Surgical adhesions: A sticky macrophage problem

doi:10.1126/science.abg5416

GSTDTAP > 气候变化

DOI	10.1126/science.abg5416
	Surgical adhesions: A sticky macrophage problem
	Sarah E. Herrick; Judith E. Allen
	2021-03-05
发表期刊	Science
出版年	2021
英文摘要	It is estimated that ∼66% of patients who have gastrointestinal surgery will develop adhesions ([ 1 ][1]). These bands of scar tissue arise in the abdominal cavity and can lead to small bowel obstruction and infertility in women as well as severe chronic abdominal pain. Unfortunately, there are no satisfactory ways to prevent adhesions, and once formed, surgery is often required to lyse them, which predisposes to further adhesions. Thus, there is an urgent need to develop more effective means to prevent them from forming or to minimize their growth. On page 1013 of this issue, Zindel et al. ([ 2 ][2]) demonstrate that macrophages in the peritoneal cavity home to sites of damage, forming an immediate protective wound covering. In response to surgical insult, these macrophages act like platelets to form superaggregates, which then develop into adhesions. A fascinating parallel exists with invertebrates whereby body-cavity macrophages express evolutionarily ancient receptors, which may be potential targets for adhesion prevention. The peritoneum is a gliding interface that lines the fluid-filled body cavity and internal organs. It comprises a surface monolayer of mesothelial cells adherent to a basement membrane, overlying a submesothelial connective tissue rich in capillaries and lymphatics. Surgical adhesions are proposed to evolve from initial fibrin clots spanning between internal organs and/or the cavity wall ([ 3 ][3]). Critically, reduced fibrinolysis after surgery and subsequent collagen production stabilizes these initial connections and stimulates the formation of mature myofibroblast-rich fibrous bands. Indeed, experimental animal studies and clinical trials investigating the prevention of surgical adhesions have been based on the idea of regulating coagulation and fibrinolytic pathways ([ 4 ][4]). More recently, attention has shifted to identifying the source of myofibroblasts that stabilize early adhesions. In addition to tissue-resident fibroblasts ([ 5 ][5]), mesothelial cells have been shown to participate in the generation of fibroblasts and adhesion development ([ 6 ][6], [ 7 ][7]) by undergoing a phenotypic switch, called mesothelial-to-mesenchymal transition (MMT). Anti-adhesion strategies are exploring ways to reduce MMT and hence prevent adhesions from forming ([ 8 ][8]). Although reduced fibrinolysis and MMT are recognized events in the biology of surgical adhesions, data on the contribution of macrophages are inconclusive. Rigorous exploration of the heterogeneity and functional diversity of serous-cavity macrophage subpopulations during adhesion formation is needed to resolve this uncertainty ([ 9 ][9]). Macrophages that are free-floating in peritoneal fluid include monocyte-derived cells as well as resident macrophages that rely on the transcription factor GATA-binding protein 6 (GATA6) for their differentiation and survival ([ 10 ][10], [ 11 ][11]). A previous study had demonstrated that GATA6+ cavity macrophages are rapidly recruited, via a nonvascular route, to an injury site on the liver of mice where they assisted tissue repair ([ 12 ][12]). Building on these observations, Zindel et al. showed that within minutes of laser-induced wounding of the cavity wall in mice, GATA6+ macrophages provide a protective wound covering (see the figure). Although it remains unclear exactly how serous-cavity macrophages recognize sites of injury, recruitment was by passive transport, relying