Transcriptome analysis of the hormone-sensing cells in mammary epithelial reveals dynamic changes in early pregnancy

BMC Developmental Biology

Volumn 15, Issue 1, 2015, Pages

  De Silva, Duvini ^a,b   Kunasegaran, Kamini ^a,b   Ghosh, Sujoy ^a   Pietersen, Alexandra M ^a,b  

^a DIVISION OF MEDICAL ONCOLOGY   (Singapore)

^b DUKE NUS MEDICAL SCHOOL   (Singapore)

Author keywords

Estrogen receptor; Mammary gland; Microarray; Morphogenesis; Proliferation; Single cell analysis

Indexed keywords

HORMONE; TRANSCRIPTOME;

ANIMAL; BREAST TUMOR; CELL PROLIFERATION; CYTOLOGY; FEMALE; GENETICS; METABOLISM; MOUSE; PATHOLOGY; PREGNANCY; UDDER;

ANIMALS; BREAST NEOPLASMS; CELL PROLIFERATION; FEMALE; HORMONES; MAMMARY GLANDS, ANIMAL; MICE; PREGNANCY; TRANSCRIPTOME;

EID: 84989898664     PISSN: None     EISSN: 1471213X     Source Type: Journal    
DOI: 10.1186/s12861-015-0058-9     Document Type: Article

References (57)

