Gastrointestinal dysfunction and enteric neurotoxicity following treatment with anticancer chemotherapeutic agent 5-fluorouracil

Neurogastroenterology and Motility

Volumn 28, Issue 12, 2016, Pages 1861-1875

  McQuade, R M ^a,b   Stojanovska, V ^a,b   Donald, E ^a,b   Abalo, R ^c   Bornstein, J C ^d   Nurgali, K ^a,b  

^a VICTORIA UNIVERSITY   (Australia)

^b SUNSHINE HOSPITAL   (Australia)

^c UNIVERSIDAD REY JUAN CARLOS   (Spain)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

5 fluorouracil; 5 FU; colonic motility; enteric neuropathy; gastrointestinal transit; myenteric neurons

Indexed keywords

CD45 ANTIGEN; FLUOROURACIL; NEURONAL NITRIC OXIDE SYNTHASE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; ANTINEOPLASTIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; COLON; COLON MOTILITY; CONTROLLED STUDY; DIGESTIVE SYSTEM FUNCTION DISORDER; ENTERITIS; EX VIVO STUDY; GASTROINTESTINAL TOXICITY; GASTROINTESTINAL TRANSIT; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INTESTINAL DYSMOTILITY; INTESTINE CONTRACTION; LEUKOCYTE; LONG TERM EXPOSURE; MALE; MOUSE; MYENTERIC PLEXUS; NERVE CELL; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RADIOGRAPHY; ANIMAL; CHEMICALLY INDUCED; DIAGNOSTIC IMAGING; DRUG EFFECTS; GASTROINTESTINAL DISEASE; INTESTINE INNERVATION; ORGAN CULTURE TECHNIQUE; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS; COLON; ENTERIC NERVOUS SYSTEM; FLUOROURACIL; GASTROINTESTINAL DISEASES; GASTROINTESTINAL TRANSIT; MALE; MICE; MICE, INBRED BALB C; ORGAN CULTURE TECHNIQUES;

EID: 84977649149     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/nmo.12890     Document Type: Article

