Bruce D. Carter, Ph.D.


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Faculty Appointments
Professor of Biochemistry
Ph.D., Biological Chemistry, University of Michigan, Ann Arbor, MichiganB.S., Biology/Chemistry, Alma College, Alma, Michigan
Office Address
625 Light Hall
Nashville, TN 0146
Research Description
I. Mechanisms of neurotrophin signaling through the p75 receptor: Our lab studies the signaling mechanisms regulating neuronal survival. Programmed cell death in the nervous system is a naturally occurring process in mammalian development; however, abnormal apoptosis is the basis for many neuropathologies, e.g. Alzheimer''s and Parkinson''s disease and ischemic injury. The delicate balance between neuronal survival and death is regulated, in part, by a family of growth factors referred to as the neurotrophins. The target tissues to which the neurons project produce members of this family of trophic factors. The neurotrophins promote neuronal survival and differentiation through binding to the Trks, a family of tyrosine kinase receptors, and induce apoptosis through a 75kD receptor, p75. While significant progress has been made in elucidating the mechanisms by which the Trks promote survival, much less is known about how p75 induces cell death. We recently discovered that pro-death ligands promote p75 cleavage by ¿secretase, which releases a transcription factor, NRIF, to enter the nucleus. This process is required for the receptor''s apoptotic signal.This research will reveal the mechanisms underlying normal mammalian neural development and function. Moreover, understanding the regulation of neural cell survival is essential for developing therapeutic strategies for neuropathologies involving apoptosis, which include many diseases and nerve lesions.

II. Process by which apoptotic neurons are phagocytosed: Following the extensive apoptosis that occurs during development of the nervous system, the resulting neuronal corpses must be efficiently removed to prevent an inflammatory response, which can eventually lead to autoimmunity. Unfortunately, the molecular mechanisms underlying this phagocytic process in the nervous system are poorly understood. We recently demonstrated that satellite glial precursor cells are the primary phagocytes that engulf the many neuronal corpses in the developing dorsal root ganglia (DRG) and identified a novel engulfment receptor, Jedi1, as mediating the engulfment by glial precursors. Current efforts are aimed at determining the mechanisms by which Jedi1 signals engulfment and investigating its role in regulating phagocytosis in other regions of the developing nervous system.

III. Molecular mechanisms of myelin formation: The other area of research in the lab is to elucidate the mechanism by which myelin forms. Myelin is a multilamellar structure that ensheaths axons and allows for the rapid conduction of electrical signals, acts as a protective barrier for axons, regulates regeneration and provides trophic support for neurons. This structure is produced by Schwann cells in the peripheral nervous system and oligodendrocytes in the CNS. The formation of peripheral myelin during development is initiated by yet to be identified signals from the axon with which the Schwann cells are associated. The overall objective of this project is to elucidate the mechanisms regulating the formation of this essential neural structure. We found that activation of the transcription factor NF-¿B in Schwann cells is a critical factor for their differentiation into a myelinating phenotype and are currently investigating the role of NFkB in the normal differentiation process and in models of demyelinating neuropathies.
Research Keywords
neurotrophin, nerve growth factor, apoptosis, p75, NRIF, Trk, Jedi, phagocytosis, neuron, myelin, Schwann, NF kappa B, sympathetic, dorsal root ganglia, neuroscience, neurobiology, neurodevelopment, neurodegeneration, axonal trafficking, microglia
Trinh VQ, Roland JT, Wong J, Revetta F, Patel K, Shi C, DelGiorno KE, Carter BD, Tan MCB. Peak density of immature nerve cells occurs with high-grade dysplasia in intraductal papillary mucinous neoplasms of the pancreas. J Pathol [print-electronic]. 2022 Sep; 258(1): 69-82. PMID: 35686747, PMCID: PMC9378585, DOI: 10.1002/path.5978, ISSN: 1096-9896.

Follis RM, Tep C, Genaro-Mattos TC, Kim ML, Ryu JC, Morrison VE, Chan JR, Porter N, Carter BD, Yoon SO. Metabolic Control of Sensory Neuron Survival by the p75 Neurotrophin Receptor in Schwann Cells. J Neurosci [print-electronic]. 2021 Oct 10/20/2021; 41(42): 8710-24. PMID: 34507952, PMCID: PMC8528492, PII: JNEUROSCI.3243-20.2021, DOI: 10.1523/JNEUROSCI.3243-20.2021, ISSN: 1529-2401.

Marinko JT, Carter BD, Sanders CR. Direct relationship between increased expression and mistrafficking of the Charcot-Marie-Tooth-associated protein PMP22. J Biol Chem [print-electronic]. 2020 Aug 8/21/2020; 295(34): 11963-70. PMID: 32647009, PMCID: PMC7443497, PII: S0021-9258(17)50059-9, DOI: 10.1074/jbc.AC120.014940, ISSN: 1083-351X.

