Annals of Coloproctology

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Association Between c-Met and Lymphangiogenic Factors in Patients With Colorectal Cancer: Han Jo Kim, Moo-Jun Baek, Dong Hyun Kang, Sang-Cheol Lee, Sang Byung Bae, Kyu Taek Lee, Namsu Lee, Hyungjoo Kim, Dongjun Jeong, Tae Sung Ahn, Moon Soo Lee, Dae Sik Hong, Jong-Ho Won; Ann Coloproctol. 2018;34(2):88-93. Published online April 30, 2018; DOI: https://doi.org/10.3393/ac.2017.10.10

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Purpose
Animal models show a strong relationship between lymphangiogenesis and lymph node metastasis. However, the clinical significance of lymphangiogenesis in patients with colorectal cancer (CRC) remains uncertain. This study aimed to evaluate the association between c-Met and lymphangiogenic factors and to elucidate the prognostic significance of c-Met in patients with CRC.
Methods
A total of 379 tissue samples were obtained from surgically resected specimens from patients with CRC at Soonchunhyang University Cheonan Hospital between January 2002 and December 2010. The expressions of c-Met, vascular endothelial growth factor (VEGF)-C, VEGF-D, VEGF receptor (VEGFR)-3, and podoplanin were examined using immunohistochemistry. The expression of c-Met and clinical factors were analyzed.
Results
Of the 379 tissues, 301 (79.4%) had c-Met expression. High expression of c-Met in tumor cells was significantly associated with high expression of VEGF-C (P < 0.001) and VEGFR-3 (P = 0.001). However, no statistically significant association with podoplanin (P = 0.587) or VEGF-D (P = 0.096) was found. Of the 103 evaluable patients, expression of c-Met in tumor cells was significantly associated with advanced clinical stage (P = 0.020), positive lymph node status (P = 0.038), and high expression of VEGF-C (P = 0.020). However, no statistically significant association with podoplanin (P = 0.518), VEGFR-3 (P = 0.085), VEGF-D (P = 0.203), or overall survival (P = 0.360) was found.
Conclusion
Our results provide indirect evidence for an association and possible regulatory link of c-Met with the lymphangiogenic markers, but c-Met expression in patients with CRC is not a prognostic indicator for overall survival.

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Expression Profile of Microenvironmental Factors in the Interface Zone of Colorectal Cancer: Histological-Stromal Biomarkers and Cancer Cell-Cancer-Associated Fibroblast-Related Proteins Combined for the Assessment of Tumor Progression
Ricella Souza da Silva, Eduardo M. Queiroga, Cynthia de Toledo Osório, Karin S. Cunha, Fabiana P. Neves, Julieth P. Andrade, Eliane P. Dias
Pathobiology.2024; 91(2): 99. CrossRef
Recent progress in the imaging of c‐Met aberrant cancers with positron emission tomography
Giuseppe Floresta, Vincenzo Abbate
Medicinal Research Reviews.2022; 42(4): 1588. CrossRef
Involvement of Met receptor pathway in aggressive behavior of colorectal cancer cells induced by parathyroid hormone-related peptide
María Belén Novoa Díaz, Pedro Carriere, Graciela Gigola, Ariel Osvaldo Zwenger, Natalia Calvo, Claudia Gentili
World Journal of Gastroenterology.2022; 28(26): 3177. CrossRef
The potential therapeutic and prognostic impacts of the c‐MET/HGF signaling pathway in colorectal cancer
Seyed Mostafa Parizadeh, Reza Jafarzadeh‐Esfehani, Danial Fazilat‐Panah, Seyed Mahdi Hassanian, Soodabeh Shahidsales, Majid Khazaei, Seyed Mohammad Reza Parizadeh, Majid Ghayour‐Mobarhan, Gordon A. Ferns, Amir Avan
IUBMB Life.2019; 71(7): 802. CrossRef

