The roles of nitric oxide in murine cardiovascular development

Developmental Biology

Volumn 292, Issue 1, 2006, Pages 25-33

  Nath, Anjali K ^a,b   Madri, Joseph A ^b  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiovascular; Development; Diabetes; Nitric oxide; Nitric oxide synthase; Vasculopathy; Vitelline; Yolk sac

Indexed keywords

NITRIC OXIDE;

ANGIOGENESIS; CARDIOVASCULAR SYSTEM; CELL AGGREGATION; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONGENITAL HEART MALFORMATION; DEVELOPMENT; DIABETES MELLITUS; EMBRYO DEVELOPMENT; GENE EXPRESSION; HUMAN; HYPERGLYCEMIA; KNOCKOUT MOUSE; LUNG DEVELOPMENT; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; ORGANOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REPRODUCTION; REVIEW; ANIMAL; EXPERIMENTAL DIABETES MELLITUS; METABOLISM; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PRENATAL DEVELOPMENT;

MAMMALIA; MURINAE;

ANIMALS; CARDIOVASCULAR SYSTEM; DIABETES MELLITUS, EXPERIMENTAL; HUMANS; MICE; NITRIC OXIDE;

EID: 33646457351     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2005.12.039     Document Type: Review

References (96)

1. Akassoglou K. NGF requirement for neuronal survival? NO thanks!. Mol. Pharmacol. (2005) (18 July [electronic publication ahead of print])
2. Akool E.S., Doller A., Muller R., Gutwein P., Xin C., Huwiler A., Pfeilschifter J., Pfeilschifter J., and Eberhardt W. Nitric oxide induces TIMP-1 expression by activating the TGFbeta-SMAD signaling pathway. J. Biol. Chem. (2005) (Sep 23; electronic publication)
3. Al-Shabrawey M., El-Remessy A.B., Xiaolin Gu X., Steven S., Brooks S.S., Hamed M.S., Huang P., and Caldwell R.B. Normal vascular development in mice deficient in endothelial NO synthase: possible role of neuronal NO synthase. Mol. Vision 9 (2003) 549-558
4. Baker L., and Piddlington R. Diabetic embryopathy; a selective review of recent trends. J. Diabetes Its Complicat. 7 (1993) 404-412
5. Basson C.T., Cowley G.S., Solomon S.D., Weissman B., Poznanski A.K., Traill T.A., Seidman J.G., and Seidman C.E. Clinical and genetic spectrum of the Holt-Oram syndrome (heart-hand syndrome). N. Engl. J. Med.. 330 (1994) 885-891
6. Bicker G. STOP and GO with NO: nitric oxide as a regulator of cell motility in simple brains. BioEssays 27 (2005) 495-505
7. Bloch W., Fleischmann B.K., Lorke D.E., Andressen C., Hop s.B., Hescheler J., and Addicks K. Nitric oxide synthase expression and role during cardiomyogenesis. Cardiovasc. Res. 43 (1999) 675-684
8. Brodsky S.V., Morrishow A.M., Dharia N., Gross S.S., and Goligorsky M.S. Glucose scavenging of nitric oxide. Am. J. Physiol.: Renal. Physiol. 280 (2001) F480-F486
9. Brune B., von Knethen A., and Sandau K.B. Nitric oxide (NO): an effector of apoptosis. Cell Death Differ. 6 (1999) 969-975
10. Brune B., von Knethen A., and Sandau K.B. Transcription factors p53 and HIF-1alpha as targets of nitric oxide. Cell Signalling 13 (2001) 525-533
11. Channon K.M., Qian H., and George S.E. Nitric oxide synthase in atherosclerosis and vascular injury: insights from experimental gene therapy. Arterioscler. Thromb. Vasc. Biol. 20 (2000) 1873-1881
12. Chen H.H., and Wang D.L. Nitric oxide inhibits matrix metalloproteinase-2 expression via the induction of activating transcription factor 3 in endothelial cells. Mol. Pharmacol. 65 (2004) 1130-1140
