Use of folate-conjugated imaging agents to target alternatively activated macrophages in a murine model of asthma

Molecular Pharmaceutics

Volumn 10, Issue 5, 2013, Pages 1918-1927

  Shen, Jiayin ^a   Chelvam, Venkatesh ^a,c   Cresswell, Gregory ^b   Low, Philip S ^a  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c INDIAN INSTITUTE OF TECHNOLOGY INDORE   (India)

Author keywords

alternatively activated macrophages; EC20; folate receptor ; folate targeting; radioimaging of asthma; technetium 99m imaging

Indexed keywords

ARGINASE 1; EC 20; ETARFOLATIDE TC 99M; FLUORESCENT DYE; FOLATE RECEPTOR 2; FOLIC ACID; MANNOSE RECEPTOR; RADIOPHARMACEUTICAL AGENT; TECHNETIUM 99M; UNCLASSIFIED DRUG; ARG1 PROTEIN, MOUSE; ARGINASE; CELL SURFACE RECEPTOR; EC20 FOLATE PEPTIDE; LECTIN; MANNOSE BINDING LECTIN; OLIGOPEPTIDE; TECHNETIUM;

ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG CONJUGATION; DRUG DELIVERY SYSTEM; DRUG FORMULATION; DRUG TARGETING; FEMALE; LUNG ALVEOLUS MACROPHAGE; LUNG PARENCHYMA; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RADIOGRAPHY; ANALOGS AND DERIVATIVES; ANIMAL; ASTHMA; BAGG ALBINO MOUSE; DIAGNOSTIC IMAGING; DIAGNOSTIC USE; DISEASE MODEL; HUMAN; IMMUNOLOGY; LUNG; MACROPHAGE; METABOLISM; PROCEDURES; SCINTISCANNING;

ANIMALS; ARGINASE; ASTHMA; DIAGNOSTIC IMAGING; DISEASE MODELS, ANIMAL; FEMALE; FLUORESCENT DYES; FOLATE RECEPTOR 2; FOLIC ACID; HUMANS; LECTINS, C-TYPE; LUNG; MACROPHAGE ACTIVATION; MACROPHAGES; MANNOSE-BINDING LECTINS; MICE; MICE, INBRED BALB C; OLIGOPEPTIDES; RADIOPHARMACEUTICALS; RECEPTORS, CELL SURFACE; TECHNETIUM;

EID: 84877274683     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp3006962     Document Type: Article

References (38)

