Vascular endothelial hyperpermeability induces the clinical symptoms of Clarkson disease (the systemic capillary leak syndrome)

Blood

Volumn 119, Issue 18, 2012, Pages 4321-4332

  Xie, Zhihui ^a   Ghosh, Chandra C ^b   Patel, Roshni ^a   Iwaki, Shoko ^a   Gaskins, Donna ^a   Nelson, Celeste ^a   Jones, Nina ^a   Greipp, Philip R ^c   Parikh, Samir M ^b   Druey, Kirk M ^a,d  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Mayo Clinic   (United States)

^d NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ANGIOPOIETIN 2; BEVACIZUMAB; IMMUNOGLOBULIN; TERBUTALINE; THEOPHYLLINE; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN;

ADULT; APOPTOSIS; ARTICLE; BLOOD VESSEL PERMEABILITY; CAPILLARY LEAK SYNDROME; CLINICAL ARTICLE; CLINICAL FEATURE; FEMALE; HUMAN; MALE; PATHOGENESIS; PRIORITY JOURNAL; REMISSION; STRESS FIBER; VASCULAR ENDOTHELIUM;

EID: 84860797968     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-08-375816     Document Type: Article

References (58)

1. Clarkson B, Thompson D, Horwith M, Luckey EH. Cyclical edema and shock due to increased capillary permeability. Am J Med. 1960;29:193-216.
2. Dhir V, Arya V, Malav IC, Suryanarayanan BS, Gupta R, Dey AB. Idiopathic systemic capillary leak syndrome (SCLS): case report and systematic review of cases reported in the last 16 years. Intern Med. 2007;46(12):899-904. (Pubitemid 47261675)
3. Amoura Z, Papo T, Ninet J, et al. Systemic capillary leak syndrome: report on 13 patients with special focus on course and treatment. Am J Med. 1997;103(6):514-519. (Pubitemid 28018654)
4. Gousseff M, Arnaud L, Lambert M, et al. The systemic capillary leak syndrome: a case series of 28 patientsfrom a European registry. Ann Intern Med. 2011;154(7):464-471.
5. Druey KM, Greipp PR. Narrative review: the systemic capillary leak syndrome. Ann Intern Med. 2010;153(2):90-98.
6. Kapoor P, Greipp PT, Schaefer EW, et al. Idiopathic systemic capillary leak syndrome (Clarkson's disease): the Mayo clinic experience. Mayo Clin Proc. 2010;85(10):905-912.
7. Kawabe S, Saeki T, Yamazaki H, Nagai M, Aoyagi R, Miyamura S. Systemic capillary leak syndrome. Intern Med. 2002;41(3):211-215. (Pubitemid 34285440)
8. Gousseff M, Amoura Z. Idiopathic capillary leak syndrome [in French]. Rev Med Interne. 2009;30(9):754-768.
9. Lambert M, Launay D, Hachulla E, et al. High-dose intravenous immunoglobulins dramatically reverse systemic capillary leak syndrome. Crit Care Med. 2008;36(7):2184-2187.
10. Lesterhuis WJ, Rennings AJ, Leenders WP, et al. Vascular endothelial growth factor in systemic capillary leak syndrome. Am J Med. 2009;122(6):e5-e7.
11. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science. 1983;219(4587):983-985.
12. Thurston G, Suri C, Smith K, et al. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science. 1999;286(5449):2511- 2514.
13. Michels S, Rosenfeld PJ, Puliafito CA, Marcus EN, Venkatraman AS. Systemic bevacizumab (Avastin) therapy for neovascular age-related macular degeneration twelve-week results of an uncontrolled open-label clinical study. Ophthalmology. 2005;112(6):1035-1047. (Pubitemid 40797459)
14. David S, Ghosh CC, Kuempers P, et al. Effects of a synthetic PEG-ylated Tie-2 agonist peptide on endotoxemic lung injury and mortality. Am J Physiol Lung Cell Mol Physiol. 2011;300(6):L851-L862.
15. Assaly R, Olson D, Hammersley J, et al. Initial evidence of endothelial cell apoptosis as a mechanism of systemic capillary leak syndrome. Chest. 2001;120(4):1301-1308. (Pubitemid 32960108)
16. Thuret G, Chiquet C, Herrag S, et al. Mechanisms of staurosporine induced apoptosis in a human corneal endothelial cell line. Br J Ophthalmol. 2003;87(3):346-352. (Pubitemid 36307913)
17. Dudek AZ, Bodempudi V, Welsh BW, et al. Systemic inhibition of tumour angiogenesis by endothelial cell-based gene therapy. Br J Cancer. 2007;97(4):513-522. (Pubitemid 47258448)
18. Dejana E, Tournier-Lasserve E, Weinstein BM. The control of vascular integrity by endothelial cell junctions: molecular basis and pathological implications. Dev Cell. 2009;16(2):209-221.
