Aptamer-based Membrane Protein Analysis and Molecular Diagnostics

Abstract

Membrane proteins are vital components of the cell membrane and play crucial roles in various cellular activities. Analysis of membrane proteins is of paramount importance for studying molecular events inside cells and organisms and holds promising prospects for early disease diagnosis and treatment assessment. Benefiting from obvious merits including high affinity, high specificity and ease of modification, aptamers have been regarded as ideal molecular recognition elements in membrane protein analysis and molecular diagnostics strategies. This review summarised recent advances in membrane protein-specific aptamer screening, aptamer-based static and dynamic membrane protein analysis, and aptamer-based molecular diagnostic techniques. Prospects and challenges were also discussed.

Keywords

Membrane protein / Aptamer / DNA nanotechnology / Bioanalysis / Molecular diagnostics

References

[1] Uhlén M, Fagerberg L, Hallström B M, Lindskog C, Oksvold P, Mardinoglu A, Sivertsson Å, Kampf C, Sjöstedt E, Asplund A, Olsson I, Edlund K, Lundberg E, Navani S, Szigyarto C A-K, Odeberg J, Djureinovic D, Takanen J O, Hober S, Alm T, Edqvist P-H, Berling H, Tegel H, Mulder J, Rockberg J, Nilsson P, Schwenk J M, Hamsten M, von Feilitzen K, Forsberg M, Persson L, Johansson F, Zwahlen M, von Heijne G, Nielsen J, Pontén F. Science, 2015, 347: 1260419.

[2] Chatzi K E, Sardis M F, Karamanou S, Economou A. Biochem. J., 2013, 449: 25.

[3] Hedin L E, Illergard K, Elofsson A. J Proteome Res., 2011, 10: 3324.

[4] Oradd F, Andersson M. J. Membr. Biol., 2021, 254: 51.

[5] Zhang K, Gao H, Deng R, Li J. Angew. Chem. Int. Ed., 2019, 58: 4790.

[6] Caricasole A, Copani A, Caruso A, Caraci F, Iacovelli L, Sortino M A, Terstappen G C, Nicoletti F. Trends Pharmacol. Sci., 2003, 24: 233.

[7] Loibl S, Gianni L. Lancet, 2017, 389: 2415.

[8] Famulok M, Hartig J S, Mayer G. Chem. Rev., 2007, 107: 3715.

[9] Levy-Nissenbaum E, Radovic-Moreno A F, Wang A Z, Langer R, Farokhzad O C. Trends in Biotech., 2008, 26: 442.

[10] Pestourie C, Tavitian B, Duconge F. Biochimie, 2005, 87: 921.

[11] Meng H-M, Liu H, Kuai H, Peng R, Mo L, Zhang X-B. Chem. Soc. Rev., 201, 45: 2583.

[12] Ellington A D, Szostak J W. Nature, 1990, 346: 818.

[13] Tuerk C, Gold L. Science, 1990, 249: 505.

[14] Tan W, Donovan M J, Jiang J. Chem. Rev., 2013, 113: 2842.

[15] Fang X, Tan W. Acc. Chem. Res., 2009, 43: 48.

[16] Kong H Y, Byun J. Biomol Ther., 2013, 21: 423.

[17] Ababneh N, Alshaer W, Al-Louzi O, Mahafzah A, El-Khateeb M, Hillaireau H, Noiray M, Fattal E, Ismail S. Nucleic Acid Therapeutics, 2013, 23: 401.

[18] Song Z, Mao J, Barrero RA, Wang P, Zhang F, Wang T. Molecules, 2020, 25: 5585.

[19] Meng H-M, Fu T, Zhang X-B, Tan W. Natl. Sci. Rev., 2015, 2: 71.

[20] Shangguan D, Li Y, Tang Z, Cao Z C, Chen H W, Mallikaratchy P, Sefah K, Yang C J, Tan W. P. N. A. S., 200, 103: 11838.

