Gene expression in the mammary gland of the tammar wallaby during the lactation cycle reveals conserved mechanisms regulating mammalian lactation
C. J. Vander Jagt A B D , J. C. Whitley B , B. G. Cocks B C and M. E. Goddard A B
+ Author Affiliations
- Author Affiliations
A Department of Agriculture and Food Systems, Melbourne School of Land and Environment, The University of Melbourne, Parkville, Vic. 3010, Australia.
B Computational Biology, Department of Environment and Primary Industries, AgriBio, Centre for AgriBioscience, 5 Ring Road, Bundoora, Vic. 3083, Australia.
C School of Applied Systems Biology, La Trobe University, Bundoora, Vic. 3083, Australia.
D Corresponding author. Email: christy.vanderjagt@depi.vic.gov.au
Reproduction, Fertility and Development 28(9) 1241-1257 https://doi.org/10.1071/RD14210
Submitted: 16 June 2014 Accepted: 21 December 2014 Published: 23 February 2015
Abstract
The tammar wallaby (Macropus eugenii), an Australian marsupial, has evolved a different lactation strategy compared with eutherian mammals, making it a valuable comparative model for lactation studies. The tammar mammary gland was investigated for changes in gene expression during key stages of the lactation cycle using microarrays. Differentially regulated genes were identified, annotated and subsequent gene ontologies, pathways and molecular networks analysed. Major milk-protein gene expression changes during lactation were in accord with changes in milk-protein secretion. However, other gene expression changes included changes in genes affecting mRNA stability, hormone and cytokine signalling and genes for transport and metabolism of amino acids and lipids. Some genes with large changes in expression have poorly known roles in lactation. For instance, SIM2 was upregulated at lactation initiation and may inhibit proliferation and involution of mammary epithelial cells, while FUT8 was upregulated in Phase 3 of lactation and may support the large increase in milk volume that occurs at this point in the lactation cycle. This pattern of regulation has not previously been reported and suggests that these genes may play a crucial regulatory role in marsupial milk production and are likely to play a related role in other mammals.
Additional keywords: DAVID, EST, gene ontology, IPA, microarray, milk, network.
References
Akers, M. R. (2002). ‘Lactation and the Mammary Gland’. (Iowa State Press: Ames, Iowa.)Anderson, S. M., Rudolph, M. C., Mcmanaman, J. L., and Neville, M. C. (2007). Key stages in mammary gland development. Secretory activation in the mammary gland: it’s not just about milk-protein synthesis! Breast Cancer Res. 9, 204.
| Key stages in mammary gland development. Secretory activation in the mammary gland: it’s not just about milk-protein synthesis!Crossref | GoogleScholarGoogle Scholar | 17338830PubMed |
Bininda-Emonds, O. R. P., Cardillo, M., Jones, K. E., Macphee, R. D. E., Beck, R. M. D., Grenyer, R., Price, S. A., Vos, R. A., Gittleman, J. L., and Purvis, A. (2007). The delayed rise of present-day mammals. Nature 446, 507–512.
| The delayed rise of present-day mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsV2itb0%3D&md5=8d771c0acd233cc516bf3ff11e68f17fCAS |
Börchers, T., Hohoff, C., Buhlmann, C., and Spener, F. (1997). Heart-type fatty-acid-binding protein – involvement in growth inhibition and differentiation. Prostaglandins Leukot. Essent. Fatty Acids 57, 77–84.
| Heart-type fatty-acid-binding protein – involvement in growth inhibition and differentiation.Crossref | GoogleScholarGoogle Scholar | 9250612PubMed |
Campbell, S. M., Rosen, J. M., Hennighausen, L. G., Strech-Jurk, U., and Sippel, A. E. (1984). Comparison of the whey acidic protein gene of the rat and mouse. Nucleic Acids Res. 12, 8685–8697.
