Id proteins: Small molecules, mighty regulators

Current Topics in Developmental Biology

Volumn 110, Issue , 2014, Pages 189-216

  Ling, Flora ^a   Kang, Bin ^a   Sun, Xiao Hong ^a  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

E protein; E2A; Helix loop helix; Id1; Id2; Id3; Id4

Indexed keywords

ID1 PROTEIN, HUMAN; INHIBITOR OF DIFFERENTIATION 1; INHIBITOR OF DIFFERENTIATION PROTEIN;

ADIPOGENESIS; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNE SYSTEM; METABOLISM; MOLECULAR GENETICS; NEOPLASM; PHYSIOLOGY; STEM CELL;

ADIPOGENESIS; AMINO ACID SEQUENCE; ANIMALS; GENE EXPRESSION REGULATION; HUMANS; IMMUNE SYSTEM; INHIBITOR OF DIFFERENTIATION PROTEIN 1; INHIBITOR OF DIFFERENTIATION PROTEINS; MOLECULAR SEQUENCE DATA; NEOPLASMS; STEM CELLS;

EID: 84907710593     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-405943-6.00005-1     Document Type: Chapter

References (148)

1. Alani R.M., Young A.Z., Shifflett C.B. Id1 regulation of cellular senescence through transcriptional repression of p16/Ink4a. Proceedings of the National Academy of Sciences of United States of America 2001, 98:7812-7816.
2. Ao J., Meng J., Zhu L., Nie H., Yang C., Li J., et al. Activation of androgen receptor induces ID1 and promotes hepatocellular carcinoma cell migration and invasion. Molecular Oncology 2012, 6:507-515.
3. Asirvatham A.J., Carey J.P., Chaudhary J. ID1-, ID2-, and ID3-regulated gene expression in E2A positive or negative prostate cancer cells. Prostate 2007, 67:1411-1420.
4. Asirvatham A.J., Schmidt M.A., Chaudhary J. Non-redundant inhibitor of differentiation (Id) gene expression and function in human prostate epithelial cells. Prostate 2006, 66:921-935.
5. Bai X., Cerimele F., Ushio-Fukai M., Waqas M., Campbell P.M., Govindarajan B., et al. Honokiol, a small molecular weight natural product, inhibits angiogenesis in vitro and tumor growth in vivo. Journal of Biological Chemistry 2003, 278:35501-35507.
6. Bai G., Sheng N., Xie Z., Bian W., Yokota Y., Benezra R., et al. Id sustains Hes1 expression to inhibit precocious neurogenesis by releasing negative autoregulation of Hes1. Developmental Cell 2007, 13:283-297.
7. Bain G., Cravatt C.B., Loomans C., Alberola-Ila J., Hedrick S.M., Murre C. Regulation of the helix-loop-helix proteins, E2A and Id3, by the Ras- ERK MAPK cascade. Nature Immunology 2001, 2:165-171.
8. Bain G., Engel I., Robanus Maandag E.C., te Riele H.P., Voland J.R., Sharp L.L., et al. E2A deficiency leads to abnormalities in alphabeta T-cell development and to rapid development of T-cell lymphomas. Molecular and Cellular Biology 1997, 17:4782-4791.
9. Ball A.J., Levine F. Telomere-independent cellular senescence in human fetal cardiomyocytes. Aging Cell 2005, 4:21-30.
10. Barak Y., Nelson M.C., Ong E.S., Jones Y.Z., Ruiz-Lozano P., Chien K.R., et al. PPAR gamma is required for placental, cardiac, and adipose tissue development. Molecular Cell 1999, 4:585-595.
11. Barone M.V., Pepperkok R., Peverali F.A., Philipson L. Id proteins control growth induction in mammalian cells. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:4985-4988.
12. Bendelac A., Savage P.B., Teyton L. The biology of NKT cells. Annual Review of Immunology 2007, 25:297-336.
13. Benezra R., Davis R.L., Lockshon D., Turner D.L., Weintraub H. Τhe protein Id: A negative regulator of helix-loop-helix DNA binding proteins. Cell 1990, 61:49-59.
14. Beyan E., Beyan C., Turan M. Hematological presentation in systemic lupus erythematosus and its relationship with disease activity. Hematology 2007, 12:257-261.
15. Boos M.D., Yokota Y., Eberl G., Kee B.L. Mature natural killer cell and lymphoid tissue-inducing cell development requires Id2-mediated suppression of E protein activity. Journal of Experimental Medicine 2007, 204:1119-1130.
