A novel SULF1 splice variant inhibits Wnt signalling but enhances angiogenesis by opposing SULF1 activity

Experimental Cell Research

Volumn 315, Issue 16, 2009, Pages 2752-2764

  Sahota, Amrit Paul ^a   Dhoot, Gurtej K ^a  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

Author keywords

Angiogenesis; Splice variant; Sulf1; Wnt signalling

Indexed keywords

COMPLEMENTARY DNA; MESSENGER RNA; SULFATASE; SULFATASE 1A; SULFATASE 1B; UNCLASSIFIED DRUG; WNT PROTEIN;

AMINO ACID SEQUENCE; ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CHICK; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME RELEASE; GENETIC VARIABILITY; HISTOGENESIS; INHIBITION KINETICS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUAIL; RNA SPLICING; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

EID: 68949158449     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.06.029     Document Type: Article

References (33)

1. Dhoot G.K., Gustafsson M.K., Ai X., Sun W., Standiford D.M., and Emerson C.P. Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science 293 (2001) 1663-1666
2. Morimoto-Tomita M., Uchimura K., Werb Z., Hemmerich S., and Rosen S.D. Cloning and characterization of two extracellular heparin-degrading endosulfatases in mice and humans. J. Biol. Chem. 277 (2002) 49175-49185
3. Robertson D.A., Freeman C., Morris C.P., and Hopwood J.J. A cDNA clone for human glucosamine-6-sulphatase reveals differences between arylsulphatases and non-arylsulphatases. Biochem. J. 288 (1992) 539-544
4. Lukatela G., Krauss N., Theis K., selmer T., gieselmann V., von Figura K., and Saenger W. Crystal structure of human arylsulfatase A: the aldehyde function and the metal ion at the active site suggest a novel mechanism for sulfate ester hydrolysis. Biochemistry 37 (1998) 3654-3664
5. Knaust A., Schmidt B., Dierks T., von Bulow R., and von Figura K. Residues critical for formylglycine formation and/or catalytic activity of arylsulfatase A. Biochemistry 37 (1998) 13941-13946
6. Lamanna W.C., Baldwin R.J., Padva M., Kalus I., Ten Dam G., van Kuppevelt T.H., Gallagher J.T., von Figura K., Dierks T., and Merry C.L. Heparan sulfate 6-O-endosulfatases: discrete in vivo activities and functional co-operativity. Biochem. 400 (2006) 63-73
7. Lum D.H., Tan J., Rosen S.D., and Werb Z. Gene trap disruption of the mouse heparan sulfate 6-O-endosulfatase gene, Sulf2. Mol. Cell. Biol. 27 (2007) 678-688
8. Holst C.R., Bou-Reslan H., Gore B.B., Wong K., Grant D., Chalasani S., Carano R.A., Frantz G.D., Tessier-Lavigne M., Bolon B., French D.M., and Ashkenazi A. Secreted sulfatases Sulf1 and Sulf2 have overlapping yet essential roles in mouse neonatal survival. PLoS ONE 2 6 (2007) e575
9. Ai X., Kitazawa T., Do A.T., Kusche-Gullberg O.M., Labosky P.A., and Emerson C.P. SULF1 and SULF2 regulate heparan sulfate-mediated GDNF signaling for esophageal innervation. Development 134 (2007) 3327-3338
10. Lai J.P., Chien J., Moser J.D.R., Staub J.K., Aderca I., Montoya D.P., Matthews T.A., Nagorney D.M., Cunningham J.M., Smith D.I., Greene E.L., Shridhar V., and Roberts L.R. hSulf1 Sulfatase promotes apoptosis of hepatocellular cancer cells by decreasing heparin-binding growth factor signaling. Gastroenterology 126 (2004) 231-248
11. Li J., Kleeff J., Abiatari I., Kayed H., Giese N.A., Felix K., Giese T., Buchler M.W., and Friss H. Enhanced levels of Hsulf-1 interfere with heparin-binding growth factor signaling in pancreatic cancer. Mol. Cancer 4 (2005) 14
12. Ai X., Do A.T., Kusche-Gullberg O.M., Lindahl U., Lu K., and Emerson C.P. Substrate specificity and domain functions of extracellular heparan sulfate 6-O-endosulfatases, QSulf1 and QSulf2. J. Biol. Chem. 281 (2006) 4969-4976
13. Schmidt B., Selmer T., Ingendoh A., and von Figura K. A novel amino acid modification in sulfatases that is defective in multiple sulfatase deficiency. Cell 82 (1995) 271-278
