Colorado PROFILES, The Colorado Clinical and Translational Sciences Institute (CCTSI)
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Susan Ingram

TitleProfessor
InstitutionUniversity of Colorado Denver - Anschutz Medical Campus
DepartmentSOM-AN Res General Operations
    Other Positions
    TitleAssoc Chair
    InstitutionUniversity of Colorado Denver - Anschutz Medical Campus
    DepartmentSOM-AN Res General Operations


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    Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Faculty can login to make corrections and additions.
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    1. Coutens B, Bouchet CA, Patti LC, McPherson KB, Boston BS, Jewett DC, Ingram SL. Corticosterone stimulates synthesis of 2-arachidonoylglycerol via putative membrane-bound glucocorticoid receptors and inhibits GABA release via CB1 cannabinoid receptors in the ventrolateral periaqueductal gray. Mol Pharmacol. 2025 Aug; 107(8):100058. PMID: 40729946.
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    2. Klawitter J, Clauw AD, Seifert JA, Klawitter J, Tompson B, Sempio C, Ingram SL, Christians U, Moreland LW. Endocannabinoid Tone and Oxylipins in Rheumatoid Arthritis and Osteoarthritis-A Novel Target for the Treatment of Pain and Inflammation? Int J Mol Sci. 2025 Jun 14; 26(12). PMID: 40565171.
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    3. Rios SM, Mootz JRK, Phillips TJ, Ingram SL. Absence of TAAR1 function increases methamphetamine-induced excitability of dorsal raphe serotonin neurons and drives binge-level methamphetamine intake. Neuropsychopharmacology. 2025 Jun; 50(7):1136-1144. PMID: 39934409.
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    4. Li M, Sorensen M, Johnson MA, Ingram SL, Andresen MC, Habecker BA. Hypertension increases sympathetic neuron activity by enhancing intraganglionic cholinergic collateral connections. J Physiol. 2025 Mar; 603(7):2005-2020. PMID: 39031543.
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    5. Bouchet CA, McPherson KB, Coutens B, Janowsky A, Ingram SL. Monoacylglycerol Lipase Protects the Presynaptic Cannabinoid 1 Receptor from Desensitization by Endocannabinoids after Persistent Inflammation. J Neurosci. 2023 07 26; 43(30):5458-5467. PMID: 37414560.
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    6. McPherson KB, Bouchet CA, Coutens B, Ingram SL. Persistent inflammation selectively activates opioid-sensitive phasic-firing neurons within the vlPAG. J Neurophysiol. 2023 05 01; 129(5):1237-1248. PMID: 37073984.
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    7. Clyburn C, Li MH, Ingram SL, Andresen MC, Habecker BA. Cholinergic collaterals arising from noradrenergic sympathetic neurons in mice. J Physiol. 2023 04; 601(7):1247-1264. PMID: 36797985.
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    8. Coutens B, Ingram SL. Key differences in regulation of opioid receptors localized to presynaptic terminals compared to somas: Relevance for novel therapeutics. Neuropharmacology. 2023 03 15; 226:109408. PMID: 36584882.
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    9. Sanchez GA, Jutkiewicz EM, Ingram S, Smrcka AV. Coincident Regulation of PLC? Signaling by Gq-Coupled and ?-Opioid Receptors Opposes Opioid-Mediated Antinociception. Mol Pharmacol. 2022 Dec; 102(6):269-279. PMID: 36116788.
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    10. McPherson KB, Ingram SL. Cellular and circuit diversity determines the impact of endogenous opioids in the descending pain modulatory pathway. Front Syst Neurosci. 2022; 16:963812. PMID: 36045708.
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    11. Clyburn C, Andresen MC, Ingram SL, Habecker BA. Untangling Peripheral Sympathetic Neurocircuits. Front Cardiovasc Med. 2022; 9:842656. PMID: 35224065.
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    12. Ingram SL. Toward understanding the opioid paradox: cellular mechanisms of opioid-induced hyperalgesia. Neuropsychopharmacology. 2022 01; 47(2):427-428. PMID: 34732843.
