Differential gene expression in functional classes of interstitial cells of Cajal in murine small intestine

Physiological Genomics

Volumn 31, Issue 3, 2007, Pages 492-509

  Chen, Hui ^a   Ördög, Tamás ^a   Chen, Junwei ^a   Young, David L ^a   Bardsley, Michael R ^a   Redelman, Doug ^a,b,c   Ward, Sean M ^a   Sanders, Kenton M ^a  

^a UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NEVADA   (United States)

^c Sierra Cytometry   (United States)

Author keywords

Affymetrix Mouse Genome 430.2 geneChips; Bioconductor; Enteric nervous system; Ion channel; Signal transduction

Indexed keywords

CALCIUM ION; NEUROTRANSMITTER;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL ISOLATION; CELL JUNCTION; CELL VACUOLE; CONTROLLED STUDY; DNA MICROARRAY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; INTERSTITIAL CELL OF CAJAL; INTESTINE MUSCLE; METABOLISM; MICROARRAY ANALYSIS; MOUSE; NEUROTRANSMISSION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SMALL INTESTINE; TRANSCRIPTOMICS; UPREGULATION;

ANIMALS; COILED BODIES; GENE EXPRESSION PROFILING; INTESTINE, SMALL; MICE; SYNAPTIC TRANSMISSION;

MURINAE;

EID: 36248984347     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00113.2007     Document Type: Article

References (66)

