Impairment of tight junctions and glucose transport in endothelial cells of human cerebral cavernous malformations

Journal of Neuropathology and Experimental Neurology

Volumn 70, Issue 6, 2011, Pages 417-429

  Schneider, Hannah ^a   Errede, Mariella ^b   Ulrich, Nils H ^a   Virgintino, Daniela ^b   Frei, Karl ^a   Bertalanffy, Helmut ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF BARI MEDICAL SCHOOL   (Italy)

Author keywords

Cerebral cavernous malformation; Claudin 5; GLUT 1; Occludin; Tight junctions; ZO 1

Indexed keywords

CLAUDIN 5; GLUCOSE TRANSPORTER 1; OCCLUDIN; PROTEIN ZO1;

ADULT; ARTICLE; BLEEDING; CAVERNOUS HEMANGIOMA; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GLUCOSE TRANSPORT; HEMIPARESIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE MICROSCOPY; MALE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEIZURE; TEMPORAL LOBECTOMY; TIGHT JUNCTION;

ADOLESCENT; ADULT; CENTRAL NERVOUS SYSTEM VASCULAR MALFORMATIONS; CHILD; DOWN-REGULATION; ENDOTHELIAL CELLS; FEMALE; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; HUMANS; INTERCELLULAR JUNCTIONS; MALE; MEMBRANE PROTEINS; MIDDLE AGED; PHOSPHOPROTEINS; RNA, MESSENGER; TIGHT JUNCTIONS; YOUNG ADULT;

EID: 79957515304     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0b013e31821bc40e     Document Type: Article

References (61)

