Inhibition of hyaluronan synthase-3 decreases subcutaneous colon cancer growth in mice

Diseases of the Colon and Rectum

Volumn 53, Issue 4, 2010, Pages 475-482

  Lai, Eric ^a   Singh, Rahul ^a   Teng, Brian ^a   Zhao, Yali ^b   Sharratt, Elizabeth ^b   Howell, Gillian ^c   Rajput, Ashwani ^d   Dunn, Kelli Bullard ^a,c  

^a UNIVERSITY AT BUFFALO   (United States)

^b ROSWELL PARK CANCER INSTITUTE   (United States)

^c NEBRASKA MEDICAL CENTER   (United States)

^d UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

Author keywords

Colon cancer; Hyaluronan; Hyaluronan synthase

Indexed keywords

HYALURONIC ACID; HYALURONIC ACID SYNTHASE 3; SMALL INTERFERING RNA; SYNTHETASE; UNCLASSIFIED DRUG; GLUCURONOSYLTRANSFERASE; HYALURONAN SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; COLON CANCER; CONTROLLED STUDY; ENZYME INHIBITION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LIVER METASTASIS; LUNG METASTASIS; MALE; METASTASIS INHIBITION; MOUSE; NONHUMAN; TREATMENT RESPONSE; TUMOR VOLUME; UPREGULATION; ANIMAL; APOPTOSIS; BAGG ALBINO MOUSE; COLON TUMOR; DRUG ANTAGONISM; ENZYME IMMUNOASSAY; ENZYMOLOGY; METABOLISM; NUDE MOUSE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE;

ANIMALS; APOPTOSIS; COLONIC NEOPLASMS; GLUCURONOSYLTRANSFERASE; IMMUNOENZYME TECHNIQUES; MICE; MICE, INBRED BALB C; MICE, NUDE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 77951931897     PISSN: 00123706     EISSN: 15300358     Source Type: Journal    
DOI: 10.1007/dcr.0b013e3181c87084     Document Type: Article

References (44)

