Neuronal control of metabolism through nutrient-dependent modulation of tracheal branching

Cell

Volumn 156, Issue 1-2, 2014, Pages 69-83

  Linneweber, Gerit A ^a   Jacobson, Jake ^a   Busch, Karl Emanuel ^b   Hudry, Bruno ^a   Christov, Christo P ^c   Dormann, Dirk ^a   Yuan, Michaela ^d   Otani, Tomoki ^c   Knust, Elisabeth ^d   De Bono, Mario ^b   Miguel Aliaga, Irene ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN LIKE NEUROPEPTIDE; NEUROPEPTIDE; UNCLASSIFIED DRUG; VIP LIKE NEUROPEPTIDE; INSULIN; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; DROSOPHILA; INTESTINE; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; NUTRIENT; PRIORITY JOURNAL; TRACHEA; ANGIOGENESIS; ANIMAL TISSUE; BLOOD VESSEL; BRANCHING MORPHOGENESIS; CONTROLLED STUDY; MAMMAL; METABOLIC REGULATION; NEUROMODULATION; OXYGEN TRANSPORT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TARGET ORGAN; TRACHEAL BRANCHING;

ANIMALS; CALCIUM; DIGESTIVE SYSTEM; DROSOPHILA MELANOGASTER; HUMANS; MODELS, ANIMAL; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; NEURONS; NEUROPEPTIDES; OXYGEN; SIGNAL TRANSDUCTION; VASOACTIVE INTESTINAL PEPTIDE;

EID: 84892775294     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.12.008     Document Type: Article

References (75)

