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Molecular imaging of EGFR/HER2 cancer biomarkers by protein MRI contrast agents

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Abstract

Epidermal growth factor receptor (EGFR) and HER2 are major prognosis biomarkers and drug targets overexpressed in various types of cancer cells. There is a pressing need to develop MRI contrast agents capable of enhancing the contrast between normal tissues and tumors with high relaxivity, capable of targeting tumors, and with high intratumoral distribution and minimal toxicity. In this review, we first discuss EGFR signaling and its role in tumor progression as a major drug target. We then report our progress in the development of protein contrast agents with significant improvement of both r 1 and r 2 relaxivities, pharmacokinetics, in vivo retention time, and in vivo dose efficiency. Finally, we report our effort in the development of EGFR-targeted protein contrast agents with the capability to cross the endothelial boundary and with good tissue distribution across the entire tumor mass. The noninvasive capability of MRI to visualize spatially and temporally the intratumoral distribution as well as quantify the levels of EGFR and HER2 would greatly improve our ability to track changes of the biomarkers during tumor progression, monitor treatment efficacy, aid in patient selection, and further develop novel targeted therapies for clinical application.

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References

  1. Yewale C, Baradia D, Vhora I, Patil S, Misra A (2013) Biomaterials 34(34):8690–8707

    CAS  PubMed  Google Scholar 

  2. Kramer-Marek G, Longmire MR, Choyke PL, Kobayashi H (2012) Curr Med Chem 19(28):4759–4766

    CAS  PubMed  Google Scholar 

  3. Wang W, Ke S, Wu Q, Charnsangavej C, Gurfinkel M, Gelovani JG, Abbruzzese JL, Sevick-Muraca EM, Li C (2004) Mol Imaging 3(4):343–351

    CAS  PubMed  Google Scholar 

  4. Semmler W, Schwaiger M (eds) (2008) Molecular Imaging. In: Handbook of Experimental Pharmacology. Springer, Berlin, Heidelberg, pp 167–224

  5. Johnston DL, Liu P, Lauffer RB, Newell JB, Wedeen VJ, Rosen BR, Brady TJ, Okada RD (1987) J Nucl Med 28(5):871–877

    CAS  PubMed  Google Scholar 

  6. Caravan P, Ellison JJ, McMurry TJ, Lauffer RB (1999) Chem Rev 99(9):2293–2352

    CAS  PubMed  Google Scholar 

  7. Tweedle MF (1997) Eur Radiol 7(Suppl 5):225–230

    PubMed  Google Scholar 

  8. Bousquet J-C, Saini S, Stark D, Hahn P, Nigam M, Wittenberg J, Ferrucci J (1988) Radiology 166(3):693–698

    CAS  PubMed  Google Scholar 

  9. Vogl TJ, Kümmel S, Hammerstingl R, Schellenbeck M, Schumacher G, Balzer T, Schwarz W, Müller P, Bechstein WO, Mack MG (1996) Radiology 200(1):59–67

    CAS  PubMed  Google Scholar 

  10. Kaiser W, Zeitler E (1989) Radiology 170(3):681–686

    CAS  PubMed  Google Scholar 

  11. Flacke S, Fischer S, Scott MJ, Fuhrhop RJ, Allen JS, McLean M, Winter P, Sicard GA, Gaffney PJ, Wickline SA, Lanza GM (2001) Circulation 104(11):1280–1285

