The C. elegans peroxidasin PXN-2 is essential for embryonic morphogenesis and inhibits adult axon regeneration

Development

Volumn 137, Issue 21, 2010, Pages 3603-3613

  Gotenstein, Jennifer R ^a   Swale, Ryann E ^b   Fukuda, Tetsuko ^a   Wu, Zilu ^c   Giurumescu, Claudiu A ^a   Goncharov, Alexandr ^c   Jin, Yishi ^c   Chisholm, Andrew D ^a,b,c  

^a SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Axon guidance; Caenorhabditis elegans; Epidermis; Extracellular matrix; Genetic suppression; Laser axotomy; Leucine rich repeat

Indexed keywords

PEROXIDASE;

ARTICLE; BASEMENT MEMBRANE; CAENORHABDITIS ELEGANS; CATALYSIS; CELL FUNCTION; EMBRYO DEVELOPMENT; EXTRACELLULAR MATRIX; LOSS OF FUNCTION MUTATION; MORPHOGENESIS; MUTANT; NERVE FIBER; NERVE FIBER REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; ULTRASTRUCTURE;

AGING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL ADHESION; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; EPIDERMIS; EXTRACELLULAR MATRIX PROTEINS; MORPHOGENESIS; MUSCLES; NERVE REGENERATION; PEROXIDASE; PEROXIREDOXINS; PHYLOGENY;

CAENORHABDITIS ELEGANS;

EID: 78049341349     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.049189     Document Type: Article

References (63)

