Gli1 promotes cell survival and is predictive of a poor outcome in ERα-negative breast cancer

Breast Cancer Research and Treatment

Volumn 123, Issue 1, 2010, Pages 59-71

  Xu, Lusheng ^a   Kwon, Yeon Jin ^a   Frolova, Natalya ^a   Steg, Adam D ^a   Yuan, Kun ^a   Johnson, Martin R ^b   Grizzle, William E ^a   Desmond, Renee A ^c   Frost, Andra R ^a  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

Breast; Cancer; Estrogen receptor ; Gli1; Prognosis

Indexed keywords

ANTIESTROGEN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR ALPHA; MESSENGER RNA; PROGESTERONE RECEPTOR; PROTEIN P53; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR GLI1; ESTRADIOL; ESTROGEN; GLI PROTEIN; ONCOPROTEIN; TRANSACTIVATOR PROTEIN;

ADULT; AGED; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER SURVIVAL; CELL GROWTH; CELL NUCLEUS; CELL PROLIFERATION; CELL STRAIN MCF 7; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MAJOR CLINICAL STUDY; OUTCOME ASSESSMENT; PREDICTION; PRIORITY JOURNAL; PROGNOSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; BREAST TUMOR; CANCER STAGING; DRUG EFFECTS; FEMALE; GENETICS; KAPLAN MEIER METHOD; METABOLISM; MIDDLE AGED; PATHOLOGY; TISSUE MICROARRAY; TREATMENT OUTCOME; TUMOR CELL LINE; VERY ELDERLY; WESTERN BLOTTING;

ADULT; AGED; AGED, 80 AND OVER; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; GENE EXPRESSION; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIERS ESTIMATE; MIDDLE AGED; NEOPLASM STAGING; ONCOGENE PROTEINS; PROGNOSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TISSUE ARRAY ANALYSIS; TRANS-ACTIVATORS; TREATMENT OUTCOME; KAPLAN-MEIER ESTIMATE;

EID: 77955770432     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-009-0617-5     Document Type: Article

References (61)

