The Secretory Pathway Calcium ATPase PMR-1/SPCA1 Has Essential Roles in Cell Migration during Embryonic Development
Maintaining levels of calcium in the cytosol is important for many cellular events, including cell migration, where localized regions of high calcium are required to regulate cytoskeletal dynamics, contractility, and adhesion. Studies show inositol-trisphosphate receptors (IP3R) and ryanodine receptors (RyR), which release calcium into the cytosol, are important regulators of cell migration. Similarly, proteins that return calcium to secretory stores are likely to be important for cell migration. The secretory protein calcium ATPase (SPCA) is a Golgi-localized protein that transports calcium from the cytosol into secretory stores. SPCA has established roles in protein processing, metal homeostasis, and inositol-trisphosphate signaling. Defects in the human SPCA1/ATP2C1 gene cause Hailey-Hailey disease (MIM# 169600), a genodermatosis characterized by cutaneous blisters and fissures as well as keratinocyte cell adhesion defects. We have determined that PMR-1, the Caenorhabditis elegans ortholog of SPCA1, plays an essential role in embryogenesis. Pmr-1 strains isolated from genetic screens show terminal phenotypes, such as ventral and anterior enclosure failures, body morphogenesis defects, and an unattached pharynx, which are caused by earlier defects during gastrulation. In Pmr-1 embryos, migration rates are significantly reduced for cells moving along the embryo surface, such as ventral neuroblasts, C-derived, and anterior-most blastomeres. Gene interaction experiments show changing the activity of itr-1/IP3R and unc-68/RyR modulates levels of embryonic lethality in Pmr-1 strains, indicating pmr-1 acts with these calcium channels to regulate cell migration. This analysis reveals novel genes involved in C. elegans cell migration, as well as a new role in cell migration for the highly conserved SPCA gene family.
Vyšlo v časopise:
The Secretory Pathway Calcium ATPase PMR-1/SPCA1 Has Essential Roles in Cell Migration during Embryonic Development. PLoS Genet 9(5): e32767. doi:10.1371/journal.pgen.1003506
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003506
Souhrn
Maintaining levels of calcium in the cytosol is important for many cellular events, including cell migration, where localized regions of high calcium are required to regulate cytoskeletal dynamics, contractility, and adhesion. Studies show inositol-trisphosphate receptors (IP3R) and ryanodine receptors (RyR), which release calcium into the cytosol, are important regulators of cell migration. Similarly, proteins that return calcium to secretory stores are likely to be important for cell migration. The secretory protein calcium ATPase (SPCA) is a Golgi-localized protein that transports calcium from the cytosol into secretory stores. SPCA has established roles in protein processing, metal homeostasis, and inositol-trisphosphate signaling. Defects in the human SPCA1/ATP2C1 gene cause Hailey-Hailey disease (MIM# 169600), a genodermatosis characterized by cutaneous blisters and fissures as well as keratinocyte cell adhesion defects. We have determined that PMR-1, the Caenorhabditis elegans ortholog of SPCA1, plays an essential role in embryogenesis. Pmr-1 strains isolated from genetic screens show terminal phenotypes, such as ventral and anterior enclosure failures, body morphogenesis defects, and an unattached pharynx, which are caused by earlier defects during gastrulation. In Pmr-1 embryos, migration rates are significantly reduced for cells moving along the embryo surface, such as ventral neuroblasts, C-derived, and anterior-most blastomeres. Gene interaction experiments show changing the activity of itr-1/IP3R and unc-68/RyR modulates levels of embryonic lethality in Pmr-1 strains, indicating pmr-1 acts with these calcium channels to regulate cell migration. This analysis reveals novel genes involved in C. elegans cell migration, as well as a new role in cell migration for the highly conserved SPCA gene family.
Zdroje
1. BriniM, CarafoliE (2009) Calcium pumps in health and disease. Phys Rev 89: 1341–1378.
2. BrundageRA, FogartyKE, TuftRA, FayFS (1991) Calcium gradients underlying polarization and chemotaxis of eosinophils. Science 254: 703–706.
3. RidleyAJ, SchwartzMA, BurridgeK, FirtelRA, GinsbergMH, et al. (2003) Cell Migration: Integrating signals from front to back. Science 302: 1704–1709.
