Updating old ideas and recent advances regarding the Interstitial Cells of Cajal

Brain Research Reviews

Volumn 61, Issue 2, 2009, Pages 154-169

  Garcia Lopez, P ^a   Garcia Marin, V ^a   Martinez Murillo R ^a   Freire, M ^a  

^a INSTITUTO CAJAL   (Spain)

Author keywords

Cajal; Interstitial Cells of Cajal

Indexed keywords

IMATINIB; MIDOSTAURIN; PROTEIN KINASE INHIBITOR; STEM CELL FACTOR RECEPTOR; TYROSINE KINASE RECEPTOR;

ANTINEOPLASTIC ACTIVITY; CELL FUNCTION; CELL STRUCTURE; CELL TYPE; CELLULAR DISTRIBUTION; CLINICAL TRIAL; DIGESTIVE SYSTEM DISEASE; FIBROBLAST; GASTROINTESTINAL STROMAL TUMOR; GLIA; HISTOLOGY; HUMAN; INTERSTITIAL CELL OF CAJAL; NERVE CELL; NERVE PLEXUS; NEURAL CREST; NEURAL TUBE; NEUROTRANSMISSION; NONHUMAN; PANCREAS; PATHOGENESIS; PERISTALSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SENSOR;

ANIMALS; BIOLOGICAL CLOCKS; ENTERIC NERVOUS SYSTEM; GASTROINTESTINAL TRACT; MUSCLE, SMOOTH; NEURONS;

EID: 70349507321     PISSN: 01650173     EISSN: 18726321     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2009.06.001     Document Type: Review

References (171)

1. Aguado F., Majo G., Ruiz-Montasell B., Llorens J., Marsal J., and Blasi J. Syntaxin 1A and 1B display distinct distribution patterns in the rat peripheral nervous system. Neuroscience 88 (1999) 437-446
2. Ambache N. The electrical activity of isolated mammalian intestines. J. Physiol. 106 (1947) 139-153
3. Beaumont W. Experiments and Observations on the Gastric Juice and the Physiology of Digestion (1833), Plattsburg Edition
4. d mice. J. Physiol. 543 (2002) 871-887
5. Beckett E.A., Takeda Y., Yanase H., Sanders K.M., and Ward S.M. Synaptic specializations exist between enteric motor nerves and interstitial cells of Cajal in the murine stomach. J. Comp Neurol. 493 (2005) 193-206
6. Beghini A., Tibiletti M.G., Roversi G., Chiaravalli A.M., Serio G., Capella C., and Larizza L. Germline mutation in the juxtamembrane domain of the kit gene in a family with gastrointestinal stromal tumors and urticaria pigmentosa. Cancer 92 (2001) 657-662
7. Berkley H.J. On complex nerve terminations and ganglion cells in the muscular tissue of the heart ventricle. Anat. Anz. 9 (1893) 34-42
8. Bockman D.E., and Sohal G.S. A new source of cells contributing to the developing gastrointestinal tract demonstrated in chick embryos. Gastroenterology 114 (1998) 878-882
9. Burns A.J., Lomax A.E., Torihashi S., Sanders K.M., and Ward S.M. Interstitial cells of Cajal mediate inhibitory neurotransmission in the stomach. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 12008-12013
10. Burnstock G., and Lavin S. Interstitial cells of Cajal and purinergic signalling. Auton. Neurosci. 97 (2002) 68-72
11. Cajal S.R. Estructura del centro nervioso de las aves. Rev. Trimes. Hist. Norm y Patol. 1 (1888) 1-10
12. Cajal S.R. Nuevas aplicaciones del método de coloración de Golgi. Gac. Méd. Catalana 12 (1889) 1-8
13. Cajal S.R. El plexo de Auerbach de los batracios. Trab. Lab. Histol. Facultad Med. Barcelona (1892) 23-28 Febrary
14. Cajal S.R. Los Ganglios y Plexos Nerviosos del Intestino de los Mamíferos. (1893), Imprenta y Libreía de Nicolás Moya, Madrid
15. Cajal S.R. Textura del Sistema Nervioso del Hombre y de los Vertebrados, 2 Vols 1 (1899-1904), Imprenta y librería de Nicolás Moya, Madrid
16. Cajal S.R. Neuronismo o Reticularimo? (1933), Imprenta y Libreria de Nicolás Moya, Madrid
17. Cajal S.R., and Sala C. Terminación de los nervios y tubos glandulares del páncreas de los vertebrados. Trab. Lab. Histol. Facultad Med. Barcelona 28 (1891) 1-5 Diciembre
18. Cannon W.B. The movements of the intestines studied by means of the Röntgen rays. Am. J. Physiol. 6 (1902) 251-277
19. Carballo M., Roig I., Aguilar F., Pol M.A., Gamundi M.J., Hernan I., and Martinez-Gimeno M. Novel c-KIT germline mutation in a family with gastrointestinal stromal tumors and cutaneous hyperpigmentation. Am. J. Med. Genet., A 132 (2005) 361-364
20. Chen H., Redelman D., Ro S., Ward S.M., Ordog T., and Sanders K.M. Selective labeling and isolation of functional classes of interstitial cells of Cajal of human and murine small intestine. Am. J. Physiol., Cell Physiol. 292 (2007) C497-C507
21. Ciontea S.M., Radu E., Regalia T., Ceafalan L., Cretoiu D., Gherghiceanu M., Braga R.I., Malincenco M., Zagrean L., Hinescu M.E., and Popescu L.M. C-kit immunopositive interstitial cells Cajal-type in human myometrium. J. Cell. Mol. Med. 9 (2005) 407-420