1. A Ruiz i Altaba C Mas B Stecca 2007 The Gli code: an information nexus regulating cell fate, stemness and cancer Trends Cell Biol 17 438 447 10.1016/j.tcb.2007.06.007 1:CAS:528:DC%2BD2sXhtFeiur%2FK 17845852 (Pubitemid 47505310)
2. ME Fernandez-Zapico 2008 Primers on molecular pathways GLI: more than just hedgehog? Pancreatology 8 227 229 10.1159/000134271 1:CAS:528: DC%2BD1cXntVCmsrw%3D 18497536 (Pubitemid 351832474)
3. RJ Lipinski JJ Gipp J Zhang JD Doles W Bushman 2006 Unique and complimentary activities of the Gli transcription factors in hedgehog signaling Exp Cell Res 312 1925 1938 10.1016/j.yexcr.2006.02.019 1:CAS:528: DC%2BD28Xls1Gqsrk%3D 16571352 (Pubitemid 43850919)
4. M Kasper G Regl AM Frischauf F Aberger 2006 GLI transcription factors: mediators of oncogenic hedgehog signalling Eur J Cancer 42 437 445 10.1016/j.ejca.2005.08.039 1:CAS:528:DC%2BD28XhsFOjsLg%3D 16406505 (Pubitemid 43227920)
5. S Dennler J Andre I Alexaki A Li T Magnaldo P ten Dijke XJ Wang F Verrecchia A Mauviel 2007 Induction of sonic hedgehog mediators by transforming growth factor-beta: Smad3-dependent activation of Gli2 and Gli1 expression in vitro and in vivo Cancer Res 67 6981 6986 10.1158/0008-5472.CAN-07-0491 1:CAS:528:DC%2BD2sXnslOit7c%3D 17638910 (Pubitemid 47105546)
6. H Schnidar M Eberl S Klingler D Mangelberger M Kasper C Hauser-Kronberger G Regl R Kroismayr R Moriggl M Sibilia F Aberger 2009 Epidermal growth factor receptor signaling synergizes with Hedgehog/GLI in oncogenic transformation via activation of the MEK/ERK/JUN pathway Cancer Res 69 1284 1292 10.1158/0008-5472.CAN-08-2331 1:CAS:528:DC%2BD1MXhslynsr4%3D 19190345
7. Z Ji FC Mei J Xie X Cheng 2007 Oncogenic KRAS activates hedgehog signaling pathway in pancreatic cancer cells J Biol Chem 282 14048 14055 10.1074/jbc.M611089200 1:CAS:528:DC%2BD2sXkvVygu7k%3D 17353198 (Pubitemid 47100411)
8. B Stecca C Mas V Clement M Zbinden R Correa V Piguet F Beermann IAA Ruiz 2007 Melanomas require HEDGEHOG-GLI signaling regulated by interactions between GLI1 and the RAS-MEK/AKT pathways Proc Natl Acad Sci USA 104 5895 5900 10.1073/pnas.0700776104 1:CAS:528:DC%2BD2sXkt1CqtLg%3D 17392427 (Pubitemid 47175630)
9. JM Ruppert B Vogelstein KW Kinzler 1991 The zinc finger protein GLI transforms primary cells in cooperation with adenovirus E1A Mol Cell Biol 11 1724 1728 1:CAS:528:DyaK3MXhtlOhsLw%3D 1825351
10. M Pasca di Magliano M Hebrok 2003 Hedgehog signalling in cancer formation and maintenance Nat Rev 3 903 911
11. DM Berman SS Karhadkar A Maitra R Montes De Oca MR Gerstenblith K Briggs AR Parker Y Shimada JR Eshleman DN Watkins PA Beachy 2003 Widespread requirement for hedgehog ligand stimulation in growth of digestive tract tumours Nature 425 846 851 10.1038/nature01972 1:CAS:528:DC%2BD3sXotlWqsLc%3D 14520411 (Pubitemid 37351469)
12. SS Karhadkar G Steven Bova N Abdallah S Dhara D Gardner A Maitra JT Isaacs DM Berman PA Beachy 2004 Hedgehog signalling in prostate regeneration, neoplasia and metastasis Nature 431 707 712 10.1038/nature02962 1:CAS:528:DC%2BD2cXotFGru74%3D 15361885 (Pubitemid 39382619)
13. H Kayed J Kleeff S Keleg J Guo K Ketterer PO Berberat N Giese I Esposito T Giese MW Buchler H Friess 2004 Indian hedgehog signaling pathway: expression and regulation in pancreatic cancer Int J Cancer 110 668 676 10.1002/ijc.20194 1:CAS:528:DC%2BD2cXkvFOksLw%3D 15146555 (Pubitemid 38746024)
14. DN Watkins DM Berman SG Burkholder B Wang PA Beachy SB Baylin 2003 Hedgehog signalling within airway epithelial progenitors and in small-cell lung cancer Nature 422 313 317 10.1038/nature01493 1:CAS:528:DC%2BD3sXitFKmu7s%3D 12629553 (Pubitemid 36378358)
15. SP Thayer MP di Magliano PW Heiser CM Nielsen DJ Roberts GY Lauwers YP Qi S Gysin C Fernandez-del Castillo V Yajnik B Antoniu M McMahon AL Warshaw M Hebrok 2003 Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis Nature 425 851 856 10.1038/nature02009 1:CAS:528: DC%2BD3sXotlWqsb8%3D 14520413 (Pubitemid 37355945)
