Login Register Cart 0
Generic placeholder image

Current Cancer Therapy Reviews

Editor-in-Chief

ISSN (Print): 1573-3947
ISSN (Online): 1875-6301

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

An Analysis of Structure-function Co-relation between GLI Oncoprotein and HLA Immune-gene Transcriptional Regulation through Molecular Docking

Author(s): Durjoy Majumder*

Volume 17, Issue 4, 2021

Published on: 05 August, 2021

Page: [319 - 334] Pages: 16

DOI: 10.2174/1573394717666210805115050

Price: $65

conference banner
Abstract

Background: GLI proteins play a significant role in the transduction of the Hedgehog (Hh) signaling pathway. A variety of human cancers, including the brain, gastrointestinal, lung, breast, and prostate cancers, demonstrate inappropriate activation of this pathway. GLI helps in proliferation and has an inhibitory role in the differentiation of hematopoietic stem cells. Malignancies may have a defect in differentiation. Different types of malignancies and undifferentiated cells have a low level of HLA expression on their cell surface.

Objective: Human Leukocytic Antigen (HLA) downregulation is frequently observed in cancer cells. This work is aimed to hypothesize whether this downregulation of HLA molecules is GLI oncoprotein mediated or not. To understand the roles of different types of GLI oncoproteins on different classes of HLA transcriptional machinery was carried out through structure-based modeling and molecular docking studies.

Methods: To investigate the role of GLI in HLA expression /downregulation is Hh-GLI mediated or not, molecular docking based computational interaction studies were performed between different GLI proteins (GLI1, GLI2, and GLI3) with TATA box binding protein (TBP) and compare the binding efficiencies of different HLA gene (both HLA class I and –II) regulating transcription factors (RelA, RFX5, RFXAP, RFXANK, CIITA, CREB1, and their combinations) with TBP. Due to unavailability of 3D protein structures of GLI2 and cyclin D2 (a natural ligand of GLI1) were modelled followed by structural validation by Ramachandran plot analysis.

Results: GLI proteins especially, GLI1 and GLI2, have almost similar binding energy of RFX5-RFXANK- RFXAP and CIITA multi-protein complex to TBP but has lower binding energy between RelA to TBP.

Conclusion: This study suggests that HLA class I may not be downregulated by GLI; however, over-expression of GLI1 is may be responsible for HLA class II downregulation. Thus this protein may be responsible for the maintenance of the undifferentiated state of malignant cells. This study also suggests the implicative role of GLI1 in the early definitive stage of hematopoiesis.

Keywords: GLI, hedgehog signaling, HLA regulation, cancer, stemness, malignant cells.

