Organic/polymer photothermal nanoagents for photoacoustic imaging and photothermal therapy in vivo

Hanlin Ou; Jun Li; Chao Chen; Heqi Gao; Xue Xue; Dan Ding

doi:10.1007/s40843-019-9470-3

journal article·2019-11Open access

Organic/polymer photothermal nanoagents for photoacoustic imaging and photothermal therapy in vivo

Hanlin Ou, Jun Li, Chao Chen, Heqi Gao, Xue Xue, Dan Ding

Science China Materials· Volume 62· Issue 11

Publisher page Open full text

Source abstract

Abstract

In recent years, organic/polymer photothermal nanoagents including semiconducting polymer nanoparticles and small-molecule organic photothermal agents-encapsulated nanoparticles have attracted large attention from researchers in the biomedical field, owing to their excellent optical properties, good biocompatibility, easy processability, and flexible surface functionalization, as well as their combined functions of photoacoustic (PA) imaging and photothermal therapy (PTT). In this review, we summarize the recent advances in organic/polymer photothermal nanoagents for in vivo PA imaging and PTT applications. In particular, we focus on the design strategies, which are composed of traditional approaches and emerging mechanisms, especially based on “intramolecular motion-induced photothermy” strategy to regulate the photophysical properties of organic/polymer photothermal nanoagents for boosted in vivo PA imaging and PTT.

Source: openaire · Quality: candidate unverified · Source record ↗

Research context

Polymers Nanomaterials Biomaterials

OpenAlex topics: Nanoplatforms for cancer theranostics · Photoacoustic and Ultrasonic Imaging · Gold and Silver Nanoparticles Synthesis and Applications

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (100+)

Show source-provided references

1. Kim JW, Galanzha EI, Shashkov EV, et al. Golden carbon nanotubes as multimodal photoacoustic and photothermal high-contrast molecular agents. Nat Nanotech, 2009, 4: 688–69410.1038/nnano.2009.231 ↗

2. Liu Y, Bhattarai P, Dai Z, et al. Photothermal therapy and pho-toacoustic imaging via nanotheranostics in fighting cancer. Chem Soc Rev, 2019, 48: 2053–210810.1039/C8CS00618K ↗

3. Jokerst JV, Gambhir SS. Molecular imaging with theranostic nanoparticles. Acc Chem Res, 2011, 44: 1050–106010.1021/ar200106e ↗

4. Ke H, Wang J, Dai Z, et al. Gold-nanoshelled microcapsules: a theranostic agent for ultrasound contrast imaging and photothermal therapy. Angew Chem Int Ed, 2011, 50: 3017–302110.1002/anie.201008286 ↗

5. Zhang D, Qi GB, Zhao YX, et al. In situ formation of nanofibers from purpurin18-peptide conjugates and the assembly induced retention effect in tumor sites. Adv Mater, 2015, 27: 6125–613010.1002/adma.201502598 ↗

6. Lyu Y, Zeng J, Jiang Y, et al. Enhancing both biodegradability and efficacy of semiconducting polymer nanoparticles for photoacoustic imaging and photothermal therapy. ACS Nano, 2018, 12: 1801–181010.1021/acsnano.7b08616 ↗

7. Mou J, Chen Y, Ma M, et al. Facile synthesis of liposome/Cu2−xS-based nanocomposite for multimodal imaging and photothermal therapy. Sci China Mater, 2015, 58: 294–30110.1007/s40843-015-0044-3 ↗

8. Kim C, Favazza C, Wang LV. In vivo photoacoustic tomography of chemicals: high-resolution functional and molecular optical imaging at new depths. Chem Rev, 2010, 110: 2756–278210.1021/cr900266s ↗

9. Zhang D, Wang Z, Wang L, et al. High-performance identification of human bladder cancer using a signal self-amplifiable photoacoustic nanoprobe. ACS Appl Mater Interfaces, 2018, 10: 28331–2833910.1021/acsami.8b08357 ↗

10. Liu Y, Teng L, Liu HW, et al. Recent advances in organic-dye-based photoacoustic probes for biosensing and bioimaging. Sci China Chem, 2019, 24: doi: https://doi.org/10.1007/s11426-019-9506-210.1007/s11426-019-9506-2 ↗

