Impact of (chemo)radiotherapy on immune cell composition and function in cervical cancer patients

References

• Sturdza A, Potter R, Fokdal LU, Haie-Meder C, Tan LT, Mazeron R, Petric P, Segedin B, Jurgenliemk-Schulz IM, Nomden C et al. Image guided brachytherapy in locally advanced cervical cancer: Improved pelvic control and survival in RetroEMBRACE, a multicenter cohort study. Radiother Oncol 2016; 120(3):428-33; PMID:27134181; http://dx.doi.org/S0167-8140(16)31018-0 [pii];10.1016/j.radonc.2016.03.011.
   PubMed Web of Science ®Google Scholar
• Ganss R, Ryschich E, Klar E, Arnold B, Hammerling GJ. Combination of T-cell therapy and trigger of inflammation induces remodeling of the vasculature and tumor eradication. Cancer Res 2002; 62(5):1462-70; PMID:11888921
   PubMed Web of Science ®Google Scholar
• Jain RK. Normalization of tumor vasculature: An emerging concept in antiangiogenic therapy. Science 2005; 307(5706):58-62; PMID:15637262; http://dx.doi.org/10.1126/science.1104819
   PubMed Web of Science ®Google Scholar
• Tartour E, Pere H, Maillere B, Terme M, Merillon N, Taieb J, Sandoval F, Quintin-Colonna F, Lacerda K, Karadimou A et al. Angiogenesis and immunity: A bidirectional link potentially relevant for the monitoring of antiangiogenic therapy and the development of novel therapeutic combination with immunotherapy. Cancer Metastasis Rev 2011; 30(1):83-95; PMID:21249423; http://dx.doi.org/10.1007/s10555-011-9281-4
   PubMed Web of Science ®Google Scholar
• Bhardwaj N. Harnessing the immune system to treat cancer. J Clin Invest 2007; 117(5):1130-6; PMID:17476342; http://dx.doi.org/10.1172/JCI32136
   PubMed Web of Science ®Google Scholar
• Vacchelli E, Vitale I, Tartour E, Eggermont A, Sautes-Fridman C, Galon J, Zitvogel L, Kroemer G, Galluzzi L. Trial watch: Anticancer radioimmunotherapy. Oncoimmunology 2013; 2(9):e25595; PMID:24319634; http://dx.doi.org/10.4161/onci.25595
   PubMed Web of Science ®Google Scholar
• Formenti SC, Demaria S. Combining radiotherapy and cancer immunotherapy: A paradigm shift. J Natl Cancer Inst 2013; 105(4):256-65; PMID:23291374; http://dx.doi.org/10.1093/jnci/djs629
   PubMed Web of Science ®Google Scholar
• Barker HE, Paget JT, Khan AA, Harrington KJ. The tumour microenvironment after radiotherapy: Mechanisms of resistance and recurrence. Nat Rev Cancer 2015; 15(7):409-25; PMID:26105538; http://dx.doi.org/10.1038/nrc3958
   PubMed Web of Science ®Google Scholar
• Choi CH, Kang H, Kim WY, Kim TJ, Lee JW, Huh SJ, Lee JH, Kim BG, Bae DS. Prognostic value of baseline lymphocyte count in cervical carcinoma treated with concurrent chemoradiation. Int J Radiat Oncol Biol Phys 2008; 71(1):199-204; PMID:18037578; http://dx.doi.org/10.1016/j.ijrobp.2007.09.024
   PubMed Web of Science ®Google Scholar
• Hoskin PJ, Rojas AM, Peiris SN, Mullassery V, Chong IY. Pre-treatment haemoglobin and peripheral blood lymphocyte count as independent predictors of outcome in carcinoma of cervix. Clin Oncol (R Coll Radiol) 2014; 26(4):179-84; PMID:24439272; http://dx.doi.org/10.1016/j.clon.2013.11.023
   PubMed Web of Science ®Google Scholar
• Ho GYF, Bierman R, Beardsley L, Chang CJ, Burk RD. Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 1998; 338(7):423-8; PMID:9459645; http://dx.doi.org/10.1056/NEJM199802123380703
   PubMed Web of Science ®Google Scholar
• Gorter A, Prins F, van Diepen M, Punt S, van der Burg SH. The tumor area occupied by Tbet+ cells in deeply invading cervical cancer predicts clinical outcome. J Transl Med 2015; 13:295; PMID:26357849; http://dx.doi.org/10.1186/s12967-015-0664-0
   PubMed Web of Science ®Google Scholar
• Jordanova ES, Gorter A, Ayachi O, Prins F, Durrant LG, Kenter GG, van der Burg SH, Fleuren GJ. Human leukocyte antigen class I, MHC class I chain-related molecule A, and CD8(+)/regulatory T-cell ratio: Which variable determines survival of cervical cancer patients? Clin Cancer Res 2008; 14(7):2028-35; PMID:18381941; http://dx.doi.org/10.1158/1078-0432.CCR-07-4554
