{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,30]],"date-time":"2026-04-30T15:56:15Z","timestamp":1777564575420,"version":"3.51.4"},"reference-count":51,"publisher":"The Company of Biologists","issue":"4","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2007,2,15]]},"abstract":"<jats:title>SUMMARY<\/jats:title>\n               <jats:p>Over a quarter of a century ago, Mykles described the presence of putative endocrine cells in the midgut epithelium of the crab Cancer magister(Mykles, 1979). In the years that have followed, these cells have been largely ignored and nothing is known about their hormone content or the functions they play in this species. Here,we used a combination of immunohistochemistry and mass spectrometric techniques to investigate these questions. Using immunohistochemistry, we identified both SIFamide- and tachykinin-related peptide (TRP)-like immunopositive cells in the midgut epithelium of C. magister, as well as in that of Cancer borealis and Cancer productus. In each species, the SIFamide-like labeling was restricted to the anterior portion of the midgut, including the paired anterior midgut caeca, whereas the TRP-like immunoreactivity predominated in the posterior midgut and the posterior midgut caecum. Regardless of location, label or species, the morphology of the immunopositive cells matched that of the putative endocrine cells characterized ultrastructurally by Mykles(Mykles, 1979). Matrix-assisted laser desorption\/ionization-Fourier transform mass spectrometry identified the peptides responsible for the immunoreactivities as GYRKPPFNGSIFamide (Gly1-SIFamide) and APSGFLGMRamide [Cancer borealis tachykinin-related peptide Ia (CabTRP Ia)], respectively, both of which are known neuropeptides of Cancer species. Although the function of these midgut-derived peptides remains unknown, we found that both Gly1-SIFamide and CabTRP Ia were released when the midgut was exposed to high-potassium saline. In addition, CabTRP Ia was detectable in the hemolymph of crabs that had been held without food for several days, but not in that of fed animals, paralleling results that were attributed to TRP release from midgut endocrine cells in insects. Thus, one function that midgut-derived CabTRP Ia may play in Cancer species is paracrine\/hormonal control of feeding-related behavior, as has been postulated for TRPs released from homologous cells in insects.<\/jats:p>","DOI":"10.1242\/jeb.02696","type":"journal-article","created":{"date-parts":[[2007,2,3]],"date-time":"2007-02-03T01:08:25Z","timestamp":1170464905000},"page":"699-714","source":"Crossref","is-referenced-by-count":56,"title":["Midgut epithelial endocrine cells are a rich source of the neuropeptides APSGFLGMRamide (<i>Cancer borealis<\/i> tachykinin-related peptide Ia) and GYRKPPFNGSIFamide (Gly1-SIFamide) in the crabs <i>Cancer borealis<\/i>, <i>Cancer magister<\/i> and <i>Cancer productus<\/i>"],"prefix":"10.1242","volume":"210","author":[{"given":"Andrew E.","family":"Christie","sequence":"first","affiliation":[{"name":"Department of Biology, University of Washington, Box 351800, Seattle, WA 98195-1800, USA"},{"name":"Mount Desert Island Biological Laboratory, PO Box 35, Old Bar Harbor Road,Salisbury Cove, ME 04672, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kimberly K.","family":"Kutz-Naber","sequence":"additional","affiliation":[{"name":"Department of Chemistry, University of Wisconsin-Madison, 1101 University Avenue, Madison, WI 53706-1369, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elizabeth A.","family":"Stemmler","sequence":"additional","affiliation":[{"name":"Department of Chemistry, Bowdoin