[21] Lin M, Zhang J, Wan H, Yan C, Xia F. ACS Appl. Mater. Inter., 2020, 13: 9369.

[22] Zhu H, Wu E, Pan Z, Zhang C, Zhang Y, Liao Q, Wang Y, Sun Y, Ye M, Wu W. Anal. Chem., 2023, 95: 3238.

[23] Fang X, Tan W. Acc. Chem. Res., 2010, 43: 48.

[24] Gao T, Mao Z, Li W, Pei R. J. Mater. Chem. B, 2021, 9: 746.

[25] Bayat P, Taghdisi S M, Rafatpanah H, Abnous K, Ramezani M. Talanta, 2019, 194: 399.

[26] Raddatz M-S L, Dolf A, Endl E, Knolle P, Famulok M, Mayer G. Angew. Chem. Int. Ed., 2008, 47: 5190.

[27] Mayer G, Ahmed M-S L, Dolf A, Endl E, Knolle P A, Famulok M. Nat. Protoc., 2010, 5: 1993.

[28] Hicke B J, Marion C, Chang Y-F, Gould T, Lynott C K, Parma D, Schmidt P G, Warren S. J. Bio. Chem., 2001, 276: 48644.

[29] Souza A G, Marangoni K, Fujimura P T, Alves P T, Silva M J, Bastos V A F, Goulart L R, Goulart V A. Experimental Cell Research, 201, 341: 147.

[30] Lao Y-H, Phua K K L, Leong K W. ACS Nano, 2015, 9: 2235.

[31] Chushak Y, Stone M O. Nucleic Acids Res., 2009, 37: 87.

[32] Manju N, Samiha C M, Kumar S P P, Gururaj H L, Flammini F. IEEE Access, 2022, 10: 49677.

[33] Sun D, Sun M, Zhang J, Lin X, Zhang Y, Lin F, Zhang P, Yang C, Song J. TrAC Trends in Analytical Chemistry, 2022, 157: 116767.

[34] Camorani S, Esposito C L, Rienzo A, Catuogno S, Iaboni M, Condorelli G, de Franciscis V, Cerchia L. Molecular Therapy, 2014, 22: 828.

[35] Hu Y, Duan J, Zhan Q, Wang F, Lu X, Yang X-D. PLoS One, 2012, 7: 31970.

[36] Wang D-L, Song Y-L, Zhu Z, Li X-L, Zou Y, Yang H-T, Wang J-J, Yao P-S, Pan R-J, Yang C J, Kang D-Z. Biochem. Bio. Res. Co., 2014, 453: 681.

[37] Gao T, Ding P, Li W, Wang Z, Lin Q, Pei R. Nanoscale, 2020, 12: 22574.

[38] Fafińska J, Czech A, Sitz T, Ignatova Z, Hahn U. Nucleic Acid Therapeutics, 2018, 28: 326.

[39] Du J, Hong J, Xu C, Cai Y, Xiang B, Zhou C, Xu X. BioMed. Res. Int., 2015, 2015: 1.

[40] Bing T, Shangguan D, Wang Y. Molecular & Cellular Proteomics, 2015, 14: 2692.

[41] Plummer K A, Carothers J M, Yoshimura M, Szostak J W, Verdine G L. Nucleic Acids Res., 2005, 33: 5602.

[42] Jeon W, Lee S, Dh M, Ban C. Anal. Biochem., 2013, 439: 11.

[43] Lin C Y, Lee C H, Chuang Y H, Lee J Y, Chiu Y Y, Wu Lee Y H, Jong Y J, Hwang J K, Huang S H, Chen L C, Wu C H, Tu S H, Ho Y S, Yang J M. Nat. Commun., 2019, 10: 3131.

[44] Huang H, Groth J, Sossey-Alaoui K, Hawthorn L, Beall S, Geradts J. Clinic. Cancer Res., 2005, 11: 4357.

[45] Hosonaga M, Arima Y, Kohno N, Saya H. J. Clini. Oncol., 2014, 32: 11572.

