2,272
Views
9
CrossRef citations to date
0
Altmetric
Review

The role of trogocytosis in immune surveillance of Hodgkin lymphoma

&
Article: 1781334 | Received 11 May 2020, Accepted 03 Jun 2020, Published online: 17 Jun 2020

References

  • Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA. 2018;68:394–7.
  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin. 2019;69:7–34.
  • Kuppers R, Hansmann ML. The Hodgkin and Reed/Sternberg cell. Int J Biochem Cell Biol. 2005;37:511–517.
  • Aldinucci D, Gloghini A, Pinto A, De Filippi R, Carbone A. The classical Hodgkin’s lymphoma microenvironment and its role in promoting tumour growth and immune escape. The J Pathol. 2010;221:248–263.
  • Aldinucci D, Borghese C, Casagrande N. Formation of the immunosuppressive microenvironment of classic hodgkin lymphoma and therapeutic approaches to counter it. int j mol sci. 2019;20:2416.
  • Calabretta E, d’Amore F, Carlo-Stella C. Immune and inflammatory cells of the tumor microenvironment represent novel therapeutic targets in classical hodgkin lymphoma. Int J Mol Sci. 2019;20:5503.
  • Aldinucci D, Celegato M, Casagrande N. Microenvironmental interactions in classical Hodgkin lymphoma and their role in promoting tumor growth, immune escape and drug resistance. Cancer Lett. 2016;380:243–252.
  • Cirillo M, Reinke S, Klapper W, Borchmann S. The translational science of hodgkin lymphoma. Br J Haematol. 2019;184:30–44.
  • Dance A. Core Concept: cells nibble one another via the under-appreciated process of trogocytosis. Proc Nat Acad Sci. 2019;116:17608–17610.
  • Bettadapur A, Miller HW, Ralston KS. B iting off what can be chewed: trogocytosis in health, infection and disease. Infect Immunity. 2020.
  • Soskic B, Qureshi OS, Hou T, Sansom DM. A transendocytosis perspective on the CD28/CTLA-4 pathway. Adv Immunol. 2014;124:95–136.
  • Shanbhag S, Ambinder RF. Hodgkin lymphoma: A review and update on recent progress. CA. 2018;68:116–132.
  • von Tresckow B, Moskowitz CH. Treatment of relapsed and refractory Hodgkin Lymphoma. Semin Hematol. 2016;53:180–185.
  • Renner C, Stenner F. Cancer immunotherapy and the immune response in hodgkin lymphoma. Front Oncol. 2018;8:193.
  • Wang D, Zeng C, Xu B, Xu JH, Wang J, Jiang LJ, Wang QX, Li CR, Wang N, Huang L, et al. Anti-CD30 chimeric antigen receptor T cell therapy for relapsed/refractory CD30+ lymphoma patients. Blood Cancer J. 2020;10:8.
  • Wang CM, Wu ZQ, Wang Y, Guo YL, Dai HR, Wang XH, Li X, Zhang YJ, Zhang WY, Chen MX, et al. Autologous T cells expressing CD30 chimeric antigen receptors for relapsed or refractory hodgkin lymphoma: an open-label phase I trial. Clin Cancer Res. 2017;23:1156–1166.
  • Ramos CA, Ballard B, Zhang H, Dakhova O, Gee AP, Mei Z, Bilgi M, Wu MF, Liu H, Grilley B, et al. Clinical and immunological responses after CD30-specific chimeric antigen receptor-redirected lymphocytes. J Clin Invest. 2017;127:3462–3471.
  • Campana D, Schwarz H, Imai C. 4-1BB chimeric antigen receptors. Cancer J. 2014;20:134–140.
  • Mottok A, Steidl C. Biology of classical Hodgkin lymphoma: implications for prognosis and novel therapies. Blood. 2018;131:1654–1665.
