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

Journal of Gastroenterology

Volumn 41, Issue 11, 2006, Pages 1076-1087

  Iwasaki, Hirohiko ^a   Kajimura, Masayoshi ^a   Osawa, Satoshi ^a   Kanaoka, Shigeru ^a   Furuta, Takahisa ^a   Ikuma, Mutsuhiro ^a   Hishida, Akira ^a  

^a HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Diabetes mellitus; Interstitial cells of Cajal; Neuronalnitric oxide synthase; Stomach; Substance P

Indexed keywords

NEURONAL NITRIC OXIDE SYNTHASE; PARAFFIN; SUBSTANCE P;

ARTICLE; CELL COUNT; CELL DENSITY; CELL FUNCTION; CLINICAL ARTICLE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; FEMALE; GASTRECTOMY; GASTROINTESTINAL MOTILITY DISORDER; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INTERSTITIAL CELL OF CAJAL; MALE; MYENTERIC PLEXUS; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH ANTRUM; STOMACH CANCER; STOMACH PARESIS;

BIOLOGICAL MARKERS; CELL COUNT; DIABETES MELLITUS, TYPE 2; FEMALE; GASTRIC EMPTYING; GASTRIC MUCOSA; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, CONFOCAL; MYENTERIC PLEXUS; NEURONS; NITRIC OXIDE SYNTHASE TYPE I; RETROSPECTIVE STUDIES; SUBSTANCE P;

EID: 33845420362     PISSN: 09441174     EISSN: 14355922     Source Type: Journal    
DOI: 10.1007/s00535-006-1909-8     Document Type: Article

References (43)

