Black phosphorus-based photothermal therapy with aCD47-mediated immune checkpoint blockade for enhanced cancer immunotherapy

Zhongjian Xie; Minhua Peng; Ruitao Lu; Xiangying Meng; Weiyuan Liang; Zhongjun Li; Meng Qiu; Bin Zhang; Guohui Nie; Ni Xie; Han Zhang; Paras N. Prasad

doi:10.1038/s41377-020-00388-3

Go to Nature Website

Your Location：

Home >

Browse articles >

Black phosphorus-based photothermal therapy with aCD47-mediated immune checkpoint blockade for enhanced cancer immunotherapy

Original Articles

- Black phosphorus-based photothermal therapy with aCD47-mediated immune checkpoint blockade for enhanced cancer immunotherapy
- Light: Science & Applications Vol. 9, Issue 5, Pages: 1534-1548(2020)
- Affiliations：
  
  1.Shenzhen International Institute for Biomedical Research, Shenzhen 518116 Guangdong, PR China
  2.Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055 Guangdong, PR China
  3.School of Basic Medical Sciences, Guangzhou Medical University, Guangzhou 511436 Guangdong, PR China
  4.Key Laboratory of Optoelectronic Devices and Systems of Ministry of Education and Guangdong Province, Institute of Microscale Optoelectronics, and Otolaryngology Department and Biobank of the First Affiliated Hospital, Shenzhen Second People's Hospital, Health Science Center, Shenzhen University, Shenzhen 518060, PR China
  5.Key Laboratory of Marine Chemistry Theory and Technology (Ocean University of China), Ministry of Education, Qingdao 266100, PR China
  6.Department of Chemistry, Institute for Lasers, Photonics, and Biophotonics, University at Buffalo, StateUniversity of New York, Buffalo, NY, USA
- Author bio：
  
  Han Zhang (hzhang@szu.edu.cn)
  Paras N. Prasad (pnprasad@buffalo.edu)
- Funds：
- DOI：10.1038/s41377-020-00388-3
  CLC：
- Published：2020，
  
  Published Online：15 September 2020，
  
  Received：15 April 2020，
  
  Revised：13 July 2020，
  
  Accepted：13 August 2020
- Accepted：
Scan QR Code
Xie, Z. J. et al. Black phosphorus-based photothermal therapy with aCD47-mediated immune checkpoint blockade for enhanced cancer immunotherapy. Light: Science & Applications, 9, 1534-1548 (2020).
DOI：

Xie, Z. J. et al. Black phosphorus-based photothermal therapy with aCD47-mediated immune checkpoint blockade for enhanced cancer immunotherapy. Light: Science & Applications, 9, 1534-1548 (2020). DOI： 10.1038/s41377-020-00388-3.

摘要

Abstract

Here

we describe a combination strategy of black phosphorus (BP)-based photothermal therapy together with anti-CD47 antibody (aCD47)-based immunotherapy to synergistically enhance cancer treatment. Tumour resistance to immune checkpoint blockades in most cancers due to immune escape from host surveillance

along with the initiation of metastasis through immunosuppressive cells in the tumour microenvironment

remains a significant challenge for cancer immunotherapy. aCD47

an agent for CD47/SIRPα axis blockade

induces modest phagocytic activity and a low response rate for monotherapy

resulting in failures in clinical trials. We showed that BP-mediated ablation of tumours through photothermal effects could serve as an effective strategy for specific immunological stimulation

improving the inherently poor immunogenicity of tumours

which is particularly useful for enhancing cancer immunotherapy. BP in combination with aCD47 blockade activates both innate and adaptive immunities and promotes local and systemic anticancer immune responses

thus offering a synergistically enhanced effect in suppression of tumour progression and in inducing abscopal effects for inhibition of metastatic cancers. Our combination strategy provides a promising platform in which photothermal agents could help to enhance the therapeutic efficacy of immunotherapy.

关键词

Keywords

references

Pardoll, D. M.&Topalian, S. L. The role of CD4+ T cell responses in antitumor immunity.Curr. Opin. Immunol.10, 588–594 (1998)..

Dong H. D. et al. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion.Nat. Med.5, 1365–1369 (1999)..

Topalian S. L. et al. Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab.J. Clin. Oncol.32, 1020–1030 (2014)..

Sharma, P.&Allison, J. P. Immune checkpoint targeting in cancer therapy: toward combination strategies with curative potential.Cell161, 205–214 (2015)..

