Heparanase 2, Mutated in urofacial syndrome, Mediates peripheral neural development in Xenopus

Human Molecular Genetics

Volumn 23, Issue 16, 2014, Pages 4302-4314

  Roberts, Neil A ^a   Woolf, Adrian S ^a   Stuart, Helen M ^a   Thuret, Raphaël ^b   McKenzie, Edward A ^b   Newman, William G ^a   Hilton, Emma N ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; HEPARANASE; HEPARANASE 1; HEPARANASE 2; MITOGEN ACTIVATED PROTEIN KINASE; MORPHOLINO OLIGONUCLEOTIDE; UNCLASSIFIED DRUG; BETA GLUCURONIDASE; PERK KINASE; PROTEIN KINASE R;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; BIOAVAILABILITY; BLADDER DISEASE; CHEMICAL ANALYSIS; CLINICAL FEATURE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FACIAL EXPRESSION; GENE MUTATION; IN VIVO STUDY; MORPHOLOGY; MOTONEURON; MUSCLE WEAKNESS; NERVE CELL DIFFERENTIATION; NEURAL TUBE; NONHUMAN; PARALYSIS; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; SKELETAL MUSCLE; UPREGULATION; UROFACIAL SYNDROME; XENOPUS TROPICALIS; ANIMAL; EMBRYOLOGY; FACIES; GENE SILENCING; GENETICS; METABOLISM; MUTATION; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; URINARY TRACT DISEASE; XENOPUS; ANIMAL TISSUE; GENETIC TRANSCRIPTION; PERIPHERAL NERVE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SEQUENCE ALIGNMENT;

ANIMALS; EIF-2 KINASE; FACIES; FIBROBLAST GROWTH FACTOR 2; GENE KNOCKDOWN TECHNIQUES; GLUCURONIDASE; MOTOR NEURONS; MUSCLE, SKELETAL; MUTATION; NEURAL TUBE; NEUROGENESIS; UROLOGIC DISEASES; XENOPUS;

EID: 84904750832     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu147     Document Type: Article

References (53)

