Skip to main content
Top
Published in: BMC Cancer 1/2019

Open Access 01-12-2019 | Melanoma | Research article

The role of vascular mimicry as a biomarker in malignant melanoma: a systematic review and meta-analysis

Authors: Zhenhua Zhang, Saber Imani, Marzieh Dehghan Shasaltaneh, Hossein Hosseinifard, Linglin Zou, Yu Fan, Qinglian Wen

Published in: BMC Cancer | Issue 1/2019

Login to get access

Abstract

Background

Vasculogenic mimicry (VM) a microvascular system consisting of non-endothelial cells that is newly formed by aggressive tumors, has been proposed as an important therapeutic target in malignant melanoma (MM). We performed a systematic literature review to evaluate the diagnostic and prognostic accuracy of VM status for overall survival of MM patients.

Methods

The quality of the included studies was evaluated using the QUADAS-2 tool. Diagnostic capacity of VM variables, including sensitivity, specificity, positive likelihood ratio (PLR), negative likelihood ratio (NLR), diagnostic odds ratio (DOR), and the area under summary receiver operating characteristic (SROC), were pooled using Meta-DiSc software.

Results

A retrospective observational study was conducted based on twelve clinical studies including 978 clinically confirmed melanoma patients with proportion (P). VM+ melanoma cells were associated with poor prognosis in 38% of MM group (P = 0.35, 95% confidence intervals (CI): 0.27–0.42, p < 0.001). The pooled sensitivity and specificity were 0.82 (95% CI: 0.79–0.84) and 0.69 (95% CI: 0.66–0.71), respectively. Furthermore, the pooled PLR, NLR, and DOR were 2.56 (95% CI: 1.94–3.93), 0.17 (95% CI: 0.07–0.42), and 17.75 (95% CI: 5.30–59.44), respectively. Furthermore, the AUC of SROC was 0.63, indicating high reliability of VM status as a biomarker. Importantly, subgroup results suggested that VM+ status is a significantly accurate prognostic biomarker when diagnosed by the CD31−/PAS+ staining methods in Asian MM samples (p < 0.001).

