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2019 | 79 | 4 |

Tytuł artykułu

Roux‑en‑Y gastric bypass surgery triggers rapid DNA fragmentation in vagal afferent neurons in rats

Warianty tytułu

Języki publikacji

EN

Abstrakty

EN
Previous studies have shown that Roux‑en‑Y gastric bypass (RYGB), one of the most effective weight loss treatments for obesity, results in neurodegenerative responses in vagal afferent gut‑brain connection reflected by microglia activation and reduced sensory input to the nucleus tractus solitarius (NTS). However, it is not known whether RYGB‑induced microglia activation is the cause or an effect of the reported neuronal damage. Therefore, the aim of this study was to establish the order of neurodegenerative responses in vagal afferents after RYGB in the nodose ganglia (NG) and NTS in male and female rats. Sprague‑Dawley rats were fed regular chow or an energy‑dense diet for two weeks followed by RYGB or sham surgery. Twenty‑four hours later, animals were sacrificed and NG and NTS were collected. Neuronal cell damage was determined by TUNEL assay. Microglia activation was determined by quantifying the fluorescent staining against the ionizing calcium adapter‑binding molecule 1. Reorganization of vagal afferents was evaluated by fluorescent staining against isolectin 4. Results of the study revealed significantly increased DNA fragmentation in vagal neurons in the NG when observed at 24 h after RYGB. The surgery did not produce rapid changes in the density of vagal afferents and microglia activation in the NTS. These data indicate that decreased density of vagal afferents and increased microglia activation in the NTS likely ensue as a result of RYGB‑induced neuronal damage.

Słowa kluczowe

Wydawca

-

Rocznik

Tom

79

Numer

4

Opis fizyczny

p.432-444, fig.,ref.

Twórcy

autor
  • Department of Veterinary Biosciences and Diagnostic Imaging, University of Georgia, Athens, USA
  • Department of Psychology, Binghamton University, Binghamton, USA
autor
  • Department of Neural and Behavioral Sciences, College of Medicine, Pennsylvania State University, Hershey, USA
autor
  • Department of Veterinary Biosciences and Diagnostic Imaging, University of Georgia, Athens, USA

