Skip to main content

Main menu

  • Home
  • Current Issue
  • Archive
  • Info for
    • Authors
    • Editorial Policies
    • Advertisers
    • Editorial Board
  • Other Publications
    • Anticancer Research
    • Cancer Genomics & Proteomics
    • Cancer Diagnosis & Prognosis
  • More
    • IIAR
    • Conferences
  • About Us
    • General Policy
    • Contact
  • Other Publications
    • In Vivo
    • Anticancer Research
    • Cancer Genomics & Proteomics

User menu

  • Register
  • Subscribe
  • My alerts
  • Log in
  • My Cart

Search

  • Advanced search
In Vivo
  • Other Publications
    • In Vivo
    • Anticancer Research
    • Cancer Genomics & Proteomics
  • Register
  • Subscribe
  • My alerts
  • Log in
  • My Cart
In Vivo

Advanced Search

  • Home
  • Current Issue
  • Archive
  • Info for
    • Authors
    • Editorial Policies
    • Advertisers
    • Editorial Board
  • Other Publications
    • Anticancer Research
    • Cancer Genomics & Proteomics
    • Cancer Diagnosis & Prognosis
  • More
    • IIAR
    • Conferences
  • About Us
    • General Policy
    • Contact
  • Visit iiar on Facebook
  • Follow us on Linkedin
Research ArticleExperimental Studies

A Non-invasive Imageable GFP-expressing Mouse Model of Orthotopic Human Bladder Cancer

YU SUN, HIROTO NISHINO, MING ZHAO, KENTARO MIYAKE, NORIHIKO SUGISAWA, JUN YAMAMOTO, YOSHIHIKO TASHIRO, SACHIKO INUBUSHI, KAZUYUKI HAMADA, GUANGWEI ZHU, HYEIN LIM and ROBERT M. HOFFMAN
In Vivo November 2020, 34 (6) 3225-3231; DOI: https://doi.org/10.21873/invivo.12158
YU SUN
1AntiCancer, Inc., San Diego, CA, U.S.A.
2Department of Surgery, University of California San Diego, San Diego, CA, U.S.A.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
HIROTO NISHINO
1AntiCancer, Inc., San Diego, CA, U.S.A.
2Department of Surgery, University of California San Diego, San Diego, CA, U.S.A.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
MING ZHAO
1AntiCancer, Inc., San Diego, CA, U.S.A.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
KENTARO MIYAKE
1AntiCancer, Inc., San Diego, CA, U.S.A.
2Department of Surgery, University of California San Diego, San Diego, CA, U.S.A.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
NORIHIKO SUGISAWA
1AntiCancer, Inc., San Diego, CA, U.S.A.
2Department of Surgery, University of California San Diego, San Diego, CA, U.S.A.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
JUN YAMAMOTO
1AntiCancer, Inc., San Diego, CA, U.S.A.
2Department of Surgery, University of California San Diego, San Diego, CA, U.S.A.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
YOSHIHIKO TASHIRO
1AntiCancer, Inc., San Diego, CA, U.S.A.
2Department of Surgery, University of California San Diego, San Diego, CA, U.S.A.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
SACHIKO INUBUSHI
1AntiCancer, Inc., San Diego, CA, U.S.A.
2Department of Surgery, University of California San Diego, San Diego, CA, U.S.A.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
KAZUYUKI HAMADA
1AntiCancer, Inc., San Diego, CA, U.S.A.
2Department of Surgery, University of California San Diego, San Diego, CA, U.S.A.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
GUANGWEI ZHU
1AntiCancer, Inc., San Diego, CA, U.S.A.
2Department of Surgery, University of California San Diego, San Diego, CA, U.S.A.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
HYEIN LIM
1AntiCancer, Inc., San Diego, CA, U.S.A.
2Department of Surgery, University of California San Diego, San Diego, CA, U.S.A.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
ROBERT M. HOFFMAN
1AntiCancer, Inc., San Diego, CA, U.S.A.
2Department of Surgery, University of California San Diego, San Diego, CA, U.S.A.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: all@anticancer.com
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

