Kalopanaxsaponin A inhibits the invasion of human oral squamous cell carcinoma by reducing metalloproteinase-9 mRNA stability and protein trafficking

Biological and Pharmaceutical Bulletin

Volumn 35, Issue 3, 2012, Pages 289-300

  Hwang, Young Sun ^a   Park, Kwang Kyun ^a,b   Chung, Won Yoon ^a,b  

^a Yonsei University College of Dentistry   (South Korea)

^b Yonsei University   (South Korea)

Author keywords

Anti invasive effect; HuR; Kalopanaxsaponin A; Metalloproteinase 9; Oral cancer; Ras associated binding 1A

Indexed keywords

BINDING PROTEIN; CYCLINE; GELATINASE B; HUR PROTEIN; KALOPANAXSAPONIN A; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAS ASSOCIATED BINDING PROTEIN 1A; SAPONIN DERIVATIVE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOACCUMULATION; CANCER INHIBITION; CANCER INVASION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; DOSE RESPONSE; ENZYME PHOSPHORYLATION; ENZYME RELEASE; FEMALE; HUMAN; HUMAN CELL; MOUSE; MOUTH CARCINOMA; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TRANSPORT; RNA STABILITY; SQUAMOUS CELL CARCINOMA;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL SURVIVAL; FEMALE; HUMANS; MATRIX METALLOPROTEINASE 9; MICE; MICE, NUDE; MOUTH NEOPLASMS; NEOPLASM INVASIVENESS; OLEANOLIC ACID; PROTEIN TRANSPORT; RNA, MESSENGER; SAPONINS; TETRADECANOYLPHORBOL ACETATE; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84857883685     PISSN: 09186158     EISSN: 13475215     Source Type: Journal    
DOI: 10.1248/bpb.35.289     Document Type: Article

References (49)

