497
Views
13
CrossRef citations to date
0
Altmetric
Review Article

Candidate mucosal and surrogate biomarkers of inflammatory bowel disease in the era of new technology

&
Pages 1407-1417 | Received 13 Aug 2011, Accepted 21 Sep 2011, Published online: 01 Nov 2011

References

  • Kaser A, Zeissig S, Blumberg. Inflammatory bowel disease. Ann Rev Immunol 2010;28:573–621.
  • Mendoza JL, Abreu MT. Biological markers in inflammatory bowel disease. Practical considerations for clinicians. Gastroenterol Clin Biol 2009;33(Suppl 3):S 158–73.
  • Atkinson AJ, Colburn WA, DeGruttola VG, DeMets DL, Downing GJ, Hoth DF, Biomarkers and surrogate endpoints. Preferred definitions and conceptual framework. Clin Pharmacol Ther 2001;69:85–95.
  • Editorial. Valid concerns. Nature 2010;463:7280.
  • Guanglin C, Olsen T, Christiansen I, Vonen B, Florholmen J, Goll R. Improvement of real-time polymerase chain reaction for quantifying TNF-alpha mRNA expression in inflamed colorectal mucosa: An approach to optimize procedures for clinical use. Scand J Clin Lab Invest 2006;66:249–60.
  • Neuman MG. Immune dysfunction in inflammatory bowel disease. Transl Res 2007;149:173–86.
  • Torres MI, Rios A. Current view of the immunopathogenesis in inflammatory bowel disease and its implications for therapy. World J Gatroenterol 2008;14:1972–80.
  • Scaldaferri F, Correale C, Gasbarrini A, Danese S. Mucosal biomarkers in inflammatory bowel disease: key pathogenic players or disease predictors? World J Gastroenterol 2010;16:2616–25.
  • Roda G, Caponi A, Benevento M, Nanni P, Mezzanotte L, Belluzzi A, Mayer L, Roda A. New proteomic approaches for biomarker discovery in inflammatory bowel disease. Inflamm Bowel Dis 2010;16:1239–46.
  • Himmel ME, Hardenberg G, Piccirillo CA, Steiner TS, Levings MK. The role of T-regulatory cells and Toll-like receptors in the pathogenesis of human inflammatory bowel disease. Immunology 2008;125:145–53.
  • Rietdijk ST, Burwell T, Bertin J, Coyle AJ. Sensing intracellular pathogens-NOD-like receptors. Curr Opin Pharmacol 2008;8:261–6.
  • Fuss IJ. Is the Th1/Th2 paradigm of immune regulation applicable to IBD? Inflamm Bowel Dis 2008;4:S110-12.
  • Dong C. TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat Rev Immunol 2008;8:337–48.
  • Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005;6:1123–32.
  • Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005;6:1133–41.
  • Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006;441:235–8.
  • Bettelli E, Oukka M, Kuchroo VK. T(H)-17 cells in the circle of immunity and autoimmunity. Nat Immunol 2007;8:345–50.
  • Dong C. Diversification of T-helper-cell lineages: finding the family root of IL-17-producing cells. Nat Rev Immunol 2006;6:329–33.
  • Hovhannisyan Z, Treatman J, Littman DR, Mayer L. Characterization of interleukin-17-producing regulatory T cells in inflamed intestinal mucosa from patients with inflammatory bowel diseases. Gastroenterology 2011;140:957–65.
  • Steinman L. A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage. Nat Med 2007;13:139–45.
  • Maloy KJ. The Interleukin-23/Interleukin-17 axis in intestinal inflammation. J Intern Med 2008;263:584–90.
  • Uhlig HH, McKenzie BS, Hue S, Thompson C, Joyce-Shaikh B, Stepankova R, Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology. Immunity 2006;25:309–18.
  • Sarra M, Pallone F, MacDonald TT, Monteleone G. IL-23/IL-17 axis in IBD. Inflamm Bowel Dis 2010;16:1808–13.
  • Yu QT, Saruta M, Avanesyan A, Fleshner PR, Banham AH, Papadakis KA. Expression and functional characterization of FOXP3+ CD4+ regulatory T cells in ulcerative colitis. Inflamm Bowel Dis 2007; 13:191–9.
