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Published in: Inflammation Research 9/2020

01-09-2020 | Celiac Disease | Original Research Paper

The expression levels of CHI3L1 and IL15Rα correlate with TGM2 in duodenum biopsies of patients with celiac disease

Authors: Paola Catrogiovanni, Giuseppe Musumeci, Salvatore Giunta, Rosa Imbesi, Michelino Di Rosa

Published in: Inflammation Research | Issue 9/2020

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Abstract

Objective and design

Celiac disease (CD) is an intestinal inflammatory disorder of the small intestine. Gliadins are a component of gluten and there are three main types (α, γ, and ω). Recent studies indicate that gliadin peptides are able to activate an innate immune response. IL15 is a major mediator of the innate immune response and is involved in the early alteration of CD mucosa. The chitinase molecules are highly expressed by the innate immune cells during the inflammatory processes.

Material or subjects

We analyzed several microarray datasets of PBMCs and duodenum biopsies of CD patients and healthy control subjects (HCs). We verified the modulation CHI3L1 in CD patients and correlated the expression levels to the IL15, IL15Rα, TGM2, IFNγ, and IFNGR1/2. Duodenal biopsy samples belonged to nine active and nine treated children patients (long-term effects of gliadin), and 17 adult CD patients and 10 adults HCs. We also selected 169 samples of PBMCs from 127 CD patients on adherence to a gluten-free diet (GFD) for at least 2 years and 44 HCs.

Results

Our analysis showed that CHI3L1 and IL15Rα were significantly upregulated in adult and children’s celiac duodenum biopsies. In addition, the two genes were correlated significantly both in children than in adults CD duodenum biopsies. No significant modulation was observed in PBMCs of adult CD patients compared to the HCs. The correlation analysis of the expression levels of CHI3L1 and IL15Rα compared to TGM showed significant values both in adults and in children duodenal biopsies. Furthermore, the IFNγ expression levels were positively correlated with CHI3L1 and IL15Rα. Receiver operating characteristic (ROC) analysis confirmed the diagnostic ability of CHI3L1 and IL15Rα to discriminate CD from HCs.

Conclusion

Our data suggest a role for CHI3L1 underlying the pathophysiology of CD and represent a starting point aiming to inspire new investigation that proves the possible use of CHI3L1 as a diagnostic factor and therapeutic target.
Literature
1.
go back to reference Stenman SM, Lindfors K, Korponay-Szabo IR, Lohi O, Saavalainen P, Partanen J, et al. Secretion of celiac disease autoantibodies after in vitro gliadin challenge is dependent on small-bowel mucosal transglutaminase 2-specific IgA deposits. BMC Immunol. 2008;9:6.PubMedPubMedCentral Stenman SM, Lindfors K, Korponay-Szabo IR, Lohi O, Saavalainen P, Partanen J, et al. Secretion of celiac disease autoantibodies after in vitro gliadin challenge is dependent on small-bowel mucosal transglutaminase 2-specific IgA deposits. BMC Immunol. 2008;9:6.PubMedPubMedCentral
2.
go back to reference Schuppan D, Junker Y, Barisani D. Celiac disease: from pathogenesis to novel therapies. Gastroenterology. 2009;137:1912–33.PubMed Schuppan D, Junker Y, Barisani D. Celiac disease: from pathogenesis to novel therapies. Gastroenterology. 2009;137:1912–33.PubMed
3.
go back to reference Sollid LM, Jabri B. Triggers and drivers of autoimmunity: lessons from coeliac disease. Nat Rev Immunol. 2013;13:294–302.PubMed Sollid LM, Jabri B. Triggers and drivers of autoimmunity: lessons from coeliac disease. Nat Rev Immunol. 2013;13:294–302.PubMed
4.
go back to reference Barbagallo I, Tibullo D, Di Rosa M, Giallongo C, Palumbo GA, Raciti G, et al. A cytoprotective role for the heme oxygenase-1/CO pathway during neural differentiation of human mesenchymal stem cells. J Neurosci Res. 2008;86:1927–35.PubMed Barbagallo I, Tibullo D, Di Rosa M, Giallongo C, Palumbo GA, Raciti G, et al. A cytoprotective role for the heme oxygenase-1/CO pathway during neural differentiation of human mesenchymal stem cells. J Neurosci Res. 2008;86:1927–35.PubMed
5.
go back to reference Stefanson AL, Bakovic M. Falcarinol is a potent inducer of heme oxygenase-1 and was more effective than sulforaphane in attenuating intestinal inflammation at diet-achievable doses. Oxid Med Cell Longev. 2018;2018:3153527.PubMedPubMedCentral Stefanson AL, Bakovic M. Falcarinol is a potent inducer of heme oxygenase-1 and was more effective than sulforaphane in attenuating intestinal inflammation at diet-achievable doses. Oxid Med Cell Longev. 2018;2018:3153527.PubMedPubMedCentral
6.
