Mechanisms of vascular stability and the relationship to human disease

Current Opinion in Hematology

Volumn 17, Issue 3, 2010, Pages 237-244

  Smith, Matthew C P ^a   Li, Dean Y ^a,b,c   Whitehead, Kevin J ^a,b  

^a Program in Molecular Medicine   (United States)

^b Department of Oncological Sciences ^*  (United States)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Cavernous malformation arteriovenous malformation; Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy; Cerebral cavernous malformation; Cutaneomucosal venous malformation; Vascular stability

Indexed keywords

GUANOSINE TRIPHOSPHATASE; NOTCH RECEPTOR;

ARTERIOVENOUS MALFORMATION; AUTOSOMAL DOMINANT DISORDER; BRAIN INFARCTION; CONGENITAL BLOOD VESSEL MALFORMATION; GENETIC ASSOCIATION; HUMAN; LEUKOENCEPHALOPATHY; PRIORITY JOURNAL; REVIEW;

ANIMALS; BLOOD VESSELS; HUMANS; VASCULAR DISEASES;

EID: 77951497811     PISSN: 10656251     EISSN: 15317048     Source Type: Journal    
DOI: 10.1097/MOH.0b013e3283386750     Document Type: Review

References (64)

1. Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. Physiol Rev 2006; 86:279-367.
2. Vestweber D, Winderlich M, Cagna G, Nottebaum AF. Cell adhesion dynamics at endothelial junctions: VE-cadherin as a major player. Trends Cell Biol 2009; 19:8-15.
3. Wallez Y, Huber P. Endothelial adherens and tight junctions in vascular homeostasis, inflammation and angiogenesis. Biochim Biophys Acta 2008; 1778:794-809.
4. Lindahl P, Johansson BR, Leveen P, Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 1997; 277:242-245.
5. Nagy JA, Benjamin L, Zeng H, et al. Vascular permeability, vascular hyper-permeability and angiogenesis. Angiogenesis 2008; 11:109-119.
6. Vikkula M, Boon LM, Carraway KL 3rd, et al. Vascular dysmorphogenesis caused by an activating mutation in the receptor tyrosine kinase TIE2. Cell 1996; 87:1181-1190.
7. Goldstein JL, Brown MS. Molecular medicine. The cholesterol quartet. Science 2001; 292:1310-1312.
8. Brouillard P, Vikkula M. Vascular malformations: localized defects in vascular morphogenesis. Clin Genet 2003; 63:340-351.
9. Wouters V, Limaye N, Uebelhoer M, et al. Hereditary cutaneomucosal venous malformations are caused by TIE2 mutations with widely variable hyper-phosphorylating effects. Eur J Hum Genet 2009 [Epub ahead of print].
10. Limaye N, Boon LM, Vikkula M. From germline towards somatic mutations in the pathophysiology of vascular anomalies. Hum Mol Genet 2009; 18 (R1):R65-R74.
11. Limaye N, Wouters V, Uebelhoer M, et al. Somatic mutations in angiopoietin receptor gene TEK cause solitary and multiple sporadic venous malformations. Nat Genet 2009; 41:118-124.
12. Hu HT, Huang YH, Chang YA, et al. Tie2-R849W mutant in venous malformations chronically activates afunctional STAT1 to modulate gene expression. J Invest Dermatol 2008; 128:2325-2333.
13. Benjamin LE, Golijanin D, Itin A, et al. Selective ablation of immature blood vessels in established human tumors follows vascular endothelial growth factor withdrawal. J Clin Invest 1999; 103:159-165.
14. Battle TE, Lynch RA, Frank DA. Signal transducer and activator of transcription 1 activation in endothelial cells is a negative regulator of angiogenesis. Cancer Res 2006; 66:3649-3657.
15. Karnoub AE, Weinberg RA. Ras oncogenes: split personalities. Nat Rev 2008; 9:517-531.
16. Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature 2002; 420:629-635.
17. Jaffe AB, Hall A, Schmidt A. Association of CNK1 with Rho guanine nucleotide exchange factors controls signaling specificity downstream of Rho. Curr Biol 2005; 15:405-412.
18. Eerola I, Boon LM, Mulliken JB, et al. Capillary malformation- arteriovenous malformation, a new clinical and genetic disorder caused by RASA1 mutations. Am J Hum Genet 2003; 73:1240-1249.
