Laser dyes for experimental phototherapy of human cancer: Comparison of three rhodamines
Shaghayegh Haghighat MS
Division of Head and Neck Surgery (Otolaryngology) (D.J.C., R.E.S., S.H., P.H.W.), Department of Radiological Sciences (R.B.L.) and Department of Electrical Engineering (H.R.F.), UCLA School of Medicine, Los Angeles
California Paramedical and Technical College (D.J.C.), Long Beach, California
Service of ORL and Cervicofacial Surgery (J.S.), Hospital De La Pitié, Paris, France
Search for more papers by this authorCorresponding Author
Dan J. Castro MD
Division of Head and Neck Surgery (Otolaryngology) (D.J.C., R.E.S., S.H., P.H.W.), Department of Radiological Sciences (R.B.L.) and Department of Electrical Engineering (H.R.F.), UCLA School of Medicine, Los Angeles
California Paramedical and Technical College (D.J.C.), Long Beach, California
Service of ORL and Cervicofacial Surgery (J.S.), Hospital De La Pitié, Paris, France
Division of Head and Neck Surgery, UCLA School of Medicine, Los Angeles, CA 90024-1624Search for more papers by this authorRobert B. Lufkin MD
Division of Head and Neck Surgery (Otolaryngology) (D.J.C., R.E.S., S.H., P.H.W.), Department of Radiological Sciences (R.B.L.) and Department of Electrical Engineering (H.R.F.), UCLA School of Medicine, Los Angeles
California Paramedical and Technical College (D.J.C.), Long Beach, California
Service of ORL and Cervicofacial Surgery (J.S.), Hospital De La Pitié, Paris, France
Search for more papers by this authorHarold R. Fetterman PhD
Division of Head and Neck Surgery (Otolaryngology) (D.J.C., R.E.S., S.H., P.H.W.), Department of Radiological Sciences (R.B.L.) and Department of Electrical Engineering (H.R.F.), UCLA School of Medicine, Los Angeles
California Paramedical and Technical College (D.J.C.), Long Beach, California
Service of ORL and Cervicofacial Surgery (J.S.), Hospital De La Pitié, Paris, France
Search for more papers by this authorDonna J. Castro CST
Division of Head and Neck Surgery (Otolaryngology) (D.J.C., R.E.S., S.H., P.H.W.), Department of Radiological Sciences (R.B.L.) and Department of Electrical Engineering (H.R.F.), UCLA School of Medicine, Los Angeles
California Paramedical and Technical College (D.J.C.), Long Beach, California
Service of ORL and Cervicofacial Surgery (J.S.), Hospital De La Pitié, Paris, France
Search for more papers by this authorJacques Soudant MD
Division of Head and Neck Surgery (Otolaryngology) (D.J.C., R.E.S., S.H., P.H.W.), Department of Radiological Sciences (R.B.L.) and Department of Electrical Engineering (H.R.F.), UCLA School of Medicine, Los Angeles
California Paramedical and Technical College (D.J.C.), Long Beach, California
Service of ORL and Cervicofacial Surgery (J.S.), Hospital De La Pitié, Paris, France
Search for more papers by this authorPaul H. Ward MD
Division of Head and Neck Surgery (Otolaryngology) (D.J.C., R.E.S., S.H., P.H.W.), Department of Radiological Sciences (R.B.L.) and Department of Electrical Engineering (H.R.F.), UCLA School of Medicine, Los Angeles
California Paramedical and Technical College (D.J.C.), Long Beach, California
Service of ORL and Cervicofacial Surgery (J.S.), Hospital De La Pitié, Paris, France
Search for more papers by this authorRomaine E. Saxton PhD
Division of Head and Neck Surgery (Otolaryngology) (D.J.C., R.E.S., S.H., P.H.W.), Department of Radiological Sciences (R.B.L.) and Department of Electrical Engineering (H.R.F.), UCLA School of Medicine, Los Angeles
California Paramedical and Technical College (D.J.C.), Long Beach, California
Service of ORL and Cervicofacial Surgery (J.S.), Hospital De La Pitié, Paris, France
Search for more papers by this authorShaghayegh Haghighat MS
Division of Head and Neck Surgery (Otolaryngology) (D.J.C., R.E.S., S.H., P.H.W.), Department of Radiological Sciences (R.B.L.) and Department of Electrical Engineering (H.R.F.), UCLA School of Medicine, Los Angeles
California Paramedical and Technical College (D.J.C.), Long Beach, California
Service of ORL and Cervicofacial Surgery (J.S.), Hospital De La Pitié, Paris, France
Search for more papers by this authorCorresponding Author
Dan J. Castro MD
Division of Head and Neck Surgery (Otolaryngology) (D.J.C., R.E.S., S.H., P.H.W.), Department of Radiological Sciences (R.B.L.) and Department of Electrical Engineering (H.R.F.), UCLA School of Medicine, Los Angeles