go back to reference Fernandez-Jimenez N, Castellanos-Rubio A, Plaza-Izurieta L, Irastorza I, Elcoroaristizabal X, Jauregi-Miguel A, et al. Coregulation and modulation of NFkappaB-related genes in celiac disease: uncovered aspects of gut mucosal inflammation. Hum Mol Genet. 2014;23:1298–310.PubMed Fernandez-Jimenez N, Castellanos-Rubio A, Plaza-Izurieta L, Irastorza I, Elcoroaristizabal X, Jauregi-Miguel A, et al. Coregulation and modulation of NFkappaB-related genes in celiac disease: uncovered aspects of gut mucosal inflammation. Hum Mol Genet. 2014;23:1298–310.PubMed
7.
go back to reference Maiuri MC, De Stefano D, Mele G, Fecarotta S, Greco L, Troncone R, et al. Nuclear factor kappa B is activated in small intestinal mucosa of celiac patients. J Mol Med (Berl). 2003;81:373–9. Maiuri MC, De Stefano D, Mele G, Fecarotta S, Greco L, Troncone R, et al. Nuclear factor kappa B is activated in small intestinal mucosa of celiac patients. J Mol Med (Berl). 2003;81:373–9.
8.
9.
go back to reference Furst DE, Emery P. Rheumatoid arthritis pathophysiology: update on emerging cytokine and cytokine-associated cell targets. Rheumatology. 2014;53:1560–9.PubMed Furst DE, Emery P. Rheumatoid arthritis pathophysiology: update on emerging cytokine and cytokine-associated cell targets. Rheumatology. 2014;53:1560–9.PubMed
10.
go back to reference Rentzos M, Rombos A. The role of IL-15 in central nervous system disorders. Acta Neurol Scand. 2012;125:77–82.PubMed Rentzos M, Rombos A. The role of IL-15 in central nervous system disorders. Acta Neurol Scand. 2012;125:77–82.PubMed
11.
go back to reference Michalak-Stoma A, Pietrzak A, Szepietowski JC, Zalewska-Janowska A, Paszkowski T, Chodorowska G. Cytokine network in psoriasis revisited. Eur Cytokine Netw. 2011;22:160–8.PubMed Michalak-Stoma A, Pietrzak A, Szepietowski JC, Zalewska-Janowska A, Paszkowski T, Chodorowska G. Cytokine network in psoriasis revisited. Eur Cytokine Netw. 2011;22:160–8.PubMed
12.
go back to reference Jabri B, de Serre NP, Cellier C, Evans K, Gache C, Carvalho C, et al. Selective expansion of intraepithelial lymphocytes expressing the HLA-E-specific natural killer receptor CD94 in celiac disease. Gastroenterology. 2000;118:867–79.PubMed Jabri B, de Serre NP, Cellier C, Evans K, Gache C, Carvalho C, et al. Selective expansion of intraepithelial lymphocytes expressing the HLA-E-specific natural killer receptor CD94 in celiac disease. Gastroenterology. 2000;118:867–79.PubMed
13.
go back to reference Mention JJ, Ben Ahmed M, Begue B, Barbe U, Verkarre V, Asnafi V, et al. Interleukin 15: a key to disrupted intraepithelial lymphocyte homeostasis and lymphomagenesis in celiac disease. Gastroenterology. 2003;125:730–45.PubMed Mention JJ, Ben Ahmed M, Begue B, Barbe U, Verkarre V, Asnafi V, et al. Interleukin 15: a key to disrupted intraepithelial lymphocyte homeostasis and lymphomagenesis in celiac disease. Gastroenterology. 2003;125:730–45.PubMed
14.
go back to reference Escudero-Hernandez C, Plaza-Izurieta L, Garrote JA, Bilbao JR, Cegec, Arranz E. Association of the IL-15 and IL-15Ralpha genes with celiac disease. Cytokine. 2017;99:73–9.PubMed Escudero-Hernandez C, Plaza-Izurieta L, Garrote JA, Bilbao JR, Cegec, Arranz E. Association of the IL-15 and IL-15Ralpha genes with celiac disease. Cytokine. 2017;99:73–9.PubMed
15.
go back to reference Maiuri L, Ciacci C, Auricchio S, Brown V, Quaratino S, Londei M. Interleukin 15 mediates epithelial changes in celiac disease. Gastroenterology. 2000;119:996–1006.PubMed Maiuri L, Ciacci C, Auricchio S, Brown V, Quaratino S, Londei M. Interleukin 15 mediates epithelial changes in celiac disease. Gastroenterology. 2000;119:996–1006.PubMed
16.
