LRIG1 regulates ontogeny of smooth muscle-derived subsets of interstitial cells of cajal in mice

Gastroenterology

Volumn 149, Issue 2, 2015, Pages 407-419.e8

  Kondo, Jumpei ^a   Powell, Anne E ^a   Wang, Yang ^a   Musser, Melissa A ^a   Michelle Southard Smith, E ^a   Franklin, Jeffrey L ^a   Coffey, Robert J ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Development; ICC DMP; ICC SMP; Intestinal Transit

Indexed keywords

ANOCTAMIN 1; DEXTRAN; LEUCINE RICH REPEAT AND IMMUNOGLOBULIN LIKE DOMAIN PROTEIN 1; NEUROKININ 1 RECEPTOR; PROTEIN; RHODAMINE B; UNCLASSIFIED DRUG; CRE RECOMBINASE; INTEGRASE; LRIG1 PROTEIN, MOUSE; MEMBRANE PROTEIN; NERVE PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTONOMIC NERVOUS SYSTEM; CONTROLLED STUDY; GASTROINTESTINAL TRANSIT; HOMOZYGOTE; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; INTERSTITIAL CELL OF CAJAL; INTESTINAL STEM CELL; MOUSE; NONHUMAN; ONTOGENY; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SMOOTH MUSCLE FIBER; WILD TYPE; ANIMAL; CYTOLOGY; DEFICIENCY; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC RECOMBINATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; KNOCKOUT MOUSE; METABOLISM; MYENTERIC PLEXUS; SMALL INTESTINE; SMOOTH MUSCLE; SUBMUCOUS PLEXUS;

ANIMALS; FLUORESCENT ANTIBODY TECHNIQUE; HOMOZYGOTE; INTEGRASES; INTERSTITIAL CELLS OF CAJAL; INTESTINE, SMALL; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH; MYENTERIC PLEXUS; NERVE TISSUE PROTEINS; RECOMBINATION, GENETIC; SUBMUCOUS PLEXUS;

EID: 84938069108     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2015.04.018     Document Type: Article

References (42)

