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Inflammation Modulates RLIP76/RALBP1 Electrophile-Glutathione Conjugate Transporter and Housekeeping Genes in Human Blood-Brain Barrier Endothelial Cells

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Bennani-Baiti, Barbara, Toegel, Stefan, Viernstein, Helmut, Urban, Ernst, Noe, Christian R., Bennani-Baiti, Idriss M.·2015·PLOS ONE
DOI 10.1371/journal.pone.0139101PMC PMC4583384
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Abstract

Endothelial cells are often present at inflammation sites. This is the case of endothelial cells of the blood-brain barrier (BBB) of patients afflicted with neurodegenerative disorders such as Alzheimer's, Parkinson's, or multiple sclerosis, as well as in cases of bacterial meningitis, trauma, or tumor-associated ischemia. Inflammation is a known modulator of gene expression through the activation of transcription factors, mostly NF-κB. RLIP76 (a.k.a. RALBP1), an ATP-dependent transporter of electrophile-glutathione conjugates, modulates BBB permeability through the regulation of tight junction function, cell adhesion, and exocytosis. Genes and pathways regulated by RLIP76 are transcriptional targets of tumor necrosis factor alpha (TNF-α) pro-inflammatory molecule, suggesting that RLIP76 may also be an inflammation target. To assess the effects of TNF-α on RLIP76, we faced the problem of choosing reference genes impervious to TNF-α. Since such genes were not known in human BBB endothelial cells, we subjected these to TNF-α, and measured by quantitative RT-PCR the expression of housekeeping genes commonly used as reference genes. We find most to be modulated, and analysis of several inflammation datasets as well as a metaanalysis of more than 5000 human tissue samples encompassing more than 300 cell types and diseases show that no single housekeeping gene may be used as a reference gene. Using three different algorithms, however, we uncovered a reference geneset impervious to TNF-α, and show for the first time that RLIP76 expression is induced by TNF-α and follows the induction kinetics of inflammation markers, suggesting that inflammation can influence RLIP76 expression at the BBB. We also show that MRP1 (a.k.a. ABCC1), another electrophile-glutathione transporter, is not modulated in the same cells and conditions, indicating that RLIP76 regulation by TNF-α is not a general property of glutathione transporters. The reference geneset uncovered herein should aid in future gene expression studies in inflammatory conditions of the BBB.

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  • TNFα induces Rlip expression in blood brain barrier endothelial cells during inflammation.

    “In keeping with Rlip’s role as a stress responsive protein, it has been reported that TNFα induces Rlip expression in blood brain barrier endothelial cells during inflammation [42].”

    From Rlip76: An Unexplored Player in Neurodegeneration and Alzheimer’s Disease? (2022) · cites this paper as [42]

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  1. [1]Golias C, Tsoutsi E, Matziridis A, Makridis P, Batistatou A, Charalabopoulos K. Review. Leukocyte and endothelial cell adhesion molecules in inflammation focusing on inflammatory heart disease. In Vivo. 2007; 21(5): 757– 69.. 18019409
  2. [2]Schmid MC, Schulein R, Dehio M, Denecker G, Carena I, Dehio C. The VirB type IV secretion system of Bartonella henselae mediates invasion, proinflammatory activation and antiapoptotic protection of endothelial cells. Mol Microbiol. 2004; 52(1): 81– 92.. 15049812
  3. [3]Vallance P, Collier J, Bhagat K. Infection, inflammation, and infarction: does acute endothelial dysfunction provide a link? Lancet. 1997; 349(9062): 1391– 2.. 9149715
  4. [4]Silva Y, Leira R, Tejada J, Lainez JM, Castillo J, Davalos A. Molecular signatures of vascular injury are associated with early growth of intracerebral hemorrhage. Stroke. 2005; 36(1): 86– 91.. 15550687
