DOI: 10.1111/j.1751-1097.1995.tb02356.x. THE ROLE OF TRANSFERRIN RECEPTOR (CD71) IN PHOTODYNAMIC THERAPY OF ACTIVATED AND MALIGNANT LYMPHOCYTES USING THE HEME PRECURSOR δ‐AMINOLEVULINIC ACID (ALA)

THE ROLE OF TRANSFERRIN RECEPTOR (CD71) IN PHOTODYNAMIC THERAPY OF ACTIVATED AND MALIGNANT LYMPHOCYTES USING THE HEME PRECURSOR δ‐AMINOLEVULINIC ACID (ALA)

10.1111/j.1751-1097.1995.tb02356.x

Crossref journal-article

Wiley

Photochemistry and Photobiology (311)

Abstract

AbstractEndogenously generated protoporphyrin IX (PpIX) from exogenous ALA can be an effective photosensitizer. PpIX accumulation is inversely dependent on available intracellular iron, which is required for the conversion of PpIX to heme. Iron also is necessary for cell replication. Since iron can be toxic, intracellular iron levels are tightly controlled. Activated and proliferating cells respond to the demand for intracellular iron by upregulating membrane expression of the transferrin receptor (CD71) which is needed for iron uptake. We predicted that activated lymphocytes (CD71 +) would preferentially accumulate PpIX because of their lower intracellular iron levels and because of competition for iron between ALA‐induced heme production and cellular growth processes. Thus, the CD71+ cells could serve as PDT targets. Stimulation of human peripheral blood lymphocytes (PBL) with the mitogens, phytohemagglutinin A, concanavalin A and pokeweed prior to incubation with ALA results in PpIX accumulation correlating with level of activation. Activated lymphocytes expressing high levels of surface CD71 transferrin receptors generated more PpIX than those with low CD71 expression. Incubating activated cells in transferrin depleted medium (thereby decreasing the iron availability) further increased PpIX levels. Malignant, CD71 + T lymphocytes from a patient with cutaneous T‐cell lymphoma (CTCL)/Sezary syndrome also accumulated increased PpIX levels in comparison to norma] lymphocytes. PDT of activated lymphocytes and Sezary cells after ALA incubation demonstrated preferential killing compared to normal, unstimulated PBL. These findings suggest a possible mechanism for the selectivity of ALA PDT for activated CD71+ cells. They also indicate a clinical use for ALA‐PDT in therapy directed towards the malignant lymphocytes in leukemias and lymphomas, and as animmunomodulatory agent.

Bibliography

RittenhouseâDiakun, K., Leengoed, H. V., Morgan, J., Hryhorenko, E., Paszkiewicz, G., Whitaker, J. E., & Oseroff, A. R. (1995). THE ROLE OF TRANSFERRIN RECEPTOR (CD71) IN PHOTODYNAMIC THERAPY OF ACTIVATED AND MALIGNANT LYMPHOCYTES USING THE HEME PRECURSOR Î´âAMINOLEVULINIC ACID (ALA). Photochemistry and Photobiology, 61(5), 523â528. Portico.

Authors 7

K. Rittenhouse‐Diakun (first)
H. VAN Leengoed (additional)
J. Morgan (additional)
E. Hryhorenko (additional)
G. Paszkiewicz (additional)
J. E. Whitaker (additional)
A. R. Oseroff (additional)

