Gadolinium-Doped Iron Nanostructures Decorated with Novel Drugs for Magnetic Resonance Imaging, Photodynamic, and Photothermal Therapy Applications

  • Muhammad Fakhar-e-AlamEmail author
  • Arslan MahmoodEmail author
  • Shabab Nasir
  • Malik Saadullah
  • M. Waseem Akram
  • Magnus Willander
Part of the Nanomedicine and Nanotoxicology book series (NANOMED)


Multidrug drug resistance (MDR) builds many limitations/troubles/problems in magnetic resonance imaging (MRI) and treatment techniques. In this strategy, novel idea of polyethylene glycol/polyacrylic acid (PEG-co-PAA)-decorated gadolinium-doped iron was employed for cancer diagnostics and therapy purposes. In real sense, multifarious/various morphology of Gd-doped Fe-NMPs was found to be useful in versatile format of biomedical applications. Schematic of ongoing experimental strategy illustrates that three efficient photosensitizers, e.g., chlorine e6, Foscan®, and 5-ALA were decorated with Gd-doped iron capsulated with PEG-co-PAA such that their size/morphology consists within range of 100–120 nm of nanospheres. Final form of this nanospheres/nanocapsule plays a vital role through synergistic response of mutual plasmonic reaction of drug decorated nanocapsule. One of the prime focus of this novel experimental approach/review is to trace feasibility of PEG-co-PAA-decorated Gd-doped Fe-NMPs complex with drugs for photothermal therapy, magnetic resonance imaging (MRI) and photodynamic therapy (PDT) application. Current chapter consists of diverse flavor of original results includes SEM and TEM analysis, UV-Visible spectroscopy, NMR analysis of final product of PEG-co-PAA-doped Gd-Fe3O4 decorated with effective drugs, and cytotoxic and phototoxic effects of current developed organic–inorganic nanocapsule. The results indicate that PEG-co-PAA-encapsulated Gd-doped Fe-NMPs are very promising nanospecies for T1-MRI applications. Both the individual Gd-doped Fe-NPs and its conjugated species exhibited significant toxic effects for photodynamic therapy (PDT) and photothermal therapy (PTT) applications as observed in MCF-7/Hela cancer cell model. These results led to the empirical modeling of individual Gd-doped Fe-NPs and its conjugated species with cancer cells by analyzing the statistical data obtained from experiments and thus novel way toward a more practical strategy for the concept of PEG-co-PAA-encapsulated Gd-doped Fe-NMPs and its conjugates as photosensitizers for MRI, PTT and/or PDT.


  1. Akilov OE, Kosaka S, O’Riordan K, Hasan T (2007) Photodynamic therapy for cutaneous leishmaniasis: the effectiveness of topical phenothiaziniums in parasite eradication and Th1 immune response stimulation. Photochem Photobiol Sci 6(10):1067–1075CrossRefGoogle Scholar
  2. Allen CM, Sharman WM, Van Lier JE (2001) Current status of phthalocyanines in the photodynamic therapy of cancer. J Porphyrins Phthalocyanines 5(02):161–169Google Scholar
  3. Atif M, Firdous S, Khurshid A, Noreen L, Zaidi SS, Ikram M (2009) In vitro study of 5-aminolevulinic acid-based photodynamic therapy for apoptosis in human cervical HeLa cell line. Laser Phys Lett 6(12):886CrossRefGoogle Scholar
  4. Atif M, Fakhar-e-Alam M, Firdous S, Zaidi SSZ, Suleman R, Ikram M (2010) Study of the efficacy of 5-ALA mediated photodynamic therapy on human rhabdomyosarcoma cell line (RD). Laser Phys Lett 7(10):757Google Scholar
  5. Bases R, Brodie SS, Rubenfeld S (1958) Attempts at tumor localization using CU64-labeled copper porphyrins. Cancer 11(2):259–263CrossRefGoogle Scholar
