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Scientific Publications​

​All these papers have been published in peer-reviewed journals. 

The full text can be accessed by clicking on the hyperlinks, either the PMC number (free access) or the journal name (may be behind a paywall). Older papers do not have hyperlinks to the full text. 

My name appears in the list of authors as JCG Marvizón, which is my real name. 

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Neurotransmitter uptake

Uptake systems are protein in the synapses that eliminate neurotransmitters by transporting them back into the presynaptic terminal. This terminate their activation of the receptors. This is my first work in a lab, done as a student volunteer while I was finishing college at the Universidad Autónoma de Madrid (UAM). 

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  1. Marvizón, JCG, F. Mayor, Jr., MC Aragón, C. Giménez and F. Valdivieso. L-Aspartate transport into plasma membrane vesicles derived from rat brain synaptosomes. J. Neurochem. 37: 1401-1406, 1981.

  2. Mayor, F., Jr., JCG Marvizón, MC Aragón, C. Giménez, and F. Valdivieso. Glycine transport into plasma membrane vesicles derived from rat brain synaptosomes. Biochem. J. 198: 534-541, 1981. PMC1163299

  3. Aragón, MC, C. Giménez, F. Mayor, Jr., JCG Marvizón and F. Valdivieso. Tyrosine transport by membrane vesicles isolated from rat brain. Biochim. Biophys. Act 646: 465-470, 1981.

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Glycine receptors

The first two papers are my doctoral thesis at the UAM, done under the direction of Dr. Jesús Benavides. Glycine is the smallest amino acid and also an inhibitory neurotransmitter. I studied these receptors in the rat spinal cord by measuring the binding of strychnine, a poison that blocks these receptors. The third paper is a continuation of this work that I did when I was a postdoc at the National Institutes of Health (NIH) in Bethesda, MD, under the direction of Dr. Phil Skolnick. The last two papers were written in collaboration with the lab of Dr. Federico Mayor when I returned to the UAM as an Assistant Professor after my postdoc at the NIH. 

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  1. Marvizón, JCG, J. Vázquez, M. García Calvo, F. Mayor, Jr., A. Ruiz Gómez, F. Valdivieso, and J. Benavides. The glycine receptor: pharmacological studies and mathematical modeling of the allosteric interaction between the glycine- and the strychnine-binding sites. Mol. Pharmacol. 30: 590-597, 1986.

  2. Marvizón, JCG, M. García Calvo, J. Vázquez, F. Mayor, Jr., A. Ruiz Gómez, F. Valdivieso, and J. Benavides. Activation and inhibition of [3H]strychnine binding to the glycine receptor by Eccles' anions: modulatory effect of cations. Mol. Pharmacol. 30: 598-602, 1986.

  3. Marvizon, JCG and P. Skolnick. Anion regulation of [3H]strychnine binding to glycine-gated chloride channels is explained by the presence of two anion binding sites. Mol. Pharmacol. 34: 806-813, 1988.

  4. Ruiz-Gómez, A., C. Fernández-Shaw, E. Morato, JCG Marvizón, J. Vázquez, F. Valdivieso, F. Mayor, Jr. Sulfydryl groups modulate the allosteric interaction between glycine binding sites at the inhibitory glycine receptor. J. Neurochem. 56: 1690-1697, 1991.

  5. Ruiz-Gómez, A., M. García-Calvo, J. Vázquez, JCG Marvizón, F. Valdivieso and F. Mayor, Jr. Thermodynamics of agonist and antagonist interaction with the strychnine-sensitive glycine receptor. J. Neurochem. 52: 1775-1780, 1989.

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Oncogenes

Oncogenes are genes that can produce cancer. This is a paper that I did in collaboration with the lab of Dr. Eugenio Santos at the NIH. I helped them to measure intracellular calcium concentrations using fluorescent indicators.