1. Warnakulasuriya S. Global epidemiology of oral and oropharyngeal cancer. Oral Oncol., 45, 309-316 (2009).
2. Kurahara S, Shinohara M, Ikebe T, Nakamura S, Beppu M, Hiraki A, Takeuchi H, Shirasuna K. Expression of MMPS, MT-MMP, and TIMPs in squamous cell carcinoma of the oral cavity: correlations with tumor invasion and metastasis. Head Neck, 21, 627-638 (1999).
3. Ikebe T, Shinohara M, Takeuchi H, Beppu M, Kurahara S, Nakamura S, Shirasuna K. Gelatinolytic activity of matrix metalloproteinase in tumor tissues correlates with the invasiveness of oral cancer. Clin. Exp. Metastasis, 17, 315-323 (1999).
4. Hong SD, Hong SP, Lee JI, Lim CY. Expression of matrix metalloproteinase-2 and -9 in oral squamous cell carcinomas with regard to the metastatic potential. Oral Oncol., 36, 207-213 (2000).
5. Liu SY, Liu YC, Huang WT, Huang GC, Su HJ, Lin MH. Requirement of MMP-3 in anchorage-independent growth of oral squamous cell carcinomas. J. Oral Pathol. Med., 36, 430-435 (2007).
6. Vairaktaris E, Serefoglou Z, Yapijakis C, Vylliotis A, Nkenke E, Derka S, Vassiliou S, Avgoustidis D, Neukam FW, Patsouris E. High gene expression of matrix metalloproteinase-7 is associated with early stages of oral cancer. Anticancer Res., 27(4B), 2493-2498 (2007).
7. Luukkaa H, Klemi P, Hirsimäki P, Vahlberg T, Kivisaari A, Kähäri VM, Grénman R. Matrix metalloproteinase (MMP)-1, -9 and -13 as prognostic factors in salivary gland cancer. Acta Otolaryngol., 128, 482-490 (2008).
8. Hohberger L, Wuertz BR, Xie H, Griffin T, Ondrey F. TNF-alpha drives matrix metalloproteinase-9 in squamous oral carcinogenesis. Laryngoscope, 118, 1395-1399 (2008).
9. Ohnishi Y, Lieger O, Attygalla M, Iizuka T, Kakudo K. Effects of epidermal growth factor on the invasion activity of the oral cancer cell lines HSC3 and SAS. Oral Oncol., 44, 1155-1159 (2008).
10. Sun L, Diamond ME, Ottaviano AJ, Joseph MJ, Ananthanarayan V, Munshi HG. Transforming growth factor-beta 1 promotes matrix metalloproteinase-9-mediated oral cancer invasion through snail expression. Mol. Cancer Res., 6, 10-20 (2008).
11. Juarez J, Clayman G, Nakajima M, Tanabe KK, Saya H, Nicolson GL, Boyd D. Role and regulation of expression of 92-kDa type-IV collagenase (MMP-9) in 2 invasive squamous-cell-carcinoma cell lines of the oral cavity. Int. J. Cancer, 55, 10-18 (1993).
12. Chiang YY, Tsai MH, Lin TY, Chiang IP. Expression profile of metastasis-related genes in invasive oral cancers. Histol. Histopathol., 23, 1213-1222 (2008).
13. de Vicente JC, Fresno MF, Villalain L, Vega JA, Hernández Vallejo G. Expression and clinical significance of matrix metalloproteinase-2 and matrix metalloproteinase-9 in oral squamous cell carcinoma. Oral Oncol., 41, 283-293 (2005).
14. Patel BP, Shah SV, Shukla SN, Shah PM, Patel PS. Clinical significance of MMP-2 and MMP-9 in patients with oral cancer. Head Neck, 29, 564-572 (2007).
15. Kim DW, Bang KH, Rhee YH, Lee KT, Park HJ. Growth inhibitory activities of kalopanaxsaponins A and I against human pathogenic fungi. Arch. Pharm. Res., 21, 688-691 (1998).
16. Kim YK, Kim RG, Park SJ, Ha JH, Choi JW, Park HJ, Lee KT. In vitro antiinflammatory activity of kalopanaxsaponin A isolated from Kalopanax pictus in murine macrophage RAW 264.7 cells. Biol. Pharm. Bull., 25, 472-476 (2002).
17. Lee KT, Sohn IC, Park HJ, Kim DW, Jung GO, Park KY. Essential moiety for antimutagenic and cytotoxic activity of hederagenin monodesmosides and bisdesmosides isolated from the stem bark of Kalopanax pictus. Planta Med., 66, 329-332 (2000).
18. Park HJ, Kwon SH, Lee JH, Lee KH, Miyamoto K, Lee KT. Kalopanaxsaponin A is a basic saponin structure for the anti-tumor activity of hederagenin monodesmosides. Planta Med., 67, 118-121 (2001).
19. Kumara SS, Huat BT. Extraction, isolation and characterisation of antitumor principle, alpha-hederin, from the seeds of Nigella sativa. Planta Med., 67, 29-32 (2001).
20. + influx and caspase-8 dependent pathways. Food Chem. Toxicol., 46, 3486-3492 (2008).
21. Cho HJ, Kang JH, Kwak JY, Lee TS, Lee IS, Park NG, Nakajima H, Magae J, Chang YC. Ascofuranone suppresses PMA-mediated matrix metalloproteinase-9 gene activation through the Ras/Raf/MEK/ERK- and Ap1-dependent mechanisms. Carcinogenesis, 28, 1104-1110 (2007).
22. Weng CJ, Chau CF, Hsieh YS, Yang SF, Yen GC. Lucidenic acid inhibits PMA-induced invasion of human hepatoma cells through inactivating MAPK/ERK signal transduction pathway and reducing binding activities of NF-kappaB and AP-1. Carcinogenesis, 29, 147-156 (2008).
23. Park SK, Hwang YS, Park KK, Park HJ, Seo JY, Chung WY. Kalopanaxsaponin A inhibits PMA-induced invasion by reducing matrix metalloproteinase-9 via PI3K/Akt- and PKCdelta-mediated signaling in MCF-7 human breast cancer cells. Carcinogenesis, 30, 1225-1233 (2009).
24. Shimada K, Uzawa K, Kato M, Endo Y, Shiiba M, Bukawa H, Yokoe H, Seki N, Tanzawa H. Aberrant expression of RAB1A in human tongue cancer. Br. J. Cancer, 92, 1915-1921 (2005).
25. Cha JD, Li S, Cha IH. Association between expression of embryonic lethal abnormal vision-like protein HuR and cyclooxygenase-2 in oral squamous cell carcinoma. Head Neck, 33, 627-637 (2011).
