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Biological

Sex-related Differences in Gene Expression in Salivary Glands of BALB/c Mice

N.S. Treister1,2,*, S.M. Richards2,3, M.J. Lombardi4, P. Rowley4, R.V. Jensen4,5 and D.A. Sullivan2,3

1 Department of Oral Medicine, Infection, and Immunity, Harvard School of Dental Medicine, Boston, MA, USA;
2 Schepens Eye Research Institute, 20 Staniford Street, Boston, MA 02114, USA;
3 Department of Ophthalmology, Harvard Medical School, Boston, MA, USA;
4 Center for Neurologic Diseases, Brigham and Women’s Hospital and Harvard Medical School, Cambridge, MA, USA; and
5 Department of Physics, Wesleyan University, Middletown, CT, USA;

Correspondence: * corresponding author, ntreister{at}partners.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 
Sex-related differences exist in the structure and function of the major glands in a variety of species. Moreover, many of these variations appear to be unique to each tissue. We hypothesized that this sexual dimorphism is due, at least in part, to gland-specific differences in gene expression between males and females. Glands were collected from male and female BALB/c mice (n = 5/sex/experiment), and total RNA was isolated. Samples were analyzed for differentially expressed mRNAs with CodeLink microarrays, and data were evaluated by GeneSifter. Our results demonstrate that significant (P < 0.05) sex-related differences exist in the expression of numerous genes in the major salivary glands, and many of these differences were tissue-specific. These findings support our hypothesis that sex-related differences in the salivary glands are due, at least in part, to tissue-specific variations in gene expression.

Key Words: salivary glands • microarrays • gene expression • sex differences


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS & METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 
Many significant sex-related differences have been identified in the structure and function of the submandibular (SMG), sublingual (SLG), and parotid (PG) glands in a variety of species (Denny et al., 1993; Pinkstaff, 1998). These differences include variations in the ratio of granular convoluted tubules to acini, total protein concentration, glucose oxidation, and amylase activity (Floridi and Lindsay, 1971; Mudd and White, 1975). Moreover, the nature and extent of many of these disparities-including protein expression levels, concentrations of neurotransmitters and estrogen receptors, and the effects of stress on gland morphology-appear to be tissue-specific (Campbell et al., 1990; Murai et al., 1998; Pellegrini et al., 1998; Pinkstaff, 1998).

These differences may have a significant impact on salivary gland and oral diseases. Sex-related differences have been linked to discrepancies in the prevalence and severity of many diseases, including autoimmune diseases (Slavkin, 1998; Whitacre, 2001). Sjögren’s syndrome (SS), an autoimmune disease characterized by salivary gland lymphocytic infiltration, hypofunction, and risk of malignancy, affects women at a rate of 9:1 compared with men (Brennan and Fox, 1999; Parke, 2000). It is quite possible that sex-related variations in the salivary gland microenvironment may explain this disparity.

We hypothesized that major salivary gland sexual dimorphism is due, at least in part, to gland-specific differences in gene expression between males and females.


   MATERIALS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 
Animals
Male and female age-matched BALB/c mice were purchased from Taconic Laboratories (Germantown, NY, USA) and maintained in constant-temperature rooms with fixed light/dark periods of 12 hrs’ duration. At age 9 wks, the mice were killed in a CO2 chamber, and the submandibular, sublingual, and parotid glands were removed, cleared of adherent debris, and pooled (5 mice/sex/experiment, 10 pooled glands/experiment). Tissues were immediately frozen in liquid nitrogen and stored until RNA isolation. All animal study protocols were approved by the Institutional Animal Care and Use Committee of the Schepens Eye Research Institute, thus ensuring that humane practices would be followed.

Molecular Biological Procedures
RNA isolation
Frozen glands were pulverized by means of a mortar and pestle. RNA was isolated with the use of TRIzol reagent (Invitrogen, Carlsbad, CA, USA), and the concentration of RNA was measured by UV photospectrometry at 260 nm and 280 nm. RNA was further purified with RNAqueous columns (Ambion, Austin, TX, USA), and each sample was run on an RNA 6000 Nano LabChip on the Agilent 2100 Bioanalyzer (Agilent Technologies, Palo Alto, CA, USA) to ensure RNA integrity. RNA samples were then stored at –80°C until use for either microarray hybridization or real-time PCR experiments.

