Molecular aspects of adipoepithelial transdifferentiation in mouse mammary gland

Stem Cells

Volumn 32, Issue 10, 2014, Pages 2756-2766

  Prokesch, A ^a,b   Smorlesi, A ^c   Perugini, J ^c   Manieri, M ^c   Ciarmela, P ^c   Mondini, E ^c   Trajanoski, Z ^d   Kristiansen, K ^e   Giordano, A ^c   Bogner Strauss, J G ^a,b   Cinti, Saverio ^c  

^a GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^b GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^c UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Adipocytes; Cell transdifferentiation; Elf5 protein; Mouse mammary gland; Spp1 protein

Indexed keywords

ACID PROTEIN; INTEGRIN; OSTEOPONTIN; PERILIPIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ELF5; UNCLASSIFIED DRUG; WHEY ACIDIC PROTEIN; DNA BINDING PROTEIN; ELF5 PROTEIN, MOUSE;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREAST EPITHELIUM; CELL COMPARTMENTALIZATION; CELL CULTURE; CELL NUCLEUS; CELL SPECIFICITY; CELL STRUCTURE; CELL TRANSDIFFERENTIATION; CELL TYPE; CONTROLLED STUDY; FEMALE; GENE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MAMMARY GLAND; MARKER GENE; MOUSE; NONHUMAN; PARACRINE SIGNALING; PHENOTYPE; PREDICTION; PREGNANCY; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; 3T3 CELL LINE; ANIMAL; BIOLOGY; CYTOLOGY; DNA MICROARRAY; EPITHELIUM CELL; GENETICS; METABOLISM; MILK; UDDER; UPREGULATION;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; CELL COMPARTMENTATION; CELL TRANSDIFFERENTIATION; CELLS, CULTURED; COMPUTATIONAL BIOLOGY; DNA-BINDING PROTEINS; EPITHELIAL CELLS; FEMALE; MAMMARY GLANDS, ANIMAL; MICE; MILK; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PARACRINE COMMUNICATION; PHENOTYPE; PREGNANCY; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 84908116572     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1756     Document Type: Article

References (83)