1. J.L. Adolphe, S.J. Whiting, B.H. Juurlink, L.U. Thorpe, and J. Alcorn Health effects with consumption of the flax lignan secoisolariciresinol diglucoside Br. J. Nutr. 103 2010 929 938
2. D.S. Andersen, J. Colombani, and P. Léopold Coordination of organ growth: principles and outstanding questions from the world of insects Trends Cell Biol. 23 2013 336 344
3. A. Asano, M. Morimatsu, H. Nikami, T. Yoshida, and M. Saito Adrenergic activation of vascular endothelial growth factor mRNA expression in rat brown adipose tissue: implication in cold-induced angiogenesis Biochem. J. 328 1997 179 183
4. L. Belkacemi, D.M. Nelson, M. Desai, and M.G. Ross Maternal undernutrition influences placental-fetal development Biol. Reprod. 83 2010 325 331
5. R. Böhni, J. Riesgo-Escovar, S. Oldham, W. Brogiolo, H. Stocker, B.F. Andruss, K. Beckingham, and E. Hafen Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4 Cell 97 1999 865 875
6. W. Brogiolo, H. Stocker, T. Ikeya, F. Rintelen, R. Fernandez, and E. Hafen An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control Curr. Biol. 11 2001 213 221
7. Y. Cao Angiogenesis modulates adipogenesis and obesity J. Clin. Invest. 117 2007 2362 2368
8. Y. Cao Adipose tissue angiogenesis as a therapeutic target for obesity and metabolic diseases Nat. Rev. Drug Discov. 9 2010 107 115
9. P. Carmeliet, and M. Tessier-Lavigne Common mechanisms of nerve and blood vessel wiring Nature 436 2005 193 200
10. L. Centanin, A. Dekanty, N. Romero, M. Irisarri, T.A. Gorr, and P. Wappner Cell autonomy of HIF effects in Drosophila: tracheal cells sense hypoxia and induce terminal branch sprouting Dev. Cell 14 2008 547 558
11. A. Chaudhuri, P. Dandona, and V. Fonseca Cardiovascular benefits of exogenous insulin J. Clin. Endocrinol. Metab. 97 2012 3079 3091
12. J.M. Chell, and A.H. Brand Nutrition-responsive glia control exit of neural stem cells from quiescence Cell 143 2010 1161 1173
13. U. Cheung, M. Moghaddasi, H.L. Hall, J.J. Smith, L.T. Buck, and M.A. Woodin Excitatory actions of GABA mediate severe-hypoxia-induced depression of neuronal activity in the pond snail (Lymnaea stagnalis) J. Exp. Biol. 209 2006 4429 4435
14. P. Cognigni, A.P. Bailey, and I. Miguel-Aliaga Enteric neurons and systemic signals couple nutritional and reproductive status with intestinal homeostasis Cell Metab. 13 2011 92 104
15. A.M. Davies Extracellular signals regulating sympathetic neuron survival and target innervation during development Auton. Neurosci. 151 2009 39 45
16. P.A. Foley, and L.S. Luckinbill The effects of selection for larval behavior on adult life-history features in Drosophila melanogaster Evolution 55 2001 2493 2502
17. P. Fraisl, M. Mazzone, T. Schmidt, and P. Carmeliet Regulation of angiogenesis by oxygen and metabolism Dev. Cell 16 2009 167 179
18. N. Fujiwara, H. Higashi, K. Shimoji, and M. Yoshimura Effects of hypoxia on rat hippocampal neurones in vitro J. Physiol. 384 1987 131 151
19. C. Géminard, E.J. Rulifson, and P. Léopold Remote control of insulin secretion by fat cells in Drosophila Cell Metab. 10 2009 199 207
20. L. Gervais, and J. Casanova The Drosophila homologue of SRF acts as a boosting mechanism to sustain FGF-induced terminal branching in the tracheal system Development 138 2011 1269 1274
21. A. Ghabrial, S. Luschnig, M.M. Metzstein, and M.A. Krasnow Branching morphogenesis of the Drosophila tracheal system Annu. Rev. Cell Dev. Biol. 19 2003 623 647
22. S. Grönke, D.F. Clarke, S. Broughton, T.D. Andrews, and L. Partridge Molecular evolution and functional characterization of Drosophila insulin-like peptides PLoS Genet. 6 2010 e1000857
23. Z. Guo, I. Driver, and B. Ohlstein Injury-induced BMP signaling negatively regulates Drosophila midgut homeostasis J. Cell Biol. 201 2013 945 961
24. P. Holzer Neural regulation of gastrointestinal blood flow L.R. Johnson, Physiology of the gastrointestinal tract 2006 Elsevier Academic Press Amsterdam 817 840
25. Y.C. Jang, F.F. Isik, and N.S. Gibran Nerve distribution in hemangiomas depends on the proliferative state of the microvasculature J. Surg. Res. 93 2000 144 148
