Skip to main content

Advertisement

SpringerLink
Log in

Regulation of Motor Function and Behavior by Atypical Chemokine Receptor 1

  • Original Research
  • Published:
Behavior Genetics Aims and scope Submit manuscript

Abstract

Atypical Chemokine Receptor 1 (ACKR1), previously known as Duffy Antigen Receptor for Chemokines, stands out among chemokine receptors for high selective expression on cerebellar Purkinje neurons. Although ACKR1 ligands activate Purkinje cells in vitro, evidence for ACKR1 regulation of brain function in vivo is lacking. Here we demonstrate that Ackr1 −/− mice have markedly impaired balance and ataxia on a rotating rod and increased tremor when injected with harmaline, which induces whole-body tremor by activating Purkinje cells. Ackr1 −/− mice also exhibited impaired exploratory behavior, increased anxiety-like behavior and frequent episodes of marked hypoactivity under low-stress conditions. Surprisingly, Ackr1 +/− had similar behavioral abnormalities, indicating pronounced haploinsufficiency. The behavioral phenotype of Ackr1 −/− mice was the opposite of mouse models of cerebellar degeneration, and the defects persisted when Ackr1 was deficient only on non-hematopoietic cells. Together, the results suggest that normal motor function and behavior may partly depend on negative regulation of Purkinje cell activity by Ackr1.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Adler MW, Geller EB, Chen X, Rogers TJ (2005) Viewing chemokines as a third major system of communication in the brain. AAPS J 7:E865–E870. doi:10.1208/aapsj070484

    Article  PubMed Central  Google Scholar 

  • Ambrosini E, Aloisi F (2004) Chemokines and glial cells: a complex network in the central nervous system. Neurochem Res 29:1017–1038. doi:10.1023/B:NERE.0000021246.96864.89

    Article  PubMed  Google Scholar 

  • Aspide R, Gironi Carnevale UA, Sergeant JA, Sadile AG (1998) Non-selective attention and nitric oxide in putative animal models of attention-deficit hyperactivity disorder. Behav Brain Res 95:123–133. doi:10.1016/S0166-4328(97)00217-9

    Article  PubMed  Google Scholar 

  • Baldacara L, Borgio JG, Lacerda AL, Jackowski AP (2008) Cerebellum and psychiatric disorders. Rev Bras Psiquiatr 30:281–289. doi:10.1590/S1516-44462008000300016

    Article  PubMed  Google Scholar 

  • Baltanás FC, Casafont I, Lafarga V, Weruaga E, Alonso JR, Berciano MT, Lafarga M (2011) Purkinje cell degeneration in pcd mice reveals large scale chromatin reorganization and gene silencing linked to defective DNA repair. J Biol Chem 286:28287–28302. doi:10.1074/jbc.M111.246041

    Article  PubMed Central  PubMed  Google Scholar 

  • Banisadr G, Gosselin RD, Mechighel P, Kitabgi P, Rostene W, Parsadaniantz SM (2005) Highly regionalized neuronal expression of monocyte chemoattractant protein-1 (MCP-1/CCL2) in rat brain: evidence for its colocalization with neurotransmitters and neuropeptides. J Comp Neurol 489:275–292. doi:10.1002/cne.20598

    Article  PubMed  Google Scholar 

  • Cancellieri C, Vacchini A, Locati M, Bonecchi R, Borroni EM (2013) Atypical chemokine receptors: from silence to sound. Biochem Soc Trans 41:231–236. doi:10.1042/BST20120246

    Article  PubMed  Google Scholar 

  • Chakera A, Seeber RM, John AE, Eidne KA, Greaves DR (2008) The duffy antigen/receptor for chemokines exists in an oligomeric form in living cells and functionally antagonizes CCR5 signaling through hetero-oligomerization. Mol Pharmacol 73:1362–1370. doi:10.1124/mol.107.040915

    Article  PubMed  Google Scholar 

  • Chaudhuri A, Polyakova J, Zbrzezna V, Williams K, Gulati S, Pogo AO (1993) Cloning of glycoprotein D cDNA, which encodes the major subunit of the Duffy blood group system and the receptor for the Plasmodium vivax malaria parasite. Proc Natl Acad Sci USA 90:10793–10797

