Role of nitric oxide in chick embryonic organogenesis and dysmorphogenesis

Birth Defects Research Part A - Clinical and Molecular Teratology

Volumn 79, Issue 8, 2007, Pages 581-594

  Alexander, Peter G ^a   Chau, Lillian ^a,b   Tuan, Rocky S ^a,c  

^a NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^b Ichor Medical Systems Inc   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Carbon monoxide; Morphogenesis; Nitric oxide; Nitric oxide synthase; Organogenesis; Reactive nitrogen species; Teratogenesis

Indexed keywords

CARBON MONOXIDE; N(G) METHYLARGININE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITROPRUSSIDE SODIUM; TERATOGENIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CHICK EMBRYO; CONGENITAL MALFORMATION; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMBRYO; EMBRYO DEVELOPMENT; HISTOCHEMISTRY; NEURAL TUBE; NONHUMAN; ORGANOGENESIS; OXIDATIVE STRESS; PRENATAL EXPOSURE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SOMITE; TERATOGENICITY;

ANIMALS; APOPTOSIS; CARBON MONOXIDE; CHICK EMBRYO; DRUG COMBINATIONS; EMBRYO LOSS; EMBRYONIC DEVELOPMENT; ENZYME INHIBITORS; NEURAL TUBE DEFECTS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; NITROPRUSSIDE; OMEGA-N-METHYLARGININE; ORGANOGENESIS; SOMITES; TERATOGENS;

EID: 34548062331     PISSN: 15420752     EISSN: 15420760     Source Type: Journal    
DOI: 10.1002/bdra.20386     Document Type: Article

References (103)

