The Journal of Experimental Medicine
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Published 7 June 2004. doi:10.1084/jem.20032083
Rockefeller University Press, 0022-1007 $8.00
JEM, Volume 199, Number 11, 1585-1593
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Distinct Time Effects of Vaccination on Long-Term Proliferative and IFN-{gamma}–producing T Cell Memory to Smallpox in Humans

Behazine Combadiere1, Alexandre Boissonnas1, Guislaine Carcelain, Evelyne Lefranc1, Assia Samri1, François Bricaire2, Patrice Debre1, and Brigitte Autran1

1 Laboratoire d'Immunologie Cellulaire, INSERM U543, and 2 Service de Maladies Infectieuses, Hôpital Pitié-Salpétrière, Université Pierre et Marie Curie, 75013 Paris, France

Correspondence should be addressed to Brigitte Autran, Laboratoire d'Immunologie Cellulaire, Hôpital Pitié-Salpétrière, 83 Bd de l'Hôpital, 75013 Paris, France. Phone: 33-1-42-177481; Fax: 33-1-42-177490; email: brigitte.autran{at}psl.ap-hop-paris.fr

Residual immunity to the smallpox virus raises key questions about the persistence of long-term immune memory in the absence of antigen, since vaccination ended in 1980. IFN-{gamma}–producing effector–memory and proliferative memory T cells were compared in 79 vaccinees 13–25 yr after their last immunization and in unvaccinated individuals. Only 20% of the vaccinees displayed both immediate IFN-{gamma}–producing effector–memory responses and proliferative memory responses at 6 d; 52.5% showed only proliferative responses; and 27.5% had no detectable vaccinia-specific responses at all. Both responses were mediated by CD4 and CD8 T cells. The vaccinia-specific IFN-{gamma}–producing cells were composed mainly of CD4Pos CD45RANeg CD11aHi CD27Pos and CCR7Neg T cells. Their frequency was low but could be expanded in vitro within 7 d. Time since first immunization affected their persistence: they vanished 45 yr after priming, but proliferative responses remained detectable. The number of recalls did not affect the persistence of residual effector–memory T cells. Programmed revaccination boosted both IFN-{gamma} and proliferative responses within 2 mo of recall, even in vaccinees with previously undetectable residual effector–memory cells. Such long-term maintenance of vaccinia-specific immune memory in the absence of smallpox virus modifies our understanding of the mechanism of persistence of long-term memory to poxviruses and challenges vaccination strategies.

Key Words: smallpox • vaccine • central memory T cells • effector–memory T cells

B. Combadiere and A. Boissonnas contributed equally to this work.

Abbreviations used in this paper: BCG, Bacille de Calmette et Guérin; BrdU, bromodeoxyuridine; SFC, spot-forming cell.


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