| Comparison of the whey acidic protein gene of the rat and mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXntlCnsw%3D%3D&md5=5ebf353f94291cee99d661610248a06dCAS | 6095207PubMed |
Choi, K. M., Barash, I., and Rhoads, R. E. (2004). Insulin and prolactin synergistically stimulate b-casein messenger ribonucleic acid translation by cytoplasmic polyadenylation. Mol. Endocrinol. 18, 1670–1686.
| Insulin and prolactin synergistically stimulate b-casein messenger ribonucleic acid translation by cytoplasmic polyadenylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXls1aktb0%3D&md5=ef39430b3cf2838d5d912f45648cd5e0CAS | 15071091PubMed |
Clarkson, R. W. E., Wayland, M. T., Lee, J., Freeman, T., and Watson, C. J. (2004). Gene expression profiling of mammary-gland development reveals putative roles for death receptors and immune mediators in post-lactational regression. Breast Cancer Res. 6, R92–R109.
| Gene expression profiling of mammary-gland development reveals putative roles for death receptors and immune mediators in post-lactational regression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptVyjsg%3D%3D&md5=7486b8e15564cc8bebeef119fded0949CAS |
Dahlhoff, M., Blutke, A., Wanke, R. D., Wolf, E., and Schneider, M. R. (2011). In vivo evidence for epidermal growth factor receptor (EGFR)-mediated release of prolactin from the pituitary gland. J. Biol. Chem. 286, 39 297–39 306.
| In vivo evidence for epidermal growth factor receptor (EGFR)-mediated release of prolactin from the pituitary gland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVSqtL7J&md5=fc593d90bd1b32f47e4989384448b1bfCAS |
Deane, E. M., and Cooper, D. W. (1988). Immunological development. In ‘The Developing Marsupial: Models for Biomedical Research’. (Eds C. H. Tyndale-Biscoe and P. A. Janssens.) pp. 190–199. (Springer: Berlin.)
Deane, E. M., Cooper, D. W., and Renfree, M. B. (1990). Immunoglobulin G levels in fetal and newborn tammar wallabies (Macropus eugenii). Reprod. Fertil. Dev. 2, 369–375.
| Immunoglobulin G levels in fetal and newborn tammar wallabies (Macropus eugenii).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlt1er&md5=3203d60fdcd4a6af585c509c0c48d990CAS | 2120744PubMed |
Demmer, J., Stasiuk, S. J., Grigor, M. R., Simpson, K. J., and Nicholas, K. R. (2001). Differential expression of the whey acidic protein gene during lactation in the brushtail possum (Trichosurus vulpecula). Biochim. Biophys. Acta 1522, 187–194.
| Differential expression of the whey acidic protein gene during lactation in the brushtail possum (Trichosurus vulpecula).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xls1ehsg%3D%3D&md5=1fe48c331eca3afe5a5b3968ba57a27dCAS | 11779633PubMed |
Dennis, G., Sherman, B., Hosack, D., Yang, J., Gao, W., Lane, H. C., and Lempicki, R. (2003). DAVID: Database for Annotation, Visualisation and Integrated Discovery. Genome Biol. 4, 3.
| DAVID: Database for Annotation, Visualisation and Integrated Discovery.Crossref | GoogleScholarGoogle Scholar |
Devinoy, E., Hubert, C., Jolivet, G., Thepot, D., Clergue, N., Desaleux, M., Dion, M., Servely, J. L., and Houdebine, L. M. (1988). Recent data on the structure of rabbit milk-protein genes and on the mechanism of the hormonal control of their expression. Reprod. Nutr. Dev. 28, 1145–1164.
| Recent data on the structure of rabbit milk-protein genes and on the mechanism of the hormonal control of their expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXht12mtb4%3D&md5=6a62600d28e1ab71859d9488e76043f9CAS | 3072627PubMed |
Edgar, R., Domrachev, M., and Lash, A. E. (2002). Gene Expression Omnibus: NCBI gene expression and hybridisation array data repository. Nucleic Acids Res. 30, 207–210.
