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Brief Report

Tumors exploit CXCR4hiCD62Llo aged neutrophils to facilitate metastatic spread

, , , , , , , , , & ORCID Icon show all
Article: 1870811 | Received 25 Aug 2020, Accepted 28 Dec 2020, Published online: 20 Jan 2021

References

  • Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science. 2011;331(6024):1559–10. doi:10.1126/science.1203543.
  • Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420(6917):860–867. doi:10.1038/nature01322.
  • Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell. 2010;140(6):883–899. doi:10.1016/j.cell.2010.01.025.
  • Cortez-Retamozo V, Etzrodt M, Newton A, Rauch PJ, Chudnovskiy A, Berger C, Ryan RJH, Iwamoto Y, Marinelli B, Gorbatov R, et al. Origins of tumor-associated macrophages and neutrophils. Proc Natl Acad Sci U S A. 2012;109(7):2491–2496. doi:10.1073/pnas.1113744109.
  • Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008;454(7203):436–444. doi:10.1038/nature07205.
  • Templeton AJ, McNamara MG, Seruga B, Vera-Badillo FE, Aneja P, Ocana A, Leibowitz-Amit R, Sonpavde G, Knox JJ, Tran B, et al. Prognostic role of neutrophil-to-lymphocyte ratio in solid tumors: a systematic review and meta-analysis. J Natl Cancer Inst. 2014;106(6):dju124. doi:10.1093/jnci/dju124.
  • Kumar V, Patel S, Tcyganov E, Gabrilovich DI. The nature of myeloid-derived suppressor cells in the tumor microenvironment. Trends Immunol. 2016;37(3):208–220. doi:10.1016/j.it.2016.01.004.
  • Alshetaiwi H, Pervolarakis N, McIntyre LL, Ma D, Nguyen Q, Rath JA, Nee K, Hernandez G, Evans K, Torosian L, et al. Defining the emergence of myeloid-derived suppressor cells in breast cancer using single-cell transcriptomics. Sci Immunol. 2020;5(44):eaay6017. doi:10.1126/sciimmunol.aay6017.
  • Granot Z, Henke E, Comen EA, King TA, Norton L, Benezra R. Tumor entrained neutrophils inhibit seeding in the premetastatic lung. Cancer Cell. 2011;20(3):300–314. doi:10.1016/j.ccr.2011.08.012.
  • Lopez-Lago MA, Posner S, Thodima VJ, Molina AM, Motzer RJ, Chaganti RS. Neutrophil chemokines secreted by tumor cells mount a lung antimetastatic response during renal cell carcinoma progression. Oncogene. 2013;32(14):1752–1760. doi:10.1038/onc.2012.201.
  • Ng LG, Ostuni R, Hidalgo A. Heterogeneity of neutrophils. Nat Rev Immunol. 2019;19(4):255–265. doi:10.1038/s41577-019-0141-8.
  • Adrover JM, Del Fresno C, Crainiciuc G, Cuartero MI, Casanova-Acebes M, Weiss LA, Huerga-Encabo H, Silvestre-Roig C, Rossaint J, Cossío I, et al. A neutrophil timer coordinates immune defense and vascular protection. Immunity. 2019;50(2):390–402 e10. doi:10.1016/j.immuni.2019.01.002.
  • Casanova-Acebes M, Pitaval C, Weiss LA, Nombela-Arrieta C, Chevre R, AG N, Kunisaki Y, Zhang D, van Rooijen N, Silberstein L, et al. Rhythmic modulation of the hematopoietic niche through neutrophil clearance. Cell. 2013;153(5):1025–1035. doi:10.1016/j.cell.2013.04.040.
  • Uhl B, Vadlau Y, Zuchtriegel G, Nekolla K, Sharaf K, Gaertner F, Massberg S, Krombach F, Reichel CA. Aged neutrophils contribute to the first line of defense in the acute inflammatory response. Blood. 2016;128(19):2327–2337. doi:10.1182/blood-2016-05-718999.
  • Zhang D, Chen G, Manwani D, Mortha A, Xu C, Faith JJ, Burk RD, Kunisaki Y, Jang J-E, Scheiermann C, et al. Neutrophil ageing is regulated by the microbiome. Nature. 2015;525(7570):528–532. doi:10.1038/nature15367.
  • Zhang DC, Frenette PS. Cross talk between neutrophils and the microbiota. Blood. 2019;133(20):2168–2177. doi:10.1182/blood-2018-11-844555.