1. Kim, H. Y.; DeKruyff, R. H.; Umetsu, D. T. The many paths to asthma: phenotype shaped by innate and adaptive immunity Nat. Immunol. 2010, 11, 577-584
2. Zimmermann, N.; King, N. E.; Laporte, J.; Yang, M.; Mishra, A.; Pope, S. M.; Muntel, E. E.; Witte, D. P.; Pegg, A. A.; Foster, P. S.; Hamid, Q.; Rothenberg, M. E. Dissection of experimental asthma with DNA microarray analysis identifies arginase in asthma pathogenesis J. Clin. Invest. 2003, 111, 1863-1874
3. Zhu, Z.; Zheng, T.; Homer, R. J.; Kim, Y. K.; Chen, N. Y.; Cohn, L.; Hamid, Q.; Elias, J. A. Acidic mammalian Chitinase in asthmatic Th2 inflammation and IL-13 pathway activation Science 2004, 304, 1678-1682
4. Maarsingh, H.; Zuidhof, A. B.; Bos, I. S.; van Duin, M.; Boucher, J. L.; Zaagsma, J.; Meurs, H. Arginase inhibition protects against allergen-induced airway obstruction, hyperresponsiveness, and inflammation Am. J. Respir. Crit. Care. Med. 2008, 178, 565-573
5. Mantovani, A.; Sica, A.; Sozzani, S.; Allavena, P.; Vecchi, A.; Locati, M. The chemokine system in diverse forms of macrophage activation and polarization Trends Immunol. 2004, 25, 677-686
6. Melgert, B. N.; Oriss, T. B.; Qi, Z.; Dixon-McCarthy, B.; Geerlings, M.; Hylkema, M. N.; Ray, A. Macrophages: regulators of sex differences in asthma? Am. J. Respir. Cell Mol. Biol. 2010, 42, 595-603
7. Kamen, B. A. Folate receptor α, a review. In Symposium on folates and human development; Massaro, E.; Rogers, J. M., Eds.; Humana Press: New York, 2002; pp 117-135.
8. Ross, J. F.; Chaudhuri, P. K.; Ratnam, M. Differential regulation of folate receptor isoforms in normal and malignant tissues in vivo and in established cell lines. Physiologic and clinical implications Cancer 1994, 73, 2432-2443
9. Ross, J. F.; Wang, H.; Behm, F. G.; Mathew, P.; Wu, M.; Booth, R.; Ratnam, M. Folate receptor type beta is a neutrophilic lineage marker and is differentially expressed in myeloid leukemia Cancer 1999, 85, 348-357
10. Reddy, J. A.; Haneline, L. S.; Srour, E. F.; Antony, A. C.; Clapp, D. W.; Low, P. S. Expression and functional characterization of the beta-isoform of the folate receptor on CD34(+) cells Blood 1999, 93, 3940-3948
11. Pan, X. Q.; Zheng, X.; Shi, G.; Wang, H.; Ratnam, M.; Lee, R. J. Strategy for the treatment of acute myelogenous leukemia based on folate receptor beta-targeted liposomal doxorubicin combined with receptor induction using all-trans retinoic acid Blood 2002, 100, 594-602
12. Matteson, E. L.; Lowe, V. J.; Prendergast, F. G.; Crowson, C. S.; Moder, K. G.; Morgenstern, D. E.; Messmann, R. A.; Low, P. S. Assessment of disease activity in rheumatoid arthritis using a novel folate targeted radiopharmaceutical Folatescan Clin. Exp. Rheumatol. 2009, 27, 253-259
13. Xia, W.; Hilgenbrink, A. R.; Matteson, E. L.; Lockwood, M. B.; Cheng, J. X.; Low, P. S. A functional folate receptor is induced during macrophage activation and can be used to target drugs to activated macrophages Blood 2009, 113, 438-446
14. Ayala-Lopez, W.; Xia, W.; Varghese, B.; Low, P. S. Imaging of Atherosclerosis in Apoliprotein E Knockout Mice: Targeting of a Folate-Conjugated Radiopharmaceutical to Activated Macrophages J. Nucl. Med. 2010, 51, 768-774
15. Varghese, B.; Haase, N.; Low, P. S. Depletion of Folate-Receptor-Positive Macrophages Leads to Alleviation of Symptoms and Prolonged Survival in Two Murine Models of Systemic Lupus Erythematosus Mol. Pharmaceutics 2007, 4, 679-685
16. Low, P. S.; Henne, W. A.; Doorneweerd, D. D. Discovery and Development of Folic-Acid-Based Receptor Targeting for Imaging and Therapy of Cancer and Inflammatory Diseases Acc. Chem. Res. 2008, 41, 120-129
17. Tsuneyoshi, Y.; Tanaka, M.; Nagai, T.; Sunahara, N.; Matsuda, T.; Sonoda, T.; Ijiri, K.; Komiya, S.; Matsuyama, T. Functional folate receptor beta-expressing macrophages in osteoarthritis synovium and their M1/M2 expression profiles Scand. J. Rheumatol. 2012, 41, 132-140
18. Puig-Kröger, A.; Sierra-Filardi, E.; Domínguez-Soto, A.; Samaniego, R.; Corcuera, M. T.; Gómez-Aguado, F.; Ratnam, M.; Sánchez-Mateos, P.; Corbí, A. L. Folate receptor beta is expressed by tumor-associated macrophages and constitutes a marker for M2 anti-inflammatory/regulatory macrophages Cancer Res. 2009, 69, 9395-9403
19. Kurahara, H.; Takao, S.; Kuwahata, T.; Nagai, T.; Ding, Q.; Maeda, K.; Shinchi, H.; Mataki, Y.; Maemura, K.; Matsuyama, T.; Natsugoe, S. Clinical significance of folate receptor β-expressing tumor-associated macrophages in pancreatic cancer Ann. Surg. Oncol. 2012, 19, 2264-2271