16. Cammenga J., Mulloy J.C., Berguido F.J., MacGrogan D., Viale A., Nimer S.D. Induction of C/EBPalpha activity alters gene expression and differentiation of human CD34+ cells. Blood 2003, 101:2206-2214.
17. Cao Y. Angiogenesis as a therapeutic target for obesity and metabolic diseases. Chemical Immunology and Allergy 2014, 99:170-179.
18. Carey J.P., Knowell A.E., Chinaranagari S., Chaudhary J. Id4 promotes senescence and sensitivity to doxorubicin-induced apoptosis in DU145 prostate cancer cells. Anticancer Research 2013, 33:4271-4278.
19. Cheung P.Y., Yip Y.L., Tsao S.W., Ching Y.P., Cheung A.L. Id-1 induces cell invasiveness in immortalized epithelial cells by regulating cadherin switching and Rho GTPases. Journal of Cellular Biochemistry 2011, 112:157-168.
20. Christy B.A., Sanders L.K., Lau L.F., Copeland N.G., Jenkins N.A., Nathans D. An Id-related helix-loop-helix protein encoded by a growth factor-inducible gene. Proceedings of the National Academy of Sciences of the United States of America 1991, 88:1815-1819.
21. Ciarrocchi A., Piana S., Valcavi R., Gardini G., Casali B. Inhibitor of DNA binding-1 induces mesenchymal features and promotes invasiveness in thyroid tumour cells. European Journal of Cancer 2011, 47:934-945.
22. Cochrane S.W., Zhao Y., Welner R.S., Sun X.H. Balance between Id and E proteins regulates myeloid-versus-lymphoid lineage decisions. Blood 2009, 113:1016-1026.
23. Cutchins A., Harmon D.B., Kirby J.L., Doran A.C., Oldham S.N., Skaflen M., et al. Inhibitor of differentiation-3 mediates high fat diet-induced visceral fat expansion. Arteriosclerosis, Thrombosis, and Vascular Biology 2012, 32:317-324.
24. Deed R.W., Hara E., Atherton G.T., Peters G., Norton J.D. Regulation of Id3 cell cycle function by Cdk-2-dependent phosphorylation. Molecular and Cellular Biology 1997, 17:6815-6821.
25. Desprez P.Y., Lin C.Q., Thomasset N., Sympson C.J., Bissell M.J., Campisi J. A novel pathway for mammary epithelial cell invasion induced by the helix-loop-helix protein Id-1. Molecular and Cellular Biology 1998, 18:4577-4588.
26. Dias S., Mansson R., Gurbuxani S., Sigvardsson M., Kee B.L. E2A proteins promote development of lymphoid-primed multipotent progenitors. Immunity 2008, 29:217-227.
27. Doran A.C., Lehtinen A.B., Meller N., Lipinski M.J., Slayton R.P., Oldham S.N., et al. Id3 is a novel atheroprotective factor containing a functionally significant single-nucleotide polymorphism associated with intima-media thickness in humans. Circulation Research 2010, 106:1303-1311.
28. Doran A.C., Lipinski M.J., Oldham S.N., Garmey J.C., Campbell K.A., Skaflen M.D., et al. B-cell aortic homing and atheroprotection depend on Id3. Circulation Research 2012, 110:e1-e12.
29. Doran A.C., Meller N., Cutchins A., Deliri H., Slayton R.P., Oldham S.N., et al. The helix-loop-helix factors Id3 and E47 are novel regulators of adiponectin. Circulation Research 2008, 103:624-634.
30. Engel I., Murre C. Disruption of pre-TCR expression accelerates lymphomagenesis in E2A- deficient mice. Proceedings of the National Academy of the Sciences of the United States of America 2002, 99:11322-11327.
31. Fong S., Itahana Y., Sumida T., Singh J., Coppe J.P., Liu Y., et al. Id-1 as a molecular target in therapy for breast cancer cell invasion and metastasis. Proceedings of the National Academy of the Sciences of the United States of America 2003, 100:13543-13548.
32. Guo Z., Li H., Han M., Xu T., Wu X., Zhuang Y. Modeling Sjogren's syndrome with Id3 conditional knockout mice. Immunology Letters 2011, 135:34-42.
33. Gupta G.P., Perk J., Acharyya S., De C.P., Mittal V., Todorova-Manova K. ID genes mediate tumor reinitiation during breast cancer lung metastasis. Proceedings of the National Academy of the Sciences of the United States of America 2007, 104:19506-19511.