11. Nie L, Chen X. Structural and functional photoacoustic molecular tomography aided by emerging contrast agents. Chem Soc Rev, 2014, 43: 7132–717010.1039/C4CS00086B ↗

12. Wang LV, Hu S. Photoacoustic tomography: in vivo imaging from organelles to organs. Science, 2012, 335: 1458–146210.1126/science.1216210 ↗

13. Zhang HF, Maslov K, Stoica G, et al. Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging. Nat Biotechnol, 2006, 24: 848–85110.1038/nbt1220 ↗

14. Jung HS, Verwilst P, Sharma A, et al. Organic molecule-based photothermal agents: an expanding photothermal therapy universe. Chem Soc Rev, 2018, 47: 2280–229710.1039/C7CS00522A ↗

15. Yang K, Zhang S, Zhang G, et al. Graphene in mice: ultrahigh in vivo tumor uptake and efficient photothermal therapy. Nano Lett, 2010, 10: 3318–332310.1021/nl100996u ↗

16. Li Y, Bai X, Xu M, et al. Photothermo-responsive Cu7S4@polymer nanocarriers with small sizes and high efficiency for controlled chemo/photothermo therapy. Sci China Mater, 2016, 59: 254–26410.1007/s40843-016-5035-6 ↗

17. Gao J, Sanchez-Purra M, Huang H, et al. Synthesis of different-sized gold nanostars for Raman bioimaging and photothermal therapy in cancer nanotheranostics. Sci China Chem, 2017, 60: 1219–122910.1007/s11426-017-9088-x ↗

18. Qi J, Fang Y, Kwok RTK, et al. Highly stable organic small molecular nanoparticles as an advanced and biocompatible photo-theranostic agent of tumor in living mice. ACS Nano, 2017, 11: 7177–718810.1021/acsnano.7b03062 ↗

19. Zhang J, Yang C, Zhang R, et al. Biocompatible D-A semiconducting polymer nanoparticle with light-harvesting unit for highly effective photoacoustic imaging guided photothermal therapy. Adv Funct Mater, 2017, 27: 160509410.1002/adfm.201605094 ↗

20. Chen D, Wang C, Nie X, et al. Photoacoustic imaging guided near-infrared photothermal therapy using highly water-dispersible single-walled carbon nanohorns as theranostic agents. Adv Funct Mater, 2014, 24: 6621–662810.1002/adfm.201401560 ↗

21. Mou J, Li P, Liu C, et al. Ultrasmall Cu2−xS nanodots for highly efficient photoacoustic imaging-guided photothermal therapy. Small, 2015, 11: 2275–228310.1002/smll.201403249 ↗

22. Ni D, Jiang D, Valdovinos HF, et al. Bioresponsive polyoxometalate cluster for redox-activated photoacoustic imagingguided photothermal cancer therapy. Nano Lett, 2017, 17: 3282–328910.1021/acs.nanolett.7b00995 ↗

23. Mallidi S, Luke GP, Emelianov S. Photoacoustic imaging in cancer detection, diagnosis, and treatment guidance. Trends Biotech, 2011, 29: 213–22110.1016/j.tibtech.2011.01.006 ↗

24. Yang Z, Song J, Dai Y, et al. Self-assembly of semiconductingplasmonic gold nanoparticles with enhanced optical property for photoacoustic imaging and photothermal therapy. Theranostics, 2017, 7: 2177–218510.7150/thno.20545 ↗

25. Zheng X, Mao H, Huo D, et al. Successively activatable ultrasensitive probe for imaging tumour acidity and hypoxia. Nat Biomed Eng, 2017, 1: 005710.1038/s41551-017-0057 ↗

26. Chen Y, Shi J. Mesoporous carbon biomaterials. Sci China Mater, 2015, 58: 241–25710.1007/s40843-015-0037-2 ↗

27. Gao YJ, Qiao ZY, Wang H. Polymers with tertiary amine groups for drug delivery and bioimaging. Sci China Chem, 2016, 59: 991–100210.1007/s11426-015-0516-2 ↗

28. Huang P, Lin J, Li W, et al. Biodegradable gold nanovesicles with an ultrastrong plasmonic coupling effect for photoacoustic imaging and photothermal therapy. Angew Chem Int Ed, 2013, 52: 13958–1396410.1002/anie.201308986 ↗

