Sympathetic Innervation during Development Is Necessary for Pancreatic Islet Architecture and Functional Maturation

Borden, Philip, Houtz, Jessica, Leach, Steven D., Kuruvilla, Rejji·2013·Cell Reports
DOI 10.1016/j.celrep.2013.06.019

Cited by (192)

Items 101–192 of 192

  1. Innervation in organogenesis
    Samuel E. Honeycutt, Pierre-Emmanuel N'Guetta, Lori L. O’Brien · 2022 · Current topics in developmental biology/Current Topics in Developmental Biology
  2. Dissecting Human Gene Functions Regulating Islet Development With Targeted Gene Transduction
    Philip T. Pauerstein, 拓也 杉山, Susan E. Stanley, Graeme W. McLean, Jing Wang, Martı́n G. Martı́n, Seung K. Kim · 2015 · Diabetes
  3. MafB-dependent neurotransmitter signaling promotes β cell migration in the developing pancreas
    Sara Bsharat, Emanuela Monni, Tania Singh, Jenny Kristina Johansson, Kavya Achanta, Ludivine Bertonnier‐Brouty, Anja Schmidt-Christensen, Dan Holmberg, Zaal Kokaia, Rashmi B. Prasad et al. · 2023 · Development
  4. Schwann Cells in Digestive System Disorders
    K. Goluba, Liga Kunrade, U. Riekstiņa, V. Parfejevs · 2022 · Cells
  5. Transcriptomic and Quantitative Proteomic Profiling Reveals Signaling Pathways Critical for Pancreatic Islet Maturation
    Yu‐Chin Lien, Kyoung‐Jae Won, Rebecca Anne Simmons · 2020 · Endocrinology
  6. Harnessing conserved signaling and metabolic pathways to enhance the maturation of functional engineered tissues
    Neal I. Callaghan, Lauren J. Durland, Ronald G. Ireland, J. Paul Santerre, Craig A. Simmons, Locke Davenport Huyer · 2022 · npj Regenerative Medicine
  7. Intercellular Communication in the Islet of Langerhans in Health and Disease
    Xue-Wen Ng, Hee-Chung Yong, D. W. Piston · 2021 · Comprehensive Physiology
  8. Pancreatic Islets of Langerhans: Adapting Cell and Molecular Biology to Changes of Metabolism
    Fernanda Ornellas, Iara Karise, Márcia Barbosa Águila, Carlos Alberto Mandarim‐de‐Lacerda · 2020 · Springer eBooks
  9. Neuropancreatology: The Nervous System and Pain Management in Pancreatic Diseases
    A. Nicoletti, Federica Vitale, M. Paratore, G. Quero, Marcantonio Negri, E. Nista, Sergio Alfieri, A. Gasbarrini, Lorenzo Zileri Dal Verme · 2024 · Life
  10. Daily injection of the β2 adrenergic agonist clenbuterol improved poor muscle growth and body composition in lambs following heat stress-induced intrauterine growth restriction
    Rachel L Gibbs, Rebecca M Swanson, Joslyn K Beard, Zena M Hicks, Micah S Most, Haley N Beer, Pablo Cesar C Grijalva, Shawna M. Clement, Eileen S. Marks-Nelson, Ty B Schmidt et al. · 2023 · Frontiers in Physiology
  11. The Price of Surviving on Adrenaline: Developmental Programming Responses to Chronic Fetal Hypercatecholaminemia Contribute to Poor Muscle Growth Capacity and Metabolic Dysfunction in IUGR-Born Offspring
    Rachel L Gibbs, Dustin T Yates · 2021 · Frontiers in Animal Science
  12. Phosphoproteome reveals molecular mechanisms of aberrant rhythm in neurotransmitter‐mediated islet hormone secretion in diabetic mice
    Yunqiang He, Qi Fu, Min Sun, Yu Qian, Yucheng Liang, Jie Zhang, R. Gao, Hemin Jiang, Hao Dai, Yuwei Liu et al. · 2022 · Clinical and Translational Medicine
  13. Pancreatic organogenesis mapped through space and time
