Skip to main content
Top
Published in: Cancer and Metastasis Reviews 4/2022

01-12-2022 | Prostate Cancer | Non-Thematic Review

The vulnerable primed cancer stem cells in disguise: demystifying the role of Maspin

Authors: Shijie Sheng, Margarida Bernardo, Sijana H. Dzinic, Kang Chen, Wael A. Sakr

Published in: Cancer and Metastasis Reviews | Issue 4/2022

Login to get access

Abstract

Epithelial-specific Maspin is widely known as a tumor suppressor. However, while the level of maspin expression is inversely correlated with tumor grade and stage, emerging clinical evidence shows a correlation between seemingly better differentiated tumor cells that express Maspin in both the nucleus and the cytoplasm, (n + c)Maspin, with a poor prognosis of many types of cancer. Biological studies demonstrate that Maspin plays an essential role in stem cell differentiation. In light of the recently established characterization of primed stem cells (P-SCs) in development, we propose, for the first time, that cancer stem cells (CSCs) also need to undergo priming (P-CSCs) before their transition to various progeny phenotypes. We envisage major differences in the steady state kinetics between P-SCs and P-CSCs. We further propose that P-CSCs of carcinoma are both marked and regulated by (n + c)Maspin. The concept of P-CSCs helps explain the apparent dichotomous relationships of (n + c)Maspin expression with cancer diagnosis and prognosis, and is supported by the evidence from mechanistic studies. We believe that the potential utility of (n + c)Maspin as a molecular marker of P-CSCs may significantly accelerate the advancement in our understanding of the genesis of tumor phenotypic plasticity in response to changes of tumor microenvironments (TME) or drug treatments. The vulnerabilities of the cellular state of (n + c)Maspin-expressing P-CSCs are also discussed as the rationale for future development of P-CSC-targeted chemotherapeutic and immunotherapeutic strategies.
Literature
6.
go back to reference A.K. Sood, A. K., Fletcher, M. S., Gruman, L. M., Coffin, J. E., Jabbari, S., Khalkhali-Ellis, Z., Arbour, N., Seftor, E. A., & Hendrix, M. J. (2002). The paradoxical expression of maspin in ovarian carcinoma. Clinical Cancer Research, 8(4), 2924–2932. A.K. Sood, A. K., Fletcher, M. S., Gruman, L. M., Coffin, J. E., Jabbari, S., Khalkhali-Ellis, Z., Arbour, N., Seftor, E. A., & Hendrix, M. J. (2002). The paradoxical expression of maspin in ovarian carcinoma. Clinical Cancer Research, 8(4), 2924–2932.
8.
go back to reference Carozzi, F., Tamburrino, L., Bisanzi, S., Marchiani, S., Paglierani, M., Di Lollo, S., Crocetti, E., Buzzoni, C., Burroni, E., Greco, L., Baldi, E., & Sani, C. (2016). Are biomarkers evaluated in biopsy specimens predictive of prostate cancer aggressiveness? Journal of Cancer Research and Clinical Oncology, 142(1), 201–212. https://doi.org/10.1007/s00432-015-2015-1CrossRef Carozzi, F., Tamburrino, L., Bisanzi, S., Marchiani, S., Paglierani, M., Di Lollo, S., Crocetti, E., Buzzoni, C., Burroni, E., Greco, L., Baldi, E., & Sani, C. (2016). Are biomarkers evaluated in biopsy specimens predictive of prostate cancer aggressiveness? Journal of Cancer Research and Clinical Oncology, 142(1), 201–212. https://​doi.​org/​10.​1007/​s00432-015-2015-1CrossRef
9.
go back to reference Chim, S. S., Tong, Y. K., Chiu, R. W., Lau, T. K., Leung, T. N., Chan, L. Y., Oudejans, C. B., Ding, C., & Lo, Y. M. (2005). Detection of the placental epigenetic signature of the maspin gene in maternal plasma. Proceedings of the National Academy of Sciences of the USA, 102(41), 14753–14758. https://doi.org/10.1073/pnas.0503335102CrossRef Chim, S. S., Tong, Y. K., Chiu, R. W., Lau, T. K., Leung, T. N., Chan, L. Y., Oudejans, C. B., Ding, C., & Lo, Y. M. (2005). Detection of the placental epigenetic signature of the maspin gene in maternal plasma. Proceedings of the National Academy of Sciences of the USA, 102(41), 14753–14758. https://​doi.​org/​10.​1073/​pnas.​0503335102CrossRef
10.
