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Review

Animal models for studying tumor microenvironment (TME) and resistance to lymphocytic infiltration

ORCID Icon &
Pages 745-754 | Received 05 Dec 2017, Accepted 24 Apr 2018, Published online: 16 May 2018

References

  • Ambrose J, Livitz M, Wessels D, Kuhl S, Lusche DF, Scherer A, Voss E, Soll DR. Mediated coalescence: a possible mechanism for tumor cellular heterogeneity. Am J Cancer. 2015;5(11):3485–504.
  • Cassetta L, Noy R, Swierczak A, Sugano G, Smith H. Isolation of mouse and human tumor-associated macrophages. Adv Exp Med Biol. 2016;899:211–29. doi:10.1007/978-3-319-26666-4.
  • Tommelein J, Verset L, Boterberg T, Demetter P, Bracke M, Wever O De. Cancer-associated fibroblasts connect metastasis- promoting communication in colorectal cancer. Front Oncol. 2015;5(March):1–11. doi:10.3389/fonc.2015.00063.
  • Quatromoni JG, Eruslanov E. Tumor-associated macrophages: function, phenotype, and link to prognosis in human lung cancer. Am J Transl Res. 2012;4(4):376–89.
  • Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006;6(May):392–401. doi:10.1038/nrc1877.
  • Elpek KG, Cremasco V, Shen H, Harvey CJ, Wucherpfennig KW, Goldstein DR, Monach PA, Turley SJ. The tumor microenvironment shapes lineage, transcriptional , and functional diversity of infi ltrating myeloid cells. Cancer Immunol Res. 2014;2(7):1–14. doi:10.1158/2326-6066.CIR-13-0209.
  • Joyce JA, Fearon D. T cell exclusion, immune privilege, and the tumor microenvironment. Science. 2015;348(6230):74–80.
  • Pepin F, Bertos N, Laferrière J, Sadekova S, Souleimanova M, Zhao H, Finak G, Meterissian S, Hallett MT, Park M. Gene-expression profiling of microdissected breast cancer microvasculature identifies distinct tumor vascular subtypes. Breast Cancer Res. 2012;14(4):R120.
  • Saleh SMI, Bertos N, Gruosso T, Gigoux M, Souleimanova M, Zhao H, Omeroglu A, Hallett MT, Park M. Identification of interacting stromal axes in triple-negative breast cancer. Cancer Res. 2017;77(17):4673–84. doi:10.1158/0008-5472.CAN-16-3427.
  • Quail DF, Joyce JA. Perspective the microenvironmental landscape of brain tumors. Cancer Cell. 2017;31(3):326–41. doi:10.1016/j.ccell.2017.02.009.
  • Sharma P, Allison J. The future of immune checkpoint therapy. Science. 2015;348(6230):55–61. doi:10.1126/science.aaa8172.
  • Andreola G, Rivoltini L, Castelli C, Huber V, Perego P, Deho P, Squarcina P, Accornero P, Lozupone F, Lugini L, et al. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing Microvesicles. JEM. 2002;195(10):1303–16. doi:10.1084/jem.20011624.
  • Motz GT, Santoro SP, Wang L, Garrabrant T, Lastra RR, Hagemann IS, Lal P, Feldman MD, Benencia F, Coukos G. Tumor endothelium FasL establishes a selective immune barrier promoting tolerance in tumors. Nat Med. 2014;20(6):607–15. doi:10.1038/nm.3541.
  • Buckanovich RJ, Facciabene A, Kim S, Benencia F, Sasaroli D, Balint K, Katsaros D, O'Brien-Jenkins A, Gimotty PA, Coukos G. Endothelin B receptor mediates the endothelial barrier to T cell homing to tumors and disables immune therapy. Nat Med. 2008;14(1):28–36. doi:10.1038/nm1699.
  • Molon B, Ugel S, Del Pozzo F, et al. Chemokine nitration prevents intratumoral infiltration of antigen-specific T cells. JEM. 2011;208(10):1949–62. doi:10.1084/jem.20101956.
