Antimetastatic effect of nobiletin through the down-regulation of CXC chemokine receptor type 4 and matrix metallopeptidase-9

Pharmaceutical Biology

Volumn 50, Issue 10, 2012, Pages 1210-1218

  Ahn, Kwang Seok ^a   Baek, Seung Ho ^a   Kim, Sung Moo ^a   Nam, Dongwoo ^a   Lee, Jun Hee ^a   Ahn, Kyoo Seok ^a   Choi, Seung Hoon ^a   Kim, Sung Hoon ^a   Shim, Bum Sang ^a   Chang, Il Moo ^a  

^a Kyung Hee University   (South Korea)

Author keywords

Breast cancer; CXCR4; Metastasis; MMP 9; Nobiletin

Indexed keywords

BIOFLAVONOID; CHEMOKINE RECEPTOR CXCR4; CHLOROQUINE; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; NATURAL PRODUCT; NOBILETIN;

ARTICLE; BREAST CANCER; CANCER CELL; CANCER INVASION; CELL INVASION; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; DRUG SCREENING; DRUG STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IC 50; METASTASIS INHIBITION; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ZYMOGRAPHY;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; DOWN-REGULATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FLAVONES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INHIBITORY CONCENTRATION 50; MATRIX METALLOPROTEINASE 9; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASM METASTASIS; NF-KAPPA B; RECEPTORS, CXCR4; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

CITRUS;

EID: 84866072453     PISSN: 13880209     EISSN: 17445116     Source Type: Journal    
DOI: 10.3109/13880209.2012.664151     Document Type: Article

References (61)