go back to reference Huang, Y., Cai, L. W., & Yang, R. (2012). Expression of maspin in the early pregnant mouse endometrium and its role during embryonic implantation. Comparative Medicine, 62(3), 179–184. Huang, Y., Cai, L. W., & Yang, R. (2012). Expression of maspin in the early pregnant mouse endometrium and its role during embryonic implantation. Comparative Medicine, 62(3), 179–184.
12.
go back to reference Dzinic, S. H., Bernardo, M. M., Li, X., Fernandez-Valdivia, R., Ho, Y. S., Mi, Q. S., Bandyopadhyay, S., Lonardo, F., Vranic, S., Oliveira, D. S., Bonfil, R. D., Dyson, G., Chen, K., Omerovic, A., Sheng, X., Han, X., Wu, D., Bi, X., Cabaravdic, D., … Sheng, S. (2017). An essential role of maspin in embryogenesis and tumor suppression. Cancer Research, 77(4), 886–896. https://doi.org/10.1158/0008-5472.CAN-16-2219CrossRef Dzinic, S. H., Bernardo, M. M., Li, X., Fernandez-Valdivia, R., Ho, Y. S., Mi, Q. S., Bandyopadhyay, S., Lonardo, F., Vranic, S., Oliveira, D. S., Bonfil, R. D., Dyson, G., Chen, K., Omerovic, A., Sheng, X., Han, X., Wu, D., Bi, X., Cabaravdic, D., … Sheng, S. (2017). An essential role of maspin in embryogenesis and tumor suppression. Cancer Research, 77(4), 886–896. https://​doi.​org/​10.​1158/​0008-5472.​CAN-16-2219CrossRef
14.
go back to reference Centonze, A., Lin, S., Tika, E., Sifrim, A., Fioramonti, M., Malfait, M., Song, Y., Wuidart, A., Van Herck, J., Dannau, A., Bouvencourt, G., Dubois, C., Dedoncker, N., Sahay, A., de Maertelaer, V., Siebel, C. W., Van Keymeulen, A., Voet, T., & Blanpain, C. (2020). Heterotypic cell-cell communication regulates glandular stem cell multipotency. Nature, 584(7822), 608–613. https://doi.org/10.1038/s41586-020-2632-yCrossRef Centonze, A., Lin, S., Tika, E., Sifrim, A., Fioramonti, M., Malfait, M., Song, Y., Wuidart, A., Van Herck, J., Dannau, A., Bouvencourt, G., Dubois, C., Dedoncker, N., Sahay, A., de Maertelaer, V., Siebel, C. W., Van Keymeulen, A., Voet, T., & Blanpain, C. (2020). Heterotypic cell-cell communication regulates glandular stem cell multipotency. Nature, 584(7822), 608–613. https://​doi.​org/​10.​1038/​s41586-020-2632-yCrossRef
15.
go back to reference Dzinic, S. H., Mahdi, Z., Bernardo, M. M., Vranic, S., Beydoun, H., Nahra, N., Alijagic, A., Harajli, D., Pang, A., Saliganan, D. M., Rahman, A. M., Skenderi, F., Hasanbegovic, B., Dyson, G., Beydoun, R., & Sheng, S. (2019). Maspin differential expression patterns as a potential marker for targeted screening of esophageal adenocarcinoma/gastroesophageal junction adenocarcinoma. PLoS ONE, 14(4), e0215089. https://doi.org/10.1371/journal.pone.0215089CrossRef Dzinic, S. H., Mahdi, Z., Bernardo, M. M., Vranic, S., Beydoun, H., Nahra, N., Alijagic, A., Harajli, D., Pang, A., Saliganan, D. M., Rahman, A. M., Skenderi, F., Hasanbegovic, B., Dyson, G., Beydoun, R., & Sheng, S. (2019). Maspin differential expression patterns as a potential marker for targeted screening of esophageal adenocarcinoma/gastroesophageal junction adenocarcinoma. PLoS ONE, 14(4), e0215089. https://​doi.​org/​10.​1371/​journal.​pone.​0215089CrossRef
16.