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  1. Alonso, T., RO Morgan, JCG Marvizón, H. Zarbl, and E. Santos. Malignant transformation by ras and other oncogenes produces common alterations in phosphoinositide signaling pathways. Proc. Nat. Acad. Sci. USA 85: 4271-4275, 1988. PMC280409

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GABA receptors

Together with the glycine receptors, gamma-aminobutyric acid (GABA) receptors are the main inhibitory neurotransmitters. I studied them in the rat brain while I was a postdoc at NIH. In this paper I compared their properties with those of the glycine receptors.

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  1. Marvizon, JCG and P. Skolnick. Enhancement of t-[35S]Butylbicyclophosphorothionate and [3H]strychnine binding by monovalent anions reveals similarities between gamma-aminobutyric acid and glycine-gated chloride channels. J. Neurochem. 50: 1632-1639, 1988.

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NMDA receptors

​N-Methyl-D-aspartate (NMDA) receptors are a type of receptors for glutamate, the main excitatory neurotransmitter. They are important because they induce long term potentiation (LTP) of synapses, the mechanism that neurons use to store memory. NMDA receptors have a binding site for glycine, which is different from the glycine receptor. I started this work at the NIH with Dr. Skolnick and finished it while I was research faculty at the University of Southern California under the direction of Dr. Michel Baudry.

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  1. Marvizon, JCG and P. Skolnick. [3H]Glycine binding is modulated by Mg+2 and other ligands of the NMDA receptor-cation channel complex. Eur. J. Pharmacol. 151: 157-58, 1988.

  2. Marvizon, JCG, A. Lewin, and P. Skolnick. 1-Amino-cyclopropane carboxylic acid: a potent and selective ligand for the glycine modulatory site of the N-methyl-D-Aspartate receptor complex. J. Neurochem. 52: 992-994, 1989.

  3. Skolnick, P., JCG Marvizón, BW Jackson., JA Monn, KC Rice, and A. Lewin. Blockade of N-methyl-D-aspartate induced convulsions by 1-aminocyclopropane-carboxylates. Life Sci. 45: 1647-1655, 1989.

  4. Marvizón, JCG, and P. Skolnick. An endogenous modulator of N-methyl-D-aspartate receptor-coupled glycine receptors. Eur. J. Pharmacol. Mol. Pharmacol. 188: 23-32, 1990.

  5. Shahi, K., JCG Marvizón and M. Baudry. High concentrations of glycine induce long-lasting changes in synaptic efficacy in rat hippocampal slices. Neurosci. Lett. 149: 185-188, 1993.

  6. Marvizón, JCG, and M. Baudry. NMDA receptor activation by spermine requires glutamate but not glycine. Eur. J. Pharmacol. Mol. Pharmacol. 244: 103-104, 1993.

  7. Lewin, AH, P. Skolnick, JCG Marvizón, IA Paul, and JP Bowen. Requirements for high affinity binding of glycine analogs to the glycine site of the NMDA receptor complex. Eur. J. Pharmacol. Mol. Pharmacol. 247: 1-10, 1993.

  8. Marvizón, JCG, and M. Baudry. Receptor activation by two agonists: Analysis by non-linear regression and application to N-methyl-D-aspartate receptors. Anal. Biochem 213: 3-11, 1993.

  9. Marvizón, JCG, and M. Baudry. [3H]Dizocilpine association kinetics distinguish stimulatory and inhibitory polyamine sites of N-Methyl-D-Aspartate receptors. J. Neurochem. 63: 963-971, 1994.

  10. Marvizón, JCG, and M. Baudry. Allosteric interactions and modulator requirement for NMDA receptor function. Eur. J. Pharmacol. Mol. Pharmacol. 269: 165-175, 1994.

