Shared signaling pathways in normal and breast cancer stem cells

Journal of Carcinogenesis

Volumn 10, Issue , 2011, Pages

  Malhotra, Gautam ^a   Zhao, Xiangshan ^a   Band, Hamid ^b   Band, Vimla ^b  

^a NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Cancer stem cell; hedgehog; mammary stem cell; notch; Wnt

Indexed keywords

NOTCH RECEPTOR; NOTCH1 RECEPTOR; NOTCH2 RECEPTOR; NOTCH3 RECEPTOR; NOTCH4 RECEPTOR; SONIC HEDGEHOG PROTEIN; WNT PROTEIN;

ARTICLE; BREAST CANCER; BREAST DEVELOPMENT; CANCER STEM CELL; CELL DIFFERENTIATION; CELL FATE; CELL INTERACTION; MOLECULAR INTERACTION; PROTEIN EXPRESSION; WNT SIGNALING PATHWAY;

EID: 84863955787     PISSN: 09746773     EISSN: 14773163     Source Type: Journal    
DOI: 10.4103/1477-3163.91413     Document Type: Article

References (89)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA: Cancer J Clin 2010;60:277-300.
2. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003;100:3983-8. (Pubitemid 36418143)
3. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70. (Pubitemid 30046295)
4. Simpson P. Developmental genetics. The Notch connection. Nature 1995;375:736-7.
5. Zhao Y, Katzman RB, Delmolino LM, Bhat I, Zhang Y, Gurumurthy CB, et al. The notch regulator MAML1 interacts with p53 and functions as a coactivator. J Biol Chem 2007;282:11969-81. (Pubitemid 47100726)
6. Ehebauer M, Hayward P, Martinez-Arias A. Notch signaling pathway. Sci STKE 2006;2006:cm7.
7. Ronchini C, Capobianco AJ. Induction of cyclin D1 transcription and CDK2 activity by Notch(ic): implication for cell cycle disruption in transformation by Notch(ic). Mol Cell Biol 2001;21:5925-34. (Pubitemid 32737809)
8. Rangarajan A, Talora C, Okuyama R, Nicolas M, Mammucari C, Oh H, et al. Notch signaling is a direct determinant of keratinocyte growth arrest and entry into differentiation. EMBO J 2001;20:3427-36. (Pubitemid 32634350)
9. Oswald F, Liptay S, Adler G, Schmid RM. NF-kappaB2 is a putative target gene of activated Notch-1 via RBP-Jkappa. Mol Cell Biol 1998;18:2077-88. (Pubitemid 28152657)
10. Palomero T, Lim WK, Odom DT, Sulis ML, Real PJ, Margolin A, et al. NOTCH1 directly regulates c-MYC and activates a feed-forward-loop transcriptional network promoting leukemic cell growth. Proc Natl Acad Sci USA 2006;103:18261-6. (Pubitemid 44871646)
11. Weng AP, Millholland JM, Yashiro-Ohtani Y, Arcangeli ML, Lau A, Wai C, et al. c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia/lymphoma. Genes Dev 2006;20:2096-109. (Pubitemid 44157460)
12. Harrison H, Farnie G, Howell SJ, Rock RE, Stylianou S, Brennan KR, et al. Regulation of breast cancer stem cell activity by signaling through the Notch4 receptor. Cancer Res 2010;70:709-18.
13. Raouf A, Zhao Y, To K, Stingl J, Delaney A, Barbara M, et al. Transcriptome analysis of the normal human mammary cell commitment and differentiation process. Cell Stem Cell 2008;3:109-18.
14. Leong KG, Niessen K, Kulic I, Raouf A, Eaves C, Pollet I, et al. Jagged1-mediated Notch activation induces epithelial-to-mesenchymal transition through Slug-induced repression of E-cadherin. J Exp Med 2007;204:2935-48. (Pubitemid 350179562)
15. Gudjonsson T, Villadsen R, Nielsen HL, Ronnov-Jessen L, Bissell MJ, Petersen OW. Isolation, immortalization, and characterization of a human breast epithelial cell line with stem cell properties. Genes Dev 2002;16:693-706. (Pubitemid 34274039)
16. Jhappan C, Gallahan D, Stahle C, Chu E, Smith GH, Merlino G, et al. Expression of an activated Notch-related int-3 transgene interferes with cell differentiation and induces neoplastic transformation in mammary and salivary glands. Genes Dev 1992;6:345-55.
