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

详细信息    查看全文

• 作者：Duvini De Silva (1) (2)
  Kamini Kunasegaran (1) (2)
  Sujoy Ghosh (3)
  Alexandra M Pietersen (1) (2) (4)
  
  1. Laboratory of Mammary Gland Biology ; National Cancer Centre Singapore ; 11 Hospital Dr ; Singapore ; 169610 ; Singapore
  2. Program in Cancer & Stem Cell Biology ; Duke-NUS Graduate Medical School ; 8 College ; Rd ; 169857 ; Singapore ; Singapore
  3. Program in Cardiovascular & Metabolic Disorders ; Duke-NUS Graduate Medical School ; 8 College Rd ; Singapore ; 169857 ; Singapore
  4. Department of Physiology ; National University of Singapore ; 21 Lower Kent Ridge Rd ; Singapore ; 119077 ; Singapore
  
• 关键词：Mammary gland ; Morphogenesis ; Single cell analysis ; Proliferation ; Estrogen receptor ; Microarray
• 刊名：BMC Developmental Biology
• 出版年：2015
• 出版时间：December 2015
• 年：2015
• 卷：15
• 期：1
• 全文大小：3,220 KB
• 参考文献：1. Brisken C, O鈥橫alley B. Hormone action in the mammary gland. Cold Spring Harbor Perspectives in Biology. 2010;2:a003178. CrossRef
  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. CrossRef
  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. CrossRef
  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鈥?1.
  5. Zeps N, Bentel JM, Papadimitriou JM, D鈥橝ntuono MF, Dawkins HJ. Estrogen receptor-negative epithelial cells in mouse mammary gland development and growth. Differentiation. 1998;62:221鈥?. CrossRef
  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. CrossRef
  7. Wicha MS. Targeting breast cancer stem cells. Breast. 2009;18:S56鈥?. CrossRef
  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. CrossRef
  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鈥?7. CrossRef
  10. Mastroianni M, Kim S, Kim YC, Esch A, Wagner C, Alexander CM. Wnt signaling can substitute for estrogen to induce division of ER伪-positive cells in a mouse mammary tumor model. Cancer Lett. 2010;289:23鈥?1. CrossRef
  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鈥?4. CrossRef
  12. van Amerongen R, Bowman AN, Nusse R. Developmental stage and time dictate the fate of Wnt/尾-catenin-responsive stem cells in the mammary gland. Cell Stem Cell. 2012;11:387鈥?00. CrossRef
  13. 艩ale S, Lafkas D, Artavanis-Tsakonas S. Notch2 genetic fate mapping reveals two previously unrecognized mammary epithelial lineages. Nat Cell Biol. 2013;15:1鈥?1. CrossRef
  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. CrossRef
  15. Alexander CM, Joshi PA, Khokha R. Fully Interlocking: A Story of Teamwork among Breast Epithelial Cells. Dev Cell. 2014;28:114鈥?. CrossRef
  16. Lee HJ, Ormandy CJ. Interplay between progesterone and prolactin in mammary development and implications for breast cancer. Mol Cell Endocrinol. 2012;357:101鈥?. CrossRef
  17. Brisken C, Kaur S, Chavarria T, Binart N. Prolactin controls mammary gland development via direct and indirect mechanisms. Dev Biol. 1999;210:96鈥?06. CrossRef
  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鈥?. CrossRef
  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鈥?4.
  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鈥?2.
  21. Domen茅 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鈥?6.
  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鈥?7.
  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. CrossRef
  24. Kaffer CR, Grinberg A, Pfeifer K. Regulatory mechanisms at the mouse Igf2/H19 locus. Mol Cell Biol. 2001;21:8189鈥?6. CrossRef
  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鈥?2. CrossRef
  26. Lei M, Tye BK. Initiating DNA synthesis: from recruiting to activating the MCM complex. J Cell Sci. 2001;114:1447鈥?4.
  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鈥?0. CrossRef
  28. Ismail PM, DeMayo FJ, Amato P, Lydon JP. Progesterone induction of calcitonin expression in the murine mammary gland. J Endocrinol. 2004;180:287鈥?5. CrossRef
  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鈥?0. CrossRef
  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. CrossRef
  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鈥?7. CrossRef
  32. Yu X, Shen H, Liu L, Lin L, Gao M, Wang S. Changes of sodium iodide symporter regulated by IGF-I and TGF-尾1 in mammary gland cells from lactating mice at different iodine levels. Biol Trace Elem Res. 2012;146:73鈥?. CrossRef
  33. Said TK, Conneely OM, Medina D, O鈥橫alley BW, Lydon JP. Progesterone, in addition to estrogen, induces cyclin D1 expression in the murine mammary epithelial cell, in vivo. Endocrinology. 1997;138:3933鈥?.
  34. Lain AR, Creighton CJ, Conneely OM. Research resource: progesterone receptor targetome underlying mammary gland branching morphogenesis. Mol Endocrinol. 2013;27:1743鈥?1. CrossRef
  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鈥?6. CrossRef
  36. Amiano NO, Costa MJ, Reiteri RM, Pay茅s 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鈥?5. CrossRef
  37. Crouch EC. Structure, biologic properties, and expression of surfactant protein D (SP-D). Biochim Biophys Acta (BBA) - Mol Basis Dis. 1997;1408:278鈥?9. CrossRef
  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鈥?. CrossRef
  39. Kang W, Reid KBM. DMBT1, a regulator of mucosal homeostasis through the linking of mucosal defense and regeneration? Febs Letters. 2003;540:21鈥?. CrossRef
  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. CrossRef
  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鈥?2. CrossRef
  42. Sakamoto K, Kadomatsu K. Midkine in the pathology of cancer, neural disease, and inflammation. Pathol Int. 2012;62:445鈥?5. CrossRef
  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鈥?. CrossRef
  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鈥?. CrossRef
  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鈥?0. CrossRef
  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鈥?5. CrossRef
  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鈥?5. CrossRef
  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鈥?. CrossRef
  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鈥?1. CrossRef
  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. CrossRef
  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鈥?4.
  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. CrossRef
  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鈥?5. CrossRef
  54. Smalley MJ. Isolation, culture and analysis of mouse mammary epithelial cells. Methods Mol Biol. 2010;633:139鈥?0. CrossRef
  55. Baldi P, Long AD. A Bayesian framework for the analysis of microarray expression data: regularized t -test and statistical inferences of gene changes. Bioinformatics (Oxford, England). 2001;17:509鈥?9. CrossRef
  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鈥?00
  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鈥?. CrossRef
  