16. Wolf I, Bose S, Desmond JC, Lin BT, Williamson EA, Karlan BY, Koeffler HP (2007) Unmasking of epigenetically silenced genes reveals DNA promoter methylation and reduced expression of PTCH in breast cancer. Breast Cancer Res Treat 105(2):139-155
17. X Ma K Chen S Huang X Zhang PA Adegboyega BM Evers H Zhang J Xie 2005 Frequent activation of the hedgehog pathway in advanced gastric adenocarcinomas Carcinogenesis 26 1698 1705 10.1093/carcin/bgi130 1:CAS:528:DC%2BD2MXhtVWnt7bO 15905200 (Pubitemid 41487985)
18. Ma X, Sheng T, Zhang Y, Zhang X, He J, Huang S, Chen K, Sultz J, Adegboyega PA, Zhang H, Xie J (2005) Hedgehog signaling is activated in subsets of esophageal cancers. Int J Cancer 118(1):139-148
19. D Qualtrough A Buda W Gaffield AC Williams C Paraskeva 2004 Hedgehog signalling in colorectal tumour cells: induction of apoptosis with cyclopamine treatment Int J Cancer 110 831 837 10.1002/ijc.20227 1:CAS:528: DC%2BD2cXkvFCmt70%3D 15170664 (Pubitemid 38758508)
20. Das S, Harris LG, Metge BJ, Liu S, Riker AI, Samant RS, Shevde LA (2009) The hedgehog pathway transcription factor, GLI1 promotes malignant behavior of cancer cells by upregulating osteopontin. J Biol Chem 284(34):22888-22897
21. S Mukherjee N Frolova A Sadlonova Z Novak A Steg GP Page DR Welch SM Lobo-Ruppert JM Ruppert MR Johnson AR Frost 2006 Hedgehog signaling and response to cyclopamine differs in epithelial and stromal cells in benign breast and breast cancer Cancer Biol Ther 5 674 683 1:CAS:528:DC%2BD28XpvFOhsbc%3D 16855373
22. Zhang X, Harrington N, Moraes RC, Wu MF, Hilsenbeck SG, Lewis MT (2009) Cyclopamine inhibition of human breast cancer cell growth independent of smoothened (Smo). Breast Cancer Res Treat 115(3):505-521
23. M Kubo M Nakamura A Tasaki N Yamanaka H Nakashima M Nomura S Kuroki M Katano 2004 Hedgehog signaling pathway is a new therapeutic target for patients with breast cancer Cancer Res 64 6071 6074 10.1158/0008-5472.CAN-04-0416 1:CAS:528:DC%2BD2cXntFClsL0%3D 15342389 (Pubitemid 39129406)
24. S Hatsell AR Frost 2007 Hedgehog signaling in mammary gland development and breast cancer J Mammary Gland Biol Neoplasia 12 163 173 10.1007/s10911-007- 9048-2 17623270 (Pubitemid 47215434)
25. S Liu G Dontu ID Mantle S Patel NS Ahn KW Jackson P Suri MS Wicha 2006 Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells Cancer Res 66 6063 6071 10.1158/0008-5472.CAN-06-0054 1:CAS:528:DC%2BD28XlvVSksrY%3D 16778178
26. RM Neve K Chin J Fridlyand J Yeh FL Baehner T Fevr L Clark N Bayani JP Coppe F Tong T Speed PT Spellman S DeVries A Lapuk NJ Wang WL Kuo JL Stilwell D Pinkel DG Albertson FM Waldman F McCormick RB Dickson MD Johnson M Lippman S Ethier A Gazdar JW Gray 2006 A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes Cancer Cell 10 515 527 10.1016/j.ccr.2006.10.008 1:CAS:528:DC%2BD28XhtlCnsrbE 17157791 (Pubitemid 44854747)
27. R Cailleau M Olive QV Cruciger 1978 Long-term human breast carcinoma cell lines of metastatic origin: preliminary characterization In vitro 14 911 915 10.1007/BF02616120 1:STN:280:DyaE1M%2FoslCqtQ%3D%3D 730202
28. AJ Hackett HS Smith EL Springer RB Owens WA Nelson-Rees JL Riggs MB Gardner 1977 Two syngeneic cell lines from human breast tissue: the aneuploid mammary epithelial (hs578t) and the diploid myoepithelial (hs578bst) cell lines J Natl Cancer Inst 58 1795 1806 1:STN:280:DyaE2s7ptVajuw%3D%3D 864756
29. M Lacroix G Leclercq 2004 Relevance of breast cancer cell lines as models for breast tumours: an update Breast Cancer Res Treat 83 249 289 10.1023/B:BREA.0000014042.54925.cc 1:CAS:528:DC%2BD2cXos1Cisw%3D%3D 14758095 (Pubitemid 38264873)
