Role of Notch signaling in regulating innate immunity and inflammation in health and disease
Yingli Shang, Sinead Smith, Xiaoyu Hu
Role of Notch signaling in regulating innate immunity and inflammation in health and disease
The Notch signaling pathway is conserved from Drosophila to mammals and is critically involved in developmental processes. In the immune system, it has been established that Notch signaling regulates multiple steps of T and B cell development in both central and peripheral lymphoid organs. Relative to the well documented role of Notch signaling in lymphocyte development, less is known about its role in regulating myeloid lineage development and function, especially in the context of acute and chronic inflammation. In this review article, we will describe the evidence accumulated during the recent years to support a key regulatory role of the Notch pathway in innate immune and inflammatory responses and discuss the potential implications of such regulation for pathogenesis and therapy of inflammatory disorders.
inflammation / innate immunity / macrophages / Notch signaling / RBP-J
[1] |
Aguilera C, Hoya-Arias R, Haegeman G, Espinosa L, Bigas A (2004) Recruitment ofIkappaBalphato thehes1promoterisassociatedwith transcriptional repression. Proc Natl Acad SciUSA 101:16537–16542
|
[2] |
Amsen D, Blander JM, Lee GR, Tanigaki K, Honjo T
CrossRef
Google scholar
|
[3] |
Amsen D, Antov A, Jankovic D, Sher A, Radtke F
CrossRef
Google scholar
|
[4] |
Ando K, Kanazawa S, Tetsuka T, Ohta S, Jiang X
CrossRef
Google scholar
|
[5] |
Aoyama T, Takeshita K, Kikuchi R, Yamamoto K, Cheng XW
CrossRef
Google scholar
|
[6] |
Bai S, Kopan R, Zou W, Hilton MJ, Ong CT
CrossRef
Google scholar
|
[7] |
Bansal K, Narayana Y, Patil SA, Balaji KN (2009) M. bovis BCG induced expression of COX-2 involves nitric oxide-dependent and-independent signalingpathways. JLeukoc Biol 85:804–816
CrossRef
Google scholar
|
[8] |
Bigas A, Martin DI, Milner LA (1998) Notch1 and Notch2 inhibit myeloid differentiation in response to different cytokines. Mol Cell Biol 18:2324–2333
CrossRef
Google scholar
|
[9] |
Bigas A, Robert-Moreno A, Espinosa L(2010) The Notch pathwayin the developing hematopoietic system. IntJDev Biol 54:1175–1188
|
[10] |
Blanpain C, Lowry WE, Pasolli HA, Fuchs E(2006) Canonical notch signaling functions as a commitment switch in the epidermal lineage. Genes Dev 20:3022–3035
CrossRef
Google scholar
|
[11] |
Borggrefe T, Oswald F (2009) The Notch signaling pathway: transcriptional regulation at Notch target genes. Cell Mol Life Sci 66:1631–1646
CrossRef
Google scholar
|
[12] |
Bozkulak EC, Weinmaster G (2009) Selective use of ADAM10 and ADAM17 in activation ofNotch1 signaling. Mol Cell Biol 29:5679–5695
CrossRef
Google scholar
|
[13] |
Carlesso N, Aster JC, Sklar J, Scadden DT (1999) Notch1-induced delay of human hematopoietic progenitor cell differentiation is associated with altered cell cycle kinetics. Blood 93:838–848
|
[14] |
Caton ML, Smith-Raska MR, Reizis B(2007) Notch-RBP-J signaling controls the homeostasis of CD8-dendritic cells in the spleen. J Exp Med 204:1653–1664