  5. [5]Marboeuf P, Corseaux D, Mouquet F, Van Belle E, Jude B, Susen S. Inflammation triggers colony forming endothelial cell mobilization after angioplasty in chronic lower limb ischemia. J Thromb Haemost. 2008; 6(1): 195– 7.. 17916228
  6. [6]Beekhuizen H, van de Gevel JS. Endothelial cell adhesion molecules in inflammation and postischemic reperfusion injury. Transplant Proc. 1998; 30(8): 4251– 6.. 9865357
  7. [7]Kupatt C, Habazettl H, Becker BF, Boekstegers P. Endothelial activation—a strategic event during postischemic myocardial inflammation. Z Kardiol. 2000; 89 Suppl 9:IX/ 96– 100.. 11151805
  8. [8]Arnaud C, Mach F. Pleiotropic effects of statins in atherosclerosis: role on endothelial function, inflammation and immunomodulation. Arch Mal Coeur Vaiss. 2005; 98(6): 661– 6.. 16007821
  9. [9]Gimbrone MA Jr., Bevilacqua MP, Cybulsky MI. Endothelial-dependent mechanisms of leukocyte adhesion in inflammation and atherosclerosis. Ann N Y Acad Sci. 1990; 598: 77– 85.. 1701076
  10. [10]Lahera V, Goicoechea M, de Vinuesa SG, Miana M, de las Heras N, Cachofeiro V, et al Endothelial dysfunction, oxidative stress and inflammation in atherosclerosis: beneficial effects of statins. Curr Med Chem. 2007; 14(2): 243– 8.. 17266583
  11. [11]Deban L, Correale C, Vetrano S, Malesci A, Danese S. Multiple pathogenic roles of microvasculature in inflammatory bowel disease: a Jack of all trades. Am J Pathol. 2008; 172(6): 1457– 66. 10.2353/ajpath.2008.070593 18458096 PMC2408406 · DOI
  12. [12]Horowitz S, Binion DG, Nelson VM, Kanaa Y, Javadi P, Lazarova Z, et al Increased arginase activity and endothelial dysfunction in human inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol. 2007; 292(5): G1323– 36.. 17218473
  13. [13]Schinzari F, Armuzzi A, De Pascalis B, Mores N, Tesauro M, Melina D, et al Tumor necrosis factor-alpha antagonism improves endothelial dysfunction in patients with Crohn's disease. Clin Pharmacol Ther. 2008; 83(1): 70– 6.. 17507924
  14. [14]Minagar A, Jy W, Jimenez JJ, Alexander JS. Multiple sclerosis as a vascular disease. Neurol Res. 2006; 28(3): 230– 5.. 16687046
  15. [15]Higashi Y, Goto C, Jitsuiki D, Umemura T, Nishioka K, Hidaka T, et al Periodontal infection is associated with endothelial dysfunction in healthy subjects and hypertensive patients. Hypertension. 2008; 51(2): 446– 53.. 18039979
  16. [16]Moutsopoulos NM, Madianos PN. Low-grade inflammation in chronic infectious diseases: paradigm of periodontal infections. Ann N Y Acad Sci. 2006; 1088: 251– 64.. 17192571
  17. [17]Seinost G, Wimmer G, Skerget M, Thaller E, Brodmann M, Gasser R, et al Periodontal treatment improves endothelial dysfunction in patients with severe periodontitis. Am Heart J. 2005; 149(6): 1050– 4.. 15976787
  18. [18]Tonetti MS, D'Aiuto F, Nibali L, Donald A, Storry C, Parkar M, et al Treatment of periodontitis and endothelial function. N Engl J Med. 2007; 356(9): 911– 20.. 17329698
  19. [19]Gonzalez-Gay MA, Gonzalez-Juanatey C, Martin J. Inflammation and endothelial dysfunction in rheumatoid arthritis. Clin Exp Rheumatol. 2006; 24(2): 115– 7.. 16762143
  20. [20]Kerekes G, Szekanecz Z, Der H, Sandor Z, Lakos G, Muszbek L, et al Endothelial dysfunction and atherosclerosis in rheumatoid arthritis: a multiparametric analysis using imaging techniques and laboratory markers of inflammation and autoimmunity. J Rheumatol. 2008; 35(3): 398– 406.. 18203326
  21. [21]Antoniades C, Tousoulis D, Marinou K, Papageorgiou N, Bosinakou E, Tsioufis C, et al Effects of insulin dependence on inflammatory process, thrombotic mechanisms and endothelial function, in patients with type 2 diabetes mellitus and coronary atherosclerosis. Clin Cardiol. 2007; 30(6): 295– 300.. 17551966 PMC6653670
