The phospholipase A 1 activity of lysophospholipase A-I links platelet activation to LPA production during blood coagulation

Alyssa L. Bolen, Anjaparavanda P. Naren, Sunitha Yarlagadda, Sarka Beranova, Li Chen, Derek Norman, Daniel L. Baker, Meng M. Rowland, Michael D. Best, Takamitsu Sano, Tamotsu Tsukahara, Karoly Liliom, Yasuyuki Igarashi, Gabor Tigyi

Research output: Contribution to journalArticle

32 Citations (Scopus)

Abstract

Platelet activation initiates an upsurge in polyunsaturated (18:2 and 20:4) lysophosphatidic acid (LPA) production. The biochemical pathway(s) responsible for LPA production during blood clotting are not yet fully understood. Here we describe the purifi cation of a phospholipase A 1 (PLA 1 ) from thrombin-activated human platelets using sequential chromatographic steps followed by fl uorophosphonate (FP)-biotin affi nity labeling and proteomics characterization that identifi ed acyl-protein thioesterase 1 (APT1), also known as lysophospholipase A-I (LYPLA-I; accession code O75608) as a novel PLA 1 . Addition of this recombinant PLA 1 signifi - cantly increased the production of sn -2-esterifi ed polyunsaturated LPCs and the corresponding LPAs in plasma. We examined the regioisomeric preference of lysophospholipase D/autotaxin (ATX), which is the subsequent step in LPA production. To prevent acyl migration, ether-linked regioisomers of oleyl- sn -glycero-3-phosphocholine (lyso-PAF) were synthesized. ATX preferred the sn -1 to the sn -2 regioisomer of lyso-PAF. We propose the following LPA production pathway in blood: 1 ) Activated platelets release PLA Platelet activation initiates an upsurge in polyunsaturated (18:2 and 20:4) lysophosphatidic acid (LPA) production. The biochemical pathway(s) responsible for LPA production during blood clotting are not yet fully understood. Here we describe the purifi cation of a phospholipase A 1 (PLA 1 ) from thrombin-activated human platelets using sequential chromatographic steps followed by fl uorophosphonate (FP)-biotin affi nity labeling and proteomics characterization that identifi ed acyl-protein thioesterase 1 (APT1), also known as lysophospholipase A-I (LYPLA-I; accession code O75608) as a novel PLA 1 . Addition of this recombinant PLA 1 signifi - cantly increased the production of sn -2-esterifi ed polyunsaturated LPCs and the corresponding LPAs in plasma. We examined the regioisomeric preference of lysophospholipase D/autotaxin (ATX), which is the subsequent step in LPA production. To prevent acyl migration, ether-linked regioisomers of oleyl- sn -glycero-3-phosphocholine (lyso-PAF) were synthesized. ATX preferred the sn -1 to the sn -2 regioisomer of lyso- PAF. We propose the following LPA production pathway in blood: 1 ) Activated platelets release PLA 1 ; 2 ) PLA 1 generates a pool of sn-2 lysophospholipids; 3 ) These newly generated sn-2 lysophospholipids undergo acyl migration to yield sn-1 lysophospholipids, which are the preferred substrates of ATX; and 4 ) ATX cleaves the sn-1 lysophospholipids to generate sn-1 LPA species containing predominantly 18:2 and 20:4 fatty acids.-Bolen, A. L., A. P. Naren, S. Yarlagadda, S. Beranova- Giorgianni, L. Chen, D. Norman, D. L. Baker, M. M. Rowland, M. D. Best, T. Sano, T. Tsukahara, K. Liliom, Y. Igarashi, and G. Tigyi. The phospholipase A 1 activity of lysophospholipase A-I links platelet activation to LPA production during blood coagulation. J. Lipid Res. 2011. 52: 958-970. 1 ; 2 ) PLA 1 generates a pool of sn-2 lysophospholipids; 3 ) These newly generated sn-2 lysophospholipids undergo acyl migration to yield sn-1 lysophospholipids, which are the preferred substrates of ATX; and 4 ) ATX cleaves the sn-1 lysophospholipids to generate sn-1 LPA species containing predominantly 18:2 and 20:4 fatty acids.

