The RHO-1 RhoGTPase modulates fertility and multiple behaviors in adult C. elegans

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  McMullan, Rachel ^a   Nurrish, Stephen J ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EXOENZYME C3; RHO 1 PROTEIN; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; RHO 1 PROTEIN, C ELEGANS; RHO-1 PROTEIN, C ELEGANS; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ADULT ANIMAL; ANIMAL BEHAVIOR; ARTICLE; CAENORHABDITIS ELEGANS; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DEATH; DEFECATION DISORDER; DEVELOPMENTAL STAGE; FERTILITY; GENE EXPRESSION; GENE FUNCTION; GENE INDUCTION; LOCOMOTION; NONHUMAN; ORTHOLOGY; OVARY INSUFFICIENCY; SIGNAL TRANSDUCTION; AGE; AGING; ANIMAL; GASTROINTESTINAL SYMPTOM; GENE EXPRESSION REGULATION; GENETICS; HEAT SHOCK RESPONSE; METABOLISM; PHYSIOLOGY; TRANSGENIC ANIMAL;

ANIMALIA; CAENORHABDITIS ELEGANS;

AGE FACTORS; AGING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BEHAVIOR, ANIMAL; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; FERTILITY; GAGGING; GENE EXPRESSION REGULATION; HEAT-SHOCK RESPONSE; RHO GTP-BINDING PROTEINS; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION;

EID: 79952223153     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017265     Document Type: Article

References (75)

1. Jaffe AB, Hall A, (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21: 247-269.
2. Lundquist EA, (2006) Small GTPases. WormBook the online review of C elegans biology pp. 1-18.
3. Jantsch-Plunger V, Gönczy P, Romano A, Schnabel H, Hamill D, et al. (2000) CYK-4: A Rho family gtpase activating protein (GAP) required for central spindle formation and cytokinesis. J Cell Biol 149: 1391-1404.
4. Zallen JA, Peckol EL, Tobin DM, Bargmann CI, (2000) Neuronal cell shape and neurite initiation are regulated by the Ndr kinase SAX-1, a member of the Orb6/COT-1/warts serine/threonine kinase family. Mol Biol Cell 11: 3177-3190.
5. Withee J, Galligan B, Hawkins N, Garriga G, (2004) Caenorhabditis elegans WASP and Ena/VASP proteins play compensatory roles in morphogenesis and neuronal cell migration. Genetics 167: 1165-1176.
6. Soto MC, Qadota H, Kasuya K, Inoue M, Tsuboi D, et al. (2002) The GEX-2 and GEX-3 proteins are required for tissue morphogenesis and cell migrations in C. elegans. Genes Dev 16: 620-632.
7. Canevascini S, Marti M, Fröhli E, Hajnal A, (2005) The Caenorhabditis elegans homologue of the proto-oncogene ect-2 positively regulates RAS signalling during vulval development. EMBO Rep 6: 1169-1175.
8. Strutt DI, Weber U, Mlodzik M, (1997) The role of RhoA in tissue polarity and Frizzled signalling. Nature 387: 292-295.
9. Sugihara K, Nakatsuji N, Nakamura K, Nakao K, Hashimoto R, et al. (1998) Rac1 is required for the formation of three germ layers during gastrulation. Oncogene 17: 3427-3433.
10. Wang L, Zheng Y, (2007) Cell type-specific functions of Rho GTPases revealed by gene targeting in mice. Trends Cell Biol 17: 58-64.
11. Corbetta S, Gualdoni S, Albertinazzi C, Paris S, Croci L, et al. (2005) Generation and characterization of Rac3 knockout mice. Mol Cell Biol 25: 5763-5776.
12. Hakem A, Sanchez-Sweatman O, You-Ten A, Duncan G, Wakeham A, et al. (2005) RhoC is dispensable for embryogenesis and tumor initiation but essential for metastasis. Genes Dev 19: 1974-1979.