22. Corless C.L., Schroeder A., Griffith D., Town A., McGreevey L., Harrell P., Shiraga S., Bainbridge T., Morich J., and Heinrich M.C. PDGFRA mutations in gastrointestinal stromal tumors: frequency, spectrum and in vitro sensitivity to imatinib. J. Clin. Oncol. 23 (2005) 5357-5364
23. Daniel E.E. Nerves and motor activity of the gut. In: E.P.e F.P., and Brooks (Eds). Nerves and the gut. (1977), Slack, New York 154-196
24. Daniel E.E. Communication between interstitial cells of Cajal and gastrointestinal muscle. Neurogastroenterol. Motil. 16 Suppl. 1 (2004) 118-122
25. Daniel E.E., and Posey-Daniel V. Neuromuscular structures in opossum esophagus: role of interstitial cells of Cajal. Am. J. Physiol. 246 (1984) G305-G315
26. Daniel E.E., Yazbi A.E., Mannarino M., Galante G., Boddy G., Livergant J., and Oskouei T.E. Do gap junctions play a role in nerve transmissions as well as pacing in mouse intestine?. Am. J. Physiol., Gastrointest. Liver Physiol. 292 (2007) G734-G745
27. Debiec-Rychter M., Cools J., Dumez H., Sciot R., Stul M., Mentens N., Vranckx H., Wasag B., Prenen H., Roesel J., Hagemeijer A., van O.A., and Marynen P. Mechanisms of resistance to imatinib mesylate in gastrointestinal stromal tumors and activity of the PKC412 inhibitor against imatinib-resistant mutants. Gastroenterology 128 (2005) 270-279
28. Demetri G.D., von M.M., Blanke C.D., Van den Abbeele A.D., Eisenberg B., Roberts P.J., Heinrich M.C., Tuveson D.A., Singer S., Janicek M., Fletcher J.A., Silverman S.G., Silberman S.L., Capdeville R., Kiese B., Peng B., Dimitrijevic S., Druker B.J., Corless C., Fletcher C.D., and Joensuu H. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N. Engl. J. Med. 347 (2002) 472-480
29. Demetri G.D., van Oosterom A.T., Garrett C.R., Blackstein M.E., Shah M.H., Verweij J., McArthur G., Judson I.R., Heinrich M.C., Morgan J.A., Desai J., Fletcher C.D., George S., Bello C.L., Huang X., Baum C.M., and Casali P.G. Efficacy and safety of sunitinib in patients with advanced gastrointestinal stromal tumour after failure of imatinib: a randomised controlled trial. Lancet 368 (2006) 1329-1338
30. Dickens E.J., Edwards F.R., and Hirst G.D. Selective knockout of intramuscular interstitial cells reveals their role in the generation of slow waves in mouse stomach. J. Physiol. 531 (2001) 827-833
31. Edwards F.R., Hirst G.D., and Suzuki H. Unitary nature of regenerative potentials recorded from circular smooth muscle of guinea-pig antrum. J. Physiol. 519 Pt. 1 (1999) 235-250
32. Epperson A., Hatton W.J., Callaghan B., Doherty P., Walker R.L., Sanders K.M., Ward S.M., and Horowitz B. Molecular markers expressed in cultured and freshly isolated interstitial cells of Cajal. Am. J. Physiol. Cell Physiol. 279 (2000) C529-C539
33. Faussone-Pellegrini M.S. Relationships between neurokinin receptor-expressing interstitial cells of Cajal and tachykininergic nerves in the gut. J. Cell. Mol. Med. 10 (2006) 20-32
34. Faussone-Pellegrini M.S., Cortesini C., and Romagnoli P. Ultrastructure of the tunica muscularis of the cardial portion of the human esophagus and stomach, with special reference to the so-called Cajal's interstitial cells. Arch. Ital. Anat. Embriol. 82 (1977) 157-177
35. Faussone-Pellegrini M.S., and Thuneberg L. Guide to the identification of interstitial cells of Cajal. Microsc. Res. Tech. 47 (1999) 248-266
36. Furitsu T., Tsujimura T., Tono T., Ikeda H., Kitayama H., Koshimizu U., Sugahara H., Butterfield J.H., Ashman L.K., and Kanayama Y. Identification of mutations in the coding sequence of the proto-oncogene c-kit in a human mast cell leukemia cell line causing ligand-independent activation of c-kit product. J. Clin. Invest. 92 (1993) 1736-1744
37. Furuya S., and Furuya K. Subepithelial fibroblasts in intestinal villi: roles in intercellular communication. Int. Rev. Cytol. 264 (2007) 165-223
38. Furuya S., Furuya K., Sokabe M., Hiroe T., and Ozaki T. Characteristics of cultured subepithelial fibroblasts in the rat small intestine. II. Localization and functional analysis of endothelin receptors and cell-shape-independent gap junction permeability. Cell Tissue Res. 319 (2005) 103-119
39. Glatzle J., Sternini C., Robin C., Zittel T.T., Wong H., Reeve Jr. J.R., and Raybould H.E. Expression of 5-HT3 receptors in the rat gastrointestinal tract. Gastroenterology 123 (2002) 217-226