College, 6600 College Station, Brunswick,ME 04011, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alexandra","family":"Klein","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Washington, Box 351800, Seattle, WA 98195-1800, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Daniel I.","family":"Messinger","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Washington, Box 351800, Seattle, WA 98195-1800, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christopher C.","family":"Goiney","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Washington, Box 351800, Seattle, WA 98195-1800, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anna J.","family":"Conterato","sequence":"additional","affiliation":[{"name":"Department of Chemistry, Bowdoin College, 6600 College Station, Brunswick,ME 04011, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Emily A.","family":"Bruns","sequence":"additional","affiliation":[{"name":"Department of Chemistry, Bowdoin College, 6600 College Station, Brunswick,ME 04011, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yun-Wei A.","family":"Hsu","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Washington, Box 351800, Seattle, WA 98195-1800, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lingjun","family":"Li","sequence":"additional","affiliation":[{"name":"Department of Chemistry, University of Wisconsin-Madison, 1101 University Avenue, Madison, WI 53706-1369, USA"},{"name":"School of Pharmacy, University of Wisconsin-Madison, 777 Highland Avenue,Madison, WI 53705-2222, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Patsy S.","family":"Dickinson","sequence":"additional","affiliation":[{"name":"Department of Biology, Bowdoin College, 6500 College Station, Brunswick,ME 04011, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"237","reference":[{"key":"2021042511103281100_REF1","doi-asserted-by":"crossref","unstructured":"Brown, M. R., Raikhel, A. S. and Lea, A. O.(1985). Ultrastructure of midgut endocrine cells in the adult mosquito, Aedes aegypti.Tissue Cell17,709-721.","DOI":"10.1016\/0040-8166(85)90006-0"},{"key":"2021042511103281100_REF2","doi-asserted-by":"crossref","unstructured":"Christie, A. E., Skiebe, P. and Marder, E.(1995). Matrix of neuromodulators in the neurosecretory structures of the crab Cancer borealis.J. Exp. Biol.198,2431-2439.","DOI":"10.1242\/jeb.198.12.2431"},{"key":"2021042511103281100_REF3","doi-asserted-by":"crossref","unstructured":"Christie, A. E., Lundquist, C. T., Na\u0308ssel, D. R. and Nusbaum, M. P. (1997). Two novel tachykinin-related peptides from the nervous system of the crab Cancer borealis.J. Exp. Biol.200,2279-2294.","DOI":"10.1242\/jeb.200.17.2279"},{"key":"2021042511103281100_REF4","unstructured":"Christie, A. E., Kutz, K. K., Messinger, D. I., Hsu, Y. A.,Savage, E. E., Dickinson, P. S. and Li, L. (2005).Midgut endocrine cells are a rich source of neuropeptides in the crab Cancer productus. Program No. 30.7. 2005 Abstract Viewer\/Itinerary Planner. Washington, DC: Society for Neuroscience, 2005. Online."},{"key":"2021042511103281100_REF5","doi-asserted-by":"crossref","unstructured":"Christie, A. E., Stemmler, E. A., Peguero, B., Messinger, D. I.,Provencher, H. L., Scheerlinck, P., Hsu, Y. W., Guiney, M. E., de la Iglesia,H. O. and Dickinson, P. S. (2006). Identification,physiological actions, and distribution of VYRKPPFNGSIFamide(Val1-SIFamide) in the stomatogastric nervous system of the American lobster Homarus americanus.J. Comp. Neurol. 496,406-421.","DOI":"10.1002\/cne.20932"},{"key":"2021042511103281100_REF6","doi-asserted-by":"crossref","unstructured":"Chung, J. S., Dircksen, H. and Webster, S. G.