Abstract

Background/Aim: A more realistic mouse model of bladder cancer is necessary to develop effective drugs for the disease. Tumor models enhanced by bright fluorescent-reporter genes to follow the disease in real-time would enhance the ability to accurately predict the efficacy of various therapeutics on this particularly-malignant human cancer. Materials and Methods: A highly-fluorescent green fluorescent protein (GFP)-expressing bladder cancer model was orthotopically established in nude mice using the UM-UC-3 human bladder-cancer cell line (UM-UC-3-GFP). Fragments from a subcutaneous tumor of UM-UC-3-GFP were surgically implanted into the nude mouse bladder. Non-invasive and intra-vital fluorescence imaging was obtained with a simple imaging box. Results: The GFP-expressing orthotopic bladder tumor was imaged in real-time non-invasively as well as intra-vitally, with the two methods correlating at r=0.99. Conclusion: This is the first non-invasive-fluorescence-imaging orthotopic model of bladder cancer and can be used for rapidly screening novel effective agents for this recalcitrant disease.

  • Bladder cancer
  • nude mice
  • orthotopic
  • GFP
  • imaging
  • non-invasive

Transitional-epithelium-derived bladder cancer is a recalcitrant disease. Our laboratory has developed an intact-tissue method of orthotopic implantation of human tumors in nude mice termed surgical orthotopic implantation (SOI) (1). We developed an SOI mouse model of bladder cancer thirty years ago, which was the first to show metastases (2-4). Orthotopic models are more accurate cancer models than subcutaneous xenografts, which typically do not metastasize (5) and may respond differently to chemotherapeutic agents than in situ human disease (6). By accurately modeling human disease, orthotopic xenograft models may be used to develop and test various therapeutics and predict their activity on human cancer. For an orthotopic model to fully express its malignant potential, SOI of intact tissue is necessary, as opposed to orthotopic injection of cells (2, 7, 8).

Our laboratory pioneered the in vivo use of the green fluorescent protein (GFP) to establish orthotopic fluorescent human cancer xenografts (9-15). In these models, the GFP gene is stably transduced into human cancer cell lines, which subsequently express GFP at high levels in vitro and in vivo, including primary and metastatic tumors. We have used this technology to engineer fluorescent orthotopic models of pancreatic cancer (9-11), as well as lung cancer (12), prostate cancer (13), colon cancer (16), sarcoma (17), stomach cancer (18), melanoma (19), glioma (20), nasopharyngeal cancer (21), liver metastases (22), head and neck cancer (23) and breast cancer (24). We also developed an orthotopic model of GFP-expressing bladder cancer that could be imaged intra-vitally (15).

Recently, Naito et al. reported a cell-injection orthotopic model of UM-UC-3 bladder cancer (25). Huebner et al. have developed a luciferase-expressing cell-injection orthotopic model of UM-UC-3 bladder cancer (26). However, luciferase produces a weak signal that cannot be imaged and relies on expensive and cumbersome photon counting (27, 28). In the present study, we developed a new GFP-expressing SOI model of human bladder cancer using UM-UC-3-GFP that could be imaged non-invasively, without anesthesia, with a simple foot-pedal-controlled light box, as well as intra-vitally imaged.

Materials and Methods

Mice. Female nude nu/nu mice 6-8 weeks (AntiCancer, Inc., San Diego, CA, USA) were used. An inspection was performed to ensure their suitability for the study before cancer-cell implantation. The animals were maintained in a HEPA-filtered environment in a Micro-VENT full-ventilation rodent housing system (Allentown Caging Equipment Co., Allentown, NJ, USA) at AntiCancer, Inc. Animal-room controls were set to maintain temperature and relative humidity at 22°C±2°C and 55%±15%, respectively. The rooms were lit by artificial light for 12 h each day. Cages and bedding were autoclaved. Water was purified by Milli-Q Biocel System (Millipore, Billerica, MA, USA), autoclaved and supplied ad libitum to each cage via water bottles. Autoclavable rodent diet 5010 was obtained from PMI Nutrition International Inc. (Brentwood, MO, USA). All animals were weighed using an electronic balance (Spectrum; APX-203, Gardena, CA, USA) and given a clinical examination to ensure that they were in good condition. All animal studies were conducted with an AntiCancer Institutional Animal Care and Use Committee (IACUC)-protocol approved for this study and in accordance with the principles and procedures outlined in the National Institutes of Health Guide for the Care and Use of Animals under Assurance Number A3873-1 (29).

