A Response Element for the Homeodomain Transcription Factor
Ptx3 in the Tyrosine Hydroxylase Gene Promoter
Pilar Cazorla, Marten P. Smidt, *Karen L. O’Malley, and J. Peter H. Burbach
Rudolf Magnus Institute for Neurosciences, Department of Medical Pharmacology, Medical Faculty, Utrecht University, Utrecht,
The Netherlands; and *Washington University School of Medicine, St. Louis, Missouri, U.S.A.
Abstract: Tyrosine hydroxylase (TH) is the rate-limiting
enzyme in the biosynthesis of catecholamines, which
takes place in different types of neuronal systems and
nonneuronal tissues. The transcriptional regulation of the
TH gene, which is complex and highly variable among
different tissues, reflects this heterogeneity. We recently
isolated a homeodomain transcription factor, named
Ptx3, that is uniquely expressed in the dopaminergic
neurons of the substantia nigra pars compacta and ven-
tral tegmental area, which together form the mesence-
phalic dopaminergic system. This strict localization and
its coinciding induction of expression with the TH gene
during development suggested a possible role for this
transcription factor in the control of the TH gene. We
report here the presence of a responsive element for Ptx3
located at position -50 to -45 of the rat TH promoter.
Transient transfections using TH promoter constructs
and electrophoretic mobility shift assays using Ptx3-con-
taining nuclear extracts demonstrated that this region
binds Ptx3 protein and confers a transcriptional effect on
the TH gene. Depending on the cell type, the effect of
Ptx3 was an eight- to 12-fold enhancement of TH pro-
moter activity in Neuro2A neuroblastoma cells, or a 60 –
80% repression in nonneuronal human embryonic kidney
293 cells. Despite the close association of the Ptx3-
binding site and the major cyclic AMP-response element
in the TH gene, no interplay was found between Ptx3 and
cyclic AMP-modulating agents. In combination with the
orphan nuclear receptor Nurr1, which is required for the
induction of the TH gene in mesencephalic dopaminergic
neurons, the TH promoter activity to Ptx3 was enhanced
in Neuro2A cells. Nurr1 alone displayed only very weak
activity on the TH promoter in this cell type. The results
demonstrate that the homeodomain protein Ptx3 has the
potential to act on the promoter of the TH gene in a
markedly cell type-dependent fashion. This suggests that
Ptx3 contributes to the regulation of TH expression in
mesencephalic dopaminergic neurons. Key Words: Ty-
rosine hydroxylase —Ptx3—Mesencephalic dopaminer-
gic neurons—Tissue specificity—Bicoid-type binding
element.
J. Neurochem. 74, 1829 –1837 (2000).
Tyrosine hydroxylase (TH; EC 1.14.16.2) is the first
and rate-limiting enzyme in the synthesis pathway of the
catecholamines. Due to this role, TH expression is crit-
ically modulated by multiple regulatory mechanisms (for
review, see Kumer and Vrana, 1996). In the brain, TH is
expressed in several cell groups, including the dopami-
nergic neurons of the substantia nigra, ventral tegmental
area, hypothalamus, and olfactory bulb, the noradrener-
gic neurons of the locus coeruleus and lateral tegmental
system, and the adrenergic neurons of the brainstem. In
the periphery, TH is expressed in sympathetic ganglia
and adrenal chromaffin cells. Given this wide distribu-
tion, it is clear that different transcriptional regulatory
mechanisms may account for regulated expression of the
TH gene in different cell populations. Some positive and
negative cis-regulatory elements have been identified in
the control of cell type-specific expression within the TH
gene (Yang et al., 1998a), but their sequence and posi-
tion are not always conserved across species (Gandelman
et al., 1990).
The 5'-flanking region of the TH gene has been
studied in great detail by using in vitro and in vivo
techniques. There are several binding sites for ubiq-
uitous transcription factors in the proximal TH pro-
moter. These include binding sites for activating pro-
tein-1 (AP1) (Angel et al., 1987), SP1 (Jones et al.,
1986), and activating protein-2 (AP2) (Imagawa et al.,
1987), two cyclic AMP-response elements (CRE)
(Comb et al., 1986; Best et al., 1995), the Oct/HEPT
motif (Dawson et al., 1994), and an E box/dyad ele-
ment (Yoon and Chikaraishi, 1992). However, their
relative contribution to the transcriptional activity var-
ies among cell types (Wong et al., 1994) and may be
differentially used in different developmental stages
Received October 11, 1999; revised manuscript received December
27, 1999; accepted January 2, 2000.
Address correspondence and reprint requests to Dr. J. P. H.
Burbach at Rudolf Magnus Institute for Neurosciences, Department
of Medical Pharmacology, Medical Faculty, Utrecht University,
Universiteitsweg 100, 3584 CG Utrecht, The Netherlands. E-mail:
J.P.H.Burbach@med.uu.nl
Abbreviations used: AP1, activating protein-1; AP2, activating pro-
tein-2; BBE, bicoid-type binding element; CRE, cyclic AMP-response
element; DTT, dithiothreitol; E, embryonic day; EMSA, electro-
phoretic mobility shift assay; HEK 293, human embryonic kidney 293;
mesDA, mesencephalic dopaminergic; TH, tyrosine hydroxylase.
1829
Journal of Neurochemistry
Lippincott Williams & Wilkins, Inc., Philadelphia
© 2000 International Society for Neurochemistry