The role of NRG3 in mammary development

Journal of Mammary Gland Biology and Neoplasia

Volumn 13, Issue 2, 2008, Pages 195-203

  Howard, Beatrice A ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

Anlagen; ERBB4; Mammary gland development; NRG3; Placode

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 4; NEU DIFFERENTIATION FACTOR; NEU DIFFERENTIATION FACTOR 3; TRASTUZUMAB;

ARTICLE; BREAST CANCER; BREAST CELL; BREAST DEVELOPMENT; BREAST DUCT; BREAST EPITHELIUM; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CELL MIGRATION; CELL PROLIFERATION; DRUG TARGETING; GENE EXPRESSION; GENE FUNCTION; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; BREAST NEOPLASMS; CELL DIFFERENTIATION; FEMALE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAMMARY GLANDS, ANIMAL; MAMMARY GLANDS, HUMAN; MICE; PROTEIN ISOFORMS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 44149127678     PISSN: 10833021     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10911-008-9082-8     Document Type: Article

References (76)

1. Howard B, Panchal H, McCarthy A, Ashworth A. Identification of the scaramanga gene implicates Neuregulin3 in mammary gland specification. Genes Dev. 2005;19(17):2078-90.
2. Tidcombe H, Jackson-Fisher A, Mathers K, Stern DF, Gassmann M, Golding JP. Neural and mammary gland defects in ErbB4 knockout mice genetically rescued from embryonic lethality. Proc Natl Acad Sci USA. 2003;100(14):8281-6.
3. Long W, Wagner KU, Lloyd KC, Binart N, Shillingford JM, Hennighausen L, et al. Impaired differentiation and lactational failure of Erbb4-deficient mammary glands identify ERBB4 as an obligate mediator of STAT5. Development. 2003;130(21):5257-68.
4. Propper AY. Wandering epithelial cells in the rabbit embryo milk line. A preliminary scanning electron microscope study. Dev Biol. 1978;67(1):225-31.
5. Balinsky BI. On the prenatal growth of the mammary gland rudiment in the mouse. J Anat. 1950;84(3):227-35.
6. Lechler T, Fuchs E. Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature. 2005;437(7056):275-80.
7. Smart IH. Variation in the plane of cell cleavage during the process of stratification in the mouse epidermis. Br J Dermatol. 1970;82(3):276-82.
8. Sakakura T. Mammary embryogenesis. In: Daniel MCNACW, editor. The mammary gland. Development, regulation, and function. New York: Plenum Press; 1987.
9. Cunha GR, Hom YK. Role of mesenchymal-epithelial interactions in mammary gland development. J Mammary Gland Biol Neoplasia. 1996;1(1):21-35.
10. Blanpain C, Fuchs E. Epidermal stem cells of the skin. Annu Rev Cell Dev Biol. 2006;22:339-73.
11. Mikkola ML, Millar SE. The mammary bud as a skin appendage: Unique and shared aspects of development. J Mammary Gland Biol Neoplasia. 2006;11(3-4):187-203.
12. Olivera-Martinez I, Thelu J, Dhouailly D. Molecular mechanisms controlling dorsal dermis generation from the somitic dermomyotome. Int J Dev Biol. 2004;48(2-3):93-101.
13. Watt FM, Lo Celso C, Silva-Vargas V. Epidermal stem cells: An update. Curr Opin Genet Dev. 2006;16(5):518-24.
14. Kratochwil K. Development and loss of androgen responsiveness in the embryonic rudiment of the mouse mammary gland. Dev Biol. 1977;61(2):358-65.
15. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, et al. Generation of a functional mammary gland from a single stem cell. Nature. 2006;439(7072):84-8.
16. Deome KB, Faulkin LJ Jr, Bern HA, Blair PB. Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice. Cancer Res. 1959;19(5):515-20.
