The cross-talk between canonical and non-canonical Wnt-dependent pathways regulates P-glycoprotein expression in human blood-brain barrier cells

Journal of Cerebral Blood Flow and Metabolism

Volumn 34, Issue 8, 2014, Pages 1258-1269

  Pinzón Daza, Martha L ^a,b   Salaroglio, Iris C ^a   Kopecka, Joanna ^a   Garzòn, Ruth ^b   Couraud, Pierre Olivier ^c   Ghigo, Dario ^a,d   Riganti, Chiara ^a,d  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSIDAD DEL ROSARIO   (Colombia)

^c INSTITUT COCHIN   (France)

^d UNIVERSITY OF TURIN   (Italy)

Author keywords

catenin; blood brain barrier; glycogen synthase kinase 3; P glycoprotein; RhoA kinase; Wnt;

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; BETA CATENIN; DOXORUBICIN; GLYCOGEN SYNTHASE KINASE 3; MULTIDRUG RESISTANCE PROTEIN; PROTEIN TYROSINE PHOSPHATASE 1B; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TYROSINE; WNT PROTEIN;

ARTICLE; BLOOD BRAIN BARRIER; COCULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEPHOSPHORYLATION; DRUG EFFICACY; DRUG PENETRATION; DRUG TRANSPORT; ENZYME ACTIVATION; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE SILENCING; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; MICROVASCULAR ENDOTHELIAL CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION; UBIQUITINATION; WNT SIGNALING PATHWAY;

AMIDES; BETA CATENIN; BLOOD-BRAIN BARRIER; CELL LINE, TUMOR; CELL SURVIVAL; COCULTURE TECHNIQUES; DOXORUBICIN; ENDOTHELIAL CELLS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; P-GLYCOPROTEIN; PERMEABILITY; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 1; PYRIDINES; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; WNT SIGNALING PATHWAY;

EID: 84905510048     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2014.100     Document Type: Article

References (40)

