In vivo Self-assembled Peptide Nanoprobes for Disease Diagnosis

Abstract

I n vivo imaging is creating great opportunities for disease diagnosis as a research tool. Probes are usually used to observe physiological structures in vivo clearly. Recent progresses of nanoprobes are important for the generation of high resolution and high contrast images required by accurate and precision disease diagnosis. In vivo self-assembled peptide(SAP) nanoprobes are playing major roles in in vivo imaging by modularity of design, high imaging contrast, response to the location of the lesion, and long-time retention in the lesion. And the response to lesion and long-term retention in there can enhance imaging sensitivity and specificity of in vivo SAP nanoprobes. Therefore, in vivo SAP nanoprobes are simple ancillary contrast entities to optimize the imaging effect. In this review, the recent progress of in vivo SAP nanoprobes for in vivo imaging, from molecular design of peptides to biomedical and clinical applications including disease diagnosis and disease-related molecular imaging is systematically summarized. We evaluate their ability, including sensitivity and specificity to provide relevant information under preoperative and during surgery circumstances and critically their likelihood to be clinically translated. Finally, a brief outlook on remaining challenges and potential directions for future research in this area is presented.

Keywords

In vivo self-assembly / Nanoprobe / Peptide / Disease diagnosis

References

[1] Lee S, Huang H, Zelen M. Stat. Methods. Med. Res., 2004, 13: 443.

[2] Dou K, Huang W, Xiang Y, Li S, Liu Z. Anal. Chem., 2020, 92: 4177.

[3] Heo C H, Sarkar A R, Baik S H, Jung T S, Kim J J, Kang H, Mook-Jung I, Kim H M. Chem. Sci., 201, 7: 4600.

[4] Zhang J, Smaga L P, Satyavolu N S R, Chan J, Lu Y. J. Am. Chem. Soc., 2017, 139: 17225.

[5] Xiao L, Zhang Y, Berr S S, Chordia M D, Pramoonjago P, Pu L, Pan D. Mol. Imaging, 2012, 11: 372.

[6] Li C Y, Wang Q B. ACS Nano, 2018, 12: 9654.

[7] An H-W, Hou D, Zheng R, Wang M-D, Zeng X-Z, Xiao W-Y, Yan T-D, Wang J-Q, Zhao C-H, Cheng L-M, Zhang J-M, Wang L, Wang Z-Q, Wang H, Xu W. ACS Nano, 2020, 14: 927.

[8] An H-W, Li L-L, Wang Y, Wang Z, Hou D, Lin Y-X, Qiao S-L, Wang M-D, Yang C, Cong Y, Ma Y, Zhao X-X, Cai Q, Chen W-T, Lu C-Q, Xu W, Wang H, Zhao Y. Nat. Commun., 2019, 10: 4861.

[9] Smith B R, Gambhir S S. Chem. Rev., 2017, 117: 901.

[10] Qi G-B, Gao Y-J, Wang L, Wang H. Adv. Mater., 2018, 30: 1703444.

[11] Zheng R., Yang J., Mamuti M., Hou D. Y., An H. W., Zhao Y. L., Wang H., Angew. Chem., Int. Ed., 2021, DOI: https://doi.org/10.1002/anie.202015126

[12] Lu S Z, Guo X Y, Zou M S, Zheng Z Q, Li Y C, Li X D, Li L L, Wang H. Adv. Healthcare Mater., 2020, 9: 8.

[13] Levin A, Hakala T A, Schnaider L, Bernardes G J L, Gazit E, Knowles T P J. Nat. Rev. Chem., 2020, 4: 615.

[14] Chen J, Zou X N. Bioact. Mater., 2019, 4: 120.

[15] Tao K, Makam P, Aizen R, Gazit E. Science, 2017, 358: eaa-9756.

[16] Yang J, An H-W, Wang H. ACS Appl. Bio Mater., 2021, 4: 24.

[17] Zhang L, Wang T, Shen Z, Liu M. Adv. Mater., 201, 28: 1044.

[18] Ulijn R V, Smith A M. Chem. Soc. Rev., 2008, 37: 664.