   PubMed Web of Science ®Google Scholar
• Piersma SJ, Jordanova ES, van Poelgeest MIE, Kwappenberg KMC, van der Hulst JM, Drijfhout JW, Melief CJM, Kenter GG, Fleuren GJ, Offringa R et al. High number of intraepithelial CD8(+) tumor-infiltrating lymphocytes is associated with the absence of lymph node metastases in patients with large early-stage cervical cancer. Cancer Res 2007; 67(1):354-61; PMID:17210718; http://dx.doi.org/10.1158/0008-5472.CAN-06-3388
   PubMed Web of Science ®Google Scholar
• de Vos van Steenwijk PJ, Ramwadhdoebe TH, Goedemans R, Doorduijn EM, van Ham JJ, Gorter A, van Hall T, Kuijjer ML, van Poelgeest MIE, van der Burg SH et al. Tumor-infiltrating CD14-positive myeloid cells and CD8-positive T-cells prolong survival in patients with cervical carcinoma. Int J Cancer 2013; 133(12):2884-94; PMID:23740735; http://dx.doi.org/10.1002/ijc.28309
   PubMed Web of Science ®Google Scholar
• Karim R, Jordanova ES, Piersma SJ, Kenter GG, Chen LP, Boer JM, Melief CJM, van der Burg SH. Tumor-expressed B7-H1 and B7-DC in relation to PD-1+T-cell infiltration and survival of patients with cervical carcinoma. Clin Cancer Res 2009; 15(20):6341-7; PMID:19825956; http://dx.doi.org/10.1158/1078-0432.CCR-09-1652
   PubMed Web of Science ®Google Scholar
• Peggs KS, Quezada SA, Allison JP. Cell intrinsic mechanisms of T-cell inhibition and application to cancer therapy. Immunol Rev 2008; 224:141-65; PMID:18759925; http://dx.doi.org/10.1111/j.1600-065X.2008.00649.x
   PubMed Web of Science ®Google Scholar
• Chakraborty M, Abrams SI, Coleman CN, Camphausen K, Schlom J, Hodge JW. External beam radiation of tumors alters phenotype of tumor cells to render them susceptible to vaccine-mediated T-cell killing. Cancer Res 2004; 64(12):4328-37; PMID:15205348; http://dx.doi.org/10.1158/0008-5472.CAN-04-0073
   PubMed Web of Science ®Google Scholar
• Lee YJ, Auh SL, Wang YG, Burnette B, Wang Y, Meng YR, Beckett M, Sharma R, Chin R, Tu T et al. Therapeutic effects of ablative radiation on local tumor require CD8(+) T cells: changing strategies for cancer treatment. Blood 2009; 114(3):589-95; PMID:19349616; http://dx.doi.org/10.1182/blood-2009-02-206870
   PubMed Web of Science ®Google Scholar
• Tseng CW, Trimble C, Zeng Q, Monie A, Alvarez RD, Huh WK, Hoory T, Wang MC, Hung CF, Wu TC. Low-dose radiation enhances therapeutic HPV DNA vaccination in tumor-bearing hosts. Cancer Immunol Immunother 2009; 58(5):737-48; PMID:18815785; http://dx.doi.org/10.1007/s00262-008-0596-0
   PubMed Web of Science ®Google Scholar
• Mizunuma M, Yokoyama Y, Futagami M, Aoki M, Takai Y, Mizunuma H. The pretreatment neutrophil-to-lymphocyte ratio predicts therapeutic response to radiation therapy and concurrent chemoradiation therapy in uterine cervical cancer. Int J Clin Oncol 2015; 20(5):989-96; PMID:25736530; http://dx.doi.org/10.1007/s10147-015-0807-6
   PubMed Web of Science ®Google Scholar
• Nedergaard BS, Ladekarl M, Nyengaard JR, Nielsen K. A comparative study of the cellular immune response in patients with stage IB cervical squamous cell carcinoma. Low numbers of several immune cell subtypes are strongly associated with relapse of disease within 5 years. Gynecol Oncol 2008; 108(1):106-11; PMID:17945335; http://dx.doi.org/10.1016/j.ygyno.2007.08.089
   PubMed Web of Science ®Google Scholar
• Welters MJ, van der Sluis TC, van Meir H, Loof NM, van Ham VJ, van Duikeren DS, Santegoets SJ, Arens R, de Kam ML, Cohen AF et al. Vaccination during myeloid cell depletion by cancer chemotherapy fosters robust T cell responses. Sci Transl Med 2016; 8(334):334ra52; PMID:27075626; http://dx.doi.org/10.1126/scitranslmed.aad8307
