ID2 and ID3 protein expression mirrors granulopoietic maturation and discriminates between acute leukemia subtypes

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• 作者：Annette M. May (1)
  Anna-Verena Frey (1)
  Lioudmila Bogatyreva (2)
  Marco Benkisser-Petersen (3) (4)
  Dieter Hauschke (2)
  Michael Lübbert (3) (6)
  Ralph W?sch (3) (6)
  Martin Werner (1) (6) (7)
  Jens Hasskarl (3)
  Silke Lassmann (1) (5) (6) (7)
  
• 关键词：Hematopoiesis ; Acute leukemia ; Inhibitor of DNA binding (ID) ; Immunohistochemistry
• 刊名：Histochemistry and Cell Biology
• 出版年：2014
• 出版时间：April 2014
• 年：2014
• 卷：141
• 期：4
• 页码：431-440
• 全文大小：518 KB
• 参考文献：1. Akashi K, He X, Chen J, Iwasaki H, Niu C, Steenhard B, Zhang J, Haug J, Li L (2003) Transcriptional accessibility for genes of multiple tissues and hematopoietic lineages is hierarchically controlled during early hematopoiesis. Blood 101:383-89 CrossRef
  2. Aspland SE, Bendall HH, Murre C (2001) The role of E2A–PBX1 in leukemogenesis. Oncogene 20:5708-717 CrossRef
  3. Back J, Dierich A, Bronn C, Kastner P, Chan S (2004) PU.1 determines the self-renewal capacity of erythroid progenitor cells. Blood 103:3615-623 CrossRef
  4. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H (1990) The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61:49-9 CrossRef
  5. Benezra R, Rafii S, Lyden D (2001) The Id proteins and angiogenesis. Oncogene 20:8334-341 CrossRef
  6. Buitenhuis M, van Deutekom HW, Verhagen LP, Castor A, Jacobsen SE, Lammers JW, Koenderman L, Coffer PJ (2005) Differential regulation of granulopoiesis by the basic helix-loop-helix transcriptional inhibitors Id1 and Id2. Blood 105:4272-281 CrossRef
  7. Cooper CL, Brady G, Bilia F, Iscove NN, Quesenberry PJ (1997) Expression of the Id family helix-loop-helix regulators during growth and development in the hematopoietic system. Blood 89:3155-165
  8. Doulatov S, Notta F, Rice KL, Howell L, Zelent A, Licht JD, Dick JE (2009) PLZF is a regulator of homeostatic and cytokine-induced myeloid development. Genes Dev 23:2076-087 CrossRef
  9. Gardini A, Cesaroni M, Luzi L, Okumura AJ, Biggs JR, Minardi SP, Venturini E, Zhang DE, Pelicci PG, Alcalay M (2008) AML1/ETO oncoprotein is directed to AML1 binding regions and co-localizes with AML1 and HEB on its targets. PLoS Genet 4:e1000275 CrossRef
  10. Guo C, Hu Q, Yan C, Zhang J (2009) Multivalent binding of the ETO corepressor to E proteins facilitates dual repression controls targeting chromatin and the basal transcription machinery. Mol Cell Biol 29:2644-657 CrossRef
  11. Hasskarl J, Münger K (2002) Id proteins–tumor markers or oncogenes? Cancer Biol Ther 1:91-6
  12. Hong SH, Lee JH, Lee JB, Ji J, Bhatia M (2011) ID1 and ID3 represent conserved negative regulators of human embryonic and induced pluripotent stem cell hematopoiesis. J Cell Sci 124:1445-452 CrossRef
  13. Hunger SP (1996) Chromosomal translocations involving the E2A gene in acute lymphoblastic leukemia: clinical features and molecular pathogenesis. Blood 87:1211-224
  14. Hunger SP, Ohyashiki K, Toyama K, Cleary ML (1992) Hlf, a novel hepatic bZIP protein, shows altered DNA-binding properties following fusion to E2A in t (17;19) acute lymphoblastic leukemia. Genes Dev 6:1608-620 CrossRef
  15. Inaba T, Roberts WM, Shapiro LH, Jolly KW, Raimondi SC, Smith SD, Look AT (1992) Fusion of the leucine zipper gene HLF to the E2A gene in human acute B-lineage leukemia. Science 257:531-34 CrossRef
  16. Ishiguro A, Spirin KS, Shiohara M, Tobler A, Gombart AF, Israel MA, Norton JD, Koeffler HP (1996) Id2 expression increases with differentiation of human myeloid cells. Blood 87:5225-231
  17. Ji M, Li H, Suh HC, Klarmann KD, Yokota Y, Keller JR (2008) Id2 intrinsically regulates lymphoid and erythroid development via interaction with different target proteins. Blood 112:1068-077 CrossRef
  18. Kreider BL, Benezra R, Rovera G, Kadesch T (1992) Inhibition of myeloid differentiation by the helix-loop-helix protein Id. Science 255:1700-702 CrossRef
