3,021
Views
22
CrossRef citations to date
0
Altmetric
Research Article

B lymphocytes contribute to stromal reaction in pancreatic ductal adenocarcinoma

, , , , , , , , , , , , , , , , , ORCID Icon & show all
Article: 1794359 | Received 07 Oct 2019, Accepted 07 Jul 2020, Published online: 16 Jul 2020

References

  • Vincent A, Herman J, Schulick R, Hruban RH, Goggins M. Pancreatic cancer. Lancet. 2011;378:607–10. doi:10.1016/S0140-6736(10)62307-0.
  • Rucki AA, Zheng L. Pancreatic cancer stroma: understanding biology leads to new therapeutic strategies. World J Gastroenterol. 2014;20(9):2237–2246. doi:10.3748/wjg.v20.i9.2237.
  • Neesse A, Algül H, Tuveson DA, Gress TM. Stromal biology and therapy in pancreatic cancer: a changing paradigm. Gut. 2015;64(9):1476–1484. doi:10.1136/gutjnl-2015-309304.
  • Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, Mc-Intyre D, Honess D, Madhu B, Goldgraben MA, Caldwell ME, Allard D, et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science. 2009;324(5933):1457–1461. doi:10.1126/science.1171362.
  • Bruun Nielsen MF, Mortensen MB, Detlefsen S. Key Players in Pancreatic Cancer-Stroma Interaction: cancer-associated Fibroblasts, Endothelial and Inflammatory Cells. World J Gastroenterol. 2016;22(9):2678–2700. doi:10.3748/wjg.v22.i9.2678.
  • Beatty GL, Chiorean EG, Fishman MP, Saboury B, Teitelbaum UR, Sun W, Huhn RD, Song W, Li D, Sharp LL, et al. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science. 2011;331(6024):1612–1616. doi:10.1126/science.1198443.
  • Heinemann V, Reni M, Ychou M, Richel DJ, Macarulla T, Ducreux M. Tumour-stroma interactions in pancreatic ductal adenocarcinoma: rationale and current evidence for new therapeutic strategies. Cancer Treat Rev. 2014;40(1):118–128. doi:10.1016/j.ctrv.2013.04.004.
  • Rhim AD, Oberstein PE, Thomas DH, Mirek ET, Palermo CF, Sastra SA, Dekleva E, Saunders T, Becerra C, Tattersall I, et al. Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell. 2014;25(6):735–747. doi:10.1016/j.ccr.2014.04.021.
  • Moffitt RA, Marayati R, Flate EL, Volmar KE, Loeza SG, Hoadley KA, Rashid NU, Williams LA, Eaton SC, Chung AH, et al. Virtual microdissection identifies distinct tumor- and stroma-specific subtypes of pancreatic ductal adenocarcinoma. Nat Genet. 2015;47(10):1168–1178. doi:10.1038/ng.3398.
  • Mathew E, Brannon AL, Del Vecchio A, Garcia PE, Penny MK, Kane KT, Vinta A, Buckanovich RJ, Di Magliano MP. Mesenchymal Stem Cells Promote Pancreatic Tumor Growth by Inducing Alternative Polarization of Macrophages. Neoplasia. 2016;18(3):142–151. doi:10.1016/j.neo.2016.01.005.
  • Della-Torre E, Feeney E, Deshpande V, Mattoo H, Mahajan V, Kulikova M, Wallace ZS, Carruthers M, Chung RT, Pillai S, et al. B-cell depletion attenuates serological biomarkers of fibrosis and myofibroblast activation in IgG4-related disease. Ann Rheum Dis. 2015;74(12):2236–2243. doi:10.1136/annrheumdis-2014-205799.
  • Della-Torre E, Rigamonti E, Perugino CA, Sain SB, Sun N, Kaneko N, Maehara T, Rovati L, Ponzoni M, Milani R, et al. B lymphocytes directly contribute to tissue fibrosis in IgG4-Related Disease. J Allergy Clin Immunol. 2020;145(3):968–981.e14. doi:10.1016/j.jaci.2019.07.004.
  • Zhang X, Liu X, Joseph L, Zhao L, Hart J, Xiao SY. Pancreatic ductal adenocarcinoma with autoimmune pancreatitis-like histologic and immunohistochemical features. Hum Pathol. 2014;45(3):621–627. doi:10.1016/j.humpath.2013.08.027.
  • Bledsoe JR, Della-Torre E, Rovati L, Deshpande V. IgG4-related disease: review of the histopathologic features, differential diagnosis, and therapeutic approach. APMIS. 2018;126(6):459–476. doi:10.1111/apm.12845.
