中文
Earlier issues
Announcement
More
Progress in Chemistry 2021, Vol. 33 Issue (1): 1-12 DOI: 10.7536/PC200423   Next Articles

• Invited Account •

Detection of Circulating Tumor Cell in Vivo:Technology and Application

Shan Guo1,2,*(), Xiang Zhou2   

  1. 1 Department of Biological Repositories, Zhongnan Hospital of Wuhan University,Wuhan 430071, China
    2 College of Chemistry and Molecular Sciences, Wuhan University,Wuhan 430072, China
  • Received: Revised: Online: Published:
  • Contact: Shan Guo
  • Supported by:
    the National Natural Science Foundation of China(21904101); and the Program of Excellent Doctoral(Postdoctoral) of Zhongnan Hospital of Wuhan University(ZNYB2019015)
Richhtml ( 98 ) PDF ( 996 ) Cited
Export

EndNote

Ris

BibTeX

Cancer cells that shed from solid tumor and circulate into bloodstream, namely circulating tumor cells(CTCs), are closely related to tumor metastasis. Therefore, CTCs detection is of great significance for cancer diagnosis, treatment monitoring, disease assessment and understanding of the mechanisms underlying tumor metastasis. However, CTCs are extraordinarily rare, heterogeneous, nonuniform in blood. Even if strategies for detection of CTCs in static blood collected from patients have made significant progress, they still face the tumor cell loss, cell death, low fidelity, and low sensitivity. It is essential to develop approaches available for detection of tumor cells in fast-flowing blood, allowing real-time monitoring of CTC dynamic changes under physiological conditions. In this review, we summarize techniques developed for CTC detection in vivo and their related applications. Furthermore, the advantages and disadvantages of these techniques are analyzed. Finally, future techniques for detection of CTCs in vivo are discussed and predicted.

Contents

1 Introduction

2 Detection of circulating tumor cells(CTCs) in vivo

2.1 Optical imaging-based CTC detection in vivo

2.2 In vivo flow cytometry-based CTC enumeration

2.3 Scaffold implant-based CTC recruiting in vivo

2.4 Intravenous indwelling device-based CTC capture in vivo

2.5 Microfluidic chip-based CTC detection in vivo

3 Conclusion and outlook

Key words: cancer, circulating tumor cells, in vivo detection
Fig. 1 In vivo detection of circulating tumor cells by SM-OCT[58]. (a) TEM image and Vis-NIR absorbance spectrum of gold nanorod contrast agents.(b) RPMI-8226 cells are incubated with gold nanorods, resulting in gold nanorod-labeled cells.(c) SM-OCT scans at the cross section of blood vessels found in the ear of the mouse, determining the number of cells flowing through the blood vessel over time. Gold nanorod-labeled cells are injected into the tail vein of the mouse for detection. Copyright 2019, American Chemical Society
Fig. 2 In vivo detection of CTCs based on cytophone device[95]. (a) Schematic diagram of cytophone platform for photoacoustic detection of CTCs.(b) Photoacoustic peaks of single CTC, CTC cluster, CBC and CTC-CBC generated from cytophone platform. Copyright 2019, the Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science
Fig. 3 Capture of CTCs in vivo based on intravenous indwelling device. (a) Schematic diagram of functionalized Seldinger medical guidewire for in vivo capture of CTCs[100]. Seldinger medical guidewire is slowly pushed forward into the indwelling cannula until functionalized guidewire is exposed to the blood flow within the lumen of the vein.(b) Schematic diagram of in vivo capture of CTCs based on transfusion with a vein indwelling needle[110]. The surface of indwelling needle was modified with anti-EpCAM antibody. Copyright 2015, American Chemical Society(c) Schematic diagram of 3D PDMS scaffold-embedded hollow needle for in vivo capture and downstream analysis of CTCs[112]. Copyright 2020, American Chemical Society
Fig. 4 Schematic diagram of magnetic chip for in vivo detection of CTCs based on extracorporeal circulation[115]. Copyright 2019, American Chemical Society
[1]
Ashworth T R. Med. J. Aust., 1869, 14: 146.
[2]
Paget S. Cancer Metastasis Rev., 1989, 8: 98.
[3]
Bonnet D, Dick J E. Nat. Med., 1997, 3: 730.

doi: 10.1038/nm0797-730
[4]
Gupta A S. Nanomedicine , 2014, 9: 1517.

