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Eunice Kennedy Shriver National Institute of Child Health and Human Development - Section on Cellular Neurobiology - Dr. Peng Loh Lab
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Publications

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 2013

Cheng Y, Cawley NX, Loh YP.  Carboxypeptidase E/NFα1: a new neurotrophic factor against oxidative stress-induced apoptotic cell death mediated by ERK and PI3-K/AKT pathways. PLoS One. 2013 Aug 15;8(8):e71578. doi: 10.1371/journal.pone.0071578. 

Murthy SR, Dupart E, Al-Sweel N, Chen A, Cawley NX, Loh YP. Carboxypeptidase E promotes cancer cell survival, but inhibits migration and invasion. Cancer Lett. 2013 Dec 1;341(2):204-13. doi: 10.1016/j.canlet.2013.08.011. Epub 2013 Aug 11. PMID:23941827

Lee C, Hu J, Ralls S, Kitamura T, Loh YP, Yang Y, Mukouyama YS, Ahn S. The molecular profiles of neural stem cell niche in the adult subventricular zone.  PLoS One. 2012;7(11):e50501. doi: 10.1371/journal.pone.0050501. Epub 2012 Nov 29.

Crippa L, Bianco M, Colombo B, Gasparri AM, Ferrero E, Loh YP, Curnis F, Corti A. A new chromogranin A-dependent angiogenic switch activated by thrombin. Blood. 2013 Jan 10;121(2):392-402. doi: 10.1182/blood-2012-05-430314. Epub 2012 Nov 27.

 

2012

Gondré-Lewis MC, Park JJ, Loh YP. Cellular mechanisms for the biogenesis and transport of synaptic and dense-core vesicles. Int Rev Cell Mol Biol. 2012;299:27-115. doi: 10.1016/B978-0-12-394310-1.00002-3. Review.

Lou H, Park JJ, Phillips A, Loh YP. γ-Adducin promotes process outgrowth and secretory protein exit from the Golgi apparatus. J Mol Neurosci. 2013 Jan;49(1):1-10. doi: 10.1007/s12031-012-9827-0. Epub 2012 Jun 17.

Loh YP, Corti A.  Commentary: granins, secretory granule biogenesis, and transport. J Mol Neurosci. 2012 Oct;48(2):315-6.

Loh YP, Zhou Z, Kao LS. Proceedings of the 16th International Symposium on Chromaffin Cell Biology. J Mol Neurosci. 2012 Oct;48(2):313-4.

Kao LS, Loh YP. Commentary: neurotransmitter secretion and cell signaling. J Mol Neurosci. 2012 Oct;48(2):427-8.

Carbone E, Guérineau NC, Loh YP, Zhou Z. Commentary: ion channels, fusion pores and exocytosis. J Mol Neurosci. 2012 Oct;48(2):357-9.

Tota B, Gentile S, Pasqua T, Bassino E, Koshimizu H, Cawley NX, Cerra MC, Loh YP, Angelone T. The novel chromogranin A-derived serpinin and pyroglutaminated serpinin peptides are positive cardiac β-adrenergic-like inotropes. FASEB J. 2012 Jul;26(7):2888-98. doi: 10.1096/fj.11-201111. Epub 2012 Mar 29.

Cawley NX, Wetsel WC, Murthy SR, Park JJ, Pacak K, Loh YP. New roles of carboxypeptidase E in endocrine and neural function and cancer. Endocr Rev. 2012 Apr;33(2):216-53. doi: 10.1210/er.2011-1039. Epub 2012 Mar 7. Review.

Loh YP, Cheng Y, Mahata SK, Corti A, Tota B. Chromogranin A and derived peptides in health and disease. J Mol Neurosci. 2012 Oct;48(2):347-56. Epub 2012 Mar 3. Review.

Cawley NX, Sridhar M, Hong H, Loh P. Exploring the membrane topology of prohormone convertase 1 in AtT20 Cells: in situ analysis by immunofluorescence microscopy.  F1000Res. 2012 Aug 8;2. doi: 10.12688/f1000research.1-9.v1.

2011

Park JJ, Loh YP. Visualization of peptide secretory vesicles in living nerve cells. Methods Mol Biol. 2011;789:137-45.

Bartolomucci A, Possenti R, Mahata SK, Fischer-Colbrie R, Loh YP, Salton SR. The Extended Granin Family: Structure, Function, and Biomedical Implications. Endocr Rev. 2011 Dec;32(6):755-97. Epub 2011 Aug 23

Cawley NX, Portela-Gomes G, Lou H, Loh YP. Yapsin 1 immunoreactivity in alpha-cells of human pancreatic islets: implications for the processing of human proglucagon by mammalian aspartic proteases. Endocrinol. 2011 Aug;210(2):181-7.