Conclusions

Our findings support the potential of VM status of tumors as a promising prognostic biomarker and emphasize an effective adjuvant therapeutic strategy in the prognosis of Asian MM patients.
Appendix
Available only for authorised users
Literature
2.
go back to reference Jemal A, Saraiya M, Patel P, Cherala SS, Barnholtz-Sloan J, Kim J, Wiggins CL, Wingo PA. Recent trends in cutaneous melanoma incidence and death rates in the United States, 1992–2006. J Am Acad Dermatol. 2011;65(5 Suppl 1):S17–25.e11–13.PubMed Jemal A, Saraiya M, Patel P, Cherala SS, Barnholtz-Sloan J, Kim J, Wiggins CL, Wingo PA. Recent trends in cutaneous melanoma incidence and death rates in the United States, 1992–2006. J Am Acad Dermatol. 2011;65(5 Suppl 1):S17–25.e11–13.PubMed
3.
go back to reference Teh YL, Goh WL, Tan SH, Yong G, Sairi ANH, Soo KC, Ong J, Chia C, Tan G, Soeharno Het al: Treatment and outcomes of melanoma in Asia: Results from the National Cancer Centre Singapore. Asia-Pacific journal of clinical oncology. 2017;4(2):95-102. Teh YL, Goh WL, Tan SH, Yong G, Sairi ANH, Soo KC, Ong J, Chia C, Tan G, Soeharno Het al: Treatment and outcomes of melanoma in Asia: Results from the National Cancer Centre Singapore. Asia-Pacific journal of clinical oncology. 2017;4(2):95-102.
4.
go back to reference Chang JW, Yeh KY, Wang CH, Yang TS, Chiang HF, Wei FC, Kuo TT, Yang CH. Malignant melanoma in Taiwan: a prognostic study of 181 cases. Melanoma Res. 2004;14(6):537–41.CrossRefPubMed Chang JW, Yeh KY, Wang CH, Yang TS, Chiang HF, Wei FC, Kuo TT, Yang CH. Malignant melanoma in Taiwan: a prognostic study of 181 cases. Melanoma Res. 2004;14(6):537–41.CrossRefPubMed
5.
go back to reference Sng J, Koh D, Siong WC, Choo TB. Skin cancer trends among Asians living in Singapore from 1968 to 2006. J Am Acad Dermatol. 2009;61(3):426–32.CrossRefPubMed Sng J, Koh D, Siong WC, Choo TB. Skin cancer trends among Asians living in Singapore from 1968 to 2006. J Am Acad Dermatol. 2009;61(3):426–32.CrossRefPubMed
6.
go back to reference Koh D, Wang H, Lee J, Chia KS, Lee HP, Goh CL. Basal cell carcinoma, squamous cell carcinoma and melanoma of the skin: analysis of the Singapore Cancer Registry data 1968-97. Br J Dermatol. 2003;148(6):1161–6.CrossRefPubMed Koh D, Wang H, Lee J, Chia KS, Lee HP, Goh CL. Basal cell carcinoma, squamous cell carcinoma and melanoma of the skin: analysis of the Singapore Cancer Registry data 1968-97. Br J Dermatol. 2003;148(6):1161–6.CrossRefPubMed
7.
go back to reference Shoo BA, Kashani-Sabet M. Melanoma arising in African-, Asian-, Latino- and native-American populations. Semin Cutan Med Surg. 2009;28(2):96–102.CrossRefPubMed Shoo BA, Kashani-Sabet M. Melanoma arising in African-, Asian-, Latino- and native-American populations. Semin Cutan Med Surg. 2009;28(2):96–102.CrossRefPubMed
8.
go back to reference Shoo BA, Sagebiel RW, Kashani-Sabet M. Discordance in the histopathologic diagnosis of melanoma at a melanoma referral center. J Am Acad Dermatol. 2010;62(5):751–6.CrossRefPubMed Shoo BA, Sagebiel RW, Kashani-Sabet M. Discordance in the histopathologic diagnosis of melanoma at a melanoma referral center. J Am Acad Dermatol. 2010;62(5):751–6.CrossRefPubMed
9.
go back to reference Kim HK, Lee S, Kim K, Heo MH, Lee H, Cho J, Kim NKD, Park W, Lee SJ, Kim JH, et al. Efficacy of BRAF inhibitors in Asian metastatic melanoma patients: potential implications of genomic sequencing in BRAF-mutated melanoma. Transl Oncol. 2016;9(6):557–64.CrossRefPubMedPubMedCentral Kim HK, Lee S, Kim K, Heo MH, Lee H, Cho J, Kim NKD, Park W, Lee SJ, Kim JH, et al. Efficacy of BRAF inhibitors in Asian metastatic melanoma patients: potential implications of genomic sequencing in BRAF-mutated melanoma. Transl Oncol. 2016;9(6):557–64.CrossRefPubMedPubMedCentral
10.
11.