doi: 10.2217/NNM.14.94
[5]
Pantel K, Brakenhoff R H. Nat. Rev. Cancer , 2004, 4: 448.

doi: 10.1038/nrc1370
[6]
Schroeder A, Heller D A, Winslow M M, Dahlman J E, Pratt G W, Langer R, Jacks T, Anderson D G. Nat. Rev. Cancer , 2012, 12: 39.

doi: 10.1038/nrc3180
[7]
Dotan E, Cohen S J, Alpaugh K R, Meropol N J. The Oncologist , 2009, 14: 1070.

doi: 10.1634/theoncologist.2009-0094
[8]
Dasgupta A, Lim A R, Ghajar C M. Mol. Oncol. , 2017, 11: 40.

doi: 10.1002/1878-0261.12022
[9]
Micalizzi D S, Maheswaran S, Haber D A. Genes Dev., 2017, 31: 1827.

doi: 10.1101/gad.305805.117
[10]
Dianat-Moghadam H, Azizi M, Eslami-S Z, Cortes-Hernandez L E, Heidarifard M, Nouri M, Alix-Panabieres C. Cancers ( Basel), 2020, 12: 867.

doi: 10.3390/cancers12040867
[11]
Chaffer C L, Weinberg R A. Science , 2011, 331: 1559.

doi: 10.1126/science.1203543
[12]
Alix-Panabieres C, Pantel K. Nat. Rev. Cancer , 2014, 14: 623.

doi: 10.1038/nrc3820
[13]
Stott S L, Lee R J, Nagrath S, Yu M, Miyamoto D T, Ulkus L, Inserra E J, Ulman M, Springer S, Nakamura Z, Moore A L, Tsukrov D I, Kempner M E, Dahl D M, Wu C L, Iafrate A J, Smith M R, Tompkins R G, Sequist L V, Toner M, Haber D A, Maheswaran S. Sci. Transl. Med., 2010, 2: 23.
[14]
Banys M, Krawczyk N, Becker S, Jakubowska J, Staebler A, Wallwiener D, Fehm T, Rothmund R. Breast Cancer Res. Treat , 2012, 132: 121.

doi: 10.1007/s10549-011-1569-0
[15]
Seal S H. Cancer, 1964, 17: 637.

doi: 10.1002/(ISSN)1097-0142
[16]
Vona G, Sabile A, Louha M, Sitruk V, Romana S, Schutze K, Capron F, Franco D, Pazzagli M, Vekemans M, Lacour B, Brechot C, Paterlini-Brechot P. Am. J. Pathol., 2000, 156: 57.

doi: 10.1016/S0002-9440(10)64706-2
[17]
Lee H J, Oh J H, Oh J M, Park J M, Lee J G, Kim M S, Kim Y J, Kang H J, Jeong J, Kim S I, Lee S S, Choi J W, Huh N. Angew. Chem. Int. Ed. , 2013, 52: 8337.

doi: 10.1002/anie.v52.32
[18]
Gascoyne P R, Noshari J, Anderson T J, Becker F F. Electrophoresis , 2009, 30: 1388.

doi: 10.1002/elps.v30:8
[19]
Moon H S, Kwon K, Kim S I, Han H, Sohn J, Lee S, Jung H I. Lab Chip , 2011, 11: 1118.

doi: 10.1039/c0lc00345j
[20]
Huang S, Wu M, Lin Y, Hsieh C, Yang C, Lin H, Tseng C, Lee G. Lab Chip , 2013, 13: 1371.

doi: 10.1039/c3lc41256c
[21]
Cristofanilli M, Budd G T, Ellis M J, Stopeck A, Matera J, Miller M C, Reuben J M, Doyle G V, Allard W J, Terstappen L W, Hayes D F. N. Engl. J. Med., 2004, 351: 781.

doi: 10.1056/NEJMoa040766
[22]
Wen C Y, Wu L L, Zhang Z L, Liu Y L, Wei S Z, Hu J, Tang M, Sun E Z, Gong Y P, Yu J, Pang D W. ACS Nano , 2014, 8: 941.

doi: 10.1021/nn405744f
[23]
Jo S M, Lee J J, Heu W, Kim H S. Small , 2015, 11: 1975.

doi: 10.1002/smll.v11.16
[24]
Xie M, Lu N N, Cheng S B, Wang X Y, Wang M, Guo S, Wen C Y, Hu J, Pang D W, Huang W H. Anal. Chem., 2014, 86: 4618.