  • Hudrisier D, Joly E. Plasma membrane nibbling: all lymphocytes do it, but why. ELSO Gaz. 2002;9:1–5.
  • Ahmed KA, Munegowda MA, Xie Y, Xiang J. Intercellular trogocytosis plays an important role in modulation of immune responses. Cell Mol Immunol. 2008;5:261–269.
  • Arnold PY, Davidian DK, Mannie MD. Antigen presentation by T cells: T cell receptor ligation promotes antigen acquisition from professional antigen-presenting cells. Eur J Immunol. 1997;27:3198–3205.
  • Li G, Bethune MT, Wong S, Joglekar AV, Leonard MT, Wang JK, Kim JT, Cheng D, Peng S, Zaretsky JM, et al. T cell antigen discovery via trogocytosis. Nat Meth. 2019;16:183–190.
  • LeMaoult J, Caumartin J, Daouya M, Switala M, Rebmann V, Arnulf B, Carosella ED. Trogocytic intercellular membrane exchanges among hematological tumors. J Hematol Oncol. 2015;8:24.
  • Xiang J, Huang H, Liu Y. A new dynamic model of CD8+ T effector cell responses via CD4+ T helper-antigen-presenting cells. J Immunol. 2005;174:7497–7505.
  • He T, Zong S, Wu X, Wei Y, Xiang J. CD4+ T cell acquisition of the bystander pMHC I colocalizing in the same immunological synapse comprising pMHC II and costimulatory CD40, CD54, CD80, OX40L, and 41BBL. Biochemi Biophys Res Com. 2007;362:822–828.
  • Taylor RP, Lindorfer MA. Fcγ-receptor–mediated trogocytosis impacts mAb-based therapies: historical precedence and recent developments. Blood. 2015;125:762–766.
  • Lin A, Yan W-H. Intercellular transfer of HLA-G: its potential in cancer immunology. Clin Transl Immunol. 2019;8:e1077.
  • Drenkard D, Becke FM, Langstein J, Spruss T, Kunz-Schughart LA, Tan TE, Lim YC, Schwarz H. CD137 is expressed on blood vessel walls at sites of inflammation and enhances monocyte migratory activity. Faseb J. 2007;21:456–463.
  • Anderson MW, Zhao S, Freud AG, Czerwinski DK, Kohrt H, Alizadeh AA, Houot R, Azambuja D, Biasoli I, Morais JC, et al. CD137 is expressed in follicular dendritic cell tumors and in classical Hodgkin and T-cell lymphomas: diagnostic and therapeutic implications. Am J Pathol. 2012;181:795–803.
  • Broll K, Richter G, Pauly S, Hofstaedter F, Schwarz H. CD137 expression in tumor vessel walls. High correlation with malignant tumors. Am J Clin Pathol. 2001;115:543–549.
  • Schwarz H, Valbracht J, Tuckwell J, von Kempis J, Lotz M. ILA, the human 4-1BB homologue, is inducible in lymphoid and other cell lineages. Blood. 1995;85:1043–1052.
  • Melero I, Shuford WW, Newby SA, Aruffo A, Ledbetter JA, Hellstrom KE, Mittler RS, Chen L. Monoclonal antibodies against the 4-1BB T-cell activation molecule eradicate established tumors. Nat Med. 1997;3:682–685.
  • Dharmadhikari B, Wu M, Abdullah NS, Rajendran S, Ishak ND, Nickles E, Harfuddin Z, Schwarz H. CD137 and CD137L signals are main drivers of type 1, cell-mediated immune responses. Oncoimmunol. 2016;5:e1113367.
  • Thum E, Shao Z, Schwarz H. CD137, implications in immunity and potential for therapy. Front Biosci. 2009;14:4173–4188.
  • Chu D-T, Bac ND, Nguyen K-H, Tien NLB, Thanh VV, Nga VT, Ngoc VTN, Anh Dao DT, Hoan LN, Hung NP, et al. An update on anti-CD137 antibodies in immunotherapies for cancer. Int J Mol Sci. 2019;20:1822.