Original languageEnglish (US)
Pages (from-to)958-970
Number of pages13
JournalJournal of lipid research
Volume52
Issue number5
DOIs
StatePublished - May 1 2011

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Lysophospholipase
Phospholipases A
Platelet Activation
Blood Coagulation
Platelets
Coagulation
Lysophospholipids
Blood
Chemical activation
Blood Platelets
Phosphorylcholine
Thrombin
Ether
Proteomics
Labeling
Cations
lysophosphatidic acid
Fatty Acids
Plasmas
Substrates

All Science Journal Classification (ASJC) codes

  • Biochemistry
  • Endocrinology
  • Cell Biology

Cite this

The phospholipase A 1 activity of lysophospholipase A-I links platelet activation to LPA production during blood coagulation. / Bolen, Alyssa L.; Naren, Anjaparavanda P.; Yarlagadda, Sunitha; Beranova, Sarka; Chen, Li; Norman, Derek; Baker, Daniel L.; Rowland, Meng M.; Best, Michael D.; Sano, Takamitsu; Tsukahara, Tamotsu; Liliom, Karoly; Igarashi, Yasuyuki; Tigyi, Gabor.

In: Journal of lipid research, Vol. 52, No. 5, 01.05.2011, p. 958-970.

Research output: Contribution to journalArticle

Bolen, AL, Naren, AP, Yarlagadda, S, Beranova, S, Chen, L, Norman, D, Baker, DL, Rowland, MM, Best, MD, Sano, T, Tsukahara, T, Liliom, K, Igarashi, Y & Tigyi, G 2011, 'The phospholipase A 1 activity of lysophospholipase A-I links platelet activation to LPA production during blood coagulation', Journal of lipid research, vol. 52, no. 5, pp. 958-970. https://doi.org/10.1194/jlr.M013326
Bolen, Alyssa L. ; Naren, Anjaparavanda P. ; Yarlagadda, Sunitha ; Beranova, Sarka ; Chen, Li ; Norman, Derek ; Baker, Daniel L. ; Rowland, Meng M. ; Best, Michael D. ; Sano, Takamitsu ; Tsukahara, Tamotsu ; Liliom, Karoly ; Igarashi, Yasuyuki ; Tigyi, Gabor. / The phospholipase A 1 activity of lysophospholipase A-I links platelet activation to LPA production during blood coagulation. In: Journal of lipid research. 2011 ; Vol. 52, No. 5. pp. 958-970.
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abstract = "Platelet activation initiates an upsurge in polyunsaturated (18:2 and 20:4) lysophosphatidic acid (LPA) production. The biochemical pathway(s) responsible for LPA production during blood clotting are not yet fully understood. Here we describe the purifi cation of a phospholipase A 1 (PLA 1 ) from thrombin-activated human platelets using sequential chromatographic steps followed by fl uorophosphonate (FP)-biotin affi nity labeling and proteomics characterization that identifi ed acyl-protein thioesterase 1 (APT1), also known as lysophospholipase A-I (LYPLA-I; accession code O75608) as a novel PLA 1 . Addition of this recombinant PLA 1 signifi - cantly increased the production of sn -2-esterifi ed polyunsaturated LPCs and the corresponding LPAs in plasma. We examined the regioisomeric preference of lysophospholipase D/autotaxin (ATX), which is the subsequent step in LPA production. To prevent acyl migration, ether-linked regioisomers of oleyl- sn -glycero-3-phosphocholine (lyso-PAF) were synthesized. ATX preferred the sn -1 to the sn -2 regioisomer of lyso-PAF. We propose the following LPA production pathway in blood: 1 ) Activated platelets release PLA Platelet activation initiates an upsurge in polyunsaturated (18:2 and 20:4) lysophosphatidic acid (LPA) production. The biochemical pathway(s) responsible for LPA production during blood clotting are not yet fully understood. Here we describe the purifi cation of a phospholipase A 1 (PLA 1 ) from thrombin-activated human platelets using sequential chromatographic steps followed by fl uorophosphonate (FP)-biotin affi nity labeling and proteomics characterization that identifi ed acyl-protein thioesterase 1 (APT1), also known as lysophospholipase A-I (LYPLA-I; accession code O75608) as a novel PLA 1 . Addition of this recombinant PLA 1 signifi - cantly increased the production of sn -2-esterifi ed polyunsaturated LPCs and the corresponding LPAs in plasma. We examined the regioisomeric preference of lysophospholipase D/autotaxin (ATX), which is the subsequent step in LPA production. To prevent acyl migration, ether-linked regioisomers of oleyl- sn -glycero-3-phosphocholine (lyso-PAF) were synthesized. ATX preferred the sn -1 to the sn -2 regioisomer of lyso- PAF. We propose the following LPA production pathway in blood: 1 ) Activated platelets release PLA 1 ; 2 ) PLA 1 generates a pool of sn-2 lysophospholipids; 3 ) These newly generated sn-2 lysophospholipids undergo acyl migration to yield sn-1 lysophospholipids, which are the preferred substrates of ATX; and 4 ) ATX cleaves the sn-1 lysophospholipids to generate sn-1 LPA species containing predominantly 18:2 and 20:4 fatty acids.-Bolen, A. L., A. P. Naren, S. Yarlagadda, S. Beranova- Giorgianni, L. Chen, D. Norman, D. L. Baker, M. M. Rowland, M. D. Best, T. Sano, T. Tsukahara, K. Liliom, Y. Igarashi, and G. Tigyi. The phospholipase A 1 activity of lysophospholipase A-I links platelet activation to LPA production during blood coagulation. J. Lipid Res. 2011. 52: 958-970. 1 ; 2 ) PLA 1 generates a pool of sn-2 lysophospholipids; 3 ) These newly generated sn-2 lysophospholipids undergo acyl migration to yield sn-1 lysophospholipids, which are the preferred substrates of ATX; and 4 ) ATX cleaves the sn-1 lysophospholipids to generate sn-1 LPA species containing predominantly 18:2 and 20:4 fatty acids.",
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T1 - The phospholipase A 1 activity of lysophospholipase A-I links platelet activation to LPA production during blood coagulation