  22. [22]Leinonen ES, Hiukka A, Hurt-Camejo E, Wiklund O, Sarna SS, Mattson Hulten L, et al Low-grade inflammation, endothelial activation and carotid intima-media thickness in type 2 diabetes. J Intern Med. 2004; 256(2): 119– 27.. 15257724
  23. [23]Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008; 454(7203): 436– 44. Epub 2008/07/25. nature07205 [pii] 10.1038/nature07205. 18650914 · DOI · Paper page
  24. [24]Pitroda SP, Zhou T, Sweis RF, Filippo M, Labay E, Beckett MA, et al Tumor endothelial inflammation predicts clinical outcome in diverse human cancers. PLoS One. 2012; 7(10): e46104 Epub 2012/10/12. doi: 10.1371/journal.pone.0046104 PONE-D-12-07623 [pii]. 23056240 PMC3464251 · DOI
  25. [25]Kalinowska A, Losy J. PECAM-1, a key player in neuroinflammation. Eur J Neurol. 2006; 13(12): 1284– 90.. 17116209
  26. [26]Sharief MK, Ciardi M, Thompson EJ. Blood-brain barrier damage in patients with bacterial meningitis: association with tumor necrosis factor-alpha but not interleukin-1 beta. J Infect Dis. 1992; 166(2): 350– 8.. 1634806
  27. [27]Beck KD, Nguyen HX, Galvan MD, Salazar DL, Woodruff TM, Anderson AJ. Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain. 2010; 133(Pt 2): 433– 47. Epub 2010/01/21. doi: 10.1093/brain/awp322 awp322 [pii]. 20085927 PMC2858013 · DOI
  28. [28]Chapouly C, Tadesse Argaw A, Horng S, Castro K, Zhang J, Asp L, et al Astrocytic TYMP and VEGFA drive blood-brain barrier opening in inflammatory central nervous system lesions. Brain. 2015; 138(Pt 6): 1548– 67. Epub 2015/03/26. doi: 10.1093/brain/awv077 awv077 [pii].. 25805644 PMC4614128 · DOI
  29. [29]Minten C, Alt C, Gentner M, Frei E, Deutsch U, Lyck R, et al DARC shuttles inflammatory chemokines across the blood-brain barrier during autoimmune central nervous system inflammation. Brain. 2014; 137(Pt 5): 1454– 69. Epub 2014/03/15. doi: 10.1093/brain/awu045 awu045 [pii]. 24625696 PMC3999718 · DOI
  30. [30]Stamatovic SM, Dimitrijevic OB, Keep RF, Andjelkovic AV. Inflammation and brain edema: new insights into the role of chemokines and their receptors. Acta Neurochir Suppl. 2006; 96: 444– 50.. 16671502
  31. [31]Liu JY, Thom M, Catarino CB, Martinian L, Figarella-Branger D, Bartolomei F, et al Neuropathology of the blood-brain barrier and pharmaco-resistance in human epilepsy. Brain. 2012; 135(Pt 10): 3115– 33. Epub 2012/07/04. doi: 10.1093/brain/aws147 aws147 [pii].. 22750659 · DOI
  32. [32]Vezzani A, Granata T. Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia. 2005; 46(11): 1724– 43.. 16302852
  33. [33]Carvey PM, Zhao CH, Hendey B, Lum H, Trachtenberg J, Desai BS, et al 6-Hydroxydopamine-induced alterations in blood-brain barrier permeability. Eur J Neurosci. 2005; 22(5): 1158– 68.. 16176358
  34. [34]Wilms H, Zecca L, Rosenstiel P, Sievers J, Deuschl G, Lucius R. Inflammation in Parkinson's diseases and other neurodegenerative diseases: cause and therapeutic implications. Curr Pharm Des. 2007; 13(18): 1925– 8.. 17584117
  35. [35]Franscini N, Bachli EB, Blau N, Leikauf MS, Schaffner A, Schoedon G. Gene expression profiling of inflamed human endothelial cells and influence of activated protein C. Circulation. 2004; 110(18): 2903– 9.. 15505101
  36. [36]Gu J, Chen Y, Li S, Li Y. Identification of responsive gene modules by network-based gene clustering and extending: application to inflammation and angiogenesis. BMC Syst Biol. 2010; 4: 47 Epub 2010/04/22. doi: 10.1186/1752-0509-4-47 1752-0509-4-47 [pii]. 20406493 PMC2873318 · DOI
  37. [37]Lok CA, Boing AN, Reitsma PH, van der Post JA, van Bavel E, Boer K, et al Expression of inflammation-related genes in endothelial cells is not directly affected by microparticles from preeclamptic patients. J Lab Clin Med. 2006; 147(6): 310– 20.. 16750669
  38. [38]Zhou J, Jin Y, Gao Y, Wang H, Hu G, Huang Y, et al Genomic-scale analysis of gene expression profiles in TNF-alpha treated human umbilical vein endothelial cells. Inflamm Res. 2002; 51(7): 332– 41.. 12146724