4. WeiC, WangX, ZhengM, ChengH (2012) Calcium gradients underlying cell migration. Curr Opin Cell Biol 24: 254–261.
5. WeiC, WangX, ChenM, OuyangK, ZhengM, et al. (2010) Flickering calcium microdomains signal turning of migrating cells. Can J Physiol Pharmacol 88: 105–110.
6. WeiC, WangX, ChenM, OuyangK, SongLS, et al. (2009) Calcium flickers steer cell migration. Nature 457: 901–906.
7. ZampeseE, PizzoP (2012) Intracellular organelles in the saga of Ca2+ homeostasis: different molecules for different purposes? Cell Mol Life Sci 69: 1077–1104.
8. HoweAK (2011) Cross-talk between calcium and protein kinase A in the regulation of cell migration. Curr Opin Cell Biology 23: 554–561.
9. VandecaetsbeekI, VangheluweP, RaeymaekersL, WuytackF, VanoevelenJ (2011) The Ca2+ Pumps of the endoplasmic reticulum and Golgi apparatus. Cold Spring Harbor Perspectives in Biology 3: a004184.
10. MissiaenL, DodeL, VanoevelenJ, RaeymaekersL, WuytackF (2007) Calcium in the Golgi apparatus. Cell Calcium 41: 405–416.
11. HeW, HuZ (2012) The role of the Golgi-resident SPCA Ca2+ Mn2+ pump in ionic homeostasis and neural function. Neurochem Res 37: 455–468.
12. HaileyH, HaileyH (1939) Familial benign chronic pemphigus. Arch Dermatol Syphilol 39: 679–685.
13. HuZ, BonifasJM, BeechJ, BenchG, ShigiharaT, et al. (2000) Mutations in ATP2C1, encoding a calcium pump, cause Hailey-Hailey disease. Nature Genet 24: 61–65.
14. KellermayerR (2005) Hailey-Hailey disease is an orthodisease of PMR-1 deficiency in Saccharomyces cerevisiae. FEBS Letters 579: 2021–2025.
15. Missiaenv, RaeymaekersL, DodeL, VanoevelenJ, Van BaelenK, et al. (2004) SPCA1 pumps and Hailey-Hailey disease. Biochem Biophys Res Comm 322: 1204–1213.
16. SudbrakR, BrownJ, Dobson-StoneC, CarterS, RamserJ, et al. (2000) Hailey-Hailey disease is caused by mutations in ATP2C1 encoding a novel Ca2+ pump. Hum Mol Genet 12: 1131–1140.
17. HwangL, LeeJ, RichardG, UittoJ, HsuS (2004) Type 1 segmental manifestation of Hailey-Hailey disease. J Am Acad Dermatol 49: 712–714.
18. Poblete-GutierrezP, WiederholtT, KonigA, JugertF, MarquardtY, et al. (2004) Allelic loss underlies type 2 segmental Hailey-Hailey disease, providing molecular confirmation of a novel genetic concept. J Clin Invest 114: 1407–1409.
19. OkunadeGW, MillerML, AzharM, AndringaA, SanfordL, et al. (2007) Loss of the Atp2c1 Secretory Pathway Ca2+-ATPase (SPCA1) in mice causes Golgi stress, apoptosis, and midgestational death in homozygous embryos and squamous cell tumors in adult heterozygotes. J Biol Chem 282: 26517–26527.
20. ChunSI, WhangKC, SuWP (1988) Squamous cell carcinoma arising in Hailey-Hailey disease. J Cutan Pathol 15: 234–237.
21. CockayneSE, RasslDM, ThomasSE (2000) Squamous cell carcinoma arising in Hailey-Hailey disease of the vulva. Br J Dermatol 142: 540–542.
22. HolstVA, FairKP, WilsonBB, PattersonJW (2000) Squamous cell carcinoma arising in Hailey-Hailey disease. J Am Acad Dermatol 43: 368–371.
23. MetzeD, HammH, SchoratA, LugerT (1995) Involvement of the adherens junction-actin filament system in acantholytic dyskeratosis of Hailey-Hailey disease. A histological, ultrastructural, and histochemical study of lesional and non-lesional skin. J Cutan Pathol 23: 211–222.
24. HashimotoK, FujiwaraK, TadaJ, HaradaM, SetoyamaM, et al. (1995) Desmosomal dissolution in Grover's disease, Hailey-Hailey's disease and Darier's disease. J Cutan Pathol 1995: 488–501.