40. Goodman V.L., Rock E.P., Dagher R., Ramchandani R.P., Abraham S., Gobburu J.V., Booth B.P., Verbois S.L., Morse D.E., Liang C.Y., Chidambaram N., Jiang J.X., Tang S., Mahjoob K., Justice R., and Pazdur R. Approval summary: sunitinib for the treatment of imatinib refractory or intolerant gastrointestinal stromal tumors and advanced renal cell carcinoma. Clin. Cancer Res. 13 (2007) 1367-1373
41. Grady E.F., Baluk P., Bohm S., Gamp P.D., Wong H., Payan D.G., Ansel J., Portbury A.L., Furness J.B., McDonald D.M., and Bunnett N.W. Characterization of antisera specific to NK1, NK2, and NK3 neurokinin receptors and their utilization to localize receptors in the rat gastrointestinal tract. J. Neurosci. 16 (1996) 6975-6986
42. Growney J.D., Clark J.J., Adelsperger J., Stone R., Fabbro D., Griffin J.D., and Gilliland D.G. Activation mutations of human c-KIT resistant to imatinib mesylate are sensitive to the tyrosine kinase inhibitor PKC412. Blood 106 (2005) 721-724
43. Güldner F.H., Wolff J.R., and Keyserlingk D.G. Fibroblasts as a part of the contractile system in duodenal villi of rat. Z. Zellforsch. Mikrosk. Anat. 135 (1972) 349-360
44. Hanani M., Farrugia G., and Komuro T. Intercellular coupling of interstitial cells of Cajal in the digestive tract. Int. Rev. Cytol. 242 (2005) 249-282
45. Hara Y., Kubota M., and Szurszewski J.H. Electrophysiology of smooth muscle of the small intestine of some mammals. J. Physiol. 372 (1986) 501-520
46. Hartmann K., Wardelmann E., Ma Y., Merkelbach-Bruse S., Preussner L.M., Woolery C., Baldus S.E., Heinicke T., Thiele J., Buettner R., and Longley B.J. Novel germline mutation of KIT associated with familial gastrointestinal stromal tumors and mastocytosis. Gastroenterology 129 (2005) 1042-1046
47. Hashitani H., Garcia-Londono A.P., Hirst G.D., and Edwards F.R. Atypical slow waves generated in gastric corpus provide dominant pacemaker activity in guinea pig stomach. J. Physiol. 569 (2005) 459-465
48. Heinrich M.C., Corless C.L., Duensing A., McGreevey L., Chen C.J., Joseph N., Singer S., Griffith D.J., Haley A., Town A., Demetri G.D., Fletcher C.D., and Fletcher J.A. PDGFRA activating mutations in gastrointestinal stromal tumors. Science 299 (2003) 708-710
49. Hinescu M.E., and Popescu L.M. Interstitial Cajal-like cells ICLC in human atrial myocardium. J. Cell. Mol. Med. 9 (2005) 972-975
50. Hirota S., and Isozaki K. Pathology of gastrointestinal stromal tumors. Pathol. Int. 56 (2006) 1-9
51. Hirota S., Isozaki K., Moriyama Y., Hashimoto K., Nishida T., Ishiguro S., Kawano K., Hanada M., Kurata A., Takeda M., Muhammad T.G., Matsuzawa Y., Kanakura Y., Shinomura Y., and Kitamura Y. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 279 (1998) 577-580
52. Hirota S., Okazaki T., Kitamura Y., O'Brien P., Kapusta L., and Dardick I. Cause of familial and multiple gastrointestinal autonomic nerve tumors with hyperplasia of interstitial cells of Cajal is germline mutation of the c-kit gene. Am. J. Surg. Pathol. 24 (2000) 326-327
53. Hirota S., Nishida T., Isozaki K., Taniguchi M., Nakamura J., Okazaki T., and Kitamura Y. Gain-of-function mutation at the extracellular domain of KIT in gastrointestinal stromal tumours. J. Pathol. 193 (2001) 505-510
54. Hirota S., Nishida T., Isozaki K., Taniguchi M., Nishikawa K., Ohashi A., Takabayashi A., Obayashi T., Okuno T., Kinoshita K., Chen H., Shinomura Y., and Kitamura Y. Familial gastrointestinal stromal tumors associated with dysphagia and novel type germline mutation of KIT gene. Gastroenterology 122 (2002) 1493-1499
55. Hirota S., Ohashi A., Nishida T., Isozaki K., Kinoshita K., Shinomura Y., and Kitamura Y. Gain-of-function mutations of platelet-derived growth factor receptor alpha gene in gastrointestinal stromal tumors. Gastroenterology 125 (2003) 660-667
56. Hirst G.D., Beckett E.A., Sanders K.M., and Ward S.M. Regional variation in contribution of myenteric and intramuscular interstitial cells of Cajal to generation of slow waves in mouse gastric antrum. J. Physiol. 540 (2002) 1003-1012
57. Hirst G.D., Dickens E.J., and Edwards F.R. Pacemaker shift in the gastric antrum of guinea-pigs produced by excitatory vagal stimulation involves intramuscular interstitial cells. J. Physiol. 541 (2002) 917-928
58. Horiguchi K., and Komuro T. Ultrastructural characterization of interstitial cells of Cajal in the rat small intestine using control and Ws/Ws mutant rats. Cell Tissue Res. 293 (1998) 277-284
59. Horiguchi K., Sanders K.M., and Ward S.M. Enteric motor neurons form synaptic-like junctions with interstitial cells of Cajal in the canine gastric antrum. Cell Tissue Res. 311 (2003) 299-313