« Previous Next »
Graphical Abstract

[1]
Hahn H, Wicking C, Zaphiropoulous PG, et al. Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell 1996; 85(6): 841-51.
[http://dx.doi.org/10.1016/S0092-8674(00)81268-4] [PMID: 8681379]
[2]
Reifenberger J, Wolter M, Weber RG, et al. Missense mutations in SMOH in sporadic basal cell carcinomas of the skin and primitive neuroectodermal tumors of the central nervous system. Cancer Res 1998; 58(9): 1798-803.
[PMID: 9581815]
[3]
Beachy PA, Karhadkar SS, Berman DM. Tissue repair and stem cell renewal in carcinogenesis. Nature 2004; 432(7015): 324-31.
[http://dx.doi.org/10.1038/nature03100] [PMID: 15549094]
[4]
Pietsch T, Waha A, Koch A, et al. Medulloblastomas of the desmoplastic variant carry mutations of the human homologue of Drosophila patched. Cancer Res 1997; 57(11): 2085-8.
[PMID: 9187099]
[5]
Tostar U, Malm CJ, Meis-Kindblom JM, Kindblom LG, Toftgård R, Undén AB. Deregulation of the hedgehog signalling pathway: a possible role for the PTCH and SUFU genes in human rhabdomyoma and rhabdomyosarcoma development. J Pathol 2006; 208(1): 17-25.
[http://dx.doi.org/10.1002/path.1882] [PMID: 16294371]
[6]
Sheng X, Bowen N, Wang Z. GLI pathogenesis-related 1 functions as a tumor-suppressor in lung cancer. Mol Cancer 2016; 15: 25.
[http://dx.doi.org/10.1186/s12943-016-0508-4] [PMID: 26988096]
[7]
Taylor MD, Liu L, Raffel C, et al. Mutations in SUFU predispose to medulloblastoma. Nat Genet 2002; 31(3): 306-10.
[http://dx.doi.org/10.1038/ng916] [PMID: 12068298]
[8]
Di Marcotullio L, Ferretti E, De Smaele E, et al. REN(KCTD11) is a suppressor of Hedgehog signaling and is deleted in human medulloblastoma. Proc Natl Acad Sci USA 2004; 101(29): 10833-8.
[http://dx.doi.org/10.1073/pnas.0400690101] [PMID: 15249678]
[9]
Kimura H, Stephen D, Joyner A, Curran T. Gli1 is important for medulloblastoma formation in Ptc1+/- mice. Oncogene 2005; 24(25): 4026-36.
[http://dx.doi.org/10.1038/sj.onc.1208567] [PMID: 15806168]
[10]
Heretsch P, Tzagkaroulaki L, Giannis A. Modulators of the hedgehog signaling pathway. Bioorg Med Chem 2010; 18(18): 6613-24.
[http://dx.doi.org/10.1016/j.bmc.2010.07.038] [PMID: 20708941]
[11]
Beauchamp E, Bulut G, Abaan O, et al. GLI1 is a direct transcriptional target of EWS-FLI1 oncoprotein. J Biol Chem 2009; 284(14): 9074-82.
[http://dx.doi.org/10.1074/jbc.M806233200] [PMID: 19189974]
[12]
Sell S, Pierce GB. Maturation arrest of stem cell differentiation is a common pathway for the cellular origin of teratocarcinomas and epithelial cancers. Lab Invest 1994; 70(1): 6-22.
[PMID: 8302019]
[13]
Sell S. Stem cell origin of cancer and differentiation therapy. Crit Rev Oncol Hematol 2004; 51(1): 1-28.
[http://dx.doi.org/10.1016/j.critrevonc.2004.04.007] [PMID: 15207251]
[14]
Thayer SP, di Magliano MP, Heiser PW, et al. Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis. Nature 2003; 425(6960): 851-6.
[http://dx.doi.org/10.1038/nature02009] [PMID: 14520413]
[15]
Pasca di Magliano M, Hebrok M. Hedgehog signalling in cancer formation and maintenance. Nat Rev Cancer 2003; 3(12): 903-11.
[http://dx.doi.org/10.1038/nrc1229] [PMID: 14737121]
[16]
Sheng T, Li C, Zhang X, et al. Activation of the hedgehog pathway in advanced prostate cancer. Mol Cancer 2004; 3: 29.
[http://dx.doi.org/10.1186/1476-4598-3-29] [PMID: 15482598]
[17]
Ji Z, Mei FC, Xie J, Cheng X. Oncogenic KRAS activates hedgehog signaling pathway in pancreatic cancer cells. J Biol Chem 2007; 282(19): 14048-55.
[http://dx.doi.org/10.1074/jbc.M611089200] [PMID: 17353198]
[18]
Yauch RL, Gould SE, Scales SJ, et al. A paracrine requirement for hedgehog signalling in cancer. Nature 2008; 455(7211): 406-10.
[http://dx.doi.org/10.1038/nature07275] [PMID: 18754008]
[19]