[46] Chen Y, Munteanu A C, Huang Y F, Phillips J, Zhu Z, Mavros M, Tan W. Chemistry, 2009, 15: 5327.

[47] Shi H, He X, Wang K, Wu X, Ye X, Guo Q, Tan W, Qing Z, Yang X, Zhou B. Proc. Natl. Acad. Sci. USA, 2011, 108: 3900.

[48] Zhao G, Li H, Gao J, Cai M, Xu H, Shi Y, Wang H, Wang H. Anal. Chem., 2021, 93: 14113.

[49] Letschert S, Göhler A, Franke C, Bertleff-Zieschang N, Memmel E, Doose S, Seibel J, Sauer M. Angew. Chem. Int. Ed., 2014, 53: 10921.

[50] Chen J, Li H, Wu Q, Yan Q, Sun J, Liang F, Liu Y, Wang H. Anal. Chem., 2021, 93: 936.

[51] Strauss S, Nickels P C, Strauss M T, Jimenez Sabinina V, Ellenberg J, Carter J D, Gupta S, Janjic N, Jungmann R. Nature Methods, 2018, 15: 685.

[52] Vaught J D, Bock C, Carter J, Fitzwater T, Otis M, Schneider D, Rolando J, Waugh S, Wilcox S K, Eaton B E. J. Am. Chem. Soc., 2010, 132: 4141.

[53] Rohloff J C, Gelinas A D, Jarvis T C, Ochsner U A, Schneider D J, Gold L, Janjic N. Mol. Ther. Nucleic Acids, 2014, 3: 201.

[54] Jiang Y, Shi M, Liu Y, Wan S, Cui C, Zhang L, Tan W. Angew. Chem. Int. Ed. Engl., 2017, 56: 11916.

[55] Li L, Wang Q, Feng J, Tong L, Tang B. Anal. Chem., 2014, 86: 5101.

[56] Chen Y, Munteanu A C, Huang Y F, Phillips J, Zhu Z, Mavros M, Tan W. Chemistry, 2009, 15: 5327.

[57] Rubin C S, Rosen O M. Annual Rev. Biochem., 1975, 44: 831.

[58] Paik W K, Paik D C, Kim S. Trends. Biochem. Sci., 2007, 32: 146.

[59] Zhao S, Xu W, Jiang W, Yu W, Lin Y, Zhang T, Yao J, Zhou L, Zeng Y, Li H. Science, 2010, 327: 1000.

[60] Paleček E, Tkáč J, Bartosik M, Bertók T S, Ostatná V, Paleček J. Chem. Rev., 2015, 115: 2045.

[61] Pinho S S, Reis C A. Nature Rev. Cancer, 2015, 15: 540.

[62] Brownlee M D M. Annual Rev. Med., 1995, 46: 223.

[63] Liddy K A, White M Y, Cordwell S J. Genome Medicine, 2013, 5: 1.

[64] Saxon E, Bertozzi C R. Science, 2000, 287: 2007.

[65] Jewett JC, Bertozzi C R. Chem. Soc. Rev., 2010, 39: 1272.

[66] Robinson P V, de Almeida-Escobedo G, de Groot A E, McKechnie J L, Bertozzi C R. J. Am. Chem. Soc., 2015, 137: 10452.

[67] Piston D W, Kremers G-J. Trends Biochem. Sci., 2007, 32: 407.

[68] Yuan B, Chen Y, Sun Y, Guo Q, Huang J, Liu J, Meng X, Yang X, Wen X, Li Z, Li L, Wang K. Anal. Chem., 2018, 90: 6131.

[69] Liu Z, Liang Y, Cao W, Gao W, Tang B. Anal. Chem., 2021, 93: 8915.

[70] Li J, Liu S, Sun L, Li W, Zhang S-Y, Yang S, Li J, Yang H-H. J. Am. Chem. Soc., 2018, 140: 16589.