    CAS  PubMed  Google Scholar 

  12. Terreno E, Castelli DD, Viale A, Aime S (2010) Chem Rev 110(5):3019–3042

    CAS  PubMed  Google Scholar 

  13. Weinmann H-J, Ebert W, Misselwitz B, Schmitt-Willich H (2003) Eur J Radiol 46(1):33–44

    PubMed  Google Scholar 

  14. Tóth E, Helm L, Merbach AE (2002) Top Curr Chem 221:61–102

    Google Scholar 

  15. Zhou G, Li Y, Liu Y, Ge C, Li W, Sun B, Li B, Gao Y, Chen C (2010) J Nanosci Nanotechnol 10(12):8597–8602

    CAS  PubMed  Google Scholar 

  16. Arbab AS, Liu W, Frank JA (2006) Expert Rev Med Devices 3(4):427–439

    CAS  PubMed  Google Scholar 

  17. Ranganathan RS, Raju N, Fan H, Zhang X, Tweedle MF, Desreux JF, Jacques V (2002) Inorg Chem 41(25):6856–6866

    CAS  PubMed  Google Scholar 

  18. Villaraza AJ, Bumb A, Brechbiel MW (2010) Chem Rev 110(5):2921–2959

    CAS  PubMed Central  PubMed  Google Scholar 

  19. Caravan P (2006) Chem Soc Rev 35(6):512–523

    CAS  PubMed  Google Scholar 

  20. Gibby WA, Gibby KA (2004) Invest Radiol 39(3):138–142

    PubMed  Google Scholar 

  21. Prince MR, Zhang HL, Prowda JC, Grossman ME, Silvers DN (2009) Radiographics 29(6):1565–1574

    PubMed  Google Scholar 

  22. Grobner T (2006) Nephrol Dial Transplant 21:1104–1108

    CAS  PubMed  Google Scholar 

  23. Thomsen HS, Morcos SK, Dawson P (2006) Clin Radiol 61(11):905–906

    CAS  PubMed  Google Scholar 

  24. Clarkson RB (2002) Top Curr Chem 221:201–235

    CAS  Google Scholar 

  25. McMurry TJ, Parmelee DJ, Sajiki H, Scott DM, Ouellet HS, Walovitch RC, Tyeklar Z, Dumas S, Bernard P, Nadler S, Midelfort K, Greenfield M, Troughton J, Lauffer RB (2002) J Med Chem 45(16):3465–3474

    CAS  PubMed  Google Scholar 

  26. Ringe KI, Husarik DB, Sirlin CB, Merkle EM (2010) AJR Am J Roentgenol 195(1):13–28

    PubMed  Google Scholar 

  27. Wedeking P, Sotak CH, Telser J, Kumar K, Chang CA, Tweedle MF (1992) Magn Reson Imaging 10(1):97–108

    CAS  PubMed  Google Scholar 

  28. Matsumoto Y, Jasanoff A (2013) FEBS Lett 587(8):1021–1029

    CAS  PubMed  Google Scholar 

  29. Shapiro MG, Westmeyer GG, Romero PA, Szablowski JO, Kuster B, Shah A, Otey CR, Langer R, Arnold FH, Jasanoff A (2010) Nat Biotechnol 28(3):264–270

    CAS  PubMed Central  PubMed  Google Scholar 

  30. Sana B, Poh CL, Lim S (2012) Chem Commun 48(6):862–864

    CAS  Google Scholar 

  31. Sana B, Johnson E, Sheah K, Poh CL, Lim S (2010) Biointerphases 5(3):FA48–FA52

    PubMed  Google Scholar 

  32. Bryant LH Jr, Jordan EK, Bulte JW, Herynek V, Frank JA (2002) Acad Radiol 9(Suppl 1):S29–S33

    PubMed  Google Scholar 

  33. Bryant LH Jr, Brechbiel MW, Wu C, Bulte JW, Herynek V, Frank JA (1999) J Magn Reson Imaging 9(2):348–352

    PubMed  Google Scholar 

  34. Bryant LH Jr, Hodges MW, Bryant RG (1999) Inorg Chem 38(5):1002–1005

    CAS  PubMed  Google Scholar 

  35. Kobayashi H, Brechbiel MW (2004) Curr Pharm Biotechnol 5(6):539–549

    CAS  PubMed  Google Scholar 

  36. Kobayashi H, Reijnders K, English S, Yordanov AT, Milenic DE, Sowers AL, Citrin D, Krishna MC, Waldmann TA, Mitchell JB, Brechbiel MW (2004) Clin Cancer Res 10(22):7712–7720

    CAS  PubMed  Google Scholar 

  37. Kobayashi H, Kawamoto S, Saga T, Sato N, Hiraga A, Ishimori T, Konishi J, Togashi K, Brechbiel MW (2001) Magn Reson Med 46(4):781–788

