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REVIEW

The Role of Podoplanin in the Immune System and Inflammation

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Pages 3561-3572 | Published online: 17 Jun 2022

References

  • Medzhitov R. Origin and physiological roles of inflammation. Nature. 2008;454(7203):428–435. doi:10.1091/mbc.E10-06-0489
  • Quintanilla M, Montero-Montero L, Renart J, Martin-Villar E. Podoplanin in inflammation and cancer. Int J Mol Sci. 2019;20(3):707. doi:10.3390/ijms20030707
  • Ester M-V, Scholl FG, Carlos G, et al. Characterization of human PA2.26 antigen (T1alpha-2, podoplanin), a small membrane mucin induced in oral squamous cell carcinomas. Int J Cancer. 2005;113(6). doi:10.1002/ijc.20656
  • Ozaki Y, Tamura S, Suzuki-Inoue K. New horizon in platelet function: with special reference to a recently-found molecule, CLEC-2. Thromb J. 2016;14(Suppl 1):27. doi:10.1186/s12959-016-0099-8
  • Suzuki-Inoue K, Tsukiji N, Shirai T, Osada M, Inoue O, Ozaki Y. Platelet CLEC-2: roles beyond hemostasis. Semin Thromb Hemost. 2018;44(2):126–134. doi:10.1055/s-0037-1604090
  • Colonna M, Samaridis J, Angman L. Molecular characterization of two novel C-type lectin-like receptors, one of which is selectively expressed in human dendritic cells. Eur J Immunol. 2000;30(2):697–704. doi:10.1002/1521-4141(200002)30:2<697::AID-IMMU697>3.0.CO;2-M
  • Kerrigan AM, Dennehy KM, Mourão-Sá D, et al. CLEC-2 is a phagocytic activation receptor expressed on murine peripheral blood neutrophils. J Immunol. 2009;182(7):4150–4157. doi:10.4049/jimmunol.0802808
  • Acton SE, Astarita JL, Malhotra D, et al. Podoplanin-rich stromal networks induce dendritic cell motility via activation of the C-type lectin receptor CLEC-2. Immunity. 2012;37(2):276–289. doi:10.1016/j.immuni.2012.05.022
  • Suzuki-Inoue K, Fuller G, García A, et al. A novel Syk-dependent mechanism of platelet activation by the C-type lectin receptor CLEC-2. Blood. 2006;107(2):542–549. doi:10.1182/blood-2005-05-1994
  • Fuller G, Williams J, Tomlinson M, et al. The C-type lectin receptors CLEC-2 and Dectin-1, but not DC-SIGN, signal via a novel YXXL-dependent signaling cascade. J Biol Chem. 2007;282(17):12397–12409. doi:10.1074/jbc.M609558200
  • Suzuki-Inoue K, Inoue O, Ozaki YJ. Novel platelet activation receptor CLEC-2: from discovery to prospects. J Thromb Haemost. 2011;9:44–55. doi:10.1111/j.1538-7836.2011.04335.x
  • Martín-Villar E, Megías D, Castel S, Yurrita M, Vilaró S, Quintanilla MJ. Podoplanin binds ERM proteins to activate RhoA and promote epithelial-mesenchymal transition. J Cell Sci. 2006;119(21):4541–4553. doi:10.1242/jcs.03218
  • Astarita J, Acton S, Turley SJ. Podoplanin: emerging functions in development, the immune system, and cancer. Front Immunol. 2012;3:283. doi:10.3389/fimmu.2012.00283
  • Jaime R, Patricia C-R, Beatriz F-M, et al. New insights into the role of podoplanin in epithelial-mesenchymal transition. Int Rev Cell Mol Biol. 2015;317. doi:10.1016/bs.ircmb.2015.01.009