go back to reference Tsoutsos D, Papadopoulos S, Kehagias G, Mara A, Kyriopoulou E, Karonidis A, Spiliopoulos K, Mpalitsaris E, Karapiperis G, Panayotou P, et al. Epidemiological trends in the diagnosis of melanoma in a southern European population: analysis of a large database from a tertiary referral center. Melanoma Res. 2018;28(4):348–58.PubMed Tsoutsos D, Papadopoulos S, Kehagias G, Mara A, Kyriopoulou E, Karonidis A, Spiliopoulos K, Mpalitsaris E, Karapiperis G, Panayotou P, et al. Epidemiological trends in the diagnosis of melanoma in a southern European population: analysis of a large database from a tertiary referral center. Melanoma Res. 2018;28(4):348–58.PubMed
12.
go back to reference Brunssen A, Jansen L, Eisemann N, Waldmann A, Weberpals J, Kraywinkel K, Eberle A, Holleczek B, Zeissig SR, Brenner H, et al. Long-term relative survival from melanoma in Germany 1997-2013. Melanoma Res. 2018;17(1):1-10. Brunssen A, Jansen L, Eisemann N, Waldmann A, Weberpals J, Kraywinkel K, Eberle A, Holleczek B, Zeissig SR, Brenner H, et al. Long-term relative survival from melanoma in Germany 1997-2013. Melanoma Res. 2018;17(1):1-10.
13.
go back to reference Yamazaki N, Kiyohara Y, Uhara H, Uehara J, Fujimoto M, Takenouchi T, Otsuka M, Uchi H, Ihn H, Minami H. Efficacy and safety of nivolumab in Japanese patients with previously untreated advanced melanoma: a phase II study. Cancer Sci. 2017;108(6):1223–30.CrossRefPubMedPubMedCentral Yamazaki N, Kiyohara Y, Uhara H, Uehara J, Fujimoto M, Takenouchi T, Otsuka M, Uchi H, Ihn H, Minami H. Efficacy and safety of nivolumab in Japanese patients with previously untreated advanced melanoma: a phase II study. Cancer Sci. 2017;108(6):1223–30.CrossRefPubMedPubMedCentral
15.
go back to reference Tringali C, Silvestri I, Testa F, Baldassari P, Anastasia L, Mortarini R, Anichini A, Lopez-Requena A, Tettamanti G, Venerando B. Molecular subtyping of metastatic melanoma based on cell ganglioside metabolism profiles. BMC Cancer. 2014;14:560.CrossRefPubMedPubMedCentral Tringali C, Silvestri I, Testa F, Baldassari P, Anastasia L, Mortarini R, Anichini A, Lopez-Requena A, Tettamanti G, Venerando B. Molecular subtyping of metastatic melanoma based on cell ganglioside metabolism profiles. BMC Cancer. 2014;14:560.CrossRefPubMedPubMedCentral
16.
go back to reference Zhang J, Qiao L, Liang N, Xie J, Luo H, Deng G, Zhang J. Vasculogenic mimicry and tumor metastasis. J BUON. 2016;21(3):533–41.PubMed Zhang J, Qiao L, Liang N, Xie J, Luo H, Deng G, Zhang J. Vasculogenic mimicry and tumor metastasis. J BUON. 2016;21(3):533–41.PubMed
17.
go back to reference Delgado-Bellido D, Serrano-Saenz S, Fernandez-Cortes M, Oliver FJ. Vasculogenic mimicry signaling revisited: focus on non-vascular VE-cadherin. Mol Cancer. 2017;16(1):65.CrossRefPubMedPubMedCentral Delgado-Bellido D, Serrano-Saenz S, Fernandez-Cortes M, Oliver FJ. Vasculogenic mimicry signaling revisited: focus on non-vascular VE-cadherin. Mol Cancer. 2017;16(1):65.CrossRefPubMedPubMedCentral
18.
go back to reference Hendrix MJ, Seftor EA, Seftor RE, Chao JT, Chien DS, Chu YW. Tumor cell vascular mimicry: novel targeting opportunity in melanoma. Pharmacol Ther. 2016;159:83–92.CrossRefPubMedPubMedCentral Hendrix MJ, Seftor EA, Seftor RE, Chao JT, Chien DS, Chu YW. Tumor cell vascular mimicry: novel targeting opportunity in melanoma. Pharmacol Ther. 2016;159:83–92.CrossRefPubMedPubMedCentral
19.
go back to reference Cao Z, Bao M, Miele L, Sarkar FH, Wang Z, Zhou Q. Tumour vasculogenic mimicry is associated with poor prognosis of human cancer patients: a systemic review and meta-analysis. Eur J Cancer. 2013;49(18):3914–23.CrossRefPubMed Cao Z, Bao M, Miele L, Sarkar FH, Wang Z, Zhou Q. Tumour vasculogenic mimicry is associated with poor prognosis of human cancer patients: a systemic review and meta-analysis. Eur J Cancer. 2013;49(18):3914–23.CrossRefPubMed
20.
go back to reference Wu S, Yu L, Wang D, Zhou L, Cheng Z, Chai D, Ma L, Tao Y. Aberrant expression of CD133 in non-small cell lung cancer and its relationship to vasculogenic mimicry. BMC Cancer. 2012;12:535.CrossRefPubMedPubMedCentral Wu S, Yu L, Wang D, Zhou L, Cheng Z, Chai D, Ma L, Tao Y. Aberrant expression of CD133 in non-small cell lung cancer and its relationship to vasculogenic mimicry. BMC Cancer. 2012;12:535.CrossRefPubMedPubMedCentral
