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• W2969885938 abstract "Secreted molecules coordinate organ function. In a recent issue of Cell, Hudry et al., 2019Hudry B. Goeij E.d. Mineo A. Gaspar P. Hadjieconomou D. Studd C. Mokochinski J.B. Kramer H.B. Plaçais P.-Y. Preat T. et al.Sex differences in intestinal carbohydrate metabolism promote food intake and sperm maturation.Cell. 2019; 178: 901-918Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar uncover a Drosophila testis-midgut interaction via cytokine and citrate signaling that regulates intestinal metabolism, spermatogenesis, and food intake. This impressive study is a striking example of the role of spatial organization in sex-specific interorgan communication. Secreted molecules coordinate organ function. In a recent issue of Cell, Hudry et al., 2019Hudry B. Goeij E.d. Mineo A. Gaspar P. Hadjieconomou D. Studd C. Mokochinski J.B. Kramer H.B. Plaçais P.-Y. Preat T. et al.Sex differences in intestinal carbohydrate metabolism promote food intake and sperm maturation.Cell. 2019; 178: 901-918Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar uncover a Drosophila testis-midgut interaction via cytokine and citrate signaling that regulates intestinal metabolism, spermatogenesis, and food intake. This impressive study is a striking example of the role of spatial organization in sex-specific interorgan communication. Organs are specialized, interdependent, and regulated by an interorgan communication network (ICN) of secreted molecules that are beginning to be revealed from work in both vertebrates and invertebrates (Droujinine and Perrimon, 2016Droujinine I.A. Perrimon N. Interorgan communication pathways in physiology: focus on Drosophila.Annu. Rev. Genet. 2016; 50: 539-570Crossref PubMed Scopus (111) Google Scholar). For instance, to regulate growth, metabolism, immunity, and digestive enzymes, the Drosophila gut secretes hedgehog, insulin growth factor binding protein-like ImpL2, PDGF- and VEGF-related factor 1 (Pvf1), activin, and, from gut-associated corpora cardiaca, limostatin and adipokinetic hormone and senses activin-like dawdle (Daw) and peptidoglycan recognition proteins (PGRPs) (Droujinine and Perrimon, 2016Droujinine I.A. Perrimon N. Interorgan communication pathways in physiology: focus on Drosophila.Annu. Rev. Genet. 2016; 50: 539-570Crossref PubMed Scopus (111) Google Scholar, Rodenfels et al., 2014Rodenfels J. Lavrynenko O. Ayciriex S. Sampaio J.L. Carvalho M. Shevchenko A. Eaton S. Production of systemically circulating Hedgehog by the intestine couples nutrition to growth and development.Genes Dev. 2014; 28: 2636-2651Crossref PubMed Scopus (70) Google Scholar, Song et al., 2019Song W. Kir S. Hong S. Hu Y. Wang X. Binari R. Tang H.-W. Chung V. Banks A.S. Spiegelman B. et al.Tumor-derived ligands trigger tumor growth and host wasting via differential MEK activation.Dev. Cell. 2019; 48: 277-286Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar). The midgut consists of multiple interacting cell types: intestinal stem cells (ISCs) and differentiated enterocytes (ECs) and enteroendocrine cells. Interestingly, male and female guts show sex differences; for example, there is more ISC proliferation in female guts than in male guts, and ECs located in the posterior R4 region of the male midgut show increased expression of genes involved in carbohydrate metabolism (Hudry et al., 2016Hudry B. Khadayate S. Miguel-Aliaga I. The sexual identity of adult intestinal stem cells controls organ size and plasticity.Nature. 2016; 530: 344-348Crossref PubMed Scopus (107) Google Scholar). Interestingly, while the sex determination pathway controls differences in ISC proliferation cell autonomously, male-specific expression of genes involved in sugar metabolism does not depend on the sex of the ECs themselves. Puzzled by this observation, Hudry et al., 2019Hudry B. Goeij E.d. Mineo A. Gaspar P. Hadjieconomou D. Studd C. Mokochinski J.B. Kramer H.B. Plaçais P.-Y. Preat T. et al.Sex differences in intestinal carbohydrate metabolism promote food intake and sperm maturation.Cell. 2019; 178: 901-918Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar observed that the apical tip of the testes and the posterior R4 region of the midgut are in close proximity to one another and made the remarkable hypothesis that signaling from the male somatic gonad may be responsible for the pattern of expression of sugar genes in the male gut. In a search for such a signal, they found that the testis soma produces the cytokine Upd1, which induces JAK-STAT signaling in the R4 region of the midgut, which is in turn essential for sugar gene expression. In determining the physiological consequences of the testis-gut interaction, Hudry et al., 2019Hudry B. Goeij E.d. Mineo A. Gaspar P. Hadjieconomou D. Studd C. Mokochinski J.B. Kramer H.B. Plaçais P.