Identification of a calmodulin-binding domain in Sema4D that regulates its exodomain shedding in platelets

Blood

Volumn 121, Issue 20, 2013, Pages 4221-4230

  Mou, Peipei ^a   Zeng, Zhao ^a   Li, Qiang ^a   Liu, Xiaohui ^a   Xin, Xiaoran ^a   Wannemacher, Kenneth M ^b   Ruan, Changgeng ^a,c   Li, Renhao ^d   Brass, Lawrence F ^b   Zhu, Li ^a,c  

^a SOOCHOW UNIVERSITY   (China)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c Key Laboratory of Thrombosis and Hemostasis of Ministry of Health   (China)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALMODULIN BINDING PROTEIN; COLLAGEN; SEMAPHORIN; SEMAPHORIN 4D; THROMBIN; THROMBOXANE A2; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; UNCLASSIFIED DRUG; CALMODULIN; CD100 ANTIGEN; ENZYME INHIBITOR; LEUKOCYTE ANTIGEN; N (6 AMINOHEXYL) 5 CHLORO 1 NAPHTHALENESULFONAMIDE; SULFONAMIDE;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; BLOOD CLOTTING; CHO CELL LINE; CONTROLLED STUDY; DISSOCIATION; ENDOTHELIUM CELL; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE MEMBRANE; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CHO CELL; CRICETULUS; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; HAMSTER; HUMAN; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN DOMAIN; PROTEIN PROCESSING;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD; BLOOD PLATELETS; CALMODULIN; CHO CELLS; CRICETINAE; CRICETULUS; ENZYME INHIBITORS; HUMANS; MOLECULAR SEQUENCE DATA; PLATELET ACTIVATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEMAPHORINS; SULFONAMIDES;

MLCS; MLOWN;

EID: 84880984610     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-11-470609     Document Type: Article

References (49)

