Tenascin-C: Exploitation and collateral damage in cancer management

Cell Adhesion and Migration

Volumn 9, Issue 1-2, 2015, Pages 141-153

  Spenlé, Caroline ^a,b   Saupe, Falk ^a,b,c   Midwood, Kim ^d   Burckel, Héléne ^a   Noel, Georges ^a   Orend, Gertraud ^a,b  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b Fédé Ration de Médecine Translationnelle de Strasbourg FMTS   (France)

^c UPPSALA UNIVERSITY   (Sweden)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cancer; Extracellular matrix; Tenascin C; Tumor microenvironment

Indexed keywords

DICKKOPF 1 PROTEIN; STROMELYSIN; TENASCIN;

ANGIOGENESIS; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; CANCER RECURRENCE; CELL INVASION; CELL PROLIFERATION; CELL SURVIVAL; EXTRACELLULAR MATRIX; GENE TARGETING; HUMAN; HYPOXIA; IMMUNOHISTOCHEMISTRY; METASTASIS; NONHUMAN; OVERALL SURVIVAL; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PROTEIN EXPRESSION; REVIEW; RNA INTERFERENCE; TUMOR GROWTH; TUMOR MICROENVIRONMENT; WNT SIGNALING PATHWAY; ANIMAL; IMMUNOTHERAPY; METABOLISM; NEOPLASMS; PHYSIOLOGY;

ANIMALS; EXTRACELLULAR MATRIX; HUMANS; IMMUNOTHERAPY; NEOPLASMS; RNA INTERFERENCE; TENASCIN; TUMOR MICROENVIRONMENT;

EID: 84931041572     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: 10.1080/19336918.2014.1000074     Document Type: Review

References (119)

1. Pàez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Vi ñals F, Inoue M, Bergers G, Hanahan D, Casanovas O. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009; 15:220-31; http://dx.doi.org/10.1016/j.ccr.2009.01.027
2. Orend G, Saupe F, Schwenzer A, Midwood K. The Extracellular Matrix and Cancer: Regulation of Tumor Cell Biology by Tenascin-C. iConcept Press; 2014. ISBN: 978-1922227515
3. Orend G, Chiquet-Ehrismann R. Tenascin-C induced signaling in cancer. Cancer Lett 2006; 244:143-63; http://dx.doi.org/10.1016/j.canlet.2006.02.017
4. Saupe F, Schwenzer A, Jia Y, Gasser I, Spenle C, Langlois B, Kammerer M, Lefebvre O, Hlushchuk R, Rupp T, et al. Tenascin-C downregulates wnt inhibitor dickkopf-1, promoting tumorigenesis in a neuroendocrine tumor model. Cell Rep 2013; 5:482-92; http://dx.doi.org/10.1016/j.celrep.2013.09.014
5. Lieber CS, Weiss DG, Paronetto F, Veterans Affairs Cooperative Study 391 Group. Value of fibrosis markers for staging liver fibrosis in patients with precirrhotic alcoholic liver disease. Alcohol Clin Exp Res 2008; 32:1031-9; http://dx.doi.org/10.1111/j.1530-0277.2008.00664.x
6. Päiväniemi OE, Maasilta PK, Alho HS, Vainikka TLS, Salminen U-S. Epithelial tenascin predicts obliterative airway disease. J Heart Lung Transplant Off Publ Int Soc Heart Transplant 2008; 27:400-7; http://dx.doi.org/10.1016/j.healun.2008.01.009
7. Tsukada B, Terasaki F, Shimomura H, Otsuka K, Otsuka K, Katashima T, Fujita S, Imanaka-Yoshida K, Yoshida T, Hiroe M, et al. High prevalence of chronic myocarditis in dilated cardiomyopathy referred for left ventriculoplasty: expression of tenascin C as a possible marker for inflammation. Hum Pathol 2009; 40:1015-22; http://dx.doi.org/10.1016/j.humpath.2008.12.017
8. Schenk S, Muser J, Vollmer G, Chiquet-Ehrismann R. Tenascin-C in serum: a questionable tumor marker. Int J Cancer 1995; 61:443-9; http://dx.doi.org/10.1002/ijc.2910610402
9. Fouda GG, Jaeger FH, Amos JD, Ho C, Kunz EL, Anasti K, Stamper LW, Liebl BE, Barbas KH, Ohashi T, et al. Tenascin-C is an innate broadspectrum, HIV-1-neutralizing protein in breast milk. Proc Natl Acad Sci U S A 2013; 110:18220-5; http://dx.doi.org/10.1073/pnas.1307336110
10. Riedl S, Tandara A, Reinshagen M, Hinz U, Faissner A, Bodenmüller H, Buhr HJ, Herfarth C, Möller P. Serum tenascin-C is an indicator of inflammatory bowel disease activity. Int J Colorectal Dis 2001; 16:285-91; http://dx.doi.org/10.1007/s003840100312
