Vasohibin-1 Expression Can Predict Pathological Complete Remission of Advanced Bladder Cancer with Neoadjuvant Chemotherapy.

Angiogenesis Biomarkers Bladder cancer Chemotherapy Pathological outcome

Journal

Annals of surgical oncology
ISSN: 1534-4681
Titre abrégé: Ann Surg Oncol
Pays: United States
ID NLM: 9420840

Informations de publication

Date de publication:
20 Feb 2024
Historique:
received: 28 11 2023
accepted: 21 01 2024
medline: 20 2 2024
pubmed: 20 2 2024
entrez: 20 2 2024
Statut: aheadofprint

Résumé

Neoadjuvant chemotherapy (NAC) is a well-established standard practice in invasive bladder cancer (BCa), however patient selection remains challenging. High expression of vasohibin-1 (VASH1), an endogenous regulator of angiogenesis, has been reported in high-grade and advanced BCa; however, its prognostic value for chemotherapy outcomes remains unexplored. In this study, we sought to identify biomarkers of chemotherapy response focusing on the relationship between angiogenesis and tissue hypoxia. Forty Japanese patients with BCa who underwent NAC and radical cystectomy were included in the present analysis. We compared the immunohistochemical expression of CD34, VASH1, and carbonic anhydrase 9 (CA9) between patients who achieved tumor clearance at operation (ypT0) and those with residual disease after cystectomy. There were 19 patients in the ypT0 group, while the remaining 21 patients had residual tumors at operation. Patients in the ypT0 group had high microvessel density (p = 0.031), high VASH1 density (p < 0.001), and stronger CA9 staining (p = 0.046) than their counterparts. Multivariate analysis identified microvessel and VASH1 density as independent predictive factors for pathological ypT0 disease (p = 0.043 and 0.002, respectively). The 5-year recurrence-free survival rate was higher in the high VASH1 density group than in the low VASH1 density group (66.3% vs. 33.3%, p = 0.036). VASH1 density is a potential therapeutic biomarker for chemotherapy response in BCa.

Sections du résumé

BACKGROUND AND PURPOSE OBJECTIVE
Neoadjuvant chemotherapy (NAC) is a well-established standard practice in invasive bladder cancer (BCa), however patient selection remains challenging. High expression of vasohibin-1 (VASH1), an endogenous regulator of angiogenesis, has been reported in high-grade and advanced BCa; however, its prognostic value for chemotherapy outcomes remains unexplored. In this study, we sought to identify biomarkers of chemotherapy response focusing on the relationship between angiogenesis and tissue hypoxia.
METHODS METHODS
Forty Japanese patients with BCa who underwent NAC and radical cystectomy were included in the present analysis. We compared the immunohistochemical expression of CD34, VASH1, and carbonic anhydrase 9 (CA9) between patients who achieved tumor clearance at operation (ypT0) and those with residual disease after cystectomy.
RESULTS RESULTS
There were 19 patients in the ypT0 group, while the remaining 21 patients had residual tumors at operation. Patients in the ypT0 group had high microvessel density (p = 0.031), high VASH1 density (p < 0.001), and stronger CA9 staining (p = 0.046) than their counterparts. Multivariate analysis identified microvessel and VASH1 density as independent predictive factors for pathological ypT0 disease (p = 0.043 and 0.002, respectively). The 5-year recurrence-free survival rate was higher in the high VASH1 density group than in the low VASH1 density group (66.3% vs. 33.3%, p = 0.036).
CONCLUSION CONCLUSIONS
VASH1 density is a potential therapeutic biomarker for chemotherapy response in BCa.

Identifiants

pubmed: 38376711
doi: 10.1245/s10434-024-15009-1
pii: 10.1245/s10434-024-15009-1
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Japan Society for the Promotion of Science
ID : # 21K1957
Organisme : Japan Society for the Promotion of Science
ID : #20H03817

Informations de copyright

© 2024. The Author(s).