    Marissa A. Scavuzzo, Wojciech J. Szlachcic, Matthew C. Hill, Natalia Ziojla, Jessica Teaw, Jeffrey C. Carlson, Jonathan Tiessen, Jolanta Chmielowiec, James F. Martin, Malgorzata Borowiak · 2025 · Experimental & Molecular Medicine
  14. Substance P preserves pancreatic β-cells in streptozotocin-induced type 1 diabetic mice
    Nunggum Jung, Jihyun Um, Do Yeon Kim, Maria Jose Dubon, Yeji Byeon, Dong-Jin Kim, Youngsook Son, Ki‐Sook Park · 2017 · Biochemical and Biophysical Research Communications
  15. Daily Injection of the β2 Adrenergic Agonist Clenbuterol Improved Muscle Glucose Metabolism, Glucose-Stimulated Insulin Secretion, and Hyperlipidemia in Juvenile Lambs Following Heat-Stress-Induced Intrauterine Growth Restriction
    Rachel L Gibbs, James A. Wilson, Rebecca M Swanson, Joslyn K Beard, Zena M Hicks, Haley N Beer, Eileen S. Marks-Nelson, Ty B Schmidt, Jessica L. Petersen, Dustin T Yates · 2024 · Metabolites
  16. Pancreatic islet adaptation in pregnancy and postpartum
    Nelmari Ruiz-Otero, Jeffery S. Tessem, Ronadip R. Banerjee · 2024 · Trends in Endocrinology and Metabolism
  17. Sympathetic nerve signals: orchestrators of mammary development and stem cell vitality
    Zi Ye, Yu Xu, Mengna Zhang, Cheguo Cai · 2024 · Journal of Molecular Cell Biology
  18. Deciphering the Molecular Mechanisms of Autonomic Nervous System Neuron Induction through Integrative Bioinformatics Analysis
    Yuzo Takayama, Yuka Akagi, Yasuyuki S. Kida · 2023 · International Journal of Molecular Sciences
  19. Reprogramming of human exocrine pancreas cells to beta cells.
    Willem Staels, Y. Heremans, H. Heimberg · 2015 · Best practice & research. Clinical endocrinology & metabolism
  20. Soy isoflavones recover pancreatic islet function and prevent metabolic dysfunction in male rats
    Tatiane Aparecida Ribeiro, Audrei Pavanello, Laize Peron Tófolo, Júlio Cézar de Oliveira, Ana Maria Praxedes de Moraes, Claudinéia Conationi da Silva Franco, Kelly Valério Prates, Isabela Peixoto Martins, Kesia Palma‐Rigo, Rosana Torrezan et al. · 2021 · Journal of Endocrinology
  21. Role of Delta/Notch-like EGF-related receptor in blood glucose homeostasis
    Nelmari Ruiz-Otero, Rejji Kuruvilla · 2023 · Frontiers in Endocrinology
  22. The nerve center of organ engineering
    Suradip Das, Wisberty J. Gordián-Vélez, Jay R. Dave, Zarina S. Ali, H. Ledebur, D. K. Cullen · 2025 · Nature Communications
  23. The connection between innervation and metabolic rearrangements in pancreatic cancer through serine
    Meng-Meng Dong, Lidong Cao, R. Cui, Ying-Jun Xie · 2022 · Frontiers in Oncology
  24. Mapping histologic and functional maturation of human endocrine pancreas across early postnatal periods
    Diane C. Saunders, Fan Feng, Alexander L. Hopkirk, Kristie I. Aamodt, Nathaniel J. Hart, Fong C. Pan, Conrad V. Reihsmann, N. Izmaylov, Shaojun Mei, Brandon A. Sherrod et al. · 2026 · Nature Communications
  25. Polytherapy with Reserpine and Glucagon-like Peptide-1 (GLP-1) Improves the Symptoms in Streptozotocin-Induced Type-1 Diabetic Mice by Reducing Inflammation and Inducting Beta Cell Regeneration
    Е. G. Skurikhin, О. V. Pershina, Natalia Nicolaevna Ermakova, Lubov Aexandrovna Ermolaeva, Vyacheslav Andreevich Krupin, Angelina Vladimirovna Pakhomova, Edgar Sergeevich Pan, Marie Zeuner, Darius Widera, E. S. Khmelevskaya et al. · 2018 · Journal of Stem Cell Research & Therapy