11. Didem T, Faruk T, Senem K, Derya D, Murat S, Murat G, Oznur K. Clinical significance of serum tenascin-c levels in epithelial ovarian cancer. Tumour Biol J Int Soc Oncodevelopmental Biol Med 2014; 35:6777-82; http://dx.doi.org/10.1007/s13277-014-1923-z
12. Tastekin D, Tas F, Karabulut S, Duranyildiz D, Serilmez M, Guveli M, Vatansever S. Clinical significance of serum tenascin-C levels in breast cancer. Tumour Biol J Int Soc Oncodevelopmental Biol Med 2014; 35:6619-25; http://dx.doi.org/10.1007/s13277-014-1875-3
13. Langlois B, Saupe F, Rupp T, Arnold C, van der Heyden M, Orend G, Hussenet T. AngioMatrix, a signature of the tumor angiogenic switch-specific matrisome, correlates with poor prognosis for glioma and colorectal cancer patients. Oncotarget 2014; 5: 10529-45
14. Thomasset N, Lochter A, Sympson CJ, Lund LR, Williams DR, Behrendtsen O, Werb Z, Bissell MJ. Expression of autoactivated stromelysin-1 in mammary glands of transgenic mice leads to a reactive stroma during early development. Am J Pathol 1998; 153:457-67; http://dx.doi.org/10.1016/S0002-9440(10)65589-7
15. Sternlicht MD, Bissell MJ, Werb Z. The matrix metalloproteinase stromelysin-1 acts as a natural mammary tumor promoter. Oncogene 2000; 19:1102-13; http://dx.doi.org/10.1038/sj.onc.1203347
16. Taraseviciute A, Vincent BT, Schedin P, Jones PL. Quantitative analysis of three-dimensional human mammary epithelial tissue architecture reveals a role for tenascin-C in regulating c-met function. Am J Pathol 2010; 176:827-38; http://dx.doi.org/10.2353/ajpath.2010.090006
17. Kääriäinen E, Nummela P, Soikkeli J, Yin M, Lukk M, Jahkola T, Virolainen S, Ora A, Ukkonen E, Saksela O, et al. Switch to an invasive growth phase in melanoma is associated with tenascin-C, fibronectin, and procollagen-I forming specific channel structures for invasion. J Pathol 2006; 210:181-91; http://dx.doi.org/10.1002/path.2045
18. Midwood KS, Orend G. The role of tenascin-C in tissue injury and tumorigenesis. J Cell Commun Signal 2009; 3:287-310; http://dx.doi.org/10.1007/s12079-009-0075-1
19. Van Obberghen-Schilling E, Tucker RP, Saupe F, Gasser I, Cseh B, Orend G. Fibronectin and tenascin-C: accomplices in vascular morphogenesis during development and tumor growth. Int J Dev Biol 2011; 55:511-25; http://dx.doi.org/10.1387/ijdb.103243eo
20. Chiquet-Ehrismann R, Tucker RP. Tenascins and the importance of adhesion modulation. Cold Spring Harb Perspect Biol 2011; 3; a004960; http://dx.doi.org/10.1101/cshpers-pect.a004960
21. Zukiel R, Nowak S, Wyszko E, Rolle K, Gawronska I, Barciszewska MZ, Barciszewski J. Suppression of human brain tumor with interference RNA specific for tenascin-C. Cancer Biol Ther 2006; 5:1002-7; http://dx.doi.org/10.4161/cbt.5.8.2886
22. Wyszko E, Rolle K, Nowak S, Zukiel R, Nowak M, Piestrzeniewicz R, Gawronska I, Barciszewska MZ, Barciszewski J. A multivariate analysis of patients with brain tumors treated with ATN-RNA. Acta Pol Pharm 2008; 65:677-84
23. Rolle K, Nowak S, Wyszko E, Nowak M, Zukiel R, Piestrzeniewicz R, Gawronska I, Barciszewska MZ, Barciszewski J. Promising human brain tumors therapy with interference RNA intervention (iRNAi). Cancer Biol Ther 2010; 9:396-406; http://dx.doi.org/10.4161/cbt.9.5.10958
24. Midwood KS, Hussenet T, Langlois B, Orend G. Advances in tenascin-C biology. Cell Mol Life Sci CMLS 2011; 68:3175-99; http://dx.doi.org/10.1007/s00018-011-0783-6
25. Fujinaga K, Onoda K, Yamamoto K, Imanaka-Yoshida K, Takao M, Shimono T, Shimpo H, Yoshida T, Yada I. Locally applied cilostazol suppresses neointimal hyperplasia by inhibiting tenascin-C synthesis and smooth muscle cell proliferation in free artery grafts. J Thorac Cardiovasc Surg 2004; 128:357-63; http://dx.doi.org/10.1016/j.jtcvs.2003.11.015
26. Yamamoto K, Onoda K, Sawada Y, Fujinaga K, Imanaka-Yoshida K, Yoshida T, Shimpo H. Locally applied cilostazol suppresses neointimal hyperplasia and medial thickening in a vein graft model. Ann Thorac Cardiovasc Surg Off J Assoc Thorac Cardiovasc Surg Asia 2007; 13:322-30