CrossRef
Google scholar
|
[15] |
Cheng P, Gabrilovich D(2008) Notch signaling in differentiation and function of dendritic cells. Immunol Res 41:1–14
CrossRef
Google scholar
|
[16] |
Cheng P, Zlobin A, Volgina V, Gottipati S, Osborne B
CrossRef
Google scholar
|
[17] |
Cheng P, Nefedova Y, Miele L, Osborne BA, Gabrilovich D (2003) Notch signalingis necessary but not sufficient for differentiation of dendritic cells. Blood 102:3980–3988
CrossRef
Google scholar
|
[18] |
Cheng P, Nefedova Y, Corzo CA, Gabrilovich DI (2007) Regulation of dendritic-cell differentiation by bone marrow stroma via different Notch ligands. Blood 109:507–515
CrossRef
Google scholar
|
[19] |
Dees C, Zerr P, Tomcik M, Beyer C, Horn A
CrossRef
Google scholar
|
[20] |
Demehri S, Liu Z, Lee J, Lin MH, Crosby SD
|
[21] |
Dontje W, Schotte R, Cupedo T, Nagasawa M, Scheeren F
CrossRef
Google scholar
|
[22] |
Dumortier A, Durham AD, Di Piazza M, Vauclair S, Koch U
|
[23] |
Eagar TN, Tang Q, Wolfe M, He Y, Pear WS
|
[24] |
Engin F, Yao Z, Yang T, Zhou G, Bertin T
CrossRef
Google scholar
|
[25] |
Espinosa L, Cathelin S, D’Altri T, Trimarchi T, Statnikov A
CrossRef
Google scholar
|
[26] |
Fang TC, Yashiro-Ohtani Y, Del Bianco C, Knoblock DM, Blacklow SC
CrossRef
Google scholar
|
[27] |
Feng F, Wang YC, Hu XB, Liu XW, Ji G
CrossRef
Google scholar
|
[28] |
Ferrero I, Held W, Wilson A, Tacchini-Cottier F, Radtke F
CrossRef
Google scholar
|
[29] |
Foldi J, Chung AY, Xu H, Zhu J, Outtz HH
CrossRef
Google scholar
|
[30] |
Franklin RA, Liao W, Sarkar A, Kim MV, Bivona MR
CrossRef
Google scholar
|
[31] |
Fukushima H, Nakao A, Okamoto F, Shin M, Kajiya H
CrossRef
Google scholar
|
[32] |
Fung E, Tang SM, Canner JP, Morishige K, Arboleda-Velasquez JF
CrossRef
Google scholar
|
[33] |
Gibb DR, El Shikh M, Kang DJ, Rowe WJ, El Sayed R
CrossRef
Google scholar
|
[34] |
Goh F, Irvine KM, Lovelace E, Donnelly S, Jones MK
CrossRef
Google scholar
|
[35] |
Hamidi H, Gustafason D, Pellegrini M, Gasson J(2011) Identification of novel targets of CSL-dependent Notch signaling in hematopoiesis. PLoS One 6:e20022
|
[36] |
Han W, Ye Q, Moore MA (2000)Asoluble formof human Delta-like-1 inhibits differentiation of hematopoietic progenitor cells. Blood 95:1616–1625
|
[37] |
Hass MR, Sato C, Kopan R, Zhao G (2009) Presenilin: RIP and beyond. Semin Cell Dev Biol 20:201–210
CrossRef
Google scholar
|
[38] |
Hilton MJ, Tu X, Wu X, Bai S, Zhao H
CrossRef
Google scholar
|
[39] |
Hoffman C, Park SH, Daley E, Emson C, Louten J
|
[40] |
Hoyne GF, Le Roux I, Corsin-Jimenez M, Tan K, Dunne J
CrossRef
Google scholar
|
[41] |
Hu X, Ivashkiv LB (2009) Cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases. Immunity 31:539–550
CrossRef
Google scholar
|
[42] |
Hu X, Chung AY, Wu I, Foldi J, Chen J
CrossRef
Google scholar
|
[43] |
Ishii H, Nakazawa M, Yoshino S, Nakamura H, Nishioka K
CrossRef
Google scholar
|
[44] |
Iso T, Kedes L, Hamamori Y (2003) HES and HERP families: multiple effectors of the Notch signaling pathway. J Cell Physiol 194:237–255
CrossRef
