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CD96 Is an Immune Checkpoint That Regulates CD8+ T-cell Antitumor Function.

Mittal D, Lepletier A, Madore J, Aguilera AR, Stannard K, Blake SJ, Whitehall VLJ, Liu C, Bettington ML, Takeda K, Long GV, Scolyer RA, Lan R, Siemers N, Korman A, Teng MWL, Johnston RJ, Dougall WC, Smyth MJ.

Cancer Immunol Res. 2019 Apr;7(4):559-571. doi: 10.1158/2326-6066.CIR-18-0637. Epub 2019 Mar 20.


An observational study of concomitant immunotherapies and denosumab in patients with advanced melanoma or lung cancer.

Liede A, Hernandez RK, Wade SW, Bo R, Nussbaum NC, Ahern E, Dougall WC, Smyth MJ.

Oncoimmunology. 2018 Sep 5;7(12):e1480301. doi: 10.1080/2162402X.2018.1480301. eCollection 2018.


Roles of the RANKL-RANK axis in antitumour immunity - implications for therapy.

Ahern E, Smyth MJ, Dougall WC, Teng MWL.

Nat Rev Clin Oncol. 2018 Nov;15(11):676-693. doi: 10.1038/s41571-018-0095-y. Review.


The immune checkpoint CD96 defines a distinct lymphocyte phenotype and is highly expressed on tumor-infiltrating T cells.

Lepletier A, Lutzky VP, Mittal D, Stannard K, Watkins TS, Ratnatunga CN, Smith C, McGuire HM, Kemp RA, Mukhopadhyay P, Waddell N, Smyth MJ, Dougall WC, Miles JJ.

Immunol Cell Biol. 2019 Feb;97(2):152-164. doi: 10.1111/imcb.12205. Epub 2018 Oct 17.


Receptor activator of NF-κB (RANK)-mediated induction of metastatic spread and association with poor prognosis in renal cell carcinoma.

Steven A, Leisz S, Fussek S, Nowroozizadeh B, Huang J, Branstetter D, Dougall WC, Burchardt M, Belldegrun AS, Seliger B, Pantuck A, Kroeger N.

Urol Oncol. 2018 Nov;36(11):502.e15-502.e24. doi: 10.1016/j.urolonc.2018.07.013. Epub 2018 Aug 28.


TIGIT immune checkpoint blockade restores CD8+ T-cell immunity against multiple myeloma.

Guillerey C, Harjunpää H, Carrié N, Kassem S, Teo T, Miles K, Krumeich S, Weulersse M, Cuisinier M, Stannard K, Yu Y, Minnie SA, Hill GR, Dougall WC, Avet-Loiseau H, Teng MWL, Nakamura K, Martinet L, Smyth MJ.

Blood. 2018 Oct 18;132(16):1689-1694. doi: 10.1182/blood-2018-01-825265. Epub 2018 Jul 9.


Deficiency of host CD96 and PD-1 or TIGIT enhances tumor immunity without significantly compromising immune homeostasis.

Harjunpää H, Blake SJ, Ahern E, Allen S, Liu J, Yan J, Lutzky V, Takeda K, Aguilera AR, Guillerey C, Mittal D, Li XY, Dougall WC, Smyth MJ, Teng MWL.

Oncoimmunology. 2018 Mar 26;7(7):e1445949. doi: 10.1080/2162402X.2018.1445949. eCollection 2018.


RANKL blockade improves efficacy of PD1-PD-L1 blockade or dual PD1-PD-L1 and CTLA4 blockade in mouse models of cancer.

Ahern E, Harjunpää H, O'Donnell JS, Allen S, Dougall WC, Teng MWL, Smyth MJ.

Oncoimmunology. 2018 Feb 14;7(6):e1431088. doi: 10.1080/2162402X.2018.1431088. eCollection 2018.


CD155 loss enhances tumor suppression via combined host and tumor-intrinsic mechanisms.

Li XY, Das I, Lepletier A, Addala V, Bald T, Stannard K, Barkauskas D, Liu J, Aguilera AR, Takeda K, Braun M, Nakamura K, Jacquelin S, Lane SW, Teng MW, Dougall WC, Smyth MJ.

J Clin Invest. 2018 Jun 1;128(6):2613-2625. doi: 10.1172/JCI98769. Epub 2018 May 14.