60. Huizinga J.D. Physiology and pathophysiology of the interstitial cell of Cajal: from bench to bedside. II. Gastric motility: lessons from mutant mice on slow waves and innervation. Am. J. Physiol., Gastrointest. Liver Physiol. 281 (2001) G1129-G1134
61. Huizinga J.D., Thuneberg L., Kluppel M., Malysz J., Mikkelsen H.B., and Bernstein A. W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity. Nature 373 (1995) 347-349
62. Huizinga J.D., Thuneberg L., Vanderwinden J.M., and Rumessen J.J. Interstitial cells of Cajal as targets for pharmacological intervention in gastrointestinal motor disorders. Trends Pharmacol. Sci. 18 (1997) 393-403
63. Huizinga J.D., Berezin I., Sircar K., Hewlett B., Donnelly G., Bercik P., Ross C., Algoufi T., Fitzgerald P., Der T., Riddell R.H., Collins S.M., and Jacobson K. Development of interstitial cells of Cajal in a full-term infant without an enteric nervous system. Gastroenterology 120 (2001) 561-567
64. Huizinga J.D., and Faussone-Pellegrini M.S. About the presence of interstitial cells of Cajal outside the musculature of the gastrointestinal tract. J. Cell. Mol. Med. 9 (2005) 468-473
65. Iino S., and Nojyo Y. Muscarinic M2 acetylcholine receptor distribution in the guinea-pig gastrointestinal tract. Neuroscience 138 (2006) 549-559
66. Iino S., Ward S.M., and Sanders K.M. Interstitial cells of Cajal are functionally innervated by excitatory motor neurones in the murine intestine. J. Physiol. 556 (2004) 521-530
67. Imaizumi M., and Hama K. An electron microscopic study on the interstitial cells of the gizzard in the love-bird Uroloncha domestica. Z. Zellforsch. Mikrosk. Anat. 97 (1969) 351-357
68. Isozaki K., and Hirota S. Gain-of-function mutations of receptor tyrosine kinases in gastrointestinal stromal tumors. Curr. Genomics 7 (2006) 469-475
69. Isozaki K., Terris B., Belghiti J., Schiffmann S., Hirota S., and Vanderwinden J.M. Germline-activating mutation in the kinase domain of KIT gene in familial gastrointestinal stromal tumors. Am. J. Pathol. 157 (2000) 1581-1585
70. Jabonero V. El problema de las y el modo de terminar las vías vegetativas eferentes. Trab. Lab. Histol. Facultad Med. Barcelona 52 (1960) 21-100
71. Joensuu H., Roberts P.J., Sarlomo-Rikala M., Andersson L.C., Tervahartiala P., Tuveson D., Silberman S., Capdeville R., Dimitrijevic S., Druker B., and Demetri G.D. Effect of the tyrosine kinase inhibitor STI571 in a patient with a metastatic gastrointestinal stromal tumor. N. Engl. J. Med. 344 (2001) 1052-1056
72. Keith A. A new theory of the causation of enterostasis. Lancet 2 (1915) 371-375
73. Kim H.J., Lim S.J., Park K., Yuh Y.J., Jang S.J., and Choi J. Multiple gastrointestinal stromal tumors with a germline c-kit mutation. Pathol. Int. 55 (2005) 655-659
74. Kindblom L.G., Remotti H.E., Aldenborg F., and Meis-Kindblom J.M. Gastrointestinal pacemaker cell tumor GIPACT: gastrointestinal stromal tumors show phenotypic characteristics of the interstitial cells of Cajal. Am. J. Pathol. 152 (1998) 1259-1269
75. Kinoshita K., Isozaki K., Hirota S., Nishida T., Chen H., Nakahara M., Nagasawa Y., Ohashi A., Shinomura Y., Kitamura Y., and Matsuzawa Y. c-kit gene mutation at exon 17 or 13 is very rare in sporadic gastrointestinal stromal tumors. J. Gastroenterol. Hepatol. 18 (2003) 147-151
76. Kluppel M., Huizinga J.D., Malysz J., and Bernstein A. Developmental origin and Kit-dependent development of the interstitial cells of cajal in the mammalian small intestine. Dev. Dyn. 211 (1998) 60-71
77. Komuro T. Three-dimensional observation of the fibroblast-like cells associated with the rat myenteric plexus, with special reference to the interstitial cells of Cajal. Cell Tissue Res. 255 (1989) 343-351
78. Komuro T. Re-evaluation of fibroblasts and fibroblast-like cells. Anat. Embryol. Berl 182 (1990) 103-112
79. Komuro T. Comparative morphology of interstitial cells of Cajal: ultrastructural characterization. Microsc. Res. Tech. 47 (1999) 267-285
80. Komuro T. Morphological features of interstitial cells of Cajal. In: Kitamur Y., Miettinenn M., Hirota S., and kanakura Y. (Eds). Gastrointestinal Stromal Tumor (GIST): from pathology to molecular target therapy, Gann Monograph on Cancer Research No 53 (2004), Japan Scientific Societies Press & Karger, Tokyo, Basel 109-134
81. Komuro T. Structure and organization of interstitial cells of Cajal in the gastrointestinal tract. J. Physiol. 576 (2006) 653-658
