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Prepublished online as a Blood First Edition Paper on October 10, 2002; DOI 10.1182/blood-2002-07-1989.
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Blood, 15 February 2003, Vol. 101, No. 4, pp. 1637-1644
TRANSPLANTATION
T-cell clones can be rendered specific for CD19: toward the
selective augmentation of the graft-versus-B-lineage leukemia
effect
Laurence J. N. Cooper,
Max S. Topp,
Lisa Marie Serrano,
Sergio Gonzalez,
Wen-Chung Chang,
Araceli Naranjo,
Christine Wright,
Leslie Popplewell,
Andrew Raubitschek,
Stephen J. Forman, and
Michael C. Jensen
From the Divisions of Pediatric Hematology/Oncology,
Molecular Medicine and Hematology and Bone Marrow
Transplant, and Department of Radioimmunotherapy, Beckman
Research Institute and City of Hope National Medical Center, Duarte,
CA; and Fred Hutchinson Cancer Research Center, Division of Clinical
Research, Seattle, WA.
Relapse of B-lineage acute lymphoblastic leukemia (B-ALL) after
allogeneic hematopoietic stem cell transplantation (HSCT) commonly
results from the failure of a graft-versus-leukemia (GVL) effect to
eradicate minimal residual disease. Augmenting the GVL effect by the
adoptive transfer of donor-derived B-ALL-specific T-cell clones is a
conceptually attractive strategy to decrease relapse rates without
exacerbating graft-versus-host disease (GVHD). Toward this end, we
investigated whether a genetic engineering approach could render
CD8+ cytotoxic T lymphocytes (CTLs) specific for tumor
cells that express the B-cell lineage cell surface molecule CD19. This
was accomplished by the genetic modification of CTLs to express a chimeric immunoreceptor composed of a CD19-specific single-chain immunoglobulin extracellular targeting domain fused to a
CD3- intracellular signaling domain. CD19-redirected CTL clones
display potent CD19-specific lytic activity and chimeric
immunoreceptor-regulated cytokine production and proliferation. Because
B-ALL cells can evade T-cell/natural killer- cell recognition by
down-regulation of cell surface accessory molecules that participate in
the formation of a functional immunologic synapse, we compared the
CD19-specific effector function of genetically modified
CD8+ CTLs toward CD19+ cells with disparate
levels of intercellular adhesion molecule 1 (ICAM-1), leukocyte
function-associated antigen 1 (LFA-1), and LFA-3. We observed that
recognition of B-lineage tumor lines by CD19-specific CTLs was not
impaired by low levels of ICAM-1, LFA-1, and LFA-3 cell surface
expression, a functional attribute that is likely a consequence of our
high-affinity CD19-specific chimeric immunoreceptor. Furthermore, the
CD19-specific CTLs could lyse primary B-ALL blasts. These preclinical
observations form the basis for implementing clinical trials using
donor-derived CD19-specific T-cell clones to treat
or prevent relapse of B-ALL after allogeneic HSCT.
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