[71] Huang M, Zhu L, Kang S, Chen F, Wei X, Lin L, Chen X, Wang W, Zhu Z, Yang C, Song Y. Anal. Chem., 2021, 93: 15958.

[72] Tommasone S, Allabush F, Tagger Y K, Norman J, Kopf M, Tucker J H R, Mendes P M. Chem. Soc. Rev., 2019, 48: 5488.

[73] Li M, Lin N, Huang Z, Du L, Altier C, Fang H, Wang B. J. Am. Chem. Soc., 2008, 130: 12636.

[74] Díaz-Fernández A, Miranda-Castro R, de-los-Santos-Álvarez N, Rodríguez E F, Lobo-Castañón M J. Biosens. Bioelectron., 2019, 128: 83.

[75] Yoshikawa A M, Rangel A, Feagin T, Chun E M, Wan L, Li A, Moeckl L, Wu D, Eisenstein M, Pitteri S, Soh H T. Nat Commun., 2021, 12: 7106.

[76] Cui Y, Yu M, Yao X, Xing J, Lin J, Li X. Molecular Plant, 2018, 11: 1315.

[77] Kusumi A, Tsunoyama T A, Hirosawa K M, Kasai R S, Fujiwara T K. Nat. Chem. Bio., 2014, 10: 524.

[78] Wolfbeis O S. Chem. Soc. Rev., 2015, 44: 4743.

[79] Howarth M, Takao K, Hayashi Y, Ting A Y. P. N. A. S., 2005, 102: 7583.

[80] Chen L Q, Xiao S J, Hu P P, Peng L, Ma J, Luo L F, Li Y F, Huang C Z. Anal. Chem., 2012, 84: 3099.

[81] Delcanale P, Porciani D, Pujals S, Jurkevich A, Chetrusca A, Tawiah K D, Burke D H, Albertazzi L. Angew. Chem. Int. Ed., 2020, 59: 18546.

[82] Shen H, Tauzin L J, Baiyasi R, Wang W, Moringo N, Shuang B, Landes C F. Chem Rev., 2017, 117: 7331.

[83] Zhang L, Chu M, Ji C, Wei J, Yang Y, Huang Z, Tan W, Tan J, Yuan Q. Anal. Chem., 2022, 94: 17413.

[84] Albright S, Cacace M, Tivon Y, Deiters A. J. Am. Chem. Soc., 2023, 145: 16458.

[85] Du Y, Lyu Y, Li S, Ding D, Chen J, Yang C, Sun Y, Qu F, Xiao Z, Jiang J, Tan W. Angew. Chem. Int. Ed., 2022, 62: 202215387.

[86] Klemm J D, Schreiber S L, Crabtree G R. Annu. Rev. Immunol., 1998, 16: 569.

[87] Hynes N E, Lane H A. Nature Rev. Cancer, 2005, 5: 341.

[88] You M, Lyu Y, Han D, Qiu L, Liu Q, Chen T, Sam Wu C, Peng L, Zhang L, Bao G, Tan W. Nat. Nanotechnol., 2017, 12: 453.

[89] Fredriksson S, Gullberg M, Jarvius J, Olsson C, Pietras K, Gústafsdóttir S M, Östman A, Landegren U. Nat. Biotechnol., 2002, 20: 473.

[90] Liang H, Chen S, Li P, Wang L, Li J, Li J, Yang H H, Tan W. J. Am. Chem. Soc., 2018, 140: 4186.

[91] Wang L, Li W, Sun J, Zhang S-Y, Yang S, Li J, Li J, Yang H H. Anal. Chem., 2018, 90: 14433.

[92] Li Y, Zhang X, Pan W, Li N, Tang B. Anal. Chem., 2020, 92: 11921.

[93] Bing T, Shen L, Wang J, Wang L, Liu X, Zhang N, Xiao X, Shangguan D. Adv. Sci., 2019, 6: 1900143.

[94] Dong C, Fang X, Qin X, Wang Y, Zhang J, Song C, Wang L. Anal. Chem., 2023, 95: 6810.