  • Harlin H, Meng Y, Peterson AC, Zha Y, Tretiakova M, Slingluff C, McKee M, Gajewski TF. Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res. 2009;69(7):3077–86. doi:10.1158/0008-5472.CAN-08-2281.
  • Overmeire V, Ja VG. Tissue-resident versus monocyte-derived macrophages in the tumor microenvironment. Biochim biophys acta. 2016;1865(1):23–34. doi:10.1016/j.bbcan.2015.06.009.
  • Leigh IM, Navsaria H, Purkis PE, Mckay IA, Bowden PE, Riddle PN. Keratins (Kl6 and Kl7) as markers of keratinocyte hyperproliferation in psoriasis. Br J Dermatol. 1995;133(4):6501–11. doi:10.1111/j.1365-2133.1995.tb02696.x.
  • Zarbo R, Gown A, Nagle R, Visscher D, Crissman J. Anomalous cytokeratin expression in malignant melanoma: one- and two- dimensional western blot analysis and immunohistochemical survey of 100. Mod Pathol. 1990;3(4):4949–501.
  • Brissette JL, Kumar NM, Gilula NB, Hall JE, Dotto GP. Switch in gap junction protein expression is associated with selective changes in junctional permeability during keratinocyte differentiation. Proc Natl Acad Sci U S A. 1994;91(July):6453–7.
  • Jiang YJ, Kim P, Lu YF, Feingold KR. PPARgamma activators stimulate aquaporin 3 expression in keratinocytes⁄epidermis. Exp Deramatology. 2011;20:595–9. doi:10.1111/j.1600-0625.2011.01269.x.
  • Jefferson JJ, Leung CL, Liem RKH. Plakins : Goliaths that link cell junctions and the cytoskeleton PLAKINS : Goliaths that link cell junctions and the cytoskeleton. Nat Rev Mol Cell Bio. 2015;5(August 2004):542–53. doi:10.1038/nrm1425.
  • Goodenough DA, Paul DL. Gap junctions. Cold Spring Harb Perspect Biol. 2009;1:1–19.
  • Shi X, Jin L, Dang E, Chang T, Feng Z, Liu Y, Wang G. IL-17A upregulates Keratin 17 expression in keratinocytes through STAT1- and STAT3-dependent mechanisms. J Invest Dermatol. 2011;131(12):2401–8. doi:10.1038/jid.2011.222.
  • Whatcott CJ, Diep CH, Jiang P, Watanabe A, LoBello J, Sima C, Hostetter G, Shepard HM, Von Hoff DD, Han H. Desmoplasia in primary tumors and metastatic lesions of pancreatic cancer. Clin Cancer Res. 2015;21:3561–9. doi:10.1158/1078-0432.CCR-14-1051.
  • Augsten M. Cancer-associated fibroblasts as another polarized cell type of the tumor microenvironment. Front Oncol. 2014;4(March):1–8. doi:10.3389/fonc.2014.00062.
  • Fan H, Hall P, Santos LL, Gregory JL, Fingerle-Rowson G, Bucala R, Morand EF, Hickey MJ. Macrophage migration inhibitory factor and CD74 regulate macrophage chemotactic responses via MAPK and Rho GTPase. J Immunol. 2011;186:4915–24. doi:10.4049/jimmunol.1003713.
  • Lu J, Chatterjee M, Schmid H, Beck S, Gawaz M. CXCL14 as an emerging immune and inflammatory modulator. J Inflamm. 2016;13((1)):1–8. doi:10.1186/s12950-015-0109-9.
  • Tanegashima K, Suzuki K, Nakayama Y, Tsuji K, Shigenaga A, Otaka A, Hara T. CXCL14 is a natural inhibitor of the CXCL12 – CXCR4 signaling axis. FEBS Lett. 2013;587(12):1731–5. doi:10.1016/j.febslet.2013.04.046.