References (55)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. Cancer J Clin 2011; 61: 69–90.
2. Haggar FA, Boushey RP. Colorectal cancer epidemiology: incidence, mortality, survival, and risk factors. Clin Colon Rectal Surg 2009; 22: 191.
3. Siegel R, DeSantis C, Jemal A. Colorectal cancer statistics, 2014. Cancer J Clin 2014; 64: 104–17.
4. World Health Organization. CancerStats cancer worldwide. London, UK: Cancer Research UK, 2011.
5. Kanas GP, Taylor A, Primrose JN, Langeberg WJ, Kelsh MA, Mowat FS, Alexander DD, Choti MA et al. Survival after liver resection in metastatic colorectal cancer: review and meta-analysis of prognostic factors. Clin Epidemiol 2012; 4: 283.
6. Binefa G, Rodríguez-Moranta F, Teule À, Medina-Hayas M. Colorectal cancer: from prevention to personalized medicine. World J Gastroenterol 2014; 20: 6786.
7. Goldberg RM. Advances in the treatment of metastatic colorectal cancer. Oncologist 2005; 10: 40–8.
8. Wohlhueter RM, McIvor RS, Plagemann PG. Facilitated transport of uracil and 5-fluorouracil, and permeation of orotic acid into cultured mammalian cells. J Cell Physiol 1980; 104: 309–19.
9. Longley DB, Harkin DP, Johnston PG. 5-fluorouracil: mechanisms of action and clinical strategies. Nat Rev Cancer 2003; 3: 330–8.
10. Giacchetti S, Perpoint B, Zidani R, Le Bail N, Faggiuolo R, Focan C, Chollet P, Llory JF et al. Phase III multicenter randomized trial of oxaliplatin added to chronomodulated fluorouracil–leucovorin as first-line treatment of metastatic colorectal cancer. J Clin Oncol 2000; 18: 136.
11. Douillard JY, Cunningham D, Roth AD, Navarro M, James RD, Karasek P, Jandik P, Iveson T et al. Irinotecan combined with fluorouracil compared with fluorouracil alone as first-line treatment for metastatic colorectal cancer: a multicentre randomised trial. Lancet 2000; 355: 1041–7.
12. Duncan M, Grant G. Oral and intestinal mucositis—causes and possible treatments. Aliment Pharmacol Ther 2003; 18: 853–74.
13. Soares PMG, Mota JMSC, Gomes AS, Oliveira RB, Assreuy AMS, Brito GAC, Santos AA, Ribeiro RA et al. Gastrointestinal dysmotility in 5-fluorouracil-induced intestinal mucositis outlasts inflammatory process resolution. Cancer Chemother Pharmacol 2008; 63: 91–8.
14. Furness JB. The enteric nervous system and neurogastroenterology. Nat Rev Gastroenterol Hepatol 2012; 9: 286–94.
15. Wafai L, Taher M, Jovanovska V, Bornstein JC, Dass CR, Nurgali K. Effects of oxaliplatin on mouse myenteric neurons and colonic motility. Front Neurosci 2013; 7: 30.
16. Vera G, Castillo M, Cabezos PA, Chiarlone A, Martín MI, Gori A, Pasquinelli G, Barbara G et al. Enteric neuropathy evoked by repeated cisplatin in the rat. Neurogastroenterol Motil 2011; 23: 370–e163.
17. Reagan-Shaw S, Nihal M, Ahmad N. Dose translation from animal to human studies revisited. FASEB J 2008; 22: 659–61.
18. Cao Z, Zhang Z, Huang Z, Wang R, Yang A, Liao L, Du J. Antitumor and immunomodulatory effects of low-dose 5-FU on hepatoma 22 tumor-bearing mice. Oncol Lett 2014; 7: 1260–4.
19. Cabezos PA, Vera G, Castillo M, Fernández-Pujol R, Martín MI, Abalo R. Radiological study of gastrointestinal motor activity after acute cisplatin in the rat. Temporal relationship with pica. Auton Neurosci 2008; 141: 54–65.
20. Cabezos P, Vera G, Martín-fontelles M, Fernández-pujol R, Abalo R. Cisplatin-induced gastrointestinal dysmotility is aggravated after chronic administration in the rat. Comparison with pica. Neurogastroenterol Motil 2010; 22: 797–e225.
21. Girón R, Pérez-García I, Abalo R. X-ray analysis of gastrointestinal motility in conscious mice. Effects of morphine and comparison with rats. Neurogastroenterol Motil 2016; 28: 74–84.
22. Roberts RR, Murphy JF, Young HM, Bornstein JC. Development of colonic motility in the neonatal mouse-studies using spatiotemporal maps. Am J Physiol Gastrointest Liver Physiol 2007; 292: G930–8.
23. Roberts RR, Bornstein JC, Bergner AJ, Young HM. Disturbances of colonic motility in mouse models of Hirschsprung's disease. Am J Physiol Gastrointest Liver Physiol 2008; 294: G996–1008.
24. Spencer N, Bywater R. Enteric nerve stimulation evokes a premature colonic migrating motor complex in mouse. Neurogastroenterol Motil 2002; 14: 657–65.
25. Gwynne RM, Thomas E, Goh S, Sjövall H, Bornstein J. Segmentation induced by intraluminal fatty acid in isolated guinea-pig duodenum and jejunum. J Physiol 2004; 556: 557–69.
26. Nurgali K, Qu Z, Hunne B, Thacker M, Pontell L, Furness JB. Morphological and functional changes in guinea-pig neurons projecting to the ileal mucosa at early stages after inflammatory damage. J Physiol 2011; 589: 325–39.
27. Robinson AM, Sakkal S, Park A, Jovanovska V, Payne NL, Carbone SE, Miller S, Bornstein JC et al. Mesenchymal stem cells and conditioned medium avert enteric neuropathy and colon dysfunction in guinea pig TNBS-induced colitis. Am J Physiol Gastrointest Liver Physiol 2014; 307: G1115–29.
28. Keating DJ, Spencer NJ. Release of 5-hydroxytryptamine from the mucosa is not required for the generation or propagation of colonic migrating motor complexes. Gastroenterology 2010; 138: 659–70. e652.
29. Bachman MA, Miller VL, Weiser JN. Mucosal lipocalin 2 has pro-inflammatory and iron-sequestering effects in response to bacterial enterobactin. PLoS Pathog 2009; 5: e1000622.