  39. [39]De Martin R, Hoeth M, Hofer-Warbinek R, Schmid JA. The transcription factor NF-kappa B and the regulation of vascular cell function. Arterioscler Thromb Vasc Biol. 2000; 20(11): E83– 8.. 11073859
  40. [40]Kracht M, Saklatvala J. Transcriptional and post-transcriptional control of gene expression in inflammation. Cytokine. 2002; 20(3): 91– 106.. 12453467
  41. [41]Lee YW, Eum SY, Chen KC, Hennig B, Toborek M. Gene expression profile in interleukin-4-stimulated human vascular endothelial cells. Mol Med. 2004; 10(1–6): 19– 27.. 15502879 PMC1431351
  42. [42]Rahman I. Oxidative stress, chromatin remodeling and gene transcription in inflammation and chronic lung diseases. J Biochem Mol Biol. 2003; 36(1): 95– 109.. 12542980
  43. [43]Ruminy P, Gangneux C, Claeyssens S, Scotte M, Daveau M, Salier JP. Gene transcription in hepatocytes during the acute phase of a systemic inflammation: from transcription factors to target genes. Inflamm Res. 2001; 50(8): 383– 90.. 11556518
  44. [44]Mori R, Wang Q, Danenberg KD, Pinski JK, Danenberg PV. Both beta-actin and GAPDH are useful reference genes for normalization of quantitative RT-PCR in human FFPE tissue samples of prostate cancer. Prostate. 2008; 68(14): 1555– 60. 10.1002/pros.20815 18651557 · DOI
  45. [45]Murthi P, Fitzpatrick E, Borg AJ, Donath S, Brennecke SP, Kalionis B. GAPDH, 18S rRNA and YWHAZ are suitable endogenous reference genes for relative gene expression studies in placental tissues from human idiopathic fetal growth restriction. Placenta. 2008; 29(9): 798– 801. 10.1016/j.placenta.2008.06.007 18684503 · DOI
  46. [46]Cummings M, Sarveswaran J, Homer-Vanniasinkam S, Burke D, Orsi NM. Glyceraldehyde-3-phosphate Dehydrogenase is an Inappropriate Housekeeping Gene for Normalising Gene Expression in Sepsis. Inflammation. 2014; 37(5): 1889– 94. Epub 2014/05/27. 10.1007/s10753-014-9920-3. 24858725 · DOI
  47. [47]Thorrez L, Van Deun K, Tranchevent LC, Van Lommel L, Engelen K, Marchal K, et al Using ribosomal protein genes as reference: a tale of caution. PLoS ONE. 2008; 3(3): e1854 10.1371/journal.pone.0001854 18365009 PMC2267211 · DOI
  48. [48]Bamias G, Goukos D, Laoudi E, Balla IG, Siakavellas SI, Daikos GL, et al Comparative study of candidate housekeeping genes for quantification of target gene messenger RNA expression by real-time PCR in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2013; 19(13): 2840– 7. Epub 2013/10/22. 10.1097/01.MIB.0000435440.22484.e8. 24141710 · DOI
  49. [49]Montero-Melendez T, Perretti M. Gapdh gene expression is modulated by inflammatory arthritis and is not suitable for qPCR normalization. Inflammation. 2014; 37(4): 1059– 69. Epub 2014/02/05. 10.1007/s10753-014-9829-x. 24493325 · DOI
  50. [50]Barar J, Gumbleton M, Asadi M, Omidi Y. Barrier functionality and transport machineries of human ECV304 cells. Med Sci Monit. 2010; 16(1): BR52– 60. Epub 2009/12/29. 878321 [pii].. 20037486
  51. [51]Gonzalez-Burgos E, Carretero ME, Gomez-Serranillos MP. In vitro permeability study of CNS-active diterpenes from Sideritis spp. using cellular models of blood-brain barrier. Planta Med. 2013; 79(16): 1545– 51. Epub 2013/09/14. 10.1055/s-0033-1350797. 24030291 · DOI
  52. [52]Liverani E, Paul C. Glucocorticoids alter adrenomedullin receptor expression and secretion in endothelial-like cells and astrocytes. Int J Biochem Cell Biol. 2013; 45(12): 2715– 23. Epub 2013/10/08. doi: 10.1016/j.biocel.2013.09.009 S1357-2725(13)00298-7 [pii].. 24096124 · DOI
  53. [53]Neuhaus W, Freidl M, Szkokan P, Berger M, Wirth M, Winkler J, et al Effects of NMDA receptor modulators on a blood-brain barrier in vitro model. Brain Res. 2011; 1394: 49– 61. Epub 2011/05/10. doi: 10.1016/j.brainres.2011.04.003 S0006-8993(11)00670-6 [pii].. 21549356 · DOI
  54. [54]Neuhaus W, Mandikova J, Pawlowitsch R, Linz B, Bennani-Baiti B, Lauer R, et al Blood-brain barrier in vitro models as tools in drug discovery: assessment of the transport ranking of antihistaminic drugs. Pharmazie. 2012; 67(5): 432– 9. Epub 2012/07/07.. 22764578