13. Chen A.F., Ren J., and Miao C.Y. Nitric oxide synthase gene therapy for cardiovascular disease. Jpn. J. Pharmacol. 89 (2002) 327-336
14. Chen J., Zacharek A., Zhang C., Jiang H., Li Y., Roberts C., Lu M., Kapke A., and Chopp M. Endothelial nitric oxide synthase regulates brain-derived neurotrophic factor expression and neurogenesis after stroke in mice. J. Neurosci. 25 (2005) 2366-2375
15. Chwalisz K., Buhimschi I., and Garfield R.E. Role of nitric oxide in obstetrics. Prenat. Neonatal. Med. (Berlin) 1 (1996) 292-328
16. Ekerhovd E., Brannstrom M., Alexandersson M., and Norstrom A. Evidence for nitric oxide mediation of contractile activity in isolated strips of the human fallopian tube. Hum. Reprod. 12 (1997) 301-305
17. Ellington S.K. Effects of excess glucose on mammalian post-implantation embryos. Int. J. Dev. Biol. 41 (1997) 299-306
18. Enciso J.M., Gratzinger D., Camenisch T.D., Canosa S., Pinter E., and Madri J.A. Elevated glucose inhibits VEGF-A-mediated endocardial cushion formation: modulation by PECAM-1 and MMP-2. J. Cell Biol. 160 (2003) 605-615
19. Eriksson U.J., Hakan-Borg L.A., Forsberg H., and Styrud J. Studies with animal and in vitro models. Diabetes 40 (1991) 94-98
20. Erwin P.A., Lin A.J., Golan D.E., and Michel T. Receptor-regulated dynamic S-nitrosylation of endothelial nitric-oxide synthase in vascular endothelial cells. J. Biol. Chem. 280 (2005) 19888-19894
21. Feng Q., Song W., Lu X., Hamilton J.A., Lei M., Peng T., and Yee S.P. Development of heart failure and congenital septal defects in mice lacking endothelial nitric oxide synthase. Circulation 106 (2002) 873-879
22. Ferencz C., Rubin J.D., McCarter R.J., and Clark E.B. Maternal diabetes and cardiovascular malformations: predominance of double outlet right ventricular and truncus arteriosus. Teratology 41 (1990) 319-326
23. Forstermann U., Boissel J.P., and Kleinert H. Expressional control of the 'constitutive' isoforms of nitric oxide synthase (NOS I and NOS III). FASEB J. 12 (1998) 773-790
24. Gagioti S., Scavone C., and Bevilacqua E. Participation of the mouse implanting trophoblast in nitric oxide production during pregnancy. Biol. Reprod. 62 (2000) 260-268
25. Galambos C., Ng Y.S., Ali A., Noguchi A., Lovejoy S., D'Amore P.A., and DeMello D.E. Defective pulmonary development in the absence of heparin-binding vascular endothelial growth factor isoforms. Am. J. Respir. Cell Mol. Biol. 27 (2002) 194-203
26. Gewaltig M.T., and Kojda G. Vasoprotection by nitric oxide: mechanisms and therapeutic potential. Cardiovasc. Res. 55 (2002) 250-260
27. Godfrey E.W., and Schwarte R.C. The role of nitric oxide signaling in the formation of the neuromuscular junction. J. Neurocytol. 32 (2003) 591-602
28. Gouge R.C., Marshburn P., Gordon B.E., Nunley W., and Huet-Hudson Y.M. Nitric oxide as a regulator of embryonic development. Biol. Reprod. 58 (1998) 875-879
29. Gratzinger D., Canosa S., Engelhardt B., and Madri J.A. Platelet endothelial cell adhesion molecule-1 modulates endothelial cell motility through the small G-protein Rho. FASEB J. 17 (2003) 1458-1469
30. Gregg A.R. Mouse models and the role of nitric oxide in reproduction. Curr. Pharm. Des. 9 (2003) 391-398