go back to reference Umekita, Y., Ohi, Y., Souda, M., Rai, Y., Sagara, Y., Sagara, Y., Tamada, S., A., & Tanimoto, A. (2011). Maspin expression is frequent and correlates with basal markers in triple-negative breast cancer, Diagnostic Pathology, 6, 36. https://doi.org/10.1186/1746-1596-6-36. Umekita, Y., Ohi, Y., Souda, M., Rai, Y., Sagara, Y., Sagara, Y., Tamada, S., A., & Tanimoto, A. (2011). Maspin expression is frequent and correlates with basal markers in triple-negative breast cancer, Diagnostic Pathology, 6, 36. https://​doi.​org/​10.​1186/​1746-1596-6-36.
18.
go back to reference Zou, Z., Zhang, W., Young, D., Gleave, M. G., Rennie, P., Connell, T., Connelly, R., Moul, J., Srivastava, S., & Sesterhenn, I. (2002). Maspin expression profile in human prostate cancer (CaP) and in vitro induction of Maspin expression by androgen ablation. Clinical Cancer Research, 8(5), 1172–1177. Zou, Z., Zhang, W., Young, D., Gleave, M. G., Rennie, P., Connell, T., Connelly, R., Moul, J., Srivastava, S., & Sesterhenn, I. (2002). Maspin expression profile in human prostate cancer (CaP) and in vitro induction of Maspin expression by androgen ablation. Clinical Cancer Research, 8(5), 1172–1177.
21.
26.
go back to reference Cao, D., Wilentz, R. E., Abbruzzese, J. L., Ho, L., & Maitra, A. (2005). Aberrant expression of maspin in idiopathic inflammatory bowel disease is associated with disease activity and neoplastic transformation. International Journal of Gastrointestinal Cancer, 36(1), 39–46. https://doi.org/10.1385/IJGC:36:1:039CrossRef Cao, D., Wilentz, R. E., Abbruzzese, J. L., Ho, L., & Maitra, A. (2005). Aberrant expression of maspin in idiopathic inflammatory bowel disease is associated with disease activity and neoplastic transformation. International Journal of Gastrointestinal Cancer, 36(1), 39–46. https://​doi.​org/​10.​1385/​IJGC:​36:​1:​039CrossRef
29.
go back to reference Murakami, K., Gunesdogan, U., Zylicz, J. J., Tang, W. W. C., Sengupta, R., Kobayashi, T., Kim, S., Butler, R., Dietmann, S., & Surani, M. A. (2016). NANOG alone induces germ cells in primed epiblast in vitro by activation of enhancers. Nature, 529(7586), 403–407. https://doi.org/10.1038/nature16480CrossRef Murakami, K., Gunesdogan, U., Zylicz, J. J., Tang, W. W. C., Sengupta, R., Kobayashi, T., Kim, S., Butler, R., Dietmann, S., & Surani, M. A. (2016). NANOG alone induces germ cells in primed epiblast in vitro by activation of enhancers. Nature, 529(7586), 403–407. https://​doi.​org/​10.​1038/​nature16480CrossRef
34.
35.
go back to reference Giaginis, C., Alexandrou, P., Delladetsima, I., Giannopoulou, I., Patsouris, E., & Theocharis, S. (2014). Clinical significance of histone deacetylase (HDAC)-1, HDAC-2, HDAC-4, and HDAC-6 expression in human malignant and benign thyroid lesions. Tumour Biology, 35(1), 61–71. https://doi.org/10.1007/s13277-013-1007-5CrossRef Giaginis, C., Alexandrou, P., Delladetsima, I., Giannopoulou, I., Patsouris, E., & Theocharis, S. (2014). Clinical significance of histone deacetylase (HDAC)-1, HDAC-2, HDAC-4, and HDAC-6 expression in human malignant and benign thyroid lesions. Tumour Biology, 35(1), 61–71. https://​doi.​org/​10.​1007/​s13277-013-1007-5CrossRef
36.
go back to reference Su, J. M., Hsu, Y. Y., Lin, P., & Chang, H. (2016). Nuclear accumulation of heat-shock protein 90 is associated with poor survival and metastasis in patients with non-small cell lung cancer. Anticancer Research, 36(5), 2197–2203. Su, J. M., Hsu, Y. Y., Lin, P., & Chang, H. (2016). Nuclear accumulation of heat-shock protein 90 is associated with poor survival and metastasis in patients with non-small cell lung cancer. Anticancer Research, 36(5), 2197–2203.