  • Harini K, Julie R, Tomoyuki M, et al. Podoplanin: an emerging cancer biomarker and therapeutic target. Cancer Sci. 2018;109(5). doi:10.1111/cas.13580
  • Herzog B, Fu J, Wilson S, et al. Podoplanin maintains high endothelial venule integrity by interacting with platelet CLEC-2. Nature. 2013;502(7469):105–109. doi:10.1038/nature12501
  • Acton S, Astarita J, Malhotra D, et al. Podoplanin-rich stromal networks induce dendritic cell motility via activation of the C-type lectin receptor CLEC-2. Immunity. 2012;37(2):276–289. doi:10.1016/j.immuni.2012.05.022
  • Hur J, Jang JH, Oh I-Y, et al. Human podoplanin-positive monocytes and platelets enhance lymphangiogenesis through the activation of the podoplanin/CLEC-2 axis. Mol Ther. 2014;22(8):1518–1529. doi:10.1038/mt.2014.61
  • Tal O, Lim H, Gurevich I, et al. DC mobilization from the skin requires docking to immobilized CCL21 on lymphatic endothelium and intralymphatic crawling. J Exp Med. 2011;208(10):2141–2153. doi:10.1084/jem.20102392
  • Fuertbauer E, Zaujec J, Uhrin P, et al. Thymic medullar conduits-associated podoplanin promotes natural regulatory T cells. Immunol Lett. 2013;154(1–2):31–41. doi:10.1016/j.imlet.2013.07.007
  • Chen WS, Cao Z, Sugaya S, et al. Pathological lymphangiogenesis is modulated by galectin-8-dependent crosstalk between podoplanin and integrin-associated VEGFR-3. Nat Commun. 2016;7(1):11302. doi:10.1038/ncomms11302
  • Youya N, Shigeo S, Mikihiko N, et al. Tetraspanin family member CD9 inhibits Aggrus/podoplanin-induced platelet aggregation and suppresses pulmonary metastasis. Blood. 2008;112(5). doi:10.1182/blood-2007-11-124693
  • Ester M-V, Beatriz F-M, Maddy P, et al. Podoplanin associates with CD44 to promote directional cell migration. Mol Biol Cell. 2010;21:24. doi:10.1091/mbc.E10-06-0489
  • Karin M, Clevers H. Reparative inflammation takes charge of tissue regeneration. Nature. 2016;529(7586):307–315. doi:10.1038/nature17039
  • Serhan CN, Savill J. Resolution of inflammation: the beginning programs the end. Nat Immunol. 2005;6(12):1191–1197. doi:10.1038/ni1276
  • Bonilla FA, Oettgen HC. Adaptive immunity. J Allergy Clin Immunol. 2010;125(2 Suppl 2):S33–S40. doi:10.1016/j.jaci.2009.09.017
  • Gray KJ, Gibbs JE. Adaptive immunity, chronic inflammation and the clock. Semin Immunopathol. 2022;44(2):209–224. doi:10.1007/s00281-022-00919-7
  • Alitalo K, Tammela T, Petrova TV. Lymphangiogenesis in development and human disease. Nature. 2005;438(7070):946–953. doi:10.1038/nature04480
  • Peters A, Pitcher L, Sullivan J, et al. Th17 cells induce ectopic lymphoid follicles in central nervous system tissue inflammation. Immunity. 2011;35(6):986–996. doi:10.1016/j.immuni.2011.10.015
  • Miyamoto Y, Uga H, Tanaka S, et al. Podoplanin is an inflammatory protein upregulated in Th17 cells in SKG arthritic joints. Mol Immunol. 2013;54(2):199–207. doi:10.1016/j.molimm.2012.11.013
  • Kerrigan AM, Navarro‐nuñez L, Pyz E. Podoplanin-expressing inflammatory macrophages activate murine platelets via CLEC-2. J Thromb Haemost. 2012;10(3):484–486. doi:10.1111/j.1538-7836.2011.04614.x