  • Weinkove R, George P, Dasyam N, McLellan AD. Selecting costimulatory domains for chimeric antigen receptors: functional and clinical considerations. Clin Transl Immunol. 2019;8:e1049–e.
  • Zhang H, Merchant MS, Chua KS, Khanna C, Helman LJ, Telford B, Ward Y, Summers J, Toretsky J, Thomas EK, et al. Tumor expression of 4-1BB ligand sustains tumor lytic T cells. Cancer Biol Ther. 2003;2:579–586.
  • Guinn BA, DeBenedette MA, Watts TH, Berinstein NL. 4-1BBL cooperates with B7-1 and B7-2 in converting a B cell lymphoma cell line into a long-lasting antitumor vaccine. J Immunol. 1999;162:5003–5010.
  • Labiano S, Palazon A, Bolanos E, Azpilikueta A, Sanchez-Paulete AR, Morales-Kastresana A, Quetglas JI, Perez-Gracia JL, Gurpide A, Rodriguez-Ruiz M, et al. Hypoxia-induced soluble CD137 in malignant cells blocks CD137L-costimulation as an immune escape mechanism. Oncoimmunol. 2016;5:e1062967.
  • Furtner M, Straub RH, Kruger S, Schwarz H. Levels of soluble CD137 are enhanced in sera of leukemia and lymphoma patients and are strongly associated with chronic lymphocytic leukemia. Leukemia. 2005;19:883–885.
  • Zeng Q, Gupta A, Xin L, Poon M, Schwarz H. plasma factors for the differentiation of hodgkin’s lymphoma and diffused large B cell lymphoma and for monitoring remission. J Hematol. 2019;8:47–54.
  • Ho WT, Pang WL, Chong SM, Castella A, Al-Salam S, Tan TE, Moh MC, Koh LK, Gan SU, Cheng CK, et al. Expression of CD137 on hodgkin and reed-sternberg cells inhibits T-cell activation by eliminating CD137 ligand expression. Cancer Res. 2013;73:652–661.
  • Shi YF, Gao ZF, Liu CL, Huang X, Song YQ, Zhang C, Lin DM, Zhou LX, Zhao M, Lai YM, et al. Expression of CD137 in tumor cells of Hodgkin lymphoma from Northern China and its application in pathological differential diagnosis. Zhonghua Xue Ye Xue Za Zhi. 2016;37:484–490.
  • Rajendran S, Ho WT, Schwarz H. CD137 signaling in Hodgkin and Reed-Sternberg cell lines induces IL-13 secretion, immune deviation and enhanced growth. Oncoimmunol. 2016;5:e1160188.
  • Aravinth SP, Rajendran S, Li Y, Wu M, Yi Wong AH, Schwarz H. Epstein-Barr virus-encoded LMP1 induces ectopic CD137 expression on Hodgkin and Reed-Sternberg cells via the PI3K-AKT-mTOR pathway. Leuk Lymphoma. 2019;60:2697–2704.
  • Shao Z, Harfuddin Z, Pang WL, Nickles E, Koh LK, Schwarz H. Trogocytic CD137 transfer causes an internalization of CD137 ligand on murine APCs leading to reduced T cell costimulation. J Jeukoc Biol. 2015;97:909–919.
  • Zhang X, Voskens CJ, Sallin M, Maniar A, Montes CL, Zhang Y, Lin W, Li G, Burch E, Tan M, et al. CD137 promotes proliferation and survival of human B cells. J Immunol. 2010;184:787–795.
  • Nakaima Y, Watanabe K, Koyama T, Miura O, Fukuda T. CD137 Is Induced by the CD40 signal on chronic lymphocytic leukemia b cells and transduces the survival signal via NF-κB activation. PLoS One. 2013;8:e64425.
