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Review Article | Open Access

Emerging roles of activating transcription factor (ATF) family members in tumourigenesis and immunity: Implications in cancer immunotherapy

Meilin ChenYijun LiuYuqin YangYanbing QiuZhicheng WangXiaoxu LiWenling Zhang( )
Department of Medical Laboratory Science, The Third Xiangya Hospital, Central South University, Changsha, Hunan 410013, PR China
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Abstract

Activating transcription factors, ATFs, are a group of bZIP transcription factors that act as homodimers or heterodimers with a range of other bZIP factors. In general, ATFs respond to extracellular signals, indicating their important roles in maintaining homeostasis. The ATF family includes ATF1, ATF2, ATF3, ATF4, ATF5, ATF6, and ATF7. Consistent with the diversity of cellular processes reported to be regulated by ATFs, the functions of ATFs are also diverse. ATFs play an important role in cell proliferation, apoptosis, differentiation and inflammation-related pathological processes. The expression and phosphorylation status of ATFs are also related to neurodegenerative diseases and polycystic kidney disease. Various miRNAs target ATFs to regulate cancer proliferation, apoptosis, autophagy, sensitivity and resistance to radiotherapy and chemotherapy. Moreover, ATFs are necessary to maintain cell redox homeostasis. Therefore, deepening our understanding of the regulation and function of ATFs will provide insights into the basic regulatory mechanisms that influence how cells integrate extracellular and intracellular signals into genomic responses through transcription factors. Under pathological conditions, especially in cancer biology and response to treatment, the characterization of ATF dysfunction is important for understanding how to therapeutically utilize ATF2 or other pathways controlled by transcription factors. In this review, we will demonstrate how ATF1, ATF2, ATF3, ATF4, ATF5, ATF6, and ATF7 function in promoting or suppressing cancer development and identify their roles in tumour immunotherapy.

References

1
Hai T. The ATF transcription factors in cellular adaptive responses. In: Gene Expression and Regulation. New York, NY: Springer; 2006: 329-340.
2

Thompson MR, Xu D, Williams BR. ATF3 transcription factor and its emerging roles in immunity and cancer. J Mol Med (Berl). 2009;87(11): 1053-1060.

3

Persengiev SP, Green MR. The role of ATF/CREB family members in cell growth, survival and apoptosis. Apoptosis. 2003;8(3): 225-228.

4

Angel P, Imagawa M, Chiu R, et al. Phorbol ester-inducible genes contain a common cis element recognized by a TPA-modulated trans-acting factor. Cell. 1987;49(6): 729-739.

5

Shaulian E, Karin M. AP-1 as a regulator of cell life and death. Nat Cell Biol. 2002;4(5): E131-E136.

6

Eferl R, Wagner EF. AP-1: a double-edged sword in tumorigenesis. Nat Rev Canc. 2003;3(11): 859-868.

7

Glover JN, Harrison SC. Crystal structure of the heterodimeric bZIP transcription factor c-Fos-c-Jun bound to DNA. Nature. 1995;373(6511): 257-261.

8

Salat-Canela C, Paulo E, Sánchez-Mir L, et al. Deciphering the role of the signal- and Sty1 kinase-dependent phosphorylation of the stress-responsive transcription factor Atf1 on gene activation. J Biol Chem. 2017;292(33): 13635-13644.

9

Al-Huseini LM, Aw Yeang HX, Sethu S, et al. Nuclear factor-erythroid 2 (NF-E2) p45-related factor-2 (Nrf2) modulates dendritic cell immune function through regulation of p38 MAPK-cAMP-responsive element binding protein/activating transcription factor 1 signaling. J Biol Chem. 2013;288(31): 22281-22288.

10

Tsai EY, Jain J, Pesavento PA, Rao A, Goldfeld AE. Tumor necrosis factor alpha gene regulation in activated T cells involves ATF-2/Jun and NFATp. Mol Cell Biol. 1996;16(2): 459-467.

11

Thomas DA, Massague J. TGF-beta directly targets cytotoxic T cell functions during tumor evasion of immune surveillance. Cancer Cell. 2005;8(5): 369-380.

12

Xu Y, Zhou W, Zhang C, et al. Long non-coding RNA RP11-552M11.4 favors tumorigenesis and development of cervical cancer via modulating miR-3941/ATF1 signaling. Int J Biol Macromol. 2019;130: 24-33.

13

Li M, Zhang D, Ge X, et al. TRAF6-p38/JNK-ATF2 axis promotes microglial inflammatory activation. Exp Cell Res. 2019;376(2): 133-148.

14

Rohini M, Arumugam B, Vairamani M, Selvamurugan N. Stimulation of ATF3 interaction with Smad4 via TGF-beta1 for matrix metalloproteinase 13 gene activation in human breast cancer cells. Int J Biol Macromol. 2019;134: 954-961.

