journal article·2022-03-22Open access

Albumin Nanoparticle Endocytosing Subset of Neutrophils for Precision Therapeutic Targeting of Inflammatory Tissue Injury

Kurt Bachmaier, Andrew Stuart, Abhalaxmi Singh, Amitabha Mukhopadhyay, Sreeparna Chakraborty, Zhigang Hong, Li Wang, Yoshikazu Tsukasaki, Mark Maienschein-Cline, Balaji B. Ganesh, Prasad Kanteti, Jalees Rehman, Asrar B. Malik

ACS Nano· Volume 16· Issue 3

Abstract

The complex involvement of neutrophils in inflammatory diseases makes them intriguing but challenging targets for therapeutic intervention. Here, we tested the hypothesis that varying endocytosis capacities would delineate functionally distinct neutrophil subpopulations that could be specifically targeted for therapeutic purposes. By using uniformly sized (∼120 nm in diameter) albumin nanoparticles (ANP) to characterize mouse neutrophils in vivo, we found two subsets of neutrophils, one that readily endocytosed ANP (ANPhigh neutrophils) and another that failed to endocytose ANP (ANPlow population). These ANPhigh and ANPlow subsets existed side by side simultaneously in bone marrow, peripheral blood, spleen, and lungs, both under basal conditions and after inflammatory challenge. Human peripheral blood neutrophils showed a similar duality. ANPhigh and ANPlow neutrophils had distinct cell surface marker expression and transcriptomic profiles, both in naive mice and in mice after endotoxemic challenge. ANPhigh and ANPlow neutrophils were functionally distinct in their capacities to kill bacteria and to produce inflammatory mediators. ANPhigh neutrophils produced inordinate amounts of reactive oxygen species and inflammatory chemokines and cytokines. Targeting this subset with ANP loaded with the drug piceatannol, a spleen tyrosine kinase (Syk) inhibitor, mitigated the effects of polymicrobial sepsis by reducing tissue inflammation while fully preserving neutrophilic host-defense function.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Neutrophil, Myeloperoxidase and Oxidative Mechanisms · Immune Response and Inflammation · Immune cells in cancer

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of Pharmacology and Regenerative Medicine and the Center for Lung and Vascular Biology, The University of Illinois College of Medicine, E403, 835 South Wolcott Avenue, Chicago, Illinois 60612, United States

Nano Biotherapeutics, Inc., 2201 West Campbell Park Drive, Chicago, Illinois 60612, United States

Division of Cardiology, Department of Medicine, The University of Illinois College of Medicine, Chicago, Illinois 60612, United States

Research Resources Center, University of Illinois at Chicago, Chicago, Illinois 60612, United States

Funding

National Heart, Lung, and Blood Institute

References (79)