Figure 1.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 1.

Comparison of non-invasive and invasive (intra-vital) imaging of the orthotopic bladder tumor.

Cell line. UM-UC-3-GFP cells (AntiCancer Inc.) were cultured in Dulbecco's modified Eagle's medium supplemented with 1% penicillin and streptomycin (Invitrogen) and 10% fetal bovine serum (Sigma-Aldrich). The cells were incubated at 37°C in a humidified atmosphere of 5% CO2 in air.

Figure 2.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 2.

Orthotopic bladder-cancer growth curves comparing non-invasive and intra-vital imaging. (A) Tumor growth monitored by fluorescent area; (B) Tumor growth monitored by volume.

Orthotopic mouse model. UM-UC-3-GFP cells (5×106) in 100 μl PBS were initially subcutaneously injected on both flanks in nude mice. After subcutaneous tumor growth, the tumors were excised and divided into small fragments and 5 mice were implanted orthotopically with one 2 mm3 fragment of tumor on the bladder using SOI in each mouse.

The establishment of a bladder cancer orthotopic model was as follows: A 5 mm incision was made on the lower-abdominal area and the bladder was exposed from the intra-abdominal space. Then, a 2 mm3 tumor fragment was implanted on the dome of the bladder using 7-0 surgical sutures. The bladder was returned to the intra-abdominal space and the incision was closed in one layer using 6-0 surgical sutures.

Fluorescence imaging. Tumor size, using both non-invasive and intra-vital imaging, was measured using the real-time fluorescence imaging FluorVivo system and its software (INDEC Systems, Santa Clara, CA, USA). Non-invasive imaging was recorded through the intact skin. Invasive intra-vital imaging was recorded during laparotomy. Non-invasive imaging and intra-vital imaging were evaluated on days 7, 14, 21 and 28 after implantation. All the mice were euthanized on day 28. At autopsy, the abdominal cavity was opened to image the primary tumor and metastasis.

Tumor-size and body-weight measurement. Tumor size was measured once a week using the FluorVivo. Body weight was recorded using an electronic scale. The approximate tumor volume was calculated by measuring the perpendicular minor dimension (W) and major dimension (L). Approximate tumor volume (mm3) was calculated with the formula (W × W × L) × 1/2. Fluorescence area was measured using ImageJ 1.52a software (National Institutes of Health).

Statistical analysis. Correlation was measured using the Pearson product-moment correlation coefficient: p≤0.05 was considered statistically significant.

Results

Tumor growth monitoring. Tumor progression was visualized both by non-invasive and intra-vital imaging (Figure 1).

Over 28 days, the mean fluorescence area increased from 20.5 mm2 to 112.1 mm2 in the non-invasive images and from 25.2 mm2 to 119.4 mm2 in the intra-vital images (Figure 2A).

Over 28 days, the mean tumor volume increased from 62.3 mm3 to 781.6 mm3 in the non-invasive images and from 87.4 mm3 to 862.0 mm3 in the intra-vital images (Figure 2B).

Metastasis incidence. All the mice were sacrificed at the end of the study on day 28. Three of 5 mice had metastasis, as examined by necropsy. Among the 3 mice which had metastasis, 3 mice had mesenteric lymph-node metastasis, 2 mice had lumber lymph-node metastasis, testicular metastasis and pancreatic metastasis and 1 mouse had liver metastasis (Figure 3).

Correlation of non-invasive and intra-vital imaging. There was a positive correlation between non-invasive and invasive imaging for both tumor volume (R=0.9949, p<0.0001) and fluorescent area (R=0.9971, p<0.0001) (Figure 4).

There was a positive correlation between tumor volume and fluorescent area for both non-invasive imaging (R=0.9951, p<0.0001) and intra-vital imaging (R=0.9939, p<0.0001) (Figure 5).

Figure 3.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 3.

Representative images of metastasis at autopsy. Yellow arrows: liver metastasis; Orange arrow: pancreatic metastasis; Red arrow: lumbar lymph-node metastasis; Blue arrows: testicular metastasis; White arrows: mesenteric lymph-node metastasis.

Figure 4.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 4.

Correlation of tumor size between non-invasive and intra-vital imaging. (A) Comparison of non-invasive and intra-vital tumor volume. R=0.9949, p<0.0001; (B) Comparison of non-invasive and intra-vital fluorescent area. R=0.9971, p<0.0001.