[19] Papapostolou D, Smith A M, Atkins E D T, Oliver S J, Ryadnov M G, Serpell L C, Woolfson D N. Proc. Natl. Acad. Sci., 2007, 104: 10853.

[20] Eisenberg D. Proc. Natl. Acad. Sci., 2003, 100: 11207.

[21] Aggeli A, Nyrkova I A, Bell M, Harding R, Carrick L, McLeish T C B, Semenov A N, Boden N. Proc. Natl. Acad. Sci., 2001, 98: 11857.

[22] Zhang S, Holmes T, Lockshin C, Rich A. Proc. Natl. Acad. Sci., 1993, 90: 3334.

[23] Kunitake T. Angew. Chem., Int. Ed., 1992, 31: 709.

[24] Ren C, Wang Z, Wang Q, Yang C, Liu J. Small Methods, 2020, 4: 1900403.

[25] Shi H, Kwok R T K, Liu J, Xing B, Tang B Z, Liu B. J. Am. Chem. Soc., 2012, 134: 17972.

[26] Zhang D, Qi G B, Zhao Y X, Qiao S L, Yang C, Wang H. Adv. Mater., 2015, 27: 6125.

[27] Gazit E. Chem. Soc. Rev., 2007, 36: 1263.

[28] Ma M, Kuang Y, Gao Y, Zhang Y, Gao P, Xu B. J. Am. Chem. Soc., 2010, 132: 2719.

[29] Ishizaki J, Waki Y, Takahashi-Nishioka T, Yokogawa K, Miyamoto K. J. Bone Miner. Metab., 2009, 27: 1.

[30] Ebenhan T, Zeevaart J R, Venter J D, Govender T, Kruger G H, Jarvis N V, Sathekge M M. J. Nucl. Med., 2014, 55: 308.

[31] Qi G B, Gao Y J, Wang L, Wang H. Adv. Mater., 2018, 30: 34.

[32] Moradi-Marjaneh R, Hassanian S M, Mehramiz M, Rezayi M, Ferns G A, Khazaei M, Avan A. J. Cell Physiol., 2019, 234: 10072.

[33] Dai Y, Yang Z, Cheng S, Wang Z, Zhang R, Zhu G, Wang Z, Yung B C, Tian R, Jacobson O. J. A. M., 2018, 30: 1704877.

[34] Liu Y, Yang Z, Huang X, Yu G, Wang S, Zhou Z, Shen Z, Fan W, Liu Y, Davisson M, Kalish H, Niu G, Nie Z, Chen X. ACS Nano, 2018, 12: 8129.

[35] Tonge S R, Tighe B J. Adv. Drug Delivery Rev., 2001, 53: 109.

[36] Anajafi T, Mallik S. Ther. Delivery, 2015, 6: 521.

[37] He H, Lin X, Wu D, Wang J, Guo J, Green D R, Zhang H, Xu B. Cell Rep. Phys. Sci., 2020, 1: 100270.

[38] Feng Z, Wang H, Wang F, Oh Y, Berciu C, Cui Q, Egelman E H, Xu B. Cell Rep. Phys. Sci., 2020, 1: 100085.

[39] Tan W., Zhang Q., Wang J., Yi M., He H., Xu B., Angew. Chem., Int. Ed., 2021, DOI: https://doi.org/10.1002/anie.202102601

[40] Wolf P L. Jour. Clin. Lab. Anal., 1994, 8: 172.

[41] Zhou J, Du X W, Berciu C, He H J, Shi J F, Nicastro D, Xu B. Chem, 201, 1: 19.

[42] Ding D, Liang J, Shi H, Kwok R T K, Gao M, Feng G, Yuan Y, Tang B Z, Liu B. J. Mater. Chem. B, 2014, 2: 231.

[43] Xu T, Cai Y, Zhong X, Zhang L, Zheng D, Gao Z, Pan X, Wang F, Chen M, Yang Z. Chem. Commun., 2019, 55: 7175.

[44] Hajdin K, D’Alessandro V, Niggli F K, Schäfer B W, Bernasconi M. PLoS One, 2010, 5: e10445.

