Research progress on the role of Ndfip1 (Nedd4 family interacting protein 1) in immune cells
Main Article Content
Keywords
CD4 T cells, cell differentiation, cell proliferation, immune regulation, Ndfip1
Abstract
Nedd4 family interacting protein 1 (Ndfip1) was first mentioned in an article in 2000. Since its discovery, related studies have shown that this protein is associated with apoptosis, neuroprotection, substance transport, ubiquitination, and immune regulation. It is noteworthy that the lack of Ndfip1 can lead to death in fetal mice. Researchers generally believe that the function of Ndfip1 is closely related to individual immune capacity and have published a large number of articles. However, a comprehensive classification of the immune regulatory function of Ndfip1 is still lacking. In this review, we will overview and discuss this new perspective, focusing on the role of Ndfip1 in the proliferation, differentiation, and cell activity of CD4+ T cells, CD8+ T cells, mast cells, and eosinophils. This review provides an updated summary of Ndfip1, which will unveil novel therapeutic targets. Finally, the conclusion is that Ndfip1 mainly plays a negative regulatory role in immune cells by maintaining the stability of the immune response and limiting its overexpression.
References
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45. Routila J, Leivo I, Minn H, Westermarck J, Ventelä S. Evaluation of prognostic biomarkers in a population-validated Finnish HNSCC patient cohort. Eur Arch Otorhinolaryngol. 2021;278(11):4575–85. 10.1007/s00405-021-06650-7
46. Besse A, Sana J, Lakomy R, Kren L, Fadrus P, Smrcka M, et al. MiR-338-5p sensitizes glioblastoma cells to radiation through regulation of genes involved in DNA damage response. Tumour Biol. 2016;37(6):7719–27. 10.1007/s13277-015-4654-x
47. Tian Z, He W, Tang J, Liao X, Yang Q, Wu Y, et al. Identification of important modules and biomarkers in breast cancer based on WGCNA. Onco Targets Ther. 2020;13:6805–17. 10.2147/OTT.S258439
2. Lackovic J, Howitt J, Callaway JK, Silke J, Bartlett P, Tan SS. Differential regulation of Nedd4 ubiquitin ligases and their adaptor protein Ndfip1 in a rat model of ischemic stroke. Exp Neurol. 2012;235(1):326–35. 10.1016/j.expneurol.2012.02.014
3. Howitt J, Gysbers AM, Ayton S, Carew-Jones F, Putz U, Finkelstein DI, et al. Increased Ndfip1 in the substantia nigra of Parkinsonian brains is associated with elevated iron levels. PLoS One. 2014;9(1):e87119. 10.1371/journal.pone.0087119
4. Sang Q, Kim MH, Kumar S, Bye N, Morganti-Kossman MC, Gunnersen J, et al. Nedd4-WW domain-binding protein 5 (Ndfip1) is associated with neuronal survival after acute cortical brain injury. J Neurosci. 2006;26(27):7234–44. 10.1523/JNEUROSCI.1398-06.2006
5. Howitt J, Putz U, Lackovic J, Doan A, Dorstyn L, Cheng H, et al. Divalent metal transporter 1 (DMT1) regulation by Ndfip1 prevents metal toxicity in human neurons. Proc Natl Acad Sci U S A. 2009;106(36):15489–94. 10.1073/pnas.0904880106
6. Foot NJ, Leong YA, Dorstyn LE, Dalton HE, Ho K, Zhao L, et al. Ndfip1-deficient mice have impaired DMT1 regulation and iron homeostasis. Blood. 2011;117(2):638–46. 10.1182/blood-2010-07-295287
7. Xu H, Chang Q, Jia W, Jiang H, Sun P, Xie J. Iron status and lipopolysaccharide regulate Ndfip1 by activation of nuclear factor-kappa B. Biometals. 2013;26(6):981–8. 10.1007/s10534-013-9674-7
8. Traeger L, Wiegand SB, Sauer AJ, Corman BHP, Peneyra KM, Wunderer F, et al. UBA6 and NDFIP1 regulate the degradation of ferroportin. Haematologica. 2022;107(2):478–88. 10.3324/haematol.2021.278530
9. Garrick MD, Zhao L, Roth JA, Jiang H, Feng J, Foot NJ, et al. Isoform specific regulation of divalent metal (ion) transporter (DMT1) by proteasomal degradation. Biometals. 2012;25(4):787–93. 10.1007/s10534-012-9522-1
10. Oliver PM, Cao X, Worthen GS, Shi P, Briones N, MacLeod M, et al. Ndfip1 protein promotes the function of itch ubiquitin ligase to prevent T cell activation and T helper 2 cell-mediated inflammation. Immunity. 2006;25(6):929–40. 10.1016/j.immuni.2006.10.012