  26. Adapting Physiology in Functional Human Islet Organogenesis
    Eiji Yoshihara · 2022 · Frontiers in Cell and Developmental Biology
  27. Painting the Pancreas in Three Dimensions: Whole-Mount Immunofluorescence Method
    Maricela Maldonado, Jeffrey Serrill, Hung-Ping Shih · 2020 · Methods in molecular biology
  28. Bioink materials for translational applications
    Naresh Mahajan, James J. Yoo, Anthony Atala · 2022 · MRS Bulletin
  29. Type 2 Diabetes and Developmental Origin of Non-Alcohol Fatty Liver Disease and Future Directions of Treatment
    Hassan I. El‐Sayyad, El Shahary · 2016 · Clinical and Experimental Pharmacology
  30. L’îlot pancréatique : ce que nous savons 150 ans après Langerhans
    C. A. Mandarim-de-Lacerda · 2019 · Bulletin de l'Académie Nationale de Médecine
  31. Integrating Spatial and Single‐Nucleus Transcriptomic Data to Assess the Effects of Intrauterine Hyperglycemia on Fetal Pancreatic Development
    Yu Deng, Shuting Wan, Zan Yuan, Huixia Yang · 2025 · Advanced Science
  32. Recent Advancements in the Relationship Between the Autonomic Nervous System and the Pancreas, Encompassing the Regulation of Regeneration and Apoptosis
    T. Kiba · 2025 · Cells
  33. Crosstalk between brain and the peripheral tissues
    Kumar Sarvottam, Ratnesh Namdeo Gajbhiye, Ashish Arvind, Bhupendra Singh Yadav · 2024 · Elsevier eBooks
  34. Development of Human Pancreatic Innervation
    A. Proshchina, Yuliya S. Krivova, O. Leonova, V. Barabanov, S. Saveliev · 2018 · The Autonomic Nervous System
  35. Differential contributions of G protein‐ or arrestin subtype‐mediated signalling underlie urocortin 3‐induced somatostatin secretion in pancreatic δ cells
    Kaiyu Wang, Ming‐Xin Gao, Hai‐Bo Qi, Wentao An, Jing‐Yu Lin, Shanglei Ning, Fan Yang, Peng Xiao, Jie Cheng, Wei Pan et al. · 2024 · British Journal of Pharmacology
  36. High-resolution imaging atlas reveals the context-dependent role of pancreatic sympathetic innervation in diabetic mice
    Qingqing Xu, Yu-Xin Chen, Xin-Yan Ni, Han-Ying Zhuang, Shenxi Cao, Liwei Zhao, Leying Wang, Jian-Hui Chen, Wen Z. Yang, Wen-Wen Zeng et al. · 2024 · Acta Biochimica et Biophysica Sinica
  37. Synchronized β cell response to glucose is lost concomitant with loss of islet architecture in Robo deficient islets of Langerhans in vivo
    Melissa T Adams, Christopher A. Reissaus, JaeAnn M. Dwulet, Er-Li Jin, Joseph M. Szulczewski, Melissa R. Lyman, Sophia M. Sdao, Sutichot D Nimkulrat, S. Ponik, M. Merrins et al. · 2019 · bioRxiv
  38. The stem cell within the vessel wall: multipotent pericytes modulating β-cell function and diabetic complications
    Huanjing Bi, Ruiyang Ma, Zuhan Chen, Ying Wang, Xiaoming Ding · 2025 · Stem Cell Research & Therapy
  39. The innate thermogenic capacity of brown adipose tissue develops independently of sympathetic signaling
    Ethan C. Fein, Sarmistha Mukherjee, Joseph A. Baur, Patrick Seale · 2025 · Molecular Metabolism
  40. Pancreatic sympathetic innervation disturbance in type 1 diabetes.
    Sen-Lin Li, Huimin Yuan, Keshan Yang, Qing Li, M. Xiang · 2023 · Clinical Immunology
  41. Effect of isoproterenol, a β-adrenergic agonist, on the differentiation of insulin-producing pancreatic β cells derived from human pluripotent stem cells.
