Heparanase 2 expression inversely correlates with bladder carcinoma grade and stage

Oncotarget

Volumn 7, Issue 16, 2016, Pages 22556-22565

  Gross Cohen, Miriam ^a   Feld, Sari ^a   Naroditsky, Inna ^b   Nativ, Ofer ^c   Ilan, Neta ^a   Vlodavsky, Israel ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b Rambam Health Care Campus ^*  (Israel)

^c BNAI ZION MEDICAL CENTER   (Israel)

Author keywords

Bladder cancer; Heparanase 2; LOX; Tumor grade; Tumor growth

Indexed keywords

COLLAGEN; HEPARANASE; HEPARANASE 2; PROTEIN LYSINE 6 OXIDASE; UNCLASSIFIED DRUG; BETA GLUCURONIDASE;

ADULT; AGED; ARTICLE; BLADDER CANCER CELL LINE; BLADDER CARCINOMA; BLADDER EPITHELIUM; CANCER GRADING; CANCER INHIBITION; CANCER STAGING; CELL DIFFERENTIATION; CELL MOTILITY; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ANALYSIS; ENZYME PURIFICATION; ENZYME REGULATION; ENZYME SYNTHESIS; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; MIGRATION INHIBITION; PROTEIN EXPRESSION; STROMA CELL; ANIMAL; BLADDER TUMOR; CARCINOMA; ENZYMOLOGY; METABOLISM; MIDDLE AGED; MOUSE; NONOBESE DIABETIC MOUSE; PATHOLOGY; RETROSPECTIVE STUDY; SCID MOUSE; TUMOR CELL LINE; VERY ELDERLY; XENOGRAFT;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CARCINOMA; CELL LINE, TUMOR; FEMALE; GLUCURONIDASE; HETEROGRAFTS; HUMANS; MALE; MICE; MICE, INBRED NOD; MICE, SCID; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM STAGING; RETROSPECTIVE STUDIES; URINARY BLADDER NEOPLASMS;

EID: 84965056853     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8003     Document Type: Article

References (32)