Références

World Health Organization International Agency for Research on Cancer. 2020. Available at: https://gco.iarc.fr/today/online-analysis-table . Accessed 22 Feb 2023.
Schrier BP, Hollander MP, van Rhijn BW, Kiemeney LA, Witjes JA. Prognosis of muscle-invasive bladder cancer: difference between primary and progressive tumours and implications for therapy. Eur Urol. 2004;45(3):292–296. https://doi.org/10.1016/j.eururo.2003.10.006 .
doi: 10.1016/j.eururo.2003.10.006 pubmed: 15036673
Witjes JA, Bruins HM, Cathomas R, et al. European association of urology guidelines on muscle-invasive and metastatic bladder cancer: summary of the 2020 guidelines. EurUrol. 2021;79(1):82–104.  https://doi.org/10.1016/j.eururo.2020.03.055 .
doi: 10.1016/j.eururo.2020.03.055
Yin M, Joshi M, Meijer RP, et al. Neoadjuvant chemotherapy for muscle-invasive bladder cancer: a systematic review and two-step meta-analysis. Oncologist. 2016;21(6):708–715.  https://doi.org/10.1634/theoncologist.2015-0440 .
doi: 10.1634/theoncologist.2015-0440 pubmed: 27053504 pmcid: 4912364
Eales KL, Hollinshead KE, Tennant DA. Hypoxia and metabolic adaptation of cancer cells. Oncogenesis. 2016;5(1):e190. https://doi.org/10.1038/oncsis.2015.50 .
doi: 10.1038/oncsis.2015.50 pubmed: 26807645 pmcid: 4728679
Claesson-Welsh L, Welsh M. VEGFA and tumour angiogenesis. J Intern Med. 2013;273(2):114–127.  https://doi.org/10.1111/joim.12019 .
doi: 10.1111/joim.12019 pubmed: 23216836
Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407(6801):249–257.   https://doi.org/10.1038/35025220 .
doi: 10.1038/35025220 pubmed: 11001068
Lodhi T, Song YP, West C, Hoskin P, Choudhury A. Hypoxia and its modification in bladder cancer: current and future perspectives. Clin Oncol (R Coll Radiol). 2021;33(6):376–390.  https://doi.org/10.1016/j.clon.2021.03.001 .
doi: 10.1016/j.clon.2021.03.001 pubmed: 33762140
Bochner BH, Cote RJ, Weidner N, et al. Angiogenesis in bladder cancer: relationship between microvessel density and tumor prognosis. J Natl Cancer Inst. 1995;87(21):1603–1612. https://doi.org/10.1093/jnci/87.21.1603 .
doi: 10.1093/jnci/87.21.1603 pubmed: 7563203
Sato Y. Double-face of vasohibin-1 for the maintenance of vascular homeostasis and healthy longevity. J Atheroscler Thromb. 2018;25(6):461–466. https://doi.org/10.5551/jat.43398 .
doi: 10.5551/jat.43398 pubmed: 29398681 pmcid: 6005230
Watanabe K, Hasegawa Y, Yamashita H, et al. Vasohibin as an endothelium-derived negative feedback regulator of angiogenesis. J Clin Investig. 2004;114(7):898–907. https://doi.org/10.1172/JCI21152 .
doi: 10.1172/JCI21152 pubmed: 15467828 pmcid: 518662
Kimura H, Miyashita H, Suzuki Y, et al. Distinctive localization and opposed roles of vasohibin-1 and vasohibin-2 in the regulation of angiogenesis. Blood. 2009;113(19):4810–4818.  https://doi.org/10.1182/blood-2008-07-170316 .
doi: 10.1182/blood-2008-07-170316 pubmed: 19204325
Zhang B, Wu Z, Xie W, et al. The expression of vasohibin-1 and its prognostic significance in bladder cancer. Exp Ther Med. 2017;14(4):3477–3484. https://doi.org/10.3892/etm.2017.4969 .
doi: 10.3892/etm.2017.4969 pubmed: 29042936 pmcid: 5639433
Soukup V, Čapoun O, Cohen D, et al. Prognostic performance and reproducibility of the 1973 and 2004/2016 World Health Organization grading classification systems in non-muscle-invasive bladder cancer: A European Association of Urology non-muscle invasive bladder cancer guidelines panel systematic review. Eur Urol. 2017;72(5):801–813.   https://doi.org/10.1016/j.eururo.2017.04.015 .
doi: 10.1016/j.eururo.2017.04.015 pubmed: 28457661
Klatte T, Seligson DB, Rao J, et al. Carbonic anhydrase IX in bladder cancer: a diagnostic, prognostic, and therapeutic molecular marker. Cancer. 2009;115(7):1448–1458.   https://doi.org/10.1002/cncr.24163 .
doi: 10.1002/cncr.24163 pubmed: 19195047
Ziello JE, Jovin IS, Huang Y. Hypoxia-inducible factor (HIF)-1 regulatory pathway and its potential for therapeutic intervention in malignancy and ischemia. Yale J Biol Med. 2007;80(2):51–60.
pubmed: 18160990 pmcid: 2140184
Krock BL, Skuli N, Simon MC. Hypoxia-induced angiogenesis: good and evil. Genes Cancer. 2011;2(12):1117–1133. https://doi.org/10.1177/1947601911423654 .
doi: 10.1177/1947601911423654 pubmed: 22866203 pmcid: 3411127
Jain RK. Molecular regulation of vessel maturation. Nat Med. 2003;9(6):685–693. https://doi.org/10.1038/nm0603-685 .
doi: 10.1038/nm0603-685 pubmed: 12778167
Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 1996;86(3):353–364.   https://doi.org/10.1016/s0092-8674(00)80108-7 .
doi: 10.1016/s0092-8674(00)80108-7 pubmed: 8756718
Iessi E, Logozzi M, Mizzoni D, et al. Rethinking the combination of proton exchanger inhibitors in cancer therapy. Metabolites. 2017;8(1):2.  https://doi.org/10.3390/metabo8010002 .
doi: 10.3390/metabo8010002 pubmed: 29295495 pmcid: 5875992
Kolosenko I, Avnet S, Baldini N, Viklund J, De Milito A. Therapeutic implications of tumor interstitial acidification. Semin Cancer Biol. 2017;43:119–133.   https://doi.org/10.1016/j.semcancer.2017.01.008 .
doi: 10.1016/j.semcancer.2017.01.008 pubmed: 28188829
Huang J, Ma X, Chen X, et al. Microvessel density as a prognostic factor in bladder cancer: a systematic review of literature and meta-analysis. Cancer Biomark. 2014;14(6):505–514.   https://doi.org/10.3233/CBM-140417 .
doi: 10.3233/CBM-140417 pubmed: 25335742
Armulik A, Abramsson A, Betsholtz C. Endothelial/pericyte interactions. Circ Res. 2005;97(6):512–523.   https://doi.org/10.1161/01.RES.0000182903.16652.d7 .
doi: 10.1161/01.RES.0000182903.16652.d7 pubmed: 16166562
Kern J, Steurer M, Gastl G, Gunsilius E, Untergasser G. Vasohibin inhibits angiogenic sprouting in vitro and supports vascular maturation processes in vivo. BMC Cancer. 2009;9:284.  https://doi.org/10.1186/1471-2407-9-284 .
doi: 10.1186/1471-2407-9-284 pubmed: 19682397 pmcid: 2739223
Miyazaki Y, Kosaka T, Mikami S, et al. The prognostic significance of vasohibin-1 expression in patients with upper urinary tract urothelial carcinoma. Clin Cancer Res. 2012;18(15):4145–4153. https://doi.org/10.1158/1078-0432.CCR-12-0073 .
doi: 10.1158/1078-0432.CCR-12-0073 pubmed: 22675166
Todenhöfer T, Gibb EA, Seiler R, et al. Evaluation of carbonic anhydrase IX as a potential therapeutic target in urothelial carcinoma. Urol Oncol. 2021;39(8):498.e1–498.e11.  https://doi.org/10.1016/j.urolonc.2021.04.011 .
doi: 10.1016/j.urolonc.2021.04.011 pubmed: 34083096
Hoskin PJ, Sibtain A, Daley FM, Wilson GD. GLUT1 and CAIX as intrinsic markers of hypoxia in bladder cancer: relationship with vascularity and proliferation as predictors of outcome of ARCON. Br J Cancer. 2003;89(7):1290–1297.   https://doi.org/10.1038/sj.bjc.6601260 .
doi: 10.1038/sj.bjc.6601260 pubmed: 14520462 pmcid: 2394309
Feng Y, Wang D, Liu Y, Pang X, Zhang H. Serum levels of vasohibin-1 in type 2 diabetes mellitus patients with diabetic retinopathy. Eur J Ophthalmol. 2022;32(5):2864–2869. https://doi.org/10.1177/11206721211073403 .
doi: 10.1177/11206721211073403 pubmed: 35001686
Kuerer HM, Smith BD, Krishnamurthy S, et al. Eliminating breast surgery for invasive breast cancer in exceptional responders to neoadjuvant systemic therapy: a multicentre, single-arm, phase 2 trial. Lancet Oncol. 2022;23(12):1517–1524.  https://doi.org/10.1016/S1470-2045(22)00613-1 .
doi: 10.1016/S1470-2045(22)00613-1 pubmed: 36306810

