Engineering Micro Oxygen Factories to Slow Tumour Progression Via Hyperoxic Microenvironments

Overview

Journal Nat Commun

Specialty Biology

Date 2022 Aug 2

PMID 35918337

Authors

Weili Wang

Huizhen Zheng

Jun Jiang

Zhi Li

Dongpeng Jiang

Xiangru Shi

Hui Wang

Jie Jiang

Qianqian Xie

Meng Gao

Jianhong Chu

Xiaoming Cai

Tian Xia

Ruibin Li

Affiliations

Soon will be listed here.

Abstract

While hypoxia promotes carcinogenesis, tumour aggressiveness, metastasis, and resistance to oncological treatments, the impacts of hyperoxia on tumours are rarely explored because providing a long-lasting oxygen supply in vivo is a major challenge. Herein, we construct micro oxygen factories, namely, photosynthesis microcapsules (PMCs), by encapsulation of acquired cyanobacteria and upconversion nanoparticles in alginate microcapsules. This system enables a long-lasting oxygen supply through the conversion of external radiation into red-wavelength emissions for photosynthesis in cyanobacteria. PMC treatment suppresses the NF-kB pathway, HIF-1α production and cancer cell proliferation. Hyperoxic microenvironment created by an in vivo PMC implant inhibits hepatocarcinoma growth and metastasis and has synergistic effects together with anti-PD-1 in breast cancer. The engineering oxygen factories offer potential for tumour biology studies in hyperoxic microenvironments and inspire the exploration of oncological treatments.

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References

Nicoli S, Padula C, Aversa V, Vietti B, Wertz P, Millet A . Characterization of rabbit ear skin as a skin model for in vitro transdermal permeation experiments: histology, lipid composition and permeability. Skin Pharmacol Physiol. 2008; 21(4):218-26. DOI: 10.1159/000135638. View

Rankin E, Giaccia A . Hypoxic control of metastasis. Science. 2016; 352(6282):175-80. PMC: 4898055. DOI: 10.1126/science.aaf4405. View

Harris A . Hypoxia--a key regulatory factor in tumour growth. Nat Rev Cancer. 2002; 2(1):38-47. DOI: 10.1038/nrc704. View

Ebright R, Lee S, Wittner B, Niederhoffer K, Nicholson B, Bardia A . Deregulation of ribosomal protein expression and translation promotes breast cancer metastasis. Science. 2020; 367(6485):1468-1473. PMC: 7307008. DOI: 10.1126/science.aay0939. View

Yan J . Antitumor γδ T cells need oxygen to function. Nat Immunol. 2021; 22(3):268-269. PMC: 11418018. DOI: 10.1038/s41590-021-00874-9. View

Yang L, Liu Q, Zhang X, Liu X, Zhou B, Chen J . DNA of neutrophil extracellular traps promotes cancer metastasis via CCDC25. Nature. 2020; 583(7814):133-138. DOI: 10.1038/s41586-020-2394-6. View

Zelivianski S, Spellman M, Kellerman M, Kakitelashvilli V, Zhou X, Lugo E . ERK inhibitor PD98059 enhances docetaxel-induced apoptosis of androgen-independent human prostate cancer cells. Int J Cancer. 2003; 107(3):478-85. DOI: 10.1002/ijc.11413. View

Salic A, Mitchison T . A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc Natl Acad Sci U S A. 2008; 105(7):2415-20. PMC: 2268151. DOI: 10.1073/pnas.0712168105. View

Semenza G . Targeting HIF-1 for cancer therapy. Nat Rev Cancer. 2003; 3(10):721-32. DOI: 10.1038/nrc1187. View

10.

Yang J, Kumar A, Vilgelm A, Chen S, Ayers G, Novitskiy S . Loss of CXCR4 in Myeloid Cells Enhances Antitumor Immunity and Reduces Melanoma Growth through NK Cell and FASL Mechanisms. Cancer Immunol Res. 2018; 6(10):1186-1198. PMC: 6170679. DOI: 10.1158/2326-6066.CIR-18-0045. View

11.

Pastushenko I, Mauri F, Song Y, de Cock F, Meeusen B, Swedlund B . Fat1 deletion promotes hybrid EMT state, tumour stemness and metastasis. Nature. 2020; 589(7842):448-455. PMC: 7612440. DOI: 10.1038/s41586-020-03046-1. View

12.

Meininger I, Griesbach R, Hu D, Gehring T, Seeholzer T, Bertossi A . Alternative splicing of MALT1 controls signalling and activation of CD4(+) T cells. Nat Commun. 2016; 7:11292. PMC: 4832065. DOI: 10.1038/ncomms11292. View

13.

Laplante M, Sabatini D . mTOR signaling in growth control and disease. Cell. 2012; 149(2):274-93. PMC: 3331679. DOI: 10.1016/j.cell.2012.03.017. View

14.

Cheong H, Lu C, Lindsten T, Thompson C . Therapeutic targets in cancer cell metabolism and autophagy. Nat Biotechnol. 2012; 30(7):671-8. PMC: 3876738. DOI: 10.1038/nbt.2285. View

15.

Shim S, PATTERSON F, Kendall M . Hyperbaric chamber and decompression sickness: an experimental study. Can Med Assoc J. 1967; 97(21):1263-72. PMC: 1923513. View

16.

Pugh C, Ratcliffe P . Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med. 2003; 9(6):677-84. DOI: 10.1038/nm0603-677. View

17.

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

18.

Lengyel C, Altuna S, Habeeb B, Trapani D, Khan S . The Potential of PI3K/AKT/mTOR Signaling as a Druggable Target for Endometrial and Ovarian Carcinomas. Curr Drug Targets. 2019; 21(10):946-961. DOI: 10.2174/1389450120666191120123612. View

19.

Wang W, Kong Y, Jiang J, Xie Q, Huang Y, Li G . Engineering the Protein Corona Structure on Gold Nanoclusters Enables Red-Shifted Emissions in the Second Near-infrared Window for Gastrointestinal Imaging. Angew Chem Int Ed Engl. 2020; 59(50):22431-22435. DOI: 10.1002/anie.202010089. View

20.

Rohwer N, Zasada C, Kempa S, Cramer T . The growing complexity of HIF-1α's role in tumorigenesis: DNA repair and beyond. Oncogene. 2012; 32(31):3569-76. DOI: 10.1038/onc.2012.510. View