Heparin induces apoptosis through suppression of AKt in oral squamous cell carcinoma cells

Anticancer Research

Volumn 29, Issue 4, 2009, Pages 1079-1088

  Ueda, Kohei ^a   Inoue, Shuichi ^a,c   Zhang, Y E ^b   Kutsuna, Tomohiko ^a   Inoue, Sayaka ^a   Noto, Kumiko ^a   Arai, Naoya ^a   Noguchi, Makoto ^a  

^a UNIVERSITY OF TOYAMA   (Japan)

^b PEKING UNIVERSITY SCHOOL AND HOSPITAL OF STOMATOLOGY   (China)

^c UNIVERSITY OF TOYAMA   (Japan)

Author keywords

AKt; Apoptosis; Heparin; Oral squamous cell carcinoma

Indexed keywords

FLUORESCEIN ISOTHIOCYANATE; HEPARIN; LIPOCORTIN 5; PROTEIN KINASE B;

APOPTOSIS; ARTICLE; ASSAY; CANCER CELL CULTURE; CELL GROWTH; CELL VIABILITY; DRUG EFFECT; DRUG MECHANISM; ENZYME REPRESSION; HUMAN; HUMAN CELL; MITOCHONDRION; MOUTH CARCINOMA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SQUAMOUS CELL CARCINOMA; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-ASSOCIATED DEATH PROTEIN; BLOTTING, WESTERN; CARCINOMA, SQUAMOUS CELL; CELL PROLIFERATION; CISPLATIN; FIBRINOLYTIC AGENTS; HEPARIN; HUMANS; MOUTH NEOPLASMS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; TUMOR CELLS, CULTURED;

EID: 64949091745     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (45)