  6. Battah SH, Chee CE, Nakanishi H, Gerscher S, MacRobert AJ, Edwards C (2001) Synthesis and biological studies of 5-aminolevulinic acid-containing dendrimers for photodynamic therapy. Bioconjug Chem 12(6):980–988CrossRefGoogle Scholar
  7. Battah S, O’Neill S, Edwards C, Balaratnam S, Dobbin P, MacRobert AJ (2006) Enhanced porphyrin accumulation using dendritic derivatives of 5-aminolaevulinic acid for photodynamic therapy: an in vitro study. Int J Biochem Cell Biol 38(8):1382–1392CrossRefGoogle Scholar
  8. Bellnier DA, Dougherty TJ (1996) A preliminary pharmacokinetic study of intravenous Photofrin® in patients. J Clin Laser Med Surg 14(5):311–314CrossRefGoogle Scholar
  9. Berger Y, Greppi A, Siri O, Neier R, Juillerat-Jeanneret L (2000) Ethylene glycol and amino acid derivatives of 5-aminolevulinic acid as new photosensitizing precursors of protoporphyrin IX in cells. J Med Chem 43(25):4738–4746CrossRefGoogle Scholar
  10. Berlin JC (2006) Silicon phthalocyanines for photodynamic therapy. Case Western Reserve UniversityGoogle Scholar
  11. Bernardi P, Scorrano L, Colonna R, Petronilli V, Di Lisa F (1999) Mitochondria and cell death. Eur J Biochem 264(3):687–701CrossRefGoogle Scholar
  12. Boix-Garriga E, Acedo P, Casado A, Villanueva A, Stockert JC, Cañete M, Mora M, Sagrista ML, Nonell S (2015) Poly(D, L-lactide-co-glycolide) nanoparticles as delivery agents for photodynamic therapy: enhancing singlet oxygen release and photototoxicity by surface PEG coating. Nanotechnology 38(26)Google Scholar
  13. Bourre L, Giuntini F, Eggleston IM, Wilson M, MacRobert AJ (2008) 5-Aminolaevulinic acid peptide prodrugs enhance photosensitization for photodynamic therapy. Mol Cancer Ther 7(6):1720–1729CrossRefGoogle Scholar
  14. Boyle RW, Dolphin D (1996) Structure and biodistribution relationships of photodynamic sensitizers. Photochem Photobiol 64(3):469–485Google Scholar
  15. Cairnduff F, Stringer MR, Hudson EJ, Ash DV, Brown SB (1994) Superficial photodynamic therapy with topical 5-aminolaevulinic acid for superficial primary and secondary skin cancer. Br J Cancer 69(3):605CrossRefGoogle Scholar
  16. Casas A, Batlle A (2006) Aminolevulinic acid derivatives and liposome delivery as strategies for improving 5-aminolevulinic acid-mediated photodynamic therapy. Curr Med Chem 13(10):1157–1168CrossRefGoogle Scholar
  17. Casas A, Perotti C, Saccoliti M, Sacca P, Fukuda H, del C Batlle AM (2002) ALA and ALA hexyl ester in free and liposomal formulations for the photosensitisation of tumour organ cultures. Brit J Cancer 86(5):837Google Scholar
  18. Christensen HN (1985) On the strategy of kinetic discrimination of amino acid transport systems. J Membr Biol 84(2):97–103CrossRefGoogle Scholar
  19. Christofori G (2006) New signals from the invasive front. Nature 441(7092):7444CrossRefGoogle Scholar
  20. Collaud S, Juzeniene A, Moan J, Lange N (2004) On the selectivity of 5-aminolevulinic acid-induced protoporphyrin IX formation. Curr Med Chem Anti-Cancer Agents 4(3):301–316CrossRefGoogle Scholar
  21. Di Venosa GM, Casas AG, Battah S, Dobbin P, Fukuda H, MacRobert AJ, Batlle A (2006) Investigation of a novel dendritic derivative of 5-aminolaevulinic acid for photodynamic therapy. Int J Biochem Cell Biol 38(1):82–91CrossRefGoogle Scholar
  22. Dolmans DEJGJ, Fukumura D, Jain RK (2003) Photodynamic therapy for cancer. Nat Rev Cancer 3(5):380Google Scholar
  23. Dougherty TJ, Gomer CJ, Henderson BW, Jori G, Kessel D, Korbelik M, Moan J, Peng Q (1998) Photodynamic therapy. JNCI J Nat Cancer Inst 90(12):889–905Google Scholar
  24. Fakhar-e-Alam M, Butt AR et al (2018) Magnesium oxide in nanodimension: model for MRI and multimodal therapy. J Nanomater Article ID 4210920:12 pages.
