The effect of cytostatics and hyperthermia on RAJI human lymphoma cells
Aim of this article is to evaluate the effect of hyperthermia on cytostatic activity of chemotherapeutic drugs carboplatin, cisplatin, oxaliplatin, carmustine, gemcitabine and etoposide in human lymphoma cell culture.
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nasplib_isofts_kiev_ua-123456789-323132025-02-23T18:22:57Z The effect of cytostatics and hyperthermia on RAJI human lymphoma cells Istomin, Yu.Р. Zhavrid, E.A. Sachivko, N.V. Alexandrova, E.N. Pocheshinsky, P.V. Original contributions Aim of this article is to evaluate the effect of hyperthermia on cytostatic activity of chemotherapeutic drugs carboplatin, cisplatin, oxaliplatin, carmustine, gemcitabine and etoposide in human lymphoma cell culture. 2011 Article The effect of cytostatics and hyperthermia on RAJI human lymphoma cells / Yu.Р. Istomin, E.A. Zhavrid, N.V. Sachivko, E.N. Alexandrova, P.V. Pocheshinsky // Experimental Oncology. — 2011. — Т. 33, № 1. — С. 19-23. — Біліогр.: 29 назв. — англ. 1812-9269 https://nasplib.isofts.kiev.ua/handle/123456789/32313 en Experimental Oncology application/pdf Інститут експериментальної патології, онкології і радіобіології ім. Р.Є. Кавецького НАН України |
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Original contributions Original contributions |
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Original contributions Original contributions Istomin, Yu.Р. Zhavrid, E.A. Sachivko, N.V. Alexandrova, E.N. Pocheshinsky, P.V. The effect of cytostatics and hyperthermia on RAJI human lymphoma cells Experimental Oncology |
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Aim of this article is to evaluate the effect of hyperthermia on cytostatic activity of chemotherapeutic drugs carboplatin, cisplatin, oxaliplatin, carmustine, gemcitabine and etoposide in human lymphoma cell culture. |
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Article |
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Istomin, Yu.Р. Zhavrid, E.A. Sachivko, N.V. Alexandrova, E.N. Pocheshinsky, P.V. |
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Istomin, Yu.Р. Zhavrid, E.A. Sachivko, N.V. Alexandrova, E.N. Pocheshinsky, P.V. |
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Istomin, Yu.Р. |
| title |
The effect of cytostatics and hyperthermia on RAJI human lymphoma cells |
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The effect of cytostatics and hyperthermia on RAJI human lymphoma cells |
| title_full |
The effect of cytostatics and hyperthermia on RAJI human lymphoma cells |
| title_fullStr |
The effect of cytostatics and hyperthermia on RAJI human lymphoma cells |
| title_full_unstemmed |
The effect of cytostatics and hyperthermia on RAJI human lymphoma cells |
| title_sort |
effect of cytostatics and hyperthermia on raji human lymphoma cells |
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Інститут експериментальної патології, онкології і радіобіології ім. Р.Є. Кавецького НАН України |
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2011 |
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Original contributions |
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https://nasplib.isofts.kiev.ua/handle/123456789/32313 |
| citation_txt |
The effect of cytostatics and hyperthermia on RAJI human lymphoma cells / Yu.Р. Istomin, E.A. Zhavrid, N.V. Sachivko, E.N. Alexandrova, P.V. Pocheshinsky // Experimental Oncology. — 2011. — Т. 33, № 1. — С. 19-23. — Біліогр.: 29 назв. — англ. |
| series |
Experimental Oncology |
| work_keys_str_mv |
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| first_indexed |
2025-11-24T09:38:52Z |
| last_indexed |
2025-11-24T09:38:52Z |
| _version_ |
1849664086203170816 |
| fulltext |
Experimental Oncology ��� ������ ���� ��arc����� ������ ���� ��arc�� ��arc�� ��
THE EFFECT OF CYTOSTATICS AND HYPERTHERMIA ON RAJI
HUMAN LYMPHOMA CELLS
Yu. Р. Istomin*, E.A. Zhavrid, N.V. Sachivko, E.N. Alexandrova, P.V. Pocheshinsky
N.N. Alexandrov National Cancer Center of Belarus, Minsk 223040, Belarus
Aim: To evaluate the effect of hyperthermia on cytostatic activity of chemotherapeutic drugs carboplatin, cisplatin, oxaliplatin,
carmustine, gemcitabine and etoposide in human lymphoma cell culture. Methods: RAJI human lymphoma cells were incubated
with cytostatics at 37 °C or 42 °C and evaluated for cell culture growth. Results: The number of viable cells after incubation with
the drugs (except for gemcitabine) at 42 °C for 30 min was significantly lower than at 37 °C. There were synergism of cytostatic
effects of platinum drugs (carboplatin, cisplatin and oxaliplatin) with cytostatic effect of 42 °C and the summation of cytostatic effect
of carmustine or etoposide with the action of hyperthermia. The thermal enhancement ratio was 3.0 for oxaliplatin, 2.0 for cisplatin,
1.8–2.4 for carboplatin. The combination of platinum drugs with gemcitabine resulted in a significant enhancement of cytostatic
activity. Conclusion: Our findings suggest that a gain in sensitivity of RAJI human lymphoma cells to platinum drugs occurs at 42 °C.