Auteurs

Minami Omura (M)

Department of Urology, Keio University School of Medicine, Tokyo, Japan.

Takeo Kosaka (T)

Department of Urology, Keio University School of Medicine, Tokyo, Japan. Takemduro@gmail.com.

Hiroaki Kobayashi (H)

Department of Urology, Keio University School of Medicine, Tokyo, Japan.

Keisuke Shigeta (K)

Department of Urology, Kawasaki Municipal Hospital, Kanagawa, Japan.

Kazuhiro Matsumoto (K)

Department of Urology, Keio University School of Medicine, Tokyo, Japan.

Satoshi Hara (S)

Department of Urology, Kawasaki Municipal Hospital, Kanagawa, Japan.

Eiji Kikuchi (E)

Department of Urology, St. Marianna University School of Medicine, Kanagawa, Japan.

Shuji Mikami (S)

Department of Pathology, Keio University School of Medicine, Tokyo, Japan.

Hideyuki Saya (H)

Division of Gene Regulation, Institute for Advanced Medical Research, Graduate School of Medicine, Keio University, Tokyo, Japan.

Yasufumi Sato (Y)

Department of Vascular Biology, Institute of Development, Aging and Cancer, Tohoku University, Miyagi, Japan.

Mototsugu Oya (M)

Department of Urology, Keio University School of Medicine, Tokyo, Japan.

Classifications MeSH