  25. Fakhar-e-Alam M, Roohi S, Atif M, Firdous S, Amir N, Zahoor R (2010) Labelling and optimization of PHOTOFRIN® with 99mTc. Radiochim Acta Int J Chem Aspects Nucl Sci Technol 98(12):813–818Google Scholar
  26. Fakhar-e-Alam M, Kishwar S, Khan Y, Siddique M, Atif M, Nur O, Willander M (2011a) Tumoricidal effects of nanomaterials in HeLa cell line. Laser Phys 2011(21):1978–1988CrossRefGoogle Scholar
  27. Fakhar-e-Alam M, Usman Ali SM, Ibupoto ZH, Atif M, Willander M (2011b) Role of ALA sensitivity in HepG2 cell in the presence of diode laser. Laser Phys 21:2165–2170Google Scholar
  28. Fakhar-e-Alam M, Khan Y et al (2011c) The potential applications of ZnO nanoparticles conjugated with ALA and Photofrin® as a biomarker in HepG2 cells. Laser Phys 2011(21):2156–2164CrossRefGoogle Scholar
  29. Fakhar-e-Alam M, Waseem Akram M, Iqbal S, Alimgeer KS, Atif M, Sultana K, Willander M, Wang ZM (2017a) Empirical modeling of physiochemical immune response of zinc oxide nanowires under UV exposure to melanoma and foreskin fibroblast. Sci Rep 7:46603.
  30. Fakhar-e-Alam M, Waseem Akram M, Iqbal S, Alimgeer KS, Atif M, Sultana K, Willander M, Wang ZM (2017b) Empirical modeling of physiochemical immune response of zinc oxide nanowires under UV exposure to melanoma and foreskin fibroblast. Sci Rep 7:46603.
  31. Fawwaz R, Bohdiewicz P, Lavallee D, Wang T, Oluwole S, Newhouse J, Alderson P (1990) Use of metalloporphyrins in diagnostic imaging. Nucl Med Biol 17(1):65–72Google Scholar
  32. Ferreira J, Kurachi C, Moriyama LT, Menezes PFC, Perussi JR, Sibata C et al (2006) Laser Phys Lett 3:91Google Scholar
  33. Ferriera J, Menezes PFC, Kurachi C, Sibata C, Allison RR, Bagnato VS (2008) Laser Phys Lett 2008(5):161–166Google Scholar
  34. Frangville C et al (2016) Assembly of double-hydrophilic block copolymers triggered by gadolinium ions: new colloidal MRI contrast agents. Nanoletter 16:4069–4073CrossRefGoogle Scholar
  35. Friesen SA, Hjortland GO, Madsen SJ, Hirschberg H, Engebraten O, Nesland JM, Peng Q (2002) 5-Aminolevulinic acid-based photodynamic detection and therapy of brain tumors. Int J Oncol 21(3):577–582Google Scholar
  36. Furre IE, Shahzidi S, Luksiene Z, Møller MT, Borgen E, Morgan J, Tkacz-Stachowska K, Nesland JM, Peng Q (2005) Targeting PBR by hexaminolevulinate-mediated photodynamic therapy induces apoptosis through translocation of apoptosis-inducing factor in human leukemia cells. Can Res 65(23):11051–11060CrossRefGoogle Scholar
  37. Furuse K, Fukuoka M, Kato H, Horai T, Kubota K, Kodama N, Kusunoki Y, Takifuji N, Okunaka T, Konaka C (1993) A prospective phase II study on photodynamic therapy with photofrin II for centrally located early-stage lung cancer. The Japan Lung Cancer Photodynamic Therapy Study Group. J Clin Oncol 11(10):1852–1857Google Scholar
  38. Gahlen J, Stern J, Laubach HH, Pietschmann M, Herfarth C (1999) Improving diagnostic staging laparoscopy using intraperitoneal lavage of δ-aminolevulinic acid (ALA) for laparoscopic fluorescence diagnosis. Surgery 126(3):469–473CrossRefGoogle Scholar
  39. Gardner LC, Smith SJ, Cox TM (1991) Biosynthesis of delta-aminolevulinic acid and the regulation of heme formation by immature erythroid cells in man. J Biol Chem 266(32):22010–22018Google Scholar
