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The Role of G-Protein-Coupled Receptors in Adult Neurogenesis

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G Protein-Coupled Receptor Genetics

Part of the book series: Methods in Pharmacology and Toxicology ((MIPT))

Abstract

Adult neurogenesis is the process of creating new brain cells during adulthood. This involves several stages including proliferation, migration, differentiation, integration, and survival. G-protein-coupled receptors (GPCRs) regulate this process in both neurogenic regions of the brain: the subgranular and subventricular zones. The regulation of adult neurogenesis by GPCRs holds therapeutic promise for many neuropathologies. Several GPCRs activated by the neurotransmitters dopamine, glutamate, norepinephrine, and serotonin were shown to regulate adult neurogenesis. Melatonin, a neurohormone, and inflammatory molecules such as chemokines and prostaglandins modulate different stages of neurogenesis through GPCRs as well. The methods for studying the adult neurogenic stages depend upon labeling of dividing cells using the synthetic thymidine analog, nucleoside 5-bromo-2′-deoxyuridine (BrdU). BrdU incorporates into the DNA, is transferred to daughter cells, and is labeled using antibodies. The length of time after injection determines which stage of neurogenesis is being examined. Additional methods include culture of neonatal or adult neurospheres isolated from the subventricular zone, monolayer cultures of isolated neural stem cells, as well as transgenic manipulations via standard or viral-mediated techniques. In recent years, the use of Cre-inducible transgenic animals has developed and led to the creation of double- and triple-transgenic animals with specific activation of receptors in selected cell types. Future work in GPCR regulation of adult neurogenesis will likely include the use of opsin-receptor chimeras allowing precise spatial and temporal activation of GPCRs in neural stem/progenitor cells via optogenetics. This chapter summarizes the roles of various GPCRs involved in the regulation of adult neural stem cells and their progenitors and the current methods used to examine the actions of GPCRs in adult neurogenesis.

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References

  1. Sanai N, Tramontin AD, Quiñones-Hinojosa A et al (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427:740–744

    Article  CAS  PubMed  Google Scholar 

  2. Kam M, Curtis MA, McGlashan SR et al (2009) The cellular composition and morphological organization of the rostral migratory stream in the adult human brain. J Chem Neuroanat 37:196–205

    Article  CAS  PubMed  Google Scholar 

  3. Winner B, Cooper-Kuhn CM, Aigner R et al (2002) Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur J Neurosci 16:1681–1689

    Article  PubMed  Google Scholar 

  4. Petreanu L, Alvarez-Buylla A (2002) Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 22:6106–6113

    CAS  PubMed  Google Scholar 

  5. Dayer AG, Ford AA, Cleaver KM et al (2003) Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460:563–572

    Article  PubMed  Google Scholar 

  6. Kuipers SD, Tiron A, Soule J et al (2009) Selective survival and maturation of adult-born dentate granule cells expressing the immediate early gene Arc/Arg3.1. PLoS One 4:e4885

    Article  PubMed Central  PubMed  Google Scholar 

  7. Shors TJ, Anderson ML, Curlik DM et al (2012) Use it or lose it: how neurogenesis keeps the brain fit for learning. Behav Brain Res 227:450–458

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Ge S, Pradhan DA, Ming G-L et al (2007) GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci 30:1–8

    Article  PubMed  Google Scholar 

  9. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319–335

    Article  CAS  PubMed  Google Scholar 

  10. Taghipour M, Razmkon A (2012) Isolation and growth of neural stem cells derived from adult human hippocampus. J Inj Violence Res 4:S1

    Article  Google Scholar 

  11. Höglinger GU, Rizk P, Muriel MP et al (2004) Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat Neurosci 7:726–735

    Article  PubMed  Google Scholar 

  12. O’Keeffe G, Barker RA, Caldwell MA (2009) Dopaminergic modulation of neurogenesis in the subventricular zone of the adult brain. Cell Cycle 8:2888–2894

