1932

Abstract

Many organisms have developed a robust ability to adapt and survive in the face of environmental perturbations that threaten the integrity of their genome, proteome, or metabolome. Studies in multiple model organisms have shown that, in general, when exposed to stress, cells activate a complex prosurvival signaling network that includes immune and DNA damage response genes, chaperones, antioxidant enzymes, structural proteins, metabolic enzymes, and noncoding RNAs. The manner of activation runs the gamut from transcriptional induction of genes to increased stability of transcripts to posttranslational modification of important biosynthetic proteins within the stressed tissue. Superimposed on these largely autonomous effects are nonautonomous responses in which the stressed tissue secretes peptides and other factors that stimulate tissues in different organs to embark on processes that ultimately help the organism as a whole cope with stress. This review focuses on the mechanisms by which tissues in one organ adapt to environmental challenges by regulating stress responses in tissues of different organs.

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2015-11-13
2024-04-26
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Literature Cited

  1. Adams AC, Coskun T, Cheng CC, O'Farrell LS, Dubois SL, Kharitonenkov A. 2013. Fibroblast growth factor 21 is not required for the antidiabetic actions of the thiazolidinediones. Mol. Metab. 2:205–14 [Google Scholar]
  2. Alfa RW, Park S, Skelly KR, Poffenberger G, Jain N. et al. 2015. Suppression of insulin production and secretion by a decretin hormone. Cell Metab. 21:323–33 [Google Scholar]
  3. Alic N, Hoddinott MP, Vinti G, Partridge L. 2011. Lifespan extension by increased expression of the Drosophila homologue of the IGFBP7 tumour suppressor. Aging Cell 10:137–47 [Google Scholar]
  4. Amat J, Baratta MV, Paul E, Bland ST, Watkins LR, Maier SF. 2005. Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat. Neurosci. 8:365–71 [Google Scholar]
  5. Amcheslavsky A, Song W, Li Q, Nie Y, Bragatto I. et al. 2014. Enteroendocrine cells support intestinal stem-cell–mediated homeostasis in Drosophila. Cell Rep. 9:32–39 [Google Scholar]
  6. Andersen DS, Colombani J, Leopold P. 2013. Coordination of organ growth: principles and outstanding questions from the world of insects. Trends Cell Biol. 23:336–44 [Google Scholar]
  7. Andreux PA, Houtkooper RH, Auwerx J. 2013. Pharmacological approaches to restore mitochondrial function. Nat. Rev. Drug Discov. 12:465–83 [Google Scholar]
  8. Apidianakis Y, Pitsouli C, Perrimon N, Rahme L. 2009. Synergy between bacterial infection and genetic predisposition in intestinal dysplasia. PNAS 106:20883–88 [Google Scholar]
  9. Arida RM, Gomes da Silva S, de Almeida AA, Cavalheiro EA, Zavala-Tecuapetla C. et al. 2015. Differential effects of exercise on brain opioid receptor binding and activation in rats. J. Neurochem. 132:206–17 [Google Scholar]
  10. Augusto AC, Miguel F, Mendonca S, Pedrazzoli J Jr, Gurgueira SA. 2007. Oxidative stress expression status associated to Helicobacter pylori virulence in gastric diseases. Clin. Biochem. 40:615–22 [Google Scholar]
  11. Bai H, Kang P, Hernandez AM, Tatar M. 2013. Activin signaling targeted by insulin/dFOXO regulates aging and muscle proteostasis in Drosophila. PLOS Genet. 9:e1003941 [Google Scholar]
  12. Balkwill F. 2009. Tumour necrosis factor and cancer. Nat. Rev. Cancer 9:361–71 [Google Scholar]
  13. Baratta MV, Zarza CM, Gomez DM, Campeau S, Watkins LR, Maier SF. 2009. Selective activation of dorsal raphe nucleus–projecting neurons in the ventral medial prefrontal cortex by controllable stress. Eur. J. Neurosci. 30:1111–16 [Google Scholar]
  14. Barbatelli G, Murano I, Madsen L, Hao Q, Jimenez M. et al. 2010. The emergence of cold-induced brown adipocytes in mouse white fat depots is determined predominantly by white to brown adipocyte transdifferentiation. Am. J. Physiol. Endocrinol. Metab. 298:E1244–53 [Google Scholar]
  15. Basu R, Pajvani UB, Rizza RA, Scherer PE. 2007. Selective downregulation of the high molecular weight form of adiponectin in hyperinsulinemia and in type 2 diabetes: differential regulation from nondiabetic subjects. Diabetes 56:2174–77 [Google Scholar]
  16. Baumbach J, Hummel P, Bickmeyer I, Kowalczyk KM, Frank M. et al. 2014. A Drosophila in vivo screen identifies store-operated calcium entry as a key regulator of adiposity. Cell Metab. 19:331–43 [Google Scholar]
  17. Becker T, Loch G, Beyer M, Zinke I, Aschenbrenner AC. et al. 2010. FOXO-dependent regulation of innate immune homeostasis. Nature 463:369–73 [Google Scholar]