  55. [55]Novakova I, Subileau EA, Toegel S, Gruber D, Lachmann B, Urban E, et al Transport rankings of non-steroidal antiinflammatory drugs across blood-brain barrier in vitro models. PLoS One. 2014; 9(1): e86806 Epub 2014/01/28. doi: 10.1371/journal.pone.0086806 PONE-D-13-36709 [pii]. 24466249 PMC3900635 · DOI
  56. [56]Poetsch V, Bennani-Baiti B, Neuhaus W, Muchitsch EM, Noe CR. Serum-derived immunoglobulins alter amyloid beta transport across a blood-brain barrier in vitro model. Pharmazie. 2010; 65(4): 267– 73. Epub 2010/05/04.. 20432623
  57. [57]Rodriguez-Gaztelumendi A, Alvehus M, Andersson T, Jacobsson SO. Comparison of the effects of nicotine upon the transcellular electrical resistance and sucrose permeability of human ECV304/rat C6 co-cultures and human CaCo(2) cells. Toxicol Lett. 2011; 207(1): 1– 6. Epub 2011/09/06. doi: 10.1016/j.toxlet.2011.08.014 S0378-4274(11)01500-1 [pii].. 21889975 · DOI
  58. [58]Untucht C, Rasch J, Fuchs E, Rohde M, Bergmann S, Steinert M. An optimized in vitro blood-brain barrier model reveals bidirectional transmigration of African trypanosome strains. Microbiology. 2011; 157(Pt 10): 2933– 41. Epub 2011/07/09. doi: 10.1099/mic.0.049106–0 mic.0.049106–0 [pii].. 21737496 · DOI
  59. [59]Wang GY, Wang N, Liao HN. Effects of Muscone on the Expression of P-gp, MMP-9 on Blood-Brain Barrier Model In Vitro. Cell Mol Neurobiol. in press. Epub 2015/05/16. 10.1007/s10571-015-0204-8. 25976179 PMC11488062 · DOI
  60. [60]Wang LF, Li X, Gao YB, Wang SM, Zhao L, Dong J, et al Activation of VEGF/Flk-1-ERK Pathway Induced Blood-Brain Barrier Injury After Microwave Exposure. Mol Neurobiol. 2014 Epub 2014/09/10. 10.1007/s12035-014-8848-9. 25195697 · DOI
  61. [61]Wang Q, Luo W, Zhang W, Liu M, Song H, Chen J. Involvement of DMT1 +IRE in the transport of lead in an in vitro BBB model. Toxicol In Vitro. 2011; 25(4): 991– 8. Epub 2009/11/17. doi: 10.1016/j.tiv.2009.11.006 S0887-2333(09)00335-X [pii].. 19913089 · DOI
  62. [62]Plattner VE, Germann B, Neuhaus W, Noe CR, Gabor F, Wirth M. Characterization of two blood-brain barrier mimicking cell lines: distribution of lectin-binding sites and perspectives for drug delivery. Int J Pharm. 2010; 387(1–2): 34– 41. Epub 2009/12/08. doi: 10.1016/j.ijpharm.2009.11.030 S0378-5173(09)00851-5 [pii].. 19963051 · DOI
  63. [63]Bennani-Baiti B, Bennani-Baiti IM. Gene symbol precision. Gene. 2012; 491(2): 103– 9. Epub 2011/10/25. S0378-1119(11)00562-2 [pii] 10.1016/j.gene.2011.09.035. 22019431 · DOI
  64. [64]Bustin SA, Benes V, Garson J, Hellemans J, Huggett J, Kubista M, et al The need for transparency and good practices in the qPCR literature. Nat Methods. 2013; 10(11): 1063– 7. Epub 2013/11/01. doi: 10.1038/nmeth.2697 nmeth.2697 [pii].. 24173381 · DOI · Paper page
  65. [65]Bustin SA, Beaulieu JF, Huggett J, Jaggi R, Kibenge FS, Olsvik PA, et al MIQE precis: Practical implementation of minimum standard guidelines for fluorescence-based quantitative real-time PCR experiments. BMC Mol Biol. 2010; 11: 74 Epub 2010/09/23. doi: 10.1186/1471-2199-11-74 1471-2199-11-74 [pii]. 20858237 PMC2955025 · DOI
  66. [66]Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002; 3(7):RESEARCH0034. Epub 2002/08/20. 12184808 PMC126239
  67. [67]Andersen CL, Jensen JL, Orntoft TF. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 2004; 64(15): 5245– 50.. 15289330
  68. [68]Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper—Excel-based tool using pair-wise correlations. Biotechnol Lett. 2004; 26(6): 509– 15.. 15127793
  69. [69]Bennani-Baiti IM, Cooper A, Lawlor ER, Kauer M, Ban J, Aryee DN, et al Intercohort gene expression co-analysis reveals chemokine receptors as prognostic indicators in Ewing's sarcoma. Clin Cancer Res. 2010; 16(14): 3769– 78. Epub 2010/06/08. doi: 10.1158/1078-0432.CCR-10-0558 1078-0432.CCR-10-0558 [pii]. 20525755 PMC2905506 · DOI
