Holly Ingraham, PhD

Title(s)Professor, Cellular Molecular Pharmacology
SchoolSchool of Medicine
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    Collapse Biography 
    Collapse Awards and Honors
    2002Brook Byers Award
    2012Elected AAAS Fellow
    2006Herzstein Distinguished Investigator in Molecular Physiology
    2017Chancellor’s Award for theMartin Luther King, Jr. (MLK) Leadership
    2018Joseph Larner Memorial Lectureship Award in Pharmacology
    2019Keynote Speaker – Society for Behavioral Neuroendocrinology
    201942nd Annual Steenbook Lectureship Award in Biochemistry
    2019Elected American Academy of Arts and Science

    Collapse Overview 

    Collapse Research 
    Collapse Research Activities and Funding
    UCSF Nutrition Obesity Research Center
    NIH/NIDDK P30DK098722Aug 1, 2015 - Jul 31, 2020
    Role: Co-Investigator
    Mapping Hypothalamic Neurocircuits Controlling Physical Activity
    NIH/NIDDK R01DK099722Apr 1, 2014 - Mar 31, 2019
    Role: Principal Investigator
    Molecular Mechanisms of Atrazine in Altering the Endocrine Gene Network
    NIH/NIEHS R21ES017136Jul 1, 2009 - Jun 30, 2011
    Role: Principal Investigator
    UCSF IRACDA Scholars Program
    NIH/NIGMS K12GM081266Aug 3, 2007 - Jul 31, 2022
    Role: Principal Investigator
    Structural Analyses of NR5 Orphan Nuclear Receptors
    NIH/NIDDK R01DK072246Jul 15, 2005 - May 31, 2012
    Role: Principal Investigator
    Modulating Nuclear Receptor Activity via Sumoylation
    NIH/NIDDK R01DK070024Sep 30, 2004 - Jul 31, 2013
    Role: Principal Investigator
    NIH/NIDDK P01DK058390Aug 15, 2000 - Jul 31, 2006
    Role: Co-Investigator
    NIH/NIDDK R13DK056229Jul 15, 1999 - Jun 30, 2000
    Role: Principal Investigator
    NIH/NICHD R01HD036233Apr 15, 1998 - Mar 31, 2004
    Role: Principal Investigator
    NIH/NICHD K02HD001178Jul 1, 1997 - Jun 30, 2002
    Role: Principal Investigator
    Developmental Programs of Neural Circuits in the Mouse Medial Hypothalamus
    NIH/NIDDK R01DK063592Aug 1, 1993 - Mar 31, 2014
    Role: Principal Investigator
    NIH/NICHD R01HD030725Aug 1, 1993 - Jul 31, 2002
    Role: Principal Investigator
    NIH/NIDDK R01DK046048Jul 1, 1993 - Jun 30, 1997
    Role: Principal Investigator

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    Collapse In The News
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    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.
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    1. Herber CB, Krause WC, Wang L, Bayrer JR, Li A, Schmitz M, Fields A, Ford B, Zhang Z, Reid MS, Nomura DK, Nissenson RA, Correa SM, Ingraham HA. Estrogen signaling in arcuate Kiss1 neurons suppresses a sex-dependent female circuit promoting dense strong bones. Nat Commun. 2019 01 11; 10(1):163. PMID: 30635563.
      View in: PubMed
    2. Bayrer JR, Wang H, Nattiv R, Suzawa M, Escusa HS, Fletterick RJ, Klein OD, Moore DD, Ingraham HA. LRH-1 mitigates intestinal inflammatory disease by maintaining epithelial homeostasis and cell survival. Nat Commun. 2018 10 10; 9(1):4055. PMID: 30305617.
      View in: PubMed
    3. Miranda DA, Krause WC, Cazenave-Gassiot A, Suzawa M, Escusa H, Foo JC, Shihadih DS, Stahl A, Fitch M, Nyangau E, Hellerstein M, Wenk MR, Silver DL, Ingraham HA. LRH-1 regulates hepatic lipid homeostasis and maintains arachidonoyl phospholipid pools critical for phospholipid diversity. JCI Insight. 2018 Mar 08; 3(5). PMID: 29515023.
      View in: PubMed
    4. Xing Y, Morohashi KI, Ingraham HA, Hammer GD. Timing of adrenal regression controlled by synergistic interaction between Sf1 SUMOylation and Dax1. Development. 2017 10 15; 144(20):3798-3807. PMID: 28893949.
      View in: PubMed
    5. Bellono NW, Bayrer JR, Leitch DB, Castro J, Zhang C, O'Donnell TA, Brierley SM, Ingraham HA, Julius D. Enterochromaffin Cells Are Gut Chemosensors that Couple to Sensory Neural Pathways. Cell. 2017 Jun 29; 170(1):185-198.e16. PMID: 28648659.
