RORγt+ innate lymphoid cells promote lymph node metastasis of breast cancers

Cancer Research

Volumn 77, Issue 5, 2017, Pages 1083-1096

  Irshad, Sheeba ^a   Flores Borja, Fabian ^a   Lawler, Katherine ^a   Monypenny, James ^a   Evans, Rachel ^a   Male, Victoria ^a   Gordon, Peter ^a   Cheung, Anthony ^a   Gazinska, Patrycja ^a   Noor, Farzana ^a   Wong, Felix ^a   Grigoriadis, Anita ^a   Fruhwirth, Gilbert O ^a,b   Barber, Paul R ^c   Woodman, Natalie ^d   Patel, Dominic ^e   Rodriguez Justo, Manuel ^e   Owen, Julie ^d   Martin, Stewart G ^f   Sarah, E Pinder ^d,g   Cheryl, E Gillett ^d,g   Poland, Simon P ^a   Ameer Beg, Simon ^a   McCaughan, Frank ^a,h   Carlin, Leo M ^b   Hasan, Uzma ^e   Withers, David R ⁱ   Lane, Peter ⁱ   Vojnovic, Borivoj ^c   Quezada, Sergio A ^j   Ellis, Paul ^k   Tutt, Andrew N J ^a,l   Ng, Tony ^a,j   more..

^a KING'S COLLEGE LONDON   (United Kingdom)

^b BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^f NOTTINGHAM UNIVERSITY HOSPITALS NHS TRUST   (United Kingdom)

^g GUY S HOSPITAL   (United Kingdom)

^h UNIVERSITY OF CAMBRIDGE   (United Kingdom)

ⁱ MEDICAL RESEARCH COUNCIL   (United Kingdom)

^j UNIVERSITY COLLEGE LONDON   (United Kingdom)

^k GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

^l INSTITUTE OF CANCER RESEARCH   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CXCL13 CHEMOKINE; OSTEOCLAST DIFFERENTIATION FACTOR; RETINOID RELATED ORPHAN RECEPTOR GAMMA; RETINOID RELATED ORPHAN RECEPTOR GAMMA T; SECONDARY LYMPHOID TISSUE CHEMOKINE; UNCLASSIFIED DRUG; ORPHAN NUCLEAR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; BREAST CANCER; BREAST CANCER CELL LINE; CELL INTERACTION; CONTROLLED STUDY; CORRELATIONAL STUDY; DISEASE ASSOCIATION; FEEDBACK SYSTEM; GENE EXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPH NODE METASTASIS; LYMPHOID CELL; MOUSE; NONHUMAN; STROMA CELL; TUMOR MICROENVIRONMENT; ANIMAL; BAGG ALBINO MOUSE; BREAST TUMOR; EXPERIMENTAL MAMMARY NEOPLASM; FEMALE; IMMUNOLOGY; INNATE IMMUNITY; LYMPHOCYTE; METASTASIS; PATHOLOGY; TRANSGENIC MOUSE; TRIPLE NEGATIVE BREAST CANCER; TUMOR CELL LINE;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CHEMOKINE CCL21; CHEMOKINE CXCL13; FEMALE; HUMANS; IMMUNITY, INNATE; LYMPHATIC METASTASIS; LYMPHOCYTES; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; NEOPLASM METASTASIS; ORPHAN NUCLEAR RECEPTORS; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 85015847460     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-16-0598     Document Type: Article

References (51)