20. Nagai, T.; Tanaka, M.; Hasui, K.; Shirahama, H.; Kitajima, S.; Yonezawa, S.; Xu, B.; Matsuyama, T. Effect of an immunotoxin to folate receptor beta on bleomycin-induced experimental pulmonary fibrosis Clin. Exp. Immunol. 2010, 161, 348-356
21. Song, C.; Luo, L.; Lei, Z.; Li, B.; Liang, Z.; Liu, G.; Li, D.; Zhang, G.; Huang, B.; Feng, Z. H. IL-17-producing alveolar macrophages mediate allergic lung inflammation related to asthma J. Immunol. 2008, 181, 6117-6124
22. Yamaguchi, T.; Hirota, K.; Nagahama, K.; Ohkawa, K.; Takahashi, T.; Nomura, T.; Sakaguchi, S. Control of immune responses by antigen-specific regulatory T cells expressing the folate receptor Immunity 2007, 27, 145-159
23. Nagai, T.; Tanaka, M.; Tsuneyoshi, Y.; Xu, B.; Michie, S. A.; Hasui, K.; Hirano, H.; Arita, K.; Matsuyama, T. Targeting tumor-associated macrophages in an experimental glioma model with a recombinant immunotoxin to folate receptor beta Cancer Immunol. Immunother. 2009, 58, 1577-1586
24. Rauh, M. J.; Ho, V.; Pereira, C.; Sham, A.; Sly, L. M.; Lam, V.; Huxham, L.; Minchinton, A. I.; Mui, A.; Krystal, G. SHIP represses the generation of alternatively activated macrophages Immunity 2005, 23, 361-374
25. Yang, M.; Rangasamy, D.; Matthaei, K. I.; Frew, A. J.; Zimmmermann, N.; Mahalingam, S.; Webb, D. C.; Tremethick, D. J.; Thompson, P. J.; Hogan, S. P.; Rothenberg, M. E.; Cowden, W. B.; Foster, P. S. Inhibition of arginase I activity by RNA interference attenuates IL-13-induced airways hyperresponsiveness J. Immunol. 2006, 177, 5595-5603
26. Stolarski, B.; Kurowska-Stolarska, M.; Kewin, P.; Xu, D.; Liew, F. Y. IL-33 exacerbates eosinophil-mediated airway inflammation J. Immunol. 2010, 185, 3472-3480
27. Martinez, F. O.; Helming, L.; Gordon, S. Alternative activation of macrophages: an immunologic functional perspective Annu. Rev. Immunol. 2009, 27, 451-483
28. Reddy, J. A.; Xu, L. C.; Parker, N.; Vetzel, M.; Leamon, C. P. Preclinical evaluation of (99m)Tc-EC20 for imaging folate receptor-positive tumors J. Nucl. Med. 2004, 45, 857-866
29. Turk, M. J.; Breur, G. J.; Widmer, W. R.; Paulos, C. M.; Xu, L. C.; Grote, L. A.; Low, P. S. Folate-targeted Imaging of Activated Macrophages in Rats with Adjuvant-Induced Arthritis Arthritis Rheum. 2002, 46, 1947-1955
30. Piscaer, T. M.; Müller, C.; Mindt, T. L.; Lubberts, E.; Verhaar, J. A.; Krenning, E. P.; Schibli, R.; De Jong, M.; Weinans, H. Imaging of activated macrophages in experimental osteoarthritis using folate-targeted animal single-photon-emission computed tomography/computed tomography Arthritis Rheum. 2011, 63, 1898-907
31. Henne, W. A.; Rothenbuhler, R.; Ayala-Lopez, W.; Xia, W.; Varghese, B.; Low, P. S. Imaging sites of infection using a 99mTc-labeled folate conjugate targeted to folate receptor positive macrophages Mol. Pharmaceutics 2012, 9, 1435-1440
32. Lu, Y.; Stinnette, T. W.; Westrick, E.; Klein, P. J.; Gehrke, M. A.; Cross, V. A.; Vlahov, I. R.; Low, P. S.; Leamon, C. P. Treatment of experimental adjuvant arthritis with a novel folate receptor-targeted folic acid-aminopterin conjugate Arthritis Res. Ther. 2011, 13, R56
33. Wynn, T. A. Fibrotic disease and the T(H)1/T(H)2 paradigm Nat. Rev. Immunol. 2004, 4, 583-594
34. Murray, P. J.; Wynn, T. A. Protective and pathogenic functions of macrophage subsets Nat. Rev. Immunol. 2011, 11, 723-737
35. Qian, B. Z.; Pollard, J. W. Macrophage diversity enhances tumor progression and metastasis Cell 2010, 141, 39-51
36. Steidl, C.; Lee, T.; Shah, S. P.; Farinha, P.; Han, G.; Nayar, T.; Delaney, A.; Jones, S. J.; Iqbal, J.; Weisenburger, D. D.; Bast, M. A.; Rosenwald, A.; Muller-Hermelink, H. K.; Rimsza, L. M.; Campo, E.; Delabie, J.; Braziel, R. M.; Cook, J. R.; Tubbs, R. R.; Jaffe, E. S.; Lenz, G.; Connors, J. M.; Staudt, L. M.; Chan, W. C.; Gascoyne, R. D. Tumor-associated macrophages and survival in classic Hodgkin's lymphoma N. Engl. J. Med. 2010, 362, 875-885
37. Leek, R. D.; Lewis, C. E.; Whitehouse, R.; Greenall, M.; Clarke, J.; Harris, A. L. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma Cancer Res. 1996, 56, 4625-4629
38. Sandoval, R. M.; Kennedy, M. D.; Low, P. S.; Molitoris, B. A. Uptake and Trafficking of Fluorescent Conjugates of Folic Acid in the Intact Kidney Using Intra-Vital 2-Photon Microscopy Am. J. Physiol. Cell Physiol. 2004, 287, C517-526