Vol. 7, 917s-924s, March 2001 (Suppl.) Clinical Cancer Research 917s
Intrathecal Cytotoxic T-Cell Immunotherapy for Metastatic
Leptomeningeal Melanoma a
Annette R. Clemons-Miller, Gurkamal S. Chatta,
Laura Hutchins, Edgardo J. Angtuaco,
Antonella Ravaggi, Alessandro D. Santin, and
Martin J. Cannon 2
Departments of Geriatrics [A. R. C-M., G. S. C.], Medicine [G. S. C.,
L. H.], Radiology [E. J. A.], Obstetrics and Gynecology [A. R.,
A. D. S.], and Microbiology and Immunology [A. R. C-M., M. J. C.],
University of Arkansas for Medical Sciences, Little Rock, Arkansas
72205, and Division of Gynecologic Oncology, University of Brescia
Medical School, Brescia, Italy [A. R., A. D. S.]
Abstract
A 49-year-old patient with primary, recurrent melanoma
on the lower extremity developed metastatic leptomeningeal
melanoma that did not respond to treatment with radiation
therapy or intrathecal interleukin 2 (IL-2). Disease was char-
acterized by neurological symptoms, including loss of hearing,
loss of short-term memory, and gait disturbance. CD8 + CTLs
were generated in vitro using autologous dendritic cells pulsed
with peptides from the melanoma-associated antigens tyrosin-
ase (145-156), Melan-A/MART-1 (26-35), and gpl00/Pmel 17
(209-217). The CTLs exhibited up to 74% specific lysis against
peptide-pulsed autologous EBV-transformed B cells, with
Melan-A-specific CTLs yielding the greatest lytic activity.
CD8 + CTLs possessed a type 1 cytokine profile, expressing
tumor necrosis factor oL and IFN~/but not IL-4. Infusions of
CTLs were supported with systemic low-dose IL-2 administra-
tion. 111In labeling and computerized gamma imaging were
used to monitor the distribution of CTLs up to 48 h after
infusion. Intra-arterial delivery via the right carotid artery was
followed by redistribution of the CTLs to the lungs, liver, and
spleen within 16 h. In contrast, delivery via an indwelling
Ommaya reservoir resulted in prolonged retention of CTLs
within the brain for at least 48 h after infusion. Marked but
transient elevations in tumor necrosis factor e~, IFN-% and
IL-6 in the cerebrospinal fluid were observed within 4 h of
CTL infusion. There was no evidence of tumor progression
throughout the treatment period, and clinically the patient
showed some resolution of neurological symptoms.
Introduction
Although the immunogenic potential of melanoma has
been recognized for some time, clinical trials involving the use
of tumor-infiltrating lymphocytes or lymphokine-activated
killer cells in the treatment of malignant melanoma have met
with only modest success (1-6). The reasons for the limited
efficacy may include poor definition of the effector cells, failure
of the effector cells to recognize defined antigens, and poor
localization of the effector cells to the site of the tumor. The
recent identification of defined melanoma-associated tumor an-
tigens such as gp 100, Melan-A/MART-1, tyrosinase, MAGE-1,
and MAGE-3 (7-12), combined with the ability to induce T-cell
responses of defined function and phenotype, has led to a strong
resurgence of interest in immunotherapy of melanoma. Most
notably, the application of DCs 3 as powerful inducers of mela-
noma tumor antigen-specific CD8 + cytotoxic CTL responses
has provided investigators with the tools necessary for a targeted
approach to the treatment of disease (13-19).
Notwithstanding the major advances in DC-based induc-
tion of tumor-antigen-specific T-cell responses in patients with
malignant disease, clinical administration of autologous anti-
gen-specific CTLs presents some practical challenges. One of
the more important issues centers on election of an appropriate
route of delivery for optimal localization and retention of CTLs
at the tumor site. The use of radioisotopic cell labeling and
subsequent imaging of T-cell localization in the patient affords
us the opportunity to tailor the route and method of CTL
immunotherapy for optimum delivery to the tumor. Isotopes
such as ~In can be used for short-term visualization and
tracking of cellular components in real time using standard
scanning techniques (20-23).
In this study, we have used autologous DCs pulsed with
defined HLA-restricted peptides from the gpl00, Melan-A/
MART-l, and tyrosinase melanoma antigens to stimulate CD8 +
CTLs for immunotherapeutic treatment of a patient with metastatic
leptomeningeal melanoma. Antigen-specific CTLs were delivered
through catheterization of the internal carotid artery or local deliv-
ery through an indwelling intracranial Ommaya reservoir. ~11In
labeling and computerized gamma imaging were used to monitor
CTL migration and elucidation of the most effective route of
delivery. CTL activity in vivo was assessed indirectly through
measurement of T-cell and inflammatory cytokine production in
the CSF at various time points after treatment.
Materials and Methods
Case History. A 49-year-old woman presented with a
melanocytic nevus (Breslow thickness, 0.8 ram), which was re-
moved in February 1995. A local recurrence (Breslow thickness,
1 This study was supported by NIH Grants CA 63931 (to M. J. C.) and
CA 76033 (G. S. C.) and the Arkansas Cancer Research Center.
a To whom requests for reprints should be addressed, at Department of
Microbiology and Immunology, Mail Slot 511, University of Arkansas
for Medical Sciences, 4301 West Markham, Little Rock, AR 72205.
Phone: (501)296-1254; Fax: (501)686-5359; E-mail: cannonmartin@
exchange.uams.edu.
3 The abbreviations used are: DC, dendritic cell; PBMC, peripheral
blood mononuclear cell; CSF, cerebrospinal fluid; MRI, magnetic res-
onance imaging; GM-CSF, granulocyte/macrophage-colony stimulating
factor; TNF, tumor necrosis factor; IL, interleukin; NK, natural killer;
PMA, phorbol myristate acetate; CNS, central nervous system.
Research.
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