  40. Georgakoudi I, Nichols MG, Foster TH (1997) The mechanism of Photofrin photobleaching and its consequences for photodynamic dosimetry. Photochem Photobiol 65(1):135–144CrossRefGoogle Scholar
  41. Gerscher S, Connelly JP, Griffiths J, Brown SB, MacRobert AJ, Wong G, Rhodes LE (2000) Comparison of the pharmacokinetics and phototoxicity of protoporphyrin IX metabolized from 5-aminolevulinic acid and two derivatives in human skin in vivo. Photochem Photobiol 72(4):569–574CrossRefGoogle Scholar
  42. Ghaghada KB, Ravoori M, Sabapathy D, Bankson J, Kundra V, Annapragada A (2009) New dual mode gadolinium nanoparticle contrast agent for magnetic resonance imaging. Plos One 4(10):e7628Google Scholar
  43. Gomer CJ, Ferrario A, Murphree AL (1987) The effect of localized porphyrin photodynamic therapy on the induction of tumour metastasis. Br J Cancer 56(1):27CrossRefGoogle Scholar
  44. Grebeňová D, Kuželová K, Smetana K, Pluskalová M, Cajthamlová H, Marinov I, Fuchs O, Souček J, Jarolı́m P, Hrkal Z (2003) Mitochondrial and endoplasmic reticulum stress-induced apoptotic pathways are activated by 5-aminolevulinic acid-based photodynamic therapy in HL60 leukemia cells. J Photochem Photobiol B Biol 69(2):71–85Google Scholar
  45. Grossweiner LI, Grossweiner JB, Gerald Rogers BH (2005) The science of phototherapy: an introduction. Springer, Dordrecht, The NetherlandsGoogle Scholar
  46. Gu M-J, Li K-F, Zhang L-X, Wang H, Liu L-S, Zheng Z-Z, Han N-Y, Yang Z-J, Fan T-Y (2015) In vitro study of novel gadolinium-loaded liposomes guided by GBI-10 aptamer for promising tumor targeting and tumor diagnosis by magnetic resonance imaging. Int J Nanomed 10:5187–5520Google Scholar
  47. Helm L (2010) Optimization of gadolinium-based MRI contrast agents for high magnetic-field applications. Future Med Chem 2(3):385–396.
  48. Hinnen P, de Rooij FW, Van Velthuysen ML, Edixhoven A, Van Hillegersberg R, Tilanus HW, Wilson JH, Siersema PD (1998) Biochemical basis of 5-aminolaevulinic acid-induced protoporphyrin IX accumulation: a study in patients with (pre) malignant lesions of the oesophagus. Br J Cancer 78(5):679CrossRefGoogle Scholar
  49. Huang Z (2005) A review of progress in clinical photodynamic therapy. Technol Cancer Res Treat 4(3):283–293Google Scholar
  50. Ikram M, Khan RU, Firdous S, Atif M, Nawaz M (2011) Photodynamic therapy of non-melanoma skin cancers. Laser Phys 21(2):427–433CrossRefGoogle Scholar
  51. Jeffes EW, McCullough JL, Weinstein GD, Fergin PE, Nelson JS, Shull TF, Simpson KR, Bukaty LM, Hoffman WL, Fong NL (1997) Photodynamic therapy of actinic keratosis with topical 5-aminolevulinic acid: a pilot dose-ranging study. Arch Dermatol 133(6):727–732CrossRefGoogle Scholar
  52. Kanal E (2016) Gadolinium based contrast agents (GBCA): safety overview after 3, decades of clinical experience. Magn Reson Imaging 2016(34):1341–1345CrossRefGoogle Scholar
  53. Kanda T, Nakai Y, Oba H, Toyoda K, Kitajima K, Furui S (2016) Gadolinium deposition in the brain. Magn Reson Imaging 34:1346–1350Google Scholar
