{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,30]],"date-time":"2026-04-30T14:51:34Z","timestamp":1777560694692,"version":"3.51.4"},"reference-count":59,"publisher":"MDPI AG","issue":"16","license":[{"start":{"date-parts":[[2024,8,13]],"date-time":"2024-08-13T00:00:00Z","timestamp":1723507200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>In this study, we have investigated the immunolocalization of NGF (Nerve Growth Factor) and BDNF (Brain-Derived Neurotrophic Factor) in the pancreas of two species of marine mammals: Tursiops truncatus (common bottlenose dolphin), belonging to the order of the Artiodactyla, and Otaria flavescens (South American sea lion), belonging to the order of the Carnivora. Our results demonstrated a significant presence of NGF and BDNF in the pancreas of both species with a wide distribution pattern observed in the exocrine and endocrine components. We identified some differences that can be attributed to the different feeding habits of the two species, which possess a different morphological organization of the digestive system. Altogether, these preliminary observations open new perspectives on the function of neurotrophins and the adaptive mechanisms of marine mammals in the aquatic environment, suggesting potential parallels between the physiology of marine and terrestrial mammals.<\/jats:p>","DOI":"10.3390\/ani14162336","type":"journal-article","created":{"date-parts":[[2024,8,13]],"date-time":"2024-08-13T10:54:54Z","timestamp":1723546494000},"page":"2336","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Immunolocalization of Two Neurotrophins, NGF and BDNF, in the Pancreas of the South American Sea Lion Otaria flavescens and Bottlenose Dolphin Tursiops truncatus"],"prefix":"10.3390","volume":"14","author":[{"given":"Claudia","family":"Gatta","sequence":"first","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via F. Delpino 1, 80137 Naples, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Luigi","family":"Avallone","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via F. Delpino 1, 80137 Naples, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anna","family":"Costagliola","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via F. Delpino 1, 80137 Naples, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4506-967X","authenticated-orcid":false,"given":"Paola","family":"Scocco","sequence":"additional","affiliation":[{"name":"School of Biosciences and Veterinary Medicine, University of Camerino, Via Gentile III da Varano, 62032 Camerino, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5050-642X","authenticated-orcid":false,"given":"Livia","family":"D\u2019Angelo","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via F. Delpino 1, 80137 Naples, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Paolo","family":"de Girolamo","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via F. Delpino 1, 80137 Naples, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1012-902X","authenticated-orcid":false,"given":"Elena","family":"De Felice","sequence":"additional","affiliation":[{"name":"School of Biosciences and Veterinary Medicine, University of Camerino, Via Gentile III da Varano, 62032 Camerino, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2024,8,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"e13446","DOI":"10.1111\/nmo.13446","article-title":"Neurotrophic factors in enteric physiology and pathophysiology","volume":"30","author":"Liu","year":"2018","journal-title":"Neurogastroenterol. Motil."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1038\/372266a0","article-title":"Neurotrophin-6 is a new member of the nerve growth factor family","volume":"372","author":"Gotz","year":"1994","journal-title":"Nature"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1006\/mcne.1998.0666","article-title":"Cloning and expression of a novel neurotrophin, NT-7, from Carp","volume":"11","author":"Lai","year":"1998","journal-title":"Mol. Cell. Neurosci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1016\/S0014-5793(98)00192-6","article-title":"Neurotrophin-7: A novel member of the neurotrophin family from the zebrafish","volume":"424","author":"Nilsson","year":"1998","journal-title":"FEBS Lett."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1038\/350158a0","article-title":"Tyrosine phosphorylation and tyrosine kinase activity of the trk protooncogene product induced by NGF","volume":"350","author":"Kaplan","year":"1991","journal-title":"Nature"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1101\/SQB.1992.057.01.006","article-title":"The Trk family of tyrosine kinases: Receptors for NGF-related neurotrophins","volume":"57","author":"Parada","year":"1992","journal-title":"Cold Spring Harb. Symp. Quant. Biol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1002\/ar.1081","article-title":"TrkA and TrkB neurotrophin receptor immunoreactivity in the teleost (Scorpaena porcus) endocrine pancreas","volume":"263","author":"Lucini","year":"2001","journal-title":"Anat. Rec."