Nrk2b-mediated NAD+ production regulates cell adhesion and is required for muscle morphogenesis in vivo. Nrk2b and NAD+ in muscle morphogenesis

Developmental Biology

Volumn 344, Issue 2, 2010, Pages 809-826

  Goody, Michelle F ^a   Kelly, Meghan W ^a   Lessard, Kevin N ^a   Khalil, Andre ^a,b   Henry, Clarissa A ^a,b  

^a UNIVERSITY OF MAINE   (United States)

^b JACKSON LABORATORY   (United States)

Author keywords

Cell matrix adhesion; Laminin; Nicotinamide adenine dinucleotide; Nicotinamide riboside kinase; Paxillin; Skeletal muscle

Indexed keywords

BETA DYSTROGLYCAN; FOCAL ADHESION KINASE; LAMININ; MORPHOLINE DERIVATIVE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE RIBOSIDE; NICOTINAMIDE RIBOSIDE KINASE 2B; PAXILLIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; ENZYME PHOSPHORYLATION; GENE FUNCTION; GENE LOCUS; GENE OVEREXPRESSION; GENE TARGETING; HUMAN; IN VIVO STUDY; MUSCLE CELL; MUSCLE DEVELOPMENT; MYOTOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; ZEBRA FISH;

DANIO RERIO;

EID: 77955276934     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.05.513     Document Type: Article

References (75)