AU - Bolen, Alyssa L.

AU - Naren, Anjaparavanda P.

AU - Yarlagadda, Sunitha

AU - Beranova, Sarka

AU - Chen, Li

AU - Norman, Derek

AU - Baker, Daniel L.

AU - Rowland, Meng M.

AU - Best, Michael D.

AU - Sano, Takamitsu

AU - Tsukahara, Tamotsu

AU - Liliom, Karoly

AU - Igarashi, Yasuyuki

AU - Tigyi, Gabor

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N2 - Platelet activation initiates an upsurge in polyunsaturated (18:2 and 20:4) lysophosphatidic acid (LPA) production. The biochemical pathway(s) responsible for LPA production during blood clotting are not yet fully understood. Here we describe the purifi cation of a phospholipase A 1 (PLA 1 ) from thrombin-activated human platelets using sequential chromatographic steps followed by fl uorophosphonate (FP)-biotin affi nity labeling and proteomics characterization that identifi ed acyl-protein thioesterase 1 (APT1), also known as lysophospholipase A-I (LYPLA-I; accession code O75608) as a novel PLA 1 . Addition of this recombinant PLA 1 signifi - cantly increased the production of sn -2-esterifi ed polyunsaturated LPCs and the corresponding LPAs in plasma. We examined the regioisomeric preference of lysophospholipase D/autotaxin (ATX), which is the subsequent step in LPA production. To prevent acyl migration, ether-linked regioisomers of oleyl- sn -glycero-3-phosphocholine (lyso-PAF) were synthesized. ATX preferred the sn -1 to the sn -2 regioisomer of lyso-PAF. We propose the following LPA production pathway in blood: 1 ) Activated platelets release PLA Platelet activation initiates an upsurge in polyunsaturated (18:2 and 20:4) lysophosphatidic acid (LPA) production. The biochemical pathway(s) responsible for LPA production during blood clotting are not yet fully understood. Here we describe the purifi cation of a phospholipase A 1 (PLA 1 ) from thrombin-activated human platelets using sequential chromatographic steps followed by fl uorophosphonate (FP)-biotin affi nity labeling and proteomics characterization that identifi ed acyl-protein thioesterase 1 (APT1), also known as lysophospholipase A-I (LYPLA-I; accession code O75608) as a novel PLA 1 . Addition of this recombinant PLA 1 signifi - cantly increased the production of sn -2-esterifi ed polyunsaturated LPCs and the corresponding LPAs in plasma. We examined the regioisomeric preference of lysophospholipase D/autotaxin (ATX), which is the subsequent step in LPA production. To prevent acyl migration, ether-linked regioisomers of oleyl- sn -glycero-3-phosphocholine (lyso-PAF) were synthesized. ATX preferred the sn -1 to the sn -2 regioisomer of lyso- PAF. We propose the following LPA production pathway in blood: 1 ) Activated platelets release PLA 1 ; 2 ) PLA 1 generates a pool of sn-2 lysophospholipids; 3 ) These newly generated sn-2 lysophospholipids undergo acyl migration to yield sn-1 lysophospholipids, which are the preferred substrates of ATX; and 4 ) ATX cleaves the sn-1 lysophospholipids to generate sn-1 LPA species containing predominantly 18:2 and 20:4 fatty acids.-Bolen, A. L., A. P. Naren, S. Yarlagadda, S. Beranova- Giorgianni, L. Chen, D. Norman, D. L. Baker, M. M. Rowland, M. D. Best, T. Sano, T. Tsukahara, K. Liliom, Y. Igarashi, and G. Tigyi. The phospholipase A 1 activity of lysophospholipase A-I links platelet activation to LPA production during blood coagulation. J. Lipid Res. 2011. 52: 958-970. 1 ; 2 ) PLA 1 generates a pool of sn-2 lysophospholipids; 3 ) These newly generated sn-2 lysophospholipids undergo acyl migration to yield sn-1 lysophospholipids, which are the preferred substrates of ATX; and 4 ) ATX cleaves the sn-1 lysophospholipids to generate sn-1 LPA species containing predominantly 18:2 and 20:4 fatty acids.

