NKG2D ligands mediate immunosurveillance of senescent cells

Aging

Volumn 8, Issue 2, 2016, Pages 328-344

  Sagiv, Adi ^a   Burton, Dominick G A ^a,c   Moshayev, Zhana ^a   Vadai, Ezra ^a   Wensveen, Felix ^b   Ben Dor, Shifra ^a   Golani, Ofra ^a   Polic, Bojan ^b   Krizhanovsky, Valery ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b UNIVERSITY OF RIJEKA   (Croatia)

^c ASTON UNIVERSITY   (United Kingdom)

Author keywords

DNA damage response; ERK; Fibrosis; Natural Killer Cell; NKG2D; Senescence

Indexed keywords

LIGAND; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K;

ANIMAL; CELL AGING; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMAN; IMMUNOLOGY; IMMUNOSURVEILLANCE; KNOCKOUT MOUSE; LIVER CIRRHOSIS; MOUSE; NATURAL KILLER CELL;

ANIMALS; CELL AGING; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOLOGIC SURVEILLANCE; KILLER CELLS, NATURAL; LIGANDS; LIVER CIRRHOSIS; MICE; MICE, KNOCKOUT; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K;

EID: 84961201728     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.100897     Document Type: Article

References (58)

1. Salama R, Sadaie M, Hoare M and Narita M. Cellular senescence and its effector programs. Genes Dev. 2014; 28:99-114.
2. Munoz-Espin D and Serrano M. Cellular senescence: from physiology to pathology. Nat Rev Mol Cell Biol. 2014; 15:482-496.
3. Burton DG and Krizhanovsky V. Physiological and pathological consequences of cellular senescence. Cell Mol Life Sci. 2014; 71:4373-4386.
4. Campisi J. Aging, cellular senescence, and cancer. Annual review of physiology. 2013; 75:685-705.
5. Kuilman T, Michaloglou C, Mooi WJ and Peeper DS. The essence of senescence. Genes Dev. 2010; 24:2463-2479.
6. Chuprin A, Gal H, Biron-Shental T, Biran A, Amiel A, Rozenblatt S and Krizhanovsky V. Cell fusion induced by ERVWE1 or measles virus causes cellular senescence. Genes Dev. 2013; 27:2356-2366.
7. Mallette FA, Gaumont-Leclerc MF and Ferbeyre G. The DNA damage signaling pathway is a critical mediator of oncogeneinduced senescence. Genes Dev. 2007; 21:43-48.
8. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, Luise C, Schurra C, Garre M, Nuciforo PG, Bensimon A, Maestro R, Pelicci PG and d'Adda di Fagagna F. Oncogene-induced senescence is a DNA damage response triggered by DNA hyperreplication. Nature. 2006; 444:638-642.
9. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, Vassiliou LV, Kolettas E, Niforou K, Zoumpourlis VC, Takaoka M, Nakagawa H, Tort F, et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature. 2006; 444:633-637.
10. Narita M, Narita M, Krizhanovsky V, Nunez S, Chicas A, Hearn SA, Myers MP and Lowe SW. A novel role for high-mobility group a proteins in cellular senescence and heterochromatin formation. Cell. 2006; 126:503-514.
11. Narita M, Nunez S, Heard E, Narita M, Lin AW, Hearn SA, Spector DL, Hannon GJ and Lowe SW. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell. 2003; 113:703-716.
12. Ovadya Y and Krizhanovsky V. Senescent cells: SASPected drivers of age-related pathologies. Biogerontology. 2014; 15:627-642.
13. Naylor RM, Baker DJ and van Deursen JM. Senescent cells: a novel therapeutic target for aging and age-related diseases. Clinical pharmacology and therapeutics. 2013; 93:105-116.
14. Sagiv A and Krizhanovsky V. Immunosurveillance of senescent cells: the bright side of the senescence program. Biogerontology. 2013; 14:617-628.
15. Hoenicke L and Zender L. Immune surveillance of senescent cells-biological significance in cancer-and non-cancer pathologies. Carcinogenesis. 2012; 33:1123-1126.
16. Burton DG and Faragher RG. Cellular senescence: from growth arrest to immunogenic conversion. Age (Dordr). 2015; 37:27.
17. Narita M and Lowe SW. Senescence comes of age. Nat Med. 2005; 11:920-922.
18. Serrano M, Lin AW, McCurrach ME, Beach D and Lowe SW. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell. 1997; 88:593-602.