Lee TK, Murthy SR, Cawley NX, Dhanvantari S, Hewitt SM, Lou H, Lau T, Ma S, Huynh T, Wesley RA, Ng IO, Pacak K, Poon RT, Loh YP. An N-terminal truncated carboxypeptidase E splice isoform induces tumor growth and is a biomarker for predicting future metastasis in human cancers. J Clin Invest. 2011 Mar 1;121(3):880-92.

Koshimizu H, Cawley NX, Yergy AL, Loh YP. Role of pGlu-Serpinin, a Novel Chromogranin A-Derived Peptide in Inhibition of Cell Death. J Mol Neurosci. 2011 May 3.

Koshimizu H, Cawley NX, Kim T, Yergey AL, Loh YP. Serpinin: a novel chromogranin A-derived, secreted peptide up-regulates protease nexin-1 expression and granule biogenesis in endocrine cells. Mol Endocrinol. 2011 May;25(5):732-44.

Park JJ, Gondré-Lewis MC, Eiden LE, Loh YP.. A distinct trans-Golgi network subcompartment for sorting of synaptic and granule proteins in neurons and neuroendocrine cells. J Cell Sci. 2011 Mar 1;124(Pt 5):735-44.

2010

Murthy SR, Pacak K, Loh YP. Carboxypeptidase E: elevated expression correlated with tumor growth and metastasis in pheochromocytomas and other cancers. Cell Mol Neurobiol. 2010 Nov;30(8):1377-81.

Voutetakis A, Cotrim AP, Rowzee A, Zheng C, Rathod T, Yanik T, Loh YP, Baum BJ, Cawley NX. Systemic delivery of bioactive glucagon-like peptide 1 after adenoviral-mediated gene transfer in the murine salivary gland.Endocrinology. 2010 Sep;151(9):4566-72. Epub 2010 Jul 7.

Lou H, Park JJ, Cawley NX, Sarcon A, Su L, Adams T, and Loh YP. Carboxypeptidase E Cytoplasmic Tail Mediates Localization of Synaptic Vesicles to the Pre-Active Zone in Hypothalamic Pre-Synaptic Terminals. J Neurochem. 2010 Aug;114(3):886-96. Epub 2010 May 18.

Cawley NX, Yanik T, Woronowicz A, Chang W, Marini JC, Loh YP. Obese carboxypeptidase E knockout mice exhibit multiple defects in peptide hormone processing contributing to low bone mineral density.
Am J Physiol Endocrinol Metab. 2010 Aug;299(2):E189-97. Epub 2010 May 11.

Koshimizu H, Kim T, Cawley NX, Loh YP. Chromogranin A: A new proposal for trafficking, processing and induction of granule biogenesis. Regul Pept 2010 Feb 25;160(1-3):153-9.

Woronowicz A, Cawley NX, Chang SY, Koshimizu H, Phillips AW, Xiong ZG, Loh YP. Carboxypeptidase E knockout mice exhibit abnormal dendritic arborization and spine morphology in central nervous system neurons. J Neurosci Res 2010 Jan;88(1):64-72.

2009

Plum L, Lin HV, Dutia R, Tanaka J, Aizawa KS, Matsumoto M, Kim AJ, Cawley NX, Paik JH, Loh YP, DePinho RA, Wardlaw SL, Accili D.. The obesity susceptibility gene Cpe links FoxO1 signaling in hypothalamic pro-opiomelanocortin neurons with regulation of food intake. Nat Med 2009 Oct;15(10):1195-201.

Zhang X, Zhu J, Loh YP, Berghman LR. Carboxypeptidase E, an essential element of the regulated secretory pathway, is expressed and partially co-localized with chromogranin A in chicken thymus. Cell Tissue Res 2009 Sep;337(3):371-9.

Koshimizu H, Senatorov V, Loh YP, Gozes I. Neuroprotective protein and carboxypeptidase E. J Mol Neurosci 2009 Sep;39(1-2):1-8.

Park JJ, Koshimizu H, Loh YP. Biogenesis and Transport of Secretory Granules to Release Site in Neuroendocrine Cells. J Mol Neurosci 2009 Feb;37(2):151-9.