  18. Begriche K, Massart J, Abbey-Toby A, Igoudjil A, Letteron P, Fromenty B. 2008. β-aminoisobutyric acid prevents diet-induced obesity in mice with partial leptin deficiency. Obesity 16:2053–67 [Google Scholar]
  19. Belmont PJ, Tadimalla A, Chen WJ, Martindale JJ, Thuerauf DJ. et al. 2008. Coordination of growth and endoplasmic reticulum stress signaling by regulator of calcineurin 1 (RCAN1), a novel ATF6-inducible gene. J. Biol. Chem. 283:14012–21 [Google Scholar]
  20. Benkel BF, Hickey DA. 1986. Glucose repression of amylase gene expression in Drosophila melanogaster. Genetics 114:137–44 [Google Scholar]
  21. Berrilli F, Di Cave D, Cavallero S, D'Amelio S. 2012. Interactions between parasites and microbial communities in the human gut. Front. Cell Infect. Microbiol. 2:141 [Google Scholar]
  22. Blake MJ, Buckley DJ, Buckley AR. 1993. Dopaminergic regulation of heat shock protein-70 expression in adrenal gland and aorta. Endocrinology 132:1063–70 [Google Scholar]
  23. Blake MJ, Udelsman R, Feulner GJ, Norton DD, Holbrook NJ. 1991. Stress-induced heat shock protein 70 expression in adrenal cortex: an adrenocorticotropic hormone-sensitive, age-dependent response. PNAS 88:9873–77 [Google Scholar]
  24. Bortoluzzi S, Scannapieco P, Cestaro A, Danieli GA, Schiaffino S. 2006. Computational reconstruction of the human skeletal muscle secretome. Proteins 62:776–92 [Google Scholar]
  25. Bostrom P, Wu J, Jedrychowski MP, Korde A, Ye L. et al. 2012. A PGC1α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481:463–68 [Google Scholar]
  26. Brun CE, Rudnicki MA. 2015. GDF11 and the mythical Fountain of Youth. Cell Metab. 22:54–56 [Google Scholar]
  27. Caers J, Peeters L, Janssen T, De Haes W, Gade G, Schoofs L. 2012. Structure-activity studies of Drosophila adipokinetic hormone (AKH) by a cellular expression system of dipteran AKH receptors. Gen. Comp. Endocrinol. 177:332–37 [Google Scholar]
  28. Chan XC, McDermott JC, Siu KW. 2007. Identification of secreted proteins during skeletal muscle development. J. Proteome Res. 6:698–710 [Google Scholar]
  29. Chaturvedi R, Asim M, Romero-Gallo J, Barry DP, Hoge S. et al. 2011. Spermine oxidase mediates the gastric cancer risk associated with Helicobacter pylori CagA. Gastroenterology 141:1696–708 [Google Scholar]
  30. Chen H, Zheng X, Zheng Y. 2014. Age-associated loss of lamin-B leads to systemic inflammation and gut hyperplasia. Cell 159:829–43 [Google Scholar]
  31. Cheng A, Wan R, Yang JL, Kamimura N, Son TG. et al. 2012. Involvement of PGC-1α in the formation and maintenance of neuronal dendritic spines. Nat. Commun. 3:1250 [Google Scholar]
  32. Chintapalli VR, Al Bratty M, Korzekwa D, Watson DG, Dow JA. 2013. Mapping an atlas of tissue-specific Drosophila melanogaster metabolomes by high-resolution mass spectrometry. PLOS ONE 8:e78066 [Google Scholar]
  33. Chng WB, Bou Sleiman MS, Schupfer F, Lemaitre B. 2014. Transforming growth factor β/activin signaling functions as a sugar-sensing feedback loop to regulate digestive enzyme expression. Cell Rep. 9:336–48 [Google Scholar]
  34. Circu ML, Aw TY. 2011. Redox biology of the intestine. Free Radic. Res. 45:1245–66 [Google Scholar]
  35. Colombani J, Raisin S, Pantalacci S, Radimerski T, Montagne J, Leopold P. 2003. A nutrient sensor mechanism controls Drosophila growth. Cell 114:739–49 [Google Scholar]
  36. Cook KS, Min HY, Johnson D, Chaplinsky RJ, Flier JS. et al. 1987. Adipsin: a circulating serine protease homolog secreted by adipose tissue and sciatic nerve. Science 237:402–5 [Google Scholar]
  37. Cotman CW, Berchtold NC, Christie LA. 2007. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci. 30:464–72 [Google Scholar]
  38. Cremers CM, Jakob U. 2013. Oxidant sensing by reversible disulfide bond formation. J. Biol. Chem. 288:26489–96 [Google Scholar]
  39. Crooks DR, Natarajan TG, Jeong SY, Chen C, Park SY. et al. 2014. Elevated FGF21 secretion, PGC-1α and ketogenic enzyme expression are hallmarks of iron-sulfur cluster depletion in human skeletal muscle. Hum. Mol. Genet. 23:24–39 [Google Scholar]
  40. De Groot J, Harris GW. 1950. Hypothalmic control of the anterior pituitary gland and blood lymphocytes. J. Physiol. 111:335–46 [Google Scholar]
  41. Demontis F, Patel VK, Swindell WR, Perrimon N. 2014. Intertissue control of the nucleolus via a myokine-dependent longevity pathway. Cell Rep. 7:1481–94 [Google Scholar]
  42. Demontis F, Perrimon N. 2010. FOXO/4E-BP signaling in Drosophila muscles regulates organism-wide proteostasis during aging. Cell 143:813–25 [Google Scholar]