      View in: PubMed
    6. Krause WC, Ingraham HA. Origins and Functions of the Ventrolateral VMH: A Complex Neuronal Cluster Orchestrating Sex Differences in Metabolism and Behavior. Adv Exp Med Biol. 2017; 1043:199-213. PMID: 29224096.
      View in: PubMed
    7. Conde K, Fabelo C, Krause WC, Propst R, Goethel J, Fischer D, Hur J, Meza C, Ingraham HA, Wagner EJ. Testosterone Rapidly Augments Retrograde Endocannabinoid Signaling in Proopiomelanocortin Neurons to Suppress Glutamatergic Input from Steroidogenic Factor 1 Neurons via Upregulation of Diacylglycerol Lipase-a. Neuroendocrinology. 2017; 105(4):341-356. PMID: 27871072.
      View in: PubMed
    8. de Jesus Cortez F, Suzawa M, Irvy S, Bruning JM, Sablin E, Jacobson MP, Fletterick RJ, Ingraham HA, England PM. Disulfide-Trapping Identifies a New, Effective Chemical Probe for Activating the Nuclear Receptor Human LRH-1 (NR5A2). PLoS One. 2016; 11(7):e0159316. PMID: 27467220; PMCID: PMC4965143.
    9. Suzawa M, Miranda DA, Ramos KA, Ang KK, Faivre EJ, Wilson CG, Caboni L, Arkin MR, Kim YS, Fletterick RJ, Diaz A, Schneekloth JS, Ingraham HA. A gene-expression screen identifies a non-toxic sumoylation inhibitor that mimics SUMO-less human LRH-1 in liver. Elife. 2015 Dec 11; 4. PMID: 26653140.
      View in: PubMed
    10. Sablin EP, Blind RD, Uthayaruban R, Chiu HJ, Deacon AM, Das D, Ingraham HA, Fletterick RJ. Structure of Liver Receptor Homolog-1 (NR5A2) with PIP3 hormone bound in the ligand binding pocket. J Struct Biol. 2015 Dec; 192(3):342-348. PMID: 26416531.
      View in: PubMed
    11. Cheung CC, Krause WC, Edwards RH, Yang CF, Shah NM, Hnasko TS, Ingraham HA. Sex-dependent changes in metabolism and behavior, as well as reduced anxiety after eliminating ventromedial hypothalamus excitatory output. Mol Metab. 2015 Nov; 4(11):857-66. PMID: 26629409; PMCID: PMC4632173.
    12. Correa SM, Newstrom DW, Warne JP, Flandin P, Cheung CC, Lin-Moore AT, Pierce AA, Xu AW, Rubenstein JL, Ingraham HA. An estrogen-responsive module in the ventromedial hypothalamus selectively drives sex-specific activity in females. Cell Rep. 2015 Jan 06; 10(1):62-74. PMID: 25543145; PMCID: PMC4324838.
    13. Blind RD, Sablin EP, Kuchenbecker KM, Chiu HJ, Deacon AM, Das D, Fletterick RJ, Ingraham HA. The signaling phospholipid PIP3 creates a new interaction surface on the nuclear receptor SF-1. Proc Natl Acad Sci U S A. 2014 Oct 21; 111(42):15054-9. PMID: 25288771; PMCID: PMC4210282.
    14. Cheung CC, Kurrasch DM, Liang JK, Ingraham HA. Genetic labeling of steroidogenic factor-1 (SF-1) neurons in mice reveals ventromedial nucleus of the hypothalamus (VMH) circuitry beginning at neurogenesis and development of a separate non-SF-1 neuronal cluster in the ventrolateral VMH. J Comp Neurol. 2013 Apr 15; 521(6):1268-88. PMID: 22987798; PMCID: PMC4304766.
    15. Blind RD, Suzawa M, Ingraham HA. Direct modification and activation of a nuclear receptor-PIP2 complex by the inositol lipid kinase IPMK. Sci Signal. 2012 Jun 19; 5(229):ra44. PMID: 22715467; PMCID: PMC3395721.
    16. Lee FY, Faivre EJ, Suzawa M, Lontok E, Ebert D, Cai F, Belsham DD, Ingraham HA. Eliminating SF-1 (NR5A1) sumoylation in vivo results in ectopic hedgehog signaling and disruption of endocrine development. Dev Cell. 2011 Aug 16; 21(2):315-27. PMID: 21820362; PMCID: PMC3157481.