Adipose-tissue-derived Stem Cells Enhance the Healing of Ischemic Colonic Anastomoses: An Experimental Study in Rats: Jong Han Yoo, Jae Ho Shin, Min Sung An, Tae Kwun Ha, Kwang Hee Kim, Ki Beom Bae, Tae Hyeon Kim, Chang Soo Choi, Kwan Hee Hong, Jeong Kim, Soo Jin Jung, Sun Hee Kim, Kuk Hwan Rho, Jong Tae Kim, Young Il Yang; J Korean Soc Coloproctol. 2012;28(3):132-139. Published online June 30, 2012; DOI: https://doi.org/10.3393/jksc.2012.28.3.132

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Abstract PDF

Purpose

This experimental study verified the effect of adipose-tissue-derived stem cells (ASCs) on the healing of ischemic colonic anastomoses in rats.

Methods

ASCs were isolated from the subcutaneous fat tissue of rats and identified as mesenchymal stem cells by identification of different potentials. An animal model of colonic ischemic anastomosis was induced by modifying Nagahata's method. Sixty male Sprague-Dawley rats (10-week-old, 370 ± 50 g) were divided into two groups (n = 30 each): a control group in which the anastomosis was sutured in a single layer with 6-0 polypropylene without any treatment and an ASCtreated group (ASC group) in which the anastomosis was sutured as in the control group, but then ASCs were locally transplanted into the bowel wall around the anastomosis. The rats were sacrificed on postoperative day 7. Healing of the anastomoses was assessed by measuring loss of body weight, wound infection, anastomotic leakage, mortality, adhesion formation, ileus, anastomotic stricture, anastomotic bursting pressure, histopathological features, and microvascular density.

Results

No differences in wound infection, anastomotic leakage, or mortality between the two groups were observed. The ASC group had significantly more favorable anastomotic healing, including less body weight lost, less ileus, and fewer ulcers and strictures, than the control group. ASCs augmented bursting pressure and collagen deposition. The histopathological features were significantly more favorable in the ASC group, and microvascular density was significantly higher than it was in the control group.

Conclusion

Locally-transplanted ASCs enhanced healing of ischemic colonic anastomoses by increasing angiogenesis. ASCs could be a novel strategy for accelerating healing of colonic ischemic risk anastomoses.

