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Neural Plasticity in the Gastrointestinal Tract: Chronic Inflammation, Neurotrophic Signals, and Hypersensitivity

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Neural Plasticity in the Gastrointestinal Tract: Chronic Inflammation, Neurotrophic Signals, and Hypersensitivity Acta Neuropathol DOI 10.1007/s00401-013-1099-4 REVIEW Neural plasticity in the gastrointestinal tract: chronic inflammation, neurotrophic signals, and hypersensitivity Ihsan Ekin Demir • Karl-Herbert Scha¨fer • Elke Tieftrunk • Helmut Friess • Gu¨ralp O. Ceyhan Received: 11 September 2012 / Revised: 31 January 2013 / Accepted: 7 February 2013 Ó Springer-Verlag Berlin Heidelberg 2013 Abstract Neural plasticity is not only the adaptive inflammatory, infectious, neoplastic/malignant, or degen- response of the central nervous system to learning, struc- erative—neural plasticity in the GI tract primarily occurs in tural damage or sensory deprivation, but also an the presence of chronic tissue- and neuro-inflammation. It increasingly recognized common feature of the gastroin- seems that studying the abundant trophic and activating testinal (GI) nervous system during pathological states. signals which are generated during this neuro-immune- Indeed, nearly all chronic GI disorders exhibit a disease- crosstalk represents the key to understand the remarkable stage-dependent, structural and functional neuroplasticity. neuroplasticity of the GI tract. At structural level, GI neuroplasticity usually comprises local tissue hyperinnervation (neural sprouting, neural, and Keywords Neural plasticity Á Gastrointestinal tract Á ganglionic hypertrophy) next to hypoinnervated areas, a Enteric nervous system Á Neuro-inflammation Á switch in the neurochemical (neurotransmitter/neuropep- Hypersensitivity Á Pain tide) code toward preferential expression of neuropeptides which are frequently present in nociceptive neurons (e.g., substance P/SP, calcitonin-gene-related-peptide/CGRP) Introduction and of ion channels (TRPV1, TRPA1, PAR2), and con- comitant activation of peripheral neural glia. The In the peripheral nervous system, neuronal plasticity was functional counterpart of these structural alterations is described more than 100 years ago in the pioneering works altered neuronal electric activity, leading to organ dys- by Cajal and Langley [12, 56] after nerve transsection and function (e.g., impaired motility and secretion), together neuro-regeneration. In the past two decades, plasticity was with reduced sensory thresholds, resulting in hypersensi- also recognized as a striking feature of autonomic nerves in tivity and pain. The present review underlines that neural the enteric nervous system (ENS) owing to intensifying plasticity in all GI organs, starting from esophagus, stom- research in neurogastroenterology [34, 70, 110, 111]. ach, small and large intestine to liver, gallbladder, and Changes in innervation density, different neuropeptide pancreas, actually exhibits common phenotypes and release patterns, and the entailing functional disturbances mechanisms. Careful appraisal of these GI neuroplastic are detected at the same fascinating extent in the ENS as in alterations reveals that—no matter which etiology, i.e., the central nervous system (CNS) [110]. However, our knowledge on the functional implications of visceral neu- roplasticity is scarce. & I. E. Demir ( ) Á E. Tieftrunk Á H. Friess Á G. O. Ceyhan The present review aims at illustrating the various Department of Surgery, Klinikum rechts der Isar, Technische Universita¨tMu¨nchen, Ismaninger str. 22, structural and functional neuroplastic alterations in the 81675 Munich, Germany gastrointestinal (GI) tract and underlining the similarities e-mail: [email protected] between the reactions of peripheral autonomic nerves in different GI organs as a response to insult. Furthermore, the K.-H. Scha¨fer Department of Biotechnology, University of Applied Sciences so far identified functional aspects of neural plasticity in Kaiserslautern/Zweibru¨cken, Zweibrucken, Germany the GI tract are interpreted on the basis of their relevance 123 Acta Neuropathol Liver cancer (HCC, CCC): • Loss of innervation in Central Achalasia: tumor-affected tissue reorganization • Loss of neurons and areas ICC Pain • Ganglionitis Liver cirrhosis: Nutcracker esophagus: • Hypoinnervation in Hypersensitivity • Imbalance of neuro- fibrotic areas transmitters • Hyperinnervation along portal veins GERD: • Mast cell infiltration • More nociceptive fibers • NGF, GDNF, NMDA Chronic pancreatitis & • Throacic spinal neuron Pancreatic cancer: hypersensitivity • Increased neural density & • Cross-sensitization in the hypertrophy spinal cord • Neural remodelling • NR1 (NMDA) upregulation • Pancretic neuritis • Enhanced excitability Gastric cancer: • Suppression of A-type • Increase in potassium currents nociceptive fibers • TRPV1 in DRG neurons Gastroparesis: Chronic cholecystitis: • Loss