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Endocrinology Vol. 143, No. 6 2080-2084
Copyright © 2002 by The Endocrine Society

RECEPTORS

Identification of a Novel First Exon of Prolactin Receptor Gene Expressed in the Rat Brain

Minoru Tanaka, Yukinobu Hayashida, Tadashi Iguchi, Nobuhiro Nakao, Maiko Suzuki, Naoya Nakai and Kunio Nakashima

Department of Biochemistry, Faculty of Medicine (M.T., T.I., N.N., M.S., N.N., K.N.), and Department of Animal Science, Faculty of Bioresources (Y.H.), Mie University, 2-174 Edobashi, Tsu, Mie 514-8507, Japan

Address all correspondence and requests for reprints to: Dr. Minoru Tanaka, Department of Biochemistry, Mie University Faculty of Medicine, 2-174 Edobashi, Tsu, Mie 514-8507, Japan.


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results and Discussion
 References
 
A novel first exon, E14, whose sequence was distinct from those of the three known first exons, E11, E12, and E13, of the rat PRL receptor (PRL-R) gene was identified by cDNA cloning for the 5'-end region of PRL-R mRNA expressed in the rat brain. Sequence analysis revealed the presence of two different length E14 cDNAs. The longer cDNA contained the 243-bp E14 sequence, and the shorter cDNA lacked the 139-bp sequence at the 5'-end of the longer one. Neither E14 cDNA has a second exon sequence, indicating that the E14 first exon is extensively spliced to the third exon. E14-containing PRL-R mRNAs were detected only in the brain by RT-PCR and ribonuclease protection assay. The longer E14 mRNA was expressed as the major PRL-R mRNA species in the brain and was greatly increased in pregnant (d 18) and lactating (d 5) rats. A genomic clone containing the E14 first exon together with its 5'- and 3'-flanking regions was isolated from a rat kidney genomic library. Ribonuclease protection assay revealed that the position corresponding to the 5'-end of the shorter E14 cDNA is the major transcription start point for the E14 exon. The 5'-flanking region of E14 contained a TATA box-like element 23 bp upstream of the major transcription start point. Other putative transcription factor-binding sites, such as CCAAT, Sp1, and glucocorticoid-responsive elements, were observed at further upstream regions. These results suggest that PRL-R gene expression in rat brain is controlled by the promoter for the E14 first exon.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results and Discussion
 References
 
PRL EXERTS many actions of the brain function (1, 2), including maternal behavior (3), sexual behavior (4), and stress tolerance (5). The actions of PRL are mediated by the PRL receptor (PRL-R), which belongs to the type 1 cytokine receptor superfamily (6). Mammalian PRL-R genes consisted of 11 exons (7, 8), and long and short forms of PRL-R, differing in length and sequence of their cytoplasmic domains, are generated by alternative splicing from a single transcript (9). In rodents, splicing of exon 9 to exon 10 results in generation of the long-form receptor mRNA, whereas splicing of exon 9 to multiple exon 11s generates mRNAs encoding short-form receptors containing distinct carboxyl-termini (10, 11, 12). Both the long- and short-form receptor mRNAs are distributed in a wide range of tissues, and PRL-R gene expression is regulated by complex mechanisms. Three distinct first exons, E11, E12, and E13, have been identified in the rat PRL gene (13). E11 and E12 are specifically expressed in gonadal tissues and liver, respectively, and E13 is expressed in various tissues. The distinct expression patterns of these three alternative first exons are controlled by promoters located at upstream regions of each first exon. The promoter for E11 contains a consensus element for steroidogenic factor I directing the gonad-specific expression of E11 exon (14). Hepatic nuclear factor 4 has been shown to be largely responsible for the liver-specific expression of E12 by acting on its binding site in the E12 promoter (15). C/EBPß and SP1 have been demonstrated to act on the E13 promoter, which accounts for the generic expression of E13 (16).

