The bulk of autotaxin activity is dispensable for adult mouse life

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Katsifa, Aggeliki ^a   Kaffe, Eleanna ^a   Nikolaidou Katsaridou, Nefeli ^a   Economides, Aris N ^b   Newbigging, Susan ^c,d   McKerlie, Colin ^c,d   Aidinis, Vassilis ^a  

^a BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

^b REGENERON PHARMACEUTICALS INC   (United States)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOTAXIN; BETA GALACTOSIDASE; TAMOXIFEN; 6-(3-(PIPERAZIN-1-YL)PROPANOYL)BENZO(D)OXAZOL-2(3H)-ONE; ALKYLGLYCEROPHOSPHOETHANOLAMINE PHOSPHODIESTERASE; BENZOXAZOLE DERIVATIVE; CRE RECOMBINASE; INTEGRASE; PHOSPHODIESTERASE; PIPERAZINE DERIVATIVE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG TARGETING; DRUG TOLERABILITY; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; GENE DELETION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIFE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING; AGING; ANIMAL; BLOOD; C57BL MOUSE; DRUG EFFECTS; ENZYME ACTIVATION; METABOLISM; PHYSIOLOGY;

AGING; ANIMALS; BENZOXAZOLES; ENZYME ACTIVATION; INTEGRASES; MICE, INBRED C57BL; PHOSPHORIC DIESTER HYDROLASES; PIPERAZINES; TAMOXIFEN;

EID: 84957110331     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0143083     Document Type: Article

References (50)