doi: 10.1021/ac500820p
[25]
Chen W, Weng S, Zhang F, Allen S, Li X, Bao L, Lam R H, Macoska J A, Merajver S D, Fu J. ACS Nano , 2013, 7: 566.

doi: 10.1021/nn304719q
[26]
Wang S, Wang H, Jiao J, Chen K J, Owens G E, Kamei K, Sun J, Sherman D J, Behrenbruch C P, Wu H, Tseng H R. Angew. Chem. Int. Ed., 2009, 48: 8970.

doi: 10.1002/anie.v48:47
[27]
Zhang N, Deng Y, Tai Q, Cheng B, Zhao L, Shen Q, He R, Hong L, Liu W, Guo S, Liu K, Tseng H R, Xiong B, Zhao X Z. Adv. Mater., 2012, 24: 2756.

doi: 10.1002/adma.v24.20
[28]
Wan Y, Mahmood M A, Li N, Allen P B, Kim Y T, Bachoo R, Ellington A D, Iqbal S M. Cancer , 2012, 118: 1145.

doi: 10.1002/cncr.26349
[29]
Guo S, Xu J, Xie M, Huang W, Yuan E, Liu Y, Fan L, Cheng S, Liu S, Wang F, Yuan B, Dong W, Zhang X, Huang W, Zhou X. ACS Appl. Mater. Interfaces , 2016, 8: 15917.

doi: 10.1021/acsami.6b04002
[30]
Zhang F, Jiang Y, Liu X, Meng J, Zhang P, Liu H, Yang G, Li G, Jiang L, Wan L J, Hu J S, Wang S. Nano Lett., 2016, 16: 766.

doi: 10.1021/acs.nanolett.5b04731
[31]
Yu X, He R, Li S, Cai B, Zhao L, Liao L, Liu W, Zeng Q, Wang H, Guo S S, Zhao X Z. Small , 2013, 9: 3895.

doi: 10.1002/smll.v9.22
[32]
Mohamadi R M, Besant J D, Mepham A, Green B, Mahmoudian L, Gibbs T, Ivanov I, Malvea A, Stojcic J, Allan A L, Lowes L E, Sargent E H, Nam R K, Kelley S O. Angew. Chem. Int. Ed., 2015, 54: 139.
[33]
Stott S L, Hsu C H, Tsukrov D I, Yu M, Miyamoto D T, Waltman B A, Rothenberg S M, Shah A M, Smas M E, Korir G K, Floyd F J, Gilman A J, Lord J B, Winokur D, Springer S, Irimia D, Nagrath S, Sequist L V, Lee R J, Isselbacher K J, Maheswaran S, Haber D A, Toner M. Proc. Natl. Acad. Sci. U. S. A., 2010, 107: 18392.
[34]
Sheng W, Chen T, Tan W, Fan Z H. ACS Nano , 2013, 7: 7067.

doi: 10.1021/nn4023747
[35]
Yoon H J, Kim T H, Zhang Z, Azizi E, Pham T M, Paoletti C, Lin J, Ramnath N, Wicha M S, Hayes D F, Simeone D M, Nagrath S. Nat. Nanotechnol. , 2013, 8: 735.

doi: 10.1038/nnano.2013.194
[36]
Cheng S B, Xie M, Xu J Q, Wang J, Lv S W, Guo S, Shu Y, Wang M, Dong W G, Huang W H. Anal. Chem. , 2016, 88: 6773.

doi: 10.1021/acs.analchem.6b01130
[37]
Karabacak N M, Spuhler P S, Fachin F, Lim E J, Pai V, Ozkumur E, Martel J M, Kojic N, Smith K, Chen P I, Yang J, Hwang H, Morgan B, Trautwein J, Barber T A, Stott S L, Maheswaran S, Kapur R, Haber D A, Toner M. Nat. Protoc., 2014, 9: 694.

doi: 10.1038/nprot.2014.044
[38]
Poudineh M, Aldridge P M, Ahmed S, Green B J, Kermanshah L, Nguyen V, Tu C, Mohamadi R M, Nam R K, Hansen A, Sridhar S S, Finelli A, Fleshner N E, Joshua A M, Sargent E H, Kelley S O. Nat. Nanotechnol., 2017, 12: 274.

doi: 10.1038/nnano.2016.239
[39]
Ahmed M G, Abate M F, Song Y, Zhu Z, Yan F, Xu Y, Wang X, Li Q, Yang C. Angew. Chem. Int. Ed., 2017, 56: 10681.