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Effects of Local and Systematic Administration of Adipose Tissue–Derived Stem Cells to Intestinal Anastomosis in Intestinal Ishemic Rerfusion Injury: Ani̇mal Experi̇ment Model
İbrahim Doğan, Bahar Kartal, Bülent Cavit Yüksel, Umut Fırat Turan, Metin Bozkaya, Gökçe Yağmur Summak, Ömür Besbinar, Açelya Yilmazer, Sadettin Er
Journal of Surgical Research.2026; 318: 290. CrossRef
Experimental models of high-risk bowel anastomosis in rats: A systematic review
Georgios Ntampakis, Manousos-Georgios Pramateftakis, Elissavet Anestiadou, Stefanos Bitsianis, Orestis Ioannidis, Chryssa Bekiari, George Koliakos, Maria Karakota, Anastasia Tsakona, Angeliki Cheva, Stamatios Angelopoulos
World Journal of Experimental Medicine.2024;[Epub] CrossRef
The Role of Adipose Tissue Mesenchymal Stem Cells in Colonic Anastomosis Healing in Inflammatory Bowel Disease: Experimental Study in Rats
Georgios Ntampakis, Manousos-Georgios Pramateftakis, Orestis Ioannidis, Stefanos Bitsianis, Panagiotis Christidis, Savvas Symeonidis, Georgios Koliakos, Maria Karakota, Chrysanthi Bekiari, Anastasia Tsakona, Angeliki Cheva, Stamatios Aggelopoulos
Journal of Clinical Medicine.2023; 12(19): 6336. CrossRef
The application of regenerative medicine in colorectal surgery
Ilan Kent, Michael R. Freund, Samir Agarwal, Steven D. Wexner
Surgery.2022; 171(4): 867. CrossRef
Stem cell therapy applied for digestive anastomosis: Current state and future perspectives
Jacobo Trébol, Tihomir Georgiev-Hristov, Isabel Pascual-Miguelañez, Hector Guadalajara, Mariano García-Arranz, Damian García-Olmo
World Journal of Stem Cells.2022; 14(1): 117. CrossRef
Stem Cell Therapies for Gastrointestinal Anastomotic Healing: A Systematic Review and Meta-Analysis on Results from Animal Studies
Apostolos Gaitanidis, Leonidas Kandilogiannakis, Eirini Filidou, Alexandra Tsaroucha, George Kolios, Michail Pitiakoudis
European Surgical Research.2022; 63(4): 173. CrossRef
Effect of Adipose-Derived Stem Cells on Colonic Anastomosis in Rats Immunosuppressed With Everolimus: An Experimental Study
Emre Karakaya, Aydincan Akdur, Alev Ok Atilgan, Ahmet Cagri Uysal, Huriye Eda Ozturan Ozer, Sedat Yildirim, Mehmet Haberal
Experimental and Clinical Transplantation.2021; 19(9): 970. CrossRef
The use of mesenchymal stem cells in animal models for gastrointestinal anastomotic leak: A systematic review
Joshua Richard Burke, Jack Helliwell, Jason Wong, Aaron Quyn, Sarah Herrick, David Jayne
Colorectal Disease.2021; 23(12): 3123. CrossRef
Human Oral Mucosal Stem Cells Reduce Anastomotic Leak in an Animal Model of Colonic Surgery
Ilan Kent, Cyrus Jahansouz, Amandeep Ghuman, Baruch Shpitz, Debora Kidron, Victoria Yaffe, Imad Abu El-Naaj, Shareef Araidy, Luciana Reina, Sandu Pitaru, Steven David Wexner, Shmuel Avital
European Surgical Research.2021; 62(1): 32. CrossRef
Anastomotic leak in colorectal cancer patients: New insights and perspectives
Caterina Foppa, Siew Chien Ng, Marco Montorsi, Antonino Spinelli
European Journal of Surgical Oncology.2020; 46(6): 943. CrossRef
Locally Transplanted Adipose Stem Cells Reduce Anastomotic Leaks in Ischemic Colorectal Anastomoses: A Rat Model
Andrew Morgan, Andrew Zheng, Kimberly M. Linden, Ping Zhang, Spencer A. Brown, Jeffrey P. Carpenter, Francis R. Spitz, Michael E. Kwiatt
Diseases of the Colon & Rectum.2020; 63(7): 955. CrossRef
The Proliferation and Differentiation of Adipose-Derived Stem Cells in Neovascularization and Angiogenesis
Greg Hutchings, Krzysztof Janowicz, Lisa Moncrieff, Claudia Dompe, Ewa Strauss, Ievgeniia Kocherova, Mariusz J. Nawrocki, Łukasz Kruszyna, Grzegorz Wąsiatycz, Paweł Antosik, Jamil A. Shibli, Paul Mozdziak, Bartłomiej Perek, Zbigniew Krasiński, Bartosz Kem
International Journal of Molecular Sciences.2020; 21(11): 3790. CrossRef
Wound healing and fibrosis: current stem cell therapies
Ruth Ellen Jones, Deshka S. Foster, Michael S. Hu, Michael T. Longaker
Transfusion.2019; 59(S1): 884. CrossRef
Protective effect of adipose tissue–derived mesenchymal stromal cells in an experimental model of high-risk colonic anastomosis
Valter Alvarenga, Pedro Teixeira da Silva, Natália Deoclécio Bonfá, Beatriz Pêgo, Hayandra Nanini, Cláudio Bernardazzi, Kalil Madi, Wagner Baetas da Cruz, Morgana Teixeira Castelo-Branco, Heitor Siffert Pereira de Souza, Alberto Schanaider
Surgery.2019; 166(5): 914. CrossRef
Adipose Tissue-Derived Stem Cell Sheet Application for Tissue Healing In Vivo : A Systematic Review
Panithi Sukho, Abigael Cohen, Jan Willem Hesselink, Jolle Kirpensteijn, Femke Verseijden, Yvonne M. Bastiaansen-Jenniskens
Tissue Engineering Part B: Reviews.2018; 24(1): 37. CrossRef
Adipose-Derived Mesenchymal Stromal Cells Improve the Healing of Colonic Anastomoses Following High Dose of Irradiation Through Anti-Inflammatory and Angiogenic Processes
Dirk Van de putte, Christelle Demarquay, Elke Van Daele, Lara Moussa, Christian Vanhove, Marc Benderitter, Wim Ceelen, Piet Pattyn, Noëlle Mathieu
Cell Transplantation.2017; 26(12): 1919. CrossRef
Autologous adipose-derived stem cell sheets enhance the strength of intestinal anastomosis
Yasuhiro Maruya, Nobuo Kanai, Shinichiro Kobayashi, Kurodo Koshino, Teruo Okano, Susumu Eguchi, Masayuki Yamato
Regenerative Therapy.2017; 7: 24. CrossRef
Effects of adipose stem cell sheets on colon anastomotic leakage in an experimental model: Proof of principle
Panithi Sukho, Geesien S.A. Boersema, Abigael Cohen, Nicole Kops, Johan F. Lange, Jolle Kirpensteijn, Jan Willem Hesselink, Yvonne M. Bastiaansen-Jenniskens, Femke Verseijden
Biomaterials.2017; 140: 69. CrossRef
Novel therapy for pancreatic fistula using adipose-derived stem cell sheets treated with mannose
Hirokazu Kaneko, Toshio Kokuryo, Yukihiro Yokoyama, Junpei Yamaguchi, Tokunori Yamamoto, Rei Shibata, Momokazu Gotoh, Toyoaki Murohara, Akira Ito, Masato Nagino
Surgery.2017; 161(6): 1561. CrossRef
Therapeutic angiogenesis of adipose-derived stem cells for ischemic diseases
Lina Zhao, Takerra Johnson, Dong Liu
Stem Cell Research & Therapy.2017;[Epub] CrossRef