California Paramedical and Technical College (D.J.C.), Long Beach, California
Service of ORL and Cervicofacial Surgery (J.S.), Hospital De La Pitié, Paris, France
Division of Head and Neck Surgery, UCLA School of Medicine, Los Angeles, CA 90024-1624Search for more papers by this authorRobert B. Lufkin MD
Division of Head and Neck Surgery (Otolaryngology) (D.J.C., R.E.S., S.H., P.H.W.), Department of Radiological Sciences (R.B.L.) and Department of Electrical Engineering (H.R.F.), UCLA School of Medicine, Los Angeles
California Paramedical and Technical College (D.J.C.), Long Beach, California
Service of ORL and Cervicofacial Surgery (J.S.), Hospital De La Pitié, Paris, France
Search for more papers by this authorHarold R. Fetterman PhD
Division of Head and Neck Surgery (Otolaryngology) (D.J.C., R.E.S., S.H., P.H.W.), Department of Radiological Sciences (R.B.L.) and Department of Electrical Engineering (H.R.F.), UCLA School of Medicine, Los Angeles
California Paramedical and Technical College (D.J.C.), Long Beach, California
Service of ORL and Cervicofacial Surgery (J.S.), Hospital De La Pitié, Paris, France
Search for more papers by this authorDonna J. Castro CST
Division of Head and Neck Surgery (Otolaryngology) (D.J.C., R.E.S., S.H., P.H.W.), Department of Radiological Sciences (R.B.L.) and Department of Electrical Engineering (H.R.F.), UCLA School of Medicine, Los Angeles
California Paramedical and Technical College (D.J.C.), Long Beach, California
Service of ORL and Cervicofacial Surgery (J.S.), Hospital De La Pitié, Paris, France
Search for more papers by this authorJacques Soudant MD
Division of Head and Neck Surgery (Otolaryngology) (D.J.C., R.E.S., S.H., P.H.W.), Department of Radiological Sciences (R.B.L.) and Department of Electrical Engineering (H.R.F.), UCLA School of Medicine, Los Angeles
California Paramedical and Technical College (D.J.C.), Long Beach, California
Service of ORL and Cervicofacial Surgery (J.S.), Hospital De La Pitié, Paris, France
Search for more papers by this authorPaul H. Ward MD
Division of Head and Neck Surgery (Otolaryngology) (D.J.C., R.E.S., S.H., P.H.W.), Department of Radiological Sciences (R.B.L.) and Department of Electrical Engineering (H.R.F.), UCLA School of Medicine, Los Angeles
California Paramedical and Technical College (D.J.C.), Long Beach, California
Service of ORL and Cervicofacial Surgery (J.S.), Hospital De La Pitié, Paris, France
Search for more papers by this authorRomaine E. Saxton PhD
Division of Head and Neck Surgery (Otolaryngology) (D.J.C., R.E.S., S.H., P.H.W.), Department of Radiological Sciences (R.B.L.) and Department of Electrical Engineering (H.R.F.), UCLA School of Medicine, Los Angeles
California Paramedical and Technical College (D.J.C.), Long Beach, California
Service of ORL and Cervicofacial Surgery (J.S.), Hospital De La Pitié, Paris, France
Search for more papers by this authorAbstract
The mitochondrial dye Rhodamine 123 (Rh-123) has been shown to be an effective photosensitizer for argon-laser irradiation of some types of human cancer cells in vitro. We reported that 514.5-nm laser illumination of Rh-123 sensitized human melanoma, and squamous carcinoma cells strongly inhibited tumor-cell proliferation as measured by decreased 3H-thymidine (3H-T) uptake in vitro and may eradicate some tumors when grown as transplants in nude mice. However, several other human tumors were resistant to Rh-123 laser therapy in vitro and in vivo. In the current study, it was possible to obtain 100- to 1000-fold increased sensitivity to 514.5-nm laser illumination by replacement of Rh-123 with the cationic rhodamine dyes Rh-3G and Rh-6G. Cell viability was decreased over 95% and 3H-T incorporation reduced at least 80% by laser phototherapy after sensitizing tumor cells with 1 μg/mL Rh-123, 0.01 μg/mL Rh-3G, or 0.001 μg/mL Rh-6G. However, Rh-123 alone did not decrease 3H-T uptake significantly unless present at over 10- to 100-fold higher levels than Rh-3G, respectively. The tumor cell dye uptake level was measured by N-butanol extraction and absorption scans at 400 to 600 nm. The results revealed that dye uptake was more rapid, and retention of Rh-3G and Rh-6G was 5- to 10-fold higher than for Rh-123 in the human tumor cells. The data suggest that Rh-3G and Rh-6G may be highly sensitive chromophores for laser phototherapy of human cancer cells.
