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- Publisher
- Pubmed Central
- ISSN
- 0910-5050
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- 1876-4673
- DOI
- 10.1111/j.1349-7006.2000.tb00886.x
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Abstract
Jpn. J. Cancer Res. 91, 1065–1072, October 2000 1, 4 1 2 3 1 Masanori Kato, Naomasa Ioritani, Takashi Suzuki, Mariko Kambe, Yasuo Inaba, Ryuji 1 2 1 Watanabe, Hironobu Sasano and Seiichi Orikasa 1 2 Department of Urology and Department of Pathology, Tohoku University School of Medicine, 1-1 Seiryou-chou, Aoba-ku, Sendai 980-8575 and Department of Internal Medicine, Senseki Hospital, 53-7 Akai Aza Dai, Monow-gun, Miyagi 981-0501 We have previously reported marked enhancement of the cytocidal effect of bleomycin (BLM) on cancer cell suspensions in vitro by the combination with shock waves. In this study, we evaluated the synergistic effects on cancer cell proliferation and apoptosis in solid tumors. A spherical piezo- ceramic element was used as the shock wave source, with a pressure peak of 40 MPa. A human colon cancer cell line, SW480 was implanted onto the back of nude mice. Two thousand shock waves were administered to the tumor immediately following an intravenous injection of BLM at a dose of one-tenth of the LD . The tumor was extirpated at 3, 6, 12, 24, 72 h and 1 week following shock exposure. Cell proliferation and apoptosis were detected by Ki-67 using antibody MIB-1 and by the terminal deoxynucleotidyl transferase (TdT)-mediated dUTP-biotin nick-end labeling (TUNEL) method. The lowest percentage (35.7%) of Ki-67-positive cells appeared 24 h following the treatment. The maximum apoptotic index was detected within 6 h following the treatment. Moreover, numerous large cells with enlarged nuclei were detected histologically. These results suggest that shock waves may enhance chemotherapeutic effects by increasing apoptosis and decreasing cell proliferation in the tumor tissue. Key words: Shock wave — Bleomycin — SW480 — TUNEL — Mitotic death A focused underwater shock wave can exert a high membrane, because reagents such as propidium iodide and acoustic intensity in deep portions of the body without 5(6)-carboxyfluorescein could enter the cytoplasm of the causing damage to adjacent tissues because of its high per- cells treated with shock waves. The mechanism of this 1 – 3) meability through the tissues. The apparent feasibility enhancement of chemotherapeutic effect was considered to of exposing a spatially limited region of the body to a be the entry of BLM molecules into cells through pores potentially destructive form of mechanical energy has led opened by the shock waves, but the details remain 4) to the idea of applying shock waves in tumor therapy. unknown. Previous results have not necessarily been promising, in When SW480, a human colon cancer cell line, was 4 – 8) cases of shock wave therapy alone, or in combination transplanted onto the back of nude mice, which were with various anti-cancer agents, for example, cis- treated with a combination of intravenously (i.v.) injected 9 – 13) 12, 13) 12) platinum, mitomycin C (MMC), actinomycin D, BLM and regional exposure to shock waves, a significant 13) 11, 13, 14) methotrexete and adriamycin (ADR). However, enhancement in the chemotherapeutic effects was also 15, 16) we have reported that the combination of focused shock detected in terms of tumor growth. Therefore, in this waves and bleomycin (BLM) reduced the IC of BLM to study, we examined the synergistic effect on cancer cell 1 / 10 000 –1/100 000 in various human cancer cell lines, proliferation and apoptosis in vivo using immunohis- 15, 16) when compared to BLM alone. This effect was tochemical staining with MIB-1 and the terminal deoxynu- detected even with a weak shock wave energy, which cleotidyl transferase (TdT)-mediated dUTP-biotin nick- alone had almost no cytotoxic effect, and the degree of end labelling (TUNEL) method, as well as transmission cytotoxicity enhancement was proportional to the amount electron microscopy, in an effort to elucidate the mecha- 15, 16) of shock wave energy applied. Immediately after nism involved. shock wave exposure, cancer