  19. Laiosa CV, Stadtfeld M, Graf T (2006) Determinants of lymphoid–myeloid lineage diversification. Annu Rev Immunol 24:705-38 CrossRef
  20. Laslo P, Spooner CJ, Warmflash A, Lancki DW, Lee HJ, Sciammas R, Gantner BN, Dinner AR, Singh H (2006) Multilineage transcriptional priming and determination of alternate hematopoietic cell fates. Cell 126:755-66 CrossRef
  21. Laslo P, Pongubala JM, Lancki DW, Singh H (2008) Gene regulatory networks directing myeloid and lymphoid cell fates within the immune system. Semin Immunol 20:228-35 CrossRef
  22. Lasorella A, Iavarone A, Israel MA (1996) Id2 specifically alters regulation of the cell cycle by tumor suppressor proteins. Mol Cell Biol 16:2570-578
  23. Lasorella A, Boldrini R, Dominici C, Donfrancesco A, Yokota Y, Inserra A, Iavarone A (2002) Id2 is critical for cellular proliferation and is the oncogenic effector of N-myc in human neuroblastoma. Cancer Res 62:301-06
  24. Lasorella A, Stegmuller J, Guardavaccaro D, Liu G, Carro MS, Rothschild G, de la Torre-Ubieta L, Pagano M, Bonni A, Iavarone A (2006) Degradation of Id2 by the anaphase-promoting complex couples cell cycle exit and axonal growth. Nature 442:471-74 CrossRef
  25. Leeanansaksiri W, Wang H, Gooya JM, Renn K, Abshari M, Tsai S, Keller JR (2005) IL-3 induces inhibitor of DNA-binding protein-1 in hemopoietic progenitor cells and promotes myeloid cell development. J Immunol 174:7014-021
  26. Li H, Ji M, Klarmann KD, Keller JR (2010) Repression of Id2 expression by Gfi-1 is required for B-cell and myeloid development. Blood 116:1060-069 CrossRef
  27. Lister J, Forrester WC, Baron MH (1995) Inhibition of an erythroid differentiation switch by the helix-loop-helix protein Id1. J Biol Chem 270:17939-7946 CrossRef
  28. Lyden D, Young AZ, Zagzag D, Yan W, Gerald W, O’Reilly R, Bader BL, Hynes RO, Zhuang Y, Manova K, Benezra R (1999) Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401:670-77 CrossRef
  29. Manthey C, Mern DS, Gutmann A, Zielinski AJ, Herz C, Lassmann S, Hasskarl J (2010) Elevated endogenous expression of the dominant negative basic helix-loop-helix protein ID1 correlates with significant centrosome abnormalities in human tumor cells. BMC Cell Biol 11:2 CrossRef
  30. Maruyama H, Kleeff J, Wildi S, Friess H, Buchler MW, Israel MA, Korc M (1999) Id-1 and Id-2 are overexpressed in pancreatic cancer and in dysplastic lesions in chronic pancreatitis. Am J Pathol 155:815-22 CrossRef
  31. Maruyama T, Li J, Vaque JP, Konkel JE, Wang W, Zhang B, Zhang P, Zamarron BF, Yu D, Wu Y, Zhuang Y, Gutkind JS, Chen W (2011) Control of the differentiation of regulatory T cells and T(H)17 cells by the DNA-binding inhibitor Id3. Nat Immunol 12:86-5 CrossRef
  32. Massari ME, Murre C (2000) Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 20:429-40 CrossRef
  33. Maw MK, Fujimoto J, Tamaya T (2009) Overexpression of inhibitor of DNA-binding (ID)-1 protein related to angiogenesis in tumor advancement of ovarian cancers. BMC Cancer 9:430 CrossRef
  34. Mellentin JD, Murre C, Donlon TA, McCaw PS, Smith SD, Carroll AJ, McDonald ME, Baltimore D, Cleary ML (1989) The gene for enhancer binding proteins E12/E47 lies at the t (1;19) breakpoint in acute leukemias. Science 246:379-82 CrossRef
  35. Mern DS, Hasskarl J, Burwinkel B (2010a) Inhibition of Id proteins by a peptide aptamer induces cell-cycle arrest and apoptosis in ovarian cancer cells. Br J Cancer 103:1237-244 CrossRef
  36. Mern DS, Hoppe-Seyler K, Hoppe-Seyler F, Hasskarl J, Burwinkel B (2010b) Targeting Id1 and Id3 by a specific peptide aptamer induces E-box promoter activity, cell cycle arrest, and apoptosis in breast cancer cells. Breast Cancer Res Treat 124:623-33 CrossRef
  37. Mufti GJ, Flandrin G, Schaefer H-E, Sandberg AA, Kanfer EJ (1996) An atlas of malignant haematology: cytology, histology and cytogenetics. Martin Dunitz Ltd, London
