Home LiteratureArticle Details
PMID: 23300607 Published · ppublish English Journal Article

PG545, a heparan sulfate mimetic, reduces heparanase expression in vivo, blocks spontaneous metastases and enhances overall survival in the 4T1 breast carcinoma model.

PloS one ·Vol. 7 ·No. 12 ·2012-00-00 ·Pages e52175

Hammond E, Brandt R, Dredge K

Abstract

PG545 is a clinically relevant heparan sulfate (HS) mimetic which, in addition to possessing anti-angiogenic properties, also acts as a heparanase inhibitor which may differentiate its mechanism(s) of action from approved angiogenesis inhibitors. The degradation of HS by heparanase has been strongly implicated in cell dissemination and the metastatic process. Thus, the anti-metastatic activity of PG545 has been linked to the enzymatic function of heparanase - the only endoglycosidase known to cleave HS, an important component of the extracellular matrix (ECM) which represents a potential avenue for therapeutic intervention for certain metastatic cancer indications. Recent concerns raised about the paucity of overall survival as an endpoint in mouse models of clinically relevant metastasis led us to examine the effect of PG545 on the progression of both primary tumor growth and the spontaneously metastasizing disease in the 4T1 syngeneic breast carcinoma model in a non-surgical and surgical (mastectomy) setting. PG545 significantly inhibited primary tumor growth but importantly also inhibited lung metastasis in treated mice, an effect not observed with the tyrosine kinase inhibitor sorafenib. Importantly, PG545 significantly enhanced overall survival compared to vehicle control and the sorafenib group, suggesting PG545's inhibitory effect on heparanase is indeed a critical attribute to induce anti-metastatic activity. In addition to blocking a common angiogenic signalling pathway in tumor cells, the expression of heparanase in the primary tumor and lung was also significantly reduced by PG545 treatment. These results support the ongoing development of PG545 and highlight the potential utility in metastatic disease settings.