[45] Hosaka M, Nagahama M, Kim W S, Watanabe T, Hatsuzawa K, Ikemizu J, Murakami K, Nakayama K. J. Biol. Chem., 1991, 266: 12127.

[46] Zhao X, Lv G, Peng Y, Liu Q, Li X, Wang S, Li K, Qiu L, Lin J. ChemBioChem, 2018, 19: 1060.

[47] Gao D G, Ma J Z, Guo H Q. New J. Chem., 2010, 34: 2034.

[48] Philippova O E, Hourdet D, Audebert R, Khokhlov A R. Macromolecules, 1997, 30: 8278.

[49] Duan Z, Gao Y J, Qiao Z Y, Qiao S, Wang Y, Hou C, Wang L, Wang H. Nanotechnology, 2015, 26: 355703.

[50] Moyer T J, Finbloom J A, Chen F, Toft D J, Cryns V L, Stupp S I. J. Am. Chem. Soc., 2014, 136: 14746.

[51] Yang P P, Luo Q, Qi G B, Gao Y J, Li B N, Zhang J P, Wang L, Wang H. Adv. Mater., 2017, 29: 9.

[52] Urry D W. J. Phys. Chem. B, 1997, 101: 11007.

[53] Sun M M, Peng D, Hao H J, Hu J, Wang D L, Wang K, Liu J, Guo X M, Wei Y, Gao W P. ACS Appl. Mater. Interfaces, 2017, 9: 10453.

[54] Yang P P, Zhao X X, Xu A P, Wang L, Wang H. J. Mat. Chem. B, 201, 4: 2662.

[55] Puklin-Faucher E, Vogel V. J. Biol. Chem., 2009, 284: 36557.

[56] Xiong J-P, Stehle T, Diefenbach B, Zhang R, Dunker R, Scott D L, Joachimiak A, Goodman S L, Arnaout M A. Science, 2001, 294: 339.

[57] Chen J F, Takagi J, Xie C, Xiao T, Luo B H, Springer T A. J. Biol. Chem., 2004, 279: 55556.

[58] Xu A P, Yang P P, Yang C, Gao Y J, Zhao X X, Luo Q, Li X D, Li L Z, Wang L, Wang H. Nanoscale, 201, 8: 14078.

[59] Xiao W-Y, Wang Y, An H-W, Hou D, Mamuti M, Wang M-D, Wang J, Xu W, Hu L, Wang H. ACS Appl. Mater. Interfaces, 2020, 12: 40042.

[60] Wang Z Q, An H W, Hou D Y, Wang M D, Zeng X Z, Zheng R, Wang L, Wang K L, Wang H, Xu W H. Adv. Mater., 2019, 31: 9.

[61] Zhan J, Cai Y B, He S S, Wang L, Yang Z M. Angew. Chem. Int. Ed., 2018, 57: 1813.

[62] White E H, Field G F, McCapra F. J. Am. Chem. Soc., 1963, 85: 337.

[63] Liang G L, Ren H J, Rao J H. Nat. Chem., 2010, 2: 54.

[64] Ye D J, Liang G L, Ma M L, Rao J H. Angew. Chem. Int. Ed., 2011, 50: 2275.

[65] Ye D J, Shuhendler A J, Cui L N, Tong L, Tee S S, Tikhomirov G, Felsher D W, Rao J H. Nat. Chem., 2014, 6: 519.

[66] Gao Y, Shi J, Yuan D, Xu B. Nat. Commun., 2012, 3: 1033.

[67] Lee M H, Kim J S, Sessler J L. J. Am. Chem. Soc., 2015, 44: 4185.

[68] Luo J., Xie Z., Lam J. W. Y., Cheng L., Chen H., Qiu C., Kwok H. S., Zhan X., Liu Y., Zhu D., Tang B. Z., Chem. Commun., 2001, 1740

[69] Zhu C, Kwok R T K, Lam J W Y, Tang B Z. ACS Appl. Bio Mater., 2018, 1: 1768.

[70] Kenry, Chong K C, Liu B. Acc. Chem. Res., 2019, 52: 3051.