27. Fischer JW. Tenascin-C: a key molecule in graft stenosis. Cardiovasc Res 2007; 74:335-6; http://dx.doi.org/10.1016/j.cardiores.2007.04.001
28. Midwood KS, Williams LV, Schwarzbauer JE. Tissue repair and the dynamics of the extracellular matrix. Int J Biochem Cell Biol 2004; 36:1031-7; http://dx.doi.org/10.1016/j.biocel.2003.12.003
29. Reilly RM. Monoclonal Antibody and Peptide-Targeted Radiotherapy of Cancer. Wiley VCH Book Chapter 5.4 2010; ISSN: 978-0-470-24372-5
30. Brack SS, Silacci M, Birchler M, Neri D. Tumor-targeting properties of novel antibodies specific to the large isoform of tenascin-C. Clin Cancer Res 2006; 12:3200-8; http://dx.doi.org/10.1158/1078-0432.CCR-05-2804
31. Pedretti M, Verpelli C, Marlind J, Bertani G, Sala C, Neri D, Bello L. Combination of temozolomide with immunocytokine F16-IL2 for the treatment of glioblastoma. Br J Cancer 2010; 103:827-36; http://dx.doi.org/10.1038/sj.bjc.6605832
32. Schliemann C, Wiedmer A, Pedretti M, Szczepanowski M, Klapper W, Neri D. Three clinical-stage tumor targeting antibodies reveal differential expression of oncofetal fibronectin and tenascin-C isoforms in human lymphoma. Leuk Res 2009; 33:1718-22; http://dx.doi.org/10.1016/j.leukres.2009.06.025
33. Berndt A, Kollner R, Richter P, Franz M, Voigt A, Berndt A, Borsi L, Giavazzi R, Neri D, Kosmehl H. A comparative analysis of oncofetal fibronectin and tenascin-C incorporation in tumour vessels using human recombinant SIP format antibodies. Histochem Cell Biol 2010; 133:467-75; http://dx.doi.org/10.1007/s00418-010-0685-y
34. Pedretti M, Soltermann A, Arni S, Weder W, Neri D, Hillinger S. Comparative immunohistochemistry of L19 and F16 in non-small cell lung cancer and mesothelioma: two human antibodies investigated in clinical trials in patients with cancer. Lung Cancer 2009; 64:28-33; http://dx.doi.org/10.1016/j.lungcan.2008.07.013
35. Schwager K, Villa A, Rosli C, Neri D, Rosli-Khabas M, Moser G. A comparative immunofluorescence analysis of three clinical-stage antibodies in head and neck cancer. Head Neck Oncol 2011; 3:25; http://dx.doi.org/10.1186/1758-3284-3-25
36. Frey K, Fiechter M, Schwager K, Belloni B, Barysch MJ, Neri D, Dummer R. Different patterns of fibronectin and tenascin-C splice variants expression in primary and metastatic melanoma lesions. Exp Dermatol 2011; 20:685-8; http://dx.doi.org/10.1111/j.1600-0625.2011.01314.x
37. Marlind J, Kaspar M, Trachsel E, Sommavilla R, Hindle S, Bacci C, Giovannoni L, Neri D. Antibodymediated delivery of interleukin-2 to the stroma of breast cancer strongly enhances the potency of chemotherapy. Clin Cancer Res 2008; 14:6515-24; http://dx.doi.org/10.1158/1078-0432.CCR-07-5041
38. Gutbrodt KL, Schliemann C, Giovannoni L, Frey K, Pabst T, Klapper W, Berdel WE, Neri D. Antibodybased delivery of interleukin-2 to neovasculature has potent activity against acute myeloid leukemia. Sci Transl Med 2013; 5:201-1118; http://dx.doi.org/10.1126/scitranslmed.3006221
39. De Braud FG, Catania C, Onofri A, Pierantoni C, Cascinu S, Maur M, Masini C, Conte PF, Giovannoni L, Tasciotti A, et al. Combination of the immunocytokine F16-IL2 with doxorubicin or paclitaxel in patients with solid tumors: Results from two phase Ib trials. J Clin Oncol 29 ASCO Annu Meet 2011 2011; Abstract 2595.
40. Heuveling DA, de Bree R, Vugts DJ, Huisman MC, Giovannoni L, Hoekstra OS, Leemans CR, Neri D, van Dongen GA. Phase 0 microdosing PET study using the human mini antibody F16SIP in head and neck cancer patients. J Nucl Med 2013; 54:397-401; http://dx.doi.org/10.2967/jnumed.112.111310
41. Aloj L, D’Ambrosio L, Aurilio M, Marreno R, Neri D, Menssen HD, Giovannoni L, Di Gennaro F, Caraco C, Arcamone M, et al. Preliminary evaluation of radioimmunotherapy with Τenarad, a I-131 labeled antibody fragment targeting the extra-domain A1 of tenascin-C, in patients with refractory Η odgkin lymphoma. J Clin Oncol 29 ASCO Annu Meet 2011 2011; Abstract 8063.