• 刊物主题：Developmental Biology; Animal Models; Life Sciences, general;
• 出版者：BioMed Central
• ISSN：1471-213X

文摘

Background Alveoli, the milk-producing units of the mammary gland, are generated during pregnancy by collaboration of different epithelial cell types. We present the first analysis of transcriptional changes within the hormone sensing population during pregnancy. Hormone-receptor positive (HR+) cells play a key role in the initiation of alveologenesis as they sense systemic hormonal changes and translate these into local instructions for neighboring HR- cells. We recently showed that IGF2 is produced specifically by HR+ cells in early pregnancy, but is undetectable in the virgin state. Here, we define the transcriptome of HR+ cells in early pregnancy with the aim to elucidate additional changes that are unique for this dynamic developmental time window. Results We harvested mammary glands from virgin, 3-day and 7-day pregnant mice and isolated a few hundred hormone-sensing cells per animal by FACS for microarray analysis. There was a high concordance between animals with a clear induction of cell cycle progression genes at day 3 of pregnancy and molecules involved in paracrine signalling at day 7. Conclusions These findings underscore the proliferative capacity of HR+ cells upon specific stimuli and elucidate developmentally-restricted changes in cellular communication. Since the majority of breast cancers are HR+, with a variable proportion of HR+ cells per tumor, we anticipate that this data set will aid further studies into the regulation of HR+ cell proliferation and the role of heterotypic signalling within tumors.