  54. Karmakar S, Banik NL, Patel SJ, Ray SK (2007) 5-Aminolevulinic acid-based photodynamic therapy suppressed survival factors and activated proteases for apoptosis in human glioblastoma U87MG cells. Neurosci Lett 415(3):242–247CrossRefGoogle Scholar
  55. Kaushik A, Khan R, Solanki PR, Pandey P, Alam J, Ahmad S, Malhota BD (2008) Iron oxide nanoparticlrs-chitosan composite based glucose biosensor. Biosens Bioelectron 24:676–683Google Scholar
  56. Kennedy JC, Pottier RH (1992) New trends in photobiology: endogenous protoporphyrin IX, a clinically useful photosensitizer for photodynamic therapy. J Photochem Photobiol B 14(4):275–292CrossRefGoogle Scholar
  57. Kennedy JC, Pottier RH, Pross DC (1990) Photodynamic therapy with endogenous protoporphyrin: IX: basic principles and present clinical experience. J Photochem Photobiol B 6(1–2):143–148CrossRefGoogle Scholar
  58. Kennedy JC, Marcus SL, Pottier RH (1996) Photodynamic therapy (PDT) and photodiagnosis (PD) using endogenous photosensitization induced by 5-aminolevulinic acid (ALA): mechanisms and clinical results. J Clin Laser Med Surg 14(5):289–304CrossRefGoogle Scholar
  59. Khursid A, Atif M, Firdous S, Zaidi SS, Salman R, Ikram M (2010) Study of the efficacy of 5 ALA-mediated photodynamic therapy on human larynx squamous cell carcinoma (Hep2c) cell line. Laser Phys 20(7):1673–1678CrossRefGoogle Scholar
  60. Kloek J, Beijersbergen van Henegouwen GM (1996) Prodrugs of 5‐aminolevullinic acid for photodynamic therapy. Photochem Photobiol 64(6):994–1000Google Scholar
  61. Kondo M, Hirota N, Takaoka T, Kajiwara M (1993) Heme-biosynthetic enzyme activities and porphyrin accumulation in normal liver and hepatoma cell lines of rat. Cell Biol Toxicol 9(1):95–105CrossRefGoogle Scholar
  62. Kopera D, Cerroni L, Fink-Puches R, Kerl H (1996) Different treatment modalities for the management of a patient with the nevoid basal cell carcinoma syndrome. J Am Acad Dermatol 34(5):937–939CrossRefGoogle Scholar
  63. Korbelik M (1996) Induction of tumor immunity by photodynamic therapy. J Clin Laser Med Surg 14(5):329–334Google Scholar
  64. Krieg RC, Messmann H, Rauch J, Seeger S, Knuechel R (2002) Metabolic characterization of tumor cell–specific protoporphyrin IX accumulation after exposure to 5-aminolevulinic acid in human colonic cells. Photochem Photobiol 76(5):518–525CrossRefGoogle Scholar
  65. Kriska T, Korytowski W, Girotti AW (2005) Role of mitochondrial cardiolipin peroxidation in apoptotic photokilling of 5-aminolevulinate-treated tumor cells. Arch Biochem Biophys 433(2):435–446CrossRefGoogle Scholar
  66. Kübler A, Haase T, Rheinwald M, Barth T, Mühling J (1998) Treatment of oral leukoplakia by topical application of 5-aminolevulinic acid. Int J Oral Maxillofac Surg 27(6):466–469CrossRefGoogle Scholar
  67. Lisnjak IO, Kutsenok VV, Polyschuk LZ, Gorobets OB, Gamaleia NF (2005) Effect of photodynamic therapy on tumor angiogenesis and metastasis in mice bearing Lewis lung carcinoma. Exp Oncol 27(4):333–335Google Scholar
  68. Liza S, Valappil Mohanan P (2016) Toxicological evaluation of dextran stabilized iron oxide nanoparticles in human peripheral blood lymphocytes. Biointerphases 11(4):04B302.
