title: Light-sensitive coupling of rhodopsin and melanopsin to G(i/o) and G(q) signal transduction in Caenorhabditis elegans.
abstract: Activation of G-protein-coupled receptors (GPCRs) initiates signal transduction cascades that affect many physiological responses. The worm Caenorhabditis elegans expresses >1000 of these receptors along with their cognate heterotrimeric G proteins. Here, we report properties of 9-cis-retinal regenerated bovine opsin [(b)isoRho] and human melanopsin [(h)Mo], two light-activated, heterologously expressed GPCRs in the nervous system of C. elegans with various genetically engineered alterations. Profound transient photoactivation of G(i/o) signaling by (b)isoRho led to a sudden and transient loss of worm motility dependent on cyclic adenosine monophosphate, whereas transient photoactivation of G(q) signaling by (h)Mo enhanced worm locomotion dependent on phospholipase Cβ. These transgenic C. elegans models provide a unique way to study the consequences of G(i/o) and G(q) signaling in vivo with temporal and spatial precision and, by analogy, their relationship to human neuromotor function.
authors.affiliation: Department of Pharmacology, Case Western Reserve University, Cleveland, OH 44106-4965, USA.
authors.forename: Pengxiu
authors.initials: P
authors.lastname: Cao
authors.forename: Wenyu
authors.initials: W
authors.lastname: Sun
authors.forename: Kristopher
authors.initials: K
authors.lastname: Kramp
authors.forename: Maohua
authors.initials: M
authors.lastname: Zheng
authors.forename: David
authors.initials: D
authors.lastname: Salom
authors.forename: Beata
authors.initials: B
authors.lastname: Jastrzebska
authors.forename: Hui
authors.initials: H
authors.lastname: Jin
authors.forename: Krzysztof
authors.initials: K
authors.lastname: Palczewski
authors.forename: Zhaoyang
authors.initials: Z
authors.lastname: Feng
mesh_terms: D015105:3',5'-Cyclic-AMP Phosphodiesterases / Q000378:metabolism; D000818:Animals; D030801:Animals, Genetically Modified; D001483:Base Sequence; D017173:Caenorhabditis elegans / Q000235:genetics / Q000378:metabolism* / Q000502:physiology / Q000528:radiation effects; D029742:Caenorhabditis elegans Proteins / Q000378:metabolism*; D002417:Cattle; D017931:DNA Primers / Q000235:genetics; D004224:Diterpenes; D019206:GTP-Binding Protein alpha Subunits, Gi-Go / Q000378:metabolism*; D043802:GTP-Binding Protein alpha Subunits, Gq-G11 / Q000378:metabolism*; D006801:Humans; D008027:Light; D008954:Models, Biological; D009043:Motor Activity / Q000528:radiation effects; D009474:Neurons / Q000378:metabolism; D011994:Recombinant Proteins / Q000235:genetics / Q000378:metabolism; D012172:Retinaldehyde / Q000378:metabolism; D012243:Rhodopsin / Q000235:genetics / Q000378:metabolism*; D017299:Rod Opsins / Q000235:genetics / Q000378:metabolism*; D015398:Signal Transduction; D000099210:Melanopsin
chemical_list: D015105:3',5'-Cyclic-AMP Phosphodiesterases; D029742:Caenorhabditis elegans Proteins; D017931:DNA Primers; D004224:Diterpenes; D019206:GTP-Binding Protein alpha Subunits, Gi-Go; D043802:GTP-Binding Protein alpha Subunits, Gq-G11; D011994:Recombinant Proteins; D012172:Retinaldehyde; D012243:Rhodopsin; D017299:Rod Opsins; D000099210:Melanopsin; C042882:isorhodopsin; C031390:9-cis-retinal
references.citation: J Neurosci Methods. 2011 Apr 30;197(2):315-23
references.pmid: 21376755
references.citation: Nat Methods. 2011 Feb;8(2):147-52
references.pmid: 21240279
references.citation: Nat Methods. 2006 Oct;3(10):785-92
references.pmid: 16990810
references.citation: Nat Methods. 2011 Jan;8(1):26-9
references.pmid: 21191368
references.citation: Infect Immun. 2001 Oct;69(10):6271-5
references.pmid: 11553570
references.citation: Science. 1998 Dec 11;282(5396):2028-33
references.pmid: 9851919
references.citation: Nat Methods. 2011 Feb;8(2):153-8
references.pmid: 21240278
references.citation: Trends Neurosci. 1996 Dec;19(12):547-54
references.pmid: 8961484
references.citation: Nature. 2007 Apr 5;446(7136):633-9
references.pmid: 17410168
references.citation: Cell. 2006 Nov 3;127(3):621-33
references.pmid: 17081982
references.citation: PLoS One. 2007 Mar 21;2(3):e299
references.pmid: 17375185