17. Kordon EC, Smith GH. An entire functional mammary gland may comprise the progeny from a single cell. Development. 1998;125(10):1921-30.
18. Boulanger CA, Mack DL, Booth BW, Smith GH. Interaction with the mammary microenvironment redirects spermatogenic cell fate in vivo. Proc Natl Acad Sci USA 2007;104(10):3871-6.
19. Panchal H, Wansbury O, Parry S, Ashworth A, Howard B. Neuregulin3 alters cell fate in the epidermis and mammary gland. BMC Dev Biol. 2007;7(1):105.
20. Boras-Granic K, Chang H, Grosschedl R, Hamel PA. Lef1 is required for the transition of Wnt signaling from mesenchymal to epithelial cells in the mouse embryonic mammary gland. Dev Biol. 2006.
21. Mailleux AA, Spencer-Dene B, Dillon C, Ndiaye D, Savona-Baron C, Itoh N, et al. Role of FGF10/FGFR2b signaling during mammary gland development in the mouse embryo. Development. 2002;129(1):53-60.
22. Veltmaat JM, Relaix F, Le LT, Kratochwil K, Sala FG, van Veelen W, et al. Gli3-mediated somitic Fgf10 expression gradients are required for the induction and patterning of mammary epithelium along the embryonic axes. Development. 2006;133(12):2325-35.
23. Hatsell SJ, Cowin P. Gli3-mediated repression of Hedgehog targets is required for normal mammary development. Development. 2006;133(18):3661-70.
24. Cunha GR, Young P, Christov K, Guzman R, Nandi S, Talamantes F, et al. Mammary phenotypic expression induced in epidermal cells by embryonic mammary mesenchyme. Acta Anat (Basel). 1995;152(3):195-204.
25. Propper A, Gomot L. [Tissue interactions during organogenesis of the mammary gland in the rabbit embryo]. C R Acad Sci Hebd Seances Acad Sci D. 1967;264(22):2573-5.
26. Robinson GW. Cooperation of signalling pathways in embryonic mammary gland development. Nat Rev Genet. 2007;8(12):963-72.
27. Waikel RL, Kawachi Y, Waikel PA, Wang XJ, Roop DR. Deregulated expression of c-Myc depletes epidermal stem cells. Nat Genet. 2001;28(2):165-8.
28. Frye M, Gardner C, Li ER, Arnold I, Watt FM. Evidence that Myc activation depletes the epidermal stem cell compartment by modulating adhesive interactions with the local microenvironment. Development. 2003;130(12):2793-808.
29. Arnold I, Watt FM. c-Myc activation in transgenic mouse epidermis results in mobilization of stem cells and differentiation of their progeny. Curr Biol. 2001;11(8):558-68.
30. Smalley M, Ashworth A. Stem cells and breast cancer: A field in transit. Nat Rev Cancer. 2003;3(11):832-44.
31. Zhang D, Sliwkowski MX, Mark M, Frantz G, Akita R, Sun Y, et al. Neuregulin-3 (NRG3): A novel neural tissue-enriched protein that binds and activates ErbB4. Proc Natl Acad Sci USA. 1997;94(18):9562-7.
32. Muraoka-Cook RS, Sandahl M, Husted C, Hunter D, Miraglia L, Feng SM, et al. The intracellular domain of ErbB4 induces differentiation of mammary epithelial cells. Mol Biol Cell. 2006;17(9):4118-29.
33. Williams CC, Allison JG, Vidal GA, Burow ME, Beckman BS, Marrero L, et al. The ERBB4/HER4 receptor tyrosine kinase regulates gene expression by functioning as a STAT5A nuclear chaperone. J Cell Biol. 2004;167(3):469-78.
34. Srinivasan R, Poulsom R, Hurst HC, Gullick WJ. Expression of the c-erbB-4/HER4 protein and mRNA in normal human fetal and adult tissues and in a survey of nine solid tumour types. J Pathol. 1998;185(3):236-45.
35. Gullick WJ. c-erbB-4/HER4: Friend or foe. J Pathol. 2003;200(3):279-81.
36. Aubele M, Auer G, Walch AK, Munro A, Atkinson MJ, Braselmann H, et al. PTK (protein tyrosine kinase)-6 and HER2 and 4, but not HER1 and 3 predict long-term survival in breast carcinomas. Br J Cancer. 2007;96(5):801-7.