1. Agarwal S, Sane R, Oberoi R, Ohlfest JR, Elmquist WF. Delivery of molecularly targeted therapy to malignant glioma, a disease of the whole brain. Expert Rev Mol Med 2011; 13: e17.
2. Lim JC, Kania KD, Wijesuriya H, Chawla S, Sethi JK, Pulaski L et al. Activation of b-catenin signalling by GSK-3 inhibition increases p-glycoprotein expression in brain endothelial cells. J Neurochem 2008; 106: 1855-1865.
3. Kania KD, Wijesuriya HC, Hladky SB, Barrand MA. Beta amyloid effects on expression of multidrug efflux transporters in brain endothelial cells. Brain Res 2011; 1418: 1-11.
4. Katoh M, Katoh M. WNT signalling pathway and stem cells signaling network. Clin Cancer Res 2007; 13: 4042-4045.
5. MacDonald BT, Tamai K, He X. Wnt/b-catenin signaling: components, mechanisms, and diseases. Dev Cell 2009; 17: 9-26.
6. Riganti C, Salaroglio IC, Pinzòn-Daza ML, Caldera V, Campia I, Kopecka J et al. Temozolomide down-regulates P-glycoprotein in human blood-brain barrier cells by disrupting Wnt3-signalling. Cell Mol Life Sci 2014; 71: 499-516.
7. Tsuji T, Ohta Y, Kanno Y, Hirose K, Ohashi K, Mizuno K. Involvement of p114- RhoGEF and Lfc in Wnt-3a- and dishevelled-induced RhoA activation and neurite retraction in N1E-115 mouse neuroblastoma cells. Mol Biol Cell 2010; 21: 3590-3600.
8. Rossol-Allison J, Stemmle LN, Swenson-Fields KI, Kelly P, Fields PE, McCall SJ et al. Rho GTPase activity modulates Wnt3a/beta-catenin signaling. Cell Signal 2009; 21: 1559-1568.
9. Chang CC, Lee PS, Chou Y, Hwang LL, Juan SH. Mediating effects of aryl-hydrocarbon receptor and RhoA in altering brain vascular integrity: the therapeutic potential of statins. Am J Pathol 2012; 181: 211-221.
10. Allen C, Srivastava K, Bayraktutan U. Small GTPase RhoA and its effector rho kinase mediate oxygen glucose deprivation-evoked in vitro cerebral barrier dysfunction. Stroke 2010; 41: 2056-2063.
11. Pinzón-Daza ML, Garzón R, Couraud PO, Romero IA, Weksler B, Ghigo D et al. The association of statins plus LDL receptor-targeted liposome-encapsulated doxorubicin increases the in vitro drug delivery across blood-brain barrier cells. Brit J Pharmacol 2012; 167: 1431-1447.
12. Flatau G, Lemichez E, Gauthier M, Chardin P, Paris S, Fiorentini C et al. Toxininduced activation of the G protein p21 Rho by deamidation of glutamine. Nature 1997; 387: 729-733.
13. Weksler BB, Subileau EA, Perrière N, Charneau P, Holloway K, Leveque M et al. Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J 2005; 19: 1872-1894.
14. Doublier S, Riganti C, Voena C, Costamagna C, Aldieri E, Pescarmona G et al. RhoA silencing reverts the resistance to doxorubicin in human colon cancer cells. Mol Cancer Res 2008; 6: 1607-1620.
15. Monnaert V, Betbeder D, Fenart L, Bricout H, Lenfant AM, Landry C et al. Effects of g- and hydroxypropyl-g-cyclodextrins on the transport of doxorubicin across an in vitro model of blood-brain barrier. J Pharmacol Exp Ther 2004; 311: 1115-1120.
16. Eigenmann DE, Xue G, Kim KS, Moses AV, Hamburger M, Oufir M. Comparative study of four immortalized human brain capillary endothelial cell lines, hCMEC/ D3, hBMEC, TY10, and BB19, and optimization of culture conditions, for an in vitro blood-brain barrier model for drug permeability studies. Fluids Barriers CNS 2013; 10: e33.
17. Siflinger-Birnboim A, Del Vecchio PJ, Cooper JA, Blumenstock FA, Shepard JM, Malik AB. Molecular sieving characteristics of the cultured endothelial monolayer. J Cell Physiol 1987; 132: 111-117.
18. Riganti C, Salaroglio IC, Caldera V, Campia I, Kopecka J, Mellai M et al. Temozolomide down-regulates P-glycoprotein expression in glioblastoma stem cells by interfering with the Wnt3a/GSK3/b-catenin pathway. Neuro Oncol 2013; 15: 1502-1517.
19. Mobasher MA, González-Rodriguez A, Santamaría B, Ramos S, Martín MÁ, Goya L et al. Protein tyrosine phosphatase 1B modulates GSK3b/Nrf2 and IGFIR signaling pathways in acetaminophen-induced hepatotoxicity. Cell Death Dis 2003; 4: e626.