11. Ramon HE, Riling CR, Bradfield J, Yang B, Hakonarson H, Oliver PM. The ubiquitin ligase adaptor Ndfip1 regulates T cell-mediated gastrointestinal inflammation and inflammatory bowel disease susceptibility. Mucosal Immunol. 2011;4(3):314–24. 10.1038/mi.2010.69
12. Kurzweil V, Tarangelo A, Oliver PM. Gastrointestinal microbiota do not significantly contribute to T cell activation or GI inflammation in Ndfip1-cKO mice. PLoS One. 2012;7(4):e34478. 10.1371/journal.pone.0034478
13. Ramos-Hernández N, Ramon HE, Beal AM, Laroche A, Dekleva EA, Oliver PM. Ndfip1 enforces a requirement for CD28 costimulation by limiting IL-2 production. J Immunol. 2013;191(4):1536–46. 10.4049/jimmunol.1203571
14. Altin JA, Daley SR, Howitt J, Rickards HJ, Batkin AK, Horikawa K, et al. Ndfip1 mediates peripheral tolerance to self and exogenous antigen by inducing cell cycle exit in responding CD4+ T cells. Proc Natl Acad Sci U S A. 2014;111(6):2067–74. 10.1073/pnas.1322739111
15. O’Leary CE, Riling CR, Spruce LA, Ding H, Kumar S, Deng G, et al. Ndfip-mediated degradation of Jak1 tunes cytokine signalling to limit expansion of CD4+ effector T cells. Nat Commun. 2016;7:11226. 10.1038/ncomms11226
16. Del Prete G. Human Th1 and Th2 lymphocytes: Their role in the pathophysiology of atopy. Allergy. 1992;47(5):450–5. 10.1111/j.1398-9995.1992.tb00662.x
17. Romagnani S, Maggi E, Parronchi P, Macchia D, Piccinni MP, Ricci M. Increased numbers of Th2-like CD4+ T cells in target organs and in the allergen-specific repertoire of allergic patients. Possible role of IL-4 produced by non-T cells. Int Arch Allergy Appl Immunol. 1991;94(1–4):133–6. 10.1159/000235344
18. Gao M, Labuda T, Xia Y, Gallagher E, Fang D, Liu YC, et al. Jun turnover is controlled through JNK-dependent phosphorylation of the E3 ligase Itch. Science. 2004;306(5694):271–5. 10.1126/science.1099414
19. Fang D, Elly C, Gao B, Fang N, Altman Y, Joazeiro C, et al. Dysregulation of T lymphocyte function in itchy mice: A role for Itch in TH2 differentiation. Nat Immunol. 2002;3(3):281–7. 10.1038/ni763
20. Hartenstein B, Teurich S, Hess J, Schenkel J, Schorpp-Kistner M, Angel P. Th2 cell-specific cytokine expression and allergen-induced airway inflammation depend on JunB. EMBO J. 2002;21(23):6321–9. 10.1093/emboj/cdf648
21. Li B, Tournier C, Davis RJ, Flavell RA. Regulation of IL-4 expression by the transcription factor JunB during T helper cell differentiation. EMBO J. 1999;18(2):420–32. 10.1093/emboj/18.2.420
22. Perry WL, Hustad CM, Swing DA, O’Sullivan TN, Jenkins NA, Copeland NG. The itchy locus encodes a novel ubiquitin protein ligase that is disrupted in a18H mice. Nat Genet. 1998;18(2):143–6. 10.1038/ng0298-143
23. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 Cells. Annu Rev Immunol. 2009;27:485–517. 10.1146/annurev.immunol.021908.132710
24. Louten J, Boniface K, de Waal Malefyt R. Development and function of TH17 cells in health and disease. J Allergy Clin Immunol. 2009;123(5):1004–11. 10.1016/j.jaci.2009.04.003
25. Ramon HE, Beal AM, Liu Y, Worthen GS, Oliver PM. The E3 ubiquitin ligase adaptor Ndfip1 regulates Th17 differentiation by limiting the production of proinflammatory cytokines. J Immunol. 2012;188(8):4023–31. 10.4049/jimmunol.1102779
26. Yang XO, Panopoulos AD, Nurieva R, Chang SH, Wang D, Watowich SS, et al. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J Biol Chem. 2007;282(13):9358–63. 10.1074/jbc.C600321200
27. Layman AAK, Sprout SL, Phillips D, Oliver PM. Ndfip1 restricts Th17 cell potency by limiting lineage stability and proinflammatory cytokine production. Sci Rep. 2017;7:39649. 10.1038/srep39649
28. Beal AM, Ramos-Hernández N, Riling CR, Nowelsky EA, Oliver PM. TGF-β induces the expression of the adaptor Ndfip1 to silence IL-4 production during iTreg cell differentiation. Nat Immunol. 2011;13(1):77–85. 10.1038/ni.2154
29. Newton R, Priyadharshini B, Turka LA. Immunometabolism of regulatory T cells. Nat Immunol. 2016;17(6):618–25. 10.1038/ni.3466