1. Cinti S. Between brown and white: Novel aspects of adipocyte differentiation. Ann Med 2011;43:104-115.
2. Frontini A, Cinti S. Distribution and development of brown adipocytes in the murine and human adipose organ. Cell Metab 2010;11:253-256.
3. Gesta S, Tseng YH, Kahn CR. Developmental origin of fat: Tracking obesity to its source. Cell 2007;131:242-256.
4. Smorlesi A, Frontini A, Giordano A et al. The adipose organ: White-brown adipocyte plasticity and metabolic inflammation. Obes Rev 2012;13 Suppl 2:83-96.
5. Zuk PA, Zhu M, Mizuno H et al. Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng 2001;7:211-228.
6. Zuk PA. The adipose-derived stem cell: Looking back and looking ahead. Mol Biol Cell 2010;21:1783-1787.
7. Matsumoto T, Kano K, Kondo D et al. Mature adipocyte-derived dedifferentiated fat cells exhibit multilineage potential. J Cell Physiol 2008;215:210-222.
8. Fernyhough ME, Hausman GJ, Guan LL et al. Mature adipocytes may be a source of stem cells for tissue engineering. Biochem Biophys Res Commun 2008;368:455-457.
9. Cinti S. Transdifferentiation properties of adipocytes in the adipose organ. Am J Physiol Endocrinol Metab 2009;297:E977-E986.
10. Seale P, Conroe HM, Estall J et al. Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J Clin Invest 2011;121:96-105.
11. Barbatelli G, Murano I, Madsen L et al. The emergence of cold-induced brown adipocytes in mouse white fat depots is determined predominantly by white to brown adipocyte transdifferentiation. Am J Physiol Endocrinol Metab 2010;298:E1244-E1253.
12. Himms-Hagen J, Melnyk A, Zingaretti MC et al. Multilocular fat cells in WAT of CL-316243- treated rats derive directly from white adipocytes. Am J Physiol Cell Physiol 2000;279:C670-C681.
13. Granneman JG, Li P, Zhu Z et al. Metabolic and cellular plasticity in white adipose tissue I: Effects of beta3-adrenergic receptor activation. Am J Physiol Endocrinol Metab 2005;289:E608-E616.
14. Lee YH, Petkova AP, Mottillo EP et al. In vivo identification of bipotential adipocyte progenitors recruited by beta3-adrenoceptor activation and high-fat feeding. Cell Metab 2012;15:480-491.
15. Elias JJ, Pitelka DR, Armstrong RC. Changes in fat cell morphology during lactation in the mouse. Anat Rec 1973;177:533-547.
16. Richert MM, Schwertfeger KL, Ryder JW et al. An atlas of mouse mammary gland development. J Mammary Gland Biol Neoplasia 2000;5:227-241.
17. Hovey RC, Trott JF. Morphogenesis of mammary gland development. Adv Exp Med Biol 2004;554:219-228.
18. Smith GH, Medina D. Re-evaluation of mammary stem cell biology based on in vivo transplantation. Breast Cancer Res 2008;10:203.
19. Couldrey C, Moitra J, Vinson C et al. Adipose tissue: A vital in vivo role in mammary gland development but not differentiation. Dev Dyn 2002;223:459-468.
20. Morroni M, Giordano A, Zingaretti MC et al. Reversible transdifferentiation of secretory epithelial cells into adipocytes in the mammary gland. Proc Natl Acad Sci U S A 2004;101:16801-16806.
21. De MR, Zingaretti MC, Murano I et al. In vivo physiological transdifferentiation of adult adipose cells. Stem Cells 2009;27:2761-2768.
22. Poloni A, Maurizi G, Leoni P et al. Human dedifferentiated adipocytes show similar properties to bone marrow-derived mesenchymal stem cells. Stem Cells 2012;30: 965-974.
23. Howlett AR, Bissell MJ. The influence of tissue microenvironment (stroma and extracellular matrix) on the development and function of mammary epithelium. Epithelial Cell Biol 1993;2:79-89.
24. McCave EJ, Cass CA, Burg KJ et al. The normal microenvironment directs mammary gland development. J Mammary Gland Biol Neoplasia 2010;15:291-299.
25. Boulanger CA, Mack DL, Booth BW et al. Interaction with the mammary microenvironment redirects spermatogenic cell fate in vivo. Proc Natl Acad Sci U S A 2007;104: 3871-3876.
26. Lee HJ, Ormandy CJ. Elf5, hormones and cell fate. Trends Endocrinol Metab 2012;23: 292-298.
27. Rasmussen SB, Young LJT, Smith GH. Preparing mammary gland whole mount from mice. In: Ip MM, Ash BB, eds. Methods in Mammary Gland Biology and Breast Cancer Research. New York: Kluwer Academic Plenum Publisher, 2000, pp 75-85.
28. Hsu SM, Raine L, Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 1981;29: 577-580.
29. Prokesch A, Bogner-Strauss JG, Hackl H et al. Arxes: Retrotransposed genes required for adipogenesis. Nucleic Acids Res 2011;39: 3224-3239.