1. Umezu-Goto M, Kishi Y, Taira A, Hama K, Dohmae N, Takio K, et al. Autotaxin has lysophospholipase D activity leading to tumor cell growth and motility by lysophosphatidic acid production. The Journal of cell biology. 2002; 158(2):227-33. doi: 10.1083/jcb.200204026 PMID: 12119361.
2. Barbayianni E, Kaffe E, Aidinis V, Kokotos G. Autotaxin, a secreted lysophospholipase D, as a promising therapeutic target in chronic inflammation and cancer. Progress in lipid research. 2015; 58:76-96. Epub 2015/02/24. doi: 10.1016/j.plipres.2015.02.001 PMID: 25704398.
3. Perrakis A, Moolenaar WH. Autotaxin: structure-function and signaling. J Lipid Res. 2014. Epub 2014/02/20. doi: 10.1194/jlr.R046391 PMID: 24548887.
4. Nakanaga K, Hama K, Aoki J. Autotaxin-an LPA producing enzyme with diverse functions. J Biochem. 2010; 148(1):13-24. Epub 2010/05/25. doi: 10.1093/jb/mvq052 PMID: 20495010.
5. Fotopoulou S, Oikonomou N, Grigorieva E, Nikitopoulou I, Paparountas T, Thanassopoulou A, et al. ATX expression and LPA signalling are vital for the development of the nervous system. Dev Biol. 2010; 339(2):451-64. PMID: 20079728. doi: 10.1016/j.ydbio.2010.01.007.
6. Tanaka M, Okudaira S, Kishi Y, Ohkawa R, Iseki S, Ota M, et al. Autotaxin stabilizes blood vessels and is required for embryonic vasculature by producing lysophosphatidic acid. J Biol Chem. 2006; 281 (35):25822-30. PMID: 16829511.
7. van Meeteren LA, Ruurs P, Stortelers C, Bouwman P, van Rooijen MA, Pradere JP, et al. Autotaxin, a secreted lysophospholipase D, is essential for blood vessel formation during development. Molecular and cellular biology. 2006; 26(13):5015-22. PMID: 16782887.
8. Okudaira S, Yukiura H, Aoki J. Biological roles of lysophosphatidic acid signaling through its production by autotaxin. Biochimie. 2010; 92(6):698-706. Epub 2010/04/27. S0300-9084(10)00153-7 [pii] doi: 10. 1016/j.biochi.2010.04.015 PMID: 20417246.
9. Choi JW, Herr DR, Noguchi K, Yung YC, Lee CW, Mutoh T, et al. LPA receptors: subtypes and biological actions. Annu Rev Pharmacol Toxicol. 2010; 50:157-86. Epub 2010/01/09. doi: 10.1146/annurev. pharmtox.010909.105753 PMID: 20055701.
10. Yanagida K, Kurikawa Y, Shimizu T, Ishii S. Current progress in non-Edg family LPA receptor research. Biochim Biophys Acta. 2013; 1831(1):33-41. Epub 2012/08/21. S1388-1981(12)00168-0 [pii] doi: 10. 1016/j.bbalip.2012.08.003 PMID: 22902318.
11. Sevastou I, Kaffe E, Mouratis MA, Aidinis V. Lysoglycerophospholipids in chronic inflammatory disorders: The PLA(2)/LPC and ATX/LPA axes. Biochim Biophys Acta. 2013; 1831(1):42-60. Epub 2012/08/08. S1388-1981(12)00154-0 [pii] doi: 10.1016/j.bbalip.2012.07.019 PMID: 22867755.
12. Benesch MG, Ko YM, McMullen TP, Brindley DN. Autotaxin in the crosshairs: Taking aim at cancer and other inflammatory conditions. FEBS letters. 2014. Epub 2014/02/25. doi: 10.1016/j.febslet.2014.02. 009 PMID: 24560789.
13. Nikitopoulou I, Oikonomou N, Karouzakis E, Sevastou I, Nikolaidou-Katsaridou N, Zhao Z, et al. Autotaxin expression from synovial fibroblasts is essential for the pathogenesis of modeled arthritis. J Exp Med. 2012; 209(5):925-33. Epub 2012/04/12. jem.20112012 [pii] doi: 10.1084/jem.20112012 PMID: 22493518.
14. Oikonomou N, Mouratis MA, Tzouvelekis A, Kaffe E, Valavanis C, Vilaras G, et al. Pulmonary autotaxin expression contributes to the pathogenesis of pulmonary fibrosis. American journal of respiratory cell and molecular biology. 2012; 47(5):566-74. Epub 2012/06/30. doi: 10.1165/rcmb.2012-0004OC PMID: 22744859.
15. Bourgoin SG, Zhao C. Autotaxin and lysophospholipids in rheumatoid arthritis. Curr Opin Investig Drugs. 2010; 11(5):515-26. Epub 2010/04/27. PMID: 20419597.
16. Tager AM. Autotaxin emerges as a therapeutic target for idiopathic pulmonary fibrosis: limiting fibrosis by limiting lysophosphatidic acid synthesis. American journal of respiratory cell and molecular biology. 2012; 47(5):563-5. Epub 2012/11/06. doi: 10.1165/rcmb.2012-0235ED PMID: 23125419; PubMed Central PMCID: PMC3547105.
17. Liu S, Umezu-Goto M, Murph M, Lu Y, Liu W, Zhang F, et al. Expression of autotaxin and lysophosphatidic acid receptors increases mammary tumorigenesis, invasion, and metastases. Cancer Cell. 2009; 15(6):539-50. PMID: 19477432. doi: 10.1016/j.ccr.2009.03.027.
