Temporal changes in microvessel leakiness during wound healing discriminated by in vivo fluorescence recovery after photobleaching

Journal of Physiology

Volumn 589, Issue 19, 2011, Pages 4681-4696

  Machado, Maria J C ^a   Mitchell, Christopher A ^a  

^a UNIVERSITY OF ULSTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCEIN ISOTHIOCYANATE DEXTRAN;

ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; BLOOD VESSEL WALL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; IN VIVO STUDY; MALE; MATHEMATICAL ANALYSIS; MICROVASCULATURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SKINFOLD; VASCULAR ENDOTHELIUM; WOUND HEALING;

ANGIOGENESIS INHIBITORS; ANIMALS; CAPILLARY PERMEABILITY; CYCLOHEXANES; DEXTRANS; ENDOTHELIUM; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; LINEAR MODELS; MALE; MICE; MICE, INBRED BALB C; MICROSCOPY, FLUORESCENCE; MICROSCOPY, VIDEO; MICROVESSELS; SESQUITERPENES; WOUND HEALING;

EID: 80053420126     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.208355     Document Type: Article

References (59)

1. Arturson G (2000). Forty years in burn research - the postburn inflammatory response. Burns 26, 599-604.
2. Axelrod D, Koppel DE, Schlessinger J, Elson E & Webb WW (1976). Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys J 16, 1055-1069.
3. Beecken W-D, Engl T, Blaheta R, Bentas W, Achilles E-G, Jonas D, Shing Y & Camphausen K (2004). Angiogenesis inhibition by angiostatin, endostatin and TNP-470 prevents cyclosphophamide induced cystitis. Angiogenesis 7, 69-73.
4. Berk DA, Yuan F, Leunig M & Jain RK (1997). Direct in vivo measurement of targeted binding in a human tumour xenograft. Proc Natl Acad Sci USA 94, 1785-1790.
5. Berk DA, Swartz MA, Leu AJ & Jain RK (1996). Transport in lymphatic capillaries. II: microscopic velocity measurement with fluorescence photobleaching. Am J Physiol Heart Circ Physiol 270, H330-H337.
6. Bini A, Wu D & Schuer J (1999). Characterization of stromelysin (MMP-3), matrilysin (MMP-7) and MT1-MMP derived fibrin(ogen) fragments D-dimer and D-like monomer: NH2-terminal sequences of late-stage digest fragment. Biochemistry 38, 13928-13936.
7. Bond SJ & Klein SA (2001). TNP-470 reduces collagen and macrophage accumulation in expanded polytetrafluoroethylene tube implants. J Surg Res 101, 99-103.
8. Bond SJ, Klein SA, Anderson GL & Wittliff JL (2000). Interaction of angiogenesis inhibitor TNP-470 with basic fibroblast growth factor receptors. J Surg Res 92, 18-22.
9. Burri PH, Hlushchuck R & Djonov V (2004). Intussusceptive angiogenesis: its emergence, its characteristics, and its significance. Dev Dyn 231, 474-488.
10. Chary SR & Jain RK (1989). Direct measurement of interstitial convection and diffusion of albumin in normal and neoplastic tissues by fluorescence photobleaching. Proc Natl Acad Sci USA 86, 5385-5389.
11. Chary SR & Jain RK (1987). Analysis of diffusive and convective recovery of fluorescence after photobleaching - effect of uniform flow field. Chem Eng Commun 55, 235-249.
12. Cheresh DA & Stupack DG (2008). Regulation of angiogenesis: apoptotic cues from the ECM. Oncogene 27, 6285-6298.
13. Curry F-RE (1986). Determinants of capillary permeability: a review of mechanisms based on single capillary studies in the frog. Circ Res 59, 367-380.
14. Dvorak HF, Brown LF & Detmar M (1995). Vascular permeability factor/VEGF, microvascular hyperpermeability and angiogenesis. Am J Pathol 146, 1029-1039.
15. Gargett CE & Rogers PA (2001). Human endometrial angiogenesis. Reproduction 121, 181-186.
16. Gerlowski LE & Jain RK (1986). Microvascular permeability of normal and neoplastic tissues. Microvasc Res 31, 288-305.
17. Goldman D & Popel AS (2001). A computational study of the effect of vasomotion on oxygen transport from capillary networks. J Theor Biol 209, 189-199.
