Epidermal growth factor upregulates serotonin transporter and its association with visceral hypersensitivity in irritable bowel syndrome

World Journal of Gastroenterology

Volumn 20, Issue 37, 2014, Pages 13521-13529

  Cui, Xiu Fang ^a   Zhou, Wei Mei ^a   Yang, Yan ^a   Zhou, Jun ^a   Li, Xue Liang ^a   Lin, Lin ^a   Zhang, Hong Jie ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

Author keywords

Epidermal growth factor; Intestinal epithelial cells; Irritable bowel syndrome; Rat models; Rat small intestinal epithelial cells; Serotonin transporter; Visceral hypersensitivity

Indexed keywords

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; MESSENGER RNA; SEROTONIN; SEROTONIN TRANSPORTER; ACETIC ACID; EGFR PROTEIN, RAT; ENZYME INHIBITOR; SLC6A4 PROTEIN, RAT;

ABDOMINAL REFLEX; ABDOMINAL WALL MUSCULATURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLON; CONTROLLED STUDY; DISEASE ASSOCIATION; ELECTROMYOGRAPHY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTERNAL OBLIQUE MUSCLE; GENE EXPRESSION REGULATION; INTESTINAL DYSMOTILITY; INTESTINE EPITHELIUM CELL; IRRITABLE COLON; MALE; NEWBORN; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; REAL TIME POLYMERASE CHAIN REACTION; TISSUE LEVEL; UPREGULATION; VISCERAL HYPERSENSITIVITY; WESTERN BLOTTING; WITHDRAWAL REFLEX; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; CELL LINE; CHEMICALLY INDUCED; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; EPITHELIUM CELL; GENETICS; HYPERALGESIA; INNERVATION; INTESTINE; METABOLISM; PAIN THRESHOLD; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TIME; VISCERAL PAIN;

ACETIC ACID; ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; EPIDERMAL GROWTH FACTOR; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HYPERALGESIA; INTESTINES; IRRITABLE BOWEL SYNDROME; MALE; PAIN THRESHOLD; RATS, SPRAGUE-DAWLEY; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, MESSENGER; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SIGNAL TRANSDUCTION; TIME FACTORS; VISCERAL PAIN;

EID: 84910007034     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i37.13521     Document Type: Article

References (33)