30. T Blick E Widodo H Hugo M Waltham ME Lenburg RM Neve EW Thompson 2008 Epithelial mesenchymal transition traits in human breast cancer cell lines Clin Exp Metastasis 25 629 642 10.1007/s10585-008-9170-6 1:STN:280: DC%2BD1cvltFelsA%3D%3D 18461285
31. TA Guise JJ Yin KS Mohammad 2003 Role of endothelin-1 in osteoblastic bone metastases Cancer 97 779 784 10.1002/cncr.11129 12548575
32. T Yoneda T Michigami B Yi PJ Williams M Niewolna T Hiraga 2000 Actions of bisphosphonate on bone metastasis in animal models of breast carcinoma Cancer 88 2979 2988 10.1002/1097-0142(20000615)88:12+<2979::AID-CNCR13>3.0.CO;2-U 1:CAS:528:DC%2BD3cXksVCmsL0%3D 10898341
33. RD Zhang IJ Fidler JE Price 1991 Relative malignant potential of human breast carcinoma cell lines established from pleural effusions and a brain metastasis Invasion Metastasis 11 204 215 1:STN:280:DyaK387ht1Citw%3D%3D 1765433
34. X Li W Deng CD Nail SK Bailey MH Kraus JM Ruppert SM Lobo-Ruppert 2006 Snail induction is an early response to Gli1 that determines the efficiency of epithelial transformation Oncogene 25 609 621 1:CAS:528:DC%2BD28XnsFSjsg%3D%3D 16158046
35. K Yanai S Nagai J Wada N Yamanaka M Nakamura N Torata H Noshiro M Tsuneyoshi M Tanaka M Katano 2007 Hedgehog signaling pathway is a possible therapeutic target for gastric cancer J Surg Oncol 95 55 62 10.1002/jso.20606 1:CAS:528:DC%2BD2sXhs12hs7o%3D 17192867 (Pubitemid 46122719)
36. H Kayed J Kleeff S Keleg MW Buchler H Friess 2003 Distribution of Indian hedgehog and its receptors patched and smoothened in human chronic pancreatitis J Endocrinol 178 467 478 10.1677/joe.0.1780467 1:CAS:528:DC%2BD3sXotFOhtrw%3D 12967338 (Pubitemid 37220173)
37. MK Thomas N Rastalsky JH Lee JF Habener 2000 Hedgehog signaling regulation of insulin production by pancreatic beta-cells Diabetes 49 2039 2047 10.2337/diabetes.49.12.2039 1:CAS:528:DC%2BD3cXos1ejs78%3D 11118005
38. LI Talley WE Grizzle JW Waterbor D Brown H Weiss AR Frost 2002 Hormone receptors and proliferation in breast carcinomas of equivalent histologic grades in pre- and postmenopausal women Int J Cancer 98 118 127 10.1002/ijc.10171 1:CAS:528:DC%2BD38Xht1Wgtr8%3D 11857395 (Pubitemid 34113428)
39. L Talley DC Chhieng WC Bell WE Grizzle AR Frost 2008 Immunohistochemical detection of egfr, p185(erbb-2), bcl-2 and p53 in breast carcinomas in pre-menopausal and post-menopausal women Biotech Histochem 83 5 14 10.1080/10520290701822436 1:CAS:528:DC%2BD1cXmsVWgs70%3D 18568671 (Pubitemid 351863899)
40. C Tapia K Glatz H Novotny A Lugli M Horcic CA Seemayer L Tornillo L Terracciano H Spichtin M Mirlacher R Simon G Sauter 2007 Close association between HER-2 amplification and overexpression in human tumors of non-breast origin Mod Pathol 20 192 198 10.1038/modpathol.3800729 1:CAS:528: DC%2BD2sXivVSlsb0%3D 17361205 (Pubitemid 46422173)
41. E Kaplan P Meier 1958 Nonparametric estimation from incomplete observations J Am Stat Assoc 53 457 481 10.2307/2281868
42. S Katayama K Ashizawa H Gohma T Fukuhara K Narumi Y Tsuzuki H Tatemoto T Nakada K Nagai 2006 The expression of hedgehog genes (ihh, dhh) and hedgehog target genes (ptc1, gli1, coup-tfii) is affected by estrogenic stimuli in the uterus of immature female rats Toxicol Appl Pharmacol 217 375 383 10.1016/j.taap.2006.10.003 1:CAS:528:DC%2BD28Xht12rsbjP 17109907 (Pubitemid 44855826)
43. K Koga M Nakamura H Nakashima T Akiyoshi M Kubo N Sato S Kuroki M Nomura M Tanaka M Katano 2008 Novel link between estrogen receptor alpha and hedgehog pathway in breast cancer Anticancer Res 28 731 740 1:CAS:528: DC%2BD1cXmt1eiurk%3D 18507014
44. O Nolan-Stevaux J Lau ML Truitt GC Chu M Hebrok ME Fernandez-Zapico D Hanahan 2009 GLI1 is regulated through smoothened-independent mechanisms in neoplastic pancreatic ducts and mediates PDAC cell survival and transformation Genes Dev 23 24 36 10.1101/gad.1753809 1:CAS:528:DC%2BD1MXptFWlsQ%3D%3D 19136624