  • Izumi KM, McFarland EC, Ting AT, Riley EA, Seed B, Kieff ED. The epstein-barr virus oncoprotein latent membrane protein 1 engages the tumor necrosis factor receptor-associated proteins TRADD and receptor-interacting protein (RIP) but does not induce apoptosis or require RIP for NF-κB activation. Mol Cell Biol. 1999;19:5759–5767.
  • Kaykas A, Worringer K, Sugden B. CD40 and LMP-1 both signal from lipid rafts but LMP-1 assembles a distinct, more efficient signaling complex. Embo J. 2001;20:2641–2654.
  • Lam N, Sugden B. CD40 and its viral mimic, LMP1: similar means to different ends. Cell Signal. 2003;15:9–16.
  • Yoshimori M, Imadome K, Komatsu H, Wang L, Saitoh Y, Yamaoka S, Fukuda T, Kurata M, Koyama T, Shimizu N, et al. CD137 expression is induced by Epstein-Barr virus infection through LMP1 in T or NK cells and mediates survival promoting signals. PLoS One. 2014;9:e112564.
  • Wu M, Wong HY, Lin JL, Moliner A, Schwarz H. Induction of CD137 expression by viral genes reduces T cell costimulation. J Cell Physiol. 2019;234:21076–21088.
  • Somekh I, Thian M, Medgyesi D, Gülez N, Magg T, Gallón Duque A, Stauber T, Lev A, Genel F, Unal E, et al. CD137 deficiency causes immune dysregulation with predisposition to lymphomagenesis. Blood. 2019;134:1510–1516.
  • Alosaimi MF, Hoenig M, Jaber F, Platt CD, Jones J, Wallace J, Debatin K-M, Schulz A, Jacobsen E, Möller P, et al. Immunodeficiency and EBV-induced lymphoproliferation caused by 4-1BB deficiency. J Allergy Clin Immunol. 2019;144:574–83.e5.
  • Rodriguez R, Fournier B, Cordeiro DJ, Winter S, Izawa K, Martin E, Boutboul D, Lenoir C, Fraitag S, Kracker S, et al. Concomitant PIK3CD and TNFRSF9 deficiencies cause chronic active Epstein-Barr virus infection of T cells. J Exp Med. 2019;216:2800–2818.
  • Luu K, Nickles E, Schwarz H. Destroy, what destroys you. Oncoimmunology. 2020;9:1685301.
  • Zheng G, Wang B, Chen A. The 4-1BB Costimulation Augments the Proliferation of CD4+ CD25+ Regulatory T Cells. J Immunol. 2004;173:2428–2434.
  • Nowak A, Lock D, Bacher P, Hohnstein T, Vogt K, Gottfreund J, Giehr P, Polansky JK, Sawitzki B, Kaiser A, et al. CD137+CD154- Expression As a Regulatory T Cell (Treg)-Specific Activation Signature for Identification and Sorting of Stable Human Tregs from In Vitro Expansion Cultures. Front Immunol. 2018;9:199.
  • Tsai YG, Yang KD, Wen YS, Hung CH, Chien JW, Lin CY. Allergen-specific immunotherapy enhances CD8(+) CD25(+) CD137(+) regulatory T cells and decreases nasal nitric oxide. Ped Allergy Immunol. 2019;30:531–539.
  • Kao JK, Hsue YT, Lin CY. Role of new population of peripheral CD11c(+)CD8(+) T cells and CD4(+)CD25(+) regulatory T cells during acute and remission stages in rheumatoid arthritis patients. J Microbiol Immunol Infect. 2007;40:419–427.
  • Guo X, Zhang Y, Zheng L, Zheng C, Song J, Zhang Q, Kang B, Liu Z, Jin L, Xing R, et al. Global characterization of T cells in non-small-cell lung cancer by single-cell sequencing. Nat Med. 2018;24:978–985.