  38. Münch C, May AM, Hauschke D, Roth J, Lassmann S, Werner M (2011) Internuclear chromosome distribution of dysplastic megakaryocytes in myelodysplastic syndromes is dependent on the level of ploidy. Chromosoma 120:265-73 CrossRef
  39. Nigten J, Breems-de Ridder MC, Erpelinck-Verschueren CA, Nikoloski G, van der Reijden BA, van Wageningen S, van Hennik PB, de Witte T, Lowenberg B, Jansen JH (2005) ID1 and ID2 are retinoic acid responsive genes and induce a G0/G1 accumulation in acute promyelocytic leukemia cells. Leukemia 19:799-05 CrossRef
  40. Nogueira MM, Mitjavila-Garcia MT, Le Pesteur F, Filippi MD, Vainchenker W, Dubart Kupperschmitt A, Sainteny F (2000) Regulation of Id gene expression during embryonic stem cell-derived hematopoietic differentiation. Biochem Biophys Res Commun 276:803-12 CrossRef
  41. Norton JD (2000) ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis. J Cell Sci 113(Pt 22):3897-905
  42. Ouyang XS, Wang X, Lee DT, Tsao SW, Wong YC (2002) Over expression of ID-1 in prostate cancer. J Urol 167:2598-602 CrossRef
  43. Pascal LE, True LD, Campbell DS, Deutsch EW, Risk M, Coleman IM, Eichner LJ, Nelson PS, Liu AY (2008) Correlation of mRNA and protein levels: cell type-specific gene expression of cluster designation antigens in the prostate. BMC Genomics 9:246 CrossRef
  44. Perk J, Iavarone A, Benezra R (2005) Id family of helix-loop-helix proteins in cancer. Nat Rev Cancer 5:603-14 CrossRef
  45. Perk J, Gil-Bazo I, Chin Y, de Candia P, Chen JJ, Zhao Y, Chao S, Cheong W, Ke Y, Al-Ahmadie H, Gerald WL, Brogi E, Benezra R (2006) Reassessment of id1 protein expression in human mammary, prostate, and bladder cancers using a monospecific rabbit monoclonal anti-id1 antibody. Cancer Res 66:10870-0877 CrossRef
  46. Quesenberry PJ, Iscove NN, Cooper C, Brady G, Newburger PE, Stein GS, Stein JS, Reddy GP, Pearson-White S (1996) Expression of basic helix-loop-helix transcription factors in explant hematopoietic progenitors. J Cell Biochem 61:478-88 CrossRef
  47. Sikder HA, Devlin MK, Dunlap S, Ryu B, Alani RM (2003) Id proteins in cell growth and tumorigenesis. Cancer Cell 3:525-30 CrossRef
  48. Suh HC, Leeanansaksiri W, Ji M, Klarmann KD, Renn K, Gooya J, Smith D, McNiece I, Lugthart S, Valk PJ, Delwel R, Keller JR (2008) Id1 immortalizes hematopoietic progenitors in vitro and promotes a myeloproliferative disease in vivo. Oncogene 27:5612-623 CrossRef
  49. Sun XH, Copeland NG, Jenkins NA, Baltimore D (1991) Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol Cell Biol 11:5603-611
  50. Tang R, Hirsch P, Fava F, Lapusan S, Marzac C, Teyssandier I, Pardo J, Marie JP, Legrand O (2009) High Id1 expression is associated with poor prognosis in 237 patients with acute myeloid leukemia. Blood 114:2993-000 CrossRef
  51. Wazir U, Jiang WG, Sharma AK, Newbold RF, Mokbel K (2013) The mRNA expression of inhibitors of DNA binding-1 and -2 is associated with advanced tumour stage and adverse clinical outcome in human breast cancer. Anticancer Res 33:2179-183
  52. Wilson JW, Deed RW, Inoue T, Balzi M, Becciolini A, Faraoni P, Potten CS, Norton JD (2001) Expression of Id helix-loop-helix proteins in colorectal adenocarcinoma correlates with p53 expression and mitotic index. Cancer Res 61:8803-810
  53. Wong YC, Wang X, Ling MT (2004) Id-1 expression and cell survival. Apoptosis 9:279-89 CrossRef
  54. Yang HY, Liu HL, Ke J, Wu H, Zhu H, Liu JR, Liu LX, Jiang HC (2010) Expression and prognostic value of Id protein family in human breast carcinoma. Oncol Rep 23:321-28 CrossRef
  55. Yang HY, Liu HL, Liu GY, Zhu H, Meng QW, Qu LD, Liu LX, Jiang HC (2011) Expression and prognostic values of Id-1 and Id-3 in gastric adenocarcinoma. J Surg Res 167:258-66 CrossRef
  56. Yokota Y, Mori S (2002) Role of Id family proteins in growth control. J Cell Physiol 190:21-8 CrossRef
  57. Zebedee Z, Hara E (2001) Id proteins in cell cycle control and cellular senescence. Oncogene 20:8317-325 CrossRef
  