go back to reference Di Sabatino A, Ciccocioppo R, Cupelli F, Cinque B, Millimaggi D, Clarkson MM, et al. Epithelium derived interleukin 15 regulates intraepithelial lymphocyte Th1 cytokine production, cytotoxicity, and survival in coeliac disease. Gut. 2006;55:469–77.PubMedPubMedCentral Di Sabatino A, Ciccocioppo R, Cupelli F, Cinque B, Millimaggi D, Clarkson MM, et al. Epithelium derived interleukin 15 regulates intraepithelial lymphocyte Th1 cytokine production, cytotoxicity, and survival in coeliac disease. Gut. 2006;55:469–77.PubMedPubMedCentral
17.
go back to reference Chirdo FG, Millington OR, Beacock-Sharp H, Mowat AM. Immunomodulatory dendritic cells in intestinal lamina propria. Eur J Immunol. 2005;35:1831–40.PubMed Chirdo FG, Millington OR, Beacock-Sharp H, Mowat AM. Immunomodulatory dendritic cells in intestinal lamina propria. Eur J Immunol. 2005;35:1831–40.PubMed
18.
19.
go back to reference DePaolo RW, Abadie V, Tang F, Fehlner-Peach H, Hall JA, Wang W, et al. Co-adjuvant effects of retinoic acid and IL-15 induce inflammatory immunity to dietary antigens. Nature. 2011;471:220–4.PubMedPubMedCentral DePaolo RW, Abadie V, Tang F, Fehlner-Peach H, Hall JA, Wang W, et al. Co-adjuvant effects of retinoic acid and IL-15 induce inflammatory immunity to dietary antigens. Nature. 2011;471:220–4.PubMedPubMedCentral
20.
go back to reference Jabri B, Sollid LM. Tissue-mediated control of immunopathology in coeliac disease. Nat Rev Immunol. 2009;9:858–70.PubMed Jabri B, Sollid LM. Tissue-mediated control of immunopathology in coeliac disease. Nat Rev Immunol. 2009;9:858–70.PubMed
21.
go back to reference Abadie V, Kim SM, Lejeune T, Palanski BA, Ernest JD, Tastet O, et al. IL-15, gluten and HLA-DQ8 drive tissue destruction in coeliac disease. Nature. 2020;578:600–4.PubMedPubMedCentral Abadie V, Kim SM, Lejeune T, Palanski BA, Ernest JD, Tastet O, et al. IL-15, gluten and HLA-DQ8 drive tissue destruction in coeliac disease. Nature. 2020;578:600–4.PubMedPubMedCentral
22.
go back to reference Herrera-Estrella A, Chet I. Chitinases in biological control. Exs. 1999;87:171–84.PubMed Herrera-Estrella A, Chet I. Chitinases in biological control. Exs. 1999;87:171–84.PubMed
23.
go back to reference Boot RG, Blommaart EF, Swart E, Ghauharali-van der Vlugt K, Bijl N, Moe C, et al. Identification of a novel acidic mammalian chitinase distinct from chitotriosidase. J Biol Chem. 2001;276:6770–8.PubMed Boot RG, Blommaart EF, Swart E, Ghauharali-van der Vlugt K, Bijl N, Moe C, et al. Identification of a novel acidic mammalian chitinase distinct from chitotriosidase. J Biol Chem. 2001;276:6770–8.PubMed
24.
go back to reference Di Rosa M, Malaguarnera G, De Gregorio C, D'Amico F, Mazzarino MC, Malaguarnera L. Modulation of chitotriosidase during macrophage differentiation. Cell Biochem Biophys. 2013;66:239–47.PubMed Di Rosa M, Malaguarnera G, De Gregorio C, D'Amico F, Mazzarino MC, Malaguarnera L. Modulation of chitotriosidase during macrophage differentiation. Cell Biochem Biophys. 2013;66:239–47.PubMed
25.
go back to reference Malaguarnera L, Ohazuruike LN, Tsianaka C, Antic T, Di Rosa M, Malaguarnera M. Human chitotriosidase polymorphism is associated with human longevity in Mediterranean nonagenarians and centenarians. J Hum Genet. 2010;55:8–12.PubMed Malaguarnera L, Ohazuruike LN, Tsianaka C, Antic T, Di Rosa M, Malaguarnera M. Human chitotriosidase polymorphism is associated with human longevity in Mediterranean nonagenarians and centenarians. J Hum Genet. 2010;55:8–12.PubMed
26.
go back to reference Di Rosa M, Tibullo D, Cambria D, Distefano G, Saccone S, Di Raimondo F, et al. Chitotriosidase expression during monocyte-derived dendritic cells differentiation and maturation. Inflammation. 2015;38:2082–91.PubMed Di Rosa M, Tibullo D, Cambria D, Distefano G, Saccone S, Di Raimondo F, et al. Chitotriosidase expression during monocyte-derived dendritic cells differentiation and maturation. Inflammation. 2015;38:2082–91.PubMed
27.