  43. Deng Y, Wang ZV, Tao C, Gao N, Holland WL. et al. 2013. The Xbp1s/GalE axis links ER stress to postprandial hepatic metabolism. J. Clin. Invest. 123:455–68 [Google Scholar]
  44. Dinas PC, Koutedakis Y, Flouris AD. 2011. Effects of exercise and physical activity on depression. Ir. J. Med. Sci. 180:319–25 [Google Scholar]
  45. Doroudgar S, Thuerauf DJ, Marcinko MC, Belmont PJ, Glembotski CC. 2009. Ischemia activates the ATF6 branch of the endoplasmic reticulum stress response. J. Biol. Chem. 284:29735–45 [Google Scholar]
  46. Droujinine IA, Perrimon N. 2013. Defining the interorgan communication network: systemic coordination of organismal cellular processes under homeostasis and localized stress. Front. Cell Infect. Microbiol. 3:82 [Google Scholar]
  47. Durieux J, Wolff S, Dillin A. 2011. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 144:79–91 [Google Scholar]
  48. Dutchak PA, Katafuchi T, Bookout AL, Choi JH, Yu RT. et al. 2012. Fibroblast growth factor-21 regulates PPARγ activity and the antidiabetic actions of thiazolidinediones. Cell 148:556–67 [Google Scholar]
  49. Egerman MA, Cadena SM, Gilbert JA, Meyer A, Nelson HN. et al. 2015. GDF11 increases with age and inhibits skeletal muscle regeneration. Cell Metab. 22:164–74 [Google Scholar]
  50. Elkasrawy MN, Hamrick MW. 2010. Myostatin (GDF-8) as a key factor linking muscle mass and bone structure. J. Musculoskelet. Neuronal Interact. 10:56–63 [Google Scholar]
  51. Ellingsgaard H, Hauselmann I, Schuler B, Habib AM, Baggio LL. et al. 2011. Interleukin-6 enhances insulin secretion by increasing glucagon-like peptide-1 secretion from L cells and α cells. Nat. Med. 17:1481–89 [Google Scholar]
  52. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2:953–71 [Google Scholar]
  53. Ferguson GB, Martinez-Agosto JA. 2014. Yorkie and Scalloped signaling regulates Notch-dependent lineage specification during Drosophila hematopoiesis. Curr. Biol. 24:2665–72 [Google Scholar]
  54. Figueroa-Clarevega A, Bilder D. 2015. Malignant Drosophila tumors interrupt insulin signaling to induce cachexia-like wasting. Dev. Cell 33:47–55 [Google Scholar]
  55. Fisher FM, Chui PC, Antonellis PJ, Bina HA, Kharitonenkov A. et al. 2010. Obesity is a fibroblast growth factor 21 (FGF21)-resistant state. Diabetes 59:2781–89 [Google Scholar]
  56. Fisher FM, Kleiner S, Douris N, Fox EC, Mepani RJ. et al. 2012. FGF21 regulates PGC-1α and browning of white adipose tissues in adaptive thermogenesis. Genes Dev. 26:271–81 [Google Scholar]
  57. Franchimont N, Wertz S, Malaise M. 2005. Interleukin-6: an osteotropic factor influencing bone formation?. Bone 37:601–6 [Google Scholar]
  58. Frizzell N, Rajesh M, Jepson MJ, Nagai R, Carson JA. et al. 2009. Succination of thiol groups in adipose tissue proteins in diabetes: succination inhibits polymerization and secretion of adiponectin. J. Biol. Chem. 284:25772–81 [Google Scholar]
  59. Frost RA, Nystrom GJ, Lang CH. 2006. Multiple Toll-like receptor ligands induce an IL-6 transcriptional response in skeletal myocytes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290:R773–84 [Google Scholar]
  60. Garcia SM, Casanueva MO, Silva MC, Amaral MD, Morimoto RI. 2007. Neuronal signaling modulates protein homeostasis in Caenorhabditis elegans post-synaptic muscle cells. Genes Dev. 21:3006–16 [Google Scholar]
  61. Geminard C, Rulifson EJ, Leopold P. 2009. Remote control of insulin secretion by fat cells in Drosophila. Cell Metab. 10:199–207 [Google Scholar]
  62. Ghosh A, Rideout EJ, Grewal SS. 2014. TIF-IA-dependent regulation of ribosome synthesis in Drosophila muscle is required to maintain systemic insulin signaling and larval growth. PLOS Genet. 10:e1004750 [Google Scholar]
  63. Ghosh AC, O'Connor MB. 2014. Systemic Activin signaling independently regulates sugar homeostasis, cellular metabolism, and pH balance in Drosophila melanogaster. PNAS 111:5729–34 [Google Scholar]
  64. Glembotski CC, Thuerauf DJ, Huang C, Vekich JA, Gottlieb RA, Doroudgar S. 2012. Mesencephalic astrocyte-derived neurotrophic factor protects the heart from ischemic damage and is selectively secreted upon sarco/endoplasmic reticulum calcium depletion. J. Biol. Chem. 287:25893–904 [Google Scholar]
  65. Gnad T, Scheibler S, von Kugelgen I, Scheele C, Kilic A. et al. 2014. Adenosine activates brown adipose tissue and recruits beige adipocytes via A2A receptors. Nature 516:395–99 [Google Scholar]
  66. Gough DJ, Corlett A, Schlessinger K, Wegrzyn J, Larner AC, Levy DE. 2009. Mitochondrial STAT3 supports Ras-dependent oncogenic transformation. Science 324:1713–16 [Google Scholar]