30. Chassaing B, Srinivasan G, Delgado MA, Young AN, Gewirtz AT, Vijay-Kumar M. Fecal lipocalin 2, a sensitive and broadly dynamic non-invasive biomarker for intestinal inflammation. PLoS ONE 2012; 7: e44328.
31. Cao S, Frank C, Rustum YM. Role of fluoropyrimidine schedule and (6R, S) leucovorin dose in a preclinical animal model of colorectal carcinoma. J Natl Cancer Inst 1996; 88: 430–6.
32. Cao S, Rustum YM, Spector T. 5-Ethynyluracil (776C85): modulation of 5-fluorouracil efficacy and therapeutic index in rats bearing advanced colorectal carcinoma. Cancer Res 1994; 54: 1507–10.
33. De Jonge WJ, Van Den Wijngaard RM, The FO, Ter Beek ML, Bennink RJ, Tytgat GNJ, Buijs RM et al. Postoperative ileus is maintained by intestinal immune infiltrates that activate inhibitory neural pathways in mice. Gastroenterology 2003; 125: 1137–47.
34. Kindt S, Tertychnyy A, De Hertogh G, Geboes K, Tack J. Intestinal immune activation in presumed post-infectious functional dyspepsia. Neurogastroenterol Motil 2009; 21: 832–e856.
35. Van Der Voort IR, Osmanoglou E, Seybold M, Heymann-Mönnikes I, Tebbe J, Wiedenmann B, Klapp BF, Mönnikes H. Electrogastrography as a diagnostic tool for delayed gastric emptying in functional dyspepsia and irritable bowel syndrome. Neurogastroenterol Motil 2003; 15: 467–73.
36. Annese V, Bassotti G, Napolitano G, Frusciante V, Bruno M, Conoscitore P, Germani U, Morelli A et al. Gastric emptying of solids in patients with nonobstructive Crohn's disease is sometimes delayed. J Clin Gastroenterol 1995; 21: 279–82.
37. Grill BB, Lange R, Markowitz R, Hillemeier AC, McCallum RW, Gryboski JD. Delayed gastric emptying in children with Crohn's disease. J Clin Gastroenterol 1985; 7: 216–26.
38. De Schepper HU, De Man JG, Van Nassauw L, Timmermans J-P, Herman AG, Pelckmans PA, De Winter BY. Acute distal colitis impairs gastric emptying in rats via an extrinsic neuronal reflex pathway involving the pelvic nerve. Gut 2007; 56: 195–202.
39. Cottone L, Capobianco A, Gualteroni C, Perrotta C, Bianchi ME, Rovere-Querini P, Manfredi AA. 5-Fluorouracil causes leukocytes attraction in the peritoneal cavity by activating autophagy and HMGB1 release in colon carcinoma cells. Int J Cancer 2015; 136: 1381–9.
40. Akiho H, Deng Y, Blennerhassett P, Kanbayashi H, Collins SM. Mechanisms underlying the maintenance of muscle hypercontractility in a model of postinfective gut dysfunction. Gastroenterology 2005; 129: 131–41.
41. Moreels TG, De Man JG, Bogers JJ, De Winter BY, Vrolix G, Herman AG, Van Marck EA, Pelckmans PA. Effect of Schistosoma mansoni-induced granulomatous inflammation on murine gastrointestinal motility. Am J Physiol Gastrointest Liver Physiol 2001; 280: G1030–42.
42. O'Hara JR, Lomax AE, Mawe GM, Sharkey KA. Ileitis alters neuronal and enteroendocrine signalling in guinea pig distal colon. Gut 2007; 56: 186–94.
43. Demedts I, Geboes K, Kindt S, Vanden Berghe P, Andrioli A, Janssens J, Tack J. Neural mechanisms of early postinflammatory dysmotility in rat small intestine. Neurogastroenterol Motil 2006; 18: 1102–11.
44. Barnes KJ, Spencer NJ. Can colonic migrating motor complexes occur in mice lacking the endothelin-3 gene? Clin Exp Pharmacol Physiol 2015; 42: 485–95.
45. Ro S, Hwang SJ, Muto M, Jewett WK, Spencer NJ. Anatomic modifications in the enteric nervous system of piebald mice and physiological consequences to colonic motor activity. Am J Physiol Gastrointest Liver Physiol 2006; 290: G710–8.
46. Huizinga JD, Chen J-H. The myogenic and neurogenic components of the rhythmic segmentation motor patterns of the intestine. Front Neurosci 2014; 8: 78.
47. Fung C, Ellis M, Bornstein JC. Luminal cholera toxin alters motility in isolated guinea-pig jejunum via a pathway independent of 5-HT3 receptors. Front Neurosci 2010; 4: 162.
48. Foong JPP, Tough IR, Cox HM, Bornstein JC. Properties of cholinergic and non-cholinergic submucosal neurons along the mouse colon. J Physiol 2014; 592: 777–93.
49. Lomax A, Fernandez E, Sharkey K. Plasticity of the enteric nervous system during intestinal inflammation. Neurogastroenterol Motil 2005; 17: 4–15.
50. Lomax AE, O'Hara JR, Hyland NP, Mawe GM, Sharkey KA. Persistent alterations to enteric neural signaling in the guinea pig colon following the resolution of colitis. Am J Physiol Gastrointest Liver Physiol 2007; 292: G482–91.
51. Linden DR, Sharkey KA, Mawe GM. Enhanced excitability of myenteric AH neurones in the inflamed guinea-pig distal colon. J Physiol 2003; 547: 589–601.
52. Krauter E, Strong D, Brooks E, Linden D, Sharkey K, Mawe G. Changes in colonic motility and the electrophysiological properties of myenteric neurons persist following recovery from trinitrobenzene sulfonic acid colitis in the guinea pig. Neurogastroenterol Motil 2007; 19: 990–1000.
53. Nurgali K, Nguyen TV, Matsuyama H, Thacker M, Robbins HL, Furness JB. Phenotypic changes of morphologically identified guinea-pig myenteric neurons following intestinal inflammation. J Physiol 2007; 583: 593–609.
54. Nurgali K, Nguyen TV, Thacker M, Pontell L, Furness JB. Slow synaptic transmission in myenteric AH neurons from the inflamed guinea pig ileum. Am J Physiol Gastrointest Liver Physiol 2009; 297: G582–93.
55. Stojanovska V, Sakkal S, Nurgali K. Platinum-based chemotherapy: gastrointestinal immunomodulation and enteric nervous system toxicity. Am J Physiol Gastrointest Liver Physiol 2015; 308: G223–32.