go back to reference van Aalten DM, Komander D, Synstad B, Gaseidnes S, Peter MG, Eijsink VG. Structural insights into the catalytic mechanism of a family 18 exo-chitinase. Proc Natl Acad Sci USA. 2001;98:8979–84.PubMed van Aalten DM, Komander D, Synstad B, Gaseidnes S, Peter MG, Eijsink VG. Structural insights into the catalytic mechanism of a family 18 exo-chitinase. Proc Natl Acad Sci USA. 2001;98:8979–84.PubMed
28.
go back to reference Di Rosa M, Malaguarnera G, De Gregorio C, Drago F, Malaguarnera L. Evaluation of CHI3L-1 and CHIT-1 expression in differentiated and polarized macrophages. Inflammation. 2013;36:482–92.PubMed Di Rosa M, Malaguarnera G, De Gregorio C, Drago F, Malaguarnera L. Evaluation of CHI3L-1 and CHIT-1 expression in differentiated and polarized macrophages. Inflammation. 2013;36:482–92.PubMed
29.
go back to reference Di Rosa M, Tibullo D, Saccone S, Distefano G, Basile MS, Di Raimondo F, et al. CHI3L1 nuclear localization in monocyte derived dendritic cells. Immunobiology. 2016;221:347–56.PubMed Di Rosa M, Tibullo D, Saccone S, Distefano G, Basile MS, Di Raimondo F, et al. CHI3L1 nuclear localization in monocyte derived dendritic cells. Immunobiology. 2016;221:347–56.PubMed
30.
go back to reference Di Rosa M, Tibullo D, Vecchio M, Nunnari G, Saccone S, Di Raimondo F, et al. Determination of chitinases family during osteoclastogenesis. Bone. 2014;61:55–63.PubMed Di Rosa M, Tibullo D, Vecchio M, Nunnari G, Saccone S, Di Raimondo F, et al. Determination of chitinases family during osteoclastogenesis. Bone. 2014;61:55–63.PubMed
31.
go back to reference Tibullo D, Di Rosa M, Giallongo C, La Cava P, Parrinello NL, Romano A, et al. Bortezomib modulates CHIT1 and YKL40 in monocyte-derived osteoclast and in myeloma cells. Front Pharmacol. 2015;6:226.PubMedPubMedCentral Tibullo D, Di Rosa M, Giallongo C, La Cava P, Parrinello NL, Romano A, et al. Bortezomib modulates CHIT1 and YKL40 in monocyte-derived osteoclast and in myeloma cells. Front Pharmacol. 2015;6:226.PubMedPubMedCentral
32.
go back to reference Qiu QC, Wang L, Jin SS, Liu GF, Liu J, Ma L, et al. CHI3L1 promotes tumor progression by activating TGF-beta signaling pathway in hepatocellular carcinoma. Sci Rep. 2018;8:15029.PubMedPubMedCentral Qiu QC, Wang L, Jin SS, Liu GF, Liu J, Ma L, et al. CHI3L1 promotes tumor progression by activating TGF-beta signaling pathway in hepatocellular carcinoma. Sci Rep. 2018;8:15029.PubMedPubMedCentral
33.
go back to reference Di Rosa M, Malaguarnera L. Chitinase 3 like-1: an emerging molecule involved in diabetes and diabetic complications. Pathobiology. 2016;83:228–42.PubMed Di Rosa M, Malaguarnera L. Chitinase 3 like-1: an emerging molecule involved in diabetes and diabetic complications. Pathobiology. 2016;83:228–42.PubMed
34.
go back to reference Szychlinska MA, Trovato FM, Di Rosa M, Malaguarnera L, Puzzo L, Leonardi R, et al. Co-expression and co-localization of cartilage glycoproteins CHI3L1 and lubricin in osteoarthritic cartilage: morphological, immunohistochemical and gene expression profiles. Int J Mol Sci. 2016;17:359.PubMedPubMedCentral Szychlinska MA, Trovato FM, Di Rosa M, Malaguarnera L, Puzzo L, Leonardi R, et al. Co-expression and co-localization of cartilage glycoproteins CHI3L1 and lubricin in osteoarthritic cartilage: morphological, immunohistochemical and gene expression profiles. Int J Mol Sci. 2016;17:359.PubMedPubMedCentral
35.
go back to reference Malaguarnera L, Imbesi R, Di Rosa M, Scuto A, Castrogiovanni P, Messina A, et al. Action of prolactin, IFN-gamma, TNF-alpha and LPS on heme oxygenase-1 expression and VEGF release in human monocytes/macrophages. Int Immunopharmacol. 2005;5:1458–69.PubMed Malaguarnera L, Imbesi R, Di Rosa M, Scuto A, Castrogiovanni P, Messina A, et al. Action of prolactin, IFN-gamma, TNF-alpha and LPS on heme oxygenase-1 expression and VEGF release in human monocytes/macrophages. Int Immunopharmacol. 2005;5:1458–69.PubMed
36.
go back to reference Di Rosa M, Sanfilippo C, Libra M, Musumeci G, Malaguarnera L. Different pediatric brain tumors are associated with different gene expression profiling. Acta Histochem. 2015;117:477–85.PubMed Di Rosa M, Sanfilippo C, Libra M, Musumeci G, Malaguarnera L. Different pediatric brain tumors are associated with different gene expression profiling. Acta Histochem. 2015;117:477–85.PubMed
37.
go back to reference Di Rosa M, Szychlinska MA, Tibullo D, Malaguarnera L, Musumeci G. Expression of CHI3L1 and CHIT1 in osteoarthritic rat cartilage model. A morphological study. Eur J Histochem. 2014;58:2423.PubMedPubMedCentral Di Rosa M, Szychlinska MA, Tibullo D, Malaguarnera L, Musumeci G. Expression of CHI3L1 and CHIT1 in osteoarthritic rat cartilage model. A morphological study. Eur J Histochem. 2014;58:2423.PubMedPubMedCentral
38.
go back to reference Higashiyama M, Tomita K, Sugihara N, Nakashima H, Furuhashi H, Nishikawa M, et al. Chitinase 3-like 1 deficiency ameliorates liver fibrosis by promoting hepatic macrophage apoptosis. Hepatol Res. 2019;49:1316–28. Higashiyama M, Tomita K, Sugihara N, Nakashima H, Furuhashi H, Nishikawa M, et al. Chitinase 3-like 1 deficiency ameliorates liver fibrosis by promoting hepatic macrophage apoptosis. Hepatol Res. 2019;49:1316–28.
39.
go back to reference Kwak EJ, Hong JY, Kim MN, Kim SY, Kim SH, Park CO, et al. Chitinase 3-like 1 drives allergic skin inflammation via Th2 immunity and M2 macrophage activation. Clin Exp Allergy. 2019;49:1464–74.PubMed Kwak EJ, Hong JY, Kim MN, Kim SY, Kim SH, Park CO, et al. Chitinase 3-like 1 drives allergic skin inflammation via Th2 immunity and M2 macrophage activation. Clin Exp Allergy. 2019;49:1464–74.PubMed
40.
go back to reference Sanfilippo C, Nunnari G, Calcagno A, Malaguarnera L, Blennow K, Zetterberg H, et al. The chitinases expression is related to Simian Immunodeficiency Virus Encephalitis (SIVE) and in HIV encephalitis (HIVE). Virus Res. 2017;227:220–30.PubMed Sanfilippo C, Nunnari G, Calcagno A, Malaguarnera L, Blennow K, Zetterberg H, et al. The chitinases expression is related to Simian Immunodeficiency Virus Encephalitis (SIVE) and in HIV encephalitis (HIVE). Virus Res. 2017;227:220–30.PubMed
41.
go back to reference Scarpino M, Pinzone MR, Di Rosa M, Madeddu G, Foca E, Martellotta F, et al. Kidney disease in HIV-infected patients. Eur Rev Med Pharmacol Sci. 2013;17:2660–7.PubMed Scarpino M, Pinzone MR, Di Rosa M, Madeddu G, Foca E, Martellotta F, et al. Kidney disease in HIV-infected patients. Eur Rev Med Pharmacol Sci. 2013;17:2660–7.PubMed
42.
go back to reference Hall S, Surova Y, Ohrfelt A, Swedish Bio FS, Blennow K, Zetterberg H, et al. Longitudinal measurements of cerebrospinal fluid biomarkers in Parkinson's disease. Mov Disord. 2016;31:898–905.PubMedPubMedCentral Hall S, Surova Y, Ohrfelt A, Swedish Bio FS, Blennow K, Zetterberg H, et al. Longitudinal measurements of cerebrospinal fluid biomarkers in Parkinson's disease. Mov Disord. 2016;31:898–905.PubMedPubMedCentral
43.
go back to reference Sanfilippo C, Longo A, Lazzara F, Cambria D, Distefano G, Palumbo M, et al. CHI3L1 and CHI3L2 overexpression in motor cortex and spinal cord of sALS patients. Mol Cell Neurosci. 2017;85:162–9.PubMed Sanfilippo C, Longo A, Lazzara F, Cambria D, Distefano G, Palumbo M, et al. CHI3L1 and CHI3L2 overexpression in motor cortex and spinal cord of sALS patients. Mol Cell Neurosci. 2017;85:162–9.PubMed
44.