Show source-provided references
1. 10.1053/j.gastro.2012.09.00810.1053/j.gastro.2012.09.008 ↗
2. 10.1016/j.immuni.2016.12.01210.1016/j.immuni.2016.12.012 ↗
3. 10.1016/j.it.2019.05.00110.1016/j.it.2019.05.001 ↗
4. 10.1056/NEJM19890209320060610.1056/NEJM198902093200606 ↗
5. 10.1038/s41590-019-0399-910.1038/s41590-019-0399-9 ↗
6. 10.1016/j.cell.2014.11.01810.1016/j.cell.2014.11.018 ↗
7. 10.1126/science.125141410.1126/science.1251414 ↗
8. 10.1038/nature1203410.1038/nature12034 ↗
9. 10.1016/j.it.2019.04.01310.1016/j.it.2019.04.013 ↗
10. 10.1016/j.cell.2020.10.00310.1016/j.cell.2020.10.003 ↗
11. 10.3389/fimmu.2014.0050810.3389/fimmu.2014.00508 ↗
12. 10.1016/j.ccr.2009.06.01710.1016/j.ccr.2009.06.017 ↗
13. 10.1038/nrc.2016.5210.1038/nrc.2016.52 ↗
14. 10.1093/eurheartj/ehw00210.1093/eurheartj/ehw002 ↗
15. 10.1038/s41590-019-0496-910.1038/s41590-019-0496-9 ↗
16. 10.1038/nrneph.2016.7110.1038/nrneph.2016.71 ↗
17. 10.1161/STROKEAHA.113.00247010.1161/STROKEAHA.113.002470 ↗
18. 10.1016/j.immuni.2004.07.00610.1016/j.immuni.2004.07.006 ↗
19. 10.1371/journal.ppat.100482710.1371/journal.ppat.1004827 ↗
20. 10.1172/JCI5799010.1172/JCI57990 ↗
21. 10.1126/sciimmunol.aay601710.1126/sciimmunol.aay6017 ↗
22. 10.1016/j.immuni.2019.03.00910.1016/j.immuni.2019.03.009 ↗
23. 10.1177/002203451664556410.1177/0022034516645564 ↗
24. 10.1038/s41573-019-0054-z10.1038/s41573-019-0054-z ↗
25. 10.1038/ncomms1215010.1038/ncomms12150 ↗
26. 10.1016/j.addr.2018.07.01110.1016/j.addr.2018.07.011 ↗
27. 10.1038/nnano.2014.1710.1038/nnano.2014.17 ↗
28. 10.1074/jbc.M00632720010.1074/jbc.M006327200 ↗
29. 10.1111/imr.1262110.1111/imr.12621 ↗
30. 10.1038/nbt.259410.1038/nbt.2594 ↗
31. 10.1172/JCI1651010.1172/JCI16510 ↗
32. 10.1038/nm166510.1038/nm1665 ↗
33. 10.1073/pnas.090276110610.1073/pnas.0902761106 ↗
34. 10.1084/jem.2010023910.1084/jem.20100239 ↗
35. 10.1016/j.tim.2011.01.00110.1016/j.tim.2011.01.001 ↗
36. 10.1016/S0021-9258(18)43936-110.1016/S0021-9258(18)43936-1 ↗
37. 10.1016/S0014-2999(02)01534-010.1016/S0014-2999(02)01534-0 ↗
38. 10.1165/rcmb.2021-0318MA10.1165/rcmb.2021-0318MA ↗
39. Mayadas T. N. · 2014 · 9 · 181
40. 10.1089/ars.2012.514910.1089/ars.2012.5149 ↗
41. 10.1016/S1074-7613(02)00303-510.1016/S1074-7613(02)00303-5 ↗
42. 10.1016/S1074-7613(00)80004-710.1016/S1074-7613(00)80004-7 ↗
43. 10.1126/sciimmunol.aam892910.1126/sciimmunol.aam8929 ↗
44. 10.1172/JCI11760710.1172/JCI117607 ↗
45. 10.1172/JCI6033110.1172/JCI60331 ↗
46. 10.1136/bmj.i158510.1136/bmj.i1585 ↗
47. 10.1378/chest.126.4_MeetingAbstracts.873S10.1378/chest.126.4_MeetingAbstracts.873S ↗
48. 10.1080/00984109616133910.1080/009841096161339 ↗
49. 10.1182/blood-2009-05-22080610.1182/blood-2009-05-220806 ↗
50. 10.1038/nrdp.2016.4510.1038/nrdp.2016.45 ↗
51. Whyte M. K. · J. Immunol. · 1993 · 150 · 512410.4049/jimmunol.150.11.5124 ↗
52. 10.1038/nature1536710.1038/nature15367 ↗
53. 10.1056/NEJMra05272310.1056/NEJMra052723 ↗
54. 10.1002/path.149110.1002/path.1491 ↗
55. 10.1038/nri307010.1038/nri3070 ↗
56. 10.1084/jem.2005077810.1084/jem.20050778 ↗
57. 10.1038/s41590-019-0571-210.1038/s41590-019-0571-2 ↗
58. 10.1136/thoraxjnl-2013-20474210.1136/thoraxjnl-2013-204742 ↗
59. 10.1016/j.jconrel.2014.05.03610.1016/j.jconrel.2014.05.036 ↗
60. 10.1038/s41565-021-00997-y10.1038/s41565-021-00997-y ↗
61. 10.1038/nm.193910.1038/nm.1939 ↗
62. 10.1016/j.ijid.2020.03.00410.1016/j.ijid.2020.03.004 ↗
63. 10.1016/S2213-2600(20)30527-010.1016/S2213-2600(20)30527-0 ↗
64. 10.1126/science.abb892510.1126/science.abb8925 ↗
65. 10.1016/j.cytogfr.2020.05.00310.1016/j.cytogfr.2020.05.003 ↗
66. 10.1002/JLB.3RI0917-361R10.1002/JLB.3RI0917-361R ↗
67. 10.1038/nm160710.1038/nm1607 ↗
68. 10.1093/bioinformatics/bts63510.1093/bioinformatics/bts635 ↗
69. 10.1093/bioinformatics/btt65610.1093/bioinformatics/btt656 ↗
70. 10.1093/nar/gks04210.1093/nar/gks042 ↗
71. 10.1093/bioinformatics/btp61610.1093/bioinformatics/btp616 ↗
72. 10.1111/j.2517-6161.1995.tb02031.x10.1111/j.2517-6161.1995.tb02031.x ↗
73. 10.1038/nprot.2008.7310.1038/nprot.2008.73 ↗
74. 10.3791/5204410.3791/52044 ↗
75. 10.1002/cyto.a.2022210.1002/cyto.a.20222 ↗
76. Bachmaier K. · Circulation · 1997 · 96 · 585
77. 10.1007/978-1-61779-527-5_810.1007/978-1-61779-527-5_8 ↗
78. 10.1016/0022-1759(94)00247-T10.1016/0022-1759(94)00247-T ↗
79. 10.1038/nmeth.154310.1038/nmeth.1543 ↗