Key Words: RAJI human lymphoma cells, hyperthermia, thermochemotherapy.
Intrinsic drug resistance of tumor cells or t�at
acquired during t�e c�emot�erapy is considered
to be t�e main cause of failures in t�e treatment
of malignant tumors. Overcoming of t�e tumor drug
resistance may open new perspectives in t�e man-
agement of patients for w�om standard t�erapeutic
approac�es are ineffective.
To overcome t�e c�emoresistance� different
p�ysicoc�emical modalities are currently used t�at
can selectively en�ance t�e sensitivity of tumor cells
to anticancer t�erapy. Hypert�ermia is regarded as t�e
most promising modifying factor. It s�ould also take
into account t�e important fact of direct damaging
effect of �eat on t�e tumor.
T�e clinical experience gained until now confirms
t�ese t�eoretical prerequisites. Encouraging results
of w�ole-body �ypert�ermia are ac�ieved in c�emo-
t�erapy for disseminated melanoma [�]� metastatic
sarcoma [�]� recurrent ovarian cancer [��4]� pleural
mesot�elioma [5]� malignant tumors in c�ildren [6]
and ot�er types of tumors [7���]. In a number of cases
�ypert�ermia makes it possible to reduce t�e doses
of administered cytostatics by up to 5�% wit� concur-
rent en�ancement of antitumor effect and decrease
of nep�rotoxic� cardiotoxic and �epatotoxic effects
of t�e c�emot�erapeutic agents.
In experimental models of various tumors� ampli-
fication of cytostatic antitumor effect wit� increased
temperature was demonstrated. Numerous studies
of tumor cell cultures reported increased cytotoxicity
of cyclop�osp�amide� melp�alan� ifosfamide� nitro-
sourea� bleomycin� doxorubicin� platinum prepara-
tions� etoposide� vincristine� taxanes� gemcitabine
[����5]. T�e deat� of tumor cells induced by cyto-
statics was found to rise wit� elevated temperature
and prolonged duration of �eating� and t�e �ig�est-
cytotoxicity was recorded wit� concurrent exposure
to a c�emot�erapeutic agent and �ypert�ermia.
T�e mec�anism of en�ancing antitumor activity
of c�emot�erapeutic agents at elevated temperature
�as not been definitively determined. T�e available
findings suggest t�at permeability of cell membranes
and penetration of drugs into tumor cells are improved�
and t�at t�e mec�anisms of repair of primary and
secondary damage of tumor cells are in�ibited [�6].
Notably� t�e results of experimental studies inves-
tigating t�e interaction between �ypert�ermia and cy-
tostatic drugs are quite contradictive. T�e use of vari-
ous cell lines and experimental tumors� treatment
regimens� temperature levels and drug concentrations
makes it difficult to interpret t�e results of t�e studies.
Investigation of possible t�ermal en�ancement
of �uman lymp�oma cell sensitivity to cytostatic drugs
used in t�e management of t�e disease is of interest
for t�e development of t�ermoc�emot�erapy sc�emes
for malignant lymp�omas. T�e objective of t�is study
was investigation of t�e effect of �ypert�ermia on t�e
cytostatic activity of c�emot�erapeutic agents used
in t�e treatment of malignant lymp�oma; t�e investiga-
tion was conducted on RAJI �uman lymp�oma cell line.
MATERIALS AND METHODS
Chemotherapeutic drugs. T�e effect of t�e
following c�emot�erapeutic agents was evaluated:
carboplatin �c�emocarb� Dabur P�arma Ltd.� In-
dia�� oxaliplatin �eloxatin� Sanofi-Wint�rop Industria�
France�� cisplatin �cytoplatin� CIPLA Ltd.� India��
carmustine �BiCNU� Bristol-�eiers Squibb� Italy��
etoposide �etoposide-Ebewe� Austria�� gemcitabine
�citogem� Dr. Reddy’s Laboratories Ltd.� India�. T�e
drugs were diluted wit� saline or distilled water for
injections according to t�e package insert instructions�
just before t�e experiment.
