Iranian
Biomedical Journal
Volume 26, Issue 6 (11-2022)
IBJ 2022, 26(6): 440-453 |
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Ardalan Khales S, Aarabi A, Abbaszadegan M R, Forghanifard M M. INPP5A/HLA-G1/IL-10/MMP-21 Axis in Progression of Esophageal Squamous Cell Carcinoma. IBJ 2022; 26 (6) :440-453
URL: http://ibj.pasteur.ac.ir/article-1-4446-en.html
URL: http://ibj.pasteur.ac.ir/article-1-4446-en.html
Abstract:
Background: INPP5A is involved in different cellular events, including cell proliferation. Since INPP5A, HLAG1, IL-10, and MMP-21 genes play fundamental roles in ESCC tumorigenesis, we aimed in this study to clarify the possible interplay of these genes and explore the potential of these chemistries as a predictor marker for diagnosis in ESCC disease.
Methods: Gene expression analysis of INPP5A, HLAG-1, IL-10, and MMP-21 was performed using relative comparative real-time PCR in 56 ESCCs compared to their margin normal tissues. Immunohistochemical staining was accomplished for INPP5A in ESCCs. Analysis of ROC curves and the AUC were applied to evaluate the diagnostic capability of the candidate genes.
Results: High levels of HLA-G1, MMP-21, and IL-10 were detected in nearly 23.2%, 62.5%, and 53.5% of ESCCs compared to the normal tissues, respectively, whereas INPP5A underexpression was detected in 19.6% of ESCCs, which all tested genes indicated significant correlations with each other. The protein expression level of INPP5A in ESCC tissues was significantly lower than that of the non-tumor esophageal tissues (p = 0.001). Interestingly, the concomitant expression of the INPP5A/HLA-G1, INPP5A/MMP-21, INPP5A/IL-10, HLA-G1/MMP-21, HLA-G1/IL-10, and MMP-21/IL-10 was significantly correlated with several clinicopathological variables. INPP5A, HLA-G1, MMP-21, and IL-10 showed to be the most appropriate candidates to discriminate tumor/non-tumor groups due to the total AUCs of all combinations (>60%).
Conclusion: Our results represent a new regulatory axis containing INPP5A/HLAG-1/IL-10/MMP-21 markers in ESCC development and may provide novel insight into the mechanism of immune evasion mediated by the INPP5A/HLAG-1/IL-10/MMP-21 regulatory network in the disease.
Methods: Gene expression analysis of INPP5A, HLAG-1, IL-10, and MMP-21 was performed using relative comparative real-time PCR in 56 ESCCs compared to their margin normal tissues. Immunohistochemical staining was accomplished for INPP5A in ESCCs. Analysis of ROC curves and the AUC were applied to evaluate the diagnostic capability of the candidate genes.
Results: High levels of HLA-G1, MMP-21, and IL-10 were detected in nearly 23.2%, 62.5%, and 53.5% of ESCCs compared to the normal tissues, respectively, whereas INPP5A underexpression was detected in 19.6% of ESCCs, which all tested genes indicated significant correlations with each other. The protein expression level of INPP5A in ESCC tissues was significantly lower than that of the non-tumor esophageal tissues (p = 0.001). Interestingly, the concomitant expression of the INPP5A/HLA-G1, INPP5A/MMP-21, INPP5A/IL-10, HLA-G1/MMP-21, HLA-G1/IL-10, and MMP-21/IL-10 was significantly correlated with several clinicopathological variables. INPP5A, HLA-G1, MMP-21, and IL-10 showed to be the most appropriate candidates to discriminate tumor/non-tumor groups due to the total AUCs of all combinations (>60%).
Conclusion: Our results represent a new regulatory axis containing INPP5A/HLAG-1/IL-10/MMP-21 markers in ESCC development and may provide novel insight into the mechanism of immune evasion mediated by the INPP5A/HLAG-1/IL-10/MMP-21 regulatory network in the disease.