(1999). A remarkable, precisely timed release of hyperglycemic hormone from endocrine cells in the gut is associated with ecdysis in the crab Carcinus maenas.Proc. Natl. Acad. Sci. USA96,13103-13107.","DOI":"10.1073\/pnas.96.23.13103"},{"key":"2021042511103281100_REF7","doi-asserted-by":"crossref","unstructured":"Cuello, A. C., Galfre, G. and Milstein, C.(1979). Detection of substance P in the central nervous system by a monoclonal antibody. Proc. Natl. Acad. Sci. USA76,3532-3536.","DOI":"10.1073\/pnas.76.7.3532"},{"key":"2021042511103281100_REF8","doi-asserted-by":"crossref","unstructured":"Dall, W. and Moriarty, D. J. W. (1983). Functional aspects of nutrition and digestion. In The Biology of Crustacea, Vol. 5, Internal Anatomy and Physiological Regulation(ed. L. H. Mantel), pp. 215-261. New York: Academic Press.","DOI":"10.1016\/B978-0-12-106405-1.50015-1"},{"key":"2021042511103281100_REF9","doi-asserted-by":"crossref","unstructured":"Davey, M., Duve, H., Thorpe, A. and East, P.(1999). Characterisation of the helicostatin peptide precursor gene from Helicoverpa armigera (Lepidoptera: Noctuidae). Insect Biochem. Mol. 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Gut endocrine cells in insects: the ultrastructure of the gut endocrine cells of the lepidopterous insects. Biomed. Res. 2, 270-280.","DOI":"10.2220\/biomedres.2.270"},{"key":"2021042511103281100_REF13","doi-asserted-by":"crossref","unstructured":"Endo, Y. and Nishiitsutsuji-Uwo, J. (1982). Exocytotic release of secretory granules from endocrine cells in the midgut of insects. Cell Tissue Res. 222,515-522.","DOI":"10.1007\/BF00213851"},{"key":"2021042511103281100_REF14","doi-asserted-by":"crossref","unstructured":"Fu, Q., Kutz, K. K., Schmidt, J. J., Hsu, Y. W., Messinger, D. I., Cain, S. D., de la Iglesia, H. O., Christie, A. E. and Li, L.(2005). Hormone complement of the Cancer productus sinus gland and pericardial organ: an anatomical and mass spectrometric investigation. J. Comp. Neurol. 493,607-626.","DOI":"10.1002\/cne.20773"},{"key":"2021042511103281100_REF15","doi-asserted-by":"crossref","unstructured":"Fujita, T., Kanno, T. and Kobayashi, S. (1988). The Paraneuron. Berlin, Heidelberg, New York:Springer.","DOI":"10.1007\/978-4-431-68066-6"},{"key":"2021042511103281100_REF16","doi-asserted-by":"crossref","unstructured":"Hecker, H. (1977). Structure and function of midgut epithelial cells in culicidae mosquitoes (insecta, diptera). Cell Tissue Res. 184,321-341.","DOI":"10.1007\/BF00219894"},{"key":"2021042511103281100_REF17","doi-asserted-by":"crossref","unstructured":"Huybrechts, J., Nusbaum, M. P., Bosch, L. V., Baggerman, G., De Loof, A. and Schoofs, L. (2003). Neuropeptidomic analysis of the brain and thoracic ganglion from the Jonah crab, Cancer borealis.Biochem. Biophys. Res. Commun. 308,535-544.","DOI":"10.1016\/S0006-291X(03)01426-8"},{"key":"2021042511103281100_REF18","unstructured":"Icely, J. D. and Nott, J. A. (1992). Digestion and absorption: digestive system and associated organs. In Microscopic Anatomy of Invertebrates, Vol. 10, Decapod Crustacea (ed. F. W. Harrison and A. G. Humes), pp.147-201. New York: Wiley-Liss."},{"key":"2021042511103281100_REF19","doi-asserted-by":"crossref","unstructured":"Janssen, I., Schoofs, L., Spittaels, K., Neven, H., Vanden Broeck, J.,\n          Devreese, B., Van Beeumen, J., Shabanowitz, J., Hunt, D. F. and De Loof, A. (1996). Isolation of NEB-LFamide, a novel myotropic neuropeptide from the grey fleshfly. Mol. Cell. Endocrinol. 