MeSH Terms
Angiogenesis Inhibitors/pharmacology Animals Antineoplastic Agents/pharmacology Antineoplastic Combined Chemotherapy Protocols Cells, Cultured Disease Progression Enzyme-Linked Immunosorbent Assay Female Glucuronidase/antagonists & inhibitors,metabolism Human Umbilical Vein Endothelial Cells/drug effects Humans Immunoenzyme Techniques Lung Neoplasms/drug therapy,mortality,secondary Mammary Neoplasms, Experimental/drug therapy,mortality,pathology Mice Neovascularization, Pathologic/prevention & control Niacinamide/analogs & derivatives,pharmacology Phenylurea Compounds/pharmacology Saponins/pharmacology Sorafenib
Chemicals
Angiogenesis Inhibitors Antineoplastic Agents PG 545 Phenylurea Compounds Saponins Niacinamide Sorafenib heparanase Glucuronidase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Hammond Edward
Research and Development, Progen Pharmaceuticals, Darra, Queensland, Australia. [email protected]
Brandt Ralf
Dredge Keith
References (48)
48 references, click to expand
  1. An open letter to the FDA and other regulatory agencies: Preclinical drug development must consider the impact on metastasis.
    Clin Cancer Res. 2009 Jul 15;15:4529 PMID: 25278743
  2. Heparanase expression in circulating lymphocytes of breast cancer patients depends on the presence of the primary tumor and/or systemic metastasis.
    Neoplasia. 2007 Jun;9(6):504-10 PMID: 17603633
  3. Proteoglycans in health and disease: new concepts for heparanase function in tumor progression and metastasis.
    FEBS J. 2010 Oct;277(19):3890-903 PMID: 20840586
  4. Marine-derived oligosaccharide sulfate (JG3) suppresses heparanase-driven cell adhesion events in heparanase over-expressing CHO-K1 cells.
    Acta Pharmacol Sin. 2009 Jul;30(7):1033-8 PMID: 19543297
  5. Assessing the measure of a new drug: is survival the only thing that matters?
    J Clin Oncol. 2008 Apr 20;26(12):1922-3 PMID: 18421044
  6. Heparanase promotes growth, angiogenesis and survival of primary breast tumors.
    Int J Cancer. 2006 Apr 1;118(7):1609-17 PMID: 16217746
  7. The PG500 series: novel heparan sulfate mimetics as potent angiogenesis and heparanase inhibitors for cancer therapy.
    Invest New Drugs. 2010 Jun;28(3):276-83 PMID: 19357810
  8. Extending survival with chemotherapy in metastatic breast cancer.
    Oncologist. 2005;10 Suppl 3:20-9 PMID: 16368868
  9. Metastatic breast cancer: the treatment challenge.
    Clin Breast Cancer. 2008 Jun;8(3):224-33 PMID: 18650152
  10. MicroRNA-1258 suppresses breast cancer brain metastasis by targeting heparanase.
    Cancer Res. 2011 Feb 1;71(3):645-54 PMID: 21266359
  11. Rethinking the metastatic cascade as a therapeutic target.
    Nat Rev Clin Oncol. 2011 Jun;8(6):325-32 PMID: 21502993
  12. Heparanase as mediator of angiogenesis: mode of action.
    FASEB J. 2001 Jul;15(9):1661-3 PMID: 11427519
  13. Heparanase, a potential regulator of cell-matrix interactions.
    Trends Biochem Sci. 2000 Aug;25(8):349-51 PMID: 10916150
  14. Direct targeting of Sec23a by miR-200s influences cancer cell secretome and promotes metastatic colonization.
    Nat Med. 2011 Aug 07;17(9):1101-8 PMID: 21822286
  15. Preclinical therapeutic response of residual metastatic disease is distinct from its primary tumor of origin.
    Int J Cancer. 2012 Jan 1;130(1):190-9 PMID: 21312195
  16. Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths.
    CA Cancer J Clin. 2011 Jul-Aug;61(4):212-36 PMID: 21685461
  17. Heparanase-1 expression is associated with the metastatic potential of breast cancer.
    Surgery. 2002 Aug;132(2):326-33 PMID: 12219030
  18. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis.
    Cancer Cell. 2009 Mar 3;15(3):232-9 PMID: 19249681
  19. M402, a novel heparan sulfate mimetic, targets multiple pathways implicated in tumor progression and metastasis.
    PLoS One. 2011;6(6):e21106 PMID: 21698156
  20. Sulfated hexasaccharides attenuate metastasis by inhibition of P-selectin and heparanase.
    Neoplasia. 2011 May;13(5):445-52 PMID: 21532885
  21. Heparanase induces Akt phosphorylation via a lipid raft receptor.
    Biochem Biophys Res Commun. 2007 Oct 5;361(4):829-34 PMID: 17689495
  22. PG545, a dual heparanase and angiogenesis inhibitor, induces potent anti-tumour and anti-metastatic efficacy in preclinical models.
    Br J Cancer. 2011 Feb 15;104(4):635-42 PMID: 21285983