doi: 10.1002/anie.201702675
[40]
Guo S, Huang H, Deng X, Chen Y, Jiang Z, Xie M, Liu S, Huang W, Zhou X. Nano Res., 2018, 11: 2592.

doi: 10.1007/s12274-017-1885-8
[41]
Huang D , Xiang N , Tang W L , Zhang X J , Ni Z H. Progress in Chemistry , 2015, 27: 882.

doi: 10.7536/PC150121
黄笛, 项南, 唐文来, 张鑫杰, 倪中华. 化学进展, 2015, 27: 882.

doi: 10.7536/PC150121
[42]
Pei H, Li L, Wang Y, Sheng R, Wang Y, Xie S, Shui L, Si H, Tang B. Anal. Chem., 2019, 91: 11078.

doi: 10.1021/acs.analchem.9b01647
[43]
Wu L, Tang M, Zhang Z, Qi C, Hu J, Ma X, Pang D. Anal. Chem., 2018, 90: 10518.

doi: 10.1021/acs.analchem.8b02585
[44]
Dong J, Jan Y J, Cheng J, Zhang R Y, Meng M, Smalley M, Chen P J, Tang X, Tseng P, Bao L, Huang T Y, Zhou D, Liu Y, Chai X, Zhang H, Zhou A, Agopian V G, Posadas E M, Shyue J J, Jonas S J, Weiss P S, Li M, Zheng G, Yu H H, Zhao M, Tseng H R, Zhu Y. Sci. Adv., 2019, 5: v9186.
[45]
Abdulla A, Liu W, Gholamipour-Shirazi A, Sun J, Ding X. Anal. Chem., 2018, 90: 4397.

doi: 10.1021/acs.analchem.7b04210
[46]
Kim J, Galanzha E I, Zaharoff D A, Griffin R J, Zharov V P. Mol. Pharmaceutics , 2013, 10: 813.

doi: 10.1021/mp300577s
[47]
Hartmann C, Patil R, Lin C P, Niedre M. Phys. Med. Biol., 2017, 63: 1T.
[48]
Pons T, Bouccara S, Loriette V, Lequeux N, Pezet S, Fragola A. ACS Nano , 2019, 13: 3125.

doi: 10.1021/acsnano.8b08463
[49]
Adonai N, Adonai N, Nguyen K N, Walsh J, Iyer M, Toyokuni T, Phelps M E, McCarthy T, McCarthy D W, Gambhir S S. Proc. Natl. Acad. Sci. U. S. A., 2002, 99: 3030.
[50]
Ahrens E T, Bulte J W. Nat. Rev. Immunol. Immunology , 2013, 13: 755.
[51]
Zhang H F, Maslov K, Stoica G, Wang L V. Nat. Biotechnol., 2006, 24: 848.

doi: 10.1038/nbt1220
[52]
Yi J, Backman V. Opt. Lett., 2012, 37: 4443.

doi: 10.1364/OL.37.004443
[53]
Kircher M F, Gambhir S S, Grimm J. Nat. Rev. Clin. Oncol., 2011, 8: 677.

doi: 10.1038/nrclinonc.2011.141
[54]
Kuo C W, Chueh D, Chen P. Nanobiotechnol., 2019, 17: 26.
[55]
Hu Y, Tang W, Cheng P, Zhou Q, Tian X, Wei X, He H. Cytometry A , 2019, 95( 6): 657.

doi: 10.1002/cyto.v95.6
[56]
Hai P, Zhou Y, Zhang R, Ma J, Li Y, Shao J Y, Wang L V. J. Biomed. Opt., 2017, 22: 41004.
[57]
Hai P, Qu Y, Li Y, Zhu L, Shmuylovich L, Cornelius L A, Wang L V. J. Biomed. Opt., 2020, 25: 1.
[58]
Dutta R, Liba O, Sorelle E D, Winetraub Y, Ramani V C, Jeffrey S S, Sledge G W, de la Zerda A. Nano Lett. , 2019, 19: 2334.

doi: 10.1021/acs.nanolett.8b05005
[59]
Suo Y, Gu Z, Wei X. Cytometry A , 2020, 97: 15.

doi: 10.1002/cyto.a.v97.1
[60]
Galanzha E, Zharov V. Cancers , 2013, 5: 1691.

doi: 10.3390/cancers5041691
[61]
Novak J, Georgakoudi I, Wei X, Prossin A, Lin C P. Opt. Lett., 2004, 29: 77.