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Substance P release and neurokinin 1 receptor internalization in pain neurons

Substance P is a neuropeptide that binds to neurokinin 1 receptors in neurons in the dorsal horn of the spinal cord that send pain signals to the brain. By increasing the excitability of these neurons, substance P plays a crucial role in the induction of chronic pain. By using the internalization of neurokinin 1 receptors to measure substance P release, I investigating how opioids (endorphins), noradrenaline, serotonin, endocannabinoids and other neurotransmitters modulate its release. This work earned me a coveted R01 grant from the NIH in 2000, establishing me as faculty at UCLA and making me an independent investigator. Other R01 grants from the NIH and grants from the Veterans Administration (VA) continued to fund my research until 2020. 

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  1. Marvizón, JCG, V. Martínez, EF Grady, NW Bunnett, and EA Mayer. Neurokinin 1 receptor internalization in spinal cord slices induced by dorsal root stimulation is mediated by NMDA receptors. J. Neurosci. 17: 8129-8136, 1997. PMC6573757

  2. Marvizón, JCG, S. Eskandari, H. Ennes, and EA Mayer. Substance P induces brief, localized increases in [Ca2+]i in dorsal horn neurons. Neuro Report 9 (15): 3369-3374, 1998. 

  3. Marvizon, JCG, EF Grady, E. Stefani, NW Bunnett, and EA Mayer. Substance P release in the dorsal horn assessed by receptor internalization: NMDA receptors counteract a tonic inhibition by GABA-B receptors. Eur. J. Neurosci. 11: 417-426, 1999.

  4. Wang, X., and JCG Marvizón. Time-course of the internalization and recycling of neurokinin 1 receptors in rat dorsal horn neurons. Brain Res. 944: 239-247, 2002.

  5. Marvizón, JCG, X. Wang, Y. Matsuka, JK Neubert, and I. Spigelman. Relationship between capsaicin-evoked substance P release and NK1 receptor internalization in the rat dorsal horn. Neuroscience 118 (2): 535-545, 2003.

  6. Lao, LJ, Song, B. and JCG Marvizón. Neurokinin release produced by capsaicin acting on the central terminals and axons of primary afferents: relationship with NMDA and GABAB receptors. Neuroscience 121: 667-680, 2003.

  7. Marvizón, JCG, X. Wang, L. Lao, and B. Song. Effect of peptidases on the ability of exogenous and endogenous neurokinins to produce neurokinin 1 receptor internalization in the rat spinal cord. Br. J. Pharmacol. 140: 1389-1398, 2003. PMC1574162

  8. Lao L., and JCG Marvizón. GABA-A receptor facilitation of neurokinin release from primary afferent terminals in the rat spinal cord. Neuroscience 130: 1013-1027, 2005.

  9. Kondo, I., JCG Marvizón, B. Song, F. Salgado, S. Codeluppi, X.-Y. Hua and T. Yaksh. Inhibition by spinal m- and d-opioid agonists of afferent-evoked substance P release. J. Neurosci. 25: 3651-3660, 2005. PMC6725388

  10. Bradesi, S. , E. Kokkotou, S. Simeonidis, S. Patierno, HS Ennes, Y. Mittal, JA McRoberts, G. Ohning, JCG Marvizon, C. Sternini, C. Pothoulakis and EA Mayer. The role of neurokinin 1 receptors in the maintenance of visceral hyperalgesia induced by repeated stress in rats. Gastroenterology 130: 1729-1742, 2006.

  11. Adelson, DW, L. Lao, G. Zhang, W. Kim, and JCG Marvizón. Substance P release and neurokinin 1 receptor activation in the rat spinal cord increases with the firing frequency of C-fibers. Neuroscience 161: 538-553, 2009. PMC2692762

  12. Zhang G., W. Chen, L. Lao and JCG Marvizon. Cannabinoid CB1 receptor facilitation of substance P release in the rat spinal cord, measured as neurokinin 1 receptor internalization. Eur. J. Neurosci. 31: 225-237, 2010. PMC2857979

  13. Chen, W., G. Zhang and JCG Marvizon. Src family kinases mediate the inhibition of substance P release in the spinal cord by µ-opioid receptors and GABA-B receptors, but not α2 adrenergic receptors. Eur. J. Neurosci. 32: 963-973, 2010. PMC2942982