Microarray hybridization and image processing
RNA samples were processed for microarray hybridization as previously described (Redmond et al., 2003). In brief, the CodeLink Expression Assay Reagent Kit (Amersham, Piscataway, NJ, USA) was used for cDNA synthesis of total RNA (2 µg). The double-stranded cDNA was purified with the use of a QIAquick purification kit (Qiagen, Valencia, CA, USA). After drying, cRNA was synthesized with use of the CodeLink Expression Assay Reagent Kit, and the target product was recovered with the use of an RNeasy kit (Qiagen) and quantified with a UV photospectrometer.

Target cRNA (10 µg) was fragmented with fragmentation buffer and added to the hybridization solution. For array hybridization, a 250-µL quantity of denatured target solution was injected into each hybridization chamber of a CodeLink Mouse Uniset I microarray (Amersham, Piscataway, NJ, USA), which contains approximately 10,000 mouse oligonucleotide gene probes. For the male and female submandibular glands, triplicate samples (e.g., experiments, 5 different mice/experiment) were hybridized, and for the male and female sublingual and parotid glands, duplicate samples were hybridized. The slides were incubated at 37°C for 18 hrs with shaking, followed by several washes in TNT buffer and signal detection with streptavidin-Alexa 647. Arrays were scanned with the use of ScanArray Express software and a ScanArray Express HT scanner (Packard BioScience, Meriden, CT, USA) with the laser set at 635 nm, laser power at 100%, and photomultiplier tube voltage at 60%. Scanned image files were analyzed with the use of CodeLink image and data analysis software, which produced both raw and normalized hybridization signal intensities for each spot on the arrays. Normalized signal intensities were used in this study.

Real-time PCR
We used real-time PCR (RT-PCR) to verify the differential expression of selected genes (online APPENDIX). The cDNA was transcribed from DNase-treated mRNA (5 µg) by SuperScript II Reverse Transcriptase (Invitrogen, Carlsbad, CA, USA) and oligo dT priming (Promega, Madison, WI, SUA). We designed forward and reverse primers using Primer Express Software, version 1.5 (Applied Biosystems, Inc., Foster City, CA, USA) (Appendix TableGo). RT-PCR reactions (50 µL) were performed with the primers at optimal concentrations, target cDNA, SYBR Green PCR Master Mix (Applied Biosystems), MicroAmp Optical 96-Well Reaction Plates (Applied Biosystems), ABI PRISM Optical Adhesive Covers (Applied Biosystems), and the GeneAmp 7900 HT Sequence Detection System (Applied Biosystems), according to the manufacturer’s protocol. Expression levels were standardized to glyceraldehyde-3-phosphate dehydrogenase, and calculations were based on both the Comparative Ct and the Relative Standard Curve methods of relative quantitation of gene expression (Applied Biosystems). Dissociation curves were checked to ensure the absence of secondary PCR products.


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  		Table. Genes Confirmed by Real-time PCR
 
Microarray Data Analysis and Statistics
We analyzed normalized data from the CodeLink software package using GeneSifter (VizX Labs LLC, Seattle, WA, USA; http://www.genesifter.net). We determined differential expression of genes by averaging the triplicate samples and running a pair-wise analysis. Statistical significance was determined by Student’s t test (two-tailed, unpaired), and data were filtered for spot quality (> 0.75). Only genes that passed the quality filtering, and with p values < 0.05, were included in the analysis. Gene ontology reports and z scores (Biological Process, Cellular Component, and Molecular Function) were also generated with GeneSifter.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
DISCUSSION
 APPENDIX
 REFERENCES
 
To study the sex-related differential expression of genes in major salivary glands, we collected submandibular, sublingual, and parotid glands from male and female mice and processed them for analysis by using CodeLink Mouse Uniset I microarrays and GeneSifter analytical software.

Our results demonstrate that significant (p < 0.05) sex-related differences exist in the expression of genes in all 3 major salivary glands (Table 1Go). There were over 700 genes differentially expressed between males and females in the submandibular gland, over 150 genes in the sublingual gland, and over 100 genes in the parotid gland. Several of these genes were expressed at more than a two-fold level, and additional genes were expressed at greater than a 10-fold level. The data from the individual arrays (n = 14) are accessible for download through the National Center for Biotechnology Information’s Gene Expression Omnibus (http://www.ncbi.nlm.nih.gov/geo) via series accession number GSE1503. These data are also available for statistical evaluation through GeneSifter (http://genesifter.net/datacenter/treister2004).


