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    Joann Trejo

    TitleProfessor
    SchoolUniversity of California, San Diego
    DepartmentPharmacology
    Address9500 Gilman Drive #0636
    CA La Jolla 92093
    Phone858-246-0150
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      Collapse Biography 
      Collapse Education and Training
      University of California, San DiegoM.B.A.Rady School of Management2015
      University of California, San DiegoPh.D.School of Medicine1992
      University of California, DavisB.S.Toxicology/Biochemistry1986
      Collapse Awards and Honors
      2015American Society for Biochemistry and Molecular Biology Ruth Kirchstein Diversity in Science Award
      2014UC San Diego Chancellor’s Award for Excellence in Postdoctoral Scholar Mentoring
      2012Women Who Mean Business Award, San Diego Business Journal
      2006American Heart Association Established Investigator Award
      1995American Heart Association Scientist Career Development Grant Award
      1993University of California President’s Postdoctoral Fellowship Award

      Collapse Overview 
      Collapse Overview
      Our research is focused on cell signaling and how it regulates vascular barrier leakage and breast cancer progression. We are examining how activation of GPCRs, specifically PARs, by distinct proteases differentially regulates endothelial barrier breakdown (pro-inflammatory signaling) versus cytoprotection (anti-inflammatory signaling) through selective activation of specific signaling pathways. We discovered that aberrant PAR1 trafficking results in dysregulated signaling in invasive breast cancer and consequently promotes tumor progression. We are examining how the endocytic machinery and the tumor suppressor ARRDC3 contribute to the dysregulation of GPCR trafficking and signaling to the Hippo pathway and the impact on breast carcinoma growth, invasion and metastasis.

      Collapse Interests
      endothelial cells, sepsis, breast cancer, proteases, GPCRs, cell signaling, membrane trafficking, endocytosis, caveolae, lysosomes, G proteins, thrombin, cytoprotection, arrestins, ubiquitin

      Collapse ORNG Applications 
      Collapse Featured Publications
      Collapse Websites
      Collapse In The News
      Collapse NIH Awarded Grants

      Collapse Bibliographic 
      Collapse Publications
      Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Researchers can login to make corrections and additions, or contact us for help.
      List All   |   Timeline
      1. Dores MR, Grimsey NJ, Mendez F, Trejo J. ALIX Regulates the Ubiquitin-Independent Lysosomal Sorting of the P2Y1 Purinergic Receptor via a YPX3L Motif. PLoS One. 2016; 11(6):e0157587. PMID: 27301021.
        View in: PubMed
      2. Grimsey NJ, Trejo J. Integration of endothelial protease-activated receptor-1 inflammatory signaling by ubiquitin. Curr Opin Hematol. 2016 May; 23(3):274-9. PMID: 26845544.
        View in: PubMed
      3. Grimsey NJ, Coronel LJ, Cordova IC, Trejo J. Recycling and Endosomal Sorting of Protease-activated Receptor-1 Is Distinctly Regulated by Rab11A and Rab11B Proteins. J Biol Chem. 2016 Jan 29; 291(5):2223-36. PMID: 26635365.
        View in: PubMed
      4. Dores MR, Lin H, J Grimsey N, Mendez F, Trejo J. The a-arrestin ARRDC3 mediates ALIX ubiquitination and G protein-coupled receptor lysosomal sorting. Mol Biol Cell. 2015 Dec 15; 26(25):4660-73. PMID: 26490116.
        View in: PubMed
      5. Grimsey NJ, Aguilar B, Smith TH, Le P, Soohoo AL, Puthenveedu MA, Nizet V, Trejo J. Ubiquitin plays an atypical role in GPCR-induced p38 MAP kinase activation on endosomes. J Cell Biol. 2015 Sep 28; 210(7):1117-31. PMID: 26391660.
        View in: PubMed
      6. Dores MR, Trejo J. GPCR sorting at multivesicular endosomes. Methods Cell Biol. 2015; 130:319-32. PMID: 26360043.
        View in: PubMed
      7. Soto AG, Smith TH, Chen B, Bhattacharya S, Cordova IC, Kenakin T, Vaidehi N, Trejo J. N-linked glycosylation of protease-activated receptor-1 at extracellular loop 2 regulates G-protein signaling bias. Proc Natl Acad Sci U S A. 2015 Jul 7; 112(27):E3600-8. PMID: 26100877.