Cell culture. T�e investigations were conducted
on RAJI �uman lymp�oma cell line �Russian Collection
of Cell Cultures� Cytology Institute of Russian Acad-
emy of Sciences� St. Petersburg�. T�e cell culture was
Received: October 28, 2010.
*Correspondence: E-mail: istomin06@mail.ru
Abbreviations used: IC50 — drug concentration resulting in growth
inhibition by 50% vs. the control; TER — thermal enhancement ratio.
Exp Oncol ����
��� �� �����
�� Experimental Oncology ��� ������ ���� ��arc��
grown in RP�I-�64� culture medium supplemented
wit� ��% fetal calf serum.
Cell treatment. To perform t�e experiments� t�e
cell culture was plated in culture vials� ������� cells
in � ml of t�e culture medium in eac�. Twenty-four �ours
later 5����� µl of cytostatic solution were added into
t�e vials for different final concentrations. T�e vials wit�
t�e cell culture were incubated in �eating bat� circulator
EXATER� U� �Julabo� Germany� at �7 °C or 4� °C for
�5 or �� min and for 48 � in t�e t�ermostat at �7 °C. After
adding �.�% trypan blue to t�e suspension� live �un-
stained� cells were counted in �emocytometer. T�ree
vials wit� cells were used for eac� drug concentration.
Regression analysis of t�e data was employed
to calculate t�e rate of growt� in�ibition of t�e tu-
mor cell culture �IC5� — drug concentration resulting
in growt� in�ibition by 5�% versus t�e control�. T�er-
mal en�ancement ratios �TER� for in�ibition of cell
proliferation for eac� c�emot�erapeutic drug were
calculated as IC5� for drug alone divided by IC5� for
drug combined wit� �ypert�ermia [�7].
T�e values obtained were processed using stand-
ard statistical met�ods of Origin 7.�.
RESULTS AND DISCUSSION
T�e study of RAJI �uman lymp�oma cell culture
growt� demonstrated t�at t�e effect of 4� °C tem-
perature was more prominent wit� increased duration
of �eating. T�e �eating of t�e cells for �5 min did not
actually affect t�e number of viable cells� w�ereas t�e
increase in t�ermal treatment duration up to �� and
6� min resulted in t�e reduction of viable cell numbers
to 64% and 4�%� respectively.
Fig. � presents t�e results of RAJI �uman lym-
p�oma cells incubation wit� c�emot�erapeutic agents
at different concentrations in temperature settings
of �7 °C or 4� °C for �5 and �� min. T�e findings sug-
gest t�at examined drugs induce significant in�ibition
of �uman lymp�oma cell culture growt� at �7 °C� wit�
growing cytostatic effect upon increasing t�e final
concentration of t�e drug in t�e culture medium. T�e
calculation of cytostatic activity rate �IC5�� demonstrated
t�at RAJI �uman lymp�oma cell culture at �7 °C is most
sensitive to etoposide �IC5� = �.� µg/ml�� oxaliplatin
�IC5� = �.� µg/ml� and cisplatin �IC5� = �.8 µg/ml�.
IC5� was 8.5 µg/ml for carboplatin� �.� µg/ml for car-µg/ml for carboplatin� �.� µg/ml for car-�.� µg/ml for car-µg/ml for car-
mustine and 6.5 µg/ml for gemcitabine �Table ��.
Table 1. Cytostatic activity of chemotherapeutic agents at 37 оС and hy-
perthermia setting
Agent IC5�, µg/ml
37 °С 42 °С, 15 min 42 °С, 30 min
Cisplatin 0.8 0.4 (TER = 2.0) 0.4 (TER = 2.0)
Carboplatin 8.5 4.8 (TER = 1.8) 3.6 (TER = 2.4)
Oxaliplatin 0.3 0.1 (TER = 3.0) 0.1 (TER = 3.0)
Carmustine 9.3 8.9 (TER = 1.0) 9.2 (TER = 1.0)
Gemcitabine 6.5 4.7 (TER = 1.4) 8.4 (TER = 0.8)
Etoposide 0.1 0.1 (TER = 1.0) 0.1 (TER = 1.0)
Incubation of RAJI �uman lymp�oma cells wit�
oxaliplatin at 4� °C for �5 min resulted in significant
reduction of cell number compared to �7 °C. Effective-°C. Effective-C. Effective-
ness of gemcitabine and etoposide was not c�anged�
and t�e en�ancement of t�e effect of carboplatin�
cisplatin and carmustine at 4� °C for �5 min was ob-°C for �5 min was ob-C for �5 min was ob-
served only at certain concentrations of t�e drug. Cell
incubation at 4� °C for �� min significantly increased
t�e efficiency of all investigated drugs� except for
gemcitabine �Fig. ��.