Invasiveness of and Drug Sensitivity to Various Anti-cancer Regimens in Five Colorectal Cancer Cell Lines.: Lee, Yoo Mi , Yoon, Yong Sik , Roh, Seon Ae , Cho, Dong Hyung , Kim, Jin Cheon; J Korean Soc Coloproctol. 2010;26(2):98-104.; DOI: https://doi.org/10.3393/jksc.2010.26.2.98

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Abstract PDF

PURPOSE
Colorectal cancer (CRC) is one of the leading causes of cancer death in South Korea. Angiogenesis has been associated with invasion and metastasis of tumors and with the secretion of various growth factors. Bevacizumab is a humanized monoclonal antibody that recognizes and blocks vascular endothelial growth factor (VEGF) and that targets integrin alphaVbeta3 and matrix metalloproteinases (MMPs) as angiogensis inhibitors. The aims of this study were identification of the mechanism of target molecules related to angiogenesis and demonstration of identifiable invasion by using chemotherapeutic regimens in vitro.
METHODS
The five colorectal cancer cell lines were treated with bevacizumab using standard or combined regimens. The expression of integrin alphaVbeta3 was detected and the investigation of apoptosis was done by using flow cytometry. The activations of MMP-2 and MMP-9 were measured by using gelatin zymography.
RESULTS
The apoptotic cell death was significantly increased for the combined regimens, especially for FOLFOX (5-FU, leucovorin, and oxaliplatin) with bevacizumab. Bevacizumab inhibited the expression of integrin alphaVbeta3 in the HT29 (59%), LoVo (67%), and SW480 (17%) cell lines, but did not in the AMC5 and the RKO cell lines. The activations of MMP-2 and MMP-9 were significantly reduced by treatment with bevacizumab in the HT29 and the LoVo cell lines. In the HT29 and the LoVo cell lines, thus, bevacizumab inhibited invasion and metastasis activity through down-regulation of integrin alphaVbeta3 and MMPs.
CONCLUSION
Our results provide biological evidence of potent angiogenic activity and indicate that angiogenesis is a complex process that involves multiple factors, including VEGF, integrin alphaVbeta3, and MMPs.

