Identification of reference genes for RT-qPCR in ovine mammary tissue during late pregnancy and lactation and in response to maternal nutritional programming

Physiological Genomics

Volumn 46, Issue 15, 2014, Pages 560-570

  Paten, A M ^a,b,c   Pain, S J ^b,c   Peterson, S W ^b,c   Blair, H T ^b,c   Kenyon, P R ^b,c   Dearden, P K ^a,c   Duncan, E J ^a,c  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b MASSEY UNIVERSITY   (New Zealand)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Mammary gland; Nutritional programming; Ovine; Reference gene; RT qPCR

Indexed keywords

CULLIN; CULLIN 1; EUKARYOTIC TRANSLATION INITIATION FACTOR 6; IMPORTIN 9; KARYOPHERIN; MITOCHONDRIAL RIBOSOMAL PROTEIN L39; RIBOSOME PROTEIN; SENTRIN SPECIFIC PROTEASE 2 ISOFORM 1; SMALL NUCLEAR RIBONUCLEOPROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN PRP3; SOLUTE CARRIER ORGANIC ANION TRANSPORTER 1A1; SPLICING FACTOR 1 ISOFORM 2; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BREAST; CONTROLLED STUDY; DNA METHYLATION; EXPERIMENTAL SHEEP; FEMALE; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC ANALYSIS; LACTATION; MAMMARY GLAND; MATERNAL NUTRITION; NEEDLE BIOPSY; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; QUALITATIVE ANALYSIS; REFERENCE GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION QUALITATIVE POLYMERASE CHAIN REACTION; SENSITIVITY ANALYSIS; THIRD TRIMESTER PREGNANCY; ANIMAL; BIOLOGICAL MODEL; BREEDING; DOMESTIC SHEEP; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PREGNANCY; SHEEP; UDDER;

ANIMALS; DNA METHYLATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LACTATION; MAMMARY GLANDS, ANIMAL; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; MODELS, GENETIC; PREGNANCY; PREGNANCY, ANIMAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SHEEP; SHEEP, DOMESTIC;

EID: 84905284539     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00030.2014     Document Type: Article

References (44)