Google scholar
|
[45] |
Ito T, Schaller M, Hogaboam CM, Standiford TJ, Sandor M
|
[46] |
Ito T, Allen RM, Carson WFT, Schaller M, Cavassani KA
|
[47] |
Izon DJ, Aster JC, He Y, Weng A, Karnell FG
CrossRef
Google scholar
|
[48] |
Jaiswal MK, Agrawal V, Pamarthy S, Katara GK, Kulshrestha A
CrossRef
Google scholar
|
[49] |
Jiao Z, Wang W, Guo M, Zhang T, Chen L
CrossRef
Google scholar
|
[50] |
Kapoor N, Narayana Y, Patil SA, Balaji KN (2010) Nitric oxide is involved in Mycobacterium bovis Bacillus calmette-guerin-activated Jagged1 and Notch1 signaling. JImmunol 184:3117–3126
CrossRef
Google scholar
|
[51] |
Klinakis A, Lobry C, Abdel-Wahab O, Oh P, Haeno H
CrossRef
Google scholar
|
[52] |
Kopan R, Ilagan MX (2009) The canonical Notch signalingpathway: unfolding the activation mechanism. Cell 137:216–233
CrossRef
Google scholar
|
[53] |
Kumano K, Chiba S, Shimizu K, Yamagata T, Hosoya N
CrossRef
Google scholar
|
[54] |
Lam LT, Ronchini C, Norton J, Capobianco AJ, Bresnick EH (2000) Suppression of erythroid but not megakaryocytic differentiation of human K562 erythroleukemic cells by notch-1. J Biol Chem 275:19676–19684
CrossRef
Google scholar
|
[55] |
Lewis KL, Caton ML, Bogunovic M, Greter M, Grajkowska LT
CrossRef
Google scholar
|
[56] |
Li S, Miller CH, Giannopoulou E, Hu X, Ivashkiv LB
CrossRef
Google scholar
|
[57] |
Maekawa Y, Tsukumo S, Chiba S, Hirai H, Hayashi Y
CrossRef
Google scholar
|
[58] |
Maillard I, Fang T, Pear WS (2005) Regulation of lymphoid development, differentiation, and functionby the Notch pathway. Annu Rev Immunol 23:945–974
CrossRef
Google scholar
|
[59] |
Maniati E, Bossard M, Cook N, Candido JB, Emami-Shahri N
CrossRef
Google scholar
|
[60] |
Martinez Arias A, Zecchini V, Brennan K (2002) CSL-independent Notch signalling: a checkpoint in cell fate decisions during development? Curr Opin Genet Dev 12:524–533
|
[61] |
Milner LA, Bigas A, Kopan R, Brashem-Stein C, Bernstein ID
CrossRef
Google scholar
|
[62] |
Mizutani K, Matsubayashi T, Iwase S, Doi TS, Kasai K
CrossRef
Google scholar
|
[63] |
Monsalve E, Perez MA, Rubio A, Ruiz-Hidalgo MJ, Baladron V
CrossRef
Google scholar
|
[64] |
Monsalve E, Ruiz-Garcia A, Baladron V, Ruiz-Hidalgo MJ, Sanchez-Solana B
CrossRef
Google scholar
|
[65] |
Murea M, Park JK, Sharma S, Kato H, Gruenwald A
CrossRef
Google scholar
|
[66] |
Murthy A, Shao YW, Narala SR, Molyneux SD, Zuniga-Pflucker JC
CrossRef
Google scholar
|
[67] |
Nakazawa M, Ishii H, Aono H, Takai M, Honda T
|
[68] |
Nakazawa M, Ishii H, Nakamura H, Yoshino SI, Fukamizu A
|
[69] |
Narayana Y, Balaji KN (2008) NOTCH1 up-regulation and signaling involved in Mycobacterium bovis BCG-induced SOCS3 expression in macrophages. J Biol Chem 283:12501–12511
CrossRef
Google scholar
|
[70] |
Ohishi K, Varnum-Finney B, Serda RE, Anasetti C, Bernstein ID (2001) The Notch ligand, Delta-1, inhibits the differentiation of monocytes into macrophages but permits their differentiation into dendritic cells. Blood 98:1402–1407
CrossRef
Google scholar
|
[71] |
