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01-08-2021 | Metastasis | Review Paper

The role of redox system in metastasis formation

Authors: Chiara Cencioni, Valentina Comunanza, Emanuele Middonti, Edoardo Vallariello, Federico Bussolino

Published in: Angiogenesis | Issue 3/2021

Abstract

The metastatic cancer disease represents the real and urgent clinical need in oncology. Therefore, an understanding of the complex molecular mechanisms sustaining the metastatic cascade is critical to advance cancer therapies. Recent studies highlight how redox signaling influences the behavior of metastatic cancer cells, contributes to their travel in bloodstream from the primary tumor to the distant organs and conditions the progression of the micrometastases or their dormant state. Radical oxygen species not only regulate intracellular processes but participate to paracrine circuits by diffusion to nearby cells, thus assuming unpredicted roles in the communication between metastatic cancer cells, blood circulating cells, and stroma cells at site of colonization. Here, we review recent insights in the role of radical oxygen species in the metastasis formation with a special focus on extravasation at metastatic sites.

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Lambert AW, Pattabiraman DR, Weinberg RA (2017) Emerging biological principles of metastasis. Cell 168(4):670–691. https://doi.org/10.1016/j.cell.2016.11.037PubMedPubMedCentralCrossRef

Mariotto AB, Etzioni R, Hurlbert M, Penberthy L, Mayer M (2017) Estimation of the number of women living with metastatic breast cancer in the United States. Cancer Epidemiol Biomarkers Prev 26(6):809–815. https://doi.org/10.1158/1055-9965.EPI-16-0889PubMedPubMedCentralCrossRef

Wang D, Sun H, Wei J, Cen B, DuBois RN (2017) CXCL1 is critical for premetastatic niche formation and metastasis in colorectal cancer. Cancer Res 77(13):3655–3665. https://doi.org/10.1158/0008-5472.CAN-16-3199PubMedPubMedCentralCrossRef

Fang JH, Zhang ZJ, Shang LR, Luo YW, Lin YF, Yuan Y, Zhuang SM (2018) Hepatoma cell-secreted exosomal microRNA-103 increases vascular permeability and promotes metastasis by targeting junction proteins. Hepatology 68(4):1459–1475. https://doi.org/10.1002/hep.29920PubMedCrossRef

Headley MB, Bins A, Nip A, Roberts EW, Looney MR, Gerard A, Krummel MF (2016) Visualization of immediate immune responses to pioneer metastatic cells in the lung. Nature 531(7595):513–517. https://doi.org/10.1038/nature16985PubMedPubMedCentralCrossRef

Celià-Terrassa T, Kang Y (2018) Metastatic niche functions and therapeutic opportunities. Nat Cell Biol 20(8):868–877. https://doi.org/10.1038/s41556-018-0145-9PubMedCrossRef

Massagué J, Obenauf AC (2016) Metastatic colonization by circulating tumour cells. Nature 529(7586):298–306. https://doi.org/10.1038/nature17038PubMedPubMedCentralCrossRef

Labelle M, Hynes RO (2012) The initial hours of metastasis: the importance of cooperative host-tumor cell interactions during hematogenous dissemination. Cancer Discov 2(12):1091–1099. https://doi.org/10.1158/2159-8290.CD-12-0329PubMedPubMedCentralCrossRef

Sies H, Berndt C, Jones DP (2017) Oxidative stress. Annu Rev Biochem 86:715–748. https://doi.org/10.1146/annurev-biochem-061516-045037PubMedCrossRef

10.

Cheung EC, DeNicola GM, Nixon C, Blyth K, Labuschagne CF, Tuveson DA, Vousden KH (2020) Dynamic ROS control by TIGAR regulates the initiation and progression of pancreatic cancer. Cancer Cell 37(2):168–182. https://doi.org/10.1016/j.ccell.2019.12.012PubMedPubMedCentralCrossRef

11.

Bodega G, Alique M, Puebla L, Carracedo J, Ramírez RM (2019) Microvesicles: ROS scavengers and ROS producers. J Extracell Vesicles 8(1):1626654. https://doi.org/10.1080/20013078.2019.1626654PubMedPubMedCentralCrossRef

12.

Dastmalchi N, Baradaran B, Latifi-Navid S, Safaralizadeh R, Khojasteh SMB, Amini M, Roshani E, Lotfinejad P (2020) Antioxidants with two faces toward cancer. Life Sci 258:118186. https://doi.org/10.1016/j.lfs.2020.118186PubMedCrossRef

13.