1. S. Torihashi, S.M. Ward, S.-I. Nishikawa, and et al. c-kit-Dependent development of interstitial cells and electrical activity in the murine gastrointestinal tract Cell Tissue Res 280 1995 97 111
2. L. Thomson, T.L. Robinson, J.C.F. Lee, and et al. Interstitial cells of Cajal generate a rhythmic pacemaker current Nat Med 4 1998 848 851
3. S. Iino, S.M. Ward, and K.M. Sanders Interstitial cells of Cajal are functionally innervated by excitatory motor neurones in the murine intestine J Physiol 556 2004 521 530
4. S. Klein, B. Seidler, A. Kettenberger, and et al. Interstitial cells of Cajal integrate excitatory and inhibitory neurotransmission with intestinal slow-wave activity Nat Commun 4 2013 1630
5. I. Gockel, J.R. Bohl, V.F. Eckardt, and et al. Reduction of interstitial cells of Cajal (ICC) associated with neuronal nitric oxide synthase (n-NOS) in patients with achalasia Am J Gastroenterol 103 2008 856 864
6. V.J. Horváth, H. Vittal, A. Lörincz, and et al. Reduced stem cell factor links smooth myopathy and loss of interstitial cells of Cajal in murine diabetic gastroparesis Gastroenterology 130 2006 759 770
7. A. Forrest, J.D. Huizinga, X.-Y. Wang, and et al. Increase in stretch-induced rhythmic motor activity in the diabetic rat colon is associated with loss of ICC of the submuscular plexus Am J Physiol Gastrointest Liver Physiol 294 2008 G315 G326
8. C. Porcher, M. Baldo, M. Henry, and et al. Deficiency of interstitial cells of Cajal in the small intestine of patients with Crohn's disease Am J Gastroenterol 97 2002 118 125
9. C.-L. He, L. Burgart, L. Wang, and et al. Decreased interstitial cell of Cajal volume in patients with slow-transit constipation Gastroenterology 118 2000 14 21
10. P. Kashyap, P.J. Gomez-Pinilla, M.J. Pozo, and et al. Immunoreactivity for Ano1 detects depletion of Kit-positive interstitial cells of Cajal in patients with slow transit constipation Neurogastroenterol Motil 23 2011 760 765
11. S. Iino, and K. Horiguchi Interstitial cells of Cajal are involved in neurotransmission in the gastrointestinal tract Acta Histochem Cytochem 39 2006 145 153
12. D. Al-Sajee, and J.D. Huizinga Interstitial cells of Cajal Sultan Qaboos Univ Med J 12 2012 411 421
13. S.M. Ward, A.J. Burns, S. Torihashi, and et al. Mutation of the proto-oncogene c-kit blocks development of interstitial cells and electrical rhythmicity in murine intestine J Physiol 480 1994 91 97
14. J.D. Huizinga, L. Thuneberg, M. Klüppel, and et al. W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity Nature 373 1995 347 349
15. X.-Y. Wang, M.-G. Vannucchi, F. Nieuwmeyer, and et al. Changes in interstitial cells of Cajal at the deep muscular plexus are associated with loss of distention-induced burst-type muscle activity in mice infected by Trichinella spiralis Am J Pathol 167 2005 437 453
16. S.M. Ward, G.J. McLaren, and K.M. Sanders Interstitial cells of Cajal in the deep muscular plexus mediate enteric motor neurotransmission in the mouse small intestine J Physiol 573 2006 147 159
17. S. Torihashi, S.M. Ward, and K.M. Sanders Development of c-Kit-positive cells and the onset of electrical rhythmicity in murine small intestine Gastroenterology 112 1997 144 155
18. S. Torihashi, K. Nishi, Y. Tokutomi, and et al. Blockade of kit signaling induces transdifferentiation of interstitial cells of Cajal to a smooth muscle phenotype Gastroenterology 117 1999 140 148
19. S. Iino, K. Horiguchi, and Y. Nojyo Wsh/Wsh c-Kit mutant mice possess interstitial cells of Cajal in the deep muscular plexus layer of the small intestine Neurosci Lett 459 2009 123 126
20. P. Chi, Y. Chen, L. Zhang, and et al. ETV1 is a lineage-specific survival factor in GIST and cooperates with KIT in oncogenesis Nature 467 2010 849 853
21. M. Klüppel, J.D. Huizinga, J. Malysz, and et al. Developmental origin and kit-dependent development of the interstitial cells of cajal in the mammalian small intestine Dev Dyn 211 1998 60 71
22. J. Han, W.-H. Shen, Y.-Z. Jiang, and et al. Distribution, development and proliferation of interstitial cells of Cajal in murine colon: an immunohistochemical study from neonatal to adult life Histochem Cell Biol 133 2010 163 175
23. M.S.F. Pellegrini Morphogenesis of the special circular muscle layer and of the interstitial cells of Cajal related to the plexus muscularis profundus of mouse intestinal muscle coat Anat Embryol (Berl) 169 1984 151 158
24. G. Gur, C. Rubin, M. Katz, and et al. LRIG1 restricts growth factor signaling by enhancing receptor ubiquitylation and degradation EMBO J 23 2004 3270 3281
25. M.B. Laederich, M. Funes-Duran, L. Yen, and et al. The leucine-rich repeat protein LRIG1 is a negative regulator of ErbB family receptor tyrosine kinases J Biol Chem 279 2004 47050 47056
26. A.E. Powell, Y. Wang, Y. Li, and et al. The Pan-ErbB negative regulator Lrig1 is an intestinal stem cell marker that functions as a tumor suppressor Cell 149 2012 146 158
27. K.B. Jensen, C.A. Collins, E. Nascimento, and et al. Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis Cell Stem Cell 4 2009 427 439
28. T. Nakamura, J. Hamuro, M. Takaishi, and et al. LRIG1 inhibits STAT3-dependent inflammation to maintain corneal homeostasis J Clin Invest 124 2014 385 397
29. E.J. Poulin, A.E. Powell, Y. Wang, and et al. Using a new Lrig1 reporter mouse to assess differences between two Lrig1 antibodies in the intestine Stem Cell Res 13 2014 422 430
30. A. Wirth, Z. Benyó, M. Lukasova, and et al. G12-G13-LARG-mediated signaling in vascular smooth muscle is required for salt-induced hypertension Nat Med 14 2008 64 68
31. S. Srinivas, T. Watanabe, C.-S. Lin, and et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus BMC Dev Biol 1 2001 4
32. M.S. Miller, J.J. Galligan, and T.F. Burks Accurate measurement of intestinal transit in the rat J Pharmacol Methods 6 1981 211 217
33. Y. Suzuki, N. Sato, M. Tohyama, and et al. cDNA Cloning of a novel membrane glycoprotein that is expressed specifically in glial cells in the mouse brain LIG-1, a protein with leucine-rich repeats and immunoglobulin-like domains J Biol Chem 271 1996 22522 22527
34. P.J. Gomez-Pinilla, S.J. Gibbons, M.R. Bardsley, and et al. Ano1 is a selective marker of interstitial cells of Cajal in the human and mouse gastrointestinal tract Am J Physiol Gastrointest Liver Physiol 296 2009 G1370 G1381
35. M.-S. Faussone-Pellegrini Relationships between neurokinin receptor-expressing interstitial cells of Cajal and tachykininergic nerves in the gut J Cell Mol Med 10 2006 20 32
36. S. Iino, K. Horiguchi, S. Horiguchi, and et al. c-Kit-negative fibroblast-like cells express platelet-derived growth factor receptor α in the murine gastrointestinal musculature Histochem Cell Biol 131 2009 691 702
37. S. Iino, and Y. Nojyo Immunohistochemical demonstration of c-Kit-negative fibroblast-like cells in murine gastrointestinal musculature Arch Histol Cytol 72 2009 107 115
38. J.B. Furness The enteric nervous system and neurogastroenterology Nat Rev Gastroenterol Hepatol 9 2012 286 294
39. K.M. Sanders, S.D. Koh, S. Ro, and et al. Regulation of gastrointestinal motility - insights from smooth muscle biology Nat Rev Gastroenterol Hepatol 9 2012 633 645
40. J.D. Huizinga, and W.J.E.P. Lammers Gut peristalsis is governed by a multitude of cooperating mechanisms Am J Physiol Gastrointest Liver Physiol 296 2009 G1 G8
41. J. Yin, and J.D.Z. Chen Roles of interstitial cells of Cajal in regulating gastrointestinal motility: in vitro versus in vivo studies J Cell Mol Med 12 2008 1118 1129
42. V.W.Y. Wong, D.E. Stange, M.E. Page, and et al. Lrig1 controls intestinal stem-cell homeostasis by negative regulation of ErbB signalling Nat Cell Biol 14 2012 401 408