  • Spicer JD, McDonald B, Cools-Lartigue JJ, Chow SC, Giannias B, Kubes P, Ferri LE. Neutrophils promote liver metastasis via Mac-1-mediated interactions with circulating tumor cells. Cancer Res. 2012;72(16):3919–3927. doi:10.1158/0008-5472.CAN-11-2393.
  • Fidler IJ. Selection of successive tumour lines for metastasis. Nat New Biol. 1973;242(118):148–149. doi:10.1038/newbio242148a0.
  • Shen XZ, Li P, Weiss D, Fuchs S, Xiao HD, Adams JA, Williams IR, Capecchi MR, Taylor WR, Bernstein KE, et al. Mice with enhanced macrophage angiotensin-converting enzyme are resistant to melanoma. Am J Pathol. 2007;170(6):2122–2134. doi:10.2353/ajpath.2007.061205.
  • Evrard M, Kwok IWH, Chong SZ, Teng KWW, Becht E, Chen J, Sieow JL, Penny HL, Ching GC, Devi S, et al. Developmental analysis of bone marrow neutrophils reveals populations specialized in expansion, trafficking, and effector functions. Immunity. 2018;48(2):364–79 e8. doi:10.1016/j.immuni.2018.02.002.
  • Chow A, Lucas D, Hidalgo A, Mendez-Ferrer S, Hashimoto D, Scheiermann C, Battista M, Leboeuf M, Prophete C, van Rooijen N, et al. Bone marrow CD169+ macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J Exp Med. 2011;208(2):261–271. doi:10.1084/jem.20101688.
  • Albrengues J, Shields MA, Ng D, Park CG, Ambrico A, Poindexter ME, Upadhyay P, Uyeminami DL, Pommier A, Küttner V, et al. Neutrophil extracellular traps produced during inflammation awaken dormant cancer cells in mice. Science. 2018;361(6409):eaao4227. doi:10.1126/science.aao4227.
  • Cao DY, Spivia WR, Veiras LC, Khan Z, Peng Z, Jones AE, Bernstein EA, Saito S, Okwan-Duodu D, Parker SJ, et al. ACE overexpression in myeloid cells increases oxidative metabolism and cellular ATP. J Biol Chem. 2020;295(5):1369–1384. doi:10.1074/jbc.RA119.011244.
  • Bernstein KE, Koronyo Y, Salumbides BC, Sheyn J, Pelissier L, Lopes DH, Shah KH, Bernstein EA, Fuchs D-T, Yu JJY, et al. Angiotensin-converting enzyme overexpression in myelomonocytes prevents Alzheimer’s-like cognitive decline. J Clin Invest. 2014;124(3):1000–1012. doi:10.1172/JCI66541.
  • Coffelt SB, Wellenstein MD, de Visser KE. Neutrophils in cancer: neutral no more. Nat Rev Cancer. 2016;16(7):431–446. doi:10.1038/nrc.2016.52.
  • Kim JH, Podstawka J, Lou Y, Li L, Lee EKS, Divangahi M, Petri B, Jirik FR, Kelly MM, Yipp BG, et al. Aged polymorphonuclear leukocytes cause fibrotic interstitial lung disease in the absence of regulation by B cells. Nat Immunol. 2018;19(2):192–201. doi:10.1038/s41590-017-0030-x.
  • Mastio J, Condamine T, Dominguez G, Kossenkov AV, Donthireddy L, Veglia F, Lin C, Wang F, Fu S, Zhou J, et al. Identification of monocyte-like precursors of granulocytes in cancer as a mechanism for accumulation of PMN-MDSCs. J Exp Med. 2019;216(9):2150–2169. doi:10.1084/jem.20181952.
  • Youn JI, Gabrilovich DI. New roles of Rb1 in expansion of MDSCs in cancer. Cell Cycle. 2013;12(9):1329–1330. doi:10.4161/cc.24577.
  • Veglia F, Tyurin VA, Blasi M, De Leo A, Kossenkov AV, Donthireddy L, To TKJ, Schug Z, Basu S, Wang F, et al. Fatty acid transport protein 2 reprograms neutrophils in cancer. Nature. 2019;569(7754):73–78. doi:10.1038/s41586-019-1118-2.
  • Aarts CEM, Hiemstra IH, Beguin EP, Hoogendijk AJ, Bouchmal S, van Houdt M, Tool ATJ, Mul E, Jansen MH, Janssen H, et al. Activated neutrophils exert myeloid-derived suppressor cell activity damaging T cells beyond repair. Blood Adv. 2019;3(22):3562–3574. doi:10.1182/bloodadvances.2019031609.
