Gonad morphogenesis and distal tip cell migration in the Caenorhabditis elegans hermaphrodite

Wiley Interdisciplinary Reviews: Developmental Biology

Volumn 1, Issue 4, 2012, Pages 519-531

  Wong, Ming Ching ^a   Schwarzbauer, Jean E ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; G PROTEIN COUPLED RECEPTOR KINASE; INTEGRIN; MEMBRANE PROTEIN; NETRIN; P21 ACTIVATED KINASE 1; STEROID RECEPTOR COACTIVATOR 1; TALIN;

BASEMENT MEMBRANE; CAENORHABDITIS ELEGANS; CELL ADHESION; CELL MIGRATION; CYTOSKELETON; EXTRACELLULAR MATRIX; FBL 1 GENE; GENE; GON 1 GENE; GONAD DEVELOPMENT; HERMAPHRODITE; INTRACELLULAR SIGNALING; MIG 6 GENE; MORPHOGENESIS; PRIMORDIUM; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN SUBUNIT; REVIEW; TRANSCRIPTION REGULATION;

ANIMALS; CAENORHABDITIS ELEGANS; CELL MOVEMENT; EXTRACELLULAR MATRIX PROTEINS; GONADS; HERMAPHRODITIC ORGANISMS; MORPHOGENESIS; TRANSCRIPTION FACTORS;

EID: 84886306412     PISSN: 17597684     EISSN: 17597692     Source Type: Journal    
DOI: 10.1002/wdev.45     Document Type: Review

References (92)

1. Kimble J, Hirsh D. The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. Dev Biol 1979, 70:396-417.
2. Kimble JE, White JG. On the control of germ cell development in Caenorhabditis elegans. Dev Biol 1981, 81:208-219.
3. Hubbard EJ, Greenstein D. The Caenorhabditis elegans gonad: a test tube for cell and developmental biology. Dev Dyn 2000, 218:2-22.
4. Hall DH, Winfrey VP, Blaeuer G, Hoffman LH, Furuta T, Rose KL, Hobert O, Greenstein D. Ultrastructural features of the adult hermaphrodite gonad of Caenorhabditis elegans: relations between the germ line and soma. Dev Biol 1999, 212:101-123.
5. Huang CC, Hall DH, Hedgecock EM, Kao G, Karantza V, Vogel BE, Hutter H, Chisholm AD, Yurchenco PD, Wadsworth WG. Laminin α subunits and their role in C. elegans development. Development 2003, 130: 3343-3358.
6. Kramer JM. Basement Membranes. The C. elegans Research Community, WormBook; 2005. doi:10.1895/ wormbook.1.16.1. Available at: http://www.worm book.org.
7. Graham PL, Johnson JJ, Wang S, Sibley MH, Gupta MC, Kramer JM. Type IV collagen is detectable in most, but not all, basement membranes of Caenorhabditis elegans and assembles on tissues that do not express it. J Cell Biol 1997, 137:1171-1183.
8. Kubota Y, Kuroki R, Nishiwaki K. A fibulin-1 homolog interacts with an ADAM protease that controls cell migration in C. elegans. Curr Biol 2004, 14: 2011-2018.
9. Lints R, Hall DH. Reproductive System, Somatic Gonad. WormAtlas. 2009, doi:10.3908/wormatlas.1.22.
10. Hedgecock EM, Culotti JG, Hall DH, Stern BD. Genetics of cell and axon migrations in Caenorhabditis elegans. Development 1987, 100:365-382.
11. Cram EJ, Shang H, Schwarzbauer JE. A systematic RNA interference screen reveals a cell migration gene network in C. elegans. J Cell Sci 2006, 119:4811-4818.
12. Nishiwaki K. Mutations affecting symmetrical migration of distal tip cells in Caenorhabditis elegans. Genetics 1999, 152:985-997.
13. Vicente-Manzanares M, Horwitz AR. Cell migration: an overview. Methods Mol Biol 2011, 769:1-24.
14. Kawano T, Zheng H, Merz DC, Kohara Y, Tamai KK, Nishiwaki K, Culotti JG. C. elegans mig-6 encodes papilin isoforms that affect distinct aspects of DTC migration, and interacts genetically with mig-17 and collagen IV. Development 2009, 136:1433-1442.
