How Tim proteins differentially exploit membrane features to attain robust target sensitivity

Kerr, Daniel; Gong, Zhiliang; Suwatthee, Tiffany; Luoma, Adrienne; Roy, Sobhan; Scarpaci, Renee; Hwang, Hyeondo Luke; Henderson, J. Michael; Cao, Kathleen D.; Bu, Wei; Lin, Binhua; Tietjen, Gregory T.; Steck, Theodore L.; Adams, Erin J.; Lee, Ka Yee C.

doi:10.1016/j.bpj.2021.09.016

How Tim proteins differentially exploit membrane features to attain robust target sensitivity

Journal Article · 01 November 2021 · Biophys. J.

DOI:https://doi.org/10.1016/j.bpj.2021.09.016· OSTI ID:1841215

Kerr, Daniel; Gong, Zhiliang; Suwatthee, Tiffany; Luoma, Adrienne; Roy, Sobhan; Scarpaci, Renee; Hwang, Hyeondo Luke; Henderson, J. Michael; Cao, Kathleen D.; Bu, Wei; Lin, Binhua; Tietjen, Gregory T.; Steck, Theodore L.; Adams, Erin J.; Lee, Ka Yee C.

Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: DOE - Office Of Science; National Science Foundation (NSF)

OSTI ID:: 1841215

Journal Information:: Biophys. J., Vol. 120, Issue (21)

Country of Publication:: United States

Language:: ENGLISH

References (80)