  14. Chen W, McRoberts JA, Marvizon JCG. µ-Opioid receptor inhibition of substance P release from primary afferents disappears during neuropathic pain but not inflammatory pain. Neuroscience 267: 67-82, 2014. PMC3998911

  15. Chen W., HS Ennes, JA McRoberts, JC Marvizon. Mechanisms of µ-opioid receptor inhibition of NMDA receptor-induced substance P release in the rat spinal cord. Neuropharmacology 128: 255-268, 2018. PMC5726399

  16. Chen, W, McRoberts JA, Ennes HS, Marvizon JC. cAMP signaling through protein kinase A and Epac2 induces substance P release in the rat spinal cord. Neuropharmacology 189: 108533 (2021) PMC8577816

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Endorphin release and mu-opioid receptor internalization

Endorphins are a family of 36 neuropeptides that activate the four opioid receptors: mu, delta, kappa and orphanin/nociceptin. The mu-opioid receptor mediates the analgesia and the euphoria produced by morphine and other opioid drugs. As I did with substance P, I used the internalization of mu-opioid receptors to measure endorphin release in the spinal cord. We investigated how is modulated by neurotransmitters and how it changes in chronic pain. 

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  1. Marvizón, JCG, EF Grady, J. Wazsak-McGee, and E. Mayer. Internalization of m-opioid receptors in rat spinal cord slices. Neuro Report 10 (11): 2329-2334, 1999.

  2. Song, B., and JCG Marvizon. Peptidases prevent m-opioid receptor internalization in dorsal horn neurons by endogenously released opioids. J. Neurosci. 23: 1847-1858, 2003. PMC2464295

  3. Song, B., and JCG Marvizón. Dorsal horn neurons firing at high frequency, but not primary afferents, release opioid peptides that produce m-opioid receptor internalization in the rat spinal cord. J. Neurosci. 23: 9171-9184, 2003. PMC2561240

  4. Song, B., and JCG Marvizón. NMDA receptors and large conductance calcium-sensitive potassium channels inhibit the release of opioid peptides that induce mu-opioid receptor internalization in the rat spinal cord. Neuroscience 136: 549-562, 2005. PMC1435407

  5. Chen, W., B. Song, L. Lao, OA Perez, W. Kim, and JCG Marvizon. Comparing analgesia and µ-opioid receptor internalization produced by intrathecal enkephalin: Requirement for peptidase inhibition. Neuropharmacology 53: 664-667, 2007. PMC2083640

  6. Lao, L., B. Song, W. Chen, and JCG Marvizon. Noxious mechanical stimulation evokes the segmental release of opioid peptides that induces µ-opioid receptor internalization. Brain Res. 1197: 85-93, 2008. PMC2292347

  7. Chen, W., B. Song, G. Zhang, and JCG Marvizon. Ability of veratridine and high potassium to produce μ-opioid receptor internalization by evoking the release of opioid peptides in the rat spinal cord. J. Neurosci. Methods 170: 285-293, 2008. PMC2410100

  8. Chen, W., B. Song and JCG Marvizón. Inhibition of opioid release in the rat spinal cord by α2C adrenergic receptors. Neuropharmacology 54: 944-953, 2008. PMC2365759

  9. Song, B., W. Chen and JCG Marvizon. Inhibition of opioid release in the rat spinal cord by serotonin 5-HT1A receptors. Brain Res. 1158: 57-62, 2007. PMC2377402

  10. Chen, W., and JCG Marvizón. Acute inflammation induces segmental, bilateral, supraspinally mediated opioid release in the rat spinal cord, as measured by µ-opioid receptor internalization. Neuroscience 161: 157-172, 2009. PMC2727879

  11. Marvizon, JCG, W. Chen, and N. Murphy. Enkephalins, dynorphins and β-endorphin in the rat dorsal horn: an immunofluorescence colocalization study. J.Comp. Neurol. 517: 51-68, 2009. PMC2924145

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NMDA receptors involved in pain

NMDA receptors are present in the presynaptic terminals in the spinal cord of the nerves that  transmit pain. By regulating the strength of that synapse, these NMDA receptors play a role in the induction of chronic pain.