  • Della-Torre E, Stone JH. “How I manage” IgG4-related disease. J Clin Immunol. 2016;36(8):754–763. doi:10.1007/s10875-016-0331-0.
  • Wallace ZS, Khosroshahi A, Carruthers MD, Perugino CA, Choi H, Campochiaro C, Culver EL, Cortazar F, Della‐torre E, Ebbo M, et al. An international multispecialty validation study of the IgG4-related disease responder index. Arthritis Care Res (Hoboken). 2018;70(11):1671–1678. doi:10.1002/acr.23543.
  • Della-Torre E, Mattoo H, Mahajan VS, Deshpande V, Krause D, Song P, Pillai S, Stone JH. IgG4-related midline destructive lesion. Ann Rheum Dis. 2014;73(7):1434–1436. doi:10.1136/annrheumdis-2014-205187.
  • Lanzillotta M, Della-Torre E, Stone JH. Roles of Plasmablasts and B Cells in IgG4-Related Disease: implications for Therapy and Early Treatment Outcomes. Curr Top Microbiol Immunol. 2017;401:85–92. doi:10.1007/82_2016_58.
  • Lanzillotta M, Della-Torre E, Milani R, Bozzolo E, Bozzalla-Cassione E, Rovati L, Arcidiacono PG, Partelli S, Falconi M, Ciceri F, et al. Effects of glucocorticoids on B-cell subpopulations in patients with IgG4-related disease. Clin Exp Rheumatol. 2019;37(3):159–166.
  • Lanzillotta M, Della-Torre E, Milani R, Bozzolo E, Bozzalla-Cassione E, Rovati L, Arcidiacono PG, Partelli S, Falconi M, Ciceri F, et al. Increase of circulating memory B cells after glucocorticoid-induced remission identifies patients at risk of IgG4-related disease relapse. Arthritis Res Ther. 2018;3(1):222. doi:10.1186/s13075-018-1718-5.
  • Tanaka N, Yamada S, Sonohara F, Suenaga M, Hayashi M, Takami H, Niwa Y, Hattori N, Iwata N, Kanda M, et al. Clinical Implications of Lysyl Oxidase-Like Protein 2 Expression in Pancreatic Cancer. Sci Rep. 2018;8(1):9846. doi:10.1038/s41598-018-28253-9.
  • Park JS, Lee JH, Lee YS, Kim JK, Dong SM, Yoon DS. Emerging role of LOXL2 in the promotion of pancreas cancer metastasis. Oncotarget. 2016;7(27):42539–42552. doi:10.18632/oncotarget.9918.
  • Le Calvé B, Griveau A, Vindrieux D, Maréchal R, Wiel C, Svrcek M, Gout J, Azzi L, Payen L, Cros J, et al. Lysyl oxidase family activity promotes resistance of pancreatic ductal adenocarcinoma to chemotherapy by limiting the intratumoral anticancer drug distribution. Oncotarget. 2016;7(22):32100–32112. doi:10.18632/oncotarget.8527.
  • Kagan HM, Li W. Lysyl oxidase: properties. specificity, and biological roles inside and outside of the cell. J Cell Biochem. 2003;88:660–672.
  • Ikenaga N, Peng ZW, Vaid KA, Liu SB, Yoshida S, Sverdlov DY, Mikels-Vigdal A, Smith V, Schuppan D, Popov YV, et al. Selective targeting of lysyl oxidase-like 2 (LOXL2) suppresses hepatic fibrosis progression and accelerates its reversal. Gut. 2017;66(9):1697–1708. doi:10.1136/gutjnl-2016-312473.
  • Santos A, Lagares D. Matrix Stiffness: the Conductor of Organ Fibrosis. Curr Rheumatol Rep. 2018;20(1):2. doi:10.1007/s11926-018-0710-z.
  • Aumiller V, Strobel B, Romeike M, Schuler M, Stierstorfer BE, Kreuz S. Comparative analysis of lysyl oxidase (like) family members in pulmonary fibrosis. Sci Rep. 2017;10;7(1):149. doi:10.1038/s41598-017-00270-0.
  • Millanes-Romero A, Herranz N, Perrera V, Iturbide A, Loubat-Casanovas J, Gil J, Jenuwein T, García de Herreros A, Peiró S. Regulation of heterochromatin transcription by Snail1/LOXL2 during epithelial-to-mesenchymal transition. Mol Cell. 2013;52(5):746–757. doi:10.1016/j.molcel.2013.10.015.