1. Abramowitz LK, Bartolomei MS. Genomic imprinting: recognition and marking of imprinted loci. Curr Opin Genet Dev 22: 72-78, 2012
2. Aggarwal J, Sharma A, Kishore A, Mishra BP, Yadav A, Mohanty A, Sodhi M, Kataria RS, Malakar D, Mukesh M. Identification of suitable housekeeping genes for normalization of quantitative real-time PCR data during different physiological stages of mammary gland in riverine buffaloes (Bubalus bubalis). J Anim Physiol Anim Nutr 97: 1132-1141, 2013
3. Andersen CL, Jensen JL, Orntoft TF. Normalization of real-time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64: 5245-5250, 2004
4. Bionaz M, Loor JJ. Identification of reference genes for quantitative real-time PCR in the bovine mammary gland during the lactation cycle. Physiol Genomics 29: 312-319, 2007
5. Bionaz M, Periasamy K, Rodriguez-Zas SL, Everts RE, Lewin HA, Hurley WL, Loor JJ. Old and new stories: revelations from functional analysis of the bovine mammary transcriptome during the lactation cycle. PLoS One 7: e33268, 2012
6. Blair HT, Jenkinson CM, Peterson SW, Kenyon PR, van der Linden DS, Davenport LC, Mackenzie DD, Morris ST, Firth EC. Dam and granddam feeding during pregnancy in sheep affects milk supply in offspring and reproductive performance in grand-offspring. J Anim Sci 88: E40-E50, 2010
7. Burns MJ, Nixon GJ, Foy CA, Harris N. Standardisation of data from real-time quantitative PCR methods - evaluation of outliers and comparison of calibration curves. BMC Biotechnol 5: 31, 2005
8. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55: 611-622, 2009
9. Calcagno AM, Chewning KJ, Wu CP, Ambudkar SV. Plasma membrane calcium ATPase (PMCA4): a housekeeper for RT-PCR relative quantification of polytopic membrane proteins. BMC Mol Biol 7: 29, 2006
10. Cameron RC, Duncan EJ, Dearden PK. Stable reference genes for the measurement of transcript abundance during larval caste development in the honeybee. Apidologie 44: 357-366, 2013
11. Capuco AV, Akers RM. Management and environmental influences on mammary gland development and milk production. In: Managing the Prenatal Environment to Enhance Livestock Productivity, edited by Greenwood PL, Vercoe PE, Viljoen GJ. Dordrecht: Springer, 2010, p. 259-292
12. Ferreira AM, Bislev SL, Bendixen E, Almeida AM. The mammary gland in domestic ruminants: a systems biology perspective. J Proteomics 94: 110-123, 2013
13. Foret S, Kucharski R, Pellegrini M, Feng S, Jacobsen SE, Robinson GE, Maleszka R. DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees. Proc Natl Acad Sci USA 109: 4968-4973, 2012
14. He YF, Li BZ, Li Z, Liu P, Wang Y, Tang Q, Ding J, Jia Y, Chen Z, Li L, Sun Y, Li X, Dai Q, Song CX, Zhang K, He C, Xu GL. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333: 1303-1307, 2011
15. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8: R19, 2007
16. Hilakivi-Clarke L, Clarke R, Onojafe I, Raygada M, Cho E, Lippman M. A maternal diet high in n - 6 polyunsaturated fats alters mammary gland development, puberty onset, and breast cancer risk among female rat offspring. Proc Natl Acad Sci USA 94: 9372-9377, 1997
17. Hovey RC, Trott JF, Vonderhaar BK. Establishing a framework for the functional mammary gland: From endocrinology to morphology. J Mammary Gland Biol 7: 17-38, 2002
18. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13: 484-492, 2012
19. Kadegowda AK, Bionaz M, Thering B, Piperova LS, Erdman RA, Loor JJ. Identification of internal control genes for quantitative polymer-ase chain reaction in mammary tissue of lactating cows receiving lipid supplements. J Dairy Sci 92: 2007-2019, 2009
20. Kendziorski C, Irizarry RA, Chen KS, Haag JD, Gould MN. On the utility of pooling biological samples in microarray experiments. Proc Natl Acad Sci USA 102: 4252-4257, 2005
21. Kendziorski CM, Zhang Y, Lan H, Attie AD. The efficiency of pooling mRNA in microarray experiments. Biostatistics 4: 465-477, 2003
22. Kenyon PR, Pain SJ, Hutton PG, Jenkinson CMC, Morris ST, Peterson SW, Blair HT. Effects of twin-bearing ewe nutritional treatments on ewe and lamb performance to weaning. Anim Prod Sci 51: 406-415, 2011
23. Konczal M, Koteja P, Stuglik MT, Radwan J, Babik W. Accuracy of allele frequency estimation using pooled RNA-Seq. Mol Ecol Res 14: 381-392, 2014