39.
go back to reference Law, R. H., Irving, J. A., Buckle, A. M., Ruzyla, K., Buzza, M., Bashtannyk-Puhalovich, T. A., Beddoe, T. C., Nguyen, K., Worrall, D. M., Bottomley, S. P., Bird, P. I., Rossjohn, J., & Whisstock, J. C. (2005). The high resolution crystal structure of the human tumor suppressor maspin reveals a novel conformational switch in the G-helix. Journal of Biological Chemistry, 280(23), 22356–22364. https://doi.org/10.1074/jbc.M412043200CrossRef Law, R. H., Irving, J. A., Buckle, A. M., Ruzyla, K., Buzza, M., Bashtannyk-Puhalovich, T. A., Beddoe, T. C., Nguyen, K., Worrall, D. M., Bottomley, S. P., Bird, P. I., Rossjohn, J., & Whisstock, J. C. (2005). The high resolution crystal structure of the human tumor suppressor maspin reveals a novel conformational switch in the G-helix. Journal of Biological Chemistry, 280(23), 22356–22364. https://​doi.​org/​10.​1074/​jbc.​M412043200CrossRef
40.
go back to reference Sheng, S., Truong, B., Fredrickson, D., Wu, R., Pardee, A. B., & R. Sager, R. (1998).Tissue-type plasminogen activator is a target of the tumor suppressor gene maspin. Proceedings of the National Academy of Sciences of the USA, 95(2), 499-504.https://doi.org/10.1073/pnas.95.2.499. Sheng, S., Truong, B., Fredrickson, D., Wu, R., Pardee, A. B., & R. Sager, R. (1998).Tissue-type plasminogen activator is a target of the tumor suppressor gene maspin. Proceedings of the National Academy of Sciences of the USA, 95(2), 499-504.https://​doi.​org/​10.​1073/​pnas.​95.​2.​499.
41.
go back to reference Biliran, H. Jr., & Sheng, S. (2001). Pleiotrophic inhibition of pericellular urokinase-type plasminogen activator system by endogenous tumor suppressive maspin. Cancer Research, 61(24) 8676–8682. Biliran, H. Jr., & Sheng, S. (2001). Pleiotrophic inhibition of pericellular urokinase-type plasminogen activator system by endogenous tumor suppressive maspin. Cancer Research, 61(24) 8676–8682.
42.
go back to reference McGowen, R., Biliran, H. Jr., Sager, R., & Sheng, S. (2000). The surface of prostate carcinoma DU145 cells mediates the inhibition of urokinase-type plasminogen activator by maspin. Cancer Research, 60(17), 4771–4778. McGowen, R., Biliran, H. Jr., Sager, R., & Sheng, S. (2000). The surface of prostate carcinoma DU145 cells mediates the inhibition of urokinase-type plasminogen activator by maspin. Cancer Research, 60(17), 4771–4778.
43.
go back to reference Yin, S., Lockett, J., Meng, Y., Biliran, H. Jr., Blouse, G. E., Li, X., Reddy, N., Zhao, Z., Lin, X., Anagli, J., Cher, M. L., & Sheng, S. (2006). Maspin retards cell detachment via a novel interaction with the urokinase-type plasminogen activator/urokinase-type plasminogen activator receptor system. Cancer Research, 66(8) 4173–4181. https://doi.org/10.1158/0008-5472.CAN-05-3514. Yin, S., Lockett, J., Meng, Y., Biliran, H. Jr., Blouse, G. E., Li, X., Reddy, N., Zhao, Z., Lin, X., Anagli, J., Cher, M. L., & Sheng, S. (2006). Maspin retards cell detachment via a novel interaction with the urokinase-type plasminogen activator/urokinase-type plasminogen activator receptor system. Cancer Research, 66(8) 4173–4181. https://​doi.​org/​10.​1158/​0008-5472.​CAN-05-3514.