1. Elejalde, B.R. (1979) Genetic and diagnostic considerations in three families with abnormalities of facial expression and congenital urinary obstruction: 'the Ochoa syndrome'. Am. J. Med. Genet., 3, 97-108.
2. Ochoa, B. (2004) Can a congenital dysfunctional bladder be diagnosed from a smile? Pediatr. Nephrol., 19, 6-12.
3. Ganesan, I. and Thomas, T. (2011) More than meets the smile: facial muscle expression in children with Ochoa syndrome. Med. J. Malaysia, 66, 507-509.
4. Newman, W.G., Woolf, A.S. and Stuart, H.M. (2013) Urofacial syndrome. In Pagon, R.A. (ed.), GeneReviewsTM. University of Washington, Seattle, pp. 1993-2013.
5. Mermerkaya, M., Süer, E., Oztürk, E.,Gülpinar, O.,Gökçe, M.I., Yalçindag̊ , F.N., Soygü r, T. and Burgu, B. (2013) Nocturnal lagophthalmos in children with urofacial syndrome (Ochoa): a novel sign. Eur. J. Pediatr. DOI: 10.1007/s00431-013-2172-7.
6. Garcia-Minaur, S., Oliver, F., Yanez, J.M., Soriano, J.R., Quinn, F. and Reardon, W. (2001) Three new European cases of urofacial (Ochoa) syndrome. Clin. Dysmorphol., 10, 165-170.
7. Daly, S.B., Urquhart, J.E., Hilton, E., McKenzie, E.A., Kammerer, R.A., Lewis, M., Kerr, B., Stuart, H., Donnai, D., Long, D.A. et al. (2010) Mutations in HPSE2 cause urofacial syndrome. Am. J. Hum. Genet., 11, 963-969.
8. Pang, J., Zhang, S., Yang, P., Hawkins-Lee, B., Zhong, J., Zhang, Y., Ochoa, B., Agundez, J.A.G., Voelckel, M.A., Gu, W. et al. (2010) Loss-of-function mutations in HPSE2 cause the autosomal recessive urofacial syndrome. Am. J. Hum. Genet., 11, 957-962.
9. Al Badr, W., Al Bader, S., Otto, E., Hildebrandt, F., Ackley, T., Peng, W., Xu, J., Li, J., Owens, K.M., Bloom, D. et al. (2011)Exomecapture and massively parallel sequencing identifies a novel HPSE2 mutation in a Saudi Arabian child with Ochoa (urofacial) syndrome. J. Pediatr. Urol., 7, 569-573.
10. Mahmood, S., Beetz, C., Tahir, M.M., Imran, M., Mumtaz, R., Bassmann, I., Jahic, A., Malik, M., Nürnberg, G., Hassan, S.A. et al. (2012) First HPSE2 missense mutation in urofacial syndrome. Clin. Genet., 81, 88-92.
11. McKenzie, E., Tyson, K., Stamps, A., Smith, P., Turner, P., Barry, R., Hircock, M., Patel, S., Barry, E., Stubberfield, C. et al. (2000) Cloning and expression profiling of Hpa2, a novel mammalian heparanase family member. Biochem. Biophys. Res. Commun., 276, 1170-1177.
12. Levy-Adam, F., Ilan, N. and Vlodavsky, I. (2010) Tumorigenic and adhesive properties of heparanase. Semin. Cancer Biol., 20, 153-160.
13. Arvatz, G., Shafat, I., Levy-Adam, F., Ilan, N. and Vlodavsky, I. (2011) The heparanase system and tumor metastasis: is heparanase the seed and soil? Cancer Metastasis Rev., 30, 253-268.
14. Vlodavsky, I., Fuks, Z., Ishai-Michaeli, R., Bashkin, P., Levi, E., Korner, G., Bar-Shavit, R. and Klagsbrun, M. (1991) Extracellular matrix-resident basic fibroblast growth factor: implication for the control of angiogenesis. J. Cell. Biochem., 45, 167-176.
15. Myler, H.A. and West, J.L. (2002) Heparanase and platelet factor-4 induce smooth muscle cell proliferation and migration via bFGF release from the ECM. J. Biochem., 131, 913-922.
16. Reiland, J., Kempf, D., Roy, M., Denkins, Y. and Marchetti,D. (2006) FGF2 binding, signaling, and angiogenesis are modulated by heparanase in metastatic melanoma cells. Neoplasia, 8, 596-606.
17. Levy-Adam, F., Feld, S., Cohen-Kaplan, V., Steingaus, A., Gross, M., Arvatz, G., Naroditsy, I., Ilan, N., Doweck, I. and Vlodavsky, I. (2010) Heparanase 2 interacts with heparan sulfate with high affinity and inhibits heparanase activity. J. Biol. Chem., 285, 280-289.