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RGD peptide in cancer targeting: Benefits, challenges, solutions, and possible integrin–RGD interactions
Hossein Javid, Mahsa Akbari Oryani, Nastaran Rezagholinejad, Ali Esparham, Mahboubeh Tajaldini, Mehdi Karimi‐Shahri
Cancer Medicine.2024;[Epub] CrossRef

Expression of Hypoxia-inducible Factor-1alpha and Vascular Endothelial Growth Factor in Colon Cancer: Relationship to the Prognosis and Tumor Markers.: Choi, Yoon Young , Cho, Hyun Deuk , Park, Dong Guk , Kim, Sung Young , Lee, Moon Soo , Kim, Chang Ho , Cho, Moo Sik , Baek, Moo Jun; J Korean Soc Coloproctol. 2008;24(5):337-344.; DOI: https://doi.org/10.3393/jksc.2008.24.5.337

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Abstract PDF

PURPOSE
Angiogenesis is one of the key steps in solid tumor growth and metastasis. We investigated the prognostic significance of vascular endothelial growth factor (VEGF) and hypoxia-inducible factor 1alpha (HIF-1alpha) expressions as markers of angiogenesis in colon cancer.
METHODS
We retrospectively reviewed the medical records of 78 patients with colon or rectal cancer who underwent a surgical resection at Soonchunhyang University Hospital from January 2000 to December 2001, and we evaluated the expression of VEGF and HIF-1alpha in archival tumor tissues by using immunohistochemistry. We recorded the clinical and the pathological characteristics of the patients and analyzed their survival outcomes.
RESULTS
Thirty-four (34) patients were male, and the mean age of all the patients was 66.7 years. HIF-1alpha and VEGF were positive in 56% (44 patients) and 53% (42 patients) of the tumors, respectively. HIF-1alpha expression was significantly associated with several pathological parameters, such as TNM stage (P=0.001), lymph node metastasis (P=0.001). HIF-1alpha expression was also associated with VEGF expression (P=0.032). The survival of patients with HIF-1alpha expression was worse than that of patients with no HIF-1alpha expression (P=0.036). However, VEGF expression was not associated with other pathological characteristics.
CONCLUSIONS
We suggest that, in cases of colorectal cancer, HIF-1alpha expression may be associated with expression of VEGF, progression of tumors, and poor prognosis.

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Expression of LDH-5 in Colorectal Carcinomas: Correlation with Prognosis and Tumor Angiogenesis
Tae Sung Ahn, Chang Jin Kim, Dong Jun Jung, Dong Guk Park, Sung Woo Cho, Sung Young Kim, Moon Soo Lee, Chang Ho Kim, Moo Sik Cho, Moo Jun Baek
Journal of the Korean Society of Coloproctology.2010; 26(1): 62. CrossRef

Tumor Angiogenesis as a Prognostic Assay for Patients with Colorectal.: Hyun, Moon Soo , Choi, Hong Jo , Jung, Ghap Joong , Kim, Sang Soon; J Korean Soc Coloproctol. 1997;13(2):161-174.

