Analysis of immune cells from human mammary ductal epithelial organoids reveals Vδ2+ T cells that efficiently target breast carcinoma cells in the presence of bisphosphonate

Cancer Prevention Research

Volumn 9, Issue 4, 2016, Pages 305-316

  Zumwalde, Nicholas A ^a,b   Haag, Jill D ^b   Sharma, Deepak ^b,c   Mirrielees, Jennifer A ^a   Wilke, Lee G ^a   Gould, Michael N ^b   Gumperz, Jenny E ^a,d  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c BHABHA ATOMIC RESEARCH CENTRE   (India)

^d NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BISPHOSPHONIC ACID DERIVATIVE; CD103 ANTIGEN; CD27 ANTIGEN; CD31 ANTIGEN; CD45 ANTIGEN; CD45RO ANTIGEN; EPITHELIAL CELL ADHESION MOLECULE; GAMMA INTERFERON; NATURAL KILLER CELL RECEPTOR NKG2D; ZOLEDRONIC ACID; IFNG PROTEIN, HUMAN; IMIDAZOLE DERIVATIVE;

ARTICLE; BREAST; BREAST CARCINOMA; BREAST EPITHELIUM; CD8+ T LYMPHOCYTE; CYTOPLASM; CYTOTOXICITY; FLOW CYTOMETRY; GAMMA DELTA T LYMPHOCYTE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IMMUNOSURVEILLANCE; MEMORY T LYMPHOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRIPLE NEGATIVE BREAST CANCER; CARCINOMA, INTRADUCTAL, NONINFILTRATING; CELL TRANSFORMATION; CYTOLOGY; DRUG EFFECTS; FEMALE; IMMUNOLOGY; MAMMARY GLAND; METABOLISM; PRIMARY CELL CULTURE; T LYMPHOCYTE; TUMOR CELL LINE;

CARCINOMA, INTRADUCTAL, NONINFILTRATING; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DIPHOSPHONATES; FEMALE; HUMANS; IMIDAZOLES; IMMUNOLOGIC SURVEILLANCE; INTERFERON-GAMMA; MAMMARY GLANDS, HUMAN; ORGANOIDS; PRIMARY CELL CULTURE; T-LYMPHOCYTES;

EID: 84964031111     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-15-0370-T     Document Type: Article

References (47)