Pathak A, Clark S, Bronfman FC, Deppmann CD, Carter BD. Long-distance regressive signaling in neural development and disease. Wiley Interdiscip Rev Dev Biol [print-electronic]. 2020 May 5/11/2020; e382. PMID: 32391977, DOI: 10.1002/wdev.382, ISSN: 1759-7692.

DeSisto JA, Flannery P, Lemma R, Pathak A, Mestnik S, Philips N, Bales NJ, Kashyap T, Moroze E, Venkataraman S, Kung AL, Carter BD, Landesman Y, Vibhakar R, Green AL. Exportin 1 Inhibition Induces Nerve Growth Factor Receptor Expression to Inhibit the NF-¿B Pathway in Preclinical Models of Pediatric High-Grade Glioma. Mol. Cancer Ther [print-electronic]. 2020 Feb; 19(2): 540-51. PMID: 31594826, PMCID: PMC7007851, PII: 1535-7163.MCT-18-1319, DOI: 10.1158/1535-7163.MCT-18-1319, ISSN: 1538-8514.

Aravamudhan P, Raghunathan K, Konopka-Anstadt J, Pathak A, Sutherland DM, Carter BD, Dermody TS. Reovirus uses macropinocytosis-mediated entry and fast axonal transport to infect neurons. PLoS Pathog. 2020 Feb; 16(2): e1008380. PMID: 32109948, PMCID: PMC7065821, PII: PPATHOGENS-D-19-01848, DOI: 10.1371/journal.ppat.1008380, ISSN: 1553-7374.

Trevisan AJ, Bauer MB, Brindley RL, Currie KPM, Carter BD. Jedi-1 deficiency increases sensory neuron excitability through a non-cell autonomous mechanism. Sci Rep. 2020 Jan 1/28/2020; 10(1): 1300. PMID: 31992767, PMCID: PMC6987110, PII: 10.1038/s41598-020-57971-2, DOI: 10.1038/s41598-020-57971-2, ISSN: 2045-2322.

Vanoye CG, Sakakura M, Follis RM, Trevisan AJ, Narayan M, Li J, Sanders CR, Carter BD. Peripheral myelin protein 22 modulates store-operated calcium channel activity, providing insights into Charcot-Marie-Tooth disease etiology. J. Biol. Chem [print-electronic]. 2019 Aug 8/9/2019; 294(32): 12054-65. PMID: 31213528, PMCID: PMC6690708, PII: RA118.006248, DOI: 10.1074/jbc.RA118.006248, ISSN: 1083-351X.

Pathak A, Stanley EM, Hickman FE, Wallace N, Brewer B, Li D, Gluska S, Perlson E, Fuhrmann S, Akassoglou K, Bronfman F, Casaccia P, Burnette DT, Carter BD. Retrograde Degenerative Signaling Mediated by the p75 Neurotrophin Receptor Requires p150Glued Deacetylation by Axonal HDAC1. Dev. Cell. 2018 Aug 8/6/2018; 46(3): 376-387.e7. PMID: 30086304, PMCID: PMC6093198, PII: S1534-5807(18)30554-9, DOI: 10.1016/j.devcel.2018.07.001, ISSN: 1878-1551.

Pathak A, Stanley EM, Hickman FE, Wallace N, Brewer B, Li D, Gluska S, Perlson E, Fuhrmann S, Akassoglou K, Bronfman F, Casaccia P, Burnette DT, Carter BD. Retrograde Degenerative Signaling Mediated by the p75 Neurotrophin Receptor Requires p150Glued Deacetylation by Axonal HDAC1. Dev. Cell. 2018 Aug 8/6/2018; 46(3): 376-387.e7. PMID: 30086304, PMCID: PMC6093198, PII: S1534-5807(18)30554-9, DOI: 10.1016/j.devcel.2018.07.001, ISSN: 1878-1551.

Hickman FE, Stanley EM, Carter BD. Neurotrophin Responsiveness of Sympathetic Neurons Is Regulated by Rapid Mobilization of the p75 Receptor to the Cell Surface through TrkA Activation of Arf6. J. Neurosci [print-electronic]. 2018 Jun 6/13/2018; 38(24): 5606-19. PMID: 29789375, PMCID: PMC6001035, PII: JNEUROSCI.0788-16.2018, DOI: 10.1523/JNEUROSCI.0788-16.2018, ISSN: 1529-2401.

Hickman FE, Stanley EM, Carter BD. Neurotrophin Responsiveness of Sympathetic Neurons Is Regulated by Rapid Mobilization of the p75 Receptor to the Cell Surface through TrkA Activation of Arf6. J. Neurosci [print-electronic]. 2018 Jun 6/13/2018; 38(24): 5606-19. PMID: 29789375, PMCID: PMC6001035, PII: JNEUROSCI.0788-16.2018, DOI: 10.1523/JNEUROSCI.0788-16.2018, ISSN: 1529-2401.

