Optimal effector functions in human natural killer cells rely upon autocrine bone morphogenetic protein signaling

Cancer Research

Volumn 74, Issue 18, 2014, Pages 5019-5031

  Robson, Neil C ^a   Hidalgo, Laura ^b   McAlpine, Tristan ^c   Wei, Heng ^c   Martínez, Víctor G ^b   Entrena, Ana ^b   Melen, Gustavo J ^d   MacDonald, Andrew S ^e   Phythian Adams, Alexander ^e   Sacedón, Rosa ^b   Maraskovsky, Eugene ^f   Cebon, Jonathan ^c   Ramírez, Manuel ^d   Vicente, Angeles ^b   Varas, Alberto ^b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c LUDWIG INSTITUTE FOR CANCER RESEARCH   (Australia)

^d HOSPITAL INFANTIL UNIVERSITARIO NIÑO JESÚS   (Spain)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

^f CSL LIMITED   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR; MESSENGER RNA;

AUTOCRINE EFFECT; BIOSYNTHESIS; CELL DIFFERENTIATION; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; NATURAL KILLER CELL; SIGNAL TRANSDUCTION;

AUTOCRINE COMMUNICATION; BONE MORPHOGENETIC PROTEIN RECEPTORS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; HUMANS; KILLER CELLS, NATURAL; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84907486880     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-2845     Document Type: Article

References (51)

1. Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, et al. Innate or adaptive immunity? The example of natural killer cells. Science 2011;331:44-9.
2. Lanier LL, Le AM, Civin CI, Loken MR, Phillips JH. The relationship of CD16 (Leu-11) and Leu-19 (NKH-1) antigen expression on human peripheral blood NK cells and cytotoxic T lymphocytes. J Immunol 1986;136:4480-6.
3. Fehniger TA, Cooper MA, Nuovo GJ, Cella M, Facchetti F, Colonna M, et al. CD56bright natural killer cells are present in human lymph nodes and are activated by T cell-derived IL-2: a potential new link between adaptive and innate immunity. Blood 2003;101:3052-7.
4. Vitale M, Della Chiesa M, Carlomagno S, Romagnani C, Thiel A, Moretta L, et al. The small subset of CD56brightCD16-natural killer cells is selectively responsible for both cell proliferation and interferongamma production upon interaction with dendritic cells. Eur J Immunol 2004;34:1715-22.
5. Fernandez LA, Pope B, Lee C, Zayed E. Aggressive natural killer cell leukemia in an adult with establishment of an NK cell line. Blood 1986;67:925-30.
6. Chan A, Filer A, Parsonage G, Kollnberger S, Gundle R, Buckley CD, et al. Mediation of the proinflammatory cytokine response in rheumatoid arthritis and spondylarthritis by interactions between fibroblast-like synoviocytes and natural killer cells. Arthritis Rheum 2008;58:707-17.
7. Banchereau J, Pascual V, O'Garra A. From IL-2 to IL-37: the expanding spectrum of anti-inflammatory cytokines. Nat Immunol 2012;13:925-31.
8. Moretta A, Vitale M, Sivori S, Bottino C, Morelli L, Augugliaro R, et al. Human natural killer cell receptors for HLA-class I molecules. Evidence that the Kp43 (CD94) molecule functions as receptor for HLA-B alleles. J Exp Med 1994;180:545-55.
9. Agaugue S, Marcenaro E, Ferranti B, Moretta L, Moretta A. Human natural killer cells exposed to IL-2, IL-12, IL-18, or IL-4 differently modulate priming of naive T cells by monocyte-derived dendritic cells. Blood 2008;112:1776-83.
10. Castriconi R, Cantoni C, Della Chiesa M, Vitale M, Marcenaro E, Conte R, et al. Transforming growth factor beta 1 inhibits expression of NKp30 and NKG2D receptors: consequences for the NK-mediated killing of dendritic cells. Proc Natl Acad Sci U S A 2003;100:4120-5.
11. Robson NC, Wei H, McAlpine T, Kirkpatrick N, Cebon J, Maraskovsky E. Activin-A attenuates several human natural killer cell functions. Blood 2009;113:3218-25.
12. Hidalgo L, Martinez VG, Valencia J, Hernandez-Lopez C, Vazquez MN, Nunez JR, et al. Expression of BMPRIA on human thymic NK cell precursors: role of BMP signaling in intrathymic NK cell development. Blood 2012;119:1861-71.
13. Mueller TD, Nickel J. Promiscuity and specificity in BMP receptor activation. FEBS Lett 2012;586:1846-59.
14. Sieber C, Kopf J, Hiepen C, Knaus P. Recent advances in BMP receptor signaling. Cytokine Growth Factor Rev 2009;20:343-55.
15. Liu F, Hata A, Baker JC, Doody J, Carcamo J, Harland RM, et al. A human Mad protein acting as a BMP-regulated transcriptional activator. Nature 1996;381:620-3.
16. Urist MR. Bone: formation by autoinduction. Science 1965;150:893-9.
17. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, et al. Novel regulators of bone formation: molecular clones and activities. Science 1988;242:1528-34.
18. Plikus MV, Mayer JA, De La Cruz D, Baker RE, Maini PK, Maxson R, et al. Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 2008;451:340-4.
19. Liu A, Niswander LA. Bone morphogenetic protein signalling and vertebrate nervous system development. Nat Rev Neurosci 2005;6:945-54.
20. Francis PH, Richardson MK, Brickell PM, Tickle C. Bone morphogenetic proteins and a signalling pathway that controls patterning in the developing chick limb. Development 1994;120:209-18.
21. Vukicevic S, Latin V, Chen P, Batorsky R, Reddi AH, Sampath TK. Localization of osteogenic protein-1 (bone morphogenetic protein-7) during human embryonic development: high affinity binding to basement membranes. Biochem Biophys Res Commun 1994;198:693-700.
22. Dudley AT, Lyons KM, Robertson EJ. A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev 1995;9:2795-807.
23. Nakashima M, Reddi AH. The application of bone morphogenetic proteins to dental tissue engineering. Nat Biotechnol 2003;21:1025-32.
24. Ozkaynak E, Schnegelsberg PN, Oppermann H. Murine osteogenic protein (OP-1): high levels of mRNA in kidney. Biochem Biophys Res Commun 1991;179:116-23.
25. Kingsley DM, Bland AE, Grubber JM, Marker PC, Russell LB, Copeland NG, et al. The mouse short ear skeletal morphogenesis locus is associated with defects in a bone morphogenetic member of the TGF beta superfamily. Cell 1992;71:399-410.
26. Gong Y, Krakow D, Marcelino J, Wilkin D, Chitayat D, Babul-Hirji R, et al. Heterozygous mutations in the gene encoding noggin affect human joint morphogenesis. Nat Genet 1999;21:302-4.