15

Chen Y, Mi Y, Zhang X, et al. Dihydroartemisinin-induced unfolded protein response feedback attenuates ferroptosis via PERK/ATF4/HSPA5 pathway in glioma cells. J Exp Clin Cancer Res. 2019;38(1): 402.

16

Darini C, Ghaddar N, Chabot C, et al. An integrated stress response via PKR suppresses HER2+ cancers and improves trastuzumab therapy. Nat Commun. 2019;10(1): 2139.

17

Li G, Xu Y, Guan D, Liu Z, Liu DX. HSP70 protein promotes survival of C6 and U87 glioma cells by inhibition of ATF5 degradation. J Biol Chem. 2011;286(23): 20251-20259.

18

Meng J, Liu K, Shao Y, et al. ID1 confers cancer cell chemoresistance through STAT3/ATF6-mediated induction of autophagy. Cell Death Dis. 2020;11(2): 137.

19

Spaan CN, Smit WL, van Lidth de Jeude JF, et al. Expression of UPR effector proteins ATF6 and XBP1 reduce colorectal cancer cell proliferation and stemness by activating PERK signaling. Cell Death Dis. 2019;10(7): 490.

20

Gozdecka M, Breitwieser W. The roles of ATF2 (activating transcription factor 2) in tumorigenesis. Biochem Soc Trans. 2012;40(1): 230-234.

21

Hai T, Hartman MG. The molecular biology and nomenclature of the activating transcription factor/cAMP responsive element binding family of transcription factors: activating transcription factor proteins and homeostasis. Gene. 2001;273(1): 1-11.

22

Cui J, Yin Z, Liu G, et al. Activating transcription factor 1 promoted migration and invasion in lung cancer cells through regulating EGFR and MMP-2. Mol Carcinog. 2019;58(10): 1919-1924.

23

Desmeules P, Joubert P, Zhang L, et al. A subset of malignant mesotheliomas in young adults are associated with recurrent EWSR1/FUS-ATF1 fusions. Am J Surg Pathol. 2017;41(7): 980-988.

24

Thway K, Fisher C. Tumors with EWSR1-CREB1 and EWSR1-ATF1 fusions: the current status. Am J Surg Pathol. 2012;36(7): e1-e11.

25

Kujiraoka S, Tsunematsu T, Sato Y, et al. Establishment and characterization of a clear cell odontogenic carcinoma cell line with EWSR1-ATF1 fusion gene. Oral Oncol. 2017;69: 46-55.

26

Zucman J, Delattre O, Desmaze C, et al. EWS and ATF-1 gene fusion induced by t(12;22) translocation in malignant melanoma of soft parts. Nat Genet. 1993;4(4): 341-345.

27

Hao Q, Zhao X, Zhang Y, Dong Z, Hu T, Chen P. Targeting overexpressed activating transcription factor 1 (ATF1) inhibits proliferation and migration and enhances sensitivity to paclitaxel in esophageal cancer cells. Med Sci Monit Basic Res. 2017;23: 304-312.

28

Ghoneim C, Soula-Rothhut M, Blanchevoye C, Martiny L, Antonicelli F, Rothhut B. Activating transcription factor-1-mediated hepatocyte growth factor-induced down-regulation of thrombospondin-1 expression leads to thyroid cancer cell invasion. J Biol Chem. 2007;282(21): 15490-15497.

29

Ding G, Li W, Liu J, et al. LncRNA GHET1 activated by H3K27 acetylation promotes cell tumorigenesis through regulating ATF1 in hepatocellular carcinoma. Biomed Pharmacother. 2017;94: 326-331.

30

Zhao X, Weng W, Long Y, Pan W, Li Z, Sun F. LINC00665/miR-9-5p/ATF1 is a novel axis involved in the progression of colorectal cancer. Hum Cell. 2020;33(4): 1142-1154.

31

Shi Y, Wang W, Yang B, Tian H. ATF1 and RAS in exosomes are potential clinical diagnostic markers for cervical cancer. Cell Biochem Funct. 2017;35(7): 477-483.

32

Gutierrez CM, Lopez-Valdez R, Subramani R, et al. A breast tissue protein expression profile contributing to early parity-induced protection against breast cancer. Cell Physiol Biochem. 2015;37(5): 1671-1685.

33

Huang GL, Guo HQ, Yang F, et al. Activating transcription factor 1 is a prognostic marker of colorectal cancer. Asian Pac J Cancer Prev. 2012;13(3): 1053-1057.

34

Tian J, Chang J, Gong J, et al. Systematic functional interrogation of genes in GWAS loci identified ATF1 as a key driver in colorectal cancer modulated by a promoter-enhancer interaction. Am J Hum Genet. 2019;105(1): 29-47.

