Critical review in oral biology and medicine: Sensitivity of salivary glands to radiation: From animal models to therapies

Journal of Dental Research

Volumn 88, Issue 10, 2009, Pages 894-903

  Grundmann, O ^a   Mitchell, G C ^b   Limesand, K H ^a,b  

^a Cancer Biology Program   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Animal models; Radiation; Salivary gland dysfunction; Salivary glands; Therapy; Xerostomia.

Indexed keywords

RADIOPROTECTIVE AGENT;

ANIMAL; APOPTOSIS; COMPARATIVE STUDY; DISEASE MODEL; HEAD AND NECK TUMOR; HUMAN; PHYSIOLOGY; RADIATION DOSE; RADIATION EXPOSURE; RADIATION INJURY; RADIOTHERAPY; REVIEW; SALIVARY GLAND; SALIVARY GLAND DISEASE; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; DISEASE MODELS, ANIMAL; HEAD AND NECK NEOPLASMS; HUMANS; RADIATION INJURIES; RADIATION TOLERANCE; RADIATION-PROTECTIVE AGENTS; RADIOTHERAPY; RADIOTHERAPY DOSAGE; SALIVARY GLAND DISEASES; SALIVARY GLANDS; SIGNAL TRANSDUCTION;

EID: 70349792245     PISSN: 00220345     EISSN: 15440591     Source Type: Journal    
DOI: 10.1177/0022034509343143     Document Type: Article

References (104)

1. Anne PR (2002). Phase II trial of subcutaneous amifostine in patients undergoing radiation therapy for head and neck cancer. Semin Oncol 29 (6 Suppl 19). 80-83 ; erratum in Semin Oncol 30: 417, 2003.
2. Avila JL, Grundmann O., Burd R., Limesand KH (2009). Radiation-induced salivary gland dysfunction results from p53-dependent apoptosis. Int J Radiat Oncol Biol Phys 73: 523-529.
3. Bao S., Wu Q., McLendon RE, Hao Y., Shi Q., Hjelmeland AB, et al. (2006). Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444: 756-760.
4. Baum BJ, Zheng C., Cotrim AP, Goldsmith CM, Atkinson JC, Brahim JS, et al. (2006). Transfer of the AQP1 cDNA for the correction of radiation-induced salivary hypofunction. Biochim Biophys Acta 1758: 1071-1077.
5. Braam PM, Terhaard CH, Roesink JM, Raaijmakers CP (2006). Intensity-modulated radiotherapy significantly reduces xerostomia compared with conventional radiotherapy. Int J Radiat Oncol Biol Phys 66: 975-980.
6. Bralic M., Muhvic-Urek M., Stemberga V., Golemac M., Jurkovic S., Borcic J., et al. (2005). Cell death and cell proliferation in mouse submandibular gland during early post-irradiation phase. Acta Med Okayama 59: 153-159.
7. Brizel DM, Wasserman TH, Henke M., Strnad V., Rudat V., Monnier A., et al. (2000). Phase III randomized trial of amifostine as a radioprotector in head and neck cancer. J Clin Oncol 18: 3339-3345.
8. Brizel DM, Murphy BA, Rosenthal DI, Pandya KJ, Gluck S., Brizel HE, et al. (2008). Phase II study of palifermin and concurrent chemoradiation in head and neck squamous cell carcinoma. J Clin Oncol 26: 2489-2496.
9. Bussels B., Maes A., Flamen P., Lambin P., Erven K., Hermans R., et al. (2004). Dose-response relationships within the parotid gland after radiotherapy for head and neck cancer. Radiother Oncol 73: 297-306.
10. Cady J. (2007). Nutritional support during radiotherapy for head and neck cancer: the role of prophylactic feeding tube placement. Clin J Oncol Nurs 11: 875-880.
11. Calabro-Jones PM, Fahey RC, Smoluk GD, Ward JF (1985). Alkaline phosphatase promotes radioprotection and accumulation of WR-1065 in V79-171 cells incubated in medium containing WR-2721. Int J Radiat Biol Relat Stud Phys Chem Med 47: 23-27.
