Abstract
The aim of this article is to give an insight into the future of photodynamic therapy (PDT) in head and neck squamous cell carcinoma (HNSCC). Through the combination of a photosensitizing agent with light and oxygen, PDT produces highly cytotoxic reactive oxygen species leading to selective tumor eradication. PDT is an attractive treatment for focal therapy of localized tumors, especially in the case of unresectable tumors. In HNSCC, over 1500 patients have been treated by PDT, and the majority of them responded quite favorably to this treatment. However, the non-negligible photosensitization of healthy tissue is a major limitation for the clinical application of PDT. Improvement in tumor selectivity is the main challenge that can be taken up by the use of a new generation of photosensitizing nanoparticles. Passive targeting, by using functionalised nanocarriers to target to overexpressed transmembrane receptors afford attractive solutions. To this day, epidermal growth factor receptor (EGFR) remains the only validated molecular target for HNSCC, and photosensitizer immunoconjugates to EGFR have been developed for the intracellular delivery of photosensitizing agents. Depending on coordinated research between biomarkers, specific ligands, and photosensitizers, similar approaches could be rapidly developed. In addition, some photosensitizers hold high fluorescence yield and therefore could emerge as theranostic agents.
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Argiris A, Karamouzis MV, Raben D, Ferris RL (2008) Head and neck cancer. Lancet 371:1695–1709
Siegel R, Naishadham D, Jemal A (2012) Cancer statistics, 2012. CA Cancer J Clin 62:10–29
Agostinis P, Berg K, Cengel KA et al (2011) Photodynamic therapy of cancer: an update. CA Cancer J Clin 61:250–281
Bredell MG, Besic E, Maake C, Walt H (2010) The application and challenges of clinical PD-PDT in the head and neck region: a short review. J Photochem Photobiol B 101:185–190
Bonner JA, Harari PM, Giralt J et al (2010) Radiotherapy plus cetuximab for locoregionally advanced head and neck cancer: 5-year survival data from a phase 3 randomised trial, and relation between cetuximab-induced rash and survival. Lancet Oncol 11:21–28
Reuther T, Kubler AC, Zillmann U et al (2001) Comparison of the in vivo efficiency of photofrin II-, mTHPC-, mTHPC-PEG- and mTHPCnPEG-mediated PDT in a human xenografted head and neck carcinoma. Lasers Surg Med 29:314–322
Biel MA (2010) Photodynamic therapy of head and neck cancers. Methods Mol Biol 635:281–293
Schweitzer VG, Somers ML (2010) PHOTOFRIN-mediated photodynamic therapy for treatment of early stage (Tis-T2N0M0) SqCCa of oral cavity and oropharynx. Lasers Surg Med 42:1–8
de Visscher SA, Dijkstra PU, Tan IB et al (2013) mTHPC mediated photodynamic therapy (PDT) of squamous cell carcinoma in the head and neck: a systematic review. Oral Oncol 49:192–210
Jerjes W, Upile T, Hamdoon Z et al (2011) Photodynamic therapy outcome for T1/T2 N0 oral squamous cell carcinoma. Lasers Surg Med 43:463–469
Karakullukcu B, Stoker SD, Wildeman AP et al (2013) A matched cohort comparison of mTHPC-mediated photodynamic therapy and trans-oral surgery of early stage oral cavity squamous cell cancer. Eur Arch Otorhinolaryngol 270:1093–1097
Tan IB, Dolivet G, Ceruse P et al (2010) Temoporfin-mediated photodynamic therapy in patients with advanced, incurable head and neck cancer: a multicenter study. Head Neck 32:1597–1604
Jerjes W, Upile T, Akram S, Hopper C (2010) The surgical palliation of advanced head and neck cancer using photodynamic therapy. Clin Oncol (R Coll Radiol) 22:785–791
Karakullukcu B, Nyst HJ, van Veen RL et al (2012) mTHPC mediated interstitial photodynamic therapy of recurrent nonmetastatic base of tongue cancers: development of a new method. Head Neck 34:1597–1606