46.
go back to reference Bernardo, M. M., Meng, Y., Lockett, J., Dyson, G., Dombkowski, A., Kaplun, A., Li, X., Yin, S., Dzinic, S., Olive, M., Dean, I., Krass, D., Moin, K., Bonfil, R. D., Cher, M., Sakr, W., & Sheng, S. (2011). Maspin reprograms the gene expression profile of prostate carcinoma cells for differentiation. Genes & Cancer, 2(11), 1009–1022. https://doi.org/10.1177/1947601912440170CrossRef Bernardo, M. M., Meng, Y., Lockett, J., Dyson, G., Dombkowski, A., Kaplun, A., Li, X., Yin, S., Dzinic, S., Olive, M., Dean, I., Krass, D., Moin, K., Bonfil, R. D., Cher, M., Sakr, W., & Sheng, S. (2011). Maspin reprograms the gene expression profile of prostate carcinoma cells for differentiation. Genes & Cancer, 2(11), 1009–1022. https://​doi.​org/​10.​1177/​1947601912440170​CrossRef
48.
go back to reference Yin, S. P., Li, X. H., Meng, Y. H., Finley, R. L., Sakr, W., Yang, H., Reddy, N., & Sheng, S. J. (2005). Tumor-suppressive maspin regulates cell response to oxidative stress by direct interaction with glutathione S-transferase. Journal of Biological Chemistry, 280(41), 34985–34996. https://doi.org/10.1074/jbc.M503522200CrossRef Yin, S. P., Li, X. H., Meng, Y. H., Finley, R. L., Sakr, W., Yang, H., Reddy, N., & Sheng, S. J. (2005). Tumor-suppressive maspin regulates cell response to oxidative stress by direct interaction with glutathione S-transferase. Journal of Biological Chemistry, 280(41), 34985–34996. https://​doi.​org/​10.​1074/​jbc.​M503522200CrossRef
50.
go back to reference Goldstein, A. S., Lawson, D. A., Cheng, D., Sun, W., Garraway, I. P., & Witte, O. N. (2008). Trop2 identifies a subpopulation of murine and human prostate basal cells with stem cell characteristics. Proceedings of the National Academy of Sciences of the USA, 105(52), 20882–20887. https://doi.org/10.1073/pnas.0811411106CrossRef Goldstein, A. S., Lawson, D. A., Cheng, D., Sun, W., Garraway, I. P., & Witte, O. N. (2008). Trop2 identifies a subpopulation of murine and human prostate basal cells with stem cell characteristics. Proceedings of the National Academy of Sciences of the USA, 105(52), 20882–20887. https://​doi.​org/​10.​1073/​pnas.​0811411106CrossRef
51.
go back to reference Bernardo, M. M., Kaplun, A., Dzinic, S. H., Li, X., Irish, J., Mujagic, A., Jakupovic, B., Back, J. B., Van Buren, E., Han, X., Dean, I., Chen, Y. Q., Heath, E., Sakr, W., & Sheng, S. (2015). Maspin expression in prostatetumor cells averts stemness and stratifies drug sensitivity. Cancer Research, 75(18), 3970–3979. https://doi.org/10.1158/0008-5472.CAN-15-0234CrossRef Bernardo, M. M., Kaplun, A., Dzinic, S. H., Li, X., Irish, J., Mujagic, A., Jakupovic, B., Back, J. B., Van Buren, E., Han, X., Dean, I., Chen, Y. Q., Heath, E., Sakr, W., & Sheng, S. (2015). Maspin expression in prostatetumor cells averts stemness and stratifies drug sensitivity. Cancer Research, 75(18), 3970–3979. https://​doi.​org/​10.​1158/​0008-5472.​CAN-15-0234CrossRef
52.