82. Komuro T., and Hashimoto Y. Three-dimensional structure of the rat intestinal wall mucosa and submucosa. Arch. Histol. Cytol. 53 (1990) 1-21
83. Lang R.J., and Klemm M.F. Interstitial cell of Cajal-like cells in the upper urinary tract. J. Cell. Mol. Med. 9 (2005) 543-556
84. Langton P., Ward S.M., Carl A., Norell M.A., and Sanders K.M. Spontaneous electrical activity of interstitial cells of Cajal isolated from canine proximal colon. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 7280-7284
85. Lasota J., Jasinski M., Sarlomo-Rikala M., and Miettinen M. Mutations in exon 11 of c-Kit occur preferentially in malignant versus benign gastrointestinal stromal tumors and do not occur in leiomyomas or leiomyosarcomas. Am. J. Pathol. 154 (1999) 53-60
86. Lasota J., Wozniak A., Sarlomo-Rikala M., Rys J., Kordek R., Nassar A., Sobin L.H., and Miettinen M. Mutations in exons 9 and 13 of KIT gene are rare events in gastrointestinal stromal tumors. A study of 200 cases. Am. J. Pathol. 157 (2000) 1091-1095
87. Lasota J., Stachura J., and Miettinen M. GISTs with PDGFRA exon 14 mutations represent subset of clinically favorable gastric tumors with epithelioid morphology. Lab. Invest. 86 (2006) 94-100
88. LaVilla I. Estructura de los ganglios intestinales. Rev. Trimest. Microgr. 2 (1897) 187-192
89. LaVilla I. Estructura de los ganglios intestinales. Rev. Trimest. Microgr. 3 (1898) 1-13
90. Lavin S.T., Southwell B.R., Murphy R., Jenkinson K.M., and Furness J.B. Activation of neurokinin 1 receptors on interstitial cells of Cajal of the guinea-pig small intestine by substance P. Histochem. Cell Biol. 110 (1998) 263-271
91. Lecoin L., Gabella G., and Le D.N. Origin of the c-kit-positive interstitial cells in the avian bowel. Development 122 (1996) 725-733
92. Li C.X., Liu B.H., Tong W.D., Zhang L.Y., and Jiang Y.P. Dissociation, culture and morphologic changes of interstitial cells of Cajal in vitro. World J. Gastroenterol. 11 (2005) 2838-2840
93. Liu L.W., Thuneberg L., Daniel E.E., and Huizinga J.D. Selective accumulation of methylene blue by interstitial cells of Cajal in canine colon. Am. J. Physiol. 264 (1993) G64-G73
94. Liu L.W., Thuneberg L., and Huizinga J.D. Selective lesioning of interstitial cells of Cajal by methylene blue and light leads to loss of slow waves. Am. J. Physiol. 266 (1994) G485-G496
95. 4 receptors in the mouse enteric nervous system. Am. J. Physiol., Gastrointest. Liver Physiol. 289 (2005) G1148-G1163
96. Lux M.L., Rubin B.P., Biase T.L., Chen C.J., Maclure T., Demetri G., Xiao S., Singer S., Fletcher C.D., and Fletcher J.A. KIT extracellular and kinase domain mutations in gastrointestinal stromal tumors. Am. J. Pathol. 156 (2000) 791-795
97. Maeda H., Yamagata A., Nishikawa S., Yoshinaga K., Kobayashi S., Nishi K., and Nishikawa S. Requirement of c-kit for development of intestinal pacemaker system. Development 116 (1992) 369-375
98. Maeyama H., Hidaka E., Ota H., Minami S., Kajiyama M., Kuraishi A., Mori H., Matsuda Y., Wada S., Sodeyama H., Nakata S., Kawamura N., Hata S., Watanabe M., Iijima Y., and Katsuyama T. Familial gastrointestinal stromal tumor with hyperpigmentation: association with a germline mutation of the c-kit gene. Gastroenterology 120 (2001) 210-215
99. Martinez A., Marin V.G., Junquera S.R., Martinez-Murillo R., and Freire M. The contributions of Santiago Ramon y Cajal to cancer research - 100 years on. Nat. Rev. Cancer 5 (2005) 904-909 Review
100. Mazur M.T., and Clark H.B. Gastric stromal tumors. Reappraisal of histogenesis. Am. J. Surg. Pathol. 7 (1983) 507-519
101. Moskaluk C.A., Tian Q., Marshall C.R., Rumpel C.A., Franquemont D.W., and Frierson Jr. H.F. Mutations of c-kit JM domain are found in a minority of human gastrointestinal stromal tumors. Oncogene 18 (1999) 1897-1902
102. Nakayama S., Kajioka S., Goto K., Takaki M., and Liu H.N. Calcium-associated mechanisms in gut pacemaker activity. J. Cell. Mol. Med. 11 (2007) 958-968 Review
103. Nirasawa Y., Ito Y., Seki N., and Akagawa K. HPC-1/syntaxin-1A activity in the enteric nervous system of developing rat gastrointestinal tract. J. Smooth Muscle Res. 33 (1997) 61-66
104. Nishida T., Hirota S., Taniguchi M., Hashimoto K., Isozaki K., Nakamura H., Kanakura Y., Tanaka T., Takabayashi A., Matsuda H., and Kitamura Y. Familial gastrointestinal stromal tumours with germline mutation of the KIT gene. Nat. Genet. 19 (1998) 323-324
