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Original Articles

TGF-β3 increases the severity of radiation-induced oral mucositis and salivary gland fibrosis in a mouse model

ORCID Icon, , ORCID Icon, , , & show all
Pages 767-776 | Received 17 Sep 2023, Accepted 06 Feb 2024, Published online: 05 Mar 2024

References

  • Annes JP, Munger JS, Rifkin DB. 2003. Making sense of latent TGFbeta activation. J Cell Sci. 116(Pt 2):217–224. doi:10.1242/JCS.00229
  • Ask K, Bonniaud P, Maass K, Eickelberg O, Margetts PJ, Warburton D, Groffen J, Gauldie J, Kolb M. 2008. Progressive pulmonary fibrosis is mediated by TGF-β isoform 1 but not TGF-β3. Int J Biochem Cell Biol. 40(3):484–495. doi:10.1016/j.biocel.2007.08.016
  • Barcellos-Hoff MH. 2022. The radiobiology of TGFβ. Semin Cancer Biol. 86(Pt 3):857–867. doi:10.1016/j.semcancer.2022.02.001
  • Booth D, Haley JD, Bruskin AM, Potten CS. 2000. Transforming growth factor-B3 protects murine small intestinal stem cells and animal survival after irradiation, possibly by reducing stem-cell cycling. Int J Cancer. 86(1):53–59. doi:10.1002/(sici)1097-0215(20000401)86:1<53::aid-ijc8>3.0.co;2-z
  • Boria AJ, Perez-Torres CJ, Perez-Torres CJ. 2020. Impact of mouse strain and sex when modeling radiation necrosis. Radiat Oncol. 15(1):141. doi:10.1186/s13014-020-01585-5
  • Bush J, Duncan JAL, Bond JS, Durani P, So K, Mason T, O'Kane S, Ferguson MWJ. 2010. Scar-improving efficacy of avotermin administered into the wound margins of skin incisions as evaluated by a randomized, double-blind, placebo-controlled, phase II clinical trial. Plast Reconstr Surg. 126(5):1604–1615. doi:10.1097/PRS.0b013e3181ef8e66
  • Cancedda R, Mastrogiacomo M. 2023. Transit amplifying cells (TACs): a still not fully understood cell population. Front Bioeng Biotechnol. 11:1189225. doi:10.3389/fbioe.2023.1189225
  • Chang Z, Kishimoto Y, Hasan A, Welham NV. 2014. TGF-β3 modulates the inflammatory environment and reduces scar formation following vocal fold mucosal injury in rats. Dis Model Mech. 7(1):83–91. doi:10.1242/dmm.013326
  • Choi JS, Park IS, Kim SK, Lim JY, Kim YM. 2013. Analysis of age-related changes in the functional morphologies of salivary glands in mice. Arch Oral Biol. 58(11):1635–1642. doi:10.1016/J.ARCHORALBIO.2013.07.008
  • Du X, Cai L, Xie J, Zhou X. 2023. The role of TGF-beta3 in cartilage development and osteoarthritis. Bone Res. 11(1):2. doi:10.1038/s41413-022-00239-4
  • Escasany E, Lanzón B, García-Carrasco A, Izquierdo-Lahuerta A, Torres L, Corrales P, Rodríguez Rodríguez AE, Luis-Lima S, Martínez Álvarez C, Javier Ruperez F, et al. 2021. Transforming growth factor β 3 deficiency promotes defective lipid metabolism and fibrosis in murine kidney. Dis Model Mech. 14(9):dmm048249. doi:10.1242/dmm.048249
  • Ferguson MW, Duncan J, Bond J, Bush J, Durani P, So K, Taylor L, Chantrey J, Mason T, James G, et al. 2009. Prophylactic administration of avotermin for improvement of skin scarring: three double-blind, placebo-controlled, phase I/II studies. Lancet. 373(9671):1264–1274. doi:10.1016/S0140-6736(09)60322-6