[95] Keskin O, Gursoy A, Ma B, Nussinov R. Chem. Rev., 2008, 108: 1225.

[96] Massimino M L, Simonato M, Spolaore B, Franchin C, Arrigoni G, Marin O, Monturiol-Gross L, Fernandez J, Lomonte B, Tonello F. Sci. Rep., 2018, 8: 10619.

[97] Zhu L, Xu Y, Wei X, Lin H, Huang M, Lin B, Song Y, Yang C. Angew. Chem. Int. Ed. Engl., 2021, 60: 18111.

[98] Mori T, Oguro A, Ohtsu T, Nakamura Y. Nucleic. Acids Res., 2004, 32: 6120.

[99] Zhang H Q, Li X F, Le X C. Anal. Chem., 2009, 81: 7795.

[100] Lee H, Kim T H, Park D, Jang M, Chung J J, Kim S H, Kim S H, Lee K H, Jung Y, Oh S J. Pharmaceutics, 2020, 12: 689.

[101] Sengupta P, Jovanovic-Talisman T, Skoko D, Renz M, Veatch S L, Lippincott-Schwartz J. Nature Methods, 2011, 8: 969.

[102] Eraslan G, Avsec Ž, Gagneur J, Theis FJ. Nat. Rev. Genet., 2019, 20: 389.

[103] Hollingsworth M A, Swanson B J. Nature Rev. Cancer, 2004, 4: 45.

[104] Zhang Y, Chen W, Fang Y, Zhang X, Liu Y, Ju H. J. Am. Chem. Soc., 2021, 143: 15233.

[105] You M, Peng L, Shao N, Zhang L, Qiu L, Cui C, Tan W. J. Am. Chem. Soc., 2014, 136: 1256.

[106] You M, Zhu G, Chen T, Donovan M J, Tan W. J. Am. Chem. Soc., 2015, 137: 667.

[107] Feng C, Chen T, Mao D, Zhang F, Tian B, Zhu X. ACS Sens., 2020, 5: 3116.

[108] El Andaloussi S, Mäger I, Breakefield X O, Wood M J A. Nat. Rev. Drug Discov., 2013, 12: 347.

[109] Yan H, Li Y, Cheng S, Zeng Y. Anal. Chem., 2021, 93: 4739.

[110] Im H, Shao H, Park Y I, Peterson V M, Castro C M, Weissleder R, Lee H. Nat. Biotechnol., 2014, 32: 490.

[111] Fan Q, Yang L, Zhang X, Peng X, Wei S, Su D, Zhai Z, Hua X, Li H. Cancer Lett., 2018, 414: 107.

[112] Hoshino A, Kim H S, Bojmar L, Gyan K E, Cioffi M, Hernandez J, Zambirinis C P, Rodrigues G, Molina H, Heissel S, Mark M T, Steiner L, Benito-Martin A, Lucotti S, Di Giannatale A, Offer K, Nakajima M, Williams C, Nogués L, Pelissier Vatter F A, Hashimoto A, Davies A E, Freitas D, Kenific C M, Ararso Y, Buehring W, Lauritzen P, Ogitani Y, Sugiura K, Takahashi N, Aleckovic M, Bailey K A, Jolissant J S, Wang H, Harris A, Schaeffer L M, García-Santos G, Posner Z, Balachandran V P, Khakoo Y, Raju G P, Scherz A, Sagi I, Scherz-Shouval R, Yarden Y, Oren M, Malladi M, Petriccione M, De Braganca K C, Donzelli M, Fischer C, Vitolano S, Wright G P, Ganshaw L, Marrano M, Ahmed A, DeStefano J, Danzer E, Roehrl M H A, Lacayo N J, Vincent T C, Weiser M R, Brady M S, Meyers P A, Wexler L H, Ambati S R, Chou A J, Slotkin E K, Modak S, Roberts S S, Basu E M, Diolaiti D, Krantz B A, Cardoso F, Simpson A L, Berger M, Rudin C M, Simeone D M, Jain M, Ghajar C M, Batra S K, Stanger B Z, Bui J, Brown K A, Rajasekhar V K, Healey J H, De Sousa M, Kramer K, Sheth S, Baisch J, Pascual V, Heaton T E, La Quaglia M P, Pisapia D J, Schwartz R, Zhang H, Liu Y, Shukla A, Blavier L, DeClerck Y A, LaBarge M, Bissell M J, Caffrey T C, Grandgenett P M, Hollingsworth M A, Bromberg J, Costa-Silva B, Peinado H, Kang Y, Garcia B A, O’Reilly E M, Kelsen D, Trippett T M, Jones D R, Matei IR, Jarnagin W R, Lyden D. Cell, 2020, 182: 1044.