31. Han R.N., Babae i.S., Robb M., Lee T., Ridsdale R., Ackerley C., Post M., and Stewart D.J. Defective lung vascular development and fatal respiratory distress in endothelial NO synthase-deficient mice: a model of alveolar capillary dysplasia?. Circ. Res. 94 (2004) 1115-1123
32. Hefler L.A., Reyes C.A., and O'Brien W.E. Perinatal development of endothelial nitric oxide synthase-deficient mice. Biol. Reprod. 64 (2001) 666-673
33. Huber A., Saur D., Kurjak M., Schusdziarra V., and Allescher H.D. Characterization and splice variants of neuronal nitric oxide synthase in rat small intestine. Am. J. Physiol.: Gastrointest. Liver Physiol. 275 (1998) G1146-G1156
34. Jablonka-Shariff A., and Olson L.M. The role of nitric oxide in oocyte meiotic maturation and ovulation: meiotic abnormalities of endothelial nitric oxide synthase knock-out mouse oocytes. Endocrinology 139 (1998) 2944-2954
35. Jozkowicz A., Cooke J.P., Guevara I., Huk I., Funovics P., Pachinger O., Weidinger F., and Dulak J. Genetic augmentation of nitric oxide synthase increases the vascular generation of VEGF. Cardiovasc. Res. 51 (2001) 773-783
36. Jozkowicz A., Dulak J., Nigisch A., Funovics P., Weigel G., Polterauer P., Huk I., and Malinski T. Involvement of nitric oxide in angiogenic activities of vascular endothelial growth factor isoforms. Growth Factors 22 (2004) 19-28
37. Kasapinovic S., McCallum G.P., Wiley M.J., and Wells P.G. The peroxynitrite pathway in development: phenytoin and benzo(a)pyrene embryopathies in inducible nitric oxide synthase knockout mice. Free Radical Biol. Med. 37 (2004) 1703-1711
38. Kitzmiller J.L., Buchanan T.A., Kjos S., Combs A.C., and Ratner R.E. Pre-conception care of diabetes, congenital malformations, and spontaneous abortions. Diabetes Care 19 (1996) 514-541
39. Kleinert H., Pautz A., Linker K., and Schwarz P.M. Regulation of the expression of inducible nitric oxide synthase. Eur. J. Pharmacol. 500 (2004) 255-266
40. Kolesnikov Y.A., Pan Y.X., Babey A.M., Wilson S., and Pasternak R. Functionally differentiating two neuronal nitric oxide synthase isoforms through antisense mapping: evidence for opposing NO actions on morphine analgesia and tolerance. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 8220-8225
41. Kone B.C., Kuncewicz T., Zhang W., and Yu Z.Y. Protein interactions with nitric oxide synthases: controlling the right time, the right place, and the right amount of nitric oxide. Am. J. Physiol.: Renal. Physiol. 285 (2003) 178-190
42. Kuzin B., Roberts I., Peunova N., and E. G. Nitric oxide regulates cell proliferation during Drosophila development. Cell 87 (1996) 639-649
43. Kuzin B., Regulski M., Stasiv Y., Scheinker V., Tully T., and Enikolopov G. Nitric oxide interacts with the retinoblastoma pathway to control eye development in Drosophila. Curr. Biol. 10 (2000) 459-462
44. Lacza Z., Pankotai E., Csordas A., Gero D., Kiss L., Horvath E.M., Kollai M., Busija D.W., and Szabo C. Mitochondrial NO and reactive nitrogen species production: does mtNOS exist. Nitric Oxide (2005) (Jul 25; [electronic publuication ahead of print])
45. Lee T.C., Zhao Y.D., Courtman D.W., and Stewart D.J. Abnormal aortic valve development in mice lacking endothelial nitric oxide synthase. Circulation 101 (2000) 2345-2348
