BIN1 Inhibits Colony Formation and Induces Apoptosis in Neuroblastoma Cell
Lines with MYCN Amplification
Michael D. Hogarty, MD,* Xueyuan Liu, MA, Patricia M. Thompson, BS,
Peter S. White, PhD, Erik P. Sulman, BA, John M. Maris, MD, and
Garrett M. Brodeur, MD
Background. MYCN amplification and
overexpression occurs in 25% of neuroblasto-
mas and independently predicts for poor prog-
nosis disease, an effect thought to be mediated
by its role as a transcriptional activator of
growth promoting genes. However, in many
mammalian cells, deregulated expression of
MYC family genes (including MYCN) induces
apoptosis. We hypothesized that BIN1, a MYC
interacting protein capable of inducing apopto-
sis, may be an important regulator of MYCN in
neuroblastoma. Results. BIN1 expression was
found to be reduced in MYCN-amplified cell
lines. Further, forced expression of BIN1 mark-
edly reduced colony formation in MYCN-
amplified, but not single-copy, cell lines. This
effect appeared to be caused by an increase in
apoptosis, and was augmented by serum depri-
vation and concurrent cytotoxic drug therapy in
cell culture Conclusion. BIN1 inactivation may
be necessary for MYCN overexpression to lead
to cellular proliferation rather than pro-
grammed cell death in neuroblastomas with
MYCN amplification. Med. Pediatr. Oncol.
35:559–562, 2000 © 2000 Wiley-Liss, Inc.
Key words: neuroblastoma; BIN1; MYCN; genes; suppressor; tumor; apoptosis
INTRODUCTION
Amplification of the MYCN proto-oncogene occurs in
a subset of highly aggressive neuroblastomas and por-
tends poor disease outcome independent of other clinical
or biological factors [1,2]. This effect is believed to be
mediated through the function of MYCN as a transcrip-
tional regulator of genes critical to cell cycle entry and
progression [3]. Interestingly however, the MYC family
of oncogenes (which includes MYC, MYCN, and MYCL)
are also strong inducers of apoptosis when their expres-
sion is deregulated from mitogenic signaling pathways
[4], which is postulated as a protective mechanism
against neoplastic transformation. In many malignancies,
however, circumventing the apoptotic response to dereg-
ulated MYC expression is achieved through constitutive
cytokine signaling or up-regulation of antiapoptotic
genes such as BCL2, as commonly occurs in lymphomas
[5]. Similarly, inactivation of proapoptotic genes, such as
has recently been described with caspase 8 in neuroblas-
toma [6], may be instrumental in circumventing apopto-
sis.
BIN1 is a MYC-interacting protein cloned through its
physical interaction with MYC in a yeast two-hybrid
system, which has been shown to strongly and specifi-
cally inhibit MYC-mediated transformation in rat embryo
fibroblasts [7]. Further, BIN1 expression is reduced or
absent in many malignant cell lines and primary tumors,
and forced expression of BIN1 in these cells results in a
reduction in colony formation [7]. These results suggest
that BIN1 may function as a MYC-interacting tumor sup-
pressor. MYCN shares 100% identity with MYC in the
BIN1-interacting domain and BIN1 is highly expressed
in neural tissues. Therefore, we hypothesized that BIN1
may be a regulator of MYCN function in developing
neuroblasts, and that BIN1 inactivation may be necessary
for MYCN overexpression to drive cellular proliferation
rather than programmed cell death in neuroblastomas
with MYCN amplification.
MATERIALS AND METHODS
Cell Culture
The neuroblastoma cell lines used in this study have
been described previously and included eight cell lines
with MYCN amplification (NMB, NGP, IMR5, SMS-
KAN, NLF, CHP134, CHP126, SMS-KCN) and four
MYCN single-copy cell lines (SK-N-AS, NB69, LA-N-6,
NBL-S) [8]. The cell lines SJRH30 (alveolar rhabdomyo-
sarcoma) and T47D (breast carcinoma) were used as con-
trols. All cell lines were grown in supplemented RPMI
Media 1640 (Life Technologies, Gaithersburg, MD) at
37°C in a humidified atmosphere of 5% CO
2
as previ-
ously described [8].
Department of Pediatrics, University of Pennsylvania School of Medi-
cine and The Children’s Hospital of Philadelphia, Philadelphia, Penn-
sylvania.
Grant Sponsor: American Society of Clinical Oncology (MDH); Grant
Sponsor: MAPS-CHRC (MDH).
*Correspondence to: M.D. Hogarty, Division of Oncology, ARC
Room 902, The Children’s Hospital of Philadelphia, 3516 Civic Cen-
ter Boulevard, Philadelphia, PA 19104-4318.
E-mail: hogartym@email.chop.edu
Medical and Pediatric Oncology 35:559–562 (2000)
© 2000 Wiley-Liss, Inc.