1. Delaire S, Elhabazi A, Bensussan A, Boumsell L. CD100 is a leukocyte semaphorin. Cell Mol Life Sci. 1998;54(11): 1265-1276.
2. Kumanogoh A, Kikutani H. Immune semaphorins: a new area of semaphorin research. J Cell Sci. 2003;116(Pt 17):3463-3470.
3. Hall KT, Boumsell L, Schultze JL, et al. Human CD100, a novel leukocyte semaphorin that promotes B-cell aggregation and differentiation. Proc Natl Acad Sci USA. 1996;93(21):11780-11785.
4. Love CA, Harlos K, Mavaddat N, Davis SJ, Stuart DI, Jones EY, Esnouf RM. The ligand-binding face of the semaphorins revealed by the high-resolution crystal structure of SEMA4D. Nat Struct Biol. 2003;10(10):843-848.
5. Esnouf RM, Love CA, Harlos K, Stuart DI, Jones EY. Structure determination of human semaphorin 4D as an example of the use of MAD in non-optimal cases. Acta Crystallogr D Biol Crystallogr. 2006;62(Pt 1):108-115.
6. Kumanogoh A, Watanabe C, Lee I, et al. Identification of CD72 as a lymphocyte receptor for the class IV semaphorin CD100: a novel mechanism for regulating B cell signaling. Immunity. 2000;13(5):621-631.
7. Bougeret C, Mansur IG, Dastot H, Schmid M, Mahouy G, Bensussan A, Boumsell L. Increased surface expression of a newly identified 150-kDa dimer early after human T lymphocyte activation. J Immunol. 1992;148(2):318-323.
8. Furuyama T, Inagaki S, Kosugi A, et al. Identification of a novel transmembrane semaphorin expressed on lymphocytes. J Biol Chem. 1996;271(52):33376-33381.
9. Oinuma I, Ito Y, Katoh H, Negishi M. Semaphorin 4D/Plexin-B1 stimulates PTEN activity through R-Ras GTPase-activating protein activity, inducing growth cone collapse in hippocampal neurons. J Biol Chem. 2010;285(36): 28200-28209.
10. Ito Y, Oinuma I, Katoh H, Kaibuchi K, Negishi M. Sema4D/plexin-B1 activates GSK-3beta through R-Ras GAP activity, inducing growth cone collapse. EMBO Rep. 2006;7(7):704-709.
11. Oinuma I, Katoh H, Negishi M. Molecular dissection of the semaphorin 4D receptor plexin-B1-stimulated R-Ras GTPase-activating protein activity and neurite remodeling in hippocampal neurons. J Neurosci. 2004;24(50):11473-11480.
12. Oinuma I, Ishikawa Y, Katoh H, Negishi M. The Semaphorin 4D receptor Plexin-B1 is a GTPase activating protein for R-Ras. Science. 2004; 305(5685):862-865.
13. Basile JR, Barac A, Zhu T, Guan KL, Gutkind JS. Class IV semaphorins promote angiogenesis by stimulating Rho-initiated pathways through plexinB. Cancer Res. 2004;64(15):5212-5224.
14. Conrotto P, Valdembri D, Corso S, et al. Sema4D induces angiogenesis through Met recruitment by Plexin B1. Blood. 2005;105(11):4321-4329.
15. Sierra JR, Corso S, Caione L, et al. Tumor angiogenesis and progression are enhanced by Sema4D produced by tumor-associated macrophages. J Exp Med. 2008;205(7): 1673-1685.
16. Binmadi NO, Proia P, Zhou H, Yang YH, Basile JR. Rho-mediated activation of PI(4)P5K and lipid second messengers is necessary for promotion of angiogenesis by Semaphorin 4D. Angiogenesis. 2011;14(3):309-319.
17. Xu XG, Zhu Y, Liu XS, et al. Preparation and identification of monoclonal antibodies against CD100 molecule. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi. 2003;19(1):80-82.
18. Kato S, Kubota K, Shimamura T, et al. Semaphorin 4D, a lymphocyte semaphorin, enhances tumor cell motility through binding its receptor, plexinB1, in pancreatic cancer. Cancer Sci. 2011;102(11):2029-2037.
19. Conrotto P, Corso S, Gamberini S, Comoglio PM, Giordano S. Interplay between scatter factor receptors and B plexins controls invasive growth. Oncogene. 2004;23(30):5131-5137.
20. Ch’ng ES, Kumanogoh A. Roles of Sema4D and plexin-B1 in tumor progression. Mol Cancer. 2010;9:251.
21. Friedel RH, Kerjan G, Rayburn H, et al. Plexin-B2 controls the development of cerebellar granule cells. J Neurosci. 2007;27(14):3921-3932.
22. Hirschberg A, Deng S, Korostylev A, et al. Gene deletion mutants reveal a role for semaphorin receptors of the plexin-B family in mechanisms underlying corticogenesis. Mol Cell Biol. 2010; 30(3):764-780.
23. Zhu L, Bergmeier W, Wu J, et al. Regulated surface expression and shedding support a dual role for semaphorin 4D in platelet responses to vascular injury. Proc Natl Acad Sci USA. 2007; 104(5):1621-1626.
24. Wannemacher KM, Zhu L, Jiang H, et al. Diminished contact-dependent reinforcement of Syk activation underlies impaired thrombus growth in mice lacking Semaphorin 4D. Blood. 2010;116(25):5707-5715.