29. Yang T, Tang Y’, Liu L, et al. Size-dependent Ag2S nanodots for second near-infrared fluorescence/photoacoustics imaging and simultaneous photothermal therapy. ACS Nano, 2017, 11: 1848–185710.1021/acsnano.6b07866 ↗

30. Zhang S, Guo W, Wei J, et al. Terrylenediimide-based intrinsic theranostic nanomedicines with high photothermal conversion efficiency for photoacoustic imaging-guided cancer therapy. ACS Nano, 2017, 11: 3797–380510.1021/acsnano.6b08720 ↗

31. Zhu H, Lai Z, Fang Y, et al. Ternary chalcogenide nanosheets with ultrahigh photothermal conversion efficiency for photoacoustic theranostics. Small, 2017, 13: 160413910.1002/smll.201604139 ↗

32. Shashkov EV, Everts M, Galanzha EI, et al. Quantum dots as multimodal photoacoustic and photothermal contrast agents. Nano Lett, 2008, 8: 3953–395810.1021/nl802442x ↗

33. Borg RE, Rochford J. Molecular photoacoustic contrast agents: design principles & applications. Photochem Photobiol, 2018, 94: 1175–120910.1111/php.12967 ↗

34. Frenette M, Hatamimoslehabadi M, Bellinger-Buckley S, et al. Shining light on the dark side of imaging: excited state absorption enhancement of a bis-styryl BODIPY photoacoustic contrast agent. J Am Chem Soc, 2014, 136: 15853–1585610.1021/ja508600x ↗

35. Lyu Y, Fang Y, Miao Q, et al. Intraparticle molecular orbital engineering of semiconducting polymer nanoparticles as amplified theranostics for in vivo photoacoustic imaging and photothermal therapy. ACS Nano, 2016, 10: 4472–448110.1021/acsnano.6b00168 ↗

36. Aoki H, Nojiri M, Mukai R, et al. Near-infrared absorbing polymer nano-particle as a sensitive contrast agent for photoacoustic imaging. Nanoscale, 2015, 7: 337–34310.1039/C4NR04724A ↗

37. Yang K, Xu H, Cheng L, et al. In vitro and in vivo near-infrared photothermal therapy of cancer using polypyrrole organic nanoparticles. Adv Mater, 2012, 24: 5586–559210.1002/adma.201202625 ↗

38. Hong G, Antaris AL, Dai H. Near-infrared fluorophores for biomedical imaging. Nat Biomed Eng, 2017, 1: 001010.1038/s41551-016-0010 ↗

39. Ding F, Zhan Y, Lu X, et al. Recent advances in near-infrared II fluorophores for multifunctional biomedical imaging. Chem Sci, 2018, 9: 4370–438010.1039/C8SC01153B ↗

40. Song G, Liang C, Gong H, et al. Core-shell MnSe@Bi2Se3 fabricated via a cation exchange method as novel nanotheranostics for multimodal imaging and synergistic thermoradiotherapy. Adv Mater, 2015, 27: 6110–611710.1002/adma.201503006 ↗

41. Chen S, Jia Q, Zheng X, et al. PEGylated carbon dot/MnO2 nanohybrid: a new pH/H2O2-driven, turn-on cancer nanotheranostics. Sci China Mater, 2018, 61: 1325–133810.1007/s40843-018-9261-x ↗

42. Huang P, Lin J, Wang X, et al. Light-triggered theranostics based on photosensitizer-conjugated carbon dots for simultaneous enhanced-fluorescence imaging and photodynamic therapy. Adv Mater, 2012, 24: 5104–511010.1002/adma.201200650 ↗

43. Kim J, Park S, Lee C, et al. Organic nanostructures for photoacoustic imaging. ChemNanoMat, 2016, 2: 156–16610.1002/cnma.201500171 ↗

44. Geng J, Sun C, Liu J, et al. Biocompatible conjugated polymer nanoparticles for efficient photothermal tumor therapy. Small, 2015, 11: 1603–161010.1002/smll.201402092 ↗

45. Xiong Z, Shen M, Shi X. Dendrimer-based strategies for cancer therapy: recent advances and future perspectives. Sci China Mater, 2018, 61: 1387–140310.1007/s40843-018-9271-4 ↗