  • Zhang XHF, Jin X, Malladi S, Zou Y, Wen YH, Brogi E, Smid M, Foekens JA, Massagué J. Selection of bone metastasis seeds by mesenchymal signals in the primary tumor stroma. Cell. 2013;154:1060–73. doi:10.1016/j.cell.2013.07.036.
  • Marcus A, Gowen BG, Thompson TW, Iannello A, Ardolino M, Deng W, Wang L, Shifrin N, Raulet DH. Recognition of tumors by the innate immune system and natural killer cells. Adv Immunol. 1st ed. Elsevier Inc.; 2014;122:91–128. doi:10.1016/B978-0-12-800267-4.00003-1.
  • Malladi S, Macalinao DG, Jin X, Zou Y, Stanchina E De, Massague J. Metastatic latency and immune evasion through autocrine inhibition of WNT. Cell. 2016;165:45–60. doi:10.1016/j.cell.2016.02.025.
  • Spranger S, Bao R, Gajewski TF. Melanoma-intrinsic b -catenin signalling prevents anti-tumour immunity. Nature. 2015;523:231–5. doi:10.1038/nature14404.
  • Malanchi I, Peinado H, Kassen D, Hussenet T, Metzger D, Chambon P, Huber M, Hohl D, Cano A, Birchmeier W, et al. Cutaneous cancer stem cell maintenance is dependent on b -catenin signalling. Nature. 2008;452(April):650–3. doi:10.1038/nature06835.
  • Enholm B, Paavonen K, Ristima A, Kumar V, Gunji Y, Klefstrom J, Kivinen L, Laiho M, Olofsson B, Joukov V, et al. Comparison of VEGF , VEGF-B , VEGF-C and Ang-1 mRNA regulation by serum, growth factors, oncoproteins and hypoxia. Oncogene. 1997;14:2475–83.
  • Velasquez S, Killian D, Schulte J, Sticht C, Thiel M, Lindner HA. Short term hypoxia synergizes with Interleukin 15 priming in driving glycolytic gene transcription and supports human natural killer cell activities. JBC. 2016;291(25):12960–77. doi:10.1074/jbc.M116.721753.
  • Strengell M, Matikainen S, Sirén J, Foster D, Julkunen I, Sareneva T. IL-21 in synergy with IL-15 or IL-18 enhances IFN- γ production in human NK and T cells. J Immunol. 2018;170:5464–5469. doi:10.4049/jimmunol.170.11.5464.
  • Krzywinska E, Kantari-mimoun C, Kerdiles Y, Sobecki M, Isagawa T, Gotthardt D, Castells M, Haubold J, Millien C, Viel T, et al. Loss of HIF-1α in natural killer cells inhibits tumour growth by stimulating non-productive angiogenesis. Nat Commun. 2017;8:1597. doi:10.1038/s41467-017-01599-w.
  • Zhang J, Basher F, Wu JD. NKG2D ligands in tumor immunity : two sides of a coin. Front Immunol. 2015;6(March):1–7. doi:10.3389/fimmu.2015.00097.
  • Diefenbach A, Jamieson AM, Liu SD, Shastri N, Raulet DH. Ligands for the murine NKG2D receptor : expression by tumor cells and activation of NK cells and macrophages. Nat Immunolgy. 2000;1(2):119–26.
  • Terada N, Hamazaki T, Oka M, Hoki M, Mastalerz DM, Nakano Y, Meyer EM, Morel L, Petersen BE, Scott EW. Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature. 2002;416(April):542–5.
  • Noubissi FK, Ogle BM. Cancer cell fusion : Mechanisms slowly unravel. Int J Mol Sci. 2016;17:1587. doi:10.3390/ijms17091587.
  • Sellappan S, Grijalva R, Zhou X, Yang W, Eli MB, Mills GB, Yu D. Lineage infidelity of MDA-MB-435 cells : Expression of melanocyte proteins in a breast cancer cell line. Cancer Resrearch. 2004;64:3479–85.
