Galectin-1 drives pancreatic carcinogenesis through stroma remodeling and hedgehog signaling activation

Cancer Research

Volumn 74, Issue 13, 2014, Pages 3512-3524

  Martínez Bosch, Neus ^a   Fern̊andez Barrena, Maite G ^d   Moreno, Mireia ^a   Ortiz Zapater, Elena ^a   Munn̊e Collado, Jessica ^a,b   Iglesias, Mar ^a,b   Andr̊e, Sabine ^f   Gabius, Hans Joachim ^f   Hwang, Rosa F ^e   Coise Poirier, Fraņ ^g   Navas, Carolina ^c   Guerra, Carmen ^c   Fern̊andez Zapico, Martin E ^d   Navarro, Pilar ^a  

^a INST MUNIC D INVESTIGACIO MEDICA   (Spain)

^b HOSPITAL DEL MAR   (Spain)

^c Centro Nacional de Investigaciones Oncológicas   (Spain)

^d MAYO CLINIC   (United States)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^f UNIVERSITY OF MUNICH   (Germany)

^g INSTITUT JACQUES MONOD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GALECTIN 1; SONIC HEDGEHOG PROTEIN;

ACINAR TO DUCTAL METAPLASIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER MODEL; CARCINOGENESIS; CARCINOGENICITY; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOSTIMULATION; IN VITRO STUDY; IN VIVO STUDY; METAPLASIA; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STROMA CELL; TISSUE REACTION; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION;

ADENOCARCINOMA; ANIMALS; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DESMOPLASTIC SMALL ROUND CELL TUMOR; GALECTIN 1; HEDGEHOG PROTEINS; HEK293 CELLS; HUMANS; MICE; NEOVASCULARIZATION, PATHOLOGIC; PANCREATIC NEOPLASMS; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84903955050     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-3013     Document Type: Article

