Cre Recombinase Expression in the Floorplate, Notochord
and Gut Epithelium in Transgenic Embryos Driven by the
Hoxa-1 Enhancer III
Xue Li and Thomas Lufkin*
Brookdale Center for Developmental and Molecular Biology, Mount Sinai School of Medicine, New York, New York
Received October 1999; Accepted 5 October 1999
The Hoxa-1 homeobox gene functions as a director of
CNS patterning beginning at the neural plate stage of
embryogenesis, and in the absence of Hoxa-1 activity,
several hindbrain rhombomeres fail to undergo normal
development (Carpenter et al., 1993; Lufkin et al., 1991;
Mark et al., 1993). The Hoxa-1 gene has three well-
characterized enhancers (I-III), which together are nec-
essary for recapitulating the full expression pattern of
Hoxa-1 in transgenic embryos (Frasch et al., 1995).
Individually each of the enhancers gives a defined subset
of the Hoxa-1 expression domain. The 0.5 kb Hoxa-1
Enhancer III is located 3' to the Hoxa-1 polyadenylation
site and contains a functional retinoic acid regulatory
element (RARE), which is necessary for its activity and
for driving expression of the Hoxa-1 locus in neuroepi-
thelium (Frasch et al., 1995, Fig 1.). The activity of
Enhancer III has been examined in over 14 expressing
stable transgenic lines and 12 expressing transient F0
embryos. Ten of the 14 stable lines and 10 of the 12
transient F0 embryos gave an identical pattern of trans-
gene expression (Frasch et al., 1995; Xue Li, 1998)
showing activity in the floorplate, notochord, and gut
epithelium beginning at E8.5 and continuing strongly
through E12.5, followed by a decrease to background
levels by E14.5 (Fig. 2).
The Enhancer III-Cre (EIII-Cre) construct (Fig. 1) has the
Hoxa-1 Enhancer III driving transcription from a basal
TATA box promoter (Frasch et al., 1995). The dicistronic
mRNA has the Cre recombinase ORF (Sauer, 1987) at the 5'
end, followed by the human placental alkaline phosphatase
(AP) ORF (Cepko et al., 1993), which is linked to an IRES
sequence to allow cap-independent translation initiation as
previously described (Kim et al., 1992; Li et al., 1997). The
sequence surrounding the ATG start codon of the Cre ORF
was modified by site-directed mutagenesis (Deng and Nick-
oloff, 1992) to more closely resemble a consensus Kozak
sequence (Kozak, 1991). The transgene mRNA is pro-
cessed at the 3' end by an SV40 polyadenylation signal
(Frasch et al., 1995). Five EnIII-Cre transgenic founder lines
were generated. Four of the EnIII-Cre transgenics lines
(Lines 1, 4 – 6) gave the predicted restriction fragment
banding pattern when digested with BamHI and probed
with the Cre and AP ORF fragments (Fig. 2). Lines 1, 4, and
5 expressed Cre and AP, and lines 1 and 5 displayed an
identical pattern of Cre and AP expression, which was
characteristic for the Hoxa-1 Enhancer III (Fig. 1).
ACKNOWLEDGMENTS
We would like to thank Heidi Stuhlmann for providing
the Alkaline Phosphatase cDNA, Brian Sauer for the Cre
recombinase cDNA, and Hee-Sup Shin for the IRES se-
quence.
LITERATURE CITED
Carpenter EM, Goddard JM, Chisaka O, Manley NR, Capecchi MR.
1993. Loss of Hox-A1 (Hox-1.6) function results in the reorgani-
zation of the murine hindbrain. Development 118:1063–1075.
Cepko CL, Ryder EF, Austin CP, Walsh C, Fekete DM. 1993. Lineage
analysis using retrovirus vectors. Meth Enzymol 225:933–960.
Deng WP, Nickoloff JA. 1992. Site-directed mutagenesis of virtually any
plasmid by eliminating a unique site. Anal Biochem 200:81– 88.
Frasch M, Chen X, Lufkin T. 1995. Evolutionary-conserved enhancers
direct region-specific expression of the murine Hoxa-1 and Hoxa-2
loci in both mice and Drosophila. Development 121:957–974.
Kim DG, Kang HM, Jang SK, Shin HS. 1992. Construction of a bifunctional
mRNA in the mouse by using the internal ribosomal entry site of the
encephalomyocarditis virus. Mol Cell Biol 12:3636 –3643.
Kozak M. 1991. An analysis of vertebrate mRNA sequences: Intimations
of translational control. J Cell Biol 115:887–903.
Li X, Wang W, Lufkin T. 1997. Dicistronic lacZ and alkaline phosphatase
reporter constructs permit simultaneous histological analysis of ex-
pression from multiple transgenes. BioTechniques 23:874 – 882.
Li X. 1998. A Cre/loxP binary genetic approach to study murine spinal
cord and limb development. PhD Thesis, Mt. Sinai School of
Medicine, New York, NY.
Lufkin T, Dierich A, LeMeur M, Mark M, Chambon P. 1991. Disruption of
the Hox-1.6 homeobox gene results in defects in a region corre-
sponding to its rostral domain of expression. Cell 66:1105–1119.
Lufkin T, Mark M, Hart CP, LeMeur M, Chambon P. 1992. Homeotic
transformation of the occipital bones of the skull by ectopic
expression of a homeobox gene. Nature 359:835– 841.
Mark M, Lufkin T, Vonesch J, Ruberte E, Olivo J, Dolle ´ P, Gorry P,
Lumsden A, Chambon P. 1993. Two rhombomeres are altered in
Hoxa-1 mutant mice. Development 119:319 –338.
Sauer B. 1987. Functional expression of the cre-lox site-specific recom-
bination system in the yeast Saccharomyces cerevisiae. Mol Cell
Biol 7:2087–2096.
* Correspondence to: Thomas Lufkin, Brookdale Center for Developmen-
tal and Molecular Biology, Mount Sinai School of Medicine, Box 1020, One
Gustave L. Levy Place, New York, NY 10029-6574.
E-mail: lufkit01@doc.mssm.edu
© 2000 Wiley-Liss, Inc. genesis 26:121–122 (2000)