1. Brisken C, O'Malley B. Hormone action in the mammary gland. Cold Spring Harbor Perspectives in Biology. 2010;2:a003178.
2. Tarulli GA, De Silva D, Ho V, Kunasegaran K, Ghosh K, Tan BC, et al. Hormone-sensing cells require Wip1 for paracrine stimulation in normal and premalignant mammary epithelium. Breast Cancer Res. 2013;15:R10.
3. Kendrick H, Regan JL, Magnay F-A, Grigoriadis A, Mitsopoulos C, Zvelebil M, et al. Transcriptome analysis of mammary epithelial subpopulations identifies novel determinants of lineage commitment and cell fate. BMC Genomics. 2008;9:591.
4. Clarke RB, Howell A, Potten CS, Anderson E. Dissociation between steroid receptor expression and cell proliferation in the human breast. Cancer Res. 1997;57:4987-91.
5. Zeps N, Bentel JM, Papadimitriou JM, D'Antuono MF, Dawkins HJ. Estrogen receptor-negative epithelial cells in mouse mammary gland development and growth. Differentiation. 1998;62:221-6.
6. Shehata M, Teschendorff A, Sharp G, Novcic N, Russell A, Avril S, et al. Phenotypic and functional characterization of the luminal cell hierarchy of the mammary gland. Breast Cancer Res. 2012;14:R134.
7. Wicha MS. Targeting breast cancer stem cells. Breast. 2009;18:S56-8.
8. Lim E, Wu D, Pal B, Bouras T, Asselin-Labat M-L, Vaillant F, et al. Transcriptome analyses of mouse and human mammary cell subpopulations reveal multiple conserved genes and pathways. Breast Cancer Res. 2010;12:R21.
9. Ewan KBR, Oketch-Rabah HA, Ravani SA, Shyamala G, Moses HL, Barcellos-Hoff MH. Proliferation of estrogen receptor-Alpha-positive mammary epithelial cells is restrained by transforming growth factor-beta1 in adult mice. Am J Pathol. 2005;167:409-17.
10. Mastroianni M, Kim S, Kim YC, Esch A, Wagner C, Alexander CM. Wnt signaling can substitute for estrogen to induce division of ERα-positive cells in a mouse mammary tumor model. Cancer Lett. 2010;289:23-31.
11. Beleut M, Rajaram RD, Caikovski M, Ayyanan A, Germano D, Choi Y, et al. Two distinct mechanisms underlie progesterone-induced proliferation in the mammary gland. Proc Natl Acad Sci. 2010;107:2989-94.
12. van Amerongen R, Bowman AN, Nusse R. Developmental stage and time dictate the fate of Wnt/β-catenin-responsive stem cells in the mammary gland. Cell Stem Cell. 2012;11:387-400.
13. Šale S, Lafkas D, Artavanis-Tsakonas S. Notch2 genetic fate mapping reveals two previously unrecognized mammary epithelial lineages. Nat Cell Biol. 2013;15:1-11.
14. Chang TH-T, Kunasegaran K, Tarulli GA, De Silva D, Voorhoeve PM, Pietersen AM. New insights into lineage restriction of mammary gland epithelium using parity-identified mammary epithelial cells. Breast Cancer Res. 2014;16:R1.
15. Alexander CM, Joshi PA, Khokha R. Fully Interlocking: A Story of Teamwork among Breast Epithelial Cells. Dev Cell. 2014;28:114-5.
16. Lee HJ, Ormandy CJ. Interplay between progesterone and prolactin in mammary development and implications for breast cancer. Mol Cell Endocrinol. 2012;357:101-7.
17. Brisken C, Kaur S, Chavarria T, Binart N. Prolactin controls mammary gland development via direct and indirect mechanisms. Dev Biol. 1999;210:96-106.
18. Lange CA, Shen T, Horwitz KB. Phosphorylation of human progesterone receptors at serine-294 by mitogen-Activated protein kinase signals their degradation by the 26S proteasome. Proc Natl Acad Sci U S A. 2000;97:1032-7.
19. Hilton HN, Doan TB, Graham JD, Oakes SR, Silvestri A, Santucci N, et al. Acquired convergence of hormone signaling in breast cancer: ER and PR transition from functionally distinct in normal breast to predictors of metastatic disease. Oncotarget. 2014;5:8651-64.
20. Ho V, Yeo SY, Kunasegaran K, De Silva D, Tarulli GA, Voorhoeve PM, et al. Expression analysis of rare cellular subsets: direct RT-PCR on limited cell numbers obtained by FACS or soft agar assays. BioTechniques. 2013;54:208-12.
21. Domené HM, Scaglia PA, Jasper HG. Deficiency of the insulin-like growth factor-binding protein acid-labile subunit (ALS) of the circulating ternary complex in children with short stature. Pediatr Endocrinol Rev. 2010;7:339-46.
22. Tonner E, Barber MC, Allan GJ, Beattie J, Webster J, Whitelaw CBA, et al. Insulin-like growth factor binding protein-5 (IGFBP-5) induces premature cell death in the mammary glands of transgenic mice. Development. 2002;129:4547-57.
23. Chatterjee S, Bacopulos S, Yang W, Amemiya Y, Spyropoulos D, Raouf A, et al. Loss of igfbp7 causes precocious involution in lactating mouse mammary gland. PLoS One. 2014;9:e87858.
24. Kaffer CR, Grinberg A, Pfeifer K. Regulatory mechanisms at the mouse Igf2/H19 locus. Mol Cell Biol. 2001;21:8189-96.
25. Gaudet S, Branton D, Lue RA. Characterization of PDZ-binding kinase, a mitotic kinase. Proc Natl Acad Sci U S A. 2000;97:5167-72.
26. Lei M, Tye BK. Initiating DNA synthesis: from recruiting to activating the MCM complex. J Cell Sci. 2001;114:1447-54.
27. Miyagawa K, Tsuruga T, Kinomura A, Usui K, Katsura M, Tashiro S, et al. A role for RAD54B in homologous recombination in human cells. EMBO J. 2002;21:175-80.
28. Ismail PM, DeMayo FJ, Amato P, Lydon JP. Progesterone induction of calcitonin expression in the murine mammary gland. J Endocrinol. 2004;180:287-95.