  70. [70]Bennani-Baiti IM, Aryee DN, Ban J, Machado I, Kauer M, Muhlbacher K, et al Notch signalling is off and is uncoupled from HES1 expression in Ewing's sarcoma. J Pathol. 2011; 225(3): 353– 63. Epub 2011/10/11. 10.1002/path.2966. 21984123 · DOI
  71. [71]Lukk M, Kapushesky M, Nikkila J, Parkinson H, Goncalves A, Huber W, et al A global map of human gene expression. Nat Biotechnol. 2010; 28(4): 322– 4. Epub 2010/04/10. doi: 10.1038/nbt0410-322 nbt0410-322 [pii]. 20379172 PMC2974261 · DOI
  72. [72]Chen G, Zhao L, Feng J, You G, Sun Q, Li P, et al Validation of reliable reference genes for real-time PCR in human umbilical vein endothelial cells on substrates with different stiffness. PLoS One. 2013; 8(6): e67360 Epub 2013/07/11. doi: 10.1371/journal.pone.0067360 PONE-D-13-02338 [pii]. 23840676 PMC3696109 · DOI
  73. [73]Wei R, Stewart EA, Amoaku WM. Suitability of endogenous reference genes for gene expression studies with human intraocular endothelial cells. BMC Res Notes. 2013; 6: 46 Epub 2013/02/06. doi: 10.1186/1756-0500-6-46 1756-0500-6-46 [pii]. 23379847 PMC3567942 · DOI
  74. [74]Zyzynska-Granica B, Koziak K. Identification of suitable reference genes for real-time PCR analysis of statin-treated human umbilical vein endothelial cells. PLoS One. 2012; 7(12): e51547 Epub 2012/12/20. doi: 10.1371/journal.pone.0051547 PONE-D-12-17286 [pii]. 23251572 PMC3519707 · DOI
  75. [75]Garcia-Vallejo JJ, Van Het Hof B, Robben J, Van Wijk JA, Van Die I, Joziasse DH, et al Approach for defining endogenous reference genes in gene expression experiments. Anal Biochem. 2004; 329(2): 293– 9.. 15158490
  76. [76]Pinhu L, Park JE, Yao W, Griffiths MJ. Reference gene selection for real-time polymerase chain reaction in human lung cells subjected to cyclic mechanical strain. Respirology. 2008; 13(7): 990– 9. 10.1111/j.1440-1843.2008.01396.x 18785913 · DOI
  77. [77]Liu PQ, Rebar EJ, Zhang L, Liu Q, Jamieson AC, Liang Y, et al Regulation of an endogenous locus using a panel of designed zinc finger proteins targeted to accessible chromatin regions. Activation of vascular endothelial growth factor A. J Biol Chem. 2001; 276(14): 11323– 34. Epub 2001/01/19. doi: 10.1074/jbc.M011172200 M011172200 [pii].. 11145970 · DOI
  78. [78]Bennani-Baiti IM, Asa SL, Song D, Iratni R, Liebhaber SA, Cooke NE. DNase I-hypersensitive sites I and II of the human growth hormone locus control region are a major developmental activator of somatotrope gene expression. Proc Natl Acad Sci U S A. 1998; 95(18): 10655– 60. Epub 1998/09/02. 9724759 PMC27950
  79. [79]Kwon MJ, Oh E, Lee S, Roh MR, Kim SE, Lee Y, et al Identification of novel reference genes using multiplatform expression data and their validation for quantitative gene expression analysis. PLoS One. 2009; 4(7): e6162 Epub 2009/07/09. 10.1371/journal.pone.0006162 19584937 PMC2703796 · DOI
  80. [80]Moskalenko S, Henry DO, Rosse C, Mirey G, Camonis JH, White MA. The exocyst is a Ral effector complex. Nat Cell Biol. 2002; 4(1): 66– 72. Epub 2001/12/12. doi: 10.1038/ncb728 ncb728 [pii].. 11740492 · DOI · Paper page
  81. [81]Sugihara K, Asano S, Tanaka K, Iwamatsu A, Okawa K, Ohta Y. The exocyst complex binds the small GTPase RalA to mediate filopodia formation. Nat Cell Biol. 2002; 4(1): 73– 8. Epub 2001/12/18. doi: 10.1038/ncb720 ncb720 [pii].. 11744922 · DOI · Paper page
  82. [82]Vandenbroucke E, Mehta D, Minshall R, Malik AB. Regulation of endothelial junctional permeability. Ann N Y Acad Sci. 2008; 1123: 134– 45. Epub 2008/04/01. 1123/1/134 [pii] 10.1196/annals.1420.016. 18375586 · DOI
  83. [83]Lee S, Wurtzel JG, Goldfinger LE. The RLIP76 N-terminus binds ARNO to regulate PI 3-kinase, Arf6 and Rac signaling, cell spreading and migration. Biochem Biophys Res Commun. 2014; 454(4): 560– 5. Epub 2014/12/03. S0006-291X(14)01934-2 [pii] 10.1016/j.bbrc.2014.10.114 25450693 PMC4254618 · DOI