The interactions of peripheral membrane proteins with biological membranes Whited, A. M.; Johs, A. Chemistry and Physics of Lipids, Vol. 192 https://doi.org/10.1016/j.chemphyslip.2015.07.015	journal	November 2015
Binding of Peripheral Proteins to Mixed Lipid Membranes: Effect of Lipid Demixing upon Binding Heimburg, Thomas; Angerstein, Brigitta; Marsh, Derek Biophysical Journal, Vol. 76, Issue 5 https://doi.org/10.1016/S0006-3495(99)77410-2	journal	May 1999
Lipid dynamics and peripheral interactions of proteins with membrane surfaces Kinnunen, Paavo K. J.; Kõiv, Anu; Lehtonen, Jukka Y. A. Chemistry and Physics of Lipids, Vol. 73, Issue 1-2 https://doi.org/10.1016/0009-3084(94)90181-3	journal	September 1994
A novel type of allosteric regulation: Functional cooperativity in monomeric proteins Denisov, Ilia G.; Sligar, Stephen G. Archives of Biochemistry and Biophysics, Vol. 519, Issue 2 https://doi.org/10.1016/j.abb.2011.12.017	journal	March 2012
TIM genes: a family of cell surface phosphatidylserine receptors that regulate innate and adaptive immunity: TIM genes: a family of PtdSer receptors Freeman, Gordon J.; Casasnovas, Jose M.; Umetsu, Dale T. Immunological Reviews, Vol. 235, Issue 1 https://doi.org/10.1111/j.0105-2896.2010.00903.x	journal	April 2010
Lag-3, Tim-3, and TIGIT: Co-inhibitory Receptors with Specialized Functions in Immune Regulation Anderson, Ana C.; Joller, Nicole; Kuchroo, Vijay K. Immunity, Vol. 44, Issue 5 https://doi.org/10.1016/j.immuni.2016.05.001	journal	May 2016
TIM-3 Regulates Distinct Functions in Macrophages Ocaña-Guzman, Ranferi; Torre-Bouscoulet, Luis; Sada-Ovalle, Isabel Frontiers in Immunology, Vol. 7 https://doi.org/10.3389/fimmu.2016.00229	journal	June 2016
Regulation of T cell trafficking by the T cell immunoglobulin and mucin domain 1 glycoprotein Angiari, Stefano; Constantin, Gabriela Trends in Molecular Medicine, Vol. 20, Issue 12 https://doi.org/10.1016/j.molmed.2014.10.003	journal	December 2014
The phosphatidylserine receptor TIM4 utilizes integrins as coreceptors to effect phagocytosis Flannagan, Ronald S.; Canton, Johnathan; Furuya, Wendy Molecular Biology of the Cell, Vol. 25, Issue 9 https://doi.org/10.1091/mbc.e13-04-0212	journal	May 2014
Soluble T Cell Immunoglobulin Mucin Domain 3 Is Shed from CD8 ⁺ T Cells by the Sheddase ADAM10, Is Increased in Plasma during Untreated HIV Infection, and Correlates with HIV Disease Progression Clayton, Kiera L.; Douglas-Vail, Matthew B.; Rahman, A. K. M. Nur-ur Journal of Virology, Vol. 89, Issue 7 https://doi.org/10.1128/JVI.00006-15	journal	April 2015
Soluble T cell immunoglobulin and mucin domain (TIM)-1 and -4 generated by A Disintegrin And Metalloprotease (ADAM)-10 and -17 bind to phosphatidylserine Schweigert, Olga; Dewitz, Christin; Möller-Hackbarth, Katja Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1843, Issue 2 https://doi.org/10.1016/j.bbamcr.2013.11.014	journal	February 2014
TIM-1 and TIM-4 Glycoproteins Bind Phosphatidylserine and Mediate Uptake of Apoptotic Cells Kobayashi, Norimoto; Karisola, Piia; Peña-Cruz, Victor Immunity, Vol. 27, Issue 6 https://doi.org/10.1016/j.immuni.2007.11.011	journal	December 2007
Tim-3 mediates phagocytosis of apoptotic cells and cross-presentation Nakayama, Masafumi; Akiba, Hisaya; Takeda, Kazuyoshi Blood, Vol. 113, Issue 16 https://doi.org/10.1182/blood-2008-10-185884	journal	April 2009
Molecular mechanism for differential recognition of membrane phosphatidylserine by the immune regulatory receptor Tim4 Tietjen, G. T.; Gong, Z.; Chen, C. -H. Proceedings of the National Academy of Sciences, Vol. 111, Issue 15 https://doi.org/10.1073/pnas.1320174111	journal	March 2014
Structures of T Cell Immunoglobulin Mucin Protein 4 Show a Metal-Ion-Dependent Ligand Binding Site where Phosphatidylserine Binds Santiago, César; Ballesteros, Angela; Martínez-Muñoz, Laura Immunity, Vol. 27, Issue 6 https://doi.org/10.1016/j.immuni.2007.11.008	journal	December 2007