    Article  PubMed Central  PubMed  Google Scholar 

  • Chaudhuri A, Zbrzezna V, Polyakova J, Pogo AO, Hesselgesser J, Horuk R (1994) Expression of the Duffy antigen in K562 cells. Evidence that it is the human erythrocyte chemokine receptor. J Biol Chem 269:7835–7838

    PubMed  Google Scholar 

  • Chaumont J, Guyon N, Valera AM, Dugue GP, Popa D, Marcaggi P, Gautheron V, Reibel-Foisset S, Dieudonne S, Stephan A, Barrot M, Cassel JC, Dupont JL, Doussau F, Poulain B, Selimi F, Lena C, Isope P (2013) Clusters of cerebellar Purkinje cells control their afferent climbing fiber discharge. Proc Natl Acad Sci USA. doi:10.1073/pnas.1302310110

    PubMed Central  PubMed  Google Scholar 

  • Crawley JN (2007) What’s wrong with my mouse?—behavioral phenotyping of transgenic and knockout mice. Wiley, Hoboken

    Google Scholar 

  • Cutbush M, Mollison PL (1950) The Duffy blood group system. Heredity (Edinb) 4:383–389. doi:10.1038/hdy.1950.31

    Article  Google Scholar 

  • Cutbush M, Mollison PL, Parkin DM (1950) A new human blood group. Nature 165:188–189. doi:10.1038/165188b0

    Article  Google Scholar 

  • Dawson TC, Lentsch AB, Wang Z, Cowhig JE, Rot A, Maeda N, Peiper SC (2000) Exaggerated response to endotoxin in mice lacking the Duffy antigen/receptor for chemokines (DARC). Blood 96:1681–1684

    PubMed  Google Scholar 

  • D’Hooge R, De Deyn PP (2001) Applications of the Morris water maze in the study of learning and memory. Brain Res Brain Res Rev 36:60–90. doi:10.1016/S0165-0173(01)00067-4

    Article  PubMed  Google Scholar 

  • Dickson PE, Rogers TD, Del Mar N, Martin LA, Heck D, Blaha CD, Goldowitz D, Mittleman G (2010) Behavioral flexibility in a mouse model of developmental cerebellar Purkinje cell loss. Neurobiol Learn Mem 94:220–228. doi:10.1016/j.nlm.2010.05.010

    Article  PubMed Central  PubMed  Google Scholar 

  • Florenzano F, Bentivoglio M (2000) Degranulation, density, and distribution of mast cells in the rat thalamus: a light and electron microscopic study in basal conditions and after intracerebroventricular administration of nerve growth factor. J Comp Neurol 424:651–669. doi:10.1002/1096-9861(20000904)424:4<651:AID-CNE7>3.0.CO;2-G

    Article  PubMed  Google Scholar 

  • Fowler SC, Birkestrand BR, Chen R, Moss SJ, Vorontsova E, Wang G, Zarcone TJ (2001) A force-plate actometer for quantitating rodent behaviors: illustrative data on locomotion, rotation, spatial patterning, stereotypies, and tremor. J Neurosci Methods 107:107–124.

  • Fowler SC, Zarcone TJ, Vorontsova E, Chen R (2002) Motor and associative deficits in D2 dopamine receptor knockout mice. Int J Dev Neurosci 20:309–321. doi:10.1016/S0736-5748(02)00009-6

    Article  PubMed  Google Scholar 

  • Fowler SC, Miller BR, Gaither TW, Johnson MA, Rebec GV (2009) Force-plate quantification of progressive behavioral deficits in the R6/2 mouse model of Huntington’s disease. Behav Brain Res 202:130–137. doi:10.1016/j.bbr.2009.03.022

    Article  PubMed Central  PubMed  Google Scholar 

  • Gao JL, Schneider EH, Dimitrov EL, Haun F, Pham TM, Mohammed AH, Usdin TB, Murphy PM (2011) Reduced fear memory and anxiety-like behavior in mice lacking formylpeptide receptor 1. Behav Genet 41:724–733. doi:10.1007/s10519-011-9467-0