cells were examined under scanning and transmission electron microscopes. Numer- MATERIALS AND METHODS ous dimples (diameters distributed from 0.05 to 0.5 µ m) 15, 16) became apparent on the cell surface. These dimples Mice Male BALB / c nude mice, 5 weeks of age, weighing were concluded to be pores penetrating through the cell 16 – 20 g, were purchased from CLEA Japan Inc. (Tokyo). Cells SW480 cells, histologically demonstrating adeno- 17) carcinoma features, derived from human colon cancer To whom correspondence should be addressed. E-mail: [email protected] were obtained from the Cell Resource Center for Biomedi- 1065 Jpn. J. Cancer Res. 91, October 2000 cal Research, Institute of Developing, Aging and Cancer, BLM dose was one-tenth of the LD and the dose of the Tohoku University (Sendai). The SW480 cell line was cul- shock wave was 2000 shots at 40 MPa. For the combina- tured in modified Eagle’s minimum essential medium tion treatment, BLM was administered i.v. just before (MEM) with 10% fetal bovine serum (FBS) (GIBCO exposure to the shock waves. BRL, Grand Island, NY), penicillin (100 U / ml) and strep- Tumors were extirpated 3, 6, 12, 24, 72 h and 7 days tomycin (100 µ g/ml) (Bio Whittaker, Walkersville, ML), after the treatment. Each group consisted of at least 4 at 37°C and 5% CO . For transplantation in vivo, 1 × 10 mice. Fixation was performed using 4% paraformaldehyde SW480 cells were injected subcutaneously (s.c.) into the overnight. backs of nude mice to grow tumors. Autoradiography Cobalt-57 was obtained as carrier-free Anticancer agent Water-soluble Bleomycin (BLM) was CoCl (37 MBq/ ml) in 0.1 N HCl from the Japan Radio- supplied by Nihon Kayaku Co., Ltd. (Tokyo). isotope Association (Tokyo). The labeling procedure has 18) Shock wave generator The shock wave generator was been described by Grove et al. The final concentration designed to generate focused underwater shock waves at of Co-BLM was adjusted to 300 kBq/ml, 3 mg/ml. various frequencies and intensities by Toshiba Co., Ltd. These labeled BLM complexes were injected into the (Tokyo). This instrument is comprised of a high-voltage tumor-bearing mouse i.v. (BLM 1 mg, 100 kBq/mouse). electric current generator and a reflector. On the surface of Immediately after the injection of Co-BLM, the tumor the generator, piezo-ceramic elements were arranged to was exposed to 2000 shock wave shots at 20 MPa. A form part of a sphere. The pressure on the focal area (the control mouse was treated with Co-BLM (i.v.) alone. center of the sphere) was proportional to the voltage Ten minutes after the injection, the mice were sacrificed applied to the elements. For in vivo experiments, the and prepared for whole body autoradiography according to 19) reflector was covered with a rubber bag filled with the method established by Ullberg. Mice were sliced 20, 21) degassed water and the mice were fixed so the tumor was into 35 µ m sections and exposed to an imaging plate located at the focal area (Fig. 1). (Fuji Photo Film Co., Ltd., Tokyo) for 3 h, and then ana- Shock wave exposure When tumors that were trans- lyzed with a Bio-imaging analyzer, BAS 2000 (Fuji Photo planted s.c. into nude mice had grown to approximately Film Co., Ltd.). 10 ×10 mm, shock wave exposure and administration of Morphological analysis The paraffin-embedded blocks, BLM were performed following anesthesia with intraperi- fixed in 4% paraformaldehyde, were cut into 4 µ m sec- toneally injected pentobarbital sodium (40 mg/kg). The tions. One section from each sample was stained with hematoxylin and eosin (HE). For electron microscopy, treated tumors were fixed with 2% glutaraldehyde for 1 h, dehydrated, processed and observed using a H-600 (Hita- chi Co., Ltd., Tokyo) electron microscope. Immunohisochemistry Analysis of the synergistic effect of shock waves and BLM on cell proliferation was per- formed using a Ki-67 immunostain, employing MIB-1 antibody (Immunotech, Marseille, France) as the primary antibody. Tissue sections (4 µ m), which were cut from 4% paraformaldehyde-fixed, paraffin-embedded blocks, were deparaffinized and autoclaved in 10 mM acetate buffer at 120°C for 5 min. After cooling, slides were incubated overnight