Colonic motor dysfunction in human diabetes is associated with enteric neuronal loss and increased oxidative stress

Neurogastroenterology and Motility

Volumn 23, Issue 2, 2011, Pages

  Chandrasekharan, B ^a   Anitha, M ^a   Blatt, R ^a   Shahnavaz, N ^a   Kooby, D ^a   Staley, C ^a   Mwangi, S ^a   Jones, D P ^b   Sitaraman, S V ^a   Srinivasan, S ^a,c  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c ATLANTA VA MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Diabetes; Enteric neurons; Motility; Oxidative stress

Indexed keywords

CASPASE 3; CHOLINE ACETYLTRANSFERASE; GENE PRODUCT; GLUTATHIONE; NEURONAL NITRIC OXIDE SYNTHASE; NEUROPEPTIDE Y; PERIPHERIN; PHOSPHATIDYLINOSITOL 3 KINASE; SUPEROXIDE DISMUTASE; THIOCTIC ACID; VASOACTIVE INTESTINAL POLYPEPTIDE;

ADULT; AGED; ANIMAL CELL; APOPTOSIS; ARTICLE; CLINICAL ARTICLE; CONSTIPATION; CONTROLLED STUDY; DIABETES MELLITUS; DIARRHEA; FEMALE; GANGLION; GENE EXPRESSION; HUMAN; HUMAN TISSUE; HYPERGLYCEMIA; INTESTINAL DYSMOTILITY; INTESTINE CONTRACTION; INTESTINE INNERVATION; MALE; MOUSE; MUSCLE EXCITATION; MUSCLE ISOMETRIC CONTRACTION; NERVE CELL NECROSIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE RELAXATION;

AGED; ANIMALS; ANTIOXIDANTS; APOPTOSIS; BIOPSY; CASE-CONTROL STUDIES; CELL LINE; COLON; DIABETES COMPLICATIONS; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; ENTERIC NERVOUS SYSTEM; FEMALE; GASTROINTESTINAL DISEASES; HUMANS; MALE; MICE; MIDDLE AGED; MUSCLE CONTRACTION; MUSCLE RELAXATION; OXIDATIVE STRESS; PHOSPHATIDYLINOSITOL 3-KINASES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; THIOCTIC ACID;

EID: 78651419160     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2010.01611.x     Document Type: Article

References (33)