2008

Park JJ, Loh YP. How Peptide Hormone Vesicles are Transported to the Secretion Site for Exocytosis. Mol Endocrinol 2008 Dec;22(12):2583-95.

Park JJ, Cawley NX, Loh YP. A bi-directional carboxypeptidase E-driven transport mechanism controls BDNF vesicle homeostasis in hippocampal neurons. Mol Cell Neurosci 2008 Sep;39(1):63-73.

Woronowicz A, Koshimizu H, Chang SY, Cawley NX, Hill JM, Rodriguiz RM, Abebe D, Dorfman C, Senatorov V, Zhou A, Xiong ZG, Wetsel WC, Loh YP. Absence of carboxypeptidase E leads to adult hippocampal neuronal degeneration and memory deficits. Hippocampus 2008;18(10):1051-63.

Samuni Y, Zheng C, Cawley NX, Cotrim AP, Loh YP, Baum BJ. Sorting of growth hormone-erythropoietin fusion proteins in rat salivary glands.
Biochem Biophys Res Commun 2008 Aug 15;373(1):136-9.

Arnaoutova I, Cawley NX, Patel N, Kim T, Rathod T, Loh YP. Aquaporin 1 is important for maintaining secretory granule biogenesis in endocrine cells. Mol Endocrinol 2008 Aug;22(8):1924-34.

Samuni Y, Cawley NX, Zheng C, Cotrim AP, Loh YP, Baum BJ. Sorting behavior of a transgenic erythropoietin-growth hormone fusion protein in murine salivary glands. Hum Gene Ther 2008 Mar;19(3):279-86.

Park JJ, Cawley NX, Loh YP. Carboxypeptidase E cytoplasmic tail-driven vesicle transport is key for activity-dependent secretion of peptide hormones. Mol Endocrinol 2008 Apr;22(4):989-1005.

2007

Lou H, Smith AM, Coates LC, Cawley NX, Loh YP, Birch NP. The transmembrane domain of the prohormone convertase PC3: a key motif for targeting to the regulated secretory pathway. Mol Cell Endocrinol 2007 Mar 15;267(1-2):17-25.

Cawley NX, Arnaoutova I, Yanik T, Lou H, Patel N, Loh YP Techniques in neuropeptides processing, trafficking, and secretion. Methods in Neurobiology Humana Press, 2007; 67-96.

2006

Kim T., Gondre-Lewis M., Arnaoutova I., and Loh Y.P. (2006) Dense-core Secretory Granule Biogenesis. Physiology 21:124-33.

Gondre-Lewis M., Petrache H., Wassif C., Harries D., Parsegian A., Porter F., and Loh Y.P. (2006) Abnormal sterols in cholesterol deficiency diseases cause secretory granule malformation and decreased membrane curvature. J Cell Science 1:119:1876-85.

Kim T. and Loh Y.P. (2006) Protease nexin-1 promotes secretory granule biogenesis by preventing granule protein degradation. Mol Biol Cell 17(2):789-98.

Yanik T, Dominguez G, Kuhar MJ, Del Giudice EM, Loh YP. (2006) The Leu34Phe ProCART mutation leads to cocaine- and amphetamine-regulated transcript (CART) deficiency: a possible cause for obesity in humans. Endocrinology 147(1):39-43.

2005

Zhu X., Wu K., Rife L., Cawley N., Brown B., Adams T., Teofilo K., Lillo C., Williams D., Loh Y.P.*, and Craft C. (2005) Carboxypeptidase E is requred for normal synaptic transmission from photoreceptors to the inner retina. J Neurochem 95:1351-1362. *Co-corresponding author.

Kim T. and Loh Y.P. (2005) Chromogranin A: The surprise link between granule biogenesis and hypertension. J Clinical Investigation 115:1711-1713.

Kim T., Zhang C., Sun Z., Wu H., and Loh Y.P. (2005) Chromogranin A deficiency in transgenic mice leads to aberrant chromaffin granule biogenesis. J Neuroscience 25:6958-6961.

Lou H., Kim S-K., Zaitsev E., Snell C., Lu B., and Loh Y.P. (2005) Sorting and activity-dependent secretion of BDNF require interaction of motif with the sorting receptor, carboxypeptidase E. Neuron 45:245-255.

Wang J., Cawley N. X., Voutetakis A., Rodriguez Y., Goldsmith C., Nieman L., Hoque A., Frank S., Snell C., Loh Y.P.*, and B B. (2005) Partial re-direction of transgenic human growth hormone secretion from rat salivary glands. Human Gene Therapy 16:571-583. *Co-corresponding author.