Zeng Z, Wang ZY, Li YK, Ye DM, Zeng J, Hu JL, Chen PF, Xiao J, Zou J, Li ZH (2020) Nuclear factor erythroid 2 (NF-E2)-related factor 2 (Nrf2) in non-small cell lung cancer. Life Sci 254:117325. https://doi.org/10.1016/j.lfs.2020.117325PubMedCrossRef

14.

Nieto MA, Huang RY, Jackson RA, Thiery JP (2016) EMT: 2016. Cell 166(1):21–45. https://doi.org/10.1016/j.cell.2016.06.028PubMedCrossRef

15.

Piskounova E, Agathocleous M, Murphy MM, Hu Z, Huddlestun SE, Zhao Z, Leitch AM, Johnson TM, DeBerardinis RJ, Morrison SJ (2015) Oxidative stress inhibits distant metastasis by human melanoma cells. Nature 527(7577):186–191. https://doi.org/10.1038/nature15726PubMedPubMedCentralCrossRef

16.

Kudo Y, Sugimoto M, Arias E, Kasashima H, Cordes T, Linares JF, Duran A, Nakanishi Y, Nakanishi N, L’Hermitte A, Campos A, Senni N, Rooslid T, Roberts LR, Cuervo AM, Metallo CM, Karin M, Diaz-Meco MT, Moscat J (2020) PKClambda/iota loss induces autophagy, oxidative phosphorylation, and NRF2 to promote liver cancer progression. Cancer Cell. https://doi.org/10.1016/j.ccell.2020.05.018PubMedCrossRefPubMedCentral

17.

Batlle E, Massagué J (2019) Transforming growth factor-β signaling in immunity and cancer. Immunity 50(4):924–940. https://doi.org/10.1016/j.immuni.2019.03.024PubMedPubMedCentralCrossRef

18.

Bastakoty D, Young PP (2016) Wnt/β-catenin pathway in tissue injury: roles in pathology and therapeutic opportunities for regeneration. FASEB J 30(10):3271–3284. https://doi.org/10.1096/fj.201600502RPubMedPubMedCentralCrossRef

19.

Kajla S, Mondol AS, Nagasawa A, Zhang Y, Kato M, Matsuno K, Yabe-Nishimura C, Kamata T (2012) A crucial role for Nox 1 in redox-dependent regulation of Wnt-β-catenin signaling. FASEB J 26(5):2049–2059. https://doi.org/10.1096/fj.11-196360PubMedCrossRef

20.

Zhou T, Zhou KK, Lee K, Gao G, Lyons TJ, Kowluru R, Ma JX (2011) The role of lipid peroxidation products and oxidative stress in activation of the canonical wingless-type MMTV integration site (WNT) pathway in a rat model of diabetic retinopathy. Diabetologia 54(2):459–468. https://doi.org/10.1007/s00125-010-1943-1PubMedCrossRef

21.

Ishimoto T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, Oshima M, Ikeda T, Asaba R, Yagi H, Masuko T, Shimizu T, Ishikawa T, Kai K, Takahashi E, Imamura Y, Baba Y, Ohmura M, Suematsu M, Baba H, Saya H (2011) CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell 19(3):387–400. https://doi.org/10.1016/j.ccr.2011.01.038PubMedCrossRef

22.

Kipp AP, Deubel S, Arnér ESJ, Johansson K (2017) Time- and cell-resolved dynamics of redox-sensitive Nrf2, HIF and NF-κB activities in 3D spheroids enriched for cancer stem cells. Redox Biol 12:403–409. https://doi.org/10.1016/j.redox.2017.03.013PubMedPubMedCentralCrossRef

23.

Kim D, Choi BH, Ryoo IG, Kwak MK (2018) High NRF2 level mediates cancer stem cell-like properties of aldehyde dehydrogenase (ALDH)-high ovarian cancer cells: inhibitory role of all-trans retinoic acid in ALDH/NRF2 signaling. Cell Death Dis 9(9):896. https://doi.org/10.1038/s41419-018-0903-4PubMedPubMedCentralCrossRef

24.

Bellot G, Garcia-Medina R, Gounon P, Chiche J, Roux D, Pouysségur J, Mazure NM (2009) Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol Cell Biol 29(10):2570–2581. https://doi.org/10.1128/MCB.00166-09PubMedPubMedCentralCrossRef

25.

Chan SY, Zhang YY, Hemann C, Mahoney CE, Zweier JL, Loscalzo J (2009) MicroRNA-210 controls mitochondrial metabolism during hypoxia by repressing the iron-sulfur cluster assembly proteins ISCU1/2. Cell Metab 10(4):273–284. https://doi.org/10.1016/j.cmet.2009.08.015PubMedPubMedCentralCrossRef

26.