  • Johnson-léger C, Aurrand-lions M, Imhof BA. The parting of the endothelium : miracle , or simply a junctional affair? J Cell Sci. 2000;113:921–33.
  • Shulman Z, Shinder V, Klein E, Grabovsky V, Yeger O, Geron E, Montresor A, Bolomini-Vittori M, Feigelson SW, Kirchhausen T, et al. Lymphocyte crawling and transendothelial migration require chemokine triggering of high-affinity LFA-1 integrin. Immunity. 2010;30(3):384–96. doi:10.1016/j.immuni.2008.12.020.Lymphocyte.
  • Shulman Z, Cohen SJ, Roediger B, et al. Transendothelial migration of lymphocytes mediated by intraendothelial vesicle stores rather than by extracellular chemokine depots. Nat Immunol. 2012;13(1):67–77. doi:10.1038/ni.2173.
  • Ren G, Zhao X, Zhang L, Zhang J, L'Huillier A, Ling W, Roberts AI, Le AD, Shi S, Shao C, et al. Inflammatory cytokine-induced intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in mesenchymal stem cells are critical for immunosuppression. J Immunol. 2010;184:2321–8. doi:10.4049/jimmunol.0902023.
  • Stocker CJ, Sugars KL, Harari OA, Landis C, Morley BJ, Haskard DO. TNF- α , IL-4, and IFN- γ regulate differential expression of P- and E-selectin expression by porcine aortic endothelial cells. J Immunol. 2000;164:3309–15. doi:10.4049/jimmunol.164.6.3309.
  • Nakajima C, Uekusa Y, Iwasaki M. A role of interferon- γ ( IFN- γ ) in tumor immunity : T cells with the capacity to reject tumor cells are generated but fail to migrate to tumor sitesin IFN- γ -deficient mice. Cancer Res. 2001:3399–405.
  • Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ, Schreiber RD. IFN g and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature. 2001;410(6832, April):1107–11.
  • Miller CP, Thorpe JD, Kortum AN, Coy CM, Cheng WY, Ou Yang TH, Anastassiou D, Beatty JD, Urban ND, Blau CA, et al. JAK2 expression is associated with tumor-infiltrating lymphocytes and improved breast cancer outcomes : Implications for evaluating JAK2 inhibitors. Cancer Immunol Res. 2014;2(File 6643):301–7. doi:10.7303/syn4517.1.
  • Trivedi PM, Graham KL, Scott NA, Jenkins MR, Majaw S, Sutherland RM, Fynch S, Lew AM, Burns CJ, Krishnamurthy B, et al. Repurposed JAK1/JAK2 inhibitor reverses established autoimmune insulitis in non-obese diabetic mice. Diabetes. 2017;66( October 2016):db161250. doi:10.2337/db16-1250.
  • Shea JJO, Kontzias A, Yamaoka K, Tanaka Y, Laurence A. Janus kinase inhibitors in autoimmune diseases. Ann Rheum Dis. 2013;72(Suppl 2):ii111–5. doi:10.1136/annrheumdis-2012-202576.
  • Crispin MK, Ko JM, Craiglow BG, Li S, Shankar G, Urban JR, Chen JC, Cerise JE, Jabbari A, Winge MC, et al. Safety and efficacy of the JAK inhibitor tofacitinib citrate in patients with alopecia areata. JCI Insight. 2016;1(15):e89776. doi:10.1172/jci.insight.89776.
  • Strachan DC, Ruffell B, Oei Y, Bissell MJ, Coussens LM, Pryer N, Daniel D. CSF1R inhibition delays cervical and mammary tumor growth in murine models by attenuating the turnover of tumor-associated macrophages and enhancing infiltration by CD8 T cells. Oncoimmunology. 2013;2(12):e26968. doi:10.4161/onci.26968.
