Functional regulation of P-glycoprotein at the blood-brain barrier in proton-coupled folate transporter (PCFT) mutant mice

FASEB Journal

Volumn 27, Issue 3, 2013, Pages 1167-1175

  Wang, Xueqian ^a   Cabrera, Robert M ^a   Li, Yue ^a   Miller, David S ^c   Finnell, Richard H ^a,b  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

ABC transporters; Brain capillaries; Valproic acid

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; CLAUDIN 1; MULTIDRUG RESISTANCE PROTEIN; OCCLUDIN; PROTEIN ZO1; PROTON COUPLED FOLATE TRANSPORTER; VALPROIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY; CONTROLLED STUDY; FOLIC ACID DEFICIENCY; IMMUNOHISTOCHEMISTRY; MOUSE; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN FUNCTION; TIGHT JUNCTION; WESTERN BLOTTING; WILD TYPE;

ANIMALS; ANTICONVULSANTS; BIOLOGICAL TRANSPORT, ACTIVE; BLOOD-BRAIN BARRIER; LEUCOVORIN; MICE; MICE, MUTANT STRAINS; NERVOUS SYSTEM DISEASES; P-GLYCOPROTEIN; PROTON-COUPLED FOLATE TRANSPORTER; TERATOGENS; TETRACHLORODIBENZODIOXIN; TIGHT JUNCTIONS; VALPROIC ACID; VITAMIN B COMPLEX;

EID: 84874638954     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-218495     Document Type: Article

References (41)

