2,103
Views
5
CrossRef citations to date
0
Altmetric
Research Article

Human innate immune cell crosstalk induces melanoma cell senescence

, , , , , , , , , & show all
Article: 1808424 | Received 29 Nov 2019, Accepted 24 Jul 2020, Published online: 30 Aug 2020

References

  • Schakel K, Mayer E, Federle C, Schmitz M, Riethmuller G, Rieber EP. A novel dendritic cell population in human blood: one-step immunomagnetic isolation by a specific mAb (M-DC8) and in vitro priming of cytotoxic T lymphocytes. Eur J Immunol. 1998;28:4084–12. doi:10.1002/(SICI)1521-4141(199812)28:12<4084::AID-IMMU4084>3.0.CO;2-4.
  • Schakel K, Kannagi R, Kniep B, Goto Y, Mitsuoka C, Zwirner J, Soruri A, von Kietzell M, Rieber EP. 6-Sulfo LacNAc, a novel carbohydrate modification of PSGL-1, defines an inflammatory type of human dendritic cells. Immunity. 2002;17(3):289–301. doi:10.1016/S1074-7613(02)00393-X.
  • Schakel K, von Kietzell M, Hansel A, Ebling A, Schulze L, Haase M, Semmler C, Sarfati M, Barclay AN, Randolph GJ. Human 6-sulfo LacNAc-expressing dendritic cells are principal producers of early interleukin-12 and are controlled by erythrocytes. Immunity. 2006;24:767–777. doi:10.1016/j.immuni.2006.03.020.
  • Schmitz M, Zhao S, Deuse Y, Schakel K, Wehner R, Wohner H, Hölig K, Wienforth F, Kiessling A, Bornhäuser M, et al. Tumoricidal potential of native blood dendritic cells: direct tumor cell killing and activation of NK cell-mediated cytotoxicity. J Immunol. 2005;174(7):4127–4134. doi:10.4049/jimmunol.174.7.4127.
  • Vermi W, Micheletti A, Lonardi S, Costantini C, Calzetti F, Nascimbeni R, Bugatti M, Codazzi M, Pinter PC, Schäkel K, et al. slanDCs selectively accumulate in carcinoma-draining lymph nodes and marginate metastatic cells. Nat Commun. 2014;5(1):3029. doi:10.1038/ncomms4029.
  • Vermi W, Micheletti A, Finotti G, Tecchio C, Calzetti F, Costa S, Bugatti M, Calza S, Agostinelli C, Pileri S. slan(+) Monocytes and macrophages mediate CD20-dependent B-cell lymphoma elimination via ADCC and ADCP. Cancer Res. 2018;78:3544–3559. doi:10.1158/0008-5472.CAN-17-2344.
  • Micheletti A, Finotti G, Calzetti F, Lonardi S, Zoratti E, Bugatti M, Stefini S, Vermi W, Cassatella MA. slanDCs/M-DC8+ cells constitute a distinct subset of dendritic cells in human tonsils [corrected]. Oncotarget. 2016;7:161–175. doi:10.18632/oncotarget.6660.
  • Wehner R, Lobel B, Bornhauser M, Schakel K, Cartellieri M, Bachmann M, Rieber EP, Schmitz M. Reciprocal activating interaction between 6-sulfo LacNAc + dendritic cells and NK cells. Int J Cancer. 2009;124(2):358–366. doi:10.1002/ijc.23962.
  • Schmitz M, Zhao S, Schakel K, Bornhauser M, Ockert D, Rieber EP. Native human blood dendritic cells as potent effectors in antibody-dependent cellular cytotoxicity. Blood. 2002;100:1502–1504. doi:10.1182/blood.V100.4.1502.h81602001502_1502_1504.
  • Tufa DM, Ahmad F, Chatterjee D, Ahrenstorf G, Schmidt RE, Jacobs R. IL-1beta limits the extent of human 6-sulfo LacNAc dendritic cell (slanDC)-mediated NK cell activation and regulates CD95-induced apoptosis. Cell Mol Immunol. 2017;14:976–985. doi:10.1038/cmi.2016.17.
  • Hanna RN, Cekic C, Sag D, Tacke R, Thomas GD, Nowyhed H, Herrley E, Rasquinha N, McArdle S, Wu R. Patrolling monocytes control tumor metastasis to the lung. Science. 2015;350(6263):985–990. doi:10.1126/science.aac9407.