Type of Study: Full Length/Original Article |
Subject:
Cancer Biology
References
1. Njei B, McCarty TR, Birk JW. Trends in esophageal cancer survival in United States adults from 1973 to 2009: a SEER database analysis. Journal of gastroenterology and hepatology 2016; 31(6): 1141-1146. [DOI:10.1111/jgh.13289]
2. Wang QL, Xie SH, Wahlin K, Lagergren J. Global time trends in the incidence of esophageal squamous cell carcinoma. Clinical epidemiology 2018; 10: 717. [DOI:10.2147/CLEP.S166078]
3. Laha D, Portela-Torres P, Desfougères P, Saiardi A. Inositol phosphate kinases in the eukaryote landscape. Advances in biological regulation 2021; 79: 100782. [DOI:10.1016/j.jbior.2020.100782]
4. Rezuchova I, Hudecova S, Soltysova A, Matuskova M, Durinikova E, Chovancova B, Zuzcak B, Cihova M, Burikova M, Penesova A, Lencesova L, Breza J, Krizanova O. Type 3 inositol 1, 4, 5-trisphosphate receptor has antiapoptotic and proliferative role in cancer cells. Cell death and disease 2019; 10(3): 1-10. [DOI:10.1038/s41419-019-1433-4]
5. Wilczyński J.R, Nowak M. Cancer Immunoediting: Elimination, Equilibrium, and Immune Escape in Solid Tumors. Experientia supplementum 2022; 113: 1-57. [DOI:10.1007/978-3-030-91311-3_1]
6. Apps R, Gardner L, Sharkey AM, Holmes N, Moffett A. A homodimeric complex of HLA‐G on normal trophoblast cells modulates antigen‐presenting cells via LILRB1. European journal of immunology 2007; 37(7): 1924-1937. [DOI:10.1002/eji.200737089]
7. Martín-Villa JM, Vaquero-Yuste C, Molina-Alejandre M, Juarez I, Suárez-Trujillo F, López-Nares A, Palacio-Gruber J, Barrera-Gutiérrez L, Fernández-Cruz E, Rodríguez-Sainz C, Arnaiz-Villena A. HLA-G: Too Much or Too Little? Role in Cancer and Autoimmune Disease. Frontiers in immunology 2022; 13: 796054. [DOI:10.3389/fimmu.2022.796054]
8. Chang CM, Pekkle Lam HY, Hsu HJ, Jiang SJ. Interleukin-10: A double-edged sword in breast cancer. Tzu chi medical journal 2021; 33(3): 203. [DOI:10.4103/tcmj.tcmj_162_20]
9. Vinod C, Jyothy A. A common SNP of IL-10
10. (-1082A/G) is associated with increased risk of premenopausal breast cancer in South Indian women. Iranian journal of cancer prevention 2015; 8(4): e3434. [DOI:10.17795/ijcp-3434]
11. Ouyang W, Garra A O. IL-10 family cytokines IL-10 and IL-22: from basic science to clinical translation. Immunity 2019; 50(4): 871-891. [DOI:10.1016/j.immuni.2019.03.020]
12. Hassuneh MR, Nagarkatti M, Nagarkatti PS. Role of interleukin-10 in the regulation of tumorigenicity of a T cell lymphoma. Leukemia and lymphoma 2013; 54(4): 827-834. [DOI:10.3109/10428194.2012.726721]
13. Cabral-Pacheco GA, Garza-Veloz J, Castruita-De la Rosa C, Ramirez-Acuña JM, Perez-Romero BA, Guerrero-Rodriguez JF, Martinez-Avila N, Martinez-Fierro ML. The roles of matrix metalloproteinases and their inhibitors in human diseases. International journal of molecular sciences 2020; 21(24): 9739. [DOI:10.3390/ijms21249739]
14. Gialeli C, Theocharis AD, Karamanos NK. Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. The FEBS journal 2011; 278(1): 16-27. [DOI:10.1111/j.1742-4658.2010.07919.x]
15. Iizuka S, Ishimaru N, Kudo Y. Matrix metallo-proteinases: the gene expression signatures of head and neck cancer progression. Cancers 2014; 6(1): 396-415. [DOI:10.3390/cancers6010396]