CD96 targeted antibodies need not block CD96-CD155 interactions to promote NK cell anti-metastatic activity.

Roman Aguilera A, Lutzky VP, Mittal D, Li XY, Stannard K, Takeda K, Bernhardt G, Teng MWL, Dougall WC, Smyth MJ.

Oncoimmunology. 2018 Feb 1;7(5):e1424677. doi: 10.1080/2162402X.2018.1424677. eCollection 2018.


RANK rewires energy homeostasis in lung cancer cells and drives primary lung cancer.

Rao S, Sigl V, Wimmer RA, Novatchkova M, Jais A, Wagner G, Handschuh S, Uribesalgo I, Hagelkruys A, Kozieradzki I, Tortola L, Nitsch R, Cronin SJ, Orthofer M, Branstetter D, Canon J, Rossi J, D'Arcangelo M, Botling J, Micke P, Fleur L, Edlund K, Bergqvist M, Ekman S, Lendl T, Popper H, Takayanagi H, Kenner L, Hirsch FR, Dougall W, Penninger JM.

Genes Dev. 2017 Oct 15;31(20):2099-2112. doi: 10.1101/gad.304162.117. Epub 2017 Nov 8.


Co-administration of RANKL and CTLA4 Antibodies Enhances Lymphocyte-Mediated Antitumor Immunity in Mice.

Ahern E, Harjunpää H, Barkauskas D, Allen S, Takeda K, Yagita H, Wyld D, Dougall WC, Teng MWL, Smyth MJ.

Clin Cancer Res. 2017 Oct 1;23(19):5789-5801. doi: 10.1158/1078-0432.CCR-17-0606. Epub 2017 Jun 20.


Poor prognosis of patients with triple-negative breast cancer can be stratified by RANK and RANKL dual expression.

Reyes ME, Fujii T, Branstetter D, Krishnamurthy S, Masuda H, Wang X, Reuben JM, Woodward WA, Edwards BJ, Hortobagyi GN, Tripathy D, Dougall WC, Eckhardt BL, Ueno NT.

Breast Cancer Res Treat. 2017 Jul;164(1):57-67. doi: 10.1007/s10549-017-4233-5. Epub 2017 Apr 17.


TIGIT and CD96: new checkpoint receptor targets for cancer immunotherapy.

Dougall WC, Kurtulus S, Smyth MJ, Anderson AC.

Immunol Rev. 2017 Mar;276(1):112-120. doi: 10.1111/imr.12518. Review.


Distribution of RANK and RANK Ligand in Normal Human Tissues as Determined by an Optimized Immunohistochemical Method.

Taylor CR, Branstetter D, Manna E, Dougall WC, Bussiere J, Johnson CW.

Appl Immunohistochem Mol Morphol. 2017 May/Jun;25(5):299-307. doi: 10.1097/PAI.0000000000000503.


Molecular Pathways: Targeting CD96 and TIGIT for Cancer Immunotherapy.

Blake SJ, Dougall WC, Miles JJ, Teng MW, Smyth MJ.

Clin Cancer Res. 2016 Nov 1;22(21):5183-5188. Epub 2016 Sep 12. Review.


RANK and RANK ligand expression in primary human osteosarcoma.

Branstetter D, Rohrbach K, Huang LY, Soriano R, Tometsko M, Blake M, Jacob AP, Dougall WC.

J Bone Oncol. 2015 Jul 29;4(3):59-68. doi: 10.1016/j.jbo.2015.06.002. eCollection 2015 Sep.


RANK Signaling Blockade Reduces Breast Cancer Recurrence by Inducing Tumor Cell Differentiation.

Yoldi G, Pellegrini P, Trinidad EM, Cordero A, Gomez-Miragaya J, Serra-Musach J, Dougall WC, Muñoz P, Pujana MA, Planelles L, González-Suárez E.

Cancer Res. 2016 Oct 1;76(19):5857-5869. Epub 2016 Aug 1.


RANK ligand as a potential target for breast cancer prevention in BRCA1-mutation carriers.

Nolan E, Vaillant F, Branstetter D, Pal B, Giner G, Whitehead L, Lok SW, Mann GB; Kathleen Cuningham Foundation Consortium for Research into Familial Breast Cancer (kConFab), Rohrbach K, Huang LY, Soriano R, Smyth GK, Dougall WC, Visvader JE, Lindeman GJ.