        View in: PubMed
      8. Stoner TD, Weston TA, Trejo J, Doran KS. Group B streptococcal infection and activation of human astrocytes. PLoS One. 2015; 10(6):e0128431. PMID: 26030618.
        View in: PubMed
      9. Yang H, Fang L, Zhan R, Hegarty JM, Ren J, Hsiai TK, Gleeson JG, Miller YI, Trejo J, Chi NC. Polo-like kinase 2 regulates angiogenic sprouting and blood vessel development. Dev Biol. 2015 Aug 15; 404(2):49-60. PMID: 26004360.
        View in: PubMed
      10. Chen B, Soto AG, Coronel LJ, Goss A, van Ryn J, Trejo J. Characterization of thrombin-bound dabigatran effects on protease-activated receptor-1 expression and signaling in vitro. Mol Pharmacol. 2015 Jul; 88(1):95-105. PMID: 25934730.
        View in: PubMed
      11. Kawamura T, Stephens B, Qin L, Yin X, Dores MR, Smith TH, Grimsey N, Abagyan R, Trejo J, Kufareva I, Fuster MM, Salanga CL, Handel TM. A general method for site specific fluorescent labeling of recombinant chemokines. PLoS One. 2014; 9(1):e81454. PMID: 24489642.
        View in: PubMed
      12. Grimsey N, Lin H, Trejo J. Endosomal signaling by protease-activated receptors. Methods Enzymol. 2014; 535:389-401. PMID: 24377935.
        View in: PubMed
      13. Dores MR, Trejo J. Atypical regulation of G protein-coupled receptor intracellular trafficking by ubiquitination. Curr Opin Cell Biol. 2014 Apr; 27:44-50. PMID: 24680429.
        View in: PubMed
      14. Chen B, Siderovski DP, Neubig RR, Lawson MA, Trejo J. Regulation of Protease-activated Receptor 1 Signaling by the Adaptor Protein Complex 2 and R4 Subfamily of Regulator of G Protein Signaling Proteins. J Biol Chem. 2014 Jan 17; 289(3):1580-91. PMID: 24297163.
        View in: PubMed
      15. Lin H, Liu AP, Smith TH, Trejo J. Cofactoring and dimerization of proteinase-activated receptors. Pharmacol Rev. 2013; 65(4):1198-213. PMID: 24064459.
        View in: PubMed
      16. Gilliland CT, Salanga CL, Kawamura T, Trejo J, Handel TM. The Chemokine Receptor CCR1 Is Constitutively Active, Which Leads to G Protein-independent, ß-Arrestin-mediated Internalization. J Biol Chem. 2013 Nov 8; 288(45):32194-210. PMID: 24056371.
        View in: PubMed
      17. Canto I, Trejo J. Palmitoylation of protease-activated receptor-1 regulates adaptor protein complex-2 and -3 interaction with tyrosine-based motifs and endocytic sorting. J Biol Chem. 2013 May 31; 288(22):15900-12. PMID: 23580642.
        View in: PubMed
      18. Lin H, Trejo J. Transactivation of the PAR1-PAR2 heterodimer by thrombin elicits ß-arrestin-mediated endosomal signaling. J Biol Chem. 2013 Apr 19; 288(16):11203-15. PMID: 23476015.
        View in: PubMed
      19. Antoniak S, Owens AP, Baunacke M, Williams JC, Lee RD, Weithäuser A, Sheridan PA, Malz R, Luyendyk JP, Esserman DA, Trejo J, Kirchhofer D, Blaxall BC, Pawlinski R, Beck MA, Rauch U, Mackman N. PAR-1 contributes to the innate immune response during viral infection. J Clin Invest. 2013 Mar 1; 123(3):1310-22. PMID: 23391721.
        View in: PubMed
      20. Marchese A, Trejo J. Ubiquitin-dependent regulation of G protein-coupled receptor trafficking and signaling. Cell Signal. 2013 Mar; 25(3):707-16. PMID: 23201781.
        View in: PubMed
      21. Canto I, Soh UJ, Trejo J. Allosteric modulation of protease-activated receptor signaling. Mini Rev Med Chem. 2012 Aug; 12(9):804-11. PMID: 22681248.
        View in: PubMed
      22. Dores MR, Paing MM, Lin H, Montagne WA, Marchese A, Trejo J. AP-3 regulates PAR1 ubiquitin-independent MVB/lysosomal sorting via an ALIX-mediated pathway. Mol Biol Cell. 2012 Sep; 23(18):3612-23. PMID: 22833563.
