P-glycoprotein binds to ezrin at amino acid residues 149-242 in the FERM domain and plays a key role in the multidrug resistance of human osteosarcoma

International Journal of Cancer

Volumn 130, Issue 12, 2012, Pages 2824-2834

  Brambilla, Daria ^a   Zamboni, Silvia ^a   Federici, Cristina ^a   Lugini, Luana ^a   Lozupone, Francesco ^a   Milito, Angelo De ^a   Cecchetti, Serena ^a   Cianfriglia, Maurizio ^a   Fais, Stefano ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

ezrin; human osteosarcoma; lipid rafts; multidrug resistance; P glycoprotein

Indexed keywords

AMINO ACID; CARBOPLATIN; DOXORUBICIN; EZRIN; GANGLIOSIDE GM1; GLYCOPROTEIN P; MUTANT PROTEIN; RADIXIN; VINBLASTINE SULFATE;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; DRUG CYTOTOXICITY; HUMAN; HUMAN CELL; LIPID RAFT; MULTIDRUG RESISTANCE; OSTEOSARCOMA; OSTEOSARCOMA CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

EID: 84859883906     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.26285     Document Type: Article

References (48)

1. Basaran M, Bavbek ES, Saglam S, Eralp L, Sakar B, Atalar AC, Bilgic B, Ozger H, Onat H,. A phase II study of cisplatin, ifosfamide and epirubicin combination chemotherapy in adults with non metastatic and extremity osteosarcomas. Oncology 2007; 72: 255-60. (Pubitemid 351161619)
2. Bacci G, Forni C, Longhi A,., Ferrari S, Mercuri M, Bertoni F, Serra M, Briccoli A, Balladelli A, Picci P,. Local recurrence and local control of non-metastatic osteosarcoma of the extremities: a 27-year experience in a single institution. J Surg Oncol 2007; 96: 118-23. (Pubitemid 47264814)
3. Le Deley MC, Guinebretière JM, Gentet JC, Pacquement H, Pichon F, Marec-Bérard P, Entz-Werlé N, Schmitt C, Brugières L, Vanel D, Dupoüy N, Tabone MD, et al. and Société Française d'Oncologie Pédiatrique (SFOP). SFOP OS94: a randomised trial comparing preoperative high-dose methotrexate plus doxorubicin to high-dose methotrexate plus etoposide and ifosfamide in osteosarcoma patients. Eur J Cancer 2007; 43: 752-61. (Pubitemid 46502910)
4. Chou AJ, Merola PR, Wexler LH, Gorlick RG, Vyas YM, Healey JH, LaQuaglia MP, Huvos AG, Meyers PA,. Treatment of osteosarcoma at first recurrence after contemporary therapy: the Memorial Sloan-Kettering Cancer Center experience. Cancer 2005; 104: 2214-21. (Pubitemid 41579969)
5. Murren JR,. Modulating MDR: can we target this therapy? Clin Cancer Res 2002; 8: 633-5. (Pubitemid 34742089)
6. Borges-Walmsley MI, McKeegan KS, Walmsley AR,. Structure and function of efflux pumps that confer resistance to drugs. Biochem J 2003; 376: 313-38. (Pubitemid 38010517)
7. Shustik C, Dalton W, Gros P,. P-glycoprotein mediated MDR in tumor cells: biochemistry, clinical relevance and modulation. Mol Aspects Med 1995; 16: 1-78.
8. Ng WF, Sarangi F, Zastawny RL, Veinot-Drebot L, Ling V,. Identification of members of the P-glycoprotein multigene family. Mol Cell Biol 1989; 9: 1224-32. (Pubitemid 19071691)
9. Gottesman MM, Pastan I,. Biochemistry of MDR mediated by the multidrug transporter. Annu Rev Biochem 1993; 62: 385-427. (Pubitemid 23237876)
10. Leith CP, Kopecky KJ, Chen IM, Eijdems L, Slovak ML, McConnell TS, Head DR, Weick J, Grever MR, Appelbaum FR, Willman CL,. Frequency and clinical significance of the expression of the MDR proteins MDR1/P-glycoprotein, MRP1, and LRP in acute myeloid leukemia: a Southwest Oncology Group Study. Blood 1999; 94: 1086-99. (Pubitemid 29361842)
11. Baldini N, Scotlandi K, Barbanti-BrÃdano G, Manara MC, Maurici D, Bacci G, Bertoni F, Picci P, Sottili S, Campanacci M, Serra M,. Expression of P-glycoprotein in high-grade osteosarcomas in relation to clinical outcome. N Engl J Med 1995; 333: 1380-5.
12. Chan HS, Grogan TM, Haddad G, DeBoer G, Ling V,. P-glycoprotein expression: critical determinant in the response to osteosarcoma chemotherapy. J Natl Cancer Inst 1997; 89: 1706-15. (Pubitemid 27508195)