  84. [84]Lee S, Goldfinger LE. RLIP76 regulates HIF-1 activity, VEGF expression and secretion in tumor cells, and secretome transactivation of endothelial cells. FASEB J. 2014; 28(9): 4158– 68. Epub 2014/06/15. doi: 10.1096/fj.14-255711 fj.14-255711 [pii]. 24928198 PMC4139904 · DOI
  85. [85]Lee S, Wurtzel JG, Singhal SS, Awasthi S, Goldfinger LE. RALBP1/RLIP76 depletion in mice suppresses tumor growth by inhibiting tumor neovascularization. Cancer Res. 2012; 72(20): 5165– 73. Epub 2012/08/21. doi: 10.1158/0008-5472.CAN-12-0468 0008-5472.CAN-12-0468 [pii]. 22902412 PMC3473090 · DOI
  86. [86]Awasthi S, Hallene KL, Fazio V, Singhal SS, Cucullo L, Awasthi YC, et al RLIP76, a non-ABC transporter, and drug resistance in epilepsy. BMC Neurosci. 2005; 6: 61 Epub 2005/09/29. 1471-2202-6-61 [pii] 10.1186/1471-2202-6-61 16188027 PMC1249579 · DOI
  87. [87]Awasthi S, Singhal SS, Awasthi YC, Martin B, Woo JH, Cunningham CC, et al RLIP76 and Cancer. Clin Cancer Res. 2008; 14(14): 4372– 7. Epub 2008/07/17. 14/14/4372 [pii] 10.1158/1078-0432.CCR-08-0145 18628450 PMC2919285 · DOI
  88. [88]Lim KH, Baines AT, Fiordalisi JJ, Shipitsin M, Feig LA, Cox AD, et al Activation of RalA is critical for Ras-induced tumorigenesis of human cells. Cancer Cell. 2005; 7(6): 533– 45. Epub 2005/06/14. S1535-6108(05)00157-1 [pii] 10.1016/j.ccr.2005.04.030. 15950903 · DOI · Paper page
  89. [89]Singhal SS, Sehrawat A, Sahu M, Singhal P, Vatsyayan R, Rao Lelsani PC, et al Rlip76 transports sunitinib and sorafenib and mediates drug resistance in kidney cancer. Int J Cancer. 2010; 126(6): 1327– 38. Epub 2009/07/25. 10.1002/ijc.24767 19626587 PMC3065777 · DOI
  90. [90]Singhal SS, Yadav S, Roth C, Singhal J. RLIP76: A novel glutathione-conjugate and multi-drug transporter. Biochem Pharmacol. 2009; 77(5): 761– 9. Epub 2008/11/06. S0006-2952(08)00715-6 [pii] 10.1016/j.bcp.2008.10.006 18983828 PMC2664079 · DOI
  91. [91]Singhal SS, Yadav S, Singhal J, Zajac E, Awasthi YC, Awasthi S. Depletion of RLIP76 sensitizes lung cancer cells to doxorubicin. Biochem Pharmacol. 2005; 70(3): 481– 8. Epub 2005/06/14. S0006-2952(05)00312-6 [pii] 10.1016/j.bcp.2005.05.005. 15950949 · DOI
  92. [92]Vatsyayan R, Chaudhary P, Lelsani PC, Singhal P, Awasthi YC, Awasthi S, et al Role of RLIP76 in doxorubicin resistance in lung cancer. Int J Oncol. 2009; 34(6): 1505– 11. Epub 2009/05/09. 19424567 PMC2916676
  93. [93]Vatsyayan R, Lelsani PC, Awasthi S, Singhal SS. RLIP76: a versatile transporter and an emerging target for cancer therapy. Biochem Pharmacol. 2010; 79(12): 1699– 705. Epub 2010/01/26. doi: 10.1016/j.bcp.2010.01.016 S0006-2952(10)00027-4 [pii]. 20097178 PMC2874070 · DOI
  94. [94]Bae YS, Chung W, Han K, Park KY, Kim H, Kim E, et al Down-regulation of RalBP1 expression reduces seizure threshold and synaptic inhibition in mice. Biochem Biophys Res Commun. 2013; 433(2): 175– 80. Epub 2013/03/15. doi: 10.1016/j.bbrc.2013.02.056 S0006-291X(13)00316-1 [pii].. 23485460 · DOI · Paper page
  95. [95]Birukov KG, Bochkov VN, Birukova AA, Kawkitinarong K, Rios A, Leitner A, et al Epoxycyclopentenone-containing oxidized phospholipids restore endothelial barrier function via Cdc42 and Rac. Circ Res. 2004; 95(9): 892– 901. Epub 2004/10/09. 01.RES.0000147310.18962.06 [pii] 10.1161/01.RES.0000147310.18962.06. 15472119 · DOI
  96. [96]Zhao D, Kuhnt-Moore S, Zeng H, Pan A, Wu JS, Simeonidis S, et al Substance P-stimulated interleukin-8 expression in human colonic epithelial cells involves Rho family small GTPases. Biochem J. 2002; 368(Pt 2): 665– 72. Epub 2002/08/10. doi: 10.1042/BJ20020950 BJ20020950 [pii]. 12169092 PMC1222994 · DOI
  97. [97]Zhao D, Kuhnt-Moore S, Zeng H, Wu JS, Moyer MP, Pothoulakis C. Neurotensin stimulates IL-8 expression in human colonic epithelial cells through Rho GTPase-mediated NF-kappa B pathways. Am J Physiol Cell Physiol. 2003; 284(6): C1397– 404. Epub 2003/02/14. doi: 10.1152/ajpcell.00328.2002 00328.2002 [pii].. 12584113 · DOI