12. Cannon DM, Lee NY (2008). Recurrence in region of spared parotid gland after definitive intensity-modulated radiotherapy for head and neck cancer. Int J Radiat Oncol Biol Phys 70: 660-665.
13. Chambers MS, Posner M., Jones CU, Biel MA, Hodge KM, Vitti R., et al. (2007 a). Cevimeline for the treatment of postirradiation xerostomia in patients with head and neck cancer. Int J Radiat Oncol Biol Phys 68: 1102-1109. (Pubitemid 47053952)
14. Chambers MS, Jones CU, Biel MA, Weber RS, Hodge KM, Chen Y., et al. (2007 b). Open-label, long-term safety study of cevimeline in the treatment of postirradiation xerostomia. Int J Radiat Oncol Biol Phys 69: 1369-1376.
15. Coppes RP, Roffel AF, Zeilstra LJ, Vissink A., Konings AW (2000). Early radiation effects on muscarinic receptor-induced secretory responsiveness of the parotid gland in the freely moving rat. Radiat Res 153: 339-346.
16. Coppes RP, Meter A., Latumalea SP, Roffel AF, Kampinga HH (2005). Defects in muscarinic receptor-coupled signal transduction in isolated parotid gland cells after in vivo irradiation: evidence for a non-DNA target of radiation. Br J Cancer 92: 539-546.
17. Cotrim AP, Baum BJ (2008). Gene therapy: some history, applications, problems, and prospects. Toxicol Pathol 36: 97-103.
18. Cotrim AP, Hyodo F., Matsumoto K., Sowers AL, Cook JA, Baum BJ, et al. (2007 a). Differential radiation protection of salivary glands versus tumor by Tempol with accompanying tissue assessment of Tempol by magnetic resonance imaging. Clin Cancer Res 13: 4928-4933.
19. Cotrim AP, Sowers A., Mitchell JB, Baum BJ (2007 b). Prevention of irradiation-induced salivary hypofunction by microvessel protection in mouse salivary glands. Mol Ther 15: 2101-2106.
20. de Almeida PdelV, Gr?©gio AM, Machado MA, Soares de Lima AA, Azevedo LR (2008). Saliva composition and functions: a comprehensive review. J Contemp Dent Pract 9 (3). 72-80.
21. Delporte C., Oĝ€™Connell BC, He X., Lancaster HE, Oĝ€™Connell AC, Agre P., et al. (1997). Increased fluid secretion after adenoviral-mediated transfer of the aquaporin-1 cDNA to irradiated rat salivary glands. Proc Natl Acad Sci USA 94: 3268-3273.
22. Denny PC, Denny PA (1999). Dynamics of parenchymal cell division, differentiation, and apoptosis in the young adult female mouse submandibular gland. Anat Rec 254: 408-417.
23. Dirix P., Nuyts S., Van den Bogaert W. (2006). Radiation-induced xerostomia in patients with head and neck cancer: a literature review. Cancer 107: 2525-2534.
24. Eisbruch A., Ten Haken RK, Kim HM, Marsh LH, Ship JA (1999). Dose, volume, and function relationships in parotid salivary glands following conformal and intensity-modulated irradiation of head and neck cancer. Int J Radiat Oncol Biol Phys 45: 577-587.
25. Eisbruch A., Kim HM, Terrell JE, Marsh LH, Dawson LA, Ship JA (2001). Xerostomia and its predictors following parotid-sparing irradiation of head-and-neck cancer. Int J Radiat Oncol Biol Phys 50: 695-704.
26. Friedrich RE, Bartel-Friedrich S., Holzhausen HJ, Lautenschlager C. (2002). The effect of external fractionated irradiation on the distribution pattern of extracellular matrix proteins in submandibular salivary glands of the rat. J Craniomaxillofac Surg 30: 246-254.
27. Grisius MM, Fox PC (1998). Salivary gland dysfunction and xerostomia. Front Oral Biol 9: 156-167.
28. Gudkov AV, Komarova EA (2003). The role of p53 in determining sensitivity to radiotherapy. Nat Rev Cancer 3: 117-129.
29. Hall E. (2000). Radiobiology for the radiologist. 5 th ed. Philadelphia: Lippincott, Williams and Wilkins.
30. Hancock PJ, Epstein JB, Sadler GR (2003). Oral and dental management related to radiation therapy for head and neck cancer. J Can Dent Assoc 69: 585-590.