Body weight monitoring. The mean body weight decreased gradually during the experimental period due to cachexia because of the orthotopic bladder cancer and metastasis. The body-weight ratio is shown in Figure 6. The final body-weight ratio (day 28/day 1) was 0.89±0.21.

Discussion

To the best of our knowledge, this study is the first to report a non-invasive fluorescence-imaging orthotopic bladder-cancer mouse model.

We were the first to report that tumor fluorescence enables real-time, sequential whole-body imaging and quantification of tumor burden without the need for anesthesia, laparotomy, contrast agents, or invasive procedures using fluorescent proteins (14, 27). The visualized area of fluorescence emitted by the internally-implanted tumors correlated significantly with tumor volume, as calculated using standard measurements obtained at autopsy (30). Tumor weight also correlated with tumor fluorescence (31).

The cellular orthotopic methods of bladder cancer described by Huebner et al. (26) and Naito et al. (25) where cancer cells were installed in the bladder whose inner surface was previously modified, resulted in inconsistent models. The present report describes a much simpler and reproducible model of suturing tumor fragments on the bladder. A luciferase-expressing orthotopic bladder-cancer model was previously reported by Huebner et al. (26). However, luciferase expression is too weak for imaging and only allows photon counting, which requires expensive and cumbersome equipment (27).

Figure 5.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 5.

Correlation of tumor volume and fluorescent area. (A) Comparison of tumor volume and fluorescent area in non-invasive images. R=0.9949, p<0.0001; (B). Comparison of tumor volume and fluorescent area in intra-vital images. R=0.9939, p<0.0001.

Our improved GFP-expressing orthotopic bladder cancer mouse model can be used to elucidate the therapeutic mechanisms of existing agents and to develop novel therapeutics for recurrent bladder cancer. Non-invasive imaging, using very simple equipment, will allow rapid screening to identify effective new agents.

Figure 6.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 6.

Time course of body-weight ratio. A stable body weight was observed in the first three weeks after tumor implantation, and a decrease in body weight in the last week was due to cachexia.

Footnotes

  • Authors' Contributions

    YS designed the study; YS, HN, KM, NS, JY, YT, SI, KH, HL performed the experiments; YS, GZ analyzed the data; YS, HN drafted the manuscript; MZ, RMH revised the manuscript; RMH supervised the study.

  • This article is freely accessible online.

  • Conflicts of Interest

    None of the Authors declare any conflicts of interest related to this study. AntiCancer Inc. offers orthotopic mouse models of cancer for contract research.

  • Received August 2, 2020.
  • Revision received August 24, 2020.
  • Accepted August 25, 2020.
  • Copyright© 2020, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved

References

  1. ↵
    1. Fu XY,
    2. Besterman JM,
    3. Monosov A,
    4. Hoffman RM
    : Models of human metastatic colon cancer in nude mice orthotopically constructed by using histologically intact patient specimens. Proc Natl Acad Sci USA 88(20): 9345-9349, 1991. PMID: 1924398. DOI: 10.1073/pnas.88.20.9345
    OpenUrlAbstract/FREE Full Text
  2. ↵
    1. Fu XY,
    2. Theodorescu D,
    3. Kerbel RS,
    4. Hoffman RM
    : Extensive multi-organ metastasis following orthotopic onplantation of histologically-intact human bladder carcinoma tissue in nude mice. Int J Cancer 49(6): 938-939, 1991. PMID: 1959996. DOI: 10.1002/ijc.2910490623
    OpenUrlPubMed
    1. Fu X,
    2. Hoffman RM
    : Human RT-4 bladder carcinoma is highly metastatic in nude mice and comparable to RAS-H-transformed RT-4 when orthotopically onplanted as histologically intact tissue. Int J Cancer 51(6): 989-991, 1992. PMID: 1639544. DOI: 10.1002/ijc.2910510625
    OpenUrlCrossRefPubMed
  3. ↵
    1. Chang SG,
    2. Kim JI,
    3. Jung JC,
    4. Rho YS,
    5. Lee KT,
    6. An Z,
    7. Wang X,
    8. Hoffman RM
    : Antimetastatic activity of the new platinum analog [Pt(cis-dach) (DPPE).2NO3] in a metastatic model of human bladder cancer. Anticancer Res 17(5A): 3239-3242, 1997. PMID: 9413154.
    OpenUrlPubMed
  4. ↵
    1. Kyriazis AP,
    2. DiPersio L,
    3. Michael GJ,
    4. Pesce AJ,
    5. Stinnett JD
    : Growth patterns and metastatic behavior of human tumors growing in athymic mice. Cancer Res 38(10): 3186-3190, 1978. PMID: 688209.
    OpenUrlAbstract/FREE Full Text
  5. ↵
    1. Kuo TH,
    2. Kubota T,
    3. Watanabe M,
    4. Furukawa T,
    5. Kase S,
    6. Tanino H,
    7. Saikawa Y,
    8. Ishibiki K,
    9. Kitajima M,
    10. Hoffman RM
    : Site-specific chemosensitivity of human small-cell lung carcinoma growing orthotopically compared to subcutaneously in scid mice: The importance of orthotopic models to obtain relevant drug evaluation data. Anticancer Res 13(3): 627-630, 1993. PMID: 8391244.
    OpenUrlPubMed
  6. ↵
    1. Furukawa T,
    2. Fu X,
    3. Kubota T,
    4. Watanabe M,
    5. Kitajima M,
    6. Hoffman RM
    : Nude mouse metastatic models of human stomach cancer constructed using orthotopic implantation of histologically intact tissue. Cancer Res 53(5): 1204-1208, 1993. PMID: 8439965.
    OpenUrlAbstract/FREE Full Text
  7. ↵
    1. An Z,
    2. Jiang P,
    3. Wang X,
    4. Moossa AR,
    5. Hoffman RM
    : Development of a high metastatic orthotopic model of human renal cell carcinoma in nude mice: Benefits of fragment implantation compared to cell-suspension injection. Clin Exp Metastasis 17(3): 265-270, 1999. PMID: 10432012. DOI: 10.1023/a:1006654600095
    OpenUrlCrossRefPubMed
  8. ↵
    1. Bouvet M,
    2. Wang J,
    3. Nardin SR,
    4. Nassirpour R,
    5. Yang M,
    6. Baranov E,
    7. Jiang P,
    8. Moossa AR,
    9. Hoffman RM
    : Real-time optical imaging of primary tumor growth and multiple metastatic events in a pancreatic cancer orthotopic model. Cancer Res 62(5): 1534-1540, 2002. PMID: 11888932.
    OpenUrlAbstract/FREE Full Text
    1. Bouvet M,
    2. Yang M,
    3. Nardin S,
    4. Wang X,
    5. Jiang P,
    6. Baranov E,
    7. Moossa AR,
    8. Hoffman RM
    : Chronologically-specific metastatic targeting of human pancreatic tumors in orthotopic models. Clin Exp Metastasis 18(3): 213-218, 2000. PMID: 11315094. DOI: 10.1023/a:1006767405609
    OpenUrlCrossRefPubMed
  9. ↵
    1. Sun FX,
    2. Tohgo A,
    3. Bouvet M,
    4. Yagi S,
    5. Nassirpour R,
    6. Moossa AR,
    7. Hoffman RM
    : Efficacy of camptothecin analog DX-8951f (exatecan mesylate) on human pancreatic cancer in an orthotopic metastatic model. Cancer Res 63(1): 80-85, 2003. PMID: 12517781.
    OpenUrlAbstract/FREE Full Text
  10. ↵
    1. Rashidi B,