Berg K, Folini M, Prasmickaite L et al (2007) Photochemical internalization: a new tool for drug delivery. Curr Pharm Biotechnol 8:362–372
Berg K, Nordstrand S, Selbo PK et al (2011) Disulfonated tetraphenyl chlorin (TPCS2a), a novel photosensitizer developed for clinical utilization of photochemical internalization. Photochem Photobiol Sci 10:1637–1651
Morrison SA, Hill SL, Rogers GS, Graham RA (2014) Efficacy and safety of continuous low-irradiance photodynamic therapy in the treatment of chest wall progression of breast cancer. J Surg Res 192:235–241
Wang HW, Rickter E, Yuan M et al (2007) Effect of photosensitizer dose on fluence rate responses to photodynamic therapy. Photochem Photobiol 83:1040–1048
Henderson BW, Gollnick SO, Snyder JW et al (2004) Choice of oxygen-conserving treatment regimen determines the inflammatory response and outcome of photodynamic therapy of tumors. Cancer Res 64:2120–2126
Garrier J, Bressenot A, Grafe S et al (2010) Compartmental targeting for mTHPC-based photodynamic treatment in vivo: correlation of efficiency, pharmacokinetics, and regional distribution of apoptosis. Int J Radiat Oncol Biol Phys 78:563–571
Bugaj AM (2011) Targeted photodynamic therapy—a promising strategy of tumor treatment. Photochem Photobiol Sci 10:1097–1109
Lim CK, Heo J, Shin S et al (2013) Nanophotosensitizers toward advanced photodynamic therapy of cancer. Cancer Lett 334:176–187
Master A, Livingston M, Sen Gupta A (2013) Photodynamic nanomedicine in the treatment of solid tumors: perspectives and challenges. J Control Release 168:88–102
Ernsting MJ, Murakami M, Roy A, Li SD (2013) Factors controlling the pharmacokinetics, biodistribution and intratumoral penetration of nanoparticles. J Control Release 172:782–794
Buchholz J, Wergin M, Walt H et al (2007) Photodynamic therapy of feline cutaneous squamous cell carcinoma using a newly developed liposomal photosensitizer: preliminary results concerning drug safety and efficacy. J Vet Intern Med 21:770–775
Buchholz J, Kaser-Hotz B, Khan T et al (2005) Optimizing photodynamic therapy: in vivo pharmacokinetics of liposomal meta-(tetrahydroxyphenyl)chlorin in feline squamous cell carcinoma. Clin Cancer Res 11:7538–7544
de Visscher SA, Kascakova S, de Bruijn HS et al (2011) Fluorescence localization and kinetics of mTHPC and liposomal formulations of mTHPC in the window-chamber tumor model. Lasers Surg Med 43:528–536
Lassalle HP, Dumas D, Grafe S et al (2009) Correlation between in vivo pharmacokinetics, intratumoral distribution and photodynamic efficiency of liposomal mTHPC. J Control Release 134:118–124
Bovis MJ, Woodhams JH, Loizidou M et al (2012) Improved in vivo delivery of m-THPC via pegylated liposomes for use in photodynamic therapy. J Control Release 157:196–205
Igarashi A, Konno H, Tanaka T et al (2003) Liposomal photofrin enhances therapeutic efficacy of photodynamic therapy against the human gastric cancer. Toxicol Lett 145:133–141
Hofman JW, Carstens MG, van Zeeland F et al (2008) Photocytotoxicity of mTHPC (temoporfin) loaded polymeric micelles mediated by lipase catalyzed degradation. Pharm Res 25:2065–2073
Low K, Knobloch T, Wagner S et al (2011) Comparison of intracellular accumulation and cytotoxicity of free mTHPC and mTHPC-loaded PLGA nanoparticles in human colon carcinoma cells. Nanotechnology 22:245102
Rojnik M, Kocbek P, Moret F et al (2012) In vitro and in vivo characterization of temoporfin-loaded PEGylated PLGA nanoparticles for use in photodynamic therapy. Nanomedicine (Lond) 7:663–677
Lee SJ, Park K, Oh YK et al (2009) Tumor specificity and therapeutic efficacy of photosensitizer-encapsulated glycol chitosan-based nanoparticles in tumor-bearing mice. Biomaterials 30:2929–2939
Yang PW, Hung MC, Hsieh CY et al (2012) The effects of photofrin-mediated photodynamic therapy on the modulation of EGFR in esophageal squamous cell carcinoma cells. Lasers Med Sci 28:605–614