Bibliography
- 1 Dougherty, T.J., Kaufman, J.E., Goldfarb, A., et al.: Photoradiation Therapy for the Treatment of Malignant Tumors. Cancer Res, 38: 2628–2635, 1978.
- 2 Moore, G.E.: Fluorescein as an Agent in the Differentiation of Normal and Malignant Tissues. Science, 106: 130–131, 1947.
- 3
Rassmussen-Taxdal, D.S.,
Ward, G.E. and
Figge, F.H.J.:
Fluorescence of Human Lymphatic and Cancer Tissues Following High Doses of Intravenous Hematoporphyrin.
Cancer,
8:
78–81,
1955.
10.1002/1097-0142(1955)8:1<78::AID-CNCR2820080109>3.0.CO;2-L CAS PubMed Web of Science® Google Scholar
- 4 Kochevar, I.E.: Phototoxicity Mechanisms: Chlorpromazine Photosensitized Damage to DNA and Cell Membranes. J Invest Dermatol, 77: 59–64, 1981.
- 5 Figge, F.H.J., Weiland, G.S. and Manganiello, L.O.J.: Cancer Detection and Therapy. Affinity of Neoplastic, Embryonic, and Traumatized Tissues for Porphyrins and Metalloporphyrins. Proc Soc Exp Biol Med, 68: 640–641, 1948.
- 6 Castro, D.J., Gaskin, A., Saxton, R.E., et al.: Photodynamic Therapy Using Rhodamine-123 as a New Laser Dye: Biodistribution, Metabolism and Histology in New Zealand Rabbits. LARYNGOSCOPE, 101: 158–164, 1991.
- 7 Castro, D.J., Saxton, R.E., Reisler, E., et al.: Pharmacokinetics of Rhodamine-123 in Nude Mice Heterotransplanted With Human Carcinomas. LARYNGOSCOPE. Submitted.
- 8 Castro, D.J., Saxton, R.E., Fetterman, H.R., et al.: Rhodamine-123 as a New Photochemosensitizing Versus Toxic Agent on Human Squamous Carcinoma Cells and Fibroblast Cultures. Arch Otolaryngol. Submitted.
- 9 Castro, D.J., Saxton, R.E., Fetterman, H.R., et al.: Rhodamine-123 as a New Photochemosensitizing Agent With the Argon Laser: “Nonthermal” and Thermal Effects on Human Squamous Carcinoma Cells In Vitro. LARYNGOSCOPE, 97: 554–561, 1987.
- 10 Castro, D.J., Saxton, R.E., Fetterman, H.R., et al.: The Effects of Argon Laser on Human Melanoma Cells Sensitized With Rhodamine-123 In-Vitro: Study of a New Photochemosensitizing Agent. Am J Otolaryngol, 8: 18–29, 1988.
- 11 Castro, D.J., Saxton, R.E., Fetterman, H.R., et al.: Rhodamine-123 as a Chemosensitizing Agent for Argon Laser Therapy: A New Technique for Treatment of Superficial Malignancies. Arch Otolaryngol, 113: 1176–1182, 1987.
- 12 Castro, D.J., Saxton, R.E., Fetterman, H.R., et al.: Photodynamic Therapy Using the Argon Laser on Human Carcinoma Cells Sensitized With Rhodamine-123: A Study of Tumor Growth Rate After Heterotransplantation to Nude Mice. Presented at the Meeting of the American Society for Head and Neck Surgery, Denver, April 30, 1987.
- 13 Castro, D.J., Saxton, R.E., Fetterman, H.R., et al.: Phototherapy With the Argon Laser on Human Melanoma Cells “Sensitized” With Rhodamine-123: New Method of Tumor Growth Inhibition. LARYNGOSCOPE, 98: 369–376, 1988.
- 14 Castro, D.J., Saxton, R.E., Fetterman, H.R., et al.: Phototherapy With Argon Lasers and Rhodamine-123 for Tumor Eradication. Otolaryngol Head Neck Surg, 98: 581–588, 1988.
