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-Giorgianni, Li Chen, Derek Norman, Daniel L. Baker, Meng M. Rowland, Michael D. Best, Takamitsu Sano, Tamotsu Tsukahara, K. 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
Pages (from-to)958-970
Number of pages13
JournalJournal of Lipid Research
Volume52
Issue number5
DOIs
Publication statusPublished - May 2011

Fingerprint

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

Keywords

  • Acyl protein thioesterase
  • Autotoxin
  • Lysophosphatidic acid
  • Lysophospholipid

ASJC Scopus subject areas

  • Biochemistry
  • Cell Biology
  • Endocrinology

Cite this

Bolen, A. L., Naren, A. P., Yarlagadda, S., Beranova-Giorgianni, S., Chen, L., Norman, D., ... 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, 52(5), 958-970. https://doi.org/10.1194/jlr.M013326

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-Giorgianni, Sarka; Chen, Li; Norman, Derek; Baker, Daniel L.; Rowland, Meng M.; Best, Michael D.; Sano, Takamitsu; Tsukahara, Tamotsu; Liliom, K.; Igarashi, Yasuyuki; Tigyi, Gabor.

In: Journal of Lipid Research, Vol. 52, No. 5, 05.2011, p. 958-970.

Research output: Contribution to journalArticle

Bolen, AL, Naren, AP, Yarlagadda, S, Beranova-Giorgianni, 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-Giorgianni, Sarka ; Chen, Li ; Norman, Derek ; Baker, Daniel L. ; Rowland, Meng M. ; Best, Michael D. ; Sano, Takamitsu ; Tsukahara, Tamotsu ; Liliom, K. ; 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-Giorgianni, 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

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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.

KW - Acyl protein thioesterase

KW - Autotoxin

KW - Lysophosphatidic acid

KW - Lysophospholipid

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