go back to reference Cher, M. L., Biliran, H. R., Jr., Bhagat, S., Meng, Y., Che, M., Lockett, J., Abrams, J., Fridman, R., Zachareas, M., & Sheng, S. (2003). Maspin expression inhibits osteolysis, tumor growth, and angiogenesis in a model of prostate cancer bone metastasis. Proceedings of the National Academy of Sciences of the USA, 100(13), 7847–7852. https://doi.org/10.1073/pnas.1331360100CrossRef Cher, M. L., Biliran, H. R., Jr., Bhagat, S., Meng, Y., Che, M., Lockett, J., Abrams, J., Fridman, R., Zachareas, M., & Sheng, S. (2003). Maspin expression inhibits osteolysis, tumor growth, and angiogenesis in a model of prostate cancer bone metastasis. Proceedings of the National Academy of Sciences of the USA, 100(13), 7847–7852. https://​doi.​org/​10.​1073/​pnas.​1331360100CrossRef
53.
go back to reference Dzinic, S. H., Chen, K., Thakur, A., Kaplun, A., Bonfil, R. D., Li, X., Liu, J., Bernardo, M. M., Saliganan, A., Back, J. B., Yano, H., Schalk, D. L., Tomaszewski, E. N., Beydoun, A. S., Dyson, G., Mujagic, A., Krass, D., Dean, I., Mi, Q. S., Heath, E., Sakr, W., Lum, L. G., & Sheng, S. (2014). Maspin expression in prostate tumor elicits host anti-tumor immunity. Oncotarget, 5(22), 11225–11236. https://doi.org/10.18632/oncotarget.2615. Dzinic, S. H., Chen, K., Thakur, A., Kaplun, A., Bonfil, R. D., Li, X., Liu, J., Bernardo, M. M., Saliganan, A., Back, J. B., Yano, H., Schalk, D. L., Tomaszewski, E. N., Beydoun, A. S., Dyson, G., Mujagic, A., Krass, D., Dean, I., Mi, Q. S., Heath, E., Sakr, W., Lum, L. G., & Sheng, S. (2014). Maspin expression in prostate tumor elicits host anti-tumor immunity. Oncotarget, 5(22), 11225–11236. https://​doi.​org/​10.​18632/​oncotarget.​2615.
55.
go back to reference Bascones-Martinez, A., Lopez-Duran, M., Cano-Sanchez, J., Sanchez-Verde, L., Diez-Rodriguez, A., Aguirre-Echebarria, P., Alvarez-Fernandez, E., Gonzalez-Moles, M. A., Bascones-Ilundain, J., Muzio, L. L., & Campo-Trapero, J. (2012). Differences in the expression of five senescence markers in oral cancer, oral leukoplakia and control samples in humans. Oncology Letters, 3(6), 1319–1325. https://doi.org/10.3892/ol.2012.649CrossRef Bascones-Martinez, A., Lopez-Duran, M., Cano-Sanchez, J., Sanchez-Verde, L., Diez-Rodriguez, A., Aguirre-Echebarria, P., Alvarez-Fernandez, E., Gonzalez-Moles, M. A., Bascones-Ilundain, J., Muzio, L. L., & Campo-Trapero, J. (2012). Differences in the expression of five senescence markers in oral cancer, oral leukoplakia and control samples in humans. Oncology Letters, 3(6), 1319–1325. https://​doi.​org/​10.​3892/​ol.​2012.​649CrossRef
62.
go back to reference Berner, F., Bomze, D., Diem, S., Ali, O. H., Fassler, M., Ring, S., Niederer, R., Ackermann, C. J., Baumgaertner, P., Pikor, N., Cruz, C. G., van de Veen, W., Akdis, M., Nikolaev, S., Laubli, H., Zippelius, A., Hartmann, F., Cheng, H. W., Honger, G., … Flatz, L. (2019). Association of Checkpoint Inhibitor-Induced Toxic Effects With Shared Cancer and Tissue Antigens in Non-Small Cell Lung Cancer. JAMA Oncology, 5(7), 1–6. https://doi.org/10.1001/jamaoncol.2019.0402CrossRef Berner, F., Bomze, D., Diem, S., Ali, O. H., Fassler, M., Ring, S., Niederer, R., Ackermann, C. J., Baumgaertner, P., Pikor, N., Cruz, C. G., van de Veen, W., Akdis, M., Nikolaev, S., Laubli, H., Zippelius, A., Hartmann, F., Cheng, H. W., Honger, G., … Flatz, L. (2019). Association of Checkpoint Inhibitor-Induced Toxic Effects With Shared Cancer and Tissue Antigens in Non-Small Cell Lung Cancer. JAMA Oncology, 5(7), 1–6. https://​doi.​org/​10.​1001/​jamaoncol.​2019.​0402CrossRef
63.