1. Gould MN. The utility of comparative genetics to inform breast cancer prevention strategies. Genetics 2009;183:409-12.
2. Smits BM, Sharma D, Samuelson DJ, Woditschka S, Mau B, Haag JD, et al. The non-protein coding breast cancer susceptibility locus Mcs5a acts in a non-mammary cell-autonomous fashion through the immune system and modulates T-cell homeostasis and functions. Breast Cancer Res 2011;13: R81.
3. Smyth MJ, Dunn GP, Schreiber RD. Cancer immunosurveillance and immunoediting: the roles of immunity in suppressing tumor development and shaping tumor immunogenicity. Adv Immunol 2006;90:1-50.
4. Visvader JE. Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis. Genes Dev 2009;23:2563-77.
5. Ruffell B, Au A, Rugo HS, Esserman LJ, Hwang ES, Coussens LM. Leukocyte composition of human breast cancer. Proc Natl Acad Sci U S A 2012; 109:2796-801.
6. Huo CW, Chew G, Hill P, Huang D, Ingman W, Hodson L, et al. High mammographic density is associated with an increase in stromal collagen and immune cells within the mammary epithelium. Breast Cancer Res 2015;17:79.
7. Degnim AC, Brahmbhatt RD, Radisky DC, Hoskin TL, Stallings-Mann M, Laudenschlager M, et al. Immune cell quantitation in normal breast tissue lobules with and without lobulitis. Breast Cancer Res Treat 2014;144: 539-49.
8. Hussein MR, Hassan HI. Analysis of the mononuclear inflammatory cell infiltrate in the normal breast, benign proliferative breast disease, in situ and infiltrating ductal breast carcinomas: preliminary observations. J Clin Pathol 2006;59:972-7.
9. Sandstrom A, Peigne CM, Leger A, Crooks JE, Konczak F, Gesnel MC, et al. The intracellular B30.2 domain of butyrophilin 3A1 binds phosphoantigens to mediate activation of human Vgamma9Vdelta2 T cells. Immunity 2014;40:490-500.
10. Wang H, Henry O, Distefano MD, Wang YC, Raikkonen J, Monkkonen J, et al. Butyrophilin 3A1 plays an essential role in prenyl pyrophosphate stimulation of human Vgamma2Vdelta2 T cells. J Immunol 2013;191: 1029-42.
11. Gober HJ, Kistowska M, Angman L, Jeno P, Mori L, De Libero G. Human T cell receptor gammadelta cells recognize endogenous mevalonate metabolites in tumor cells. J Exp Med 2003;197:163-8.
12. Bukowski JF, Morita CT, Tanaka Y, Bloom BR, Brenner MB, Band H. V gamma 2V delta 2 TCR-dependent recognition of non-peptide antigens and Daudi cells analyzed by TCR gene transfer. J Immunol 1995;154: 998-1006.
13. Bukowski JF, Morita CT, Band H, Brenner MB. Crucial role of TCR gamma chain junctional region in prenyl pyrophosphate antigen recognition by gamma delta T cells. J Immunol 1998;161:286-93.
14. Morita CT, Jin C, Sarikonda G, Wang H. Nonpeptide antigens, presentation mechanisms, and immunological memory of human Vgamma2Vdelta2 T cells: discriminating friend from foe through the recognition of prenyl pyrophosphate antigens. Immunol Rev 2007;215:59-76.
15. Dieli F, Gebbia N, Poccia F, Caccamo N, Montesano C, Fulfaro F, et al. Induction of gammadelta T-lymphocyte effector functions by bisphosphonate zoledronic acid in cancer patients in vivo. Blood 2003;102: 2310-1.
16. Winter MC, Holen I, Coleman RE. Exploring the anti-tumour activity of bisphosphonates in early breast cancer. Cancer Treat Rev 2008;34:453-75.
17. Gnant M, Mlineritsch B, Schippinger W, Luschin-Ebengreuth G, Postlberger S, Menzel C, et al. Endocrine therapy plus zoledronic acid in premenopausal breast cancer. N Engl J Med 2009;360:679-91.
18. Eidtmann H, de Boer R, Bundred N, Llombart-Cussac A, Davidson N, Neven P, et al. Efficacy of zoledronic acid in postmenopausal women with early breast cancer receiving adjuvant letrozole: 36-month results of the ZO-FAST Study. Ann Oncol 2010;21:2188-94.
19. Chlebowski RT, Col N. Bisphosphonates and breast cancer incidence and recurrence. Breast Dis 2011;33:93-101.
20. Coleman R, Powles T, Paterson A, Gnant M, Anderson S, Diel I, et al. Adjuvant bisphosphonate treatment in early breast cancer: meta-analyses of individual patient data from randomised trials. Lancet 2015;386: 1353-61.
21. Hue TF, Cummings SR, Cauley JA, Bauer DC, Ensrud KE, Barrett-Connor E, et al. Effect of bisphosphonate use on risk of postmenopausal breast cancer: results from the randomized clinical trials of alendronate and zoledronic acid. JAMA Intern Med 2014;174:1550-7.
22. Proia DA, Kuperwasser C. Reconstruction of human mammary tissues in a mouse model. Nat Protoc 2006;1:206-14.
23. Labarge MA, Garbe JC, Stampfer MR. Processing of human reduction mammoplasty and mastectomy tissues for cell culture. J Visual Exp 2013 Jan 3;pii:50011. doi: 10.3791/50011.
24. Sharma D, Smits BM, Eichelberg MR, Meilahn AL, Muelbl MJ, Haag JD, et al. Quantification of epithelial cell differentiation in mammary glands and carcinomas from DMBA-and MNU-exposed rats. PLoS One 2011;6: e26145.
