Head and neck cancer relapse after chemoradiotherapy correlates with CD163+ macrophages in primary tumour and CD11b+ myeloid cells in recurrences

British Journal of Cancer

Volumn 111, Issue 8, 2014, Pages 1509-1518

  Balermpas, P ^a   Rodel F ^a   Liberz, R ^a   Oppermann, J ^a   Wagenblast, J ^a   Ghanaati, S ^a   Harter, P N ^a   Mittelbronn, M ^a   Weiss, C ^a   Rodel C ^a,b   Fokas, E ^a  

^a GOETHE UNIVERSITY   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

CD11b+ myeloid cells; Chemoradiotherapy; Head and neck cancer; Macrophages; Prognostic

Indexed keywords

CD11B ANTIGEN; CD163 ANTIGEN; CD68 ANTIGEN; CISPLATIN; FLUOROURACIL; ANTINEOPLASTIC AGENT; CELL SURFACE RECEPTOR; DIFFERENTIATION ANTIGEN; ITGAM PROTEIN, HUMAN; LEUKOCYTE ANTIGEN;

ADULT; ARTICLE; BONE MARROW CELL; CANCER GRADING; CANCER RECURRENCE; CANCER STAGING; CHEMORADIOTHERAPY; CONTINUOUS INFUSION; CONTROLLED STUDY; DISTANT METASTASIS FREE SURVIVAL; FEMALE; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN TISSUE; LOCAL FAILURE FREE SURVIVAL; MAJOR CLINICAL STUDY; MALE; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; RADIATION DOSE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR LOCALIZATION; HEAD AND NECK NEOPLASMS; IMMUNOLOGY; MACROPHAGE; MIDDLE AGED; PATHOLOGY; TUMOR RECURRENCE;

ANTIGENS, CD; ANTIGENS, CD11B; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; ANTINEOPLASTIC AGENTS; BONE MARROW CELLS; FEMALE; HEAD AND NECK NEOPLASMS; HUMANS; MACROPHAGES; MALE; MIDDLE AGED; NEOPLASM RECURRENCE, LOCAL; RADIOTHERAPY; RECEPTORS, CELL SURFACE;

EID: 84922008349     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2014.446     Document Type: Article

References (51)