go back to reference Kantoff, P. W., Higano, C. S., Shore, N. D., Berger, E. R., Small, E. J., Penson, D. F., Redfern, C. H., Ferrari, A. C., Dreicer, R., Sims, R. B., Xu, Y., Frohlich, M. W., Schellhammer, P. F., & Impact Study Investigators. (2010). Sipuleucel-T immunotherapy for castration-resistant prostate cancer. The New England Journal of Medicine, 363(5), 411-422. https://doi.org/10.1056/NEJMoa1001294. Kantoff, P. W., Higano, C. S., Shore, N. D., Berger, E. R., Small, E. J., Penson, D. F., Redfern, C. H., Ferrari, A. C., Dreicer, R., Sims, R. B., Xu, Y., Frohlich, M. W., Schellhammer, P. F., & Impact Study Investigators. (2010). Sipuleucel-T immunotherapy for castration-resistant prostate cancer. The New England Journal of Medicine, 363(5), 411-422. https://​doi.​org/​10.​1056/​NEJMoa1001294.
64.
go back to reference Thakur, A., Lum, L. G., Hwang, C., Paller, C. J., Schalk, D. L., Kondadasular, V., Heilrun, L. K., & Heath, E.I. (2017). Immune evaluation study of sipuleucel-T (Sip-T) in African-American and European-American men with castration-resistant prostate cancer. Journal of Clinical Oncology, 35(Supplement S6), 206. https://doi.org/10.1200/JCO.2017.35.6_suppl.206 Thakur, A., Lum, L. G., Hwang, C., Paller, C. J., Schalk, D. L., Kondadasular, V., Heilrun, L. K., & Heath, E.I. (2017). Immune evaluation study of sipuleucel-T (Sip-T) in African-American and European-American men with castration-resistant prostate cancer. Journal of Clinical Oncology, 35(Supplement S6), 206. https://​doi.​org/​10.​1200/​JCO.​2017.​35.​6_​suppl.​206
65.
go back to reference Gulley, J. L., Madan, R. A., Pachynski, R., Mulders, P., Sheikh, N. A., Trager, J., & Drake, C. G. (2017). Role of antigen spread and distinctive characteristics of immunotherapy in cancer treatment. Journal of the National Cancer Institute, 109(4), djw261. https://doi.org/10.1093/jnci/djw261. Gulley, J. L., Madan, R. A., Pachynski, R., Mulders, P., Sheikh, N. A., Trager, J., & Drake, C. G. (2017). Role of antigen spread and distinctive characteristics of immunotherapy in cancer treatment. Journal of the National Cancer Institute, 109(4), djw261. https://​doi.​org/​10.​1093/​jnci/​djw261.
67.
go back to reference Dean, I., Dzinic, S. H., Bernardo, M. M., Zou, Y., Kimler, V., Li, X., Kaplun, A., Granneman, J., Mao, G., & S. Sheng, S. (2017). The secretion and biological function of tumor suppressor maspin as an exosome cargo protein. Oncotarget, 8 (2017 5) 8043–8056. https://doi.org/10.18632/oncotarget.13302. Dean, I., Dzinic, S. H., Bernardo, M. M., Zou, Y., Kimler, V., Li, X., Kaplun, A., Granneman, J., Mao, G., & S. Sheng, S. (2017). The secretion and biological function of tumor suppressor maspin as an exosome cargo protein. Oncotarget, 8 (2017 5) 8043–8056. https://​doi.​org/​10.​18632/​oncotarget.​13302.
Metadata
Title
The vulnerable primed cancer stem cells in disguise: demystifying the role of Maspin
Authors
Shijie Sheng
Margarida Bernardo
Sijana H. Dzinic
Kang Chen
Wael A. Sakr
Publication date
01-12-2022
Publisher
Springer US
Published in
Cancer and Metastasis Reviews / Issue 4/2022
Print ISSN: 0167-7659
Electronic ISSN: 1573-7233
DOI
https://doi.org/10.1007/s10555-022-10070-2

Other articles of this Issue 4/2022

Cancer and Metastasis Reviews 4/2022 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