1. Baluk P, Gabella G. Scanning electron microscopy of the muscle coat of the guinea-pig small intestine. Cell Tissue Res 250: 551-561, 1987.
2. Beckett EA, Takeda Y, Yanase H, Sanders KM, Ward SM. Synaptic specializations exist between enteric motor nerves and interstitial cells of Cajal in the murine stomach. J Comp Neurol 493: 193-206, 2005.
3. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statist Soc B 57: 289-300, 1995.
4. 2+ exchange to spontaneous activity in interstitial cells of Cajal in the rabbit urethra. J Physiol 574: 651-661, 2006.
5. Burns AJ, Lomax AEJ, Torihashi S, Sanders KM, Ward SM. Interstitial cells of Cajal mediate inhibitory neurotransmission in the stomach. Proc Natl Acad Sci USA 93: 12008-12013, 1996.
6. Carson WE, Haldar S, Baiocchi RA, Croce CM, Caligiuri MA. The Kit ligand suppresses apoptosis of human natural killer cells through the upregulation of bcl-2. Proc Natl Acad Sci USA 91: 7553-7557, 1994.
7. Chen H, Redelman D, Ro S, Ward SM, Ördög T, Sanders KM. Selective labeling and isolation of functional classes of interstitial cells of Cajal of human and murine small intestine. Am J Physiol Cell Physiol 292: C497-C507, 2007.
8. Cho SY, Beckett EA, Baker SA, Han I, Park KJ, Monaghan K, Ward SM, Sanders KM, Koh SD. A pH-sensitive potassium conductance (TASK) and its function in the murine gastrointestinal tract. J Physiol 565: 243-259, 2005.
9. Cousins HM, Edwards FR, Hickey H, Hill CE, Hirst GD. Electrical coupling between the myenteric interstitial cells of Cajal and adjacent muscle layers in the guinea-pig gastric antrum. J Physiol 550: 829-844, 2003.
10. Craxton M. Synaptotagmin gene content of the sequenced genomes. BMC Genomics 5: 43, 2004.
11. Domen J, Weissman IL. Hematopoietic stem cells need two signals to prevent apoptosis; BCL-2 can provide one of these, Kitl/Kit signaling the other. J Exp Med 192: 1707-1718, 2000.
12. Duchon G, Henderson R, Daniel EE. Circular muscle layers in the small intestine In: Proceedings of the Fourth International Symposium on Gastrointestinal Motility, edited by Daniel EE, Gilbert JAL, Schofield B, Schnitka TK, Scott G. Vancouver, British Columbia: 1974, p. 635-646.
13. FitzGerald UF, Gilbey T, Brodie S, Barnett SC. Transcription factor expression and cellular redox in immature oligodendrocyte cell death: effect of Bcl-2. Mol Cell Neurosci 22: 516-529, 2003.
14. Gentlemen R, Falcon S. How to use GOstats: testing gene lists for GO term association. http://bioconductor.org/packages/2.1/bioc/vignettes/ GOstats/inst/doc/GOstatsHyperG.pdf.
15. Huber A, Trudrung P, Storr M, Franck H, Schusdziarra V, Ruth P, Allescher HD. Protein kinase G expression in the small intestine and functional importance for smooth muscle relaxation. Am J Physiol Gastrointest Liver Physiol 275: G629-G637, 1998.
16. Huizinga JD, Thuneberg L, Kluppel M, Malysz J, Mikkelsen HB, Bernstein A. W/kit gene required for intestinal pacemaker activity. Nature 373: 347-349, 1995.
17. Iino S, Ward SM, Sanders KM. Interstitial cells of Cajal are functionally innervated by excitatory motor neurons in the murine intestine. J Physiol 556: 521-530, 2004.
18. Irizzary RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264, 2003.
19. Ito M, Kawa Y, Ono H, Okura M, Baba T, Kubota Y, Nishikawa SI, Mizoguchi M. Removal of stem cell factor or addition of monoclonal anti-Kit antibody induces apoptosis in murine melanocyte precursors. J Invest Dermatol 112: 796-801, 1999.
20. Kim BJ, Lim HH, Yang DK, Jun JY, Chang IY, Park CS, So I, Stanfield PR, Kim KW. Melastatin-type transient receptor potential channel 7 is required for intestinal pacemaking activity. Gastroenterology 129: 1504-1517, 2005.
21. Kim YC, Koh SD, Sanders KM. Voltage-dependent inward currents of interstitial cells of Cajal from murine colon and small intestine. J Physiol 541: 797-810, 2002.
22. Kito Y, Suzuki H. Properties of pacemaker potentials recorded from myenteric interstitial cells of Cajal distributed in the mouse small intestine. J Physiol 553: 803-818, 2003.
23. Kito Y, Ward SM, Sanders KM. Pacemaker potentials generated by interstitial cells of Cajal in the murine intestine. Am J Physiol Cell Physiol 288: C710-C720, 2005.