    Article  PubMed  Google Scholar 

  13. Diaz J, Ridray S, Mignon V et al (1997) Selective expression of dopamine D3 receptor mRNA in proliferative zones during embryonic development of the rat brain. J Neurosci 17:4282–4292

    CAS  PubMed  Google Scholar 

  14. Araki KY, Sims JR, Bhide PG (2007) Dopamine receptor mRNA and protein expression in the mouse corpus striatum and cerebral cortex during pre- and postnatal development. Brain Res 1156:31–45

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Coronas V, Bantubungi K, Fombonne J et al (2004) Dopamine D3 receptor stimulation promotes the proliferation of cells derived from the post-natal subventricular zone. J Neurochem 91:1292–1301

    Article  CAS  PubMed  Google Scholar 

  16. Lao CL, Lu CS, Chen JC (2013) Dopamine D(3) receptor activation promotes neural stem/progenitor cell proliferation through AKT and ERK1/2 pathways and expands type-B and-C cells in adult subventricular zone. Glia 61:475–489

    Article  PubMed  Google Scholar 

  17. Van Kampen JM, Hagg T, Robertson HA (2004) Induction of neurogenesis in the adult rat subventricular zone and neostriatum following dopamine D3 receptor stimulation. Eur J Neurosci 19:2377–2387

    Article  PubMed  Google Scholar 

  18. Kim Y, Wang W-Z, Comte I et al (2010) Dopamine stimulation of postnatal murine subventricular zone neurogenesis via the D3 receptor. J Neurochem 114:750–760

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Baker SA, Baker KA, Hagg T (2005) D3 dopamine receptors do not regulate neurogenesis in the subventricular zone of adult mice. Neurobiol Dis 18:523–527

    Article  CAS  PubMed  Google Scholar 

  20. Egeland M, Zhang X, Millan MJ et al (2012) Pharmacological or genetic blockade of the dopamine D3 receptor increases cell proliferation in the hippocampus of adult mice. J Neurochem 123:811–823

    Article  CAS  PubMed  Google Scholar 

  21. Luján R, Nusser Z, Roberts J et al (1996) Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci 8:1488–1500

    Article  PubMed  Google Scholar 

  22. Simonyi A, Ngomba RT, Storto M et al (2005) Expression of groups I and II metabotropic glutamate receptors in the rat brain during aging. Brain Res 1043:95–106

    Article  CAS  PubMed  Google Scholar 

  23. Castiglione M, Calafiore M, Costa L et al (2008) Group I metabotropic glutamate receptors control proliferation, survival and differentiation of cultured neural progenitor cells isolated from the subventricular zone of adult mice. Neuropharmacology 55:560–567

    Article  CAS  PubMed  Google Scholar 

  24. Zhao L, Jiao Q, Chen X et al (2012) mGluR5 is involved in proliferation of rat neural progenitor cells exposed to hypoxia with activation of mitogen-activated protein kinase signaling pathway. J Neurosci Res 90:447–460

    Article  CAS  PubMed  Google Scholar 

  25. Ciceroni C, Mosillo P, Mastrantoni E et al (2010) mGLU3 metabotropic glutamate receptors modulate the differentiation of subventricular zone-derived neural stem cells towards the astrocytic lineage. Glia 58:813–822

    CAS  PubMed  Google Scholar 

  26. Tian Y, Liu Y, Chen X et al (2010) AMN082 promotes the proliferation and differentiation of neural progenitor cells with influence on phosphorylation of MAPK signaling pathways. Neurochem Int 57:8–15

    Article  CAS  PubMed  Google Scholar 

  27. Wu D, Katz A, Lee C et al (1992) Activation of phospholipase C by alpha1-adrenergic receptors is mediated by the alpha subunits of Gq family. J Bio Chem 267:25798–25802

    CAS  Google Scholar 

  28. Gurdal H, Seasholtz T, Wang H et al (1997) Role of Gαq or Gαo proteins in α1-adrenoceptor subtype-mediated responses in Fischer 344 rat aorta. Mol Pharmacol 52:1064–1070