In the brain, PRL-R mRNA has been identified in different brain areas, with higher abundance in choroid plexus and hypothalamus (17, 18, 19, 20, 21, 22, 23), and PRL-R protein has also been mapped in the same brain areas (24, 25, 26, 27, 28, 29, 30). We have previously shown that the expression of long-form PRL-R mRNA, but not that of short-form mRNA, is remarkably increased in the rat brain at the midstage of pregnancy and remains at high levels during the following period of pregnancy and lactation (31, 32). These expression profiles of PRL-R mRNAs in the brain differ from those in the liver and mammary gland (33). In the liver, long-form PRL-R mRNA levels remain almost constant during pregnancy and lactation, and short-form PRL-R mRNA levels increase in the late stage of pregnancy, followed by a rapid decrease after parturition. In the mammary gland, the levels of both long- and short-form PRL-R mRNAs remain low during pregnancy and then increase in lactation. In the brain, the expression of long-form, but not short-form, PRL-R mRNA is induced by pup contact stimuli in male rats as well as in nulliparous female rats, with concomitant induction of maternal behavior (34). These findings suggest that PRL-R gene expression in the brain is regulated in a brain-specific manner associated with the induction of maternal behavior. In an effort to clarify the regulatory mechanisms of PRL-R gene expression in the brain, we have identified and characterized a brain-specific first exon of the rat PRL-R gene.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results and Discussion
 References
 
Animals
Adult male and female Sprague-Dawley rats (10 wk of age) were purchased from SLC (Sizuoka, Japan) and housed in a temperature-controlled room. Food and water were available ad libitum. Estrous cycles were examined by virginal smears. The day when spermatozoa were detected was designated d 1 of pregnancy. Animals were killed by decapitation. Brain (cerebrum), pituitary, liver, kidney, intestine, adrenal, and ovary were rapidly dissected and frozen in liquid nitrogen before extraction of RNA.

cDNA cloning for 5'-regions of PRL-R mRNAs from rat brain
Total RNA was extracted from the brain with an ISOGEN kit (Nippon Gene, Toyama, Japan), and poly(A)+ RNA was isolated with Oligotex-dT30 (Takara, Tokyo, Japan) according to the manufacturer’s instructions. The 5'-end of the PRL-R cDNA was cloned by the oligo-capping method (35), with slight modification. Briefly, poly(A)+ RNA was decapped with tobacco acid pyrophosphatase (Nippon Gene) and recapped with an oligonucleotide RNA linker (Nippon Gene). Then, the oligo-capped PRL-R mRNA was subjected to RT-PCR using an RNA linker-primer and an antisense primer deriving from positions 113–133 of the reported rat PRL-R cDNA sequence (12) (corresponding to positions 411–431 of the E14 cDNA sequence in Fig. 1Go). The synthesized cDNA was cloned into pGEM-T Easy vector (Promega Corp., Palo Alto, CA) and sequenced.



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  		Figure 1. The nucleotide sequence of the longer cDNA for E14 PRL-R mRNA obtained by the oligo-capping method. The region of the E14 first exon is underlined. The position of 5'-end of the shorter cDNA is shown by an arrowhead.

 
Ribonuclease (RNase) protection assay
Appropriate E14 cDNA and E14 genomic fragments were subcloned into pGEM-T Easy vector, and RNA probes were synthesized using T7 or SP6 RNA polymerases and [{alpha}-32P]CTP. The RNA probes were hybridized with total RNA or poly(A)+ RNA and were digested with RNase A and RNase T1. The protected fragments of the RNA probes were separated by electrophoresis on a 6% polyacrylamide-7 M urea gel and detected by autoradiography. The radioactivities of the protected fragments were analyzed using a BAS1000 imaging analyzer (Fuji Photo Film Co., Ltd., Tokyo, Japan).

RT-PCR analysis
Total RNA (10 µg) from rat tissues was reverse transcribed using an oligo-(deoxythymidine) primer and the resulting cDNA was subjected to 25 cycles of PCR (96 C for 1 min, 60 C for 1 min, and 72 C for 1 min) using a sense primer deriving from positions 153–177 of E14 PRL-R cDNA in Fig. 1Go and an antisense primer deriving from positions 341–364 of the reported rat PRL-R cDNA sequence (12) (corresponding to positions 639–662 of E14 cDNA). The PCR products were separated by electrophoresis on a 1.5% agarose gel and subjected to Southern blot analysis with a radiolabeled oligomer probe deriving from positions 299–328 of E14 PRL-R cDNA.

Cloning of E14 exon of rat PRL-R gene
A genomic fragment containing E14 was cloned from a {lambda}-DASH rat genomic library (Stratagene, Tokyo, Japan) by screening with the E14 cDNA probe. The cloned phage DNA was digested with appropriate restriction enzymes, subcloned into pBluescript II SK- vector (Stratagene), and sequenced.