| Gene Expression Omnibus: NCBI gene expression and hybridisation array data repository.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xht12kurs%3D&md5=16d950d0398d5934846e8cb789e39e96CAS | 11752295PubMed |
Finucane, K. A., Mcfadden, T. B., Bond, J. P., Kennelly, J. J., and Zhao, F. Q. (2008). Onset of lactation in the bovine mammary gland: gene expression profiling indicates a strong inhibition of gene expression in cell proliferation. Funct. Integr. Genomics 8, 251–264.
| Onset of lactation in the bovine mammary gland: gene expression profiling indicates a strong inhibition of gene expression in cell proliferation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntVWiur8%3D&md5=bf8d495ee84f24241705d5901c38040cCAS | 18259788PubMed |
Green, B. (1984). Composition of milk and energetics of growth. In ‘Physiological strategies in lactation: the Proceedings of a Symposium held at the Zoological Society of London’. pp. 369–387. (Academic Press: London.)
Green, B., Griffiths, M., and Leckie, R. (1983). Qualitative and quantitative changes in milk fat during lactation in the tammar wallaby (Macropus eugenii). Aust. J. Biol. Sci. 36, 455–461.
| 1:CAS:528:DyaL2cXotlCmuw%3D%3D&md5=3035786058869755b2c61511caa4103eCAS | 6675645PubMed |
Guyette, W. A., Matusik, R. J., and Rosen, J. M. (1979). Prolactin-mediated transcriptional and post-transcriptional control of casein gene expression. Cell 17, 1013–1023.
| Prolactin-mediated transcriptional and post-transcriptional control of casein gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXlsFWltrk%3D&md5=2c3560745dae5e630e39dacd0a9a8773CAS | 487427PubMed |
Hasselbalch, H., Jeppesen, D., Engelmann, M., Michaelsen, K., and Nielsen, M. (1996). Decreased thymus size in formula-fed infants compared with breastfed infants. Acta Paediatr. 85, 1029–1032.
| Decreased thymus size in formula-fed infants compared with breastfed infants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s%2Fktlynsw%3D%3D&md5=15c549a565cbe7d672791ec0680bb21eCAS | 8888912PubMed |
Hennighausen, L. G., and Sippel, A. E. (1982). Mouse whey acidic protein is a novel member of the family of ‘four-disulfide core’ proteins. Nucleic Acids Res. 10, 2677–2684.
| Mouse whey acidic protein is a novel member of the family of ‘four-disulfide core’ proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XktFygt7Y%3D&md5=16a4ff317dedbcc72ff6ba3896ac453cCAS | 6896234PubMed |
Hosack, D. A., Dennis, G., Sherman, B. T., Lane, H. C., and Lempicki, R. A. (2003). Identifying biological themes within lists of genes with EASE. Genome Biol. 4, R70.
| Identifying biological themes within lists of genes with EASE.Crossref | GoogleScholarGoogle Scholar | 14519205PubMed |
Huang, D. W., Sherman, B. T., and Lempicki, R. A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44–57.
| Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFCkurnI&md5=e95521288c9064241695903dc4556814CAS |
Jenness, R. (1986). Lactational performance of various mammalian species. J. Dairy Sci. 69, 869–885.
| Lactational performance of various mammalian species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL283isVyiug%3D%3D&md5=201b081f4b8d599a91981f15bc016f6dCAS | 3519706PubMed |
Joss, J. L., Molloy, M. P., Hinds, L., and Deane, E. (2009). A longitudinal study of the protein components of marsupial milk from birth to weaning in the tammar wallaby (Macropus eugenii). Dev. Comp. Immunol. 33, 152–161.
| A longitudinal study of the protein components of marsupial milk from birth to weaning in the tammar wallaby (Macropus eugenii).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlWrsbnP&md5=4a3f80c48340488c3375d4af2c92956cCAS | 18778730PubMed |
Khalil, E., Digby, M. R., Thomson, P. C., Lefèvre, C., Mailer, S. L., Pooley, C., and Nicholas, K. R. (2011). Acute involution in the tammar wallaby: identification of genes and putative novel milk proteins implicated in mammary gland function. Genomics 97, 372–378.
