The human heart contains distinct macrophage subsets with divergent origins and functions

Nature Medicine

Volumn 24, Issue 8, 2018, Pages 1234-1245

  Bajpai, Geetika ^a   Schneider, Caralin ^a   Wong, Nicole ^a   Bredemeyer, Andrea ^a   Hulsmans, Maarten ^b   Nahrendorf, Matthias ^b   Epelman, Slava ^c   Kreisel, Daniel ^a   Liu, Yongjian ^a   Itoh, Akinobu ^a   Shankar, Thirupura S ^d   Selzman, Craig H ^d   Drakos, Stavros G ^d   Lavine, Kory J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR2;

ADULT; ARTICLE; CARDIAC MUSCLE; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; GRAFT RECIPIENT; HEART; HEART TRANSPLANTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MACROPHAGE; MALE; MONOCYTE; PRIORITY JOURNAL; CYTOLOGY; HEART FAILURE; HEART LEFT VENTRICLE FUNCTION; INFLAMMATION; METABOLISM; PATHOLOGY; WEIGHT BEARING;

ADULT; HEART FAILURE; HUMANS; INFLAMMATION; MACROPHAGES; MYOCARDIUM; RECEPTORS, CCR2; VENTRICULAR DYSFUNCTION, LEFT; WEIGHT-BEARING;

EID: 85048281756     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/s41591-018-0059-x     Document Type: Article

References (46)