42. Aloj L, D’Ambrosio L, Aurilio M, Morisco A, Frigeri F, Caraco C, Di Gennaro F, Capobianco G, Giovannoni L, Menssen HD, et al. Radioimmunotherapy with Tenarad, a 131I-labelled antibody fragment targeting the extra-domain A1 of tenascin-C, in patients with refractory Hodgkin’s lymphoma. Eur J Nucl Med Mol Imaging 2014; 41:867-77; http://dx.doi.org/10.1007/s00259-013-2658-6
43. Tuerk C, MacDougal S, Gold L. RNA pseudoknots that inhibit human immunodeficiency virus type 1 reverse transcriptase. Proc Natl Acad Sci U A 1992; 89:6988-92; http://dx.doi.org/10.1073/pnas.89.15.6988
44. Hicke BJ, Marion C, Chang YF, Gould T, Lynott CK, Parma D, Schmidt PG, Warren S. Tenascin-C aptamers are generated using tumor cells and purified protein. J Biol Chem 2001; 276:48644-54; http://dx.doi.org/10.1074/jbc.M104651200
45. Schmidt KS, Borkowski S, Kurreck J, Stephens AW, Bald R, Hecht M, Friebe M, Dinkelborg L, Erdmann VA. Application of locked nucleic acids to improve aptamer in vivo stability and targeting function. Nucleic Acids Res 2004; 32:5757-65; http://dx.doi.org/10.1093/nar/gkh862
46. Hicke BJ, Stephens AW, Gould T, Chang YF, Lynott CK, Heil J, Borkowski S, Hilger CS, Cook G, Warren S, et al. Tumor targeting by an aptamer. J Nucl Med 2006; 47:668-78
47. Daniels DA, Chen H, Hicke BJ, Swiderek KM, Gold L. A tenascin-C aptamer identified by tumor cell SELEX: systematic evolution of ligands by exponential enrichment. Proc Natl Acad Sci U A 2003; 100:15416-21; http://dx.doi.org/10.1073/pnas.2136683100
48. Ko HY, Choi KJ, Lee CH, Kim S. A multimodal nanoparticle-based cancer imaging probe simultaneously targeting nucleolin, integrin alphavbeta3 and tenascin-C proteins. Biomaterials 2011; 32:1130-8; http://dx.doi.org/10.1016/j.biomaterials.2010.10.034
49. Burnett JC, Rossi JJ. RNA-based therapeutics: current progress and future prospects. Chem Biol 2012; 19:60-71; http://dx.doi.org/10.1016/j.chembiol.2011.12.008
50. Weissleder R. Molecular imaging in cancer. Science 2006; 312:1168-71; http://dx.doi.org/10.1126/science.1125949
51. Banerjee SR, Pullambhatla M, Byun Y, Nimmagadda S, Green G, Fox JJ, Horti A, Mease RC, Pomper MG. 68Ga-labeled inhibitors of prostate-specific membrane antigen (PSMA) for imaging prostate cancer. J Med Chem 2010; 53:5333-41; http://dx.doi.org/10.1021/jm100623e
52. Shah C, Miller TW, Wyatt SK, McKinley ET, Olivares MG, Sanchez V, Nolting DD, Buck JR, Zhao P, Ansari MS, et al. Imaging biomarkers predict response to anti-HER2 (ErbB2) therapy in preclinical models of breast cancer. Clin Cancer Res 2009; 15:4712-21; http://dx.doi.org/10.1158/1078-0432.CCR-08-2635
53. Christine C, Koubemba M, Shakir S, Clavier S, Ehret-Sabatier L, Saupe F, Orend G, Charbonniere LJ. Synthesis of an activated phosphonated bifunctional chelate with potential for PET imaging and radiotherapy. Org. Biomol. Chem. 2012; 10:9183-90; http://dx.doi.org/10.1039/c2ob26452h
54. Abada S, Lecointre A, Christine C, Ehret-Sabatier L, Saupe F, Orend G, Brasse D, Ouadi A, Hussenet T, Laquerriere P, et al. Phosphonated Chelates for Nuclear Imaging. Org. Biomol. Chem. 2014; 12: 9601-20; http://dx.doi.org/10.1039/C4OB01514B
55. Abada S, Lecointre A, Elhabiri M, Charbonniere LJ. Formation of very stable and selective Cu(II) complexes with a non-macrocyclic ligand: can basicity rival pre-organization? Dalton Trans 2010; 39:9055-62; http://dx.doi.org/10.1039/c0dt00453g
56. Aufderheide E, Ekblom P. Tenascin during gut development: appearance in the mesenchyme, shift in molecular forms, and dependence on epithelial-mesenchymal interactions. J Cell Biol 1988; 107:2341-9; http://dx.doi.org/10.1083/jcb.107.6.2341
57. Huijbers EJ, Ringvall M, Femel J, Kalamajski S, Lukinius A, Abrink M, Hellman L, Olsson AK. Vaccination against the extra domain-B of fibronectin as a novel tumor therapy. Faseb J 2010; 24:4535-44; http://dx.doi.org/10.1096/fj.10-163022