46. Li H., Wallerath T., Munzel T., and Fostermann U. Regulation of endothelial-type NO synthase expression in pathophysiology and in response to drugs. Nitric Oxide 7 (2002) 149-164
47. Madri J.A., Enciso J., and Pinter E. Maternal diabetes: effects on embryonic vascular development-a vascular endothelial growth factor-A-mediated process. Pediatr. Dev. Pathol. 6 (2003) 334-341
48. Martins G.A., Cardoso M.A., Aliberti J.C., and Silva J.S. Nitric oxide-induced apoptotic cell death in the acute phase of Trypanosoma cruzi infection in mice. Immunol. Lett. 63 (1998) 113-120
49. Mashimo H., and Goyal R.K. Lessons from genetically engineered animal models. IV. Nitric oxide synthase gene knockout mice. Am. J. Physiol. 277 (1999) G745-G750
50. Miquerol L., Gertsenstein M., Harpal K., Rossant J., and Nagy A. Multiple developmental roles of VEGF suggested by a LacZ-tagged allele. Dev. Biol. 212 (1999) 307-322
51. Miquerol L., Langille B.L., and Nagy A. Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development 127 (2000) 3941-3946
52. Mize R.R., and Lo F. Nitric oxide, impulse activity, and neurotrophins in visual system development (1). Brain Res. 886 (2000) 15-32
53. Moncada S., Higgs A., and Furchgott R. International union of pharmacology nomenclature in nitric oxide research. Pharmacol. Rev. 49 (1997) 137-142
54. Moore Z.W., and Hui D.Y. Apolipoprotein E inhibition of vascular cell proliferation and neointimal formation in vivo requires inducible nitric oxide synthase. J. Lipid. Res. (2005) (Aug 1; [electronic publication ahead of print])
55. Morishita T., Tsutsui M., Shimokawa H., Sabanai K., Tasaki H., Suda O., Nakata S., Tanimoto A., Wang K.Y., Ueta Y., Sasaguri Y., Nakashima Y., and Yanagishara N. Nephrogenic diabetes insipidus in mice lacking all nitric oxide synthase isoforms. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 10616-10621
56. Mügge A., Elwell J.H., Peterson T.E., Hofmeyer T.G., Heistad D.D., and Harrison D.G. Chronic treatment with polyethylene-glycolated superoxide dismutase partially restores endothelium-dependent vascular relaxations in cholesterol-fed rabbits. Circ. Res. 69 (1991) 1293-1300
57. Naseem K.M. The role of nitric oxide in cardiovascular diseases. Mol. Aspects Med. 26 (2005) 33-65
58. Nath A.K., Enciso J., Kuniyasu M., Hao X.-Y., Madri J.A., and Pinter E. Nitric oxide modulates murine yolk sac vasculogenesis and rescues glucose induced vasculopathy. Development 131 (2004) 2485-2496
59. Nathan C., and Xie Q.N. Nitric oxide synthases: roles, tolls, and controls. Cell 78 (1994) 915-918
60. Nicotera P., Bernassola F., and Melino G. Nitric oxide (NO), a signaling molecule with a killer soul. Cell Death Differ. 6 (1999) 931-933
61. Novaro V., Gonzalez E., and Jawerbaum A. Nitric oxide synthase regulation during embryonic implantation. Reprod. Fertil. Dev. 9 (1997) 557-564
62. Pampfer S., Vanderheyden I., McCracken J.E., Vesela J., and DeHertogh R. Increased cell death in rat blastocysts exposed to maternal diabetes in utero and to high glucose or tumor necrosis factor-a in vitro. Development 124 (1997) 4827-4836
63. Panda, K., Adak, S., Aulak, K., Santolini, J., McDonald, J.F., and Stuehr, D.J., Distinct influence of N-terminal elements on neuronal nitric-oxide synthase structure and catalysis. J. Biol. Chem.. 278, 37122-37131.