1. Albertson R.C., Yelick P.C. Fgf8 haploinsufficiency results in distinct craniofacial defects in adult zebrafish. Dev. Biol. 2007, 306:505-515.
2. Arnedo A. A wavelet-based method for multifractal image analysis. I. Methodology and test applications on isotropic and anisotropic random rough surfaces. Eur. J. Phys. B 2000, 15:567-600.
3. Bassett, D.I., Currie, P.D., 2003. The zebrafish as a model for muscular dystrophy and congenital myopathy. Hum. Mol. Genet. 12 Spec No 2, R265-R270.
4. Bassett D.I., Bryson-Richardson R.J., Daggett D.F., Gautier P., Keenan D.G., Currie P.D. Dystrophin is required for the formation of stable muscle attachments in the zebrafish embryo. Development 2003, 130:5851-5860.
5. Belenky P., Bogan K.L., Brenner C. NAD+ metabolism in health and disease. Trends Biochem. Sci. 2007, 32:12-19.
6. Belenky P., Christensen K.C., Gazzaniga F., Pletnev A.A., Brenner C. Nicotinamide riboside and nicotinic acid riboside salvage in fungi and mammals: quantitative basis for Urh1 and purine nucleoside phosphorylase function in NAD+ metabolism. J. Biol. Chem. 2009, 284:158-164.
7. Belenky P., Racette F.G., Bogan K.L., McClure J.M., Smith J.S., Brenner C. Nicotinamide riboside promotes Sir2 silencing and extends lifespan via Nrk and Urh1/Pnp1/Meu1 pathways to NAD+. Cell 2007, 129:473-484.
8. Bertolucci C.M., Guibao C.D., Zheng J. Structural features of the focal adhesion kinase-paxillin complex give insight into the dynamics of focal adhesion assembly. Protein Sci. 2005, 14:644-652.
9. Bieganowski P., Brenner C. Discoveries of nicotinamide riboside as a nutrient and conserved NRK genes establish a Preiss-Handler independent route to NAD+ in fungi and humans. Cell 2004, 117:495-502.
10. Bissell M.J., Hall H.G., Parry G. How does the extracellular matrix direct gene expression?. J. Theor. Biol. 1982, 99:31-68.
11. Bogan K.L., Brenner C. Nicotinic acid, nicotinamide, and nicotinamide riboside: a molecular evaluation of NAD+ precursor vitamins in human nutrition. Annu. Rev. Nutr. 2008, 28:115-130.
12. Briguet A., Courdier-Fruh I., Foster M., Meier T., Magyar J.P. Histological parameters for the quantitative assessment of muscular dystrophy in the mdx-mouse. Neuromuscul. Disord. 2004, 14:675-682.
13. Chatzizacharias N.A., Kouraklis G.P., Theocharis S.E. Clinical significance of FAK expression in human neoplasia. Histol. Histopathol. 2008, 23:629-650.
14. Cooper W.J., Albertson R.C. Quantification and variation in experimental studies of morphogenesis. Dev. Biol. 2008, 321:295-302.
15. Crawford B.D., Henry C.A., Clason T.A., Becker A.L., Hille M.B. Activity and distribution of paxillin, focal adhesion kinase, and cadherin indicate cooperative roles during zebrafish morphogenesis. Mol. Biol. Cell 2003, 14:3065-3081.
16. Deakin N.O., Turner C.E. Paxillin comes of age. J. Cell Sci. 2008, 121:2435-2444.
17. Digman M.A., Brown C.M., Horwitz A.R., Mantulin W.W., Gratton E. Paxillin dynamics measured during adhesion assembly and disassembly by correlation spectroscopy. Biophys. J. 2008, 94:2819-2831.
18. Eisen J.S., Smith J.C. Controlling morpholino experiments: don't stop making antisense. Development 2008, 135:1735-1743.
19. Gao G., Prutzman K.C., King M.L., Scheswohl D.M., DeRose E.F., London R.E., Schaller M.D., Campbell S.L. NMR solution structure of the focal adhesion targeting domain of focal adhesion kinase in complex with a paxillin LD peptide: evidence for a two-site binding model. J. Biol. Chem. 2004, 279:8441-8451.
20. Geiger B., Bershadsky A., Pankov R., Yamada K.M. Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat. Rev. Mol. Cell Biol. 2001, 2:793-805.
21. Gordon S.E., Fluck M., Booth F.W. Selected contribution: skeletal muscle focal adhesion kinase, paxillin, and serum response factor are loading dependent. J. Appl. Physiol. 2001, 90:1174-1183. discussion 1165.
22. Guyon J.R., Steffen L.S., Howell M.H., Pusack T.J., Lawrence C., Kunkel L.M. Modeling human muscle disease in zebrafish. Biochim. Biophys. Acta 2007, 1772:205-215.
23. Hagel M., George E.L., Kim A., Tamimi R., Opitz S.L., Turner C.E., Imamoto A., Thomas S.M. The adaptor protein paxillin is essential for normal development in the mouse and is a critical transducer of fibronectin signaling. Mol. Cell. Biol. 2002, 22:901-915.
24. Hall T.E., Bryson-Richardson R.J., Berger S., Jacoby A.S., Cole N.J., Hollway G.E., Berger J., Currie P.D. The zebrafish candyfloss mutant implicates extracellular matrix adhesion failure in laminin {alpha}2-deficient congenital muscular dystrophy. Proc. Natl. Acad. Sci. U S A 2007, 104:7092-7097.
