Inhibition of hyaluronan synthase-3 decreases subcutaneous colon cancer growth by increasing apoptosis

Anti-Cancer Agents in Medicinal Chemistry

Volumn 11, Issue 7, 2011, Pages 620-628

  Teng, Brian P ^a   Heffler, Melissa D ^a   Lai, Eric C ^a   Zhao, Ya Li ^a   LeVea, Charles M ^a   Golubovskaya, Vita M ^a   Bullarddunn, Kelli M ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

Apoptosis proliferation; Colon carcinoma; HCT116; Hyaluronan; Hyaluronan synthase; SW620

Indexed keywords

ANTINEOPLASTIC AGENT; HYALURONAN SYNTHASE 3; SMALL INTERFERING RNA; SYNTHETASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CARCINOGENESIS; CELL PROLIFERATION; COLON CANCER; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME SYNTHESIS; GENE SILENCING; GENETIC TRANSFECTION; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RNA SEQUENCE;

ANIMALS; APOPTOSIS; CASPASE 3; CELL PROLIFERATION; COLONIC NEOPLASMS; GLUCURONOSYLTRANSFERASE; HCT116 CELLS; HUMANS; HYALURONIC ACID; INJECTIONS, SUBCUTANEOUS; KI-67 ANTIGEN; MALE; MICE; MICE, INBRED C57BL; MICE, NUDE; RNA, SMALL INTERFERING; TRANSFECTION; TUMOR BURDEN; TUMOR MARKERS, BIOLOGICAL; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 80051714439     PISSN: 18715206     EISSN: 18755992     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Watanabe, K.; Yamaguchi, Y. Molecular identification of a putative human hyaluronan synthase. J. Biol. Chem., 1996, 271, 22945-22948.
2. Menzel, E.; Farr, C. Hyaluronidase and its substrate hyaluronan: biochemistry, biological activities and therapeutic uses. Cancer Letters, 1998, 131, 3-11.
3. Simpson, M.; Wilson, C.; Furcht, L.; Spicer, A.; Oegema, T.; McCarthy, J. Manipulation of hyaluronan synthase expression in prostate adenocarcinoma cells alters pericellular matrix retention and adhesion to bone marrow endothelial cells. J. Biol. Chem., 2002, 277(12), 10050-10057.
4. Bullard, K.; Kim, H.-R.; Wheeler, M.; Wilson, C.; Neudauer, C.; Simpson, M.; McCarthy, J. Hyaluronan synthase-3 is upregulated in metastatic colon carcinoma cells and manipulation of expression alters matrix retention and cellular growth. Int. J. Cancer, 2003, 107(5), 739-746.
5. Kim, H.-R.; Wheeler, M.; Wilson, C.; Iida, J.; Eng, D.; Simpson, M.; McCarthy, J.; Bullard, K. Hyaluronan facilitates invasion of colon carcinoma cells in vitro via interaction with CD44. Cancer Research, 2004, 64, 4569-4576.
6. Laurich, C.; Wheeler, M.; Iida, J.; Neudauer, C.; McCarthy, J.; Bullard, K. Hyaluronan mediates adhesion of metastatic colon carcinoma cells. J. Surg. Res., 2004, 122, 70-74.
7. Kosaki, R.; Watanabe, K.; Yamaguchi, Y. Overproduction of hyaluronan by expression of the hyaluronan synthase Has2 enhances anchorage independent growth and tumorigenecity. Cancer Research, 1999, 59, 1141-1145.
8. Itano, N.; Fukiko, A.; Sawai, T.; Yamada, Y.; Miyaishi, O.; Senga, T.; Hamaguchi, M.; Kimata, K. Abnormal accumulation of hyaluronan matrix diminishes contact inhibition of cell growth and promotes cell migration. Proc. Natl. Acad. Sci. USA, 2002, 99(6), 3609-3614.
9. Itano, N.; Sawai, T.; Miyaishi, O.; Kimata, K. Relationship between hyaluronan production and metastatic potential of mouse mammary carcinoma cells. Cancer Research, 1999, 59, 2499-2504.