45. C Kameda H Tanaka A Yamasaki M Nakamura K Koga N Sato M Kubo S Kuroki M Tanaka M Katano 2009 The hedgehog pathway is a possible therapeutic target for patients with estrogen receptor-negative breast cancer Anticancer Res 29 871 879 1:CAS:528:DC%2BD1MXltlOqtr0%3D 19414322
46. AJ Munro S Lain DP Lane 2005 P53 abnormalities and outcomes in colorectal cancer: a systematic review Br J Cancer 92 434 444 1:CAS:528: DC%2BD2MXhtFWntr0%3D 15668707
47. SJ Payne RL Bowen JL Jones CA Wells 2008 Predictive markers in breast cancer-the present Histopathology 52 82 90 1:STN:280:DC%2BD1c%2FosVGnsA%3D%3D 18171419
48. ML Helin MJ Helle HJ Helin JJ Isola 1989 Proliferative activity and steroid receptors determined by immunohistochemistry in adjacent frozen sections of 102 breast carcinomas Arch Pathol Lab Med 113 854 857 1:STN:280: DyaL1MzjsVGltA%3D%3D 2667495
49. Zhao J, Chen G, Cao D, Li Y, Diao F, Cai H, Jin Y, Lu J (2009) Expression of gli1 correlates with the transition of breast cancer cells to estrogen-independent growth. Breast Cancer Res Treat. doi: 10.1007/s10549-009- 0323-3
50. VG Keshamouni RR Mattingly KB Reddy 2002 Mechanism of 17-beta-estradiol-induced Erk1/2 activation in breast cancer cells. A role for HER2 and PKC-delta J Biol Chem 277 22558 22565 10.1074/jbc.M202351200 1:CAS:528:DC%2BD38XltVGktLo%3D 11960991 (Pubitemid 34967232)
51. H Tanaka M Nakamura C Kameda M Kubo N Sato S Kuroki M Tanaka M Katano 2009 The Hedgehog signaling pathway plays an essential role in maintaining the cd44+cd24- /low subpopulation and the side population of breast cancer cells Anticancer Res 29 2147 2157 1:CAS:528:DC%2BD1MXos1Wms7g%3D 19528475
52. M Al-Hajj MS Wicha A Benito-Hernandez SJ Morrison MF Clarke 2003 Prospective identification of tumorigenic breast cancer cells Proc Natl Acad Sci USA 100 3983 3988 10.1073/pnas.0530291100 1:CAS:528:DC%2BD3sXivFSqtbs%3D 12629218 (Pubitemid 36418143)
53. Bartkowiak K, Wieczorek M, Buck F, Harder S, Moldenhauer J, Effenberger KE, Pantel K, Peter-Katalinic J, Brandt BH (2009) Two-dimensional differential gel electrophoresis of a cell line derived from a breast cancer micrometastasis revealed a stem/progenitor cell protein profile. J Proteome Res 8(4):2004-2014
54. E Charafe-Jauffret C Ginestier F Iovino J Wicinski N Cervera P Finetti MH Hur ME Diebel F Monville J Dutcher M Brown P Viens L Xerri F Bertucci G Stassi G Dontu D Birnbaum MS Wicha 2009 Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature Cancer Res 69 1302 1313 10.1158/0008-5472.CAN-08-2741 1:CAS:528: DC%2BD1MXhslynsrw%3D 19190339
55. EM Hurt WL Farrar 2008 Cancer stem cells: the seeds of metastasis? Mol Interv 8 140 142 10.1124/mi.8.3.7 18693193
56. G Honeth PO Bendahl M Ringner LH Saal SK Gruvberger-Saal K Lovgren D Grabau M Ferno A Borg C Hegardt 2008 The cd44+/cd24- phenotype is enriched in basal-like breast tumors Breast Cancer Res 10 R53 10.1186/bcr2108 18559090
57. H Nakshatri EF Srour S Badve 2009 Breast cancer stem cells and intrinsic subtypes: controversies rage on Curr Stem Cell Res Ther 4 50 60 10.2174/157488809787169110 1:CAS:528:DC%2BD1MXkvVSgtLo%3D 19149630
58. EA Rakha IO Ellis 2009 Triple-negative/basal-like breast cancer: review Pathology 41 40 47 10.1080/00313020802563510 19089739
59. M Fiaschi B Rozell A Bergstrom R Toftgard 2009 Development of mammary tumors by conditional expression of GLI1 Cancer Res 69 4810 4817 10.1158/0008-5472.CAN-08-3938 1:CAS:528:DC%2BD1MXmsFGlu7k%3D 19458072
60. B Stecca A Ruiz i Altaba 2009 A GLI1-p53 inhibitory loop controls neural stem cell and tumour cell numbers EMBO J 28 663 676 10.1038/emboj.2009.16 1:CAS:528:DC%2BD1MXhslymsbY%3D 19214186
61. Y Abe E Oda-Sato K Tobiume K Kawauchi Y Taya K Okamoto M Oren N Tanaka 2008 Hedgehog signaling overrides p53-mediated tumor suppression by activating Mdm2 Proc Natl Acad Sci USA 105 4838 4843 10.1073/pnas.0712216105 1:CAS:528:DC%2BD1cXkt12qtL4%3D 18359851 (Pubitemid 351753833)