P130Cas alters the differentiation potential of mammary luminal progenitors by deregulating C-Kit activity

Stem Cells

Volumn 31, Issue 7, 2013, Pages 1422-1433

  Tornillo, Giusy ^a   Elia, Angela Rita ^a   Castellano, Isabella ^b   Spadaro, Michela ^a   Bernabei, Paola ^c   Bisaro, Brigitte ^a   Camacho Leal, Maria Del Pilar ^a   Pincini, Alessandra ^a   Provero, Paolo ^a   Sapino, Anna ^b   Turco, Emilia ^b   Defilippi, Paola ^a   Cabodi, Sara ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c CANDIOLO CANCER INSTITUTE   (Italy)

Author keywords

Basal like breast cancer; c Kit; Differentiation; Mammary luminal progenitor; p130Cas

Indexed keywords

CRK ASSOCIATED SUBSTRATE PROTEIN; PROLACTIN; STEM CELL FACTOR RECEPTOR;

ANIMAL CELL; ARTICLE; BASAL CELL; BREAST EPITHELIUM; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL FUNCTION; CONTROLLED STUDY; GENE OVEREXPRESSION; IN VITRO STUDY; NONHUMAN; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; TRANSGENIC ANIMAL;

BASAL-LIKE BREAST CANCER; C-KIT; DIFFERENTIATION; MAMMARY LUMINAL PROGENITOR; P130CAS;

ANIMALS; CELL DIFFERENTIATION; CELL GROWTH PROCESSES; CELLS, CULTURED; CRK-ASSOCIATED SUBSTRATE PROTEIN; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MAMMARY GLANDS, ANIMAL; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, TRANSGENIC; PREGNANCY; PROTO-ONCOGENE PROTEINS C-KIT; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST NEOPLASMS;

MUS MUSCULUS;

EID: 84879979916     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1403     Document Type: Article

References (50)