[71] Mei J, Huang Y, Tian H. ACS Appl. Mater. Interfaces, 2018, 10: 12217.

[72] Fleming S, Ulijn R V. Chem. Soc. Rev., 2014, 43: 8150.

[73] Reches M, Gazit E. Science, 2003, 300: 625.

[74] Görbitz C H. Chemistry: A European Journal, 2001, 7: 5153.

[75] Tao K, Levin A, Adler-Abramovich L, Gazit E. Chem. Soc. Rev., 201, 45: 3935.

[76] Wang H, Feng Z, Xu B. Angew. Chem., Int. Ed., 2019, 131: 10532.

[77] Shy A N, Kim B J, Xu B. Matter, 2019, 1: 1127.

[78] Zhang Z., Zhang X., Xu X., Li Y., Li Y., Zhong D., He Y., Gu Z., 2015, 25, 5250

[79] Zhang L, Jing D, Jiang N, Rojalin T, Baehr C M, Zhang D, Xiao W, Wu Y, Cong Z, Li J J, Li Y, Wang L, Lam K S. Nat. Nanotechnol., 2020, 15: 145.

[80] Cheng D B, Wang D, Gao Y J, Wang L, Qiao Z Y, Wang H. J. Am. Chem. Soc., 2019, 141: 4406.

[81] Zhao X X, Li L L, Zhao Y, An H W, Cai Q, Lang J Y, Han X X, Peng B, Fei Y, Liu H, Qin H, Nie G J, Wang H. Angew. Chem., Int. Ed., 2019, 57: 15287.

[82] Deng Y, Zhan W, Liang G. Adv. Healthcare Mater., 2021, 10: 2001211.

[83] Pan D, Boon-Unge K, Govitrapong P, Zhou J. Oncol. Lett., 2011, 2: 1309.

[84] Blankenberg F G. J. Nucl. Med., 2008, 49: 81.

[85] Brindle K. Nat. Rev. Cancer, 2008, 8: 94.

[86] Shen B, Jeon J, Palner M, Ye D, Shuhendler A, Chin F T, Rao J. Angew. Chem. Int. Ed., 2013, 52: 10511.

[87] Edgington L E, Berger A B, Blum G, Albrow V E, Paulick M G, Lineberry N, Bogyo M. Nat. Med., 2009, 15: 967.

[88] Ye D, Shuhendler A J, Cui L, Tong L, Tee S S, Tikhomirov G, Felsher D W, Rao J. Nat. Chem., 2014, 6: 519.

[89] Coppola J M, Bhojani M S, Ross B D, Rehemtulla A. Neoplasia, 2008, 10: 363.

[90] de Cicco R L, Bassi D E, Benavides F, Conti C J, Klein-Szanto A J P. Mol. Carcinog., 2007, 46: 654.

[91] Yuan Y, Zhang J, Cao Q, An L, Liang G. Anal. Chem., 2015, 87: 6180.

[92] Dragulescu-Andrasi A, Kothapalli S R, Tikhomirov G A, Rao J, Gambhir S S. J. Am. Chem. Soc., 2013, 135: 110152.

[93] Brooks P C, Strömblad S, Sanders L C, von Schalscha T L, Aimes R T, Stetler-Stevenson W G, Quigley J P, Cheresh D A. Cell, 199, 85: 683.

[94] Pacheco M M, Mourao M, Mantovani E B, Nishimoto I N, Mitzi Brentani M. Clin. Exp. Metastasis, 1998, 16: 577.

[95] Remacle A G, Noël A, Duggan C, McDermott E, O’Higgins N, Foidart J M, Duffy M J. Br. J. Cancer, 1998, 77: 926.

[96] Baker E A, Bergin F G, Leaper D J. Br. J. Surg., 2000, 87: 1215.

[97] Kuniyasu H, Troncoso P, Johnston D, Bucana C D, Pettaway C A. Clin. Cancer Res., 2000, 6: 2295.

[98] Sier C F M, Kubben F, Ganesh S, Heerding M M, Griffioen G, Hanemaaijer R, van Krieken J, Lamers C, Verspaget H W. Br. J. Cancer, 199, 74: 413.