37. Maatta JA, Sundvall M, Junttila TT, Peri L, Laine VJ, Isola J, et al. Proteolytic cleavage and phosphorylation of a tumor-associated ErbB4 isoform promote ligand-independent survival and cancer cell growth. Mol Biol Cell. 2006;17(1):67-79.
38. Junttila TT, Sundvall M, Lundin M, Lundin J, Tanner M, Harkonen P, et al. Cleavable ErbB4 isoform in estrogen receptor-regulated growth of breast cancer cells. Cancer Res. 2005;65(4):1384-93.
39. Citri A, Yarden Y. EGF-ERBB signalling: Towards the systems level. Nat Rev Mol Cell Biol. 2006;7(7):505-16.
40. Gizatullin RZ, Muravenko OV, Al-Amin AN, Wang F, Protopopov AI, Kashuba VI, et al. Human NRG3 gene Map position 10q22-q23. Chromosome Res. 2000;8(6):560.
41. Assimacopoulos S, Grove EA, Ragsdale CW. Identification of a Pax6-dependent epidermal growth factor family signaling source at the lateral edge of the embryonic cerebral cortex. J Neurosci. 2003;23(16):6399-403.
42. Anton ES, Ghashghaei HT, Weber JL, McCann C, Fischer TM, Cheung ID, et al. Receptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain. Nat Neurosci. 2004;7(12):1319-28.
43. Golding JP, Trainor P, Krumlauf R, Gassmann M. Defects in pathfinding by cranial neural crest cells in mice lacking the neuregulin receptor ErbB4. Nat Cell Biol. 2000;2(2):103-9.
44. Balciuniene J, Feng N, Iyadurai K, Hirsch B, Charnas L, Bill BR, et al. Recurrent 10q22-q23 deletions: A genomic disorder on 10q associated with cognitive and behavioral abnormalities. Am J Hum Genet. 2007;80(5):938-47.
45. Benzel I, Bansal A, Browning BL, Galwey NW, Maycox PR, McGinnis R, et al. Interactions among genes in the ErbB-Neuregulin signalling network are associated with increased susceptibility to schizophrenia. Behav Brain Funct. 2007;3:31.
46. Law AJ, Kleinman JE, Weinberger DR, Weickert CS. Disease-associated intronic variants in the ErbB4 gene are related to altered ErbB4 splice-variant expression in the brain in schizophrenia. Hum Mol Genet. 2007;16(2):129-41.
47. Stefansson H, Sigurdsson E, Steinthorsdottir V, Bjornsdottir S, Sigmundsson T, Ghosh S, et al. Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet. 2002;71(4):877-92.
48. Eriksson PS. Schizophrenia - a stem cell disorder. Exp Neurol. 2006;199(1):26-7.
49. Carteron C, Ferrer-Montiel A, Cabedo H. Characterization of a neural-specific splicing form of the human neuregulin 3 gene involved in oligodendrocyte survival. J Cell Sci. 2006;119(Pt 5):898-909.
50. Li L, Cleary S, Mandarano MA, Long W, Birchmeier C, Jones FE. The breast proto-oncogene, HRGalpha regulates epithelial proliferation and lobuloalveolar development in the mouse mammary gland. Oncogene. 2002;21(32):4900-7.
51. Rio C, Buxbaum JD, Peschon JJ, Corfas G. Tumor necrosis factor-alpha-converting enzyme is required for cleavage of erbB4/HER4. J Biol Chem. 2000;275(14):10379-87.
52. Elenius K, Choi CJ, Paul S, Santiestevan E, Nishi E, Klagsbrun M. Characterization of a naturally occurring ErbB4 isoform that does not bind or activate phosphatidyl inositol 3-kinase. Oncogene. 1999;18(16):2607-15.
53. Zeng F, Zhang MZ, Singh AB, Zent R, Harris RC. ErbB4 isoforms selectively regulate growth factor induced Madin-Darby canine kidney cell tubulogenesis. Mol Biol Cell. 2007;18(11):4446-56.
54. Jones JT, Akita RW, Sliwkowski MX. Binding specificities and affinities of egf domains for ErbB receptors. FEBS Lett. 1999;447(2-3):227-31.
55. Mautino B, Dalla Costa L, Gambarotta G, Perroteau I, Fasolo A, Dati C. Bioactive recombinant neuregulin-1, -2, and -3 expressed in Escherichia coli. Protein Expr Purif. 2004;35(1):25-31.