  67. Groitl B, Jakob U. 2014. Thiol-based redox switches. Biochim. Biophys. Acta 1844:1335–43 [Google Scholar]
  68. Guillemin R, Rosenberg B. 1955. Humoral hypothalamic control of anterior pituitary: a study with combined tissue cultures. Endocrinology 57:599–607 [Google Scholar]
  69. Hamrick MW, McNeil PL, Patterson SL. 2010. Role of muscle-derived growth factors in bone formation. J. Musculoskelet Neuronal Interact 10:64–70 [Google Scholar]
  70. Han MS, Jung DY, Morel C, Lakhani SA, Kim JK. et al. 2013. JNK expression by macrophages promotes obesity-induced insulin resistance and inflammation. Science 339:218–22 [Google Scholar]
  71. Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell 144:646–74 [Google Scholar]
  72. Handke B, Poernbacher I, Goetze S, Ahrens CH, Omasits U. et al. 2013. The hemolymph proteome of fed and starved Drosophila larvae. PLOS ONE 8:e67208 [Google Scholar]
  73. Hara K, Boutin P, Mori Y, Tobe K, Dina C. et al. 2002. Genetic variation in the gene encoding adiponectin is associated with an increased risk of type 2 diabetes in the Japanese population. Diabetes 51:536–40 [Google Scholar]
  74. Heijmans J, van Lidth de Jeude JF, Koo BK, Rosekrans SL, Wielenga MC. et al. 2013. ER stress causes rapid loss of intestinal epithelial stemness through activation of the unfolded protein response. Cell Rep. 3:1128–39 [Google Scholar]
  75. Hickey DA, Benkel B. 1982. Regulation of amylase activity in Drosophila melanogaster: effects of dietary carbohydrate. Biochem. Genet. 20:1117–29 [Google Scholar]
  76. Hochmuth CE, Biteau B, Bohmann D, Jasper H. 2011. Redox regulation by Keap1 and Nrf2 controls intestinal stem cell proliferation in Drosophila. Cell Stem Cell 8:188–99 [Google Scholar]
  77. Holland WL, Adams AC, Brozinick JT, Bui HH, Miyauchi Y. et al. 2013. An FGF21-adiponectin-ceramide axis controls energy expenditure and insulin action in mice. Cell Metab. 17:790–97 [Google Scholar]
  78. Hondares E, Iglesias R, Giralt A, Gonzalez FJ, Giralt M. et al. 2011. Thermogenic activation induces FGF21 expression and release in brown adipose tissue. J. Biol. Chem. 286:12983–90 [Google Scholar]
  79. Hotta Y, Nakamura H, Konishi M, Murata Y, Takagi H. et al. 2009. Fibroblast growth factor 21 regulates lipolysis in white adipose tissue but is not required for ketogenesis and triglyceride clearance in liver. Endocrinology 150:4625–33 [Google Scholar]
  80. Hull-Thompson J, Muffat J, Sanchez D, Walker DW, Benzer S. et al. 2009. Control of metabolic homeostasis by stress signaling is mediated by the lipocalin NLaz. PLOS Genet. 5:e1000460 [Google Scholar]
  81. Itoh N. 2014. FGF21 as a hepatokine, adipokine, and myokine in metabolism and diseases. Front. Endocrinol. 5:107 [Google Scholar]
  82. Jorgensen LH, Petersson SJ, Sellathurai J, Andersen DC, Thayssen S. et al. 2009. Secreted protein acidic and rich in cysteine (SPARC) in human skeletal muscle. J. Histochem. Cytochem. 57:29–39 [Google Scholar]
  83. Kannan K, Fridell YW. 2013. Functional implications of Drosophila insulin-like peptides in metabolism, aging, and dietary restriction. Front. Physiol. 4:288 [Google Scholar]
  84. Karsenty G. 2011. Bone endocrine regulation of energy metabolism and male reproduction. C R Biol. 334:720–24 [Google Scholar]
  85. Kaser A, Lee AH, Franke A, Glickman JN, Zeissig S. et al. 2008. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 134:743–56 [Google Scholar]
  86. Katewa SD, Demontis F, Kolipinski M, Hubbard A, Gill MS. et al. 2012. Intramyocellular fatty-acid metabolism plays a critical role in mediating responses to dietary restriction in Drosophila melanogaster. Cell Metab. 16:97–103 [Google Scholar]
  87. Keipert S, Ost M, Johann K, Imber F, Jastroch M. et al. 2014. Skeletal muscle mitochondrial uncoupling drives endocrine cross-talk through the induction of FGF21 as a myokine. Am. J. Physiol. Endocrinol. Metab. 306:E469–82 [Google Scholar]
  88. Kernbauer E, Ding Y, Cadwell K. 2014. An enteric virus can replace the beneficial function of commensal bacteria. Nature 516:94–98 [Google Scholar]
  89. Killip LE, Grewal SS. 2012. DREF is required for cell and organismal growth in Drosophila and functions downstream of the nutrition/TOR pathway. Dev. Biol. 371:191–202 [Google Scholar]
  90. Kim KH, Jeong YT, Oh H, Kim SH, Cho JM. et al. 2013. Autophagy deficiency leads to protection from obesity and insulin resistance by inducing Fgf21 as a mitokine. Nat. Med. 19:83–92 [Google Scholar]
  91. Kim KH, Lee MS. 2014. FGF21 as a stress hormone: the roles of FGF21 in stress adaptation and the treatment of metabolic diseases. Diabetes Metab. J. 38:245–51 [Google Scholar]