29. Lu SS, Becker KAK, Hagen MJM, Yan HH, Roberts ALA, Mathews LAL, et al. Transcriptional responses to estrogen and progesterone in mammary gland identify networks regulating p53 activity. Endocrinology. 2008;149:4809-20.
30. Levina V, Su Y, Gorelik E. Immunological and nonimmunological effects of indoleamine 2, 3-dioxygenase on breast tumor growth and spontaneous metastasis formation. Clin Dev Immunol. 2012;2012:173029.
31. Soliman H, Rawal B, Fulp J, Lee J-H, Lopez A, Bui MM, et al. Analysis of indoleamine 2-3 dioxygenase (IDO1) expression in breast cancer tissue by immunohistochemistry. Cancer Immunol Immunother. 2013;62:829-37.
32. Yu X, Shen H, Liu L, Lin L, Gao M, Wang S. Changes of sodium iodide symporter regulated by IGF-I and TGF-β1 in mammary gland cells from lactating mice at different iodine levels. Biol Trace Elem Res. 2012;146:73-8.
33. Said TK, Conneely OM, Medina D, O'Malley BW, Lydon JP. Progesterone, in addition to estrogen, induces cyclin D1 expression in the murine mammary epithelial cell, in vivo. Endocrinology. 1997;138:3933-9.
34. Lain AR, Creighton CJ, Conneely OM. Research resource: progesterone receptor targetome underlying mammary gland branching morphogenesis. Mol Endocrinol. 2013;27:1743-61.
35. Hurle B, Swanson W, Swanson W, Green ED. Comparative sequence analyses reveal rapid and divergent evolutionary changes of the WFDC locus in the primate lineage. Genome Res. 2007;17:276-86.
36. Amiano NO, Costa MJ, Reiteri RM, Payés C, Guerrieri D, Tateosian NL, et al. Anti-Tumor effect of SLPI on mammary but not colon tumor growth. J Cell Physiol. 2013;228:469-75.
37. Crouch EC. Structure, biologic properties, and expression of surfactant protein D (SP-D). Biochim Biophys Acta (BBA) - Mol Basis Dis. 1997;1408:278-89.
38. Holmskov U, Mollenhauer J, Madsen J, Vitved L, Gronlund J, Tornoe I, et al. Cloning of gp-340, a putative opsonin receptor for lung surfactant protein D. Proc Natl Acad Sci U S A. 1999;96:10794-9.
39. Kang W, Reid KBM. DMBT1, a regulator of mucosal homeostasis through the linking of mucosal defense and regeneration? Febs Letters. 2003;540:21-5.
40. Braidotti P, Nuciforo PG, Mollenhauer J, Poustka A, Pellegrini C, Moro A, et al. DMBT1 expression is down-regulated in breast cancer. BMC Cancer. 2004;4:46.
41. Winkler C, Yao S. The midkine family of growth factors: diverse roles in nervous system formation and maintenance. Br J Pharmacol. 2014;171:905-12.
42. Sakamoto K, Kadomatsu K. Midkine in the pathology of cancer, neural disease, and inflammation. Pathol Int. 2012;62:445-55.
43. Chen Y, McKenzie KE, Aldaz CM, Sukumar S. Midkine in the progression of rat N-nitroso-N-methylurea-induced mammary tumors. Mol Carcinog. 1996;17:112-6.
44. Ibusuki MM, Fujimori HH, Yamamoto YY, Ota KK, Ueda MM, Shinriki SS, et al. Midkine in plasma as a novel breast cancer marker. Cancer Sci. 2009;100:1735-9.
45. Li LQ, Huang HL, Ping JL, Xu W, Li J, Dai LC. Expression of midkine and endoglin in breast carcinomas with different immunohistochemical profiles. APMIS. 2011;119:103-10.
46. Hsing CH, Cheng HC, Hsu YH, Chan CH, Yeh CH, Li CF, et al. Upregulated IL-19 in Breast Cancer Promotes Tumor Progression and Affects Clinical Outcome. Clin Cancer Res. 2012;18:713-25.
47. Pichery M, Mirey E, Mercier P, Lefrancais E, Dujardin A, Ortega N, et al. Endogenous IL-33 Is Highly Expressed in Mouse Epithelial Barrier Tissues, Lymphoid Organs, Brain, Embryos, and Inflamed Tissues: In Situ Analysis Using a Novel Il-33-LacZ Gene Trap Reporter Strain. J Immunol. 2012;188:3488-95.
48. Oboki K, Ohno T, Kajiwara N, Arae K, Morita H, Ishii A, et al. IL-33 is a crucial amplifier of innate rather than acquired immunity. Proc Natl Acad Sci U S A. 2010;107:18581-6.
49. Jovanovic IP, Pejnovic NN, Radosavljevic GD, Arsenijevic NN, Lukic ML. IL-33/ST2 axis in innate and acquired immunity to tumors. Oncoimmunology. 2012;1:229-31.
50. Lemay DG, Neville MC, Rudolph MC, Pollard KS, German JB. Gene regulatory networks in lactation: identification of global principles using bioinformatics. BMC Syst Biol. 2007;1:56.
51. Anantamongkol U, Charoenphandhu N, Wongdee K, Teerapornpuntakit J, Suthiphongchai T, Prapong S, et al. Transcriptome analysis of mammary tissues reveals complex patterns of transporter gene expression during pregnancy and lactation. Cell Biol Int. 2009;34:67-74.
52. Meier-Abt F, Milani E, Roloff T, Brinkhaus H, Duss S, Meyer DS, et al. Parity induces differentiation and reduces Wnt/Notch signaling ratio and proliferation potential of basal stem/progenitor cells isolated from mouse mammary epithelium. Breast Cancer Res. 2013;15:R36.
53. Hammond MEH, Hayes DF, Dowsett M, Allred DC, Hagerty KL, Badve S, et al. American Society of Clinical Oncology/College Of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J Clin Oncol. 2010;28:2784-95.
54. Smalley MJ. Isolation, culture and analysis of mouse mammary epithelial cells. Methods Mol Biol. 2010;633:139-70.
55. Baldi P, Long AD. A Bayesian framework for the analysis of microarray expression data: Regularized t -Test and statistical inferences.
56. Benjamini Y, Hochberg Y: Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 1995:289-300.
57. Xiao Y, Hsiao TH, Suresh U, Chen H, Wu X. A novel significance score for gene selection and ranking. Bioinformatics (Oxford, England). 2014;30:801-7.