  98. [98]Hunt C, Morimoto RI. Conserved features of eukaryotic hsp70 genes revealed by comparison with the nucleotide sequence of human hsp70. Proc Natl Acad Sci U S A. 1985; 82(19): 6455– 9. Epub 1985/10/01. 3931075 PMC390735
  99. [99]Duret L, Bucher P. Searching for regulatory elements in human noncoding sequences. Curr Opin Struct Biol. 1997; 7(3): 399– 406. Epub 1997/06/01. S0959-440X(97)80058-9 [pii].. 9204283
  100. [100]Tian H, Cao L, Tan Y, Williams S, Chen L, Matray T, et al Multiplex mRNA assay using electrophoretic tags for high-throughput gene expression analysis. Nucleic Acids Res. 2004; 32(16): e126 Epub 2004/09/10. doi: 10.1093/nar/gnh119 32/16/e126 [pii]. 15356286 PMC519123 · DOI
  101. [101]Ammar Z, Plazolles N, Baltz T, Coustou V. Identification of trans-sialidases as a common mediator of endothelial cell activation by African trypanosomes. PLoS Pathog. 2013; 9(10): e1003710 Epub 2013/10/17. doi: 10.1371/journal.ppat.1003710 PPATHOGENS-D-13-01000 [pii]. 24130501 PMC3795030 · DOI
  102. [102]Walker L, Sills GJ. Inflammation and epilepsy: the foundations for a new therapeutic approach in epilepsy? Epilepsy Curr. 2012; 12(1): 8– 12. Epub 2012/03/01. 10.5698/1535-7511-12.1.8 22368518 PMC3280476 · DOI
  103. [103]Gorter JA, van Vliet EA, Aronica E. Status epilepticus, blood-brain barrier disruption, inflammation, and epileptogenesis. Epilepsy Behav. 2015 Epub 2015/05/11. S1525-5050(15)00216-4 [pii] 10.1016/j.yebeh.2015.04.047. 25958228 · DOI · Paper page
  104. [105]Dupuis N, Auvin S. Inflammation and epilepsy in the developing brain: clinical and experimental evidence. CNS Neurosci Ther. 2015; 21(2): 141– 51. Epub 2015/01/22. 10.1111/cns.12371. 25604829 PMC6495285 · DOI
  105. [106]Tudur Smith C, Marson AG, Clough HE, Williamson PR. Carbamazepine versus phenytoin monotherapy for epilepsy. Cochrane Database Syst Rev. 2002;(2):CD001911. Epub 2002/06/22. CD001911 [pii] 10.1002/14651858.CD001911. 12076427 · DOI
  106. [107]Kaminski R, Kozicka M, Parada-turska J, Dziki M, Kleinrok Z, Turski WA, et al Effect of non-steroidal anti-inflammatory drugs on the anticonvulsive activity of valproate and diphenylhydantoin against maximal electroshock-induced seizures in mice. Pharmacol Res. 1998; 37(5): 375– 81. Epub 1998/06/27. S1043-6618(98)90309-7 [pii] 10.1006/phrs.1998.0309. 9642033 · DOI

Cited by

Sorted by citations

Authors
Bennani-Baiti, B., Toegel, S., Viernstein, H., Urban, E., Noe, C. R., & Bennani-Baiti, I. M.
Affiliations
  • Medical University of Vienna (AT)
  • University of Vienna (AT)
ORCID
Venue
PLOS ONE
Publisher
Public Library of Science (PLoS)
Published
2015-09-25
Volume
10
Issue
9
Pages
e0139101
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0139101
PMC
PMC4583384
OpenAlex
W2231106822
Cited by
20
References
1
Citations by year
2026: 3 · 2025: 1 · 2024: 1 · 2023: 1 · 2022: 3 · 2021: 1 · 2020: 2 · 2019: 1 · 2018: 1 · 2017: 3 · 2016: 2 · 2015: 1
FWCI
1.15
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Phaidra (Universität Wien) (submittedVersion, cc-by-nc-nd)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
Temple University
Topics
  • Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Molecular Biology Techniques and Applications
  • Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
Keywords
RLIP76, RALBP1, blood-brain barrier endothelial cells, inflammation, TNF-α, housekeeping genes, reference genes, MRP1, glutathione transporters, gene expression normalization, NF-κB
MeSH terms
Animals, Binding Sites, Blood-Brain Barrier, Gene Expression Regulation, Glutathione, Humans, Inflammation, Promoter Regions, Genetic, Software, Tumor Necrosis Factor-alpha, Biomarkers, NF-kappa B, ATP-Binding Cassette Transporters, Genes, Essential, GTPase-Activating Proteins, Endothelial Cells, Mice, Rats, Genetic Association Studies

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