10. Ropponen, K.; Tammi, M.; Parkkinen, J.; Eskelinen, M.; Tammi, R.; Lipponen, P.; Agren, U.; Alhava, E.; Kosma, V.-M. Tumor cellassociated hyaluronan as an unfavorable prognostic factor in colorectal cancer. Cancer Research, 1998, 58, 342-347.
11. Wang, C.; Tammi, M.; Guo, H.; Tammi, R. Hyaluronan distribution in the normal epithelium of esophagus, stomach, and colon and their cancers. Am. J. Pathol., 1996, 148, 1861-1869.
12. Bullard Dunn, K.; Lee, P.; Wilson, C.; Iida, J.; Wasiluk, K.; Wheeler, M.; McCarthy, J. Inhibition of Hyaluronan synthase-3 decreases MMP-7 expression and activity. Surgery 2009, 145, 322-329.
13. Lai, E.; Singh, R.; Teng, B.; Zhao, Y.-L.; Sharratt, E.; Howell, G.; Rajput, A.; Bullard Dunn, K. Inhibition of hyaluronan synthase-3 decreases subcutaneous colon cancer growth in mice. Dis. Colon Rectum, 2010, 53, 475-482.
14. Rajput, A.; Dominguez San Martin, I.; Rose, R.; Beko, A.; Levea, C.; Sharratt, E.; Mazurchuk, R.; Hoffman, R.M.; Brattain, M.G.; Wang, J. Characterization of HCT116 human colon cancer cells in an orthotopic model. J. Surg. Res., 2008, 147(2), 276-281.
15. Manual of Histologic Staining Methods of the Armed Forces Institute of Pathology, 3rd ed.; McGraw-Hill Book Co.: New York, 1968.
16. Simpson, M.; Wilson, C.; McCarthy, J. Inhibition of prostate tumor cell hyaluronan synthesis impairs subcutaneous growth and vascularization in immunocompromised mice. Am. J. Pathol., 2002, 161(3), 849-857.
17. Auvinen, P.; Tammi, R.; Parkkinen, J.; Tammi, M.; Agren, U.; Johanddon, R.; Hirvikoski, P.; Eskelinen, M.; Kosma, V.-M. Hyaluronan in peritumoral stroma and malignant cells associates with breast cancer spreading and predicts survival. Am. J. Pathol., 2000, 156, 529-536.
18. Ghatak, S.; Misra, S.; Toole, B. Hyaluronan oligosaccharides inhibit anchorage-independent growth of tumor cells by suppressing the phosphoinosotide 3-kinase/Akt cell survival pathway. J. Biol. Chem., 2002, 277(41), 38013-38020.
19. Peng, H.; Zhou, J.L.; Liu, S.Q.; Hu, Q.J.; Ming, J.H.; Qiu, B. Hyaluronic acid inhibits nitric oxide-induced apoptosis and dedifferentiation of articular chondrocytes in vitro. Inflamm. Res., 59(7), 519-530.
20. Pauloin, T.; Dutot, M.; Joly, F.; Warnet, J.M.; Rat, P. High molecular weight hyaluronan decreases UVB-induced apoptosis and inflammation in human epithelial corneal cells. Molecular vision, 2009, 15, 577-83.
21. Lokeshwar, V.B.; Lopez, L.E.; Munoz, D.; Chi, A.; Shirodkar, S.P.; Lokeshwar, S.D.; Escudero, D.O.; Dhir, N.; Altman, N. Antitumor activity of hyaluronic acid synthesis inhibitor 4- methylumbelliferone in prostate cancer cells. Cancer Research, 70(7), 2613-26123.
22. Bourguignon, L.Y.; Spevak, C.C.; Wong, G.; Xia, W.; Gilad, E. Hyaluronan-CD44 interaction with protein kinase C(epsilon) promotes oncogenic signaling by the stem cell marker Nanog and the Production of microRNA-21, leading to down-regulation of the tumor suppressor protein PDCD4, anti-apoptosis, and chemotherapy resistance in breast tumor cells. J. Biol. Chem., 2009, 284(39), 26533-26546.
23. Edward, M.; Quinn, J.A.; Pasonen-Seppanen, S.M.; McCann, B.A.; Tammi, R.H. 4-Methylumbelliferone inhibits tumour cell growth and the activation of stromal hyaluronan synthesis by melanoma cell-derived factors. Br. J. Dermatol., 2010, 162 (6), 1224-1232.