15. Nishiwaki K, Hisamoto N, Matsumoto K. A metalloprotease disintegrin that controls cell migration in Caenorhabditis elegans. Science 2000, 288:2205-2208.
16. Blelloch R, Kimble J. Control of organ shape by a secreted metalloprotease in the nematode Caenorhabditis elegans. Nature 1999, 399:586-590.
17. Meighan CM, Schwarzbauer JE. Control of C. elegans hermaphrodite gonad size and shape by vab-3/Pax6-mediated regulation of integrin receptors. Genes Dev 2007, 21:1615-1620.
18. Baum PD, Garriga G. Neuronal migrations and axon fasciculation are disrupted in ina-1 integrin mutants. Neuron 1997, 19:51-62.
19. Gettner SN, Kenyon C, Reichardt LF. Characterization of β pat-3 heterodimers, a family of essential integrin receptors in C. elegans. J Cell Biol 1995, 129:1127-1141.
20. Lee M, Cram EJ, Shen B, Schwarzbauer JE. Roles for β(pat-3) integrins in development and function of Caenorhabditis elegans muscles and gonads. J Biol Chem 2001, 276:36404-36410.
21. Porter S, Clark IM, Kevorkian L, Edwards DR. The ADAMTS metalloproteinases. Biochem J 2005, 386:15-27.
22. Kramerova IA, Kawaguchi N, Fessler LI, Nelson RE, Chen Y, Kramerov AA, Kusche-Gullberg M, Kramer JM, Ackley BD, Sieron AL, et al. Papilin in development; a pericellular protein with a homology to the ADAMTS metalloproteinases. Development 2000, 127:5475-5485.
23. Apte SS. A disintegrin-like and metalloprotease (reprolysin-type) with thrombospondin type 1 motif (ADAMTS) superfamily: functions and mechanisms. J Biol Chem 2009, 284:31493-31497.
24. Blelloch R, Anna-Arriola SS, Gao D, Li Y, Hodgkin J, Kimble J. The gon-1 gene is required for gonadal morphogenesis in Caenorhabditis elegans. Dev Biol 1999, 216:382-393.
25. Hesselson D, Newman C, Kim KW, Kimble J. GON-1 and fibulin have antagonistic roles in control of organ shape. Curr Biol 2004, 14:2005-2010.
26. Somerville RP, Longpre JM, Jungers KA, Engle JM, Ross M, Evanko S, Wight TN, Leduc R, Apte SS. Characterization of ADAMTS-9 and ADAMTS-20 as a distinct ADAMTS subfamily related to Caenorhabditis elegans GON-1. J Biol Chem 2003, 278:9503-9513.
27. Tortorella MD, Burn TC, Pratta MA, Abbaszade I, Hollis JM, Liu R, Rosenfeld SA, Copeland RA, Decicco CP, Wynn R, et al. Purification and cloning of aggrecanase-1: a member of the ADAMTS family of proteins. Science 1999, 284:1664-1666.
28. Kao G, Huang CC, Hedgecock EM, Hall DH, Wadsworth WG. The role of the laminin β subunit in laminin heterotrimer assembly and basement membrane function and development in C. elegans. Dev Biol 2006, 290:211-219.
29. Kubota Y, Ohkura K, Tamai KK, Nagata K, Nishiwaki K. MIG-17/ADAMTS controls cell migration by recruiting nidogen to the basement membrane in C. elegans. Proc Natl Acad Sci U S A 2008, 105:20804-20809.
30. Muriel JM, Dong C, Hutter H, Vogel BE. Fibulin-1C and Fibulin-1D splice variants have distinct functions and assemble in a hemicentin-dependent manner. Development 2005, 132:4223-4234.
31. Lee NV, Rodriguez-Manzaneque JC, Thai SN, Twal WO, Luque A, Lyons KM, Argraves WS, Iruela-Arispe ML. Fibulin-1 acts as a cofactor for the matrix metalloprotease ADAMTS-1. J Biol Chem 2005, 280:34796-34804.
32. Ziel JW, Sherwood DR. Roles for netrin signaling outside of axon guidance: a view from the worm. Dev Dyn 2010, 239:1296-1305.
33. Wadsworth WG. Moving around in a worm: netrin UNC-6 and circumferential axon guidance in C. elegans. Trends Neurosci 2002, 25:423-429.
