318
BRES 17048
Brain Research, 561 (1991) 318-323
© 1991 Elsevier Science Publishers B.V. All rights reserved. 0006-8993/91/$03.50
ADONIS 0006899391170482
Transferrin can alter physiological properties of retinal neurons
Arnold G. Hyndman 1, Philip E. Hockberger 2'*, Gail D. Zeevalk 1'** and John A. Connor 3
t Department of Biological Sciences, Rutgers University, Piscataway, NJ 08855 (U.S.A.), 2Department of Molecular Biophysics, Bell
Laboratories, Murray Hill, NJ 07974 (U.S.A.) and 3Department of Neuroscience, Roche Institute of Molecular Biology, Nutley,
NJ 07110 (U.S.A.)
(Accepted 21 May 1991)
Key words: Transferrin; Calcium; Retina; Glutamate; Neuron; Culture
The role of transferrin as a possible neurotransmitter was examined in cultured chick retinal cells. Brief exposure to transferrin caused a
dramatic and transient increase in intracellular calcium levels in approximately 20% of the total population of cultured retinal neurons. The
increase in intracellular calcium was observed in cell bodies and neuronal processes. Electrophysiological analysis of a subset of the popu-
lation, bipolar-like neurons, demonstrated that more than half of these cells responded to the application of transferrin with a transient
membrane depolarization. Under voltage clamp conditions, the currents evoked by transferrin were similar to glutamate in that they both
displayed non-linearvoltage dependence. Furthermore, acute transferrin exposure resulted in a 200% increase in the amount of Na ÷ indepen-
dent [3H]glutamate binding observed in these cultures. These results suggest that transferrin may function as a neurotransmitter or neuro-
modulator in the developing vertebrate nervous system.
INTRODUCTION
The serum glycoprotein, transferrin, has long been
known as a major iron transport protein and is widely
used as a growth factor for cells maintained in vitro 3'z°.
There is evidence suggesting that transferrin has a role
in CNS growth, differentiation and function 2'11'17'27"35.
Among the more novel and interesting suggestions is
that transferrin may serve as a neua'omodulator, or in-
fluence the maintenance and regulation of synaptic con-
tacts in the developing CNS 28'30'34.
Using immunohistochemical techniques, we have
shown that transferrin is present in neurites during for-
mation of the inner and outer plexiform layers, as well
as the optic nerve fiber layer of the embryonic chick ret-
ina 34. The relative concentration of transferrin in the
neural retina increases 5-fold between embryonic day
(E) 6 and 10, and then rapidly declines by El4 35. This
time is a critical period in retinal maturation, including
the formation of the retinal synaptic layers.
The coincident timing between elevated transferrin
and retinal maturation suggests that transferrin may be
important for certain cellular activities associated with
neurite growth and connectivity. In this study, we exam-
ined the effects of transferrin on intracellular calcium
levels, electrical activity and transmitter binding. Other
neurotrophic factors such as epidermal growth factor,
insulin and nerve growth factor have been shown to be
capable of modulating these types of neuronal activities 5"
29,33
Our monolayer tissue culture system of purified chick
retinal neurons has proven useful in the examination of
transferrin's effects on the developing CNS. These neu-
rons can be maintained in vitro without transferrin and
yet are capable of binding and internalizing transferrin
in a manner consistent with their developmental stage 2°'
35. In this study, retinal cultures were used to examine
the effects of transferrin on neuronal physiology.
MATERIALS AND METHODS
Purified neuronal cultures
The preparation and characterization of purified retinal neurons
from chick embryo has previously been described 1"22'33. Briefly,
neural retinas from 8-day chick embryos were dissected free from
other ocular tissue, incubated for 10 min in Ca2+-Mg2+-free Hank's
balanced salt solution (CMF) and further incubated for 20 min in
0.25% trypsin (1:250 Nutritional Biochemical, Cleveland, OH) in
CMF. Cells were mechanically dissociated and suspended in 2 ml
of modified Eagle's basal medium (Gibco, Grand Island, NY) sup-
plemented with eatalase (5.6 U/ml) and insulin (8.3 x 10-TM). All
media supplements were purchased from Sigma Chemical Corp.
Cells were seeded (982 cell/mm 2) on 15-mm coverslips coated with
0.1% polyornithine in 60-mm tissue culture dishes. All cultures
were incubated at 37 °C in a humidified atmosphere of 5% CO2 in
air.
* Current address: Department of Physiology, Northwestern University Medical School, 303 E. Chicago Ave., Chicago, IL 60611, U.S.A.
** Current address: UMDNJ-Robert Wood Johnson Medical School, Department of Neurology, Piscataway, NJ 08855, U.S.A.
Correspondence: A.G. Hyndman, Department of Biological Sciences, Rutgers University, Piscataway, NJ 08855, U.S,A.