25. Hassa P.O., Hottiger M.O. The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases. Front. Biosci. 2008, 13:3046-3082.
26. Henry C.A., McNulty I.M., Durst W.A., Munchel S.E., Amacher S.L. Interactions between muscle fibers and segment boundaries in zebrafish. Dev. Biol. 2005, 287:346-360.
27. Ilic D., Furuta Y., Kanazawa S., Takeda N., Sobue K., Nakatsuji N., Nomura S., Fujimoto J., Okada M., Yamamoto T. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 1995, 377:539-544.
28. Jones K.S., Alimov A.P., Rilo H.L., Jandacek R.J., Woollett L.A., Penberthy W.T. A high throughput live transparent animal bioassay to identify non-toxic small molecules or genes that regulate vertebrate fat metabolism for obesity drug development. Nutr. Metab. 2008, 5:23. (Lond).
29. Kahn R.A. Toward a model for Arf GTPases as regulators of traffic at the Golgi. FEBS Lett. 2009, 583:3872-3879.
30. Kanagawa M., Toda T. The genetic and molecular basis of muscular dystrophy: roles of cell-matrix linkage in the pathogenesis. J. Hum. Genet. 2006.
31. Keppler B.R., Archer T.K. Chromatin-modifying enzymes as therapeutic targets-Part 1. Expert Opin. Ther. Targets 2008, 12:1301-1312.
32. Khalil A. Morphological analysis of HI features. II. Wavelet-based multifractal formalism. Astrophys. J. Suppl. Ser. 2006, 165:512-550.
33. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203:253-310.
34. Koch-Nolte F., Kernstock S., Mueller-Dieckmann C., Weiss M.S., Haag F. Mammalian ADP-ribosyltransferases and ADP-ribosylhydrolases. Front. Biosci. 2008, 13:6716-6729.
35. Kudo H., Amizuka N., Araki K., Inohaya K., Kudo A. Zebrafish periostin is required for the adhesion of muscle fiber bundles to the myoseptum and for the differentiation of muscle fibers. Dev. Biol. 2004, 267:473-487.
36. Kwan K.M., Fujimoto E., Grabher C., Mangum B.D., Hardy M.E., Campbell D.S., Parant J.M., Yost H.J., Kanki J.P., Chien C.B. The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 2007, 236:3088-3099.
37. Li J., Mayne R., Wu C. A novel muscle-specific beta 1 integrin binding protein (MIBP) that modulates myogenic differentiation. J. Cell Biol. 1999, 147:1391-1398.
38. Li J., Rao H., Burkin D., Kaufman S.J., Wu C. The muscle integrin binding protein (MIBP) interacts with alpha7beta1 integrin and regulates cell adhesion and laminin matrix deposition. Dev. Biol. 2003, 261:209-219.
39. Lieschke G.J., Currie P.D. Animal models of human disease: zebrafish swim into view. Nat. Rev. Genet. 2007, 8:353-367.
40. Link V., Shevchenko A., Heisenberg C.P. Proteomics of early zebrafish embryos. BMC Dev. Biol. 2006, 6:1.
41. Lock J.G., Wehrle-Haller B., Stromblad S. Cell-matrix adhesion complexes: master control machinery of cell migration. Semin. Cancer Biol. 2008, 18:65-76.
42. Lunt S.J., Chaudary N., Hill R.P. The tumor microenvironment and metastatic disease. Clin. Exp. Metastasis 2009, 26:19-34.
43. Myers K.R., Casanova J.E. Regulation of actin cytoskeleton dynamics by Arf-family GTPases. Trends Cell Biol. 2008, 18:184-192.
44. Nixon S.J., Wegner J., Ferguson C., Mery P.F., Hancock J.F., Currie P.D., Key B., Westerfield M., Parton R.G. Zebrafish as a model for caveolin-associated muscle disease; caveolin-3 is required for myofibril organization and muscle cell patterning. Hum. Mol. Genet. 2005, 14:1727-1743.
45. Pagnon-Minot A., Malbouyres M., Haftek-Terreau Z., Kim H.R., Sasaki T., Thisse C., Thisse B., Ingham P.W., Ruggiero F., Le Guellec D. Collagen XV, a novel factor in zebrafish notochord differentiation and muscle development. Dev. Biol. 2008, 316:21-35.
46. Park T.J., Mitchell B.J., Abitua P.B., Kintner C., Wallingford J.B. Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nat. Genet. 2008, 40:871-879.
47. Parsons M.J., Campos I., Hirst E.M., Stemple D.L. Removal of dystroglycan causes severe muscular dystrophy in zebrafish embryos. Development 2002, 129:3505-3512.
48. Parsons M.J., Pollard S.M., Saude L., Feldman B., Coutinho P., Hirst E.M., Stemple D.L. Zebrafish mutants identify an essential role for laminins in notochord formation. Development 2002, 129:3137-3146.
49. Postel R., Vakeel P., Topczewski J., Knoll R., Bakkers J. Zebrafish integrin-linked kinase is required in skeletal muscles for strengthening the integrin-ECM adhesion complex. Dev. Biol. 2008, 318:92-101.
50. Quach N.L., Rando T.A. Focal adhesion kinase is essential for costamerogenesis in cultured skeletal muscle cells. Dev. Biol. 2006, 293:38-52.
51. Robu M.E., Larson J.D., Nasevicius A., Beiraghi S., Brenner C., Farber S.A., Ekker S.C. p53 activation by knockdown technologies. PLoS Genet. 2007, 3:e78.