18. Hausmann J, Kamtekar S, Christodoulou E, Day JE, Wu T, Fulkerson Z, et al. Structural basis of substrate discrimination and integrin binding by autotaxin. Nat Struct Mol Biol. 2011; 18(2):198-204. PMID: 21240271. doi: 10.1038/nsmb.1980.
19. Albers HM, Ovaa H. Chemical Evolution of Autotaxin Inhibitors. Chem Rev. 2012. Epub 2012/02/18. doi: 10.1021/cr2003213 PMID: 22335786.
20. Barbayianni E, Magrioti V, Moutevelis-Minakakis P, Kokotos G. Autotaxin inhibitors: A patent review. Expert Opin Ther Pat. 2013. Epub 2013/05/07. doi: 10.1517/13543776.2013.796364 PMID: 23641951.
21. Nishimasu H, Okudaira S, Hama K, Mihara E, Dohmae N, Inoue A, et al. Crystal structure of autotaxin and insight into GPCR activation by lipid mediators. Nat Struct Mol Biol. 2011; 18(2):205-12. Epub 2011/01/18. nsmb.1998 [pii] doi: 10.1038/nsmb.1998 PMID: 21240269.
22. Economides AN, Frendewey D, Yang P, Dominguez MG, Dore AT, Lobov IB, et al. Conditionals by inversion provide a universal method for the generation of conditional alleles. Proc Natl Acad Sci U S A. 2013; 110(34):E3179-88. Epub 2013/08/07. doi: 10.1073/pnas.1217812110 PMID: 23918385; PubMed Central PMCID: PMC3752204.
23. Higashi AY, Ikawa T, Muramatsu M, Economides AN, Niwa A, Okuda T, et al. Direct hematological toxicity and illegitimate chromosomal recombination caused by the systemic activation of CreERT2. J Immunol. 2009; 182(9):5633-40. Epub 2009/04/22. doi: 10.4049/jimmunol.0802413 PMID: 19380810.
24. Soriano P. Generalizedlac Z expression with the ROSA26 Cre reporter strain. Nat Genet. 1999; 21 (1):70-1. Epub 1999/01/23. doi: 10.1038/5007 PMID: 9916792.
25. Nikitopoulou I, Kaffe E, Sevastou I, Sirioti I, Samiotaki M, Madan D, et al. A metabolically-stabilized phosphonate analog of lysophosphatidic acid attenuates collagen-induced arthritis. PLoS One. 2013; 8 (7):e70941. doi: 10.1371/journal.pone.0070941. Print 2013. PMID: 23923032.
26. Hameyer D, Loonstra A, Eshkind L, Schmitt S, Antunes C, Groen A, et al. Toxicity of ligand-dependent Cre recombinases and generation of a conditional Cre deleter mouse allowing mosaic recombination in peripheral tissues. Physiol Genomics. 2007; 31(1):32-41. Epub 2007/04/26. doi: 10.1152/physiolgenomics.00019.2007 PMID: 17456738.
27. Seibler J, Zevnik B, Kuter-Luks B, Andreas S, Kern H, Hennek T, et al. Rapid generation of inducible mouse mutants. Nucleic Acids Res. 2003; 31(4):e12. Epub 2003/02/13. PMID: 12582257; PubMed Central PMCID: PMC150244.
28. p53 function leads to tumour regression in vivo. Nature. 2007; 445(7128):661-5. Epub 2007/01/26. doi: 10. 1038/nature05541 PMID: 17251932.
29. Feil R, Wagner J, Metzger D, Chambon P. Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem Biophys Res Commun. 1997; 237(3):752-7. Epub 1997/08/28. doi: 10.1006/bbrc.1997.7124 PMID: 9299439.
30. Brake RL, Simmons PJ, Begley CG. Cross-contamination with tamoxifen induces transgene expression in non-exposed inducible transgenic mice. Genet Mol Res. 2004; 3(4):456-62. Epub 2005/02/03. PMID: 15688312.
31. Schmidt-Supprian M, Rajewsky K. Vagaries of conditional gene targeting. Nat Immunol. 2007; 8 (7):665-8. Epub 2007/06/21. doi: 10.1038/ni0707-665 PMID: 17579640.
32. Boucharaba A, Serre CM, Gres S, Saulnier-Blache JS, Bordet JC, Guglielmi J, et al. Platelet-derived lysophosphatidic acid supports the progression of osteolytic bone metastases in breast cancer. The Journal of clinical investigation. 2004; 114(12):1714-25. PMID: 15599396.
33. Saulnier-Blache JS. [Lysophosphatidic acid: A "bioactive" phospholipid]. Med Sci (Paris). 2004; 20(8-9):799-803. PMID: 15361348.
34. Dusaulcy R, Rancoule C, Gres S, Wanecq E, Colom A, Guigne C, et al. Adipose-specific disruption of autotaxin enhances nutritional fattening and reduces plasma lysophosphatidic acid. J Lipid Res. 2011; 52(6):1247-55. Epub 2011/03/23. jlr.M014985 [pii] doi: 10.1194/jlr.M014985 PMID: 21421848; PubMed Central PMCID: PMC3090245.