105. O'Brien P., Kapusta L., Dardick I., Axler J., and Gnidec A. Multiple familial gastrointestinal autonomic nerve tumors and small intestinal neuronal dysplasia. Am. J. Surg. Pathol. 23 (1999) 198-204
106. Oki M., and Daniel E.E. Ultrastructural basis for electrical coupling in the dog stomach. In: Daniel E.E. (Ed). Proc. 4th. Int. Symp.Gastrointest, e (1973), Mitchell Press, Vancouver 85-95
107. O'Riain C., Corless C.L., Heinrich M.C., Keegan D., Vioreanu M., Maguire D., and Sheahan K. Gastrointestinal stromal tumors: insights from a new familial GIST kindred with unusual genetic and pathologic features. Am. J. Surg. Pathol. 29 (2005) 1680-1683
108. Patterson L.M., Zheng H., Ward S.M., and Berthoud H.R. Immunohistochemical identification of cholecystokinin A receptors on interstitial cells of Cajal, smooth muscle, and enteric neurons in rat pylorus. Cell Tissue Res. 305 (2001) 11-23
109. Paula J.S., de Souza E.S., Oliveira M.B., Rodrigues Mde L., and Garcia S.B. Is the positive c-kit immunostaining associated with the presence of cells analogous to the interstiticial cells of Cajal in the ciliary muscle. Arg. Bras. Oftalmol. 72 (2009) 43-46
110. Poole D.P., Van Nguyen T., Kawai M., and Furness J.B. Protein kinases expressed by interstitial cells of Cajal. Histochem. Cell Biol. 121 (2004) 21-30
111. Poole D.P., Xu B., Koh S.L., Hunne B., Coupar I.M., Irving H.R., Shinjo K., and Furness J.B. Identification of neurons that express 5-hydroxytryptamine4 receptors in intestine. Cell Tissue Res. 325 (2006) 413-422
112. Popescu L.M., Hinescu M.E., Ionescu N., Ciontea S.M., Cretoiu D., and Ardelean C. Interstitial cells of Cajal in pancreas. J. Cell. Mol. Med. 9 (2005) 169-190
113. Popescu L.M., Gherghiceanu M., Hinescu M.E., Cretoiu D., Ceafalan L., Regalia T., Popescu A.C., Ardeleanu C., and Mandache E. Insights into the interstitium of ventricular myocardium: interstitial Cajal-like cells ICLC. J. Cell. Mol. Med. 10 (2006) 429-458
114. Popescu L.M., Ciontea S.M., and Cretoiu D. Interstitial Cajal-like cells in human uterus and fallopian tube. Ann. N.Y. Acad. Sci. 1101 (2007) 139-165
115. Porcher C., Baldo M., Henry M., Orsoni P., Jule Y., and Ward S.M. Deficiency of interstitial cells of Cajal in the small intestine of patients with Crohn's disease. Am. J. Gastroenterol. 97 (2002) 118-125
116. Porcher C., Juhem A., Peinnequin A., and Bonaz B. Bombesin receptor subtype-3 is expressed by the enteric nervous system and by interstitial cells of Cajal in the rat gastrointestinal tract. Cell Tissue Res. 320 (2005) 21-31
117. Portbury A.L., Furness J.B., Young H.M., Southwell B.R., and Vigna S.R. Localisation of NK1 receptor immunoreactivity to neurons and interstitial cells of the guinea-pig gastrointestinal tract. J. Comp. Neurol. 367 (1996) 342-351
118. Richardson K.C. Electron microscopic observations on Auerbach's plexus in the rabbit, with special reference to the problem of smooth muscle innervation. Am. J. Anat. 103 (1958) 99-135
119. Robinson T.L., Sircar K., Hewlett B.R., Chorneyko K., Riddell R.H., and Huizinga J.D. Gastrointestinal stromal tumors may originate from a subset of CD34-positive interstitial cells of Cajal. Am. J. Pathol. 156 (2000) 1157-1163
120. Robson M.E., Glogowski E., Sommer G., Antonescu C.R., Nafa K., Maki R.G., Ellis N., Besmer P., Brennan M., and Offit K. Pleomorphic characteristics of a germ-line KIT mutation in a large kindred with gastrointestinal stromal tumors, hyperpigmentation, and dysphagia. Clin. Cancer Res. 10 (2004) 1250-1254
121. Rubin B.P., Singer S., Tsao C., Duensing A., Lux M.L., Ruiz R., Hibbard M.K., Chen C.J., Xiao S., Tuveson D.A., Demetri G.D., Fletcher C.D., and Fletcher J.A. KIT activation is a ubiquitous feature of gastrointestinal stromal tumors. Cancer Res. 61 (2001) 8118-8121
122. Rumessen J.J., and Vanderwinden J.M. Interstitial cells in the musculature of the gastrointestinal tract: Cajal and beyond. Int. Rev. Cytol. 229 (2003) 115-208
123. Sanders K.M., and Ward S.M. Interstitial cells of Cajal: a new perspective on smooth muscle function. J. Physiol. 576 (2006) 721-726
124. Sarlomo-Rikala M., Kovatich A.J., Barusevicius A., and Miettinen M. CD117: a sensitive marker for gastrointestinal stromal tumors that is more specific than CD34. Mod. Pathol. 11 (1998) 728-734
125. Scaife C.L., Hunt K.K., Patel S.R., Benjamin R.S., Burgess M.A., Chen L.L., Trent J., Raymond A.K., Cormier J.N., Pisters P.W., Pollock R.E., and Feig B.W. Is there a role for surgery in patients with "unresectable" cKIT+ gastrointestinal stromal tumors treated with imatinib mesylate?. Am. J. Surg. 186 (2003) 665-669