24. Torre, C.; Wang, S.J.; Xia, W.; Bourguignon, L.Y. Reduction of hyaluronan-CD44-mediated growth, migration, and cisplatin resistance in head and neck cancer due to inhibition of Rho kinase and PI-3 kinase signaling. Arch. Otolaryngol.--Head & Neck Surg., 136(5), 493-501.
25. Twarock, S.; Tammi, M.I.; Savani, R.C.; Fischer, J.W. Hyaluronan stabilizes focal adhesions, filopodia and the proliferative phenotype in esophageal squamous carcinoma cells. J. Biol. Chem., 2010, 285(30), 23276-23284.
26. Toole, B.P. Hyaluronan-CD44 Interactions in Cancer: Paradoxes and Possibilities. Clin. Cancer Res., 2009, 15(24), 7462-7468.
27. Assmann, V.; Gillett, C.; Poulsom, R.; Ryder, K.; Hart, I.; Hanby, A. The pattern of expression of the microtubule-binding protein RHAMM/IHABP in mammary carcinoma suggests a role in the invasive behaviour of tumour cells. J. Pathol., 2001, 195(2), 191-196.
28. Banerji, S.; Ni, J.; Wang, S.; Clasper, S.; Su, J.; Tammi, R.; Jones, M.; Jackson, D. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J. Cell Biol., 1999, 144(4), 789-801.
29. Bono, P.; Rubin, K.; Higgins, J.; Hynes, R. Layilin, a novel integral membrane protein, is a hyaluronan receptor. Mol Biol Cell, 2001, 12(4), 891-900.
30. Turley, E.; Noble, P.; Bourguignon, L. Signaling properties of hyaluronan receptors. J. Biol. Chem., 2002, 277, 4589-4592.
31. Weigel, J.; Weigel, P. Characterization of the recombinant rat 175-kDa hyaluronan receptor for endocytosis (HARE). J. Biol. Chem., 2003, 278(44), 42802-42811.
32. Politz, O.; Gratchev, A.; McCourt, P.; Schledzewski, K.; Guillot, P.; Johansson, S.; Svineng, G.; Franke, P.; Kannicht, C.; Kzhyshkowska, J.; Longati, P.; Velten, F.; Johansson, S.; Goerdt, S. Stabilin-1 and -2 constitute a novel family of fasciclin-like hyaluronan receptor homologues. Biochem. J., 2002, 362 (Pt. 2), 144-164.
33. Kopp, R.; Fichter, M.; Schalhorn, G.; Danescu, J.; Classen, S. Frequent expression of the high molecular, 673-bp CD44v3,v8-10 variant in colorectal adenomas and carcinomas. Inter. J. Molecul. Med., 2009, 24(5), 677-683.
34. Yamada, Y.; Itano, N.; Narimatsu, H.; Kudo, T.; Hirohashi, S.; Ochiai, A.; Niimi, A.; Ueda, M.; Kimata, K. Receptor for hyaluronan-mediated motility and CD44 expression in colon cancer assessed by quantitative analysis using real-time reverse transcriptase- polymerase chain reaction. Jpn. J.Cancer Res., 1999, 90(9), 987-992.
35. Zlobec, I.; Baker, K.; Terracciano, L.; Peter, S.; Degen, L.; Beglinger, C.; Lugli, A. Two-marker protein profile predicts poor prognosis in patients with early rectal cancer. Br. J. Cancer, 2008, 99(10), 1712-1717.
36. Lugli, A.; Zlobec, I.; Gunthert, U.; Minoo, P.; Baker, K.; Tornillo, L.; Terracciano, L.; Jass, J.R. Overexpression of the receptor for hyaluronic acid mediated motility is an independent adverse prognostic factor in colorectal cancer. Mod. Pathol., 2006, 19(10), 1302-1309.
37. Zlobec, I.; Baker, K.; Terracciano, L.M.; Lugli, A. RHAMM, p21 combined phenotype identifies microsatellite instability-high colorectal cancers with a highly adverse prognosis. Clin. Cancer Res., 2008, 14(12), 3798-806.
38. Nagel, S.; Hirschmann, P.; Dirnhofer, S.; Gunthert, U.; Tzankov, A. Coexpression of CD44 variant isoforms and receptor for hyaluronic acid-mediated motility (RHAMM, CD168) is an International Prognostic Index and C-MYC gene status-independent predictor of poor outcome in diffuse large B-cell lymphomas. Exper. Hematol., 38(1), 38-45.