  • Wynn T, Chawla A, Pollard JJN. Macrophage biology in development, homeostasis and disease. Nature. 2013;496(7446):445–455. doi:10.1038/nature12034
  • Hou T, Bystrom J, Sherlock J, et al. A distinct subset of podoplanin (gp38) expressing F4/80+ macrophages mediate phagocytosis and are induced following zymosan peritonitis. FEBS Lett. 2010;584(18):3955–3961. doi:10.1016/j.febslet.2010.07.053
  • Lawrence T, Natoli GJ. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Immunol. 2011;11(11):750–761. doi:10.1038/nri3088
  • Fei M, Wang H, Zhou M, Deng C, Zhang L, Han Y. Podoplanin influences the inflammatory phenotypes and mobility of microglia in traumatic brain injury. Biochem Biophys Res Commun. 2020;523(2):361–367. doi:10.1016/j.bbrc.2019.12.003
  • Rayes J, Lax S, Wichaiyo S, et al. The podoplanin-CLEC-2 axis inhibits inflammation in sepsis. Nat Commun. 2017;8(1):2239. doi:10.1038/s41467-017-02402-6
  • Bourne J, Beristain-Covarrubias N, Zuidscherwoude M, et al. CLEC-2 prevents accumulation and retention of inflammatory macrophages during murine peritonitis. Front Immunol. 2021;12:693974. doi:10.3389/fimmu.2021.693974
  • Krishnan H, Ochoa-Alvarez JA, Shen Y, et al. Serines in the intracellular tail of Podoplanin (PDPN) regulate cell motility. J Biol Chem. 2013;288(17). doi:10.1074/jbc.C112.446823
  • Cheok Y, Tan G, Fernandez K, et al. Podoplanin drives motility of active macrophage via regulating Filamin C during Helicobacter pylori infection. Front Immunol. 2021;12:702156. doi:10.3389/fimmu.2021.702156
  • Stossel T, Condeelis J, Cooley L, et al. Filamins as integrators of cell mechanics and signalling. Nat Rev Mol Cell Biol. 2001;2(2):138–145. doi:10.1038/35052082
  • Peters A, Pitcher LA, Sullivan JM, et al. Th17 cells induce ectopic lymphoid follicles in central nervous system tissue inflammation. Immunity. 2011;35(6):986–996. doi:10.1016/j.immuni.2011.10.015
  • Yasuda K, Takeuchi Y, Hirota K. The pathogenicity of Th17 cells in autoimmune diseases. Semin Immunopathol. 2019;41(3):283–297. doi:10.1007/s00281-019-00733-8
  • Nylander AN, Ponath GD, Axisa PP, et al. Podoplanin is a negative regulator of Th17 inflammation. JCI Insight. 2017;2(17). doi:10.1172/jci.insight.92321
  • Lee Y, Awasthi A, Yosef N, et al. Induction and molecular signature of pathogenic TH17 cells. Nat Immunol. 2012;13(10):991–999. doi:10.1038/ni.2416
  • Joller N, Peters A, Anderson A, Kuchroo VJ. Immune checkpoints in central nervous system autoimmunity. Immunol Rev. 2012;248(1):122–139. doi:10.1111/j.1600-065X.2012.01136.x
  • Peters A, Burkett P, Sobel R, et al. Podoplanin negatively regulates CD4+ effector T cell responses. J Clin Invest. 2015;125(1):129–140. doi:10.1172/JCI74685
  • Chihara N, Madi A, Kondo T, et al. Induction and transcriptional regulation of the co-inhibitory gene module in T cells. Nature. 2018;558(7710):454–459. doi:10.1038/s41586-018-0206-z
  • Li J, Huston G, Swain SL. IL-7 promotes the transition of CD4 effectors to persistent memory cells. J Exp Med. 2003;198(12):1807–1815. doi:10.1084/jem.20030725