  • Narasimhan PB, Eggert T, Zhu YP, Marcovecchio P, Meyer MA, Wu R, Hedrick CC. Patrolling monocytes control NK cell expression of activating and stimulatory receptors to curtail lung metastases. J Immunol. 2020;204(1):192–198. doi:10.4049/jimmunol.1900998.
  • Castriconi R, Carrega P, Dondero A, Bellora F, Casu B, Regis S, Ferlazzo G, Bottino C. Molecular mechanisms directing migration and retention of natural killer cells in human tissues. Front Immunol. 2018;9:2324. doi:10.3389/fimmu.2018.02324.
  • Lima M, Leander M, Santos M, Santos AH, Lau C, Queiros ML, Gonçalves M, Fonseca S, Moura J, Teixeira MDA. Chemokine receptor expression on normal blood CD56 + NK-cells elucidates cell partners that comigrate during the innate and adaptive immune responses and identifies a transitional NK-cell population. J Immunol Res. 2015;2015:839684. doi:10.1155/2015/839684.
  • Vujanovic L, Ballard W, Thorne SH, Vujanovic NL, Butterfield LH. Adenovirus-engineered human dendritic cells induce natural killer cell chemotaxis via CXCL8/IL-8 and CXCL10/IP-10. Oncoimmunology. 2012;1(4):448–457. doi:10.4161/onci.19788.
  • Barrow AD, Edeling MA, Trifonov V, Luo J, Goyal P, Bohl B, Bando JK, Kim AH, Walker J, Andahazy M. Natural killer cells control tumor growth by sensing a growth factor. Cell. 2018;172(3):e19. doi:10.1016/j.cell.2017.11.037.
  • Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell. 1997;88(5):593–602. doi:10.1016/S0092-8674(00)81902-9.
  • Schmitt CA, Fridman JS, Yang M, Lee S, Baranov E, Hoffman RM, Lowe SW. A senescence program controlled by p53 and p16INK4a contributes to the outcome of cancer therapy. Cell. 2002;109(3):335–346. doi:10.1016/S0092-8674(02)00734-1.
  • Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP, et al. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science. 1998;282:1497–1501. doi:10.1126/science.282.5393.1497.
  • Wang S, Zhou M, Lin F, Liu D, Hong W, Lu L, Zhu Y, Xu A. Interferon-gamma induces senescence in normal human melanocytes. PLoS One. 2014;9:e93232. doi:10.1371/journal.pone.0093232.
  • Kumar PS, Shiras A, Das G, Jagtap JC, Prasad V, Shastry P. Differential expression and role of p21cip/waf1 and p27kip1 in TNF-alpha-induced inhibition of proliferation in human glioma cells. Mol Cancer. 2007;6:42. doi:10.1186/1476-4598-6-42.
  • Kandhaya-Pillai R, Miro-Mur F, Alijotas-Reig J, Tchkonia T, Kirkland JL, Schwartz S. TNFalpha-senescence initiates a STAT-dependent positive feedback loop, leading to a sustained interferon signature, DNA damage, and cytokine secretion. Aging (Albany NY). 2017;9:2411–2435. doi:10.18632/aging.101328.
  • Wieder T, Brenner E, Braumuller H, Bischof O, Rocken M. Cytokine-induced senescence for cancer surveillance. Cancer Metastasis Rev. 2017;36:357–365. doi:10.1007/s10555-017-9667-z.
  • Braumuller H, Wieder T, Brenner E, Assmann S, Hahn M, Alkhaled M, Schilbach K, Essmann F, Kneilling M, Griessinger C. T-helper-1-cell cytokines drive cancer into senescence. Nature. 2013;494(7437):361–365. doi:10.1038/nature11824.
  • Richardson RM, Pridgen BC, Haribabu B, Ali H, Snyderman R. Differential cross-regulation of the human chemokine receptors CXCR1 and CXCR2. Evidence for time-dependent signal generation. J Biol Chem. 1998;273(37):23830–23836. doi:10.1074/jbc.273.37.23830.
  • Nasser MW, Raghuwanshi SK, Grant DJ, Jala VR, Rajarathnam K, Richardson RM. Differential activation and regulation of CXCR1 and CXCR2 by CXCL8 monomer and dimer. J Immunol. 2009;183:3425–3432. doi:10.4049/jimmunol.0900305.
  • Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A. 1995;92:9363–9367. doi:10.1073/pnas.92.20.9363.
  • Coppe JP, Desprez PY, Krtolica A, Campisi J. The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu Rev Pathol. 2010;5:99–118. doi:10.1146/annurev-pathol-121808-102144.
  • Collison JL, Carlin LM, Eichmann M, Geissmann F, Peakman M. Heterogeneity in the locomotory behavior of human monocyte subsets over human vascular endothelium in vitro. J Immunol. 2015;195:1162–1170. doi:10.4049/jimmunol.1401806.
  • Cros J, Cagnard N, Woollard K, Patey N, Zhang SY, Senechal B, Puel A, Biswas SK, Moshous D, Picard C. Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity. 2010;33:375–386. doi:10.1016/j.immuni.2010.08.012.
  • Bellora F, Castriconi R, Dondero A, Carrega P, Mantovani A, Ferlazzo G, Moretta A, Bottino C. Human NK cells and NK receptors. Immunol Lett. 2014;161(2):168–173. doi:10.1016/j.imlet.2013.12.009.
  • Carrega P, Bonaccorsi I, Di Carlo E, Morandi B, Paul P, Rizzello V, Cipollone G, Navarra G, Mingari MC, Moretta L. CD56(bright)perforin(low) noncytotoxic human NK cells are abundant in both healthy and neoplastic solid tissues and recirculate to secondary lymphoid organs via afferent lymph. J Immunol. 2014;192:3805–3815. doi:10.4049/jimmunol.1301889.
  • Levi I, Amsalem H, Nissan A, Darash-Yahana M, Peretz T, Mandelboim O, Rachmilewitz J. Characterization of tumor infiltrating natural killer cell subset. Oncotarget. 2015;6:13835–13843. doi:10.18632/oncotarget.3453.
  • Alfaro C, Teijeira A, Onate C, Perez G, Sanmamed MF, Andueza MP, Alignani D, Labiano S, Azpilikueta A, Rodriguez-Paulete A. Tumor-produced interleukin-8 attracts human myeloid-derived suppressor cells and elicits extrusion of neutrophil extracellular traps (NETs). Clin Cancer Res. 2016;22(15):3924–3936. doi:10.1158/1078-0432.CCR-15-2463.
  • Ogawa R, Yamamoto T, Hirai H, Hanada K, Kiyasu Y, Nishikawa G, Mizuno R, Inamoto S, Itatani Y, Sakai Y, et al. Loss of SMAD4 promotes colorectal cancer progression by recruiting tumor-associated neutrophils via the cxcl1/8-cxcr2 axis. Clin Cancer Res. 2019;25:2887–2899. doi:10.1158/1078-0432.CCR-18-3684.
  • Highfill SL, Cui Y, Giles AJ, Smith JP, Zhang H, Morse E, Kaplan RN, Mackall CL. Disruption of CXCR2-mediated MDSC tumor trafficking enhances anti-PD1 efficacy. Sci Transl Med. 2014;6(237):237ra67. doi:10.1126/scitranslmed.3007974.
  • Bottcher JP, Bonavita E, Chakravarty P, Blees H, Cabeza-Cabrerizo M, Sammicheli S, Rogers NC, Sahai E, Zelenay S, Reis E Sousa C. NK cells stimulate recruitment of cDC1 into the tumor microenvironment promoting cancer immune control. Cell. 2018;172(5):e14. doi:10.1016/j.cell.2018.01.004.
  • Castellano M, Pollock PM, Walters MK, Sparrow LE, Down LM, Gabrielli BG, Parsons PG, Hayward NK. CDKN2A/p16 is inactivated in most melanoma cell lines. Cancer Res. 1997;57:4868–4875.
  • Cayrol C, Knibiehler M, Ducommun B. p21 binding to PCNA causes G1 and G2 cell cycle arrest in p53-deficient cells. Oncogene. 1998;16:311–320. doi:10.1038/sj.onc.1201543.
  • Barr AR, Cooper S, Heldt FS, Butera F, Stoy H, Mansfeld J, Novák B, Bakal C. DNA damage during S-phase mediates the proliferation-quiescence decision in the subsequent G1 via p21 expression. Nat Commun. 2017;8(1):14728. doi:10.1038/ncomms14728.