    2. Yang M,
    3. Jiang P,
    4. Baranov E,
    5. An Z,
    6. Wang X,
    7. Moossa AR,
    8. Hoffman RM
    : A highly metastatic lewis lung carcinoma orthotopic green fluorescent protein model. Clin Exp Metastasis 18(1): 57-60, 2000. PMID: 11206839. DOI: 10.1023/a:10265 96131504
    OpenUrlCrossRefPubMed
  11. ↵
    1. Yang M,
    2. Jiang P,
    3. Sun FX,
    4. Hasegawa S,
    5. Baranov E,
    6. Chishima T,
    7. Shimada H,
    8. Moossa AR,
    9. Hoffman RM
    : A fluorescent orthotopic bone metastasis model of human prostate cancer. Cancer Res 59(4): 781-786, 1999. PMID: 10029062.
    OpenUrlAbstract/FREE Full Text
  12. ↵
    1. Yang M,
    2. Baranov E,
    3. Jiang P,
    4. Sun FX,
    5. Li XM,
    6. Li L,
    7. Hasegawa S,
    8. Bouvet M,
    9. Al-Tuwaijri M,
    10. Chishima T,
    11. Shimada H,
    12. Moossa AR,
    13. Penman and,
    14. Hoffman RM
    : Whole-body optical imaging of green fluorescent protein-expressing tumors and metastases. Proc Natl Acad Sci U S A 97(3): 1206-1211, 2000. PMID: 10655509. DOI: 10.1073/pnas.97.3.1206
    OpenUrlAbstract/FREE Full Text
  13. ↵
    1. Zhou JH,
    2. Rosser CJ,
    3. Tanaka M,
    4. Yang M,
    5. Baranov E,
    6. Hoffman RM,
    7. Benedict WF
    : Visualizing superficial human bladder cancer cell growth in vivo by green fluorescent protein expression. Cancer Gene Ther 9(8): 681-686, 2002. PMID: 12136429. DOI: 10.1038/sj.cgt.7700489
    OpenUrlCrossRefPubMed
  14. ↵
    1. Fu X,
    2. Herrera H,
    3. Kubota T,
    4. Hoffman RM
    : Extensive liver metastasis from human colon cancer in nude and scid mice after orthotopic onplantation of histologically-intact human colon carcinoma tissue. Anticancer Res 12(5): 1395-1397, 1992. PMID: 1444196.
    OpenUrlPubMed
  15. ↵
    1. Kiyuna T,
    2. Murakami T,
    3. Tome Y,
    4. Kawaguchi K,
    5. Igarashi K,
    6. Zhang Y,
    7. Zhao M,
    8. Li Y,
    9. Bouvet M,
    10. Kanaya F,
    11. Singh A,
    12. Dry S,
    13. Eilber FC,
    14. Hoffman RM
    : High efficacy of tumor-targeting Salmonella typhimurium A1-R on a doxorubicin- and dactolisib-resistant follicular dendritic-cell sarcoma in a patient-derived orthotopic xenograft PDOX nude mouse model. Oncotarget 7(22): 33046-33054, 2016. PMID: 27105519. DOI: 10.18632/oncotarget.8848
    OpenUrl
  16. ↵
    1. Yano S,
    2. Zhang Y,
    3. Miwa S,
    4. Tome Y,
    5. Hiroshima Y,
    6. Uehara F,
    7. Yamamoto M,
    8. Suetsugu A,
    9. Kishimoto H,
    10. Tazawa H,
    11. Zhao M,
    12. Bouvet M,
    13. Fujiwara T,
    14. Hoffman RM
    : Spatial-temporal FUCCI imaging of each cell in a tumor demonstrates locational dependence of cell cycle dynamics and chemoresponsiveness. Cell Cycle 13(13): 2110-2119, 2014. PMID: 24811200. DOI: 10.4161/cc.29156
    OpenUrlCrossRefPubMed
  17. ↵
    1. Yamamoto M,
    2. Zhao M,
    3. Hiroshima Y,
    4. Zhang Y,
    5. Shurell E,
    6. Eilber FC,
    7. Bouvet M,
    8. Noda M,
    9. Hoffman RM
    : Efficacy of tumor-targeting Salmonella A1-R on a melanoma patient-derived orthotopic xenograft (PDOX) nude-mouse model. PLoS One 11(8): e0160882, 2016. PMID: 27500926. DOI: 10.1371/journal.pone.0160882
    OpenUrl
  18. ↵
    1. Momiyama M,
    2. Hiroshima Y,
    3. Suetsugu A,
    4. Tome Y,
    5. Mii S,
    6. Yano S,
    7. Bouvet M,
    8. Chishima T,
    9. Endo I,
    10. Hoffman RM
    : Enhanced resection of orthotopic red-fluorescent-protein-expressing human glioma by fluorescence-guided surgery in nude mice. Anticancer Res 33(1): 107-111, 2013. PMID: 23267134.
    OpenUrlAbstract/FREE Full Text
  19. ↵
    1. Liu T,
    2. Ding Y,
    3. Xie W,
    4. Li Z,
    5. Bai X,
    6. Li X,
    7. Fang W,
    8. Ren C,
    9. Wang S,
    10. Hoffman RM,
    11. Yao K