20. Moeslein FM, Myers MP, Landreth GE. The CLK family kinases, CLK1 and CLK2, phosphorylate and activate the tyrosine phosphatase, PTP-1B. J Biol Chem 1999; 274: 26697-26704.
21. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATPdependent transporters. Nat Rev Cancer 2002; 2: 48-58.
22. Tai LM, Loughlin AJ, Male DK, Romero IA. P-glycoprotein and breast cancer resistance protein restrict apical-to-basolateral permeability of human brain endothelium to amyloid-b. J Cereb Blood Flow Metab 2009; 29: 1079-1083.
23. de Jesus Perez VA, Alastalo TP, Wu JC, Axelrod JD, Cooke JP, Amieva M et al. Bone morphogenetic protein 2 induces pulmonary angiogenesis via Wnt-beta-catenin and Wnt-RhoA-Rac1 pathways. J Cell Biol 2009; 184: 83-99.
24. Liu J, Zhang Y, Xu R, Du J, Hu Z, Yang L et al. PI3K/Akt-dependent phosphorylation of GSK3b and activation of RhoA regulate Wnt5a-induced gastric cancer cell migration. Cell Signal 2013; 25: 447-456.
25. Uchida Y, Ohtsuki S, Katsukura Y, Ikeda C, Suzuki T, Kamiie J et al. Quantitative targeted absolute proteomics of human blood-brain barrier transporters and receptors. J Neurochem 2011; 117: 333-345.
26. Jope RS, Johnson GV. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci 2004; 29: 95-102.
27. Bareiss S, Kim K, Lu Q. Delta-catenin/NPRAP: A new member of the glycogen synthase kinase-3beta signaling complex that promotes beta-catenin turnover in neurons. J Neurosci Res 2010; 88: 2350-2363.
28. Zoerle T, Ilodigwe DC, Wan H, Lakovic K, Sabri M, Ai J et al. Pharmacologic reduction of angiographic vasospasm in experimental subarachnoid hemorrhage: systematic review and meta-analysis. J Cereb Blood Flow Metab 2012; 32: 1645-1658.
29. Shin HK, Huang PL, Ayata C. Rho-kinase inhibition improves ischemic perfusion deficit in hyperlipidemic mice. J Cereb Blood Flow Metab 2014; 34: 284-287.
30. Eldawoody H, Shimizu H, Kimura N, Saito A, Nakayama T, Takahashi A et al. Fasudil, a Rho-kinase inhibitor, attenuates induction and progression of cerebral aneurysms: experimental study in rats using vascular corrosion casts. Neurosci Lett 2010; 470: 76-80.
31. Hau P, Fabel K, Baumgart U, Rummele P, Grauer O, Bock A et al. Pegylated liposomal doxorubicin-efficacy in patients with recurrent high-grade glioma. Cancer 2004; 100: 1199-1207.
32. Agarwal S, Hartz AM, Elmquist WF, Bauer B. Breast cancer resistance protein and P-glycoprotein in brain cancer: two gatekeepers team up. Curr Pharm Des 2011; 17: 2793-2802.
33. Qu Q, Chu JW, Sharom FJ. Transition state P-glycoprotein binds drugs and modulators with unchanged affinity, suggesting a concerted transport mechanism. Biochemistry 2003; 42: 1345-1353.
34. Chikazawa N, Tanaka H, Tasaka T, Nakamura M, Tanaka M, Onishi H et al. Inhibition of Wnt signaling pathway decreases chemotherapy-resistant side-population colon cancer cells. Anticancer Res 2010; 30: 2041-2048.
35. Flahaut M, Meier R, Coulon A, Nardou KA, Niggli FK, Martinet D et al. The Wnt receptor FZD1 mediates chemoresistance in neuroblastoma through activation of the Wnt/beta-catenin pathway. Oncogene 2009; 28: 2245-2256.
36. Corrêa S, Binato R, Du Rocher B, Castelo-Branco MT, Pizzatti L, Abdelhay E. Wnt/bcatenin pathway regulates ABCB1 transcription in chronic myeloid leukemia. BMC Cancer 2012; 12: e303.
37. Shen DY, Zhang W, Zeng X, Liu CQ. Inhibition of Wnt/b-catenin signaling downregulates P-glycoprotein and reverses multi-drug resistance of cholangiocarcinoma. Cancer Sci 2013; 104: 1303-1308.
38. Kobune M, Chiba H, Kato J, Kato K, Nakamura K, Kawano Y et al. Wnt3/RhoA/ROCK signaling pathway is involved in adhesion-mediated drug resistance of multiple myeloma in an autocrine mechanism. Mol Cancer Ther 2007; 6: 1774-1784.
39. Serwer LP, James CD. Challenges in drug delivery to tumors of the central nervous system: an overview of pharmacological and surgical considerations. Adv Drug Deliv Rev 2012; 64: 590-597.
40. Pinzón-Daza ML, Campia I, Kopecka J, Garzón R, Ghigo D, Riganti C. Nanoparticleand liposome-carried drugs: new strategies for active targeting and drug delivery across blood-brain barrier. Curr Drug Metab 2013; 14: 625-640.