Chronic whole-body hypoxia induces intussusceptive angiogenesis and microvascular remodeling in the mouse retina

Microvascular Research

Volumn 79, Issue 2, 2010, Pages 93-101

  Taylor, Alyssa C ^a   Seltz, Lara M ^a   Yates, Paul A ^a,b   Peirce, Shayn M ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Angiogenesis; Hypoxia; Intussusceptive microvascular growth; Microvascular remodeling; Mouse; Retina

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; LECTIN;

ADAPTATION; ANGIOGENESIS; ANIMAL TISSUE; ANTIBODY LABELING; ARTERIOLE; ARTICLE; BLOOD VESSEL DIAMETER; CAPILLARY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENSITY; ENVIRONMENTAL EXPOSURE; FEMALE; HYPOXIA; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; INTUSSUSCEPTIVE ANGIOGENESIS; MICROVASCULARIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RETINA; STAINING;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANOXIA; BIOLOGICAL MARKERS; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MICROVESSELS; RETINAL NEOVASCULARIZATION; RETINAL VESSELS;

ANIMALIA; MUS;

EID: 76749167435     PISSN: 00262862     EISSN: 10959319     Source Type: Journal    
DOI: 10.1016/j.mvr.2010.01.006     Document Type: Article

References (50)

1. Alvarez Y., et al. Genetic determinants of hyaloid and retinal vasculature in zebrafish. BMC Dev. Biol. 7 (2007) 114
2. Antonetti D.A., et al. Diabetic retinopathy: seeing beyond glucose-induced microvascular disease. Diabetes 55 (2006) 2401-2411
3. Arjamaa O., and Nikinmaa M. Oxygen-dependent diseases in the retina: role of hypoxia-inducible factors. Exp. Eye Res. 83 (2006) 473-483
4. Burri P.H., and Djonov V. Intussusceptive angiogenesis-the alternative to capillary sprouting. Mol. Aspects Med. 23 (2002) S1-S27
5. Burri P.H., et al. Intussusceptive angiogenesis: its emergence, its characteristics, and its significance. Dev. Dyn. 231 (2004) 474-488
6. Campochiaro P.A. Retinal and choroidal neovascularization. J. Cell. Physiol. 184 (2000) 301-310
7. Cao R., et al. Hypoxia-induced retinal angiogenesis in zebrafish as a model to study retinopathy. PLoS ONE e2748 (2008) 3
8. Claxton S., and Fruttiger M. Oxygen modifies artery differentiation and network morphogenesis in the retinal vasculature. Dev. Dyn. 233 (2005) 822-828
9. Crivellato E., et al. Recombinant human erythropoietin induces intussusceptive microvascular growth in vivo. Leukemia 18 (2004) 331-336
10. Das A., and McGuire P.G. Retinal and choroidal angiogenesis: pathophysiology and strategies for inhibition. Prog. Retin. Eye Res. 22 (2003) 721-748
11. Deveci D., et al. Chronic hypoxia induces prolonged angiogenesis in skeletal muscles of rat. Exp. Physiol. 87 (2002) 287-291
12. Dhillon D.P., et al. The enlarged carotid body of the chronically hypoxic and chronically hypoxic and hypercapnic rat: a morphometric analysis. Q. J. Exp. Physiol. 69 (1984) 301-317
13. Djonov V., and Makanya A.N. New insights into intussusceptive angiogenesis. EXS (2005) 17-33
14. Djonov V., et al. Vascular remodelling during the normal and malignant life cycle of the mammary gland. Microsc. Res. Tech. 52 (2001) 182-189
15. Djonov V.G., et al. Optimality in the developing vascular system: branching remodeling by means of intussusception as an efficient adaptation mechanism. Dev. Dyn. 224 (2002) 391-402
16. Djonov V., et al. Vascular remodeling by intussusceptive angiogenesis. Cell. Tissue Res. 314 (2003) 107-117
17. Dome B., et al. Alternative vascularization mechanisms in cancer: pathology and therapeutic implications. Am. J. Pathol. 170 (2007) 1-15
18. Dunlop S.A., et al. Changing patterns of vasculature in the developing amphibian retina. J. Exp. Biol. 200 (1997) 2479-2492
19. Egginton S., et al. Unorthodox angiogenesis in skeletal muscle. Cardiovasc. Res. 49 (2001) 634-646
20. Engelson E.T., et al. The microvasculature in skeletal muscle: I. Arteriolar network in rat spinotrapezius muscle. Microvasc. Res. 30 (1985) 29-44
21. Fruttiger M. Development of the retinal vasculature. Angiogenesis 10 (2007) 77-88
22. Funk R.H. Blood supply of the retina. Ophthalmic Res. 29 (1997) 320-325
23. Gariano R.F., and Gardner T.W. Retinal angiogenesis in development and disease. Nature 438 (2005) 960-966