1. Blom, H. J., Shaw, G. M., den Heijer, M., and Finnell, R. H. (2006) Neural tube defects and folate: case far from closed. Nat. Rev. Neurosci. 7, 724-731 (Pubitemid 44267496)
2. Goh, Y. I., and Koren, G. (2008) Folic acid in pregnancy and fetal outcomes. J. Obstet. Gynaecol. 28, 3-13 (Pubitemid 351220605)
3. Obican, S. G., Finnell, R. H., Mills, J. L., Shaw, G. M., and Scialli, A. R. (2010) Folic acid in early pregnancy: a public health success story. FASEB J. 24, 4167-4174
4. Mangold, S., Blau, N., Opladen, T., Steinfeld, R., Wessling, B., Zerres, K., and Hausler, M. (2011) Cerebral folate deficiency: a neurometabolic syndrome? Mol. Genet. Metab. 104, 369-372
5. Zhao, R., Diop-Bove, N., Visentin, M., and Goldman, I. D. (2011) Mechanisms of membrane transport of folates into cells and across epithelia. Annu. Rev. Nutr. 31, 177-201
6. Hyland, K., Shoffner, J., and Heales, S. J. (2010) Cerebral folate deficiency. J. Inherit. Metab. Dis. 33, 563-570
7. Carney, R. M., Wolpert, C. M., Ravan, S. A., Shahbazian, M., Ashley-Koch, A., Cuccaro, M. L., Vance, J. M., and Pericak-Vance, M. A. (2003) Identification of MeCP2 mutations in a series of females with autistic disorder. Pediatr. Neurol. 28, 205-211 (Pubitemid 36593431)
8. Mercimek-Mahmutoglu, S., and Stockler-Ipsiroglu, S. (2007) Cerebral folate deficiency and folinic acid treatment in hypomyelination with atrophy of the basal ganglia and cerebellum (H-ABC) syndrome. Tohoku J. Exp. Med. 211, 95-96, author reply 97 (Pubitemid 46062224)
9. Piedrahita, J. A., Oetama, B., Bennett, G. D., van Waes, J., Kamen, B. A., Richardson, J., Lacey, S. W., Anderson, R. G., and Finnell, R. H. (1999) Mice lacking the folic acid-binding protein Folbp1 are defective in early embryonic development. Nat. Genet. 23, 228-232 (Pubitemid 29455399)
10. Salojin, K. V., Cabrera, R. M., Sun, W., Chang, W. C., Lin, C., Duncan, L., Platt, K. A., Read, R., Vogel, P., Liu, Q., Finnell, R. H., and Oravecz, T. (2011) A mouse model of hereditary folate malabsorption: deletion of the PCFT gene leads to systemic folate deficiency. Blood 117, 4895-4904
11. Abbott, N. J., Patabendige, A. A., Dolman, D. E., Yusof, S. R., and Begley, D. J. Structure and function of the blood-brain barrier. Neurobiol. Dis. 37, 13-25
12. Miller, D. S. (2010) Regulation of P-glycoprotein and other ABC drug transporters at the blood-brain barrier. Trends Pharmacol. Sci. 31, 246-254
13. Assaraf, Y. G., Rothem, L., Hooijberg, J. H., Stark, M., Ifergan, I., Kathmann, I., Dijkmans, B. A., Peters, G. J., and Jansen, G. (2003) Loss of multidrug resistance protein 1 expression and folate efflux activity results in a highly concentrative folate transport in human leukemia cells. J. Biol. Chem. 278, 6680-6686 (Pubitemid 36800654)
14. Assaraf, Y. G. (2006) The role of multidrug resistance efflux transporters in antifolate resistance and folate homeostasis. Drug Resist. Updat. 9, 227-246 (Pubitemid 44750843)
15. Hooijberg, J. H., Broxterman, H. J., Kool, M., Assaraf, Y. G., Peters, G. J., Noordhuis, P., Scheper, R. J., Borst, P., Pinedo, H. M., and Jansen, G. (1999) Antifolate resistance mediated by the multidrug resistance proteins MRP1 and MRP2. Cancer Res. 59, 2532-2535 (Pubitemid 29269093)
16. Hooijberg, J. H., Peters, G. J., Assaraf, Y. G., Kathmann, I., Priest, D. G., Bunni, M. A., Veerman, A. J., Scheffer, G. L., Kaspers, G. J., and Jansen, G. (2003) The role of multidrug resistance proteins MRP1, MRP2 and MRP3 in cellular folate homeostasis. Biochem. Pharmacol. 65, 765-771 (Pubitemid 36293693)
17. Wang, X., Sykes, D. B., and Miller, D. S. (2010) Constitutive androstane receptor-mediated up-regulation of ATP-driven xenobiotic efflux transporters at the blood-brain barrier. Mol. Pharmacol. 78, 376-383
18. Wang, X., Hawkins, B. T., and Miller, D. S. (2011) Aryl hydrocarbon receptor-mediated up-regulation of ATP-driven xenobiotic efflux transporters at the blood-brain barrier. FASEB J. 25, 644-652
19. Bauer, B., Hartz, A. M., Fricker, G., and Miller, D. S. (2004) Pregnane X receptor up-regulation of P-glycoprotein expression and transport function at the blood-brain barrier. Mol. Pharmacol. 66, 413-419 (Pubitemid 39329239)
20. Schramm, U., Fricker, G., Wenger, R., and Miller, D. S. (1995) P-glycoprotein-mediated secretion of a fluorescent cyclosporin analogue by teleost renal proximal tubules. Am. J. Physiol. 268, F46-F52 (Pubitemid 124005459)
21. Hartz, A. M., Bauer, B., Fricker, G., and Miller, D. S. (2004) Rapid regulation of P-glycoprotein at the blood-brain barrier by endothelin-1. Mol. Pharmacol. 66, 387-394 (Pubitemid 39329237)