1. Talley NJ, Spiller R. Irritable bowel syndrome: a little understood organic bowel disease? Lancet 2002; 360: 555-564 [PMID: 12241674 DOI: 10.1016/S0140-6736(02)09712-X]
2. Yan C, Xin-Guang L, Hua-Hong W, Jun-Xia L, Yi-Xuan L. Effect of the 5-HT4 receptor and serotonin transporter on visceral hypersensitivity in rats. Braz J Med Biol Res 2012; 45: 948-954 [PMID: 22832600 DOI: 10.1590/S0100-879X2012007500122]
3. Miwa J, Echizen H, Matsueda K, Umeda N. Patients with constipation-predominant irritable bowel syndrome (IBS) may have elevated serotonin concentrations in colonic mucosa as compared with diarrhea-predominant patients and subjects with normal bowel habits. Digestion 2001; 63: 188-194 [PMID: 11351146 DOI: 10.1159/000051888]
4. Stasi C, Bellini M, Bassotti G, Blandizzi C, Milani S. Serotonin receptors and their role in the pathophysiology and therapy of irritable bowel syndrome. Tech Coloproctol 2014; 18: 613-621 [PMID: 24425100 DOI: 10.1007/s10151-013-1106-8]
5. Coates MD, Mahoney CR, Linden DR, Sampson JE, Chen J, Blaszyk H, Crowell MD, Sharkey KA, Gershon MD, Mawe GM, Moses PL. Molecular defects in mucosal serotonin content and decreased serotonin reuptake transporter in ulcerative colitis and irritable bowel syndrome. Gastroenterology 2004; 126: 1657-1664 [PMID: 15188158 DOI: 10.1053/j.gastro.2004.03.013]
6. Dunlop SP, Coleman NS, Blackshaw E, Perkins AC, Singh G, Marsden CA, Spiller RC. Abnormalities of 5-hydroxytryptamine metabolism in irritable bowel syndrome. Clin Gastroenterol Hepatol 2005; 3: 349-357 [PMID: 15822040 DOI: 10.1016/S1542-3565(04)00726-8]
7. Latorre E, Mendoza C, Matheus N, Castro M, Grasa L, Mesonero JE, Alcalde AI. IL-10 modulates serotonin transporter activity and molecular expression in intestinal epithelial cells. Cytokine 2013; 61: 778-784 [PMID: 23410504 DOI: 10.1016/j.cyto.2013.01.01]
8. Martel F, Monteiro R, Lemos C. Uptake of serotonin at the apical and basolateral membranes of human intestinal epithelial (Caco-2) cells occurs through the neuronal serotonin transporter (SERT). J Pharmacol Exp Ther 2003; 306: 355-362 [PMID: 12682218 DOI: 10.1124/jpet.103.049668]
9. Faure C, Patey N, Gauthier C, Brooks EM, Mawe GM. Serotonin signaling is altered in irritable bowel syndrome with diarrhea but not in functional dyspepsia in pediatric age patients. Gastroenterology 2010; 139: 249-258 [PMID: 20303355 DOI: 10.1053/j.gastro.2010.03.032]
10. El-Salhy M, Wendelbo I, Gundersen D. Serotonin and serotonin transporter in the rectum of patients with irritable bowel disease. Mol Med Rep 2013; 8: 451-455 [PMID: 23778763 DOI: 10.3892/mmr.2013.1525]
11. Gill RK, Anbazhagan AN, Esmaili A, Kumar A, Nazir S, Malakooti J, Alrefai WA, Saksena S. Epidermal growth factor upregulates serotonin transporter in human intestinal epithelial cells via transcriptional mechanisms. Am J Physiol Gastrointest Liver Physiol 2011; 300: G627-G636 [PMID: 21273531 DOI: 10.1152/ajpgi.00563.2010]
12. Gil C, Najib A, Aguilera J. Serotonin transport is modulated differently by tetanus toxin and growth factors. Neurochem Int 2003; 42: 535-542 [PMID: 12590935 DOI: 10.1016/S0197-0186(02)00187-0]
13. Dvorak B. Milk epidermal growth factor and gut protection. J Pediatr 2010; 156: S31-S35 [PMID: 20105663 DOI: 10.1016/j.jpeds.2009.11.018]
14. Niederlechner S, Baird C, Petrie B, Wischmeyer E, Wischmeyer PE. Epidermal growth factor receptor expression and signaling are essential in glutamine's cytoprotective mechanism in heat-stressed intestinal epithelial-6 cells. Am J Physiol Gastrointest Liver Physiol 2013; 304: G543-G552 [PMID: 23275616 DOI: 10.1152/ajpgi.00418]
15. Alexander RJ, Panja A, Kaplan-Liss E, Mayer L, Raicht RF. Expression of growth factor receptor-encoded mRNA by colonic epithelial cells is altered in inflammatory bowel disease. Dig Dis Sci 1995; 40: 485-494 [PMID: 7895532]
16. Dubé PE, Yan F, Punit S, Girish N, McElroy SJ, Washington MK, Polk DB. Epidermal growth factor receptor inhibits colitis-associated cancer in mice. J Clin Invest 2012; 122: 2780-2792 [PMID: 22772467]