1. Alfonso, T. B. and Jones, B. W. (2002). gcm2 promotes glial cell differentiation and is required with glial cells missing for macrophage development in Drosophila. Dev. Biol. 248, 369-383.
2. Andersen, S. O. (1964). The cross-links in resilin identified as dityrosine and trityrosine. Biochim. Biophys. Acta 93, 213-215.
3. Aratani, Y., Koyama, H., Nyui, S., Suzuki, K., Kura, F. and Maeda, N. (1999). Severe impairment in early host defense against Candida albicans in mice deficient in myeloperoxidase. Infect. Immunol. 67, 1828-1836.
4. Benard, C. Y., Boyanov, A., Hall, D. H. and Hobert, O. (2006). DIG-1, a novel giant protein, non-autonomously mediates maintenance of nervous system architecture. Development 133, 3329-3340.
5. Busch, S. A. and Silver, J. (2007). The role of extracellular matrix in CNS regeneration. Curr. Opin. Neurobiol. 17, 120-127.
6. Chavez, V., Mohri-Shiomi, A. and Garsin, D. A. (2009). Ce-Duox1/BLI-3 generates reactive oxygen species as a protective innate immune mechanism in Caenorhabditis elegans. Infect. Immunol. 77, 4983-4989.
7. Cheng, G., Salerno, J. C., Cao, Z., Pagano, P. J. and Lambeth, J. D. (2008). Identification and characterization of VPO1, a new animal heme-containing peroxidase. Free Radic. Biol. Med. 45, 1682-1694.
8. Chisholm, A. D. and Hardin, J. (2005). Epidermal morphogenesis. WormBook, http://www.wormbook.org.
9. Clark, S. G. and Chiu, C. (2003). C. elegans ZAG-1, a Zn-finger-homeodomain protein, regulates axonal development and neuronal differentiation. Development 130, 3781-3794.
10. Daiyasu, H. and Toh, H. (2000). Molecular evolution of the myeloperoxidase family. J. Mol. Evol. 51, 433-445.
11. Dixon, S. J., Alexander, M., Fernandes, R., Ricker, N. and Roy, P. J. (2006). FGF negatively regulates muscle membrane extension in Caenorhabditis elegans. Development 133, 1263-1275.
12. Edens, W. A., Sharling, L., Cheng, G., Shapira, R., Kinkade, J. M., Lee, T., Edens, H. A., Tang, X., Sullards, C., Flaherty, D. B. et al. (2001). Tyrosine cross-linking of extracellular matrix is catalyzed by Duox, a multidomain oxidase/peroxidase with homology to the phagocyte oxidase subunit gp91phox. J. Cell Biol. 154, 879-891.
13. Furtmuller, P. G., Zederbauer, M., Jantschko, W., Helm, J., Bogner, M., Jakopitsch, C. and Obinger, C. (2006). Active site structure and catalytic mechanisms of human peroxidases. Arch. Biochem. Biophys. 445, 199-213.
14. George, S. E., Simokat, K., Hardin, J. and Chisholm, A. D. (1998). The VAB-1 Eph receptor tyrosine kinase functions in neural and epithelial morphogenesis in C. elegans. Cell 92, 633-643.
15. Gupta, M. C., Graham, P. L. and Kramer, J. M. (1997). Characterization of alpha1(IV) collagen mutations in Caenorhabditis elegans and the effects of alpha1 and alpha2(IV) mutations on type IV collagen distribution. J. Cell Biol. 137, 1185-1196.
16. Hansson, M., Olsson, I. and Nauseef, W. M. (2006). Biosynthesis, processing, and sorting of human myeloperoxidase. Arch. Biochem. Biophys. 445, 214-224.
17. Hart, A. C. (2006). Behavior. WormBook, http://www.wormbook.org.
18. Heinecke, J. W., Li, W., Daehnke, H. L., 3rd and Goldstein, J. A. (1993). Dityrosine, a specific marker of oxidation, is synthesized by the myeloperoxidase-hydrogen peroxide system of human neutrophils and macrophages. J. Biol. Chem. 268, 4069-4077.
19. Hesselson, D., Newman, C., Kim, K. W. and Kimble, J. (2004). GON-1 and fibulin have antagonistic roles in control of organ shape. Curr. Biol. 14, 2005-2010.
20. Hobert, O. (2002). PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32, 728-730.
21. Hobert, O., Mori, I., Yamashita, Y., Honda, H., Ohshima, Y., Liu, Y. and Ruvkun, G. (1997). Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene. Neuron 19, 345-357.
22. Homma, S., Shimada, T., Hikake, T. and Yaginuma, H. (2009). Expression pattern of LRR and Ig domain-containing protein (LRRIG protein) in the early mouse embryo. Gene Expr. Patterns 9, 1-26.