Bibliografia

  • Alamuddin N, Vetter ML, Ahima RS, Hesson  L, Ritter S, Minnick A, Faulconbridge LF, Allison KC, Sarwer DB, Chittams J (2017) Changes in fasting and prandial gut and adiposity hormones following vertical sleeve gastrectomy or Roux‑en‑Y‑gastric bypass: an 18‑month prospective study. Obes Surg 27: 1563–1572.
  • Altschuler SM, Bao X, Bieger D, Hopkins DA, Miselis RR (1989) Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol 283: 248–268.
  • Bahceci M, Gokalp D, Bahceci S, Tuzcu A, Atmaca S, Arikan S (2007) The correlation between adiposity and adiponectin, tumor necrosis factor α, interleukin‑6 and high sensitivity C‑reactive protein levels. Is adipocyte size associated with inflammation in adults? J Endocrinol Invest 30: 210–214.
  • Ballsmider L, Vaughn A, David M, Hajnal A, Di Lorenzo P, Czaja K (2015) Sleeve gastrectomy and Roux‑en‑Y gastric bypass alter the gut‑brain communication. Neural Plast 2015: 601985.
  • Berthoud HR, Shin AC, Zheng H (2011) Obesity surgery and gut–brain communication. Physiol Behav 105: 106–119.
  • Berthoud HR, Carlson N, Powley T (1991) Topography of efferent vagal innervation of the rat gastrointestinal tract. Am J Physiol 260: R200‑R207.
  • Berthoud HR, Powley TL (1992) Vagal afferent innervation of the rat fundic stomach: morphological characterization of the gastric tension receptor. J Comp Neurol 319: 261–276.
  • Broussard DL, Altschuler SM (2000) Brainstem viscerotopic organization of afferents and efferents involved in the control of swallowing. Am J Med 108: 79–86.
  • Czaja K, Burns G, Ritter R (2008) Capsaicin‑induced neuronal death and proliferation of the primary sensory neurons located in the nodose ganglia of adult rats. Neuroscience 154: 621–630.
  • Czaja K, Ritter RC, Burns GA (2006) Vagal afferent neurons projecting to the stomach and small intestine exhibit multiple N‑methyl‑D‑aspartate receptor subunit phenotypes. Brain Res 1119: 86–93.
  • Daly DM, Park SJ, Valinsky WC, Beyak MJ (2011) Impaired intestinal afferent nerve satiety signalling and vagal afferent excitability in diet induced obesity in the mouse. J Physiol 589: 2857–2870.
  • De Lartigue G, de la Serre CB, Espero E, Lee J, Raybould HE (2011) Diet‑induced obesity leads to the development of leptin resistance in vagal afferent neurons. Am J Physiol Endocrinol Metab 301: E187–E195.
  • Engin A (2017) The definition and prevalence of obesity and metabolic syndrome. Adv Exp Med Biol 960: 1–17.
  • Ferrante Jr AW (2007) Obesity‐induced inflammation: a metabolic dialogue in the language of inflammation. J Intern Med 262: 408–414.
  • Gallaher Z, Ryu V, Herzog T, Ritter R, Czaja K (2012) Changes in microglial activation within the hindbrain, nodose ganglia, and the spinal cord following subdiaphragmatic vagotomy. Neurosci Lett 513: 31–36.
  • Gallaher ZR, Ryu V, Larios RM, Sprunger LK, Czaja K (2011) Neural proliferation and restoration of neurochemical phenotypes and compromised functions following capsaicin‑induced neuronal damage in the nodose ganglion of the adult rat. Front Neurosci 5: 12.
  • Gautron L, Zechner J, Aguirre V (2013). Vagal innervation patterns following Roux‑en‑Y gastric bypass in the mouse. Int J Obes 37: 1603.
  • Hajnal A, Kovacs P, Ahmed T, Meirelles K, Lynch CJ, Cooney RN (2010) Gastric bypass surgery alters behavioral and neural taste functions for sweet taste in obese rats. Am J Physiol Gastrointest Liver Physiol 299: G967–979.
  • Hales CM, Carroll MD, Fryar CD, Ogden CL (2017) Prevalence of obesity among adults and youth: United States, 2015–2016. NCHS Data Brief 288: 1–8.
  • Hamilton RB, Norgren R (1984) Central projections of gustatory nerves in the rat. J Comp Neurol 222: 560–577.
  • Heron MP (2018) Deaths: Leading causes for 2016. Natl Vital Stat Rep 67: 1–77.
  • Kaas JH (1991) Plasticity of sensory and motor maps in adult mammals. Annu Rev Neurosci 14: 137–167.
  • Kaas JH, Collins CE (2003) Anatomic and functional reorganization of somatosensory cortex in mature primates after peripheral nerve and spinal cord injury. Adv Neurol 93: 87–95.
  • Kentish SJ, O’Donnell TA, Frisby CL, Li H, Wittert GA, Page AJ (2014) Altered gastric vagal mechanosensitivity in diet‑induced obesity persists on return to normal chow and is accompanied by increased food intake. Int J Obes 38: 636–642.