Chaudhry N, Bachelin C, Zujovic V, Hilaire M, Baldwin KT, Follis RM, Giger R, Carter BD, Baron-Van Evercooren A, Filbin MT. Myelin-Associated Glycoprotein Inhibits Schwann Cell Migration and Induces Their Death. J. Neurosci [print-electronic]. 2017 Jun 6/14/2017; 37(24): 5885-99. PMID: 28522736, PMCID: PMC5473206, PII: JNEUROSCI.1822-16.2017, DOI: 10.1523/JNEUROSCI.1822-16.2017, ISSN: 1529-2401.

Novaleski CK, Carter BD, Sivasankar MP, Ridner SH, Dietrich MS, Rousseau B. Apoptosis and Vocal Fold Disease: Clinically Relevant Implications of Epithelial Cell Death. J. Speech Lang. Hear. Res. 2017 May 5/24/2017; 60(5): 1264-72. PMID: 28492834, PII: 2627560, DOI: 10.1044/2016_JSLHR-S-16-0326, ISSN: 1558-9102.

Yang YP, Ma H, Starchenko A, Huh WJ, Li W, Hickman FE, Zhang Q, Franklin JL, Mortlock DP, Fuhrmann S, Carter BD, Ihrie RA, Coffey RJ. A Chimeric Egfr Protein Reporter Mouse Reveals Egfr Localization and Trafficking In Vivo. Cell Rep. 2017 May 5/9/2017; 19(6): 1257-67. PMID: 28494873, PMCID: PMC5517093, PII: S2211-1247(17)30542-9, DOI: 10.1016/j.celrep.2017.04.048, ISSN: 2211-1247.

Pathak A, Carter BD. Retrograde apoptotic signaling by the p75 neurotrophin receptor. Neuronal Signal. 2017 Feb; 1(1): NS20160007. PMID: 32714573, PMCID: PMC7373242, PII: NS20160007, DOI: 10.1042/NS20160007, ISSN: 2059-6553.

Follis RM, Carter BD. Myelin Avoids the JAM. Neuron. 2016 Aug 8/17/2016; 91(4): 713-6. PMID: 27537479, PII: S0896-6273(16)30466-4, DOI: 10.1016/j.neuron.2016.08.003, ISSN: 1097-4199.

Yazlovitskaya EM, Tseng HY, Viquez O, Tu T, Mernaugh G, McKee KK, Riggins K, Quaranta V, Pathak A, Carter BD, Yurchenco P, Sonnenberg A, Böttcher RT, Pozzi A, Zent R. Integrin a3ß1 regulates kidney collecting duct development via TRAF6-dependent K63-linked polyubiquitination of Akt. Mol. Biol. Cell [print-electronic]. 2015 May 5/15/2015; 26(10): 1857-74. PMID: 25808491, PMCID: PMC4436831, PII: mbc.E14-07-1203, DOI: 10.1091/mbc.E14-07-1203, ISSN: 1939-4586.

Mobley BC, Kwon M, Kraemer BR, Hickman FE, Qiao J, Chung DH, Carter BD. Expression of MYCN in Multipotent Sympathoadrenal Progenitors Induces Proliferation and Neural Differentiation, but Is Not Sufficient for Tumorigenesis. PLoS ONE. 2015; 10(7): e0133897. PMID: 26222553, PMCID: PMC4519318, PII: PONE-D-15-06683, DOI: 10.1371/journal.pone.0133897, ISSN: 1932-6203.

Kraemer BR, Snow JP, Vollbrecht P, Pathak A, Valentine WM, Deutch AY, Carter BD. A role for the p75 neurotrophin receptor in axonal degeneration and apoptosis induced by oxidative stress. J. Biol. Chem [print-electronic]. 2014 Aug 8/1/2014; 289(31): 21205-16. PMID: 24939843, PMCID: PMC4118083, PII: M114.563403, DOI: 10.1074/jbc.M114.563403, ISSN: 1083-351X.

Sullivan CS, Scheib JL, Ma Z, Dang RP, Schafer JM, Hickman FE, Brodsky FM, Ravichandran KS, Carter BD. The adaptor protein GULP promotes Jedi-1-mediated phagocytosis through a clathrin-dependent mechanism. Mol. Biol. Cell [print-electronic]. 2014 Jun 6/15/2014; 25(12): 1925-36. PMID: 24743597, PMCID: PMC4055271, PII: mbc.E13-11-0658, DOI: 10.1091/mbc.E13-11-0658, ISSN: 1939-4586.