Feldmann G, Fendrich V, McGovern K, et al. An orally bioavailable small-molecule inhibitor of Hedgehog signaling inhibits tumor initiation and metastasis in pancreatic cancer. Mol Cancer Ther 2008; 7(9): 2725-35.
[http://dx.doi.org/10.1158/1535-7163.MCT-08-0573] [PMID: 18790753]
[20]
Nolan-Stevaux O, Lau J, Truitt ML, et al. GLI1 is regulated through Smoothened-independent mechanisms in neoplastic pancreatic ducts and mediates PDAC cell survival and transformation. Genes Dev 2009; 23(1): 24-36.
[http://dx.doi.org/10.1101/gad.1753809] [PMID: 19136624]
[21]
Stecca B, Ruiz i Altaba A. A GLI1-p53 inhibitory loop controls neural stem cell and tumour cell numbers. EMBO J 2009; 28(6): 663-76.
[http://dx.doi.org/10.1038/emboj.2009.16] [PMID: 19214186]
[22]
Rasheed ZA, Yang J, Wang Q, et al. Prognostic significance of tumorigenic cells with mesenchymal features in pancreatic adenocarcinoma. J Natl Cancer Inst 2010; 102(5): 340-51.
[http://dx.doi.org/10.1093/jnci/djp535] [PMID: 20164446]
[23]
Roberts WM, Douglass EC, Peiper SC, Houghton PJ, Look AT. Amplification of the gli gene in childhood sarcomas. Cancer Res 1989; 49(19): 5407-13.
[PMID: 2766305]
[24]
Samuels S, Spaans VM, Osse M, et al. Human Leukocyte Antigen-DR expression is significantly related to an increased disease-free and disease-specific survival in patients with cervical adenocarcinoma. Int J Gynecol Cancer 2016; 26(8): 1503-9.
[http://dx.doi.org/10.1097/IGC.0000000000000783] [PMID: 27654088]
[25]
Dahlén A, Fletcher CD, Mertens F, et al. Activation of the GLI oncogene through fusion with the beta-actin gene (ACTB) in a group of distinctive pericytic neoplasms: pericytoma with t(7;12). Am J Pathol 2004; 164(5): 1645-53.
[http://dx.doi.org/10.1016/S0002-9440(10)63723-6] [PMID: 15111311]
[26]
Nessling M, Richter K, Schwaenen C, et al. Candidate genes in breast cancer revealed by microarray-based comparative genomic hybridization of archived tissue. Cancer Res 2005; 65(2): 439-47.
[PMID: 15695385]
[27]
Bhatia N, Thiyagarajan S, Elcheva I, et al. Gli2 is targeted for ubiquitination and degradation by beta-TrCP ubiquitin ligase. J Biol Chem 2006; 281(28): 19320-6.
[http://dx.doi.org/10.1074/jbc.M513203200] [PMID: 16651270]
[28]
Mar BG, Amakye D, Aifantis I, Buonamici S. The controversial role of the Hedgehog pathway in normal and malignant hematopoiesis. Leukemia 2011; 25(11): 1665-73.
[http://dx.doi.org/10.1038/leu.2011.143] [PMID: 21660044]
[29]
Merchant A, Joseph G, Wang Q, Brennan S, Matsui W. Gli1 regulates the proliferation and differentiation of HSCs and myeloid progenitors. Blood 2010; 115(12): 2391-6.
[http://dx.doi.org/10.1182/blood-2009-09-241703] [PMID: 20107231]
[30]
Kern D, Regl G, Hofbauer SW, et al. Hedgehog/GLI and PI3K signaling in the initiation and maintenance of chronic lymphocytic leukemia. Oncogene 2015; 34(42): 5341-51.
[http://dx.doi.org/10.1038/onc.2014.450] [PMID: 25639866]
[31]
Wellbrock J, Latuske E, Köhler J, et al. Expression of Hedgehog pathway mediator GLI represents a negative prognostic marker in human acute myeloid leukemia and its inhibition exerts antileukemic effects. Clin Cancer Res 2015; 21(10): 2388-98.
[http://dx.doi.org/10.1158/1078-0432.CCR-14-1059] [PMID: 25745035]
[32]
Long B, Wang LX, Zheng FM, et al. Targeting GLI1 suppresses cell growth and enhances chemosensitivity in CD34+ enriched acute myeloid leukemia progenitor cells. Cell Physiol Biochem 2016; 38(4): 1288-302.
[http://dx.doi.org/10.1159/000443075] [PMID: 27008269]
[33]
Carpenter RL, Lo HW. Hedgehog pathway and GLI1 isoforms in human cancer. Discov Med 2012; 13(69): 105-13.
[PMID: 22369969]
[34]
Bermudez O, Hennen E, Koch I, Lindner M, Eickelberg O. Gli1 mediates lung cancer cell proliferation and Sonic Hedgehog-dependent mesenchymal cell activation. PLoS One 2013; 8(5): e63226.