1. Akazawa S. 2005. Diabetic embryopathy: Studies using a rat embryo culture system and an animal model. Cong Anom 45:73-79.
2. Albina JE, Cui S, Mateo RB, et al. 1993. Nitric oxide-mediated apoptosis in murine peritoneal macrophages. J Immunol 150:5080-5085.
3. Alexander PG, Chau L, Tuan RS. 2002. Mechanisms of carbon monoxide-induced axial skeletal dysmorphogenesis in the chick embryo. Trans Orthop Res Soc 48:343.
4. Alexander PG, Tuan RS. 2003. Carbon monoxide-induced axial skeletal dysmorphogenesis in the chick embryo. Birth Defects Res A Clin Mol Teratol 67:219-230.
5. Barnes GL, Alexander PG, Hsu CW, et al. 1997. Cloning and characterization of chicken Paraxis: a regulator of paraxial mesoderm development and somite formation. Dev Biol 189:95-111.
6. Barnes GL, Hsu CW, Mariani BD, et al. 1996. Chicken Pax-1 gene: structure and expression during embryonic somite development. Differentiation 61:13-23.
7. Bishop A, Marquis JC, Cashman NR, et al. 1999. Adaptive resistance to nitric oxide in motor neurons. Free Radic Biol Med 26:978-986.
8. Bishop A, Yet SF, Lee ME, et al. 2004. A key role for heme oxygenase-1 in nitric oxide resistance in murine motor neurons and glia. Biochem Biophys Res Comm 325:3-9.
9. Blom HJ, Shaw GM, den Heijer M, et al. 2006. Neural tube defects and folate: case far from closed. Nature Rev 7:724-731.
10. Bogdan C. 2001a. Nitric oxide and the immune response. Nature Immunol 2:907-916.
11. Bogdan C. 2001b. Nitric oxide and the regulation of gene expression. Trends Cell Biol 11:66-75.
12. Bouton C, Demple B. 2000. Nitric oxide-inducible expression of heme oxygenase-1 in human cells. Translation-independent stabilization of the mRNA and evidence for direct action of nitric oxide. J Biol Chem 275:32688-32693.
13. Bredt DS, Snyder SH. 1994. Nitric oxide: a physiologic messenger molecule. Annu Rev Biochem 63:175-195.
14. Brune B, Sandau K, von Knethen A. 1998a. Apoptotic cell death and nitric oxide: activating and antagonistic transducing pathways. Biochemistry (Mosc) 63:817-825.
15. Brune B, von Knethen A, Sandau KW. 1998b. Nitric oxide and its role in apoptosis. Eur J Pharmacol 351:261-272.
16. Burdon RH. 1995. Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radic Biol Med 18:775-794.
17. Burgess R, Cserjesi P, Ligon KL, et al. 1995. Paraxis: a basic helix-loop-helix protein expressed in paraxial mesoderm and developing somites. Dev Biol 168:296-306.
18. Chen CM, Kraut N, Groudine M, et al. 1996. I-mf, a novel myogenic repressor, interacts with members of the MyoD family. Cell 86:731-741.
19. Chevallier A, Kieny M, Mauger A, et al. 1977. Developmental fate of the somitic mesoderm in the chick embryo. In: Ede DA, Hinchcliffe JR, Balls J, editors. Vertebrate Limb and Somite Morphogenesis. Cambridge: Cambridge University Press. pp. 421-432.
20. Christ B, Huang R, Wilting J. 2000. The development of the avian vertebral column. Anat Embryol (Berl) 202:179-194.
21. Christ B, Jacob HJ, Jacob M. 1977. Experimental analysis of the origin of the wing musculature in avian embryos. Anat Embryol (Berl) 150: 171-186.
22. Christ B, Schmidt C, Huang R, et al. 1998. Segmentation of the vertebrate body. Anat Embryol (Berl) 197:1-8.
23. Clavert A. 1970a. A few points on the nature of the normal development of ocular rudiment in rabbits. CR Assoc Anat 147:187-191.
24. Clavert A. 1970b. Studies of ocular abnormalities in the rabbit embryo induced by cyclophosphamide. Arch Anat Histol Embryol 53:209-271.
25. Clementi E, Nisoli E. 2005 Nitric oxide and mitochondrial biogenesis: a key to long-term regulation of cellular metabolism. Comp Biochem Physiol A Mol Integr Physiol 142:102-110.
26. Darley-Usmar V, Wiseman H, Halliwell B. 1995. Nitric oxide and oxygen radicals: a question of balance. FEBS Lett 369:131-135.