doi: 10.1364/OL.29.000077
[62]
Georgakoudi I, Solban N, Novak J, Rice W L, Wei X, Hasan T, Lin C P. Cancer Res., 2004, 64: 5044.

doi: 10.1158/0008-5472.CAN-04-1058
[63]
Li Y, Guo J, Wang C, Fan Z, Liu G, Wang C, Gu Z, Damm D, Mosig A, Wei X. Cytometry A , 2011, 79: 848.
[64]
Guo J, Fan Z, Gu Z, Wei X. J. Innov. Opt. Health Sci . , 2012, 5: 1250027.

doi: 10.1142/S1793545812500277
[65]
Fan Z C, Yan J, Liu G D, Tan X Y, Weng X F, Wu W Z, Zhou J, Wei X B. Cancer Res., 2012, 7: 2683.
[66]
Yan J, Fan Z, Wu X, Xu M, Jiang J, Tan C, Wu W, Wei X, Zhou J. Cytometry A , 2015, 87: 1020.

doi: 10.1002/cyto.a.22782
[67]
Pang K, Xie C, Yang Z, Suo Y, Zhu X, Wei D, Weng X, Wei X, Gu Z. Cytometry A , 2018, 93: 517.

doi: 10.1002/cyto.a.v93.5
[68]
Yu Q, Yao Y, Zhu X, Gao Y, Chen Y, Wang R, Xu P, Wei X, Jiang L. Cytometry A , 2020, DOI: 10.1002/cyto.a.24014.
[69]
Aceto N, Bardia A, Miyamoto D T, Donaldson M C, Wittner B S, Spencer J A, Yu M, Pely A, Engstrom A, Zhu H, Brannigan B W, Kapur R, Stott S L, Shioda T, Ramaswamy S, Ting D T, Lin C P, Toner M, Haber D A, Maheswaran S. Cell , 2014, 158: 1110.

doi: 10.1016/j.cell.2014.07.013
[70]
Plaks V, Koopman C D, Werb Z. Science , 2013, 341: 1186.

doi: 10.1126/science.1235226
[71]
Au S H, Storey B D, Moore J C, Tang Q, Chen Y, Javaid S, Sarioglu A F, Sullivan R, Madden M W, O Keefe R, Haber D A, Maheswaran S, Langenau D M, Stott S L, Toner M. Proc. Natl. Acad. Sci. U. S. A. , 2016, 113: 4947.
[72]
Suo Y, Xie C, Zhu X, Fan Z, Yang Z, He H, Wei X. Cytometry A , 2017, 91: 250.

doi: 10.1002/cyto.a.23037
[73]
Cho E H, Wendel M, Luttgen M, Yoshioka C, Marrinucci D, Lazar D, Schram E, Nieva J, Bazhenova L, Morgan A, Ko A H, Korn W M, Kolatkar A, Bethel K, Kuhn P. Phys. Biol., 2012, 9: 16001.

doi: 10.1088/1478-3975/9/1/016001
[74]
Paterlini-Brechot P, Benali N L. Cancer Lett., 2007, 253: 180.

doi: 10.1016/j.canlet.2006.12.014
[75]
Kallergi G, Konstantinidis G, Markomanolaki H, Papadaki M A, Mavroudis D, Stournaras C, Georgoulias V, Agelaki S. Mol. Cancer Ther., 2013, 12: 1886.

doi: 10.1158/1535-7163.MCT-12-1167
[76]
Wei X, Sipkins D A, Pitsillides C M, Novak J, Georgakoudi I, Lin C P. Mol. Imaging , 2005, 4: 415.
[77]
Nolan J, Nedosekin D A, Galanzha E I, Zharov V P. Cytometry A , 2019, 95: 664.

doi: 10.1002/cyto.v95.6
[78]
Markovic S, Li S, Niedre M. J. Biomed. Opt., 2015, 20: 35005.
[79]
Zettergren E, Vickers D, Runnels J, Murthy S K, Lin C P, Niedre M. J. Biomed. Opt., 2012, 17: 37001.

doi: 10.1117/1.JBO.17.3.037001
[80]
Patil R A, Srinivasarao M, Amiji M M, Low P S, Niedre M. Mol. Imaging Biol. , 2020, DOI: 10.1007/s11307-020-01505-9.
[81]
Bartosik P B, Fitzgerald J E, El K M, Yaseen M A, Vinogradov S A, Niedre M. Int. J. Nanomed., 2020, 15: 1709.

