Altered expression of type I insulin-like growth factor receptor in Crohn's disease

[en] The fibrotic and antiapoptotic effects of insulin-like growth factors (IGF) are mediated by type I IGF receptor (IGF-1R). IGFs could play a role in intestinal stricturing and in the maintenance of inflammation in Crohn's disease (CD). We aimed to describe IGF-1R expression in CD intestinal lesions, to compare it to other intestinal inflammatory diseases and to correlate it with fibrosis and apoptosis. IGF-1R expression and apoptosis (active caspase-3) were studied by immunohistochemistry. Surgical intestinal specimens [17 CD, nine controls, six diverticulitis and four ulcerative colitis (UC)] were used. IGF-1R was expressed transmurally mainly by inflammatory cells (IC) and smooth muscle cells, both in diseased intestine and controls. IGF-1R positive IC were increased in the mucosa and the submucosa of CD (P < 0.007), and in involved areas compared to uninvolved areas (P = 0.03). In UC, the number of IGF-1R positive IC was only increased in the mucosa, and was not different from controls in the submucosa. In diverticulitis, the number of IGF-1R positive IC did not differ from controls. In CD submucosa, IGF-1R expression in IC was inversely correlated with apoptosis in uninvolved areas (P = 0.01). Expression of IGF-1R in submucosal fibroblast-like cells, subserosal adipocytes and hypertrophic nervous plexi was specific for CD. We have shown a transmural altered expression of IGF-1R in CD. This may suggest a role for IGF-1R in the maintenance of chronic inflammation and stricture formation in CD.

Disciplines :

Immunology & infectious disease
Gastroenterology & hepatology

Author, co-author :

El Yafi, F.

Winkler, Rose ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Anatomie et cytologie pathologiques

Delvenne, Philippe ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Anatomie et cytologie pathologiques

Boussif, N.

Belaiche, Jacques ; Université de Liège - ULiège > Département des sciences cliniques > Hépato-gastroentérologie

Louis, Edouard ; Université de Liège - ULiège > Département des sciences cliniques > Hépato-gastroentérologie

Language :

English

Title :

Altered expression of type I insulin-like growth factor receptor in Crohn's disease

Publication date :

March 2005

Journal title :

Clinical and Experimental Immunology

ISSN :

0009-9104

eISSN :

1365-2249

Publisher :

Blackwell Publishing Ltd, Oxford, United Kingdom

Volume :

139

Issue :

Pages :

526-533

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 26 October 2009

Statistics

Number of views

78 (1 by ULiège)