    CAS  PubMed  Google Scholar 

  29. Papay RS, Gaivin RJ, Jha A et al (2006) Localization of the mouse α1A-adrenergic receptor (AR) in the brain: α1AAR is expressed in neurons, GABAergic interneurons, and NG2 oligodendrocyte progenitors. J Comp Neurol 497:209–222

    Article  CAS  PubMed  Google Scholar 

  30. Gupta MK, Papay RS, Jurgens CWD et al (2009) α1-adrenergic receptors regulate neurogenesis and gliogenesis. Mol Pharmacol 76:314

    Article  CAS  PubMed  Google Scholar 

  31. Wang R, Macmillan LB, Fremeau RT et al (1996) Expression of alpha 2-adrenergic receptor subtypes in the mouse brain: evaluation of spatial and temporal information imparted by 3 kb of 5′ regulatory sequence for the alpha 2A AR-receptor gene in transgenic animals. Neuroscience 74:199–218

    Article  CAS  PubMed  Google Scholar 

  32. Karkoulias G, Mastrogianni O, Ilias I et al (2006) Alpha 2-adrenergic receptors decrease DNA replication and cell proliferation and induce neurite outgrowth in transfected rat pheochromocytoma cells. Ann N Y Acad Sci 1088:335–345

    Article  CAS  PubMed  Google Scholar 

  33. Taraviras S, Olli-Lähdesmäki T, Lymperopoulos A et al (2002) Subtype-specific neuronal differentiation of PC12 cells transfected with alpha2-adrenergic receptors. Eur J Cell Biol 81:363–374

    Article  CAS  PubMed  Google Scholar 

  34. Yanpallewar SU, Fernandes K, Marathe SV et al (2010) Alpha2-adrenoceptor blockade accelerates the neurogenic, neurotrophic, and behavioral effects of chronic antidepressant treatment. J Neurosci 30:1096–1109

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Rizk P, Salazar J, Raisman-Vozari R et al (2006) The alpha2-adrenoceptor antagonist dexefaroxan enhances hippocampal neurogenesis by increasing the survival and differentiation of new granule cells. Neuropsychopharmacology 31:1146–1157

    CAS  PubMed  Google Scholar 

  36. Masuda T, Nakagawa S, Boku S et al (2012) Noradrenaline increases neural precursor cells derived from adult rat dentate gyrus through β2 receptor. Prog Neuropsychopharmacol Biol Psychiatry 36:44–51

    Article  CAS  PubMed  Google Scholar 

  37. Jhaveri DJ, Mackay EW, Hamlin AS et al (2010) Norepinephrine directly activates adult hippocampal precursors via beta3-adrenergic receptors. J Neurosci 30:2795–2806

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Aghajanian GK, Sanders-Bush E (2002) Serotonin. In: Davis KL, Charney D, Coyle JT et al (eds) Neuropsychopharmacology: the fifth generation of progress. Lippincott Williams & Wilkins, Philadelphia

    Google Scholar 

  39. Klempin F, Babu H, De Pietri Tonelli D et al (2010) Oppositional effects of serotonin receptors 5-HT1a, 2, and 2c in the regulation of adult hippocampal neurogenesis. Front Mol Neurosci 3:1–11

    Google Scholar 

  40. Arnold SA, Hagg T (2012) Serotonin 1A receptor agonist increases species-and region-selective adult CNS proliferation, but not through CNTF. Neuropharmacology 63:1238–1247

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Banasr M, Hery M, Printemps R et al (2004) Serotonin-induced increases in adult cell proliferation and neurogenesis are mediated through different and common 5-HT receptor subtypes in the dentate gyrus and the subventricular zone. Neuropsychopharmacology 29:450–460

    Article  CAS  PubMed  Google Scholar 

  42. Huang G-J, Herbert J (2005) The role of 5-HT1A receptors in the proliferation and survival of progenitor cells in the dentate gyrus of the adult hippocampus and their regulation by corticoids. Neuroscience 135:803–813