17. Gallahan D, Callahan R. The mouse mammary tumor associated gene INT3 is a unique member of the NOTCH gene family (NOTCH4). Oncogene 1997;14:1883-90. (Pubitemid 27217801)
18. Gallahan D, Jhappan C, Robinson G, Hennighausen L, Sharp R, Kordon E, et al. Expression of a truncated Int3 gene in developing secretory mammary epithelium specifically retards lobular differentiation resulting in tumorigenesis. Cancer Res 1996;56:1775-85. (Pubitemid 26118213)
19. Uyttendaele H, Soriano JV, Montesano R, Kitajewski J. Notch4 and Wnt-1 proteins function to regulate branching morphogenesis of mammary epithelial cells in an opposing fashion. Dev Biol 1998;196:204-17. (Pubitemid 28198847)
20. Soriano JV, Uyttendaele H, Kitajewski J, Montesano R. Expression of an activated Notch4(int-3) oncoprotein disrupts morphogenesis and induces an invasive phenotype in mammary epithelial cells in vitro. Int J Cancer 2000;86:652-9. (Pubitemid 30249875)
21. Dontu G, Jackson KW, McNicholas E, Kawamura MJ, Abdallah WM, Wicha MS. Role of Notch signaling in cell-fate determination of human mammary stem/progenitor cells. Breast Cancer Res 2004;6:R605-15.
22. Gallahan D, Callahan R. Mammary tumorigenesis in feral mice: identification of a new int locus in mouse mammary tumor virus (Czech II)-induced mammary tumors. J Virol 1987;61:66-74. (Pubitemid 17212445)
23. Imatani A, Callahan R. Identification of a novel NOTCH-4/INT-3 RNA species encoding an activated gene product in certain human tumor cell lines. Oncogene 2000;19:223-31. (Pubitemid 30077218)
24. Farnie G, Clarke RB, Spence K, Pinnock N, Brennan K, Anderson NG, et al. Novel cell culture technique for primary ductal carcinoma in situ: Role of Notch and epidermal growth factor receptor signaling pathways. J Natl Cancer Inst 2007;99:616-27. (Pubitemid 47073543)
25. Stylianou S, Clarke RB, Brennan K. Aberrant activation of notch signaling in human breast cancer. Cancer Res 2006;66:1517-25. (Pubitemid 43259933)
26. Girard L, Hanna Z, Beaulieu N, Hoemann CD, Simard C, Kozak CA, et al. Frequent provirus insertional mutagenesis of Notch1 in thymomas of MMTVD/myc transgenic mice suggests a collaboration of c-myc and Notch1 for oncogenesis. Genes Dev 1996;10:1930-44. (Pubitemid 26281687)
27. Dievart A, Beaulieu N, Jolicoeur P. Involvement of Notch1 in the development of mouse mammary tumors. Oncogene 1999;18:5973-81. (Pubitemid 29535009)
28. Weijzen S, Rizzo P, Braid M, Vaishnav R, Jonkheer SM, Zlobin A, et al. Activation of Notch-1 signaling maintains the neoplastic phenotype in human Ras-transformed cells. Nat Med 2002;8:979-86. (Pubitemid 35033702)
29. Hu C, Dievart A, Lupien M, Calvo E, Tremblay G, Jolicoeur P. Overexpression of activated murine Notch1 and Notch3 in transgenic mice blocks mammary gland development and induces mammary tumors. Am J Pathol 2006;168:973-90. (Pubitemid 43327749)
30. Nusse R, Varmus HE. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell 1982;31:99-109.
31. Grigoryan T, Wend P, Klaus A, Birchmeier W. Deciphering the function of canonical Wnt signals in development and disease: Conditional loss-and gain-of-function mutations of beta-catenin in mice. Genes Dev 2008;22:2308-41.
32. Klaus A, Birchmeier W. Wnt signaling and its impact on development and cancer. Nat Rev Cancer 2008;8:387-98. (Pubitemid 351589714)
33. Angers S, Moon RT. Proximal events in Wnt signal transduction. Nat Rev Mol Cell Biol 2009;10:468-77.
34. He B, Reguart N, You L, Mazieres J, Xu Z, Lee AY, et al. Blockade of Wnt-1 signaling induces apoptosis in human colorectal cancer cells containing downstream mutations. Oncogene 2005;24:3054-8. (Pubitemid 40675537)
