Crosstalk between Muscularis Macrophages and Enteric Neurons Regulates Gastrointestinal Motility

Aberle, 2002, wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila, Neuron, 33, 545, 10.1016/S0896-6273(02)00589-5 Abrams, 1967, Effect of the normal microbial flora on gastrointestinal motility, Proc. Soc. Exp. Biol. Med., 126, 301, 10.3181/00379727-126-32430 Anderson, 2010, Bmp2 and Bmp4 exert opposing effects in hypoxic pulmonary hypertension, Am. J. Physiol. Regul. Integr. Comp. Physiol., 298, R833, 10.1152/ajpregu.00534.2009 Anitha, 2012, Gut microbial products regulate murine gastrointestinal motility via Toll-like receptor 4 signaling, Gastroenterology, 143, 1006, 10.1053/j.gastro.2012.06.034 Boeckxstaens, 2009, Neuroimmune mechanisms in postoperative ileus, Gut, 58, 1300, 10.1136/gut.2008.169250 Bogunovic, 2007, Enteroendocrine cells express functional Toll-like receptors, Am. J. Physiol. Gastrointest. Liver Physiol., 292, G1770, 10.1152/ajpgi.00249.2006 Bogunovic, 2009, Origin of the lamina propria dendritic cell network, Immunity, 31, 513, 10.1016/j.immuni.2009.08.010 Bogunovic, 2012, Mononuclear phagocyte diversity in the intestine, Immunol. Res., 54, 37, 10.1007/s12026-012-8323-5 Bulbring, 1959, The action of 5-hydroxytryptamine, 5-hydroxytryptophan and reserpine on intestinal peristalsis in anaesthetized guinea-pigs, J. Physiol., 146, 29, 10.1113/jphysiol.1959.sp006176 Bulbring, 1959, The release of 5-hydroxytryptamine in relation to pressure exerted on the intestinal mucosa, J. Physiol., 146, 18, 10.1113/jphysiol.1959.sp006175 Chalazonitis, 2004, Bone morphogenetic protein-2 and -4 limit the number of enteric neurons but promote development of a TrkC-expressing neurotrophin-3-dependent subset, J. Neurosci., 24, 4266, 10.1523/JNEUROSCI.3688-03.2004 Chalazonitis, 2008, Bone morphogenetic protein regulation of enteric neuronal phenotypic diversity: relationship to timing of cell cycle exit, J. Comp. Neurol., 509, 474, 10.1002/cne.21770 Chalazonitis, 2011, Bone morphogenetic proteins regulate enteric gliogenesis by modulating ErbB3 signaling, Dev. Biol., 350, 64, 10.1016/j.ydbio.2010.11.017 Chow, 2011, Bone marrow CD169+ macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche, J. Exp. Med., 208, 261, 10.1084/jem.20101688 Chow, 2013, CD169+ macrophages provide a niche promoting erythropoiesis under homeostasis and stress, Nat. Med., 19, 429, 10.1038/nm.3057 Dahan, 2011, Notch-1 signaling regulates intestinal epithelial barrier function, through interaction with CD4+ T cells, in mice and humans, Gastroenterology, 140, 550, 10.1053/j.gastro.2010.10.057 Derynck, 2003, Smad-dependent and Smad-independent pathways in TGF-beta family signalling, Nature, 425, 577, 10.1038/nature02006 Eaton, 2005, LIM Kinase1 controls synaptic stability downstream of the type II BMP receptor, Neuron, 47, 695, 10.1016/j.neuron.2005.08.010 Eaton, 2002, Dynactin is necessary for synapse stabilization, Neuron, 34, 729, 10.1016/S0896-6273(02)00721-3 Faure, 2007, Visceral hypersensitivity in irritable bowel syndrome: does it really normalize over time?, Gastroenterology, 132, 464, 10.1053/j.gastro.2006.11.037 Faure, 2007, Gangliogenesis in the enteric nervous system: roles of the polysialylation of the neural cell adhesion molecule and its regulation by bone morphogenetic protein-4, Dev. Dyn., 236, 44, 10.1002/dvdy.20943 Flores-Langarica, 2005, Network of dendritic cells within the muscular layer of the mouse intestine, Proc. Natl. Acad. Sci. USA, 102, 19039, 10.1073/pnas.0504253102 Frigo, 1970, An improved method for studying the peristaltic reflex in the isolated colon, Br. J. Pharmacol., 39, 346, 10.1111/j.1476-5381.1970.tb12898.x Fu, 2006, BMP signaling regulates