at 4°C with a 1:50 dilution of the primary antibody MIB-1. The avidin-biotin-peroxidase complex method was used for immunohistochemical staining. Slides were incubated with the biotinylated anti-immuno- globulins for 20 min at room temperature. The streptavi- din-conjugated peroxidase was applied to the slides for 20 min, followed by exposure to 0.05% diaminobenzidine Fig. 1. Experimental apparatus for in vivo shock wave expo- (DAB). Following immunostaining, sections were counter- sure. Piezo-ceramic elements were arranged in partial spherical stained with hematoxylin and coverslipped with an aque- form, and the generated shock wave propagates inside the rubber ous mounting medium. bag filled with degassed water and is focused at the geometric In situ detection of apoptosis To detect apoptotic cells in center. An anesthetized mouse was fixed so its tumor was sections of paraformaldehyde-fixed, paraffin-embedded located at the focal area. The interface between the rubber bag tissue, TUNEL method was used according to the proce- and the skin of the mouse was daubed with acoustic gel to adapt the acoustic impedance. dures included in the Wako in situ apoptosis detection kit 1066 Shock Wave Chemotherapy on Solid Tumor (Wako Co., Ltd., Osaka). Briefly, after deparaffinization, Time course of suppression of cell proliferation caused sections were incubated with a protein digestion enzyme by BLM with shock waves The proliferation of SW480 for 5 min at 37°C. TdT with biotin-11-dUTP and dATP was suppressed following shock wave exposure with BLM was applied to the slides for 10 min at 37°C in a moist administration, based on counting of the positive ratio of chamber. Endogenous peroxidase was inactivated by cov- Ki-67 expression (Fig. 3, A and B). The suppression began ering the sections with 3% hydrogen peroxide for 5 min at just following the treatment (closed circle, Fig. 3A) and room temperature. Then, anti-biotin-11-dUTP labeling was was maintained until almost 24 h after treatment. The per- conducted for 10 min at 37°C, followed by exposure to centage of Ki-67 positive cells, which was 68.7% at begin- DAB. Sections were counterstained with 0.5% methyl ning of treatment, reached a minimum of 35.7% after a time 22) green solution. One thousand cells were counted in a period corresponding roughly to the doubling time. Our visual field at random, and the average of four fields was findings show that the Ki-67-positive ratio decreased until used to determine the apoptotic index. 24 h and then gradually increased over the next 7 days. Time course of apoptosis after exposure to shock waves with BLM The percentage of TUNEL-positive cells, RESULTS which was 1.22% at the beginning of treatment, reached a Introduction of Co-BLM into the tumor analyzed by maximum of 6.21% at 6 h following the combined treat- autoradiography We performed autoradiography as a pre- ment with shock waves and BLM (Fig. 4A). We also ana- liminary study to examine the difference of accumulation lyzed the expression of an apoptotic cell marker 6 h of labeled BLM between shock wave-treated mouse and following the treatment in four groups, control, BLM the control. Significant accumulation of Co-BLM was alone, shock waves alone and combination of shock waves detected in the liver, bone marrow, skin, and lung 10 min and BLM (Fig. 4B). The apoptotic index in the combined following the i.v. injection. However, accumulation in the therapy group was significantly higher than that of the tumor was not marked (Fig. 2A). In the tumor exposed to other three groups (Fig. 4C). shock waves, a two-fold higher level of radiation was Morphological analysis SW480 tumor cells showed detected compared to the control. The level of radioactiv- great morphological variation 6 h following combined ity in the tumor was divided by that of the liver in the treatment. There were many enlarged cells with a diameter same body to calculate relative radioactivity. Relative more than twice the normal cell diameter (Fig. 5A). Some radioactivity of the tumor exposed to shock waves was were binucleated and showed micronuclei (Fig. 5B), while 1.7-fold higher than that of the control (Fig. 2B). others displayed arrest