Activated K-RAS increases polyamine uptake in human colon cancer cells through modulation of caveolar endocytosis

Molecular Carcinogenesis

Volumn 47, Issue 7, 2008, Pages 538-553

  Basu Roy, Upal K ^a   Rial, Nathaniel S ^a   Kachel, Karen L ^a   Gerner, Eugene W ^a,b  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Caveolin 1; Colon cancer; Endocytosis; K RAS; Polyamine uptake

Indexed keywords

CAVEOLIN 1; DYNAMIN; GUANOSINE TRIPHOSPHATASE; POLYAMINE; TYROSINE; CALCIUM BINDING PROTEIN; EPS15 PROTEIN, HUMAN; PHOSPHOPROTEIN; SIGNAL PEPTIDE;

ARTICLE; CANCER CELL CULTURE; CAVEOLA; CELL MEMBRANE; COLON CANCER; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVITY; GENE ACTIVATION; HUMAN; HUMAN CELL; LIPID RAFT; ONCOGENE K RAS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; CELL CULTURE; COLON TUMOR; DRUG ANTAGONISM; METABOLISM; ONCOGENE RAS; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL; WESTERN BLOTTING;

MAMMALIA;

BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CALCIUM-BINDING PROTEINS; CAVEOLAE; CAVEOLIN 1; CELL MEMBRANE; COLONIC NEOPLASMS; DYNAMINS; ENDOCYTOSIS; GENES, RAS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE MICRODOMAINS; PHOSPHOPROTEINS; PHOSPHORYLATION; POLYAMINES; TUMOR CELLS, CULTURED; TYROSINE;

EID: 45949103740     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20414     Document Type: Article

References (60)