35

Ardeshna KM, Pizzey AR, Devereux S, Khwaja A. The PI3 kinase, p38 SAP kinase, and NF-kappaB signal transduction pathways are involved in the survival and maturation of lipopolysaccharide-stimulated human monocyte-derived dendritic cells. Blood. 2000;96(3): 1039-1046.

36

Avni D, Ernst O, Philosoph A, Zor T. Role of CREB in modulation of TNFalpha and IL-10 expression in LPS-stimulated RAW264.7 macrophages. Mol Immunol. 2010;47(7–8): 1396-1403.

37

Penix LA, Sweetser MT, Weaver WM, Hoeffler JP, Kerppola TK, Wilson CB. The proximal regulatory element of the interferon-gamma promoter mediates selective expression in T cells. J Biol Chem. 1996;271(50): 31964-31972.

38

Hai T, Curran T. Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proc Natl Acad Sci U S A. 1991;88(9): 3720-3724.

39

Yu T, Li YJ, Bian AH, et al. The regulatory role of activating transcription factor 2 in inflammation. Mediat Inflamm. 2014;2014: e950472.

40

Watson G, Ronai ZA, Lau E. ATF2, a paradigm of the multifaceted regulation of transcription factors in biology and disease. Pharmacol Res. 2017;119: 347-357.

41

Brinckerhoff CE, Matrisian LM. Matrix metalloproteinases: a tail of a frog that became a prince. Nat Rev Mol Cell Biol. 2002;3(3): 207-214.

42

Parks WC, Wilson CL, Lopez-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol. 2004;4(8): 617-629.

43

Kitanaka N, Nakano R, Sakai M, et al. ERK1/ATF-2 signaling axis contributes to interleukin-1beta-induced MMP-3 expression in dermal fibroblasts. PloS One. 2019;14(9): e0222869.

44

Chacon-Solano E, Leon C, Diaz F, et al. Fibroblast activation and abnormal extracellular matrix remodelling as common hallmarks in three cancer-prone genodermatoses. Br J Dermatol. 2019;181(3): 512-522.

45

Shen Y, Park CS, Suppipat K, et al. Inactivation of KLF4 promotes T-cell acute lymphoblastic leukemia and activates the MAP2K7 pathway. Leukemia. 2017;31(6): 1314-1324.

52

Li N, Guo X, Liu L, Wang L, Cheng R. Molecular mechanism of miR-204 regulates proliferation, apoptosis and autophagy of cervical cancer cells by targeting ATF2. Artif Cells Nanomed Biotechnol. 2019;47(1): 2529-2535.

46

Lau E, Feng Y, Claps G, et al. The transcription factor ATF2 promotes melanoma metastasis by suppressing protein fucosylation. Sci Signal. 2015;8(406): ra124.

47

Wu DS, Chen C, Wu ZJ, et al. ATF2 predicts poor prognosis and promotes malignant phenotypes in renal cell carcinoma. J Exp Clin Cancer Res. 2016;35(1): 108.

48

Bhoumik A, Fichtman B, Derossi C, et al. Suppressor role of activating transcription factor 2 (ATF2) in skin cancer. Proc Natl Acad Sci U S A. 2008;105(5): 1674-1679.

49

Gozdecka M, Lyons S, Kondo S, et al. JNK suppresses tumor formation via a gene-expression program mediated by ATF2. Cell Rep. 2014;9(4): 1361-1374.

50

Bhoumik A, Jones N, Ronai Ze. Transcriptional switch by activating transcription factor 2-derived peptide sensitizes melanoma cells to apoptosis and inhibits their tumorigenicity. Proc Natl Acad Sci U S A. 2004;101(12): 4222-4227.

51

Varsano T, Lau E, Feng Y, et al. Inhibition of melanoma growth by small molecules that promote the mitochondrial localization of ATF2. Clin Cancer Res. 2013;19(10): 2710-2722.

53

Song S, Fajol A, Tu X, Ren B, Shi S. miR-204 suppresses the development and progression of human glioblastoma by targeting ATF2. Oncotarget. 2016;7(43): 70058-70065.

54

Segura E, Touzot M, Bohineust A, et al. Human inflammatory dendritic cells induce Th17 cell differentiation. Immunity. 2013;38(2): 336-348.

55

Segura E, Amigorena S. Inflammatory dendritic cells in mice and humans. Trends Immunol. 2013;34(9): 440-445.

56

Goldszmid RS, Caspar P, Rivollier A, et al. NK cell-derived interferon-gamma orchestrates cellular dynamics and the differentiation of monocytes into dendritic cells at the site of infection. Immunity. 2012;36(6): 1047-1059.

57

Walsh KP, Mills KH. Dendritic cells and other innate determinants of T helper cell polarisation. Trends Immunol. 2013;34(11): 521-530.