Escudero CA, Lazo OM, Galleguillos C, Parraguez JI, Lopez-Verrilli MA, Cabeza C, Leon L, Saeed U, Retamal C, Gonzalez A, Marzolo MP, Carter BD, Court FA, Bronfman FC. The p75 neurotrophin receptor evades the endolysosomal route in neuronal cells, favouring multivesicular bodies specialised for exosomal release. J. Cell. Sci [print-electronic]. 2014 May 5/1/2014; 127(Pt 9): 1966-79. PMID: 24569882, PMCID: PMC4004974, PII: jcs.141754, DOI: 10.1242/jcs.141754, ISSN: 1477-9137.

Forsyth PA, Krishna N, Lawn S, Valadez JG, Qu X, Fenstermacher DA, Fournier M, Potthast L, Chinnaiyan P, Gibney GT, Zeinieh M, Barker PA, Carter BD, Cooper MK, Kenchappa RS. P75 neurotrophin receptor cleavage by a- and ¿-secretases is required for neurotrophin-mediated proliferation of brain tumor-initiating cells. J. Biol. Chem [print-electronic]. 2014 Mar 3/21/2014; 289(12): 8067-85. PMID: 24519935, PMCID: PMC3961639, PII: M113.513762, DOI: 10.1074/jbc.M113.513762, ISSN: 1083-351X.

Guo J, Wang L, Zhang Y, Wu J, Arpag S, Hu B, Imhof BA, Tian X, Carter BD, Suter U, Li J. Abnormal junctions and permeability of myelin in PMP22-deficient nerves. Ann. Neurol [print-electronic]. 2014 Feb; 75(2): 255-65. PMID: 24339129, PMCID: PMC4206215, DOI: 10.1002/ana.24086, ISSN: 1531-8249.

Kraemer BR, Yoon SO, Carter BD. The biological functions and signaling mechanisms of the p75 neurotrophin receptor. Handb Exp Pharmacol. 2014; 220: 121-64. PMID: 24668472, DOI: 10.1007/978-3-642-45106-5_6, ISSN: 0171-2004.

Lewin GR, Carter BD. Neurotrophic factors. Preface [editorial]. Handb Exp Pharmacol. 2014; 220: v-vi. PMID: 24941498, ISSN: 0171-2004.

Schlebach JP, Peng D, Kroncke BM, Mittendorf KF, Narayan M, Carter BD, Sanders CR. Reversible folding of human peripheral myelin protein 22, a tetraspan membrane protein. Biochemistry [print-electronic]. 2013 May 5/14/2013; 52(19): 3229-41. PMID: 23639031, PMCID: PMC3762913, DOI: 10.1021/bi301635f, ISSN: 1520-4995.

Limpert AS, Bai S, Narayan M, Wu J, Yoon SO, Carter BD, Lu QR. NF-¿B forms a complex with the chromatin remodeler BRG1 to regulate Schwann cell differentiation. J. Neurosci. 2013 Feb 2/6/2013; 33(6): 2388-97. PMID: 23392668, PMCID: PMC3711599, PII: 33/6/2388, DOI: 10.1523/JNEUROSCI.3223-12.2013, ISSN: 1529-2401.

Wei C, Thatcher EJ, Olena AF, Cha DJ, Perdigoto AL, Marshall AF, Carter BD, Broadie K, Patton JG. MiR-153 regulates SNAP-25, synaptic transmission, and neuronal development. PLoS ONE [print-electronic]. 2013; 8(2): e57080. PMID: 23451149, PMCID: PMC3581580, PII: PONE-D-12-37460, DOI: 10.1371/journal.pone.0057080, ISSN: 1932-6203.

Scheib JL, Sullivan CS, Carter BD. Jedi-1 and MEGF10 signal engulfment of apoptotic neurons through the tyrosine kinase Syk. J. Neurosci. 2012 Sep 9/19/2012; 32(38): 13022-31. PMID: 22993420, PMCID: PMC3464495, PII: 32/38/13022, DOI: 10.1523/JNEUROSCI.6350-11.2012, ISSN: 1529-2401.

Benesh AE, Fleming JT, Chiang C, Carter BD, Tyska MJ. Expression and localization of myosin-1d in the developing nervous system. Brain Res [print-electronic]. 2012 Feb 2/27/2012; 1440: 9-22. PMID: 22284616, PMCID: PMC3278530, PII: S0006-8993(11)02323-7, DOI: 10.1016/j.brainres.2011.12.054, ISSN: 1872-6240.

Tep C, Kim ML, Opincariu LI, Limpert AS, Chan JR, Appel B, Carter BD, Yoon SO. Brain-derived neurotrophic factor (BDNF) induces polarized signaling of small GTPase (Rac1) protein at the onset of Schwann cell myelination through partitioning-defective 3 (Par3) protein. J. Biol. Chem [print-electronic]. 2012 Jan 1/6/2012; 287(2): 1600-8. PMID: 22128191, PMCID: PMC3256919, PII: M111.312736, DOI: 10.1074/jbc.M111.312736, ISSN: 1083-351X.