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  		Table 1. Differential Expression of Genes in the Major Salivary Glands
 
The nature of these sex-related variations in gene expression was typically unique to each tissue. For example, transforming growth factor β2 mRNA levels were increased over four-fold in the male submandibular gland, nearly two-fold in the male sublingual gland, and were not differentially expressed in the parotid gland. Hydroxysteroid (17β) dehydrogenase 3 (17β-HSD3) mRNA amounts were significantly elevated in the male submandibular gland, but were not differentially expressed in the sublingual or parotid glands. The gene for interleukin 3 was up-regulated only in the female sublingual gland, and the gene for interleukin 1 receptor type II was up-regulated only in the male parotid gland (data not shown).

Of particular interest, the differentially expressed genes in the submandibular, sublingual, and parotid glands appear to be involved in a diverse array of biological processes, molecular functions, and cellular components (Table 2Go). Sex influenced genes associated with growth, metabolism, transport, signal transduction, enzyme activity, and the regulation of transcription in the submandibular gland. Similarly, sex-related and tissue-specific differences were found in the gene ontologies of the sublingual and parotid glands.


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  		Table 2. Z Scoresa for Selected Gene Ontologies in the Male and Female Submandibular Gland
 
For partial verification of the microarray results, 10 genes were selected for RT-PCR evaluation (Table 3Go). The genes were chosen to highlight differential expression that was both sex- and tissue-specific. Genes up-regulated primarily in males included epidermal growth factor (EGF), 17β-HSD3, nerve growth factor β (NGF β), prostaglandin D2 synthase, sulfotransferase, transforming growth factor β2 (TGF β2), and vascular endothelial growth factor A (VEGFA). Genes up-regulated primarily in females included pancreatic lipase-related protein 1 (PLRP1) and sialyltransferase 4a. The RT-PCR results confirmed the microarray data (Table 4Go). In addition, despite the differences between RT-PCR and microarray technologies, the magnitude of differential gene expression was similar with both approaches.


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  		Table 3. Intensitiesa of Selected Genes from the CodeLink Microarrays
 

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  		Table 4. Comparison of CodeLink and Real-time PCR (RT-PCR) Results for Selected Genes
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
APPENDIX
 REFERENCES
 
The present study demonstrates that numerous, sex-related differences in gene expression exist in the major salivary glands of male and female mice. There were hundreds of genes differentially expressed in the submandibular gland, fewer in the sublingual gland, and even fewer in the parotid gland, indicating significant gland-specific variations as well. Many more genes were up-regulated in tissues of males compared with females. These observations support our hypothesis that major salivary gland sexual dimorphism is due, at least in part, to gland-specific differences in gene expression between males and females.

Our finding that sex-related differences in gene expression exist in and between salivary tissues is not unique. Sex-associated and tissue-specific variations in mRNA levels have previously been reported in salivary glands (Murphy et al., 1980; Gerald et al., 1986; Gubits et al., 1986; Senorale-Pose et al., 1998). However, our discovery of the extent and diversity of such sex- and gland-specific differences in gene expression within salivary tissues is unique. The fact that so many sex-associated differences exist, and in a tissue-specific manner, may relate not only to structural and functional differences among the major salivary glands, but also to their responsiveness to sex steroid hormones and other sex-related factors.

To verify the microarray results, we confirmed the expression of selected genes by RT-PCR. Gene selection criteria were based upon the pattern of differential expression, as well as on the potential insight into the understanding of sex-related differences in the major salivary glands. The selected genes fell into 3 major categories, including those associated with growth factors (i.e., EGF, NGF β, VEGF A, and TGF β2), sex steroidogenic enzymes (i.e., 17β-HSD3 and sulfotransferase, estrogen-preferring), and other enzymes (i.e., PLRP1, prostaglandin D2 synthase, and sialyltransferase 4a). The mRNA levels of EGF-a peptide with endocrine, autocrine, and paracrine activities that affects cell proliferation and differentiation (Sheflin et al., 1996a)-were increased in male glands. Highest amounts were found in the submandibular gland and the least in the parotid gland. Elevated content of EGF mRNA in male submandibular tissue has also been reported by others (Gubits et al., 1986), and is apparently associated with a dramatic sex difference in the pattern of polyadenylation (Sheflin et al., 1996b). The patterns of expression of NGF β and VEGFA mRNAs were analogous to that of EGF, with highest levels observed in the male submandibular gland. This differential expression of NGF β also extends to the translated form, which is the biologically active subunit of nerve growth factor. Thus, NGF β protein shows a striking sexual dimorphism in the submandibular gland, as well as the brain, adrenal gland, and spinal chord (Katoh-Semba et al., 1989). The biological relevance of NGF β, though, is unknown (Murphy et al., 1980). In contrast, VEGFA is one of the most potent angiogenic growth factors produced by many different cell types, and expression in salivary glands may contribute to the remarkable healing capacity of the oral mucosa and digestive tract (Taichman et al., 1998). The level of TFG β2 mRNA was highest in the male submandibular gland, elevated only slightly in the male sublingual gland, and similar in the male and female parotid glands. This factor is chemotactic for fibroblasts and inflammatory cells, and has potent immunosuppressive properties (Koski et al., 1997). Increased levels of TFG β2 have been linked to immune defects associated with malignancies and autoimmune disorders (Letterio and Roberts, 1998).