[http://dx.doi.org/10.1371/journal.pone.0063226] [PMID: 23667589]
[35]
Yoon JW, Liu CZ, Yang JT, Swart R, Iannaccone P, Walterhouse D. GLI activates transcription through a herpes simplex viral protein 16-like activation domain. J Biol Chem 1998; 273(6): 3496-501.
[http://dx.doi.org/10.1074/jbc.273.6.3496] [PMID: 9452474]
[36]
Scholl T, Mahanta SK, Strominger JL. Specific complex formation between the type II bare lymphocyte syndrome-associated transactivators CIITA and RFX5. Proc Natl Acad Sci USA 1997; 94(12): 6330-4.
[http://dx.doi.org/10.1073/pnas.94.12.6330] [PMID: 9177217]
[37]
Yoon JW, Kita Y, Frank DJ, et al. Gene expression profiling leads to identification of GLI1-binding elements in target genes and a role for multiple downstream pathways in GLI1-induced cell transformation. J Biol Chem 2002; 277(7): 5548-55.
[http://dx.doi.org/10.1074/jbc.M105708200] [PMID: 11719506]
[38]
van den Elsen PJ, Peijnenburg A, van Eggermond MC, Gobin SJ. Shared regulatory elements in the promoters of MHC class I and class II genes. Immunol Today 1998; 19(7): 308-12.
[http://dx.doi.org/10.1016/S0167-5699(98)01287-0] [PMID: 9666603]
[39]
Girdlestone J. Synergistic induction of HLA class I expression by RelA and CIITA. Blood 2000; 95(12): 3804-8.
[http://dx.doi.org/10.1182/blood.V95.12.3804] [PMID: 10845913]
[40]
Majumder D. HLA expression in leukemia: Status, regulation & therapeutic implications of HLA expression in leukemia.Lap lambert. Saarbrucken, Berlin, Leipzig, UK: Academic Publishing 2012.
[41]
aMajumder D. Application of information theory for understanding of HLA gene regulation in leukemia. Advances in Computing and Information Technology 2012; 177: 161-73.; bMeghanathan N, Nagamalai D, Chaki N. Berlin, Heidelberg: Springer-Verleg 2012.
[42]
Das B, Majumder D. Information theory based analysis for understanding the regulation of HLA gene expression in human leukemia. Int J Inform Sci Tech 2012; 2(5): 39-50.
[http://dx.doi.org/10.5121/ijist.2012.2504]
[43]
Das B, Majumder D. Maximum Entropy based multivariate dependence analysis with a case study for HLA gene regulatory network in human leukemia. Int J Ind Eng 2013; 3(4): 137-42.
[44]
Deb Pal A, Banerjee S. Epstein-Barr virus latent membrane protein 2A mediated activation of Sonic Hedgehog pathway induces HLA class Ia downregulation in gastric cancer cells. Virology 2015; 484: 22-32.
[http://dx.doi.org/10.1016/j.virol.2015.05.007] [PMID: 26057149]
[45]
Das B, Majumder D. Interactions of transcription factors in HLA class I transcriptosome. Int J Comput Inform Sys Indus Manage Appl 2014; 6: 592-602.
[46]
Chen PM, Yen ML, Liu KJ, Sytwu HK, Yen BL. Immunomodulatory properties of human adult and fetal multipotent mesenchymal stem cells. J Biomed Sci 2011; 18(1): 49.
[http://dx.doi.org/10.1186/1423-0127-18-49] [PMID: 21762539]
[47]
Hass R, Kasper C, Böhm S, Jacobs R. Different populations and sources of human mesenchymal stem cells (MSC): A comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal 2011; 9: 12.
[http://dx.doi.org/10.1186/1478-811X-9-12] [PMID: 21569606]
[48]
Kubo M, Sonoda Y, Muramatsu R, Usui M. Immunogenicity of human amniotic membrane in experimental xenotransplantation. Invest Ophthalmol Vis Sci 2001; 42(7): 1539-46.
[PMID: 11381058]
[49]
Abdulrazzak H, Moschidou D, Jones G, Guillot PV. Biological characteristics of stem cells from foetal, cord blood and extraembryonic tissues. J R Soc Interface 2010; 7(Suppl. 6): S689-706.
[http://dx.doi.org/10.1098/rsif.2010.0347.focus] [PMID: 20739312]
[50]
Ji F, Wang Y, Sun H, et al. Human umbilical cord blood-derived non-hematopoietic stem cells suppress lymphocyte proliferation and CD4, CD8 expression. J Neuroimmunol 2008; 197(2): 99-109.
[http://dx.doi.org/10.1016/j.jneuroim.2008.04.013] [PMID: 18534691]
[51]