  69. Loh CS, MacRobert AJ, Bedwell J, Regula J, Krasner N, Bown SG (1993) Oral versus intravenous administration of 5-aminolaevulinic acid for photodynamic therapy. Br J Cancer 68(1):41CrossRefGoogle Scholar
  70. Loncaster JA, Moore JV, Allan D, Allan E (2005) An ultrasound analysis of the response of Gorlin syndrome-related and sporadic basal cell carcinomas to aminolaevulinic acid photodynamic therapy. Photodiagn Photodyn Ther 2(2):149–155CrossRefGoogle Scholar
  71. Luksiene Z (2003) Photodynamic therapy: mechanism of action and ways to improve the efficiency of treatment. Medicina 39(12):1137–1150Google Scholar
  72. Mang TS (2004) Lasers and light sources for PDT: past, present and future. Photodiagn Photodyn Ther 1(1):43–48CrossRefGoogle Scholar
  73. Messmann H, Mlkvy P, Buonaccorsi G, Davies CL, MacRobert AJ, Bown SG (1995) Enhancement of photodynamic therapy with 5-aminolaevulinic acid-induced porphyrin photosensitisation in normal rat colon by threshold and light fractionation studies. Br J Cancer 72(3):589CrossRefGoogle Scholar
  74. Mĺkvy P, Messmann H, Regula J, Conio M, Pauer M, Millson CE, MacRobert AJ, Bown SG (1998) Photodynamic therapy for gastrointestinal tumors using three photosensitizers—ALA induced PPIX, Photofrin and MTHPC. Pilot Study. Neoplasma 45(3):157–161Google Scholar
  75. Moan J, Berg K (1992) Photochemotherapy of cancer. Exp Res Photochem Photobiol 55(6):931–948CrossRefGoogle Scholar
  76. Morgan J, Oseroff AR (2001) Mitochondria-based photodynamic anti-cancer therapy. Adv Drug Deliv Rev 49(1–2):71–86CrossRefGoogle Scholar
  77. Peng Q (1996) Build-up of esterified aminolevulinic-acid-derivative-induced porphyrin fluorescence in normal mouse skin. J Photochem Photobiol B Biol 34:95–96CrossRefGoogle Scholar
  78. Peng Q, Berg K, Moan J, Kongshaug M, Nesland JM (1997a) 5-Aminolevulinic acid-based photodynamic therapy: principles and experimental research. Photochem Photobiol 65(2):235–251CrossRefGoogle Scholar
  79. Peng Q, Warloe T, Berg K, Moan J, Kongshaug M, Giercksky KE, Nesland JM (1997a) 5‐Aminolevulinic acid‐based photodynamic therapy: clinical research and future challenges. Cancer Interdisc Int J Am Cancer Soc 79(12):2282–2308Google Scholar
  80. Peng Q, Warloe T, Berg K, Moan J, Kongshaug M, Giercksky KE, Nesland JM (1997b) 5‐Aminolevulinic acid‐based photodynamic therapy: clinical research and future challenges. Cancer Interdisc Int J Am Cancer Soc 79(12):2282–2308Google Scholar
  81. Peng Q, Berg K, Moan J, Kongshaug M, Nesland JM (1997) 5‐aminolevulinic acid‐based photodynamic therapy: principles and experimental research. Photochem Photobiol 65(2):235–251Google Scholar
  82. Peng Q, Warloe T, Moan J, Godal A, Apricena F, Giercksky KE, Nesland JM (2001) Antitumor effect of 5-aminolevulinic acid-mediated photodynamic therapy can be enhanced by the use of a low dose of photofrin in human tumor xenografts. Can Res 61(15):5824–5832Google Scholar
  83. Prasad PN (2003) Introduction to biophotonics, Chap 1, pp 1–593. Wiley InterscienceGoogle Scholar