[113] Li Y, Deng J, Han Z, Liu C, Tian F, Xu R, Han D, Zhang S, Sun J. J. Am. Chem. Soc., 2021, 143: 1290.

[114] Yu Y, Guo Q, Jiang W, Zhang H, Cai C. Anal. Chem., 2021, 93: 11298.

[115] Wu N, Zhang X-Y, Xia J, Li X, Yang T, Wang J-H. ACS Nano, 2021, 15: 19522.

[116] Cristiano S, Leal A, Phallen J, Fiksel J, Adleff V, Bruhm D C, Jensen S Ø, Medina J E, Hruban C, White J R, Palsgrove D N, Niknafs N, Anagnostou V, Forde P, Naidoo J, Marrone K, Brahmer J, Woodward B D, Husain H, van Rooijen K L, Ørntoft M-B W, Madsen A H, van de Velde C J H, Verheij M, Cats A, Punt CJA, Vink G R, van Grieken NCT, Koopman M, Fijneman R J A, Johansen J S, Nielsen H J, Meijer G A, Andersen C L, Scharpf R B, Velculescu V E. Nature, 2019, 570: 385.

[117] Pastorino U, Silva M, Sestini S, Sabia F, Boeri M, Cantarutti A, Sverzellati N, Sozzi G, Corrao G, Marchiano A. Anna. Oncol., 2019, 30: 1162.

[118] Crosby D, Bhatia S, Brindle K M, Coussens L M, Dive C, Emberton M, Esener S, Fitzgerald R C, Gambhir S S, Kuhn P, Rebbeck T R, Balasubramanian S. Science, 2022, 375: 9040.

[119] Xiao S, Yao Y, Liao S, Xu B, Li X, Zhang Y, Zhang L, Chen Q, Tang H, Song Q, Dong M. Nano Lett., 2023, 23: 8115.

[120] Li P, Yu X, Han W, Kong Y, Bao W, Zhang J, Zhang W, Gu Y. ACS Sens., 2019, 4: 1433.

[121] Liu C, Zhao J, Tian F, Cai L, Zhang W, Feng Q, Chang J, Wan F, Yang Y, Dai B, Cong Y, Ding B, Sun J, Tan W. Nat. Biomed. Eng., 2019, 3: 183.

[122] Tian F, Zhang S, Liu C, Han Z, Liu Y, Deng J, Li Y, Wu X, Cai L, Qin L, Chen Q, Yuan Y, Liu Y, Cong Y, Ding B, Jiang Z, Sun J. Nat. Commun., 2021, 12: 2536.

[123] Li J, Li Y, Li Q, Sun L, Tan Q, Lu Y, Zhu J, Qu F, Tan W. Angew. Chem. Int. Ed., 2024, 63: e202314262.

[124] Zhou X, Jia Y, Mao C, Liu S. Cancer Lett., 2024, 580: 216481.

[125] Emami N, Pakchin P S, Ferdousi R. J. Theor. Biol., 2020, 497: 110268.

[126] Thirunavukarasu D, Chen T, Liu Z, Hongdilokkul N, Romesberg F E. J. Am. Chem. Soc., 2017, 139: 2892.