27. Diket AL, Pierce MR, Munshi UK, et al. 1994. Nitric oxide inhibition causes intrauterine growth retardation and hind-limb disruption in rats. Am J Obstet Gynecol 171:1243-1250.
28. Droge W. 2002. Free radicals in the physiological control of cell function. Physiol Rev 82:47-95.
29. Durante W, Christodoulides N, Cheng K, et al. 1997a. cAMP induces heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle. Am J Physiol 273:H317-H323.
30. Durante W, Kroll MH, Christodoulides N, et al. 1997b. Nitric oxide induces heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle cells. Circ Res 80:557-564.
31. Erenpreisa J, Freivalds T, Roach H, et al. 1997. Apoptotic cell nuclei favour aggregation and fluorescence quenching of DNA dyes. Histochem Cell Biol 108:67-75.
32. Fan CM, Tessier-Lavigne M. 1994. Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homolog. Cell 79:1175-1186.
33. Fantel AG, Person RE. 2002. Involvement of mitochondrial and other free radical sources in normal and abnormal fetal development. Ann NY Acad Sci 959:424-433.
34. Forstermann U, Boissel JP, Kleinert H. 1998. Expressional control of the 'constitutive' isoforms of nitric oxide synthase (NOS I and NOS III). FASEB J 12:773-790.
35. Forstermann U, Dun N. 1996. Immunohistochemical localization of nitric oxide synthases. Methods Enzymol 268:510-515.
36. Fridovich I. 1978. Superoxide radicals, superoxide dismutases and the aerobic lifestyle. Photochem Photobiol 28:733-741.
37. Friebe A, Schultz G, Koesling D. 1996. Sensitizing soluble guanylyl cyclase to become a highly CO-sensitive enzyme. EMBO J 15:6863-6868.
38. Fukuda N, Izumi Y, Soma M, et al. 1992. Effects of L-NG-monomethyl arginine on the cyclic GMP formations in rat mesenteric arteries. Jpn J Pharmacol 58:55-60.
39. Garthwaite J, Boulton CL. 1995. Nitric oxide signaling in the central nervous system. Annu Rev Physiol 57:683-706.
40. Gouge RC, Marshburn P, Gordon BE, et al. 1998. Nitric oxide as a regulator of embryonic development. Biol Reprod 58:875-879.
41. Grabowski CT. 1961. A quantitative study of the lethal and teratogenic effects of hypoxia on the three-day chick embryo. Am J Anat 109:25-35.
42. Griffith OW, Stuehr DJ. 1995. Nitric oxide synthases: properties and catalytic mechanism. Ann Rev Physiol 57:707-736.
43. Halliwell B, Gutteridge J. 1998. Free Radicals in Biology and Medicine. Oxford: Claredon Press.
44. Hamburger V, Hamilton H. 1951. A series of normal stages in the development of the chick embryo. J Morphol 88:49-92.
45. Hansen JM. 2006. Oxidative stress as a mechanism of teratogenesis. Birth Defects Res C Embryo Today 78:293-307.
46. Hara E, Takahashi K, Takeda K, et al. 1999. Induction of heme oxygenase-1 as a response in sensing the signals evoked by distinct nitric oxide donors. Biochem Pharmacol 58:227-236.
47. Hartsfield CL, Alam J, Cook JL, et al. 1997. Regulation of heme oxygenase-1 gene expression in vascular smooth muscle cells by nitric oxide. Am J Physiol 273:L980-988.
48. Hobel M, Kreye VA, Pill J. 1978. Effect of sodium nitroprusside alone and in combination with sodium thiosulfate on the acid-base balance, and on thiocyanate and iron plasma levels in the rabbit. Klin Wochenschr 56 Suppl 1:147-152.
49. Ignarro LJ, Buga GM, Wood KS, et al. 1987. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 84:9265-9269.
50. Irani K, Xia Y, Zweier JL, et al. 1997. Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 275:1649-1652.
51. Jacobsson C. 1997. Teratological studies on craniofacial malformations. Swed Dent J Suppl 121:3-84.
52. Jawerbaum A, Higa R, White V, et al. 2005. Peroxynitrates and impaired modulation of nitric oxide concentrations in embryos from diabetic rats during early organogenesis. Reproduction 130:695-703.
53. Johnson RL, Laufer E, Riddle RD, et al. 1994a. Ectopic expression of Sonic hedgehog alters dorsal-ventral patterning of somites. Cell 79:1165-1173.