-Y. Preat T. et al.Sex differences in intestinal carbohydrate metabolism promote food intake and sperm maturation.Cell. 2019; 178: 901-918Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar found that intestinal glucose metabolism and JAK-STAT signaling affect food intake through extracellular citrate. This metabolite was found to be downstream of glycolysis, pyruvate, and the pyruvate-citrate pathway and secreted from ECs and imported to neurons through the Indy channel. In addition, intestinal citrate production and uptake play a role in the testis soma to promote sperm maturation (Figure 1). These remarkable findings have significant implications for interorgan communication studies and raise a number of questions. The importance of citrate for spermatogenesis and food intake suggests that gonads may regulate metabolism to promote reproductive capacity (Hudry et al., 2019Hudry B. Goeij E.d. Mineo A. Gaspar P. Hadjieconomou D. Studd C. Mokochinski J.B. Kramer H.B. Plaçais P.-Y. Preat T. et al.Sex differences in intestinal carbohydrate metabolism promote food intake and sperm maturation.Cell. 2019; 178: 901-918Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar). Given that sexual dimorphism can be altered in adults and has significant effects on reproduction and feeding behavior, are there dietary or environmental cues affecting these carbohydrate metabolism-related phenomena? Other processes and cell types may be regulated by sexually dimorphic intracellular or extracellular cues. For instance, yolk proteins are expressed in female but not male midguts, and oxidative stress genes are increased in male R4 over female midguts. Also, enteroendocrine cells show male-biased Maltase-A3 glucoside hydrolase expression, suggesting that cell types other than ECs are regulated sex specifically (Hudry et al., 2019Hudry B. Goeij E.d. Mineo A. Gaspar P. Hadjieconomou D. Studd C. Mokochinski J.B. Kramer H.B. Plaçais P.-Y. Preat T. et al.Sex differences in intestinal carbohydrate metabolism promote food intake and sperm maturation.Cell. 2019; 178: 901-918Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar). Interestingly, in non-R4 gut regions in males or females, JAK-STAT signaling was neither necessary nor sufficient for carbohydrate metabolism gene expression, suggesting the involvement of factors unrelated to sex determination in these regions (Hudry et al., 2019Hudry B. Goeij E.d. Mineo A. Gaspar P. Hadjieconomou D. Studd C. Mokochinski J.B. Kramer H.B. Plaçais P.-Y. Preat T. et al.Sex differences in intestinal carbohydrate metabolism promote food intake and sperm maturation.Cell. 2019; 178: 901-918Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar). Broadly, this work has implications for interorgan regulation of sexually dimorphic phenotypes. Reproduction in female flies regulates motility, food intake, lipid metabolism, and lifespan, suggesting that gonads may produce additional physiologically significant interorgan factors (Avila et al., 2011Avila F.W. Sirot L.K. LaFlamme B.A. Rubinstein C.D. Wolfner M.F. Insect seminal fluid proteins: identification and function.Annu. Rev. Entomol. 2011; 56: 21-40Crossref PubMed Scopus (605) Google Scholar, Reiff et al., 2015Reiff T. Jacobson J. Cognigni P. Antonello Z. Ballesta E. Tan K.J. Yew J.Y. Dominguez M. Miguel-Aliaga I. Endocrine remodelling of the adult intestine sustains reproduction in Drosophila.Elife. 2015; 4: e06930Crossref PubMed Scopus (127) Google Scholar). This paper also has relevance to mammals, in which cytokine production can differ between sexes (Couillard et al., 1997Couillard C. Mauriège P. Prud’homme D. Nadeau A. Tremblay A. Bouchard C. Després J.P. Plasma leptin concentrations: gender differences and associations with metabolic risk factors for cardiovascular disease.Diabetologia. 1997; 40: 1178-1184Crossref PubMed Scopus (126) Google Scholar). The work of Hudry et al., 2019Hudry B. Goeij E.d. Mineo A. Gaspar P. Hadjieconomou D. Studd C. Mokochinski J.B. Kramer H.B. Plaçais P.-Y. Preat T. et al.Sex differences in intestinal carbohydrate metabolism promote food intake and sperm maturation.Cell. 2019; 178: 901-918Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar is a striking example of a metabolite, in this case citrate, that is derived from a central metabolic process and affects systemic physiology. Systemic roles of other metabolites such as succinate have also been documented (Mills et al., 2018Mills E.L. Pierce K.A. Jedrychowski M.P. Garrity R. Winther S. Vidoni S. Yoneshiro T. Spinelli J.B. Lu G.Z. Kazak L. et al.Accumulation of succinate controls activation of adipose tissue thermogenesis.Nature. 2018; 560: 102-106Crossref PubMed Scopus (250) Google Scholar). While it is unclear how spermatogenesis is affected by citrate, it could function as a substrate for the TCA cycle or fatty acid generation, or affect histone acetylation (Hudry et al., 2019Hudry B. Goeij E.d. Mineo A. Gaspar P. Hadjieconomou D. Studd C. Mokochinski J.B. Kramer H.B. Plaçais P.-Y. Preat T. et al.Sex differences in intestinal carbohydrate metabolism promote food intake and sperm maturation.Cell. 2019; 178: 901-918Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar). Furthermore, the neural mechanisms of the effect of citrate on food intake are unclear. Finally, citrate also has a neuronal role in affecting food intake, although the precise neural populations that detect it and the intracellular mechanisms are unknown. The paper by Hudry et al., 2019Hudry B. Goeij E.d. Mineo A. Gaspar P. Hadjieconomou D. Studd C. Mokochinski J.B. Kramer H.B. Plaçais P.