21.
go back to reference Abazis-Stamboulieh D, Oikonomou P, Papadoulis N, Panayiotidis P, Vrakidou E, Tsezou A. Association of interleukin-1A, interleukin-1B and interleukin-1 receptor antagonist gene polymorphisms with multiple myeloma. Leuk Lymphoma. 2007;48(11):2196–203.CrossRefPubMed Abazis-Stamboulieh D, Oikonomou P, Papadoulis N, Panayiotidis P, Vrakidou E, Tsezou A. Association of interleukin-1A, interleukin-1B and interleukin-1 receptor antagonist gene polymorphisms with multiple myeloma. Leuk Lymphoma. 2007;48(11):2196–203.CrossRefPubMed
22.
go back to reference Caramel J, Papadogeorgakis E, Hill L, Browne GJ, Richard G, Wierinckx A, Saldanha G, Osborne J, Hutchinson P, Tse G, et al. A switch in the expression of embryonic EMT-inducers drives the development of malignant melanoma. Cancer Cell. 2013;24(4):466–80.CrossRefPubMed Caramel J, Papadogeorgakis E, Hill L, Browne GJ, Richard G, Wierinckx A, Saldanha G, Osborne J, Hutchinson P, Tse G, et al. A switch in the expression of embryonic EMT-inducers drives the development of malignant melanoma. Cancer Cell. 2013;24(4):466–80.CrossRefPubMed
23.
go back to reference Vartanian A, Baryshnikov AY. Crosstalk between apoptosis and antioxidants in melanoma vasculogenic mimicry. Adv Exp Med Biol. 2007;601:145–53.CrossRefPubMed Vartanian A, Baryshnikov AY. Crosstalk between apoptosis and antioxidants in melanoma vasculogenic mimicry. Adv Exp Med Biol. 2007;601:145–53.CrossRefPubMed
24.
go back to reference Paulis YW, Soetekouw PM, Verheul HM, Tjan-Heijnen VC, Griffioen AW. Signalling pathways in vasculogenic mimicry. Biochim Biophys Acta. 2010;1806(1):18–28.PubMed Paulis YW, Soetekouw PM, Verheul HM, Tjan-Heijnen VC, Griffioen AW. Signalling pathways in vasculogenic mimicry. Biochim Biophys Acta. 2010;1806(1):18–28.PubMed
25.
go back to reference Cao Z, Yu D, Fu S, Zhang G, Pan Y, Bao M, Tu J, Shang B, Guo P, Yang P, et al. Lycorine hydrochloride selectively inhibits human ovarian cancer cell proliferation and tumor neovascularization with very low toxicity. Toxicol Lett. 2013;218(2):174–85.CrossRefPubMed Cao Z, Yu D, Fu S, Zhang G, Pan Y, Bao M, Tu J, Shang B, Guo P, Yang P, et al. Lycorine hydrochloride selectively inhibits human ovarian cancer cell proliferation and tumor neovascularization with very low toxicity. Toxicol Lett. 2013;218(2):174–85.CrossRefPubMed
26.
go back to reference Xu XD, Yang L, Zheng LY, Pan YY, Cao ZF, Zhang ZQ, Zhou QS, Yang B, Cao C. Erratum to: Suberoylanilide hydroxamic acid, an inhibitor of histone deacetylase, suppresses vasculogenic mimicry and proliferation of highly aggressive pancreatic cancer PaTu8988 cells. BMC Cancer. 2016;16(1):374.CrossRefPubMedPubMedCentral Xu XD, Yang L, Zheng LY, Pan YY, Cao ZF, Zhang ZQ, Zhou QS, Yang B, Cao C. Erratum to: Suberoylanilide hydroxamic acid, an inhibitor of histone deacetylase, suppresses vasculogenic mimicry and proliferation of highly aggressive pancreatic cancer PaTu8988 cells. BMC Cancer. 2016;16(1):374.CrossRefPubMedPubMedCentral
27.
go back to reference Shirakawa K, Kobayashi H, Heike Y, Kawamoto S, Brechbiel MW, Kasumi F, Iwanaga T, Konishi F, Terada M, Wakasugi H. Hemodynamics in vasculogenic mimicry and angiogenesis of inflammatory breast cancer xenograft. Cancer Res. 2002;62(2):560–6.PubMed Shirakawa K, Kobayashi H, Heike Y, Kawamoto S, Brechbiel MW, Kasumi F, Iwanaga T, Konishi F, Terada M, Wakasugi H. Hemodynamics in vasculogenic mimicry and angiogenesis of inflammatory breast cancer xenograft. Cancer Res. 2002;62(2):560–6.PubMed
28.
go back to reference Baeten CI, Hillen F, Pauwels P, de Bruine AP, Baeten CG. Prognostic role of vasculogenic mimicry in colorectal cancer. Dis Colon Rectum. 2009;52(12):2028–35.CrossRefPubMed Baeten CI, Hillen F, Pauwels P, de Bruine AP, Baeten CG. Prognostic role of vasculogenic mimicry in colorectal cancer. Dis Colon Rectum. 2009;52(12):2028–35.CrossRefPubMed