AB - Platelet activation initiates an upsurge in polyunsaturated (18:2 and 20:4) lysophosphatidic acid (LPA) production. The biochemical pathway(s) responsible for LPA production during blood clotting are not yet fully understood. Here we describe the purifi cation of a phospholipase A 1 (PLA 1 ) from thrombin-activated human platelets using sequential chromatographic steps followed by fl uorophosphonate (FP)-biotin affi nity labeling and proteomics characterization that identifi ed acyl-protein thioesterase 1 (APT1), also known as lysophospholipase A-I (LYPLA-I; accession code O75608) as a novel PLA 1 . Addition of this recombinant PLA 1 signifi - cantly increased the production of sn -2-esterifi ed polyunsaturated LPCs and the corresponding LPAs in plasma. We examined the regioisomeric preference of lysophospholipase D/autotaxin (ATX), which is the subsequent step in LPA production. To prevent acyl migration, ether-linked regioisomers of oleyl- sn -glycero-3-phosphocholine (lyso-PAF) were synthesized. ATX preferred the sn -1 to the sn -2 regioisomer of lyso-PAF. We propose the following LPA production pathway in blood: 1 ) Activated platelets release PLA Platelet activation initiates an upsurge in polyunsaturated (18:2 and 20:4) lysophosphatidic acid (LPA) production. The biochemical pathway(s) responsible for LPA production during blood clotting are not yet fully understood. Here we describe the purifi cation of a phospholipase A 1 (PLA 1 ) from thrombin-activated human platelets using sequential chromatographic steps followed by fl uorophosphonate (FP)-biotin affi nity labeling and proteomics characterization that identifi ed acyl-protein thioesterase 1 (APT1), also known as lysophospholipase A-I (LYPLA-I; accession code O75608) as a novel PLA 1 . Addition of this recombinant PLA 1 signifi - cantly increased the production of sn -2-esterifi ed polyunsaturated LPCs and the corresponding LPAs in plasma. We examined the regioisomeric preference of lysophospholipase D/autotaxin (ATX), which is the subsequent step in LPA production. To prevent acyl migration, ether-linked regioisomers of oleyl- sn -glycero-3-phosphocholine (lyso-PAF) were synthesized. ATX preferred the sn -1 to the sn -2 regioisomer of lyso- PAF. We propose the following LPA production pathway in blood: 1 ) Activated platelets release PLA 1 ; 2 ) PLA 1 generates a pool of sn-2 lysophospholipids; 3 ) These newly generated sn-2 lysophospholipids undergo acyl migration to yield sn-1 lysophospholipids, which are the preferred substrates of ATX; and 4 ) ATX cleaves the sn-1 lysophospholipids to generate sn-1 LPA species containing predominantly 18:2 and 20:4 fatty acids.-Bolen, A. L., A. P. Naren, S. Yarlagadda, S. Beranova- Giorgianni, L. Chen, D. Norman, D. L. Baker, M. M. Rowland, M. D. Best, T. Sano, T. Tsukahara, K. Liliom, Y. Igarashi, and G. Tigyi. The phospholipase A 1 activity of lysophospholipase A-I links platelet activation to LPA production during blood coagulation. J. Lipid Res. 2011. 52: 958-970. 1 ; 2 ) PLA 1 generates a pool of sn-2 lysophospholipids; 3 ) These newly generated sn-2 lysophospholipids undergo acyl migration to yield sn-1 lysophospholipids, which are the preferred substrates of ATX; and 4 ) ATX cleaves the sn-1 lysophospholipids to generate sn-1 LPA species containing predominantly 18:2 and 20:4 fatty acids.

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