[99] Zhang X, Bresee J, Fields G B, Edwards W B. Bioorg. Med. Chem. Lett., 2014, 24: 3786.

[100] López-Otín C, Matrisian L M. Nat. Rev. Cancer, 2007, 7: 800.

[101] Sinha A A, Jamuar M P, Wilson M J, Rozhin J, Sloane B F. Prostate, 2001, 49: 172.

[102] Ryu J H, Kim S A, Koo H, Yhee J Y, Lee A, Na J H, Youn I, Choi K, Kwon I C, Kim B-S, Kim K. J. Mater. Chem., 2011, 21: 17631.

[103] Wang H, Feng Z, Xu B. Adv. Drug Delivery Rev., 2017, 110: 102. 111

[104] Zhang K, Gao Y-J, Yang P-P, Qi G-B, Zhang J-P, Wang L, Wang H. Adv. Healthcare Mater., 2018, 7: 1800344.

[105] He P-P, Li X-D, Wang L, Wang H. Acc. Chem. Res., 2019, 52: 367.

[106] Qi G-B, Gao Y-J, Wang L, Wang H. Adv. Mater., 2018, 30: 1703444.

[107] Yang P-P, Luo Q, Qi G-B, Gao Y-J, Li B-N, Zhang J-P, Wang L, Wang H. Adv. Mater., 2017, 29: 1605869.

[108] Esler W P, Stimson E R, Ghilardi J R, Lu Y-A, Felix A M, Vinters H V, Mantyh P W, Lee J P, Maggio J E. Biochemistry, 199, 35: 13914.

[109] Yang P-P, Zhao X-X, Xu A-P, Wang L, Wang H. J. Mater. Chem. B, 201, 4: 2662.

[110] Yuan Y, Zhang J, Qi X, Li S, Liu G, Siddhanta S, Barman I, Song X, McMahon M T, Bulte J W M. Nat. Mater., 2019, 18: 1376.

[111] Moyer T J, Finbloom J A, Chen F, Toft D J, Cryns V L, Stupp S I. J. Am. Chem. Soc., 2014, 136: 14746.

[112] Stewart P S, William Costerton J. Lancet, 2001, 358: 135.

[113] Yang C, Ren C, Zhou J, Liu J, Zhang Y, Huang F, Ding D, Xu B, Liu J. Angew. Chem. Int. Ed., 2017, 56: 2356.

[114] Cao H, Wang Y, Gao Y, Deng X, Cong Y, Liu Y, Jiang X. Angew. Chem. Int. Ed., 2019, 58: 1626.

[115] Wolfe L S, Calabrese M F, Nath A, Blaho D V, Miranker A D, Xiong Y. Proc. Natl. Acad. Sci., 2010, 107: 16863.

[116] Hernot S, van Manen L, Debie P, Mieog J S D, Vahrmeijer A L. Lancet Oncol., 2019, 20: e354.

[117] Zhang K, Gao Y-J, Yang P-P, Qi G-B, Zhang J-P, Wang L, Wang H. Adv. Healthcare Mater., 2018, 7: e1800344.

[118] Landau M J, Gould D J, Patel K M. Ann. Transl. Med., 201, 4: 3.

[119] Damian C D, Rednic N, Munteanu D, Cazacu M. Med. Ultrason, 2014, 16: 114.

[120] Xi L, Zhou G, Gao N, Yang L, Gonzalo D A, Hughes S J, Jiang H. Ann. Transl. Med., 2014, 21: 1602.

[121] Vahrmeijer A L, Hutteman M, van der Vorst J R, van de Velde C J, Frangioni J V. Nat. Rev. Clin. Oncol., 2013, 10: 507.

[122] Andreou C, Neuschmelting V, Tschaharganeh D F, Huang C H, Oseledchyk A, Iacono P, Karabeber H, Colen R R, Mannelli L, Lowe S W, Kircher M F. ACS Nano, 201, 10: 5015.

