Hyaluronan stimulates pancreatic cancer cell motility

Oncotarget

Volumn 7, Issue 4, 2016, Pages 4829-4840

  Cheng, Xiao Bo ^a,b   Kohi, Shiro ^a   Koga, Atsuhiro ^a   Hirata, Keiji ^a   Sato, Norihiro ^a  

^a UNIVERSITY OF OCCUPATIONAL AND ENVIRONMENTAL HEALTH   (Japan)

^b CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Hyaluronan; Hyaluronan synthase genes; Hyaluronidase genes; Migration; Pancreatic cancer

Indexed keywords

HYALURONIC ACID; HYALURONIDASE; MESSENGER RNA; GLUCURONOSYLTRANSFERASE; HYALURONAN SYNTHASE; IMMUNOLOGICAL ADJUVANT;

ARTICLE; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; FIBROBLAST; GENE EXPRESSION; GENETIC ASSOCIATION; HAS3 GENE; MOLECULAR SIZE; PANCREAS CANCER; REAL TIME POLYMERASE CHAIN REACTION; SHORT TANDEM REPEAT; TUMOR INVASION; APOPTOSIS; CARCINOMA, PANCREATIC DUCTAL; CELL MOTION; CELL PROLIFERATION; COCULTURE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PANCREATIC NEOPLASMS; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STROMA CELL; TUMOR CELL CULTURE; WESTERN BLOTTING; WOUND HEALING;

ADJUVANTS, IMMUNOLOGIC; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, PANCREATIC DUCTAL; CELL MOVEMENT; CELL PROLIFERATION; COCULTURE TECHNIQUES; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCURONOSYLTRANSFERASE; HUMANS; HYALURONIC ACID; PANCREATIC NEOPLASMS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STROMAL CELLS; TUMOR CELLS, CULTURED; WOUND HEALING;

EID: 84958025863     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6617     Document Type: Article

References (42)