  • Malhotra D, Fletcher AL, Turley SJ. Stromal and hematopoietic cells in secondary lymphoid organs: partners in immunity. Immunol Rev. 2013;251(1):160–176. doi:10.1111/imr.12023
  • Malhotra D, Fletcher A, Astarita J, et al. Transcriptional profiling of stroma from inflamed and resting lymph nodes defines immunological hallmarks. Nat Immunol. 2012;13(5):499–510. doi:10.1038/ni.2262
  • Osada M, Inoue O, Ding G, et al. Platelet activation receptor CLEC-2 regulates blood/lymphatic vessel separation by inhibiting proliferation, migration, and tube formation of lymphatic endothelial cells. J Biol Chem. 2012;287(26):22241–22252. doi:10.1074/jbc.M111.329987
  • Navarro A, Perez RE, Rezaiekhaligh M, Mabry SM, Ekekezie II. T1alpha/podoplanin is essential for capillary morphogenesis in lymphatic endothelial cells. Am J Physiol Lung Cell Mol Physiol. 2008;295(4):L543–L551. doi:10.1152/ajplung.90262.2008
  • Navarro A, Perez RE, Rezaiekhaligh MH, Mabry SM, Ekekezie II. Polarized migration of lymphatic endothelial cells is critically dependent on podoplanin regulation of Cdc42. Am J Physiol Lung Cell Mol Physiol. 2011;300(1):L32–42. doi:10.1152/ajplung.00171.2010
  • Kasinath V, Yilmam O, Uehara M, et al. Activation of fibroblastic reticular cells in kidney lymph node during crescentic glomerulonephritis. Kidney Int. 2019;95(2):310–320. doi:10.1016/j.kint.2018.08.040
  • Astarita J, Cremasco V, Fu J, et al. The CLEC-2-podoplanin axis controls the contractility of fibroblastic reticular cells and lymph node microarchitecture. Nat Immunol. 2015;16(1):75–84. doi:10.1038/ni.3035
  • Acton S, Farrugia A, Astarita J, et al. Dendritic cells control fibroblastic reticular network tension and lymph node expansion. Nature. 2014;514(7523):498–502. doi:10.1038/nature13814
  • Kushal K, Moises F-A, Bechberger JF, et al. Podoplanin: a marker for reactive gliosis in gliomas and brain injury. J Neuropathol Exp Neurol. 2015;74(1). doi:10.1097/NEN.0000000000000150
  • Song Y, Shen J, Lin Y, et al. Up-regulation of podoplanin involves in neuronal apoptosis in LPS-induced neuroinflammation. Cell Mol Neurobiol. 2014;34(6):839–849. doi:10.1007/s10571-014-0060-y
  • Lax S, Rayes J, Wichaiyo S, et al. Platelet CLEC-2 protects against lung injury via effects of its ligand podoplanin on inflammatory alveolar macrophages in the mouse. Am J Physiol Lung Cell Mol Physiol. 2017;313(6):L1016–L1029. doi:10.1152/ajplung.00023.2017
  • Dean RA, Cox JH, Bellac CL, et al. Macrophage-specific metalloelastase (MMP-12) truncates and inactivates ELR+ CXC chemokines and generates CCL2, −7, −8, and −13 antagonists: potential role of the macrophage in terminating polymorphonuclear leukocyte influx. Blood. 2008;112(8). doi:10.1182/blood-2007-12-129080
  • Eltzschig HK, Eckle T. Ischemia and reperfusion–from mechanism to translation. Nat Med. 2011;17(11):1391–1401. doi:10.1038/nm.2507
  • Meng D, Ma X, Li H, et al. A role of the podoplanin-CLEC-2 axis in promoting inflammatory response after ischemic stroke in mice. Neurotox Res. 2021;39(2):477–488. doi:10.1007/s12640-020-00295-w