    Hye Ryeong Jun, Y. Kim, Ji Eun Moon, Sehui Jeong, Han-Se Goh, H. Hoang, Yu-Na Lee, Hyemin Jeong, I. Shim, Song Cheol Kim · 2024 · Experimental Cell Research
  42. Neural signaling contributes to heart formation and growth in the invertebrate chordate, Ciona robusta
    Hannah N. Gruner, Christopher J. Pickett, Jasmine Yimeng Bao, Richard Garcia, Akiko Hozumi, Tal D. Scully, Shaoyang Ning, Mavis Gao, Gia Bautista, Keren Maze et al. · 2026 · PLoS Biology
  43. Expression and functional studies of the GDNF family receptor alpha 3 in the pancreas
    Laure Nivlet, Joel Herrmann, Delia Esteban Martin, A. Meunier, Christophe Orvain, Gérard Gradwohl · 2015 · Journal of Molecular Endocrinology
  44. Neuro-Insular Complexes in the Human Pancreas
    Yuliya S. Krivova, A. Proshchina, V. Barabanov, S. Saveliev · 2017 · InTech eBooks
  45. Cambrian explosion
    Nelson R. Cabej · 2019 · Elsevier eBooks
  46. Neural Control of Postphylotypic Development
    Nelson R. Cabej · 2018 · Elsevier eBooks
  47. Neurotech Report
    James Cavuoto · 2013 · Neuromodulation Technology at the Neural Interface
  48. From architecture to function: mechanisms shaping pancreatic islet morphogenesis
    Mireia Molina Van den Bosch, Tobias Greisle, Christos Karampelias, Heiko Lickert · 2026 · Trends in Endocrinology and Metabolism
  49. VIP Pipes Up: Neuronal Signals Direct Tubulogenesis
    Jessica Houtz, Rejji Kuruvilla · 2014 · Developmental Cell
  50. Insights on β-cell regeneration from the zebrafish shoal: from generation of cells to functional integration
    Prateek Chawla, Luis Fernando Delgadillo-Silva, Nikolay Ninov · 2019 · Current Opinion in Physiology
  51. Deep into the niche: Deciphering local endoderm‐microenvironment interactions in development, homeostasis, and disease of pancreas and intestine
    Wojciech J. Szlachcic, Katherine C. Letai, Marissa A. Scavuzzo, Malgorzata Borowiak · 2023 · BioEssays
  52. Hormonal Imbalance as a Prognostic Factor of Physical Development of Children with Intellectual Disability
    Olga Valentinovna Smirnova, Elizaveta Sergeevna Ovcharenko, Э. В. Каспаров · 2024 · Children
  53. Tumor Tissue Is Innervated
    Boris Mravec · 2024 · Springer eBooks
  54. Mammary stem cells: from molecular cues to orchestrated regulatory mechanisms and its implications in breast cancer
    Mengna Zhang, Lingxian Zhang, Jie Liu, Jiahui Zhao, Jiayu Mei, Jiahua Zou, Yaogan Luo, Cheguo Cai · 2025 · Journal of genetics and genomics/Journal of Genetics and Genomics
  55. Scaffold-free endocrine tissue engineering: role of islet organization and implications in type 1 diabetes
    Tuğba Bal · 2025 · BMC Endocrine Disorders
  56. 5’tRNA-derived fragments modulate β-cell homeostasis and islet macrophage activation in type 2 diabetes
    Cosentino, Cristina, Klein, Rémy, Menoud, Véronique, Guay, Claudiane, Aiello, Elena, Auddino, Stefano, Di Giuseppe, Gianfranco, Ciccarelli, Gea, Galli, Alessandra, Alabiso, Francesco et al. · 2026 · Nature Communications
  57. Age-related changes in the sympathetic innervation of the pancreas
    Chumasov Ei, Elena S. Petrova, Dmitriy E. Korzhevsky · 2017 · Russian Journal of Developmental Biology
  58. High-Resolution Imaging Atlas Reveals Context-Dependent Role of Pancreatic Sympathetic Innervation in Diabetic Mice
    Qingqing Xu, Yunxin Chen, Xinyan Ni, Hanying Zhuang, Shenxi Cao, Liwei Zhao, Leying Wang, Wen Zheng Yang, Wenwen Zeng, Jianhui Chen et al. · 2024 · Qeios
  59. A neuroendocrine principle: Pancreatic islets actively shape sympathetic innervation
    Dongxue Li, Jiamei Luo, Junjie Wang, Yun-Zhen Qian, Dilinazi Abudujilile, Musitaba Mutailifu, Tian Yang, Yuan-Xin Hong, Wentao Shi, Xiaoyi Ma et al. · 2025 · bioRxiv (Cold Spring Harbor Laboratory)