34. Hara E., Hall M., Peters G. Cdk2-dependent phosphorylation of Id2 modulates activity of E2A-related transcription factors. EMBO Journal 1997, 16:332-342.
35. Hayakawa I., Tedder T.F., Zhuang Y. B-lymphocyte depletion ameliorates Sjogren's syndrome in Id3 knockout mice. Immunology 2007, 122:73-79.
36. Heemskerk M.H., Blom B., Oda K., Stegmann A.P., Bakker A.Q., Weijer K., et al. Inhibition of T cell and promotion of natural killer cell development by the dominant negative helix loop helix factor Id3. Journal of Experimental Medicine 1997, 186:1597-1602.
37. Hollnagel A., Oehlmann V., Heymer J., Ruther U., Nordheim A. Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells. Journal of Biological Chemistry 1999, 274:19838-19845.
38. Hu T., Wang H., Simmons A., Bajana S., Zhao Y., Kovats S., et al. Increased level of E protein activity during invariant NKT development promotes differentiation of invariant NKT2 and invariant NKT17 subsets. Journal of Immunology 2013, 191:5065-5073.
39. Hwang Y.Y., McKenzie A.N. Innate lymphoid cells in immunity and disease. Advances in Experimental Medicine & Biology 2013, 785:9-26.
40. Ikuta K., Weissman I.L. Evidence that hematopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation. Proceedings of the National Academy of the Sciences of the United States of America 1992, 89:1502-1506.
41. Itahana Y., Singh J., Sumida T., Coppe J.P., Parrinello S., Bennington J.L., et al. Role of Id-2 in the maintenance of a differentiated and noninvasive phenotype in breast cancer cells. Cancer Research 2003, 63:7098-7105.
42. Jackson J.T., Hu Y., Liu R., Masson F., D'Amico A., Carotta S., et al. Id2 expression delineates differential checkpoints in the genetic program of CD8alpha+ and CD103+ dendritic cell lineages. EMBO Journal 2011, 30:2690-2704.
43. Jankovic V., Ciarrocchi A., Boccuni P., Deblasio T., Benezra R., Nimer S.D. Id1 restrains myeloid commitment, maintaining the self-renewal capacity of hematopoietic stem cells. Proceedings of the National Academy of the Sciences of the United States of America 2007, 104:1260-1265.
44. Ji M., Li H., Suh H.C., Klarmann K.D., Yokota Y., Keller J.R. Id2 intrinsically regulates lymphoid and erythroid development via interaction with different target proteins. Blood 2008, 112:1068-1077.
45. Jones M.E., Zhuang Y. Acquisition of a functional T cell receptor during T lymphocyte development is enforced by HEB and E2A transcription factors. Immunity 2007, 27:860-870.
46. Jones-Mason M.E., Zhao X., Kappes D., Lasorella A., Iavarone A., Zhuang Y. E protein transcription factors are required for the development of CD4(+) lineage T cells. Immunity 2012, 36:348-361.
47. Jung S., Park R.H., Kim S., Jeon Y.J., Ham D.S., Jung M.Y., et al. Id proteins facilitate self-renewal and proliferation of neural stem cells. Stem Cells and Development 2010, 19:831-841.
48. Karaya K., Mori S., Kimoto H., Shima Y., Tsuji Y., Kurooka H., et al. Regulation of Id2 expression by CCAAT/enhancer binding protein beta. Nucleic Acids Research 2005, 33:1924-1934.
49. Katagiri T., Imada M., Yanai T., Suda T., Takahashi N., Kamijo R. Identification of a BMP-responsive element in Id1, the gene for inhibition of myogenesis. Genes to Cells 2002, 7:949-960.
50. Kee B.L. E and ID proteins branch out. Nature Reviews Immunology 2009, 9:175-184.
51. Kim D., Peng X.C., Sun X.H. Massive apoptosis of thymocytes in T-cell-deficient Id1 transgenic mice. Molecular and Cellular Biology 1999, 19:8240-8253.
52. Kim D., Xu M., Nie L., Peng X.C., Jimi E., Voll R.E., et al. Helix-loop-helix proteins regulate pre-TCR and TCR signaling through modulation of Rel/NF-kappaB activities. Immunity 2002, 16:9-21.
53. Kusunoki T., Sugai M., Katakai T., Omatsu Y., Iyoda T., Inaba K., et al. TH2 dominance and defective development of a CD8+ dendritic cell subset in Id2-deficient mice. Journal of Allergy and Clinical Immunology 2003, 111:136-142.