1. Wallace HM, Fraser AV, Hughes A. A perspective of polyamine metabolism. Biochem J 2003;376:1-14.
2. Basuroy UK, Gerner EW. Emerging concepts in targeting the polyamine metabolic pathway in epithelial cancer chemoprevention and chemotherapy. J Biochem (Tokyo) 2006;139:27-33.
3. Gerner EW, Meyskens FL, Jr. Polyamines and cancer: Old molecules, new understanding. Nat Rev Cancer 2004;4:781-792.
4. Xie X, Tome ME, Gerner EW. Loss of intracellular putrescine pool-size regulation induces apoptosis. Exp Cell Res 1997;230:386-392.
5. Igarashi K, Kashiwagi K. Polyamine transport in bacteria and yeast. Biochem J 1999;344:633-642.
6. Hasne MP, Ullman B. Identification and characterization of a polyamine permease from the protozoan parasite Leishmania major. J Biol Chem 2005;280:15188-15194.
7. Belting M, Persson S, Fransson LA. Proteoglycan involvement in polyamine uptake. Biochem J 1999;338:317-323.
8. Soulet D, Covassin L, Kaouass M, Charest-Gaudreault R, Audette M, Poulin R. Role of endocytosis in the internalization of spermidine-C(2)-BODIPY, a highly fluorescent probe of polyamine transport. Biochem J 2002;367:347-357.
9. Cullis PM, Green RE, Merson-Davies L, Travis N. Probing the mechanism of transport and compartmentalisation of polyamines in mammalian cells. Chem Biol 1999;6:717-729.
10. Ding K, Sandgren S, Mani K, Belting M, Fransson LA. Modulations of glypican-1 heparan sulfate structure by inhibition of endogenous polyamine synthesis. Mapping of spermine-binding sites and heparanase, heparin lyase, and nitric oxide/nitrite cleavage sites. J Biol Chem 2001;276:46779-46791.
11. Cheng F, Mani K, van den Born J, Ding K, Belting M, Fransson LA. Nitric oxide-dependent processing of heparan sulfate in recycling S-nitrosylated glypican-1 takes place in caveolin-1-containing endosomes. J Biol Chem 2002;277:44431-44439.
12. Soulet D, Gagnon B, Rivest S, Audette M, Poulin R. A fluorescent probe of polyamine transport accumulates into intracellular acidic vesicles via a two-step mechanism. J Biol Chem 2004;279:49355-49366.
13. Mukherjee S, Ghosh RN, Maxfield FR. Endocytosis. Physiol Rev 1997;77:759-803.
14. Nabi IR, Le PU. Caveolae/raft-dependent endocytosis. J Cell Biol 2003;161:673-677.
15. Brown DA, London E. Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 1998;14:111-136.
16. Parton RG. Caveolae and caveolins. Curr Opin Cell Biol 1996;8:542-548.
17. Fra AM, Williamson E, Simons K, Parton RG. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc Natl Acad Sci USA 1995;92:8655-8659.
18. Milovic V, Turchanowa L. Polyamines and colon cancer. Biochem Soc Trans 2003;31:381-383.
19. Thomas T, Thomas TJ. Polyamines in cell growth and cell death: Molecular mechanisms and therapeutic applications. Cell Mol Life Sci 2001;58:244-258.
20. Nilsson JA, Keller UB, Baudino TA, et al. Targeting ornithine decarboxylase in Myc-induced lymphomagenesis prevents tumor formation. Cancer Cell 2005;7:433-444.
21. Hessels J, Kingma AW, Ferwerda H, Keij J, van den Berg GA, Muskiet FA. Microbial flora in the gastrointestinal tract abolishes cytostatic effects of alpha-difluoromethylornithine in vivo. Int J Cancer 1989;43:1155-1164.
22. Quemener V, Moulinoux JP, Havouis R, Seiler N. Polyamine deprivation enhances antitumoral efficacy of chemotherapy. Anticancer Res 1992;12:1447-1453.
23. Bachrach U, Seiler N. Formation of acetylpolyamines and putrescine from spermidine by normal and transformed chick embryo fibroblasts. Cancer Res 1981;41:1205-1208.
24. Cavallo-Medved D, Mai J, Dosescu J, Sameni M, Sloane BF. Caveolin-1 mediates the expression and localization of cathepsin B, pro-urokinase plasminogen activator and their cell-surface receptors in human colorectal carcinoma cells. J Cell Sci 2005;118:1493-1503.
25. Bender FC, Reymond MA, Bron C, Quest AF. Caveolin-1 levels are down-regulated in human colon tumors, and ectopic expression of caveolin-1 in colon carcinoma cell lines reduces cell tumorigenicity. Cancer Res 2000;60:5870-5878.
26. Shirasawa S, Furuse M, Yokoyama N, Sasazuki T. Altered growth of human colon cancer cell lines disrupted at activated Ki-ras. Science 1993;260:85-88.
27. Cao H, Garcia F, McNiven MA. Differential distribution of dynamin isoforms in mammalian cells. Mol Biol Cell 1998;9:2595-2609.
28. Benmerah A, Bayrou M, Cerf-Bensussan N, Dautry-Varsat A. Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J Cell Sci 1999;112:1303-1311.
29. Seiler N, Knodgen B. High-performance liquid chromatographic procedure for the simultaneous determination of the natural polyamines and their monoacetyl derivatives. J Chromatogr 1980;221:227-235.
30. Song KS, Li S, Okamoto T, Quilliam LA, Sargiacomo M, Lisanti MP. Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae microdomains. J Biol Chem 1996;271:9690-9697.
31. Damm EM, Pelkmans L, Kartenbeck J, Mezzacasa A, Kurzchalia T, Helenius A. Clathrin- and caveolin-1 -independent endocytosis: Entry of simian virus 40 into cells devoid of caveolae. J Cell Biol 2005;168:477-488.