1. Hidalgo M. Pancreatic cancer. N Engl J Med. 2010; 362:1605-1617.
2. Kelly E. Craven, Jesse Gore, Julie L. Wilson, Murray Korc. Angiogenic gene signature in human pancreatic cancer correlates with TGF-beta and inflammatory transcriptomes. Oncotarget. 2015; doi: 10.18632/oncotarget.6345.
3. Misra S, Hascall VC, Markwald RR, Ghatak S. Interactions between hyaluronan and its receptors (CD44, RHAMM) regulate the activities of inflammation and cancer. Front Immunol. 2015; 6:201.
4. Itano N, Kimata K. Mammalian hyaluronan synthases. IUBMB Life. 2002; 54:195-199.
5. Stern R. Hyaluronan catabolism: a new metabolic pathway. Eur J Cell Biol. 2004; 83:317-325.
6. Toole BP. Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer. 2004; 4:528-539.
7. Itano N, Zhuo L, Kimata K. Impact of the hyaluronan-rich tumor microenvironment on cancer initiation and progression. Cancer Sci. 2008; 99:1720-1725.
8. Sironen RK, Tammi M, Tammi R, Auvinen PK, Anttila M, Kosma VM. Hyaluronan in human malignancies. Exp Cell Res. 2011; 317:383-391.
9. Itano N, Atsumi F, 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 U S A. 2002; 99:3609-3614.
10. Toole BP, Slomiany MG. Hyaluronan: a constitutive regulator of chemoresistance and malignancy in cancer cells. Semin Cancer Biol. 2008; 18:244-250.
11. Wu M, Cao M, He Y, Liu Y, Yang C, Du Y, Wang W, Gao F. A novel role of low molecular weight hyaluronan in breast cancer metastasis. FASEB J. 2015; 29:1290-1298.
12. Schmaus A, Klusmeier S, Rothley M, Dimmler A, Sipos B, Faller G, Thiele W, Allgayer H, Hohenberger P, Post S, Sleeman JP. Accumulation of small hyaluronan oligosaccharides in tumour interstitial fluid correlates with lymphatic invasion and lymph node metastasis. Br J Cancer. 2014; 111:559-567.
13. Karbownik MS, Nowak JZ. Hyaluronan: towards novel anti-cancer therapeutics. Pharmacol Rep. 2013; 65:1056-1074.
14. Theocharis AD, Tsara ME, Papageorgacopoulou N, Karavias DD, Theocharis DA. Pancreatic carcinoma is characterized by elevated content of hyaluronan and chondroitin sulfate with altered disaccharide composition. Biochim Biophys Acta. 2000; 1502:201-206.
15. Fries H, Elsasser HP, Mahlbacher V, Neumann K, Kern HF. Localisation of hyaluronate (HA) in primary tumors and nude mouse xenografts of human pancreatic carcinomas using a biotinylated HA-binding protein. Virchows Arch. 1994; 424:7-12.
16. Mahlbacher V, Sewing A, Elsasser HP, Kern HF. Hyaluronan is a secretory product of human pancreatic adenocarcinoma cells. Eur J Cell Biol. 1992; 58:28-34.
17. Cheng XB, Sato N, Kohi S, Yamaguchi K. Prognostic impact of hyaluronan and its regulators in pancreatic ductal adenocarcinoma. PLoS One. 2013; 8:e80765.
18. Kultti A, Zhao C, Singha NC, Zimmerman S, Osgood RJ, Symons R, Jiang P, Li X, Thompson CB, Infante JR, Jacobetz MA, Tuveson DA, Frost GI, et al. Accumulation of extracellular hyaluronan by hyaluronan synthase 3 promotes tumor growth and modulates the pancreatic cancer microenvironment. Biomed Res Int. 2014; 2014:817613.
19. Nakamura T, Takagaki K, Shibata S, Tanaka K, Higuchi T, Endo M. Hyaluronic-acid-deficient extracellular matrix induced by addition of 4-methylumbelliferone to the medium of cultured human skin fibroblasts. Biochem Biophys Res Commun. 1995; 208:470-475.
20. Kakizaki I, Kojima K, Takagaki K, Endo M, Kannagi R, Ito M, Maruo Y, Sato H, Yasuda T, Mita S, Kimata K, Itano N. A novel mechanism for the inhibition of hyaluronan biosynthesis by 4-methylumbelliferone. J Biol Chem. 2004; 279:33281-33289.
21. Ullrich SJ, Hawkes SP. The effect of the tumor promoter, phorbol myristate acetate (PMA), on hyaluronic acid (HA) synthesis by chicken embryo fibroblasts. Exp Cell Res. 1983; 148:377-386.
22. Heldin P, Asplund T, Ytterberg D, Thelin S, Laurent TC. Characterization of the molecular mechanism involved in the activation of hyaluronan synthetase by platelet-derived growth factor in human mesothelial cells. Biochem J. 1992; 283:165-170.
23. Knudson W, Biswas C, Toole BP. Interactions between human tumor cells and fibroblasts stimulate hyaluronate synthesis. Proc Natl Acad Sci U S A. 1984; 81:6767-6771.