14. Ai X., Do A.T., Lozynska O., Kusche-Gullberg M., Lindahl U., and Emerson C.P. QSulf1 remodels the 6-O sulfation states of cell surface heparan sulfate proteoglycans to promote Wnt signaling. J. Cell Biol. 162 (2003) 341-351
15. Nawroth R., van Zante A., Cervantes S., McManus M., Hebrok M., and Rosen S.D. Extracellular sulfatases, elements of the Wnt signaling pathway, positively regulate growth and tumorigenicity of human pancreatic cancer cells. PLoS ONE 2 4 (2007) e392
16. Armstrong V.J., Muzylak M., Sunters A., Zaman G., Saxon L.K., Price J.S., and Lanyon L.E. Wnt/beta-catenin signaling is a component of osteoblastic bone cell early responses to load-bearing and requires estrogen receptor alpha. J. Biol. Chem. 282 (2007) 20715-20727
17. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
18. Towbin H., Staehelin T., and Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. 76 (1979) 4350-4354
19. Zhao W., Sala-Newby G.B., and Dhoot G.K. Sulf1 expression pattern and its role in cartilage and joint development. Dev. Dyn. 235 (2006) 3327-3335
20. Zhao W., and Dhoot G.K. Both smooth and skeletal muscle precursors are present in foetal mouse oesophagus and they follow different differentiation pathways. Dev. Dyn. 218 (2000) 587-602
21. Dhoot G.K. Selective synthesis and degradation of slow skeletal myosin heavy chains in developing muscle fibers. Muscle Nerve 9 2 (1986) 155-164
22. Williams K., Zak R., and Dhoot G.K. Identification of multiple myotube and myosin heavy chain types during embryonic development of chicken skeletal muscles. Basic Appl. Myol. 2 (1992) 17-26
23. Wang S., Ai X., Freeman S.D., Pownall M.E., Lu Q., Kessler D.S., and Emerson C.P. QSulf1, a heparan sulfate 6-O-endosulfatase, inhibits fibroblast growth factor signaling in mesoderm induction and angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 4833-4838
24. Narita K., Staub J., Chien J., Meyer K., Bauer M., Friedl A., Ramakrishnan S., and Shridhar V. HSulf-1 inhibits angiogenesis and tumorigenesis in vivo. Cancer Res. 66 (2006) 6025-6032
25. Licatalosi D.D., Mele A., Fak J.J., Ule J., Kayikci M., Chi S.W., Clark T.A., Schweitzer A.C., Blume J.E., Wang X., Darnell J.C., and Darnell R.B. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 456 (2008) 464-469
26. Lai J.P., Chien J., Staub J., Avula R., Greene E.L., Matthews T.A., Smith D.I., Kaufman S.H., Roberts L.R., and Shridhar V. Loss of HSulf-1 up-regulates heparin-binding growth factor signaling in cancer. J. Biol. Chem. 278 (2003) 23107-23117
27. Lai J.P., Chien J., Strome J.S.E., Staub J., Montoya D.P., Greene E.L., Smith D.I., Roberts L.R., and Shridhar V. HSulf-1 modulates HGF-mediated tumor cell invasion and signaling in head and neck squamous carcinoma. Oncogene 23 (2004) 1439-1447
28. Pajares M.J., Ezponda T., Catena R., Calvo A., Pio R., and Montuenga L.M. Alternative splicing: an emerging topic in molecular and clinical oncology. Lancet Oncol. 8 (2007) 349-357
29. Licatalosi D.D., and Darnell R.B. Splicing regulation in neurologic disease. Neuron 52 (2006) 93-101
30. Medrek B., and Lee C. A genomic view of alternative splicing. Nat. Genet. 30 (2002) 13-19
31. Behrends S., Harteneck C., Schultz G.D., and Koesling D. A variant of the alpha 2 subunit of soluble guanylyl cyclase contains an insert homologous to a region within adenylyl cyclases and functions as a dominant negative protein. J. Biol. Chem. 270 (1995) 21109-21113
32. Demolombe S., Baro I., Pereon Y., Bliek J., Mohammad-Panah R., Pollard H., Morid S., Mannens M., Wilde A., Barhanin J., Charpentier F., and Escande D. A dominant negative isoform of the long QT syndrome 1 gene product. J. Biol. Chem. 273 (1998) 6837-6843
33. Hwu W.L., Yeh H.Y., Fang S.W., Chiang H.S., Chiou Y.W., and Lee Y.M. Regulation of GTP cyclohydrolase I by alternative splicing in mononuclear cells. Biochem. Biophys. Res. Commun. 306 (2003) 937-942