Nuclear translocation of FGFR1 and FGF2 in pancreatic stellate cells facilitates pancreatic cancer cell invasion

EMBO Molecular Medicine

Volumn 6, Issue 4, 2014, Pages 467-481

  Coleman, Stacey J ^a   Chioni, Athina Myrto ^a   Ghallab, Mohammed ^a   Anderson, Rhys K ^a   Lemoine, Nicholas R ^a   Kocher, Hemant M ^a,b   Grose, Richard P ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b ROYAL LONDON HOSPITAL   (United Kingdom)

Author keywords

FGF signalling; Human cancer; Invasion; Organotypic cultures

Indexed keywords

1 TERT BUTYL 3 [6 (3,5 DIMETHOXYPHENYL) 2 (4 DIETHYLAMINOBUTYLAMINO)PYRIDO[2,3 D]PYRIMIDIN 7 YL]UREA; ALPHA SMOOTH MUSCLE ACTIN; CYCLIN D1; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 1; LAMIN A; LAMIN C; MITOGEN ACTIVATED PROTEIN KINASE; TUBULIN; VIMENTIN;

ARTICLE; CANCER CELL; CELL COUNT; CELL FRACTIONATION; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SPACE; MYOFIBROBLAST; PANCREAS CANCER; PANCREATIC STELLATE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TUMOR INVASION; TUMOR MICROENVIRONMENT; WESTERN BLOTTING; CELL NUCLEUS; ENZYMOLOGY; GENETICS; METABOLISM; PANCREAS TUMOR; PATHOLOGY; PATHOPHYSIOLOGY; PROTEIN TRANSPORT; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL NUCLEUS; CELL PROLIFERATION; FIBROBLAST GROWTH FACTOR 2; HUMANS; NEOPLASM INVASIVENESS; PANCREATIC NEOPLASMS; PANCREATIC STELLATE CELLS; PROTEIN TRANSPORT; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; TUMOR MICROENVIRONMENT;

EID: 84897413643     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201302698     Document Type: Article

References (55)