1. Kjellen L and Lindahl U: Proteoglycans: structures and interactions. Annu Rev Biochem 60: 443-475, 1991.
2. Capila I and Linhardt RJ: Heparin-protein interactions. Angew Chem Int Ed Engl 41(3): 391-412, 2002.
3. Smorenburg SM and Van Noorden CJ: The complex effects of heparins on cancer progression and metastasis in experimental studies. Pharmacol Rev 53(1): 93-105, 2001.
4. Regelson W: Anionic dyes, heparin, and heparinoids: the rediscovery of polyanionic tumor inhibitors. J Natl Cancer Inst 81(24): 1929-1930, 1989.
5. Au YP, Kenagy RD, Clowes MM and Clowes AW: Mechanisms of inhibition by heparin of vascular smooth muscle cell proliferation and migration. Haemostasis 23: 177-782, 1993.
6. Miralem T, Wang A, Whiteside CI and Templeton DM: Heparin inhibits mitogen-activated protein kinase-dependent and -independent c-fos induction in mesangial cells. J Biol Chem 271: 17100-17106, 1996.
7. Tiozzo R, Cingi MR, Pietrangelo A, Albertazzi L, Calandra S and Milani MR: Effect of heparin-like compounds on the in vitro proliferation and protein synthesis of various cell types. Arzneimittelforschung 39: 15-20, 1989.
8. Pross M, Lippert H, Misselwitz F, Nestler G, Krüger S, Langer H, Halangk W and Schulz HU: Low-molecular-weight heparin (reviparin) diminishes tumor cell adhesion and invasion in vitro, and decreases intraperitoneal growth of colon adenocarcinoma cells in rats after laparoscopy. Thromb Res 110: 215-220, 2003.
9. Erduran E, Tekelioǧlu Y, Gedik Y and Yildiran A: Apoptotic effects of heparin on lymphoblasts, neutrophils, and mononuclear cells: results of a preliminary in vitro study. Am J Hematol 61(2): 90-93, 1999.
10. Li HL, Ye KH, Zhang HW, Luo YR, Ren XD, Xiong AH and Situ R: Effect of heparin on apoptosis in human nasopharyngeal carcinoma CNE2 cells. Cell Res 11(4): 311-315, 2001.
11. Castellot JJ Jr, Pukac LA, Caleb BL, Wright TC Jr and Karnovsky MJ: Heparin selectively inhibits a protein kinase C-dependent mechanism of cell cycle progression in calf aortic smooth muscle cells. J Cell Biol 109: 3147-3155, 1989.
12. Pukac LA, Ottlinger ME and Karnovsky MJ: Heparin suppresses specific second messenger pathways for protooncogene expression in rat vascular smooth muscle cells. J Biol Chem 267: 3707-3711, 1992.
13. Ottlinger ME, Pukac LA and Karnovsky MJ: Heparin inhibits mitogenactivated protein kinase activation in intact rat vascular smooth muscle cells. J Biol Chem 268(26):19173-19176, 1993.
14. Hathaway GM, Lubben TH and Traugh JA: Inhibition of casein kinase II by heparin. J Biol Chem 255: 8038-8041, 1980.
15. Tuazon PT and Traugh JA: CK1 and 11-multipotential serine protein kinases: structure, function, and regulation. Adv Second Messenger Phosphoprotein Res 23: 124-164, 1991.
16. Maira G Di, Salvi M, Arrigoni G, Marin O, Sarno S, Brustolon F, Pinna LA and Ruzzene M: Protein kinase CK2 subunits are positive regulators of AKT kinase. Cell Death and Differentiation 12: 668-677, 2005.
17. Duncan JS and Litchfield DW: Too much of a good thing: the role of protein kinase CK2 in tumorigenesis and prospects for therapeutic inhibition of CK2. Biochim Biophys Acta 1784(1): 33-47, 2008.
18. Kandel ES and Hay N: The regulation and activities of the multifunctional serine/threonine kinase Akt/PKB. Exp Cell Res 253: 210-229, 1999.
19. Franke TF, Hornik CP, Segev L, Shostak GA and Sugimoto C: PI3K/Akt and apoptosis: size matters. Oncogene 22: 8983-8998, 2003.
20. Song G, Ouyang G and Bao S: The activation of Akt/PKB signaling pathway and cell survival. J Cell Mol Med 9(1): 59-71, 2005.
21. Jemal A, Murray T, Samuels A, Ghafoor A, Ward E and Thun MJ: Cancer Stat 53(1): 5-26, 2003.
22. Parker SL, Tong T and Wingo PA: Cancer statistics, 1996. CA Cancer J Clin 65: 5-27, 1996.
23. Vokes EE, Weichselbaum RR, Lipman SM and Hong WK: Head and neck cancer. N Engl J Med 328: 184-194, 1993.
24. Mosmann T: Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55-63, 1983.
25. Simon JA: Using isoform-specific inhibitors to target lipid kinases. Cell 125(4): 41-649, 2006.
26. Berry D, Lynn DM, Sasisekharan R and Langer R: Poly(|3-amino ester) s promote cellular uptake of heparin and cancer cell death. Chem Biol 11(4): 487-498, 2004.