  92. Kim SK, Rulifson EJ. 2004. Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells. Nature 431:316–20 [Google Scholar]
  93. Kir S, White JP, Kleiner S, Kazak L, Cohen P. et al. 2014. Tumour-derived PTH-related protein triggers adipose tissue browning and cancer cachexia. Nature 513:100–04 [Google Scholar]
  94. Kishimoto T. 2005. Interleukin-6: from basic science to medicine—40 years in immunology. Annu. Rev. Immunol. 23:1–21 [Google Scholar]
  95. Koh EH, Park JY, Park HS, Jeon MJ, Ryu JW. et al. 2007. Essential role of mitochondrial function in adiponectin synthesis in adipocytes. Diabetes 56:2973–81 [Google Scholar]
  96. Kwak SJ, Hong SH, Bajracharya R, Yang SY, Lee KS, Yu K. 2013. Drosophila adiponectin receptor in insulin producing cells regulates glucose and lipid metabolism by controlling insulin secretion. PLOS ONE 8:e68641 [Google Scholar]
  97. Kwon Y, Song W, Droujinine IA, Hu Y, Asara JM, Perrimon N. 2015. Systemic organ wasting induced by localized expression of the secreted insulin/IGF antagonist ImpL2. Dev. Cell 33:36–46 [Google Scholar]
  98. Laws KM, Sampson LL, Drummond-Barbosa D. 2015. Insulin-independent role of adiponectin receptor signaling in Drosophila germline stem cell maintenance. Dev. Biol. 399:226–36 [Google Scholar]
  99. Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD. et al. 2007. Endocrine regulation of energy metabolism by the skeleton. Cell 130:456–69 [Google Scholar]
  100. Lee WJ, Brey PT. 2013. How microbiomes influence metazoan development: insights from history and Drosophila modeling of gut-microbe interactions. Annu. Rev. Cell Dev. Biol. 29:571–92 [Google Scholar]
  101. Li YP, Stashenko P. 1992. Proinflammatory cytokines tumor necrosis factor-α and IL-6, but not IL-1, down-regulate the osteocalcin gene promoter. J. Immunol. 148:788–94 [Google Scholar]
  102. Lin Z, Tian H, Lam KS, Lin S, Hoo RC. et al. 2013. Adiponectin mediates the metabolic effects of FGF21 on glucose homeostasis and insulin sensitivity in mice. Cell Metab. 17:779–89 [Google Scholar]
  103. Liu M, Xiang R, Wilk SA, Zhang N, Sloane LB. et al. 2012. Fat-specific DsbA-L overexpression promotes adiponectin multimerization and protects mice from diet-induced obesity and insulin resistance. Diabetes 61:2776–86 [Google Scholar]
  104. Lo JC, Ljubicic S, Leibiger B, Kern M, Leibiger IB. et al. 2014. Adipsin is an adipokine that improves β cell function in diabetes. Cell 158:41–53 [Google Scholar]
  105. Loffredo FS, Steinhauser ML, Jay SM, Gannon J, Pancoast JR. et al. 2013. Growth differentiation factor 11 is a circulating factor that reverses age-related cardiac hypertrophy. Cell 153:828–39 [Google Scholar]
  106. Mabery EM, Schneider DS. 2010. The Drosophila TNF ortholog eiger is required in the fat body for a robust immune response. J. Innate Immun. 2:371–78 [Google Scholar]
  107. Mai K, Andres J, Biedasek K, Weicht J, Bobbert T. et al. 2009. Free fatty acids link metabolism and regulation of the insulin-sensitizing fibroblast growth factor-21. Diabetes 58:1532–38 [Google Scholar]
  108. Mai K, Bobbert T, Groth C, Assmann A, Meinus S. et al. 2010. Physiological modulation of circulating FGF21: relevance of free fatty acids and insulin. Am. J. Physiol. Endocrinol. Metab. 299:E126–30 [Google Scholar]
  109. Marshall L, Rideout EJ, Grewal SS. 2012. Nutrient/TOR-dependent regulation of RNA polymerase III controls tissue and organismal growth in Drosophila. EMBO J. 31:1916–30 [Google Scholar]
  110. Martin JF, Hersperger E, Simcox A, Shearn A. 2000. minidiscs encodes a putative amino acid transporter subunit required non-autonomously for imaginal cell proliferation. Mech. Dev. 92:155–67 [Google Scholar]
  111. Mattson MP. 2012. Energy intake and exercise as determinants of brain health and vulnerability to injury and disease. Cell Metab. 16:706–22 [Google Scholar]
  112. Mondal BC, Mukherjee T, Mandal L, Evans CJ, Sinenko SA. et al. 2011. Interaction between differentiating cell- and niche-derived signals in hematopoietic progenitor maintenance. Cell 147:1589–600 [Google Scholar]
  113. Mukherjee T, Kim WS, Mandal L, Banerjee U. 2011. Interaction between Notch and Hif-α in development and survival of Drosophila blood cells. Science 332:1210–13 [Google Scholar]
  114. Musselman LP, Fink JL, Narzinski K, Ramachandran PV, Hathiramani SS. et al. 2011. A high-sugar diet produces obesity and insulin resistance in wild-type Drosophila. Dis. Model. Mech. 4:842–49 [Google Scholar]
  115. Nasrallah CM, Horvath TL. 2014. Mitochondrial dynamics in the central regulation of metabolism. Nat. Rev. Endocrinol. 10:650–58 [Google Scholar]