31. Henson BS, Eisbruch A., Dĝ€™Hondt E., Ship JA (1999). Two-year longitudinal study of parotid salivary flow rates in head and neck cancer patients receiving unilateral neck parotid-sparing radiotherapy treatment. Oral Oncol 35: 234-241.
32. Hoebers FJ, Kartachova M., de Bois J., van den Brekel MW, van Tinteren H., van Herk M., et al. (2008). 99mTc Hynic-rh-Annexin V scintigraphy for in vivo imaging of apoptosis in patients with head and neck cancer treated with chemoradiotherapy. Eur J Nucl Med Mol Imaging 35: 509-518.
33. Horn HF, Vousden KH (2007). Coping with stress: multiple ways to activate p53. Oncogene 26: 1306-1316.
34. Humphries MJ, Limesand KH, Schneider JC, Nakayama KI, Anderson SM, Reyland ME (2006). Suppression of apoptosis in the PKCdelta null mouse in vivo. J Biol Chem 281: 9728-9737.
35. Jemal A., Siegel R., Ward E., Hao Y., Xu J., Murray T., et al. (2008). Cancer statistics, 2008. CA Cancer J Clin 58: 71-96.
36. Kaplan I., Zuk-Paz L., Wolff A. (2008). Association between salivary flow rates, oral symptoms, and oral mucosal status. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 106: 235-241.
37. Konings AW, Cotteleer F., Faber H., van Luijk P., Meertens H., Coppes RP (2005 a). Volume effects and region-dependent radiosensitivity of the parotid gland. Int J Radiat Oncol Biol Phys 62: 1090-1095.
38. Konings AW, Coppes RP, Vissink A. (2005 b). On the mechanism of salivary gland radiosensitivity. Int J Radiat Oncol Biol Phys 62: 1187-1194 ; erratum in Int J Radiat Oncol Biol Phys 64: 330, 2006.
39. Konings AW, Faber H., Cotteleer F., Vissink A., Coppes RP (2006). Secondary radiation damage as the main cause for unexpected volume effects: a histopathologic study of the parotid gland. Int J Radiat Oncol Biol Phys 64: 98-105.
40. Koukourakis MI, Kyrias G., Kakolyris S., Kouroussis C., Frangiadaki C., Giatromanolaki A., et al. (2000). Subcutaneous administration of amifostine during fractionated radiotherapy: a randomized phase II study. J Clin Oncol 18: 2226-2233.
41. Krysko DV, Vanden Berghe T., Dĝ€™Herde K., Vandenabeele P. (2008). Apoptosis and necrosis: detection, discrimination and phagocytosis. Methods 44: 205-221.
42. Li J., Shan Z., Ou G., Liu X., Zhang C., Baum BJ, et al. (2005). Structural and functional characteristics of irradiation damage to parotid glands in the miniature pig. Int J Radiat Oncol Biol Phys 62: 1510-1516.
43. Li Y., Taylor JM, Ten Haken RK, Eisbruch A. (2007). The impact of dose on parotid salivary recovery in head and neck cancer patients treated with radiation therapy. Int J Radiat Oncol Biol Phys 67: 660-669.
44. Li Z., Zhao D., Gong B., Xu Y., Sun H., Yang B., et al. (2006). Decreased saliva secretion and down-regulation of AQP5 in submandibular gland in irradiated rats. Radiat Res 165: 678-687.
45. Limesand KH, Barzen KA, Quissell DO, Anderson SM (2003 a). Synergistic suppression of apoptosis in salivary acinar cells by IGF1 and EGF. Cell Death Differ 10: 345-355.
46. Limesand KH, Barzen KA, Sanders LA, Sclafani RA, Raynolds MV, Reyland ME, et al. (2003 b). Characterization of rat parotid and submandibular acinar cell apoptosis in primary culture. In Vitro Cell Dev Biol Anim 39: 170-177.
47. Limesand KH, Schwertfeger KL, Anderson SM (2006). MDM2 is required for suppression of apoptosis by activated Akt1 in salivary acinar cells. Mol Cell Biol 26: 8840-8856.