29.
go back to reference Ding J, Jia X, Zuo B, He J, Yang J, He Y. A novel monoclonal antibody targeting a novel epitope of VEcadherin inhibits vasculogenic mimicry of lung cancer cells. Oncol Rep. 2018;39(6):2837–44.PubMed Ding J, Jia X, Zuo B, He J, Yang J, He Y. A novel monoclonal antibody targeting a novel epitope of VEcadherin inhibits vasculogenic mimicry of lung cancer cells. Oncol Rep. 2018;39(6):2837–44.PubMed
30.
go back to reference Liu WB, Xu GL, Jia WD, Li JS, Ma JL, Chen K, Wang ZH, Ge YS, Ren WH, Yu JH, et al. Prognostic significance and mechanisms of patterned matrix vasculogenic mimicry in hepatocellular carcinoma. Med Oncol. 2011;28(Suppl 1):S228–38.CrossRefPubMed Liu WB, Xu GL, Jia WD, Li JS, Ma JL, Chen K, Wang ZH, Ge YS, Ren WH, Yu JH, et al. Prognostic significance and mechanisms of patterned matrix vasculogenic mimicry in hepatocellular carcinoma. Med Oncol. 2011;28(Suppl 1):S228–38.CrossRefPubMed
31.
go back to reference Tang HS, Feng YJ, Yao LQ. Angiogenesis, vasculogenesis, and vasculogenic mimicry in ovarian cancer. Int J Gynecol Cancer. 2009;19(4):605–10.CrossRefPubMed Tang HS, Feng YJ, Yao LQ. Angiogenesis, vasculogenesis, and vasculogenic mimicry in ovarian cancer. Int J Gynecol Cancer. 2009;19(4):605–10.CrossRefPubMed
32.
go back to reference Guo Q, Yuan Y, Jin Z, Xu T, Gao Y, Wei H, Li C, Hou W, Hua B. Association between tumor vasculogenic mimicry and the poor prognosis of gastric cancer in China: an updated systematic review and meta-analysis. Biomed Res Int. 2016;2016:2408645.PubMedPubMedCentral Guo Q, Yuan Y, Jin Z, Xu T, Gao Y, Wei H, Li C, Hou W, Hua B. Association between tumor vasculogenic mimicry and the poor prognosis of gastric cancer in China: an updated systematic review and meta-analysis. Biomed Res Int. 2016;2016:2408645.PubMedPubMedCentral
33.
go back to reference Fujimoto A, Onodera H, Mori A, Nagayama S, Yonenaga Y, Tachibana T. Tumour plasticity and extravascular circulation in ECV304 human bladder carcinoma cells. Anticancer Res. 2006;26(1A):59–69.CrossRefPubMed Fujimoto A, Onodera H, Mori A, Nagayama S, Yonenaga Y, Tachibana T. Tumour plasticity and extravascular circulation in ECV304 human bladder carcinoma cells. Anticancer Res. 2006;26(1A):59–69.CrossRefPubMed
34.
35.
go back to reference Panic N, Leoncini E, de Belvis G, Ricciardi W, Boccia S. Evaluation of the endorsement of the preferred reporting items for systematic reviews and meta-analysis (PRISMA) statement on the quality of published systematic review and meta-analyses. PLoS One. 2013;8(12):e83138.CrossRefPubMedPubMedCentral Panic N, Leoncini E, de Belvis G, Ricciardi W, Boccia S. Evaluation of the endorsement of the preferred reporting items for systematic reviews and meta-analysis (PRISMA) statement on the quality of published systematic review and meta-analyses. PLoS One. 2013;8(12):e83138.CrossRefPubMedPubMedCentral
36.
go back to reference Richardson WS, Wilson MC, Nishikawa J, Hayward RS. The well-built clinical question: a key to evidence-based decisions. ACP J Club. 1995;123(3):A12–3.PubMed Richardson WS, Wilson MC, Nishikawa J, Hayward RS. The well-built clinical question: a key to evidence-based decisions. ACP J Club. 1995;123(3):A12–3.PubMed
37.
go back to reference Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–5.CrossRefPubMed Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–5.CrossRefPubMed
38.
go back to reference Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang MM, Sterne JA, Bossuyt PM, Group Q. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155(8):529–36.CrossRefPubMed Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang MM, Sterne JA, Bossuyt PM, Group Q. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155(8):529–36.CrossRefPubMed
39.