26. Lee EJ, Kim J, Lee SA, Kim EJ, Chun YC, Ryu MH, Yook JI. Characterization of newly established oral cancer cell lines derived from six squamous cell carcinoma and two mucoepidermoid carcinoma cells. Exp. Mol. Med., 37, 379-390 (2005).
27. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer, 2, 161-174 (2002).
28. Guttman D, Stern Y, Shpitzer T, Ulanovski D, Druzd T, Feinmesser R. Expression of MMP-9, TIMP-1, CD-34 and factor-8 as prognostic markers for squamous cell carcinoma of the tongue. Oral Oncol., 40, 798-803 (2004).
29. Woo JH, Lim JH, Kim YH, Suh SI, Min DS, Chang JS, Lee YH, Park JW, Kwon TK. Resveratrol inhibits phorbol myristate acetate-induced matrix metalloproteinase-9 expression by inhibiting JNK and PKC delta signal transduction. Oncogene, 23, 1845-1853 (2004).
30. Chen CY, Shyu AB. Selective degradation of early-response-gene mRNAs: functional analyses of sequence features of the AU-rich elements. Mol. Cell. Biol., 14, 8471-8482 (1994).
31. Kakuguchi W, Kitamura T, Kuroshima T, Ishikawa M, Kitagawa Y, Totsuka Y, Shindoh M, Higashino F. HuR knockdown changes the oncogenic potential of oral cancer cells. Mol. Cancer Res., 8, 520-528 (2010).
32. Annabi B, Rojas-Sutterlin S, Laroche M, Lachambre MP, Moumdjian R, Béliveau R. The diet-derived sulforaphane inhibits matrix metalloproteinase-9-activated human brain microvascular endothelial cell migration and tubulogenesis. Mol. Nutr. Food Res., 52, 692-700 (2008).
33. Dixon DA, Tolley ND, King PH, Nabors LB, McIntyre TM, Zimmerman GA, Prescott SM. Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J. Clin. Invest., 108, 1657-1665 (2001).
34. Erkinheimo TL, Lassus H, Sivula A, Sengupta S, Furneaux H, Hla T, Haglund C, Butzow R, Ristimäki A. Cytoplasmic HuR expression correlates with poor outcome and with cyclooxygenase 2 expression in serous ovarian carcinoma. Cancer Res., 63, 7591-7594 (2003).
35. Heinonen M, Bono P, Narko K, Chang SH, Lundin J, Joensuu H, Furneaux H, Hla T, Haglund C, Ristimäki A. Cytoplasmic HuR expression is a prognostic factor in invasive ductal breast carcinoma. Cancer Res., 65, 2157-2161 (2005).
36. López de Silanes I, Lal A, Gorospe M. HuR: post-transcriptional paths to malignancy. RNA Biol., 2, 11-13 (2005).
37. Sbai O, Ferhat L, Bernard A, Gueye Y, Ould-Yahoui A, Thiolloy S, Charrat E, Charton G, Tremblay E, Risso JJ, Chauvin JP, Arsanto JP, Rivera S, Khrestchatisky M. Vesicular trafficking and secretion of matrix metalloproteinases-2, -9 and tissue inhibitor of metalloproteinases-1 in neuronal cells. Mol. Cell. Neurosci., 39, 549-568 (2008).
38. Schnaeker EM, Ossig R, Ludwig T, Dreier R, Oberleithner H, Wilhelmi M, Schneider SW. Microtubule-dependent matrix metalloproteinase-2/matrix metalloproteinase-9 exocytosis: prerequisite in human melanoma cell invasion. Cancer Res., 64, 8924-8931 (2004).
39. Rahat MA, Marom B, Bitterman H, Weiss-Cerem L, Kinarty A, Lahat N. Hypoxia reduces the output of matrix metalloproteinase-9 (MMP-9) in monocytes by inhibiting its secretion and elevating membranal association. J. Leukoc. Biol., 79, 706-718 (2006).
40. Fukuda M. Regulation of secretory vesicle traffic by Rab small GTPases. Cell. Mol. Life Sci., 65, 2801-2813 (2008).
41. Corbeel L, Freson K. Rab proteins and Rab-associated proteins: major actors in the mechanism of protein-trafficking disorders. Eur. J. Pediatr., 167, 723-729 (2008).
42. Bravo-Cordero JJ, Marrero-Diaz R, Megías D, Genís L, García-Grande A, García MA, Arroyo AG, Montoya MC. MT1-MMP proinvasive activity is regulated by a novel Rab8-dependent exocytic pathway. EMBO J., 26, 1499-1510 (2007).
43. Catz SD. Characterization of Rab27a and JFC1 as constituents of the secretory machinery of prostate-specific antigen in prostate carcinoma cells. Methods Enzymol., 438, 25-40 (2008).
44. Yoon SO, Shin S, Mercurio AM. Hypoxia stimulates carcinoma invasion by stabilizing microtubules and promoting the Rab11 trafficking of the alpha6beta4 integrin. Cancer Res., 65, 2761-2769 (2005).
45. Hou Q, Wu YH, Grabsch H, Zhu Y, Leong SH, Ganesan K, Cross D, Tan LK, Tao J, Gopalakrishnan V, Tang BL, Kon OL, Tan P. Integrative genomics identifies RAB23 as an invasion mediator gene in diffuse-type gastric cancer. Cancer Res., 68, 4623-4630 (2008).
46. Wang JS, Wang FB, Zhang QG, Shen ZZ, Shao ZM. Enhanced expression of Rab27A gene by breast cancer cells promoting invasiveness and the metastasis potential by secretion of insulin-like growth factor-II. Mol. Cancer Res., 6, 372-382 (2008).
47. Mishima K, Yamada E, Masui K, Shimokawara T, Takayama K, Sugimura M, Ichijima K. Overexpression of the ERK/MAP kinases in oral squamous cell carcinoma. Mod. Pathol., 11, 886-891 (1998).
48. Mukhopadhyay S, Munshi HG, Kambhampati S, Sassano A, Platanias LC, Stack MS. Calcium-induced matrix metalloproteinase 9 gene expression is differentially regulated by ERK1/2 and p38 MAPK in oral keratinocytes and oral squamous cell carcinoma. J. Biol. Chem., 279, 33139-33146 (2004).
49. Hara S, Nakashiro K, Goda H, Hamakawa H. Role of Akt isoforms in HGF-induced invasive growth of human salivary gland cancer cells. Biochem. Biophys. Res. Commun., 370, 123-128 (2008).