  84. Rhodes LE, Tsoukas MM, Anderson RR, Kollias N (1997) Iontophoretic delivery of ALA provides a quantitative model for ALA pharmacokinetics and PpIX phototoxicity in human skin. J Invest Dermatol 108(1):87–91CrossRefGoogle Scholar
  85. Richter C (2000) Mitochondria as targets for the induction of apoptosis in photodynamic therapy. Photomed Gynecol Reprod 157Google Scholar
  86. Rifkin R, Reed B, Hetzel F, Chen K (1997) Photodynamic therapy using SnET2 for basal cell nevus syndrome: a case report. Clin Ther 19(4):639–641CrossRefGoogle Scholar
  87. Rud E, Gederaas O, Høgset A, Berg K (2000) 5-aminolevulinic acid, but not 5-aminolevulinic acid esters, is transported into adenocarcinoma cells by system BETA transporters. Photochem Photobiol 71(5):640–647CrossRefGoogle Scholar
  88. Schmidt-Erfurth U, Bauman W, Gragoudas E, Flotte TJ, Michaud NA, Birngruber R, Hasan T (1994) Photodynamic therapy of experimental choroidal melanoma using lipoprotein-delivered benzoporphyrin. Ophthalmology 101(1):89–99CrossRefGoogle Scholar
  89. Schreiber S, Gross S, Brandis A, Harmelin A, Rosenbach-Belkin V, Scherz A, Salomon Y (2002) Local photodynamic therapy (PDT) of rat C6 glioma xenografts with Pd-bacteriopheophorbide leads to decreased metastases and increase of animal cure compared with surgery. Int J Cancer 99(2):279–285CrossRefGoogle Scholar
  90. Semelka R, Ramalho J, Vakharia A, AlObaidy M, Burke LM, Jay M, Ramalho M (2016) Gadolinium deposition disease: initial description of a disease that has been around for a while. Magn Reson Imag 34:1383–1390Google Scholar
  91. Shaheen F, Aziz MH, Fakhar-e-Alam M et al (2017a) An In vitro study of the photodynamic effectiveness of GO-Ag nanocomposites against human breast cancer cells. Nanomaterials 7(401).
  92. Shaheen F, Aziz MH, Fakhar-e-Alam M et al (2017b) An in vitro study of the photodynamic effectiveness of GO-Ag nanocomposites against human breast cancer cells. Nanomaterials; MDPI 7(401).
  93. Soikkeli M, Sievänen K, Peltonen J, Kaasalainen T, Timonen M, Heinonen P, Rönkkö S, Lehto VP, Kavakka JS, Heikkinen S (2015) Synthesis and in vitro phantom NMR and MRI studies of fully organic free radicals, TEEPO-glucose and TEMPO-glucose, potential contrast agents for MRI. RSC Adv 5(20):15507–15510. Scholar
  94. Solban N, Rizvi I, Hasan T (2006) Targeted photodynamic therapy. Lasers in surgery and medicine. Offic J Am Soc Laser Med Surg 38(5):522–531Google Scholar
  95. Soler AM, Angell-Petersen E, Warloe T, Tausjø J, Steen HB, Moan J, Giercksky KE (2000) Photodynamic therapy of superficial basal cell carcinoma with 5-aminolevulinic acid with dimethylsulfoxide and ethylendiaminetetraacetic acid: a comparison of two light sources. Photochem Photobiol 71(6):724–729CrossRefGoogle Scholar
  96. Tang J, Liu X, Li D, Yang Y, Khan X, Mehmood ur Rehman K Structure and magnetic analyses of hexaferrite Sr1 − xLaxFe22 + Fe163 + O27 prepared via the solid-state reaction. J Mater Sci Mater Electron.
