Impairment of nitrergic system and delayed gastric emptying in low density lipoprotein receptor deficient female mice

Neurogastroenterology and Motility

Volumn 23, Issue 8, 2011, Pages

  Gangula, P R ^a,b   Chinnathambi, V ^a   Hale, A B ^b   Mukhopadhyay, S ^a   Channon, K M ^b   Ravella, K ^a  

^a MEHARRY MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Gastroparesis; Low density lipoprotein receptor knockout mice; Nitrergic relaxation; NNOS dimerization; Nrf2; Sepiapterin

Indexed keywords

BIOPTERIN; ESTRONE GLUCURONIDE; GLUCOSE; LOW DENSITY LIPOPROTEIN RECEPTOR; SEPIAPTERIN; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL MIGRATION; CONTROLLED STUDY; DIET RESTRICTION; DIMERIZATION; FEMALE; GASTROINTESTINAL TRANSIT; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INTESTINE MOTILITY; KNOCKOUT MOUSE; MORNING DOSAGE; MOUSE; NITRERGIC NERVE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PYLORUS; SMALL INTESTINE; STOMACH EMPTYING; STOMACH FUNDUS; STOMACH PARESIS; TREATMENT DURATION; WILD TYPE;

ANIMALS; ANTIOXIDANTS; BIOPTERIN; BLOOD GLUCOSE; BODY WEIGHT; FEMALE; GASTRIC EMPTYING; GASTROINTESTINAL MOTILITY; GASTROPARESIS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; OXIDATIVE STRESS; PTERINS; RECEPTORS, LDL;

EID: 79960423790     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2011.01695.x     Document Type: Article

References (38)