117,157-165.","DOI":"10.1016\/0303-7207(95)03746-2"},{"key":"2021042511103281100_REF20","doi-asserted-by":"crossref","unstructured":"Jorge-Rivera, J. C. and Marder, E. (1996). TNRNFLRFamide and SDRNFLRFamide modulate muscles of the stomatogastric system of the crab Cancer borealis.J. Comp. Physiol. A179,741-751.","DOI":"10.1007\/BF00207353"},{"key":"2021042511103281100_REF21","doi-asserted-by":"crossref","unstructured":"Kegel, G., Reichwein, B., Weese, S., Gaus, G., Peter-Katalinic,J. and Keller, R. (1989). Amino acid sequence of the crustacean hyperglycemic hormone (CHH) from the shore crab, Carcinus maenas.FEBS Lett. 255,10-14.","DOI":"10.1016\/0014-5793(89)81051-8"},{"key":"2021042511103281100_REF22","doi-asserted-by":"crossref","unstructured":"Kutz, K. K., Schmidt, J. J. and Li, L. (2004). In situ tissue analysis of neuropeptides by MALDI FTMS in-cell accumulation. Anal. Chem.76,5630-5640.","DOI":"10.1021\/ac049255b"},{"key":"2021042511103281100_REF23","doi-asserted-by":"crossref","unstructured":"Lee, K. Y., Horodyski, F. M. and Chamberlin, M. E.(1998). Inhibition of midgut ion transport by allatotropin(Mas-AT) and Manduca FLRFamides in the tobacco hornworm Manduca sexta.J. Exp. Biol.201,3067-3074.","DOI":"10.1242\/jeb.201.22.3067"},{"key":"2021042511103281100_REF24","doi-asserted-by":"crossref","unstructured":"Leite, A. C. and Evangelista, L. G. (2001). Ultrastructure of endocrine cells from the abdominal midgut epithelium of Lutzomyia longipalpis (Diptera: Psychodidae). J. Med. Entomol. 38,749-752.","DOI":"10.1603\/0022-2585-38.5.749"},{"key":"2021042511103281100_REF25","doi-asserted-by":"crossref","unstructured":"Li, L., Kelley, W. P., Billimoria, C. P., Christie, A. E.,Pulver, S., Sweedler, J. V. and Marder, E. (2003). Mass spectrometric investigation of the neuropeptide complement and release in the pericardial organs of the crab, Cancer borealis.J. Neurochem.87,642-656.","DOI":"10.1046\/j.1471-4159.2003.02031.x"},{"key":"2021042511103281100_REF26","doi-asserted-by":"crossref","unstructured":"Messinger, D. I., Kutz, K. K., Le, T., Verley, D. R., Hsu, Y. A., Ngo, C. T., Cain, S. D., Birmingham, J. T., Li, L. and Christie, A. E.(2005). Identification and characterization of a tachykinin-containing neuroendocrine organ in the commissural ganglion of the crab Cancer productus.J. Exp. Biol.208,3303-3319.","DOI":"10.1242\/jeb.01787"},{"key":"2021042511103281100_REF27","unstructured":"Mykles, D. L. (1979). Ultrastructure of alimentary epithelia of lobsters, Homarus americanus and H. gammarus, and crab, Cancer magister.Zoomorphologie92,201-215."},{"key":"2021042511103281100_REF28","doi-asserted-by":"crossref","unstructured":"Na\u0308ssel, D. R. (1999). Tachykinin-related peptides in invertebrates: a review. Peptides20,141-158.","DOI":"10.1016\/S0196-9781(98)00142-9"},{"key":"2021042511103281100_REF29","doi-asserted-by":"crossref","unstructured":"Neves, C. A., Gitirana, L. B. and Serrao, J. E.(2003). Ultrastructure of the midgut endocrine cells in Melipona quadrifasciata anthidioides (Hymenoptera, Apidae). Braz. J. Biol. 63,683-690.","DOI":"10.1590\/S1519-69842003000400015"},{"key":"2021042511103281100_REF30","doi-asserted-by":"crossref","unstructured":"Pabla, N. and Lange, A. B. (1999). The distribution and myotropic activity of locustatachykinin-like peptides in locust midgut. Peptides20,1159-1167.","DOI":"10.1016\/S0196-9781(99)00119-9"},{"key":"2021042511103281100_REF31","doi-asserted-by":"crossref","unstructured":"Reichwald, K., Unnithan, G. C., Davis, N. T., Agricola, H. and Feyereisen, R. (1994). Expression of the allatostatin gene in endocrine cells of the cockroach midgut. Proc. Natl. Acad. Sci. USA91,11894-11898.","DOI":"10.1073\/pnas.91.25.11894"},{"key":"2021042511103281100_REF32","unstructured":"Reinhardt, C. A. (1976). Ultrastructural comparison of the midgut epithelia of fleas with different feeding behavior patterns (Xenopsylla cheopis, Echidnophaga gallinacea, Tunga penetrans, Siphonaptera, Pulicidae). Acta Trop. 33,105-132."