24. Leth-Larsen R, Lund R, Hansen HV, Laenkholm AV, Tarin D, Jensen ON, Ditzel HJ. Metastasis-related plasma membrane proteins of human breast cancer cells identified by comparative quantitative mass spectrometry. Mol Cell Proteom 8: 1436-1449, 2009
25. Lorincz MC, Dickerson DR, Schmitt M, Groudine M. Intragenic DNA methylation alters chromatin structure and elongation efficiency in mammalian cells. Nat Struct Mol Biol 11: 1068-1075, 2004
26. Lyko F, Foret S, Kucharski R, Wolf S, Falckenhayn C, Maleszka R. The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol 8: e1000506, 2010
27. Maiti A, Drohat AC. Thymine DNA glycosylase can rapidly excise 5-formylcytosine and 5-carboxylcytosine: potential implications for active demethylation of CpG sites. J Biol Chem 286: 35334-35338, 2011
28. Martin NP, Kenyon PR, Morel PCH, Pain SJ, Jenkinson CMC, Hutton PG, Morris ST, Peterson SW, Firth EC, Blair HT. Ewe nutrition in early and mid- to late pregnancy has few effects on fetal development. Anim Prod Sci 52: 533-539, 2012
29. Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D'Souza C, Fouse SD, Johnson BE, Hong C, Nielsen C, Zhao Y, Turecki G, Delaney A, Varhol R, Thiessen N, Shchors K, Heine VM, Rowitch DH, Xing X, Fiore C, Schillebeeckx M, Jones SJ, Haussler D, Marra MA, Hirst M, Wang T, Costello JF. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 466: 253-257, 2010
30. Molenaar AJ, Davis SR, Wilkins RJ. Expression of alpha-lactalbumin, alpha-S1-casein, and lactoferrin genes is heterogeneous in sheep and cattle mammary tissue. J Histochem Cytochem 40: 611-618, 1992
31. Neville MC, McFadden TB, Forsyth I. Hormonal regulation of mammary differentiation and milk secretion. J Mammary Gland Biol 7: 49-66, 2002
32. Paten AM, Kenyon PR, Lopez-Villalobos N, Peterson SW, Jenkinson CMC, Pain SJ, Blair HT. Lactation Biology Symposium: Maternal nutrition during early and mid-to-late pregnancy: comparative effects on milk production of twin-born ewe progeny during their first lactation. J Anim Sci 91: 676-684, 2013
33. Sati S, Tanwar VS, Kumar KA, Patowary A, Jain V, Ghosh S, Ahmad S, Singh M, Reddy SU, Chandak GR, Raghunath M, Sivasubbu S, Chakraborty K, Scaria V, Sengupta S. High resolution methylome map of rat indicates role of intragenic DNA methylation in identification of coding region. PLoS One 7: e31621, 2012
34. Shukla S, Kavak E, Gregory M, Imashimizu M, Shutinoski B, Kashlev M, Oberdoerffer P, Sandberg R, Oberdoerffer S. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 479: 74-79, 2011
35. Spruijt CG, Gnerlich F, Smits AH, Pfaffeneder T, Jansen PW, Bauer C, Munzel M, Wagner M, Muller M, Khan F, Eberl HC, Mensinga A, Brinkman AB, Lephikov K, Muller U, Walter J, Boelens R, van Ingen H, Leonhardt H, Carell T, Vermeulen M. Dynamic readers for 5-(hydroxy) methylcytosine and its oxidized derivatives. Cell 152: 1146-1159, 2013
36. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, Rao A. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324: 930-935, 2009
37. Tramontana S, Bionaz M, Sharma A, Graugnard DE, Cutler EA, Ajmone-Marsan P, Hurley WL, Loor JJ. Internal controls for quantitative polymerase chain reaction of swine mammary glands during pregnancy and lactation. J Dairy Sci 91: 3057-3066, 2008
38. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. Primer3-new capabilities and interfaces. Nucleic Acids Res 40: e115, 2012
39. Valasek MA, Repa JJ. The power of real-time PCR. Adv Physiol Educ 29: 151-159, 2005
40. van der Linden DS, Kenyon PR, Blair HT, Lopez-Villalobos N, Jenkinson CMC, Peterson SW, Mackenzie DDS. Effects of ewe size and nutrition on fetal mammary gland development and lactational performance of offspring at their first lactation. J Anim Sci 87: 3944-3954, 2009
41. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034, 2002
42. Wielscher M, Liou W, Pulverer W, Singer CF, Rappaport-Fuerhauser C, Kandioler D, Egger G, Weinhausel A. Cytosine 5-hydroxymethylation of the LZTS1 gene is reduced in breast cancer. Transl Oncol 6: 715-721, 2013
43. Wutz A, Gribnau J. X inactivation Xplained. Curr Opin Genet Dev 17: 387-393, 2007
44. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13: 134, 2012.