Number of downloads

168 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Boirivant M, Marini M, Di Felice G et al. Lamina propria T cells in Crohn's disease and other gastrointestinal inflammation show defective CD2 pathway-induced apoptosis. Gastroenterology 1999; 116:557-65.
Brannigan AE, O'Connell PR, Hurley H et al. Neutrophil apoptosis is delayed in patients with inflammatory bowel disease. Shock 2000; 13:361-6.
Graham MF, Diegelmann RF, Elson CO et al. Collagen content and types in the intestinal strictures of Crohn's disease. Gastroenterology 1988; 94:257-65.
Lund PK, Zimmermann EM. Insulin-like growth factors and inflammatory bowel disease. Baillière's Clin Gastroenterol 1996; 10:83-96.
Vincent AM, Feldman EL. Control of cell survival by IGF signaling pathways. Growth Horm IGF Res 2002; 12:193-7.
Jones JI, Clemmons DR. Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev 1995; 16:3-34.
Zimmermann EM, Li L, Hou YT, Cannon M, Christman GM, Bitar KN. IGF-1 induces collagen and IGFBP-5 mRNA in rat intestinal smooth muscle. Am J Physiol 1997; 273:G875-82.
Stallmach A, Schuppan D, Riese HH, Matthes H, Riecken EO. Increased collagen type III synthesis by fibroblasts isolated from strictures of patients with Crohn's disease. Gastroenterology 1992; 102:1920-9.
Simmons JG, Pucilowska JB, Lund PK. Autocrine and paracrine actions of intestinal fibroblast-derived insulin-like growth factors. Am J Physiol 1999; 276:G817-27.
Zhang S, Smartt H, Holgate ST, Roche WR. Growth factors secreted by bronchial epithelial cells control myofibroblast proliferation: an in vitro co-culture model of airway remodeling in asthma. Lab Invest 1999; 79:395-405.
Kuemmerle JF. Autocrine regulation of growth in cultured human intestinal muscle by growth factors. Gastroenterology 1997; 113:817-24.
Valentinis B, Morrione A, Peruzzi F, Prisco M, Reiss K, Baserga R. Anti-apoptotic signaling of the IGF-1 receptor in fibroblasts following loss of matrix adhesion. Oncogene 1999; 18:1827-36.
Stewart CE, Rotwein P. Insulin-like growth factor-II is an autocrine survival factor for differentiating myoblasts. J Biol Chem 1996; 271:11330-8.
Walsh PT, O'Connor R. The insulin-like growth factor-I receptor is regulated by CD28 and protects activated T cells from apoptosis. Eur J Immunol 2000; 30:1010-18.
Remacle-Bonnet MM, Garrouste FL, Heller S, Andre F, Marvaldi JL, Pommier GJ. Insulin-like growth factor I protects colon cancer cells from death factor-induced apoptosis by potentiating tumor necrosis factor alpha-induced mitogen-activated protein kinase and nuclear factor kappaB signaling pathways. Cancer Res 2000; 60:2007-17.
Okura Y, Brink M, Zahid AA, Anwar A, Delafontaine P. Decreased expression of insulin-like growth factor-1 and apoptosis of vascular smooth muscle cells in human atherosclerotic plaque. J Mol Cell Cardiol 2001; 33:1777-89.
Ghosh S, Humphreys K, Papachrysostomou M, Ferguson A. Detection of insulin-like growth factor-I and transforming growth factor-beta in whole gut lavage fluid: a novel method of studying intestinal fibrosis. Eur J Gastroenterol Hepatol 1997; 9:505-8.
Cohen JA, Zimmermann EM, Sartor RB, Lund PK. IGF-1 and IGF-2 are overexpressed in inflamed and strictured intestine in CD [Abstract]. Gastroenterology 1993; 104:A683.
Lawrance IC, Maxwell, L, Doe W. Inflammation location, but not type, determines the increase in TGF-β1 and IGF-1 expression and collagen deposition in IBD intestine. Inflamm Bowel Dis 2001; 7:16-26.
Zimmermann EM, Li L, Hou YT, Mohapatra NK, Pucilowska JB. Insulin-like growth factor I and insulin-like growth factor binding protein 5 in Crohn's disease. Am J Physiol Gastrointest Liver Physiol 2001; 280:G1022-9.
Kuemmerle JF, Murthy KS. Coupling of the insulin-like growth factor-I receptor tyrosine kinase to Gi2 in human intestinal smooth muscle. Gbetagamma-dependent mitogen activated protein kinase activation and growth. J Biol Chem 2001; 276:7187-94.