Duggan KC, Hermanson DJ, Musee J, Prusakiewicz JJ, Scheib JL, Carter BD, Banerjee S, Oates JA, Marnett LJ. (R)-Profens are substrate-selective inhibitors of endocannabinoid oxygenation by COX-2. Nat. Chem. Biol. 2011 Nov; 7(11): 803-9. PMID: 22053353, PMCID: PMC3298755, ISSN: 1552-4469.

Astuti D, Ricketts CJ, Chowdhury R, McDonough MA, Gentle D, Kirby G, Schlisio S, Kenchappa RS, Carter BD, Kaelin WG, Ratcliffe PJ, Schofield CJ, Latif F, Maher ER. Mutation analysis of HIF prolyl hydroxylases (PHD/EGLN) in individuals with features of phaeochromocytoma and renal cell carcinoma susceptibility. Endocr. Relat. Cancer [electronic-print]. 2011 Feb; 18(1): 73-83. PMID: 20959442, PMCID: PMC3006001, PII: ERC-10-0113, DOI: 10.1677/ERC-10-0113, ISSN: 1479-6821.

Perdigoto AL, Chaudhry N, Barnes GN, Filbin MT, Carter BD. A novel role for PTEN in the inhibition of neurite outgrowth by myelin-associated glycoprotein in cortical neurons. Mol. Cell. Neurosci [print-electronic]. 2011 Jan; 46(1): 235-44. PMID: 20869442, PMCID: PMC3018674, PII: S1044-7431(10)00226-5, DOI: 10.1016/j.mcn.2010.09.006, ISSN: 1095-9327.

Kenchappa RS, Tep C, Korade Z, Urra S, Bronfman FC, Yoon SO, Carter BD. P75 neurotrophin receptor-mediated apoptosis in sympathetic neurons involves a biphasic activation of JNK and up-regulation of tumor necrosis factor-alpha-converting enzyme/ADAM17. J. Biol. Chem [print-electronic]. 2010 Jun 6/25/2010; 285(26): 20358-68. PMID: 20421303, PMCID: PMC2888447, PII: M109.082834, DOI: 10.1074/jbc.M109.082834, ISSN: 1083-351X.

Carter BD, Feng N, Paolocci N. The p75 neurotrophin receptor, semaphorins, and sympathetic traffic in the heart [editorial]. Am. J. Physiol. Heart Circ. Physiol [print-electronic]. 2010 Jun; 298(6): H1633-6. PMID: 20304820, PMCID: PMC2886656, PII: 00253.2010, DOI: 10.1152/ajpheart.00253.2010, ISSN: 1522-1539.

Limpert AS, Carter BD. Axonal neuregulin 1 type III activates NF-kappaB in Schwann cells during myelin formation. J. Biol. Chem [print-electronic]. 2010 May 5/28/2010; 285(22): 16614-22. PMID: 20360002, PMCID: PMC2878070, PII: M109.098780, DOI: 10.1074/jbc.M109.098780, ISSN: 1083-351X.

Scheib JL, Carter BD. Eaters of the dead: glial precursors clear neuron corpses during development [editorial]. Cell Cycle [print-electronic]. 2010 May 5/15/2010; 9(10): 1867-8. PMID: 20436291, PMCID: PMC3093807, PII: 11678, ISSN: 1551-4005.

Carter BD. Degeneration keeps axons on the straight and narrow. Nat. Neurosci. 2010 May; 13(5): 526-8. PMID: 20421896, PII: nn0510-526, DOI: 10.1038/nn0510-526, ISSN: 1546-1726.

Wu HH, Bellmunt E, Scheib JL, Venegas V, Burkert C, Reichardt LF, Zhou Z, Fariñas I, Carter BD. Glial precursors clear sensory neuron corpses during development via Jedi-1, an engulfment receptor. Nat. Neurosci [print-electronic]. 2009 Dec; 12(12): 1534-41. PMID: 19915564, PMCID: PMC2834222, PII: nn.2446, DOI: 10.1038/nn.2446, ISSN: 1546-1726.

Vilar M, Charalampopoulos I, Kenchappa RS, Reversi A, Klos-Applequist JM, Karaca E, Simi A, Spuch C, Choi S, Friedman WJ, Ericson J, Schiavo G, Carter BD, Ibáñez CF. Ligand-independent signaling by disulfide-crosslinked dimers of the p75 neurotrophin receptor. J. Cell. Sci [print-electronic]. 2009 Sep 9/15/2009; 122(Pt 18): 3351-7. PMID: 19706676, PMCID: PMC2736866, PII: jcs.055061, DOI: 10.1242/jcs.055061, ISSN: 1477-9137.