Samanta D, Park Y, Andrabi SA, Shelton LM, Gilkes DM, Semenza GL (2016) PHGDH expression is required for mitochondrial redox homeostasis, breast cancer stem cell maintenance, and lung metastasis. Cancer Res 76(15):4430–4442. https://doi.org/10.1158/0008-5472.CAN-16-0530PubMedCrossRef

27.

Sporn MB, Liby KT (2012) NRF2 and cancer: the good, the bad and the importance of context. Nat Rev Cancer 12(8):564–571. https://doi.org/10.1038/nrc3278PubMedCrossRef

28.

Chang CW, Chen YS, Tsay YG, Han CL, Chen YJ, Yang CC, Hung KF, Lin CH, Huang TY, Kao SY, Lee TC, Lo JF (2018) ROS-independent ER stress-mediated NRF2 activation promotes warburg effect to maintain stemness-associated properties of cancer-initiating cells. Cell Death Dis 9(2):194. https://doi.org/10.1038/s41419-017-0250-xPubMedPubMedCentralCrossRef

29.

Panieri E, Santoro MM (2015) ROS signaling and redox biology in endothelial cells. Cell Mol Life Sci 72(17):3281–3303. https://doi.org/10.1007/s00018-015-1928-9PubMedCrossRef

30.

Sena CM, Leandro A, Azul L, Seiça R, Perry G (2018) Vascular oxidative stress: impact and therapeutic approaches. Front Physiol 9:1668. https://doi.org/10.3389/fphys.2018.01668PubMedPubMedCentralCrossRef

31.

Karuppiah K, Druhan LJ, Chen CA, Smith T, Zweier JL, Sessa WC, Cardounel AJ (2011) Suppression of eNOS-derived superoxide by caveolin-1: a biopterin-dependent mechanism. Am J Physiol Heart Circ Physiol 301(3):H903-911. https://doi.org/10.1152/ajpheart.00936.2010PubMedPubMedCentralCrossRef

32.

Mistry RK, Brewer AC (2017) Redox regulation of gasotransmission in the vascular system: a focus on angiogenesis. Free Radic Biol Med 108:500–516. https://doi.org/10.1016/j.freeradbiomed.2017.04.025PubMedPubMedCentralCrossRef

33.

Potente M, Carmeliet P (2017) The link between angiogenesis and endothelial metabolism. Annu Rev Physiol 79:43–66. https://doi.org/10.1146/annurev-physiol-021115-105134PubMedCrossRef

34.

De Bock K, Georgiadou M, Schoors S, Kuchnio A, Wong BW, Cantelmo AR, Quaegebeur A, Ghesquière B, Cauwenberghs S, Eelen G, Phng LK, Betz I, Tembuyser B, Brepoels K, Welti J, Geudens I, Segura I, Cruys B, Bifari F, Decimo I, Blanco R, Wyns S, Vangindertael J, Rocha S, Collins RT, Munck S, Daelemans D, Imamura H, Devlieger R, Rider M, Van Veldhoven PP, Schuit F, Bartrons R, Hofkens J, Fraisl P, Telang S, Deberardinis RJ, Schoonjans L, Vinckier S, Chesney J, Gerhardt H, Dewerchin M, Carmeliet P (2013) Role of PFKFB3-driven glycolysis in vessel sprouting. Cell 154(3):651–663. https://doi.org/10.1016/j.cell.2013.06.037PubMedCrossRef

35.

Yetkin-Arik B, Vogels IMC, Nowak-Sliwinska P, Weiss A, Houtkooper RH, Van Noorden CJF, Klaassen I, Schlingemann RO (2019) The role of glycolysis and mitochondrial respiration in the formation and functioning of endothelial tip cells during angiogenesis. Sci Rep 9(1):12608. https://doi.org/10.1038/s41598-019-48676-2PubMedPubMedCentralCrossRef

36.

Kalucka J, Bierhansl L, Conchinha NV, Missiaen R, Elia I, Brüning U, Scheinok S, Treps L, Cantelmo AR, Dubois C, de Zeeuw P, Goveia J, Zecchin A, Taverna F, Morales-Rodriguez F, Brajic A, Conradi LC, Schoors S, Harjes U, Vriens K, Pilz GA, Chen R, Cubbon R, Thienpont B, Cruys B, Wong BW, Ghesquière B, Dewerchin M, De Bock K, Sagaert X, Jessberger S, Jones EAV, Gallez B, Lambrechts D, Mazzone M, Eelen G, Li X, Fendt SM, Carmeliet P (2018) Quiescent endothelial cells upregulate fatty acid β-oxidation for vasculoprotection via redox homeostasis. Cell Metab 28(6):881-894.e813. https://doi.org/10.1016/j.cmet.2018.07.016PubMedCrossRef

37.