on the natural movement of peritoneal fluid. Free-floating macrophages became adherent only after injury. Within several hours, macrophages formed cell-to-cell aggregates with secondary tethers to the initially adherent cells. Notably, GATA6+ macrophages have been found to also aggregate around bacteria introduced into the body cavities of mice ([ 13 ][13]). Zindel et al. showed that cavity macrophage aggregation was calcium dependent and strongly resembled intravascular platelet aggregation. ![Figure][14] Macrophages as precursors to adhesions Free-floating GATA-binding protein 6 (GATA6)–expressing macrophages in the abdominal cavity are recruited to wound sites and form aggregates using scavenger receptors. In response to more severe injury, such as abdominal surgery, they form superaggregates that evolve into mature collagen-rich adhesions. GRAPHIC: C. BICKEL/ SCIENCE An important connection was made to repair processes in invertebrates, such as the purple sea urchin, that also have a body cavity. Macrophage equivalents, known as co elomocytes, also repair internal wounds by initial adherence and then aggregation. As such, Zindel et al. concluded that both coelomocytes and GATA6+ macrophages have conserved evolutionarily ancient roles, functioning as platelets as well as phagocytes after injury. The corollaries with invertebrates also helped to identify the way in which macrophages formed aggregates. The authors ruled out many traditional cell-to-cell adhesion molecules that they had expected to be involved but found that heparin prevented macrophage aggregation. Coelomocytes aggregate using a type of scavenger receptor that contains conserved scavenger receptor cysteine-rich (SRCR) domains, which recognize negatively charged ligands such as heparin. Zindel et al. identified two scavenger receptors with SRCR domains, MARCO (macrophage receptor with collagenous structure) and MSR1 (macrophage scavenger receptor 1), which were highly expressed on peritoneal-cavity macrophages in mice. Inhibition of these receptors did not prevent initial cavity macrophage adherence but did prevent secondary tethering and aggregation. Furthermore, evidence of delayed serosal healing with specific receptor inhibitors highlighted that aggregate formation was integral to the repair process. To investigate the effect of surgery on macrophage aggregation, Zindel et al. made an incisional wound into the abdominal cavity of mice and imaged GATA6+ macrophages over time. As before, initial adherence to the wound and aggregation occurred, but now tethering continued, with macrophages forming superaggregates a hundred times greater in size than those made after a simple laser injury in the closed abdomen. Notably, these superaggregates evolved into collagen-rich adhesions covered with mesothelial cells within 7 days. Switching to a more clinically relevant mouse model of ischaemia-induced adhesions ([ 7 ][7], [ 8 ][8]), the authors found that, again, extensive GATA6+ macrophage superaggregates formed that acted as precursors for adhesion development. Depleting these macrophages or blocking receptor-mediated aggregation resulted in reduced adhesions, and those that did form were not as strong. Of note, cavity macrophage number dropped significantly in peritoneal lavage after surgery, indicating that a large quantity participated in this process. How do these new findings connect with our current understanding of adhesion formation involving reduced fibrinolysis and MMT? Although the extent of injury may determine if GATA6+ macrophages form superaggregates, this process alone is unlikely to drive adhesion formation, which also involves coagulation and fibrin