C.J., Hope J.C., et al. DNA vaccine construct incorporating intercellular trafficking and intracellular targeting motifs effectively primes and induces memory B- and T-cell responses in outbred animals. Clin Vaccine Immunol 2007, 14(March (3)):304-311.
72. Mwangi W., Brown W.C., Splitter G.A., Zhuang Y., Kegerreis K., Palmer G.H. Enhancement of antigen acquisition by dendritic cells and MHC class II-restricted epitope presentation to CD4+ T cells using VP22 DNA vaccine vectors that promote intercellular spreading following initial transfection. J Leukoc Biol 2005, 78(August (2)):401-411.
73. Pan P-Y., Li Y., Li Q., Gu P., Martinet O., Thung S., et al. In situ recruitment of antigen-presenting cells by intratumoral GM-CSF gene delivery. Cancer Immunol Immunother 2004, 53(1):17-25.
74. Shalaby W.S.W., Yeh H., Woo E., Corbett J.T., Gray H., June C.H., et al. Absorbable microparticulate cation exchanger for immunotherapeutic delivery. J Biomed Mater Res Part B: Appl Biomater 2004, 69B(2):173-182.
75. Mwangi W., Brown W.C., Splitter G.A., Davies C.J., Howard C.J., Hope J.C., et al. DNA vaccine construct incorporating intercellular trafficking and intracellular targeting motifs effectively primes and induces memory B- and T-cell responses in outbred animals. Clin Vaccine Immunol 2007, 14(3):304-311.
76. Norimine J., Han S., Brown W. Quantitation of Anaplasma marginale major surface protein (MSP)1a and MSP2 epitope-specific CD4 T lymphocytes using bovine DRB3*1101 and DRB3*1201 tetramers. Immunogen 2006, 58(9):726-739.
77. Maamary J., Array F., Gao Q., Garcia-Sastre A., Steinman R.M., Palese P., et al. Newcastle disease virus expressing a dendritic cell-targeted HIV gag protein induces a potent gag-specific immune response in mice. J Virol 2011, 85(March (5)):2235-2246.
78. Nchinda G., Kuroiwa J., Oks M., Trumpfheller C., Park C.G., Huang Y., et al. The efficacy of DNA vaccination is enhanced in mice by targeting the encoded protein to dendritic cells. J Clin Invest 2008, 118(4):1427-1436.
79. Tewari K., Flynn B.J., Boscardin S.B., Kastenmueller K., Salazar A.M., Anderson C.A., et al. Poly(I:C) is an effective adjuvant for antibody and multi-functional CD4+ T cell responses to Plasmodium falciparum circumsporozoite protein (CSP) and αDEC-CSP in non human primates. Vaccine 2010, 28(45):7256-7266.
80. Huang H-I., Wu P-Y., Teo C-Y., Chen M-N., Chen Y-C., Silin D., et al. Improved immunogenicity of a self tumor antigen by covalent linkage to CD40 ligand. Int J Cancer 2004, 108(5):696-703.
81. Chen H-W., Huang H-I., Lee Y-P., Chen L-L., Liu H-K., Cheng M-L., et al. Linkage of CD40L to a self-tumor antigen enhances the antitumor immune responses of dendritic cell-based treatment. Cancer Immunol Immunother 2002, 51(6):341-348.
82. Gares S.L., Fischer K.P., Congly S.E., Lacoste S., Addison W.R., Tyrrell D.L., et al. Immunotargeting with CD154 (CD40 ligand) enhances DNA vaccine responses in ducks. Clin Vaccine Immunol 2006, 13(August (8)):958-965.
83. Yao Q., Fischer K.P., Li L., Agrawal B., Berhane Y., Tyrrell D.L., et al. Immunogenicity and protective efficacy of a DNA vaccine encoding a chimeric protein of avian influenza hemagglutinin subtype H5 fused to CD154 (CD40L) in Pekin ducks. Vaccine 2010, 28(51):8147-8156.
84. Li W. Synergistic antibody induction by antigen-CD40 ligand fusion protein as improved immunogen. Immunology 2005, 115(2):215-222.
85. Han S., Norimine J., Palmer G.H., Mwangi W., Lahmers K.K., Brown W.C. Rapid deletion of antigen-specific CD4+ T cells following infection represents a strategy of immune evasion and persistence for Anaplasma marginale. J Immunol 2008, 181(December (11)):7759-7769.
86. Park Y., Joo Y.S., Park J.Y., Moon J.S., Kim S.H., Kwon N.H., et al. Characterization of lymphocyte subpopulations and major histocompatibility complex haplotypes of mastitis-resistant and susceptible cows. J Vet Sci 2004, 5(1):29-39.