19. Xue W, Zender L, Miething C, Dickins RA, Hernando E, Krizhanovsky V, Cordon-Cardo C and Lowe SW. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature. 2007; 445:656-660.
20. Kang TW, Yevsa T, Woller N, Hoenicke L, Wuestefeld T, Dauch D, Hohmeyer A, Gereke M, Rudalska R, Potapova A, Iken M, Vucur M, Weiss S, et al. Senescence surveillance of premalignant hepatocytes limits liver cancer development. Nature. 2011; 479:547-551.
21. Krizhanovsky V, Yon M, Dickins RA, Hearn S, Simon J, Miething C, Yee H, Zender L and Lowe SW. Senescence of activated stellate cells limits liver fibrosis. Cell. 2008; 134:657-667.
22. Jun JI and Lau LF. The matricellular protein CCN1 induces fibroblast senescence and restricts fibrosis in cutaneous wound healing. Nat Cell Biol. 2010; 12:676-685.
23. Sagiv A, Biran A, Yon M, Simon J, Lowe SW and Krizhanovsky V. Granule exocytosis mediates immune surveillance of senescent cells. Oncogene. 2013; 32:1971-1977.
24. Iannello A and Raulet DH. Immune surveillance of unhealthy cells by natural killer cells. Cold Spring Harb Symp Quant Biol. 2013; 78:249-257.
25. Bernardini G, Gismondi A and Santoni A. Chemokines and NK cells: regulators of development, trafficking and functions. Immunology letters. 2012; 145:39-46.
26. Iannello A, Thompson TW, Ardolino M, Lowe SW and Raulet DH. p53-dependent chemokine production by senescent tumor cells supports NKG2D-dependent tumor elimination by natural killer cells. J Exp Med. 2013; 210:2057-2069.
27. Soriani A, Zingoni A, Cerboni C, Iannitto ML, Ricciardi MR, Di Gialleonardo V, Cippitelli M, Fionda C, Petrucci MT, Guarini A, Foa R and Santoni A. ATM-ATR-dependent up-regulation of DNAM-1 and NKG2D ligands on multiple myeloma cells by therapeutic agents results in enhanced NK-cell susceptibility and is associated with a senescent phenotype. Blood. 2009; 113:3503-3511.
28. Lanier LL. NKG2D Receptor and Its Ligands in Host Defense. Cancer immunology research. 2015; 3:575-582.
29. Eagle RA and Trowsdale J. Promiscuity and the single receptor: NKG2D. Nat Rev Immunol. 2007; 7:737-744.
30. Soriani A, Fionda C, Ricci B, Iannitto ML, Cippitelli M and Santoni A. Chemotherapy-elicited upregulation of NKG2D and DNAM-1 ligands as a therapeutic target in multiple myeloma. Oncoimmunology. 2013; 2:e26663.
31. Chahroudi A, Silvestri G and Feinberg MB. Measuring T cellmediated cytotoxicity using fluorogenic caspase substrates. Methods. 2003; 31:120-126.
32. Gasser S, Orsulic S, Brown EJ and Raulet DH. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature. 2005; 436:1186-1190.
33. Deschenes-Simard X, Gaumont-Leclerc MF, Bourdeau V, Lessard F, Moiseeva O, Forest V, Igelmann S, Mallette FA, Saba-El-Leil MK, Meloche S, Saad F, Mes-Masson AM and Ferbeyre G. Tumor suppressor activity of the ERK/MAPK pathway by promoting selective protein degradation. Genes Dev. 2013; 27:900-915.
34. Stanietsky N and Mandelboim O. Paired NK cell receptors controlling NK cytotoxicity. FEBS Lett. 2010; 584:4895-4900.
35. Chan CJ, Martinet L, Gilfillan S, Souza-Fonseca-Guimaraes F, Chow MT, Town L, Ritchie DS, Colonna M, Andrews DM and Smyth MJ. The receptors CD96 and CD226 oppose each other in the regulation of natural killer cell functions. Nature immunology. 2014; 15:431-438.
36. Puche JE, Saiman Y and Friedman SL. Hepatic stellate cells and liver fibrosis. Comprehensive Physiology. 2013; 3:1473-1492.
37. Radaeva S, Sun R, Jaruga B, Nguyen VT, Tian Z and Gao B. Natural killer cells ameliorate liver fibrosis by killing activated stellate cells in NKG2D-dependent and tumor necrosis factorrelated apoptosis-inducing ligand-dependent manners. Gastroenterology. 2006; 130:435-452.
38. Kim TW, Kim HJ, Lee C, Kim HY, Baek SH, Kim JH, Kwon KS and Kim JR. Identification of replicative senescence-associated genes in human umbilical vein endothelial cells by an annealing control primer system. Exp Gerontol. 2008; 43:286-295.