        View in: PubMed
      23. Dores MR, Trejo J. Ubiquitination of G protein-coupled receptors: functional implications and drug discovery. Mol Pharmacol. 2012 Oct; 82(4):563-70. PMID: 22700696.
        View in: PubMed
      24. Dores MR, Chen B, Lin H, Soh UJ, Paing MM, Montagne WA, Meerloo T, Trejo J. ALIX binds a YPX(3)L motif of the GPCR PAR1 and mediates ubiquitin-independent ESCRT-III/MVB sorting. J Cell Biol. 2012 Apr 30; 197(3):407-19. PMID: 22547407.
        View in: PubMed
      25. Malik R, Soh UJ, Trejo J, Marchese A. Novel roles for the E3 ubiquitin ligase atrophin-interacting protein 4 and signal transduction adaptor molecule 1 in G protein-coupled receptor signaling. J Biol Chem. 2012 Mar 16; 287(12):9013-27. PMID: 22275353.
        View in: PubMed
      26. Soh UJ, Trejo J. Activated protein C promotes protease-activated receptor-1 cytoprotective signaling through ß-arrestin and dishevelled-2 scaffolds. Proc Natl Acad Sci U S A. 2011 Dec 13; 108(50):E1372-80. PMID: 22106258.
        View in: PubMed
      27. Chen B, Dores MR, Grimsey N, Canto I, Barker BL, Trejo J. Adaptor protein complex-2 (AP-2) and epsin-1 mediate protease-activated receptor-1 internalization via phosphorylation- and ubiquitination-dependent sorting signals. J Biol Chem. 2011 Nov 25; 286(47):40760-70. PMID: 21965661.
        View in: PubMed
      28. Grimsey N, Soto AG, Trejo J. Regulation of protease-activated receptor signaling by post-translational modifications. IUBMB Life. 2011 Jun; 63(6):403-11. PMID: 21438117.
        View in: PubMed
      29. Laroche G, Giguère PM, Roth BL, Trejo J, Siderovski DP. RNA interference screen for RGS protein specificity at muscarinic and protease-activated receptors reveals bidirectional modulation of signaling. Am J Physiol Cell Physiol. 2010 Sep; 299(3):C654-64. PMID: 20573995.
        View in: PubMed
      30. Soh UJ, Dores MR, Chen B, Trejo J. Signal transduction by protease-activated receptors. Br J Pharmacol. 2010 May; 160(2):191-203. PMID: 20423334.
        View in: PubMed
      31. Soto AG, Trejo J. N-linked glycosylation of protease-activated receptor-1 second extracellular loop: a critical determinant for ligand-induced receptor activation and internalization. J Biol Chem. 2010 Jun 11; 285(24):18781-93. PMID: 20368337.
        View in: PubMed
      32. Ricks TK, Trejo J. Phosphorylation of protease-activated receptor-2 differentially regulates desensitization and internalization. J Biol Chem. 2009 Dec 4; 284(49):34444-57. PMID: 19815543.
        View in: PubMed
      33. Seminario-Vidal L, Kreda S, Jones L, O'Neal W, Trejo J, Boucher RC, Lazarowski ER. Thrombin promotes release of ATP from lung epithelial cells through coordinated activation of rho- and Ca2+-dependent signaling pathways. J Biol Chem. 2009 Jul 31; 284(31):20638-48. PMID: 19439413.
        View in: PubMed
      34. Russo A, Soh UJ, Trejo J. Proteases display biased agonism at protease-activated receptors: location matters! Mol Interv. 2009 Apr; 9(2):87-96. PMID: 19401541.
        View in: PubMed
      35. Russo A, Soh UJ, Paing MM, Arora P, Trejo J. Caveolae are required for protease-selective signaling by protease-activated receptor-1. Proc Natl Acad Sci U S A. 2009 Apr 14; 106(15):6393-7. PMID: 19332793.
        View in: PubMed
      36. Arora P, Cuevas BD, Russo A, Johnson GL, Trejo J. Persistent transactivation of EGFR and ErbB2/HER2 by protease-activated receptor-1 promotes breast carcinoma cell invasion. Oncogene. 2008 Jul 24; 27(32):4434-45. PMID: 18372913.
        View in: PubMed
      37. Alam MR, Dixit V, Kang H, Li ZB, Chen X, Trejo J, Fisher M, Juliano RL. Intracellular delivery of an anionic antisense oligonucleotide via receptor-mediated endocytosis. Nucleic Acids Res. 2008 May; 36(8):2764-76. PMID: 18367474.