  • Kasinath V, Yilmam O, Uehara M, et al. Urine podoplanin heralds the onset of ischemia-reperfusion injury of the kidney. Am J Physiol Renal Physiol. 2019;316(5):F957–F965. doi:10.1152/ajprenal.00538.2018
  • Hitchcock J, Cook C, Bobat S, et al. Inflammation drives thrombosis after Salmonella infection via CLEC-2 on platelets. J Clin Invest. 2015;125(12):4429–4446. doi:10.1172/JCI79070
  • Xie Z, Shao B, Hoover C, et al. Monocyte upregulation of podoplanin during early sepsis induces complement inhibitor release to protect liver function. JCI Insight. 2020;5(13). doi:10.1172/jci.insight.134749
  • Miossec P, Korn T, Kuchroo VK. Interleukin-17 and type 17 helper T cells. N Engl J Med. 2009;361(9):888–898. doi:10.1056/NEJMra0707449
  • Miossec P, Kolls JK. Targeting IL-17 and TH17 cells in chronic inflammation. Nat Rev Drug Discov. 2012;11(10):763–776. doi:10.1038/nrd3794
  • Noack M, Ndongo-Thiam N, Miossec P. Interaction among activated lymphocytes and mesenchymal cells through podoplanin is critical for a high IL-17 secretion. Arthritis Res Ther. 2016;18(1):148. doi:10.1186/s13075-016-1046-6
  • Weyand C, Kurtin P, Goronzy J. Ectopic lymphoid organogenesis: a fast track for autoimmunity. Am J Pathol. 2001;159(3):787–793. doi:10.1016/S0002-9440(10)61751-8
  • Jones GW, Bombardieri M, Greenhill CJ, et al. Interleukin-27 inhibits ectopic lymphoid-like structure development in early inflammatory arthritis. J Exp Med. 2015;212(11):1793–1802. doi:10.1084/jem.20132307
  • Takakubo Y, Oki H, Naganuma Y, et al. Distribution of podoplanin in synovial tissues in rheumatoid arthritis patients using biologic or conventional disease-modifying anti-rheumatic drugs. Curr Rheumatol Rev. 2017;13(1):72–78. doi:10.2174/1573397112666160331143607
  • Bartok B, Firestein GS. Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol Rev. 2010;233(1):233–255. doi:10.1111/j.0105-2896.2009.00859.x
  • Tolboom TCA, van der Helm-Van Mil AHM, Nelissen RG, Breedveld FC, Toes REM, Huizinga TWJ. Invasiveness of fibroblast-like synoviocytes is an individual patient characteristic associated with the rate of joint destruction in patients with rheumatoid arthritis. Arthritis Rheum. 2005;52(7):1999–2002. doi:10.1002/art.21118
  • Huber LC, Distler O, Tarner I, Gay RE, Gay S, Pap T. Synovial fibroblasts: key players in rheumatoid arthritis. Rheumatology. 2006;45(6):669–675. doi:10.1093/rheumatology/kel065
  • Baier A, Meineckel I, Gay S, Pap T. Apoptosis in rheumatoid arthritis. Curr Opin Rheumatol. 2003;15(3):274–279. doi:10.1097/00002281-200305000-00015
  • Karouzakis E, Gay RE, Gay S, Neidhart M. Epigenetic control in rheumatoid arthritis synovial fibroblasts. Nat Rev Rheumatol. 2009;5(5):266–272. doi:10.1038/nrrheum.2009.55
  • Martín-Villar E, Scholl FG, Gamallo C, et al. Characterization of human PA2.26 antigen (T1alpha-2, podoplanin), a small membrane mucin induced in oral squamous cell carcinomas. Int J Cancer. 2005;113(6):899–910. doi:10.1002/ijc.20656
  • Wicki A, Lehembre F, Wick N, Hantusch B, Kerjaschki D, Christofori G. Tumor invasion in the absence of epithelial-mesenchymal transition: podoplanin-mediated remodeling of the actin cytoskeleton. Cancer Cell. 2006;9(4):261–272. doi:10.1016/j.ccr.2006.03.010