| Acute involution in the tammar wallaby: identification of genes and putative novel milk proteins implicated in mammary gland function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXms12kt74%3D&md5=6bb1c597149e1bde111a58861b4363e3CAS | 21419215PubMed |
Kruse, P. E. (1983). The importance of colostral immunoglobulins and their absorption from the intestine of the newborn animals. Ann. Rech. Vet. 14, 349–353.
| 1:STN:280:DyaL2c3ivFOksg%3D%3D&md5=60d617eb135118add87328be38fdfbf8CAS | 6677175PubMed |
Kwek, J. H. L., Wijesundera, C., Digby, M. R., and Nicholas, K. R. (2007). The endocrine regulation of milk-lipid synthesis and secretion in tammar wallaby (Macropus eugenii). Biochim. Biophys. Acta 1770, 48–54.
| The endocrine regulation of milk-lipid synthesis and secretion in tammar wallaby (Macropus eugenii).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlalsbfI&md5=4da7c4018a0f19ed62528e4ed6aaf210CAS |
Laffin, B., Wellberg, E., Kwak, H. I., Burghardt, R. C., Metz, R. P., Gustafson, T., Schedin, P., and Porter, W. W. (2008). Loss of singleminded-2s in the mouse mammary gland induces an epithelial–mesenchymal transition associated with upregulation of slug and matrix metalloprotease 2. Mol. Cell. Biol. 28, 1936–1946.
| Loss of singleminded-2s in the mouse mammary gland induces an epithelial–mesenchymal transition associated with upregulation of slug and matrix metalloprotease 2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtlKjur8%3D&md5=cfae7ce2c8ad85a1cd11c8bd8d6b2da5CAS | 18160708PubMed |
Lefèvre, C. M., Digby, M. R., Whitley, J. C., Strahm, Y., and Nicholas, K. R. (2007). Lactation transcriptomics in the Australian marsupial, Macropus eugenii: transcript sequencing and quantification. BMC Genomics 8, 417.
| Lactation transcriptomics in the Australian marsupial, Macropus eugenii: transcript sequencing and quantification.Crossref | GoogleScholarGoogle Scholar | 17997866PubMed |
Lemay, D. G., Neville, M. C., Rudolph, M. C., Pollard, K. S., and German, J. B. (2007). Gene regulatory networks in lactation: identification of global principles using bioinformatics. BMC Syst. Biol. 1, 56.
| Gene regulatory networks in lactation: identification of global principles using bioinformatics.Crossref | GoogleScholarGoogle Scholar | 18039394PubMed |
Lu, B., Asara, J. M., Sanda, M. G., and Arredouani, M. S. (2011). The role of the transcription factor SIM2 in prostate cancer. PLoS ONE 6, e28837.
| The role of the transcription factor SIM2 in prostate cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFal&md5=4103b7639f1009dc8ef5fce67047f79eCAS | 22174909PubMed |
Luo, Z.-X., Ji, Q., Wible, J. R., and Yuan, C.-X. (2003). An early Cretaceous tribosphenic mammal and metatherian evolution. Science 302, 1934–1940.
| An early Cretaceous tribosphenic mammal and metatherian evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXps1ams78%3D&md5=02dae8949602362411c43a2b99a7f2aaCAS | 14671295PubMed |
Master, S. R., Hartman, J. L., D’Cruz, C. M., Moody, S. E., Keiper, E. A., Ha, S. I., Cox, J. D., Belka, G. K., and Chodosh, L. A. (2002). Functional microarray analysis of mammary organogenesis reveals a developmental role in adaptive thermogenesis. Mol. Endocrinol. 16, 1185–1203.
| Functional microarray analysis of mammary organogenesis reveals a developmental role in adaptive thermogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlWktLw%3D&md5=67191d656f6d9b146ba6addbf9d410acCAS | 12040007PubMed |
Mead, J. R., Irvine, S. A., and Ramji, D. P. (2002). Lipoprotein lipase: structure, function, regulation and role in disease. J. Mol. Med. 80, 753–769.