With regard to steroidogenic enzymes, the gene encoding 17β-HSD3 was up-regulated in the male submandibular gland, but was not differentially expressed in the sublingual or parotid glands. This enzyme plays a central role in the peripheral synthesis of all active estrogens and androgens (Martel et al., 1992). A related form of this enzyme, 17β-HSD, has previously been identified by immunohistochemistry in the ductal epithelium of male and female human submandibular and parotid glands; weak staining was also found in female glandular acini (Sirigu et al., 1982). Sulfotransferase (estrogen-preferring) mRNA content was increased in all 3 male glands. Sulfotransferase catalyzes the sulfoconjugation and inactivation of estrogen, has high substrate specificity, is androgen-dependent, and may act as a molecular switch in estrogen target tissues to regulate local estrogen activity and target tissue sensitivity (Song, 2001).

As concerns other enzymes, the gene for PLRP1 was up-regulated in the female submandibular gland and the male sublingual gland, but was not differentially expressed in the parotid gland. For comparison, an earlier investigation also found PLRP1 mRNA in the sublingual gland, but was unable to identify the associated sexual dimorphism or detect transcripts in either the submandibular or parotid tissue (Remington et al., 1999). Pancreatic lipase-related protein 1 belongs to a superfamily of enzymes that includes lipases, esterases, and thioesterases (Wong and Schotz, 2002). The mRNA levels for prostaglandin D2 synthase were increased in the male submandibular and sublingual, but not parotid, glands. This enzyme is involved in a variety of physiological responses, including allergic responses, inhibition of platelet aggregation, relaxation of vascular and non-vascular smooth muscle, and inflammation (Mong et al., 2003). Gene expression for sialyltransferase 4a was up-regulated in the female submandibular gland, with little change in the sublingual or parotid glands. Sialyltransferase 4a catalyzes the transfer of sialic acids (Jamieson et al., 1993), which may also influence hormone regulation, enzyme activity, hemostasis, synaptic transmission, and immune activity.

Ontological analyses showed that enormous, sex-related differences exist in the expression of salivary gland genes associated with fundamental biological processes, diverse molecular functions, and many cellular components. These differences may affect salivary gland pathophysiology, especially in cases where the sexes are affected unequally, such as in Sjögren’s syndrome (SS). Interestingly, several of the genes highlighted in this study have been associated with SS. Tissue levels of minor salivary gland EGF have been shown to be lower in SS patients compared with controls (Koski et al., 1997). In contrast, minor salivary gland amounts of TGF β2 have been demonstrated to be higher in SS patients (Koski et al., 1997). Also, there may be a dysregulation of sialyltransferases that could account for the oversialylation of IgA and other glycoproteins in SS (Basset et al., 2000).

Future studies are essential if the present findings are to be further confirmed and expanded. In addition, it is critical that we identify the salivary gland cells that harbor these sex-related differences in mRNA levels and determine whether these variations in gene activity are translated into corresponding changes in protein expression.

In conclusion, through microarray technology, we found numerous sex-related and tissue-specific differences in gene expression in the submandibular, sublingual, and parotid glands in mice. These findings may explain, in part, the striking sex-associated variations known to exist in the microenvironments of salivary glands.


   APPENDIX
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 APPENDIX
REFERENCES
 


   ACKNOWLEDGMENTS
 
We thank Drs. Christian Wade and Eric Olsen and the personnel at GeneSifter for their assistance with analysis and technical support. This research was supported by NIH grants EY05612 and K16. An abstract of this study was presented at the 2004 IADR/AADR annual meeting in Honolulu, HI, March 10–13, 2004.


   FOOTNOTES
 
A supplemental appendix to this article is published electronically only at http://www.dentalresearch.org.

Received for publication April 6, 2004. Revision received November 1, 2004. Accepted for publication November 3, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 

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Journal of Dental Research, Vol. 84, No. 2, 160-165 (2005)
DOI: 10.1177/154405910508400210
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