16. Lian IB, Tseng YT, Su CC, Tsai K-Y. Progression of precancerous lesions to oral cancer: results based on the Taiwan National Health Insurance Database. Oral oncology 2013; 49(5): 427-430. [DOI:10.1016/j.oraloncology.2012.12.004]
17. Golyan FF, Abbaszadegan MR, Forghanifard MM. TWIST1, MMP-21, and HLAG-1 co-overexpression is associated with ESCC aggressiveness. Journal of cellular biochemistry 2019; 120(9): 14838-14846. [DOI:10.1002/jcb.28745]
18. Pu Y, Wang L, Wu H, Feng Z, Wang Y, Guo C. High MMP-21 expression in metastatic lymph nodes predicts unfavorable overall survival for oral squamous cell carcinoma patients with lymphatic metastasis. Oncology reports. 2014; 31(6): 2644-2650. [DOI:10.3892/or.2014.3124]
19. Bister V, Skoog T, Virolainen S, Kiviluoto T, Puolakkainen P, Saarialho-Kere U. Increased expression of matrix metalloproteinases-21 and-26 and TIMP-4 in pancreatic adenocarcinoma. Modern pathology 2007; 20(11): 1128-1140. [DOI:10.1038/modpathol.3800956]
20. Zhao Z, Yan L, Li S, Sun H, Zhou Y, Li X. Increased MMP-21 expression in esophageal squamous cell carcinoma is associated with progression and prognosis. Medical oncology 2014; 31(8): 91. [DOI:10.1007/s12032-014-0091-8]
21. Brierley JD, Gospodarowicz MK, Wittekind C. TNM Classification of Malignant Tumours. Unites States: John Wiley & Sons; 2017. [DOI:10.1002/9780471420194.tnmc26.pub3]
22. Hashemi Bidokhti M, Abbaszadegan MR, Sharifi N, Abbasi Sani S, Mahdi Forghanifard M. Contribution of MAML1 in esophageal squamous cell carcinoma tumorigenesis. Annals of diagnostic pathology 2017; 27: 79-82. [DOI:10.1016/j.anndiagpath.2017.01.010]
23. Fedchenko, N, Reifenrath J. Different approaches for interpretation and reporting of immunohistochemistry analysis results in the bone tissue-a review. Diagnostic pathology 2014; 9(1): 1-12. [DOI:10.1186/s13000-014-0221-9]
24. Nahm FS. Receiver operating characteristic curve: overview and practical use for clinicians. Korean journal of anesthesiology 2022; 75(1): 25-36. [DOI:10.4097/kja.21209]
25. Moccia F. Endothelial Ca2+ signaling and the resistance to anticancer treatments: partners in crime. International journal of molecular sciences 2018; 19(1): 217. [DOI:10.3390/ijms19010217]
26. Catarina R G Fonseca A, Moreira PI, Oliveira CR, Cardoso SM, Pinton P, Pereira CF. Amyloid-beta disrupts calcium and redox homeostasis in brain endothelial cells. Molecular neurobiology 2015; 51(2): 610-622. [DOI:10.1007/s12035-014-8740-7]
27. Dragoni S, Laforenza U, Bonetti E, Reforgiato M, Poletto V, Lodola F, Bottino C, Guido D, Rappa A, Pareek S, Tomasello M, Guarrera MR, Cinelli MP, Aronica A, Guerra G, Barosi G, Tanzi F, Rosti V, Moccia F. Enhanced expression of Stim, Orai, and TRPC transcripts and proteins in endothelial progenitor cells isolated from patients with primary myelofibrosis. PLoS one 2014; 9(3): e91099. [DOI:10.1371/journal.pone.0091099]
28. Prendergast C, Quayle J, Burdyga T, Wray S. Atherosclerosis affects calcium signalling in endothelial cells from apolipoprotein E knockout mice before plaque formation. Cell calcium 2014; 55(3): 146-154. [DOI:10.1016/j.ceca.2014.02.012]