18. Gribbon P & Hardingham TE (1998). Macromolecular diffusion of biological polymers measured by confocal fluorescence recovery after photobleaching. Biophys J 75, 1032-1039.
19. Guerreiro-Lucas LA, Pop SR, Machado MJC, Ma YL, Waters SL, Richardson GL, Saetzler K, Jensen OE & Mitchell CA (2008). Experimental and theoretical modelling of blind-ended vessels within a developing angiogenic plexus. Microvasc Res 76, 161-168.
20. Gustafsson H, Mulvany MJ & Nilsson H (1993). Rhythmic contractions of isolated small arteries from rat: influence of the endothelium. Acta Physiol Scand 148, 153-163.
21. Guyton AC, Prather J, Scheel K & McGehee J (1966). Interstitial fluid pressure. 4. Its effects on fluid movement through capillary walls. Circ Res 19, 1022-1030.
22. Hansen-Smith F (2000). Capillary network patterning during angiogenesis. Clin Exp Pharmacol Physiol 27, 830-835.
23. Hill CE, Eade J & Sandow SL (1999). Mechanisms underlying spontaneous rhythmical contractions in irideal arterioles of the rat. J Physiol 521, 507-516.
24. Hiller O, Lichte A & Oberpichler A (2000). Matrix metalloproteinases, collagenase-2, macrophage elastase, collagenase-3, and membrane type I-matrix metalloproteinase impair clotting by degradation of fibrinogen and factor XII. J Biol Chem 275, 33008-33013.
25. Iida N (1990). Effects of vasomotion and venous pressure elevation on capillary-tissue fluid exchange across heteroporous membranes. Biorheology 27, 205-224.
26. Ingber D, Fujita T, Kishimoto S, Sudo K, Kanamaru T, Brem H & Folkman J (1990). Synthetic analogues of fumagillin that inhibit angiogenesis and suppress tumour growth. Nature 348, 555-557.
27. Jain RK, Stock RJ, Chary SR & Rueter M (1990). Convection and diffusion measurements using fluorescence recovery after photobleaching and video image analysis: in vitro calibration and assessment. Microvasc Res 39, 77-93.
28. Klein SA, Bond SJ, Gupta SC, Yacoub OA & Anderson GL (1999). Angiogenesis inhibitor TNP-470 inhibits murine cutaneous wound healing. J Surg Res 82, 268-274.
29. Larson DR, Zipfel WR, Williams RM, Clark SW, Bruchez MP, Wise FW & Webb WW (2003). Water-soluble quantum dots for multiphoton fluorescence imaging in vivo. Science 300, 1434-6.
30. Li J, Zhang Y-P & Kirsner RS (2003). Angiogenesis in wound repair: angiogenic growth factors and the extracellular matrix. Mic Res Tech 60, 107-114.
31. Machado MJC, Watson M, Devlin AH, Chaplain MAJ, McDougall SR & Mitchell CA (2011). Dynamics of angiogenesis during wound healing: a coupled in vivo and in silico paradigm. Microcirculation 18, 183-197.
32. McKinney RV & Panner BJ (1972). Regenerating capillary basement membrane in skeletal muscle wounds. Ultrastructural and histochemical study. Lab Invest 26, 100-113.
33. Michel CC & Phillips ME (1987). Steady-sate fluid filtration at different capillary pressures in perfused frog mesenteric capillaries. J Physiol 388, 421-435.
34. Minshall RD & Malik AB (2006). Transport across the endothelium: regulation of endothelial permeability. Handb Ex Pharmacol 176, 107-144.
35. Mysliwski A, Kubasik-Juraniec J, Koszalka P & Szmit E (2004). The effect of angiogenesis inhibitor TNP-470 on the blood vessels of the lungs, kidneys and livers of treated hamsters. Folia Morphol (Warsz) 63, 5-9.
36. Nahari D, Satchi-Fainaro R, Chen M, Mitchell I, Task LB, Liu Z, Kihneman J, Carroll AB, Terada LS & Nwariaku FE (2007). Tumour cytotoxicity and endothelial Rac inhibition induced by TNP-470 in anaplastic thyroid cancer. Mol Cancer Ther 6, 1329-1337.
37. Netti PA, Berk DA, Swartz MA, Grodzinsky AJ & Jain RK (2000). Role of extracellular matrix assembly in interstitial transport in solid tumours. Cancer Res 60, 2497-2503.