34. Wadsworth WG, Bhatt H, Hedgecock EM. Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans. Neuron 1996, 16:35-46.
35. Chan SS, Zheng H, Su MW, Wilk R, Killeen MT, Hedgecock EM, Culotti JG. UNC-40, a C. elegans homolog of DCC (deleted in colorectal cancer), is required in motile cells responding to UNC-6 netrin cues. Cell 1996, 87:187-195.
36. Su M, Merz DC, Killeen MT, Zhou Y, Zheng H, Kramer JM, Hedgecock EM, Culotti JG. Regulation of the UNC-5 netrin receptor initiates the first reorientation of migrating distal tip cells in Caenorhabditis elegans. Development 2000, 127:585-594.
37. Merz DC, Zheng H, Killeen MT, Krizus A, Culotti JG. Multiple signaling mechanisms of the UNC-6/netrin receptors UNC-5 and UNC-40/DCC in vivo. Genetics 2001, 158:1071-1080.
38. Motola DL, Cummins CL, Rottiers V, Sharma KK, Li T, Li Y, Suino-Powell K, Xu HE, Auchus RJ, Antebi A, et al. Identification of ligands for DAF-12 that govern dauer formation and reproduction in C. elegans. Cell 2006, 124:1209-1223.
39. Colavita A, Culotti JG. Suppressors of ectopic UNC-5 growth cone steering identify eight genes involved in axon guidance in Caenorhabditis elegans. Dev Biol 1998, 194:72-85.
40. Colavita A, Krishna S, Zheng H, Padgett RW, Culotti JG. Pioneer axon guidance by UNC-129, a C. elegans TGF-β. Science 1998, 281:706-709.
41. Nash B, Colavita A, Zheng H, Roy PJ, Culotti JG. The forkhead transcription factor UNC-130 is required for the graded spatial expression of the UNC-129 TGF-β guidance factor in C. elegans. Genes Dev 2000, 14:2486-2500.
42. MacNeil LT, Hardy WR, Pawson T, Wrana JL, Culotti JG. UNC-129 regulates the balance between UNC-40 dependent and independent UNC-5 signaling pathways. Nat Neurosci 2009, 12:150-155.
43. Lai Wing Sun K, Correia JP, Kennedy TE. Netrins: versatile extracellular cues with diverse functions. Development 2011, 138:2153-2169.
44. Killeen M, Tong J, Krizus A, Steven R, Scott I, Pawson T, Culotti J. UNC-5 function requires phosphorylation of cytoplasmic tyrosine 482, but its UNC-40-independent functions also require a region between the ZU-5 and death domains. Dev Biol 2002, 251:348-366.
45. Lee J, Li W, Guan KL. SRC-1 mediates UNC-5 signaling in Caenorhabditis elegans. Mol Cell Biol 2005, 25:6485-6495.
46. Li W, Aurandt J, Jurgensen C, Rao Y, Guan KL. FAK and Src kinases are required for netrin-induced tyrosine phosphorylation of UNC5. J Cell Sci 2006, 119:47-55.
47. Cram EJ, Fontanez KM, Schwarzbauer JE. Functional characterization of KIN-32, the Caenorhabditis elegans homolog of focal adhesion kinase. Dev Dyn 2008, 237:837-846.
48. Lucanic M, Kiley M, Ashcroft N, L'Etoile N, Cheng HJ. The Caenorhabditis elegans P21-activated kinases are differentially required for UNC-6/netrin-mediated commissural motor axon guidance. Development 2006, 133:4549-4559.
49. Nikolopoulos SN, Giancotti FG. Netrin-integrin signaling in epithelial morphogenesis, axon guidance and vascular patterning. Cell Cycle 2005, 4:e131-e135.
50. Cram EJ, Clark SG, Schwarzbauer JE. Talin loss-of-function uncovers roles in cell contractility and migration in C. elegans. J Cell Sci 2003, 116:3871-3878.
51. Itoh B, Hirose T, Takata N, Nishiwaki K, Koga M, Ohshima Y, Okada M. SRC-1, a non-receptor type of protein tyrosine kinase, controls the direction of cell and growth cone migration in C. elegans. Development 2005, 132:5161-5172.