58. Femel J, Huijbers EJM, Saupe F, Cedervall J, Zhang L, Roswall P, Larsson E, Olofsson H, Pietras K, Dimberg A, et al. Therapeutic vaccination against fibronectin ED-A attenuates progression of metastatic breast cancer. Oncotarget 2014; 5:12418-27
59. Huijbers EJ. Development of a Cancer Vaccine Targeting Tumor Blood Vessels. 2012; ISBN: 987-91-554-8317-3
60. Dutoit V, Herold-Mende C, Hilf N, Schoor O, Beckhove P, Bucher J, Dorsch K, Flohr S, Fritsche J, Lewandrowski P, et al. Exploiting the glioblastoma peptidome to discover novel tumour-associated antigens for immunotherapy. Brain J Neurol 2012; 135:1042-54; http://dx.doi.org/10.1093/brain/aws042
61. Halford S, Rampling R, James A, Peoples S, Mulholland P, Al-Salihi O, Twelves C, McBain C, Jefferies S, Kutscher S, et al. Results from a cancer research UK first in man phase I trial of Ima950 (a novel multi peptide vaccine) plus Gm-Csf in patients with newly diagnosed glioblastoma. Ann Oncol 2014; 25:iv364-5
62. Immatics biotechnologies GmbH (2014). Promising results in phase 1 trial lead immatics to continue work on vaccine (IMA950) for glioblastoma. [Press release]. http://www.immatics.com/index.php?page=57&modaction=detail&modid=403&PHPSESSID= 03b364a73eeccf59034b3463a64245f0
63. Raghow R. The role of extracellular matrix in postinflammatory wound healing and fibrosis. FASEB J Off Publ Fed Am Soc Exp Biol 1994; 8:823-31
64. Delanian S, Lefaix J-L. The radiation-induced fibroatrophic process: therapeutic perspective via the antioxidant pathway. Radiother Oncol J Eur Soc Ther Radiol Oncol 2004; 73:119-31; http://dx.doi.org/10.1016/j.radonc.2004.08.021
65. Lafuma C, El Nabout RA, Crechet F, Hovnanian A, Martin M. Expression of 72-kDa gelatinase (MMP-2), collagenase (MMP-1), and tissue metalloproteinase inhibitor (TIMP) in primary pig skin fibroblast cultures derived from radiationinduced skin fibrosis. J Invest Dermatol 1994; 102:945-50; http://dx.doi.org/10.1111/1523-1747.ep12384118
66. Kis E, Szatmari T, Keszei M, Farkas R, Esik O, Lumniczky K, Falus A, Safrany G. Microarray analysis of radiation response genes in primary human fibroblasts. Int J Radiat Oncol Biol Phys 2006; 66:1506-14; http://dx.doi.org/10.1016/j.ijrobp.2006.08.004
67. Cordes N, van Beuningen D. Cell adhesion to the extracellular matrix protein fibronectin modulates radiation-dependent G2 phase arrest involving integrin-linked kinase (ILK) and glycogen synthase kinase-3beta (GSK-3beta) in vitro. Br J Cancer 2003; 88:1470-9; http://dx.doi.org/10.1038/sj.bjc.6600912
68. Ng Q-S, Goh V, Milner J, Padhani AR, Saunders MI, Hoskin PJ. Acute tumor vascular effects following fractionated radiotherapy in human lung cancer: In vivo whole tumor assessment using volumetric perfusion computed tomography. Int J Radiat Oncol Biol Phys 2007; 67:417-24; http://dx.doi.org/10.1016/j.ijrobp.2006.10.005
69. Nagata Y. Recent advances in radiation oncology. Int J Clin Oncol 2014; 19:563; http://dx.doi.org/10.1007/s10147-014-0720-4
70. Chino J, Das S, Wong T. Positron emission tomography in radiation treatment planning: the potential of metabolic imaging. Radiol Clin North Am 2013; 51:913-25; http://dx.doi.org/10.1016/j.rcl.2013.05.007
71. De Neve W, De Gersem W, Madani I. Rational use of intensity-modulated radiation therapy: the importance of clinical outcome. Semin Radiat Oncol 2012; 22:40-9; http://dx.doi.org/10.1016/j.semradonc.2011.09.003
72. Brada M, Bortfeld T. Proton therapy: the present and the future. Semin Radiat Oncol 2013; 23:75-6; http://dx.doi.org/10.1016/j.semradonc.2012.11.001
73. Lawrence WF. Comparative effectiveness research in practice and policy for radiation oncology. Semin Radiat Oncol 2014; 24:54-60; http://dx.doi.org/10.1016/j.semradonc.2013.09.001