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  1. McRoberts, JA, SV Coutinho, JCG Marvizon, EF Grady, M. Tognett, JN Sengupta, HS Ennes, VV Chaban, S. Amadesi, Ch. Creminon, T. Lanthorn, P. Geppetti, NW Bunnett, and EA Mayer. Role of peripheral N-methyl-D-aspartate (NMDA) receptors in visceral nociception in rats. Gastroenterology 120: 1737-1748, 2001.

  2. Marvizón, JCG, J. McRoberts, HS Ennes, B. Song, X. Wang, L. Jinton, B. Corneliussen, and EA Mayer. Two NMDA receptors in rat dorsal root ganglia with different subunit composition and localization. J.Comp. Neurol. 446: 325-341, 2002.

  3. McRoberts JA, Ennes H., Marvizon JCG, Fanselow M., Mayer EA, Vissel B. Selective knockdown of NMDA receptors in primary afferent neurons decreases pain during phase 2 of the formalin test. Neuroscience 172: 474-482, 2011. PMC3010451

  4. Chen W., G. Zhang and JCG Marvizon. NMDA receptors in primary afferents require phosphorylation by Src family kinases to induce substance P release in the rat spinal cord. Neuroscience 166: 924-934, 2010. PMC2837134

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Calcitonin gene-related peptide (CGRP) receptors

CGRP receptors, like the neurokinin 1 receptors for substance P, mediate the induction of chronic pain. They are formed by two proteins: the calcitonin receptor-like receptor and receptor activity modifying protein 1. In collaboration with the labs of Dr. Nigel Bunnett and Dr. Andrew Todd, we studied the distribution of these two proteins in the gut, pain fibers and the spinal cord.

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  1. Cottrell,GS, D. Roosterman, JC Marvizon, B. Song, E. Wick, S. Pikios, H. Wong, C. Berthelier, Y. Tang, C. Sternini, CW Tam, SD Brain, NW Bunnett, E. Grady. Localization of calcitonin receptor-like receptor and receptor activity modifying protein 1 in enteric neurons, dorsal root ganglia, and the spinal cord of the rat. J.Comp. Neurol. 490: 235-255, 2005.

  2. Marvizon, JCG, OA Perez, B. Song, W. Chen, NW Bunnett, EF Grady, and AJ Todd. Calcitonin Receptor-Like Receptor and Receptor Activity Modifying Protein 1 in the rat dorsal horn: localization in excitatory presynaptic terminals containing opioids and adrenergic α2C receptors. Neuroscience 148: 250-265, 2007. PMC2329818

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Brain-derived neurotrophic factor (BDNF)

BDNF is a neuropeptide required for the differentiation and survival of neurons. In collaboration with Dr. Marzia Malcangio, we determined that its release in the spinal cord requires bursts of action potentials in pain sensory fibers. In the second paper, we found that BDNF in the spinal cord initiates neuropathic pain by increasing the activity of the NMDA receptors present in the presynaptic of pain fibers in the spinal cord.

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  1. IJ Lever, EJ Bradbury, JR Cunningham, DW Adelson, MG Jones, SB McMahon, JCG Marvizon and M. Malcangio. Brain-derived neurotrophic factor is released in the dorsal horn by distinctive patterns of nociceptor stimulation. J. Neurosci. 21(12): 4469-4477, 2001. PMC6762751 

  2. Chen W., W. Walwyn, H. Ennes, JA McRoberts, JCG Marvizón. BDNF released by microglia during neuropathic pain potentiates NMDA receptors in primary afferent terminals. Eur. J. Neurosci. 39: 1439-1454, 2014. PMC4122572

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Thyrotropin-releasing hormone (TRH) and diabetes

This is a study I did in collaboration with Dr. Hong Yang at the Greater Los Angeles VA Healthcare System, where I also worked. 