35. Tsukamoto AS, Grosschedl R, Guzman RC, Parslow T, Varmus HE. Expression of the int-1 gene in transgenic mice is associated with mammary gland hyperplasia and adenocarcinomas in male and female mice. Cell 1988;55:619-25.
36. Chu EY, Hens J, Andl T, Kairo A, Yamaguchi TP, Brisken C, et al. Canonical WNT signaling promotes mammary placode development and is essential for initiation of mammary gland morphogenesis. Development 2004;131:4819-29. (Pubitemid 39433468)
37. 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;295:219-31. (Pubitemid 44043115)
38. Lindvall C, Zylstra CR, Evans N, West RA, Dykema K, Furge KA, et al. The Wnt co-receptor Lrp6 is required for normal mouse mammary gland development. PLoS One 2009;4:e5813.
39. Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, et al. Purification and unique properties of mammary epithelial stem cells. Nature 2006;439:993-7. (Pubitemid 43292419)
40. 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;439:84-8. (Pubitemid 43053633)
41. Roelink H, Wagenaar E, Lopes da Silva S, Nusse R. Wnt-3, a gene activated by proviral insertion in mouse mammary tumors, is homologous to int-1/Wnt-1 and is normally expressed in mouse embryos and adult brain. Proc Natl Acad Sci USA 1990;87:4519-23.
42. Roelink H, Nusse R. Expression of two members of the Wnt family during mouse development-restricted temporal and spatial patterns in the developing neural tube. Genes Dev 1991;5:381-8. (Pubitemid 21905961)
43. Gavin BJ, McMahon AP. Differential regulation of the Wnt gene family during pregnancy and lactation suggests a role in postnatal development of the mammary gland. Mol Cell Biol 1992;12:2418-23.
44. Weber-Hall SJ, Phippard DJ, Niemeyer CC, Dale TC. Developmental and hormonal regulation of Wnt gene expression in the mouse mammary gland. Differentiation 1994;57:205-14. (Pubitemid 24296447)
45. Buhler TA, Dale TC, Kieback C, Humphreys RC, Rosen JM. Localization and quantification of Wnt-2 gene expression in mouse mammary development. Dev Biol 1993;155:87-96. (Pubitemid 23112048)
46. Kouros-Mehr H, Werb Z. Candidate regulators of mammary branching morphogenesis identified by genome-wide transcript analysis. Dev Dyn 2006;235:3404-12. (Pubitemid 44888206)
47. Bradbury JM, Edwards PA, Niemeyer CC, Dale TC. Wnt-4 expression induces a pregnancy-like growth pattern in reconstituted mammary glands in virgin mice. Dev Biol 1995;170:553-63.
48. Brisken C, Heineman A, Chavarria T, Elenbaas B, Tan J, Dey SK, et al. Essential function of Wnt-4 in mammary gland development downstream of progesterone signaling. Genes Dev 2000;14:650-4. (Pubitemid 30176819)
49. Imbert A, Eelkema R, Jordan S, Feiner H, Cowin P. Delta N89 beta-catenin induces precocious development, differentiation, and neoplasia in mammary gland. J Cell Biol 2001;153:555-68. (Pubitemid 34280142)
50. Brennan KR, Brown AM. Wnt proteins in mammary development and cancer. J Mammary Gland Biol Neoplasia 2004;9:119-31. (Pubitemid 39177498)
51. Bafico A, Liu G, Goldin L, Harris V, Aaronson SA.An autocrine mechanism for constitutive Wnt pathway activation in human cancer cells. Cancer Cell 2004;6:497-506. (Pubitemid 39469985)
52. Nagahata T, Shimada T, Harada A, Nagai H, Onda M, Yokoyama S, et al. Amplification, up-regulation and over-expression of DVL-1, the human counterpart of the Drosophila disheveled gene, in primary breast cancers. Cancer Sci 2003;94:515-8. (Pubitemid 36849715)
