Key Discoveries

The National Cancer Institute has assumed a leading role in Acquired Immunodeficiency Syndrome (AIDS) research since the disease was first recognized in 1981. Because of the research programs and administrative mechanisms already in place, investigators were able to rapidly apply existing methods in drug screening and advances in cancer virus research technology to the study of AIDS. The large scale preparation of HIV-1 in permanent cell lines led to the development of a serological test for AIDS which enabled the detection of AIDS in our nation's blood supply. Detection of the virus in latent form has been established through the in situ hybridization method which allowed scientists to detect the virus in brain and blood cells, T lymphocytes and macrophages. Selected recent key discoveries, by NCI investigators include:
Development, testing and successful clinical trials of the drugs azidothymidine (AZT), dideoxyinosine
(ddI) and dideoxycytidine (ddC), confirming their effectiveness as anti-retroviral agents against AIDS.
Progress in treating children with AIDS has occurred through the rapid introduction of antiretroviral
agents into clinical trials. The studies performed by the Pediatric Branch contributed to the licensure of
AZT for children in May of 1990 and dideoxyinosine (ddI) in October 1991. The latter, based solely on
Pediatric Branch Studies, occurred simultaneously with licensure for adults, a historical event. The
Pediatric Branch is currently completing studies of combination regimens to optimize activity (e.g., AZT
plus ddI) as well as to offset toxicity (e.g., AZT plus G-CSF and erythropoietin).
Viral particles are detectable in plasma throughout the early stages of primary infection. The number of
viral particles in plasma decrease by up to 200-fold following the initial viremia of primary infection, but
increases again as the infection moves from the asymptomatic phase in AIDS-related complex (ARC)
to full blown AIDS. The increase in viral particles bears an inverse relationship to CD4 count. Scientists
at NCI and elsewhere have adapted Polymerase Chain Reaction (PCR) technology to detect and
quantitate the amount of HIV-1 RNA present in plasma. A new adaptation of PCR technology,
designated "immuno-PCR", is capable of detecting minute amounts of HIV regulatory proteins (e.g. Tat,
Rev) in solution or in tissue. "Immuno-PCR" can be applied to the in situ analysis of certain clinical
specimens, such as lymph node. Thus, PCR technologies provide the opportunity to correlate HIV
protein expression with virulence and pathogenicity in both the laboratory and clinical settings, and may
serve as sensitive markers by which to measure response to therapy.
The ability to provide effective long-term anti-retroviral therapy using single agents for HIV infection is
complicated by the emergence of drug-resistant HIV strains. Longitudinal studies of the phenotypic and
genotypic changes of HIV strains isolated before and after prolonged therapy with either an alternating
regimen of AZT and ddC or ddI alone demonstrate that HIV develops reduced susceptibility to AZT
more readily than to ddC and with ddI. A new acyclic purine analog, PMEA, inhibits both HIV RT and
DNA polymerase-alpha from CMV and other herpes viruses and may inhibit latent as well as replicating
HIV, with perhaps a special activity against the HIV reservoir in monocytes/macrophages. NCI scientists
began the Phase I clinical testing of PMEA in combination with AZT in January 1994, in conjunction with
assessment of intrinsic or induced HIV resistance to PMEA.
A recent clinical trial by NCI investigators suggests that the simultaneous administration of AZT and ddI
results in higher and more sustained elevations of CD4+ cells over a one year period than alternating
drug administration. This difference in clinical activity may relate to differential intracellular drug
activation. AZT is preferentially phosphorylated to the active triphosphate form (AZT-TP) in
proliferating cells. In contrast, the phosphorylation of ddI (to ddATP) and ddC (to ddC-TP) occurs
preferentially in resting cells. Thus, the data suggest that AZT, ddC and ddI may exert their antiviral
effects depending on the activation state of the target cells; i.e., ddI and ddC likely exert antiviral activity
against resting cells, while AZT protects actively growing cells against HIV infection. The combination
of AZT+ddI may target both latent and actively replicating pools of virus, providing complementary and
possibly synergistic anti-HIV activity.