30. Rainer J, Sanchez-Cabo F, Stocker G et al. CARMAweb: Comprehensive R-and bioconductor-based web service for microarray data analysis. Nucleic Acids Res 2006; 34(Web Server Issue):W498-W503.
31. Sturn A, Quackenbush J, Trajanoski Z. Genesis: Cluster analysis of microarray data. Bioinformatics 2002;18:207-208.
32. Dennis G, Jr., Sherman BT, Hosack DA et al. DAVID: Database for annotation, visualization, and integrated discovery. Genome Biol 2003;4:3.
33. Subramanian A, Tamayo P, Mootha VK et al. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 2005;102:15545-15550.
34. Chen Y, Zhang Y, Yin Y et al. SPD - A webbased secreted protein database. Nucleic Acids Res 2005;33(Database Issue):D169-D173.
35. Petersen TN, Brunak S, von HG et al. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat Methods 2011;8:785-786.
36. Zangani D, Darcy KM, Shoemaker S et al. Adipocyte-epithelial interactions regulate the in vitro development of normal mammary epithelial cells. Exp Cell Res 1999; 247:399-409.
37. Schupp M, Chen F, Briggs ER et al. Metabolite and transcriptome analysis during fasting suggest a role for the p53-Ddit4 axis in major metabolic tissues. BMC Genomics 2013;14:758.
38. Pabinger S, Thallinger GG, Snajder R et al. QPCR: Application for real-time PCR data management and analysis. BMC Bioinformat 2009;10:268.
39. Zhao S, Fernald RD. Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 2005;12: 1047-1064.
40. Brasaemle DL. Thematic review series: Adipocyte biology. The perilipin family of structural lipid droplet proteins: Stabilization of lipid droplets and control of lipolysis. J Lipid Res 2007;48:2547-2559.
41. Greenberg AS, Egan JJ, Wek SA et al. Perilipin, a major hormonally regulated adipocyte-specific phosphoprotein associated with the periphery of lipid storage droplets. J Biol Chem 1991;266:11341-11346.
42. Brasaemle DL, Barber T, Wolins NE et al. Adipose differentiation-related protein is an ubiquitously expressed lipid storage dropletassociated protein. J Lipid Res 1997;38:2249-2263.
43. Russell TD, Palmer CA, Orlicky DJ et al. Cytoplasmic lipid droplet accumulation in developing mammary epithelial cells: Roles of adipophilin and lipid metabolism. J Lipid Res 2007;48:1463-1475.
44. Wolins NE, Quaynor BK, Skinner JR et al. S3-12, Adipophilin, and TIP47 package lipid in adipocytes. J Biol Chem 2005;280:19146-19155.
45. Russell TD, Palmer CA, Orlicky DJ et al. Mammary glands of adipophilin-null mice produce an amino-terminally truncated form of adipophilin that mediates milk lipid droplet formation and secretion. J Lipid Res 2008; 49:206-216.
46. Robinson GW, McKnight RA, Smith GH et al. Mammary epithelial cells undergo secretory differentiation in cycling virgins but require pregnancy for the establishment of terminal differentiation. Development 1995; 121:2079-2090.
47. Lapinskas EJ, Palmer J, Ricardo S et al. A major site of expression of the ets transcription factor Elf5 is epithelia of exocrine glands. Histochem Cell Biol 2004;122:521-526.
48. Choi YS, Chakrabarti R, Escamilla- Hernandez R et al. Elf5 conditional knockout mice reveal its role as a master regulator in mammary alveolar development: Failure of Stat5 activation and functional differentiation in the absence of Elf5. Dev Biol 2009;329: 227-241.
49. Oakes SR, Naylor MJ, Asselin-Labat ML et al. The Ets transcription factor Elf5 specifies mammary alveolar cell fate. Genes Dev 2008;22:581-586.
50. Schupp M, Cristancho AG, Lefterova MI et al. Re-expression of GATA2 cooperates with peroxisome proliferator-activated receptor- gamma depletion to revert the adipocyte phenotype. J Biol Chem 2009;284:9458-9464.
51. Steger DJ, Grant GR, Schupp M et al. Propagation of adipogenic signals through an epigenomic transition state. Genes Dev 2010; 24:1035-1044.
52. Hennighausen L, Robinson GW. Information networks in the mammary gland. Nat Rev Mol Cell Biol 2005;6:715-725.
53. Nair BK, De Ome KB. A growthstimulating factor released by cultured mouse mammary tumor cells. Cancer Res 1973;33:2754-2760.
54. Ashburner M, Ball CA, Blake JA et al. Gene ontology: Tool for the unification of biology. The gene ontology consortium. Nat Genet 2000;25:25-29.
55. Kanehisa M, Goto S, Sato Y et al. KEGG for integration and interpretation of largescale molecular data sets. Nucleic Acids Res 2012;40(Database Issue):D109-D114.