38. Ng CP, Helm CE & Swartz MA (2004). Interstitial flow differentially stimulates blood and lymphatic endothelial cell morphogenesis in vitro. Microvasc Res 68, 258-264.
39. Ng CP, Hinz B & Swartz MA (2005). Interstitial fluid flow induces myofibroblast differentiation and collagen alignment in vitro. J Cell Sci 118, 4731-4739.
40. Nilsson H & Aalkjær C (2003). Vasomotion: mechanisms and physiological importance. Mol Interv 3, 79-89.
41. Niwano M, Arii S, Mori A, Ishigami S, Harada T, Mise M, Furutani M, Fujioka M & Imamura M (1998). Inhibition of tumour growth and microvascular angiogenesis by the potent angiogenesis inhibitor, TNP-470, in rats. Surg Today 28, 915-922.
42. Nugent LJ & Jain RK (1984). Plasma pharmacokinetics and interstitial diffusion of macromolecules in a capillary bed. Am J Physiol Heart Circ Physiol 246, H129-H137.
43. Peirce SM & Skalak TC (2003). Microvascular remodelling: A complex continuum spanning angiogenesis to arteriogenesis. Microcirculation 10, 99-111.
44. Perrin RM, Harper SJ & Bates DO (2007). A role for the endothelial glycocalyx in regulating microvascular permeability in diabetes mellitus. Cell Biochem Biophys 49, 65-72.
45. Predescu D & Palade GE (1993). Plasmalemmal vesicles represent the large pore system of continuous microvascular endothelium. Am J Physiol Heart Circ Physiol 265, H725-H733.
46. Proske S, Vollmar B & Menger MD (2000). Microvascular consequences of thrombosis in small venules: An in vivo microscopic study using a novel model in the ear of the hairless mouse. Thromb Res 98, 491-498.
47. Roy R, Zhang B & Moses MA (2006). Making the cut: protease-mediated regulation of angiogenesis. Exp Cell Res 312, 608-622.
48. Rücker M, Strobel O, Vollmar B & Menger MD (2000). Vasomotion in critically perfused muscle protects adjacent tissues from capillary perfusion failure. Am J Physiol Heart Circ Physiol 269, H550-H558.
49. Satchi-Fainaro R, Mamluk R, Wang L, Short SM, Nagy JA, Feng D, Dvorak AM, Dvorak HF, Puder M, Mukhopadhyay D & Folkman J (2005). Inhibition of vessel permeability by TNP-470 and its polymer conjugate, caplostatin. Cancer Cell 7, 251-261.
50. Schnitzer JE, Oh P, Pinney E & Allard J (1994). Filipin-sensitive caveolae mediated transport in endothelium: reduced transcytosis, scavenger endocytosis and capillary permeability of selected macromolecules. J Cell Biol 127, 1217-1232.
51. Schoefl GI (1963). Studies on inflammation. III. Growing capillaries: their structure and permeability. Virchows Arch Path Anat Physiol Kin Med 337, 97-141.
52. Singer AJ & Clark RAF (1999). Cutaneous wound healing. New Engl J Med 341, 738-746.
53. Simon JR, Gough A, Urbanik E, Wang F, Lanni F, Ware BR & Taylor DL (1988). Analysis of rhodamine and fluorescein-labelled F-actin diffusion in vitro by fluorescence recovery after photobleaching. Biophys J 54, 801-815.
54. Sorg H, Krueger C & Vollmar B (2007). Intravital insights in skin wound healing using the mouse dorsal skinfold chamber. J Anat 211, 811-818.
55. Stansberry KB, Shapiro SA, Hill MA, McNitt PM, Meyer MD & Vinik AI (1996). Impaired peripheral vasomotion in diabetes. Diabetes Care 19, 715-721.
56. Wilkin JK (1986). Periodic cutaneous blood flow during post-occlusive reactive hyperaemia. Am J Physiol Heart Circ Physiol 250, H765-H768.
57. Witte MB & Barbul A (1997). General principles of wound healing. Surg Clin North Am 77, 509-528.
58. Yuan F, Leunig M, Berk DA & Jain RK (1993). Microvascular permeability of albumin, vascular surface area, and vascular volume measured in human adenocarcinomas LS174T using dorsal chamber in SCID mice. Microvasc Res 45, 269-289.
59. Velnar T, Bailey T & Smrkolj V (2009). The wound healing process: an overview of the cellular and molecular mechanisms. J Int Med Res 37, 1528-42.