Identification through the high-capacity AIDS drug screen of many new compounds which are active
against the AIDS virus in tissue culture experiments. These compounds include both synthetic drugs
and natural products. Several of these are in the initial phases of development.
NCI's AIDS Drug Screen has recently uncovered an active compound with an unprecedented
mechanism of action, namely the disruption of the highly conserved zinc finger regions of the HIV
nucleocapsid protein, p7. The nucleocapsid protein is necessary for the incorporation of the viral RNA
genome into intact viral particles and the ultimate packaging of the infectious virions. The ability to
block viral reproduction and dissemination by inhibiting the structural and functional integrity of p7 will
serve two critical goals: a heightened molecular understanding of the late stages of the viral life cycle,
and a template for rational drug design based upon the protein sequence and structure.
The HIV-1 enzyme reverse transcriptase (RT) is the target for inhibition by many of the currently
available anti-retroviral agents, in particular the nucleosides (AZT, ddI, ddC, d4T). Unfortunately, RT is
able to undergo mutations that confer resistance to the inhibitory effects of these drugs. Scientists at
NCI's Frederick Cancer Research and Development Center have both structural and biochemical data
to suggest that the Leu74Val mutation, which causes resistance to ddI, affects the interaction between
RT and its nucleic acid substrate. In addition, these scientists continue to define the structure of HIV-1
RT and the complexes formed between RT and its nucleic acid substrates.
Integration of RT-transcribed HIV DNA into the host genome is facilitated by HIV integrase, an enzyme
encoded by the HIV pol gene. NCI scientists have devised rapid fluorescent assays that identify both
the DNA cleavage reaction and the subsequent integration process in response to purified HIV
integrase. The ability to quantitate integrase activity by measuring cleavage-induced changes in
fluorescence will also identify agents that block integrase action and thus present a novel molecular
target for therapy.
Determination of the first crystal structure of retroviral protease and its successful use to predict the
structure of the HIV protease and substrate using supercomputer methodology. HIV protease is an
enzyme whose action is required in the processing of HIV proteins and production of infectious virions.
NCI scientists have identified several inhibitors of the HIV protease including KNI-272 which has
exhibited potent anti-HIV activity and favorable pharmacokinetics in test animals. In March 1994 NCI
scientists began Phase 1 clinical trials of KNI-272.
Individuals infected with HIV may be asymptomatic for years before progressing to overt AIDS. Since
monocytes possess surface CD4 molecules, they can bind and act as a reservoir for HIV in infected
individuals. Thus, monocytes in AIDS patients can harbor latent HIV inducible by T cells during an
immune response. HIV produced by such monocytes infects T cells leading to viral-induced
pathology. In addition to monocytes, NIAID scientists determined that follicular dendritic cells (FDC)
also serve as reservoirs for latent HIV infection, sequestering HIV for eventual transmission to CD4+
cells.
IL-12, produced by macrophages and B cells in response to diverse infectious pathogens, is a natural
killer (NK) cell stimulatory factor which activates NK cells in vitro and appears to have a significant
antitumor effect in tumor-bearing animals. IL-12 drives the differentiation of naive CD4+ T cells into TH1
cells, thereby promoting cell-mediated immunity. IL-12 may have a special role as an immunostimulant
in HIV infection, where both NK cell and TH1 cell functions are defective. IL-12 may also be able to
restore the HIV-related imbalance between TH1 and TH2 cells which, in turn, leads to defects in cellular
immunity and excessive humoral (antibody) responses.
The magnitude of CNS disease is often more prominent and the latency period which precedes HIV-
related encephalopathy shorter in children than in adults, suggesting that fetal or developing brain cells
(in particular, glial cells) may release cytokines capable of activating expression of latent HIV.
To address the pathogenesis of neurologic disorders in HIV-1 infected children, NCI scientists have
developed an in vitro model using a normal fetal olfactory neuroblast cell line, to investigate the
potential contributions of direct viral infection and virally-induced cytokines in glial (and perhaps other
accessory) cells to neurodevelopmental impairment.
NCI epidemiologists have played a major role in uncovering the emergence of a new peak of
tuberculosis (TB)-associated death in young individuals (ages 20-49) that appears linked to AIDS.