1. Schreyer SA, Vick C, Lystig TC, Mystkowski P, Leboeuf REC. LDL receptor but not apolipoprotein E deficiency increases diet-induced obesity and diabetes in mice. Am J Physiol Endocrinol Metab 2002; 282: E207-14.
2. Brown MS, Goldstein JL. A receptor-mediated pathway for cholesterol homeostasis. Science (Washington DC) 1986; 232: 34-47.
3. Ishibashi S, Brown MS, Goldstein JL, Gerard RD, Hammer RE, Herz J. Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J Clin Invest 1993; 92: 883-93.
4. Knowles JW, Maeda N. Genetic modifiers of atherosclerosis in mice. Arterioscler Thromb Vasc Biol 2000; 20: 2336-45.
5. Xiea W, Xingb D, Zhaob Y et al. A new tactic to treat postprandial hyperlipidemia in diabetic rats with gastroparesis by improving gastrointestinal transit. European J Pharmacol 2005; 510: 113-20.
6. Soykan I, Sivri B, Sarosiek I, Kiernan B, McCallum RW. Demography, clinical characteristics, psychological and abuse profiles, treatment, and long-term follow-up of patients with gastroparesis. Dig Dis Sci 1998; 43: 2398-404.
7. Chandrasekharan B, Srinivasan S. Diabetes and the enteric nervous system. Neurogastroenterol Motil 2007; 19: 951-60.
8. Huang PL, Dawson TM, Bredt DS, Snyder SH, Fishman MC. Targeted disruption of the neuronal nitric oxide synthase gene. Cell 1993; 75: 1273-86.
9. Mashimo H, Kjellin A, Goyal RK. Gastric stasis in neuronal nitric oxide synthase-deficient knockout mice. Gastroenterology 2000; 119: 766-73.
10. Klatt P, Pfeiffer S, List BM et al. Characterization of heme-deficient neuronal nitric-oxide synthase reveals a role for heme in subunit dimerization and binding of the amino acid substrate and tetrahydrobiopterin. J Biol Chem 1996; 271: 7336-42.
11. Crane BR, Arvai AS, Ghosh DK et al. Structure of nitric oxide synthase oxygenase dimer with pterin and substrate. Science 1998; 279: 2121-6.
12. Vasquez-Vivar J, Hogg N, Martasek P, Karoui H, Pritchard KA Jr, Kalyanaraman B. Tetrahydrobiopterin-dependent inhibition of superoxide generation from neuronal nitric oxide synthase. J Biol Chem 1999; 274: 26736-42.
13. Gangula PR, Maner WL, Micci MA, Garfield RE, Pasricha PJ. Diabetes induces sex-dependent changes in neuronal nitric oxide synthase dimerization and function in the rat gastric antrum. Am J Physiol Gastrointest Liver Physiol 2007; 292: G725-33.
14. Gangula PR, Mukhopadhyay S, Ravella K et al. Tetrahydrobiopterin (BH4), a cofactor for nNOS, restores gastric emptying and nNOS expression in female diabetic rats. Am J Physiol Gastrointest Liver Physiol 2010; 298: G692-9.
15. Lee JM, Li J, Johnson DA et al. Nrf2, a multi-organ protector? FASEB J 2005; 19: 1061-6.
16. Aleksunes LM, Manautou JE. Emerging role of Nrf2 in protecting against hepatic and gastrointestinal disease. Toxicol Pathol 2007; 35: 459-73.
17. Kalthoff S, Ehmer U, Freiberg N, Manns MP, Strassburg CP. Interaction between oxidative stress sensor Nrf2 and xenobiotic-activated aryl hydrocarbon receptor in the regulation of the human phase II detoxifying UDP-glucuronosyltransferase 1A10. J Biol Chem 2010; 285: 5993-6002.
18. Shibuya A, Onda K, Kawahara H et al. Sofalcone, a gastric mucosa protective agent, increases vascular endothelial growth factor via the Nrf2-heme-oxygenase-1 dependent pathway in gastric epithelial cells. Biochem Biophys Res Commun 2010; 398: 581-4.
19. Iwasaki T, Takahashi S, Takahashi M et al. Deficiency of the very low-density lipoprotein (VLDL) receptors in streptozotocin-induced diabetic rats: insulin dependency of the VLDL receptor. Endocrinology 2005; 146: 3286-94.
20. Keren P, George J, Shaish A et al. Effect of hyperglycemia and hyperlipidemia on atherosclerosis in LDL receptor-deficient mice: establishment of a combined model and association with heat shock protein 65 immunity. Diabetes 2000; 49: 1064-9.
21. Vikramadithyan RK, Hu Y, Noh HL et al. Human aldose reductase expression accelerates diabetic atherosclerosis in transgenic mice. J Clin Invest 2005; 115: 2434-43.
22. Pannirselvam M, Simon V, Verma S, Anderson T, Triggle CR. Chronic oral supplementation with sepiapterin prevents endothelial dysfunction and oxidative stress in small mesenteric arteries from diabetic (db/db) mice. Br J Pharmacol 2003; 140: 701-6.
23. Gangula PR, Mukhopadhyay S, Pasricha PJ, Ravella K. Sepiapterin reverse the changes in gastric nNOS dimerization and function in diabetic gastroparesis. Neurogastroenterol Motil 2010; 22: 1325-31.
24. Li ZS, Schmauss C, Cuenca A, Ratcliffe E, Gershon MD. Physiological modulation of intestinal motility by enteric dopaminergic neurons and the D2 receptor: analysis of dopamine receptor expression, location, development, and function in wild-type and knock-out mice. J Neurosci 2006; 26: 2798-807.
25. Anitha M, Chandrasekharan B, Salgado JR et al. Glial-derived neurotrophic factor modulates enteric neuronal survival and proliferation through neuropeptide Y. Gastroenterology 2006; 131: 1164-78.
26. Anitha M, Gondha C, Sutliff R et al. GDNF rescues hyperglycemia-induced diabetic enteric neuropathy through activation of the PI3K/Akt pathway. J Clin Invest 2006; 116: 344-56.
27. Crabtree M. J., Tatham A. L., Al-Wakeel Y. et al. Quantitative regulation of intracellular endothelial nitric-oxide synthase (eNOS) coupling by both tetrahydrobiopterin-eNOS stoichiometry and biopterin redox status: insights from cells with tet-regulated GTP cyclohydrolase I expression. J Biol Chem 2009; 284: 1136-44.
28. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 2007; 87: 315-424.
29. Tayeh MA, Marletta MA. Macrophage oxidation of L-arginine to nitric oxide, nitrite, and nitrate: tetrahydrobiopterin is required as a cofactor. J Biol Chem 1989; 264: 19654-8.
30. Pall ML. Nitric oxide synthase partial uncoupling as a key switching mechanism for the NO/ONOO- cycle. Med Hypotheses 2007; 69: 821-5.
31. Takeda M, Yamashita T, Shinohara M et al. Plasma tetrahydrobiopterin/dihydrobiopterin ratio: a possible marker of endothelial dysfunction. Circ J 2009; 73: 955-62.
32. Crabtree MJ, Tatham AL, Hale AB, Alp NJ, Channon KM. Critical role for tetrahydrobiopterin recycling by dihydrofolate reductase in regulation of endothelial nitric-oxide synthase coupling: relative importance of the de novo biopterin synthesis vs salvage pathways. J Biol Chem 2009; 284: 28128-36.
33. Tanaka Y, Aleksunes LM, Yeager RL et al. NF-E2-related factor 2 inhibits lipid accumulation and oxidative stress in mice fed a high-fat diet. J Pharmacol Exp Ther 2008; 325: 655-64.
34. Choi KM, Gibbons SJ, Nguyen TV et al. Heme oxygenase-1 protects interstitial cells of Cajal from oxidative stress and reverses diabetic gastroparesis. Gastroenterology 2008; 135: 2055-64.
35. Choi KM, Kashyap PC, Dutta N et al. CD206-positive M2 macrophages that express heme oxygenase-1 protect against diabetic gastroparesis in mice. Gastroenterology 2010; 138: 2399-409.
36. Parkman HP, Yates K, Hasler WL et al. Clinical features of idiopathic gastroparesis vary with sex, body mass, symptom onset, delay in gastroparesis, and gastroparesis severity. Gastroenterol 2011: 140: 101-15.
37. Farrugia G. Interstitial cells of Cajal in health and disease. Neurogastroenterol Motil 2008; 20: 54-63.
38. Kashyap P, Farrugia G. Oxidative stress: key player in gastrointestinal complications of diabetes. Neurogastroenterol Motil 2011; 23: 111-4.