1. Moumen M, Chiche A, Cagnet S et al. The mammary myoepithelial cell. Int J Dev Biol 2011;55:763-771.
2. Sleeman KE, Kendrick H, Robertson D et al. Dissociation of estrogen receptor expression and in vivo stem cell activity in the mammary gland. J Cell Biol 2007;176:19-26.
3. Visvader JE. Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis. Genes Dev 2009;23:2563-2577.
4. Stingl J, Eirew P, Ricketson I et al. Purification and unique properties of mammary epithelial stem cells. Nature 2006;439:993-997.
5. Stingl J, Raouf A, Eirew P et al. Deciphering the mammary epithelial cell hierarchy. Cell Cycle 2006;5:1519-1522.
6. Asselin-Labat ML, Vaillant F, Shackleton M et al. Delineating the epithelial hierarchy in the mouse mammary gland. Cold Spring Harb Symp Quant Biol 2008;73:469-478.
7. Sleeman KE, Kendrick H, Ashworth A et al. CD24 staining of mouse mammary gland cells defines luminal epithelial, myoepithelial/basal and non-epithelial cells. Breast Cancer Res 2006;8:R7.
8. Kendrick H, Regan JL, Magnay FA et al. Transcriptome analysis of mammary epithelial subpopulations identifies novel determinants of lineage commitment and cell fate. BMC Genomics 2008;9:591.
9. Regan J, Smalley M. Prospective isolation and functional analysis of stem and differentiated cells from the mouse mammary gland. Stem Cell Rev 2007;3:124-136.
10. Stingl J. Detection and analysis of mammary gland stem cells. J Pathol 2009;217:229-241.
11. Visvader JE. Cells of origin in cancer. Nature 2011;469:314-322.
12. Pal SK, Childs BH, Pegram M. Triple negative breast cancer: Unmet medical needs. Breast Cancer Res Treat 2011;125:627-636.
13. Lim E, Vaillant F, Wu D et al. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med 2009;15:907-913.
14. Molyneux G, Geyer FC, Magnay FA et al. BRCA1 basal-like breast cancers originate from luminal epithelial progenitors and not from basal stem cells. Cell Stem Cell 2010;7:403-417.
15. Proia TA, Keller PJ, Gupta PB et al. Genetic predisposition directs breast cancer phenotype by dictating progenitor cell fate. Cell Stem Cell 2011;8:149-163.
16. Smart CE, Wronski A, French JD et al. Analysis of Brca1-deficient mouse mammary glands reveals reciprocal regulation of Brca1 and ckit. Oncogene 2011;30:1597-1607.
17. Regan JL, Kendrick H, Magnay FA et al. c-Kit is required for growth and survival of the cells of origin of Brca1-mutation-associated breast cancer. Oncogene 2012;31:869-883.
18. Tikhmyanova N, Little JL, Golemis EA. CAS proteins in normal and pathological cell growth control. Cell Mol Life Sci 2010;67: 1025-1048.
19. Defilippi P, Di Stefano P, Cabodi S. p130Cas: A versatile scaffold in signaling networks. Trends Cell Biol 2006;16:257-263.
20. Cabodi S, del Pilar Camacho-Leal M, Di Stefano P et al. Integrin signalling adaptors: Not only figurants in the cancer story. Nat Rev Cancer 2010;10:858-870.
21. Cabodi S, Tinnirello A, Di Stefano P et al. p130Cas as a new regulator of mammary epithelial cell proliferation, survival, and HER2-neu oncogene-dependent breast tumorigenesis. Cancer Res 2006;66: 4672-4680.
22. Cabodi S, Tinnirello A, Bisaro B et al. p130Cas is an essential transducer element in ErbB2 transformation. FASEB J 2010;24:3796-3808.
23. Tornillo G, Bisaro B, Camacho-Leal Mdel P et al. p130Cas promotes invasiveness of three-dimensional ErbB2-transformed mammary acinar structures by enhanced activation of mTOR/p70S6K and Rac1. Eur J Cell Biol 2011;90:237-248.
24. Hochgrafe F, Zhang L, O'Toole SA et al. Tyrosine phosphorylation profiling reveals the signaling network characteristics of Basal breast cancer cells. Cancer Res 2010;70:9391-9401.
25. Gordon KE, Binas B, Chapman RS et al. A novel cell culture model for studying differentiation and apoptosis in the mouse mammary gland. Breast Cancer Res 2000;2:222-235.
26. Lennartsson J, Ronnstrand L. Stem cell factor receptor/c-Kit: From basic science to clinical implications. Physiol Rev 2012;92: 1619-1649.
27. Welm BE, Dijkgraaf GJ, Bledau AS et al. Lentiviral transduction of mammary stem cells for analysis of gene function during development and cancer. Cell Stem Cell 2008;2:90-102.
28. Sapino A, Marchio C, Senetta R et al. Routine assessment of prognostic factors in breast cancer using a multicore tissue microarray procedure. Virchows Arch 2006;449:288-296.
29. Smalley MJ, Titley J, Paterson H et al. Differentiation of separated mouse mammary luminal epithelial and myoepithelial cells cultured on EHS matrix analyzed by indirect immunofluorescence of cytoskeletal antigens. J Histochem Cytochem 1999;47:1513-1524.
30. Shehata M, Teschendorff A, Sharp G et al. Phenotypic and functional characterization of the luminal cell hierarchy of the mammary gland. Breast Cancer Res 2012;14:R134.
31. Yalcin-Ozuysal O, Fiche M, Guitierrez M et al. Antagonistic roles of Notch and p63 in controlling mammary epithelial cell fates. Cell Death Differ 2010;17:1600-1612.
32. Li H, Cherukuri P, Li N et al. Nestin is expressed in the basal/myoepithelial layer of the mammary gland and is a selective marker of basal epithelial breast tumors. Cancer Res 2007;67:501-510.
33. DiRenzo J, Signoretti S, Nakamura N et al. Growth factor requirements and basal phenotype of an immortalized mammary epithelial cell line. Cancer Res 2002;62:89-98.
34. Dutt P, Wang JF, Groopman JE. Stromal cell-derived factor-1 alpha and stem cell factor/kit ligand share signaling pathways in hemopoietic progenitors: A potential mechanism for cooperative induction of chemotaxis. J Immunol 1998;161:3652-3658.
35. Gastaldi S, Sassi F, Accornero P et al. Met signaling regulates growth, repopulating potential and basal cell-fate commitment of mammary luminal progenitors: Implications for basal-like breast cancer. Oncogene 2013;32:1428-1440.
36. Bouras T, Pal B, Vaillant F et al. Notch signaling regulates mammary stem cell function and luminal cell-fate commitment. Cell Stem Cell 2008;3:429-441.
37. Balko JM, Miller TW, Morrison MM et al. The receptor tyrosine kinase ErbB3 maintains the balance between luminal and basal breast epithelium. Proc Natl Acad Sci USA 2012;109:221-226.
38. Kouros-Mehr H, Kim JW, Bechis SK et al. GATA-3 and the regulation of the mammary luminal cell fate. Curr Opin Cell Biol 2008;20: 164-170.
39. Chakrabarti R, Wei Y, Romano RA et al. Elf5 regulates mammary gland stem/progenitor cell fate by influencing notch signaling. Stem Cells 2012;30:1496-1508.
40. Carr JR, Kiefer MM, Park HJ et al. FoxM1 regulates mammary luminal cell fate. Cell Rep 2012;1:715-729.
41. Romano RA, Ortt K, Birkaya B et al. An active role of the DeltaN isoform of p63 in regulating basal keratin genes K5 and K14 and directing epidermal cell fate. PLoS One 2009;4:e5623.
42. Guo W, Keckesova Z, Donaher JL et al. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 2012;148:1015-1528.
43. Tikhmyanova N, Golemis EA. NEDD9 and BCAR1 negatively regulate E-cadherin membrane localization, and promote E-cadherin degradation. PLoS One 2011;6:e22102.
44. Bisaro B, Montani M, Konstantinidou G et al. p130Cas/Cyclooxygenase- 2 axis in the control of mesenchymal plasticity of breast cancer cells. Breast Cancer Res 2012;14:R137.
45. Mol CD, Dougan DR, Schneider TR et al. Structural basis for the autoinhibition and STI-571 inhibition of c-Kit tyrosine kinase. J Biol Chem 2004;279:31655-31663.
46. Roskoski R, Jr. Signaling by Kit protein-tyrosine kinase-The stem cell factor receptor. Biochem Biophys Res Commun 2005;337:1-13.
47. Toft DJ, Cryns VL. Minireview: Basal-like breast cancer: From molecular profiles to targeted therapies. Mol Endocrinol 2011;25: 199-211.
48. Turner N, Tutt A, Ashworth A. Hallmarks of 'BRCAness' in sporadic cancers. Nat Rev Cancer 2004;4:814-819.
49. Nielsen TO, Hsu FD, Jensen K et al. Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res 2004;10:5367-5374.
50. Simon R, Panussis S, Maurer R et al. KIT (CD117)-positive breast cancers are infrequent and lack KIT gene mutations. Clin Cancer Res 2004;10:178-183.