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Abstract PDF: The growth and maintenance of solid tumors are dependent on new capillary ingrowth:a process called "angiogenesis." Thus, after a new tumor has attained a smallsize of a few millimeters in diameter(about 106 cells), further expansion of the tumor-cell population requires the induction of new capillary blood vessels. These new vessels also increase the opportunity for hematogenous or lymph node metastasis. Thus this study was designed to examine the microvessel count at the invasive margin in colorectal carcinoma to determine how angiogenesis correlates with clinicopathologic factors and prognosis. Paraffinembedded tissues from 127 patients with primary colorectal carcinomas that had been completely removed were retrieved and analyzed for angiogenesis. Vessels were immunostained with anti-factor VIII polyclonal antibody, and areas with the most discrete microvessels were counted in a 200 x field, which were defined as angiogenesis score(AS). The mean AS for anti-factor VIII antibody in this study was 55+/-08; therefore, cases were classified into two subgroups : AS high group(n=67), for which AS was greater than 55 and AS low group(n=60), for which AS was equal to 55 or less. There were no significant intergroup difference regarding sex ratio, histologic grade, depth of invasion, or lymphatic invasion. AS was, however, significantly related to tumor size, venous invasion, lymph node metastasis, and liver metastasis(P=0.000, P=0.001, P=0.021, and P=0.004, respectively). The incidence of high AS group in Antler-Coller D was significantly greater than that in Antler-Coller A and B, and Antler-Coller C(P<0.05, respectively). The recurrence rate in high AS group was 32.0%, which was, though statistically insignificant, higher than that in low AS group(17.2%). The 3 year survival rates of high AS group were significantly (P=0.004 both for overall cases and curatively-resected ones) worse than those of low AS group. This study suggests that the growth of colorectal carcinoma is dependent on ingrowth of new blood vessels, and that angiogenesis assessed by the microvessel count using immunohistochemical stains is an important predictor of tumor behavior and may identify patients at higher risk for recurrence and early death.

Expression of Vascular Endothelial Growth Factor and Tumor Necrosis Factor-alpha in Angiogenesis Induced by Lipopolysaccharide and Thalidomide in CT26 Murine Colon Cancer of BALB/c Mouse.: Choi, Dong Lak , Cho, Chang Ho , Jeong, Jin Sook , Hong, Sook Hee , Yoon, Ghil Suk; J Korean Soc Coloproctol. 2004;20(3):125-132.

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Abstract PDF: PURPOSE
The growth, progression, and metastasis of malignant neoplasms are influenced by the environment of the tumor and by proliferation of the tumor itself. Angiogenesis of a malignant neoplasm is a very important environmental factor of tumor growth and metastasis. Also, it is a prognostic factor for malignant neoplasms. The mechanism of angiogenesis, such as the effects of cytokines and angiogenesis-promoting factors, is incompletely understood.
METHODS
This study was designed to define the role of tumor necrosis factor-alpha (TNF-alpha) and the vascular endothelial growth factor (VEGF) in angiogenesis induced by lipopolysaccharide (LPS) and thalidomide (anticytokine drug) in CT26 murine colon cancer transplanted to BALB/c mice.
RESULTS
The tumor size in the LPS-treated group (n=3, 2.1+/-0.26 cm) was larger than it was in the LPS thalidomide-treated group (n=4, 1.95+/-0.19 cm) and in the control group (n=3, 1.6+/-0.20 cm) (P<0.05). The microvessel density determined by CD31 immunostaining was lowest for the control group and highest for the LPS- treated group, but the differences were not statistically significant. An immunohistochemical study showed that the expressions of TNF-alpha (P<0.01) and VEGF (P<0.05) were higher in the experimental groups than they were in the control group. Also, the LPS thalidomide-treated group had lower expressions of TNF-alpha (P<0.01) and VEGF (P<0.05) than the LPS-treated group. Western blots revealed that the TNF-alpha and the VEGF levels semiquantitatively increased from the control group to the LPS thalidomide-treated group to the LPS-treated group.
CONCLUSIONS
Our study revealed that low doses of LPS stimulated angiogenesis through increased expression of TNF-alpha and VEGF. Thalidomide decreased angiogenesis, probably through suppression of TNF-alpha with a decreased expression of VEGF. We conclude that TNF-alpha, suppressed by thalidomide, in the model of transplanted colon cancer may inhibit angiogenesis through coincident decrease in the expression of VEGF.

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