  • Acosta JC, Banito A, Wuestefeld T, Georgilis A, Janich P, Morton JP, Athineos D, Kang T-W, Lasitschka F, Andrulis M. A complex secretory program orchestrated by the inflammasome controls paracrine senescence. Nat Cell Biol. 2013;15(8):978–990. doi:10.1038/ncb2784.
  • Xue W, Zender L, Miething C, Dickins RA, Hernando E, Krizhanovsky V, Cordon-Cardo C, Lowe SW. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature. 2007;445(7128):656–660. doi:10.1038/nature05529.
  • Lujambio A, Akkari L, Simon J, Grace D, Tschaharganeh DF, Bolden JE, Zhao Z, Thapar V, Joyce J, Krizhanovsky V. Non-cell-autonomous tumor suppression by p53. Cell. 2013;153(2):449–460. doi:10.1016/j.cell.2013.03.020.
  • Eggert T, Wolter K, Ji J, Ma C, Yevsa T, Klotz S, Medina-Echeverz J, Longerich T, Forgues M, Reisinger F, et al. Distinct functions of senescence-associated immune responses in liver tumor surveillance and tumor progression. Cancer Cell. 2016;30(4):533–547. doi:10.1016/j.ccell.2016.09.003.
  • Kim YH, Choi YW, Lee J, Soh EY, Kim JH, Park TJ. Senescent tumor cells lead the collective invasion in thyroid cancer. Nat Commun. 2017;8:15208. doi:10.1038/ncomms15208.
  • Liu D, Hornsby PJ. Senescent human fibroblasts increase the early growth of xenograft tumors via matrix metalloproteinase secretion. Cancer Res. 2007;67:3117–3126. doi:10.1158/0008-5472.CAN-06-3452.
  • Angelini PD, Zacarias FMF, Pedersen K, Parra-Palau JL, Guiu M, Bernado Morales C, et al. Constitutive HER2 signaling promotes breast cancer metastasis through cellular senescence. Cancer Res. 2013;73:450–458. doi:10.1158/0008-5472.CAN-12-2301.
  • Milanovic M, Fan DNY, Belenki D, Dabritz JHM, Zhao Z, Yu Y, Dörr JR, Dimitrova L, Lenze D, Monteiro Barbosa IA, et al. Senescence-associated reprogramming promotes cancer stemness. Nature. 2018;553(7686):96–100. doi:10.1038/nature25167.
  • Yang L, Fang J, Chen J. Tumor cell senescence response produces aggressive variants. Cell Death Discov. 2017;3(1):17049. doi:10.1038/cddiscovery.2017.49.
  • Iannello A, Thompson TW, Ardolino M, Lowe SW, Raulet DH. p53-dependent chemokine production by senescent tumor cells supports NKG2D-dependent tumor elimination by natural killer cells. J Exp Med. 2013;210:2057–2069. doi:10.1084/jem.20130783.
  • Textor S, Fiegler N, Arnold A, Porgador A, Hofmann TG, Cerwenka A. Human NK cells are alerted to induction of p53 in cancer cells by upregulation of the NKG2D ligands ULBP1 and ULBP2. Cancer Res. 2011;71:5998–6009. doi:10.1158/0008-5472.CAN-10-3211.
  • Sagiv A, Burton DG, Moshayev Z, Vadai E, Wensveen F, Ben-Dor S, Golani O, Polic B, Krizhanovsky V. NKG2D ligands mediate immunosurveillance of senescent cells. Aging (Albany NY). 2016;8(2):328–344. doi:10.18632/aging.100897.
  • Ellis LZ, Cohen JL, High W, Stewart L. Melanoma in situ treated successfully using imiquimod after nonclearance with surgery: review of the literature. Dermatol Surg. 2012;38:937–946. doi:10.1111/j.1524-4725.2012.02362.x.
  • Steinmann A, Funk JO, Schuler G, von den Driesch P. Topical imiquimod treatment of a cutaneous melanoma metastasis. J Am Acad Dermatol. 2000;43:555–556.
  • Fan Q, Cohen S, John B, Riker AI. Melanoma in situ treated with topical imiquimod for management of persistently positive margins: a review of treatment methods. Ochsner J. 2015;15:443–447.
  • Tio D, van Montfrans C, Ruijter CGH, Hoekzema R, Bekkenk MW. Effectiveness of 5% Topical Imiquimod for Lentigo Maligna Treatment. Acta Derm Venereol. 2019;99:884–888. doi:10.2340/00015555-3241.