52. Kim C, Ye F, Ginsberg MH. Regulation of Integrin Activation. Annu Rev Cell Dev Biol 2011.
53. Anthis NJ, Campbell ID. The tail of integrin activation. Trends Biochem Sci 2011, 36:191-198.
54. Moulder GL, Huang MM, Waterston RH, Barstead RJ. Talin requires β-integrin, but not vinculin, for its assembly into focal adhesion-like structures in the nematode Caenorhabditis elegans. Mol Biol Cell 1996, 7:1181-1193.
55. Ihara S, Nishiwaki K. Prodomain-dependent tissue targeting of an ADAMTS protease controls cell migration in Caenorhabditis elegans. EMBO J 2007, 26:2607-2620.
56. Ihara S, Nishiwaki K. Stage-specific activation of MIG-17/ADAMTS controls cell migration in Caenorhabditis elegans. FEBS J 2008, 275:4296-4305.
57. Nishiwaki K, Kubota Y, Chigira Y, Roy SK, Suzuki M, Schvarzstein M, Jigami Y, Hisamoto N, Matsumoto K. An NDPase links ADAM protease glycosylation with organ morphogenesis in C. elegans. Nat Cell Biol 2004, 6:31-37.
58. Kubota Y, Sano M, Goda S, Suzuki N, Nishiwaki K. The conserved oligomeric Golgi complex acts in organ morphogenesis via glycosylation of an ADAM protease in C. elegans. Development 2006, 133:263-273.
59. Suzuki N, Toyoda H, Sano M, Nishiwaki K. Chondroitin acts in the guidance of gonadal distal tip cells in C. elegans. Dev Biol 2006, 300:635-646.
60. Kinnunen T, Huang Z, Townsend J, Gatdula MM, Brown JR, Esko JD, Turnbull JE. Heparan 2-O-sulfotransferase, hst-2, is essential for normal cell migration in Caenorhabditis elegans. Proc Natl Acad Sci U S A 2005, 102:1507-1512.
61. Merz DC, Alves G, Kawano T, Zheng H, Culotti JG. UNC-52/perlecan affects gonadal leader cell migrations in C. elegans hermaphrodites through alterations in growth factor signaling. Dev Biol 2003, 256:173-186.
62. Schwabiuk M, Coudiere L, Merz DC. SDN-1/syndecan regulates growth factor signaling in distal tip cell migrations in C. elegans. Dev Biol 2009, 334:235-242.
63. Trzebiatowska A, Topf U, Sauder U, Drabikowski K, Chiquet-Ehrismann R. 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 2008, 19:3898-3908.
64. Drabikowski K, Trzebiatowska A, Chiquet-Ehrismann R. ten-1, an essential gene for germ cell development, epidermal morphogenesis, gonad migration, and neuronal pathfinding in Caenorhabditis elegans. Dev Biol 2005, 282:27-38.
65. Johnson RP, Kang SH, Kramer JM. C. elegans dystroglycan DGN-1 functions in epithelia and neurons, but not muscle, and independently of dystrophin. Development 2006, 133:1911-1921.
66. Xu X, Ahn JH, Tam P, Yu EJ, Batra S, Cram EJ, Lee M. Analysis of conserved residues in the βpat-3 cytoplasmic tail reveals important functions of integrin in multiple tissues. Dev Dyn 2010, 239:763-772.
67. Moser M, Legate KR, Zent R, Fassler R. The tail of integrins, talin, and kindlins. Science 2009, 324:895-899.
68. Darom A, Bening-Abu-Shach U, Broday L. RNF-121 is an endoplasmic reticulum-membrane E3 ubiquitin ligase involved in the regulation of β-integrin. Mol Biol Cell 2010, 21:1788-1798.
69. Mackinnon AC, Qadota H, Norman KR, Moerman DG, Williams BD. C. elegans PAT-4/ILK functions as an adaptor protein within integrin adhesion complexes. Curr Biol 2002, 12:787-797.
70. Rogalski TM, Mullen GP, Gilbert MM, Williams BD, Moerman DG. The UNC-112 gene in Caenorhabditis elegans encodes a novel component of cell-matrix adhesion structures required for integrin localization in the muscle cell membrane. J Cell Biol 2000, 150:253-264.
71. Lin X, Qadota H, Moerman DG, Williams BD. C. elegans PAT-6/actopaxin plays a critical role in the assembly of integrin adhesion complexes in vivo. Curr Biol 2003, 13:922-932.
72. Xu X, Rongali SC, Miles JP, Lee KD, Lee M. pat-4/ILK and unc-112/Mig-2 are required for gonad function in Caenorhabditis elegans. Exp Cell Res 2006, 312:1475-1483.
