TGF-β1-dependent L1CAM expression has an essential role in macrophage-induced apoptosis resistance and cell migration of human intestinal epithelial cells

Oncogene

Volumn 32, Issue 2, 2013, Pages 180-189

  Schafer H ^a   Struck, B ^a   Feldmann, E M ^a   Bergmann, F ^b   Grage Griebenow, E ^a   Geismann, C ^a   Ehlers, S ^c   Altevogt, P ^d   Sebens, S ^a  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c RESEARCH CENTER BORSTEL   (Germany)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

CD171; cellular microenvironment; colon cancer; inflammatory bowel disease

Indexed keywords

CD33 ANTIGEN; CELL ADHESION MOLECULE; COLONY STIMULATING FACTOR 1; PROTEIN L1CAM; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR SLUG; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL MIGRATION; CELL MOTILITY; CLINICAL ARTICLE; COLON BIOPSY; CONTROLLED STUDY; DISEASE DURATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTESTINE EPITHELIUM CELL; MACROPHAGE; MALE; MALIGNANT TRANSFORMATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; UPREGULATION;

ADULT; AGED; APOPTOSIS; CELL LINE; CELL MOVEMENT; CELL TRANSFORMATION, NEOPLASTIC; COCULTURE TECHNIQUES; COLORECTAL NEOPLASMS; EPITHELIAL CELLS; FEMALE; HUMANS; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; MACROPHAGES; MALE; MIDDLE AGED; MITOGEN-ACTIVATED PROTEIN KINASE 8; NEURAL CELL ADHESION MOLECULE L1; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIALIC ACID BINDING IG-LIKE LECTIN 3; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA1; YOUNG ADULT;

EID: 84872189872     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.44     Document Type: Article

References (47)