1. Arvatz G, Shafat I, Levy-Adam F, Ilan N and Vlodavsky I. The heparanase system and tumor metastasis: is heparanase the seed and soil? Cancer Metastasis Rev. 2011; 30:253-268.
2. Barash U, Cohen-Kaplan V, Dowek I, Sanderson RD, Ilan N and Vlodavsky I. Proteoglycans in health and disease: new concepts for heparanase function in tumor progression and metastasis. FEBS J. 2010; 277:3890-3903.
3. Barash U, Zohar Y, Wildbaum G, Beider K, Nagler A, Karin N, Ilan N and Vlodavsky I. Heparanase enhances myeloma progression via CXCL10 downregulation. Leukemia. 2014; 28:2178-2187.
4. Boyango I, Barash U, Naroditsky I, Li JP, Hammond E, Ilan N and Vlodavsky I. Heparanase cooperates with Ras to drive breast and skin tumorigenesis. Cancer Res. 2014; 74:4504-4514.
5. Ilan N, Elkin M and Vlodavsky I. Regulation, function and clinical significance of heparanase in cancer metastasis and angiogenesis. Intl J Biochem & Cell Biol. 2006; 38:2018-2039.
6. Ramani VC, Zhan F, He J, Barbieri P, Noseda A, Tricot G and Sanderson RD. Targeting heparanase overcomes chemoresistance and diminishes relapse in myeloma. Oncotarget. 2016; 7:1598-1607. doi: 10.18632/oncotarget.6408.
7. Shteingauz A, Boyango I, Naroditsky I, Hammond E, Gruber M, Doweck I, Ilan N and Vlodavsky I. Heparanase Enhances Tumor Growth and Chemoresistance by Promoting Autophagy. Cancer Res. 2015; 75:3946-3957.
8. Casu B, Vlodavsky I and Sanderson RD. Non-anticoagulant heparins and inhibition of cancer. Pathophysiol Haemost Thromb. 2008; 36:195-203.
9. Hammond E, Khurana A, Shridhar V and Dredge K. The role of heparanase and sulfatases in the modification of heparan sulfate proteoglycans within the tumor microenvironment and opportunities for novel cancer therapeutics. Front Oncol. 2014; 4:195.
10. Vlodavsky I, Beckhove P, Lerner I, Pisano C, Meirovitz A, Ilan N and Elkin M. Significance of heparanase in cancer and inflammation. Cancer Microenviron. 2012; 5:115-132.
11. McKenzie E, Tyson K, Stamps A, Smith P, Turner P, Barry R, Hircock M, Patel S, Barry E, Stubberfield C, Terrett J and Page M. Cloning and expression profiling of Hpa2, a novel mammalian heparanase family member. Biochem Biophys Res Commun. 2000; 276:1170-1177.
12. Levy-Adam F, Feld S, Cohen-Kaplan V, Shteingauz A, Gross M, Arvatz G, Naroditsky I, Ilan N, Doweck I and Vlodavsky I. Heparanase 2 interacts with heparan sulfate with high affinity and inhibits heparanase activity. J Biol Chem. 2010; 285:28010-28019.
13. Kutchuk L, Laitala A, Soueid-Bomgarten S, Shentzer P, Rosendahl AH, Eilot S, Grossman M, Sagi I, Sormunen R, Myllyharju J, Maki JM and Hasson P. Muscle composition is regulated by a Lox-TGFbeta feedback loop. Development. 2015; 142:983-993.
14. Barry-Hamilton V, Spangler R, Marshall D, McCauley S, Rodriguez HM, Oyasu M, Mikels A, Vaysberg M, Ghermazien H, Wai C, Garcia CA, Velayo AC, Jorgensen B, Biermann D, Tsai D, Green J, et al. Allosteric inhibition of lysyl oxidase-like-2 impedes the development of a pathologic microenvironment. Nat Med. 2010; 16:1009-1017.
15. Rodriguez C, Rodriguez-Sinovas A and Martinez-Gonzalez J. Lysyl oxidase as a potential therapeutic target. Drug News Perspect. 2008; 21:218-224.
16. Knowles MA and Hurst CD. Molecular biology of bladder cancer: new insights into pathogenesis and clinical diversity. Nat Rev Cancer. 2015; 15:25-41.
17. Soloway MS. Bladder cancer: Lack of progress in bladder cancer-what are the obstacles? Nat Rev Urol. 2013; 10:5-6.
18. Daly SB, Urquhart JE, Hilton E, McKenzie EA, Kammerer RA, Lewis M, Kerr B, Stuart H, Donnai D, Long DA, Burgu B, Aydogdu O, Derbent M, Garcia-Minaur S, Reardon W, Gener B, et al. Mutations in HPSE2 cause urofacial syndrome. Am J Hum Genet. 2010; 86:963-969.
19. Guo C, Kaneko S, Sun Y, Huang Y, Vlodavsky I, Li X and Li ZR. A mouse model of urofacial syndrome with dysfunctional urination. Hum Mol Genet. 2015; 24:1991-1999.
20. Wu G, Guo Z, Chang X, Kim MS, Nagpal JK, Liu J, Maki JM, Kivirikko KI, Ethier SP, Trink B and Sidransky D. LOXL1 and LOXL4 are epigenetically silenced and can inhibit ras/extracellular signal-regulated kinase signaling pathway in human bladder cancer. Cancer Res. 2007; 67:4123-4129.
21. Roberts NA, Woolf AS, Stuart HM, Thuret R, McKenzie EA, Newman WG and Hilton EN. Heparanase 2, mutated in urofacial syndrome, mediates peripheral neural development in Xenopus. Hum Mol Genet. 2014; 23:4302-4314.
22. Su Z, Yemul S, Estabrook A, Friedman R, Zimmer S and Fisher P. Transcriptional switching model for the regulation of tumorigenesis and metastasis by the ha-ras oncogene-transcriptional changes in the ha-ras tumor-suppressor gene lysyl oxidase. Int J Oncol. 1995; 7:1279-1284.
23. Tan RS, Taniguchi T and Harada H. Identification of the lysyl oxidase gene as target of the antioncogenic transcription factor, IRF-1, and its possible role in tumor suppression. Cancer Res. 1996; 56:2417-2421.
24. Barker HE, Cox TR and Erler JT. The rationale for targeting the LOX family in cancer. Nat Rev Cancer. 2012; 12:540-552.
25. Ochoa B. Can a congenital dysfunctional bladder be diagnosed from a smile? The Ochoa syndrome updated. Pediatr Nephrol. 2004; 19:6-12.
26. Pang J, Zhang S, Yang P, Hawkins-Lee B, Zhong J, Zhang Y, Ochoa B, Agundez JA, Voelckel MA, Fisher RB, Gu W, Xiong WC, Mei L, She JX and Wang CY. Loss-of-function mutations in HPSE2 cause the autosomal recessive urofacial syndrome. Am J Hum Genet. 2010; 86:957-962.
27. Stuart HM, Roberts NA, Hilton EN, McKenzie EA, Daly SB, Hadfield KD, Rahal JS, Gardiner NJ, Tanley SW, Lewis MA, Sites E, Angle B, Alves C, Lourenco T, Rodrigues M, Calado A, et al. Urinary tract effects of HPSE2 mutations. J Am Soc Nephrol. 2015; 26:797-804.
28. Liu G, Daneshgari F, Li M, Lin D, Lee U, Li T and Damaser MS. Bladder and urethral function in pelvic organ prolapsed lysyl oxidase like-1 knockout mice. BJU Int. 2007; 100:414-418.
29. Remus EW, O'Donnell RE, Jr., Rafferty K, Weiss D, Joseph G, Csiszar K, Fong SF and Taylor WR. The role of lysyl oxidase family members in the stabilization of abdominal aortic aneurysms. Am J Physiol Heart Cir Physiol. 2012; 303:H1067-1075.
30. Maki JM, Rasanen J, Tikkanen H, Sormunen R, Makikallio K, Kivirikko KI and Soininen R. Inactivation of the lysyl oxidase gene Lox leads to aortic aneurysms, cardiovascular dysfunction, and perinatal death in mice. Circulation. 2002; 106:2503-2509.
31. Gohji K, Okamoto M, Kitazawa S, Toyoshima M, Dong J, Katsuoka Y and Nakajima M. Heparanase protein and gene expression in bladder cancer. J Urol. 2001; 166:1286-1290.
32. Shafat I, Pode D, Peretz T, Ilan N, Vlodavsky I and Nisman B. Clinical significance of urine heparanase in bladder cancer progression. Neoplasia. 2008; 10:125-130.