56. Anderson SM, Rudolph MC, McManaman JL et al. Key stages in mammary gland development. Secretory activation in the mammary gland: It's not just about milk protein synthesis! Breast Cancer Res 2007;9:204.
57. Vastrik I, D'Eustachio P, Schmidt E et al. Reactome: A knowledge base of biologic pathways and processes. Genome Biol 2007;8:R39.
58. Morrison B, Cutler ML. The contribution of adhesion signaling to lactogenesis. J Cell Commun Signal 2010;4:131-139.
59. Andres AC, Djonov V. The mammary gland vasculature revisited. J Mammary Gland Biol Neoplasia 2010;15:319-328.
60. Akopian D, Shen K, Zhang X et al. Signal recognition particle: An essential proteintargeting machine. Annu Rev Biochem 2013; 82:693-721.
61. Nemir M, Bhattacharyya D, Li X et al. Targeted inhibition of osteopontin expression in the mammary gland causes abnormal morphogenesis and lactation deficiency. J Biol Chem 2000;275:969-976.
62. Rogers RL, Van S, I, Gould J et al. Transcript profiling of Elf51/-mammary glands during pregnancy identifies novel targets of Elf5. PLoS One 2010;5:e13150.
63. Miyauchi A, Alvarez J, Greenfield EM et al. Recognition of osteopontin and related peptides by an alpha v beta 3 integrin stimulates immediate cell signals in osteoclasts. J Biol Chem 1991;266:20369-20374.
64. Van KA, Rocha AS, Ousset M et al. Distinct stem cells contribute to mammary gland development and maintenance. Nature 2011;479:189-193.
65. Visvader JE, Smith GH. Murine mammary epithelial stem cells: Discovery, function, and current status. Cold Spring Harb Perspect Biol 2011;3.
66. Giordano A, Smorlesi A, Frontini A et al. White, brown and pink adipocytes: The extraordinary plasticity of the adipose organ. Eur J Endocrinol 2014.
67. Zaret KS, Carroll JS. Pioneer transcription factors: Establishing competence for gene expression. Genes Dev 2011;25:2227-2241.
68. Kouros-Mehr H, Slorach EM, Sternlicht MD et al. GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland. Cell 2006;127:1041-1055.
69. Tong Q, Dalgin G, Xu H et al. Function of GATA transcription factors in preadipocyteadipocyte transition. Science 2000;290:134-138.
70. Takahashi K, Tanabe K, Ohnuki M et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861-872.
71. Wapinski OL, Vierbuchen T, Qu K et al. Hierarchical mechanisms for direct reprogramming of fibroblasts to neurons. Cell 2013; 155:621-635.
72. Brandebourg T, Hugo E, Ben-Jonathan N. Adipocyte prolactin: Regulation of release and putative functions. Diabetes Obes Metab 2007;9:464-476.
73. Rodriguez-Cuenca S, Gianotti M, Roca P et al. Sex steroid receptor expression in different adipose depots is modified during midpregnancy. Mol Cell Endocrinol 2006;249: 58-63.
74. Rittling SR, Novick KE. Osteopontin expression in mammary gland development and tumorigenesis. Cell Growth Differ 1997; 8:1061-1069.
75. Hubbard NE, Chen QJ, Sickafoose LK et al. Transgenic mammary epithelial osteopontin (spp1) expression induces proliferation and alveologenesis. Genes Cancer 2013; 4:201-212.
76. Asselin-Labat ML, Sutherland KD, Barker H et al. Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation. Nat Cell Biol 2007;9:201-209.
77. Siegel PM, Muller WJ. Transcription factor regulatory networks in mammary epithelial development and tumorigenesis. Oncogene 2010;29:2753-2759.
78. Wolff G. I. Die Regeneration der Urodelenlinse. Entwicklungsphysiologische Studien. Wilhelm Roux' Arch 1895:380-390.
79. Jopling C, Boue S, Izpisua Belmonte JC. Dedifferentiation, transdifferentiation and reprogramming: Three routes to regeneration. Nat Rev Mol Cell Biol 2011;12:79-89.
80. Eguizabal C, Montserrat N, Veiga A et al. Dedifferentiation, transdifferentiation, and reprogramming: Future directions in regenerative medicine. Semin Reprod Med 2013;31: 82-94.
81. Ladewig J, Koch P, Brustle O. Leveling Waddington: The emergence of direct programming and the loss of cell fate hierarchies. Nat Rev Mol Cell Biol 2013;14:225-236.
82. Cristancho AG, Lazar MA. Forming functional fat: A growing understanding of adipocyte differentiation. Nat Rev Mol Cell Biol 2011;12:722-734.
83. Apostoli AJ, Skelhorne-Gross GE, Rubino RE et al. Loss of PPARgamma expression in mammary secretory epithelial cells creates a pro-breast tumorigenic environment. Int J Cancer 2014;134:1055-1066.