Mellman, I., Coukos, G.&Dranoff, G. Cancer immunotherapy comes of age.Nature480, 480–489 (2011)..

Leach, D. R., Krummel, M. F.&Allison, J. P. Enhancement of antitumor immunity by CTLA-4 blockade.Science271, 1734–1736 (1996)..

Hodi F. S. et al. Improved survival with ipilimumab in patients with metastatic melanoma.N. Engl. J. Med.363, 711–723 (2010)..

Quail, D. F.&Joyce, J. A. Microenvironmental regulation of tumor progression and metastasis.Nat. Med.19, 1423–1437 (2013)..

Kitamura, T., Qian, B. Z.&Pollard, J. W. Immune cell promotion of metastasis.Nat. Rev. Immunol.15, 73–86 (2015)..

Sica A. et al. Macrophage polarization in tumour progression.Semin. Cancer Biol.18, 349–355 (2008)..

Lewis, C. E.&Pollard, J. W. Distinct role of macrophages in different tumor microenvironments.Cancer Res.66, 605–612 (2006)..

Qian, B. Z.&Pollard, J. W. Macrophage diversity enhances tumor progression and metastasis.Cell141, 39–51 (2010)..

Wang Y. C. et al. Notch signaling determines the M1 versus M2 polarization of macrophages in antitumor immune responses.Cancer Res.70, 4840–4849 (2010)..

Lawrence, T.&Natoli, G. Transcriptional regulation of macrophage polarization: enabling diversity with identity.Nat. Rev. Immunol.11, 750–761 (2011)..

Pyonteck S. M. et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression.Nat. Med.19, 1264–1272 (2013)..

Guerriero J. L. et al. Class IIa HDAC inhibition reduces breast tumours and metastases through anti-tumour macrophages.Nature543, 428–432 (2017)..

Jaiswal S. et al. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis.Cell138, 271–285 (2009)..

Liu M. G. et al. Metabolic rewiring of macrophages by CpG potentiates clearance of cancer cells and overcomes tumor-expressed CD47-mediated 'don't-eat-me' signal.Nat. Immunol.20, 265–275 (2019)..

Majeti R. et al. CD47 is an adverse prognostic factor and therapeutic antibody target on human acutemyeloid leukemia stem cells.Cell138, 286–299 (2009)..

Liu X. J. et al. Is CD47 an innate immune checkpoint for tumor evasion?J. Hematol. Oncol.10, 12 (2017)..

Xiao Z. Y. et al. Antibody mediated therapy targeting CD47 inhibits tumor progression of hepatocellular carcinoma.Cancer Lett.360, 302–309 (2015)..

Edris B. et al. Antibody therapy targeting the CD47 protein is effective in a model of aggressive metastatic leiomyosarcoma.Proc. Natl Acad. Sci. USA109, 6656–6661 (2012)..

Willingham S. B. et al. The CD47-signal regulatory protein alpha (SIRPa) interaction is a therapeutic target for human solid tumors.Proc. Natl Acad. Sci. USA109, 6662–6667 (2012)..

Chen J. et al. SLAMF7 is critical for phagocytosis of haematopoietic tumour cells via Mac-1 integrin.Nature544, 493–497 (2017)..

Wang Y. et al. Ara-C and anti-CD47 antibody combination therapy eliminates acute monocytic leukemia THP-1 cells in vivo and in vitro.Genet. Mol. Res.14, 5630–5641 (2015)..

Kiss B. et al. CD47-targeted near-infrared photoimmunotherapy for human bladder cancer.Clin. Cancer Res.25, 3561–3571 (2019)..

Brace C. Thermal tumor ablation in clinical use.IEEE Pulse2, 28–38 (2011)..

Huang X. H. et al. Cancer cell imaging and photothermal therapy in the near-infrared region by using gold nanorods.J. Am. Chem. Soc.128, 2115–2120 (2006)..

Kaczmarek, A., Vandenabeele, P.&Krysko, D. V. Necroptosis: the release of damage-associated molecular patterns and its physiological relevance.Immunity38, 209–223 (2013)..

Panzarini E. et al. Rose bengal acetate photodynamic therapy (RBAc-PDT) induces exposure and release of Damage-Associated Molecular Patterns (DAMPs) in human HeLa cells.PLoS ONE9, e105778 (2014)..