1. Ahn KS, Sethi G, Krishnan K, Aggarwal BB. (2007). Gammatocotrienol inhibits nuclear factor-?B signaling pathway through inhibition of receptor-interacting protein and TAK1 leading to suppression of antiapoptotic gene products and potentiation of apoptosis. J Biol Chem, 282, 809-820. (Pubitemid 47076658)
2. Balkwill F. (2004). Cancer and the chemokine network. Nat Rev Cancer, 4, 540-550. (Pubitemid 38868623)
3. Bhandari D, Trejo J, Benovic JL, Marchese A. (2007). Arrestin-2 interacts with the ubiquitin-protein isopeptide ligase atrophininteracting protein 4 and mediates endosomal sorting of the chemokine receptor CXCR4. J Biol Chem, 282, 36971-36979.
4. Biswas DK, Iglehart JD. (2006). Linkage between EGFR family receptors and nuclear factor ?B (NF-?B) signaling in breast cancer. J Cell Physiol, 209, 645-652. (Pubitemid 44665682)
5. Bogenrieder T, Herlyn M. (2003). Axis of evil: Molecular mechanisms of cancer metastasis. Oncogene, 22, 6524-6536. (Pubitemid 37372332)
6. Brummer O, Athar S, Riethdorf L, Löning T, Herbst H. (1999). Matrixmetalloproteinases 1, 2, and 3 and their tissue inhibitors 1 and 2 in benign and malignant breast lesions: an in situ hybridization study. Virchows Arch, 435, 566-573.
7. Chen KH, Weng MS, Lin JK. (2007). Tangeretin suppresses IL-1?-induced cyclooxygenase (COX)-2 expression through inhibition of p38 MAPK, JNK, and AKT activation in human lung carcinoma cells. Biochem Pharmacol, 73, 215-227.
8. Chen X, Beutler JA, McCloud TG, Loehfelm A, Yang L, Dong HF, Chertov OY, Salcedo R, Oppenheim JJ, Howard OM. (2003). Tannic acid is an inhibitor of CXCL12 (SDF-1)/CXCR4 with antiangiogenic activity. Clin Cancer Res, 9, 3115-3123. (Pubitemid 36993274)
9. Choi SY, Hwang JH, Ko HC, Park JG, Kim SJ. (2007). Nobiletin from citrus fruit peel inhibits the DNA-binding activity of NF-?B and ROS production in LPS-activated RAW 264.7 cells. J Ethnopharmacol, 113, 149-155.
10. Cox G, O'Byrne KJ. (2001). Matrix metalloproteinases and cancer. Anticancer Res, 21, 4207-4219. (Pubitemid 34240952)
11. De Clercq E. (2005). Potential clinical applications of the CXCR4 antagonist bicyclam AMD3100. Mini Rev Med Chem, 5, 805-824. (Pubitemid 41167497)
12. Egeblad M, Werb Z. (2002). New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer, 2, 161-174. (Pubitemid 37328786)
13. Fernandis AZ, Prasad A, Band H, Klösel R, Ganju RK. (2004). Regulation of CXCR4-mediated chemotaxis and chemoinvasion of breast cancer cells. Oncogene, 23, 157-167. (Pubitemid 38142250)
14. Fidler IJ. (1989). Origin and biology of cancer metastasis. Cytometry, 10, 673-680. (Pubitemid 20004725)
15. Gschwind A, Prenzel N, Ullrich A. (2002). Lysophosphatidic acidinduced squamous cell carcinoma cell proliferation and motility involves epidermal growth factor receptor signal transactivation. Cancer Res, 62, 6329-6336. (Pubitemid 35244489)
16. Gupta PB, Mani S, Yang J, Hartwell K, Weinberg RA. (2005). The evolving portrait of cancer metastasis. Cold Spring Harb Symp Quant Biol, 70, 291-297. (Pubitemid 44124883)
17. Helbig G, Christopherson KW 2nd, Bhat-Nakshatri P, Kumar S, Kishimoto H, Miller KD, Broxmeyer HE, Nakshatri H. (2003). NF-κB promotes breast cancer cell migration and metastasis by inducing the expression of the chemokine receptor CXCR4. J Biol Chem, 278, 21631-21638. (Pubitemid 36792563)
18. Hernandez PA, Gorlin RJ, Lukens JN, Taniuchi S, Bohinjec J, Francois F, Klotman ME, Diaz GA. (2003). Mutations in the chemokine receptor gene CXCR4 are associated with WHIM syndrome, a combined immunodeficiency disease. Nat Genet, 34, 70-74. (Pubitemid 36548793)
19. Hirata Y, Masuda Y, Kakutani H, Higuchi T, Takada K, Ito A, Nakagawa Y, Ishii H. (2008). Sp1 is an essential transcription factor for LPSinduced tissue factor expression in THP-1 monocytic cells, and nobiletin represses the expression through inhibition of NF-B, AP-1, and Sp1 activation. Biochem Pharmacol, 75, 1504-1514.
20. Huang CY, Lee CY, Chen MY, Yang WH, Chen YH, Chang CH, Hsu HC, Fong YC, Tang CH. (2009). Stromal cell-derived factor-1/CXCR4 enhanced motility of human osteosarcoma cells involves MEK1/2, ERK and NF-B-dependent pathways. J Cell Physiol, 221, 204-212.