53. Ugolini F, Adelaide J, Charafe-Jauffret E, Nguyen C, Jacquemier J, Jordan B, et al. Differential expression assay of chromosome arm 8p genes identifies Frizzled-related (FRP1/FRZB) and Fibroblast Growth Factor Receptor 1 (FGFR1) as candidate breast cancer genes. Oncogene 1999;18:1903-10. (Pubitemid 29145858)
54. Virmani AK, Rathi A, Sathyanarayana UG, Padar A, Huang CX, Cunnigham HT, et al. Aberrant methylation of the adenomatous polyposis coli (APC) gene promoter 1A in breast and lung carcinomas. Clin Cancer Res 2001;7:1998-2004. (Pubitemid 32994838)
55. Furuuchi K, Tada M, Yamada H, Kataoka A, Furuuchi N, Hamada J, et al. Somatic mutations of the APC gene in primary breast cancers. Am J Pathol 2000;156:1997-2005. (Pubitemid 30641768)
56. Kuraguchi M, Ohene-Baah NY, Sonkin D, Bronson RT, Kucherlapati R. Genetic mechanisms in Apc-mediated mammary tumorigenesis. PLoS Genet 2009;5:e1000367.
57. Li Y, Welm B, Podsypanina K, Huang S, Chamorro M, Zhang X, et al. Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammary cancers from progenitor cells. Proc Natl Acad Sci USA 2003;100:15853-8. (Pubitemid 38021079)
58. Nusslein-Volhard C, Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature 1980;287:795-801. (Pubitemid 11214475)
59. McMahon AP, Ingham PW, Tabin CJ. Developmental roles and clinical significance of hedgehog signaling. Curr Top Dev Biol 2003;53:1-114. (Pubitemid 137639458)
60. Micchelli CA, The I, Selva E, Mogila V, Perrimon N. Rasp, a putative transmembrane acyltransferase, is required for Hedgehog signaling. Development 2002;129:843-51. (Pubitemid 34874109)
61. Kasper M, Regl G, Frischauf AM, Aberger F. GLI transcription factors: mediators of oncogenic Hedgehog signaling. Eur J Cancer 2006;42:437-45. (Pubitemid 43227920)
62. Michno K, Boras-Granic K, Mill P, Hui CC, Hamel PA. Shh expression is required for embryonic hair follicle but not mammary gland development. Dev Biol 2003;264:153-65. (Pubitemid 37393453)
63. Lewis MT, Ross S, Strickland PA, Sugnet CW, Jimenez E, Scott MP, et al. Defects in mouse mammary gland development caused by conditional haploinsufficiency of Patched-1. Development 1999;126:5181-93. (Pubitemid 30000430)
64. Gallego MI, Beachy PA, Hennighausen L, Robinson GW. Differential requirements for shh in mammary tissue and hair follicle morphogenesis. Dev Biol 2002;249:131-9.
65. Bitgood MJ, Shen L, McMahon AP. Sertoli cell signaling by Desert hedgehog regulates the male germline. Curr Biol 1996;6:298-304.
66. Moraes RC, Chang H, Harrington N, Landua JD, Prigge JT, Lane TF, et al. Ptch1 is required locally for mammary gland morphogenesis and systemically for ductal elongation. Development 2009;136:1423-32.
67. Li N, Singh S, Cherukuri P, Li H, Yuan Z, Ellisen LW, et al. Reciprocal intraepithelial interactions between TP63 and hedgehog signaling regulate quiescence and activation of progenitor elaboration by mammary stem cells. Stem Cells 2008;26:1253-64.
68. Goodrich LV, Milenkovic L, Higgins KM, Scott MP. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 1997;277:1109-13. (Pubitemid 27371635)
69. Hatsell SJ, Cowin P. Gli3-mediated repression of Hedgehog targets is required for normal mammary development. Development 2006;133:3661-70. (Pubitemid 44614288)
70. Park HL, Bai C, Platt KA, Matise MP, Beeghly A, Hui CC, et al. Mouse Gli1 mutants are viable but have defects in SHH signaling in combination with a Gli2 mutation. Development 2000;127:1593-605. (Pubitemid 30234917)
71. Lewis MT, Ross S, Strickland PA, Sugnet CW, Jimenez E, Hui C, et al. The Gli2 transcription factor is required for normal mouse mammary gland development. Dev Biol 2001;238:133-44. (Pubitemid 32939291)