Kienast Y, von Baumgarten L, Fuhrmann M, Klinkert WE, Goldbrunner R, Herms J, Winkler F (2010) Real-time imaging reveals the single steps of brain metastasis formation. Nat Med 16(1):116–122. https://doi.org/10.1038/nm.2072PubMedCrossRef

38.

Hordijk PL (2016) Recent insights into endothelial control of leukocyte extravasation. Cell Mol Life Sci 73(8):1591–1608. https://doi.org/10.1007/s00018-016-2136-yPubMedCrossRef

39.

Osmani N, Follain G, García León MJ, Lefebvre O, Busnelli I, Larnicol A, Harlepp S, Goetz JG (2019) Metastatic tumor cells exploit their adhesion repertoire to counteract shear forces during intravascular arrest. Cell Rep 28(10):2491-2500.e2495. https://doi.org/10.1016/j.celrep.2019.07.102PubMedCrossRef

40.

Reymond N, d’Água BB, Ridley AJ (2013) Crossing the endothelial barrier during metastasis. Nat Rev Cancer 13(12):858–870. https://doi.org/10.1038/nrc3628PubMedCrossRef

41.

Shea DJ, Li YW, Stebe KJ, Konstantopoulos K (2017) E-selectin-mediated rolling facilitates pancreatic cancer cell adhesion to hyaluronic acid. FASEB J 31(11):5078–5086. https://doi.org/10.1096/fj.201700331RPubMedPubMedCentralCrossRef

42.

Deem TL, Cook-Mills JM (2004) Vascular cell adhesion molecule 1 (VCAM-1) activation of endothelial cell matrix metalloproteinases: role of reactive oxygen species. Blood 104(8):2385–2393. https://doi.org/10.1182/blood-2004-02-0665PubMedCrossRef

43.

Winterbourn CC, Kettle AJ, Hampton MB (2016) Reactive oxygen species and neutrophil function. Annu Rev Biochem 85:765–792. https://doi.org/10.1146/annurev-biochem-060815-014442PubMedCrossRef

44.

Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A (2004) Neutrophil extracellular traps kill bacteria. Science 303(5663):1532–1535. https://doi.org/10.1126/science.1092385PubMedCrossRef

45.

Björnsdottir H, Welin A, Michaëlsson E, Osla V, Berg S, Christenson K, Sundqvist M, Dahlgren C, Karlsson A, Bylund J (2015) Neutrophil NET formation is regulated from the inside by myeloperoxidase-processed reactive oxygen species. Free Radic Biol Med 89:1024–1035. https://doi.org/10.1016/j.freeradbiomed.2015.10.398PubMedCrossRef

46.

Begonja AJ, Gambaryan S, Geiger J, Aktas B, Pozgajova M, Nieswandt B, Walter U (2005) Platelet NAD(P)H-oxidase-generated ROS production regulates alphaIIbbeta3-integrin activation independent of the NO/cGMP pathway. Blood 106(8):2757–2760. https://doi.org/10.1182/blood-2005-03-1047PubMedCrossRef

47.

Kim K, Li J, Tseng A, Andrews RK, Cho J (2015) NOX2 is critical for heterotypic neutrophil-platelet interactions during vascular inflammation. Blood 126(16):1952–1964. https://doi.org/10.1182/blood-2014-10-605261PubMedPubMedCentralCrossRef

48.

Li J, Kim K, Jeong SY, Chiu J, Xiong B, Petukhov PA, Dai X, Li X, Andrews RK, Du X, Hogg PJ, Cho J (2019) Platelet protein disulfide isomerase promotes glycoprotein Ibα-mediated platelet-neutrophil interactions under thromboinflammatory conditions. Circulation 139(10):1300–1319. https://doi.org/10.1161/CIRCULATIONAHA.118.036323PubMedPubMedCentralCrossRef

49.

Arthur JF, Shen Y, Gardiner EE, Coleman L, Murphy D, Kenny D, Andrews RK, Berndt MC (2011) TNF receptor-associated factor 4 (TRAF4) is a novel binding partner of glycoprotein Ib and glycoprotein VI in human platelets. J Thromb Haemost 9(1):163–172. https://doi.org/10.1111/j.1538-7836.2010.04091.xPubMedCrossRef

50.

Senis YA, Mazharian A, Mori J (2014) Src family kinases: at the forefront of platelet activation. Blood 124(13):2013–2024. https://doi.org/10.1182/blood-2014-01-453134PubMedPubMedCentralCrossRef

51.