References (50)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013;63:11-30.
2. Hidalgo M. Pancreatic cancer. N Engl J Med 2010;362:1605-17.
3. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008;321:1801-6.
4. Provenzano PP, Cuevas C, Chang AE, Goel VK, Von Hoff DD, Hingorani SR. Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell 2012; 21:418-29.
5. Camby I, Le Mercier M, Lefranc F, Kiss R. Galectin-1: a small protein with major functions. Glycobiology 2006;16:137R-57R.
6. Perillo NL, Pace KE, Seilhamer JJ, Baum LG. Apoptosis of T cells mediated by galectin-1. Nature 1995;378:736-9.
7. Demydenko D, Berest I. Expression of galectin-1 in malignant tumors. Exp Oncol 2009;31:74-9.
8. Berberat PO, Friess H, Wang L, Zhu Z, Bley T, Frigeri L, et al. Comparative analysis of galectins in primary tumors and tumor metastasis in human pancreatic cancer. J Histochem Cytochem 2001;49:539-49.
9. Grutzmann R, Pilarsky C, Ammerpohl O, Luttges J, Bohme A, Sipos B, et al. Gene expression profiling of microdissected pancreatic ductal carcinomas using high-density DNA microarrays. Neoplasia 2004;6: 611-22.
10. Iacobuzio-Donahue CA, Ashfaq R, Maitra A, Adsay NV, Shen-Ong GL, Berg K, et al. Highly expressed genes in pancreatic ductal adenocarcinomas: a comprehensive characterization and comparison of the transcription profiles obtained from three major technologies. Cancer Res 2003;63:8614-22.
11. Shen J, Person MD, Zhu J, Abbruzzese JL, Li D. Protein expression profiles in pancreatic adenocarcinoma compared with normal pancreatic tissue and tissue affected by pancreatitis as detected by twodimensional gel electrophoresis and mass spectrometry. Cancer Res 2004;64:9018-26.
12. Roda O, Ortiz-Zapater E, Martinez-Bosch N, Gutierrez-Gallego R, Vila- Perello M, Ampurdanes C, et al. Galectin-1 is a novel functional receptor for tissue plasminogen activator in pancreatic cancer. Gastroenterology 2009;136:1379-5.
13. Pan S, Chen R, Reimel BA, Crispin DA, Mirzaei H, Cooke K, et al. Quantitative proteomics investigation of pancreatic intraepithelial neoplasia. Electrophoresis 2009;30:1132-44.
14. Martinez-Bosch N, Navarro P. Glycans and galectins: sweet new approaches in pancreatic cancer diagnosis and treatment. In:Srivastava S, editor. Pancreatic cancer: molecular mechanism and targets. Rijeka, Croatia: In Tech 2012. p. 305-28.
15. Chung JC, Oh MJ, Choi SH, Bae CD. Proteomic analysis to identify biomarker proteins in pancreatic ductal adenocarcinoma. ANZ J Surg 2008;78:245-51.
16. Sandgren EP, Quaife CJ, Paulovich AG, Palmiter RD, Brinster RL. Pancreatic tumor pathogenesis reflects the causative genetic lesion. Proc Natl Acad Sci U S A 1991;88:93-7.
17. Grippo PJ, Sandgren EP. Acinar-to-ductal metaplasia accompanies cmyc- induced exocrine pancreatic cancer progression in transgenic rodents. Int J Cancer 2012;131:1243-8.
18. Guerra C, Schuhmacher AJ, Canamero M, Grippo PJ, Verdaguer L, Perez-Gallego L, et al. Chronic pancreatitis is essential for induction of pancreatic ductal adenocarcinoma by K-Ras oncogenes in adult mice. Cancer Cell 2007;11:291-302.
19. Ortiz-Zapater E, Pineda D, Martinez-Bosch N, Iglesias MM, Moreno MM, Eliscovich C, et al. Key contribution of CPEB4-mediated translational control to pancreatic cancer progression. Nat Med 2011; 18:83-90.
20. Hwang RF, Moore T, Arumugam T, Ramachandran V, Amos KD, Rivera A, et al. Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res 2008;68:918-26.
21. Sasaki H, Hui C, Nakafuku M, Kondoh H. A binding site for Gli proteins is essential for HNF-3beta floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 1997; 124:1313-22.
22. Lin WC, Rajbhandari N, Liu C, Sakamoto K, Zhang Q, Triplett AA, et al. Dormant cancer cells contribute to residual disease in a model of reversible pancreatic cancer. Cancer Res 2013;73:1821-30.
23. Ischenko I, Zhi J, Moll UM, Nemajerova A, Petrenko O. Direct reprogramming by oncogenic Ras and Myc. Proc Natl Acad Sci U S A 2013;110:3937-42.
24. Schleger C, Verbeke C, Hildenbrand R, Zentgraf H, Bleyl U. c-MYC activation in primary and metastatic ductal adenocarcinoma of the pancreas: incidence, mechanisms, and clinical significance. Mod Pathol 2002;15:462-9.
25. Parsa I, Longnecker DS, Scarpelli DG, Pour P, Reddy JK, Lefkowitz M. Ductal metaplasia of human exocrine pancreas and its association with carcinoma. Cancer Res 1985;45:1285-90.
26. Reichert M, Rustgi AK. Pancreatic ductal cells in development, regeneration, and neoplasia. J Clin Invest 2011;121:4572-8.