Diverse roles of TIM4 in immune activation: implications for alloimmunity McGrath, Martina M. Current Opinion in Organ Transplantation, Vol. 23, Issue 1 https://doi.org/10.1097/MOT.0000000000000487	journal	January 2018
TIM‐3 and CEACAM1 do not interact in cis and in trans De Sousa Linhares, Annika; Kellner, Florian; Jutz, Sabrina European Journal of Immunology, Vol. 50, Issue 8 https://doi.org/10.1002/eji.201948400	journal	April 2020
TIM-3 Does Not Act as a Receptor for Galectin-9 Leitner, Judith; Rieger, Armin; Pickl, Winfried F. PLoS Pathogens, Vol. 9, Issue 3 https://doi.org/10.1371/journal.ppat.1003253	journal	March 2013
The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity Zhu, Chen; Anderson, Ana C.; Schubart, Anna Nature Immunology, Vol. 6, Issue 12 https://doi.org/10.1038/ni1271	journal	November 2005
A TIM-3/Gal-9 Autocrine Stimulatory Loop Drives Self-Renewal of Human Myeloid Leukemia Stem Cells and Leukemic Progression Kikushige, Yoshikane; Miyamoto, Toshihiro; Yuda, Junichiro Cell Stem Cell, Vol. 17, Issue 3 https://doi.org/10.1016/j.stem.2015.07.011	journal	September 2015
Evidence for carbohydrate recognition and homotypic and heterotypic binding by the TIM family Wilker, P. R.; Sedy, J. R.; Grigura, V. International Immunology, Vol. 19, Issue 6 https://doi.org/10.1093/intimm/dxm044	journal	May 2007
Tumor-infiltrating DCs suppress nucleic acid–mediated innate immune responses through interactions between the receptor TIM-3 and the alarmin HMGB1 Chiba, Shigeki; Baghdadi, Muhammad; Akiba, Hisaya Nature Immunology, Vol. 13, Issue 9 https://doi.org/10.1038/ni.2376	journal	July 2012
CEACAM1 regulates TIM-3-mediated tolerance and exhaustion Huang, Yu-Hwa; Zhu, Chen; Kondo, Yasuyuki Nature, Vol. 517, Issue 7534 https://doi.org/10.1038/nature13848	journal	October 2014
The role of phosphatidylserine recognition receptors in multiple biological functions Naeini, Mehri Bemani; Bianconi, Vanessa; Pirro, Matteo Cellular & Molecular Biology Letters, Vol. 25, Issue 1 https://doi.org/10.1186/s11658-020-00214-z	journal	March 2020
T Cell Immunoglobulin Mucin-3 Crystal Structure Reveals a Galectin-9-Independent Ligand-Binding Surface Cao, Erhu; Zang, Xingxing; Ramagopal, Udupi A. Immunity, Vol. 26, Issue 3 https://doi.org/10.1016/j.immuni.2007.01.016	journal	March 2007
T Cell/Transmembrane, Ig, and Mucin-3 Allelic Variants Differentially Recognize Phosphatidylserine and Mediate Phagocytosis of Apoptotic Cells DeKruyff, Rosemarie H.; Bu, Xia; Ballesteros, Angela The Journal of Immunology, Vol. 184, Issue 4 https://doi.org/10.4049/jimmunol.0903059	journal	January 2010
Structures of T Cell Immunoglobulin Mucin Receptors 1 and 2 Reveal Mechanisms for Regulation of Immune Responses by the TIM Receptor Family Santiago, César; Ballesteros, Angela; Tami, Cecilia Immunity, Vol. 26, Issue 3 https://doi.org/10.1016/j.immuni.2007.01.014	journal	March 2007
Phosphatidic acid- and phosphatidylserine-binding proteins Stace, C.; Ktistakis, N. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1761, Issue 8 https://doi.org/10.1016/j.bbalip.2006.03.006	journal	August 2006
Getting to the Outer Leaflet: Physiology of Phosphatidylserine Exposure at the Plasma Membrane Bevers, Edouard M.; Williamson, Patrick L. Physiological Reviews, Vol. 96, Issue 2 https://doi.org/10.1152/physrev.00020.2015	journal	April 2016
Revisiting transbilayer distribution of lipids in the plasma membrane Murate, Motohide; Kobayashi, Toshihide Chemistry and Physics of Lipids, Vol. 194 https://doi.org/10.1016/j.chemphyslip.2015.08.009	journal	January 2016
Constitutive exposure of phosphatidylserine on viable cells Segawa, K.; Suzuki, J.; Nagata, S. Proceedings of the National Academy of Sciences, Vol. 108, Issue 48 https://doi.org/10.1073/pnas.1114799108	journal	November 2011
Phospholipid Scramblase Activation Pathways in Lymphocytes Williamson, Patrick; Christie, Allison; Kohlin, Torvald Biochemistry, Vol. 40, Issue 27 https://doi.org/10.1021/bi001929z	journal	June 2001
Protein–Phospholipid Interaction Motifs: A Focus on Phosphatidic Acid Tanguy, Emeline; Kassas, Nawal; Vitale, Nicolas Biomolecules, Vol. 8, Issue 2 https://doi.org/10.3390/biom8020020	journal	April 2018