go back to reference Imani S, Zhang X, Hosseinifard H, Fu S, Fu J. The diagnostic role of microRNA-34a in breast cancer: a systematic review and meta-analysis. Oncotarget. 2017;8(14):23177–87.CrossRefPubMedPubMedCentral Imani S, Zhang X, Hosseinifard H, Fu S, Fu J. The diagnostic role of microRNA-34a in breast cancer: a systematic review and meta-analysis. Oncotarget. 2017;8(14):23177–87.CrossRefPubMedPubMedCentral
40.
go back to reference Imani S, Hosseinifard H, Cheng J, Wei C, Fu J. Prognostic value of EMT-inducing transcription factors (EMT-TFs) in metastatic breast cancer: a systematic review and meta-analysis. Sci Rep. 2016;6:28587.CrossRefPubMedPubMedCentral Imani S, Hosseinifard H, Cheng J, Wei C, Fu J. Prognostic value of EMT-inducing transcription factors (EMT-TFs) in metastatic breast cancer: a systematic review and meta-analysis. Sci Rep. 2016;6:28587.CrossRefPubMedPubMedCentral
41.
go back to reference Song H, Jing G, Wang L, Guo W, Ren G. Periodic acid-Schiff-positive loops and networks as a prognostic factor in oral mucosal melanoma. Melanoma Res. 2016;26(2):145–52.CrossRefPubMed Song H, Jing G, Wang L, Guo W, Ren G. Periodic acid-Schiff-positive loops and networks as a prognostic factor in oral mucosal melanoma. Melanoma Res. 2016;26(2):145–52.CrossRefPubMed
42.
go back to reference Zhang W, Zhou P, Meng A, Zhang R, Zhou Y: Down-regulating Myoferlin inhibits the vasculogenic mimicry of melanoma via decreasing MMP-2 and inducing mesenchymal-to-epithelial transition. Journal of cellular and molecular medicine. 2018;22(3):1743-54. Zhang W, Zhou P, Meng A, Zhang R, Zhou Y: Down-regulating Myoferlin inhibits the vasculogenic mimicry of melanoma via decreasing MMP-2 and inducing mesenchymal-to-epithelial transition. Journal of cellular and molecular medicine. 2018;22(3):1743-54.
43.
go back to reference Munafo MR, Clark TG, Flint J. Assessing publication bias in genetic association studies: evidence from a recent meta-analysis. Psychiatry Res. 2004;129(1):39–44.CrossRefPubMed Munafo MR, Clark TG, Flint J. Assessing publication bias in genetic association studies: evidence from a recent meta-analysis. Psychiatry Res. 2004;129(1):39–44.CrossRefPubMed
45.
go back to reference Massi D, Franchi A, Paglierani M, Ketabchi S, Borgognoni L, Reali UM, Santucci M. Vasculogenic mimicry has no prognostic significance in pT3 and pT4 cutaneous melanoma. Hum Pathol. 2004;35(4):496–502.CrossRefPubMed Massi D, Franchi A, Paglierani M, Ketabchi S, Borgognoni L, Reali UM, Santucci M. Vasculogenic mimicry has no prognostic significance in pT3 and pT4 cutaneous melanoma. Hum Pathol. 2004;35(4):496–502.CrossRefPubMed
46.
go back to reference Sun B, Zhang S, Zhao X, Zhang W, Hao X. Vasculogenic mimicry is associated with poor survival in patients with mesothelial sarcomas and alveolar rhabdomyosarcomas. Int J Oncol. 2004;25(6):1609–14.PubMed Sun B, Zhang S, Zhao X, Zhang W, Hao X. Vasculogenic mimicry is associated with poor survival in patients with mesothelial sarcomas and alveolar rhabdomyosarcomas. Int J Oncol. 2004;25(6):1609–14.PubMed
47.
go back to reference Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe'er J, Trent JM, Meltzer PS, Hendrix MJ. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol. 1999;155(3):739–52.CrossRefPubMedPubMedCentral Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe'er J, Trent JM, Meltzer PS, Hendrix MJ. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol. 1999;155(3):739–52.CrossRefPubMedPubMedCentral
48.
go back to reference Hillen F, Baeten CI, van de Winkel A, Creytens D, van der Schaft DW, Winnepenninckx V, Griffioen AW. Leukocyte infiltration and tumor cell plasticity are parameters of aggressiveness in primary cutaneous melanoma. Cancer Immunol Immunother. 2008;57(1):97–106.CrossRefPubMed Hillen F, Baeten CI, van de Winkel A, Creytens D, van der Schaft DW, Winnepenninckx V, Griffioen AW. Leukocyte infiltration and tumor cell plasticity are parameters of aggressiveness in primary cutaneous melanoma. Cancer Immunol Immunother. 2008;57(1):97–106.CrossRefPubMed