Statistical analysis
The data were analyzed for statistical significance using the Macintosh Super ANOVA program and were expressed as the mean ± SE. The significance of differences between the values was analyzed using Scheffé’s post-hoc test.


   Results and Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
References
 
Identification of a novel first exon by cloning the 5'-ends for PRL-R cDNAs from rat brain
The rat PRL-R gene has been shown to contain at least three first exons that encode 5'-untranslated regions of PRL-R mRNAs (13). To determine the first exon expressed in the brain, cDNAs for the 5'-end regions of PRL-R mRNAs were cloned from the brain by the oligo-capping method. Two longer and six shorter cDNAs were identified from the eight independent cDNA clones obtained. The longer cDNAs contained an exon 1-derived sequence of 243 bp at their 5'-end, and the shorter cDNAs lacked the 136-bp sequence at the 5'-end of the longer cDNA (Fig. 1Go). The 243-bp sequence differed from those of the known three exons 1 (E11, E12, and E13); therefore, the novel first exon was referred to as E14. None of the E14 PRL-R cDNA clones contained an exon 2 sequence.

Tissue distribution of E14 PRL-R mRNA
Tissue distribution of E14 PRL-R mRNA was examined by RNase protection assay with a RNA probe synthesized from a common region (positions 153–364 in Fig. 1Go) of the longer and shorter E14 cDNAs (Fig. 2AGo). A 212-base fragment corresponding to the longer and shorter E14 PRL-R mRNAs was detected only in the brain as a weak signal. On the other hand, a 121-base fragment corresponding to other PRL-R mRNAs was detected with strong signals in the liver, adrenal, and ovary while weakly in the kidney, intestine, and pituitary. These results indicated that E14 PRL-R mRNAs are expressed only in the brain among the tissues examined. The tissue specificity of expression for E14 PRL-R mRNAs was confirmed by the RT-PCR analysis (Fig. 2BGo). The amplified E14 PRL-R cDNA contained no exon 2 sequence as observed in the oligo-capping cDNAs, indicating that E14 is spliced to exon 3 after transcription in the brain. Such an exon 2-lacking mRNA species has also been identified in E11 PRLR mRNAs in the liver (13).



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  		Figure 2. Tissue distributions of PRL-R mRNAs containing E14 and other first exons. A, RNase protection assay of E14 and other PRL-R mRNAs in the tissues of a 12-wk-old female rat in the diestrous stage. The positions of protected fragments for E14 and other PRL-R mRNAs are indicated under the autoradiogram. MspI digests of pUC19 plasmid DNA were used as the size markers. B, RT-PCR analysis of E14 PRL-R mRNA. Arrowheads and a square indicate the positions of PCR primers and hybridization probe, respectively. The positions of size markers are shown at the left margin of the autoradiogram.

 
Expression profiles of E14 PRL-R mRNAs in the brain at various reproductive stages
The expression levels of E14 PRL-R mRNA in the brain of male, diestrous female, pregnant (18 d), and lactating (5 d) rats were examined by RNase protection assay with a RNA probe synthesized from the longer E14 PRL-R cDNA (positions 1–431 in Fig. 1Go). As shown in Fig. 3Go, the shorter E14 PRL-R mRNA was detected as a 292-base protected fragment in the brain at all the reproductive stages. The expression level of the shorter E14 PRL-R mRNA in males was comparable to that in diestrous females, and the levels at the pregnant and lactating stages were about 4-fold higher than that at the diestrous stage. On the other hand, the longer E14 PRL-R mRNA (431-base fragment) was undetectable in the brain at all the reproductive stages. PRL-R mRNAs containing other exon 1 sequences were faintly detected as a 188-base fragment in the brain at all the reproductive stages and were clearly detected in the liver at the diestrous stage. We have previously demonstrated that expression of long-form, but not short-form, PRL-R mRNA in rat brain was increased during pregnancy and lactation (31). Our current observations suggest that the induction of long-form mRNA expression during pregnant and lactating periods is due to activation of transcription of E14 first exon generating the shorter E14 PRL-R mRNA.