deposition. Indeed, GATA6+ cavity macrophages in mice express coagulation cascade factors and promote macrophage-rich fibrin-containing clots, which are largely responsible for macrophage disappearance after insult to the cavity ([ 13 ][13]). Together, these studies strongly implicate resident macrophages in adhesion development, but much remains to be discovered. For example, it is unclear whether specific GATA6+ macrophage subpopulations are responsible for superaggregation and/or clot formation and whether these “platelet-like” properties can be promoted or inhibited by the immune environment or prior activation history. Although the study of Zindel et al. is perhaps most immediately relevant to adhesions, it would be fascinating to know if SRCR domain–mediated macrophage aggregation contributes to other poorly understood processes, such as the initiation of macrophage-rich granulomas, which encase many pathogens. A critical question is whether macrophages retain extravascular platelet-like functions in the other two body cavities that contain the lung (pleural cavity) and the heart (pericardial cavity), where adhesions can also be a major problem after surgery. In this respect, Wilmstumor-1 (WT1)–expressing mesothelial and fibroblastic stromal cells that are present in all three serosal cavities provide precise signals that instruct the tissue-specific GATA6+ transcriptional program of cavity macrophages ([ 14 ][15]). It is highly likely that there is a reciprocal dialogue whereby cavity resident macrophages regulate stromal cell behavior. The high conservation between mouse and human scavenger receptors with SRCR domains ([ 15 ][16]) presents an exciting opportunity to inhibit these receptors as a potential therapeutic strategy to prevent adhesion formation. 1. [↵][17]1. K. Okabayashi et al ., Surg. Today 44, 405 (2014). [OpenUrl][18] 2. [↵][19]1. J. Zindel et al ., Science 371, eabe0595 (2021). [OpenUrl][20][Abstract/FREE Full Text][21] 3. [↵][22]1. G. B. Ryan, 2. J. Grobéty, 3. G. Majno , Am. J. Pathol. 65, 117 (1971). [OpenUrl][23][PubMed][24][Web of Science][25] 4. [↵][26]1. J. Tang, 2. Z. Xiang, 3. M. T. Bernards, 4. S. Chen , Acta Biomater. 116, 84 (2020). [OpenUrl][27] 5. [↵][28]1. D. S. Foster et al ., Nat. Commun. 11, 4061 (2020). [OpenUrl][29] 6. [↵][30]1. S. Namvar et al ., J. Pathol. 245, 491 (2018). [OpenUrl][31][CrossRef][32] 7. [↵][33]1. P. Sandoval et al ., J. Pathol. 239, 48 (2016). [OpenUrl][34] 8. [↵][35]1. J. M. Tsai et al ., Sci. Transl. Med. 10, eaan6735 (2018). [OpenUrl][36][Abstract/FREE Full Text][37] 9. [↵][38]1. C. C. Bain, 2. S. J. Jenkins , Cell. Immunol. 330, 126 (2018). [OpenUrl][39][PubMed][40] 10. [↵][41]1. E. L. Gautier et al ., J. Exp. Med. 211, 1525 (2014). [OpenUrl][42][Abstract/FREE Full Text][43] 11. [↵][44]1. M. Rosas et al ., Science 344, 645 (2014). [OpenUrl][45][Abstract/FREE Full Text][46] 12. [↵][47]1. J. Wang, 2. P. Kubes , Cell 165, 668 (2016). [OpenUrl][48][CrossRef][49][PubMed][50] 13. [↵][51]1. N. Zhang et al ., J. Exp. Med. 216, 1291 (2019). [OpenUrl][52][Abstract/FREE Full Text][53] 14. [↵][54]1. M. B. Buechler et al ., Immunity 51, 119 (2019). [OpenUrl][55][CrossRef][56] 15. [↵][57]1. D. M. E. Bowdish, 2. S. Gordon , Immunol. Rev. 227, 19 (2009). [OpenUrl][58][CrossRef][59][PubMed][60] [1]: #ref-1 [2]: #ref-2 [3]: #ref-3 [4]: #ref-4 [5]: #ref-5 [6]: #ref-6 [7]: #ref-7 [8]: #ref-8 [9]: #ref-9 [10]: #ref-10 [11]: #ref-11 [12]: #ref-12 [13]: #ref-13 [14]: pending:yes [15]: #ref-14 [16]: #ref-15 [17]: #xref-ref-1-1 "View reference 1 in text" [18]: {openurl}?query=rft.jtitle%253DSurg.