murine enteric nervous system precursor migration, neurite fasciculation, and patterning via altered Ncam1 polysialic acid addition, Dev. Biol., 299, 137, 10.1016/j.ydbio.2006.07.016 Furness, 2012, The enteric nervous system and neurogastroenterology, Nat. Rev. Gastroenterol. Hepatol., 9, 286, 10.1038/nrgastro.2012.32 Goldstein, 2005, BMP signaling is necessary for neural crest cell migration and ganglion formation in the enteric nervous system, Mech. Dev., 122, 821, 10.1016/j.mod.2005.03.003 Greter, 2012, Stroma-derived interleukin-34 controls the development and maintenance of langerhans cells and the maintenance of microglia, Immunity, 37, 1050, 10.1016/j.immuni.2012.11.001 Gustafsson, 1970, Effects of microbial contamination on the cecum enlargement of germfree rats, Scand. J. Gastroenterol., 5, 309, 10.1080/00365521.1970.12096595 Hashimoto, 2011, Pretransplant CSF-1 therapy expands recipient macrophages and ameliorates GVHD after allogeneic hematopoietic cell transplantation, J. Exp. Med., 208, 1069, 10.1084/jem.20101709 Hashimoto, 2011, Dendritic cell and macrophage heterogeneity in vivo, Immunity, 35, 323, 10.1016/j.immuni.2011.09.007 Helbing, 2011, BMP activity controlled by BMPER regulates the proinflammatory phenotype of endothelium, Blood, 118, 5040, 10.1182/blood-2011-03-339762 Heredia, 2013, Important role of mucosal serotonin in colonic propulsion and peristaltic reflexes: in vitro analyses in mice lacking tryptophan hydroxylase 1, J. Physiol., 591, 5939, 10.1113/jphysiol.2013.256230 Hoffman, 2010, Natural Helicobacter infection modulates mouse intestinal muscularis macrophage responses, Cell Biochem. Funct., 28, 686, 10.1002/cbf.1709 Hogan, 1996, Bone morphogenetic proteins: multifunctional regulators of vertebrate development, Genes Dev., 10, 1580, 10.1101/gad.10.13.1580 Huizinga, 1995, W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity, Nature, 373, 347, 10.1038/373347a0 Huynh, 2009, Colony stimulating factor-1 dependence of paneth cell development in the mouse small intestine, Gastroenterology, 137, 136, 10.1053/j.gastro.2009.03.004 Kirsch, 2000, BMP-2 antagonists emerge from alterations in the low-affinity binding epitope for receptor BMPR-II, EMBO J., 19, 3314, 10.1093/emboj/19.13.3314 Li, 2006, Physiological modulation of intestinal motility by enteric dopaminergic neurons and the D2 receptor: analysis of dopamine receptor expression, location, development, and function in wild-type and knock-out mice, J. Neurosci., 26, 2798, 10.1523/JNEUROSCI.4720-05.2006 Li, 2011, Essential roles of enteric neuronal serotonin in gastrointestinal motility and the development/survival of enteric dopaminergic neurons, J. Neurosci., 31, 8998, 10.1523/JNEUROSCI.6684-10.2011 Lin, 2008, Discovery of a cytokine and its receptor by functional screening of the extracellular proteome, Science, 320, 807, 10.1126/science.1154370 Lindberg, 2009, Full-thickness biopsy findings in chronic intestinal pseudo-obstruction and enteric dysmotility, Gut, 58, 1084, 10.1136/gut.2008.148296 Mikkelsen, 2010, Interstitial cells of Cajal, macrophages and mast cells in the gut musculature: morphology, distribution, spatial and possible functional interactions, J. Cell. Mol. Med., 14, 818, 10.1111/j.1582-4934.2010.01025.x Mikkelsen, 1992, Characterization of macrophage-like cells in the external layers of human small and large intestine, Cell Tissue Res., 270, 273, 10.1007/BF00328013 Mikkelsen, 1999, Op/op mice defective in production of functional colony-stimulating factor-1 lack macrophages in muscularis externa of the small intestine, Cell Tissue Res., 295, 485, 10.1007/s004410051254 Mikkelsen, 1985, Macrophage-like cells in the muscularis externa of mouse