Hypoxia in the Initiation and Progression of Neuroblastoma Tumours

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2019 Dec 22

PMID 31861671

Citations 16

Authors

Carlos Huertas-Castano

Maria A Gomez-Munoz

Ricardo Pardal

Francisco M Vega

Affiliations

Soon will be listed here.

Abstract

Neuroblastoma is the most frequent extracranial solid tumour in children, causing 10% of all paediatric oncology deaths. It arises in the embryonic neural crest due to an uncontrolled behaviour of sympathetic nervous system progenitors, giving rise to heterogeneous tumours. Low local or systemic tissue oxygen concentration has emerged as a cellular stimulus with important consequences for tumour initiation, evolution and progression. In neuroblastoma, several evidences point towards a role of hypoxia in tumour initiation during development, tumour cell differentiation, survival and metastatic spreading. However, the heterogeneous nature of the disease, its developmental origin and the lack of suitable experimental models have complicated a clear understanding of the effect of hypoxia in neuroblastoma tumour progression and the molecular mechanisms implicated. In this review, we have compiled available evidences to try to shed light onto this important field. In particular, we explore the effect of hypoxia in neuroblastoma cell transformation and differentiation. We also discuss the experimental models available and the emerging alternatives to study this problem, and we present hypoxia-related therapeutic avenues being explored in the field.

Citing Articles

Emerging Trends in Neuroblastoma Diagnosis, Therapeutics, and Research.

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Neuroblastoma-derived hypoxic extracellular vesicles promote metastatic dissemination in a zebrafish model.

Fietta A, Fusco P, Germano G, Micheli S, Sorgato M, Lucchetta G PLoS One. 2024; 19(12):e0316103.

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BAP31 Promotes Angiogenesis via Galectin-3 Upregulation in Neuroblastoma.

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Enhancing the sensitization of neuroblastoma to radiotherapy by the construction of a dual-channel parallel free radicals nanoamplifier.

Zhang W, Li X, Zeng J, Wen X, Zhang C, Zhang Y Mater Today Bio. 2023; 23:100828.

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References

Cantilena S, Pastorino F, Pezzolo A, Chayka O, Pistoia V, Ponzoni M . Frizzled receptor 6 marks rare, highly tumourigenic stem-like cells in mouse and human neuroblastomas. Oncotarget. 2012; 2(12):976-83. PMC: 3282103. DOI: 10.18632/oncotarget.410. View

van Houdt I, Oudejans J, van den Eertwegh A, Baars A, Vos W, Bladergroen B . Expression of the apoptosis inhibitor protease inhibitor 9 predicts clinical outcome in vaccinated patients with stage III and IV melanoma. Clin Cancer Res. 2005; 11(17):6400-7. DOI: 10.1158/1078-0432.CCR-05-0306. View

Cimmino F, Pezone L, Avitabile M, Acierno G, Andolfo I, Capasso M . Inhibition of hypoxia inducible factors combined with all-trans retinoic acid treatment enhances glial transdifferentiation of neuroblastoma cells. Sci Rep. 2015; 5:11158. PMC: 4460899. DOI: 10.1038/srep11158. View

Nieminen A, Qanungo S, Schneider E, Jiang B, Agani F . Mdm2 and HIF-1alpha interaction in tumor cells during hypoxia. J Cell Physiol. 2005; 204(2):364-9. DOI: 10.1002/jcp.20406. View

Krawczyk E, Hong S, Galli S, Trinh E, Wietlisbach L, Misiukiewicz S . Murine neuroblastoma cell lines developed by conditional reprogramming preserve heterogeneous phenotypes observed in vivo. Lab Invest. 2019; 100(1):38-51. PMC: 6920526. DOI: 10.1038/s41374-019-0297-7. View

Ognibene M, Cangelosi D, Morini M, Segalerba D, Bosco M, Sementa A . Immunohistochemical analysis of PDK1, PHD3 and HIF-1α expression defines the hypoxic status of neuroblastoma tumors. PLoS One. 2017; 12(11):e0187206. PMC: 5678880. DOI: 10.1371/journal.pone.0187206. View

Covello K, Kehler J, Yu H, Gordan J, Arsham A, Hu C . HIF-2alpha regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev. 2006; 20(5):557-70. PMC: 1410808. DOI: 10.1101/gad.1399906. View

