Sonic hedgehog-Gli1 signaling pathway regulates the Epithelial Mesenchymal Transition (EMT) by mediating a new target gene, S100A4, in pancreatic cancer cells

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Xu, Xuanfu ^a   Su, Bin ^a   Xie, Chuangao ^b   Wei, Shumei ^b   Zhou, Yingqun ^a   Liu, Hua ^a   Dai, Weiqi ^a   Cheng, Ping ^a   Wang, Fan ^a   Xu, Xiaorong ^a   Guo, Chuanyong ^a  

^a TONGJI UNIVERSITY   (China)

^b THE SECOND AFFILIATED HOSPITAL OF ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM BINDING PROTEIN; CALCYCLIN; CALVASCULIN; COMPLEMENTARY DNA; PROTEIN S100A11; PROTEIN S100A2; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; CADHERIN; GLI1 PROTEIN, HUMAN; PROTEIN BINDING; PROTEIN S 100; S100A4 PROTEIN, HUMAN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR;

ADULT; AGED; ARTICLE; BINDING SITE; CELL MIGRATION; CONTROLLED STUDY; DNA MICROARRAY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION; GENE TARGETING; GENETIC TRANSDUCTION; GLI1 GENE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTRACELLULAR SIGNALING; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; NUCLEOTIDE SEQUENCE; PANCREAS CANCER; PANCREATIC CANCER CELL LINE; PREDICTION; PROTEIN EXPRESSION; REGULATORY MECHANISM; S100A11 GENE; S100A2 GENE; S100A4 GENE; S100A6 GENE; SHH GENE; TUMOR INVASION; ANTAGONISTS AND INHIBITORS; CELL MOTION; DOWN REGULATION; GENETICS; HT 29 CELL LINE; METABOLISM; PANCREAS TUMOR; PATHOLOGY; PROMOTER REGION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR CELL LINE; UPREGULATION;

ADULT; AGED; BASE SEQUENCE; BINDING SITES; CADHERINS; CELL LINE, TUMOR; CELL MOVEMENT; DOWN-REGULATION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HEDGEHOG PROTEINS; HT29 CELLS; HUMANS; MALE; MIDDLE AGED; PANCREATIC NEOPLASMS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RNA INTERFERENCE; RNA, SMALL INTERFERING; S100 PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UP-REGULATION; VIMENTIN;

EID: 84905001546     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096441     Document Type: Article

References (42)