27. Mandal M, Younes M, Swan EA, Jasser SA, Doan D, Yigitbasi O, McMurphey A, Ludwick J, El-Naggar AK, Bucana C, Mills GB and Myers JN: The Akt inhibitor KP372-1 inhibits proliferation and induces apoptosis and anoikis in squamous cell carcinoma of the head and neck. Oral Oncol 42(4): 430-439, 2006.
28. Amornphimoltham P, Sriuranpong V, Patel V, Benavides F, Conti CJ, Sauk J, Sausville EA, Molinolo AA and Gutkind JS: Persistent activation of the Akt pathway in head and neck squamous cell carcinoma: a potential target for UCN-01. Clinical Cancer Research 10: 4029-4037, 2004.
29. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y and Greenberg ME: Akt phosphorylation of BAD couples survival signals to the cell-Intrinsic death machinery. Cell 91: 231-241, 1997.
30. Downward J: PI 3-kinase, Akt and cell survival. Semin Cell Dev Biol 15(2): 177-182, 2004.
31. Datta SR, Brunet A and Greenberg ME: Cellular survival: a play in three Akts. Genes Dev 13: 2905-2927, 1999.
32. Hayakawa J, Ohmichi M, Kurachi H, Kanda Y, Hisamoto K, Nishio Y, Adachi K, Tasaka K, Kanzaki T and Murata Y: Inhibition of BAD phosphorylation either at serine 112 via extracellular signal-regulated protein kinase cascade or at serine 136 via Akt cascade sensitizes human ovarian cancer cells to cisplatin. Cancer Res 60: 5988-5994, 2000.
33. Zha J, Harada H, Yang F, Jockel J and Korsmeyer SJ: Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not Bcl-XL. Cell 87: 619-628, 1996.
34. Kim R, Tanabe K, Uchida Y, Emi M, Inoue H and Toge T: Current status of the molecular mechanisms of anticancer drug-induced apoptosis. Cancer chemotherapy and pharmacology 50(5): 343-352, 2002.
35. Weir NM, Selvendiran K, Kutala VK, Tong L, Vishwanath S, Rajaram M, Tridandapani S, Anant S and Kuppusamy P: Curcumin induces G2/M arrest and apoptosis in cisplatin-resistant human ovarian cancer cells by modulating Akt and p38 MAPK. Cancer Biol Ther 6(2): 178-184, 2007.
36. Uddin S, Hussain A, Al-Hussein K, Platanias LC and Bhatia KG: Inhibition of phosphatidylinositol 30-kinase induces preferentially killing of PTEN-null T leukemias through AKT pathway. Biochemical and Biophysical Research Communications 320: 932-938, 2004.
37. Lee S, Choi EJ, Jin C and Kim DH: Activation of PI3K/Akt pathway by PTEN reduction and PIK3CA mRNA amplification contributes to cisplatin resistance in an ovarian cancer cell line. Gynecol Oncol 97: 26-34, 2005.
38. Mathieu I, Sexton E, Leblanc K and Asselin E: AKT involvement in cisplatin chemoresistance of human uterine cancer cells. Gynecol Oncol 94(3): 785-795, 2004.
39. Han Z, Hong L, Wu K, Han S, Shen H, Liu C, Han Y, Liu Z, Han Y and Fan D: Reversal of multidrug resistance of gastric cancer cells by downregulation of Akt1 with Akt1 siRNA. J Exp Clin Cancer Res 25(4): 601-606, 2006.
40. Ohkoshi M, Akagawa T and Nakajima M: Effects of serine protease inhibitor FOY-305 and heparin on the growth of squamous cell carcinoma. Anticancer Res 13: 963-966, 1993.
41. Hasan J, Shnyder SD, Clamp AR, McGown AT, Bicknell R, Presta M, Bibby M, Double J, Craig S, Leeming D, Stevenson K, Gallagher JT and Jayson GC: Heparin octasaccharides inhibit angiogenesis in vivo. Clin Cancer Res 11: 8172-8179, 2005.
42. Yang E, Zha J, Jockel J, Boise LH, Thompson CB and Korsmeyer SJ: Bad, a heterodimeric partner for Bc1-x1 and Bc1-2, displaces Bax and promotes cell death. Cell 80: 285-291, 1995.
43. Chandra D, Liu JW and Tang DG: Early mitochondrial activation and cytochrome c up-regulation during apoptosis. J Biol Chem 277(52): 50842-50854, 2002.
44. Rooney M, Kish J, Jacobs J, Kinzie J, Weaver A, Crissman J and AL-Sarraf M: Improved complete response rate and survival in advanced head and neck cancer after three-course induction therapy with 120-hour 5-FU infusion and cisplatin. Cancer 55(5): 1123-1128, 1985.
45. Psyrri A, Kwong M, DiStasio S, Lekakis L, Kassar M, Sasaki C, Wilson LD, Haffty BG, Son YH, Ross DA, Weinberger PM, Chung GG, Zelterman D, Burtness BA and Cooper DL: Cisplatin, fluorouracil, and leucovorin induction chemotherapy followed by concurrent cisplatin chemoradiotherapy for organ preservation and cure in patients with advanced head and neck cancer: long-term follow-up. J Clin Oncol 22(15): 3061-9, 2004.