49.
go back to reference Zhang S, Li M, Zhang D, Xu S, Wang X, Liu Z, Zhao X, Sun B. Hypoxia influences linearly patterned programmed cell necrosis and tumor blood supply patterns formation in melanoma. Lab Invest. 2009;89(5):575–86.CrossRefPubMed Zhang S, Li M, Zhang D, Xu S, Wang X, Liu Z, Zhao X, Sun B. Hypoxia influences linearly patterned programmed cell necrosis and tumor blood supply patterns formation in melanoma. Lab Invest. 2009;89(5):575–86.CrossRefPubMed
50.
go back to reference Shi L, Lei D, Ma C, Xu F, Li Y, Wang Y, Cong N, Liu D, Pan XL. Clinicopathological implications of tumour-associated macrophages and vascularization in sinonasal melanoma. J Int Med Res. 2010;38(4):1276–86.CrossRefPubMed Shi L, Lei D, Ma C, Xu F, Li Y, Wang Y, Cong N, Liu D, Pan XL. Clinicopathological implications of tumour-associated macrophages and vascularization in sinonasal melanoma. J Int Med Res. 2010;38(4):1276–86.CrossRefPubMed
51.
go back to reference van Beurden A, Schmitz RF, van Dijk CM, Baeten CI. Periodic acid Schiff loops and blood lakes associated with metastasis in cutaneous melanoma. Melanoma Res. 2012;22(6):424–9.CrossRefPubMed van Beurden A, Schmitz RF, van Dijk CM, Baeten CI. Periodic acid Schiff loops and blood lakes associated with metastasis in cutaneous melanoma. Melanoma Res. 2012;22(6):424–9.CrossRefPubMed
52.
go back to reference Baocun S, Shiwu Z, Xiulan Z, Danfang Z, Xishan H. Pilot study of molecular mechanism on vasculogenic mimicry in bi-directional differentiated malignant tumors. Chin-Ger J Clin Oncol. 2015;4(1):50–2. Baocun S, Shiwu Z, Xiulan Z, Danfang Z, Xishan H. Pilot study of molecular mechanism on vasculogenic mimicry in bi-directional differentiated malignant tumors. Chin-Ger J Clin Oncol. 2015;4(1):50–2.
53.
go back to reference Zhao X, Sun B, Li Y, Liu Y, Zhang D, Wang X, Gu Q, Zhao J, Dong X, Liu Z, et al. Dual effects of collagenase-3 on melanoma: metastasis promotion and disruption of vasculogenic mimicry. Oncotarget. 2015;6(11):8890–9.PubMedPubMedCentral Zhao X, Sun B, Li Y, Liu Y, Zhang D, Wang X, Gu Q, Zhao J, Dong X, Liu Z, et al. Dual effects of collagenase-3 on melanoma: metastasis promotion and disruption of vasculogenic mimicry. Oncotarget. 2015;6(11):8890–9.PubMedPubMedCentral
54.
go back to reference Liang X, Sun R, Zhao X, Zhang Y, Gu Q, Dong X, Zhang D, Sun J, Sun B. Rictor regulates the vasculogenic mimicry of melanoma via the AKT-MMP-2/9 pathway. J Cell Mol Med. 2017;21(12):3579–91.CrossRefPubMedPubMedCentral Liang X, Sun R, Zhao X, Zhang Y, Gu Q, Dong X, Zhang D, Sun J, Sun B. Rictor regulates the vasculogenic mimicry of melanoma via the AKT-MMP-2/9 pathway. J Cell Mol Med. 2017;21(12):3579–91.CrossRefPubMedPubMedCentral
55.
go back to reference Itzhaki O, Greenberg E, Shalmon B, Kubi A, Treves AJ, Shapira-Frommer R, Avivi C, Ortenberg R, Ben-Ami E, Schachter J, et al. Nicotinamide inhibits vasculogenic mimicry, an alternative vascularization pathway observed in highly aggressive melanoma. PLoS One. 2013;8(2):e57160.CrossRefPubMedPubMedCentral Itzhaki O, Greenberg E, Shalmon B, Kubi A, Treves AJ, Shapira-Frommer R, Avivi C, Ortenberg R, Ben-Ami E, Schachter J, et al. Nicotinamide inhibits vasculogenic mimicry, an alternative vascularization pathway observed in highly aggressive melanoma. PLoS One. 2013;8(2):e57160.CrossRefPubMedPubMedCentral
56.
go back to reference Liu Q, Qiao L, Liang N, Xie J, Zhang J, Deng G, Luo H, Zhang J. The relationship between vasculogenic mimicry and epithelial-mesenchymal transitions. J Cell Mol Med. 2016;20(9):1761–9.CrossRefPubMedPubMedCentral Liu Q, Qiao L, Liang N, Xie J, Zhang J, Deng G, Luo H, Zhang J. The relationship between vasculogenic mimicry and epithelial-mesenchymal transitions. J Cell Mol Med. 2016;20(9):1761–9.CrossRefPubMedPubMedCentral
57.