1. G Bassotti 1991 Diabetes and gastrointestinal motor activity Recenti Prog Med 82 334-7 1:STN:280:By2D387nsVA%3D 1924990
2. P Bytzer NJ Talley M Leemon LJ Young MP Jones M Horowitz 2001 Prevalence of gastrointestinal symptoms associated with diabetes mellitus: A population-based survey of 15,000 adults Arch Intern Med 161 1989-96 10.1001/archinte.161.16.1989 1:STN:280:DC%2BD3Mrit1ylsA%3D%3D 11525701
3. M Samsom JR Vermeijden AJ Smout E Van Doorn J Roelofs PS Van Dam 2003 Prevalence of delayed gastric emptying in diabetic patients and relationship to dyspeptic symptoms: A prospective study in unselected diabetic patients Diabetes Care 26 3116-22 1:STN:280:DC%2BD3srivVejtA%3D%3D 14578248
4. KM Sanders SD Koh SM Ward 2006 Interstitial cells of Cajal as pacemakers in the gastrointestinal tract Annu Rev Physiol 68 307-43 10.1146/ annurev.physiol.68.040504.094718 1:CAS:528:DC%2BD28XksFWks74%3D 16460275
5. J Forster I Damjanov Z Lin I Sarosiek P Wetzel RW McCallum 2005 Absence of the interstitial cells of Cajal in patients with gastroparesis and correlation with clinical findings J Gastrointest Surg 9 102-8 10.1016/ j.gassur.2004.10.001 15623450
6. T Wedel J Spiegler S Soellner UJ Roblick TH Schiedeck HP Bruch 2002 Enteric nerves and interstitial cells of Cajal are altered in patients with slow-transit constipation and megacolon Gastroenterology 123 1459-67 10.1053/gast.2002.36600 12404220
7. CL He L Burgart L Wang J Pemberton T Young-Fadok J Szurszewski 2000 Decreased interstitial cell of Cajal volume in patients with slow-transit constipation Gastroenterology 118 14-21 10.1016/ S0016-5085(00)70409-4 1:STN:280:DC%2BD3c%2FnvFWitw%3D%3D 10611149
8. GL Lyford CL He E Soffer TL Hull SA Strong AJ Senagore 2002 Pan-colonic decrease in interstitial cells of Cajal in patients with slow transit constipation Gut 51 496-501 10.1136/gut.51.4.496 1:STN:280:DC%2BD38vpvFSqsQ%3D%3D 12235070
9. JM Vanderwinden H Liu MH De Laet JJ Vanderhaeghen 1996 Study of the interstitial cells of Cajal in infantile hypertrophic pyloric stenosis Gastroenterology 111 279-88 10.1053/gast.1996.v111.pm8690192 1:STN:280:BymA3crgvFE%3D 8690192
10. AP Piotrowska V Solari P Puri 2003 Distribution of heme oxygenase-2 in nerves and interstitial cells of Cajal in the normal pylorus and in infantile hypertrophic pyloric stenosis Arch Pathol Lab Med 127 1182-6 12946226
11. JM Vanderwinden JJ Rumessen H Liu D Descamps MH De Laet JJ Vanderhaeghen 1996 Interstitial cells of Cajal in human colon and in Hirschsprung's disease Gastroenterology 111 901-10 10.1016/S0016-5085(96)70057-4 1:STN:280:BymH38fkvVU%3D 8831584
12. AP Piotrowska V Solari D de Caluwe P Puri 2003 Immunocolocalization of the heme oxygenase-2 and interstitial cells of Cajal in normal and aganglionic colon J Pediatr Surg 38 73-7 10.1053/jpsu.2003.50014 12592623
13. JJ Rumessen 1996 Ultrastructure of interstitial cells of Cajal at the colonic submuscular border in patients with ulcerative colitis Gastroenterology 111 1447-55 10.1016/S0016-5085(96)70005-7 1:STN:280:ByiD1MfhvVU%3D 8942722
14. C Porcher M Baldo M Henry P Orsoni Y Jule SM Ward 2002 Deficiency of interstitial cells of Cajal in the small intestine of patients with Crohn's disease Am J Gastroenterol 97 118-25 10.1111/ j.1572-0241.2002.05430.x 11808934
15. T Ordog I Takayama WK Cheung SM Ward KM Sanders 2000 Remodeling of networks of interstitial cells of Cajal in a murine model of diabetic gastroparesis Diabetes 49 1731-9 1:CAS:528:DC%2BD3cXntVyht70%3D 11016458
16. QL Long DC Fang HT Shi YH Luo 2004 Gastro-electric dysrhythm and lack of gastric interstitial cells of Cajal World J Gastroenterol 10 1227-30 15069732
17. CL He EE Soffer CD Ferris RM Walsh JH Szurszewski G Farrugia 2001 Loss of interstitial cells of Cajal and inhibitory innervation in insulin-dependent diabetes Gastroenterology 121 427-34 10.1053/ gast.2001.26264 1:STN:280:DC%2BD3MvktFGmsA%3D%3D 11487552
18. M Nakahara K Isozaki S Hirota JM Vanderwinden R Takakura K Kinoshita 2002 Deficiency of KIT-positive cells in the colon of patients with diabetes mellitus J Gastroenterol Hepatol 17 666-70 10.1046/ j.1440-1746.2002.02756.x 12100611
19. A Epperson WJ Hatton B Callaghan P Doherty RL Walker KM Sanders 2000 Molecular markers expressed in cultured and freshly isolated interstitial cells of Cajal Am J Physiol Cell Physiol 279 C529-39 1:CAS:528:DC%2BD3cXmtFyjsbc%3D 10913020
20. S Iino SM Ward KM Sanders 2004 Interstitial cells of Cajal are functionally innervated by excitatory motor neurones in the murine intestine J Physiol 556 521-30 10.1113/jphysiol.2003.058792 1:CAS:528:DC%2BD2cXjslKjsbw%3D 14754997
21. VC Smith MA Sagot H Wong AM Buchan 2000 Cellular expression of the neurokinin 1 receptor in the human antrum J Auton Nerv Syst 79 165-72 10.1016/S0165-1838(99)00092-2 1:CAS:528:DC%2BD3cXhsVagsrs%3D 10699648
22. EE Colpaert JP Timmermans RA Lefebvre 2002 Immunohistochemical localization of the antioxidant enzymes biliverdin reductase and heme oxygenase-2 in human and pig gastric fundus Free Radic Biol Med 32 630-7 10.1016/S0891-5849(02)00754-2 1:CAS:528:DC%2BD38XitFWlsbY%3D 11909697