25. Zhu L, Stalker TJ, Fong KP, et al. Disruption of SEMA4D ameliorates platelet hypersensitivity in dyslipidemia and confers protection against the development of atherosclerosis. Arterioscler Thromb Vasc Biol. 2009;29(7):1039-1045.
26. Yukawa K, Tanaka T, Kishino M, et al. Deletion of Sema4D gene reduces intimal neovascularization and plaque growth in apolipoprotein E-deficient mice. Int J Mol Med. 2010;26(1):39-44.
27. Fong KP, Barry C, Tran AN, et al. Deciphering the human platelet sheddome. Blood. 2011;117(1): e15-e26.
28. Lewandrowski U, Wortelkamp S, Lohrig K, Zahedi RP, Wolters DA, Walter U, Sickmann A. Platelet membrane proteomics: a novel repository for functional research. Blood. 2009;114(1):e10-e19.
29. Qiao JL, Shen Y, Gardiner EE, Andrews RK. Proteolysis of platelet receptors in humans and other species. Biol Chem. 2010;391(8):893-900.
30. Gardiner EE, Al-Tamimi M, Andrews RK, Berndt MC. Platelet receptor shedding. Methods Mol Biol. 2012;788:321-339.
31. Berndt MC, Karunakaran D, Gardiner EE, Andrews RK. Programmed autologous cleavage of platelet receptors. J Thromb Haemost. 2007; 5(Suppl 1):212-219.
32. Andrews RK, Munday AD, Mitchell CA, Berndt MC. Interaction of calmodulin with the cytoplasmic domain of the platelet membrane glycoprotein Ib-IX-V complex. Blood. 2001;98(3):681-687.
33. Mo X, Nguyen NX, Mu FT, et al. Transmembrane and trans-subunit regulation of ectodomain shedding of platelet glycoprotein Ibalpha. J Biol Chem. 2010;285(42):32096-32104.
34. Locke D, Liu C, Peng X, Chen H, Kahn ML. Fc Rgamma -independent signaling by the platelet collagen receptor glycoprotein VI. J Biol Chem. 2003;278(17):15441-15448.
35. Andrews RK, Suzuki-Inoue K, Shen Y, Tulasne D, Watson SP, Berndt MC. Interaction of calmodulin with the cytoplasmic domain of platelet glycoprotein VI. Blood. 2002;99(11):4219-4221.
36. Wong MX, Harbour SN, Wee JL, Lau LM, Andrews RK, Jackson DE. Proteolytic cleavage of platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31) is regulated by a calmodulin-binding motif. FEBS Lett. 2004;568(1-3):70-78.
37. Elhabazi A, Delaire S, Bensussan A, Boumsell L, Bismuth G. Biological activity of soluble CD100. I. The extracellular region of CD100 is released from the surface of T lymphocytes by regulated proteolysis. J Immunol. 2001;166(7): 4341-4347.
38. Ruan CG, Du XP, Xi XD, Castaldi PA, Berndt MC. A murine antiglycoprotein Ib complex monoclonal antibody, SZ 2, inhibits platelet aggregation induced by both ristocetin and collagen. Blood. 1987;69(2):570-577.
39. Chen H, Locke D, Liu Y, Liu C, Kahn ML. The platelet receptor GPVI mediates both adhesion and signaling responses to collagen in a receptor density-dependent fashion. J Biol Chem. 2002; 277(4):3011-3019.
40. Prevost N, Woulfe D, Tanaka T, Brass LF. Interactions between Eph kinases and ephrins provide a mechanism to support platelet aggregation once cell-to-cell contact has occurred. Proc Natl Acad Sci USA. 2002;99(14): 9219-9224.
41. Deng W, Srinivasan S, Zheng X, Putkey JA, Li R. Interaction of calmodulin with L-selectin at the membrane interface: implication on the regulation of L-selectin shedding. J Mol Biol. 2011;411(1): 220-233.
42. Yap KL, Kim J, Truong K, Sherman M, Yuan T, Ikura M. Calmodulin target database. J Struct Funct Genomics. 2000;1(1):8-14.
43. Rabie T, Strehl A, Ludwig A, Nieswandt B. Evidence for a role of ADAM17 (TACE) in the regulation of platelet glycoprotein V. J Biol Chem. 2005;280(15):14462-14468.
44. Gardiner EE, Arthur JF, Berndt MC, Andrews RK. Role of calmodulin in platelet receptor function. Curr Med Chem Cardiovasc Hematol Agents. 2005;3(4):283-287.
45. Osawa M, Kuwamoto S, Izumi Y, et al. Evidence for calmodulin inter-domain compaction in solution induced by W-7 binding. FEBS Lett. 1999;442(2-3):173-177.
46. Osawa M, Swindells MB, Tanikawa J, Tanaka T, Mase T, Furuya T, Ikura M. Solution structure of calmodulin-W-7 complex: the basis of diversity in molecular recognition. J Mol Biol. 1998;276(1): 165-176.
47. Andrews RK, Karunakaran D, Gardiner EE, Berndt MC. Platelet receptor proteolysis: a mechanism for downregulating platelet reactivity. Arterioscler Thromb Vasc Biol. 2007; 27(7):1511-1520.
48. Gardiner EE, Arthur JF, Kahn ML, Berndt MC, Andrews RK. Regulation of platelet membrane levels of glycoprotein VI by a platelet-derived metalloproteinase. Blood. 2004;104(12): 3611-3617.
49. Zielonka M, Xia J, Friedel RH, Offermanns S, Worzfeld T. A systematic expression analysis implicates Plexin-B2 and its ligand Sema4C in the regulation of the vascular and endocrine system. Exp Cell Res. 2010;316(15): 2477-2486.