doi: 10.2147/IJN
[82]
Tan X, Patil R, Bartosik P, Runnels J M, Lin C P, Niedre M. Sci. Rep., 2019, 9: 3366.

doi: 10.1038/s41598-019-40143-2
[83]
Woodard H Q, White D R. Br. J. Radiol. , 1986, 59: 1209.

doi: 10.1259/0007-1285-59-708-1209
[84]
Suo Y, Liu T, Xie C, Wei D, Tan X, Wu L, Wang X, He H, Shi G, Wei X, Shi C. Cytometry A , 2015, 87: 878.

doi: 10.1002/cyto.a.22711
[85]
Labelle M, Begum S, Hynes R O. Proc. Natl. Acad. Sci. U. S. A. , 2014, 111: 3053.
[86]
Ding Y, Wang J, Fan Z, Wei D, Shi R, Luo Q, Zhu D, Wei X. Biomed. Opt .Express , 2013, 4: 2518.

doi: 10.1364/BOE.4.002518
[87]
Zharov V P, Galanzha E I, Shashkov E V, Kim J, Khlebtsov N G, Tuchin V V. J. Biomed. Opt., 2007, 12: 51503.

doi: 10.1117/1.2793746
[88]
Galanzha E I, Shashkov E V, Spring P M, Suen J Y, Zharov V P. Cancer Res., 2009, 69: 7926.

doi: 10.1158/0008-5472.CAN-08-4900
[89]
Galanzha E I, Shashkov E V, Kelly T, Kim J, Yang L, Zharov V P. Nat. Nanotechnol., 2009, 4: 855.

doi: 10.1038/nnano.2009.333
[90]
Galanzha E I, Kim J, Zharov V P. J. Biophoton., 2009, 2: 725.

doi: 10.1002/jbio.v2:12
[91]
Galanzha E I, Kokoska M S, Shashkov E V, Kim J, Tuchin V V, Zharov V P. J. Biophoton. , 2009, 2: 528.

doi: 10.1002/jbio.v2:8/9
[92]
Nedosekin D A, Juratli M A, Sarimollaoglu M, Moore C L, Rusch N J, Smeltzer M S, Zharov V P, Galanzha E I. J. Biophoton., 2013, 6: 523.

doi: 10.1002/jbio.v6.6/7
[93]
de la Zerda A, Kim J W, Galanzha E I, Gambhir S S, Zharov V P. Contrast Media Mol. Imaging , 2011, 6: 346.

doi: 10.1002/cmmi.455
[94]
Juratli M A, Sarimollaoglu M, Siegel E R, Nedosekin D A, Galanzha E I, Suen J Y, Zharov V P. Head Neck , 2014, 36: 1207.

doi: 10.1002/pro.v36.8
[95]
Galanzha E I, Menyaev Y A, Yadem A C, Sarimollaoglu M, Juratli M A, Nedosekin D A, Foster S R, Jamshidi-Parsian A, Siegel E R, Makhoul I, Hutchins L F, Suen J Y, Zharov V P. Sci. Transl. Med., 2019, 11: 5857.
[96]
Sarimollaoglu M, Nedosekin D A, Menyaev Y A, Juratli M A, Zharov V P. Photoacoustics , 2014, 2: 1.

doi: 10.1016/j.pacs.2013.11.002
[97]
Moreau J E, Anderson K, Mauney J R, Nguyen T, Kaplan D L, Rosenblatt M. Cancer Res., 2007, 67: 10304.

doi: 10.1158/0008-5472.CAN-07-2483
[98]
Lee J, Li M, Milwid J, Dunham J, Vinegoni C, Gorbatov R, Iwamoto Y, Wang F, Shen K, Hatfield K, Enger M, Shafiee S, McCormack E, Ebert B L, Weissleder R, Yarmush M L, Parekkadan B. Proc. Natl. Acad. Sci. U. S. A. , 2012, 109: 19638.
[99]
Azarin S M, Yi J, Gower R M, Aguado B A, Sullivan M E, Goodman A G, Jiang E J, Rao S S, Ren Y, Tucker S L, Backman V, Jeruss J S, Shea L D. Nat. Commun., 2015, 6: 8094.