  • Cuevas EP, Eraso P, Mazón MJ, Santos V, Moreno-Bueno G, Cano A, Portillo F. LOXL2 drives epithelial-mesenchymal transition via activation of IRE1-XBP1 signalling pathway. Sci Rep. 2017;23(7):44988. doi:10.1038/srep44988.
  • Zhang D, Li L, Jiang H, Li Q, Wang-Gillam A, Yu J, Head R, Liu J, Ruzinova MB, Lim K-H, et al. Tumor-Stroma IL1β-IRAK4 Feedforward Circuitry Drives Tumor Fibrosis, Chemoresistance, and Poor Prognosis in Pancreatic Cancer. Cancer Res. 2018;78(7):1700–1710. doi:10.1158/0008-5472.CAN-17-1366.
  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674. doi:10.1016/j.cell.2011.02.013.
  • Kleeff J, Korc M, Apte M, La Vecchia C, Johnson CD, Biankin AV, Neale RE, Tempero M, Tuveson DA, Hruban RH, et al. Pancreatic cancer. Nat Rev Dis Primers. 2016;2(1):16022. doi:10.1038/nrdp.2016.22.
  • Ozdemir BC, Pentcheva-Hoang T, Carstens JL, Zheng X, Wu CC, Simpson TR, Laklai H, Sugimoto H, Kahlert C, Novitskiy S, et al. Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell. 2014;25(6):719–734. doi:10.1016/j.ccr.2014.04.005.
  • Ligorio M, Sil S, Malagon-Lopez J, Nieman LT, Misale S, Di Pilato M, Ebright RY, Karabacak MN, Kulkarni AS, Liu A, et al. Stromal Microenvironment Shapes the Intratumoral Architecture of Pancreatic Cancer. Cell. 2019;178(1):160–175. doi:10.1016/j.cell.2019.05.012.
  • Zhang Y, Morgan R, Podack ER, Rosenblatt J. B cell regulation of anti-tumor immune response. Immunol Res. 2013;57(1–3):115–124. doi:10.1007/s12026-013-8472-1.
  • Nelson BH. CD20+B Cells: the Other Tumor-Infiltrating Lymphocytes. J Immunol. 2010;185(9):4977–4982. doi:10.4049/jimmunol.1001323.
  • de Visser KE, Korets LV, Coussens LM. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell. 2005;7(5):411–423. doi:10.1016/j.ccr.2005.04.014.
  • Yuen GJ, Demissie E, Pillai S. B lymphocytes and cancer: a love-hate relationship. Trends Cancer. 2016;2(12):747–757. doi:10.1016/j.trecan.2016.10.010.
  • Affara NI, Ruffell B, Medler TR, Gunderson AJ, Johansson M, Bornstein S, Bergsland E, Steinhoff M, Li Y, Gong Q, et al. B cells regulate macrophage phenotype and response to chemotherapy in squamous carcinomas. Cancer Cell. 2014;25(6):809–821. doi:10.1016/j.ccr.2014.04.026.
  • Gunderson AJ, Kaneda MM, Tsujikawa T, Nguyen AV, Affara NI, Ruffell B, Gorjestani S, Liudahl SM, Truitt M, Olson P, et al. Bruton Tyrosine Kinase-Dependent Immune Cell Cross-talk Drives Pancreas Cancer. Cancer Discov. 2016;6(3):270–285. doi:10.1158/2159-8290.CD-15-0827.
  • Lee KE, Spata M, Bayne LJ, Buza EL, Durham AC, Allman D, Vonderheide RH, Simon MC. Hif1a Deletion Reveals Pro-Neoplastic Function of B Cells in Pancreatic Neoplasia. Cancer Discov. 2016;6(3):256–269. doi:10.1158/2159-8290.CD-15-0822.
  • Pylayeva-Gupta Y, Das S, Handler JS, Hajdu CH, Coffre M, Koralov SB, Bar-Sagi D. IL35-Producing B Cells Promote the Development of Pancreatic Neoplasia. Cancer Discov. 2016;6(3):247–255. doi:10.1158/2159-8290.CD-15-0843.
  • Hosaka K, Yang Y, Seki T, Nakamura M, Andersson P, Rouhi P, Yang X, Jensen L, Lim S, Feng N, et al. Tumour PDGF-BB expression levels determine dual effects of anti-PDGF drugs on vascular remodelling and metastasis. Nat Commun. 2013;4(1):2129. doi:10.1038/ncomms3129.