24. Lavin ST, Southwell BR, Murphy R, Jenkinson KM, Furness JB. Activation of neurokinin 1 receptors on interstitial cells of Cajal of the guinea-pig small intestine by substance P. Histochem Cell Biol 110: 263-271, 1998.
25. Lin YH, Park ZY, Lin D, Brahmbhatt AA, Rio MC, Yates JR 3rd, Klemke RL. Regulation of cell migration and survival by focal adhesion targeting of Lasp-1. J Cell Biol 165: 421-432, 2004.
26. Liu LW, Thuneberg L, Huizinga JD. Cyclopiazonic acid, inhibiting the endoplasmic reticulum calcium pump, reduces the canine colonic pacemaker frequency. J Pharmacol Exp Ther 275: 1058-1068, 1995.
27. Maeda H, Yamagata A, Nishikawa S, Yoshinaga K, Kobayashi S, Nishi K, Nishikawa S. Requirement of Kit for development of intestinal pacemaker system. Development 116: 369-375, 1992.
28. Mages HW, Hutloff A, Heuck C, Buchner K, Himmelbauer H, Oliveri F. Kroczek RA. Molecular cloning and characterization of murine ICOS and identification of B7h as ICOS ligand. Eur J Immunol 30: 1040-1047, 2000.
29. McLoughlin RM, Hurst SM, Nowell MA, Harris DA, Horiuchi S, Morgan LW, Wilkinson TS, Yamamoto N, Topley N, Jones SA. Differential regulation of neutrophil-activating chemokines by IL-6 and its soluble receptor isoforms. J Immunol 172: 5676-5683, 2004.
30. Mekori YA, Gilfillan AM, Akin C, Hartmann K, Metcalfe DD. Human mast cell apoptosis is regulated through Bcl-2 and Bcl-XL. J Clin Immunol 21: 171-174, 2001.
31. Miller CJ. Description of Simpleaffy: easy analysis routines for affymetrix data. http://bioconductor.org/packages/2.1/bioc/vignettes/simpleaffy/ inst/doc/simpleAffy.pdf.
32. Nicholson SE, Willson TA, Farley A, Starr R, Zhang JG, Baca M, Alexander WS, Metcalf D, Hilton DJ, Nicola NA. Mutational analyses of the SOCS proteins suggest a dual domain requirement but distinct mechanisms for inhibition of LIF and IL-6 signal transduction. EMBO J 18: 375-385, 1999.
33. 2+ exchanger, NCX3. J Biol Chem 271: 24914-24921, 1996.
34. Nishio M, Oda A, Koizumi K, Satoh I, Sato Y, Endoh T, Tsutsumi A, Fujihara M, Ikebuchi K, Ikeda H, Koike T, Sawada KI. Stem cell factor prevents Fas-mediated apoptosis of human erythroid precursor cells with Src-family kinase dependency. Exp Hematol 29: 19-29, 2001.
35. Ohya S, Asakura K, Muraki K, Watanabe M, Imaizumi Y. Molecular and functional characterization of ERG, KCNQ, and KCNE subtypes in rat stomach smooth muscle. Am J Physiol Gastrointest Liver Physiol 282: G277-G287, 2002.
36. Ördög T, Redelman D, Horvath VJ, Miller LJ, Horowitz B, Sanders KM. Quantitative analysis by flow cytometry of interstitial cells of Cajal, pacemakers, and mediators of neurotransmission in the gastrointestinal tract. Cytometry A 62: 139-149, 2004.
37. Park KJ, Hennig GW, Lee HT, Spencer NJ, Ward SM, Smith TK, Sanders KM. Spatial and temporal mapping of pacemaker activity in interstitial cells of Cajal in mouse ileum in situ. Am J Physiol Cell Physiol 290: C1411-C1427, 2006.
38. 2+ exchange. Cell Calcium 34: 19-26, 2003.
39. Rumessen JJ, Thuneberg L. Interstitial cells of Cajal in human small intestine. Ultrastructural identification and organization between the main smooth muscle layers. Gastroenterology 100: 1417-1431, 1991.
40. Salmhofer H, Neuhuber WL, Ruth P, Huber A, Russwurm M, Allescher HD. Pivotal role of the interstitial cells of Cajal in the nitric oxide signaling pathway of rat small intestine. Morphological evidence. Cell Tissue Res 305: 331-340, 2001.
41. Sanders KM. G protein-coupled receptors in gastrointestinal physiology. IV. Neural regulation of gastrointestinal smooth muscle. Am J Physiol Gastrointest Liver Physiol 275: G1-G7, 1998.
42. Sanders KM, Ördög T, Koh SD, Torihashi S, Ward SM. Development and plasticity of interstitial cells of Cajal. Neurogastroenterol Motil 11: 311-338, 1999.
43. Sanders KM, Koh SD, Ward SM. Interstitial cells of Cajal as pacemakers in the gastrointestinal tract. Annu Rev Physiol 68: 307-343, 2006.
44. Schmitz J, Weissenbach M, Haan S, Heinrich PC, Schaper F. SOCS3 exerts its inhibitory function on interleukin-6 signal transduction through the SHP2 recruitment site of gp130. J Biol Chem 275: 12848-12856, 2000.
45. Smith CA. Textual description of Annaffy. http://bioconductor.org/ packages/2.1/bioc/vignettes/annaffy/inst/doc/annaffy.pdf.