21. Juarez JG, Thien M, Dela Pena A, Baraz R, Bradstock KF, Bendall LJ. (2009). CXCR4 mediates the homing of B cell progenitor acute lymphoblastic leukaemia cells to the bone marrow via activation of p38MAPK. Br J Haematol, 145, 491-499.
22. Ju-Ichi M. (2005). [Chemical study of citrus plants in the search for cancer chemopreventive agents]. Yakugaku Zasshi, 125, 231-254. (Pubitemid 40628393)
23. Kawabata K, Murakami A, Ohigashi H. (2005). Nobiletin, a citrus flavonoid, down-regulates matrix metalloproteinase-7 (matrilysin) expression in HT-29 human colorectal cancer cells. Biosci Biotechnol Biochem, 69, 307-314. (Pubitemid 40413251)
24. Klein G, Vellenga E, Fraaije MW, Kamps WA, de Bont ES. (2004). The possible role of matrix metalloproteinase (MMP)-2 and MMP-9 in cancer, e.g. acute leukemia. Crit Rev Oncol Hematol, 50, 87-100. (Pubitemid 38638736)
25. Knaut H, Werz C, Geisler R, Nüsslein-Volhard C; Tübingen 2000 Screen Consortium. (2003). A zebrafish homologue of the chemokine receptor CXCR4 is a germ-cell guidance receptor. Nature, 421, 279-282. (Pubitemid 36139133)
26. Krueger JS, Keshamouni VG, Atanaskova N, Reddy KB. (2001). Temporal and quantitative regulation of mitogen-activated protein kinase (MAPK) modulates cell motility and invasion. Oncogene, 20, 4209-4218. (Pubitemid 32762195)
27. Kruizinga RC, Bestebroer J, Berghuis P, de Haas CJ, Links TP, de Vries EG, Walenkamp AM. (2009). Role of chemokines and their receptors in cancer. Curr Pharm Des, 15, 3396-3416.
28. Lai CS, Li S, Chai CY, Lo CY, Dushenkov S, Ho CT, Pan MH, Wang YJ. (2008). Anti-inflammatory and antitumor promotional effects of a novel urinary metabolite, 3',4'-didemethylnobiletin, derived from nobiletin. Carcinogenesis, 29, 2415-2424.
29. Lee SO, Jeong YJ, Kim M, Kim CH, Lee IS. (2008). Suppression of PMAinduced tumor cell invasion by capillarisin via the inhibition of NF-B-dependent MMP-9 expression. Biochem Biophys Res Commun, 366, 1019-1024.
30. Lee YC, Cheng TH, Lee JS, Chen JH, Liao YC, Fong Y, Wu CH, Shih YW. (2011). Nobiletin, a citrus flavonoid, suppresses invasion and migration involving FAK/PI3K/Akt and small GTPase signals in human gastric adenocarcinoma AGS cells. Mol Cell Biochem, 347, 103-115.
31. Leivonen SK, Kähäri VM. (2007). Transforming growth factor-α signaling in cancer invasion and metastasis. Int J Cancer, 121, 2119-2124.
32. Li S, Sang S, Pan MH, Lai CS, Lo CY, Yang CS, Ho CT. (2007). Antiinflammatory property of the urinary metabolites of nobiletin in mouse. Bioorg Med Chem Lett, 17, 5177-5181. (Pubitemid 47259653)
33. Liotta LA, Steeg PS, Stetler-Stevenson WG. (1991). Cancer metastasis and angiogenesis: An imbalance of positive and negative regulation. Cell, 64, 327-336. (Pubitemid 121001258)
34. Marchese A, Benovic JL. (2001). Agonist-promoted ubiquitination of the G protein-coupled receptor CXCR4 mediates lysosomal sorting. J Biol Chem, 276, 45509-45512.
35. Miyamoto S, Yasui Y, Tanaka T, Ohigashi H, Murakami A. (2008). Suppressive effects of nobiletin on hyperleptinemia and colitisrelated colon carcinogenesis in male ICR mice. Carcinogenesis, 29, 1057-1063. (Pubitemid 351982252)
36. Müller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, Barrera JL, Mohar A, Verástegui E, Zlotnik A. (2001). Involvement of chemokine receptors in breast cancer metastasis. Nature, 410, 50-56. (Pubitemid 32225831)
37. Murakami A, Matsumoto K, Koshimizu K, Ohigashi H. (2003). Effects of selected food factors with chemopreventive properties on combined lipopolysaccharide-and interferon-gamma-induced I?B degradation in RAW264.7 macrophages. Cancer Lett, 195, 17-25. (Pubitemid 36588974)
38. Murakami A, Nakamura Y, Torikai K, Tanaka T, Koshiba T, Koshimizu K, Kuwahara S, Takahashi Y, Ogawa K, Yano M, Tokuda H, Nishino H, Mimaki Y, Sashida Y, Kitanaka S, Ohigashi H. (2000). Inhibitory effect of citrus nobiletin on phorbol ester-induced skin inflammation, oxidative stress, and tumor promotion in mice. Cancer Res, 60, 5059-5066.
39. Murphy PM. (2001). Chemokines and the molecular basis of cancer metastasis. N Engl J Med, 345, 833-835.
40. Nagasawa T, Hirota S, Tachibana K, Takakura N, Nishikawa S, Kitamura Y, Yoshida N, Kikutani H, Kishimoto T. (1996). Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature, 382, 635-638. (Pubitemid 26268957)
41. Nagase H, Woessner JF Jr. (1999). Matrix metalloproteinases. J Biol Chem, 274, 21491-21494.