13. Scotlandi K, Serra M, Nicoletti G, Vaccari M, Manara MC, Nini G, Landuzzi L, Colacci A, Bacci G, Bertoni F, Picci P, Campanacci M, Baldini N,. MDR and malignancy in human osteosarcoma. Cancer Res 1996; 56: 2434-9.
14. Serra M, Pasello M, Manara MC, Scotlandi K, Ferrari S, Bertoni F, Mercuri M, Alvegard TA, Picci P, Bacci G, Smeland S,. May P-glycoprotein status be used to stratify high-grade osteosarcoma patients? Results from the Italian/Scandinavian Sarcoma Group 1 treatment protocol. Int J Oncol 2006; 29: 1459-68.
15. Pakos EE, Nearchou AD, Grimer RJ, Koumoullis HD, Abudu A, Bramer JA, Jeys LM, Franchi A, Scoccianti G, Campanacci D, Capanna R, Aparicio J, et al. Prognostic factors and outcomes for osteosarcoma: an international collaboration. Eur J Cancer 2009; 45: 2367-75.
16. Luciani F, Molinari A, Lozupone F, Calcabrini A, Lugini L, Stringaro A, Puddu P, Arancia G, Cianfriglia M, Fais S,. P-glycoprotein-actin association through ERM family proteins: a role in P-glycoprotein function in human cells of lymphoid origin. Blood 2002; 99: 641-8. (Pubitemid 34533103)
17. Takeshita H, Kusuzaki K, Ashihara T, Gebhardt MC, Mankin HJ, Hirasawa Y,. Actin organization associated with the expression of multidrug resistant phenotype in osteosarcoma cells and the effect of actin depolymerization on drug resistance. Cancer Lett 1998; 126: 75-81. (Pubitemid 28142974)
18. Fais S, Luciani F, Logozzi M, Parlato S, Lozupone F,. Linkage between cell membrane proteins and actin-based cytoskeleton: the cytoskeletal-driven cellular functions. Histol Histopathol 2000; 15: 539-49. (Pubitemid 30218850)
19. Ramoni C, Luciani F, Spadaro F, Lugini L, Lozupone F, Fais S,. Differential expression and distribution of ezrin, radixin and moesin in human natural killer cells. Eur J Immunol 2002; 32: 3059-65. (Pubitemid 35414863)
20. Fais S, Malorni W,. Leukocyte uropod formation and membrane/cytoskeleton linkage in immune interactions. J Leuk Biol 2003; 73: 556-63. (Pubitemid 38040467)
21. Fais S, De Milito A, Lozupone F,. The role of FAS to ezrin association in FAS-mediated apoptosis. Apoptosis 2005; 10: 941-7. (Pubitemid 41285573)
22. Fenyvesi F, Fenyvesi E, Szente L, Goda K, Bacsó Z, Bácskay I, Váradi J, Kiss T, Molnár E, Janáky T, Szabó G Jr., Vecsernyés M,. P-glycoprotein inhibition by membrane cholesterol modulation. Eur J Pharm Sci 2008; 34: 236-42.
23. Patra SK,. Dissecting lipid raft facilitated cell signalling pathways in cancer. Biochim Biophys Acta 2008; 1785: 182-206.
24. Roepstorff K, Thomsen P, Sandvig K, van Deurs B,. Sequestration of epidermal growth factor receptors in non-caveolar lipid rafts inhibits ligand binding. J Biol Chem 2002; 277: 18954-60. (Pubitemid 34959960)
25. Angata T, Varki A,. Chemical diversity in the sialic acids and relate alpha-keto acids: an evolutionary perspective. Chem Rev 2002; 102: 439-70.
26. Yoshitaka N,. Cell regulatory function of glycosphingolipids: carbohydrate recognition and biosignaling. Pure Appl Chem (Printed in Great Britain) 1998; 70: 49-53.
27. Garrigues A, Escargueil AE, Orlowski S,. The multidrug transporter, P-glycoprotein, actively mediates cholesterol redistribution in the cell membrane. Proc Natl Acad Sci USA 2002; 99: 10347-52.
28. Gupta N, Wollscheid B, Watts JD, Scheer B, Aebersold R, DeFranco AL,. Quantitative proteomic analysis of B cell lipid rafts reveals that ezrin regulates antigen receptor-mediated lipid raft dynamics. Nat Immunol 2006; 7: 625-33. (Pubitemid 43797344)
29. Gajate C,. Cytoskeleton-mediated death receptor and ligand concentration in lipid rafts forms apoptosis-promoting clusters in cancer chemotherapy. Biol Chem 2005; 280: 11641-7. (Pubitemid 40418478)
30. Prag S, Parsons M, Keppler MD, Ameer-Beg SM, Barber P, Hunt J, Beavil AJ, Calvert R, Arpin M, Vojnovic B, Ng T,. Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42. Mol Biol Cell 2007; 18: 2935-48. (Pubitemid 47235301)