   PubMed Web of Science ®Google Scholar
• Santin AD, Hermonat PL, Ravaggi A, Bellone S, Roman J, Pecorelli S, Cannon M, Parham GP. Effects of concurrent cisplatinum administration during radiotherapy vs. radiotherapy alone on the immune function of patients with cancer of the uterine cervix. Int J Radiat Oncol Biol Phys 2000; 48(4):997-1006; PMID:11072156; http://dx.doi.org/10.1016/S0360-3016(00)00769-0
   PubMed Web of Science ®Google Scholar
• Parikh F, Duluc D, Imai N, Clark A, Misiukiewicz K, Bonomi M, Gupta V, Patsias A, Parides M, Demicco EG et al. Chemoradiotherapy-induced upregulation of PD-1 antagonizes immunity to HPV-related oropharyngeal cancer. Cancer Res 2014; 74(24):7205-16; PMID:25320012; http://dx.doi.org/10.1158/0008-5472.CAN-14-1913
   PubMed Web of Science ®Google Scholar
• Keisari Y, Hochman I, Confino H, Korenstein R, Kelson I. Activation of local and systemic anti-tumor immune responses by ablation of solid tumors with intratumoral electrochemical or alpha radiation treatments. Cancer Immunol Immunother 2014; 63(1):1-9; PMID:23955682; http://dx.doi.org/10.1007/s00262-013-1462-2
   PubMed Web of Science ®Google Scholar
• Mauch P, Constine L, Greenberger J, Knospe W, Sullivan J, Liesveld JL, Deeg HJ. Hematopoietic stem cell compartment: Acute and late effects of radiation therapy and chemotherapy. Int J Radiat Oncol Biol Phys 1995; 31(5):1319-39; PMID:7713791; http://dx.doi.org/10.1016/0360-3016(94)00430-S
   PubMed Web of Science ®Google Scholar
• Ellis RE. The distribution of active bone marrow in the adult. Phys Med Biol 1961; 5:255-8; PMID:13726497; http://dx.doi.org/10.1088/0031-9155/5/3/302
   PubMed Web of Science ®Google Scholar
• McGuire SM, Bhatia SK, Sun W, Jacobson GM, Menda Y, Ponto LL, Smith BJ, Gross BA, Bayouth JE, Sunderland JJ et al. Using [18F]Fluorothymidine imaged with positron emission tomography to quantify and reduce hematologic toxicity due to chemoradiation therapy for pelvic cancer patients. Int J Radiat Oncol Biol Phys 2016; 96(1):228-39; PMID:27319286; http://dx.doi.org/10.1016/j.ijrobp.2016.04.009
   PubMed Web of Science ®Google Scholar
• Battaglia A, Buzzonetti A, Martinelli E, Fanelli M, Petrillo M, Ferrandina G, Scambia G, Fattorossi A. Selective changes in the immune profile of tumor-draining lymph nodes after different neoadjuvant chemoradiation regimens for locally advanced cervical cancer. Int J Radiat Oncol Biol Phys 2010; 76(5):1546-53; PMID:20338481; http://dx.doi.org/10.1016/j.ijrobp.2009.10.014
   PubMed Web of Science ®Google Scholar
• Klug F, Prakash H, Huber PE, Seibel T, Bender N, Halama N, Pfirschke C, Voss RH, Timke C, Umansky L et al. Low-dose irradiation programs macrophage differentiation to an iNOS(+)/M1 phenotype that orchestrates effective T cell immunotherapy. Cancer Cell 2013; 24(5):589-602; PMID:24209604; http://dx.doi.org/10.1016/j.ccr.2013.09.014
   PubMed Web of Science ®Google Scholar
• Klopp AH, Moughan J, Portelance L, Miller BE, Salehpour MR, Hildebrandt E, Nuanjing J, D'Souza D, Souhami L, Small W Jr et al. Hematologic toxicity in RTOG 0418: A phase 2 study of postoperative IMRT for gynecologic cancer. Int J Radiat Oncol Biol Phys 2013; 86(1):83-90; PMID:23582248; http://dx.doi.org/10.1016/j.ijrobp.2013.01.017
   PubMed Web of Science ®Google Scholar
• Albuquerque K, Giangreco D, Morrison C, Siddiqui M, Sinacore J, Potkul R, Roeske J. Radiation-related predictors of hematologic toxicity after concurrent chemoradiation for cervical cancer and implications for bone marrow-sparing pelvic IMRT. Int J Radiat Oncol Biol Phys 2011; 79(4):1043-7; PMID:20471182; http://dx.doi.org/10.1016/j.ijrobp.2009.12.025
   PubMed Web of Science ®Google Scholar