  60. The role of sympathetic innervation in the development of postnatal cardiomyocytes
    Sagarika Utture · 2015 · Brandeis Institutional Repository
  61. Sympathetic nerve activity promotes cardiomyocyte cell-cycle arrest and binucleation
    Li Chen, Alexander Y. Payumo, Kentaro Hirose, Rachel B. Bigley, Jonathan Lovas, Rejji Kuruvilla, Guo N. Huang · 2017 · bioRxiv (Cold Spring Harbor Laboratory)
  62. In vivo Imaging β-cell Function Reveals Two Waves of β-cell Maturation
    Jia Zhao, Weijian Zong, Yi Wu, Jiayu Shen, Dongzhou Gou, Yiwen Zhao, Runlong Wu, Fuzeng Niu, Xu Wang, Xuan Zheng et al. · 2017 · bioRxiv (Cold Spring Harbor Laboratory)
  63. Structural Organization and Interaction of Intrapancreatic Ganglia with the Myenteric Nerve Plexus of the Duodenum at the Early Stages of Postnatal Ontogeny in Rats
    E. Chumasov, E. Petrova, D. E. Korzhevskii · 2017 · Neuroscience and Behavioral Physiology
  64. Decreased intracellular granule movement and glucagon secretion in pancreatic α cells attached to superior cervical ganglion neurites
    Kiyoto Watabe, Satoru Yokawa, Yoshikazu Inoh, Takahiro Suzuki, T. Furuno · 2018 · Molecular and Cellular Biochemistry
  65. FORMATION OF MULTI-CELLULAR SPHEROIDS IN DIFFERENT AGE PORCINE ADRENAL CELL CULTURE
    Y. M. Ushakova, О. С. Сидоренко, Г. А. Бабийчук, Т. П. Бондаренко, Г. А. Божок · 2018 · Bulletin of Problems Biology and Medicine
  66. Islet cell circuit
    Jing‐Yu Lin, Jie Cheng, Xiao Yu, Jin Wang · 2018 · Scientia Sinica Vitae
  67. The inductive brain in animal development
    Nelson R. Cabej · 2021 · Elsevier eBooks
  68. Epilogue
    Nelson R. Cabej · 2019 · Elsevier eBooks
  69. Faculty Opinions recommendation of Hyperactivation of sympathetic nerves drives depletion of melanocyte stem cells.
    Iwei Yeh · 2020 · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature
  70. Advances in islet organoids
    Tao Yu, XinYi CHEN, Cissy Qing YU, Arial Yi ZENG · 2022 · Scientia Sinica Vitae
  71. Sympathetic Reinnervation of Intact and Upper Follicle Xenografts into BALB/c-nu/nu Mice
    Xiu-Wen Chen, Na Ni, Xiaojun Xie, Yinglin Zhao, Wen-Zi Liang, Yuxin Huang, Changmin Lin · 2023 · Life
  72. Comparative study of endocrine pancreatic tissue in bats: Assessing variations among frugivorous, insectivorous, and nectarivorous diets
    M. Contini, Mateus Rodrigues Beguelini, Thalles Fernando Rocha Ruiz, Sebastião Roberto Taboga, Alex Rafacho · 2024 · Tissue and Cell
  73. Progenitor and bihormonal cells in neuroinsular complexes of the developing human pancreas
    Yuliya S. Krivova, A. E. Proshchina, Olga S. Godovalova, Sergey V. Saveliev · 2026 · Morphology
  74. A modular platform to generate functional sympathetic neuron-innervated heart assembloids
    Hsueh‐Fu Wu, Christina James, JESSICA N. MCALPINE, Kenyi Saito‐Diaz, Xin Sun, Ming Song, Tripti Saini, Courtney Grant, Kimata Safi Thomas, William H. Delaney et al. · 2026 · Research Square
  75. Role of the trigeminal system in pancreatic innervation: new concept and challenge – a narrative review
    Fady M. Bou Malhab, S. Jabbour, R. DeFronzo, Rita Nemr · 2026 · Endocrine Research
  76. Partial reduction of sympathetic noradrenaline synthesis enhanced insulin secretion and cell-cycle-associated activity of pancreatic β cells in mice
    Ryohei Ogawa, Minori Suzuki, Satoshi Hara, Daisuke Sakano, Shoen Kume, Hiroshi Ichinose · 2026 · American Journal of Physiology-Cell Physiology
  77. Perinatal liver sympathetic innervation governs body size
    Verónica Bobo-Jiménez, Silvia Gomila, Rebeca Lapresa, Jesús Agulla, Julie Angibaud, Irene Sánchez‐Morán, María Delgado‐Esteban, Águeda González‐Rodríguez, Alberto Fernández‐Jaén, Pedro Ramos‐Cabrer et al. · 2026 · Communications Biology