54. Johnson RL, Riddle RD, Lafeur E, et al. 1994b. Sonic hedgehog: a key mediator of anteriorposterior patterning of the limb and dorso-ventral patterning of axial embryonic structures. Biochem Soc Trans 22:569-574.
55. Keyse SM, Tyrrell RM. 1989. Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci USA 86:99-103.
56. Kim YM, Bergonia H, Lancaster JR Jr. 1995. Nitrogen oxide-induced autoprotection in isolated rat hepatocytes. FEBS Lett 374:228-232.
57. Kitamura Y, Matsuoka Y, Nomora Y, et al. 1998. Induction of inducible nitric oxide synthase and heme oxygenase-1 in rat glial cells. Life Sci 62:1717-1721.
58. Kovacic P, Somanathan R. 2006. Mechanism of teratogenesis: Electron transfer, reactive oxygen species, and antioxidants. Birth Defects Res C Embryo Today 78:308-325.
59. Krumenacker JS, Katsuki S, Kots A, et al. 2006. Differential expression of genes involved in cGMP-dependent nitric oxide signaling in murine embryonic stem (ES) cells and ES-derived cardiomyocytes. Nitric Oxide 14:1-11.
60. Lee QP, Juchau MR. 1994. Dysmorphogenic effects of nitric oxide (NO) and NO-synthase inhibition: studies with intra-amniotic injections of sodium nitroprusside and Ngmonomethyl-L-arginine. Teratology 49:452-464.
61. Lee QP, Park HW, Thayer J, et al. 1996. Apoptosis induced in cultured rat embryos by intraamniotically microinjected sodium nitroprusside. Teratology 53:21-30.
62. Linker C, Lesbros C, Gros J, et al. 2005. p-Catenin-dependent Wnt signalling controls the epithelial organisation of somites through the activation of paraxis. Development 132:3895-3905.
63. Maines MD. 1996. Carbon monoxide and nitric oxide homology: differential modulation of heme oxygenases in brain and detection of protein and activity. Methods Enzymol 268:473-488.
64. Maines MD. 1997. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37:517-554.
65. Maines MD. 2005. The heme oxygenase system: update 2005. Antioxid Redox Signal 7:1761-1766.
66. Marquis JC, Demple B. 1998. Complex genetic response of human cells to sublethal levels of pure nitric oxide. Cancer Res 58:3435-3440.
67. McCord JM, Fridovich I. 1978. The biology and pathology of oxygen radicals. Ann Intern Med 89:122-127.
68. Meier S. 1979. Development of the chick embryo mesoblast. Formation of the embryonic axis and establishment of the metameric pattern. Dev Biol 73:24-45.
69. Moncada S, Palmer RM, Higgs EA. 1991. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43:109-142.
70. Monsoro-Burq AH. 2005. Sclerotome development and morphogenesis: when experimental embryology meets genetics. Int J Dev Biol 49:301-308.
71. Morbidelli L, Donnini S, Ziche M. 2003. Role of nitric oxide in the modulation of angiogenesis. Curr Pharmaceut Des 9:521-530.
72. Motterlini R, Foresti R, Intaglietta M, et al. 1996. NO-mediated activation of heme oxygenase: endogenous cytoprotection against oxidative stress to endothelium. Am J Physiol 270:H107-114.
73. Mungrue IN, Bredt DS, Stewart DJ, et al. 2003. From molecules to mammals: what's NOS got to do with it? Acta Physiol Scand 179:123-135.
74. Munsterberg AE, Kitajewski J, Bumcrot DA, et al. 1995. Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes Dev 9:2911-2922.
75. Murphy BJ, Laderoute KR, Short SM, et al. 1991. The identification of heme oxygenase as a major hypoxic stress protein in Chinese hamster ovary cells. Br J Cancer 64:69-73.
76. Nachmany A, Gold V, Tsur A, et al. 2006. Neural tube closure depends on nitric oxide synthase activity. J Neurochem 96:247-253.
77. Ordahl CP, Le Douarin NM. 1992. Two myogenic lineages within the developing somite. Development 114:339-353.
78. Packard DS Jr. 1976. The influence of axial structures on chick somite formation. Dev Biol 53:36-48.
79. Pae HO, Oh GS, Choi BM, et al. 2005. A molecular cascade showing nitric oxide-heme oxygenase-1-vascular endothelial growth factor-interleukin-8 sequence in human endothelial cells. Endocrinol 146:2229-2238.