1. Ahn GO, Brown JM (2008) Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: role of bone marrow-derived myelomonocytic cells. Cancer Cell 13(3): 193-205.
2. Ahn GO, Tseng D, Liao CH, Dorie MJ, Czechowicz A, Brown JM (2010) Inhibition of Mac-1 (CD11b/CD18) enhances tumor response to radiation by reducing myeloid cell recruitment. Proc Natl Acad Sci USA 107(18): 8363-8368.
3. Ambarus CA, Krausz S, van Eijk M, Hamann J, Radstake TR, Reedquist KA, Tak PP, Baeten DL (2012) Systematic validation of specific phenotypic markers for in vitro polarised human macrophages. J Immunol Methods 375(1-2): 196-206.
4. Ang KK, Harris J, Wheeler R, Weber R, Rosenthal DI, Nguyen-Tan PF, Westra WH, Chung CH, Jordan RC, Lu C, Kim H, Axelrod R, Silverman CC, Redmond KP, Gillison ML (2010) Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med 363(1): 24-35.
5. Argiris A, Karamouzis MV, Raben D, Ferris RL (2008) Head and neck cancer. Lancet 371(9625): 1695-1709.
6. Baeten CI, Castermans K, Lammering G, Hillen F, Wouters BG, Hillen HF, Griffioen AW, Baeten CG (2006) Effects of radiotherapy and chemotherapy on angiogenesis and leukocyte infiltration in rectal cancer. Int J Radiat Oncol Biol Phys 66(4): 1219-1227.
7. Balermpas P, Michel Y, Wagenblast J, Seitz O, Weiss C, Rodel F, Rodel C, Fokas E (2014) Tumour-infiltrating lymphocytes predict response to definitive chemoradiotherapy in head and neck cancer. Br J Cancer 110(2): 501-509.
8. Baumgarten P, Harter PN, Tonjes M, Capper D, Blank AE, Sahm F, von Deimling A, Kolluru V, Schwamb B, Rabenhorst U, Starzetz T, Kogel D, Rieker RJ, Plate KH, Ohgaki H, Radlwimmer B, Zornig M, Mittelbronn M (2014) Loss of FUBP1 expression in gliomas predicts FUBP1 mutation and is associated with oligodendroglial differentiation, IDH1 mutation and 1p/19q loss of heterozygosity. Neuropathol Appl Neurobiol 40(2): 205-216.
9. Bhardwaj N (2007) Harnessing the immune system to treat cancer. J Clin Invest 117(5): 1130-1136.
10. Bruchard M, Mignot G, Derangere V, Chalmin F, Chevriaux A, Vegran F, Boireau W, Simon B, Ryffel B, Connat JL, Kanellopoulos J, Martin F, Rebe C, Apetoh L, Ghiringhelli F (2013) Chemotherapy-triggered cathepsin B release in myeloid-derived suppressor cells activates the Nlrp3 inflammasome and promotes tumor growth. Nat Med 19(1): 57-64.
11. Budach V, Stuschke M, Budach W, Baumann M, Geismar D, Grabenbauer G, Lammert I, Jahnke K, Stueben G, Herrmann T, Bamberg M, Wust P, Hinkelbein W, Wernecke KD (2005) Hyperfractionated accelerated chemoradiation with concurrent fluorouracil-mitomycin is more effective than dose-escalated hyperfractionated accelerated radiation therapy alone in locally advanced head and neck cancer: final results of the radiotherapy cooperative clinical trials group of the German Cancer Society 95-06 Prospective Randomized Trial. J Clin Oncol 23(6): 1125-1135.
12. Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, Kim E, Jiang B, Goodman MT, Sibug-Saber M, Cozen W, Liu L, Lynch CF, Wentzensen N, Jordan RC, Altekruse S, Anderson WF, Rosenberg PS, Gillison ML (2011) Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol 29(32): 4294-4301.
13. Chen FH, Chiang CS, Wang CC, Tsai CS, Jung SM, Lee CC, McBride WH, Hong JH (2009) Radiotherapy decreases vascular density and causes hypoxia with macrophage aggregation in TRAMP-C1 prostate tumors. Clin Cancer Res 15(5): 1721-1729.
14. Chung FT, Lee KY, Wang CW, Heh CC, Chan YF, Chen HW, Kuo CH, Feng PH, Lin TY, Wang CH, Chou CL, Chen HC, Lin SM, Kuo HP (2012) Tumor-associated macrophages correlate with response to epidermal growth factor receptor-tyrosine kinase inhibitors in advanced non-small cell lung cancer. Int J Cancer 131(3): E227-E235.
15. Daly ME, Le QT, Kozak MM, Maxim PG, Murphy JD, Hsu A, Loo Jr BW, Kaplan MJ, Fischbein NJ, Chang DT (2011) Intensity-modulated radiotherapy for oral cavity squamous cell carcinoma: patterns of failure and predictors of local control. Int J Radiat Oncol Biol Phys 80(5): 1412-1422.