1. Apte MV, Haber PS, Applegate TL, Norton ID, McCaughan GW, Korsten MA, Pirola RC, Wilson JS (1998) Periacinar stellate shaped cells in rat pancreas: identification, isolation, and culture. Gut 43: 128-133
2. Apte MV, Haber PS, Darby SJ, Rodgers SC, McCaughan GW, Korsten MA, Pirola RC, Wilson JS (1999) Pancreatic stellate cells are activated by proinflammatory cytokines: implications for pancreatic fibrogenesis. Gut 44: 534-541
3. Apte MV, Park S, Phillips PA, Santucci N, Goldstein D, Kumar RK, Ramm GA, Buchler M, Friess H, McCarroll JA et al (2004) Desmoplastic reaction in pancreatic cancer: role of pancreatic stellate cells. Pancreas 29: 179-187
4. Bachem MG, Schunemann M, Ramadani M, Siech M, Beger H, Buck A, Zhou S, Schmid-Kotsas A, Adler G (2005) Pancreatic carcinoma cells induce fibrosis by stimulating proliferation and matrix synthesis of stellate cells. Gastroenterology 128: 907-921
5. Bouche G, Gas N, Prats H, Baldin V, Tauber JP, Teissie J, Amalric F (1987) Basic fibroblast growth factor enters the nucleolus and stimulates the transcription of ribosomal genes in ABAE cells undergoing G0-G1 transition. Proc Natl Acad Sci USA 84: 6770-6774
6. Bryant DM, Wylie FG, Stow JL (2005) Regulation of endocytosis, nuclear translocation, and signaling of fibroblast growth factor receptor 1 by E-cadherin. Mol Biol Cell 16: 14-23
7. Bugler B, Caizergues-Ferrer M, Bouche G, Bourbon H, Amalric F (1982) Detection and localization of a class of proteins immunologically related to a 100-kDa nucleolar protein. Eur J Biochem 128: 475-480
8. Chen G, Tian X, Liu Z, Zhou S, Schmidt B, Henne-Bruns D, Bachem M, Kornmann M (2010) Inhibition of endogenous SPARC enhances pancreatic cancer cell growth: modulation by FGFR1-III isoform expression. Br J Cancer 102: 188-195
9. Chioni AM, Grose R (2012) FGFR1 cleavage and nuclear translocation regulates breast cancer cell behavior. J Cell Biol 197: 801-817
10. Clarke WE, Berry M, Smith C, Kent A, Logan A (2001) Coordination of fibroblast growth factor receptor 1 (FGFR1) and fibroblast growth factor-2 (FGF-2) trafficking to nuclei of reactive astrocytes around cerebral lesions in adult rats. Mol Cell Neurosci 17: 17-30
11. Corson LB, Yamanaka Y, Lai KM, Rossant J (2003) Spatial and temporal patterns of ERK signaling during mouse embryogenesis. Development 130: 4527-4537
12. Coupland VH, Kocher HM, Berry DP, Allum W, Linklater KM, Konfortion J, Moller H, Davies EA (2012) Incidence and survival for hepatic, pancreatic and biliary cancers in England between 1998 and 2007. Cancer Epidemiol 36: e207-e214
13. Crispino JD, Blencowe BJ, Sharp PA (1994) Complementation by SR proteins of pre-mRNA splicing reactions depleted of U1 snRNP. Science 265: 1866-1869
14. Dunham-Ems SM, Lee YW, Stachowiak EK, Pudavar H, Claus P, Prasad PN, Stachowiak MK (2009) Fibroblast growth factor receptor-1 (FGFR1) nuclear dynamics reveal a novel mechanism in transcription control. Mol Biol Cell 20: 2401-2412
15. Erkan M, Adler G, Apte MV, Bachem MG, Buchholz M, Detlefsen S, Esposito I, Friess H, Gress TM, Habisch HJ et al (2012) StellaTUM: current consensus and discussion on pancreatic stellate cell research. Gut 61: 172-178
16. Froeling FE, Feig C, Chelala C, Dobson R, Mein CE, Tuveson DA, Clevers H, Hart IR, Kocher HM (2011) Retinoic acid-induced pancreatic stellate cell quiescence reduces paracrine Wnt-beta-catenin signaling to slow tumor progression. Gastroenterology 141: 1486-1497, 1497 e1481-1414
17. Froeling FE, Mirza TA, Feakins RM, Seedhar A, Elia G, Hart IR, Kocher HM (2009) Organotypic culture model of pancreatic cancer demonstrates that stromal cells modulate E-cadherin, beta-catenin, and Ezrin expression in tumor cells. Am J Pathol 175: 636-648
18. Furukawa H, Takayasu K, Mukai K, Kanai Y, Kosuge T, Mizuguchi Y, Ushio K (1996) Serous cystadenoma of the pancreas communicating with a pancreatic duct. Int J Pancreatol 19: 141-144