  • Grundtner P, Gruber S, Murray SS, Vermeire S, Rutgeerts P, Decker T, The IL-10R1 S138G loss-of-function allele and ulcerative colitis. Genes Immun 2009;10:84–92.
  • Boschetti G, Nancey S, Sardi F, Roblin X, Flourié B, Kaiserlian D. Therapy with anti-TNFα antibody enhances number and function of Foxp3(+) regulatory T cells in inflammatory bowel diseases. Inflamm Bowel Dis 2011; 17:60–70.
  • Cario E. Toll-like receptors in inflammatory bowel disease. A decade later. Inflamm Bowel Dis 2010;16:1583–97.
  • Yamamoto-Furusho JK, Podolsky DK. Innate immunity in inflammatory bowel disease. World J Gastroenterol 2007;13:5577–80.
  • Akazawa A, Sakaida I, Higaki S, Kubo Y, Uchida K, Okita K. Increased expression of tumor necrosis factor-alpha messenger RNA in the intestinal mucosa of inflammatory bowel disease, particularly in patients with disease in the inactive phase. J Gastroenterol 2002;37:345–53.
  • Olsen T, Goll R, Cui G, Husebekk A, Vonen B, Birketvedt GS, Florholmen J. Tissue levels of tumor necrosis factor-alpha correlates with grade of inflammation in untreated ulcerative colitis. Scand J Gastroenterol 2007;42:1312–20.
  • Dionne S, Hiscott J, D'Agata I, Duhaime A, Seidman EG. Quantitative PCR analysis of TNF-alpha and IL-1 beta mRNA levels in pediatric IBD mucosal biopsies. Dig Dis Sci 1997;42:1557–66.
  • Schmidt C, Giese T. Hermann E, Zeuzem S, Meuer SC, Stallmach A. Predictive value of mucosal TNF-alpha transcripts in steroid-refractory Crohn's disease patients receiving intensive immunosuppressive therapy. Inflamm Bowel Dis 2007;13:65–70.
  • Olsen T, Goll R, Cui G, Christiansen I, Florholmen J. TNF-alpha gene expression in colorectal mucosa as a predictor of remission after induction therapy with infliximab in ulcerative colitis. Cytokine 2009;46:222–7.
  • Arsenescu R, Bruno ME, Rogier EW, Stefka AT, McMahan AE, Wright TB, Signature biomarkers in Crohn's disease: toward a molecular classification. Mucosal Immunol 2008;1:399–411.
  • Ishiguro Y. Mucosal proinflammatory cytokine production correlates with endoscopic activity of ulcerative colitis. J Gastroenterol 1999;34:66–74.
  • Raddatz D, Bockemühl M, Ramadori G. Quantitative measurement of cytokine mRNA in inflammatory bowel disease: relation to clinical and endoscopic activity and outcome. Eur J Gastroenterol Hepatol 2005;17:547–57.
  • Olsen T, Rismo R, Goll R, Goll R, Cui G, Christiansen I, Florholmen J. Normalization of Mucosal TNF-alpha as a criterion when to stop treatment with anti TNF in UC patients? A preliminary report. JCC 2001;5:29.
  • Arijs I, Li K, Toedter G, Quintens R, Van Lommel L, Van Steen K, Mucosal gene signatures to predict response to infliximab in patients with ulcerative colitis. Gut 2009;58:1612–9.
  • Strober W, Zhang F, Kitani A, Fuss I, Fichtner-Feigl S. Proinflammatory cytokines underlying the inflammation of Crohn's disease. Curr Opin Gastroenterol 2010; 26:310–17.
  • Kobayashi T, Okamoto S, Hisamatsu T, Kamada N, Chinen H, Saito R, Kitazume MT, IL23 differentially regulates the Th1/Th17 balance in ulcerative colitis and Crohn's disease. Gut 2008;57:1682–9.
  • Olsen T, Rismo R (equal contribution), Guanglin C, Goll R, Christiansen I, Husebekk A, Florholmen J. Th1 and Th17 interactions in untreated inflamed mucosa of inflammatory bowel disease, and their potential to mediate the inflammation. Cytokine 2011 Sep 23. [Epub ahead of print]
  • Agnholt J, Dahlerup JF, Buntzen S, Tøttrup A, Nielsen SL, Lundorf E. Response, relapse and mucosal immune regulation after infliximab treatment in fistulating Crohn's disease. Aliment Pharmacol Ther 2003;17:703–10.