  78. Lysosomal degradation of insulin granules promotes β-cell failure in type 2 diabetes
    Adrien Pasquier · 2016
  79. How are pancreatic tumors innervated?
    Thi Trang Huyen Nguyen · 2017
  80. Analyse 3D des remodelages des réseaux neuronaux dans le cancer du pancréas
    Adrien Lucchesi · 2018
  81. A Novel Mouse Model of Sympathoadrenal Catecholamine Deficiency by Ablation of the Tyrosine Hydroxylase Gene With Slc6a4‐Cre
    Ryohei Ogawa, Ryo Fukumoto, Satoshi Hara, Nobuhiro Hayashi, Hiroshi Ichinose · 2026 · Journal of Neurochemistry
  82. Rôle du systèrme nerveux sympathique dans le développement des tumeurs pancréatiques
    Jérémy Guillot · 2019
  83. The role of noradrenergic innervation and β-cell dedifferentiation in diabetes
    ADRIANA AVOLIO, Cassandra Morciano, Shawn Gugliandolo, Amelia Splendore, Umberto Capece, Teresa Mezza, Gianfranco Di Giuseppe, Gea Ciccarelli, Laura Soldovieri, Michela Brunetti et al. · 2026 · Trends in Endocrinology and Metabolism
  84. Satellite Glial Cells Drive Homeostatic Synaptic Structural Plasticity in Sympathetic Neurons
    Joshua Harrison, Ellie Greene, Aaron Yang, Jumana Akoad, Laurie Chen, Rui Gong, Xianghan Liu, Susan J. Birren · 2026 · bioRxiv (Cold Spring Harbor Laboratory)
  85. Stromal and Neuronal Sources of Slit2/3 Ligands in the Adult Pancreas Exhibit Distinct Expression Patterns Independent of Robo2 Receptor Expression in the Islet
    Matthew R. Wagner, Nicolas G Pintozzi, Bjorn M. Schoff, Marissa I. Gold, Rachel H. Kasper, Nina G. Steele, Barak Blum · 2026 · bioRxiv (Cold Spring Harbor Laboratory)
  86. Nongenetic Mechanisms of Animal Evolution
    Nelson R. Cabej · 2026 · Springer eBooks
  87. Unravelling the developmental origins of cystic fibrosis-related diabetes
    Alex Cho, M. Cristina Nostro · 2026 · Diabetologia
  88. Primary cilia as platforms for islet neurotransmitter signaling
    Shannon E. Townsend, Jing W. Hughes · 2026 · Endocrinology
  89. Islet ultrastructure: past achievements and future directions
    Andreas Müller, Solange Aurrecoechea Duran, Patrícia I. Santos, Aubrey V. Weigel, Isabel Espinosa-Medina, Michele Solimena · 2026 · Diabetologia
  90. MAFB in Pancreatic β-Cell Development and Dysfunction: Implications for Diabetes and Translational Applications
    Razik Mu-u-min, Abdoulaye Diané, Heba Al-Siddiqi · 2026 · Biomolecules
  91. The bile acid-sensive ion channel (BASIC) is expressed in pancreatic α-cells and involved in glucagon secretion
    J. Yang, Stefan Gründer, Dominik Wiemuth · 2026 · Pflügers Archiv - European Journal of Physiology
  92. Effects of Celiac and Hepatic Sympathetic Denervation on Glucose Homeostasis: A Scoping Review
    Tushar Garg, Melissa S. Putman, Yi‐Fen Yen, Thomas J. An, Leo L. Tsai · 2026 · Journal of Vascular and Interventional Radiology