48. Limesand KH, Siad S., Anderson SM (2009). Suppression of radiation-induced salivary gland dysfunction by IGF-1. PLoS One 4 (3). e4663.
49. Lindegaard JC, Grau C. (2000). Has the outlook improved for amifostine as a clinical radioprotector ? Radiother Oncol 57: 113-118.
50. Lombaert IM, Brunsting JF, Wierenga PK, Faber H., Stokman MA, Kok T., et al. (2008). Rescue of salivary gland function after stem cell transplantation in irradiated glands. PLoS ONE 3 (4). e2063.
51. Makkonen TA, Tenovuo J., Vilja P., Heimdahl A. (1986). Changes in the protein composition of whole saliva during radiotherapy in patients with oral or pharyngeal cancer. Oral Surg Oral Med Oral Pathol 62: 270-275.
52. Malouf JG, Aragon C., Henson BS, Eisbruch A., Ship JA (2003). Influence of parotid-sparing radiotherapy on xerostomia in head and neck cancer patients. Cancer Detect Prev 27: 305-310.
53. Man YG, Ball WD, Marchetti L., Hand AR (2001). Contributions of intercalated duct cells to the normal parenchyma of submandibular glands of adult rats. Anat Rec 263: 202-214.
54. Manning BD, Cantley LC (2007). AKT/PKB signaling: navigating downstream. Cell 129: 1261-1274.
55. Martinet W., De Meyer GR, Andries L., Herman AG, Kockx MM (2006). Detection of autophagy in tissue by standard immunohistochemistry: possibilities and limitations. Autophagy 2: 55-57.
56. Muhvic-Urek M., Bralic M., Curic S., Pezelj-Ribaric S., Borcic J., Tomac J. (2006). Imbalance between apoptosis and proliferation causes late radiation damage of salivary gland in mouse. Physiol Res 55: 89-95.
57. Murdoch-Kinch CA, Kim HM, Vineberg KA, Ship JA, Eisbruch A. (2008). Dose-effect relationships for the submandibular salivary glands and implications for their sparing by intensity modulated radiotherapy. Int J Radiat Oncol Biol Phys 72: 373-382.
58. Nagler RM (1998). Short- and long-term functional vs morphometrical salivary effects of irradiation in a rodent model. Anticancer Res 18 (1A). 315-320.
59. Nagler RM, Laufer D. (1998). Protection against irradiation-induced damage to salivary glands by adrenergic agonist administration. Int J Radiat Oncol Biol Phys 40: 477-481.
60. Nagler R., Marmary Y., Fox PC, Baum BJ, Har-El R., Chevion M. (1997). Irradiation-induced damage to the salivary glands: the role of redox-active iron and copper. Radiat Res 147: 468-476.
61. Nagler RM, Baum BJ, Miller G., Fox PC (1998). Long-term salivary effects of single-dose head and neck irradiation in the rat. Arch Oral Biol 43: 297-303.
62. Nguyen NP, Vos P., Karlsson U., Nguyen P., Dutta S., Lemanski C., et al. (2007). Quality of life following chemoradiation and postoperative radiation for locally advanced head and neck cancer. ORL J Otorhinolaryngol Relat Spec 69: 271-276. (Pubitemid 47360929)
63. Oĝ€™Connell AC, Lillibridge CD, Zheng C., Baum BJ, Oĝ€™Connell BC, Ambudkar IS (1998). Gamma-irradiation-induced cell cycle arrest and cell death in a human submandibular gland cell line: effect of E2F1 expression. J Cell Physiol 177: 264-273.
64. Oĝ€™Connell AC, Baccaglini L., Fox PC, Oĝ€™Connell BC, Kenshalo D., Oweisy H., et al. (1999 a). Safety and efficacy of adenovirus-mediated transfer of the human aquaporin-1 cDNA to irradiated parotid glands of non-human primates. Cancer Gene Ther 6: 505-513.
65. Oĝ€™Connell AC, Redman RS, Evans RL, Ambudkar IS (1999 b). Radiation-induced progressive decrease in fluid secretion in rat submandibular glands is related to decreased acinar volume and not impaired calcium signaling. Radiat Res 151: 150-158.