in mitosis (Fig. 5A). Electron AB Fig. 2. (A) Autoradiography, utilizing Co-labeled BLM, measured with an imaging plate. (a) Control, (b) exposed to shock waves. Radioluminescence of the exposed tumor was higher than that of the control. (B) The level of radioactivity in the tumor was divided by that of the liver in the same body to calculate relative radioactivity. Relative radioactivity of the tumor exposed to shock waves was 1.7- fold higher than that of control. Relative radioactivity Jpn. J. Cancer Res. 91, October 2000 A B Fig. 3. (A) Positive rate of Ki-67 immunoreactivity in SW480 following the treatment. Time course of suppression of cell proliferation of control ( ), BLM alone ( ), SW alone ( ), and SW and BLM ( ) (mean ± SD). The percentage of Ki-67-positive cells reached the minimum (35.7%) at 24 h after the combined treatment. (B) Time profiles of immunohistochemistry for Ki-67 in SW480 following combined treatment. (a) Control, (b) 12 h, (c) 24 h, (d) 7 days. AB Fig. 4. (A) Expression of apoptotic cells on SW480 following the treatment. Time course of expression of TUNEL-positive cells in control ( ), BLM alone ( ), SW alone ( ), SW and BLM ( ) (mean ± SD). The apoptotic index reached the maximum (6.21%) at 6 h following the combined treatment. (B) TUNEL staining 6 h after treatment was compared in four groups: (a) control, (b) shock waves alone (SW alone), (c) BLM alone and (d) shock wave with BLM (SW + BLM). Immunohistochemical staining for apoptotic features in SW480 after the treatment is shown. (C) Apoptotic index values in the four groups 6 h after treatment: control, shock waves alone (SW alone), BLM alone, and shock waves with BLM (SW +BLM). The apoptotic index of the SW +BLM group was significantly higher (P < 0.05) than those of the other three groups. 1068 Shock Wave Chemotherapy on Solid Tumor AB Fig. 5. (A) Histopathological findings in SW480 tumors stained with HE. ×200. (a) Control. (b) 6 h after the combined shock waves and BLM treatment. Cells with an enlarged nucleus, with a diameter more than twice that of the control cells, were frequently observed. (B) Electron microscopy of SW480 tumor cells treated with shock waves and BLM. (a) Chromatin condensation forming granular masses along the nuclear membrane, usually associated with apoptosis (6 h after treatment, ×3500). (b) Cells are enlarged and polynucleated compared to untreated cells (6 h after treatment, × 3000). microscopy studies with SW480 cells 6 h following com- was reported that when several million molecules of BLM bined treatment confirmed these observations (Fig. 5B). are internalized, morphological changes, identical to those usually associated with apoptosis, are observed, as well as very rapid DNA fragmentation into oligonucleosomal- DISCUSSION 23) sized fragments. On the other hand, when only a few This study shows that anti-proliferative and pro-apo- thousand BLM molecules are internalized, cells display an ptotic effects of BLM combined with shock wave treatment arrest in the G -M phase of the cell cycle and become 23) are seen not only in vitro, but also in vivo in a solid tumor. enlarged and polynucleated before dying. These obser- Immunohistochemical staining, using MIB-1 antibody, vations correspond to mitotic death, generally a slow pro- revealed that the suppression of cancer cell proliferation cess that is dependent upon mitotic activity, during which began just after the treatment and the proliferation ratio cells will usually complete at least one mitosis prior to 24, 25) reached the minimum at 24 h after the treatment, almost their disintegration. Thus, the clusters of enlarged and equivalent to the doubling time. The maximal apoptotic polynucleated cells we observed 6 h following the com- index was detected 6 h after the combined treatment and at bined treatment may be the result of mitotic death. This the same time, clusters of enlarged cells, polynucleated is the first report, to our knowledge, of mitotic death cells and mitosis were also detected morphologically. It observed in vivo. 1069 Jpn. J. Cancer Res. 91, October 2000 BLM is a water-soluble antibiotic that was first isolated BLM for autoradiography to investigate BLM