46. Smyth GK. Limma: linear models for microarray data. In: Bioinformatics and Computational Biology Solutions Using R and Bioconductor, edited by Gentlemen R, Carey V, Dudoit S, Irizarry R, Huber W. New York: Springer, 2005, p. 397-420.
47. Sokolow S, Manto M, Gailly P, Molgo J, Vandebrouck C, Vanderwinden JM, Herchuelz A, Schurmans S. Impaired neuromuscular transmission and skeletal muscle fiber necrosis in mice lacking Na/Ca exchanger 3. J Clin Invest 113: 265-273, 2004.
48. Sommer U, Schmid C, Sobota RM, Lehmann U, Stevenson NJ, Johnston JA, Schaper F, Heinrich PC, Haan S. Mechanisms of SOCS3 phosphorylation upon interleukin-6 stimulation. Contributions of Src- and receptor-tyrosine kinases. J Biol Chem 280: 31478-31488, 2005.
49. Suzuki H, Ward SM, Bayguinov YR, Edwards F, Hirst GDS. Involvement in intramuscular interstitial cells of Cajal in nitrergic inhibition in the mouse gastric antrum. J Physiol 546: 751-763, 2003.
50. Torihashi S, Kobayashi S, Sanders KM. Interstitial cells in deep muscular plexus of canine small intestine may be specialized smooth muscle cells. Am J Physiol Gastrointest Liver Physiol 265: G638-G645, 1993.
51. Torihashi S, Ward SM, Nishikawa SI, Nishi K, Kobayashi S, Sanders KM. Kit-dependent development of interstitial cells and electrical activity in the murine gastrointestinal tract. Cell Tissue Res 280: 97-111, 1995.
52. Walker RL, Koh SD, Sergeant GP, Sanders KM, Horowitz B. TRPC4 currents have properties similar to the pacemaker current in interstitial cells of Cajal. Am J Physiol Cell Physiol 283: C1637-C1645, 2002.
53. Wang X, Athayde N, Trudinger B. A proinflammatory cytokine response is present in the fetal placental vasculature in placental insufficiency. Am J Obstet Gynecol 189: 1445-1451, 2003.
54. Wang XY, Sanders KM, Ward SM. Intimate relationship between interstitial cells of Cajal and enteric nerves in the guinea-pig small intestine. Cell Tissue Res 295: 247-256, 1999.
55. Wang XY, Ward SM, Gerthoffer WT, Sanders KM. Protein kinase C? translocation in enteric neurons and interstitial cells of Cajal in response to muscarinic stimulation. Am J Physiol Gastrointest Liver Physiol 285: G593-G601, 2003.
56. Wang XY, Paterson C, Huizinga JD. Cholinergic and nitrergic innervation of ICC-DMP and ICC-IM in the human small intestine. Neurogastroenterol Motil 15: 531-543, 2003.
57. Wang YF, Daniel EE. Gap junctions in gastrointestinal muscle contain multiple connexins. Am J Physiol Gastrointest Liver Physiol 281: G533-G543, 2001.
58. Ward SM, Burns AJ, Torihashi S, Sanders KM. Mutation of the proto-oncogene Kit blocks development of interstitial cells and electrical rhythmicity in murine intestine. J Physiol 480: 91-97, 1994.
59. Ward SM, Beckett EAH, Wang XY, Baker F, Khoyi M, Sanders KM. Interstitial cells of Cajal mediate cholinergic neurotransmission from enteric motor neurons. J Neurosci 20: 1393-1403, 2000.
60. Ward SM, Ordog T, Koh SD, Baker SA, Jun JY, Amberg G, Monaghan K, Sanders KM. Pacemaking in interstitial cells of Cajal depends upon calcium handling by endoplasmic reticulum and mitochondria. J Physiol 525: 355-361, 2000.
61. Ward SM, McLaren GJ, Sanders KM. Interstitial cells of Cajal in the deep muscular plexus mediate enteric motor neurotransmission in the mouse small intestine. J Physiol 573: 147-159, 2006.
62. Yamamoto M. Electron microscopic studies on the innervation of the smooth muscle and the interstitial cell of Cajal in the small intestine of the mouse and bat. Arch Histol Jpn 40: 171-201, 1977.
63. Yee NS, Hsiau CW, Serve H, Vosseller K, Besmer P. Mechanism of down-regulation of Kit receptor. Roles of receptor tyrosine kinase, phosphatidylinositol 3′-kinase, and protein kinase C. J Biol Chem 269: 31991-31998, 1994.
64. Yoshihara M, Montana ES. The synaptotagmins: calcium sensors for vesicular trafficking. Neuroscientist 10: 566-574, 2004.
65. Yus-Najera E, Munoz A, Salvador N, Jensen BS, Rasmussen HB, Defelipe J, Villarroel A. Localization of KCNQ5 in the normal and epileptic human temporal neocortex and hippocampal formation. Neuroscience 120: 353-364, 2003.
66. Zhou DS, Komuro T. The cellular network of interstitial cells associated with the deep muscular plexus of the guinea pig small intestine. Anat Embryol (Berl) 186: 519-527, 1992.