66. Ogata M., Hino S., Saito A., Morikawa K., Kondo S., Kanemoto S., et al. (2006). Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 26: 9220-9231.
67. Ogawara Y., Kishishita S., Obata T., Isazawa Y., Suzuki T., Tanaka K., et al. (2002). Akt enhances Mdm2-mediated ubiquitination and degradation of p53. J Biol Chem 277: 21843-21850.
68. Paardekooper GM, Cammelli S., Zeilstra LJ, Coppes RP, Konings AW (1998). Radiation-induced apoptosis in relation to acute impairment of rat salivary gland function. Int J Radiat Biol 73: 641-648.
69. Pinkstaff CA (1992). Cytology, histology, and histochemistry of salivary glands: an overview. In: Biology of the salivary glands. Dobrosielski-Vergona K, editor. Boca Raton: CRC Press, pp. 15-38.
70. Potten CS (2004). Radiation, the ideal cytotoxic agent for studying the cell biology of tissues such as the small intestine. Radiat Res 161: 123-136.
71. Proctor GB, Carpenter GH (2007). Regulation of salivary gland function by autonomic nerves. Auton Neurosci 133: 3-18.
72. Rachidi W., Harfourche G., Lemaitre G., Amiot F., Vaigot P., Martin MT (2007). Sensing radiosensitivity of human epidermal stem cells. Radiother Oncol 83: 267-276.
73. Rades D., Fehlauer F., Bajrovic A., Mahlmann B., Richter E., Alberti W. (2004). Serious adverse effects of amifostine during radiotherapy in head and neck cancer patients. Radiother Oncol 70: 261-264.
74. Radfar L., Sirois DA (2003). Structural and functional injury in minipig salivary glands following fractionated exposure to 70 Gy of ionizing radiation: an animal model for human radiation-induced salivary gland injury. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 96: 267-274.
75. Reyland ME (2007). Protein kinase Cdelta and apoptosis. Biochem Soc Trans 35 (Pt 5). 1001-1004.
76. Riedl SJ, Shi Y. (2004). Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol 5: 897-907.
77. Rieger K., Marinets O., Fietz T., Korper S., Sommer D., Mucke C., et al. (2005). Mesenchymal stem cells remain of host origin even a long time after allogeneic peripheral blood stem cell or bone marrow transplantation. Exp Hematol 33: 605-611.
78. Riley T., Sontag E., Chen P., Levine A. (2008). Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 9: 402-412.
79. Robar JL, Day A., Clancey J., Kelly R., Yewondwossen M., Hollenhorst H., et al. (2007). Spatial and dosimetric variability of organs at risk in head-and-neck intensity-modulated radiotherapy. Int J Radiat Oncol Biol Phys 68: 1121-1130.
80. Roesink JM, Moerland MA, Hoekstra A., Van Rijk PP, Terhaard CH (2004). Scintigraphic assessment of early and late parotid gland function after radiotherapy for head-and-neck cancer: a prospective study of dose-volume response relationships. Int J Radiat Oncol Biol Phys 58: 1451-1460.
81. Rubin P., Casarett G. (1968). Clinical radiation pathology. Philadelphia: WB Saunders.
82. Rudat V., Meyer J., Momm F., Bendel M., Henke M., Strnad V., et al. (2000). Protective effect of amifostine on dental health after radiotherapy of the head and neck. Int J Radiat Oncol Biol Phys 48: 1339-1343.
83. Sagowski C., Wenzel S., Tesche S., Jenicke L., Jaehne M. (2003). Investigation of radiosialadenitis during fractioned irradiation: sialoscintigraphical and histomorphological findings in rats. Eur Arch Otorhinolaryngol 260: 513-517.
84. Savill J., Fadok V., Henson P., Haslett C. (1993). Phagocyte recognition of cells undergoing apoptosis. Immunol Today 14: 131-136.
85. Seiwert TY, Cohen EE (2005). State-of-the-art management of locally advanced head and neck cancer. Br J Cancer 92: 1341-1348.
86. Seiwert TY, Salama JK, Vokes EE (2007). The chemoradiation paradigm in head and neck cancer. Nat Clin Pract Oncol 4: 156-171.