| Lipoprotein lipase: structure, function, regulation and role in disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xptlylur0%3D&md5=4be2c63b7301507279c89b7ca72069dcCAS | 12483461PubMed |
Menzies, K. K., Lefèvre, C., Sharp, J. A., Macmillan, K. L., Sheehy, P. A., and Nicholas, K. R. (2009). A novel approach identified the FOLR1 gene, a putative regulator of milk-protein synthesis. Mamm. Genome 20, 498–503.
| A novel approach identified the FOLR1 gene, a putative regulator of milk-protein synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1Cis7bJ&md5=c4f25945be70314f30c73afd7f039bf7CAS | 19669235PubMed |
Messer, M., and Green, B. (1979). Milk carbohydrates of marsupials. II. Quantitative and qualitative changes in milk carbohydrates during lactation in the tammar wallaby (Macropus eugenii). Aust. J. Biol. Sci. 32, 519–531.
| 1:CAS:528:DyaL3cXntlGksw%3D%3D&md5=d96b6bbb9b3da1468875775bc30d0aeaCAS | 549552PubMed |
Moshel, Y., Rhoads, R. E., and Barash, I. (2006). Role of amino acids in translational mechanisms governing milk-protein synthesis in murine and ruminant mammary epithelial cells. J. Cell. Biochem. 98, 685–700.
| Role of amino acids in translational mechanisms governing milk-protein synthesis in murine and ruminant mammary epithelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltVejtb0%3D&md5=828c08c99f3d01205f1fd985925a9dabCAS | 16440312PubMed |
Nadin-Davis, S. A., and Mezl, V. A. (1985). Variation in the lack of polyadenylation of the rat milk-protein mRNAs during the lactation cycle. Int. J. Biochem. 17, 1067–1075.
| Variation in the lack of polyadenylation of the rat milk-protein mRNAs during the lactation cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlvFCjsbo%3D&md5=d60d9e72241eba539ab0eee01cd98d23CAS | 3840750PubMed |
Neville, M. C., Allen, J. C., Archer, P. C., Casey, C. E., Seacat, J., Keller, R. P., Lutes, V., Rasbach, J., and Neifert, M. (1991). Studies in human lactation: milk volume and nutrient composition during weaning and lactogenesis. Am. J. Clin. Nutr. 54, 81–92.
| 1:STN:280:DyaK3M3otFOhtA%3D%3D&md5=ad9a32ce32a25963b6a7317bac9a94ceCAS | 2058592PubMed |
Nicholas, K. R. (1988). Asynchronous dual lactation in a marsupial, the tammar wallaby (Macropus eugenii). Biochem. Biophys. Res. Commun. 154, 529–536.
| Asynchronous dual lactation in a marsupial, the tammar wallaby (Macropus eugenii).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c3ptlCkuw%3D%3D&md5=3c57235ea1c463aa4de9787d9cc954afCAS | 2456758PubMed |
Nicholas, K. R., Wilde, C. J., Bird, P. H., Hendry, K. A. K., Tregenza, K., and Warner, B. 1995. Asynchronous concurrent secretion of milk proteins in the tammar wallaby (Macropus eugenii). In ‘Intercellular Signalling in the Mammary Gland’. (Ed. C. J. W. E. Al.) pp. 153–170. (Plenum Press: New York.)
Nicholas, K., Simpson, K., Wilson, M., Trott, J., and Shaw, D. (1997). The tammar wallaby: a model to study putative autocrine-induced changes in milk composition. J. Mammary Gland Biol. Neoplasia 2, 299–310.
| The tammar wallaby: a model to study putative autocrine-induced changes in milk composition.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3czosF2htQ%3D%3D&md5=82e79ed2898ee0e9c7152da708cd9ae1CAS | 10882313PubMed |
Nilsson, M. A., Churakov, G., Sommer, M., Tran, N. V., Zemann, A., Brosius, J., and Schmitz, J. (2010). Tracking marsupial evolution using archaic genomic retroposon insertions. PLoS Biol. 8, e1000436.