  23. Heparin/heparan sulphate-based drugs.
    Drug Discov Today. 2010 Dec;15(23-24):1058-69 PMID: 20974281
  24. Cancer metastasis as a therapeutic target.
    Eur J Cancer. 2010 May;46(7):1177-80 PMID: 20307970
  25. R428, a selective small molecule inhibitor of Axl kinase, blocks tumor spread and prolongs survival in models of metastatic breast cancer.
    Cancer Res. 2010 Feb 15;70(4):1544-54 PMID: 20145120
  26. A novel orthotopic model of breast cancer metastasis to bone.
    Clin Exp Metastasis. 1999 Mar;17(2):163-70 PMID: 10411109
  27. Antiangiogenic therapy, hypoxia, and metastasis: risky liaisons, or not?
    Nat Rev Clin Oncol. 2011 May 31;8(7):393-404 PMID: 21629216
  28. Erythromycin and clarithromycin modulation of growth factor-induced expression of heparanase mRNA on human lung cancer cells in vitro.
    Mediators Inflamm. 2001 Oct;10(5):259-67 PMID: 11759110
  29. Mutual enhancement between heparanase and vascular endothelial growth factor: a novel mechanism for melanoma progression.
    Cancer Lett. 2011 Sep 1;308(1):100-11 PMID: 21624769
  30. SST0001, a chemically modified heparin, inhibits myeloma growth and angiogenesis via disruption of the heparanase/syndecan-1 axis.
    Clin Cancer Res. 2011 Mar 15;17(6):1382-93 PMID: 21257720
  31. Cancer statistics, trends, and multiple primary cancer analyses from the Surveillance, Epidemiology, and End Results (SEER) Program.
    Oncologist. 2007 Jan;12(1):20-37 PMID: 17227898
  32. Heparanase, hyaluronan, and CD44 in cancers: a breast carcinoma perspective.
    Cancer Res. 2006 Nov 1;66(21):10233-7 PMID: 17079438
  33. Antitumor activity of a novel podophyllotoxin derivative (TOP-53) against lung cancer and lung metastatic cancer.
    Cancer Res. 1996 Jun 15;56(12):2809-14 PMID: 8665518
  34. In the end what matters most? A review of clinical endpoints in advanced breast cancer.
    Oncologist. 2011;16(1):25-35 PMID: 21212428
  35. Chemical Tumor Biology of Heparan Sulfate Proteoglycans.
    Curr Chem Biol. 2010 Jan 1;4(1):20-31 PMID: 20596243
  36. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis.
    Cancer Cell. 2009 Mar 3;15(3):220-31 PMID: 19249680
  37. Heparanase induces vascular endothelial growth factor expression: correlation with p38 phosphorylation levels and Src activation.
    Cancer Res. 2006 Feb 1;66(3):1455-63 PMID: 16452201
  38. Antiangiogenic therapy: impact on invasion, disease progression, and metastasis.
    Nat Rev Clin Oncol. 2011 Mar 01;8(4):210-21 PMID: 21364524
  39. Early growth response gene 1 (EGR1) regulates heparanase gene transcription in tumor cells.
    J Biol Chem. 2005 Oct 21;280(42):35136-47 PMID: 16093249
  40. An improved model to study tumor cell autonomous metastasis programs using MTLn3 cells and the Rag2(-/-) gammac (-/-) mouse.
    Clin Exp Metastasis. 2009;26(7):673-84 PMID: 19466569
  41. Guidelines for the welfare and use of animals in cancer research.
    Br J Cancer. 2010 May 25;102(11):1555-77 PMID: 20502460
  42. COX-2 induction by heparanase in the progression of breast cancer.
    Int J Mol Med. 2006 Feb;17(2):221-8 PMID: 16391819
  43. The impact of heparanese and heparin on cancer metastasis and angiogenesis.
    Pathophysiol Haemost Thromb. 2006;35(1-2):116-27 PMID: 16855356
  44. Tumor and host-mediated pathways of resistance and disease progression in response to antiangiogenic therapy.
    Clin Cancer Res. 2009 Aug 15;15(16):5020-5 PMID: 19671869
  45. Regulation of inducible heparanase gene transcription in activated T cells by early growth response 1.
    J Biol Chem. 2003 Dec 12;278(50):50377-85 PMID: 14522979
  46. Heparanase inhibitor PI-88 as adjuvant therapy for hepatocellular carcinoma after curative resection: a randomized phase II trial for safety and optimal dosage.
    J Hepatol. 2009 May;50(5):958-68 PMID: 19303160
  47. Heparanase: a target for drug discovery in cancer and inflammation.
    Br J Pharmacol. 2007 May;151(1):1-14 PMID: 17339837
  48. Ductal carcinoma in situ of the breast and heparanase-1 expression: a molecular explanation for more aggressive subtypes.
    J Am Coll Surg. 2005 Mar;200(3):328-35 PMID: 15737842
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
Published
2012-00-00
Epub
2012-00-26
Pages
e52175
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC3530599
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]