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    13. Bouchet CA, McPherson KB, Li MH, Traynor JR, Ingram SL. Mice Expressing Regulators of G protein Signaling-insensitive Gao Define Roles of ? Opioid Receptor Gao and Gai Subunit Coupling in Inhibition of Presynaptic GABA Release. Mol Pharmacol. 2021 09; 100(3):217-223. PMID: 34135098.
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    14. Kandasamy R, Hillhouse TM, Livingston KE, Kochan KE, Meurice C, Eans SO, Li MH, White AD, Roques BP, McLaughlin JP, Ingram SL, Burford NT, Alt A, Traynor JR. Positive allosteric modulation of the mu-opioid receptor produces analgesia with reduced side effects. Proc Natl Acad Sci U S A. 2021 04 20; 118(16). PMID: 33846240.
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    15. Ryan RM, Ingram SL, Scimemi A. Regulation of Glutamate, GABA and Dopamine Transporter Uptake, Surface Mobility and Expression. Front Cell Neurosci. 2021; 15:670346. PMID: 33927596.
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    16. Segarra VA, Primus C, Unguez GA, Edwards A, Etson C, Flores SC, Fry C, Guillory AN, Ingram SL, Lawson M, McGee R, Paxson S, Phelan L, Suggs K, Vega LR, Vuong E, Havran JC, Leon A, Burton MD, Lujan JL, Ramirez-Alvarado M. Scientific societies fostering inclusivity through speaker diversity in annual meeting programming: a call to action. Mol Biol Cell. 2020 11 01; 31(23):2495-2501. PMID: 33119460.
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    17. Womack VY, Thakore BK, Wood CV, Jewett DC, Jones RF, Ingram SL, Clark JA, Fry CL, Wecker L, McGee R. The ASPET Mentoring Network: Enhancing Diversity and Inclusion through Career Coaching Groups within a Scientific Society. CBE Life Sci Educ. 2020 09; 19(3):ar29. PMID: 32643998.
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    18. Segarra VA, Vega LR, Primus C, Etson C, Guillory AN, Edwards A, Flores SC, Fry C, Ingram SL, Lawson M, McGee R, Paxson S, Phelan L, Suggs K, Vuong E, Hammonds-Odie L, Leibowitz MJ, Zavala M, Lujan JL, Ramirez-Alvarado M. Scientific Societies Fostering Inclusive Scientific Environments through Travel Awards: Current Practices and Recommendations. CBE Life Sci Educ. 2020 06; 19(2):es3. PMID: 32453676.
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    19. Bagley EE, Ingram SL. Endogenous opioid peptides in the descending pain modulatory circuit. Neuropharmacology. 2020 08 15; 173:108131. PMID: 32422213.
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    20. Bouchet CA, Ingram SL. Cannabinoids in the descending pain modulatory circuit: Role in inflammation. Pharmacol Ther. 2020 05; 209:107495. PMID: 32004514.
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    21. Underhill SM, Hullihen PD, Chen J, Fenollar-Ferrer C, Rizzo MA, Ingram SL, Amara SG. Amphetamines signal through intracellular TAAR1 receptors coupled to Ga13 and GaS in discrete subcellular domains. Mol Psychiatry. 2021 04; 26(4):1208-1223. PMID: 31399635.
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    22. Bobeck EN, Schoo SM, Ingram SL, Morgan MM. Lack of Antinociceptive Cross-Tolerance With Co-Administration of Morphine and Fentanyl Into the Periaqueductal Gray of Male Sprague-Dawley Rats. J Pain. 2019 09; 20(9):1040-1047. PMID: 30853505.
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    23. McPherson KB, Leff ER, Li MH, Meurice C, Tai S, Traynor JR, Ingram SL. Regulators of G-Protein Signaling (RGS) Proteins Promote Receptor Coupling to G-Protein-Coupled Inwardly Rectifying Potassium (GIRK) Channels. J Neurosci. 2018 10 10; 38(41):8737-8744. PMID: 30150362.
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    24. Underhill SM, Ingram SL, Ahmari SE, Veenstra-VanderWeele J, Amara SG. Neuronal excitatory amino acid transporter EAAT3: Emerging functions in health and disease. Neurochem Int. 2019 02; 123:69-76. PMID: 29800605.