1. Xie J, Itzkowitz SH. Cancer in inflammatory bowel disease. Cancer in inflammatory bowel disease. World J Gastroenterol 2008; 14: 378-389.
2. Herszenyi L, Miheller P, Tulassy Z. Carcinogenesis in inflammatory bowel disease. Dig Dis 2007; 25: 267-269. (Pubitemid 350194181)
3. Bernstein CN, Blanchard JF, Kliewer E, Wajda A. Cancer risk in patients with inflammatory bowel disease: A population-based study. Cancer 2001; 91: 854-862. (Pubitemid 32173312)
4. Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007; 448: 427-434. (Pubitemid 47123518)
5. Roessner A, Kuester D, Malfertheiner P, Schneider-Stock R. Oxidative stress in ulcerative colitis-Associated carcinogenesis. Pathology 2008; 204: 511-524.
6. Smith PD, Ochsenbauer-Jambor C, Smithies LE. Intestinal macrophages: Unique effector cells of the innate immune systems. Immunol Rev 2005; 206: 149-159. (Pubitemid 41105168)
7. Takeda K, Clausen BE, Kaisho T, Tsujimura T, Terada N, Forster I et al. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 1999; 10: 39-49. (Pubitemid 29077382)
8. Kamada N, Hisamatsu T, Okamoto S, Sato T, Matsuoka K, Arai K et al. Abnormally differentiated subsets of intestinal macrophages play a key role in Th1-dominant chronic colitis through excess production of IL-12 and IL-23 in response to bacteria. J Immunol 2005; 175: 6900-6908. (Pubitemid 41598935)
9. Bull DM, Bookmann MA. Isolation and functional characterization of human intestinal mucosal lymphoid cells. J Clin Invest 1987; 59: 966-974.
10. Golder JP, Doe WF. Isolation and preliminary characterization of human intestinal macrophages. Gastroenterology 1983; 84: 795-802. (Pubitemid 13152629)
11. Rogler G, Andus T, Aschenbrenner E, Vogl D, Falk W, Andreesen R et al. Alterations of the phenotype of colonic macrophages in inflammatory bowel disease. Eur J Gastroenterol Hepatol 1997; 9: 893-899. (Pubitemid 27404418)
12. Smith PD, Smythies LE, Mosteller-Barnum M, Sibley DA, Russel MW, Merger M et al. Intestinal macrophages lack CD14 and CD89 and consequently are down-regulated for LPS-And IgA-mediated activities. J Immunol 2001; 167: 2651-2656. (Pubitemid 32768894)
13. Babyatsky MW, Rossiter G, Podolsky DK. Expression of transforming growth factor alpha and beta in colonic mucosa in inflammatory bowel disease. Gastroenterology 1996; 110: 975-984. (Pubitemid 26113734)
14. Stadnicki A, Machnik G, Klimacka-Nawrot E, Wolanska-Karut A, Labuzek K. Transforming growth factor-beta1 and its receptors in patients with ulcerative colitis. Int Immunopharm 2009; 9: 761-766.
15. Lawrance IC, Maxwell L, Doe W. Inflammation location, but not type, determines the increase in TGF-b1 and IGF-1 expression and collagen deposition in IBD intestine. Inflamm Bowel Dis 2001; 7: 67-75.
16. Clavel T, Haller D. Bacteria-And host-derived mechanisms to control intestinal epithelial cell homeostasis: Implications for chronic inflammation. Inflamm Bowel Dis 2007; 13: 1153-1164. (Pubitemid 47402601)
17. Wiercinska-Drapalo A, Flisiak R, Prokopowicz D. Effect of ulcerative colitis activity on plasma concentration of transforming growth factor beta1. Cytokine 2001; 14: 343-346. (Pubitemid 32730475)
18. Rezaie A, Ghorbani F, Eshghtork A, Zamani MJ, Dehghan G, Taghavi B et al. Alterations in salivary antioxidants, nictric oxide, and transforming growth factor-b1 in relation to disease activity in Crohn's disease patients. Ann NY Acad Sci 2006; 1091: 110-122. (Pubitemid 47092230)
19. Ellenrieder V, Buck A, Gress TM. TGFbeta-regulated transcriptional mechanisms in cancer. Int J Gastrointest Cancer 2002; 31: 61-69.
20. Ellenrieder V, Hendler SF, Boeck W, Seufferlein T, Menke A, Ruhland C et al. Transforming growth factor beta1 treatment leads to an epithelial- mesenchymal transdifferentiation of pancreatic cancer cells requiring extracellular signalregulated kinase 2 activation. Cancer Res 2001; 61: 4222-4228. (Pubitemid 32720992)
21. Zavadil J, Bottinger EP. TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 2005; 24: 5764-5774.
22. Geismann C, Morscheck M, Koch D, Ungefroren H, Arlt A, Tsao M-S et al. Up-regulation of L1CAM in pancreatic duct cells is transforming growth factor b1-And Slug-dependent: Role in malignant transformation of pancreatic cancer. Cancer Res 2009; 69: 4517-4526.
23. Gavert N, Conacci-Sorrell M, Gast D, Schneider A, Altevogt P, Brabletz T et al. L1, a novel target of beta-catenin signaling, transforms cells and is expressed at the invasive front of colon cancers. J Cell Biol 2005; 168: 633-642. (Pubitemid 40271028)
24. Kaifi JT, Reichelt U, Quaas A, Schurr PG, Wachowiak R, Yekebas EF et al. L1 is associated with micrometastatic spread and poor outcome in colorectal cancer. Mod Pathol 2007; 20: 1183-1190. (Pubitemid 47609067)
25. Sebens Muerkoster S, Werbing V, Sipos B, Debus MA, Witt M, Grossmann M et al. Drug-induced expression of the cellular adhesion molecule L1CAM confers antiapoptotic protection and chemoresistance in pancreatic ductal adenocarcinoma cells. Oncogene 2007; 26: 2759-2768.