    Article  PubMed Central  PubMed  Google Scholar 

  • Gardner L, Patterson AM, Ashton BA, Stone MA, Middleton J (2004) The human Duffy antigen binds selected inflammatory but not homeostatic chemokines. Biochem Biophys Res Commun 321:306–312. doi:10.1016/j.bbrc.2004.06.146

    Article  PubMed  Google Scholar 

  • Gillard SE, Lu M, Mastracci RM, Miller RJ (2002) Expression of functional chemokine receptors by rat cerebellar neurons. J Neuroimmunol 124:16–28. doi:10.1016/S0165-5728(02)00005-X

    Article  PubMed  Google Scholar 

  • Giovannelli A, Limatola C, Ragozzino D, Mileo AM, Ruggieri A, Ciotti MT, Mercanti D, Santoni A, Eusebi F (1998) CXC chemokines interleukin-8 (IL-8) and growth-related gene product alpha (GROalpha) modulate Purkinje neuron activity in mouse cerebellum. J Neuroimmunol 92:122–132. doi:10.1016/S0165-5728(98)00192-1

    Article  PubMed  Google Scholar 

  • Goodlett CR, Hamre KM, West JR (1992) Dissociation of spatial navigation and visual guidance performance in Purkinje cell degeneration (pcd) mutant mice. Behav Brain Res 47:129–141. doi:10.1016/S0166-4328(05)80119-6

    Article  PubMed  Google Scholar 

  • Hadley TJ, Lu ZH, Wasniowska K, Martin AW, Peiper SC, Hesselgesser J, Horuk R (1994) Postcapillary venule endothelial cells in kidney express a multispecific chemokine receptor that is structurally and functionally identical to the erythroid isoform, which is the Duffy blood group antigen. J Clin Invest 94:985–991. doi:10.1172/JCI117465

    Article  PubMed Central  PubMed  Google Scholar 

  • Handforth A (2012) Harmaline tremor: underlying mechanisms in a potential animal model of essential tremor. Tremor Other Hyperkinet Mov (N Y) 2: http://tremorjournal.org/article/view/92.

  • Hilber P, Lorivel T, Delarue C, Caston J (2004) Stress and anxious-related behaviors in Lurcher mutant mice. Brain Res 1003:108–112. doi:10.1016/j.brainres.2004.01.008

    Article  PubMed  Google Scholar 

  • Horuk R, Martin A, Hesselgesser J, Hadley T, Lu ZH, Wang ZX, Peiper SC (1996) The Duffy antigen receptor for chemokines: structural analysis and expression in the brain. J Leukoc Biol 59:29–38

    PubMed  Google Scholar 

  • Horuk R, Martin AW, Wang Z, Schweitzer L, Gerassimides A, Guo H, Lu Z, Hesselgesser J, Perez HD, Kim J, Parker J, Hadley TJ, Peiper SC (1997) Expression of chemokine receptors by subsets of neurons in the central nervous system. J Immunol 158:2882–2890

    PubMed  Google Scholar 

  • Huang DR, Wang J, Kivisakk P, Rollins BJ, Ransohoff RM (2001) Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J Exp Med 193:713–726

    Article  PubMed Central  PubMed  Google Scholar 

  • Ikeda Y, Kumagai H, Skach A, Sato M, Yanagisawa M (2013) Modulation of circadian glucocorticoid oscillation via Adrenal Opioid-CXCR7 signaling alters emotional behavior. Cell 155:1323–1336. doi:10.1016/j.cell.2013.10.052

    Article  PubMed Central  PubMed  Google Scholar 

  • Jaehne EJ, Baune BT (2014) Effects of chemokine receptor signalling on cognition-like, emotion-like and sociability behaviours of CCR6 and CCR7 knockout mice. Behav Brain Res 261:31–39

    Article  PubMed  Google Scholar 

  • Korelusova I, Cendelin J, Vozez F (2007) Motor and visuospatial abilities in a model of olivocerebellar and retinal degeneration—Lurcher mutant mice of C3H strain. Prague Med Rep 108:37–48

    PubMed  Google Scholar 

  • Lalonde R, Strazielle C (2003a) The effects of cerebellar damage on maze learning in animals. Cerebellum 2:300–309. doi:10.1080/14734220310017456

