Endothelial nitric oxide synthase is critical for ischemic remodeling, mural cell recruitment, and blood flow reserve

被引:277
作者
Yu, J
deMuinck, ED
Zhuang, ZW
Drinane, M
Kauser, K
Rubanyi, GM
Qian, HS
Murata, T
Escalante, B
Sessa, WC
机构
[1] Yale Univ, Sch Med, Boyer Ctr Mol Med, Dept Pharmacol, New Haven, CT 06536 USA
[2] Yale Univ, Sch Med, Boyer Ctr Mol Med, Vasc Cell Signaling & Therapeut Program, New Haven, CT 06536 USA
[3] Dartmouth Coll Sch Med, Angiogenesis Res Ctr, Lebanon, NH 03756 USA
[4] Berlex Biosci, Gene Therapy Dept, Richmond, CA 94806 USA
[5] Inst Politecn Nacl, Ctr Invest & Estudios Avanzados, Dept Mol Biomed, Mexico City 07360, DF, Mexico
关键词
angiogenesis; arteriogenesis; genetics;
D O I
10.1073/pnas.0501444102
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The genetic loss of endothelial-derived nitric oxide synthase (eNOS) in mice impairs vascular endothelial growth factor (VEGF) and ischemia-initiated blood flow recovery resulting in critical limb ischemia. This result may occur through impaired arteriogenesis, angiogenesis, or mobilization of stem and progenitor cells. Here, we show that after ischemic challenge, eNOS knockout mice [eNOS (-/-)] have defects in arteriogenesis and functional blood flow reserve after muscle stimulation and pericyte recruitment, but no impairment in endothelial progenitor cell recruitment. More importantly, the defects in blood flow recovery, clinical manifestations of ischemia, ischemic reserve capacity, and pericyte recruitment into the growing neovasculature can be rescued by local intramuscular delivery of an adenovirus encoding a constitutively active allele of eNOS, eNOS S1179D, but not a control virus. Collectively, our data suggest that endogenous eNOS-derived NO exerts direct effects in preserving blood flow, thereby promoting arteriogenesis, angiogenesis, and mural cell recruitment to immature angiogenic sprouts.
引用
收藏
页码:10999 / 11004
页数:6
相关论文
共 41 条
[1]   Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells [J].
Aicher, A ;
Heeschen, C ;
Mildner-Rihm, C ;
Urbich, C ;
Ihling, C ;
Technau-Ihling, K ;
Zeiher, AM ;
Dimmeler, S .
NATURE MEDICINE, 2003, 9 (11) :1370-1376
[2]   Expression and function of recombinant S1179D endothelial nitric oxide synthase in canine cerebral arteries [J].
Akiyama, M ;
Eguchi, D ;
Weiler, D ;
O'Brien, T ;
Kovesdi, I ;
Scotland, RS ;
Sessa, WC ;
Katusic, ZS .
STROKE, 2002, 33 (04) :1071-1076
[3]   Endothelial NOS is main mediator for shear stress-dependent angiogenesis in skeletal muscle after prazosin administration [J].
Baum, O ;
Da Silva-Azevedo, L ;
Willerding, G ;
Wöckel, A ;
Planitzer, G ;
Gossrau, R ;
Pries, AR ;
Zakrzewicz, A .
AMERICAN JOURNAL OF PHYSIOLOGY-HEART AND CIRCULATORY PHYSIOLOGY, 2004, 287 (05) :H2300-H2308
[4]   Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions [J].
Carmeliet, P ;
Moons, L ;
Luttun, A ;
Vincenti, V ;
Compernolle, V ;
De Mol, M ;
Wu, Y ;
Bon, F ;
Devy, L ;
Beck, H ;
Scholz, D ;
Acker, T ;
DiPalma, T ;
Dewerchin, M ;
Noel, A ;
Stalmans, I ;
Barra, A ;
Blacher, S ;
Vandendriessche, T ;
Ponten, A ;
Eriksson, U ;
Plate, KH ;
Foidart, JM ;
Schaper, W ;
Charnock-Jones, DS ;
Hicklin, DJ ;
Herbert, JM ;
Collen, D ;
Persico, MG .
NATURE MEDICINE, 2001, 7 (05) :575-583
[5]  
Couffinhal T, 1998, AM J PATHOL, V152, P1667
[6]   Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation [J].
Dimmeler, S ;
Fleming, I ;
Fisslthaler, B ;
Hermann, C ;
Busse, R ;
Zeiher, AM .
NATURE, 1999, 399 (6736) :601-605
[7]   Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability [J].
Fukumura, D ;
Gohongi, T ;
Kadambi, A ;
Izumi, Y ;
Ang, J ;
Yun, CO ;
Buerk, DG ;
Huang, PL ;
Jain, RK .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2001, 98 (05) :2604-2609
[8]   Regulation of endothelium-derived nitric oxide production by the protein kinase Akt [J].
Fulton, D ;
Gratton, JP ;
McCabe, TJ ;
Fontana, J ;
Fujio, Y ;
Walsh, K ;
Franke, TF ;
Papapetropoulos, A ;
Sessa, WC .
NATURE, 1999, 399 (6736) :597-601
[9]   Cell-permeable peptides improve cellular uptake and therapeutic gene delivery of replication-deficient viruses in cells and in vivo [J].
Gratton, JP ;
Yu, J ;
Griffith, JW ;
Babbitt, RW ;
Scotland, RS ;
Hickey, R ;
Giordano, FJ ;
Sessa, WC .
NATURE MEDICINE, 2003, 9 (03) :357-362
[10]   Selective inhibition of tumor microvascular permeability by cavtratin blocks tumor progression in mice [J].
Gratton, JP ;
Lin, MI ;
Yu, J ;
Weiss, ED ;
Jiang, ZJ ;
Fairchild, TA ;
Iwakiri, Y ;
Groszmann, R ;
Claffey, KP ;
Cheng, YC ;
Sessa, WC .
CANCER CELL, 2003, 4 (01) :31-39