56. Sweeney C, Lai C, Riese DJ 2nd, Diamonti AJ, Cantley LC, Carraway KL 3rd. Ligand discrimination in signaling through an ErbB4 receptor homodimer. J Biol Chem. 2000;275(26):19803-7.
57. Hobbs SS, Coffing SL, Le AT, Cameron EM, Williams EE, Andrew M, et al. Neuregulin isoforms exhibit distinct patterns of ErbB family receptor activation. Oncogene. 2002;21(55):8442-52.
58. Hijazi MM, Young PE, Dougherty MK, Bressette DS, Cao TT, Pierce JH, et al. NRG-3 in human breast cancers: Activation of multiple erbB family proteins. Int J Oncol. 1998;13(5):1061-7.
59. Nanba D, Nakanishi Y, Hieda Y. Changes in adhesive properties of epithelial cells during early morphogenesis of the mammary gland. Dev Growth Differ. 2001;43(5):535-44.
60. Katz E, Streuli CH. The extracellular matrix as an adhesion checkpoint for mammary epithelial function. Int J Biochem Cell Biol. 2007;39(4):715-26.
61. Guo W, Pylayeva Y, Pepe A, Yoshioka T, Muller WJ, Inghirami G, et al. Beta 4 integrin amplifies ErbB2 signaling to promote mammary tumorigenesis. Cell. 2006;126(3):489-502.
62. Bon G, Folgiero V, Di Carlo S, Sacchi A, Falcioni R. Involvement of alpha6beta4 integrin in the mechanisms that regulate breast cancer progression. Breast Cancer Res. 2007;9(1):203.
63. Lahlou H, Sanguin-Gendreau V, Zuo D, Cardiff RD, McLean GW, Frame MC, et al. Mammary epithelial-specific disruption of the focal adhesion kinase blocks mammary tumor progression. Proc Natl Acad Sci U S A. 2007.
64. Kanakry CG, Li Z, Nakai Y, Sei Y, Weinberger DR. Neuregulin-1 Regulates Cell Adhesion via an ErbB2/Phosphoinositide-3 Kinase/Akt-Dependent Pathway: Potential Implications for Schizophrenia and Cancer. PLoS ONE. 2007;2(12):e1369.
65. Nie S, Chang C. PI3K and Erk MAPK mediate ErbB signaling in Xenopus gastrulation. Mech Dev. 2007;124(9-10):657-67.
66. Nie S, Chang C. Regulation of Xenopus gastrulation by ErbB signaling. Dev Biol. 2007;303(1):93-107.
67. Wansbury O, Panchal H, James M, Parry S, Ashworth A, Howard B. Dynamic expression of Erbb pathway members during early mammary gland morphogenesis. J Invest Dermatol. 2008;128(4):1009-21.
68. Britsch S. The neuregulin-I/ErbB signaling system in development and disease. Adv Anat Embryol Cell Biol. 2007;190:1-65.
69. Dunn M, Sinha P, Campbell R, Blackburn E, Levinson N, Rampaul R, et al. Co-expression of neuregulins 1, 2, 3 and 4 in human breast cancer. J Pathol. 2004;203(2):672-80.
70. Marshall C, Blackburn E, Clark M, Humphreys S, Gullick WJ. Neuregulins 1-4 are expressed in the cytoplasm or nuclei of ductal carcinoma (in situ) of the human breast. Breast Cancer Res Treat. 2006;96(2):163-8.
71. Bieche I, Onody P, Tozlu S, Driouch K, Vidaud M, Lidereau R. Prognostic value of ERBB family mRNA expression in breast carcinomas. Int J Cancer. 2003;106(5):758-65.
72. Revillion F, Lhotellier V, Hornez L, Bonneterre J, Peyrat JP. ErbB/HER ligands in human breast cancer, and relationships with their receptors, the bio-pathological features and prognosis. Ann Oncol. 2008;19(1):73-80.
73. de Alava E, Ocana A, Abad M, Montero JC, Esparis-Ogando A, Rodriguez CA, et al. Neuregulin expression modulates clinical response to trastuzumab in patients with metastatic breast cancer. J Clin Oncol. 2007;25(19):2656-63.
74. Breuleux M. Role of heregulin in human cancer. Cell Mol Life Sci. 2007;64(18):2358-77.
75. Zahnow CA. ErbB receptors and their ligands in the breast. Expert Rev Mol Med. 2006;8(23):1-21.
76. Howard B, Ashworth A. Signalling pathways implicated in early mammary gland morphogenesis and breast cancer. PLoS Genet. 2006;2(8):e112.