54. Lasorella A., Boldrini R., Dominici C., Donfrancesco A., Yokota Y., Inserra A., et al. Id2 is critical for cellular proliferation and is the oncogenic effector of N-myc in human neuroblastoma. Cancer Research 2002, 62:301-306.
55. Lasorella A., Iavarone A., Israel M.A. Id2 specifically alters regulation of the cell cycle by tumor suppressor proteins. Molecular and Cellular Biology 1996, 16:2570-2578.
56. Lasorella A., Noseda M., Beyna M., Yokota Y., Iavarone A. Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins. Nature 2000, 407:592-598.
57. Li H., Dai M., Zhuang Y. A T cell intrinsic role of Id3 in a mouse model for primary Sjogren's syndrome. Immunity 2004, 21:551-560.
58. Li H., Ji M., Klarmann K.D., Keller J.R. Repression of Id2 expression by Gfi-1 is required for B-cell and myeloid development. Blood 2010, 116:1060-1069.
59. Li J., Wu D., Jiang N., Zhuang Y. Combined deletion of Id2 and Id3 genes reveals multiple roles for E proteins in invariant NKT cell development and expansion. Journal of Immunology 2013, 191:5052-5064.
60. Lin J., Guan Z., Wang C., Feng L., Zheng Y., Caicedo E., et al. Inhibitor of differentiation 1 contributes to head and neck squamous cell carcinoma survival via the NF-kappaB/survivin and phosphoinositide 3-kinase/Akt signaling pathways. Clinical Cancer Research 2010, 16:77-87.
61. Ling M.T., Wang X., Lee D.T., Tam P.C., Tsao S.W., Wong Y.C. Id-1 expression induces androgen-independent prostate cancer cell growth through activation of epidermal growth factor receptor (EGF-R). Carcinogenesis 2004, 25:517-525.
62. Ling M.T., Wang X., Ouyang X.S., Xu K., Tsao S.W., Wong Y.C. Id-1 expression promotes cell survival through activation of NF-kappaB signalling pathway in prostate cancer cells. Oncogene 2003, 22:4498-4508.
63. Lipinski M.J., Campbell K.A., Duong S.Q., Welch T.J., Garmey J.C., Doran A.C., et al. Loss of Id3 increases VCAM-1 expression, macrophage accumulation, and atherogenesis in Ldlr-/- mice. Arteriosclerosis, Thrombosis, and Vascular Biology 2012, 32:2855-2861.
64. Liu H., Jia D., Li A., Chau J., He D., Ruan X., et al. p53 regulates neural stem cell proliferation and differentiation via BMP-Smad1 signaling and Id1. Stem Cells and Development 2013, 22:913-927.
65. Lowery J.W., Frump A.L., Anderson L., DiCarlo G.E., Jones M.T., de Caestecker M.P. ID family protein expression and regulation in hypoxic pulmonary hypertension. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 2010, 299:R1463-R1477.
66. Lyden D., Hattori K., Dias S., Costa C., Blaikie P., Butros L., et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nature Medicine 2001, 7:1194-1201.
67. Lyden D., Young A.Z., Zagzag D., Yan W., Gerald W., O'Reilly R., et al. Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 1999, 401:670-677.
68. Maeda K., Malykhin A., Teague-Weber B.N., Sun X.H., Farris A.D., Coggeshall K.M. Interleukin-6 aborts lymphopoiesis and elevates production of myeloid cells in systemic lupus erythematosus-prone B6.Sle1.Yaa animals. Blood 2009, 113:4534-4540.
69. Mahlios J., Zhuang Y. Contribution of IL-13 to early exocrinopathy in Id3-/- mice. Molecular Immunology 2011, 49:227-233.
70. Martini M., Cenci T., D'Alessandris G.Q., Cesarini V., Cocomazzi A., Ricci-Vitiani L., et al. Epigenetic silencing of Id4 identifies a glioblastoma subgroup with a better prognosis as a consequence of an inhibition of angiogenesis. Cancer 2013, 119:1004-1012.
71. Maruyama T., Li J., Vaque J.P., Konkel J.E., Wang W., Zhang B., et al. Control of the differentiation of regulatory T cells and T(H)17 cells by the DNA-binding inhibitor Id3. Nature Immunology 2011, 12:86-95.
72. Massari M.E., Murre C. Helix-loop-helix proteins: Regulators of transcription in eucaryotic organisms. Molecular and Cellular Biology 2000, 20:429-440.