T�e calculation of cell culture growt� in�ibition using
IC5� criterion and taking into account t�e reduced num-
ber of cells due to t�e effect of increased temperature
alone demonstrated t�at synergetic amplification of t�e
cytostatic effect by �ypert�ermia occurred wit� oxali-
platin� carboplatin and cisplatin: drug IC5� decreased
from �.� at �7 °C to �.� µg/ml at 4� °C for oxaliplatin�
from 8.5 to 4.8��.6 µg/ml for carboplatin� and from
�.8 to �.4 µg/ml for cisplatin. Summation of drug and
�ypert�ermia effects was observed wit� carmustine and
etoposide� as drug IC5� did not c�ange. Hypert�ermic ex-
posure wit� gemcitabine produced a small amplification
of cell growt� in�ibition wit� �5 min duration of �eating
�IC5� decreased from 6.5 to 4.7 µg/ml compared to t�at
at �7 °C� or reduction of t�e effect wit� �� min duration
of �eating �IC5� increased from 6.5 to 8.4 µg/ml com-
pared to t�at at �7 °C�. T�e t�ermal en�ancement
ratio �TER� of t�e cytostatic effect �t�e ratio of drug
IC5� at �7 °C to IC5� at 4� °C� was �.� for oxaliplatin�
�.� for cisplatin� �.8��.4 for carboplatin� �.� for car-
mustine� �.� for etoposide. T�e TER for gemcitabine
was �.4 wit� �5 min duration of �eating. T�e increase
in �eating duration up to �� min resulted in gemcitabine
effect reduction �see Table ��. T�e differences between
t�e effects at t�e temperatures of �7 °C and 4� °C for
all platinum preparations were statistically significant.
T�e data obtained suggest t�at lymp�oma cells
growt� in�ibition by alkylating c�emot�erapeutic
agents carboplatin� cisplatin� oxaliplatin� carmustine
and plant-derived drug etoposide increases under
�ypert�ermia. For platinum drugs synergetic activ-
ity wit� �ypert�ermia was observed� for carmustine
or etoposide t�ere was t�e summation of cytostatic
effects of drug and �ypert�ermia.
It s�ould be noted t�at t�ere are contradictory
reports about t�e interaction of �ypert�ermia and
gemcitabine. Simultaneous application of gemcitabine
and �eating led to t�e decreased cytotoxicity [�6� ��]�
�ad no influence on cytotoxicity [��] or augmented
cytotoxic effect of t�e drug [��� �8� ��]. Our data did
not allow to consider gemcitabine as a promising drug
for t�ermoc�emot�erapy of lymp�omas. But as gem-
citabine in combination wit� platinum drugs is used for
t�e treatment of refractory lymp�oma� we investigated
t�e effect of �ypert�ermia on t�e cytostatic effect
of t�is combination.
T�e data presented on Fig. � indicate t�at t�e
combination of platinum drugs wit� gemcitabine
�5 µg/ml� at t�e temperature of �7 °C results in signifi-
cant in�ibition of RAJI �uman lymp�oma cell culture
growt�� t�e effect of cytostatics increasing wit� t�e
rise of t�e final concentration of platinum agents.
A convincing corroboration of antitumor effect en-
�ancement is t�e reduction of drug IC5�. W�ile IC5� for
cisplatin alone was �.8 µg/ml� for carboplatin alone
Experimental Oncology ��� ������ ���� ��arc����� ������ ���� ��arc�� ��arc�� ��
8.5 µg/ml� and for oxaliplatin alone �.� µg/ml �see
Table ��� it decreased to �.�6 µg/ml for cisplatin wit�
gemcitabine �5 µg/ ml�� to �.5 µg/ml for carboplatin
wit� gemcitabine� and to �.�� µg/ml for oxaliplatin
wit� gemcitabine �Table ��. T�us� cytostatic activity
of platinum preparations in combination wit� gem-
citabine increased ��-fold for cisplatin� �7-fold for
carboplatin� and ��-fold for oxaliplatin. Gemcitabine
alone �5 µg/ml� at �7 °C reduced t�e number of RAJI
�uman lymp�oma cells only �-folds. T�us� we can
conclude about t�e synergistic action of gemcitabine
wit� t�e platinum drugs at �7 °C.