16. De Palma M, Lewis CE (2013) Macrophage regulation of tumor responses to anticancer therapies. Cancer Cell 23(3): 277-286.
17. DeNardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF, Gallagher WM, Wadhwani N, Keil SD, Junaid SA, Rugo HS, Hwang ES, Jirstrom K, West BL, Coussens LM (2011) Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov 1(1): 54-67.
18. Fokas E, McKenna WG, Muschel RJ (2012a) The impact of tumor microenvironment on cancer treatment and its modulation by direct and indirect antivascular strategies. Cancer Metastasis Rev 31(3-4): 823-842.
19. Fokas E, Prevo R, Pollard JR, Reaper PM, Charlton PA, Cornelissen B, Vallis KA, Hammond EM, Olcina MM, Gillies McKenna W, Muschel RJ, Brunner TB (2012b) Targeting ATR in vivo using the novel inhibitor VE-822 results in selective sensitization of pancreatic tumors to radiation. Cell Death Dis 3: e441.
20. Fujii N, Shomori K, Shiomi T, Nakabayashi M, Takeda C, Ryoke K, Ito H (2012) Cancer-associated fibroblasts and CD163-positive macrophages in oral squamous cell carcinoma: their clinicopathological and prognostic significance. J Oral Pathol Med 41(6): 444-451.
21. Gabrilovich DI, Nagaraj S (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9(3): 162-174.
22. Gupta T, Jain S, Agarwal JP, Ghosh-Laskar S, Phurailatpam R, Pai-Shetty R, Dinshaw KA (2011) Prospective assessment of patterns of failure after high-precision definitive (chemo)radiation in head-and-neck squamous cell carcinoma. Int J Radiat Oncol Biol Phys 80(2): 522-531.
23. Ibe S, Qin Z, Schuler T, Preiss S, Blankenstein T (2001) Tumor rejection by disturbing tumor stroma cell interactions. J Exp Med 194(11): 1549-1559.
24. Jensen TO, Schmidt H, Moller HJ, Hoyer M, Maniecki MB, Sjoegren P, Christensen IJ, Steiniche T (2009) Macrophage markers in serum and tumor have prognostic impact in American Joint Committee on Cancer stage I/II melanoma. J Clin Oncol 27(20): 3330-3337.
25. Kerrebijn JD, Balm AJ, Knegt PP, Meeuwis CA, Drexhage HA (1994) Macrophage and dendritic cell infiltration in head and neck squamous-cell carcinoma; an immunohistochemical study. Cancer Immunol Immunother 38(1): 31-37.
26. Kioi M, Vogel H, Schultz G, Hoffman RM, Harsh GR, Brown JM (2010) Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. J Clin Invest 120(3): 694-705.
27. Kozin SV, Kamoun WS, Huang Y, Dawson MR, Jain RK, Duda DG (2010) Recruitment of myeloid but not endothelial precursor cells facilitates tumor regrowth after local irradiation. Cancer Res 70(14): 5679-5685.
28. Kuonen F, Secondini C, Ruegg C (2012) Molecular pathways: emerging pathways mediating growth, invasion, and metastasis of tumors progressing in an irradiated microenvironment. Clin Cancer Res 18(19): 5196-5202.
29. Lassen P, Eriksen JG, Hamilton-Dutoit S, Tramm T, Alsner J, Overgaard J (2009) Effect of HPV-associated p16INK4A expression on response to radiotherapy and survival in squamous cell carcinoma of the head and neck. J Clin Oncol 27(12): 1992-1998.
30. Lau SK, Chu PG, Weiss LM (2004) CD163: a specific marker of macrophages in paraffin-embedded tissue samples. Am J Clin Pathol 122(5): 794-801.
31. Lee CH, Espinosa I, Vrijaldenhoven S, Subramanian S, Montgomery KD, Zhu S, Marinelli RJ, Peterse JL, Poulin N, Nielsen TO, West RB, Gilks CB, van de Rijn M (2008) Prognostic significance of macrophage infiltration in leiomyosarcomas. Clin Cancer Res 14(5): 1423-1430.
32. Li C, Shintani S, Terakado N, Nakashiro K, Hamakawa H (2002) Infiltration of tumor-associated macrophages in human oral squamous cell carcinoma. Oncol Rep 9(6): 1219-1223.
33. Lima L, Oliveira D, Tavares A, Amaro T, Cruz R, Oliveira MJ, Ferreira JA, Santos L (2013) The predominance of M2-polarised macrophages in the stroma of low-hypoxic bladder tumors is associated with BCG immunotherapy failure. Urol Oncol 32(4): 449-457.
34. Luo Y, Zhou H, Krueger J, Kaplan C, Lee SH, Dolman C, Markowitz D, Wu W, Liu C, Reisfeld RA, Xiang R (2006) Targeting tumor-associated macrophages as a novel strategy against breast cancer. J Clin Invest 116(8): 2132-2141.