  116. Nassel DR, Kubrak OI, Liu Y, Luo J, Lushchak OV. 2013. Factors that regulate insulin producing cells and their output in Drosophila. Front. Physiol. 4:252 [Google Scholar]
  117. Niederreiter L, Fritz TM, Adolph TE, Krismer AM, Offner FA. et al. 2013. ER stress transcription factor Xbp1 suppresses intestinal tumorigenesis and directs intestinal stem cells. J. Exp. Med. 210:2041–56 [Google Scholar]
  118. Nielsen AR, Mounier R, Plomgaard P, Mortensen OH, Penkowa M. et al. 2007. Expression of interleukin-15 in human skeletal muscle effect of exercise and muscle fibre type composition. J. Physiol. 584:305–12 [Google Scholar]
  119. Odegaard JI, Chawla A. 2011. Alternative macrophage activation and metabolism. Annu. Rev. Pathol. 6:275–97 [Google Scholar]
  120. Okamoto N, Nakamori R, Murai T, Yamauchi Y, Masuda A, Nishimura T. 2013. A secreted decoy of InR antagonizes insulin/IGF signaling to restrict body growth in Drosophila. Genes Dev. 27:87–97 [Google Scholar]
  121. Okamoto N, Yamanaka N, Yagi Y, Nishida Y, Kataoka H. et al. 2009. A fat body–derived IGF-like peptide regulates postfeeding growth in Drosophila. Dev. Cell 17:885–91 [Google Scholar]
  122. Owusu-Ansah E, Banerjee U. 2009. Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461:537–41 [Google Scholar]
  123. Owusu-Ansah E, Perrimon N. 2014. Modeling metabolic homeostasis and nutrient sensing in Drosophila: implications for aging and metabolic diseases. Dis. Model. Mech. 7:343–50 [Google Scholar]
  124. Owusu-Ansah E, Song W, Perrimon N. 2013. Muscle mitohormesis promotes longevity via systemic repression of insulin signaling. Cell 155:699–712 [Google Scholar]
  125. Ozcan L, Ergin AS, Lu A, Chung J, Sarkar S. et al. 2009. Endoplasmic reticulum stress plays a central role in development of leptin resistance. Cell Metab. 9:35–51 [Google Scholar]
  126. Pajvani UB, Du X, Combs TP, Berg AH, Rajala MW. et al. 2003. Structure-function studies of the adipocyte-secreted hormone Acrp30/adiponectin. Implications for metabolic regulation and bioactivity. J. Biol. Chem. 278:9073–85 [Google Scholar]
  127. Pajvani UB, Hawkins M, Combs TP, Rajala MW, Doebber T. et al. 2004. Complex distribution, not absolute amount of adiponectin, correlates with thiazolidinedione-mediated improvement in insulin sensitivity. J. Biol. Chem. 279:12152–62 [Google Scholar]
  128. Parisi F, Stefanatos RK, Strathdee K, Yu Y, Vidal M. 2014. Transformed epithelia trigger non-tissue-autonomous tumor suppressor response by adipocytes via activation of Toll and Eiger/TNF signaling. Cell Rep. 6:855–67 [Google Scholar]
  129. Pasco MY, Leopold P. 2012. High sugar-induced insulin resistance in Drosophila relies on the lipocalin Neural Lazarillo. PLOS ONE 7:e36583 [Google Scholar]
  130. Patel H, Shaw SG, Shi-Wen X, Abraham D, Baker DM, Tsui JC. 2012. Toll-like receptors in ischaemia and its potential role in the pathophysiology of muscle damage in critical limb ischaemia. Cardiol. Res. Pract. 2012:121237 [Google Scholar]
  131. Patti GJ, Tautenhahn R, Johannsen D, Kalisiak E, Ravussin E. et al. 2014. Meta-analysis of global metabolomic data identifies metabolites associated with life-span extension. Metabolomics 10:737–43 [Google Scholar]
  132. Pedersen BK, Febbraio MA. 2012. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat. Rev. Endocrinol. 8:457–65 [Google Scholar]
  133. Perrimon N, Ni JQ, Perkins L. 2010. In vivo RNAi: today and tomorrow. Cold Spring Harb. Perspect. Biol. 2:a003640 [Google Scholar]
  134. Prahlad V, Cornelius T, Morimoto RI. 2008. Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons. Science 320:811–14 [Google Scholar]
  135. Prahlad V, Morimoto RI. 2011. Neuronal circuitry regulates the response of Caenorhabditis elegans to misfolded proteins. PNAS 108:14204–9 [Google Scholar]
  136. Rajan A, Perrimon N. 2012. Drosophila cytokine unpaired 2 regulates physiological homeostasis by remotely controlling insulin secretion. Cell 151:123–37 [Google Scholar]
  137. Rao RR, Long JZ, White JP, Svensson KJ, Lou J. et al. 2014. Meteorin-like is a hormone that regulates immune-adipose interactions to increase beige fat thermogenesis. Cell 157:1279–91 [Google Scholar]
  138. Ricklin D, Hajishengallis G, Yang K, Lambris JD. 2010. Complement: a key system for immune surveillance and homeostasis. Nat. Immunol. 11:785–97 [Google Scholar]
  139. Ristow M, Zarse K. 2010. How increased oxidative stress promotes longevity and metabolic health: the concept of mitochondrial hormesis (mitohormesis). Exp. Gerontol. 45:410–18 [Google Scholar]