Martinez-Carpio PA, Trelles MA (2010) The role of epidermal growth factor receptor in photodynamic therapy: a review of the literature and proposal for future investigation. Lasers Med Sci 25:767–771
Edmonds C, Hagan S, Gallagher-Colombo SM et al (2012) Photodynamic therapy activated signaling from epidermal growth factor receptor and STAT3: targeting survival pathways to increase PDT efficacy in ovarian and lung cancer. Cancer Biol Ther 13:1463–1470
Jin CS, Zheng G (2011) Liposomal nanostructures for photosensitizer delivery. Lasers Surg Med 43:734–748
Gijsens A, Missiaen L, Merlevede W, de Witte P (2000) Epidermal growth factor-mediated targeting of chlorin e6 selectively potentiates its photodynamic activity. Cancer Res 60:2197–2202
Hemming AW, Davis NL, Dubois B et al (1993) Photodynamic therapy of squamous cell carcinoma. An evaluation of a new photosensitizing agent, benzoporphyrin derivative and new photoimmunoconjugate. Surg Oncol 2:187–196
Kameyama N, Matsuda S, Itano O et al (2011) Photodynamic therapy using an anti-EGF receptor antibody complexed with verteporfin nanoparticles: a proof of concept study. Cancer Biother Radiopharm 26:697–704
Master A, Malamas A, Solanki R et al (2013) A cell-targeted photodynamic nanomedicine strategy for head and neck cancers. Mol Pharm 10:1988–1997
Christopoulos A, Ahn SM, Klein JD, Kim S (2011) Biology of vascular endothelial growth factor and its receptors in head and neck cancer: beyond angiogenesis. Head Neck 33:1220–1229
Dabkeviciene D, Sasnauskiene A, Leman E et al (2012) mTHPC-mediated photodynamic treatment up-regulates the cytokines VEGF and IL-1alpha. Photochem Photobiol 88:432–439
Solban N, Selbo PK, Sinha AK et al (2006) Mechanistic investigation and implications of photodynamic therapy induction of vascular endothelial growth factor in prostate cancer. Cancer Res 66:5633–5640
Bhuvaneswari R, Yuen GY, Chee SK, Olivo M (2011) Antiangiogenesis agents avastin and erbitux enhance the efficacy of photodynamic therapy in a murine bladder tumor model. Lasers Surg Med 43:651–662
Ferrario A, Gomer CJ (2006) Avastin enhances photodynamic therapy treatment of Kaposi's sarcoma in a mouse tumor model. J Environ Pathol Toxicol Oncol 25:251–259
Uehara M, Ikeda H, Nonaka M et al (2011) Predictive factor for photodynamic therapy effects on oral squamous cell carcinoma and oral epithelial dysplasia. Arch Oral Biol 56:1366–1372
Zheng G, Chen J, Stefflova K et al (2007) Photodynamic molecular beacon as an activatable photosensitizer based on protease-controlled singlet oxygen quenching and activation. Proc Natl Acad Sci U S A 104:8989–8994
Rai P, Mallidi S, Zheng X et al (2010) Development and applications of photo-triggered theranostic agents. Adv Drug Deliv Rev 62:1094–1124
Reddy GR, Bhojani MS, McConville P et al (2006) Vascular targeted nanoparticles for imaging and treatment of brain tumors. Clin Cancer Res 12:6677–6686
Li Z, Wang C, Cheng L et al (2013) PEG-functionalized iron oxide nanoclusters loaded with chlorin e6 for targeted, NIR light induced, photodynamic therapy. Biomaterials 34:9160–9170
Duncan R, Gaspar R (2011) Nanomedicine(s) under the microscope. Mol Pharm 8:2101–2141
Senge MO, Brandt JC (2011) Temoporfin (Foscan(R), 5,10,15,20-tetra(m-hydroxyphenyl)chlorin)—a second-generation photosensitizer. Photochem Photobiol 87:1240–1296
Rigual NR, Shafirstein G, Frustino J et al (2013) Adjuvant intraoperative photodynamic therapy in head and neck cancer. JAMA Otolaryngol Head Neck Surg 139:706–711
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Marchal, S., Dolivet, G., Lassalle, HP. et al. Targeted photodynamic therapy in head and neck squamous cell carcinoma: heading into the future. Lasers Med Sci 30, 2381–2387 (2015). https://doi.org/10.1007/s10103-014-1703-4
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DOI: https://doi.org/10.1007/s10103-014-1703-4