Das B, Majumder D. Interactions among MARM binding factors. Proceedings of the 2nd World Congress Information and Communication Technologies (WICT 12). 191-6.
[52]
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215(3): 403-10.
[http://dx.doi.org/10.1016/S0022-2836(05)80360-2] [PMID: 2231712]
[53]
Cuff JA, Clamp ME, Siddiqui AS, Finlay M, Barton GJ. JPred: A consensus secondary structure prediction server. Bioinformatics 1998; 14(10): 892-3.
[http://dx.doi.org/10.1093/bioinformatics/14.10.892] [PMID: 9927721]
[54]
Shi J, Blundell TL, Mizuguchi K. FUGUE: Sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J Mol Biol 2001; 310(1): 243-57.
[http://dx.doi.org/10.1006/jmbi.2001.4762] [PMID: 11419950]
[55]
Kelley LA, Sternberg MJE. Protein structure prediction on the Web: A case study using the Phyre server. Nat Protoc 2009; 4(3): 363-71.
[http://dx.doi.org/10.1038/nprot.2009.2] [PMID: 19247286]
[56]
Pieper U, Webb BM, Barkan DT, et al. ModBase, a database of annotated comparative protein structure models, and associated resources. Nucleic Acids Res 2011; 39(Database issue): D465-74.
[http://dx.doi.org/10.1093/nar/gkq1091] [PMID: 21097780]
[57]
Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22(22): 4673-80.
[http://dx.doi.org/10.1093/nar/22.22.4673] [PMID: 7984417]
[58]
Larkin MA, Blackshields G, Brown NP, et al. Clustal W and clustal X version 2.0. Bioinformatics 2007; 23(21): 2947-8.
[http://dx.doi.org/10.1093/bioinformatics/btm404] [PMID: 17846036]
[59]
Fiser A, Do RK, Sali A. Modeling of loops in protein structures. Protein Sci 2000; 9(9): 1753-73.
[http://dx.doi.org/10.1110/ps.9.9.1753] [PMID: 11045621]
[60]
Eswar N, Webb B, Marti-Renom M A, et al. Comparative protein structure modeling with modeller. Curr Protoc Protein Sci 2006; 2(2.9): 5.6.1-5.6.30.
[http://dx.doi.org/10.1002/0471250953.bi0506s15]
[61]
Melo F, Sánchez R, Sali A. Statistical potentials for fold assessment. Protein Sci 2002; 11(2): 430-48.
[http://dx.doi.org/10.1002/pro.110430] [PMID: 11790853]
[62]
Chinea G, Padron G, Hooft RW, Sander C, Vriend G. The use of position-specific rotamers in model building by homology. Proteins 1995; 23(3): 415-21.
[http://dx.doi.org/10.1002/prot.340230315] [PMID: 8710834]
[63]
Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PROCHECK - a program to check the stereochemical quality of protein structures. J Appl Cryst 1993; 26: 283-91.
[http://dx.doi.org/10.1107/S0021889892009944]
[64]
Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM. AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. J Biomol NMR 1996; 8(4): 477-86.
[http://dx.doi.org/10.1007/BF00228148] [PMID: 9008363]
[65]
Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJ. GROMACS: fast, flexible, and free. J Comput Chem 2005; 26(16): 1701-18.
[http://dx.doi.org/10.1002/jcc.20291] [PMID: 16211538]
[66]
Ritchie DW, Kemp GJL. Protein docking using spherical polar Fourier correlations. Proteins 2000; 39(2): 178-94.
[http://dx.doi.org/10.1002/(SICI)1097-0134(20000501)39:2<178::AID-PROT8>3.0.CO;2-6] [PMID: 10737939]
[67]
Bradford JR, Westhead DR. Improved prediction of protein-protein binding sites using a support vector machines approach. Bioinformatics 2005; 21(8): 1487-94.
[http://dx.doi.org/10.1093/bioinformatics/bti242] [PMID: 15613384]
[68]
Dolinky TJ, Nielsen JE, McCammon JA, Baker NA. PDB2PQR: An automated pipeline for the setup, execution, and analysis of poisson-boltzmann electrostatics calculations. Nucleic Acids Res 2004; 32: W665-7.
[http://dx.doi.org/10.1093/nar/gkh381] [PMID: 15215472]
[69]
Wang J. Challenges in binding free energy calculation using PB/GBSA. Bioenergetics 2012; 1: e102.
[http://dx.doi.org/10.4172/2167-7662.1000e102]
[70]
Aptsiauri N, Garcia-Lora AM, Cabrera T. MHC class I antigens in malignant cells: Immune escape and response to immunotherapy. Springer Briefs Cancer Res 2013; 2013: 6.