        View in: PubMed
      38. Marchese A, Paing MM, Temple BR, Trejo J. G protein-coupled receptor sorting to endosomes and lysosomes. Annu Rev Pharmacol Toxicol. 2008; 48:601-29. PMID: 17995450.
        View in: PubMed
      39. Bhandari D, Trejo J, Benovic JL, Marchese A. Arrestin-2 interacts with the ubiquitin-protein isopeptide ligase atrophin-interacting protein 4 and mediates endosomal sorting of the chemokine receptor CXCR4. J Biol Chem. 2007 Dec 21; 282(51):36971-9. PMID: 17947233.
        View in: PubMed
      40. Wolfe BL, Marchese A, Trejo J. Ubiquitination differentially regulates clathrin-dependent internalization of protease-activated receptor-1. J Cell Biol. 2007 Jun 4; 177(5):905-16. PMID: 17535965.
        View in: PubMed
      41. Traynelis SF, Trejo J. Protease-activated receptor signaling: new roles and regulatory mechanisms. Curr Opin Hematol. 2007 May; 14(3):230-5. PMID: 17414212.
        View in: PubMed
      42. Wolfe BL, Trejo J. Clathrin-dependent mechanisms of G protein-coupled receptor endocytosis. Traffic. 2007 May; 8(5):462-70. PMID: 17376169.
        View in: PubMed
      43. Arora P, Ricks TK, Trejo J. Protease-activated receptor signalling, endocytic sorting and dysregulation in cancer. J Cell Sci. 2007 Mar 15; 120(Pt 6):921-8. PMID: 17344429.
        View in: PubMed
      44. Camerer E, Trejo J. Cryptic messages: is noncoagulant tissue factor reserved for cell signaling? Proc Natl Acad Sci U S A. 2006 Sep 26; 103(39):14259-60. PMID: 16985001.
        View in: PubMed
      45. Dho SE, Trejo J, Siderovski DP, McGlade CJ. Dynamic regulation of mammalian numb by G protein-coupled receptors and protein kinase C activation: Structural determinants of numb association with the cortical membrane. Mol Biol Cell. 2006 Sep; 17(9):4142-55. PMID: 16837553.
        View in: PubMed
      46. Paing MM, Johnston CA, Siderovski DP, Trejo J. Clathrin adaptor AP2 regulates thrombin receptor constitutive internalization and endothelial cell resensitization. Mol Cell Biol. 2006 Apr; 26(8):3231-42. PMID: 16581796.
        View in: PubMed
      47. Gullapalli A, Wolfe BL, Griffin CT, Magnuson T, Trejo J. An essential role for SNX1 in lysosomal sorting of protease-activated receptor-1: evidence for retromer-, Hrs-, and Tsg101-independent functions of sorting nexins. Mol Biol Cell. 2006 Mar; 17(3):1228-38. PMID: 16407403.
        View in: PubMed
      48. Morris DR, Ding Y, Ricks TK, Gullapalli A, Wolfe BL, Trejo J. Protease-activated receptor-2 is essential for factor VIIa and Xa-induced signaling, migration, and invasion of breast cancer cells. Cancer Res. 2006 Jan 1; 66(1):307-14. PMID: 16397244.
        View in: PubMed
      49. Urs NM, Jones KT, Salo PD, Severin JE, Trejo J, Radhakrishna H. A requirement for membrane cholesterol in the beta-arrestin- and clathrin-dependent endocytosis of LPA1 lysophosphatidic acid receptors. J Cell Sci. 2005 Nov 15; 118(Pt 22):5291-304. PMID: 16263766.
        View in: PubMed
      50. Griffin CT, Trejo J, Magnuson T. Genetic evidence for a mammalian retromer complex containing sorting nexins 1 and 2. Proc Natl Acad Sci U S A. 2005 Oct 18; 102(42):15173-7. PMID: 16214895.
        View in: PubMed
      51. Trejo J. Internal PDZ ligands: novel endocytic recycling motifs for G protein-coupled receptors. Mol Pharmacol. 2005 May; 67(5):1388-90. PMID: 15713849.
        View in: PubMed
      52. Stalheim L, Ding Y, Gullapalli A, Paing MM, Wolfe BL, Morris DR, Trejo J. Multiple independent functions of arrestins in the regulation of protease-activated receptor-2 signaling and trafficking. Mol Pharmacol. 2005 Jan; 67(1):78-87. PMID: 15475570.