46. Li J, Pu K. Development of organic semiconducting materials for deep-tissue optical imaging, phototherapy and photoactivation. Chem Soc Rev, 2019, 48: 38–7110.1039/C8CS00001H ↗

47. Li K, Liu B. Polymer-encapsulated organic nanoparticles for fluorescence and photoacoustic imaging. Chem Soc Rev, 2014, 43: 6570–659710.1039/C4CS00014E ↗

48. Weber J, Beard PC, Bohndiek SE. Contrast agents for molecular photoacoustic imaging. Nat Methods, 2016, 13: 639–65010.1038/nmeth.3929 ↗

49. Chen P, Ma Y, Zheng Z, et al. Facile syntheses of conjugated polymers for photothermal tumour therapy. Nat Commun, 2019, 10: 119210.1038/s41467-019-09226-6 ↗

50. Jiang Y, Pu K. Multimodal biophotonics of semiconducting polymer nanoparticles. Acc Chem Res, 2018, 51: 1840–184910.1021/acs.accounts.8b00242 ↗

51. Pu K, Shuhendler AJ, Jokerst JV, et al. Semiconducting polymer nanoparticles as photoacoustic molecular imaging probes in living mice. Nat Nanotech, 2014, 9: 233–23910.1038/nnano.2013.302 ↗

52. Zhang X, Xia LY, Chen X, et al. Hydrogel-based phototherapy for fighting cancer and bacterial infection. Sci China Mater, 2017, 60: 487–50310.1007/s40843-017-9025-3 ↗

53. Gunnlaugsson T. Integrating NIR light photocage enables in vivo dual-channel tracking of drug release. Sci China Chem, 2018, 61: 1347–134810.1007/s11426-018-9298-0 ↗

54. Szabó C, Ischiropoulos H, Radi R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov, 2007, 6: 662–68010.1038/nrd2222 ↗

55. Medzhitov R. Origin and physiological roles of inflammation. Nature, 2008, 454: 428–43510.1038/nature07201 ↗

56. Guo B, Sheng Z, Hu D, et al. Molecular engineering of conjugated polymers for biocompatible organic nanoparticles with highly efficient photoacoustic and photothermal performance in cancer theranostics. ACS Nano, 2017, 11: 10124–1013410.1021/acsnano.7b04685 ↗

57. Ng KK, Zheng G. Molecular interactions in organic nanoparticles for phototheranostic applications. Chem Rev, 2015, 115: 11012–1104210.1021/acs.chemrev.5b00140 ↗

58. Lovell JF, Jin CS, Huynh E, et al. Porphysome nanovesicles generated by porphyrin bilayers for use as multimodal biophotonic contrast agents. Nat Mater, 2011, 10: 324–33210.1038/nmat2986 ↗

59. Chen C, Ou H, Liu R, et al. Regulating the photophysical property of organic/polymer optical agents for promoted cancer photo-theranostics. Adv Mater, 2019, 35: 180633110.1002/adma.201806331 ↗

60. Cai X, Liu J, Liew WH, et al. Organic molecules with propeller structures for efficient photoacoustic imaging and photothermal ablation of cancer cells. Mater Chem Front, 2017, 1: 1556–156210.1039/C7QM00056A ↗

61. Dong T, Wen K, Chen J, et al. Significant enhancement of photothermal and photoacoustic efficiencies for semiconducting polymer nanoparticles through simply molecular engineering. Adv Funct Mater, 2018, 28: 180013510.1002/adfm.201800135 ↗

62. Miao Q, Lyu Y, Ding D, et al. Semiconducting oligomer nanoparticles as an activatable photoacoustic probe with amplified brightness for in vivo imaging of pH. Adv Mater, 2016, 28: 3662–366810.1002/adma.201505681 ↗

63. Coakley RJ, Taggart C, McElvaney NG, et al. Cytosolic pH and the inflammatory microenvironment modulate cell death in human neutrophils after phagocytosis. Blood, 2002, 100: 3383–339110.1182/blood.V100.9.3383 ↗

64. Webb BA, Chimenti M, Jacobson MP, et al. Dysregulated pH: a perfect storm for cancer progression. Nat Rev Cancer, 2011, 11: 671–67710.1038/nrc3110 ↗