Nat Med. 2016 Aug;22(8):933-9. doi: 10.1038/nm.4118. Epub 2016 Jun 20.


Rankl Impairs Lactogenic Differentiation Through Inhibition of the Prolactin/Stat5 Pathway at Midgestation.

Cordero A, Pellegrini P, Sanz-Moreno A, Trinidad EM, Serra-Musach J, Deshpande C, Dougall WC, Pujana MA, González-Suárez E.

Stem Cells. 2016 Apr;34(4):1027-39. doi: 10.1002/stem.2271. Epub 2016 Jan 13.


Osteoprotegerin (OPG), The Endogenous Inhibitor of Receptor Activator of NF-κB Ligand (RANKL), is Dysregulated in BRCA Mutation Carriers.

Widschwendter M, Burnell M, Fraser L, Rosenthal AN, Philpott S, Reisel D, Dubeau L, Cline M, Pan Y, Yi PC, Gareth Evans D, Jacobs IJ, Menon U, Wood CE, Dougall WC.

EBioMedicine. 2015 Sep 9;2(10):1331-9. doi: 10.1016/j.ebiom.2015.08.037. eCollection 2015 Oct.


Aberrant Activation of the RANK Signaling Receptor Induces Murine Salivary Gland Tumors.

Szwarc MM, Kommagani R, Jacob AP, Dougall WC, Ittmann MM, Lydon JP.

PLoS One. 2015 Jun 10;10(6):e0128467. doi: 10.1371/journal.pone.0128467. eCollection 2015.


RANK-ligand (RANKL) expression in young breast cancer patients and during pregnancy.

Azim HA Jr, Peccatori FA, Brohée S, Branstetter D, Loi S, Viale G, Piccart M, Dougall WC, Pruneri G, Sotiriou C.

Breast Cancer Res. 2015 Feb 21;17:24. doi: 10.1186/s13058-015-0538-7.


Inhibition of leukemia cell engraftment and disease progression in mice by osteoblasts.

Krevvata M, Silva BC, Manavalan JS, Galan-Diez M, Kode A, Matthews BG, Park D, Zhang CA, Galili N, Nickolas TL, Dempster DW, Dougall W, Teruya-Feldstein J, Economides AN, Kalajzic I, Raza A, Berman E, Mukherjee S, Bhagat G, Kousteni S.

Blood. 2014 Oct 30;124(18):2834-46. doi: 10.1182/blood-2013-07-517219. Epub 2014 Aug 18.


RANKL expression in normal and malignant breast tissue responds to progesterone and is up-regulated during the luteal phase.

Hu H, Wang J, Gupta A, Shidfar A, Branstetter D, Lee O, Ivancic D, Sullivan M, Chatterton RT Jr, Dougall WC, Khan SA.

Breast Cancer Res Treat. 2014 Aug;146(3):515-23. doi: 10.1007/s10549-014-3049-9. Epub 2014 Jul 10.


Targeting RANKL in metastasis.

Dougall WC, Holen I, González Suárez E.

Bonekey Rep. 2014 Apr 9;3:519. doi: 10.1038/bonekey.2014.14. eCollection 2014. Review.


RANK expression as a prognostic and predictive marker in breast cancer.

Pfitzner BM, Branstetter D, Loibl S, Denkert C, Lederer B, Schmitt WD, Dombrowski F, Werner M, Rüdiger T, Dougall WC, von Minckwitz G.

Breast Cancer Res Treat. 2014 Jun;145(2):307-15. doi: 10.1007/s10549-014-2955-1. Epub 2014 Apr 16.


RANKL inhibition blocks osteolytic lesions and reduces skeletal tumor burden in models of non-small-cell lung cancer bone metastases.

Miller RE, Jones JC, Tometsko M, Blake ML, Dougall WC.

J Thorac Oncol. 2014 Mar;9(3):345-54. doi: 10.1097/JTO.0000000000000070.


RANK expression on breast cancer cells promotes skeletal metastasis.

Blake ML, Tometsko M, Miller R, Jones JC, Dougall WC.