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    25. Chen Q, Roeder Z, Li MH, Zhang Y, Ingram SL, Heinricher MM. Optogenetic Evidence for a Direct Circuit Linking Nociceptive Transmission through the Parabrachial Complex with Pain-Modulating Neurons of the Rostral Ventromedial Medulla (RVM). eNeuro. 2017 May-Jun; 4(3). PMID: 28660248.
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    26. Li MH, Suchland KL, Ingram SL. Compensatory Activation of Cannabinoid CB2 Receptor Inhibition of GABA Release in the Rostral Ventromedial Medulla in Inflammatory Pain. J Neurosci. 2017 01 18; 37(3):626-636. PMID: 28100744.
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    27. Li MH, Underhill SM, Reed C, Phillips TJ, Amara SG, Ingram SL. Amphetamine and Methamphetamine Increase NMDAR-GluN2B Synaptic Currents in Midbrain Dopamine Neurons. Neuropsychopharmacology. 2017 Jun; 42(7):1539-1547. PMID: 27976681.
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    28. Tonsfeldt KJ, Suchland KL, Beeson KA, Lowe JD, Li MH, Ingram SL. Sex Differences in GABAA Signaling in the Periaqueductal Gray Induced by Persistent Inflammation. J Neurosci. 2016 Feb 03; 36(5):1669-81. PMID: 26843648.
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    29. Bobeck EN, Ingram SL, Hermes SM, Aicher SA, Morgan MM. Ligand-biased activation of extracellular signal-regulated kinase 1/2 leads to differences in opioid induced antinociception and tolerance. Behav Brain Res. 2016 Feb 01; 298(Pt B):17-24. PMID: 26497105.
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    30. Li MH, Suchland KL, Ingram SL. GABAergic transmission and enhanced modulation by opioids and endocannabinoids in adult rat rostral ventromedial medulla. J Physiol. 2015 Jan 01; 593(1):217-30. PMID: 25556797.
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    31. Underhill SM, Wheeler DS, Li M, Watts SD, Ingram SL, Amara SG. Amphetamine modulates excitatory neurotransmission through endocytosis of the glutamate transporter EAAT3 in dopamine neurons. Neuron. 2014 Jul 16; 83(2):404-416. PMID: 25033183.
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    32. Macey TA, Bobeck EN, Suchland KL, Morgan MM, Ingram SL. Change in functional selectivity of morphine with the development of antinociceptive tolerance. Br J Pharmacol. 2015 Jan; 172(2):549-61. PMID: 24666417.
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    33. Bobeck EN, Chen Q, Morgan MM, Ingram SL. Contribution of adenylyl cyclase modulation of pre- and postsynaptic GABA neurotransmission to morphine antinociception and tolerance. Neuropsychopharmacology. 2014 Aug; 39(9):2142-52. PMID: 24622471.
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    34. Ingram SL. Pain: novel analgesics from traditional Chinese medicines. Curr Biol. 2014 Feb 03; 24(3):R114-6. PMID: 24502784.
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    35. Mehalick ML, Ingram SL, Aicher SA, Morgan MM. Chronic inflammatory pain prevents tolerance to the antinociceptive effect of morphine microinjected into the ventrolateral periaqueductal gray of the rat. J Pain. 2013 Dec; 14(12):1601-10. PMID: 24161274.
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    36. Lamberts JT, Smith CE, Li MH, Ingram SL, Neubig RR, Traynor JR. Differential control of opioid antinociception to thermal stimuli in a knock-in mouse expressing regulator of G-protein signaling-insensitive Gao protein. J Neurosci. 2013 Mar 06; 33(10):4369-77. PMID: 23467353.
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    37. Williams JT, Ingram SL, Henderson G, Chavkin C, von Zastrow M, Schulz S, Koch T, Evans CJ, Christie MJ. Regulation of ?-opioid receptors: desensitization, phosphorylation, internalization, and tolerance. Pharmacol Rev. 2013 Jan; 65(1):223-54. PMID: 23321159.