64. Papapetropoulos A., Desai K.M., Rudic R.D., Mayer B., Zhang R., Ruiz-Torres M.P., Garcia-Cardena G., Madri J.A., and Sessa W.C. Nitric oxide synthase inhibitors attenuate transforming-growth-factor-beta 1-stimulated capillary organization in vitro. Am. J. Pathol. 150 (1997) 1835-1844
65. Papapetropoulos A., Garcia-Cardena G., Madri J.A., and Sessa W.C. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J. Clin. Invest. 100 (1997) 3131-3139
66. Phillips P.G., Birnby L.M., Narendran A., and Milonovich W.L. Nitric oxide modulates capillary formation at the endothelial cell-tumor cell interface. Am. J. Physiol.: Lung Cell Mol. Physiol. 281 (2001) L278-L290
67. Phillips P.G., and Birnby L.M. Nitric oxide modulates caveolin-1 and matrix metalloproteinase-9 expression and distribution at the endothelial cell/tumor cell interface. Am. J. Physiol.: Lung Cell Mol. Physiol. 286 (2004) L1055-L1065
68. Pineda-Molina E., and Lamas S. Nitric oxide as a regulator of gene expression: studies with the transcription factor proteins cJun and p50. BioFactors 15 (2001) 113-115
69. Pinter E., Reece E.A., Leranth C.Z., Sanyal M.K., Hobbins J.C., Mahoney M.J., and Naftolin F. Yolk sac failure in embryopathy due to hyperglycemia: ultrastructural analysis of yolk sac differentiation associated with embryopathy in rat conceptuses under hyperglycemic conditions. Teratology 33 (1986) 73-84
70. Pinter E., Barreuther M., Lu T.T., Imhof B.A., and Madri J.A. Platelet-endothelial cell adhesion molecule-1 (PECAM-1/CD31) tyrosine phosphorylation state changes during vasculogenesis in the murine conceptus. Am. J. Pathol. 150 (1997) 1523-1530
71. Pinter E., Mahooti S., Wang V., Imhof B.A., and Madri J.A. Hyperglycemia-induced vasculopathy in the murine vitelline vasculature: correlation with PECAM-1/CD31 tyrosine phosphorylation state. Am. J. Pathol. 154 (1999) 1367-1379
72. Pinter E., Haigh J., Nagy A., and Madri J.A. Hyperglycemia-induced vasculopathy in the murine conceptus is mediated via reductions of VEGF-A expression and VEGF receptor activation. Am. J. Pathol. 158 (2001) 1199-1206
73. Purcell T.L., Given R., Chwalisz K., and Garfield R.E. Nitric oxide synthase distribution during implantation in the mouse. Mol. Hum. Reprod. 5 (1999) 467-475
74. Richard C., Gao J., LaFleur B., Christman B.W., Anderson J., Brown N., and Reese J. Patency of the preterm fetal ductus arteriosus is regulated by endothelial nitric oxide synthase and is independent of vasa vasorum in the mouse. Am. J. Physiol.: Regul., Integr. Comp. Physiol. 287 (2004) R652-R660
75. Salvemini D., Misko T.P., Masferrer J.L., Seirbert L.K., Currie M.G., and Needleman P. Nitric oxide activates cyclooxygenase enzymes. Proc. Natl. Acad. Sci. 90 (1993) 7240-7244
76. Schwarte R.C., and Godfrey E.W. Nitric oxide synthase activity is required for postsynaptic differentiation of the embryonic neuromuscular junction. Dev. Biol. 273 (2004) 276-284
77. Schwarz R., and Teramo K.A. Effects of diabetic pregnancy on the fetus and newborn. Sem. Perinatol. 24 (2000) 120-135
78. Sengoku K., Takuma N., Horikawa M., Tsuchiya K., Komori H., Sharifa D., Tamate K., and Ishikawa M. Requirement of nitric oxide for murine oocyte maturation, embryo development, and trophoblast outgrowth in vitro. Mol. Reprod. Dev. 58 (2001) 262-268