1. Mohammed RA, Ellis IO,MahmmodAM, Hawkes EC, Green AR, Rakha EA, et al. Lymphatic and blood vessels in basal and triple-negative breast cancers: characteristics and prognostic significance. Mod Pathol 2011;24: 774-85.
2. Stein JV,Nombela-Arrieta C. Chemokine control of lymphocyte trafficking: a general overview. Immunology 2005;116:1-12.
3. Ansel KM, Ngo VN, Hyman PL, Luther SA, Forster R, Sedgwick JD, et al. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature 2000;20;406:309-14.
4. Ohl L, Henning G, Krautwald S, Lipp M, Hardtke S, Bernhardt G, et al. Cooperating mechanisms of CXCR5 and CCR7 in development and organization of secondary lymphoid organs. J Exp Med 2003;197: 1199-204.
5. van de Pavert SA, Olivier BJ, Goverse G, VondenhoffMF, GreuterM, Beke P, et al. Chemokine CXCL13 is essential for lymph node initiation and is induced by retinoic acid and neuronal stimulation. Nat Immunol 2009; 10:1193-9.
6. Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP, Eberl G, et al. Innate lymphoid cells-A proposal for uniform nomenclature. Nat Rev Immunol 2013;13:145-9.
7. Sun Z, Unutmaz D, Zou YR, Sunshine MJ, Pierani A, Brenner-Morton S, et al. Requirement for RORgamma in thymocyte survival and lymphoid organ development. Science 2000;288:2369-73.
8. Tsuji M, Suzuki K, Kitamura H, Maruya M, Kinoshita K, Ivanov II, et al. Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut. Immunity 2008;29:261-71.
9. Scandella E, Bolinger B, Lattmann E, Miller S, Favre S, Littman DR, et al. Restoration of lymphoid organ integrity through the interaction of lymphoid tissue-inducer cells with stroma of the T cell zone. Nat Immunol 2008;9:667-75.
10. Honda K, Nakano H, Yoshida H, Nishikawa S, Rennert P, Ikuta K, et al. Molecular basis for hematopoietic/mesenchymal interaction during initiation of Peyer's patch organogenesis. J Exp Med 2001;193:621-30.
11. Weigelt B, Mackay A, A'Hern R, Natrajan R, TanDS, Dowsett M, et al. Breast cancer molecular profiling with single sample predictors: a retrospective analysis. Lancet Oncol 2010;11:339-49.
12. Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 2009;27:1160-7.
13. Gazinska P, Grigoriadis A, Brown JP, Millis RR, Mera A, Gillett CE, et al. Comparison of basal-like triple-negative breast cancer defined by morphology, immunohistochemistry and transcriptional profiles. Mod Pathol 2013;26:955-66.
14. Withers DR, Gaspal FM, Mackley EC, Marriott CL, Ross EA, Desanti GE, et al. Cutting edge: lymphoid tissue inducer cells maintain memory CD4 T cells within secondary lymphoid tissue. J Immunol 2012;189:2094-8.
15. Lelekakis M, Moseley JM, Martin TJ, Hards D, Williams E, Ho P, et al. A novel orthotopic model of breast cancer metastasis to bone. Clin Exp Metastasis 1999;17:163-70.
16. Kedrin D, Gligorijevic B, Wyckoff J, Verkhusha VV, Condeelis J, Segall JE, et al. Intravital imaging of metastatic behavior through a mammary imaging window. Nat Methods 2008;5:1019-21.
17. Hothorn T, Hornik H, van de Wiel MA, Zeileis A. A lego system for conditional inference. Am Stat 2006;60:257-63.
18. Kaur P, Nagaraja GM, Zheng H, Gizachew D, Galukande M, Krishnan S, et al. A mouse model for triple-negative breast cancer tumor-initiating cells (TNBC-TICs) exhibits similar aggressive phenotype to the human disease. BMC Cancer 2012;12:120.
19. Walker JA, Barlow JL, McKenzie AN. Innate lymphoid cells-how did we miss them? Nat Rev Immunol 2013;13:75-87.
20. Kim S, Han S, Withers DR, Gaspal F, Bae J, Baik S, et al. CD117(+) CD3(-) CD56(-) OX40Lhigh cells express IL-22 and display an LTi phenotype in human secondary lymphoid tissues. Eur J Immunol 2011;41:1563-72.
21. Shields JD, Kourtis IC, Tomei AA, Roberts JM, Swartz MA. Induction of lymphoidlike stroma and immune escape by tumors that express the chemokine CCL21. Science 2010;328:749-52.
22. Brendolan A, Caamano JH. Mesenchymal cell differentiation during lymph node organogenesis. Front Immunol 2012;3:381.
23. Evans I, Kim MY. Involvement of lymphoid inducer cells in the development of secondary and tertiary lymphoid structure. BMB Rep 2009;42:189-93.
24. Bernardo ME, Locatelli F, Fibbe WE. Mesenchymal stromal cells. Ann N Y Acad Sci 2009;1176:101-17.
25. Monticelli LA, Sonnenberg GF, Abt MC, Alenghat T, Ziegler CG, Doering TA, et al. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat Immunol 2011;12:1045-54.
26. Mueller CG, Hess E. Emerging functions of RANKL in lymphoid tissues. Front Immunol 2012;3:261.