  97. Thaller RA, Lyster DM, Dolphin D (1983) Potential use of radiolabelled porphyrins for tumor scanning. In: Porphyrin photosensitization. Springer, Boston, MA, pp 265–278Google Scholar
  98. Tsai JC, Hsiao YY, Teng LJ, Chen CT, Kao MC (1999) Comparative study on the ALA photodynamic effects of human glioma and meningioma cells. Lasers in surgery and medicine. Offic J Am Soc Laser Med Surg 24(4):296–305CrossRefGoogle Scholar
  99. Tsai T, Hong RL, Tsai JC, Lou PJ, Ling IF, Chen CT (2004) Effect of 5-aminolevulinic acid-mediated photodynamic therapy on MCF-7 and MCF-7/ADR cells. Lasers Surg Med 34(1):62–72CrossRefGoogle Scholar
  100. Uzdensky A, Kolpakova E, Juzeniene A, Juzenas P, Moan J (2005) The effect of sub-lethal ALA-PDT on the cytoskeleton and adhesion of cultured human cancer cells. Biochim et Biophys Acta (BBA) General Subj 1722(1):43–50Google Scholar
  101. Valenzeno DP (1987) Photomodification of biological membranes with emphasis on singlet oxygen mechanisms. Photochem Photobiol 46(1):147–160Google Scholar
  102. Verma S, Watt GM, Mai Z, Hasan T (2007) Strategies for enhanced photodynamic therapy effects. Photochem Photobiol 83(5):996–1005Google Scholar
  103. Vishwanath M, Takashima A (2007) J Invest Dermatol 127:1546–1549Google Scholar
  104. Waseem Akram M, Fakhare-Alam M et al (2018) Temperature dependent toxic effects of multifarious assembly of magnesium oxide (MgO). In: Nanostructures in a human cervical model in press in scientific report, vol 7Google Scholar
  105. Whelan HT, Schmidt MH, Segura AD, McAuliffe TL, Bajic DM, Murray KJ, Moulder JE, Strother DR, Thomas JP, Meyer GA (1993) The role of photodynamic therapy in posterior fossa brain tumors: a preclinical study in a canine glioma model. J Neurosurg 79(4):562–568CrossRefGoogle Scholar
  106. Whelan HT, Kras LH, Ozker K, Bajic D, Schmidt MH, Liu Y, Trembath LA, Uzum F, Meyer GA, Segura AD, Collier BD (1994) Selective incorporation of 111 In-labeled PHOTOFRIN™ by glioma tissuein vivo. J Neurooncol 22(1):7–13CrossRefGoogle Scholar
  107. Wu SM, Ren QG, Zhou MO, Peng Q, Chen JY (2003) Protoporphyrin IX production and its photodynamic effects on glioma cells, neuroblastoma cells and normal cerebellar granule cells in vitro with 5-aminolevulinic acid and its hexylester. Cancer Lett 200(2):123–131Google Scholar
  108. Xue LY, Chiu SM, Oleinick NL (2001) Photodynamic therapy-induced death of MCF-7 human breast cancer cells: a role for caspase-3 in the late steps of apoptosis but not for the critical lethal event. Exp Cell Res 263(1):145–155CrossRefGoogle Scholar
  109. Zeng L, Ren W, Xiang L, Zheng J, Chen B, Wu A (2013) Multifunctional Fe3O4–TiO2 nanocomposites for magnetic resonance imaging and potential photodynamic therapy. Nanoscale 5(5):2107–2113Google Scholar
  110. Zhang SJ, Zhang ZX (2004) 5-aminolevulinic acid-based photodynamic therapy in leukemia cell HL60. Photochem Photobiol 79(6):545–550CrossRefGoogle Scholar
  111. Zubair Iqbal M, Chen T, Ma X, Zhang L, Ren W et al (2015) Silica coated super-paramagnetic iron oxide nanoparticles (SPIONPs): a new type contrast agent of T1 magnetic resonance imaging (MRI). J Mater Chem B 3:5172–5181Google Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Muhammad Fakhar-e-Alam
    • 1
    • 2
    Email author
  • Arslan Mahmood
    • 1
    Email author
  • Shabab Nasir
    • 3
  • Malik Saadullah
    • 4
  • M. Waseem Akram
    • 5
  • Magnus Willander
    • 6
  1. 1.Department of PhysicsGC UniversityFaisalabadPakistan
  2. 2.Key Laboratory of Magnetic Materials and Devices & Division of Functional Materials and NanodevicesNingbo Institute of Materials Technology and Engineering, Chinese Academy of SciencesNingboChina
  3. 3.Department of ZoologyGC UniversityFaisalabadPakistan
  4. 4.Department of Pharmaceutical ChemistryGC UniversityFaisalabadPakistan
  5. 5.Institute of Fundamental and Frontier Sciences (IFFS), University of Electronic Science and TechnologyChengduChina
  6. 6.Department of Science and TechnologyLinköping UniversityNorrköpingSweden

Personalised recommendations