%2BToday%26rft.volume%253D44%26rft.spage%253D405%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [19]: #xref-ref-2-1 "View reference 2 in text" [20]: {openurl}?query=rft.jtitle%253DScience%26rft.stitle%253DScience%26rft.aulast%253DZindel%26rft.auinit1%253DJ.%26rft.volume%253D371%26rft.issue%253D6533%26rft.spage%253Deabe0595%26rft.epage%253Deabe0595%26rft.atitle%253DPrimordial%2BGATA6%2Bmacrophages%2Bfunction%2Bas%2Bextravascular%2Bplatelets%2Bin%2Bsterile%2Binjury%26rft_id%253Dinfo%253Adoi%252F10.1126%252Fscience.abe0595%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [21]: /lookup/ijlink/YTozOntzOjQ6InBhdGgiO3M6MTQ6Ii9sb29rdXAvaWpsaW5rIjtzOjU6InF1ZXJ5IjthOjQ6e3M6ODoibGlua1R5cGUiO3M6NDoiQUJTVCI7czoxMToiam91cm5hbENvZGUiO3M6Mzoic2NpIjtzOjU6InJlc2lkIjtzOjE3OiIzNzEvNjUzMy9lYWJlMDU5NSI7czo0OiJhdG9tIjtzOjIyOiIvc2NpLzM3MS82NTMzLzk5My5hdG9tIjt9czo4OiJmcmFnbWVudCI7czowOiIiO30= [22]: #xref-ref-3-1 "View reference 3 in text" [23]: {openurl}?query=rft.jtitle%253DAmerican%2BJournal%2BOf%2BPathology%26rft.stitle%253DAm.%2BJ.%2BPathol.%26rft.aulast%253DRyan%26rft.auinit1%253DG.%26rft.volume%253D65%26rft.issue%253D1%26rft.spage%253D117%26rft.epage%253D148%26rft.atitle%253DPostoperative%2Bperitoneal%2Badhesions.%2BA%2Bstudy%2Bof%2Bthe%2Bmechanisms%26rft_id%253Dinfo%253Apmid%252F5315369%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [24]: /lookup/external-ref?access_num=5315369&link_type=MED&atom=%2Fsci%2F371%2F6533%2F993.atom [25]: /lookup/external-ref?access_num=A1971K624200008&link_type=ISI [26]: #xref-ref-4-1 "View reference 4 in text" [27]: 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{openurl}?query=rft.jtitle%253DJ.%2BPathol.%26rft.volume%253D245%26rft.spage%253D491%26rft_id%253Dinfo%253Adoi%252F10.1002%252Fpath.5101%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [32]: /lookup/external-ref?access_num=10.1002/path.5101&link_type=DOI [33]: #xref-ref-7-1 "View reference 7 in text" [34]: {openurl}?query=rft.jtitle%253DJ.%2BPathol.%26rft.volume%253D239%26rft.spage%253D48%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [35]: #xref-ref-8-1 "View reference 8 in text" [36]: {openurl}?query=rft.jtitle%253DScience%2BTranslational%2BMedicine%26rft.stitle%253DSci%2BTransl%2BMed%26rft.aulast%253DTsai%26rft.auinit1%253DJ.%2BM.%26rft.volume%253D10%26rft.issue%253D469%26rft.spage%253Deaan6735%26rft.epage%253Deaan6735%26rft.atitle%253DSurgical%2Badhesions%2Bin%2Bmice%2Bare%2Bderived%2Bfrom%2Bmesothelial%2Bcells%2Band%2Bcan%2Bbe%2Btargeted%2Bby%2Bantibodies%2Bagainst%2Bmesothelial%2Bmarkers%26rft_id%253Dinfo%253Adoi%252F10.1126%252Fscitranslmed.aan6735%26rft_id%253Dinfo%253Apmid%252F30487249%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [37]: 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{openurl}?query=rft.jtitle%253DJ.%2BExp.%2BMed.%26rft_id%253Dinfo%253Adoi%252F10.1084%252Fjem.20140570%26rft_id%253Dinfo%253Apmid%252F25024137%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [43]: /lookup/ijlink/YTozOntzOjQ6InBhdGgiO3M6MTQ6Ii9sb29rdXAvaWpsaW5rIjtzOjU6InF1ZXJ5IjthOjQ6e3M6ODoibGlua1R5cGUiO3M6NDoiQUJTVCI7czoxMToiam91cm5hbENvZGUiO3M6MzoiamVtIjtzOjU6InJlc2lkIjtzOjEwOiIyMTEvOC8xNTI1IjtzOjQ6ImF0b20iO3M6MjI6Ii9zY2kvMzcxLzY1MzMvOTkzLmF0b20iO31zOjg6ImZyYWdtZW50IjtzOjA6IiI7fQ== [44]: #xref-ref-11-1 "View reference 11 in text" [45]: 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领域	气候变化 ; 资源环境
URL	查看原文
引用统计	被引频次：7[WOS] [WOS记录] [WOS相关记录]
文献类型	期刊论文
条目标识符	http://119.78.100.173/C666/handle/2XK7JSWQ/316987
专题	气候变化资源环境科学
推荐引用方式 GB/T 7714	Sarah E. Herrick,Judith E. Allen. Surgical adhesions: A sticky macrophage problem[J]. Science,2021.
APA	Sarah E. Herrick,&Judith E. Allen.(2021).Surgical adhesions: A sticky macrophage problem.Science.
MLA	Sarah E. Herrick,et al."Surgical adhesions: A sticky macrophage problem".Science (2021).