1. Al-Shahi R, Bhattacharya JJ, Currie DG, et al. Prospective, population-based detection of intracranial vascular malformations in adults: The Scottish Intracranial Vascular Malformation Study (SIVMS). Stroke 2003;34:1163-69 (Pubitemid 36547507)
2. Del Curling O Jr, Kelly DL Jr, Elster AD, et al. An analysis of the natural history of cavernous angiomas. J Neurosurg 1991;75:702-8
3. Rigamonti D, Hadley MN, Drayer BP, et al. Cerebral cavernous malformations. Incidence and familial occurrence. N Engl J Med 1988;319: 343-47
4. Leblanc GG, Golanov E, Awad IA, et al. Biology of vascular malformations of the brain. Stroke 2009;40:e694-e702
5. Rothbart D, Awad IA, Lee J, et al. Expression of angiogenic factors and structural proteins in central nervous system vascular malformations. Neurosurgery 1996;38:915-24; discussion 24-25
6. Kilic T, Pamir MN, Kullu S, et al. Expression of structural proteins and angiogenic factors in cerebrovascular anomalies. Neurosurgery 2000;46: 1179-91; discussion 91-92
7. Wustehube J, Bartol A, Liebler SS, et al. From the cover: Cerebral cavernous malformation protein CCM1 inhibits sprouting angiogenesis by activating DELTA-NOTCH signaling. Proc Natl Acad Sci USA 2010; 107:12640-45
8. Mindea SA, Yang BP, Shenkar R, et al. Cerebral cavernous malformations: Clinical insights from genetic studies. Neurosurg Focus 2006:21;e1
9. Labauge P, Denier C, Bergametti F, et al. Genetics of cavernous angio-mas. Lancet Neurol 2007;6:237-44
10. Gault J, Shenkar R, Recksiek P, et al. Biallelic somatic and germ line CCM1 truncating mutations in a cerebral cavernous malformation lesion. Stroke 2005;36:872-74
11. Akers AL, Johnson E, Steinberg GK, et al. Biallelic somatic and germ line mutations in cerebral cavernous malformations (CCMs): Evidence for a two-hit mechanism of CCM pathogenesis. Hum Mol Genet 2009; 18:919-30
12. Shenkar R, Venkatasubramanian PN, Wyrwicz AM, et al. Advanced magnetic resonance imaging of cerebral cavernous malformations: Part II. Imaging of lesions in murine models. Neurosurgery 2008;63:790-98; discussion 7-8
13. Plummer NW, Gallione CJ, Srinivasan S, et al. Loss of p53 sensitizes mice with a mutation in Ccm1 (KRIT1) to development of cerebral vascular malformations. Am J Pathol 2004;165:1509-18 (Pubitemid 39435151)
14. Kleaveland B, Zheng X, Liu JJ, et al. Regulation of cardiovascular development and integrity by the heart of glassYcerebral cavernous malformation protein pathway. Nat Med 2009;15:169-76
15. Whitehead KJ, Chan AC, Navankasattusas S, et al. The cerebral cavernous malformation signaling pathway promotes vascular integrity via Rho GTPases. Nat Med 2009;15:177-84
16. Zhu Y, Wloch A, Wu Q, et al. Involvement of PTEN promoter methyl-ation in cerebral cavernous malformations. Stroke 2009;40:820-26
17. Stockton RA, Shenkar R, Awad IA, et al. Cerebral cavernous malformations proteins inhibit Rho kinase to stabilize vascular integrity. J Exp Med 2010:207:881-96
18. Zhao Y, Tan YZ, Zhou LF, et al. Morphological observation and in vitro angiogenesis assay of endothelial cells isolated from human cerebral cavernous malformations. Stroke 2007;38:1313-19 (Pubitemid 351664290)
19. Wong JH, Awad IA, Kim JH. Ultrastructural pathological features of cerebrovascular malformations: A preliminary report. Neurosurgery 2000; 46:1454-59 (Pubitemid 32037675)
20. Clatterbuck RE, Eberhart CG, Crain BJ, et al. Ultrastructural and immu-nocytochemical evidence that an incompetent blood-brain barrier is related to the pathophysiology of cavernous malformations. J Neurol Neurosurg Psychiatry 2001;71:188-92 (Pubitemid 32675143)
21. Glading A, Han J, Stockton RA, et al. KRIT-1/CCM1 is a Rap1 effector that regulates endothelial cell-cell junctions. J Cell Biol 2007;179: 247-54 (Pubitemid 350004889)
22. Lischper M, Beuck S, Thanabalasundaram G, et al. Metalloproteinase mediated occludin cleavage in the cerebral microcapillary endothelium under pathological conditions. Brain Res 2010;1326:114-27
23. Cornford EM, Hyman S. Localization of brain endothelial luminal and abluminal transporters with immunogold electron microscopy. NeuroRx 2005;2:27-43 (Pubitemid 40128024)
24. Rosenberg GA, Yang Y. Vasogenic edema due to tight junction disruption by matrix metalloproteinases in cerebral ischemia. Neurosurg Focus 2007;22:E4
25. Anderson JM, Van Itallie CM. Tight junctions and the molecular basis for regulation of paracellular permeability. Am J Physiol 1995;269:G467YG75
26. Tsukita S, Furuse M. Occludin and claudins in tight-junction strands: Leading or supporting players? Trends Cell Biol 1999;9:268-73 (Pubitemid 29305516)
27. Furuse M. Molecular basis of the core structure of tight junctions. Cold Spring Harb Perspect Biol 2010;2:a002907
28. Fanning AS, Jameson BJ, Jesaitis LA, et al. The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J Biol Chem 1998;273:29745-53 (Pubitemid 28509986)
29. Feldman GJ, Mullin JM, Ryan MP. Occludin: Structure, function and regulation. Adv Drug Deliv Rev 2005;57:883-917 (Pubitemid 40488109)
30. McCarthy KM, Skare IB, Stankewich MC, et al. Occludin is a functional component of the tight junction. J Cell Sci 1996;109:2287-98 (Pubitemid 26325491)
31. Dobrogowska DH, Vorbrodt AW. Quantitative immunocytochemical study of blood-brain barrier glucose transporter (GLUT-1) in four regions of mouse brain. J Histochem Cytochem 1999;47:1021-30
32. Gerhart DZ, LeVasseur RJ, Broderius MA, et al. Glucose transporter localization in brain using light and electron immunocytochemistry. J Neurosci Res 1989;22:464-72 (Pubitemid 19145630)