73. Mern D.S., Hoppe-Seyler K., Hoppe-Seyler F., Hasskarl J., Burwinkel B. 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 Research and Treatment 2010, 124:623-633.
74. Miyazono K., Miyazawa K. A target of BMP signaling. Science's Signal Transduction Knowledge Environment 2002, 2002:E40.
75. Moldes M., Lasnier F., Feve B., Pairault J., Djian P. Id3 prevents differentiation of preadipose cells. Molecular and Cellular Biology 1997, 17:1796-1804.
76. Morrison S.J., Weissman I.L. The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1994, 1:661-673.
77. Morrow M.A., Mayer E.W., Perez C.A., Adlam M., Siu G. Overexpression of the helix-loop-helix protein Id2 blocks T cell development at multiple stages. Molecular Immunology 1999, 36:491-503.
78. Mui A.L., Wakao H., Kinoshita T., Kitamura T., Miyajima A. Suppression of interleukin-3-induced gene expression by a C-terminal truncated Stat5: Role of Stat5 in proliferation. EMBO Journal 1996, 15:2425-2433.
79. Murad J.M., Place C.S., Ran C., Hekmatyar S.K., Watson N.P., Kauppinen R.A., et al. Inhibitor of DNA binding 4 (ID4) regulation of adipocyte differentiation and adipose tissue formation in mice. Journal of Biological Chemistry 2010, 285:24164-24173.
80. Murre C. Helix-loop-helix proteins and lymphocyte development. Nature Immunology 2005, 6:1079-1086.
81. Nakahiro T., Kurooka H., Mori K., Sano K., Yokota Y. Identification of BMP-responsive elements in the mouse Id2 gene. Biochemical and Biophysical Research Communications 2010, 399:416-421.
82. Nam H.S., Benezra R. High levels of Id1 expression define B1 type adult neural stem cells. Cell Stem Cell 2009, 5:515-526.
83. Nickoloff B.J., Chaturvedi V., Bacon P., Qin J.Z., Denning M.F., Diaz M.O. Id-1 delays senescence but does not immortalize keratinocytes. Journal of Biological Chemistry 2000, 275:27501-27504.
84. Nieborowska-Skorska M., Hoser G., Rink L., Malecki M., Kossev P., Wasik M.A., et al. Id1 transcription inhibitor-matrix metalloproteinase 9 axis enhances invasiveness of the breakpoint cluster region/abelson tyrosine kinase-transformed leukemia cells. Cancer Research 2006, 66:4108-4116.
85. Nishiyama K., Takaji K., Kataoka K., Kurihara Y., Yoshimura M., Kato A., et al. Id1 gene transfer confers angiogenic property on fully differentiated endothelial cells and contributes to therapeutic angiogenesis. Circulation 2005, 112:2840-2850.
86. O'Brien C.A., Kreso A., Ryan P., Hermans K.G., Gibson L., Wang Y., et al. ID1 and ID3 regulate the self-renewal capacity of human colon cancer-initiating cells through p21. Cancer Cell 2012, 21:777-792.
87. Ohtani N., Zebedee Z., Huot T.J., Stinson J.A., Sugimoto M., Ohashi Y., et al. Opposing effects of Ets and Id proteins on p16INK4a expression during cellular senescence. Nature 2001, 409:1067-1070.
88. Ouyang X.S., Wang X., Lee D.T., Tsao S.W., Wong Y.C. Over expression of ID-1 in prostate cancer. Journal of Urology 2002, 167:2598-2602.
89. Owens A.P., Subramanian V., Moorleghen J.J., Guo Z., McNamara C.A., Cassis L.A., et al. Angiotensin II induces a region-specific hyperplasia of the ascending aorta through regulation of inhibitor of differentiation 3. Circulation Research 2010, 106:611-619.
90. Paolella B.R., Havrda M.C., Mantani A., Wray C.M., Zhang Z., Israel M.A. p53 directly represses Id2 to inhibit the proliferation of neural progenitor cells. Stem Cells 2011, 29:1090-1101.
91. Park S.T., Nolan G.P., Sun X.-H. Growth inhibition and apoptosis due to restoration of E2A activity in T cell acute lymphoblastic leukemia cells. Journal of Experimental Medicine 1999, 189:501-508.
92. Park S.T., Sun X.H. The Tal1 oncoprotein inhibits E47-mediated transcription mechanism of inhibition. Journal of Bioliological Chemistry 1998, 273:7030-7037.