79. Shah A.M. Inducible nitric oxide synthase and cardiovascular disease. Cardiovasc. Res. 45 (2000) 148-155
80. Shukovski L., and Tsafriri T. The involvement of nitric oxide in the ovulatory process in the rat. Endocrinology 135 (1995) 2287-2290
81. Stamler J.S. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 78 (1994) 931-936
82. Stamler J.S., Singel D.J., and Loscalzo J. Biochemistry of nitric oxide and its redox-activated forms. Science 258 (1992) 1898-1902
83. Takizawa T., Kihara T., Kamata A., Yamamoto M., and Arishima K. Role of nitric oxide in regulating the ductus arteriosus caliber in fetal rats. J. Vet. Med. Sci. 62 (2000) 707-710
84. Tammela T., Enholm B., Alitalo K., and Paavonen K. The biology of vascular endothelial growth factors. Cardiovasc. Res. 65 (2005) 550-563
85. Telfer J.F., Norman J.E., and Cameron I.T. Identification of nitric oxide synthase in human uterus. Hum. Reprod. 10 (1995) 19-23
86. Tranguch S., and Huet-Hudson Y.M. Decreased viability of nitric oxide synthase double knockout mice. Mol. Reprod. Dev. 65 (2003) 175-179
87. Urbich C., Dernbach E., Aicher A., Zeiher A.M., and Dimmeler S. CD40 ligand inhibits endothelial cell migration by increasing production of endothelial reactive oxygen species. Circulation 106 (2002) 981-986
88. Ushio-Fukai M., and Alexander R.W. Reactive oxygen species as mediators of angiogenesis signaling: role of NAD(P)H oxidase. Mol. Cell. Biochem. 264 (2004) 85-97
89. Villamor E., Kessels C.G., van Suylen R.J., De May J.G., and Blanco C.F. Cardiopulmonary effects of chronic administration of the NO synthase inhibitor l-NAME in the chick embryo. Biol. Neonate 88 (2005) 156-163
90. Wang Y., Newton D.C., and Marsden P.A. Neuronal NOS: gene structure, mRNA diversity, and functional relevance. Crit. Rev. Neurobiol. 13 (1999) 21-43
91. Wu H.H., Cork R.J., Huang P.L., Shuman D.L., and Mize R.R. Refinement of the ipsilateral retinocollicular projection is disrupted in double endothelial and neuronal nitric oxide synthase gene knockout mice. Brain Res. Dev. Brain Res. 120 (2000) 105-111
92. Yang J.Z., Ajonuma L.C., Rowlands D.K., Tsang L.L., Ho L.S., Lam S.Y., Chen W.Y., Zhou C.X., Chung Y.W., Cho C.Y., Hoi Tse J.Y., James A.E., and Chan H.C. The role of inducible nitric oxide synthase in gamete interaction and fertilization: a comparative study on knockout mice of three NOS isoforms. Cell Biol. Int. (2005) (Aug 5; [electronic publiaction ahead of print])
93. Young S.L., Evans K., and Eu J.P. Nitric oxide modulates branching morphogenesis in fetal rat lung explants. Am. J. Physiol.: Lung Cell Mol. Physiol. 282 (2002) L379-L385
94. Zhang D.X., Zou A.P., and Li P.L. Ceramide reduces endothelium-dependent vasodilation by increasing superoxide production in small bovine coronary arteries. Circ. Res. 88 (2001) 824-831
95. Zhang W., Kuncewicz T., Yu Z.Y., Zou L., Xu X., and Kone B.C. Protein-protein interactions involving inducible nitric oxide synthase. Acta Physiol. Scand. 179 (2003) 137-142
96. Zhao X., Lu X., and Feng Q. Deficiency in endothelial nitric oxide synthase impairs myocardial angiogenesis. Am. J. Physiol.: Heart Circ. Physiol. 283 (2002) H2371-H2378