    CAS  PubMed  Google Scholar 

  38. Kellar KE, Henrichs PM, Hollister R, Koenig SH, Eck J, Wei D (1997) Magn Reson Med 38(5):712–716

    CAS  PubMed  Google Scholar 

  39. Vander Elst L, Chapelle F, Laurent S, Muller RN (2001) J Biol Inorg Chem 6(2):196–200

    CAS  PubMed  Google Scholar 

  40. Behra-Miellet J, Briand G, Kouach M, Gressier B, Cazin M, Cazin JC (1998) Biomed Chromatogr 12(1):21–26

    CAS  PubMed  Google Scholar 

  41. Lauffer RB, Brady TJ (1985) Magn Reson Imaging 3(1):11–16

    CAS  PubMed  Google Scholar 

  42. Lauffer RB, Brady TJ, Brown RD 3rd, Baglin C, Koenig SH (1986) Magn Reson Med 3(4):541–548

    CAS  PubMed  Google Scholar 

  43. Ogan MD (1988) Invest Radiol 23(12):961

    CAS  PubMed  Google Scholar 

  44. Lauffer RB, Parmelee DJ, Dunham SU, Ouellet HS, Dolan RP, Witte S, McMurry TJ, Walovitch RC (1998) Radiology 207(2):529–538

    CAS  PubMed  Google Scholar 

  45. Lauffer RB, Parmelee DJ, Ouellet HS, Dolan RP, Sajiki H, Scott DM, Bernard PJ, Buchanan EM, Ong KY, Tyeklar Z, Midelfort KS, McMurry TJ, Walovitch RC (1996) Acad Radiol 3(Suppl 2):S356–S358

    PubMed  Google Scholar 

  46. Karfeld-Sulzer LS, Waters EA, Kohlmeir EK, Kissler H, Zhang X, Kaufman DB, Barron AE, Meade TJ (2011) Magn Reson Med 65(1):220–228

    PubMed Central  PubMed  Google Scholar 

  47. Liepold L, Anderson S, Willits D, Oltrogge L, Frank JA, Douglas T, Young M (2007) Magn Reson Med 58(5):871–879

    CAS  PubMed  Google Scholar 

  48. Caravan P, Greenwood JM, Welch JT, Franklin SJ (2003) Chem Commun 2574–2575

  49. Overoye-Chan K, Koerner S, Looby RJ, Kolodziej AF, Zech SG, Deng Q, Chasse JM, McMurry TJ, Caravan P (2008) J Am Chem Soc 130(18):6025–6039

    CAS  PubMed  Google Scholar 

  50. Caravan P, Das B, Dumas S, Epstein FH, Helm PA, Jacques V, Koerner S, Kolodziej A, Shen L, Sun WC, Zhang Z (2007) Angew Chem Int Ed 46(43):8171–8173

    CAS  Google Scholar 

  51. Uppal R, Medarova Z, Farrar CT, Dai G, Moore A, Caravan P (2012) Invest Radiol 47(10):553–558

    CAS  PubMed  Google Scholar 

  52. Pomper MG (2002) J Cell Biochem 87(Suppl 39):211–220

    Google Scholar 

  53. Jarrett BR, Correa C, Ma KL, Louie AY (2010) PLoS ONE 5(10):13254

    Google Scholar 

  54. Tu C, Ma X, House A, Kauzlarich SM, Louie AY (2011) ACS Med Chem Lett 2(4):285–288

    CAS  PubMed Central  PubMed  Google Scholar 

  55. Wadas TJ, Wong EH, Weisman GR, Anderson CJ (2010) Chem Rev 110(5):2858–2902

    CAS  PubMed Central  PubMed  Google Scholar 

  56. De Leon-Rodriguez LM, Lubag AJ, Malloy CR, Martinez GV, Gillies RJ, Sherry AD (2009) Acc Chem Res 42(7):948–957

    PubMed Central  PubMed  Google Scholar 

  57. Artemov D, Mori N, Ravi R, Bhujwalla ZM (2003) Cancer Res 63(11):2723–2727

    CAS  PubMed  Google Scholar 

  58. Zhu W, Okollie B, Bhujwalla ZM, Artemov D (2008) Magn Reson Med 59(4):679–685

    CAS  PubMed Central  PubMed  Google Scholar 

  59. Louie AY, Huber MM, Ahrens ET, Rothbacher U, Moats R, Jacobs RE, Fraser SE, Meade TJ (2000) Nat Biotechnol 18(3):321–325