Korade Z, Kenchappa RS, Mirnics K, Carter BD. NRIF is a regulator of neuronal cholesterol biosynthesis genes. J. Mol. Neurosci [print-electronic]. 2009 Jun; 38(2): 152-8. PMID: 18677445, PMCID: PMC3118441, DOI: 10.1007/s12031-008-9136-9, ISSN: 0895-8696.

Vilar M, Charalampopoulos I, Kenchappa RS, Simi A, Karaca E, Reversi A, Choi S, Bothwell M, Mingarro I, Friedman WJ, Schiavo G, Bastiaens PI, Verveer PJ, Carter BD, Ibáñez CF. Activation of the p75 neurotrophin receptor through conformational rearrangement of disulphide-linked receptor dimers. Neuron. 2009 Apr 4/16/2009; 62(1): 72-83. PMID: 19376068, PMCID: PMC2810632, PII: S0896-6273(09)00165-2, DOI: 10.1016/j.neuron.2009.02.020, ISSN: 1097-4199.

Antar AA, Konopka JL, Campbell JA, Henry RA, Perdigoto AL, Carter BD, Pozzi A, Abel TW, Dermody TS. Junctional adhesion molecule-A is required for hematogenous dissemination of reovirus. Cell Host Microbe. 2009 Jan 1/22/2009; 5(1): 59-71. PMID: 19154988, PMCID: PMC2642927, PII: S1931-3128(08)00398-3, DOI: 10.1016/j.chom.2008.12.001, ISSN: 1934-6069.

Bertrand MJ, Kenchappa RS, Andrieu D, Leclercq-Smekens M, Nguyen HN, Carter BD, Muscatelli F, Barker PA, De Backer O. NRAGE, a p75NTR adaptor protein, is required for developmental apoptosis in vivo. Cell Death Differ [print-electronic]. 2008 Dec; 15(12): 1921-9. PMID: 18772898, PMCID: PMC2735073, PII: cdd2008127, DOI: 10.1038/cdd.2008.127, ISSN: 1476-5403.

Volosin M, Trotter C, Cragnolini A, Kenchappa RS, Light M, Hempstead BL, Carter BD, Friedman WJ. Induction of proneurotrophins and activation of p75NTR-mediated apoptosis via neurotrophin receptor-interacting factor in hippocampal neurons after seizures. J. Neurosci. 2008 Sep 9/24/2008; 28(39): 9870-9. PMID: 18815271, PMCID: PMC2578816, PII: 28/39/9870, DOI: 10.1523/JNEUROSCI.2841-08.2008, ISSN: 1529-2401.

Yoon C, Korade Z, Carter BD. Protein kinase A-induced phosphorylation of the p65 subunit of nuclear factor-kappaB promotes Schwann cell differentiation into a myelinating phenotype. J. Neurosci. 2008 Apr 4/2/2008; 28(14): 3738-46. PMID: 18385332, PII: 28/14/3738, DOI: 10.1523/JNEUROSCI.4439-07.2008, ISSN: 1529-2401.

Schlisio S, Kenchappa RS, Vredeveld LC, George RE, Stewart R, Greulich H, Shahriari K, Nguyen NV, Pigny P, Dahia PL, Pomeroy SL, Maris JM, Look AT, Meyerson M, Peeper DS, Carter BD, Kaelin WG. The kinesin KIF1Bbeta acts downstream from EglN3 to induce apoptosis and is a potential 1p36 tumor suppressor. Genes Dev [print-electronic]. 2008 Apr 4/1/2008; 22(7): 884-93. PMID: 18334619, PMCID: PMC2279200, PII: gad.1648608, DOI: 10.1101/gad.1648608, ISSN: 0890-9369.

Hundahl CA, Allen GC, Nyengaard JR, Dewilde S, Carter BD, Kelsen J, Hay-Schmidt A. Neuroglobin in the rat brain: localization. Neuroendocrinology [print-electronic]. 2008; 88(3): 173-82. PMID: 18451642, PII: 000129698, DOI: 10.1159/000129698, ISSN: 1423-0194.

Qu S, Rinehart C, Wu HH, Wang SE, Carter B, Xin H, Kotlikoff M, Arteaga CL. Gene targeting of ErbB3 using a Cre-mediated unidirectional DNA inversion strategy. Genesis. 2006 Oct; 44(10): 477-86. PMID: 16991114, DOI: 10.1002/dvg.20243, ISSN: 1526-954X.

Kenchappa RS, Zampieri N, Chao MV, Barker PA, Teng HK, Hempstead BL, Carter BD. Ligand-dependent cleavage of the P75 neurotrophin receptor is necessary for NRIF nuclear translocation and apoptosis in sympathetic neurons. Neuron. 2006 Apr 4/20/2006; 50(2): 219-32. PMID: 16630834, PII: S0896-6273(06)00179-6, DOI: 10.1016/j.neuron.2006.03.011, ISSN: 0896-6273.