126. Sergeant G.P., Hollywood M.A., McHale N.G., and Thornbury K.D. Ca2+ signalling in urethral interstitial cells of Cajal. J. Physiol. 576 (2006) 715-720
127. Sircar K., Hewlett B.R., Huizinga J.D., Chorneyko K., Berezin I., and Riddell R.H. Interstitial cells of Cajal as precursors of gastrointestinal stromal tumors. Am. J. Surg. Pathol. 23 (1999) 377-389
128. Smith T.K., Reed J.B., and Sanders K.M. Origin and propagation of electrical slow waves in circular muscle of canine proximal colon. Am. J. Physiol. 252 (1987) C215-C224
129. Sohal G.S., Bockman D.E., Ali M.M., and Tsai N.T. DiI labeling and homeobox gene islet-1 expression reveal the contribution of ventral neural tube cells to the formation of the avian trigeminal ganglion. Int. J. Dev. Neurosci. 14 (1996) 419-427
130. Sohal G.S., Ali M.M., and Farooqui F.A. A second source of precursor cells for the developing enteric nervous system and interstitial cells of Cajal. Int. J. Dev. Neurosci. 20 (2002) 619-626
131. Song G., Hirst G.D.S., Sanders K.M., and Ward S.M. Regional variation in ICC distribution, pacemaking activity and neural responses in the longitudinal muscle of the murine stomach. J. Physiol. 564 (2005) 523-540
132. Southwell B.R. Localization of protein kinase C theta immunoreactivity to interstitial cells of Cajal in guinea-pig gastrointestinal tract. Neurogastroenterol. Motil. 15 (2003) 139-147
133. Sternini C., Su D., Gamp P.D., and Bunnett N.W. Cellular sites of expression of the neurokinin-1 receptor in the rat gastrointestinal tract. J. Comp. Neurol. 358 (1995) 531-540
134. Sternini C., Wong H., Wu S.V., de Giorgio R., Yang M., Reeve Jr. J., Brecha N.C., and Walsh J.H. Somatostatin 2A receptor is expressed by enteric neurons, and by interstitial cells of Cajal and enterochromaffin-like cells of the gastrointestinal tract. J. Comp. Neurol. 386 (1997) 396-408
135. Streutker C.J., Huizinga J.D., Driman D.K., and Riddell R.H. Interstitial cells of Cajal in health and disease. Part II: ICC and gastrointestinal stromal tumours. Histopathology 50 (2007) 190-202
136. Suciu L., Popescu L.M., and Gherghiceanu M. Human placenta: de visu demonstration of interstitial Cajal-like cells. J. Cell. Mol. Med. 11 (2007) 590-597
137. Suzuki H. Cellular mechanisms of myogenic activity in gastric smooth muscle. Jpn. J. Physiol. 50 (2000) 289-301
138. Suzuki N., Prosser C.L., and Dahms V. Boundary cells between longitudinal and circular layers: essential for electrical slow waves in cat intestine. Am. J. Physiol. 250 (1986) G287-G294
139. Taniguchi M., Nishida T., Hirota S., Isozaki K., Ito T., Nomura T., Matsuda H., and Kitamura Y. Effect of c-kit mutation on prognosis of gastrointestinal stromal tumors. Cancer Res. 59 (1999) 4297-4300
140. Taxi J. Cellules de Schwann et 'cellules interstitielles de Cajal' au niveau des plexus nerveux de la musculeuse intestinale du Cobaye: retour aux definitions. Arch. Anat. Microsc. Morph. Exp. 41 (1952) 281-304
141. Taxi J. Contribution a' l'étude des connexions des neurones moteurs du système nerveux autonome. Ann. Sci. Nat. Zool. 7 (1965) 413-674
142. Thomsen L., Robinson T.L., Lee J.C., Farraway L.A., Hughes M.J., Andrews D.W., and Huizinga J.D. Interstitial cells of Cajal generate a rhythmic pacemaker current. Nat. Med. 4 (1998) 848-851
143. Thuneberg L. Interstitial cells of Cajal: intestinal pacemaker cells?. Adv. Anat. Embryol. Cell Biol. 71 (1982) 1-130
144. Thuneberg L. Interstitial cells of Cajal. In: Wood J.D. (Ed). Handbook of physiology. The gastrointestinal system, vol.1., e (1989), Am Physiol. Soc., Bethesda, MD 349-386
145. Thuneberg L. Methylene blue as a pharmacological probe of intestinal pacemaker activity. Am. J. Physiol. 258 (1990) G992-G994
146. Thuneberg L. One hundred years of interstitial cells of Cajal. Microsc. Res. Tech. 47 (1999) 223-238
147. Thuneberg L., and Peters S. Toward a concept of stretch-coupling in smooth muscle. I. Anatomy of intestinal segmentation and sleeve contractions. Anat. Rec. 262 (2001) 110-124
148. Thuneberg L., Johansen V., Rumessen J.J., and Andersen B.G. Interstitial cells of Cajal ICC: Selective uptake of methylene blue inhibits slow wave activity. In: Roman C. (Ed). Gastrointestinal motility., e. (1983), MTP Press., Lancaster, PA 495-502