  • Foncuberta MC, Cagnoni PJ, Brandts CH, Mandanas R, Fields K, Derigs HG, Reed E, Sonis ST, Fay J, LeVeque F, et al. 2001. Topical transforming growth factor-β3 in the prevention or alleviation of chemotherapy-induced oral mucositis in patients with lymphomas or solid tumors. J Immunother. 24(4):384–388. doi:10.1097/00002371-200107000-00014
  • Frangogiannis NG. 2020. Transforming growth factor–ß in tissue fibrosis. J Exp Med. 217(3):e20190103. doi:10.1084/jem.20190103
  • Fujio K, Komai T, Inoue M, Morita K, Okamura T, Yamamoto K. 2016. Revisiting the regulatory roles of the TGF-β family of cytokines. Autoimmun Rev. 15(9):917–922. doi:10.1016/J.AUTREV.2016.07.007
  • Hanson I, Pitman KE, Edin NFJ. 2023. The role of TGF-β3 in radiation response. Int J Mol Sci. 24(8):7614. doi:10.3390/ijms24087614
  • Hosokawa R, Nonaka K, Morifuji M, Shum L, Ohishi M. 2003. TGF-β3 decreases type I collagen and scarring after labioplasty. J Dent Res. 82(7):558–564. doi:10.1177/154405910308200714
  • Jiajia Zhao JL. 2015. The expression level of TGF-β1, TGF-β3 and VEGF in transplanted oral mucosal and cutaneous wounds. Clin Microbiol. 04(02):198. doi:10.4172/2327-5073.1000198
  • Juvkam IS, Zlygosteva O, Arous D, Galtung HK, Malinen E, Søland TM, Jeppesen Edin N. 2022. A preclinical model to investigate normal tissue damage following fractionated radiotherapy to the head and neck. J Radiat Res. 64(1):44–52. doi:10.1093/jrr/rrac066
  • Juvkam IS, Zlygosteva O, Malinen E, Edin NJ, Galtung HK, Søland TM. 2023. Fractionated irradiation of murine salivary glands resulted in focal acinar cell atrophy, immune cell infiltration, fibrosis, and hyposalivation. BioRxiv 20230905556313 [Preprint] [Internet doi:10.1101/2023.09.05.556313
  • Karamichos D, Hutcheon AEK, Zieske JD, Dimitrios K. 2014. Reversal of fibrosis by TGF-β3 in a 3D in vitro model. Exp Eye Res. 124:31–36. doi:10.1016/j.exer.2014.04.020
  • Khalil N, O'Connor RN, Flanders KC, Shing W, Whitman CI. 1994. Regulation of type II alveolar epithelial cell proliferation by TGF-β during bleomycin-induced lung injury in rats. Am J Physiol. 267(5 Pt 1):L498–507. doi:10.1152/ajplung.1994.267.5.l498
  • De Kroon LMG, Narcisi R, Davidson ENB, Cleary MA, Van Beuningen HM, Koevoet WJLM, Van Osch GJVM, Van Der Kraan PM. 2015. Activin receptor-like kinase receptors ALK5 and ALK1 are both required for TGFβ-induced chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells. PLOS One. 10(12):e0146124. doi:10.1371/JOURNAL.PONE.0146124
  • Lanning DA, Diegelmann RF, Yager DR, Wallace ML, Bagwell CE, Haynes JH. 2000. Myofibroblast induction with transforming growth factor-β1 and -β3 in cutaneous fetal excisional wounds. J Pediatr Surg. 35(2):183–188. doi:10.1016/S0022-3468(00)90007-1
  • Laverty HG, Wakefield LM, Occleston NL, O'Kane S, Ferguson MWJ. 2009. TGF-β3 and cancer: A review. Cytokine Growth Factor Rev. 20(4):305–317. doi:10.1016/j.cytogfr.2009.07.002
  • Li H, Kucharavy HC, Hajj C, Zhao L, Hua G, Glass R, Paty PB, Fuks Z, Kolesnick R, Hubbard K, et al. 2023. Radiation-induced gastrointestinal (GI) syndrome as a function of age. Cell Death Discov. 9(1):31. doi:10.1038/s41420-023-01298-0
  • Loewen MS, Walner DL, Caldarelli DD. 2001. Improved airway healing using transforming growth factor beta-3 in a rabbit model. Wound Repair Regen. 9(1):44–49. doi:10.1046/j.1524-475x.2001.00044.x