25. Keller PJ, Arendt LM, Skibinski A, Logvinenko T, Klebba I, Dong S, et al. Defining the cellular precursors to human breast cancer. Proc Natl Acad Sci U S A 2012;109:2772-7.
26. Arendt LM, Keller PJ, Skibinski A, Goncalves K, Naber SP, Buchsbaum RJ, et al. Anatomical localization of progenitor cells in human breast tissue reveals enrichment of uncommitted cells within immature lobules. Breast Cancer Res 2014;16:453.
27. Ishikawa H, Naito T, Iwanaga T, Takahashi-Iwanaga H, Suematsu M, Hibi T, et al. Curriculum vitae of intestinal intraepithelial T cells: their developmental and behavioral characteristics. Immunol Rev 2007;215: 154-65.
28. Ochsenbein AF, Riddell SR, Brown M, Corey L, Baerlocher GM, Lansdorp PM, et al. CD27 expression promotes long-term survival of functional effector-memory CD8+ cytotoxic T lymphocytes in HIV-infected patients. J Exp Med 2004;200:1407-17.
29. Kuss I, Donnenberg AD, Gooding W, Whiteside TL. Effector CD8+CD45RO-CD27-T cells have signalling defects in patients with squamous cell carcinoma of the head and neck. Br J Cancer 2003; 88:223-30.
30. Cepek KL, Shaw SK, Parker CM, Russell GJ, Morrow JS, Rimm DL, et al. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature 1994;372:190-3.
31. Thompson K, Roelofs AJ, Jauhiainen M, Monkkonen H, Monkkonen J, Rogers MJ. Activation of gammadelta T cells by bisphosphonates. Adv Exp Med Biol 2010;658:11-20.
32. Benevides L, da Fonseca DM, Donate PB, Tiezzi DG, De Carvalho DD, de Andrade JM, et al. IL17 promotes mammary tumor progression by changing the behavior of tumor cells and eliciting tumorigenic neutrophils recruitment. Cancer Res. 2015;75:3788-99.
33. Wrobel P, Shojaei H, Schittek B, Gieseler F, Wollenberg B, Kalthoff H, et al. Lysis of a broad range of epithelial tumour cells by human gamma delta T cells: involvement of NKG2D ligands and T-cell receptor-versus NKG2Ddependent recognition. Scand J Immunol 2007;66:320-8.
34. Benzaid I, Monkkonen H, Stresing V, Bonnelye E, Green J, Monkkonen J, et al. High phosphoantigen levels in bisphosphonate-treated human breast tumors promote Vgamma9Vdelta2 T-cell chemotaxis and cytotoxicity in vivo. Cancer Res 2011;71:4562-72.
35. Girardi M, Oppenheim DE, Steele CR, Lewis JM, Glusac E, Filler R, et al. Regulation of cutaneous malignancy by gammadelta T cells. Science 2001;294:605-9.
36. Liu Z, Eltoum IE, Guo B, Beck BH, Cloud GA, Lopez RD. Protective immunosurveillance and therapeutic antitumor activity of gammadelta T cells demonstrated in a mouse model of prostate cancer. J Immunol 2008;180:6044-53.
37. Strid J, Roberts SJ, Filler RB, Lewis JM, Kwong BY, Schpero W, et al. Acute upregulation of anNKG2Dligand promotes rapid reorganization of a local immune compartment with pleiotropic effects on carcinogenesis. Nat Immunol 2008;9:146-54.
38. Gertner-Dardenne J, Castellano R, Mamessier E, Garbit S, Kochbati E, Etienne A, et al.Human Vgamma9Vdelta2 T cells specifically recognize and kill acute myeloid leukemic blasts. J Immunol 2012;188:4701-8.
39. D'Asaro M, La Mendola C, Di Liberto D, Orlando V, Todaro M, Spina M, et al. V gamma 9V delta 2 T lymphocytes efficiently recognize and kill zoledronate-sensitized, imatinib-sensitive, and imatinib-resistant chronic myelogenous leukemia cells. J Immunol 2010;184:3260-8.
40. Coffelt SB, Kersten K, Doornebal CW, Weiden J, Vrijland K, Hau CS, et al. IL-17-producing gammadelta T cells and neutrophils conspire to promote breast cancer metastasis. Nature 2015;522:345-8.
41. Ma C, Zhang Q, Ye J, Wang F, Zhang Y, Wevers E, et al. Tumor-infiltrating gammadelta T lymphocytes predict clinical outcome in human breast cancer. J Immunol 2012;189:5029-36.
42. GirardiM. Immunosurveillance and immunoregulation by gammadelta T cells. J Invest Dermatol 2006;126:25-31.
43. Wang H, Sarikonda G, Puan KJ, Tanaka Y, Feng J, Giner JL, et al. Indirect stimulation of human Vgamma2Vdelta2 T cells through alterations in isoprenoid metabolism. J Immunol 2011;187:5099-113.
44. Knight A, Mackinnon S, Lowdell MW. Human Vdelta1 gamma-delta T cells exert potent specific cytotoxicity against primary multiple myeloma cells. Cytotherapy 2012;14:1110-8.
45. Meeh PF, King M, O'Brien RL, Muga S, Buckhalts P, Neuberg R, et al. Characterization of the gammadelta T cell response to acute leukemia. Cancer Immunol Immunother 2006;55:1072-80.
46. Luoma AM, Castro CD, Mayassi T, Bembinster LA, Bai L, Picard D, et al. Crystal structure of Vdelta1 T cell receptor in complex with CD1d-sulfatide shows MHC-like recognition of a self-lipid by human gammadelta T cells. Immunity 2013;39:1032-42.
47. Gapin L. Check MAIT. J Immunol 2014;192:4475-80.