• 作者单位：Annette M. May (1)
  Anna-Verena Frey (1)
  Lioudmila Bogatyreva (2)
  Marco Benkisser-Petersen (3) (4)
  Dieter Hauschke (2)
  Michael Lübbert (3) (6)
  Ralph W?sch (3) (6)
  Martin Werner (1) (6) (7)
  Jens Hasskarl (3)
  Silke Lassmann (1) (5) (6) (7)
  
  1. Department of Pathology, University Medical Center, Breisacher Str. 115a, 79106, Freiburg, Germany
  2. Institute of Medical Biometry and Medical Informatics, University Medical Center, Freiburg, Germany
  3. Department of Hematology and Oncology, Comprehensive Cancer Center Freiburg (CCCF), University Medical Center, Freiburg, Germany
  4. Faculty of Biology, BIOSS Centre for Biological Signalling Studies, Albert-Ludwigs-University, Freiburg, Germany
  6. Comprehensive Cancer Center Freiburg (CCCF), University Medical Center, Freiburg, Germany
  7. German Cancer Consortium (DKTK) and German Cancer Research Center (DKFZ), Heidelberg, Germany
  5. BIOSS Centre for Biological Signalling Studies, Albert-Ludwigs-University, Freiburg, Germany
  
• ISSN：1432-119X

文摘

The inhibitors of DNA binding (ID) inhibit basic helix-loop-helix transcription factors and thereby guide cellular differentiation and proliferation. To elucidate the involvement of IDs in hematopoiesis and acute leukemias (AL), we analyzed ID2 and ID3 expression in hematopoiesis and leukemic blasts in bone marrow biopsies (BMB). BMB of healthy stem cell donors (n?=?19) and BMB of patients with acute myeloid leukemia (AML) with myelodysplasia-related changes (AML-MD; n?=?19), de novo AML (n?=?20), B-acute lymphoblastic leukemia (B-ALL) (n?=?23), T-ALL (n?=?19), were immunohistochemically stained for ID2 and ID3 expression. The expression patterns were evaluated and quantified for each hematopoietic lineage and each leukemia subtype. In normal BMB, immature granulopoiesis showed weak ID2 and strong ID3 expression, which was lost during maturation (p?<?0.001). Erythropoiesis remained negative for ID2/3 (p?<?0.001). ID2/3 expression differed between immature granulopoiesis and leukemic blasts (p?<?0.001). Moreover, differential ID2/3 expression was seen between AL subgroups: AML, especially AML-MD, had more ID2- (p?<?0.001) and ID3-positive (p?<?0.001) blasts than ALL. We show a comprehensive in situ picture of ID2/3 expression in hematopoiesis and AL. Morphologically, ID2/3 proteins seem to be involved in the granulopoietic maturation. Importantly, the distinct ID2/3 expression patterns in AL indicate a specific deregulation of ID2/3 in the various types of AL and may support subtyping of AL.