    Article  PubMed  Google Scholar 

  • Lalonde R, Strazielle C (2003b) Motor coordination, exploration, and spatial learning in a natural mouse mutation (nervous) with Purkinje cell degeneration. Behav Genet 33:59–66. doi:10.1023/A:1021003600900

    Article  PubMed  Google Scholar 

  • Lalonde R, Thifault S (1994) Absence of an association between motor coordination and spatial orientation in lurcher mutant mice. Behav Genet 24:497–501. doi:10.1007/BF01071563

    Article  PubMed  Google Scholar 

  • Lalonde R, Botez MI, Boivin D (1986a) Spontaneous alternation and habituation in a t-maze in nervous mutant mice. Behav Neurosci 100:350–352

    Article  PubMed  Google Scholar 

  • Lalonde R, Lamarre Y, Smith AM, Botez MI (1986b) Spontaneous alternation and habituation in lurcher mutant mice. Brain Res 362:161–164. doi:10.1016/0006-8993(86)91410-1

    Article  PubMed  Google Scholar 

  • Lalonde R, Manseau M, Botez MI (1987) Spontaneous alternation and habituation in Purkinje cell degeneration mutant mice. Brain Res 411:187–189. doi:10.1016/0006-8993(87)90699-8

    Article  PubMed  Google Scholar 

  • Lalonde R, Botez MI, Joyal CC, Caumartin M (1992) Motor abnormalities in lurcher mutant mice. Physiol Behav 51:523–525. doi:10.1016/0031-9384(92)90174-Z

    Article  PubMed  Google Scholar 

  • Lalonde R, Filali M, Bensoula AN, Lestienne F (1996) Sensorimotor learning in three cerebellar mutant mice. Neurobiol Learn Mem 65:113–120. doi:10.1006/nlme.1996.0013

    Article  PubMed  Google Scholar 

  • Lee JS, Wurfel MM, Matute-Bello G, Frevert CW, Rosengart MR, Ranganathan M, Wong VW, Holden T, Sutlief S, Richmond A, Peiper S, Martin TR (2006) The Duffy antigen modifies systemic and local tissue chemokine responses following lipopolysaccharide stimulation. J Immunol 177:8086–8094

    Article  PubMed Central  PubMed  Google Scholar 

  • Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong HW, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, Estin LK, Faber C, Facer BA, Fields R, Fischer SR, Fliss TP, Frensley C, Gates SN, Glattfelder KJ, Halverson KR, Hart MR, Hohmann JG, Howell MP, Jeung DP, Johnson RA, Karr PT, Kawal R, Kidney JM, Knapik RH, Kuan CL, Lake JH, Laramee AR, Larsen KD, Lau C, Lemon TA, Liang AJ, Liu Y, Luong LT, Michaels J, Morgan JJ, Morgan RJ, Mortrud MT, Mosqueda NF, Ng LL, Ng R, Orta GJ, Overly CC, Pak TH, Parry SE, Pathak SD, Pearson OC, Puchalski RB, Riley ZL, Rockett HR, Rowland SA, Royall JJ, Ruiz MJ, Sarno NR, Schaffnit K, Shapovalova NV, Sivisay T, Slaughterbeck CR, Smith SC, Smith KA, Smith BI, Sodt AJ, Stewart NN, Stumpf KR, Sunkin SM, Sutram M, Tam A, Teemer CD, Thaller C, Thompson CL, Varnam LR, Visel A, Whitlock RM, Wohnoutka PE, Wolkey CK, Wong VY et al (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168–176. doi:10.1038/nature05453

    Article  PubMed  Google Scholar 

  • Luo H, Chaudhuri A, Johnson KR, Neote K, Zbrzezna V, He Y, Pogo AO (1997) Cloning, characterization, and mapping of a murine promiscuous chemokine receptor gene: homolog of the human Duffy gene. Genome Res 7:932–941. doi:10.1101/gr.7.9.932

    PubMed Central  PubMed  Google Scholar 

  • Luo H, Chaudhuri A, Zbrzezna V, He Y, Pogo AO (2000) Deletion of the murine Duffy gene (Dfy) reveals that the Duffy receptor is functionally redundant. Mol Cell Biol 20:3097–3101. doi:10.1128/MCB.20.9.3097-3101.2000