1. Van Furth, R. & Cohn, Z. A. The origin and kinetics of mononuclear phagocytes. J. Exp. Med. 128, 415–435 (1968).
2. Volkman, A., Chang, N. C., Strausbauch, P. H. & Morahan, P. S. Differential effects of chronic monocyte depletion on macrophage populations. Lab. Invest. 49, 291–298 (1983).
3. Sawyer, R. T., Strausbauch, P. H. & Volkman, A. Resident macrophage proliferation in mice depleted of blood monocytes by strontium-89. Lab. Invest. 46, 165–170 (1982).
4. Ginhoux, F. et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330, 841–845 (2010).
5. Schulz, C. et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336, 86–90 (2012).
6. Yona, S. et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38, 79–91 (2013).
7. Hashimoto, D. et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 38, 792–804 (2013).
8. Epelman, S. et al. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity 40, 91–104 (2014).
9. Guilliams, M. et al. Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J. Exp. Med. 210, 1977–1992 (2013).
10. Jakubzick, C. et al. Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes. Immunity 39, 599–610 (2013).
11. Gordon, S. & Pluddemann, A. Tissue macrophages: heterogeneity and functions. BMC Biol. 15, 53 (2017).
12. Boyer, S. W., Schroeder, A. V., Smith-Berdan, S. & Forsberg, E. C. All hematopoietic cells develop from hematopoietic stem cells through Flk2/Flt3-positive progenitor cells. Cell Stem Cell 9, 64–73 (2011).
13. Hoeffel, G. et al. Adult Langerhans cells derive predominantly from embryonic fetal liver monocytes with a minor contribution of yolk sac–derived macrophages. J. Exp. Med. 209, 1167–1181 (2012).
14. Sieweke, M. H. & Allen, J. E. Beyond stem cells: self-renewal of differentiated macrophages. Science 342, 1242974 (2013).
15. Davies, L. C., Jenkins, S. J., Allen, J. E. & Taylor, P. R. Tissue-resident macrophages. Nat. Immunol. 14, 986–995 (2013).
16. Wynn, T. A., Chawla, A. & Pollard, J. W. Macrophage biology in development, homeostasis and disease. Nature 496, 445–455 (2013).
17. Lavine, K. J. et al. Distinct macrophage lineages contribute to disparate patterns of cardiac recovery and remodeling in the neonatal and adult heart. Proc. Natl Acad. Sci. USA 111, 16029–16034 (2014).
18. Leid, J. et al. Primitive embryonic macrophages are required for coronary development and maturation. Circ. Res. 118, 1498–1511 (2016).
19. Li, W. et al. Heart-resident CCR2 + macrophages promote neutrophil extravasation through TLR9/MyD88/CXCL5 signaling. JCI Insight 1, e87315 (2016).
20. Xue, J. et al. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity 40, 274–288 (2014).
21. Hulsmans, M. Macrophages facilitate electrical conduction in the heart. Cell 169, 510–522 (2017).
22. Sager, H. B. et al. Proliferation and recruitment contribute to myocardial macrophage expansion in chronic heart failure. Circ. Res. 119, 853–864 (2016).
23. Gautier, E. L. et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13, 1118–1128 (2012).
24. Reynolds, G. Human and mouse mononuclear phagocyte networks: A tale of two species. Front. Immunol. 6, 330 (2015).
25. Zarif, J. C. A phased strategy to differentiate human CD14 + monocytes into classically and alternatively activated macrophages and dendritic cells. Biotechniques 61, 33–41 (2016).
26. Garlanda, C., Bottazzi, B., Bastone, A. & Mantovani, A. Pentraxins at the crossroads between innate immunity, inflammation, matrix deposition, and female fertility. Annu. Rev. Immunol. 23, 337–366 (2005).
27. Fujiu, K. et al. A heart–brain–kidney network controls adaptation to cardiac stress through tissue macrophage activation. Nat. Med. 23, 611–622 (2017).
28. Kubin, T. et al. Oncostatin M is a major mediator of cardiomyocyte dedifferentiation and remodeling. Cell Stem Cell 9, 420–432 (2011).
29. Vickers, A. E. et al. Organ slice viability extended for pathway characterization: an in vitro model to investigate fibrosis. Toxicol. Sci. 82, 534–544 (2004).
30. Brandenburger, M. et al. Organotypic slice culture from human adult ventricular myocardium. Cardiovasc. Res. 93, 50–59 (2012).
31. Diakos, N. A. et al. Myocardial atrophy and chronic mechanical unloading of the failing human heart: implications for cardiac assist device-induced myocardial recovery. J. Am. Coll. Cardiol. 64, 1602–1612 (2014).
32. Drakos, S. G. et al. Magnitude and time course of changes induced by continuous-flow left ventricular assist device unloading in chronic heart failure: insights into cardiac recovery. J. Am. Coll. Cardiol. 61, 1985–1994 (2013).
33. Epelman, S., Lavine, K. J. & Randolph, G. J. Origin and functions of tissue macrophages. Immunity. 41, 21–35 (2014).
34. Heidt, T. et al. Differential contribution of monocytes to heart macrophages in steady-state and after myocardial infarction. Circ. Res. 115, 284–295 (2014).
35. Molawi, K. et al. Progressive replacement of embryo-derived cardiac macrophages with age. J. Exp. Med. 211, 2151–2158 (2014).
36. Kaufmann, A., Salentin, R., Gemsa, D. & Sprenger, H. Increase of CCR1 and CCR5 expression and enhanced functional response to MIP-1 alpha during differentiation of human monocytes to macrophages. J. Leukoc. Biol. 69, 248–252 (2001).
37. Weber, C. et al. Differential chemokine receptor expression and function in human monocyte subpopulations. J. Leukoc. Biol. 67, 699–704 (2000).
38. Burchfield, J. S., Xie, M. & Hill, J. A. Pathological ventricular remodeling: mechanisms: part 1 of 2. Circulation 128, 388–400 (2013).
39. Kanitakis, J., Petruzzo, P. & Dubernard, J. M. Turnover of epidermal Langerhans’ cells. N. Engl. J. Med. 351, 2661–2662 (2004).
40. Eguiluz-Gracia, I. et al. Long-term persistence of human donor alveolar macrophages in lung transplant recipients. Thorax 71, 1006–1011 (2016).
41. Bittmann, I. et al. Cellular chimerism of the lung after transplantation. An interphase cytogenetic study. Am. J. Clin. Pathol. 115, 525–533 (2001).
42. Haniffa, M. Differential rates of replacement of human dermal dendritic cells and macrophages during hematopoietic stem cell transplantation. J. Exp. Med. 206, 371–385 (2009).
43. Dickinson, R. E. et al. Exome sequencing identifies GATA-2 mutation as the cause of dendritic cell, monocyte, B and NK lymphoid deficiency. Blood 118, 2656–2658 (2011).
44. Hambleton, S. IRF8 mutations and human dendritic-cell immunodeficiency. N. Engl. J. Med. 365, 127–138 (2011).
45. Bigley, V. et al. The human syndrome of dendritic cell, monocyte, B and NK lymphoid deficiency. J. Exp. Med. 208, 227–234 (2011).
46. Desch, A. N. Flow cytometric analysis of mononuclear phagocytes in nondiseased human lung and lung-draining lymph nodes. Am. J. Respir. Crit. Care Med. 193, 614–626 (2016).