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  		Figure 3. Expression levels of E14 PRL-R mRNAs in the brain at different reproductive stages. A, A typical autoradiogram of RNase protection assay for PRL-R mRNAs in the brain and liver from 12-wk-old male (M), 12-wk-old diestrous female (F), d 18 pregnant (P), and d 5 lactating (L) rats. The RNA probe was synthesized from the longer E14 PRL-R cDNA. The diagram of protected fragments for the longer and shorter E14 PRL-R mRNAs and other PRL-R mRNAs are indicated at the right of the autoradiogram. B, The radioactivities of the 292-base protected fragments for the shorter E14 PRL-R mRNA were measured with a BAS1000 imaging analyzer and expressed as relative values to the value for diestrous female rats. Bars represent the mean ± SE of four different rats at each reproductive stage. The radioactivities of other protected fragments in the brain were not measurable. *, P < 0.01 (compared with the values of diestrous female rats).

 
Characterization of genomic sequence of E14 first exon and its 5'-flanking region
A 17-kb genomic fragment containing the 243-bp E14 first exon, the 15-kb 5'-flanking area, and the 2-kb 3'-flanking region was cloned by screening a rat kidney genomic library with an E14 PRL-R cDNA probe. The nucleotide sequences of E14 and its proximal 5'-flanking region are shown in Fig. 4Go. As the whole sequence of the 17-kb genomic fragment was not overlapping with the reported genomic sequences of E11, E12, and E13 first exons, the position of E14 first exon in relation to three other first exons is still unclear. The 3'-end of E14 was followed by the consensus sequence of the splicing donor site, gt. Based on the sequences and frequencies of the longer and shorter oligo-capping E14 PRL-R cDNAs, the positions +140 (tsp 1) and +1 (tsp 2) in Fig. 4Go are considered to be the major and minor transcription start points, respectively. Transcription start points of E14 in the brain were further analyzed by RNase protection assay with an RNA probe deriving from a genomic fragment (positions -50 to +243 in Fig. 4Go). A protected fragment corresponding to tsp 1 was detected clearly at the position about 100 bases from the brain of the lactating rat and weakly from the brain of the diestrous rat, but no protected fragment corresponding to tsp 2 was detected (Fig. 5Go). These results confirmed that the E1 exon is extensively transcribed from tsp 1 in the brain.



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  		Figure 4. Nucleotide sequence of rat E14 and its 5'-flanking region. The sequence of E14 is shown in uppercase letters. Closed and open arrowheads indicate the major and minor transcription start points, tsp1 and tsp2, respectively. A TATA box-like element is underlined, and putative binding sites for other transcription factors are shown by arrows.

 


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  		Figure 5. Analysis of transcription start points of E14 first exon in the brain by RNase protection assay. Twenty micrograms of poly(A)+ RNA prepared from the brain of 12-wk-old diestrous female (F) and d 5 lactating (L) rats were subjected to RNase protection assay. The RNA probe synthesized from the genomic region is indicated under the autoradiogram.

 
In the 5'-flanking region of E14, a TATA box-like element was found 23 bp upstream of tsp 1, and an SP1 element and two CCAAT elements were observed at a region further upstream. In addition, two putative glucocorticoid-responsive elements were found at -511 and -386. It has been shown that glucocorticoid secretion increases during lactation (36) and that its receptor is distributed in various brain areas, including hypothalamus and choroid plexus (37), where PRL-R is abundantly expressed. These observations suggest that glucocorticoid might be a factor responsible for the enhanced expression of E14 PRL-R mRNA during lactation. Serum concentrations of progesterone and estrogen are known to increase during mid and late stages of pregnancy, respectively. Serum levels of PRL and GH are also elevated at late stage of pregnancy, and the high PRL level continues during lactation. We have previously shown that administration of progesterone, estrogen, PRL, and GH to ovariectomized and/or hypophysectomized rats induces the expression of the long-form PRL-R mRNA in the brain (31). The effects of these hormones on the expression of PRL-R mRNA might also be due to activation of the promoter for the E14 first exon.

In conclusion, the identification of a novel first exon of PRL-R gene preferentially expressed in pregnancy and lactation stages in the rat brain will facilitate understanding of molecular mechanisms for PRL functions in the brain, including the induction of maternal behavior.


   Acknowledgments
 


   Footnotes
 
This work was supported in part by Grants-in-Aid for Scientific Research 13670136 from the Ministry of Education, Science, Sports, and Culture of Japan.

Abbreviations: PRL-R, PRL receptor; RNase, ribonuclease.

Received December 3, 2001.

Accepted for publication February 4, 2002.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
 References
 

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