58

Mahiddine K, Mallavialle A, Bziouech H, Larbret F, Bernard A, Bernard G. CD99 isoforms regulate CD1a expression in human monocyte-derived DCs through ATF-2/CREB-1 phosphorylation. Eur J Immunol. 2016;46(6): 1460-1471.

59

Colmone A, Li S, Wang CR. Activating transcription factor/cAMP response element binding protein family member regulated transcription of CD1A. J Immunol. 2006;177(10): 7024-7032.

60

Johannessen M, Delghandi MP, Moens U. What turns CREB on? Cell Signal. 2004;16(11): 1211-1227.

61

Han J, Guo X, Tan W, et al. The expression of p-ATF2 involved in the chondeocytes apoptosis of an endemic osteoarthritis, Kashin-Beck disease. BMC Muscoskel Disord. 2013;14: 209.

62

Li X, Udagawa N, Itoh K, et al. p38 MAPK-mediated signals are required for inducing osteoclast differentiation but not for osteoclast function. Endocrinology. 2002;143(8): 3105-3113.

63

Miyata Y, Fukuhara A, Otsuki M, Shimomura I. Expression of activating transcription factor 2 in inflammatory macrophages in obese adipose tissue. Obesity. 2013;21(4): 731-736.

64

Akiyama Y, Ogawa F, Iwata Y, et al. Autoantibody against activating transcription factor-2 in patients with systemic sclerosis. Clin Exp Rheumatol. 2009;27(5): 751-757.

65

Shen T, Yang WS, Yi YS, et al. AP-1/IRF-3 targeted anti-inflammatory activity of andrographolide isolated from andrographis paniculata. Evid Based Complement Alternat Med. 2013;2013: e210736.

66

Pearson AG, Curtis MA, Waldvogel HJ, Faull RL, Dragunow M. Activating transcription factor 2 expression in the adult human brain: association with both neurodegeneration and neurogenesis. Neuroscience. 2005;133(2): 437-451.

67

Le NH, van der Wal A, van der Bent P, et al. Increased activity of activator protein-1 transcription factor components ATF2, c-Jun, and c-Fos in human and mouse autosomal dominant polycystic kidney disease. J Am Soc Nephrol. 2005;16(9): 2724-2731.

68

Zhang S, Liu H, Liu J, Tse CA, Dragunow M, Cooper GJ. Activation of activating transcription factor 2 by p38 MAP kinase during apoptosis induced by human amylin in cultured pancreatic beta-cells. FEBS J. 2006;273(16): 3779-3791.

69

Meijer BJ, Giugliano FP, Baan B, et al. ATF2 and ATF7 are critical mediators of intestinal epithelial repair. Cell Mol Gastroenterol Hepatol. 2020;10(1): 23-42.

70

Hai TW, Liu F, Coukos WJ, Green MR. Transcription factor ATF cDNA clones: an extensive family of leucine zipper proteins able to selectively form DNA-binding heterodimers. Genes Dev. 1989;3(12b): 2083-2090.

71

Hunt D, Raivich G, Anderson PN. Activating transcription factor 3 and the nervous system. Front Mol Neurosci. 2012;5: 7.

72

Hashimoto Y, Zhang C, Kawauchi J, et al. An alternatively spliced isoform of transcriptional repressor ATF3 and its induction by stress stimuli. Nucleic Acids Res. 2002;30(11): 2398-2406.

73

Rohini M, Haritha Menon A, Selvamurugan N. Role of activating transcription factor 3 and its interacting proteins under physiological and pathological conditions. Int J Biol Macromol. 2018;120(Pt A): 310-317.

74

Cai Y, Zhang C, Nawa T, et al. Homocysteine-responsive ATF3 gene expression in human vascular endothelial cells: activation of c-Jun NH(2)-terminal kinase and promoter response element. Blood. 2000;96(6): 2140-2148.

75

Hamdi M, Popeijus HE, Carlotti F, et al. ATF3 and Fra1 have opposite functions in JNK- and ERK-dependent DNA damage responses. DNA Repair. 2008;7(3): 487-496.

76

Inoue K, Zama T, Kamimoto T, et al. TNFalpha-induced ATF3 expression is bidirectionally regulated by the JNK and ERK pathways in vascular endothelial cells. Gene Cell. 2004;9(1): 59-70.

77

Liu J, Edagawa M, Goshima H, et al. Role of ATF3 in synergistic cancer cell killing by a combination of HDAC inhibitors and agonistic anti-DR5 antibody through ER stress in human colon cancer cells. Biochem Biophys Res Commun. 2014;445(2): 320-326.

78

Wu X, Nguyen BC, Dziunycz P, et al. Opposing roles for calcineurin and ATF3 in squamous skin cancer. Nature. 2010;465(7296): 368-372.