74. Aneja S, Yu JB. Comparative effectiveness research in radiation oncology: stereotactic radiosurgery, hypofractionation, and brachytherapy. Semin Radiat Oncol 2014; 24:35-42; http://dx.doi.org/10.1016/j.semradonc.2013.08.004
75. Ahmad SS, Duke S, Jena R, Williams MV, Burnet NG. Advances in radiotherapy. BMJ 2012; 345: e7765; http://dx.doi.org/10.1136/bmj.e7765
76. Travis LB, Ng AK, Allan JM, Pui C-H, Kennedy AR, Xu XG, Purdy JA, Applegate K, Yahalom J, Constine LS, et al. Second malignant neoplasms and cardiovascular disease following radiotherapy. J Natl Cancer Inst 2012; 104:357-70; http://dx.doi.org/10.1093/jnci/djr533
77. Bristow RG. Introduction: DNA repair and radiotherapy targeting: an overview. Semin Radiat Oncol 2010; 20:215-6; http://dx.doi.org/10.1016/j.semradonc.2010.06.002
78. Garcia LM, Leblanc J, Wilkins D, Raaphorst GP. Fitting the linear-quadratic model to detailed data sets for different dose ranges. Phys Med Biol 2006; 51:2813-23; http://dx.doi.org/10.1088/0031-9155/51/11/009
79. Kirkpatrick JP, Meyer JJ, Marks LB. The linear-quadratic model is inappropriate to model high dose per fraction effects in radiosurgery. Semin Radiat Oncol 2008; 18:240-3; http://dx.doi.org/10.1016/j.semradonc.2008.04.005
80. Barcellos-Hoff MH, Park C, Wright EG. Radiation and the microenvironment -tumorigenesis and therapy. Nat Rev Cancer 2005; 5:867-75; http://dx.doi.org/10.1038/nrc1735
81. Kuonen F, Secondini C, Rüegg C. Molecular pathways: emerging pathways mediating growth, invasion, and metastasis of tumors progressing in an irradiated microenvironment. Clin Cancer Res Off J Am Assoc Cancer Res 2012; 18:5196-202; http://dx.doi.org/10.1158/1078-0432.CCR-11-1758
82. De Meerleer G, Khoo V, Escudier B, Joniau S, Bossi A, Ost P, Briganti A, Fonteyne V, Van Vulpen M, Lumen N, et al. Radiotherapy for renal-cell carcinoma. Lancet Oncol 2014; 15:e170-7; http://dx.doi.org/10.1016/S1470-2045(13)70569-2
83. Riekki R, Jukkola A, Oikarinen A, Kallioinen M. Radiation therapy induces tenascin expression and angiogenesis in human skin. Acta Derm Venereol 2001; 81:329-33; http://dx.doi.org/10.1080/000155501317140025
84. Bouchard G, Bouvette G, Therriault H, Bujold R, Saucier C, Paquette B. P re-irradiation of mouse mammary gland stimulates cancer cell migration and development of lung metastases. Br J Cancer 2013; 109:1829-38; http://dx.doi.org/10.1038/bjc.2013.502
85. Monnier Y, Farmer P, Bieler G, Imaizumi N, Sengstag T, Alghisi GC, Stehle J-C, Ciarloni L, Andrejevic-Blant S, Moeckli R, et al. CYR61 and alphaVbeta5 integrin cooperate to promote invasion and metastasis of tumors growing in preirradiated stroma. Cancer Res 2008; 68:7323-31; http://dx.doi.org/10.1158/0008-5472.CAN-08-0841
86. Geffrotin C, Tricaud Y, Crechet F, Castelli M, Lefaix JL, Vaiman M. Unlike tenascin-X, tenascin-C is highly up-regulated in pig cutaneous and underlying muscle tissue developing fibrosis after necrosis induced by very high-dose gamma radiation. Radiat Res 1998; 149:472-81; http://dx.doi.org/10.2307/3579787
87. Bartel-Friedrich S, Lautenschläger C, Holzhausen HJ, Friedrich RE. Expression and distribution of tenascin in rat submandibular glands following irradiation. Anticancer Res 2010; 30:1593-8
88. Hakim SG, Ribbat J, Berndt A, Richter P, Kosmehl H, Benedek GA, Jacobsen HC, Trenkle T, Sieg P, Rades D. Expression of Wnt-1, TGF-b and related cell-cell adhesion components following radiotherapy in salivary glands of patients with manifested radiogenic xerosto mia. Radiother Oncol J Eur Soc Ther Radiol Oncol 2011; 101:93-9; http://dx.doi.org/10.1016/j.radonc.2011.07.032