93. Park K.W., Waki H., Villanueva C.J., Monticelli L.A., Hong C., Kang S., et al. Inhibitor of DNA binding 2 is a small molecule-inducible modulator of peroxisome proliferator-activated receptor-gamma expression and adipocyte differentiation. Molecular Endocrinology 2008, 22:2038-2048.
94. Peng X., Wang Y., Kolli S., Deng J., Li L., Wang Z., et al. Physical and functional interaction between the ID1 and p65 for activation of NF-kappaB. American Journal of Physiology-Cell Physiology 2012, 303:C267-C277.
95. Perry S.S., Zhao Y., Nie L., Cochrane S.W., Huang Z., Sun X.H. Id1, but not Id3, directs long-term repopulating hematopoietic stem-cell maintenance. Blood 2007, 110:2351-2360.
96. Peverali F.A., Ramqvist T., Saffrich R., Pepperkik R., Barone M.V., Philipson L. Regulation of G1 progression by E2A and Id helix-loop-helix proteins. EMBO Journal 1994, 13:4291-4301.
97. Pillai S., Rizwani W., Li X., Rawal B., Nair S., Schell M.J., et al. ID1 facilitates the growth and metastasis of non-small cell lung cancer in response to nicotinic acetylcholine receptor and epidermal growth factor receptor signaling. Molecular and Cellular Biology 2011, 31:3052-3067.
98. Prabhu S., Ignatova A., Park S.T., Sun X.-H. Regulation of the expression of cyclin-dependent kinase inhibitor p21 by E2A and ID proteins. Molecular and Cellular Biology 1997, 17:5888-5896.
99. Riechmann V., van Cruchten I., Sablitzky F. The expression pattern of Id4, a novel dominant negative helix-loop-helix protein, is distinct from Id1, Id2 and Id3. Nucleic Acids Research 1994, 22:749-755.
100. Roberts E.C., Deed R.W., Inoue T., Norton J.D., Sharrocks A.D. Id helix-loop-helix proteins antagonize pax transcription factor activity by inhibiting DNA binding. Molecular and Cellular Biology 2001, 21:524-533.
101. Rosen E.D., Sarraf P., Troy A.E., Bradwin G., Moore K., Milstone D.S., et al. PPAR gamma is required for the differentiation of adipose tissue in vivo and in vitro. Molecular Cell 1999, 4:611-617.
102. Ruzinova M.B., Benezra R. Id proteins in development, cell cycle and cancer. Trends in Cell Biology 2003, 13:410-418.
103. Ruzinova M.B., Schoer R.A., Gerald W., Egan J.E., Pandolfi P.P., Rafii S., et al. Effect of angiogenesis inhibition by Id loss and the contribution of bone-marrow-derived endothelial cells in spontaneous murine tumors. Cancer Cell 2003, 4:277-289.
104. Saisanit S., Sun X.H. A novel enhancer, the pro-B enhancer, regulates Id1 gene expression in progenitor B cells. Molecular and Cellular Biology 1995, 15:1513-1521.
105. Saisanit S., Sun X.H. Regulation of the pro-B-cell-specific enhancer of the Id1 gene involves the C/EBP family of proteins. Molecular and Cellular Biology 1997, 17:844-850.
106. Samanta J., Kessler J.A. Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development 2004, 131:4131-4142.
107. Satyanarayana A., Klarmann K.D., Gavrilova O., Keller J.R. Ablation of the transcriptional regulator Id1 enhances energy expenditure, increases insulin sensitivity, and protects against age and diet induced insulin resistance, and hepatosteatosis. FASEB Journal 2012, 26:309-323.
108. Sellam J., Miceli-Richard C., Gottenberg J.E., Proust A., Ittah M., Lavie F., et al. Is Inhibitor of differentiation 3 involved in human primary Sjogren's syndrome?. Rheumatology (Oxford) 2008, 47:437-441.
109. Sequerra E.B., Costa M.R., Menezes J.R., Hedin-Pereira C. Adult neural stem cells: Plastic or restricted neuronal fates?. Development 2013, 140:3303-3309.
110. Sharma P., Patel D., Chaudhary J. Id1 and Id3 expression is associated with increasing grade of prostate cancer: Id3 preferentially regulates CDKN1B. Cancer Medicine 2012, 1:187-197.
111. Shimano H., Shimomura I., Hammer R.E., Herz J., Goldstein J.L., Brown M.S., et al. Elevated levels of SREBP-2 and cholesterol synthesis in livers of mice homozygous for a targeted disruption of the SREBP-1 gene. Journal of Clinical Investigation 1997, 100:2115-2124.