23. K Horiguchi KM Sanders SM Ward 2003 Enteric motor neurons form synaptic-like junctions with interstitial cells of Cajal in the canine gastric antrum Cell Tissue Res 311 299-313 12658438
24. SM Ward G Morris L Reese XY Wang KM Sanders 1998 Interstitial cells of Cajal mediate enteric inhibitory neurotransmission in the lower esophageal and pyloric sphincters Gastroenterology 115 314-29 10.1016/ S0016-5085(98)70198-2 1:STN:280:DyaK1czktl2rtw%3D%3D 9679037
25. SM Ward EA Beckett X Wang F Baker M Khoyi KM Sanders 2000 Interstitial cells of Cajal mediate cholinergic neurotransmission from enteric motor neurons J Neurosci 20 1393-403 1:CAS:528:DC%2BD3cXitVOktbc%3D 10662830
26. J Glatzle C Sternini C Robin TT Zittel H Wong JR Reeve 2002 Expression of 5-HT3 receptors in the rat gastrointestinal tract Gastroenterology 123 217-26 10.1053/gast.2002.34245 1:CAS:528:DC%2BD38Xmt1ahsrs%3D 12105850
27. MG Vannucchi L Corsani MS Faussone-Pellegrini 1999 Substance P immunoreactive nerves and interstitial cells of Cajal in the rat and guinea-pig ileum. A histochemical and quantitative study Neurosci Lett 268 49-52 10.1016/S0304-3940(99)00366-3 1:CAS:528:DyaK1MXjs1Sgt7o%3D 10400075
28. CC Watkins A Sawa S Jaffrey S Blackshaw RK Barrow SH Snyder 2000 Insulin restores neuronal nitric oxide synthase expression and function that is lost in diabetic gastropathy J Clin Invest 106 373-84 1:CAS:528:DC%2BD3cXlsFOrtLo%3D 10930440
29. WJ Yu SW Juang WT Chin TC Chi CJ Chang JT Cheng 2000 Insulin restores neuronal nitric oxide synthase expression in streptozotocin-induced diabetic rats Life Sci 68 625-34 10.1016/S0024-3205(00)00967-X 1:CAS:528:DC%2BD3MXjtVSjsA%3D%3D 11205877
30. T Takahashi K Nakamura H Itoh AA Sima C Owyang 1997 Impaired expression of nitric oxide synthase in the gastric myenteric plexus of spontaneously diabetic rats Gastroenterology 113 1535-44 10.1053/ gast.1997.v113.pm9352855 1:CAS:528:DyaK2sXnt1OlsL4%3D 9352855
31. S Cellek NA Foxwell S Moncada 2003 Two phases of nitrergic neuropathy in streptozotocin-induced diabetic rats Diabetes 52 2353-62 1:CAS:528:DC%2BD3sXntFequro%3D 12941776
32. AU Zaidi H Enomoto J Milbrandt KA Roth 2000 Dual fluorescent in situ hybridization and immunohistochemical detection with tyramide signal amplification J Histochem Cytochem 48 1369-75 1:CAS:528:DC%2BD3cXmvVyrt7c%3D 10990490
33. VJ Horvath H Vittal T Ordog 2005 Reduced insulin and IGF-I signaling, not hyperglycemia, underlies the diabetes-associated depletion of interstitial cells of Cajal in the murine stomach Diabetes 54 1528-33 1:CAS:528:DC%2BD2MXktVCksbY%3D 15855342
34. VJ Horvath H Vittal A Lorincz H Chen G Almeida-Porada D Redelman 2006 Reduced stem cell factor links smooth myopathy and loss of interstitial cells of Cajal in murine diabetic gastroparesis Gastroenterology 130 759-70 10.1053/j.gastro.2005.12.027 1:CAS:528:DC%2BD28XjsVyltr4%3D 16530517
35. M El-Salhy A Spangeus 1998 Substance P in the gastrointestinal tract of non-obese diabetic mice Scand J Gastroenterol 33 394-400 10.1080/ 00365529850171026 1:CAS:528:DyaK1cXjtVars7g%3D 9605261
36. M El-Salhy 1998 Neuroendocrine peptides of the gastrointestinal tract of an animal model of human type 2 diabetes mellitus Acta Diabetol 35 194-8 10.1007/s005920050130 1:CAS:528:DyaK1MXkvFKqtw%3D%3D 9934817
37. SM Ward T Ordog JR Bayguinov B Horowitz A Epperson L Shen 1999 Development of interstitial cells of Cajal and pacemaking in mice lacking enteric nerves Gastroenterology 117 584-94 10.1016/ S0016-5085(99)70451-8 1:STN:280:DyaK1MzpsV2qsQ%3D%3D 10464134
38. V Stanghellini 1999 Three-month prevalence rates of gastrointestinal symptoms and the influence of demographic factors: Results from the Domestic/International Gastroenterology Surveillance Study (DIGEST) Scand J Gastroenterol Suppl 231 20-8 10.1080/003655299750025237 1:STN:280:DC%2BD3c%2FivFemsg%3D%3D 10565620
39. EA Mayer B Naliboff O Lee J Munakata L Chang 1999 Review article: gender-related differences in functional gastrointestinal disorders Aliment Pharmacol Ther 13 Suppl 2 65-9 10.1046/j.1365-2036.1999.00008.x 10429743
40. L Chang 2004 Review article: Epidemiology and quality of life in functional gastrointestinal disorders Aliment Pharmacol Ther 20 Suppl 7 31-9 10.1111/j.1365-2036.2004.02183.x 1:CAS:528:DC%2BD2cXnsVehtg%3D%3D 15521853
41. OY Lee EA Mayer M Schmulson L Chang B Naliboff 2001 Gender-related differences in IBS symptoms Am J Gastroenterol 96 2184-93 10.1111/ j.1572-0241.2001.03961.x 1:STN:280:DC%2BD3MvhvFejsg%3D%3D 11467651
42. L Chang MM Heitkemper 2002 Gender differences in irritable bowel syndrome Gastroenterology 123 1686-701 10.1053/gast.2002.36603 12404243
43. ZL Xiao V Pricolo P Biancani J Behar 2005 Role of progesterone signaling in the regulation of G-protein levels in female chronic constipation Gastroenterology 128 667-75 10.1053/j.gastro.2004.12.001 1:CAS:528:DC%2BD2MXivFWntLo%3D 15765402