-Y. Preat T. et al.Sex differences in intestinal carbohydrate metabolism promote food intake and sperm maturation.Cell. 2019; 178: 901-918Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar will inspire studies of the roles of citrate on food intake and spermatogenesis in mammals. The spatial proximity of the testis to the gut R4 region is likely to be physiologically significant, as male JAK-STAT activity is adjacent to the testis tip and citrate concentrations are regulated in the gut and testis, but not in the hemolymph (Hudry et al., 2019Hudry B. Goeij E.d. Mineo A. Gaspar P. Hadjieconomou D. Studd C. Mokochinski J.B. Kramer H.B. Plaçais P.-Y. Preat T. et al.Sex differences in intestinal carbohydrate metabolism promote food intake and sperm maturation.Cell. 2019; 178: 901-918Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar). It would be interesting to determine the effects of diet, regeneration, age, reproductive status, and putative interorgan adhesion molecules on gut-testis co-localization, as well as to determine the effects of changes to this co-localization on gut-testis crosstalk. There is potential for additional interorgan proximal communication from other extended organs, including among other gut regions, Malpighian tubules, accessory glands, and the crop, and between the brain and a head-capsule-localized fat body, and between ovary and posterior midgut (Droujinine and Perrimon, 2016Droujinine I.A. Perrimon N. Interorgan communication pathways in physiology: focus on Drosophila.Annu. Rev. Genet. 2016; 50: 539-570Crossref PubMed Scopus (111) Google Scholar, Reiff et al., 2015Reiff T. Jacobson J. Cognigni P. Antonello Z. Ballesta E. Tan K.J. Yew J.Y. Dominguez M. Miguel-Aliaga I. Endocrine remodelling of the adult intestine sustains reproduction in Drosophila.Elife. 2015; 4: e06930Crossref PubMed Scopus (127) Google Scholar). In vertebrates, the blood or lymphatic vessel organization of one organ relative to another could also be significant in interorgan communication. Moreover, the observation that incorrect orientations of organs in human patients can impact health, including effects on metabolism, suggests that interorgan contacts could also be important for interorgan communication in humans (Jung et al., 2017Jung J.E. Hur J.H. Jung M.K. Kwon A. Chae H.W. Kim D.H. Kim H.-S. Diabetes mellitus due to agenesis of the dorsal pancreas in a patient with heterotaxy syndrome.Ann. Pediatr. Endocrinol. Metab. 2017; 22: 125-128Crossref PubMed Google Scholar). Could changes in spatial organization or proportions during obesity, anorexia, disease, injury, deformation, or mechanical forces result in defects in interorgan signaling? In addition, it would be interesting to determine the extent of changes to interorgan contacts that occur during development and aging, and the effects of these changes on interorgan communication (Hudry et al., 2019Hudry B. Goeij E.d. Mineo A. Gaspar P. Hadjieconomou D. Studd C. Mokochinski J.B. Kramer H.B. Plaçais P.-Y. Preat T. et al.Sex differences in intestinal carbohydrate metabolism promote food intake and sperm maturation.Cell. 2019; 178: 901-918Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar). We previously hypothesized that interorgan communication enabled and co-evolved with organ specialization (Droujinine and Perrimon, 2016Droujinine I.A. Perrimon N. Interorgan communication pathways in physiology: focus on Drosophila.Annu. Rev. Genet. 2016; 50: 539-570Crossref PubMed Scopus (111) Google Scholar). The work by Hudry et al., 2019Hudry B. Goeij E.d. Mineo A. Gaspar P. Hadjieconomou D. Studd C. Mokochinski J.B. Kramer H.B. Plaçais P.-Y. Preat T. et al.Sex differences in intestinal carbohydrate metabolism promote food intake and sperm maturation.Cell. 2019; 178: 901-918Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar suggests that spatial organization of organs may facilitate interorgan communication. Therefore, could interorgan communication influence the positioning of organs? Altogether, the work of Hudry et al., 2019Hudry B. Goeij E.d. Mineo A. Gaspar P. Hadjieconomou D. Studd C. Mokochinski J.B. Kramer H.B. Plaçais P.-Y. Preat T. et al.Sex differences in intestinal carbohydrate metabolism promote food intake and sperm maturation.Cell. 2019; 178: 901-918Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar will inspire future studies on interorgan regulation of sex-specific growth, physiology and metabolism, and organ spatiotemporal organization. Sex Differences in Intestinal Carbohydrate Metabolism Promote Food Intake and Sperm MaturationHudry et al.CellAugust 08, 2019In BriefInter-organ communication couples diet with gamete production. The male gonad promotes sex differences in carbohydrate metabolism within an adjacent intestinal portion via JAK-STAT signalling. In response to this gonadal signal, gut-derived citrate controls food intake and sperm maturation. 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• W2969885938 title "The Multidimensional Organization of Interorgan Communication Networks" @default.
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