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  1. Ao Y, M. Ko, A. Chen, JC Marvizon, DW Adelson, MK Song, LW Go, LL Liu, H. Yang. Potent hyperglycemic and hyperinsulinemic effects of thyrotropin-releasing hormone microinjected into the rostroventrolateral medulla and abnormal responses in type 2 diabetic rats. Neuroscience 169: 706-719, 2010. PMC3896326

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Neuropeptide Y receptors

Just like we did with neurokinin 1 receptors for substance P and mu-opioid receptors for endorphins, we used the internalization of its Y1 receptors to measure the release of neuropeptide Y in the spinal cord. This was a collaboration with Dr. Brad Taylor. 

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  1. Taylor BK, W. Fu, KE Kuphal, C.-O. Stiller, MK Winter, W. Chen, GF Corder, JH Urban, KE McCarson, and JC Marvizon. Inflammation enhances Y1 receptor signaling, neuropeptide Y-mediated inhibition of hyperalgesia, and substance P release from primary afferent neurons. Neuroscience 256:178-194, 2014. PMC4363128

  2. Marvizon, JC, W Chen, W Fu, and BK Taylor. Neuropeptide Y release in the rat spinal cord measured with Y1 receptor internalization is increased after nerve injury. Neuropharmacology 158: 107732, 2019. PMC6904115

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The latent sensitization model of chronic pain

Latent sensitization is a model of chronic pain in which pain sensitivity in increased in a mouse or a rat by inflammation or nerve injury. After several weeks, the pain sensitivity disappears, but it can be brought back by injecting opioid receptors antagonists like naloxone, which does not have any effect in normal animals. Stress also brings back the pain sensitivity. This reproduces what happens in patients with chronic pain: the pain comes and goes depending of the level of stress. In collaboration with Dr. Brad Taylor, we found that mu-opioid receptors are permanently activated during latent sensitization (which is called constitutive activity). In my lab, we also found that latent sensitization is maintained by neurokinin 1 receptor and a family of proteins called Src. 

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  1. Marvizón JC, Walwyn W, Minasayan A, Chen W, Taylor BK. Latent Sensitization: a model for stress-sensitive chronic pain. Current Protocols in Neuroscience 71: 9.50.1-9.50.14, 2015. PMC4532319

  2. Walwyn W., W. Chen, H. Kim, A. Minasayan, H. Ennes, JA McRoberts, JC Marvizón. Sustained suppression of hyperalgesia during latent sensitization by µ, δ and κ opioid receptors and α2A adrenergic receptors - role of constitutive activity. J. Neurosci. 36: 204-221, 2016. PMC4701961

  3. Chen W, Tache Y, Marvizon JCG. Corticotropin Releasing Factor in the brain and blocking spinal descending signals induces hyperalgesia in the latent sensitization model of chronic pain. Neuroscience 381: 149-158, 2018. PMC5962032

  4. Severino, A, W Chen, JK Hakimian, B Kieffer, C Gaveriaux-Ruff, W Walwyn, JC Marvizon. Mu-opioid receptors in nociceptive afferents produce a sustained suppression of hyperalgesia in chronic pain. Pain 159: 1607-1620, 2018. PMC6053329  full-text

  5. Chen, W, JC Marvizon. A Src family kinase maintains latent sensitization in rats, a model of inflammatory and neuropathic pain. Brain Res 1746: 146999 (2020). Biorxiv

  6. Chen, W, JC Marvizon. Neurokinin 1 receptor activation in the rat spinal cord maintains latent sensitization, a model of inflammatory and neuropathic chronic pain. Neuropharmacology 177: 108253 (2020). Biorxiv. PubMed.

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