1. Lomax AE, Sharkey KA, Furness JB. The participation of the sympathetic innervation of the gastrointestinal tract in disease states. Neurogastroenterol Motil 2010; 22: 7-18.
2. Bytzer P, Talley NJ, Leemon M, Young LJ, Jones MP, Horowitz M. Prevalence of gastrointestinal symptoms associated with diabetes mellitus: a population-based survey of 15, 000 adults. Arch Intern Med 2001; 161: 1989-96.
3. Samsom M, Vermeijden JR, Smout AJ et al. Prevalence of delayed gastric emptying in diabetic patients and relationship to dyspeptic symptoms: a prospective study in unselected diabetic patients. Diabetes Care 2003; 26: 3116-22.
4. Feldman M, Schiller LR. Disorders of gastrointestinal motility associated with diabetes mellitus. Ann Intern Med 1983; 98: 378-84.
5. Camilleri M. Gastrointestinal problems in diabetes. Endocrinol Metab Clin North Am 1996; 25: 361-78.
6. Coyle JT, Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders. Science 1993; 262: 689-95.
7. Nishikawa T, Edelstein D, Du XL et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000; 404: 787-90.
8. Ceriello A, Mercuri F, Quagliaro L et al. Detection of nitrotyrosine in the diabetic plasma: evidence of oxidative stress. Diabetologia 2001; 44: 834-8.
9. Rosen P, Nawroth PP, King G, Moller W, Tritschler HJ, Packer L. The role of oxidative stress in the onset and progression of diabetes and its complications: a summary of a Congress Series sponsored by UNESCO-MCBN, the American Diabetes Association and the German Diabetes Society. Diabetes Metab Res Rev 2001; 17: 189-212.
10. Abdo H, Derkinderen P, Gomes P et al. Enteric glial cells protect neurons from oxidative stress in part via reduced glutathione. FASEB J 2009; 24: 1082-94.
11. Harrison JF, Hollensworth SB, Spitz DR, Copeland WC, Wilson GL, LeDoux SP. Oxidative stress-induced apoptosis in neurons correlates with mitochondrial DNA base excision repair pathway imbalance. Nucleic Acids Res 2005; 33: 4660-71.
12. Noda K, Umeda F, Ono H et al. Decreased VIP content in peripheral nerve from streptozocin-induced diabetic rats. Diabetes 1990; 39: 608-12.
13. Yu WJ, Juang SW, Chin WT, Chi TC, Chang CJ, Cheng JT. Insulin restores neuronal nitric oxide synthase expression in streptozotocin-induced diabetic rats. Life Sci 2000; 68: 625-34.
14. Adeghate E, al-Ramadi B, Saleh AM et al. Increase in neuronal nitric oxide synthase content of the gastroduodenal tract of diabetic rats. Cell Mol Life Sci 2003; 60: 1172-9.
15. Koo JR, Vaziri ND. Effects of diabetes, insulin and antioxidants on NO synthase abundance and NO interaction with reactive oxygen species. Kidney Int 2003; 63: 195-201.
16. Shen WZ, Lin HS, Guo GQ. Changes of neuronal nitric oxide synthase-immunoreactive neurons in the paraventricular hypothalamic nucleus of diabetic rats. Di Yi Jun Yi Da Xue Xue Bao 2003; 23: 692-5.
17. Iwasaki H, Kajimura M, Osawa S et al. A deficiency of gastric interstitial cells of Cajal accompanied by decreased expression of neuronal nitric oxide synthase and substance P in patients with type 2 diabetes mellitus. J Gastroenterol 2006; 41: 1076-87.
18. 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, 2064 e2051-2052.
19. Herman WH, Fajans SS. Hemoglobin A1c for the diagnosis of diabetes: practical considerations. Pol Arch Med Wewn 2010; 120: 37-40.
20. Anitha M, Joseph I, Ding X et al. Characterization of fetal and postnatal enteric neuronal cell lines with improvement in intestinal neural function. Gastroenterology 2008; 134: 1424-35.
21. Jones DP, Mody VC Jr, Carlson JL, Lynn MJ, Sternberg P Jr. Redox analysis of human plasma allows separation of pro-oxidant events of aging from decline in antioxidant defenses. Free Radic Biol Med 2002; 33: 1290-300.
22. Chandrasekharan BP, Kolachala VL, Dalmasso G et al. Adenosine 2B receptors (A(2B)AR) on enteric neurons regulate murine distal colonic motility. FASEB J 2009; 23: 2727-34.
23. Bredt DS, Hwang PM, Snyder SH. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 1990; 347: 768-70.
24. Bult H, Boeckxstaens GE, Pelckmans PA, Jordaens FH, Van Maercke YM, Herman AG. Nitric oxide as an inhibitory non-adrenergic non-cholinergic neurotransmitter. Nature 1990; 345: 346-7.
25. Boeckxstaens GE, Pelckmans PA, Bult H, De Man JG, Herman AG, van Maercke YM. Evidence for nitric oxide as mediator of non-adrenergic non-cholinergic relaxations induced by ATP and GABA in the canine gut. Br J Pharmacol 1991; 102: 434-8.
26. Cox HM. Neuropeptide Y receptors; antisecretory control of intestinal epithelial function. Auton Neurosci 2007; 133: 76-85.
27. Meister A, Anderson ME. Glutathione. Annu Rev Biochem 1983; 52: 711-60.
28. 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.
29. Ametov AS, Barinov A, Dyck PJ et al. The sensory symptoms of diabetic polyneuropathy are improved with alpha-lipoic acid: the SYDNEY trial. Diabetes Care 2003; 26: 770-6.
30. Brownlee M, Cerami A, Vlassara H. Advanced glycosylation end products in tissue and the biochemical basis of diabetic complications. N Engl J Med 1988; 318: 1315-21.
31. Wrzos HF, Cruz A, Polavarapu R, Shearer D, Ouyang A. Nitric oxide synthase (NOS) expression in the myenteric plexus of streptozotocin-diabetic rats. Dig Dis Sci 1997; 42: 2106-10.
32. Spangeus A, El-Salhy M. Myenteric plexus of obese diabetic mice (an animal model of human type 2 diabetes). Histol Histopathol 2001; 16: 159-65.
33. Chandrasekharan B, Srinivasan S. Diabetes and the enteric nervous system. Neurogastroenterol Motil 2007; 19: 951-60.