• Jie HB, Gildener-Leapman N, Li J, Srivastava RM, Gibson SP, Whiteside TL, Ferris RL. Intratumoral regulatory T cells upregulate immunosuppressive molecules in head and neck cancer patients. Br J Cancer 2013; 109(10):2629-35; PMID:24169351; http://dx.doi.org/10.1038/bjc.2013.645
   PubMed Web of Science ®Google Scholar
• Quinn MA, Benedet JL, Odicino F, Maisonneuve P, Beller U, Creasman WT, Heintz AP, Ngan HY, Pecorelli S. Carcinoma of the cervix uteri. FIGO 26th annual report on the results of treatment in gynecological cancer. Int J Gynaecol Obstet 2006; 95(Suppl 1):S43-103; PMID:17161167; http://dx.doi.org/10.1016/S0020-7292(06)60030-1
   PubMed Web of Science ®Google Scholar
• Hellebrekers BWJ, Zwinderman AH, Kenter GG, Peters AAW, Snijders-Keilholz A, Graziosi GCM, Fleuren GJ, Trimbos JB. Surgically-treated early cervical cancer: Prognostic factors and the significance of depth of tumor invasion. Int J Gynecol Cancer 1999; 9(3):212-9; PMID:11240769
   PubMed Web of Science ®Google Scholar
• Pieterse QD, Trimbos JBMZ, Dijkman A, Creutzberg CL, Gaarenstroom KN, Peters AAW, Kenter GG. Postoperative radiation therapy improves prognosis in patients with adverse risk factors in localized, early-stage cervical cancer: A retrospective comparative study. Int J Gynecol Cancer 2006; 16(3):1112-8; PMID:16803494; http://dx.doi.org/10.1111/j.1525-1438.2006.00600.x
   PubMed Web of Science ®Google Scholar
• Sevin BU, Nadji M, Lampe B, Lu Y, Hilsenbeck S, Koechli OR, Averette HE. Prognostic factors of early-stage cervical-cancer treated by radical hysterectomy. Cancer 1995; 76(10):1978-86; PMID:8634988; http://dx.doi.org/10.1002/1097-0142(19951115)76
   PubMed Web of Science ®Google Scholar
• Soisson AP, Soper JT, Clarkepearson DL, Berchuck A, Montana G, Creasman WT. Adjuvant radiotherapy following radical hysterectomy for patients with stage Ib and IIa cervical cancer. Gynecol Oncol 1990; 37(3):390-5; PMID:2351324; http://dx.doi.org/10.1016/0090-8258(90)90374-T
   PubMed Web of Science ®Google Scholar
• Rijkmans EC, Nout RA, Rutten IH, Ketelaars M, Neelis KJ, Laman MS, Coen VL, Gaarenstroom KN, Kroep JR, Creutzberg CL. Improved survival of patients with cervical cancer treated with image-guided brachytherapy compared with conventional brachytherapy. Gynecol Oncol 2014; 135(2):231-8; PMID:25172763; http://dx.doi.org/10.1016/j.ygyno.2014.08.027
   PubMed Web of Science ®Google Scholar
• Dimopoulos JC, Petrow P, Tanderup K, Petric P, Berger D, Kirisits C, Pedersen EM, van Limbergen E, Haie-Meder C, Pötter R. Recommendations from Gynaecological (GYN) GEC-ESTRO Working Group (IV): Basic principles and parameters for MR imaging within the frame of image based adaptive cervix cancer brachytherapy. Radiother Oncol 2012; 103(1):113-22; PMID:22296748; http://dx.doi.org/10.1016/j.radonc.2011.12.024
   PubMed Web of Science ®Google Scholar
• Welters MJ, Kenter GG, de Vos van Steenwijk PJ, Lowik MJ, Berends-van der Meer DM, Essahsah F, Stynenbosch LF, Vloon AP, Ramwadhdoebe TH, Piersma SJ et al. Success or failure of vaccination for HPV16-positive vulvar lesions correlates with kinetics and phenotype of induced T-cell responses. Proc Natl Acad Sci USA 2010; 107(26):11895-9; PMID:20547850; http://dx.doi.org/10.1073/pnas.1006500107
   PubMed Web of Science ®Google Scholar
• Santegoets SJ, Dijkgraaf EM, Battaglia A, Beckhove P, Britten CM, Gallimore A, Godkin A, Gouttefangeas C, de Gruijl TD, Koenen HJ et al. Monitoring regulatory T cells in clinical samples: Consensus on an essential marker set and gating strategy for regulatory T cell analysis by flow cytometry. Cancer Immunol Immunother 2015; 64(10):1271-86; PMID:26122357; http://dx.doi.org/10.1007/s00262-015-1729-x
   PubMed Web of Science ®Google Scholar
• G.I.W.G. European Medicines Agency. Reflection paper for laboratories that perform the analysis or evaluation of clinical trial samples, EMA/INS/GCP/532137/2010 2012; 1-19.
   Google Scholar