33. Lippoldt A, Kniesel U, Liebner S, et al. Structural alterations of tight junctions are associated with loss of polarity in stroke-prone spontaneously hypertensive rat blood-brain barrier endothelial cells. Brain Res 2000;885:251-61
34. Birnbaum MJ, Haspel HC, Rosen OM. Cloning and characterization of a cDNA encoding the rat brain glucose-transporter protein. Proc Natl Acad Sci USA 1986;83:5784-88 (Pubitemid 16000596)
35. Fukumoto H, Seino S, Imura H, et al. Sequence, tissue distribution, and chromosomal localization of mRNA encoding a human glucose transporter-like protein. Proc Natl Acad Sci USA 1988;85:5434-38
36. Pardridge WM, Boado RJ, Farrell CR. Brain-type glucose transporter (GLUT-1) is selectively localized to the blood-brain barrier. Studies with quantitative Western blotting and in situ hybridization. J Biol Chem 1990; 265:18035-40
37. Yadla S, Jabbour PM, Shenkar R, et al. Cerebral cavernous malformations as a disease of vascular permeability: From bench to bedside with caution. Neurosurg Focus 2010;29:E4
38. Ishihara H, Kubota H, Lindberg RL, et al. Endothelial cell barrier impairment induced by glioblastomas and transforming growth factor beta2 involves matrix metalloproteinases and tight junction proteins. J Neuro-pathol Exp Neurol 2008;67:435-48 (Pubitemid 351653535)
39. Al-Shahi Salman R, Berg MJ, Morrison L, et al. Hemorrhage from cavernous malformations of the brain: Definition and reporting standards. Angioma Alliance Scientific Advisory Board. Stroke 2008;39:3222-30
40. Kivelev J, Niemela M, Kivisaari R, et al. Long-term outcome of patients with multiple cerebral cavernous malformations. Neurosurgery 2009;65: 450-55; discussion 5
41. van Swieten JC, Koudstaal PJ, Visser MC, et al. Interobserver agreement for the assessment of handicap in stroke patients. Stroke 1988;19:604-7
42. Di Iorio E, Barbaro V, Ferrari S, et al. Q-FIHC: Quantification of fluorescence immunohistochemistry to analyze p63 isoforms and cell cycle phases in human limbal stem cells. Microsc Res Tech 2006;69:983-91 (Pubitemid 44888242)
43. Nagy Z, Peters H, Huttner I. Fracture faces of cell junctions in cerebral endothelium during normal and hyperosmotic conditions. Lab Invest 1984;50:313-22 (Pubitemid 14154642)
44. Furuse M, Hirase T, Itoh M, et al. Occludin: A novel integral membrane protein localizing at tight junctions. J Cell Biol 1993;123:1777-88 (Pubitemid 24012933)
45. Nitta T, Hata M, Gotoh S, et al. Size-selective loosening of the blood-brain barrier in claudin-5Ydeficient mice. J Cell Biol 2003;161: 653-60 (Pubitemid 36578587)
46. Ohtsuki S, Sato S, Yamaguchi H, et al. Exogenous expression of claudin-5 induces barrier properties in cultured rat brain capillary endothelial cells. J Cell Physiol 2007:210;81-86 (Pubitemid 44904703)
47. Harhaj NS, Antonetti DA. Regulation of tight junctions and loss of barrier function in pathophysiology. Int J Biochem Cell Biol 2004;36: 1206-37 (Pubitemid 38519069)
48. Hawkins BT, Davis TP. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 2005;57:173-85 (Pubitemid 41043883)
49. Bolton SJ, Anthony DC, Perry VH. Loss of the tight junction proteins occludin and zonula occludens-1 from cerebral vascular endothelium during neutrophil-induced blood-brain barrier breakdown in vivo. Neuro-science 1998;86:1245-57 (Pubitemid 28318549)
50. Citi S. The molecular organization of tight junctions. J Cell Biol 1993; 121:485-89 (Pubitemid 23131261)
51. Vorbrodt AW, Dobrogowska DH, Tarnawski M. Immunogold study of interendothelial junction-associated and glucose transporter proteins during postnatal maturation of the mouse blood-brain barrier. J Neuro-cytol 2001;30:705-16
52. Forster C. Tight junctions and the modulation of barrier function in disease. Histochem Cell Biol 2008;130:55-70
53. Argaw AT, Gurfein BT, Zhang Y, et al. VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown. Proc Natl Acad Sci USA 2009;106:1977-82
54. Kebir H, KreymborgK, IferganI, et al. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat Med 2007;13:1173-75 (Pubitemid 47530640)
55. Sakakibara A, Furuse M, Saitou M, et al. Possible involvement of phos-phorylation of occludin in tight junction formation. J Cell Biol 1997;137: 1393-401 (Pubitemid 27265950)
56. Wachtel M, Bolliger MF, Ishihara H, et al. Down-regulation of occludin expression in astrocytes by tumor necrosis factor (TNF) is mediated via TNF type-1 receptor and nuclear factor-kappaB activation. J Neurochem 2001;78:155-62 (Pubitemid 32622597)
57. Tu J, Stoodley MA, Morgan MK, et al. Ultrastructural characteristics of hemorrhagic, nonhemorrhagic, and recurrent cavernous malformations. J Neurosurg 2005;103:903-9 (Pubitemid 43194585)
58. Fujimura M, Watanabe M, Shimizu H, et al. Expression of matrix metalloproteinases (MMPs) and tissue inhibitor of metalloproteinase (TIMP) in cerebral cavernous malformations: Immunohistochemical analysis of MMP-2, -9 and TIMP-2. Acta Neurochir (Wien) 2007;149: 179-83; discussion 83 (Pubitemid 46208901)
59. Hou WK, Xian YX, Zhang L, et al. Influence of blood glucose on the expression of glucose transporter proteins 1 and 3 in the brain of diabetic rats. Chin Med J (Engl) 2007;120:1704-9 (Pubitemid 47603961)
60. Dejana E, Corada M, Lampugnani MG. Endothelial cell-to-cell junctions. FASEB J 1995;9:910-18
61. Birukova AA, Zebda N, Fu P, et al. Association between adherens junctions and tight junctions via Rap1 promotes barrier protective effects of oxidized phospholipids. J Cell Physiol 2011;226:2052-62