go back to reference Sanfilippo C, Castrogiovanni P, Imbesi R, Kazakowa M, Musumeci G, Blennow K, et al. Sex difference in CHI3L1 expression levels in human brain aging and in Alzheimer's disease. Brain Res. 2019;1720:146305.PubMed Sanfilippo C, Castrogiovanni P, Imbesi R, Kazakowa M, Musumeci G, Blennow K, et al. Sex difference in CHI3L1 expression levels in human brain aging and in Alzheimer's disease. Brain Res. 2019;1720:146305.PubMed
45.
go back to reference Sanfilippo C, Malaguarnera L, Di Rosa M. Chitinase expression in Alzheimer's disease and non-demented brains regions. J Neurol Sci. 2016;369:242–9.PubMed Sanfilippo C, Malaguarnera L, Di Rosa M. Chitinase expression in Alzheimer's disease and non-demented brains regions. J Neurol Sci. 2016;369:242–9.PubMed
46.
go back to reference Mizoguchi E. Chitinase 3-like-1 exacerbates intestinal inflammation by enhancing bacterial adhesion and invasion in colonic epithelial cells. Gastroenterology. 2006;130:398–411.PubMed Mizoguchi E. Chitinase 3-like-1 exacerbates intestinal inflammation by enhancing bacterial adhesion and invasion in colonic epithelial cells. Gastroenterology. 2006;130:398–411.PubMed
47.
go back to reference Deutschmann C, Sowa M, Murugaiyan J, Roesler U, Rober N, Conrad K, et al. Identification of chitinase-3-like protein 1 as a novel neutrophil antigenic target in Crohn's disease. J Crohns Colitis. 2019;13:894–904.PubMedPubMedCentral Deutschmann C, Sowa M, Murugaiyan J, Roesler U, Rober N, Conrad K, et al. Identification of chitinase-3-like protein 1 as a novel neutrophil antigenic target in Crohn's disease. J Crohns Colitis. 2019;13:894–904.PubMedPubMedCentral
49.
go back to reference Rempel H, Sun B, Calosing C, Pillai SK, Pulliam L. Interferon-alpha drives monocyte gene expression in chronic unsuppressed HIV-1 infection. Aids. 2010;24:1415–23.PubMedPubMedCentral Rempel H, Sun B, Calosing C, Pillai SK, Pulliam L. Interferon-alpha drives monocyte gene expression in chronic unsuppressed HIV-1 infection. Aids. 2010;24:1415–23.PubMedPubMedCentral
50.
go back to reference Castellanos-Rubio A, Santin I, Martin-Pagola A, Irastorza I, Castano L, Vitoria JC, et al. Long-term and acute effects of gliadin on small intestine of patients on potentially pathogenic networks in celiac disease. Autoimmunity. 2010;43:131–9.PubMed Castellanos-Rubio A, Santin I, Martin-Pagola A, Irastorza I, Castano L, Vitoria JC, et al. Long-term and acute effects of gliadin on small intestine of patients on potentially pathogenic networks in celiac disease. Autoimmunity. 2010;43:131–9.PubMed
51.
go back to reference Heap GA, Trynka G, Jansen RC, Bruinenberg M, Swertz MA, Dinesen LC, et al. Complex nature of SNP genotype effects on gene expression in primary human leucocytes. BMC Med Genom. 2009;2:1. Heap GA, Trynka G, Jansen RC, Bruinenberg M, Swertz MA, Dinesen LC, et al. Complex nature of SNP genotype effects on gene expression in primary human leucocytes. BMC Med Genom. 2009;2:1.
52.
go back to reference Jorgensen SF, Reims HM, Frydenlund D, Holm K, Paulsen V, Michelsen AE, et al. A cross-sectional study of the prevalence of gastrointestinal symptoms and pathology in patients with common variable immunodeficiency. Am J Gastroenterol. 2016;111:1467–75.PubMed Jorgensen SF, Reims HM, Frydenlund D, Holm K, Paulsen V, Michelsen AE, et al. A cross-sectional study of the prevalence of gastrointestinal symptoms and pathology in patients with common variable immunodeficiency. Am J Gastroenterol. 2016;111:1467–75.PubMed
53.
go back to reference Sangineto M, Graziano G, D'Amore S, Salvia R, Palasciano G, Sabba C, et al. Identification of peculiar gene expression profile in peripheral blood mononuclear cells (PBMC) of celiac patients on gluten free diet. PLoS ONE. 2018;13:e0197915.PubMedPubMedCentral Sangineto M, Graziano G, D'Amore S, Salvia R, Palasciano G, Sabba C, et al. Identification of peculiar gene expression profile in peripheral blood mononuclear cells (PBMC) of celiac patients on gluten free diet. PLoS ONE. 2018;13:e0197915.PubMedPubMedCentral
54.
go back to reference Xiao J, Cao H, Chen J. False discovery rate control incorporating phylogenetic tree increases detection power in microbiome-wide multiple testing. Bioinformatics. 2017;33:2873–81.PubMed Xiao J, Cao H, Chen J. False discovery rate control incorporating phylogenetic tree increases detection power in microbiome-wide multiple testing. Bioinformatics. 2017;33:2873–81.PubMed
55.
go back to reference Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004;3:Article3. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004;3:Article3.