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    38. Suckow SK, Deichsel EL, Ingram SL, Morgan MM, Aicher SA. Columnar distribution of catecholaminergic neurons in the ventrolateral periaqueductal gray and their relationship to efferent pathways. Synapse. 2013 Feb; 67(2):94-108. PMID: 23152302.
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    39. Bobeck EN, Haseman RA, Hong D, Ingram SL, Morgan MM. Differential development of antinociceptive tolerance to morphine and fentanyl is not linked to efficacy in the ventrolateral periaqueductal gray of the rat. J Pain. 2012 Aug; 13(8):799-807. PMID: 22766006.
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    40. Cyr MC, Ingram SL, Aicher SA, Morgan MM. Chronic psychostimulant exposure to adult, but not periadolescent rats reduces subsequent morphine antinociception. Pharmacol Biochem Behav. 2012 Jun; 101(4):538-43. PMID: 22405777.
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    41. Ingram SL. Association of mu-opioid and NMDA receptors in the periaqueductal gray: what does it mean for pain control? Neuropsychopharmacology. 2012 Jan; 37(2):315-6. PMID: 22157945.
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    42. Fyfe LW, Cleary DR, Macey TA, Morgan MM, Ingram SL. Tolerance to the antinociceptive effect of morphine in the absence of short-term presynaptic desensitization in rat periaqueductal gray neurons. J Pharmacol Exp Ther. 2010 Dec; 335(3):674-80. PMID: 20739455.
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    43. Macey TA, Ingram SL, Bobeck EN, Hegarty DM, Aicher SA, Arttamangkul S, Morgan MM. Opioid receptor internalization contributes to dermorphin-mediated antinociception. Neuroscience. 2010 Jun 30; 168(2):543-50. PMID: 20394808.
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    44. Ingram SL, Traynor JR. Role of protein kinase C in functional selectivity for desensitization at the mu-opioid receptor: from pharmacological curiosity to therapeutic potential. Br J Pharmacol. 2009 Sep; 158(1):154-6. PMID: 19719778.
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    45. Macey TA, Bobeck EN, Hegarty DM, Aicher SA, Ingram SL, Morgan MM. Extracellular signal-regulated kinase 1/2 activation counteracts morphine tolerance in the periaqueductal gray of the rat. J Pharmacol Exp Ther. 2009 Nov; 331(2):412-8. PMID: 19684256.
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    46. Morgan MM, Bobeck EN, Ingram SL. Glutamate modulation of antinociception, but not tolerance, produced by morphine microinjection into the periaqueductal gray of the rat. Brain Res. 2009 Oct 27; 1295:59-66. PMID: 19664608.
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    47. Morgan MM, Ashley MD, Ingram SL, Christie MJ. Behavioral consequences of delta-opioid receptor activation in the periaqueductal gray of morphine tolerant rats. Neural Plast. 2009; 2009:516328. PMID: 19266049.
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    48. Meyer PJ, Morgan MM, Kozell LB, Ingram SL. Contribution of dopamine receptors to periaqueductal gray-mediated antinociception. Psychopharmacology (Berl). 2009 Jun; 204(3):531-40. PMID: 19225762.
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    49. Fossum EN, Lisowski MJ, Macey TA, Ingram SL, Morgan MM. Microinjection of the vehicle dimethyl sulfoxide (DMSO) into the periaqueductal gray modulates morphine antinociception. Brain Res. 2008 Apr 14; 1204:53-8. PMID: 18342296.
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    50. Ingram SL, Macey TA, Fossum EN, Morgan MM. Tolerance to repeated morphine administration is associated with increased potency of opioid agonists. Neuropsychopharmacology. 2008 Sep; 33(10):2494-504. PMID: 18046309.
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    51. Meyer PJ, Fossum EN, Ingram SL, Morgan MM. Analgesic tolerance to microinjection of the micro-opioid agonist DAMGO into the ventrolateral periaqueductal gray. Neuropharmacology. 2007 Jun; 52(8):1580-5. PMID: 17445843.
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    52. Morgan MM, Fossum EN, Levine CS, Ingram SL. Antinociceptive tolerance revealed by cumulative intracranial microinjections of morphine into the periaqueductal gray in the rat. Pharmacol Biochem Behav. 2006 Sep; 85(1):214-9. PMID: 16979226.