23. Hong, L., Elbl, T., Ward, J., Franzini-Armstrong, C., Rybicka, K. K., Gatewood, B. K., Baillie, D. L. and Bucher, E. A. (2001). MUP-4 is a novel transmembrane protein with functions in epithelial cell adhesion in Caenorhabditis elegans. J. Cell Biol. 154, 403-414.
24. Horikoshi, N., Cong, J., Kley, N. and Shenk, T. (1999). Isolation of differentially expressed cDNAs from p53-dependent apoptotic cells: activation of the human homologue of the Drosophila peroxidasin gene. Biochem. Biophys. Res. Commun. 261, 864-869. (Pubitemid 29408149)
25. Huang, C. C., Hall, D. H., Hedgecock, E. M., Kao, G., Karantza, V., Vogel, B. E., Hutter, H., Chisholm, A. D., Yurchenco, P. D. and Wadsworth, W. G. (2003). Laminin alpha subunits and their role in C. elegans development. Development 130, 3343-3358.
26. Huang, X., Cheng, H. J., Tessier-Lavigne, M. and Jin, Y. (2002). MAX-1, a novel PH/MyTH4/FERM domain cytoplasmic protein implicated in netrin-mediated axon repulsion. Neuron 34, 563-576.
27. Hudson, M. L., Kinnunen, T., Cinar, H. N. and Chisholm, A. D. (2006). C. elegans Kallmann syndrome protein KAL-1 interacts with syndecan and glypican to regulate neuronal cell migrations. Dev. Biol. 294, 352-365.
28. Ihalin, R., Loimaranta, V. and Tenovuo, J. (2006). Origin, structure, and biological activities of peroxidases in human saliva. Arch. Biochem. Biophys. 445, 261-268.
29. Jacquet, A., Garcia-Quintana, L., Deleersnyder, V., Fenna, R., Bollen, A. and Moguilevsky, N. (1994). Site-directed mutagenesis of human myeloperoxidase: further identification of residues involved in catalytic activity and heme interaction. Biochem. Biophys. Res. Commun. 202, 73-81.
30. Johansson, M. W., Lind, M. I., Holmblad, T., Thornqvist, P. O. and Soderhall, K. (1995). Peroxinectin, a novel cell adhesion protein from crayfish blood. Biochem. Biophys. Res. Commun. 216, 1079-1087.
31. Johansson, M. W., Patarroyo, M., Oberg, F., Siegbahn, A. and Nilsson, K. (1997). Myeloperoxidase mediates cell adhesion via the alpha M beta 2 integrin (Mac-1, CD11b/CD18). J. Cell Sci. 110, 1133-1139.
32. Kamath, R. S., Fraser, A. G., Dong, Y., Poulin, G., Durbin, R., Gotta, M., Kanapin, A., Le Bot, N., Moreno, S., Sohrmann, M. et al. (2003). Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231-237.
33. Konstandi, O. A., Papassideri, I. S., Stravopodis, D. J., Kenoutis, C. A., Hasan, Z., Katsorchis, T., Wever, R. and Margaritis, L. H. (2005). The enzymatic component of Drosophila melanogaster chorion is the Pxd peroxidase. Insect Biochem. Mol. Biol. 35, 1043-1057.
34. Kraemer, B. C., Burgess, J. K., Chen, J. H., Thomas, J. H. and Schellenberg, G. D. (2006). Molecular pathways that influence human tau-induced pathology in Caenorhabditis elegans. Hum. Mol. Genet. 15, 1483-1496.
35. Kramer, J. M. (2005). Basement membranes. WormBook, http://www.wormbook. org.
36. Kubota, Y., Kuroki, R. and Nishiwaki, K. (2004). A fibulin-1 homolog interacts with an ADAM protease that controls cell migration in C. elegans. Curr. Biol. 14, 2011-2018.
37. Lehrer, R. I. and Cline, M. J. (1969). Leukocyte myeloperoxidase deficiency and disseminated candidiasis: the role of myeloperoxidase in resistance to Candida infection. J. Clin. Invest. 48, 1478-1488.
38. Lynch, M. and Force, A. (2000). The probability of duplicate gene preservation by subfunctionalization. Genetics 154, 459-473.
39. Mitchell, M. S., Kan-Mitchell, J., Minev, B., Edman, C. and Deans, R. J. (2000). A novel melanoma gene (MG50) encoding the interleukin 1 receptor antagonist and six epitopes recognized by human cytolytic T lymphocytes. Cancer Res. 60, 6448-6456.
40. Muriel, J. M., Dong, C., Hutter, H. and Vogel, B. E. (2005). Fibulin-1C and Fibulin-1D splice variants have distinct functions and assemble in a hemicentin-dependent manner. Development 132, 4223-4234.
41. Myllyharju, J. and Kivirikko, K. I. (2004). Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 20, 33-43.