19. Shay-Salit A, Shushy M, Wolfovitz E, et al. VEGF receptor 2 and the adherens junction as a mechanical transducer in vascular endothelial cells. Proc Natl Acad Sci U S A. 2002;99(14):9462-9467. (Pubitemid 34764636)
20. Gavrilovskaya IN, Gorbunova EE, Mackow NA, Mackow ER. Hantaviruses direct endothelial cell permeability by sensitizing cells to the vascular permeability factor VEGF, while angiopoietin 1 and sphingosine 1-phosphate inhibit hantavirus-directed permeability. J Virol. 2008;82(12):5797-5806. (Pubitemid 351822254)
21. Shrivastava-Ranjan P, Rollin PE, Spiropoulou CF. Andes virus disrupts the endothelial cell barrier by induction of vascular endothelial growth factor and downregulation of VE-cadherin. J Virol. 2010;84(21):11227-11234.
22. Kinoshita Y, Kasaoka S, Fujita M, et al. Synchronized changes in serum vascular endothelial growth factor during the clinical course of chronic systemic capillary leak syndrome. Intern Med. 2010;49(8):791-794.
23. Dowden AM, Rullo OJ, Aziz N, Fasano MB, Chatila T, Ballas ZK. Idiopathic systemic capillary leak syndrome: Novel therapy for acute attacks. J Allergy Clin Immunol. 2009;124(5):1111-1113.
24. Nagao Y, Harada H, Yamanaka H, Fukuda K. Possible mediators for systemic capillary leak syndrome. Am J Med. 2011;124(1):e7-e9.
25. Kuhnert F, Tam BY, Sennino B, et al. Soluble receptor-mediated selective inhibition of VEGFR and PDGFRbeta signaling during physiologic and tumor angiogenesis. Proc Natl Acad Sci U S A. 2008;105(29):10185-10190.
26. Findley CM, Cudmore MJ, Ahmed A, Kontos CD. VEGF induces Tie2 shedding via a phosphoinositide 3-kinase/Akt dependent pathway to modulate Tie2 signaling. Arterioscler Thromb Vasc Biol. 2007;27(12):2619-2626. (Pubitemid 350158914)
27. Atkinson JP, Waldmann TA, Stein SF, et al. Systemic capillary leak syndrome and monoclonal IgG gammopathy; studies in a sixth patient and a review of the literature. Medicine (Baltimore). 1977;56(3):225-239. (Pubitemid 8111455)
28. Fardet L, Kerob D, Rybojad M, et al. Idiopathic systemic capillary leak syndrome: cutaneous involvement can be misleading. Dermatology. 2004;209(4):291-295. (Pubitemid 39482619)
29. Cicardi M, Berti E, Caputo V, Radice F, Gardinali M, Agostoni A. Idiopathic capillary leak syndrome: evidence of CD8-positive lymphocytes surrounding damaged endothelial cells. J Allergy Clin Immunol. 1997;99(3):417-419. (Pubitemid 27123923)
30. Fellows IW, Powell RJ, Toghill PJ, Williams TJ, Cohen GF. Epoprostenol in systemic capillary leak syndrome. Lancet. 1988;2(8620):1143.
31. Weinbren I. Spontaneous periodic oedema. A new syndrome. Lancet. 1963;2(7307):544-546.
32. Kao NL, Richmond GW, Luskin AT. Systemic capillary leak syndrome. Chest. 1993;104(5):1637-1638.
33. Horwith M, Hagstrom JW, Riggins RC, Luckey EH. Hypovolemic shock and edema due to increased capillary permeability. JAMA. 1967;200(2):101-104.
34. Johansson BR, Lofdahl CG. Ultrastructure of the microvessels in skeletal muscle in a case of systemic capillary leak syndrome. Acta Med Scand. 1979;206(5):413-416. (Pubitemid 10218479)
35. Alikhani M, Roy S, Graves DT. FOXO1 plays an essential role in apoptosis of retinal pericytes. Mol Vis. 2010;16:408-415.
36. Walshe TE, Saint-Geniez M, Maharaj AS, Sekiyama E, Maldonado AE, D'Amore PA. TGF-beta is required for vascular barrier function, endothelial survival and homeostasis of the adult microvasculature. PLoS One. 2009;4(4):e5149.
37. Harris ES, Nelson WJ. VE-cadherin: at the front, center, and sides of endothelial cell organization and function. Curr Opin Cell Biol. 2010;22(5):651-658.
38. Sumitomo N, Sakurada H, Taniguchi K, et al. Association of atrial arrhythmia and sinus node dysfunction in patients with catecholaminergic polymorphic ventricular tachycardia. Circ J. 2007;71(10):1606-1609. (Pubitemid 47529664)