    CAS  PubMed  Google Scholar 

  60. Groth RD, Lindskog M, Thiagarajan TC, Li L, Tsien RW (2011) Proc Natl Acad Sci USA 108(2):828–833

    CAS  PubMed  Google Scholar 

  61. Feinmesser RL, Wicks SJ, Taverner CJ, Chantry A (1999) J Biol Chem 274(23):16168–16173

    CAS  PubMed  Google Scholar 

  62. Cho HS, Mason K, Ramyar KX, Stanley AM, Gabelli SB, Denney DW Jr, Leahy DJ (2003) Nature 421(6924):756–760

    CAS  PubMed  Google Scholar 

  63. Burke P, Schooler K, Wiley HS (2001) Mol Biol Cell 12(6):1897–1910

    CAS  PubMed Central  PubMed  Google Scholar 

  64. Tolmachev V (2008) Curr Pharm Des 14(28):2999–3019

    CAS  PubMed  Google Scholar 

  65. Zhao X, Dai W, Zhu H, Zhang Y, Cao L, Ye Q, Lei P, Shen G (2006) Cell Biol Int 30(8):653–658

    CAS  PubMed  Google Scholar 

  66. Zhu H, Acquaviva J, Ramachandran P, Boskovitz A, Woolfenden S, Pfannl R, Bronson RT, Chen JW, Weissleder R, Housman DE, Charest A (2009) Proc Natl Acad Sci USA 106(8):2712–2716

    CAS  PubMed  Google Scholar 

  67. Tang X, Shigematsu H, Bekele BN, Roth JA, Minna JD, Hong WK, Gazdar AF, Wistuba II (2005) Cancer Res 65(17):7568–7572

    CAS  PubMed  Google Scholar 

  68. Arteaga C (2003) Semin Oncol 30(3 Suppl 7):3–14

    CAS  Google Scholar 

  69. Ross JS, Linette GP, Stec J, Clark E, Ayers M, Leschly N, Symmans WF, Hortobagyi GN, Pusztai L (2004) Expert Rev Mol Diagn 4(2):169–188

    CAS  PubMed  Google Scholar 

  70. Sternlicht MD (2006) Breast Cancer Res 8(1):201

    PubMed Central  PubMed  Google Scholar 

  71. Sternlicht MD, Sunnarborg SW, Kouros-Mehr H, Yu Y, Lee DC, Werb Z (2005) Development 132(17):3923–3933

    CAS  PubMed Central  PubMed  Google Scholar 

  72. Mitsudomi T, Yatabe Y (2010) FEBS J 277(2):301–308

    CAS  PubMed  Google Scholar 

  73. Okamoto I (2010) FEBS J 277(2):309–315

    CAS  PubMed  Google Scholar 

  74. Menard S, Casalini P, Campiglio M, Pupa S, Agresti R, Tagliabue E (2001) Ann Oncol 12(Suppl 1):S15–S19

    PubMed  Google Scholar 

  75. Amin DN, Hida K, Bielenberg DR, Klagsbrun M (2006) Cancer Res 66(4):2173–2180

    CAS  PubMed  Google Scholar 

  76. Milanezi F, Carvalho S, Schmitt FC (2008) Expert Rev Mol Diagn 8(4):417–434

    CAS  PubMed  Google Scholar 

  77. Cooke T, Reeves J, Lanigan A, Stanton P (2001) Ann Oncol 12(Suppl 1):S23–S28

    PubMed  Google Scholar 

  78. Tagliabue E, Agresti R, Ghirelli C, Morelli D, Menard S (2001) Breast Cancer Res Treat 70(2):155–156

    CAS  PubMed  Google Scholar 

  79. Yonemura Y, Ninomiya I, Yamaguchi A, Fushida S, Kimura H, Ohoyama S, Miyazaki I, Endou Y, Tanaka M, Sasaki T (1991) Cancer Res 51(3):1034–1038