26. Arlt MJ, Novak-Hofer I, Gast D, Gschwend V, Moldenhauer G, Grunberg J et al. Efficient inhibition of intra-peritoneal tumor growth and dissemination of human ovarian carcinoma cells in nude mice by anti-L1-cell adhesion molecule monoclonal antibody treatment. Cancer Res 2006; 66: 936-943. (Pubitemid 43165961)
27. Gavert N, Sheffer M, Raveh S, Spaderna S, Shtutman M, Brabletz T et al. Expression of L1-CAM and ADAM 10 in human colon cancer cells induces metastasis. Cancer Res 2007; 67: 7703-7712. (Pubitemid 47281363)
28. Huszar M, Pfeifer M, Schirmer U, Kiefel H, Konecny GE, Ben-Arie A et al. Up-regulation of L1CAM is linked to loss of hormone receptors and E-cadherin in aggressive subtypes of endometrial carcinomas. J Pathol 2010; 220: 551-561.
29. Geismann C, Arlt A, Bauer I, Pfeifer M, Altevogt P, Muerkoster SS et al. Binding of the transcription factor Slug to the L1CAM promoter is essential for transforming growth factor-b1 (TGF-b1) induced L1CAM expression in human pancreatic ductal adenocarcinoma cells. Int J Oncol 2011; 38: 257-266.
30. Stoeck A, Gast D, Sanderson MP, Issa Y, Gutwein P, Altevogt P. L1-CAM in a membrane-bound or soluble form augments protection from apoptosis in ovarian carcinoma cells. Gynecol Oncol 2007; 104: 461-469. (Pubitemid 46156956)
31. Min J-K, Kim J-M, Li S, Lee JW, Yoon H, Ryu CJ et al. L1 cell adhesion molecule is a novel therapeutic target in intrahepatic cholangiocarcinoma. Clin Cancer Res 2010; 16: 3571-3580.
32. Huszar M, Moldenhauer G, Geschwend V, Ben-Arie A, Altevogt P, Fogel M. Expression profile analysis in multiple human tumors identifies L1 (CD171) as a molecular marker for differential diagnosis and targeted therapy. Hum Pathol 2006; 37: 1000-1008. (Pubitemid 44097029)
33. Rogler G, Andus T, Aschenbrenner E, Vogl D, Falk W, Andreesen R et al. Phenotypic characterization of colonic macrophages. Clin Exp Immunol 1998; 112: 205-215.
34. Matsumoto S, Hara T, Mitsuyama K, Yamamoto M, Tsuruta O, Sata M et al. Essential roles of IL-6 trans-signaling in colonic epithelial cells, induced by the IL-6/soluble-IL-6 receptor derived from lamina propria macrophages, on the development of colitis-Associated premalignant cancer in a murine model. J Immunol 2010; 184: 1543-1551.
35. Smythies LE, Sellers M, Clements RH, Mosteller-Barnum M, Meng G, Benjamin WH et al. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J Clin Invest 2005; 115: 66-75. (Pubitemid 40385506)
36. Rahimi R, Nikfar S, Abdollahi M. Meta-Analysis technique confirms the effectiveness of anti-TNF-Alpha in the management of active ulcerative colitis when administered in combination with corticosteroids. Med Sci Monit 2002; 13: PI13-PI18. (Pubitemid 47037680)
37. Muerkoster S, Wegehenkel K, Arlt A, Witt M, Sipos B, Kruse ML et al. Tumor stroma interactions induce chemoresistance in pancreatic ductal carcinoma cells involving increased secretion and paracrine effects of nitric oxide and interleukin-1beta. Cancer Res 2004; 64: 1331-1337. (Pubitemid 38235601)
38. Hosui A, Kimura A, Yamaji D, Zhu BM, Na R, Hennighausen L. Loss of STAT5 causes liver fibrosis and cancer development through increased TGF-\{beta\} and STAT3 activation. J Exp Med 2009; 206: 819-831.
39. Gavert N, Vivanti A, Hazin J, Brabletz T, Ben-Zee'v A. L1-mediated colon cancer cell metastasis does not require changes in EMT and cancer stem cell markers. Mol Cancer Res 2011; 9: 14-24.
40. Krausgruber T, Blazek K, Smallie T, Alzabin S, Lockstone H, Sahgal N et al. IRF5 promotes inflammatory macrophages polarization and Th1-Th17 responses. Nat Immunol 2011; 12: 231-238.
41. Verreck FAW, de Boer T, Langenberg DML, van der Zanden L, Ottenhoff THM. Phenotypic and functional profiling of human proinflammatory type-1 and antiinflammatory type-2 macrophages in response to microbial antigens and IFN-A and CD40L-mediated costimulation. J Leuk Biol 2006; 79: 285-292.
42. Schiechl G, Bauer B, Fuss I, Lang SA, Moser C, Ruemmle P et al. Tumor development in murine ulcerative colitis depends on MyD88 signaling of colonic F4/80+CD11bhighGr1low macrophages. J Clin Invest 2011; 121: 1692-1708.
43. Moyer MP, Manzano LA, Merriman RL, Stauffer JS, Tanzer LR. NCM460, a normal human colon mucosal epithelial cell line. In Vitro Cell Dev Biol Anim 1996; 32: 315-317.
44. Arlt A, Bauer I, Schafmayer C, Tepel J, Muerkoster SS, Brosch M et al. Increased proteasome subunit protein expression and proteasome activity in colon cancer relate to an enhanced activation of nuclear factor E2-related factor 2 (Nrf2). Oncogene 2009; 28: 3983-3996.
45. Grage-Griebenow E, Zwatzky R, Kahlert H, Brade L, Flad H, Ernst M. Identification of a novel dendritic cell-like subset of CD64(+)/CD16(+) blood monocytes. Eur J Immunol 2001; 31: 48-56.
46. Sebens S, Bauer I, Geismann C, Grage-Griebenow E, Ehlers S, Kruse ML et al. Inflammatory macrophages induce Nrf2 transcription factor-dependent proteasome activity in colonic NCM460 cells and thereby confer anti-Apoptotic protection. J Biol Chem 2011; 286: 40911-40921.
47. Bergmann F, Wandschneider F, Sipos B, Moldenhauer G, Schniewind B, Welsch T et al. Elevated L1CAM expression in precursor lesions and primary and metastastic tissues of pancreatic ductal adenocarinoma. Oncol Rep 2010; 24: 909-915.