1. Bosetti C, Bertuccio P, Negri E, La Vecchia C, Zeegers MP (2012) Pancreatic cancer: overview of descriptive epidemiology. Mol Carcinog 51(1): 3-13.
2. Vincent A, Herman J, Schulick R, Hruban RH, Goggins M (2011) Pancreatic cancer. Lancet 378(9791): 607-620.
3. Loos M, Kleeff J, Friess H, Büchler MW (2008) Surgical treatment of pancreatic cancer. Ann N Y Acad Sci 1138: 169-180.
4. Lees C, Howie S, Sartor RB, Satsangi J (2005) The hedgehog signalling pathway in the gastrointestinal tract: implications for development, homeostasis, and disease. Gastroenterology 129(5): 1696-1710. (Pubitemid 41597408)
5. Parkin CA, Ingham PW (2008) The adventures of Sonic Hedgehog in development and repair. I. Hedgehog signaling in gastrointestinal development and disease. Am J Physiol Gastrointest Liver Physiol 294(2): G363-367. (Pubitemid 351253328)
6. Quint K, Stintzing S, Alinger B, Hauser-Kronberger C, Dietze O (2009) The expression pattern of PDX-1, SHH, Patched and Gli-1 is associated with pathological and clinical features in human pancreatic cancer. Pancreatology 9(1-2): 116-126.
7. Onishi H, Kai M, Odate S, Iwasaki H, Morifuji Y (2011) Hypoxia activates the hedgehog signaling pathway in a ligand-independent manner by upregulation of Smo transcription in pancreatic cancer. Cancer Sci 102(6): 1144-1150.
8. Carpenter RL, Lo HW (2012) Hedgehog pathway and GLI1 isoforms in human cancer. Discov Med 13(69): 105-113.
9. Tang SN, Fu J, Nall D, Rodova M, Shankar S (2012) Inhibition of sonic hedgehog pathway and pluripotency maintaining factors regulate human pancreatic cancer stem cell characteristics. Int J Cancer 131(1): 30-40.
10. Singh BN, Fu J, Srivastava RK, Shankar S (2011) Hedgehog signaling antagonist GDC-0449 (Vismodegib) inhibits pancreatic cancer stem cell characteristics: molecular mechanisms. PLoS One 6(11): e27306.
11. Li X, Ma Q, Xu Q, Liu H, Lei J (2012) SDF-1/CXCR4 signaling induces pancreatic cancer cell invasion and epithelial-mesenchymal transition in vitro through non-canonical activation of Hedgehog pathway. Cancer Lett 322(2): 169-176.
12. Bailey JM, Mohr AM, Hollingsworth MA (2009) Sonic hedgehog paracrine signaling regulates metastasis and lymphangiogenesis in pancreatic cancer. Oncogene 28(40): 3513-3525.
13. Feldmann G, Fendrich V, McGovern K, Bedja D, Bisht S (2008) An orally bioavailable small-molecule inhibitor of Hedgehog signaling inhibits tumor initiation and metastasis in pancreatic cancer. Mol Cancer Ther 7(9): 2725-2735.
14. Danilov AV, Neupane D, Nagaraja AS, Feofanova EV, Humphries LA (2011) DeltaNp63alpha-mediated induction of epidermal growth factor receptor promotes pancreatic cancer cell growth and chemoresistance. PLoS One 6(10): e26815.
15. Neupane D, Korc M (2008) 14-3-3sigma Modulates pancreatic cancer cell survival and invasiveness. Clin Cancer Res 14(23):7614-7623.
16. Li Z, Sclabas GM, Peng B, Hess KR, Abbruzzese JL (2004) Overexpression of synuclein-gamma in pancreatic adenocarcinoma. Cancer 101(1): 58-65.
17. Li D, Zhu J, Firozi PF, Abbruzzese JL, Evans DB (2003) Overexpression of oncogenic STK15/BTAK/Aurora A kinase in human pancreatic cancer. Clin Cancer Res 9(3):991-997. (Pubitemid 36323702)
18. Hejna M, Hamilton G, Brodowicz T, Haberl I, Fiebiger WC (2001) Serum levels of vasoactive intestinal peptide (VIP) in patients with adenocarcinomas of the gastrointestinal tract. Anticancer Res 21(2A):1183-1187.
19. Xu X, Zhou Y, Xie C, Wei SM, Gan H (2012) Genome-wide screening reveals an EMT molecular network mediated by Sonic hedgehog-Gli1 signaling in pancreatic cancer cells. PLoS One. 2012; 7(8): e43119.
20. Mencía N, Selga E, Rico I, de Almagro MC, Villalobos X (2010) Overexpression of S100A4 in human cancer cell lines resistant to methotrexate. BMC Cancer 10: 250.
21. Xu XF, Guo CY, Liu J, Yang WJ, Xia YJ (2009) Gli1 maintains cell survival by up-regulating IGFBP6 and Bcl-2 through promoter regions in parallel manner in pancreatic cancer cells. J Carcinog 8: 13.