        View in: PubMed
      53. Paing MM, Temple BR, Trejo J. A tyrosine-based sorting signal regulates intracellular trafficking of protease-activated receptor-1: multiple regulatory mechanisms for agonist-induced G protein-coupled receptor internalization. J Biol Chem. 2004 May 21; 279(21):21938-47. PMID: 15023990.
        View in: PubMed
      54. Booden MA, Eckert LB, Der CJ, Trejo J. Persistent signaling by dysregulated thrombin receptor trafficking promotes breast carcinoma cell invasion. Mol Cell Biol. 2004 Mar; 24(5):1990-9. PMID: 14966279.
        View in: PubMed
      55. Gullapalli A, Garrett TA, Paing MM, Griffin CT, Yang Y, Trejo J. A role for sorting nexin 2 in epidermal growth factor receptor down-regulation: evidence for distinct functions of sorting nexin 1 and 2 in protein trafficking. Mol Biol Cell. 2004 May; 15(5):2143-55. PMID: 14978220.
        View in: PubMed
      56. Chen CH, Paing MM, Trejo J. Termination of protease-activated receptor-1 signaling by beta-arrestins is independent of receptor phosphorylation. J Biol Chem. 2004 Mar 12; 279(11):10020-31. PMID: 14699102.
        View in: PubMed
      57. Trejo J. Protease-activated receptors: new concepts in regulation of G protein-coupled receptor signaling and trafficking. J Pharmacol Exp Ther. 2003 Nov; 307(2):437-42. PMID: 12966163.
        View in: PubMed
      58. Wang Y, Zhou Y, Szabo K, Haft CR, Trejo J. Down-regulation of protease-activated receptor-1 is regulated by sorting nexin 1. Mol Biol Cell. 2002 Jun; 13(6):1965-76. PMID: 12058063.
        View in: PubMed
      59. Paing MM, Stutts AB, Kohout TA, Lefkowitz RJ, Trejo J. beta -Arrestins regulate protease-activated receptor-1 desensitization but not internalization or Down-regulation. J Biol Chem. 2002 Jan 11; 277(2):1292-300. PMID: 11694535.
        View in: PubMed
      60. Trejo J, Altschuler Y, Fu HW, Mostov KE, Coughlin SR. Protease-activated receptor-1 down-regulation: a mutant HeLa cell line suggests novel requirements for PAR1 phosphorylation and recruitment to clathrin-coated pits. J Biol Chem. 2000 Oct 6; 275(40):31255-65. PMID: 10893235.
        View in: PubMed
      61. Kahn ML, Diacovo TG, Bainton DF, Lanza F, Trejo J, Coughlin SR. Glycoprotein V-deficient platelets have undiminished thrombin responsiveness and Do not exhibit a Bernard-Soulier phenotype. Blood. 1999 Dec 15; 94(12):4112-21. PMID: 10590056.
        View in: PubMed
      62. Trejo J, Coughlin SR. The cytoplasmic tails of protease-activated receptor-1 and substance P receptor specify sorting to lysosomes versus recycling. J Biol Chem. 1999 Jan 22; 274(4):2216-24. PMID: 9890984.
        View in: PubMed
      63. Trejo J, Hammes SR, Coughlin SR. Termination of signaling by protease-activated receptor-1 is linked to lysosomal sorting. Proc Natl Acad Sci U S A. 1998 Nov 10; 95(23):13698-702. PMID: 9811863; PMCID: PMC24882.
        View in: PubMed
        View in: PubMed Central
      64. Shapiro MJ, Trejo J, Zeng D, Coughlin SR. Role of the thrombin receptor's cytoplasmic tail in intracellular trafficking. Distinct determinants for agonist-triggered versus tonic internalization and intracellular localization. J Biol Chem. 1996 Dec 20; 271(51):32874-80. PMID: 8955127.
        View in: PubMed
      65. Trejo J, Connolly AJ, Coughlin SR. The cloned thrombin receptor is necessary and sufficient for activation of mitogen-activated protein kinase and mitogenesis in mouse lung fibroblasts. Loss of responses in fibroblasts from receptor knockout mice. J Biol Chem. 1996 Aug 30; 271(35):21536-41. PMID: 8702939.
        View in: PubMed
      66. Brown JL, Stowers L, Baer M, Trejo J, Coughlin S, Chant J. Human Ste20 homologue hPAK1 links GTPases to the JNK MAP kinase pathway. Curr Biol. 1996 May 1; 6(5):598-605. PMID: 8805275.
        View in: PubMed
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