    CAS  PubMed  Google Scholar 

  80. Hellstrom I, Goodman G, Pullman J, Yang Y, Hellstrom KE (2001) Cancer Res 61(6):2420–2423

    CAS  PubMed  Google Scholar 

  81. Buchler P, Reber HA, Eibl G, Roth MA, Buchler MW, Friess H, Isacoff WH, Hines OJ (2005) Int J Oncol 27(4):1125–1130

    PubMed  Google Scholar 

  82. Yarden Y (2001) Oncology 61(Suppl 2):1–13

    CAS  PubMed  Google Scholar 

  83. Yamanaka Y, Friess H, Kobrin MS, Buchler M, Beger HG, Korc M (1993) Anticancer Res 13(3):565–569

    CAS  PubMed  Google Scholar 

  84. Allison M (2010) Nat Biotechnol 28(2):117–119

    CAS  PubMed  Google Scholar 

  85. Artemov D (2003) J Cell Biochem 90(3):518–524

    CAS  PubMed  Google Scholar 

  86. Artemov D, Mori N, Okollie B, Bhujwalla ZM (2003) Magn Reson Med 49(3):403–408

    CAS  PubMed  Google Scholar 

  87. Leonessa F, Green D, Licht T, Wright A, Wingate-Legette K, Lippman J, Gottesman M, Clarke R (1996) Br J Cancer 73(2):154

    CAS  PubMed Central  PubMed  Google Scholar 

  88. Yang D, Kuan C-T, Payne J, Kihara A, Murray A, Wang L-M, Alimandi M, Pierce JH, Pastan I, Lippman ME (1998) Clin Cancer Res 4(4):993–1004

    CAS  PubMed  Google Scholar 

  89. Park J-G, Frucht H, LaRocca RV, Bliss DP, Kurita Y, Chen T-R, Henslee JG, Trepel JB, Jensen RT, Johnson BE (1990) Cancer Res 50(9):2773–2780

    CAS  PubMed  Google Scholar 

  90. Wilken JA, Webster KT, Maihle NJ (2010) J Ovarian Res 3:7

    PubMed Central  PubMed  Google Scholar 

  91. Winnard PT Jr, Pathak AP, Dhara S, Cho SY, Raman V, Pomper MG (2008) J Nucl Med 49(Suppl 2):96S–112S

    PubMed  Google Scholar 

  92. Diaz R, Nguewa PA, Parrondo R, Perez-Stable C, Manrique I, Redrado M, Catena R, Collantes M, Penuelas I, Diaz-Gonzalez JA, Calvo A (2010) BMC Cancer 10:188

    PubMed Central  PubMed  Google Scholar 

  93. Eck MJ, Yun CH (2010) Biochim Biophys Acta 1804(3):559–566

    CAS  PubMed Central  PubMed  Google Scholar 

  94. Akita RW, Sliwkowski MX (2003) Semin Oncol 30(3 Suppl 7):15–24

    CAS  PubMed  Google Scholar 

  95. Knuefermann C, Lu Y, Liu B, Jin W, Liang K, Wu L, Schmidt M, Mills GB, Mendelsohn J, Fan Z (2003) Oncogene 22(21):3205–3212

    CAS  PubMed  Google Scholar 

  96. Baselga J, Norton L, Albanell J, Kim YM, Mendelsohn J (1998) Cancer Res 58(13):2825–2831

    CAS  PubMed  Google Scholar 

  97. Dawood S, Broglio K, Buzdar AU, Hortobagyi GN, Giordano SH (2010) J Clin Oncol 28(1):92–98

    CAS  PubMed  Google Scholar 

  98. Leyland-Jones B, Gelmon K, Ayoub JP, Arnold A, Verma S, Dias R, Ghahramani P (2003) J Clin Oncol 21(21):3965–3971

    CAS  PubMed  Google Scholar 

  99. Gong H, Kovar J, Little G, Chen H, Olive DM (2010) Neoplasia 12(2):139–149

    CAS  PubMed Central  PubMed  Google Scholar 

  100. Schier R, Bye J, Apell G, McCall A, Adams GP, Malmqvist M, Weiner LM, Marks JD (1996) J Mol Biol 255(1):28–43

    CAS  PubMed  Google Scholar 

  101. Yang L, Mao H, Wang YA, Cao Z, Peng X, Wang X, Duan H, Ni C, Yuan Q, Adams G, Smith MQ, Wood WC, Gao X, Nie S (2009) Small 5(2):235–243

    CAS  PubMed Central  PubMed  Google Scholar 

  102. Wei L, Li S, Yang J, Ye Y, Zou J, Wang L, Long R, Zurkiya O, Zhao T, Johnson J, Qiao J, Zhou W, Castiblanco A, Maor N, Chen Y, Mao H, Hu X, Yang JJ, Liu ZR (2010) Mol Imaging Biol 13:416–423