    Article  CAS  PubMed  Google Scholar 

  43. Soumier A, Banasr M, Lortet S et al (2009) Mechanisms contributing to the phase-dependent regulation of neurogenesis by the novel antidepressant, agomelatine, in the adult rat hippocampus. Neuropsychopharmacology 34:2390–2403

    Article  CAS  PubMed  Google Scholar 

  44. Radley JJ, Jacobs BL (2002) 5-HT1A receptor antagonist administration decreases cell proliferation in the dentate gyrus. Brain Res 955:264–267

    Article  CAS  PubMed  Google Scholar 

  45. Santarelli L, Saxe M, Gross C et al (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301(80):805–809

    Article  CAS  PubMed  Google Scholar 

  46. Soumier A, Banasr M, Goff LK-L et al (2010) Region- and phase-dependent effects of 5-HT(1A) and 5-HT(2C) receptor activation on adult neurogenesis. Eur Neuropsychopharmacol 20:336–345

    Article  CAS  PubMed  Google Scholar 

  47. Xia L, Deloménie C, David I et al (2012) Ventral hippocampal molecular pathways and impaired neurogenesis associated with 5-HT 1A and 5-HT 1B receptors disruption in mice. Neurosci Lett 521:20–25

    Article  CAS  PubMed  Google Scholar 

  48. Gustafson EL, Durkin MM, Bard JA et al (1996) A receptor autoradiographic and in situ hybridization analysis of the distribution of the 5-ht7 receptor in rat brain. Br J Pharmacol 117:657–666

    Article  CAS  PubMed  Google Scholar 

  49. Martín-Cora FJ, Pazos A (2004) Autoradiographic distribution of 5-HT7 receptors in the human brain using [3H]mesulergine: comparison to other mammalian species. Br J Pharmacol 141:92–104

    Article  PubMed  Google Scholar 

  50. Bonaventure P, Nepomuceno D, Kwok A et al (2002) Reconsideration of 5-hydroxytryptamine (5-HT)(7) receptor distribution using [(3)H]5-carboxamidotryptamine and [(3)H]8-hydroxy-2-(di-n-propylamino)tetraline: analysis in brain of 5-HT(1A) knock-out and 5-HT(1A/1B) double-knock-out mice. J Pharmacol Exp Ther 302:240–248

    Article  CAS  PubMed  Google Scholar 

  51. Neumaier JF, Sexton TJ, Yracheta J et al (2001) Localization of 5-HT(7) receptors in rat brain by immunocytochemistry, in situ hybridization, and agonist stimulated cFos expression. J Chem Neuroanat 21:63–73

    Article  CAS  PubMed  Google Scholar 

  52. Xu H, Chen Z, He J et al (2006) Synergetic effects of quetiapine and venlafaxine in preventing the chronic restraint stress-induced decrease in cell proliferation and BDNF expression in rat hippocampus. Hippocampus 16:551–559

    Article  CAS  PubMed  Google Scholar 

  53. Musshoff U, Riewenherm D, Berger E et al (2002) Melatonin receptors in rat hippocampus: molecular and functional investigations. Hippocampus 12:165–173

    Article  CAS  PubMed  Google Scholar 

  54. Sotthibundhu A, Phansuwan-Pujito P, Govitrapong P (2010) Melatonin increases proliferation of cultured neural stem cells obtained from adult mouse subventricular zone. J Pineal Res 49:291–300

    Article  CAS  PubMed  Google Scholar 

  55. Ramirez-Rodriguez G, Ortíz-López L, Domínguez-Alonso A et al (2011) Chronic treatment with melatonin stimulates dendrite maturation and complexity in adult hippocampal neurogenesis of mice. J Pineal Res 50:29–37

    Article  CAS  PubMed  Google Scholar 

  56. Ramírez-Rodríguez G, Vega-Rivera NM, Benítez-King G et al (2012) Melatonin supplementation delays the decline of adult hippocampal neurogenesis during normal aging of mice. Neurosci Lett 530:53–58