18. Stuart, H.M., Roberts, N.A., Bergu, B., Daly, S.B., Urquhart, J.E., Bhaskar, S., Dickerson, J., Mermerkaya, M., Silay, M.S., Lewis, M.A. et al. (2013) LRIG2 mutations cause urofacial syndrome. Am. J. Hum. Genet., 92, 259-264.
19. Guo, D., Holmlund, C., Henriksson, R. and Hedman, H. (2004) The LRIG gene family has three vertebrate paralogs widely expressed in human and mouse tissues and a homolog in Ascidiacea. Genomics, 84, 157-165.
20. Wong, V.W., Stange, D.E., Page, M.E., Buczacki, S., Wabik, A., Itami, S., van de Wetering, M., Poulsom, R., Wright, N.A., Trotter, M.W. et al. (2012) Lrig1 controls intestinal stem-cell homeostasis by negative regulation of ErbB signalling. Nat. Cell Biol., 14, 401-408.
21. Rafidi, H., Mercado, F. 3rd, Astudillo, M., Fry, W.H., Saldana, M., Carraway, K.L. 3rd and Sweeney, C. (2013) Leucine-rich repeat and immunoglobulin domain-containing protein-1 (Lrig1) negative regulatory action toward ErbB receptor tyrosine kinases is opposed by leucine-rich repeat and immunoglobulin domain-containing protein 3 (Lrig3). J. Biol. Chem., 288, 21593-21605.
22. Wang, B., Han, L., Chen, R., Cai, M., Han, F., Lei, T. and Guo, D. (2009) Downregulation of LRIG2 expression by RNA interference inhibits glioblastoma cell (GL15) growth, causes cell cycle redistribution, increases cell apoptosis and enhances cell adhesion and invasion in vitro. Cancer Biol. Ther., 8, 1018-1023.
23. Woolf, A.S., Stuart, H.M., Roberts, N.A., McKenzie, E.A., Hilton, E.N. and Newman, W.G.(2014) Urofacial syndrome: a genetic and congenital disease of aberrant urinary bladder innervation. Pediatr. Nephrol., 29, 513-518.
24. Gandhi, N.S., Freeman, C., Parish, C.R. and Mancera, R.L. (2012) Computational analyses of the catalytic and heparin-binding sites and their interactions with glycosaminoglycans in glycoside hydrolase family 79 endo-b-D-glucuronidase (heparanase). Glycobiology, 22, 35-55.
25. van Mier, P., Armstrong, J. and Roberts, A. (1989) Development of early swimming in Xenopus laevis embryos: myotomal musculature, its innervation and activation. Neuroscience, 32, 113-126.
26. van Mier, P. and ten Donkelaar, H.J. (1989) Structural and functional properties of reticulospinal neurons in the early-swimming stage Xenopus embryo. J. Neurosci., 9, 25-37.
27. Huang, J.K., Dorey, K., Ishibashi, S. and Amaya, E. (2007) BDNF promotes target innervation of Xenopus mandibular trigeminal axons in vivo. BMC Dev. Biol., 7, 59.
28. Dali, L., Gustin, J., Perry, K. and Domingo, C.R. (2002) Signals that instruct somite and myotome formation persist in Xenopus laevis early tailbud stage embryos. Cells Tissues Organs, 172, 1-12.
29. McCoy, K.E., Zhou, X. and Vize, P.D. (2008) Collectrin/tmem27 is expressed at high levels in all segments of the developing Xenopus pronephric nephron and in the Wolffian duct. Gene Expr. Patterns, 8, 271-274.
30. Tseng, H.T., Shah, R. and Jamrich, M. (2004) Function and regulation of FoxF1 during Xenopus gut development. Development, 131, 3637-3647.
31. Zhou, Q. and Anderson, D.J. (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell, 109, 61-73.
32. Bronchain, O.J., Pollet, N., Ymlahi-Ouazzani, Q., Dhorne-Pollet, S., Helbling, J.C., Lecarpentier, J.E., Percheron, K. and Wegnez, M. (2007) The olig family: phylogenetic analysis and early gene expression in Xenopus tropicalis. Dev. Genes Evol., 217, 485-497.
33. Ribes, V. and Briscoe, J. (2009) Establishing and interpreting graded Sonic Hedgehog signaling during vertebrate neural tube patterning: the role of negative feedback. Cold Spring Harb. Perspect. Biol., 1, a002014.
34. Dichmann, D.S. and Harland, R.M. (2011) Nkx6 genes pattern the frog neural plate and Nkx6.1 is necessary for motoneuron axon projection. Dev. Biol., 349, 378-386.