Galluzzi L. et al. Immunogenic cell death in cancer and infectious disease.Nat. Rev. Immunol.17, 97–111 (2017)..

Krysko D. V. et al. Immunogenic cell death and DAMPs in cancer therapy.Nat. Rev. Cancer12, 860–875 (2012)..

Qiu M. et al. Omnipotent phosphorene: a next-generation, two-dimensional nanoplatform for multidisciplinary biomedical applications.Chem. Soc. Rev.47, 5588–5601 (2018)..

Xie Z. J. et al. Ultrathin 2D nonlayered tellurium nanosheets: facile liquid‐phase exfoliation, characterization, and photoresponse with high performance and enhanced stability.Adv. Funct. Mater.16, 1705833 (2018)..

Xing C. Y. et al. 2D nonlayered selenium nanosheets: facile synthesis, photoluminescence, and ultrafast photonics.Adv. Optical Mater.5, 1700884 (2017)..

Fan T. J. et al. Two-dimensional non-layered selenium nanoflakes: facile fabrications and applications for self-powered photo-detector.Nanotechnology30, 114002 (2019)..

Wu L. M. et al. Few-layer tin sulfide: a promising black-phosphorus-analogue 2D material with exceptionally large nonlinear optical response, high stability, and applications in all-optical switching and wavelength conversion.Adv. Optical Mater.2, 1700985 (2018)..

Xie Z. J. et al. Revealing of the ultrafast third-order nonlinear optical response and enabled photonic application in two-dimensional tin sulfide.Photonics Res.7, 494–502 (2019)..

Xie Z. J. et al. Black phosphorus analogue tin sulfide nanosheets: synthesis and application as near-infrared photothermal agents and drug delivery platforms for cancer therapy.J. Mater. Chem. B6, 4747–4755 (2018)..

Huang W. C. et al. Black-phosphorus-analogue tin monosulfide: an emerging optoelectronic two-dimensional material for high-performance photodetection with improved stability under ambient/harsh conditions.J. Mater. Chem. C.6, 9582–9593 (2018)..

Qiu M. et al. Novel concept of the smart NIR-light-controlled drug release of black phosphorus nanostructure for cancer therapy.Proc. Natl Acad. Sci. USA115, 501–506 (2018)..

Xie Z. J. et al. Biocompatible two-dimensional titanium nanosheets for multimodal imaging-guided cancer theranostics.ACS Appl. Mater. Interfaces11, 22129–22140 (2019)..

Xing C. Y. et al. Two-dimensional MXene (Ti3C2)-Integrated cellulose hydrogels: toward smart three-dimensional network nanoplatforms exhibiting light-induced swelling and bimodal photothermal/chemotherapy anticancer activity.ACS Appl. Mater. Interfaces10, 27631–27643 (2018)..

Liang X. et al. Photothermal cancer immunotherapy by erythrocyte membrane-coated black phosphorus formulation.J. Controlled Release296, 150–161 (2019)..

Tang X. et al. Fluorinated phosphorene: electrochemical synthesis, atomistic fluorination, and enhanced stability.Small13, 1702739 (2017)..

Xing C. Y. et al. Ultrasmall bismuth quantum dots: facile liquid-phase exfoliation, characterization, and application in high-performance UV-Vis Photodetector.ACS Photonics5, 621–629 (2018)..

Xing C. Y. et al. Conceptually novel black phosphorus/cellulose hydrogels as promising photothermal agents for effective cancer therapy. Advanced Healthcare.Materials7, 1701510 (2018)..

Guo Z. N. et al. From black phosphorus to phosphorene: basic solvent exfoliation, evolution of raman scattering, and applications to ultrafast photonics.Adv. Funct. Mater.25, 6996–7002 (2015)..

Chen J. M. et al. Advances in nanomaterials for photodynamic therapy applications: status and challenges.Biomaterials237, 119827 (2020)..

Wang M. Q. et al. Ultrasmall black phosphorus quantum dots: synthesis, characterization, and application in cancer treatment.Analyst143, 5822–5833 (2018)..

Sun Z. B. et al. Ultrasmall black phosphorus quantum dots: synthesis and use as photothermal agents.Angew. Chem. Int. Ed.54, 11526–11530 (2015)..

Wang Z. et al. Biodegradable black phosphorus-based nanomaterials in biomedicine: theranostic applications.Curr. Medicinal Chem.26, 1788–1805 (2019)..