1. Toole BP. Hyaluronan in morphogenesis. J Intern Med. 1997;242:35-40.
2. Menzel EJ, Farr C. Hyaluronidase and its substrate hyaluronan: biochemistry, biological activities and therapeutic uses. Cancer Lett. 1998;131:3-11.
3. Shyjan AM, Heldin P, Butcher EC, Yoshino T, Briskin MJ. Functional cloning of the cDNA for a human hyaluronan synthase. J Biol Chem. 1996;271:23395-23399.
4. Watanabe K, Yamaguchi Y. Molecular identification of a putative human hyaluronan synthase. J Biol Chem. 1996;271:22945-22948.
5. Spicer AP, McDonald JA. Characterization and molecular evolution of a vertebrate hyaluronan synthase gene family. J Biol Chem. 1998;273:1923-1932.
6. Itano N, Sawai T, Yoshida M, et al. Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties. J Biol Chem. 1999;274:25085-25092.
7. Kosaki R, Watanabe K, Yamaguchi Y. Overproduction of hyaluronan by expression of the hyaluronan synthase Has2 enhances anchorage-independent growth and tumorigenecity. Cancer Res. 1999;59:1141-1145.
8. Itano N, Sawai T, Miyaishi O, Kimata K. Relationship between hyaluronan production and metastatic potential of mouse mammary carcinoma cells. Cancer Res. 1999;59:2499-2504.
9. Simpson MA, Wilson CM, Furcht LT, Spicer AP, OegemaTR Jr, McCarthy JB. Manipulation of hyaluronan synthase expression in prostate adenocarcinoma cells alters pericellular matrix retention and adhesion to bone marrow endothelial cells. J Biol Chem. 2002;277:10050-10057.
10. Simpson MA, Wilson CM, McCarthy JB. Inhibition of prostate tumor cell hyaluronan synthesis impairs subcutaneous growth and vascularizationinimmunocompromised mice. AmJPathol. 2002;161:849-857.
11. Bullard KM, Kim HR, Wheeler MA, et al. Hyaluronan synthase-3 is upregulated in metastatic colon carcinoma cells and manipulation of expression alters matrix retention and cellular growth. Int J Cancer. 2003;107:739-746.
12. Laurich C, Wheeler MA, Iida J, Neudauer CL, McCarthy JB, Bullard KM. Hyaluronan mediates adhesion of metastatic colon carcinoma cells. J Surg Res. 2004;122:70-74.
13. Kim HR, Wheeler MA, Wilson CM, et al. Hyaluronan facilitates invasion of colon carcinoma cells in vitro via interaction with CD44. Cancer Res. 2004;64:4569-4576.
14. Kozlowski JM, Fidler IJ, Campbell D, Xu ZL, Kaighn ME, Hart IR. Metastatic behavior of human tumor cell lines grown in the nude mouse. Cancer Res. 1984;44:3522-3529.
15. Rajput A, Dominguez San Martin I, Rose R, et al. Characterization of HCT116 human colon cancer cells in an orthotopic model. J Surg Res. 2008;147:276-281.
16. Guo XN, Rajput A, Rose R, et al. Mutant PIK3CA-bearing colon cancer cells display increased metastasis in an orthotopic model. Cancer Res. 2007;67:5851-5858.
17. Knudson CB. Hyaluronan receptor-directed assembly of chondrocyte pericellular matrix. J Cell Biol. 1993;120:825-834.
18. Knudson CB, Knudson W. Hyaluronan-binding proteins in development, tissue homeostasis, and disease. FASEB J. 1993;7:1233-1241.
19. Arai H, Kang KY, Sato H, et al. Significance of the quantification and demonstration of hyaluronic acid in tissue specimens for the diagnosis of pleural mesothelioma. Am Rev Resp Dis. 1979;120:529-532.
20. Hopwood JJ, Dorfman A. Glycosaminglycan synthesis by Wilms' tumor. Pediatr Res. 1978;12:52-56.
21. Auvinen PK, Parkkinen JJ, Johansson RT, et al. Expression of hyaluronan in benign and malignant breast lesions. Int J Cancer. 1997;74:477-481.
22. Simpson MA, Reiland J, Burger SR, et al. Hyaluronan synthase elevation in metastatic prostate carcinoma cells correlates with hyaluronan surface retention, a prerequisite for rapid adhesion to bone marrow endothelial cells. J Biol Chem. 2001;276:17949-17957.
23. Auvinen P, Tammi R, Parkkinen J, et al. Hyaluronan in peritumoral stroma and malignant cells associates with breast cancer spreading and predicts survival. Am J Pathol. 2000;156:529-536.
24. Setälä LP, Tammi MI, Tammi RH, et al. Hyaluronan expression in gastric cancer cells is associated with local and nodal spread and reduced survival rate. Br J Cancer. 1999;79:1133-1138.
25. Lovvorn HN III, Savani RC, Ruchelli E, Cass DL, Adzick NS. Serum hyaluronan and its association with unfavorable histology and aggressiveness of heterotransplanted Wilms' tumor. J Pediatr Surg. 2000;35:1070-1078.
26. Ropponen K, Tammi M, Parkkinen J, et al. Tumor cell-associated hyaluronan as an unfavorable prognostic factor in colorectal cancer. Cancer Res. 1998;58:342-347.
27. 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.
28. Ahrens T, Assmann V, Fieber C, et al. CD44 is the principal mediator of hyaluronic-acid-induced melanoma cell proliferation. J Invest Dermatol. 2001;116:93-101.
29. Assmann V, Gillett CE, Poulsom R, Ryder K, Hart IR, Hanby AM. The pattern of expression of the microtubule-binding protein RHAMM/IHABPinmammary carcinoma suggestsarole in the invasive behaviour of tumour cells. J Pathol. 2001;195:191-196.
30. Banerji S, Ni J, Wang SX, et al. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol. 1999;144:789-801.
31. Bono P, Rubin K, Higgins JM, Hynes RO. Layilin, a novel integral membrane protein, is a hyaluronan receptor. Mol Biol Cell. 2001;12:891-900.
32. Termeer C, Benedix F, Sleeman J, et al. Oligosaccharides of Hyaluronan activate dendritic cells via toll-like receptor 4. J Exp Med. 2002;195:99-111.
33. Toole BP. Hyaluronan promotes the malignant phenotype. Glycobiology. 2002;12:37R-42R.
34. Akiyama Y, Jung S, Salhia B, et al. Hyaluronate receptors mediating glioma cell migration and proliferation. J Neurooncol. 2001;53:115-127.
35. Duval A, Rolland S, Compoint A, et al. Evolution of instability at coding and non-coding repeat sequences in human MSI-H colorectal cancers. Hum Mol Genetics. 2001;10:513-518.
36. Brecht M, Mayer U, Schlosser E, Prehm P. Increased hyaluronate synthesis is required for fibroblast detachment and mitosis. Biochem J. 1986;239:445-450.
37. Matuoka K, Namba M, Mitsui Y. Hyaluronate synthetase inhibition by normal and transformed human fibroblasts during growth reduction. J Cell Biol. 1987;104:1105-1115.
38. Knudson W. Tumor-associated hyaluronan: providinganextracellular matrix that facilitates invasion. Am J Pathol. 1996;6:1721-1726.
39. Itano N, Atsumi F, Sawai T, et al. Abnormal accumulation of hyaluronan matrix diminishes contact inhibition of cell growth and promotes cell migration. Proc Natl Acad Sci U S A. 2002;99:3609-3614.
40. Dunn KM, Lee PK, Wilson CM, et al. Inhibition of hyaluronan synthases decreases matrix metalloproteinase-7 (MMP-7) expression and activity. Surgery. 2009;145:322-329.
41. Nishida Y, Knudson W, Knudson CB, Ishiguro N. Antisense inhibition of hyaluronan synthase-2 in human osteosarcoma cells inhibits hyaluronan retention and tumorigenicity. Exp Cell Res. 2005;307:194-203.
42. Udabage L, Brownlee GR, Waltham M, et al. Antisense-mediated suppression of hyaluronan synthase 2 inhibits the tumorigenesis and progression of breast cancer. Cancer Res. 2005;65:6139-6150.
43. Ghatak S, Misra S, Toole BP. Hyaluronan oligosaccharides inhibit anchorage-independent growth of tumor cells by suppressing the phosphoinositide 3-kinase/Akt cell survival pathway. J Biol Chem. 2002;277:38013-38020.
44. Lee PK, Windsperger AP, Wilson CM, et al. The effect of a hyaluronan-carboxymethylcellulose membrane vs. polyglactin 910 mesh on intra-abdominal tumor formation in mice. Dis Colon Rectum. 2008;51:1403-1407.