112. Shuno Y., Tsuno N.H., Okaji Y., Tsuchiya T., Sakurai D., Nishikawa T., et al. Id1/Id3 knockdown inhibits metastatic potential of pancreatic cancer. Journal of Surgical Research 2010, 161:76-82.
113. Sikder H., Huso D.L., Zhang H., Wang B., Ryu B., Hwang S.T., et al. Disruption of Id1 reveals major differences in angiogenesis between transplanted and autochthonous tumors. Cancer Cell 2003, 4:291-299.
114. Spangrude G.J., Heimfeld S., Weissman I.L. Purification and characterization of mouse hematopoietic stem cells. Science 1988, 241:58-62.
115. Spits H., Couwenberg F., Bakker A.Q., Weijer K., Uittenbogaart C.H. Id2 and Id3 inhibit development of CD34(+) stem cells into predendritic cell (pre-DC)2 but not into pre-DC1. Evidence for a lymphoid origin of pre-DC2. Journal of Experimental Medicine 2000, 192:1775-1784.
116. Spits H., Di Santo J.P. The expanding family of innate lymphoid cells: Regulators and effectors of immunity and tissue remodeling. Nature Immunology 2011, 12:21-27.
117. Stankic M., Pavlovic S., Chin Y., Brogi E., Padua D., Norton L., et al. TGF-beta-Id1 signaling opposes Twist1 and promotes metastatic colonization via a mesenchymal-to-epithelial transition. Cell Reports 2013, 5:1228-1242.
118. Stighall M., Manetopoulos C., Axelson H., Landberg G. High ID2 protein expression correlates with a favourable prognosis in patients with primary breast cancer and reduces cellular invasiveness of breast cancer cells. International Journal of Cancer 2005, 115:403-411.
119. Su Y., Gao L., Teng L., Wang Y., Cui J., Peng S., et al. Id1 enhances human ovarian cancer endothelial progenitor cell angiogenesis via PI3K/Akt and NF-kappaB/MMP-2 signaling pathways. Journal of Translational Medicine 2013, 11:132.
120. Suh H.C., Ji M., Gooya J., Lee M., Klarmann K.D., Keller J.R. Cell-nonautonomous function of Id1 in the hematopoietic progenitor cell niche. Blood 2009, 114:1186-1195.
121. Sun X.-H. Constitutive expression of the Id1 gene impairs mouse B cell development. Cell 1994, 79:893-900.
122. Sun X.-H., Copeland N.G., Jenkins N.A., Baltimore D. Id proteins, Id1 and Id2, selectively inhibit DNA binding by one class of helix-loop-helix proteins. Molecular and Cellular Biology 1991, 11:5603-5611.
123. Swarbrick A., Roy E., Allen T., Bishop J.M. Id1 cooperates with oncogenic Ras to induce metastatic mammary carcinoma by subversion of the cellular senescence response. Proceedings of the National Academy of Sciences pf the United States of America 2008, 105:5402-5407.
124. Tang J., Gordon G.M., Nickoloff B.J., Foreman K.E. The helix-loop-helix protein id-1 delays onset of replicative senescence in human endothelial cells. Laboratory Investigation 2002, 82:1073-1079.
125. Taylor A.M., Li F., Thimmalapura P., Gerrity R.G., Sarembock I.J., Forrest S., et al. Hyperlipemia and oxidation of LDL induce vascular smooth muscle cell growth: An effect mediated by the HLH factor Id3. Journal of Vascular Research 2006, 43:123-130.
126. Tobin N.P., Sims A.H., Lundgren K.L., Lehn S., Landberg G. Cyclin D1, Id1 and EMT in breast cancer. BMC Cancer 2011, 11:417.
127. Ueda-Hayakawa I., Mahlios J., Zhuang Y. Id3 restricts the developmental potential of gamma delta lineage during thymopoiesis. Journal of Immunology 2009, 182:5306-5316.
128. Valdimarsdottir G., Goumans M.J., Rosendahl A., Brugman M., Itoh S., Lebrin F., et al. Stimulation of Id1 expression by bone morphogenetic protein is sufficient and necessary for bone morphogenetic protein-induced activation of endothelial cells. Circulation 2002, 106:2263-2270.
129. Verykokakis M., Krishnamoorthy V., Iavarone A., Lasorella A., Sigvardsson M., Kee B.L. Essential functions for ID proteins at multiple checkpoints in invariant NKT cell development. Journal of Immunology 2013, 191:5973-5983.