89. Beutel J, Schroder C, von Hof K, Rades D, Kosmehl H, Wedel T, Sieg P, Geerling G, Hakim SG. Pharmacological prevention of radiation-induced dry eye-an experimental study in a rabbit model. Graefes Arch Clin Exp Ophthalmol Albrecht Von Graefes Arch Für Klin Exp Ophthalmol 2007; 245:1347-55; http://dx.doi.org/10.1007/s00417-007-0548-y
90. Li XA. Adaptive Radiation Therapy. CRC Press; 2011; ISBN: 9781439816356
91. Vujaskovic Z, Anscher MS, Feng QF, Rabbani ZN, Amin K, Samulski TS, Dewhirst MW, Haroon ZA. Radiation-induced hypoxia may perpetuate late normal tissue injury. Int J Radiat Oncol Biol Phys 2001; 50:851-5; http://dx.doi.org/10.1016/S0360-3016(01)01593-0
92. Rubner Y, Wunderlich R, Rühle P-F, Kulzer L, Werthmöller N, Frey B, Weiss E-M, Keilholz L, Fietkau R, Gaipl US. How does ionizing irradiation contribute to the induction of anti-tumor immunity? Front Oncol 2012; 2:75; http://dx.doi.org/10.3389/fonc.2012.00075
93. Udalova IA, Ruhmann M, Thomson SJP, Midwood KS. Expression and immune function of tenascin-C. Crit Rev Immunol 2011; 31:115-45; http://dx.doi.org/10.1615/CritRevImmunol.v31.i2.30
94. Symon Z, Goldshmidt Y, Picard O, Yavzori M, Ben-Horin S, Alezra D, Barshack I, Chowers Y. A murine model for the study of molecular pathogenesis of radiation proctitis. Int J Radiat Oncol Biol Phys 2010; 76:242-50; http://dx.doi.org/10.1016/j.ijrobp.2009.07.1736
95. Dancea HC, Shareef MM, Ahmed MM. Role of radiation-induced TGF-beta signaling in cancer therapy. Mol Cell Pharmacol 2009; 1:44-56; http://dx.doi.org/10.4255/mcpharmacol.09.06
96. Bierie B, Moses HL. Transforming growth factor beta (TGF-beta) and inflammation in cancer. Cytokine Growth Factor Rev 2010; 21:49-59; http://dx.doi.org/10.1016/j.cytogfr.2009.11.008
97. Jinnin M, Ihn H, Asano Y, Yamane K, Trojanowska M, Tamaki K. Tenascin-C upregulation by transforming growth factor-b in human dermal fibroblasts involves Smad3, Sp1, and Ets1. Oncogene 2004; 23:1656-67; http://dx.doi.org/10.1038/sj.onc.1207064
98. Katoh D, Nagaharu K, Shimojo N, Hanamura N, Yamashita M, Kozuka Y, Imanaka-Yoshida K, Yoshida T. Binding of avb1 and avb6 integrins to tenascin-C induces epithelial-mesenchymal transition-like change of breast cancer cells. Oncogenesis 2013; 2: e65; http://dx.doi.org/10.1038/oncsis.2013.27
99. De Laporte L, Rice JJ, Tortelli F, Hubbell JA. Tenascin C promiscuously binds growth factors via its fifth fibronectin type III-like domain. PloS One 2013; 8: e62076; http://dx.doi.org/10.1371/journal.pone.0062076
100. Gulbins E. Regulation of death receptor signaling and apoptosis by ceramide. Pharmacol Res Off J Ital Pharmacol Soc 2003; 47:393-9
101. Logsdon EA, Finley SD, Popel AS, Gabhann FM. A systems biology view of blood vessel growth and remodelling. J Cell Mol Med 2014; 18:1491-508; http://dx.doi.org/10.1111/jcmm.12164
102. Imaizumi N, Monnier Y, Hegi M, Mirimanoff R-O, Rüegg C. Radiotherapy suppresses angiogenesis in mice through TGF-betaRI/ALK5-dependent inhibition of endothelial cell sprouting. PloS One 2010; 5: e11084; http://dx.doi.org/10.1371/journal.pone.0011084
103. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev 2004; 25:581-611; http://dx.doi.org/10.1210/er.2003-0027
104. Goel HL, Mercurio AM. VEGF targets the tumour cell. Nat Rev Cancer 2013; 13:871-82; http://dx.doi.org/10.1038/nrc3627
105. O’Connell JT, Sugimoto H, Cooke VG, MacDonald BA, Mehta AI, LeBleu VS, Dewar R, Rocha RM, Brentani RR, Resnick MB, et al. VEGF-A and tenascin-C produced by S100A4C stromal cells are important for metastatic colonization. Proc Natl Acad Sci U S A 2011; 108:16002-7; http://dx.doi.org/10.1073/pnas.1109493108
106. Helleman J, Jansen MPHM, Ruigrok-Ritstier K, van Staveren IL, Look MP, Meijer-van Gelder ME, Sieuwerts AM, Klijn JGM, Sleijfer S, Foekens JA, et al. Association of an extracellular matrix gene cluster with breast cancer prognosis and endocrine therapy response. Clin Cancer Res Off J Am Assoc Cancer Res 2008; 14:5555-64; http://dx.doi.org/10.1158/1078-0432.CCR-08-0555