22. Bigelow RL, Chari NS, Unden AB, Spurgers KB, Lee S (2004) Transcriptional regulation of bcl-2 mediated by the sonic hedgehog signaling pathway through gli-1. J Biol Chem 279: 1197-1205. (Pubitemid 38082643)
23. Loos M, Hedderich DM, Ottenhausen M, Giese NA, Laschinger M (2009) Expression of the costimulatory molecule B7-H3 is associated with prolonged survival in human pancreatic cancer. BMC Cancer 9: 463-473.
24. Yu M, Gipp J, Yoon JW, Iannaccone P, Walterhouse D (2009) Sonic hedgehogresponsive genes in the fetal prostate. J Biol Chem 284(9): 5620-5629.
25. Kasper M, Schnidar H, Neill GW, Hanneder M, Klingler S (2006) Selective modulation of Hedgehog/GLI target gene expression by epidermal growth factor signaling in human keratinocytes. Mol Cell Biol 26: 6283-6298. (Pubitemid 44204544)
26. Seidel K, Ahn CP, Lyons D, Nee A, Ting K (2010) Hedgehog signaling regulates the generation of ameloblast progenitors in the continuously growing mouse incisor. Development 137(22): 3753-3761.
27. Katoh Y, Katoh M (2009) Hedgehog target genes: mechanisms of carcinogenesis induced by aberrant hedgehog signaling activation. Curr Mol Med 9: 873-886.
28. Katoh Y, Katoh M (2008) Hedgehog signaling, epithelial-to-mesenchymal transition and miRNA (review). Int J Mol Med 22(3): 271-275.
29. Sipos B, Möser S, Kalthoff H, Török V, Löhr M (2003) A comprehensive characterization of pancreatic ductal carcinoma cell lines: towards the establishment of an in vitro research platform. Virchows Arch 442(5): 444-452. (Pubitemid 36718311)
30. Matthaios D, Zarogoulidis P, Balgouranidou I, Chatzaki E, Kakolyris S (2011) Molecular pathogenesis of pancreatic cancer and clinical perspectives. Oncology 81(3-4): 259-272.
31. Henry J, Toulza E, Hsu CY, Pellerin L, Balica S (2012) Update on the epidermal differentiation complex. Front Biosci 17: 1517-1532.
32. Nipp M, Elsner M, Balluff B, Meding S, Sarioglu H (2012) S100-A10, thioredoxin, and S100-A6 as biomarkers of papillary thyroid carcinoma with lymph node metastasis identified by MALDI imaging. J Mol Med (Berl) 90(2): 163-174.
33. Mishra SK, Siddique HR, Saleem M (2012) S100A4 calcium-binding protein is key player in tumor progression and metastasis: preclinical and clinical evidence. Cancer Metastasis Rev 31(1-2): 163-172.
34. Lukanidin E, Sleeman JP (2012) Building the niche: The role of the S100 proteins in metastatic growth. Semin Cancer Biol 22(3): 216-225.
35. Shang X, Cheng H, Zhou R (2008) Chromosomal mapping, differential origin and evolution of the S100 gene family. Genet Sel Evol 40(4): 449-464. (Pubitemid 351948158)
36. Ai KX, Lu LY, Huang XY, Chen W, Zhang HZ (2008) Prognostic significance of S100A4 and vascular endothelial growth factor expression in pancreatic cancer. World J Gastroenterol 14(12): 1931-1935. (Pubitemid 351523827)
37. Ikenaga N, Ohuchida K, Mizumoto K, Yu J, Fujita H (2009) S100A4 mRNA is a diagnostic and prognostic marker in pancreatic carcinoma. J Gastrointest Surg 13(10): 1852-1858.
38. Suemizu H, Monnai M, Ohnishi Y, Ito M, Tamaoki N (2007) Identification of a key molecular regulator of liver metastasis in human pancreatic carcinoma using a novel quantitative model of metastasis in NOD/SCID/gammacnull (NOG) mice. Int J Oncol 31(4): 741-751.
39. Ansari D, Rosendahl A, Elebro J, Andersson R (2011) Systematic review of immunohistochemical biomarkers to identify prognostic subgroups of patients with pancreatic cancer. Br J Surg 98(8): 1041-1055.
40. Zhang HY, Zheng XZ, Wang XH, Xuan XY, Wang F (2011) S100A4 mediated cell invasion and metastasis of esophageal squamous cell carcinoma via the regulation of MMP-2 and E-cadherin activity. Mol Biol Rep 2; 39: 199-208.
41. Boye K, Mælandsmo GM (2010) S100A4 and Metastasis A Small Actor Playing Many Roles. The American Journal of Pathology 176: 528-535.
42. Oida Y, Yamazaki H, Tobita K, Mukai M, Ohtani Y (2006) Increased S100A4 expression combined with decreased E-cadherin expression predicts a poor outcome of patients with pancreatic cancer. Oncol Rep 16(3): 457-463.