25. ShullG, MillerML, PrasadV (2011) Secretory pathway stress responses as possible mechanisms of disease involving Golgi Ca2+ pump dysfunction. Biofactors 37: 150–158.
26. BaylisH, Vazquez-ManriqueR (2012) Genetic analysis of IP3 and calcium signaling pathways in C. elegans. Biochimica et Biophysica Acta General subjects 1280: 1253–1268.
27. Thomas-VirnigCL, SimsP, SimskeJS, HardinJ (2004) The Inositol 1,4,5-Trisphosphate Receptor Regulates Epidermal Cell Migration in Caenorhabditis elegans. Curr Biol 14: 1882–1887.
28. WalkerDS, GowerNJ, LyS, BradleyGL, BaylisHA (2002) Regulated disruption of inositol 1,4,5-trisphosphate signaling in Caenorhabditis elegans reveals new functions in feeding and embryogenesis. Mol Biol Cell 1329–1337.
29. MaryonEB, SaariB, AndersonP (1998) Muscle-specific functions of ryanodine receptor channels in Caenorhabditis elegans. J Cell Sci 111: 2885–2895.
30. SakubeY, AndoH, KagawaH (1997) An abnormal ketamine response in mutants defective in the ryanodine receptor gene ryr-1 (unc-68) of Caenorhabditis elegans. J of Mol Biol 267: 849–864.
31. LiuQ, ChenB, YankovaM, MorestK, MaryonEB, et al. (2005) Presynaptic Ryanodine Receptors are required for normal quantal size at the Caenorhabditis elegans neuromuscular junction. J Neuroscience 25: 6745–6754.
32. ZalkR, LehnartSE, MarksAR (2007) Modulation of the Ryanodine Receptor and intracellular calcium. Ann Rev Biochem 76: 367–385.
33. Van BaelenK, VanoevelenJ, MissiaenL, WuytackF (2001) The Golgi pmr1 p-type ATPase of Caenorhabditis elegans. J Biol Chem 276: 10683–10691.
34. MissiaenL, Van AckerK, ParysJB, De SmedtH, Van BaelenK, et al. (2001) Baseline cytosolic Ca2+ oscillations derived from a non-endoplasmic reticulum Ca2+ store. J Biol Chem 276: 39161–39170.
35. ChoJ, KoK, GunasekaranS, AhnnJ (2005) Caenorhabditis elegans PMR1, a P-type Calcium ATPase is important for calcium/manganese homeostasis and oxidative stress response. FEBS Letters 578: 778–782.
36. CelnikerSE, DillonLAL, GersteinMB, GunsalusKC, HenikoffS, et al. (2009) Unlocking the secrets of the genome. Nature 459: 927–930.
37. TabaraH, MotohashiT, KoharaY (1996) A multi-well version of in situ hybridization on whole mount embryos of Caenorhabditis elegans. Nucl Acids Res 24: 2119–2124.
38. LevinM, HashimshonyT, WagnerF, YanaiI (2012) Developmental milestones punctuate gene expression in the Caenorhabditis embryo. Dev Cell 22: 1101–1108.
39. Hunt-NewburyR, ViveirosR, JohnsenR, MahA, AnastasD, et al. (2007) High-throughput in vivo analysis of gene expression in Caenorhabditis elegans. PLoS Biol 5: e237 doi:10.1371/journal.pbio.0050237.
40. KellyWG, XuS, MontgomeryMK, FireA (1997) Distinct requirements for somatic and germline expression of a generally expressed Caenorhabditis elegans gene. Genetics 146: 227–238.
41. BandyopadhyayJ, SongH, ParkB, SingaraveluG, SunJ, et al. (2009) Functional assessment of Nramp-like metal transporters and manganese in Caenorhabditis elegans. Biochem Biophys Res Commun 390: 136–141.
42. KourtisN, NikoletopoulouV, TavernarakisN (2012) Small heat-shock proteins protect from heat-stroke-associated neurodegeneration. Nature 490: 213–218.
43. Gengyo-AndoK, MitaniS (2000) Characterization of mutations induced by ethyl methanesulfonate, UV, and trimethylpsoralen in the nematode Caenorhabditis elegans. Biochem Biophysica Res Comm 269: 64–69.