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    53. Ingram SL, Fossum EN, Morgan MM. Behavioral and electrophysiological evidence for opioid tolerance in adolescent rats. Neuropsychopharmacology. 2007 Mar; 32(3):600-6. PMID: 16823389.
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    54. Morgan MM, Tierney BW, Ingram SL. Intermittent dosing prolongs tolerance to the antinociceptive effect of morphine microinjection into the periaqueductal gray. Brain Res. 2005 Oct 19; 1059(2):173-8. PMID: 16182261.
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    55. Connor M, Bagley EE, Mitchell VA, Ingram SL, Christie MJ, Humphrey PP, Vaughan CW. Cellular actions of somatostatin on rat periaqueductal grey neurons in vitro. Br J Pharmacol. 2004 Aug; 142(8):1273-80. PMID: 15265812.
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    56. Ingram SL, Prasad BM, Amara SG. Dopamine transporter-mediated conductances increase excitability of midbrain dopamine neurons. Nat Neurosci. 2002 Oct; 5(10):971-8. PMID: 12352983.
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    57. Carneiro AM, Ingram SL, Beaulieu JM, Sweeney A, Amara SG, Thomas SM, Caron MG, Torres GE. The multiple LIM domain-containing adaptor protein Hic-5 synaptically colocalizes and interacts with the dopamine transporter. J Neurosci. 2002 Aug 15; 22(16):7045-54. PMID: 12177201.
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    58. Christie MJ, Connor M, Vaughan CW, Ingram SL, Bagley EE. Cellular actions of opioids and other analgesics: implications for synergism in pain relief. Clin Exp Pharmacol Physiol. 2000 Jul; 27(7):520-3. PMID: 10874510.
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    59. Ingram SL, Amara SG. Arachidonic acid stimulates a novel cocaine-sensitive cation conductance associated with the human dopamine transporter. J Neurosci. 2000 Jan 15; 20(2):550-7. PMID: 10632584.
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    60. Ingram SL. Cellular and molecular mechanisms of opioid action. Prog Brain Res. 2000; 129:483-92. PMID: 11098712.
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    61. Ingram SL, Vaughan CW, Bagley EE, Connor M, Christie MJ. Enhanced opioid efficacy in opioid dependence is caused by an altered signal transduction pathway. J Neurosci. 1998 Dec 15; 18(24):10269-76. PMID: 9852564.
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    62. Nguyen VH, Ingram SL, Kassiou M, Christie MJ. Sigma-binding site ligands inhibit K+ currents in rat locus coeruleus neurons in vitro. Eur J Pharmacol. 1998 Nov 13; 361(1):157-63. PMID: 9851553.
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    63. Vaughan CW, Ingram SL, Connor MA, Christie MJ. How opioids inhibit GABA-mediated neurotransmission. Nature. 1997 Dec 11; 390(6660):611-4. PMID: 9403690.
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    64. Ingram S, Wilding TJ, McCleskey EW, Williams JT. Efficacy and kinetics of opioid action on acutely dissociated neurons. Mol Pharmacol. 1997 Jul; 52(1):136-43. PMID: 9224823.
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    65. Vaughan CW, Ingram SL, Christie MJ. Actions of the ORL1 receptor ligand nociceptin on membrane properties of rat periaqueductal gray neurons in vitro. J Neurosci. 1997 Feb 01; 17(3):996-1003. PMID: 8994054.
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    66. Ingram SL, Williams JT. Modulation of the hyperpolarization-activated current (Ih) by cyclic nucleotides in guinea-pig primary afferent neurons. J Physiol. 1996 Apr 01; 492 ( Pt 1):97-106. PMID: 8730586.
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    67. Baumann TK, Burchiel KJ, Ingram SL, Martenson ME. Responses of adult human dorsal root ganglion neurons in culture to capsaicin and low pH. Pain. 1996 Apr; 65(1):31-38. PMID: 8826487.
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    68. Ingram SL, Williams JT. Opioid inhibition of Ih via adenylyl cyclase. Neuron. 1994 Jul; 13(1):179-86. PMID: 7519024.
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