24. Gerhardt H., and Betsholtz C. Endothelial-pericyte interactions in angiogenesis. Cell. Tissue Res. 314 (2003) 15-23
25. Hansen-Smith F., et al. Growth of arterioles precedes that of capillaries in stretch-induced angiogenesis in skeletal muscle. Microvasc. Res. 62 (2001) 1-14
26. Howell K., et al. Chronic hypoxia causes angiogenesis in addition to remodelling in the adult rat pulmonary circulation. J. Physiol. 547 (2003) 133-145
27. Ji J.W., et al. A computational model of oxygen transport in skeletal muscle for sprouting and splitting modes of angiogenesis. J. Theor. Biol. 241 (2006) 94-108
28. Kurz H., et al. Angiogenesis and vascular remodeling by intussusception: from form to function. News Physiol. Sci. 18 (2003) 65-70
29. Linsenmeier R.A., et al. Retinal hypoxia in long-term diabetic cats. Invest. Ophthalmol. Vis. Sci. 39 (1998) 1647-1657
30. Miyamoto O., et al. Vascular changes in the rat brain during chronic hypoxia in the presence and absence of hypercapnia. Acta Med. Okayama 59 (2005) 135-143
31. Murfee W.L., et al. Cell proliferation in mesenteric microvascular network remodeling in response to elevated hemodynamic stress. Ann. Biomed. Eng. 32 (2004) 1662-1666
32. Norrby K., et al. Mast-cell secretion and angiogenesis, a quantitative study in rats and mice. Virchows Arch. B. Cell. Pathol. Incl. Mol. Pathol. 57 (1989) 251-256
33. Palmer L.A., et al. Hypoxia induces type II NOS gene expression in pulmonary artery endothelial cells via HIF-1. Am. J. Physiol. 274 (1998) L212-L219
34. Patan S., et al. Vascular morphogenesis and remodeling in a model of tissue repair: blood vessel formation and growth in the ovarian pedicle after ovariectomy. Circ. Res. 89 (2001) 723-731
35. Peirce S.M., and Skalak T.C. Microvascular remodeling: a complex continuum spanning angiogenesis to arteriogenesis. Microcirculation 10 (2003) 99-111
36. Peirce S.M., et al. Spatial and temporal control of angiogenesis and arterialization using focal applications of VEGF164 and Ang-1. Am. J. Physiol. Heart Circ. Physiol. 286 (2004) H918-H925
37. Pichiule P., and LaManna J.C. Angiopoietin-2 and rat brain capillary remodeling during adaptation and deadaptation to prolonged mild hypoxia. J. Appl. Physiol. 93 (2002) 1131-1139
38. Price R.J., and Skalak T.C. Arteriolar remodeling in skeletal muscle of rats exposed to chronic hypoxia. J. Vasc. Res. 35 (1998) 238-244
39. Saint-Geniez M., et al. The msr/apj gene encoding the apelin receptor is an early and specific marker of the venous phenotype in the retinal vasculature. Gene Expr. Patterns 3 (2003) 467-472
40. Shahidi M., et al. Three-dimensional mapping of chorioretinal vascular oxygen tension in the rat. Invest. Ophthalmol. Vis. Sci. 50 (2009) 820-825
41. Shao R., et al. Increase of SUMO-1 expression in response to hypoxia: direct interaction with HIF-1alpha in adult mouse brain and heart in vivo. FEBS Lett. 569 (2004) 293-300
42. Shortt A.J., et al. Chronic systemic hypoxia causes intra-retinal angiogenesis. J. Anat. 205 (2004) 349-356
43. Smith L.E. Pathogenesis of retinopathy of prematurity. Growth Horm. IGF Res. 14 Suppl. A (2004) S140-S144
44. Smith L.E., et al. Oxygen-induced retinopathy in the mouse. Invest. Ophthalmol. Vis. Sci. 35 (1994) 101-111
45. Stockmann C., and Fandrey J. Hypoxia-induced erythropoietin production: a paradigm for oxygen-regulated gene expression. Clin. Exp. Pharmacol. Physiol. 33 (2006) 968-979
46. Taylor A.C., et al. EphB4 expression along adult rat microvascular networks: EphB4 is more than a venous specific marker. Microcirculation 14 (2007) 253-267
47. Van Gieson E.J., et al. Enhanced smooth muscle cell coverage of microvessels exposed to increased hemodynamic stresses in vivo. Circ. Res. 92 (2003) 929-936
48. Wangsa-Wirawan N.D., and Linsenmeier R.A. Retinal oxygen: fundamental and clinical aspects. Arch. Ophthalmol. 121 (2003) 547-557
49. Ward N.L., et al. Cerebral angiogenic factors, angiogenesis, and physiological response to chronic hypoxia differ among four commonly used mouse strains. J. Appl. Physiol. 102 (2007) 1927-1935
50. Zhou A.L., et al. Capillary growth in overloaded, hypertrophic adult rat skeletal muscle: an ultrastructural study. Anat. Rec. 252 (1998) 49-63