  • León AJ, Gómez E, Garrote JA, Bernardo D, Barrera A, Marcos JL, High levels of proinflammatory cytokines, but not markers of tissue injury, in unaffected intestinal areas from patients with IBD. Mediators Inflamm 2009;2009:580450.
  • Dionne S, D'Agata ID, Hiscott J, Vanounou T, Seidman EG. Colonic explant production of IL-1and its receptor antagonist is imbalanced in inflammatory bowel disease (IBD). Clin Exp Immunol 1998;112:435–42.
  • Atreya R, Neurath MF. Involvement of IL_6 in the pathogenesis of inflammatory bowel disease and colon cancer. Clin Rev Allergy Immunol 2005;28:187–95.
  • Fujino S, Andoh A, Bamba S, Ogawa A, Hata K, Araki Y, Increased expression of interleukin 17 in inflammatory bowel disease. Gut 2003;52:65–70.
  • Olsen T, Rismo R, Goll R, Cui G, Christiansen I, Florholmen J. IL-17 gene expression in colorectal mucosa as a predictor of remission after induction therapy with infliximab in ulcerative colitis. Inflamm Bowel Dis 2011;16(Suppl 17):29.
  • Jürgens M, Laubender RP, Hartl F, Weidinger M, Seiderer J, Wagner J, Disease activity, ANCA, and IL23R genotype status determine early response to infliximab in patients with ulcerative colitis. Am J Gastroenterol 2010;105:1811–19.
  • Lawrance IC, Maxwell L, Doe W. Inflammation location, but not type, determines the increase in TGF-beta1 and IGF-1 expression and collagen deposition in IBD intestine. Inflamm Bowel Dis 2001;7:16–26.
  • Akagi S, Hiyama E, Imamura Y, Takesue Y, Matsuura Y, Yokoyama T. Interleukin-10 expression in intestine of Crohn disease. Int J Mol Med 2000;5:389–95.
  • Nielsen OH, Køppen T, Rüdiger N, Horn T, Eriksen J, Kirman I. Involvement of interleukin-4 and -10 in inflammatory bowel disease. Dig Dis Sci 1996;41:1786–93.
  • Olsen T, Cui G, Goll R, Husebekk A, Florholmen J. Infliximab therapy decreases the levels of TNF-alpha and IFN-gamma mRNA in colonic mucosa of ulcerative colitis. Scand J Gastroenterol 2009;44:727–35.
  • Danese S, Semeraro S, Marini M, Roberto I, Armuzzi A, Papa A, Gasbarrini A. Adhesion molecules in inflammatory bowel disease: therapeutic implications for gut inflammation. Dig Liver Dis 2005;37:811–18.
  • Raddatz D, Middel P, Bockemühl M, Benöhr P, Wissmann C, Schwörer H, Ramadori G. Glucocorticoid receptor expression in inflammatory bowel disease: evidence for a mucosal down-regulation in steroid-unresponsive ulcerative colitis. Aliment Pharmacol Ther 2004;19:47–61.
  • Nikolaus S, Raedler A, Kühbacker T, Sfikas N, Fölsch UR, Schreiber S. Mechanisms in failure of infliximab for Crohn's disease. Lancet 2000;356:1475–9.
  • Zimmerman NP, Vongsa RA, Wendt MK, Dwinell MB. Chemokines and chemokine receptors in mucosal homeostasis at the intestinal epithelial barrier in inflammatory bowel disease. Inflamm Bowel Dis 2008;14:1000–11.
  • Atreya R, Neurath MF. Chemokines in inflammatory bowel disease. Dig Dis 2010;28:386–94.
  • Zahn A, Giese T, Karner M, Braun A, Hinz U, Stremmel W, Ehehalt R. Transcript levels of different cytokines and chemokines correlate with clinical and endoscopic activity in ulcerative colitis. BMC Gastroenterol 2009;9:13.
  • Izzo RS, Witkon K, Chen AI, Hadjiyane C, Weinstein MI, Pellecchia C. Interleukin-8 and neutrophil markers in colonic mucosa from patients with ulcerative colitis. Am J Gastroenterol 1992;87:1447–52.
  • Yamamoto T, Umegae S, Kitagawa T, Matsumoto K. Systemic and local cytokine production in quiescent ulcerative colitis and its relationship to future relapse: a prospective pilot study. Inflam Bowel Dis 2005;11:589–96.