Olivier A, Lauret E, Gonin P, Galy A(2006) The Notch ligand delta-1 is a hematopoietic development cofactor for plasmacytoid dendritic cells. Blood 107:2694–2701
CrossRef
Google scholar
|
[72] |
Ong CT, Sedy JR, Murphy KM, Kopan R(2008)Notchand presenilin regulate cellular expansion and cytokine secretion but cannot instruct Th1/Th2 fate acquisition. PLoS One 3:e2823
|
[73] |
Osborne BA, Minter LM (2007) Notch signalling during peripheral T-cell activation and differentiation. Nat Rev Immunol 7:64–75
CrossRef
Google scholar
|
[74] |
Osipo C, Golde TE, Osborne BA, Miele LA (2008) Off the beaten pathway: the complex cross talk between Notch and NF-kappaB. Lab Invest 88:11–17
CrossRef
Google scholar
|
[75] |
Ostroukhova M, Qi Z, Oriss TB, Dixon-McCarthy B, Ray P
CrossRef
Google scholar
|
[76] |
Ottaviani S, Tahiri K, Frazier A, Hassaine ZN, Dumontier MF
CrossRef
Google scholar
|
[77] |
Outtz HH, Wu JK, Wang X, Kitajewski J (2010) Notch1 deficiency results in decreased inflammation during wound healing and regulates vascular endothelial growth factor receptor-1 and inflammatory cytokine expression in macrophages. J Immunol 185:4363–4373
CrossRef
Google scholar
|
[78] |
Palaga T, Buranaruk C, Rengpipat S, Fauq AH, Golde TE
CrossRef
Google scholar
|
[79] |
Palomero T, Lim WK, Odom DT, Sulis ML, Real PJ
CrossRef
Google scholar
|
[80] |
Park JS, Kim SH, Kim K, Jin CH, Choi KY
CrossRef
Google scholar
|
[81] |
Radtke F, Wilson A, Stark G, Bauer M, van Meerwijk J
CrossRef
Google scholar
|
[82] |
Radtke F, Ferrero I, Wilson A, Lees R, Aguet M
CrossRef
Google scholar
|
[83] |
Radtke F, Fasnacht N, Macdonald HR (2010) Notch signalingin the immune system. Immunity 32:14–27
CrossRef
Google scholar
|
[84] |
Rangarajan A, Talora C, Okuyama R, Nicolas M, Mammucari C
CrossRef
Google scholar
|
[85] |
Sathe P, Wu L (2011) The network of cytokines, receptors and transcription factors governing the development of dendritic cell subsets. Protein Cell 2:620–630
CrossRef
Google scholar
|
[86] |
Schaller MA, Neupane R, Rudd BD, Kunkel SL, Kallal LE
CrossRef
Google scholar
|
[87] |
Schroeder T, Just U (2000) Notch signalling via RBP-J promotes myeloid differentiation. EMBOJ 19:2558–2568
CrossRef
Google scholar
|
[88] |
Sekine C, Moriyama Y, Koyanagi A, Koyama N, Ogata H
CrossRef
Google scholar
|
[89] |
Sekine C, Koyanagi A, Koyama N, Hozumi K, Chiba S
|
[90] |
Shackel NA, McGuinness PH, Abbott CA, Gorrell MD, McCaughan GW (2001) Identification of novel molecules and pathogenic pathways in primary biliary cirrhosis: cDNA array analysis of intrahepatic differential gene expression. Gut 49:565–576
CrossRef
Google scholar
|
[91] |
Skokos D, Nussenzweig MC (2007) CD8-DCs induce IL-12independent Th1 differentiation through Delta4Notch-like ligand in response to bacterial LPS. J Exp Med 204:1525–1531
CrossRef
Google scholar
|
[92] |
Stahl EA, Raychaudhuri S, Remmers EF, Xie G, Eyre S
CrossRef
Google scholar
|
[93] |
Swarnkar G, Karuppaiah K, Mbalaviele G, Chen TH, Abu-Amer Y (2015) Osteopetrosis in TAK1-deficient mice owing to defective NF-kappaB and NOTCH signaling. Proc Natl Acad Sci USA 112:154–159
CrossRef
Google scholar