[123] Diao S, Hong G, Robinson J T, Jiao L, Antaris A L, Wu J Z, Choi C L, Dai H. J. Am. Chem. Soc., 2012, 134: 16971.

[124] Bruns O T, Bischof T S, Harris D K, Franke D, Shi Y, Riedemann L, Bartelt A, Jaworski F B, Carr J A, Rowlands C J, Wilson M W B, Chen O, Wei H, Hwang G W, Montana D M, Coropceanu I, Achorn O B, Kloepper J, Heeren J, So P T C, Fukumura D, Jensen K F, Jain R K, Bawendi M G. Nat. Biomed. Eng., 2017, 1: 0056.

[125] Hong G, Robinson J T, Zhang Y, Diao S, Antaris A L, Wang Q, Dai H. Angew. Chem. Int. Ed., 2012, 51: 9818.

[126] Wang H, Feng Z, Xu B. Chem. Soc. Rev., 2017, 46: 2421.

[127] Naczynski D J, Tan M C, Zevon M, Wall B, Kohl J, Kulesa A, Chen S, Roth C M, Riman R E, Moghe P V. Nat. Comm., 2013, 4: 2199.

[128] Antaris A L, Chen H, Cheng K, Sun Y, Hong G, Qu C, Diao S, Deng Z, Hu X, Zhang B, Zhang X, Yaghi O K, Alamparambil Z R, Hong X, Cheng Z, Dai H. Nat. Mater., 201, 15: 235.

[129] Li B, Lu L, Zhao M, Lei Z, Zhang F. Angew. Chem. Int. Ed., 2018, 57: 7483.

[130] Cheung S, O’Shea D F. Nat. Comm., 2017, 8: 1885.

[131] Che X Y. Oncol. Lett., 2013, 5: 1278.

[132] Tennvall J, Garkavij M, Chen J Q, Sjögren H O, Strand S E. Cancer, 1997, 80: 2411.

[133] Antaris A L, Chen H, Cheng K, Sun Y, Hong G, Qu C, Diao S, Deng Z, Hu X, Zhang B. Nat. Mater., 201, 15: 235.

[134] Wilhelm S, Tavares A J, Dai Q, Ohta S, Chan W C W. Nat. Rev. Mater., 201, 1: 16014.

[135] Weissleder R, Pittet M J. Nature, 2008, 452: 580.

[136] Olson E S, Jiang T, Aguilera T A, Nguyen Q T, Ellies L G, Scadeng M, Tsien R Y. Proc. Natl. Acad. Sci. U.S.A., 2010, 107: 4311.

[137] Nguyen Q T, Olson E S, Aguilera T A, Jiang T, Scadeng M, Ellies L G, Tsien R Y. Proc. Natl. Acad. Sci., 2010, 107: 4317.

[138] Wang P, Fan Y, Lu L, Liu L, Fan L, Zhao M, Xie Y, Xu C, Zhang F. Nat. Commun., 2018, 9: 2898.

[139] Wang H, Agarwal P, Zhao S, Yu J, Lu X, He X. Nat. Commun., 201, 7: 10350.

[140] Ghosh D, Bagley A F, Na Y J, Birrer M J, Bhatia S N, Belcher A M. Proc. Natl. Acad. Sci., 2014, 111: 13948.

[141] Yuan Y, Raj P, Zhang J, Siddhanta S, Barman I, Bulte J W M. Angew. Chem. Int. Ed., 2021, 133: 3869.

[142] Hollon T, Lewis S, Freudiger C W, Sunney Xie X, Orringer D A. Neurosurg Focus, 201, 40: E9.

[143] Kong K, Rowlands C J, Varma S, Perkins W, Leach I H, Koloydenko A A, Williams H C, Notingher I. Proc. Natl. Acad. Sci., 2013, 110: 15189.

[144] Thissen U, Üstün B, Melssen W J, Buydens L M C. Anal. Chem., 2004, 76: 3099.

[145] Akishiba M, Takeuchi T, Kawaguchi Y, Sakamoto K, Yu H-H, Nakase I, Takatani-Nakase T, Madani F, Gräslund A, Futaki S. Nat. Chem., 2017, 9: 751.