| Tracking marsupial evolution using archaic genomic retroposon insertions.Crossref | GoogleScholarGoogle Scholar | 20668664PubMed |
Oakes, S. R., Hilton, H. N., and Ormandy, C. J. (2006). Key stages in mammary gland development. The alveolar switch: coordinating the proliferative cues and cell-fate decisions that drive the formation of lobuloalveoli from ductal epithelium. Breast Cancer Res. 8, 207.
| Key stages in mammary gland development. The alveolar switch: coordinating the proliferative cues and cell-fate decisions that drive the formation of lobuloalveoli from ductal epithelium.Crossref | GoogleScholarGoogle Scholar | 16677418PubMed |
Ohtsubo, K., and Marth, J. D. (2006). Glycosylation in cellular mechanisms of health and disease. Cell 126, 855–867.
| Glycosylation in cellular mechanisms of health and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvVKitbo%3D&md5=11a1d869d667ba471f55f5f48ccf0fafCAS | 16959566PubMed |
Pittius, C. W., Sankaran, L., Topper, Y. J., and Hennighausen, L. (1988). Comparison of the regulation of the whey acidic protein gene with that of a hybrid gene containing the whey acidic protein gene promoter in transgenic mice. Mol. Endocrinol. 2, 1027–1032.
| Comparison of the regulation of the whey acidic protein gene with that of a hybrid gene containing the whey acidic protein gene promoter in transgenic mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXjsVKksw%3D%3D&md5=1d23b98ab481a7f2d0bda58a52b33400CAS | 2464745PubMed |
Puissant, C., and Houdebine, L. M. (1991). Cortisol induces rapid accumulation of whey acid protein mRNA but not of asl and b-casein mRNA in rabbit mammary explants. Cell Biol. Int. Rep. 15, 121–129.
| Cortisol induces rapid accumulation of whey acid protein mRNA but not of asl and b-casein mRNA in rabbit mammary explants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlt1Onu7k%3D&md5=57fcd64f78f9c3e7228446562ad96c37CAS | 2029731PubMed |
R Core Team (2013). ‘R: A language and environment for statistical computing’. (R Foundation for Statistical Computing, Vienna, Austria.) Available from http://www.R-project.org/ [Verified 13 January 2015]
Ron, M., Israeli, G., Seroussi, E., Weller, J., Gregg, J., Shani, M., and Medrano, J. (2007). Combining mouse mammary gland gene expression and comparative mapping for the identification of candidate genes for QTL of milk production traits in cattle. BMC Genomics 8, 183.
| Combining mouse mammary gland gene expression and comparative mapping for the identification of candidate genes for QTL of milk production traits in cattle.Crossref | GoogleScholarGoogle Scholar | 17584498PubMed |
Rudolph, M. C., Mcmanaman, J. L., Hunter, L., Phang, T., and Neville, M. C. (2003). Functional development of the mammary gland: use of expression profiling and trajectory clustering to reveal changes in gene expression during pregnancy, lactation and involution. J. Mammary Gland Biol. Neoplasia 8, 287–307.
| Functional development of the mammary gland: use of expression profiling and trajectory clustering to reveal changes in gene expression during pregnancy, lactation and involution.Crossref | GoogleScholarGoogle Scholar | 14973374PubMed |
Schneckener, S., Arden, N., and Schuppert, A. (2011). Quantifying stability in gene-list ranking across microarray-derived clinical biomarkers. BMC Med. Genomics 4, 73.
| Quantifying stability in gene-list ranking across microarray-derived clinical biomarkers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFOqtLo%3D&md5=e412ef11c119a9ed48ed293046fb5af8CAS | 21996057PubMed |
Schoenenberger, C.-A., Zuk, A., Groner, B., Jones, W., and Andres, A.-C. (1990). Induction of the endogenous whey acidic protein (Wap) gene and a Wap-myc hybrid gene in primary murine mammary organoids. Dev. Biol. 139, 327–337.