Carter BD. A Bex-cycle built for two. EMBO Rep. 2006 Apr; 7(4): 382-4. PMID: 16585938, PMCID: PMC1456923, PII: 7400675, DOI: 10.1038/sj.embor.7400675, ISSN: 1469-221X.

Geetha T, Kenchappa RS, Wooten MW, Carter BD. TRAF6-mediated ubiquitination regulates nuclear translocation of NRIF, the p75 receptor interactor. EMBO J [print-electronic]. 2005 Nov 11/16/2005; 24(22): 3859-68. PMID: 16252010, PMCID: PMC1283944, PII: 7600845, DOI: 10.1038/sj.emboj.7600845, ISSN: 0261-4189.

Lee S, Nakamura E, Yang H, Wei W, Linggi MS, Sajan MP, Farese RV, Freeman RS, Carter BD, Kaelin WG, Schlisio S. Neuronal apoptosis linked to EglN3 prolyl hydroxylase and familial pheochromocytoma genes: developmental culling and cancer. Cancer Cell. 2005 Aug; 8(2): 155-67. PMID: 16098468, PII: S1535-6108(05)00224-2, DOI: 10.1016/j.ccr.2005.06.015, ISSN: 1535-6108.

Linggi MS, Burke TL, Williams BB, Harrington A, Kraemer R, Hempstead BL, Yoon SO, Carter BD. Neurotrophin receptor interacting factor (NRIF) is an essential mediator of apoptotic signaling by the p75 neurotrophin receptor. J. Biol. Chem [print-electronic]. 2005 Apr 4/8/2005; 280(14): 13801-8. PMID: 15668238, PII: M410435200, DOI: 10.1074/jbc.M410435200, ISSN: 0021-9258.

Yeiser EC, Rutkoski NJ, Naito A, Inoue J, Carter BD. Neurotrophin signaling through the p75 receptor is deficient in traf6-/- mice. J. Neurosci. 2004 Nov 11/17/2004; 24(46): 10521-9. PMID: 15548667, PII: 24/46/10521, DOI: 10.1523/JNEUROSCI.1390-04.2004, ISSN: 1529-2401.

Gentry JJ, Rutkoski NJ, Burke TL, Carter BD. A functional interaction between the p75 neurotrophin receptor interacting factors, TRAF6 and NRIF. J. Biol. Chem [print-electronic]. 2004 Apr 4/16/2004; 279(16): 16646-56. PMID: 14960584, PII: M309209200, DOI: 10.1074/jbc.M309209200, ISSN: 0021-9258.

Gentry JJ, Barker PA, Carter BD. The p75 neurotrophin receptor: multiple interactors and numerous functions. Prog. Brain Res. 2004; 146: 25-39. PMID: 14699954, PII: S0079-6123(03)46002-0, DOI: 10.1016/S0079-6123(03)46002-0, ISSN: 0079-6123.

Nickols JC, Valentine W, Kanwal S, Carter BD. Activation of the transcription factor NF-kappaB in Schwann cells is required for peripheral myelin formation. Nat. Neurosci. 2003 Feb; 6(2): 161-7. PMID: 12514737, PII: nn995, DOI: 10.1038/nn995, ISSN: 1097-6256.

Fainzilber M, Carter BD. From neurotrophins to immunotrophins. NGF 2002: The 7th international conference on NGF and related molecules. EMBO Rep. 2002 Nov; 3(11): 1029-34. PMID: 12429612, PMCID: PMC1307597, PII: 3/11/1029, DOI: 10.1093/embo-reports/kvf218, ISSN: 1469-221X.

Palmada M, Kanwal S, Rutkoski NJ, Gustafson-Brown C, Johnson RS, Wisdom R, Carter BD. C-jun is essential for sympathetic neuronal death induced by NGF withdrawal but not by p75 activation. J. Cell Biol [print-electronic]. 2002 Aug 8/5/2002; 158(3): 453-61. PMID: 12163468, PMCID: PMC2173823, PII: jcb.200112129, DOI: 10.1083/jcb.200112129, ISSN: 0021-9525.

Dobrowsky RT, Carter BD. P75 neurotrophin receptor signaling: mechanisms for neurotrophic modulation of cell stress?. J. Neurosci. Res. 2000 Aug 8/1/2000; 61(3): 237-43. PMID: 10900070, PII: 10.1002/1097-4547(20000801)61:3<237::AID-JNR1>3.0.CO;2-M, ISSN: 0360-4012.