19. Hwang RF, Moore T, Arumugam T, Ramachandran V, Amos KD, Rivera A, Ji B, Evans DB, Logsdon CD (2008) Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res 68: 918-926
20. Ishiwata T, Kornmann M, Beger HG, Korc M (1998) Enhanced fibroblast growth factor 5 expression in stromal and exocrine elements of the pancreas in chronic pancreatitis. Gut 43: 134-139
21. Jarosz M, Robbez-Masson L, Chioni AM, Cross B, Rosewell I, Grose R (2012) Fibroblast growth factor 22 is not essential for skin development and repair but plays a role in tumorigenesis. PLoS ONE 7: e39436
22. Joy A, Moffett J, Neary K, Mordechai E, Stachowiak EK, Coons S, Rankin-Shapiro J, Florkiewicz RZ, Stachowiak MK (1997) Nuclear accumulation of FGF-2 is associated with proliferation of human astrocytes and glioma cells. Oncogene 14: 171-183
23. Kadaba R, Birke H, Wang J, Hooper S, Andl CD, Maggio FD, Soylu E, Ghallab M, Bor D, Froeling FE et al (2013) Imbalance of desmoplastic stromal cell numbers drives aggressive cancer processes. J Pathol 230: 107-117
24. Kim SK, Hebrok M (2001) Intercellular signals regulating pancreas development and function. Genes Dev 15: 111-127
25. Kocher HM, Sandle J, Mirza TA, Li NF, Hart IR (2009) Ezrin interacts with cortactin to form podosomal rosettes in pancreatic cancer cells. Gut 58: 271-284
26. Kornmann M, Beger HG, Korc M (1998) Role of fibroblast growth factors and their receptors in pancreatic cancer and chronic pancreatitis. Pancreas 17: 169-175
27. Kornmann M, Ishiwata T, Beger HG, Korc M (1997) Fibroblast growth factor-5 stimulates mitogenic signaling and is overexpressed in human pancreatic cancer: evidence for autocrine and paracrine actions. Oncogene 15: 1417-1424
28. Kornmann M, Ishiwata T, Matsuda K, Lopez ME, Fukahi K, Asano G, Beger HG, Korc M (2002) IIIc isoform of fibroblast growth factor receptor 1 is overexpressed in human pancreatic cancer and enhances tumorigenicity of hamster ductal cells. Gastroenterology 123: 301-313
29. Kornmann M, Lopez M, Beger H, Korc M (2001) Expression of the IIIc variant of FGF receptor-1 confers mitogenic responsiveness to heparin and FGF-5 in TAKA-1 pancreatic ductal cells. Int J Gastrointest Cancer 29: 85-92
30. Leung HY, Gullick WJ, Lemoine NR (1994a) Expression and functional activity of fibroblast growth factors and their receptors in human pancreatic cancer. Int J Cancer 59: 667-675
31. Leung H, Hughes C, Kloppel G, Williamson R, Lemoine N (1994b) Localization of expression of fibroblast growth-factors and their receptors in pancreatic adenocarcinoma by in-situ hybridization. Int J Oncol 4: 1219-1223
32. Li NF, Kocher HM, Salako MA, Obermueller E, Sandle J, Balkwill F (2009) A novel function of colony-stimulating factor 1 receptor in hTERT immortalization of human epithelial cells. Oncogene 28: 773-780
33. Maher PA (1996) Identification and characterization of a novel, intracellular isoform of fibroblast growth factor receptor-1(FGFR-1). J Cell Physiol 169: 380-390
34. Moffett J, Kratz E, Florkiewicz R, Stachowiak MK (1996) Promoter regions involved in density-dependent regulation of basic fibroblast growth factor gene expression in human astrocytic cells. Proc Natl Acad Sci USA 93: 2470-2475
35. Mohammadi M, Froum S, Hamby JM, Schroeder MC, Panek RL, Lu GH, Eliseenkova AV, Green D, Schlessinger J, Hubbard SR (1998a) Crystal structure of an angiogenesis inhibitor bound to the FGF receptor tyrosine kinase domain. EMBO J 17: 5896-5904
36. Mohammadi S, Klement R, Shchyolkina AK, Liquier J, Jovin TM, Taillandier E (1998b) FTIR and UV spectroscopy of parallel-stranded DNAs with mixed A*T/G*C sequences and their A*T/I*C analogues. Biochemistry 37: 16529-16537
37. Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, Honess D, Madhu B, Goldgraben MA, Caldwell ME, Allard D et al (2009) Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 324: 1457-1461
38. Ornitz DM, Itoh N (2001) Fibroblast growth factors. Genome Biol 2: REVIEWS3005
39. Peng H, Moffett J, Myers J, Fang X, Stachowiak EK, Maher P, Kratz E, Hines J, Fluharty SJ, Mizukoshi E et al (2001) Novel nuclear signaling pathway mediates activation of fibroblast growth factor-2 gene by type 1 and type 2 angiotensin II receptors. Mol Biol Cell 12: 449-462
40. Peng H, Myers J, Fang X, Stachowiak EK, Maher PA, Martins GG, Popescu G, Berezney R, Stachowiak MK (2002) Integrative nuclear FGFR1 signaling (INFS) pathway mediates activation of the tyrosine hydroxylase gene by angiotensin II, depolarization and protein kinase C. J Neurochem 81: 506-524
41. Reilly JF, Maher PA (2001) Importin beta-mediated nuclear import of fibroblast growth factor receptor: role in cell proliferation. J Cell Biol 152: 1307-1312
42. Somanathan S, Stachowiak EK, Siegel AJ, Stachowiak MK, Berezney R (2003) Nuclear matrix bound fibroblast growth factor receptor is associated with splicing factor rich and transcriptionally active nuclear speckles. J Cell Biochem 90: 856-869
43. Stachowiak EK, Fang X, Myers J, Dunham S, Stachowiak MK (2003) cAMP-induced differentiation of human neuronal progenitor cells is mediated by nuclear fibroblast growth factor receptor-1 (FGFR1). J Neurochem 84: 1296-1312
44. Stachowiak EK, Maher PA, Tucholski J, Mordechai E, Joy A, Moffett J, Coons S, Stachowiak MK (1997a) Nuclear accumulation of fibroblast growth factor receptors in human glial cells-association with cell proliferation. Oncogene 14: 2201-2211
45. Stachowiak MK, Maher PA, Joy A, Mordechai E, Stachowiak EK (1996a) Nuclear accumulation of fibroblast growth factor receptors is regulated by multiple signals in adrenal medullary cells. Mol Biol Cell 7: 1299-1317
46. Stachowiak MK, Maher PA, Joy A, Mordechai E, Stachowiak EK (1996b) Nuclear localization of functional FGF receptor 1 in human astrocytes suggests a novel mechanism for growth factor action. Brain Res Mol Brain Res 38: 161-165
47. Stachowiak MK, Moffett J, Joy A, Puchacz E, Florkiewicz R, Stachowiak EK (1994) Regulation of bFGF gene expression and subcellular distribution of bFGF protein in adrenal medullary cells. J Cell Biol 127: 203-223
48. Stachowiak MK, Moffett J, Maher P, Tucholski J, Stachowiak EK (1997b) Growth factor regulation of cell growth and proliferation in the nervous system. A new intracrine nuclear mechanism. Mol Neurobiol 15: 257-283
49. Tian X, Chen G, Zhou S, Henne-Bruns D, Bachem M, Kornmann M (2012) Interactions of pancreatic cancer and stellate cells are mediated by FGFR1-III isoform expression. Hepatogastroenterology 59: 1604-1608
50. Turner N, Grose R (2010) Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer 10: 116-129
51. Vonlaufen A, Phillips PA, Xu Z, Goldstein D, Pirola RC, Wilson JS, Apte MV (2008) Pancreatic stellate cells and pancreatic cancer cells: an unholy alliance. Cancer Res 68: 7707-7710
52. Xu Z, Vonlaufen A, Phillips PA, Fiala-Beer E, Zhang X, Yang L, Biankin AV, Goldstein D, Pirola RC, Wilson JS et al (2010) Role of pancreatic stellate cells in pancreatic cancer metastasis. Am J Pathol 177: 2585-2596
53. Yamanaka Y, Friess H, Buchler M, Beger HG, Uchida E, Onda M, Kobrin MS, Korc M (1993) Overexpression of acidic and basic fibroblast growth factors in human pancreatic cancer correlates with advanced tumor stage. Cancer Res 53: 5289-5296
54. Yamazaki K, Nagao T, Yamaguchi T, Saisho H, Kondo Y (1997) Expression of basic fibroblast growth factor (FGF-2)-associated with tumour proliferation in human pancreatic carcinoma. Virchows Arch 431: 95-101
55. Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M, Ornitz DM (2006) Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J Biol Chem 281: 15694-15700