27. Means AL, Meszoely IM, Suzuki K, Miyamoto Y, Rustgi AK, Coffey RJ Jr, et al. Pancreatic epithelial plasticity mediated by acinar cell transdifferentiation and generation of nestin-positive intermediates. Development 2005;132:3767-76.
28. Navas C, Hernandez-Porras I, Schuhmacher AJ, Sibilia M, Guerra C, Barbacid M. Epidermal growth factor receptor signalling is essential for K-Ras oncogene-driven pancreatic ductal adenocarcinoma. Cancer Cell 2012;11:318-30.
29. Feig C, Gopinathan A, Neesse A, Chan DS, Cook N, Tuveson DA. The pancreas cancer microenvironment. Clin Cancer Res 2012;18: 4266-76.
30. Rabinovich GA, Toscano MA. Turning 'sweet' on immunity: galectinglycan interactions in immune tolerance and inflammation. Nat Rev Immunol 2009;9:338-52.
31. Thayer SP, di Magliano MP, Heiser PW, Nielsen CM, Roberts DJ, Lauwers GY, et al. Hedgehog is an early and latemediator of pancreatic cancer tumorigenesis. Nature 2003;425:851-6.
32. Burke R, Nellen D, Bellotto M, Hafen E, Senti KA, Dickson BJ, et al. Dispatched, a novel sterol-sensing domain protein dedicated to the release of cholesterol-modified hedgehog from signaling cells. Cell 1999;99:803-15.
33. Yoon JW, Kita Y, Frank DJ, Majewski RR, Konicek BA, Nobrega MA, et al. Gene expression profiling leads to identification of GLI1-binding elements in target genes and a role for multiple downstream pathways in GLI1-induced cell transformation. J Biol Chem 2002;277:5548-55.
34. Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, Honess D, et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009;324:1457-61.
35. Erkan M, Hausmann S, Michalski CW, Fingerle AA, Dobritz M, Kleeff J, et al. The role of stroma in pancreatic cancer: diagnostic and therapeutic implications. Nat Rev Gastroenterol Hepatol 2012;9:454-67.
36. Ying H, Kimmelman AC, Lyssiotis CA, Hua S, Chu GC, Fletcher- Sananikone E, et al. Oncogenic Kras maintains pancreatic tumors through regulation of anabolic glucose metabolism. Cell 2012;149: 656-70.
37. Soucek L, Whitfield J, Martins CP, Finch AJ, Murphy DJ, Sodir NM, et al. Modelling Myc inhibition as a cancer therapy. Nature 2008;455: 679-83.
38. Banh A, Zhang J, Cao H, Bouley DM, Kwok S, Kong C, et al. Tumor galectin-1 mediates tumor growth and metastasis through regulation of T-cell apoptosis. Cancer Res 2011;71:4423-31.
39. Dalotto-Moreno T, Croci DO, Cerliani JP, Martinez-Allo VC, Dergan- Dylon S, Mendez-Huergo SP, et al. Targeting galectin-1 overcomes breast cancer-associated immunosuppression and prevents metastatic disease. Cancer Res 2013;73:1107-17.
40. Compagno D, Laderach DJ, Gentilini L, Jaworski FM, Rabinovich GA. Delineating the "galectin signature" of the tumor microenvironment. Oncoimmunology 2013;2:e23565.
41. Xue X, Lu Z, Tang D, Yao J, An Y, Wu J, et al. Galectin-1 secreted by activated stellate cells in pancreatic ductal adenocarcinoma stroma promotes proliferation and invasion of pancreatic cancer cells: an in vitro study on the microenvironment of pancreatic ductal adenocarcinoma. Pancreas 2011;40:832-9.
42. Thijssen VL, Barkan B, Shoji H, Aries IM, Mathieu V, Deltour L, et al. Tumor cells secrete galectin-1 to enhance endothelial cell activity. Cancer Res 2010;70:6216-24.
43. Masamune A, Satoh M, Hirabayashi J, Kasai K, Satoh K, Shimosegawa T
44. Wu MH, Hong HC, Hong TM, Chiang WF, Jin YT, Chen YL. Targeting Galectin-1 in Carcinoma-Associated Fibroblasts Inhibits Oral Squamous Cell Carcinoma Metastasis by Downregulating MCP-1/ CCL2 Expression. Clin Cancer Res 2011;17:1306-16.
45. Perez-Mancera PA, Guerra C, Barbacid M, Tuveson DA. What we have learned about pancreatic cancer from mouse models. Gastroenterology 2012;142:1079-92.
46. Crawford HC, Scoggins CR, Washington MK, Matrisian LM, Leach SD. Matrix metalloproteinase-7 is expressed by pancreatic cancer precursors and regulates acinar-to-ductal metaplasia in exocrine pancreas. J Clin Invest 2002;109:1437-44.
47. Camby I, Decaestecker C, Lefranc F, Kaltner H, Gabius HJ, Kiss R. Galectin-1 knocking down in human U87 glioblastoma cells alters their gene expression pattern. Biochem Biophys Res Commun 2005; 335:27-35.
48. Bailey JM, Swanson BJ, Hamada T, Eggers JP, Singh PK, Caffery T, et al. Sonic hedgehog promotes desmoplasia in pancreatic cancer. Clin Cancer Res 2008;14:5995-6004.
49. Bailey JM, Mohr AM, Hollingsworth MA. Sonic hedgehog paracrine signaling regulates metastasis and lymphangiogenesis in pancreatic cancer. Oncogene 2009;28:3513-25.
50. Pasca dM, Sekine S, Ermilov A, Ferris J, Dlugosz AA, Hebrok M. Hedgehog/Ras interactions regulate early stages of pancreatic cancer. Genes Dev 2006;20:3161-73.