87. Shan Z., Li J., Zheng C., Liu X., Fan Z., Zhang C., et al. (2005). Increased fluid secretion after adenoviral-mediated transfer of the human aquaporin-1 cDNA to irradiated miniature pig parotid glands. Mol Ther 11: 444-451.
88. Ship JA, Fox PC, Baum BJ (1991). How much saliva is enough? ĝ€?Normalĝ€™ function defined. J Am Dent Assoc 122 (3). 63-69.
89. St John MA, Abemayor E, Wong DT (2006). Recent new approaches to the treatment of head and neck cancer. Anticancer Drugs 17:365-375.
90. Stephens LC, Ang KK, Schultheiss TE, King GK, Brock WA, Peters LJ (1986a). Target cell and mode of radiation injury in rhesus salivary glands. Radiother Oncol 7:165-174.
91. Stephens LC, King GK, Peters LJ, Ang KK, Schultheiss TE, Jardine JH (1986 b). Acute and late radiation injury in rhesus monkey parotid glands. Evidence of interphase cell death. Am J Pathol 124: 469-478.
92. Stephens LC, Schultheiss TE, Small SM, Ang KK, Peters LJ (1989). Response of parotid gland organ culture to radiation. Radiat Res 120: 140-153.
93. Stephens LC, Schultheiss TE, Price RE, Ang KK, Peters LJ (1991). Radiation apoptosis of serous acinar cells of salivary and lacrimal glands. Cancer 67: 1539-1543.
94. Takakura K., Takaki S., Takeda I., Hanaue N., Kizu Y., Tonogi M., et al. (2007). Effect of cevimeline on radiation-induced salivary gland dysfunction and AQP5 in submandibular gland in mice. Bull Tokyo Dent Coll 48 (2). 47-56.
95. Thula TT, Schultz G., Tran-Son-Tay R., Batich C. (2005). Effects of EGF and bFGF on irradiated parotid glands. Ann Biomed Eng 33: 685-695.
96. Tran SD, Sugito T., Dipasquale G., Cotrim AP, Bandyopadhyay BC, Riddle K., et al. (2006). Re-engineering primary epithelial cells from rhesus monkey parotid glands for use in developing an artificial salivary gland. Tissue Eng 12: 2939-2948.
97. Trotti A., Bellm LA, Epstein JB, Frame D., Fuchs HJ, Gwede CK, et al. (2003). Mucositis incidence, severity and associated outcomes in patients with head and neck cancer receiving radiotherapy with or without chemotherapy: a systematic literature review. Radiother Oncol 66: 253-262.
98. Turner RJ (1993). Mechanisms of fluid secretion by salivary glands. Ann NY Acad Sci 694: 24-35.
99. Utley JF, Marlowe C., Waddell WJ (1976). Distribution of 35S-labeled WR-2721 in normal and malignant tissues of the mouse1,2. Radiat Res 68: 284-291.
100. Vissink A., ĝ€?s- Gravenmade EJ, Ligeon EE, Konings WT (1990). A functional and chemical study of radiation effects on rat parotid and submandibular/ sublingual glands. Radiat Res 124: 259-265.
101. Woodward WA, Chen MS, Behbod F., Alfaro MP, Buchholz TA, Rosen JM (2007). WNT/beta-catenin mediates radiation resistance of mouse mammary progenitor cells. Proc Natl Acad Sci USA 104: 618-623 ; erratum in Proc Natl Acad Sci USA 104: 7307, 2007.
102. Zhao Y., Zhan Y., Burke KA, Anderson WF (2005). Soluble factor(s) from bone marrow cells can rescue lethally irradiated mice by protecting endogenous hematopoietic stem cells. Exp Hematol 33: 428-434.
103. Zheng C., Hoque AT, Braddon VR, Baum BJ, Oĝ€™Connell BC (2001). Evaluation of salivary gland acinar and ductal cell-specific promoters in vivo with recombinant adenoviral vectors. Hum Gene Ther 12: 2215-2223.
104. Zheng C., Vitolo JM, Zhang W., Mineshiba F., Chiorini JA, Baum BJ (2008). Extended transgene expression from a nonintegrating adenoviral vector containing retroviral elements. Mol Ther 16: 1089-1097.