107. Mancuso MR, Davis R, Norberg SM, O’Brien S, Sennino B, Nakahara T, Yao VJ, Inai T, Brooks P, Freimark B, et al. Rapid vascular regrowth in tumors after reversal of VEGF inhibition. J Clin Invest 2006; 116:2610-21; http://dx.doi.org/10.1172/JCI24612
108. Huang W, Chiquet-Ehrismann R, Moyano JV, Garcia-Pardo A, Orend G. Interference of tenascin-C with syndecan-4 binding to fibronectin blocks cell adhesion and stimulates tumor cell proliferation. Cancer Res 2001; 61:8586-94
109. De Wever O, Sobczak-Thepot J, Vercoutter-Edouart A-S, Michalski J-C, Ouelaa-Benslama R, Stupack DG, Bracke M, Wang JYJ, Gespach C, Emami S. Priming and potentiation of DNA damage response by fibronectin in human colon cancer cells and tumor-derived myofibroblasts. Int J Oncol 2011; 39:393-400
110. McManus KJ, Hendzel MJ. ATM-dependent DNA damage-independent mitotic phosphorylation of H2AX in normally growing mammalian cells. Mol Biol Cell 2005; 16:5013-25; http://dx.doi.org/10.1091/mbc.E05-01-0065
111. Ruiz C, Huang W, Hegi ME, Lange K, Hamou M-F, Fluri E, Oakeley EJ, Chiquet-Ehrismann R, Orend G. Growth promoting signaling by tenascin-C [corrected]. Cancer Res 2004; 64:7377-85
112. Gosepath EM, Eckstein N, Hamacher A, Servan K, von Jonquieres G, Lage H, Györffy B, Royer HD, Kassack MU. Acquired cisplatin resistance in the head-neck cancer cell line Cal27 is associated with decreased DKK1 expression and can partially be reversed by overexpression of DKK1. Int J Cancer J Int Cancer 2008; 123:2013-9; http://dx.doi.org/10.1002/ijc.23721
113. Shou J, Ali-Osman F, Multani AS, Pathak S, Fedi P, Srivenugopal KS. Human Dkk-1, a gene encoding a Wnt antagonist, responds to DNA damage and its overexpression sensitizes brain tumor cells to apoptosis following alkylation damage of DNA. Oncogene 2002; 21:878-89; http://dx.doi.org/10.1038/sj.onc.1205138
114. Niehrs C. Function and biological roles of the Dickkopf family of Wnt modulators. Oncogene 2006; 25:7469-81; http://dx.doi.org/10.1038/sj.onc.1210054
115. Reardon DA, Akabani G, Coleman RE, Friedman AH, Friedman HS, Herndon JE, McLendon RE, Pegram CN, Provenzale JM, Quinn JA, et al. Salvage radioimmunotherapy with murine iodine-131-labeled antitenascin monoclonal antibody 81C6 for patients with recurrent primary and metastatic malignant brain tumors: phase II study results. J Clin Oncol 2006; 24:115-22; http://dx.doi.org/10.1200/JCO.2005.03.4082
116. Reardon DA, Zalutsky MR, Akabani G, Coleman RE, Friedman AH, Herndon JE, McLendon RE, Pegram CN, Quinn JA, Rich JN, et al. A pilot study: 131Iantitenascin monoclonal antibody 81c6 to deliver a 44-Gy resection cavity boost. Neuro Oncol 2008; 10:182-9; http://dx.doi.org/10.1215/15228517-2007-053
117. Zalutsky MR, Reardon DA, Akabani G, Coleman RE, Friedman AH, Friedman HS, McLendon RE, Wong TZ, Bigner DD. Clinical experience with alpha-particle emitting 211At: treatment of recurrent brain tumor patients with 211At-labeled chimeric antitenascin monoclonal antibody 81C6. J Nucl Med 2008; 49:30-8; http://dx.doi.org/10.2967/jnumed.107.046938
118. Riva P, Arista A, Tison V, Sturiale C, Franceschi G, Spinelli A, Riva N, Casi M, Moscatelli G, Frattarelli M. Intralesional radioimmunotherapy of malignant gliomas. An effective treatment in recurrent tumors. Cancer 1994; 73:1076-82; http://dx.doi.org/10.1002/1097-0142(19940201)73:3C%3c1076::AIDCNCR2820731347%3e3.0.CO;2-Z
119. Paganelli G, Bartolomei M, Ferrari M, Cremonesi M, Broggi G, Maira G, Sturiale C, Grana C, Prisco G, Gatti M, et al. Pre-targeted locoregional radioimmunotherapy with 90Y-biotin in glioma patients: phase I study and preliminary therapeutic results. Cancer Biother Radiopharm 2001; 16:227-35; http://dx.doi.org/10.1089/10849780152389410