65. Zhen X, Feng X, Xie C, et al. Surface engineering of semiconducting polymer nanoparticles for amplified photoacoustic imaging. Biomaterials, 2017, 127: 97–10610.1016/j.biomaterials.2017.03.003 ↗

66. Xie C, Zhen X, Lyu Y, et al. Nanoparticle regrowth enhances photoacoustic signals of semiconducting macromolecular probe for in vivo imaging. Adv Mater, 2017, 29: 170369310.1002/adma.201703693 ↗

67. Li LL, Ma HL, Qi GB, et al. Pathological-condition-driven construction of supramolecular nanoassemblies for bacterial infection detection. Adv Mater, 2016, 28: 254–26210.1002/adma.201503437 ↗

68. Yang Z, Tian R, Wu J, et al. Impact of semiconducting perylene diimide nanoparticle size on lymph node mapping and cancer imaging. ACS Nano, 2017, 11: 4247–425510.1021/acsnano.7b01261 ↗

69. Guo B, Sheng Z, Hu D, et al. Through scalp and skull NIR-II photothermal therapy of deep orthotopic brain tumors with precise photoacoustic imaging guidance. Adv Mater, 2018, 30: 180259110.1002/adma.201802591 ↗

70. Yu S, Tu D, Lian W, et al. Lanthanide-doped near-infrared II luminescent nanoprobes for bioapplications. Sci China Mater, 2019, 62: 1071–108610.1007/s40843-019-9414-4 ↗

71. Antaris AL, Chen H, Cheng K, et al. A small-molecule dye for NIR-II imaging. Nat Mater, 2016, 15: 235–24210.1038/nmat4476 ↗

72. Lu W, Melancon MP, Xiong C, et al. Effects of photoacoustic imaging and photothermal ablation therapy mediated by targeted hollow gold nanospheres in an orthotopic mouse xenograft model of glioma. Cancer Res, 2011, 71: 6116–612110.1158/0008-5472.CAN-10-4557 ↗

73. Lee C, Hwang HS, Lee S, et al. Rabies virus-inspired silica-coated gold nanorods as a photothermal therapeutic platform for treating brain tumors. Adv Mater, 2017, 29: 160556310.1002/adma.201605563 ↗

74. Zheng X, Wang X, Mao H, et al. Hypoxia-specific ultrasensitive detection of tumours and cancer cells in vivo. Nat Commun, 2015, 6: 583410.1038/ncomms6834 ↗

75. Li J, Liu J, Chen C. Remote control and modulation of cellular events by plasmonic gold nanoparticles: implications and opportunities for biomedical applications. ACS Nano, 2017, 11: 2403–240910.1021/acsnano.7b01200 ↗

76. Zhang J, Chen J, Ren J, et al. Biocompatible semiconducting polymer nanoparticles as robust photoacoustic and photothermal agents revealing the effects of chemical structure on high photothermal conversion efficiency. Biomaterials, 2018, 181: 92–10210.1016/j.biomaterials.2018.07.042 ↗

77. Torchilin V. Tumor delivery of macromolecular drugs based on the EPR effect. Adv Drug Deliver Rev, 2011, 63: 131–13510.1016/j.addr.2010.03.011 ↗

78. McPherson T, Kidane A, Szleifer I, et al. Prevention of protein adsorption by tethered poly(ethylene oxide) layers: Experiments and single-chain mean-field analysis. Langmuir, 1998, 14: 176–18610.1021/la9706781 ↗

79. Zhao J, Chai YD, Zhang J, et al. Long circulating micelles of an amphiphilic random copolymer bearing cell outer membrane phosphorylcholine zwitterions. Acta Biomater, 2015, 16: 94–10210.1016/j.actbio.2015.01.019 ↗

80. Knop K, Hoogenboom R, Fischer D, et al. Poly(ethylene glycol) in drug delivery: Pros and cons as well as potential alternatives. Angew Chem Int Ed, 2010, 49: 6288–630810.1002/anie.200902672 ↗

81. Owens III D, Peppas N. Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int J Pharm, 2006, 307: 93–10210.1016/j.ijpharm.2005.10.010 ↗

82. Chai Z, Hu X, Lu W. Cell membrane-coated nanoparticles for tumor-targeted drug delivery. Sci China Mater, 2017, 60: 504–51010.1007/s40843-016-5163-4 ↗