    Google Scholar 

  103. Nygren PA (2008) FEBS J 275(11):2668–2676

    CAS  PubMed  Google Scholar 

  104. Wikman M, Steffen AC, Gunneriusson E, Tolmachev V, Adams GP, Carlsson J, Stahl S (2004) Protein Eng Des Sel 17(5):455–462

    CAS  PubMed  Google Scholar 

  105. Tolmachev V, Orlova A, Pehrson R, Galli J, Baastrup B, Andersson K, Sandstrom M, Rosik D, Carlsson J, Lundqvist H, Wennborg A, Nilsson FY (2007) Cancer Res 67(6):2773–2782

    CAS  PubMed  Google Scholar 

  106. Kramer-Marek G, Kiesewetter DO, Martiniova L, Jagoda E, Lee SB, Capala J (2008) Eur J Nucl Med Mol Imaging 35(5):1008–1018

    CAS  PubMed Central  PubMed  Google Scholar 

  107. Orlova A, Rosik D, Sandstrom M, Lundqvist H, Einarsson L, Tolmachev V (2007) Q J Nucl Med Mol Imaging 51(4):314–323

    CAS  PubMed  Google Scholar 

  108. Orlova A, Magnusson M, Eriksson TL, Nilsson M, Larsson B, Hoiden-Guthenberg I, Widstrom C, Carlsson J, Tolmachev V, Stahl S, Nilsson FY (2006) Cancer Res 66(8):4339–4348

    CAS  PubMed  Google Scholar 

  109. Namavari M, Padilla De Jesus O, Cheng Z, De A, Kovacs E, Levi J, Zhang R, Hoerner JK, Grade H, Syud FA, Gambhir SS (2008) Mol Imaging Biol 10(4):177–181

    PubMed  Google Scholar 

  110. Chen TJ, Cheng TH, Chen CY, Hsu SC, Cheng TL, Liu GC, Wang YM (2008) J Biol Inorg Chem 14:253–260

    PubMed  Google Scholar 

  111. Helm L (2010) Future Med Chem 2(3):385–396

    CAS  PubMed  Google Scholar 

  112. Bloembergen N (1957) J Chem Phys 27:572–573

    CAS  Google Scholar 

  113. Bloembergen N, Morgan R (1961) J Chem Phys 34:842

    CAS  Google Scholar 

  114. Solomon I (1955) Phys Rev 99:559–565

    CAS  Google Scholar 

  115. Freed JH (1978) J Chem Phys 68(9):4034–4037

    CAS  Google Scholar 

  116. Aime S, Castelli DD, Crich SG, Gianolio E, Terreno E (2009) Acc Chem Res 42(7):822–831

    CAS  PubMed  Google Scholar 

  117. Caravan P (2009) Acc Chem Res 42(7):851–862

    CAS  PubMed  Google Scholar 

  118. Datta A, Raymond KN (2009) Acc Chem Res 42(7):938–947

    CAS  PubMed Central  PubMed  Google Scholar 

  119. Xue S, Qiao J, Pu F, Cameron M, Yang JJ (2013) Wiley Interdiscip Rev Nanomed Nanobiotechnol 5(2):163–179

    CAS  PubMed  Google Scholar 

  120. Diakova G, Goddard Y, Korb JP, Bryant RG (2011) J Magn Reson 208(2):195–203

    CAS  PubMed Central  PubMed  Google Scholar 

  121. Strauch RC, Mastarone DJ, Sukerkar PA, Song Y, Ipsaro JJ, Meade TJ (2011) J Am Chem Soc 133(41):16346–16349

    CAS  PubMed Central  PubMed  Google Scholar 

  122. Lubag AJ, De Leon-Rodriguez LM, Burgess SC, Sherry AD (2011) Proc Natl Acad Sci USA 108(45):18400–18405

    CAS  PubMed  Google Scholar 

  123. Yang JJ, Yang J, Wei L, Zurkiya O, Yang W, Li S, Zou J, Zhou Y, Maniccia AL, Mao H, Zhao F, Malchow R, Zhao S, Johnson J, Hu X, Krogstad E, Liu ZR (2008) J Am Chem Soc 130(29):9260–9267