149. Toma H., Nakamura K., Emson P.C., and Kawabuchi M. Immunohistochemical distribution of c-Kit-positive cells and nitric oxide synthase-positive nerves in the guinea-pig small intestine. J. Auton. Nerv. Syst. 75 (1999) 93-99
150. Torihashi S., Ward S.M., and Sanders K.M. Development of c-Kit-positive cells and the onset of electrical rhythmicity in murine small intestine. Gastroenterology 112 (1997) 144-155
151. Torihashi S., Horisawa M., and Watanabe Y. c-Kit immunoreactive interstitial cells in the human gastrointestinal tract. J. Auton. Nerv. Syst. 75 (1999) 38-50
152. Vannucchi M.G., and Faussone-Pellegrini M.S. NK1, NK2 and NK3 tachykinin receptor localization and tachykinin distribution in the ileum of the mouse. Anat. Embryol. Berl. 202 (2000) 247-255
153. Vannucchi M.G., Zardo C., Corsani L., and Faussone-Pellegrini M.S. Interstitial cells of Cajal, enteric neurons, and smooth muscle and myoid cells of the murine gastrointestinal tract express full-length dystrophin. Histochem. Cell Biol. 118 (2002) 449-457
154. 4 receptor in enteric glial cells and interstitial cells of Cajal within the guinea-pig gastrointestinal tract. Auton. Neurosci. 126-127 (2006) 299-306
155. Verweij J., Casali P.G., Zalcberg J., LeCesne A., Reichardt P., Blay J.Y., Issels R., van O.A., Hogendoorn P.C., van G.M., Bertulli R., and Judson I. Progression-free survival in gastrointestinal stromal tumours with high-dose imatinib: randomised trial. Lancet 364 (2004) 1127-1134
156. Vigmond E.J., Bardakjian B.L., Thuneberg L., and Huizinga J.D. Intercellular coupling mediated by potassium accumulation in peg-and-socket junctions. IEEE Trans. Biomed. Eng 47 (2000) 1576-1583
157. Wang X.Y., Sanders K.M., and Ward S.M. Intimate relationship between interstitial cells of cajal and enteric nerves in the guinea-pig small intestine. Cell Tissue Res. 295 (1999) 247-256
158. Wang X.Y., Ward S.M., Gerthoffer W.T., and Sanders K.M. PKC-epsilon translocation in enteric neurons and interstitial cells of Cajal in response to muscarinic stimulation. Am. J. Physiol., Gastrointest. Liver Physiol. 285 (2003) G593-G601
159. Ward S.M. Interstitial cells of Cajal in enteric neurotransmission. Gut 47 Suppl. 4 (2000) iv40-iv43
160. Ward S.M., and Sanders K.M. Interstitial cells of Cajal: primary targets of enteric motor innervation. Anat. Rec. 262 (2001) 125-135
161. Ward S.M., and Sanders K.M. Physiology and pathophysiology of the interstitial cell of Cajal: from bench to bedside. I. Functional development and plasticity of interstitial cells of Cajal networks. Am. J. Physiol., Gastrointest. Liver Physiol. 281 (2001) G602-G611
162. Ward S.M., and Sanders K.M. Involvement of intramuscular interstitial cells of Cajal in neuroeffector transmission in the gastrointestinal tract. J. Physiol. 576 (2006) 675-682
163. Ward S.M., Burke E.P., and Sanders K.M. Use of rhodamine 123 to label and lesion interstitial cells of Cajal in canine colonic circular muscle. Anat. Embryol. Berl. 182 (1990) 215-224
164. Ward S.M., Burns A.J., Torihashi S., and Sanders K.M. Mutation of the proto-oncogene c-kit blocks development of interstitial cells and electrical rhythmicity in murine intestine. J. Physiol. 480 Pt. 1 (1994) 91-97
165. Ward S.M., Burns A.J., Torihashi S., Harney S.C., and Sanders K.M. Impaired development of interstitial cells and intestinal electrical rhythmicity in steel mutants. Am. J. Physiol. 269 (1995) C1577-C1585
166. Ward S.M., Morris G., Reese L., Wang X.Y., and Sanders K.M. Interstitial cells of Cajal mediate enteric inhibitory neurotransmission in the lower esophageal and pyloric sphincters. Gastroenterology 115 (1998) 314-329
167. Ward S.M., Beckett E.A., Wang X., Baker F., Khoyi M., and Sanders K.M. Interstitial cells of Cajal mediate cholinergic neurotransmission from enteric motor neurons. J. Neurosci. 20 (2000) 1393-1403
168. Won K.J., Sanders K.M., and Ward S.M. Interstitial cells of Cajal mediate mechanosensitive responses in the stomach. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 14913-14918
169. 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 (1977) 171-201
170. Young H.M., Ciampoli D., Johnson P.J., and Stebbing M.J. Inhibitory transmission to the longitudinal muscle of the mouse caecum is mediated largely by nitric oxide acting via soluble guanylyl cyclase. J. Auton. Nerv. Syst. 61 (1996) 103-108
171. Zhang S.C., and Fedoroff S. Cellular localization of stem cell factor and c-kit receptor in the mouse nervous system. J. Neurosci. Res. 47 (1997) 1-15