  • Pavlovic A, Glavina Durdov M, Capkun V, Jakelic Pitesa J, Bozic Sakic M. Classical hodgkin lymphoma with positive epstein-barr virus status is associated with more FOXP3 regulatory T cells. Med Sci Mon. 2016;22:2340–2346.
  • van der Weyden CA, Pileri SA, Feldman AL, Whisstock J, Prince HM. Understanding CD30 biology and therapeutic targeting: a historical perspective providing insight into future directions. Blood Cancer J. 2017;7:e603–e.
  • Horie R, Watanabe T, Morishita Y, Ito K, Ishida T, Kanegae Y, Saito I, Higashihara M, Mori S, Kadin ME, et al. Ligand-independent signaling by overexpressed CD30 drives NF-kappaB activation in Hodgkin-reed-sternberg cells. Oncogene. 2002;21:2493–2503.
  • Guo F, Sun A, Wang W, He J, Hou J, Zhou P, Chen Z. TRAF1 is involved in the classical NF-κB activation and CD30-induced alternative activity in Hodgkin’s lymphoma cells. Mol Immunol. 2009;46:2441–2448.
  • Gruss HJ, Boiani N, Williams DE, Armitage RJ, Smith CA, Goodwin RG. Pleiotropic effects of the CD30 ligand on CD30-expressing cells and lymphoma cell lines. Blood. 1994;83:2045–2056.
  • Nakashima M, Watanabe M, Uchimaru K, Horie R. Trogocytosis of ligand–receptor complex and its intracellular transport in CD30 signalling. Biol Cell. 2018;110:109–124.
  • Green MR, Rodig S, Juszczynski P, Ouyang J, Sinha P, O’Donnell E, Neuberg D, Shipp MA. Constitutive AP-1 activity and EBV infection induce PD-L1 in Hodgkin lymphomas and posttransplant lymphoproliferative disorders: implications for targeted therapy. Clin Cancer Res. 2012;18:1611–1618.
  • Yamamoto R, Nishikori M, Kitawaki T, Sakai T, Hishizawa M, Tashima M, Kondo T, Ohmori K, Kurata M, Hayashi T, et al. PD-1-PD-1 ligand interaction contributes to immunosuppressive microenvironment of Hodgkin lymphoma. Blood. 2008;111:3220–3224.
  • Roemer MG, Advani RH, Ligon AH, Natkunam Y, Redd RA, Homer H, Connelly CF, Sun HH, Daadi SE, Freeman GJ, et al. PD-L1 and PD-L2 genetic alterations define classical hodgkin lymphoma and predict outcome. J Clin Oncol. 2016;34:2690–2697.
  • Carey CD, Gusenleitner D, Lipschitz M, Roemer MGM, Stack EC, Gjini E, Hu X, Redd R, Freeman GJ, Neuberg D, et al. Topological analysis reveals a PD-L1-associated microenvironmental niche for reed-sternberg cells in hodgkin lymphoma. Blood. 2017;130:2420–2430.
  • Steidl C, Lee T, Shah SP, Farinha P, Han G, Nayar T, Delaney A, Jones SJ, Iqbal J, Weisenburger DD, et al. Tumor-associated macrophages and survival in classic hodgkin’s lymphoma. New Engl J Med. 2010;362:875–885.
  • Gary R, Voelkl S, Palmisano R, Ullrich E, Bosch JJ, Mackensen A. Antigen-Specific Transfer of Functional Programmed Death Ligand 1 from Human APCs onto CD8+ T Cells via Trogocytosis. J Immunol. 2012;188:744–752.
  • Kawashima M, Carreras J, Higuchi H, Kotaki R, Hoshina T, Okuyama K, Suzuki N, Kakizaki M, Miyatake Y, Ando K, et al. PD-L1/L2 protein levels rapidly increase on monocytes via trogocytosis from tumor cells in classical Hodgkin lymphoma. Leukemia. 2020. doi:10.1038/s41375-020-0737-9
  • Qureshi OS, Zheng Y, Nakamura K, Attridge K, Manzotti C, Schmidt EM, Baker J, Jeffery LE, Kaur S, Briggs Z, et al. Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science (New York, NY). 2011;332:600–603.