39. Stern-Ginossar N and Mandelboim O. An integrated view of the regulation of NKG2D ligands. Immunology. 2009; 128:1-6.
40. Lasry A and Ben-Neriah Y. Senescence-associated inflammatory responses: aging and cancer perspectives. Trends Immunol. 2015; 36:217-228.
41. Laberge RM, Sun Y, Orjalo AV, Patil CK, Freund A, Zhou L, Curran SC, Davalos AR, Wilson-Edell KA, Liu S, Limbad C, Demaria M, Li P, et al. MTOR regulates the pro-tumorigenic senescence associated secretory phenotype by promoting IL1A translation. Nat Cell Biol. 2015; 17:1049-1061.
42. Freund A, Patil CK and Campisi J. p38MAPK is a novel DNA damage response-independent regulator of the senescenceassociated secretory phenotype. EMBO J. 2011; 30:1536-1548.
43. Chien Y, Scuoppo C, Wang X, Fang X, Balgley B, Bolden JE, Premsrirut P, Luo W, Chicas A, Lee CS, Kogan SC and Lowe SW. Control of the senescence-associated secretory phenotype by NF-(kappa)B promotes senescence and enhances chemosensitivity. Genes Dev. 2011; 25:2125-2136.
44. Rodier F, Coppe JP, Patil CK, Hoeijmakers WA, Munoz DP, Raza SR, Freund A, Campeau E, Davalos AR and Campisi J. Persistent DNA damage signalling triggers senescenceassociated inflammatory cytokine secretion. Nat Cell Biol. 2009; 11:973-979.
45. Kuilman T, Michaloglou C, Vredeveld LC, Douma S, van Doorn R, Desmet CJ, Aarden LA, Mooi WJ and Peeper DS. Oncogeneinduced senescence relayed by an interleukin-dependent inflammatory network. Cell. 2008; 133:1019-1031.
46. Acosta JC, O'Loghlen A, Banito A, Guijarro MV, Augert A, Raguz S, Fumagalli M, Da Costa M, Brown C, Popov N, Takatsu Y, Melamed J, d'Adda di Fagagna F, et al. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell. 2008; 133:1006-1018.
47. Liu XV, Ho SS, Tan JJ, Kamran N and Gasser S. Ras activation induces expression of Raet1 family NK receptor ligands. J Immunol. 2012; 189:1826-1834.
48. Katlinskaya YV, Carbone CJ, Yu Q and Fuchs SY. Type 1 interferons contribute to the clearance of senescent cell. Cancer Biol Ther. 2015; 16:1214-1219.
49. Yu Q, Katlinskaya YV, Carbone CJ, Zhao B, Katlinski KV, Zheng H, Guha M, Li N, Chen Q, Yang T, Lengner CJ, Greenberg RA, Johnson FB, et al. DNA-damage-induced type I interferon promotes senescence and inhibits stem cell function. Cell Rep. 2015; 11:785-797.
50. Wortzel I and Seger R. The ERK Cascade: Distinct Functions within Various Subcellular Organelles. Genes & cancer. 2011; 2:195-209.
51. Deschenes-Simard X, Kottakis F, Meloche S and Ferbeyre G. ERKs in cancer: friends or foes? Cancer Res. 2014; 74:412-419.
52. Gaumont-Leclerc MF, Mukhopadhyay UK, Goumard S and Ferbeyre G. PEA-15 is inhibited by adenovirus E1A and plays a role in ERK nuclear export and Ras-induced senescence. J Biol Chem. 2004; 279:46802-46809.
53. Lorenzini A, Tresini M, Mawal-Dewan M, Frisoni L, Zhang H, Allen RG, Sell C and Cristofalo VJ. Role of the Raf/MEK/ERK and the PI3K/Akt(PKB) pathways in fibroblast senescence. Exp Gerontol. 2002; 37:1149-1156.
54. Biran A, Perelmutter M, Gal H, Burton DG, Ovadya Y, Vadai E, Geiger T and Krizhanovsky V. Senescent cells communicate via intercellular protein transfer. Genes Dev. 2015; 29:791-802.
55. Hazeldine J and Lord JM. The impact of ageing on natural killer cell function and potential consequences for health in older adults. Ageing research reviews. 2013; 12:1069-1078.
56. Hanna J, Wald O, Goldman-Wohl D, Prus D, Markel G, Gazit R, Katz G, Haimov-Kochman R, Fujii N, Yagel S, Peled A and Mandelboim O. CXCL12 expression by invasive trophoblasts induces the specific migration of CD16-human natural killer cells. Blood. 2003; 102:1569-1577.
57. Zafirova B, Mandaric S, Antulov R, Krmpotic A, Jonsson H, Yokoyama WM, Jonjic S and Polic B. Altered NK cell development and enhanced NK cell-mediated resistance to mouse cytomegalovirus in NKG2D-deficient mice. Immunity. 2009; 31:270-282.
58. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012; 9:676-682.