83. Chen Z, Zhao P, Luo Z, et al. Cancer cell membrane-biomimetic nanoparticles for homologous-targeting dual-modal imaging and photothermal therapy. ACS Nano, 2016, 10: 10049–1005710.1021/acsnano.6b04695 ↗

84. Feng G, Liu B. Multifunctional AIEgens for future theranostics. Small, 2016, 12: 6528–653510.1002/smll.201601637 ↗

85. Yang K, Hu L, Ma X, et al. Multimodal imaging guided photothermal therapy using functionalized graphene nanosheets anchored with magnetic nanoparticles. Adv Mater, 2012, 24: 1868–187210.1002/adma.201104964 ↗

86. Huang P, Rong P, Jin A, et al. Dye-loaded ferritin nanocages for multimodal imaging and photothermal therapy. Adv Mater, 2014, 26: 6401–640810.1002/adma.201400914 ↗

87. Qi J, Chen C, Zhang X, et al. Light-driven transformable optical agent with adaptive functions for boosting cancer surgery outcomes. Nat Commun, 2018, 9: 184810.1038/s41467-018-04222-8 ↗

88. Lv JA, Liu Y, Wei J, et al. Photocontrol of fluid slugs in liquid crystal polymer microactuators. Nature, 2016, 537: 179–18410.1038/nature19344 ↗

89. Qian H, Cousins ME, Horak EH, et al. Suppression of Kasha’s rule as a mechanism for fluorescent molecular rotors and aggregation-induced emission. Nat Chem, 2017, 9: 83–8710.1038/nchem.2612 ↗

90. Goh WL, Lee MY, Joseph TL, et al. Molecular rotors as conditionally fluorescent labels for rapid detection of biomolecular interactions. J Am Chem Soc, 2014, 136: 6159–616210.1021/ja413031h ↗

91. Jin M, Chung TS, Seki T, et al. Phosphorescence control mediated by molecular rotation and aurophilic interactions in amphidynamic crystals of 1,4-bis[tri-(p-fluorophenyl)phosphane-gold(I)-ethynyl]benzene. J Am Chem Soc, 2017, 139: 18115–1812110.1021/jacs.7b11316 ↗

92. Zhao Z, Chen C, Wu W, et al. Highly efficient photothermal nanoagent achieved by harvesting energy via excited-state intramolecular motion within nanoparticles. Nat Commun, 2019, 10: 76810.1038/s41467-019-08722-z ↗

93. Ni X, Zhang X, Duan X, et al. Near-infrared afterglow luminescent aggregation-induced emission dots with ultrahigh tumor-to-liver signal ratio for promoted image-guided cancer surgery. Nano Lett, 2019, 19: 318–33010.1021/acs.nanolett.8b03936 ↗

94. Mei J, Leung NLC, Kwok RTK, et al. Aggregation-induced emission: Together we shine, united we soar! Chem Rev, 2015, 115: 11718–1194010.1021/acs.chemrev.5b00263 ↗

95. Gao H, Zhang X, Chen C, et al. Unity makes strength: How aggregation-induced emission luminogens advance the biomedical field. Adv Biosys, 2018, 2: 180007410.1002/adbi.201800074 ↗

96. Hong Y, Lam JWY, Tang BZ. Aggregation-induced emission: phenomenon, mechanism and applications. Chem Commun, 2009, 1: 4332–435310.1039/b904665h ↗

97. Liang J, Tang BZ, Liu B. Specific light-up bioprobes based on AIEgen conjugates. Chem Soc Rev, 2015, 44: 2798–281110.1039/C4CS00444B ↗

98. Jiang N, Shen T, Sun JZ, et al. Aggregation-induced emission: Right there shining. Sci China Mater, 2019, 62: 1227–123510.1007/s40843-019-9443-8 ↗

99. Ou H, Dai S, Liu R, et al. Manipulating the intramolecular motion of AIEgens for boosted biomedical applications. Sci China Chem, 2019, 62: 929–93210.1007/s11426-019-9497-2 ↗

100. Xu M, Wang X, Wang Q, et al. Analyte-responsive fluorescent probes with AIE characteristic based on the change of covalent bond. Sci China Mater, 2019, 62: 1236–125010.1007/s40843-019-9407-9 ↗