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1154","DOI":"10.1126\/science.3306916","article-title":"The nerve growth factor 35 years later","volume":"237","year":"1987","journal-title":"Science"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/0968-0004(93)90052-O","article-title":"Nerve growth factor revisited","volume":"18","author":"Bradshaw","year":"1993","journal-title":"Trends Biochem. Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"10059","DOI":"10.1073\/pnas.86.24.10059","article-title":"Nerve growth factor induces growth and differentiation of human B lymphocytes","volume":"86","author":"Otten","year":"1989","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1697","DOI":"10.1210\/endo.135.4.7925134","article-title":"Nerve growth factor in the anterior pituitary: Regulation of secretion","volume":"135","author":"Patterson","year":"1994","journal-title":"Endocrinology"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1210\/endo.136.2.7835308","article-title":"In vivo presence of the high-affinity NGF receptor Trk-A in the rat pancreas: Differential localization during pancreatic development","volume":"136","author":"Tazi","year":"1995","journal-title":"Endocrinology"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1677\/joe.0.1560431","article-title":"Expression of nerve growth factor and its high-affinity receptor Trk-A in the rat pancreas during embryonic and fetal life","volume":"156","author":"Miralles","year":"1998","journal-title":"J. Endocrinol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1281","DOI":"10.1007\/s001250100650","article-title":"NGF-withdrawal induces apoptosis in pancreatic beta cells in vitro","volume":"44","author":"Pierucci","year":"2001","journal-title":"Diabetologia"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"7882","DOI":"10.1074\/jbc.270.14.7882","article-title":"Glucose, other secretagogues, and nerve growth factor stimulate mitogen-activated protein kinase in the insulin-secreting beta-cell line INS-1","volume":"270","author":"Sekine","year":"1995","journal-title":"J. Biol. Chem."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1755","DOI":"10.2337\/diabetes.50.8.1755","article-title":"Nerve growth factor increases insulin secretion and barium current in pancreatic beta-cells","volume":"50","author":"Rosenbaum","year":"2001","journal-title":"Diabetes"},{"key":"ref_17","first-page":"408","article-title":"Nerve growth factor promotes development of glucose induced insulin secretion in rat neonate pancreatic beta cells by modulating calcium channels","volume":"1","author":"Fiordelisio","year":"2008","journal-title":"Channels"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1950","DOI":"10.1038\/s41467-020-15833-5","article-title":"Novel metabolic role for BDNF in pancreatic \u03b2-cell insulin secretion","volume":"11","author":"Fulgenzi","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1046\/j.1463-1326.2003.00238.x","article-title":"Brain-derived neurotrophic factor modulates glucagon secretion from pancreatic alpha cells: Its contribution to glucose metabolism","volume":"5","author":"Hanyu","year":"2003","journal-title":"Diabetes Obes. Metab."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.tins.2012.12.009","article-title":"BDNF and the central control of feeding: Accidental bystander or essential player?","volume":"36","author":"Rios","year":"2013","journal-title":"Trends Neurosci."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Moosaie, F., Mohammadi, S., Saghazade, A., Firouzabadi, F.D., and Rezaei, N. (2023). Brain-derived neutrophic factor in diabetes mellitus: A systematic review and meta-analysis. PLoS ONE, 18.","DOI":"10.1371\/journal.pone.0268816"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1153","DOI":"10.1113\/expphysiol.2009.048561","article-title":"Role of exercise-induced brain-derived neurotrophic factor production in the regulation of energy homeostasis in mammals","volume":"94","author":"Pedersen","year":"2009","journal-title":"Exp. Physiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"436","DOI":"10.2337\/diabetes.49.3.436","article-title":"Brain-derived neurotrophic factor regulates glucose metabolism by modulating energy balance in diabetic mice","volume":"49","author":"Nakagawa","year":"2000","journal-title":"Diabetes"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"14265","DOI":"10.1523\/JNEUROSCI.3308-07.2007","article-title":"Selective deletion of Bdnf in the ventromedial and dorsomedial hypothalamus of adult mice results in hyperphagic behavior and obesity","volume":"27","author":"Unger","year":"2007","journal-title":"J. Neurosci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1183","DOI":"10.1016\/S0002-9440(10)65221-2","article-title":"Abundant production of brain-derived neurotrophic factor by adult visceral epithelia. implications