    : An imageable metastatic treatment model of nasopharyngeal carcinoma. Clin Cancer Res 13(13): 3960-3967, 2007. PMID: 17606730. DOI: 10.1158/1078-0432.CCR-07-0089
    OpenUrlAbstract/FREE Full Text
  20. ↵
    1. Murakami T,
    2. Hiroshima Y,
    3. Zhao M,
    4. Zhang Y,
    5. Chishima T,
    6. Tanaka K,
    7. Bouvet M,
    8. Endo I,
    9. Hoffman RM
    : Therapeutic efficacy of tumor-targeting Salmonella typhimurium A1-R on human colorectal cancer liver metastasis in orthotopic nude-mouse models. Oncotarget 6(31): 31368-31377, 2015. PMID: 26375054. DOI: 10.18632/oncotarget.5187
    OpenUrl
  21. ↵
    1. Lee SE,
    2. Bairstow SF,
    3. Werling JO,
    4. Chaubal MV,
    5. Lin L,
    6. Murphy MA,
    7. DiOrio JP,
    8. Gass J,
    9. Rabinow B,
    10. Wang X,
    11. Zhang Y,
    12. Yang Z,
    13. Hoffman RM
    : Paclitaxel nanosuspensions for targeted chemotherapy - nanosuspension preparation, characterization, and use. Pharm Dev Technol 19(4): 438-453, 2014. PMID: 23617261. DOI: 10.3109/10837450.2013.789911
    OpenUrl
  22. ↵
    1. Yano S,
    2. Takehara K,
    3. Miwa S,
    4. Kishimoto H,
    5. Tazawa H,
    6. Urata Y,
    7. Kagawa S,
    8. Bouvet M,
    9. Fujiwara T,
    10. Hoffman RM
    : Fluorescence-guided surgery of a highly-metastatic variant of human triple-negative breast cancer targeted with a cancer-specific GFP adenovirus prevents recurrence. Oncotarget 7(46): 75635-75647, 2016. PMID: 27689331. DOI: 10.18632/oncotarget.12314
    OpenUrl
  23. ↵
    1. Naito T,
    2. Higuchi T,
    3. Shimada Y,
    4. Kakinuma C
    : An improved mouse orthotopic bladder cancer model exhibiting progression and treatment response characteristics of human recurrent bladder cancer. Oncol Lett 19(1): 833-839, 2020. PMID: 31885717. DOI: 10.3892/ol.2019.11172
    OpenUrl
  24. ↵
    1. Huebner D,
    2. Rieger C,
    3. Bergmann R,
    4. Ullrich M,
    5. Meister S,
    6. Toma M,
    7. Wiedemuth R,
    8. Temme A,
    9. Novotny V,
    10. Wirth MP,
    11. Bachmann M,
    12. Pietzsch J,
    13. Fuessel S
    : An orthotopic xenograft model for high-risk non-muscle invasive bladder cancer in mice: Influence of mouse strain, tumor cell count, dwell time and bladder pretreatment. BMC Cancer 17(1): 790, 2017. PMID: 29169339. DOI: 10.1186/s12885-017-3778-3
    OpenUrl
  25. ↵
    1. Hoffman RM
    : The multiple uses of fluorescent proteins to visualize cancer in vivo. Nat Rev Cancer 5(10): 796-806, 2005. PMID: 16195751. DOI: 10.1038/nrc1717
    OpenUrlCrossRefPubMed
  26. ↵
    1. Hoffman RM,
    2. Yang M
    : Subcellular imaging in the live mouse. Nat Protoc 1(2): 775-782, 2006. PMID: 17406307. DOI: 10.1038/nprot.2006.109
    OpenUrlCrossRefPubMed
  27. ↵
    1. Yang M,
    2. Reynoso J,
    3. Bouvet M,
    4. Hoffman RM
    : A transgenic red fluorescent protein-expressing nude mouse for color-coded imaging of the tumor microenvironment. J Cell Biochem 106(2): 279-284, 2009. PMID: 19097136. DOI: 10.1002/jcb.21999
    OpenUrlCrossRefPubMed
  28. ↵
    1. Katz MH,
    2. Takimoto S,
    3. Spivack D,
    4. Moossa AR,
    5. Hoffman RM,
    6. Bouvet M
    : A novel red fluorescent protein orthotopic pancreatic cancer model for the preclinical evaluation of chemotherapeutics. J Surg Res 113(1): 151-160, 2003. PMID: 12943825. DOI: 10.1016/s0022-4804(03)00234-8
    OpenUrlCrossRefPubMed
  29. ↵
    1. Hiroshima Y,
    2. Zhao M,
    3. Maawy A,
    4. Zhang Y,
    5. Katz MH,
    6. Fleming JB,
    7. Uehara F,
    8. Miwa S,
    9. Yano S,
    10. Momiyama M,
    11. Suetsugu A,
    12. Chishima T,
    13. Tanaka K,
    14. Bouvet M,
    15. Endo I,
    16. Hoffman RM
    : Efficacy of Salmonella typhimurium A1-R versus chemotherapy on a pancreatic cancer patient-derived orthotopic xenograft (PDOX). J Cell Biochem 115(7): 1254-1261, 2014. PMID: 24435915. DOI: 10.1002/jcb.24769
    OpenUrlPubMed
PreviousNext
Back to top