Coupling X-Ray Reflectivity and In Silico Binding to Yield Dynamics of Membrane Recognition by Tim1 Tietjen, Gregory T.; Baylon, Javier L.; Kerr, Daniel Biophysical Journal, Vol. 113, Issue 7 https://doi.org/10.1016/j.bpj.2017.08.003	journal	October 2017
Blockade of Tim-3 binding to phosphatidylserine and CEACAM1 is a shared feature of anti-Tim-3 antibodies that have functional efficacy Sabatos-Peyton, Catherine A.; Nevin, James; Brock, Ansgar OncoImmunology, Vol. 7, Issue 2 https://doi.org/10.1080/2162402X.2017.1385690	journal	October 2017
The 2.5 Å Structure of CD1c in Complex with a Mycobacterial Lipid Reveals an Open Groove Ideally Suited for Diverse Antigen Presentation Scharf, Louise; Li, Nan-Sheng; Hawk, Andrew J. Immunity, Vol. 33, Issue 6 https://doi.org/10.1016/j.immuni.2010.11.026	journal	December 2010
Small-volume extrusion apparatus for preparation of large, unilamellar vesicles MacDonald, Robert C.; MacDonald, Ruby I.; Menco, Bert Ph. M. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1061, Issue 2 https://doi.org/10.1016/0005-2736(91)90295-J	journal	January 1991
Quantitative Analysis of Protein-Lipid Interactions Using Tryptophan Fluorescence Kraft, C. A.; Garrido, J. L.; Leiva-Vega, L. Science Signaling, Vol. 2, Issue 99 https://doi.org/10.1126/scisignal.299pl4	journal	November 2009
Membrane Fluidity Is a Key Modulator of Membrane Binding, Insertion, and Activity of 5-Lipoxygenase Pande, Abhay H.; Qin, Shan; Tatulian, Suren A. Biophysical Journal, Vol. 88, Issue 6 https://doi.org/10.1529/biophysj.104.056788	journal	June 2005
Amphipathic Lipid Packing Sensor Motifs: Probing Bilayer Defects with Hydrophobic Residues Vanni, Stefano; Vamparys, Lydie; Gautier, Romain Biophysical Journal, Vol. 104, Issue 3 https://doi.org/10.1016/j.bpj.2012.11.3837	journal	February 2013
Hetero-multivalent binding of cholera toxin subunit B with glycolipid mixtures Krishnan, Pratik; Singla, Akshi; Lee, Chin-An Colloids and Surfaces B: Biointerfaces, Vol. 160 https://doi.org/10.1016/j.colsurfb.2017.09.035	journal	December 2017
The perturbed membrane of cells undergoing apoptosis is susceptible to type II secretory phospholipase A2 to liberate arachidonic acid Atsumi, Gen-ichi; Murakami, Makoto; Tajima, Masae Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism, Vol. 1349, Issue 1 https://doi.org/10.1016/S0005-2760(97)00082-9	journal	November 1997
Phospholipid composition of cultured human endothelial cells Murphy, Eric J.; Joseph, Laurie; Stephens, Ralph Lipids, Vol. 27, Issue 2 https://doi.org/10.1007/BF02535816	journal	February 1992
Phospholipid composition of the mammalian red cell membrane can be rationalized by a superlattice model Virtanen, J. A.; Cheng, K. H.; Somerharju, P. Proceedings of the National Academy of Sciences, Vol. 95, Issue 9 https://doi.org/10.1073/pnas.95.9.4964	journal	April 1998
Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement Zachowski, A. Biochemical Journal, Vol. 294, Issue 1 https://doi.org/10.1042/bj2940001	journal	August 1993
Plasma membranes are asymmetric in lipid unsaturation, packing and protein shape Lorent, J. H.; Levental, K. R.; Ganesan, L. Nature Chemical Biology, Vol. 16, Issue 6 https://doi.org/10.1038/s41589-020-0529-6	journal	May 2020
Entropic and Enthalpic Contributions to Annexin V-Membrane Binding Jeppesen, Brian; Smith, Christina; Gibson, Donald F. Journal of Biological Chemistry, Vol. 283, Issue 10 https://doi.org/10.1074/jbc.M707637200	journal	March 2008
The activation of rat platelets increases the exposure of polyunsaturated fatty acid enriched phospholipids on the external leaflet of the plasma membrane Joo, Ferenc; Chevy, Françoise; Colard, Odile Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1149, Issue 2 https://doi.org/10.1016/0005-2736(93)90206-F	journal	July 1993