| Induction of the endogenous whey acidic protein (Wap) gene and a Wap-myc hybrid gene in primary murine mammary organoids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXkt1Wgu70%3D&md5=a3d2fdacd8fd5ce2de6ef2b8806b42bbCAS | 2186946PubMed |
Scribner, K. C., Wellberg, E. A., Metz, R. P., and Porter, W. W. (2011). Singleminded-2s (Sim2s) promotes delayed involution of the mouse mammary gland through suppression of Stat3 and NFKB. Mol. Endocrinol. 25, 635–644.
| Singleminded-2s (Sim2s) promotes delayed involution of the mouse mammary gland through suppression of Stat3 and NFKB.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsVKrur4%3D&md5=faa81f1f7bb950960c3c01149eb37ec4CAS | 21292822PubMed |
Simpson, K. J., and Nicholas, K. R. (2002). The comparative biology of whey proteins. J. Mammary Gland Biol. Neoplasia 7, 313–326.
| The comparative biology of whey proteins.Crossref | GoogleScholarGoogle Scholar | 12751894PubMed |
Simpson, K., Shaw, D., and Nicholas, K. (1998a). Developmentally regulated expression of a putative protease inhibitor gene in the lactating mammary gland of the tammar wallaby, Macropus eugenii. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 120, 535–541.
| Developmentally regulated expression of a putative protease inhibitor gene in the lactating mammary gland of the tammar wallaby, Macropus eugenii.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M%2FgsVSrsw%3D%3D&md5=ec07c7d0279737e94567079a7627ad43CAS | 9787813PubMed |
Simpson, K. J., Bird, P., Shaw, D., and Nicholas, K. (1998b). Molecular characterisation and hormone-dependent expression of the porcine whey acidic protein gene. J. Mol. Endocrinol. 20, 27–35.
| Molecular characterisation and hormone-dependent expression of the porcine whey acidic protein gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtlygtbc%3D&md5=23e52dd3875b1d7a1c393fe54d13d4a1CAS | 9513079PubMed |
Smyth, G. K. (2004). Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Statistical Applications in Genetics and Molecular Biology 3, Article 3.
| Linear models and empirical Bayes methods for assessing differential expression in microarray experiments.Crossref | GoogleScholarGoogle Scholar |
Smyth, G. K. (2005). Limma: linear models for microarray data. In ‘Bioinformatics and Computational Biology Solutions using R and Bioconductor’. (Eds R. Gentleman, V. Carey, S. Dudoit, R. Irizarry, W. Huber) pp. 397–420. (Springer: New York)
Smyth, G. K., and Speed, T. (2003). Normalisation of cDNA microarray data. Methods 31, 265–273.
| Normalisation of cDNA microarray data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXos1Chur4%3D&md5=b2737b5e9aaecec522f26c9bcd1563a2CAS | 14597310PubMed |
Smyth, G. K., Ritchie, M. E., Thorne, N., and Wettenhall, J. (2005). ‘LIMMA: Linear Models for Microarray Data User’s Guide’. Available from http://www.bioconductor.org/packages/release/bioc/vignettes/limma/inst/doc/usersguide.pdf [Verified 13 January 2015]
Stein, T., Morris, J., Davies, C., Weber-Hall, S., Duffy, M.-A., Heath, V., Bell, A., Ferrier, R., Sandilands, G., and Gusterson, B. (2004). Involution of the mouse mammary gland is associated with an immune cascade and an acute-phase response, involving LBP, CD14 and STAT3. Breast Cancer Res. 6, R75–R91.
| Involution of the mouse mammary gland is associated with an immune cascade and an acute-phase response, involving LBP, CD14 and STAT3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptVOqsw%3D%3D&md5=796d72ae31870ac43a469d3cb44dd83cCAS | 14979920PubMed |
Thompson, J. M. D., Becroft, D. M. O., and Mitchell, E. A. (2000). Previous breastfeeding does not alter thymic size in infants dying of sudden infant death syndrome. Acta Paediatr. 89, 112–114.
| Previous breastfeeding does not alter thymic size in infants dying of sudden infant death syndrome.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7ktVaguw%3D%3D&md5=2f46b53a4ec248cc0cb7495c48a27124CAS |
Tyndale-Biscoe, C., and Janssens, P. (1988). ‘The Developing Marsupial: Models for Biomedical Research’. (Springer-Verlag: Heidelberg.)