for paracrine and target-derived Neurotrophic functions","volume":"155","author":"Lommatzsch","year":"1999","journal-title":"Am. J. Pathol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1002\/(SICI)1097-0215(19990505)81:3<417::AID-IJC16>3.0.CO;2-6","article-title":"Neurotrophins and Trk receptors in human pancreatic ductal adenocarcinoma: Expression patterns and effects on in vitro invasive behavior","volume":"81","author":"Miknyoczki","year":"1999","journal-title":"Int. J. Cancer"},{"key":"ref_27","first-page":"105","article-title":"Neurotrophins and neurotrophin receptors mRNAs expression in pancreatic islets and insulinoma cell lines","volume":"2","author":"Bonini","year":"2001","journal-title":"JOP"},{"key":"ref_28","first-page":"477","article-title":"Expression of Trk tyrosine kinase receptor is a biologic marker for cell proliferation and perineural invasion of human pancreatic ductal adenocarcinoma","volume":"8","author":"Sakamoto","year":"2001","journal-title":"Oncol. Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1633","DOI":"10.1023\/A:1010684916863","article-title":"Brain-derived neurotrophic factor (BDNF) is upregulated and associated with pain in chronic pancreatitis","volume":"46","author":"Zhu","year":"2001","journal-title":"Dig. Dis. Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1007\/s00429-002-0304-3","article-title":"Brain-derived neurotrophic factor in higher vertebrate pancreas: Immunolocalization in glucagon cell","volume":"206","author":"Lucini","year":"2003","journal-title":"Anat. Embryol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Davis, R.W. (2019). Marine Mammals. Adaptations for an Aquatic Life, Springer Nature. [1st ed.].","DOI":"10.1007\/978-3-319-98280-9"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1002\/ar.20541","article-title":"Anatomical adaptations of aquatic mammals","volume":"290","author":"Reidenberg","year":"2007","journal-title":"Anat. Rec."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.yexcr.2017.03.050","article-title":"The pancreas: Bandmaster of glucose homeostasis","volume":"360","author":"Jouvet","year":"2017","journal-title":"Exp. Cell Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.mce.2015.06.028","article-title":"The role of pancreatic polypeptide in the regulation of energy homeostasis","volume":"418","author":"Khandekar","year":"2015","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_35","first-page":"390","article-title":"Big brains and blood glucose: Common ground for diabetes mellitus in humans and healthy dolphins","volume":"57","author":"Ridgway","year":"2007","journal-title":"Comp. Med."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"167","DOI":"10.3354\/dao02187","article-title":"Clinical relevance of urate nephrolithiasis in bottlenose dolphins Tursiops truncatus","volume":"89","author":"Smith","year":"2010","journal-title":"Dis. Aquat. Organ."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Venn-Watson, S., Smith, C.R., Stevenson, S., Parry, C., Daniels, R., Jensen, E., Cendejas, V., Balmer, B., Janech, M., and Neely, B.A. (2013). Blood-based indicators of insulin resistance and metabolic syndrome in bottlenose dolphins (Tursiops truncatus). Front. Endocrinol., 4.","DOI":"10.3389\/fendo.2013.00136"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Champagne, C.D., Crocker, D.E., Fowler, M.A., and Houser, D.S. (2012). Fasting physiology of the pinnipeds: The challenges of fasting while maintaining high energy expenditure and nutrient delivery for lactation. Comparative Physiology of Fasting, Starvation, and Food Limitation, Springer. Chapter 19.","DOI":"10.1007\/978-3-642-29056-5_19"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1482","DOI":"10.1002\/ar.22532","article-title":"Expression and immunohistochemical detection of leptin-like peptide in the gastrointestinal tract of the South American sea lion (Otaria flavescens) and the bottlenose dolphin (Tursiops truncatus)","volume":"295","author":"Russo","year":"2012","journal-title":"Anat. Rec."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Gatta, C., Russo, F., Russolillo, M.G., Varricchio, E., Paolucci, M., Castaldo, L., Lucini, C., de Girolamo, P., Cozzi, B., and Maruccio, L. (2014). The orexin system in the enteric nervous system of the bottlenose dolphin (Tursiops truncatus). PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0105009"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Gatta, C., De Felice, E., D\u2019Angelo, L., Maruccio, L., Leggieri, A., Lucini, C., Palladino, A., Paolucci, M., Scocco, P., and Varricchio, E. (2018). The case study of nesfatin-1 in the pancreas of Tursiops truncatus. Front. Physiol., 9.","DOI":"10.3389\/fphys.2018.01845"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"De Felice, E., Gatta, C., Giaquinto, D., Fioretto, F., Maruccio, L., d\u2019Angelo, D., Scocco, P., de Girolamo, P., and D\u2019Angelo, L. (2022). Immunolocalization of Nesfatin-1 in the gastrointestinal tract of the common bottlenose dolphin Tursiops truncatus. Animals, 12.","DOI":"10.3390\/ani12162148"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1002\/jmor.20530","article-title":"Neurotrohpins and their Trk-receptors in the cerebellum of zebrafish","volume":"277","author":"Gatta","year":"2016","journal-title":"J. Morphol."