  140. Roberts LD, Bostrom P, O'Sullivan JF, Schinzel RT, Lewis GD. et al. 2014. β-Aminoisobutyric acid induces browning of white fat and hepatic β-oxidation and is inversely correlated with cardiometabolic risk factors. Cell Metab. 19:96–108 [Google Scholar]
  141. Rodenfels J, Lavrynenko O, Ayciriex S, Sampaio JL, Carvalho M. et al. 2014. Production of systemically circulating Hedgehog by the intestine couples nutrition to growth and development. Genes Dev. 28:2636–51 [Google Scholar]
  142. Rosen BS, Cook KS, Yaglom J, Groves DL, Volanakis JE. et al. 1989. Adipsin and complement factor D activity: an immune-related defect in obesity. Science 244:1483–87 [Google Scholar]
  143. Ruas JL, White JP, Rao RR, Kleiner S, Brannan KT. et al. 2012. A PGC-1α isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell 151:1319–31 [Google Scholar]
  144. Saffran M, Schally AV, Benfey BG. 1955. Stimulation of the release of corticotropin from the adenohypophysis by a neurohypophysial factor. Endocrinology 57:439–44 [Google Scholar]
  145. Schmid MR, Anderl I, Vesala L, Vanha-aho LM, Deng XJ. et al. 2014. Control of Drosophila blood cell activation via Toll signaling in the fat body. PLOS ONE 9:e102568 [Google Scholar]
  146. Schraw T, Wang ZV, Halberg N, Hawkins M, Scherer PE. 2008. Plasma adiponectin complexes have distinct biochemical characteristics. Endocrinology 149:2270–82 [Google Scholar]
  147. Serrano AL, Baeza-Raja B, Perdiguero E, Jardi M, Munoz-Canoves P. 2008. Interleukin-6 is an essential regulator of satellite cell–mediated skeletal muscle hypertrophy. Cell Metab. 7:33–44 [Google Scholar]
  148. Shemesh N, Shai N, Ben-Zvi A. 2013. Germline stem cell arrest inhibits the collapse of somatic proteostasis early in Caenorhabditis elegans adulthood. Aging Cell 12:814–22 [Google Scholar]
  149. Shim J, Mukherjee T, Banerjee U. 2012. Direct sensing of systemic and nutritional signals by haematopoietic progenitors in Drosophila. Nat. Cell Biol. 14:394–400 [Google Scholar]
  150. Shim J, Mukherjee T, Mondal BC, Liu T, Young GC. et al. 2013. Olfactory control of blood progenitor maintenance. Cell 155:1141–53 [Google Scholar]
  151. Sinenko SA, Shim J, Banerjee U. 2012. Oxidative stress in the haematopoietic niche regulates the cellular immune response in Drosophila. EMBO Rep. 13:83–89 [Google Scholar]
  152. Sinha M, Jang YC, Oh J, Khong D, Wu EY. et al. 2014. Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science 344:649–52 [Google Scholar]
  153. Slaidina M, Delanoue R, Gronke S, Partridge L, Leopold P. 2009. A Drosophila insulin-like peptide promotes growth during nonfeeding states. Dev. Cell 17:874–84 [Google Scholar]
  154. Song W, Veenstra JA, Perrimon N. 2014. Control of lipid metabolism by tachykinin in Drosophila. Cell Rep. 9:40–47 [Google Scholar]
  155. Suomalainen A, Elo JM, Pietilainen KH, Hakonen AH, Sevastianova K. et al. 2011. FGF-21 as a biomarker for muscle-manifesting mitochondrial respiratory chain deficiencies: a diagnostic study. Lancet Neurol. 10:806–18 [Google Scholar]
  156. Tadimalla A, Belmont PJ, Thuerauf DJ, Glassy MS, Martindale JJ. et al. 2008. Mesencephalic astrocyte-derived neurotrophic factor is an ischemia-inducible secreted endoplasmic reticulum stress response protein in the heart. Circ. Res. 103:1249–58 [Google Scholar]
  157. Tapia PC. 2006. Sublethal mitochondrial stress with an attendant stoichiometric augmentation of reactive oxygen species may precipitate many of the beneficial alterations in cellular physiology produced by caloric restriction, intermittent fasting, exercise and dietary phytonutrients: “mitohormesis” for health and vitality. Med. Hypotheses 66:832–43 [Google Scholar]
  158. Targownik LE, Bernstein CN, Leslie WD. 2013. Inflammatory bowel disease and the risk of osteoporosis and fracture. Maturitas 76:315–19 [Google Scholar]
  159. Taylor RC, Dillin A. 2013. XBP-1 is a cell-nonautonomous regulator of stress resistance and longevity. Cell 153:1435–47 [Google Scholar]
  160. Termine JD, Kleinman HK, Whitson SW, Conn KM, McGarvey ML, Martin GR. 1981. Osteonectin, a bone-specific protein linking mineral to collagen. Cell 26:99–105 [Google Scholar]
  161. Thomas CM, Versalovic J. 2010. Probiotics-host communication: modulation of signaling pathways in the intestine. Gut Microbes 1:148–63 [Google Scholar]
  162. Thuerauf DJ, Marcinko M, Belmont PJ, Glembotski CC. 2007. Effects of the isoform-specific characteristics of ATF6α and ATF6β on endoplasmic reticulum stress response gene expression and cell viability. J. Biol. Chem. 282:22865–78 [Google Scholar]
  163. Thuerauf DJ, Marcinko M, Gude N, Rubio M, Sussman MA, Glembotski CC. 2006. Activation of the unfolded protein response in infarcted mouse heart and hypoxic cultured cardiac myocytes. Circ. Res. 99:275–82 [Google Scholar]