56.
go back to reference Davis S, Meltzer PS. GEOquery: a bridge between the gene expression omnibus (GEO) and BioConductor. Bioinformatics. 2007;23:1846–7.PubMed Davis S, Meltzer PS. GEOquery: a bridge between the gene expression omnibus (GEO) and BioConductor. Bioinformatics. 2007;23:1846–7.PubMed
57.
go back to reference Fagone P, Nunnari G, Lazzara F, Longo A, Cambria D, Distefano G, et al. Induction of OAS gene family in HIV monocyte infected patients with high and low viral load. Antivir Res. 2016;131:66–73.PubMed Fagone P, Nunnari G, Lazzara F, Longo A, Cambria D, Distefano G, et al. Induction of OAS gene family in HIV monocyte infected patients with high and low viral load. Antivir Res. 2016;131:66–73.PubMed
58.
go back to reference Cheadle C, Vawter MP, Freed WJ, Becker KG. Analysis of microarray data using Z score transformation. J Mol Diagn. 2003;5:73–81.PubMedPubMedCentral Cheadle C, Vawter MP, Freed WJ, Becker KG. Analysis of microarray data using Z score transformation. J Mol Diagn. 2003;5:73–81.PubMedPubMedCentral
59.
go back to reference Castrogiovanni P, Li Volti G, Sanfilippo C, Tibullo D, Galvano F, Vecchio M, et al. Fasting and fast food diet play an opposite role in mice brain aging. Mol Neurobiol. 2018;55:6881–933.PubMed Castrogiovanni P, Li Volti G, Sanfilippo C, Tibullo D, Galvano F, Vecchio M, et al. Fasting and fast food diet play an opposite role in mice brain aging. Mol Neurobiol. 2018;55:6881–933.PubMed
60.
go back to reference Di Rosa M, Malaguarnera L. Genetic variants in candidate genes influencing NAFLD progression. J Mol Med. 2012;90:105–18.PubMed Di Rosa M, Malaguarnera L. Genetic variants in candidate genes influencing NAFLD progression. J Mol Med. 2012;90:105–18.PubMed
61.
go back to reference Sanfilippo C, Castrogiovanni P, Imbesi R, Tibullo D, Li Volti G, Barbagallo I, et al. Middle-aged healthy women and Alzheimer's disease patients present an overlapping of brain cell transcriptional profile. Neuroscience. 2019;406:333–44.PubMed Sanfilippo C, Castrogiovanni P, Imbesi R, Tibullo D, Li Volti G, Barbagallo I, et al. Middle-aged healthy women and Alzheimer's disease patients present an overlapping of brain cell transcriptional profile. Neuroscience. 2019;406:333–44.PubMed
62.
go back to reference Low D, DeGruttola AK, Poltrak A, Mizoguchi A, Mino-Kenudson M, Mizoguchi E. High endogenous expression of chitinase 3-like 1 and excessive epithelial proliferation with colonic tumor formation in MOLF/EiJ mice. PLoS ONE. 2015;10:e0139149.PubMedPubMedCentral Low D, DeGruttola AK, Poltrak A, Mizoguchi A, Mino-Kenudson M, Mizoguchi E. High endogenous expression of chitinase 3-like 1 and excessive epithelial proliferation with colonic tumor formation in MOLF/EiJ mice. PLoS ONE. 2015;10:e0139149.PubMedPubMedCentral
63.
go back to reference Low D, Subramaniam R, Lin L, Aomatsu T, Mizoguchi A, Ng A, et al. Chitinase 3-like 1 induces survival and proliferation of intestinal epithelial cells during chronic inflammation and colitis-associated cancer by regulating S100A9. Oncotarget. 2015;6:36535–50.PubMedPubMedCentral Low D, Subramaniam R, Lin L, Aomatsu T, Mizoguchi A, Ng A, et al. Chitinase 3-like 1 induces survival and proliferation of intestinal epithelial cells during chronic inflammation and colitis-associated cancer by regulating S100A9. Oncotarget. 2015;6:36535–50.PubMedPubMedCentral
64.