Clin Exp Metastasis. 2014 Feb;31(2):233-45. doi: 10.1007/s10585-013-9624-3. Epub 2013 Nov 24.


Progestin effects on cell proliferation pathways in the postmenopausal mammary gland.

Wood CE, Branstetter D, Jacob AP, Cline JM, Register TC, Rohrbach K, Huang LY, Borgerink H, Dougall WC.

Breast Cancer Res. 2013;15(4):R62.


Constitutive activation of RANK disrupts mammary cell fate leading to tumorigenesis.

Pellegrini P, Cordero A, Gallego MI, Dougall WC, Muñoz P, Pujana MA, Gonzalez-Suarez E.

Stem Cells. 2013 Sep;31(9):1954-65. doi: 10.1002/stem.1454. Erratum in: Stem Cells. 2014 Apr;32(4):1057. Purificación, Muñoz [corrected to Muñoz, Purificación]. Stem Cells. 2014 Feb;32(2):600. Pasquale, Pellegrini [corrected to Pellegrini, Pasquale]; Alex, Cordero [corrected to Cordero, Alex]; Marta Ines, Gallego [corrected to Gallego, Marta Ines ]; William, Dougall C [corrected to Dougall, William C]; Miguel Angel, Pujana [corrected to Pujana,.


Progesterone/RANKL is a major regulatory axis in the human breast.

Tanos T, Sflomos G, Echeverria PC, Ayyanan A, Gutierrez M, Delaloye JF, Raffoul W, Fiche M, Dougall W, Schneider P, Yalcin-Ozuysal O, Brisken C.

Sci Transl Med. 2013 Apr 24;5(182):182ra55. doi: 10.1126/scitranslmed.3005654.


RANKL inhibition combined with tamoxifen treatment increases anti-tumor efficacy and prevents tumor-induced bone destruction in an estrogen receptor-positive breast cancer bone metastasis model.

Canon J, Bryant R, Roudier M, Branstetter DG, Dougall WC.

Breast Cancer Res Treat. 2012 Oct;135(3):771-80. doi: 10.1007/s10549-012-2222-2. Epub 2012 Aug 29.


The development of denosumab for the treatment of diseases of bone loss and cancer-induced bone destruction.

Goessl C, Katz L, Dougall WC, Kostenuik PJ, Zoog HB, Braun A, Dansey R, Wagman RB.

Ann N Y Acad Sci. 2012 Aug;1263:29-40. doi: 10.1111/j.1749-6632.2012.06674.x. Epub 2012 Jul 25. Review.


Bench to bedside: elucidation of the OPG-RANK-RANKL pathway and the development of denosumab.

Lacey DL, Boyle WJ, Simonet WS, Kostenuik PJ, Dougall WC, Sullivan JK, San Martin J, Dansey R.

Nat Rev Drug Discov. 2012 May;11(5):401-19. doi: 10.1038/nrd3705. Review.


RANK induces epithelial-mesenchymal transition and stemness in human mammary epithelial cells and promotes tumorigenesis and metastasis.

Palafox M, Ferrer I, Pellegrini P, Vila S, Hernandez-Ortega S, Urruticoechea A, Climent F, Soler MT, Muñoz P, Viñals F, Tometsko M, Branstetter D, Dougall WC, González-Suárez E.

Cancer Res. 2012 Jun 1;72(11):2879-88. doi: 10.1158/0008-5472.CAN-12-0044. Epub 2012 Apr 10.


Molecular pathways: osteoclast-dependent and osteoclast-independent roles of the RANKL/RANK/OPG pathway in tumorigenesis and metastasis.

Dougall WC.

Clin Cancer Res. 2012 Jan 15;18(2):326-35. doi: 10.1158/1078-0432.CCR-10-2507. Epub 2011 Oct 26.


Combined inhibition of the BMP pathway and the RANK-RANKL axis in a mixed lytic/blastic prostate cancer lesion.

Virk MS, Alaee F, Petrigliano FA, Sugiyama O, Chatziioannou AF, Stout D, Dougall WC, Lieberman JR.

Bone. 2011 Mar 1;48(3):578-87. doi: 10.1016/j.bone.2010.11.003. Epub 2010 Nov 10.


RANK ligand mediates progestin-induced mammary epithelial proliferation and carcinogenesis.

