Blocking Hedgehog release from pancreatic cancer cells increases paracrine signaling potency

Journal of Cell Science

Volumn 128, Issue 1, 2015, Pages 129-139

  Damhofer, Helene ^a   Veenstra, Veronique L ^a   Tol, Johanna A M G ^a   van Laarhoven, Hanneke W M ^a,b   Medema, Jan Paul ^a   Bijlsma, Maarten F ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

ADAM; Pancreatic cancer; Shedding; Sonic Hedgehog

Indexed keywords

ADAM PROTEIN; SONIC HEDGEHOG PROTEIN; TUMOR PROTEIN;

ARTICLE; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; PANCREATIC CANCER CELL LINE; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN SECRETION; SOLUBILIZATION; STROMA CELL; ANIMAL; GENETICS; HEK293 CELL LINE; METABOLISM; MOUSE; PANCREAS TUMOR; PATHOLOGY; SECRETION (PROCESS); SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ERINACEIDAE;

ADAM PROTEINS; ANIMALS; CELL LINE, TUMOR; HEDGEHOG PROTEINS; HEK293 CELLS; HUMANS; MICE; NEOPLASM PROTEINS; PANCREATIC NEOPLASMS; PARACRINE COMMUNICATION; SIGNAL TRANSDUCTION;

EID: 84921657433     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.157966     Document Type: Article

References (42)