go back to reference Francis JH, Kim J, Lin A, Folberg R, Iyer S, Abramson DH. Growth of uveal melanoma following intravitreal bevacizumab. Ocul Oncol Pathol. 2017;3(2):117–21.CrossRefPubMed Francis JH, Kim J, Lin A, Folberg R, Iyer S, Abramson DH. Growth of uveal melanoma following intravitreal bevacizumab. Ocul Oncol Pathol. 2017;3(2):117–21.CrossRefPubMed
58.
go back to reference Schnegg CI, Yang MH, Ghosh SK, Hsu MY. Induction of vasculogenic mimicry overrides VEGF-A silencing and enriches stem-like cancer cells in melanoma. Cancer Res. 2015;75(8):1682–90.CrossRefPubMedPubMedCentral Schnegg CI, Yang MH, Ghosh SK, Hsu MY. Induction of vasculogenic mimicry overrides VEGF-A silencing and enriches stem-like cancer cells in melanoma. Cancer Res. 2015;75(8):1682–90.CrossRefPubMedPubMedCentral
59.
go back to reference Liu J, Qu X, Shao L, Hu Y, Yu X, Lan P, Guo Q, Han Q, Zhang J, Zhang C. Pim-3 enhances melanoma cell migration and invasion by promoting STAT3 phosphorylation. Cancer Biol Ther. 2018;19(3):160–8.CrossRefPubMedPubMedCentral Liu J, Qu X, Shao L, Hu Y, Yu X, Lan P, Guo Q, Han Q, Zhang J, Zhang C. Pim-3 enhances melanoma cell migration and invasion by promoting STAT3 phosphorylation. Cancer Biol Ther. 2018;19(3):160–8.CrossRefPubMedPubMedCentral
60.
go back to reference Pulford E, Hocking A, Griggs K, McEvoy J, Bonder C, Henderson DW, Klebe S. Vasculogenic mimicry in malignant mesothelioma: an experimental and immunohistochemical analysis. Pathology. 2016;48(7):650–9.CrossRefPubMed Pulford E, Hocking A, Griggs K, McEvoy J, Bonder C, Henderson DW, Klebe S. Vasculogenic mimicry in malignant mesothelioma: an experimental and immunohistochemical analysis. Pathology. 2016;48(7):650–9.CrossRefPubMed
62.
go back to reference Matthews NH, Li WQ, Qureshi AA, Weinstock MA, Cho E. Epidemiology of melanoma. In: Ward WH, Farma JM, editors. Cutaneous melanoma: etiology and therapy. edn. Brisbane: Codon Publications; 2017. Matthews NH, Li WQ, Qureshi AA, Weinstock MA, Cho E. Epidemiology of melanoma. In: Ward WH, Farma JM, editors. Cutaneous melanoma: etiology and therapy. edn. Brisbane: Codon Publications; 2017.
63.
go back to reference Qin L, Ren Y, Chen AM, Guo FJ, Xu F, Gong C, Cheng P, Du Y, Liao H. Peroxisome proliferator-activated receptor gamma ligands inhibit VEGF-mediated vasculogenic mimicry of prostate cancer through the AKT signaling pathway. Mol Med Rep. 2014;10(1):276–82.CrossRefPubMed Qin L, Ren Y, Chen AM, Guo FJ, Xu F, Gong C, Cheng P, Du Y, Liao H. Peroxisome proliferator-activated receptor gamma ligands inhibit VEGF-mediated vasculogenic mimicry of prostate cancer through the AKT signaling pathway. Mol Med Rep. 2014;10(1):276–82.CrossRefPubMed
64.
go back to reference Shen Y, Quan J, Wang M, Li S, Yang J, Lv M, Chen Z, Zhang L, Zhao X, Yang J. Tumor vasculogenic mimicry formation as an unfavorable prognostic indicator in patients with breast cancer. Oncotarget. 2017;8(34):56408–16.PubMedPubMedCentral Shen Y, Quan J, Wang M, Li S, Yang J, Lv M, Chen Z, Zhang L, Zhao X, Yang J. Tumor vasculogenic mimicry formation as an unfavorable prognostic indicator in patients with breast cancer. Oncotarget. 2017;8(34):56408–16.PubMedPubMedCentral
65.
go back to reference Yang JP, Liao YD, Mai DM, Xie P, Qiang YY, Zheng LS, Wang MY, Mei Y, Meng DF, Xu L, et al. Tumor vasculogenic mimicry predicts poor prognosis in cancer patients: a meta-analysis. Angiogenesis. 2016;19(2):191–200.CrossRefPubMed Yang JP, Liao YD, Mai DM, Xie P, Qiang YY, Zheng LS, Wang MY, Mei Y, Meng DF, Xu L, et al. Tumor vasculogenic mimicry predicts poor prognosis in cancer patients: a meta-analysis. Angiogenesis. 2016;19(2):191–200.CrossRefPubMed
Metadata
Title
The role of vascular mimicry as a biomarker in malignant melanoma: a systematic review and meta-analysis
Authors
Zhenhua Zhang
Saber Imani
Marzieh Dehghan Shasaltaneh
Hossein Hosseinifard
Linglin Zou
Yu Fan
Qinglian Wen
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2019
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-019-6350-5

Other articles of this Issue 1/2019

BMC Cancer 1/2019 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine