Heparin-degrading sulfatases in hepatocellular carcinoma: Roles in pathogenesis and therapy targets

Future Oncology

Volumn 4, Issue 6, 2008, Pages 803-814

  Lai, Jin Ping ^a   Thompson, James R ^b   Sandhu, Dalbir S ^a   Roberts, Lewis R ^c  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

^c Mayo Clinic   (United States)

Author keywords

Akt; Glypican 3; Heparan sulfate glycosaminoglycans; Heparan sulfate proteoglycan; Heparin binding growth factor; Hepatocellular carcinoma; MAPK kinase; SULF1; SULF2

Indexed keywords

FIBROBLAST GROWTH FACTOR; HEPARIN; HISTONE DEACETYLASE INHIBITOR; HISTONE H4; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; PROTEOHEPARAN SULFATE; SULFATASE; SULFATASE 1; SULFATASE 2; UNCLASSIFIED DRUG; SULF1 PROTEIN, HUMAN; SULF2 PROTEIN, HUMAN; SULFOTRANSFERASE;

ACETYLATION; CANCER CELL CULTURE; CANCER INHIBITION; CANCER STAGING; CANCER SURVIVAL; CELL GROWTH; CELL SURFACE; DOWN REGULATION; DROSOPHILA; DRUG RESEARCH; DRUG TARGETING; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; MEDICAL DECISION MAKING; MOLECULAR CLONING; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROGNOSIS; PROTEIN INTERACTION; QUAIL; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; ENZYMOLOGY; GENETICS; LIVER TUMOR; METABOLISM; PHYSIOLOGY;

ANIMALS; CARCINOMA, HEPATOCELLULAR; HEPARIN; HUMANS; LIVER NEOPLASMS; SIGNAL TRANSDUCTION; SULFOTRANSFERASES;

EID: 61449446524     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.2217/14796694.4.6.803     Document Type: Review

References (61)

1. Parkin DM, Bray F, Ferlay J, Pisani P: Global cancer statistics, 2002. CA Cancer J. Clin. 55(2), 74-108 (2005).
2. El-Serag HB, Mason AC: Rising incidence of hepatocellular carcinoma in the United States. N. Engl. J. Med. 340(10), 745-750 (1999).
3. Thomas MB, Abbruzzese JL: Opportunities for targeted therapies in hepatocellular carcinoma. J. Clin. Oncol. 23(31), 8093-8108 (2005).
4. El-Serag HB: Hepatocellular carcinoma: recent trends in the United States. Gastroenterology 127(5 Suppl. 1), S27-S34 (2004).
5. Wilson JF: Liver cancer on the rise. Ann. Intern. Med. 142(12 Pt 1), 1029-1032 (2005).
6. El-Serag HB, Rudolph KL: Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132(7), 2557-2576 (2007).
7. Avila MA, Berasain C, Sangro B, Prieto J: New therapies for hepatocellular carcinoma. Oncogene 25(27), 3866-3884 (2006).
8. Esko JD, Lindahl U: Molecular diversity of heparan sulfate. J. Clin. Invest. 108(2), 169-173 (2001).
9. Kreuger J, Spillmann D, Li JP, Lindahl U: Interactions between heparan sulfate and proteins: the concept of specificity. J. Cell Biol. 174 (3), 323-327 (2006).
10. Ai X, Do AT, Kusche-Gullberg M, Lindahl U, Lu K, Emerson CP Jr: Substrate specificity and domain functions of extracellular heparan sulfate 6-O-endosulfatases, QSulf1 and QSulf2. J. Biol. Chem. 281(8), 4969-4976 (2006).
11. Lamanna WC, Baldwin RJ, Padva M et al.: Heparan sulfate 6.-O-endosulfatases: discrete in vivo activities and functional co-operativity. Biochem. J. 400(1), 63-73 (2006).
12. Lai JP, Chien JR, Moser DR et al.: hSulf1 sulfatase promotes apoptosis of hepatocellular cancer cells by decreasing heparin-binding growth factor signaling. Gastroenterology 126(1), 231-248 (20 04).
13. Lai JP, Yu C, Moser CD et al.: SULF1 inhibits tumor growth and potentiates the effects of histone deacerylase inhibitors in hepatocellular carcinoma. Gastroenterology 130(7), 2130-2144 (2006).
14. Morimoto-Tomita M, Uchimura K, Werb Z, Hemmerich S, Rosen SD: Cloning and Characterization of two extracellular heparin-degrading endosulfatases in mice and humans. J. Biol. Chem. 277(51), 49175-49185 (2002).
15. Sardiello M, Annunziata I, Roma G, Ballabio A: Sulfatases and sulfatase modifying factors: an exclusive and promiscuous relationship. Hum. Mol. Genet. 14(21), 3203-3217 (2005).
16. Lamanna WC, Kalus I, Padva M, Baldwin RJ, Merry CL, Dierks T: The heparmome - the enigma of encoding and decoding heparan sulfate sulfation. J. Biotechnol. 129(2), 290-307 (2007).
17. Ambasta RK, Ai X, Emerson CP Jr: Quail Sulf1 function requires asparagine-linked glycosylation. J. Biol. Chem. 282(47), 34492-34499 (2007).
18. Wittstock U, Fischer M, Svendsen I, Halkier BA: Cloning and characterization of two cDNAs encoding sulfatases in the Roman snail, Helix pomatia. IUBMB Life 49(1), 71-76 (2000).
19. von Figura K, Schmidt B, Selmer T, Dierks T: A novel protein modification generating an aldehyde group in sulfatases: its role in catalysis and disease. Bioessays 20(6), 505-510 (1998).
20. Dierks T, Lecca MR, Schlotterhose P, Schmidt B, von Figura K: Sequence determinants directing conversion of cysteine to formylglycine in eukaryotic sulfatases. Embo J. 18(8), 2084-2091 (1999).
21. Dierks T, Schmidt B, Borissenko LV et al.: Multiple sulfarase deficiency is caused by mutations in the gene encoding the human C(α)-formylglycine generating enzyme. Cell 113(4), 435-444 (2003).
22. Von Bulow R, Schmidt B, Dierks T, von Figura K, Uson I: Crystal structure of an enzyme-substrate complex provides insight into the interaction between human arylsulfatase A and its substrates during catalysis. J. Mol. Biol. 305(2), 269-277 (2001).
23. Boltes I, Czapinska H, Kahnert A et al.: 1.3 A structure of arylsulfatase from Pseudomonas aeruginosa establishes the catalytic mechanism of sulfate ester cleavage in the sulfatase family. Structure 9(6), 483-491 (2001).
24. Hanson SR, Best MD, Wong CH: Sulfatases: structure, mechanism, biological activity, inhibition, and synthetic utility. Angew Chem. Int. Ed. Engl. 43(43), 5736-5763 (2004).
25. Bennett-Lovsey RM, Herbert AD, Sternberg MJ, Kelley LA: Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre. Proteins 70(3), 611-625 (2008).
26. Dhoot GK, Gustafsson MK, Ai X, Sun W, Standiford DM, Emerson CP Jr: Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science 293(5535), 1663-1666 (2001).
27. Wei G, Bai X, Gabb MM et al.: Location of the glucuronosyltransferase domain in the heparan sulfate copolymerase EXT1 by analysis of Chinese banister ovary cell mutants. J. Biol. Chem. 275(36), 27733-27740 (2000).
28. Shridhar V, Sen A, Chien J et al.: Identification of underexpressed genes in early- and late-stage primary ovarian tumors by suppression subtraction hybridization. Cancer Res. 62(1), 262-270 (2002).
29. Lai J, Chien J, Staub J et al.: Loss of HSulf-1 up-regulates heparin-binding growth factor signaling in cancer. J. Biol. Chem. 278(25), 23107-23117 (2003).
30. David G, Bai XM, Van der Schueren B, Cassiman JJ, Van den Berghe H: Developmental changes in heparan sulfate expression: in situ detection with mAbs. J. Cell Biol. 119(4), 961-975 (1992).
31. Bai XM, Van der Schueren B, Cassiman JJ, Van den Berghe H, David G: Differential expression of multiple cell-surface heparan sulfate proteoglycans during embryonic tooth development. J. Histochem. Cytochem. 42(8), 1043-1054 (1994).
32. Nackaerts K, Verbeken E, Deneffe G, Vanderschueren B, Demedts M, David G: Heparan sulfate proteoglycan expression in human lung-cancer cells. Int. J. Cancer 74(3), 335-345 (1997).
33. van den Born J, Salmivirta K, Henttinen T et al.: Novel heparan sulfate structures revealed by monoclonal antibodies. J. Biol. Chem. 280(21), 20516-20523 (2005).
34. Li J, Kleeff J, Abiatari I et al.: Enhanced levels of Hsulf-1 interfere with heparin-binding growth factor signaling in pancreatic cancer. Mol. Cancer 4(1), 14 (2005).
35. Lundin L, Larsson H, Kreuger J et al.: Selectively desulfated heparin inhibits fibroblast growth factor-induced mitogenicity and angiogenesis. J. Biol. Chem. 275(32), 24653-24660 (2000).
36. Delehedde M, Lyon M, Gallagher JT, Rudland PS, Fernig DG: Fibroblast growth factor-2 binds to small heparin-derived oligosaccharides and, stimulates a sustained phosphorylation of p42/44 mitogen-activated protein kinase and proliferation of rat mammary fibroblasts. Biochem. J. 366(Pt 1), 235-244 (2002).
37. Mohammadi M, Schlessinger J, Hubbard SR: Structure of the FGF receptor tyrosine kinase domain reveals a novel autoinhibitory mechanism. Cell 86(4), 577-587 (1996).
38. Schlessinger J, Plotnikov AN, Ibrahimi OA et al.: Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol. Cell 6(3), 743-750 (2000).
39. Lai JP, Chien J, Strome SE et al.: HSulf-1 modulates HGF-mediated tumor cell invasion and signaling in head and neck squamous carcinoma. Oncogene 23(7), 1439-1447 (2004).
40. Dong G, Chen Z, Li ZY, Yeh NT, Bancroft CC, Van Waes C: Hepatocyte growth factor/scatter factor-induced activation of MEK and PI3K signal pathways contributes to expression of proangiogenic cytokines interleukin-8 and vascular lendothelial growth factor in head and neck squamous cell carcinoma. Cancer Res. 61(15), 5911-5918 (2001).
41. Zeng M, Kumar A, Meng G et al.: Human papilloma virus 16 E6 oncoprotein inhibits retinoic X receptor-mediated transactivation by targeting human ADA3 coactivator. J. Biol. Chem. 277(47), 45611-45618 (2002).
42. Matsumoto K, Matsumoto K, Nakamura T, Kramer RH: Hepatocyte growth factor/scatter factor induces tyrosine phosphorylation of focal adhesion kinase (p125FAK) and promotes migration and invasion by oral squamous cell carcinoma cells. J. Biol. Chem. 269(50), 31807-31813 (1994).
43. Galeazzi E, Olivero M, Gervasio FC et al.: Detection of MET oncogene/hepatocyte growth factor receptor in lymph node metastases from head and neck squamous cell carcinomas. Eur. Arch. Otorhinolaryngol. 254(Suppl. 1), S138-S143 (1997).
44. Narita K, Staub J, Chien J et al.: HSulf-1 inhibits angiogenesis and tumorigenesis in vivo. Cancer Res. 66(12), 6025-6032 (2006).
45. Lai JP, Sandhu DS, Yu C et al.: Sulfatase 2 up-regulates glypican 3, promotes fibroblast growth factor signaling, and decreases survival in hepatocellular carcinoma. Hepatology 47(4), 1211-1222 (2008).
46. Lee JS, Chu IS, Heo J et al.: Classification and prediction of survival in hepatocellular carcinoma by gene expression profiling. Hepatology 40(3), 667-676 (2004).
47. Dai Q, Qian SB, Li HH et al.: Regulation of the cytoplasmic quality control protein degradation pathway by BAG2. J. Biol. Chem. 280(46), 38673-38681 (2005).
48. Morimoto-Tomita M, Uchimura K, Bistrup A et al.: Sulf-2, a proangiogenic heparan sulfate endosulfatase, is upregulated in breast cancer. Neoplasia 7(11), 1001-1010 (2005).
49. Uchimura K, Morimoto-Tomita M, Bistrup A et al. HSulf-2, an extracellular endoglucosamine-6-sulfatase, selectively mobilizes heparin-bound growth factors and chemokines: effects on VEGF, FGF-1, and SDF-1. BMC Biochem. 7, 2 (2006).
50. Sjoblom T, Jones S, Wood LD et al.: The consensus coding sequences of human breast and colorectal cancers. Science 314(5797), 268-274 (2006).
51. Nawroth R, van Zante A, Cervantes S, McManus M, Hebrok-M, Rosen SD: Extracellular sulfatases, elements of the Wnt signaling pathway, positively regulate growth and tumorigenicity of human pancreatic cancer cells. PLoS ONE 2(4), e392 (2007).
52. Chekhun VF, Lukyanova NY, Kovalchuk O, Tryndyak VP, Pogribny IP: Epigenetic profiling of multidrug-resistant human MCF-7 breast adenocarcinoma cells reveals novel hyper- and hypomethylated targets. Mol. Cancer Ther. 6(3), 1089-1098 (2007).
53. Lee JS, Heo J, Libbrecht L et al.: A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells. Nat. Med. 42(4), 410-416 (2006).
54. Capurro M, Wanless IR, Sherman M et al.: Glypican-3: a novel serum and histochemical marker for hepatocellular carcinoma. Gastroenterology 125(1), 89-97 (2003).
55. Capurro MI, Shi W, Sandal S, Filmus J: Processing by convertases is not required for glypican-3-induced stimulation of, hepatocellular carcinoma growth. J. Biol. Chem. 280(50), 41201-41206 (2005).
56. Cheng W, Tseng CJ, Lin TT et al.: Glypican-3-mediated oncogenesis involves the IGF signaling pathway. Carcinogenesis 29(7), 1319-1326 (2008).
57. Lum DH, Tan J, Rosen SD, Werb Z: Gene trap disruption of the mouse heparan sulfate 6-O-endosulfatase gene, Sulf2. Mol. Cell Biol. 27(2), 678-688 (2007).
58. Holst CR, Bou-Reslan H, Gore BB et al.: Secreted sulfatases Sulf1 and Sulf2 have overlapping yet essential roles in mouse neonatal survival. PLoS ONE 2(6), E575 (2007).
59. Ai X, Kitazawa T, Do AT, Kusche-Gullberg M, Labosky PA, Emerson CP Jr: SULF1 and SULF2 regulate heparan sulfate-mediated GDNF signaling for esophageal innervation. Development 134(18), 3327-3338 (2007).
60. Langsdorf A, Do AT, Kusche-Gullberg M, Emerson CP Jr, Ai X: Sulfs are regulators of growth factor signaling for satellite cell differentiation and muscle regeneration. Dev. Biol. 311(2), 464-477 (2007).
61. Ratzka A, Kalus I, Moser M, Dierks T, Mundlos S, Vortkamp A: Redundant function of the heparan sulfate 6-O-endosulfatases Sulf1 and Sulf2 during skeletal development. Dev. Dyn. 237(2), 339-353 (2008).