Molecular details of membrane fluidity changes during apoptosis and relationship to phospholipase A2 activity Gibbons, Elizabeth; Pickett, Katalyn R.; Streeter, Michael C. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1828, Issue 2 https://doi.org/10.1016/j.bbamem.2012.08.024	journal	February 2013
Comparative lipid analysis of purified plasma membranes and shed extracellular membrane vesicles from normal murine thymocytes and leukemic GRSL cells van Blitterswijk, W. J.; de Veer, G.; Krol, J. H. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 688, Issue 2 https://doi.org/10.1016/0005-2736(82)90361-3	journal	June 1982
Phospholipid metabolism of stimulated lymphocytes Ferber, Ernst; De Pasquale, Gabriel G.; Resch, Klaus Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism, Vol. 398, Issue 3 https://doi.org/10.1016/0005-2760(75)90187-3	journal	September 1975
Polyunsaturated fatty acids are enriched in the plasma membranes of mitogen-stimulated T-lymphocytes Goppelt-Strübe, Margarete; Resch, Klaus Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 904, Issue 1 https://doi.org/10.1016/0005-2736(87)90082-4	journal	November 1987
Fatty acid metabolism in human lymphocytes. I. Time-course changes in fatty acid composition and membrane fluidity during blastic transformation of peripheral blood lymphocytes Anel, Alberto; Naval, Javier; González, Blanca Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism, Vol. 1044, Issue 3 https://doi.org/10.1016/0005-2760(90)90076-A	journal	June 1990
The Distribution and Function of Phosphatidylserine in Cellular Membranes Leventis, Peter A.; Grinstein, Sergio Annual Review of Biophysics, Vol. 39, Issue 1 https://doi.org/10.1146/annurev.biophys.093008.131234	journal	April 2010
Membrane recognition by phospholipid-binding domains Lemmon, Mark A. Nature Reviews Molecular Cell Biology, Vol. 9, Issue 2 https://doi.org/10.1038/nrm2328	journal	February 2008
Comparative lipidomics analysis of HIV-1 particles and their producer cell membrane in different cell lines: Lipidomics of HIV-1 particles and producer plasma membranes Lorizate, Maier; Sachsenheimer, Timo; Glass, Bärbel Cellular Microbiology, Vol. 15, Issue 2 https://doi.org/10.1111/cmi.12101	journal	January 2013
Sensitivity of peripheral membrane proteins to the membrane context: A case study of phosphatidylserine and the TIM proteins Kerr, Daniel; Tietjen, Gregory T.; Gong, Zhiliang Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1860, Issue 10 https://doi.org/10.1016/j.bbamem.2018.06.010	journal	October 2018
Electrostatics and reduction of dimensionality produce apparent cooperativity when basic peptides bind to acidic lipids in membranes Mosior, Marian; McLaughlin, Stuart Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1105, Issue 1 https://doi.org/10.1016/0005-2736(92)90178-O	journal	March 1992
Effect of Phosphatidic Acid on Biomembrane: Experimental and Molecular Dynamics Simulations Study Kwolek, Urszula; Kulig, Waldemar; Wydro, Paweł The Journal of Physical Chemistry B, Vol. 119, Issue 31 https://doi.org/10.1021/acs.jpcb.5b03604	journal	July 2015
Examining the Contributions of Lipid Shape and Headgroup Charge on Bilayer Behavior Dickey, Allison; Faller, Roland Biophysical Journal, Vol. 95, Issue 6 https://doi.org/10.1529/biophysj.107.128074	journal	September 2008
An Electrostatic/Hydrogen Bond Switch as the Basis for the Specific Interaction of Phosphatidic Acid with Proteins Kooijman, Edgar E.; Tieleman, D. Peter; Testerink, Christa Journal of Biological Chemistry, Vol. 282, Issue 15 https://doi.org/10.1074/jbc.M609737200	journal	February 2007
Putting the pH into phosphatidic acid signaling Shin, John JH; Loewen, Christopher JR BMC Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1741-7007-9-85	journal	December 2011
Increased pH-sensitivity of protein binding to lipid membranes through the electrostatic-hydrogen bond switch Loew, Stephan; Kooijman, Edgar E.; May, Sylvio Chemistry and Physics of Lipids, Vol. 169 https://doi.org/10.1016/j.chemphyslip.2013.01.008	journal	April 2013