movement 26) by Umezawa et al., and exhibits cytotoxic activity because of the close resemblance in molecular weight and against mammalian cells. The cytotoxicity of BLM chemical structure to those of BLM and the high specific depends greatly on its ability to induce double-strand radioactivity of the chelate, as well as the very high stabil- 27) breaks in DNA. BLM cytotoxity is considerably potenti- ity of the Co-BLM coordination complex. In this study, ated in vitro when cultured cells are exposed to appropri- the accumulation of Co-BLM in the shock wave-treated 28 – 30) ate electric pulses. The antitumor effects of the tumor was 1.7-fold higher than that of control. This sug- compound are also highly increased in vivo by electric gests that insertion of BLM caused by shock waves 30 – 33) pulses delivered locally to the tumor site. The plasma occurred not only in vitro, but also in vivo. Our previous 29) membrane is known to limit BLM uptake and electro- study showed the anticancer effect on a cancer cell sus- 34) permeabilization is an efficient means of circumventing pension in vitro and the suppression of tumor growth in 15, 16) this barrier, thus allowing the direct internalization of vivo caused by shock wave chemotherapy, but histo- 29) BLM molecules into the cytoplasm. logical evaluation of the effects on solid tumors in vivo Although electrochemotherapy on human skin tumors was not done. There appear to be differences in the effect 35 – 37) has shown good results, direct application of electric of shock waves from the viewpoint of acoustics between current to cancerous tissue deep inside the human body cells suspended in a solution and cells tightly grouped in a can cause unacceptable side effects. Moreover, many diffi- solid tumor. In this study, we showed that shock wave che- culties remain before routine clinical use of electrochemo- motherapy suppresses cell proliferation and induces apo- therapy can be considered in human patients. On the other ptosis not only in vitro, but also in solid tumors in vivo. hand, focused high-energy shock waves were first applied Furthermore, some of the cell death appeared to be quite 38) to ureteral stones in humans in 1980. This is now a stan- similar to mitotic death. 39) dard procedure for ureteral stone treatment. Focused Several reports have shown that shock wave exposure 46, 47) shock waves have successfully introduced high energy of a solid tumor promotes necrosis. However, in this into deep portions of the human body without causing study, we could not evaluate whether the extent of necrosis damage to adjacent tissues. We have demonstrated that was affected by shock wave chemotherapy or not, because under-water shock waves can open the micropores on the the implanted SW480 tumor usually has central necrosis surface of suspended cells, thereby increasing the perme- of varying degree. 40) ability of the cell membrane, like electroporation. There- The response of cancer cells in vivo is affected by many fore, clinical application of the combination therapy, BLM factors, for example, the vascular system, immune system and shock waves, may be feasible. Our study suggests that and so on. This study deals with early events in the this combination therapy may be effective in adenocarci- expression of anticancer effects by shock wave chemother- nomas, which are normally refractory to BLM, and that apy. Further studies are planned to investigate the longer- this method should be effectively applicable to multidrug- term efficacy of this approach. resistant tumors expressing multidrug-resistance genes (MDRs) and/or multidrug-resistance-associated proteins ACKNOWLEDGMENTS (MRPs). In vivo gene transfection into solid tumors using 41, 42) shock waves has recently been reported. These studies The authors thank Dr. Kouwa Yamashita and Mr. Masato Suwa (Nihon Kayaku Co., Ltd.) for their excellent technical demonstrate that shock waves can insert reagents into the assistance in macroautoradiography, Mrs. Fumiko Date (Depart- cytoplasm, not only in vitro, but also in vivo. 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Journal
Japanese Journal of Cancer Research : Gann – Pubmed Central
Published: Oct 1, 2000