2004

Michael D., Geng X., Cawley N., Loh Y.P., Rhodes C., Drain P., and Chow R. (2004) Fluorescent cargo proteins in pancreatic beta cells: Design determines secretion kinetics at exocytosis. Biophysical Journal 87:L03-L05.

Cawley N.X., Zhou J., Hill J., Abebe D., Romboz S., Yanik T., Rodriguiz R., Wetsel W., and Loh Y.P. (2004) The carboxypeptidase E knockout mouse exhibits endocrinological and behavioral deficits. Endocrinology 145:5807-5819.

Voutetakis, A., Kok, M.R., Zheng, C., Bossis, I., Wang, J., Cotrim, A.P., Marracino, N., Goldsmith, C.M., Chiorini, J.A., Loh, Y.P., Nieman, L.K., and Baum, B.J. (2004) Reengineered salivary glands are stable endogenous bioreactors for systemic gene therapeutics. Proc Natl Acad Sci USA 101:3053-8.

Loh, Y.P., Kim, T., Rodriguez, Y.M., and Cawley, N.X.(2004) Secretory granule biogenesis and neuropeptide sorting to the regulated secretory pathway in neuroendocrine cells. J Mol Neurosci 22:63-71.

Assadi, M., Sharpe, J.C., Snell, C., and Loh, Y.P.(2004) The C-Terminus of Prohormone Convertase 2 Is Sufficient and Necessary for Raft Association and Sorting to the Regulated Secretory Pathway. Biochemistry 43:7798-7807.

2003

Zhang, C.F., Dhanvantari, S., Lou, H., and Loh, Y.P.(2003) Sorting of carboxypeptidase E to the regulated secretory pathway requires interaction of its transmembrane domain with lipid rafts. Biochem J 369:453-60.

Fukuda, M., Kanno, E., Ogata, Y., Saegusa, C., Kim, T., Loh, Y.P., and Yamamoto, A. (2003) Nerve growth factor-dependent sorting of synaptotagmin IV protein to mature dense-core vesicles that undergo calcium-dependent exocytosis in PC12 cells. J Biol Chem 278:3220-6.

Dhanvantari, S., Shen, F.S., Adams, T., Snell, C.R., Zhang, C., Mackin, R.B., Morris, S.J., and Loh, Y.P. (2003) Disruption of a receptor-mediated mechanism for intracellular sorting of proinsulin in familial hyperproinsulinemia. Mol Endocrinol 17:1856-67.

Cawley, N.X., Rodriguez, Y.M., Maldonado, A., and Loh, Y.P. (2003) Trafficking of mutant carboxypeptidase E to secretory granules in a beta-cell line derived from Cpe(fat)/Cpe(fat) mice. Endocrinology 144:292-8.

Cawley, N.X., Chino, M., Maldonado, A., Rodriguez, Y.M., Loh, Y.P., and Ellman, J.A. (2003) Synthesis and characterization of the first potent inhibitor of yapsin 1. Implications for the study of yapsin-like enzymes. J Biol Chem 278:5523-30.

Arnaoutova, I., Jackson, C.L., Al-Awar, O.S., Donaldson, J.G., and Loh, Y.P. (2003) Recycling of Raft-associated prohormone sorting receptor carboxypeptidase E requires interaction with ARF6. Mol Biol Cell 14:4448-57.

Arnaoutova, I., Smith, A.M., Coates, L.C., Sharpe, J.C., Dhanvantari, S., Snell, C.R., Birch, N.P., and Loh, Y.P. (2003) The prohormone processing enzyme PC3 is a lipid raft-associated transmembrane protein. Biochemistry 42:10445-55.

2002

Loh, Y.P., Maldonado, A., Zhang, C., Tam, W.H., and Cawley, N. (2002) Mechanism of sorting proopiomelanocortin and proenkephalin to the regulated secretory pathway of neuroendocrine cells. Ann N Y Acad Sci 971:416-25.

Kim, T., Tao-Cheng, J.H., Eiden, L.E., and Loh, Y.P. (2002) Large dense-core secretory granule biogenesis is under the control of chromogranin A in neuroendocrine cells. Ann N Y Acad Sci 971:323-31.

Dhanvantari, S., Arnaoutova, I., Snell, C.R., Steinbach, P.J., Hammond, K., Caputo, G.A., London, E., and Loh, Y.P. (2002) Carboxypeptidase E, a prohormone sorting receptor, is anchored to secretory granules via a C-terminal transmembrane insertion. Biochemistry 41:52-60.