|
[94] |
Tanigaki K, Honjo T (2007) Regulation of lymphocyte development by Notch signaling. Nat Immunol 8:451–456
CrossRef
Google scholar
|
[95] |
Tan-Pertel HT, Walker L, Browning D, Miyamoto A, Weinmaster G
CrossRef
Google scholar
|
[96] |
Tsao PN, Wei SC, Huang MT, Lee MC, Chou HC
CrossRef
Google scholar
|
[97] |
Varnum-Finney B, Purton LE, Yu M, Brashem-Stein C, Flowers D
|
[98] |
Varnum-Finney B, Brashem-Stein C, Bernstein ID (2003) Combined effects of Notch signaling and cytokines induce a multiple log increase in precursors with lymphoid and myeloid reconstituting ability. Blood 101:1784–1789
CrossRef
Google scholar
|
[99] |
Wang YC, Hu XB, He F, Feng F, Wang L
CrossRef
Google scholar
|
[100] |
Wang YC, He F, Feng F, Liu XW, Dong GY
CrossRef
Google scholar
|
[101] |
Wang H, Zou J, Zhao B, Johannsen E, Ashworth T
CrossRef
Google scholar
|
[102] |
Weber S, Niessen MT, Prox J, Lullmann-Rauch R, Schmitz A
|
[103] |
Weijzen S, Velders MP, Elmishad AG, Bacon PE, Panella JR
CrossRef
Google scholar
|
[104] |
Wu Y, Cain-Hom C, Choy L, Hagenbeek TJ, deLeon GP
CrossRef
Google scholar
|
[105] |
Xu H, Zhu J, Smith S, Foldi J, Zhao B
CrossRef
Google scholar
|
[106] |
Xu J, Chi F, Guo T, Punj V, Lee WN
CrossRef
Google scholar
|
[107] |
Yabe Y, Matsumoto T, Tsurumoto T, Shindo H (2005) Immunohistological localization of Notch receptors and their ligands Delta and Jagged in synovial tissues of rheumatoid arthritis. J Orthop Sci 10:589–594
CrossRef
Google scholar
|
[108] |
Yamada T, Yamazaki H, Yamane T, Yoshino M, Okuyama H
CrossRef
Google scholar
|
[109] |
Yashiro-Ohtani Y, Ohtani T, Pear WS (2010) Notch regulation of early thymocyte development. Semin Immunol 22:261–269
CrossRef
Google scholar
|
[110] |
Yuan JS, Kousis PC, Suliman S, Visan I, Guidos CJ (2010) Functions of notch signaling in the immune system: consensus and controversies. Annu Rev Immunol 28:343–365
CrossRef
Google scholar
|
[111] |
Zanotti S, Canalis E (2010) Notch and the skeleton. Mol Cell Biol 30:886–896
CrossRef
Google scholar
|
[112] |
Zeng Q, Li S, Chepeha DB, Giordano TJ, Li J
CrossRef
Google scholar
|
[113] |
Zhang W, Xu W, Xiong S (2010) Blockade of Notch1 signaling alleviates murine lupus via blunting macrophage activation and M2b polarization. J Immunol 184:6465–6478
CrossRef
Google scholar
|
[114] |
Zhang Q, Wang C, Liu Z, Liu X, Han C,
CrossRef
Google scholar
|
[115] |
Zhao B, Ivashkiv LB (2011) Negative regulation of osteoclastogenesis and bone resorption by cytokines and transcriptional repressors. Arthritis Res Ther 13:234
CrossRef
Google scholar
|
[116] |
Zhao B, Zou J, Wang H, Johannsen E, Peng CW
CrossRef
Google scholar
|
[117] |
Zhao B, Grimes SN, Li S, Hu X, Ivashkiv LB (2012) TNF-induced osteoclastogenesis and inflammatory bone resorption are inhibitedby transcription factor RBP-J. J Exp Med 209:319–334
CrossRef
Google scholar
|
[118] |
Zhou J, Cheng P, Youn JI, Cotter MJ, Gabrilovich DI (2009) Notch and wingless signaling cooperate in regulation of dendritic cell differentiation. Immunity 30:845–859
CrossRef
Google scholar
|
/
〈 | 〉 |