44. ToyoshimaC, MizutaniT (2004) Crystal structure of the calcium pump with a bound ATP analogue. Nature 430: 529–535.
45. SonnichsenB, KoskiLB, WalshA, MarschallP, NeumannB, et al. (2005) Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434: 462–469.
46. Wormbase (2012) http://www.wormbase.org/db/get?name=WBGene00004063class=Gene.
47. SulstonJE, SchierenbergE, WhiteJG, ThomsonJN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Developmental Biology 100: 64–119.
48. Williams-MassonEM, HeidPJ, LavinCA, HardinJ (1998) The cellular mechanism of epithelial rearrangement during morphogenesis of the Caenorhabditis elegans dorsal hypodermis. Developmental Biology 204: 263–276.
49. PortereikoM, MangoS (2001) Early morphogenesis of the Caenorhabditis elegans pharynx. Dev Biol 233: 482–494.
50. BaoZ, MurrayJI, BoyleT, OoiSL, SandelMJ, et al. (2006) Automated cell lineage tracing in Caenorhabditis elegans. PNAS 2707–2712.
51. BoyleTJ, BaoZ, MurrayJI, ArayaCL, WaterstonRH (2006) AceTree: a tool for visual analysis of Caenorhabditis elegans embryogenesis. BMC Bioinformatics 7: 275.
52. MurrayJI, BaoZ, BoyleTJ, BoeckME, MericleBL, NicholasTJ, et al. (2008) Automated analysis of embryonic gene expression with cellular resolution in C. elegans. Nature Methods 5: 703–709.
53. MurrayJI, BaoZ, BoyleT, WaterstonRH (2006) The lineaging of fluorescently-labeled Caenorhabditis elegans embryos with StarryNite and AceTree. Nature Protocols 1: 1468–1476.
54. AhringerJ (1996) Posterior patterning by the Caenorhabditis elegans even-skipped homolog vab-7. Genes Dev 10: 1120–1130.
55. WittmannC, BossingerO, GoldsteinB, FleischmannM, KohlerR, et al. (1997) The expression of the C. elegans labial-like Hox gene ceh-13 during early embryogenesis relies on cell fate and on anteroposterior cell polarity. Development 124: 4193–4200.
56. CassataG, ShemerG, MorandiP, DonhauserR, PodbilewiczB (2005) ceh-16/engrailed patterns the embryonic epidermis of Caenorhabditis elegans. Development 132: 739–749.
57. BrunschwigK, WittmanC, SchnabelR, BurglinT, ToblerH, et al. (1999) Anterior organization of the C. elegans embryo by the labial-like Hox gene ceh-13. Development 126: 1537–1546.
58. Nance, J. et al.. Gastrulation in C. elegans (September 26, 2005), WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.23.1, http://www.wormbook.org.
59. RohrschneiderM, NanceJ (2009) Polarity and cell fate specification in the control of Caenorhabditis elegans gastrulation. Dev Dynamics 238: 789–796.
60. HarrellJB, GoldsteinB (2011) Internalization of multiple cells during C. elegans gastrulation depends on common cytoskeletal mechanisms but different cell polarity and cell fate regulators. Dev Biol 350: 1–12.
61. NanceJ, MunroEM, PriessJ (2003) C. elegans PAR-3 and PAR-6 are required for apicobasal asymmetries associated with cell adhesion and gastrulation. Development 130: 5339–5350.
62. PraitisV, CicconeE, AustinJ (2005) SMA-1 spectrin has essential roles in epithelial cell sheet morphogenesis in C. elegans. Dev l Biol 283: 157–170.
63. KangS, KramerJ (2000) Nidogen is nonessential and not required for normal type IV collagen localization in Caenorhabditis elegans. Mol Biol Cell 3911–3923.
64. TrzebiatowskaA, TopfU, SauderU, DrabikowskiK, Chiquet-EhrismannR (2008) Caenorhabditis elegans teneurin, ten-1, is required for gonadal and pharyngeal basement membrane integrity and acts redundantly with integrin ina-1 and dystroglycan dgn-1. Mol Biol Cell 19: 3898–3908.
65. SimskeJS, KoppenM, SimsP, HodgkinJ, YonkofA, et al. (2003) The cell junction protein VAB-9 regulates adhesion and epidermal morphology in C. elegans. Nat Cell Biol 5: 619–625.