2001

Kim, T., Tao-Cheng, J-H, Eiden, L.E. and Loh, Y.P. (2001) Chromogranin A, an "on/off" switch controlling dense-core secretory granule biogenesis. Cell 106:499-509

Shen F.S., Snell C.R. and Loh Y.P. (2001) A novel sorting motif targets proinsulin into the regulated secretory pathway. (submission to Nature)

Cawley N.X., Tam W.W.H. and Y.P. Loh. (2001) Mutant carboxypeptidase E targets proinsulin to the regulated secretory pathway in a ß-cell line derived from Cpefat/Cpefat mice. J Biological Chemistry (under revision for J Biologial Chemistry)

2000

Dhanvantari S. and Loh Y.P. (2000) Lipid raft association of carboxypeptidase E is necessary for its function as a regulated secretory pathway sorting receptor. J Biological Chemistry 275:29887-29893.

Olsen V. and Loh Y.P. (2000) In vitro processing of nonanchored yapsin 1. Arch Biochem and Biophys 375:315-321

Cawley NX, Normant E, Chen A, Loh YP. (2000) Oligomerization of pro-opiomelanocortin is independent of pH, calcium and the sorting signal for the regulated secretory pathway. FEBS Lett 481(1):37-41.

1999

Shen FS, Aguilera G, and Loh Y.P. (1999) Altered biosynthesis and secretion of pro-opiomelanocortin in the intermediate and anterior pituitary of Carboxypeptidase E - defficient Cpe fat / Cpe fat mice. Neuropeptides 33:276-280.

Olsen V., Cawley N., Brandt J., Egel-Mitani M., and Loh Y.P. (1999) Identification and characterization of Saccharomyces cerevisiae yapsin 3, a new member of the yapsin aspartic proteases encoded by the YPS3 gene. Biochemical J 339:407-411.

Zhang C-F., Snell C.R. and Loh Y.P. (1999). Identification of a novel prohormone binding site on carboxypeptidase E, a regulated secretory pathway sorting receptor. Mol Endocrinol 13:527-536.

1998

Cool D.R. and Loh Y.P. (1998) Carboxypeptidase E is a sorting receptor for prohormones: Binding and kinetic studies. Molecular and Cellular Endocrinology 139:7-13.

Normant E. and Loh Y.P. (1998) Depletion of Carboxypeptidase E, a regulated secretory pathway sorting receptor causes misrouting and constitutive secretion of proinsulin and proenkephalin, but not chromogranin A. Endocrinology 139:2137-2145.

Olsen V., Guruprasad K., Cawley N.X., Chen H-C., Blundell T.L. and Loh Y.P. (1998) Cleavage efficiency of the novel aspartic protease yapsin 1 (yap3p) enhanced for sustrates with arginine residues flanking the P1 site: Correlation with electronegative active site pockets identified by molecular modeling. Biochemistry 37:4168-4176.

1997

Ting P., Cushenberry P.A., Friedman T.C. and Loh Y.P. (1997) Enhanced Brain Opioid Receptor Activity Precedes Blood-Brain Barrier Disruption. Acta Neurochir 70:250-253.

Cawley N.X., Olsen V., Zhang C.F., Chen H-C., Tan M., and Loh Y.P. (1997) Yapsin 1 (Yap 3p): Activation and processing of non-anchored Yapsin 1 (Yap3p). J Biol Chem 273:584-591.

Shen F-S., and Loh Y.P. (1997) Intracellular misrouting and Abnormal Secretion of Adrencorticortropin and Growth Hormone in Cpefat Mice Associated with a Carboxypeptidase E Mutation. Proc Natl Acad Sci USA 94:5314-5319.

Lecchi P., Loh Y.P., Snell C.R., and Pannell L.K. (1997) The structure of synenkephalin (pro-enkephalin 1-73) is dictated by three disulfide bridges. Biochem, Biophys Res Commun 232:800-80.

Chodobski A., Loh Y.P., Corsetti S., Szmydynger-Chodobska J., Johanson C.E., Lim Y-P., and Monfils P.R. (1997) The presence of arginine vasopressin and its mRNA in rat choroid plexus epithelium. Mol Brain Res 48:67-72.

Cool D.R., Normant E., Shen F-S., Chen H-C., Pannell L., Zhang Y., and Loh Y.P. (1997) Carboxypeptiase E is a regulated secretory pathway sorting receptor: Genetic obliteration leads to endocrine disorders in Cpefat mice. Cell 88:73-83.