Recent studies of vaginally-delivered multiple birth cohorts in HIV-infected women demonstrate that
HIV transmission is greatest for the first-born infant, suggesting that some component of HIV
transmission occurs at the time of the delivery in the cervix or vagina.
Indeed, about 60 percent of mother-to-infant HIV transmission occurs at the time of birth. On this basis,
scientists are designing a clinical trial of inexpensive viricidal solution to cleanse the birth canal to lower
the risk of HIV transmission in this setting.
NCI has established a multi-state AIDS/cancer match registry linking AIDS and cancer registries in five
areas of NCI's Surveillance, Epidemiology and End Results (SEER) program (San Francisco, Los
Angeles, Atlanta, Detroit and Connecticut) and 10 other sites (New York City and state, New Jersey,
Puerto Rico, San Diego, Sacramento, Florida, Illinois, Colorado and Massachusetts). The Registry
encompasses about 75 percent of all reported AIDS cases and involves approximately 85,000 matches
of individuals with AIDS to cancer registries. This very large data base allows for the first time
quantitative estimates of rare as well as common malignancies and provides a framework for
determining the role of HIV as a cofactor in the development of diverse malignancies. The registry will
also serve to identify patients with concomitant AIDS and cancer from whom tumor tissue and other
biologic specimens can be obtained for molecular epidemiologic studies.
NCI scientists have developed prototype synthetic vaccines consisting of broadly-recognized
histocompatibility determinants of T helper cells (so-called "cluster peptides") and a combined site
constructed to elicit both cytotoxic T lymphocytes (CTL) and neutralizing antibody. Clinical trials of
these constructs are now being launched.
NCI scientist have constructed novel vaccines comprised of various recombinant and live vectors
carrying HIV-1, HIV-2 and SIV antigenic proteins or protein units. These constructs are now being
tested in rhesus macaques for their efficacy as initial immunogens, followed by "boosters" using
purified native or viral antigens, in eliciting protective immune responses. Recombinant constructs
coupling vaccinia virus (poxvirus) vectors to various HIV antigens induce virus-specific cellular and
humoral responses in primates. Vaccine constructs coupling adenovirus with HIV-1 MN or IIIB env
genes have been shown to elicit both T cell and neutralizing antibody responses, and will be examined
in chimpanzees for their protective effects against viral challenge. Finally, influenza recombinants,
designed such that the V3 loop is located within a region of the hemagglutinin molecule that is
conformationally accessible to antibodies, are being developed as a booster immunogen.
NCI investigators have put the poly Tat activation region (TAR) which binds to the viral regulatory
protein, Tat, into the HIV promoter, thereby inhibiting viral replication. Since binding of Tat to TAR is
necessary for RNA expression and viral replication, the polymeric TAR (poly TAR) provides a
molecular decoy which inhibits viral replication. Cultures containing the protected cells show a gradual
decline in virus production that reaches 90 percent in two months. Six months after infection the
protected cell cultures express little detectable virus and are resistant to reinfection. Poly TAR
appears to be an effective antiviral gene that may have eventual clinical application as a gene therapy
modality.
NCI investigators have detected large numbers of KS-like spindle cells in cultures of circulating
peripheral blood of HIV+ patients with active KS or at high risk for development of KS. These cells
have spindle-shaped morphology and immunophenotypic characteristics of activated endothelial cells,
and produce angiogenic factors. The numbers of peripheral blood spindle cells from HIV+ patients with
active KS and from those at high risk are increased 78-fold and 18-fold, respectively, over the numbers
detectable in HIV- or HIV+ low-risk individuals. The ability to detect such cells may predict
susceptibility to develop KS and could serve to monitor the impact of therapeutic and prevention
interventions.
NCI scientists have developed spindle cell strains that provide models of KS for the exploration of new
therapeutic approaches. Most recently, a unique KS patient-derived cell line exhibits unlimited cellular
life span in vitro and aggressive, metastatic behavior in vivo in immunosuppressed mice, with formation
of highly vascularized tumor nodules. This model mimics KS progression in the human setting and
thus may provide an excellent model for dissection of KS pathophysiology and development of targeted
antitumor modalities.