- 15 Castro, D.J., Saxton, R.E., Fetterman, H.R., et al.: New Concepts in Photodynamic Therapy With Lasers. In: Head and Neck Cancers, W. Fee, H. Goepfert, M. Johns, et al. (Eds.). B.C. Decker, Toronto, pp. 400–408, 1989.
- 16 Castro, D.J., Saxton, R.E., Rodgerson, D.O., et al.: Rhodamine-123 as a New Laser Dye: In Vivo Study of Dye Effects on Murine Metabolism, Histology and Ultrastructure. LARYNGOSCOPE, 99: 1057–1062, 1989.
- 17 Sugita, K., Giulliano, A.E., Sugita, N., et al.: Tumors of Diverse Histology Are Sensitive to Rhodamine-123 Laser Phototherapy In Vitro. Am J Otolaryngol, 11: 1–7, 1990.
- 18 Johnson, L.V., Walsh, M.L. and Chen, L.B.: Localization of Mitochondria in Living Cells With Rhodamine 123. Proc Natl Acad Sci (USA), 77: 990–994, 1980.
- 19 Kasai, M., Saxton, R.E., Holmes, E.C., et al.: Hybridoma Monoclonal Antibody: Use in Defining Surface Antigens on Human Lung Carcinoma Cells. Transplant Proc, 13 (4): 1942–1945, 1981.
- 20 Kasai, M., Saxton, R.E., Holmes, E.C., et al.: Membrane Antigens Detected on Human Lung Carcinoma Cells by Hybridoma Monoclonal Antibody. J Surg Res, 30: 403–408, 1981.
- 21 Iwaki, Y., Jasai, M., Terasaki, P.I., et al.: Monoclonal Antibody Against A1 Lewis Antigen Produced by the Hybridoma Immunized With a Pulmonary Carcinoma. Cancer Res, 42: 409–411, 1982.
- 22 Castro, D.J., Saxton, R.E., Markley, J., et al.: Argon Laser Phototherapy of Human Malignancies Using Rhodamine-123 as a New Laser Dye: The Intracellular Role of Oxygen. LARYNGOSCOPE, 100: 884–891, 1990.
- 23 Powers, S.K., Pribil, S., Gillespie, G.Y., et al.: Laser Photochemotherapy of Rhodamine-123 Sensitized Human Glioma Cells In Vitro. J Neurosurg, 64: 918–923, 1986.
- 24 Kubin, R.F. and Fletcher, A.N.: Fluorescence Quantum Yields of Some Rhodamine Dyes. J Lumin, 27: 455–462, 1982.
- 25 Modica-Napolitano, J.S., Weiss, M.J., Chen, L.B., et al.: Rhodamine-123 Inhibits Bioenergetic Function in Isolated Rat Liver Mitochondria. Biochem Biophys Res Commun, 118: 717–723, 1984.
- 26 Summerhayes, I.C., Lampidis, T.J., Bernal, S.D., et al.: Unusual Retention of R-123 by Muscle and Carcinoma Cells. Proc Natl Acad Sci USA, 79: 5292–5296, 1982.
- 27 Johnson, L.V., Walsh, M.L. and Chen, L.B.: Localization of Mitochondria in Living Cells With Rhodamine-123. Proc Natl Acad Sci USA, 77: 990–994, 1980.
- 28 Marchesini, R., Melloni, B., Dasdia, T., et al.: Photosensitizing Properties of Rhodamine-123 on Different Human Tumor Cell Lines. Lasers Surg Med, 6 (2): 163, 1986.
- 29 Powers, S.K., Pribil, S., Gillespie, G.Y., et al.: Laser Phototherapy of Rhodamine-123 Sensitized Human Glioma In-Vitro. J Neurosurg, 6, 4: 918–923, 1986.
- 30 Melloni, G., Dasdia, T., Fava, G., et al.: In-Vitro Photosensitizing Properties of Rhodamine-123 on Different Human Tumor Cell Lines. Photochem Photobiol, 48: 311–314, 1988.
- 31 Weishaupt, K.R., Doiron, D.R. and Fisher, G.U.: Identification of Singlet Oxygen and the Cytotoxic Agent in Photoradiation of Murine Tumor. Cancer Res, 36: 2316–2319, 1976.
- 32 Chow, A., Kennedy, S., Pottier, R., et al.: Rhodamine-123 Photophysical and Photochemical Properties. Photobiochem Photobiophys, 11: 139–148, 1986.
- 33 Shea, C.R., Chen, N., Wimberly, J., et al.: Rhodamine Dyes as Potential Agents for Photochemotherapy of Cancer in Human Bladder Carcinoma Cells. Cancer Res, 49: 3961–3965, 1989.