    17. Ingraham HA. Metabolism: A lipid for fat disorders. Nature. 2011 Jun 22; 474(7352):455-6. PMID: 21697939.
      View in: PubMed
    18. Hayes TB, Anderson LL, Beasley VR, de Solla SR, Iguchi T, Ingraham H, Kestemont P, Kniewald J, Kniewald Z, Langlois VS, Luque EH, McCoy KA, Muñoz-de-Toro M, Oka T, Oliveira CA, Orton F, Ruby S, Suzawa M, Tavera-Mendoza LE, Trudeau VL, Victor-Costa AB, Willingham E. Demasculinization and feminization of male gonads by atrazine: consistent effects across vertebrate classes. J Steroid Biochem Mol Biol. 2011 Oct; 127(1-2):64-73. PMID: 21419222; PMCID: PMC4303243.
    19. Whitby RJ, Stec J, Blind RD, Dixon S, Leesnitzer LM, Orband-Miller LA, Williams SP, Willson TM, Xu R, Zuercher WJ, Cai F, Ingraham HA. Small molecule agonists of the orphan nuclear receptors steroidogenic factor-1 (SF-1, NR5A1) and liver receptor homologue-1 (LRH-1, NR5A2). J Med Chem. 2011 Apr 14; 54(7):2266-81. PMID: 21391689; PMCID: PMC4151520.
    20. Blackshaw S, Scholpp S, Placzek M, Ingraham H, Simerly R, Shimogori T. Molecular pathways controlling development of thalamus and hypothalamus: from neural specification to circuit formation. J Neurosci. 2010 Nov 10; 30(45):14925-30. PMID: 21068293.
      View in: PubMed
    21. Mullaney BC, Blind RD, Lemieux GA, Perez CL, Elle IC, Faergeman NJ, Van Gilst MR, Ingraham HA, Ashrafi K. Regulation of C. elegans fat uptake and storage by acyl-CoA synthase-3 is dependent on NR5A family nuclear hormone receptor nhr-25. Cell Metab. 2010 Oct 06; 12(4):398-410. PMID: 20889131.
      View in: PubMed
    22. Lin BC, Suzawa M, Blind RD, Tobias SC, Bulun SE, Scanlan TS, Ingraham HA. Stimulating the GPR30 estrogen receptor with a novel tamoxifen analogue activates SF-1 and promotes endometrial cell proliferation. Cancer Res. 2009 Jul 01; 69(13):5415-23. PMID: 19549922; PMCID: PMC2756996.
    23. Kurrasch DM, Nevin LM, Wong JS, Baier H, Ingraham HA. Neuroendocrine transcriptional programs adapt dynamically to the supply and demand for neuropeptides as revealed in NSF mutant zebrafish. Neural Dev. 2009 Jun 23; 4:22. PMID: 19549326; PMCID: PMC2715394.
    24. Sablin EP, Woods A, Krylova IN, Hwang P, Ingraham HA, Fletterick RJ. The structure of corepressor Dax-1 bound to its target nuclear receptor LRH-1. Proc Natl Acad Sci U S A. 2008 Nov 25; 105(47):18390-5. PMID: 19015525; PMCID: PMC2587556.
    25. Sablin EP, Blind RD, Krylova IN, Ingraham JG, Cai F, Williams JD, Fletterick RJ, Ingraham HA. Structure of SF-1 bound by different phospholipids: evidence for regulatory ligands. Mol Endocrinol. 2009 Jan; 23(1):25-34. PMID: 18988706; PMCID: PMC2646595.
    26. Campbell LA, Faivre EJ, Show MD, Ingraham JG, Flinders J, Gross JD, Ingraham HA. Decreased recognition of SUMO-sensitive target genes following modification of SF-1 (NR5A1). Mol Cell Biol. 2008 Dec; 28(24):7476-86. PMID: 18838537; PMCID: PMC2593425.
    27. Suzawa M, Ingraham HA. The herbicide atrazine activates endocrine gene networks via non-steroidal NR5A nuclear receptors in fish and mammalian cells. PLoS One. 2008 May 07; 3(5):e2117. PMID: 18461179; PMCID: PMC2362696.
    28. Kurrasch DM, Cheung CC, Lee FY, Tran PV, Hata K, Ingraham HA. The neonatal ventromedial hypothalamus transcriptome reveals novel markers with spatially distinct patterning. J Neurosci. 2007 Dec 12; 27(50):13624-34. PMID: 18077674.
      View in: PubMed
    29. Benoit G, Cooney A, Giguere V, Ingraham H, Lazar M, Muscat G, Perlmann T, Renaud JP, Schwabe J, Sladek F, Tsai MJ, Laudet V. International Union of Pharmacology. LXVI. Orphan nuclear receptors. Pharmacol Rev. 2006 Dec; 58(4):798-836. PMID: 17132856.
      View in: PubMed
    30. Tran PV, Akana SF, Malkovska I, Dallman MF, Parada LF, Ingraham HA. Diminished hypothalamic bdnf expression and impaired VMH function are associated with reduced SF-1 gene dosage. J Comp Neurol. 2006 Oct 10; 498(5):637-48. PMID: 16917842.