  • Lux A, Attisano L, Marchuk DA. 1999. Assignment of transforming growth factor 1 and 3 and a third new ligand to the type I receptor ALK-1*. J Biol Chem. 274(15):9984–9992. doi:10.1074/jbc.274.15.9984
  • Mallick S, Benson R, Rath GK. 2016. Radiation induced oral mucositis: a review of current literature on prevention and management. Eur Arch Otorhinolaryngol. 273(9):2285–2293. doi:10.1007/s00405-015-3694-6
  • McCormack ES, Borzillo GV, Ambrosino C, Mak G, Hamablet L, Qu GY, Haley JD. 1997. Transforming growth factor-β3 protection of epithelial cells from cycle-selective chemotherapy in vitro. Biochem Pharmacol. 53(8):1149–1159. doi:10.1016/S0006-2952(97)00094-4
  • Nakamura SI, Kawai T, Kamakura T, Ookura T. 2010. TGF-β3 is expressed in taste buds and inhibits proliferation of primary cultured taste epithelial cells. In Vitro Cell Dev Biol Anim. 46(1):36–44. doi:10.1007/s11626-009-9239-9
  • Potten CS, Booth D, Haley JD. 1997. Pretreatment with transforming growth factor beta-3 protects small intestinal stem cells against radiation damage in vivo. Br J Cancer. 75(10):1454–1459. doi:10.1038/bjc.1997.249
  • Robson H, Spence K, Anderson E, Potten CS, Hendry JH. 1997. Differential influence of TGFβ1 and TGFβ3 isoforms on cell cycle kinetics and postirradiation recovery of normal and malignant colorectal epithelial cells. Int J Radiat Oncol Biol Phys. 38(1):183–190. doi:10.1016/S0360-3016(97)00248-4
  • Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 9(7):671–675. doi:10.1038/nmeth.2089
  • Schrementi ME, Ferreira AM, Zender C, DiPietro LA. 2008. Site-specific production of TGF-β in oral mucosal and cutaneous wounds. Wound Repair Regen. 16(1):80–86. doi:10.1111/j.1524-475X.2007.00320.x
  • Seong J, Kim SH, Chung EJ, Lee WJ, Suh CO. 2000. Early alteration in TGF-β mRNA expression in irradiated rat liver. Int J Radiat Oncol Biol Phys. 46(3):639–643. doi:10.1016/S0360-3016(99)00401-0
  • Shah M, Foreman D, Ferguson MWJ. 1995. Neutralisation of TGF-β1 and TGF-β2 or exogenous addition of TGF-β3 to cutaneous rat wounds reduces scarring. J Cell Sci. 108(3):985–1002. doi:10.1242/jcs.108.3.985
  • Shi Y, Massagué J. 2003. Mechanisms of TGF-B signaling from cell membrane to the nucleus. Cell. 113(6):685–700. doi:10.1016/s0092-8674(03)00432-x
  • Siddiqui F, Movsas B. 2017. Management of radiation toxicity in head and neck cancers. Semin Radiat Oncol. 27(4):340–349. doi:10.1016/J.SEMRADONC.2017.04.008
  • So K, McGrouther DA, Bush JA, Durani P, Taylor L, Skotny G, Mason T, Metcalfe A, O'Kane S, Ferguson MWJ. 2011. Avotermin for scar improvement following scar revision surgery: A randomized, double-blind, within-patient, placebo-controlled, phase II clinical trial. Plast Reconstr Surg. 128(1):163–172. doi:10.1097/PRS.0b013e318217429b
  • Sonis ST, Elting LS, Keefe D, Peterson DE, Schubert M, Hauer-Jensen M, Bekele BN, Raber-Durlacher J, Donnelly JP, Rubenstein EB. 2004. Perspectives on cancer therapy-induced mucosal injury: pathogenesis, measurement, epidemiology, and consequences for patients. Cancer. 100(9 Suppl):1995–2025. doi:10.1002/CNCR.20162
  • Sonis ST, Lindquist L, Van Vugt A, Stewart AA, Stam K, Qu G-Y, Iwata KK, Haley JD. 1994. Prevention of chemotherapy-induced ulcerative mucositis by transforming growth factor β3. Cancer Res. 54:1135–1138.