  • Wicki A, Christofori G. The potential role of podoplanin in tumour invasion. Br J Cancer. 2007;96(1):1–5. doi:10.1038/sj.bjc.6603518
  • Ekwall A, Eisler T, Anderberg C, et al. The tumour-associated glycoprotein podoplanin is expressed in fibroblast-like synoviocytes of the hyperplastic synovial lining layer in rheumatoid arthritis. Arthritis Res Ther. 2011;13(2):R40. doi:10.1186/ar3274
  • Ekwall A-KH, Eisler T, Anderberg C, et al. The tumour-associated glycoprotein podoplanin is expressed in fibroblast-like synoviocytes of the hyperplastic synovial lining layer in rheumatoid arthritis. Arthritis Res Ther. 2011;13(2):R40. doi:10.1186/ar3274
  • Mizoguchi F, Slowikowski K, Wei K, et al. Functionally distinct disease-associated fibroblast subsets in rheumatoid arthritis. Nat Commun. 2018;9(1):789. doi:10.1038/s41467-018-02892-y
  • Croft A, Naylor A, Marshall J, et al. Rheumatoid synovial fibroblasts differentiate into distinct subsets in the presence of cytokines and cartilage. Arthritis Res Ther. 2016;18(1):270. doi:10.1186/s13075-016-1156-1
  • Tammela T, Alitalo K. Lymphangiogenesis: molecular mechanisms and future promise. Cell. 2010;140(4):460–476. doi:10.1016/j.cell.2010.01.045
  • D’Alessio S, Correale C, Tacconi C, et al. VEGF-C-dependent stimulation of lymphatic function ameliorates experimental inflammatory bowel disease. J Clin Invest. 2014;124(9):3863–3878. doi:10.1172/JCI72189
  • Schacht V, Ramirez MI, Hong Y-K, et al. T1alpha/podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema. EMBO J. 2003;22(14):3546–3556. doi:10.1093/emboj/cdg342
  • Fu J, Gerhardt H, McDaniel JM, et al. Endothelial cell O-glycan deficiency causes blood/lymphatic misconnections and consequent fatty liver disease in mice. J Clin Invest. 2008;118(11):3725–3737. doi:10.1172/JCI36077
  • Wick N, Haluza D, Gurnhofer E, et al. Lymphatic precollectors contain a novel, specialized subpopulation of podoplanin low, CCL27-expressing lymphatic endothelial cells. Am J Pathol. 2008;173(4):1202–1209. doi:10.2353/ajpath.2008.080101
  • Kang J, Yoo J, Lee S, et al. An exquisite cross-control mechanism among endothelial cell fate regulators directs the plasticity and heterogeneity of lymphatic endothelial cells. Blood. 2010;116(1):140–150. doi:10.1182/blood-2009-11-252270
  • Cueni LN, Detmar M. Galectin-8 interacts with podoplanin and modulates lymphatic endothelial cell functions. Exp Cell Res. 2009;315(10):10. doi:10.1016/j.yexcr.2009.02.021
  • Salven P, Mustjoki S, Alitalo R, Alitalo K, Rafii SJB. VEGFR-3 and CD133 identify a population of CD34+ lymphatic/vascular endothelial precursor cells. Blood. 2003;101(1):168–172. doi:10.1182/blood-2002-03-0755
  • Lee J, Park C, Cho Y, et al. Podoplanin-expressing cells derived from bone marrow play a crucial role in postnatal lymphatic neovascularization. Circulation. 2010;122(14):1413–1425. doi:10.1161/CIRCULATIONAHA.110.941468
  • Changming W, Xin L, Hua T, et al. Monocytes can be induced to express lymphatic phenotypes. Lymphology. 2011;44(2).