29. Patel AB, Mangold AR, Costello CM, Nagel TH, Smith ML, Hayden RE, Sekulic A. Frequent loss of inositol polyphosphate-5-phosphatase in oropharyngeal squamous cell carcinoma. Journal of the European academy of dermatology and venereology 2018; 32(1): e36. [DOI:10.1111/jdv.14462]
30. Berridge M. The inositol trisphosphate/calcium signaling pathway in health and disease. Physiological reviews 2016; 96(4): 1261-1296. [DOI:10.1152/physrev.00006.2016]
31. Mitchell CA, Speed CJ, Nicholl J, Sutherland GR. Chromosomal mapping of the gene (INPP5A) encoding the 43-kDa membrane-associated inositol polyphosphate 5-phosphatase to 10q26. 3 by fluorescence in situ hybridization. Genomics 1996; 31(1): 139-140. [DOI:10.1006/geno.1996.0023]
32. Sekulic A, Kim SY, Hostetter G, Savage S, Einspahr JG, Prasad A, Sagerman P, Curiel-Lewandrowski C, Krouse R, Timothy Bowden G, Warneke J, Alberts DS, Pittelkow MR, DiCaudo D, Nickoloff BJ, Trent, Michael Bittner. Loss of inositol polyphosphate 5-phosphatase is an early event in development of cutaneous squamous cell carcinoma. Cancer prevention research 2010; 3(10): 1277-1283. [DOI:10.1158/1940-6207.CAPR-10-0058]
33. Lee SH, Davison JX, Vidal SM, Belouchi A. Cloning, expression and chromosomal location of NKX6B TO 10Q26, a region frequently deleted in brain tumors. Mammalian genome 2001; 12(2): 157-162. [DOI:10.1007/s003350010247]
34. Ohashi S, Miyamoto S , Kikuchi S, Goto T, Amanuma Y, Muto M. Recent advances from basic and clinical studies of esophageal squamous cell carcinoma. Gastroenterology 2015; 149(7): 1700-1715. [DOI:10.1053/j.gastro.2015.08.054]
35. Holdenrieder S, Wehnl B, Hettwer K, Simon K, Uhlig S, Dayyani F. Carcinoembryonic antigen and cytokeratin-19 fragments for assessment of therapy response in
36. non-small cell lung cancer: a systematic review and meta-analysis. British journal of cancer 2017; 116(8): 1037-1045. [DOI:10.1038/bjc.2017.45]
37. Bauer TM, El-Rayes BF, Li X, Hammad N, Philip PA, Shields AF, Zalupski MM, Bekaii-Saab T. Carbohydrate antigen 19‐9 is a prognostic and predictive biomarker in patients with advanced pancreatic cancer who receive gemcitabine‐containing chemotherapy: a pooled analysis of 6 prospective trials. Cancer 2013; 119(2): 285-292. [DOI:10.1002/cncr.27734]
38. Charakorn C, Thadanipon K, Chaijindaratana S, Rattanasiri S, Numthavaj P, Thakkinstian A. The association between serum squamous cell carcinoma antigen and recurrence and survival of patients with cervical squamous cell carcinoma: a systematic review and meta-analysis. Gynecologic oncology 2018; 150(1): 190-200. [DOI:10.1016/j.ygyno.2018.03.056]
39. Batlle E, Clevers H. Cancer stem cells revisited. Nature medicine 2017; 23(10): 1124-1134. [DOI:10.1038/nm.4409]
40. Yang Y, Huang X, Zhou L, Deng T, Ning T, Liu R, Zhang L, Bai M, Zhang H, Li H, Ba Y. Clinical use of tumor biomarkers in prediction for prognosis and chemotherapeutic effect in esophageal squamous cell carcinoma. BMC cancer 201; 19(1): 1-10. [DOI:10.1186/s12885-019-5755-5]
41. Jain S, Jónasson JO, Pauphilet J, Flower B, Moshe M, Fontana G, Satkunarajah S, Tedder, R, McClure M, Ashrafian H, Elliott, P, Barclay WS, Atchison C, Ward, H, Cooke G, Darzi A, Ramdas K. A new combination testing methodology to identify accurate and economical point-of-care testing strategies. BMJ yale DOI:
https://doi.org/10.1101/2021.06.15.21257351 [DOI:10.1101/2021.06.15.21257351.]