doi: 10.1038/ncomms9094
[100]
Saucedo-Zeni N, Mewes S, Niestroj R, Gasiorowski L, Murawa D, Nowaczyk P, Tomasi T, Weber E, Dworacki G, Morgenthaler N G, Jansen H, Propping C, Sterzynska K, Dyszkiewicz W, Zabel M, Kiechle M, Reuning U, Schmitt M, Lücke K. Int. J. Oncol., 2012, 41: 1241.

doi: 10.3892/ijo.2012.1557
[101]
Gallerani G, Cocchi C, Bocchini M, Piccinini F, Fabbri F. J. Vis. Exp., 2017, 130: 56930.
[102]
Mandair D, Vesely C, Ensell L, Lowe H, Spanswick V, Hartley J A, Caplin M E, Meyer T. Endocr. Relat. Cancer , 2016, 23: 29.
[103]
Gasiorowski L, Dyszkiewicz W, Zielinski P. Neoplasma , 2017, 64: 938.

doi: 10.4149/neo_2017_618
[104]
El-Heliebi A, Hille C, Laxman N, Svedlund J, Haudum C, Ercan E, Kroneis T, Chen S, Smolle M, Rossmann C, Krzywkowski T, Ahlford A, Darai E, von Amsberg G, Alsdorf W, Konig F, Lohr M, de Kruijff I, Riethdorf S, Gorges T M, Pantel K, Bauernhofer T, Nilsson M, Sedlmayr P. Clin. Chem., 2018, 64: 536.

doi: 10.1373/clinchem.2017.281295
[105]
Markou A, Lazaridou M, Paraskevopoulos P, Chen S, Swierczewska M, Budna J, Kuske A, Gorges T M, Joosse S A, Kroneis T, Zabel M, Sedlmayr P, Alix-Panabieres C, Pantel K, Lianidou E S. Clin. Chem., 2018, 64: 297.

doi: 10.1373/clinchem.2017.275503
[106]
Chen S, Tauber G, Langsenlehner T, Schmolzer L M, Potscher M, Riethdorf S, Kuske A, Leitinger G, Kashofer K, Czyz Z T, Polzer B, Pantel K, Sedlmayr P, Kroneis T, El-Heliebi A. Cancers ( Basel), 2019, 11: 933.

doi: 10.3390/cancers11070933
[107]
Li J B , Geng C Z , Yan M , Wang Y S , Ouyang Q C , Yin Y M , Wu L N , He J , Jiang Z F. Zhonghua Yi Xue Za Zhi , 2017, 97: 1857.
李健斌, 耿翠芝, 闫敏, 王永胜, 欧阳取长, 殷咏梅, 武林楠, 贺佳, 江泽飞. 中华医学杂志, 2017, 97: 1857.
[108]
Dizdar L, Fluegen G, van Dalum G, Honisch E, Neves R P, Niederacher D, Neubauer H, Fehm T, Rehders A, Krieg A, Knoefel W T, Stoecklein N H. Mol. Oncol., 2019, 13: 1548.

doi: 10.1002/mol2.2019.13.issue-7
[109]
Wang H, Yue G, Dong C, Wu F, Wei J, Yang Y, Zou Z, Wang L, Qian X, Zhang T, Liu B. ACS Appl. Mater. Interfaces , 2014, 6: 4550.

doi: 10.1021/am500394j
[110]
Zhang H, Jia Z, Wu C, Zang L, Yang G, Chen Z, Tang B. ACS Appl. Mater. Interfaces , 2015, 7: 20477.

doi: 10.1021/acsami.5b06874
[111]
Jia M, Mao Y, Wu C, Wang S, Zhang H. Anal. Chim. Acta , 2019, 1082: 136.

doi: 10.1016/j.aca.2019.07.051
[112]
Cheng S B, Wang M, Zhang C, Chen M M, Wang Y K, Tian S, Zhan N, Dong W G, Xie M, Huang W H. Anal. Chem. , 2020, 92: 5447.

doi: 10.1021/acs.analchem.0c00203
[113]
Vermesh O, Aalipour A, Ge T J, Saenz Y, Guo Y, Alam I S, Park S, Adelson C N, Mitsutake Y, Vilches-Moure J, Godoy E, Bachmann M H, Ooi C C, Lyons J K, Mueller K, Arami H, Green A, Solomon E I, Wang S X, Gambhir S S. Nat. Biomed. Eng., 2018, 2: 696.