66. KoppenM, SimskeJS, SimsPA, FiresteinBL, HallDH, et al. (2001) Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nat Cell Biol 3: 983–991.
67. PieknyAJ, MainsPE (2002) Rho-binding kinase (LET-502) and myosin phosphatase (MEL-11) regulate cytokinesis in the early Caenorhabditis elegans embryo. J Cell Sci 115: 2271–2282.
68. PieknyAJ, JohnsonJL, ChamGD, MainsPE (2003) The Caenorhabditis elegans nonmuscle myosin genes nmy-1 and nmy-2 function as redundant components of the let-502/Rho-binding kinase and mel-11/myosin phosphatase pathway during embryonic morphogenesis. Development 130: 5695–5704.
69. NakaoF, HudsonM, SuzukiM, PecklerZ, KurokawaR, et al. (2007) The plexin PLX-2 and the ephrin EFN-4 have distinct roles in MAB-20/Semaphorin 2A signaling in C. elegans morphogenesis. Genetics 176: 1591–1607.
70. RugarliE, Di SchiaviE, HilliardM, ArbucciS, GhezziC, et al. (2002) The Kallmann syndrome gene homolog in C. elegans is involved in epidermal morphogenesis and neurite branching. Development 129: 1283–1294.
71. ClandininT, DeModenaJ, SternbergP (1998) Inositol trisphosphate mediates a RAS-independent response to LET-23 receptor tyrosine kinase activation in C. elegans. Cell 92: 523–533.
72. EspeltMV, EstevezAY, YinX, StrangeK (2005) Oscillatory calcium signaling in the isolated Caenorhabditis elegans intestine: Role of the Inositol-1,4,5-trisphosphate Receptor and Phospholipases C beta and gamma. J Gen Physiol 126: 379–392.
73. FoskettJK, WhiteC, CheungK-H, MakD-OD (2007) Inositol Trisphosphate Receptor Ca2 Release Channels. Physiol Rev 87: 593–658.
74. Van PetegemF (2012) Ryanodine Receptors: Structure and function. J Biol Chem 287: 31624–31632.
75. Stiernagle, T. Maintenance of C. elegans (February 11, 2006), WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.101.1, http://www.wormbook.org.
76. KarabinosA, SchmidtH, HarborthJ, SchnabelR, WeberK (2001) Essential roles for four cytoplasmic intermediate filament proteins in Caenorhabditis elegans development. Proc Natl Acad Sci U S A 98: 7863–7868.
77. HapiakV, HreskoMC, SchrieferLA, SaiyasisongkhramK, BercherM, et al. (2003) mua-6, a gene required for tissue integrity in Caenorhabditis elegans, encodes a cytoplasmic intermediate filament. Developmental Biology 263: 330–342.
78. WooWM, GoncharovA, JinY, ChisholmAD (2004) Intermediate filaments are required for C. elegans epidermal elongation. Dev Biol 267: 216–229.
79. CarberryK, WiesenfahrtT, WindofferR, BossingerO, LeubeRE (2009) Intermediate Filaments in Caenorhabditis elegans. Cell Motility and the Cytoskeleton 66: 852–864.
80. DingM, GoncharovA, JinY, ChisholmAD (2003) C. elegans ankyrin repeat protein VAB-19 is a component of epidermal attachment structures and is essential for epidermal morphogenesis. Development 130: 5791–5801.
81. BosherJM, HahnBS, LegouisR, SookhareeaS, WeimerRM, et al. (2003) The Caenorhabditis elegans vab-10 spectraplakin isoforms protect the epidermis against internal and external forces. J Cell Biol 161: 757–768.
82. HreskoMC, SchrieferLA, ShrimankarP, WaterstonRH (1999) Myotactin, a novel hypodermal protein involved in muscle-cell adhesion in Caenorhabditis elegans. J Cell Biol 146: 659–672.
83. HongL, ElblT, WardJ, Franzini-ArmstrongC, RybickaKK, et al. (2001) MUP-4 is a novel transmembrane protein with functions in epithelial cell adhesion in Caenorhabditis elegans. J Cell Biol 154: 403–414.