Jang JY, Wang SB, Min JH, Chae YH, Baek JY, Yu DY, Chang TS (2015) Peroxiredoxin II is an antioxidant enzyme that negatively regulates collagen-stimulated platelet function. J Biol Chem 290(18):11432–11442. https://doi.org/10.1074/jbc.M115.644260PubMedPubMedCentralCrossRef

52.

Clutton P, Miermont A, Freedman JE (2004) Regulation of endogenous reactive oxygen species in platelets can reverse aggregation. Arterioscler Thromb Vasc Biol 24(1):187–192. https://doi.org/10.1161/01.ATV.0000105889.29687.CCPubMedCrossRef

53.

Saini M, Szczerba BM, Aceto N (2019) Circulating tumor cell-neutrophil tango along the metastatic process. Cancer Res. https://doi.org/10.1158/0008-5472.CAN-19-1972PubMedPubMedCentralCrossRef

54.

Coffelt SB, Wellenstein MD, de Visser KE (2016) Neutrophils in cancer: neutral no more. Nat Rev Cancer 16(7):431–446. https://doi.org/10.1038/nrc.2016.52PubMedCrossRef

55.

Szczerba BM, Castro-Giner F, Vetter M, Krol I, Gkountela S, Landin J, Scheidmann MC, Donato C, Scherrer R, Singer J, Beisel C, Kurzeder C, Heinzelmann-Schwarz V, Rochlitz C, Weber WP, Beerenwinkel N, Aceto N (2019) Neutrophils escort circulating tumour cells to enable cell cycle progression. Nature 566(7745):553–557. https://doi.org/10.1038/s41586-019-0915-yPubMedCrossRef

56.

Verbon EH, Post JA, Boonstra J (2012) The influence of reactive oxygen species on cell cycle progression in mammalian cells. Gene 511(1):1–6. https://doi.org/10.1016/j.gene.2012.08.038PubMedCrossRef

57.

Han Y, Ishibashi S, Iglesias-Gonzalez J, Chen Y, Love NR, Amaya E (2018) Ca 2+ -induced mitochondrial ROS regulate the early embryonic cell cycle. Cell Rep 22(1):218–231. https://doi.org/10.1016/j.celrep.2017.12.042PubMedPubMedCentralCrossRef

58.

Mollinedo F, Janssen H, de la Iglesia-Vicente J, Villa-Pulgarin JA, Calafat J (2010) Selective fusion of azurophilic granules with Leishmania-containing phagosomes in human neutrophils. J Biol Chem 285(45):34528–34536. https://doi.org/10.1074/jbc.M110.125302PubMedPubMedCentralCrossRef

59.

Sprouse ML, Welte T, Boral D, Liu HN, Yin W, Vishnoi M, Goswami-Sewell D, Li L, Pei G, Jia P, Glitza-Oliva IC, Marchetti D (2019) PMN-MDSCs enhance CTC metastatic properties through reciprocal interactions via ROS/Notch/nodal signaling. Int J Mol Sci 20:1916. https://doi.org/10.3390/ijms20081916PubMedCentralCrossRef

60.

Schlesinger M (2018) Role of platelets and platelet receptors in cancer metastasis. J Hematol Oncol 11(1):125. https://doi.org/10.1186/s13045-018-0669-2PubMedPubMedCentralCrossRef

61.

Cho MS, Noh K, Haemmerle M, Li D, Park H, Hu Q, Hisamatsu T, Mitamura T, Mak SLC, Kunapuli S, Ma Q, Sood AK, Afshar-Kharghan V (2017) Role of ADP receptors on platelets in the growth of ovarian cancer. Blood 130(10):1235–1242. https://doi.org/10.1182/blood-2017-02-769893PubMedPubMedCentralCrossRef

62.

Placke T, Örgel M, Schaller M, Jung G, Rammensee HG, Kopp HG, Salih HR (2012) Platelet-derived MHC class I confers a pseudonormal phenotype to cancer cells that subverts the antitumor reactivity of natural killer immune cells. Cancer Res 72(2):440–448. https://doi.org/10.1158/0008-5472.CAN-11-1872PubMedCrossRef

63.

Takemoto A, Okitaka M, Takagi S, Takami M, Sato S, Nishio M, Okumura S, Fujita N (2017) A critical role of platelet TGF-β release in podoplanin-mediated tumour invasion and metastasis. Sci Rep 7:42186. https://doi.org/10.1038/srep42186PubMedPubMedCentralCrossRef

64.

Zhang JL, Liu Y, Yang H, Zhang HQ, Tian XX, Fang WG (2017) ATP-P2Y2-β-catenin axis promotes cell invasion in breast cancer cells. Cancer Sci 108(7):1318–1327. https://doi.org/10.1111/cas.13273PubMedPubMedCentralCrossRef

65.