27. Sambandam Y, Sundaram K, Liu A, Kirkwood KL, Ries WL, Reddy SV. CXCL13 activation of c-Myc induces RANK ligand expression in stromal/preosteoblast cells in the oral squamous cell carcinoma tumor-bone microenvironment. Oncogene 2013;32:97-105.
28. PalafoxM, Ferrer I, Pellegrini P, Vila S, Hernandez-Ortega S, Urruticoechea A, et al. RANK induces epithelial-mesenchymal transition and stemness in humanmammary epithelial cells and promotes tumorigenesis and metastasis. Cancer Res 2012;72:2879-88.
29. Curtis C, Shah SP, Chin SF, TurashviliG, Rueda OM, Dunning MJ, et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 2012;486:346-52.
30. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, et al. Molecular portraits of human breast tumours. Nature 2000;406: 747-52.
31. Pages F, Galon J, Dieu-Nosjean MC, Tartour E, Sautes-Fridman C, Fridman WH. Immune infiltration in human tumors: a prognostic factor that should not be ignored. Oncogene 2010;29:1093-102.
32. Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med 2013;19:1423-37.
33. Eisenring M, vom Berg J, Kristiansen G, Saller E, Becher B. IL-12 initiates tumor rejection via lymphoid tissue-inducer cells bearing the natural cytotoxicity receptor NKp46. Nat Immunol 2010;11:1030-8.
34. Carrega P, Loiacono F, Di Carlo E, Scaramuccia A, Mora M, Conte R, et al. NCR(+)ILC3 concentrate in human lung cancer and associate with intratumoral lymphoid structures. Nat Commun 2015;6:8280.
35. Mashino K, Sadanaga N, Yamaguchi H, Tanaka F,Ohta M, Shibuta K, et al. Expression of chemokine receptor CCR7 is associated with lymph node metastasis of gastric carcinoma. Cancer Res 2002;62:2937-41.
36. Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001;410:50-6.
37. Spaeth E, Klopp A, Dembinski J, Andreeff M, Marini F. Inflammation and tumor microenvironments: defining the migratory itinerary of mesenchymal stem cells. Gene Ther 2008;15:730-8.
38. Dvorak HF. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 1986;315:1650-9.
39. Benezech C, White A, Mader E, Serre K, Parnell S, Pfeffer K, et al. Ontogeny of stromal organizer cells during lymph node development. J Immunol 2010;184:4521-30.
40. Biswas S, Sengupta S, Roy Chowdhury S, Jana S, Mandal G, Mandal PK, et al. CXCL13-CXCR5 co-expression regulates epithelial to mesenchymal transition of breast cancer cells during lymph node metastasis. Breast Cancer Res Treat 2014;143:265-76.
41. Panse J, Friedrichs K, Marx A, Hildebrandt Y, Luetkens T, Barrels K, et al. Chemokine CXCL13 is overexpressed in the tumour tissue and in the peripheral blood of breast cancer patients. Br J Cancer 2008;99:930-8.
42. Razis E, Kalogeras KT, Kotoula V, Eleftheraki AG, Nikitas N, Kronenwett R, et al. Improved outcome of high-risk early HER2 positive breast cancer with high CXCL13-CXCR5 messenger RNA expression. Clin Breast Cancer 2012;12:183-93.
43. Yau C, Esserman L, Moore DH, Waldman F, Sninsky J, Benz CC. A multigene predictor of metastatic outcome in early stage hormone receptornegative and triple-negative breast cancer. Breast Cancer Res 2010;12:R85.
44. Sabatier R, Finetti P, Mamessier E, Raynaud S, Cervera N, Lambaudie E, et al. Kinome expression profiling and prognosis of basal breast cancers. Mol Cancer 2011;10:86.
45. DeNardo DG, Andreu P, Coussens LM. Interactions between lymphocytes and myeloid cells regulate pro-versus anti-tumor immunity. Cancer Metastasis Rev 2010;29:309-16.
46. Viola A, Sarukhan A, Bronte V, Molon B. The pros and cons of chemokines in tumor immunology. Trends Immunol 2012;33: 496-504.
47. Gu-Trantien C, Loi S, Garaud S, Equeter C, Libin M, de Wind A, et al. CD4+ follicular helper T cell infiltration predicts breast cancer survival. J Clin Invest 2013;123:2873-92.
48. Loi S, Sirtaine N, Piette F, Salgado R, Viale G, Van Eenoo F, et al. Prognostic and predictive value of tumor-infiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: BIG 02-98. J Clin Oncol 2013;31: 860-7.
49. Denkert C, Loibl S, Noske A, Roller M, Muller BM, Komor M, et al. Tumor-Associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol 2010; 28:105-13.
50. Ono M, Tsuda H, Shimizu C, Yamamoto S, Shibata T, Yamamoto H, et al. Tumor-infiltrating lymphocytes are correlated with response to neoadjuvant chemotherapy in triple-negative breast cancer. Breast Cancer Res Treat 2012;132:793-805.
51. Cyster JG. Chemokines and cell migration in secondary lymphoid organs. Science 1999;286:2098-102.