  • Zhu Y, Knolhoff BL, Meyer MA, Nywening TM, West BL, Luo J, Wang-Gillam A, Goedegebuure SP, Linehan DC, DeNardo DG. CSF1 / CSF1R blockade reprograms tumor-infiltrating macrophages and improves response to T-cell checkpoint immunotherapy in pancreatic cancer models. Cancer Res. 2014;74:5057–70. doi:10.1158/0008-5472.CAN-13-3723.
  • Feig C, Jones JO, Kraman M, Wells RJ, Deonarine A, Chan DS, Connell CM, Roberts EW, Zhao Q, Caballero OL, et al. Targeting CXCL12 from FAP-expressing carcinoma- associated fibroblasts synergizes with anti–PD-L1 immunotherapy in pancreatic cancer. PNAS. 2013;110(50):20212–7.
  • Bayne LJ, Beatty GL, Jhala N, Clark CE, Rhim AD, Stanger BZ. Tumor-derived granulocytes-macrophage colony-stimulating factor regulates myeloid inflammation and T cell immunity in pancreatic cancer. Cancer Cell. 2012;21(6):822–35. doi:10.1016/j.ccr.2012.04.025.
  • Pylayeva-gupta Y, Lee KE, Hajdu CH, Miller G, Bar-sagi D. Oncogenic kras-induced GM-CSF production promotes the development of pancreatic Neoplasia. Cancer Cell. 2012;21(6):836–47. doi:10.1016/j.ccr.2012.04.024.
  • Garcia AJ, Ruscetti M, Arenzana TL, Tran LM, Bianci-frias D, Sybert E. Pten null prostate epithelium promotes localized myeloid-derived suppressor cell expansion and immune suppression during tumor. Mol Cell Biol. 2017;34(11):2017–28. doi:10.1128/MCB.00090-14.
  • Lesokhin AM, Hohl TM, Kitano S, Cortez C, Hirschhorn-Cymerman D, Avogadri F, Rizzuto GA, Lazarus JJ, Pamer EG, Houghton AN, et al. Monocytic CCR2 þ myeloid-derived suppressor cells promote immune escape by limiting activated CD8 T-cell In fi ltration into the tumor microenvironment. Cancer Res. 2012;72(4):876–87. doi:10.1158/0008-5472.CAN-11-1792.
  • Tabbekh M, Franciszkiewicz K. Rescue of tumor-infiltrating lymphocytes from activation-induced cell death enhances the antitumor CTL response in CD5-deficient mice. J Immunol. 2018;187:102–9. doi:10.4049/jimmunol.1004145.
  • Brossard C, Semichon M, Trautmann A, Bismuth G. CD5 inhibits signaling at the immunological synapse without impairing its formation. J Immunol. 2018;170:4623–9. doi:10.4049/jimmunol.170.9.4623.
  • Tarakhovsky A, Muller W, Rajewsky K. Lymphocyte populations and immune responses in CD5- deficient mice. Eur J Immunol. 1994;24(7):1677–84. doi:10.1002/eji.1830240733.
  • Zhou R, He P, Ren Y, Wang WH, Zhou RY, Wan H, Ono S, Fujiwara H, Zuo JP. Myeloid suppressor cell-associated immune dysfunction in CSA1M fibrosarcoma tumor-bearing mice. Cancer Sci. 2007;98(6):882–9. doi:10.1111/j.1349-7006.2007.00465.x.
  • Lee E, Schultz KLW, Griffin DE. Mice deficient in interferon-gamma or interferon-gamma receptor 1 have distinct inflammatory responses to acute viral encephalomyelitis. PLoS One. 2013;8(10):1–13. doi:10.1371/journal.pone.0076412.
  • Swiercz JM, Kuner R, Offermanns S. Plexin-B1 directly interacts with PDZ-RhoGEF / LARG to regulate RhoA and growth cone morphology. Neuron. 2002;35:51–63.
  • Negishi-koga T, Shinohara M, Komatsu N, Bito H, Kodama T, Friedel RH, Takayanagi H. Suppression of bone formation by osteoclastic expression of semaphorin 4D. Nat Med. 2011;17(11):1473–80. doi:10.1038/nm.2489.