35. Lyford-Pike S, Peng S, Young GD, Taube JM, Westra WH, Akpeng B, Bruno TC, Richmon JD, Wang H, Bishop JA, Chen L, Drake CG, Topalian SL, Pardoll DM, Pai SI (2013) Evidence for a role of the PD-1:PD-L1 pathway in immune resistance of HPV-associated head and neck squamous cell carcinoma. Cancer Res 73(6): 1733-1741.
36. Marcus B, Arenberg D, Lee J, Kleer C, Chepeha DB, Schmalbach CE, Islam M, Paul S, Pan Q, Hanash S, Kuick R, Merajver SD, Teknos TN (2004) Prognostic factors in oral cavity and oropharyngeal squamous cell carcinoma. Cancer 101(12): 2779-2787.
37. Martin BJ (2013) Inhibiting vasculogenesis after radiation: a new paradigm to improve local control by radiotherapy. Semin Radiat Oncol 23(4): 281-287.
38. Medrek C, Ponten F, Jirstrom K, Leandersson K (2012) The presence of tumour associated macrophages in tumor stroma as a prognostic marker for breast cancer patients. BMC Cancer 12: 306.
39. Milas L (1990) Tumor bed effect in murine tumors: relationship to tumor take and tumor macrophage content. Radiat Res 123(2): 232-236.
40. Moeller BJ, Cao Y, Li CY, Dewhirst MW (2004) Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell 5(5): 429-441.
41. Mori K, Hiroi M, Shimada J, Ohmori Y (2011) Infiltration of m2 tumorassociated macrophages in oral squamous cell carcinoma correlates with tumor malignancy. Cancers (Basel) 3(4): 3726-3739.
42. Nakasone ES, Askautrud HA, Kees T, Park JH, Plaks V, Ewald AJ, Fein M, Rasch MG, Tan YX, Qiu J, Park J, Sinha P, Bissell MJ, Frengen E, Werb Z, Egeblad M (2012) Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance. Cancer Cell 21(4): 488-503.
43. Osterholzer JJ, Christensen PJ, Lama V, Horowitz JC, Hattori N, Subbotina N, Cunningham A, Lin Y, Murdock BJ, Morey RE, Olszewski MA, Lawrence DA, Simon RH, Sisson TH (2012) PAI-1 promotes the accumulation of exudate macrophages and worsens pulmonary fibrosis following type II alveolar epithelial cell injury. J Pathol 228(2): 170-180.
44. Pyonteck SM, Akkari L, Schuhmacher AJ, Bowman RL, Sevenich L, Quail DF, Olson OC, Quick ML, Huse JT, Teijeiro V, Setty M, Leslie CS, Oei Y, Pedraza A, Zhang J, Brennan CW, Sutton JC, Holland EC, Daniel D, Joyce JA (2013) CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med 19(10): 1264-1272.
45. Qian BZ, Pollard JW (2010) Macrophage diversity enhances tumor progression and metastasis. Cell 141(1): 39-51.
46. Russell SM, Angell T, Lechner MG, Liebertz DJ, Correa AJ, Sinha UK, Kokot N, Epstein AL (2013) Immune cell infiltration patterns and survival in head and neck squamous cell carcinoma. Head Neck Oncol 5(3): 24.
47. Steidl C, Lee T, Shah SP, Farinha P, Han G, Nayar T, Delaney A, Jones SJ, Iqbal J, Weisenburger DD, Bast MA, Rosenwald A, Muller-Hermelink HK, Rimsza LM, Campo E, Delabie J, Braziel RM, Cook JR, Tubbs RR, Jaffe ES, Lenz G, Connors JM, Staudt LM, Chan WC, Gascoyne RD (2010) Tumour-associated macrophages and survival in classic Hodgkin's lymphoma. N Engl J Med 362(10): 875-885.
48. Tan KL, Scott DW, Hong F, Kahl BS, Fisher RI, Bartlett NL, Advani RH, Buckstein R, Rimsza LM, Connors JM, Steidl C, Gordon LI, Horning SJ, Gascoyne RD (2012) Tumor-associated macrophages predict inferior outcomes in classic Hodgkin lymphoma: a correlative study from the E2496 Intergroup trial. Blood 120(16): 3280-3287.
49. Wu Y, Li Y, Zhang C, A X, Wang Y, Cui W, Li H, Du J (2014) S100a8/a9 Released by CD11b+Gr1+ Neutrophils Activates Cardiac Fibroblasts to Initiate Angiotensin II-Induced Cardiac Inflammation and Injury. Hypertension 63(6): 1241-1250.
50. Xu J, Escamilla J, Mok S, David J, Priceman S, West B, Bollag G, McBride W, Wu L (2013) CSF1R signaling blockade stanches tumor-infiltrating myeloid cells and improves the efficacy of radiotherapy in prostate cancer. Cancer Res 73(9): 2782-2794.
51. Zaleska K, Bruechner K, Baumann M, Zips D, Yaromina A (2011) Tumourinfiltrating CD11b+ myelomonocytes and response to fractionated irradiation of human squamous cell carcinoma (hSCC) xenografts. Radiother Oncol 101(1): 80-85.