  • Kentish SJ, O’Donnell TA, Isaacs NJ, Young RL, Li H, Harrington AM, Brierley SM, Wittert GA, Blackshaw LA, Page AJ (2013) Gastric vagal afferent modulation by leptin is influenced by food intake status. J Physiol 591: 1921–1934.
  • Kirchgessner A, Gershon  M (1989) Identification of vagal efferent fibers and putative target neurons in the enteric nervous system of the rat. J Comp Neurol 285: 38–53.
  • Kizy S, Jahansouz C, Downey MC, Hevelone N, Ikramuddin S, Leslie D (2017) National trends in bariatric surgery 2012–2015: demographics, procedure selection, readmissions, and cost. Obes Surg 27: 2933–2939.
  • Kochkodan J, Telem DA, Ghaferi AA (2018) Physiologic and psychological gender differences in bariatric surgery. Surg Endosc 32: 1382–1388.
  • Künnecke B, Verry P, Bénardeau A, Von Kienlin M (2004) Quantitative body composition analysis in awake mice and rats by magnetic resonance relaxometry. Obes Res 12: 1604–1615.
  • Marques‑Vidal P, Bochud M, Bastardot F, Lüscher T, Ferrero F, Gaspoz JM, Paccaud F, Urwyler A, von Känel R, Hock C (2012) Association between inflammatory and obesity markers in a Swiss population‑based sample (CoLaus Study). Obes Facts 5: 734–744.
  • Meek CL, Lewis HB, Reimann F, Gribble FM, Park AJ (2016) The effect of bariatric surgery on gastrointestinal and pancreatic peptide hormones. Peptides 77: 28–37.
  • Moran TH, Baldessarini AR, Salorio CF, Lowery T, Schwartz GJ (1997) Vagal afferent and efferent contributions to the inhibition of food intake by cholecystokinin. Am J Physiol 272: R1245‑R1251.
  • Mulla CM, Middelbeek RJ, Patti ME (2018) Mechanisms of weight loss and improved metabolism following bariatric surgery. Ann N Y Acad Sci 1411: 53–64.
  • Navarro X, Vivó M, Valero‑Cabré A (2007) Neural plasticity after peripheral nerve injury and regeneration. Prog Neurobiol 82: 163–201.
  • Norgren R (1983) Afferent interactions of cranial nerves involved in ingestion. J Auton Nerv Syst 9: 67–77.
  • Peters JH, Gallaher ZR, Ryu V, Czaja K (2013) Withdrawal and restoration of central vagal afferents within the dorsal vagal complex following subdiaphragmatic vagotomy. J Comp Neurol 521: 3584–3599.
  • Prechtl JC, Powley TL (1990) The fiber composition of the abdominal vagus of the rat. Anat Embryol (Berl) 181: 101–115.
  • Ritter RC (2004) Gastrointestinal mechanisms of satiation for food. Physiol Behav 81: 249–273.
  • Ryu V, Gallaher Z, Czaja K (2010) Plasticity of nodose ganglion neurons after capsaicin‑and vagotomy‑induced nerve damage in adult rats. Neuroscience 167: 1227–1238.
  • Schwartz GJ (2000) The role of gastrointestinal vagal afferents in the control of food intake: current prospects. Nutrition 16: 866–873.
  • Sen T, Cawthon CR, Ihde BT, Hajnal A, DiLorenzo PM, Claire B, Czaja K (2017) Diet‑driven microbiota dysbiosis is associated with vagal remodeling and obesity. Physiol Behav 173: 305–317.
  • Shehab SA (2009) Acute and chronic sectioning of fifth lumbar spinal nerve has equivalent effects on the primary afferents of sciatic nerve in rat spinal cord. J Comp Neurol 517: 481–492.
  • Shortland PJ, Baytug B, Krzyzanowska A, McMahon SB, Priestley JV, Averill S (2006) ATF3 expression in L4 dorsal root ganglion neurons after L5 spinal nerve transection. Eur J Neurosci 23: 365–373.
  • Skandalakis J, Gray S, Soria R, Sorg J, Rowe JJ (1980) Distribution of the vagus nerve to the stomach. Am Surg 46: 130–139.
  • Vaughn AC, Cooper EM, DiLorenzo PM, O’Loughlin LJ, Konkel ME, Peters JH, Hajnal A, Sen T, Lee SH, de La Serre CB (2017) Energy‑dense diet triggers changes in gut microbiota, reorganization of gut‑brain vagal communication and increases body fat accumulation. Acta Neurobiol Exp 77: 18–30.
  • Wall J, Xu J, and Wang X (2002) Human brain plasticity: an emerging view of the multiple substrates and mechanisms that cause cortical changes and related sensory dysfunctions after injuries of sensory inputs from the body. Brain Res Rev 39: 181–215.
  • Woods SC, Seeley RJ, Rushing PA, D’Alessio D, Tso P (2003) A controlled high‑fat diet induces an obese syndrome in rats. J Nutr 133: 1081–1087.

Typ dokumentu

Bibliografia

Identyfikatory

Identyfikator YADDA

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