19. Thiex R, Mulliken JB, Revencu N, et al. A novel association between RASA1 mutations and spinal arteriovenous anomalies. AJNR Am J Neuradiol 2009 [Epub ahead of print].
20. Boon LM, Mulliken JB, Vikkula M. RASA1: variable phenotype with capillary and arteriovenous malformations. Curr Opin Genet Dev 2005; 15:265-269.
21. Settleman J, Albright CF, Foster LC, Weinberg RA. Association between GTPase activators for Rho and Ras families. Nature 1992; 359:153-154.
22. Settleman J, Narasimhan V, Foster LC, Weinberg RA. Molecular cloning of cDNAs encoding the GAP-associated protein p190: implications for a signaling pathway from ras to the nucleus. Cell 1992; 69:539-549.
23. Frech M, John J, Pizon V, et al. Inhibition of GTPase activating protein stimulation of Ras-p21 GTPase by the Krev-1 gene product. Science 1990; 249:169-171.
24. Serebriiskii I, Estojak J, Sonoda G, et al. Association of Krev-1/rap1a with Krit1, a novel ankyrin repeat-containing protein encoded by a gene mapping to 7q21-22. Oncogene 1997; 15:1043-1049.
25. Laberge-le Couteulx S, Jung HH, Labauge P, et al. Truncating mutations in CCM1, encoding KRIT1, cause hereditary cavernous angiomas. Nat Genet 1999; 23:189-193.
26. Sahoo T, Johnson EW, Thomas JW, et al. Mutations in the gene encoding KRIT1, a Krev-1/rap1a binding protein, cause cerebral cavernous malformations (CCM1). Hum Mol Genet 1999; 8:2325-2333.
27. Labauge P, Brunereau L, Levy C, et al. The natural history of familial cerebral cavernomas: a retrospective MRI study of 40 patients. Neuroradiology 2000; 42:327-332.
28. Clatterbuck RE, Eberhart CG, Crain BJ, Rigamonti D. Ultrastructural and immunocytochemical evidence that an incompetent blood-brain barrier is related to the pathophysiology of cavernous malformations. J Neurol Neuro-surg Psychiatry 2001; 71:188-192.
29. Vernooij MW, Ikram MA, Tanghe HL, et al. Incidental findings on brain MRI in the general population. N Engl J Med 2007; 357:1821-1828.
30. Otten P, Pizzolato GP, Rilliet B, Berney J. One hundred and thirty-one cases of cavernous angioma (cavernomas) of the CNS, discovered by retrospective analysis of 24,535 autopsies. Neurochirurgie 1989; 35:82-83; 128-131.
31. Liquori CL, Berg MJ, Siegel AM, et al. Mutations in a gene encoding a novel protein containing a phosphotyrosine-binding domain cause type 2 cerebral cavernous malformations. Am J Hum Genet 2003; 73:1459-1464.
32. Denier C, Goutagny S, Labauge P, et al. Mutations within the MGC4607 gene cause cerebral cavernous malformations. Am J Hum Genet 2004; 74:326-337. (Pubitemid 38168620)
33. Bergametti F, Denier C, Labauge P, et al. Mutations within the programmed cell death 10 gene cause cerebral cavernous malformations. Am J Hum Genet 2005; 76:42-51.
34. Riant F, Bergametti F, Ayrignac X, et al. Recent insights into cerebral cavernous malformations: the molecular genetics of CCM. FEBS J 2010; 277:1070-1075.
35. Faurobert E, Albiges-Rizo C. Recent insights into cerebral cavernous malformations: a complex jigsaw puzzle under construction. FEBS J 2010;277:1084-1096.
36. Glading A, Han J, Stockton RA, Ginsberg MH. KRIT-1/CCM1 is a Rap1 effector that regulates endothelial cell-cell junctions. J Cell Biol 2007; 179:247-254.
37. Glading AJ, Ginsberg MH. Rap1 and its effector KRIT1/CCM1 regulate beta-catenin signaling. Dis Models Mech 2010; 3:73-83.
38. Gore AV, Lampugnani MG, Dye L, et al. Combinatorial interaction between CCM pathway genes precipitates hemorrhagic stroke. Dis Models Mech 2008; 1 (4-5):275-281.
39. UhlikMT, Abell AN, Johnson NL, et al. Rac-MEKK3-MKK3 scaffolding for p38 MAPK activation during hyperosmotic shock. Nat Cell Biol 2003; 5:1104-1110.
40. Whitehead KJ, Chan AC, Navankasattusas S, et al. The cerebral cavernous malformation signaling pathway promotes vascular integrity via Rho GTPases. Nat Med 2009; 15:177-184.