79

Tamura K, Hua B, Adachi S, et al. Stress response gene ATF3 is a target of c-myc in serum-induced cell proliferation. EMBO J. 2005;24(14): 2590-2601.

80

Mathiasen DP, Egebjerg C, Andersen SH, et al. Identification of a c-Jun N-terminal kinase-2-dependent signal amplification cascade that regulates c-Myc levels in ras transformation. Oncogene. 2012;31(3): 390-401.

81

Kang Y, Chen CR, Massagué J. A self-enabling TGFbeta response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol Cell. 2003;11(4): 915-926.

82

Inoue M, Uchida Y, Edagawa M, et al. The stress response gene ATF3 is a direct target of the Wnt/beta-catenin pathway and inhibits the invasion and migration of HCT116 human colorectal cancer cells. PloS One. 2018;13(7): e0194160.

83

Avraham S, Korin B, Aviram S, Shechter D, Shaked Y, Aronheim A. ATF3 and JDP2 deficiency in cancer associated fibroblasts promotes tumor growth via SDF-1 transcription. Oncogene. 2019;38(20): 3812-3823.

84

Wang Z, Xu D, Ding HF, et al. Loss of ATF3 promotes Akt activation and prostate cancer development in a Pten knockout mouse model. Oncogene. 2015;34(38): 4975-4984.

85

Zeng Z, Xu FY, Zheng H, et al. LncRNA-MTA2TR functions as a promoter in pancreatic cancer via driving deacetylation-dependent accumulation of HIF-1alpha. Theranostics. 2019;9(18): 5298-5314.

86

Hao ZF, Ao JH, Zhang J, Su YM, Yang RY. ATF3 activates Stat3 phosphorylation through inhibition of p53 expression in skin cancer cells. Asian Pac J Cancer Prev. 2013;14(12): 7439-7444.

87

Kwok S, Rittling SR, Partridge NC, et al. Transforming growth factor-beta1 regulation of ATF-3 and identification of ATF-3 target genes in breast cancer cells. J Cell Biochem. 2009;108(2): 408-414.

88

Song X, Lu F, Liu RY, et al. Association between the ATF3 gene and non-small cell lung cancer. Thorac Cancer. 2012;3(3): 217-223.

89

Wu ZY, Wei ZM, Sun SJ, Yuan J, Jiao SC. Activating transcription factor 3 promotes colon cancer metastasis. Tumour Biol. 2014;35(8): 8329-8334.

90

Wang A, Arantes S, Yan L, et al. The transcription factor ATF3 acts as an oncogene in mouse mammary tumorigenesis. BMC Cancer. 2008;8: 268.

91

Zhao W, Sun M, Li S, Chen Z, Geng D. Transcription factor ATF3 mediates the radioresistance of breast cancer. J Cell Mol Med. 2018;22(10): 4664-4675.

92

Yin X, Wolford CC, Chang YS, et al. ATF3, an adaptive-response gene, enhances TGF{beta} signaling and cancer-initiating cell features in breast cancer cells. J Cell Sci. 2010;123(Pt 20): 3558-3565.

93

Cao Y, Yang Q, Deng H, et al. Transcriptional factor ATF3 protects against colitis by regulating follicular helper T cells in Peyer's patches. Proc Natl Acad Sci U S A. 2019;116(13): 6286-6291.

94

Hodi FS, O'Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363(8): 711-723.

95

Brahmer JR, Tykodi SS, Chow LQM, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med. 2012;366(26): 2455-2465.

96

Whitmore MM, Iparraguirre A, Kubelka L, Weninger W, Hai T, Williams BRG. Negative regulation of TLR-signaling pathways by activating transcription factor-3. J Immunol. 2007;179(6): 3622-3630.

97

Gilchrist M, Thorsson V, Li B, et al. Systems biology approaches identify ATF3 as a negative regulator of Toll-like receptor 4. Nature. 2006;441(7090): 173-178.

98

Boespflug ND, Kumar S, McAlees JW, et al. ATF3 is a novel regulator of mouse neutrophil migration. Blood. 2014;123(13): 2084-2093.

99

Khuu CH, Barrozo RM, Hai T, Weinstein SL. Activating transcription factor 3 (ATF3) represses the expression of CCL4 in murine macrophages. Mol Immunol. 2007;44(7): 1598-1605.

100

Liu H, Kuang X, Zhang Y, et al. ADORA1 inhibition promotes tumor immune evasion by regulating the ATF3-PD-L1 Axis. Cancer Cell. 2020;37(3): 324-339.

101

Labzin LI, Schmidt SV, Masters SL, et al. ATF3 is a key regulator of macrophage IFN responses. J Immunol. 2015;195(9): 4446-4455.