72. Caro I, Low JA. The role of the hedgehog signaling pathway in the development of basal cell carcinoma and opportunities for treatment. Clin Cancer Res 2010;16:3335-9.
73. Xie J, Johnson RL, Zhang X, Bare JW, Waldman FM, Cogen PH, et al. Mutations of the PATCHED gene in several types of sporadic extracutaneous tumors. Cancer Res 1997;57:2369-72. (Pubitemid 27255892)
74. Vorechovsky I, Benediktsson KP, Toftgard R. The patched/hedgehog/ smoothened signaling pathway in human breast cancer: no evidence for H133Y SHH, PTCH and SMO mutations. Eur J Cancer 1999;35:711-3. (Pubitemid 29258138)
75. Wicking C, Evans T, Henk B, Hayward N, Simms LA, Chenevix-Trench G, et al. No evidence for the H133Y mutation in SONIC HEDGEHOG in a collection of common tumour types. Oncogene 1998;16:1091-3. (Pubitemid 28107947)
76. Naylor TL, Greshock J, Wang Y, Colligon T, Yu QC, Clemmer V, et al. High resolution genomic analysis of sporadic breast cancer using array-based comparative genomic hybridization. Breast Cancer Res 2005;7:R1186-98.
77. Xuan Y, Lin Z. Expression of Indian Hedgehog signaling molecules in breast cancer. J Cancer Res Clin Oncol 2009;135:235-40.
78. Wolf I, Bose S, Desmond JC, Lin BT, Williamson EA, Karlan BY, et al. Unmasking of epigenetically silenced genes reveals DNA promoter methylation and reduced expression of PTCH in breast cancer. Breast Cancer Res Treat 2007;105:139-55. (Pubitemid 47366878)
79. Moraes RC, Zhang X, Harrington N, Fung JY, Wu MF, Hilsenbeck SG, et al. Constitutive activation of smoothened (SMO) in mammary glands of transgenic mice leads to increased proliferation, altered differentiation and ductal dysplasia. Development 2007;134:1231-42. (Pubitemid 46630090)
80. Mukherjee S, Frolova N, Sadlonova A, Novak Z, Steg A, Page GP, et al. Hedgehog signaling and response to cyclopamine differ in epithelial and stromal cells in benign breast and breast cancer. Cancer Biol Ther 2006;5:674-83. (Pubitemid 44024723)
81. Visbal AP, Lewis MT. Hedgehog signaling in the normal and neoplastic mammary gland. Curr Drug Targets 2010;11:1103-11.
82. Fiaschi M, Rozell B, Bergstrom A, Toftgard R. Development of mammary tumors by conditional expression of GLI1. Cancer Res 2009;69:4810-7.
83. Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW, et al. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res 2006;66:6063-71.
84. Ma J, Meng Y, Kwiatkowski DJ, Chen X, Peng H, Sun Q, et al. Mammalian target of rapamycin regulates murine and human cell differentiation through STAT3/p63/Jagged/Notch cascade. J Clin Invest 2010;120:103-14.
85. Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, et al. Notch signaling regulates stem cell numbers in vitro and in vivo. Nature 2006;442:823-6. (Pubitemid 44258913)
86. Katoh Y, Katoh M. Hedgehog signaling, epithelial-to-mesenchymal transition and miRNA (review). Int J Mol Med 2008;22:271-5.
87. Lopez SL, Paganelli AR, Siri MV, Ocana OH, Franco PG, Carrasco AE. Notch activates sonic hedgehog and both are involved in the specification of dorsal midline cell-fates in Xenopus. Development 2003;130:2225-38. (Pubitemid 36656717)
88. He J, Sheng T, Stelter AA, Li C, Zhang X, Sinha M, et al. Suppressing Wnt signaling by the hedgehog pathway through sFRP-1. J Biol Chem 2006;281:35598-602. (Pubitemid 46041289)
89. Ayyanan A, Civenni G, Ciarloni L, Morel C, Mueller N, Lefort K, et al. Increased Wnt signaling triggers oncogenic conversion of human breast epithelial cells by a Notch-dependent mechanism. Proceedings of the National Academy of Sciences of the United States of America 2006;103:3799-804. (Pubitemid 43376635)