27. Lehmann K, Seemann P, Stricker S, Sammar M, Meyer B, Suring K, et al. Mutations in bone morphogenetic protein receptor 1B cause brachydactyly type A2. Proc Natl Acad Sci USA 2003;100:12277-82.
28. Shore EM, Xu M, Feldman GJ, Fenstermacher DA, Cho TJ, Choi IH, et al. A recurrent mutation in the BMP type I receptor ACVR1 causes inherited and sporadic fibrodysplasia ossificans progressiva. Nat Genet 2006;38:525-7.
29. Israel DI, Nove J, Kerns KM, Kaufman RJ, Rosen V, Cox KA, et al. Heterodimeric bone morphogenetic proteins show enhanced activity in vitro and in vivo. Growth Factors 1996;13:291-300.
30. Kotzsch A, Nickel J, Seher A, Heinecke K, Van Geersdaele L, Herrmann T, et al. Structure analysis of bone morphogenetic protein-2 type I receptor complexes reveals a mechanism of receptor inactivation in juvenile polyposis syndrome. J Biol Chem 2008;283:5876-87.
31. Harth S, Kotzsch A, Hu J, Sebald W, Mueller TD. A selection fit mechanism in BMP receptor IA as a possible source for BMP ligand-receptor promiscuity. PLoS ONE 2010;5.
32. Alarcon C, Zaromytidou AI, Xi Q, Gao S, Yu J, Fujisawa S, et al. Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-beta pathways. Cell 2009;139:757-69.
33. Onichtchou KD, Chen YG, Dosch R, Gawantka V, Delius H, Massague J, et al. Silencing of TGF-beta signalling by the pseudoreceptor BAMBI. Nature 1999;401:480-5.
34. Takase M, Imamura T, Sampath TK, Takeda K, Ichijo H, Miyazono K, et al. Induction of Smad6 mRNA by bone morphogenetic proteins. Biochem Biophys Res Commun 1998;244:26-9.
35. Hata A, Lagna G, Massague J, Hemmati-Brivanlou A. Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev 1998;12:186-97.
36. Casellas R, Brivanlou AH. Xenopus Smad7 inhibits both the activin and BMP pathways and acts as a neural inducer. Dev Biol 1998;198:1-12.
37. Zhu H, Kavsak P, Abdollah S, Wrana JL, Thomsen GH. A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 1999;400:687-93.
38. Zhang Y, Chang C, Gehling DJ, Hemmati-Brivanlou A, Derynck R. Regulation of Smad degradation and activity by Smurf2, an E3 ubiquitin ligase. Proc Natl Acad Sci U S A 2001;98:974-9.
39. Katsuno Y, Hanyu A, Kanda H, Ishikawa Y, Akiyama F, Iwase T, et al. Bone morphogenetic protein signaling enhances invasion and bone metastasis of breast cancer cells through Smad pathway. Oncogene 2008;27:6322-33.
40. Langenfeld E, Hong CC, Lanke G, Langenfeld J. Bone morphogenetic protein type I receptor antagonists decrease growth and induce cel death of lung cancer cell lines. PLoS ONE 2013;8:e61256.
41. Hardwick JC, Van Den Brink GR, Bleuming SA, Ballester I, Van Den Brande JM, Keller JJ, et al. Bone morphogenetic protein 2 is expressed by, and acts upon, mature epithelial cells in the colon. Gastroenterology 2004;126:111-21.
42. Piccirillo SG, Reynolds BA, Zanetti N, Lamorte G, Binda E, Broggi G, et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 2006;444:761-5.
43. Martinez-Laperche C, Gomez-Garcia AM, Lassaletta A, Moscardo C, Vivanco JL, Molina J, et al. Detection of occult cerebrospinal fluid involvement during maintenance therapy identifies a group of children with acute lymphoblastic leukemia at high risk for relapse. Am J Hematol 2013;88:359-64.
44. Yu PB, Hong CC, Sachidanandan C, Babitt JL, Deng DY, Hoyng SA, et al. Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat Chem Biol 2008;4:33-41.
45. Zimmerman LB, De Jesus-Escobar JM, Harland RM. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 1996;86:599-606.
46. Laouar Y, Sutterwala FS, Gorelik L, Flavell RA. Transforming growth factor-betacontrolsThelpertype 1 cell development through regulation of natural killer cell interferon-gamma. Nat Immunol 2005;6:600-7.
47. Robson NC, Phillips DJ, McAlpine T, Shin A, Svobodova S, Toy T, et al. Activin-A: a novel dendritic cell-derived cytokine that potently attenuates CD40 ligand-specific cytokine and chemokine production. Blood 2008;111:2733-43.
48. Song GA, Kim HJ, Woo KM, Baek JH, Kim GS, Choi JY, et al. Molecular consequences of the ACVR1 (R206H) mutation of fibrodysplasia ossificans progressiva. J Biol Chem 2010;285:22542-53.
49. Shi W, Chang C, Nie S, Xie S, Wan M, Cao X. Endofin acts as a Smad anchor for receptor activation in BMP signaling. J Cell Sci 2007;120:1216-4.
50. Itoh F, Divecha N, Brocks L, Oomen L, Janssen H, Calafat J, et al. The FYVE domain in Smad anchor for receptor activation (SARA) is sufficient for localization of SARA in early endosomes and regulates TGF-beta/Smad signalling. Genes Cells 2002;7:321-31.
51. Miura S, Takeshita T, Asao H, Kimura Y, Murata K, Sasaki Y, et al. Hgs (Hrs), a FYVE domain protein, is involved in Smad signaling through cooperation with SARA. Mol Cell Biol 2000;20:9346-9355.