26. J. Jarecki, E. Johnson, and M.A. Krasnow Oxygen regulation of airway branching in Drosophila is mediated by branchless FGF Cell 99 1999 211 220
27. S. Javerzat, P. Auguste, and A. Bikfalvi The role of fibroblast growth factors in vascular development Trends Mol. Med. 8 2002 483 489
28. R.S. Kerbel Tumor angiogenesis N. Engl. J. Med. 358 2008 2039 2049
29. K. Krnjević Early effects of hypoxia on brain cell function Croat. Med. J. 40 1999 375 380
30. M. Kumar, R. Nagpal, V. Verma, A. Kumar, N. Kaur, R. Hemalatha, S.K. Gautam, and B. Singh Probiotic metabolites as epigenetic targets in the prevention of colon cancer Nutr. Rev. 71 2013 23 34
31. S.J. Leevers, D. Weinkove, L.K. MacDougall, E. Hafen, and M.D. Waterfield The Drosophila phosphoinositide 3-kinase Dp110 promotes cell growth EMBO J. 15 1996 6584 6594
32. Z. Li, Y. Zhang, L. Han, L. Shi, and X. Lin Trachea-derived dpp controls adult midgut homeostasis in Drosophila Dev. Cell 24 2013 133 143
33. H.R. Lijnen Angiogenesis and obesity Cardiovasc. Res. 78 2008 286 293
34. K.S. Madden, M.J. Szpunar, and E.B. Brown β-Adrenergic receptors (β-AR) regulate VEGF and IL-6 production by divergent pathways in high β-AR-expressing breast cancer cell lines Breast Cancer Res. Treat. 130 2011 747 758
35. P.J. Matheson, M.A. Wilson, and R.N. Garrison Regulation of intestinal blood flow J. Surg. Res. 93 2000 182 196
36. R.J. Metzger, O.D. Klein, G.R. Martin, and M.A. Krasnow The branching programme of mouse lung development Nature 453 2008 745 750
37. I. Miguel-Aliaga, S. Thor, and A.P. Gould Postmitotic specification of Drosophila insulinergic neurons from pioneer neurons PLoS Biol. 6 2008 e58
38. Y.S. Mukouyama, D. Shin, S. Britsch, M. Taniguchi, and D.J. Anderson Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin Cell 109 2002 693 705
39. Y.S. Mukouyama, H.P. Gerber, N. Ferrara, C. Gu, and D.J. Anderson Peripheral nerve-derived VEGF promotes arterial differentiation via neuropilin 1-mediated positive feedback Development 132 2005 941 952
40. L.E. O'Brien, S.S. Soliman, X. Li, and D. Bilder Altered modes of stem cell division drive adaptive intestinal growth Cell 147 2011 603 614
41. F. O'Farrell, S. Wang, N. Katheder, T.E. Rusten, and C. Samakovlis Two-tiered control of epithelial growth and autophagy by the insulin receptor and the ret-like receptor, stitcher PLoS Biol. 11 2013 e1001612
42. M. Ogasawara, J. Murata, Y. Kamitani, K. Hayashi, and I. Saiki Inhibition by vasoactive intestinal polypeptide (VIP) of angiogenesis induced by murine Colon 26-L5 carcinoma cells metastasized in liver Clin. Exp. Metastasis 17 1999 283 291
43. R. Pardal, and J. López-Barneo Low glucose-sensing cells in the carotid body Nat. Neurosci. 5 2002 197 198
44. M. Potente, H. Gerhardt, and P. Carmeliet Basic and therapeutic aspects of angiogenesis Cell 146 2011 873 887
45. N.R. Prabhakar Oxygen sensing by the carotid body chemoreceptors J. Appl. Physiol. 88 2000 2287 2295
46. A. Quaegebeur, C. Lange, and P. Carmeliet The neurovascular link in health and disease: molecular mechanisms and therapeutic implications Neuron 71 2011 406 424
47. D. Ribatti, M.T. Conconi, and G.G. Nussdorfer Nonclassic endogenous novel [corrected] regulators of angiogenesis Pharmacol. Rev. 59 2007 185 205
48. E.J. Rulifson, S.K. Kim, and R. Nusse Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes Science 296 2002 1118 1120
49. C.S. Rutland, A.O. Latunde-Dada, A. Thorpe, R. Plant, S. Langley-Evans, and L. Leach Effect of gestational nutrition on vascular integrity in the murine placenta Placenta 28 2007 734 742
50. C.A. Schneider, W.S. Rasband, and K.W. Eliceiri NIH Image to ImageJ: 25 years of image analysis Nat. Methods 9 2012 671 675
51. M. Slaidina, R. Delanoue, S. Gronke, L. Partridge, and P. Léopold A Drosophila insulin-like peptide promotes growth during nonfeeding states Dev. Cell 17 2009 874 884
52. R. Sousa-Nunes, L.L. Yee, and A.P. Gould Fat cells reactivate quiescent neuroblasts via TOR and glial insulin relays in Drosophila Nature 471 2011 508 512