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Gatta, C., Schiano, V., Attanasio, C., Lucini, C., and Palladino, A. (2022). Neurotrophins in zebrafish taste buds. Animals, 12.","DOI":"10.3390\/ani12131613"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1007\/978-1-61779-310-3_2","article-title":"Neuropeptide localization in nonmammalian vertebrates","volume":"789","author":"Lucini","year":"2011","journal-title":"Methods Mol. Biol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1016\/0168-9525(93)90122-X","article-title":"Molecular evolution of the dog family","volume":"9","author":"Wayne","year":"1993","journal-title":"Trends Genet."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"590","DOI":"10.1055\/s-2007-1009296","article-title":"Porcine islet isolation, cellular composition and secretory response","volume":"21","author":"Crowther","year":"1989","journal-title":"Horm. Metab. Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1034\/j.1399-3089.1999.00009.x","article-title":"The distribution of porcine pancreatic beta-cells at ages 5, 12, and 24 weeks","volume":"6","author":"Jay","year":"1999","journal-title":"Xenotransplantation"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1002\/ar.20536","article-title":"Stomach anatomy and use in defining systemic relationships of the Cetacean family Ziphiidae (beaked whales)","volume":"290","author":"Mead","year":"2007","journal-title":"Anat. Rec."},{"key":"ref_50","unstructured":"Perrin, W., Wursing, B., and Thewissen, J. (2008). Gastrointestinal tract. Encyclopedia of Marine Mammals, Academic Press. [2nd ed.]."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Bombardi, C., Rambaldi, A.M., Galiazzo, G., Giancola, F., Gra\u00efc, J.M., Salamanca, G., Cozzi, B., and Chiocchetti, R. (2021). Nitrergic and substance p immunoreactive neurons in the enteric nervous system of the bottlenose dolphin (Tursiops truncatus) intestine. Animals, 11.","DOI":"10.3390\/ani11041057"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.ygcen.2015.02.023","article-title":"Histomorphology of the bottlenose dolphin (Tursiops truncatus) pancreas and association of increasing islet \u03b2-cell size with chronic hypercholesterolemia","volume":"214","author":"Colegrove","year":"2015","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"654","DOI":"10.1002\/dmrr.2339","article-title":"The relation among NGF, EGF and insulin is important for triggering pancreatic \u03b2 cell apoptosis","volume":"28","author":"Karatug","year":"2012","journal-title":"Diabetes Metab. Res. Rev."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1016\/j.devcel.2016.10.003","article-title":"Neurotrophin signaling is required for glucose-induced insulin. secretion","volume":"39","author":"Houtz","year":"2016","journal-title":"Dev. Cell"},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Burganova, G., Bridges, C., Thorn, P., and Landsman, L. (2021). The role of vascular cells in pancreatic beta-cell function. Front. Endocrinol., 12.","DOI":"10.3389\/fendo.2021.667170"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1080\/08977190310001629566","article-title":"Expression of nerve growth factor in human pancreatic beta cells","volume":"21","author":"Vidaltamayo","year":"2003","journal-title":"Growth Factors"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1002\/dmrr.290","article-title":"Brain-derived neurotrophic factor (BDNF) regulates glucose and energy metabolism in diabetic mice","volume":"18","author":"Nakagawa","year":"2002","journal-title":"Diabetes Metab. Res. Rev."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"655","DOI":"10.1038\/nn0703-655","article-title":"The skinny on neurotrophins","volume":"6","author":"Wisse","year":"2003","journal-title":"Nat. Neurosci."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"455","DOI":"10.3389\/fphys.2019.00455","article-title":"BDNF actions in the cardiovascular system: Roles in development, adulthood and response to injury","volume":"10","author":"Kermani","year":"2019","journal-title":"Front. Physiol."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/14\/16\/2336\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T15:36:02Z","timestamp":1760110562000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/14\/16\/2336"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,8,13]]},"references-count":59,"journal-issue":{"issue":"16","published-online":{"date-parts":[[2024,8]]}},"alternative-id":["ani14162336"],"URL":"https:\/\/doi.org\/10.3390\/ani14162336","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,8,13]]}}}