52. Sabe H., Onodera Y., Mazaki Y., Hashimoto S. ArfGAP family proteins in cell adhesion, migration and tumor invasion. Curr. Opin. Cell Biol. 2006, 18:558-564.
53. Sadkowski T., Jank M., Zwierzchowski L., Siadkowska E., Oprzadek J., Motyl T. Gene expression profiling in skeletal muscle of Holstein-Friesian bulls with single-nucleotide polymorphism in the myostatin gene 5'-flanking region. J. Appl. Genet. 2008, 49:237-250.
54. Saporita A.J., Maggi L.B., Apicelli A.J., Weber J.D. Therapeutic targets in the ARF tumor suppressor pathway. Curr. Med. Chem. 2007, 14:1815-1827.
55. Schaller M.D., Borgman C.A., Cobb B.S., Vines R.R., Reynolds A.B., Parsons J.T. pp 125FAK a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc. Natl Acad. Sci. USA 1992, 89:5192-5196.
56. Schessl J., Zou Y., Bonnemann C.G. Congenital muscular dystrophies and the extracellular matrix. Semin. Pediatr. Neurol. 2006, 13:80-89.
57. Scheswohl D.M., Harrell J.R., Rajfur Z., Gao G., Campbell S.L., Schaller M.D. Multiple paxillin binding sites regulate FAK function. J. Mol. Signal. 2008, 3:1.
58. Snow C.J., Goody M., Kelly M.W., Oster E.C., Jones R., Khalil A., Henry C.A. Time-lapse analysis and mathematical characterization elucidate novel mechanisms underlying muscle morphogenesis. PLoS Genet. 2008, 4:e1000219.
59. Snow C.J., Henry C.A. Dynamic formation of microenvironments at the myotendinous junction correlates with muscle fiber morphogenesis in zebrafish. Gene Expr. Patterns 2008.
60. Snow C.J., Peterson M.T., Khalil A., Henry C.A. Muscle development is disrupted in zebrafish embryos deficient for fibronectin. Dev. Dyn. 2008, 237:2542-2553.
61. Steffen L.S., Guyon J.R., Vogel E.D., Beltre R., Pusack T.J., Zhou Y., Zon L.I., Kunkel L.M. Zebrafish orthologs of human muscular dystrophy genes. BMC Genomics 2007, 8:79.
62. Stockwin L.H., Vistica D.T., Kenney S., Schrump D.S., Butcher D.O., Raffeld M., Shoemaker R.H. Gene expression profiling of alveolar soft-part sarcoma (ASPS). BMC Cancer 2009, 9:22.
63. Tariq M., Azeem Z., Ali G., Chishti M.S., Ahmad W. Mutation in the HPGD gene encoding NAD+ dependent 15-hydroxyprostaglandin dehydrogenase underlies isolated congenital nail clubbing (ICNC). J. Med. Genet. 2009, 46:14-20.
64. Tempel W., Rabeh W.M., Bogan K.L., Belenky P., Wojcik M., Seidle H.F., Nedyalkova L., Yang T., Sauve A.A., Park H.W., Brenner C. Nicotinamide riboside kinase structures reveal new pathways to NAD+. PLoS Biol. 2007, 5:e263.
65. Thisse B., Heyer V., Lux A., Alunni V., Degrave A., Seiliez I., Kirchner J., Parkhill J.P., Thisse C. Spatial and temporal expression of the zebrafish genome by large-scale in situ hybridization screening. Meth. Cell Biol. 2004, 77:505-519.
66. Thomas J.W., Cooley M.A., Broome J.M., Salgia R., Griffin J.D., Lombardo C.R., Schaller M.D. The role of focal adhesion kinase binding in the regulation of tyrosine phosphorylation of paxillin. J. Biol. Chem. 1999, 274:36684-36692.
67. Thornhill P., Bassett D., Lochmuller H., Bushby K., Straub V. Developmental defects in a zebrafish model for muscular dystrophies associated with the loss of fukutin-related protein (FKRP). Brain 2008, 131:1551-1561.
68. Tzu J., Marinkovich M.P. Bridging structure with function: structural, regulatory, and developmental role of laminins. Int. J. Biochem. Cell Biol. 2008, 40:199-214.
69. Wade R., Bohl J., Vande Pol S. Paxillin null embryonic stem cells are impaired in cell spreading and tyrosine phosphorylation of focal adhesion kinase. Oncogene 2002, 21:96-107.
70. Waller J.C., Dhanoa P.K., Schumann U., Mullen R.T., Snedden W.A. Subcellular and tissue localization of NAD kinases from Arabidopsis: compartmentalization of de novo NADP biosynthesis. Planta 2010, 231:305-317.
71. Webb D.J., Donais K., Whitmore L.A., Thomas S.M., Turner C.E., Parsons J.T., Horwitz A.F. FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat. Cell Biol. 2004, 6:154-161.
72. White E.S., Baralle F.E., Muro A.F. New insights into form and function of fibronectin splice variants. J. Pathol. 2008, 216:1-14.
73. Yin C., Kiskowski M., Pouille P.A., Farge E., Solnica-Krezel L. Cooperation of polarized cell intercalations drives convergence and extension of presomitic mesoderm during zebrafish gastrulation. J. Cell Biol. 2008, 180:221-232.
74. Zhao Z., Gruszczynska-Biegala J., Zolkiewska A. ADP-ribosylation of integrin alpha7 modulates the binding of integrin alpha7beta1 to laminin. Biochem. J. 2005, 385:309-317.
75. Zolkiewska A., Moss J. The alpha 7 integrin as a target protein for cell surface mono-ADP-ribosylation in muscle cells. Adv. Exp. Med. Biol. 1997, 419:297-303.