  • Blair SA, Kane SV, Clayburgh DR, Turner JR. Epithelial myosin light chain kinase expression and activity are upregulated in inflammatory bowel disease. Lab Invest 2006;86:191–201.
  • Palatka K, Serfozo Z, Veréb Z, Hargitay Z, Lontay B, Erdodi F, Changes in the expression and distribution of the inducible and endothelial nitric oxide synthase in mucosal biopsy specimens of inflammatory bowel disease. Scand J Gastroenterol 2005;40:670–80.
  • Menchén L, Colón AL, Madrigal JL, Beltrán L, Botella S, Lizasoain I, Activity of inducible and neuronal nitric oxide synthases in colonic mucosa predicts progression of ulcerative colitis. Am J Gastroenterol 2004;99:1756–64.
  • von Lampe B, Barthel B, Coupland SE, Riecken EO, Rosewicz S. Differential expression of matrix metalloproteinases and their tissue inhibitors in colon mucosa of patients with inflammatory bowel disease. Gut 2000;47:63–73.
  • Ravi A, Garg P, Sitaraman SV. Matrix metalloproteinases in inflammatory bowel disease: boon or a bane? Inflamm Bowel Dis 2007;13:97–107.
  • Mäkitalo L, Sipponen T, Kärkkäinen P, Kolho KL, Saarialho-Kere U. Changes in matrix metalloproteinase (MMP) and tissue inhibitors of metalloproteinases (TIMP) expression profile in Crohn's disease after immunosuppressive treatment correlate with histological score and calprotectin values. Int J Colorectal Dis 2009,24:1157–67.
  • Meijer MJ, Mieremet-Ooms MA, van Duijn W, van der Zon AM, Hanemaaijer R, Verheijen JH, Effect of the anti-tumor necrosis factor-alpha antibody infliximab on the ex vivo mucosal matrix metalloproteinase-proteolytic phenotype in inflammatory bowel disease. Inflamm Bowel Dis 2007;13:200–10.
  • Silva MA, López CB, Riverin F, Oligny L, Menezes J, Seidman EG. Characterization and distribution of colonic dendritic cells in Crohn's disease. Inflamm Bowel Dis 2004;10:504–12.
  • Maul J, Loddenkemper C, Mundt P, Berg E, Giese T, Stallmach A, Peripheral and intestinal regulatory CD4+ CD25(high) T cells in inflammatory bowel disease. Gastroenterology 2005;128:1868–78.
  • Baert FJ, D'Haens GR, Peeters M, Hiele MI, Schaible TF, Shealy D, Tumor necrosis factor alpha antibody (infliximab) therapy profoundly down-regulates the inflammation in Crohn's ileocolitis. Gastroenterology 1999;116:22–8.
  • Franke A, McGovern DP, Barrett JC, Wang K, Radford-Smith GL, Ahmad T, Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat Genet 2011;43:246–52.
  • Franke A, McGovern DP, Barrett JC, Wang K, Radford-Smith GL, Ahmad T, Genome-wide metaanalysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat Genet 2010;42:1118–25.
  • Hlavaty T, Pierik M, Henckaerts L, Ferrante M, Joossens S, van Schuerbeek N, Polymorphisms in apoptosis genes predict response to infliximab therapy in luminal and fistulizing Crohn's disease. Aliment Pharmacol Ther 2005;22:613–26.
  • Dubinsky MC, Mei L, Friedman M, Dhere T, Haritunians T, Hakonarson H, Genome wide association (GWA) predictors of anti-TNFalpha therapeutic responsiveness in pediatric inflammatory bowel disease. Inflamm Bowel Dis 2010;16:1357–66.
  • Meuwis MA, Fillet M, Geurts P, de Seny D, Lutteri L, Chapelle JP, Biomarker discovery for inflammatory bowel disease, using proreomic serum profiling. Biochem Pharmacol 2007;73:1422–33.
  • Meuwis MA, Fillet M, Chapelle JP, Malaise M, Louis E, Merville MP. New biomarkers of Crohn's disease: serum biomarkers and development of diagnostic tools. Expert Rev Diagn 2008;8:327–37.