Shao J. D. et al. Biodegradable black phosphorus-based nanospheres for in vivo photothermal cancer therapy.Nat. Commun.7, 12967 (2016)..

Tao W. et al. Black phosphorus nanosheets as a robust delivery platform for cancer theranostics.Adv. Mater.29, 1603276 (2017)..

Ling X. et al. The renaissance of black phosphorus.Proc. Natl Acad. Sci. USA112, 4523–4530 (2015)..

Arabi Y. M. et al. Treatment of Middle East respiratory syndrome with a combination of lopinavir/ritonavir and interferon-β1b (MIRACLE trial): statistical analysis plan fora recursive two-stage group sequential randomized controlled trial.Trials21, 8 (2020)..

Knavel, E. M.&Brace, C. L. Tumor ablation: common modalities and general practices.Tech. Vasc. Interventional Radiol.16, 192–200 (2013)..

Mildner, A., Marinkovic, G.&Jung, S. Murine monocytes: origins, subsets, fates, and functions.Microbiol. Spectr.4, 141–153 (2016)..

Andersen M. H. et al. Cytotoxic T cells.J. Investigative Dermatol.126, 32–41 (2006)..

Kim D. et al. Anti-CD47 antibodies promote phagocytosis and inhibit the growth of human myeloma cells.Leukemia26, 2538–2545 (2012)..

Scholzen, T.&Gerdes, J. The Ki-67 protein: from the known and the unknown.J. Cell. Physiol.182, 311–322 (2000)..

Zhang M. et al. Anti-CD47 treatment stimulates phagocytosis of glioblastoma by M1 and M2 polarized macrophages and promotes M1 polarized macrophages in vivo.PLoS ONE11, e0153550 (2016)..

Gu S. L. et al. CD47 blockade inhibits tumor progression through promoting phagocytosis of tumor cells by M2 polarized macrophages in endometrial cancer.J. Immunol. Res.2018, 6156757(2018)..

Couzin-Frankel J. Cancer immunotherapy.Science342, 1432–1433 (2013)..

Farhood, B., Najafi, M.&Mortezaee, K. CD8+ cytotoxic T lymphocytes in cancer immunotherapy: a review.J. Cell. Physiol.234, 8509–8521 (2019)..

Gutcher, I.&Becher, B. APC-derived cytokines and T cell polarization in autoimmune inflammation.J. Clin. Investig.117, 1119–1127 (2007)..

Van der Meide, P. H.&Schellekens, H. Cytokines and the immune response.Biotherapy8, 243–249 (1996)..

Bhat P. et al. Interferon-γ derived from cytotoxic lymphocytes directly enhances their motility and cytotoxicity.Cell Death Dis.8, e2836 (2017)..

Fisher D. T. et al. The two faces of IL-6 in the tumor microenvironment.Semin. Immunol.26, 38–47 (2014)..

Wang, X.&Lin, Y. Tumor necrosis factor and cancer, buddies or foes?Acta Pharmacologica Sin.29, 1275–1288 (2008)..

Mélik-Parsadaniantz, S.&Rostène, W. Chemokines and neuromodulation.J. Neuroimmunol.198, 62–68 (2008)..

Nagarsheth, N., Wicha, M. S.&Zou, W. P. Chemokines in the cancer microenvironment and their relevance in cancer immunotherapy.Nat. Rev. Immunol.17, 559–572 (2017)..

Lin, Y., Sharma, S.&John, M. S. CCL21 cancer immunotherapy.Cancers6, 1098–1110 (2014)..

Romagnani P. et al. Cell cycle-dependent expression of CXC chemokine receptor 3 by endothelial cells mediates angiostatic activity.J. Clin. Investig.107, 53–63 (2001)..

Pearson G. et al. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions.Endocr. Rev.22, 153–183 (2001)..

Vermeulen L. et al. The versatile role of MSKs in transcriptional regulation.Trends Biochemical Sci.34, 311–318 (2009)..

Chaffer, C. L.&Weinberg, R. A. A perspective on cancer cell metastasis.Science331, 1559–1564 (2011)..

Xie Z. et al. Emerging combination strategies with phototherapy in cancer nanomedicine.Chem. Soc. Rev.https://doi.org/10.1039/D0CS00215Ahttps://doi.org/10.1039/D0CS00215A(2020)..

Views

Downloads

CSCD

Alert me when the article has been cited

Submit

Tools

Publicity Resources

No data

Related Author

No data

Related Institution

No data

⁰