doi: 10.1038/s41551-018-0257-3
[114]
Hamza B, Ng S R, Prakadan S M, Delgado F F, Chin C R, King E M, Yang L F, Davidson S M, Degouveia K L, Cermak N, Navia A W, Winter P S, Drake R S, Tammela T, Li C M, Papagiannakopoulos T, Gupta A J, Shaw Bagnall J, Knudsen S M, Vander Heiden M G, Wasserman S C, Jacks T, Shalek A K, Manalis S R. Proc. Natl. Acad. Sci. U. S. A., 2019, 116: 2232.
[115]
Tang M, Xia H, Xu C, Feng J, Ren J, Miao F, Wu M, Wu L, Pang D, Chen G, Zhang Z. Anal. Chem., 2019, 91: 15260.

doi: 10.1021/acs.analchem.9b04286
[1] Dang Zhang, Xi Wang, Lei Wang. Biomedical Applications of Enzyme-Powered Micro/Nanomotors [J]. Progress in Chemistry, 2022, 34(9): 2035-2050.
[2] Jiali Wang, Ling Zhu, Chen Wang, Shengbin Lei, Yanlian Yang. Nanotechnology for Detection of Circulating Tumor Cells and Extracellular Vesicles [J]. Progress in Chemistry, 2022, 34(1): 178-197.
[3] Xiaodong Jing, Ying Sun, Bing Yu, Youqing Shen, Hao Hu, Hailin Cong. Rational Design of Tumor Microenvironment Responsive Drug Delivery Systems [J]. Progress in Chemistry, 2021, 33(6): 926-941.
[4] Jiajia Wang, Huiying Wu, Renfeng Dong, Yuepeng Cai. Micro/Nanomotors on the Way to Intelligent Cancer Diagnosis, Delivery and Therapy [J]. Progress in Chemistry, 2021, 33(5): 883-894.
[5] Yunxue Wu, Hengyi Zhang, Yu Liu. Application of Azobenzene Derivative Probes in Hypoxia Cell Imaging [J]. Progress in Chemistry, 2021, 33(3): 331-340.
[6] Ziru Sun, Shengnan Liu, Qingzhi Gao. Development of Anticancer Drugs Targeting Glucose Transporters(GLUTs) [J]. Progress in Chemistry, 2020, 32(12): 1869-1878.
[7] Xinyi Lai, Zhiyong Wang, Yongtai Zheng, Yongming Chen. Nanoscale Metal Organic Frameworks for Drug Delivery [J]. Progress in Chemistry, 2019, 31(6): 783-790.
[8] Bingde Zheng, Yuanyuan Zhao, Hongcai Li, Biyuan Zheng, Meirong Ke, Jiandong Huang*. Activatable Photodynamic Anticancer Photosensitizers [J]. Progress in Chemistry, 2018, 30(9): 1403-1414.
[9] Liang He, Caiping Tan, Qian Cao, Zongwan Mao. Application of Phosphorescent Cyclometalated Iridium(Ⅲ) Complexes in Cancer Treatment [J]. Progress in Chemistry, 2018, 30(10): 1548-1556.
[10] Juan Shen, Yang Zhu, Hongdong Shi, Yangzhong Liu. Multifunctional Nanodrug Delivery Systems for Platinum-Based Anticancer Drugs [J]. Progress in Chemistry, 2018, 30(10): 1557-1572.
[11] Gong Zhaocui, Yin Chao, Zhao Hui, Lu Xiaomei, Fan Quli, Huang Wei. Light-Controlled Nanocarriers for Drug Release [J]. Progress in Chemistry, 2016, 28(9): 1387-1396.
[12] Jiang Ge, Luo Feng, Xu Yaozhong, Zhang Xiaohui. UVA Assisted 4-Thiothymidine for Cancer Treatment [J]. Progress in Chemistry, 2016, 28(8): 1224-1237.
[13] Zheng Xiaohui, Xia Lixin, Mao Zongwan. The New Anticancer Platinum Complex Designed on the Basis of Nucleic Acid [J]. Progress in Chemistry, 2016, 28(7): 1029-1038.
[14] Ye Jiqing, Yue Xiaohong, Sun Liping. Small Molecule Inhibitors of IL-6/STAT3 Signaling [J]. Progress in Chemistry, 2016, 28(7): 1099-1111.
[15] Huang Di, Xiang Nan, Tang Wenlai, Zhang Xinjie, Ni Zhonghua. Microfluidics-Based Circulating Tumor Cells Separation [J]. Progress in Chemistry, 2015, 27(7): 882-912.