102

Sha H, Zhang D, Zhang Y, Wen Y, Wang Y. ATF3 promotes migration and M1/M2 polarization of macrophages by activating tenascin-C via Wnt/β-catenin pathway. Mol Med Rep. 2017;16(3): 3641-3647.

103

Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science. 2011;334(6059): 1081-1086.

104

Tameire F, II Verginadis, Leli NM, et al. ATF4 couples MYC-dependent translational activity to bioenergetic demands during tumour progression. Nat Cell Biol. 2019;21(7): 889-899.

105

Ye J, Kumanova M, Hart LS, et al. The GCN2-ATF4 pathway is critical for tumour cell survival and proliferation in response to nutrient deprivation. EMBO J. 2010;29(12): 2082-2096.

106

Mu N, Lei Y, Wang Y, et al. Inhibition of SIRT1/2 upregulates HSPA5 acetylation and induces pro-survival autophagy via ATF4-DDIT4-mTORC1 axis in human lung cancer cells. Apoptosis. 2019;24(9–10): 798-811.

107

Jain S, Chakraborty G, Raja R, Kale S, Kundu GC. Prostaglandin E2 regulates tumor angiogenesis in prostate cancer. Cancer Res. 2008;68(19): 7750-7759.

108

Igarashi T, Izumi H, Uchiumi T, et al. Clock and ATF4 transcription system regulates drug resistance in human cancer cell lines. Oncogene. 2007;26(33): 4749-4760.

109

Guan X, Chen S, Liu Y, Wang LL, Zhao Y, Zong ZH. PUM1 promotes ovarian cancer proliferation, migration and invasion. Biochem Biophys Res Commun. 2018;497(1): 313-318.

110

Xia LH, Yan QH, Sun QD, Gao YP. MiR-411-5p acts as a tumor suppressor in non-small cell lung cancer through targeting PUM1. Eur Rev Med Pharmacol Sci. 2018;22(17): 5546-5553.

111

Dai H, Shen K, Yang Y, et al. PUM1 knockdown prevents tumor progression by activating the PERK/eIF2/ATF4 signaling pathway in pancreatic adenocarcinoma cells. Cell Death Dis. 2019;10(8): 595.

112

Luo J, Xia Y, Yin Y, et al. ATF4 destabilizes RET through nonclassical GRP78 inhibition to enhance chemosensitivity to bortezomib in human osteosarcoma. Theranostics. 2019;9(21): 6334-6353.

113

Liu J, Qi YB. Activation of LXRbeta inhibits proliferation, promotes apoptosis, and increases chemosensitivity of gastric cancer cells by upregulating the expression of ATF4. J Cell Biochem. 2019;120(9): 14336-14347.

114

Abdel-Nour M, Carneiro LAM, Downey J, et al. The heme-regulated inhibitor is a cytosolic sensor of protein misfolding that controls innate immune signaling. Science. 2019;365(6448): eaaw4144.

115

Srivastava RK, Li C, Wang Y, et al. Activating transcription factor 4 underlies the pathogenesis of arsenic trioxide-mediated impairment of macrophage innate immune functions. Toxicol Appl Pharmacol. 2016;308: 46-58.

116

Liu B, Chen P, Xi D, Zhu H, Gao Y. ATF4 regulates CCL2 expression to promote endometrial cancer growth by controlling macrophage infiltration. Exp Cell Res. 2017;360(2): 105-112.

117

Yang X, Xia R, Yue C, et al. ATF4 regulates CD4+ T cell immune responses through metabolic reprogramming. Cell Rep. 2018;23(6): 1754-1766.

118

Zhang C, Bai N, Chang A, et al. ATF4 is directly recruited by TLR4 signaling and positively regulates TLR4-trigged cytokine production in human monocytes. Cell Mol Immunol. 2013;10(1): 84-94.

119

Baxevanis AD, Vinson CR. Interactions of coiled coils in transcription factors: where is the specificity? Curr Opin Genet Dev. 1993;3(2): 278-285.

120

Ellenberger TE, Brandl CJ, Struhl K, Harrison SC. The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted alpha helices: crystal structure of the protein-DNA complex. Cell. 1992;71(7): 1223-1237.

121

Vinson C, Myakishev M, Acharya A, Mir AA, Moll JR, Bonovich M. Classification of human B-ZIP proteins based on dimerization properties. Mol Cell Biol. 2002;22(18): 6321-6335.

122

Newman JR, Keating AE. Comprehensive identification of human bZIP interactions with coiled-coil arrays. Science. 2003;300(5628): 2097-2101.

123

Al Sarraj J, Vinson C, Thiel G. Regulation of asparagine synthetase gene transcription by the basic region leucine zipper transcription factors ATF5 and CHOP. Biol Chem. 2005;386(9): 873-879.

124

Greene LA, Lee HY, Angelastro JM. The transcription factor ATF5: role in neurodevelopment and neural tumors. J Neurochem. 2009;108(1): 11-22.