San Juan BP, Garcia-Leon MJ, Rangel L, Goetz JG, Chaffer CL (2019) The complexities of metastasis. Cancers (Basel) 11:1575. https://doi.org/10.3390/cancers11101575CrossRef

66.

Aragon-Sanabria V, Pohler SE, Eswar VJ, Bierowski M, Gomez EW, Dong C (2017) VE-cadherin disassembly and cell contractility in the endothelium are necessary for barrier disruption induced by tumor cells. Sci Rep 7:45835. https://doi.org/10.1038/srep45835PubMedPubMedCentralCrossRef

67.

Roh-Johnson M, Bravo-Cordero JJ, Patsialou A, Sharma VP, Guo P, Liu H, Hodgson L, Condeelis J (2014) Macrophage contact induces RhoA GTPase signaling to trigger tumor cell intravasation. Oncogene 33(33):4203–4212. https://doi.org/10.1038/onc.2013.377PubMedCrossRef

68.

Gianni D, Diaz B, Taulet N, Fowler B, Courtneidge SA, Bokoch GM (2009) Novel p47(phox)-related organizers regulate localized NADPH oxidase 1 (Nox1) activity. Sci Signal 88:ra54. https://doi.org/10.1126/scisignal.2000370CrossRef

69.

Al-Mehdi AB, Tozawa K, Fisher AB, Shientag L, Lee A, Muschel RJ (2000) Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis. Nat Med 6(1):100–102. https://doi.org/10.1038/71429PubMedCrossRef

70.

Yang L, Joseph S, Sun T, Hoffmann J, Thevissen S, Offermanns S, Strilic B (2019) TAK1 regulates endothelial cell necroptosis and tumor metastasis. Cell Death Differ 26(10):1987–1997. https://doi.org/10.1038/s41418-018-0271-8PubMedPubMedCentralCrossRef

71.

Ajibade AA, Wang Q, Cui J, Zou J, Xia X, Wang M, Tong Y, Hui W, Liu D, Su B, Wang HY, Wang RF (2012) TAK1 negatively regulates NF-κB and p38 MAP kinase activation in Gr-1+CD11b+ neutrophils. Immunity 36(1):43–54. https://doi.org/10.1016/j.immuni.2011.12.010PubMedPubMedCentralCrossRef

72.

Kajino-Sakamoto R, Omori E, Nighot PK, Blikslager AT, Matsumoto K, Ninomiya-Tsuji J (2010) TGF-beta-activated kinase 1 signaling maintains intestinal integrity by preventing accumulation of reactive oxygen species in the intestinal epithelium. J Immunol 185(8):4729–4737. https://doi.org/10.4049/jimmunol.0903587PubMedCrossRef

73.

Huh SJ, Liang S, Sharma A, Dong C, Robertson GP (2010) Transiently entrapped circulating tumor cells interact with neutrophils to facilitate lung metastasis development. Cancer Res 70(14):6071–6082. https://doi.org/10.1158/0008-5472.CAN-09-4442PubMedPubMedCentralCrossRef

74.

Inoue M, Nakashima R, Enomoto M, Koike Y, Zhao X, Yip K, Huang SH, Waldron JN, Ikura M, Liu FF, Bratman SV (2018) Plasma redox imbalance caused by albumin oxidation promotes lung-predominant NETosis and pulmonary cancer metastasis. Nat Commun 9(1):5116. https://doi.org/10.1038/s41467-018-07550-xPubMedPubMedCentralCrossRef

75.

Zhang N, Zhang WJ, Cai HQ, Liu HL, Peng L, Li CH, Ye LY, Xu SQ, Yang ZH, Lou JN (2011) Platelet adhesion and fusion to endothelial cell facilitate the metastasis of tumor cell in hypoxia-reoxygenation condition. Clin Exp Metastasis 28(1):1–12. https://doi.org/10.1007/s10585-010-9353-9PubMedCrossRef

76.

Ward Y, Lake R, Faraji F, Sperger J, Martin P, Gilliard C, Ku KP, Rodems T, Niles D, Tillman H, Yin J, Hunter K, Sowalsky AG, Lang J, Kelly K (2018) Platelets promote metastasis via binding tumor CD97 leading to bidirectional signaling that coordinates transendothelial migration. Cell Rep 23(3):808–822. https://doi.org/10.1016/j.celrep.2018.03.092PubMedPubMedCentralCrossRef

77.

Labelle M, Begum S, Hynes RO (2014) Platelets guide the formation of early metastatic niches. Proc Natl Acad Sci USA 111(30):E3053-3061. https://doi.org/10.1073/pnas.1411082111PubMedPubMedCentralCrossRef

78.