  • Gu P, Fang Gao J, D’Souza CA, Kowalczyk A, Chou K-Y, Zhang L. Trogocytosis of CD80 and CD86 by induced regulatory T cells. Cell Mol Immunol. 2012;9:136–146.
  • Bashey A, Medina B, Corringham S, Pasek M, Carrier E, Vrooman L, Lowy I, Solomon SR, Morris LE, Holland HK, et al. CTLA4 blockade with ipilimumab to treat relapse of malignancy after allogeneic hematopoietic cell transplantation. Blood. 2009;113:1581–1588.
  • Davids MS, Kim HT, Bachireddy P, Costello C, Liguori R, Savell A, Lukez AP, Avigan D, Chen Y-B, McSweeney P, et al. Ipilimumab for Patients with Relapse after Allogeneic Transplantation. New Engl J Med. 2016;375:143–153.
  • Zhou H, Fu X, Li Q, Niu T. Safety and efficacy of anti-PD-1 monoclonal antibodies in patients with relapsed or refractory lymphoma: a meta-analysis of prospective clinic trails. Front Pharmacol. 2019;10:387.
  • Rodriguez R, Fournier B, Cordeiro DJ, Winter S, Izawa K, Martin E, Boutboul D, Lenoir C, Fraitag S, Kracker S, et al. Concomitant PIK3CD and TNFRSF9 deficiencies cause chronic active Epstein-Barr virus infection of T cells. J Exp Med. 2019;216:2800–2818.
  • Rajendran S, Li Y, Ngoh E, Wong HY, Cheng MS, Wang CI, Schwarz H. Development of a Bispecific Antibody Targeting CD30 and CD137 on Hodgkin and Reed-Sternberg Cells. Front Oncol. 2019;9:945.
  • Bhatt G, Maddocks K, Christian B. CD30 and CD30-targeted therapies in hodgkin lymphomA AND Other B cell Lymphomas. Cur Hematol Malign Rep. 2016;11:480–491.
  • Hansen HP, Trad A, Dams M, Zigrino P, Moss M, Tator M, Schön G, Grenzi PC, Bachurski D, Aquino B, et al. CD30 on extracellular vesicles from malignant Hodgkin cells supports damaging of CD30 ligand-expressing bystander cells with Brentuximab-Vedotin, in vitro. Oncotarget. 2016;7:30523–30535.
  • Lim SH, Vaughan AT, Ashton-Key M, Williams EL, Dixon SV, Chan HTC, Beers SA, French RR, Cox KL, Davies AJ, et al. Fc gamma receptor IIb on target B cells promotes rituximab internalization and reduces clinical efficacy. Blood. 2011;118:2530–2540.
  • Beum PV, Kennedy AD, Williams ME, Lindorfer MA, Taylor RP. The Shaving Reaction: rituximab/CD20 complexes are removed from mantle cell lymphoma and chronic lymphocytic leukemia cells by THP-1 monocytes. J Immunol. 2006;176:2600–2609.
  • Yang J, Li L, Kopeček J. Biorecognition: A key to drug-free macromolecular therapeutics. Biomaterials. 2019;190–191:11–23.
  • Gardell JL, Parker DC. CD40L is transferred to antigen-presenting B cells during delivery of T-cell help. Eur J Immunol. 2017;47:41–50.
  • Fanale M, Assouline S, Kuruvilla J, Solal-Céligny P, Heo DS, Verhoef G, Corradini P, Abramson JS, Offner F, Engert A, et al. Phase IA/II, multicentre, open-label study of the CD40 antagonistic monoclonal antibody lucatumumab in adult patients with advanced non-Hodgkin or Hodgkin lymphoma. Br J Haematol. 2014;164:258–265.