Multiple cytokines (growth factors) with inflammatory, growth-promoting and immunostimulating
activities make pivotal contributions to the molecular pathogenesis and clinical phenotype of AIDS-KS.
The HIV Tat protein, in particular the biologically active form that is released extracellularly, augments
both viral and host gene expression. Basic fibroblast growth factor (b-FGF), an inflammatory cytokine
produced by AIDS-KS cells as well as stromal cells, promotes new blood vessel formation
(angiogenesis) and wound healing. It has now been shown that b-FGF and Tat interact synergistically
to induce proliferation of normal vascular cells and produce KS-like angiogenic lesions in mice in vivo.
This cooperation is magnified in the HIV+ setting, where b-FGF, extracellular Tat and Tat receptors are
present to drive the emergence and aggressive progression of KS.
A glycoprotein growth factor known as Oncostatin M, derived from activated T-cells, is a potent growth
stimulator for AIDS-KS cells. This growth factor is distinct from other important cytokines in AIDS-KS,
namely IL-6 and the HIV Tat protein, but binds to the active subunit of the IL-6 receptor. Oncostatin M
appears to cause AIDS-KS cell proliferation both directly and in part by enhancing the expression of IL-
6 by vascular endothelial cells, and further induces morphologic changes in AIDS-KS cells, namely to
the spindle configuration of smooth muscle cells.
NCI scientists have found a non-cytotoxic bacterial product, a sulfated polysaccharide-peptidoglycan
compound (SP-PG) which inhibits the growth and vascular responses, in particular the induction of
angiogenesis and hyperpermeability, of AIDS-KS spindle cells in vitro and in a nude mouse model.
The striking production of autostimulatory and angiogenic growth factors by KS cells suggest that
these factors should be an important target for therapy. Phase I clinical trials of angiogenesis inhibitors
are underway.
NCI scientists are investigating the antitumor effects of the cytotoxic natural product taxol, a unique
tubulin-binding agent, in AIDS-related Kaposi's sarcoma (KS). Of 17 patients treated to date, 50
percent have achieved objective partial responses with roughly 50 percent decreases in number, size
and/or nodularity of KS lesions and an additional 40 percent have had stabilization of disease.
Profound cellular immunodeficiency plays a central role in lymphomagenesis. NCI investigators have
found that the most important risk factor determinant for both the AZT- and ddI-treated cohort/s is a
CD4 count below the critical level of 50/mm3. In addition, elevated serum levels of IL-6 predict a high
risk for NHL development.
The remarkable occurrence of high-grade B-cell, non-Hodgkin's lymphomas (NHL) has recently
emerged as a major sequela of HIV infection, especially in patients who survive other consequences of
AIDS in a protracted state of profound immunosuppression. NHLs develop in approximately 10
percent of AIDS patients treated with dideoxynucleosides. NCI investigators have developed a
"lymphoma subpanel" comprised of two AIDS lymphoma cell lines including an EBV+ Burkitt's
lymphoma, and eight non-AIDS lymphoma cell lines for screening potential therapeutic compounds.
The severe combined immunodeficiency (SCID) mouse provides a unique model for the study of AIDS-
related lymphoma biology and anti-lymphoma drug development. To date, about 500 agents have been
examined for in vitro antitumor activity against an EBV+ Burkitt's lymphoma derived from an HIV-infected
patient. This human tumor cell line has been established as a reproducible in vivo model within the SCID
mouse. Approximately 18 agents have been evaluated in the in vivo model with 3 showing antitumor
activity. Further, the CNS involvement of the SCID mouse with this lymphoma provides an opportunity to
predict agents that have access to this frequently involved sanctuary in patients. The lymphoma subpanel
is being expanded to establish and characterize new AIDS-related lymphoma cell lines, develop
"mechanism of action" assays (e.g. IL-6 inhibition, induction of programmed cell death, antiviral effects
targeting EBV or other viral cofactors) and define the differential drug sensitivity testing in the in vivo SCID
model.