Chuen Choi S, Lin D, Gout P, Collins C, Xu Y, Wang Y . Lessons from patient-derived xenografts for better in vitro modeling of human cancer. Adv Drug Deliv Rev. 2014; 79-80:222-37. DOI: 10.1016/j.addr.2014.09.009. View

Skuli N, Monferran S, Delmas C, Lajoie-Mazenc I, Favre G, Toulas C . Activation of RhoB by hypoxia controls hypoxia-inducible factor-1alpha stabilization through glycogen synthase kinase-3 in U87 glioblastoma cells. Cancer Res. 2006; 66(1):482-9. DOI: 10.1158/0008-5472.CAN-05-2299. View

10.

Boeva V, Louis-Brennetot C, Peltier A, Durand S, Pierre-Eugene C, Raynal V . Heterogeneity of neuroblastoma cell identity defined by transcriptional circuitries. Nat Genet. 2017; 49(9):1408-1413. DOI: 10.1038/ng.3921. View

11.

Poomthavorn P, Wong S, Higgins S, Werther G, Russo V . Activation of a prometastatic gene expression program in hypoxic neuroblastoma cells. Endocr Relat Cancer. 2009; 16(3):991-1004. DOI: 10.1677/ERC-08-0340. View

12.

Bishop T, Gallagher D, Pascual A, Lygate C, de Bono J, Nicholls L . Abnormal sympathoadrenal development and systemic hypotension in PHD3-/- mice. Mol Cell Biol. 2008; 28(10):3386-400. PMC: 2423159. DOI: 10.1128/MCB.02041-07. View

13.

Zaatiti H, Abdallah J, Nasr Z, Khazen G, Sandler A, Abou-Antoun T . Tumorigenic proteins upregulated in the MYCN-amplified IMR-32 human neuroblastoma cells promote proliferation and migration. Int J Oncol. 2018; 52(3):787-803. PMC: 5807036. DOI: 10.3892/ijo.2018.4236. View

14.

Jogi A, Ora I, Nilsson H, Lindeheim A, Makino Y, Poellinger L . Hypoxia alters gene expression in human neuroblastoma cells toward an immature and neural crest-like phenotype. Proc Natl Acad Sci U S A. 2002; 99(10):7021-6. PMC: 124521. DOI: 10.1073/pnas.102660199. View

15.

Patterson D, Gao D, Trahan D, Johnson B, Ludwig A, Barbieri E . Effect of MDM2 and vascular endothelial growth factor inhibition on tumor angiogenesis and metastasis in neuroblastoma. Angiogenesis. 2011; 14(3):255-66. DOI: 10.1007/s10456-011-9210-8. View

16.

Thienpont B, Steinbacher J, Zhao H, DAnna F, Kuchnio A, Ploumakis A . Tumour hypoxia causes DNA hypermethylation by reducing TET activity. Nature. 2016; 537(7618):63-68. PMC: 5133388. DOI: 10.1038/nature19081. View

17.

Cohn S, Pearson A, London W, Monclair T, Ambros P, Brodeur G . The International Neuroblastoma Risk Group (INRG) classification system: an INRG Task Force report. J Clin Oncol. 2008; 27(2):289-97. PMC: 2650388. DOI: 10.1200/JCO.2008.16.6785. View

18.

Dubois S, Kalika Y, Lukens J, Brodeur G, Seeger R, Atkinson J . Metastatic sites in stage IV and IVS neuroblastoma correlate with age, tumor biology, and survival. J Pediatr Hematol Oncol. 1999; 21(3):181-9. DOI: 10.1097/00043426-199905000-00005. View

19.

Baek J, Jang J, Kang C, Chung H, Kim N, Kim K . Hypoxia-induced VEGF enhances tumor survivability via suppression of serum deprivation-induced apoptosis. Oncogene. 2000; 19(40):4621-31. DOI: 10.1038/sj.onc.1203814. View

20.

Yin C, Guan S, Zhang B, Wang X, Yue S . Upregulation of HIF-1α protects neuroblastoma cells from hypoxia-induced apoptosis in a RhoA-dependent manner. Mol Med Rep. 2015; 12(5):7123-31. DOI: 10.3892/mmr.2015.4267. View