35. Rudnicki, M.A., Le Grand, F., McKinnell, I. and Kuang, S. (2008) The molecular regulation of muscle stem cell function. Cold Spring Harb. Symp. Quant. Biol., 73, 323-331.
36. Havis, E., Coumailleau, P., Bonnet, A., Bismuth, K., Bonnin, M.A., Johnson, R., Fan, C.M., Relaix, F., Shi, D.L. and Duprez, D. (2012) Sim2 prevents entry into the myogenic program by repressing MyoD transcription during limb embryonic myogenesis. Development, 139, 1910-1920.
37. Takeda, Y., Koh, S.D., Sanders, K.M. and Ward, S.M. (2008) Differential expression of ionic conductances in interstitial cells of Cajal in the murine gastric antrum. J. Physiol., 586, 859-873.
38. Lu, B., Czernik, A.J., Popov, S., Wang, T., Poo, M.M. and Greengard, P. (1996) Expression of synapsin I correlates with maturation of the neuromuscular synapse. Neuroscience, 74, 1087-1097.
39. Baldwin, T.J., Yoshihara, C.M., Blackmer, K., Kintner, C.R. and Burden, S.J. (1988) Regulation of acetylcholine receptor transcript expression during development in Xenopus laevis. J. Cell Biol., 106, 469-478.
40. Li, P.P., Chen, C., Lee, C.W., Madhavan, R. and Peng, H.B. (2011) Axonal filopodial asymmetry induced by synaptic target. Mol. Biol. Cell, 22, 2480-2490.
41. Li, P.P., Zhou, J.J., Meng, M., Madhavan, R. and Peng, H.B. (2012) Reciprocal regulation of axonal filopodia and outgrowth during neuromuscular junction development. PLoS ONE, 7, e44759.
42. Bertolesi, G.E., Su, H.Y., Michaiel, G., Dueck, S.M., Hehr, C.L. and McFarlane, S. (2011) Two promoters with distinct activities in different tissues drive the expression of heparanase in Xenopus. Dev. Dyn., 240, 2657-2672.
43. Bertolesi, G.E., Michaiel, G. and McFarlane, S. (2008) Two heparanase splicing variants with distinct properties are necessary in early Xenopus development. J. Biol. Chem., 283, 16004-16016.
44. Bilican, B., Fiore-Heriche, C., Compston, A., Allen, N.D. and Chandran, S. (2008) Induction of Olig2 precursors by FGF involves BMP signalling blockade at the Smad level. PLoS ONE, 3, e2863.
45. Del Rio, T., Nishitani, A.M., Yu, W.M. and Goodrich, L.V. (2013) In vivo analysis of Lrig genes reveals redundant and independent functions in the inner ear. PLoS Genet., 9, e1003824.
46. Rondahl, V., Holmlund, C., Karlsson, T., Wang, B., Faraz, M., Henriksson, R. and Hedman, H. (2013) Lrig2-deficient mice are protected against PDGFB-Induced glioma. PLoS ONE, 8, e73635.
47. Hufton, A.L., Vinayagam, A., Suhai, S. and Baker, J.C. (2006) Genomic analysis of Xenopus organizer function. BMC Dev. Biol., 6, 27.
48. Fowler, C.J., Griffiths, D. and de Groat, W.C. (2008) The neural control of micturition. Nat. Rev. Neurosci., 9, 453-466.
49. Weber, S., Thiele, H., Mir, S., Toliat, M.R., Sozeri, B., Reutter, H., Draaken, M., Ludwig, M., Altmü ller, J., Frommolt, P. et al. (2011) Muscarinic acetylcholine receptor M3 mutation causes urinary bladder disease and a prune -belly-like syndrome. Am. J. Hum. Genet, 89, 668-674.
50. Cruz, C.D., McMahon, S.B. and Cruz, F. (2006) Spinal ERK activation contributes to the regulation of bladder function in spinal cord injured rats. Exp. Neurol., 200, 66-73.
51. Jones, E.A. (2005) Xenopus: a prince among models for kidney development. J. Am. Soc. Nephrol., 16, 313-321.
52. Hilton, E.N., Manson, F.D., Urquhart, J.E., Johnston, J.J., Slavotinek, A.M., Hedera, P., Stattin, E.L., Nordgren, A., Biesecker, L.G. and Black, G.C. (2007) Left-sided embryonic expression of the BCL-6 corepressor, BCOR, is required for vertebrate laterality determination. Hum. Mol. Genet., 16, 1773-1782.
53. Nieuwkoop, P.D. and Faber, J. (1967) Normal Table of Xenopus laevis (Daudin). 2nd edn. North Holland Publishing Company, Amsterdam.