  • Finisguerra V, Di Conza G, Di Matteo M, Serneels J, Costa S, Thompson AA, Wauters E, Walmsley S, Prenen H, Granot Z, et al. MET is required for the recruitment of anti-tumoural neutrophils. Nature. 2015;522(7556):349–353. doi:10.1038/nature14407.
  • Debnath B, Xu S, Grande F, Garofalo A, Neamati N. Small molecule inhibitors of CXCR4. Theranostics. 2013;3(1):47–75. doi:10.7150/thno.5376.
  • Cortez-Retamozo V, Etzrodt M, Newton A, Ryan R, Pucci F, Sio SW, Kuswanto W, Rauch P, Chudnovskiy A, Iwamoto Y, et al. Angiotensin II drives the production of tumor-promoting macrophages. Immunity. 2013;38(2):296–308. doi:10.1016/j.immuni.2012.10.015.
  • Casbon AJ, Reynaud D, Park C, Khuc E, Gan DD, Schepers K, Passegué E, Werb Z. Invasive breast cancer reprograms early myeloid differentiation in the bone marrow to generate immunosuppressive neutrophils. Proc Natl Acad Sci U S A. 2015;112(6):E566–75. doi:10.1073/pnas.1424927112.
  • Hong C, Kidani Y, Noelia A, Phung T, Ito A, Rong X, Ericson K, Mikkola H, Beaven SW, Miller LS, et al. Coordinate regulation of neutrophil homeostasis by liver X receptors in mice. J Clin Invest. 2012;122(1):337–347. doi:10.1172/JCI58393.
  • Cai B, Kasikara C, Doran AC, Ramakrishnan R, Birge RB, Tabas I. MerTK signaling in macrophages promotes the synthesis of inflammation resolution mediators by suppressing CaMKII activity. Sci Signal. 2018;11(549):eaar3721. doi:10.1126/scisignal.aar3721.
  • Thorp E, Vaisar T, Subramanian M, Mautner L, Blobel C, Tabas I. Shedding of the Mer tyrosine kinase receptor is mediated by ADAM17 protein through a pathway involving reactive oxygen species, protein kinase Cdelta, and p38 mitogen-activated protein kinase (MAPK). J Biol Chem. 2011;286(38):33335–33344. doi:10.1074/jbc.M111.263020.
  • Gavard J, Gutkind JS. VE-cadherin and claudin-5: it takes two to tango. Nat Cell Biol. 2008;10(8):883–885. doi:10.1038/ncb0808-883.
  • Tohme S, Yazdani HO, Al-Khafaji AB, Chidi AP, Loughran P, Mowen K, Wang Y, Simmons RL, Huang H, Tsung A, et al. Neutrophil extracellular traps promote the development and progression of liver metastases after surgical stress. Cancer Res. 2016;76(6):1367–1380. doi:10.1158/0008-5472.CAN-15-1591.
  • Rayes RF, Mouhanna JG, Nicolau I, Bourdeau F, Giannias B, Rousseau S, Quail D, Walsh L, Sangwan V, Bertos N, et al. Primary tumors induce neutrophil extracellular traps with targetable metastasis promoting effects. JCI Insight. 2019;5. doi:10.1172/jci.insight.128008
  • Teijeira A, Garasa S, Gato M, Alfaro C, Migueliz I, Cirella A, de Andrea C, Ochoa MC, Otano I, Etxeberria I, et al. CXCR1 and CXCR2 chemokine receptor agonists produced by tumors induce neutrophil extracellular traps that interfere with immune cytotoxicity. Immunity. 2020;52(5):856–71 e8. doi:10.1016/j.immuni.2020.03.001.
  • Fridlender ZG, Albelda SM. Tumor-associated neutrophils: friend or foe? Carcinogenesis. 2012;33(5):949–955. doi:10.1093/carcin/bgs123.
  • Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, Worthen GS, Albelda SM. Polarization of tumor-associated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN. Cancer Cell. 2009;16(3):183–194. doi:10.1016/j.ccr.2009.06.017.
  • Millrud CR, Kagedal A, Kumlien Georen S, Winqvist O, Uddman R, Razavi R, Munck-Wikland E, Cardell LO. NET-producing CD16 high CD62L dim neutrophils migrate to tumor sites and predict improved survival in patients with HNSCC. Int J Cancer. 2017;140(11):2557–2567. doi:10.1002/ijc.30671.