30. Apostolidis SA, Rodríguez-Rodríguez N, Suárez-Fueyo A, Dioufa N, Ozcan E, Crispín JC, et al. Phosphatase PP2A is requisite for the function of regulatory T cells. Nat Immunol. 2016;17(5):556–64. 10.1038/ni.3390
31. Wei J, Long L, Yang K, Guy C, Shrestha S, Chen Z, et al. Autophagy enforces functional integrity of regulatory T cells by coupling environmental cues and metabolic homeostasis. Nat Immunol. 2016;17(3):277–85. 10.1038/ni.3365
32. Zeng H, Cohen S, Guy C, Shrestha S, Neale G, Brown SA, et al. mTORC1 and mTORC2 Kinase signaling and glucose metabolism drive follicular helper T cell differentiation. Immunity. 2016;45(3):540–54. 10.1016/j.immuni.2016.08.017
33. Layman AAK, Deng G, O’Leary CE, Tadros S, Thomas RM, Dybas JM, et al. Ndfip1 restricts mTORC1 signalling and glycolysis in regulatory T cells to prevent autoinflammatory disease. Nat Commun. 2017;8:15677. 10.1038/ncomms15677
34. Wagle MV, Marchingo JM, Howitt J, Tan SS, Goodnow CC, Parish IA. The ubiquitin ligase adaptor NDFIP1 selectively enforces a CD8+ T cell tolerance checkpoint to high-dose antigen. Cell Rep. 2018;24(3):577–84. 10.1016/j.celrep.2018.06.060
35. Hernandez J, Aung S, Redmond WL, Sherman LA. Phenotypic and functional analysis of CD8(+) T cells undergoing peripheral deletion in response to cross-presentation of self-antigen. J Exp Med. 2001;194(6):707–17. 10.1084/jem.194.6.707
36. Parish IA, Rao S, Smyth GK, Juelich T, Denyer GS, Davey GM, et al. The molecular signature of CD8+ T cells undergoing deletional tolerance. Blood. 2009;113(19):4575–85. 10.1182/blood-2008-10-185223
37. Yip KH, Kolesnikoff N, Hauschild N, Biggs L, Lopez AF, Galli SJ, et al. The Nedd4-2/Ndfip1 axis is a negative regulator of IgE-mediated mast cell activation. Nat Commun. 2016;7:13198. 10.1038/ncomms13198
38. Costello PS, Turner M, Walters AE, Cunningham CN, Bauer PH, Downward J, et al. Critical role for the tyrosine kinase Syk in signalling through the high affinity IgE receptor of mast cells. Oncogene. 1996;13(12):2595–605. PMid: 9000133
39. Zhang J, Chiang YJ, Hodes RJ, Siraganian RP. Inactivation of c-Cbl or Cbl-b differentially affects signaling from the high affinity IgE receptor. J Immunol. 2004;173(3):1811–18. 10.4049/jimmunol.173.3.1811
40. Gustin SE, Thien CB, Langdon WY. Cbl-b is a negative regulator of inflammatory cytokines produced by IgE-activated mast cells. J Immunol. 2006;177(9):5980–9. 10.4049/jimmunol.177.9.5980
41. Zhang Y, Zhang C, Zhao Q, Wei W, Dong Z, Shao L, et al. The miR-873/NDFIP1 axis promotes hepatocellular carcinoma growth and metastasis through the AKT/mTOR-mediated Warburg effect. Am J Cancer Res. 2019;9(5):927–44. PMid: 31218102.
42. Peng J, Liu H, Liu C. MiR-155 promotes uveal melanoma cell proliferation and invasion by regulating NDFIP1 expression. Technol Cancer Res Treat. 2017;16(6):1160–7. 10.1177/1533034617737923
43. Ben Q, Sun Y, Liu J, Wang W, Zou D, Yuan Y. Nicotine promotes tumor progression and epithelial-mesenchymal transition by regulating the miR-155-5p/NDFIP1 axis in pancreatic ductal adenocarcinoma. Pancreatology. 2020;20(4):698–708. 10.1016/j.pan.2020.04.004
44. Routila J, Suvila K, Grénman R, Leivo I, Westermarck J, Ventelä S. Cancer cell line microarray as a novel screening method for identification of radioresistance biomarkers in head and neck squamous cell carcinoma. BMC Cancer. 2021;21(1):868. 10.1186/s12885-021-08618-6
45. Routila J, Leivo I, Minn H, Westermarck J, Ventelä S. Evaluation of prognostic biomarkers in a population-validated Finnish HNSCC patient cohort. Eur Arch Otorhinolaryngol. 2021;278(11):4575–85. 10.1007/s00405-021-06650-7
46. Besse A, Sana J, Lakomy R, Kren L, Fadrus P, Smrcka M, et al. MiR-338-5p sensitizes glioblastoma cells to radiation through regulation of genes involved in DNA damage response. Tumour Biol. 2016;37(6):7719–27. 10.1007/s13277-015-4654-x
47. Tian Z, He W, Tang J, Liao X, Yang Q, Wu Y, et al. Identification of important modules and biomarkers in breast cancer based on WGCNA. Onco Targets Ther. 2020;13:6805–17. 10.2147/OTT.S258439
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