    Article  PubMed  Google Scholar 

  57. Ramírez-Rodríguez G, Klempin F, Babu H et al (2009) Melatonin modulates cell survival of new neurons in the hippocampus of adult mice. Neuropsychopharmacology 34:2180–2191

    Article  PubMed  Google Scholar 

  58. Fava M, Targum SD, Nierenberg AA et al (2012) An exploratory study of combination buspirone and melatonin SR in major depressive disorder (MDD): a possible role for neurogenesis in drug discovery. J Psychiatr Res 46:1553–1563

    Article  PubMed  Google Scholar 

  59. Lu M, Grove EA, Miller RJ (2002) Abnormal development of the hippocampal dentate gyrus in mice lacking the CXCR4 chemokine receptor. Proc Natl Acad Sci U S A 99:7090–7095

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  60. Bagri A, Gurney T, He X et al (2002) The chemokine SDF1 regulates migration of dentate granule cells. Development 129:4249–4260

    CAS  PubMed  Google Scholar 

  61. Bhattacharyya BJ, Banisadr G, Jung H et al (2008) The chemokine stromal cell-derived factor-1 regulates GABAergic inputs to neural progenitors in the postnatal dentate gyrus. J Neurosci 28:6720–6730

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  62. Dziembowska M, Tham TN, Lau P et al (2005) A role for CXCR4 signaling in survival and migration of neural and oligodendrocyte precursors. Glia 50:258–269

    Article  CAS  PubMed  Google Scholar 

  63. Kolodziej A, Schulz S, Guyon A et al (2008) Tonic activation of CXC chemokine receptor 4 in immature granule cells supports neurogenesis in the adult dentate gyrus. J Neurosci 28:4488–4500

    Article  CAS  PubMed  Google Scholar 

  64. Chizzolini C, Brembilla NC (2009) Prostaglandin E2: igniting the fire. Immunol Cell Biol 87:510–511

    Article  PubMed  Google Scholar 

  65. Chen C, Magee JC, Bazan NG (2002) Cyclooxygenase-2 regulates prostaglandin E2 signaling in hippocampal long-term synaptic plasticity. J Neurophysiol 87:2851–2857

    CAS  PubMed  Google Scholar 

  66. Uchida K, Kumihashi K, Kurosawa S et al (2002) Stimulatory effects of prostaglandin E2 on neurogenesis in the dentate gyrus of the adult rat stimulatory effects of prostaglandin E2 on neurogenesis in the dentate gyrus of the adult rat. Zoolog Sci 19:1211–1216

    Article  CAS  PubMed  Google Scholar 

  67. Sasaki T, Kitagawa K, Sugiura S et al (2003) Implication of cyclooxygenase-2 on enhanced proliferation of neural progenitor cells in the adult mouse hippocampus after ischemia. J Neurosci Res 72:461–471

    Article  CAS  PubMed  Google Scholar 

  68. Kumihashi K, Uchida K, Miyazaki H et al (2001) Acetylsalicylic acid reduces ischemia-induced proliferation of dentate cells in gerbils. Neuroreport 12:915–917

    Article  CAS  PubMed  Google Scholar 

  69. Thomas née Williams SA, Segal MB (1996) Identification of a saturable uptake system for deoxyribonucleosides at the blood–brain and blood-cerebrospinal fluid barriers. Brain Res 741:230–239

    Article  PubMed  Google Scholar 

  70. Cameron H, McKay RD (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406–417

    Article  CAS  PubMed  Google Scholar 

  71. Parent JM, Yu TW, Leibowitz RT et al (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17:3727–3738

    CAS  PubMed  Google Scholar 

  72. Olariu A, Cleaver KM, Shore LE et al (2005) A natural form of learning can increase and decrease the survival of new neurons in the dentate gyrus. Hippocampus 15:750–762

    Article  PubMed  Google Scholar 

  73. Van Praag H, Kempermann G, Gage FH (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266–270

    Article  PubMed  Google Scholar 

  74. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027–2033

    CAS  PubMed  Google Scholar 

  75. Kempermann G, Gage FH (2002) Genetic influence on phenotypic differentiation in adult hippocampal neurogenesis. Brain Res Dev Brain Res 134:1–12