  • Maruyama K, Nakazawa T, Cursiefen C, et al. The maintenance of lymphatic vessels in the cornea is dependent on the presence of macrophages. Invest Ophthalmol Vis Sci. 2012;53(6):3145–3153. doi:10.1167/iovs.11-8010
  • Kazuichi M, Masaaki I, Claus C, et al. Inflammation-induced lymphangiogenesis in the cornea arises from CD11b-positive macrophages. J Clin Invest. 2005;115(9). doi:10.1172/JCI23874
  • Maruyama K, Asai J, Ii M, Thorne T, Losordo D, D’Amore P. Decreased macrophage number and activation lead to reduced lymphatic vessel formation and contribute to impaired diabetic wound healing. Am J Pathol. 2007;170(4):1178–1191. doi:10.2353/ajpath.2007.060018
  • Cimini M, Garikipati VNS, de Lucia C, et al. Podoplanin neutralization improves cardiac remodeling and function after acute myocardial infarction. JCI Insight. 2019;5. doi:10.1172/jci.insight.126967
  • Cimini M, Kishore R. Role of podoplanin-positive cells in cardiac fibrosis and angiogenesis after ischemia. Front Physiol. 2021;12:667278. doi:10.3389/fphys.2021.667278
  • Abe S, Morita Y, Kaneko MK, et al. A novel targeting therapy of malignant mesothelioma using anti-podoplanin antibody. J Immunol. 2013;190(12):6239–6249. doi:10.4049/jimmunol.1300448
  • Chandramohan V, Bao X, Kato Kaneko M, et al. Recombinant anti-podoplanin (NZ-1) immunotoxin for the treatment of malignant brain tumors. Int J Cancer. 2013;132(10):2339–2348. doi:10.1002/ijc.27919
  • Shiina S, Ohno M, Ohka F, et al. CAR T cells targeting podoplanin reduce orthotopic glioblastomas in mouse brains. Cancer Immunol Res. 2016;4(3):259–268. doi:10.1158/2326-6066.CIR-15-0060
  • Kaneko MK, Nakamura T, Kunita A, et al. ChLpMab-23: cancer-specific human-mouse chimeric anti-podoplanin antibody exhibits antitumor activity via antibody-dependent cellular cytotoxicity. Monoclon Antib Immunodiagn Immunother. 2017;36(3):104–112. doi:10.1089/mab.2017.0014
  • Hasan SS, Ashraf GM, Banu N. Galectins - potential targets for cancer therapy. Cancer Lett. 2007;253(1):25–33. doi:10.1016/j.canlet.2006.11.030
  • Pusztai A, Bardocz S, Ewen SWB. Uses of plant lectins in bioscience and biomedicine. Front Biosci. 2008;13(13):1130–1140. doi:10.2741/2750
  • Scholl F, Gamallo C, Vilaró S, Quintanilla MJ. Identification of PA2.26 antigen as a novel cell-surface mucin-type glycoprotein that induces plasma membrane extensions and increased motility in keratinocytes. J Cell Sci. 1999;112(24):4601–4613. doi:10.1242/jcs.112.24.4601
  • Geisler C, Jarvis DL. Effective glycoanalysis with Maackia amurensis lectins requires a clear understanding of their binding specificities. Glycobiology. 2011;21(8):988–993. doi:10.1093/glycob/cwr080
  • Wang WC, Cummings RD. The immobilized leukoagglutinin from the seeds of Maackia amurensis binds with high affinity to complex-type Asn-linked oligosaccharides containing terminal sialic acid-linked alpha-2,3 to penultimate galactose residues. J Biol Chem. 1988;263(10):4576–4585. doi:10.1016/S0021-9258(18)68821-0
  • Imberty A, Gautier C, Lescar J, Pérez S, Wyns L, Loris R. An unusual carbohydrate binding site revealed by the structures of two Maackia amurensis lectins complexed with sialic acid-containing oligosaccharides. J Biol Chem. 2000;275(23):17541–17548. doi:10.1074/jbc.M000560200
  • Carpintero-Fernandez P, Varela-Eirin M, Lacetera A, et al. New therapeutic strategies for osteoarthritis by targeting sialic acid receptors. Biomolecules. 2020;10(4):637. doi:10.3390/biom10040637