go back to reference Pascual V, Dieli-Crimi R, Lopez-Palacios N, Bodas A, Medrano LM, Nunez C. Inflammatory bowel disease and celiac disease: overlaps and differences. World J Gastroenterol. 2014;20:4846–56.PubMedPubMedCentral Pascual V, Dieli-Crimi R, Lopez-Palacios N, Bodas A, Medrano LM, Nunez C. Inflammatory bowel disease and celiac disease: overlaps and differences. World J Gastroenterol. 2014;20:4846–56.PubMedPubMedCentral
65.
go back to reference Erzin Y, Uzun H, Karatas A, Celik AF. Serum YKL-40 as a marker of disease activity and stricture formation in patients with Crohn's disease. J Gastroenterol Hepatol. 2008;23:e357–e362362.PubMed Erzin Y, Uzun H, Karatas A, Celik AF. Serum YKL-40 as a marker of disease activity and stricture formation in patients with Crohn's disease. J Gastroenterol Hepatol. 2008;23:e357–e362362.PubMed
66.
go back to reference Kawada M, Chen CC, Arihiro A, Nagatani K, Watanabe T, Mizoguchi E. Chitinase 3-like-1 enhances bacterial adhesion to colonic epithelial cells through the interaction with bacterial chitin-binding protein. Lab Investig. 2008;88:883–95.PubMed Kawada M, Chen CC, Arihiro A, Nagatani K, Watanabe T, Mizoguchi E. Chitinase 3-like-1 enhances bacterial adhesion to colonic epithelial cells through the interaction with bacterial chitin-binding protein. Lab Investig. 2008;88:883–95.PubMed
67.
go back to reference Chen CC, Llado V, Eurich K, Tran HT, Mizoguchi E. Carbohydrate-binding motif in chitinase 3-like 1 (CHI3L1/YKL-40) specifically activates Akt signaling pathway in colonic epithelial cells. Clin Immunol. 2011;140:268–75.PubMedPubMedCentral Chen CC, Llado V, Eurich K, Tran HT, Mizoguchi E. Carbohydrate-binding motif in chitinase 3-like 1 (CHI3L1/YKL-40) specifically activates Akt signaling pathway in colonic epithelial cells. Clin Immunol. 2011;140:268–75.PubMedPubMedCentral
68.
go back to reference Libreros S, Iragavarapu-Charyulu V. YKL-40/CHI3L1 drives inflammation on the road of tumor progression. J Leukoc Biol. 2015;98:931–6.PubMedPubMedCentral Libreros S, Iragavarapu-Charyulu V. YKL-40/CHI3L1 drives inflammation on the road of tumor progression. J Leukoc Biol. 2015;98:931–6.PubMedPubMedCentral
69.
go back to reference Patil NS, Hall FC, Drover S, Spurrell DR, Bos E, Cope AP, et al. Autoantigenic HCgp39 epitopes are presented by the HLA-DM-dependent presentation pathway in human B cells. J Immunol. 2001;166:33–41.PubMed Patil NS, Hall FC, Drover S, Spurrell DR, Bos E, Cope AP, et al. Autoantigenic HCgp39 epitopes are presented by the HLA-DM-dependent presentation pathway in human B cells. J Immunol. 2001;166:33–41.PubMed
70.
go back to reference Tang H, Sun Y, Shi Z, Huang H, Fang Z, Chen J, et al. YKL-40 induces IL-8 expression from bronchial epithelium via MAPK (JNK and ERK) and NF-kappaB pathways, causing bronchial smooth muscle proliferation and migration. J Immunol. 2013;190:438–46.PubMed Tang H, Sun Y, Shi Z, Huang H, Fang Z, Chen J, et al. YKL-40 induces IL-8 expression from bronchial epithelium via MAPK (JNK and ERK) and NF-kappaB pathways, causing bronchial smooth muscle proliferation and migration. J Immunol. 2013;190:438–46.PubMed
71.
go back to reference Kawada M, Seno H, Kanda K, Nakanishi Y, Akitake R, Komekado H, et al. Chitinase 3-like 1 promotes macrophage recruitment and angiogenesis in colorectal cancer. Oncogene. 2012;31:3111–233.PubMed Kawada M, Seno H, Kanda K, Nakanishi Y, Akitake R, Komekado H, et al. Chitinase 3-like 1 promotes macrophage recruitment and angiogenesis in colorectal cancer. Oncogene. 2012;31:3111–233.PubMed
Metadata
Title
The expression levels of CHI3L1 and IL15Rα correlate with TGM2 in duodenum biopsies of patients with celiac disease
Authors
Paola Catrogiovanni
Giuseppe Musumeci
Salvatore Giunta
Rosa Imbesi
Michelino Di Rosa
Publication date
01-09-2020
Publisher
Springer International Publishing
Published in
Inflammation Research / Issue 9/2020
Print ISSN: 1023-3830
Electronic ISSN: 1420-908X
DOI
https://doi.org/10.1007/s00011-020-01371-9

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