73. Lundquist EA. Small GTPases. The C. elegans Research Community, WormBook; 2006. doi:10.1895/ wormbook.1.67.1. Available at: http://www.worm book.org.
74. Reddien PW, Horvitz HR. CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat Cell Biol 2000, 2:131-136.
75. Lundquist EA, Reddien PW, Hartwieg E, Horvitz HR, Bargmann CI. Three C. elegans Rac proteins and several alternative Rac regulators control axon guidance, cell migration and apoptotic cell phagocytosis. Development 2001, 128:4475-4488.
76. Gumienny TL, Brugnera E, Tosello-Trampont AC, Kinchen JM, Haney LB, Nishiwaki K, Walk SF, Nemergut ME, Macara IG, Francis R, et al. CED-12/ELMO, a novel member of the CrkII/Dock180/Rac pathway, is required for phagocytosis and cell migration. Cell 2001, 107:27-41.
77. Wu YC, Horvitz HR. C. elegans phagocytosis and cell-migration protein CED-5 is similar to human DOCK180. Nature 1998, 392:501-504.
78. Wu YC, Tsai MC, Cheng LC, Chou CJ, Weng NY. C. elegans CED-12 acts in the conserved crkII/DOCK180/Rac pathway to control cell migration and cell corpse engulfment. Dev Cell 2001, 1:491-502.
79. Zhou Z, Caron E, Hartwieg E, Hall A, Horvitz HR. The C. elegans PH domain protein CED-12 regulates cytoskeletal reorganization via a Rho/Rac GTPase signaling pathway. Dev Cell 2001, 1:477-489.
80. Reddien PW, Horvitz HR. The engulfment process of programmed cell death in caenorhabditis elegans. Annu Rev Cell Dev Biol 2004, 20:193-221.
81. Lee M, Shen B, Schwarzbauer JE, Ahn J, Kwon J. Connections between integrins and Rac GTPase pathways control gonad formation and function in C. elegans. Biochim Biophys Acta 2005, 1723:248-255.
82. Hoefen RJ, Berk BC. The multifunctional GIT family of proteins. J Cell Sci 2006, 119:1469-1475.
83. Frank SR, Hansen SH. The PIX-GIT complex: a G protein signaling cassette in control of cell shape. Semin Cell Dev Biol 2008, 19:234-244.
84. Ong CC, Jubb AM, Zhou W, Haverty PM, Harris AL, Belvin M, Friedman LS, Koeppen H, Hoeflich KP. p21-activated kinase 1: PAK'ed with potential. Oncotarget 2011, 2:491-496.
85. Lucanic M, Cheng HJ. A RAC/CDC-42-independent GIT/PIX/PAK signaling pathway mediates cell migration in C. elegans. PLoS Genet 2008, 4:e1000269.
86. Hurwitz ME, Vanderzalm PJ, Bloom L, Goldman J, Garriga G, Horvitz HR. Abl kinase inhibits the engulfment of apoptotic [corrected] cells in Caenorhabditis elegans. PLoS Biol 2009, 7:e99.
87. Tannoury H, Rodriguez V, Kovacevic I, Ibourk M, Lee M, Cram EJ. CACN-1/Cactin interacts genetically with MIG-2 GTPase signaling to control distal tip cell migration in C. elegans. Dev Biol 2010, 341:176-185.
88. Kim HS, Murakami R, Quintin S, Mori M, Ohkura K, Tamai KK, Labouesse M, Sakamoto H, Nishiwaki K. VAB-10 spectraplakin acts in cell and nuclear migration in Caenorhabditis elegans. Development 2011, 138:4013-4023.
89. Cabello J, Neukomm LJ, Gunesdogan U, Burkart K, Charette SJ, Lochnit G, Hengartner MO, Schnabel R. The Wnt pathway controls cell death engulfment, spindle orientation, and migration through CED-10/Rac. PLoS Biol 2010, 8:e1000297.
90. Ridley AJ. Life at the leading edge. Cell 2011, 145: 1012-1022.
91. WormAtlas. Altun ZF, Hall DH, eds. 2002-2006. Available at: http://www.wormatlas.org.
92. WormBook, the Online Review of C. elegans Biology. Chalfie M. ed. ISSN:1551-8507. Available at: http://www.wormbook.org.