31. Federici C, Brambilla D, Lozupone F, Matarrese P, de Milito A, Lugini L, Iessi E, Cecchetti S, Marino M, Perdicchio M, Logozzi M, Spada M, et al. Pleiotropic function of ezrin in human metastatic melanomas. Int J Cancer 2009; 124: 2804-12.
32. Brambilla D, Fais S,. The Janus-faced role of ezrin in linking cells to either normal or metastatic phenotype. Int J Cancer 2009; 125: 2239-45.
33. Lozupone F, Lugini L, Matarrese PLuciani F, Federici C, Iessi E, Margutti P, Stassi G, Malorni W, Fais S,. Identification and relevance of the CD95-binding domain in the N-terminal region of ezrin. J Biol Chem 2004; 279: 9199-207. (Pubitemid 38295983)
34. Lugini L, Matarrese P, Tinari A Lozupone F, Federici C, Iessi E, Gentile M, Luciani F, Parmiani G, Rivoltini L, Malorni W, Fais S,. Cannibalism of live lymphocytes by human metastatic but not primary melanoma cells. Cancer Res 2006; 66: 3629-38.
35. Fogh J, Trempe G,. New human tumor cell lines in Fogh J. editor. New York: Plenum Press, 1975. 115-59.
36. Maraldi NM, Zini N, Sabatelli P, Valmori A, Scotlandi K, Serra M, Baldini N,. Ultrastructural features and P-glycoprotein immunolocalization in Saos-2/DX580 multidrug-resistant human osteosarcoma cells. J Submicrosc Cytol Pathol 1996; 28: 93-100.
37. Cianfriglia M, Willingham MC, Tombesi M, Scagliotti GV, Frasca G, Chersi A,. P-glycoprotein epitope mapping. Identification of a linear human-specific epitope in the fourth loop of the P-glycoprotein extracellular domain by MM4.17 murine monoclonal antibody to human multi-drug-resistant cells. Int J Cancer 1994; 56: 153-60.
38. Liu YW, Sanders MA, Basson MD,. Human Caco-2 intestinal epithelial motility is associated with tyrosine kinase and cytoskeletal focal adhesion kinase signals. J Surg Res 1998; 77: 112-18. (Pubitemid 28413500)
39. Eramo A, Sargiacomo M, Ricci-Vitiani L, Todaro M, Stassi G, Messina CG, Parolini I, Lotti F, Sette G, Peschle C, De Maria R,. CD95 death-inducing signaling complex formation and internalization occur in lipid rafts of type I and type II cells. Eur J Immunol 2004; 34: 1930-40. (Pubitemid 39256074)
40. Epand RM,. Cholesterol and the interaction of proteins with membrane domains. Prog Lipid Res 2006; 45: 279-94. (Pubitemid 43818129)
41. Thiebaut F, Tsuruo T, Hamada H, Gottesman MM, Pastan I, Willingham MC,. Immunohistochemical localization in normal tissues of different epitopes in the multidrug transport protein P170: evidence for localization in brain capillaries and crossreactivity of one antibody with a muscle protein. J Histochem Cytochem 1989; 37: 159-64. (Pubitemid 19039163)
42. Cianfriglia M, Cenciarelli C, Barca S, Tombesi M, Flego M, Dupuis ML,. Monoclonal antibodies as a tool for structure-function studies of the MDR1-P-glycoprotein. Curr Prot Pept Sci 2002; 3: 513-30. (Pubitemid 35157722)
43. Tomas EM, Chau TA, Madrenas J,. Clustering of a lipid-raft associated pool of ERM proteins at the immunological synapse upon T cell receptor or CD28 ligation. Immunol Lett 2002; 83: 143-7. (Pubitemid 34626948)
44. Kumta SM, Zhu QS, Lee KM, Griffith J, Chow LT, Leung PC,. Doxo efflux indicative of tumor resistance assay. Clinical significance of P-glycoprotein immunohistochemistry and doxorubicin binding assay in patients with osteosarcoma. Int Orthop 2001; 25: 279-82. (Pubitemid 33026861)
45. Fehon RG, McClatchey AI, Bretscher A,. Organizing the cell cortex: the role of ERM proteins. Nat Rev Mol Cell Biol 2010; 11: 276-87.
46. Fais S,. Moulding the shape of a metastatic cell. Leuk Res 2010; 34: 843-7.
47. Parlato S, Giammarioli AM, Logozzi M, Lozupone F, Matarrese P, Luciani F, Falchi M, Malorni W, Fais S,. CD95 (APO-1/Fas) linkare to the actin cytoskeleton through ezrin in human T lymphocytes: a novel regulatory mechanism of the CD95 apoptotic pathway. EMBO J 2000; 19: 5123-34.
48. Lee CA, Cook JA, Reyner EL, Smith DA,. P-glycoprotein related drug interactions: clinical importance and a consideration of disease states. Expert Opin Drug Metab Toxicol 2010; 6: 603-19.