Engblom C, Pfirschke C, Zilionis R, Da Silva Martins J, Bos SA, Courties G, Rickelt S, Severe N, Baryawno N, Faget J, Savova V, Zemmour D, Kline J, Siwicki M, Garris C, Pucci F, Liao HW, Lin YJ, Newton A, Yaghi OK, Iwamoto Y, Tricot B, Wojtkiewicz GR, Nahrendorf M, Cortez-Retamozo V, Meylan E, Hynes RO, Demay M, Klein A, Bredella MA, Scadden DT, Weissleder R, Pittet MJ (2017) Osteoblasts remotely supply lung tumors with cancer-promoting SiglecF. Science 358:eaal5081. https://doi.org/10.1126/science.aal5081PubMedPubMedCentralCrossRef

79.

Orino K, Lehman L, Tsuji Y, Ayaki H, Torti SV, Torti FM (2001) Ferritin and the response to oxidative stress. Biochem J 357(Pt 1):241–247. https://doi.org/10.1042/0264-6021:3570241PubMedPubMedCentralCrossRef

80.

Lee W, Ko SY, Mohamed MS, Kenny HA, Lengyel E, Naora H (2019) Neutrophils facilitate ovarian cancer premetastatic niche formation in the omentum. J Exp Med 216(1):176–194. https://doi.org/10.1084/jem.20181170PubMedPubMedCentralCrossRef

81.

Albrengues J, Shields MA, Ng D, Park CG, Ambrico A, Poindexter ME, Upadhyay P, Uyeminami DL, Pommier A, Küttner V, Bružas E, Maiorino L, Bautista C, Carmona EM, Gimotty PA, Fearon DT, Chang K, Lyons SK, Pinkerton KE, Trotman LC, Goldberg MS, Yeh JT, Egeblad M (2018) Neutrophil extracellular traps produced during inflammation awaken dormant cancer cells in mice. Science 361:eaao4227. https://doi.org/10.1126/science.aao4227PubMedPubMedCentralCrossRef

82.

Mensurado S, Rei M, Lança T, Ioannou M, Gonçalves-Sousa N, Kubo H, Malissen M, Papayannopoulos V, Serre K, Silva-Santos B (2018) Tumor-associated neutrophils suppress pro-tumoral IL-17+ γδ T cells through induction of oxidative stress. PLoS Biol 16(5):e2004990. https://doi.org/10.1371/journal.pbio.2004990PubMedPubMedCentralCrossRef

83.

Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, Oh EY, Gaber MW, Finklestein D, Allen M, Frank A, Bayazitov IT, Zakharenko SS, Gajjar A, Davidoff A, Gilbertson RJ (2007) A perivascular niche for brain tumor stem cells. Cancer Cell 11(1):69–82PubMedCrossRef

84.

Huang YJ, Nan GX (2019) Oxidative stress-induced angiogenesis. J Clin Neurosci 63:13–16. https://doi.org/10.1016/j.jocn.2019.02.019PubMedCrossRef

85.

Kim YM, Kim SJ, Tatsunami R, Yamamura H, Fukai T, Ushio-Fukai M (2017) ROS-induced ROS release orchestrated by Nox4, Nox2, and mitochondria in VEGF signaling and angiogenesis. Am J Physiol Cell Physiol 312(6):C749–C764. https://doi.org/10.1152/ajpcell.00346.2016PubMedPubMedCentralCrossRef

86.

West XZ, Malinin NL, Merkulova AA, Tischenko M, Kerr BA, Borden EC, Podrez EA, Salomon RG, Byzova TV (2010) Oxidative stress induces angiogenesis by activating TLR2 with novel endogenous ligands. Nature 467(7318):972–976. https://doi.org/10.1038/nature09421PubMedPubMedCentralCrossRef

87.

Shimizu K, Iyoda T, Okada M, Yamasaki S, Fujii SI (2018) Immune suppression and reversal of the suppressive tumor microenvironment. Int Immunol 30(10):445–454. https://doi.org/10.1093/intimm/dxy042PubMedCrossRef

88.

Corzo A, Cotter M, Cheng P, Cheng F, Kusmartsev S, Sotomayor E, Padhya T, McCaffrey T, McCaffrey J, Gabrilovich D (2009) Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J Immunol 182:5693–5701PubMedCrossRef

89.

Nagaraj S, Gupta K, Pisarev V, Kinarsky L, Sherman S, Kang L, Herber DL, Schneck J, Gabrilovich DI (2007) Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat Med 13(7):828–835. https://doi.org/10.1038/nm1609PubMedPubMedCentralCrossRef

90.