Incubation of t�e cells wit� platinum drugs in com-
bination wit� gemcitabine at 4� °C for �5 min virtually
did not affect t�e cytostatics activity compared to t�at
at �7 °C. T�e increased duration of cell incubation
at 4� °C up to �� min led to t�e reduction in t�e number
of viable cells compared to t�e numbers observed
at �7 °C �Fig. ��. T�e calculation of cytostatic effect
rates for platinum drugs� taking into account t�e re-
duced number of cells due to t�e effect of increased
temperature alone� demonstrated t�at it was t�e case
of summation of cytostatic effect of platinum drugs
wit� gemcitabine and cytostatic effect of �ypert�ermia
as drug’s IC5� did not actually c�ange after exposure
to �ypert�ermia �see Table ��.
Table 2. Cytostatic activity of platinum drugs in combination with gem-
citabine
Drugs IC5�, µg/ml
37 °С 42 °С, 15 min 42 °С, 30 min
Gemcitabine + cisplatin 0.06 0.06 0.05
Gemcitabine + carboplatin 0.5 0.5 0.4
Gemcitabine + oxaliplatin 0.03 0.03 0.03
0 1 5,0
0
20
40
60
80
100
120 cisplatin
C
el
ln
um
be
r,
%
Concentration, µg/ml
0 10 50
0
20
40
60
80
100
120 carmustine
C
el
ln
um
be
r,
%
Concentration, µg/ml
0 10 50
10
20
30
40
50
60
70
80
90
100
110
120
gemcitabine
C
el
ln
um
be
r,
%
Concentration, µg/ml
0 10 50
-80
-60
-40
-20
0
20
40
60
80
100
120
carboplatin
C
el
ln
um
be
r,
%
Concentration, µg/ml
0,0 0,2 0,4 0,6 0,8 1,0
10
20
30
40
50
60
70
80
90
100
110
120
etoposide
C
el
ln
um
be
r,
%
Concentration, µg/ml
0,0 0,2 0,4 0,6 0,8 1,0
0
20
40
60
80
100
120
oxaliplatin
C
el
ln
um
be
r,
%
Concentration, µg/ml
37 °C 42 °C, 15 min 42 °C, 30 min
Fig. 1. Cytostatic effect related to drug concentration and cell incubation temperature
�� Experimental Oncology ��� ������ ���� ��arc��
0,0 0,1 0,50
-40
-20
0
20
40
60
80
100
120
gemcitabine+oxaliplatin
Concentration of oxaliplatin, µg/ml
0,0 0,1 0,50
-60
-40
-20
0
20
40
60
80
100
120
gemcitabine+cisplatin
Concentration of cisplatin, µg/ml
0 1 5,0
-40
-20
0
20
40
60
80
100
120
gemcitabine+carboplatin
Concentration of carboplatin, µg/ml
Ce
lln
um
be
r,
%
Ce
lln
um
be
r,
%
Ce
lln
um
be
r,
%
Fig. 2. T�e impact of �ypert�ermic exposure �4� °C� �5 or �� min�
and gemcitabine �5 µg/ml� on cytostatic effect of platinum drugs
T�e results of t�e study allowed to assert t�at growt�
in�ibition of RAJI cells by carboplatin� cisplatin� oxali-
platin� carmustine and etoposide was increased by t�e
exposure to 4� °C for �� min. Summation of drug and
�ypert�ermia cytostatic effects was observed for car-
mustine and etoposide� synergic effect — for all plati-
num drugs. T�e t�ermal en�ancement ratio was �.� for
oxaliplatin� �.� for cisplatin and �.8��.4 for carboplatin.
T�e combination of platinum agents wit� gem-
citabine at �7 °C produces a synergic effect of t�e
cytostatics. In suc� combination� IC5� of platinum
drugs was reduced ��-fold for oxaliplatin� ��-fold for
cisplatin� �7-fold for carboplatin. Incubation of t�e cells
wit� platinum preparations in combination wit� gem-
citabine at 4� °C for �� min causes a reduction in t�e
number of viable cells compared to cell incubated
at �7 °C� w�ic� is a result of summation of cytostatic
effects of drugs and �ypert�ermia.
T�e obtained results give grounds to continue
t�e study on animal models wit� feasible prospects
of clinical application.
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