42. Morandi F, Airoldi I. HLA-G and Other Immune Checkpoint Molecules as Targets for Novel Combined Immunotherapies. Internationaljournal of molecular sciences 2022; 23(6): 2925. [DOI:10.3390/ijms23062925]
43. Moreau P, Adrian-Cabestre F, Menier C, Guiard V, Gourand L, Dausset J, Carosella E D, Paul P. IL-10 selectively induces HLA-G expression in human trophoblasts and monocytes. International immunology 1999; 11(5): 803-811. [DOI:10.1093/intimm/11.5.803]
44. Urosevic M, Dummer R. HLA-G and IL-10 expression in human cancer-different stories with the same message. in Seminars in cancer biology 2003; 13(5): 337-42. [DOI:10.1016/S1044-579X(03)00024-5]
45. Hiden U, Glitzner E, Ivanisevic M, Djelmis J, Wadsack C, Lang U, Desoye G. MT1-MMP expression in first-trimester placental tissue is upregulated in type 1 diabetes as a result of elevated insulin and tumor necrosis factor-α levels. Diabetes 2008; 57(1): 150-157. [DOI:10.2337/db07-0903]
46. Lin A, Xu HH, Xu DP, Zhang X, Wang, Wei-Hua Yan Q. Multiple steps of HLA-G in ovarian carcinoma metastasis: alter NK cytotoxicity and induce matrix metalloproteinase-15 (MMP-15) expression. Human immunology 2013; 74(4): 439-446. [DOI:10.1016/j.humimm.2012.11.021]
47. Haseeb M, Pirzada RH, Ain QU, Choi S. Wnt signaling in the regulation of immune cell and cancer therapeutics. Cells 2019; 8(11): 1380. [DOI:10.3390/cells8111380]
48. Janghorban M, Xin L, Rosen JM, HF Zhang X. Notch signaling as a regulator of the tumor immune response: to target or not to target? Frontiers in immunology 2018; 9: 1649. [DOI:10.3389/fimmu.2018.01649]
49. Forghanifard MM, Azaraz S, Ardalan Khales S, Morshedi Rad D, Abbaszadegan MR. MAML1 promotes ESCC aggressiveness through upregulation of EMT marker TWIST1. Molecular biology reports 2020; 47(4): 2659-2668. [DOI:10.1007/s11033-020-05356-z]
50. Luo K. Signaling cross talk between TGF-β/Smad and other signaling pathways. Cold spring harbor perspectives in biology 2017; 9(1): a022137. [DOI:10.1101/cshperspect.a022137]
51. Zhou B, Lin W, Long Y, Yang Y, Zhang H, Wu K, Chu Q. Notch signaling pathway: architecture, disease, and therapeutics. Signal transduction and targeted therapy 2022; 7(1): 1-33. [DOI:10.1038/s41392-022-00934-y]
52. Clara JA, Monge CE, Yang Y, Takebe N. Targeting signalling pathways and the immune microenvironment of cancer stem cells-A clinical update. Nature reviews clinical oncology 2019; 17(4): 204-232. [DOI:10.1038/s41571-019-0293-2]
53. Hong Y, Manoharan I, Suryawanshi A, Majumdar T, Angus-Hill ML, Koni PA, Manicassamy B, Mellor AL, Munn DH, Manicassamy S. β-catenin promotes regulatory T-cell responses in tumors by inducing vitamin A metabolism in dendritic cells. Cancer research 2015; 75(4): 656-665. [DOI:10.1158/0008-5472.CAN-14-2377]
54. Suryawanshi A, Manoharan I, Hong Y, Swafford D, Majumdar T, Taketo TM, Manicassamy B, Koni PA, Thangaraju M, Sun Z, Mellor AL, Munn DH, Manicassamy S. Canonical WNT signaling in dendritic cells regulates Th1/Th17 responses and suppresses autoimmune neuroinflammation. The Journal of immunology 2015; 194(7): 3295-3304. [DOI:10.4049/jimmunol.1402691]
55. Suryawanshi A, Manoharan I, Hong Y, Swafford D, Majumdar T, Taketo MM, et al. Canonical wnt signaling in dendritic cells regulates Th1/Th17 responses and suppresses autoimmune neuro-inflammation. The Journal of Immunology. 2015; 194(7): 3295-3304. [DOI:10.4049/jimmunol.1402691]
56. Rutz S, Janke M, Kassner N, Hohnstein T, Krueger M, Scheffold A. Notch regulates IL-10 production by T helper 1 cells. Proceedings of the national academy of sciences 2008; 105(9): 3497-3502. [DOI:10.1073/pnas.0712102105]
57. Acar A, Hidalgo-Sastre A, Leverentz MK, Mills CG, Woodcock S, Baron M, Collu GM, Brennan K. Inhibition of Wnt signalling by Notch via two distinct mechanisms. Scientific reports 2021; 11(1): 1-12. [DOI:10.1038/s41598-021-88618-5]
58. Ishiguro H, Okubo T, Kuwabara Y, Kimura M, Mitsui A, Sugito N, et al. NOTCH1 activates the Wnt/β-catenin signaling pathway in colon cancer. Oncotarget 2017; 8(36): 60378. [DOI:10.18632/oncotarget.19534]
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