  • Evans EE, Paris M, Smith ES, Zauderer M. Immunomodulation of the tumor microenvironment by neutralization of Semaphorin 4D. Oncoimmunology. 2015;4(12):e1054599.
  • Evans EE, Jonason AS, Jr, Bussler H, Torno S, Veeraraghavan J, Reilly C, Doherty MA, Seils J, Winter LA, Mallow C, et al. Antibody blockade of semaphorin 4D promotes immune infiltration into tumor and enhances response to other immunomodulatory therapies. Cancer Immunol Res. 2015;3(19):689–702. doi:10.1158/2326-6066.CIR-14-0171.
  • Delaire S, Billard C, Tordjman R, Chédotal A, Elhabazi A, Bensussan A, Boumsell L. Biological activity of soluble CD100. II. Soluble CD100, similarly to H-SemaIII, inhibits immune cell migration. J Immunol. 2001;166:4348–54. doi:10.4049/jimmunol.166.7.4348.
  • Shi W, Kumanogoh A, Watanabe C, Uchida J, Wang X, Yasui T, Yukawa K, Ikawa M, Okabe M, Parnes JR, et al. The Class IV Semaphorin CD100 plays nonredundant roles in the immune system : Defective B and T cell activation in CD100-Deficient mice. Immunity. 2000;13:633–42.
  • Ito T, Bai TAO, Tanaka T, Yoshida K, Ueyama T. Semaphorin 4D induces vaginal epithelial cell apoptosis to control mouse postnatal vaginal tissue remodeling. Mol Med Rep. 2015;11:829–36. doi:10.3892/mmr.2014.2773.
  • Man Y. Tumor cell budding from focally disrupted tumor capsules : a common pathway for all breast cancer subtype derived invasion ? J Cancer. 2010;1:32–37.
  • Cho A, Reidy MA. Matrix Metalloproteinase-9 is necessary for the regulation of smooth muscle cell replication and migration after arterial injury. Circ Res. 2002;2002(91):845–51. doi:10.1161/01.RES.0000040420.17366.2E.
  • Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ. Efficient tumour formation by single human melanoma cells. Nature. 2008;456(7222):593–8. doi:10.1038/nature07567.
  • Ribas A. Adaptive immune resistance : How cancer protects from immune attack. Cancer Discov. 2015;5(September):915–20. doi:10.1158/2159-8290.CD-15-0563.
  • Morgan RA, Chinnasamy N, Abate-daga DD, et al. Cancer regressions and neurologic toxicity following anti-MAGE-A3 TCR gene therapy. J Immunother. 2014;36(2):133–51. doi:10.1097/CJI.0b013e3182829903.Cancer.
  • Morgan RA, Yang JC, Kitano M, Dudley ME, Laurencot CM, Rosenberg SA. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ErbB2. Mol Ther. 2010;18(4):843–51. doi:10.1038/mt.2010.24.
  • Ramos CA, Savoldo B, Dotti G. CD19-CAR trials. Cancer J. 2014;20(2):112–8. doi:doi:10.1097/PPO.0000000000000031.
  • Zhang W, Wang Y, Guo Y, Dai HR, Yang QM, Zhang YJ, Zhang Y, Chen MX, Wang CM, Feng KC, et al. Treatment of CD20-directed chimeric antigen receptor-modified T cells in patients with relapsed or refractory B-cell non-Hodgkin lymphoma : an early phase IIa trial report. Signal Transduct Target Ther. 2016;1(November 2015):1–9. doi:10.1038/sigtrans.2016.2.
  • Chen DR, Cohen PL. Living life without B cells: is repeated B-cell depletion a safe and effective long-term treatment plan for rheumatoid arthrits? Int J Clin Rheumtol. 2012;7(2):159–66.
  • Lim WA, June CH. The principles of engineering immune cells to treat cancer. Cell. 2017;168(4):724–40. doi:10.1016/j.cell.2017.01.016.