35. Rai V, Toure F, Chitayat S, Pei R, Song F, Li Q, et al. Lysophosphatidic acid targets vascular and oncogenic pathways via RAGE signaling. J Exp Med. 2012; 209(13):2339-50. Epub 2012/12/05. doi: 10. 1084/jem.20120873 PMID: 23209312; PubMed Central PMCID: PMC3526353.
36. Tigyi G, Parrill AL. Molecular mechanisms of lysophosphatidic acid action. Progress in lipid research. 2003; 42(6):498-526. Epub 2003/10/16. PMID: 14559069.
37. McIntyre TM, Pontsler AV, Silva AR, St Hilaire A, Xu Y, Hinshaw JC, et al. Identification of an intracellular receptor for lysophosphatidic acid (LPA): LPA is a transcellular PPARgamma agonist. Proc Natl Acad Sci U S A. 2003; 100(1):131-6. Epub 2002/12/28. [pii]. PMID: 12502787; PubMed Central PMCID: PMC140905.
38. Parrill AL, Tigyi G. Integrating the puzzle pieces: The current atomistic picture of phospholipid-G protein coupled receptor interactions. Biochim Biophys Acta. 2013; 1831(1):2-12. Epub 2012/09/18. S1388-1981(12)00199-0 [pii] doi: 10.1016/j.bbalip.2012.09.002 PMID: 22982815.
39. Gierse JK, Thorarensen A, Beltey K, Bradshaw-Pierce E, Cortes-Burgos L, Hall T, et al. A Novel Autotaxin Inhibitor Reduces Lysophosphatidic Acid Levels in Plasma and the Site of Inflammation. The Journal of pharmacology and experimental therapeutics. 2010. PMID: 20392816.
40. Saga H, Ohhata A, Hayashi A, Katoh M, Maeda T, Mizuno H, et al. A Novel Highly Potent Autotaxin/ENPP2 Inhibitor Produces Prolonged Decreases in Plasma Lysophosphatidic Acid Formation In Vivo and Regulates Urethral Tension. PLoS One. 2014; 9(4):e93230. Epub 2014/04/22. doi: 10.1371/journal.pone.0093230 PMID: 24747415; PubMed Central PMCID: PMC3991570.
41. Benesch MG, Tang X, Maeda T, Ohhata A, Zhao YY, Kok BP, et al. Inhibition of autotaxin delays breast tumor growth and lung metastasis in mice. Faseb J. 2014. Epub 2014/03/07. doi: 10.1096/fj.13-248641 PMID: 24599971.
42. Aoki J, Inoue A, Okudaira S. Two pathways for lysophosphatidic acid production. Biochim Biophys Acta. 2008; 1781(9):513-8. PMID: 18621144. doi: 10.1016/j.bbalip.2008.06.005.
43. Nikitopoulou I, Sevastou I, Madan D, Prestwich GD, Aidinis V. A bromo-phosphonate analogue of lysophosphatidic acid attenuates the development of collagen induced arthritis. PLoS One. 2013;in press.
44. Park GY, Lee YG, Berdyshev E, Nyenhuis S, Du J, Fu P, et al. Autotaxin production of Lysophosphatidic Acid Mediates Allergic Asthmatic Inflammation. Am J Respir Crit Care Med. 2013. Epub 2013/09/21. doi: 10.1164/rccm.201306-1014OC PMID: 24050723.
45. Zhang H, Xu X, Gajewiak J, Tsukahara R, Fujiwara Y, Liu J, et al. Dual activity lysophosphatidic acid receptor pan-antagonist/autotaxin inhibitor reduces breast cancer cell migration in vitro and causes tumor regression in vivo. Cancer research. 2009; 69(13):5441-9. PMID: 19509223. doi: 10.1158/0008-5472.CAN-09-0302.
46. Lee SC, Fujiwara Y, Liu J, Yue J, Shimizu Y, Norman DD, et al. Autotaxin, LPA Receptors (1 and 5) Exert Disparate Functions in Tumor Cells Versus the Host Tissue Microenvironment in Melanoma Invasion and Metastasis. Mol Cancer Res. 2014. Epub 2014/08/28. PMID: 25158955.
47. Leblanc R, Lee SC, David M, Bordet JC, Norman DD, Patil R, et al. Interaction of platelet-derived autotaxin with tumor integrin alphaVbeta3 controls metastasis of breast cancer cells to bone. Blood. 2014. Epub 2014/10/04. doi: 10.1182/blood-2014-04-568683 PMID: 25277122.
48. Benesch MG, Tang X, Dewald J, Dong WF, Mackey JR, Hemmings DG, et al. Tumor-induced inflammation in mammary adipose tissue stimulates a vicious cycle of autotaxin expression and breast cancer progression. Faseb J. 2015. Epub 2015/06/14. doi: 10.1096/fj.15-274480 PMID: 26071407.
49. Brindley DN, Lin FT, Tigyi GJ. Role of the autotaxin-lysophosphatidate axis in cancer resistance to chemotherapy and radiotherapy. Biochim Biophys Acta. 2012. Epub 2012/09/08. S1388-1981(12)00186-2 [pii] doi: 10.1016/j.bbalip.2012.08.015 PMID: 22954454.
50. Venkatraman G, Benesch MG, Tang X, Dewald J, McMullen TP, Brindley DN. Lysophosphatidate signaling stabilizes NRF2 and increases the expression of genes involved in drug resistance and oxidative stress responses: implications for cancer treatment. Faseb J. 2014. Epub 2014/11/16. doi: 10.1096/fj. 14-262659 PMID: 25398768.