},{"key":"2021042511103281100_REF33","doi-asserted-by":"crossref","unstructured":"Sehnal, F. and Zitnan, D. (1996). Midgut endocrine cells. In Biology of the Insect Midgut (ed. M. J. Lehane and P. F. Billingsley), pp. 55-85. London: Chapman & Hall.","DOI":"10.1007\/978-94-009-1519-0_3"},{"key":"2021042511103281100_REF34","doi-asserted-by":"crossref","unstructured":"Sliwowska, J., Rosinsk, G. and Na\u0308ssel, D. R.(2001). Cardioacceleratory action of tachykinin-related neuropeptides and proctolin in two coleopteran insect species. Peptides22,209-217.","DOI":"10.1016\/S0196-9781(00)00384-3"},{"key":"2021042511103281100_REF35","doi-asserted-by":"crossref","unstructured":"Sithigorngul, P., Pupuem, J., Krungkasem, C., Longyant, S.,Chaivisuthangkura, P., Sithigorngul, W. and Petsom, A.(2002). Seven novel FMRFamide-like neuropeptide sequences from the eyestalk of the giant tiger prawn Penaeus monodon.Comp. Biochem. Physiol.131B,325-337.","DOI":"10.1016\/S1096-4959(01)00499-7"},{"key":"2021042511103281100_REF36","doi-asserted-by":"crossref","unstructured":"Stemmler, E. A., Provencher, H. L., Guiney, M. E., Gardner, N. P. and Dickinson, P. S. (2005). Matrix assisted laser desorption\/ionization-Fourier transform mass spectrometry for the identification of orcokinin neuropeptides in crustaceans using metastable decay and sustained off-resonance irradiation. Anal. Chem.77,3594-3606.","DOI":"10.1021\/ac0502347"},{"key":"2021042511103281100_REF37","doi-asserted-by":"crossref","unstructured":"Swensen, A. M. and Marder, E. (2000). Multiple peptides converge to activate the same voltage-dependent current in a central pattern-generating circuit. J. Neurosci. 20,6752-6759.","DOI":"10.1523\/JNEUROSCI.20-18-06752.2000"},{"key":"2021042511103281100_REF38","doi-asserted-by":"crossref","unstructured":"Swensen, A. M. and Marder, E. (2001). Modulators with convergent cellular actions elicit distinct circuit outputs. J. Neurosci. 21,4050-4058.","DOI":"10.1523\/JNEUROSCI.21-11-04050.2001"},{"key":"2021042511103281100_REF39","doi-asserted-by":"crossref","unstructured":"Tensen, C. P., Verhoeven, A. H., Gaus, G., Janssen, K. P.,Keller, R. and\n          Van Herp, F. (1991). Isolation and amino acid sequence of crustacean hyperglycemic hormone precursor-related peptides. Peptides12,673-681.","DOI":"10.1016\/0196-9781(91)90119-A"},{"key":"2021042511103281100_REF40","doi-asserted-by":"crossref","unstructured":"Thirumalai, V. and Marder, E. (2002). Colocalized neuropeptides activate a central pattern generator by acting on different circuit targets. J. Neurosci. 22,1874-1882.","DOI":"10.1523\/JNEUROSCI.22-05-01874.2002"},{"key":"2021042511103281100_REF41","doi-asserted-by":"crossref","unstructured":"Vanden Broeck, J. (2001). Neuropeptides and their precursors in the fruitfly, Drosophila melanogaster.Peptides22,241-254.","DOI":"10.1016\/S0196-9781(00)00376-4"},{"key":"2021042511103281100_REF42","doi-asserted-by":"crossref","unstructured":"Veenstra, J. A., Lau, G. W., Agricola, H. J. and Petzel, D. H. (1995). Immunohistological localization of regulatory peptides in the midgut of the female mosquito Aedes aegypti.Histochem. Cell Biol.104,337-347.","DOI":"10.1007\/BF01458127"},{"key":"2021042511103281100_REF43","doi-asserted-by":"crossref","unstructured":"Verleyen, P., Huybrechts, J., Baggerman, G., Van Lommel, A., De Loof, A. and Schoofs, L. (2004). SIFamide is a highly conserved neuropeptide: a comparative study in different insect species. Biochem. Biophys. Res. Commun. 