13. Li S, Yamauchi A, Marchal CC, Molitoris JK, Quilliam LA, et al. (2002) Chemoattractant-stimulated Rac activation in wild-type and Rac2-deficient murine neutrophils: preferential activation of Rac2 and Rac2 gene dosage effect on neutrophil functions. J Immunol 169: 5043-5051.
14. Liu AX, Rane N, Liu JP, Prendergast GC, (2001) RhoB is dispensable for mouse development, but it modifies susceptibility to tumor formation as well as cell adhesion and growth factor signaling in transformed cells. Mol Cell Biol 21: 6906-6912.
15. Glogauer M, Marchal CC, Zhu F, Worku A, Clausen BE, et al. (2003) Rac1 deletion in mouse neutrophils has selective effects on neutrophil functions. J Immunol 170: 5652-5657.
16. Gu Y, Jia B, Yang FC, D'Souza M, Harris CE, et al. (2001) Biochemical and biological characterization of a human Rac2 GTPase mutant associated with phagocytic immunodeficiency. J Biol Chem 276: 15929-15938.
17. Williams DA, Tao W, Yang F, Kim C, Gu Y, et al. (2000) Dominant negative mutation of the hematopoietic-specific Rho GTPase, Rac2, is associated with a human phagocyte immunodeficiency. Blood 96: 1646-1654.
18. Meng Y, Takahashi H, Meng J, Zhang Y, Lu G, et al. (2004) Regulation of ADF/cofilin phosphorylation and synaptic function by LIM-kinase. Neuropharmacology 47: 746-754.
19. Meng Y, Zhang Y, Tregoubov V, Janus C, Cruz L, et al. (2002) Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron 35: 121-133.
20. Soderling SH, Langeberg LK, Soderling JA, Davee SM, Simerly R, et al. (2003) Loss of WAVE-1 causes sensorimotor retardation and reduced learning and memory in mice. Proc Natl Acad Sci USA 100: 1723-1728.
21. Chechlacz M, Gleeson JG, (2003) Is mental retardation a defect of synapse structure and function? Pediatr Neurol 29: 11-17.
22. Ramakers GJA, (2002) Rho proteins, mental retardation and the cellular basis of cognition. Trends Neurosci 25: 191-199.
23. Gu Y, Filippi M-D, Cancelas JA, Siefring JE, Williams EP, et al. (2003) Hematopoietic cell regulation by Rac1 and Rac2 guanosine triphosphatases. Science 302: 445-449.
24. McMullan R, Hiley E, Morrison P, Nurrish SJ, (2006) Rho is a presynaptic activator of neurotransmitter release at pre-existing synapses in C. elegans. Genes Dev 20: 65-76.
25. Hodgkin J, Kuwabara PE, Corneliussen B, (2000) A novel bacterial pathogen, Microbacterium nematophilum, induces morphological change in the nematode C. elegans. Curr Biol 10: 1615-1618.
26. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
27. van der Linden AM, Moorman C, Cuppen E, Korswagen HC, Plasterk RHA, (2003) Hyperactivation of the G12-mediated signaling pathway in Caenorhabditis elegans induces a developmental growth arrest via protein kinase C. Curr Biol 13: 516-521.
28. Nurrish S, Ségalat L, Kaplan JM, (1999) Serotonin inhibition of synaptic transmission: Galpha(0) decreases the abundance of UNC-13 at release sites. Neuron 24: 231-242.
29. Liu DW, Thomas JH, (1994) Regulation of a periodic motor program in C. elegans. J Neurosci 14: 1953-1962.
30. Norman KR, Fazzio RT, Mellem JE, Espelt MV, Strange K, et al. (2005) The Rho/Rac-family guanine nucleotide exchange factor VAV-1 regulates rhythmic behaviors in C. elegans. Cell 123: 119-132.
31. Koelle MR, Horvitz HR, (1996) EGL-10 regulates G protein signaling in the C. elegans nervous system and shares a conserved domain with many mammalian proteins. Cell 84: 115-125.
32. Ségalat L, Elkes DA, Kaplan JM, (1995) Modulation of serotonin-controlled behaviors by Go in Caenorhabditis elegans. Science 267: 1648-1651.