    Article  PubMed Central  PubMed  Google Scholar 

  • Marshall JS (2004) Mast-cell responses to pathogens. Nat Rev Immunol 4:787–799. doi:10.1038/nri1460

    Article  PubMed  Google Scholar 

  • Mei J, Liu Y, Dai N, Favara M, Greene T, Jeyaseelan S, Poncz M, Lee JS, Worthen GS (2010) CXCL5 regulates chemokine scavenging and pulmonary host defense to bacterial infection. Immunity 33:106–117. doi:10.1016/j.immuni.2010.07.009

    Article  PubMed Central  PubMed  Google Scholar 

  • Miller LH, Mason SJ, Clyde DF, Mcginniss MH (1976) The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N Engl J Med 295:302–304. doi:10.1056/NEJM197608052950602

    Article  PubMed  Google Scholar 

  • Milner TE, Cadoret G, Lessard L, Smith AM (1995) EMG analysis of harmaline-induced tremor in normal and three strains of mutant mice with Purkinje cell degeneration and the role of the inferior olive. J Neurophysiol 73:2568–2577

    PubMed  Google Scholar 

  • Minten C, Alt C, Gentner M, Frei E, Deutsch U, Lyck R, Schaeren-Wiemers N, Rot A, Engelhardt B (2014) DARC shuttles inflammatory chemokines across the blood-brain barrier during autoimmune central nervous system inflammation. Brain 137:1454–1469

    Article  PubMed Central  PubMed  Google Scholar 

  • Nautiyal KM, Ribeiro AC, Pfaff DW, Silver R (2008) Brain mast cells link the immune system to anxiety-like behavior. Proc Natl Acad Sci USA 105:18053–18057. doi:10.1073/pnas.0809479105

    Article  PubMed Central  PubMed  Google Scholar 

  • Neote K, Mak JY, Kolakowski LF Jr, Schall TJ (1994) Functional and biochemical analysis of the cloned Duffy antigen: identity with the red blood cell chemokine receptor. Blood 84:44–52

    PubMed  Google Scholar 

  • Ogawa S, Chan J, Gustafsson JA, Korach KS, Pfaff DW (2003) Estrogen increases locomotor activity in mice through estrogen receptor alpha: specificity for the type of activity. Endocrinology 144:230–239

    Article  PubMed  Google Scholar 

  • Peiper SC, Wang ZX, Neote K, Martin AW, Showell HJ, Conklyn MJ, Ogborne K, Hadley TJ, Lu ZH, Hesselgesser J, Horuk R (1995) The Duffy antigen/receptor for chemokines (DARC) is expressed in endothelial cells of Duffy negative individuals who lack the erythrocyte receptor. J Exp Med 181:1311–1317

    Article  PubMed  Google Scholar 

  • Pollak Y, Ovadia H, Orion E, Weidenfeld J, Yirmiya R (2003) The EAE-associated behavioral syndrome: I. Temporal correlation with inflammatory mediators. J Neuroimmunol 137:94–99

    Article  PubMed  Google Scholar 

  • Pruenster M, Mudde L, Bombosi P, Dimitrova S, Zsak M, Middleton J, Richmond A, Graham GJ, Segerer S, Nibbs RJ, Rot A (2009) The Duffy antigen receptor for chemokines transports chemokines and supports their promigratory activity. Nat Immunol 10:101–108. doi:10.1038/ni.1675

    Article  PubMed Central  PubMed  Google Scholar 

  • Ragozzino D, Giovannelli A, Mileo AM, Limatola C, Santoni A, Eusebi F (1998) Modulation of the neurotransmitter release in rat cerebellar neurons by GRO beta. NeuroReport 9:3601–3606

    Article  PubMed  Google Scholar 

  • Réaux-Le Goazigo A, Van Steenwinckel J, Rostène W, Mélik Parsadaniantz S (2013) Current status of chemokines in the adult CNS. Prog Neurobiol 104:67–92