84. FuchsE, RaghavanS (2002) Getting under the skin of epidermal morphogenesis. Nature Reviews, Genetics 3: 199–209.
85. BrennerS (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94.
86. PraitisV, CaseyE, CollarD, AustinJ (2001) Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157: 1217–1226.
87. Fay, D. Genetic mapping and manipulation: Chapter 5-SNPs: Three-point mapping (February 17, 2006), WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.94.1, http://www.wormbook.org.
88. WilliamsBD, SchrankB, HuynhC, ShownkeenR, WaterstonRH (1992) A genetic mapping system in C. elegans based on polymorphic sequence-tagged sites. Genetics 131: 609–624.
89. WicksS, YehR, GishW, WaterstonR, PlasterkR (2001) Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nature Genetics 28: 160–164.
90. Fay, D. Genetic mapping and manipulation: Chapter 5-SNPs: Three-point mapping (February 17, 2006), WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.94.1, http://www.wormbook.org.
91. BigelowH, DoitsidouM, SarinS, HobertO (2009) MAQGene: Software to facilitate C. elegans mutant genome sequence analysis. Nature Methods 6: 549.
92. MelloCC, KramerJM, StinchcombD, AmbrosV (1991) Efficient gene transfer in C. elegans : extrachromosomal maintanance and integration of transforming sequences. EMBO Journal 10: 3959–3970.
93. EvansTC, CrittendenSL, KoyoyianniV, KimbleJ (1994) Translational control of maternal glp-1 mRNA establishes an asymmetry in the C. elegans embryo. Cell 77: 183–194.
94. McKeownC, PraitisV, AustinJ (1998) sma-1 encodes a BH-spectrin homolog required for Caenorhabditis elegans morphogenesis. Development 125: 2087–2098.
95. Ahringer, J., ed. Reverse genetics (April 6, 2006), WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.47.1, http://www.wormbook.org.
96. HadwigerG, DourS, ArurS, FoxP, NonetM (2010) A monoclonal antibody toolkit for C. elegans. PLoS ONE 5: e10161 doi:10.1371/journal.pone.0010161.
97. Sulston, J E and White, J G (1988) “Parts list”. In: Wood, W. B., Wood, W. B.s. The Nematode Caenorhabditis elegans. Cold Spring Harbor, New York, USA: Cold Spring Harbor Laboratory Press. pp. 415–431.
98. WormAtlas, Altun, Z.F., Herndon, L.A., Crocker, C., Lints, R.and Hall, D.H.(eds); 2002–22012. http://www.wormatlas.org
99. MohlerWA, SimskeJS, Williams-MassonEM, HardinJD, WhiteJG (1998) Dynamics and ultrastructure of developmental cell fusions in the Caenorhabditis elegans hypodermis. Curr Biol 8: 1087–1090.
100. KrauseM, HarrisonSW, XuSQ, ChenL, FireA (1994) Elements regulating cell- and stage-specific expression of the C. elegans MyoD family homolog hlh-1. Developmental Biology 166: 133–148.
101. ChenLM, KrauseM, Sepanski, FireA (1994) The Caenorhabditis elegans MYOD homologue HLH-1 is essential for proper muscle function and complete morphogenesis. Development 120: 1631–1640.
102. KingRS, MaidenSL, HawkinsNC, KiddAR, KimbleJ, et al. (2009) The N- or C-terminal domains of DSH-2 can activate the C. elegans Wnt/beta-catenin asymmetry pathway. Developmental Biology 238: 234–244.
103. ChalfieM, TuY, EuskirchenG, WardWW, PrasherDC (1994) Green fluorescent protein as a marker for gene expression. Science 263: 802–805.
104. Altun-GultekinZF, AndachiY, TsalikEL, PilgrimD, KoharaY, et al. (2001) A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23, controls cell fate specification of a defined interneuron class in C. elegans. Development 128: 1951–1969.
105. IkegamiR, SimokatK, ZhengH, BrownL, GarrigaG, et al. (2012) Semaphorin and Eph receptor signaling guide a series of cell movements for ventral enclosure in C. elegans. Current Biology 22: 1–11.
106. GranaTM, CoxEA, LynchAM, HardinJ (2010) SAX-7/L1CAM and HMR-1/cadherin function redundantly in blastomere compaction and non-muscle myosin accumulation during Caenorhabditis elegans gastrulation. Developmental Biology 344: 731–744.
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