    CAS  PubMed Central  PubMed  Google Scholar 

  124. Lu ZR, Parker DL, Goodrich KC, Wang X, Dalle JG, Buswell HR (2004) Magn Reson Med 51(1):27–34

    CAS  PubMed  Google Scholar 

  125. Yang JJ, Ye Y, Carroll A, Yang W, Lee HW (2001) Curr Protein Pept Sci 2(1):1–17

    CAS  PubMed  Google Scholar 

  126. Zhou Y, Xue S, Chen Y, Yang JJ (2013) Methods Mol Biol 963:37–53

    CAS  PubMed  Google Scholar 

  127. Zhou Y, Xue S, Yang JJ (2013) Metallomics 5(1):29–42

    CAS  PubMed Central  PubMed  Google Scholar 

  128. Yanyi C, Shenghui X, Yubin Z, Jie YJ (2010) Sci China Chem 53(1):52–60

    PubMed Central  PubMed  Google Scholar 

  129. Yang W, Wilkins AL, Ye Y, Liu ZR, Li SY, Urbauer JL, Hellinga HW, Kearney A, van der Merwe PA, Yang JJ (2005) J Am Chem Soc 127(7):2085–2093

    CAS  PubMed  Google Scholar 

  130. Yang W, Jones LM, Isley L, Ye Y, Lee HW, Wilkins A, Liu ZR, Hellinga HW, Malchow R, Ghazi M, Yang JJ (2003) J Am Chem Soc 125(20):6165–6171

    CAS  PubMed  Google Scholar 

  131. Yang W, Wilkins AL, Li S, Ye Y, Yang JJ (2005) Biochemistry 44(23):8267–8273

    CAS  PubMed  Google Scholar 

  132. Wilkins AL, Ye Y, Yang W, Lee HW, Liu ZR, Yang JJ (2002) Protein Eng 15(7):571–574

    CAS  PubMed  Google Scholar 

  133. Wang X, Kirberger M, Qiu F, Chen G, Yang JJ (2009) Proteins 75(4):787–798

    CAS  PubMed Central  PubMed  Google Scholar 

  134. Li S, Jiang J, Zou J, Qiao J, Xue S, Wei L, Long R, Wang L, Castiblanco A, White N, Ngo J, Mao H, Liu ZR, Yang JJ (2012) J Inorg Biochem 107(1):111–118

    CAS  PubMed Central  PubMed  Google Scholar 

  135. Nord K, Gunneriusson E, Ringdahl J, Stahl S, Uhlen M, Nygren PA (1997) Nat Biotechnol 15(8):772–777

    CAS  PubMed  Google Scholar 

  136. Qiao J, Li S, Wei L, Jiang J, Long R, Mao H, Wei L, Wang L, Yang H, Grossniklaus HE, Liu ZR, Yang JJ (2011) PLoS ONE 6(3):e18103

    CAS  PubMed Central  PubMed  Google Scholar 

  137. Morse DL, Gillies RJ (2010) Biochem Pharmacol 80(5):731–738

    CAS  PubMed Central  PubMed  Google Scholar 

  138. Shigematsu H, Lin L, Takahashi T, Nomura M, Suzuki M, Wistuba II, Fong KM, Lee H, Toyooka S, Shimizu N, Fujisawa T, Feng Z, Roth JA, Herz J, Minna JD, Gazdar AF (2005) J Natl Cancer Inst 97(5):339–346

    CAS  PubMed  Google Scholar 

  139. Toi M, Sperinde J, Huang W, Saji S, Winslow J, Jin X, Tan Y, Ohno S, Nakamura S, Iwata H, Masuda N, Aogi K, Morita S, Petropoulos C, Bates M (2010) BMC Cancer 10:56

    PubMed Central  PubMed  Google Scholar 

  140. Aime S, Botta M, Garino E, Crich SG, Giovenzana G, Pagliarin R, Palmisano G, Sisti M (2000) Chemistry 6(14):2609–2617

    CAS  PubMed  Google Scholar 

  141. Mankoff DA, Eary JF (2008) Clin Cancer Res 14(22):7159–7160

    PubMed  Google Scholar 

  142. Srinivas M, Aarntzen EH, Bulte JW, Oyen WJ, Heerschap A, de Vries IJ, Figdor CG (2010) Adv Drug Deliv Rev 62(11):1080–1093

    CAS  PubMed  Google Scholar 

  143. Lanza GM, Yu X, Winter PM, Abendschein DR, Karukstis KK, Scott MJ, Chinen LK, Fuhrhop RW, Scherrer DE, Wickline SA (2002) Circulation 106(22):2842–2847