    Article  CAS  PubMed  Google Scholar 

  76. Mathews EA, Morgenstern NA, Piatti VC et al (2010) A distinctive layering pattern of mouse dentate granule cells is generated by developmental and adult neurogenesis. J Comp Neurol 518:4479–4490

    Article  PubMed Central  PubMed  Google Scholar 

  77. Hockfield S, Carlson S, Evans C et al (1993) Immunocytochemistry. In: Selected methods for antibody and nucleic acid probes. Cold Spring Harbor Laboratory Press, Plainview

    Google Scholar 

  78. Gage GJ, Kipke DR, Shain W (2012) Whole animal perfusion fixation for rodents (video). J Vis Exp 30:3564

    Google Scholar 

  79. Franklin G, Paxinos KBJ (2003) The mouse brain in stereotaxic coordinates, 2nd edn. Academic Press/Elsevier, Amsterdam

    Google Scholar 

  80. Slomianka L, West MJ (2005) Estimators of the precision of stereological estimates: an example based on the CA1 pyramidal cell layer of rats. Neuroscience 136:757–767

    Article  CAS  PubMed  Google Scholar 

  81. Peltier J, Schaffer DV (2010) Viral packaging and transduction of adult hippocampal neural progenitors. Methods Mol Biol 621:103–116

    Article  CAS  PubMed  Google Scholar 

  82. Kiyota T, Ingraham KL, Swan RJ et al (2012) AAV serotype 2/1-mediated gene delivery of anti-inflammatory interleukin-10 enhances neurogenesis and cognitive function in APP+PS1 mice. Gene Ther 19:724–733

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  83. Lee N, Batt MK, Cronier BA et al (2013) Ciliary neurotrophic factor receptor regulation of adult forebrain neurogenesis. J Neurosci 33:1241–1258

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  84. Pastrana E, Silva-Vargas V, Doetsch F (2011) Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell Stem Cell 8:486–498

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  85. Azari H, Rahman M, Sharififar S et al (2010) Isolation and expansion of the adult mouse neural stem cells using the neurosphere assay. J Vis Exp 45:2–5

    Google Scholar 

  86. Babu H, Claasen J-H, Kannan S et al (2011) A protocol for isolation and enriched monolayer cultivation of neural precursor cells from mouse dentate gyrus. Front Neurosci 5:10

    Article  Google Scholar 

  87. Airan RD, Thompson KR, Fenno LE et al (2009) Temporally precise in vivo control of intracellular signalling. Nature 458:1025–1029

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported in part by the National Science Foundation [Grant 0347259]; the National Institutes of Health National Center for Research Resources [Grant P20RR016471]; the National Heart, Lung, and Blood Institute [Grant R01HL098279]; and the American Heart Association [Grant-in-Aid, Great Rivers Affiliate]. No conflicts of interest are noted.

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Authors and Affiliations

  1. Department of Basic Sciences, School of Medicine and Health Sciences, University of North Dakota, Grand Forks, ND, USA

    Katie M. Collette

  2. Department of Pharmacology, Physiology and Therapeutics, School of Medicine and Health Sciences, University of North Dakota, Grand Forks, ND, USA

    Van A. Doze

  3. Department of Molecular Cardiology, Lerner Research Institute, The Cleveland Clinic Foundation, Cleveland, OH, USA

    Dianne M. Perez

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  1. Katie M. Collette
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  2. Van A. Doze
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  1. Oklahoma State University, Tulsa, Oklahoma, USA

    Craig W. Stevens

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Collette, K.M., Doze, V.A., Perez, D.M. (2014). The Role of G-Protein-Coupled Receptors in Adult Neurogenesis. In: Stevens, C. (eds) G Protein-Coupled Receptor Genetics. Methods in Pharmacology and Toxicology. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-62703-779-2_21

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