33. Community TCeR, eds. Stiernagle T Maintenance of C. elegans. WormBook: WormBook.
34. Luo L, (2000) Rho GTPases in neuronal morphogenesis. Nat Rev Neurosci 1: 173-180.
35. Schwamborn JC, Puschel AW, (2004) The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat Neurosci 7: 923-929.
36. Threadgill R, (1997) Regulation of dendritic growth and remodeling by Rho, Rac, and Cdc42. Neuron 19: 625-634.
37. Rand JB, (2007) Acetylcholine. WormBook pp. 1-21.
38. Raizen DM, Lee RY, Avery L, (1995) Interacting genes required for pharyngeal excitation by motor neuron MC in Caenorhabditis elegans. Genetics 141: 1365-1382.
39. Rand JB, Russell RL, (1984) Choline acetyltransferase-deficient mutants of the nematode Caenorhabditis elegans. Genetics 106: 227-248.
40. Weinshenker D, Garriga G, Thomas JH, (1995) Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans. J Neurosci 15: 6975-6985.
41. Swärd K, Mita M, Wilson DP, Deng JT, Susnjar M, et al. (2003) The role of RhoA and Rho-associated kinase in vascular smooth muscle contraction. Curr Hypertens Rep 5: 66-72.
42. Schafer WR, (2005) Egg-laying. WormBook the online review of C elegans biology pp. 1-7.
43. Bany IA, Dong M-Q, Koelle MR, (2003) Genetic and cellular basis for acetylcholine inhibition of Caenorhabditis elegans egg-laying behavior. J Neurosci 23: 8060-8069.
44. Diogon M, Wissler F, Quintin S, Nagamatsu Y, Sookhareea S, et al. (2007) The RhoGAP RGA-2 and LET-502/ROCK achieve a balance of actomyosin-dependent forces in C. elegans epidermis to control morphogenesis. Development 134: 2469-2479.
45. Branicky R, Hekimi S, (2006) What keeps C. elegans regular: the genetics of defecation. Trends Genet 22: 571-579.
46. Eisenmann DM, Kim SK, (2000) Protruding vulva mutants identify novel loci and Wnt signaling factors that function during Caenorhabditis elegans vulva development. Genetics 156: 1097-1116.
47. Miller KG, Alfonso A, Nguyen M, Crowell JA, Johnson CD, et al. (1996) A genetic selection for Caenorhabditis elegans synaptic transmission mutants. Proc Natl Acad Sci USA 93: 12593-12598.
48. Nguyen M, Alfonso A, Johnson CD, Rand JB, (1995) Caenorhabditis elegans mutants resistant to inhibitors of acetylcholinesterase. Genetics 140: 527-535.
49. Rogers CM, Franks CJ, Walker RJ, Burke JF, Holden-Dye L, (2001) Regulation of the pharynx of Caenorhabditis elegans by 5-HT, octopamine, and FMRFamide-like neuropeptides. J Neurobiol 49: 235-244.
50. Sieburth D, Madison JM, Kaplan JM, (2007) PKC-1 regulates secretion of neuropeptides. Nat Neurosci 10: 49-57.
51. McMullan R, Nurrish SJ, (2007) Rho deep in thought. Genes Dev 21: 2677-2682.
52. Davis MW, Morton JJ, Carroll D, Jorgensen EM, (2008) Gene activation using FLP recombinase in C. elegans. PLoS Genet 4: e1000028.
53. Allen WE, Zicha D, Ridley AJ, Jones GE, (1998) A role for Cdc42 in macrophage chemotaxis. J Cell Biol 141: 1147-1157.
54. Luo L, Liao YJ, Jan LY, Jan YN, (1994) Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev 8: 1787-1802.
55. Fukushige T, Brodigan TM, Schriefer LA, Waterston RH, Krause M, (2006) Defining the transcriptional redundancy of early bodywall muscle development in C. elegans: evidence for a unified theory of animal muscle development. Genes Dev 20: 3395-3406.