1. Albrechtsen, R., Kveiborg, M., Stautz, D., Vikeså, J., Noer, J. B., Kotzsh, A., Nielsen, F. C., Wewer, U. M. and Fröhlich, C. (2013). ADAM12 redistributes and activates MMP-14, resulting in gelatin degradation, reduced apoptosis and increased tumor growth. J. Cell Sci. 126, 4707-4720.
2. Ashe, H. L. and Briscoe, J. (2006). The interpretation of morphogen gradients. Development 133, 385-394.
3. Ayers, K. L., Gallet, A., Staccini-Lavenant, L. and Thérond, P. P. (2010). The long-range activity of Hedgehog is regulated in the apical extracellular space by the glypican Dally and the hydrolase Notum. Dev. Cell 18, 605-620.
4. Badea, L., Herlea, V., Dima, S. O., Dumitrascu, T. and Popescu, I. (2008). Combined gene expression analysis of whole-tissue and microdissected pancreatic ductal adenocarcinoma identifies genes specifically overexpressed in tumor epithelia. Hepatogastroenterology 55, 2016-2027.
5. Bellaiche, Y., The, I. and Perrimon, N. (1998). Tout-velu is a Drosophila homologue of the putative tumour suppressor EXT-1 and is needed for Hh diffusion. Nature 394, 85-88.
6. Bijlsma, M. F., Spek, C. A. and Peppelenbosch, M. P. (2004). Hedgehog: an unusual signal transducer. BioEssays 26, 387-394.
7. Bischoff, M., Gradilla, A. C., Seijo, I., Andrés, G., Rodríguez-Navas, C., González-Méndez, L. and Guerrero, I. (2013). Cytonemes are required for the establishment of a normal Hedgehog morphogen gradient in Drosophila epithelia. Nat. Cell Biol. 15, 1269-1281.
8. Blobel, C. P. (2005). ADAMs: key components in EGFR signalling and development. Nat. Rev. Mol. Cell Biol. 6, 32-43.
9. Burke, R., Nellen, D., Bellotto, M., Hafen, E., Senti, K. A., Dickson, B. J. and Basler, K. (1999). Dispatched, a novel sterol-sensing domain protein dedicated to the release of cholesterol-modified hedgehog from signaling cells. Cell 99, 803-815.
10. Caspary, T., García-García, M. J., Huangfu, D., Eggenschwiler, J. T., Wyler, M. R., Rakeman, A. S., Alcorn, H. L. and Anderson, K. V. (2002). Mouse Dispatched homolog1 is required for long-range, but not juxtacrine, Hh signaling. Curr. Biol. 12, 1628-1632.
11. Chamoun, Z., Mann, R. K., Nellen, D., von Kessler, D. P., Bellotto, M., Beachy, P. A. and Basler, K. (2001). Skinny hedgehog, an acyltransferase required for palmitoylation and activity of the hedgehog signal. Science 293, 2080-2084.
12. Chen, M. H., Li, Y. J., Kawakami, T., Xu, S. M. and Chuang, P. T. (2004). Palmitoylation is required for the production of a soluble multimeric Hedgehog protein complex and long-range signaling in vertebrates. Genes Dev. 18, 641-659.
13. Dierker, T., Dreier, R., Petersen, A., Bordych, C. and Grobe, K. (2009). Heparan sulfate-modulated, metalloprotease-mediated sonic hedgehog release from producing cells. J. Biol. Chem. 284, 8013-8022.
14. Echelard, Y., Epstein, D. J., St-Jacques, B., Shen, L., Mohler, J., McMahon, J. A. and McMahon, A. P. (1993). Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417-1430.
15. Etheridge, L. A., Crawford, T. Q., Zhang, S. and Roelink, H. (2010). Evidence for a role of vertebrate Disp1 in long-range Shh signaling. Development 137, 133-140.
16. Gaida, M. M., Haag, N., Günther, F., Tschaharganeh, D. F., Schirmacher, P., Friess, H., Giese, N. A., Schmidt, J. and Wente, M. N. (2010). Expression of A disintegrin and metalloprotease 10 in pancreatic carcinoma. Int. J. Mol. Med. 26, 281-288.
17. Goodrich, L. V., Milenkovic, L., Higgins, K. M. and Scott, M. P. (1997). Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277, 1109-1113.
18. Gschwind, A., Hart, S., Fischer, O. M. and Ullrich, A. (2003). TACE cleavage of proamphiregulin regulates GPCR-induced proliferation and motility of cancer cells. EMBO J. 22, 2411-2421.
19. Han, C., Belenkaya, T. Y., Wang, B. and Lin, X. (2004). Drosophila glypicans control the cell-to-cell movement of Hedgehog by a dynamin-independent process. Development 131, 601-611.
20. Horiuchi, K., Le Gall, S., Schulte, M., Yamaguchi, T., Reiss, K., Murphy, G., Toyama, Y., Hartmann, D., Saftig, P. and Blobel, C. P. (2007). Substrate selectivity of epidermal growth factor-receptor ligand sheddases and their regulation by phorbol esters and calcium influx. Mol. Biol. Cell 18, 176-188.
21. Lee, J. J., Perera, R. M., Wang, H., Wu, D. C., Liu, X. S., Han, S., Fitamant, J., Jones, P. D., Ghanta, K. S., Kawano, S. et al. (2014). Stromal response to Hedgehog signaling restrains pancreatic cancer progression. Proc. Natl. Acad. Sci. USA 111, E3091-E3100.