Gentry JJ, Casaccia-Bonnefil P, Carter BD. Nerve growth factor activation of nuclear factor kappaB through its p75 receptor is an anti-apoptotic signal in RN22 schwannoma cells. J. Biol. Chem. 2000 Mar 3/17/2000; 275(11): 7558-65. PMID: 10713062, ISSN: 0021-9258.

Casademunt E, Carter BD, Benzel I, Frade JM, Dechant G, Barde YA. The zinc finger protein NRIF interacts with the neurotrophin receptor p75(NTR) and participates in programmed cell death. EMBO J. 1999 Nov 11/1/1999; 18(21): 6050-61. PMID: 10545116, PMCID: PMC1171670, DOI: 10.1093/emboj/18.21.6050, ISSN: 0261-4189.

Dobrowsky RT, Carter BD. Coupling of the p75 neurotrophin receptor to sphingolipid signaling. Ann. N. Y. Acad. Sci. 1998 Jun 6/19/1998; 845: 32-45. PMID: 9668341, ISSN: 0077-8923.

Yoon SO, Casaccia-Bonnefil P, Carter BD and Chao MV. Competitive signaling between TrkA and p75 NGF receptors determines cell survival. J Neurosci. 1998; 18: 3273-81.

Chao, M., Casaccia-Bonnefil, P., Carter, B., Chittka, A., Kong, H. and Yoon, S.O. Neurotrophin receptors: mediators of life and death. Brain Res. Brain Res. Rev. 1998; 26: 295-301.

Carter BD, Lewin GR. Neurotrophins live or let die: does p75NTR decide?. Neuron. 1997 Feb; 18(2): 187-90. PMID: 9052790, PII: S0896-6273(00)80259-7, ISSN: 0896-6273.

Casaccia-Bonnefil P, Carter BD, Dobrowsky RT, Chao MV. Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature. 1996 Oct 10/24/1996; 383(6602): 716-9. PMID: 8878481, DOI: 10.1038/383716a0, ISSN: 0028-0836.

Strohmaier C, Carter BD, Urfer R, Barde YA, Dechant G. A splice variant of the neurotrophin receptor trkB with increased specificity for brain-derived neurotrophic factor. EMBO J. 1996 Jul 7/1/1996; 15(13): 3332-7. PMID: 8670834, PMCID: PMC451896, ISSN: 0261-4189.

Carter BD, Kaltschmidt C, Kaltschmidt B, Offenhäuser N, Böhm-Matthaei R, Baeuerle PA, Barde YA. Selective activation of NF-kappa B by nerve growth factor through the neurotrophin receptor p75. Science. 1996 Apr 4/26/1996; 272(5261): 542-5. PMID: 8614802, ISSN: 0036-8075.

Carter BD, Dechant G, Frade JM, Kaltschmidt C, Barde YA. Neurotrophins and their p75 receptor. Cold Spring Harb. Symp. Quant. Biol. 1996; 61: 407-15. PMID: 9246469, ISSN: 0091-7451.

Carter BD, Zirrgiebel U, Barde YA. Differential regulation of p21ras activation in neurons by nerve growth factor and brain-derived neurotrophic factor. J. Biol. Chem. 1995 Sep 9/15/1995; 270(37): 21751-7. PMID: 7665594, ISSN: 0021-9258.

Biffo S, Offenhäuser N, Carter BD, Barde YA. Selective binding and internalisation by truncated receptors restrict the availability of BDNF during development. Development. 1995 Aug; 121(8): 2461-70. PMID: 7671810, ISSN: 0950-1991.

Carter BD, Medzihradsky F. Go mediates the coupling of the mu opioid receptor to adenylyl cyclase in cloned neural cells and brain. Proc. Natl. Acad. Sci. U.S.A. 1993 May 5/1/1993; 90(9): 4062-6. PMID: 8097884, PMCID: PMC46446, ISSN: 0027-8424.

Carter BD, Medzihradsky F. Receptor mechanisms of opioid tolerance in SH-SY5Y human neural cells. Mol. Pharmacol. 1993 Mar; 43(3): 465-73. PMID: 8383804, ISSN: 0026-895X.

Carter BD, Medzihradsky F. Opioid signal transduction in intact and fragmented SH-SY5Y neural cells. J. Neurochem. 1992 May; 58(5): 1611-9. PMID: 1560222, ISSN: 0022-3042.

Medzihradsky, F. and B.D. Carter. Opioid receptor mechanisms. Chapt. 10 of Biochemistry and Physiology of Substance Abuse (Watson, R.R. ed.) CRC Press Inc., Boca Raton, Fl. 1991.

Clark MJ, Carter BD, Medzihradsky F. Selectivity of ligand binding to opioid receptors in brain membranes from the rat, monkey and guinea pig. Eur. J. Pharmacol. 1988 Apr 4/13/1988; 148(3): 343-51. PMID: 2898375, ISSN: 0014-2999.

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