56. Wissmann A, Ingles J, McGhee JD, Mains PE, (1997) Caenorhabditis elegans LET-502 is related to Rho-binding kinases and human myotonic dystrophy kinase and interacts genetically with a homolog of the regulatory subunit of smooth muscle myosin phosphatase to affect cell shape. Genes Dev 11: 409-422.
57. Sahai E, Alberts AS, Treisman R, (1998) RhoA effector mutants reveal distinct effector pathways for cytoskeletal reorganization, SRF activation and transformation. EMBO J 17: 1350-1361.
58. Nurrish S, Segalat L, Kaplan JM, (1999) Serotonin inhibition of synaptic transmission: Galpha(0) decreases the abundance of UNC-13 at release sites. Neuron 24: 231-242.
59. Mahoney TR, Luo S, Round EK, Brauner M, Gottschalk A, et al. (2008) Intestinal signaling to GABAergic neurons regulates a rhythmic behavior in Caenorhabditis elegans. Proc Natl Acad Sci U S A 105: 16350-16355.
60. Chen JC, Zhuang S, Nguyen TH, Boss GR, Pilz RB, (2003) Oncogenic Ras leads to Rho activation by activating the mitogen-activated protein kinase pathway and decreasing Rho-GTPase-activating protein activity. J Biol Chem 278: 2807-2818.
61. Fujishiro S-H, Tanimura S, Mure S, Kashimoto Y, Watanabe K, et al. (2008) ERK1/2 phosphorylate GEF-H1 to enhance its guanine nucleotide exchange activity toward RhoA. Biochem Biophys Res Commun 368: 162-167.
62. Li W, Chong H, Guan KL, (2001) Function of the Rho family GTPases in Ras-stimulated Raf activation. J Biol Chem 276: 34728-34737.
63. Nicholas HR, Hodgkin J, (2004) The ERK MAP kinase cascade mediates tail swelling and a protective response to rectal infection in C. elegans. Curr Biol 14: 1256-1261.
64. Kayne PS, Sternberg PW, (1995) Ras pathways in Caenorhabditis elegans. Curr Opin Genet Dev 5: 38-43.
65. Sundaram MV, (2006) RTK/Ras/MAPK signaling. WormBook the online review of C elegans biology pp. 1-19.
66. Matthews HK, Marchant L, Carmona-Fontaine C, Kuriyama S, Larraín J, et al. (2008) Directional migration of neural crest cells in vivo is regulated by Syndecan-4/Rac1 and non-canonical Wnt signaling/RhoA. Development 135: 1771-1780.
67. Steven R, Zhang L, Culotti J, Pawson T, (2005) The UNC-73/Trio RhoGEF-2 domain is required in separate isoforms for the regulation of pharynx pumping and normal neurotransmission in C. elegans. Genes Dev 19: 2016-2029.
68. Williams SL, Lutz S, Charlie NK, Vettel C, Ailion M, et al. (2007) Trio's Rho-specific GEF domain is the missing Galpha q effector in C. elegans. Genes Dev 21: 2731-2746.
69. Hiley E, McMullan R, Nurrish SJ, (2006) The Galpha12-RGS RhoGEF-RhoA signalling pathway regulates neurotransmitter release in C. elegans. EMBO J 25: 5884-5895.
70. Ellenbroek SIJ, Collard JG, (2007) Rho GTPases: functions and association with cancer. Clin Exp Metastasis 24: 657-672.
71. Govek E-E, Newey SE, Van Aelst L, (2005) The role of the Rho GTPases in neuronal development. Genes Dev 19: 1-49.
72. Rolfe BE, Worth NF, World CJ, Campbell JH, Campbell GR, (2005) Rho and vascular disease. Atherosclerosis 183: 1-16.
73. Sharpe CC, Hendry BM, (2003) Signaling: focus on Rho in renal disease. J Am Soc Nephrol 14: 261-264.
74. Hall A, (1998) Rho GTPases and the actin cytoskeleton. Science 279: 509-514.
75. Bustelo XR, (2002) Understanding Rho/Rac biology in T-cells using animal models. Bioessays 24: 602-612.