32. van der Bliek AM, Redelmeier TE, Damke H, Tisdale EJ, Meyerowitz EM, Schmid SL. Mutations in human dynamin block an intermediate stage in coated vesicle formation. J Cell Biol 1993;122:553-563.
33. Marks DL, Singh RD, Choudhury A, Wheatley CL, Pagano RE. Use of fluorescent sphingolipid analogs to study lipid transport along the endocytic pathway. Methods 2005;36:186-195.
34. Lawson KR, Ignatenko NA, Piazza GA, Cui H, Gerner EW. Influence of K-ras activation on the survival responses of Caco-2 cells to the chemopreventive agents sulindac and difluoromethylomithine. Cancer Epidemiol Biomarkers Prev 2000;9:1155-1162.
35. Roy S, Luetterforst R, Harding A, et al. Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nat Cell Biol 1999;1:98-105.
36. Smart EJ, Graf GA, McNiven MA, et al. Caveolins, liquid-ordered domains, and signal transduction. Mol Cell Biol 1999;19:7289-7304.
37. Cavallo-Medved D, Dosescu J, Linebaugh BE, Sameni M, Rudy D, Sloane BF. Mutant K-ras regulates cathepsin B localization on the surface of human colorectal carcinoma cells. Neoplasia 2003;5:507-519.
38. Allgayer H, Wang H, Shirasawa S, Sasazuki T, Boyd D. Targeted disruption of the K-ras oncogene in an invasive colon cancer cell line down-regulates urokinase receptor expression and plasminogen-dependent proteolysis. Br J Cancer 1999;80:1884-1891.
39. Nichols B. Caveosomes and endocytosis of lipid rafts. J Cell Sci 2003;116:4707-4714.
40. Dermine JF, Duclos S, Garin J, et al. Flotillin-1-enriched lipid raft domains accumulate on maturing phagosomes. J Biol Chem 2001;276:18507-18512.
41. Volonte D, Galbiati F, Li S, Nishiyama K, Okamoto T, Lisanti MP. Flotillins/cavatellins are differentially expressed in cells and tissues and form a hetero-oligomeric complex with caveolins in vivo. Characterization and epitope-mapping of a novel flotillin-1 monoclonal antibody probe. J Biol Chem 1999;274:12702-12709.
42. Sharma DK, Brown JC, Choudhury A, et al. Selective stimulation of caveolar endocytosis by glycosphingolipids and cholesterol. Mol Biol Cell 2004;15:3114-3122.
43. Rodal SK, Skretting G, Garred O, Vilhardt F, van Deurs B, Sandvig K. Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol Biol Cell 1999;10:961-974.
44. Le PU, Guay G, Altschuler Y, Nabi IR. Caveolin-1 is a negative regulator of caveolae-mediated endocytosis to the endoplasmic reticulum. J Biol Chem 2002;277:3371-3379.
45. Minshall RD, Tiruppathi C, Vogel SM, et al. Endothelial cell-surface gp60 activates vesicle formation and trafficking via G(i)-coupled Src kinase signaling pathway. J Cell Biol 2000;150:1057-1070.
46. Le PU, Nabi IR. Distinct caveolae-mediated endocytic pathways target the Golgi apparatus and the endoplasmic reticulum. J Cell Sci 2003;116:1059-1071.
47. Aoki T, Nomura R, Fujimoto T. Tyrosine phosphorylation of caveolin-1 in the endothelium. Exp Cell Res 1999;253:629-636.
48. del Pozo MA, Balasubramanian N, Alderson NB, et al. Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat Cell Biol 2005;7:901-908.
49. Kim YN, Dam P, Bertics PJ. Caveolin-1 phosphorylation in human squamous and epidermoid carcinoma cells: Dependence on ErbB1 expression and Src activation. Exp Cell Res 2002;280:134-147.
50. Milovic V, Deubner C, Zeuzem S, Piiper A, Caspary WF, Stein J. EGF stimulates polyamine uptake in Caco-2 cells. Biochem Biophys Res Commun 1995;206:962-968.
51. Pegg AE. Regulation of ornithine decarboxylase. J Biol Chem 2006;281:14529-14532.
52. Chu CL, Buczek-Thomas JA, Nugent MA. Heparan sulphate proteoglycans modulate fibroblast growth factor-2 binding through a lipid raft-mediated mechanism. Biochem J 2004;379:331-341.
53. Bianco C, Strizzi L, Rehman A, et al. A Nodal- and ALK4-independent signaling pathway activated by Cripto-1 through Glypican-1 and c-Src. Cancer Res 2003;63:1192-1197.
54. Roff CF, Fuchs R, Mellman I, Robbins AR. Chinese hamster ovary cell mutants with temperature-sensitive defects in endocytosis. I. Loss of function on shifting to the non-permissive temperature. J Cell Biol 1986;103:2283-2297.
55. Ohashi M, Miwako I, Nakamura K, et al. An arrested late endosome-lysosome intermediate aggregate observed in a Chinese hamster ovary cell mutant isolated by novel three-step screening. J Cell Sci 1999;112:1125-1138.
56. Ohashi M, Miwako I, Yamamoto A, Nagayama K. Arrested maturing multivesicular endosomes observed in a Chinese hamster ovary cell mutant, LEX2, isolated by repeated flow-cytometric cell sorting. J Cell Sci 2000;113:2187-2205.
57. Milovic V. Polyamines in the gut lumen: Bioavailability and biodistribution. Eur J Gastroenterol Hepatol 2001;13:1021-1025.
58. Ivanov AI, Nusrat A, Parkos CA. Endocytosis of epithelial apical junctional proteins by a clathrin-mediated pathway into a unique storage compartment. Mol Biol Cell 2004;15:176-188.
59. Vogel U, Sandvig K, van Deurs B. Expression of caveolin-1 and polarized formation of invaginated caveolae in Caco-2 and MDCK II cells. J Cell Sci 1998;111:825-832.
60. von Ruhland CJ, Campbell L, Gumbleton M, Jasani B, Newman GR. Immunolocalization of caveolin-1 in rat and human mesothelium. J Histochem Cytochem 2004;52:1415-1425.