125

Ishihara S, Yasuda M, Ishizu A, Ishikawa M, Shirato H, Haga H. Activating transcription factor 5 enhances radioresistance and malignancy in cancer cells. Oncotarget. 2015;6(7): 4602-4614.

126

Kong X, Meng W, Zhou Z, et al. Overexpression of activating transcription factor 5 in human rectal cancer. Exp Ther Med. 2011;2(5): 827-831.

127

Hua XM, Wang J, Qian DM, et al. DNA methylation level of promoter region of activating transcription factor 5 in glioma. J Zhejiang Univ - Sci B. 2015;16(9): 757-762.

128

Karpel-Massler G, Horst BA, Shu C, et al. A synthetic cell-penetrating dominant-negative ATF5 peptide exerts anticancer activity against a broad spectrum of treatment-resistant cancers. Clin Cancer Res. 2016;22(18): 4698-4711.

129

Monaco SE, Angelastro JM, Szabolcs M, Greene LA. The transcription factor ATF5 is widely expressed in carcinomas, and interference with its function selectively kills neoplastic, but not nontransformed, breast cell lines. Int J Canc. 2007;120(9): 1883-1890.

130

Chen A, Qian D, Wang B, et al. ATF5 is overexpressed in epithelial ovarian carcinomas and interference with its function increases apoptosis through the downregulation of Bcl-2 in SKOV-3 cells. Int J Gynecol Pathol. 2012;31(6): 532-537.

131

Shuai Y, Fan E, Zhong Q, et al. ATF5 involved in radioresistance in nasopharyngeal carcinoma by promoting epithelial-to-mesenchymal phenotype transition. Eur Arch Oto-Rhino-Laryngol. 2020;277(10): 2869-2879.

132

Sheng Z, Li L, Zhu LJ, et al. A genome-wide RNA interference screen reveals an essential CREB3L2-ATF5-MCL1 survival pathway in malignant glioma with therapeutic implications. Nat Med. 2010;16(6): 671-677.

133

Dluzen D, Li G, Tacelosky D, Moreau M, Liu DX. BCL-2 is a downstream target of ATF5 that mediates the prosurvival function of ATF5 in a cell type-dependent manner. J Biol Chem. 2011;286(9): 7705-7713.

134

Fiorese CJ, Schulz AM, Lin YF, Rosin N, Pellegrino MW, Haynes CM. The transcription factor ATF5 mediates a mammalian mitochondrial UPR. Curr Biol. 2016;26(15): 2037-2043.

135

Li G, Li W, Angelastro JM, Greene LA, Liu DX. Identification of a novel DNA binding site and a transcriptional target for activating transcription factor 5 in c6 glioma and mcf-7 breast cancer cells. Mol Cancer Res. 2009;7(6): 933-943.

1366

Laeger T, Henagan TM, Albarado DC, et al. FGF21 is an endocrine signal of protein restriction. J Clin Invest. 2014;124(9): 3913-3922.

137

Ishihara S, Haga H. ATF5: development of oncogenic resistance to radiotherapy. Aging (Albany NY). 2015;7(7): 453-454.

138

Nukuda A, Endoh H, Yasuda M, Mizutani T, Kawabata K, Haga H. Role of ATF5 in the invasive potential of diverse human cancer cell lines. Biochem Biophys Res Commun. 2016;474(3): 509-514.

139

Gho JW, Ip WK, Chan KY, Law PT, Lai PB, Wong N. Re-expression of transcription factor ATF5 in hepatocellular carcinoma induces G2-M arrest. Cancer Res. 2008;68(16): 6743-6751.

140

Feldheim J, Kessler AF, Schmitt D, et al. Expression of activating transcription factor 5 (ATF5) is increased in astrocytomas of different WHO grades and correlates with survival of glioblastoma patients. OncoTargets Ther. 2018;11: 8673-8684.

141

Angelastro JM, Canoll PD, Kuo J, et al. Selective destruction of glioblastoma cells by interference with the activity or expression of ATF5. Oncogene. 2006;25(6): 907-916.

142

Cates CC, Arias AD, Nakayama Wong LS, et al. Regression/eradication of gliomas in mice by a systemically-deliverable ATF5 dominant-negative peptide. Oncotarget. 2016;7(11): 12718-12730.

143

Moll JR, Olive M, Vinson C. Attractive interhelical electrostatic interactions in the proline- and acidic-rich region (PAR) leucine zipper subfamily preclude heterodimerization with other basic leucine zipper subfamilies. J Biol Chem. 2000;275(44): 34826-34832.

144

Sun X, Jefferson P, Zhou Q, Angelastro JM, Greene LA. Dominant-negative ATF5 compromises cancer cell survival by targeting CEBPB and CEBPD. Mol Cancer Res. 2020;18(2): 216-228.