53. E. Storkebaum, A. Quaegebeur, M. Vikkula, and P. Carmeliet Cerebrovascular disorders: molecular insights and therapeutic opportunities Nat. Neurosci. 14 2011 1390 1397
54. K. Sun, I. Wernstedt Asterholm, C.M. Kusminski, A.C. Bueno, Z.V. Wang, J.W. Pollard, R.A. Brekken, and P.E. Scherer Dichotomous effects of VEGF-A on adipose tissue dysfunction Proc. Natl. Acad. Sci. USA 109 2012 5874 5879
55. H.K. Sung, K.O. Doh, J.E. Son, J.G. Park, Y. Bae, S. Choi, S.M. Nelson, R. Cowling, K. Nagy, and I.P. Michael et al. Adipose vascular endothelial growth factor regulates metabolic homeostasis through angiogenesis Cell Metab. 17 2013 61 72
56. A. Suska, I. Miguel-Aliaga, and S. Thor Segment-specific generation of Drosophila Capability neuropeptide neurons by multi-faceted Hox cues Dev. Biol. 353 2011 72 80
57. P.H. Taghert, and M.N. Nitabach Peptide neuromodulation in invertebrate model systems Neuron 76 2012 82 97
58. A.D. Talsma, C.P. Christov, A. Terriente-Felix, G.A. Linneweber, D. Perea, M. Wayland, O.T. Shafer, and I. Miguel-Aliaga Remote control of renal physiology by the intestinal neuropeptide pigment-dispersing factor in Drosophila Proc. Natl. Acad. Sci. USA 109 2012 12177 12182
59. H.Y. Tang, M.S. Smith-Caldas, M.V. Driscoll, S. Salhadar, and A.W. Shingleton FOXO regulates organ-specific phenotypic plasticity in Drosophila PLoS Genet. 7 2011 e1002373
60. L. Tian, S.A. Hires, T. Mao, D. Huber, M.E. Chiappe, S.H. Chalasani, L. Petreanu, J. Akerboom, S.A. McKinney, and E.R. Schreiter et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators Nat. Methods 6 2009 875 881
61. M. Toda, T. Suzuki, K. Hosono, I. Hayashi, S. Hashiba, Y. Onuma, H. Amano, Y. Kurihara, H. Kurihara, and H. Okamoto et al. Neuronal system-dependent facilitation of tumor angiogenesis and tumor growth by calcitonin gene-related peptide Proc. Natl. Acad. Sci. USA 105 2008 13550 13555
62. C. Tonello, A. Giordano, V. Cozzi, S. Cinti, M.J. Stock, M.O. Carruba, and E. Nisoli Role of sympathetic activity in controlling the expression of vascular endothelial growth factor in brown fat cells of lean and genetically obese rats FEBS Lett. 442 1999 167 172
63. A. Uv, R. Cantera, and C. Samakovlis Drosophila tracheal morphogenesis: intricate cellular solutions to basic plumbing problems Trends Cell Biol. 13 2003 301 309
64. A. Vesalius De humani corporis fabrica 1543 Oporinus Basel
65. M. Willecke, J. Toggweiler, and K. Basler Loss of PI3K blocks cell-cycle progression in a Drosophila tumor model Oncogene 30 2011 4067 4074
66. B.J. Zwaan, R. Bijlsma, and R.F. Hoekstra On the developmental theory of ageing. I. starvation resistance and longevity in Drosophila melanogaster in relation to pre-adult breeding conditions Heredity (Edinb) 66 1991 29 39
67. D.W. Allan, S.E. St Pierre, I. Miguel-Aliaga, and S. Thor Specification of neuropeptide cell identity by the integration of retrograde BMP signaling and a combinatorial transcription factor code Cell 113 2003 73 86
68. R.A. Baines, J.P. Uhler, A. Thompson, S.T. Sweeney, and M. Bate Altered electrical properties in Drosophila neurons developing without synaptic transmission J. Neurosci. 21 2001 1523 1531
69. 2 sensors sets neural circuit activity and behavioral state Nat. Neurosci. 15 2012 581 591
70. F.N. Hamada, M. Rosenzweig, K. Kang, S.R. Pulver, A. Ghezzi, T.J. Jegla, and P.A. Garrity An internal thermal sensor controlling temperature preference in Drosophila Nature 454 2008 217 220
71. D.P. Harrington, and T.R. Fleming A class of rank test procedures for censored survival data Biometrika 69 1982 553 566
72. T. Lee, and L. Luo Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis Neuron 22 1999 451 461
73. S.C. Renn, J.H. Park, M. Rosbash, J.C. Hall, and P.H. Taghert A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila Cell 99 1999 791 802
74. M. Shiga, M. Tanaka-Matakatsu, and S. Hayashi A nuclear GFP/β-galactosidase fusion protein as a marker for morphogenesis in living Drosophila Dev. Growth Differ. 38 1996 99 106
75. C.H. Yang, P. Belawat, E. Hafen, L.Y. Jan, and Y.N. Jan Drosophila egg-laying site selection as a system to study simple decision-making processes Science 319 2008 1679 1683