[71]
Sconocchia G, Eppenberger-Castori S, Zlobec I, et al. HLA class II antigen expression in colorectal carcinoma tumors as a favorable prognostic marker. Neoplasia 2014; 16(1): 31-42.
[http://dx.doi.org/10.1593/neo.131568] [PMID: 24563618]
[72]
Kinzler KW, Bigner SH, Bigner DD, et al. Identification of an amplified, highly expressed gene in a human glioma. Science 1987; 236(4797): 70-3.
[http://dx.doi.org/10.1126/science.3563490] [PMID: 3563490]
[73]
Passlick B, Pantel K, Kubuschok B, et al. Expression of MHC molecules and ICAM-1 on non-small cell lung carcinomas: Association with early lymphatic spread of tumour cells. Eur J Cancer 1996; 32A(1): 141-5.
[http://dx.doi.org/10.1016/0959-8049(95)00551-X] [PMID: 8695222]
[74]
Garrido F, Ruiz-Cabello F. MHC expression on human tumors-its relevance for local tumor growth and metastasis. Semin Cancer Biol 1991; 2(1): 3-10.
[PMID: 1912516]
[75]
Doonan BP, Haque A. HLA Class II antigen presentation in prostate cancer cells: A novel approach to prostate tumor immunotherapy. Open Cancer Immunol J 2010; 3(3): 1-7.
[http://dx.doi.org/10.2174/1876401001003010001] [PMID: 24163711]
[76]
Amria S, Cameron C, Stuart R, Haque A. Defects in HLA class II antigen presentation in B-cell lymphomas. Leuk Lymphoma 2008; 49(2): 353-5.
[http://dx.doi.org/10.1080/10428190701814305] [PMID: 18231926]
[77]
Tada K, Maeshima AM, Hiraoka N, et al. Prognostic significance of HLA class I and II expression in patients with diffuse large B cell lymphoma treated with standard chemoimmunotherapy. Cancer Immunol Immunother 2016; 65(10): 1213-22.
[http://dx.doi.org/10.1007/s00262-016-1883-9] [PMID: 27522583]
[78]
Newman RA, Greaves MF. Characterization of HLA-DR antigens on leukaemic cells. Clin Exp Immunol 1982; 50(1): 41-50.
[PMID: 6959750]
[79]
Forero A, Li Y, Chen D, et al. Expression of the MHC class II pathway in triple-negative breast cancer tumor cells is associated with a good prognosis and infiltrating lymphocytes. Cancer Immunol Res 2016; 4(5): 390-9.
[http://dx.doi.org/10.1158/2326-6066.CIR-15-0243] [PMID: 26980599]
[80]
Fitchen JH, Foon KA, Cline MJ. The antigenic characteristics of hematopoietic stem cells. N Engl J Med 1981; 305(1): 17-25.
[http://dx.doi.org/10.1056/NEJM198107023050104] [PMID: 6785649]
[81]
Caux C, Favre C, Saeland S, et al. Sequential loss of CD34 and class II MHC antigens on purified cord blood hematopoietic progenitors cultured with IL-3: characterization of CD34-, HLA-DR+ cells. Blood 1989; 74(4): 1287-94.
[http://dx.doi.org/10.1182/blood.V74.4.1287.1287] [PMID: 2475184]
[82]
Cao LX, Le Bousse-Kerdiles MC, Clay D, Oshevski S, Jasmin C, Krief P. Implication of a new molecule IK in CD34+ hematopoietic progenitor cell proliferation and differentiation. Blood 1997; 89(10): 3615-23.
[http://dx.doi.org/10.1182/blood.V89.10.3615] [PMID: 9160666]
[83]
Das B, Majumder D. Differences of HLA gene regulatory network in human myeloid and lymphoid leukemias. Proceedings of the International Conference on Bioinformatics and Systems Biology 2018 (BSB-2018). 165-9.978-1-5386-6434-6
[http://dx.doi.org/10.1109/BSB.2018.8770568]
[84]
Yoon JW, Lamm M, Iannaccone S, et al. p53 modulates the activity of the GLI1 oncogene through interactions with the shared coactivator TAF9. DNA Repair (Amst) 2015; 34: 9-17.
[http://dx.doi.org/10.1016/j.dnarep.2015.06.006] [PMID: 26282181]
[85]
Niewiadomski P, Niedziółka SM, Markiewicz Ł, Uśpieński T, Baran B, Chojnowska K. Gli Proteins: Regulation in development and cancer. Cells 2019; 8(2): 147.
[http://dx.doi.org/10.3390/cells8020147] [PMID: 30754706]

Rights & Permissions Print Cite
Article Metrics
14
2
Wayfinder Image
© 2024 Bentham Science Publishers | Privacy Policy