80. Pelster B, Grillitsch S, Schwerte T. 2005. NO as a mediator during the early development of the cardiovascular system in the zebrafish. Comp Biochem Physiol Part A 142:215-220.
81. Poelmann RE, Gittenberger-de Groot AC. 2005. Apoptosis as an instrument in cardiovascular development. Birth Defects Res C Embryo Today 75:305-313.
82. Pourquie O. 2003. Vertebrate somitogenesis: a novel paradigm for animal segmentation? Int J Dev Biol 47:597-603.
83. Robertson CP, Gibbs SM, Roelink H. 2001. cGMP enhances the sonic hedgehog response in neural plates cells. Dev Biol 238:157-167.
84. Salas-Vidal E, Lomeli H, Castro-Obregon S, et al. 1998. Reactive oxygen species participate in the control of mouse embryonic cell death. Exp Cell Res 238:136-147.
85. Sarih M, Souvannavong V, Adam A. 1993. Nitric oxide synthase induces macrophage death by apoptosis. Biochem Biophys Res Comm 191: 503-508.
86. Saunders EL, Maines MD, Meredith MJ, et al. 1991. Enhancement of heme oxygenase-1 synthesis by glutathione depletion in Chinese hamster ovary cells. Arch Biochem Biophys 288:368-373.
87. Schulz V, Gross R, Pascht T, et al. 1982. Cyanide toxicity of sodium nitroprusside in therapeutic use with and without sodium thiosulphate. Klin Wochenschr 60:1393-1400.
88. Schulz V, Loeschcke G. 1985. Hypotensive efficacy of a mixed solution of 0.1% sodium nitroprusside and 1% sodium thiosulphate. J Hypertens 3:485-489.
89. Shibanuma M, Kuroki T, Nose K. 1988. Superoxide as a signal for increase in intracellular pH. J Cell Physiol 136:379-383.
90. Smith CA, Tuan RS. 1995. Functional involvement of Pax-1 in somite development: somite dysmorphogenesis in chick embryos treated with Pax-1 paired-box antisense oligodeoxynucleotide. Teratology 52:333-345.
91. Stern HM, Brown AM, Hauschka SD. 1995. Myogenesis in paraxial mesoderm: preferential induction by dorsal neural tube and by cells expressing Wnt-1. Development 121:3675-3686.
92. Takahashi K, Hara E, Suzuki H, et al. 1996. Expression of heme oxygenase isozyme mRNAs in the human brain and induction of heme oxygenase-1 by nitric oxide donors. J Neurochem 67:482-489.
93. Thompson CB. 1995. Apoptosis in the pathogenesis and treatment of disease. Science 267:1456-1462.
94. Tiboni GM, Clementini E. 2004. Teratological consequences of nitric oxide synthesis inhibition. Curr Pharmaceut Design 10:2759-2767.
95. Traister A, Abashidze S, Gold V, et al. 2002. Evidence that nitric oxide regulates cell cycle progression in the developing chick neurepithelium. Dev Dyn 225:271-276.
96. Traister A, Abashidze S, Gold V, et al. 2004. BMP controls nitric oxide-mediated regulation of cell numbers in the developing neural tube. Cell Death Differ 11:832-841.
97. Vesey CJ, Cole PV, Simpson PJ. 1976. Cyanide and thiocyanate concentrations following sodium nitroprusside infusion in man. Br J Anaesth 48:651-660.
98. Weil M, Abeles R, Nachmanny A, et al. 2004. Folic acid rescues nitric oxide-induced neural tube closure defects. Cell Death Diff 11:361-363.
99. Willis D, Tomlinson A, Frederick R, et al. 1995. Modulation of heme oxygenase activity in rat brain and spleen by inhibitors and donors of nitric oxide. Biochem Biophys Res Comm 214:1152-1156.
100. Wright JW, Schwinof KM, Snyder MA, et al. 1998. A delayed role for nitric oxide-sensitive guanylate cyclases in a migratory population of embryonic neurons. Dev Biol 204:15-33.
101. Wu L, Wang R. 2005. Carbon monoxide: endogenous production, physiological functions, and pharmacological applications. Pharmacol Rev 57:585-630.
102. Yet SF, Pellacani A, Patterson C, et al. 1997. Induction of heme oxygenase-1 expression in vascular smooth muscle cells. A link to endotoxic shock. J Biol Chem 272:4295-4301.
103. Zweiman B, Slavin RG, Feinberg RJ, et al. 1972. Effects of air pollution on asthma: a review. J Allergy Clin Immunol 50:305-314.