      View in: PubMed
    31. Ingraham HA, Redinbo MR. Orphan nuclear receptors adopted by crystallography. Curr Opin Struct Biol. 2005 Dec; 15(6):708-15. PMID: 16263271.
      View in: PubMed
    32. Lee MB, Lebedeva LA, Suzawa M, Wadekar SA, Desclozeaux M, Ingraham HA. The DEAD-box protein DP103 (Ddx20 or Gemin-3) represses orphan nuclear receptor activity via SUMO modification. Mol Cell Biol. 2005 Mar; 25(5):1879-90. PMID: 15713642; PMCID: PMC549377.
    33. Krylova IN, Sablin EP, Moore J, Xu RX, Waitt GM, MacKay JA, Juzumiene D, Bynum JM, Madauss K, Montana V, Lebedeva L, Suzawa M, Williams JD, Williams SP, Guy RK, Thornton JW, Fletterick RJ, Willson TM, Ingraham HA. Structural analyses reveal phosphatidyl inositols as ligands for the NR5 orphan receptors SF-1 and LRH-1. Cell. 2005 Feb 11; 120(3):343-55. PMID: 15707893.
      View in: PubMed
    34. Bland ML, Fowkes RC, Ingraham HA. Differential requirement for steroidogenic factor-1 gene dosage in adrenal development versus endocrine function. Mol Endocrinol. 2004 Apr; 18(4):941-52. PMID: 14726490.
      View in: PubMed
    35. Jordan BK, Shen JH, Olaso R, Ingraham HA, Vilain E. Wnt4 overexpression disrupts normal testicular vasculature and inhibits testosterone synthesis by repressing steroidogenic factor 1/beta-catenin synergy. Proc Natl Acad Sci U S A. 2003 Sep 16; 100(19):10866-71. PMID: 12949260; PMCID: PMC196894.
    36. Fowkes RC, Desclozeaux M, Patel MV, Aylwin SJ, King P, Ingraham HA, Burrin JM. Steroidogenic factor-1 and the gonadotrope-specific element enhance basal and pituitary adenylate cyclase-activating polypeptide-stimulated transcription of the human glycoprotein hormone alpha-subunit gene in gonadotropes. Mol Endocrinol. 2003 Nov; 17(11):2177-88. PMID: 12920232.
      View in: PubMed
    37. Sablin EP, Krylova IN, Fletterick RJ, Ingraham HA. Structural basis for ligand-independent activation of the orphan nuclear receptor LRH-1. Mol Cell. 2003 Jun; 11(6):1575-85. PMID: 12820970.
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    38. Bland ML, Desclozeaux M, Ingraham HA. Tissue growth and remodeling of the embryonic and adult adrenal gland. Ann N Y Acad Sci. 2003 May; 995:59-72. PMID: 12814939.
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    39. Tran PV, Lee MB, Marín O, Xu B, Jones KR, Reichardt LF, Rubenstein JR, Ingraham HA. Requirement of the orphan nuclear receptor SF-1 in terminal differentiation of ventromedial hypothalamic neurons. Mol Cell Neurosci. 2003 Apr; 22(4):441-53. PMID: 12727442; PMCID: PMC2710097.
    40. Huber BR, Desclozeaux M, West BL, Cunha-Lima ST, Nguyen HT, Baxter JD, Ingraham HA, Fletterick RJ. Thyroid hormone receptor-beta mutations conferring hormone resistance and reduced corepressor release exhibit decreased stability in the N-terminal ligand-binding domain. Mol Endocrinol. 2003 Jan; 17(1):107-16. PMID: 12511610.
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    41. Desclozeaux M, Krylova IN, Horn F, Fletterick RJ, Ingraham HA. Phosphorylation and intramolecular stabilization of the ligand binding domain in the nuclear receptor steroidogenic factor 1. Mol Cell Biol. 2002 Oct; 22(20):7193-203. PMID: 12242296; PMCID: PMC139795.
    42. Shen JH, Ingraham HA. Regulation of the orphan nuclear receptor steroidogenic factor 1 by Sox proteins. Mol Endocrinol. 2002 Mar; 16(3):529-40. PMID: 11875113.
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    43. Roberts LM, Visser JA, Ingraham HA. Involvement of a matrix metalloproteinase in MIS-induced cell death during urogenital development. Development. 2002 Mar; 129(6):1487-96. PMID: 11880357.
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    44. Durlinger AL, Gruijters MJ, Kramer P, Karels B, Ingraham HA, Nachtigal MW, Uilenbroek JT, Grootegoed JA, Themmen AP. Anti-Müllerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology. 2002 Mar; 143(3):1076-84. PMID: 11861535.
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