    Article  PubMed  Google Scholar 

  • Rios M, Chaudhuri A, Mallinson G, Sausais L, Gomensoro-Garcia AE, Hannon J, Rosenberger S, Poole J, Burgess G, Pogo O, Reid M (2000) New genotypes in Fy(a-b-) individuals: nonsense mutations (Trp to stop) in the coding sequence of either FY A or FY B. Br J Haematol 108:448–454. doi:10.1046/j.1365-2141.2000.01882.x

    Article  PubMed  Google Scholar 

  • Tournamille C, Colin Y, Cartron JP, Le Van Kim C (1995) Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy-negative individuals. Nat Genet 10:224–228. doi:10.1038/ng0695-224

    Article  PubMed  Google Scholar 

  • Trivedi R, Khan AR, Rana P, Haridas S, Hemanth Kumar BS, Manda K, Rathore RK, Tripathi RP, Khushu S (2012) Radiation-induced early changes in the brain and behavior: serial diffusion tensor imaging and behavioral evaluation after graded doses of radiation. J Neurosci Res 90:2009–2019. doi:10.1002/jnr.23073

    Article  PubMed  Google Scholar 

  • Van Gassen KL, Netzeband JG, De Graan PN, Gruol DL (2005) The chemokine CCL2 modulates Ca2+ dynamics and electrophysiological properties of cultured cerebellar Purkinje neurons. Eur J Neurosci 21:2949–2957. doi:10.1111/j.1460-9568.2005.04113.x

    Article  PubMed  Google Scholar 

  • Wohleb ES, Powell ND, Godbout JP, Sheridan JF (2013) Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior. J Neurosci 33:13820–13833. doi:10.1523/JNEUROSCI.1671-13.2013

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Division of Intramural Research, National Institute of Allergy and Infectious Diseases, NIH, USA. Financial support was also provided to E. H. S. through German Research Foundation Grant SCHN1192/1-1. S.C. Fowler received support from NIH Grant HD002528 and from the Life Span Institute at the University of Kansas. Experimental support by Alex Bredenkamp is gratefully acknowledged.

Conflict of interest

All authors declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This study was ethically approved by the Institutional Animal Care and Use Committee of the National Institute of Allergy and Infectious Diseases (NIAID/NIH, Bethesda, USA) and performed in accordance with the criteria defined by the rules of the committee.

Author information

Author notes

  1. Erich H. Schneider

    Present address: Institute of Pharmacology, Hannover Medical School, Hannover, Germany

  2. Michail S. Lionakis & Muthulekha Swamydas

    Present address: Fungal Pathogenesis Unit, Laboratory of Clinical Infectious Diseases, NIAID/NIH, Bethesda, MD, USA

Authors and Affiliations

  1. Laboratory of Molecular Immunology, National Institute of Allergy and Infectious Diseases (NIAID)/NIH, Bethesda, MD, USA

    Erich H. Schneider, Michail S. Lionakis, Muthulekha Swamydas, Gibran Holmes, Ji-Liang Gao & Philip M. Murphy

  2. Department of Pharmacology and Toxicology, University of Kansas, Lawrence, KS, USA

    Stephen C. Fowler

  3. In Vivo NMR Center, National Institute of Neurological Diseases and Stroke (NINDS)/NIH, Bethesda, MD, USA

    Vivian Diaz & Jeeva Munasinghe

  4. Institute of Pathology, Anatomy and Cell Biology, Jefferson Medical College, Philadelphia, PA, USA

    Stephen C. Peiper

  5. Bldg 10, Room 11N113, NIH, Bethesda, MD, 20892, USA

    Philip M. Murphy

Authors
  1. Erich H. Schneider
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen C. Fowler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michail S. Lionakis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Muthulekha Swamydas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gibran Holmes
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Vivian Diaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jeeva Munasinghe
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Stephen C. Peiper
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ji-Liang Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Philip M. Murphy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Philip M. Murphy.

Additional information

Edited by Tamara Phillips.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schneider, E.H., Fowler, S.C., Lionakis, M.S. et al. Regulation of Motor Function and Behavior by Atypical Chemokine Receptor 1. Behav Genet 44, 498–515 (2014). https://doi.org/10.1007/s10519-014-9665-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10519-014-9665-7

Keywords

Search

Navigation