Kraaij MD, Savage ND, van der Kooij SW, Koekkoek K, Wang J, van den Berg JM, Ottenhoff TH, Kuijpers TW, Holmdahl R, van Kooten C, Gelderman KA (2010) Induction of regulatory T cells by macrophages is dependent on production of reactive oxygen species. Proc Natl Acad Sci USA 107(41):17686–17691. https://doi.org/10.1073/pnas.1012016107PubMedPubMedCentralCrossRef

91.

van de Geer A, Cuadrado E, Slot MC, van Bruggen R, Amsen D, Kuijpers TW (2019) Regulatory T cell features in chronic granulomatous disease. Clin Exp Immunol 197(2):222–229. https://doi.org/10.1111/cei.13300PubMedPubMedCentralCrossRef

92.

Wen Z, Shimojima Y, Shirai T, Li Y, Ju J, Yang Z, Tian L, Goronzy JJ, Weyand CM (2016) NADPH oxidase deficiency underlies dysfunction of aged CD8+ Tregs. J Clin Invest 126(5):1953–1967. https://doi.org/10.1172/JCI84181PubMedPubMedCentralCrossRef

93.

Tan HY, Wang N, Li S, Hong M, Wang X, Feng Y (2016) The reactive oxygen species in macrophage polarization: reflecting its dual role in progression and treatment of human diseases. Oxid Med Cell Longev 2016:2795090. https://doi.org/10.1155/2016/2795090PubMedPubMedCentralCrossRef

94.

Zhang Y, Choksi S, Chen K, Pobezinskaya Y, Linnoila I, Liu ZG (2013) ROS play a critical role in the differentiation of alternatively activated macrophages and the occurrence of tumor-associated macrophages. Cell Res 23(7):898–914. https://doi.org/10.1038/cr.2013.75PubMedPubMedCentralCrossRef

95.

Erler JT, Bennewith KL, Cox TR, Lang G, Bird D, Koong A, Le QT, Giaccia AJ (2009) Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 15(1):35–44. https://doi.org/10.1016/j.ccr.2008.11.012PubMedPubMedCentralCrossRef

96.

Liu Y, Lv J, Liang X, Yin X, Zhang L, Chen D, Jin X, Fiskesund R, Tang K, Ma J, Zhang H, Dong W, Mo S, Zhang T, Cheng F, Zhou Y, Xie J, Wang N, Huang B (2018) Fibrin stiffness mediates dormancy of tumor-repopulating cells via a Cdc42-Driven Tet2 epigenetic program. Cancer Res 78(14):3926–3937. https://doi.org/10.1158/0008-5472.CAN-17-3719PubMedCrossRef

97.

Bertero T, Oldham WM, Grasset EM, Bourget I, Boulter E, Pisano S, Hofman P, Bellvert F, Meneguzzi G, Bulavin DV, Estrach S, Feral CC, Chan SY, Bozec A, Gaggioli C (2019) Tumor-stroma mechanics coordinate amino acid availability to sustain tumor growth and malignancy. Cell Metab 29(1):124-140.e110. https://doi.org/10.1016/j.cmet.2018.09.012PubMedCrossRef

98.

Eble JA, de Rezende FF (2014) Redox-relevant aspects of the extracellular matrix and its cellular contacts via integrins. Antioxid Redox Signal 20(13):1977–1993. https://doi.org/10.1089/ars.2013.5294PubMedPubMedCentralCrossRef

99.

Nelson KK, Subbaram S, Connor KM, Dasgupta J, Ha XF, Meng TC, Tonks NK, Melendez JA (2006) Redox-dependent matrix metalloproteinase-1 expression is regulated by JNK through Ets and AP-1 promoter motifs. J Biol Chem 281(20):14100–14110. https://doi.org/10.1074/jbc.M601820200PubMedCrossRef

100.

Bartling TR, Subbaram S, Clark RR, Chandrasekaran A, Kar S, Melendez JA (2014) Redox-sensitive gene-regulatory events controlling aberrant matrix metalloproteinase-1 expression. Free Radic Biol Med 74:99–107. https://doi.org/10.1016/j.freeradbiomed.2014.06.017PubMedPubMedCentralCrossRef

Title: The role of redox system in metastasis formation
Authors: Chiara Cencioni
Valentina Comunanza
Emanuele Middonti
Edoardo Vallariello
Federico Bussolino
Publication date: 01-08-2021
Publisher: Springer Netherlands
Keyword: Metastasis
Published in: Angiogenesis / Issue 3/2021
Print ISSN: 0969-6970
Electronic ISSN: 1573-7209
DOI: https://doi.org/10.1007/s10456-021-09779-5

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