24. Itano N, Sawai T, Atsumi F, Miyaishi O, Taniguchi S, Kannagi R, Hamaguchi M, Kimata K. Selective expression and functional characteristics of three mammalian hyaluronan synthases in oncogenic malignant transformation. J Biol Chem. 2004; 279:18679-18687.
25. Tian X, Azpurua J, Hine C, Vaidya A, Myakishev-Rempel M, Ablaeva J, Mao Z, Nevo E, Gorbunova V, Seluanov A. High-molecular-mass hyaluronan mediates the cancer resistance of the naked mole rat. Nature. 2013; 499:346-349.
26. West DC, Hampson IN, Arnold F, Kumar S. Angiogenesis induced by degradation products of hyaluronic acid. Science. 1985; 228:1324-1326.
27. Sugahara KN, Murai T, Nishinakamura H, Kawashima H, Saya H, Miyasaka M. Hyaluronan oligosaccharides induce CD44 cleavage and promote cell migration in CD44-expressing tumor cells. J Biol Chem. 2003; 278:32259-32265.
28. Mahadevan D, Von Hoff DD. Tumor-stroma interactions in pancreatic ductal adenocarcinoma. Mol Cancer Ther. 2007; 6:1186-1197.
29. Pandol S, Edderkaoui M, Gukovsky I, Lugea A, Gukovskaya A. Desmoplasia of pancreatic ductal adenocarcinoma. Clin Gastroenterol Hepatol. 2009; 7:S44-47.
30. Hwang RF, Moore T, Arumugam T, Ramachandran V, Amos KD, Rivera A, Ji B, Evans DB, Logsdon CD. Cancerassociated stromal fibroblasts promote pancreatic tumor progression. Cancer Res. 2008; 68:918-926.
31. Sato N, Maehara N, Goggins M. Gene expression profiling of tumor-stromal interactions between pancreatic cancer cells and stromal fibroblasts. Cancer Res. 2004; 64:6950-6956.
32. Uchakina ON, Ban H, McKallip RJ. Targeting hyaluronic acid production for the treatment of leukemia: treatment with 4-methylumbelliferone leads to induction of MAPKmediated apoptosis in K562 leukemia. Leuk Res. 2013; 37:1294-1301.
33. Urakawa H, Nishida Y, Wasa J, Arai E, Zhuo L, Kimata K, Kozawa E, Futamura N, Ishiguro N. Inhibition of hyaluronan synthesis in breast cancer cells by 4-methylumbelliferone suppresses tumorigenicity in vitro and metastatic lesions of bone in vivo. Int J Cancer. 2012; 130:454-466.
34. Twarock S, Tammi MI, Savani RC, Fischer JW. Hyaluronan stabilizes focal adhesions, filopodia, and the proliferative phenotype in esophageal squamous carcinoma cells. J Biol Chem. 2010; 285:23276-23284.
35. Lokeshwar VB, Lopez LE, Munoz D, Chi A, Shirodkar SP, Lokeshwar SD, Escudero DO, Dhir N, Altman N. Antitumor activity of hyaluronic acid synthesis inhibitor 4-methylumbelliferone in prostate cancer cells. Cancer Res. 2010; 70:2613-2623.
36. Hajime M, Shuichi Y, Makoto N, Masanori Y, Ikuko K, Atsushi K, Mutsuo S, Keiichi T. Inhibitory effect of 4-methylesculetin on hyaluronan synthesis slows the development of human pancreatic cancer in vitro and in nude mice. Int J Cancer. 2007; 120:2704-2709.
37. Yoshihara S, Kon A, Kudo D, Nakazawa H, Kakizaki I, Sasaki M, Endo M, Takagaki K. A hyaluronan synthase suppressor, 4-methylumbelliferone, inhibits liver metastasis of melanoma cells. FEBS Lett. 2005; 579:2722-2726.
38. Nagy N, Kuipers HF, Frymoyer AR, Ishak HD, Bollyky JB, Wight TN, Bollyky PL. 4-methylumbelliferone treatment and hyaluronan inhibition as a therapeutic strategy in inflammation, autoimmunity, and cancer. Front Immunol. 2015; 6:123.
39. Yates TJ, Lopez LE, Lokeshwar SD, Ortiz N, Kallifatidis G, Jordan A, Hoye K, Altman N, Lokeshwar VB. Dietary supplement 4-methylumbelliferone: an effective chemopreventive and therapeutic agent for prostate cancer. J Natl Cancer Inst. 2015; 107:djv085.
40. Provenzano PP, Cuevas C, Chang AE, Goel VK, Von Hoff DD, Hingorani SR. Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell. 2012; 21:418-429.
41. Jacobetz MA, Chan DS, Neesse A, Bapiro TE, Cook N, Frese KK, Feig C, Nakagawa T, Caldwell ME, Zecchini HI, Lolkema MP, Jiang P, Kultti A, et al. Hyaluronan impairs vascular function and drug delivery in a mouse model of pancreatic cancer. Gut. 2013; 62:112-120.
42. Cheng XB, Sato N, Kohi S, Koga A, Hirata K. Receptor for hyaluronic acid-mediated motility is associated with poor survival in pancreatic ductal adenocarcinoma. J Cancer. 2015; 6:1093-1098.