39. Onoda, M.; Nakaseko, C.; Yokota, A.; Saito, Y. Ligation of CD44 with low-molecular-weight hyaluronan and a monoclonal antibody leads to inhibition of drug-induced apoptosis in a human myeloid cell line. Hematology (Amsterdam, Netherlands), 2009, 14(4), 213-9.
40. Misra, S.; Obeid, L.M.; Hannun, Y.A.; Minamisawa, S.; Berger, F.G.; Markwald, R.R.; Toole, B.P.; Ghatak, S. Hyaluronan constitutively regulates activation of COX-2-mediated cell survival activity in intestinal epithelial and colon carcinoma cells. J. Biol. Chem., 2008, 283(21), 14335-44.
41. Subramaniam, V.; Vincent, I.R.; Gilakjan, M.; Jothy, S. Suppression of human colon cancer tumors in nude mice by siRNA CD44 gene therapy. Exper. Molecul. Pathol., 2007, 83(3), 332-340.
42. Sohr, S.; Engeland, K. RHAMM is differentially expressed in the cell cycle and downregulated by the tumor suppressor p53. Cell cycle (Georgetown, Tex, 2008, 7(21), 3448-3460.
43. Tolg, C.; Hamilton, S.R.; Nakrieko, K.A.; Kooshesh, F.; Walton, P.; McCarthy, J.B.; Bissell, M.J.; Turley, E.A. Rhamm-/- fibroblasts are defective in CD44-mediated ERK1,2 motogenic signaling, leading to defective skin wound repair. J. Cell Biol., 2006, 175(6), 1017-1028.
44. Hamilton, S.R.; Fard, S.F.; Paiwand, F.F.; Tolg, C.; Veiseh, M.; Wang, C.; McCarthy, J.B.; Bissell, M.J.; Koropatnick, J.; Turley, E.A. The hyaluronan receptors CD44 and Rhamm (CD168) form complexes with ERK1,2 that sustain high basal motility in breast cancer cells. J. Biol. Chem., 2007, 282(22), 16667-16680.
45. Tolg, C.; Hamilton, S.J.; Morningsar, L.; Zhang, J.; Esguerra, K.V.; Telmer, P.G.; Luyt, L.G.; Harrison, R.; McCarthy, J.B.; Turley, E.A. RHAMM promotes interphase microtubule instability and mitotic spindle integrity through MEK1/ERK1, 2 activity. J. Biol. Chem., 2010, 285, 26461-26474.
46. Alaniz, L.; Rizzo, M.; Malvicini, M.; Jaunarena, J.; Avella, D.; Atorrasagasti, C.; Aquino, J.B.; Garcia, M.; Matar, P.; Silva, M.; Mazzolini, G. Low molecular weight hyaluronan inhibits colorectal carcinoma growth by decreasing tumor cell proliferation and stimulating immune response. Cancer Lett, 2009, 278(1), 9-16.
47. Sheehan, K.M.; DeLott, L.B.; West, R.A.; Bonnema, J.D.; DeHeer, D.H. Hyaluronic acid of high molecular weight inhibits proliferation and induces cell death in U937 macrophage cells. Life Sciences, 2004, 75(26), 3087-3102.
48. Itano, N.; Sawai, T.; Yoshida, M.; Lenas, P.; Yamada, Y.; Imagawa, M.; Shinomura, T.; Hamaguchi, M.; Yoshida, Y.; Ohnuki, Y.; Miyauchi, S.; Spicer, A.; McDonald, J.; Kimata, K. Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties. J. Biol. Chem., 1999, 274, 25085-25092.
49. Lee, P.; Windsperger, A.; Wilson, C.; McCarthy, J.; Wasiluk, K.; Rothenberger, D.; Bullard Dunn, K. The effect of a hyaluronanmethylcellulose membrane versus polyglactin 910 mesh on intraabdominal tumor formation in mice. Dis. Colon Rectum, 2008, 51(9), 1403-1407.
50. Gibbs, P.; Clingan, P.R.; Ganju, V.; Strickland, A.H.; Wong, S.S.; Tebbutt, N.C.; Underhill, C.R.; Fox, R.M.; Clavant, S.P.; Leung, J.; Pho, M.; Brown, T.J. Hyaluronan-Irinotecan improves progressionfree survival in 5-fluorouracil refractory patients with metastatic colorectal cancer: a randomized phase II trial. Cancer Chemother. Pharmacol., 2011, 67(1), 153-163.