    CAS  PubMed  Google Scholar 

  144. Pan D, Caruthers SD, Hu G, Senpan A, Scott MJ, Gaffney PJ, Wickline SA, Lanza GM (2008) J Am Chem Soc 130(29):9186–9187

    CAS  PubMed Central  PubMed  Google Scholar 

  145. Onn A, Correa AM, Gilcrease M, Isobe T, Massarelli E, Bucana CD, O’Reilly MS, Hong WK, Fidler IJ, Putnam JB, Herbst RS (2004) Clin Cancer Res 10(1 Pt 1):136–143

    CAS  PubMed  Google Scholar 

  146. Selvaggi G, Novello S, Torri V, Leonardo E, De Giuli P, Borasio P, Mossetti C, Ardissone F, Lausi P, Scagliotti GV (2004) Ann Oncol 15(1):28–32

    CAS  PubMed  Google Scholar 

  147. Ohtsuka K, Ohnishi H, Furuyashiki G, Nogami H, Koshiishi Y, Ooide A, Matsushima S, Watanabe T, Goya T (2006) J Thorac Oncol 1(8):787–795

    PubMed  Google Scholar 

  148. Dancer J, Takei H, Ro JY, Lowery-Nordberg M (2007) Oncol Rep 18(1):151–155

    CAS  PubMed  Google Scholar 

  149. Bloomston M, Bhardwaj A, Ellison EC, Frankel WL (2006) Dig Surg 23(1–2):74–79

    CAS  PubMed  Google Scholar 

  150. Thybusch-Bernhardt A, Beckmann S, Juhl H (2001) Int J Surg Investig 2(5):393–400

    CAS  PubMed  Google Scholar 

  151. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL (1987) Science 235(4785):177–182

    CAS  PubMed  Google Scholar 

  152. Paik S, Bryant J, Tan-Chiu E, Yothers G, Park C, Wickerham DL, Wolmark N (2000) J Natl Cancer Inst 92(24):1991–1998

    CAS  PubMed  Google Scholar 

  153. Owens MA, Horten BC, Da Silva MM (2004) Clin Breast Cancer 5(1):63–69

    CAS  PubMed  Google Scholar 

  154. Seshadri R, Firgaira FA, Horsfall DJ, McCaul K, Setlur V, Kitchen P (1993) J Clin Oncol 11(10):1936–1942

    CAS  PubMed  Google Scholar 

  155. Andrulis IL, Bull SB, Blackstein ME, Sutherland D, Mak C, Sidlofsky S, Pritzker KP, Hartwick RW, Hanna W, Lickley L, Wilkinson R, Qizilbash A, Ambus U, Lipa M, Weizel, H, Katz A, Baida M, Mariz S, Stoik G, Dacamara P, Strongitharm D, Geddie W, McCready D (1998) J Clin Oncol 16(4):1340–1349

    CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Katheryn Meenach, Anvi Patel, and Rose Auguste for careful editing of the manuscript, and Robert Long, Hua Yang, and Hans Grossniklaus for MRI and immunohistological experiments. This work was supported by research grants from the National Institutes of Health (EB007268 and GM62999) to J.J.Y.

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Authors and Affiliations

  1. Department of Chemistry, Georgia State University, 50 Decatur Street, 550 NSC, Atlanta, GA, 30303, USA

    Jingjuan Qiao, Shenghui Xue, Fan Pu, Natalie White, Jie Jiang & Jenny J. Yang

  2. Department of Biology, Georgia State University, Atlanta, GA, 30303, USA

    Shenghui Xue & Zhi-Ren Liu

  3. Center for Diagnostics and Therapeutics, Georgia State University, Atlanta, GA, 30303, USA

    Zhi-Ren Liu & Jenny J. Yang

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  1. Jingjuan Qiao
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  2. Shenghui Xue
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Correspondence to Jenny J. Yang.

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Responsible Editor: Valerie C. Pierre

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Qiao, J., Xue, S., Pu, F. et al. Molecular imaging of EGFR/HER2 cancer biomarkers by protein MRI contrast agents. J Biol Inorg Chem 19, 259–270 (2014). https://doi.org/10.1007/s00775-013-1076-3

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  • DOI: https://doi.org/10.1007/s00775-013-1076-3

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