22. Ma, Y., Erkner, A., Gong, R., Yao, S., Taipale, J., Basler, K. and Beachy, P. A. (2002). Hedgehog-mediated patterning of the mammalian embryo requires transporter-like function of dispatched. Cell 111, 63-75.
23. Matthews, V., Schuster, B., Schütze, S., Bussmeyer, I., Ludwig, A., Hundhausen, C., Sadowski, T., Saftig, P., Hartmann, D., Kallen, K. J. et al. (2003). Cellular cholesterol depletion triggers shedding of the human interleukin-6 receptor by ADAM10 and ADAM17 (TACE). J. Biol. Chem. 278, 38829-38839.
24. Murphy, G. (2008). The ADAMs: signalling scissors in the tumour microenvironment. Nat. Rev. Cancer 8, 932-941.
25. Ohlig, S., Farshi, P., Pickhinke, U., van den Boom, J., Höing, S., Jakuschev, S., Hoffmann, D., Dreier, R., Schöler, H. R., Dierker, T. et al. (2011). Sonic hedgehog shedding results in functional activation of the solubilized protein. Dev. Cell 20, 764-774.
26. Ohlig, S., Pickhinke, U., Sirko, S., Bandari, S., Hoffmann, D., Dreier, R., Farshi, P., Götz, M. and Grobe, K. (2012). An emerging role of Sonic hedgehog shedding as a modulator of heparan sulfate interactions. J. Biol. Chem. 287, 43708-43719.
27. Panáková, D., Sprong, H., Marois, E., Thiele, C. and Eaton, S. (2005). Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature 435, 58-65.
28. Pei, H., Li, L., Fridley, B. L., Jenkins, G. D., Kalari, K. R., Lingle, W., Petersen, G., Lou, Z. and Wang, L. (2009). FKBP51 affects cancer cell response to chemotherapy by negatively regulating Akt. Cancer Cell 16, 259-266.
29. Queiroz, K. C., Tio, R. A., Zeebregts, C. J., Bijlsma, M. F., Zijlstra, F., Badlou, B., de Vries, M., Ferreira, C. V., Spek, C. A., Peppelenbosch, M. P. et al. (2010). Human plasma very low density lipoprotein carries Indian hedgehog. J. Proteome Res. 9, 6052-6059.
30. Reya, T., Duncan, A. W., Ailles, L., Domen, J., Scherer, D. C., Willert, K., Hintz, L., Nusse, R. and Weissman, I. L. (2003). A role for Wnt signalling in selfrenewal of haematopoietic stem cells. Nature 423, 409-414.
31. Rhim, A. D., Oberstein, P. E., Thomas, D. H., Mirek, E. T., Palermo, C. F., Sastra, S. A., Dekleva, E. N., Saunders, T., Becerra, C. P., Tattersall, I. W. et al. (2014). Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell 25, 735-747.
32. Ringel, J., Jesnowski, R., Moniaux, N., Lüttges, J., Ringel, J., Choudhury, A., Batra, S. K., Klöppel, G. and Löhr, M. (2006). Aberrant expression of a disintegrin and metalloproteinase 17/tumor necrosis factor-alpha converting enzyme increases the malignant potential in human pancreatic ductal adenocarcinoma. Cancer Res. 66, 9045-9053.
33. Sanders, T. A., Llagostera, E. and Barna, M. (2013). Specialized filopodia direct long-range transport of SHH during vertebrate tissue patterning. Nature 497, 628-632.
34. Sasaki, H., Hui, C., Nakafuku, M. and Kondoh, H. (1997). 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 124, 1313-1322.
35. Sato, M. and Kornberg, T. B. (2002). FGF is an essential mitogen and chemoattractant for the air sacs of the drosophila tracheal system. Dev. Cell 3, 195-207.
36. Seals, D. F. and Courtneidge, S. A. (2003). The ADAMs family of metalloproteases: multidomain proteins with multiple functions. Genes Dev. 17, 7-30.
37. Taipale, J., Chen, J. K., Cooper, M. K., Wang, B., Mann, R. K., Milenkovic, L., Scott, M. P. and Beachy, P. A. (2000). Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 406, 1005-1009.
38. Thérond, P. P. (2012). Release and transportation of Hedgehog molecules. Curr. Opin. Cell Biol. 24, 173-180.
39. Traiffort, E., Dubourg, C., Faure, H., Rognan, D., Odent, S., Durou, M. R., David, V. and Ruat, M. (2004). Functional characterization of sonic hedgehog mutations associated with holoprosencephaly. J. Biol. Chem. 279, 42889-42897.
40. Tukachinsky, H., Kuzmickas, R. P., Jao, C. Y., Liu, J. and Salic, A. (2012). Dispatched and scube mediate the efficient secretion of the cholesterol-modified hedgehog ligand. Cell Rep. 2, 308-320.
41. Yauch, R. L., Gould, S. E., Scales, S. J., Tang, T., Tian, H., Ahn, C. P., Marshall, D., Fu, L., Januario, T., Kallop, D. et al. (2008). A paracrine requirement for hedgehog signalling in cancer. Nature 455, 406-410.
42. Zeng, X., Goetz, J. A., Suber, L. M., Scott, W. J., Jr, Schreiner, C. M. and Robbins, D. J. (2001). A freely diffusible form of Sonic hedgehog mediates long-range signalling. Nature 411, 716-720.