Heinz-Erian P, Kessler U, Funk B, Gais P, Kiess W. Identification and in situ localization of the insulin-like growth factor-II/mannose-6-phosphate (IGF-1I/M6P) receptor in the rat gastrointestinal tract: comparison with the IGF-1 receptor. Endocrinology 1991; 129:1769-78.
Fridman V, Humblet C, Bonjean K, Boniver J. Assessment of tumor angiogenesis in invasive breast carcinomas: absence of correlation with prognosis and pathological factors. Virchows Arch 2000; 437:611-17.
Groos S, Reale E, Luciano L. General suitability of techniques for in situ detection of apoptosis in small intestinal epithelium. Anat Rec 2003; 272A:503-13.
Pucilowska JB, McNaughton KK, Mohapatra NK et al. IGF-1 and procollagen alpha 1(I) are coexpressed in a subset of mesenchymal cells in active Crohn's disease. Am J Physiol Gastrointest Liver Physiol 2000; 279:G1307-22.
Walsh PT, Smith LM, O'Connor R. Insulin-like growth factor-1 activates Akt and Jun N-terminal kinases (JNKs) in promoting the survival of T lymphocytes. Immunology 2002; 107:461-71.
Johnson EW, Jones LA, Kozak RW. Expression and function of insulin-like growth factor receptors on anti-CDS-activated human T lymphocytes. J Immunol 1992; 148:63-71.
Fell JM, Walker-Smith JA, Spencer J, MacDonald TT. The distribution of dividing T cells throughout the intestinal wall in inflammatory bowel disease (IBD). Clin Exp Immunol 1996; 104:280-5.
Pala L, Giannini S, Rosi E et al. Direct measurement of IGF-1 and IGFBP-3 in bronchoalveolar lavage fluid from idiopathic pulmonary fibrosis. J Endocrinol Invest 2001; 24:856-64.
Wang XZ, Chen ZX, Zhang LJ et al. Expression of insulin-like growth factor 1 and insulin-like growth factor 1 receptor and it's intervention by interleukin-10 in experimental hepatic fibrosis. World J Gastroenterol 2003; 9:1287-91.
Lawrance IC, Maxwell L, Doe W. Altered response of intestinal mucosal fibroblasts to profibrogenic cytokines in inflammatory bowel disease. Inflamm Bowel Dis 2001; 7:226-36.
Krein PM, Sabatini PJ, Tinmouth W, Green FH, Winston BW. Localization of insulin-like growth factor-1 in lung tissues of patients with fibroproliferative acute respiratory distress syndrome. Am J Respir Crit Care Med 2003; 167:83-90.
Rom WN, Paakko P. Activated alveolar macrophages express the insulin-like growth factor-I receptor. Am J Respir Cell Mol Biol 1991; 4:432-9.
Lee TC, Gold LI, Reibman J et al. Immunohistochemical localization of transforming growth factor-beta and insulin-like growth factor-I in asbestosis in the sheep model. Int Arch Occup Environ Health 1997; 69:157-64.
Liu JP, Baker J, Perkins AS, Robertson EJ, Efstratiadis A. Mice carrying null mutations of the genes encoding insulin-like growth factor I (IGF-1) and type 1 IGF receptor. Cell 1993; 75:59-72.
Williams KL, Fuller CR, Fagin J, Lund PK. Mesenchymal IGF-1 overexpression: paracrine effects in the intestine, distinct from endocrine actions. Am J Physiol Gastrointest Liver Physiol 2002; 283:G875-85.
Wang J, Niu W, Nikiforov Y et al. Targeted overexpression if IGF-1 evokes distinct patterns of organ remodeling in smooth muscle cell tissue beds of transgenic mice. J Clin Invest 1997; 100:1425-39.
Sordella R, Jiang W, Chen GC, Curto M, Settleman J. Modulation of Rho GTPase signalling regulates a switch between adipogenesis and myogenesis. Cell 2003; 18:147-58.
Sheehan AL, Warren BF, Gear MW, Shepherd NA. Fat-wrapping in Crohn's disease: pathological basis and relevance to surgical practice. Br J Surg 1992; 79:955-8.
Colombel JF, Tampoli CP, Dubuquoy L. New hypothesis on fat tissue and Crohn's disease: is it time to rectify an oversight? Inflamm Bowel Dis Monitor 2003; 4:78-81.
Desreumaux P, Ernst O, Geboes K et al. Inflammation alterations in mesenteric adipose tissue in Crohn's disease. Gastroenterology 1999; 117:73-81.
D'Ercole AJ, Ye P, O'Kusky JR. Mutant mouse models of insulin-like growth factor actions in the central nervous system. Neuropeptides 2002; 36:209-20.