In this issue

In Vivo
Vol. 34, Issue 6
November-December 2020
  • Table of Contents
  • Table of Contents (PDF)
  • Index by author
  • Back Matter (PDF)
  • Ed Board (PDF)
  • Front Matter (PDF)
Print
Download PDF
Article Alerts
Sign In to Email Alerts with your Email Address
Email Article

Thank you for your interest in spreading the word on In Vivo.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
A Non-invasive Imageable GFP-expressing Mouse Model of Orthotopic Human Bladder Cancer
(Your Name) has sent you a message from In Vivo
(Your Name) thought you would like to see the In Vivo web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
10 + 6 =
Solve this simple math problem and enter the result. E.g. for 1+3, enter 4.
Citation Tools
A Non-invasive Imageable GFP-expressing Mouse Model of Orthotopic Human Bladder Cancer
YU SUN, HIROTO NISHINO, MING ZHAO, KENTARO MIYAKE, NORIHIKO SUGISAWA, JUN YAMAMOTO, YOSHIHIKO TASHIRO, SACHIKO INUBUSHI, KAZUYUKI HAMADA, GUANGWEI ZHU, HYEIN LIM, ROBERT M. HOFFMAN
In Vivo Nov 2020, 34 (6) 3225-3231; DOI: 10.21873/invivo.12158

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Reprints and Permissions
Share
A Non-invasive Imageable GFP-expressing Mouse Model of Orthotopic Human Bladder Cancer
YU SUN, HIROTO NISHINO, MING ZHAO, KENTARO MIYAKE, NORIHIKO SUGISAWA, JUN YAMAMOTO, YOSHIHIKO TASHIRO, SACHIKO INUBUSHI, KAZUYUKI HAMADA, GUANGWEI ZHU, HYEIN LIM, ROBERT M. HOFFMAN
In Vivo Nov 2020, 34 (6) 3225-3231; DOI: 10.21873/invivo.12158
Reddit logo Twitter logo Facebook logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Google Plus One

Jump to section

  • Article
    • Abstract
    • Materials and Methods
    • Results
    • Discussion
    • Footnotes
    • References
  • Figures & Data
  • Info & Metrics
  • PDF

Related Articles

  • No related articles found.
  • PubMed
  • Google Scholar

Cited By...

  • No citing articles found.
  • Google Scholar

More in this TOC Section

  • Evaluation of the Relationship Between miRNA-22-3p and Gal-9 Levels in Glioblastoma
  • Metformin Inhibits the Estrogen-mediated Epithelial-Mesenchymal Transition of Ectopic Endometrial Stromal Cells in Endometriosis
  • MCC950 Ameliorates Acute Exogenous Lipoid Pneumonia Induced by Sewing Machine Oil in Rats via the NF-κB/NLRP3 Inflammasome Pathway
Show more Experimental Studies

Similar Articles

Keywords

  • bladder cancer
  • nude mice
  • orthotopic
  • GFP
  • imaging
  • non-invasive
In Vivo

© 2023 In Vivo

Powered by HighWire