22. Miller, D. S., Nobmann, S. N., Gutmann, H., Toeroek, M., Drewe, J., and Fricker, G. (2000) Xenobiotic transport across isolated brain microvessels studied by confocal microscopy. Mol. Pharmacol. 58, 1357-1367
23. Bauer, B., Yang, X., Hartz, A. M., Olson, E. R., Zhao, R., Kalvass, J. C., Pollack, G. M., and Miller, D. S. (2006) In vivo activation of human pregnane X receptor tightens the blood-brain barrier to methadone through P-glycoprotein up-regulation. Mol. Pharmacol. 70, 1212-1219 (Pubitemid 44435972)
24. Yang, H. W., Liu, H. Y., Liu, X., Zhang, D. M., Liu, Y. C., Liu, X. D., Wang, G. J., and Xie, L. (2008) Increased P-glycoprotein function and level after long-term exposure of four antiepileptic drugs to rat brain microvascular endothelial cells in vitro. Neurosci. Lett. 434, 299-303
25. Cerveny, L., Svecova, L., Anzenbacherova, E., Vrzal, R., Staud, F., Dvorak, Z., Ulrichova, J., Anzenbacher, P., and Pavek, P. (2007) Valproic acid induces CYP3A4 and MDR1 gene expression by activation of constitutive androstane receptor and pregnane X receptor pathways. Drug Metab. Dispos. 35, 1032-1041 (Pubitemid 46956421)
26. Miller, D. S., Bauer, B., and Hartz, A. M. (2008) Modulation of P-glycoprotein at the blood-brain barrier: opportunities to improve central nervous system pharmacotherapy. Pharmacol. Rev. 60, 196-209 (Pubitemid 351962009)
27. Loscher, W., and Potschka, H. (2005) Drug resistance in brain diseases and the role of drug efflux transporters. Nat. Rev. Neurosci. 6, 591-602 (Pubitemid 41059334)
28. Takizawa, D., Kakizaki, S., Horiguchi, N., Tojima, H., Yamazaki, Y., Ichikawa, T., Sato, K., and Mori, M. (2010) Histone deacetylase inhibitors induce cytochrome P-450 2B by activating nuclear receptor constitutive androstane receptor. Drug Metab. Dispos. 38, 1493-1498
29. Wang, X., Hawkins, B. T., and Miller, D. S. (2011) Activating PKC-beta1 at the blood-brain barrier reverses induction of P-glycoprotein activity by dioxin and restores drug delivery to the CNS. J. Cereb. Blood Flow Metab. 31, 1371-1375
30. Bednarczyk, J., and Lukasiuk, K. (2011) Tight junctions in neurological diseases. Acta Neurobiol. Exp. (Wars.) 71, 393-408
31. Blau, N., Bonafe, L., Krageloh-Mann, I., Thony, B., Kierat, L., Hausler, M., and Ramaekers, V. (2003) Cerebrospinal fluid pterins and folates in Aicardi-Goutieres syndrome: a new phenotype. Neurology 61, 642-647 (Pubitemid 37082601)
32. Garcia-Cazorla, A., Quadros, E. V., Nascimento, A., Garcia-Silva, M. T., Briones, P., Montoya, J., Ormazabal, A., Artuch, R., Sequeira, J. M., Blau, N., Arenas, J., Pineda, M., and Ramaekers, V. T. (2008) Mitochondrial diseases associated with cerebral folate deficiency. Neurology 70, 1360-1362 (Pubitemid 351550342)
33. Steinfeld, R., Grapp, M., Kraetzner, R., Dreha-Kulaczewski, S., Helms, G., Dechent, P., Wevers, R., Grosso, S., and Gartner, J. (2009) Folate receptor alpha defect causes cerebral folate transport deficiency: a treatable neurodegenerative disorder associated with disturbed myelin metabolism. Am. J. Hum. Genet. 85, 354-363
34. Perez-Duenas, B., Toma, C., Ormazabal, A., Muchart, J., Sanmarti, F., Bombau, G., Serrano, M., Garcia-Cazorla, A., Cormand, B., and Artuch, R. (2010) Progressive ataxia and myoclonic epilepsy in a patient with a homozygous mutation in the FOLR1 gene. J. Inherit. Metab. Dis. 33, 795-802
35. Zhao, R., Min, S. H., Wang, Y., Campanella, E., Low, P. S., and Goldman, I. D. (2009) A role for the proton-coupled folate transporter (PCFT-SLC46A1) in folate receptor-mediated endocytosis. J. Biol. Chem. 284, 4267-4274
36. Cario, H., Bode, H., Debatin, K. M., Opladen, T., and Schwarz, K. (2009) Congenital null mutations of the FOLR1 gene: a progressive neurologic disease and its treatment. Neurology 73, 2127-2129
37. Kruh, G. D., and Belinsky, M. G. (2003) The MRP family of drug efflux pumps. Oncogene 22, 7537-7552 (Pubitemid 37487175)
38. Ifergan, I., Shafran, A., Jansen, G., Hooijberg, J. H., Scheffer, G. L., and Assaraf, Y. G. (2004) Folate deprivation results in the loss of breast cancer resistance protein (BCRP/ABCG2) expression. A role for BCRP in cellular folate homeostasis. J. Biol. Chem. 279, 25527-25534 (Pubitemid 38756812)
39. Deeley, R. G., Westlake, C., and Cole, S. P. (2006) Transmembrane transport of endo- and xenobiotics by mammalian ATPbinding cassette multidrug resistance proteins. Physiol. Rev. 86, 849-899 (Pubitemid 44033384)
40. Mottino, A. D., Hoffman, T., Jennes, L., and Vore, M. (2000) Expression and localization of multidrug resistant protein mrp2 in rat small intestine. J. Pharmacol. Exp. Ther. 293, 717-723 (Pubitemid 30417835)
41. Robey, R. W., To, K. K., Polgar, O., Dohse, M., Fetsch, P., Dean, M., and Bates, S. E. (2009) ABCG2: a perspective. Adv. Drug Deliv. Rev. 61, 3-13