39. Spindler V, Peter D, Harms GS, Asan E, Waschke J. Ultrastructural analysis reveals cAMP-dependent enhancement of microvascular endothelial barrier functions via Rac1-mediated reorganization of intercellular junctions. Am J Pathol. 2011;178(5):2424-2436.
40. Spindler V, Waschke J. Beta-adrenergic stimulation contributes to maintenance of endothelial barrier functions under baseline conditions. Microcirculation. 2011;18(2):118-127.
41. Rampersad SN, Ovens JD, Huston E, et al. Cyclic AMP phosphodiesterase 4D (PDE4D) tethers EPAC1 in a vascular endothelial cadherin (VE-Cad)-based signaling complex and controls cAMP-mediated vascular permeability. J Biol Chem. 2010;285(44):33614-33622.
42. Gavard J, Gutkind JS. VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol. 2006;8(11):1223-1234. (Pubitemid 44660587)
43. Parikh SM, Mammoto T, Schultz A, et al. Excess circulating angiopoietin-2 may contribute to pulmonary vascular leak in sepsis in humans. PLoS Med. 2006;3(3):e46.
44. Mammoto T, Parikh SM, Mammoto A, et al. Angiopoietin-1 requires p190 RhoGAP to protect against vascular leakage in vivo. J Biol Chem. 2007;282(33):23910-23918. (Pubitemid 47328051)
45. Gallagher DC, Bhatt RS, Parikh SM, et al. Angiopoietin 2 is a potential mediator of high-dose interleukin 2-induced vascular leak. Clin Cancer Res. 2007;13(7):2115-2120. (Pubitemid 46649880)
46. van der Heijden M, van Nieuw Amerongen GP, Koolwijk P, van Hinsbergh VW, Groeneveld AB. Angiopoietin-2, permeability oedema, occurrence and severity of ALI/ARDS in septic and non-septic critically ill patients. Thorax. 2008;63(10):903-909.
47. Rissanen TT, Vajanto I, Hiltunen MO, et al. Expression of vascular endothelial growth factor and vascular endothelial growth factor receptor-2 (KDR/Flk-1) in ischemic skeletal muscle and its regeneration. Am J Pathol. 2002;160(4):1393-1403. (Pubitemid 34411643)
48. Iacobellis G, Cipriani R, Gabriele A, Di Mario U, Morano S. High circulating vascular endothelial growth factor (VEGF) is related to a better systolic function in diabetic hypertensive patients. Cytokine. 2004;27(1):25-30. (Pubitemid 38786456)
49. Dixit M, Bess E, Fisslthaler B, et al. Shear stressinduced activation of the AMP-activated protein kinase regulates FoxO1a and angiopoietin-2 in endothelial cells. Cardiovasc Res. 2008;77(1):160-168. (Pubitemid 351195147)
50. Scharpfenecker M, Fiedler U, Reiss Y, Augustin HG. The Tie-2 ligand angiopoietin-2 destabilizes quiescent endothelium through an internal autocrine loop mechanism. J Cell Sci. 2005;118(Pt 4):771-780. (Pubitemid 40372585)
51. Tabruyn SP, Colton K, Morisada T, et al. Angiopoietin-2-driven vascular remodeling in airway inflammation. Am J Pathol. 2010;177(6): 3233-3243.
52. Eliceiri BP, Paul R, Schwartzberg PL, Hood JD, Leng J, Cheresh DA. Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol Cell. 1999;4(6):915-924. (Pubitemid 30054898)
53. Weis S, Shintani S, Weber A, et al. Src blockade stabilizes a Flk/cadherin complex, reducing edema and tissue injury following myocardial infarction. J Clin Invest. 2004;113(6):885-894. (Pubitemid 38544147)
54. Eremina V, Jefferson JA, Kowalewska J, et al. VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med. 2008;358(11):1129-1136. (Pubitemid 351398487)
55. Ballow M. The IgG molecule as a biological immune response modifier: mechanisms of action of intravenous immune serum globulin in autoimmune and inflammatory disorders. J Allergy Clin Immunol. 2011;127(2):315-323; quiz 324-315.
56. Anthony RM, Kobayashi T, Wermeling F, Ravetch JV. Intravenous gammaglobulin suppresses inflammation through a novel T(H)2 pathway. Nature. 2011;475(7354):110-113.
57. Kumpers P, David S, Haubitz M, et al. The Tie2 receptor antagonist angiopoietin-2 facilitates vascular inflammation in systemic lupus erythematosus. Ann Rheum Dis. 2009;68(10):1638-1643.
58. Yang ZY, Duckers HJ, Sullivan NJ, Sanchez A, Nabel EG, Nabel GJ. Identification of the Ebola virus glycoprotein as the main viral determinant of vascular cell cytotoxicity and injury. Nat Med. 2000;6(8):886-889. (Pubitemid 30644746)