References 41 Referenced 102

10.1038/bjc.1987.246
10.1016/0304-3835(88)90211-X
10.1038/bjc.1992.83
10.1016/0304-3835(92)90156-P
{'key': 'e_1_2_2_6_2', 'first-page': '363', 'article-title': 'Effect of available iron on the accumulation of protoporphyrinIX, an endogenously synthesized photosensitizer produced from exogenous U‐aminolevu‐linic acid', 'volume': '34', 'author': 'Licznerski B.', 'year': '1993', 'journal-title': 'Proc. Annu. Meet. Am. Assoc. Cancer Res'} / Proc. Annu. Meet. Am. Assoc. Cancer Res / Effect of available iron on the accumulation of protoporphyrinIX, an endogenously synthesized photosensitizer produced from exogenous U‐aminolevu‐linic acid by Licznerski B. (1993)
10.1038/bjc.1994.244
10.1006/abbi.1993.1099
10.1159/000163610
{'key': 'e_1_2_2_10_2', 'first-page': '241', 'article-title': 'The transferrin receptor', 'volume': '4', 'author': 'Testa U.', 'year': '1993', 'journal-title': 'Critical Reviews in Oncogenesis'} / Critical Reviews in Oncogenesis / The transferrin receptor by Testa U. (1993)
10.1016/S0021-9258(19)38621-1 / Journal of Biological Chemistry / Interleukin‐2‐dependent transcriptional and post‐transcriptional regulation of transferrin receptor mRNA by Seiser C. (1993)
{'key': 'e_1_2_2_12_2', 'first-page': '615', 'article-title': 'PDT with topical U‐aminolevulinic acid (ALA) for the treatment of patch and plaque stage cutaneous T‐cell lymphoma.', 'volume': '102', 'author': 'Shanler S.D.', 'year': '1994', 'journal-title': 'J. Invest. Dermatol.'} / J. Invest. Dermatol. / PDT with topical U‐aminolevulinic acid (ALA) for the treatment of patch and plaque stage cutaneous T‐cell lymphoma. by Shanler S.D. (1994)
10.1111/j.1365-2133.1994.tb03412.x
10.1016/S0190-9622(08)81742-2
Shanler S.D. D.A.Buscaglia H.L.Stoll E.Van Leengoed W.Wan J.E.Whitaker M.Barcos S.H.PincusandA.R.Oseroff(1995)Photodynamic therapy with topical U‐aminolcvulinic acid (ALA) for the treatment of cutaneous T‐cell lymphoma. submitted.
10.1016/0022-1759(94)90396-4
10.4049/jimmunol.142.6.2037 / J. Immunol. / Synthetic antigens as immungens: Part III. Specificity analysis of an anti‐anti‐idiotypic antibody to a carbohydrate tumor associated antigen by Diakun K.R. (1989)
10.1016/1011-1344(89)80005-3
10.1016/1011-1344(90)85083-9
10.1016/1011-1344(92)85108-7
10.1016/1011-1344(93)80048-E
{'key': 'e_1_2_2_22_2', 'first-page': '43', 'article-title': 'Clinical studies with topical 5‐aminolevulinic acid (ALA) and Photofrin: Results and mechanisms', 'volume': '14', 'author': 'Oseroff A.R.', 'year': '1994', 'journal-title': 'Lasers Surg. Med.'} / Lasers Surg. Med. / Clinical studies with topical 5‐aminolevulinic acid (ALA) and Photofrin: Results and mechanisms by Oseroff A.R. (1994)
10.1038/bjc.1994.288
10.1038/bjc.1994.112
10.1111/j.1600-0560.1982.tb01042.x
10.1016/S0190-9622(86)70163-1
10.1111/j.1751-1097.1987.tb04741.x
{'key': 'e_1_2_2_28_2', 'first-page': '387', 'volume-title': 'Clinical Photomedicine', 'author': 'Oseroff A.R.', 'year': '1993'} / Clinical Photomedicine by Oseroff A.R. (1993)
{'key': 'e_1_2_2_29_2', 'first-page': '81', 'volume-title': 'Iron in Immunity, Cancer and Inflammation', 'author': 'Brock J.H.', 'year': '1989'} / Iron in Immunity, Cancer and Inflammation by Brock J.H. (1989)
10.4049/jimmunol.136.7.2342 / J. Immunol. / Desferoxamine blocks IL2 receptor expression on human T lymphocytes by Carotenuto P. (1986)
10.1182/blood.V75.10.1903.1903
{'key': 'e_1_2_2_32_2', 'first-page': '4144', 'article-title': 'Inhibition of hematopoetic tumor growth by combined treatment with deferoxamine and an IgG monoclonal antibody against the transferrin receptor: Evidence for a threshold model of iron deprivation toxicity', 'volume': '52', 'author': 'Kemp J.D.', 'year': '1992', 'journal-title': 'Cancer Res'} / Cancer Res / Inhibition of hematopoetic tumor growth by combined treatment with deferoxamine and an IgG monoclonal antibody against the transferrin receptor: Evidence for a threshold model of iron deprivation toxicity by Kemp J.D. (1992)
10.4049/jimmunol.153.7.3286 / J. Immunol. / Inhibition of human peripheral blood lymphocyte function by protoporphyrin and longwave ultraviolet light by Barrett K.E. (1994)
10.4049/jimmunol.144.11.4327 / J. Immunol. / Dual effects of protoporphyrin and longwave ultraviolet radiation on histamine release from rat peritoneal and cutaneous mast cells by Yen A. (1994)
10.1111/j.1751-1097.1988.tb02894.x
{'key': 'e_1_2_2_36_2', 'first-page': '131', 'article-title': 'Immunosuppression in phototherapy', 'volume': '146', 'author': 'Ulrich S.E.', 'year': '1989', 'journal-title': 'Ciba Found. Symp'} / Ciba Found. Symp / Immunosuppression in phototherapy by Ulrich S.E. (1989)
10.1002/jca.2920090108
10.1006/clin.1994.1139
10.1001/archderm.128.11.1479
10.1016/0190-9622(90)70360-T
10.1111/1523-1747.ep12466140
10.1016/0190-9622(91)70111-E

Dates

Type	When
Created	17 years, 8 months ago (Jan. 2, 2008, 2:41 p.m.)
Deposited	1 year, 10 months ago (Oct. 26, 2023, 7:39 p.m.)
Indexed	1 year ago (Aug. 11, 2024, 11:49 a.m.)
Issued	30 years, 4 months ago (May 1, 1995)
Published	30 years, 4 months ago (May 1, 1995)
Published Online	17 years, 8 months ago (Jan. 2, 2008)
Published Print	30 years, 4 months ago (May 1, 1995)

Funders 0

None

BibTeX

@article{Rittenhouse_Diakun_1995, title={THE ROLE OF TRANSFERRIN RECEPTOR (CD71) IN PHOTODYNAMIC THERAPY OF ACTIVATED AND MALIGNANT LYMPHOCYTES USING THE HEME PRECURSOR δ‐AMINOLEVULINIC ACID (ALA)}, volume={61}, ISSN={1751-1097}, url={http://dx.doi.org/10.1111/j.1751-1097.1995.tb02356.x}, DOI={10.1111/j.1751-1097.1995.tb02356.x}, number={5}, journal={Photochemistry and Photobiology}, publisher={Wiley}, author={Rittenhouse‐Diakun, K. and Leengoed, H. VAN and Morgan, J. and Hryhorenko, E. and Paszkiewicz, G. and Whitaker, J. E. and Oseroff, A. R.}, year={1995}, month=may, pages={523–528} }

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