42. Nelson, R. E., Fessler, L. I., Takagi, Y., Blumberg, B., Keene, D. R., Olson, P. F., Parker, C. G. and Fessler, J. H. (1994). Peroxidasin: a novel enzyme-matrix protein of Drosophila development. EMBO J. 13, 3438-3447.
43. O'Brien, P. J. (2000). Peroxidases. Chem. Biol. Interact. 129, 113-139.
44. Olofsson, B. and Page, D. T. (2005). Condensation of the central nervous system in embryonic Drosophila is inhibited by blocking hemocyte migration or neural activity. Dev. Biol. 279, 233-243.
45. Priess, J. R. and Hirsh, D. I. (1986). Caenorhabditis elegans morphogenesis: the role of the cytoskeleton in elongation of the embryo. Dev. Biol. 117, 156-173.
46. Rees, M. D., Kennett, E. C., Whitelock, J. M. and Davies, M. J. (2008). Oxidative damage to extracellular matrix and its role in human pathologies. Free Radic. Biol. Med. 44, 1973-2001.
47. Robins, S. P. (2007). Biochemistry and functional significance of collagen crosslinking. Biochem. Soc. Trans. 35, 849-852.
48. Ruf, J. and Carayon, P. (2006). Structural and functional aspects of thyroid peroxidase. Arch. Biochem. Biophys. 445, 269-277.
49. Schafer, W. F. (2006). Genetics of egg-laying in worms. Annu. Rev. Genet. 40, 487-509.
50. Stofanko, M., Kwon, S. Y. and Badenhorst, P. (2008). A misexpression screen to identify regulators of Drosophila larval hemocyte development. Genetics 180, 253-267.
51. Thein, M. C., Winter, A. D., Stepek, G., McCormack, G., Stapleton, G., Johnstone, I. L. and Page, A. P. (2009). Combined extracellular matrix crosslinking activity of the peroxidase MLT-7 and the dual oxidase BLI-3 is critical for post-embryonic viability in Caenorhabditis elegans. J. Biol. Chem. 284, 17549-17563.
52. Tindall, A. J., Pownall, M. E., Morris, I. D. and Isaacs, H. V. (2005). Xenopus tropicalis peroxidasin gene is expressed within the developing neural tube and pronephric kidney. Dev. Dyn. 232, 377-384.
53. Tvrdik, P. and Capecchi, M. R. (2006). Reversal of Hox1 gene subfunctionalization in the mouse. Dev. Cell 11, 239-250.
54. Vogel, B. E. and Hedgecock, E. M. (2001). Hemicentin, a conserved extracellular member of the immunoglobulin superfamily, organizes epithelial and other cell attachments into oriented line-shaped junctions. Development 128, 883-894.
55. Wang, J. and Slungaard, A. (2006). Role of eosinophil peroxidase in host defense and disease pathology. Arch. Biochem. Biophys. 445, 256-260.
56. Wang, Y., Rosen, H., Madtes, D. K., Shao, B., Martin, T. R., Heinecke, J. W. and Fu, X. (2007). Myeloperoxidase inactivates TIMP-1 by oxidizing its N-terminal cysteine residue: an oxidative mechanism for regulating proteolysis during inflammation. J. Biol. Chem. 282, 31826-31834.
57. Weimer, R. M. (2006). Preservation of C. elegans tissue via high-pressure freezing and freeze-substitution for ultrastructural analysis and immunocytochemistry. Methods Mol. Biol. 351, 203-221.
58. Wicks, S. R., Yeh, R. T., Gish, W. R., Waterston, R. H. and Plasterk, R. H. (2001). Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat. Genet. 28, 160-164.
59. Williams, B. D. and Waterston, R. H. (1994). Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J. Cell Biol. 124, 475-490.
60. Wong, J. L. and Wessel, G. M. (2008). Free-radical crosslinking of specific proteins alters the function of the egg extracellular matrix at fertilization. Development 135, 431-440.
61. Woo, W. M., Berry, E. C., Hudson, M. L., Swale, R. E., Goncharov, A. and Chisholm, A. D. (2008). The C. elegans F-spondin family protein SPON-1 maintains cell adhesion in neural and non-neural tissues. Development 135, 2747-2756.
62. Wu, Z., Ghosh-Roy, A., Yanik, M. F., Zhang, J. Z., Jin, Y. and Chisholm, A. D. (2007). Caenorhabditis elegans neuronal regeneration is influenced by life stage, ephrin signaling, and synaptic branching. Proc. Natl. Acad. Sci. USA 104, 15132-15137.
63. Zamocky, M., Jakopitsch, C., Furtmuller, P. G., Dunand, C. and Obinger, C. (2008). The peroxidase-cyclooxygenase superfamily: reconstructed evolution of critical enzymes of the innate immune system. Proteins 72, 589-605.