  164. Thuerauf DJ, Morrison L, Glembotski CC. 2004. Opposing roles for ATF6α and ATF6β in endoplasmic reticulum stress response gene induction. J. Biol. Chem. 279:21078–84 [Google Scholar]
  165. Tsao TS, Murrey HE, Hug C, Lee DH, Lodish HF. 2002. Oligomerization state–dependent activation of NF-κB signaling pathway by adipocyte complement-related protein of 30 kDa (Acrp30). J. Biol. Chem. 277:29359–62 [Google Scholar]
  166. Tsao TS, Tomas E, Murrey HE, Hug C, Lee DH. et al. 2003. Role of disulfide bonds in Acrp30/adiponectin structure and signaling specificity. Different oligomers activate different signal transduction pathways. J. Biol. Chem. 278:50810–17 [Google Scholar]
  167. Tyynismaa H, Carroll CJ, Raimundo N, Ahola-Erkkila S, Wenz T. et al. 2010. Mitochondrial myopathy induces a starvation-like response. Hum. Mol. Genet. 19:3948–58 [Google Scholar]
  168. Udelsman R, Blake MJ, Stagg CA, Holbrook NJ. 1994. Endocrine control of stress-induced heat shock protein 70 expression in vivo. Surgery 115:611–16 [Google Scholar]
  169. Ulgherait M, Rana A, Rera M, Graniel J, Walker DW. 2014. AMPK modulates tissue and organismal aging in a non-cell-autonomous manner. Cell Rep. 8:1767–80 [Google Scholar]
  170. van Hall G, Steensberg A, Sacchetti M, Fischer C, Keller C. et al. 2003. Interleukin-6 stimulates lipolysis and fat oxidation in humans. J. Clin. Endocrinol. Metab. 88:3005–10 [Google Scholar]
  171. Verras M, Papandreou I, Lim AL, Denko NC. 2008. Tumor hypoxia blocks Wnt processing and secretion through the induction of endoplasmic reticulum stress. Mol. Cell. Biol. 28:7212–24 [Google Scholar]
  172. Waki H, Yamauchi T, Kamon J, Ito Y, Uchida S. et al. 2003. Impaired multimerization of human adiponectin mutants associated with diabetes. Molecular structure and multimer formation of adiponectin. J. Biol. Chem. 278:40352–63 [Google Scholar]
  173. Wang CH, Wang CC, Huang HC, Wei YH. 2013. Mitochondrial dysfunction leads to impairment of insulin sensitivity and adiponectin secretion in adipocytes. FEBS J. 280:1039–50 [Google Scholar]
  174. Wang L, Zeng X, Ryoo HD, Jasper H. 2014. Integration of UPRER and oxidative stress signaling in the control of intestinal stem cell proliferation. PLOS Genet. 10:e1004568 [Google Scholar]
  175. Whitham M, Chan MH, Pal M, Matthews VB, Prelovsek O. et al. 2012. Contraction-induced interleukin-6 gene transcription in skeletal muscle is regulated by c-Jun terminal kinase/activator protein-1. J. Biol. Chem. 287:10771–79 [Google Scholar]
  176. Williams KW, Elmquist JK. 2012. From neuroanatomy to behavior: central integration of peripheral signals regulating feeding behavior. Nat. Neurosci. 15:1350–55 [Google Scholar]
  177. Williams KW, Liu T, Kong X, Fukuda M, Deng Y. et al. 2014. Xbp1s in Pomc neurons connects ER stress with energy balance and glucose homeostasis. Cell Metab. 20:471–82 [Google Scholar]
  178. Won JC, Jang PG, Namkoong C, Koh EH, Kim SK. et al. 2009. Central administration of an endoplasmic reticulum stress inducer inhibits the anorexigenic effects of leptin and insulin. Obesity 17:1861–65 [Google Scholar]
  179. Woodcock KJ, Kierdorf K, Pouchelon CA, Vivancos V, Dionne MS, Geissmann F. 2014. Macrophage-derived upd3 cytokine causes impaired glucose homeostasis and reduced lifespan in Drosophila fed a lipid-rich diet. Immunity 42:133–44 [Google Scholar]
  180. Wrann CD, White JP, Salogiannnis J, Laznik-Bogoslavski D, Wu J. et al. 2013. Exercise induces hippocampal BDNF through a PGC-1α/FNDC5 pathway. Cell Metab. 18:649–59 [Google Scholar]
  181. Wu SC, Liao CW, Pan RL, Juang JL. 2012. Infection-induced intestinal oxidative stress triggers organ-to-organ immunological communication in Drosophila. Cell Host Microbe 11:410–17 [Google Scholar]
  182. Zhang X, Zhang G, Zhang H, Karin M, Bai H, Cai D. 2008. Hypothalamic IKKβ/NF-κB and ER stress link overnutrition to energy imbalance and obesity. Cell 135:61–73 [Google Scholar]
  183. Zhang Y, Li R, Meng Y, Li S, Donelan W. et al. 2014. Irisin stimulates browning of white adipocytes through mitogen-activated protein kinase p38 MAP kinase and ERK MAP kinase signaling. Diabetes 63:514–25 [Google Scholar]
  184. Zhou L, Liu F. 2010. Autophagy: roles in obesity-induced ER stress and adiponectin downregulation in adipocytes. Autophagy 6:1196–97 [Google Scholar]
  185. Zhou L, Liu M, Zhang J, Chen H, Dong LQ, Liu F. 2010. DsbA-L alleviates endoplasmic reticulum stress-induced adiponectin downregulation. Diabetes 59:2809–16 [Google Scholar]
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