Wang, X., Inoue, S., Gu, J., Miyoshi, E., Noda, K., Li, W., Mizuno-Horikawa, Y., Nakano, M., Asahi, M., Takahashi, M., Uozumi, N., Ihara, S., Lee, S. H., Ikeda, Y., Yamaguchi, Y., Aze, Y., Tomiyama, Y., Fujii, J., Suzuki, K., Kondo, A., Shapiro, S. D., Lopez-Otin, C., Kuwaki, T., Okabe, M., Honke, K., and Taniguchi, N. (2005). Dysregulation of TGF-β1 receptor activation leads to abnormal lung development and emphysema-like phenotype in core fucose-deficient mice. Proc. Natl. Acad. Sci. USA 102, 15 791–15 796.
| Dysregulation of TGF-β1 receptor activation leads to abnormal lung development and emphysema-like phenotype in core fucose-deficient mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Wru7nN&md5=5d3e969704f356b3bd68aa229ce7e2ceCAS |
Ward, J. H. (1963). Hierarchical grouping to optimise an objective function. J. Am. Stat. Assoc. 58, 236–244.
| Hierarchical grouping to optimise an objective function.Crossref | GoogleScholarGoogle Scholar |
Wilson, J. R., Williams, D., and Schachter, H. (1976). The control of glycoprotein synthesis: n-acetylglucosamine linkage to a mannose residue as a signal for the attachment of l-fucose to the asparagine-linked n-acetylglucosamine residue of glycopeptide from alpha1-acid glycoprotein. Biochem. Biophys. Res. Commun. 72, 909–916.
| The control of glycoprotein synthesis: n-acetylglucosamine linkage to a mannose residue as a signal for the attachment of l-fucose to the asparagine-linked n-acetylglucosamine residue of glycopeptide from alpha1-acid glycoprotein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XlvVOrsbs%3D&md5=94772d48954dbe8c0220f7705bd012a7CAS | 985526PubMed |
Wongtrakul-Kish, K., Kolarich, D., Pascovici, D., Joss, J. L., Deane, E., and Packer, N. H. (2012). Characterisation of n- and o-linked glycosylation changes in milk of the tammar wallaby (Macropus eugenii) over lactation. Glycoconj. J. 30, 523–536.
| Characterisation of n- and o-linked glycosylation changes in milk of the tammar wallaby (Macropus eugenii) over lactation.Crossref | GoogleScholarGoogle Scholar | 23053637PubMed |
Yago, T., Fu, J., Mcdaniel, J. M., Miner, J. J., Mcever, R. P., and Xia, L. (2010). Core 1-derived o-glycans are essential E-selectin ligands on neutrophils. Proc. Natl. Acad. Sci. USA 107, 9204–9209.
| Core 1-derived o-glycans are essential E-selectin ligands on neutrophils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmslGrt7k%3D&md5=0a140b1ab158e4142b50b6654567983cCAS | 20439727PubMed |
Yang, X., and Sun, X. (2007). Meta-analysis of several gene lists for distinct types of cancer: a simple way to reveal common prognostic markers. BMC Bioinformatics 8, 118.
| Meta-analysis of several gene lists for distinct types of cancer: a simple way to reveal common prognostic markers.Crossref | GoogleScholarGoogle Scholar | 17411443PubMed |
Yang, X., Bentink, S., Scheid, S., and Spang, R. (2006). Similarities of ordered gene lists. J. Bioinform. Comput. Biol. 4, 693–708.
| Similarities of ordered gene lists.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptFCls7c%3D&md5=0b54b10269890f38c66246cec3c94385CAS | 16960970PubMed |
Yang, X., Scheid, S., and Lottaz, C. (2008). ‘OrderedList: Similarities of Ordered Gene Lists. R package version 1.38.0’. Available from http://compdiag.molgen.mpg.de/software/index.shtml [Verified 13 January 2015]