references.citation: J Biol Chem. 2001 Mar 30;276(13):10000-9
references.pmid: 11116153
references.citation: Nature. 2009 Apr 23;458(7241):1025-9
references.pmid: 19295515
references.citation: Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):13940-5
references.pmid: 14615590
references.citation: Proc Natl Acad Sci U S A. 2003 Dec 9;100(25):14748-53
references.pmid: 14657363
references.citation: Mol Cells. 2005 Feb 28;19(1):149-54
references.pmid: 15750353
references.citation: Neuron. 1996 May;16(5):999-1009
references.pmid: 8630258
references.citation: Genes Dev. 1997 Jun 15;11(12):1493-503
references.pmid: 9203577
references.citation: FASEB J. 2012 Feb;26(2):492-502
references.pmid: 22090314
references.citation: Nat Neurosci. 2010 Jun;13(6):715-22
references.pmid: 20436480
references.citation: Neuron. 2000 Jun;26(3):619-31
references.pmid: 10896158
references.citation: Genetics. 2006 May;173(1):111-30
references.pmid: 16624912
references.citation: Nat Neurosci. 2008 Aug;11(8):916-22
references.pmid: 18604203
references.citation: Proc Natl Acad Sci U S A. 2008 Dec 30;105(52):20982-7
references.pmid: 19074276
references.citation: Genetics. 1993 Oct;135(2):385-404
references.pmid: 8244003
references.citation: Genome Biol. 2005;6(3):213
references.pmid: 15774036
references.citation: Genes Dev. 1989 Dec;3(12A):1823-33
references.pmid: 2576011
references.citation: J Biol Chem. 2011 Jul 22;286(29):25848-58
references.pmid: 21628464
references.citation: Nucleic Acids Res. 1994 Jul 11;22(13):2437-46
references.pmid: 8041603
references.citation: J Biol Chem. 2010 Dec 31;285(53):41501-8
references.pmid: 21030591
references.citation: Nat Neurosci. 1999 Sep;2(9):791-7
references.pmid: 10461217
references.citation: Nature. 2005 Feb 17;433(7027):745-9
references.pmid: 15674243
references.citation: Genes Dev. 1999 Jul 15;13(14):1780-93
references.pmid: 10421631
references.citation: Nat Neurosci. 2005 Sep;8(9):1263-8
references.pmid: 16116447
references.citation: J Biol Chem. 2006 Apr 28;281(17):11917-22
references.pmid: 16495215
references.citation: Trends Biochem Sci. 2010 Jul;35(7):400-10
references.pmid: 20188572
references.citation: Science. 1995 Mar 17;267(5204):1648-51
references.pmid: 7886454
references.citation: WormBook. 2006 Feb 11;:1-11
references.pmid: 18050451
references.citation: Nature. 2010 Jan 7;463(7277):98-102
references.pmid: 20054397
references.citation: Biochemistry. 2008 Dec 16;47(50):13296-307
references.pmid: 19053287
references.citation: Proc Natl Acad Sci U S A. 1983 Apr;80(7):1887-91
references.pmid: 6572950
references.citation: WormBook. 2006 Oct 13;:1-25
references.pmid: 18050432
references.citation: J Neurochem. 2011 Feb;116(4):616-25
references.pmid: 21166803
references.citation: Science. 1996 Nov 1;274(5288):768-70
references.pmid: 8864113
references.citation: Science. 1995 Mar 17;267(5204):1652-5
references.pmid: 7886455
references.citation: Development. 2005 Jul;132(14):3197-207
references.pmid: 15983401
references.citation: Science. 2005 Jan 28;307(5709):600-4
references.pmid: 15681390
references.citation: Neurobiol Aging. 2009 Sep;30(9):1498-503
references.pmid: 18255194
references.citation: PLoS Biol. 2008 Aug 5;6(8):e198
references.pmid: 18687026
references.citation: Biochim Biophys Acta. 2012 Jan;1821(1):137-51
references.pmid: 21447403
references.citation: Cell Regul. 1991 Feb;2(2):135-54
references.pmid: 1907494
references.citation: Neuron. 1999 Oct;24(2):335-46
references.pmid: 10571228
references.citation: Annu Rev Biochem. 2006;75:743-67
references.pmid: 16756510
references.citation: Biochemistry. 1993 Jul 20;32(28):7229-36
references.pmid: 8343512
references.citation: Nat Struct Mol Biol. 2010 Jun;17(6):650-2
references.pmid: 20520658
references.citation: Annu Rev Cell Biol. 1986;2:391-419
references.pmid: 3103658
references.citation: Science. 2011 Jun 24;332(6037):1565-8
references.pmid: 21700876
references.citation: Curr Biol. 2003 Mar 18;13(6):516-21
references.pmid: 12646136
references.citation: Proc Natl Acad Sci U S A. 2008 Jul 1;105(26):8861-5
references.pmid: 18579788
references.citation: Nature. 2006 Mar 30;440(7084):684-7
references.pmid: 16572173