small intestine, Anat. Rec., 213, 77, 10.1002/ar.1092130111 Miller, 2012, Deciphering the transcriptional network of the dendritic cell lineage, Nat. Immunol., 13, 888, 10.1038/ni.2370 Nahm, 2013, Spartin regulates synaptic growth and neuronal survival by inhibiting BMP-mediated microtubule stabilization, Neuron, 77, 680, 10.1016/j.neuron.2012.12.015 Nandi, 2012, The CSF-1 receptor ligands IL-34 and CSF-1 exhibit distinct developmental brain expression patterns and regulate neural progenitor cell maintenance and maturation, Dev. Biol., 367, 100, 10.1016/j.ydbio.2012.03.026 Parkhurst, 2013, Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor, Cell, 155, 1596, 10.1016/j.cell.2013.11.030 Peralta, 2009, Small intestine bacterial overgrowth and irritable bowel syndrome-related symptoms: experience with Rifaximin, World J. Gastroenterol., 15, 2628, 10.3748/wjg.15.2628 Pimentel, 2000, Eradication of small intestinal bacterial overgrowth reduces symptoms of irritable bowel syndrome, Am. J. Gastroenterol., 95, 3503, 10.1111/j.1572-0241.2000.03368.x Pimentel, 2002, Lower frequency of MMC is found in IBS subjects with abnormal lactulose breath test, suggesting bacterial overgrowth, Dig. Dis. Sci., 47, 2639, 10.1023/A:1021039032413 Pimentel, 2003, Normalization of lactulose breath testing correlates with symptom improvement in irritable bowel syndrome. a double-blind, randomized, placebo-controlled study, Am. J. Gastroenterol., 98, 412 Rakoff-Nahoum, 2004, Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis, Cell, 118, 229, 10.1016/j.cell.2004.07.002 Reigstad, 2013, Beyond phylotyping: understanding the impact of gut microbiota on host biology, Neurogastroenterol. Motil., 25, 358, 10.1111/nmo.12134 Rumessen, 2003, Interstitial cells in the musculature of the gastrointestinal tract: Cajal and beyond, Int. Rev. Cytol., 229, 115, 10.1016/S0074-7696(03)29004-5 Sudo, 1995, Functional hierarchy of c-kit and c-fms in intramarrow production of CFU-M, Oncogene, 11, 2469 Swapna, 2012, Interplay between electrical activity and bone morphogenetic protein signaling regulates spinal neuron differentiation, Proc. Natl. Acad. Sci. USA, 109, 16336, 10.1073/pnas.1202818109 Törnblom, 2002, Full-thickness biopsy of the jejunum reveals inflammation and enteric neuropathy in irritable bowel syndrome, Gastroenterology, 123, 1972, 10.1053/gast.2002.37059 Uramatsu, 2010, Involvement of endotoxin in the mortality of mice with gut-derived sepsis due to methicillin-resistant Staphylococcus aureus, Microbiol. Immunol., 54, 330, 10.1111/j.1348-0421.2010.00217.x Wang, 2007, Drosophila spichthyin inhibits BMP signaling and regulates synaptic growth and axonal microtubules, Nat. Neurosci., 10, 177, 10.1038/nn1841 Wang, 2012, IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia, Nat. Immunol., 13, 753, 10.1038/ni.2360 Wehner, 2007, Inhibition of macrophage function prevents intestinal inflammation and postoperative ileus in rodents, Gut, 56, 176, 10.1136/gut.2005.089615 Wiktor-Jedrzejczak, 1991, Correction by CSF-1 of defects in the osteopetrotic op/op mouse suggests local, developmental, and humoral requirements for this growth factor, Exp. Hematol., 19, 1049 Wynn, 2013, Macrophage biology in development, homeostasis and disease, Nature, 496, 445, 10.1038/nature12034 Yeung, 1987, Purification of the colony-stimulating factor 1 receptor and demonstration of its tyrosine kinase activity, Proc. Natl. Acad. Sci. USA, 84, 1268, 10.1073/pnas.84.5.1268 Yu, 2008, Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism, Nat. Chem. Biol., 4, 33, 10.1038/nchembio.2007.54 Zhang, 1996, Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development, Development, 122, 2977, 10.1242/dev.122.10.2977