41. Gault J, Shenkar R, Recksiek P, Awad IA. Biallelic somatic and germ line CCM1 truncating mutations in a cerebral cavernous malformation lesion. Stroke 2005; 36:872-874.
42. Pagenstecher A, Stahl S, Sure U, Felbor U. A two-hit mechanism causes cerebral cavernous malformations: complete inactivation of CCM1, CCM2 or CCM3 in affected endothelial cells. Hum Mol Genet 2009; 18:911-918.
43. Akers AL, Johnson E, Steinberg GK, et al. Biallelic somatic and germline mutations in cerebral cavernous malformations (CCMs): evidence for a two-hit mechanism of CCM pathogenesis. Hum Mol Genet 2009; 18:919-930.
44. Gault J, Awad IA, Recksiek P, et al. Cerebral cavernous malformations: somatic mutations in vascular endothelial cells. Neurosurgery 2009; 65:138-144; discussion 144-145.
45. Whitehead KJ, Plummer NW, Adams JA, et al. Ccm1 is required for arterial morphogenesis: implications for the etiology of human cavernous malformations. Development 2004; 131:1437-1448.
46. Kleaveland B, Zheng X, Liu JJ, et al. Regulation of cardiovascular development and integrity by the heart of glass-cerebral cavernous malformation protein pathway. Nat Med 2009; 15:169-176.
47. Boulday G, Blecon A, Petit N, et al. Tissue-specific conditional CCM2 knockout mice establish the essential role of endothelial CCM2 in angiogen-esis: implications for human cerebral cavernous malformations. Dis Models Mech 2009; 2:168-177.
48. 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; 63:790-797; discussion 797-798.
49. Hogan BM, Bussmann J, Wolburg H, Schulte-Merker S. ccm1 cell autonomously regulates endothelial cellular morphogenesis and vascular tubulogen-esis in zebrafish. Hum Mol Genet 2008; 17:2424-2432.
50. Seker A, Pricola KL, Guclu B, et al. CCM2 expression parallels that of CCM1. Stroke 2006; 37:518-523.
51. Plummer NW, Squire TL, Srinivasan S, et al. Neuronal expression of theCcm2 gene in a new mouse model of cerebral cavernous malformations. Mamm Genome 2006; 17:119-128.
52. Petit N, Blecon A, Denier C, Tournier-Lasserve E. Patterns of expression of the three cerebral cavernous malformation (CCM) genes during embryonic and postnatal brain development. Gene Expr Patterns 2006; 6:495-503.
53. Cave-Riant F, DenierC, Labauge P, et al. Spectrum and expression analysis of KRIT1 mutations in 121 consecutive and unrelated patients with cerebral cavernous malformations. Eur J Hum Genet 2002; 10:733-740.
54. Harel L, Costa B, Tcherpakov M, et al. CCM2 mediates death signaling by the TrkA receptor tyrosine kinase. Neuron 2009; 63:585-591.
55. Gale NW, Dominguez MG, Noguera I, et al. Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development. Proc Natl Acad Sci USA 2004; 101:15949-15954.
56. Limbourg FP, Takeshita K, Radtke F, et al. Essential role of endothelial Notch1 in angiogenesis. Circulation 2005; 111:1826-1832.
57. Ehebauer M, Hayward P, Martinez-Arias A. Notch signaling pathway. Sci STKE 2006; 2006:cm7.
58. Lai EC. Notch signaling: control of cell communication and cell fate. Development 2004; 131:965-973.
59. HellstromM,PhngLK, HofmannJJ,et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 2007; 445:776-780.
60. Benedito R, Roca C, Sorensen I, et al. The notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis. Cell 2009; 137:1124-1135.
61. Chabriat H, Joutel A, Dichgans M, et al. CADASIL. Lancet Neurology 2009; 8:643-653.
62. Joutel A, Monet-Lepretre M, Gosele C, et al. Cerebrovascular dysfunction and microcirculation rarefaction precede white matter lesions in a mouse genetic model of cerebral ischemic small vessel disease. J Clin Invest 2010; 120;433-445.
63. Domenga V, Fardoux P, Lacombe P, et al. Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev 2004; 18:2730-2735.
64. Belin de Chantemele EJ, Retailleau K, Pinaud F, et al. Notch3 is a major regulator of vascular tone in cerebral and tail resistance arteries. Arterioscler Thromb Vasc Biol 2008; 28:2216-2224.