  • Demoulin JB, Essaghir A. PDGF receptor signaling networks in normal and cancer cells. Cytokine Growth Factor Rev. 2014;25(3):273–283. doi:10.1016/j.cytogfr.2014.03.003.
  • Andrae J, Gallini R, Betsholtz C. Role of platelet-derived growth factors in physiology and medicine. Genes Dev. 2008;22(10):1276–1312. doi:10.1101/gad.1653708.
  • Wynn TA, Ramalingam TR. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med. 2012;18(7):1028–1040. doi:10.1038/nm.2807.
  • Della-Torre E, Bozzalla-Cassione E, Sciorati C, Ruggiero E, Lanzillotta M, Bonfiglio S, Mattoo H, Perugino CA, Bozzolo E, Rovati L, et al. A CD8α- Subset of CD4+ SLAMF7+ Cytotoxic T Cells is Expanded in Patients with IgG4-Related Disease and Decreases following Glucocorticoid Treatment. Arthritis Rheumatol. 2018;70(7):1133–1143. doi:10.1002/art.40469.
  • De Monte L, Wörmann S, Brunetto E, Heltai S, Magliacane G, Reni M, Paganoni AM, Recalde H, Mondino A, Falconi M et al. Basophil Recruitment into Tumor-Draining Lymph Nodes Correlates with Th2 Inflammation and Reduced Survival in Pancreatic Cancer Patients. Cancer Res. 2016 Apr 1;76(7):1792–1803. doi:10.1158/0008-5472.CAN-15-1801-T.
  • De Monte L, Reni M, Tassi E, Clavenna D, Papa I, Recalde H, Braga M, Di Carlo V, Doglioni C, Protti MP, et al. Intratumor T helper type 2 cell infiltrate correlates with cancer-associated fibroblast thymic stromal lymphopoietin production and reduced survival in pancreatic cancer. J Exp Med. 2011;208(3):469–478. doi:10.1084/jem.20101876.
  • Zhang A, Qian Y, Ye Z, Chen H, Xie H, Zhou L, Shen Y, Zheng S. Cancer-associated fibroblasts promote M2 polarization of macrophages in pancreatic ductal adenocarcinoma. Cancer Med. 2017;6(2):463–470. doi:10.1002/cam4.993.
  • Sherry B, Tekamp-Olson P, Gallegos C, Bauer D, Davatelis G, Wolpe SD, Masiarz F, Coit D, Cerami A. Resolution of the two components of macrophage inflammatory protein 1, and cloning and characterization of one of those components, macrophage inflammatory protein 1 beta.. J Exp Med. 1988;168(6):2251–2259. doi:10.1084/jem.168.6.2251.
  • Cocchi F, DeVico AL, Garzino-Demo A, Arya SK, Gallo RC, Lusso P. Identification of RANTES, MIP-1 alpha, and MIP-1 beta as the major HIV-suppressive factors produced by CD8+ T cells. Science. 1995;270(5243):1811–1815. doi:10.1126/science.270.5243.1811.
  • Jose PJ, Griffiths-Johnson DA, Collins PD, Walsh DT, Moqbel R, Totty NF, Truong O, Hsuan JJ, Williams TJ. Eotaxin: a potent eosinophil chemoattractant cytokine detected in a guinea pig model of allergic airways inflammation. J Exp Med. 1994;179(3):881–887. doi:10.1084/jem.179.3.881.
  • Cohen SJ, Alpaugh RK, Palazzo I, Meropol NJ, Rogatko A, Xu Z, Hoffman JP, Weiner LM, Cheng JD. Fibroblast activation protein and its relationship to clinical outcome in pancreatic adenocarcinoma. Pancreas. 2008;37(2):154–158. doi:10.1097/MPA.0b013e31816618ce.
  • Hiepe F, Dörner T, Hauser AE, Hoyer BF, Mei H, Radbruch A. Long-lived autoreactive plasma cells drive persistent autoimmune inflammation. Nat Rev Rheumatol. 2011;7(3):170–178. doi:10.1038/nrrheum.2011.1.
  • Amin MB, Edge S, Greene F, Byrd DR, Brookland RK, Washington MK, Gershenwald JE, Compton CC, Hess KR, Sullivan DC,  et al. AJCC Cancer Staging Manual.Eight Ediction 2016.Springer: Switzerland. ISBN 978-3-319-40617-6.
  • Soloff EV, Zaheer A, Meier J, Zins M, Tamm EP. Staging of pancreatic cancer: resectable, borderline resectable, and unresectable disease. Abdom Radiol (NY). 2018;43(2):301–313. doi:10.1007/s00261-017-1410-2.