130. Volpert O.V., Pili R., Sikder H.A., Nelius T., Zaichuk T., Morris C., et al. Id1 regulates angiogenesis through transcriptional repression of thrombospondin-1. Cancer Cell 2002, 2:473-483.
131. Vrijens K., Lin W., Cui J., Farmer D., Low J., Pronier E., et al. Identification of small molecule activators of BMP signaling. PLoS One 2013, 8:e59045.
132. Wagner K., Zhang P., Rosenbauer F., Drescher B., Kobayashi S., Radomska H.S., et al. Absence of the transcription factor CCAAT enhancer binding protein alpha results in loss of myeloid identity in bcr/abl-induced malignancy. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:6338-6343.
133. Wazir U., Jiang W.G., Sharma A.K., Newbold R.F., Mokbel K. 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 Research 2013, 33:2179-2183.
134. Wu Z., Bucher N.L., Farmer S.R. Induction of peroxisome proliferator-activated receptor gamma during the conversion of 3T3 fibroblasts into adipocytes is mediated by C/EBPbeta, C/EBPdelta, and glucocorticoids. Molecular and Cellular Biology 1996, 16:4128-4136.
135. Wu Z., Rosen E.D., Brun R., Hauser S., Adelmant G., Troy A.E., et al. Cross-regulation of C/EBP alpha and PPAR gamma controls the transcriptional pathway of adipogenesis and insulin sensitivity. Molecular Cell 1999, 3:151-158.
136. Xu M., Nie L., Kim S.H., Sun X.H. STAT5-induced Id-1 transcription involves recruitment of HDAC1 and deacetylation of C/EBPbeta. EMBO Journal 2003, 22:893-904.
137. Yamauchi T., Kadowaki T. Adiponectin receptor as a key player in healthy longevity and obesity-related diseases. Cell Metabolism 2013, 17:185-196.
138. Yan W., Young A.Z., Soares V.C., Kelley R., Benezra R., Zhuang Y. High incidence of T-cell tumors in E2A-null mice and E2A/Id1 double-knockout mice. Molecular and Cellular Biology 1997, 17:7317-7327.
139. Yang J., Li X., Li Y., Southwood M., Ye L., Long L., et al. Id proteins are critical downstream effectors of BMP signaling in human pulmonary arterial smooth muscle cells. American Journal of Physiology. Lung Cellular and Molecular Physiology 2013, 305:L312-L321.
140. Yang Y., Liou H.C., Sun X.H. Id1 potentiates NF-kappaB activation upon T cell receptor signaling. Journal of Biological Chemistry 2006, 281:34989-34996.
141. Yeh W.C., Cao Z., Classon M., McKnight S.L. Cascade regulation of terminal adipocyte differentiation by three members of the C/EBP family of leucine zipper proteins. Genes and Development 1995, 9:168-181.
142. Yokota Y., Mansouri A., Mori S., Sugawara S., Adachi S., Nishikawa S., et al. Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 1999, 397:702-706.
143. Zeng H., Yucel R., Kosan C., Klein-Hitpass L., Moroy T. Transcription factor Gfi1 regulates self-renewal and engraftment of hematopoietic stem cells. EMBO Journal 2004, 23:4116-4125.
144. Zhang X., Ling M.T., Wang Q., Lau C.K., Leung S.C., Lee T.K., et al. Identification of a novel inhibitor of differentiation-1 (ID-1) binding partner, caveolin-1, and its role in epithelial-mesenchymal transition and resistance to apoptosis in prostate cancer cells. Journal of Biological Chemistry 2007, 282:33284-33294.
145. Zhang P., Zhao Y., Sun X.H. Notch-regulated periphery B cell differentiation involves suppression of E protein function. Journal of Immunology 2013, 191:726-736.
146. Zhao Q., Beck A.J., Vitale J.M., Schneider J.S., Gao S., Chang C., et al. Developmental ablation of Id1 and Id3 genes in the vasculature leads to postnatal cardiac phenotypes. Developmental Biology 2011, 349:53-64.
147. Zhao Y., Ling F., Wang H.C., Sun X.H. Chronic TLR signaling impairs the long-term repopulating potential of hematopoietic stem cells of wild type but not Id1 deficient mice. PLoS One 2013, 8:e55552.
148. Zheng W., Wang H., Xue L., Zhang Z., Tong T. Regulation of cellular senescence and p16(INK4a) expression by Id1 and E47 proteins in human diploid fibroblast. Journal of Biological Chemistry 2004, 279:31524-31532.