42. Nguyen DX, Massagué J. (2007). Genetic determinants of cancer metastasis. Nat Rev Genet, 8, 341-352. (Pubitemid 46625811)
43. Onozuka H, Nakajima A, Matsuzaki K, Shin RW, Ogino K, Saigusa D, Tetsu N, Yokosuka A, Sashida Y, Mimaki Y, Yamakuni T, Ohizumi Y. (2008). Nobiletin, a citrus flavonoid, improves memory impairment and Aβ pathology in a transgenic mouse model of Alzheimer's disease. J Pharmacol Exp Ther, 326, 739-744.
44. Porcile C, Bajetto A, Barbero S, Pirani P, Schettini G. (2004). CXCR4 activation induces epidermal growth factor receptor transactivation in an ovarian cancer cell line. Ann N Y Acad Sci, 1030, 162-169. (Pubitemid 40378910)
45. Proudfoot AE. (2002). Chemokine receptors: Multifaceted therapeutic targets. Nat Rev Immunol, 2, 106-115. (Pubitemid 37323234)
46. Raman D, Baugher PJ, Thu YM, Richmond A. (2007). Role of chemokines in tumor growth. Cancer Lett, 256, 137-165. (Pubitemid 47418345)
47. Sasaki K, Tateoka N, Ando H, Yoshizaki F. (2005). Effect of flavones on rat brain and lung matrix metalloproteinase activity measured by film in-situ zymography. J Pharm Pharmacol, 57, 459-465. (Pubitemid 40515867)
48. Sato T, Takahashi A, Kojima M, Akimoto N, Yano M, Ito A. (2007). A citrus polymethoxy flavonoid, nobiletin inhibits sebum production and sebocyte proliferation, and augments sebum excretion in hamsters. J Invest Dermatol, 127, 2740-2748. (Pubitemid 350134822)
49. Scarlatti G, Tresoldi E, Björndal A, Fredriksson R, Colognesi C, Deng HK, Malnati MS, Plebani A, Siccardi AG, Littman DR, Fenyö EM, Lusso P. (1997). In vivo evolution of HIV-1 co-receptor usage and sensitivity to chemokine-mediated suppression. Nat Med, 3, 1259-1265. (Pubitemid 27508828)
50. Sharony R, Pintucci G, Saunders PC, Grossi EA, Baumann FG, Galloway AC, Mignatti P. (2006). Matrix metalloproteinase expression in vein grafts: role of inflammatory mediators and extracellular signal-regulated kinases-1 and-2. Am J Physiol Heart Circ Physiol, 290, H1651-H1659.
51. Simon C, Goepfert H, Boyd D. (1998). Inhibition of the p38 mitogenactivated protein kinase by SB 203580 blocks PMA-induced Mr 92,000 type IV collagenase secretion and in vitro invasion. Cancer Res, 58, 1135-1139. (Pubitemid 28183199)
52. Sivaraman VS, Wang H, Nuovo GJ, Malbon CC. (1997). Hyperexpression of mitogen-activated protein kinase in human breast cancer. J Clin Invest, 99, 1478-1483. (Pubitemid 27163797)
53. Steeg PS. (2003). Metastasis suppressors alter the signal transduction of cancer cells. Nat Rev Cancer, 3, 55-63. (Pubitemid 37328887)
54. Taichman RS, Cooper C, Keller ET, Pienta KJ, Taichman NS, McCauley LK. (2002). Use of the stromal cell-derived factor-1/CXCR4 pathway in prostate cancer metastasis to bone. Cancer Res, 62, 1832-1837. (Pubitemid 34408510)
55. Uchida D, Begum NM, Almofti A, Nakashiro K, Kawamata H, Tateishi Y, Hamakawa H, Yoshida H, Sato M. (2003). Possible role of stromal-cell-derived factor-1/CXCR4 signaling on lymph node metastasis of oral squamous cell carcinoma. Exp Cell Res, 290, 289-302. (Pubitemid 37272173)
56. Van Laere SJ, Van der Auwera I, Van den Eynden GG, van Dam P, Van Marck EA, Vermeulen PB, Dirix LY. (2007). NF-B activation in inflammatory breast cancer is associated with oestrogen receptor down-regulation, secondary to EGFR and/or ErbB2 overexpression and MAPK hyperactivation. Br J Cancer, 97, 659-669. (Pubitemid 47339884)
57. Vihinen P, Kähäri VM. (2002). Matrix metalloproteinases in cancer: Prognostic markers and therapeutic targets. Int J Cancer, 99, 157-166. (Pubitemid 34309470)
58. Westermarck J, Kähäri VM. (1999). Regulation of matrix metalloproteinase expression in tumor invasion. FASEB J, 13, 781-792. (Pubitemid 29220691)
59. Whitman SC, Kurowska EM, Manthey JA, Daugherty A. (2005). Nobiletin, a citrus flavonoid isolated from tangerines, selectively inhibits class A scavenger receptor-mediated metabolism of acetylated LDL by mouse macrophages. Atherosclerosis, 178, 25-32. (Pubitemid 39600812)
60. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. (2004). Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell, 117, 927-939. (Pubitemid 38798858)
61. Zlotnik A. (2006). Chemokines and cancer. Int J Cancer, 119, 2026-2029. (Pubitemid 44423657)