  • Lin HM, Helsby NA, Rowan DD, Ferguson LR. Using metabolomic analysis to understand inflammatory bowel diseases. Inflamm Bowel Dis 2011;17:1021–9.
  • Bjerrum JT, Nielsen OH, Hao F, Tang H, Nicholson JK, Wang Y, Olsen J. Metabonomics in ulcerative colitis: diagnostics, biomarker identification, and insight into the pathophysiology. Proteome Res 2010;9:954–62.
  • Marchesi JR, Holmes E, Khan F, Kochhar S, Scanlan P, Shanahan F, Rapid and noninvasive metabonomic characterization of inflammatory bowel disease. J Proteome Res 2007;6:546–51.
  • Jansson J, Willing B, Lucio M, Fekete A, Dicksved J, Halfvarson J, Metabolomics reveals metabolic biomarkers of Crohn's disease. PLoS One 2009;28:e6386.
  • Martinez-Borra J, Lopez-Larrea C, Gonzalez S, Fuentes D, Dieguez A, Deschamps EM, High serum tumor necrosis factor-alpha levels are associated with lack of response to infliximab in fistulizing Crohn's disease. Am J Gastroenterol 2002;97:2350–6.
  • Kato S, Ochiai M, Sakurada T, Ohno S, Miyamoto K, Sagara M, Increased expression of long pentraxin PTX3 in inflammatory bowel diseases. Dig Dis Sci 2008;53:1910–6.
  • Savchenko AS, Inoue A, Ohashi R, Jiang S, Hasegawa G, Tanaka T, Long pentraxin 3 (PTX3) expression and release by neutrophils in vitro and in ulcerative colitis. Pathol Int 2011;61:290–7.
  • Chung-Faye G, Hayee B, Maestranzi S, Donaldson N, Forgacs I, Sherwood R. Fecal M2-pyruvate kinase (M2-PK): a novel marker of intestinal inflammation. Inflamm Bowel Dis 2007;13:1374–8.
  • Turner D, Leach ST, Mack D, Uusoue K, McLernon R, Hyams J, Faecal calprotectin, lactoferrin, M2-pyruvate kinase and S100A12 in severe ulcerative colitis: a prospective multicentre comparison of predicting outcomes and monitoring response. Gut 2010;59:1207–12.
  • Sylvester FA, Turner D, Draghi A 2nd, Uuosoe K, McLernon R, Koproske K, Fecal osteoprotegerin may guide the introduction of second-line therapy in hospitalized children with ulcerative colitis. Inflamm Bowel Dis 2010. [Epub ahead of print].
  • Nahidi L, Leach ST, Sidler MA, Levin A, Lemberg DA, Day AS. Osteoprotegerin in pediatric Crohn's disease and the effects of exclusive enteral nutrition. Inflamm Bowel Dis 2011;17:516–23.
  • Prior C, Bollbach R, Fuchs D, Hausen A, Judmaier G, Niederwieser D, Urinary neopterin, a marker of clinical activity in patients with Crohn's disease. Clin Chim Acta 1986;155:11–21.
  • Nancey S, Perret-Liaudet A, Moussata D, Graber I, Boschetti G, Renaud B, Urinary neopterin is a valuable tool in monitoring Crohn's disease activity. Inflamm Bowel Dis 2008;14:1548–54.
  • Nielsen BS, Borregaard N, Bundgaard JR, Timshel S, Sehested M, Kjeldsen L. Induction of NGAL synthesis in epithelial cells of human colorectal neoplasia and inflammatory bowel diseases. Gut 1996;38:414–20.
  • Bolignano D, Bolignano A, Della Torre A, Lacquaniti G, Costantino W, Fries M. Buemi. Neutrophil Gelatinase-associated Lipocalin (NGAL) levels in patients with Crohn's disease undergoing treatment with infliximab. J Investig Med 2010;58:569–71.
  • Stanke-Labesque F, Pofelski J, Moreau-Gaudry A, Bessard G, Bonaz B. Urinary Leukotriene E4 excretion: a biomarker of inflammatory bowel disease activity. Inflamm Bowel Dis 2008;14:769–74.
  • Manfredi MA, Zurakowski D, Rufo PA, Walker TR, Fox VL, Moses MA. Increased incidence of urinary matrix metalloproteinases as predictors of disease in pediatric patients with inflammatory bowel disease. Inflamm Bowel Dis 2008;14:1091–6.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.