of neurons & ICC • Increased neural • Activation of ATP- density & sensitive K+-channels hypertrophy Chronic gastritis: Colon cancer: • Increased neural • Hypo- and hyper- density, peri-neuritis innervation • DRG & nodose neuron hyperexcitability Chagas enteropathy: • Neuro-degeneration IBS: IBD: • Myenteric ganglionitis • Ganglionic hyperplasia • Mast cell infiltration • Ganglionic hypertrophy • NGF, BDNF and TRPV1 • Hyperplasia of glia • Decreased descending • Myenteric plexitis pain inhibition • AH and S neuron hyperexcitability Diverticulosis: • Decreased neuron and Appendicitis: glia content • Neuronal hyperplasia • Fewer ganglia • Neural hypertrophy Chronic diverticulitis: • Neuroma-like bodies • Increased neural • NGF, GAP-43 density • Mast cell infiltration • Neuro-inflammation 123 Acta Neuropathol b Fig. 1 Structural and functional neural plasticity in the gastrointes- generation of neurogenic appendicopathy [43]. In a tinal (GI) tract. Morphological analysis of nerves and intrinsic ganglia pathomorphological study on acute appendicitis, the num- within GI organs reveals that all parts of the GI tract, starting from esophagus to the distal end of the large intestine, undergo in part very ber of Schwann cells, the number and size of ganglia, and similar structural alterations during disease processes. The upward the immunoreactivity for the nerve growth factor/NGF arrows denote upregulation of the preceding factors. In contrast to the were all elevated when compared to normal appendix. well-described pathomorphological alterations of GI nerves in disease Furthermore, a significant correlation between NGF states, the concomitant functional alterations (yellow-colored text)of peripheral GI neuronal networks have not yet been understood in expression and mast cell density was noted (Fig. 1)[19]. sufficient detail. The depicted alterations are all derived from Interestingly, the density of mast cells strongly correlated experimental models of the respective diseases. AH afterhyperpolar- to the degree of neuronal hyperplasia and hypertrophy in izing, DRG dorsal root ganglia, TRPV1 transient receptor potential acute appendicitis [19]. Interconnecting nerve bundles in vanilloid 1, ATP adenosine triphosphate, cAMP cyclic adenosine monophosphate, CREB cAMP response element binding protein, the myenteric plexus were detected to be enlarged in 55 % HCC hepatocellular cancer, CCC cholangiocellular cancer, NMDA of patients who underwent appendectomy for acute N-methyl-D-aspartate, NGF nerve growth factor, GDNF glial-cell- appendicitis and also in 41 % of patients with histologi- derived neurotrophic factor, GAP-43 growth-associated-protein 43, cally normal appendix [72]. Therefore, neuroplastic ICC interstitial cells of Cajal, IBD inflammatory bowel disease. Please refer to the manuscript for the respective references alterations in the appendix seem to result from repetitive bouts of inflammation together with chronic luminal obstruction [72]. Based on the extensive neural hypertro- phy, elevated growth-associated-protein-43 (GAP-43) for the pathophysiology of pain and the progression of the content, increased presence of substance P (SP)-, vasoac- diseases with which they are associated. Finally, it aims to tive intestinal peptide (VIP)-positive nerve fibers (Table 1) emphasize that these similarities in neuroplastic reactions and the concomitant perineural inflammatory cell infiltra- of different organs seem to be generated upon a common tion, and non-acute appendicitis were suggested to be of pathomechanistic background, i.e., their predominant ‘‘neuroimmune’’ origin [26]. occurrence in states of chronic tissue inflammation, in the presence of specific peripheral neuro-inflammation and the Small and large intestine corresponding neurotrophic signals. The part of the GI tract in which visceral neuroplasticity has probably been best studied is the intestine [110]. The Structural neuroplasticity in the GI tract: tissue ENS which represents an independently functioning com- hyperinnervation and altered chemical coding ponent of the autonomic nervous system can undergo profound structural plasticity in different contexts, e.g., Owing to advances in histopathology and increased atten- during inflammation, infection, aging, and (congenital) tion toward neural alterations, pathologists reported on enteric neuropathies [110]. In this regard, inflammatory numerous structural plastic alterations in the GI tract, from bowel diseases (IBD), i.e., ulcerative colitis and Crohn’s its very proximal (oral) end to its most distal parts, i.e., disease, harbor numerous alterations in different compo- from esophagus to rectum. The following sections provide nents of the ENS [110]. In particular, both entities an overview of the so far observed structural neuroplastic frequently demonstrate hypertrophy and/or hyperplasia of alterations and associated chemical codes during the ENS
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