145

Hu M, Wang B, Qian D, et al. Interference with ATF5 function enhances the sensitivity of human pancreatic cancer cells to paclitaxel-induced apoptosis. Anticancer Res. 2012;32(10): 4385-4394.

146

Thuerauf DJ, Marcinko M, Belmont PJ, Glembotski CC. Effects of the isoform-specific characteristics of ATF6 alpha and ATF6 beta on endoplasmic reticulum stress response gene expression and cell viability. J Biol Chem. 2007;282(31): 22865-22878.

147

Namba T. Regulation of endoplasmic reticulum functions. Aging. 2015;7(11): 901-902.

148

Luo B, Lee AS. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene. 2013;32(7): 805-818.

149

Szegezdi E, Logue SE, Gorman AM, Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 2006;7(9): 880-885.

150

Sosa MS, Bragado P, Debnath J, Aguirre-Ghiso JA. Regulation of tumor cell dormancy by tissue microenvironments and autophagy. Adv Exp Med Biol. 2013;734: 73-89.

151

Schewe DM, Aguirre-Ghiso JA. ATF6alpha-Rheb-mTOR signaling promotes survival of dormant tumor cells in vivo. Proc Natl Acad Sci U S A. 2008;105(30): 10519-10524.

152

Hanaoka M, Ishikawa T, Ishiguro M, et al. Expression of ATF6 as a marker of pre-cancerous atypical change in ulcerative colitis-associated colorectal cancer: a potential role in the management of dysplasia. J Gastroenterol. 2018;53(5): 631-641.

153

Liu CY, Hung MH, Wang DS, et al. Tamoxifen induces apoptosis through cancerous inhibitor of protein phosphatase 2A-dependent phospho-Akt inactivation in estrogen receptor-negative human breast cancer cells. Breast Cancer Res. 2014;16(5): 431.

154

Teng HW, Yang SH, Lin JK, et al. CIP2A is a predictor of poor prognosis in colon cancer. J Gastrointest Surg. 2012;16(5): 1037-1047.

155

Liu CY, Hsu CC, Huang TT, et al. ER stress-related ATF6 upregulates CIP2A and contributes to poor prognosis of colon cancer. Mol Oncol. 2018;12(10): 1706-1717.

156

Romero-Ramirez L, Cao H, Nelson D, et al. XBP1 is essential for survival under hypoxic conditions and is required for tumor growth. Cancer Res. 2004;64(17): 5943-5947.

157

Coleman OI, Lobner EM, Bierwirth S, et al. Activated ATF6 induces intestinal dysbiosis and innate immune response to promote colorectal tumorigenesis. Gastroenterology. 2018;155(5): 1539-1552.

158

Walczynski J, Lyons S, Jones N, Breitwieser W. Sensitisation of c-MYC-induced B-lymphoma cells to apoptosis by ATF2. Oncogene. 2014;33(8): 1027-1036.

159

Guo H-Q, Ye S, Huang G-L, Liu L, Liu O-F, Yang S-J. Expression of activating transcription factor 7 is correlated with prognosis of colorectal cancer. J Cancer Res Therapeut. 2015;11(2): 319-323.

160

Hu X, Miao J, Zhang M, et al. miRNA-103a-3p promotes human gastric cancer cell proliferation by targeting and suppressing ATF7 in vitro. Mol Cell. 2018;41(5): 390-400.

161

Song F, Wei M, Wang J, et al. Hepatitis B virus-regulated growth of liver cancer cells occurs through the microRNA-340-5p-activating transcription factor 7-heat shock protein A member 1B axis. Cancer Sci. . 2019;110(5): 1633-1643.

162

Shivers RP, Pagano DJ, Kooistra T, et al. Phosphorylation of the conserved transcription factor ATF-7 by PMK-1 p38 MAPK regulates innate immunity in Caenorhabditis elegans. PLoS Genet. 2010;6(4): e1000892.

163

Vandewynckel Y-P, Laukens D, Geerts A, et al. The paradox of the unfolded protein response in cancer. Anticancer Res. 2013;33(11): 4683-4694.

164

Vesely PW, Staber PB, Hoefler G, Kenner L. Translational regulation mechanisms of AP-1 proteins. Mutat Res. 2009;682(1): 7-12.

Genes & Diseases
Pages 981-999
Cite this article:
Chen M, Liu Y, Yang Y, et al. Emerging roles of activating transcription factor (ATF) family members in tumourigenesis and immunity: Implications in cancer immunotherapy. Genes & Diseases, 2022, 9(4): 981-999. https://doi.org/10.1016/j.gendis.2021.04.008

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Received: 17 October 2020
Revised: 20 April 2021
Accepted: 26 April 2021
Published: 03 June 2021
© 2021, Chongqing Medical University.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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