320,334-341.","DOI":"10.1016\/j.bbrc.2004.05.173"},{"key":"2021042511103281100_REF44","doi-asserted-by":"crossref","unstructured":"Vonk, H. J. (1960). Digestion and metabolism. In The Physiology of Crustacea, Vol. 1, Metabolism and Growth (ed. T. H. Waterman), pp.291-316. New York: Academic Press.","DOI":"10.1016\/B978-0-12-395628-6.50014-2"},{"key":"2021042511103281100_REF45","doi-asserted-by":"crossref","unstructured":"Webster, S. G., Dircksen, H. and Chung, J. S.(2000). Endocrine cells in the gut of the shore crab Carcinus maenas immunoreactive to crustacean hyperglycaemic hormone and its precursor-related peptide. Cell Tissue Res. 300,193-205.","DOI":"10.1007\/s004410050060"},{"key":"2021042511103281100_REF46","doi-asserted-by":"crossref","unstructured":"Weidemann, W., Gromoll, J. and Keller, R.(1989). Cloning and sequence analysis of cDNA for precursor of a crustacean hyperglycemic hormone. FEBS Lett. 257, 31-34.","DOI":"10.1016\/0014-5793(89)81778-8"},{"key":"2021042511103281100_REF47","doi-asserted-by":"crossref","unstructured":"Winther, A. M. and Na\u0308ssel, D. R. (2001). Intestinal peptides as circulating hormones: release of tachykinin-related peptide from the locust and cockroach midgut. J. Exp. Biol.204,1269-1280.","DOI":"10.1242\/jeb.204.7.1269"},{"key":"2021042511103281100_REF48","doi-asserted-by":"crossref","unstructured":"Winther, A. M., Muren, J. E., Ahlborg, N. and Na\u0308ssel, D. R. (1999). Differential distribution of isoforms of Leucophaea tachykinin-related peptides (LemTRPs) in endocrine cells and neuronal processes of the cockroach midgut. J. Comp. Neurol. 406,15-28.","DOI":"10.1002\/(SICI)1096-9861(19990329)406:1<15::AID-CNE2>3.0.CO;2-G"},{"key":"2021042511103281100_REF49","doi-asserted-by":"crossref","unstructured":"Wood, D. E., Stein, W. and Nusbaum, M. P.(2000). Projection neurons with shared cotransmitters elicit different motor patterns from the same neural circuit. J. Neurosci. 20,8943-8953.","DOI":"10.1523\/JNEUROSCI.20-23-08943.2000"},{"key":"2021042511103281100_REF50","doi-asserted-by":"crossref","unstructured":"Yasuda, A., Yasuda-Kamatani, Y., Nozaki, M. and Nakajima, T.(2004). Identification of GYRKPPFNGSIFamide (crustacean-SIFamide)in the crayfish Procambarus clarkii by topological mass spectrometry analysis. Gen. Comp. Endocrinol. 135,391-400.","DOI":"10.1016\/j.ygcen.2003.10.001"},{"key":"2021042511103281100_REF51","doi-asserted-by":"crossref","unstructured":"Zudaire, E., Simpson, S. J. and Montuenga, L. M.(1998). Effects of food nutrient content, insect age and stage in the feeding cycle on the FMRFamide immunoreactivity of diffuse endocrine cells in the locust gut. J. Exp. Biol.201,2971-2979.","DOI":"10.1242\/jeb.201.21.2971"}],"container-title":["Journal of Experimental Biology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/journals.biologists.com\/jeb\/article-pdf\/210\/4\/699\/1262021\/699.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/jeb\/article-pdf\/210\/4\/699\/1262021\/699.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,4,25]],"date-time":"2021-04-25T12:45:05Z","timestamp":1619354705000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/jeb\/article\/210\/4\/699\/17239\/Midgut-epithelial-endocrine-cells-are-a-rich"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2007,2,15]]},"references-count":51,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2007,2,15]]}},"URL":"https:\/\/doi.org\/10.1242\/jeb.02696","relation":{},"ISSN":["1477-9145","0022-0949"],"issn-type":[{"value":"1477-9145","type":"electronic"},{"value":"0022-0949","type":"print"}],"subject":[],"published":{"date-parts":[[2007,2,15]]}}}