Phosphatidic acid binding proteins display differential binding as a function of membrane curvature stress and chemical properties Putta, Priya; Rankenberg, Johanna; Korver, Ruud A. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1858, Issue 11 https://doi.org/10.1016/j.bbamem.2016.07.014	journal	November 2016
Molecular dynamics simulation of a phosphatidylglycerol membrane Elmore, Donald E. FEBS Letters, Vol. 580, Issue 1 https://doi.org/10.1016/j.febslet.2005.11.064	journal	December 2005
Molecular Dynamics Simulation of a Palmitoyl-Oleoyl Phosphatidylserine Bilayer with Na+ Counterions and NaCl Mukhopadhyay, Parag; Monticelli, Luca; Tieleman, D. Peter Biophysical Journal, Vol. 86, Issue 3 https://doi.org/10.1016/S0006-3495(04)74227-7	journal	March 2004
Phosphatidic acid: A lipid messenger involved in intracellular and extracellular signalling English, Denis Cellular Signalling, Vol. 8, Issue 5 https://doi.org/10.1016/0898-6568(95)00076-3	journal	August 1996
A novel ecto-phosphatidic acid phosphohydrolase activity mediates activation of neutrophil superoxide generation by exogenous phosphatidic acid. Perry, D. K.; Stevens, V. L.; Widlanski, T. S. Journal of Biological Chemistry, Vol. 268, Issue 34 https://doi.org/10.1016/S0021-9258(19)74392-0	journal	December 1993
Time-course changes in content and fatty acid composition of phosphatidic acid from rat thymocytes during concanavalin A stimulation el Bawab, S.; Macovschi, O.; Lagarde, M. Biochemical Journal, Vol. 308, Issue 1 https://doi.org/10.1042/bj3080113	journal	May 1995
Phospholipase D: a lipid centric review Jenkins, G. M.; Frohman, M. A. Cellular and Molecular Life Sciences, Vol. 62, Issue 19-20 https://doi.org/10.1007/s00018-005-5195-z	journal	September 2005
Signaling functions of phosphatidic acid Wang, X.; Devaiah, S.; Zhang, W. Progress in Lipid Research, Vol. 45, Issue 3 https://doi.org/10.1016/j.plipres.2006.01.005	journal	May 2006
Phospholipase D Signaling Pathways and Phosphatidic Acid as Therapeutic Targets in Cancer Bruntz, Ronald C.; Lindsley, Craig W.; Brown, H. Alex Pharmacological Reviews, Vol. 66, Issue 4 https://doi.org/10.1124/pr.114.009217	journal	September 2014
Regulation of phospholipase D1 subcellular cycling through coordination of multiple membrane association motifs Du, Guangwei; Altshuller, Yelena M.; Vitale, Nicolas Journal of Cell Biology, Vol. 162, Issue 2 https://doi.org/10.1083/jcb.200302033	journal	July 2003
Phospholipase D1 is specifically required for regulated secretion of von Willebrand factor from endothelial cells Disse, Jennifer; Vitale, Nicolas; Bader, Marie-France Blood, Vol. 113, Issue 4 https://doi.org/10.1182/blood-2008-06-165282	journal	January 2009
Procoagulant and prothrombotic activation of human erythrocytes by phosphatidic acid Noh, Ji-Yoon; Lim, Kyung-Min; Bae, Ok-Nam American Journal of Physiology-Heart and Circulatory Physiology, Vol. 299, Issue 2 https://doi.org/10.1152/ajpheart.01144.2009	journal	August 2010
Phospholipase D and immune receptor signalling Melendez, Alirio J.; Allen, Janet M. Seminars in Immunology, Vol. 14, Issue 1 https://doi.org/10.1006/smim.2001.0341	journal	February 2002
Respiratory burst in human neutrophils Dahlgren, Claes; Karlsson, Anna Journal of Immunological Methods, Vol. 232, Issue 1-2 https://doi.org/10.1016/S0022-1759(99)00146-5	journal	December 1999
Targeting granulocyte apoptosis: mechanisms, models, and therapies: Targeting granulocyte apoptosis Duffin, Rodger; Leitch, Andrew E.; Fox, Sarah Immunological Reviews, Vol. 236, Issue 1 https://doi.org/10.1111/j.1600-065X.2010.00922.x	journal	June 2010
Constitutive neutrophil apoptosis: Mechanisms and regulation Luo, Hongbo R.; Loison, Fabien American Journal of Hematology, Vol. 83, Issue 4 https://doi.org/10.1002/ajh.21078	journal	April 2008
A novel protein kinase target for the lipid second messenger phosphatidic acid McPhail, Linda C.; Waite, Kristin A.; Regier, Debra S. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1439, Issue 2 https://doi.org/10.1016/S1388-1981(99)00100-6	journal	July 1999

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