Gonzalez-Suarez E, Jacob AP, Jones J, Miller R, Roudier-Meyer MP, Erwert R, Pinkas J, Branstetter D, Dougall WC.

Nature. 2010 Nov 4;468(7320):103-7. doi: 10.1038/nature09495. Epub 2010 Sep 29.


Inhibition of RANKL increases the anti-tumor effect of the EGFR inhibitor panitumumab in a murine model of bone metastasis.

Canon J, Bryant R, Roudier M, Osgood T, Jones J, Miller R, Coxon A, Radinsky R, Dougall WC.

Bone. 2010 Jun;46(6):1613-9. doi: 10.1016/j.bone.2010.03.001. Epub 2010 Mar 6.


Combined therapy with the RANKL inhibitor RANK-Fc and rhApo2L/TRAIL/dulanermin reduces bone lesions and skeletal tumor burden in a model of breast cancer skeletal metastasis.

Holland PM, Miller R, Jones J, Douangpanya H, Piasecki J, Roudier M, Dougall WC.

Cancer Biol Ther. 2010 Apr 1;9(7):539-50. Epub 2010 Apr 1.


Denosumab, a fully human monoclonal antibody to RANKL, inhibits bone resorption and increases BMD in knock-in mice that express chimeric (murine/human) RANKL.

Kostenuik PJ, Nguyen HQ, McCabe J, Warmington KS, Kurahara C, Sun N, Chen C, Li L, Cattley RC, Van G, Scully S, Elliott R, Grisanti M, Morony S, Tan HL, Asuncion F, Li X, Ominsky MS, Stolina M, Dwyer D, Dougall WC, Hawkins N, Boyle WJ, Simonet WS, Sullivan JK.

J Bone Miner Res. 2009 Feb;24(2):182-95. doi: 10.1359/jbmr.081112.


Influence of simultaneous targeting of the bone morphogenetic protein pathway and RANK/RANKL axis in osteolytic prostate cancer lesion in bone.

Virk MS, Petrigliano FA, Liu NQ, Chatziioannou AF, Stout D, Kang CO, Dougall WC, Lieberman JR.

Bone. 2009 Jan;44(1):160-7. doi: 10.1016/j.bone.2008.09.009. Epub 2008 Sep 26.


RANKL signaling in bone physiology and cancer.

Dougall WC.

Curr Opin Support Palliat Care. 2007 Dec;1(4):317-22. doi: 10.1097/SPC.0b013e3282f335be. Review.


RANK ligand inhibition plus docetaxel improves survival and reduces tumor burden in a murine model of prostate cancer bone metastasis.

Miller RE, Roudier M, Jones J, Armstrong A, Canon J, Dougall WC.

Mol Cancer Ther. 2008 Jul;7(7):2160-9. doi: 10.1158/1535-7163.MCT-08-0046. Epub 2008 Jul 7.


RANKL inhibition is an effective adjuvant for docetaxel in a prostate cancer bone metastases model.

Ignatoski KM, Escara-Wilke JF, Dai JL, Lui A, Dougall W, Daignault S, Yao Z, Zhang J, Day ML, Sargent EE, Keller ET.

Prostate. 2008 Jun 1;68(8):820-9. doi: 10.1002/pros.20744.


Inhibition of RANKL blocks skeletal tumor progression and improves survival in a mouse model of breast cancer bone metastasis.

Canon JR, Roudier M, Bryant R, Morony S, Stolina M, Kostenuik PJ, Dougall WC.

Clin Exp Metastasis. 2008;25(2):119-29. Epub 2007 Dec 5.


RANKL acts directly on RANK-expressing prostate tumor cells and mediates migration and expression of tumor metastasis genes.

Armstrong AP, Miller RE, Jones JC, Zhang J, Keller ET, Dougall WC.

Prostate. 2008 Jan 1;68(1):92-104.


RANKL inhibition: from mice to men (and women).

Stolina M, Kostenuik PJ, Dougall WC, Fitzpatrick LA, Zack DJ.

Adv Exp Med Biol. 2007;602:143-50. Review.


RANK ligand as a therapeutic target for bone metastases and multiple myeloma.

Roodman GD, Dougall WC.

Cancer Treat Rev. 2008 Feb;34(1):92-101. Epub 2007 Oct 26. Review.


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