17. Kerckhoffs AP, ter Linde JJ, Akkermans LM, Samsom M. SERT and TPH-1 mRNA expression are reduced in irritable bowel syndrome patients regardless of visceral sensitivity state in large intestine. Am J Physiol Gastrointest Liver Physiol 2012; 302: G1053-G1060 [PMID: 22323131 DOI: 10.1152/ajpgi.00153.2011]
18. Kerckhoffs AP, Ter Linde JJ, Akkermans LM, Samsom M. Trypsinogen IV, serotonin transporter transcript levels and serotonin content are increased in small intestine of irritable bowel syndrome patients. Neurogastroenterol Motil 2008; 20: 900-907 [PMID: 18363639 DOI: 10.1111/j.1365-2982.2008.01100.x]
19. Xu GY, Shenoy M, Winston JH, Mittal S, Pasricha PJ. P2X receptor-mediated visceral hyperalgesia in a rat model of chronic visceral hypersensitivity. Gut 2008; 57: 1230-1237 [PMID: 18270243 DOI: 10.1136/gut.2007.134221]
20. Winston J, Shenoy M, Medley D, Naniwadekar A, Pasricha PJ. The vanilloid receptor initiates and maintains colonic hypersensitivity induced by neonatal colon irritation in rats. Gastroenterology 2007; 132: 615-627 [PMID: 17258716 DOI: 10.1053/j.gastro.2006.11.014]
21. Al-Chaer ED, Kawasaki M, Pasricha PJ. A new model of chronic visceral hypersensitivity in adult rats induced by colon irritation during postnatal development. Gastroenterology 2000; 119: 1276-1285 [PMID: 11054385 DOI: 10.1053/gast.2000.19576]
22. Gulec S, Collins JF. Silencing the Menkes copper-transporting ATPase (Atp7a) gene in rat intestinal epithelial (IEC-6) cells increases iron flux via transcriptional induction of ferroportin 1 (Fpn1). J Nutr 2014; 144: 12-19 [PMID: 24174620 DOI: 10.3945/jn.113.183160]
23. Gendron FP, Mongrain S, Laprise P, McMahon S, Dubois CM, Blais M, Asselin C, Rivard N. The CDX2 transcription factor regulates furin expression during intestinal epithelial cell differentiation. Am J Physiol Gastrointest Liver Physiol 2006; 290: G310-G318 [PMID: 16239403 DOI: 10.1152/ajpgi.00217.2005]
24. Gordillo-Bastidas D, Oceguera-Contreras E, Salazar-Montes A, González-Cuevas J, Hernández-Ortega LD, Armendáriz-Borunda J. Nrf2 and Snail-1 in the prevention of experimental liver fibrosis by caffeine. World J Gastroenterol 2013; 19: 9020-9033 [PMID: 24379627 DOI: 10.3748/wjg.v19.i47.9020]
25. Koldzic-Zivanovic N, Seitz PK, Cunningham KA, Thomas ML, Hughes TK. Serotonin regulation of serotonin uptake in RN46A cells. Cell Mol Neurobiol 2006; 26: 979-987 [PMID: 16858637 DOI: 10.1007/s10571-006-9097-x]
26. Rao RK. Biologically active peptides in the gastrointestinal lumen. Life Sci 1991; 48: 1685-1704 [PMID: 2020253]
27. Rao R, Porreca F. Epidermal growth factor protects mouse ileal mucosa from Triton X-100-induced injury. Eur J Pharmacol 1996; 303: 209-212 [PMID: 8813570 DOI: 10.1016/0014-2999(96)00186-0]
28. Rao RK, Thomas DW, Pepperl S, Porreca F. Salivary epidermal growth factor plays a role in protection of ileal mucosal integrity. Dig Dis Sci 1997; 42: 2175-2181 [PMID: 9365155 DOI: 10.1023/A:1018855525989]
29. Tepperman BL, Vozzolo BL, Soper BD. Effect of maternal sialoadenectomy on ontogenic response of rat gastric mucosa to luminal H+. Am J Physiol 1993; 265: G354-G360 [PMID: 8368317]
30. Kubota N, Kiuchi Y, Nemoto M, Oyamada H, Ohno M, Funahashi H, Shioda S, Oguchi K. Regulation of serotonin transporter gene expression in human glial cells by growth factors. Eur J Pharmacol 2001; 417: 69-76 [PMID: 11301061 DOI: 10.1016/S0014-2999(01)00906-2]
31. Kekuda R, Torres-Zamorano V, Leibach FH, Ganapathy V. Human serotonin transporter: regulation by the neuroprotective agent aurintricarboxylic acid and by epidermal growth factor. J Neurochem 1997; 68: 1443-1450 [PMID: 9084414 DOI: 10.1046/j.1471-4159.1997.68041443.x]
32. McCole DF, Rogler G, Varki N, Barrett KE. Epidermal growth factor partially restores colonic ion transport responses in mouse models of chronic colitis. Gastroenterology 2005; 129: 591-608 [PMID: 16083715 DOI: 10.1016/j.gastro.2005.06.004]
33. Riegler M, Sedivy R, Sogukoglu T, Cosentini E, Bischof G, Teleky B, Feil W, Schiessel R, Hamilton G, Wenzl E. Effect of growth factors on epithelial restitution of human colonic mucosa in vitro. Scand J Gastroenterol 1997; 32: 925-932 [PMID: 9299673]