  • Sonis ST, Van Vugt AG, Brien JP, Muska AD, Bruskin AM, Rose A, Haley JD. 1997. Transforming growth factor-β3 mediated modulation of cell cycling and attenuation of 5-fluorouracil induced oral mucositis. Oral Oncol. 33(1):47–54. doi:10.1016/s0964-1955(96)00043-7
  • Sroussi HY, Epstein JB, Bensadoun R-J, Saunders DP, Lalla RV, Migliorati CA, Heaivilin N, Zumsteg ZS. 2017. Common oral complications of head and neck cancer radiation therapy: mucositis, infections, saliva change, fibrosis, sensory dysfunctions, dental caries, periodontal disease, and osteoradionecrosis. Cancer Med. 6(12):2918–2931. doi:10.1002/cam4.1221
  • Straub JM, New J, Hamilton CD, Lominska C, Shnayder Y, Thomas SM. 2015. Radiation-induced fibrosis: mechanisms and implications for therapy. J Cancer Res Clin Oncol. 141(11):1985–1994. doi:10.1007/s00432-015-1974-6
  • Taliaferro LP, Agarwal RK, Coleman CN, Andrea L, Hofmeyer KA, Loelius SG, Molinar-Inglis O, Tedesco DC, Satyamitra MM, Taliaferro LP. 2023. Sex differences in radiation research. Int J Radiat Biol. 100(3):466–485. doi:10.1080/09553002.2023.2283089
  • Trotti A, Byhardt R, Stetz J, Gwede C, Corn B, Fu K, Gunderson L, McCormick B, Morrisintegral M, Rich T, et al. 2000. Common toxicity criteria: version 2.0. An improved reference for grading the acute effects of cancer treatment: impact on radiotherapy. Int J Radiat Oncol Biol Phys. 47(1):13–47. doi:10.1016/S0360-3016(99)00559-3
  • Wang J, Robbins MEC. 1996. Radiation-induced alteration of rat mesangial cell transforming growth factor-β and expression of the genes associated with the extracellular matrix. Radiat Res. 146(5):561–568. doi:10.2307/3579557
  • Wang K, Tepper JE. 2021. Radiation therapy‐associated toxicity: etiology, management, and prevention. CA Cancer J Clin. 71(5):437–454. doi:10.3322/caac.21689
  • Wilson SE. 2021. TGF beta −1, −2 and −3 in the modulation of fibrosis in the cornea and other organs. Exp Eye Res. 207:108594. doi:10.1016/j.exer.2021.108594
  • Wu Y, Peng Y, Gao D, Feng C, Yuan X, Li H, Wang Y, Yang L, Huang S, Fu X. 2015. Mesenchymal stem cells suppress fibroblast proliferation and reduce skin fibrosis through a TGF-β3-dependent activation. Int J Low Extrem Wounds. 14(1):50–62. doi:10.1177/1534734614568373
  • Wymenga ANM, van der Graaf WTA, Hofstra LS, Spijkervet FKL, Timens W, Timmer-Bosscha H, Sluiter WJ, van Buuren A, Mulder NH, de VE. 1999. Phase I study of transforming growth factor-3 mouthwashes for prevention of chemotherapy-induced mucositis. Clin Cancer Res. 5:1363–1368.
  • Xu L, Xiong S, Guo R, Yang Z, Wang Q, Xiao F, Wang H, Pan X, Zhu M. 2014. Transforming growth factor β3 attenuates the development of radiation-induced pulmonary fibrosis in mice by decreasing fibrocyte recruitment and regulating IFN-γ/IL-4 balance. Immunol Lett. 162(1 Pt A):27–33. doi:10.1016/J.IMLET.2014.06.010
  • Xue K, Zhang J, Li C, Li J, Wang C, Zhang Q, Chen X, Yu X, Sun L, Yu X. 2019. The role and mechanism of transforming growth factor beta 3 in human myocardial infarction-induced myocardial fibrosis. J Cell Mol Med. 23(6):4229–4243. doi:10.1111/jcmm.14313
  • Zhao W, O'Malley Y, Wei S, Robbins ME. 2000. Irradiation of rat tubule epithelial cells alters the expression of gene products associated with the synthesis and degradation of extracellular matrix. Int J Radiat Biol. 76(3):391–402. doi:10.1080/095530000138736